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Perspectives
in Plant Ecology,
Evolution and
Systematics
Perspectives in Plant Ecology, Evolution and Systematics 11 (2009) 311–320
www.elsevier.de/ppees
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Rethinking the common garden in invasion research
Kirk A. Moloneya,, Claus Holzapfelb, Katja Tielbörgerc,
Florian Jeltschd, Frank M. Schurrd
a
Department of Ecology, Evolution and Organismal Biology, Iowa State University, 253 Bessey Hall, Ames, IA 50011-1020, USA
Department of Biological Sciences, Rutgers University, Newark, NJ 07102, USA
c
Department of Plant Ecology, University of Tübingen, D-72076 Tübingen, Germany
d
Plant Ecology and Nature Conservation, Universität Potsdam, D-14469 Potsdam, Germany
b
Received 18 December 2008; received in revised form 24 April 2009; accepted 31 May 2009
Abstract
In common garden experiments, a number of genotypes are raised in a common environment in order to quantify
the genetic component of phenotypic variation. Common gardens are thus ideally suited for disentangling how genetic
and environmental factors contribute to the success of invasive species in their new non-native range. Although
common garden experiments are increasingly employed in the study of invasive species, there has been little discussion
about how these experiments should be designed for greatest utility. We argue that this has delayed progress in
developing a general theory of invasion biology. We suggest a minimum optimal design (MOD) for common garden
studies that target the ecological and evolutionary processes leading to phenotypic differentiation between native and
invasive ranges. This involves four elements: (A) multiple, strategically sited garden locations, involving at the very
least four gardens (2 in the native range and 2 in the invaded range); (B) careful consideration of the genetic design of
the experiment; (C) standardization of experimental protocols across all gardens; and (D) care to ensure the biosafety
of the experiment. Our understanding of the evolutionary ecology of biological invasions will be greatly enhanced by
common garden studies, if and only if they are designed in a more systematic fashion, incorporating at the very least
the MOD suggested here.
r 2009 Rübel Foundation, ETH Zürich. Published by Elsevier GmbH. All rights reserved.
Keywords: Adaptive evolution; Common garden; Lythrum salicaria; Maron effect; Phenotypic plasticity; Invasive species
Introduction
Invasive species are those naturalized, exotic species
that exhibit runaway population growth once they
become established and are generally considered to be
of environmental concern due to their impact on native
species and ecosystem services (Randall, 1996; Vitousek
Corresponding author.
E-mail address: kmoloney@iastate.edu (K.A. Moloney).
et al., 1996; Kolar and Lodge, 2001; Pimentel et al.,
2001; Sakai et al., 2001; Lockwood et al., 2007).
Invasion biology aims to explain why certain species
that are inconspicuous in their native range become
successful invaders after introduction to new non-native
ranges. This phenomenon might be explained by purely
ecological differences in environmental conditions between the native and the introduced range. However,
there is growing interest in quantifying the extent to
which differential success of a species in its native and
1433-8319/$ - see front matter r 2009 Rübel Foundation, ETH Zürich. Published by Elsevier GmbH. All rights reserved.
doi:10.1016/j.ppees.2009.05.002
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Table 1.
K.A. Moloney et al. / Perspectives in Plant Ecology, Evolution and Systematics 11 (2009) 311–320
Experimental designs utilized in invasive plant studies incorporating a common garden approach.
