Basic and Applied Ecology 17 (2016) 377–387
Is biotic resistance to invaders dependent upon local
environmental conditions or primary productivity?
A meta-analysis
Gisela C. Stotz∗ , Gregory J. Pec, James F. Cahill
Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada T6G 2E9
Received 16 June 2015; accepted 2 April 2016
Available online 7 April 2016
Abstract
Biotic resistance is an important component to limiting the spread of invasive plants into native communities. However, under
certain conditions native plants may also facilitate invasion, a process identified as biotic assistance. Identifying the conditions
that associate with resistance and assistance is needed to better understand the factors driving species invasion.
Substantial theory and empirical work suggests net effects of neighbors may be dependent upon habitat productivity and
environmental conditions. How that applies to the interaction among the resident community and the invaders is largely untested.
Here we compiled data from 23 articles, which had experimentally determined the strength of biotic resistance and/or assistance.
We then combined these data with remote-sensing estimates of productivity, precipitation and temperature at each study site.
Using standard meta-analytical techniques we determined the overall effect resident communities had on the emergence, growth,
reproduction and survival of non-native invaders. Further, we tested whether the interaction between resident communities and
invasive species was influenced by primary productivity, temperature and precipitation.
Across all sites, we found broad support for biotic resistance, while evidence for biotic assistance was rare. However, we
found the relative magnitude of biotic resistance on invaders increased with temperature or precipitation; a pattern consistent
with the stress gradient hypothesis. In contrast we found no evidence that the strength of biotic resistance varied as a function of
primary productivity. Further evaluation of the relationship between productivity and environmental conditions on the direction
and strength of the effect of resident species on invaders may help predict invasion establishment and success. Understanding
or predicting the susceptibility of communities to invasion may help prioritize management efforts.
Zusammenfassung
Biotische Resistenz ist eine wichtige Komponente für die Begrenzung des Eindringens von invasiven Pflanzen in einheimische
Gemeinschaften. Indessen können einheimische Pflanzen unter bestimmten Bedingungen die Invasion begünstigen, ein Prozess,
der hier als “biotische Assistenz” (‘biotic assistance’) bezeichnet wird. Die Bedingungen herauszufinden, die mit Resistenz und
Assistenz verbunden sind, ist notwendig, um die Faktoren, die die Invasion von Arten steuern, besser zu verstehen. Umfangreiche
theoretische und empirische Forschungen legen nahe, dass der Nettoeffekt von Nachbarn von der Produktivität des Lebensraums
und den Umweltbedingungen abhängen könnte. Wie dies auf die Interaktion zwischen der vorhandenen Gemeinschaft und den
Neuankömmlingen zutrifft, blieb weitgehend ungeprüft. Wir stellten Daten aus 23 Artikeln zusammen, die die Stärke von
∗ Corresponding
author. Tel.: +1 780 492 4587.
E-mail address: [email protected] (G.C. Stotz).
http://dx.doi.org/10.1016/j.baae.2016.04.001
1439-1791/© 2016 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.
378
G.C. Stotz et al. / Basic and Applied Ecology 17 (2016) 377–387
biotischer Resistenz und/oder Assistenz experimentell bestimmt hatten. Für jeden Untersuchungsstandort kombinierten wir
diese Daten mit Schätzungen der Produktivität, Niederschlagsmenge und Temperatur aus der Fernerkundung. Mit normalen
Techniken der Metaanalyse bestimmten wir den Gesamteinfluss, den die vorhandenen Gemeinschaften auf Keimungserfolg,
Wachstum, Reproduktion und Überleben der invasiven Arten ausübten. Wir testeten ebenfalls, ob die Interaktionen zwischen
vorhandenen Gemeinschaften und invasiven Arten von Primärproduktion, Temperatur oder Niederschlag beeinflusst wurden.
Über alle Standorte hinweg fanden wir breite Unterstützung für biotische Resistenz, während Belege für biotische Assistenz
selten waren. Allerdings fanden wir, dass die relative Größe der biotischen Resistenz gegen Invasoren mit der Temperatur oder
der Niederschlagsmenge zunahm, ein Muster, welches mit der Stressgradienten-Hypothese übereinstimmt. Dagegen fanden wir
keine Belege dafür, dass die Stärke der biotischen Resistenz als Funktion der Primärproduktion variierte. Weitere Untersuchungen zur Beziehung zwischen Produktivität und Umweltbedingungen und der Richtung und Stärke des Einflusses der vorhandenen
Artengemeinschaft auf die Invasoren könnten dazu beitragen, Besiedlung und Erfolg von Invasoren vorherzusagen. Die Anfälligkeit von Gemeinschaften gegen Invasionen zu verstehen oder vorherzusagen, könnte helfen, Managementbemühungen zu
priorisieren.
