Do seeds from invasive bromes experience less granivory than seeds from native congeners in the Great Basin Desert?

Abstract

In part, the enemy release hypothesis of plant invasion posits that generalist herbivores in the non-native ranges of invasive plants will prefer native plants to exotic invaders. However, the extent to which this occurs in natural communities is unclear. Here, I examined the foraging preferences of an important guild of generalist herbivores—granivorous rodents—with respect to seeds from a suite of native and invasive Bromus (“brome”) species at five study sites distributed across ≈ 80,000 km² of the Great Basin Desert, USA. By examining only congeners, I accounted for a potentially large source of interspecific variation (phylogenetic relatedness). In general, granivorous rodents removed seeds from native bromes at a 23% higher rate than seeds from invasive bromes, suggesting a preference for native species. This preference was not entirely explained by seed size, and patterns of seed removal were consistent across study sites. These findings suggest that invasive bromes in the Great Basin might experience less rodent granivory than native congeners, which is consistent with a key prediction derived from the enemy release hypothesis.

Full text

Do seeds from invasive bromes experience less granivory
than seeds from native congeners in the Great Basin Desert?
Jacob E. Lucero
Received: 15 February 2018 / Accepted: 7 July 2018
ÓSpringer Nature B.V. 2018
Abstract In part, the enemy release hypothesis of
plant invasion posits that generalist herbivores in the
non-native ranges of invasive plants will prefer native
plants to exotic invaders. However, the extent to which
this occurs in natural communities is unclear. Here, I
examined the foraging preferences of an important
guild of generalist herbivores—granivorous rodents—
with respect to seeds from a suite of native and
invasive Bromus (‘‘brome’’) species at five study sites
distributed across &80,000 km
2
of the Great Basin
Desert, USA. By examining only congeners, I
accounted for a potentially large source of interspeci-
fic variation (phylogenetic relatedness). In general,
granivorous rodents removed seeds from native
bromes at a 23% higher rate than seeds from invasive
bromes, suggesting a preference for native species.
This preference was not entirely explained by seed
size, and patterns of seed removal were consistent
across study sites. These findings suggest that invasive
bromes in the Great Basin might experience less
rodent granivory than native congeners, which is
consistent with a key prediction derived from the
enemy release hypothesis.
Keywords Bromus Enemy release hypothesis 
Generalist herbivores Granivory Great Basin 
Rodents
Introduction
One of the most well-known explanations for the
success of introduced plants in their non-native ranges
is enemy release (Elton 1958; Keane and Crawley
2002). In part, this hypothesis predicts that generalist
and specialist herbivores in recipient communities will
selectively consume native species over exotic, inva-
sive species, resulting in relative freedom from
herbivory for invaders (Fig. 1 in Keane and Crawley
2002). However, with respect to generalist herbivores,
this prediction is not necessarily intuitive. Generalists
are equipped to attack a variety of host species and are
found in both the native and non-native ranges of
exotic species. Thus, both native and translocated
plants in any community could be attacked by
generalists. In this context, there may be ‘‘no obvious
reason’’ (Keane and Crawley 2002) why exotic plants
Communicated by Lauchlan Fraser.
Electronic supplementary material The online version of
this article (https://doi.org/10.1007/s11258-018-0858-7) con-
tains supplementary material, which is available to authorized
users.
J. E. Lucero (&)
Division of Biological Sciences and the Institute on
Ecosystems, University of Montana, Missoula, MT 59812,
USA
e-mail: jacob.lucero@umontana.edu
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Plant Ecol
https://doi.org/10.1007/s11258-018-0858-7

in recipient communities should escape generalist
herbivory relative to natives.
Empirical studies evaluating the responses of native
generalists to native versus exotic plants have yielded
mixed results. Some authors have found that native
generalists avoid (Lankau et al. 2004; Pearson et al.
