Research Article |
Corresponding author: Martin Streinzer ( martin.streinzer@univie.ac.at ) Corresponding author: Johannes Spaethe ( johannes.spaethe@uni-wuerzburg.de ) Academic editor: Michael Ohl
© 2019 Martin Streinzer, Jharna Chakravorty, Johann Neumayer, Karsing Megu, Jaya Narah, Thomas Schmitt, Himender Bharti, Johannes Spaethe, Axel Brockmann.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Streinzer M, Chakravorty J, Neumayer J, Megu K, Narah J, Schmitt T, Bharti H, Spaethe J, Brockmann A (2019) Species composition and elevational distribution of bumble bees (Hymenoptera, Apidae, Bombus Latreille) in the East Himalaya, Arunachal Pradesh, India. ZooKeys 851: 71-89. https://doi.org/10.3897/zookeys.851.32956
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The East Himalaya is one of the world’s most biodiverse ecosystems. However, very little is known about the abundance and distribution of many plant and animal taxa in this region. Bumble bees are a group of cold-adapted and high elevation insects that fulfil an important ecological and economical function as pollinators of wild and agricultural flowering plants and crops. The Himalayan mountain range provides ample suitable habitats for bumble bees. Systematic study of Himalayan bumble bees began a few decades ago and the main focus has centred on the western region, while the eastern part of the mountain range has received little attention and only a few species have been verified. During a three-year survey, more than 700 bumble bee specimens of 21 species were collected in Arunachal Pradesh, the largest of the north-eastern states of India. The material included a range of species that were previously known from a limited number of collected specimens, which highlights the unique character of the East Himalayan ecosystem. Our results are an important first step towards a future assessment of species distribution, threat, and conservation. Clear elevation patterns of species diversity were observed, which raise important questions about the functional adaptations that allow bumble bees to thrive in this particularly moist region in the East Himalaya.
Alpine habitats, Apidae, conservation, global change, insect collection, pollination
Bumble bees (Hymenoptera, Apidae, Bombus Latreille) are a group of conspicuous, large and colourful bees that mainly inhabit cold and temperate habitats at high latitudes and elevations. Their conspicuous appearance and abundance established them a prime object of study for numerous early naturalists and insect collectors. After extensive revision in the past decades, around 260 species are currently recognized (
Current global sampling efforts focus on revising the bumble bee taxonomy at the subgeneric level and filling in blank spots in global distribution data for a worldwide IUCN red list assessment of all species (http://iucn.org/bumblebees). The latter is urgently needed, since a number of bumble bee species have recently shown dramatic declines in their abundance and range (
Bumble bees are pollinators of many wild flowers. They are abundant throughout the season and, due to their thermoregulatory abilities, are able to be active at very low ambient temperatures (
Bumble bees are cold adapted and therefore are most diverse and abundant in northern temperate habitats and in alpine environments. The Himalaya, the longest mountain range in the world, is home to a high bumble bee diversity due to its variety of suitable habitats. The mountain range spreads over 3,000 km between the Karakorum in the west and the Patkai and Hengduan mountain ranges in the east. As a major barrier for the south-eastern monsoon winds, it plays an important role in shaping the climate of entire South Asia (
So far, bumble bee composition was intensively studied in the West (
In this study, the results from the first systematic survey of bumble bees in Arunachal Pradesh are reported based on material collected during three major and a few minor field trips during the years 2015–2017. The survey represents the first phase of a project aiming to (1) document the bumble bee diversity in the East Himalaya to aid global distribution range assessments, (2) identify local pollinators of fruits, vegetables and other crops, and (3) describe functional adaptations that allow bumble bees to thrive in the particularly challenging climate of the East Himalaya.
Arunachal Pradesh is the largest of the North-East Indian states and is bordered by Bhutan in the west, the People’s Republic of China (Autonomous region of Tibet) in the north, Myanmar in the east and the Indian states of Assam and Nagaland in the south (Fig.
Bumble bee specimens were collected during three major field surveys in the years 2015–2017. The field trips covered the entire flowering season, pre-monsoon (May–Jun. 2016), during monsoon (Aug.–Sep. 2017), and post-monsoon (Sep.–Oct. 2015). Additional specimens were collected from the entire state during shorter field visits (post-monsoon) in the years 2016–2017 (Fig.
Sampling locations A Mainland India (light grey) showing the geographic location of Arunachal Pradesh (red) in the northeast region (NER, dark grey). Outlines denote Indian state borders. B Sampling locations within the state of Arunachal Pradesh for three major and a few minor field trips between 2015 and 2017. The locations are projected from GPS data to a SRTM elevation data set. The colour scale refers to elevation and does not reflect vegetation zone. Scale in B represents 100 km.
Bumble bee habitats in Arunachal Pradesh A Grass–/shrubland at 1,950–2,050 m elevation (Mechuka, West Siang district). Workers of B. festivus and B. luteipes and workers and males of B. flavescens were observed visiting Cotoneaster bushes B Agricultural crops located in a river valley at 1,500 m elevation (Old Dirang, West Kameng district). Workers of B. flavescens were collected from Punica granatum flowers C Ever-green deciduous Rhododendron– and Pinus-forests at 3,500 m (Karpo, Tawang district), where we collected queens of B. festivus and B. pressus D Alpine meadow with flowering Primula sp. and Rhododendron sp. (Se-La Pass, Tawang district) at 4,260 m, where we collected B. mirus, B. lemniscatus, B. nobilis, B. festivus, B. rufofasciatus, B. miniatus, and B. novus.
