Acta Ecologica Sinica 34 (2014) 85–91

Contents lists available at ScienceDirect

Acta Ecologica Sinica

journal homepage: www.elsevier.com/locate/chnaes

Relationships between functional diversity and ecosystem functioning: A review

Yantao Song a,c, Ping Wang b, Guangdi Li a,c, Daowei Zhou a,⇑
a
Northeast Institute of Geography and Agroecology, Chinese Academy of Sciences, Changchun 130102, China
b
School of Environment, Northeast Normal University, Changchun 130117, China
c
Graham Centre for Agricultural Innovation (alliance between Industry & Investment NSW and Charles Sturt University), Wagga Wagga Agricultural Institute,
PMB, Wagga Wagga, NSW 2650, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Functional diversity, which is the value, variation and distribution of traits in a community assembly, is
Received 9 November 2011 an important component of biodiversity. Functional diversity is generally viewed as a key to understand
Revised 18 July 2012 ecosystem and community functioning. There are three components of functional diversity, i.e. functional
Accepted 8 June 2013
richness, evenness and divergence. Functional diversity and species diversity can be either positively or
negatively correlated, or uncorrelated, depending on the environmental conditions and disturbance
intensity. Ecosystem functioning includes ecosystem processes, ecosystem properties and ecosystem sta-
Keywords:
bility. The diversity hypothesis and the mass ratio hypothesis are the two major hypotheses of explaining
Traits
Species richness
the effect of functional diversity on ecosystem functioning, diversity hypothesis reflects that organisms
Functional diversity and their functional traits in a assemblage effect on ecosystem functioning by the complementarity of
Ecosystem functioning using resources, and mass ratio hypothesis emphasises the identify of the dominant species in a assem-
Biodiversity blage. These two hypotheses do not contradict each other and instead they reflect the two different sides
of functional diversity and functional composition. The effect of functional diversity on ecosystem func-
tioning also depends on abiotic factors, perturbation, management actions, etc. Function diversity poten-
tially influences ecosystem service and management by effecting on ecosystem functioning. Ecosystem
management groups should include functional diversity in their scheme and not just species richness.
Ó 2014 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85
2. Functional diversity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
2.1. Concept of functional diversity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
2.2. Relationship between functional diversity and species richness . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86
3. Ecosystem functioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
3.1. Concept of ecosystem functioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87
3.2. Relationship between ecosystem functioning and ecosystem services . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
4. Relationship between functional diversity and ecosystem functioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88
5. Conclusions and prospects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 90

1. Introduction [1]. As a result, biodiversity is lost at an unprecedented speed on

a global scale [2]. The loss of biodiversity potentially threatens
Human activities have extensively altered the global environ- ecosystem processes and ecosystem services [3]. Therefore, the
ment, biogeochemistry cycles, land coverage and biota changes relationship between biodiversity and ecosystem functioning has
been one of the core ecological topics [4,5], although it still remains
highly in dispute [6]. Biodiversity is usually measured by species
⇑ Corresponding author. richness [4,7,8]. Adler et al. [9] found that there was no clear
E-mail address: zhoudaowei@neigae.ac.cn (D. Zhou). relationship between species richness and productivity within

