Pollen theft by introduced honeybees depresses seed set but improves offspring performance in a Himalayan gentian

1.In many dichogamous, herkogamous and dioecious plants, introduced honeybees (Apis mellifera) often only visit stamens to collect pollen without contacting the stigmas, thus acting as pollen thieves. Because these floral traits are prevalent, and introduced honeybees are now dominant floral visitors on a global scale, pollen theft is likely a key factor affecting native plants reproductive success. How pollen theft affects native pollinators’ behaviour, and in turn, plant mating and fitness, remains unclear.
2.We address this question by investigating the ecological consequences of introduced A. mellifera on the native pollinator (Bombus sushikini), reproductive success and offspring performance of Gentiana straminea, an alpine endemic species from the Qinghai-Xizang Plateau. Field experiments were conducted across alpine meadows with varying A. mellifera abundances, simultaneously assessing their impacts on (1) the abundance, visit frequency, and foraging behaviours of B. sushikini, and (2) the pollen availability, seed-setting rates, and offspring fitness of G. straminea.
3.We found that high A. mellifera abundance was associated with lower abundance and visitation rate of B. sushikini, caused a severe depletion of pollen resources in G. straminea, and was associated with a lower seed-setting rate (quantitative pollen limitation). Unexpectedly, A. mellifera altered B. sushikini foraging behaviour –reducing successive flower visits within plants and increasing interplant flight distances– consistent with reduced geitonogamy and increased outcrossing. Offspring from high-honeybee sites had higher seed mass, seedling survival, and seedling biomass, suggesting improved pollen genetic quality.
4.Synthesis and applications. Our study highlights that pollen theft by introduced honeybees simultaneously reduces seed production and improves offspring performance via indirect effects on native pollinators, revealing a trade-off between pollen quantity and genetic quality in the impacts of alien pollinators on native plant-pollinator mutualisms. This trade-off emphasizes the need to evaluate both quantitative and qualitative dimensions of pollination when assessing the ecological consequences of managed honeybees. More broadly, our work calls for context-specific guidelines on introduced honeybee deployment in regions with dichogamous, herkogamous or dioecious plants, where pollen theft could reshape long-term plant population viability.