Garden location Provenance of plants Replication within location Number of Studies Hypotheses Examined
(number of studies)
N
I
N&I
I
No
Yes
0
0
NA
NA
N&I
No
Yes
5
3
EICA(5)a
PPvAE(2)b Misc(1)c
I
No
Yes
7
2
PvAE(2)d Misc.(5)e
PPvAE(2)f
N&I
No
Yes
13
1
EICA(8)g NvI(2)h PPvAE(1)i Misc(2)j
EICA(1)k
I
No
Yes
0
0
NA
NA
N&I
No
Yes
3
2
PPvAE(1)l Misc(2)m
EICA(2)n
A literature search was conducted on Web of Science to find invasive species studies incorporating common gardens in their approach. We used the
search phrase ‘‘(‘‘invasive’’ or ‘‘invasion’’ or ‘‘exotic’’) AND (‘‘Common Garden’’ OR ‘‘Common gardens’’) AND (‘‘plant’’ or ‘‘plants’’)’’, yielding 77
papers spanning the years from 1994 to early 2009 that explicitly incorporated common gardens in the study of invasion biology. We further pared
the number of papers down to 33 (for a total of 36 independent experiments) that included only experimental studies explicitly utilizing common
gardens to examine causes of phenotypic differentiation between plants from native and invasive ranges (Fig. 1). Garden locations could be in the
native provenance (N) and/or in the invaded provenance (I) of the plants used in the experiment. Provenance of the plants used in the experiment was
either from only the invaded range (I) or from both native and invaded ranges (N & I). Replication within location was considered to be yes (Y) for
studies which included replicate gardens within a specific study location; otherwise it was evaluated as no (N). We also categorize studies with respect
to the major hypotheses being tested and break this into 4 major categories: EICA – evolution of increased competitive ability; PPvAe – phenotypic
plasticity versus adaptive evolution; NvI – trait comparison between plants of the native versus invasive provenance; and Misc – other assorted
hypotheses regarding invasive species.
a
Wolfe et al. (2004); Stastny et al. (2005); Joshi and Vrieling (2005); Zou et al. (2008a, b).
b
Leger and Rice (2003); Leger and Rice (2007).
c
Williams et al. (2008).
d
Poulin et al. (2007) – 2 experiments
e
Kollmann and Banuelos (2004); Weber and Schmid (1998;) Weber and D’Antonio (1999); Ebeling et al. (2008); Monty and Mahy (2009).
f
Byers and Quinn (1998); Geng et al. (2007).
g
Siemann and Rogers (2001); Siemann and Rogers (2003b); van Kleunen and Schmid (2003); Blair and Wolfe (2004); Buschmann et al. 2005
(2005); Meyer et al. (2005); Rogers and Siemann (2005) – 2 experiments;
h
Guesewell et al. (2006); Feng et al. (2007).
i
Caño et al. (2008).
j
Buschmann et al. (2006); Wolfe et al. (2007).
k
Siemann and Rogers (2003a).
l
Maron et al. (2007).
m
Maron et al. (2004a); Williams et al. (2008).
n
Maron et al. (2004b); Genton et al. (2005).
introduced range results from evolutionary processes
causing genetic differentiation (Bossdorf et al., 2005;
Wares et al., 2005; Keller and Taylor, 2008).
Common garden experiments are ideally suited for
disentangling how genetic and environmental factors
contribute to the success of invasive species in their
introduced range. In common garden experiments, a
number of genotypes are raised in a common environment so that the phenotypic variation observed in the
field can be attributed to genetic causes or to a non-
genetic phenotypic response. The common garden
approach has a long tradition in plant evolutionary
ecology (Turesson, 1922; Clausen et al., 1940). In recent
years, common garden experiments are increasingly
being used to address research questions in invasion
biology (see Table 1 and Fig. 1). Two of the most
commonly addressed questions are (1) tests of the
evolution of increased competitive ability hypothesis
(EICA, 44% of the 36 experiments listed in Table 1; see
Blossey and Nötzold (1995) for a definition of the EICA
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K.A. Moloney et al. / Perspectives in Plant Ecology, Evolution and Systematics 11 (2009) 311–320
7
Papers Published
6
5
4
3
2
1
0
1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008
Year Published
Fig. 1. Number of papers published that contained a study
focusing on invasive, exotic species with a common garden
experiment (see Table 1 for details).
hypothesis) and (2) an exploration of the relative
importance of phenotypic plasticity versus adaptive
evolution (PPvAE, 22%) in producing successful invaders. These two areas of research reflect current ideas
regarding the most likely processes driving exotic species
to become invasive. A long treatise could be written on
the relative merits of the various hypotheses and
research questions in invasion biology being explored
using common gardens, but the intent of this paper is to
focus on something that has not yet received serious
attention: what, if any, is the ideal design for a common
garden study that targets the ecological and evolutionary processes causing phenotypic differentiation between native and invasive ranges, and has this design
ever been applied?
