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Grooming by honey bees as a component of varroa resistant behavior
Journal of Apicultural Research
Abstract
Grooming behavior of honey bees can be considered in two major categories: autogrooming or self-grooming and inter-bee grooming, called allogrooming. Allogrooming can be one-on-one, or social, involving several nestmates acting collaboratively. In addition, some house bees become allogrooming specialists, and for them grooming their nestmates can be a full-time occupation for most of their lives. Early observations on the Eastern honey bee, Apis cerana, recorded autogrooming, one-on-one, and social allogrooming, all of which result in dead, visibly mutilated varroa mites falling to the hive floor. Similar behavior has been sought in the Western honey bee. Apis mellifera, with variant observations for the different subspecies. Most descriptions relate to A. m. carnica, some to A. m. ligustica, but with one notable exception, almost none to A. m. mellifera. The most impressive findings are from “Africanized” bees, which provide some of the best cases of natural, long-lasting tolerance to varroa mites in A. mellifera, although even some of these are controversial. The speed of both autogrooming and allogrooming responses is generally reported to be much slower in A. mellifera than in A. cerana, and the frequency and degree of damage to mites are also lower. Serious damage, such as severance of limbs and gashes of the idiosoma, shows a heritability (h²) of around .16 in A. mellifera overall.
... This collective mechanism is known as "social immunity" [32,[35][36][37][38] and includes strategies such as the spatial segregation of high-risk individuals [39,40], contact reduction and the removal of infected bees [41][42][43], and the altruistic self-removal of infected worker bees [44]. Other significant aspects of social immunity include grooming and hygienic behavior [45][46][47][48][49]. ...
... Grooming behavior involves activities by which adult bees remove and injure mites from their own body (auto-grooming) or the bodies of other bees (allogrooming) [45]. This behavior significantly contributes to the colony's resistance against mites by increasing mite mortality and regulating their population growth [49][50][51]. Notably, Africanized bees provide some of the best examples of natural, long-term tolerance to Varroa mites in colonies [49,[52][53][54]. ...
... This behavior significantly contributes to the colony's resistance against mites by increasing mite mortality and regulating their population growth [49][50][51]. Notably, Africanized bees provide some of the best examples of natural, long-term tolerance to Varroa mites in colonies [49,[52][53][54]. ...
The honey bee is an important insect pollinator that provides critical pollination services for natural and agricultural systems worldwide. However, inadequate food weakens honey bee colonies, making them vulnerable to various biotic and abiotic factors. In this study, we examined the impact of supplementary feeding on bees’ genes for antioxidative enzymes and vitellogenin, oxidative stress parameters, and the hygienic and grooming behavior. The colonies were divided into two experimental groups (with ten hives each): a treatment group that received the plant-based supplement and a control group. The experiment was conducted in two seasons, spring and summer. After the treatment, in both seasons, all the monitored parameters in the treatment group differed from those in the control group. The expression levels of genes for antioxidative enzymes were significantly lower, but the vitellogenin gene transcript level was significantly higher. Values of oxidative stress parameters were significantly lower. The levels of hygienic and grooming behavior were significantly higher. Therefore, our field study indicates that the tested supplement exerted beneficial effects on bees, reflected in reduced oxidative stress and enhanced hygienic and grooming behavior.
... Allogrooming is a social behavior by which a bee removes foreign particles and parasites from another bee (30,31). Apis mellifera is able to remove and kill Varroa through allogrooming activity, albeit less effectively than Apis cerana (32). Generally, this sporadic behavior is exhibited by young bees, at an age between 6 and 11 days (33), when they mainly act as nurse bees (34). ...
... The second line of evidence is represented by the differences in the spatial pattern of allogrooming detected between infested and uninfested colonies. We found that allogrooming, which can reduce the spread and incidence of parasitism (32), occurred more frequently on central frames rather than on lateral ones, in the central areas of the comb, usually occupied by brood, and on uncapped brood in infested hives when compared to uninfested hives. In infested colonies, allogrooming would be expected to be concentrated in the core of the colony, i.e., in the region of the comb with brood, where nurses remain and where newly emerged bees carrying mites might emerge more frequently (17,19). ...
... On the contrary, infested bees were even more central than the noninfested ones, likely because of the higher levels of allogrooming, antennation, and trophallaxis received. This lack of social distancing, with an even higher connectivity of infested individuals, contradicts the organizational immunity predictions, whereas an increase in caregiving could be a reasonable explanation from a social immune perspective, as this behavior might help to reduce the parasite load (32). However, we should consider that caregiving behavior, which requires physical contact, can have opposing effects: It can reduce infection levels by killing some of the mites attacking the infested bees, but it could also facilitate its spread to the caregivers (45). ...
Social distancing in response to infectious diseases is a strategy exhibited by human and nonhuman animals to counteract the spread of pathogens and/or parasites. Honey bee (Apis mellifera) colonies are ideal models to study this behavior because of the compartmentalized structure of these societies, evolved under exposure to parasite pressure and the need to ensure efficient functioning. Here, by using a combination of spatial and behavioral approaches, we investigated whether the presence of the ectoparasite mite Varroa destructor induces changes in the social organization of A. mellifera colonies that could reduce the spread of the parasite. Our results demonstrated that honey bees react to the intrusion of V. destructor by modifying space use and social interactions to increase the social distancing between young (nurses) and old (foragers) cohorts of bees. These findings strongly suggest a behavioral strategy not previously reported in honey bees to limit the intracolony parasite transmission.
... Regarding honey bees colonies, it is considered the most effective approach to mitigate the damage caused by Varroa and minimize the use of acaricides Noël et al., 2020;Jack and Ellis, 2021). Among the resistance behaviors exhibited by honey bees against Varroa, grooming holds particular significance (reviewed by Pritchard, 2016). Autogrooming is the ability of parasitized bees to dislodge mites by themselves, while allogrooming refers to this behavior with assistance from other bees (Boecking and Spivak, 1999;Pritchard, 2016;Mondet et al., 2020). ...
... Among the resistance behaviors exhibited by honey bees against Varroa, grooming holds particular significance (reviewed by Pritchard, 2016). Autogrooming is the ability of parasitized bees to dislodge mites by themselves, while allogrooming refers to this behavior with assistance from other bees (Boecking and Spivak, 1999;Pritchard, 2016;Mondet et al., 2020). Since, in a standard Langstroth hive with wooden bottom boards, the 50% of the mites fallen are still alive and can reinfest new bees (Lobb and Martin, 1997), the effectiveness of grooming behavior in controlling Varroa could be further increased if hives are equipped with bottom boards that prevent detached mites from reinfesting the colony (Harbo and Harris, 2004;Araneda and Calzadilla, 2011). ...
Introduction
Varroa destructor stands as the primary global pest of honey bees, inflicting direct harm on bees while also acting as a vector for a multitude of viruses. Integrated pest management is widely recognized as the optimal strategy for minimizing acaricide application. Designed bottom boards that can limit the growth of the mite population by removing them from the hive and preventing their return and reinfestation of the colony show promising potential.
Methods
The aim of this study was to compare Varroa population growth by employing three different types of bottom boards. An apiary of 55 colonies was randomly divided into five groups according to the bottom board they had: 1) tubular bottom board, 2) screen bottom board, 3) sticky bottom board, 4) conventional bottom board with a permanent treatment with acaricide (positive control), and 5) conventional bottom board (negative control). Varroa infestation level in bees, colony strength (bee and brood population), and honey reserves were determined between April and December (between autumn and spring in the southern hemisphere).
Results
Colonies that had sticky bottom boards had approximately 50% less Varroa infestation than colonies with conventional bottom boards at the end of the study. Varroa infestation levels did not differ significantly between the tubular, screen, and conventional bottom boards. Colony strength was similar in all groups. No differences were observed in honey production between colonies from different groups.
Discussion
The use of sticky bottom boards was the most promising board to limit Varroa population growth and prevent colonies' reinfestation. This result encourages future studies to analyze the incorporation of this strategy in integrated pest management programs.
... These surrounding bees inspect the parasitized worker's body with their antennae, searching for the mite. Once located, they use their upper jaw to pick up and kill the mite [13][14][15]. ...
... Newly emerged bees were individually marked on the thorax using a marker pen with distinct colors (bees of the same age were assigned the same color) and introduced into their original colony for natural rearing. At intervals of 5,7,9,11,13, and 15 days post-emergence, marked bees were selected from the colony and transferred into a honeybee feeding box containing 50% sugar water, allowing the bees to feed freely. Approximately one hundred color-marked bees per age group were collected and transported to the laboratory for behavioral assays. ...
The grooming behavior of honeybees serves as a crucial auto-protective mechanism against Varroa mite infestations. Compared to Apis mellifera, Apis cerana demonstrates more effective grooming behavior in removing Varroa mites from the bodies of infested bees. However, the underlying mechanisms regulating grooming behavior remain elusive. In this study, we evaluated the efficacy of the auto-grooming behavior between A. cerana and A. mellifera and employed RNA-sequencing technology to identify differentially expressed genes (DEGs) in bee brains with varying degrees of grooming behavior intensity. We observed that A. cerana exhibited a higher frequency of mite removal between day 5 and day 15 compared to A. mellifera, with day-9 bees showing the highest frequency of mite removal in A. cerana. RNA-sequencing results revealed the differential expression of the HTR2A and SLC17A8 genes in A. cerana and the CCKAR and TpnC47D genes in A. mellifera. Subsequent homology analysis identified the HTR2A gene and SLC17A8 gene of A. cerana as homologous to the HTR2A gene and SLC17A7 gene of A. mellifera. These DEGs are annotated in the neuroactive ligand–receptor interaction pathway, the glutamatergic synaptic pathway, and the calcium signaling pathway. Moreover, CCKAR, TpnC47D, HTR2A, and SLC17A7 may be closely related to the auto-grooming behavior of A. mellifera, conferring resistance against Varroa infestation. Our results further explain the relationship between honeybee grooming behavior and brain function at the molecular level and provide a reference basis for further studies of the mechanism of honeybee grooming behavior.
... Various studies have demonstrated the effectiveness of grooming and hygienic behaviours in keeping the population of mites in bee colonies at low levels (Russo et al. 2020;Fries et al. 1996;Nganso et al. 2017;de Figueiró et al. 2016;Pritchard 2016;Torres and Torres 2020). However, it is not clear if these bees natural defence mechanisms against mites can be enough to control an outbreak of viruses, specifically DWV, in Varroa-infested colonies. ...
... A clear understanding of the effects of these behaviours on the mites and the viruses they transmit can be important in reducing the losses of honeybee colonies. The effects of these mechanisms on the population of Varroa mites have been studied by several authors (Russo et al. 2020;Fries et al. 1996;Nganso et al. 2017;de Figueiró et al. 2016;Pritchard 2016;Torres and Torres 2020). In this study, a stochastic model was formulated using the assumptions of an ordinary differential equation model of the system similar to that used by Kang et al. (2016) but including parameters for grooming and hygienic behaviours. ...
Honeybees are important plant pollinators. Unfortunately, there is a growing increase in the loss of honeybee colonies, and this is having a serious economic impact on crop farmers. A major cause of these losses is the parasitic mite Varroadestructor, which is a vector of deformed wing virus (DWV). Some bee species have resistant mechanisms, such as grooming and hygienic behaviours, against Varroa mites. A clear understanding of the effects of these control behaviours on the mites and the viruses they transmit can be important in reducing colony losses. Here, a stochastic model is formulated and analysed to consider the extent to which these control behaviours reduce the probability of an outbreak of DWV in honeybee colonies. Vector and bee-to-bee transmission routes are considered. Using branching process theory, it is shown that without any hygienic or grooming behaviour, a large probability of a DWV outbreak is possible. Also, if bees apply grooming or hygienic behaviour, this can reduce the probability of a virus outbreak, especially in the case of vector transmission, where it can be reduced to zero. Hygienic behaviour is the most significant factor in reducing a DWV outbreak. Thus, bee selection for hygienic behaviour may be important to reduce honeybee colony losses caused by DWV.
... Boot (1995) also highlighted that varroa mites invade drone cells approximately 12 times more frequently than worker cells within a honey bee colony, implying that invasion into drone cells occurs much faster than invasion into worker cells. Nevertheless, the lower mite infestation rate observed in adult worker bees than in brood bees suggests the regular grooming behaviour of adult worker bees to minimize varroa infestation rates by removing and damaging mites from their bodies (Pritchard, 2016). Interestingly, African honey bees have developed a distinctive grooming behaviour to remove phoretic mites from their bodies, which has been identified as a key factor in reducing varroa infestation at colony level (Bąk & Wilde, 2015;Nganso et al., 2017;Pritchard, 2016 in the Tigray region of Ethiopia (Begna, 2014), 83% in Kenya (Muli et al., 2014), 59% in Uganda (Chemurot et al., 2016) and 48% in Tanzania (Mumbi et al., 2014). ...
... Nevertheless, the lower mite infestation rate observed in adult worker bees than in brood bees suggests the regular grooming behaviour of adult worker bees to minimize varroa infestation rates by removing and damaging mites from their bodies (Pritchard, 2016). Interestingly, African honey bees have developed a distinctive grooming behaviour to remove phoretic mites from their bodies, which has been identified as a key factor in reducing varroa infestation at colony level (Bąk & Wilde, 2015;Nganso et al., 2017;Pritchard, 2016 in the Tigray region of Ethiopia (Begna, 2014), 83% in Kenya (Muli et al., 2014), 59% in Uganda (Chemurot et al., 2016) and 48% in Tanzania (Mumbi et al., 2014). Therefore, our current study shows an increasing trend in the prevalence rate and widespread distribu- Because the current situation may not ensure the survival of local bee colonies in the future in the face of the mite's rapid expansion, and lessons have to be learned from western countries on the global impact of this parasite on bee health and the beekeeping industry. ...
