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Production of honey, pot-pollen and propolis from Indonesian stingless bee Tetragonula laeviceps and the physicochemical properties of honey: A review

Agussalim and Ali Agus

Department of Animal Nutrition and Feed Science, Faculty of Animal Science, Universitas Gadjah Mada, Jl. Fauna No. 3, Bulaksumur, Yogyakarta 55281, Indonesia
aliagus@ugm.ac.id

Abstract

Beekeeping in stingless bees is called meliponiculture to make it easier to control the colonies health and development, to make it easy when harvesting stingless bee products (honey, pot-pollen, and propolis). Furthermore, for advanced study and development like multiple colonies, to produce honey, pot-pollen, and propolis. Therefore, this paper was discussed focus briefly on stingless bee Tetragonula laeviceps: the domestication and beekeeping technique, production of stingless bee products (honey, pot-pollen, and propolis), the daily activity of foragers, the chemical composition (sugars profile, moisture, protein, ash, phenolic, flavonoid, vitamin C, antioxidant activity, minerals content, and amino acids) of honey from T. laeviceps.

Keywords: foragers, meliponiculture, nectar, pollen, resin


Introduction

The stingless bees are eusocial bees and include the tropical group, whereas the number of species have been identified are 500 species and possibly more than 100 species yet undescribed. The stingless bees include family Apidae, sub-family Apinae, and tribe Meliponini. In tropical regions of the world, they are divided into three zones are the American tropics (Neotropics), sub-Saharan African (Afrotropical region), and the Indoaustralian (Austroasian) region (Michener, 2007; 2013). In Indonesia, the stingless bees species at least 46 species from genus Austroplebeia Moure, Geniotrigona Moure, Heterotrigona Schwarz, Homotrigona Moure, Lepidotrigona Schwarz, Lisotrigona Moure, Papuatrigona Michener and Sakagami, Pariotrigona Moure, Tetragonula Moure and Wallacetrigona Engel and Rasmussen which are spread in several islands like Sumatera, Java, Timor, Borneo, Sulawesi, Ambon, Maluku, and Papua (Kahono et al 2018).

Stingless bees species in Indonesia are Austroplebeia cincta, Geniotrigona lacteifasciata, G. thoracica, Heterotrigona erythrogastra, H. itama, Platytrigona flaviventris, P. hobbyi, P. keyensis, P. lamingtonia, P. planifrons, Sahulotrigona atricornis, Sundatrigona lieftincki, S. moorei, Homotrigona aliceae, H. anamitica, H. fimbriata, Lophotrigona canifrons, Odontotrigona haematoptera, Tetrigona apicalis, T. binghami, T. vidua, Lepidotrigona javanica, L. latebalteata, L. nitidiventris, L. terminata, L. trochanterica, L. ventralis, Lisotrigona cacciae, Papuatrigona genalis, Pariotrigona pendleburyi, Tetragonila atripes, T. collina, T. fuscibasis, Tetragonula biroi, T. clypearis, T. drescheri, T. fuscobalteata, T. geissleri, T. laeviceps, T. melanocephala, T. melina, T. minangkabau, T. reepeni, T. sapiens, T. sarawakensis, and Wallacetrigona incisa (Kahono et al 2018). In addition, the recently reported that the seven species of stingless bees were found in the Special Region of Yogyakarta including the local and introduced of stingless bees are T. laeviceps, T. biroi, T. sapiens, T. iridipennis, T. sarawakensis, L. terminata, and H. itama (Trianto and Purwanto 2020).

Furthermore, the T. laeviceps is a species whose distribution in Indonesia is quite large, whereas all the islands are covered (Kahono et al 2018). In Indonesia, stingless bees can be found in the forest, plantations, and they create the nest in wood or tree trunk, bamboo, sugar palm stalks, and in the ground. Especially stingless bee T. laeviceps can be found nesting in bamboo, wood or tree trunk, and in the ground (Supeno et al 2022; Agus et al 2019ab; Agussalim et al 2019a; Agussalim et al 2015). The meliponiculture of T. laeviceps requirement nectar and pollen sources from plant flowers as the raw material to produce honey and pot-pollen. In addition, the bees requirement of resin from the plants to produce propolis to construct the hive, to made pots to storage honey and pollen, to construct entrance, and to embalm of hole hive. Honey is used by the bees as the energy source while pot-pollen as the protein source to support the productivity of colony especially queen bee (Agussalim 2020). Therefore, this paper is focused on stingless bee T. laeviceps: the domestication and meliponiculture technique, production of stingless bee products, the daily activity of workers (foragers), and the chemical composition of honey.

