Journal of Vegetation Science 10: 621-630, 1999

IAVS; Opulus Press Uppsala. Printed in Sweden

- Disturbance response in vegetation towards a global perspective on functional traits - 621

Disturbance response in vegetation

towards a global perspective on functional traits

McIntyre, S.1*, Lavorel, S.2, Landsberg, J.3 & Forbes, T.D.A.4

1
CSIRO Division of Tropical Agriculture, Cunningham Laboratory, 306 Carmody Rd, St Lucia, QLD 3067, Australia;
2
Centre dEcologie Fonctionnelle et Evolutive, CNRS UPR 9056, 1919 route de Mende,
F-34293 Montpellier Cedex 5, France;
3
CSIRO Division of Wildlife and Ecology, PO Box 84, Lyneham, ACT 2602, Australia;
4
Texas A&M University, Agricultural Research and Extension Center, Garner Field Road, Uvalde, TX 78801-6205, USA;
*
Author for correspondence; E-mail: sue.mcintyre@tag.csiro.au

Abstract. Previous work on trait correlation patterns has
contributed to the identification of broad patterns of plant
distribution along environmental gradients in vegetation.
However, these general trends may conceal subtle mechanisms
of response that are specific to particular types of disturbance.
To address this, we propose a generic methodology for the
analysis of traits, using herb-dominated vegetation as a model.
Hypothetical biological traits are identified for testing
against disturbance gradients. The traits were selected for their
perceived relevance to disturbance response generally, but
also include a specific focus on domestic livestock grazing.
The analysis is structured hierarchically to enable attributes to
be analysed within major life forms. A different selection of
traits is identified as being relevant to each major life form.
Flexible adaptation in the use of the trait set is suggested as
a way of comparing functional response to disturbance over a
series of locations. For example, assemblages will vary in their
representation of the major life forms, and it may be relevant to
analyse traits within a subset of these life-form groups. Because
individual studies encompass a limited range of environmental
variation, and local floras may be constrained by their evolu-
tionary context, similar approaches need to be tested over a
range of vegetation types and geographic situations. A signifi-
cant advance in functional trait analysis could be achieved if
individual studies provide explicit descriptions of their evolu-
tionary and ecological context from a global perspective.
Keywords: Grassland; Grazing; Herbaceous vegetation; Life-
history trait.
Introduction
Functional classifications are important ecological
frameworks for describing biological traits and the mecha-
nisms that may underlie vegetation response. They have
been used to achieve a range of outcomes: broad-scale
models of global vegetation (Woodward 1987; Prentice
et al. 1992; Steffen et al. 1992); schemes describing
functional responses of a regional flora to environmental
factors (Grime et al. 1988); and schemes addressing
specific disturbances (Noble & Slatyer 1980; Noble &
Gitay 1996). Broad comparisons across a wide range of
biota (e.g. unicells to angiosperms) provide valuable
generality, but can be imprecise and limited in informa-
tion (Duarte et al. 1995), particularly when classifica-
tions have poorly articulated objectives. This is because
functional traits are likely to vary with the function of
interest (Thompson et al. 1996). A method of addressing
this is to define functional types according to specific
ecosystem processes or response to changes in environ-
mental variables (Gitay & Noble 1997; Skarpe 1996).
However, even in the case of disturbance response as a
specified variable, to date there has been identification
of only a few general trends that relate to a small number
of traits (Lavorel et al. 1997).
In further exploring the functional aspects of distur-
bance response globally, we suggest an approach that
will capitalize on current knowledge, but at the same
time attempt to move beyond the relatively ad hoc
approach described in the literature. If there is no func-
tional classification that is widely applicable to a range
of climates, regions, vegetation and disturbance types,
how specific do functional classifications need to be?
We focus on traits underlying disturbance response in
herb-dominated vegetation, i.e. grasslands or the ground
stratum of shrublands and woodlands.
This paper outlines a philosophy and flexible ap-
proach to investigate disturbance response in terms of
functional traits, which can cover a range of environ-
ments and disturbance situations. The basic stages are:
1. Identification of a hypothetical trait list;
2. Description of floristic changes along disturbance gradients;
3. Collection of relevant trait attributes for all species recorded;
4. Statistical testing for correlations of attributes along disturbance
gradients;
5. Synthesis of results of various studies in a global context.
This paper focuses particularly on the development of a
checklist of traits for testing. The role of the compara-
tive synthesis and its implications is further developed
by McIntyre et al. (1999).
