Over the last 20 years, large-scale monitoring initiatives have been developed to estimate honey bee colony loss in different regions of the world, of which the LA region was poorly documented [22]. These surveys highlighted generalization of colony losses between 20% and 40% of the livestock of beekeepers each year in the United States [13, 14, 20, 27, 30, 50, 51] and Europe [15–17, 21, 26], leading to important concerns on the sustainability of the beekeeping activity and the crop pollination services. In this study, we present the results of the first large-scale, standardized survey of honey bee and stingless bee colony losses in LA. Based on two years of data collection, our results suggest difficulties for both beekeepers and meliponiculturists in LA. Overall, about one-third of honey bee and stingless bee colonies were lost on average per year in LA. Results are particularly alarming in countries such as Colombia, Bolivia and Brazil, with records of high colony loss rates (above 30% annual losses) for both honey bees and stingless bees. On the other hand, other LA countries such as Mexico, Cuba and Panama have relatively low colony loss rates (below 20% annual loss), illustrating the heterogeneity of situations across LA. While the challenge of carrying out questionnaire-based survey in developing countries is well documented [22], our survey encompassed more than 1% of representativeness in all the LA countries monitored, reaching 30% in some cases, suggesting an accepted measure for proper estimation of bee colony losses.
We tested whether operation size could affect colony loss in LA as observed in the United States [14, 27, 28, 52, 53] and Europe [16, 54], and we found that operation size increased summer loss in both honey bees and stingless bees. Since in the United States, summer colony loss by large beekeepers has been attributed to migration of the operation for honey production or commercial crop pollination [14, 27, 28], we could consider those practices as potential drivers of honey bee colony losses in LA. However, these hypotheses about migration or pollination service effects need to be formally tested. Furthermore, we found the same significant trend with stingless bees. Migration of stingless bee colonies is not a common practice and if performed, it only involves a few stingless bee species. Nevertheless, other management practices could impact the colony health and survival of stingless bees in a different way than for honey bees. During summer, the impact of the temperature and humidity may disturb the homeostasis of the colony since different models of rational hive models used in meliponiculture are commonly adapted to the vast diversity of species [55]. However, our understanding on the advantages of each type of hive in regards to biological parameters is scarce [56]. Furthermore, the summer period also increases the activity of predators or robbers, sometimes coupled with the exposure to fumigation to control insects vectoring diseases in the hives. Another hypothesis is the competition for food during the summer period with A. mellifera or even between stingless bee colonies in an environment with a high density of colonies [57, 58].
On the other hand, we found that winter colony loss decreased with operation size in stingless bees, but not in honey bees although a negative pattern (not significant) was observed. These results also agree with the findings in the United States [14, 27, 28, 52, 53] and Europe [16, 54]. One hypothesis to explain the non-significant pattern with honey bees could be that the large heterogeneity of participants’ profiles would mitigate the operation size effect. For instance, large operation-size beekeepers (i.e. professional) in Peru own fewer colonies (µ = 119 colonies) than intermediate operation-size beekeepers (i.e. semi-professional) in Uruguay (µ = 220 colonies), illustrating the large variety of beekeeper profiles and situations across the different LA countries. The operation size does not integrate all practices and contexts of beekeeping and future studies should consider multiple parameters of beekeeping management practices [59, 60].
Winter is a major challenge for bee colonies in temperate regions, as colonies must survive months with low temperatures, confinement in the hive and lack of pollen and nectar intake. Furthermore, in some temperate regions, the temperature still allows the foraging flights and the lying activity of the queen and therefore the possibility of parasite reproduction in preimaginal stages, such as Varroa mites. It is expected that weak colonies, with a low bee population and/or a lack of adequate reserves, will not survive these conditions [61]. Thus, winter colony losses are expected to be higher than summer losses. However, in several LA countries (e.g. Argentina, Bolivia, Colombia), similar or even higher loss rates were found in the summer compared to the winter in honey bees. Similar results were observed in the United States, with summer losses reaching or even exceeding winter losses [13, 14, 20, 27, 30, 50, 51]. Moreover, in South Africa where only summer losses were estimated, honey bee colony loss reached up to 46% [35]. We also observed higher loss rates in summer compared to winter in stingless bees for several LA countries (Argentina, Bolivia, Brazil and Colombia). This high level of summer losses could be associated with the operation size effect as discussed before, but also with other abiotic factors that are known to impact bee health and survival, such as pesticide exposures [40, 51, 62], flower resource availability [23–26] and climate [29–32]. Biotic factors can also be linked with summer colony loss [63–65], and overall, the combination of all these factors is a hypothesis that should be investigated in future research [66, 67]. One point that needs to be clarified is that we estimated colony loss in three fixed periods: from October 1st to March 31st, from April 1st to September 30th, and from October 1st of one year, to September 30th of the next year. Following previous published studies [14, 15, 22, 38, 39, 68, 69], we allocated these periods to summer, winter and annual losses, respectively, with distinctions between the North and South hemisphere locations of the countries. This method facilitated the comparison of colony loss between LA and other regions of the world (e.g. the United States and Europe). However, it is important to notice that LA includes a large variety of climates and the generalization of the terms “summer” and “winter” could not fit rigorously with the entire region. Part of the LA region could be distinguished between dry or rainy seasons instead of winter or summer periods, although this specificity would limit comparisons across regions.
Overall, this study shows the results of the first large-scale monitoring initiative in LA and reveals an alarming situation for honey bees and native stingless bees in the region. Comparing honey bee colony losses between large-scale monitoring initiatives from the perspective of cross-continental analysis, we found that winter losses in LA places between the United States and Europe trends. This result confirms that honey bee colony losses are a global concern, and Latin America is not exempted. Although direct comparisons between datasets should be made with caution, since different sample sizes and methods were used for data collection, the results highlight the alarming situation of the LA. Similarly to beekeepers, meliponiculturists are suffering a high rate of colony loss in LA, and facing some other challenges in the sustained development of meliponiculture, as an increasingly expanding practice in Latin America. These challenges include the acquisition of colonies through non-extractive methods (which are becoming less common but still persist) and the regulation of trade and movement of colonies to non-native locations, which has been observed to potentially contribute to the loss of colonies of native bees [70]. Moreover, the management and control of the major Phoridae fly pests impacts the survival of managed stingless bees in central America [71]. Besides the importance of those native bees in the maintenance of biodiversity in natural ecosystems, and the improvement of agricultural production, meliponiculture is a tool for sustainable development, representing additional incomes, food and medicine for rural communities. It is necessary to promote the sustainable growth of this activity, considering local and traditional knowledge, and it is also important to better understand the biology and diversity of the species involved by means of accurate scientific approaches. This study also highlights the need (i) to coordinate among individual survey initiatives [39, 72], (ii) to standardize methods [21, 50], and (iii) to consider seasonal (e.g. summer/winter, dry/rainy seasons) and annual losses, in order to improve the effectiveness of monitoring initiatives and enhance bee health. Finally, this study can help understanding beekeeping challenges that occur in LA in order to foster research on how abiotic risk factors potentially involved in colony losses, such as flower resource availability [23–26], beekeeping management [14, 16, 27, 28, 52–54], pesticide exposures [51, 62, 73], and climate [29–32], could affect honey bee and stingless bees in LA.