1. Introduction

Honey bee is an insect that has a social system (eusocial) included in the family Apidae, order Hymenoptera. The Hymenoptera is one of the largest orders of class Insecta comprising more than 100,000 species [11,9]. With the diversity of around 20,000 species of bees worldwide, the honey bees (Apis L.) are the most heavily researched and managed, focusing on the efforts of thousands of researchers [6]. Apis dorsata Fabricius has 3 subspecies, namely: Apis dorsata dorsata, Apis dorsata binghami, and Apis dorsata breviligula. From the results of a study by [10] that with mtDNA analysis of Apis cerana from Indonesia, China, Korea, Malaysia, Russia, Taiwan, Vietnam, Thailand, and Japan, it was concluded that the Apis cerana of Far East Russia is a subspecies. [16] reported four species belonging to the genus Tetragonula were found, namely T. fuscobalteata, T. biroi, T. sapiens, and T. laeviceps. Two species, T. biroi and T. sapiens are the new records in Sulawesi island. Stingless bees, for example, Trigona, are pollinating insects that are important for plants and useful for producing honey. Types of honey bees that have been known consist of: Apis mellifera; Apis dorsata; Apis cerana; Apis moluensis; Apis koschevnikovi; Apis nigrocincta; Apis laboriosa; Apis florea; Apis andreniformis. Meanwhile, the distribution of bee species in Java is the stingless bee, forest honey bee (Apis dorsata), Apis mellifera, and Apis cerana.

Apis cerana is a bee species distributed mainly in Asia and closely related to species of Apis mellifera, Apis cerana was earlier considered as a sub-species of honeybees Apis mellifera. The representatives of the Korean population of Apis cerana could be called further as a subspecies of Apis cerana koreana. [17] reported the genetic diversity of the honeybee Apis cerana in Yunnan, China, based on mitochondrial DNA. GMR Genetics and Molecular Research.

Honey bees produces honey from flower nectar and pollen, in place of flower nectar or other parts of various types of plants that contain liquid nectar. Plants produce a resinous sap, then it is carried by honey bees and used to seal holes in their nests. That resin substance is called propolis. Propolis is a plant-derived product that bees produce from resins that they collect from different plant organs and with which they mix beeswax. It is one of the most fascinating honey bee (Apis mellifera L.) products [3].

The activities of bees inadvertently also play a role in pollination, so that they can increase agricultural and plantation production. Likewise, it can carry out the evolutionary process of bees and various types of plants naturally. The diversity of flowering plant species (Spermatophyta) produces nectar, pollen, resin, which are processed by honey bees as honey producers. These processed products can support the honey bee production industry.

[7] reported that pollen morphological characters can be used to identify plant species in the form of number and position, aperture complexity and position, and the exine sculpturing. Pollen grains (microspores) result from the process of microsporogenesis with various structures, sizes, and shapes: radial symmetry (bilateral), round (pores), elongated (colpi), and strong pollen walls (aperture). According to [7], when the amount of phloems is higher, the honey gland content reaches 50%, and the xylem has more sugar content of only 8%. The benefits of honey are to strengthen immunity, increase stamina, heal wounds, prevent various cancers, diabetes, heart disease, influenza, and also corona virus. Honey also contains antioxidants, supports beauty regarding skin rejuvenation, and becomes a source of minerals, vitamins, carbohydrates, and fructose. The purpose of this study is to reveal members of the plant family species at Brawijaya University and Sawojajar housing estate in Malang City, which have the potential to be used as food for honey bees.

2. Materials and Methods

This study was conducted from December 2019 to September 2020 through a random survey based on the presence of types of plants with the habitus of the tree, shrub, herb, and grass visited by honey bees (Apis spp. & Trigona sp.) in Universitas Brawijaya campus area and Sawojajar residential area in Malang, East Java (Figure 1A,B). Plant species were recorded, identified, then flowers were taken to observe the part of pollen and nectar, then they were made into herbarium. The identification was conducted using the book Flora of Java by [2,4], floral morphological characters with identification books [8,15,4], while the pollen character was identified based on various journals and books. Flower characterization was done by an Olympus SZ61 microscope, a magnifying glass (loupe), while pollen was observed with an Olympus CH20 microscope equipped with micrometers.

