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

Abstract

Background Plants often use floral displays to attract mutualists and prevent antagonist attacks. Chemical displays detectable from a distance include attractive or repellent floral volatile organic compounds (FVOCs). Locally, visitors perceive contact chemicals including nutrients but also deterrent or toxic constituents of pollen and nectar. FVOC and pollen chemical composition may vary intra- and interspecifically. For certain pollinator and florivore species, responses towards these compounds are studied in specific plant systems; yet we lack a synthesis of general patterns comparing these two groups and insights into potential correlations between FVOC and pollen chemodiversity. Scope We reviewed how FVOCs and non-volatile floral chemical displays, i.e., pollen nutrients and toxins, vary in composition and affect the detection and behaviour of insect visitors. Moreover, we used meta-analyses to evaluate the detection of and responses towards FVOCs by pollinators vs. florivores within the same plant genera. We also tested whether the chemodiversity of FVOCs, pollen nutrients and toxins are correlated and hence mutually informative. Key Results According to available data, florivores could detect more FVOCs than pollinators. Frequently tested FVOCs were often reported as pollinator-attractive and florivore-repellent. Among FVOCs tested on both visitor groups, there were a higher number of attractive than repellent compounds. FVOC and pollen toxin richness correlated negatively, indicating trade-offs, while a marginal positive correlation between pollen protein amount and toxin richness was observed. Conclusions Plants face critical trade-offs, as floral chemicals mediate similar information to both mutualists and antagonists, particularly through attractive, and fewer repellent, FVOCs. Furthermore, florivores may detect more FVOCs, whose richness is correlated to reward chemical richness. FVOC chemodiversity is potentially informative of reward traits. To better understand the ecological processes shaping floral chemical displays, more research is needed on floral antagonists of diverse plant species, and on the role of floral chemodiversity towards visitor responses.

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

“…In contrast, the BThu chemotype had the highest chemical terpenoid richness in both flower heads and pollen. Pollen is known to contain specialized metabolites, but the diversity and concentration compared to other floral and vegetative tissues is not well explored (Palmer-Young et al 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 2021) or glandular trichomes (Ferreira & Janick 1995).…”

“…Flowers with higher richness, together with lower or intermediate Renyi diversity, as found in the BThu chemotype, might in fact be preferred by some flower visitors. 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.…”

“…Ideally, volatile plant metabolites should attract pollinators from a distance, while repelling antagonists, such as herbivores (Theis & Lerdau 2003;Strauss & Whittall 2006). However, floral herbivores, known as florivores, also exploit these volatiles to find host plants (Junker & Bl€ uthgen 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 2017;Zhou & Pichersky 2020).…”

“…Likewise, different sugars, such as fructose, glucose, sucrose, and isorhamnetin rhamnoglycoside, act as phagostimulants for this florivore (Kim & Mullin 2007). However, plants also incorporate deterrent or toxic compounds, including terpenoids, in these tissues to defend against over-exploitation by pollinators or florivores (Palmer-Young 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 2021).…”

“…For example, a glucosinolate and saponins deter feeding of the pollen beetle Brassicogethes aeneus (Coleoptera: Nitidulidae) on oilseed rape (Austel et al 2021). 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). The selection of a suitable host plant is also critical for the survival of florivores.…”