Are there any consistent predictors of invasion success?

 
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Biol Invasions (2008) 10:483–506
DOI 10.1007/s10530-007-9146-5

 ORIGINAL PAPER

Are there any consistent predictors of invasion success?
Keith R. Hayes Æ Simon C. Barry

Received: 4 September 2006 / Accepted: 26 July 2007 / Published online: 16 August 2007
Ó Springer Science+Business Media B.V. 2007

Abstract This article summarises the results of                  supported within plants but were either not
49 studies that together test the significance of 115            supported by independent data sets or contraindi-
characteristics in 7 biological groups: birds, finfish,          cated by datasets within or across other biological
insects, mammals, plants, reptiles/amphibians and                groups. Climate/habitat match is the only charac-
shellfish. Climate/habitat match, history of inva-               teristic that is consistently significantly associated
sive success and number of arriving/released                     with invasive behaviour (in this case exotic range
individuals are associated with establishment suc-               size) across biological groups. This finding, how-
cess in at least four independent data sets, both                ever, is not supported by two or more independent
within and across biological groups, and none are                data sets within any of the biological groups
contraindicated by other studies. In the introduced-             examined here. Within plants there are a suite of
invasive control group, two species level charac-                characteristics, predominately associated with
teristics—taxon and geographic range size—were                   reproduction, that are significantly associated with
significantly associated with establishment success              a range of invasion metrics, predominately abun-
across two biological groups. These characteristics,             dance in the invaded range. Nonef of these
however, were not supported by independent data                  characteristics, however, are supported across any
sets, or were contraindicated by these data sets,                other biological groups. We note the confounding
within the biological groups examined here. In the               effects of phylogeny, residence time and propagule
introduced-native control group, three species level             pressure and suggest that site- and taxa-specific
characteristics—geographic range size, leaf surface              analysis will provide further useful insights.
area and fertilisation system (monoecious, her-
maphroditic or dioecious)—were consistently                      Keywords Invasion  Establishment 
                                                                 Consistent  Prediction  Risk assessment

K. R. Hayes (&)
                                                                 Introduction
CSIRO Marine and Atmospheric Research,
GPO Box 1538, Hobart, TAS 7001, Australia
e-mail: keith.hayes@csiro.au                                     Successful biological invasions involve complex
                                                                 interactions between the invading species and the
S. C. Barry
                                                                 physical and biological characteristics of the recipient
CSIRO Mathematical and Information Sciences,
GPO Box 664, Canberra, ACT 2601, Australia                       environment. These interactions are made complex
e-mail: simon.barry@csiro.au                                     by the case-specific characteristics of the introduction

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484                                                                                       K. R. Hayes, S. C. Barry

event and a variety of ecological phenomena includ-      continued to follow the literature trail until no further
ing: positive feedback mechanisms (Noble 1989);          relevant publications were found.
Allee effects (Dennis 2002); behavioural changes            We deliberately excluded studies that postulate,
(Holway and Suarez 1999); genetic variability (Hold-     but do not statistically test, correlates of establish-
gate 1986); adaptation and phenotypic plasticity         ment or invasion success (Baker 1965; Arthington
(Rosecchi et al. 2001, Richards et al. 2006); the        and Mitchell 1986; Bruton 1986; Bazzaz 1986;
potential lag between establishment and invasion         Ehrlich 1989; Lodge 1993; Morton 1996; Arthington
(Sakai et al. 2001); and, cryptogenic species (Carlton   et al. 1999; Kailola 2000; Rosecchi et al. 2001;
1996).                                                   Heger and Trepl 2003; Martinez-Ghersa and Ghersa
   Over the years, invasion biologists have sought       2006). We also excluded studies that address
patterns and generality, or ecological rules of thumb    correlates associated with successful and unsuccess-
(Cote and Reynolds 2002), amongst this complex           ful introductions of native species translocated
myriad of variables. Some authors claim to be            within their native range (Griffith et al. 1989; Wolf
successful in this regard by identifying the general     et al. 1996), natural range expansions (O’Connor
characteristics of, for example, invasive plants         1986), invasive native species (Thompson et al.
(Arthington and Mitchell 1986; Baker 1965, 1986;         1995), and experimental studies using native species
Pysek 1998), fish (Arthington et al. 1999; Kailola       in the wild or non-native species under experimental
2000), molluscs (Morton 1996) and terrestrial verte-     conditions (Pattison et al. 1998; Hee et al. 2000;
brates (Ehrlich 1989). Furthermore the characteristics   Radford and Cousens 2000; Beggren 2001; Thomp-
identified by these authors are often used in risk       son et al. 2001; Grotkopp et al. 2002; Alroth et al.
assessment regimes designed to prevent deliberate        2003; Bellingham et al. 2004; Rehage and Sih
and accidental introductions of invasive species (see    2004).
the review by Ruesink et al. 1995).                         For each article included in the review we
   In this study we review the methods and results       recorded the data set(s), biological group and statis-
of a wide range of studies designed to identify          tical method(s), together with the correlates that were
statistically significant correlates of invasion or      examined. These correlates were then mapped to a
establishment success. Our primary aims are to           common classification to facilitate comparison and
synthesise data on the characteristics of invasive       synthesis. In a few cases we renamed correlates
species and identify consistent correlates—i.e.          identified in one study to facilitate grouping and
independently verified predictors of invasion or         comparison with other studies. In doing so we have
establishment success that are statistically signifi-    been careful to ensure that only biologically identical
cant either within or across different biological        characteristics are grouped. For example characteris-
groups.                                                  tics associated with fecundity such as the number of
                                                         seeds, eggs or pups and the size or mass of seeds or
                                                         eggs were grouped. If in doubt we left the original
Methods                                                  characteristic unchanged. All characteristics across
                                                         the studies where allocated to one of three species-,
This review follows the methodology of Kolar and         location- or event-level effect classes to distinguish
Lodge (2001) but extends their work by including 33      biological (species-level) characteristics from loca-
more studies. The references in this review were         tion- and event-level characteristics (Cassey et al.
collected by running the following Boolean search:       2005). We also grouped the species-level traits into
(attributes OR correlates OR characteristics) AND        the following 15 sub-groups: behaviour, diet, dis-
(alien OR non-native OR non-indigenous OR exotic)        persal, genetics, growth, human, leaf, lifespan, nest,
AND (invasion OR establishment) AND (success OR          other, reproduction, size, survival, taxon and
predict*), in the ‘‘topic’’ function of the ISI Web of   tolerance.
Science (http://portal.isiknowledge.com/portal.cgi?         The data set(s) in each article was classified into
DestApp=WOS&Func=Frame), obtaining the rele-             one of two control group categories: introduced
vant references and systematically searching their       versus invasive, or native versus invasive, and into
citations for further relevant publications. We          one of three introduction types: deliberate, accidental

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Predicting establishment and invasion success                                                               485

or deliberate and accidental, in order to highlight the   non-native ungulates in New Zealand, ant intercep-
different cases and control groups compared in each       tions in New Zealand and non-native reptiles and
study. We also noted which studies controlled for         amphibians in Florida, California and Great Britain
phylogeny. If authors performed their analysis with       (Appendix 1).
and without phylogenetic correction we only took the          The majority of studies (80%) compare intro-
results with correction. Finally, correlates of success   duced versus invasive species—i.e. species that
were distinguished for two transition states: intro-      successfully negotiated the introduced-established
duced—established and established—invasive (sensu         or established-invasive transition with those intro-
Kolar and Lodge 2001). For the latter we also             duced species that did not become established or
recorded how each study interpreted and used the          invasive. The remaining studies compare native
word ‘‘invasive’’.                                        species with successful non-native species (native
    The results of each study were entered into an        versus invasive). In most case these species were
excel spreadsheet and then grouped by transition step,    either deliberately introduced or a mixture of
characteristic, control group and (for the estab-         deliberate and accidental introductions. Analysis of
lished—invasive transition) meaning of the term           accidental introductions alone are rare—only 5 such
‘‘invasive’’. Once grouped we counted the number          studies are reported here.
of independent and overlapping data sets. Indepen-            The term ‘‘established’’ uniformly refers to self-
dent and overlapping data sets for the introduced-        maintaining populations of non-native species.
established transition were defined on the basis of the   Studies that address the introduction—establishment
biological group, control group and location where        transition and compare native versus invasive
they were studied (Fig. 1). For the established-          species report total sample sizes (N) that range
invasive transition, independence and overlap was         between 84 and 2,684 with a median of 292. This
additionally determined by the meaning of the word        is much larger than studies that compare introduced
‘‘invasive’’.                                             versus invasive species where the median total
                                                          sample size is 55. The median number of success-
                                                          fully established species (N+), however, is much
Results                                                   more similar between the two approaches (57 vs.
                                                          27), and the overall difference in range is also
Biological groups, group sizes and the tens rule          much less (Fig. 2). The first (third) quantile of
                                                          sample size changes from 45% (152%) to 19%
A total of 49 studies were eventually included in         (59%) between N and N+ in the introduced versus
this review. We believe that they represent a good        invasive category. This suggests that the proportion
proportion of studies presented in the English            of species successfully negotiating the introduc-
literature and are confident that any omission is         tion—establishment transition is higher than the
not the result of unintended bias on our part. Overall    10% suggested by the ‘‘tens rule’’ (Williamson
the studies address 115 correlates in 7 biological        1993). Note, however, that this dataset includes
groups: birds, finfish, insects, mammals, plants,         deliberately introduced species which might be
reptiles/amphibians and shellfish (the data set           expected to have a higher probability of establish-
and full list of correlates are available from the        ment. We did not test the ‘‘tens rule’’ for the
authors on request). Plants and birds feature prom-       established—invasive transition because the term
inently in the list, accounting for 76% of the            ‘‘invasive’’ is vague and context specific. The
studies examined here. Other aquatic and terrestrial      studies reviewed here use this term to refer to five
examples are relatively rare: 3 studies address non-      different metrics: size of the invaded range, abun-
native finfish introductions in California, Australia     dance in the invaded range, harmful properties,
and the Great Lakes, 3 address non-native shellfish       classified as ‘‘weedy’’ and spreading in the invaded
in the NE Pacific, Great Lakes and continental states     range. This reduces the total number of studies that
of the USA. The remaining studies address bio-            compare like with like to a maximum of only
control insects, non-native mammals in Australia,         seven for this transition.