Figure 1. A. The Map of the campus of Universitas Brawijaya, and B. Sawojajar residential area of Malang, East Java

3. Results and Discussion

Honeybee Feed Flora Diversity

Malang city has an average height of 450 m above sea level, known for many ancient historical relics, for example, the kingdom of Kanjuruan, Singhasari which is located between Mount Arjuno, Bromo Tengger Semeru, and Mount Kawi. This city is located in a cool highland with an area of 145.28 km, located in the middle of Malang Raya. Meanwhile, the location of the green campus of Universitas Brawijaya is in the middle of Malang city, where many types of flowers are planted, such as trees, shrubs, and herbs. Likewise, Sawojajar residential area, with a dense population and many types of trees, shrubs, grasses, and house ornamental plants are planted.

The diversity of flower plant species of the Monocotyledoneae group favored by honey bees includes the Arecacaeae family (Roystonia regia, Cocos nucifera, Elaeis quinenesis, Area catechu); Poaceae (Zea mays, Oryza sativa, Pennisetum purpurium), and Agavaceae (Agave sp.). Meanwhile, the Dicotyledoneae group includes guavas (Myrtaceae): Zyzygium malaccense, Zyzigium aqueunum, Zyzygium aromaticum, Zyzygium littorale, Eugenia cumini. Fabaceae (Samanea saman, Leucaena glauca, Caliandra haematocephala); Lecythidaceae (Baringtonia asiatica), Asteraceae: Brassicaceae (Brassica oleracea), Asteraceae (Thitonia diversifolia); Amaranthaceae: Amaranthus spinosus; Rutaceae (Citrus sinensis), Bombaceae (Ceiba petandra); Rubiaceae (Coffea arabica), Lauraceae: Lantana camara; Lamiaceae: Ocimum basilicum, Sapotaceae: Chrysophyllum cainitu; Lecythidaceae: Baringtonia asiatica; Tiliaceae: Muntingia calabura; Sapindaceae, Dimocarpus longan; Rosaceae (Rosa hybrida). Family characteristics have the power to interpret and determine whether the group’s members have the potential to support honeybee production. Therefore, the familia taxonomic level is the key in developing sustainable bee production. For example, farmers by planting jagung, corn (Zea mays), produce corns, while honey bee farmers benefit greatly from increased production of nectar and pollen. This symbiotic relationship occurs in other species, for example, silk-cotton tree, star-apple, longan, rambutan, coconut, palm, mango, guava, and grass.

Basically honey bee takes nectar not limited to one type of plant, but also other types of flowers that are blooming. Nectar is generally located at the base of flowers, stamens (anthera), base of ovules, stylus, crown, and other floral plant organs. The smell of flowers, the color of flowers greatly affect the arrival of the type of worker bees to look for nectar, resin, and pollen. Bees are actively involved in pollinating agricultural crops and wild plants are known to have a preference for selecting flowers for pollination. [7] epidermal tissue is covered by a cuticle and the layer below is secretory tissue, there is a network of vessels that are thought to be related to the transport bundle or perhaps the one that produces honey glands.

The people of Malang and schools in Malang, including the campus environment with the potential for flora diversity used by honey bees, have not been interested to cultivate in a traditional or modern way. Malang’s urban landscape strongly supports the honeybee industry with the presence of urban forests, many housing estates, schools, research institutions, public and private universities, dry fields, rice fields, and tourist attractions. With the results of this study, it is expected that it can provide data and scientific information to be able to develop beekeeping learning, tourism, production of modern urban honey bee innovations. The diversity of species that have the potential to develop honey production in urban areas includes 43 families (Table 1).

Table 1. Potensial plants with their correct nomenclature were arranged by local name, scientific name, family name, and habitus

The Life of Honey Bee

In the season when plant species bloom heavily, it turns out that it does not only affect the types of bees looking for nectar but also competes with various other insects such as butterflies (Figure 2), green flies, house flies, beetles, black ants, weaver ants and so on. Flowering season, distance, altitude, and environment are also important factors for the existence of visiting the flower species. An environment with crowds such as human activities on the highway, campus activities, housing affects the presence of bee species in their activity of looking for nectar, pollen, and nesting places. For the detection of nectar in flower organs, researchers are only limited to looking at the instinctive activities of choosing bees to take nectar. [5] reported that small amounts of pollen are sufficient for amplification, and in our observations were able to extend to other species where pollen samples were widely available.