© 2016 Gesellschaft für Ökologie. Published by Elsevier GmbH. All rights reserved.
Keywords: Abiotic conditions; Biotic assistance; Context-dependence; Competition; Facilitation; Stress gradient hypothesis
Introduction
Biotic resistance is the ability of a resident community
to limit recruitment and growth of invasive species (Levine,
Adler, & Yelenik 2004). As such, when looking at biotic
resistance we tend to assume that the resident community
will have a negative effect on invasive species (i.e. competition) (Levine et al. 2004). However, resident communities
may also facilitate invasive species establishment, growth
and spread (Badano, Villarroel, Bustamante, Marquet, &
Cavieres 2007). The processes where native species facilitate
exotic species have been termed biotic assistance (Inderjit
& Cahill 2015). Biotic resistance or assistance may result
from both direct as well as indirect interactions (Bever 2003;
Levine et al. 2004; Inderjit & Cahill 2015). Consequently,
the outcome of the interaction between native communities and invasive species may range from biotic resistance
to assistance (Fig. 1).
The effectiveness of native communities at limiting invasion varies (Lonsdale 1999), and this variation has been
partly explained through changes in species richness and
phylogenetic diversity within the native community (Dukes
2001; Kennedy et al. 2002; Strauss, Webb, & Salamin 2006;
Gerhold et al. 2011). Absent, however, is a broad analysis
across species and systems, investigating how habitat productivity and environmental conditions influence the ability
of the resident communities to resist, or potentially facilitate
invasion (Fig. 1). This is particularly surprising as substantial
theory suggests that the intensity and outcomes of plant–plant
interactions are dependent upon primary productivity and
environmental stress (Grime 1973; Bertness & Callaway
1994). The same may be true for invasive species’ effect
on the resident community with the strength and direction
of this effect varying depending on the habitat’s productivity
and/or environmental conditions (Fig. 1) (e.g. MacDougall,
Boucher, Turkington, & Bradfield 2006).
Plant ecologists have long focused on the relationship
between competition and productivity. It has been proposed
that competition becomes stronger and influences community
assembly as productivity increases, while stressful conditions
are more important for assembly at low productivity (Grime
1973). A slightly different model, the stress gradient hypothesis (Bertness & Callaway 1994) proposes that competition
is predominant in environments of intermediate productivity, while facilitation occurs more frequently in both highly
stressful and highly productive environments. In contrast,
an alternative theory proposes that competition is important across a productivity gradient, with different resources
being limiting at both ends of this gradient (Tilman 1988).
Further, two meta-analyses suggest a general decline in competition with increased productivity and decreased stress
(Goldberg, Rajaniemi, Gurevitch, & Stewart-Oaten 1999;
Maestre, Valladares, & Reynolds 2005). However, these theories have rarely been tested in the context of invasion and
biotic resistance (von Holle 2005, 2013; Chambers, Roundy,
Blank, Meyer, & Whittaker 2007; Lortie & Cushman 2007;
Harrison, Cornell, & Grace 2015; Reisner, Doescher, & Pyke
2015).
Evidence suggests that environmental conditions and productivity may be important in determining invasion success.
For example, invasive species are commonly found invading
productive environments with greater resource availability
(Stohlgren et al. 1999; Foster, Smith, Dickson, & Hildebrand
2002), however, this is not always the case, as invasive
species can also be found invading stressful habitats (Badano
et al. 2007; Lortie & Cushman 2007). Although invasive
species performance tends to increase under benign, fertile conditions (Dukes & Mooney 1999; Chambers et al.
2007; Gerhardt & Collinge 2007; Goldstein & Suding 2014;
Harrison et al. 2015), this advantage can be offset or
decreased by the presence of a more resistant community
in those areas (Chambers et al. 2007; Eskelinen & Harrison
G.C. Stotz et al. / Basic and Applied Ecology 17 (2016) 377–387
379
Fig. 1. The effect of neighbors on exotic species (net neighbor effect), as well as the impact of exotic species on the resident communities, may
be dependent upon habitats productivity and abiotic conditions. The net neighbor effect on invaders may range from negative (competition)
to positive (facilitation). The negative effect of neighbors on exotic species is a process generally known as biotic resistance. However, the
net neighbor effect can also be positive (where the resident communities facilitate invasive species), a process identified as biotic assistance.
