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BIODIVERSITY
REVIEW
Reproductive biology of Australian
acacias: important mediator of
invasiveness?
Michelle R. Gibson
1
*, David M. Richardson
1
, Elizabete Marchante
2
,He
´lia
Marchante
2,3
, James G. Rodger
4
, Graham N. Stone
5
, Margaret Byrne
6
, Andre
´s
Fuentes-Ramı
´rez
7,8
, Nicholas George
9
, Carla Harris
10
, Steven D. Johnson
4
,
Johannes J. Le Roux
1
, Joseph T. Miller
11
, Daniel J. Murphy
12
, Anton Pauw
13
,
Matthew N. Prescott
14
, Elizabeth M. Wandrag
15
and John R. U. Wilson
1,16
1
Centre for Invasion Biology, Department of Botany
and Zoology, Stellenbosch University, Matieland
7602, South Africa,
2
Department of Life Sciences,
Centre for Functional Ecology, University of
Coimbra, Apartado 3046, Coimbra 3001-401,
Portugal,
3
Centre for Studies of Natural Resources,
Environment and Society; Department of
Environment, Escola Superior Agra
´ria de Coimbra,
Bencanta, Coimbra 3040-316, Portugal,
4
Centre for
Invasion Biology, School of Biological and
Conservation Sciences, University of KwaZulu-Natal,
P. Bag X01 Scottsville, Pietermaritzburg 3209, South
Africa,
5
Institute of Evolutionary Biology, University
of Edinburgh, The King’s Buildings, West Mains
Road, Edinburgh EH9 3JT, UK,
6
Science Division,
Department of Environment and Conservation,
Locked Bag 104 Bentley Delivery Centre, Bentley, WA
6983, Australia,
7
Laboratorio de Invasiones
Biolo
´gicas (LIB), Facultad de Ciencias Forestales,
Universidad de Concepcio
´n, Casilla 160-C,
Concepcio
´n, Chile,
8
Instituto de Ecologı
´ay
Biodiversidad (IEB), Santiago, Chile,
9
School of Plant
Biology, Faculty of Natural and Agricultural Sciences,
The University of Western Australia, 35 Stirling
Highway, Crawley, WA 6009, Australia,
10
Plant
Invasion and Restoration Ecology Laboratory,
Department of Biological Sciences, Faculty of Science,
Macquarie University, Sydney, NSW 2109, Australia,
11
Centre for Australian National Biodiversity
Research, GPO Box 1600, CSIRO Plant Industry,
Canberra, ACT 2601, Australia,
12
National
Herbarium of Victoria, Royal Botanic Gardens
Melbourne, Private Bag 2000, Birdwood Avenue,
South Yarra, Vic. 3141, Australia,
13
Department of
Botany and Zoology, Stellenbosch University,
Matieland 7602, South Africa,
14
Department of
Zoology, Oxford University, South Parks Road,
Oxford OX1 3PS, UK,
15
Bio-Protection Research
Centre, Lincoln University, Canterbury 7647, New
Zealand,
16
South African National Biodiversity
Institute, Kirstenbosch National Botanical Gardens,
Claremont 7735, South Africa
*Correspondence: Michelle R. Gibson, Centre for
Invasion Biology, Department of Botany & Zoology,
Stellenbosch University, Matieland 7602, South Africa.
E-mail: mishka.r.g@gmail.com
ABSTRACT
Aim Reproductive traits are important mediators of establishment and spread of
introduced species, both directly and through interactions with other life-history
traits and extrinsic factors. We identify features of the reproductive biology of
Australian acacias associated with invasiveness.
Location Global.
Methods We reviewed the pollination biology, seed biology and alternative
modes of reproduction of Australian acacias using primary literature, online
searches and unpublished data. We used comparative analyses incorporating an
Acacia phylogeny to test for associations between invasiveness and eight
reproductive traits in a group of introduced and invasive (23) and non-invasive
(129) species. We also explore the distribution of groups of trait ‘syndromes’
between invasive and non-invasive species.
Results Reproductive trait data were only available for 126 of 152 introduced
species in our data set, representing 23/23 invasive and 103/129 non-invasive
species. These data suggest that invasives reach reproductive maturity earlier (10/
13 within 2 years vs. 7/26 for non-invasives) and are more commonly able to
resprout (11/21 vs. 13/54), although only time to reproductive maturity was
significant when phylogenetic relationships were controlled for. Our qualitative
survey of the literature suggests that invasive species in general tend to have
generalist pollination systems, prolific seed production, efficient seed dispersal
and the accumulation of large and persistent seed banks that often have fire-,
heat- or disturbance-triggered germination cues.
Conclusions Invasive species respond quicker to disturbance than non-invasive
taxa. Traits found to be significant in our study require more in-depth analysis
involving data for a broader array of species given how little is known of the
reproductive biology of so many taxa in this species-rich genus. Sets of
reproductive traits characteristic of invasive species and a general ability to
reproduce effectively in new locations are widespread in Australian acacias. Unless
there is substantial evidence to the contrary, care should be taken with all
introductions.
Keywords
Biological invasions, breeding system, invasive alien species, pollination,
reproductive syndromes, reproductive traits, seed dispersal
Diversity and Distributions, (Diversity Distrib.) (2011) 17, 911–933
DOI: 10.1111/j.1472-4642.2011.00808.x
ª2011 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/ddi 911
SPECIAL ISSUE:HUMAN-MEDIATED INTRODUCTIONS OF AUSTRALIAN ACACIAS—A GLOBAL EXPERIMENT IN BIOGEOGRAPHY
A Journal of Conservation Biogeography
Diversity and Distributions
INTRODUCTION
A predictive understanding of invasiveness is needed to
manage existing invasive species and for objective screening
of new introductions. Elucidating the determinants of inva-
siveness and understanding how these interact with environ-
mental features and extrinsic factors to mediate invasion
success are fundamental questions in invasion ecology (Rich-
ardson & Pys
ˇek, 2006). Anthropogenic and environmental
factors and various life-history traits, particularly features
associated with reproduction and dispersal (Rejma
´nek et al.,
2005; Thuiller et al., 2006; Pys
ˇek & Richardson, 2007), are
often associated with invasion success (or lack thereof).
Previous studies comparing life-history traits of invasive
species have found several reproductive traits including seed
mass, fecundity (number of seeds produced), dispersal mode
and dispersal ability to be important for overcoming barriers
to invasion in a new environment (Hamilton et al., 2005;
Pys
ˇek & Richardson, 2007; Moravcova
´et al., 2010; Castro-Dı
´ez
et al., 2011). There has, however, been no comprehensive
analysis of the roles of such traits in invasiveness in Australian
acacias, a speciose group of plants containing several invasive
species.
This study assesses the current state of knowledge regarding
associations between reproductive traits and invasiveness in
this group, which here refers to the ca.1012 taxa in the genus
Acacia (hereafter referred to as ‘Australian acacias’ or Acacia,
formerly placed in Acacia subgenus Phyllodineae and synon-
ymous with Racosperma) that have Australia as at least part of
their native range; see Miller et al. (2011) for a more recent
phylogenetic treatment of this and related groups. To do this,
we present an analysis in two parts: (1) a quantitative
comparative analysis of specific reproductive traits for which
appropriate data were available; and (2) a qualitative literature
review of reproductive traits for which we could not find
quantitative data, but which may be important in predicting
invasiveness. We conclude with the implications for manage-
ment.
Australian acacias are an excellent group for exploring
determinants of invasiveness and are likely to become a model
system against which other invasive plant groups are compared
(Richardson et al., 2011). They comprise a phylogenetically
and geographically distinct group (natural distributions virtu-
ally confined to the Australian continental landmass) with
1012 described species (Richardson et al., 2011), of which at
least a third have been introduced and 23 are invasive in
different parts of the world (Richardson & Rejma
´nek, 2011;
Richardson et al., 2011). Their well-documented introduction
histories (e.g. Le Roux et al., 2011) and records of invasiveness
in different introduced ranges make comparative studies
possible on continental and global scales. Australian acacias
appear to possess a suite of reproductive and other life-history
traits that have been suggested as instrumental in their success
as invasive species (Milton & Hall, 1981; Richardson & Kluge,
2008). Unfortunately, invasive taxa among Australian acacias
are far better studied than are non-invasive taxa; this is in line
with a general bias in invasion ecology whereby invasive species
that exert greater impacts on invaded environment are better
studied (Pys
ˇek et al., 2008). This complicates statistical analysis
of associations between species character traits and invasive-
ness.
Little is known in general about such associations (Gallagher
et al., 2011), and to date, no multi-species, multi-regional
study has explored how reproductive traits influence invasive-
ness of Australian acacias. In this study, we review available
published and unpublished information on their reproductive
traits and trait ‘syndromes’ (sets of reproductive traits that
repeatedly favour a particular group of pollinators, method of
reproduction, agent of seed dispersal or germination system)
and compare trait values between (1) rare and common
Australian acacias; (2) invasive Australian species in their
native and introduced ranges; and (3) introduced invasive
species and introduced non-invasive Australian acacias. Our
aim is to identify those traits associated with invasiveness. Our
approach has been dictated by the availability of data. For
those traits for which data are available (Table S1), we use
phylogenetically controlled comparative analyses to ask which
reproductive traits, alone or in combination, are significant
correlates of invasiveness. For those traits we were unable to
analyse quantitatively, we qualitatively review all available
information to address the questions: (1) Are there distinct
reproductive syndromes that differ between invasive and non-
invasive species? and (2) does pollinator-mediated seed
production reduce or enhance naturalization or invasion in
any regions? Such an approach has the potential to yield
insights that are of value to plant invasion ecology in general
and for refining screening protocols (e.g. Gordon et al., 2010)
for assessing the risk of further introductions of Acacia species
that may lead to invasions.
Methods
Species list
We used the classification scheme of Richardson & Rejma
´nek
(2011) to define which species are considered invasive
(n = 23). The objective criteria used in their study (following
Pys
ˇek et al., 2004) are more conservative than those applied by
others (e.g. Randall, 2002), and only species that have spread
considerable distances from parent populations are considered
‘invasive’. However, the criteria are not as strict as in other
studies, such as Castro-Dı
´ez et al. (2011), who regarded species
as ‘invasive’ (sensu Pys
ˇek et al., 2004) only when supported by
at least two different sources of information from different
countries. Species were defined as having been introduced
(n = 152) only if a herbarium record for that species has been
collected from outside Australia (Richardson et al., 2011).
We compiled data on at least one of eight reproductive traits
for 450 of the 1012 species in the Australian Acacia group. Of
the 860 non-introduced species, data were available for six of
the traits for 324 species (Table S2). Of the 152 introduced
species, data were available for all eight traits for 126 species
M. R. Gibson et al.
912 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
(23 invasive, 103 non-invasive; see Table S1) – see Fig. 1 for a
breakdown of species used in this study. We analysed data on
reproductive traits using only introduced species to reduce
biases caused during the introduction process.
Statistical analysis
We used R for all statistical analyses (R Development Core
Team, 2011). Reproductive traits were used as explanatory
variables, and invasive status (invasive and non-invasive) was
used as the response variable. Explanatory variables used in
quantitative analyses comprised: time to reproductive matu-
rity; index of self-incompatibility (ISI) (number of infructes-
cences/inflorescence); ISI (number of pods/inflorescence);
combined measure of breeding system; dispersal agent (ant-
or bird-dispersed seed); seed mass; resprouting ability; and
length of flowering period (see Appendix 1 for details and
references). Seed mass was log transformed to reduce skewness
in the data. Seeds were considered to be dispersed by birds
either if this was conclusively reported in the literature or,
based on seed morphological traits, if the arils/funicles or
elaiosomes were specifically described as being orange, yellow
or red. Species were considered to be ‘not bird dispersed’ if
they were reported to be dispersed by ants in the literature and
where dispersal by birds was not mentioned. Species for which
clear data were not available were omitted from the analysis. A
combined measure of breeding system was inferred from
multi-locus outcrossing rate (t
m
), both ISI measurements, and
breeding system (t
m
and breeding system not used in final
analyses; see Appendix 1 and Table S1). We considered a
species as outcrossing if t
m
‡0.8 or ISI £0.5; otherwise,
species were considered to have mixed mating systems.
Because species do not represent independent data points in
comparative studies (Hadfield & Nakagawa, 2010; Stone et al.,
2011), we incorporated phylogenetic relationships among
sampled species into our analyses using a generalized least-
squares (gls) framework in the nlme package (Pinheiro et al.,
2009). This approach assumes a Brownian model of character
evolution in which trait covariance between a pair of species
decreases linearly since their time of divergence from a shared
common ancestor. The phylogenetic relationship between taxa
was inferred using Bayesian methods incorporated in the
software MrBayes version 3.1.2 (Ronquist & Huelsenbeck,
2003). Our analysis incorporates sequence data for two nuclear
genes (nuclear ribosomal DNA internal (ITS) and external
(ETS) transcribed spacers) and four chloroplast regions (psbA-
trnH intergenic spacer, trnL-F intron and intergenic spacer,
rpl32-trnL intergenic spacer and a portion of the matK
Australian
Acacia species
n = 1012
23 invasive,
989 non-
invasive
Introduced
species
n = 152
23 invasive, 129
non-invasive
Non-introduced
species
n = 860
all non-invasive
(by deinition)
Species with
available
reproductive trait
data
n = 126
23 invasive, 103
non-invasive
Species with
available
reproductive trait
data
n = 324
Species with
available
phylogenetic data
n = 72*
17 invasive, 55
non-invasive
TABLE S1 TABLE S2
Figure 1 Breakdown of Australian Acacia
species used in this study. *One of the
species for which there was phylogenetic
data had no available reproductive trait
data.
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 913
introns), comprising a tandem alignment of 5912 base pairs.
Contiguous sequences were edited using Sequencherv.3.0
(Gene Codes Corporation) and manually aligned in BioEdit
sequence alignment editor v.4.8.6 (Hall, 1999). Appropriate
models of molecular evolution for implementation in MrBayes
were identified using the programme Modeltest v.1.1 (Posada
& Crandall, 1998), which identified the GTR + I + G model
(general time reversible model incorporating a proportion of
invariant sites and gamma-distributed rate variation in
variable sites) for both the plastid and nuclear partitions of
our data set. The Markov chain Monte Carlo search in
MrBayes was run for two million generations with trees
sampled every 1000 generations. MrBayes performed two
simultaneous analyses starting from different random trees
(Nruns = 2), each with four Markov chains (Nchains = 4).
The first 200 sampled trees were discarded from each run as
burn-in. We used the 50% majority rule consensus phylogram
as our working phylogeny, with node support expressed in
terms of posterior probability values. All trees were rooted
using Pararchidendron pruinosum as an outgroup taxon.
The resultant phylogeny incorporated 72 species of the 126
species (see Miller et al., 2011), and only data for these species
were incorporated into phylogenetically controlled analyses (17
invasive, 55 non-invasive; see Fig. 2 for phylogenetic tree and
Appendix S1 for species accession numbers). Because our
analytical approach to determine phylogenetic independence
requires a fully resolved phylogeny, polytomies were broken by
inserting very small non-zero branch lengths. Reanalysis with
such instances pruned from the data gave near-identical results
(not shown). To assess the impact of phylogenetic patterns in
our trait data, we compared analyses incorporating phyloge-
netic information for this subset of 72 species with phylogeny-
free analyses for the same species set. To illustrate patterns in
the full data set, we also carried out phylogeny-free analyses
across the full set of 126 species. For both data sets (n= 72 and
n= 126), phylogeny-free tests of trait differences between
invasive and non-invasive species involved Pearson’s chi-
square tests for binary explanatory variables and generalized
linear models for individual continuous explanatory variables.
Results
Of the eight reproductive traits we assessed, only two showed
significant differences between invasive and non-invasive
species in phylogeny-free analyses (Table 1A,B; see Appendix
S2 for actual parameter estimates, results were similar when
using either all 126 species or the subset of 72 species for which
we have a phylogeny). The proportion of species that reach
reproductive maturity within two years was significantly higher
for invasive acacias (v
2
= 6.90, d.f. = 1, P= 0.009). Invasive
species also had a significantly higher probability of being
resprouters (v
2
= 4.34, d.f. = 1, P= 0.037) than non-invasive
species. Incorporation of phylogenetic relationships into the
analysis for 72 species removed the significance of resprout
ability, but supported our results from the phylogeny-free
analyses that invasive species reach reproductive maturity
earlier (gls: coefficient = )0.553, t=)3.18, P= 0.004; Ta-
ble 1B, Appendix S3).
LITERATURE REVIEW: REPRODUCTIVE BIOLOGY
OF AUSTRALIAN ACACIAS
Pollination biology
As a broad generalization, we expect successful invasive species
to share at least some of the following floral traits (Baker, 1955;
Chittka & Schu
¨rkens, 2001; Brown et al., 2002; Ghazoul, 2002;
Gross et al., 2010):
1. High attractiveness to available flower visitors and floral
morphologies allowing pollination by many different organ-
isms.
2. Production of very large numbers of long-lived flowers
allowing seed-set even when visitation rates are low; and/or an
ability to self-pollinate or reproduce vegetatively.
3. Floral induction cues match those triggering flowering in
native species and emergence of native flower visitors.
Worldwide, taxa classified in the polyphyletic group Acacia
sensu lato (genera Acaciella,Mariosousa,Senegalia,Vachellia;
McNeill et al., 2006) share many of these morphological traits
but differ in their global distributions, pollinator assemblages
and specific aspects of floral biology (Stone et al., 2003). All
have small tubular flowers collected together into spherical or
elongated flower heads, with pollen presented on the inflo-
rescence surface (Stone et al., 2003; Raine et al., 2007).
Clustering of the pollen grains into a composite unit, termed
a ‘polyad’, is a key component of the pollination efficiency of
all acacias, providing an efficient means of dispersal via
pollinators (Kenrick & Knox, 1982). There are always fewer
ovules per ovary than pollen grains per polyad, so one polyad
from a single pollination event can potentially fertilize all the
ovules (Kenrick & Knox, 1982). The stigmas of the flowers are
also distributed over the surface of the flower heads and are
freely accessible, so that any insect that travels from one tree to
another is a potential pollinator. Recruitment of insects is
often enhanced by the release of floral scent just before pollen
release, and visual advertisement is often maximized by
synchronized opening of flowers, both within a single tree
and often within a local species’ population (Stone et al.,
2003). Floral morphology is a conserved trait across the genus
and does not distinguish invasive from non-invasive Austra-
lian acacias. Such generalized morphology may facilitate
invasion as it reduces the risk of pollinator limitation for
introduced plants (Richardson et al., 2000a). See Fig. 3 for
photographs of pollination biology traits associated with
invasiveness in Australian acacias.
Floral biology
The fundamental floral morphology shared by all Australian
acacias identifies a generalist entomophilous pollination
syndrome as it provides accessible floral rewards to almost
any insect visitor (Bernhardt, 1989). A second pollination
M. R. Gibson et al.
914 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
syndrome involves pollination by nectar-feeding birds and is
associated with the location of a large extrafloral nectary near
the inflorescence. Pollen collected on the bird’s head is
transferred while it feeds on the gland’s nectar (Knox et al.,
1985). Some species display both insect and bird pollination
syndromes (e.g. A. terminalis, Kenrick et al., 1987). As with
morphology, having a generalized pollination system reduces
pollinator limitation of seed set and is thus likely to contribute
to the invasive success of Australian acacias (Richardson et al.,
2000a).
Australian acacias show two features in their floral biology
that together distinguish them from all other related taxa
(Stone et al., 2003). First, no Australian acacias are recorded to
secrete floral nectar, although some produce extrafloral nectar
Figure 2 Bayesian phylogenetic tree
depicting relationships among taxa
included in the phylogenetic generalized
least-squares analysis. Numbers at nodes
indicate the Bayesian posterior probability
(PP). Invasive taxa are shown in red.
*No reproductive trait data were available
for A. vestita.
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 915
to attract insect and bird pollinators (Knox et al., 1985;
Vanstone & Paton, 1988). There are also other acacia (Acacia
s.l.) species that lack nectar, including A. nilotica (Stone et al.,
1998) – the most invasive African acacia in Australia (Radford
et al., 2002). A second distinctive feature is that individual
flowers and flower heads are relatively long-lived in Australian
acacias (Prescott, 2005) compared with other acacias. Flowers
on a single flower head open over a series of days, and each
flower head can last for up to two weeks (Stone et al., 2003;
George et al., 2009). Intuitively, floral longevity should con-
tribute to the success of Australian acacias as invaders, because
long-lived flowers are tolerant of competition and have a
higher probability of pollination when pollination events are
rare because of pollinator or mate limitation.
The ability of introduced Australian acacias to tolerate
competition for pollination is likely to facilitate invasion, as
introduced species enter an environment where all pollinators
have established relationships with other plant species (Pys
ˇek
et al., 2011). Flower heads of Australian acacias open gradually
and asynchronously, which favours foraging by small bees that
can gather resources in small packets (Stone et al., 2003).
Acacia flowers can be either male-only or hermaphrodite
(Kenrick, 2003; George et al., 2009). Australian Acacia species
have strictly protogynous flowers where the stigma is receptive
Table 1A Phylogeny-free analyses of correlations between reproductive traits and invasiveness of 126 introduced Australian Acacia species
(23 invasive/103 non-invasive Table S1).