1872-2032/$ - see front matter Ó 2014 Ecological Society of China. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.chnaes.2014.01.001
86 Y. Song et al. / Acta Ecologica Sinica 34 (2014) 85–91
sites, regions, or across the global by conducting standardized sam-
pling in 48 herbaceous dominated plant communities on 5
continents.
In the last decade, phrases that contain ‘functional diversity’
increased exponentially in literature [8,10]. More and more
researchers show that functional diversity plays an important
role in ecosystem functioning [11–13]. Furthermore, Journal of
Applied Ecology by the British Ecological Society had published a
special issue about applying functional diversity in 2011, inspiring
people to consider the role of functional diversity on ecosystem
management [14]. In order to better understand and cognize
the effect of functional diversity on ecosystem functioning, we
review functional diversity, relationship between functional diver-
sity and species richness, and relationship between functional
diversity and ecosystem functioning, to promote further develop-
ment of the functional plant ecology.
2. Functional diversity
2.1. Concept of functional diversity
Functional diversity is an important component of biodiversity
[11,15], but there is no standard definition of functional diversity
at present. Functional diversity was defined as ‘‘the distribution
and range of functional traits of the organisms present in a com-
munity or ecosystem’’ [3], ‘‘functional diversification within the
community’’ [16], ‘‘the components of biodiversity impact on
ecosystem working or functioning’’ [17], ‘‘the value, range and
relative abundance of traits of organism in a community’’ [2], or
‘‘the variation or distribution of traits in an assemblage [14]’’. In
general, the definitions of functional diversity could be summa-
rized into two categories: the first one is to treat the organism
as a unit, and it emphasizes on the quantity and properties of
the organism, such as the diversity of functional groups; and
the other is to regard the trait as a unit, and it emphasizes the
range and distribution of traits, such as functional traits diversity.
In fact, the functional traits diversity is paid more and more
attention [5,10].
The concept of functional diversity is relatively easy to under-
stand, however, researchers have attempted to calculate the func-
tional diversity in different ways [10]. A common method of
calculating functional diversity is expressed by functional group
richness [4]. However, functional group richness is overestimated
the functional redundancy when there are few variations within
functional groups [18]. Walker et al. expanded the concept of func-
tional diversity, and they firstly used species traits for calculation
of the functional diversity in an assemblage [19]. The simplest
functional diversity index is the sum of the Euclidean distance be-
tween any two species within the assemblage [19]. However, this
index depends strongly on species richness [20]. To overcome this
drawback, Schmera et al. suggested that functional diversity
should be calculated by the distance matrix divided by the number
of functional units [21]. With the increased knowledge of func-
tional diversity, the indices include species abundance weight
(such as the community weighted mean CWM) [12], functional
divergence [23], functional regularity [20], multiple traits [24],
intraspecific variation [10], and many more indices [25] were
developed over time. In addition, Petchey and Gaston proposed
the functional dendrogram based on multi-trait distance to calcu-
late functional diversity [11,15,26]. Cornwell created an index
which did not depend on the distance matrix, but calculated by
the volume of convex hull of the trait space [27].
Similar to the composition of species diversity, functional diver-
sity consists of functional richness, evenness and divergence.
Functional richness measures the present species occupying the
amount of niche space within an assemblage, functional evenness
measures the distribution of species traits occupying the trait
space, and functional divergence measures the maximum degree
of divergence of abundance distribution of functional trait in trait
space within an assemblage [10,28,29]. Laliberté and Legendre
suggested that functional dispersion should be the fourth compo-
nent of functional diversity [25]. Scheuter et al. summarized and
compared the functional diversity indices and developed new
functional diversity indices (Table 1). They also gave the sugges-
tions on application of the functional diversity indices [10]. Song
et al. [30] and others have introduced the method of calculation
of these indices, the selection of functional traits, and weight of
traits [30–32].
With the development of functional diversity index, some
authors developed various programs to calculate the functional
diversity index, such as R program (http://www.ecolag.univ-
montp2.fr/software) [10,25], ‘‘EstimateS’’ (http://purl.oclc.org/esti-
mates), ‘‘EcoSim’’ (http://garyentsminger.com/ecosim/index.htm),
‘‘PHYLOCOM’’ (http://phylodiversity.net/phylocom/) [38], and so
on. However, those programs just calculated or analysed one single
functional diversity index, and different programs required differ-
ent data format, which were inconvenient to users [39]. To address
the above problems, Casanoves et al. developed a free software,
‘‘FDiversity’’, available at http://www.fdiversity.nucleodiver-
sus.org, which has a user-friendly interface, and it can calculate
and/or analyse most of the functional diversity indices. In addition,
the software supports multiple data formats of .xls, .txt, .db, .r,
etc., and it can run on the operating systems of Windows, MacOS,
Linux, etc. [39,40].
2.2. Relationship between functional diversity and species richness
The relationship between functional richness and species rich-
ness puts forward challenges to compare their relative roles on
ecosystem functioning [8,41]. Functional diversity is often posi-
tively correlated with species richness, and in this case the func-
tional richness could be replaced by species richness [4,17]. In
natural communities, species richness can be higher or lower than
functional diversity because of niche overlap between species and
intraspecific variation [3]. One explanation of the significantly po-
sitive relationship between functional diversity and species rich-
ness is the ‘‘selection effects’’ [7]. It assumes that the value or
range of traits increase with the regional species pool increasing
randomly [4]. However, this positive correlation has rarely been
tested in natural ecosystem [3,7,42]. In natural communities, func-
tional redundancy, local species pool, environmental filter, etc.
could affect the relationship between diversity and ecosystem
functioning [8]. Mayfield et al. illustrated that functional diversity
and species richness had 8 possible directions with land use
changes [7]. It may be more complex in natural ecosystems. For
example, results along the 24 small streams of boreal forests in On-
tario, Canada showed that the relationships between functional
diversity and species diversity under different disturbance intensi-
ties were from positive correlation to the unrelated [42]. Further-
more, the slopes of the relationship were significantly different
under different disturbance intensities [42]. Flynn et al. found that
both the plant functional diversity and species richness did not
change significantly with different intensity of land use [43], while
the relationship between functional diversity and species richness
changed significantly between the forested and deforested habitats
[44]. The relationship between functional diversity and species
richness is also affected by the number of functional traits and
their properties [15,44], the meaning of the special functional traits
[45,46], the calculation methods of functional diversity index, etc.
[8,45,47].
 Y. Song et al. / Acta Ecologica Sinica 34 (2014) 85–91 87

Table 1
Function name, formula, and references for the different functional diversity indices [10].

Function name Formula Note Source

Function richness (FR)
FRR Functional range maxðX ts ÞminðX ts Þ
s2Sc s2Sc
s, c, and t, species, community, and trait subscripts, respectively; [28]
maxðX ts Þmin ðX ts Þ Xts, mean value of trait t in species s; Sc, set of species present in
s2[Sc s2[Sc

community c
R
FRI Functional richness max½lst ðxÞdx Ltc, number of levels of categorical trait t covered by community [10]
R s2Sc
,
(one-dimensional) max½lst ðxÞdx c; Lt, total number of levels of trait t; other abbreviations as
s2[Sc
listed above
Where lst (x) is 1, if x is between min and max, else it is 0 for
categorical variables, Ltc/Lt
FRv Functional volume The volume inside the minimum convex hull that encloses [27]
all species in functional space
FRD Functional Distance matrices: Euclidean, Gower; Clustering methods: UPGMA, unweighted pair group method using arithmetic [15,33]
dendrogram single linkage, complete linkage, UPGMA, WPGMA, UPGMC, averages; WPGMA, weighted pair group method using
WPGMC, Ward’s method arithmetic averages; UPGMC, unweighted pair group centroid
method; WPGMC, weighted pair group centroid method
R
FRI Functional richness maxðfs ðZÞÞdZ, Xs, mean value of all traits in species s arranged in a vector; Z, [10]
s2Sc
(multidimensional) P sample vector of all traits, used for the purpose of computing
Where fs ðZÞ ¼ exp½0:5ðZ  X s ÞT 1  X si Þ P
s ðZ integrals over trait space; T, number of traits studied; ,
variance/covariance matrix of traits; i, individual; other
abbreviations as listed above
Function evenness (FE)
 