2011; Maron et al. 2012; Enge et al. 2013; Lieurance
and Cipollini 2013; Lucero et al. 2015) or perform
poorly on exotic plants relative to natives (Schaffner
et al. 2011). Others have suggested that native
generalists do not distinguish between native and
exotic plants (Blaney and Kotanen 2001). Still others
have reported that native generalists prefer exotic
plants to natives (Parker and Hay 2005; Morrison and
Hay 2011). Thus, the extent to which native general-
ists selectively consume native plants over exotic-
invasive plants is unclear. This knowledge gap is
significant because relative freedom from generalist
herbivory is an essential (Keane and Crawley 2002),
but poorly understood (Torchin and Mitchell 2004;
Liu and Stilling 2006; Blumenthal 2006) aspect of
enemy release.
The Great Basin Desert, USA, presents unique
opportunities to evaluate the extent to which native
generalists select native plants over exotic invaders.
The Great Basin is home to several species of
granivorous rodents—important generalists that can
strongly influence the organization of local plant
communities (Larios et al. 2017; Bowman et al. 2017).
These generalists consume seeds from many species,
including both native and invasive species of Bromus
(‘‘brome’’; Poaceae) (Flake 1973). Native bromes in
the Great Basin include B. marginatus, B. carinatus,
and B. vulgaris; and invasive bromes include B.
rubens, B. inermis, and B. tectorum. Invasive bromes
can degrade native communities by disrupting fire
regimes (D’Anotonio and Vitousek 1992; Balch et al.
2013), soil processes (Norton et al. 2008), food webs
(Lucero et al. 2015), and by competitively displacing
native species (Humphrey and Schupp 2004; Williams
and Crone 2006; Vasquez et al. 2008; Besaw et al.
2011; Parkinson et al. 2013). These disruptions can
drastically reduce the biodiversity of local communi-
ties (Williams and Crone 2006; Ostoja and Schupp
2009; Pearson et al. 2016).
Interestingly, there is some evidence that Great
Basin rodents may prefer seeds from native species to
seeds from invasive bromes (Kelrick et al. 1986;
Ostoja et al. 2013; Lucero et al. 2015), even when
plant traits are otherwise similar (Lucero 2017). For
example, Lucero (2017) showed that Great Basin
rodents avoided seeds from B. tectorum relative to
seeds from a suite of native grass species, including
Festuca idahoensis, which produces seeds that are &
60% smaller than B. tectorum. Thus, seeds from
invasive bromes could disproportionately escape an
important form of generalist herbivory—post-disper-
sal seed predation—relative to seeds from native
species, although the extent to which this occurs
remains unclear. In addition, the genus Bromus has
produced a large number of exceptionally invasive
species in western North America (Germino et al.
2016), and no study has evaluated whether these
invasive bromes escape granivory relative to native
congeners. In general, comparing native and invasive
congeners helps to account for an important source of
variation among species—phylogenetic relatedness
(Agrawal and Kotanen 2003; Agrawal et al. 2005). My
objective was to examine the foraging preferences of
an important guild of generalist herbivores—graniv-
orous rodents—with respect to seeds from a suite of
native and invasive Bromus congeners across a large
portion of the Great Basin.
Methods
Plant materials
Native bromes used for this study were B. marginatus
(perennial), B. carinatus (perennial/facultative
annual) and B. vulgaris (perennial); and invasive
bromes were B. inermis (perennial), B. tectorum
(annual), and B. rubens (annual). These species are
broadly distributed across western North America, and
native and invasive bromes commonly co-occur in the
Great Basin, although invasive bromes often displace
native species (Salo 2005; Dillemuth et al. 2009;
Pearson et al. 2016). Each of these invasive bromes
meets all criteria proposed by Blackwell et al. (2011)
for invader status. Specifically, each invasive brome
(1) was introduced to the Great Basin from a distant
native range (i.e., Eurasia and/or northern Africa), (2)
has successfully established self-sustaining popula-
tions, and (3) has considerably expanded its non-
native range since introduction (Mack 1981; D’Ano-
tonio and Vitousek 1992;Salo2005; Dillemuth et al.
