Philippa Kaur

Plants increase their freezing resistance upon exposure to low temperatureThe freezing resistance (LT50 values) was found to vary ranging from − 6.9 °C (14-August-2017) to − 31.7 °C (04-November-2018) over the course of study period. The freezing resistance of leaves recorded during the 12 sampling time-points has been provided in Table 1 (also see39). The overlap of confidence intervals around the mean was examined for comparison of LT50 values for the different sampling time-points. Significant differences in freezing resistance were observed across the sampling time-points (Table 1). Leaves of R. anthopogon collected during summer [July and August (Air temperature and photoperiod was about 9.6 °C and 13 h day−1 respectively)] showed marginal resistance to freezing (LT50: − 7 °C) and thus, are more susceptible to freezing damage. Further, as the ambient air temperature and photoperiod decreased towards the end of growing season (i.e., October and November 2017 with air temperature and photoperiod of about − 1.1 °C and 10.5 h day−1 respectively), the plants acquired the highest freezing resistance (LT50: − 30 °C). Interestingly, a sharp increase in freezing resistance (− 29.4 °C) was observed in September 2018, when the daily mean air temperature decreased below 0 °C due to sudden snowfall (Supplementary Fig. S2). Comparison of LT50 values of all the leaf samples of R. anthopogon showed that cold de-acclimation occurred after the snowmelt during early spring in June (LT50: − 13.4 °C) with an increase in air temperature and photoperiod. These results demonstrated that R. anthopogon plants exhibit lowered freezing resistance during the warmer months [hence, these time-periods were referred as non-acclimation (NA)], progressively develop greater freezing resistance during the onset of winter season (hence, referred as cold acclimation) followed by an intermediate level of freezing resistance during the spring [hence, these time-periods were referred as de-acclimation (DA)].Table 1 The estimates of LT50, calculated by fitting sigmoidal curve to electrolyte leakage values of temperature treatments, recorded for leaves collected during the different sampling time-points (from August 22, 2017 to September 18, 2018).Full size tableDuring the acclimation period (i.e., late in the growing season), plants acquired the highest resistance to freezing (Fig. 1). The low electrolyte leakage (= high freezing resistance) observed during this period might be due to changes in cell wall properties (such as increase in lignification and suberization of cell walls), which provide resistance to diffusion of electrolytes from cells of the leaves to the extracellular water47. Moreover, high freezing resistance may also be attributed to high leaf toughness and sclerophyllous habit of this evergreen species48. Further, it was found that freezing resistance was the lowest during mid-summer period. This pattern could be explained by a trade-of between plant growth rates and freezing resistance, where warmer temperatures favour plant allocation to growth49. These observations corroborated well with earlier reports that showed a rapid increase in ‘freezing resistance’ during the transition from summer to early winter and vice versa50.Figure 1LT50 [black point (with solid fill) on the curve] calculated by fitting sigmoidal curve to relative electrolyte leakage (REL %) values recorded during the three different acclimation phases. GOF indicates ‘goodness of fit’ test values for the fitted sigmoidal curves.Full size imagePhotosynthetic rates are higher during non-acclimation and de-acclimation periodIt was found that PN of R. anthopogon varied in the range from 8.336 to 17.64 μmol(CO2)m−2 s−1 and E from 2.281 to 4.912 mol(H2O)m−2 s−1, throughout its growing season. The Gs of leaves was estimated to be in the range from 0.110 to 0.265 mol (H2O) m−2 s−1. WUE, a ratio of PN and E, varied between 52.21 and 87.68 (Table 2). The gas exchange parameters of R. anthopogon varied significantly among the sampling time-points [referred to here as different acclimation phases of the growing period of evergreen shrub (Fig. 2, Table 3)]. In particular, PN was significantly lower on 18-September-2018 (referred as cold acclimation phase), whereas it was higher on 31-August-2018 and 15-June-2018 (referred as NA and DA phases, respectively). Similarly, Gs of leaves was significantly lower during cold acclimation in comparison to the rest of the acclimation phases (i.e., NA and DA). Further, WUE was significantly higher during cold acclimation, while it was lower during both NA and DA (p ≤ 0.05) (Fig. 2).Table 2 Variability in leaf gas exchange parameters of R. anthopogon during the different acclimation phases (NA = Non-acclimation, LA = Late cold acclimation and DA = De-acclimation).Full size tableFigure 2Variability in leaf gas exchange parameters of R. anthopogon during the three acclimation phases [i.e., Non-acclimation (31 August, 2018), Cold acclimation (18 September, 2018) and De-acclimation (15 June, 2018)]. Different alphabets (a, b, c) represent statistically significant values (p  More