The answers to these questions will obviously depend
to some extent on the exact hypothesis being addressed,
but it is clear from reviewing the literature that more
critical thought needs to be given in developing
appropriate designs (Table 1). Common garden studies
with invasive species can be categorized according to
their genetic and geographic design, using three basic
criteria. The first criterion concerns the genetic composition of the experiment and distinguishes between two
basic categories: (1) all plants included in the experiment
originate from the invasive provenance (I – 25% of
the experiments included in Table 1) or (2) they
originate from both the native and invasive provenances
(N & I – 75% of the experiments in Table 1).
The second criterion refers to the geographic location
of the experiment and distinguishes among three
categories: (1) gardens located only within the native
provenance, i.e., at sites from which the invasive species
originates (N – 22% of the studies in Table 1); (2)
gardens located solely within the invasive provenance
(I – 64%); and (3) parallel studies conducted in both
native and invasive provenances (N & I – 14%). The
313
latter category surprisingly comprises only five out of 36
experiments included in a literature search reported here
in Table 1. The geographical location of the experiment
is important because it is associated with uncontrolled
environmental factors (e.g. climate, soil type, nutrient
availability, interacting species, etc.) that may influence
the outcome of the experiment and the interpretation of
its results.
The third criterion distinguishes between studies
that replicate gardens within provenance (Y) versus
those that do not (N). This is primarily a statistical
issue that can strongly influence the inference space
available to the interpretation of the outcome of
common garden experiments. Generally, the experiments in Table 1 that used replicate gardens placed all
gardens in only one geographic region. Two exceptions
were the studies of Maron et al. (2004b) and Genton et
al. (2005), which included replicated gardens within each
of the N & I provenances to incorporate a geographic
component into the inference space. Maron et al.
(2004b) were interested in examining latitudinal trends
in the evolution of invasive species between replicates
within continent, whereas in Genton et al. (2005)
replication was included as a blocking factor in the
statistical analysis that compared responses between
provenances.
The categorization scheme described above results in
12 possible experimental designs. In our literature
review (Table 1), we found that 8 of these designs had
actually been implemented. Interestingly, the two most
common research questions (EICA and PPvAE) were
addressed with multiple designs. The EICA hypothesis
alone was distributed among four designs, which implies
that not enough attention has been paid to the
relationship between the research question and the
experimental design most appropriate for addressing
it. Granted, the individual studies differed subtly in the
specific aspects of the EICA hypothesis being tested and
in some cases different designs might make sense.
However, in general a systematic approach to develop
an appropriate experimental design seems to be lacking.
We argue that this is one reason for the slow
development of a more general theory of invasive
species, a situation that has been viewed as problematic
by many invasion biologists (e.g., Cadotte et al., 2006).
One indication that we need to give critical thought to
the geographic design of common garden studies is
provided by Maron et al. (2004b). Their study was one
of the two encountered in our literature review that
conducted parallel common garden experiments in both
native and invasive provenances. They constructed four
common gardens, two in Europe (N) and two in North
America (I). One of the key findings of their study was
that the results obtained in the different gardens were
inconsistent due to an interaction effect between garden
location and genetic provenance of the plants (a form
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of environment genotype, i.e., G E, interaction), a
phenomenon that we will refer to in the following as the
‘‘Maron effect’’. The Maron effect can be defined as an
interaction between provenance (source of seed) and
garden location (a proxy for local environmental factors
outside of the control of the experiment). Because of this
effect, Maron et al. state that the overall conclusions
drawn from their experiment would have been qualitatively different depending upon which subset of the four
gardens was considered. Unfortunately, the designs they
utilized in the different gardens were not standardized so
that it is impossible to explicitly test for a ‘‘Maron
effect’’ influencing the outcomes of the experiment.
