Open access peer-reviewed chapter
Abstract
Stingless bees are one of the social bees that are spread across tropical and subtropical countries, including Indonesia. Indonesia has 46 species of 10 genera, and they are endemic in at least three distinct areas. Some species live in specific microclimates and environmental conditions; for example, Wallacetrigona incisa lives in the mountainous highlands of Sulawesi. It has many variations of nest architecture and places of nesting from natural habitats to residential environments that provide food plant sources of a variety of wild to cultivated plants. Stingless bees have a small body size, small honey pots, and limited foraging range and forage for more in short plants. In general, the forage distance and flight distances are correlated with the body size. The role of bees in nature is very important as pollinators and pray for protected wildlife and other insect eaters. Stingless bees also produce the products honey and propolis that are useful for humans. Indonesian meliponiculture provides benefits to the community but requires caution for the preservation of bees in their habitat. The transfer of colonies of stingless bees between islands and altitudes have caused many colony deaths and could not produce well. Conservation regulation is the solution.
Keywords
- diversity
- distribution
- nesting
- foraging
- meliponiculture
1. Introduction
Besides honeybees (
At least fifty species are known to belong to the Southeast Asia region [2, 3], out of 46 species of stingless bees that have been recorded in Indonesia that were recently grouped into 10 genera, namely Austroplebeia (1 sp.), Geniotrigona (2 spp.), Heterotrigona (10 spp.), Homotrigona (8 spp.), Lepidotrigona (6 spp.), Lisotrigona (1 sp.), Papuatrigona (1 sp.), Pariotrigona (1 sp.), Tetragonula (15 spp.), and Wallacetrigona (1 sp.) [4, 5, 6, 7]. The main of those species are only found in Indonesia or neighboring countries in the same geographic region [4, 8, 9]. Of the species recorded, most of them were collected on the islands of Sumatera and Kalimantan [7], although sampling bias toward the western rather than the eastern islands may obscure the true pattern of distribution and diversity. Nonetheless, we have found an inline between the distribution of stingless bees’ species and the known bioregional complexes of plants and animals.
Indonesia has a lot of naturally complex environmental conditions with macro and microclimates, topographical and other physical environments under complex geological history [10]. At least under the three biogeographic regions of the Indo-Malayan, Wallacean, and Australasia regions on the terrestrial ecological map [11], Indonesia has various species richness and high endemicity of plants and animals [12, 13, 14, 15], also stingless bees are in accordance with these facts [7]. There is a pride fact in the distribution of the genus which is only restricted discovered on a certain island or regions, for example, genus
2. Distribution and endemic species in Indonesia
Stingless bees’ distribution globally has been categorized into four tropical regional groups, namely Neotropical, Afrotropical, Australasian, and Indo-Malayan [1, 9, 20, 21, 22]. In the tropical country of Indonesian archipelago, from the west to the east of the country are stretched tens of thousands of islands. The distribution of the stingless bee species is categorized as [10] explaining the complex geological history of Indonesia; the country is grouped into at least three major regions namely Indo-Malayan, Wallacean, and Australian tropical regions with different species endemics [7, 9, 23, 24]. The high species richness and uniqueness of stingless bee distribution in Indonesia may be related to the country’s vast geographic expanse, diverse topological and environmental landscape, and complex geological history. There are at least 46 species of 10 genera of stingless bees recorded in Indonesia, spread across the archipelago. Starting from the west to the east of the islands, species of stingless bees have high endemicity, the westernmost being the islands of Sumatera (23 species), Java (7 species), Borneo (29 species), Timor (1 species), Sulawesi (3 species), and Ambon (2 species), and to the east is Irian Jaya (Indonesian Papua) (9 species) [7]. Species diversity, although dominated on the islands of Sumatera and Kalimantan, both of which are in the Indo-Malaysia region, most of which are not found in other regions [7, 21, 24], the same thing with the species of stingless bees found in the Indo-Australian region [4, 6, 7, 25, 26]. The species richness of stingless bees between the western and eastern regions gives an interpretation as if the diversity of stingless bees in eastern Indonesia is low, but if exploration is carried out more intensively, it is not impossible to find more species in eastern Indonesia.
The occurrence of the species
Eight species of stingless bees have been recently recorded in Sulawesi Island and surrounding small islands.
Figure 1.
Stingless bee species distribution map in three tropical regions of Indonesia [
3. Nest architecture and nesting behavior
The nest architecture of stingless bees has a basic structure that differs in shape, size, and appearance, which is also determined by microclimatic factors, availability of resin sources, colony age, and natural antagonists. Nest architecture could be utilized as a potential species identification tool [16, 18, 19, 33, 34]. Stingless bees build nests with several materials including resin, gums, plant exudates, and the stingless bee worker waxy secretions. All of these materials are mixed by worker bees known as cerumen [1, 34]. The composition of cerumen on the nest of
Stingless bees do not have an ability for digging solid objects, so they always use cavities of dead and living trees, soils, man-made structures like walls or cracks of buildings, drainage pipes, and poles, among others, or other materials with cavities [34, 36]. In Malaysia, stingless bee nests can mostly be found in rock crevices, underground cavities, and tree trunks or branches [37]. In Halmahera Island, it can be found in bamboo segments, logs, part of houses (part of roof, wall, and keyhole of the door), stone cavity, tree trunk, root of tree, foundation, wooden materials, furniture, electricity, iron cavity, and also over the land [28]. Stingless bees have distinct geographical distribution and nesting sites, inhabiting living and dead tree cavities, rock crevices, land, anthills, and termite nests [16]. The nests can be found under the surface of soil cavities, tree holes, wood cavities, hollow bamboo trees, and in gaps in the walls around the house [4, 38, 39, 40].