The varroa mite (Varroa destructor) is the most economically important parasitic pest of honey bees (Apis mellifera) that causes global colony decline and loss. Since its first detection in Ethiopia in 2010, little is known about the current infestation levels and contributing factors to the mite's distribution across the country. In this study, we conducted a large-scale assessment of varroa prevalence and infestation levels in managed colonies across three potential beekeeping regions of Ethiopia; Oromia, Amhara and Southern Nations, Nationalities and Peoples Region (SNNPR). A total of 360 samples from 39 apiaries were collected following standard protocols and the mite prevalence and infestation levels were determined using the established method of varroa research. Overall, 89% of sampled colonies were infested by the mite, with varying prevalence rates across the regions: 95.8% in Oromia, 85.2% in Amhara and 71.9% in SNNPR, indicating the widespread nature of the parasite throughout the country. The varroa infestation levels were lower in local hives (2.6 ± 5.9) than in frame hives (5.0 ± 0.9), and significantly higher in brood bees (5.6 ± 0.8) than in adult bees (1.93 ± 0.17) (p < 0.001). Possible factors contributing to the varied mite prevalence and infestation levels in the country include differences in agro-ecology, beekeeping practices, host age preference and the nature of bee hives. Therefore, our study provides insights into the current status of varroa prevalence and associated factors across regions in Ethiopia. Further investigation is required to explore the probable impact of the parasite on the health and productivity of local honey bees, in order to design future monitoring strategies.
... Disease management is an integral component of social evolution, because proximity to conspecifics increases risk of pathogen spread. In many social species, individuals perform behaviors that provide their groupmates disease or parasite protection ("social immunity" behaviors; Silk et al. 2003;Cremer et al. 2007Cremer et al. , 2018Smolinksy et al. 2009;Evans and Spivak 2010;Zhukovskaya et al. 2013;Stroeymeyt et al. 2014;Pritchard 2016). Grooming is one such phenotype; in group living animals, it has both self-directed (self-grooming) and social (allogrooming) forms, each with distinct implications for disease transmission to the group, and for individual and group survivorship (Fefferman et al. 2006;Boroczky et al. 2013;Zhukovskaya et al. 2013;Kalueff et al. 2016). ...
... The consequences of honey bee grooming behaviors remain unclear, and have not been thoroughly investigated across the variety of contexts that stimulate the behavior. For example, in studies focused on ectoparasites, there is relatively weak evidence that elevated allogrooming impacts mortality or parasite infestation at the colony level (at least for A. mellifera; Pettis and Pankiw 1998;Boecking and Spivak 1999;Evans and Spivak 2010;Pritchard 2016). Moreover, to our knowledge, no study has assessed mortality impacts of allogrooming or self-grooming for other contexts that elicit the behavior, e.g., pathogen infection (see Waddington and Rothenbuhler 1975). ...
In social animals, disease management behaviors such as grooming occur in response to diverse stimuli, making it difficult to interpret the evolution and function of these phenotypes. The honey bee has a grooming repertoire that includes self-directed behaviors and allogrooming from nestmates. Many stimuli provoke these behaviors, and their impacts on individual and colony survivorship are unclear. We evaluated the effects of two different stressors on grooming frequencies and survivorship. We found that self-grooming frequency is activated in distinct ways in response to pathogen infection, pesticide treatment, and social context. Moreover, self-grooming frequency predicts individual survival. Allogrooming interactions were less common and did not predict individual survival. The honey bee highlights the difficulty inherent in interpreting the evolution and function of grooming interactions in highly social species.
... Introduction grooming coupled with a high proportion of damaged mites has been shown to be associated with lower mite infestation levels in bees [21,29]. Nevertheless, the relationship between grooming intensity (and/or damage) and levels of mite-transmitted viruses remains unknown. ...
... The removal and damage of parasitic mites by a worker bee from its own body (autogrooming), or from a nest-mate's body (allo-grooming), are major behavioral mite-resistance traits in the Asian honey bee, Apis cerana [27], the original host of Varroa destructor [28]. These mite-resistance behaviors are also documented in the mite's western honey bee host, Apis mellifera, particularly as a long-term tolerance mechanism to Varroa in African honey bee subspecies [29]. Grooming is an important defensive mechanism against mites, as evidenced by the relationship between damaged mites and colony infestation level for both African and European honey bees [21,[59][60][61][62][63][64]. ...
Many pathogens and parasites have evolved to overwhelm and suppress their host’s immune system. Nevertheless, the interactive effects of these agents on colony productivity and wintering success have been relatively unexplored, particularly in large-scale phenomic studies. As a defense mechanism, honey bees have evolved remarkable social behaviors to defend against pathogen and parasite challenges, which reduce the impact of disease and improve colony health. To investigate the complex role of pathogens, parasites and social immunity behaviors in relation to colony productivity and outcomes, we extensively studied colonies at several locations across Canada for two years. In 2016 and 2017, colonies founded with 1-year-old queens of diverse genetic origin were evaluated, which represented a generalized subset of the Canadian bee population. During each experimental year (May through April), we collected phenotypic data and sampled colonies for pathogen analysis in a standardized manner. Measures included: colony size and productivity (colony weight, cluster size, honey production, and sealed brood population), social immunity traits (hygienic behavior, instantaneous mite population growth rate, and grooming behavior), as well as quantification of gut parasites (Nosema spp., and Lotmaria passim), viruses (DWV-A, DWV-B, BQCV and SBV) and external parasites (Varroa destructor). Our goal was to examine: 1) correlations between pathogens and colony phenotypes; 2) the dynamics of pathogens and parasites on colony phenotypes and productivity traits; and 3) the effects of social immunity behaviors on colony pathogen load. Our results show that colonies expressing high levels of some social immunity behaviors were associated with low levels of pathogens/parasites, including viruses, Nosema spp., and V. destructor. In addition, we determined that elevated viral and Nosema spp. levels were associated with low levels of colony productivity, and that five out of six pathogenic factors measured were negatively associated with colony size and weight in both fall and spring periods. Finally, this study also provides information about the incidence and abundance of pathogens, colony phenotypes, and further disentangles their inter-correlation, so as to better understand drivers of honey bee colony health and productivity.
... There are 2 major categories of bee's grooming behavior: self-grooming (also known as autogrooming) and intergrooming (also known as allogrooming). 64 Self-grooming behavior is effective at removing pollen grains and restraining V. destructor and Acarapis woodi (tracheal mites) population growth. 65,66 Intergrooming is characterized by the performance of a grooming dance by a bee to get assistance from nestmates to remove particles or parasites, like V. destructor, from their bodies. ...
... 65,66 Intergrooming is characterized by the performance of a grooming dance by a bee to get assistance from nestmates to remove particles or parasites, like V. destructor, from their bodies. 64 Honey bee genotypes vary in their ability to express grooming behavior. For example, Africanized honey bees (descendants of A mellifera scutellata) are more effective at removing mites from their bodies compared with European bees. ...
At the individual level, honey bees (Apis mellifera) rely on innate immunity, which operates through cellular and humoral mechanisms, to defend themselves against infectious agents and parasites. At the colony level, honey bees have developed collective defense mechanisms against pathogens and pests, such as hygienic and grooming behaviors. An understanding of the immune responses of honey bees is critical to implement strategies to reduce mortality and increase colony productivity. The major components and mechanisms of individual and social immunity of honey bees are discussed in this review.
... mellifera) has developed a set of behavioral defenses against Varroa mites to keep the mite population low, such as grooming, biting, and performing hygienic behaviors (Ruttner and Hänel, 1992;Spivak, 1996;Arechavaleta-Velasco and Guzmán-Novoa, 2001;Guzman-Novoa et al., 2012;Tsuruda et al., 2012;Villa et al., 2017). The biting behavior of worker bees, which is also considered a type of grooming behavior, enables them to bite adult mites, and remove the mites from their bodies (Peng et al., 1987;Ruttner and Hänel, 1992;Pritchard, 2016). Colonies selected for mite-biting behavior by instrumental insemination or open mating with feral colonies potentially will have greater fitness over subsequent generations. ...
... Previous research on grooming behavior and damaged mites in Apis has shown that grooming behavior is a selected trait in naturally mite-resistant colonies (Peng et al., 1987;Boecking and Ritter, 1993;Fries et al., 1996;Arechavaleta-Velasco and Guzmán-Novoa, 2001;Russo et al., 2020). The mite-biting or grooming behavior of honey bees, as a defensive behavior against parasitic Varroa mites, can be used as a parameter to select for Varroa mite resistance in honey bee stocks (Spivak, 1996;Rinderer et al., 2010;Hunt et al., 2016;Pritchard, 2016;Morfin et al., 2019). ...
The honey bee (Apis mellifera) is the most important managed pollinator to sustainable agriculture and our ecosystem. Yet managed honey bee colonies in the United States experience 30–40% losses annually. Among the many biotic stressors, the parasitic mite Varroa destructor is considered one of the main causes of colony losses. Bees’ mite-biting behavior has been selected as a Varroa-tolerant or Varroa-resistant trait in the state of Indiana for more than a decade. A survey of damaged mites from the bottom of a colony can be used as an extended phenotype to evaluate the mite-biting behavior of a colony. In this study, on average, 37% of mites sampled from the breeding stocks of 59 colonies of mite biters in Indiana were damaged or mutilated, which is significantly higher than the 19% of damaged mites found in commercial colonies in the southern United States. Indiana mite biter colonies had a higher proportion of damaged mites, although among the damaged mites, the number of missing legs was not significantly higher. In addition, the morphology of pollen-forager worker bee mandibles was compared by X-ray microcomputed tomography for six parameters in two populations, and a difference was detected in one parameter. Our results provide scientific evidence that potentially explains the defensive mechanism against Varroa mites: structural changes in the worker bee mandibles.
... In addition, fluctuations in brood production may explain, at least partly, why within-colony distribution of V. destructor is spatially heterogeneous [79,80], which affects the expression of VSH: a stronger VSH response is obtained if many infested cells are clustered in a small brood area [81]. Also affected by brood dynamics is the proportion of damaged mites, which is used as a proxy for the grooming ability of a colony [82]. More damage was recorded when the brood was emerging [83], possibly due to mites being more vulnerable to grooming Fig. 1 Overview of the theoretical framework known to lead to genetic progress towards a selection objective and to a successful solution to the V. destructor problem via selective breeding (above) and evaluation of data availability as well as of the relevance and efficacy of traits under selection for each of the steps towards achievement of the objective (below) ...
... In addition, infestation levels depend directly on brood quantities, which can be affected by multiple factors, including beekeeping management (e.g., hive size, colony divisions) as well as food resources and climate [127][128][129]. Grooming is also affected by climatic conditions [82], with less grooming being performed in spring than in summer [130]. The impact of grooming on mite mortality is generally reduced at lower temperatures [131,132] and at higher humidity [132], indicating that selecting this particular trait could be insufficiently efficient to reduce the mite population significantly during wintertime, when grooming could have a strong impact since brood is generally absent and all mites are exposed to this behavior. ...
Background
In spite of the implementation of control strategies in honey bee ( Apis mellifera ) keeping, the invasive parasitic mite Varroa destructor remains one of the main causes of colony losses in numerous countries. Therefore, this parasite represents a serious threat to beekeeping and agro-ecosystems that benefit from the pollination services provided by honey bees. To maintain their stocks, beekeepers have to treat their colonies with acaricides every year. Selecting lineages that are resistant to infestations is deemed to be a more sustainable approach.
Review
Over the last three decades, numerous selection programs have been initiated to improve the host–parasite relationship and to support honey bee survival in the presence of the parasite without the need for acaricide treatments. Although resistance traits have been included in the selection strategy of honey bees, it has not been possible to globally solve the V. destructor problem. In this study, we review the literature on the reasons that have potentially limited the success of such selection programs. We compile the available information to assess the relevance of selected traits and the potential environmental effects that distort trait expression and colony survival. Limitations to the implementation of these traits in the field are also discussed.
Conclusions
Improving our knowledge of the mechanisms underlying resistance to V. destructor to increase trait relevance, optimizing selection programs to reduce environmental effects, and communicating selection outcomes are all crucial to efforts aiming at establishing a balanced relationship between the invasive parasite and its new host.
... Otherwise, wing marking will give excellent results in the first part of the season, but the colored area is expected to decrease over time. The reason for this is likely the high mobility of the wings (compared to the thorax and abdomen), as well as mutual grooming and self-grooming by the queens [44,45], which leads to paint removal over time. ...
While marking queens is an optional rather than mandatory technique, it is increasingly becoming a standard practice in modern beekeeping. Finding queens in strong colonies and large apiaries is a time-consuming process. The visible and durable marking of the queen enables it to be seen more quickly, directly improving productivity in apiary management. This study examined a new technique for marking queens using an oil-based marker, which involved marking not only the thorax (as a standard technique) but also the wings and abdomen. The durability of the marking was assessed by measuring color retention at the start of the experiment and after five months. Two groups of queens were formed: an experimental group, marked with the new technique on three body parts—Group O (n = 12) and a control group of unmarked queens—Group N (n = 12). The most durable color retention was observed on the thorax (54.4%) and abdomen (14.4%), while retention on the wings was weaker (2.4%), necessitating reapplication during the season. Considering the proportion of the total marked area, abdomen marking gave better results (9.5%) compared to the thorax (5.4%) and wings (0.6%) marking. The application of this marking technique showed no negative effects on queen acceptance, survival, or supersedure. Marking three body parts can increase the queen’s visibility in a non-invasive way, improving work efficiency.
