For decades, beekeepers around the world have struggled to control Varroa destructor, an ectoparasitic mite, in their honey bee (Apis mellifera L.) colonies (Rosenkranz et al., 2010). The pest now has a worldwide distribution and can be found nearly everywhere honey bee colonies are managed (Boncristiani et al., 2021). Varroa’s impact is primarily linked to its ability to vector and transmit a large number of viruses (Genersch and Aubert, 2010; Traynor et al., 2020), severely weakening honey bee colony strength (Budge et al., 2015), and resulting in widespread colony losses (Brutscher et al., 2016; Gray et al., 2020).

Different non-chemical and chemical treatments are used by beekeepers to reduce V. destructor populations below the economic threshold, which is typically considered as 3 mites/100 adult bees (Jack and Ellis, 2021). The more time a colony spends above the economic threshold, the more likely it is to experience both increased viral infection and colony mortality (Kulhanek et al., 2021). Each year, beekeepers must decide which V. destructor treatment regimens are best to use in their management setting, this being based on several factors (Thoms et al., 2019; Underwood et al., 2019; Steinhauer et al., 2020). The most obvious factor is the efficacy of the treatment, which can vary under specific circumstances (Jack and Ellis, 2021). Weather conditions, particularly temperature and precipitation, have been observed to play a significant role in the efficacy of several V. destructor treatments (Beyer et al., 2018; Steube et al., 2021). Natural chemical treatments are particularly responsive to ambient temperature conditions, as volatile chemicals release gases based on the temperature where they are placed (Imdorf et al., 1995; Gracia et al., 2017). Even honey bee behaviors, such as grooming behaviors to remove V. destructor, can be affected by weather (Currie and Tahmasbi, 2008).

Beekeepers have historically relied heavily on synthetic chemical treatments to control V. destructor (Roth et al., 2020), but the efficacy of these treatments has become limited due to resistance issues (Haber et al., 2019). Some have observed treatment efficacy to vary according to location and season in which it is applied (Currie and Gatien, 2006; Gracia et al., 2017). As V. destructor can only reproduce within the capped brood cells containing honey bee pupae, the mites spend a significant amount of their lives inside these cells (Rosenkranz et al., 2010). Thus, the timing of chemical treatments is also essential for sustaining V. destructor control (Delaplane and Hood, 1997; Gatien and Currie, 2003), as the effectiveness of some treatments is considerably reduced if mites are hidden within the capped brood cells at time of application (Kraus and Berg, 1994; Rosenkranz et al., 2010; Al Toufailia and Ratnieks, 2018).

Another factor beekeepers must consider when attempting to control V. destructor is the amount of time required to apply the treatment. Some non-chemical treatments can be effective (Ellis et al., 2001; Wantuch and Tarpy, 2009; Kablau et al., 2020), but often require too much time. This makes such treatments unpopular among commercial beekeepers (Underwood et al., 2019). The length of time the treatment must remain in the hive is also an important factor to consider, as most chemical treatments are not labeled for use while honey supers are present on the hive (Honey Bee Health Coalition, 2018). To be successful with sustainable V. destructor control, beekeepers must consider all these variables in relation to beekeeping activities such as honey production, queen rearing, package bee production, and commercial pollination. It would be extremely valuable to beekeepers to have a decision tool to aid them in their selection of V. destructor treatments according to their own location and beekeeping situation.

Before a V. destructor control decision tool could be created, researchers need to understand the relationship between V. destructor population growth and the individual mite treatments. Many researchers have explored the complex dynamics of V. destructor population growth (reviewed by Fries et al., 1994; DeGrandi-Hoffman and Curry, 2004; Coffey et al., 2010; Ratti et al., 2012; DeGrandi-Hoffman et al., 2016). Some have created elaborate growth models which include several factors such as honey bee brood rearing, acaricidal efficacy, mite reproductive rates, and the total number of foragers with mites to name a few (reviewed by Fries et al., 1994; Wilkinson and Smith, 2002; DeGrandi-Hoffman and Curry, 2004; DeGrandi-Hoffman et al., 2016). Nevertheless, after thorough research, an extensive study evaluating the effect of season has not been conducted to our knowledge. By knowing the seasonal growth rate of V. destructor populations, one may be able to predict how long after treatment it takes mite populations to return to pretreatment levels.

