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ECOSYSTEMS
Ecosystems (1999) 2: 95–113
r 1999 Springer-Verlag
ORIGINAL ARTICLES
Plant Attribute Diversity, Resilience,
and Ecosystem Function: The Nature
and Significance of Dominant
and Minor Species
Brian Walker,1* Ann Kinzig,2 and Jenny Langridge1
1Division
of Wildlife and Ecology, CSIRO, PO Box 84, Lyneham, Canberra, Australia 2602; and 2Department of Ecology
and Evolutionary Biology, Princeton University, Princeton, New Jersey 08540, USA
ABSTRACT
This study tested an hypothesis concerning patterns
in species abundance in ecological communities.
Why do the majority of species occur in low abundance, with just a few making up the bulk of the
biomass? We propose that many of the minor
species are analogues of the dominants in terms of
the ecosystem functions they perform, but differ in
terms of their capabilities to respond to environmental stresses and disturbance. They thereby confer
resilience on the community with respect to ecosystem function. Under changing conditions, ecosystem function is maintained when dominants decline or are lost because functionally equivalent
minor species are able to substitute for them. We
have tested this hypothesis with respect to ecosystem functions relating to global change. In particular, we identified five plant functional attributes—
height, biomass, specific leaf area, longevity, and
leaf litter quality—that determine carbon and water
fluxes. We assigned values for these functional
attributes to each of the graminoid species in a
lightly grazed site and in a heavily grazed site in an
Australian rangeland. Our resilience proposition
was cast in the form of three specific hypotheses in
relation to expected similarities and dissimilarities
between dominant and minor species, within and
between sites. Functional similarity—or ecological
distance—was determined as the euclidean distance
between species in functional attribute space. The
analyses provide evidence in support of the resilience hypothesis. Specifically, within the lightly
grazed community, dominant species were functionally more dissimilar to one another, and functionally similar species more widely separated in abundance rank, than would be expected on the basis of
average ecological distances in the community. Between communities, depending on the test used,
two of three, or three of four minor species in the
lightly grazed community that were predicted to
increase in the heavily grazed community did in fact
do so. Although there has been emphasis on the
importance of functional diversity in supporting the
flow of ecosystem goods and services, the evidence
from this study indicates that functional similarity
(between dominant and minor species, and among
minor species) may be equally important in ensuring persistence (resilience) of ecosystem function
under changing environmental conditions.
Received 12 August 1998; accepted: 24 November 1998
2Current address: Department of Biology, Arizona State University,
Tempe, Arizona, USA.
*Corresponding author, email: [email protected]
Key words: ecosystem; function; diversity; redundancy; resilience.
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B. Walker and others
INTRODUCTION
PLANT FUNCTIONAL TYPES
Most diversity–function studies have related, in one
way or another, number of species to ecosystem
biomass or production. Some [for example, McNaughton (1985) and Tilman (1996)] have shown
that year-to-year variation in species abundance
tends to stabilize community biomass, and a few
[Vitousek and Hooper (1993) and Hooper and
Vitousek (1997), for example] have considered
aspects of ecosystem function other than biomass.
Less emphasis has been given to the different
characteristics or performance attributes of the individual species present. The debate is now shifting,
however, to recognize that the provision of ecosystem services and functions is likely to be related to
the distribution of species among guilds or functional groups, and that these distributions may be
only weakly related to diversity as measured by
numbers of species [for instance, see Leps and
others (1982), MacGillivray and Grime (1995), Tilman and others (1997), Wardle and others (1997),
and Naeem (1998)]. Improving our understanding
of diversity–function relationships across ecosystems will require a categorization of species, or of
species attributes, that can be related to function.
In this report, we explore the hypothesis that
some groups of dominant and minor species within
an ecosystem are functionally similar, and that this
functional similarity provides ‘‘buffering’’ or resilience against perturbations or environmental variability. Thus, the species that dominate under a
given set of environmental conditions serve to
maintain ecosystem function under those conditions. Minor species, on the other hand, will be
functionally similar to dominant species, but with
different environmental requirements and tolerances; these species maintain resilience in ecosystems by allowing the maintenance of function
under changing conditions. Thus, under our hypothesis, a classification scheme that relates species
attributes to function should produce guilds in
which both dominant and minor species are present; moreover, dominant and minor species should
‘‘switch’’ in abundance under changing environmental conditions, and this abundance shift should
affect functional roles as well.
We develop a method for classifying plant functional types to examine the similarities in functional
attributes between dominant and minor species,
and apply this to heavily grazed and lightly grazed
sites in an Australian rangeland.
The literature on functional types [for example,
Smith and others (1997)] is more concerned with
predicting the distribution of plant types around the
world, or with the related question of how plant
species persist in different ecosystems, than it is with
analyzing the impact of functional–type diversity on
particular aspects of ecosystem function. Few investigations thus far have developed categorization
schemes that group species into types relating to the
ecosystem-function role they perform. Most ‘‘functional’’ classification schemes have had as their goal
predicting patterns in species distributions rather
than predicting the effects of diversity on the provision or maintenance of ecosystem function. In this
sense, these schemes are more correctly labeled
plant–ecology–strategy schemes (PESSs) (Westoby
1998) than plant–function–type schemes (PFTs).
Nonetheless, in keeping with the tradition of the
literature, we call most classification schemes PFTs,
even when they have been proposed as a means of
classifying species with respect to adaptation strategies and thus distributions. The PFT we propose
below, however, differs from these previous studies
in that we seek a classification that enables a direct
mapping to ecosystem function; we briefly review
existing PFTs before introducing our own scheme.
Probably the best-known scheme for plant adaptation to the environment is the triangular model of
Grime (1979), which is based on three general
response strategies (competitiveness, weediness, and
survival). Westoby (1998) has proposed an explicit
three-dimensional PFT, using three particular measurable plant attributes (specific leaf area, canopy
height, and seed size) that allows any plant species
to be easily and exactly placed in the classification
scheme. The value of this approach is that it is
minimal and will enable it to be widely used; the
same minimalist approach will be a requirement for
any successful PFT scheme for ecosystem function.
Although Westoby’s three axes do reflect functional
contribution to some extent, they are designed to
capture in an overall way the strategies that species
have developed for persisting in their environments. These strategies for persistence may have
some bearing on the plant attributes that relate to
function, but there is no a priori reason to expect
classification schemes based on how individual species persist over time to resemble one that is related
to the functions that these species perform in an
ecosystem.
Box (1981) introduced a scheme for predicting
the presence of 90 different plant types, based on an
environmental envelope comprised of eight biocli-
Ecosystem Function and Plant Attribute Diversity
matic indices. Though this scheme produces a vegetation description, the description does provide for
a more functional interpretation than one based on
floristics. Similarly, Leishman and Westoby (1992)
determined 43 plant attributes for some 300 species
from the semiarid mulga woodlands of western New
South Wales in Australia. They used 8 vegetative, 9
life-history, 15 phenology, and 11 seed-biology attributes, and concluded that the 300 species fell into
five groups that were related with respect to growth
characteristics, reflecting adaptations of plants to
their environments. The reproductive attributes (to
do with seed size and dispersal) were unrelated to
these five groups.
Of the 18 chapters in the recent International
Global Biosphere Project (IGBP) sponsored book
Plant Functional Types (Smith and others 1997), by
far the majority are concerned with the use of PFTs
in dynamic models of vegetation change. To be sure,
the underlying purpose of the book was to derive a
global description of vegetation that could contribute to an improved understanding of vegetation–
atmosphere interactions, and some of the proposed
schemes or outlines do include both demographic
and ecosystem function attributes (for example, the
chapters by Scholes and others, Lauenroth and
others, Walker, and Hobbs). Scholes and colleagues
(1997) suggested 18 attributes for a functional
classification of South African grasses, incorporating
characteristics that relate to (a) the distribution of
the grass species in environmental space, (b) the
responses of the grasses to disturbance, and (c)
functional aspects such as production. In most of the
work to date, though, the emphasis has been primarily on how vegetation composition will respond to
changes in climate or to disturbance of some sort, as
exemplified by the ‘‘vital attributes’’ scheme of
Noble and Slatyer (1980).