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486                                                                                                                         K. R. Hayes, S. C. Barry

Fig. 1 Venn diagrams                         (a) Body mass: 6 overlapping data sets, 5 independant data sets
illustrating how overlapping
and independent data sets                                            Establishment: Introduced versus invasive species
are defined for the purposes
of this study, showing data
                                                                                Birds of the world
sets used to test the effect
of: (a) body mass; and (b)                                                                                                      Mammals
                                                                                                                               in Austtalia
date of introduction, on
establishment success of                                   Parrots of the world           Birds in New
                                                                                            Zealand
introduced versus invasive
species                                                                          Birds
                                                                                   in
                                                                                South.
                                                                                Florida

                                                                    Birds in
                                                                    Austtalia
                                                                                                                                   Ungulates
                                                                                     Land birds of the world                        in New
                                                                                                                                    Zealand

                                            (b) Date of introduction: 2 overlapping data sets, 5 independant data sets
                                                                      Establishment: Introduced versus invasive species

                                                                                                     Birds in                  Bivalves in
                                                                                                     Australia                   the NE
                                                                                                                                 Pacific

                                                                        Birds in New
                                                                          Zealand

                                                                                      Passerine
                                                                                     birds in New
                                                                                       Zealand

                                                                                                                 Birds in
                                                     Passerine                                                    South
                                                     birds in St.                                                Florida
                                                       Helena

Statistical methods and inconsistent results                          are used on various occasions, usually in concert
                                                                      with other methods. On one occasion the analysis
Most of the studies reviewed here adopt a single                      methods is unclear. Most study/statistical method
method, most notably linear models such as least                      combinations were conducted without phylogenetic
squares regression, generalised linear models with a                  control.
logit link function (logistic regression) or an identity                 For the introduced-established transition we
link function (multiple regression) (Quinn and                        found six examples of different results reported for
Keough 2002). More sophisticated extensions of                        the same characteristic in the same dataset using
this approach (generalised linear mixed models) are                   different statistical methods. All of these examples,
much rarer with only two examples in this review.                     however, can be attributed to the effect of phylo-
The next most popular method is the chi-squared                       genetic control, different sample sizes and (in the
test. The remaining techniques include a mixture of                   case of plumage dichromatism) the confounding
parametric and non-parametric approaches. These                       effect of propagule size (Table 1). We also

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Predicting establishment and invasion success                                                             487

Fig. 2 Sample sizes of
successfully established
(N+) species and total (N)
control population in 49
bio-invasion risk
assessment studies that
compared native versus
introduced species and
introduced versus invasive
species

discovered three examples of different results          biological groups, and none are contraindicated by
reported for the same characteristic in the same        other studies. The number of release/arrival
dataset using the same statistical method (Table 2).    attempts is consistently positively associated with
None of these examples, however, can be attributed      establishment in seven independent studies across
to the effects of phylogenetic control. The con-        four biological groups (finfish, insects, mammals
founding effect of propagule pressure explains the      and reptiles/amphibians) but is not consistent within
inconsistent results reported for geographic range      birds because it was found to be non-significant for
size in global bird introductions. The inconsistent     land birds in New Zealand by two studies
results reported for number of released/arrival         (Table 2).
attempts and migratory tendency also appear to be          In the introduced-invasive control group, only two
due to the confounding effects of propagule             species level characteristics—taxon and geographic
pressure.                                               range size—were consistently, significantly associ-
                                                        ated with establishment success across two biological
                                                        groups. These results, however, were not supported
Establishment success/failure                           by independent data sets, or were contraindicated by
                                                        these data sets, within the biological groups examined
Our analysis indicates that climate/habitat match,      here. In the introduced-native control group, three
history of invasive success and number of arriving/     species level characteristics—geographic range size,
released individuals are consistently associated with   leaf surface area and fertilisation system (monoe-
successful transition from introduction to establish-   cious, hermaphroditic or dioecious)—were consis-
ment (Table 3, Appendices 2, 3). All of these           tently supported within plants but were either not
characteristics have been found to be significantly     supported by independent data sets or contraindicated
associated with establishment success in at least       by datasets within or across other biological groups
four independent data sets, both within and across      (Table 3).

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488                                                                                                               K. R. Hayes, S. C. Barry

Table 1 Characteristics from the same data sets, analysed with different methods, that are inconsistently reported as positively (+),
negatively ( ) or not significantly (NS) associated with establishment success/failure
IDa       Characteristic              Data set                        Methodb                         CCc         PCd               +   NS

13        Altitude                    Plants of the British Isles     Sign test, CST                  NvI         Y                     1
49        Altitude                    Plants of the British Isles     CST                             NvI         N         1
13        Pollination type            Plants of the British Isles     Sign test, CST                  NvI         Y                     1
49        Pollination type            Plants of the British Isles     CST                             NvI         N                 1
13        Seed/egg mass/size          Plants of the British Isles     Sign test, CST                  NvI         Y                 1
49        Seed/egg mass/size          Plants of the British Isles     CST                             NvI         N                     1
17        Diet breadth/type           Birds in Australia              t-test                          IvI         Y                 1
34        Diet breadth/type           Birds in Australia              CST                             IvI         N                     1
9         Plumage dichromatism        Birds of the world              GLMM                            IvI         Y                     1
45        Plumage dichromatism        Birds of the world              GLM                             IvI         Y         1
32        Body length/size            Bivalves in NE Pacific          t-test (with bootstrap)         IvI         N                     1
42        Body length/size            Bivalves in NE Pacific          Mann–Whitney U-test             NvI         Y                 1
a
    ID: Reference identifier
b
  Statistical methods: Analysis of Variance (ANOVA), Correlation (Pearson/Spearman) (C), Correspondance Analysis (CA),
Categorical Regression Tree (CART), Chi-squared test (CST), Discriminant analysis (DA), Generalised Linear Model (GLM),
Generalised Linear Mixed Model (GLMM), Logistic regression (LR), Multiple regression (MR), Principal Components Analysis
(PCA), Regression (R)
c
    CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive
d
    PC: Phylogenetic control, Y = Yes, N = No

Table 2 Characteristics from the same data sets, analysed with the same method, that are inconsistently reported as positively (+),
negatively ( ) or not significantly (NS) associated with establishment success/failure
IDa        Characteristic                        Data set                      Methodb          CCc         PCd                 +       NS

3          Geographic range size                 Birds of the world            GLMM             IvI         Y                   1
9          Geographic range size                 Birds of the world            GLMM             IvI         Y                           1
46         No. of release/arrival attempts       Birds in New Zealand          LR, MR           IvI         N                           1
48         No. of release/arrival attempts       Birds in New Zealand          LR, MR           IvI         N                   1
46         Migratory tendency                    Birds in New Zealand          LR, MR           IvI         N                           1
48         Migratory tendency                    Birds in New Zealand          LR, MR           IvI         N           1
a
    ID: Reference identifier
b
  Statistical methods: Analysis of Variance (ANOVA), Correlation (Pearson/Spearman) (C), Correspondance Analysis (CA),
Categorical Regression Tree (CART), Chi-squared test (CST), Discriminant analysis (DA), Generalised Linear Model (GLM),
Generalised Linear Mixed Model (GLMM), Logistic regression (LR), Multiple regression (MR), Principal Components Analysis
(PCA), Regression (R)
c
    CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive
d
    PC: Phylogenetic control, Y = Yes, N = No