Explanatory variables Response variables
Test Relationship
Reproductive traits Invasive Not invasive
Continuous Summary (n; mean, l; range)
Index of self-incompatibility
(ISI) (infructescence/
inflorescence)
n=6 n= 3 GLM (negative binomial errors):
z = 0.010, P= 0.992
No effect
l= 0.425 l= 0.42
range = 0.02–0.86 range = 0.13–0.96 No effect
ISI (pods/inflorescence) n=7 n= 3 GLM (negative binomial errors):
z=)0.212, P= 0.832
No effect
l= 0.339 l= 0.447 No effect
range = 0.008–0.79 range = 0.07–1.1
Seed mass (mg) n=23 n= 99 GLM (binomial errors; response var.
log10 transformed): z= 1.14,
P= 0.254
No effect
l= 20.3 l= 21.1 No effect
range = 5.7–47.8 range = 2.72–219
Length of flowering (months) n=22 n= 59 GLM (binomial errors): z= 0.042,
P= 0.966
No effect
l= 4.909 l= 4.890 No effect
range = 2–10 range = 2–12
Binary Summary ((n, number of total for each factor level); mean, l; confidence interval (CI; 97.5%))
Time to reproductive
maturity (>2 years
or <2 years)
n=13 n=26
(10 < 2 years,
3 > 2 years)
(7, <2 years, 19,
>2 years)
Chi-square: v
2
= 6.90, d.f. = 1,
P= 0.0086
Invasive species reach
reproductive
maturity earlier than
non-invasive species
l= 77% <2 years l= 27% <2 years
CI = 54–100% CI = 12–46%
Combined measure of
breeding system (‘mixed’’
or ‘outcrossing’)
n= 10 (2 mixed, 8
outcross)
n= 3 (1 mixed, 2
outcross)
Chi-square: v
2
= 0.0903, d.f. = 1,
P= 0.764
No effect
l= 20% mixed l= 50% mixed
CI = 0–50% CI = 0–100%
Seed dispersal (‘bird’ or
‘not bird’)
n= 15 (8 bird, 7 not
bird)
n= 12 (4 bird, 8
not bird)
Chi-square: v
2
= 0.422, d.f. = 1,
P= 0.516
No effect
l= 53% bird l= 33% bird
CI = 27–80% CI = 8–58%
Ability to resprout
(True/False)
n= 21 (11 can resprout,
10 cannot)
n= 54 (13 can
resprout, 41 cannot)
Chi-square: v
2
= 4.34, d.f. = 1,
P= 0.037
Ability to resprout
significantly positively
related to species
being invasive
l= 52% l= 24%
CI = 33–71% CI = 13–35%
Details of actual parameter estimates are given in Appendix S2.
M. R. Gibson et al.
916 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
before the anthers produce pollen (Stone et al., 2003; George
et al., 2009). In contrast, the flower heads of African and
American acacias are protandrous and release pollen synchro-
nously, which makes them attractive to larger native bee
species because all the resource is presented at once (Stone
et al., 2003; Raine et al., 2007). To exploit this larger food
resource effectively, the larger African bees, which are impor-
tant pollinators of African acacias, time their arrival at each
species to coincide with its daily pollen release (Stone et al.,
1998). This foraging behaviour would be ineffective for the
exploitation of Australian acacia flowers, and it is not
surprising that the most prominent visitors to introduced
Table 1B Comparison of phylogeny-controlled and phylogeny-free analyses of relationships between reproductive traits and invasiveness
for 72 introduced Australian Acacia species (cf. 126 species in Table 1A), comprising 17 invasive and 55 non-invasive species.
Explanatory variables Response variables
Test
Phylogenetic
generalized
least squares Relationship
Reproductive traits Invasive Not invasive
Continuous Summary (n; mean, l; range)
ISI (Index of
self-incompatibility)
(infructescence/
inflorescence)
n=5 n= 1 GLM (binomial errors):
z = 0.522, P= 0.602
t= 0.107,
P= 0.920
No effect with or without
phylogenyl= 0.34 l= 0.13
range = 0.02–0.78 range = 0.13
ISI (pods/inflorescence) n=6 n= 1 GLM (binomial errors):
z= 0.475, P= 0.635
t= 0.139,
P= 0.895
No effect with or without
phylogenyl= 0.26 l= 0.07
range = 0.008–0.77 range = 0.07 No effect with or without
phylogeny
Seed mass (mg) n=17 n= 53 GLM (binomial errors);
response var. log10
transformed): z= 0.777,
P= 0.437
t= 0.1.01,
P= 0.315
No effect with or without
phylogeny
No effect with or without
phylogeny
l= 20.34
range = 7.52–40.55
l= 23.16
range = 5.21–219.77
Length of flowering
(months)
n=16
l= 4.63
range = 2–10
n=39
l= 4.80
range = 2–12
GLM (binomial errors):
z=)0.330, P= 0.741
t=)0.077,
P= 0.939
No effect with or without
phylogeny
Binary Summary ((n, number of total for each factor level); mean, l; confidence interval (CI; 97.5%))
Time to reproductive
maturity
n= 10 (8 < 2 years,
2 > 2 years)
n= 16 (7, <2 years,
19, >2 years)
Chi-square: v
2
= 5.44,
d.f. = 1, P= 0.02
t=)3.18,
P= 0.004
Invasive species reach
reproductive maturity
earlier than non-invasive
species with and without
phylogeny
l= 75% <2 years l= 48% <2 years
CI = 50–100% CI = 19–69%
Combined measure of
breeding system
n= 9 (1 mixed,
8 outcross)
n= 1 (1 outcross) Chi-square: v
2
= 1.98,
d.f. = 1, P= 0.16
t=)0.103,
P= 0.920
No effect with or without
phylogeny
l= 17% mixed l= 100% mixed
CI = 0–33% CI = 100%
Seed dispersal n= 12 (6 bird, 6
not bird)
n= 5 (2 bird, 3
not bird)
Chi-square: v
2
= 0.02,
d.f. = 1, P= 0.88
t=)0.024,
P= 0.981
No effect with or without
phylogeny
l= 49% bird l= 40% bird
CI = 23–75% CI = 0–80%
Ability to resprout n= 15 (9 can
resprout, 6 cannot)
n= 34 (7 can
resprout, 27 cannot)
Chi-square: v
2
= 5.67,
d.f. = 1, P= 0.0.02
t= 1.08,
P= 0.287
Ability to resprout
significantly positively
related to species being
invasive, but significance
lost when phylogeny
considered
l= 60% l= 23%
CI = 33–87% CI = 9–35%
Phylogenetic relationships among species were incorporated as a covariate in a generalized least-squares analysis (see Methods). Actual parameter
estimates are given in Appendix S3.
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 917
Australia acacias are often honeybees (Apis mellifera) (Bern-
hardt, 1987; Sedgley et al., 1992; Sornsathapornkul & Owens,
1998; Alves & Marins-Corder, 2009), whose sensitivity to
resource availability and ability to learn are both exceptional
among bees (Willmer & Stone, 2004).
Other floral traits that may contribute to the invasive success
of Australian acacias are precocity (early reproductive matu-
rity) and longevity. Morgan et al. (2002) found that low final
pod set (pods/inflorescence) in A. baileyana, as is seen in many
acacias (Kenrick, 2003), was offset by precocious flowering and
high flower numbers, which resulted in high seed production,
probably partly facilitating its invasiveness. Early reproductive
maturity is seen in many invasive acacias with some com-
mencing flowering at just two years of age (see Table S1). In
this study, both phylogeny-free and phylogenetic analyses
suggested that short juvenile period was a significant factor
distinguishing invasive acacias from non-invasive species. This
result makes intuitive sense, because shorter juvenile periods
enhance invasiveness by ensuring that seeds are produced
sooner and thus confer an overall high seed production and
allow for rapid accumulation of a soil seed bank. On a coarse
level, floral biology appears essentially similar for all Australian
acacias. Consequently, specific traits such as time of pollen
release and inflorescence longevity are unlikely to distinguish
invasive and non-invasive Australian acacias. However, subtle
variations in combinations of sexual receptiveness and lon-
gevity (e.g. age-dependent floral colour variation; M.N.
Prescott, unpublished data) could be important in this regard
and require proper studies before being fully ruled out.
Pollination and pollen vectors
Pollinator assemblages vary on an annual, seasonal and
geographic basis so that a diverse spectrum of floral foragers
visit Acacia species in a given location, but the dominance of
specific vectors can vary inter- and intraspecifically (Bernhardt,
1989). In their native range, Acacia species are visited by a
variety of flower foragers, but the most important pollinators
are usually bees and wasps (Apoidea), followed by flies, beetles
and birds (Kenrick et al., 1987; Vanstone & Paton, 1988;
Bernhardt, 1989; Stone et al., 2003; Prescott, 2005). Social bees
are relatively scarce in Australia, and most of the dominant
native bees are small-bodied polylectic solitary species in the
families Anthophoridae, Colletidae and Halictidae. The intro-
duced honeybee is also an important and abundant pollinator
of Australian acacias in both their native and introduced
ranges (Bernhardt, 1987; Thorp & Sugden, 1990; Sedgley et al.,
1992; Prescott, 2005). Existing studies of introduced Australian
acacias in South Africa show that native honeybees (Apis
mellifera capensis and A. mellifera scutellata) are dominant
pollen vectors followed to a lesser extent by flies and bees
(M.R. Gibson, unpublished data; J.G. Rodger unpublished
data) (see Table S3 for a comprehensive list of flower visitors).
In other parts of the introduced range of Australian acacias,
honeybees tend to be the most abundant and effective floral
visitor in terms of visitation frequency and pollen-carrying
load (Sornsathapornkul & Owens, 1998), although their
distribution may be restricted to areas with sufficient avail-
ability of nectar flowers (Alves & Marins-Corder, 2009).
Honeybees may be especially important for pollination in the
context of Acacia invasions as they can learn to exploit new
floral resources in a matter of hours (Willmer & Stone, 2004).
The importance of biotic pollination for reproductive
success depends on whether abiotic pollination occurs.
Although it remains to be tested and although pollen has
been collected downwind of flowering A. mearnsii (Wattle
Research Institute, 1952; Moncur et al., 1989), Acacia inflo-
rescences show no apparent adaptations for capture of wind-
borne pollen. In contrast to typical wind-pollinated species,
which have feathery stigmas and aerodynamic features that aid
(a)
(b)
(c)
(d)
Figure 3 Important pollination biology
traits associated with invasiveness in
Australian acacias. These species share a
generalist pollination syndrome as illus-
trated in South Africa where (a) Acacia
saligna is being visited by native beetles
(photograph: M.R. Gibson) and (b)
A. mearnsii is being visited by the native
honeybee, Apis mellifera capensis (photo-
graph: A.M. Rogers). (c) Mass flowering in
a field invaded by A. saligna in South
Africa during its flowering peak in
September (photograph: A.M. Rogers).
(d) The dense flowers of A. adunca form
an eye-catching, bright yellow floral
display in Queensland (photograph:
T. Low).
M. R. Gibson et al.
918 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
in capture of pollen grains (Niklas, 1985, 1987), Acacia flowers
have a very small cup-shaped stigma into which only one
polyad can fit and lack any obvious aerodynamic structures.
Wind-pollinated species have relatively high pollen to ovule
ratios (median 22 150: 1) relative to animal-pollinated species
(median 3450:1), although pollen-transfer efficiencies (pro-
portion of removed pollen that is captured by stigmas) are
similar (Friedman & Barrett, 2009). Typical of plants with
aggregated (i.e. polyad-like) pollen (Harder & Johnson, 2008),
the pollen to ovule ratio in Acacia is very low (53–360 for
A. mearnsii based on measurements in Kenrick & Knox, 1982;
Moncur et al., 1991), compatible with dependence on animal
pollen vectors. While it thus seems unlikely that wind
pollination would make an appreciable contribution to
fecundity, the possibility cannot yet be rejected. In the only
test for wind pollination that we are aware of, fruit set of
A. mearnsii was reduced but not eliminated in inflorescences
enclosed in cages of wire and nylon mesh. However, bags
reduced wind-borne pollen supply, and some flowers may have
protruded through the cages and been pollinated by bees
(Wattle Research Institute, 1952, 1961) so decisive experiments
are still required to assess whether wind pollination is at all
important for Acacia.
Because acacias are pollinated by generalist pollinators (such
as the widely introduced honeybee), pollinator limitation
seems an unlikely constraint to the spread of introduced
Australian acacias relative to non-invasive taxa (Richardson
et al., 2000a) but this has not yet been studied. If pollination
by A. mellifera enhances seed production of Australian acacias,
then honeybees could facilitate Acacia invasions (and the
facilitation could be reciprocal where both species are intro-
duced, as in South America) (Barthell et al., 2001; Morales &
Aizen, 2002). We conclude that generalist pollination facilitates
invasion, but there is no evidence to suggest that this factor
alone explains the relative success of different Australian
acacias as invasive and introduced non-invasive species both
possess generalist pollination systems.
Phenology
Most Australian acacias tend to flower in massive displays
from late winter to mid-spring (Bernhardt, 1989; Costermans,
2007) and have long-lived (and so competition tolerant)
inflorescences (Stone et al., 2003; Prescott, 2005), although the
number of flower heads in bloom can fluctuate greatly
depending on environmental conditions and resource avail-
ability (Sedgley, 1985; Gaol & Fox, 2002; Yates & Broadhurst,
2002). Pollen release often occurs in the middle of the day
when insect abundance is greatest, which likely confers an
advantage when it comes to adapting to new habitats in the
initial stages of invasion (M.N. Prescott, unpublished data).
Where Australian acacias are invasive in Mediterranean-type
climate regions, their flowering occurs earlier than, and
overlaps with, most native species whose peak flowering
occurs in spring (Henderson, 2001; Godoy et al., 2009).
Various studies have shown early and extended flowering
phenologies of invasive versus native plants to be correlated
with invasive potential (Cadotte & Lovett-Doust, 2001; Pys
ˇek
& Richardson, 2007; Pys
ˇek et al., 2009), thus conferring a
fitness advantage by reduced competition for pollinators
(Stone et al., 1998; Raine et al., 2007). However, while this
may be true in general, differences in overall length of
flowering period between invasive and non-invasive Australian
acacias were found to be non-significant (P. Castro-Dı
´ez,
unpublished data; see discussion in Castro-Dı
´ez et al., 2011).
Peak flowering prior to and during spring, while not unique
to invasive Australian acacias, may contribute indirectly to
invasiveness in some environments as early and prolonged
flowering in Acacia species during peak flowering of native
species in exotic ecosystems may help mitigate pollen and
pollinator limitation. Again, this alone is not likely to
contribute to invasiveness but may do so when it is combined
with other invasion-enhancing reproductive traits that are not
present in non-invasive species.
Breeding system and seed set
Completely self-incompatible species depend entirely on
pollinators and mate availability, but self-compatibility and
the ability to self-pollinate autonomously assure reproduction
against inadequate pollinator visitation and/or mate availabil-
ity (Eckert et al., 2006). Australian Acacia species range from
highly self-incompatible to completely self-compatible and
autogamous (Table S1) (Moffett, 1956; Bernhardt et al., 1984;
Kenrick & Knox, 1989; Morgan et al., 2002), and so probably
vary greatly in their dependence on pollinators for realized
fecundity. Realized outcrossing rates tend to be high (multi-
locus outcrossing rate (t
m
) > 0.9 in most species: Table S1)
indicating that pollinators do play an important role in their
reproduction. Partial self-compatibility and intraspecific
variation in self-compatibility seem relatively common in
Australian Acacia species (Philp & Sherry, 1946; Moffett &
Nixon, 1974) with some ability to reproduce by selfing known
for six species, five of which are invasive (see Table S1: Acacia
dealbata, A. decurrens, A. mearnsii, A. paradoxa, A. saligna)
(J.G. Rodger, unpublished data; George et al., 2008; Millar
et al., 2011).
The apparently high prevalence of at least some level of self-
compatibility in Australian Acacia species is significant given
the rarity of uniparental reproduction in woody plants (Barrett
et al., 1996). This is consistent with the observation by
Rambuda & Johnson (2004) that all 13 woody species
investigated in a survey of breeding systems of invasive plants
in South Africa were capable of uniparental reproduction.
Investigation of Australian Acacia species could reveal further
details about the evolution of breeding systems and their role in
invasiveness in woody species in general. Comparisons between
invasive and non-invasive Acacia species are hindered by
insufficient data here, as elsewhere, but available information
suggest that invasive taxa tend to have higher levels of self-
compatibility, suggesting ability to self-fertilize may predispose
Acacia species to invasiveness. However, in shade house trials,
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 919
selfed progeny of A. mearnsii,A. decurrens (Moffett & Nixon,
1974) and A. dealbata (J.G. Rodger, unpublished data) have
reduced growth and survival, which would erode the repro-
ductive assurance benefits of selfing (Herlihy & Eckert, 2002).
Other self-compatible tree species have such high levels of
inbreeding depression that it is unlikely that progeny arising
from self-pollination ever reach reproductive maturity (Hard-
ner & Potts, 1997; Ishida, 2006; Robertson et al., 2011). A
comparison of fixation index for trees from germination to
reproduction (e.g. Ishida, 2006) would reveal whether selfed
progeny reach reproductive maturity and therefore whether
self-compatibility potentially enhances invasiveness.
Even a low capacity for reproduction by self-fertilization
could be important in alleviating pollinator and mate limita-
tion, which are likely to occur in the early stages of
naturalization and invasion owing to small size or low density
of populations (Baker, 1955; Davis et al., 2004). Such factors
have been shown to influence seed set in Acacia in the native
range (Broadhurst & Young, 2006). However, extensive pollen
dispersal may maintain outcrossing rates in small patches or
isolated plants (Millar et al., 2008, 2011). While ability to self-
fertilize may make species more likely to become invasive or to
spread at greater rates, it is not essential for invasiveness – there
are prominent examples of invasive self-incompatible species
in Acacia (e.g. A. auriculiformis, A. pycnantha – see Table S1)
and other groups (e.g. Barthell et al., 2001). Our study found
no differences in indices of self-compatibility (ISI) nor
breeding system strategy (mixed versus outcrossing) between
invasive and non-invasive species (Table 1A,B), though data
for these traits were extremely limited (see Table S1).
Seed biology
Seed biology seems to be one of the most important factors
contributing to the invasion success of Australian acacias
(Milton & Hall, 1981; Richardson & Kluge, 2008). Seed biology
syndromes in many Acacia species are largely shaped by fire-
driven ecosystems that are present throughout much of
Australia and introduced Mediterranean-type climate regions.
Fire-adaptive traits include: production of large quantities of
hard-coated, heat-tolerant and long-lived seeds with the
capacity for long dormancy; stimulation of germination by
heat and/or smoke; seed dispersal and burial by ants; and the
ability to resprout (Berg, 1975; Bell et al., 1993; Specht &
Specht, 1999), all of which are likely essential for the
persistence and invasive success of Australian acacias (see
Fig. 4 for photographs of seed biology traits associated with
invasiveness).
Dispersal
Dispersal is a crucial aspect of progression from ‘naturalized’
to ‘invasive’ status when recruitment occurs at considerable
distances from parent plants (Richardson et al., 2000a,b).
Australian acacias possess seed adaptations for dispersal by
birds and ants (Davidson & Morton, 1984; O’Dowd & Gill,
1986), although passive dispersal via water, wind and gravity is
also common.
Broadly, biotic seed dispersal in Acacia falls into two
syndromes based on features of arils: a ‘bird-dispersal
syndrome’ and an ‘ant-dispersal syndrome’ (O’Dowd & Gill,
1986). The fleshy arillate appendages (in bird-dispersed seeds)
and an elaiosome (in ant-dispersed seeds) attach the seed to
the seed pod lining and make them accessible to a range of bird
and ant species across multiple foraging types. Such general-
ization of morphological traits associated with dispersal makes
limitation of a seed dispersal agent in the introduced range
unlikely (see Glyphis et al., 1981; Holmes, 1990a; Richardson
et al., 2000a; Underhill & Hofmeyr, 2007). Furthermore, these
traits may be evolutionarily labile since A. ligulata reportedly
displays both syndromes (Davidson & Morton, 1984), each of
which has its own advantages. Birds are important agents in
that they aid in longer distance dispersal (Holmes, 1990a) and,
through ingesting the seeds, are able to aid in the germination
of Acacia species requiring chemical scarification (e.g.
A. cyclops,A. melanoxylon) (Glyphis et al., 1981; Richardson
& Kluge, 2008). Ants rapidly remove and bury Acacia seeds in
subterranean nests and so contribute to dispersal on a local
scale (Holmes, 1990a). Species noted as having a ‘bird-
dispersal syndrome’ are likely also dispersed vertically by ants,
as myrmecochory accounts for much of the movement of seed
from the litter layer into the seed bank (Richardson & Kluge,
2008). Dispersal by birds of an ‘ant-dispersal syndrome’ species
appears less likely (O’Dowd & Gill, 1986).
Importantly, seed morphology and dispersal agents in the
native range of Australian acacias are not always accurate
predictors of dispersal agents in introduced ranges. For example,
in Portugal, South Africa and Florida, invasive Acacia seeds are
effectively dispersed by a wide range of opportunistic agents
besides those that one would consider functional equivalents of
dispersal agents in the native range. These include baboons,
domestic and wild ungulates and humans (Ridley & Moss, 1930;
Middlemiss, 1963; Kull & Rangan, 2008). In the Western Cape of
South Africa, primarily insectivorous barn swallows ingest seeds
and act as effective dispersal agents of A. cyclops (Underhill &
Hofmeyr, 2007), and other granivorous, ground-dwelling birds
disperse Acacia seeds (Duckworth & Richardson, 1988; Knight
& Macdonald, 1991). In New Zealand, most native avian seed
dispersers are now extinct (Anderson et al., 2006), and the ant
fauna is relatively depauperate and limited in distribution (Don,
2007), with only three ant species including seeds in their diet.
Despite these limitations, at least eight Australian Acacia species
have become invasive in New Zealand (Richardson & Rejma
´nek,
2011) with A. baileyana showing evidence of long-distance
dispersal although the dispersal agent is not known (E.M.
Wandrag, unpublished data). Furthermore, in many human-
dominated systems, long-distance dispersal of introduced
species is mostly human mediated (Trakhtenbrot et al., 2005),
so this distinction is likely less important in determining spread
rates than may be predicted.
