Exploring wax moth infestation in Burkina Faso: A study on prevalence, risk factors, and beekeepers’ practices

Introduction

One of the most significant challenges that the beekeeping industry faces is the disappearance of bee colonies, which is commonly known as colony collapse disorder [1] . The causes of this phenomenon are complex, with research indicating that it is the result of a combination of pathogens, parasites, and pesticides [2,3] . Colony collapse disorder not only results in bee mortality but also has economic and ecological implications [4] . Therefore, it is crucial to address this issue to ensure the sustainable development of the beekeeping industry. Indeed, beekeeping offers global benefits that are intricately connected to health, the economy, employment and the environment and plays a pivotal role in ensuring sustainable livelihoods by transforming vulnerability into security [5] . Beekeeping is also an important source of income diversification for beekeepers. The beekeeping sector in Burkina Faso is numerically significant, with over 16,000 beekeepers and more than 132,000 operational hives. However, the beekeeping is facing many constraints including sanitary ones and recent specific preliminary studies on the prevalence of wax moth and Varroa spp. infestations in bee colonies in Burkina Faso [6,7] have revealed a prevalence of 23.6% for wax moth infestation and 91.7% for Varroa spp. infestation. These infestations can lead to substantial losses in bee colonies and have a notable impact on the beekeeping economy, particularly in tropical regions [8] , where beekeepers often possess limited knowledge about bee health [9] . Certainly, the wax moth stands out as a highly significant threat to honeybee products, earning its reputation as one of the foremost pests in this context [10,11] . Therefore, there is a pressing need for more research into bee parasite/predator epidemiology and control measures in Burkina Faso to ensure the sustainability of the beekeeping industry.

To advance the understanding of the wax moth and enable effective control measures, an investigation was conducted over a larger beekeeping region. The specific objective was to evaluate the prevalence and associated risk factors as well as the knowledge and practices of beekeepers in the Central, Centre-East, Centre-West and Central Plateau regions of Burkina Faso with respect to wax moth infestation.

Materials and Methods

Study area:

The study was conducted in four administrative regions of Burkina Faso, including the Centre, Centre-East, Centre-West and Central Plateau regions (Fig 1).

Method of data collection 2.2.1 Sampling

The sample size was calculated based on an expected prevalence (p) of 23.6% 6 and a precision (e) of 5%. Using the sample size formula n=z²pq/e², a minimum sample size of 260 should be used for this study. During the investigation, a total of 296 hives belonging to 17 beekeepers were inspected for signs of wax moth infestation. The search for wax moth consisted of direct identification of the signs of wax moths by sanitary inspection of the hives: larvae, pupae, galleries in the wax and woven silk on the wax combs, in order to confirm the presence of wax moth infestation. A semi-structured questionnaire on the socio-economic characteristics of the beekeepers, the characteristics of the farms and the knowledge and practices regarding wax moth infestation was administered to the beekeepers to gather additional information.

Inspection of hives and colonies

The observation of the hives in each apiary was done after the interview with the beekeeper. Data was collected using a preprepared observation form. Only hives already colonized were inspected on the farm. After each hive was opened, observations were made to identify moths escaping from the hive or signs of wax moth inside the roof and above the bars. The combs were then removed and examined for larvae, pupal cocoons or galleries in the wax or woven silk. Finally, the walls and bottom of the hive were inspected for signs of wax moth. Other pests present in the hive were reported and colony strength was estimated using the criteria described by Kebede et al. [12] .

Statistical analysis of data

The data collected from beekeepers and hive inspections were entered into a Microsoft Excel spreadsheet (version 2019), which was used to create tables and some graphs. The database was then transferred to R Studio (version R 4.2.0) for further analysis. Descriptive statistics were used to determine parameters such as proportions, averages, standard deviations and maximum/minimum values. The association between categorical explanatory variables (related to beekeeper and apiary characteristics) and the prevalence (dependent variable) was evaluated using Pearson's Chisquare test with Yates' continuity correction and/or Fischer's exact test. The analysis of risk factors associated with colony infestation was done using logistic regression. Both univariate and multivariate logistic regression were employed to ascertain the variables that showed significant associations with infestation. These variables included region, apiary size, hive type, colony strength and colony feeding status.

