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Aim: Morphometric study of dwarf honey bees had been undertaken from five physiographic zones of Northeast India. Methodology: Bee samples were collected randomlyfrom various agro-ecosystems. 26 morphometric traits were measured under stereoscopic zoom microscope for morphometric study. Multivariate statistical analysis were used to investigate population variations and relationship between the groups. Results: Two species of dwarf honey beesviz. Apis florea and Apis andreniformis were identified. The average body length of A florea was 8.126±0.01 mm with average hamuli number of 12.150±0.07. In A. andreniformis the average body length and hamuli number were 6.940±0.08 mm and 10.467±0.03 respectively Cubital index in A. andreniformiswas 5.214±0.03 while 2.491 ±0.07 in A. florea. Interpretation: Principal component analysis accounted for82.184% of the total morphological variation. A. florea formed two morphoclusters viz., plain landraces including Brahmaputra valley and Barak valley and hill landraces including Arunachal Himalaya, Meghalaya Plateau and South eastern hill tract where they tend to cluster morphologically. Locally distributed species may be under future threat of extinction, due to changes in agricultural practices and climate change. The untapped native bee species are required to be documented properly in order to utilize the potentiality of these resources forthe sustainable utilization and economic prosperity of the region.
Abstract
Aim: Morphometric study of dwarf honey bees had been undertaken from five physiographic zones of Northeast India.
Methodology: Bee samples were collected randomlyfrom various agro-ecosystems. 26 morphometric traits were measured under stereoscopic zoom microscope for morphometric study. Multivariate statistical analysis were used to investigate population variations and relationship between the groups.
Results: Two species of dwarf honey beesviz. Apis florea and Apis andreniformis were identified. The average body length of A. florea was 8.126+0.01 mm with average hamuli number of 12.150+0.07. In A. andreniformis the average body length and пати! number were 6.940+0.08 mm and 10.467+0.03 respectively Cubital index in A. andreniformis was 5.214+0.03 while 2.491+0.07 in A. florea.
Interpretation: Principal component analysis accounted for 82.184 % of the total morphological variation. A. florea formed two morphoclusters viz., plain landraces including Brahmaputra valley and Barak valley and hill landraces including Arunachal Himalaya, Meghalaya Plateau and South eastern hill tract where they tend to cluster morphologically. Locally distributed species may be under future threat of extinction, due to changes in agricultural practices and climate change. The untapped native bee species are required to be documented properly in order to utilize the potentiality of these resources for the sustainable utilization and economic prosperity of the region.
Key words: Apis species, Dwarf honey bee, Morphometric analysis, North-east India, Physiographic zones
Introduction
Bees are among the most remarkable organisms on the planet. They are regarded as vital providers of ecosystem services and play an essential role in terrestrial ecosystems. Approximately, 17,000 species of bees have been identified, classified into 425 genera, 22 subfamilies and 6 families (Michener, 2000; Bingham, 1897). Based on the morphological traits, Ruttner (1995) categorized honey bees into four species: the European honey bee (Apis mellifera), the eastern honey bee (Apis cerana), the giant honey bee (Apis dorsata), and the dwarf honey bee (Apis florea). Dwarf honey bees are effective pollinators of numerous economically important crops and forest plants, and they have an extensive foraging range. (Wongsiri et al., 2000). The red dwarf honey bee (Apis florea) is the most widespread species of dwarf honey bees, naturally found in the Indian subcontinent to the Malay Peninsula. The black dwarf honey bee (Apis andreniformis) is rarer and is distributed across regions from the Philippines to China and Myanmar (Oldroyd and Wongsiri, 2006; Hepburn and Radloff, 2011).
Together, Apis florea and Apis andreniformis form the subgenus Micrapis, representing the most primitive species within the genus Apis. Although both species live in a single exposed comb, they differ in terms of morphology, behavior and natural history. The workers of Apis florea typically have a reddish-brown (rufous) color whereas Apis andreniformis is darker, with the first segment of its abdomen being entirely black (Wu and Kuang, 1987). Both species are key pollinators in the semi-arid to tropical regions across various parts of Asia and Africa. They are highly effective in pollinating orchard and field crops, such as oilseeds, vegetables, fruits, and condiment plants. (Sihag, 2019). Northeast India is recognized as a hotspot for both faunal and floral biodiversity. There is a growing need for detailed studies on pollinator diversity, particularly regarding insect pollinators. Recently, many bee species have experienced significant declines in both abundance and distribution (Tahmasebi et al., 2002; Cameron et al., 2011).