FE Functional PjSc j1 |Sc|, number of species present in community c; As, abundance of [20]
s¼1 min PjSc jX
j1
tsþ1 X ts j=ðAtsþ1 þAts Þ
; 1 , Where species
evenness (one- jX ts0 1 X ts0 j=ðAts0 þ1 þAts0 Þ jSc j1 species s; Ats, abundance of species s when species are sorted
s0 ¼1
dimensional) subscripts, s, are ranked by ascending order of trait value, t; following trait t ascending ranking; A, total abundance of all
Pt h i
individuals; Al, abundance of trait level l; l, level of trait (for
for categorical variables: Ll¼1 min AAl ; Llt
categorical variables); other abbreviations as listed above
 
FE Functional P E, set of edges connecting species pairs in the minimum [29]
min P
distðeÞ=ðAe =AÞ
;jS 1j1 jS 1j1
evenness e2E 0
e0 2E
c c
distðe Þ=ðAe0 =AÞ spanning tree; e, subscript of an edge; dist(e), distance between
(multidimensional) 1jS 1j1 endpoint species of edge e; Ae, sum of the abundances of the
c

endpoint species of edge e; other abbreviations as listed above

Function divergence (FD)
h  P P i
FDvar Functional 2 1 T As 2 Abbreviations as listed above [23]
p arctan 5 T t¼1 s2Sc A ðln X ts  ln X ts Þ ,
logarithmic
variance Where ln X ts is the mean of ln Xts over all species present
FDr Functional P As 2 Abbreviations as listed above [34]
s2Sc A ðX ts  X ts Þ
variance (FDvar
modified)
FDcat Functional PLt Al 2 Abbreviations as listed above [35]
FDcat ¼ 1  l¼1 A
unalikeability
FD Functional Q 1 ðY t ÞQ 3 ðY t Þ
, Where Yt is a dummy variable that takes Q1, lower quartile; Q3, upper quartile; other abbreviations as [10]
maxðX ts ÞminðX ts Þ
divergence (one- s2Sc s2Sc listed above
dimensional) values Xts with frequency As
FDQ Rao’s quadratic P P As As0 0 dist(s, s0 ), distance between species pairs based on mean trait [36,37]
s2Sc s0 2Sc 2 distðs; s Þ
A
entropy values (for continuous variables, Euclidean distance is used; for
discrete variables, the Gower distance is used); other
abbreviations as listed above
FD Functional P Vc, set of vertex species from the convex hull in community c [29]
DdþdG
Where Dd ¼ s2Sc AAs ðdGs  dGÞ,
,
DjdjþdG
divergence P (|Vc|, the corresponding number of vertices); dGs is the distance
(multidimensional) Djdj ¼ s2Sc ðAs =AÞjdGs  dGj, between species s and the gravity center of the convex hull
P
(coordinates Gt ð1=jVjÞ s2V X ts ) and dG is the mean value of dGs
over all present species; other abbreviations as listed above

