Acta Biológica Colombiana

INTRODUCTION

Honey bees are social insects known for their heat-balancing skills. Thanks to these features, bees are found worldwide, from temperate regions to cold climates (Southwick and Heldmaier, 1987; Kovac et al., 2009; Stabentheiner et al., 2021). For life to continue within the colony, the environment's temperature, humidity, and gas content must be balanced (Southwick and Moritz, 1987). Honeybees also have to operate in a colonial form to achieve these balances (Bonon et al., 2014). With such structures, it is considered that the life of a colony is theoretically infinite. With their physiological and behavioral properties, honey bees are much more specific than other insects. The temperature stabilization capabilities of honey bees, called homeostasis, have been known for a long time. This feature occurs in the form of increased body temperatures at low ambient temperatures and reduced body temperatures at high temperatures (Southwick and Heldmaier, 1987).

The continuation of colonial life necessitates the continuous production of broods. Homeostasis, which ensures this production, involves responses to environmental changes to maintain the temperature required for brood production (Southwick and Heldmaier, 1987; Bonon et al., 2014; Stabentheiner et al., 2021). Even small deviations $(0.5°C)$ in brood area temperature have significant effects on brood development and colony health. Honey bees that are not raised in favorable conditions are more susceptible to diseases, pests, and environmental conditions (Tautz, 2008).

Honey bee larvae and pupae, which are highly stenothermic (Tautz, 2008; Becker et al., 2009), require a brood area at $32-36°C$ for normal development (Seeley and Heinrich, 1981; Kronenberg and Heller, 1982; Kleinhenz et al., 2003; Petz et al., 2004). Thermal homeostasis of the colony is therefore especially important for the broods. Open brood cells (eggs and larvae) can tolerate low temperatures for a short period, while sealed brood cells (pupae) are more sensitive to these temperatures (Wang et al., 2016). Since the brood cannot regulate temperature (Petz et al., 2004), thermal constancy within the colony must be maintained by worker bees (Stabentheiner et al., 2010). Therefore, thermoregulation is more pronounced when there is a high level of brood presence in the colony (Southwick, 1985; Kleinhenz et al., 2003; Stabentheiner et al., 2010). For adult honey bees, on the other hand, low or high temperatures can cause behavioral and neural abnormalities (Stabentheiner et al., 2021).

In a cold environment, honey bees try to transfer their body heat, which they raise to warm the brood area, to the brood. For this purpose, worker bees press their heat on their pupa fields and transfer heat into their cells. Honeybees can increase their chest temperature to $43°C$ and maintain this level for 30 minutes (Tautz, 2008). To prevent heat loss, other worker bees tightly cover the brood area. Given that a bee will die when its body temperature reaches $45°C$, it will be revealed how sensitive and vital this stage is (Abou-Shaara et al., 2012; Stabentheiner et al., 2021; Millers Homestead, n.d.).

The thermal conditions that are a source of stress for honey bee colonies are not only related to cold weather. Honey bees respond to temperature changes with behavioral or metabolic adaptations (Heinrich and Esch, 1994; Zhao et al., 2021; Jhawar et al., 2023). At high temperatures that are likely to disrupt colony life, honey bees activate different cooling mechanisms. If the internal temperature of the hive rises above normal levels, bees ventilate using their wings. For ventilation, one group of worker bees circulates the air by sending fresh air in, while another group circulates hot air out of the hive. In this way, they try to reduce the temperature inside the hive to $35°C$ (Southwick and Heldmaier, 1987).

If the temperature in the brood area approaches a critical level, there is an increase in the number of foragers collecting water to lower the hive temperature, and they start collecting water (Kovac et al., 2018; Zhao et al., 2021). They sprinkle water droplets all over the hive, including the egg and larval areas (Southwick and Heldmaier, 1987; Jarimi et al., 2020; Zhao et al., 2021). By evaporating the water, they try to lower the internal temperature while preventing the open brood from drying out. In addition to the clean water carried into the hive, some water produced by the worker bees during the processing of nectar can also be used for this purpose.

Another method used by honey bees to protect their brood in a hive with increasing temperatures is for young worker bees to absorb heat by pressing the ventral side of their body against the heated surface. The heat-absorbing bees then distribute this heat to cooler areas of the hive (Bonon et al., 2014). However, if cooling measures are insufficient, many honey bees will leave the hive and form clusters outside the hive, and a new division of labor in the colony will take place (Zhao et al., 2021).

In global warming scenarios, the effects of which are beginning to be seen and which pose different dangers for the future, high environmental temperatures are expected to put honey bee colonies in difficulty (Stabentheiner et al., 2021). Overheating of the hive, which limits the activity of the bees, must therefore be considered.

Honey bees are directly affected by temperature changes in their life in conventional hives. Even if breeding is carefully planned, some factors, such as temperature, cannot allow honey bees to reach a completely comfortable state (Souza et al., 2015).

Some suggestions have been developed to increase colony productivity by reducing temperature stress in breeding, such as ventilated and insulated hives and providing shade. In addition to these, hive color is also an important issue to be considered. Although it is general knowledge that light colors reflect sunlight and dark colors absorb it, it will be useful for colony management to evaluate the influence of color in the hive. In the study prepared for this purpose, the effect of three combinations of white and blue colors on hive internal temperature was tried to be revealed. Thus, suggestions were proposed for breeding and honey bee welfare.

MATERIALS AND METHODS

RESULTS

The introductory statistics for each group resulting from the study are presented in Table 1.

Table 1.: Introductory statistics

According to the results of one-way analysis of variance regarding the hive colors and their impact on these data, the difference among the three-color ranges in terms of average temperature was found to be statistically significant (p<0.001). Subsequently, Duncan Multiple Range Test results were applied to the data to identify the specific color levels that differed, as shown in Table 2.