... The main defense mechanisms against Varroa mites that bees can employ are grooming behavior, Varroa-sensitive hygiene (VSH), and suppressed mite reproduction (SMR) [28]. By performing grooming behavior, adult bees remove parasites from themselves or other bees [29]. VSH, a form of hygienic behavior, involves workers detecting and removing mite-infested broods specifically [30,31]. ...
Background/Objectives: The increasing pressure from pathogens and parasites on Apis mellifera populations is resulting in significant colony losses. It is desirable to identify resistance-associated single-nucleotide polymorphisms (SNPs) and their variability for the purpose of breeding resilient honeybee lines. This study examined the genetic diversity of 13 SNPs previously studied for associations with various resistance-providing traits, including six linked to Varroa-specific hygiene, five linked to suppressed mite reproduction, one linked to immune response, and one linked to chalkbrood resistance. Methods: Genotyping was performed using a novel SNaPshot genotyping panel designed for this study. The sample pool consisted of 308 honeybee samples in total, covering all 77 administrative districts of the Czech Republic. Results: All examined loci were polymorphic. The frequency of positive alleles in our population is medium to low, depending on the specific SNP. An analysis of genotype frequencies revealed that most loci exhibited the Hardy–Weinberg equilibrium. A comparison of the allele and genotype frequencies of the same locus between samples from hives and samples from flowers revealed no significant differences. The genetic diversity, as indicated by the heterozygosity values, ranged from 0.05 to 0.50. The fixation index (F) was, on average, close to zero, indicating minimal influence of inbreeding or non-random mating on the genetic structure of the analyzed samples. Conclusions: The obtained results provide further insights into the genetic variation of SNPs associated with the immune response and resistance to pathogens in honeybee populations in the Czech Republic. This research provides a valuable foundation for future studies of honeybee diversity and breeding.
... It would be interesting to test this hypothesis and quantify autoand allo-grooming during the experiment, which could potentially displace mites from their ventral position. Bees' hygienic behaviour 45 should definitely be investigated in the future to understand the precise role of honey bees in the contact-making between lactic acid and mites. In addition, to better characterise the valence of lactic acid for honey bees compared to known odours, a behavioural assay in a Y-maze would be important. ...
Lactic acid is an alternative treatment to hard chemicals against Varroa destructor, the parasitic mite of the Western honey bee Apis mellifera. This soft acaricide is used only for small apiaries due to its laborious administration. However, the mode of action of this honey bee medication remains unknown. Previous studies showed that a direct contact between the arolia of V. destructor and lactic acid altered their morphology and led to an impairment of grip. Yet, there is no evidence for the way of action of lactic acid in a realistic in-hive scenario, i.e. after an indirect exposure of the mite through honey bees. We investigated the nature of lactic acid activity in the hive treatment context. The local and/or systemic way of action of this honey bee treatment against V. destructor was studied through a behavioural and toxicological approach at the individual level. On one hand, we confirmed the altered morphology for the arolia of mites and studied the evolution of the process over time. On the other hand, we found that haemolymph contaminated with lactic acid did not kill the feeding parasitic mite. These findings support a local mode of action. In order to unravel the sequence of events leading to the local contact between the acid and the mite on bees, we also documented the olfactory valence of lactic acid for A. mellifera and V. destructor. This work provides a new comprehension of lactic acid activity against the parasitic mite through honey bee exposure and gives new opportunities for control strategies against V. destructor.
... A widespread infestation of animals could potentially lead to the complete destruction of all beehives. Varroa mites are consequently considered to be the most economically damaging parasitic mites in the beekeeping sector [2][3]. Synthetic miticides have proven to be highly effective in managing Varroa mite infestations within beehives. ...
The bee Apis mellifera (Hymenoptera: Apidae) has a family called the Varroidae, which includes several distinct species. "Varroatosis" is the medical term for an illness that originates from an animal. By feeding on honeybees' hive nectar, this mite has a devastating effect on all honeybee life stages. This study aimed to assess the miticidal activity of leaf extracts from Lantana camara, Rhazya stricta, Ruta chalepensis, and Heliotropium bacciferum against the Varroa mite. L. camara, R. stricta, R. chalepen-sis, and H. bacciferum extracts were tested for their ability to suppress parasite bee mites (Varroa dest-ructor). The concentration of four extracts was applied in both laboratory and field conditions In Saudi Arabia in 2020. After 48 hours of 500 ppm miticide exposure, L. camara died 100% and R. stricta 96%. Compared to other extracts, ethanolic leaf extract killed Varroa mites the most. Mite invasion rate in honeybee hives treated with various materials from different plants at varied intervals declined to 0% after 12 days with 500 ppm of L. camara-derived materials but dropped to 0.1% with Mitac (60 mg/co-lony). The average invasion rate for R. stricta, R. chalepensis, and H. bacciferum leaves was 0.21, 1.03, and 3.11. The most effective extracts were L. camara and R. stricta. The tested chemicals had little or no effect on bees at varied dosages and times. This investigation stated that the use of natural plant materials as safe biodegradable materials should be used to control honeybee mites of Varroa especially L. camara and R. stricta.
... Tımar davranışı nispeten basittir ve yetişkin arıların dış yüzeylerindeki yetişkin akarların uzaklaştırılmasını ve etkisiz hale getirilmesini içermektedir (Pritchard, 2016). Bal arılarında davranışsal direnç mekanizmalarından diğeri olan tımar davranışı, omurgalılar ve eklembacaklılar arasında ektoparazitlerden kurtulmak için yaygın görülen bir stratejidir. ...
... Grooming behavior is typically a straightforward process, involving the cleaning and incapacitation of mites found on the bodies of adult bees (Pritchard, 2016). Another behavioral resistance mechanism in honey bees, grooming behavior, is a common strategy observed among vertebrates and arthropods to rid themselves of ectoparasites. ...
Honey bees, known as eusocial organisms, have developed behavioral strategies for various purposes
in the course of evolution. These strategies have been shaped through adaptation processes to fulfill
important functions such as maintaining colony life, protecting their offspring, finding resources, and
coping with various environmental challenges. Bee behaviors, particularly, encompass specific
behavioral resistance mechanisms against diseases and ectoparasites. Behavioral resistance is
generally examined under two main categories: hygienic and grooming behaviors. Hygienic behavior
involves the detection of diseased or parasitized larvae and pupae, the removal of infected/infested
brood, thus reducing the spread of infection/infestation. Grooming behavior is classified into two
categories based on the performer: auto- grooming and allo- grooming. A uto- grooming refers to self -
grooming behavior, while allo- grooming describes mutual grooming between two bees or the
grooming of one bee by several bees acting socially together. This review emphasizes the potential of
honey bee populations in struggling the honey bee ectoparasite Varroa destructor by examining how
hygienic and grooming behaviors are influenced by genetic and environmental factors. Additionally, it
can serve as an important resource to guide future research and to better understand the effects of
Varroa destructor challenges on the sustainability of bee colony populations.
... Among mite-resistance traits, grooming behavior involves the removal and injury of adult mites from the bodies of adult bees (Peng et al., 1987). Through this behavior, adult bees clean their bodies by grooming themselves ("auto-grooming") and by being groomed by other bees ("allo-grooming") (reviewed by Pritchard, 2016;van Alphen and Fernhout, 2020). Grooming against Varroa has been associated with higher proportions of mutilated fallen mites and lower infestation levels at the colony level (Mondragoń et al., 2005;Arechavaleta-Velasco et al., 2012;Russo et al., 2020). ...
Grooming behavior is one of the mechanisms of social immunity in Apis mellifera. This behavior has been proposed as an active strategy of honey bees to restrain the population growth of the ectoparasitic mite Varroa destructor in honey bee colonies. The characterization of honey bee stocks with high grooming behavior is of utmost importance for honey bee breeding programs to set the background for mite resistance biomarker-based selection. In this study, we analyzed the expression level of 11 candidate genes putatively involved in grooming and hygiene behaviors in adult workers from mite-resistant (R) and mite-susceptible (S) honey bee stocks. Heads and bodies of worker bees from both stocks, previously tested for grooming response to two treatments (mite infestation and a paintbrush touch control stimulus) were assessed by qPCR. In the head, R bees exposed to mite infestation showed higher levels of Nrx1 and Dop2 and lower levels of Obp3 than S bees. At the body level, R and S bees differed in the expression levels of Nrx1, Oa1, Obp4, Obp14, Obp16, Obp18, Spf45, CYP9Q3 , with no stimulus-specific pattern. Overall, our results suggest the involvement of some of the analyzed genes in the specific response to mite infestation, possibly related to the sensitivity and specificity of the R bee to this stimulus at the head level, while other genes would be involved in the non-specific motor response to irritants at the body level. The present study provides new insights into the characterization of the grooming behavior in a selected honey bee stock and increases the available information on its underlying molecular mechanisms. We discuss the putative functions and use of the assessed genes as potential tools for biomarker-assisted selection and improvement of Varroa mite control strategies in honey bee colonies.
... Resistance breeding has mostly focused on four selection criteria: mite non-reproduction or decreased mite reproduction (MNR or DMR; previously described as suppressed mite reproduction [SMR]) Von Virag et al., 2022), varroa sensitive hygiene (VSH) (Dietemann et al., 2013;Harbo & Harris, 2005), recapping (REC) (Oddie et al., 2018), and grooming (Pritchard, 2016;Russo et al., 2020). ...
A sustainable solution to the global threat of the Varroa destructor mite is the selection of varroa‐resistant honey bee (Apis mellifera) colonies. Both “mite non‐reproduction” (MNR) and “varroa sensitive hygiene” (VSH) appear to be promising selection traits for achieving the goal of a resistant honey bee. MNR describes colonies that have a high number of non‐reproductive mites (no offspring, no males, or delayed development of mite offspring). High numbers of non‐reproductive mites have been observed in selected colonies, but the mechanism behind this trait has not yet been identified. The specialized hygienic behavior of selected honey bees, called VSH, is the removal of varroa‐infested brood. These traits were thought to be linked by VSH bees preferentially removing reproductive varroa females leaving only non‐reproductive mites behind in cells and thus creating colonies with high levels of MNR. To further investigate this link, we used an experimental setup and data sets from a four‐year selection project designed to breed for MNR and VSH colonies. In addition, we sought to answer the question of whether non‐reproductive mites are a direct consequence of worker removal behavior. To test this, we artificially induced removal behavior, and after providing the mite with enough time to re‐enter another cell, we opened all capped cells, relocated the mites, and evaluated their reproduction. As shown in previous studies and in this study, VSH had no effect on MNR levels. Also, the induced removal behavior did not lead to non‐reproduction in the subsequent reproductive cycle post interruption. We thus concluded that breeding for non‐reproductive mites does not automatically breed for VSH behavior and worker removal behavior does not cause subsequent reproductive failure of the mites forced to flee and find a new cell for reproduction.
... Bumble bees can guard their provinces from Varroa vermin using specific practices including preparing habits (GB). Making harms Varroa bugs (for example GB) is a heritable persona in A. mellifera (Pritchard, 2016). Phoretic Varroa parasites; founders, gravid or little woman bugs are introduced to preparing through honey bees particularly girl bugs A lookup center have a look at has been created by (Aumeier, 2001) to survey the GB of bumble bees falsely pervaded with Varroa parasites. ...
... This explains a strong grooming behavior of A. m. bandasii stocks that could likely inflict damage to the mites' bodies and this might be contributed for colony survival. In agreement with this, Pritchard (2016) explained that colonies inflicting about 60% body damage to the total fallen mites are capable of limiting the mite infestation level and can survive the Varroa infestation without chemical treatment. Consequently, the higher intensity of grooming behavior and injuries that the bees inflict on the body of the mite can significantly influence the mites reproduction cycle and population growth in Varroa-surviving colonies (Dadoun et al., 2020;Russo et al., 2020). ...
The parasitic mite V. destructor has caused long-lasting losses to the survival of European honeybee colonies. In contrast, African honeybees are likely capable of surviving the effects of this parasitic mite with varying defense mechanisms. This study provides insights into two defense behavioral traits, including hygienic and grooming behaviors of local honeybee, Apis mellifera bandasii colonies against V. destructor mite in Ethiopia. Hygienic behavior (HB) was evaluated using the standard pin-killed brood method by calculating the dead brood removal rates (%) at 24 and 48 hrs. While grooming behavior (GB) was assessed by measuring the number of daily fallen mites and the percentage of damaged mites. The results of hygienic behavior showed greater brood removal rates of 83.1±14.3% and 97.6±3.4% at 24 hrs and 48 hrs, respectively. There were strong negative correlations between the HB and Varroa infestation rates, indicating that HB has the potential to reduce the mite population in colonies. Grooming behavior also showed higher mean daily fallen mites per colony (16.3±10.2), of which about 80% of the total fallen mites (n=488) were damaged. Ten body damage categories were identified, with most damages inflicted on mites' legs, dorsal shield, and gnathosoma because of the GB. Our study suggests that combined hygienic and grooming behaviors could be used as effective defenses against V. destructor infestations in A. m. bandasii colonies. Therefore, future selective breeding programs should integrate these specific host defenses in order to produce sustainable colonies resistant to this parasitic mite.