A review of plant functional classifications by
Lavorel and others (1997) identified four types of
functional groupings, one of which (their third
type) concerns the functions that plants perform.
However, this type is defined in relation to ‘‘either
the contribution of species to ecosystem processes or
to the response of species to changes in environmental variables.’’ The species within such functional
groups are therefore assumed to be similar in both
respects—contribution to processes and response to
environment. In accordance with the distinction
made by Walker (1997) between ‘‘response functions’’ and ‘‘feedback functions,’’ we believe these
two types of functions—response and contribution—
are significantly different and the differences are the
basis for maintaining ecosystem resilience, as we
proposed above and shall demonstrate below. In
97
other words, dominant and minor species may be
similar in their contribution to function, but will be
different in response, thus permitting a ‘‘reservoir of
resilience’’ that allows maintenance of function
under shifting conditions. Hurlbert (1997) has addressed the influence species have on the ‘‘biocenoses’’ in which they occur and offers a measure of the
functional importance of a species, which he defines
as the sum, over all species, of the changes (sign
ignored) in productivity that would occur on removal of the particular species from the biocenosis.
As he points out, however, the functional values so
defined cannot reasonably be empirically measured.
Pahl-Wostl (1995) offers a diversity measure for
primary producers, Dp, which she defines as ‘‘a
measure of dynamic and functional diversity.’’ She
has developed a theory of ecosystems as networks
and uses information theory to measure the level of
organization (and, conversely, of redundancy) in an
ecosystem. Her concept is based on placing all
organisms into delineated overlapping groups. She
defines ‘‘dynamic classes’’ (based on turnover times)
and ‘‘functional niches’’ in a number of ‘‘spatial
dimensions’’ that co-occur in particular ‘‘time intervals.’’ While her derived ‘trophic dynamic modules’
are worth further consideration, her diversity measure is difficult to use. It does not relate to any
specific functions, and it would be very difficult to
get the information needed to apply it to any
ecosystem.
In keeping with the emphasis of the meeting that
stimulated this study (see the Acknowledgments),
we concentrate on how to use plant functional
attributes in analyses of ecosystem function. The
question we are concerned with, therefore, is not
one of how the vegetation on a site might change in
response to climate change or some other disturbance, but rather, given a change in the vegetation
(that is, a change in or loss of plant biodiversity, for
whatever reason), what will be the consequences
for ecosystem function? It is analogous to Hurlbert’s
(1997) definition of functional importance, but
could and should include more than just productivity as a measure of function.
THE ROLES OF DOMINANT AND MINOR
SPECIES: AN HYPOTHESIS RELATING
FUNCTIONAL DIVERSITY TO RESILIENCE
IN ECOSYSTEM PROCESSES
Figure 1, from a savanna rangeland in southwest
Queensland, is an example of the classic distribution
of species abundance in a community. A few species
make up the bulk of the biomass, and there is a long
tail of relatively unabundant species. The particular
98
B. Walker and others
Figure 1. (a) Relative abundance of all species and (b)
standardized abundance of grass and sedge species in a
lightly grazed rangeland site in southwest Queensland,
Australia.
shape of the curve varies between ecosystem types
(flatter for tropical forests) and stages of succession
[flatter for older communities; for example, see
Bazzaz (1975)]. Whatever the particular shape,
most of the biodiversity in the world lies in this tail.
It includes the bulk of what Hurlbert (1997) describes as the ‘‘great biocenotic proletariat.’’ Taking
biomass as one indicator of ecosystem function
(carbon storage, for instance), it is therefore reasonable to conclude that it is the small set of relatively
abundant species that are functionally important.
These few species are doing the bulk of photosynthesis, transpiration, nutrient uptake, and so on. If we
consider other functions, such as nitrogen fixation,
it is likely, in systems where there is significant
nitrogen fixation, that most of the symbiotic nitrogen fixation will be done by just a few, relatively
abundant, plant species. What, then, is the role of
the tail-end species? We propose, in line with the
‘‘insurance’’ hypothesis (Main 1982; Walker 1995;
Naeem and Li 1997), that the abundant species
contribute to ecosystem function or performance at
any particular time, whereas the tail-end species
contribute to ecosystem resilience.
We hypothesize that the small number of dominant plant species have somewhat different attributes in terms of the ecosystem functions they
perform (CO2 fixation, water uptake from the soil,
and the like). The numerous other species, which all
individually make up just a small percentage of
plant biomass or cover, are mostly functional equivalents of the dominant species, but with different
environmental requirements and tolerances. Particular species in the tail are in the same functional type
as a dominant species, in terms of the ecosystem
function they perform, but they are in different
functional types in terms of their response to environmental variables. Because of these differences,
they provide the response capability of the ecosystem to disturbance and change. In other words, they
contribute to ecosystem resilience. They are low in
abundance because the conditions at the time favor
the dominants. Some, for example, are competitively inferior to similar but more abundant species,
and thus interspecific competitive interactions suppress their abundance in the community.
There are, of course, exceptions to this pattern,
since there are other reasons why species may be
rare or low in abundance within a community.
Some are habitat specialists, others are important
keystone species, and some are minor ‘‘passenger’’
species (Walker 1992) that manage to maintain
themselves in the ecosystem but do not seem to play
any role in driving it.
For the most part, however, we contend that the
minor species differ in their response capabilities
(traits) from their abundant counterparts, and the
function to which they (that is, the dominant
species plus its minor counterpart species) collectively contribute is secured in the face of environmental change because of this diversity of response
capability. It is easy to imagine how this might be so
for tail-end species that are at the edges of their
environmental ranges. Arid-adapted species hanging on in small amounts in a mesic community
provide the capacity for the community to respond
during periods of drought, and so on.
ECOLOGICAL DISTANCE
ATTRIBUTE SPACE
IN
PLANT
For an analysis of the role of biodiversity in ecosystem function, it is appropriate to consider only those
plant attributes that relate to the functions of interest. In the sense of the conceptual model of PFTs
proposed by Smith and colleagues (1993), we focus
on the intensive characters that are related to parameters in models of ecosystem function, rather than
the extensive characters that are related more to life
cycle and ‘‘response’’ features. Furthermore, in order to contribute to resource-use policy and management, ecosystem function has to be defined in terms
of human use or interest, and the relationship
between biodiversity and function has to be exam-
Ecosystem Function and Plant Attribute Diversity
ined in the context of specific functions. A general
relationship is unlikely to be meaningful (Woodward and others 1997). Since the focus of this
analysis was global change, the functions of concern
are therefore
●
Carbon stocks
●
Carbon fluxes
●
Nitrogen fluxes
●
Evapotranspiration
Different plants have different attributes that
affect the above functions in different ways. Combining these attributes leads to the formation of either
attribute sets or PFTs.
The distance that two PFTs (or species) are apart
in the attribute space is a measure of their ‘‘ecological distance.’’ The ecological distances provide a
measure of both functional diversity and functional
redundancy (resilience); large ecological distances
between species implies functional diversity, whereas
small distances implies some degree of functional
redundancy. If a function-based ecological distance
is used in the estimation of biodiversity, the functional group diversity so obtained will (it is asserted)
give stronger relationships between diversity and
function than those obtained so far. Tilman and
colleagues (1997) and Roi (CNRS, Montpellier, personal communication) have both shown, experimentally, that it is the inclusion of plants from
different functional groups that influences total
biomass, rather than just the addition of more
species.