Abiotic dispersal in water and soil is important in many
regions (Milton & Hall, 1981). There is a strong association
M. R. Gibson et al.
920 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
between A. dealbata invasions and watercourses in Chile and
Portugal (H. Marchante, unpublished data; Pauchard et al.,
2008). Movement of soil for road building is also a major
dispersal route of A. dealbata and A. longifolia in Portugal
(H. Marchante, unpublished data). Similarly in South Africa,
rivers and soil movement aid in the dispersal of acacias that
invade riparian areas, such as A. mearnsii (de Wit et al., 2001).
Seed mass in Acacia was found to be positively correlated
with invasiveness in a recent study (Castro-Dı
´ez et al., 2011)
but did not consistently differ in our study nor in a multi-
species study comparing seed mass between native and
introduced ranges (C. Harris et al., unpublished data). These
results contradict findings for Pinus where smaller seed size is
positively associated with invasiveness, as small seeds are more
suitable for long-distance dispersal by wind (Richardson,
2006). The difference between pines and acacias in this regard
is not surprising. Unlike pines, most acacias are animal
dispersed, and dispersal by wind is of trivial importance.
Factors other than size contribute to dispersibility, and seed
size plays an entirely different role as mediator of colonization
and establishment success.
Dispersal traits associated with a bird-dispersed syndrome in
Australian acacias clearly predispose these species to spread
rapidly in a new environment (see discussion of this for
A. cyclops in South African fynbos by Higgins et al., 2001)
because of the importance of long-distance dispersal events in
driving invasions (Trakhtenbrot et al., 2005). However, of the 23
species of Australian Acacia considered invasive (sensu Pys
ˇek
et al., 2004; Richardson & Rejma
´nek, 2011), only eight species
are known to be bird-dispersed or possess typical bird-dispersed
seed traits (Davidson & Morton, 1984; O’Dowd & Gill, 1986;
Langeland & Burks, 1998; Stanley & Lill, 2002): Acacia auric-
uliformis, A. cyclops, A. holosericea, A. implexa, A. longifolia,
A. mangium, A. melanoxylon and A. salicina (see Table S1).
Additionally, our analysis found that seed dispersal by birds was
not significantly correlated with invasiveness. In Portugal, two of
the most invasive and widespread Acacia species (A. dealbata
and A. longifolia) are ant-dispersed (Marchante et al., 2010), as
are A. saligna and A. mearnsii in South Africa (French & Major,
2001; Richardson & Kluge, 2008). Thus, the contribution of
different dispersal agents to invasiveness remains unclear but
further suggests a role of human-mediated dispersal and
interactions with environmental factors.
Seed bank dynamics
A reproductive trait that strongly influences invasiveness of
Australian acacias is their capacity to form extensive and
persistent soil seed banks (Richardson & Kluge, 2008).
Accumulation times differ depending on the species (see
(a) (b) (c)
(d)
(f)
(e)
Figure 4 Important seed biology traits associated with invasiveness in Australian acacias. (a) Seed production of Acacia saligna in South
Africa during the early 1980s, prior to the introduction of the rust fungus Uromycladium uromyces, which has since greatly reduced seed
production (photograph: D.M. Richardson). (b) Seed production of A. longifolia in its native range in Australia (photograph: C. Harris).
Seeds that fall to the ground can remain viable for 50+ years, making their eradication nearly impossible. (c) A. cyclops seeds remain in the
tree canopy longer than those of species that are typically ant-dispersed; the bright red aril attracts birds that disperse the seeds (photograph:
A.M. Rogers). (d) A. longifolia seeds are typically ant-dispersed in the native range, although bird-dispersal is predicted based on aril
attributes; they are attached to the seed pod by an elaiosome that attracts ants (photograph: C. Harris). (e) Invasive species, such as A. saligna
pictured here, have a greater tendency to resprout following a disturbance event than non-invasive species (photograph: D.M. Richardson).
(f) The mass germination of Acacia seeds after fire, as in A. pycnantha in South Africa shown here, is a major hurdle to control efforts
(photograph: D.M. Richardson).
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 921
Table 2 of Richardson & Kluge, 2008), and the average shortest
time frame is roughly eight years. The seeds of some Acacia
species that have become invasive can remain dormant for 50–
100 years or more (Farrell & Ashton, 1978; New, 1984).
Richardson & Kluge (2008) list four main factors that
contribute to the size of soil-stored seed banks in Australian
acacias in South Africa: the annual seed rain; the age of the
stand; stand density or canopy cover; and distance from the
canopy. Additional factors include level of granivory, decay
and germination (Marchante et al., 2010). Biological control
agents that negatively affect flower, flower bud or pod
production, such as Melanterius weevils (Dennill & Donnelly,
1991; Impson et al., 2004) that directly feed on acacia seeds,
can reduce annual seed rain. The rate of seed accumulation in
the soil increases until the stand is about 30 years old, and
denser stands produce more seeds, so control efforts to reduce
seed production should focus on younger, denser Acacia stands
(Milton & Hall, 1981; Holmes, 1990b). Seed density in the soil
is highest under the tree canopy and decreases sharply with
distance (see Zenni et al., 2009; Marchante et al., 2010),
although Marchante et al. (2010) found a few seeds of
A. longifolia up to 7 m from the edge of invaded stands.
The main drivers of seed bank persistence and maintenance
appear to be ants, although gravity and water may be the
dominant drivers where ants are absent. Once seeds have
dropped to the ground, ants bury many of them in their nests
to allow them to exploit arils (Milton & Hall, 1981). In doing
so, they often account for the majority of vertical seed
movement into the upper seed bank. Acacia seeds gain a
threefold advantage through protection from above-ground
seed predators, protection from fire and incorporation into the
seed bank (Gill, 1985; Holmes, 1990a). In South Africa, ants
may play a critical role in accumulating seed banks of
Australian acacias and aiding in their invasiveness (Holmes,
1990c; Richardson et al., 2000a).
The role of seed bank density in Acacia invasiveness is
unclear. Both higher and lower seed bank densities have been
recorded in the introduced range of various Acacia species
when compared to that in the native range (Milton & Hall,
1981; Richardson & Kluge, 2008; Marchante et al., 2010).
Additionally, methods of measuring seed bank and seed rain
vary widely, making comparisons between introduced and
native ranges problematic (see Table 2 for a summary of
Australian Acacia seed data from various introduced and
native regions). Prolific seed production and large accumula-
tions of seeds in the seed bank certainly contribute to a species’
ability to invade an ecosystem but these qualities alone do not
guarantee invasiveness. Buist (2003) found that closely related
pairs of rare and widespread Acacia species produced similar
numbers of seeds and similar-sized, persistent soil seed
reserves, indicating that level of seed production does not
necessarily determine abundance of a species. These traits likely
need to work in concert with certain physiological and
morphological traits, such as germination ability, resource
utilization, rapid growth of seedlings and dispersal investment,
to contribute to invasiveness.
Germination
The majority of invasive Acacia species possess seeds whose
germination is stimulated by fire, but some invasive species,
notably bird-dispersed taxa, may be stimulated to germinate
through chemical scarification via ingestion by an appropriate
dispersal agent (Glyphis et al., 1981; Fraser, 1990; Richardson
& Kluge, 2008). These stimuli are required to break physical
dormancy of the hard, water impermeable seed coat and allow
germination of Acacia seeds, which have consistently high
viability and low germinability over time. However, in
Portugal, total viability and germinability were found to be
significantly higher (and dormancy lower) in seeds
from recently invaded soils for A. longifolia (Marchante et al.,
2010).
Invasive Australian acacias tend to germinate after distur-
bance, although disturbance is not essential. Acacia dealbata
shows high survival within native forest and in open areas in
Chile where it can endure long periods of drought and shade
under canopies of native trees (Fuentes-Ramı
´rez et al., 2011).
Moreover, mutualistic relationships with nitrogen-fixing bac-
teria are important for successful establishment of leguminous
species, so the presence of compatible rhizobia is also essential
for determining the colonization ability of introduced species
(Parker et al., 2006; Rodrı
´guez-Echeverrı
´aet al., 2011). Inter-
estingly, Rodrı
´guez-Echeverrı
´aet al. (2011) found that these
bacterial symbionts are often cointroduced with their Acacia
hosts from Australia, suggesting the presence of suitable soil
symbionts in the introduced range may not be an important
limiting factor in Acacia invasions per se.
Studies from the introduced ranges of Australian acacias
report that a considerable number of seeds produced and
allocated to seed rain are lost to factors such as early
germination, granivory or decay (Marchante et al., 2010).
However, the consistently high seed viability found in many
species of Acacia appears to be fundamental to their ability to
invade (see Table 2) (Richardson & Kluge, 2008; Marchante
et al., 2010). Germination characters per se do not appear to be
characteristic of invasiveness as invasive Australian Acacia
species in South Africa can show opposing characteristics of
either high dormancy, low germination and decay rates and
rapid seed bank accumulation, or low dormancy, high
germination and decay rates and gradual seed bank accumu-
lation (Richardson & Kluge, 2008).
Comparisons of rare and widespread species show some
association with factors that influence seed germination. The
burial depth and heat-stimulation requirements of a species are
important factors affecting germination that can determine
how rare or widespread it is (Brown et al., 2003). Comparisons
of reproductive traits in two rare acacias and their common
relatives showed differences in the germination (reduced range
of temperature for germination in rare species) and higher
rates of predation of fruit and seed in the rare species (Buist,
2003). Seed viability and dormancy levels between invasive and
non-invasive species have not been compared. It may be
predicted that, because such traits are adaptations to
M. R. Gibson et al.
922 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
Table 2 Seed rain density (SRD), seed bank density (SBD) and seed viability (SV) for Australian acacias in native and introduced ranges.
Acacia species
Seed rain density
per m
2
per year (SRD)
Seed bank density
per m
2
(SBD)
Seed viability
(SV) Region References Observations
A. baileyana 19559 – – Australia
(native range)
17 SRD – maximum #seed/tree
A. baileyana 1824 (3010) – – New Zealand 26 SRD – average # seeds per
m
2
averaged over 7-day
period
A. cyclops – 1430–5140 (142 –281) 46–95.3% South Africa 10
A. cyclops – 2832–7792 (402–1019) 99.2% South Africa 8 SBD – range of four
different blocks
A. cyclops 1197 [1373–3019*] 2031 87% South Africa 15 SRD – *estimated #seed
per m
2
projected canopy
A. cyclops 540 (710) – – Australia
(introduced
range)
6 SRD – estimated from
reproductive output data
(determined by dividing
total mass of seeds
removed from pods by
mass per individual seed)
A. cyclops 1900 (1930) – – Australia
(native range)
6
A. dealbata – 10000 90% Chile 25
A. dealbata 2553 (3244) – – New Zealand 26 SRD – average # seeds per
m
2
averaged over 7-day
period
A. dealbata –ca. 22500 30% Portugal 13 SV: probably
underestimated (seeds
heated to 50C without
scarification)
A. elata – – 50% – 22 SV – final germination
after scarification
A. holosericea – – >95% Australia
(native range)
7
A. longifolia 2000–12000 500–1500 >85% Portugal 14 SRD – 2000: smaller trees
next to the ocean
(windward); 12000:
bigger trees leeward
A. longifolia – – >88% Portugal 16
A. longifolia 11500 34000 – South Africa 19 SRD – maximum number
A. longifolia – 2078–3473 (488–498) 99% South Africa 21
A. longifolia 2923 7646 97% South Africa 15
A. longifolia – 4528 (1075) 99% South Africa 4 After introduction of
biological control agent,
max numbers
A. longifolia 2530 (3430) – – Australia
(introduced
range)
6 SRD – estimated from
reproductive output data
(determined by dividing
total mass of seeds removed
from pods by mass per
individual seed)
A. longifolia 810 (1180) – – Australia
(native range)
6
A. mangium 410 – – Indonesia 23 SRD – estimated from seed
production in kg per ha
per year
A. mearnsii – 5314/696 – South Africa 20 SBD- maximum
number/average
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 923
Table 2 Continued.
Acacia species
Seed rain density
per m
2
per year (SRD)
Seed bank density
per m
2
(SBD)
Seed viability
(SV) Region References Observations
A. mearnsii – 38340 – South Africa 15
A. mearnsii – – >83.4% South Africa 12
A. melanoxylon 3218 48739 70% South Africa 15 SRD & SBD: Donald, 1959
cited by Milton & Hall, 1981
A. melanoxylon – – 85–91% Australia
(native range)
2
A. melanoxylon 740 (800) – – Australia
(introduced
range)
6 SRD – estimated from
reproductive output data
(determined by dividing
total mass of seeds
removed from pods by
mass per individual seed)
A. melanoxylon 1160 (1810) – – Australia
(native range)
6
A. paradoxa – 1000 – South Africa 28
A. paradoxa 58# – – Australia
(native range)
1 SRD – #firm seed
production per plant
A. pycnantha 31# – 99% Australia
(native range)
1
A. saligna – 7920–45800 (560–3220) >86% South Africa 10
A. saligna 2645–13472 – – South Africa 27 SRD – measured in 1989,
ca. 2 years after
introduction of biocontrol
agent
A. saligna 446–3035 – – South Africa 27 SRD – measured in 2004,
ca. 18 years after
introduction of biocontrol
agent
A. saligna 5443 [10562*] 11920 83% South Africa 15 SRD – #seed/tree based on
few trees; * estimated seed
per m
2
projected canopy
A. saligna – 715–8097 – South Africa 9 SBD – after introduction of
biological control agent;
values estimated from 4
places and 3 depths
A. saligna – – >90% Israel 3
A. saligna – 2000–189000 (53333) – South Africa 18 After introduction of
biological control agent;
average from 8 sites,
samplings during 6 years
A. saligna – 1389–3600 (207–279) – Australia,
New South Wales
(introduced range)
24
A. saligna – – 73% – 22 SV – final germination
after scarification
A. saligna – 3158–38714 (1194–4006) >65% South Africa 11 SBD – range of 4 sites,
at 0–15 cm
A. saligna 760 (750) – – Australia
(introduced
range)
6 SRD – estimated from
reproductive output data
(determined by dividing
total mass of seeds removed
from pods by mass per
individual seed)
A. saligna 540 (650) – – Australia
(native range)
6
M. R. Gibson et al.
924 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
fire-driven ecosystems, other Acacia species originating from
similar regions also likely possess such germination traits.
Alternative modes of reproduction and persistence
Acacia displays a variety of regeneration strategies besides
germination from seed, including root suckering, and basal
resprouting (Bell et al., 1993; Reid & Murphy, 2008), which
predispose them to weediness and can occur following
disturbance such as fire and mechanical removal (Reid &
Murphy, 2006). In South Africa, for example, species such as
A. cyclops, which lack the ability to resprout after fire, have
high demographic dependence on seeds, while species such as
A. saligna, which resprouts vigorously, depend less on seeds for
population persistence. Spooner (2005) found that disturbance
by road works in Australia triggered a range of responses, such
as a combination of basal resprouting, root suckering and
seedling emergence, which led to a population increase for
three Acacia species. Similarly, resprouting is a major repro-
ductive mechanism in A. dealbata in Chile and Europe and
may facilitate its rapid invasion of new environments (March-
ante et al., 2008; Lorenzo et al., 2010; Fuentes-Ramı
´rez et al.,
2011). Our study also found that resprout ability was greater
for invasive species than for non-invasive species where they
are introduced globally. Long-lived seed banks and ability to
resprout are key determinants of persistence; together with the
ability to disperse, these traits are hugely influential ingredients
of invasive success since they ensure persistence and effectively
permanent occupancy of invaded sites (e.g. Richardson &
Cowling, 1992).
DISCUSSION
Our literature review found that traits including generalist
pollination systems, prolific seed production, efficient seed
dispersal and the accumulation of large and persistent seed
banks, which often have fire-, heat- or disturbance-triggered
germination cues, are characteristic of Australian acacias in
general. We did not find distinct reproductive syndromes that
differed between invasive and non-invasive species, although
this may be both because trait data were not available for all
species, and those species for which data are available might
not be representative.
Pollinator-mediated seed production is likely to facilitate
invasion of Acacia species where they are introduced but
should not differ for introduced non-invasive species as
Australian acacias possess similar floral morphology and
attract similar (generalist) pollinator groups (e.g. Apis mellif-
era). Flowering and seed production are clearly important for
invasion success and account for the massive number of
propagules that accumulate to create a long-lived soil seed
bank that is the largest hurdle to effective control (Wilson
et al., 2011). We found that invasive species reach reproductive
maturity earlier, and this could certainly contribute to a faster
accumulation of a seed bank, which is a vital requirement for
ensuring persistence in regularly disturbed environments, such
as those in which most Australian acacias are invasive
(Richardson et al., 1990, p. 362). These results are supported
in other studies that have also documented the important role
of a short juvenile interval to seed production (in A. baileyana,
see Morgan et al., 2002) and spread rate (in Pinus, see Higgins
et al., 1996; Higgins & Richardson, 1999). Time to reproduc-
tive maturity was also found to be shorter for invasive than
non-invasive species when phylogeny was accounted for. This
trait has not been discovered to have phylogenetic signal, and
in an analysis using the most recent phylogeny for Australian
Acacia, Miller et al. (2011) found that invasive species were
phylogenetically over-dispersed (i.e. there was no phylogenetic
signal for invasiveness). However, our results suggest that
certain traits, which may be related to evolutionary history, can
affect invasiveness and indicate that phenological precocity
may be important for future consideration in phylogenetic
studies.
Seed dispersal is critical for the spread of introduced
Australian acacias, and although biotic dispersal agents are
important, the majority of dispersal is likely human-mediated
and focussed on economically important species. The ability to
resprout undoubtedly aids in persistence during initial estab-
lishment as it makes a population less susceptible to stochastic
events. This is supported by the results of our study that show
Table 2 Continued.
Acacia species
Seed rain density
per m
2
per year (SRD)
Seed bank density
per m
2
(SBD)
Seed viability
(SV) Region References Observations
A. salicina – – 77% – 22 SV – final germination
after scarification
A. victoriae – 50–3900 80% Australia
(native range)
5
Values refer to mean values unless otherwise specified (standard deviation in parentheses where available).
1: Brown et al. (2003); 2: Burrows et al. (2009); 3: Cohen et al. (2008); 4: Fourie (2008); 5: Grice & Westoby (1987); 6: C. Harris et al. (unpublished
data); 7: Hellum (1990); 8: Holmes (1989); 9: Holmes (2002); 10: Holmes et al. (1987); 11: Jasson (2005); 12: Kulkarni et al. (2007); 13: H. Marchante,
unpublished data; 14: Marchante et al. (2010); 15: Milton & Hall (1981); 16: M. Morais, unpublished data; 17: Morgan (2003); 18: Morris (1997); 19:
Pieterse (1987); 20: Pieterse (1997); 21: Pieterse & Cairns (1986); 22: Rehman et al. (2000); 23: Saharjo & Watanabe (2000); 24: Tozer (1998); 25: G.
Valencia, unpublished data; 26: E.M. Wandrag, unpublished data; 27: Wood & Morris (2007); 28: Zenni et al. (2009).
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 925
resprout ability to be significantly greater for invasive species.
Our results are similar to those of Pys
ˇek & Richardson (2007)
who found that vegetative reproduction is positively associated
with invasiveness in vascular plants across multiple compar-
ative studies. However, resprouting ability should not directly
aid in the ability of plants to spread.
There is much room to improve our knowledge of the
reproductive biology in this genus. The role of pollinator-
mediated seed production, especially by Apis mellifera, appears
to be important to reproductive success of Acacia where they
are introduced, and this needs to be formally tested. In
addition, self-compatibility has the potential to facilitate the
invasion process by enabling seed production when mate and
pollinator availability is low, but formal tests are needed to see
whether effects of inbreeding depression cancel out such
benefits. Whether the reproductive traits that we tested are
related to evolutionary history is unknowable at this point. The
lack of clear phylogenetic signal in Acacia is probably due to
the lack of data both in the value of the reproductive traits and
in the sampling of the phylogenetic tree. That our results
suggest reproductive traits are related to evolutionary history is
an important issue that will need further research. Thus, we
recommend that future analyses incorporate variable and
phylogenetic data for a wider array of invasive and non-
invasive species (see Box 1 for a list of research priorities).
The finding that certain reproductive traits show no obvious
correlation with invasiveness in Australian acacias may be
attributable to a number of factors. First and foremost is the
shortage of data for many Australian acacias, both invasive and
non-invasive, and consequent small sample sizes (see Table 1-
A,B for sample sizes). This makes detection of more subtle
correlations between reproductive traits and invasiveness
difficult, resulting in an incomplete picture for understanding
such relationships. Secondly, there is clearly no single ‘ideal’
reproductive syndrome that equips certain species in this
group particularly well to establish, undergo rapid population
growth (often from small founder populations), and to persist
across the full range of habitats to which they have been
introduced. Thirdly, if much of the reproductive trait data for
invasive and non-invasive introduced species comes from
studies within the native range, they may not incorporate
differences in measurements because of region-specific factors
of the introduced range. Such disparities in data highlight the
need for measuring reproductive performance of individual
invasive Acacia species in the introduced and native range. A
fourth possibility is that all Australian acacias possess inherent
reproductive and/or other life-history traits that facilitate
invasiveness, and thus, all Australian acacias have the capacity
to become invasive. Specific features of reproductive biology
may be less important than a range of human-mediated factors
that influence the abundance and distribution of species across
potentially invasible sites, such as facets of the introduction
history, propagule pressure, residence time and country-
specific utilization or treatment of particular species via
economic, environmental and social avenues.
Key stages for invasiveness of the reproductive life cycle of
Australian acacias are useful to identify to determine options
for the intervention to reduce success and achieve management
objectives (Wilson et al., 2011). Control efforts should aim, in
the first instance, to prevent the accumulation of massive seed
banks (Richardson & Kluge, 2008) as once a seed bank is
established, the population is practically impossible to erad-
icate. Biological control provides the most cost efficient, long-
term control method and should be the foundation of effective
integrated control operations. The upper seed bank is where
the majority of Acacia seeds are able to successfully germinate
and so should be the target area for control measures of which
burning is the most effective. However, the applicability in
practice of such useful additional measures as burning,
mechanical control and herbicide application is context
specific. To reduce human-mediated dispersal, planting Aus-
tralian acacias near points of dispersal pathways (e.g. near
Box 1 Priorities for future research on the reproductive ecology of Australian acacias
To elucidate determinants of invasiveness, a variety of approaches are necessary to establish a complete profile for identifying reproductive traits
consistently associated with invasion success in novel environments. This includes conducting multi-species studies encompassing native and
multiple introduced ranges and comparative studies that contrast invasive Acacia species with co-occurring native species, as well as with
non-invasive Acacia species or closely related taxa. Data for these comparisons regarding reproductive traits are widely lacking, and further
studies are needed to gather information on reproductive biology.