Meliponiculture of Tetragonula species

Stingless bee T. laeviceps is made a natural habitats from bamboo, wood or tree trunk, in the wal house, and in the ground (Agus et al 2019ab; Agussalim et al 2019a; Agussalim et al 2015) are shown in Photo 1. The domestication of stingless bee T. laeviceps can be performed in the morning, afternoon and in the night. The domestication in the morning and afternoon have advantages such as easier to performed it, all colonies condition can be seen clearly (brood cells, workers, drones, and queen bee), and to avoid the death of the queen bee when the brood cells are cut. However, the disadvantage such as both workers and drones are exit from the hive, which is impacted on, they are lot of crowding in the head and eyelashes if not using the bee net hat (Agussalim 2020).

Photo 1. The sources of natural habitats of the stingless bee T. laeviceps from bamboo (A), house wall (B),
sugar palm stalk (C), and wood or trees (D) (Pictures source from Agussalim unpublished)

Furthermore, the advantages of domestication in the night such as easier to performed it and both workers and drones are stay in the hive so easier to move from the natural habitat to new hive like box hive. However, the disadvantage namely the queen bee can’t seen clearly, because she is activity in the young brood cells or in the base of the natural hive, so when cut the brood cells may be hurt the queen bee which is impacted on their death (Agussalim 2020).

The various of the natural habitat from stingless bee T. laeviceps showed that they have ability to adaptation, to build their colonies, and production several products such as honey, pot-pollen, and propolis. In addition, the different natural habitat which is impacted on the different entrance each hive sources for example can be seen in the Photo 1B namely in yellow circle. The entrance is also differing every hive depend on the ability of the workers bee to build the entrance and to collect various resin as the raw material to produce propolis which used by the bee to construct their entrance. The different resin sources from plants which is impacted on the various of entrance colors. The entrance of T. laeviceps are made from the combination of propolis, soil, and the minerals (Agussalim 2020; Roubik, 2006). Domestication of the stingless bee T. laeviceps and the natural hive is obtained from the bamboo hives from the plantation in Yogyakarta, Indonesia and the domestication process can be shown in Photo 2.

Photo 2. The process of domestication of T. laeviceps (1. Tetragonula laeviceps in the bamboo hive, 2. Description of the colony in
the bamboo hive, 3. The brood cells, queen, workers, and drones have been moved from bamboo hives to box hives,
4. The house of bee to placed box hives for meliponiculture) (Pictures source from Agussalim unpublished)

The domestication process consists of the colonies from bamboo being split and then the brood cells, queen bee, drones, and workers are moved from bamboo to box hives. Afterward, the colonies are placed in bee house (Photo 2.4) for meliponiculture. The box hives used have a size 35 × 15 × 12 cm for length, width, and height, respectively and are made from the dry board with a thickness of 2 cm. Several factors that are very important after domestication are to avoid the colonies from the ants, lizards, and spiders. When the colonies are domesticated, must be performed carefully to avoid dripping honey in the hives because it can be inviting the ants. Consequently, the colonies in the hives can be destroyed by ants if they can be an entrance to hives, especially the new colony after domestication from bamboo hive to box hive. In nature, the domestication in stingless bees can be performed with three methods are the tree cutting, grafting, and trap system (Priawandiputra et al 2020). The colonies from stingless bee T. laeviceps in Yogyakarta are found mostly nesting in bamboo hives. The colony condition of stingless bee of T. laeviceps after four months of meliponiculture in Faculty of Animal Science, Universitas Gadjah Mada (UGM), Indonesia is shown in Photo 3.