2009). Bromus tectorum has been called the most
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‘‘significant’’ (D’Anotonio and Vitousek 1992) inva-
sive plant in the Great Basin, but B. rubens and B.
inermis can also extirpate native competitors and
dominate local communities (Salo 2005; Dillemuth
et al. 2009). Table 1describes how I procured seeds of
each species.
Study area
I conducted preference experiments at five study sites
distributed across &80,000 km
2
of the Great Basin.
Study sites were located near Jackpot, NV
(41°55028.7000N, 114°43044.9600 W); McGill, NV
(39°58026.5100N, 114°40010.1000 W); Elko, NV
(41°3049.4000N, 115°49044.0200 W); Winnemucca, NV
(40°54047.0000N, 117°23056.9600 W); and Vernon, UT
(40°6054.9900N, 112°3204.3700 W). All sites were
located on public land managed by the US Bureau of
Land Management and in plant communities domi-
nated by big sagebrush (Artemisia tridentata) with \
5% cover by invasive plants. All sites were separated
by at least 100 km, which is farther than granivorous
rodents and most plants can typically disperse over
short time periods (Harper et al. 1978; O’Farrell 1978;
Jones 1989). Thus, study sites sampled independent
communities.
Experimental design
I examined the seed preferences of granivorous
rodents at seven sampling stations per study site, each
separated by 50 m. Each sampling station consisted of
six feeding trays constructed from 150 925 mm petri
dishes, 3/4-filled with on-site soil filtered through a
500 lm sieve. Trays were placed in a rectangular
configuration (two rows of three trays) on the ground,
with all trays spaced &7 cm apart. Each feeding tray
received 3 g of seed from one of the six brome species
named above. Brome species were randomly assigned
to feeding trays, and seed offerings were thoroughly
incorporated into the filtered soil. Burying seeds in this
manner made them largely inaccessible to granivorous
ants, which do not dig for buried seeds (MacMahon
et al. 2000).
I left trays undisturbed in the field for 72 consec-
utive hours, after which they were collected and
processed. Data collection ended on Oct. 17, 2016. I
recovered seeds remaining in feeding trays by passing
the trays’ contents (filtered soil, debris introduced by
foraging rodents, remaining seeds) through a 500 lm
sieve, through which soil passed easily but not seeds. I
removed dirt and organic debris associated with
recovered seeds and then weighed the sample to the
nearest 0.01 g. I subtracted this weight from the
original 3 g to determine the mass of seeds removed
by rodents. I log-transformed seed removal data to
improve normality. I assumed that seed preference and
seed removal were positively related such that high
seed removal indicated high preference.
Statistical analysis
To evaluate the species- and provenance (i.e., whether
a species is locally native or exotic)-specific seed
preferences of granivorous rodents, I employed a
linear mixed-effects model using the lmer function in
Table 1 Mass (mg) of
Bromus seeds (per
seed ±SE) and how seeds
were procured. Native
species are labeled with an
‘‘N,’’ and invasive species
are labeled with an ‘‘I’’
Species Mass (mg) Mode of accession
Bromus marginatus (N) 7.1 (0.3) Purchased from Granite Seed Co., Lehi, UT
June 2016
Bromus carinatus (N) 6.6 (0.2) Purchased from Granite Seed Co., Lehi, UT
June 2016
Bromus vulgaris (N) 3.7 (0.1) Purchased from Silver Falls Seed Co., Silverton, OR
June 2016
Bromus inermis (I) 3.8 (0.2) Purchased from Granite Seed Co., Lehi, UT
June 2016
Bromus tectorum (I) 3.2 (0.1) Hand-collected by me on public land near Lehi, UT
June 2016
Bromus rubens (I) 3.1 (0.1) Purchased from outsidepride.com, Independence, OR
June 2016
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R (R Development Core Team 2018). This function
uses Satterthwaite’s method to calculate denominator
degrees of freedom (‘‘df’’ in Online Resource 1) and
Tukey’s method to compare multiple means. I treated
species identity and provenance as fixed factors and
study site as a random factor. Treating study site as a
random factor statistically accounted for any in situ
differences among study sites, including rodent iden-
tity/density and plant community composition.