The causes are not fully understood, but they are likely linked to pathogen spillover from commercial breeding practices, as well as changes in the agricultural methods and land use (Cameron et al, 2011; Jacobson et al, 2018). Additionally, climate change threatens numerous bee species globally, particularly those adapted to high-altitude environments, as suitable habitats continue to decrease (Hoiss et al., 2012; Kerr et al, 2015). Therefore, it is crucial to properly document the region's untapped native bee species to harness their potential for sustainable use and economic development. Morphometric studies are essential for both species identification and studying variations within populations. Morphometric analysis offers a quick, cost-effective and field-friendly method for identifying new species. It has proven to be a valuable tool for revealing both intraspecific and interspecific relationships (Amssalu et al, 2004). To date, no research has focused on the morphometric characterization of dwarf honey bees across different altitudes in the North-east India. In light of the above, aim of this study was to assess the morphometric characteristics of dwarf honey bee species, comparing their characters across five physiographic zones of North-east India, while also studying their foraging sources and preferences among available floral resources under varying climatic conditions and altitudes.
Materials and Methods
Sample collection: North-east India is situated at 25.5736° N and 93.2473° E within the Indian subcontinent. A comprehensive study of dwarf honey bee species was conducted across five physiographic zones in the North-east India, namely the Arunachal Himalaya, Barak Valley, Brahmaputra Valley, Meghalaya Plateau, and the Southeastern Hill Tract. Each zone was further divided into various locations based on GPS coordinates (Table 1; Fig. 1). Bee samples were collected from plants while they were foraging for nectar or pollen using a nylon cloth sweeping hand net, and a few samples were obtained directly from bee colonies. The sampling method primarily involved random sampling across different agro-ecosystems. In addition to the collection, live photographs were taken with a Nikon D5200 camera equipped with various macrolenses. The collected samples were initially sorted in the field and then brought to the laboratory for further identification and analysis. The coordinates (latitude and longitude) and elevation of each sampling site, as well as information on the bee foraging sources, were recorded to gather ecological data on the species. After field collection, the specimens were dry-mounted on standard insect pins for identification, while the remaining specimens were preserved in 75% ethanol to prevent deformation. The relative abundance of the dwarf honey bee species was evaluated to determine how common or rare a species is in comparison to others at a specific location. It was calculated by dividing the number of species in one group by the total number of species in all groups. The result was then multiplied by 100 to express itas a percentage.
Pasturage sources: In-situ observations were conducted while bees were foraging on plants to identify the foraging sources of nectar and/or pollen. Aplant was considered a nectar source if the bees inserted their proboscis into the flower for nectar, and a pollen source if the corbiculae became loaded with pollen during foraging. When both behaviors were observed on the same plant, it was regarded as a source of both nectar and pollen. The types of plants observed included field crops, fruit crops, ornamental plants, vegetable crops, plantation crops, medicinal and aromatic plants, trees and weeds.
Species identification: The dwarf honey bee species were examined under Leica MZ-165 stereoscopic zoom dissection microscope with a DC-300 digital camera system and identified using standard taxonomic keys (Bingham, 1897; Michener, 2000; Hepburn and Hepburn, 2005). The most reliable characters adequate for identification of A. florea and A. andreniformis are: the "thumb" of the bifurcated basitarsus of the hindleg of drones of A. florea is much longer than that of A. andreniformis (Ruttner, 1988); differences in the structure of the endophallus (Lavrekhin, 1935; Wongsiri et al., 1990; Koeniger, 1991); in worker bees, the jugal-vannal ratio of the hindwing of A. florea is greater (about 75) than that of A. andreniformis (about 65); and the cubital index of A. florea (about 3) is significantly less than in A. andreniformis (about 6). The marginal setae on the hind tibiae of A. florea are usually entirely white, those of A. andreniformis dark-brown to blackish in sclerotized individuals. Permeating the older literature is the idea that abdominal tergites 1 and 2 of A. florea are reddish and other segments at least partially reddish, while those of A. andreniformis are uniformly black (Hepburn et al., 2005).