The only other study we found with replicate gardens
located in both the native and invasive provenances had
a standardized design imposed on all the gardens, but
did not test for interactions between garden and the
other experimental variables, provenance in particular
(Genton et al., 2005). Genton et al. treated gardens
within continent as a random effect and explored the
effect of ‘‘continent’’ as a fixed effect. The random effect
of garden was not significant in their study, but
continent exhibited a strongly significant interaction
with the seed source (i.e., provenance) treatment (called
‘‘origin’’ in the original paper). The continent by
provenance interaction could be due to a number of
factors, but Genton et al. (2005) point out that plants
from one collection site were the smallest when planted
in the invasive continent and the largest when grown in
the native continent. They do not discuss other aspects
of the study resulting from the highly significant
continent provenance interactions.
The findings of Genton et al. (2005), along with those
presented in Maron et al. (2004b), indicate that we need
to consider how important a ‘‘Maron effect’’ might be
for common garden experiments with invasive species. If
results strongly depend upon the location of common
gardens, how do we make sense of experiments that
have already been conducted and how should we design
future common garden experiments? To address these
concerns, we propose an experimental design that
explicitly accounts for potential interactions between a
‘‘garden effect’’ and experimentally manipulated variables, thereby allowing an explicit test for the ‘‘Maron
effect’’.
A minimal design for common garden
experiments with invasive species
In our view, there are two critical elements in the
design of a common garden experiment that examines
the genetic and environmental factors potentially causing differences between the performance of a species in
its native and introduced range: (1) the location of
gardens, which should include both the native and
invasive provenance and should be replicated within
each, and (2) the choice of genetic source material,
which should include appropriate genotypes from both
the native and invasive provenance. Many common
garden designs take the genetic source material
into account, but most often garden location is not
appropriately integrated into the experimental design.
Fig. 2. Trait response of plants of different provenance planted in different garden locations. (A) No interaction between garden
and plant provenance in determining trait expression. (B) ‘‘Maron effect’’, i.e., a significant interaction between garden and plant
provenance in determining trait expression. Lower case letters associated with lines indicate provenance of experimental plants that
correspond to garden locations indicated by the same upper case letter. The relationships illustrated in panel B represent a situation
where adaptive evolution leads to an optimal response by plants to the conditions in their home garden, although they may still be
outperformed by a plant originating from a different location.
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Generally, the choice of garden location(s) is based on
logistical considerations alone, due to the substantial
effort required to successfully conduct common garden
experiments. However, serious issues of interpretation
may arise if the ‘‘Maron effect’’ is widespread and
unappreciated. How important might the ‘‘Maron
effect’’ be for common garden experiments exploring
the evolution of invasiveness? We believe that the
answer is ‘‘Quite important!’’, and explore this in a
hypothetical example illustrating the potential problems
arising from only including one common garden in a
study.
Imagine four genotypes sampled from four different
provenances (locations). In the absence of a Maron
effect, the rank order trait response of all genotypes
would remain the same across gardens, independent of
where they are sited (Fig. 2A). Interpretation of the
results would be independent of garden location.
However, if the Maron effect is important, then the
trait response would depend upon the location of the
garden. For example, if each genotype has its highest
fitness in its home site (fulfilling the ‘‘home-away’’
criterion of Kawecki and Ebert, 2004), then we might
find a scenario similar to the one depicted in Fig. 2B,
which is consistent with the findings of Maron et al.
(2004b) and Genton et al. (2005) that the observed
response depends critically upon the location of the
garden, as described above.
