Temporal resource partitioning of the flight activities of three bee species in East Java

Pembagian sumber daya temporal dari aktivitas terbang tiga spesies lebah di Jawa Timur

The dwarf honey bee Apis florea Fabricius, was successful coexistence with larger bees, Apis cerana Fabricius and Apis dorsata Fabricius in Bangalore, India. However, there is a lack of A. florea foraging behavior that shared the same plant resources with A. cerana and stingless bee Tetragonula laeviceps (Smith) in Indonesia. This study investigated the foraging activities of two honey bee species (A. florea and A. cerana) and the stingless bee T. laeviceps, which live sympatrically and also seek environmental factors that influence the foraging behavior of bees. The flight activity was recorded on the bee farm at Jombang Regency, East Java Province, from 06.00–16.00 hours for three consecutive days. Environmental factors of temperature, humidity, and light intensity in open and close to the nest areas were recorded. This study reported that A. florea started foraging activity at 09.00, while A. cerana and T. laeviceps started to forage earlier, at 06.00 in the morning. Therefore, the foraging activities of bees in East Java, revealed temporal resource partitioning, which confirmed the results of a previous study in Bangalore. The temperature and humidity mainly influenced the foraging activity of the three bee species (P<0,001). Temporal resource partitioning in A. florea suggests a foraging strategy that coexists with sympatric honeybees and stingless bees. The high flight activity of A. florea at midday suggests that this species can adapt to high temperatures. This result implies that A. florea could be a potential future pollinator in tropical regions facing the issue of a warming climate.

INTRODUCTION

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.

MATERIAL AND METHOD

Study sites and bee colonies

This study was conducted at a beekeeping farm in Sumbernongko Village, Ngusikan District, Jombang Regency, East Java Province, Indonesia, in July 2023 (Figure 1). The study site was located in a rural lowland area (35–40 m above mean sea level) with dominant plants of Calliandra calothyrsus (Calliandra), Tectona grandis (teak), and Bambusa sp. (bamboo) (Figure 2). Each colony of A. florea, A. cerana, and stingless bees (T. laeviceps) is located in one habitat of a rural garden. The A. florea colony was located between A. cerana and T. laeviceps. The distance between A. florea and A. cerana was close to 52.2 m, which was similar to the distance between A. florea and T. laeviceps at 31.3 m (Table 1). Based on the information from the beekeeper, the colony of A. florea originated from the Lamongan Regency and was successfully established for two years in the Jombang studied area. Therefore, A. florea has adapted to plant resources, as well as to other sympatric bee species.

Observation of the flight activities of the bees

Flight activity was observed in each colony of A. florea, A. cerana, and T. laeviceps for three consecutive days from 1 ^st to 3 ^rd July 2023. Three types of flight activities were observed: (1) the number of bees flying out of the nest (FO), (2) the number of bees returning to the nest without pollen (RWoP), and (3) the number of bees returning to the nest with pollen (RWP)(Raffiudin et al., 2022). The flight activity was observed by the direct method in 10 minutes with 10-minute intervals, starting from to 06.00–16.00, and the video of the flight activity was recorded (Pierrot & Schlindwein, 2003). The number of FO, RWP, and RWoP bees was counted using a hand counter. RWP bees are known to carry bee pollen in the pollen basket. a thermo hygrometer, and the light intensity was measured using a lux meter.

Figure 1.The landscape map of Sumbernongko Village, Jombang Regency, showing Apis florea, Apis cerana, and Tetragonula laeviceps colony location in one habitat.

Figure 2.The study site is a farm with the dominant plant of Calliandra calothyrsus in the South (A) and North (B) area, Tectona grandis in the West (C) area, and Bombusa sp. in the East (D) area.

Table 1.Study sites of three different species of Apis florea, Apis cerana, and Tetragonula laeviceps and colony distance

Species	Nest distance from Apis florea	Coordinates	Sample code
Apis florea	-	-7°24’51.388”S 112°19’25.992”E	Af1.Sbn_JMB
Apis cerana	52,2	-7°24’51.221”S 112°19’28.037”E	Ac1.Sbn_JMB
Tetragonola laeviceps	31,3	-7°24’52.406”S 112°19’25.951”E	Tl1.Sbn_JMB

Environmental parameter measurement

To understand the effect of environmental factors on bee flight activity, environmental parameters, including open area light intensity (lux), close to the nest or bee hive light intensity (lux), humidity (%), and temperature (°C) were recorded every 10 min during the interval time (Raffiudin et al., 2022). The open area light intensity was measured in the open middle area of the research station, whereas humidity, temperature, and close to the nest/hive light intensity were measured in the near area around 1 m of each bee colony. The temperature and humidity were measured using a thermo hygrometer, and the light intensity was measured using a lux meter.

Data analysis

The graphs of the mean bee’s number of flight activities every hour were constructed to show each bee’s daily flight activity pattern. General linear models (GLM) with a Gaussian distribution performed using R(Team, 2020) were used to determine the effect of light intensity both in the open area and close to the nest, humidity, and temperature on FO, RWP, and RWoP activity of A. florea, A. cerana, and T. laeviceps. The average number of bees in flight activity every hour was correlated with environmental factors to investigate the pattern of honey bee flight activity under the influence of environmental factors.

RESULTS

The flight activity of A. florea, A. cerana, and T. laeviceps

Among all bee species, A. florea showed the lowest number of flight activities (Figure 3), with a single noon peak at 11.00–1200. The highest numbers of A. florea for FO, RWP, and RWoP activity were 303, 61, and 238, respectively. Apis florea started flight activities later than the other two bee species. We observed no A. florea in the early morning. The bees started flight activity at 09.00 and peaked at noon 12.00. Subsequently, the flight of this dwarf honey bee decreased to 13.00 and ended at 16.00.

