Climate warming and plant biomechanical defences: Silicon addition contributes to herbivore suppression in a pasture grass

Abstract

Plants, notably the Poaceae, often accumulate large amounts of silicon (Si) from the soil. Si has multiple functional roles, particularly for alleviating abiotic and biotic stresses (e.g., defence against herbivores). Recent evidence suggests that environmental change, including temperature changes, can diminish Si accumulation which could affect functions such as herbivore defence. Using a field warming experiment, we grew a pasture grass (Phalaris aquatica) that was either supplemented or untreated with Si (+Si and −Si, respectively) under ambient and elevated (+2.8°C above ambient) air temperatures. We quantified soil water, plant growth rates, Si accumulation, leaf biomechanical properties and in situ relative growth rates of a herbivorous global insect pest (Helicoverpa armigera). Si supplementation promoted shoot and root biomass by c. 48% and 61%, respectively under ambient temperatures, but these gains were not apparent under warmed conditions. Warmer temperatures reduced Si uptake by −Si plants by c. 17%, potentially due to the lower levels of soil water content in warmed plots. Si supplementation, however, increased Si accumulation in leaves by c. 24% in warmed plots restoring Si levels to those seen under ambient temperatures. Si supplementation enhanced biomechanical properties in the leaves, but this was only statistically significant under ambient temperatures; leaves of +Si plants required 42% more force to fracture and were 30% tougher at the midrib than leaves of −Si plants. The relative growth rates of H. armigera declined by 56% when feeding on +Si plants under ambient temperatures, and while Si supplementation caused a trend towards declining herbivore growth rates under warmer conditions, this was not statistically significant. We conclude that climate warming may mitigate the beneficial effects of Si on Phalaris aquatica in the short term, potentially by reducing Si uptake. While Si uptake can be restored with Si supplementation, Si‐enhanced biomechanical defences against a global pest may not be fully restored under warmer temperatures. A plain language summary is available for this article.

Elevated atmospheric CO2 suppresses jasmonate and silicon‐based defences without affecting herbivores

“…In the current study we found significant negative effects of Si on herbivory (Figure 4), supporting the strong anti‐herbivory effects of Si found in previous work (Frew et al, 2016; Johnson et al, 2019; Massey & Hartley, 2009). Silicon is generally considered a mechanical defence mechanism, as Si is deposited in the leaves as solid SiO 2 phytoliths, causing abrasion of herbivore mouthparts and general decreased palatability of leaf material (Hartley, Fitt, McLarnon, & Wade, 2015; Massey & Hartley, 2009).…”

“…The consistently lower endogenous JA seen in stressed Si‐treated plants (Figure 3A) suggests that some species, when supplemented with Si, may actually be more susceptible to herbivory, particularly if the species relies more on JA‐induced chemical defences rather than Si uptake. In B. distachyon and other grasses, however, the hyper‐accumulation of Si appears to provide a significant defence against herbivory, potentially compensating for any reduction in other JA‐induced defences (Frew et al, 2017; Johnson et al, 2019; Ryalls et al, 2017).…”

“…Many grass species accumulate high amounts of silicon, averaging 1.5% of dry weight, however, some species can accumulate upwards of 10% (Epstein, 1994; Hodson, White, Mead, & Broadley, 2005). Silicon uptake has been shown to benefit plants under various stress conditions, including drought, salinity, heavy metals (Debona, Rodrigues, & Datnoff, 2017; Liang, Sun, Zhu, & Christie, 2007), pathogens (Fauteux, Chain, Belzile, Menzies, & Bélanger, 2006) and herbivory (Hartley & DeGabriel, 2016; Johnson et al, 2019; Ye et al, 2013). In particular, silicon has a negative effect on insect herbivory through the accumulation of solid silica particles in the plant (phytoliths) which act as a physical defence (Massey & Hartley, 2009).…”

“…In particular, silicon has a negative effect on insect herbivory through the accumulation of solid silica particles in the plant (phytoliths) which act as a physical defence (Massey & Hartley, 2009). Silicon incorporated into leaf tissue increases leaf toughness and force to fracture (Johnson et al, 2019). This mechanical defence provided by Si in plant tissues can contribute to the wear of insect mandibles and reduces nutrient availability and the efficiency of digestion (Hunt, Dean, Webster, Johnson, & Ennos, 2008; Massey & Hartley, 2009).…”

Association of leaf silicon content with chronic wind exposure across and within herbaceous plant species

“…Silicon in plants has been found to provide resistance to many adverse biotic and/or abiotic environmental conditions, including, for example, nutrient deficiency, drought and toxic metal stress, pathogen intrusion, antiherbivory and mechanical stress (Cooke & Leishman, ; Coskun et al, ; Frew, Weston, Reynolds, & Gurr, ; Guntzer, Keller, & Meunier, ; Strömberg et al, ). The common view has been that the main function of foliar Si accretions in solid form (e.g., phytoliths) is to protect plant tissues from herbivory (Cooke et al, ; Epstein, ; Hartley & DeGabriel, ; Hartley, Fitt, McLarnon, & Wade, ), especially from being eaten by (mostly mammalian) vertebrates (Massey & Hartley, ; Massey, Massey, Ennos, & Hartley, ; Strömberg et al, ; Teaford, Lucas, Ungar, & Glander, ; Wieczorek, Zub, Szafrańska, Książek, & Konarzewski, ) or invertebrates (Garbuzov, Reidinger, & Hartley, ; Hunt, Dean, Webster, Johnson, & Ennos, ; Johnson et al, ; Massey & Hartley, ; Reynolds, Keeping, & Meyer, ; Ryalls, Hartley, & Johnson, ; Soininen, Bråthen, Jusdado, Reidinger, & Hartley, ), and to act as a potentially cheap alternative to cellulose or lignin (Cooke & Leishman, ; Raven, ; Schoelynck et al, ). Silicon is even thought to have played a central role in the co‐evolution of grasses and their mammalian grazers, which had to evolve teeth that could withstand chronic erosion by foliar phytoliths, although this role is still under active debate (Calandra, Zub, Szafrańska, Zalewski, & Merceron, ; Hartley & DeGabriel, ; Strömberg et al, ).…”