Climate Change Alters the Chemical Arms Race Between Flowers and Butterflies

A recent study by Mari Irving and colleagues published in the Journal of Chemical Ecology sheds new light on how diet impacts painted lady butterflies. These familiar butterflies, with their orange and black-patterned wings, are a common sight in gardens worldwide. The study, conducted by researchers at the University of Central Florida, focused on understanding how the diverse flower species that painted ladies feed on affect their survival and development.

Painted ladies (Vanessa cardui) have an extraordinarily broad diet, feeding on flowers from over ten different plant families. This generalist feeding strategy allows them to thrive in a wide range of habitats. However, little research to date has examined how the specific chemicals produced by their host plants impact painted ladies at different life stages. The flowers they visit contain diverse compounds, including terpenes, which give many plants their distinctive scents. This new study set out to determine how common terpenes found in floral nectar and pollen influence painted lady caterpillars, pupae, and adults.

Examining the Impact of Floral Terpenes

Terpenes are an important class of chemical compounds that plants produce for various reasons. These diverse compounds, found in the essential oils of many flowers, trees, and herbs, serve critical roles in plant defence against pests and diseases. Terpenes also give flowers their distinctive scents, which serve to attract pollinators. The mixture of terpenes produced by a plant contributes to its unique aroma.

Given their importance in plant defence and pollinator interactions, the researchers wanted to see how terpenes impact painted lady butterflies that feed on floral nectar and pollen. They focused on four common floral terpenes: limonene, linalool, cineole, and beta-caryophyllene. Limonene provides a fresh, citrusy aroma. Linalool has a pleasant, floral scent found in lavender. Cineole has a medicinal, camphor-like smell and is a major component of eucalyptus oil. Beta-caryophyllene lends a woody, spicy fragrance. By testing this diverse set of terpenes, the researchers aimed to understand how they influence painted lady growth and survival.

Investigating Terpene Impacts Through Controlled Feeding Experiments

The researchers conducted carefully controlled feeding experiments to understand how terpenes affect painted ladies. They fed painted lady caterpillars artificial diets spiked with varying levels of the four terpenes – limonene, linalool, cineole, and beta-caryophyllene. The diets contained different concentrations of each terpene, ranging from none up to toxic levels.

Irving and colleagues conducted the experiments at three different temperatures: 24°C, 27°C, and 30°C. This variation allowed the researchers to see if temperature impacted the effects of the terpenes. After feeding the caterpillars the terpene diets, the researchers measured several effects:

• Hatching rates of the eggs
• Caterpillar survival
• Time needed for development
• Size of the adult painted lady butterflies

By systematically testing diets with different terpene levels and temperatures, the researchers could pinpoint how these floral compounds influence painted ladies at various life stages.

Terpenes Reduced Survival and Slowed Development, But Did Not Shrink Adult Size

The feeding experiments revealed several ways that terpenes impacted painted ladies. Terpenes prevented many eggs from hatching, with stronger effects observed at cooler temperatures of 24°C compared to higher temperatures. The three monoterpenes (limonene, linalool, and cineole) were most effective at inhibiting egg hatching.

Additionally, caterpillars and pupae died more frequently when fed diets containing higher levels of terpenes. As with egg hatching, the monoterpenes displayed the greatest toxicity, causing dose-dependent increases in mortality through the larval and pupal stages.

Interestingly, the researchers found that death rates increased at higher temperatures for some terpenes, like linalool. This result suggests that terpene toxicity can be enhanced with heat.

Beyond survival, terpenes also slowed down painted lady development. Caterpillars took longer to form pupae when eating more highly concentrated diets. The monoterpenes limonene, linalool and cineole exhibited this developmental delaying effect.

Despite the negative impacts of terpenes on survival and growth rate, the scientists found that the size of adult painted lady butterflies was unaffected by the terpene content of their larval diets. Adult mass only varied within about a two-fold range regardless of whether caterpillars consumed high or low levels of the compounds. This result indicates that while terpenes reduce juvenile survival, if painted ladies can successfully emerge from the pupal stage, they can develop into normal-sized adults.

Implications for Plant-Insect Interactions

The results reveal that the painted lady diet has varying effects depending on the life stage. While terpenes strongly inhibited egg hatching, if larvae successfully fed on terpene-containing diets, they could develop into normal-sized adults, though at the cost of slower development and higher mortality. This differential impact highlights how painted lady susceptibility to plant chemical defences is highly context-dependent, driven by factors like life stage, temperature, and the specific terpenes present in their floral diet.

Temperature also seems to play an important role in determining terpene toxicity. The findings help explain why plants may produce different defensive chemicals under hot versus cool conditions – their efficacy changes with temperature. For instance, all three monoterpenes were less toxic to painted lady larvae and pupae at lower temperatures. As global temperatures rise, this phenomenon may have a notable impact on painted ladies.

More broadly, this research provides insights into the complex dynamics between plants and insect herbivores. It shows how factors like wild plants and crops diverge. Irving and colleagues write:

Overall, these many individual effects suggest a potential intensification of the plant-herbivore interaction under climate change. Larger populations of faster-developing insects consume larger amounts of plant tissue, while faster growing plants produce higher quantities of lower-nutrient biomass defended with higher concentrations of more effective carbon-based chemical defenses. While plants might be expected to prevail under such conditions, if large populations of insects are subjected to diets where individuals must ingest larger quantities of more-toxic chemical defenses to meet their minimum nutritional needs, that would constitute a strong selective force for the evolution of resistance to those chemical defenses.

Irving et al. 2023.

The problem with this, the authors say, is that while wild plants will adapt, domesticated plants do not evolve; they’re selected. So, crops may become much more attractive to terpene-resistant pests. Temperature changes, particularly swings in temperature in increasing extreme seasons, will also affect plant chemical defences against herbivores. Both changes in temperature and time will have to be factored into future models of pest control.

READ THE ARTICLE
Irving, M.R., Goolsby, E.W., Stanford, H., Lim-Hing, S., Urrea, M. and Mason, C.M. (2023) “Temperature alters the toxicological impacts of plant terpenoids on the polyphagous model herbivore Vanessa cardui,” Journal of Chemical Ecology. Available at: https://doi.org/10.1007/s10886-023-01449-8.

Cover: Vanessa cardui. Image: Canva.