The nest of stingless bees consists of entrance, storage pots, and brood cells, which can be distinguished into outer and inner entrance, pollen and honey pots, and young and mature brood cells. Other important parts of stingless bee nests are completed with cerumen, batumen, and involucrum. Cerumen is a mixture of propolis (resin) and wax to construct storage pots and brood cells. Batumen consists of resin or wax as a layer of cavity nest [41]. Various shapes of batumen act as supporting parts of the nest to protect from sunrise, predators, and intruders [39, 42, 43]. The shape, color, hardness, and adhesiveness of the parts of the nest depend on the availability of the surrounding material.
Additional structures and shapes of the entrance are affected by environmental conditions, for example, its natural enemies, temperature, humidity, and wind speed. Growing colonies usually have rudimentary forms as part of the nests, for example, semi-spiral or semi-cluster brood arrangements before becoming spiral or cluster forms. Although many forms of the entrance are short because they are not yet developed, there are species of stingless bees that do not appear to have an entrance protrusion because it is only a hole whose surface is covered with resin. On the other hand, the nest entrance of
General brood comb constructions on stingless bees are spiral, stacked, layered, and clustered [44].
Honey pots are generally oval, vertical, or rounded in shape and vary in size. In honey pots that are large, the honey can be harvested by sucking it, and conversely, the small ones are squeezed out. Within their nests, the bees deposit honey, pollen, and propolis, and all of these are exploited by humans [7]. Honey pots are usually located adjoining the nest entrance. Pollen pots are situated close to the broods, so feeding the chicks can be done more easily, and they also store food as honey, which can be exploited sustainably by humans.
Stingless bees, which are small, have adaptations to various small cavities in houses and buildings, including narrow doorways, foundations of house walls, and other cavities around the house, and those small cavities are likely as a trigger to the colonies to carry out the colony splitting (Figure 2).
Figure 2.
Nesting preference of Stingless Bees in West Halmahera. A. Cavities in house parts; B. Cavities in walls of buildings; C. Cavities in oorways; D. Cavities in the foundation of a house; E. Cavities in an iron; F. Cavities in electric meter.
4. Foraging behavior
Stingless bee workers are responsible for collecting resources, such as pollen and nectar, along with materials to build and protect the nest [1, 38]. Stingless bees actively fly from morning to evening on sunny days [46]; however, stingless bees first out of the nest later and last enter the hive quicker than honeybees [47]. Unlike honeybees, stingless bees forage randomly searching for food and resin sources without being guided by their senior bees. Every species of stingless bee has preferences for food resources, so they have different behaviors in foraging. Stingless bee workers, responsible for colony nursing, feed the larvae by putting food in incubation cells before the eggs are laid by the queen [48]. In general, the forage distance and flight distance of bees correlate with the body size; the bigger the body size, the longer the foraging and flying distance of bees.
The main species of stingless bees in Indonesia are small, which affects the limited flight range of bees in finding food. Unlike honeybees, in search for food, who are primarily guided by the senior workers, stingless bees individually and freely choose to take the material of the nearest distance from the colonies, as shown in the species
Like other groups of bees, stingless bees have a mutually beneficial interaction with flowers. Flowers provide food for bees in the form of nectar and pollen, and bees help attach pollen to the stigma so that both the survival of the bees and plant reproduction are guaranteed. Physical environmental features such as the temperature and humidity affect foraging behavior [50]. Stingless bees diligently perch on flowers until they are finished picking the ingredients they want [51, 52].
Stingless bees are generalist pollinators, and their role is evident in cross pollination. Stingless bees are small, so they can forage on small flowers without causing damage and can also take food from hidden flower parts that are not visible by other larger bees. Stingless bees are often seen foraging on large flowers, which are visited by larger bees, birds, and bats [53]. Pollen analysis shows that stingless bees collect pollen of various shapes, sizes, colors, and odors. Stingless bees frequently also visit flowers that are dull and musty in smell, typical of beetle and fly flowers; however, in a heterogeneous environment, stingless bees tend to choose flowers more typical of bees [53]. The high preference of stingless bees to collect nectar from short wild plants, which are commonly used as traditional medicinal plants, cause stingless bee honey to be used more as “jamu” or herbal medicine.
Stingless bees have the behavior of using various resins to protect the nest and make it difficult for predators to enter the nest. The sticky resin and slippery sand around the entrance are used to repel and trouble insect intruders. This type of protective resin varies depending on the environment in which the stingless bees’ colony originates.
Stingless bees exhibit defensive behavior when their colony is disturbed by animals and humans by ganging up and biting. Species that have relatively high aggressiveness compared to the other are
Stingless bees have a small body size, small honey pots, and limited foraging range and forage more for short plants. This range enables the stingless bee to visit fewer and different types of flowers. However, stingless bees have another advantage in that they do not rely solely on mass flowering plants. All these reasons cause stingless bees to produce less honey than honeybees. Stingless bees can visit small flowers that larger bees cannot; however, they are able to visit large flowers.
The mature queen is not able to change the nest by flying due to her body being disproportionately fat. Unlike honeybees, who conduct long and short migrations to find abundant food resources [54, 55, 56], stingless bees do not so but only coduct a short movement during a new queen swarming.