Invasive/not invasive                                                  biological groups (Table 4, Appendices 4, 5). This
                                                                       finding, however, is not supported by two or more
Climate/habitat match is the only characteristic that is               independent data sets within any of the biological
consistently significantly associated with invasive                    groups examined here. Within plants there are a suite
behaviour (in this case exotic range size) across                      of characteristics, predominately associated with

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Predicting establishment and invasion success                                                                                       489

Table 3 Characteristics that are significantly associated with establishment success in at least two independent data sets either
within or across biological groups
Level              Characteristic                                    NIDa           CCb             Within             Across

Location           Climate/habitat match                             6              IvI             B                  B, F, I, M, P, R
Species            History of invasive success                       8              IvI             B, F, P            B, F, M, P, R
Event              Number of released/arriving individuals           4              IvI             B                  B, F, I
Event              Number of release/arrival attempts                7              IvI                                F, I, M, R
Species            Taxon                                             5              IvI                                P, R
Species            Geographic range size                             8              IvI                                I, M
Species            Geographic range size                             8              NvI             P
Species            Leaf surface area                                 3              NvI             P
Species            Fertilisation system                              2              NvI             P
a
    NID: Number of independent data sets
b
  CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive. Biological groups are Birds (B), Finfish (F),
Insects (I), Mammals (M), Plants (P) and Reptiles/Amphibians (R)

Table 4 Characteristics that are significantly associated with invasion success in at least two independent data sets either within or
across biological groups
Level             Characteristic                             MIa                NIDb          CCc             Within             Across

Location          Climate/habitat match                      RS                 3             IvI                                B, M, P
Species           History of invasive success                W                  2             IvI             P
Event             Date of introduction                       A, W               2             IvI             P
Location          Biogeographic origin                       A                  2             IvI             P
Species           Length of juvenile period                  S                  2             IvI             P
Species           Growth form                                RS, A, H           2             NvI             P
Species           Asexual/vegetative reproduction            A                  2             IvI             P
Species           Length of flowering period                 A                  2             IvI             P
Species           Flowering season                           A                  2             IvI             P
a
    MI: Meaning of invasive, W = Weedy, RS = Range size (exotic), A = Abundance, S = Spreading, H = Harmful
b
    NID: Number of independent data sets
c
  CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive. Biological groups are Birds (B), Mammals
(M) and Plants (P)

reproduction, that are significantly associated with a                  This typically leads to successful species (N+) being
range of invasion metrics, predominately abundance                      over-represented. Thus the structure of the data
in the invaded range, in two independent data sets.                     collection method is a retrospective case/control
None of these characteristics, however, are supported                   sample and not a random sample of a defined
across any other biological groups and in all cases                     population. Standard analysis shows that regression
there are only two independent data sets (Table 4).                     parameters may be consistently estimated from such
                                                                        data but that the intercept (i.e. the rate of invasion)
Discussion                                                              cannot (Breslow and Clayton 1993).
                                                                           The definition of the control sample has an
Population and confounding factors                                      important bearing on the interpretation of the results
                                                                        of the studies reported here. Native species do not
The data reviewed here is not a random sample of                        make a good control sample if the aim of the analysis
all species arriving at a particular transition, but                    is to predict which species will invade (rather than
rather a sample defined by what data is available.                      understand why species are successful) because

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490                                                                                           K. R. Hayes, S. C. Barry

differences may arise through biogeography rather than       (Lockwood et al. 2005). Deliberate introductions, by
a direct ecological process. Studies that compare native     definition, imply a high degree of human-mediated
versus invasive species are afforded the luxury of larger    selection. This selection process is controlled by
datasets (Fig. 1) but they are forced to untangle            historical, economic and sociological factors that may
differences attributable to biogeography and invasion        have no relevance to the biological characteristics of
ecology. Studies that compare introduced versus inva-        successful invasive species (for relevant examples see
sive species face similar problems if the case and/or        Cassey et al. 2004b and Garcia-Berthou et al. 2005). In
control set do not represent unbiased samples from           accidental introductions there is a direct, and arguably
relevant populations (see also Simons 2003; Cassey           more relevant, interaction between the species-level
et al. 2004b). If the model is being used as a predictive    characteristics of an invasive species (e.g. planktonic
tool to support decisions about the deliberate importa-      larval duration) and other historical or economic factors
tion of a species, then the unsuccessful species (N )        (e.g. the advent of ballast water transport). An exam-
should be an unbiased sample of species that had an          ination of significant invasion characteristics in
opportunity to invade but were unsuccessful. This data       accidental introductions may therefore provide further
is sometimes available for deliberate introductions (e.g.    useful insights into important species-level characteris-
Kolar and Lodge 2001; Cassey et al. 2004b), and in           tics. Future studies of deliberately introduced species
these instances a regression-based approach is appro-        should consider the confounding effects of propagule
priate so long as the control set (N+) is an unbiased        pressure before reporting other statistically significant
sample of species that had an opportunity to invade and      characteristics of invasion success.
were successful. This allows the model to be used to
assess the relative risk of a new deliberate introduction.
For accidental introductions, however, unbiased reports      Statistical methods
of successful (N+) and unsuccessful (N ) species are
generally not available because unsuccessful accidental      All of the statistical methods reviewed here estimate
introductions are not comprehensively reported and           how the probability of success responds conditionally
patterns of trade vary through time. As a consequence        on covariates, usually with regression-based techniques.
very few studies to date have quantitatively addressed       They vary, however, in the flexibility of their response
accidental introductions. This is an important avenue        surface with respect to the covariates. The simplest
for future research.                                         approaches, such as a t-test, measure significant differ-
    If the case and control data are truly a random          ences in the marginal success rate. More complex
sample from the population of successful and unsuc-          approaches, such as regression trees, model sets of
cessful invaders then phylogenetic correction is not         variables jointly, allow for discontinuities in the
technically necessary. The sample might not be a             response surface and can flexibly map interactions.
representative sample of all species, but may be                The appropriateness of an analytic approach
representative of the species that can potentially           depends on a number of limitations. The primary
invade a location. If the sample is biased, a correction     issue in this context is that the number of successful
for this bias may be needed and this could be based          species (N+) is typically small (Fig. 1). The com-
on the phylogeny. In this context the use of gener-          plexity of regression models must therefore be
alised linear mixed models with phylogenetic group           carefully controlled to avoid over fitting (Burnham
as a random effect would appear to provide a better          and Anderson 2002; Caley and Kuhnert 2006). The
foundation for prediction than phylogenetic contrasts,       ‘‘best’’ model (in terms of appropriateness to new
because the theoretical basis of General Linear              data) will depend on the underlying population and
models is more clearly defined.                              the particular sample at hand but a few general
    Phylogeny, however, is only one of a number of           recommendations can be made. First, modern statis-
potentially important sources of bias. Other important       tical arguments suggest it is better to model variables
sources are residence time (Richardson and Pysek             jointly rather than one at a time, as this allows the
2006) and propagule pressure as demonstrated by the          analysis to consider the effects of confounding
inconsistent results reported here. Propagule pressure is    variables and provides more concise results with a
particularly important for deliberate introductions          clearer interpretation. Regression techniques that