Photo 3. The colony condition of stingless bee T. laeviceps: pots honey (inside the yellow cycle) and
brood cells (inside the red cycle) (Pictures source from Agussalim unpublished)

Photo 3 includes a good colony of stingless bee T. laeviceps after meliponiculture for four months is characterized by brood cells and honey pots which are much. In addition, the forages as the source of nectar to produce honey in the Faculty of Animal Science UGM consist of calliandra (Calliandra calothyrsus), banana (Musa paradisiaca L.), mangoes (Mangifera indica L.), chicory (Cichorium intybus L.), sunflowers (Helianthus annuus), tamarind (Tamarindus indica), catappa (Terminalia catappa ), indigofera (Indigofera arrecta), kapok (Ceiba pentandra), syzygium (Syzygium polyanthum), alfalfa (Medicago sativa) L, kepel (Stelechocarpus burahol), star fruit (Averrhoa carambola), bilimbi (Averrhoa bilimbi), matoa (Pometia pinnata), water apple (Syzygium samarangense), guava (Psidium guajava), lemon (Citrus limon), gliricidia (Gliricidia sepium), chili (Capsicum annuum), caimito (Chrysophyllum cainito), rambutan (Nephelium lappaceum), and canarium (Canarium indicum L.) (Agussalim et al 2020).

Production of stingless bee products

In general, stingless bees can be producing honey, pot-pollen, and propolis. Production of honey from stingless bees is lower compared with honey production of honeybees from genus Apis for example Apis mellifera, A. cerana and A. dorsata, etc. In addition, propolis production in stingless bees is higher than in honeybees. T. laeviceps is one of the species of stingless bee and more meliponiculture by beekeepers in Indonesia.

Production of honey, pot-pollen, and propolis from stingless bee T. laeviceps in each region in Indonesia for meliponiculture is varied. Honey from stingless bee T. laeviceps is made by workers in the hive required 3 to 4 days after domestication (from bamboo hive to box hive) to produce 2 to 3 pots that are filled with honey. Production of honey T. laeviceps meliponiculture in Faculty of Animal Science UGM (Yogyakarta, Indonesia) is ranged from 60 to 263 ml/colony (79.2 to 328 g) with the mean 176 ml (223 g) after four months meliponiculture (Agussalim et al 2020), 49.20 to 66.60 ml/colony after two months meliponiculture for Tetragonula sp. in Gunungkidul (Yogyakarta) (Agussalim et al 2017), 1.44 g/colony/month for Cibodas, 0.93 g/colony/month for Cileunyi Wetan (Bandung) from T. laeviceps (Abduh et al 2020). The different production of honey from each region for meliponiculture is caused by the different regions as the location to meliponiculture, different plant types as the nectar source to produce honey, the different environment conditions (temperature, humidity, and altitude). In addition, the foragers activity especially when collecting nectar from plant flowers (floral nectar) and extrafloral nectar, the distance of meliponiculture site to plant types that impact the number of nectars can be collected by foragers of stingless bees.

Production of propolis from stingless bee T. laeviceps is varied from each region for meliponiculture depending on the availability of plants as the resin sources and the active level of foragers to collect resin much more. Propolis production from stingless bee T. laeviceps that meliponiculture in Faculty of Animal Science UGM (Yogyakarta, Indonesia) is ranged from 15.4 to 77.2 g/colony obtained from honey pots after meliponiculture for four months (Agussalim et al 2020), 18.20 to 30.80 g/colony after two months of meliponiculture for propolis from honey pots for Tetragonula sp. (Agussalim et al 2015), total production of propolis is 4.26 g/colony/month (propolis from the frame is 3.80 g/colony/month and 0.46 g/colony/month from honey pots) in Cileunyi Wetan region for meliponiculture, and 4.54 g/colony/month (propolis from the frame is 4.24 g/colony/month, and 0.30 g/colony/month from honey pots) in Cibodas (Bandung) (Abduh et al 2020). The different production of propolis in each region in Indonesia is related to the availability of resin from living plants, the number of workers especially foragers that collect resin, the productivity of queen bee to produce eggs as the workers.

Production of pot-pollen from stingless bee Tetragonula sp is ranged from 1.02 to 4.56 g/colony after two months of meliponiculture using various box hives in Gunungkidul (Yogyakarta, Indonesia) (Agus et al 2019a). Production of pot-pollen is dependent on the availability of pollen from plant flowers, the exit activity of foragers to collect pollen, the population of workers especially foragers, and region condition (temperature and humidity). Pot-pollen is the main source of protein in the hive which is required by workers bee to produce royal jelly as the feed of queen bee, impact the increase of productivity of queen bee to produce eggs as the workers.