Very little research has been carried out on the pollination biology of Australian acacias. Given its fundamental role in reproductive success and
therefore invasion, further research is needed to determine the relative contributions of different insect visitors and wind pollination to
outcrossing and seed set in the introduced range for invasive species and non-invasive species as well as for invasive species in exotic and native
ranges. This information could be used to determine whether pollination efficiency contributes to a species’ invasiveness.
Both breeding system data, based on controlled pollinations that indicate potential for selfing, and mating system data, based on molecular
markers that give the rates of outcrossing, are needed. Breeding system data are lacking for some invasive Acacia species and for almost all non-
invasive species in their introduced ranges. Comparisons are needed between both groups to determine how breeding system links to inva-
siveness and also between invasive species in the native range and in the introduced range to examine the extent of interspecific breeding system
plasticity. Findings have implications for management protocols regarding genetic modifications and expected seed yields following
self-pollination.
Thorough documentation of seed dispersal syndromes in the group is needed, for example, to determine whether the bird-dispersal syndrome is
overrepresented in taxa that have become invasive. Insights from such work will provide useful information for improving the management of
already invasive Australian acacias and help to refine tools for more effective screening of new introductions.
M. R. Gibson et al.
926 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
rivers, along roads) should be prohibited (Wilson et al., 2011).
Although the significant association of resprouting ability with
invasiveness in the phylogeny-free analyses may be misleading
in evolutionary terms, it is still useful from a management
perspective. Thus, wherever Australian Acacia species that
attain reproductive maturity early or have a strong capacity for
resprouting are planted, proactive measures should be imple-
mented to manage invasiveness.
Despite our attempts to test for individual reproductive
traits that contribute to invasiveness, larger sample sizes
facilitated by greater data availability are necessary before any
firm conclusions can be drawn in this regard. Because there is
still a depauperate knowledge surrounding this group of
globally important invasive plants, reproductive traits of
invasive Australian acacias and their distinguishing character-
istics need to be the focus of future research directives (see
Box 1). Hence, until there is substantial evidence to the
contrary, caution should be exercised concerning introduc-
tions of all Australian acacias given their general ability to
reproduce effectively in new locations.
ACKNOWLEDGEMENTS
We acknowledge financial support from the DST-NRF Centre
of Excellence for Invasion Biology and the Working for Water
programme through their collaborative project on ‘Research for
Integrated Management of Invasive Alien Species’, Stellenbosch
University and the Oppenheimer Memorial Trust. We thank
Peter Bernhardt for providing information and references on
Acacia pollination and Rod Griffin and Stephen Midgley for
information on features that distinguish invasive from non-
invasive Australian acacias. Graciela Valencia kindly shared
information on A. dealbata in Chile and Haylee Kaplan on
A. implexa and A. stricta in South Africa. Rod Griffin and Jane
Habbard supplied information on ploidy and breeding systems.
E. M. was supported by FCT-MCTES, grant SFRH/BPD/63211/
2009 and H. M. by FCT-MCTES, grant SFRH/BD/24987/2005.
REFERENCES
Alves, E.M.S. & Marins-Corder, M.P. (2009) Reproductive
biology of Acacia mearnsii De Wild. (Fabaceae) IV: flower
visitors. Revista Arvore,33, 443–450.
Anderson, S.H., Kelly, D., Robertson, A.W., Ladley, J.J. &
Innes, J.G. (2006) Birds as pollinators and dispersers: a case
study from New Zealand. Acta Zoologica Sinica,52, 112–115.
Andrew, R.L., Miller, J.T., Peakall, R., Crisp, M.D. & Bayer, R.J.
(2003) Genetic, cytogenetic and morphological patterns in a
mixed mulga population: evidence for apomixis. Australian
Systematic Botany,16, 69–80.
Baker, H.G. (1955) Self-compatibility and establishment after
‘long-distance’ dispersal. Evolution,9, 347–368.
Barrett, S.C.H., Harder, L.D. & Worley, A.C. (1996) The
comparative biology of pollination and mating in flowering
plants. Philosophical Transactions: Biological Sciences,351,
1271–1280.
Barthell, J.F., Randall, J.M., Thorp, R.W. & Wenner, A.M.
(2001) Promotion of seed set in yellow star-thistle by honey
bees: evidence of an invasive mutualism. Ecological Applica-
tions,11, 1870–1883.
Bell, D.T., Plummer, J.A. & Taylor, S.K. (1993) Seed germi-
nation ecology in southwestern Western Australia. Botanical
Review,59, 24–73.
Berg, R.Y. (1975) Myrmecochorous plants in Australia and
their dispersal by ants. Australian Journal of Botany,23, 475–
508.
Bernhardt, P. (1987) A comparison of the diversity, density,
and foraging behavior of bees and wasps on Australian
Acacia.Annals of the Missouri Botanical Garden,74, 42–50.
Bernhardt, P. (1989) The floral biology of Australian Acacia.
Advances in legume biology (ed. by C.H. Stirton and J.L.
Zarucchi), pp. 263–281, Missouri Botanical Garden, St
Louis, Missouri.
Bernhardt, P., Kenrick, J. & Knox, R.B. (1984) Pollination
biology and the breeding system of Acacia retinodes (Legu-
minosae: Mimosoideae). Annals of the Missouri Botanical
Garden,71, 17–29.
Broadhurst, L.M. & Young, A.G. (2006) Reproductive con-
straints for the long-term persistence of fragmented Acacia
dealbata (Mimosaceae) populations in southeast Australia.
Biological Conservation,133, 512–526.
Broadhurst, L.M., Young, A.G. & Forrester, R. (2008) Genetic
and demographic responses of fragmented Acacia dealbata
(Mimosaceae) populations in southeastern Australia. Bio-
logical Conservation,141, 2843–2856.
Brown, B.J., Mitchell, R.J. & Graham, S.A. (2002) Competition
for pollination between an invasive species (purple loose-
strife) and a native congener. Ecology,83, 2328–2336.
Brown, J., Enright, N.J. & Miller, B.P. (2003) Seed production
and germination in two rare and three common co-occurring
Acacia species from south-east Australia. Austral Ecology,28,
271–280.
Buist, M.L. (2003) Comparative ecology and conservation biol-
ogy of two critically endangered acacias (Acacia lobulata and
A. sciophanes) and two common, widespread relatives (Acacia
verricula and A. anfractuosa) from the south-west of Western
Australia. PhD thesis, The University of Western Australia.
Burrows, G.E., Virgona, J.M. & Heady, R.D. (2009) Effect of
boiling water, seed coat structure and provenance on the
germination of Acacia melanoxylon seeds. Australian Journal
of Botany,57, 139–147.
Butcher, P.A., Glaubitz, J.C. & Moran, G.F. (1999) Applica-
tions for microsatellite markers in the domestication and
conservation of forest trees. Forest Genetic Resources Infor-
mation,27, 34–42.
Cadotte, M.W. & Lovett-Doust, J. (2001) Ecological and tax-
onomic differences between native and introduced plants of
southwestern Ontario. Ecoscience,8, 230–238.
Castro-Dı
´ez, P., Godoy, O., Saldan
˜a, A. & Richardson, D.M.
(2011) Predicting invasiveness of Australian acacias on the
basis of their native climatic affinities, life-history traits and
human use. Diversity and Distributions,17, 934–945.
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 927
Chittka, L. & Schu
¨rkens, S. (2001) Successful invasion of a
floral market. Nature,411, 653.
Coates, D.J., Tischler, G. & McComb, J.A. (2006) Genetic
variation and the mating system in the rare Acacia sciophanes
compared with its common sister species Acacia anfractuosa
(Mimosaceae). Conservation Genetics,7, 931–944.
Cohen, O., Riov, J., Katan, J., Gamliel, A. & Bar, P. (2008)
Reducing persistent seed banks of invasive plants by soil
solarization- the case of Acacia saligna.Weed Science,56,
860–865.
Costermans, L. (2007) Native trees and shrubs of south-eastern
Australia, Reed New Holland, Sydney, Australia.
Davidson, D.W. & Morton, S.R. (1984) Dispersal adaptations
of some Acacia species in the Australian arid zone. Ecology,
65, 1038–1051.
Davis, H.G., Taylor, C.M., Lambrinos, J.G. & Strong, D.R.
(2004) Pollen limitation causes an Allee effect in a wind-
pollinated invasive grass (Spartina alterniflora). Proceedings
of the National Academy of Sciences USA,101, 13804–13807.
Dennill, G.B. & Donnelly, D. (1991) Biological control of
Acacia longifolia and related weed species (Fabaceae) in
South Africa. Agriculture, Ecosystems, and Environment,37,
115–135.
Don, W. (2007) Ants of New Zealand. Otago University Press,
Dunedin, New Zealand.
Duckworth, A. & Richardson, D.M. (1988) Notes on the diet of
helmeted guineafowl (203) in the Jonkershoek Valley, Stel-
lenbosch. Promerops,186, 11.
Eckert, C.G., Samis, K.E. & Dart, S. (2006) Reproductive
assurance and the evolution of uniparental reproduction in
flowering plants. Ecology and evolution of flowers (ed. by L.D.
Harder and S.C.H. Barrett), pp. 183–203. Oxford University
Press, Oxford.
Farrell, T.P. & Ashton, D.H. (1978) Population studies on
Acacia melanoxylon R. Br. I. Variation in seed and vegetative
characteristics. Australian Journal of Botany,26, 365–379.
Fourie, S. (2008) Composition of the soil seed bank in alien-
invaded grassy fynbos: potential for recovery after clearing.
South African Journal of Botany,74, 445–453.
Fraser, M.W. (1990) Foods of Redwinged Starlings and the
potential for avian dispersal of Acacia cyclops at the Cape of
Good Hope Nature Reserve. South African Journal of Ecology,
1, 73–76.
French, K. & Major, R.A. (2001) Effect of an exotic Acacia
(Fabaceae) on ant assemblages in South African fynbos.
Austral Ecology,26, 303–310.
Friedman, J. & Barrett, S.C.H. (2009) Wind of change: new
insights on the ecology and evolution of pollination and
mating in wind-pollinated plants. Annals of Botany,103,
1515–1527.
Fuentes-Ramı
´rez, A., Pauchard, A., Cavieres, L.A. & Garcı
´a,
R.A. (2011) Survival and growth of Acacia dealbata vs. native
trees across an invasion front in south-central Chile. Forest
Ecology and Management,261, 1003–1009.
Gallagher, R.V., Leishman, M.R., Miller, J.T., Hui, C., Rich-
ardson, D.M., Suda, J. & Tra
´vnı
´c
ˇek, P. (2011) Invasion
success of introduced Australian acacias: the role of species’
traits and genome size. Diversity and Distributions 17, 884–
897.
Gaol, M.L. & Fox, J.E.D. (2002) Reproductive potential of
Acacia species in the central wheatbelt: variation between
years. Conservation Science Western Australia,4, 147–157.
George, N., Byrne, M. & Yan, G. (2008) Mixed mating with
preferential outcrossing in Acacia saligna (Labill.) H. Wendl.
(Leguminosae: Mimosoideae). Silvae Genetica,57, 139–145.
George, N., Byrne, M. & Yan, G. (2009) Observations of the
reproductive biology of Acacia saligna (Labill.) H.L. Wendl.
Journal of the Royal Society of Western Australia,92, 5–14.
Ghazoul, J. (2002) Flowers at the front line of invasion?
Ecological Entomology,27, 638–640.
Gill, A.M. (1985) Acacia cyclops G. Don (Leguminosae-
Mimosaceae) in Australia: distribution and dispersal. Journal
of the Royal Society of Western Australia,67, 59–65.
Glyphis, J.P., Milton, S.J. & Siegfried, W.R. (1981) Dispersal of
Acacia cyclops by birds. Oecologia,48, 138–141.
Godoy, O., Richardson, D.M., Valladares, F. & Castro-Dı
´ez, P.
(2009) Flowering phenology of invasive alien plant species
compared with native species in three Mediterranean-type
ecosystems. Annals of Botany,103, 485–494.
Gordon, D.R., Riddle, B., Pheloung, P.C., Ansari, S., Bud-
denhagen, C., Chimera, C., Daehler, C.C., Dawson, W.,
Denslow, J.S., Tshidada, N.J., LaRosa, A., Nishida, T.,
Onderdonk, D.A., Panetta, F.D., Pys
ˇek, P., Randall, R.P.,
Richardson, D.M., Virtue, J.G. & Williams, P.A. (2010)
Guidance for addressing the Australian Weed Risk Assess-
ment questions. Plant Protection Quarterly,25(2), 56–74.
Grice, A.C. & Westoby, M. (1987) Aspects of the dynamics of
the seed-banks and seedling populations of Acacia victoriae
and Cassia spp. in arid western New South Wales. Australian
Journal of Ecology,12, 209–215.
Gross, C.L., Gorrell, L., Macdonald, M.J. & Fatemi, M. (2010)
Honeybees facilitate the invasion of Phyla canescens
(Verbenaceae) in Australia – no bees, no seed! Weed
Research,50, 364–372.
Hadfield, J.D. & Nakagawa, S. (2010) General quantitative
genetic methods for comparative biology: phylogenies,
taxonomies and multitrait models for continuous and cate-
gorical characters. Journal of Evolutionary Biology,23, 494–
508.
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence
alignment editor and analysis program for Windows 95/98/
NT. Nucleic Acids Symposium Series,41, 95–98.
Hamilton, M.A., Murray, B.R., Cadotte, M.W., Hose, G.C.,
Baker, A.C., Harris, C.J. & Licari, D. (2005) Life-history
correlates of plant invasiveness at regional and continental
scales. Ecology Letters,8, 1066–1074.
Harder, L.D. & Johnson, S.D. (2008) Function and evolution
of aggregated pollen in angiosperms. International Journal of
Plant Sciences,169, 59–78.
Hardner, C.M. & Potts, B.M. (1997) Postdispersal selection
following mixed mating in Eucalyptus regnans.Evolution,51,
103–111.
M. R. Gibson et al.
928 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
Hellum, A.K. (1990) Seed ecology in a population of Acacia
holosericea.Canadian Journal of Forest Research,20, 927–
933.
Henderson, L. (2001) Alien weeds and invasive plants: a com-
plete guide to declared weeds and invaders in South Africa,
Agricultural Research Council of South Africa, Pretoria,
South Africa.
Herlihy, C.R. & Eckert, C.G. (2002) Genetic cost of repro-
ductive assurance in a self-fertilizing plant. Nature,416, 320–
323.
Higgins, S.I. & Richardson, D.M. (1999) Predicting plant
migration in a changing world: the role of long-distance
dispersal. American Naturalist,153, 464–475.
Higgins, S.I., Richardson, D.M. & Cowling, R.M. (1996) The
role of plant–environment interactions and model structure
on the predicted rate and pattern of invasive plant spread.
Ecology,77, 2043–2054.
Higgins, S.I., Richardson, D.M. & Cowling, R.M. (2001)
Validation of a spatial simulation model of a spreading
alien plant population. Journal of Applied Ecology,38, 571–
584.
Holmes, P.M. (1989) Effects of different clearing treatments on
the seed bank dynamics of an invasive Australian shrub,
Acacia cyclops, in the southwestern Cape, South Africa. Forest
Ecology and Management,28, 33–46.
Holmes, P.M. (1990a) Dispersal and predation in alien Acacia.
Oecologia,83, 288–290.
Holmes, P.M. (1990b) Dispersal and predation of alien Acacia
seeds: effects of season and invading stand density. South
African Journal of Botany,56, 428–434.
Holmes, P.M. (1990c) Vertical movement of soil-stored seed at
a sand plain fynbos site. South African Journal of Ecology,1,
8–11.
Holmes, P.M. (2002) Depth distribution and composition of
seed-banks in alien-invaded and uninvaded fynbos vegeta-
tion. Austral Ecology,27, 110–120.
Holmes, P.M., Macdonald, I.A.W. & Juritz, J. (1987) Effects of
clearing treatment on seed banks of the alien invasive shrubs
Acacia saligna and Acacia cyclops in the southern and south-
western Cape, South Africa. Journal of Applied Ecology,24,
1045–1051.
Impson, F.A.C., Moran, V.C. & Hoffmann, J.H. (2004) Bio-
logical control of an alien tree, Acacia cyclops, in South
Africa: impact and dispersal of a seed-feeding weevil,
Melantarius servulus.Biological Control,29, 375–381.
Ishida, K. (2006) Maintenance of inbreeding depression in a
highly self-fertilizing tree, Magnolia obovata Thunb. Evolu-
tionary Ecology,20, 173–191.
Jasson, R. (2005) Management of Acacia species seed banks in
the Table Mountain National Park, Cape Peninsula, South
Africa, PhD thesis, Stellenbosch University, South Africa.
Kenrick, J. (2003) Review of pollen-pistil interactions and their
relevance to the reproductive biology of Acacia.Australian
Systematic Botany,16, 119–130.
Kenrick, J. & Knox, R.B. (1982) Function of the polyad in
reproduction of Acacia.Annals of Botany,50, 721–727.
Kenrick, J. & Knox, R.B. (1989) Quantitative analysis of self-
incompatibility in trees of seven species of Acacia.Journal of
Heredity,80, 240–245.
Kenrick, J., Bernhardt, P., Marginson, R., Beresford, G., Knox,
R.B., Baker, I. & Baker, H.G. (1987) Pollination-related
characteristics in the mimosoid legume Acacia terminalis
(Leguminosae). Plant Systematics and Evolution,157, 49–62.
Kerala Agricultural University (2002) Package of Practices
Recommendations: Crops. Kerala Agricultural University,
Trichur.
Knight, R.S. & Macdonald, I.A.W. (1991) Acacias and korha-
ans: an artificially assembled seed dispersal system. South
African Journal of Botany,57, 220–225.
Knox, R.B., Kenrick, J., Bernhardt, P., Marginson, R., Beres-
ford, G., Baker, I. & Baker, H.G. (1985) Extrafloral nectaries
as adaptations for bird pollination in Acacia terminalis.
American Journal of Botany,72, 1185–1196.
Kulkarni, M.G., Sparg, S.G. & Van Staden, J. (2007) Germi-
nation and post-germination response of Acacia seeds to
smoke-water and butenolide, a smoke-derived compound.
Journal of Arid Environments,69, 177–187.
Kull, C.A. & Rangan, H. (2008) Acacia exchanges: wattles,
thorn trees, and the study of plant movements. Geoforum,
39, 1258–1272.
Langeland, K.A. & Burks, K.C. (1998) Identification and biology
of non-native plants in Florida’s natural areas, IFAS Publi-
cation, University of Florida, Gainesville, Florida.
Le Roux, J.J., Brown, G., Byrne, M., Richardson, D.M. &
Wilson, J.R.U. (2011) Phylogeographic consequences of
different introduction histories of invasive Australian Acacia
species and Paraserianthes lophantha (Fabaceae) in South
Africa. Diversity and Distributions,17, 861–871.
Lorenzo, P., Gonzalez, L. & Reigosa, M.J. (2010) The genus
Acacia as invader: the characteristic case of Acacia dealbata
Link in Europe. Annals of Forest Science,67, 1–11.
Marchante, E., Freitas, H. & Marchante, H. (2008) Guia Pra
´tico
para a Identificac¸a
˜o de Plantas invasoras de Portugal
Continental [Invasive plant species in Portugal: guide for
identification and control]. Imprensa da Universidade de
Coimbra, Coimbra.
Marchante, H., Freitas, H. & Hoffmann, J.H. (2010) Seed
ecology of an invasive alien species, Acacia longifolia (Faba-
ceae), in Portuguese dune ecosystems. American Journal of
Botany,97, 1–11.
McNeill, J., Barrie, F.R., Burdet, H.M., Demoulin, V.,
Hawksworth, D.L., Marhold, K., Nicholson, D.H., Prado, J.,
Silva, P.C., Skog, J.E., Wiersema, J.H. & Turland, N.J. (eds)
(2006) International code of botanical nomenclature (Vienna
Code): Adopted by the Seventeenth International Botanical
Congress Vienna, Austria, July 2005. Regnum Vegetabile 146.
Gantner, Ruggell.
Middlemiss, E. (1963) The distribution of Acacia cyclops in the
Cape Peninsula area by birds and other animals. South
African Journal of Science,59, 419–420.
Millar, M.A., Byrne, M., Nuberg, I. & Sedgley, M. (2008) High
outcrossing and random pollen dispersal in a planted stand
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 929
of Acacia saligna subsp. saligna revealed by paternity analysis
using microsatellites. Tree Genetics and Genomes,4, 367–377.
Millar, M.A., Byrne, M., Nuberg, I. & Sedgley, M. (2011) High
levels of genetic contamination in remnant populations of
Acacia saligna from a genetically divergent planted stand.
Restoration Ecology,19.
Miller, J.T., Murphy, D.J., Brown, G.K., Richardson, D.M. &
Gonza
´lez-Orozco, C.E. (2011) The evolution and phylogenetic
placement of invasive Australian Acacia species. Diversity and
Distributions,17, 848–860.
Milton, S.J. & Hall, A.V. (1981) Reproductive biology of
Australian acacias in the south-western Cape Province,
South Africa. Transactions of the Royal Society of South Africa,
44, 465–485.
Moffett, A.A. (1956) Genetical studies in acacias. 1. The esti-
mation of natural crossing in Black Wattle. Heredity,10, 57–67.
