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?