Stingless bees have the capability to protect the colony from natural predators and disturbances by using sticky resin around the entrance and weak parts of the nest targeted by intruders [57]. Stingless bees also construct additional configurations to protect the nest from intruders and natural enemies [33]. The highland endemic species of Sulawesi
5. The benefit of Stingless bee
The archipelago country of Indonesia has very diverse natural ecosystems [58] that grow a huge number of wild and agricultural flowering plants, whose biodiversity has been well recorded at least in the islands of Java, Kalimantan, Sumatra, Papua, Sulawesi, Moluccas, and Lesser Sunda Islands [59]. As an agricultural country, a lot of flowering plants grow in various natural and agricultural systems [60] that exhibit diverse flower morphology, biology, and phenology [12, 61, 62], of those require various pollination by the flowers themselves, intermediary by wind, water, and animals [53, 63, 64, 65]. As a part of eusocial bees, stingless bees are potential and efficient pollinators among insects and other animal pollinators, as they visit diverse flowers, and therefore, as potential and efficient pollinators [1, 63, 65, 66, 67], they play an important role in ecosystem services in the tropics.
The ecosystem would not be able to maintain its stability without the contribution of bees. Bees serve an important function as pollinating insects [67, 68]. Without bees, the delicate balance of the ecosystem will be thrown off, which will have repercussions for many aspects of life [69]. Stingless bees have a significant value because they are the primary pollinators of both wild flowering and cultivated plants. As a result, they play an essential role in the preservation of biodiversity and the safety of food supplies. Another fantastic application for stingless bees is crop pollination. It is estimated that almost two-thirds of all cultivated plant species rely on bee pollination to bear fruits and seeds. Currently, honey production is the primary goal of meliponiculture, but crop pollination will require a significant number of colonies in the future and will most likely become the primary goal of the activity. Stingless bees can be readily managed to boost pollination and productivity of a variety of crops, including coconut, strawberry, tomato, and coffee. Bees pollinate many wild and cultivated flowers in addition to producing honey. According to [70], animal pollination accounts for around 35% of global food production volume, with [71] adding that this figure can rise to 78% in temperate zones and 94% in tropical areas. Many plants, including Arecaceae, Cucurbitaceae, and Solanaceae, have been reported to benefit from stingless bee pollination. Furthermore, stingless bees have been shown to be major pollinators of non-crop species in their natural environments [67]. According to reports, pollination activities are reducing as bee populations dwindle. The significance of bees as the primary pollinators of a wide range of wild flowering plants as well as almost 70 percent of all cultivated plants is acknowledged on a global scale [72].
In many areas of the world, stingless bees have been cultured in colonies and product management of meliponiculture [68, 73, 74], and it has been developed rapidly and spawned major industries as well as profited indigenous people who often have historical and important cultural practices associated with stingless bees [75].
Stingless bees collect nectar, pollen, and resin mainly from plants, of which the material in their nest cavities is stored as honey, bee bread, and propolis. Deposits of honey and bee bread in the nest are stored food, which will be consumed in the next lean season. Stingless bees mainly produce honey and propolis; the honey has a sour taste and is sometimes bitter [76]. This taste is the main reason why stingless bee honey is not the main choice for the public or inland people who live in the forest, who instead choose honey from honeybees (Kahono et al. unpublished data). Since ancient times, honey from stingless bees has been well known as a traditional medicine; however, they never carried out stingless beekeeping practices. Almost all species of stingless bees are targets for honey hunting. People gather honey from the wild and near their house. Initially, stingless bee honey was not found for sale in shops, only being sold by limited stingless bee breeder communities. Meliponiculture is the practice of raising stingless bees. These bees are raised primarily for their honey, which they store in cerumen pots, making it quite simple to extract [77], as well as for other valuable hive products such cerumen, propolis, and pollen. Additionally, these bees create strange items that humans can use. Their honey is their best-known item. The water content of stingless bee honey is larger (about 30%) than that of ordinary
Stingless bee honey has a sour taste and sometimes bitter taste [76]. This taste is the main reason why stingless bee honey is not the main choice for the public. Initially, stingless bee honey was not found for sale in shops, only being sold by limited stingless bee breeder communities. Since the discovery of many bioactive medicinal compounds from honey and extracted propolis from various nest parts such as entrance, pots, involucrum, and others, that are good for human health, people have wanted to consume them. Stingless bee honey has anti-inflammatory, antimicrobial, anti-diabetic, skin aging delaying, antioxidant, hypolipidemic, anti-diabetic, and control and prevent infection. Numerous religious, nutritional, and commercial uses were also extracted from their hives [35, 79] which all have been imported as the high prices have increased public interest in stingless bees. In some cases abroad, stingless bees have a significant cultural and historical value because most of the products that are harvested from the hive are put to a diverse range of uses. Many indigenous and rural cultures place high importance on stingless bees culturally [80, 81, 82, 83].
All of the promoted wax, honey, and resin are still being researched and haven’t been used well in the country. Discovering many bioactive medicinal compounds from both honey and extracted propolis from various nest parts such as entrance, pots, involucrum, and others, is good for human health. Stingless bee honey has anti-inflammatory, antimicrobial, anti-diabetic, skin aging delaying, antioxidant, hypolipidemic, anti-diabetic, and control and prevent infection [35, 79, 84]. In some cases abroad, stingless bees have a significant cultural and historical value because most of the products that are harvested from the hive are put to a diverse range of uses. We do not discover in case of indigenous and rural cultures place a high importance on stingless bees culturally [80, 81, 82, 83].
The most sought-after stingless bee is the most commonly distributed species that is well adapted to human environments,
Stingless bees play an important role in the food chain as the food of wildlife. The flying and the flower-visiting bees serve as the feed of predatory animals, that is, spiders, centipedes, predatory insects (beetles, bugs, grasshoppers, flies, and ants), reptiles, amphibians, birds, and mammals [85].
