Download An Experimental Test of Darwin`s Naturalization Hypothesis

vol. 175, no. 4
the american naturalist
april 2010
An Experimental Test of Darwin’s Naturalization Hypothesis
Lin Jiang,* Jiaqi Tan, and Zhichao Pu
School of Biology, Georgia Institute of Technology, Atlanta, Georgia 30332
Submitted October 20, 2009; Accepted November 9, 2009; Electronically published February 19, 2010
abstract: One of the oldest ideas in invasion biology, known as
Darwin’s naturalization hypothesis, suggests that introduced species
are more successful in communities in which their close relatives are
absent. We conducted the first experimental test of this hypothesis
in laboratory bacterial communities varying in phylogenetic relatedness between resident and invading species with and without a
protist bacterivore. As predicted, invasion success increased with phylogenetic distance between the invading and the resident bacterial
species in both the presence and the absence of protistan bacterivory.
The frequency of successful invader establishment was best explained
by average phylogenetic distance between the invader and all resident
species, possibly indicating limitation by the availability of the unexploited niche (i.e., organic substances in the medium capable of
supporting the invader growth); invader abundance was best explained by phylogenetic distance between the invader and its nearest
resident relative, possibly indicating limitation by the availability of
the unexploited optimal niche (i.e., the subset of organic substances
supporting the best invader growth). These results were largely driven
by one resident bacterium (a subspecies of Serratia marcescens) posting the strongest resistance to the alien bacterium (another subspecies
of S. marcescens). Overall, our findings support phylogenetic relatedness as a useful predictor of species invasion success.
Keywords: bacteria, biological invasions, competition, Darwin’s
naturalization hypothesis, microbial microcosms, phylogenetic
relatedness.
Introduction
What makes some nonnative species successful invaders
of communities to which they have been introduced? Our
ability to answer this question is key for designing effective
means to mitigate widespread biological invasions that
have profoundly changed the world’s many ecosystems
(Vitousek et al. 1996; Mack et al. 2000) and have incurred
considerable economic loss (Pimentel et al. 2005). Traditionally, this question has been tackled from two largely
disparate perspectives, with one aiming to identify specieslevel traits shared by successful invaders (Rejmanek 1996;
Rejmanek and Richardson 1996; Kolar and Lodge 2001)
* Corresponding author; e-mail: [email protected].
Am. Nat. 2010. Vol. 175, pp. 415–423. 䉷 2010 by The University of Chicago.
0003-0147/2010/17504-51669$15.00. All rights reserved.
DOI: 10.1086/650720
and the other searching for attributes of communities that
influence their invasibility (Rejmanek 1989; Levine and
D’Antonio 1999; Davis et al. 2000). The considerable
amount of work conducted within each framework so far,
however, has yielded few generalizations (Colautti et al.
2006; Moles et al. 2008). The lack of predictive power of
either approach has led to the proposition that our ability
to predict invasion success may be enhanced by considering the traits of invading species and resident communities together (e.g., Lodge 1993; Moles et al. 2008).
One idea that falls within the above proposition is Darwin’s naturalization hypothesis, which posits that naturalization of nonnative species is more likely in communities in which their close relatives are absent (Darwin
1859). This hypothesis arose from a related hypothesis of
Darwin (1859) that closely related species tend to possess
similar niches and hence perform similarly under the same
environmental conditions (for a recent empirical example,
see Brandt et al. 2009), translating into strong competition
imposed by resident species on closely related invaders
that reduces their success. These two hypotheses serve as
the conceptual base of contemporary phylogenetic community ecology: whether co-occurring species exhibit phylogenetic overdispersion (i.e., being less phylogenetically
related than expected by chance), as implied by the former
hypothesis, and whether species niche is phylogenetically
conserved, as suggested by the latter hypothesis, have been
major topics of this research field (reviewed in Webb et
al. 2002; Cavender-Bares et al. 2009). Within this context,
there have been multiple attempts at testing Darwin’s naturalization hypothesis (reviewed in Proches et al. 2008).
Together, these studies have reported positive (Daehler
2001; Duncan and Williams 2002), negative (Mack 1996;
Rejmanek 1996, 1998; Strauss et al. 2006), or no (Lambdon
and Hulme 2006; Ricciardi and Mottiar 2006) relationships between naturalization of introduced species and
their relatedness to native communities. These mixed results parallel those in studies of phylogenetic community
structure that have revealed various patterns of phylogenetic dispersion (summarized in Cavender-Bares et al.