622 McIntyre, S. et al.

Rationale of the approach - background Table 1. Checklist of traits that may have functional relevance
to disturbance response in herb-dominated vegetation. Traits
Our goal is to understand how plant traits are related were determined as being potentially (+) or unlikely () rel-
to disturbance response, using an approach that is evant to particular life forms, based on ecological and morpho-
structural-functional, inductive, hierarchical, and which logical considerations, in particular the extent to which at-
tributes tend to vary within a major life form (see text), seen
recognizes the trade-off between imprecise, general
from a global perspective. This is a base list; final life-form
classifications and site-specific descriptions of traits. groups, trait list and attribute classes in a particular study need
The factors that have influenced this methodological to be tailored to the assemblage under study. Examples of
approach are outlined below. qualitative attributes are given in brackets after the trait.
G/S = grass / sedge; Ann = annual; Per = perennial.
The use of structural-functional plant traits
G/S Forb Shrub
Ideally, considerations of ecological function in plants Ann Per Ann Per
would be related directly to purely functional traits such
Life-history traits
as respiration, photosynthesis, competitive ability, Life span +
drought tolerance etc. However, direct measurement of Life-cycle +
these physiological processes can be impractical. This is e.g. biennial, short-lived perennial, perennial
Time to first reproduction + + + +
particularly so in diverse communities where the assem-
blage comprises hundreds of species. An approach ex- Morphological traits
Height (potential height a vegetative stage) + + + + +
plicitly advocated by Box (1996) is the use of structural- Lateral spread (plant diameter) + + + + +
functional traits. These are easily-measured features Above-ground cover density ACD: high/low + + + +
that may act as surrogates for functional patterns. They ACD, plasticity: low/high + + + + +
Habit: e.g. mat, erect, scrambler, twiner) +
include physiognomic and phenological features that Specific Leaf Area (are per unit dry mass) + + + + +
have been shown experimentally to be correlated with Position of dormant buds: +
thero-, geo-, hemi-,crypto-, chamaephyte
the relevant function (in this case, disturbance response). Canopy structure: + + + +
We acknowledge the possibility that structural-func- flat-, erect-, partial-, proto-rosette
tional traits may be inadequate for a satisfactory func-
Grazing-related traits
tional classification. Nonetheless, they represent a prac- Secondary compounds: presence/absence of + + +
tical approach which has yet to be comprehensively e.g. tannins, alkaloids, volatile oils, salt, resins
Hairiness: amount and/or type + + + +
explored, and accepted or rejected. Prickliness: amount and/or type + + +
Tensile strength of leaves: high/low +
An inductive approach Waxes: present/absent +
Sclerophylly: high/low +
The relevance of any particular functional trait can Silification: present/absent +
only be tested in relation to a specific ecosystem func- Stem/leaf ratio: high/low + +
tion in our case the function of interest is response to Leaf thickness/succulence + + +
(absolute or relative measure)
disturbance. The initial selection of functional traits for Leaf width (at widest point) + +
testing is made in the context of the ecological effects of Inflorescence/relative prominence (absolute + +
or relative measure depending on assemblage)
disturbance. Our initial steps of process and trait Position of active buds + +
identification are deductive in the sense of drawing (distance from root to furthest meristem)
from our general understanding of the system. However, Maximum height relative to grazer +
Habit plasticitiy in response to defoliation: + + + +
the critical stage of trait evaluation is inductive, relying high/low
on sets of observations and experimental results (sensu Uprooting potential: high/low +
Woodward & Cramer 1996; Gitay & Noble 1997). Phenological traits
Generalizations about the utility of traits are sought by Leaf phenology: deciduous/evergreen +
analysing the representation of trait attributes (= catego- Seasonality of growth: spring/summer etc. + + + +

ries within traits) over natural, or experimentally ma- Regeneration traits

nipulated, disturbance gradients. Seed size + + + + +
Seed dispersal vector: wind, ants, etc. + + + + +
The result of the deductive stage of the process is the Dormancy: transient, persistent, none + + + + +
list of hypothetical traits (Table 1) gleaned from the Fecundity: high/low + + + + +
literature, and our experience in grasslands, woodlands Length of flowering period + +
Seasonality of germination: + + + +
and shrublands in a range of climates over three conti- e.g. warm season/cool season/plastic
nents. We have listed traits that may have a generic Timing of seed release: + + + +
e.g. spring/summer/autumn
association with disturbance tolerance in these sys- Recruitment frequency: rare/frequent +
tems and have included soil cultivation and small- Vegetative reproduction: present/absent + + +
scale mammal digging in our considerations. However, Resprouting ability: high/low/absent + + + +
 - Disturbance response in vegetation towards a global perspective on functional traits -
our strongest emphasis has been on domestic livestock
grazing and a set of grazing-specific traits has been
identified. This is illustrative of the additional sets of
traits that may need to be tailored for studies involving
distinctively different types of disturbance, e.g. fire.
