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 (<i>Apis mellifera</i>) 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 <i>A. mellifera</i> on the native pollinator (<i>Bombus sushikini</i>), reproductive success and offspring performance of <i>Gentiana straminea</i>, an alpine endemic species from the Qinghai-Xizang Plateau. Field experiments were conducted across alpine meadows with varying <i>A. mellifera</i> abundances, simultaneously assessing their impacts on (1) the abundance, visit frequency, and foraging behaviours of <i>B. sushikini</i>, and (2) the pollen availability, seed-setting rates, and offspring fitness of <i>G. straminea</i>. 3. We found that high <i>A. mellifera</i> abundance was associated with lower abundance and visitation rate of<i> B. sushikini</i>, caused a severe depletion of pollen resources in <i>G. straminea</i>, and was associated with a lower seed-setting rate (quantitative pollen limitation). Unexpectedly, <i>A. mellifera</i> altered <i>B. sushikini</i> 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.

1. 在许多雌雄异熟（dichogamous）、雌雄异位（herkogamous）以及雌雄异株（dioecious）的植物中，引入的西方蜜蜂（*Apis mellifera*）通常仅访问雄蕊以采集花粉，却不接触柱头，因此扮演了花粉盗贼（pollen thieves）的角色。由于这些花部性状普遍存在，且引入的西方蜜蜂目前已成为全球范围内占主导地位的花部访客（floral visitors），花粉盗食很可能是影响本土植物生殖成功（reproductive success）的关键因素。但花粉盗食如何影响本土传粉者的行为，进而影响植物的交配策略与适合度（fitness），目前仍不明确。
2. 本研究通过探究引入的西方蜜蜂（*Apis mellifera*）对本土传粉者祁连熊蜂（*Bombus sushikini*）、以及青藏高原特有高山物种麻花艽（*Gentiana straminea*）的生殖成功与后代表现的生态效应，来解答上述问题。研究在西方蜜蜂种群密度各异的高山草甸中开展野外实验，同时评估其对（1）祁连熊蜂的种群数量、访花频率与觅食行为，以及（2）麻花艽的花粉可获得性、结实率与后代适合度的影响。
3. 研究结果显示，西方蜜蜂的高种群密度与祁连熊蜂的种群数量和访花率下降显著相关，同时造成麻花艽的花粉资源严重耗竭，并导致其结实率降低（即定量花粉限制（quantitative pollen limitation））。出乎意料的是，西方蜜蜂改变了祁连熊蜂的觅食行为——减少了单株植物内的连续访花次数，增加了植株间的飞行距离——这与同株异花授粉（geitonogamy）减少、异交（outcrossing）率提升的结果一致。来自高西方蜜蜂密度样地的后代具有更高的种子质量、幼苗存活率与幼苗生物量，这表明花粉的遗传品质得到了提升。
4. 综合与应用。本研究表明，引入的西方蜜蜂通过对本土传粉者的间接作用，同时降低了植物的种子产量并提升了后代表现，揭示了外来传粉者对本土植物-传粉者共生关系（plant-pollinator mutualisms）的影响中，存在花粉数量与遗传品质之间的权衡。这一权衡关系强调，在评估规模化饲养蜜蜂（managed honeybees）的生态效应时，需要同时评估传粉过程的定量与定性维度。从更广泛的层面来看，本研究呼吁在存在雌雄异熟、雌雄异位或雌雄异株植物的区域，制定针对引入西方蜜蜂投放的因地制宜的指导方针，因为花粉盗食可能会重塑植物种群的长期存续能力。