Seed selection by rodents can depend on seed
mass—rodents generally prefer large seeds to small
ones (Reader et al. 1993; Pearson et al. 2011; Maron
et al. 2012 and references therein). This is important in
the context of this study because seed size varied
among the experimental brome species (Table 1). The
linear mixed-effects model described above did not
include seed mass as a covariate because seed size did
not interact with any of the model’s fixed factors—
each brome species had only one mean seed size and
not all seed sizes were represented in both native and
invader provenance groups. Therefore, to account for
any effects of seed mass at the provenance level, I
compared the mass of Bromus seeds (per seed) in
native and invader provenance groups using a ttest. If
seed mass is similar between provenance groups
(P[0.05), any significant main effect of provenance
detected by the linear mixed-effects model described
above cannot be fully ascribed to provenance-specific
differences in seed mass. I accounted for seed size
within provenance groups by regressing seed removal
against seed mass using the reg function in R (R
Development Core Team 2018). I predicted seed
removal to be positively related to seed mass within
provenance groups, as reported by other studies in
similar systems (Reader 1993; Pearson et al. 2011;
Maron et al. 2012; Connolly et al. 2014).
Results
The linear mixed-effects model revealed a significant
main effect of species (P\0.01) and a significant
main effect of provenance (P= 0.01), indicating that
rodents foraged selectively at both the species and
provenance levels (Fig. 1, Online Resource 1). At the
species level, rodents removed 2.14 g ±0.37 of B.
marginatus, 2.02 g ±0.37 of B. carinatus,
0.30 g ±0.37 of B. vulgaris, 1.91 g ±0.39 of B.
inermis, 1.26 g ±0.37 of B. tectorum, and
0.27 g ±0.37 of B. rubens per sampling station
(±SE; t-ratios and P-values of all pairwise contrasts
reported in Table 2). Thus, at the species level, rodents
preferred the seeds of some species to others but did
not always distinguish between native and invasive
bromes (Fig. 1). However, rodents did distinguish
between native and invasive bromes at the level of
species provenance. At the provenance level, rodents
removed 1.49 g ±0.27 seeds of native bromes com-
pared to 1.15 g ±0.27 seeds of invasive bromes per
sampling station (±SE) (t-ratio = 2.51, P= 0.01),
indicating that rodents removed seeds of native
bromes at a 23% higher rate than seeds of invasive
bromes (Fig. 1).
Patterns of seed removal were related to seed mass
within but not between provenance groups. Within
provenance groups, patterns of seed removal were
positively related to seed mass (adj. R
2
= 0.34,
P\0.001 for native species; adj. R
2
= 0.23,
P= 0.008 for invasive species), suggesting that
rodents selectively foraged for large seeds. However,
this was not the case between provenance groups
because seeds of native and invasive bromes did not
differ in mass. When pooled together, native seeds
Fig. 1 Mean (±SE) mass (g) of seeds from Bromus margina-
tus (Brma), Bromus carinatus (Brca), Bromus vulgaris (Brvu),
Bromus inermis (Brin), Bromus tectorum (Brte), and Bromus
rubens (Brru) removed by granivorous rodents during prefer-
ence experiments. Seed removal of native bromes is shown with
light gray bars, and seed removal of invasive bromes is shown
with dark gray bars. Within provenance groups, species are
arranged in descending order of seed mass (see Table 1). I
assumed that seed removal and seed preference were positively
related. Means that do not share letters differ significantly
(P\0.05)
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weighed 5.80 mg ±2.33 SE per seed, and invader
seeds weighed 3.34 mg ±0.46 SE per seed (t= 2.25,
P= 0.14). Thus, the significant main effect of prove-
nance (P= 0.01; Fig. 1, Online Resource 1) was not
entirely driven by provenance-specific differences in
seed size.