Hierarchical analysis of traits
A large variety of studies has addressed the relation-
ship between species response to disturbance and their
biological traits. However, review of these shows that
only a few very general trends have emerged (e.g.
disturbance favours annuals and small-statured plants).
Studies have repeatedly identified life-form based clas-
sifications (e.g. annuals and short-lived perennials, per-
ennial forbs, perennial grasses) as being important both
functionally and in terms of describing natural correla-
tions of traits (Lavorel et al. 1997). Although some
studies have subdivided life-form groups to identify
response to particular disturbance types (e.g. palatabil-
ity being used to describe grazing response; Friedel et
al. 1988; Noy-Meir et al. 1989) there is scope to explore
trait response groups in more detail. To this end we propose
a hierarchical screening of traits (Lavorel et al. 1997) in
which vegetation response is initially analysed in terms of
major life forms and their response to disturbance. In a
second stage of analysis of the same data set, trait response
to disturbance is analysed separately within each of the
life forms significantly represented in the vegetation.
A capacity for appropriate generalization
Defining one set of plant functional types for all
purposes and scales of operation is not possible, nor
necessarily desirable (Skarpe 1996). From a theoretical
perspective it is desirable to seek patterns that are likely to
be evident at global scales. Functional classifications
specific to disturbance response, applicable at this scale,
are in demand so that disturbance can be included as a
factor in mechanistic models of vegetation dynamics
under global change (Steffen et al. 1996). Because em-
pirical studies of functional traits have tended to have a
regional or local focus, patterns that may be common to
different vegetation types, disturbance types, and regions
are poorly understood. This situation will be improved by
comparative work being conducted globally, where com-
parable trait data are obtained over a range of regions,
vegetation and disturbance types. To this end, we are
proposing an approach that is pragmatic, and flexible
enough to be adapted to specific locations. Cross-site
comparisons will be largely informal and opportunistic,
and involve progressive grouping of results by region,
vegetation type, disturbance type etc. The identification
of an appropriate ecological context will be crucial to this
synthesis; approaches are discussed in this paper and in
McIntyre & Daz (1999).
623
Fig. 1. Classification of species into major life-form groups
based on divisions into growth-form and life-cycle, resulting in
five terminal and two sub-terminal groups. Shrubs are
phanerophytes with persistent buds > 20 - 30 cm on stems above
the ground (Raunkiaer 1934); forbs, grasses and sedges variously
include therophytes, geophytes, hemicryptophytes and chamae-
phytes. The choice of groups used in trait analyses would be
influenced by the composition of the assemblage under study.
Hypothetical trait list - general considerations
Initial divisions of species into major life forms
The primary division is based on growth form (gras-
ses/sedges, forbs and shrubs) with further subdivisions of
grasses/sedges and forbs into annual and perennial life-
cycles giving a total of five terminal life-form groups
(Fig. 1). The basis of these divisions is that the traits that
define them (growth form, life cycle) tend to be those
that also define functional classifications when all life
forms are analysed as a single group. The first stage of
data analysis would involve examining how the major
life-form groups vary in abundance with disturbance.
Some life-form groups may be not represented in the
assemblage, precluding the group from the first stage
analysis. Other groups, that are only represented by a
few species, may be analysed at life-form level (major
life-form analysis) but traits within the group may not
be analysed (second stage trait analysis see below).
