Research Article |
Corresponding author: Nyaton Kitnya ( nyatonkitnya@gmail.com ) Academic editor: Michael S. Engel
© 2020 Nyaton Kitnya, M. V. Prabhudev, Chet Prasad Bhatta, Thai Hong Pham, Tshering Nidup, Karsing Megu, Jharna Chakravorty, Axel Brockmann, G. W. Otis.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation:
Kitnya N, Prabhudev MV, Bhatta CP, Pham TH, Nidup T, Megu K, Chakravorty J, Brockmann A, Otis GW (2020) Geographical distribution of the giant honey bee Apis laboriosa Smith, 1871 (Hymenoptera, Apidae). ZooKeys 951: 67-81. https://doi.org/10.3897/zookeys.951.49855
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Worldwide pollinator declines have dramatically increased our need to survey and monitor pollinator distributions and abundances. The giant honey bee, Apis laboriosa, is one of the important pollinators at higher altitudes of the Himalayas. This species has a restricted distribution along the Himalayas and neighbouring mountain ranges of Asia. Previous assessments of its distribution, published more than 20 years ago, were based on museum specimens. Since then, 244 additional localities have been revealed through field trips by the authors, publications, and websites. We present a revised distribution for A. laboriosa that better defines its range and extends it eastward to the mountains of northern Vietnam, southward along the Arakan Mountains to west-central Myanmar, into the Shillong Hills of Meghalaya, India, and northwestward in Uttarakhand, India. This species is generally found at elevations between 1000–3000 m a.s.l.. In northeastern India A. laboriosa colonies occur during summer at sites as low as 850 m a.s.l. and some lower elevation colonies maintain their nests throughout the winter. Finally, we report three regions in Arunachal Pradesh, India, and nine locations in northern Vietnam, where we observed workers of A. laboriosa and A. dorsata foraging sympatrically; their co-occurrence supports the species status of Apis laboriosa.
Apidae, Apis dorsata, conservation, Himalayas, pollinator, sympatry
The Himalayan giant honey bee A. laboriosa is a spectacular but poorly understood species, in large part because it usually nests on inaccessible cliff faces in the Himalaya Mountains (
The most recent range map of A. laboriosa (
We present here an updated distribution map of A. laboriosa and present additional evidence that A. laboriosa and its sister species A. dorsata co-occur in several locations in Asia.
The Himalayan giant honey bee A. laboriosa differs significantly from the giant honey bee A. dorsata of mainland Asia in many characters noted by
Apis laboriosa and Apis dorsata worker bees. A. laboriosa (left) has a completely dark abdomen and long golden thoracic hairs. A. dorsata (right) has several orange or yellow anterior abdominal segments and dark thoracic hairs. Details for the specimens photographed: A. laboriosa, collected by BA Underwood, Kaski District, Nepal, 1860 m, 8 v 1984 (Nest 6–8); A. dorsata, collected by GW Otis, Serdang, Selangor, Malaysia, 3.00 N, 101.68 E, 8 ii 1989. Scale bar: 1 cm.
The starting point for this project was the list of collection localities reported by
Subsequently,
CPB collected specimens from many parts of Nepal to analyze genetic variability within A. laboriosa; he contributed 17 additional localities in Nepal.
TN contributed 29 new localities in Bhutan in addition to the two localities he and his colleague had reported earlier (
Within India, a team (NK, MVP, KM, JC, and AB), in their fieldwork on A. laboriosa, have added numerous localities from northern and northeastern India. Several authors have reported sites where this bee species occurs in Uttarakhand, India (
Hliang Min Oo (pers. comm.) located cliffs inhabited by ~50 colonies of A. laboriosa in the mountains of western Myanmar. He shared photos that are clearly of that species. Anne Schooffs (pers. comm.) and Kevin Kamp (pers. comm.) contributed their observations in Laos. Similarly, Xin Zhou and Li Fei Qui (pers. comm.) shared details of their 2019 collection locality in Yunnan, China. Cao and colleagues already reported two localities in Yunnan in 2012 (
We recognize that some records are stronger than others. Consequently, we have distinguished four categories of records:
We obtained additional bee localities by searching for photos on the internet and literature about the yellow-rumped honeyguide (Indicator xanthonotus). The honeyguides (Indicatoridae) are one of the few taxa of animals known to be able to digest wax (
In our personal field work, we used global positioning system (GPS) instruments (i.e., eTrex 20, Garmin Ltd, Olathe, Kansas, USA) to document locations. When that was not possible or we had only a locality name (e.g., many of the localities reported in publications), we searched for them using Google Maps. Occasionally due to changes in names or spellings, we undertook lengthy web searches to find the current names. Not all records could be located (e.g., “Pamir, Arunachal Pradesh” reported by
We plotted locality records using ArcGIS Desktop 10.3 of ESRI (Environmental System Research Institute, www.esri.com). The boundary maps of the region of interest were extracted from Google Earth Pro (v7.3) as a Keyhole Markup language Zipped (kmz) file and imported into ArcGIS.
We have compiled a list of 349 localities of Apis laboriosa foragers or nests (Suppl. material
Geographical distribution of Apis laboriosa. Each circle indicates a locality at which a nest of A. laboriosa or workers foraging on flowers were found. The color indicates the source of information. Dark red: information collected by one or several of the authors; orange: photos published on websites; tan: information from published papers; and grey: oral reports by colleagues or local people. Scale bar: 250 km.
Localities range in elevation from approximately 230–4270 m a.s.l. Nearly all records (94%) fall within the altitudinal range of 500–3500 m a.s.l., and 77.2% were between 1000–3000 m a.s.l. (Fig.