Stingless bee nests attract a variety of predators due to their abundance of food resources and abundance of breeding sites [86]. Females of the assassin bug
6. Meliponiculture in Indonesia
Traditional people utilize bee colonies around houses, taking honey without throwing away the hives and retaining them in the natural tree cavities. The basis of being able to breed stingless bees is the bee’s life in a cavity that can be replicated with artificial boxes. Compared to honey beekeeping, maintaining stingless bee colonies and harvesting their productions is quite simple. Another advantage of stingless bees is that the bees have no sting so that maintenance is safe and harmless, making them friendly. Stingless bees have a high adaptation tolerance to environmental stress so that they usually survive a period of environmental stress so that they will develop again to enter the next good period.
Initial meliponiculture activity was raised by moving natural nests from forests and keeping them near residential, plantation, and agricultural lands. Furthermore, meliponiculture continues to develop semi-natural systems by adding wooden boxes for honey in the top of a colony in the natural tree trunk. Many of them move entire bee colonies from natural hives to new wooden or other artificial boxes [7, 88]. To imitate the artificial hives of honeybees, some local stingless beekeepers have made artificial honey pots so that the bees are efficient in time and energy to collect nectar and pollen.
In general, meliponiculture is usually carried out as a side activity by farmers, animal breeders, private workers, and government employees with a limited number of species and colonies. The first of the easiest to cultivate due to their wide distribution and high adaptation to various environments is
Although the size of the bees is related to the measure of honey production, however, a small species with a large amount of colony members of
Recently, the management of meliponiculture has been developed successfully in successive recent years. Many farmers have been doing it professionally with a greater number of species and bee colonies, as well as conducting bee ecotourism and selling bee colonies and beekeeping products.
Pest of natural colonies of stingless bees is not exposed properly due to the lack of research on it in the country. Flying bees in search for food resources become targets of insectivorous birds, and those that perch to collect the necessary material for the colony become targets of spiders, lizards, and chameleons. Large predators such as lizards, jumping spiders, and frogs stay near the nest entrance, watching in and out bees and catching them [33, 89].
Stingless bees are found in different countries and are adapted to the local ecosystem. Stingless bees can adapt to environmental changes (temperature, humidity, and rainfall) and changes in food sources within a few weeks to 3 months to form perfect colonies [90]. The transfer of colonies of stingless bees between islands in Indonesia and from the highlands to the lowlands on the island of Sulawesi has caused many colony deaths, and the colonies did not produce well [91].
Local peoples in the various regions of Indonesia have developed different methods of hives. Among the stingless bee species commonly cultivated in Indonesia are
As stingless bee honey production from culture is not documented and the intensity of taking wild colonies is very high recently, scattered evidence suggests that stingless bee honey from nature has played a significant role in the national honey production.
In the national production of honeybees, there are well-known honey producing regions [7, 92]. Some areas have been started to be stingless bee honey producers, for example, North Luwu district (South Sulawesi) that provides lots of honey and raw materials for advanced products, including propolis.
In contrast to the stingless bee, the development of its cultivation occurs faster due to its easy-to-handle nature and body morphology, which is suitable for a wide range of flowers. The advancement of meliponiculture is not limited to pollination and honey production for commercial purposes. In the concept of stingless beekeeping, beekeepers have moved further into the realm of health by pollinating medicinal plants. As a result, stingless bees have been producing more medicinal honey, propolis, and derivative products over the last decade.
Indonesia needs to develop beekeeping by enhancing the existing natural ecosystems and artificial green environments as a source of feed, as well as promoting stingless native bees through formal education and bee ecotourism.
Managed meliponiculture in Indonesia is definitely the ideal choice because it can be done in all types of green environments, and meliponiculture can be conducted by ordinary people safely, cheaply, and easily and with less maintenance [93]. Recently, beekeeping of local species of stingless bees has been growing significantly in every region across their distribution, progressively increasing the national production of medicinal honey, raw propolis, and derivative products.
Consumption of honey from apiculture and wild honeybee hunting is more common as a daily drink and supplement drink in Indonesia than stingless bee honey is, mainly for traditional medicine. As a result, stingless bee honey is mostly collected in the wild or raised in small quantities traditionally.
7. Conservation
Despite the importance of bees and many other pollinators, they are threatened by a wide variety of factors. These factors include the loss of habitat because of deforestation, wildfires, changes in land use, excessive use of pesticides, and climate change. These factors are causing alarming population declines, which will have severe consequences for ecosystems as well as the diet, health, and economies of people all over the world [81, 83]. Because of these factors, developing effective and permanent conservation strategies for stingless bees (and other pollinators) is an urgent matter [94, 95]. Beekeeping methods, land use conversion, pesticides, and changes in natural habitat are all variables that could impact bee populations [96].
Despite the significance of stingless bees, there are several dangers that are leading to alarmingly low population numbers. At the moment, the commerce of stingless bee colony was glow by move the endemic species to another endemic area, so it disturbed the natural distribution and guess of the bad side effect. Maybe the bees can survive at the area, but the bad side effect to local stingless bees was not researched. The bad effects that happen are the death of colonies on the trip, killed by natural enemies, the nest captured by other species [16], and instability of the native habitat because of the decreased ecological function caused by the takeover of the stingless bee colony.
The supervision of quarantine department needs to be increased to control the transportation of endemic species, especially those who get transported to other islands. The government needs to make an explicit regulation for the quarantine department about the conservation of endemic stingless bees.