The composition of the plant assemblage under study
strongly influences which life-form groups used in both
the major life form and the trait analyses. For example, in
temperate grasslands, all five terminal life-form groups
are well represented (e.g. McIntyre et al. 1995) while
Lavorel et al. (1999) found perennial species to be virtu-
ally absent from the vegetation samples in mediterranean
grasslands; two groups, annual grasses and forbs (lump-
ing annual and perennial) were subjected to both stages of
analysis. A more complex adaptation of the hierarchy for
understorey species in semi-arid woodlands is shown by
Landsberg et al. (1999). This involved the grouping of
annual and perennial grasses/sedges and the division of
forbs into herbaceous (annual and herbaceous peren-
624 McIntyre, S. et al.
nial) and sub-shrubs (woody perennial). Only those groups
that were well represented (e.g. > 10 species) were sub-
jected to trait analysis.
Examining traits within major life forms
The overall choice of traits to be tested for functional
significance is necessarily pragmatic. Because of the
large numbers of species that may be involved, most
traits should be relatively easy to measure. Parsimony in
the number of traits selected is also important: (1) to put
bounds on trait measurement, and (2) as there are tech-
nical limitations to the number of traits that can be
effectively analysed in proportion to the total number of
species (Kazi-Aoual et al. 1995).
The idea of examining traits within major life forms
is that it enables identification of patterns that might be
obscured by the patterns associated with the major
groups. Some practical outcomes of this approach, in
terms of identifying relevant traits and defining at-
tributes within life-form groups are:
1. Certain traits will be ecologically relevant to only some life forms
(e.g. leaf phenology as defined in Table 1 is relevant only to shrubs).
2. The range of attribute variation for a particular trait may be different
for different life forms (e.g. the range of heights of grasses and forbs
may largely overlap, but be non-overlapping with shrubs).
3. Attributes of some life forms may not vary significantly for a
particular trait (e.g. herbaceous plants have little variation in
sclerophylly compared to shrubs).
Points 1 - 3 should influence the choice of traits consid-
ered relevant to particular life-form groups, and the
definition of attributes relevant to a particular trait/
group combination. All the above considerations have
influenced our choice of traits in Table 1. The degree of
commonality between major life-form groups in the
traits chosen and their attribute definition may influence
how the major life-form groups are defined for a par-
ticular study. For example, we identified more relevant
traits in common between annual and perennial forbs
than between annual and perennial grasses (Table 1) and
therefore suggest that in many studies it would be more
useful to have a single forb group, but to retain the life
cycle-based split within grasses/sedges.
The need for rapid trait measurement means that
some potentially relevant traits have not been included
because of the large effort involved in their measurement
(e.g. growth rate, leaf protein content, population traits).
Table 1 thus represents a compromise list whose traits
are likely to be accessible to many researchers and
which has been pruned to avoid redundancies. Even in
its abbreviated state, we suggest that it be used as a
checklist, to be adapted to the system under study, by
taking into account the species assemblage and the
expertise available. Studies in individual regions will
therefore involve removing, and sometimes adding,
specific traits to the checklist, and refining attributes.
Trait correlations
We have generally avoided the a priori use of syn-
thetic indices. Although some trait correlations are recog-
nized, there is the potential for assumed correlations
(expressed as indices) to conceal relevant mechanisms
and differences between species assemblages with dif-
ferent evolutionary histories. There are also interactions
between traits related to disturbance and other environ-
mental factors (as discussed in later sections relating to
herbivory defence/resource availability and seed size/
growth rates). While acknowledging the occurrence of
trait correlations, constraints to trait expression, and the
difficulties they both pose for data interpretation, we
still view empirical studies as valuable for the investiga-
tion of a wide range of potentially predictive traits.
Hypothetical trait list - the traits
Within each of the groups, the hypothetical traits are
listed under the headings: life history, morphology,
grazing response and regeneration traits (Table 1). These
categories are essentially for convenience. They may
signify general or specific disturbance responses, but
the lists are not mutually exclusive e.g. some of the traits
categorized as morphological may also confer advantages
under grazing (e.g. small stature), while several regen-
eration traits (e.g. dormancy) can be functionally linked
to soil disturbance (Lavorel et al. 1998).