Moffett, A.A. & Nixon, K.M. (1974) The effects of self-fertil-
ization on green wattle (Acacia decurrens Willd.) and black
wattle (Acacia mearnsii De Wild.). South Africa Wattle
Institute Report,1973–1974, 66–84.
Moncur, M.W., Moran, G.F., Boland, D.J. & Turner, J. (1989)
Floral morphology and breeding systems of Acacia mearnsii
De Wild. Proceedings of the Uses of Australian Trees in
China, Guangzhou.
Moncur, M.W., Moran, G.F. & Grant, J.E. (1991) Factors lim-
iting seed production in Acacia mearnsii.Advances in tropical
acacia research (ed. by J.W. Turnbull), pp. 20–25. Australian
Centre for International Agricultural Research, Canberra.
Morales, C.L. & Aizen, M.A. (2002) Does invasion of exotic
plants promote invasion of exotic flower visitors? A case
study from the temperate forests of the southern Andes.
Biological Invasions,4, 87–100.
Moran, G.F., Muona, O. & Bell, J.C. (1989a) Acacia mangium:
a tropical forest tree of the coastal lowlands with low genetic
diversity. Evolution,43, 231–235.
Moran, G.F., Muona, O. & Bell, J.C. (1989b) Breeding systems
and genetic diversity in Acacia auriculiformis and Acacia
crassicarpa.Biotropica,21, 250–256.
Moravcova
´, L., Pys
ˇek, P., Jaros
ˇı
´k, V., Havlı
´c
ˇkova
´,V.&Za
´k-
ravsky
´, P. (2010) Reproductive characteristics of neophytes
in the Czech Republic: traits of invasive and non-invasive
species. Preslia,82, 365–390.
Morgan, A. (2003) Ornamental and weed potential of Acacia
baileyana F. Muell: investigations of fertility and leaf colour.
PhD thesis, University of Adelaide, Adelaide, Australia.
Morgan, A., Carthew, S.M. & Sedgley, M. (2002) Breeding
system, reproductive efficiency and weed potential of Acacia
baileyana.Australian Journal of Botany,50, 357–364.
Morris, M.J. (1997) Impact of the gall-forming rust fungus
Uromycladium tepperianum on the invasive tree Acacia
saligna in South Africa. Biological Control,10, 75–82.
Muona, O., Moran, G.F. & Bell, J.C. (1991) Hierarchical pat-
terns of correlated mating in Acacia melanoxylon.Genetics,
127, 619–626.
New, T.R. (1984) A biology of acacias. Oxford University Press,
Melbourne.
Niklas, K.J. (1985) The aerodynamics of wind pollination.
Botanical Review,51, 328–386.
Niklas, K.J. (1987) Pollen capture and wind-induced movement
of compact and diffuse grass panicles – implications for pol-
lination efficiency. American Journal of Botany,74, 74–89.
O’Dowd, D.J. & Gill, A.M. (1986) Seed dispersal syndromes of
Australian Acacia.Seed dispersal (ed. by D. Murray), pp. 87–
121, Academic Press, New York.
Parker, M.A., Malek, W. & Parker, I.M. (2006) Growth of an
invasive legume is symbiont limited in newly occupied
habitats. Diversity and Distributions,12, 563–571.
Pauchard, A., Maheu-Giroux, M., Aguayo, M. & Esquivel, J.
(2008) COS 10–1: Detecting invasion processes at the landscape
and regional scales: Acacia dealbata in Chile. 93rd Ecological
Society of America Annual Meeting, Milwaukee, Wisconsin.
Philp, J. & Sherry, S.P. (1946) The degree of natural crossing in
green wattle, Acacia decurrens Willd. and its bearing on
wattle breeding. Journal of the South African Forestry Asso-
ciation,14, 1–28.
Pieterse, P.J. (1987) Acacia longifolia and its control: to burn or
not to burn? Veld and Flora,73, 67–68.
Pieterse, P.J. (1997) Biological studies on woody leguminous
invaders with special reference to Acacia mearnsii, Acacia
melanoxylon and Paraserianthes lophantha. PhD thesis,
Stellenbosch University, South Africa.
Pieterse, P.J. & Cairns, A.L.P. (1986) The effect of fire on an
Acacia longifolia seed bank in the south-western Cape. South
African Journal of Botany,52, 233–236.
Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D.& the R Core
team, (2009) nlme: Linear and Nonlinear Mixed Effects
Models. R package version 3.1–96.
Posada, D. & Crandall, K.A. (1998) MODELTEST: testing the
model of DNA substitution. Bioinformatics,14, 817–818.
Prescott, M.N. (2005) The pollination ecology of a south-eastern
Australia Acacia community. Unpublished PhD thesis,
Oxford University.
Pys
ˇek, P. & Richardson, D.M. (2007) Traits associated with
invasiveness in alien plants: where do we stand? Biological
invasions (ed. by W. Nentwig), pp. 97–125. Springer, Berlin.
Pys
ˇek, P., Richardson, D.M., Rejma
´nek, M., Webster, G.L.,
Williamson, M. & Kirschner, J. (2004) Alien plants in
checklists and floras: towards better communication between
taxonomists and ecologists. Taxon,53, 131–143.
Pys
ˇek, P., Richardson, D.M., Pergl, J., Jaros
ˇı
´k, V., Sixtova, Z. &
Weber, E. (2008) Geographical and taxonomic biases in
invasion ecology. Trends in Ecology and Evolution,23, 237–244.
Pys
ˇek, P., Jaros
ˇı
´k, V., Pergl, J., Randall, R., Chytry
´, M., Ku
¨hn,
I., Tichy
´, L., Danihelka, J., Chrtek, J.jun. & Sa
´dlo, J. (2009)
The global invasion success of Central European plants is
related to distribution characteristics in their native range
and species traits. Diversity and Distributions,15, 891–903.
Pys
ˇek, P., Jaros
ˇı
´k, V., Chytry
´, M., Danihelka, J., Ku
¨hn, I., Pergl,
J., Tichy
´, L., Biesmeijer, J., Ellis, W.N., Kunin, W.E. & Set-
tele, J. (2011) Successful invaders co-opt pollinators of native
flora and accumulate insect pollinators with increasing
residence time. Ecological Monographs,81, 277–293.
M. R. Gibson et al.
930 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
R Development Core Team (2011) R: A language and envi-
ronment for statistical computing. R Foundation for Statis-
tical Computing, Vienna, Austria. ISBN 3-900051-07-0.
http://www.R-project.org/.
Radford, I.J., Nicholas, M., Tiver, F., Brown, J. & Kriticos, D.
(2002) Seedling establishment, mortality, tree growth rates
and vigour of Acacia nilotica in different Astrebla grassland
habitats: implications for invasion. Austral Ecology,27, 258–
268.
Raine, N.E., Sharp Pierson, A. & Stone, G.N. (2007) Plant-
pollinator interactions in a Mexican Acacia community.
Arthropod-Plant Interactions,1, 101–117.
Rambuda, T.D. & Johnson, S.D. (2004) Breeding systems of
invasive alien plants in South Africa: does Baker’s rule apply?
Diversity and Distributions,10, 409–416.
Randall, R.P. (2002) A global compendium of weeds, R.G. & F.J.
Richardson, Meredith, Victoria, Australia.
Rehman, S., Harris, P.J.C., Bourne, W.F. & Wilkin, J. (2000)
The relationship between ions, vigour and salinity tolerance
of Acacia seeds. Plant and Soil,220, 229–233.
Reid, J.C. & Murphy, D.J. (2006) Wattles as weeds: some case
studies from western Victoria, National Herbarium of Victo-
ria, Royal Botanic Gardens, Melbourne.
Reid, J.C. & Murphy, D.J. (2008) Some case studies of acacias
as weeds and implications for herbaria. Muelleria,26, 57–66.
Rejma
´nek, M., Richardson, D.M., Higgins, S.I., Pitcairn, M.J.
& Grotkopp, E. (2005) Ecology of invasive plants: state of the
art. Invasive alien species: searching for solutions (ed. by H.A.
Mooney, R.M. Mack, J.A. McNeely, L. Neville, P. Schei and J.
Waage), pp. 104–161, Island Press, Washington, DC.
Richardson, D.M. (2006) Pinus: a model group for unlocking
the secrets of alien plant invasions? Preslia,78, 375–388.
Richardson, D.M. & Cowling, R.M. (1992) Why is mountain
fynbos invasible and which species invade? Fire in South
African mountain fynbos (ed. by B.W. van Wilgen, D.M.
Richardson, F.J. Kruger and H.J. van Hensbergen), pp. 161–
181, Springer-Verlag, Berlin.
Richardson, D.M. & Kluge, R.L. (2008) Seed banks of invasive
Australian Acacia species in South Africa: role in invasiveness
and options for management. Perspectives in Plant Ecology
Evolution and Systematics,10, 161–177.
Richardson, D.M. & Pys
ˇek, P. (2006) Plant invasions: merging
the concepts of species invasiveness and community invasi-
bility. Progress in Physical Geography,30, 409–431.
Richardson, D.M. & Rejma
´nek, M. (2011) Trees and shrubs as
invasive alien species – a global review. Diversity and Distribu-
tions,17, 788–809.
Richardson, D.M., Cowling, R.M. & Le Maitre, D.C. (1990)
Assessing the risk of invasive success in Pinus and Banksia in
South African mountain fynbos. Journal of Vegetation
Science,1, 629–642.
Richardson, D.M., Allsopp, N., D’Antonio, C.M., Milton, S.J.
& Rejma
´nek, M. (2000a) Plant invasions – the role of
mutualisms. Biological Reviews,75, 65–93.
Richardson, D.M., Pys
ˇek, P., Rejma
´nek, M., Barbour, M.G.,
Panetta, F.D. & West, C.J. (2000b) Naturalization and
invasion of alien plants: concepts and definitions. Diversity
and Distributions,6, 93–107.
Richardson, D.M., Carruthers, J., Hui, C., Impson, F.A.C.,
Robertson, M.P., Rouget, M., Le Roux, J.J. & Wilson, J.R.U.
(2011) Human-mediated introductions of Australian acacias
– a global experiment in biogeography. Diversity and Dis-
tributions,17, 771–787.
Ridley, H.N. & Moss, M.B. (1930) The dispersal of plants
throughout the world. Reeve, Ashford.
Robertson, A.W., Kelly, D. & Ladley, J.J. (2011) Futile selfing
in the trees Fuchsia excorticata (Onagraceae) and Sophora
microphylla (Fabaceae): inbreeding depression over
11 years. International Journal of Plant Sciences,172, 191–
198.
Rodrı
´guez-Echeverrı
´a, S., Le Roux, J.J., Criso
´stomo, J.A. &
Ndlovu, J. (2011) Jack of all trades and master of many?
How does associated rhizobial diversity influence the colo-
nization success of Australian Acacia species? Diversity and
Distributions,17, 946–957.
Ronquist, F. & Huelsenbeck, J.P. (2003) MrBayes 3: bayesian
phylogenetic inference under mixed models. Bioinformatics,
19, 1572–1574.
Saharjo, B.H. & Watanabe, H. (2000) Estimation of litter fall
and seed production of Acacia mangium in a forest planta-
tion in South Sumatra, Indonesia. Forest Ecology and Man-
agement,130, 265–268.
Sedgley, M. (1985) Some effects of temperature and light on
floral initiation and development in Acacia pycnantha.
Australian Journal of Plant Physiology,12, 109–118.
Sedgley, M., Harbard, J., Smith, R.-M.M., Wickneswari, R. &
Griffin, A.R. (1992) Reproductive biology and interspecific
hybridization of Acacia mangium and Acacia auriculiformis
A. Cunn. ex Benth. (Leguminosae: Mimosoideae). Australian
Journal of Botany,40, 37–48.
Sornsathapornkul, P. & Owens, J.N. (1998) Pollination biology
in a tropical Acacia hybrid (A.mangium Willd. x A. auric-
uliformis A. Cunn. ex Benth.). Annals of Botany,81, 631–645.
Specht, R.L. & Specht, A. (1999) Australian plant communities:
dynamics of structure, growth, and biodiversity. Oxford Uni-
versity Press, Oxford.
Spooner, P.G. (2005) Response of Acacia species to disturbance
by roadworks in roadside environments in southern New
South Wales, Australia. Biological Conservation,122, 231–
242.
Stanley, M.C. & Lill, A. (2002) Avian fruit consumption and
seed dispersal in a temperate Australian woodland. Austral
Ecology,27, 137–148.
Starr, F., Starr, K. & Loope, L. (2003) Acacia mangium. http://
www.hear.org/Pier/pdf/pohreports/acacia_mangium.pdf.
(Accessed on 27 November 2010).
Stone, G.N., Willmer, P. & Rowe, J.A. (1998) Partitioning of
pollinators during flowering in an African Acacia commu-
nity. Ecology,79, 2808–2827.
Stone, G.N., Raine, N.E., Prescott, M. & Willmer, P.G. (2003)
Pollination ecology of acacias (Fabaceae, Mimosoideae).
Australian Systematic Botany,16, 103–118.
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 931
Stone, G.N., Nee, S. & Felsenstein, J. (2011) Controlling for
non-independence in comparative analysis of patterns
across populations within species. Philosophical Transac-
tions of the Royal Society of London, Series B,366, 1410–
1424.
Thorp, R.W. & Sugden, E.A. (1990) Extrafloral nectaries pro-
ducing rewards for pollinator attraction in Acacia longifolia
(Andr) Willd. Israel Journal of Botany,39, 177–186.
Thuiller, W., Richardson, D.M., Rouget, M., Proches¸,S.&
Wilson, J.R. (2006) Interactions between environment,
species traits, and human use describe patterns of plant
invasions. Ecology,87, 1755–1769.
Tozer, M.G. (1998) Distribution of the soil seedbank and
influence of fire on seedling emergence in Acacia saligna
growing on the central coast of New South Wales. Australian
Journal of Botany,46, 743–756.
Trakhtenbrot, A., Nathan, R., Perry, G. & Richardson, D.M.
(2005) The importance of long-distance dispersal in biodi-
versity conservation. Diversity and Distributions,11, 173–
181.
Underhill, L.G. & Hofmeyr, J.H. (2007) Barn Swallows Hirundo
rustica disperse seeds of Rooikrans Acacia cyclops, an invasive
alien plant in the Fynbos Biome. Ibis,149, 468–471.
Vanstone, V.A. & Paton, D.C. (1988) Extrafloral nectaries and
pollination of Acacia pycnantha Benth. by birds. Australian
Journal of Botany,36, 519–531.
Willmer, P.G. & Stone, G.N. (2004) Behavioral, ecological, and
physiological determinants of the activity patterns of bees.
Advances in the Study of Behavior,34, 347–466.
Wilson, J.R.U., Gairifo, C., Gibson, M.R. et al. (2011) Risk
assessment, eradication, and biological control: global efforts
to limit Australian acacia invasions. Diversity and Distribu-
tions,17, 1030–1046.
de Wit, M.P., Crookes, D.J. & van Wilgen, B.W. (2001) Con-
flicts of interest in environmental management: estimating
the costs and benefits of a tree invasion. Biological Invasions,
3, 167–178.
Wood, A.R. & Morris, M.J. (2007) Impact of the gall-forming
rust fungus Uromycladium tepperianum on the invasive tree
Acacia saligna in South Africa: 15 years of monitoring.
Biological Control,41, 68–77.
Wattle Research Institute (1952) Annual report of the Wattle
Research Institute for 1951–1952 (fourth–fifth years). Uni-
versity of Natal, Pietermaritzburg.
Wattle Research Institute (1961) Annual report of the Wattle
Research Institute for 1960–1961 (fourth–fifth years). Uni-
versity of Natal, Pietermaritzburg.
Yates, C.J. & Broadhurst, L.M. (2002) Assessing limitations on
population growth in two critically endangered Acacia taxa.
Biological Conservation,108, 13–26.
Zenni, R.D., Wilson, J.R.U., Le Roux, J.J. & Richardson, D.M.
(2009) Evaluating the invasiveness of Acacia paradoxa
in South Africa. South African Journal of Botany,75, 485–
496.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online
version of this article:
Table S1 The complete set of reproductive traits for introduced
Australian acacias (n= 126).
Table S2 The complete set of reproductive traits for non-
introduced Australian acacias (n= 324).
Table S3 List of Australian Acacia flower visitors.
Appendix S1 Accession numbers for those species used in
phylogenetic analyses.
Appendix S2 Phylogeny-free analyses of relationships between
individual reproductive traits in Australian Acacia species and
invasive status (invasive versus non-invasive).
Appendix S3 The effect of individual reproductive traits on
Australian Acacia species’ invasive status (invasive versus non-
invasive) using phylogeny as a covariate.
As a service to our authors and readers, this journal provides
supporting information supplied by the authors. Such mate-
rials are peer-reviewed and may be re-organized for online
delivery, but are not copy-edited or typeset. Technical support
issues arising from supporting information (other than missing
files) should be addressed to the authors.
BIOSKETCH
All co-authors are actively involved in research on the ecology
of Australian Acacia species. M. G. is a Master’s student and
S.D.J., J.J.L.R., D.M.R and J.R.U.W are core team members at
the DST-NRF Centre of Excellence for Invasion Biology
(http://academic.sun.ac.za/cib/). M.G.’s thesis at Stellenbosch
University deals with the effects of Acacia saligna on native
plant–pollinator communities. Her research interests lie in
invasion biology, novel ecosystem interactions and restoration
and conservation research.
Author contributions: M.R.G. and D.M.R. conceived the ideas;
M.R.G., E.M. and H.M. collected most of the new data; M.B.,
N.G., M.R.G., C.H., E.M., H.M., J.T.M., D.J.M., M.N.P., J.G.R.
and E.M.W. contributed additional data; J.J.L.R, J.T.M. and
G.N.S. wrote the phylogenetic methods section; J.J.L.R. and
J.T.M. reconstructed the phylogeny; M.R.G. and J.R.U.W.
analysed the data; E.M. and H.M. created Table 2; J.G.R. and
G.N.S. contributed to the ‘Pollination biology’ section; M.B.,
S.D.J. and J.G.R. contributed to the ‘Breeding system’ section;
A.F.-R. contributed to ‘Germination’ section; A.P. provided
conceptual insight and revision support. M.R.G. led the
writing with support from D.M.R.
Editor: Petr Pys
ˇek
M. R. Gibson et al.
932 Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd
APPENDIX 1
Description of variables, abbreviations and levels used in statistical analyses and Table S1. T = True, F = False, NA = not applicable.
Variable type Abbreviation
No. species for
which data are
available
Levels (and range of values if
continuous) References
Explanatory
Reproductive trait
Age to reproductive
maturity
Mature 39 Categorical, binary:
‘1’ £2 years; ‘2’ ‡2 years
1–6
Multi-locus outcrossing
rate (t
m
)
Outcross 8 Continuous: 0.65–0.97 7–15
Index of self-incompatibility
(ISI) (infructescence per
inflorescence)
Compatible1 9 Continuous: 0.02–0.96 16–19
ISI (pods per inflorescence) Compatible2 10 Continuous: 0.008–1.1 16;17;19;20
Breeding system* Breed 13 Categorical: ‘apomictic’;
‘SI’ = self-incompatible;
‘pSC’ = partially
self-compatible;
‘SC’ = self-compatible
9; 12; 16; 17; 19–22
Combined measure of
breeding system
Combined 13 Categorical, binary: ‘Mixed’ or
‘Outcross’
see footnote
Seed dispersed by ants Ant 16 Categorical: T/NAà5; 20; 23-25; 26
Seed dispersed by birds Bird 13 Categorical: T/NA 6; 23; 24; 26–30
Biotic seed dispersal Dispers (combination
of previous two
columns in Table S1)
27 Categorical, binary: ‘not bird’
dispersed if ant = T &
bird = NA; ‘bird’ dispersed if
bird = T
Seed mass Seed mass 122 Continuous: 2.72–219.77 (mg) 1; 24; 31
Resprout ability Resprout 75 Categorical, binary: T/F 5; 31; 32
Duration of flowering season Flower duration 81 Continuous: 2–12 (months) 5; 31–33
Response
Invasive or not invasive Invasive Binary: 0/1 34
1: J.T. Miller, unpublished data; 2: Australian Native Plants Society, http://anpsa.org.au/a-pod.html, October 2010; 3: Global Invasive Species
Database, http://interface.creative.auckland.ac.nz/database/species/ecology.asp?si=1662&fr=1&sts=sss&lang=EN, 1 October 2010; 4: Kerala Agricul-
tural University, 2002; 5: World Wide Wattle, http://www.worldwidewattle.com, February 2011; 6: Zenni et al. (2009); 7: Broadhurst et al. (2008); 8:
Butcher et al. (1999); 9: George et al. (2008); 10: Millar et al. (2008); 11: Moffett (1956); 12: Moran et al. (1989b); 13: Muona et al. (1991); 14: Philp &
Sherry (1946); 15: Coates et al. (2006); 16: M. R. Gibson, unpublished data; 17: Kenrick & Knox (1989); 18: Moncur et al. (1991); 19: J. G. Rodger,
unpublished data; 20: Morgan et al. (2002); 21: Andrew et al. (2003); 22: Moffett & Nixon (1974); 23: Davidson & Morton (1984); 24: Kew Gardens
Seed Information Database, http://data.kew.org/sid/sidsearch.html, February 2011; 25: Lorenzo et al. (2010); 26: O’Dowd & Gill (1986); 27: Langeland
& Burks (1998); 28: Moran et al. (1989a); 29: Stanley & Lill (2002); 30: Starr et al. (2003); 31: Castro-Dı
´ez et al. (2011); 32: D. J. Murphy, unpublished
data; 33: Arbres et arbustes de La Re
´union, http://arbres-reunion.cirad.fr/especes/fabaceae/acacia_heterophylla_willd, February 2011; 34: Richardson
& Rejma
´nek (2011).
*When only t
m
was available, we used the criteria: SI is t
m
‡0.8.