Figure 2. A. Various types of insects perch on clove (Syzygium aromaticum), B. cherry (Prunus sp.)

Pollen in Monocotyledoneae

In Arecaceae, the flowers in the form of bunches, the big number of flowers may indicate that the amount of nectar and pollen is also large, for example, coconut (Cocos nucifera). In the Areca sp., the pollen shape is round, the exine is generally irregular, and slightly elongated. Meanwhile, pollen diameter is 57.75 - 66 µm; and some are slightly elongated 77-83.5 x 33-41.25 µm (Fig. 3A). In Poaceae, for instance, elephant grass (Pennisetum purpureum) was transparent, grayish-white, round in shape, clear exine, porous with streaks or spots, 55-57.75 µm in diameter (Figure 3B). Meanwhile, Liliaceae, for example, the crinum species (Crinum zeylanicum) has shape and size of 100-110 µm x 40-42 µm, uniform pollen (Figure 4).

Figure 3. A,B. Arecaceae pollen (Areca sp) and C,D. Poaceae pollen (Pennisetum purpureum)

Figure 4. Liliaceae pollen, beach spider lily (Hymenocallis littoralis)

Pollen in Dicotyledoneae

The shape and size of pollen, the color of each type of dicotyledoneae plant is generally similar, but some have various sizes. Several species of the Myrtaceae family, Surinam cherry (Eugenia uniflora), have a pollen size of 30.25-35.75 µm (Fig. 5A). Members of the Arecaceae, Myrtaceae are visited and most favored by various types of bees, both the Apis and Trigona genera. In Polygonaceae, the pollen shape is invariable, but there are different sizes, the spherical pollen’s diameter is 66-71.5 µm; while the oval is 66-71.5 m x 41.25-18.15 µm (Fig. 5 B). In Fabaceae, for example, rain tree (Samanea saman), there are two kinds of pollen’s shape in one flower (Figure 7B). In the Malvaceae family, they are generally identical, only differing in size and density of spines on the surface of exin, for example in Hibiscus rosa-sinensis where the pollen is rounded with dense spiked edges measuring 13.75 x 5.5 µm (Figure 7A). While the sea mango (Cerbera manghas), family Apocynaceae (6A); Verbenaceae, e.g. blue porterweed (Stachytarpheta jamaicensis) have triangular-shaped pollen which contains easily broken pollen liquid (Figure 6B).

Figure 5. A,B Pollen Myrtaceae (Surinam cherry-Eugenia uniflora) and B, C. Polygonaceae (knotweed-Polygonum sp.)

Figure 6. A. Sea mango (Cerbera manghas). B. Verbenaceae (blue porterweed-Stachytarpheta jamaicensis)

Figure 7. A. Malvaceae pollen (Chinese hibiscus, Hibiscus rosa-sinensis) and B, C Fabaceae (pollen from rain tree-Samanea saman)

Honeycomb

The existence of the nest of a stingless bee (Trigona sp.) follows the choice of the queen bee, in any place on dry bamboo, doors, windows, earthen mounds, caves, iron holes, dry wood, wood holes, house tiles, plant pots, etc. Similarly, Apis cerana and Apis mellifera bees are in the house, coconut tree holes, other tree species, gravestone holes, cauldron, etc. Local people usually make and move to a bee house called glodokan made of coconut trees, mahogany, and so on. According to Mr. Yacobus, the banyan tree (Ficus benyamina) is often used for nesting giant honey bees (Apis dorsata), wherein in one tree, there is more than one nest. According to Mr. Ustadi, the sustainable development of honey bees can be done with innovation from the manufacture of queen bees. Meanwwhile, the harvesting of giant honey bees by the local community is also explained by Dewi Masyitoh (Universitas Brawijaya), Ervan (Universitas Mataram), and Mr. Yacobos (Universitas Pattimura) that it is started by performing traditional rituals, the mantra to chant the drum. The character of the family taxon is the key to developing sustainable bee production.

In general, pollen with a small structure and unattractive flower color is distributed with the help of the wind. In contrast, large pollen structures and attractive flower colors are distributed with the help of insects. Variations in the shape and size of pollen between plant species are caused by differences in plant species based on the genus, so that the shape and size of pollen in plants in different genera have different pollen forms [14,1]. However, several species of the same flower plant have different shapes and sizes of pollen, for example, in the Samanea saman species (Fig. 7 B, C).