For the global-change functions of concern, the
set of plant functions and their associated plant
attributes are likely to include the following:
1. C & N cycling (C stocks, C fluxes, and N fluxes)
Plant functions: Net amount of carbon fixed and
stored per year; maximum carbon storage; seasonal changes in carbon storage; annual nitrogen
releases from litter; nitrogen retention in plants;
nitrogen fixation rate.
Plant attributes: Relative growth rate [approximated by specific leaf area (SLA); see Westoby
(1998) for discussion]; maximum total biomass
(on a per-hectare basis); deciduousness; longevity (annual, biennial, and so on); growth phenology; plant architecture (for example, height);
N-fixing capacity; leaf litter quality (for example,
nitrogen–carbon or lignin–nitrogen ratios), which
determines the rate of litter decomposition and
therefore release of both carbon and nitrogen.
2. Water budget
Plant functions: Total transpiration; water uptake
by roots from different soil layers.
99
Plant attributes: Water-use efficiency; transpiration rate; rooting depth; root-distribution in profile.
For most ecosystems, some of these attributes will
be difficult to assess because the data are not
available and cannot be acquired on reasonable
time scales. To be useful, a PFT classification will
have to include attributes that can be easily measured for all species. For an initial test of our
hypothesis, we selected those attributes for which
we already had data or for which we could assign a
classification in a multilevel ‘‘high/low’’ point
scheme. Thus, we consider the following five attributes of plants as a suggested set that (a) can be
easily measured and (b) are related to the functions
important for global change, outlined above:
Height
Mature plant biomass
SLA (related to relative growth rate)
Longevity
Leaf litter quality
We thus omit growth phenology, N-fixing capacity, and root distribution from consideration. These
measures are difficult to obtain and were not available for the Australian rangeland used in this report.
Moreover, we did not explicitly include mature
plant biomass or litter quality in our attribute set,
but instead used related measures of lateral cover
and leaf coarseness.
Some cautionary comments about the use of this
approach are appropriate here. To begin with, the
placement of species in this five-dimension attribute
space implies orthogonality between the attributes,
and this is unlikely to be true. For example, if the
SLA of a plant is related in some way to plant
longevity or leaf coarseness, then the loss of a
species with a particular SLA also means the loss of a
species with a particular life span or litter quality.
A further complication is the long-term versus
short-term effects of species. Although two species
may share the same attribute values for the above
set, they may differ in terms of their longer-term
feedback effects on the ecosystem. For example, J.
Roi (CNRS, Montpellier, personal communication)
has shown that although it makes no difference in
terms of annual biomass production whether his
experimental plots have one or several C3 grass
species, each grass species induces a different composition of soil biota, and the long-term effect on soil
properties may therefore be different. If a long-term
view of function is considered, then the associated
soil biota may need to become another attribute axis
along which plant species differ.
Finally, several of the attributes deemed to be
100
B. Walker and others
important in terms of contribution to ecosystem
function are also important in terms of species’
abilities to respond to environmental change (for
example, rooting depth and longevity). Because of
this, there is unlikely to be a simple, linear relationship between total attribute diversity and current
ecosystem function. The relationship will be stronger if function is considered as sustained performance over a long period, and potentially weaker if
one correlates function immediately after a perturbation with total attribute diversity.
Eq. (1b) over Eq. (1a) does not affect the conclusions presented below.
If sites or individuals differ in the number of
species (or attributes), the use of euclidean distance
can have drawbacks, but in this case all five attributes are measured for all species in the calculation of ED and it is therefore an appropriate measure.
Having created a matrix of ED values for the
species, the index of FAD can be calculated as the
sum of the distances the species are apart:
n
FAD2 5
MEASURING FUNCTIONAL
ATTRIBUTE DIVERSITY
FAD1: The number of different attribute combinations that occurs in the community. This must be
equal to or less than the number of species. In the
context of phylogenetic diversity, it is analogous to
the number of species, or species richness.
FAD2: The standardized distance the species are
apart in attribute space. Use of absolute values is
inappropriate, since the attributes are measured in
different units. Also, given the state of knowledge
about the quantitative values of these attributes, it is
only possible to put many of them into a number of
classes. The use of a normalized scale allows us to
develop at least a preliminary estimate of functional
diversity, and in the example below we have used a
five-point scale.
The simplest measure of distance apart that has
been used in ecology is the euclidean distance
(ecological distance, ED):
I
3o
4
(Aij 2 Aik)2
i51
1/2
(1a)
where Aij and Aik are the attribute values of species j,
k for attribute i, and I is the total number of
attributes being considered.
We have used a modified version of ED for most
of our analyses, and omit the square-root from Eq.
(1a); thus, our ecological distance is given by
I
EDjk 5
3o
i51
o o ED
ij
(2)
i51 j5i
We suggested two appropriate measures of functional attribute diversity (FAD):
EDjk 5
n
4
(Aij 2 Aik)2
(1b)
Use of Eq. (1b) over Eq. (1a) has the effect of
spreading species out in attribute space, and thus
can make similarities and differences in functional
attributes easier to identify. Because the two ecological distances are directly related to each other, use of
where n 5 the number of species
There is no direct analogue of this measure in
phylogenetic diversity terms, but the closest would
be a measure of phylogenetic distance, involving
differences in genera and families [for example, see
Faith (1992)]. This index takes no account of the
abundances of the species. Weighting the FAD2 by
abundance of species would bring it to the equivalent of the Shannon-Weaver measure (H) or Simpson’s index, but we see no reason to do this (as will
become evident).
TESTING
FROM A
HYPOTHESIS: AN EXAMPLE
SAVANNA COMMUNITY
THE
To provide a focus, we have used a savanna rangeland community in southwest Queensland, Australia (Figure 1, lightly grazed site). The data are from a
study examining the effects of artificial water supplies on rangeland biodiversity (Landsberg and others 1997) and includes five sites along a grazing
gradient, from very heavy grazing near the water
point (site 1) to very light grazing around 6 km from
water (site 5). Table 1 presents the species composition of sites 1 and 5 (the heavily grazed and the
lightly grazed sites).
Since the focus of our interest was on the functional diversity of the graminoids and how they (a)
contribute to overall grass production and (b) respond to grazing pressure, and because we were
unable to get estimates of the attributes for the
dicotyledonous species, we have, for the purposes of
this study, restricted our attention to the graminoid
community (see Figure 1b for the distribution of
graminoid abundance at the lightly grazed site). We
estimated the values of the five functional attributes
for each of the 21 grass species and one sedge species
in the rangeland, based on what is known about
them and using specimens from a reference collection from the study area. To standardize for compari-
Ecosystem Function and Plant Attribute Diversity
101
Table 1. Relative Abundance (RA), Determined as Percentage Frequency of Species in 80 by 1-m2 Quadrats
at the Lightly Grazed (LG) and Heavily Grazed (HG) Sites
RA%
RA%
Species
LG
HG
Grass
Aristida contorta
Tripogon loliiformis
Enneapogon polyphyllus
Aristida latifolia
Themeda triandra
Digitaria brownii
Chloris pectinata
Eragrostis microcarpa
Eriachne pulchella
Panicum effusum
Sporobolus actinocladus
Digitaria ammophila
Dichanthium sericeum
Austrochloris dicanthioides
Tragus australianus
Eragrostis basedownii
Monachather paradoxa
Amphipogon caricinus
Eragrostis dielsii
Thyridolepis mitchelliana
Eragrostis xerophila
6.56
5.91
4.60
3.94
2.52
2.19
1.42
0.98
0.88
0.88
0.77
0.77
0.66
0.55
0.33
0.33
0.33
0.22
0.22
0.22
—
4.59
10.11
3.68
—
—
1.68
2.45
1.23
3.06
—
—
—
—
—
0.61
—
—
—
3.22
0.46
1.07
Sedge
Fimbristylis dichotoma
4.38
8.27
5.36
5.25
4.70
4.49
2.74
2.63
2.52
2.30
2.08
1.97
1.53
1.53
1.53
1.53
1.42
1.20
2.14
6.58
5.51
8.42
3.52
2.91
—
1.84
0.92
3.68
0.15
—
0.15
0.31
1.53
0.31
1.09
0.88
5.82
1.38
Forbs
Evolvulus alsinoides
Calotis hispidula
Calotis plumulifera
Rhodanthe floribunda
Plantago turrifera
Goodenia pinnatifida
Stenopetalum nutans
Vittadinia constricta
Phyllanthus lacunellus
Centipeda thespidioides
Daucus glochidiatus
Ptilotus macrocephalus
Chamaesyce drummondii
Trachymene ochracea
Alternanthera angustifolia
Calandrinia eremaea
Lepidium
muelleri–ferdinandii
Chenopodium melanocarpum
sons between attributes, we converted each attribute to a scale of 1–5. The five-point classification
scheme for each of the five attributes is presented in
Table 2. SLA (dry weight/leaf area) was determined
from leaf samples from the reference collection. For
Species
Forbs cont.