The existence of a Maron effect may, in fact, help
explain the diverse findings reported in studies of the
EICA hypothesis (cf., Colautti et al., 2004; Joshi and
Vrieling, 2005; Williams et al., 2008). A primary
prediction of the EICA is that plants from the invasive
provenance have evolved to become better competitors
than plants from the native provenance, due to escape
from local herbivores, parasites and disease organisms.
However, experimental tests of this hypothesis have
shown a broad range of results, ranging from complete
agreement (Garden D in Fig. 2B; e.g., Blossey and
Nötzold, 1995; Siemann and Rogers, 2001; Wolfe et al.,
2004), to equivocal results (Gardens B and C in Fig. 2B;
e.g., Willis et al., 2000; van Kleunen and Schmid, 2003)
and findings contradicting the hypothesis (Garden A in
Fig. 2B; e.g., Bossdorf et al., 2004). The conflicting
outcomes could in fact be due to an underlying ‘‘Maron
effect’’ with the observed outcome depending upon the
site of the experiment (since most experiments are only
conducted at one location), as much as upon the
underlying relationships between plants of native and
invasive provenance. In summary, Maron effects may be
important for both fundamental and applied invasion
biology: the simple native-versus-invasive hypotheses
would fail to explain evolutionary processes, if native
genotypes outperform exotic genotypes in parts of the
invasive range (as in Garden C in Fig. 2b). This can also
be of applied importance: the invasion would be
315
worsened if native genotype b was introduced to site C
in the invasive range (Fig. 2b).
To address the issues discussed above, we propose a
minimum optimal design (MOD) for common garden
experiments examining genetic and environmental differences between the native and invasive range (note
that similar principles also apply to experiments
examining differentiation within the native or invasive
range, e.g. Kollmann and Banuelos, 2004). The MOD
enables one to test for the ‘‘Maron effect’’ and contains
four elements:
(1) Garden locations: There should be at least four
gardens, two in each provenance (N & I). This
provides replication within provenance. In experiments testing adaptive evolutionary hypotheses,
available phylogeographic knowledge should be
used to identify garden regions that provide proper
genetic replication (Keller and Taylor, 2008).
Ideally, the gardens should cover a broad spectrum
of the environmental variation present in both
the native and the invasive range. Other elements
of garden location might also be of interest to
explore, e.g., in the invasive range sites could be
chosen to correspond with different stages of
invasion history. The latter could be matched by
choosing sites from the native provenance that
incorporate other important aspects associated with
locations in the invaded range, such as latitude or
general climatic conditions. Including more factors
associated with garden location will obviously
increase the number of gardens needed in the study
to allow for replication of the additional design
elements.
(2) Genetic composition: Genetic material should be
obtained using the same, balanced, sampling design
in each region. The genetic material should ideally be
composed of a representative, random sample of the
genotypes within each region. Additionally, genetic
composition of plants from each region should be
tightly controlled to ensure balanced representation
of the genetic makeup from all regions included in
the experiment: for example, seeds collected from
individual plants representing maternal half-sibs in
open pollinated species; or haphazard collection of
seeds from a large number of plants that are
combined to contain a random sample representative of the region at large. The choice of how to
collect and use seed at the level of the region will
determine the inference space of the experiment. The
genetic material from each region should be equally
represented in each garden. To remove maternal
environmental effects, material from different origins should ideally be cultivated over multiple
generations in a common environment. Less ideally,
maternal environmental effects can be accounted for
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by including proxies for the quality of the maternal
environment (such as initial seedling size) as
covariates in analyses of experimental results.
(3) Standardization: The experimental protocols should
be standardized across gardens (to ensure, for
instance, that response variables are measured in
the same way). Standardization is important because
differences among gardens may ultimately result
from two factors: (1) environmental differences
between sites and (2) experimental error due to
uncontrolled differences in protocol and design.