Results

Description of beekeeper characteristics and beekeeping practices

The beekeepers surveyed in our study were all men with an average age of 55.2±9.5 and were mostly educated (table I). On average, they had 18 years of experience in beekeeping, and 94.1% (16/17) of the respondents had received training in beekeeping. About 76% of the beekeepers were involved in beekeeping associations. The acquisition of essential resources for beekeeping varied among the beekeepers. Approximately 70% of the beekeepers acquired their equipment with their own funds and/or through subsidies (12/17), while 58.8% (10/17) benefited from donations and 29.41% proceeded with self-confection. The motivations for conducting beekeeping were varied (figure 2), but profitability remained the main one. The data collected on beekeeping practices allowed for the identification of production techniques and colony management strategies in the study area, as shown in table II.

The majority of respondents practiced modern beekeeping, using modern equipment and techniques for production, and harvesting. The hives owned by the respondents were mainly of modern types, with 48.3% French hives, 41.9% Kenyan hives, 2.7% Dadant hives, and only 7.1% traditional hives.

Regarding the management of colonies, only 5.9% of the respondents provided food in times of shortage by using honey syrup, while 76.5% of the respondents provided water.

When it comes to visits to the apiaries, 76% of the respondents made them at least once a month, 7.8% once every two months, 3.4% only at harvest time, and 12.8% made irregular visits. With an average apiary size of 24±14 hives and an occupancy rate of 70.4%, the respondents used honey (100%), pollen (23.5%), wax (11.8%), propolis (5.9%), and brood (5.9%) in order of importance.

Beekeepers' knowledge and practices regarding the wax moth

All the respondents were aware of the existence of the wax moth in their area, and 82.35% of them observed it in their hives during 2019. The beekeepers surveyed recognized the wax moth mainly based on five (05) elements: moth larvae (100%), woven silk (88.24%), cocoons, and prints on hive frames (82.35%), and adult moths (47.06%). While all beekeepers use cleaning to combat the wax moth, 47.1% of them destroy highly infested frames. On the other hand, very few have means of preventing wax moth, as shown in Table II. Regarding the periods of wax moth recrudescence, Figure 3 illustrates the observations made by the beekeepers. Thus, it appears that there are two main periods of wax moth recrudescence in the year, and the peaks were observed during the months of April (41.2%) and October (64.7%).

Prevalence of wax moth

Out of a total of 296 inspected hives, signs of wax moth were identified in 48 hives, resulting in an overall prevalence of 16.2% [95% CI: 12.0%-20.4%], based on reports of wax moth presence or passage. Table III shows the prevalence according to the detected signs.

Factors influencing the prevalence of wax moth infestation

The analysis of the relationship between variables revealed that the prevalence of wax moth varied significantly according to several factors related to the study area, apiary characteristics, and beekeeper characteristics. The prevalence varied significantly by region, commune, frequency of visits, level of education, and colony strength (p<0.05), (Table IV). Specifically, higher prevalences were observed in the Centre (26.7%) and Centre West (29.3%) regions, as well as in the commune of Sindou (62.5%), compared to other regions and communes. Prevalence was also higher in apiaries belonging to beekeepers without no formal education (21.5%), as well as at those with secondary (24.6%) and university (26.7%) education levels. Membership in an association of beekeepers was also associated with higher prevalence. In terms of colony strength, the prevalence was significantly higher in weak colonies (39.1%) and hives deserted by colonies (32.1%). Finally, prevalence was significantly higher in irregularly visited apiaries (42.1%) and large apiaries, with more than 50 hives (29.3%).

