Summarizing mite removal behavior in Cuba: home to the largest population of Varroa-tolerant European honey bees in the world

We confirm that Cuba is home to the largest population of European honey bees in the world that has become naturally resistant to Varroa, with an estimated 220,000 colonies maintained without any form of chemical treatment for over two decades.19 Although some drone trapping occurred during the early years of the transition period, this despite the presence of haplotype K of dreaming20 The spread of DWV is widespread19 all over Cuba. Thus, the Cuban honey bee population is the first major case of Varroa-resistant European bees occupying an entire country with a significant size (109,884 km.2). In Europe the proportion of Varroa-resistant honey bees in each country varies greatly21, 22, but still consists of small isolated populations within a country. For example, the second largest known area of ​​Varroa-resistant European honey bees is located in North Wales, UK where 104 beekeepers have managed to manage around 500 honey bee colonies over an area of ​​2500 square kilometres.2 Without treatment for more than a decade23.

Sub-Saharan African honey bees have long been shown to be resistant to Varroa and both groups cover much larger areas than Cuba, but these honeybee subspecies are unable to thrive in temperate regions or are rejected by beekeepers in the Northern Hemisphere. However, previous studies on Africanized/African and European honey bees4And the56,9 They all seem to have evolved with the same resistance mechanism7 Cuban honey bees follow this pattern showing high elimination behaviour, high mite removal behaviour, and low mite reproduction (Figs 1, 4, Table 1).

The strongest evidence that the increased summing behavior is a direct response to the presence of Varroa, is the very low re-pollination rates in naive Varroa colonies. This is illustrated by resuming the baseline data now collected from four different groups of naïve (varroa-free) Varroa bees (Australia, UK). [two populations] and Hawaii [this study]) all lead to similar results (Fig. 1). Across the four populations, a total of 9542 working cells from 15 colonies were studied with an average reconnection rate of 2.0% (+SD 3.2). Interestingly, only two of the colonies had atypical recombination rates of 8.5% and 10.7%, from Australia and Kwai, respectively. This may indicate increased sensitivity in these colonies as obvious causes such as wax moth or dead pupa, were not detected in any of the colonies. The data summary in Figure 1 indicates that even in the Varroa-treated populations, workers were still able to detect mite-infected cells, but the average was consistently significantly lower than that in the resistant groups. That is, re-inoculation rates in uninfected working cells are much higher in the resistant groups than in the susceptible groups (Fig. 1). R4, 5= – 4.185, s= 0.0023 as well as for infected cells R4, 5= – 6.905, s= 0.00007.

The ability of Cuban honey bees to detect infected hives leads not only to high re-aggregation levels but also high removal rates of artificial mite-infected hives. The average removal rate of 81% is among the highest recorded in Apis mellifera7. The average control rate of 45% was driven by three colonies that all removed more than 75% of the controls, while the average of the remaining seven colonies was 28%. During the mite removal studies in March 2022 the natural incidence of Varroa was 23%, while in December 2021 it was only 13%. This is due to a decrease in the brood of workers due to the lack of nectar during the annual dry season. During this time, there is an increase in healthy behavior in the colonies24which could help explain the higher-than-expected removal of control cells.

The reproductive capacity of Varroa to produce viable mated female offspring.s ) in infected working cells of resistant colonies in South Africa4 (s= 0.9), Brazil4 (s= 0.8), Mexico18 (s= 0.73), Europe3 (s= 0.84) Similar to 0.87 found in Cuba (this study). in Cubas‘It drops to 0.77 when both single and multiple infected cells are considered. This decrease in mite reproduction, relative to sensitive colonies that have values sgreater than one, is directly related to the increased ability of resistant workers to detect and remove an infected pupa, via cannibalism. Thus, this ensures that the invading mites fail to reproduce7 Or reduce mite fertility due to re-pollination4. Although there was no significant difference in this study in Varroa proliferation in recycled or non-recycled cells, supporting the results of two previous studies5,9. Therefore, summarization may play a secondary role in resistance. However, recapitulation remains the best indicator or ‘proxy’ of resistance within the vast majority of honeybees because it is easier, faster and requires less skill to measure recapitulation rates compared to mite removal rates. However, summarizing is a very variable feature7thus many cells (200-300) per colony and many (>10) colonies per group ideally need to be studied to help reduce variance, and also in temperate countries, remapping measures when autumn tick infestations reach their limit Maximum detection of infected cells because cell regrouping is spatially correlated with infected cells11.