2009). Strictly speaking, however, none of these studies
can be considered rigorous tests of Darwin’s naturalization
416 The American Naturalist
hypothesis. First, all these studies have assumed high niche
similarity between closely related species without directly
testing for it. Convergent evolution, if present (e.g., Losos
et al. 2003), may result in high similarity between distantly
related species that can confound the relationship between
relatedness and invasion. Second and more important, although not explicitly stated, Darwin’s naturalization hypothesis best applies to small spatial scales at which species
interact with each other, given the assumption of strong
competition between closely related species as its driving
mechanism. Previous tests of this hypothesis, however,
were all based on observations of exotic species in regions
much larger than the scale of species interactions (e.g.,
California [Rejmanek 1996, 1998; Strauss et al. 2006], Hawaii [Daehler 2001], and New Zealand [Duncan and Williams 2002]). As observational studies, their results are also
not immune to the influences of other confounding factors, such as habitat suitability (Mitchell et al. 2006), which
may vary within and between studies. Experiments that
manipulate relatedness in local communities differing little
in other aspects are needed to directly test the 150-yearold hypothesis.
Here we report on the first experimental test of Darwin’s
naturalization hypothesis, which subjected simple microbial communities containing one or multiple species of
naturally co-occurring bacteria with and without a bacterivorous protist species to the invasion of an alien bacterial species. Microbial invasion has received less attention
than that of animals and plants, but there is increasing
awareness of its commonness and impacts on native species and ecosystems (van der Putten et al. 2007). Insights
gained from studying invasions of microorganisms may
also apply to invasions of macroorganisms, since the two
types of organisms often exhibit similar ecological patterns presumably driven by similar ecological processes
(Horner-Devine et al. 2004, 2007; Green and Bohannan
2006; Martiny et al. 2006). The common practice of sequencing 16S rRNA genes for bacterial phylogeny also
facilitates the measurement of phylogenetic relatedness between bacterial species. We asked whether Darwin’s naturalization hypothesis can explain invading species establishment and abundance, two common metrics of invasion
success. The inclusion of a treatment of protistan bacterivory, an important source of bacterial mortality in natural systems (Sherr and Sherr 2002; Pernthaler 2005), allowed us to evaluate the hypothesis under conditions more
akin to natural situations.
Material and Methods
Microcosms used in this experiment were 25-mL plug seal
test tubes, each filled with 10 mL of medium. The medium
initially contained 0.367 g crushed protozoan pellet com-
posed of dried plant matter (Carolina Biological Supply
[CBS], Burlington, NC) and 1.67 g garden soil (extracted
from the Rutgers University Display Garden, New Brunswick, NJ) per liter of deionized water. This medium was
first autoclaved in large flasks and filtered with Whatman
GF/C glass microfiber filters (Whatman, Piscataway, NJ)
to remove undissolved particles. The filtrate, autoclaved
again in individual experimental microcosms, supplied diverse organic substances for bacterial growth and has been
used in our previous experiments (e.g., Jiang 2007). Each
microcosm also received an autoclaved wheat seed as the
additional carbon source.
We assembled resident bacterial communities from a
pool of four naturally co-occurring, culturable bacterial
strains, initially isolated from a small pond in the Rutgers
University Display Garden. The names of these strains
were unknown at the time of the experiment but were
later identified as Bacillus cereus, Bacillus pumilus, Frigoribacterium sp., and Serratia marcescens via sequence analysis of the 16S rRNA gene. Colonies of these four bacterial
species were readily distinguishable on nutrient agar plates.
A ciliated protist species, Tetrahymena pyriformis, obtained
in axenic cultures (grown in proteose peptone medium)
from CBS, was used as the predator of bacteria; T. pyriformis is capable of preying on a variety of bacteria, including all the species used in this experiment (Jiang 2007;
L. Jiang, personal observation). A separate S. marcescens
strain with distinct solid red colonies on agar plates, also
obtained from CBS, was used to invade resident communities. We chose S. marcescens as the invader because
it is known to colonize a wide variety of habitats and
because its red-colored colonies allow for easy identification. Before the experiment, the stock culture of each
bacterial species was grown in 0.8% nutrient broth.
We used a factorial experimental design with the relatedness of the invader to resident communities and the
presence/absence of T. pyriformis as two main factors. We
manipulated the degree of relatedness of the invader to
resident communities by varying species composition of
resident communities. To maximize the range of relatedness given the fixed species pool, our resident communities included every possible species composition (15
total: four one-species communities, six two-species communities, four three-species communities, and one fourspecies community) drawn from the four-species pool. We
replicated each treatment combination six times for a total
of 180 microcosms.