Evidence and hypotheses vary in their predictions on how the strength and direction of the interaction vary along stress (left graph) or
productivity (right graph) gradients.
2014; Harrison et al. 2015). Thus, biotic resistance may be
greater in benign and productive areas, while under stressful conditions, the resident community has been shown to
facilitate, rather that resist invasion (von Holle 2005; Badano
et al. 2007; Lortie & Cushman 2007; Reisner et al. 2015).
Further, the susceptibility of communities along productivity
or environmental gradients may depend upon the invader’s
functional group (Gómez-Aparicio 2009), with some functional groups (e.g. trees and shrubs) being more dependent
upon facilitation for establishment (Gómez-Aparicio 2009;
Mendoza, Gómez-Aparicio, Zamora, & Matías 2009). By
evaluating the effect of productivity and environmental stress
on the strength and direction of the interaction between native
communities and invasive species, we may be able to predict under which conditions communities are more or less
susceptible to different invaders.
Here, we focus on testing the effect of resident communities on invaders along different environmental gradients. To
evaluate this, we performed a meta-analysis, which allows
us to include results from multiple systems across a broad
geographical range. Further, we integrated these results with
environmental data obtained from remote sensing databases
to evaluate the effect of productivity and environmental stress
on net neighbor effect on invasive species among sites. We
specifically evaluated (1) the effect of native communities
on invasive species performance; (2) the frequency of facilitation and competition as outcomes of those interactions
(3) whether the strength and direction of the interaction is
dependent upon the habitat’s productivity and/or environmental conditions and (4) whether the dependence upon
productivity and/or environmental conditions varied depending on an invaders’ functional group.
Materials and methods
Literature criteria and dataset construction
An ISI Web of Science search was conducted to retrieve
relevant publications to include in the meta-analysis. We
used – invasi* OR exotic* OR alien* OR introd* – as key
words, given the number of terms used to define similar concepts (Richardson et al. 2000). We then refined the results
to all articles included within the research areas of Ecology, Plant Sciences and Forestry, and to articles published
between 1995 and 2015, as environmental data are not available for previous years (Appendix A). This search resulted
in 506,678 studies screened. To minimize the likelihood
of relevant studies missed in our initial search, we further
cross-referenced each of the articles for pertinent articles to
potentially include. All resultant publications were screened
to meet the following criteria: (1) studies needed to compare
the performance of an invasive species in an area with and
without the resident community present, (2) studies needed to
be under field conditions, (3) the resident community needed
to be native to its area and (4) means, standard error and
sample sizes for treatments and the control needed to be
available. If in graphical form, graphs were digitized and
data points were extracted using the software Engauge Digitizer v.2.12 (http://digitizer.sourceforge.net). Including only
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experimental tests of biotic resistance (resident community
intact vs. removed) limited the number of studies in our
dataset, but allowed us to directly calculate the strength of
interaction among resident communities and invasive species.
We treated publications where investigators subjected different invasive species or the same invader to different
communities as separate studies (Gurevitch & Hedges 1993).
If a study included various levels of vegetation or neighbor
removal, we used data from the most severe treatment.
Response and explanatory variables
From each study, data were collected on invasive species
performance with the resident community intact vs. removed.
We classified the response variables into 4 categories: emergence, plant size, reproduction and survival. Evaluating
different response variables may be important, as some
interactions may comprise both competition and facilitation
depending on the life stage or the response variable measured
in the target species (Callaway & Walker 1997). Further, to
look at the direct effect of environmental conditions and productivity on performance, we used data on percent survival
and emergence in the absence of competition. Survival and
emergence were calculated based on total seeds added or
number of initially planted seedlings when metrics were not
reported as a percentage. We also extracted information on
the exact location of the experiments to obtain data for the
following explanatory environmental variables: net primary
productivity (NPP), normalized difference vegetation index
(NDVI), precipitation and temperature. NPP, NDVI, precipitation and temperature were obtained from the Advances
Very High Resolution Radiometer (AVHRR) and the Moderate Resolution Imaging Spectroradiometer (MODIS) remote
sensing databases (see Appendix A).
