Impacts of soil nutrition on floral traits, pollinator attraction, and fitness in cucumbers (Cucumis sativus L.)

Abstract

Annual plants allocate soil nutrients to floral display and pollinator rewards to ensure pollination success in a single season. Nitrogen and phosphorus are critical soil nutrients whose levels are altered by intensive land use that may affect plants’ fitness via pollinator attractiveness through floral display and rewards. In a controlled greenhouse study, we studied in cucumbers (Cucumis sativus) how changes in soil nitrogen and phosphorus influence floral traits, including nectar and pollen reward composition. We evaluated how these traits affect bumble bee (Bombus impatiens, an important cucumber pollinator) visitation and ultimately fruit yield. While increasing nitrogen and phosphorus increased growth and floral display, excess nitrogen created an asymptotic or negative effect, which was mitigated by increasing phosphorus. Male floral traits exhibited higher plasticity in responses to changes in soil nutrients than female flowers. At 4:1 nitrogen:phosphorus ratios, male flowers presented increased nectar volume and pollen number resulting in increased bumble bee visitation. Interestingly, other pollinator rewards remained consistent across all soil treatments: male and female nectar sugar composition, female nectar volume, and pollen protein and lipid concentrations. Therefore, although cucumber pollination success was buffered in conditions of nutrient stress, highly skewed nitrogen:phosphorus soil ratios reduced plant fitness via reduced numbers of flowers and reward quantity, pollinator attraction, and ultimately yield.

The nutritional landscape in agroecosystems: a review on how resources and management practices can shape pollinator health in agricultural environments

“…For example, Brassica napus L. (Brassicaceae) pollen can contain over 25% lipids when the exine is disrupted prior to analysis (Evans et al 1991, Lau et al 2022). Recent research have emphasized the importance of the ratio of proteins to lipids (P:L) in pollen, which can be a driving factor for bee pollen preferences (Vaudo et al 2015, 2016, 2020, 2022). Lipids shown to be essential for bees include fatty acids (oleic acid, omega 6 and omega 3 fatty acid) and phytosterols.…”

“…Intensive soil management used to manage weeds, such as tilling, can disrupt soil structure that had been established over time. Such negative impacts on the soil can affect floral traits that influence pollinator attraction and have implications on both pollinator health and crop yield (David et al 2019, Dai et al 2022, Filipiak et al 2022b, Vaudo et al 2022). Skewed nutrient ratios in the soil can affect the total number of flowers and resource nutritional quality and quantity (Vaudo et al 2022, Russo et al 2023).…”

“…Such negative impacts on the soil can affect floral traits that influence pollinator attraction and have implications on both pollinator health and crop yield (David et al 2019, Dai et al 2022, Filipiak et al 2022b, Vaudo et al 2022). Skewed nutrient ratios in the soil can affect the total number of flowers and resource nutritional quality and quantity (Vaudo et al 2022, Russo et al 2023). In contrast, no-till management practices can minimize the effects of soil erosion and nutrient loss (Pesant et al 1987), and reduced tillage can increase soil moisture by reducing evaporation rates, decreasing surface water runoff, and improving water infiltration into the soil (McVay et al 2006, Tyler and Locke 2018).…”

Manipulation of soil mycorrhizal fungi influences floral traits

“…50% of their nitrogen and upwards of 90% of phosphorus from associations with AMF (Bennett & Groten, 2022). Nitrogen and phosphorus are critical to flower production and display (White & Hammond, 2008); the availability of these soil nutrients has previously been shown to positively impact the size of floral traits including floral display, nectar volume, and pollen count (Burkle & Irwin, 2009; Vaudo et al ., 2022). In a study of the impacts of inoculation with the AMF Glomus etuniacatum on the herbaceous annual Abutilon theophrasiti , Lu & Koide (1994) found that AMF inoculation in nutrient‐poor soils was associated with a dramatic increase in the number of flowers produced, a greater proportion of flowers setting fruit, longer total flowering duration, earlier flowering, and more seeds per fruit.…”

“…In a study of the impacts of inoculation with the AMF Glomus etuniacatum on the herbaceous annual Abutilon theophrasiti , Lu & Koide (1994) found that AMF inoculation in nutrient‐poor soils was associated with a dramatic increase in the number of flowers produced, a greater proportion of flowers setting fruit, longer total flowering duration, earlier flowering, and more seeds per fruit. Furthermore, a recent study reported that increasing soil N and P concentrations lead to floral trait changes that resulted in increased visitation by bumblebees to cultivated cucumber plants (Vaudo et al ., 2022).…”