Morphometric study: Ten specimens from each location were taken for morphometric studies. Various body parts like wing, legs, sterna, mouth parts (mandibles) etc., were dissected after boiling in 10% KOH solution for 2-3 min. The morphometric characters were selected based on the morphometric studies carried out by Ruttner, 1988; Amssalu et al., 2004; Hepburn et al. 2005. A total of 26 morphometric characters were measured after dissecting the bees and images were analyzed by a Leica MZ165 stereoscopic zoom dissection microscope with a DC-300 digital camera system.
Statistical analyses: Multivariate statistical analysis, Le., Principal Component Analysis, Canonical Discriminant Analysis and Cluster Analysis were used to investigate population variations and relationship between the groups. All the statistical analyses were done by SPSS 20.0 statistical package.
Results and Discussion
In the current study, two species of dwarf honey bees, Apis florea Fabricius and A. andreniformis Smith, were identified. A. florea was found in all five physiographic zones whereas A. andreniformis was recorded in three zones: the Barak Valley, the Brahmaputra Valley and the Meghalaya Plateau. The relative abundance of Apis florea was found to be highest in the SouthEastern Hill Tract (1) and Arunachal Himalayas (1), followed by Meghalaya Plateau (0.937), Barak valley (0.830) and Brahmaputra valley (0.736) whereas the highest relative abundance of Apis andreniformis was recorded from Brahmaputra valley (0.264), followed by the Barak valley (0.169) and the lowest from the Meghalaya plateau (0.063) (Table 2). Abrief description of the dwarf bee species is as follows:
Apis florea Fabricius (1787): Worker beeswere reddish-brown (rufous) in appearance; basal two abdominal segments were black; the pubescent on head and thorax were generally white; pale yellow to white hairs on the hind tibia and basitarsus; narrow transverse band of silky white pile at the base of the 2" to 5" abdominal segments; wings hyaline and iridescent. In drones, the "thumb" of the bifurcated basitarsus of the hind leg was long. The average body length of A. florea was 8.126+0.01 mm with cubital index of 2.491+0.07. The average пати! number of 12.150+0.07 was recorded in A. florea.
Apis andreniformis Smith (1858): Workers were generally black; contained few rufous workers; black hairs on the hind tibia and basitarsus; white pilose transverse bands at the base of the 2" to 6" abdominal segments; wings hyaline were observed. In drones, the "thumb" of the bifurcated basitarsus of the hind leg was short. The average body length of A. andreniformis was 6.940+0.08 mm with cubital index of 5.214+0.03. The average hamuli number of 10.467+0.03was recorded in A. andreniformis.
Morphometric study of dwarf honey bees: Comparative morphometric study of dwarf honey bees revealed that the body length of Apis florea varied from 7.943+0.02 mm to 8.294+0.01 mm with an average of 8.126+0.01 mm, while the body length of A. anderniformis varied from 6.883+0.05 mm to 7.030+0.04 mm with an average body length of 6.940+0.08 mm (Table 3; Fig. 2 a,b). The current results closely align with those of Halling et al. (2001), who reported that the average body length of A. florea in India was 9 mm. Distance between ocille (0.223+0.01 mm), ocille ocular distance (0.345+0.09 mm), antenna length (2.584+0.01 mm) and mandible length (0.989+0.13 mm) were more in A. florea compared to A. andemiformis, where itwas recorded to be 0.182+0.6 mm, 0.327+0.01 mm, 2.456+0.01 mm and 2.456+0.01 mm, respectively (Fig. 2 c, d). Thadsanee et al. (2004) reported that the mean antennal length of Apis florea from Thailand was 2.180.087 mm. The proboscis was recorded to be longer in A. andreniformis (2.612+0.03 mm) than A. florea (2.224+0.01 mm). The fore wing and hind wing length were recorded to be longer in A. florea (5.821+0.01 mm and 4.525+0.06 mm) compared to A. andreniformis (5.749+0.01 mm and 3.997+0.02 mm). The present findings are in conformity with Ruttner (1988) who recorded the forewing length of A. florea varied between 6.0 to 6.9 mm. Comparable results were reported by Makhoor and Ahmad (1998), who found the average forewing length and hindwing length of A. florea in the Jammu region to be 6.25 mm and 4.25 mm, respectively. The hamuli number in A. florea ranged between 10 to 13 with an average of 12.150+0.07, while in A. andreniformis it varied between 8 to 11 with an average of 10.467+ 0.03 (Fig 2 д, h). The cubital index differed