Introduction
Plant-herbivore interactions link primary production and food webs. They
are the catalyst for the transfer of energy/nutrients between trophic
levels and the abiotic environment and are crucial to the shaping of
community dynamics and ecosystem function. Due to their fundamental role
in the web of life, plant-herbivore interactions have been the focus of
many fields of research, including ecology (such as, Risch et al.,
2018), evolution (such as, Johnson et al., 2015; Maron et al., 2019),
entomology (such as, Roohigohar et al., 2022; Zalucki et al., 2001) and
agriculture (such as, Christensen et al., 2013; Wari et al., 2019).
Questions range from fundamental knowledge building (Ramsey & Wilson,
1997) and practical understanding, such as learning how to produce crops
or meat more efficiently, to testing and developing ecological theory,
such as understanding the role plant/herbivore interactions play in
ecosystem coupling and stability (Risch et al., 2018).
Because of the complexity of plant-herbivore interactions, it is easy
for knowledge silos to form within respective fields of expertise and
investigation—where for example, a plant ecologist may experiment in
different ways to an entomologist. A potential silo, perhaps easily
conceived, is that which develops between different herbivore guilds,
and specifically between vertebrate and invertebrate herbivores (Peisley
et al., 2015). Due to fundamental differences in their ecology and
evolution, these two broad taxonomic groups attract sometimes
contrasting interests, expertise and methodologies (Andrew et al.,
2022). This review aims to systematically investigate differences
between vertebrate and invertebrate focused research, specifically
regarding how herbivores respond to and affect plant traits.
Plant functional traits have been used as a ‘common currency’¾ to
collate, compare and contrast response and effect correlations in plants
within and between different ecosystems and species (Lavorel & Garnier,
2002; Suding et al., 2008). Functional traits also provide the
opportunity to discover generalities which arise out of complex
interactions between species within and across trophic levels (Carmona
et al., 2011; Lind et al., 2013). Further, using a common currency
correlated with function, lends well to exploring the influence of other
abiotic or biotic variables on traits and untangling their role in
modifying plant-herbivore interactions (Funk et al., 2017).
Plants employ a variety of traits to defend themselves against
herbivory. These can be morphological (e.g., spine length, see Göldel et
al., 2016), phenological (e.g., lifeform, see De Bello et al., 2005) and
physiological (e.g., photosynthetic capacity, see Shen et al., 2019),
and usually are associated with herbivore avoidance or herbivore
tolerance (Núñez-Farfán et al., 2007). For example, plants might avoid
herbivory by being small and short (Wakatsuki et al., 2021), expressing
secondary metabolites (Jones et al., 2003) or being covered in spines
(Coverdale et al., 2019). Plants which tolerate herbivory might have a
fast growth rate and efficient nutrient acquisition strategies to allow
them to quickly regain photosynthetic tissue after feeding (Briske et
al., 1996). In general, plants with functional traits on the
conservative end of the leaf economic spectrum (e.g., relatively smaller
specific leaf area, lower nitrogen content, a slower assimilation rate)
are more tolerant of herbivores than those on the resource acquisition
end of the spectrum (e.g., relatively higher specific leaf area, higher
nitrogen, fast growth rate). Herbivory, in addition to plant
productivity, can moderate the abundance of species within this spectrum
(Wright et al., 2004).
Plant traits can be constitutive, i.e., present throughout a plants
life, or can be induced, i.e., expressed when herbivory takes place
(Barton, 2016; Züst & Agrawal, 2017). An example of a constitutive
trait is the presence of plant spines. Traits such as this are expressed
all the time, although the degree of expression can vary with abiotic
and biotic factors, including herbivory (Hulshof et al., 2013). In this
way the expression of constitutive traits can also be induced. For
example, spine length (Young, 1987), or the expression of secondary
metabolites may increase (beyond their constitutive expression) in
response to herbivore attack (Huitu et al., 2014). Expression of induced
defence traits can occur immediately in response to herbivore attack,
such as the release of volatile organic compounds (VOCs), or over time,
such as the increased accumulation of carbon or silica within an
individual’s leaves. Plant traits also can either respond to or affect
their abiotic and biotic environment (Funk et al., 2017). In the context
of herbivory, response traits ‘respond’ to herbivore attack through an
induced response and effect traits can ‘affect’ herbivory by attracting
or deterring herbivores. The capacity for plant traits to change in
response to short- and long-term changes in herbivory and other
perturbations creates the foundations for adaptation and speciation to
occur over longer evolutionary timeframes (Ackerly et al., 2000).
Plants are most of the time exposed to different types of herbivores
simultaneously, and therefore may express a suite of traits also known
as a ‘defence syndrome’, to effectively defend against different types
of herbivory (Agrawal, Fishbein 2006; Moles et al. 2013). Vertebrate and
invertebrate herbivores for instance, vary in size, feeding strategy,
behaviour and ecology. Traits of the herbivores can then significantly
influence the type, duration and degree of damage experienced by the
plant and consequently the plants defence syndrome (Kotanen &
Rosenthal, 2000b). Thorns, for example, are relatively ineffective at
reducing herbivory from small invertebrates such as aphids, but function
well against large browsing animals, like ibex or deer (Crawley, 2019).
Similarly, some plant secondary metabolites might deter invertebrate
herbivory, but may be ineffective against most vertebrate herbivores
(Marsh et al., 2020; Salminen & Karonen, 2011). The type of herbivore,
as well as the research question and context, will therefore likely
influence the scientific lens researchers adopt and the traits chosen to
be measured when asking ‘How do plant traits respond to and affect
herbivory?’.
In this review, we aim to synthesise current evidence and understanding
of how plant traits respond to and affect (in terms of forage selection)
vertebrate and invertebrate herbivory. Further, we identify and discuss
any potential biases (i.e., taxonomic, geographic and climatic) and
knowledge gaps. We will focus our literature search on grasslands and
grassy woodlands. Grasslands cover ~30% of the Earth’s
terrestrial surface (White et al., 2000) and herbivores are crucial to
their functioning, diversity and evolution (Axelrod, 1985; McNaughton,
1984). Grasslands are also important to the provision of food for
people, (Habel et al., 2013; Simon et al., 2009) and are important for
maintaining global carbon and nutrient cycling (Scurlock & Hall, 1998).
Because of the pressures of human food production, many grasslands have
been extensively used and modified by humans and as a consequence the
persistence of many grassland species are under threat (Cousins &
Eriksson, 2008; Deák et al., 2020; Scholtz & Twidwell, 2022). To
conserve plants and animals within these important and widespread
ecosystems, we need to have a mechanistic understanding of the complex
functional relationships between plants and herbivores. By studying the
potentially disparate fields of vertebrate and invertebrate focused
studies, we aim to provide a more wholistic understanding of plant
trait-herbivore interactions in grasslands and highlight knowledge gaps
to guide future research.
We structured our review around the following three questions:
1. Are their geographic, taxonomic or climatic trends evident within
grassland plant trait-herbivore literature?
2. What plant traits are measured in vertebrate and invertebrate
herbivore focussed studies?
3. How do plant traits respond to and affect (in terms of forage
selection) vertebrate and invertebrate herbivory?