At the beginning of the experiment (day 0), we introduced resident bacterial species into their designated microcosms by transferring a small volume (!0.5 mL) of their
stock cultures with an inoculating loop. The initial population density likely differed between species, given that
there were possible differences in the carrying capacity of
Phylogenetic Relatedness and Invasion 417
their stock cultures and that the transferred volume was
the same for each species. Considering the short generation
times of bacteria and their low initial densities (compared
with their carrying capacities), however, this variation
should not affect experimental results obtained after many
bacterial generations (total experimental duration p 62
days). We introduced a small number of the bacterivore
T. pyriformis into their designated microcosms on day 7.
After allowing resident communities to equilibrate, on
days 42 and 43, we destructively sampled half the microcosms (three replicates of each treatment combination,
totaling 90 microcosms) to determine species composition
of the resident communities just before invasion. Samples
from the predation microcosms also confirmed that T.
pyriformis successfully established their populations in
each of these microcosms. We did not sample the other
half of microcosms that were scheduled to receive the invader, since this would almost inevitably introduce contamination. These remaining microcosms were invaded on
day 44, with the invader inoculated the same way as the
resident species. The experiment continued for another 18
days to allow for the establishment and spread of invader
populations within microcosms before final samples were
taken to estimate invader abundance. Bacterial densities
were determined by plating serially diluted samples (five
dilution levels from 102 to 106) onto agar plates and counting the number of colonies at appropriate dilution levels
after 6 days’ incubation. Microcosms were shaken at 200
rpm and incubated at room temperature throughout the
experiment. Sterile techniques were used during all inoculation and sampling events.
To estimate phylogenetic distance between the invader
and the resident species, we constructed phylogenies based
on bacterial 16S rRNA sequences (fig. 1). Briefly, we sequenced the 16S rRNA gene of each bacterial strain,
aligned the sequences using Clustal X (ver. 2.0; Larkin et
al. 2007), selected the best sequence evolution model—
GTR⫹G—using MrModeltest (ver. 2.3; Nylander 2004),
and built the phylogeny using the Bayesian method in
MrBAYES (ver. 3.1.2; Huelsenbeck and Ronquist 2001).
The phylogenetic distance between the invader and a resident species was obtained by summing lengths of the
intervening branches between the two species on the phylogeny. Following Strauss et al. (2006), we used two metrics
to represent the phylogenetic distance between the invader
and a resident community: the phylogenetic distance between the invader and its nearest relative in the resident
community (hereafter nearest phylogenetic distance) and
the average phylogenetic distance between the invader and
all species in the resident community (hereafter average
phylogenetic distance).
We estimated trait similarity between the invader and
the resident species on the basis of their ability to utilize
Figure 1: Phylogeny of the bacterial species used in the experiment,
constructed using the Bayesian method. Scores on nodes indicate the
percentages of bootstrap support (out of 75,000 replicates). The invader
represents a different strain of Serratia marcescens.
a variety of organic compounds on Biolog plates (Biolog,
Hayward, CA). Bacterial cultures were prepared and inoculated into wells of Biolog plates following the manufacturer’s instruction; Gram-positive and Gram-negative
strains were inoculated into their corresponding type of
plates. One resident species (Frigoribacterium sp.) could
not grow in the Biolog growth medium, and its carbon
usage pattern was not determined. For each of the rest of
the species, we scored positive results—indicating that the
species was able to use carbon sources in the wells—as 1
and negative results as 0. Before calculating trait distance,
we discarded data on substrates available only on either
Gram-positive or Gram-negative plates and limited our
analysis to data on the 55 substrates available on both
types of plate. The trait distance between the invader and
a resident species was calculated as the Euclidean distance
in the 55-dimension space.
