Discussion
Our study uniquely assessed the simultaneous responses of plants,
insects, and soil microbes to gradients of invasion at multiple study
sites with two different invasive brome species. Overall, invasive
annual brome abundance was more strongly related to plant community
composition than insect and soil microbial communities. B.
tectorum also had stronger associations with insects and soil microbes,
suggesting communities show differential sensitivity to invasion based
on taxa and that even apparently similar invasive species (congeneric
C3 winter annual grasses of the same genus) may impact
communities in unique ways.
Plant species richness significantly decreased with brome invasion, and
community and functional composition shifted with invasion, aligning
with previous work (Gasch et al. 2013), as annual bromes often have a
competitive advantage over native species. B. arvensis andB. tectorum germinate in the fall or spring depending on climatic
conditions, allowing them to utilize available nutrients and moisture
earlier than perennial species (Germino et al. 2016). We found declines
with invasion in C4 perennial grasses across all
gradients. C4 perennials, growing later in the season,
are sensitive to light availability (Still et al. 2003). As annual
bromes use available moisture and decrease light earlier in the season,
they outcompete native C4 species, reducing
C4 abundance (Chambers et al. 2007). In Montana, most
plant functional groups were negatively associated with increasing
invasion, suggesting B. arvensis may create wide-ranging plant
compositional shifts in this system.
While insect richness did not vary consistently with invasion, insect
community and functional composition significantly differed with
invasion across all gradients except one (functional composition in
Wyoming B. arvensis gradients). As annual bromes shift plant
composition, insect communities are also likely to change, given the
feedback between available plant species and arthropod presence (Biere
and Bennett 2013). For both insects and plants, functional composition
results largely paralleled community composition results, suggesting a
lack of functional redundancy with potential consequences for ecosystem
services such as palatable forage availability, pollination, and pest
control (Memmott and Waser 2002, Stout and Morales 2009, Kaiser-Bunbury
et al. 2011). When insect functional groups were considered
independently, we saw declines in leaf-chewing and sap-sucking
herbivores in Montana and increases in parasitoids and sap-sucking
herbivores in Wyoming B. arvensis gradients. The declines in
certain herbivores may be a reflection of less heterogenous habitat
(Germino et al. 2016) with increased invasion cover and/or a preference
for native forage species (Cumberland et al. 2016). However, the
increase in parasitoids supports a preference for annual brome species
as an oviposition site (Perez-Mendoza et al. 2006). Positive
relationships between annual brome species and insect abundance in
Wyoming also match prior work suggesting that bromes are associated with
higher insect abundance in this short-structured prairie (Duchardt et
al. 2021).
Insect herbivory was less common on annual bromes than native species.
Interestingly, across all years and study sites, invasion level was
never related to total insect biomass (Figure 4, Appendix S1: Figure S4,
Tables S5, S6). Based on these observations, we measured herbivory in
two years in Montana. We found that insect herbivores, under any
invasion level, preferred native forage species to invasive bromes.
While there is some evidence that certain insect herbivores prefer
native species over bromes later in the growing season, insect
herbivores will consume bromes earlier in the season (Cumberland et al.
2016). However, we found that both later in the season (2021) and early
in the growing season (2022), insect herbivores avoided consuming
invasive bromes. This supports our previous finding of a decline in
certain herbivore functional group abundances in Montana as well.
Combined with a lack of response of total insect biomass to invasion,
this could indicate substantial added pressure on native forage species,
as insects compete with livestock for forage (Branson and Haferkamp
2014).
We predicted that compositional and functional changes with invasion
would occur across plants, insects, and soil microbes. However, soil
microbial communities were markedly less sensitive to brome invasion
than other taxa considered as we saw marginal changes in B.
tectorum gradients only. At the functional group scale, we found strong
declines in functional groups associated with phototrophy, asBromus spp. can increase leaf litter (and thatch) and
decrease light availability (Still et al. 2003, Bennett et al. 2014).
Given that B. tectorum also utilizes large amounts of soil
nitrogen (Blank and Morgan 2012), observed negative associations betweenB. tectorum and various nitrogen processing microbes are also
logical. While B. tectorum has previously been linked to
decreased soil microbial abundance (Gasch et al. 2013) and altered
community composition (Nasto et al. 2022), potentially due to soil
moisture differences (Gasch et al. 2013), our results newly suggest more
limited associations between microbial functional groups and B.
arvensis , implying that the microbial communities may be resilient to
even large shifts in B. arvensis abundance, protecting services
associated with microbial communities like nutrient cycling (Batten et
al. 2006). Alternatively, our sequencing methodology and functional
groupings may only partly account for functional differences relative to
other methods (e.g., soil enzyme activity or transcriptomics),
potentially overinflating functional redundancy in our study (Louca et
al. 2016).
We found plants, insects, and soil microbes did not relate to B.
arvensis and B. tectorum equally. Given the functional
similarity of these two species (both are C3 winter
annual grasses), we expected fairly similar associations between the
invasives and plants, insects, and microbes. Our results suggest thatB. tectorum may have more substantial and far-reaching
consequences for community structure than B. arvensis . While
studies comparing B. arvensis and B. tectorum are lacking,
evidence suggests niche differentiation between the species,
particularly in terms of microsite preference (Porensky and Blumenthal
2016). Underlying differences in microsite, including light availability
(bare ground cover) soil texture, moisture, and nutrient availability,
may help explain the soil microbial differences seen between the species
(Porensky et al. 2018). Encouragingly, consequences of invasion for soil
functioning may not be too damaging under invasion by B.
arvensis . In general, this supports the idea that invasion studies and
management must consider invasive species identity, as well as
functional group (Roscher et al. 2009).
Overall, this work sheds light on the understudied consequences of
annual brome invasion in northern mixed-grass prairies for plants,
insects, and soil microbes. Species interactions shape ecosystem
functions, and these dynamics are influenced by biodiversity (Thébault
and Loreau 2005) and invasion. Annual brome invasion related to plant
and insect community structure and function, highlighting the potential
for cascading consequences of invasion by B. arvensis andB. tectorum for rangeland ecosystems. To the contrary, soil
microbial communities appeared to be more resistant to change in
relation to invasive abundance, suggesting resilience to invasive
bromes. Responses to invasion vary across taxa, so further studies are
needed to examine cross-community change. Understanding how invasion
alters community composition and functional group diversity across
rangeland communities is vital not only for long-term rangeland
sustainability (DiTomaso 2000), but also for advancing invasion science
and management (Ricciardi et al. 2017).