Life-history traits
Life-history type can be a strong indicator of distur-
bance. Annuals or short-lived perennials tend to be
favoured by disturbances that create gaps in vegetation
dominated by a perennial grass matrix (Grubb 1986;
Collins 1987; Belsky 1992; Pettit et al. 1995). The
choice of traits in this category needs to reflect the
choice of major life-from groups used in the trait analy-
sis. Life span and life-cycle are not relevant to annu-
als unless they are grouped with perennials. Because
perennial forbs often have more distinctive life-cycle
patterns than grasses/sedges, specific life-cycle attributes
(Table 1) may be relevant or easier to record. Otherwise
a quantitative measure of life-span could be used.
Morphological traits
In many studies, response to disturbance has been
found to be well correlated with variation in plant mor-
phology. Plant height is often related to response to
disturbance (Gibson 1988; Sala 1988; Belsky 1992; Diaz
et al. 1992) and would be a primary variable to analyse.
Lateral spread gives a further component of plant shape
(Grime et al. 1988; Fernandez-Als et al. 1993) and de-
scribes space occupancy and ability to capture resources
 - Disturbance response in vegetation towards a global perspective on functional traits -
(Epp & Aarssen 1989). While these two measures de-
scribe the above-ground volume of the plant, the density
of the canopy remains undescribed. This is addressed in
a trait describing the degree to which above-ground
biomass fills the projected canopy area, termed above-
ground cover density.
Because the above three measures of plant archi-
tecture are static, it is necessary to capture morphologi-
cal plasticity and two traits are used to that effect. First,
degree of plasticity of above-ground cover density re-
flects changes in plant structure that are expressed under
crowding (e.g. shoot attenuation). The second trait,
habit reflects an ability to respond to competitive
situations and suggested attributes are twiner, erect,
scrambler and mat forms. For species that are plastic in
these attributes (see grazing-related traits), the ungrazed
condition is described. Specific leaf area is a core trait
which is correlated with leaf life-span, photosynthetic
capacity and leaf N-content. Plants scoring high specific
leaf area can respond to flexibly spatial patchiness of
resources (see Westoby 1998; Weiher et al. 1999).
A description of growth form, expressed in terms of
dormant bud position, as developed by Raunkiaer (1934),
encapsulated sets of correlated traits relating to persist-
ence and architecture that are relevant to disturbance
response (McIntyre et al. 1995; Pettit et al. 1995). In the
current scheme, we have captured elements of this classi-
fication at several levels rather than in a single trait. For
example, in the first hierarchical split, phanerophytes
(shrubs) are separated from other growth forms (Fig. 1).
Annuals may be separated into major growth forms or
under life cycle (as described in the previous section).
Within forbs, the trait dormant bud position enables the
remaining major life forms geophyte, hemicryptophyte,
chamaephyte to be discriminated. Perennial grasses
and sedges are generally all hemicryptophytes, making
the trait dormant bud position irrelevant to this group.
In a final trait we have adapted Raunkiaers (1934)
morphological classification of hemicryptophytes, although
here it applies to other life forms in the same way it has
been applied by Grime et al. (1988). Canopy structure
describes the architecture of the ramets of all grasses,
sedges and forbs and is a description of leaf arrangement.
The suggested attributes are erect rosette, flat rosette,
partial rosette and proto-rosette. These are as defined
for hemicryptophytes in McIntyre et al. (1995), although
here applied also to all life forms except shrubs.
Grazing response traits
Grazing is a highly complex disturbance, with both
direct and indirect impacts on plant communities. Direct
impacts include damage to plant parts through herbivory
and trampling, and immediate effects on community physi-
cal structure. This has consequences for competition
625
between the damaged plant and its neighbours. Longer-
term, less direct impacts include changes in community
composition (see Huntly 1991) and perturbation of soil
and water processes, which in turn have consequences for
plant competition and resource availability. The selectiv-
ity of grazers is a further complicating factor. While
preference can be influenced by individual plant traits
(Briske 1996), variability in preference depends on inter-
actions between the grazer and plant community (Dudinski
& Arnold 1973; McNaughton 1984; Grant et al. 1985,
1987; Gordon 1989a, b). Grazer species differ in their
choice of plants. At the level of the individual, the final
selection of plants reflects their preference, modified by
the opportunities available (Hodgson 1979).