It is necessary to create a model of natural V. destructor population growth by season as a first step toward the creation of a decision tool. Herein, we observed natural V. destructor population growth rates in north central Florida throughout multiple years and compared the growth rates by season. We hypothesized that V. destructor population growth would vary by season, with the fastest rate of growth happening in the summer and fall seasons, as that is when the greatest amount of capped brood is present in colonies. We made this hypothesis based on the knowledge that the population dynamics of V. destructor and honey bees are interwoven, as the mites can only reproduce within capped brood cells (Rosenkranz et al., 2010).

We evaluated an extensive and robust dataset composed of 160 honey bee colonies to understand V. destructor population growth seasonally. Our main goal was to generate information that can guide beekeepers as a part of a holistic approach to control this devastating honey bee parasite. Our results not only confirm the importance of seasonal effects on the efficacy of treatments for the mite, but they can also be used as a natural model of V. destructor population growth for north central Florida, and possibly colonies kept in similar climates. Additionally, we believe that the results of this study demonstrate the importance of regular V. destructor monitoring and treatment by beekeepers, as colony survival is often less than 1 year for untreated colonies in Florida. We anticipate that the benefits and information described in our study can be applied to optimize treatment and control for V. destructor in Florida and can help guide studies and research for the control of this parasite worldwide.

Although much has been written related to V. destructor population growth, to our knowledge, this is the first attempt to determine V. destructor population growth seasonally after treatment. As V. destructor population growth is closely tied to honey bee brood rearing (Wilkinson and Smith, 2002), it is not surprising that mite levels were able to rebound rapidly after treatment in the summer and fall seasons when honey bee brood is plentiful in Florida (Figure 2). However, somewhat surprising is the significantly slower V. destructor population growth after treatment in the spring when compared to that in winter (Figure 2). One might predict that in colonies where mites were reduced to near-zero in the winter, V. destructor populations would be delayed in growth due to the lack of honey bee brood required for reproduction. Interestingly, mite levels were still significantly lower in the spring than in all other seasons 3 months after treatment, making this the longest period during which mite populations were maintained below the economic threshold (Figure 2). Dolezal et al. (2016) demonstrated how the environment in which colonies are placed can influence the nutritional physiology of the colony, thus directly affecting V. destructor presence in a given environment. As honey bee colonies in the spring season have access to more floral resources, this nutritional advantage may have allowed the bees to defend or guard against V. destructor reproduction or reinfestation better than presumably nutrition-deficient colonies treated in winter.

Information regarding seasonal V. destructor population growth is applicable to beekeepers who struggle to maintain mite populations below economic thresholds (Jack and Ellis, 2021; Brodschneider et al., 2022). It appears that reducing V. destructor populations in the spring season is important for long lasting mite control. An effective reduction of mite populations in the spring could provide beekeepers sufficient coverage through the spring and summer months, effectively reducing the likelihood of necessary treatments during the major nectar flows for most temperate regions. Winter is also an effective season to treat for V. destructor, providing beekeepers with coverage through the spring season. However, even after an effective winter treatment, mite populations could still return to economic thresholds by the spring season. In this case, the beekeeper has a difficult decision; either they interrupt their colonies’ honey production during a major nectar flow or they delay treatment until after honey supers have been removed. If beekeepers are not able to reduce the V. destructor population below the economic threshold of 3 mites/100 bees, their colonies are likely to succumb to viral infection (Kulhanek et al., 2021).

While reducing V. destructor populations in summer and fall seasons may be important, the benefits of doing so could be very short-lived. A reduction of mite populations in summer only resulted in about 2 months of coverage for the beekeeper, meaning that another treatment in fall would be necessary. Unfortunately, reducing mite levels in fall again only provides 2 months of coverage, requiring another treatment in winter. Thus, it appears that multiple treatments are likely necessary if mite populations reach economic thresholds in the summer and fall seasons. Frequent treatments such as these can, increase the likelihood that the mites develop resistance to chemical treatments and the cost of controlling V. destructor to beekeepers. However, the need to reduce V. destructor populations in the summer and fall months is crucial, as viral titers tend to be at their highest and colonies are most severely impacted during these seasons (Highfield et al., 2009; Dainat et al., 2012; Traynor et al., 2016).