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Predicting establishment and invasion success                                                                  491

allow multiple variables are therefore better. The         spread in the exotic range but only within plants—
second recommendation is to use a technique, such as       none of these were consistently significant within or
regression trees, that allow for more complex              across any other biological groups (Table 4, Appen-
response surfaces. This last recommendation is             dix 4).
tempered by the typical data limitations (ten obser-           Cote and Reynolds (2002) suggest that general,
vations per variable is a useful rule of thumb—see         and sometimes broadly applicable, ecological rules of
van Belle 2002 ), and the need to provide an easily        thumb may exist. This statement is supported by the
interpretable output. Generalised linear mixed models      recent discovery of consistent spread dynamics in
are a promising analytical technique in this context,      invasive species in widely different contexts (Arim
because they can simultaneous control for confound-        et al. 2006). The collective research effort of the
ing variables, in an easily interpreted manner.            many studies reviewed here, however, suggest that
                                                           across (within) biological groups, there are only three
                                                           (nine) species-level characteristics that distinguish
Sample sizes and consistently significant                  successful established/invasive species from unsuc-
characteristics                                            cessful species, and the results within biological
                                                           groups have to date only been demonstrated for
Kolar and Lodge (2001) examined the characteristics        plants. The most significant result of this analysis is
that were quantitatively associated with establishment     that two location- and event-level correlates—cli-
and invasion success in 16 studies. We have repeated       mate/habitat match and number of introduced
their analysis but added another 33 studies and            organisms—are consistently significant predictors of
distinguished taxonomic group, population, statistical     successful establishment across all of the biological
method and sample size. Kolar and Lodge (2001)             groups in which they have been tested. Modern
note that the probability of establishment of non-         biology accepts that on average organisms are
native birds increases with the number of individuals      adapted to particular conditions and are not generally
released and the number of release events, and the         able to vary this adaptation arbitrarily. Hence some
probability of invasion by non-native plants increases     degree of climate/habitat match is a pre-requisite of
if the species has a history of invasion and reproduces    establishment success and the number of introduced
vegetatively. We found that the probability of             organisms (and number of repeat introductions) is an
establishment increases with the number of individ-        important determinant of the likelihood of establish-
uals released across all the biological groups (birds,     ment success, so long as the climate/habitat is
finfish and insects) where this correlate has been         suitable. Our results confirm that other species-level
tested (Table 3, Appendix 2). This conclusion is also      characteristics of establishment and invasion success
supported by many of the studies excluded from this        exist but (with the exception of a history of invasion
review (Williamson 1993; Ruesink et al. 1995; Wolf         success) they have only been demonstrated in plants.
et al. 1996; Gruestad 1999; Beggren 2001; Alroth           It is important to note here that the various interpre-
et al. 2003) and a quantitative meta-analysis of bird      tations of the term ‘‘invasive’’ significantly reduces
introductions (Cassey et al. 2005). The number of          the number of studies that compare like with like, and
release events was consistently statistically associated   this reduces our ability to identify patterns within the
with establishment success across finfish, insects,        results of the available literature.
mammals and reptiles/amphibians but was not con-               The concept that some species are inherently more
sistently significant within birds (Tables 2, 3,           invasive is at the core of the models reviewed here.
Appendix 2). We found that a history of invasive           This effect is obviously confounded with the impact
success was positively and consistently associated         of other variables that are correlated with invasion
with establishment success, across all of the biolog-      success. A history of invasion success is a consis-
ical groups examined here (except insects where it         tently significant correlate of establishment success
was not tested), but not with invasion success where       across all biological groups in which it has been
it was only consistently associated with weed status       tested but for the established—invasion transition it is
in plants. We found four reproduction-related char-        only consistently significant within plants. Again, this
acteristics to be the associated with abundance and        is probably due to the various different interpretations

                                                                                                        123
492                                                                                          K. R. Hayes, S. C. Barry

of the word ‘‘invasive’’ (see also Ricciardi and Cohen     very few species-level characteristics have been
2007). When this variable is analysed marginally (i.e.     independently verified as significant, and none of
on its own) a significant result indicates that some       these are consistently significant in more than two
other unknown covariate(s) has a consistent effect on      biological groups. This conclusion suggests that
invasion success. When analysed jointly with the           species-level characteristics that are predictive of
other covariates a significant result indicates that the   successful invaders are likely to be taxa-specific
pattern of success cannot be purely explained by the       (Sakai et al. 2001) and even site-specific (Lake and
available covariates.                                      Lewisham 2004). It is important to note that this
   The results of this review suggest that we still have   conclusion is not new. Plant ecologists often empha-
a long way to go to identify broadly applicable            sise habitat/species interactions and the important
species-level characteristics of successful invasive       role of location-level characteristics such as land-
species. Cassey et al. (2005) criticise ‘vote-counting’    scape and community variables, in invasion success
reviews, such as this one, on the grounds that they are    (Thompson et al. 1995; Radford and Cousens 2000;
qualitative and subjective, recommending a quantita-       Allen 2006; Bass et al. 2006; Richardson and Pysek
tive meta-analysis. We do not dispute the advantages       2006). Heger and Trepl (2003) refer to these as ‘‘key-
of a quantitative meta-analysis, but we see no reason      lock models’’ noting that there are no (species-level)
why a quantitative meta-analysis, applied across the       characteristics common to all invaders. Rather each
groups reviewed here, would reverse our conclusions.       characteristics has to suit the specific conditions of
We do not claim that particular characteristics are not    the new environment.
significantly associated with invasion/establishment          If this conclusion is true it imposes a tension
success in certain contexts. Instead, we argue that        between the generality and the accuracy of risk
most of these characteristics are not consistently         assessment schemes that rely on species-level char-
significant in different contexts. Furthermore, meta-      acteristics to prevent introductions. Furthermore this
analysis is applicable to multiple studies of the same     conclusion cautions studies that promote risk assess-
population in similar contexts. In this study we           ments, based largely on species-level characteristics,
examined multiple populations in various contexts.         as accurate and readily generalised to new locations
Hence, it is not immediately clear to us that the          (see for example Krivanek and Pysek 2006). In some
primary assumption of meta-analysis—that the stud-         cases the apparent effect of accuracy and generality
ies examined are sufficiently similar for pooled data      may be the result of no more than a simple statistical
to produce meaningful results—would be applicable          overfit in the risk assessment model (Caley and
here.                                                      Kuhnert 2006). Risk managers can, however, place
                                                           much greater faith in assessments that identify
                                                           potential invaders based on climate/habitat matching,
Risk management implications                               invasion history and number of released/arriving
                                                           individuals. These correlates must be interpreted
Invasion biologists continue to suggest and test a         carefully and are not foolproof but they are consis-
large number of species-level characteristics in           tently supported by the available literature.
search of a set that predicts invasion and establish-
ment success, and risk analysts continue to                Acknowledgements We would like to thank Piers Dunstan,
                                                           Ullrika Sahlin, Nic Bax, Mary Bomford, Dave Richardson and
recommend their use in risk management schemes             four anonymous reviewers for comments on earlier drafts of
(Stohlgren and Schnase 2006). To date, however,            this article.

123
Appendix 1   Biological groups, transition step, statistical method, sample size, introduction mode and control class in 49 biological invasion studies
              a                                                                                                                                  g
      Group        Reference                                IDb        Methodc                        Sd        Ne              N+f          N           TIh    CCi   PCj

      B            Allen (2006)                              1         LR                             E               46           26         20         D/A    IvI   N
                   Brooke et al. (1995)                      6         Kruska–Wallis test, C          E               31            5         26         D      IvI   N
                   Cassey et al. (2004a)                     9         GLMM                           E              416                                 D      IvI   Y
                   Cassey et al. (2004b)                    10         GLM                            E               54           38                    D      IvI   N
                   Cassey (2001)                            11         LR, MR                         E              118           31         87         D      IvI   N
                   Duncan et al. (1999)                     16         R, t-test                      I                            34                    D      NvI   Y
                   Duncan et al. (2001)                     17         LR, MR, t-test                 E               55           19         36         D/A    IvI   Y
                                                                                                      I                            19                    D/A    IvI   Y
                   Duncan (1997)                            18         LR, MR                         E               42           15         27         D      IvI   Y
                   Green (1997)                             22         LR, MR                         E               47           21         26         D      IvI   Y
                                                                                                                                                                            Predicting establishment and invasion success

                   Moulton and Pimm (1986)                  33         CST                            E               50           33         17         D      IvI   Y
                   Newsome and Noble (1986)                 34         CST                            E              107           59         48         D      IvI   N
                   Sorci et al. (1998)                      46         LR, MR                         E               47           27         20         D      IvI   N
                   Veltman et al. (1996)                    48         LR, MR                         E               79           27         52         D      IvI   N
                   Sol and Lefebvre (2000)                  44         LR, MR                         E               39           19         20         D      IvI   Y
                   Sol et al. (2002)                        45         GLM                            E               69           51         18         D/A    IvI   Y
                   Blackburn and Duncan (2001)               3         GLMM                           E              389                                 D/A    IvI   Y
                   Cassey (2002)                            12         GLM                            E                                                  D/A    IvI   Y
      F            Kolar and Lodge (2002)                   25         DA                             E               45           24         21         D/A    IvI   N
                                                                                                      I                            24                    D/A    IvI   N
                   Marchetti et al. (2004)                  31         LR, MR                         E              109           71         38         D/A    IvI   N
                                                                                                      I                            71                    D/A    IvI   N
                   Bomford and Glover (2004)                 4         PCA , CART, LR, C              E               50           31         19         D/A    IvI   N
      I            Lester (2005)                            27         Kruskal–Wallis test            E                            17         43         A      IvI   N
                   Crawley (1987)                           14         Unclear                        E              225         146          79         D      IvI   N
      M            Forsyth et al. (2004                     20         LR, MR                         E               40           23         17         D      IvI   Y
                                                                                                      I                            23                    D      IvI   Y
                   Forsyth and Duncan (2001)                19         LR, CST                        E               14           11            3       D      IvI   N
                                                                                                                                                                            493