... First, mites could be dislodged by the grooming behaviour of bees and come into contact with lactic acid. Regardless of the condition, we observed two grooming behaviours in honeybees: auto-grooming and allo-grooming [63]. Second, lactic acid could attract or repel mites, inducing a movement of Varroa females from their initial feeding site, thus touching the acid. ...
Beekeepers can use a variety of treatments against Varroa destructor, the parasitic mite of Apis mellifera. However, sustainable and easy-to-use solutions are still scarce, considering the complexity of reaching the parasite alone. Current treatments involve soft acaricides, although their mechanism of action is not well understood. We investigated the effects of organic acids such as tartaric, lactic, formic, and citric acids on the attachment abilities of V. destructor under laboratory conditions. Preventing parasites from gripping or holding on to their hosts is a crucial target for mite control strategies. We challenged grip skills through the Rotavar setup after the direct application of acids to mites’ arolia. We also tested the potential for mites to fall off honeybees after bee treatment. We found that tartaric, citric, and lactic acids were good candidates to impair the attachment of V. destructor twenty-four hours post-treatment. However, lactic acid remained the only candidate at a reasonable concentration to destabilise mites after the honey bee’s treatment without reducing their lifespan. While we conducted these experiments under artificial conditions, our results improved our comprehension of the organic acids’ potential impact on V. destructor. They can also help with the development of new methods for hive application for beekeepers worldwide.
... rapidly, which appears to be their natural locomotory style. This is an adaptation that must benefit the life cycle of the mite, as they need to move around on various substrates and remain safe from honeybees (e.g., the adult bee body where mites move between the abdominal tergites to feed and also avoid removal by bees 45,46 , and the wax cell which they must navigate around to defecate, reproduce and avoid being squashed by the spinning larvae 47,48 . ...
Little is known about mite gait, but it has been suggested that there could be greater variation in locomotory styles for arachnids than insects. The Varroa destructor mite is a devastating ectoparasite of the honeybee. We aim to automatically detect Varroa-specific signals in long-term vibrational recordings of honeybee hives and additionally provide the first quantification and characterisation of Varroa gait through the analysis of its unique vibrational trace. These vibrations are used as part of a novel approach to achieve remote, non-invasive Varroa monitoring in honeybee colonies, requiring discrimination between mite and honeybee signals. We measure the vibrations occurring in samples of freshly collected capped brood-comb, and through combined critical listening and video recordings we build a training database for discrimination and classification purposes. In searching for a suitable vibrational feature, we demonstrate the outstanding value of two-dimensional-Fourier-transforms in invertebrate vibration analysis. Discrimination was less reliable when testing datasets comprising of Varroa within capped brood-cells, where Varroa induced signals are weaker than those produced on the cell surface. We here advance knowledge of Varroa vibration and locomotion, whilst expanding upon the remote detection strategies available for its control.
... Later on, the mechanisms that honey bees rely on to fight the mite became evident and include grooming behavior [18,19], hygienic behavior [18][19][20][21], and suppressed mite reproduction [22,23]. Grooming is the detection, aggressive removal, and destruction of adult mites from the bodies of adult bees [24], whereas hygienic behavior (now termed 'Varroa Sensitive Hygiene' (VSH)) is a three-step process consisting of detection, opening, and removal of infested pupae by worker bees [25]. Suppressed mite reproduction represents the inability of the mites to reproduce in the brood cell. ...
Simple Summary
Globally, honey bees are exposed to many challenges, such as the Varroa destructor mite and various viruses, which lead to massive losses. It is generally believed that African honey bees are more resilient and better able to cope with these stressors. This study examined some molecular markers that may be associated with this resilience. Higher resistance to the varroa mite could be related to better olfactory sensing. Higher gene expression levels of the odorant binding protein OBP14 in the antennae of Ethiopian honey bees suggest that reproducing mites might be better detected and cleaned. Resistance or tolerance to viruses could be attributed to a better functioning antiviral RNAi system. Several genes involved in this pathway are upregulated and are positively correlated with the viral load in honey bees. Both mechanisms may contribute to the resilience of African bees to varroa infestation and viral infection.
Abstract
Varroa destructor mites and the viruses it vectors are two major factors leading to high losses of honey bees (Apis mellifera) colonies worldwide. However, honey bees in some African countries show resilience to varroa infestation and/or virus infections, although little is known about the mechanisms underlying this resilience. In this study, we investigated the expression profiles of some key molecular markers involved in olfactory sensing and RNA interference, as these processes may contribute to the bees’ resilience to varroa infestation and virus infection, respectively. We found significantly higher gene expression of the odorant binding protein, OBP14, in the antennae of Ethiopian bees compared to Belgian bees. This result suggests the potential of OBP14 as a molecular marker of resilience to mite infestation. Scanning electron microscopy showed no significant differences in the antennal sensilla occurrence and distribution, suggesting that resilience arises from molecular processes rather than morphological adaptations. In addition, seven RNAi genes were upregulated in the Ethiopian honey bees and three of them—Dicer-Drosha, Argonaute 2, and TRBP2—were positively correlated with the viral load. We can conclude that the antiviral immune response was triggered when bees were experiencing severe viral infection and that this might contribute to the bees’ resilience to viruses.
... For example, transportation by the host bees enables the mites to reach new brood cells in both, the current colony by using nurse bees, as well as non-natal colonies by attaching to drifting or robbing foragers (Frey and Rosenkranz 2014;Nazzi and Le Conte 2015;Peck and Seeley 2019). On the other hand, it may also pose dangers for the mites (Pritchard 2016;Rosenkranz et al. 2010;Xie et al. 2016) and is not obligatory for successful reproduction in every case (de Ruijter 1987;Häußermann et al. 2016). Our results show that a decrease in reproductive success on colony level can add to these previously described negative effects for the mites if the dispersal phase is prolonged. ...
The parasitic mite Varroa destructor (Anderson & Trueman) spends the dispersal phase of its life cycle on adult honeybees ( Apis mellifera L.). The meaning of this phase for both bees and mites is still not well understood. This especially applies to prolonged dispersal phases as a result of brood interruptions. Hence, it is highly important to unravel this phase for understanding the underlying biological mechanisms and implementing this knowledge in beekeeping practice and research efforts. We investigated the effects of brood interruptions on honeybee colonies and the mites naturally infesting them. Reproduction parameters, brood infestation and recapping frequency were monitored over 60 days after brood interruptions of varying durations. Our results show that recapping frequency and mite non-reproduction increased during the interruption of egg laying. The duration of interruption and the time elapsed afterwards additionally affected the occurrence of reproductive failure. Hence, the reproduction of mites was affected by brood breaks immediately and in the long run.
... 28 Honey bees utilize a variety of grooming behaviors to dislodge and kill Varroa. 29 Higher temperatures increase the rate of Varroa removal from honey bees and this effect is amplified in stocks selected for high grooming behavior. 30 The background levels of Varroa dislodging under control conditions at room temperature (22-24°C) in the amitraz efficacy test is very low, although variation is still possible outside these conditions. ...
BACKGROUND
The parasitic mite, Varroa destructor (Anderson and Trueman), is a leading cause of honey bee colony losses around the world. Application of miticides such as amitraz are often the primary method of Varroa control in commercial beekeeping operations in the United States. It is likely that excessive and exclusive amitraz application has led to the development of amitraz resistance in Varroa. A mutation of tyrosine at amino acid position 215 to histidine (Y215H) in the β2‐octopamine receptor was identified in putatively amitraz‐resistant Varroa in the United States. This research investigated the presence of the Y215H mutation in quantitatively confirmed amitraz‐resistant Varroa from the United States.
RESULTS
There was a strong association of susceptible and resistant phenotypes with the corresponding susceptible and resistant genotypes respectively, and vice versa. The resistance bioassay may understate resistance levels because of the influence of environmental conditions on the outcome of the test, whereby Varroa with an amitraz‐resistant genotype may appear with a susceptible phenotype.
CONCLUSION
Confirmation of the Y215H mutation in the β2‐octopamine receptor of amitraz‐resistant Varroa encourages the development and validation of low‐cost, high‐throughput genotyping protocols to assess amitraz resistance. Resistance monitoring via genotyping will allow for large‐scale passive monitoring to accurately determine the prevalence of amitraz resistance rather than directed sampling of apiaries with known resistance issues. Genotyping of Varroa for amitraz resistance early in the beekeeping season may predict late‐season resistance at the colony level and provide beekeepers with enough time to develop an effective Varroa management strategy. © 2023 Society of Chemical Industry. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.
... Allogrooming is a common trait displayed by honeybees in resisting the parasite and it has been found that Apis mellifera shows lesser resistance than the host Apis cerana (Dorian J. Pritchard, 2016) in which it was first discovered. In relation to the paper by Gabel et. ...
... Through this behavior, the parasitized bees can dislodge themselves and injure mites using their legs and mandibles (autogrooming) or receiving help from other bees (allogrooming) (Boecking and Spivak 1999). Such behavior is considered an important trait in the defense against V. destructor in Apis cerana Fabricius, the original host species of the mite (Büchler et al. 1992;Peng et al. 1987; reviewed by Pritchard 2016). Even though the importance of grooming behavior as a mechanism conferring mite resistance to A. mellifera colonies has been a controversial issue, a growing body of evidence suggests that this trait can increase mite mortality and hence modulate its population growth in colonies, specifically in Africanized honey bee populations (Morse et al. 1991;Moosbeckhofer 1992;Ruttner and Hänel 1992;Boecking and Ritter 1993;Moretto et al. 1993;Bienefeld et al. 1999;Arechavaleta-Velasco and Guzmán-Novoa 2001;Guzmán-Novoa et al. 2012;Invernizzi et al. 2016;Nganso et al. 2017) as well as stocks of European origin (Dadoun et al. 2020;Russo et al. 2020). ...
Grooming behavior confers resistance to honey bees against Varroa destructor, being of interest to social immunity studies and breeding programs. The objective of this study was to characterize at the individual level the grooming behavior of mite-resistant (R) and susceptible (S) A. mellifera stocks from Argentina. Assays were performed in experimental arenas by applying two treatments to nurse bees: (1) placing a V. destructor mite on the bee’s thorax and (2) touching the bee with a paintbrush. Grooming reactions were recorded on bees from both stocks at the ages of 6, 10, and 14 days after emergence. R bees exhibited lower time of first response against the mite, performed more cleaning attempts, and used all their legs with a higher probability compared to S bees. The same pattern was evident when younger and older bees from the R stock were compared. The results demonstrate that bee age and genetic
... Through this behavior, the parasitized bees can dislodge themselves and injure mites using their legs and mandibles (autogrooming) or receiving help from other bees (allogrooming) (Boecking and Spivak 1999). Such behavior is considered an important trait in the defense against V. destructor in Apis cerana Fabricius, the original host species of the mite (Büchler et al. 1992;Peng et al. 1987; reviewed by Pritchard 2016). Even though the importance of grooming behavior as a mechanism conferring mite resistance to A. mellifera colonies has been a controversial issue, a growing body of evidence suggests that this trait can increase mite mortality and hence modulate its population growth in colonies, specifically in Africanized honey bee populations (Morse et al. 1991;Moosbeckhofer 1992;Ruttner and Hänel 1992;Boecking and Ritter 1993;Moretto et al. 1993;Bienefeld et al. 1999;Arechavaleta-Velasco and Guzmán-Novoa 2001;Guzmán-Novoa et al. 2012;Invernizzi et al. 2016;Nganso et al. 2017) as well as stocks of European origin (Dadoun et al. 2020;Russo et al. 2020). ...
Grooming behavior confers resistance to honey bees against Varroa destructor, being of interest to social immunity studies and breeding programs. The objective of this study was to characterize at the individual level the grooming behavior of mite-resistant (R) and susceptible (S) A. mellifera stocks from Argentina. Assays were performed in experimental arenas by applying two treatments to nurse bees: (1) placing a V. destructor mite on the bee’s thorax and (2) touching the bee with a paintbrush. Grooming reactions were recorded on bees from both stocks at the ages of 6, 10, and 14 days after emergence. R bees exhibited lower time of first response against the mite, performed more cleaning attempts, and used all their legs with a higher probability compared to S bees. The same pattern was evident when younger and older bees from the R stock were compared. The results demonstrate that bee age and genetic origin are critical factors of grooming behavior in honey bees.
... There is very little evidence for this. Honeybees engage in self-and allo-grooming to rid themselves of Varroa mites (Pritchard 2016, Russo et al. 2020, even developing morphological changes in their mandibles when infestations are high to successfully attack and kill these mites (Smith et al. 2021). Riders are usually minute relative to the size of the vehicle and use attachment mechanisms (anal pedicel, suckers, spines, tarsal pads), and external or internal attachment locations (entering through spiracles or sheltering beneath elytra), that make removal difficult, even if detected. ...
The ability to disperse is vital for all organisms, but especially for those whose habitats deteriorate, necessitating relocation to better feeding or breeding sites. Phoresy is assisted dispersal in which one organism uses another as its vehicle. In this review, phoresy will be largely restricted to cases wherein the rider is not parasitic on the vehicular stage used for dispersal, and in which insects are riders or rides. Phoresy occurs in organisms with limited mobility, and in secondarily brachypterous or completely wingless insects. Intraspecific phoresy also occurs. Generally, immature stages resistant to environmental assaults, such as dauers in nematodes, triungulins in beetles, or deutonymphs in mites, undertake phoresy. A size differential between rider and rider enables several conspecifics to board the same vehicle, likely ensuring mating opportunities at the destination. Riders may have special attachment devices or adhesive secretions to ensure safety during travel. Life cycles of riders and vehicles are often synchronized, and when phoresy is mutualistic, vehicles may also employ chemical tactics to achieve this synchrony. Chemical cues help to identify the appropriate vehicle, for disembarkation, or to lure the vehicle towards riders. Most riders prefer female vehicles, possibly to ensure access to rich nesting sites. Density-dependent selection may operate to limit the number of riders on a vehicle and phoresy may also facilitate sexual selection among riders. Whether vehicles can avoid phoresy is barely understood. This review attempts to place phoresy within a broad evolutionary context and points out the paucity of knowledge in certain research areas.