The family of Arecaceae (palm trees), class monocotyledoneae has a tree habit, generally unbranched, with large and long leaves. Arecaceae flowers, for example Cuban royal palm (Roystonia regia), oil palm (Elaeis guineensis), and coconut (Cocos nucifera) have potential as honey bee feed because of the large number of flowers per bunch and its resistance in all seasons. Similarly, the family of grasses (Poaceae), for example corn (Zea mays), rice (Oryza sativa), and reeds (Imperata cylindrica) have great potential as producers of honey bee feed: pollen, nectar due to the amount of pollen. Pandan (Pandanus tectorius) is visited by many bees, mainly stingless bee (Trigona spp.) and honey bee genus (Apis spp.).

Dicotyledoneae (Magnoliopsida) has characteristics of either herbaceous or woody, having simple or compound leaves, sitting leaves scattered or craggy, alternate with carrier bundle elements, cambium produces layers with secondary growth. For instance, the orders Ranales (Polycarpicae), Passiflorales, Cactales (Opuntiales), Rosales, Malvales (Columniflorae), Sapindales, Urticales, Myrtales (Myrtiflorae), Santalales, Proteales, Piperales, Ebenales, Primulales, Tubiflorae, Rubiales, etc.

The order Myrtales includes several families namely Myrtaceae, Lecythidaceae, Melastomaceae, Lythraceae, Thymelaceae, Bignoniaceae, Rhizophoracea. The myrtle family (Myrtaceae) including clove (Zyzygium aromaticum), blume (Zyzygium littorale), watery rose apple (Zyzygium aqueum), and Malay apple (Zyzygium malaccense) were visited by many types of bees, among others, Western honey bee (Apis mellifera), stingless bee (Trigona spp.), and giant honey bee (Apis dorsata), as well as butterflies, green flies, house flies to many ants in the flower location. Common guava (Psidium guajava), blume, and watery rose apple generally bloom in December to January; therefore, the researchers encountered a lot of Western honey bees and stingless bees. Similarly, a number of families of Sapindaceae were also found, including rambutan (Nephelium lappaceum), lac tree (Schleichera oleosa), lychee (Litchi chinensis), matoa (Pometia pinnata), longan (Dimocarpus longan), fern tree (Filicium decipiens).

In addition, the spurge family (Euphorbiaceae) was also useful for honey bee feed. For instance, the rubber tree (Hevea brasiliensis), croton (Codiaeum spp.), cassava (Manihot esculenta), bignay (Antidesma bunius), castor bean (Ricinus communis), asthma plant (Euphorbia hirta), poinsettia (Euphorbia pulcherrima) (Table 1). The rubber tree (Hevea brasiliensis) and northern wattle (Akasia crassicarpa) are now the main supporters of honey bee production at the Kembang Joyo Sriwijaya company located in Karang Ploso, Malang East Java [12]. [3] reported that western honey bee (Apis mellifera L.) has the potential for producing mix beeswax.

4. Conclusions

The diversity of flowers which supply the pollen and also nectar in residential area, campus area, and urban area, have an implication for the development of the local honey bee industry. The shape and size of pollen vary in each family, even in one type of plant in the same flower may have two pollen morphology. Availability the type of family member and development locations which located in urban areas causing the limitation to the development of the local honey bee industry. The diversity of plant species shows the implications of the availability of bee food in the form of pollen and honey glands. The collaborative partnership between scientists and industrial enterprise (PT Kembang Joyo Sriwijaya Karang Ploso) also helps small honey bee farmers in suburban areas around the honey factory. However, it can be used as a learning innovation and unique honey bee cultivation model. Based on a survey at Brawijaya University and residential area Sawojajar in Malang City, the diversity of species that have the potential to develop honey production in urban areas includes 43 families. The nest of Trigona sp. and Apis spp. can be found in the place of dry bamboo, doors, windows, mounds of soil, trees, caves, dry wood, wood holes, house tiles, plant pots, coconut tree holes, gravestones, and cauldron.

ACKNOWLEDGEMENTS

This study was supported and funded by RISPRO LPDP (Indonesia Endowment Fund For Education), the Ministry of Finance of the Republic of Indonesia (PRJ-45/LPDP/2019).