8. Conclusion
Indonesia has various species of stingless bees that are spread throughout the Indonesian archipelago and are also endemic to at least three different regions. Wallacean island of Sulawesi has an endemic species of stingless bees, namely
Stingless bees are small bees that adapt to various sized cavities. In principle, in a good environment, all types of bees can be bred, although there is a tendency for breeders to choose superior types of bees. Stingless bees are important pollinators of the fruit crops and wild plants that are their food source. The most obvious advantage of stingless bees compared to honeybees is the production of raw propolis as the main ingredient in expensive liquid propolis,s which is important for human health.
Meliponiculture has begun to develop in Indonesia with a large number of colonies, although not evenly distributed. People conduct meliponiculture to improve their income. Moving colonies between islands and different environments is not recommended because it causes colonies to die and not develop. Likewise, the movement of endemic species to other endemic areas will disrupt their natural distribution and cause negative impacts. It is necessary to regulate the use of bees by considering their sustainability.
References
- 1.
Michener CD. The Bees of the World. 2nd ed. Baltimore: Johns Hopkins University Press; 2007. xvi+[i]+953 pp,+20 pls - 2.
Inoue T, Sakagami S, Salmah S, Yamane S. The process of Colony multiplication in the Sumateran Stingless bee Trigona (Tetragonula) laeviceps. Assoc Trop Biol Conserv Biotropica. 1984; 16 (2):100-111 - 3.
Sakagami S, Inoue T, Yamane S, Salmah S. Nests of the Myrmecophilous stingless bee, Trigona moorei: How do bees initiate their nest within an arboreal ant nest? Biotropica. 1989; 21 (3):265 - 4.
Dollin AE, Dollin LJ, Sakagami SF. Australian stingless bees of the genus Trigona (Hymenoptera: Apidae). Invertebrate Systematics. 1997;11 (6):861-896 - 5.
Sakagami SF. Tetragonula stingless bees of the continental Asia and Sri Lanka (Hymenoptera, Apidae). Journal of Faculty Science, Hokkaido University Zoology. 1978; 21 (2):165-247 - 6.
Rasmussen C, Thomas JC, Engel MS. A new genus of Eastern Hemisphere stingless bees (Hymenoptera: Apidae), with a key to the supraspecific groups of Indomalayan and Australasian Meliponini. American Museum Novitates. 2017; 3888 :1-33 - 7.
Kahono S, Chanatawannakul P, Engel MS. Social bees and the current status of beekeeping in Indonesia. In: Chantawannakul P, Williams G, Neumann P, editors. Asian Beekeeping in the 21st Century. Singapore: Springer Nature; 2018. pp. 287-306 - 8.
Sakagami SF, Inoue T, Salmah SM. Stingless Bees of Central Sumatra. In: Natural History of Social Wasps and Bees in Equatorial Sumatra. Sapporo, Jepang: Hokkaido Univ Press; 1990. pp. 125-137 - 9.
Rasmussen C, Cameron S. Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biological Journal of the Linnean Society. 2010; 99 (1):206-232 - 10.
Hill R. Southeast Asia’s changing palaeogeography. Blumea. 2009; 54 :148-161 - 11.
Olson D, Dinerstein E, Wikramanayake E, Burgess N, Powell G, Underwood E, et al. Terrestrial ecoregions of the world: A new map of life on earth. Bioscience. 2001; 51 (11):933-938 - 12.
Backer CA, Brink VDRCBJ. Flora of Java (Spermatophytes Only). Vol. Volume I. Groningen, The Netherland: NVP Noordhoff; 1963 - 13.
Backer CA, Brink VDRCBJ. Flora of Java (Spermatophytes Only). Vol. Volume II. Groningen, The Netherland: NVP Noordhoff; 1965 - 14.
Backer CA, Brink VDRCBJ. Flora of Java (Spermatophytes Only). Vol. Volume III. Groningen, The Netherland: NVP Noordhoff; 1968 - 15.
Maryanto I, Maharadatunkamsi D, Achmadi A, Sugardjito J. Checklist of the Mammals of Indonesia. Third Edit ed. Indonesia: Research Center for Biology-LIPI; 2019 - 16.
Suhri AGMI, Soesilohadi RCH, Agus A, Kahono S, Putra RE, Raffiudin R, et al. Nesting site and Nest architecture of Wallacea endemic Stingless bee species Tetragonula cf. biroi and Wallacetrigona incisa of Indonesia. Serangga. 2022; 27 (2):38-56 - 17.
Trianto M, Purwanto H. Diversity, abudance, and distribution patterns of stingless bees ( Hymenoptera meliponini ) in Yogyakarta, Indonesia. Biodiversitas. 2022;23 (2):695-702 - 18.
Suriawanto N, Atmowidi T, Kahono S. Nesting sites characteristics of stingless bees (Hymenoptera: Apidae) in Central Sulawesi, Indonesia. Journal of Insect Biodiversity. 2017; 5 (10):1-9 - 19.
Sayusti T, Raffiudin R, Kahono S, Nagir T. Stingless bees (Hymenoptera: Apidae) in South and West Sulawesi, Indonesia: Morphology, nest structure, and molecular characteristics. Journal of Apicultural Research. 2021; 60 (1):143-156 - 20.
Barbossa F, de Oliveira AR, de Almeida SB, de Carvalho C. Nest architecture of stingless bee Geotrigona subterranean (Friese, 1901) (Hymenoptera: Apidae: Meliponini). Biota Neotrop. 2013; 13 (1):147-152 - 21.
Sakagami S. Stingless Bees. In: Hermann H, editor. Social Insects. Vol. III. New York: Academic Press; 1982. pp. 361-423 - 22.