... Video-recording is probably the only possible method for quantifying natural bee-to-bee guarding behaviour which has not been influenced by human disturbance. It has not been widely documented that drone bees practice grooming behaviour (Pritchard, 2016), however, we observed multiple instances of this in our video-recordings (included in total quantification of self-grooming behaviour). ...
... Winter samples had a greatly reduced abundance of cuticular/chitin proteins in comparison to summer samples in both the head and abdomen analysis. Winter workers may have less damage to their exoskeleton compared to nurse or forager summer bees as there is a reduction in water evaporation due to lower temperatures, little to no transport of external materials into the hive, no brood and a diminished level of hygienic behaviour involving "licking" or cleaning (Seehuus et al., 2013;Pritchard, 2016). ...
Apis mellifera workers display two stages; short lived summer bees that engage in nursing, hive maintenance and foraging, and long lived winter bees (diutinus bees) which remain within the hive and are essential for thermoregulation and rearing the next generation of bees in spring before dying. Label free quantitative proteomic analysis was conducted on A. mellifera workers sampled in June and December to compare the proteomes of summer and winter bees. Proteomic analysis was performed on head, abdominal and venom sac samples and revealed an elevated level of protein abundance in summer bees. Head and abdominal samples displayed an increased abundance in cuticular proteins in summer samples whereas an increase in xenobiotic proteins was observed in winter samples. Several carbohydrate metabolism pathways which have been linked to energy production and longevity in insects were increased in abundance in winter samples in comparison to summer samples. Proteomic analysis of the venom sacs of summer samples showed an increased abundance of bee venom associated proteins in comparison to winter workers. These data provides an insight into the adaptions of A. mellifera workers in summer and winter and may aid in future treatment and disease studies on honeybee colonies. Data are available via ProteomeXchange with identifier PXD030483.
... Honey bees have developed antiparasite behaviors to prevent mite parasitism (Shakhar 2019;Spivak and Danka 2020). Autogrooming, allogrooming, in which workers groom other nestmates, and hygienic behavior, in which workers remove brood infested with mites, comprise the behavioral immune system in honey bees (Danka and Villa 1998;Pritchard 2016;Spivak and Danka 2020). The behavioral immune system requires recognition followed by the appropriate behavior, and it can be also affected by neonicotinoids. ...
The European honey bee, Apis mellifera, is the most common and important pollinator of crops worldwide. Honey bees are damaged by destructive parasitic mites, but they also have evolved a behavioral immune system to remove them. Exposures to neonicotinoids, however, can cause significant behavioral effects because these compounds alter the central role of nicotinic acetylcholine receptor in insect brains. In this study, we assessed the effects of three neonicotinoids that have a high toxicity to bees—imidacloprid, thiamethoxam, and clothianidin—on the behavioral immune system of honey bees. We used A. mellifera and the endoparasitic mite Acarapis woodi as a behavioral immune system model because A. mellifera can effectively remove the mite by autogrooming. Our results did not demonstrate an effect of neonicotinoid application on whether bees show autogrooming or on mite removal, but the time to initial autogrooming became shorter and the number of autogrooming attempts increased. As opposed to previous studies, our findings indicate that the honey bee response to parasitic mites becomes more sensitive after exposure to neonicotinoids.
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... These stressors impact honey bee health at the colony, individual bee, and cellular levels. Honey bees have evolved various strategies to mitigate these threats (97,(177)(178)(179). However, the impact of multiple, simultaneous biotic and abiotic stressors on honey bee health and longevity is currently not well understood, and difficult to assess at the colony level due to the large number of confounding variables (e.g., weather, colony management, pathogen exposure, co-infections). ...
Western honey bees (Apis mellifera) are ecologically, agriculturally, and economically important plant pollinators. High average annual losses of honey bee colonies in the US have been partially attributed to agrochemical exposure and virus infections. To examine the potential negative synergistic impacts of agrochemical exposure and virus infection, as well as the potential promise of phytochemicals to ameliorate the impact of pathogenic infections on honey bees, we infected bees with a panel of viruses (i.e., Flock House virus, deformed wing virus, or Sindbis virus) and exposed to one of three chemical compounds. Specifically, honey bees were fed sucrose syrup containing: (1) thyme oil, a phytochemical and putative immune stimulant, (2) fumagillin, a beekeeper applied fungicide, or (3) clothianidin, a grower-applied insecticide. We determined that virus abundance was lower in honey bees fed 0.16 ppb thyme oil augmented sucrose syrup, compared to bees fed sucrose syrup alone. Parallel analysis of honey bee gene expression revealed that honey bees fed thyme oil augmented sucrose syrup had higher expression of key RNAi genes (argonaute-2 and dicer-like), antimicrobial peptide expressing genes (abaecin and hymenoptaecin), and vitellogenin, a putative honey bee health and age indicator, compared to bees fed only sucrose syrup. Virus abundance was higher in bees fed fumagillin (25 ppm or 75 ppm) or 1 ppb clothianidin containing sucrose syrup relative to levels in bees fed only sucrose syrup. Whereas, honey bees fed 10 ppb clothianidin had lower virus levels, likely because consuming a near lethal dose of insecticide made them poor hosts for virus infection. The negative impact of fumagillin and clothianidin on honey bee health was indicated by the lower expression of argonaute-2, dicer-like, abaecin, and hymenoptaecin, and vitellogenin. Together, these results indicate that chemical stimulants and stressors impact the outcome of virus infection and immune gene expression in honey bees.
... Las abejas melíferas pueden proteger sus colonias de los ácaros varroa mediante comportamientos específicos, incluido el comportamiento de aseo, denominado en inglés "grooming" (Abou-Shaara, 2017) (Figura 5C). El alogrooming (aseo donde un animal usa sus extremidades, boca u otra parte de su cuerpo para limpiar a otro animal) y el autogrooming contribuyen a la resistencia a la varroa al eliminar los ácaros de las abejas adultas y también al dañar físicamente a los ácaros, evitando que busquen una nueva celda de cría para infestar (Pritchard, 2016). Las abejas pueden iniciar el acicalamiento a través de una "señal de invitación a acicalarse", una danza vibratoria de todo el cuerpo que dura varios segundos, que estimula a otras obreras a acicalar a la danzarina (Traynor et al., 2020). ...
La apicultura en el Perú ha crecido en los últimos años, influenciado principalmente por los cultivos como el palto (Persea americana Mill.), cuya polinización es asistida por los insectos. Sin embargo, cada año las colmenas de abejas enfrentan graves problemas que disminuyen su población, siendo uno de los causantes principales, el parasitismo por el ácaro Varroa destructor. Este ácaro invade celdas de larvas de abejas para reproducirse y evitan ser eliminadas de las mismas por las abejas obreras gracias a una estrategia kairomonal. Varios acaricidas son utilizados para controlar la invasión por varroa, sin embargo, existen reportes que la varroa estaría presentando resistencia a estos plaguicidas, ya sea por mutaciones en los canales de sodio dependientes de voltaje o acetilcolinesterasas, así como un incremento de la actividad desintoxicante. Como alternativa viable a la resistencia de la varroa hacia los acaricidas, se viene seleccionando colmenas con buen comportamiento higiénico, que, mediante acciones específicas como el aseo, minimizan la infestación por el ácaro. La presente revisión expone la información actual relacionada con la biología reproductiva y la alimentación de la varroa dentro de la colmena. Asimismo, describe los posibles mecanismos moleculares que explican la resistencia reportada hacia los acaricidas, proponiéndose la selección de colmenas de buen comportamiento higiénico como estrategia viable para el control de la varroa.
... Alrededor del mundo, el interés del hombre por las abejas comenzó con la caza y el robo de las colonias de abejas silvestres, que se encontraban en huecos de troncos o en hendiduras de las piedras (Alaux et al., 2010). La miel tenía valor no solo como producto comestible, sino por sus usos en la medicina popular (Berkelaar et al., 2001;Mitzman, 2012;Pritchard, 2016;Cheruiyot et al., 2018). Se ha observado y estudiado la abeja con el fin de aumentar la producción de la miel y facilitar la cosecha (Medina-Flores et al., 2014a;Kurze et al., 2016;Beaurepaire et al., 2017;Eliash & Mikheyev, 2020). ...
... Alrededor del mundo, el interés del hombre por las abejas comenzó con la caza y el robo de las colonias de abejas silvestres, que se encontraban en huecos de troncos o en hendiduras de las piedras (Alaux et al., 2010). La miel tenía valor no solo como producto comestible, sino por sus usos en la medicina popular (Berkelaar et al., 2001;Mitzman, 2012;Pritchard, 2016;Cheruiyot et al., 2018). Se ha observado y estudiado la abeja con el fin de aumentar la producción de la miel y facilitar la cosecha (Medina-Flores et al., 2014a;Kurze et al., 2016;Beaurepaire et al., 2017;Eliash & Mikheyev, 2020). ...
El ácaro Varroa destructor Delfinado & Baker, 1974 es la plaga más grave de las colonias de abejas en todo el mundo. Esta especie se ha convertido en una plaga importante para la apicultura mundial de la abeja europea (Apis mellifera Linnaeus, 1758), aunque el impacto de las infestaciones varía mucho entre los continentes. El objetivo de la investigación consistió en calcular el riesgo por varroosis tras la aplicación, individual y conjunta, de tres métodos: panal trampa, cambio de reina y buenas prácticas de manejo; así como determinar las pérdidas económicas en la provincia Villa Clara, Cuba. Se investigaron 467 apiarios, se muestrearon tres colmenas por apiario, para un tamaño de muestra de 3,257 individuos. Se realizó un análisis epidemiológico descriptivo de tipo retrospectivo, del comportamiento de la ocurrencia de varroosis. Se analizó una serie cronológica de tres años y se determinó la estacionalidad, canales de comportamiento habitual y tasa de infestación por varroosis. Se realizó un análisis de riesgo, aplicándose un estudio analítico observacional de tipo transversal, para determinar si había asociación entre los factores evaluados y la enfermedad; asimismo, se aplicó un análisis de proporción binomial y prueba de Chi cuadrado para la tasa de infestación entre municipios. La tasa de infestación fue de 3,1%. El canal enzoótico de la tasa de infestación por Varroa para el territorio, en el período de estudio fue de 2,2 a 4,6 y la tendencia es a la disminución. Se concluye que el empleo de estos tres métodos, individual y conjuntamente, constituye un factor de protección, ya que previenen significativamente la varroosis.
... For instance, structured interactions between honeybee members and their adaptive behaviors induced upon infection can reduce the impact of infectious diseases at the colony level. The mechanism is collectively known as 'social immunity' [19][20][21][22][23], including, for example, spatial separation of high-risk bees from low-risk bees [24,25], decrease in contacts with infected bees [26], cleaning the body surface of nest-mates to remove foreign material by allogrooming [27], self-removal of infected bees [28], removal of dead or infected brood [29][30][31], and removal of infected nest-mates [32,33]. ...
Honeybees (Apis mellifera) play a significant role in the pollination of various food crops and plants. In the past decades, honeybee management has been challenged with increased pathogen and environmental pressure associating with increased beekeeping costs, having a marked economic impact on the beekeeping industry. Pathogens have been identified as a contributing cause of colony losses. Evidence suggested a possible route of pathogen transmission among bees via oral-oral contacts through trophallaxis. Here we propose a model that describes the transmission of an infection within a colony when bee members engage in the trophallactic activity to distribute nectar. In addition, we examine two important features of social immunity, defined as collective disease defenses organized by honeybee society. First, our model considers the social segregation of worker bees. The segregation limits foragers, which are highly exposed to pathogens during foraging outside the nest, from interacting with bees residing in the inner parts of the nest. Second, our model includes a hygienic response, by which healthy nurse bees exterminate infected bees to mitigate horizontal transmission of the infection to other bee members. We propose that the social segregation forms the first line of defense in reducing the uptake of pathogens into the colony. If the first line of defense fails, the hygienic behavior provides a second mechanism in preventing disease spread. Our study identifies the rate of egg-laying as a critical factor in maintaining the colony’s health against an infection. We propose that winter conditions which cease or reduce the egg-laying activity combined with an infection in early spring can compromise the social immunity defenses and potentially cause colony losses.
... Allo-and auto-grooming contribute to Varroa resistance by both removing mites from adult bees and by physically damaging the mites, preventing them from seeking a new brood cell to infest (Pritchard, 2016). Honeybees can initiate allo-grooming via a "grooming invitation signal" a whole body vibrational dance lasting several seconds, which stimulates other workers to groom the dancer. ...
Background
Varroa mite, Varroa destructor Anderson and Trueman (Parasitiformes: Varroidae), is an ectoparasitic mite of the honey bee, Apis mellifera L. (Hymenoptera: Apidae), with a great economic importance. It is the major deadlock of apiculture development all over the world.