3. Ecosystem functioning of ecosystem [58]. Ecosystem functioning have many properties

and scales, but there is no standard definition. Researchers need
3.1. Concept of ecosystem functioning specific analysis according to their research questions.
Study of relationship between diversity and ecosystem func-
Ecosystem functioning was expressed simply by plant produc- tioning usually analysed the relationship between diversity and
tivity or biomass [4,48–51]. The productivity represented the most one single functioning [12]. Even though some experiments
basic features of the ecosystem and it was relatively easy to mea- referred to a number of functioning, but the functioning were
sure. Some ecologists have also used light interception, soil mois- analysed separately [12,53,54]. However, ecosystem maintains
ture, soil carbon and nitrogen content, nitrogen mineralization multiple functioning, such as grazing grassland had the basic func-
and litter decomposition to quantify ecosystem functioning tioning including forage production, nutrient cycling and litter
[12,52–54]. Costanza et al. showed that the ecosystem functioning decomposition, and it also has the functioning of resisting invasive
related to the habitats of the ecosystem, biological or ecosystem species and environmental stress and so on. Most ecosystems have
properties and processes [55]. It contained the material cycle, en- multiple functioning simultaneously, named ‘‘ecosystem multi-
ergy flow and information transfer functioning [6]. Pacala and Kin- functionality’’ [59]. Studies have shown that maintaining ecosys-
zig divided ecosystem functioning into three categories, namely, tem multifunctionality required a higher biodiversity in artificial
stocks of energy and materials, fluxes of energy or material grassland [60,61].
processing and stability of rates or stocks over time [56]. Stability There are various methods to calculate the ecosystem multi-
included aspects of resilience and resistance [57]. Giller et al. functionality. For example, Hector and Bagchi calculated a number
illustrated that ecosystem functioning should include the values of ecosystem functioning when they examined the relationship
88 Y. Song et al. / Acta Ecologica Sinica 34 (2014) 85–91
Ecosystem Human Ecosystem
Functions welfare Services
1 Provisioning
1 Material cycling
2 Regulating
2 Energy flow
3 Cultural
3 Information flow
4 Supporting
Fig. 1. Relationships between ecosystem functioning and ecosystem services [68].
Ecosystem functioning and services do not necessarily show a one to one
correspondence. In some cases a single ecosystem function contributes to two or
more ecosystem services whereas in other cases a single ecosystem service is the
product of two or more ecosystem functions [55].
between species richness and ecosystem functioning for the
ecosystem multifunctionality [60]. Mouillot et al. analysed the
relationship between functional diversity and ecosystem function-
ing with average of four normalized ecosystem functioning [62]. In
fact, the ecosystem functioning are dynamic, which means that
ecosystem multifunctionality may not be a single sum of the func-
tioning. Therefore, we suggest that normalized and/or weighted
different functioning should be more reliable.
3.2. Relationship between ecosystem functioning and ecosystem
services
Ecosystem functioning provides human with products and ser-
vices [55]. Some ecologists believe that ecosystem functioning is
approximately equivalent to the ecosystem services [57,63] or eco-
system functioning contains ecosystem services [64]. However,
Feng et al. stressed that there were two different concepts and eco-
system functioning was mainly natural properties of ecosystem,
while the ecosystem services showed the human usage of ecosys-
tem functioning from human requirements, exploitation and pref-
erences [65]. Nevertheless, ecosystem functioning and ecosystem
services were closely linked (Fig. 1). Costanza et al. grouped
ecosystem services into 17 categories, which are corresponding
to different ecosystem functioning. They emphasised that
ecosystem services and ecosystem function were not one to one
correspondence, ecosystem services were directly or indirectly
from ecosystem functioning, and different ecosystem functioning
were interdependent [55]. Recent studies have shown that the
functional diversity cognize the ability of changes in ecosystem
services in the context of global environmental change [22,66].
4. Relationship between functional diversity and ecosystem
functioning
The original motivation for the study of relationship between
diversity and ecosystem functioning was due to the increased rate
of biodiversity loss in the past few decades [67]. In order to detect
the effect of species loss on ecosystem functioning, researchers
compared the ecosystem functioning by controlling the number
of species within communities in the controlled environments
[4,68]. The development of the functional diversity made the rela-
tionship between biodiversity and ecosystem functioning under-
gone a landmark change since the 1990s [4]. Furthermore, the
research on the relationship between biodiversity and ecosystem
functioning showed that functional diversity could better explain
the variation of ecosystem functioning than that of species diver-
sity [3,69].
One of the earliest experiments by Tilman et al. revealed that
functional abundance and composition could better explain
ecosystem functioning than that of species richness in different
number of functional groups of grassland communities [4]. Cadotte
et al. claimed that functional diversity could better explain ecosys-
tem functioning than that of richness, because functional diversity
includes a range of redundancy [8]. For example, if an ecosystem
had a higher functional diversity than other ecosystems, the eco-
system should have higher functioning, even functional diversity
was closely related with species richness. If the variation of func-
tional diversity was small (e.g. high redundancy), the relationship
between biodiversity and ecosystem functioning was weak. How-
ever, if there was variation in functional diversity, it would still
be able to explain the variation of ecosystem functioning, even
there was no variation in richness [8]. Petchey et al. showed that
functional diversity, calculated by multi-traits, could better explain
the variation of ecosystem functioning than that of functional
group richness or species richness based on results of six experi-
ments that studied the relationship between biodiversity and eco-
system functioning [70].
There are two main mechanisms that can explain the relation-
ship between functional diversity and ecosystem functioning. The
first mechanism is ‘‘diversity hypothesis’’. Tilman found that
organisms and their functional traits in the community had effect
on ecosystem functioning by complementarity of using resources
[71], namely a high diversity community had less niche overlap
on resource utilization than that of a low diversity community,
then the proportion of the entire available resources would in-
crease at the high diversity community. Therefore ecosystem func-
tioning would increase [3,4]. Griffin et al. stated that high primary
productivity community could be explained by the community
with high yield species, but for the overyielding plots, functional
diversity provided a better explanation [49]. Overyielding in-
creased as functional diversity increase, especially when the
assemblage productivity is much higher than a single species,
and functional trait diversity with resource utilization could better
predict the community productivity [8]. The other mechanism is
‘‘mass ratio hypothesis’’. Grime found that the contribution of spe-
cies to ecosystem functioning is proportional to the relative input
to primary production [72]. In other words, ecosystem functioning
is mainly dominated by the dominant species traits, and low abun-
dance species is relatively insensitive [12,52]. It is consistent with
the selection effect. The special traits of some species make them
utilize a greater proportion of resources than other species in a
community, thus these species contribute disproportionately to
ecosystem functioning [8]. Therefore, measuring functional traits
could indicate the contribution of species with similar trait to eco-
system functioning [8].
The ‘‘diversity hypothesis’’ reflects the trait difference between
species which could maximize resource utilization strategies, and
it is usually calculated by Rao’s quadratic entropy (Table 1, FDQ)
[36], while ‘‘mass ratio hypothesis’’ describes the weight of commu-
nity traits and it is calculated by community weighted mean (CWM)
[12]. These two mechanisms are not contradictory, they are two
forms of functional diversity, the former is diversity and the latter
is composition of an assemblage [73]. These two mechanisms show
that both functional diversity and dominant species identity have
significant impact on ecosystem functioning. However, they are
not exactly the same role on a specific ecosystem function. Mokany
et al. found that CWM had more influence on the ecosystem
processes than the other diversity indices through comparing the
functional diversity indices in a temperature native grassland in
north of Canberra, Australia, and it is recommended to focus on
management of the dominant species for maintenance of ecosystem
 Y. Song et al. / Acta Ecologica Sinica 34 (2014) 85–91 89