418 The American Naturalist
We used simple and backward-selection multiple logistic
regressions to model the frequency of successful establishment of the invader as a function of realized nearest
phylogenetic distance, average phylogenetic distance, and
resident species richness. We included resident species
richness as a predictor variable in the regressions because
it has frequently been linked to invasion success (Fridley
et al. 2007). We viewed the invader establishment as successful if it attained above-zero density (results remained
the same when using the lowest positive invader density
as the threshold). Realized resident species richness of each
treatment was calculated as the average number of species
found in the three replicates destructively sampled before
invasion; the averaging was necessary because it prevented
the arbitrary assignment of measured species richness values (if different between replicates) to the remaining three
replicates to which the invader was introduced. Realized
nearest and average phylogenetic distances were calculated
similarly. We used simple and backward-selection multiple
linear regressions to model invader population density as
a function of the same three predictor variables. Before
performing multiple regressions, we discarded data from
communities that contained only a single resident species
before invasion, since average and nearest phylogenetic
distances were equal in these communities, confounding
the analyses. Simple linear regression was also used to
assess the relationship between invader-resident phylogenetic distance and trait distance. In all regressions, explanatory variables were deemed significant if P ≤ .05 and
marginally significant if .05 ! P ≤ .10; explanatory variables were retained in multiple regressions only if P ≤
.05. Analyses were done for the control and predation
treatments separately. Data on invader population density
were log10 transformed (log10 (x ⫹ 1)) to reduce heteroscedasity and improve normality. All analyses were conducted in SAS 9.1 (SAS Institute, Cary, NC).
Results
In the predator-free controls, the invader successfully established in all but three microcosms. Presumably because
of this low failure rate, the frequency of successful invader
establishment only marginally increased with average phylogenetic distance and was unaffected by nearest phylogenetic distance or species richness (table 1). A multiple
logistic regression eliminated all three explanatory variables as significant predictors of invader establishment.
Invader population density was also unaffected by species
richness (fig. 2; R 2 p 0.004, P p .6791) but increased with
nearest (fig. 2; R 2 p 0.429, P ! .0001) and average (fig. 2;
R 2 p 0.408, P ! .0001) phylogenetic distances. Nearest
phylogenetic distance was the only variable retained in the
multiple regression that best explained invader density.
Similar results emerged in the predation treatment,
where the invader successfully established in fewer (26 out
of 45) microcosms. The frequency of successful establishment increased significantly with increasing average phylogenetic distance but was again unaffected by nearest phylogenetic distance or species richness (table 2). A multiple
logistic regression retained average phylogenetic distance
as the only significant predictor of invader establishment.
Invader population density was again unaffected by species
richness (fig. 2; R 2 p 0.013, P p .4561) and increased with
nearest (fig. 2; R 2 p 0.764, P ! .0001) and average (fig. 2;
R 2 p 0.594, P ! .0001) phylogenetic distances. Nearest
phylogenetic distance was again the only significant variable retained in a multiple regression that explained invader density.
There was a significant positive relationship between
invader-resident phylogenetic distance and trait distance
(R 2 p 0.9997, P p .0114), indicating that carbon use patterns of these bacteria are phylogenetically conserved.
Discussion
Darwin’s naturalization hypothesis emphasizes the importance of the relatedness between invading and resident
species in determining invasion success at the scale of
species interactions. Observations of exotic species in various regions larger than this scale have provided mixed
support for this hypothesis (Mack 1996; Rejmanek 1996,
1998; Daehler 2001; Duncan and Williams 2002; Lambdon
and Hulme 2006; Ricciardi and Mottiar 2006; Strauss et
al. 2006). In particular, Diez et al. (2008) have shown that
the relationship between the abundance of exotic plant
species and that of their native congeners changed from
positive at the regional scale of Auckland, New Zealand,
to negative at the scale of ecosystems within the region;
however, the latter scale is still considerably larger than
the scale that species normally interact. Here, we took a
direct approach in examining the hypothesis by experimentally manipulating phylogenetic relatedness between
invading species and resident communities in small-scale
laboratory microcosms. In support of the hypothesis, our
results showed that invaders were more successful when
they were more distantly related to resident species in both
the presence and the absence of predators. Also as envisioned by Darwin (1859), we showed that resident species
more closely related to the invader shared more similar
traits with the invader.
Somewhat surprisingly, neither invader establishment
nor abundance was a significant function of resident species richness. This result is at odds with another classic
idea in invasion biology stating that diverse communities
are better at resisting invasion than their depauperate
counterparts (Elton 1958), which has so far received abun-
Phylogenetic Relatedness and Invasion 419
Table 1: Results of separate logistic regressions on invader establishment in
the control (no predation) treatment
Source
df
x2
P
Average phylogenetic distance
Nearest phylogenetic distance
Resident species richness
1
1
1
2.9762
.0033
1.8948
.0845
.9541
.1687
dant experimental support (Levine et al. 2002; Fridley et
al. 2007). Note that the opposite diversity-invasibility pattern has often been found in observation studies of natural
communities, which has largely been attributed to the operation of larger-scale mechanisms associated with spatial
heterogeneity (sensu Fridley et al. 2007). The principal
explanation for the negative diversity-invasibility relationship in diversity-manipulation experiments is that diverse
communities offer greater biotic resistance through more
resource use, leaving less resource available for invaders.