The more the latter can be eliminated, the more
will be learned about environmental variation
between gardens. Depending on the exact hypothesis
addressed, it may also be important to control
certain environmental factors of the experiment
(e.g. soils, nutrients, water regimes, interacting
species, etc.). Controlling certain aspects of the
environment while letting others vary helps to
identify those environmental factors that cause
between-garden variation (e.g., if soils are kept
constant, observed differences should be due to
climate and/or biotic interactions). While standardization is perhaps the most difficult requirement to
meet, it is indispensable for understanding the causes
of a potential ‘‘Maron effect’’.
(4) Biosafety: Our proposed design could potentially
cause serious biosafety problems because it requires
the introduction of foreign germplasm into the
garden sites. This may produce even more aggressive
plants in the invaded provenance and could lead to
back invasion in the native range by aggressive
plants that evolved in the invaded range (cf., Genton
et al., 2005). These concerns may limit the number of
species that can be used in the type of experiment we
are proposing. Great care needs to be taken to
minimize the potential for gene escape in both the
native and invasive provenance.
A brief example
Based on the principles outlined above, we conducted
an experiment with Lythrum salicaria L., an aggressive
wetland invader in North America that originated from
Eurasia. The experiment was designed to test whether
native and invasive genotypes of L. salicaria differ in
their response to nutrient availability and water regime
(note, however, that the exact hypothesis is not relevant
for our argument). It builds upon an experiment that
was conducted in a single common garden in Ames,
Iowa, USA and is reported in Chun et al. (2007). The
experiment involved two environmental treatments
(water regime and nutrient level) in a factorial design
(see detailed explanation in Chun et al., 2007). We
followed the same general protocol as in that experiment, but adapted it to meet the four criteria for the
minimal design outlined above:
(1) Garden locations: There were four common gardens
in our experiment, two in the invaded provenance –
Iowa (IA) and New Jersey (NJ), USA – and two in
the native provenance – Potsdam (PD) in NE
Germany and Tübingen (TÜ) in SW Germany –
providing replication within provenance. The gardens within provenance were sited in locations
representing substantially different environmental
conditions encountered within the distributional
range of L. salicaria.
(2) Genetic composition: Genetic material was obtained
from three populations within the region surrounding each of the four common gardens. Seeds were
collected from several maternal parents in each
population. From these seed collections, five half-sib
families from each population were eventually
utilized in the experiment (Fig. 3). Four half-sibs
from each parent were planted in each garden,
appearing once in each environmental treatment. To
Fig. 3. Design of an experiment employing the MOD proposed in this paper for a common garden study examining ecoevolutionary relationships in an invasive species. The common garden sites are indicated by the Region level in the hierarchy
depicted in the figure. Genetic sampling was conducted at the level of maternal half-sibs nested within the hierarchy of the
experimental design, which includes replicate populations nested within each garden region. See text for further explanation.
Regions are Iowa (IA) and New Jersey (NJ) in the United States and Potsdam (PD) and Tübingen (TU) in Germany. Three
populations, indicated by two letter acronyms, were sampled within each region.
Overview of the impact of the ‘‘garden effect’’ on the outcome of a study utilizing the MOD proposed in this paper.
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Analyses were conducted using mixed-effects models in R (function lmer, Pinheiro and Bates 2004). After fitting the maximal model, the model was simplified using stepwise backward removal of
insignificant terms (P40.05). The table indicates the fixed effect and covariate terms that remained in the resulting minimal adequate model by a solid fill in the corresponding table cell. Significant
interactions that involve garden and provenance, thereby indicating a ‘‘Moran effect’’, are highlighted in black. Fixed effects in the model were Water (two levels), Nutrients (two levels), Provenance
(Prov in the table; two levels, corresponding to origin of seed with respect to continent associated with N or I provenances) and Garden (four levels associated with the common four gardens in the
experiment). Populations nested within garden region, half-sib families nested within populations, blocks and wading pools within blocks were included as crossed random effects (not shown in the
table). Further details regarding the design of the experiment and the protocols used can be obtained from the text, Chun et al. (2007) or by contacting the corresponding author.