functioning [54]. Schumacher and Roscher illustrated that these two
hypotheses could be not isolated consideration, and they found that
the model could predict a greater degree of aboveground biomass
variation at a semi-natural grassland in Europe when the model
included these two hypotheses [74]. Similarly, Mouillot et al. also
showed that management for maintaining the ecosystem multifunc-
tionality should simultaneously take into account the composition
and functional diversity of the community [62].
The relationship between functional diversity and ecosystem
functioning is also affected by abiotic and biological factors.
Schumacher and Roscher showed that the model including abiotic
factors (particularly soil nitrogen content) and functional diversity
index could better predict the aboveground biomass than the mod-
el just containing a single diversity index at a semi-natural grass-
land in Europe [74]. Interestingly, a study by Laughlin on the
ponderosa pine forest ecosystem showed that there was significant
positive relationship between functional diversity (Rao’s quadratic
entropy index) and ecosystem functioning (nitrification) when he
just analysed the two factors. However, there was no significant
relationship between Rao’s quadratic entropy index and nitrifica-
tion when he settled a structural equation model including abiotic
factors, Rao’s quadratic entropy index and community weighted
mean index [52].
The role of functional diversity on ecosystem functioning is also
dependent on nutritional status and disturbed frequency. For
example, Bernhardt-Römermann et al. examined the effect of func-
tional diversity and species richness on grassland biomass after
fertilization and mowing, they found that functional diversity
could well explain the variation of biomass at fertilization and fre-
quent mowing plots, but species richness could best explain the
variation of biomass at infrequent mowing plots [13]. They also
showed that precipitation played a major role in the high frequent
mowing plots, while temperature contributed most to the less dis-
turbance and no fertilization plots [13]. Sutton-Grier et al. reported
that the relationship between functional diversity and denitrifica-
tion had strong positive correlation at high levels of soil resources
on between through the study of restored wetland [75].
Ecosystem functioning is often expressed through one or more
specific processes, such as litter decomposition, nitrogen cycle
[12,52], or characteristics, such as light interception, and produc-
tivity [50,53,54]. It is difficult to summarize and generalise these
functions. Furthermore, for the same natural assemblage, different
researchers have various interests and objectives, and their defini-
tions of the ecosystem and its functioning are not the same [63].
Therefore, the development of uniform standards used to define
the ecosystem and its functioning is required.
Plant functional trait and ecosystem functioning are not one to
one correspondence, neither. One trait could affect on a number of
ecosystem functioning. At the same time, ecosystem functioning is
related to different number of functional traits. Furthermore, eco-
system usually has multifunctionality, and there are interactions
between different ecosystem functioning. Therefore, further work
requires to clarify the relationship between functional diversity
and ecosystem functioning at different spatial and temporal scales
under different environmental conditions. Meanwhile, more work
needs to be done on multitrophic level to verify the relationship
between functional diversity and ecosystem functioning.
Land use change
Abiotic factors Biological factors
Species traits