Variation in seed removal was low among study
sites (variance = 0.05, SD = 0.23), suggesting that
rodent seed preferences were consistent at the spatial
scale of this study. P-values associated with random
effects (study site in this case) can be controversial
(Baayan et al. 2008), and are therefore not reported.
Discussion
The enemy release hypothesis of plant invasion
predicts that native generalists in recipient communi-
ties should selectively forage for native plant species
over exotic invaders, but the extent to which this
occurs in wild communities is unclear. Here,
granivorous rodents—an important guild of general-
ists in the Great Basin—selectively foraged for seeds
from native bromes over seeds from invasive bromes
at the level of species provenance (Fig. 1, Online
Resource 1). This result coincides with studies from
various systems reporting that native generalists prefer
native plants to invasive plants (e.g., Cappuccino and
Carpenter 2005; Pearson et al. 2011; Maron et al.
2012; Enge et al. 2013; Connolly et al. 2014; Lucero
et al. 2015). My results are unique in that I examined
generalist preferences for native and invasive con-
geners. The use of congeners is important because it
accounts to some degree for variation caused by
phylogenetic differences between native and invasive
species (Agrawal and Kotanen 2003; Agrawal et al.
2005). In addition, I examined rodent seed preferences
over an exceptionally large spatial scale.
Rodents in the Great Basin often prefer seeds from
native plants over seeds from invasive bromes (most
notably B. tectorum) in choice tests (Kelrick et al.
1986; Ostoja et al. 2013; Lucero et al. 2015), but the
reasons why remain unclear. Kelrick and MacMahon
(1985) suggested that seeds of invasive bromes may
have relatively poor nutritional quality compared to
similar-sized seeds of natives, but they did not
examine seeds from congeneric pairs. Alternatively,
seeds of invasive bromes may be armed with biogeo-
graphically novel phytochemicals that act as ‘‘novel
weapons’’ (Callaway and Aschehoug 2000) to deter
rodent granivory. Novel phytochemistry has been
invoked to explain low rates of herbivory on invasive
plants relative to native competitors in a number of
systems (Cappuccino and Carpenter 2005; Vermeij
et al. 2009; Enge et al. 2013) but has yet to be explored
among Bromus species.
Seed size explained patterns of seed removal within
but not between provenance groups. Granivorous
rodents often select large seeds over small ones
(Reader et al. 1993; Pearson et al. 2011; Maron et al.
2012 and references therein), which is germane to this
study because seed size differed among the Bromus
species I evaluated. Specifically, if seeds of native
bromes were generally larger than seeds of invasive
bromes, the significant main effect of provenance
reported here (Fig. 1, Online Resource 1) could have
been an artifact of seed size. However, seeds from
native and invasive bromes were generally the same
weight (t= 2.25, P= 0.14), suggesting that selective
foraging for native bromes (Fig. 1, Online Resource 1)
Table 2 Species-species pairwise contrasts (see ‘‘Methods’’
for model information) of the quantity of seeds (g) removed by
granivorous rodents during preference experiments
Pairwise contrast t-ratio Pvalue
Brin—Brru -2.61 0.11
Brin—Brte -1.20 0.84
Brin—Brca 0.80 0.97
Brin—Brma 2.11 0.30
Brin—Brvu -2.46 0.16
Brru—Brte 1.46 0.69
Brru—Brca 3.52 0.01
Brru—Brma 4.88 < 0.001
Brru—Brvu 0.15 1.00
Brte—Brca 2.07 0.32
Brte—Brma 3.43 0.01
Brte—Brvu -1.31 0.78
Brca—Brma 1.36 0.75
Brca—Brvu 3.37 0.02
Brma—Brvu -4.73 < 0.001
Species are: Bromus inermis (Brin), B. rubens (Brru), B.
tectorum (Brte), B. carinatus (Brca), B. marginatus (Brma), B.
vulgaris (Brvu). The provenance of each species is given in
Table 1. Statistically significant contrasts (P\0.05) appear in
bold
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was driven by something besides or in addition to seed
size. In contrast, patterns of seed removal within
provenance groups were clearly related to seed
mass—rodents selectively foraged for large seeds
(adj. R
2
= 0.34, P\0.001 for native species; adj.