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We confirm that Cuba is home to the world’s largest European honeybee population that has naturally become Varroa-resistant, with an estimated 220,000 colonies being maintained without any form of chemical treatment for over two decades19 although some drone-trapping occurred during the early years of the transition period This is despite the presence of the K-haplotype of the mite20 and the widespread occurrence of DWV19 throughout Cuba. Hence, the Cuban honeybee population is the first major case of Varroa-resistant European bees occupying an entire country of a large size (109,884 km2). In Europe the proportion of varroa-resistant honeybee populations in each country is highly variable21,22, but they still consist of small, isolated populations within any country. For example, the second largest known area of European Varroa-resistant honeybees is in North Wales, UK where 104 beekeepers have managed around 500 honey bee colonies over an area of 2500 km2 without treatment for over a decade23.It has long been established that sub-Sharan African and Africanised honeybees are Varroa-resistant and both populations cover much larger areas than Cuba, but these honeybee races are not capable of thriving in temperate regions or are rejected by beekeepers in Northern hemispheres. However, previous studies on African/Africanised and European honeybees4,5,6,9 all appear to have evolved with the same resistance mechanism7 and Cuban honeybees follow this pattern showing high recapping behaviour, high mite removal behaviour and low mite reproduction (Figs. 1, 4, Table 1).The strongest evidence that increased recapping behaviour is a direct response to the presence of Varroa, is the very low recapping rates in Varroa-naïve colonies. This is evidenced by the recapping baseline data that has now been collected from four different Varroa-naïve (Varroa free) honeybee populations (Australia, UK [two populations] and Hawaii [this study]) all producing similar results (Fig. 1). Across the four populations, a total of 9542 worker cells from 15 colonies have been studied with an average recapping rate of 2.0% (+ SD 3.2). Interestingly, only two of the colonies had atypical recapping rates of 8.5% and 10.7%, from Australia and Kauai respectively. This may suggest increased sensitivity in these colonies as no obvious causes e.g., wax moth or dead pupa, were detected in either colony. The data summary in Fig. 1 indicates that even in Varroa-treated populations the workers are still able to detect mite infested cells, but the average consistently falls significantly below that found in resistant populations. That is, in non-infested worker cells recapping rates are significantly higher in resistant populations in comparison to susceptible populations (Fig. 1) t4, 5 = − 4.185, p = 0.0023 as well as for infested cells t4, 5 = − 6.905, p = 0.00007.The ability of Cuban honeybees to detect infested cells causes not only high recapping levels but also high removal rates of artificially mite-infested cells. A mean removal rate of 81% is among one of the highest recorded in Apis mellifera7. The average control rate of 45% is 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 natural Varroa infestation was 23%, whereas in December 2021 it was only 13%. This is due to decreasing worker brood rearing, caused by a shortage of nectar during the annual dry season. During this time there is an increase in hygienic behaviour in the colonies24, which could help explain the higher-than-expected removal of control cells.The reproductive ability of Varroa to produce viable i.e., mated, female offspring (r) in infested worker cells in resistant colonies in South Africa4 (r = 0.9), Brazil4 (r = 0.8), Mexico18 (r = 0.73), Europe3 (r = 0.84) is similar to the 0.87 found in Cuba (this study). In Cuba ‘r’ reduces to 0.77 when both single and multiple infested cells are considered. This reduction in mite reproduction, relative to susceptible colonies that have values of r greater than one, is directly linked to the increased ability of resistant workers to both detect and remove, by cannibalisation, the infested pupa. Hence, this ensures the invading mite fails to reproduce7 or reduces mite fertility due to the recapping process4. Although, in this study no significant difference was found in the reproduction of Varroa in recapped or non-recapped cells, supporting the findings of two previous studies5,9. Therefore, recapping may be playing a minor role in