Pollen and vegetative secondary chemistry of three pollen‐rewarding lupines

Abstract

Premise Optimal defense theory predicts that selection should drive plants to disproportionally allocate resources for herbivore defense to tissues with high fitness values. Because pollen's primary role is the transport of gametes, plants may be expected to defend it from herbivory. However, for many animal‐pollinated plants, pollen serves a secondary role as a pollinator reward. These dual roles may present a conflict between selection to defend pollen from herbivores and selection to reward pollinators. Here, we investigate whether pollen secondary chemistry in three pollen‐rewarding Lupinus species better reflects the need to defend pollen or reward pollinators. Methods Lupinus (Fabaceae) species are nectarless, pollen‐rewarding, and produce defensive quinolizidine and/or piperidine alkaloids throughout their tissues. We used gas chromatography to identify and quantitate the alkaloids in four aboveground tissues (pollen, flower, leaf, stem) of three western North American lupines, L. argenteus, L. bakeri, and L. sulphureus, and compared alkaloid concentrations and composition among tissues within individuals. Results In L. argenteus and L. sulphureus, pollen alkaloid concentrations were 11–35% of those found in other tissues. We detected no alkaloids in L. bakeri pollen, though they were present in other tissues. Alkaloid concentrations were not strongly correlated among tissues within individuals. We detected fewer alkaloids in pollen compared to other tissues, and pollen contained no unique alkaloids. Conclusions Our results are consistent with the hypothesis that, in these pollen‐rewarding species, pollen secondary chemistry may reflect the need to attract and reward pollinators more than the need to defend pollen from herbivory.

Pollen as the link between floral phenotype and fitness

“…When pollen is the primary reward, plants face the challenge of avoiding excessive pollen loss due to grooming while ensuring attractiveness to pollinators. In this issue, Heiling et al (2023) modeled pollen packaging strategies under the influence of these constraints, confirming the expectation that optimum package size depends on the relative preference of pollinators for larger packages, but also additional factors such as total pollen production in the population and possible relationships with per-plant visitation rates. The role of pollen as a reward in some species could be easily incorporated into fitness functions (Figure 1) by including links from pollen production (or daily presentation) to pollinator visitation.…”

Defence compounds in pollen: why do they occur and how do they affect the ecology and evolution of bees?

“…In fact, they observed that some species in which pollen is completely inaccessible to bees had high concentrations of pyrrolizidine alkaloids. In addition, Fabaceae flowers have pollen hidden inside keel petals where it is accessible only to pollinators that effectively pollinate the flowers (Dunn, 1956), but nevertheless some Fabaceae species contain sufficient defence compounds in their pollen to impair pollinator development (Arnold et al, 2014;Heiling et al, 2019), or have been shown to be poor pollen sources for bee larvae (Haider et al, 2014). Second, in orchids, pollen is packaged in structures called pollinia, making it impossible for pollinators to exploit pollen from this plant family (Johnson & Edwards, 2000).…”

“…In support of this idea, Kessler & Halitschke () observed that concentrations of chlorogenic acid and rutin (a flavonoid) were correlated between leaves and pollen across individuals of Solanum peruvianum . However, Heiling et al () found that alkaloid content in pollen of Lupinus spp. was generally not correlated with the alkaloid content of flowers and vegetative tissues.…”

“…Some pollens known to contain considerable amounts of defence compounds are readily collected by generalist bees, suggesting that bees are not deterred by natural concentrations of those compounds. For example, Lupinus spp., which only offer pollen as a reward, are primarily pollinated by large‐bodied bees (Dunn, ), despite the fact that pollen of some Lupinus species can contain enough alkaloids to harm those same bees (Arnold et al , ; Heiling et al , ). Furthermore, bumblebees did not show a preference for apple over almond pollen in a behavioural experiment (Ruedenauer et al , ), despite the known high concentration of amygdalin in pollen of the latter species.…”

Pollen layering and male–male competition: Quantum dots demonstrate that pollen grains compete for space on pollinators

“…Consequently, smothering may be especially important if pollinators do not groom or cannot groom the areas of deposition. Another factor that may select for larger pollen loads is that pollen‐consuming pollinators may prefer plants or flowers with larger pollen loads (Heiling et al, 2023 [in this issue]). Importantly, our demonstration of pollen preclusion does not mean that smothering is not occurring simultaneously and having opposite effects on plant fitness.…”