K.A. Moloney et al. / Perspectives in Plant Ecology, Evolution and Systematics 11 (2009) 311–320
Table 2.
317
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account for maternal environmental effects we
included height at transplant as a covariate in
statistical analyses.
(3) Standardization: The protocols used in all gardens
were coordinated to limit variability among gardens.
For example, watering was done on exactly the same
schedule in all four gardens, after plants were
established. We used the same fertilizer formulation
from the same manufacturer in all gardens. Soil
composition was matched as closely as possible
among gardens, using commercially obtained topsoil
with similar starting nutrient charges. Measurements
of response variables were taken using the same
schedule and the same protocols. One team member
coordinated all efforts to ensure as much consistency
as possible. Still, it must be said that one lesson
learned from this experiment is that standardization
is the aspect of the MOD that is by far the hardest to
achieve.
(4) Biosafety: Gardens were located at least 3 km from
any known naturally occurring L. salicaria plants to
prohibit gene flow out of the experimental garden.
Garden sites will be monitored for the foreseeable
future to insure that plants do not successfully
escape and establish.
We have conducted a general analysis of the response
variables in our experiment to determine how pervasive
the garden effect might be in influencing the outcome of
the experiment. Of particular importance are significant
interactions between garden and provenance as these
indicate the presence of a ‘‘Maron effect’’. Table 2 shows
an overview of the analysis and highlights the importance of the ‘‘Maron effect’’ in our experiment:
significant interactions involving garden and provenance
were found for 8 of 13 response variables analyzed.
Moreover, all except one response variable were
significantly impacted by at least one interaction
between garden and an experimentally manipulated
variable. Only the ratio of leaf width to length showed
no ‘‘garden effect’’, but also was not affected by any
other explanatory variable, presumably because it is a
genetically fixed trait.
The implications of our finding are that we could
grossly misinterpret the differences between plants from
different provenances if we only conducted the experiment in one garden. This emphasizes the need for
conducting common garden experiments that apply or
expand upon the MOD proposed above.
the location of common gardens then there is a strong
case for applying, at the least, our MOD protocol in
common garden experiments with invasive species. In
the absence of utilizing multiple gardens situated in the
native and invasive provenance, the interpretation of the
results of a common garden study should not be
extrapolated beyond the context of the individual site
at which the garden was situated. This may also explain
why it has been very difficult to find universal trends in
the processes leading to successful invasion, since most
common garden studies do not replicate gardens within
or across provenances. The outcome of the experiment
may depend on the particular site at which it is
conducted, but without gardens sited at multiple
locations the implications of the ‘‘Maron effect’’ will
go unappreciated and undetected.
Adopting the proposed MOD protocol as a minimum
in conducting common garden studies is the first step in
advancing our understanding of the processes leading to
successful invasions. Perhaps the most challenging task
is to identify those components of the environment that
are involved in genotype-by-environment interactions
and thereby cause the Maron effect. To this end, the
MOD can be extended by experimentally manipulating
the environmental factor hypothesized to be important
to the levels observed in each of the provenance regions
(see Nuismer and Gandon (2008) for an experimental
design suited to do this in the case of tight coevolution
with an interacting species). Understanding the environmental factors involved in the ‘‘Maron effect’’ is crucial
for extrapolation beyond common garden locations and
for developing a more general understanding of the
evolutionary ecology of biological invasions.
Acknowledgements
We would like to thank Jack Chapman, Young Jin
Chun, Lina Weiß, and Petra Finkenbein for help in
implementing the MOD. KAM gratefully acknowledges
support by the Velux Foundation and Iowa State
University for his sabbatical at the ETH in Zürich,
during which time these ideas came to fruition. No
support was provided by the United States National
Science Foundation or United States Department of
Agriculture.
References
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If our experiment and the experiments of Maron et al.
(2004b) and Genton et al. (2005) are indicative of a
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