Related phenomena are (1) correlations between
traits for persisting under grazing and surviving water
stress (Coughenour 1985; Milchunas et al. 1988); (2)
the incidence of herbivore defence mechanisms and the
availability of resources in the habitat. The latter has
been described in optimal defence (Feeny 1976; Rhoades
& Cates 1976; Fagerstrm et al. 1987) and resource-
availability hypotheses (Bryant et al. 1985; Coley et al.
1985; Herms & Mattson 1992; Tuomi 1992; de Jong
1995). In some environments, evolution may favour
primarily those traits associated with the capture of
resources, and persistence under herbivory may be only
a secondary benefit (Rosenthal & Kotanen 1994). For
example, it is recognized that where resources for growth
are limiting, many species have inherently slow growth
rates and leaf turnover. These are correlated with traits
conferring defence against herbivory e.g. tough, sclero-
phyllous leaves with large amounts of carbon-based
structural and chemical defences.
Despite these complexities, theories about plant per-
sistence under herbivory are often concerned primarily
with the response of plants to the direct impact of defolia-
tion (e.g. Coley et al. 1985; Herms & Mattson 1992;
Rosenthal & Kotanen 1994). In contrast, experimental
work on the composition of grazed communities has
described both direct and indirect impacts of grazing.
These impacts vary with habitat attributes such as land-
scape variation, site productivity, and dominant life forms
(Friedel et al. 1988; Milchunas et al. 1990; McIntyre &
Lavorel 1994; McIntyre et al. 1995). The challenge, in
terms of identifying grazing-response groups, lies with
identifying appropriate elements from both the simplistic
and complex ends of this theoretical continuum (Westoby
1979/1980;Wilson et al. 1988; OConnor 1991).
Clearly, the range of traits potentially relevant to
persistence under grazing is extremely wide. It will also
vary from region to region, and may not be functionally
related to direct herbivore damage. The traits we have
listed as grazing-related are those that have been included
specifically with this disturbance in mind, and merely
626 McIntyre, S. et al.
supplement the wider trait list, which is also relevant to
grazing as a disturbance. As it is possible that trade-offs
between grazing tolerance, defence and plant growth
may not always be found to be consistent, we have
included these traits independently and rely on subse-
quent analyses to reveal correlation patterns.
Persistence under grazing can be considered the net
expression of several traits that in combination allow
plants to persist under a specified grazing regime, by
avoiding damage at critical times, or by tolerating dam-
age sufficiently well to allow regrowth or recruitment.
The major, yet controversial, dichotomy is that of avoid-
ance vs tolerance. Hypotheses differ regarding the extent
to which avoidance and tolerance are seen as mutually
exclusive strategies (Rosenthal & Kotanen 1994).
Avoidance of damage can be achieved through de-
fence or escape. Defence includes traits that act as
deterrents e.g. secondary compounds (Table 1).
Although difficult to measure, information on the
presence of these compounds is generally available.
Other defence traits are structural e.g. hairiness, prick-
liness, waxes, sclerophylly, silification (Table 1).
Allied to the notion of defence is its opposite, attrac-
tiveness or palatability (McClymont 1967). Palatability
as such was not included because it is effectively a
synthetic index which can vary for the same species de-
pending on grazing intensity, biomass and species compo-
sition. Although palatability is difficult to define accurately
in practice, it is possible to identify traits which confer
palatability. These also include chemical composition e.g.
sugars, amino acids, digestible energy (no traits nominated
due to difficulties of measurement) or structural features
e.g. stem/leaf ratio, leaf width (Table 1).
Escape can be achieved in space (relates to abun-
dance, size and shape) and time (relates to phenology
and dormancy). In addition to relevant morphological
and regeneration traits, the grazing traits conferring
ability to escape domestic herbivores are vulnerability
of flowering parts for grasses (infloresecence height/
relative prominence), distance of active buds from the
roots (active bud position), and the height of shrubs
relative to main herbivore grazing for shrubs (height
relative to grazer). Also important is the capacity for
plants to change their morphology in response to
defoliation, e.g. through changing internode length, leaf
size or rosette orientation (plasticity of habit).
Finally, tolerance can be achieved through rapid
vegetative growth or prolific seedling regeneration.
Vegetative growth features include intrinsic growth
rate, number, position and phenology of meristems or
regenerative buds, extent of stored reserves, and devel-
opmental plasticity. Seedling regeneration depends on
the number and position of inflorescences, seed size
and number, dispersal and dormancy strategies, season-
ality of germination and the specificity of germination
requirements. Many of these features are of broader
ecological interest and are captured in the morphologi-
cal and regeneration traits.