Data analysis
We calculated Hedge’s effect size d (Gurevitch & Hedges
1993), which is the standardized mean difference between
the control group (neighbor intact) (X̄C ) and the experiment
group (neighbor removal) (X̄E ) for plant size, emergence,
reproduction and survival, separately using the following
equation:
d=
X̄E − X̄C
J
SDpooled
A positive effect size d indicates a negative effect of neighbors on invasive species performance (competition) while a
negative effect size d indicates a positive effect of neighbors
on invasive species performance (facilitation). J was calculated to correct for small sample bias (Borenstein, Hedges,
Higgins, & Rothstein 2009) using the following equation:
J =1−
3
4(nC + nE − 2) − 1
We conducted a random-effects meta-analysis, which is
a meta-analysis model (different from a random effect linear model) that allows for variation between study effects in
contrast to a fixed-effect model that assumes variance among
study effects is known. Between study heterogeneity was
assessed by calculating and testing for the significance of Q
(see Appendix B for more details). Analyses were done using
weighted linear models, where the models were weighted by
the study’s precision (W*) using the function rma, from the
metafor package (Viechtbauer 2010) in R (v.2.15.3, R Core
Team, 2013). W* was calculated for each study as the inverse
of the variance,
Wi∗ =
1
Vyi∗
where Vyi∗ is the within-study variance plus the betweenstudies variance. Methods for meta-analysis followed those
presented in Borenstein et al. (2009). Publication bias, before
the inclusion of moderator variables, was assessed through
a funnel plot and the trim and fill method (Appendix B for
more details).
Linear models were performed to test for the direct effects
of environmental conditions on invasive species performance
using percent emergence and survival in the absence of neighbors as response variables. Linear mixed effect models were
used when testing for the effect of NPP and NDVI, where
data source (MODIS or AVHRR) was added as a random
effect to control for differences between the two sensors (see
Appendix A). Effects of environmental variables and productivity on the neighbor effects on invasive species performance
were tested for using meta-regressions. A meta-regression is
a meta-analysis that includes, in this case, a continuous variable to describe variation among study effects (moderator)
(Borenstein et al. 2009). Each explanatory variable or moderator was tested for individually, in separate models, due to
small sample size. In models including NPP and NDVI, data
source (MODIS or AVHRR) was added as a random effect;
however no random effect was added when evaluating the
effect of temperature or precipitation. All meta-regressions
were run using the lm function (for linear model) in the stats
package and lme function (for linear mixed models) in the
nlme package in R, with effect size d as the response variable
and weighted by W* (Koricheva, Gurevitch, & Mengersen
2013). To test for the robustness of our results (Koricheva &
Gurevitch 2014) and because of the significant heterogeneity
between studies (see Appendix B) we ran separate models for
different invasive functional groups (i.e. forb, shrub, grass and
tree, Appendix C) when the number of replicates per functional group allowed for it (minimum of 6 replicates). Among
all sites included in this study, there was no correlation
between precipitation and temperature (r2 = −0.07, P = 0.69).
Neither temperature nor precipitation correlated with NPP
(r2 = −0.12, P = 0.544; r2 = −0.1, P = 0.615, respectively) or
NDVI (r2 = −0.06, P = 0.74; r2 = −0.03, P = 0.873, respectively). NPP and NDVI were strongly correlated (r2 = 0.87,
G.C. Stotz et al. / Basic and Applied Ecology 17 (2016) 377–387
P < 0.01) and therefore, we only report results for NPP from
now on, as results are very similar.
Results
We found a total of 23 publications that met our criteria (see
Appendix C), of which most included more than one invasive
species or multiple study sites (treated as different studies).
In total, emergence of invasive species was evaluated in 21
studies, plant size in 27, reproduction in 11 and survival in
21. Further, 26 studies included a measure of invasive species
survival and 21 studies of emergence reported (or could be
calculated) as a percentage. Sites included in our analyses
381
range in temperature and precipitation covering drier areas
with high and low temperatures, as well as wetter ones with
low temperatures (Fig. 2). Wetter sites with low temperatures
are under-represented in most of our analyses, except when
looking at the impact of the resident community on invader’s
size (Fig. 2B). Thus, our results are applicable to systems
with those climatic conditions.
Native community’s impact on invasive species
performance
On average, native communities reduced invasive species
emergence, size, reproduction and survival, indicating biotic
resistance was common (Fig. 3).