123
Appendix 1 continued
                                                                                                                                   494

                                                                                                             g
      Groupa      Reference                         IDb   Methodc                 Sd   Ne         N+f    N       TIh   CCi   PCj

123
      P           Cadotte and Lovett-Doust (2001)    7    LR, CST                 E      1,330     484           D/A   NvI   N
                  Crawley et al. (1996)             13    GLM, Sign test, CST     E      2,684                   D/A   NvI   N
                  Daehler, (1998)                   15    CST                     I    240,100    1041           D/A   NvI   Y
                  Goodwin et al. (1999)             21    LR, MR                  E         165                  D/A   NvI   Y
                  Hamilton et al. (2005)            23    LR, MR                  I         152                  D/A   IvI   Y
                  Lake and Lewishman (2004)         26    CST, ANOVA              E          86     57    29     A     NvI   N
                                                                                  I                 57           A     NvI   N
                  Lloret et al. (2005)              28    GLM                     I         354                  D/A   IvI   Y
                  Lonsdale (1994)                   29    Kruska–Wallis test      I         466     61   405     D     IvI   N
                  Maillet and Lopez-Garcia (2000)   30    CA, CART                I          78                  D/A   IvI   N
                  Perrins et al. (1992)             35    PCA, HCA, DA            I          49                  A/D   NvI   N
                  Pysek (1998)                      36    MR, ANOVA               E      8,003                   A/D   IvI   Y
                                                                                  I      8,003                   A/D   IvI   Y
                  Reichard and Hamilton (1997)      37    DA, CART                E           .    235   114     D     IvI   N
                  Reichard (2001)                   38    DA, CART, t-test, CST   E         416    418   270     D     IvI   N
                  Rejmanek and Richardson (1996)    39    DA                      I          24     12    12     D     IvI   N
                  Rejmanek (1996)                   40    DA                      I          24     12           D     IvI   N
                  Richardson et al. (1990)          41    CA                      I          60                  D     IvI   N
                  Scott and Panetta (1993)          43    LR, MR                  I         242     36   206     D     IvI   N
                  Sutherland (2004)                 47    CST                     I                              D/A   IvI   N
                  Williamson and Fitter (1996)      49    CST                     E         974    112           D/A   NvI   N
                  Baruch and Goldstein (1999)        2    ANOVA                   E          84     30    34     D/A   NvI   N
                  Cadotte et al. (2006)              8    GLM                     I         846    272           D/A   IvI   Y
                                                     8    CST                     I      1,153                   D/A   IvI   Y
      R/A         Bomford et al. (2005)              5    LR, t-test, CST         E         163     60   103     D/A   IvI   N
                                                                                                                                   K. R. Hayes, S. C. Barry
Appendix 1 continued
                                                                                                                                             g
      Groupa          Reference                                IDb        Methodc                       Sd       Ne              N+f     N       TIh        CCi         PCj

      S               Miller et al. (2002)                     32         t-test (with bootstrap)       E              38           3    35      A          IvI         N
                      Roy et al. (2002)                        42         Mann-Whitney U-test           E             292           7            A          NvI         Y
                                                               42         LR, MR                        I              13           9        4   A          IvI         N
                      Keller et al. (2007)                     24         LR, CART                      I              15           5    10      A          IvI         N
                                                                                                                       18           8    10      A          IvI         N
      a
          Biological groups: Birds (B), Finfish (F), Insects (I), Mammals (M), Plants (P), Reptiles/Amphibians (R/A) and Shellfish (S)
      b
          ID: Reference identifier
      c
        Statistical methods: Analysis of Variance (ANOVA), Correlation (Pearson/Spearman) (C), Correspondance Analysis (CA), Categorical Regression Tree (CART), Chi-squared
      test (CST), Discriminant analysis (DA), Generalised Linear Model (GLM), Generalised Linear Mixed Model (GLMM), Logistic regression (LR), Multiple regression (MR),
      Principal Components Analysis (PCA), Regression (R)
                                                                                                                                                                               Predicting establishment and invasion success

      d
          Step: Transition step, E = Introduced to established, I = Established to invasive
      e
          N: Number of species or individual organisms
      f
          N+: Number of successful (established or invasive) species or individuals
      g
          N : Number of unsuccessful (established or invasive) species or individuals
      h
          TI: Type of introduction, D = deliberate introduced, A = Accidentally introduced
      i
          CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive
      j
          PC: Phylogenetic control, Y = Yes, N = No
                                                                                                                                                                               495

123
496                                                                                                        K. R. Hayes, S. C. Barry

Appendix 2 Number of studies where establishment success/failure is reported as positively (+), negatively ( ) or not significantly
(NS) associated with event- and location-level characteristics in at least two independent data sets
Characteristic                           NODa        NIDb        CCc       Group                      IDd               +       NS

Date of introduction                     2           5           IvI       Birds                       1                        1
                                                                                                       6                        1
                                                                                                      18                1
                                                                                                      22                        1
                                                                                                      34         1
                                                                           Shellfish                  42                        1
No. of arriving/released individuals     5           5           IvI       Birds                       9                1
                                                                                                      11                1
                                                                                                      17                1
                                                                                                      18                1
                                                                                                      22                1
                                                                                                      34                1
                                                                                                      44                1
                                                                                                      45                1
                                                                                                      46                1
                                                                                                      48                1
                                                                           Finfish                    31                1
                                                                           Insects                    14                1
No. of release/arrival attempts          3           7           IvI       Birds                      11                1
                                                                                                      17                1
                                                                                                      18                1
                                                                                                      19                1
                                                                                                      22                        1
                                                                                                      46                        1
                                                                                                      48                1
                                                                           Finfish                     4                1
                                                                           Insects                    14                1
                                                                           Mammals                    20                1
                                                                           Reptiles/Amphibians         5                1
Biogeographic origin                     2           4           IvI       Birds                       1                        1
                                                                                                      22                        1
                                                                                                      33                        1
                                                                           Plants                     36                1
                                                                                                      37                1
                                                                                                      38                        1
Climate/habitat match                    2           6           IvI       Birds                       3                1
                                                                                                      17                1
                                                                                                      34                1
                                                                           Finfish                     4                1
                                                                           Insects                    27                1
                                                                           Mammals                    20                1
                                                                           Plants                     36                1
                                                                           Reptiles/Amphibians         5                1

123
Predicting establishment and invasion success                                                                                       497

Appendix 2 continued
Characteristic                               NODa      NIDb        CCc         Group                        IDd                +    NS

Mainland/island                              2         2           IvI         Birds                         3                      1
                                                                                                             9                      1
                                                                                                            34                      1
                                                                               Plants                       38                      1
Great circle distance                        0         2           IvI         Birds                        11                 1
                                                                               Finfish                      31                      1
a
    NOD: Number of overlapping data sets
b
    NID: Number of independent data sets
c
    CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive
d
    ID: Reference identifier

Appendix 3 Number of studies where establishment success/             in at least two independent data sets for: (a) birds; (b) finfish;
failure is reported as positively (+), negatively ( ) or not          (c) insects; (d) mammals; (e) plants; (f) reptiles/amphibians;
significantly (NS) associated with species-level characteristics      and, (g) shellfish
CGa                     Characteristic                        NODb         NIDc          CCd          IDe                  +        NS

(a) Birds
Diet                    Diet breadth/type                     6            5             IvI           1                            1
                                                                                                       9                            1
                                                                                                      10                   1
                                                                                                      11                   1
                                                                                                      12                            1
                                                                                                      17                   1
                                                                                                      34                            1
                                                                                                      45                            1
                                                                                                      48                            1
Dispersal               Migratory tendency                    5            2             IvI           9                            1
                                                                                                      10                   1
                                                                                                      12          1
                                                                                                      17                            1
                                                                                                      44          1
                                                                                                      45                            1
                                                                                                      46                            1
                                                                                                      48          1
Human                   Human commensal                       2            2             IvI          17                            1
                                                                                                      45                   1
Nest                    Nest type                             4            2             IvI          12                            1
                                                                                                      34                            1
                                                                                                      44                            1
                                                                                                      45          1
Other                   History of invasive success           2            8             IvI           6                   1
                                                                                                      17                   1

                                                                                                                           123
498                                                                         K. R. Hayes, S. C. Barry

Appendix 3 continued
CGa              Characteristic                   NODb   NIDc   CCd   IDe               +        NS