Daily activities of foragers

The activities of workers in the hives are to produce stingless bee products (honey, pot-pollen, propolis, royal jelly), to carrying and feeding (eggs, larvae, and queen), while out of the hives to collect nectar, pollen, resin, water and some materials are needed to construct their nest. This paper focuses on the entrance and exit activities of foragers of stingless bee T. laeviceps. The daily activity of stingless bee T. laeviceps in the morning (07.00 to 11.00 am) is higher than activity in the afternoon (2.00 to 5.00 pm). The number of foragers who bring in pollen to the hive in the morning (07.00 to 11.00 am) is ranged from 20.15 to 25.36 times per 5 minutes per colony, while in the afternoon is ranged from 12.19 to 12.85 times per 5 minutes per colony. Furthermore, the foragers are exit from the hive to collect nectar, pollen and resin in the morning started is ranged from 05.25 to 05.30 am and the first time bring in pollen to the hive is ranged from 05.40 to 05.45 am (Agus et al 2019a).

In addition, the exit and entrance of the hive of stingless bee Tetragonula sp. is ranged from 37 to 43 times per 5 minutes per colony and ranged from 38 to 46 times per 5 minutes per colony, respectively (Agussalim et al 2017). The exit activity of foragers Tetragonula sp. in the bamboo hive in the morning (08.00 am) is ranged from 34.7 to 37.5 times and higher than in the afternoon (04.00 pm) is ranged from 24.9 to 25.5 times per 5 minutes per colony. Furthermore, the exit activity of foragers in the box hive is ranged from 49.2 to 51.3 times in the morning is higher than in the afternoon is ranged from 29.0 to 29.6 times per 5 minutes per colony (Erwan et al 2021). Furthermore, reported that the exit activity of foragers Tetragonula sp. in the morning (08.00 am) from the bamboo hive is 36.6 times and in the afternoon is 25.3 times, while in the box hive is 50.1 times in the morning (08.00 am) and 29.3 times in the afternoon. The daily activity of stingless bee T. laeviceps in each colony is differed depending on the population of bee in the colony, the environment condition (temperature, humidity, air velocity, and light intensity), and the availability of food (nectar, honeydew, and pollen) (Erwan et al 2020).

Chemical composition of honey

The moisture content is one of the very important parameters which influence the physical properties of honey such as crystallization process, colour, taste, flavour and solubility (Da Silva et al 2016; Escuredo et al 2013). The moisture content of honey from stingless bee T. laeviceps is ranged from 21.21 to 26.81% (Agussalim et al 2019) and the moisture content is lower to those previously studied (Biluca et al 2016; Guerrini et al 2009; Ranneh et al 2018; Souza et al 2006; Suntiparapop et al 2012). The moisture content of stingless bee honey is high because they also collect some material from ripe fruit which is higher in moisture content. In addition, the stingless bees species have not developed a mechanism of behaviour to evaporate water compared with honeybees from the genus Apis (Suntiparapop et al 2012). The moisture is acceptable by Indonesian standard (SNI, 2018), but the international standard by Codex Alimentarius has not been set for honey from stingless bees.

The ash content of honey from stingless bee T. laeviceps is ranged from 0.07 to 0.49 g/100 g of honey (Agussalim et al 2019) and contains the minerals consist of Ca is ranged from 2,964.86 to 3,256.83 ppm, Cu 3.9 to 12.2 ppm, Fe 9.75 to 45.4 ppm, Mg 289.48 to 2,389.65 ppm, Mn 12.5 to 33.9 ppm, Na 234.90 to 1,142.87 ppm, K 2,498.65 to 20,110.80 ppm, Zn 12.0 to 23.5 ppm, and Al 858.89 to 1,120.71 ppm. The abundance of minerals of honey from T. laeviceps is potassium followed by calcium (Sabir et al 2021). The ash content of honey is related to mineral content present in the honey and indicates the geographical origin marker (Da Silva et al 2016; Suntiparapop et al 2012). The ash and mineral content of honey is affected by the soil nutrient and the nectar source from each plant flower (Da Silva et al 2016; Karabagias et al 2014). In addition, the ash and mineral content of honey related to colour and flavour, where the higher mineral content characterized by honey is darker and stronger flavour if compared with honey bright colour with the low mineral content (Da Silva et al 2016; Escuredo et al 2013; Karabagias et al 2014).