Despite the current focus on what happens in working cells, studies focusing on the role of summation in male broods are still in their infancy. Currently, data is only available from South Africa9 (Fig. 1) and now Cuba (this study). Interestingly, both studies indicate no significant difference in revaccination rates between infected and uninfected brood. This occurs because some colonies do not recapitulate male brood, while some colonies recapitulate cells but in a non-targeted manner. While there is a significant increase in the size of the recycled area between infected working cells (3.1 mm) and uninfected cells (2.3 mm) (Fig. 3), this does not occur in male brood, where holes appear to be fully exploratory. However, failure to remove infected male brood may play an important role in mite resistance (see below).

The infestation of working cells by mites is currently between 23 and 13% in Cuba (this study), approximately 25 years after it was first discovered (1996). While in Mexico and Brazil, worker brood infection rates decreased from about 20% in 1996/1999 to 4% in 2018/197. Although Varroa was first discovered in Brazil much earlier, in 197225 The African honey bee adapted to the mites and spread north to replace susceptible European colonies. Therefore, we expect that the worker infestation rate in Cuba will continue to decline over the next 20 years, especially if high mite removal rates continue. In contrast, we would expect to see infection rates in male broods (currently at 40%) to remain high as mites likely avoid reproducing in working cells. This is likely a key, but currently overlooked, part of the resistance mechanism. Since the demo model26 indicated that negative growth of mites occurs in (resistant) African honey bee colonies only when primary drone cells are present. This is thought to have arisen because moths also show a tenfold preference for breeding in drone hives (which make up only 1-5% of all honeybee broods) and quickly become overcrowded as the mite population increases. This leads to competition between mites for food and limited space, resulting in an increased mite mortality rate27, which resulted in negative reproductive success of mite entry into the overcrowded UAV cells. Thus, the growth of mite numbers in male brood cells is constrained by a density-dependent mechanism. In Cuba it has been observed that usually vigorous castes with male brood do not weaken during the dry season, while castes without drone brood are weak and often die during drought (APP personal contact).

Although Cuban beekeepers have been familiar with moth-resistant honeybees 15-20 years ago, Cuba’s status only emerged recently.16, 18. The main reason for Varroa resistance in Cuba is due to the central decision to allow the development of natural resistance, as was also done successfully in South Africa.3, rather than shutting down to the use of acaricides, as has happened across the Northern Hemisphere. The central decision of CiAPI and the Veterinary Services to “not treat” was largely supported by all professional and registered Cuban beekeepers who are integrated into a strong local beekeeping community where the movement of colonies and the exchange of queens is within each province.

There is also a large feral population and due to Cuba’s subtropical climate, queens are replaced annually in managed colonies due to nearly continuous egg laying, similar to Hawaiian honeybees. This rapid turnover of queens accelerates natural selection relative to honeybee populations in milder climates. Finally, Cuba’s 60-year ban on importing honey bees helped isolate the country from the infestation of African bees that occurred in many neighboring regions (such as Mexico, southern USA, Puerto Rico and the neighboring Dominican Republic.13 and Haiti (D. Macdonald, Apiary Inspector, Min. of Agi BC, Canada, pers. Comm.). Cuba has many European managed colonies as well as several queen-rearing stations. These colonies are productive and have moderate manners. Thus, Cuba is an excellent example of the power of natural selection in honeybees when they are allowed to adapt naturally to Varroa with minimal human intervention.