Reproduction     Age at maturity/first breeding   0      2      IvI   10                         1
                                                                      12                         1
                 Broods per season                0      2      IvI   17                         1
                                                                      34                         1
                                                                      48                         1
                 Incubation period                4      2      IvI    3                         1
                                                                      10                         1
                                                                      12                         1
                                                                      17                         1
                 Mating system                    0      2      IvI   46                         1
                 No. of seeds/eggs/pups           4      7      IvI    3                         1
                                                                      11                         1
                                                                      17                         1
                                                                      22                         1
                                                                      34                         1
                                                                      45                         1
                                                                      48       1
                 Parental care                    2      3      IvI   45                         1
                                                                      46                         1
Size             Body length/size                 2      6      IvI   11                         1
                                                                      48                         1
                 Body mass                        6      5      IvI    1                         1
                                                                       3                         1
                                                                       9                         1
                                                                      10                         1
                                                                      12                1
                                                                      17                1
                                                                      22                         1
                                                                      45                         1
                                                                      46                         1
                                                                      48                         1
Taxon            Taxon                            2      5      IvI    3                         1
                                                                      48                         1
Tolerance        Geographic range size            7      8      IvI    3                1
                                                                       9                         1
                                                                      10                         1
                                                                      11                1
                                                                      12                         1
                                                                      17                         1
                                                                      33                1
                                                                      48                         1
(b) Finfish
Diet             Diet breadth/type                6      5      IvI   25                         1
                                                                      31                         1

123
Predicting establishment and invasion success                                       499

Appendix 3 continued
CGa                 Characteristic                NODb   NIDc   CCd   IDe       +   NS

Human               Human commensal               2      2      IvI   25            1
Lifespan            Lifespan                      0      4      IvI   25            1
                                                                      31        1
Other               History of invasive success   2      8      IvI    4        1
                                                                      25        1
                                                                      31        1
Reproduction        Incubation period             4      2      IvI   25            1
                    Length of juvenile period     0      3      IvI   25            1
                    No. of seeds/eggs/pups        4      7      IvI   25            1
                                                                      31            1
                    Parental care                 2      3      IvI   25            1
                                                                      31        1
Size                Body length/size              2      6      IvI    4            1
                                                                      25            1
                                                                      31            1
                    Seed/egg mass/size            0      2      IvI   25            1
Taxon               Taxon                         2      5      IvI    4        1
                                                                      25            1
Tolerance           Geographic range size         7      8      IvI    4        1
                                                                      25            1
                                                                      31    1
                    Physiological tolerances      0      3      IvI    4            1
                                                                      25        1
                                                                      31        1
(c) Insects
Lifespan            Lifespan                      0      5      IvI   14        1
Size                Body length/size              2      6      IvI   27            1
Tolerance           Geographic range size         7      8      IvI   14        1
(d) Mammals
Diet                Diet breadth/type             6      5      IvI   20            1
Dispersal           Migratory tendency            5      2      IvI   20    1
Lifespan            Lifespan                      0      4      IvI   19        1
                                                                      20            1
Other               History of invasive success   2      8      IvI   20        1
Reproduction        Length of juvenile period     0      3      IvI   20            1
                    Mating system                 0      2      IvI   19            1
                    No. of seeds/eggs/pups        4      7      IvI   19            1
                                                                      20            1
Size                Body mass                     6      5      IvI   19            1
                                                                      20            1
Tolerance           Geographic range size         7      8      IvI   20        1

                                                                                123
500                                                                             K. R. Hayes, S. C. Barry

Appendix 3 continued
CGa                 Characteristic                    NODb   NIDc   CCd   IDe               +        NS

(e) Plants
Growth              Growth form                       0      4      NvI    7                         1
                                                                          21                         1
                                                                          26                1
                                                                          49                1
Leaf                Leaf surface area                 0      3      NvI    2                1
                                                                          26                1
                                                                          49                1
Lifespan            Monocarpy                         0      2      NvI   49                         1
Other               History of invasive success       2      8      IvI   37                1
                                                                          38                1
Reproduction        Asexual/vegetative reproduction   0      2      NvI    7                         1
                                                                          26                1
                    Fertilisation system              0      2      NvI    7                1
                                                                          49                1
                    Length of flowering period        0      3      NvI    7                1
                                                                          21                1
                                                                          26       1
                    Length of juvenile period         0      3      IvI   38       1
                    No. of seeds/eggs/pups            0      2      NvI    7                         1
                                                                          49                         1
                    Pollination type                  0      2      NvI    7                         1
                                                                          13                         1
                                                                          49                1
Size                Canopy/stem/plant height          0      3      NvI   13                1
                                                                          21                1
                                                                          26                         1
                                                                          49                1
                    Seed/egg mass/size                0      2      IvI   38                         1
                                                                    NvI   13                1
                                                                          26                         1
                                                                          49                         1
Taxon               Taxon                             2      4      NvI    7                1
                                                             5      IvI   36                1
Tolerance           Geographic range size             6      7      NvI   13                1
                                                                          21                1
                                                      7      8      IvI   38                         1
(f) Reptiles/Amphibians
Other               History of invasive success       2      8      IvI    5                1
Taxon               Taxon                             2      5      IvI    5                1

123
Predicting establishment and invasion success                                                                                  501

Appendix 3 continued
CGa                  Characteristic                  NODb            NIDc            CCd          IDe                 +         NS

Tolerance            Geographic range size           7               8               IvI           5                            1
(g) Shellfish
Size                 Body length/size                2               6               IvI          32                            1
                                                                                                  42                  1
a
    CG: Species-level category
b
    NOD: Number of overlapping data sets
c
    NID: Number of independent data sets
d
    CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive
e
    ID: Reference identifier

Appendix 4 Number of studies where invasion success/failure is reported as positively (+), negatively ( ) or not significantly (NS)
associated with event- and location-level characteristics in at least two independent data sets
Characteristic                               NODa        NIDb        CCc        Group        MId         IDe              +     NS

Date of introduction                         0           2           IvI        Plants       A            8      1
                                                                                                         23      1
                                                                                             W           30      1
                                                                                                         43      1
No. of arriving/released individuals         0           2           IvI        Birds        RS          17                     1
                                                                                Finfish      RS, A       31                     1
No. of release/arrival attempts              0           2           IvI        Birds        RS          17                     1
                                                                                Mammals      RS          20               1
Biogeographic origin                         0           2           IvI        Plants       A            8               1
                                                                                             RS, A       36               1
Climate/habitat match                        0           3           IvI        Birds        RS          17               1
                                                                                Mammals      RS          20               1
                                                                                Plants       RS, A       36               1
a
    NOD: Number of overlapping datasets
b
    NID: Number of independent data sets
c
    CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive
d
    MI: Meaning of invasive, A = Abundance, W = Weedy, RS = Range size (exotic)
e
    ID: Reference identifier

Appendix 5 Number of studies where invasion success/failure              two independent data sets for: (a) birds; (b) finfish; (c)
is reported as positively (+), negatively ( ) or not significantly       mammals; (d) shellfish; and, (e) plants
(NS) associated with species-level characteristics in at least
CGa                  Characteristic                          NODb        NIDc      CCd      MIe           IDf             +     NS

(a) Birds
Diet                 Diet breadth/type                       0           4         IvI      RS            17                    1
Dispersal            Migratory tendency                      0           2         IvI      RS            17              1
Reproduction         No. of seeds/eggs/pups                  0           3         IvI      RS            17                    1
                                                                                   NvI      RS            16              1

                                                                                                                          123
502                                                                          K. R. Hayes, S. C. Barry

Appendix 5 continued
CGa             Characteristic                NODb   NIDc   CCd   MIe        IDf           +      NS

Size            Body mass                     0      2      IvI   RS         17                   1
                Seed/egg mass/size            0      2      NvI   RS         16                   1
Tolerance       Geographic range size         0      3      IvI   RS         17            1
(b) Finfish
Diet            Diet breadth/type             0      4      IvI   RS, A      31     1
                                                                  RS, H      25                   1
Growth          Growth rate                   0      2      IvI   RS, H      25                   1
Lifespan        Lifespan                      0      2      IvI   RS, A      31            1
                                              3      3      IvI   RS, H      25                   1
Other           History of invasive success   0      2      IvI   RS, A      31            1
Reproduction    No. of seeds/eggs/pups        0      2      IvI   RS, A      31                   1
Size            Body length/size              2      2      IvI   RS, H      25                   1
                Seed/egg mass/size            0      3      IvI   RS, H      25                   1
Taxon           Taxon                         0      2      IvI   RS, H      25                   1
Tolerance       Geographic range size         0      3      IvI   RS, A      31                   1
(c) Mammals
Diet            Diet breadth/type             0      4      IvI   RS         20            1
Dispersal       Migratory tendency            0      2      IvI   RS         20                   1
Lifespan        Lifespan                      0      2      IvI   RS         20     1
Other           History of invasive success   0      2      IvI   RS         20                   1
Reproduction    Length of juvenile period     3      2      IvI   RS         20     1
                No. of seeds/eggs/pups        0      3      IvI   RS         20            1
Size            Body mass                     0      2      IvI   RS         20     1
Tolerance       Geographic range size         0      3      IvI   RS         20                   1
(d) Shellfish
Lifespan        Lifespan                      3      3      IvI   H          24                   2
Reproduction    Fertilisation system          2      2      IvI   H          24                   2
Size            Body length/size              2      2      IvI   H          24                   2
(e) Plants
Growth          Growth form                   0      2      NvI   RS, A, H   15            1
                                                                             26            1
                Growth rate                   0      2      IvI   W          29                   1
Leaf            Leaf surface area             0      2      IvI   A          23                   1
                                                                             28            1
                                                            NvI   W          35                   1
                                                                  RS, A, H   26            1
Lifespan        Lifespan                      3      3      IvI   H          47            1
                                                                  S          39                   1
                                                                             40                   1
Other           History of invasive success   0      2      IvI   W          30            1
                                                                             43            1