The protein content of honey from stingless bee T. laeviceps is ranged from 0.18 to 0.72 g/100 g of honey (Agussalim et al 2019), while the amino acids present in honey from T. laeviceps consist of arginine is 591.83 mg/kg, histidine 561.93 mg/kg, lysine 882.03 mg/kg, phenylalanine 232.74 mg/kg, isoleucine 12.34 mg/kg, leucine 73.55 mg/kg, methionine 0.29 mg/kg, valine 20.39 mg/kg, threonine 45.72 mg/kg, tyrosine 9.24 mg/kg, proline 60.56 mg/kg, glutamic acid 119.82 mg/kg, aspartic acid 77.31 mg/kg, serine 168.65 mg/kg, alanine 62.46 mg/kg, and glycine 60.26 mg/kg of honey (Agussalim et al 2019b). The protein and amino content in honey depend on the nectar source from plant flowers and the pollen source from plant flowers. The main source of protein for honeybees or stingless bees is pollen (Da Silva et al 2016; Karabagias et al 2014). In honey, the amino acid proline can be used to detect the adulteration of honey which is made from sugar like cane, coconut, and palm sugars. The minimum content of proline is 180 mg/kg is acceptable for the minimum proline content for pure honey especially in honey from Apis mellifera (Da Silva et al 2016), but in stingless bees honey has not been confirmed as one of the parameters to detect the adulteration of honey. The lower content of proline amino acid is related to not complete maturity of honey and might be an adulteration of honey, but it needed the advanced study to verify this case.

The sugar content of honey from stingless bee T. laeviceps is lower than honey from Apis genus like Apis mellifera, Apis cerana, Apis dorsata, etc. The different geographical origins for meliponiculture impacted the sugars content of honey. The sugar content of honey from stingless bee T. laeviceps consist of glucose is ranged from 11.49 to 22.78% (w/w), fructose 7.79 to 22.92% (w/w), sucrose 2.56 to 4.49% (w/w) and reducing sugar 44.07 to 60.14 g/100 g of honey, the total of glucose and fructose 30.57 to 43.16% (w/w), and the ratio of fructose/glucose 0.34 to 1.99 (Agussalim et al 2019a). The sugars content of honey is affected by the different nectar source (plant types) to produce honey, geographical origin for meliponiculture, climate (temperature and humidity), processing (heated, manipulation, and packaging) and storage time (Da Silva et al 2016; Escuredo et al 2014; Tornuk et al 2013). The sugars content of honey from Indonesia T. laeviceps is differs from those previously studied (Biluca et al 2016; Chuttong et al 2016; Guerrini et al 2009; Oddo et al 2008; Souza et al 2006; Suntiparapop et al 2012). The sucrose content of honey is one of the very important parameters to evaluate the adulteration or manipulation of honey and the maturity of honey. The high sucrose content from honey may indicate manipulation and adulteration of honey using sugar (sugar cane, refined beet sugar, sucrose syrups). In addition, it also indicates the early harvest of honey so the sucrose is not completely transformed into glucose and fructose (Da Silva et al 2016; Escuredo et al 2013; Puscas et al 2013; Tornuk et al 2013).

The bioactive compounds of honey from stingless bee T. laeviceps have been studied to consist of total phenolic and total flavonoid. In addition, vitamin C and DPPH antioxidant activity were also studied. The total phenolic content of honey from stingless bee T. laeviceps is ranged from 0.54 to 1.69% GAE (w/w), total flavonoid content 0.21 to 0.90 mg QE/g, vitamin C content 5.67 to 7.88 mg/100 g and the DPPH antioxidant activity 47.3 to 91.2% at concentration 0.1 mM (Agus et al 2019b). The total phenolic content of honey from Indonesia T. laeviceps is differs from those previously studied (Biluca et al 2016; Guerrini et al 2009; Oddo et al 2008; Ranneh et al 2018), total flavonoid content (Oddo et al 2008; Ranneh et al 2018), vitamin C (Ranneh et al 2018), and DPPH antioxidant activity (Guerrini et al 2009; Oddo et al 2008; Ranneh et al 2018). The phenolic, flavonoid, and vitamin C is affected by the nectar source (plant types), while antioxidant activity is affected by the metabolites secondary content such as phenolic and flavonoid. Based on the Pearson correlation coefficients in our study that the DPPH antioxidant activity is affected by the total phenolic and total flavonoid contents (Agus et al 2019b).


Conclusions


Acknowledgement

The authors would like to thank the Directorate of Research, Reputation Improvement Team World Class University-Quality Assurance Office of Universitas Gadjah Mada (Indonesia) for funding sponsor through Post-Doctoral Program 2021 with contract number: 6283/UN1/DITLIT/DIT-LIT/PT/2021.


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