Glycine canescens
Bulbine alata
Boerhavia repleta
Ptilotus gaudichaudii
Marsilea drummondii
Calocephalus knappi
Calotis inermis
Convolvulus erubescens
Portulaca filifolia
Goodenia cycloptera
Wahlenbergia sp.
Gnephosis arachnoidea
Portulaca oleracea
Chrysocephalum sp.
Lepidium oxytrichum
Heliotropium tenuifolium
Tribulus terrestris
Goodenia lunata
Goodenia berardiana
Pimelea elongata
Goodenia glauca
Hyalosperma semisterile
Calotis cuneifolia
Dianella longifolia var. porracea
Spergularia sp.
Tricoryne elatior
Ptilotus helipteroides var.
helipteroides
Calandrinia ptychosperma
Chenopodium cristatum
Dysphania glomulifera
Oxalis corniculata
Subshrubs
Abutilon macrum
Sida cunninghamii
Sida platycalyx
Sida species nov. aff. filiformis
Solanum quadriloculatum
Abutilon otocarpum
Malvastrum americanum
Sclerolaena cornishiana
Solanum esuriale
Sclerolaena diacantha
LG
HG
0.88
0.88
0.88
0.77
0.77
0.77
0.66
0.66
0.66
0.66
0.66
0.55
0.55
0.44
0.33
0.33
0.33
0.33
0.22
0.22
0.11
0.11
0.11
0.11
0.11
0.11
0.31
0.15
0.46
0.77
—
—
1.53
0.31
—
—
0.46
—
1.07
1.84
0.61
0.15
—
0.77
—
—
0.15
—
—
—
—
—
—
—
—
—
—
0.46
0.77
0.61
0.15
1.38
1.31
1.09
0.88
0.55
0.22
0.11
0.11
0.11
0.11
—
0.77
—
0.77
0.15
—
—
—
0.46
0.15
0.15
leaf litter quality, we used a very rough estimate of
leaf coarseness and have included it only for the
sake of the example. We did not have data for
mature plant biomass and have used a measure of
lateral cover instead. Together with height, this
102
B. Walker and others
Table 2. Functional Attributes of the Herbaceous Layer
Functional
Attribute Value
Height (cm)
SLA a (mm mg21 )
Longevity (years)
1
2
3
4
5
,5
5–10
10–15
15–20
.20
,4
4–8
8–12
12–16
.16
Annual
40–60
Coarse
Biannual
60–80
Medium
aCorrelated
.2 years
Cover (%)
.80
Leaf Coarseness
Soft
with relative growth rate (see the text) where a rank of 1 is slow and 5 is fast.
Table 3. Frequency (Maximum of 80) and Functional Attribute Values for the Graminoid Species
at the Lightly Grazed (LG) and Heavily Grazed (HG) Sites
Frequency
Functional Attribute
Species
LG
HG
Height
SLA
Longevity
Cover
Leaf Coarseness
(1)Aristida contorta
(2)Tripogon loliiformis
(3)Enneapogon polyphyllus
(4)Fimbristylis dichotoma
(5)Aristida latifolia
(6)Themeda triandra
(7)Digitaria brownii
(8)Chloris pectinata
(9)Eragrostis microcarpa
(10)Eriachne pulchella
(11)Panicum effusum
(12)Sporobolus actinocladus
(13)Digitaria ammophila
(14)Dichanthium sericeum
(15)Austrochloris dicanthioides
(16)Tragus australianus
(17)Eragrostis basedownii
(18)Monachather paradoxa
(19)Eragrostis dielsii
(20)Amphipogon caricinus
(21)Thyridolepis mitchelliana
(22)Eragrostis xerophila
60
54
42
40
36
23
20
13
9
8
8
7
7
6
5
3
3
3
2
2
2
—
30
66
24
54
—
—
11
16
8
20
—
—
—
—
—
4
—
—
21
—
3
7
4
1
3
1
4
4
5
1
3
3
3
3
5
5
5
1
2
3
3
5
4
4
2
3
2
5
2
1
5
3
2
2
1
1
5
3
3
5
3
3
2
3
3
2
3
5
3
5
5
5
5
3
3
1
3
3
5
3
5
1
1
5
3
5
5
5
5
3
1
1
5
5
3
3
3
1
3
3
3
3
3
3
1
3
1
5
1
5
1
5
5
3
1
3
3
3
1
3
3
3
3
3
3
1
3
3
3
3
3
1
SLA, specific leaf area.
reflects the overall size of a plant. Height was
determined as the maximum height of the basal
leaves (that is, excluding culms).
Very little is known about the functional attributes of these (or any other) species, and for a
number of the attributes it was difficult to place
some species with confidence into a particular class.
In these cases, we had to resort to informed guesses
based on what was known about the species. The
values given are likely ranges for different kinds of
species in this savanna, and the example serves the
purpose of illustrating how functional attribute
diversity might be measured and used to examine
the structure of ecosystems.
The final set of five attribute values for the 22
grass/sedge species is presented in Table 3, and the
matrix of ecological distances [using Eq. (1b)] for all
22 species is presented in Table 4.
TEST 1: THE LIGHTLY
GRAZED COMMUNITY
Our hypotheses concerning the role of dominant
and minor species in maintaining functional diver-
Ecosystem Function and Plant Attribute Diversity
Table 4.
103
Ecological Distances Between Species
Figure 2. Frequencies of
ecological distances for all
species pairs, taken from
Table 4. Groupings reflect
apparent clusters of frequent ecological distances
(black, stippled, striped, or
white bars); the lower the
ecological distance, the
more functionally similar
are the two species.
sity and resilience in ecosystems leads to certain
predictions regarding species relationships and ecological distances within an unperturbed system. In
particular, we would expect that
1. Dominant species would be functionally dissimilar to each other (as it would be the differences
in functional ‘‘niches’’ that would allow these
species to be codominant in a system) and, conversely,
2. Functionally similar species would be separated
in rank—that is, those species most functionally
similar to dominant species would be found among
the tail-end (minor) species.
But which ecological distances could be categorized as being functionally similar, and what ecologi-
cal distance would two species have to exceed to
be considered functionally dissimilar? Figure 2
shows the histogram of ecological distances taken
from Table 4. The average ED for all species pairs
in the community is 18. Based on apparent groupings, we have divided the histogram into four
categories of relatedness. Thus, functionally similar
species are taken to be those whose EDs are # 6. The
next clustering of EDs occurs for 8 # ED # 14, and
so on. Other categorizations were possible—for
instance, one can subdivide the above grouping and
identify a clump for 8 # ED # 10 and another for
12 # ED # 14—but for our purposes fewer large
categories were more useful than several small
categories.