Inference from t
m
, ISI and breeding system for which species are classified as either outcrossing (if t
m
‡0.8 or ISI £0.5 a species is classified as
outcrossing) and otherwise as mixed mating.
àReferences could only confirm (and not refute) that an ant or bird dispersed seed of a given species, and thus, criteria for ‘not bird’ dispersed were
required (see Biotic seed dispersal (above) and Methods section of main article).
Reproductive biology of Australian acacias
Diversity and Distributions, 17, 911–933, ª2011 Blackwell Publishing Ltd 933
SupportingInformation
TableS1ThecompletesetofreproductivetraitsforintroducedAustralianacacias(n=126).Forreferencesandvariabledescriptions,see
Appendix1.
Acaciaspecies invasive mature outcross compatible1 compatible2 breed combined ant bird dispersed seedmass resprout flowerduration
A.abbreviata0 NA NA NA NA NA NA NA NA NA NA NA 7
A.acinacea0 NA NA NA NA NA NA NA NA NA 10.9 T NA
A.aculeatissima0 NA NA NA NA NA NA NA NA NA NA F 4
A.acuminata0 NA NA NA NA NA NA NA NA NA 16.5 T 4
A.adunca0 2 NA NA NA NA NA NA NA NA 47.9 F 5
A.alata0 NA NA NA NA NA NA NA NA NA 7.35 F 4
A.aneura0 NA NA NA NA apomictic NA T NA notbird 14.98 F 3
A.aspera0 NA NA NA NA NA NA NA NA NA 13.1 NA NA
A.aulacocarpa0 NA NA NA NA NA NA NA NA NA 19 NA 6
A.auriculiformis1 NA 0.92 NA NA SI Outcrossing NA T bird 20 T 7
A.baileyana1 1 NA NA 0.02 SI Outcrossing T NA notbird 21.8 F 4
A.beauverdiana0 NA NA NA NA NA NA NA NA NA 2.87 NA NA
A.beckleri0 NA NA NA NA NA NA NA NA NA 17.8 T 3
A.binervata0 NA NA NA NA NA NA NA NA NA 18.2 F NA
A.binervia0 NA NA NA NA NA NA NA NA NA 10.24 NA NA
A.brachybotrya0 NA NA NA NA NA NA NA NA NA 21.86 F NA
A.browniana0 NA NA NA NA NA NA NA NA NA 4.59 NA NA
A.burkittii0 NA NA NA NA NA NA NA NA NA 20.82 NA NA
A.buxifolia0 NA NA NA NA NA NA NA NA NA 15.7 F NA
A.caesiella0 2 NA NA NA NA NA NA NA NA 19.23 F 3
A.calamifolia0 2 NA NA NA NA NA NA NA NA 27 F 2
A.cardiophylla0 1 NA NA NA NA NA NA NA NA 15.1 F 4
A.cognata0 2 NA NA NA NA NA NA NA NA 8.11 F 4
A.colletioides0 NA NA NA NA NA NA NA T bird 7.64 F 5
A.coriacea0 NA NA NA NA NA NA NA T bird 70.78 NA 6
A.craspedocarpa0 NA NA NA NA NA NA NA NA NA 84.8 F NA
A.crassicarpa1 NA 0.93 NA NA NA Outcrossing NA NA NA 25.97 NA NA
A.cremiflora0 NA NA NA NA NA NA NA NA NA 24.79 NA NA
A.cultriformis0 NA NA NA NA NA NA NA NA NA 12.8 F 4
A.cupularis0 1 NA NA NA NA NA NA T bird 16.23 F 6
A.cyclops1 2 NA NA NA NA NA NA T bird 30.3 F 5
A.dealbata1 2 0.97 0.78 0.727 SC Mixed T NA notbird 12.22 T 5
A.deanei0 NA NA NA NA NA NA NA NA NA 17.29 F 6
A.decora0 1 NA NA NA NA NA NA NA NA 12.1 NA 7
A.decurrens1 NA 0.84 NA NA pSC Outcrossing NA NA NA 15.04 T 5
A.desmondii0 NA NA NA NA NA NA T NA notbird 8.42 NA 5
A.dietrichiana0 NA NA NA NA NA NA NA NA NA NA F NA
A.dodonaeifolia0 NA NA NA NA NA NA NA NA NA 20.39 NA NA
A.drummondii0 1 NA NA NA NA NA NA NA NA 11.98 F 5
A.elata1 NA NA NA NA NA NA NA NA NA 32.5 T 4
A.elongata0 NA NA NA NA NA NA NA NA NA 8.21 NA NA
A.euthycarpa0 NA NA NA NA NA NA NA NA NA 18.9 NA 3
A.falcata0 2 NA NA NA NA NA NA NA NA 13.6 NA 5
A.falciformis0 2 NA NA NA NA NA NA NA NA 42.8 NA 4
A.farinosa0 NA NA NA NA NA NA NA NA NA 8.65 NA 3
A.filicifolia0 NA NA NA NA NA NA NA NA NA 13.8 NA NA
A.filifolia0 NA NA NA NA NA NA NA NA NA 3.55 NA NA
A.fimbriata0 NA NA NA NA NA NA NA NA NA 17 F 5
A.flavescens0 2 NA NA NA NA NA NA NA NA 30.31 NA NA
A.floribunda0 2 NA NA NA NA NA NA NA NA 8 NA 4
A.genistifolia0 NA NA NA NA NA NA NA NA NA 29.95 F 6.5
A.georginae0 NA NA NA NA NA NA NA NA NA 58.51 NA NA
A.glandulicarpa0 NA NA NA NA NA NA NA NA NA 9.18 T NA
A.hakeoides0 2 NA NA NA NA NA NA NA NA 22.7 T 5
A.hamiltoniana0 NA NA NA NA NA NA NA NA NA 15.73 NA NA
A.holosericea1 NA NA NA NA NA NA NA T bird 7.52 F 4
A.howittii0 NA NA NA NA NA NA NA NA NA 5.21 F NA
A.implexa1 NA NA NA NA NA NA NA T bird 15.89 T 5
A.insolita0 NA NA NA NA NA NA NA NA NA 11.11 NA NA
A.irrorata0 NA NA NA NA NA NA NA NA NA 7.79 T 3
A.iteaphylla1 NA NA NA NA NA NA NA NA NA 27.7 T 9
A.jibberdingensis0 NA NA NA NA NA NA NA NA NA 7.54 F 5
A.jonesii0 NA NA NA NA NA NA NA NA NA 13.75 T 4
A.kempeana0 NA NA NA NA NA NA T NA notbird 14.78 NA 6
A.lanigera0 NA NA NA NA NA NA NA NA NA 12.81 NA 6
A.leiophylla0 2 NA NA NA NA NA NA NA NA 11.65 F NA
A.leprosa0 1 NA NA NA NA NA NA NA NA 5 NA NA
A.leptocarpa0 NA NA NA NA NA NA NA NA NA 10.32 NA NA
A.linearifolia0 NA NA NA NA NA NA NA NA NA NA T 3
A.lineolata0 NA NA NA NA NA NA NA NA NA 2.72 NA NA
A.longifolia1 1 NA NA NA NA NA T T bird 15.8 T 5
A.longissima0 2 NA NA NA NA NA NA NA NA 11.8 F 5
A.maidenii0 2 NA NA NA NA NA NA T bird 13.1 NA 6
A.mangium1 1 0.65 NA NA NA NA NA T bird 14.6 F 5
A.mearnsii1 1 0.85 0.088333 0.0405 pSC Outcrossing T NA notbird 13.2 F 3
A.melanoxylon1 1 0.93 NA NA NA NA NA T bird 13.2 T 4
A.microbotrya0 NA NA NA NA NA NA NA NA NA 28.67 T NA
A.monticola0 NA NA NA NA NA NA NA NA NA 31.02 NA NA
A.mucronata0 NA NA NA NA NA NA NA NA NA 7.82 F 5
A.murrayana0 1 NA NA NA NA NA NA NA NA 33.7 T 4
A.myrtifolia0 NA NA 0.17 0.17 SI Outcrossing T NA notbird 9.4 F 7
A.neriifolia0 NA NA NA NA NA NA NA NA NA 27.4 F NA
A.notabilis0 2 NA NA NA NA NA NA NA NA 15.74 F 5
A.oshanesii0 2 NA NA NA NA NA NA NA NA 14.1 NA 12
A.oxycedrus0 NA NA NA NA NA NA NA NA NA 28.8 NA NA
A.paradoxa1 1 NA 0.86 0.79 pSC Mixed T NA notbird 14 F 5
A.parramattensis0 2 NA NA NA NA NA NA NA NA 9.38 F 6
A.pendula0 2 NA NA NA NA NA NA NA NA 21.3 T NA
A.penninervis0 NA NA NA NA NA NA NA NA NA 55.74 NA NA
A.piligera0 NA NA NA NA NA NA NA NA NA 32.25 NA NA
A.platycarpa0 2 NA NA NA NA NA NA NA NA 219.77 NA 7
A.podalyriifolia1 1 NA NA NA NA NA NA NA NA 32.3 F 2
A.polystachya0 NA NA NA NA NA NA NA NA NA 17.01 NA NA
A.pravissima0 2 NA NA NA NA NA NA NA NA 8.4 F 3
A.prominens0 NA NA NA NA NA NA NA NA NA 15.5 F 3
A.pruinosa0 NA NA NA NA NA NA NA NA NA 27.1 F 3
A.pubescens0 NA NA NA NA NA NA NA NA NA 6.46 NA NA
A.pulchella0 NA NA NA NA NA NA T NA notbird 6.55 F 8
A.pycnantha1 1 NA 0.02 0.008 SI Outcrossing T NA notbird 18.2 F 5
A.pyrifolia0 NA NA NA NA NA NA NA NA NA 42.61 F 5
A.redolens0 1 NA NA NA NA NA NA NA NA 5.4 F 3
A.retinodes1 NA NA 0.06 0.02 SI Outcrossing NA NA NA 15.32 T 10
A.riceana0 NA NA NA NA NA NA NA NA NA 9.16 NA NA
A.rigens0 NA NA NA NA NA NA NA NA NA 6.34 F 4
A.rubida0 NA NA NA NA NA NA NA NA NA 14.68 NA NA
A.rupicola0 NA NA NA NA NA NA NA NA NA 20.48 F 8
A.salicina1 NA NA NA NA NA NA NA T bird 47.8 T 5
A.saligna1 1 0.945 0.74 0.77 pSC Outcrossing T NA notbird 15.97 T 2
A.schinoides0 NA NA NA NA NA NA NA NA NA 15.6 NA NA
A.sclerophylla0 NA NA NA NA NA NA NA NA NA 3.9 NA 4
A.simsii0 NA NA NA NA NA NA NA NA NA 48.78 NA NA
A.steedmanii0 NA NA NA NA NA NA NA NA NA 16.58 NA NA
A.stenophylla0 NA NA NA NA NA NA NA NA NA 123.34 T 5
A.stricta1 NA NA NA NA NA NA NA NA NA 5.7 F 4
A.suaveolens0 NA NA NA NA NA NA T NA notbird 29.7 F 6
A.subporosa0 NA NA NA NA NA NA NA NA NA 9.5 NA 2
A.subulata0 NA NA NA NA NA NA NA NA NA 23.09 F NA
A.terminalis0 NA NA 0.13 0.07 SI Outcrossing T NA notbird 28.3 NA 9
A.trineura0 NA NA NA NA NA NA NA NA NA 6.9 T 3
A.triptera0 NA NA NA NA NA NA NA NA NA 5.37 NA NA
A.truncata0 NA NA NA NA NA NA NA NA NA 5.26 NA NA
A.ulicifolia0 NA NA 0.96 1.1 SC Mixed T NA notbird 12.2 F 7
A.verniciflua0 2 NA NA NA NA NA NA NA NA 11.7 F 3
A.verticillata1 2 NA NA NA NA NA NA NA NA 11.49 F 6
A.victoriae1 1 NA NA NA NA NA T NA notbird 40.55 NA 4
A.viscidula0 NA NA NA NA NA NA NA NA NA 6.3 NA NA
TableS2Thecompletesetofreproductivetraitsfornon‐introducedAustralianacacias(n=324).Forreferencesandvariabledescriptions,
seeAppendix1.
Acaciaspecies invasive mature outcross breed combined ant bird dispersed seedmass resprout flowerduration
A.aciphylla0 NA NA NA NA NA NA NA NA F NA
A.acradenia0 NA NA NA NA T NA notbird 7.6 NA 9.5
A.acrionastes0 NA NA NA NA NA NA NA 20.42 NA NA
A.adoxa0 NA NA NA NA NA NA NA 7.31 NA NA
A.adsurgens0 NA NA NA NA T NA notbird 7.49 NA 5
A.aestivalis0 NA NA NA NA NA NA NA 111.09 NA NA
A.alcockii0 NA NA NA NA NA NA NA 18.15 NA NA
A.amblygona0 NA NA NA NA NA NA NA 10 NA NA
A.amblyophylla0 >2 NA NA NA NA T bird NA NA 2
A.ammobia0 NA NA NA NA T NA notbird 8 NA 3
A.amoena0 NA NA NA NA NA NA NA 9.88 NA NA
A.ampliceps0 NA NA NA NA NA NA NA 26.5 T NA
A.anceps0 >2 NA NA NA NA NA NA 23.23 NA 4
A.ancistrocarpa0 NA NA NA NA T NA notbird 36.67 NA 6
A.ancistrophylla0 NA NA NA NA NA NA NA NA NA 3
A.anfractuosa0 NA 0.85 NA NA T NA notbird 3.75 NA 6
A.anthochaera0 NA NA NA NA NA NA NA 14.97 NA NA
A.aphylla0 NA NA NA NA NA NA NA 16.24 NA NA
A.aprica0 NA NA NA NA NA NA NA 3.36 NA NA
A.argyrophylla0 NA NA NA NA NA NA NA 58.76 T 5
A.ascendens0 NA NA NA NA NA NA NA 5.61 NA NA
A.assimilis0 NA NA NA NA NA NA NA 2.59 NA NA
A.atkinsiana0 NA NA NA NA NA NA NA 10.23 NA NA
A.attenuata0 2 NA NA NA T NA notbird NA NA NA
A.aureocrinita0 NA NA NA NA NA NA NA 28.41 NA NA
A.ausfeldii0 NA NA NA NA NA NA NA 11.67 NA NA
A.baeuerlenii0 NA NA NA NA NA NA NA 30.65 NA NA
A.bakeri0 NA NA NA NA NA NA NA 39.79 NA NA
A.barringtonensis0 NA NA NA NA NA NA NA 11.81 NA NA
A.baueri0 NA NA NA NA NA NA NA 13.58 NA NA
A.beadleana0 NA NA NA NA NA NA NA 13.88 NA NA
A.betchei0 >2 NA NA NA NA NA NA 32.31 NA 3
A.bifaria0 NA NA NA NA NA NA NA 3.92 NA NA
A.bivenosa0 >2 NA NA NA NA T bird 26.66 NA 8
A.blakei0 NA NA NA NA NA NA NA 6.59 NA NA
A.blakelyi0 NA NA NA NA NA NA NA 23.13 NA NA
A.blayana0 >2 NA NA NA NA NA NA NA NA 2
A.boormanii0 >2 NA NA NA NA NA NA 13.26 NA 2
A.botrydion0 NA NA NA NA NA NA NA 19.47 NA NA
A.brachystachya0 NA NA NA NA NA NA NA 29.6 NA NA
A.brassii0 >2 NA NA NA NA NA NA 7.84 NA 1
A.brownii0 NA NA NA NA NA NA NA NA NA 5
A.brumalis0 NA NA NA NA NA NA NA 16.19 NA NA
A.brunioides0 NA NA NA NA NA NA NA 10.34 NA NA
A.burbidgeae0 NA NA NA NA NA NA NA 8.06 NA NA
A.burrowii0 NA NA NA NA NA NA NA 5.31 NA NA
A.caerulescens0 NA NA NA NA NA NA NA 37.86 NA NA
A.caesariata0 NA NA NA NA NA NA NA 1.55 NA NA
A.calcicola0 >2 NA NA NA NA NA NA 45 NA 4
A.cambagei0 NA NA NA NA NA NA NA 32.23 T 5
A.campylophylla0 NA NA NA NA NA NA NA 6.37 NA NA
A.cana0 NA NA NA NA T NA notbird NA NA 3
A.cangaiensis0 NA NA NA NA NA NA NA 18.38 NA NA
A.carens0 NA NA NA NA NA NA NA 30.86 NA NA
A.caroleae0 NA NA NA NA NA NA NA 10.71 NA NA
A.cedroides0 NA NA NA NA NA NA NA 9.54 NA NA
A.celastrifolia0 NA NA NA NA NA NA NA 13.08 NA NA
A.cerastes0 NA NA NA NA NA NA NA 5.51 NA NA
A.chalkeri0 NA NA NA NA NA NA NA 9.57 NA NA
A.chapmanii0 NA NA NA NA NA NA NA 3.08 NA NA
A.cheelii0 >2 NA NA NA NA NA NA 15.98 NA 3.5
A.chisholmii0 NA NA NA NA NA NA NA 15.92 NA NA
A.chrysotricha0 NA NA NA NA NA NA NA 16.6 NA NA
A.cincinnata0 NA NA NA NA NA NA NA 11.61 NA NA
A.citrinoviridis0 NA NA NA NA NA NA NA 36.53 NA NA
A.clandullensis0 NA NA NA NA NA NA NA 32.86 NA NA
A.clydonophora0 NA NA NA NA NA NA NA 22.91 NA NA
A.colei0 NA NA NA NA NA NA NA 12.1 NA NA
A.complanata0 NA NA NA NA NA NA NA 42.9 NA NA
A.concurrens0 >2 NA NA NA NA NA NA 8.68 NA 3
A.conferta0 NA NA NA NA NA NA NA 12.6 NA NA
A.congesta0 NA NA NA NA NA NA NA 14.54 NA NA
A.conspersa0 NA NA NA NA NA NA NA NA F 7
A.constablei0 NA NA NA NA NA NA NA 14.6 NA NA
A.continua0 NA NA NA NA NA NA NA 7.58 F NA
A.coolgardiensis0 >2 NA NA NA NA NA NA 2.57 NA 4
A.costiniana0 >2 NA NA NA NA NA NA 12.46 NA 3
A.cowaniana0 NA NA NA NA NA NA NA 11.3 NA NA
A.cowleana0 NA NA NA NA T T bird 11.3 NA 3
A.crassa0 >2 NA NA NA NA NA NA 9.03 NA 3
A.crassiuscula0 NA NA NA NA NA NA NA 4.5 NA NA
A.crenulata0 NA NA NA NA NA NA NA 5.14 NA NA
A.cretacea0 NA NA NA NA NA NA NA 32.18 NA NA
A.cuneifolia0 NA NA NA NA NA NA NA 18.99 NA NA
A.curranii0 NA NA NA NA NA NA NA 4.33 NA NA
A.cuthbertsonii0 NA NA NA NA T NA notbird 132.84 NA 9
A.cyperophylla0 NA NA NA NA NA NA NA 11.9 NA NA
A.dallachiana0 NA NA NA NA NA NA NA 15.37 NA NA
A.daviesioides0 1.5 NA NA NA NA NA NA 6.42 NA 4
A.dawsonii0 NA NA NA NA NA NA NA 4.6 NA 3
A.deficiens0 NA NA NA NA NA NA NA 8.53 NA NA
A.dictyoneura0 NA NA NA NA NA NA NA 8.4 NA NA
A.difficilis0 >2 NA NA NA NA NA NA 23 NA 6
A.difformis0 NA NA NA NA NA NA NA 46.9 T 12
A.disparrima0 NA NA NA NA NA NA NA 16.9 NA NA
A.distans0 >2 NA NA NA NA NA NA 20.3 NA 3
A.disticha0 NA NA NA NA NA NA NA 7.22 NA NA
A.doratoxylon0 NA NA NA NA NA NA NA 12.1 F NA
A.drepanophylla0 NA NA NA NA NA NA NA 23.9 NA NA
A.durabilis0 NA NA NA NA NA NA NA 13.91 NA NA
A.duriuscula0 NA NA NA NA NA NA NA 2.55 NA NA
A.effusa0 NA NA NA NA NA NA NA 26.37 NA NA
A.elachantha0 NA NA NA NA NA NA NA 9.59 NA NA
A.empelioclada0 NA NA NA NA NA NA NA 4.52 NA NA
A.enterocarpa0 NA NA NA NA NA NA NA 5.53 NA 3
A.eremophila0 NA NA NA NA NA NA NA 3.07 NA NA
A.erinacea0 NA NA NA NA NA NA NA 5.47 NA NA
A.eriopoda0 NA NA NA NA T NA notbird 6.52 NA 5.5
A.errabunda0 NA NA NA NA NA NA NA 9.85 NA NA
A.estrophiolata0 >2 NA NA NA NA NA NA 54.7 NA NA
A.excelsa0 NA NA NA NA NA NA NA 27.5 NA NA
A.exilis0 >2 NA NA NA NA NA NA 13.5 NA 3
A.extensa0 NA NA NA NA T NA notbird 12.3 F 3
A.flabellifolia0 NA NA NA NA NA NA NA 8.57 NA NA
A.flexifolia0 1.5 NA NA NA NA NA NA 7.18 NA 4
A.flocktoniae0 NA NA NA NA NA NA NA 4.98 NA NA
A.floydii0 NA NA NA NA NA NA NA 30.24 NA NA
A.fragilis0 NA NA NA NA NA NA NA 2.67 NA NA
A.frigescens0 >2 NA NA NA NA NA NA 14.7 NA 3
A.galeata0 NA NA NA NA NA NA NA 71.2 NA NA
A.gillii0 >2 NA NA NA NA NA NA 17.75 NA NA
A.gittinsii0 1.5 NA NA NA NA NA NA NA NA NA
A.gladiiformis0 >2 NA NA NA NA NA NA 25.91 NA 5
A.glaucissima0 NA NA NA NA NA NA NA 3.83 NA NA
A.glaucocarpa0 >2 NA NA NA NA NA NA 20.2 NA 6