Results
This work aimed to assess the effect of bee house and dark bee house on numbers of Varroa mite on white card board sheets, worker broods, and alive bees during spring and autumn of 2018 and 2019. Two types of card board for sticking the fallen Varroa mite were evaluated through winter of 2019. Keeping honey bee hives in a dark room during March and September of 2018 and 2019 for a successive 3 days resulted in a great reduction in the number of Varroa inner bee hive, i.e., on the white card board sheets, area of broods, and alive honey bee. Highest number of fallen Varroa mite on the white card board sheets was obtained in the case of using the dark bee house during March and September in 2018 and 2019, followed by keeping in a normal bee house then those fallen in the case of the open apiary.
Conclusion
The dark bee house grooming behaviour increased through 3 days of dark. Environmental management of bee house and dark bee house can be promising in colony collapse disorder. Modified adhesive sheets were more efficient in this regard than the normal ones.
... The invasion of Varroa has become a challenge for the European bee, since it has not developed the natural defense mechanisms that well developed in the original host of the mite -the Asian bee Apis cerana. The resistance of the Asian bee to the mite is due to the fact that it has well-developed behavioral defense mechanisms and the mite parasitizes mainly on drone brood (Pritchard, 2016). The currently known methods of fighting V. destructor are based on the use of synthetic acaricides and biological control methods (Dietemann et al., 2012;Kamler et al., 2016;Plettner et al., 2017). ...
In the mid-20th century, the first case of infection of European bees Apis mellifera L. with the ectoparasite mite Varroa destructor was recorded. The original host of this mite is the Asian bee Apis cerana. The mite V. destructor was widespread throughout Europe, North and South America, and Australia remained the only continent free from this parasite. Without acaricide treatment any honeybee colony dies within 1–4 years. The use of synthetic acaricides has not justified itself – they make beekeeping products unsuitable and mites develop resistance to them, which forces the use of even greater concentrations that can be toxic to the bees. Therefore, the only safe measure to combat the mite is the use of biological control methods. One of these methods is the selection of bee colonies with natural mite resistance. In this article we summarize publications devoted to the search for genetic markers associated with resistance to V. destructor. The first part discusses the basic mechanisms of bee resistance (Varroa sensitive hygienic behavior and grooming) and methods for their assessment. The second part focuses on research aimed at searching for loci and candidate genes associated with resistance to varroosis by mapping quantitative traits loci and genome-wide association studies. The third part summarizes studies of the transcriptome profile of Varroa resistant bees. The last part discusses the most likely candidate genes – potential markers for breeding Varroa resistant bees. Resistance to the mite is manifested in a variety of phenotypes and is under polygenic control. The establishing of gene pathways involved in resistance to Varroa will help create a methodological basis for the selection of Varroa resistant honeybee colonies.
... According to Pritchard [47], grooming dance is categorized into two types: auto grooming/selfgrooming and inter-bee grooming/allogrooming. Early observations on the Eastern honeybee, A. cerana, recorded auto grooming, one-on-one, and social allogrooming, all of which resulted in death, visibly utilated varroa mites falling to the hive floor. ...
Honeybee foragers dance to communicate the quantity, quality, direction and spatial location of food and other resources to their nest mates. This remarkable communication system has long served as an important model system for studying mechanisms and evolution of this complex behavior. I provide a broad overview of the research done on dance communication, earlier theories and their controversies and solution. Specific issues concentrated in this review are as follows: (a) different type of dances (b) measurement of distance and direction (c) How bees perform dance in dark hive? Various experiments have thus confirmed that bees perform different types of dance depending upon their specific function. Thus, a detailed information about other type of dances is still lacking which if worked upon will help us in solving various queries and would help us in better understanding the significance of different types of dance performed by honeybees in and outside the hive.
Honey bees use grooming to defend against the devastating parasite Varroa destructor Anderson and Trueman. We observed the grooming responses of individual bees from colonies previously chosen for high- and low-grooming behavior using a combination of mite mortality and mite damage. Our aim was to gain insight into specific aspects of grooming behavior to compare if high-grooming bees could discriminate between a standardized stimulus (chalk dust) and a stimulus of live Varroa mites and if bees from high-grooming colonies had greater sensitivity across different body regions than bees from low-grooming colonies. We hypothesized that individuals from high-grooming colonies would be more sensitive to both stimuli than bees from low-grooming colonies across different body regions and that bees would have a greater response to Varroa than a standardized irritant (chalk dust). Individuals from high-grooming colonies responded with longer bouts of intense grooming when either stimulus was applied to the head or thorax, compared to sham-stimulated controls, while bees from low-grooming colonies showed no differences between stimulated and sham-stimulated bees. Further, high-grooming bees from colonies with high mite damage exhibited greater grooming to Varroa than high-grooming colonies with only moderate mite damage rates. This study provides new insights into Varroa-specific aspects of grooming, showing that although a standardized stimulus (chalk dust) may be used to assess general grooming ability in individual bee grooming assays, it does not capture the same range of responses as a stimulus of Varroa. Thus, continuing to use Varroa mites in grooming assays should help select colonies with more precise sensitivity to Varroa.
Bees are the most important insect pollinators of the crops humans grow, and Apis mellifera, the Western honey bee, is the most commonly managed species for this purpose. In addition to providing agricultural services, the complex biology of honey bees has been the subject of scientific study since the 18th century, and the intricate behaviors of honey bees and ants - fellow Hymenopterans - inspired much sociobiological inquest. Unfortunately, honey bees are constantly exposed to parasites, pathogens, and xenobiotics, all of which pose threats to their health. Despite our curiosity about and dependence on honey bees, defining the molecular mechanisms underlying their interactions with biotic and abiotic stressors has been challenging. The very aspects of their physiology and behavior that make them so important to agriculture also make them challenging to study, relative to canonical model organisms. But because we rely on A. mellifera so much for pollination, we must continue our efforts to understand what ails them. Here, we review major advancements in our knowledge of honey bee physiology, focussing on immunity and detoxification, and highlight some challenges that remain.
Varroa is a major world-wide pest to Western honey bees (Apis mellifera), causing huge ongoing losses of colonies every year. Conversely, the Eastern honey bee (Apis cerana) is less vulnerable to the mite having existed alongside it over a long evolutionary period. Research conducted during the 1980s and 1990s, shortly after Varroa had spread across the globe, concluded that the Eastern honey bee was less vulnerable because it displayed higher levels of grooming behaviour, brood removal behaviour and mite infertility than its Western counterpart. However, this review on these Varroa resistance traits in A. cerana indicates that there is surprisingly little evidence for these conclusions. This review explores this evidence and discusses the potential flaws in the studies and the gaps that still remain in our knowledge of Varroa resistance traits in A. cerana.
The selection of honeybee strains resistant to the ectoparasitic mite Varroa destructor is generally considered as one of the most sustainable ways of coping with this major bee parasite. Thus, breeding efforts increasingly focus on resistance parameters in addition to common beekeeping traits like honey yield and gentleness. In every breeding effort, the success strongly depends on the quantifiability and heritability of the traits accounted. To find the most suitable traits among the manifold variants to assess Varroa resistance, it is necessary to evaluate how easily a trait can be measured (i.e., testing effort) in relation to the underlying heritability (i.e., expected transfer to the following generation). Various possible selection traits are described as beneficial for colony survival in the presence of Varroa destructor and therefore are measured in breeding stocks around the globe. Two of them in particular, suppressed mite reproduction (SMR, sensu lato any reproductive failure of mother mites) and recapping of already sealed brood cells have recently gained increasing attention among the breeders because they closely resemble resistance mechanisms of some Varroa -surviving honeybee populations. However, it was still unknown whether the genetic background of the trait is sufficient for targeted selection. We therefore investigated the heritabilities and genetic correlations for SMR and REC, distinguishing between recapping of infested cells (RECinf) and all cells (RECall), on an extensive dataset of Buckfast and Carniolan stock in Germany. With an accessible h² of 0.18 and 0.44 for SMR and an accessible h² of 0.44 and 0.40 for RECinf, both traits turned out to be very promising for further selection in the Buckfast and Carnica breeding population, respectively.
The ectoparasite Varroa destructor is the greatest threat to managed honey bee (Apis mellifera) colonies globally. Despite significant efforts, novel treatments to control the mite and its vectored pathogens have shown limited efficacy, as the host remains naïve. A prospective solution lies in the development of Varroa-resistant honey bee stocks, but a paucity of rigorous selection data restricts widespread adoption. Here, we characterise the parasite and viral dynamics of a Varroa-resistant honey bee stock, designated ‘Pol-line’, using a large-scale longitudinal study. Results demonstrate markedly reduced Varroa levels in this stock, diminished titres of three major viruses (DWV-A, DWV-B, and CBPV), and a two-fold increase in survival. Levels of a fourth virus that is not associated with Varroa—BQCV—do not differ between stocks, supporting a disruption of the transmission pathway. Further, we show that when decoupled from the influence of Varroa levels, viral titres do not constitute strong independent predictors of colony mortality risk. These findings highlight the need for a reassessment of Varroa etiology, and suggest that derived stocks represent a tractable solution to the Varroa pandemic.
Varroa destructor is among the greatest biological threats to western honey bee (Apis mellifera L.) health worldwide. Beekeepers routinely use chemical treatments to control this parasite, though overuse and mismanagement of these treatments have led to widespread resistance in Varroa populations. Integrated Pest Management (IPM) is an ecologically based, sustainable approach to pest management that relies on a combination of control tactics that minimize environmental impacts. Herein, we provide an in-depth review of the components of IPM in a Varroa control context. These include determining economic thresholds for the mite, identification of and monitoring for Varroa, prevention strategies, and risk conscious treatments. Furthermore, we provide a detailed review of cultural, mechanical, biological, and chemical control strategies, both longstanding and emerging, used against Varroa globally. For each control type, we describe all available treatments, their efficacies against Varroa as described in the primary scientific literature, and the obstacles to their adoption. Unfortunately, reliable IPM protocols do not exist for Varroa due to the complex biology of the mite and strong reliance on chemical control by beekeepers. To encourage beekeeper adoption, a successful IPM approach to Varroa control in managed colonies must be an improvement over conventional control methods and include cost-effective treatments that can be employed readily by beekeepers. It is our intention to provide the most thorough review of Varroa control options available, ultimately framing our discussion within the context of IPM. We hope this article is a call-to-arms against the most damaging pest managed honey bee colonies face worldwide.
The honeybees (Apis mellifera) are the most important managed pollinator for sustainable agriculture and our ecosystem. However, the managed honeybee colonies in the United States experience 30-40% of losses annually. Among all the biotic stressors, the parasitic mite Varroa destructor is considered as one of the main pests for colony losses. The mite biting behavior as a Varroa tolerant or resistant trait has been selected in the State of Indiana for a decade. A survey of damaged mites from the bottom of a colony can be used as an extended phenotype of the mite biting behavior to evaluate a colony. On average 37% of mites sampled were damaged or mutilated from the breeding stocks of 59 colonies of mite biters of Indiana, which is significantly higher than 19% of damaged mites in commercial colonies from the Southern United States. No significant difference was detected between the damage of missing legs between breeding stocks and commercial colonies. In addition, the morphology of pollen forager worker mandibles were compared between two populations via X-ray micro-computed tomography using six parameters, and the difference was detected in one parameter. Our results showed the novel scientific evidence to explain the potential defensive mechanism against Varroa mites via mandibles providing a significant knowledge of a defensive behavioral trait for mite resistance.
Grooming behavior by honey bees is regarded as an important trait that contributes to the defense against the parasitic mite Varroa destructor. We carried out an assay to investigate how effective autogrooming by honey bees is in removing V. destructor mites. We compared the behavior of the Carniolan bee (Apis mellifera carnica), represented by two lines: Kortówka and Dobra; the Caucasian bee (Apis mellifera caucasica) of the Woźnica line; the black bee (Apis mellifera mellifera) of the Augustowska line; and the crossbreed of two subspecies: Apis mellifera capensis A. m. carnica. We found that most worker bees do not tolerate the mite on their bodies. The most intense reaction, manifested by strong motor activity, was observed in A. m. mellifera worker bees; as many as 98% of worker bees in this group made an attempt to remove mites. In the remaining groups, a response was observed in 86% for Caucasian bees to 89.3% for Carniolan bees, Dobra line. The attempts made by bees of different origins to remove mites differed in effectiveness, duration, and frequency. The highest percentage of removed parasites was noted in Caucasian bees (11%), and the lowest in Carniolan bees of the Kortówka line (1.5%). A. m. mellifera devoted the most time to the reaction to varroa on their body, i.e., an average of 64.7 s of 180 s of the experiment. In most trials, worker bees manifested at least three defensive reactions, and the highest number of such trials was observed in the black bee (117). We did not observe allogrooming in all bee groups or types. The results indicate that A. m. mellifera shows the strongest grooming behavior of all bees used in the experiment.
The relationship between food flow (honey and pollen) and the reproductive ability of the mite Varroa jacobsoni in brood cells of Africanized worker bees infested with a single female of this parasite, was determined by examining 17-18 day-old pupae. For 1050 varroa females infesting worker brood, a positive correlation was found between the amount of pollen available in the bee colonies and biological variables such as percent fertile females (females leaving descendants), number of deutonymphs (effective reproductive rate) and total number of descendants (total reproductive rate). In contrast, no correlation was detected between the amount of honey stored in the bee colonies and the three variables studied. An analysis of 612 fertile varroa females demonstrated a greater reproductive ability during the months of greater pollen availability.
Tliisstudy was uiidetlakcn to dctcniiiiic whcllícr Italiaii aiid AfricaJiizcdnieilifera workcre can ridÜicitísclvcs ofÜic initc Varroa Jacobsoni aftcr artificial infcstation with adull fciiialcs oftlús parasite.
