Why is pollen in Camellia oleifera inedible to honeybees?

This Commentary examines a recent study that addressed a long-standing controversy: Is the lethal effect of Tea-oil Camellia on honeybee larvae due to nectar or pollen toxicity? Flowers of Camellia oleifera are adapting to bird pollination, evolving 'anti-bee' traits such as theasaponin-containing pollen, which is toxic to bee larvae. The evolutionary transition from bee- to bird-pollinated plants is usually associated with multiple modifications in floral traits, such as color, size, nectar and pollen presentation mode (Thomson and Wilson, 2008). Compared to bee-adapted flowers, bird-flowers usually produce a larger volume of nectar with a lower sugar concentration (Sun et al., 2017). Optimal strategies for pollen presentation are evident in terms of the amount of pollen removed by single visits and pollinator visitation rates (Thomson et al., 2000). If bee visits are frequent, flowers presenting pollen in small doses onto many individual visitors would be favored to promote male reproductive success (Castellanos et al., 2006). Meanwhile, pollen exploitation by bees in flowers with gradual pollen presentation would be minimal given that pollen feeders frequently groom pollen off their bodies to provision larvae. Bird-pollinated flowers are adaptive for infrequent pollinator visits generally with simultaneous pollen presentation, in which case bees could be parasitic antagonists, consuming a large proportion of the pollen. It has been hypothesized that bird-pollinated flowers would evolve "anti-bee" pollen-related traits to deter bees from feeding (Thomson and Wilson, 2008). Zhang et al. (2024), for the first time, demonstrated that flowers in Camellia oleifera are characterized as being bird- rather than bee-pollinated, producing a large volume (>300 μL) of nectar with a low sugar concertation (21%) and simultaneously presenting large amounts of pollen grains, which if toxic could be adaptive to avoid consumption by honeybees (Figure. 1). Although it is well known that theasaponin (TS), a secondary metabolite, is widespread in the leaves of many Camellia species in the tea family, Zhang et al. found that its concertation was higher in pollen than in the stems, leaves, petals and fruits of Camellia oleifera; it was undetectable in floral nectar. Previous observations suggested that effective pollinators for the tea-oil Camellia were solitary Andrena bees. Zhang et al. found that most floral visitors foraged for nectar only (Figure. 1A). They conducted caged-bird experiments to isolate large visitors without affecting bee visits of C. oleifera flowers. They showed that the warbling white-eye (Zosterops japonicus) was an important pollinator when insects were relatively less active on low-temperature days in winter. Honeybees dislike collecting pollen in Camellia oleifera which containing theasaponins might cause larval mortality (A) A honeybee is trying to collect nectar from outside the androecium in C. oleifera. Note that the bee's body does not have any pollen on it. (B) Zhang et al. (2024) found that honeybee larvae well developed in yeast as shown here above the white dashed line, but only a few survived for five days on a diet of pure C. oleifera pollen at the bottom three lines. Photo credit: (A) by Shuang-Quan Huang, and (B) by Chuan Zhang. Previous studies proposed that the lethal effects of Tea-oil Camellia on honeybee larvae were due to nectar and/or pollen toxicity (Kang and Fan, 1991; Li et al., 2022). However, multiyear observations in field populations of C. oleifera by Zhang et al. (2024) showed that all visitors preferred collecting nectar rather than pollen. Honeybees only collected pollen occasionally, although large amounts of pollen were freely accessible in the open-shaped flower. Therefore, it is reasonable to hypothesize that the primary cause of larva mortality could be toxic pollen, in which chemical defense may deter honeybees from grooming pollen into its corbiculae. To test pollen toxicity of C. oleifera, Zhang et al. (2024) took two approaches to estimate the effect of diet treatments on larval development. First, they added C. oleifera pollen to form four types of larva diets: Brassica napus pollen from honeybee pollen baskets, a 50:50 mixture of B. napus and C. oleifera pollen, pure C. oleifera pollen and yeast as control. The cumulative survival of honeybee larvae showed that diets with 100% and 50% C. oleifera pollen caused significant larval mortality (Figure. 1B), compared to the yeast control and pollen from B. napus. Second, they tested the toxicity of TS at seven graded concentrations to further examine whether the lethal effect could be caused by the chemical component in pollen. Their two diet treatments confirmed that the lethal effect of C. oleifera on honeybee larvae was caused by toxic pollen, likely due to pollen containing relatively high TS. The authors concluded that toxic pollen in C. oleifera could prevent pollen overconsumption from inefficient pollinators (e.g., honeybees), providing new evidence for bird-pollinated flowers evolving "anti-bee" traits. How do honeybees response to "anti-bee" pollen? The answer to this question can help us comprehensively understand the evolutionary transitions of pollen-related traits from bee- to bird-pollination systems. It is necessary to further study chemical defenses in pollen as a factor shaping honeybee behavior, especially the foraging behavior in C. oleifera flowers. Studies have suggested that honeybees could make a decision to collect or to discard pollen using associative learning to correlate pollen toxicity (Nicholls and Hempel, 2016). For example, both honeybees and bumblebees can be susceptible to bitter-tasting pollen, and they reject grooming pollen that contains high amounts of toxic components (Wang et al., 2019; Hao et al., 2023). The study by Zhang et al. (2024) could explain why pollen of C. oleifera is inedible to honeybees, illustrating the ecological function of "anti-bee" pollen against overexploitation. Seed production in C. oleifera when grown as a crop that produces high-quality edible oils relies on pollinators, but what causes larval mortality if honeybees foraging on C. oleifera remains controversial. The study provides a new perspective of chemical defense in protecting pollen from bee exploitation in bird-pollinated flowers, which will help beekeepers to manage honeybees in C. oleifera crop production. To avoid larval mortality, for example, a simply way is just to isolate toxic pollen into bee bread. We thank Prof. S.-Q. Huang, and Mr. C. Zhang kindly providing photos as illustrated in Figure 1, and Prof. Carol C. Baskin for editing an early version of this manuscript. This work was supported by the National Natural Science Foundation of China (32360268) and the Natural Science Foundation of Xinjiang Uygur Autonomous Region of China (2022D01E49). The authors declare no conflict of interest. L.T. and J.M. conceptualized the idea; W.Z. and J.M. wrote the initial draft. All authors read and approved of its content.