104
B. Walker and others
Table 5. Ecological Distances Between the Dominant Species (Five Most Abundant Species
in the Lightly Grazed Community)
Tripogon loliiformis
Enneapogon polyphyllus
Fimbristylis dichotoma
Aristida latifolia
Aristida Contorta
Tripogon Loliiformis
Enneapogon Polyphyllus
Fimbristylis Dichotoma
34
33
42
4
—
13
12
30
—
—
21
37
—
—
—
38
Therefore, from Figure 2, we have
Functionally
similar
Similar to
average
Average to
dissimilar
Functionally
dissimilar
0 $ ED # 6
12% of all pair-wise
comparisons
7 # ED # 14 37% of all pair-wise
comparisons
16 # ED # 30 38% of all pair-wise
comparisons
ED $ 33
14% of all pair-wise
comparisons
Note that for two species to have an ED 5 6, they
can, from Eq. (1b), differ by at most 1 unit for each
of the five attributes, or 2 units for one attribute and
1 unit for two attributes (being equal in two other
attributes). Note also that if we had chosen more
than five attributes for classification, our threshold
value of ecological distance for similar species may
have exceeded 6. If, for instance, we had chosen 10
attributes for classification, we might have found
that functionally similar species had ED , 12.
Consider hypothesis 1 above: Are the dominant
species functionally dissimilar? The top five species
account for two-thirds of the relative abundances of
the graminoid species in this system (Aristida contorta to A. latifolia in Table 3). If we consider only the
ecological distances between these species (shown
in Table 5), we find that, of the 10 possible EDs, 50%
can be categorized as being ‘‘functionally dissimilar’’
(ED $ 33). In contrast, only 14% of the EDs among
the full complement of 22 species (Table 4) are
greater than 33. Thus, the expectation for functional dissimilarity among the top five species based
on the average ecological distance in the community would be 1 or 2 $ 33, rather than the five
observed. Using a x2 test, the probabilities of obtaining the observed five EDs $ 33 are either just over
10% (for expected 5 2) or less than 1% (for
expected 5 1). Moreover, though not statistically
significant, 70% of the EDs are more dissimilar than
the community average of 18, compared with 44%
of the EDs in the full community. Thus, the dominant species are more dissimilar than one would
expect given the average ecological distances present in the community.
Figure 3. Functional similarities between dominant and
minor species. See the text for an explanation of the
grouping procedure.
In addition, we predict (from hypothesis 2 above)
that functionally similar species are more likely to
be widely separated in rank (as determined by
abundance). Consider Figure 3, which again shows
the rank–abundance curve for the lightly grazed
community, as in Figure 1. In this figure, however,
species are grouped by ecological distance. For
instance, the highest ranking species (no. 1: A.
contorta) has two functionally similar species (ED #
6)—A. latifolia (rank 5) and Eragrostis microcarpa
(rank 9). All three species are thus labeled A. [Note
that A. latifolia and E. microcarpa are in the ‘‘similar
to average’’ category in regard to each other (ED 5
9, Table 4). The comparison here is between each of
them and the most dominant species, A. contorta.)
Similarly, the third-ranked species, Enneapogon polyphyllus, is functionally similar to the least-abundant
species in the lightly grazed community, Thyridolepis
mitchelliana. These two species are grouped together
and labeled B. Continuing in this fashion for the top
10 dominants, we get the pattern shown in Figure 3.
(Note that once a species is assigned to a group—A,
B, C, and so on—it is not considered for membership in another group.)
Of the species falling in the top half of the
rank–abundance curve, three have no functionally
similar species [Tripogon loliiformis (no. 2), Fimbristylis dichotoma (no. 4), and Chloris pectinata (no. 8)].
Four have functionally similar counterparts in the
Ecosystem Function and Plant Attribute Diversity
minor, tail-end species (groups B, C, D, and E).
Three are functionally similar to each other (group
A); note, however, that although E. microcarpa (no.
9) is in the top half, it is minor relative to the
dominant A. contorta (no. 1). Thus, we do find
evidence for significant functional similarity between dominant and minor species in the lightly
grazed community.
Other functionally similar species pairs are not
represented in Figure 3. For instance, the minor
species Monachather paradoxa (no. 18), Amphipogon
caricinus (no. 20), and T. mitchelliana (no. 21) are all
functionally similar to another minor species, Austrochloris dicanthioides (no. 15). According to the second
part of our hypothesis (which we test in the following section), A. dicanthioides could increase in abundance if a disturbance caused its functionally similar
dominant species, Digitaria brownii (both labeled D
in Figure 3), to decrease in abundance. Then M.
paradoxa, Amphipogon caricinus, and T. mitchelliana
would provide the ‘‘reservoir of resilience’’ for the
now dominant Austrochloris dicanthioides. This suggests that maintaining resilience in ecosystems might
not only require that there be functional similarity
between dominant and minor species, but that
there be functional similarity among minor species
as well, so that resilience is maintained in the face of
further perturbations and shifts in abundance. We
return later to the question of ‘‘ideal’’ community
distributions for ecological distances and functional
similarities or dissimilarities.
Taking the same approach to creating Figure 3,
but with a different definition of ‘‘functionally similar’’ (ED # 14, thus incorporating the first two
groupings in Figure 2), produces qualitatively similar results. In the interest of space, we do not show
the figure here, but in this case all of the species
falling in the top half of the abundance curve have
functionally similar species falling into four possible
categories (A–D), and the functionally similar species in groups A, C, and D span the two halves of the
curve. It is only those species in group B (that is,
those species functionally similar to the secondrank species Tripogon loliiformis) that do not have
counterparts in the tail of the rank–abundance
curve, but Chloris pectinata (no. 8) is functionally
similar to T. loliiformis and could be considered
minor relative to T. loliiformis.
We conclude from these tests that the distribution
of EDs in the lightly grazed community lends support to our hypothesis. The dominant species are
responsible for function, and they are functionally
dissimilar from one another. The minor species
provide resilience in the system—they are functionally similar to dominant species and could increase
105
in abundance and maintain function if dominant
species were to decline or disappear.
TEST 2: A COMPARISON OF THE HEAVILY
GRAZED AND LIGHTLY GRAZED
COMMUNITIES
Our hypothesis goes beyond predictions of the
distribution of ecological distances within a community. In particular, we would predict that the loss or
decline of a dominant species would lead to a
compensatory increase in abundance of a functionally similar minor species. Thus, we examine differences in abundances and species composition between the lightly grazed (relatively unperturbed site
above) and a previously similar community that has
experienced intensive grazing, and determine
whether a species decline under heavy grazing is
accompanied by an abundance increase in a functionally similar species. Due to inherent site differences, the two communities are unlikely to have
been identical prior to grazing by livestock, so we
cannot expect a perfect fit with the hypothesis;
nonetheless, we seek evidence that minor species
are contributing to a compensatory functional response in the system under grazing stresses.
Analyzing this dynamic first requires that we are
able to identify which species have undergone a
‘‘significant’’ decline in abundance and which have
exhibited a ‘‘significant’’ increase. If we fit an exponential to the scaled (that is, sum to 100%) rank–
abundance data in Table 1 (lightly grazed community), we find that, for the nth-ranked species, the
abundance is approximated by
A(n) 5 A(dominant) Exp [20.19(n 2 1)]
where A(dominant) is the scaled relative abundance of the dominant species, Aristida contorta. A
shift in rank of 5, therefore, would correspond
approximately to an increase or decrease in abundance of a factor e [5 Exp(1)]. Therefore, we (rather
arbitrarily) take as our measure of significance a
shift in abundance that would increase or decrease
rank by five steps (if all other species were to
maintain the same relative abundance)—in other
words, a significant increase in abundance requires
Ln[lightly grazed abundance 4 heavily grazed abundance] .1, and a significant decrease requires
Ln[lightly grazed abundance 4 heavily grazed abundance] , 21.