Oliveira F, Richers B, Silva J, Farias R, Matos T. Guia ilustrado das abelhas “Sem-Ferrão” das reservas Amanã e Mamirauá, Brasil (Hymenoptera, Apidae, Meliponini). Amazonas, Brazil: Instituto de Desenvolvimento Sustentável Mamirauá IDSM/OS/MCTI; 2013 - 23.
Rasmussen C. Catalog of the indo-Malayan/Australasian stingless bees (Hymenoptera: Apidae: Meliponini). Zootaxa. 2008; 1935 :1-80 - 24.
Kahono S. Diversity and the potency of Indonesian Native Bees. In: 14th Conference of Asian Apiculture Association (AAA), 22-25 October 2018. Jakarta, Indonesia: Indonesia Apicultural Association; 2018 - 25.
Engel M, Rasmussen C. A new subgenus of Heterotrigona from New Guinea (Hymenoptera: Apidae). Journal of Melittology. 2017; 73 :1-16 - 26.
Sakagami S. Stingless bees (Excl. Tetragonula) from the continental Southeast Asia in the collection of Berince P. Bishop Museum, Honolulu (Hymenoptera, Apidae). Journal of Faculty of Science, Hokkaido University Zoology. 1975; 20 (1):49-76 - 27.
Foundation TPI. Taxonomic and faunistic overviews on the insect species living in Papua and West-Papua (Indonesian New Guinea) [Internet]. 2019 [dikutip 2 Oktober 2019]. Tersedia pada. Available from: https://www.papua-insects.nl - 28.
Salatnaya H, Fuah AM, Engel MS, Sumantri C, Widiatmaka KS. Diversity, nest preference, and forage plants of Stinglesss bee (Hymenoptera: Apidae: Meliponini) from West Halmahera, North Moluccas, Indonesia. JITV. 2021; 26 (4):167-178 - 29.
Sakagami S, Inoue T. Stingless bees of the genus Trigona (Subgen: Geniotrigona) (Hymenoptera: Apidae) with description of T. (G.) incisa sp, nov. from Sulawesi. Japanese Journal of Entomology. 1989; 57 (3):605-620 - 30.
Rasmussen C, Cameron S. A molecularphylogeny of the old world stingless bees (Hymenoptera: Apidae: Meliponini) and the non-monophyly of the large genus Trigona. Systematic Entomology. 2007; 4 (1):77-81 - 31.
Schwarz F. The Indo-Malayan species of Trigona . Bulletin of the American Museum of Natural History. 1939;76 (3):83-141 - 32.
Anaktototy Y, Priawandiputra W, Sayusti T, Lamerkabel J, Raffiudin R. Morfologi dan Variasi Morfometrik Lebah Tanpa Sengat di Kepulauan Maluku, Indonesia. Journal of Entomologi Indones. 2021; 18 (1):10-22 - 33.
Pangestika N, Atmowidi T, Kahono S. Additional nest structures and natural enemies of Stingless Bees (Hymenoptera: Apidae: Meliponinae). Journal of Sumberd HAYATI. 2018; 4 (2):42-47 - 34.
Wille A, Michener C. The nest architecture of stingless bees with special reference to those of Costa Rica (Hymenoptera, Apidae). Revista de Biología Tropical. 1973; 21 (1):1-274 - 35.
Pratami D, Mun’im A, Sundowo A, Sahlan M. Phytochemical profile and antioxidant activity of Propolis Ethanolic extract from Tetragonula bee. Pharmacognosy Journal. 2018; 10 (1):128-135 - 36.
Tarakini G, Chemura A, Tarakini T, Musundire M. Drivers of diversity and community structure of bees in an agroecological region of Zimbabwe. Ecology and Evolution. 2021; 11 (11):6415-6426 - 37.
Jalil A. Beescape for a Malaysian Meliponary (Stingless bee farm). In: Roubik D, editor. The Pollination of Cultivated Plants A Compendium for Practitioners. Vol. 2. Rome: Food and Agriculture Organization of the United Nations; 2018. pp. 71-79 - 38.
Michener C. The Social Behavior of the Bees: A Comparative Study. Cambridge: Harvard University Press; 1974 - 39.
Sakagami S, Inoue S, Yamane S, Salmah S. Nest architecture and colony composition of the Sumatran Stingless bee Trigona (Tetragonula) laeviceps. Kontyȗ. 1983; 51 (1):100-111 - 40.
Engel M, Rozen J, Sepúlveda-Cano P, Smith C, Thomas J, Ospina-Torres R, et al. Nest architecture, immature stages, and Enthnoentomologu of a New species of Trigonisca from Northern Colombia (Hymenoptera: Apidae). American Museum Novitates. 2019; 3942 :1-33 - 41.
Jalil A, Shuib I. Beescape for Meliponines. Conservation of Indo-Malayan Stingless Bees. Singapura: Patridge; 2014 - 42.
Michener CD. The Meliponini. In: Vit P, Pedro SR, Roubik D, editors. Pot-Honey: A Legacy of Stingless Bees. Berlin, Germany: Springer Verlag; 2013. pp. 3-17 - 43.
Erniwati. Kajian Biologi Lebah Tak Bersengat (Apidae: Trigona) di Indonesia. Fauna Indones. 2013; 12 (1):29-34 - 44.
Roubik D. Stingless bee nesting biology. Apidologie. 2006; 37 :124-143 - 45.
Purwanto H, Soesilohadi R, Trianto M. Stingless bees from meliponiculture in South Kalimantan, Indonesia. Biodiversitas. 2022; 23 (3):1254-1266 - 46.
Atmowidi T, Prawasti TS, Raffiudin R. Flight activities and pollen load of three species of stingless bees (Apidae: Melliponinae). In: The 2nd International Conference on Bioscience (ICoBio). 2018. pp. 1-7 - 47.