R
2
= 0.23, P= 0.008 for invasive species). This
finding coincides with a number of other studies
(Reader 1993; Pearson et al. 2011; Maron et al. 2012;
Connolly et al. 2014; Lucero 2017) but should be
interpreted with some caution here because interspeci-
fic variation in seed size was relatively modest. By
comparison, other studies that have examined seed
removal as a function of seed size have explored
ranges of seed mass that were orders of magnitude
greater that the ranges explored here (Reader 1993;
Maron et al. 2012; Connolly et al. 2014).
Given these data, it is tempting, but probably
inappropriate, to relate seed size per se to invasion
success. In general, the relationship between seed size
and invasion success is unclear. Large-seeded species
are often better competitors than small-seeded species
during establishment (Wulff 1986; Turnbull et al.
1999), but large-seeded species may be more vulner-
able to the effects granivory (Reader 1993; Maron
et al. 2012). This dichotomy may help explain why
empirical studies disagree over seed size-invasiveness
relationships. For example, Daws et al. (2007) and
Novoa et al. (2016) reported a positive relationship
between seed size and invasiveness, but Phillips and
Murray (2012) and Gallagher et al. (2014) reported no
relationship. Interestingly, none of these studies
considered how the effects of seed size, granivory,
and plant–plant competition might interact to influ-
ence community-level patterns. In this context, my
results should be interpreted only in terms of rodent
preferences for native versus invasive bromes.
I sampled rodent preferences across a large portion
of the Great Basin (&80,000 km
2
), but in situ
variation in seed removal was low (variance = 0.05,
SD = 0.23), suggesting that rodent seed preferences
were consistent across study sites. However, this may
not always be the case. Selective consumers like
rodents may become less choosy as the availability of
more-preferred food resources decreases (Krebs et al.
1977; Pulliam 1974). Thus, Great Basin rodents may
become less selective at times and/or places of
pronounced resource scarcity, such as years of low
seed productivity (Brown et al. 1979), booms in rodent
density (Hoset et al. 2014), or places where more-
preferred native competitors have been extirpated by
less-preferred exotic invaders. The foraging behavior
of selective generalists may also depend on the
abundance, density, proximity, and identity of neigh-
boring food resources (Holt 1977; Holt and Kotler
1987; Barbosa et al. 2009; Underwood et al. 2014).
Seeds of invasive bromes experienced less rodent
granivory than seeds of native bromes at the prove-
nance level (Fig. 1, Online Resource 1), but I did not
directly test the enemy release hypothesis. The central
tenet of the enemy release hypothesis postulates that
native herbivores—including both specialists and
generalists—limit populations of invasive plants in
their native communities but not in their recipient
communities (Elton 1958; Maron and Vila 2001;
Keane and Crawley 2002). This idea can be tested by
excluding herbivores in both the native and non-native
ranges of invasive plants and then comparing the
effects of herbivore exclusion in each range (see
DeWalt et al. 2004; Williams et al. 2010; Lucero 2017
for empirical examples). I did not employ this
biogeographically explicit experimental design, nor
did I explore the population-level consequences of
seed preference. Thus, I did not directly evaluate
whether invasive bromes experienced enemy release
from the effects of rodent granivory.