Elevational distribution of A. laboriosa records for Uttarakhand, Nepal, Bhutan and Arunachal Pradesh. 94% of all records were found between 500–3500 m a.s.l.. The lowest occurrence of A. laboriosa was observed in Arunachal Pradesh (229 m a.s.l.), and the highest in Nepal (4267 m a.s.l.). Uttarakhand (N = 17; range: 1008–2743 m a.s.l.; mean: 1927 ±131 m), Nepal (N= 60; range: 800–4100 m a.s.l.; mean: 2036 ±103 m), Bhutan (N = 43; range: 631–3399 m a.s.l.; mean: 2077 ±124 m), Arunachal Pradesh (N = 17; range: 229–3649 m a.s.l.; mean: 1620 ±143 m).
In their field trips, the Indian team discovered five sites in three regions of Arunachal Pradesh in northeastern India where A. laboriosa foraged together with its sister species A. dorsata. The regions and sites were: (1) Western Arunachal: West Kameng District, Nag Mandir; (2) Central Arunachal: West Siang District, Tumbin and Siang District, Modi; and (3) Southeast Arunachal: Tirap District, Kala Pahar and Tutnyu (Fig.
Sites of sympatric occurrence of Apis laboriosa and Apis dorsata in Arunachal Pradesh, India. All five localities (black dots) where we found A. laboriosa and A. dorsata foraging together were below 1500 m a.s.l. (1) West Kameng District, Nag Mandir, 27.203N, 92.561E, 1164 m a.s.l; (2) West Siang District, Tumbin, 28.456N, 94.684E, 356 m a.s.l; (3) Siang District, Modi, 28.487N, 95.087E, 534 m a.s.l; (4) Tirap District, Kala Pahar, 26.934N, 95.576E ,1470 m a.s.l; (5) Tutnyu, 26.962N, 95.631E, 1060 m a.s.l. Scale bar: 100 km.
Apis laboriosa inhabits a 2500 km swath along the southern edge of the Pan-Himalaya region. We have added considerably to the distribution of this species as last presented by
Very few (N = 10; 6.2%) collections and observations have been made at locations situated at elevations below 500 m or above 3500 m a.s.l. (Fig.
Earlier research reported that the altitudinal ranges of A. laboriosa and its sister species A. dorsata differ substantially (
Separate from its species status, A. laboriosa shows several unique characters that seem to be specific adaptations to living in mountainous habitats. Comparative studies of A. laboriosa and A. dorsata have shown that they differ in behaviour such as thermoregulation of thoracic temperature during flight (
Apis laboriosa is notably absent from the western third of Nepal, from 80.5N to 82.6E longitude. This may reflect the relatively dry climate of western Nepal, a lack of collections, or habitat degradation. Field work in several other mountainous portions of Asia may detect this species. These include:
Several lines of evidence point to the existence of A. laboriosa in Pakistan.
Worldwide pollinator declines have increased the urgency to survey abundances of pollinators and to study their biology and ecology for their conservation. Asian honey bees and in particular species like A. laboriosa, with a restricted distribution in areas difficult to access, are dramatically understudied. Our study provides a revised description of the distribution of the Himalayan giant honey bee, Apis laboriosa. This is a necessary step to revitalize studies on this important pollinator species in the Himalayas (
Numerous reports on A. laboriosa indicate that this honey bee shows specific adaptations to living in high elevation mountainous areas compared to other more tropical honey bee species. Detailed studies on its biology promise to provide interesting insights into the evolutionary history and plasticity of honey bee physiology and social behavior. Locations where A. laboriosa and A. dorsata co-occur temporally, like those we report in Arunachal Pradesh and Vietnam, are particularly suitable regions for future studies.
We thank M. Hliang (University of Veterinary Science, Yezin, Myanmar), A. Schooffs (Association for Sustainable Beekeeping, Laos), K. Kamp (Agro-Biodiversity Initiative, National Agricultural and Forestry Research Institute, Laos), V. Sarkar (Wildlife Institute of India, Dehradun, India), K. Tan (Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming, China), K.A. Khan (Unit of Bee Research and Honey Production, King Khalid University, Abha, Saudi Arabia, for information about Pakistan), and X. Zhou and L. Qui (Agricultural University, Beijing, China) for sharing information on locations of bees in the respective countries. M. Messar, J. Narah, N. Jamoh, D. Songthing and I. Haikam helped to collect data in Arunachal Pradesh and Nagaland, India. Numerous people who have posted photographs to iNaturalist and other websites (identified in Suppl. material
Research and field trips of researchers from RGU and NCBS were supported by funds from Department of Biotechnology Twinning R&D programme for the North-East NER to JC and AB (BT/PR16880/NER/95/333/2015); and institutional funding from National Centre for Biological Sciences (NCBS-TIFR; 12P4167) to AB. NCBS also provided funds for the open access fee. AB acknowledges support of the Department of Atomic Energy, Government of India, under 472 project no. 12-R&D-TFR-5.04-0800. Finally, we would like to thank the reviewers, D.R. Smith and N. Dahanukar, for their useful comments and suggestions.
Collection locality information
Data type: Excel spreadsheet
Explanation note: Abbreviations as follows – Type of data: Author’s observation (1), Photo from website (2), Publications (3), Personal communication (4). Source of Information: Authors’ initials- Chet Prasad Bhatta (CPB), Gard Williams Otis (GWO), Karsing Megu (KM), Nyaton Kitnya (NK), M.V. Prabhudev (MVP), Thai Hong Pham (THP), Tsering Nidup (TN); Organizations and Museums: Nagaland Beekeeping and Honey Mission (NBHM), Natural History Museum United Kingdom (NHMUK), National Museum of Natural History, US (USNM), Rijksmuseum of Natural History, Leiden, the Netherlands (RNH).