Varroa destructor treatments can vary widely in cost, with some treatments, for instance oxalic acid, costing less than others, such as the synthetic compound Apivar™. Thus, optimizing treatment efficacy and reducing the frequency of treatments could provide the beekeeper with considerable savings. Based on the V. destructor population growth data presented in Figure 2, we created Table 1 to provide a better understanding of when a beekeeper could expect to apply miticides for the control of the pest. Depending upon when the treatment regime is started, a beekeeper may need to apply one additional treatment over the period of 2 years. Perhaps for a hobbyist beekeeper, that would not equate to significant savings, but it might for a large commercial operation. However, we created Table 1 to be used as a reference for when colonies may need treatment, as treatment efficacy can be region-specific and not all treatments can be applied at all times of the year (Jack and Ellis, 2021). Thus, beekeepers should not stay on a strict treatment regimen but should closely monitor V. destructor populations to determine treatment timing.

The difference in colony lifespan post-treatment between the two trials was stark (Figure 3). For instance, survival was greatest in trial one after treatment in the winter. In trial 2, the winter treatment survival was similar to that of the summer group, with both being low. It is possible that these two winter treatments were affected differently by their location, as colonies receiving the winter treatment in trial one were located in the northern Gainesville apiary and while in trial 2, they were located at the Hawthorne apiary. Both apiary sites are ∼24 km apart, yet the floral resources available at the Hawthorne apiary are more plentiful than those at the northern Gainesville apiary during the late spring and summer months. Nutritionally, colonies in the Hawthorne apiary may have been better able to handle V. destructor after a winter treatment than were those at the Gainesville apiary. It is also possible that viral titers differed between colonies at the two sites, leading to the different responses of mite populations to winter treatments at both apiaries. While we believe that the bees used in this study were of the same genetic origins for both trial 1 and trial 2, slight genetic differences may have existed between the two populations. It is possible that these genetic differences of the bees used in both trials could have led to varying rates of death after exposure to elevated V. destructor levels. Weather differences, or other environmental parameters could have played a role. Unfortunately, we cannot determine the impact of location, genetics, virus load or weather on colony survival as we were only able to conduct two trials for this experiment and did not collect all the data necessary to make these determinations.

There are other variables that would likely impact V. destructor populations and warrant additional exploration. These variables could include temperature, frost-free days, rainy/dry seasons, nectar flows, and growing seasons. As mite population growth is closely tied to honey bee brood rearing (Wilkinson and Smith, 2002), the same climatic conditions that increase brood rearing likely also increase V. destructor populations. Ultimately, we can only use our results to predict the V. destructor population outcomes in north central Florida. However, beekeepers managing hives in areas with similar rates of brood rearing could use our work to assist with predictions of their own colonies’ V. destructor population growth. Therefore, regional or countrywide honey bee brood surveillance would be helpful for predicting mite population growth with greater resolution. Such a surveillance program for the southeastern USA is currently underway (G. Williams, personal communication, University of Auburn).

Beekeepers are in desperate need of effective controls to use against V. destructor. As the development of new controls can take many years, it is essential that beekeepers utilize existing treatments more efficiently. We believe that the research presented herein helps us better understand the seasonal efficacy of V. destructor treatments and could potentially aid in the development of a mite control decision tool for beekeepers. More effective timing of treatments could reduce the frequency of treatments, thereby reducing the likelihood of V. destructor development of resistance to a given miticide. Additional research related to V. destructor population predictions and modeling is essential for long-term, sustainable management of this devastating honey bee parasite.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

CJ and JE: study conception and design, and interpretation of results. CJ: data collection. CK and IB: data analysis and interpretation of results. CJ, CK, IB, and JE: draft manuscript preparation. All authors reviewed the results, contributed to the article, and approved the submitted version.