There are 10 grass species that disappear in the
heavily grazed community relative to the lightly
grazed community (Table 1) and thus are considered to show significant decreases in abundance
(though, as previously mentioned, some of them
106
B. Walker and others
Table 6. Significant Shifts in Species Abundances
Between the Lightly Grazed and Heavily
Grazed Sites
Species Showing
Significant Decrease
in Abundance Due
to Heavy Grazing
Species Showing
Significant Increase
in Abundance Due
to Heavy Grazing
Aristida latifolia
Themeda triandra
Panicum effusum
Sporobolus actinocladus
Digitaria ammophila
Dichanthium sericeum
Austrochloris dicanthioides
Eragrostis basedownii
Monachather paradoxa
Amphipogon caricinus
Eriachne pulchella
Eragrostis dielsii
Eragrostis xerophila
Table 7. Functional Similarities Between
Decreasing and Increasing Species
Species with
Increased
Abundance
Under Heavy
Grazing
Functionally Similar
Species Showing
Decline in Abundance
Under Heavy Grazing
Ecological
Distance
Between
Species
Eriachne pulchella
Eragrostis basedownii
2
Eragrostis dielsii
Panicum effusum
Sporobolus actinocladus
Eragrostis basedownii
5
5
6
Eragrostis xerophila
Aristida latifolia
Themeda triandra
Amphipogon caricinus
0
5
3
may not have been present in the original lightly
grazed community). No other species meet the
aforementioned requirements for significant decrease. Three grass species that show a significant
increase in abundance are listed in Table 6.
Our hypothesis would suggest that the species
undergoing an increase in abundance under heavy
grazing should be functionally similar to at least one
species undergoing a decrease. Are those functional
similarities evident? Table 7 shows that each of the
three species that increase in abundance is functionally similar (ED # 6) to at least one species that
disappears under heavy grazing. Moreover, the sum
of the minimum ecological distances for each of the
three species—as measured from those species that
decline in abundance—is only 7.
Perhaps, however, this appearance of functional
similarity is only coincidental. If we were to ran-
domly select 13 species from the full complement of
22 grass/sedge species and designate 10 as decreasing in abundance (high to low, or H–L) and the
remaining 3 as increasing in abundance (low to
high, or L–H), would we find equally low ecological
distances (Table 4)? We randomly generated 1000
such species collections and calculated the ecological distance between each L–H species and the most
functionally similar H–L species. Of the 1000 communities so generated, 27% had all three minimum
EDs fall in the ‘‘functionally similar’’ category (that
is, ED # 6). Only 5% of the communities, however,
had a sum of the three minimum EDs that was less
than 7 (the sum given in Table 4 for the actual
community).
Note again that this result holds even if we change
our definition of ‘‘functionally similar’’ to include all
species pairs with ED # 14. We would still find that
the functional similarities among species that shift
in abundance in the heavily grazed and lightly
grazed communities are closer than would be expected—given the existing distribution of EDs in the
community—if such abundance shifts were random, or appeared random because they were being
driven by mechanisms other than functional similarity and competitive exclusion.
Taken together, the foregoing results provide
supporting evidence that functionally similar minor
species in our rangeland site were able to increase in
abundance and thus maintain some function in the
ecosystem under changing conditions, when their
dominant counterparts declined in abundance. But
can we provide a further test? Given that we know
which 10 species disappeared from the system
under heavy grazing, can we predict which species
should increase in abundance?
TEST 3: PREDICTING WHICH SPECIES
SHOULD INCREASE IN RESPONSE
TO DISTURBANCE
The species we select should be (a) functionally
similar to a disappearing species and (b) significantly
less abundant in the lightly grazed system than the
disappearing species (so that it qualifies as being a
‘‘minor’’ species relative to a ‘‘dominant’’ species).
Thus, for each species that disappears under heavy
grazing, we identify the species that have ED # 6,
and A(UG)minor , A(UG)dominant/Exp(1); we hypothesize that the species meeting these criteria are
likely to increase in abundance under heavy grazing
after the demise of their functionally similar dominant counterparts.
Table 8 identifies each of these species. Three
species emerge as likely to increase in abundance
Ecosystem Function and Plant Attribute Diversity
107
Table 8. Method for Predicting Which Species Should Increase in Abundance Under Heavy Grazing
when ‘‘Functionally Similar’’ Is Defined as Ecological Distance I6
Species that Disappear
Under Heavy Grazing
All Functionally Similar Species
(Ecological Distance in Parentheses)
Are Functionally Similar
Species Significantly
Lower in Abundance?
Species that Should
Increase in Abundance
Under Heavy Grazing
Aristida latifolia
E. xerophila (0)
T. triandra (5)
A. caricinus (3)
Yes
No
Yes
E. xerophila
A. latifolia (5)
A. caricinus (6)
E. xerophila (5)
No
Yes
Yes
S. actinocladus (0)
E. dielsii (5)
E. microcarpa (5)
No
Yes
No
P. effusum (0)
E. microcarpa (5)
E. dielsii (5)
No
No
Yes
Digitaria ammophila
D. brownii (1)
A. dicanthioides (5)
No
No
Dichanthium sericeum
A. dicanthioides (4)
No
Austrochloris dicanthioides
D. sericeum (4)
D. brownii (4)
D. ammophila (5)
M. paradoxa (4)
A. caricinus (5)
No
No
No
No
No
Eragrostis basedownii
E. pulchella (2)
E. dielsii (6)
No
No
Monachather paradoxa
A. dicanthioides (4)
No
Amphipogon caricinus
A. dicanthioides (5)
T. triandra (6)
A. latifolia (3)
E. xerophila (3)
No
No
No
Yes
Themeda triandra
Panicum effusum
Sporobolus actinocladus
A. caricinus
A. caricinus
E. xerophila
E. dielsii
E. dielsii
E. xerophila
See Table 1 for genus names.
under heavy grazing: Amphipogon caricinus, Eragrostis xerophila, and Eragrostis dielsii. The latter two
actually do increase in abundance; the first disappears under heavy grazing. Two other species—
Thyridolepis mitchelliana and Tragus australiensis—
increase in relative abundance, but not significantly
by our arbitrary definition. If we regarded a shift in
abundance rank of 4 as significant, then T.
mitchelliana would be just on ‘‘significance.’’ Tragus
australiensis changes only three rank positions. (Note
that the use of the changes in rank to indicate
significance of relative abundance requires use of
scaled, relative values). In addition, Eriachne pulchella does increase in abundance under heavy
grazing, though we fail to predict its increase in
Table 8. Eriachne pulchella is functionally similar to
Eragrostis basedownii, but the abundance differences
in the lightly grazed system are not such that one
would expect a significant increase in E. pulchella
after the disappearance of E. basedownii. If E. basedownii were the functionally similar and functionally
superior species resulting in a competitive suppression (and thus low abundance) for E. pulchella in the
lightly grazed system, then one would expect higher
abundances for E. basedownii than for E. pulchella in
the lightly grazed system; the opposite pattern is
observed.
Note that, for a number of reasons, we would not
expect this approach to provide perfect predictions
for abundance shifts under heavy grazing. We pre-
108
B. Walker and others
dict, for instance, that Amphipogon caricinus should
increase in abundance because its functionally similar dominants—Aristida latifolia and Themeda triandra—decrease in abundance under heavy grazing.
We do not, however, consider potential competitive
suppression by other remaining dominant species.
In particular, Amphipogon caricinus is similar to Aristida contorta (ED 5 7); A. contorta may be functionally suppressing A. caricinus and preventing its competitive release even after the loss of A. latifolia and
T. triandra. Greater predictive power for shifts in
abundance would require a more sophisticated understanding of the relationship between functional
similarity and competitive exclusion than we have
been able to develop here. In addition, factors other
than interspecific competition can result in low
abundance or compensatory increases under perturbations. Here we seek only to test the hypothesis
that both functional similarities and functional differences will play important roles in community
response to perturbation; future improvements in
methodology would serve to increase predictive
power.
Finally, note that not all species that disappear
under heavy grazing have functionally similar minor species that can take over their role (Table 8).