Our results, however, suggest that species richness may
not always be a good indicator of resource use that is most
relevant for invading species. The positive relationship between phylogenetic distance and invasion success found
in our experiment, coupled with the observed phylogenetic
niche conservatism, suggests that competition from closely
related resident species most effectively suppressed invading species by virtue of sharing similar resources, just as
envisioned by Darwin (1859). Here resident species richness failed to capture this important role of phylogenetic
relatedness and trait similarity in regulating invasion success, as indicated by its lack of relationship with average
(R 2 p 0.052, P p .1326 in the controls and R 2 p 0.073,
P p .0730 in the predation treatment) and nearest
(R 2 p 0.015, P p .4292 in the controls and R 2 p 0.051,
P p .1351 in the predation treatment) phylogenetic distances. We recognize that our relatively small diversity gradient, with the highest richness level lower than that of
the majority of natural communities, and the resultant
small phylogenetic gradient likely placed a constraint on
these relationships. It is possible that resident species richness and phylogenetic relatedness are more strongly related
in experiments encompassing broader diversity ranges,
given the simple scenario that increasing species richness
by chance alone increases the likelihood of including resident species that are closely related to the invading species
(essentially a sampling effect [sensu Tilman et al. 1997]
for closely related species). Reanalyzing data from previous
diversity-invasibility experiments using a phylogenetic approach will be able to test this hypothesis.
We found that average and nearest phylogenetic distances between the invader and resident communities best
explained invader establishment and abundance, respectively. The two phylogenetic distances provide comple-
95% odds ratio
confidence interval
.047, 1999.99
!.001, 1999.99
.396, 200.863
mentary information on the relatedness of invading and
resident species (Strauss et al. 2006): whereas average distance is indicative of the distinctness of the invading species relative to the entire resident community, nearest distance is a surrogate of niche differences between the
invading species and its closest resident relative (with the
assumption of phylogenetic niche conservatism). As such,
one would expect that resident communities with smaller
average phylogenetic distances from the invading species
have a smaller unoccupied niche left for the species, resulting in its lower establishment success. On the other
hand, one should also expect that after becoming established, invaders would attain small abundance if their optimal niche has already been occupied by their closely
related resident species. In our experimental microcosms
with continuous shaking (i.e., little opportunity for spatial
niches), the diverse organic substances in the medium that
can be used by the invader may constitute its niche,
whereas the subset of substances that support the best
growth of the invader may constitute its optimal niche.
The positive relationship between average phylogenetic
distance and invader establishment thus suggests that the
availability of the unexploited niche may have limited the
successful settlement of the invader. The positive relationship between nearest phylogenetic distance and invader
abundance suggests that the availability of the unexploited
optimal niche may have limited the abundance of the invader. Together, these findings support the proposition that
mechanisms regulating invasion success may differ between the establishment and spread stage of invasions (e.g.,
Kolar and Lodge 2001; Duncan et al. 2003; Diez et al.
2008). Note that at first sight, our results do not agree
with those of Strauss et al. (2006), who found that the
invasiveness of introduced grasses in California was better
explained by average phylogenetic distance. The analyses
of Strauss et al. (2006), however, were based on categorical
classification of species invasiveness, that is, whether introduced species have become widespread (invasive species) or not (noninvasive species). It remains to be seen
whether their results would change if actual species abundance data were used. The robustness of our results, of
course, also needs to be evaluated in other systems.
It should be noted that the invader and one resident
species in our experiment represent two subspecies of the
420 The American Naturalist
Figure 2: Relationship between realized nearest phylogenetic distance (A, B), realized average phylogenetic distance (C, D), and realized resident
species richness (E, F) and invader population density in the control (left column) and predation (right column) treatments. Data are shown along
with linear regression lines (if significant). Log-transformed invader density was originally measured as the number of colony-forming units per
milliliter.
