The conserved and high K-to-Na ratio in sunflower pollen: Possible implications for bee health and plant-bee interactions

Abstract

Sodium (Na) concentrations are low in plant tissues, and its metabolic function in plants is minor; however, Na is a key nutrient for plant consumers. Previous studies have thus far focused on Na concentration. Nevertheless, a balanced potassium (K) to Na ratio (K:Na) is more important than Na concentration alone since food with high K:Na has detrimental effects on consumers irrespective of Na concentration. Therefore, plants may actively regulate K:Na in their tissues and products, shaping plant-insect interactions. Studies considering nutritional aspects of plant-insect interactions have focused on nonreproductive tissues and nectar. In this study, we consider pollen as serving a primary reproductive function for plants as well as a food of pollinivores. Plants might regulate K:Na in pollen to affect their interactions with pollinivorous pollinators. To investigate whether such a mechanism exists, we manipulated Na concentrations in soil and measured the proportion of K, Na, and 13 other nutrient elements in the pollen of two sunflower (Helianthus annuus) cultivars. This approach allowed us to account for the overall nutritional quality of pollen by investigating the proportions of many elements that could correlate with the concentrations of K and Na. Of the elements studied, only the concentrations of Na and K were highly correlated. Pollen K:Na was high in both cultivars irrespective of Na fertilization, and it remained high regardless of pollen Na concentration. Interestingly, pollen K:Na did not decrease as pollen increased the Na concentration. We hypothesize that high K:Na in pollen might benefit plant fertilization and embryonic development; therefore, a tradeoff might occur between producing low K:Na pollen as a reward for pollinators and high K:Na pollen to optimize the plant fertilization process. This is the first study to provide data on pollen K:Na regulation by plants. Our findings broaden the understanding of plant-bee interactions and provide a foundation for a better understanding of the role of the soil-plant-pollen-pollinator pathway in nutrient cycling in ecosystems. Specifically, unexplored costs and tradeoffs related to balancing the K:Na by plants and pollinivores might play a role in past and current shaping of pollination ecology.

Uncovering the significance of the ratio of food K:Na in bee ecology and evolution

“…Plants are limited by the availability of mineral nutrients in soil and thus have frequently evolved mutualistic relationships with fungi and other microbes. This limitation may impose trade-offs, and thus costs (including maintenance of mutualisms), in developing fitness-related traits, as suggested by Filipiak, Shields, et al (2022). For example, some proportion of minerals acquired from soil is invested to create pollen and nectar, which are then gathered and eaten by bees, and another proportion is allocated in other parts of the plant, such as leaves and stems, which could be eaten by leaf-eaters, for example, by butterflies, moths, or beetles.…”

“…A recent study suggests that this may indeed be the case regarding certain organic molecules (i.e., different proteins and lipids) (Huang & Gong, 2022). However, it is not known whether this also applies to K:Na (Filipiak, Shields, et al, 2022). There are two possible eco-evolutionary mechanisms related to the exceptional Na variability observed in pollen:…”

“…This finding suggests that plants might regulate K:Na in pollen by increasing/decreasing Na concentrations. However, the only study to date that has investigated this suggestion has shown that in the case of sunflower ( Helianthus annuus ) pollen, such regulation probably does not occur, at least in the short term of a single growth period (Filipiak, Shields, et al, 2022). However, some plants produce two types of pollen, one used to reward the bees and the other for reproduction (Luo et al, 2008).…”

“…A recent study suggests that this may indeed be the case regarding certain organic molecules (i.e., different proteins and lipids) (Huang & Gong, 2022). However, it is not known whether this also applies to K:Na (Filipiak, Shields, et al, 2022). There are two possible eco‐evolutionary mechanisms related to the exceptional Na variability observed in pollen: (1) some plant species might have high Na concentrations in pollen, since they produce pollen not solely to reproduce but also as a reward for pollinators (Nicholls & de Ibarra, 2017), while (2) other plants might reduce the concentration of Na in pollen to discourage pollen eating.…”

“…Furthermore, herbivores tend to prefer plant tissues and products with elevated Na (Borer et al, 2019; Finkelstein et al, 2022a; Nicolson & Worswick, 1990). Hence, it is conceivable that the soil–plant–bee pathway of the nutrient cycle is influenced by the plants' ability to use K:Na regulation in their pollinator rewards (but see Filipiak, Shields, et al, 2022). The impact of plant‐pollinator nutritional interactions on nutrient cycling within ecosystems remains to be thoroughly explored, especially considering the significance of the soil–plant–pollinator pathway of nutrient cycling for the functioning of food webs, ecosystems, and the well‐being of humans.…”