Community-level plant–pollinator interactions in a Palaeotropical montane evergreen oak forest ecosystem

The montane terrain of northern Laos is covered by species-rich subtropical evergreen oak forests, home to endemic tree genera such as <i>Mytilaria</i> (Hamamelidaceae), and characterised by the coexistence of several honeybee and bumblebee species. We explored community-level plant–pollinator interactions of this unique little-known ecosystem. Extensive direct observations on flowering phenology and flower-visitor assemblages of 288 plant species of 82 families were conducted in a montane forest ecosystem in Houaphanh and Xiangkhouang Provinces, Laos, from 2005 until 2016. Based mainly on the extensive flower-visit data, we assessed the pollination system of each plant species. Five sympatric honeybee species (<i>Apis dorsata</i>, <i>A. laboriosa</i>, <i>A. cerana</i>, <i>A. florea</i> and <i>A. andreniformis</i>) were common on various types of flowers, and floral preferences differed among species. Long-tongued bees belonging to Bombini and Anthophorini (Apidae) were species-rich and frequent visitors on various deep flowers, especially Acanthaceae, Balsaminaceae, Lamiaceae, Rubiaceae and Zingiberaceae. Character displacement by tongue length was observed among the bee species, and many relaxed species-specific and species-semispecific interactions were observed between the bees and the deep-flowers. Four plant species, in the genera <i>Mytilaria</i>, <i>Chloranthus, Dioscorea</i> and <i>Cryptocarya</i>, were visited exclusively by thrips. Two plant species, in the genera <i>Lysimachia</i> and <i>Thladiantha</i>, had oil-secreting flowers, which were specifically visited by the oil-collecting bees <i>Macropis</i> and <i>Ctenoplectra</i>, respectively. The dominant pollination system assessed was general insect pollination (31%), followed by long-tongued bee, small bee, honeybee, dipteran, lepidopteran, beetle, wasp, carpenter bee, thrips (e.g. the endemic genus <i>Mytilaria</i>), bird and hemipteran pollination. Our results suggest that the plant–pollinator interactions in the Palaeotropic montane ecosystem are characterised by significant contribution of the five honeybee species and species-rich, morphologically diverse long-tongued bees, both of which have contributed to shaping the remarkable diversity of angiosperms with deep flowers.

老挝北部的山地被物种丰富的亚热带常绿栎林所覆盖，该森林是*Mytilaria*（金缕梅科）等特有树属的原生栖息地，同时兼具多种蜜蜂与熊蜂物种共存的特征。我们针对这一鲜为人知的独特生态系统，开展了群落水平的植物-传粉者互作研究。2005年至2016年，我们在老挝华潘省与川圹省的山地森林生态系统中，对82科共计288种植物的开花物候与访花昆虫类群进行了大规模直接观测。基于大量的访花观测数据，我们逐一评估了每种植物的传粉系统。五种同域分布的蜜蜂物种（大蜜蜂*Apis dorsata*、黑大蜜蜂*A. laboriosa*、东方蜜蜂*A. cerana*、小蜜蜂*A. florea*以及绿努蜂*A. andreniformis*）在多种花卉上极为常见，且不同物种的花卉偏好存在显著差异。隶属于熊蜂族（Bombini）与无垫蜂族（Anthophorini）的蜜蜂科（Apidae）长舌蜂类物种丰富度较高，同时是多种深花冠花卉的常见访花者，尤其偏好爵床科、凤仙花科、唇形科、茜草科及姜科植物。研究中观察到不同蜂类间存在喙长的特征替换现象，同时也发现了诸多宽松的物种特异性及半物种特异性的蜂类与深花冠植物间的互作关系。有4种隶属于*Mytilaria*、*Chloranthus*、*Dioscorea*和*Cryptocarya*属的植物，其访花者仅为蓟马。另有2种隶属于*Lysimachia*和*Thladiantha*属的植物，具有泌油花朵，它们分别专属地被集油蜂*Macropis*和*Ctenoplectra*所访花。经评估的主流传粉系统中，广谱昆虫传粉占比最高（31%），其次依次为长舌蜂传粉、小型蜂传粉、蜜蜂传粉、双翅目传粉、鳞翅目传粉、甲虫传粉、胡蜂传粉、木蜂传粉、蓟马传粉（如特有属*Mytilaria*所属的传粉系统）、鸟类传粉以及半翅目传粉。本研究结果表明，古热带山地生态系统中的植物-传粉者互作，以五种蜜蜂物种以及物种丰富、形态多样的长舌蜂类的显著贡献为核心特征，二者共同塑造了深花冠被子植物的显著多样性。