3.3) What plant traits are measured in vertebrate and
invertebrate focussed studies?
Across all studies, 209 unique plant traits were measured. Of these 209,
115 were unique to vertebrate focussed studies, 50 unique to
invertebrate focussed studies. Of these traits, 44 were measured
commonly across vertebrate and invertebrate studies (Appendix C). Leaf
traits were the most frequently measured (115), but stem (34), whole
plant (24), root (16), flower/fruit (13) and seed traits (7) were also
measured.
Key areas of difference were between the proportion of biochemical and
morphological traits examined, with the former a greater focus in
invertebrate, and the later, in vertebrate studies (Figure 5). This
difference in traits studied between vertebrate and invertebrate studies
may be due to the scale at which these two herbivore guilds operate,
explained largely by differences in body size (Kotanen & Rosenthal,
2000a). Due to their greater capacity for defoliation at larger scales,
vertebrates can influence plant morphology readily (e.g., plant height
or biomass) and thus plants are potentially more likely to change their
morphology in response to herbivory. In contrast, invertebrate herbivory
usually occurs over relatively longer time periods (e.g., a caterpillar
feeds on one leaf longer than a cow), at smaller scales and targeted to
specific tissues (Hulme, 1996; Oduor et al., 2010). This may allow the
plant more time to distribute re-mobilise nutrients and induce a
biochemical defence against herbivores, for example using VOCs (Ameye et
al., 2018) or other secondary metabolites. Nevertheless, there are some
instances where insects can have huge impacts on plant morphological
traits, such as biomass. One example are migratory insects (e.g.,
grasshoppers) that can reach high densities and in regard to extent of
consumption, act like vertebrate herbivores (Tscharntke & Greiler,
1995). Many vertebrate studies were also conducted over several years
(Appendix A) and are therefore more likely to capture changes to plant
morphology than invertebrate focussed studies, which were mostly
conducted within a month or less.
Physiological traits, such as photosynthetic capacity and water use
efficiency were only examined in relation to vertebrate herbivory
(Figure 5). This is perhaps surprising as invertebrate impact on plant
physiology has been relatively well-studied for crops (Nabity et al.,
2008; Peterson et al., 1998; Thomson et al., 2003; Velikova et al.,
2010), and findings have shown invertebrate herbivory to be both
negatively and positively associated with photosynthetic rate.
Similarly, across all studies only one phenological trait, flowering
onset, was examined and only in four vertebrate focussed studies. This
may reflect constraints within research budgets and priorities as
phenological research generally requires experiments to run over several
years, for which funding is generally limited (Hughes et al., 2017;
Lindenmayer et al., 2012). The lack of focus on plant phenological
responses to herbivory in grasslands is concerning as phenological
patterns can influence regeneration capacity (Rawal et al., 2015),
community composition (Lavorel & Garnier, 2002), and adaptation across
trophic levels (Bagella et al., 2013; Wray & Elle, 2015). For example,
research in the alpine rocky ecosystems in Colorado found herbivory by
mule deer delayed flowering phenology in a perennial herb which
consequentially reduced invertebrate seed predation and overall
increased plant fitness (Freeman et al., 2003). Understanding how plant
phenology and herbivory interact with climate is also an important area
of future research, particularly under uncertain climatic conditions
(Hamann et al., 2021; Lemoine et al., 2017). With advances in remote
sensing technologies, studies on plant phenological studies are now
easier and cheaper to perform and we see these technologies already
starting to be used to answer other phenological questions (Dronova &
Taddeo, 2022).