Bumble bees were collected by sweep netting and immediately killed with cyanide or ethyl acetate. The specimens were then stored in airtight containers with a few layers of tissue and the addition of a few drops of ethyl acetate to prevent the growth of mould during transport. After the field sampling, specimens were dry-mounted on standard insect pins for identification. The collected specimens were deposited in the NCBS Research Collection (National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India) for future reference. A full list of the collecting information of the museum specimens is available upon request (curators: Dr Axel Brockmann and Dr Krushnamegh Kunte, NCBS Bangalore). In addition to the collected specimens, some field observations were conducted. Since the observed specimens are not available for later reference, only those are included that could be unambiguously identified and that were from locations where additional voucher specimens of the same species were collected. In addition to the specimens collected in this project, entomological collections were examined for bumble bees from Arunachal Pradesh.
Permits to sample bumble bees were issued by the Government of Arunachal Pradesh to Jharna Chakravorty (No. SFRI/APBB/9/2011-846, No. SFRI/APBB/09/2016/1168) and to Himender Bharti (No. CWL/G/13 (95)/2011-12/Pt./2471-75).
Specimens were identified using published identification keys for adjacent regions, e.g., Kashmir (
Between 2015 and 2017, 773 bumble bee specimens were either collected, identified in the field and from photographs or identified in entomological collections (Table
The sampled region covers most of the state Arunachal Pradesh, and the least amount of sampling was carried out in the eastern-most region (Fig.
Species and subgeneric diversity along the elevational gradient. In the lowland tropical forest (< 1,000 m) only B. haemorrhoidalis, B. albopleuralis, and B. breviceps were observed. With increasing elevation, we found an increasing diversity of species. The relatively low diversity at > 4,000 m may represent a sampling bias, since only a few locations were accessible.
Summary of the collected bumble bee specimens. All specimens (N = 773) are listed that were examined and identified by the authors, including material collected during the field trips, specimens from research and museum collections, and specimens identified in the field. Subgenera are sorted according to their phylogenetic position (
Subgenus | Species | Σ | Q | W | M | Elevation | No. Localities |
Orientalibombus | B. funerarius Smith,1852 | 3 | 0 | 2 | 1 | 2,400–3,230 | 2 |
B. haemorrhoidalis Smith,1852 | 150 | 13 | 130 | 7 | 400–3,450 | 48† | |
Megabombus | B. albopleuralis Friese,1916 | 83 | 5 | 70 | 8 | 230–2,990 | 40† |
Psithyrus | B. cornutus (Frison,1933) | 1 | 0 | NA | 1 | 3,280 | 1 |
B. novus (Frison,1933) | 1 | 1 | NA | 0 | 4,200 | 1 | |
Pyrobombus | B. abnormis (Tkalcu,1968) | 4 | 4 | 0 | 0 | 3,680–3,940 | 2 |
B. flavescens Smith,1852 | 31 | 2 | 22 | 7 | 1,510–3,130 | 8 | |
B. hypnorum s.l. (L.,1758) | 9 | 0 | 4 | 5 | 2,850–3,980 | 5 | |
B. lemniscatus Skorikov,1912 | 10 | 6 | 1 | 3 | 3,500–4,260 | 5 | |
B. luteipes Richards,1934 | 76 | 0 | 70 | 6 | 1,150–3,500 | 21 | |
B. mirus (Tkalcu,1968) | 98 | 17 | 51 | 30 | 2,850–4,260 | 24 | |
B. parthenius Richards,1934 | 20 | 0 | 16 | 4 | 2,950–3,680 | 8 | |
B. pressus (Frison,1935) | 41 | 4 | 27 | 10 | 3,510–4,030 | 19 | |
Alpigenobombus | B. breviceps Smith,1852 | 34 | 3 | 28 | 3 | 480–2,790 | 19 |
B. genalis Friese,1918 | 6 | 0 | 6 | 0 | 1,560–1,850 | 3 | |
B. grahami (Frison,1933) | 2 | 0 | 2 | 0 | 2,710 | 1 | |
B. nobilis Friese,1905 | 75 | 4 | 61 | 10 | 3,780–4,260 | 21 | |
Melanobombus | B. eximius Smith,1852 | 9 | 1 | 8 | 0 | 1,090–1,720 | 6 |
B. festivus Smith,1861 | 63 | 4 | 54 | 5 | 1,940–4,260 | 21 | |
B. miniatus Bingham,1897 | 31 | 1 | 17 | 13 | 2,400–4,240 | 11 | |
B. rufofasciatus Smith,1852 | 26 | 11 | 11 | 4 | 2,400–4,260 | 11 |
During several field trips in the Indian state of Arunachal Pradesh, over 700 bumble bee specimens were collected, belonging to 21 species. This survey represents the first systematic study of bumble bee diversity in the East Himalayan range, an area known as a biodiversity hotspot and an important region for conservation priority (
Previously, extremely few confirmed records for Bombus exist for Arunachal Pradesh.
