Floral volatiles evoke partially similar responses in both florivores and pollinators and are correlated with non-volatile reward chemicals

Abstract

Background: Plants use floral displays to attract mutualists, but simultaneously need to prevent attacks by antagonists. Chemical displays detectable from a distance include attractive or repellent floral volatile organic compounds (FVOCs). Post-landing, visitors perceive contact chemicals including nutrients, but also deterrent or toxic constituents in pollen and nectar, protecting flowers from overexploitation. The composition of FVOCs and pollen chemistry is well known to vary among and within species. However, we lack knowledge about differences and similarities in the detectability of and behavioural responses towards these compounds for insect flower visitor groups of key importance, i.e., mutualistic pollinators versus antagonistic florivores, as well as the correlation between FVOCs and pollen chemodiversity. Scope: We reviewed how FVOCs and non-volatile floral chemical displays, i.e., nutrients and toxins of pollen, vary in composition and how they affect the detection and behaviour of insect flower visitors. Moreover, we used a meta-analytic approach to evaluate the detection of and responses towards FVOCs by pollinators vs. florivores within the same plant genera. Furthermore, we tested whether the chemodiversity of FVOCs as well as nutrients and toxins stored in pollen are correlated and hence informative about each other. Key Results: According to the available data, florivores are more likely to detect FVOCs than pollinators. Common FVOCs such as linalool and methyl salicylate were often reported as attractive to pollinators and repellent towards florivores. A higher number of FVOCs was found to be attractive to both mutualists and antagonists compared to shared repellent compounds. Furthermore, a negative correlation between FVOC richness and the number of pollen toxin classes was revealed, besides a trend towards a positive correlation between pollen protein amount and the number of pollen toxins. Conclusions: Plants face critical trade-offs when producing floral chemicals, as these partly mediate the same information, particularly attraction but also repellence or toxicity, to both mutualists and antagonists. Moreover, chemodiversity of different floral parts is partly correlated and thus highly relevant for investigations of flower-insect interactions. Further research is needed on more different wild and cultivated plant species and mutualistic and antagonistic interaction partners to test for generalisation of these patterns.

Chemodiversity in flowers of Tanacetum vulgare has consequences on a florivorous beetle

“…2019; Rivest & Forrest 2020; Sasidharan et al . 2023). Terpenoids are probably not produced in the pollen but biosynthesized and stored within other floral tissues, such as anther glands (Goodger et al .…”

“…Across different plant species, volatile richness can be linked overall to low toxicity in the pollen or to high nutrient content (Sasidharan et al . 2023). These traits could also be important in attracting florivores by allowing detection of more olfactory cues from foods, such as pollen.…”

“…However, floral herbivores, known as florivores, also exploit these volatiles to find host plants (Junker & Blüthgen 2010; Schiestl 2010; Knauer & Schiestl 2015; Sasidharan et al . 2023). Terpenoids represent a major class of specialized metabolites that are very diverse in structure and occur in different plant parts, including flowers (Abbas et al .…”

“…2019; Rivest & Forrest 2020; Sasidharan et al . 2023). For example, a glucosinolate and saponins deter feeding of the pollen beetle Brassicogethes aeneus (Coleoptera: Nitidulidae) on oilseed rape (Austel et al .…”

“…The nutrient content in pollen may be correlated with its specialized metabolite diversity (Sasidharan et al . 2023), but differences in nutrient composition among plants of different chemotypes have rarely been investigated (Eilers et al . 2021).…”