Functional diversity
5. Conclusions and prospects

Ecological experiments, reviews and meta-analysis have shown

that functional diversity is one of the most effective predictors of
ecosystem functioning [11,49]. More and more studies define bio-
Mass ratio hypothesis Diversity hypothesis
diversity based on the variation and distribution of functional
traits in a community or ecosystem rather than species richness
[14]. However, it is difficult for ecologists to accept the trait based
functional diversity concept without skeptism [8]. In some cases,
measuring traits may be more difficult than counting species rich-
ness. However, in other situations, measuring a few numbers of Ecosystem functioning
traits may be more effective than spending vast amount of time
trying to identify every single species in a community [76]. In
short, if researchers want to understand the mechanism which
links biodiversity to ecosystem function accurately, one should in-
Ecosystem services Ecosystem management
clude functional diversity in the study on relationship between
biodiversity and ecosystem functioning [8].
The most fundamental questions in ecology are determining Fig. 2. Relationships between abiotic factors, biological factors, functional diversity,
which traits most relevant to ecosystem functioning and how to ecosystem functions, ecosystem services and ecosystem management under land
use change by human activities. Land use change affects the processes of
measure these traits. In addition, there is a lack of studies that cal-
community assembly, such as the environmental filtering, competition and
culate functional diversity [25,26,29,77,78]. The core elements of facilitation also change when the land use change occurs. Traits respond to abiotic
functional diversity index are: how many traits to choose, which and biological factors on one hand, and affect ecosystem functioning on the other
traits to choose, how to encode these traits, and which algorithm hand. Functional trait diversity influences ecosystem functioning by ‘‘mass ratio
to calculate the distance between the different traits among organ- hypothesis’’ or/and ‘‘diversity hypothesis’’, thus influences ecosystem services or
ecosystem management. The changes of ecosystem functioning could feed back to
ism [11,73]. The most useful index of functional diversity should be abiotic and biotic factors, and ecosystem functioning may affect by both functional
easy to calculate by ecologists, and provide the potential freeware diversity and environmental factors. Functional diversity may also directly influ-
for calculation [25]. ence ecosystem services and provide references for ecosystem management.
90 Y. Song et al. / Acta Ecologica Sinica 34 (2014) 85–91
A growing number of studies have shown that functional diver-
sity plays an important role in the prediction of ecosystem func-
tioning. However, Sasaki and Lauenroth reported that dominant
species could maintain the stability of plant communities better
than functional diversity on a Colorado grassland [79]. In Yukon,
located in Northwest Canada, McLaren and Turkington showed
that ecosystem functioning of grassland was determined by the
characters of plant functional groups [53]. Thus, the relationship
between functional diversity and ecosystem functioning need to
be further verified.
The most relevant functions of the ecosystems to human beings
are the products and services provided by ecosystems. The ques-
tion is how we manage ecosystems in a sustainable way. Func-
tional diversity affects ecosystem services and ecosystem
management through the impact of ecosystem functioning
(Fig. 2). Researchers should cognize accurately the relationship be-
tween functional diversity and ecosystem function. Ecosystem
management groups should include functional diversity in their
scheme and not just species richness [14].
Acknowledgments
We are especially grateful Xinxin Xue for the comments of ear-
lier version. We also thank the editor and reviewers for helpful
comments. This study is funded by the National Key Basic Research
Program (2011CB403203).
References
[1] F.S. Chapin, E.S. Zavaleta, V.T. Eviner, R.L. Naylor, P.M. Vitousek, H.L. Reynolds,
D.U. Hooper, S. Lavorel, O.E. Sala, S.E. Hobbie, M.C. Mack, S. Díaz, Consequences
of changing biodiversity, Nature 405 (6783) (2000) 234–242.
[2] S. Díaz, J. Fargione, F.S. Chapin III, D. Tilman, Biodiversity loss threatens human
well-being, PLoS Biol. 4 (8) (2006) 1300–1305.
[3] S. Díaz, M. Cabido, Vive la différence: plant functional diversity matters to
ecosystem processes, Trends Ecol. Evol. 16 (11) (2001) 646–655.
[4] D. Tilman, J. Knops, D. Wedin, P. Reich, M. Ritchie, E. Siemann, The influence of
functional diversity and composition on ecosystem processes, Science 277
(5330) (1997) 1300–1302.
[5] H. Hillebrand, B. Matthiessen, Biodiversity in a complex world: consolidation
and progress in functional biodiversity research, Ecol. Lett. 12 (12) (2009)
1405–1419.
[6] D.U. Hooper, F. Chapin III, J.J. Ewel, A. Hector, P. Inchausti, S. Lavorel, J.H.
Lawton, D.M. Lodge, M. Loreau, S. Naeem, H. Setälä, A.J. Symstad, J.
Vandermeer, D.A. Wardle, Effects of biodiversity on ecosystem functioning: a
consensus of current knowledge, Ecol. Monogr. 75 (1) (2005) 3–35.
[7] M.M. Mayfield, S.P. Bonser, J.W. Morgan, I. Aubin, S. McNamara, P.A. Vesk,
What does species richness tell us about functional trait diversity? Predictions
and evidence for responses of species and functional trait diversity to land-use
change, Glob. Ecol. Biogeogr. 19 (4) (2010) 423–431.
[8] M.W. Cadotte, K. Carscadden, N. Mirotchnick, Beyond species: functional
diversity and the maintenance of ecological processes and services, J. Appl.
Ecol. 48 (5) (2011) 1079–1087.
[9] P.B. Adler, E.W. Seabloom, E.T. Borer, H. Hillebrand, Y. Hautier, A. Hector, W.S.
Harpole, L.R. O’Halloran, J.B. Grace, T.M. Anderson, J.D. Bakker, L.A. Biederman,
C.S. Brown, Y.M. Buckley, L.B. Calabrese, C.J. Chu, E.E. Cleland, S.L. Collins, K.L.
Cottingham, M.J. Crawley, E.I. Damschen, K.F. Davies, N.M. DeCrappeo, P.A. Fay,
J. Firn, P. Frater, E.I. Gasarch, D.S. Gruner, N. Hagenah, R.L.J. Hille, H. Humphries,
V.L. Jin, A.D. Kay, K.P. Kirkman, J.A. Klein, J.M.H. Knops, P.K.J. La, J.G. Lambrinos,