However, previous work in this system strongly
suggests that B. tectorum has indeed experienced
enemy release from the effects of rodent foraging
(Lucero 2017; Lucero and Callaway 2018). Experi-
mental exclusion of granivorous rodents from seed
addition plots improved B. tectorum establishment by
approximately 60% in Iran (part of the native range)
but had no significant effect across a large portion of
the Great Basin (part of the non-native range) (Lucero
2017). In addition, rodent foraging in the Great Basin
reduced the establishment of a suite of native grass
species by at least 80% each but had no significant
effect on the establishment of B. tectorum (Lucero and
Callaway 2018). Thus, rodent foraging limited B.
tectorum establishment in the native range but not in
the non-native range, and B. tectorum disproportion-
ately escaped the effects of rodent granivory relative to
native competitors in the non-native range. Together,
these findings indicate that B. tectorum in the Great
Basin has experienced some degree of enemy release
from the effects of rodent foraging, which may help
explain its exceptional invasiveness (Balch et al. 2013;
Pearson et al. 2016) in this region.
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Given the evidence that B. tectorum in the Great
Basin has experienced enemy release from the effects
of rodent foraging, rodent interactions with B. tecto-
rum could have driven the significant main effect of
provenance reported here (Fig. 1, Online Resource 1).
To test this, I omitted B. tectorum from the linear
mixed-effects model described in the ‘‘Methods’’ and
reanalyzed the data. If rodent interactions with B.
tectorum drove the significant main effect of prove-
nance reported above, then excluding B. tectorum
from the data should have yielded a non-significant
main effect of provenance (i.e., P[0.05). This was
not the case. Even with B. tectorum excluded, the main
effect of provenance remained significant (t-ra-
tio = 2.21, P= 0.03), suggesting that rodent interac-
tions with B. tectorum seeds did not drive the
significant main effect of provenance (Fig. 1, Online
Resource 1). Thus, B. inermis and B. rubens may be
gravid for the kinds of biogeographically explicit tests
of enemy release that have been performed on B.
tectorum (Lucero 2017; Lucero and Callaway 2018).
There are several important experimental caveats.
First, preference experiments lasted only 72 h during a
single growing season. Experiments were broadly
replicated in space, but I only considered a snapshot of
rodent preferences. In addition, I reemphasize that
selective foraging for native seeds (Fig. 1) does not
necessarily translate to a recruitment or establishment
advantage for invasive bromes relative to native
bromes, especially if plants are microsite- rather than
seed-limited (Maron and Crone 2006). Furthermore,
seeds of native and invasive bromes were similar in
size at the a= 0.05 significance level (P= 0.14), but
this P-value could be viewed as marginally significant.
Therefore, I cannot entirely discount the possibility
that seed size influenced patterns of seed removal
between provenance groups. Finally, it is important to
recognize that escape from generalist granivores is
only one of many non-mutually exclusive factors that
potentially influence the success of exotic bromes in
the Great Basin. Other factors could include distur-
bance regimes, feedbacks with the biotic and abiotic
environment, and strong interactions with native
species (D’Anotonio and Vitousek 1992; Mitchell
et al. 2006; Norton et al. 2008; Catford et al. 2009;
Blackwell et al. 2011; Balch et al. 2013).
I found that invasive bromes in the Great Basin
might experience less rodent granivory than native
congeners (Fig. 1), which is consistent with a key
prediction derived from the enemy release hypothesis
(Keane and Crawley 2002). By supporting classic
theory on enemy release, this main result underscores
the potential for generalist herbivores to influence the
trajectory of exotic plant invasions.
Acknowledgements I am grateful for funding from task
agreement P14AC00728 between the National Park Service and
the Ragan M. Callaway Lab at the University of Montana, the
Montana Institute on Ecosystems, National Science Foundation
Established Program to Stimulate Competitive Research Track-
1 EPS-1101342 (INSTEP 3), and the Organismal Biology and
Ecology Program at the University of Montana. I especially
thank Ray Callaway for his excellent guidance and feedback.
Compliance with ethical standards
Conflict of interest The authors declare that they have no
conflict of interest.
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