Thus, although there will be some maintenance of
system function, this functional substitutability will
not be perfect; we would therefore expect some
decline in function in the system under heavy
grazing.
To test the robustness of these results, we can
again repeat the preceding analysis by using the
more generous definition of functionally similar;
that is, by defining as functionally similar those
species with ED # 14. In this case, a slight modification to the approach is required. Note that in Table 8
there were never more than two species that
emerged as being ‘‘likely to increase’’ under the
decline of a single species (for example, Eragrostis
xerophila and Amphipogon caricinus were both predicted to increase in response to the decline in
Aristida latifolia, but there was never a case where
three or more species were affected by the decline of
a single species). If, however, we adopt the more
generous definition of functionally similar (ED #
14), seven species emerge as being both functionally
similar to, and significantly less abundant than, A.
latifolia (Table 9). Although the competitive release
of two species given a decline in one seems plausible, the competitive release of seven species given
the loss of one seems less plausible. Thus, for each
species that declined in abundance (as given in Table
6), we first identified those species that were both
functionally similar and significantly less abundant.
We then hypothesized that the most similar species
from this list was likely to increase in abundance
to fill the functional niche abandoned by its dominant counterpart. The remaining species were only
assumed to increase in abundance if they were
functionally dissimilar to this ‘‘new’’ dominant;
otherwise, they were assumed to be competitively suppressed—due to functional similarity—
by this new dominant. The details are listed in
Table 9.
We predict that Amphipogon caricinus, Eragrostis
xerophila, Eragrostis dielsii, and Thyridolepis mitchelliana
should increase in abundance, similar to the results
when using the more restrictive definition of functional similarity, but with the addition of T.
mitchelliana (which would have been included in
the more restrictive set had we used a change in
rank of 4 rather than 5 to indicate a significant
change). Thus, at least in this case, the results are
fairly insensitive to the exact threshold used to
define functional similarity. Note, however, that the
predictions for which species should increase in
abundance upon the loss of a single species vary
between the two approaches. For instance, using
Table 8, we would predict that the loss of Aristida
latifolia would lead to increases in abundance for
both E. xerophila and A. caricinus; using Table 9, we
would predict increases for only E. xerophila. More
extensive datasets with different patterns of species
losses among sites would aid us in further testing
this hypothesis and determining the ‘‘appropriate’’
threshold for functional similarity.
Overall, both tests we used support the proposition that the minor species contain functional analogues of the dominants, able to increase when the
dominants declined in abundance. Depending on
the test, two of three or three of the four species
predicted to increase in abundance in the heavily
grazed site did in fact do so. Our analysis therefore
provides some evidence that minor species in ecosystems do provide a ‘‘reservoir of resilience’’ through
their functional similarity to dominant species and
their ability to increase in abundance and thus
maintain function under ecosystem perturbation or
stress.
COMMUNITY-BASED MEASURES
OF DIVERSITY AND PERFORMANCE
Most studies on diversity–function relationships
have attempted to examine the effects of increasing
diversity on function. Our hypothesis supports the
contention that, under a constant set of biogeoclimatic conditions, an increase in functional diversity
among the dominant species will correlate with
Ecosystem Function and Plant Attribute Diversity
109
Table 9. Method for Predicting Which Species Should Increase in Abundance Under Heavy Grazing when
‘‘Functionally Similar’’ Is Defined as Ecological Distance (ED) I14
All Functionally Similar and
Significantly Less Abundant
Species (Ecological Distance
in Parentheses)
Functionally Similar to Species
with Lowest ED from Column 2
(Shown with *)?
Species Predicted
to Increase Under
Heavy Grazing
Aristida latifolia
E. xerophila (0)
A. caricinus (3)
P. effusum (14)
S. actinocladus (14)
D. sericeum (14)
A. dicanthioides (10)
M. paradoxa (10)
*
Yes
Yes
Yes
Yes
Yes
Yes
E. xerophila
Themeda triandra
E. xerophila (5)
A. caricinus (6)
P. effusum (9)
S. actinocladus (9)
A. dicanthioides (9)
M. paradoxa (9)
D. sericeum (13)
E. microcarpa (14)
*
Yes
Yes
Yes
Yes
Yes
Yes
E. xerophila
Panicum effusum
E. dielsii (5)
T. mitchelliana (13)
E. xerophila (14)
*
Yes
No
E. dielsii
E. dielsii (5)
T. mitchelliana (13)
E. xerophila (14)
*
Yes
No
E. dielsii
Digitaria ammophila
T. mitchelliana (10)
A. caricinus (12)
*
No
T. mitchelliana
A. caricinus
Dichanthium sericeum
E. dielsii (9)
T. mitchelliana (9)
A. caricinus (9)
*
*
*
E. dielsii
T. mitchelliana
A. caricinus
Austrochloris dicanthioides
E. xerophila (10)
*
E. xerophila
Monachather paradoxa
E. xerophila (10)
*
E. xerophila
Amphipogon caricinus
E. xerophila (3)
*
E. xerophila
Species that Disappear
Under Heavy Grazing
Sporobolus actinocladus
E. xerophila
E. xerophila
Eragrostis basedownii
See Table 1 for genus names.
increased provision of certain functions in ecosystems (such as primary production).
If, however, the set of ‘‘functions of interest’’ is
expanded to include resilience—or the ability of a
system to maintain function under changing conditions—then it is not functional diversity but rather
functional redundancy or substitutability that maintains the function of resilience.
These dual requirements—for diversity to maintain current function and redundancy to maintain
future function—suggest that one measure of diver-
sity is unlikely to capture the important functional
features of an ecosystem. We simultaneously require measures for functional diversity among dominant guilds or species, functional redundancy between dominant and minor species, and functional
redundancy among minor species. Note that increasing both functional diversity and functional redundancy in ecosystems requires adding additional
species, but species number as a measure of functional contribution is inadequate to capture the dual
requirements of diversity and redundancy. Even the
110
B. Walker and others
Table 10. Comparison of Phylogenetic and Functional Diversity Along the Grazing Gradient from Heavy
(1, near a Water Point) to Very Light (5)
Site
Site
Phylogenetic Index
1
2
3
4
5
Functional Index
Species richness (no. of
species)
a Diversity
Simpsons index
12
13
16
15
21
No. of unique com12
12
15
15
19
binations (FAD1)
S distances apart in
functional attribute
space (FAD2)
Total a
36.0 40.8 47.2 45.9 65.3
0.54 0.52 0.39 0.44 0.31
Standardized by no.
of interspecies
comparisons b
s
C5
0.14
0.20
0.14
0.13
0.10
2.16
1.84
2.19
2.26
2.53
ni(ni 2 1)
o N(N 2 1)
i51
Shannon-Weaver index
1
2
3
4
5
s
H8 5 2
o r ln r
i
i
i51
FAD, functional attribute diversity.
aEquation 1a has been used.
bThe maximum possible sum of distances has been roughly approximated.
functional attribute diversity measures we have
suggested (FAD1 and FAD2) fail to capture the
distributions of ecological distances in ecosystems in
ways that would elucidate the presence of both
functional diversity and functional redundancy. Table
10 presents a summary analysis of community
diversity along the grazing gradient, according to
conventional species indices and analogous FAD
measures. The trends are similar, but the interpretation is very limited. The decline in the standardized
FAD2 from site 1 to site 5 reflects decreased average
distances apart in attribute space and therefore
increased similarity in attributes between species.
This is in line with the expected increase in redundancy at site 5 but, as Figure 2 clearly illustrates, the
average distance has very little significance. Therefore, although we are able to develop single indices
of functional diversity, they suffer from the same
drawbacks of all such indices.