W. Li, A.S. MacDougall, R.L. McCulley, B.A. Melbourne, C.E. Mitchell, J.L. Moore,
J.W. Morgan, B. Mortensen, J.L. Orrock, M. Prober Suzanne, D.A. Pyke, A.C. Risch,
M. Schuetz, M.D. Smith, C.J. Stevens, L.L. Sullivan, G. Wang, P.D. Wragg, J.P.
Wright, L.H. Yang, Productivity is a poor predictor of plant species richness,
Science 333 (6050) (2011) 1750–1753.
[10] D. Schleuter, M. Daufresne, F. Massol, C. Argillier, A user’s guide to functional
diversity indices, Ecol. Monogr. 80 (3) (2010) 469–484.
[11] O.L. Petchey, K.J. Gaston, Functional diversity: back to basics and looking
forward, Ecol. Lett. 9 (6) (2006) 741–758.
[12] E. Garnier, J. Cortez, G. Billès, M.L. Navas, C. Roumet, M. Debussche, G. Laurent,
A. Blanchard, D. Aubry, A. Bellmann, C. Neill, J.P. Toussaint, Plant functional
markers capture ecosystem properties during secondary succession, Ecology
85 (9) (2004) 2630–2637.
[13] M. Bernhardt-Römermann, C. Römermann, S. Sperlich, W. Schmidt, Explaining
grassland biomass–the contribution of climate, species and functional
diversity depends on fertilization and mowing frequency, J. Appl. Ecol. 48
(5) (2011) 1088–1097.
[14] M.W. Cadotte, The new diversity: management gains through insights into the
functional diversity of communities, J. Appl. Ecol. 48 (5) (2011) 1067–1069.
[15] O.L. Petchey, K.J. Gaston, Functional diversity (FD), species richness and
community composition, Ecol. Lett. 5 (3) (2002) 402–411.
[16] M. Tesfaye, N.S. Dufault, M.R. Dornbusch, D.L. Allan, C.P. Vance, D.A. Samac,
Influence of enhanced malate dehydrogenase expression by alfalfa on diversity
of rhizobacteria and soil nutrient availability, Soil Biol. Biochem. 35 (8) (2003)
1103–1113.
[17] D. Tilman, Functional diversity, in: S.A. Levin (Ed.), Encyclopedia of
Biodiversity, Academic Press, San DIego, 2001, pp. 109–120.
[18] J.P. Wright, S. Naeem, A. Hector, C. Lehman, P.B. Reich, B. Schmid, D. Tilman,
Conventional functional classification schemes underestimate the relationship
with ecosystem functioning, Ecol. Lett. 9 (2) (2006) 111–120.
[19] B. Walker, A. Kinzig, J. Langridge, Plant attribute diversity, resilience, and
ecosystem function: the nature and significance of dominant and minor
species, Ecosystems 2 (2) (1999) 95–113.
[20] D. Mouillot, W.H.N. Mason, O. Dumay, J.B. Wilson, Functional regularity: a
neglected aspect of functional diversity, Oecologia 142 (3) (2005) 353–359.
[21] D. Schmera, T. Ero }s, J. Podani, A measure for assessing functional diversity in
ecological communities, Aquat. Ecol. 43 (1) (2009) 157–167.
[22] S. Díaz, S. Lavorel, F. de Bello, F. Quétier, K. Grigulis, T.M. Robson, Incorporating
plant functional diversity effects in ecosystem service assessments, Proc. Natl.
Acad. Sci. 104 (52) (2007) 20684–20689.
[23] N.W.H. Mason, K. MacGillivray, J.B. Steel, J.B. Wilson, An index of functional
diversity, J. Veg. Sci. 14 (4) (2003) 571–578.
[24] Z. Botta-Dukát, Rao’s quadratic entropy as a measure of functional diversity
based on multiple traits, J. Veg. Sci. 16 (5) (2005) 533–540.
[25] E. Laliberté, P. Legendre, A distance-based framework for measuring functional
diversity from multiple traits, Ecology 91 (1) (2010) 299–305.
[26] O.L. Petchey, K.J. Gaston, Dendrograms and measuring functional diversity,
Oikos 116 (8) (2007) 1422–1426.
[27] W.K. Cornwell, D.W. Schwilk, D.D. Ackerly, A trait-based test for habitat
filtering: convex hull volume, Ecology 87 (6) (2006) 1465–1471.
[28] N.W.H. Mason, D. Mouillot, W.G. Lee, J.B. Wilson, Functional richness,
functional evenness and functional divergence: the primary components of
functional diversity, Oikos 111 (1) (2005) 112–118.
[29] S. Villéger, N.W.H. Mason, D. Mouillot, New multidimensional functional
diversity indices for a multifaceted framework in functional ecology, Ecology
89 (8) (2008) 2290–2301.
[30] Y.T. Song, P. Wang, D.W. Zhou, Methods of measuring plant community
functional diversity, Chin. J. Ecol. 30 (9) (2011) 2053–2059 (in Chinese).
[31] X.L. Jiang, W.G. Zhang, Functional diversity and its research method, Acta Ecol.
Sin. 30 (10) (2010) 2766–2773 (in Chinese).
[32] P. Wang, L.X. Sheng, H. Yan, D.W. Zhou, Y.T. Song, Plant functional traits
influence soil carbon sequestration in wetland ecosystem, Acta Ecol. Sin. 30
(24) (2010) 6990–7000 (in Chinese).
[33] M. Mouchet, F. Guilhaumon, S. Villéger, N.W.H. Mason, J.A. Tomasini, D.
Mouillot, Towards a consensus for calculating dendrogram-based functional
diversity indices, Oikos 117 (5) (2008) 794–800.
[34] J. Lepš, F. de Bello, S. Lavorel, S. Berman, Quantifying and interpreting
functional diversity of natural communities: practical considerations matter,
Preslia 78 (4) (2006) 481–501.
[35] G.D. Kader, M. Perry, Variability for categorical variables, J. Stat. Educ. 15(2)
(2007). Online: <http://www.amstat.org/publications/jse/v15n2/kader.html>.
[36] C.R. Rao, Diversity and dissimilarity coefficients: a unified approach, Theor.
Popul. Biol. 21 (1) (1982) 24–43.
[37] S. Champely, D. Chessel, Measuring biological diversity using euclidean
metrics, Environ. Ecol. Stat. 9 (2) (2002) 167–177.
[38] C.O. Webb, D.D. Ackerly, S.W. Kembel, Phylocom: software for the analysis of
phylogenetic community structure and trait evolution, Bioinformatics 24 (18)
(2008) 2098–2100.
[39] F. Casanoves, L. Pla, J.A. Di Rienzo, S. Díaz, Fdiversity: a software package for
the integrated analysis of functional diversity, Methods Ecol. Evol. 2 (3) (2011)
233–237.
[40] F. Casanoves, L.E. Pla, J.A. Di Rienzo, Fdiversity: an integrated tool to estimate
and analyze functional diversity, Bull. Ecol. Soc. Am. 92 (2) (2011) 147–152.
[41] S. Naeem, Disentangling the impacts of diversity on ecosystem functioning in
combinatorial experiments, Ecology 83 (10) (2002) 2925–2935.
[42] S.R. Biswas, A.U. Mallik, Species diversity and functional diversity relationship
varies with disturbance intensity, Ecosphere 2 (4) (2011) 1–10.
[43] D.F.B. Flynn, M. Gogol-Prokurat, T. Nogeire, N. Molinari, B.T. Richers, B.B. Lin, N.
Simpson, M.M. Mayfield, F. DeClerck, Loss of functional diversity under land
use intensification across multiple taxa, Ecol. Lett. 12 (1) (2009) 22–33.
[44] M.M. Mayfield, M.F. Boni, G.C. Daily, D. Ackerly, Species and functional