same bacterium (Serratia marcescens) and that, consequently, our results were strongly influenced by the presence of the resident subspecies that posed the strongest
resistance to the alien subspecies. These warrant some clarifications. First, Darwin’s naturalization hypothesis relies
on the presence of niche differences that tend to be smaller
with increasing species relatedness. Given that bacterial
subspecies propagate asexually (i.e., no crossing between
subspecies) and may be ecologically distinct, and thus can
often be considered equivalent to species (e.g., Hodgson
et al. 2002; Brockhurst et al. 2007 [both studies reported
on invasion experiments involving bacterial subspecies]),
Darwin’s hypothesis should apply equally to both subspecies and species levels. Indeed, our analyses showed that
the resident and alien S. marcescens subspecies showed
modestly different carbon usage patterns: 12 of the 95
carbon substrates on the Gram-negative Biolog plate can
be used by one but not the other subspecies. Second, ob-
Phylogenetic Relatedness and Invasion 421
Table 2: Results of separate logistic regressions on invader establishment in the
predation treatment
Source
df
x2
P
Average phylogenetic distance
Nearest phylogenetic distance
Resident species richness
1
1
1
12.0949
.0085
.2832
.0005
.9264
.5946
served positive relationships between phylogenetic distance and invader abundance were largely driven by low
invader abundances in communities containing the resident S. marcescens subspecies. This is analogous to the
phenomenon that the presence of one or a few productive species, through the sampling effect, drives positive
diversity-productivity relationships in experimental studies of biodiversity and ecosystem functioning (Cardinale
et al. 2006). Also analogous to the sampling effect often
considered as a valid biodiversity mechanism (e.g., Tilman
et al. 1997; Jiang et al. 2008), the strong invasion resistance
of communities containing the resident species with the
shortest phylogenetic distance to the invader, largely
responsible for the observed phylogenetic relatednessinvasion relationships, may also be considered a valid phylogenetic relatedness effect. Nevertheless, we recognize that
phylogenetic distances between the invader and the other
three resident species lie within a narrow range (0.309–
0.398), making it difficult to assess the role of phylogenetic
relatedness beyond that of the most closely related resident
species. A recommendation for future experiments is thus
to use species assemblages with more uniformly distributed phylogenetic distances between invading and resident
species, which may likely be achieved with a larger resident
species diversity gradient.
Our study provides the first experimental evidence that
introduced species are less likely to establish self-sustaining
populations and tend to attain smaller population sizes
after successful establishment, in resident communities
that are more closely phylogenetically related to the introduced species. While these findings clearly support Darwin’s naturalization hypothesis, it is important to recognize that phylogenetic relatedness, in general, explained a
modest fraction of variation in invasion success even in
our highly simplified communities within relatively homogenous laboratory microcosms. We can think of at least
two reasons for why this is the case. First, although phylogenetic niche conservatism was demonstrated, our
choice of characterizing bacterial traits by their carbon
usage patterns on Biolog plates means that potential differences in other aspects of species niche (e.g., the ability
to cross feed) may have been overlooked. Under this possible scenario, phylogenetic relatedness between the invader and the resident species may not be a good indicator
95% odds ratio
confidence interval
1999.99, 1999.99
!.0001, 1999.99
.316, 1.936
of their trait similarity and therefore strength of competition. Indeed, there is evidence for closely related species
to be similar in some traits but differ in other traits (e.g.,
Cavender-Bares et al. 2004). Second, even if our characterization of phylogenetic niche conservatism was accurate, it may still not be straightforward to predict invasion
success on the basis of pairwise phylogenetic distances
alone, a surrogate of pairwise species interactions. This is
because indirect interactions may arise in communities
containing more than two species, resulting in profound
indirect effects on species and communities that may not
be readily predicted on the basis of pairwise interactions
(Wootton 1994). Nevertheless, our results suggest that the
phylogenetic distinctiveness of introduced species can be
a useful factor to consider when predicting their potential
success.
Acknowledgements
We thank W. Ryberg, C. Violle, and two anonymous reviewers for comments that significantly improved this
manuscript. This project is supported by a National Science Foundation grant (DEB-0640416) to L.J.
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Associate Editor: Susan Harrison
Editor: Ruth G. Shaw
1, Common barnacles Balanus eburneus of Gould.; 2, Balanus ovularis of Gould.; 3, free-swimming young of barnacle; 3a, young barnacles directly
after attachment; 4, sea anemone expanded Metridium marginatum; 5, sea anemone contracted; 6 and 7, periwinkle Littorina palliata; 8 and 9, cockle
Purpura lapillus; 9a, egg cases of the same; 10, mussel Mytilus edulis; 11, starfish Asterias vulgaris; 12, brittle starfish Ophiopholis bellis; 13, hermit
crab Bernhardus longicarpus; 14, Spirorbis nautiloides.
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