Fig. 2. Relationship between precipitation and temperature for all sites included in our analyses. Temperature and precipitation were averaged
for the growing season or duration of the experiment. Since different studies varied in the invaders response variable measured, the sites and
therefore, the range of conditions in the analysis of each of the response variables are shown separately: (A) total (B) emergence, (C) size,
(D) reproduction and (E) survival.
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Fig. 3. Net effect of the resident native community on invader seedling emergence, size, reproduction and survival. Mean ± 95% confidence
intervals. Positive values indicate competition and negative values indicate facilitation. Larger values indicate stronger effects.
Biotic assistance was rare with only one case of net facilitative effects found when looking at the effect on size and one
when looking at survival (see Appendix D: Fig. 1). The lack of
evidence for biotic assistance is not an artifact of publication
bias since the assessment of publication bias through funnel plots revealed that the overall effect size did not change
after controlling for it. The trim and fill method revealed
three studies missing from the right hand side of the funnel (i.e. those reporting biotic resistance) when evaluating
survival (see Appendix B: Fig. 1). We also found significant heterogeneity between studies for three of the four
response variables analyzed (size, reproduction and survival)
(Appendix B). Significant heterogeneity was expected and
further justifies the need to explore other moderator variables
to explain the variance between studies.
The effect of productivity, precipitation and
temperature on invasive species performance
We found no direct effect of habitat productivity or
environmental conditions on invasive species survival and
germination in the absence of the resident community
(Table 1).
The effects of productivity, precipitation and
temperature on native community effects on
invasive species performance
In general, productivity was not related to the effect
of native communities on invasive species performance
(Fig. 4A–D, Appendix E), while temperature and precipitation were significant predictors of the interaction outcome
Table 1. Direct effect of productivity, temperature and precipitation
on emergence and survival of invasive plant species in the absence
of the native resident community.
Emergence
(n = 21)
Survival
(n = 26)
NPP
Estimate
F-value
p-Value
−0.006
0.833
0.374
0.033
0.833
0.374
Temperature
Estimate
F-value
p-Value
−0.003
3.487
0.08
−1.911
2.128
0.158
Precipitation
Estimate
F-value
p-Value
−0.074
0.026
0.872
0.118
3.099
0.091
and strength (Fig. 4F and I,Appendix E). Temperature was
positively associated with the neighbor effect on invasive
species size, indicating more biotic resistance in warmer locations. However temperature did not affect biotic resistance for
emergence, reproduction or survival (Fig. 4E–H,Appendix
E). Precipitation was positively associated with the neighbor effect on invasive species emergence and size, indicating
more biotic resistance in wetter locations, but had no effect
on the invader reproduction or survival (Fig. 4I–L, Appendix
E). Although the addition of moderator variables reduced
the heterogeneity between the studies looking at the effect
of neighbors on invasive species’ size, the remaining heterogeneity was still significant (Appendix B). This indicates that
although moderators were significant, much of the variation
remains unexplained, which may be due to the scale at which
moderator variables were measured (Appendix A).
G.C. Stotz et al. / Basic and Applied Ecology 17 (2016) 377–387
383
Fig. 4. Effect of productivity, temperature and precipitation on the net neighbor effect (effect size d) on invasive species emergence (A, E,
I), plant size (B, F, J), reproduction (C, G, K) and survival (D, H, L). Positive effect size d indicates negative effect of neighbors on invasive
species performance (competition) while a negative effect size d indicates a positive effect of neighbors on invasive species performance.
NPP, temperature and precipitation were averaged for the growing season or duration of the experiment.
When analyzing different invader functional groups separately our results remain quite consistent with our previous
results (Fig. 4, Appendix E). NPP was not a significant predictor of neighbor effects on emergence, size or survival of invasive forbs, emergence of invasive shrubs or size of invasive
grasses (Appendix F). Temperature was positively associated
with neighbor effect on the size of invasive forbs, but not the
size of invasive grasses (Appendix F). This indicates that the
relationship we observed between temperature and neighbor
effect on size is mainly driven by invasive forbs. Consistent
with Fig. 4, temperature was not related to emergence or
survival, independent of functional group. Precipitation was
positively associated with neighbor effect on invasive forb
and shrub emergence as well as on the effect on the size
of invasive forbs (Appendix F). Interestingly, when looking
at different functional groups, precipitation was negatively
associated with neighbor effect on invasive forb survival
(Appendix F). The relationship between productivity and
environmental conditions on invader’s reproduction could not
be assessed by functional group due to small sample size.