Most of the grazing traits are not relevant to annual
grasses as the majority do not have resources to develop
specific defence structures or compounds. The traits
chosen for annual grasses relate to susceptibility to
direct damage by grazing and one trait (uprooting po-
tential) has most relevance to this life form.
Phenology traits
The relationship of species phenology to timing of
disturbance (Hobbs & Mooney 1985; Gross 1987; Lavorel
et al. 1994; Howe 1995) is a potentially important trait
where disturbances are episodic. For shrubs, the trait
refers to leaf phenology which at the simplest level
would discriminate deciduous from evergreen species
(Table 1). Within these types, other patterns of leaf growth
may need to be recorded. For example, among ever-
greens, there might be differentiation between determin-
istic leafing schedules and those that are responsive to
adequate water and temperature conditions.
For annual species, growth is directly linked to
seasonality of germination (see below) and a phenology
trait relating to seasonality of growth would be redun-
dant unless it was used instead of the seasonality of
germination trait. Among perennial herbaceous species
seasonality of growth would need to record the seasons
of potential active growth. This could be recorded
through direct observations, although in some cases, the
use of pre-existing information on photosynthetic path-
ways (C3/C4) may be informative (Rogers 1993).
Regeneration traits
Studies have identified correlations of seed size to
a wide range of adult and juvenile traits including
plant size (Mazer 1989; Leishman et al. 1995), dis-
persal mode (Westoby et al. 1990; Leishman et al.
1995), persistence in the soil (Thompson et al. 1993),
drought tolerance (Jurado & Westoby 1992; Leishman
& Westoby 1994a), shade tolerance (Leishman &
Westoby 1994b; Osunkoya et al. 1994) and defoliation
tolerance (Armstrong & Westoby 1993). One of the
well-established correlations is the negative relation-
ship between seed weight and relative growth rate
(Salisbury 1942; Gross 1984; Shipley & Peters 1990;
Maraon & Grubb 1993). In our inclusion of seed
weight as a regeneration trait, we attempt to capture
this correlation as growth rates are particularly cum-
bersome to measure. On the other hand, trade-offs
between seed size and number, dispersal rate and dor-
mancy vary in a complex manner with environmental
variability (Venable & Brown 1988). Therefore dispersal
 - Disturbance response in vegetation towards a global perspective on functional traits - 627

mode (seed dispersal vector), dormancy and fe-

cundity are considered explicitly (Table 1).
The temporal aspect of the regeneration strategy
determines the response of plants to disturbances. Op-
portunities for seed production and gap colonization are
influenced by duration of the reproductive period (length
of flowering period). Also relevant to colonization and
timing of disturbances are seasonality of germination
and timing of seed release, the latter is not necessarily
related to flowering dates as seeds can be held on the
plant beyond maturity (Chiarello 1989). Traits and at-
tributes will depend on local climate and flora, e.g. in
the Mediterranean region up to five attributes (autumn,
autumn-winter, winter-spring, spring, indifferent) are rel-
evant for germination (Lavorel et al. 1993) while in arid
regions, fewer attributes (warm season, cool season, plas-
tic) may be sufficient (Baskin et al. 1993). For shrubs,
recruitment frequency is considered more useful than
the seasonality of germination trait proposed for herba-
ceous plants (Table 1).
For perennial life forms, resprouting (Noble & Slatyer
1980; Bond et al. 1992) and vegetative reproduction (Grime
1979; McIntyre et al. 1995) may be important in post-
disturbance regeneration. Vegetative reproduction can
Fig. 2. Flow diagram showing idealized stages of research and
contribute to the acquisition of space after disturbance. resulting data and information (enclosed in single line boxes).
Resprouting ability is an important component of Shaded boxes indicate data outputs of individual studies that
disturbance tolerance, particularly for shrubs (Table would be needed for a meaningful comparison and synthesis
1), as disturbance (soil disturbance, grazing, or fire) of of trait results across the globe. Statistical analyses are dis-
increasing intensity tends to favour seeders over cussed in detail in Lavorel et al. (1998).
sprouters (Fahrig et al. 1994; Bullock et al. 1995; Pettit
et al. 1995; Tyler 1995).