There is a widespread belief that wild colonies of European honeybees have been eradicated in Europe and North America, killed by viruses spread by the introduced ectoparasitic mite, Varroa destructor. In reality, however, several populations of wild colonies of honeybees in Europe and North America are persisting despite exposure to Varroa. To help understand how this is happening, we tested whether the bees in one of these populations of wild colonies—those living in and around the Arnot Forest (NY, USA)—are genetically distinct from the bees in the nearest managed colonies. We found that the Arnot Forest honeybees are genetically distinct from the honeybees in the two apiaries within 6 km of the forest. Evidently, the population of Arnot Forest honeybees is not supported by a heavy influx of swarms from the nearest managed colonies, which implies that it is self-sustaining. These results suggest that if a closed population of honeybee colonies is allowed to live naturally, it will develop a balanced relationship with its agents of disease. Indeed, it is likely to become well adapted to its local environment as a whole. We suggest four ways to modify beekeeping practices to help honeybees live in greater health.
In recent years, the world's headlines have been full of stories of the mass death of honey bee colonies. Many possible explanations for these colony losses have been suggested, but scientific consensus suggests that there is no single cause, and that different interacting factors may be occurring in different regions. It is inescapable, however, that the parasitic mite Varroa destructor is present in all regions where recent colony losses have occurred, and that the mite is known to interact with other pests and diseases, principally viruses. Varroa is, however, not a new problem. It was first identified as a serious pest more than half a century ago, and chemical and other control methods have been available for decades. Why, therefore is it still a problem? In this book, an international team of bee scientists cover the varroa problem in depth by outlining our current knowledge about the biology of the mite and its interaction with viruses, discuss the problems of chemical resistance, control methods, whether chemical, ,biological, biotechnical, or by bee breeding, and suggest solutions to enable beekeepers to live with the mite in the 21st century.
The method of using Infra-red photography was found very useful for conducting long-term behavioristic studies of honey bees against Varroa. The photographs show the defensive ability of this species and solved the earlier suspicion of direct damage. In total 30% and 26.6% artificially infested cells were uncapped and removed in two experiments. The correlations between uncapping and removal, uncapping and grooming and removal and grooming behavior were found to be r=0.37, p=0.001; 0.03, p=0.5146 and 0.01, p=0.8179, respectively. Large significant differences between colonies w.r.t. uncapping, removing and grooming and very similar results of three colonies in two experiments indicates a genetic basis for these traits. The correlations between percentages of damaged mites under field conditions and test performance of their individuals with regard to uncapping, removing and grooming were estimated to be 0.63 (p=0.07, n=9), 0.43 (p=0.25, n=9) and 0.72 (p=0.11, n=6), respectively. The outstanding performance of a few individuals in expression of various traits indicates their usefulness in carrying out breeding programs for Varroa tolerance.
We investigated the relationships between the honey bee, Apis mellifera, and the parasitic mite Varroa jacobsoni in Mexico. In an 18-month survey of European honey bees (EHB) and Africanized honey bees (AHB), we showed that EHB were highly compatible with V. jacobsoni, while AHB were not as compatible. Furthermore, mite infertility ("parasite infectivity" factor), suspected to be the main factor of low AHB/V. jacobsoni compatibility in Brazil, was not observed in Mexico. The "intrinsic rate of natural increase" of mites did not differ significantly between host subspecies, indicating that the cause of low compatibility appears only at high parasite densities. The "carrying capacity" was twice as high in EHB as in AHB, indicating that the cause of low compatibility is possibly linked to honey bees' behavior. We hypothesize that the reason why V. jacobsoni is highly fertile on Mexican AHB (whereas it has low fertility on Brazilian AHB) may be that different strains of V. jacobsoni exist in the two countries.
Morphological features of nine samples of Apis nuluensis collected at the region of Sabah, Borneo, Malaysia in mountainous areas ranging from 1 524 to 3 400 m were analysed using 38 characteristics. Seventeen measurements of sizes, ten of coloration and hairyness, and II of wing venation angles were measured according to the methods of Ruttner et al (1978). The morphological position was evaluated within a frame containing other cavity-nesting Apis species drawn from the Oberursel data bank (Apis cerana from four Asian locations, Apis koschevnikovi, Apis nigrocincta and two equatorial Apis mellifera races). A nuluensis shows some extreme characteristics which separate ii from all other cavity-nesting bees, or all A cerana groups. In size measures it is closest to A nigrocincta from Sulawesi, while wing venation measures are close to the northern A cerana groups. Factor analysis showed A nuluensis to be clearly and significantly distinct from each of the other groups on at least two of the first three principal component axes. In discriminant analysis, all A nuluensis samples were assigned to their group with high probability. In particular, A nuluensis clearly differed from the sympatric groups, A cerana from Borneo and A koschevnikovi. In relation to A cerana in general, and to the sympatric A cerana from Borneo, this distinctness is less pronounced than that of A koschevnikovi, while the results from wing venation angles alone gave the opposite result.
La mortalite naturelle de l'acarien Varroa iacobsoni reflete la croissance de la population et le potentiel reproducteur du varroa et fournit des informations concernant les mecanismes de defense active des abeilles. Wallner (1989, 1990a,b, 1991, 1992) a ete le premier a postuler l'existence de mecanismes de defense active apres avoir observe des varroas qui presentaient des pattes et la cuticule de l'idiosome endommagees. Ces faits ont ete confirmes par Ruttner (1991) et Ruttner et Hanel (1992)
Division of labour among nestmate workers is central to the colonial organization and ecological success of the eusocial Hymenoptera (ants, bees and wasps)1. Workers characteristically divide labour through (1) ontogenetic changes in individual behaviour2,3 and (2) inter-individual variation in behavioural repertoire3,4. On the basis of current evidence, optimization models of colony demography3,5,6 assume that variation among nestmates in behavioural repertoire arises solely through variation in environmental conditions, such as larval nutrition (inducing size-mediated behavioural differences in many ants)3,4,7 and adult experience (effecting behavioural differences among morphologically similar nestmates)8. A possible genetic component to division of labour, however, has received little study9. Yet, the degree of genetic heterogeneity among workers within Hymenopteran colonies is often extremely high10, a consequence of multiple mating by the queen (polyandry11,12) and/or the presence of multiple laying t (J B ) queens (polygyny13). Here we report evidence of genetically based variation in task performance among nestmate workers in the polyandrous honey bee Apis mellifera L. Such variation may be an important component to division of labour within genetically heterogeneous colonies.
This study uses sibling analysis to measure the heritability in honey bees, Apis mellifera L., of characteristics that have been associated with resistance to the mite, Varroa jacobsoni Oudemans. Twenty-eight uniform colonies of bees were established on 13 May in Baton Rouge, LA, each with 1 kg of mite-infested bees and a queen. The 28 unrelated queens in these colonies were divided into 7 groups of 4 based on the insemination of 4 queens with the same mixture of semen from 1 of 7 sire colonies. After worker progeny from these queens had replaced the initial bee populations, a colony was related as a full sister to the other 3 colonies in its sire group and unrelated to the other 24 colonies. Heritability (h 2) was 1.24 for proportion of mites in brood, 0.65 for hygienic behavior, 0.89 for the duration of the capped period, 0.46 for suppression of mite reproduction, and 0.00 for physical damage to mites (measured by the presence of physically broken or dented mites on the bottom board). These results suggest that it should be possible to enhance the expression of 4 of these 5 characteristics with selective breeding of bees, thus reinforcing confidence in our ability to breed honey bees for resistance to V. jacobsoni.
This study assessed how variation in temperature and humidity affect the costs and benefits of grooming as a defense against Varroa destructor Anderson and Trueman, 2000 in high-grooming and low-grooming groups of honey bee (Apis mellifera L., 1758) workers. Grooming was quantified as the proportion of mites falling to the bottom of cages containing worker bees or to the bottom of colonies of bees during winter. Cages of 100 mite-infested bees from each line of workers were assigned to environments with three treatment combinations of temperature (10, 25, and 34C) and humidity (low, medium, and high), and bee and mite mortality rates were quantified. The results showed relative effectiveness of high- and low-grooming groups being affected by the environment. Differences in grooming between lines were greatest at 25C and were slightly higher under conditions of low humidity than at higher levels. Mite mortality rates were greater in high-grooming groups of caged bees than in low-grooming bees held at 25 and 34C but were similar at 10C. During winter, colonies with high-grooming bees had higher daily mite mortality rates than unselected colonies. Bee mortality rates were greater in high-grooming lines than in low-grooming lines under low temperatures, indicating that there may be a biological cost associated with grooming behaviour at low temperature.
mdash; In a naturally infested colony a strong correlation between levels of falling mites and the emergence of honeybee brood was found. When comparing the number of mites falling between emerging worker and drone brood with known infestation levels, the mite fall was 2-3 times higher from worker than from drone cells. It was estimated that around half of the falling mites originate from mites that died within the sealed cell with the other half dying shortly after bee emergence. About 50% of the fallen mites were still alive and found to be able to reproduce when artificially introduced into sealed brood cells. The implications of mite mortality associated with brood emergence on the mite population dynamics and of using numbers of falling mites as a monitoring tool are discussed.
Due to the low fecundity of Varroa jacobsoni, it: is presently not possible to explain satisfactorily the observed rapid build up of mite populations in Apis mellifera colonies. The number of reproductive cycles, i.e. the number of times a mite enters brood cells to reproduce, has been suggested to be the key to this problem. Despite several studies on this aspect, large discrepancies in the published data remain. This paper describes a new experimental method for studying this aspect of the mites' biology in order to resolve this question. Colonies containing only worker bee brood were manipulated so they had discrete brood cycles. Colonies were kept in a mite-free area and infested with a known number of mites at the start of the study. To estimate the average number of reproductive cycles performed, the observed growth in the mite populations was compared with the theoretical growth of mite populations which performed different numbers of reproductive cycles, but with conditions otherwise similar to those observed in the study colonies. The level of mite drop was used as an indicator of the mite population. The average potential number of reproductive cycles required to explain the observed mite population growth was between two and three.
The distribution of Varroa jacobsoni on clustered, overwintering workers of Apis mellifera was investigated. The majority of mites were found between the 3rd and 4th ventro-lateral tergites of the abdomen with a significant preference for the left side of the host. This position would enable the mites to place their mouthparts in close proximity to the central portion of the bees' ventriculus. This may allow the mites access to nutrients at higher concentrations than would occur elsewhere in the haemolymph. At the start of winter, most infested bees carried only a single mite but towards the end increasing numbers of bees carried 2 or more mites. There was also an increase in the mite: bee ratio and more mobile mites (i.e. those moving about on the bees) were recorded. These results suggest that the mites suffer a lower overwinter mortality than the bees and are capable of transferring to a new host either before the original host dies or before it falls to the floor of the hive. This will have consequences for the transfer of diseases by Varroa within the hive.
The UK is probably unique in that much information concerning the natural incidence of bee virus diseases in apparently healthy honey bee colonies exists for the period before the arrival of Varroa destructor in 1992 (Bailey et al., 1981). Fig. 1 represents data from 73 individual honey bee colonies infested with V. destructor maintained in Devon or Hertfordshire, UK, between 1993 and 1997 as part of studies investigating the interaction between honey bees, V. destructor and viruses. All colonies were observed for at least 12 months, which included an overwintering period, and were not treated with an acaricide. Natural mite mortality was assessed on a monthly basis using open mesh floors (Carreck, 1994), and the maximum mite population estimated by use of a computer model (Martin, 1998). Samples of dead workers were collected monthly from the majority of the study colonies (others were sampled less frequently) and were tested serologically for the presence of: acute bee paralysis virus; bee virus X; bee virus Y; chronic bee paralysis virus (CBPV); cloudy wing virus (CWV); deformed wing virus (DWV); filamentous virus, Kashmir bee virus (KBV); sacbrood virus (SBV); and slow paralysis virus (SPV), as described previously (Bailey and Ball, 1991). The serological methods have since been largely superseded by molecular techniques such as PCR, but their relative insensitivity actually makes them particularly suited to this type of study, since only infections likely to have caused the mortality of the individual bee would have produced a positive result. Whilst of these 10 viruses, all but KBV were sporadically detected in our samples, only three virus infections, CWV, SPV and DWV were found to be more prevalent in colonies infested with V. destructor in our study compared to previous long term observations (Bailey et al., 1981; Bailey and Ball, unpublished observations) of uninfested colonies in Britain prior to the arrival of the mite. Of these viruses, SPV and DWV are clearly associated with the loss of infested colonies (Carreck et al., 2005; Martin, 2001), but any association between CWV and losses associated with V. destructor remains circumstantial (Carreck et al., 2010). The results showed that colonies in which none of these three key viruses (CWV, SPV, DWV) were detected could survive from one season to the next, even when mite populations exceeded several thousand (Fig. 1). Total estimated mite populations in this group of colonies varied from 60 to 15,000. In contrast, mite populations in the group of colonies that also survived but in which one or more of these three viruses was detected, were uniformly small and did not exceed 2000 mites (Fig. 1). By far the largest group of colonies, however, failed to survive from one season to the next. One or more of the three viruses were detected in the dead adult bees from all of these colonies, particularly DWV and SPV; 14 colonies had one virus, 34 had two, and eight had all three viruses. There was a large variation in the size of the mite population, but almost all colonies had mite populations that exceeded 2000 (Fig. 1). Since the different viruses have different natural histories and epidemiologies, it would seem reasonable that each virus should required different numbers of mites to kill colonies. Both modelling (Martin, 2001) and field observations (Ball, Carreck and Martin, unpublished observations) suggest, perhaps counter intuitively, that a virulent virus such as SPV requires a larger mite population to kill a honey bee colony than a virus such as DWV, which is not rapidly fatal (Sumpter and Martin, 2004). In practice however, few of the colonies studied contained a single virus; most had two, and some had three viruses present. The virus free colonies in our study all occurred within the first few years of V. destructor being found in the UK in 1992, and subsequent studies showed that after a few years, the majority of UK colonies were infected with DWV (Carreck et al., 1999; Ball, 2001). Furthermore, invasion of mites from other colonies is not predictable, so the two colonies in Fig. 1 which died with maximum mite populations of only 984 and 1680, were both in apiaries with other heavily infested colonies which had died. Entry of many mites carrying a virus into relatively mite free colonies may cause their death with fewer mites present than might be predicted from models (e.g. Martin, 2001) which rely on the natural development of the mite population. The results from this study emphasise the continuing need for beekeepers to maintain mite populations at a negligible level by appropriate treatment.