A.gnidium0 NA NA NA NA NA NA NA 6.85 NA NA
A.gonoclada0 NA NA NA NA NA NA NA 4.84 NA NA
A.gordonii0 NA NA NA NA NA NA NA 13.49 NA NA
A.grandifolia0 >2 NA NA NA NA NA NA 18.3 NA NA
A.granitica0 NA NA NA NA NA NA NA 10.31 NA NA
A.grisea0 NA NA NA NA NA NA NA 2.84 NA NA
A.gunnii0 NA NA NA NA NA NA NA 13.25 NA NA
A.halliana0 >2 NA NA NA NA NA NA 2.6 NA NA
A.hamersleyensis0 NA NA NA NA NA NA NA 16.11 NA NA
A.hammondii0 NA NA NA NA NA NA NA 6.27 NA NA
A.harveyi0 1.5 NA NA NA NA NA NA 12.02 NA 8
A.havilandiorum0 NA NA NA NA NA NA NA 6.1 NA 2
A.hemignosta0 NA NA NA NA NA NA NA 40.25 NA NA
A.hemiteles0 NA NA NA NA NA NA NA 22.1 F NA
A.hemsleyi0 NA NA NA NA NA NA NA 16.75 NA NA
A.heterochroa0 NA NA NA NA NA NA NA 8.46 NA NA
A.heteroclita0 NA NA NA NA NA NA NA 8.59 NA NA
A.hilliana0 NA NA NA NA NA NA NA 6.06 NA NA
A.hispidula0 NA NA NA NA NA NA NA 47.54 NA NA
A.hubbardiana0 NA NA NA NA NA NA NA 9.12 NA NA
A.humifusa0 NA NA NA NA NA NA NA 26.6 NA NA
A.hyaloneura0 NA NA NA NA NA NA NA 5.21 NA NA
A.imbricata0 NA NA NA NA NA NA NA 9.81 F NA
A.inaequilatera0 NA NA NA NA NA NA NA 41.98 NA NA
A.incanicarpa0 NA NA NA NA NA NA NA 9.08 NA NA
A.inceana0 NA NA NA NA NA NA NA 11.46 NA NA
A.ingramii0 NA NA NA NA NA NA NA 20.42 NA NA
A.inophloia0 NA NA NA NA NA NA NA 4.53 NA NA
A.ixiophylla0 NA NA NA NA NA NA NA 6.5 F 3
A.jennerae0 NA NA NA NA NA NA NA 71.66 NA NA
A.jucunda0 NA NA NA NA NA NA NA 15.46 NA NA
A.julifera0 >2 NA NA NA NA NA NA 26.36 NA 6
A.juncifolia0 NA NA NA NA NA NA NA 9.6 NA NA
A.karina0 NA 1 NA NA NA NA NA NA NA NA
A.kettlewelliae0 NA NA NA NA NA NA NA 16.71 NA NA
A.kybeanensis0 NA NA NA NA NA NA NA 15.8 NA NA
A.kydrensis0 NA NA NA NA NA NA NA 15.22 NA NA
A.lachnophylla0 NA NA NA NA NA NA NA 1.92 NA NA
A.lanuginophylla0 NA NA NA NA NA NA NA NA F 4
A.lasiocalyx0 >2 NA NA NA NA NA NA 24.9 F 4
A.lasiocarpa0 1.5 NA NA NA NA NA NA 4.4 NA 6
A.lateriticola0 NA NA NA NA NA NA NA 5.6 NA NA
A.latipes0 NA NA NA NA NA NA NA 4.51 NA NA
A.latisepala0 NA NA NA NA NA NA NA 66.22 NA NA
A.latzii0 NA NA NA NA T NA notbird 12.64 NA 7
A.legnota0 NA NA NA NA NA NA NA 36.33 NA NA
A.leichhardtii0 >2 NA NA NA NA NA NA 27.4 NA NA
A.leiocalyx0 NA NA NA NA NA NA NA 7.33 NA NA
A.leptoclada0 NA NA NA NA NA NA NA 13.37 NA NA
A.leptospermoides0 NA NA NA NA NA NA NA 1.36 NA NA
A.leptostachya0 NA NA NA NA NA NA NA 3.97 NA NA
A.leucoclada0 >2 NA NA NA NA NA NA 17.21 NA 4
A.ligulata0 >2 NA NA NA T T bird 27.6 F 4
A.lineata0 NA NA NA NA NA NA NA 10.79 F NA
A.linifolia0 1.5 NA NA NA T NA notbird 23.9 NA 12
A.lirellata0 NA NA NA NA NA NA NA 3.4 NA NA
A.lobulata0 NA NA NA NA T NA notbird NA NA 1
A.loderi0 >2 NA NA NA NA NA NA 10.6 NA 3
A.longispicata0 >2 NA NA NA NA NA NA 12.51 NA 3
A.longispinea0 NA NA NA NA NA NA NA 5 NA NA
A.lucasii0 NA NA NA NA NA NA NA 13.28 NA NA
A.lysiphloia0 NA NA NA NA T NA notbird 17.88 NA 5.5
A.mabellae0 NA NA NA NA NA NA NA 15.76 NA NA
A.macnuttiana0 NA NA NA NA NA NA NA 26.27 NA NA
A.maitlandii0 NA NA NA NA NA NA NA 9.83 NA 5
A.megacephala0 NA NA NA NA NA NA NA 7.73 NA NA
A.meiantha0 NA NA NA NA NA NA NA 5.62 NA NA
A.meisneri0 >2 NA NA NA NA NA NA 42.02 NA 4
A.melleodora0 NA NA NA NA NA NA NA 8.44 NA NA
A.melvillei0 NA NA NA NA NA NA NA NA NA 2
A.menzelii0 NA NA NA NA NA NA NA 7.87 NA NA
A.merrallii0 >2 NA NA NA NA T bird 2.5 F 3
A.merrickiae0 NA NA NA NA NA NA NA 17.57 NA NA
A.microcarpa0 NA NA NA NA NA NA NA 6.1 F 4
A.minutifolia0 NA NA NA NA T NA notbird 6.92 NA 4.5
A.mitchellii0 NA NA NA NA NA NA NA 15.47 NA NA
A.mollifolia0 >2 NA NA NA NA NA NA 20.29 NA 5
A.montana0 NA NA NA NA NA NA NA 10.4 F 4
A.multisiliqua0 NA NA NA NA NA NA NA 13.55 NA NA
A.multispicata0 NA NA NA NA NA NA NA 6.19 F 8
A.mutabilis0 NA NA NA NA NA NA NA 7.07 NA NA
A.nanodealbata0 NA NA NA NA NA NA NA 11.18 NA NA
A.nematophylla0 NA NA NA NA NA NA NA 17.66 NA NA
A.neurocarpa0 NA NA NA NA NA NA NA 10.63 NA NA
A.neurophylla0 NA NA NA NA NA NA NA 3.87 NA NA
A.nigripilosa0 NA NA NA NA NA NA NA 13.56 NA NA
A.nodiflora0 NA NA NA NA NA NA NA 21.55 NA NA
A.novaanglica0 NA NA NA NA NA NA NA 41.14 NA NA
A.nyssophylla0 NA NA NA NA NA NA NA NA NA 3
A.obliquinervia0 >2 NA NA NA NA NA NA 26.4 NA 5
A.obtusata0 NA NA NA NA NA NA NA 17.8 NA NA
A.obtusifolia0 NA NA NA NA NA NA NA 21.22 NA NA
A.oldfieldii0 >2 NA NA NA NA NA NA 8.1 NA 4
A.olsenii0 NA NA NA NA NA NA NA 35.9 NA NA
A.omalophylla0 NA NA NA NA NA NA NA NA NA 2
A.ophiolithica0 NA NA NA NA NA NA NA 1.84 NA NA
A.oraria0 NA NA NA NA NA NA NA 33 NA NA
A.oswaldii0 >2 NA NA NA NA T bird 79.4 F 3
A.oxyclada0 >2 NA NA NA NA NA NA 3.9 NA 3
A.pachycarpa0 NA NA NA NA NA NA NA 175 NA NA
A.papulosa0 NA NA NA NA NA NA NA 14 NA NA
A.parvipinnula0 1.5 NA NA NA NA NA NA 11.89 T 4
A.pedina0 NA NA NA NA NA NA NA 14.4 NA NA
A.perangusta0 NA NA NA NA NA NA NA 9.25 NA NA
A.phaeocalyx0 NA NA NA NA NA NA NA 25.21 NA NA
A.phasmoides0 NA NA NA NA NA NA NA 14.73 NA 4
A.phlebocarpa0 NA NA NA NA NA NA NA 16.42 NA NA
A.pilligaensis0 NA NA NA NA NA NA NA 9.04 NA NA
A.pinguiculosa0 NA NA NA NA NA NA NA 2.28 NA NA
A.pinguifolia0 NA NA NA NA NA NA NA 11.4 NA NA
A.plectocarpa0 NA NA NA NA NA NA NA 22 NA NA
A.plicata0 NA NA NA NA NA NA NA 7.88 NA NA
A.polybotrya0 NA NA NA NA NA NA NA 23.4 NA NA
A.prainii0 NA NA NA NA T NA notbird 41.09 NA 4
A.pravifolia0 NA NA NA NA NA NA NA 11.86 NA NA
A.provincialis0 NA NA NA NA NA NA NA 11.48 NA NA
A.pruinocarpa0 NA NA NA NA T NA notbird 33.28 NA 3
A.pterocaulon0 1.5 NA NA NA NA NA NA NA NA 4
A.ptychoclada0 NA NA NA NA NA NA NA 12.39 NA NA
A.pubifolia0 NA NA NA NA NA NA NA 9.98 NA NA
A.pusilla0 NA NA NA NA NA NA NA 2.75 NA NA
A.pustula0 NA NA NA NA NA NA NA 17.97 NA NA
A.pycnostachya0 NA NA NA NA NA NA NA 13.75 NA NA
A.quadrilateralis0 NA NA NA NA NA NA NA 10.64 NA NA
A.quornensis0 NA NA NA NA NA NA NA 17.4 NA NA
A.racospermoides0 NA NA NA NA NA NA NA 54.02 NA NA
A.ramulosa0 >2 NA NA NA T NA notbird 75.02 F 7
A.repanda0 NA NA NA NA NA NA NA 5.7 NA NA
A.resinimarginea0 NA NA NA NA NA NA NA 2.86 NA NA
A.retivenea0 NA NA NA NA NA NA NA 37.5 NA NA
A.rhetinocarpa0 NA NA NA NA NA NA NA 8.81 NA NA
A.rhigiophylla0 NA NA NA NA NA NA NA 4.26 NA NA
A.rhodophloia0 NA NA NA NA NA NA NA 3.19 NA NA
A.rivalis0 NA NA NA NA NA NA NA NA F 6
A.rossei0 NA NA NA NA NA NA NA 35.93 F 6
A.rostellifera0 NA NA NA NA NA T bird 18.34 NA 4
A.rothii0 NA NA NA NA NA NA NA 219.48 NA NA
A.ruppii0 NA NA NA NA NA NA NA 19.81 NA NA
A.saliciformis0 NA NA NA NA NA NA NA 23.27 F 6
A.sciophanes0 NA 0.61 NA Mixed T NA notbird NA NA 3
A.scirpifolia0 1.5 NA NA NA NA NA NA 23.13 NA 3
A.sclerosperma0 NA NA NA NA NA NA NA 243.26 F 7
A.semirigida0 >2 NA NA NA NA NA NA 27.8 NA NA
A.sertiformis0 NA NA NA NA NA NA NA 43.16 NA NA
A.shirleyi0 NA NA NA NA NA NA NA 13 NA NA
A.sibirica0 NA NA NA NA NA NA NA 13.61 F 5
A.siculiformis0 >2 NA NA NA NA NA NA 9.2 NA 4
A.silvestris0 NA NA NA NA NA NA NA 21.58 F 3
A.simmonsiana0 NA NA NA NA NA NA NA 5.62 NA NA
A.spectabilis0 1.5 NA NA NA NA NA NA 24.5 F 5
A.spilleriana0 NA NA NA NA NA NA NA 27.01 NA NA
A.spinescens0 NA NA NA NA NA NA NA 5.6 NA NA
A.splendens0 NA NA NA NA NA NA NA 26.43 NA NA
A.spondylophylla0 NA NA NA NA T NA notbird 12.64 NA 4
A.spooneri0 NA NA NA NA NA NA NA 18.21 NA NA
A.sporadica0 NA NA NA NA NA NA NA 17.61 NA NA
A.squamata0 NA NA NA NA NA NA NA 8.78 NA NA
A.stanleyi0 NA NA NA NA NA NA NA 11.46 NA NA
A.startii0 NA NA NA NA NA NA NA 23.31 NA NA
A.stellaticeps0 NA NA NA NA NA NA NA 12.89 NA NA
A.stereophylla0 NA NA NA NA NA NA NA 3.16 NA NA
A.stipuligera0 NA NA NA NA NA NA NA 10.24 NA NA
A.storyi0 >2 NA NA NA NA NA NA 17.2 NA 5
A.strongylophylla0 1.5 NA NA NA NA NA NA 18.15 NA 5
A.subcaerulea0 NA NA NA NA NA NA NA 34.93 NA NA
A.sublanata0 NA NA NA NA NA NA NA NA F NA
A.subracemosa0 NA NA NA NA NA NA NA 3.91 NA NA
A.sulcata0 NA NA NA NA NA NA NA 2.48 NA NA
A.synchronicia0 >2 NA NA NA NA NA NA 23.3 NA 5
A.telmica0 NA NA NA NA NA NA NA 24.53 NA NA
A.tenuissima0 NA NA NA NA T NA notbird 6.85 NA 6
A.tetragonophylla0 NA NA NA NA T T bird 13.5 F 4
A.tetraneura0 NA NA NA NA NA NA NA 4.33 NA NA
A.toondulya0 NA NA NA NA NA NA NA 18.83 NA NA
A.torulosa0 NA NA NA NA NA NA NA 56.04 NA NA
A.trachycarpa0 NA NA NA NA NA NA NA 37.21 NA NA
A.trachyphloia0 NA NA NA NA NA NA NA 9.27 NA NA
A.tratmaniana0 NA NA NA NA NA NA NA 3.09 NA NA
A.trinervata0 NA NA NA NA NA NA NA 14.72 NA NA
A.triquetra0 1.5 NA NA NA NA NA NA 5.49 NA NA
A.tropica0 NA NA NA NA NA NA NA 8.64 NA NA
A.tumida0 NA NA NA NA NA NA NA 46.6 NA NA
A.ulicina0 NA NA NA NA NA NA NA 62.5 NA NA
A.umbellata0 NA NA NA NA NA NA NA 6.52 NA NA
A.uncinata0 1.5 NA NA NA NA NA NA 62.5 F 3
A.undosa0 NA NA NA NA NA NA NA 2.41 NA NA
A.undulifolia0 NA NA NA NA NA NA NA 33.86 F 2
A.urophylla0 NA NA NA NA NA NA NA NA F 6
A.venulosa0 1.5 NA NA NA NA NA NA 11.6 NA 6
A.veronica0 NA NA NA NA NA NA NA 25.85 NA NA
A.verricula0 NA NA NA NA T NA notbird 3.6 NA 5
A.vittata0 NA NA NA NA NA NA NA 11.91 NA NA
A.wattsiana0 NA NA NA NA NA NA NA 14.27 T 3
A.whibleyana0 NA NA NA NA NA NA NA 6.08 NA NA
A.wilhelmiana0 NA NA NA NA NA NA NA 5.9 NA 4
A.williamsiana0 NA NA NA NA NA NA NA 12.37 NA NA
A.woodmaniorum0 NA 1 NA NA NA NA NA NA NA NA
A.xiphophylla0 NA NA NA NA NA NA NA 71.23 NA NA
A.yorkrakinensis0 NA NA NA NA NA NA NA 14.21 NA NA
TableS3
*Criteriaavailabletodeterminewhetherflowervisitormaybeapotentiallyimportantpollinator.Notallcriteriawereevaluatedforall
species.**IndicatesallpollinationstudiesfromAustraliawereinthenativerangeofthespecies.Criteriaareasfollows:1—relativeabundance
onreproductivepartsofAcaciaflowerhead(>20%);2—meanpolyadload(>10#polyads/insect);3—Acaciaspp.pollenpurity(>50%);4—
visitation(relativefrequency(>20%)orrate);5—exclusionofvisitorreducedseedset.
ListoffloralvisitorstoAustralianacaciasinnativeandintroducedranges.
Acaciaspecies Flowervisitor *Criteriafordetermining
pollinatorimportance
Polyadload
Mean±SE
Region Reference
A.auriculiformisHymenoptera
Apidae(Apismellifera) 2,3 44.0±5.4 NAustralia,
Malaysia
Sedgleyetal.,(1992)
Halictidae 2,3 298.4±16.7 NAustralia,
Malaysia
Sedgleyetal.,(1992)
Diptera
Syrphidae
2,3 77±7.1 NAustralia,
Malaysia
Sedgleyetal.,(1992)
Coleoptera3 1.7±1.6 NAustralia,
Malaysia
Sedgleyetal.,(1992)
A.dealbataDiptera
Cecidomyiidae 1 **Australia Prescott,(2005)
Mycetophilidae Australia Prescott,(2005)
Syrphidae 1 1.8±0.5 SouthAfrica J.G.Rodger,unpubl.data
OtherDiptera 3 0.25±0.13 SouthAfrica
J.G.Rodger,unpubl.data
Hymenoptera
Apismellifer
Formicidae
ascutellata1,2,3 66±19 SouthAfrica
J.G.Rodger,unpubl.data
1 Australia Prescott,(2005)
A.decurrensColeoptera
Chrysomelidae(Eumolpinae) 3 0.33±0.19 SouthAfrica
J.G.Rodger,unpubl.data
Diptera
Syrphidae
1 1.0±0.5 SouthAfrica
J.G.Rodger,unpubl.data
Hymenoptera
Apismelliferascutellata1,2,3 132±35 SouthAfrica J.G.Rodger,unpubl.data
A.longifoliaColeoptera
Scarabaeidae(Heteronyxsp.) Australia Thorp&Sugden,(1990)
Diptera
Calliphoridae(Calliphorasp.)
Australia Bernhardt(1989)
Hymeno
Apidae(Apismellifera)
ptera
1,4 Australia Bernhardt(1989);Thorp&
Sugden(1990)
Colletidae(Amphylaeussp.) 4 Australia Thorp&Sugden(1990)
Colletidae(Leioproctusspp.) Australia Bernhardt(1989)
Halictidae(Lasioglossumspp.) Australia Bernhardt(1989)
Halictidae(Homalictussp.,Lasioglossumspp.) 1,4 Australia Thorp&Sugden(1990)
Tiphiidae(unidentifiedspp.) Australia Bernhardt(1989)
Tiphiidae(Phymatothynnussp.,Neozeleboriasp.,
Tachynomiasp.)
1,4 Australia Thorp&Sugden(1990)
A.mangiumColeoptera2,3 1.7±1.6 NAustralia,
Malaysia
Sedgleyetal.(1992)
Diptera
Syrphidae
Au
N
Malaysia
stralia,Sedgleyetal.(1992)
2,3 77±7.1 NAustralia,
Malaysia
Sedgleyetal.(1992)
Hymenopte
Apidae(incl.Apismellifera)
ra
2,3 44.0±5.4 NAustralia,
Malaysia
Sedgleyetal.(1992)
Apidae( isspp.,Trigonaspp.)Ap
Halictidae
? Orwa al.(2009)et
Sedgleyetal.(1992)
2,3 298.4±16.7 NAustralia,
Malaysia
A.mearnsiiColeoptera
Anobiidae Australia Prescott(2005)
Cerambycidae(Pempsamacrasp.) Australia Bernhardt(1989)
Cerambycidae(Trachyderesdimiatus) 2 113 Brazil Alves&Marins‐Corder(2009)
Cerambycidae( ocerusviolaceus)Comps
Cleridae( spp.)
2 156 Brazil Alves&Marins‐Corder(2009)
Eleale
Cleridae:Lemidea
1 Australia Bernhardt(1989)
Australia Prescott(2005)
Chrysomelidae(Eumolpinae) 3 3.3±1.9 SouthAfrica J.G.Rodger,unpubl.data
Chrysomelidae Australia Prescott(2005)
Coccinellidae Australia Sedgley .(1992)etal
Prescott(2005)
Curculionidae Australia
Erotylidae Australia Prescott(2005)
Mordellidae 1 Australia Prescott(2005)
Mycetophacipae Australia Prescott(2005)
Scarabaeidae(Aphodinae) 2 26 Brazil Alves&Marins‐Corder(2009)
Scarabaeidae(Cetoniinae:Cyrtothyreamarginalis) 1,2,3 16±6 SouthAfrica J.G.Rodger,unpubl.data
Scarabaeidae( ylussuturatis)Macrodact
Scarabaeidae(Rutelinae)
2 229.36 Brazil Alves&Marins‐Corder(2009)
3 5.8±2.0 SouthAfrica J.G.Rodger,unpubl.data
Staphylinidae Australia Prescott(2005)
Tenebrionidae( eonissp.)Alcm
Minuteblackbeetles
Australia Bernhardt(1989)
2 1.4±0.54 SouthAfrica J.G.Rodger,unpubl.data
OtherColeoptera 2 0.67±0.38 SouthAfrica
J.G.Rodger,unpubl.data
Diptera
Agromyzidae
Australia Prescott(2005)
Cecidomyiidae Australia Prescott(2005)
Dolichopodidae(notidentified) 2 58 Brazil Alves&Marins‐Corder(2009)
Empididae(notidentified) 2 135 Brazil Alves&Marins‐Corder(2009)
Muscidae Australia Prescott(2005)
Mycetophilidae Australia Prescott(2005)
Sciaridae Australia Prescott(2005)
Syrphidae(Syrphusspp.) 1 Australia Bernhardt(1989)
Syrphidae 1,3 ¹2.7±1.0 Australia,
¹SouthAfrica
Prescott(2005);¹J.G.Rodger,
unpubl.data
Hemiptera
Reduviidae( elanolestessp.)