123
Predicting establishment and invasion success                                                                                     503

Appendix 5 continued
CGa                  Characteristic                      NODb        NIDc       CCd         MIe           IDf              +      NS

Reproduction         Annual versus perennial             0           2          IvI         A              8                      1
                                                                                                          28                      1
                     Asexual/vegetative reproduction     0           2          IvI         A              8               1
                                                                                                          28               1
                                                                                NvI         W             35                      1
                                                                                            RS, A, H      26               1
                     Fertilisation system                0           2          IvI         A              8               1
                                                                                                          28                      1
                                                         2           2          IvI         H             47               1
                     Length of flowering period          0           2          IvI         A              8               1
                                                                                                          28               1
                                                                                NvI         W             35                      1
                                                                                            RS, A, H      26               1
                     Length of juvenile period           3           2          IvI         S             39       1
                                                                                                          40       1
                                                                                                          41       1
                     No. of seeds/eggs/pups              0           2          IvI         A              8                      1
                     Flowering season                    0           2          IvI         A              8               1
                                                                                                          28               1
Size                 Canopy/stem/plant height            0           3          IvI         A              8                      1
                                                                                                          23                      1
                                                                                                          28                      1
                     Seed/egg mass/size                  0           2          IvI         A             23       1
                                                                                                          28                      1
                                                                                            W             29                      1
                                                                     3          NvI         W             35                      1
                                                                                            RS, A, H      26                      1
Taxon                Taxon                               0           2          IvI         W             43               1
a
    CG: Species-level category
b
    NOD: Number of overlapping datasets
c
    NID: Number of independent data sets
d
    CC: Control class, I v I = Introduced versus invasive, N v I = Native versus invasive
e
    MI: Meaning of invasive, A = Abundance, W = Weedy, RS = Range size (exotic), S = Spreading, H = Harmful
f
    ID: Reference identifier

                                                                     Arthington AH, Mitchell DS (1986) Aquatic invading species,
References                                                                pp 34–53. In: Groves RH, Burden JJ (eds) Ecology of
                                                                          biological invasions: an Australian perspective. Australian
Allen CR (2006) Predictors of introduction success in the south           Academy of Science, Canberra, Australia
     Florida avifauna. Biol Invasions 8:491–500                      Arthington AH, Kailola PJ, Woodland DJ, Zalucki JM (1999)
Alroth P, Alatalo RV, Holopainen A, Kumpulainen T, Suhonen                Baseline environmental data relevant to an evaluation of
     J (2003) Founder population size and the number of                   quarantine risk potentially associated with the importation
     source populations enhance colonisation success in water             to Australia of ornamental finfish. Report to the Australian
     striders. Oecologia 137:617–620                                      Quarantine and Inspection Service, Agriculture, Fisheries
Arim M, Abades SR, Neill PE, Lima M, Marquet PA (2006)                    and Forestry, Canberra, Australia, 444 pp
     Spread dynamics of invasive species. Proc Natl Acad Sci         Baker HG (1965) Characteristics and modes of origin of
     103(2):374–378                                                       weeds. In: Baker HG, Stebbins CL (eds) The genetics of

                                                                                                                          123
504                                                                                                        K. R. Hayes, S. C. Barry

     colonising species. Academic Press, New York, USA,            Cassey P (2002) Life history and ecology influences estab-
     pp 147–169                                                         lishment success of introduced land birds. Biol J Linn Soc
Baker HG (1986) Patterns of plant invasion in North America.            76:465–480
     In: Mooney HA, Drake JA (eds) Ecological of Biological        Cassey P, Blackburn TM, Sol D, Duncan RP, Lockwood JL
     Invasions of North America and Hawaii. Springer-Verlag,            (2004a) Global patterns of introduction effort and estab-
     New York, pp 44–57                                                 lishment success in birds. Proc R Soc Lond B (Suppl.)
Baruch Z, Goldstein G (1999) Leaf construction costs, nutrient          271:S405–S408
     concentration and net CO2 assimilation of native and          Cassey P, Blackburn TM, Jones KE, Lockwood JL (2004b)
     invasive species in Hawaii. Oecologia 121:183–192                  Mistakes in the analysis of exotic species establishment:
Bass DA, Crossman ND, Lawrie SL, Lethbridge MR (2006)                   source pool designation and correlates of introduction
     The importance of population growth, seed dispersal and            success among parrots (Aves: Psittaciformes) of the
     habitat suitability in determining plant invasiveness.             world. J Biogeogr 31:277–284
     Euphytica 148:97–109                                          Cassey P, Blackburn TM, Duncan RP, Lockwood JL (2005)
Bazzaz FA (1986) Life history of colonising plants: some                Lessons from the establishment of exotic species: a
     demographic, genetic and physiological features, pp 97–            meta-analytical case study using birds. J Anim Ecol
     110. In Mooney HA, Drake JA (eds) Ecology of biolog-               74:250–258
     ical invasions of North America and Hawaii. Springer-         Cote IM, Reynolds JD (2002) Predictive ecology to the rescue?
     Verlag, New York, USA                                              Science 298:1181–1182
Beggren A (2001) Colonisation success in Roesel’s bush             Crawley MJ (1987) What makes a community invasible? In:
     cricket Metrioptera roeseli: the effects of propagule size.        Gray AJ, Crawley MJ, Edwards PJ (eds) Colonization,
     Ecology 82(1):274–280                                              succession and stability. The 26th Symposium of the
Bellingham PJ, Duncan RP, Lee WG, Buxton RP (2004)                      British Ecological Society held Jointly with the Linnaean
     Seedling growth rate and survival do not predict inva-             Society of London. Blackwell Science, Oxford, England,
     siveness in naturalised woody plants in New Zealand.               pp 429–453
     Oikos 106:308–316                                             Crawley MJ, Harvey PH, Purvis A (1996) Comparative ecol-
Blackburn TM, Duncan RP (2001) Determinants of establish-               ogy of the native and alien floras of the British Isles.
     ment success in introduced birds. Nature 414(8):195–197            Philos Trans R Soc Lond B 351:1251–1259
Bomford M, Kraus J, Braysher M, Walter L, Brown L (2005)           Daehler CC (1998) The taxonomic distribution of invasive
     Risk assessment model for the import and keeping of                angiosperm plants: ecological insights and comparison to
     exotic reptiles and amphibians. Bureau of Rural Sciences,          agricultural weeds. Biol Conserv 84:167–180
     Canberra, Australia, 110 pp                                   Dennis B (2002) Allee effects in stochastic populations. Oikos
Bomford M, Glover J (2004) Risk assessment model for import             96:389–401
     and keeping of exotic freshwater and estuarine finfish.       Duncan RP (1997) The role of competition and introduction
     Bureau of Rural Sciences, Canberra, Australia, 125 pp              effort in the success of passiform birds introduced to New
Burnham KP, Anderson DR (2002) Model selection and mul-                 Zealand. Am Nat 149:903–915
     timodel inference: a practical information-theoretic          Duncan RP, Blackburn TM, Veltman CJ (1999) Determinants
     approach. Springer-Verlag, New York, USA                           of geographical range sizes: a test using introduced New
Breslow N, Clayton D (1993) Approximate inference in gen-               Zealand birds. J Anim Ecol 68:963–975
     eralized linear mixed models. J Am Stat Assoc 88:9–25         Duncan RP, Bomford M, Forsyth DM, Conibear L (2001) High
Brooke RK, Lockwood JL, Moulton MP (1995) Patterns of                   predictability in introduction outcomes and the geo-
     success in passeriform bird introductions on Saint Helena.         graphical range size of introduced Australian birds: a role
     Oecologia 103:337–342                                              for climate. J Anim Ecol 70:621–632
Bruton MN (1986) Life-history styles of invasive fishes in         Ehrlich PR (1989) Attributes of invaders and the invading
     Southern Africa, pp 201–208. In: MacDonald IAW,                    process: vertebrates. In: Drake JA (ed) Biological inva-
     Kruger FJ, Ferrar AA (eds) The ecology and management              sions: a global perspective. John Wiley & Sons Ltd.,
     of biological invasions in Southern Africa. Oxford                 Chichester, England, pp 315–327
     University Press, Cape Town, South Africa                     Forsyth DM, Duncan RP (2001) Propagule size and the relative
Cadotte MW, Lovett-Doust J (2001) Ecological and taxonomic              success of exotic ungulate and bird introductions to New
     differences between native and introduced plants of                Zealand. Am Nat 157(6):583–595
     southwestern Ontario. Ecoscience 8(2):230–238                 Forsyth DM, Duncan RP, Bomford M, Moore G (2004)
Cadotte MW, Murray BR, Lovett-Doust J (2006) Evolutionary               Climatic suitability, life-history traits, introduction effort,
     and ecological influences of plant invader success in the          and the establishment and spread of introduced mammals
     flora of Ontario. Ecoscience 13(3):388–395                         in Australia. Conserv Biol 18(2):557–569
Caley P, Kuhnert PM (2006) Application and evaluation of           Garcia-Berthou E, Alcaraz C, Pou-Rivira Q, Zamora L Co-
     classification trees for screening unwanted plants. Aust           enders G, Feo C (2005) Introduction pathways and
     Ecol 31:647–655                                                    establishment rates of invasive aquatic species in Europe.
Carlton JT (1996) Biological invasions and cryptogenic spe-             Can J Fish Aquat Sci 62:453–463
     cies. Ecology 77(6):1653–1655                                 Goodwin BJ, McAllister AJ, Fahrig L (1999) Predicting
Cassey P (2001) Determining variation in the success of New             invasiveness of plant species based on biological infor-
     Zealand land birds. Glob Ecol Biogeogr 10:161–172                  mation. Conserv Biol 13(2):422–426