The flight observation showed that the 06.00-morning forage of A. cerana and T. laeviceps occurred much earlier than A. florea. Tetragonula laeviceps also had a single morning peak for all flight activities from 08.00 to 09.00, with the highest numbers of FO, RWP, and RWoP bees being 665, 267, and 242, respectively. The stingless bee T. laeviceps increased its flight activity from 06.00 to 09.00 and decreased from 10.00 to 16.00. The lowest number of individual activities of T. laeviceps was recorded for FO, RWP, and RWoP, at 96, 28, and 70, respectively.

However, A. cerana has two peaks in the morning, 07.00–08.00 and noon, 12.00–13.00, which differs from other bees. The first peak fly activity of A. cerana revealed the number of bees of FO, RWP, and RWoP consecutively at 695, 614, and 306, respectively, while for the second peak consecutive, 612, 258, and 398, respectively.

A different flight activity pattern was observed in A. cerana; at 06.00, the flight activity was high and peaked until 08.00, then decreased until 10.00, with 141, 63, and 117 individuals, respectively. Apis cerana performed at a second peak of 13.00 and started to decease from 14.00 to 16.00.

Figure 3.The average number and standar deviation of flight activities of the sympatric Apis florea, A. cerana, and Tetragonula laeviceps in Jombang District, Province of East Java. A: FO = flying out; B: RWP = returning with pollen; C: RWoP = returning without pollen, AF = A. florea; AC = A. cerana; TL = T. laeviceps.

Environmental factors influence the flight activity pattern of honey bees and stingless bees.

The environmental factors of humidity, temperature, and closed to the nest light intensity and open area light intensity fluctuated during the three observation days Figure 4 All flight activities of A. florea were more influenced by humidity recorded near the nest than those of the other honey bees (Figure 5A–C). The flight of this dwarf honey bee was in the range of 55–67% humidity. When the humidity was higher than 79%, the flight of A. florea significantly decreased, while the flight of A. cerana and T. laeviceps were started to decrease when the humidity higher than 88%.

Temperature close to the nest or hive of the bees had a different impact on flight activity; a higher temperature at the start of fly activity was observed in A. florea compared to other species (Figure 5D–F). At a temperature of 25 ^o C, A. cerana and T. laeviceps were active; however, we found that A. florea starting their flight temperature was six degrees higher (31 ^o C) than sympatric bees. Among all bees, only A. florea increased flight activity by the increasing open-area light intensity, while no pattern was observed for the other bees see (Figure 5G–I). The flight activities of bees showed the same pattern for closed to nest light intensity (Figure 6).

The GLM analysis showed different correlations between flight activity and environmental factors for the three species (Table 2.) The FO flight activity of A. cerana was affected by temperature (P < 0.01) (Table 2). RWP was highly affected (P < 0.001) by all environmental factors. In contrast, the RWoP of A. cerana was not affected by any environmental factor (P < 0.1; P > 0.1) (Table 2). Tetragonula laeviceps showed mostly the same activity as A. cerana. The FO was affected by temperature and humidity (P < 0.001). In contrast, none of the environmental factors affected the RWoP of T. laeviceps. However, all activity records for A. florea were affected by all environmental factors (P < 0.001) (Table 2).

Figure 4.The abiotic factor measured in the location closed to the nest (A–C: humidity; D–F: temperature), and middle area of research station (G–I: open area light intensity) that affected flight activity of three bee species. AC: Apis cerana; AF: Apis florea; TL: Tetragonula laeviceps.

Figure 5.The abiotic factor measured in the location closed to the nest (A–C: humidity; D–F: temperature), and middle area of research station (G–I: open area light intensity) that affected flight activity of three bee species. AC: Apis cerana; AF: Apis florea; TL: Tetragonula laeviceps.

Figure 6.The light intensity measured in the location close to the nest of Apis florea or hive of A. cerana and Tetragonula laeviceps affected flight activity in those three bee species (A: A. florea;B:A. cerana;and C: T. laeviceps).

Table 2.Correlation among flight activities of Apis florea (AF), Apis cerana (AC), and Tetragonula laeviceps (TL), with the three environmental factors, i.e., temperature, humidity, and light intensity based on generalized linear model analysis

Species	Activity	Temperature		Humidity		Open area light intensity		Closed to the nest light intensity
		Estimate	P	Estimate	P	Estimate	P	Estimate	P
AF - JMB	FO	21.481	<0.001	-5.5496	<0.001	0.0047195	<0.001	0.1428	<0.001
	RWP	4.689	<0.001	1.2129	<0.001	0.0011969	<0.001	0.045703	<0.001
	RWoP	19.432	<0.001	-5.0656	<0.001	0.0042816	<0.001	0.16816	<0.001
AC - JMB	FO	-17.242	<0.01	3.305	<0.05	-0.002888	<0.05	0.006112	<0.1
	RWP	-32.003	<0.001	8.158	<0.001	0.004919	<0.001	-0.01169	<0.01
	RWoP	5.781	>0.1	-1.994	<0.1	0.0005350	>0.1	0.002638	>0.1
TL - JMB	FO	-20.829	<0.001	6.815	<0.001	-0.002000	>0.1	-0.1934	>0.1
	RWP	-13.263	<0.001	4.6676	<0.001	-0.002240	>0.01	-0.1593	<0.05
	RWoP	0.237	>0.1	0.9101	>0.1	0.001429	>0.1	0.1362	>0.1

DISCUSSION

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).

CONCLUSION

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.

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