Temperature alters the toxicological impacts of plant terpenoids on the polyphagous model herbivore Vanessa cardui

Abstract

Terpenes are a major class of secondary metabolites present in all plants, and long hypothesized to have diversified in response to specific plant-herbivore interactions. Herbivory is a major biotic interaction that plays out across broad temporal and spatial scales that vary dramatically in temperature regimes, both due to climatic variation across geographic locations as well as the effect of seasonality. In addition, there is an emerging understanding that global climate change will continue to alter the temperature regimes of nearly every habitat on Earth over the coming centuries. Regardless of source, variation in temperature may influence herbivory, in particular via changes in the efficacy and impacts of plant defensive chemistry. This study aims to characterize temperature-driven variation in toxicological effects across several structural classes of terpenes in the model herbivore Vanessa cardui, the painted lady butterfly. We observed a general increase in monoterpene toxicity to larvae, pupa, and adults at higher temperatures, as well as an increase in development time as terpene concentration increased. Results obtained from this study yield insights into possible drivers of seasonal variation in plant terpene production as well as inform effects of rising global temperatures on plant-insect interactions. In the context of other known effects of climate change on plant-herbivore interactions like carbon fertilization and compensatory feeding, temperature-driven changes in plant chemical defense efficacy may further complicate the prediction of climate change impacts on the fundamental ecological process of herbivory.

Keywords: Herbivory; Insect development; LC50; Lepidoptera; Plant defense.

Fig. 1

Concentration-response curves of adult mortality at 24°C, 27°C, and 30°C with V. cardui subject to varying concentrations of A) limonene, B) linalool, C) cineole, and D) beta-caryophyllene as prepared at the start of each trial. Shaded regions correspond to 95% confidence intervals around each curve. Individual points represent the proportion of adult mortality observed across replicate insects within each concentration for each trial. See Data S1 for full data

Fig. 2

Concentration versus days to pupation at 24°C, 27°C, and 30°C with V. cardui subject to varying concentrations of A) limonene, B) linalool, C) cineole, and D) beta-caryophyllene as prepared at the start of each trial. Shaded regions correspond to 95% confidence intervals around each curve. Individual points represent the time to pupation observed for each insect that reached pupation within each trial. See Data S2 for full data

Fig. 3

Broader implications of temperature-dependent terpene toxicity under climate change should the results observed for the polyphagous Vanessa cardui in this study (red text) hold for other herbivorous insects. Increased temperatures and atmospheric carbon dioxide concentrations observed under climate change are predicted to have multiple cascading effects on both plants and herbivorous insects. For plants, the increase in growing degree days [1], lengthened growing seasons [2], and the carbon fertilization effect [3] have been demonstrated to result in increased leaf C:N and C:P ratios [4] and increased carbon-based plant defenses [5]. In addition, where other factors like water and nutrient availability are not limiting (*), faster plant growth per unit time [6] is expected to result in increased plant biomass production [7]. For insects, the increase in metabolic rate with increased temperature [8] and the lengthening of active seasons [9] have been demonstrated to result in faster individual development [10] as observed in this study, as well as an increase in the number of generations per year [11], including shifts from univoltine to multivoltine life history in a given geographic region. Where other factors do not limit insect population growth (*), faster development and shorter generation time are expected to result in short-term increases in population size [12], such as within a single growing season. Larger populations of organisms are known to be more able to respond to natural selection [13]. The interactions between plant and insect responses are expected to have multiple effects that influence both the magnitude of herbivory and anti-herbivore plant traits. For insects, the phenomenon of compensatory feeding [14] due to lower leaf nutrient content combined with higher herbivore population sizes [15] would be expected to result in an increase in herbivory pressure on plants. This could be further heightened if hatching rates are higher due to reduced egg stage terpene toxicity as observed in this study, regardless of whether larvae survive to reproduction. For plants, lower nutritional content per unit leaf mass has been demonstrated to reduce herbivore survival and development [16], as have higher concentrations of carbon-based defenses (like terpenes) per unit leaf mass [17]. If the potency of these defenses (toxicity of a given concentration) is also increased by temperature as observed in this study, this will act as a multiplier of the efficacy of plant chemical defense investment. An increase in the magnitude or duration of herbivore pressure would be expected to induce additional production of chemical defenses [18], which may increase concentrations further. Additionally, to the extent that plant growth rate may increase (*) due to the factors described above, this would be expected to increase plant herbivory tolerance through the regrowth of lost or damaged plant parts [19]. Overall, these many individual effects suggest a potential intensification of the plant-herbivore interaction under climate change. References: [1+2] Park et al. ; Kukal and Irmak ; Matthews et al. ; Piao et al. ; [3] McGrath and Lobell ; Liang et al. ; Terrer et al. ; Ueyama et al. ; [4] Lincoln et al. ; Bezemer and Jones ; Gifford et al. ; Stiling and Cornelissen ; Sardans et al. ; Wang et al. ; [5+17] Filella et al. ; Helmig et al. ; Bidart-Bouzat and Imeh-Nathaniel ; Ibrahim et al. ; Cornelissen ; [6+7] Gray and Brady ; Park et al. ; Kukal and Irmak ; Piao et al. ; Babst et al. ; Ueyama et al. ; [8+9] Cayton et al. ; Deutsch et al. ; Jactel et al. ; Forrest ; [10] Colinet et al. ; Buckley et al. ; Rebaudo and Rabhi ; Harvey et al. ; [11] Tobin et al. ; Altermatt ; Ziter et al. ; Forrest ; [12+15] Colinet et al. ; Ziska and McConnell ; Tonnang et al. ; Harvey et al. ; Wagner et al. ; Schneider et al. ; [13] Lande ; Debarre and Gandon ; Gravel ; Jensen et al. ; but see Wood et al. ; [14+16] Fajer et al. ; Stiling and Cornelissen ; Trebicki et al. ; Hamann et al. ; [18] Agrawal ; Agrawal et al. ; Underwood ; Copolovici et al. ; [19] Tiffin ; Fornoni ; Gray and Brady .