Discussion
We found a consistent pattern of change in net neighbor
effect along precipitation and temperature gradients. This is
in spite of having found a limited number of case studies
that experimentally manipulated the presence of neighbors
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to evaluate their effects on invasive species (Appendix C),
which reflects an important hole in our knowledge about invasive species and their interaction with native species. Overall,
we found that native communities have a negative impact on
invasive species at all measured life stages, indicating biotic
resistance (Fig. 3), while examples of biotic assistance were
uncommon (Appendix D: Fig. 1). However, we found significant heterogeneity between studies (Appendix B) which
highlights the limitations of comparing the effect of different community types on invaders and further stresses the need
explain the variation between studies by including, for example, environmental variables. We found that the strength of the
interaction was partly explained by the habitat’s temperature
and precipitation, but not by productivity (Fig. 4). Our results
support the stress gradient hypothesis (Bertness & Callaway
1994; Maestre, Callaway, Valladares, & Lortie 2009) indicating that net neighbor effects are dependent on abiotic
conditions (Fig. 1): stronger suppression of invasive species
under warmer and wetter conditions and neutral to facilitative interactions under more stressful conditions. We found no
support for a relationship between the strength and/or direction of the interaction and productivity as proposed by Grime
(1973) (Fig. 1).
Facilitation seems to be a common outcome of plant–plant
interactions among native plants (Brooker et al. 2008; Venail
et al. 2014). Venail et al. (2014) found, when reviewing
– mostly observational – studies testing Darwin’s naturalization hypothesis, that facilitative interactions were almost
as common as competitive interactions. However, this does
not seem to be the case for the interaction between native
communities and invasive species. Further, when evaluating the effect of neighbors on species survival, studies have
found that neighbors tend to have neutral to positive effects,
while negative effects are commonly found on plant growth
(Howard & Goldberg 2001; Maestre et al. 2009). In our metaanalysis, this was not found when looking at the interaction
between native communities and invasive species. Although
the overall negative effect on survival was not as strong
as on the other response variables (Fig. 3), facilitation was
rare (Appendix D: Fig. 1). Invasive species facilitation may
be uncommon because of their strong competitive ability
(Levine et al. 2003; Vila & Weiner 2004), or potentially
because they invade areas close to their ecological optimum
(Reisner et al. 2015); both being good predictors of facilitation (Brooker & Callaghan 1998; Liancourt, Callaway,
& Michalet 2005). Although negative impacts on facilitator species are known to occur even within native species
(Schöb et al. 2014) they are thought to destabilize or select
against facilitation (Bronstein 2009). The lack of evidence for
facilitation may also be a result of the experimental designs
included in our analyses. Venail et al. (2014) reviewed mostly
observational studies, in contrast to the experimental studies included in our meta-analysis. Both observational and
experimental studies have been commonly used to measure
facilitation, but greater evidence for facilitation comes from
observational studies (Maestre et al. 2005).
Stressful habitats are generally assumed to be less susceptible to invasion, although in our meta-analysis we found
no direct effect (in the absence of the native community) of
environmental conditions on invasive species performance.
This is potentially driven by the fact that we are evaluating different species, each potentially invading areas with
climatic conditions to which they are adapted. In fact, modeling invasive species climatic niches has been one of the
tools used for predicting invasions (Thuiller et al. 2005;
Nuñez & Medley 2011). However, when looking at individual species responses, they have been shown to respond to
biotic and abiotic gradients (Chambers et al. 2007; Gerhardt
& Collinge 2007; Harrison et al. 2015). Environmental conditions did nonetheless affect the interaction between native
communities and invasive species. The relationship between
temperature and precipitation and the effect of neighbors on
invasive species performance is consistent with the stress
gradient hypothesis (Bertness & Callaway 1994; Maestre
et al. 2009). Under more stressful conditions (lower average temperature and precipitation) the effects of the resident
communities on the invaders were found to be weaker or
slightly positive (though not significant) (Fig. 4, Appendix
D). Although stressful conditions may be a relative term
(Körner 2003), we found temperatures of around 9–15 ◦ C
or precipitation of 0–50 mm per month to result in weaker
effects of the resident community on the emergence and size
of invaders (Fig. 4). Abiotic conditions seem therefore to
at least partially determine whether the effect of resident
communities on invasive species results in biotic resistance
or assistance, and the strength of the positive or negative
effect (Fig. 1). However, significant variation remained across
studies (Appendix B). Measuring environmental variables
at more local scales and accounting for other potentially
important abiotic factors (e.g. nutrients) may help better
explain the variation in the effect of neighbors on invasive
species (Fig. 1). Similar results were found at a withincommunity scale by von Holle (2005, 2013), where the
native community had a negative effect on invasive species
under more favorable conditions, but not under stressful
conditions.