resistance. However, recapping remains the best indicator or ‘proxy’ of resistance within the vast majority of honeybee populations since it’s easier, quicker, and it requires less skill to measure recapping rates than mite removal rates. However, recapping is a highly variable trait7, hence both many cells (200–300) per colony and many colonies ( > 10) per population ideally need to be studied to help reduce the variablity, also in temperate countries measuring recapping when mite-infestation rates peak in autumn maximises detecting infested cells since the recapping of cells is spatially associated with infested cells11.Despite the current focus on what is happening in worker cells, studies focusing on the role of recapping in drone brood are still in their infancy with. Currently, data is only available from South Africa9 (Fig. 1) and now Cuba (this study). Interestingly, both studies indicate no significant difference in recapping rates between infested and non-infested brood. This is caused by some colonies performing no recapping of drone brood, while some colonies do recap cells but in a non-targeted manner. Whereas there is a significant increase in the size of the recapped area between infested (3.1 mm) and non-infested (2.3 mm) worker cells (Fig. 3), this does not occur in drone brood, as it appears that the holes are entirely exploratory. However, the lack of removal of infested drone brood may be playing an important role in mite-resistance (see below).The mite infestation of worker cells currently varies between 23 and 13% in Cuba (this study), roughly 25 years after it was first detected (1996). Whereas, in Mexico and Brazil, infestation rates of worker brood have fallen from around 20% in 1996/1999 down to 4% in 2018/197. Although, Varroa was first detected in Brazil much earlier, in 197225 and the Africanised honeybees adapted to the mite and spread northward replacing the susceptible European colonies. Therefore, we predict that the worker infestation rate in Cuba will continue to fall over the next 20 years, especially if high mite-removal rates persist. Correspondingly, we would expect to see the infestation rates of the drone brood (currently at 40%) to remain high as mites potentially avoid reproduction in worker cells. This potentially is a key, but currently overlooked part, of the resistance mechanism. Since an empirical model26 indicated that negative mite population growth occurs in (resistant) Africanised honeybee colonies only when the initial drone cells are present. This is thought to arise because mites also show a tenfold preference to reproduce in drone cells (which comprises only 1–5% of all the honeybee brood) and they soon become overcrowded as the mite population increases. This leads to inter-mite competition for the limited food and space, causing an increase in mite mortality27, resulting in negative reproductive success for mites entering these overcrowded drone cells. Thus, mite population growth in drone brood cells is limited by a density-dependent mechanism. In Cuba it has been observed that strong colonies typically with drone brood do not weaken during the drought season, whereas colonies without drone brood are weak and often die during the drought (APP personal comm).Although Cuban beekeepers have been aware of their mite-resistant honeybees for 15 to 20 years’, Cuba’s situation has only recently come to light16,18. The main reason for Varroa-resistance in Cuba is due to the centralised decision to allow natural resistance to evolve, as also was done successfully in South Africa3, rather than becoming locked into using miticides, as has happened throughout the Northern hemisphere. The CIAPI and Veterinarian Services central decision to ‘not treat’ was greatly assisted by all Cuban beekeepers being professional, registered and embedded within a strong locally based beekeeping community where colony movement and exchange of queens is within each province.There is also a large feral population and due to Cuba’s sub-tropical climate, queens are replaced annually in managed colonies because of almost continuous egg-laying, similar to honeybees in Hawaii. This rapid queen turnover speeds up natural selection relative to honeybee populations in more temperate climates. Finally, Cuba’s 60-year ban on honeybee importation has helped isolate the country from been invaded by Africanised bees which has occurred in many nearby regions (eg. Mexico, Southern USA, Puerto Rico, neighbouring Dominican Republic13 and Haiti (D. Macdonald, Apiary Inspector, Min. of Agi BC, Canada, pers. Comm.). Cuba has many managed European colonies coupled with many queen rearing stations. These colonies are productive and mild mannered. 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 interference. More

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