Chuttong B, Panyaraksa L, Tiyayon C, Kumpoun W, Chantrasri P, Lertlakkanawat P, et al. Foraging behavior and pollination efficiency of honey bees (Apis mellifera L.) and stingless bes (Tetragonula laeviceps species complex) on mango (Mangifera indica L, cv. Nam Dokmai) in Northern Thailand. Journal of Ecological Environment. 2022; 46 (15):1-7 - 48.
Roldão-Sbordoni Y, Gomes G, Mateus S, Nascimento S. Scientific note: Warming nurses, a New worker role recorded for the first time in Stingless Bees. Journal of Economic Entomology. 2019; 112 (3):1485-1488 - 49.
Basari N, Ramli S, Khairi N. Food reward and distance influence the foraging pattern of Stingless bee, Heterotrigona itama . Insects. 2018;9 (4):1-10 - 50.
Salatnaya H, Widodo WD, Winarno FAM. The influence of environmental factors on the activity and Propolis production of Tetragonula laeviceps. J Ilmu Produksi dan Teknol Has Peternak. 2020; 8 (2):67-71 - 51.
Wulandari A, Atmowidi T, Kahono S. Peranan Lebah Trigona laeviceps (Hymenoptera: Apidae) dalam Produksi Biji Kailan. J Agron Indones. 2017; 45 (2):196-203 - 52.
Putra R, Subagio J, Kinasih I, Permana A, Rosmiati M. Pola kunjungan serangga liar dan efek penambahan koloni Trigona (Tetragonula) laeviceps Smith pada penyerbukan kabocha (Cucurbita maxima). J Entomol Indones. 2017; 14 (2):69-79 - 53.
Free B. Insect Pollination of Crops. London: Academic Press; 1970. p. 544 - 54.
Robinson W. Migrating honey bees ( Apis dorsata ) congregate annually at stopover site in Thailand. PlosOne. 2012 - 55.
Kahono S. Effect of extreme wet climate to the number of immigrant colonies of the giant honeybee Apis dorsata F. In: International Conference on Conservatino and Management of Pollinators September. Sarawak, Malaysia; 2011. pp. 14-17 - 56.
Kahono S, Prawiradilaga E, Peggie D, Erniwati SE. First report on hunting behavior of migratory oriental Honey-Buzzard (Pernis ptilorhynchus orientalis) toward migratory giant honeybee (Apis dorsata dorsata) (Hymenoptera: Apidae) on Java Island, Indonesia. Treubia. 2020; 47 (2):123-132 - 57.
Shanahan M, Spivak M. Resin use by stingless bees: A review. Insects. 2021; 2021 (12):719 - 58.
Kartawinata K. Diversitas Ekosistem Alami Indonesia. Indonesia: Yayasan Pustaka Obor Indonesia; 2013. p. 124 - 59.
Retnowati A, Rugayah RJ, Arifiani D. Status Keanekaragaman Hayati Indonesia, Kekayaan Jenis Tumbuhan dan Jamur Indonesia. Indonesia: LIPI Press; 2019. p. 139 - 60.
Sumarno, Hasnam I, Mustika, Bahagiawati (eds.). Sumberdaya Genetik Pertanian Indonesia. Pusat Penelitian dan Pengembangan Pertanian KPI, editor. Jakarta, Indonesia: IAARD Press; 2014. p. 496 - 61.
van Steenis C. Flora Malesiana 8: 1-577. Djakarta, Indonesia: Noordhoff-Kolff N.V; - 62.
Hatta H, Darnaedi D, editors. Phenology and Growth Habits of Tropical Trees: Long-term Observations in the Bogor and Cibodas Botanic Gardens, Indonesia. National S. Japan: National Science Museum; 2005. p. 441 - 63.
Faegri K, van der L P. The Principles of Pollination Ecology. Oxford-New York-Toronto-Sydney-Braunschweig: London Pergamon Press; 1971. p. 291 - 64.
Bawa K. Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology and Systematics. 1990; 21 :399-422 - 65.
Barth F. Insects and Flowers. The Biology of a Partnership. Princeton, New Jersey: Princeton University Press; 1991. p. 408 Translated by MA Biederman-Thorson, editor - 66.
Roubik D. Ecology and Natural History of Tropical Bees. Cambridge: Cambridge University Press; 1989. p. 514 - 67.
Heard T. The role of stingless bees in crop pollination. Annual Review of Entomology. 1999; 44 :183-206 - 68.
Heard T. The Australian Native Bee Book: Keeping Stingless Bee Hives for Pets, Pollination and Sugarbag Honey. Queensland, Australia: Sugarbag Bees; 2016. p. 247 - 69.
Majewski J. Pollination value as an ecosystem service. Ekon I Sr. 2018; 1 (64):208-219 - 70.
van der Sluijs J, Vaage N. Pollinators and global food security: The need for holistic global stewardship. Food Ethics. 2016; 1 :75-91 - 71.
Ollerton J, Winfree R, Tarrant S. How many flowering plants are pollinated by animals. Oikos. 2011; 120 :321-326 - 72.
Potts S, Imperatriz-Fonseca V, Ngo H, Aizen M, Biesmeijer J, Breeze T, et al. Safeguarding pollinators and their values to human well-being. Nature. 2016; 540 (7632):220-229 - 73.
Cortopassi-Laurino M, Imperatriz-Fonseca VL, Roubik DW, Dollin A, Heard T, Aguilar I, et al. Global meliponiculture: Challenges and opportunities. Apidologie. 2006; 37 :275-292 - 74.