diversity of native and human-dominated plant communities, Ecology 86 (9)
(2005) 2365–2372.
[45] C.R. Fonseca, G. Ganade, Species functional redundancy, random extinctions
and the stability of ecosystems, J. Ecol. 89 (1) (2001) 118–125.
[46] S. Naeem, J.P. Wright, Disentangling biodiversity effects on ecosystem
functioning: deriving solutions to a seemingly insurmountable problem,
Ecol. Lett. 6 (6) (2003) 567–579.
[47] O.L. Petchey, K.J. Gaston, Extinction and the loss of functional diversity, Proc.
Roy. Soc. Lond. B Biol. Sci. 269 (1501) (2002) 1721.
[48] J.M. Craine, D. Tilman, D. Wedin, P. Reich, M. Tjoelker, J. Knops, Functional
traits, productivity and effects on nitrogen cycling of 33 grassland species,
Funct. Ecol. 16 (5) (2002) 563–574.
 Y. Song et al. / Acta Ecologica Sinica 34 (2014) 85–91
[49] J.N. Griffin, V. Méndez, A.F. Johnson, S.R. Jenkins, A. Foggo, Functional diversity
predicts overyielding effect of species combination on primary productivity,
Oikos 118 (1) (2009) 37–44.
[50] D.F.B. Flynn, N. Mirotchnick, M. Jain, M.I. Palmer, S. Naeem, Functional and
phylogenetic diversity as predictors of biodiversity–ecosystem function
relationships, Ecology 92 (8) (2011) 1573–1581.
[51] M.W. Cadotte, J. Cavender-Bares, D. Tilman, T.H. Oakley, Using phylogenetic,
functional and trait diversity to understand patterns of plant community
productivity, PLoS One 4 (5) (2009) e5695, http://dx.doi.org/10.1371/
journal.pone.0005695.
[52] D.C. Laughlin, Nitrification is linked to dominant leaf traits rather than
functional diversity, J. Ecol. 99 (5) (2011) 1091–1099.
[53] J.R. McLaren, R. Turkington, Ecosystem properties determined by plant
functional group identity, J. Ecol. 98 (2) (2010) 459–469.
[54] K. Mokany, J. Ash, S. Roxburgh, Functional identity is more important than
diversity in influencing ecosystem processes in a temperate native grassland, J.
Ecol. 96 (5) (2008) 884–893.
[55] R. Costanza, R. d’Arge, R. De Groot, S. Farber, M. Grasso, B. Hannon, K. Limburg,
S. Naeem, R.V. O’Neill, J. Paruelo, R. Raskin, P. Sutton, M. van den Belt, The value
of the world’s ecosystem services and natural capital, Nature 387 (6630)
(1997) 253–260.
[56] S.W. Pacala, A.P. Kinzig, Introduction to theory and the common ecosystem
model, in: A.P. Kinzig, D. Tilman, S. Pacala (Eds.), Functional Consequences of
Biodiversity: Empirical Progress and Theoretical Extensions, Princeton
University Press, Princeton, 2002.
[57] D.S. Srivastava, M. Vellend, Biodiversity–ecosystem function research: is it
relevant to conservation?, Annu Rev. Ecol. Evol. Syst. 36 (2005) 267–294.
[58] P.S. Giller, H. Hillebrand, U.G. Berninger, M.O. Gessner, S. Hawkins, P. Inchausti,
C. Inglis, H. Leslie, B. Malmqvist, M.T. Monaghan, P.J. Morin, G. O’Mullan,
Biodiversity effects on ecosystem functioning: emerging issues and their
experimental test in aquatic environments, Oikos 104 (3) (2004) 423–436.
[59] M.A. Sanderson, R.H. Skinner, D.J. Barker, G.R. Edwards, B.F. Tracy, D.A. Wedin,
Plant species diversity and management of temperate forage and grazing land
ecosystems, Crop Sci. 44 (4) (2004) 1132–1144.
[60] A. Hector, R. Bagchi, Biodiversity and ecosystem multifunctionality, Nature
448 (7150) (2007) 188–190.
[61] E.S. Zavaleta, J.R. Pasari, K.B. Hulvey, G.D. Tilman, Sustaining multiple
ecosystem functions in grassland communities requires higher biodiversity,
Proc. Natl. Acad. Sci. 107 (4) (2010) 1443–1446.
[62] D. Mouillot, S. Villéger, M. Scherer-Lorenzen, N.W.H. Mason, Functional
structure of biological communities predicts ecosystem multifunctionality,
PLoS One 6 (3) (2011) e17476, http://dx.doi.org/10.1371/journal.pone.0017476.
91
[63] K. Jax, Function and ‘‘functioning’’ in ecology: what does it mean?, Oikos 111
(3) (2005) 641–648
[64] L. Gamfeldt, H. Hillebrand, P.R. Jonsson, Multiple functions increase the
importance of biodiversity for overall ecosystem functioning, Ecology 89 (5)
(2008) 1223–1231.
[65] J.F. Feng, Y. Li, L. Zhu, Discrimination of concepts of ecosystem functions and
ecosystem services, Ecol. Environ. Sci. 18 (4) (2009) 1599–1603 (in Chinese).
[66] F. Isbell, V. Calcagno, A. Hector, J. Connolly, W.S. Harpole, P.B. Reich, M.
Scherer-Lorenzen, B. Schmid, D. Tilman, J. van Ruijven, A. Weighlt, B.J. Wilsey,
E.S. Zavaleta, M. Loreau, High plant diversity is needed to maintain ecosystem
services, Nature 477 (7363) (2011) 199–202.
[67] D. Tilman, J.A. Downing, Biodiversity and stability in grasslands, Nature 367
(6461) (1994) 363–365.
[68] S. Naeem, L.J. Thompson, S.P. Lawler, J.H. Lawton, R.M. Woodfin, Declining
biodiversity can alter the performance of ecosystems, Nature 368 (6473)
(1994) 734–737.
[69] M. Loreau, Biodiversity and ecosystem functioning: a mechanistic model, Proc.
Natl. Acad. Sci. 95 (10) (1998) 5632–5636.
[70] O.L. Petchey, A. Hector, K.J. Gaston, How do different measures of functional
diversity perform?, Ecology 85 (3) (2004) 847–857
[71] D. Tilman, Distinguishing between the effects of species diversity and species
composition, Oikos 80 (1) (1997) 185.
[72] J.P. Grime, Benefits of plant diversity to ecosystems: immediate, filter and
founder effects, J. Ecol. 86 (6) (1998) 902–910.
[73] C. Ricotta, M. Moretti, CWM and Rao’s quadratic diversity: a unified
framework for functional ecology, Oecologia 167 (1) (2011) 181–188.
[74] J. Schumacher, C. Roscher, Differential effects of functional traits on
aboveground biomass in semi-natural grasslands, Oikos 118 (11) (2009)
1659–1668.
[75] A.E. Sutton-Grier, J.P. Wright, B.M. McGill, C. Richardson, Environmental
conditions influence the plant functional diversity effect on potential
denitrification, PLoS One 6 (2) (2011) e16584, http://dx.doi.org/10.1371/
journal.pone.0016584.
[76] D.W. Zhou, A phylogenic approach to comparative functional plant ecology,
Acta Ecol. Sin. 29 (10) (2009) 5644–5655 (in Chinese).
[77] J. Podani, D. Schmera, On dendrogram-based measures of functional diversity,
Oikos 115 (1) (2006) 179–185.
[78] T.T. Meng, J. Ni, G.H. Wang, Plant functional traits, environments and
ecosystem functioning, Chin. J. Plant Ecol. 31 (1) (2007) 150–165.
[79] T. Sasaki, W.K. Lauenroth, Dominant species, rather than diversity, regulates
temporal stability of plant communities, Oecologia 166 (3) (2011) 761–768.