significantly in both the species. Cubital index in A. andreniformis was recorded to be 5.214+0.03, while 2.491+0.07 in A. florea. Wongsiri et al. (1990) found that the cubital index of A. andreniformis (6.37) was significantly higher than that of A. florea (2.86). They also noted that the number of hamuli in A. florea ranged from 10.5 to 13.2, while in A. andreniformis it ranged from 10.38 to 10.88. Patil et al. (2014) reported that the number of hamuli in A. florea ranged from 10.00 to 11.00, with an average of 10.71 + 0.46. The femur and tibia were found to be longer in A. florea (1.351 + 0.0 mm and 1.603 + 0.02 mm) compared to A. andreniformis (1.241 + 0.03 mm and 1.415 + 0.01 mm). The lengths of the third sternite, wax plate, and apical tergum were quite similar in both species. Proboscis length is considered an indicator of geographical variation in some studies (Marghitas et al, 2008). Additionally, body measurements may have correlations with honey yield. Szabo and Lekovich (1988) found significant positive correlations between honey production and both fore and hind wing area. Kolmes and Sam (1991) reported that honey production was strongly correlated with overall size, corbicular area, and wing measurements in honey bees. As a result, body characteristics can serve as indirect indicators of colony productivity or be used for selecting productive bees, as those with larger legs and wings tend to have greater flight power, allowing them to collect more pollen and nectar for brood rearing, thus supporting a larger colony population. Edriss et al. (2002) indicated that honey production could be enhanced by selecting forewing width. Similarly, Mostajeran et al. (2006) showed that honey production was associated with proboscis length, forewing length and width, hindwing length, leg length, femur length, tibia length, and metatarsus width. Therefore, there is a clear evidence that morphological body traits are important and correlated with the productive capabilities of the colony. Both A. florea and A. andreniformis construct nests consisting of a single exposed comb. The brood area is located below the supporting branch, while the honey storage area is positioned above and around the branch. The nests of A. florea are generally larger than those of A. andreniformis. The brood area of A. andreniformis has a height of 10.03 + 3.29 cm and a width of 12.18 + 3.62 cm, which is approximately 25% smaller in height and 16% smaller in width compared to the brood area of A. florea, which measures 12.00 + 3.32 ст in height and 16.85 + 5.28 cm in width (Wongsiri et al., 1997). A. florea nests are typically found in more disturbed environments, such as urban and intensive agricultural areas. These bees often use small branches as a support for their nests, which are usually located in shaded spots. However, their nests are more exposed to sunlight, with the comb surface often exposed to direct sunlight for several hours each day. A. florea is also more likely to nest in a variety of locations, including high in tall trees, on building walls, or on building roofs. Their nesting height ranges from 1 to 15 m above the ground in dry evergreen forests. In contrast, A. andreniformis nests are typically found in undisturbed, mixed deciduous to evergreen forests, usually in dark and shady areas (20-35% sunlight), often near or over streams. These bees build their nests on small branches of shrubs, bamboos, bananas, or small trees, with a single, relatively small comb located between 0.7 and 9.0 m above the ground (Wongsiri et al., 1997).
In the current study, 69 plant species from 29 families were identified as forage sources for Apis florea, while 43 plant species from 13 families were identified as forage sources for Apis andreniformis across different physiographic zones of North-east India (Table 4). Layek et al. (2014) examined the foraging behavior of Apis florea during winter and spring-summer in West Bengal, identifying 71 plant species from 32 families as forage sources. Previous studies have reported varying numbers of food plants for Apis florea: 119 species by Sharma and Gupta (1993), 140 species by Bhat et al. (1990), 43 species by Kuberappa et al. (1996), 172 species by Singh et al. (2002), and 260 species by Padmanabhan and Sujana (2007). The economic importance of Apis andreniformis is not well documented; however, it is likely that many plants within its range rely on this species for pollination (Rattanawannee and Chanchao, 2011).