At the individual trait level and ignoring additional responses from
multiple species or sites examined within studies, the five most common
traits assessed in vertebrate focussed studies were specific leaf area
(SLA), plant height, leaf nitrogen, LDMC and leaf area (descending order
of use; Figure 4; Table 2). For invertebrate focused studies the most
common traits were VOCs, SLA, aboveground plant biomass, LDMC and leaf
nitrogen (Figure 4, Table 2). Specific leaf area, LDMC and leaf nitrogen
were common focal traits across both vertebrate and invertebrate
studies. These traits are often referred to as ‘soft’ traits as they are
relatively easy to measure and have been found to correlate with traits
which are harder to measure such as relative growth rate (Hodgson et
al., 1999; Perez-Harguindeguy et al., 2016). These ‘soft’ traits also
represent important components of the leaf economic spectrum (Hodgson et
al., 1999; Wright et al., 2004) and inform us about the plant’s
individual response to abiotic and biotic factors, and in the context of
herbivory can inform us about the species ability to tolerate or avoid
herbivory.
The study of VOCs was a key point of difference between vertebrate and
invertebrate focussed studies, with eight studies examining VOCs in
relation to invertebrate herbivory and only one in relation to
vertebrate herbivory (Zhang et al., 2014). Analysis of VOCs is usually
done via dynamic headspace sampling (Chen et al., 2003) under
laboratory-controlled conditions, which may limit its capacity for use
on vertebrate herbivores. Zhang et al. 2014 however used this system to
first identify and isolate the VOCs released from grass speciesArtesmia fridgida and then apply these VOCs to control plants
during a selection experiment with domestic sheep. Some studies have
also successfully employed the head-space sampling system in a field
setting to examine VOC production from grass leaves with high and low
levels of invertebrate herbivory (see Kigathi et.al. 2009). It may be
possible to use a similar strategy to examine VOC production in response
to vertebrate herbivory. In response to invertebrate herbivory, VOC
production can act as a signal to attract vertebrate and invertebrate
predators (Kessler & Baldwin, 2001; Mäntylä et al., 2008) and to
communicate the potential for herbivore attack to neighbouring plants
(Baldwin et al., 2002). In other studies, not reviewed here, vertebrates
have been shown to use plant VOCs to find food and increase feeding
efficacy (Bedoya-Pérez et al., 2014; Stutz et al., 2016). Overall, the
influence of VOCs were mostly studied in relation to invertebrates and
expanding this research to further examine their response to, and effect
on vertebrate herbivory would be an interesting avenue for future
exploration.
The huge diversity and high proportion (61%) of traits examined from a
single study was in part due to traits being generally characteristic to
particular plant families or functional groups, such as rhizome length
(Amiaud et al., 2007), woody density of shrubs and woody forbs within
grasslands (Whitworth-Hulse et al., 2016), thorns (Woodward & Coppock,
1995) or latex (Rasmann et al., 2009). Some studies researched unique
aspects of plant-herbivore interactions. For example, Ribeiro et al.
(2017) examined the influence of metals and micronutrients on
invertebrate herbivore selection and this study accounted for 31 (15 %)
of the single study traits. They found most metals examined did not
affect invertebrate selection, although aluminium, iron, magnesium,
manganese, and total leaf metals were found to have a negative effect on
herbivore selection. Other studies examined specific morphological
attributes, such as leaf symmetry or grass blade width, or specific
anatomical aspects of a plant, such as spine angle. For example, Santos
et al. (2013) found herbivory by gall midge was negatively correlated
with leaf symmetry in the plant Bauhinia brevipes . They also
found less symmetric leaves had lower leaf nitrogen, which is thought to
be favourable for gall development. These results reveal interesting
relationships between morphological and biochemical traits and their
interaction with herbivores.
Using a common list of traits across research groups exploring
plant-trait herbivore interactions would help to standardise trait
measurements and improve comparability across studies and this has been
flagged in previous reviews on the topic (Diaz et al., 2007) but at the
same time, researchers should remain open to new emerging plant traits
as technologies advance and our understandings improve. Shortlists of
traits that should be favoured or disfavoured by herbivory have been
identified (Coley et al., 1985; Weiher et al., 1999). Although these are
mostly focussed on vertebrate herbivory, used alongside results from
this review, a list of potential focal plant traits which are relevant
to both vertebrate and invertebrate herbivores can be determined.