Bees are important pollinator insects for wild plants, such as bushes, small trees, and herbaceous plants, and are the best pollinators of crop plants (Michener, 2000). The native honey bees in Indonesia, Apis dorsata Fabricius, A. cerana Fabricius, A. andreniformis Smith, and the stingless bee Tetragonula laeviceps (Smith) are known as dominant pollinators in agriculture (Siregar et al., 2016). Apis cerana is a natural pollinator of crop plants such as tomato (Solanum lycopersicum L.) (Putra & Kinasih, 2013), physic nut (Jatropha curcas L.) (Atmowidi et al., 2008), field mustard (Brassica rapa L.) (Atmowidi et al., 2007), and cucumber (Cucumis sativus L.) (Chauhan & Singh, 2022).

In Indonesia, A. cerana is a popular honeybee species in beekeeping (Buchori et al., 2022). This eastern honey bee is well distributed in almost all Asian regions with various habitats ranging from highly humid forests to dry savannahs (Hepburn & Radloff, 2011).(Radloff et al., 2010) summarized that A. cerana is distributed from Afghanistan to the north in Russia, to the East in China and Japan, and the bees spread to South and Southeast Asia up to Indonesia and Timor. The subspecies of A. cerana javana (Engel, 1999) is distributed from Java to Timor. Apis cerana is distributed across the Indonesian archipelago and shows high genetic diversity, whereas in some areas, such as Mollucas Island, West Papua (Raffiudin et al., 2022), and Sumatera (Simanjuntak et al., 2024), this species is distributed from Java through anthropogenic activity.

Another potential natural wild honey bee pollinator is the red dwarf honey bee A. florea. This honey bees pollinate crops in India, including carrots (Abrol, 2006)and onions (Abrol, 2010). Apis florea and A. cerana are sympatric species on Java (Ruttner, 1988). Apis florea was found in Tanjung Priok and Ancol Harbor, Jakarta (Maa, 1953), whereas in East Java, this dwarf honey bee was found on a ship in Surabaya (Otis, 1996), presumably carried by human transport(Hepburn & Hepburn, 2005). Originally, A. florea was native to South Asia, including India, Pakistan, and Southeast Asia in Cambodia, Myanmar, and Thailand (Otis, 1996). However, the hypothesis that A. florea was introduced into Indonesia (Otis, 1996);(Engel, 2012) has not been proven.

Besides honeybees, stingless bees are also favorable for beekeepers in Indonesia because they are easy to handle (Kahono et al., 2018). Indonesia has 46 stingless bee species (Engel et al., 2019), and a recent study showed that the number of stingless bee species in Indonesia has reached 52 species (Purwanto et al., 2022). Tetragonula laeviceps is the most commonly chosen stingless bee by beekeepers in Indonesia (Syafrizal et al., 2020);(Hanifa et al., 2021).

In urban areas, the foragers of T. laeviceps stingless bees have the flower consistency needed for cross-pollination (Atmowidi et al., 2022). This species is a potential pollinator of the rubber tree Hevea brasiliensis (Ramadani et al., 2021);(Pulungan et al., 2023) and several families of medicinal plants (Prasetyo et al., 2022). Furthermore, T. laeviceps can improve fruit formation in strawberries (Fragaria x annanassa) (Atmowidi et al., 2022) and Mauritius raspberry (Rubus rosifolius) (Putra et al., 2024).

Information on foraging activity is needed to better understand the potential of pollination services for sympatric honey bees. Based on body size, A. florea is the smallest Apis species and is inferior to the larger honey bee, A. cerana (Oldroyd et al., 1992). In the same foraging area, A. cerana started to forage in the early morning and A. florea started foraging activity in the late morning. Thus, it showed time partitioning strategies between sympatric honey bees (Young et al., 2021). However, the information on A. florea’s existence, distribution, and foraging behavior of A. florea in Java are yet to be explored. Therefore, we investigated the foraging activities of A. florea, A. cerana, and T. laeviceps in the same beekeeping farm area in Jombang Regency, East Java. We also aimed to identify the environmental factors that influence bee foraging behavior.

The flight activity pattern shows the time partitioning strategy between A. florea, A. cerana, and T. laeviceps. Based on observations of these three sympatric species, a general pattern of daily foraging activity showed that A. cerana was highly foraged in the early morning between 07.00–08.00 and 08.00–09.00 hours for T. laeviceps. In contrast, at 09.00 A. florea began to forage. This pattern is consistent with (Young et al., 2021), who stated that A. cerana starts to fly at 07.00, and the highest is at 08.00 to 09.00 hours, while A. florea begins to fly later at 09.00 or 10.00 hours and increases at noon. This phenomenon revealed the temporal partitioning of A. florea with those of A. cerana and T. laeviceps; the former increased the number of flights during the day, while A. cerana and T. laeviceps slightly decreased their flight activities. Our study confirmed that A. florea performed temporal resource partitioning during their foraging activity when the colonies of A. florea were similar to other species of honey bees, as shown by(Young et al., 2021), who sympatric with A. cerana and A. dorsata.