Principal component analysis of dwarf honey bees was conducted using 26 morphometric parameters, with 19 of these parameters showing significant contribution to the variation in the bee population. The analysis grouped the components into four categories, each containing a common variable that is influenced by factors with an eigenvalue greater than one.The first component accounted 52.997% of the total variation and was primarily associated with antenna length, hind wing width, third sternite length, metasoma length, distance between ocelli, wax plate width, femur length, tibia length, apical tergum width, head width, and mandible width. The second component, which accounted for 13.079% of the variation, was influenced by the width of the third sternite, head length, apical tergum length, hamuli number, wax plate length, and hind wing length. The third component explained 9.856% of the total variation and was mainly linked to meta-tarsus length, body length, cubital index, mandible length, and mesosoma length. The fourth component accounted for 6.252% of the variation, with key associations to proboscis length, forewing width, forewing length, and the distance between the ocelli. Together, these four components accounted 82.184% of the total morphological variation among the dwarf honey bees from different physiographic zones. (Table 5).
Cluster and discriminant analyses indicated that Apis florea from five physiographic zones formed two distinct morphoclusters: the plain landraces, which included the Brahmaputra and Barak valleys and the hill landraces, which included the Arunachal Himalaya, Meghalaya Plateau, and Southeastern Hill Tract, where they tended to cluster morphologically (Fig. 3, 4). The dendrogram, constructed using the average linkage method based on sampling locations, revealed two main clusters, A and B. Cluster A consisted of A. andreniformis from the Brahmaputra Valley, Barak Valley and Meghalaya Plateau (Fig. 5). Cluster B was divided into two subclusters, B, and B,. Sub-cluster B, was further split into two subclusters, B,, and B,,. Sub-cluster B,, included A. florea from the Barak Valley, while sub-cluster B,, included A. florea from the Brahmaputra Valley. Likewise, sub-cluster B, was divided into sub-clusters B,, and B,,. Sub-cluster B,, included A. florea from the South-eastern Hill Tract, while sub-cluster B,, comprised A. florea from the Arunachal Himalaya and Meghalaya Plateau. Singh et al. (1990) identified three biometric groups in the Eastern Himalayan region: Manipuri bees, Brahmaputra Valley bees, and Himalayan bees. Hepburn et al. (2001) also found morphoclusters linked to physiographic differences, which contributed to partial temporal reproductive isolation associated with altitude. Rattanawannee et al. (2007) studied the morphometric and genetic variation of small dwarf honeybee Apis andreniformis in Thailand and reported that factor and cluster analyses of 20 key morphological traits grouped all sampled A. andreniformis from Thailand and Malaysia into a single cluster. Populations of A. florea and A. andreniformis appear to be steadily declining, primarily due to habitat loss, excessive and indiscriminate pesticide use, and forest fires (Potts et al., 2010). Therefore, it is crucial to find effective ways to protect these species. Both are under significant environmental stress, yet they play a vital role in pollinating both cultivated and wild plants. They are essential for agricultural productivity and for maintaining natural ecosystems and their biodiversity.
Locally adapted strains, subspecies, and ecotypes of honey bees generally experience lower losses than non-native bees. As a result, conserving these native strains as genetic resources for breeding disease- and stress-resistant lines is critical. Additionally, a comprehensive understanding of the origin and distribution of these bee species is vital to uncovering how and when these adaptations developed. Studying the evolutionary relationships of these bees would lay the groundwork for behavioral studies within an evolutionary context, helping to explain the origin of complex social behaviors, such as the use of dance and sound to communicate the location of food or shelter. Furthermore, a global phylogenetic analysis would provide insights into divergence times and the ancestral biogeographic distributions of major bee groups.
Acknowledgments
The author takes the privilege to express his deep sense of gratitude to AICRP on Honey bees and Pollinators, Department of Entomology, Assam Agricultural University, Jorhat for providing necessary facilities and scientific help during the experiment.
Authors' contribution: R.R. Taye, A. Rahman and M.K. Deka: Conceptualization of the work, conducted experiments, analysis of data and preparation of manuscript; S. Borkataki and R. Saikia: Analysis of data and preparation of manuscript; A.S.N. Zaman, M.R. Choudhury, P. Khan, D. Bordoloi and N. Kakati: Preparation of manuscript, revision and proof reading.
Funding: Notapplicable.
Research content: The research content of manuscript is original and has not been published elsewhere.
Ethical approval: Not applicable.
Conflict of interest: The authors declare that is there is no conflict of interest.
Data availability: Data are presented in tabular manner within the research article.
Consent to publish: All authors agree to publish the paper in Journal of Environmental Biology.
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