Colour Patterns, Distribution and Food Plants of the Asian Bumblebee Bombus Bicoloratus (Hymenoptera: Apidae)
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Apidologie (2019) 50:340–352 Original article * INRA, DIB and Springer-Verlag France SAS, part of Springer Nature, 2019 DOI: 10.1007/s13592-019-00648-1 Colour patterns, distribution and food plants of the Asian bumblebee Bombus bicoloratus (Hymenoptera: Apidae) 1 2 1 1 1 Guiling DING , Shiwen ZHANG , Jiaxing HUANG , Muhammad NAEEM , Jiandong AN 1Key Laboratory for Insect-Pollinator Biology of the Ministry of Agriculture and Rural Affairs, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing 100093, China 2Gansu Institute of Apiculture, Tianshui 741022 Gansu, China Received 11 November 2018 – Revised 13 February 2019 – Accepted 19 March 2019 Abstract – Bombus bicoloratus is an important pollinator of wild flowers in the oriental region. We confirmed a total of 451 specimens of B. bicoloratus from China based on DNA sequences from mitochondrial cytochrome oxidase subunit I (COI) barcodes. Bombus bicoloratus is distributed mainly in tropical and subtropical areas of southern China. This species exhibits a striking intraspecific colour-pattern polymorphism both in females and males. The distribution frequency of the different colour patterns is heavily skewed, with 50.9% of the workers sharing the same colour pattern that predominates in most locations. Workers from the islands of Hainan and Taiwan possess a very distinct colour pattern, and its spatial distribution is correlated with the climate factor irradiance. Bombus bicoloratus has been recorded to collect nectar and pollen from 14 plant families, indicating that this species is polylectic. This study will be helpful for recognising bumblebee species with variable colour patterns, especially B. bicoloratus ,inAsia. Bombus bicoloratus / Colour pattern / COI / Distribution / Food plants 1. INTRODUCTION An 2018). To date, 125 bumblebee species have been identified in China, representing 50% of the As important pollinators for wild plants and bumblebee species recorded worldwide (Williams crops, bumblebees provide vital pollination ser- et al. 2017;HuangandAn2018). Although China vices in natural and agricultural ecosystems is the greatest hotspot of bumblebee diversity in the (Pywelletal.2006; Velthuis and van Doorn world, the complex taxa of this country are insuf- 2006; Goulson et al. 2008; Julier and Roulston ficiently described. These taxa include species with 2009). Bumblebees are widely distributed, and ap- diverse intraspecific colour patterns and cryptic proximately 250 species have been described species that differ little in colour and morphology. worldwide (Williams 1998). With diverse land- Further detailed species identifications and descrip- forms and rich vegetation, China harbours the tions are needed to enhance both the conservation highest richness of bumblebee species in the world of various bumblebee species and our understand- (Williams 1998; Williams et al. 2009;Huangand ing of their roles as pollinators. A prominent feature of bumblebees is that they are covered with long and brightly coloured hairs Corresponding author: J. An, [email protected] that form different colour patterns (Williams 2007). Guiling Ding and Shiwen Zhang contributed equally to High variation in colour patterns occurs within this work. some species, and the high evolutionary rates of Manuscript editor: Marina Meixner colour patterns even exceed those of mitochondrial Colour patterns, distribution and food plants of the Asian bumblebee Bombus bicoloratus (Hymenoptera: Apidae) 341 genes (Duennes et al. 2012; Hines and Williams Williams et al. 2009;Anetal.2014; Huang et al. 2012; Huang et al. 2015b). In addition, colour 2015a). Bombus bicoloratus Smith was first de- patterns often converge among bumblebee species scribed in 1879 based on specimens from Taiwan depending on geography and habitat (Williams that were in the collection of the British Museum. 2007;Lozieretal.2013). The exceptional colour- The abdominal terga are entirely ferruginous or pattern diversity within species and the conver- fulvous except for a patch of black hairs on the gence among species have led to inaccurate de- basal middle portion of the first tergite (Frison scriptions of some bumblebee species, such as the 1934). Because of the distinct colour morphs of description of the Bombus lucorum complex B. bicoloratus from Taiwan, bumblebees from (Murray et al. 2008; Waters et al. 2011). Studies mainland China with yellow bands were previously have revealed that colour patterns cannot be used to described as a separate species, Bombus identify some bumblebee species (Carolan et al. kulingensis , which was grouped into the subgenus 2012; Williams et al. 2012). New colour patterns Senexibombus with B. bicoloratus (Williams have been discovered from expanded sample col- 1998; Cameron et al. 2007). Females of lections, and quantitative and systematic studies of B. bicoloratus from mainland China typically have colour variations are lacking, especially for those hairs on the thorax with yellow anterior and poste- species with multiple colour forms. rior bands, sometimes with narrow yellow thoracic The progress in the application of molecular bands intermixed with black. Metasomal terga 1–2 methods has made it much easier and more reliable and often most of tergum 3 are yellow, and tergum to identify species and estimate phylogenetic rela- 5 is orange-red (Williams et al. 2009). As a species tionships. Nuclear genes and mitochondrial se- that is widely distributed over middle-low altitudes quences have been used to obtain robust phyloge- in Taiwan, B. bicoloratus has been screened for netic information and have led to revisions in bum- artificial rearing, and 52% of wild queens can blebee systematics (Kawakita et al. 2004;Cameron produce small colonies (Ho et al. 2002). Although et al. 2007; Vesterlund et al. 2014). Due to the high B. bicoloratus has recently been reported in some rates of sequence changes in mitochondrial cyto- regions of China (Williams et al. 2009;Anetal. chrome oxidase subunit I (COI) and constraints on 2014), its distribution patterns, food plants and intraspecific divergence, COI barcodes provide an colour-pattern polymorphism have yet to be inves- easy and reliable solution for species discrimination tigated in detail. and phylogeny reconstruction (Hebert et al. 2003). In this study, with ample samples of Studies have demonstrated that COI barcoding is a B. bicoloratus collected in China in the last decade, cost-effective approach to resolve taxonomic un- we describe this species’ geographic distribution, certainty of bumblebee taxa. It has been used to summarise the diversity and spatial distribution of clarify the taxonomy of the cullumanus group, its colour patterns and document its food plants in which comprises three species highly similar in China. The results provide information essential for morphology, Bombus semenoviellus , Bombus the conservation of B. bicoloratus and for its unicus and Bombus cullumanus (Williams et al. potential application in commercial pollination. 2013). Furthermore, it has been applied to distin- guish the similarly coloured species in the subge- 2. MATERIALS AND METHODS nus Mendacibombus (Williams et al. 2016), iden- tify the cryptic species of the subgenus Bombus s. 2.1. Materials str. (Williams et al. 2012) and recognise species with variable colour patterns, such as Bombus A systematic survey of bumblebees in China koreanus (Huang et al. 2015b). has been ongoing since 2002 (Williams et al. Bombus bicoloratus is a medium-sized oriental 2017; Huang and An 2018). Bees were collected species with highly variable colour forms and a by sweeping with a nylon hand net. Detailed long tongue. This species was recently reported to information, including the name, elevation and belong to the subgenus Megabombus ,whichis location of the collection site, was recorded with considered very diverse in China (Williams 1998; a hand-held GPS (Garmin 60CS, China). The 342 G. Ding et al. collected bumblebees were pinned, labelled, dried (Thompson et al. 1994) to align these sequences and deposited in the Institute of Apicultural Re- and jModelTest v2.1.7 (Darriba et al. 2012)to search, Chinese Academy of Agricultural Sci- select the best nucleotide substitution model ac- ences (IAR-CAAS), Beijing, China. Among these cording to Akaike’s information criterion (AIC). collections, 506 B. bicoloratus –like specimens Species of the subgenera Thoracobombus and were preliminarily identified according to the keys Subterraneobombus were used as outgroup taxa. described by Williams et al. (2009) and An et al. A Bayesian tree was constructed using MrBayes (2014). The records of B. bicoloratus from Tai- v3.2.5 (Ronquist et al. 2012) with two runs of wan, which have been confirmed by the authors, 100,000,000 generations and a sampling frequen- were obtained from the website http://gaga.biodiv. cy of once every 1000 generations. The phyloge- tw/new23/cp03_76.htm. Photographs of the food netic tree was displayed and edited using FigTree plants visited by bumblebees were also collected, v1.4.3 (http://tree.bio.ed.ac.uk/software/figtree/). and the food plants were identified from these We used three methods for species delimita- photographs. tion. The aligned sequences were analysed using Automatic Barcode Gap Discovery (ABGD) soft- 2.2. Genetic analysis ware (Puillandre et al. 2012) with a transition/ transversion ratio of 2 and simple distance. The For each of the three castes (queens, workers Bayesian Poisson tree processes (bPTP) method and males), we selected