Traits response to herbivory
Overall, there was a high proportion of studies which found
non-significant trait responses to herbivory (Figure 6). At the study
level, plant traits might not change with herbivory because the traits
measured may not be indicators of specific plant-herbivore interactions
studied in their focal system. It may also be that some traits which
confer grazing tolerance/avoidance are also helpful, or of neutral
advantage under ungrazed conditions. This is particularly relevant for
vertebrate focussed studies which often compared plant traits values
between grazed areas and exclusion plots, which usually had grazers
excluded for between 5-10 years. The dominant plants that exist in these
exclosures likely possess traits which confer grazing
avoidance/tolerance, but these traits may not be a fitness disadvantage
to the plant in ungrazed conditions and remain similarly expressed.
Trait response to vertebrate herbivory was most frequently recorded for
SLA, LDMC, leaf nitrogen, plant height and leaf area; wherefor
invertebrate herbivory it volatile organic compounds (VOCs), leaf
nitrogen, aboveground biomass, total phenols and total tannins were most
frequent. Vertebrate herbivory was mostly positively correlated with
leaf nitrogen and SLA, and negatively with LDMC (Figure 6). As SLA and
leaf nitrogen are positively correlated with high relative growth and
LDMC positively correlated with leaf carbon content (Perez-Harguindeguy
et al., 2016), these results suggest that many of the plant species and
communities examined in these grassland studies, invest more in growth
to tolerate herbivory, and less in carbon based defensive structures to
avoid herbivory. This also aligns with the response of photosynthetic
capacity and leaf phosphorous content, which mostly responded positively
to vertebrate herbivory (Figure 6). Indirect influences from grazing
such as nitrogen deposition through urine and faeces, may also increase
the availability of nutrients in grazed environments and facilitate
growth (de Mazancourt et al., 1998). Tolerating herbivory through rapid
growth, is a common strategy for species from the Poaceae family, which
dominate grasslands. This is particularly true for grass species growing
in productive environments (Briske, 1996; Briske, 1999; Diaz et al.,
2007; Díaz et al., 2001), where their dominance is often mediated via
herbivory (Lunt et al., 2007). When grazers are removed in these
environments, dominant grasses can sometimes reach a point of maximum
growth, where restrictions space and/or nutrients limits further growth,
and their growth rates may decline. In this scenario, grasses may invest
more carbon in their stems and less in their leaves as structural
support to grow tall under competitive light conditions (Irving, 2015).
In contrast, some studies found negative relationships between
vertebrate herbivory and leaf area and plant height (Figure 6), which
are typical mechanisms of grazing avoidance, documented in many other
studies (Landsberg et al., 1999; McNaughton & Sabuni, 1988; Noy-Meir et
al., 1989; Sala et al., 1986). A negative relationship between
herbivory, leaf area and plant height may also be due to increased light
availability in grazed areas, potentially reducing the need for plants
to grow tall to access the light (Borer et al., 2014).
VOCs were mostly examined in relation to invertebrate herbivory and
responded mostly positively, with only a handful of studies reporting a
negative relationship with herbivory (Figure 6). This suggests that VOCs
are mostly expressed or up regulated in response to herbivory. VOCs may
also increase in response to a variety of other stimuli (Vivaldo et al.,
2017) and play an important role in plant-plant and cross-trophic
signalling (Baldwin et al., 2002; Mäntylä et al., 2008). Kigathi et al.
(2009) who found the expression of some VOCs to decrease with
invertebrate herbivory in the field, suggest that under field conditions
the plant is responding to multiple stimuli at once and this may also
affect the type and abundance of VOC emissions. They also highlight that
reduced VOC production in response to herbivory may be due to the
allocation of carbon and nitrogen being prioritised for growth or for
production of others defensive compounds over VOCs.
Where a significant response was found, leaf nitrogen was usually
positively correlated with invertebrate herbivory, while leaf carbon to
nitrogen ratio was usually negatively correlated (Figure 6). Similar to
the response to vertebrate herbivory this result suggests that for these
plant species, herbivory potentially results in a greater investment in
growth over carbon-based defence as indicated by higher leaf nitrogen
for every part carbon. Because many invertebrate focussed studies
compared leaf traits from leaves with and without visual evidence of
herbivory, greater nitrogen in grazed leaves may reflect herbivore
preference for leaves with higher nitrogen, rather than the leaf
increasing nitrogen in response to herbivory (Loranger et al., 2012).
Aboveground biomass (measured for individual species) responded mostly
negatively, but also showed little evidence of a change with
invertebrate herbivory. The non-significant responses mostly came from
one paper however (Ladygina et al., 2010) which looked at the effect of
belowground herbivores (nematodes and wire worms) on aboveground
biomass. Because aboveground biomass was not being directly removed via
herbivory the effect of herbivory may be more nuanced. Aboveground
biomass was also mostly negatively associated with vertebrate herbivory.
One study was the exception, finding perennial forb biomass was higher
in deer grazed pastures in comparison to ungrazed exclosures, likely due
to reduced competition from grass species (Paige, 1992). In fact, in
some grasslands the abundance and richness of forbs is thought to
dependent on niche construction by large herbivores, due to the legacy
of large and mostly extinct vertebrates, such as mammoths (Bråthen et
al., 2021). This points to an important distinction between direct
herbivore effects and indirect herbivore effects on plant traits.
Phenols are often attributed to herbivore defence and are usually
hypothesised to increase in response to herbivory (Salminen & Karonen,
2011). Phenols are an extremely diverse group of compounds, however, and
play several other roles in plant metabolism (Salminen & Karonen,
2011). The production of phenols is also reliant on adequate
photosynthetic capacity to allow for the accumulation of carbon
molecules (Frier et al., 2012). Total phenols responded mostly
positively to vertebrate and invertebrate herbivory, although one study
found phenols to decline in response to herbivory across multiple sites
(Knappová et al., 2018) (Figure 6). Reported high rates of folivory in
this study may have compromised the photosynthetic capacity of plants
and limited phenol production (Knappová et al., 2018).
Leaf silica was relatively frequently measured (31 measures) in response
to both vertebrate and invertebrate herbivory and where a significant
effect was found was mostly positively associated with herbivory (Figure
6). Most studies examining the response of silica were on grass species,
which are known for their relatively high silica content in comparison
to forbs and their ability to accumulate silica in response to
herbivory, but also in response to increases in soil silica content
(Hall et al., 2019). Within the studies from this review, silica
responded positively to herbivory in eight different grass species
(Appendix B). One study from the tundra grasslands in Norway, found that
for some grass species, silica content declined with summer reindeer
herbivory (Petit Bon et al., 2022). Here they suggest that silica
accumulates with age in these grass species, and perhaps herbivory is
keeping the phenological age of the leaves young and thus maintaining
lower leaf silica levels than un-grazed plants (Bañuelos & Obeso,
2000). Understanding how plant defence traits change with stages in
plant phenology is an interesting area of future research and may help
to untangle variable responses of plant traits to herbivory.