In general, when separating invasive species by their functional groups, we find similar results to those in Fig. 4,
supporting the stress gradient hypothesis (Appendix F). The
one exception to the stress gradient hypothesis in our results
was observed in the lack of a negative effect on invasive forbs
survival in the more moist environments (Appendix F), however, this was only observed for invasive forbs, but not shrubs
(Appendix F). Overall, invasive forbs were more responsive
to the effect of neighbors along precipitation and temperature
gradients, while the contrary seems to be true for invasive
grasses (Appendix F). This may be explained by a higher
root to shoot ratio in invasive grasses which may make them
stronger competitors and less susceptible to environmental
stressors (Caldwell & Richards 1986; Gordon, Menke, &
Rice 1989; Pywell et al. 2003; Hoekstra, Suter, Finn, Husse,
& Luescher 2015).
G.C. Stotz et al. / Basic and Applied Ecology 17 (2016) 377–387
Productivity, as measured here at broad scales, seems
to have no impact on species interactions. Although the
inclusion of more studies, across a broader range of productivity values is needed to assess the role of productivity on
plant–plant interactions, our results are consistent with the
growing body of evidence suggesting that productivity is not
a strong proxy for competition strength (Fig. 1, Goldberg
et al. 1999; Maestre et al. 2005; Bennett & Cahill 2012). The
way productivity is measured may be inadequate as we tend to
ignore belowground biomass which may represent up to 80%
of the total biomass of a community (Lamb & Cahill 2006).
Alternatively, competition may not depend on community
attributes, such as productivity, but rather on the balance of
resource supply and demand (Davis, Wrage, & Reich 1998;
Davis, Grime, & Thompson 2000). Our results also show that
temperature and precipitation, within the ranges of included
studies (Fig. 2), are better predictors of competition, however,
the mechanisms behind their impact on species interactions
need to be further explored. Maestre et al. (2009) suggested
that facilitation is more probable when stress is caused by
a non-resource-related environmental factor such as salinity
or pH, while competition is more probable under resourcerelated stress. However, temperature and precipitation can
have mixed effects. They are not only a measure of nonresource stress, but also are related to resource availability.
Both precipitation and temperature are related to water availability and can alter microbial activity and nutrient cycling in
the soil affecting the amount of resources available to plants
(Brady & Weil 2007). Further research is needed to disentangle the mechanisms behind the effects of environmental
conditions on plant–plant interactions.
Conclusion and synthesis
Combining meta-analysis and remote sensing data enabled
us to test hypotheses among, instead of just within, sites
allowing for broader generalizations; however, the use of
remote sensing data measured at broad scale is not without limitations. Moreover, we wish to use this article to
emphasize the necessity of more experimental studies to
be performed in different geographic locations and community types to better understand the interaction among
native communities and invasive species. We found that
native plant communities resisted invasion, which limited
the emergence, growth, reproduction and survival of invasive species. Although there is variation in the effect on
invasive species, facilitation was not found to be a common outcome. The variation in the strength of the interaction
could not be explained by the habitat productivity, but in
part, by temperature and precipitation. Understanding why
some communities are more susceptible to invasion than
others is important not only to target invasive species management strategies, but also to understand the mechanisms
behind invasion, species interactions and overall community
assembly.
385
Acknowledgements
We thank Klaus Hövemeyer and two anonymous referees
whose comments helped improve this manuscript. We would
like to thank Charlene Nielsen for assistance in obtaining data
from GloPEM, MODIS and GPCC datasets. We would also
like to thank. E. Badano, N. Barger, L. Pfeifer-Meister and P.
Saccone for providing us with information and/or data from
their studies. This research was supported by NSERC Discovery and Accelerator Grants to JFC. GCS was supported
by CONICYT Becas-Chile scholarship. GJP was supported
by a University of Alberta Doctoral Recruitment scholarship.
Appendix A. Supplementary data
Supplementary data associated with this article can be
found, in the online version, at http://dx.doi.org/10.1016/
j.baae.2016.04.001.
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