Apis florea in Yunnan, China, also showed a short flight activity period of only 2–4 hours during midday and 6 hours at maximum (Cui & Corlett, 2016). The high flight activity of A. florea during midday could be facilitated by its small body size, which can adapt to high temperatures. The small body-sized insects showed low body heat loss during flight; thus, they rarely overheated (Digby, 1955). Small stingless bees lose and warm up their body temperature more rapidly than large stingless bees(Pereboom & Biesmeijer, 2003) because of their larger body surface size per unit weight compared to other bees (Hill et al., 2012). The smaller body size of bees is also favorable because they require less power for flight (Grula et al., 2021). On the other hand, (Young et al., 2021) explained that A. cerana in Bangalore, India, decreased flights during midday might be due to the high temperature. Therefore, A. cerana was optimized by their high foraging activity in the morning due to the abundance of nectar resources. The decreasing activity of A. cerana at midday is similar to A. dorsata in Serdang, Selangor, Malaysia, which might also be a result of heat stress (Mardan & Kevan, 2002). Thus, our findings clearly showed that A. florea could adapt more to high-temperature environments than A. cerana. This ability is advantageous for A. florea to actively forage during midday, although nectar sources are limited. This dwarf red honey bee can also coexist with another bee that actively forages in the morning.

Similar to A. cerana, the flight activity of stingless bees was high in the morning and decreased during the day. This result is supported by the flight activity of T. laeviceps in Jambi, Sumatera (Pulungan et al., 2023), and Bogor, West Java(Prasetyo et al., 2022) that showed high flight activity in the morning from 08.00 to 10.00 and decrease during midday. In another study, the abundance of A. cerana and T. iridipennis (Smith) showed peak activity in the 10.00–12.00 middle of the day (Danaraddi, 2007), while in Kerala, India, T. iridipennis peak foraging activity is in the morning and afternoon (Mythri et al., 2023). The similarity in flight activity patterns between A. cerana and T. laeviceps might lead to interspecific competition, showing that stingless bees have a lower foraging index than honey bees (O & MP, 2007).

The foraging activities of the three bee species are influenced mainly by temperature and humidity. In the present study, the flight activities of FO and RWP in A. cerana were significantly influenced by light intensity, humidity, and temperature. During flight, the thorax temperature required by A. cerana should be above 27 °C, while the body temperature limit of A. cerana is 45–50 °C (Abrol, 2013), or up to 55 °C (Li et al., 2019). High tolerance to temperate climates facilitates the wide distribution of A. cerana (Abrol, 2020).

However, the flying activity of T. laeviceps is influenced more by temperature and humidity than by open and closed to the nest light intensity. This might be due to the foraging of stingless bees being assisted by pheromone trails, which differs from solar compass navigation in honey bees (Hrncir & Maia-Silva, 2013).

The daytime flight activity of A. florea occurred as the temperature and light intensity increased and was significantly influenced by temperature and humidity (Table 2). Visiting A. florea on flowering plants in the highlands of Yunan Province, China, has a positive relationship with air temperature (Cui & Corlett, 2016) and agrees with the midday activity of this dwarf honey bee (Young et al., 2021). Apis florea has a higher minimum and maximum temperature threshold, i.e.16–46,5 °C, compared to 7–41,5 °C of A. cerana (Cui & Corlett, 2016).

Our main finding of the high flight activity of A. florea during the increasing temperature of the day showed the adaptation of the bees to the higher temperature compared to other sympatric bee species. Thus, our results imply that A. florea is a potential pollinator under warming climate conditions. Attention to climate change can lead to a decrease in natural pollinators. Moreover, the production of pollinator dependent crops (Reilly et al., 2020) is affected by homogenous and fragmented landscapes (Vasiliev & Greenwood, 2021).

The sympatrics of honey bee A. florea and A. cerana and stingless bee T. laeviceps have unique foraging activities that can be used for resource partitioning. Apis florea showed midday foraging activity compared to early morning foraging A. cerana and T. laeviceps. The different activities of the three bee species were also influenced by temperature and humidity. Thus, A. florea can forage at a higher temperature than other bees. This partitioning foraging strategy showed the adaptation of A. florea to high temperatures, which might be potential pollinators in warming climate conditions.