Nogueiro-Neto P. A Criação de Abelhas Indigenas sem Ferrão. Editôra Chacaras e Quintais. 1953; 1953 :280 - 75.
Ayala R, Gonzalez V, Engel M. Mexican stingless bees (Hymenoptera: Apidae): Diversity, distrbution, and indigenous knowledge. In: Vit P, Pedro S, Roubik D, editors. Pot Honey: A Legacy of Stingless Bees. Springer Verlag; 2013. pp. 135-152 - 76.
Amin F, Sabri S, Mohammad S, Ismail M, Chan K, Ismail N, et al. Therapeutic properties of Stingless bee honey in comparison with European bee honey. Hindawi. 2018; 2018 (Special Issue):1-12 - 77.
Vit P, Roubik D, Pedro S. Pot-Honey: A Legacy of Stingless Bees. In: Pot-Honey: A Legacy of Stingless Bees. New York: Springer New York; 2013 - 78.
Bijlsm L, de Bruijn L, Martens E, Sommeijer M. Water content of stingless bee honey (Apidae: Meliponinae): Interspesific variation and comparison with honey of Apis mellifera . Apidologie. 2006;37 :480-486 - 79.
Pimentel T, Rosset M, de Sousa J, de Oliveira L, Mafaldo I, Pintado M, et al. Stingless bee honey: An overview of health benefits and main market challenges. Journal of Food Biochemistry. 2022; 46 (3):1-21 - 80.
dos Santos G, Antonini Y. The traditional knowledge on stingless bees (Apidae: Meliponina) used by the Enawene-Nawe tribe in western Brazil. Journal of Ethnobiology and Ethnomedicine. 2008; 4 (19):1-9 - 81.
Potts S, Biesmeijer J, Kremen C, Neumann P, Schweiger O, Kunin W. Global pollinator declines: Trends, impacts and drivers. Trends in Ecology & Evolution. 2010 - 82.
Reyes-González A, Camou-Guerrero A, Reyes-Salas O, Argueta A, Casas A. Diversity, local knowledge and use of Stingless bees (Apidae: Meliponini) in the municipality of Nocupétaro, Michoacan, Mexico. Journal of Ethnobiology and Ethnomedicine. 2014; 25 (6):345-353 - 83.
Giannini T, Maia-Silva C, Acosta A, Jaffé R, Carvalho A, Martins C, et al. Protecting a managed bee pollinator against climate change: Strategies for an area with extreme climatic conditions and socioeconomic vulnerability. Apidologie. 2017; 48 :784-794 - 84.
Rao P, Krishnan K, Salleh N, Gan S. Biological and therapeutic effects of honey produced by honeybees and stingless bees. Revista Brasileira de Farmacognosia. 2016; 26 :657-664 - 85.
Vijayakumar K, Muthuraman M, Jayaraj R. Predation of stingless bees (Trigona irridipennis: Apidae, Meliponinae) by centipede (Scolopendra hardwicki: Chilopoda, Scolopendramorpha). International Journal of Advanced Life Science. 2012; 5 (2):156-159 - 86.
Velthuis H. The Biology of Stingless Bee. Netherlands: Utrecht University Press; 1997 - 87.
Silva A, Gill-Santana H. Predation of Apiomerus pillipes (Fabracricus), (Hemimptera Apiomeriini) over meliponinae bees (Hymenoptera, Apidae) in the states of Amzonas, Onas, Brazil. Rev brazileria Zool. 2004; 21 :769-774 - 88.
Ashari R, Karyaatmadja B, Sutedja I, Rakhmadi D, Abidin S. The best practices of stingless bee farming in Kapuas Hulu Regency, West Kalimantan Province, Indonesia. In: IOP Conf Ser Earth Environ Sci. Indonesia: IOP Publishing; 2019, 2019 394, 012051 - 89.
Priawandiputra W, Giffary M, Rismayanti MK, Wicaksono A, Raffiudin R, et al. In: Priawandiputra W, editor. Lebah Tanpa Sengat (Stingless Bees) di Desa Perbatasan Hutan. Jakarta, Indonesia: ZSL Indonesia; 2020. p. 92 - 90.
Hrncir M, Maia-Silva C, da Silva T-SV, Imperatriz-Fonseca V. Stingless bees and their adaptations to extreme environments. Journal of Comparative Physiology. A. 2019; 205 (3):415-426 - 91.
Suhri A, Soesilohadi R, Agus A, Kahono S. The effects of introduction of the Sulawesi endemic Stingless bee Tetragonula cf. biroi from Sulawesi to Java on foraging behavior, natural enemies, and their productivity. Biodiversitas. 2021; 22 (12):5624-5632 - 92.
Schouten C, Lloyd D. Considerations and factors influencing the success of beekeeping programs in developing countries. Bee World. 2019; 96 (3):75-80 - 93.
Kahono S. Development of LIPI beekeeping models for education, ecotourism, and production that can be implemented to the community. Technical Report of LIPI Features Activities. Indonesia; 2015 - 94.
Toledo-Hernández E, Peña-Chora G, Hernández-Velázquez V, Lormendez C, Toribio-Jiménez J, Romero-Ramírez Y, et al. The stingless bees (Hymenoptera: Apidae: Meliponini): A review of the current threats to their survival. Apidologie. 2022; 53 (8):1-23 - 95.
Lima M, Cutler G, Mazzeo G, Hrncir M. Editorial–the decline of wild bees: Causes and consequences. Frontiers in Ecology and Evolution. 2022 - 96.
Gratzer K, Purnomo D, Susilo F, Fiedler F. Challenges for beekeeping in Indonesia with Autochthonousand introduced bees. Bee World. 2019; 96 (44):1-5