Identification of risk factors for wax moth infestation

The outcomes of the univariate logistic regression (Table V) indicated a significant association between wax moth infestation and variables such as region, apiary size, and colony strength. However, when performing the multivariate logistic regression with adjusted odds ratios, only region and colony strength were identified as risk factors (Table V). Consequently, colonies located in the Center, Central-West, and Central Plateau regions were 13.3, 45.2, and 23.7 times more likely to be infested by wax moths, respectively, compared to colonies in the Central-East region. In terms of colony strength, weak colonies, and deserted colonies (hives) had respectively 39.7-and 47.9 fold higher likelihood of wax moth infestation (p<0.001) when compared to strong colonies. Ultimately, in hives that had not been colonized, the likelihood of infestation was merely 1.3 times greater compared to that of strong colonies.

Other predators/pests

The inspection of the hives revealed the presence of other pests and predators in addition to the wax moth. These predators were found in 57.8% of the inspected hives, with the small hive beetle (34.5%) and ants (31.4%) being the most prevalent (Figure 4).

Discussion

Beekeeping serves as a crucial source of income diversification for many communities, particularly in rural and peri-urban areas. Given its importance, this activity attracts a wide range of investors with diverse motivations. In this study, the characteristics of beekeepers were found to be similar or close to those reported in previous studies. The activity is mainly practiced by men with experience, consistent with the nature of beekeeping in several regions of the country [13,9,7] .

Regarding the level of education, the results reflect the national situation of low rates of schooling and limited access to advanced education. Beekeepers are mainly motivated by the profitability of beekeeping, which reinforces its potential as a promising activity for income diversification and poverty reduction. They acquire production equipment through their own purchases, subsidies, donations, or by self-construction using their endogenous know-how. Technical and financial partners play a role in promoting beekeeping through subsidies and training of actors. However, accessing credit for small-scale producers remains a challenge [14] . Regarding beekeeping practices, the results indicate the predominance of modern hives, specifically the French type, and the use of the smoker during harvesting, consistent with previous studies 13 . However, there was a difference in hive type predominance, with previous studies showing a higher prevalence of Kenyan hives. This could be explained by the promotion of different hive types to beekeepers, which varies according to geographical areas and partners.

In terms of colony management, the main contribution of beekeepers is providing water in the absence of a perennial water source. In the current context of small-scale beekeeping, most beekeepers rely on floral resources for colony survival by building up reserves after the harvest 15 .

While most beekeepers in the study area visit their apiaries regularly, the fact that most only make external visits does not allow for timely detection of the presence of predators or enemies of bee colonies. This could be addressed through improved training and support for effective monitoring practices. Indeed, the majority of beekeepers in Burkina Faso are aware of the existence of wax moth, as reported by previous studies [16, 6] . They are also able to identify the signs of wax moth infestation. Recent awareness-raising and training sessions for beekeepers include information on bee pathologies, as well as predators and pests such as the wax moth, due to the damage and losses they cause. The recent discovery of wax moth infestations in bee colonies highlights the persistence of this problem despite a lack of effective treatments and preventative measures. Beekeepers typically clean infested hives or destroy heavily affected combs to control wax moth, but these methods do not guarantee complete elimination of the pest regardless of its developmental stage. The best way to control wax moth is through good colony management, which includes having strong colonies, providing adequate nectar sources or feeding, repairing cracks and crevices in hives, and regularly monitoring for the presence of parasites and predators [8,17] . However, these measures have limited effectiveness, especially in tropical climates that are favourable for the development of the wax moth and other pests. Thus, it is important to understand the epidemiological aspects of wax moth infestations to develop better control measures through integrated pest management and good beekeeping practices. Indeed, during this study, the of wax moth signs were observed in 16.2% of the inspected hives, which is lower than the 23.6% found in a preliminary wax moth study in the Central and Central-Western regions [6] .