The present checklist for Arunachal Pradesh, comprising 22 species (including B. turneri, which was not found in our survey), places Arunachal Pradesh close to the species diversity found in the West Himalaya, e.g., Kashmir [29 species], Himachal Pradesh [25] and Uttarakhand [22] (
Future work in the region will also provide material for taxonomic revisions. Resulting from the large number of specific, subspecific, and infrasubspecific synonyms, a genus wide revision is still under progress (
Particularly high local convergence in colour pattern is often found within the genus Bombus. It is usually interpreted as Müllerian mimicry (
Three of these species were found in our study area and showed identical colour pattern across Arunachal Pradesh. Two other mimetic groups are present in the region, each comprising members of at least two different subgenera. First, B. (Pyrobombus) abnormis, B. (Pyrobombus) hypnorum s.l. and workers of B. (Melanobombus) festivus Smith all have a brown thorax and a white tail. The second group comprises B. (Pyrobombus) flavescens Smith, B. (Melanobombus) eximius and B. (Alpigenobombus) genalis Friese, which are characterized by black body pile, orange tinted wings and orange-brown cuticle and hairs on the legs (see examples in Fig.
Examples of bumble bee species collected in Arunachal Pradesh A Bombus miniatus (queen) is a West Himalayan species of the subgenus Melanobombus reaching its eastern distribution limit in Arunachal Pradesh B Bombus genalis (worker), a rare species of the mid-elevation narrowly distributed in the East Himalaya C Bombus albopleuralis (worker), a widespread Himalayan species that occurs in a large elevational range from the tropical lowlands to the subalpine zone in Arunachal Pradesh D Bombus abnormis (queen), an elusive and very rare high elevation species of the subgenus Pyrobombus narrowly distributed in the East Himalaya.
Colour pattern convergence within Bombus is also often observed between the parasitic species of the subgenus Psithyrus and their preferred host species (
Covering a large range of elevations and habitat types, clear patterns of species-specific elevational ranges were recognised (Fig.
Our observations may have multiple, not mutually exclusive, explanations. First, the specific climate of the East Himalaya probably allows certain bumble bee species to thrive at relatively lower elevations (see below). Indeed, there seems to be a gradual decrease in the lower elevation limit from the west to the east that supports this interpretation (
B. haemorrhoidalis, B. albopleuralis, and B. breviceps cover a wide range of elevations and usually were most abundant at medium elevations (Table
Several physiological and behavioural adaptations have been discussed in the context of elevational adaptation in bumble bees and previous work shows that behavioural plasticity enables quick adaptation to different elevations (
The discovery of many rare and confined species of bumble bees in Arunachal Pradesh highlights the importance of extensive sampling in remote regions to better understand species distribution and ecological requirements (see also the discussion in
Arunachal Pradesh can currently be considered a remote region without serious recent land use changes, only small-scale agriculture and a low population density (
In the Himalaya, bumble bees serve as important pollinators of many fruits, vegetables, e.g., cardamom (
We are particularly grateful to the students that assisted us during the field collections (Rajiv Gandhi University: Mosses Messar, Mohin Raza Naqvi, Nyaton Kitnya; Punjabi University: Joginder Singh, Sishal Sasi; University of Würzburg: Franziska Bandorf) as well as Tapir Darang, and the drivers and carriers who made the field trips possible.
We further thank the curators of the NCBS Research Collection (Dr K Kunte) and the Collection of the Entomology Department of the University of Agricultural Sciences, GKVK, Bangalore (Prof V Belavadi) for access and support during our visits to the collections and the permit to use their data for our distribution records. PH Williams (National History Museum, London, UK) provided much valuable information and kindly identified some voucher specimens. We thank J Plant for linguistic support.
The bumble bee mapping project is part of the Chemical Ecology Network Programme funded by the Department of Biotechnology, Govt of India (Sanction number DBT-NER/Agri/24/2013). The field trips of researchers from RGU and NCBS were supported by funds from Chemical Ecology Project. Researchers from the University of Würzburg and Vienna were supported by institutional funds from the University of Würzburg to Thomas Schmitt and Johannes Spaethe. This publication was partially funded by the German Research Foundation (DFG) and the University of Wuerzburg in the funding programme Open Access Publishing.
Distribution maps of all collected bumble bee species
Data type: occurrence
Explanation note: Distribution maps were created from projecting GPS collection data to an SRTM elevation dataset. The colour scale represents elevation and does not reflect vegetation zone. Each map is accompanied with a histogram of the elevations at which we collected the specimen. Species grouping follows Table
Examples of bumble bee species collected in Arunachal Pradesh
Data type: species data
Explanation note: (A) Queens of the social parasite Bombus (Psithyrus) novus and two potential host species from the subgenus Melanobombus, (B) B. miniatus and (C) B. rufofasciatus. All species were found to co-occur in the west of Arunachal Pradesh (~ 4,200 m, Se-La Pass environment, Tawang Region).