Regeneration traits are often inferred to be key fac-
tors in disturbance ecology but tend to be neglected in
trait analyses, possibly because of the effort involved in
their measurement. Our listing of regeneration traits is been measured. The first filter will exclude:
admittedly less pragmatic than other categories due to Traits that cannot be measured for practical reasons;
this perceived importance. Many traits require collections Traits that are known to not vary across the assemblage;
of seeds in quantities that may not be available if Traits that are not considered relevant to the disturbance in question.
fecundity is low. This limitation may be reflected in the It would be appropriate to discriminate between these
final choice of regeneration traits for a particular study. reasons, but in practice, this information is generally not
reported. The second filter will involve deleting:
Traits that were measured but turned out not to vary significantly;
Summary of research stages Traits that could not be recorded for all species (e.g. due to lack of
seed availability);
Traits that were measured but not analysed because the major life-form
Individual studies group to which they belonged did not have enough species for an
The significance of starting with a trait checklist is analysis.
that even when a trait is not used in an analysis, the fact Running parallel to the measurement of traits, is the
that it has been considered is pertinent to a broad over- recording of floristic change in relation to a disturbance
view of a range of individual studies. The steps through gradient or a series of disturbance levels, measured ex-
which traits are considered and subsequently discarded perimentally or in a field situation (Fig. 2). The identifica-
or analysed in a particular study are depicted in Fig. 2. tion of traits correlated with different disturbance levels
The initial trait checklist (Table 1) passes through two is achieved through the merging of the trait and floristic
filters, (1) the selection of traits to be measured; and (2) data sets and their analysis in two stages: first the
the selection of traits to be analysed from those that have response of the major life forms and second the response
628 McIntyre, S. et al.
of traits within the life forms represented by significant
numbers of species. Again these two stages are critical
to the broader synthesis. Where assemblages differ in
their representation of major life forms, comparing the
utility of specific traits may become redundant. Factors
other than the current disturbance regime may determine
the overall vegetation structure; this context is important
to consider alongside the trait interpretations.
Synthesis of individual studies
As individual studies will inevitably sample only a
section of the global environmental and disturbance
gradients, the function of the synthesis will be to fit
individual studies into the global framework for com-
parison of results. Three types of input are required for
this (see shaded boxes in Fig. 2). Trait attributes that are
correlated with particular disturbance levels are rou-
tinely reported in detail in trait studies. Site information
is also given, although not necessarily in enough detail
for a global synthesis. The third form of information is
less often provided, but is equally important - a descrip-
tion of the entire assemblage in terms of the representa-
tion of all the major life forms and the trait attributes.
Ideally this would include the traits considered or meas-
ured, but which did not vary in their attributes and were
not analysed. For a framework in which individual
studies can be compared, see McIntyre et al. (1999).
Conclusion
Any proposal that aims to address a specific, but
complex, habitat variable (disturbance) in the broadest
context (global) will have deficiencies apparent to those
with particular specializations. Grazing as a disturbance
is a case in point. While certain attributes may influence
sensitivity to grazing, in many instances it is not only
the inherent traits of individual plants, but also interac-
tions with other species of plants and herbivores in the
community which determines the impact of grazers.
Many of these processes occur at a scale larger than that
of the individual species and would be overlooked if
only specific traits were evaluated. In proposing that
trait studies be made comparable in the broadest context,
we hope to indirectly address this issue by identifying
the extent to which functional classifications are useful,
and circumstances under which they may have generality.
The proposed scheme aims at gaining a different
perspective on functional classification and providing a
framework that is flexible, yet structured enough to en-
able regional and global comparisons to be made. This
comparison would be a specific exercise that draws from
the array of existing information in which traits are corre-
lated with disturbance responses. The research methodol-
ogy proposed represents a strategy for the collection and
reporting of data that would contribute maximally to
future efforts in the comparison and synthesis of results.
Acknowledgements. This work was supported by a travel
grant from the Australian Bilateral Science and Technology
Program to the first author. It contributes to the IGBP-Global
Change and Terrestrial Ecosystems Core Research Programme
(Task 2.2.1). Thanks to A. Ash, R. Hobbs, T. Grice and I.
Radford for reading earlier drafts of the manuscript.
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Received 17 December 1997;
Revision received 12 June 1998;
Accepted 9 February 1999.