Aus
M
Membracidae
2 74.67 Brazil Alves&Marins‐Corder(2009)
Australia Prescott(2005)
Miridae Australia Prescott(2005)
Hymenoptera
Anthophoridae(Exoneuraspp.) 1 Australia Bernhardt(1989)
Apidae(Apismellifera) 2 ¹448.5 Brazil;
Australia
¹Alves&Marins‐Corder
(2009);Moncur .(1991)
etal
J.G.Rodger,unpubl.data
Apismelliferascutellata
Braconidae:Cheloninae
1,2,3 141±68 SouthAfrica
Australia Prescott(2005)
Colletidae Australia Prescott(2005)
Encyrtidae Australia Prescott(2005)
Eumenidae(Antamenessp.) Australia Bernhardt(1989)
Formicidae Australia Prescott(2005)
Halictidae(Homalictussp.,Nomiaspp.) Australia Bernhardt(1989)
Halictidae(Lassioglossumspp.) 1 Australia Bernhardt(1989)
Scelionidae:Baginae Australia Prescott(2005)
Vespidae(Vespinae) 2 54.91 Brazil Alves&Marins‐Corder(2009)
Vespidae(Braconidae) 2 95.5 Brazil Alves&Marins‐Corder(2009)
Otherbees 2,3 121 SouthAfrica
J.G.Rodger,unpubl.data
Lepidoptera
Geometridae Australia Prescott(2005)
Gracillariidae Australia Prescott(2005)
M
Passeriformes
Acanthizachrysorrhoatraliaoncuretal.(1991)
A.melanoxylonDiptera
Cecidomyiidae Australia Prescott(2005)
Chironomidae Australia Prescott(2005)
Lauxaniidae 1 Australia Prescott(2005)
Coleoptera Australia Prescott(2005)
Chrysomelidae 1 Australia Prescott(2005)
A.paradoxaColeoptera
Belidae( otiasp.)Rhin
Buprestidae( elobasisspp.)
Australia Bernhardt(1989)
M
Chrysomelidae
Australia Bernhardt(1989)
Australia Prescott(2005)
Coccinellidae Australia Prescott(2005)
Mycetophacipae Australia Prescott(2005)
Diptera
Cecidomyiidae
1 Australia Prescott(2005)
Lauxaniidae Australia Prescott(2005)
Muscidae(Helinasp.) Australia Bernhardt(1989)
Syrphidae(Syrphusspp.) 1 Australia Bernhardt(1989)
Syrphidae Australia Prescott(2005)
Hymeno
Apidae(Apismellifera)
ptera
1 Australia;
SouthAfrica
Bernhardt(1989);Prescott
(2005);Zenni .(2009)
etal
Bernhardt(1989)
Colletidae(Euryglossaspp.,Leioproctusspp.) 1 Australia
Halictidae(Homalictussp.,Lassioglossumspp.) 1 Australia Bernhardt(1989)
Mymaridae Australia Prescott(2005)
Pteromalidae Australia Prescott(2005)
A.pycnanthaColeoptera
Chrysomelidae Australia Prescott(2005)
Cleridae( idiasp.,Phlogistussp.)Lem
Coccinellidae
Australia Bernhardt(1989)
Australia Prescott(2005)
Diptera
Calliphoridae(Calliphorasp.)
Australia Bernhardt(1989)
Cecidomyiidae Australia Prescott(2005)
Empididae Australia Prescott(2005)
Muscidae Australia Prescott(2005)
Mycetophilidae Australia Prescott(2005)
Syrphidae(Syrphussp.) 1 Australia Bernhardt(1989)
Syrphidae Australia Prescott(2005)
Hymeno
Apidae(Apismellifera)
ptera
1,4,51 Australia Bernhardt(1989);Vanstone&
Patton(1988);Prescott(2005)
Colletidae(Euhesmaspp.,Leioproctusspp.) 1 Australia Bernhardt(1989)
Colletidae Australia Prescott(2005)
Eulophidae Australia Prescott(2005)
Halictidae(Lassioglossumspp.) 1 Australia Bernhardt(1989)
Mymaridae Australia Prescott(2005)
Pteromalidae Australia Prescott(2005)
Tenthredinidae Australia Prescott(2005)
Tiphiidae(Phymatothynnussp.,Rhagigestersp.,
Tachynomiasp.)
Australia Bernhardt(1989)
Passeriformes
Phylidonyrisspp.,Lichenostomusspp.,Melithreptus
sp.,Acanthorhynchussp.,Zosteropssp.,Acanthiza
spp.
5 Australia Vanstone&Patton(1988)
A.retinodesvar.
retinodes
Diptera
Sarcophagidae Australia Bernhardt(1989)
Hymenoptera
Anthophoridae(Exoneuraspp.)
Australia Bernhardt(1989)
Apidae( smellifer )Api a
Colletidae(Euhesmaspp.,Leioproctusspp.)
1 Australia Bernhardt(1989)
1 Australia Bernhardt(1989)
Halictidae(Lasioglossumspp.) 1 Australia Bernhardt(1989)
1Exclusionexperimentsshowedthatinsects(presumablybees)musttransferpollenbetweenplantssincesubstantialpodproduction
occurredwhenonlyinsectshadaccesstoflowers(Vantsone&Patton,1988).
A.retinodesvar.
uncifolia
Coleoptera
Cerambycidae(Stenoderissp.),Scarabaeidae
(sp.)
Automolus
Coccinelidae(Cleoborasp.)
3 Australia Bernhardtetal.(1984);
Bernhardt(1989)
3 Australia Bernhardtetal.(1984)
Diptera
Calliphoridae(Stom asp.)
orhin
Syrphidae(Eristalisspp.,Syrphussp.,Xanthogramma
sp.)
1 Australia Bernhardt(1989)
1,3 Australia Bernhardtetal.(1984);
Bernhardt(1989)
Muscidae( asp.)Musc
Sarcophagidae(Trichareaesp.)
Australia Bernhardt(1989)
3 Australia Bernhardtetal.(1984)
Hymeno
Apidae(Apismellifera)
ptera
1,3 Australia Bernhardtetal.(1984);
Bernhardt(1989)
Colletidae(Leioproctusspp.) 1,3 Australia Bernhardtetal.(1984);
Bernhardt(1989)
Halictidae(Homalictusspp.,Lasioglossumspp.) 1,3 Australia Bernhardtetal.(1984);
Bernhardt(1989)
Megachilidae(Megach spp.)ile
Tiphiidae(Anthoboscaspp.)
3 Australia Bernhardt .(1984)etal
Bernhardt(1989)
Australia
A.salignaColeoptera
Coccinelidae( )Coccinellatransversalis
Curculionidae,Scarabaeidae(Rutelinae:Hoplinii)
1 Australia George(2005)
SouthAfrica M.R.Gibson,unpubl.data
Minuteblackbeetles(Anthicidae,Cleridae,
Chrysomelidae,Mordellidae)
1,4 SouthAfrica M.R.Gibson,unpubl.data
Other(Notobrachypterussp.,Trogodermasp.,
sp.)
Amycterinae
Scarabaediae(Colymbomorphasp.,Sphaeroscelissp.)
1 Australia George(2005)
Australia George(2005)
Diptera
Calliphoridae,Bibionidae,Empididae
SouthAfrica M.R.Gibson,unpubl.data
Heleomyzidae 1 Australia George(2005)
Syrphidae 1 Australia George(2005)
Other(Muscidae,Empididae,Dolichopodidae) 1 Australia George(2005)
Hemiptera
Pentatomidae(Oechaliasp.),Reduviidae
Australia George(2005)
Psyllidae1 Australia George(2005)
Hymeno
Apidae(Apismellifera apensis)
ptera
c
Apidae( mellifera)
1,4 SouthAfrica M.R.Gibson,unpubl.data
Apis
Formicidae( sp.,other)
Australia George(2005)
Iridomyrmex
otherwaspsandbees(unidentified)
1 Australia George(2005)
Australia George(2005)
ReferencesforTableS3
Alves,E.M.S.&Marins‐Corder,M.P.(2009)ReproductivebiologyofAcaciamearnsiiDeWild.(Fabaceae)IV:flowervisitors.RevistaArvore,
,443–450.33
Bernhardt,P.(1989)ThefloralbiologyofAustralianAcacia.AdvancesinLegumeBiology(ed.byC.H.StirtonandJ.L.Zarucchi),pp.263–281.
MissouriBotanicalGarden,St.Louis,Missouri.
Bernhardt,P.,Kenrick,J.&Knox,R.B.(1984)PollinationbiologyandthebreedingsystemofAcaciaretinodes(Leguminosae:Mimosoideae).
Missouri,71,17–29.AnnalsoftheBotanicalGarden
George,N.A.(2005)Koojong(Acaciasaligna),aspecieswithpotentialasaperennialforagefordrylandsalinitymanagement.PhDthesis,The
UniversityofWesternAustralia,Perth.
Moncur,M.W.,Moran,G.F.&Grant,J.E.(1991)FactorslimitingseedproductioninAcaciamearnsii.AdvancesintropicalAcaciaresearch.
ProceedingsofaninternationalworkshopheldinBangkok,Thailand,pp.20–25.AustralianCentreforInternationalAgricultural
Research.
Orwa,C.,Mutua,A.,Kindt,R.,Jamnadass,R.&Anthony,S.(2009)AgroforestreeDatabase:atreereferenceandselectionguideversion4.0.
http://www.worldagroforestry.org/SEA/Products/AFDbases/AF/index.asp.
Prescott,M.N.(2005)ThepollinationecologyofasoutheasternAustraliaAcaciacommunity.UnpublishedPhDthesis,OxfordUniversity.
Sedgley,M.,Harbard,J.,Smith,R.‐M.M.,Wickneswari,R.&Griffin,A.R.(1992)ReproductivebiologyandinterspecifichybridizationofAcacia
and A.Cunn.exBenth.(Leguminosae:Mimosoideae). ournalofBotany, ,37–48.mangium Acaciaauriculiformis AustralianJ40
Thorp,R.W.&Sugden,E.A.(1990)ExtrafloralnectariesproducingrewardsforpollinatorattractioninAcacialongifolia(Andr)Willd.Israel
, ,177–186.JournalofBotany 39
Vanstone,V.A.&Paton,D.C.(1988)ExtrafloralnectariesandpollinationofAcaciapycnanthaBenth.bybirds.AustralianJournalofBotany,36,
519–531.
Zenni,R.D.,Wilson,J.R.U.,LeRoux,J.J.&Richardson,D.M.(2009)EvaluatingtheinvasivenessofAcaciaparadoxainSouthAfrica.South
AfricanJournalofBotany,75,485–496.
AppendixS1Accessionnumbersforthosespeciesusedinphylogeneticanalyses.
AcaciaspeciesHerbariumvoucherGenbankNumbers
abbreviataCANB793276 JF420395,JF419963,JF420177,JF420499,JF420065,JF420287
acuminata MtAnnanBG866885 JF420424JF420205,JF420526,JF420092,JF420313
aduncaANBG8502778 JF420365,JF419934,JF420145,JF420471,JF420035,JF420258
alataCANB00579597 JF420440,JF420001,JF420221,JF420541
aneuraCANB635377 JF420366,JF419935,JF420146,JF420472,JF420036,JF420259
asperaCANB793290 JF420409,JF419976,JF420189,JF420300
aulacocarpaClarkeB JF420398,JF419966JF420501,JF420068,JF420289
auriculiformisATSC15688 JM1812,JN088171,JN088172,JN088173,JN088175,JN088177,JN0
8
baileyanaCANB00693196 JF420439,JF420000,JF420220,JF420540,JF420106,JF420328
beckleriANBG9707897 JF420367,JF419936,JF420147,JF420473,JF420037,JF420260
binervataATSC16245 JF420437,JF419998,JF420218JF420104,JF420326
brachybotryaClarke17b JN006080,JN006091,JN006102,JN006113,JN006122,JN006133
burkittiClarke15b JN006081,JN006092,JN006103,JN006114,JN006123,JN006134
caesiellaCANB643851 JN006082,JN006093,JN006104,JN006115,JN006124,JN006135
calamifoliaCANB793310 JF420351,JF419920,JF420131,JF420457,JF420021,JF420245
cardiophyllaCANB492118 JF420420JF420201,JF420522,JF420088,JF420309
cognataCANB615708 JF420352,JF419921,JF420132,JF420458,JF420022,JF420246
colletioidesCANB633905 JN006083,JN006094,JN006105,JN006116,JN006125,JN006136
crassicarpaATSC15698 JF420343,JF420122,JF420236
cultriformisCANB793341 JF420387,JF419954,JF420168,JF420494,JF420056,JF420278
cupularisCANB633912 JF420353,JF419922,JF420133,JF420459,JF420023,JF420247
cyclopsCANB793345 JF420354,JF419923,JF420134,JF420460,JF420024,JF420248
dealbataCANB738126 JF420421JF420202,JF420523,JF420089,JF420310
deaneiClarke20d JF420403,JF419971,JF420183,JF420506,JF420073,JF420294
decurrensCANB793354 JF420344JF420123,JF420237
dodonaeifolianindethanaNS‐8657 JN006084,JN006095,JN006106,JN006117,JN006126,JN006137
elataANBG632927 JF420369,JF419938,JF420149,JF420475,JF420039,JF420262
elongataClarke27e JF420405,JF419973,JF420185,JF420508,JF420075,JF420296
euthycarpaCANB793378 JF420391,JF419958,JF420172,JF420498,JF420060,JF420282
falcataClarke4f JF420340,JF419913,JF420119,JF420451,JF420014,JF420233
filicifoliaCANB633941 JN006085,JN006096,JN006107,JN006118,JN006127
fimbriataClarke26f JF420404,JF419972,JF420184,JF420507,JF420074,JF420295
flexifoliaCANB793390 JF420341,JF419914,JF420120,JF420452,JF420015,JF420234
floribundaANBG9611057 JF420371,JF419940,JF420151,JF420477,JF420041,
genistifoliaCANB793395 JF420348,JF419917,JF420128,JF420454,JF420019,JF420242
hakeoides CANB793281 JF420356,JF419925,JF420136,JF420462,JF420026,JF420250
holosericeaATSC15669 JF420346,JF419916,JF420126,JF420240
howittiiCANB793419 JF420410,JF419977,JF420190,JF420512,JF420079,JF420301
implexaClarke11i JF420401,JF419969,JF420182,JF420504,JF420071,JF420292
irrorataCANB793423 JF420386,JF419953,JF420167,JF420493,JF420055,JF420277
jibberdingensisAji2492 JN006086,JN006097,JN006108,JN006119,JN006128,JN006138
jonesiiMELU‐SRA20 JN006087,JN006098,JN006109,JN006129
leptocarpaATSC15478 JN006088,JN006099,JN006110,JN006130,JN006139
longifoliaJN782 JF420444,JF420006,JF420225JF420111,JF420332
longissima CANB793457 JF420428,JF419989,JF420209,JF420530,JF420094,JF420316
mearnsiiCANB793467 JF420379,JF419949,JF420160,JF420486JF420270
melanoxylonMtAnnanBG860538 JF420425,JF419987,JF420206,JF420527,JF420093,JF420314
mucronataCANB615743 JF420441,JF420002JF420542,JF420107,JF420329
murrayanaCANB793477 JF420429,JF419990,JF420210,JF420531,JF420095,JF420317
neriifoliaClarke8n JF420400,JF419968,JF420181,JF420503,JF420070,JF420291
oshanesiiClarke28o JN006089,JN006100,JN006111,JN006120,JN006131
Pararchidendron_pruinosumANBG820099 JF419980,JF420193,JF420515,JF420082,JF420304
Paraserianthes_lophanthaMEL2057862 JF420005,JF420224,JF420545,JF420110,JF420331
penninervisCANB793506 JF420385,JF419952,JF420125JF420018,JF420239
platycarpaKingsParkBG19920462item376 JN006090,JN006101,JN006112,JN006121,JN006132
podalyriifoliaANBG9406554 JF420374,JF419944,JF420155,JF420481,JF420045,JF420265
pravissimaCANB793515 JF420362,JF419931,JF420142,JF420468,JF420032,JF420255
prominensMtAnnanBG981404 JF420423JF420204,JF420525,JF420091,JF420312
pruinosaCANB793518 JF420392,JF419959,JF420173JF420061,JF420283
pubescensMEL2111926 JF420416,JF419984,JF420197,JF420519
pycnanthaCANB793526 JF420382JF420163,JF420489,JF420051,JF420273
pyrifoliaCANB793527 JF420345JF420124JF420017,JF420238
retinodesCANB587946 JF420422JF420203,JF420524,JF420090,JF420311
rigensCANB634045 JF420442,JF420003,JF420222,JF420543,JF420108,JF420330
salignaCANB634053 JF420443,JF420004,JF420223,JF420544,JF420109,
schinoidesCANB793542 JF420434,JF419996,JF420215,JF420536,JF420101,JF420323
stenophyllaCANB793555 JF420432,JF419994,JF420213,JF420534,JF420099,JF420321
suaveolensANBG643849 JF420375,JF419945,JF420156,JF420482,JF420046,JF420266
terminalis JM1915,JN088170,JN088174,JN088176,JN088178,JN088180
tripteraClarke18t JF420334,JF419907,JF420113,JF420446,JF420008,JF420227
vernicifluaMtAnnanBG13007 JF420414,JF419982,JF420195,JF420517,JF420084,
vestitaCANB793583 JF420438,JF419999,JF420219,JF420539,JF420105,JF420327
victoriaeAD99835210s51 JF420419JF420200JF420087,JF420308
viscidulaClarke1v JF420399,JF419967,JF420180,JF420502,JF420069,JF420290
AppendixS2Phylogeny‐freeanalysesofrelationshipsbetweenindividualreproductive
traitsinAustralianAcaciaspeciesandinvasivestatus(invasivevs.non‐invasive).
Generalizedlinearmodels(GLM)withnegativebinomialerrors(compatible1and
ompatible2)andbinomialerrors(seedmassandflower)wereusedforcontinuous
ariables,andχ²testswere inaryva
c
v
usedforb riables.
Continuousvariable
(Intercept)
co
Estimate
0.41022
Std.Error
.61695
zvalue
0.665
Pr(>|z
.506
|)
‐ 0 ‐ 0
mpatible1 0.01121 1.08908 0.010 0.992
(Intercept)
co
0.2839
.5004
0.567
.570
‐ 0 ‐ 0
mpatible2 ‐0.2048 0.9661 ‐0.212
0.832
(Intercept)
log10(
2.4477
.9134
2.680
.00737
5
‐ 0 ‐ 0
seedmass)
(Inte
0.8160
0.7149 1.142
0.2536
rcept)
flower
‐1.014795
0.005776
0.715022
0.136621
‐1.419
0.042
0.156
0.966
Binaryvariablen df χ² Pr(>F)
4
mature
c
d
39 1 6.8954 0.0086 2
ombined
ispersed
resprout
13
27
75
1
1
1
0.0903
0.4219
4.3428
0.7638
0.516
0.03717
AppendixS3TheeffectofindividualreproductivetraitsonAustralianAcaciaspecies’
invasivestatus(invasivevs.non‐invasive)usingphylogenyasacovariate.Generalized
linearmodels(GLM)withbinomialerrorswereusedforcontinuousvariables,andχ²
testswereusedforbinaryvariables(non‐phylogeneticanalyses).Phylogenetic
generalizedleastsquareswereu lvariasedforal
bles.
ror
Phylogenyfreeanalyses:
Continuousvariable
(Intercept)
co
Estima
.014
te
Std.Er
.360
zvalue
.745
Pr(>|z
.456
|)
1 1 0 0
mpatible1 2.757 5.287 0.522 0.602
(Intercept)
co
.365
.205
.133
.257
1 1 1 0
mpatible2 2.943
6.197 0.475
0.635
(Intercept)
log10(
2.0314
.1978
1.696
.0899
‐ 1 ‐ 0
seedmass)
(Inte
0.7227 0.9305 0.777 0.4373
rcept)
flower
‐0.63241
‐0.05485
0.83059
0.16598
‐0.761
‐0.330
0.446
0.741
Binaryvariablen df χ² Pr(>F)
mature
c
d
39 1 5.4408 0.01967
ombined
ispersed
resprout
13
27
75
1
1
1
1.9753
0.0246
5.6687
0.1599
0.8754
0.01727
Phyloge ra squaresneticgene lizedleast analyses:
Variable
(Intercept)
co
Estimate
.8141309
Std.Error
.5559794
tvalue
.4643185
Pr(>|z|)
.2170
0 0 1 0
mpatible1 0.0682263 0.6366747 0.1071603 0.9198
(Intercept)
co
.8238341
.4688128
.7572773
.1392
0 0 1 0
mpatible2 0.0728951 0.5269803 0.1383261 0.8954
(Intercept)
log10(
.3051452
.5123549
.595574
.5534
0 0 0 0
seedmass)
(Inte
0.2038274 0.2013822 1.012142 0.3151
rcept)
.4609615
.4456732
.0343037
1
.3057
0 0 1 0
flower
(In
‐0.0015824 0.0205977 ‐0.076823 0.9391
tercept)
.8133886
.3694093
.201863
.0375
0 0 2 0
mature2 ‐0.5525716 0.1735119 ‐3.184631 0.0040
(Intercept)
combined
O
0.9478223
0.0311115
0.4287861
.3014137
2.2104782
0.1032186
0.0580
.9203
utcrossing
‐ 0 ‐ 0
(Intercept)
dispers
.6840623
.3327042
.0560672
4
.0567
0 0 2 0
ednotbird ‐0.0081362 0.3437120 ‐0.023671 0.9814
(Intercept)
resproutTRUE
0.5374438
0.1228271
0.461042
0.114156
1.165713
1.075958
0.2496
0.2874