The histogram in Figure 3 may provide a measure
of both functional diversity and redundancy. But
note that there is no a priori definition of ‘‘ideal’’
levels of diversity and/or redundancy in ecosystems. We may find that ecosystems that have been
subjected to relatively low biogeoclimatic variability
over evolutionary time scales show greater functional diversity and less functional redundancy,
whereas ecosystems subjected to greater biogeoclimatic variability might exhibit more functional
redundancy than diversity. Therefore, there is no
one pattern for the distribution of functional diversity or redundancy that we should expect or desire
in ecosystems, and no preexisting expectation of
how a histogram like that in Figure 3 ‘‘should’’ look.
This also suggests that no one general pattern will
emerge for diversity–function relationships in ecosystems, particularly as many of the published
relationships tend to examine the system under a
particular set of conditions and thus miss the potentially important role of functional redundancy and
resilience.
The diversity–function debate needs to be expanded to include assessment of these complementary and, in some cases, competing roles for functional types in ecosystems, and assessments of the
positive influences of increased diversity need to be
accompanied by assessments of the positive influences of redundancy in maintaining ‘‘latent functionality,’’ or resilience, in systems. Observations of the
importance of functional redundancy in maintaining ecosystem function have, of course, been made
elsewhere, but these observations have yet to manifest themselves in the diversity–function debate in
any systematic way.
DISCUSSION
The tests of the various hypotheses relating to
ecological distances among species all lend support
to the proposition that minor species in ecological
communities confer resilience in terms of ecosystem
function. [It should be noted that we take resilience
to mean the persistence of function, or the capacity
for function to be restored after major change,
rather than just the rate of return following a minor
perturbation (cf. Ludwig and others 1997)]. The
Ecosystem Function and Plant Attribute Diversity
ability of these minor species to increase in abundance in response to a decrease in their functionally
equivalent, dominant counterparts enables the
maintenance of ecosystem function under stress or
disturbance. Of course, this is but a single test of the
overall proposition, and further investigations of
this kind are needed. They would greatly add to our
understanding of the relationships between biodiversity and ecosystem function, and would provide the
basis for the theoretical framework needed to apply
the insights gained from such studies to the understanding and management of other ecosystems. The
approach adopted in this study, and our attempts at
defining, measuring, and analyzing functional attributes, raise a number of conceptual and methodological issues. A few of these are discussed next.
We have used a set of available data for the
purpose of setting out and exploring the proposition, and it has served the purpose. Before developing the approach further, however, the choice of
variables and the measures we have used must be
addressed in more detail. In particular, the choice of
an abundance measurement for the species (the
combined relative abundance measure we have
used is not without problems), the choice of functional attributes, their definition, and how best to
estimate them in a standardized way are all subject
to debate. There is a need for ease of measurement
and repeatability [the same arguments as in Westoby’s (1998) criteria for the PESS attributes] if functional diversity analysis is to become widely used.
One particular aspect of the choice of ecological
separation concerns the use of ecological distance
(as used in this study) versus the use of minimum
distance along one axis. It is possible that resilience
is maintained in ecosystems not by each dominant
species having one or two functionally similar minor counterparts, but by having several, with each
minor counterpart similar with respect to only one
or two attributes or functions. Again, understanding
the patterns of functional compensation and abundance shifts under changing conditions will require
more data and a greater range of conditions than we
have here.
Assuming the measurement issues can be resolved (and we are confident they can be), a
number of theoretical issues arise. One of these
concerns the argument that diversity measures based
on a phylogenetic classification capture all of the
important, heritable differences in plant attributes
[for example, see Williams and others (1997)]. Such
a proposition is initially appealing, given the present
lack of data on functional attributes. However,
while the phylogeny may well capture different
traits in a species, unless the traits can be individu-
111
ally identified it is not possible to get a mechanistic
understanding of the relationship between biodiversity and ecosystem function. The sort of predictive
understanding that emerges from our analysis of
functional distances cannot be derived from a phylogenetic classification. The similarity in patterns of
overall trends in the phylogenetic and FAD indices
in Table 10 lends support to the argument of
Williams and colleagues (1997), but we contend
that neither kind of index provides much insight.
Only through the use of a functional analysis of the
sort outlined in this report can we develop a predictive understanding of the relationships between
biodiversity and ecosystem function.
A second, interesting consideration arises out of
the similarity in the pattern of occurrences of
ecological distances in Figure 2, and the pattern
obtained by Holling (1992) for his data on the
body-mass difference index for various groups of
animals. Holling’s interpretation centered on the
influence of a few structuring processes interacting
across scales, resulting in this ‘‘lumpy’’ distribution.
The significance of scale effects on ecological resilience is further developed by Peterson and others
(1998), who propose that resilience is generated by
having diverse, but overlapping, function within a
scale and by ‘‘apparently redundant species that
operate at different scales, thereby reinforcing function across scales.’’ Our interpretation of the Australian rangeland data is that the resilience is generated
by having, within each functional type, a number of
species with a diversity of environmental response
capabilities. It may be that one dimension of this
response capacity relates to differences in space and
time scales of response (for example, dispersal distances and rates of regeneration), but the most
significant component of diversity in our case (related to the dominance of grazing as an environmental pressure) involves the diversity of responses to
being defoliated. In a general sense, it seems most
likely that resilience in communities is generated by
a diversity of response capabilities, and that these
response capabilities can involve both responses to
different scales of disturbance, as well as different
responses to an environmental disturbance at a
particular scale.
A final theoretical issue arises out of the predictability of the functional attributes portrayed in this
analysis. It raises the question of how such a
complementary functional composition arises. Is it
selected? If each species is selected (in an evolutionary sense) for its survival attributes, how does a
functionally complementary set eventuate? A fortuitous juxtapositioning of such species seems unlikely, given the results of our tests. A possible
112
B. Walker and others
explanation for the pattern lies in an iterative
process—a reciprocal feedback between individual
selection and persistence of ecosystem function,
something like as follows: A particular environmental pattern favors a particular suite of species, and
the dominants among these are sorted out through
performance, resulting in a complementary (rather
than a strongly overlapping, intensely competing)
set. Those that lose out in the competition (and they
would be species that do strongly overlap in performance with dominants) are either eliminated or
relegated to minor species status. If an environmental change leads to a decline in a dominant, the
minor species that emerges to replace it is one that
can both thrive under the new environmental
conditions and also complement the performance of
the remaining dominants. A complementary pattern of functional attributes is therefore favored,
leading to persistence of the existing levels of function. The continuous interplay between ecosystem
form and function, between the players and the
performance, ensures that the nature of the species
composition of a community tends to a combination
of functional diversity and redundancy, as outlined
in this report.
In conclusion, we mentioned in the preceding
section that community-based measures of functional diversity/redundancy raise the question of
how much of each (redundancy and diversity)
might or should be expected. Norms of this kind will
only emerge from comparisons of many sites across
a wide range of environmental and management
conditions. Questions such as how many and what
kinds of attributes are needed, how ‘‘full’’ the attribute space is or should be, and overall patterns in
the tables of species by attributes, can (for example)
be addressed through the techniques of ordination
and will be worth pursuing in further development
of this approach, within and between sites. The next
step is to assemble a set of comparative datasets
from different ecosystem types.
ACKNOWLE D G M E N T S
We thank NASA and NERC UK for supporting our
participation in the workshop that gave rise to this
report (Biodiversity and Ecosystem Processes: Theory and
Modelling, cosponsored by Diversitas, GCTE, NASA,
& TERI, Imperial College, Silwood Park, United
Kingdom, in June 1997), and Prof. H. H. Shugart
and the Department of Environmental Sciences at
the University of Virginia, who hosted Brian Walker
for the period during which the first draft of this
report was written. We are indebted to Jill Landsberg and Craig James for use of data from their
rangeland study. We also thank Tom Smith and
Steve Pacala for useful discussion on the topic of
functional attributes, Mike Austin for comments on
the measurement of ecological distance, and C. S.
Holling and an anonymous referee for valuable
suggestions.
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