123
Predicting establishment and invasion success                                                                                    505

Green RE (1997) The influence of numbers released on the            Lonsdale WM (1994) Inviting trouble: introduced pasture
     outcome of attempts to introduce exotic bird species to             species in northern Australia. Aust J Ecol 19:345–354
     New Zealand. J Anim Ecol 66:25–36                              Maillet J, Lopez-Garcia C (2000) What criteria are relevant for
Griffith B, Scott JM, Carpenter JW, Reed C (1989) Translo-               predicting the invasive capacity of a new agricultural
     cation as a species conservation tool: status and strategy.         weed? The case of invasive American species in France.
     Science 245:477–480                                                 Weed Res 40:11–26
Grotkopp E, Rejmanek M, Rost TL (2002) Toward a causal              Marchetti MP, Moyle PB, Levine R (2004) Invasive species
     explanation of plant invasiveness: seedling growth and              profiling? Exploring the characteristics of non-native
     life-history strategies of 29 pine (Pinus) species. Am Nat          fishes across invasion stages in California. Freshw Biol
     159(4):396–419                                                      49:646–661
Greustad FS (1999) Experimental invasions using biological          Martinez-Ghersa MA, Ghersa CM (2006) The relationship of
     control introductions: the influence of release size on the         propagule pressure to invasion potential in plants.
     chance of population establishment. Biol Invasions                  Euphytica 148:87–96
     1:313–323                                                      Memmott J, Craze PG, Harman M, Syrett P, Fowler SV (2005)
Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC,                   The effect of propagule size on the invasion of an alien
     Harris CJ, Licari D (2005) Life-history correlates of plant         insect. J Anim Ecol 74:50–62
     invasiveness at regional and continental scales. Ecol Lett     Miller AW, Hewitt CL, Ruiz GM (2002) Invasion success:
     8:1066–1074                                                         does size really matter? Ecol Lett 5:159–162
Hee JJ, Holway DA, Suarez AV, Case TJ (2000) Role of                Morton B (1996) The aquatic nuisance species problem: a
     propagule size in the success of incipient colonies of the          global perspective and review. In: D’itri F (ed) Zebra
     invasive argentine ant. Conserv Biol 14(2):559–563                  mussels and other aquatic nuisance species. Ann Arbor
Heger T, Trepl L (2003) Predicting biological invasions. Biol            Press, New York, USA, pp 1–54
     Invasions 5:313–321                                            Moulton MP, Pimm SL (1986) Species introductions to
Holdgate MW (1986) Summary and conclusions: characteris-                 Hawaii. In: Mooney HA, Drake JA (eds) Ecology of
     tics and consequences of biological invasions. Philos               biological invasions of North America and Hawaii.
     Trans R Soc Lond B314:733–742                                       Springer-Verlag, New York, USA, pp 231–249
Holway DA, Suarez AV (1999) Animal behaviour: an essential          Newsome AE, Noble IR (1986) Ecological and physiological
     component of invasion biology. Trends Ecol Evol                     characters of invading species. In: Groves RH, Burdon JJ
     14(8):328–330                                                       (eds) Ecology of biological invasions: an Australian per-
Kailola PJ (2000) Development of an alert list for non-native            spective. Australian Academy of Science, Canberra,
     freshwater fishes. Final report to Environment Australia,           Australia, pp 1–20
     Patricia Kailola, Consultant, Newnham, Tasmania,               Noble IR (1989) Attributes of invaders and the invading pro-
     Australia, 43 pp                                                    cess: terrestrial and vascular plants. In: Drake JA (ed)
Keller RP, Drake JM, Lodge DM (2007) Fecundity as a basis                Biological invasions: a global perspective. John Wiley &
     for risk assessment of non-indigenous freshwater mol-               Sons Ltd., Chichester, England, pp 301–313
     luscs. Conserv Biol 21(1):191–200                              O’Connor RJ (1986) Biological characteristics of invaders
Kolar CS, Lodge DM (2002) Ecological predictions and risk                among bird species in Britain. Philos Trans R Soc Lond
     assessment for alien fishes in North America. Science               B314:589–598
     298:1233–1236                                                  Pattison RR, Goldstein G, Ares A (1998) Growth, biomass
Kolar CS, Lodge DM (2001) Progress in invasion biology:                  allocation and photosynthesis of invasive and native
     predicting invaders. Trends Ecol Evol 16(4):199–204                 Hawaiian rainforest species. Oecologia 117:449–459
Krivanek M, Pysek P (2006) Predicting invasion by woody             Perrins J, Williamson W, Fitter A (1992) Do annual weeds
     species in a temperate zone: a test of three risk assessment        have predictable characters? Acta Ecol 13(5):517–533
     schemes in the Czech Republic (Central Europe). Divers         Pysek P (1998) Is there a taxonomic pattern to plant invasions.
     Distrib 12:319–327                                                  Oikos 82:282–294
Lake JC, Lewisham MR (2004) Invasion success of exotic              Quinn GP, Keough MJ (2002) Experimental design and data
     plants in natural ecosystems: the role of disturbance, plant        analysis for biologists. Cambridge University Press,
     attributes and freedom from herbivores. Biolo Conserv               Cambridge, England, 556 pp
     117:215–226                                                    Radford IJ, Cousens RD (2000) Invasiveness and comparative
Lester PJ (2005) Determinants for the successful establishment           life-history traits of exotic and indigenous Senecio species
     of exotic ants in New Zealand. Divers Distrib 11:                   in Australia. Oecologia 125:531–542
     279–288                                                        Rehage JS, Sih A (2004) Dispersal behaviour, boldness, and
Lloret F, Medial F, Brundu G, Camarda I, Moragues E, Rita J,             the link to invasiveness: a comparison of four Gambusia
     Lambdon P, Hulme PE (2005) Species attributes and                   species. Biol Invasions 6(3):379–391
     invasion success by alien plants on Mediterranean islands.     Reichard SH (2001) The search for patterns that enable pre-
     J Ecol 93:512–520                                                   diction of invasion. In: Groves RH, Panetta FD, Virtue JG
Lockwood JL, Cassey P, Blackburn T (2005) The role of                    (eds) Weed risk assessment. CSIRO publishing, Canberra,
     propagule pressure in explaining species invasions.                 Australia, pp 10–19
     Trends Ecol Evol 20(5):223–228                                 Reichard SH, Hamilton CW (1997) Predicting invasions of
Lodge DM (1993) Biological invasions: lessons for ecology.               woody plants introduced into North America. Conserv
     Trends Ecol Evol 8:133–137                                          Biol 11:193–203

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