Table 2.: Duncan Multiple Range Test Results

According to Duncan's Multiple Range Test results, each color group exhibited a significant difference in average temperature. Specifically, the highest average temperature was recorded in the blue group at $24.93°C$ followed by the white/blue group at $24.26°C$, and lastly, the white group at $22.36°C$.

In the study, considering that ambient temperature could be more impactful on in-hive temperature during certain times of the day, the data between 10:00 a.m. and 5:00 p.m. were separately analyzed, and the relevant statistical tests were repeated.

Table 3.: Introductory Statistics for hours between 10.00 a.m. -5.00 p.m.

According to the one-way analysis of variance results for the data recorded between 10:00 a.m. and 5:00 p.m., the difference among the three-color levels in average temperature was also found to be statistically significant (p<0.001). Detailed temperature values and Duncan Multiple Range Test results are presented in Table 4.

Table 4.: Duncan Multiple Range Test Results for hours between 10.00 a.m -5.00 p.m

Overall, in terms of average temperature, all three-color groups exhibited differences, consistent with the findings from the entire day's data. The Duncan Lettering Boxplot (Fig. 1) chart below provides an alternative visualization of the study's results.

Figure 1.: Box-Plot Chart for hours between 10.00 a.m. -5.00 p.m.

DISCUSSION

In this study, which aimed to examine the potential effects of hive color on honey bee colony performance, the temperature averages recorded every 59 minutes from white, white/blue, and blue hives were calculated as $22.36\pm 7.23°C$, $24.26\pm 8.27°C$, and $24.93\pm 8.91°C$, respectively, for the entire day; and as $30.47\pm 3.90°C$, $33.28\pm 3.34°C$, and $34.90\pm 4.92°C$, respectively, for the hours between 10:00 a.m. - 5:00 p.m. Consequently, the white color group showed a lower temperature average when considering data for the entire day and the hot hours. If these values obtained in empty hives are recorded in colonized hives, they will likely increase due to various activities.

A hive internal temperature exceeding $36°C$ is harmful to honey bees. Even an increase of $1-2°C$ in this value can lead to the death of offspring in the comb cells (Winston, 1991). The maximum values obtained for all three groups in the experiment exceeded this limit.

The thermal homeostasis in the colony is achieved through the collaboration of thousands of bees (Stabentheiner et al., 2010; Cook et al., 2016). Worker bees, aiming to maintain the internal temperature of the hive between $32-35°C$ to prevent overheating (Heinrich, 1980; Seeley, 1985; Tautz, 2008; Kovac et al., 2018), attempt to cool the hive by ventilating and evaporating the water they bring into the hive (Southwick and Heldmaier, 1987; Kovac et al., 2018; Zhao et al., 2021). If all efforts prove insufficient, the colony may leave the hive (Santos et al., 2017).

All activities to reduce the inside temperature of the hive result in significant energy and time losses. Honey bees assigned to brood care focus on hive ventilation, while those collecting nectar and pollen concentrate on water transport (Kühnholz and Seeley, 1997). The unreduced internal temperature of the hive can render individuals in the brood stage more susceptible to diseases and pests, reduce their lifespan, and damage the wax material.

So far, studies have shown that even when the environmental temperature reaches $60°C$, honey bees can maintain a balance at $35-36°C$ (Millers Homestead, n.d.). This super community can provide air changes, reaching $60\text{l/min}$ when needed (Southwick and Heldmaier, 1987), and can continue ventilation for hours.

Another method to reduce the high temperature inside the hive is to vaporize the water brought into the hive. Under normal conditions, the colony's water needs are around 0.12 liters per day (Hegic and Bubalo, 2006), but this rate can increase further during activities and high environmental temperatures. The energy consumed to evaporate every gram of water used to reduce ambient temperature and provide the required humidity is approximately 580 cal (Al-Rajhi, 2017).

The activities carried out by worker bees to ensure thermoregulation result in a waste of energy and time. Additionally, uncontrolled temperature increases cause damage to the brood.

The main recommendations to protect colonies from high temperatures include providing ventilation to hives and shade (Lopes et al., 2011). Al-Rajhi (2017), who evaluated shading and ventilation together, found that it is more advantageous to produce with colonies with good ventilation and shade in summer. Additionally, in one of the rare studies on hive color, Mitchener (1940) stated that the white color of hives has a positive effect on internal temperature. Similarly, Souza et al. (2015) recorded lower internal temperatures in white-colored hives compared to blue-colored hives.

When considering the hot hours of the day (10:00 a.m.- 5:00 p.m.) in the study, a difference of $4.43°C$ was observed between the blue and white color groups. This difference was calculated as $6.40°C$ at maximum values. The temperature difference caused by painting the covers white in blue hives is $1.62°C$. The same difference was $3.20°C$ at maximum values. These temperature changes mean that the bees in the blue hives will spend more effort on thermoregulation than the others.

Honey bees are highly dependent on nature, and many environmental factors affect their lives. High temperatures are among these factors, and global climate changes are increasingly affecting colonies every day.

CONCLUSIONS

As a result of the study, only the internal temperature differences caused by the different colors of the hives were revealed. With the obtained data, it was found that, in addition to insulation, shading, and ventilation arrangements to enhance the performance of honey bee colonies on hot summer days, the white color of the hive significantly contributes to colony performance. Additionally, placing geometric shapes in different colors at hive entrances will be sufficient to eliminate errors that bees may encounter in finding the right hive when all hives are painted white, especially in crowded apiaries with dense colonies.