Similarly, the prevalence is lower previous findings in Burkina Faso (90%) [18] , and Kebede et al. [12] in Ethiopia (27.4%). These differences in prevalence can be attributed to variations in the investigation periods and environmental conditions in the different study areas. The development cycle of the wax moth is significantly influenced by environmental factors such as season and temperature, which vary throughout the year and affect the moth's activity [8,19] . The various stages of the wax moth life cycle are influenced by both warm and cool temperatures and the presence of favourable environmental conditions has the potential to enhance wax moth activity. The optimal temperature range for rapid reproduction and development of wax moths is between 28 °C and 30 °C [20,21] and the short duration of the larval to pupal stage is thought to be related to the predominance of cocoons in warm climates, where a pupa can develop and hatch in as little as 3-6 days [20] . Concerning the factors of variation, the prevalence of wax moth was significantly higher in the Centre and Centre-West region but remains close to the 23.6% found by Kaboré et al. [6] in the same area. This level of prevalence would be related to the different beekeeping practices in the zones. Indeed, if in the Central Plateau regions, most beekeepers surveyed visit their colonies at least once a year, those in the other regions visit once every two months or irregularly and sometimes twice a year. The prevalence was significantly higher in apiaries with irregular visits supporting the importance of visits in the implementation of wax moth prevention measures including cleaning of hives, removal of old or unoccupied combs [12,22] . In addition to the factors discussed earlier, the prevalence of wax moth infestation was found to be significantly higher in apiaries with more than 50 hives and in weak colonies. The high prevalence in large apiaries could be due to the heavy workload that prevents beekeepers from regularly checking all hives. Similarly, weak colonies are more vulnerable to wax moth infestations because they have unoccupied combs and are unable to eliminate the different stages of wax moth unlike strong colonies. It is also possible that the high prevalence in deserted colonies may indicate the role of wax moth in the desertion of severely affected colonies.

Our results also showed that beekeeper characteristics were associated with wax moth prevalence. Specifically, membership in an association, lack of education, or high education level were all linked to higher prevalence rates. In the study area, most beekeepers work in associations, which use common equipment without practising disinfection, leading to the spread of infestations. Uneducated beekeepers may have limited access to knowledge of good practices and colony health, while highly educated beekeepers may have other responsibilities that prevent them from managing their colonies properly. The region and colony strength were identified as risk factors. Wax moth development is dependent on climatic conditions, and the environmental conditions in different regions can impact its development and distribution, consequently affecting the risk of infestation in colonies. Ambient temperature is the most influential bioclimatic variable affecting wax moth distribution [23] . In addition, weak colonies and those that have been abandoned appeared to be more susceptible to infestation. The strength of a colony serves as a protective factor against wax moth infestation. Strong colonies can maintain low wax moth populations by occupying all the combs in the hive, and the presence of a significant number of adult bees helps prevent wax moth damage. Although wax moth larvae may occasionally be found in an active and healthy colony, they are promptly removed or rejected [17] . Conversely, in a weak colony, the availability of unoccupied space provides an opportunity for wax moths to hide and develop. The presence of wax moth signs in deserted hives may lead to the abandonment of infested weak colonies that could not effectively eliminate the wax moth infestation. Moreover, previous studies have reported the coexistence of wax moth with other predators/pests in bee colonies [24] . This indicates that while wax moths cause significant damage to bee colonies, the presence of other predators can exacerbate the impact of the threat on the colony and the profitability of the farms. Therefore, implementing good beekeeping practices should take into account the broader spectrum of potential threats to ensure effective colony management and sustainability.

Conclusion

This study, conducted over a wide geographical area, underscores the extensive prevalence of wax moth infestations in bee colonies. Although beekeepers are generally aware of the issue, they often lack effective strategies for controlling this pest in their apiaries. The high incidence of wax moths, coupled with factors such as infrequent colony inspections, large apiary sizes, and weak colonies, suggests that insufficient beekeeping practices are the main contributors to colony vulnerability. To address this challenge, it is recommended that beekeepers prioritize regular colony inspections and undergo training in the sanitary management of bee colonies. Support programs should focus on enhancing beekeeping skills through education on best practices, promoting production guidelines, and strengthening colony health management. Future research should aim to quantify the economic losses attributed to wax moth infestations and investigate integrated pest management approaches. These efforts are essential for developing effective control strategies and ensuring the longterm sustainability of the beekeeping industry

Conflict of Interest Not available

Financial Support

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