The rich variety of native honeybee subspecies and ecotypes in Europe offers a good genetic resource for selection towards Varroa resistance. There are some examples of mite resistance that have de-veloped as a consequence of natural selection in wild and managed European populations. However, most colonies are influenced by selective breeding and are intensively managed, including the regular use of miti-cides. We describe all characters used in European breeding programs to test for Varroa resistance. Some of them (e.g., mite population growth, hygienic behavior) have been implemented in large-scale selection pro-grams and significant selection effects have been achieved. Survival tests of pre-selected breeder colonies and drone selection under infestation pressure are new attempts to strengthen effects of natural selection within selective breeding programs. Some perspectives for future breeding activities are discussed.
Keywordschewed mites–
Varroa destructor
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Apis mellifera
The objective of this study was to demonstrate genotypic variability and analyze the relationships between the infestation levels of the parasitic mite Varroa destructor in honey bee (Apis mellifera) colonies, the rate of damage of fallen mites, and the intensity with which bees of different genotypes groom themselves to remove mites from their bodies. Sets of paired genotypes that are presumably susceptible and resistant to the varroa mite were compared at the colony level for number of mites falling on sticky papers and for proportion of damaged mites. They were also compared at the individual level for intensity of grooming and mite removal success. Bees from the "resistant" colonies had lower mite population rates (up to 15 fold) and higher percentages of damaged mites (up to 9 fold) than bees from the "susceptible" genotypes. At the individual level, bees from the "resistant" genotypes performed significantly more instances of intense grooming (up to 4 fold), and a significantly higher number of mites were dislodged from the bees' bodies by intense grooming than by light grooming (up to 7 fold) in all genotypes. The odds of mite removal were high and significant for all "resistant" genotypes when compared with the "susceptible" genotypes. The results of this study strongly suggest that grooming behavior and the intensity with which bees perform it, is an important component in the resistance of some honey bee genotypes to the growth of varroa mite populations. The implications of these results are discussed.
The ectoparasitic mite Varroa jacobsoni Oud. presently poses one of the most serious problems faced by keepers of honeybees Apis mellifera L. To help understand why the mite has become such a serious problem a population dynamics model using recently published data has been constructed. The simulation model has been built by linking together various aspects of the mites’ biology using computer software (ModelMaker®) in such a way that an initial population of mites can change daily over any period. The model predicts a yearly 12-fold increase in mite numbers or an intrinsic rate of daily increase of 0.021 during the presence of bee brood. This corresponds well with field data. Values derived from the model for behaviours such as drone preference (5.5–12 times) and phoretic period (4–11 days) are similar to those actually observed. Therefore, the model can be used to predict the number of mites within any colony and their subsequent development over any period. Since the daily development of both the live population and numbers of dead mites are predicted by the model it can be used as a mite population monitoring tool. The model predicts that the ratio of live to dead mites will change dramatically between periods when bee brood is present or absent. However, since the ratios were shown to be stable within the periods, the mite population can be estimated throughout the year by multiplying the daily mite drop by ≈250–500 or 20–40 when brood is absent or present, respectively. This will allow beekeepers to optimise their mite control strategy. The model also reveals the complex pattern in infestation levels that occurred throughout the year which was caused by the interactions between the bee and mite breeding cycles and will allow the role of bee viruses in the collapse of the colony to be studied in much greater detail.
Breeding for resistance to Varroa destructor in North America provides the long-term solution to the economic troubles the mite brings. This review reports the development of two breeding successes that have produced honey bees of commercial quality that do not require pesticide treatment to control Varroa, highlights other traits that could be combined to increase resistance and examines the potential uses of marker-assisted selection (MAS) for breeding for Varroa resistance. Breeding work continues with these stocks to enhance their commercial utility. This work requires knowledge of the mechanisms of resistance that can be further developed or improved in selected stocks and studied with molecular techniques as a prelude to MAS.
We observed social grooming behavior in the Carniolan bee, Apis mellifera carnica. Bouts of grooming lasted up to 45 s, and were directed to the wing axis (44.6%), the petiolus (18%) and the sternite regions of abdomen (2.8%) of the receiving bee (41 bees). During grooming, the receiving bees held their wings perpendicular to the body axis. Groomer bees most often cleaned those body parts which could not be reached during self-cleaning by receiving bees. During 18% of the grooming time, groomer bees cleaned their own mouth parts and antennae. The grooming behavior removed dust and pollen from the wing bases and petiolus and realigned the body hairs. No attempts to remove Varroa mites were observed during self-cleaning or social grooming behavior.
A one year study was conducted to evaluate the population growth of three kinds of honey bee colonies and Varroa destructor mites in Mexico, and to estimate the relative contributions of three resistance mechanisms of the bees: hygienic behavior, grooming behavior, and reproductive ability of the parasite. Very significant changes over the year were observed in the number of mated female offspring produced per mother mite (Wr), mite fertility and mutilation of V. destructor. These changes were correlated to the total number of mites per colony. A factorial analysis showed that two mechanisms explained the variation in the amount of mites per colony: Wr (r2 = 0.73) and proportion of mutilated mites (r2 = 0.51). A multi-factorial model including these two mechanisms was significant (r2 = 0.97). The mite fecundity and the hygienic behavior could not explain the population changes of the mite, and the different kinds of bees showed no differences in the expression of the resistance mechanisms.
This study was conducted to determine the existence of phenotypic and genotypic variation in the ability of honey bee colonies to restrain the population growth of the mite Varroa destructor Anderson and Trueman, and to asses the relative effect of four characteristics that may confer tolerance to honey bees toward the mite. Fifty-eight colonies infested with an equal number of mites were sampled monthly during six months to determine their levels of infestation on adult bees and in worker brood. At the end of this period, 16 colonies were selected to study the effect of grooming behavior, hygienic behavior, brood attractiveness, and host-induced non-reproduction. The infestation-levels in adult bees varied significantly between colonies (range: 6.6-44.7% ), but no differences were found in the brood infestation levels. The variation between colonies was partially genetic in origin. Grooming behavior explained most of the variation (). Negative correlations were found between the mite population growth and both the total number of mites and the number of injured mites collected from the bottom-boards ( and , respectively). Differences were found for hygienic behavior but the effect of this mechanism was not clear. No differences were found among colonies for brood attractiveness, or for the effect of the brood on the mite's reproduction.
The proportion of damaged mites in natural mite fall is considered a useful criterion in the breeding of Varroa-tolerant bees. This study, observing about 16 000 mites, tested several modifications of recording this trait. The effects of a predator-proof hive, coating the bottom boards with grease, and the time intervals between recordings were examined. Studies were also conducted to determine the extent of damage by bees to already dead mites, and the influence of storage conditions of the dead mites. The type and the amount of damage to immature and adult mites differed considerably. Protection of the bottom board against predators significantly reduced the extent of damaged mites. Mites should not remain on the bottom board for longer than 2 days, because the extent of damage increases significantly after that, especially when wax moth larvae are present. Conditions under which the mites are stored significantly affect the extent of the damage. Quantity and quality of damage in natural mortality indicate that a proportion of mites died due to specific defensive behaviour of the bees. © Inra/DIB/AGIB/Elsevier, Paris
Two behaviors of honey bees, hygienic behavior and grooming, are mechanisms of defense against brood diseases and parasitic mites. Studies have shown that Apis mellifera colonies remove worker brood infested with Varroa jacobsoni mites from the nest (hygienic behavior), and groom the mites off other adult bees, but to a limited extent compared to the original host of V. jacobsoni, A. cerana. Research is reviewed on hygienic and grooming behaviors with respect to their potential as mechanisms of resistance to V. jacobsoni. Studies related to hygienic behavior include the removal of experimentally infested and naturally infested brood, measurements of heritability, the uncapping and recapping of cells containing infested pupae, and the detection of infested brood. Studies on grooming include the process by which a groomer detects and damages a mite found on itself or on another adult bee, how the behavior is quantified, and problems with these methods of quantification. Finally, unresolved questions concerning grooming and the effects of hygienic and non-hygienic behaviors on limiting the population growth of V. jacobsoni are discussed. © Inra/DIB/AGIB/Elsevier, Paris
Suppressed Mite Reproduction (SMR) is a trait of honey bees that provides resistance to Varroa destructor. The mechanism of resistance in SMR bees is the removal of infested pupae from capped brood, so a better name is VSH bees (acronym for Varroa Sensitive Hygiene). This study compared the removal of infested brood by VSH and control bees to determine whether VSH bees removed infested pupae of different ages at similar rates. A pair of infested combs containing all stages of pupae were transferred into each host colony (six VSH and six control colonies) for 40 hours. VSH bees removed significantly more (55%) infested cells (singly and multiply infested), than controls (13%). They removed significantly more (66%) singly infested pupae aged from one to five days post capping (cohort A) than did controls (16%). The two types did not differ in the removal of singly infested pupae aged five to 10 days post capping (cohort B) (5–22%). Many pupae were found in uncapped cells at the end of the test, and most of the uncapped pupae were infested with mites. None of the uncapped cells contained prepupae, the development stage occurring during the first three days post capping. Thus, removal of infested pupae may be triggered by stimuli in cells with pupae aged 3–5 days post capping.La supresión de la reproducción del ácaro (SMR) es un rasgo de las abejas que les proporciona resistencia ante Varroa destructor. El mecanismo de resistencia en abejas SMR consiste en retirar las pupas infestadas de la cría operculada, por lo que abejas VSH (siglas de higiene sensitiva a la varroa) es un término más adecuado. Este estudio comparó la retirada de cría infestada por abejas VSH y abejas control para determinar si las abejas VSH quitaban pupas infestadas de diferentes edades en proporciones similares. Un par de cuadros infestados que contenían pupas de todas las etapas fueron introducidos en colmenas anfitrionas (seis VSH y seis colmenas control) durante 40 horas. Las abejas VSH retiraron significativamente más pupas de celdas infestadas (55%) (única ó múltiple infestación) que las colmenas control (13%). Las abejas VSH eliminaron considerablemente más (66%) pupas maduras de infestación única de uno a cinco días tras la operculación (cohorte A) que las colmenas control (16%). Los dos tipos de abejas no presentaron diferencias en la retirada de pupas maduras entre los cinco y diez días tras la operculación (cohorte B) (5–22%). Muchas pupas fueron encontradas en celdas desoperculadas al final de la prueba, y la mayor parte de las pupas desoperculadas estaban infestadas por el ácaro. Ninguna de las celdas desoperculadas contuvo pre-pupas, etapa del desarrollo que trascurre durante los primeros tres días tras la operculación. Por lo tanto, la retirada de pupas infestadas se puede activar mediante el estímulo en celdas con pupas de entre 3–5 días tras la operculación.
The ectoparasitic mite Varroa destructor is one of the main plagues of honey bees Apis mellifera. Grooming behavior is a resistance mechanism through which parasitized bees can dislodge mites by themselves (autogrooming) or by the action of other bees (allogrooming). The objective of this study was to evaluate grooming behavior in Italian (A. m. ligustica) and Africanized (hybrids of A. m. scutellata) bees at the individual, group, and colony levels. Firstly, five behaviors were recorded observing bees individually placed on a Petri dish and after placing a mite on their thorax. Secondly, 30 bees of each colony were placed in a Petri dish along with 20 mites and 24 h later fallen mites were counted. Lastly, the proportion of injured mites collected in the hive floor was determined. At the individual level, Africanized bees showed a higher total number of reaction behaviors to V. destructor than did Italian bees (U = 182.5; p = 0.02). Groups of Italian bees could dislodge 60.8 ± 20.0% of mites and Africanized bees dislodged 65.9 ± 15.6% of mites, without showing significant differences (t = 0.735; p = 0.47). Colonies of Africanized bees showed a higher proportion of injured mites (29.0 ± 8.6%) than colonies of Italian bees did (17.7 ± 9.8%) (t = 2.92; p = 0.009). Africanized bees are characterized by presenting higher resistance to V. destructor than European bees. This study shows that such difference can be, partly due to grooming behavior. The importance of auto and allogrooming regarding resistance to V. destructor is discussed.
It has now been nearly ten years since we started a project on the selection for varroa tolerance at the institute in Kirchhain, Germany. From the very beginning, the project was designed in adaptation to the existing breeding structure in oar country.
The kinds of damage found on Varroa jacobsoni located in worker brood, on adult honey bees, on the bottom board (floorboard) traps and in Gary traps, were investigated in Apis mellifera ligustica colonies. Light-coloured adult mites with damage to the cuticle of the idiosoma were found in the brood cells: 2.8% from undamaged mother mites and 17.9% from damaged mother mites. No mites with leg damage were found on adult honey bees. Mites in Gary traps showed more damage (45.9%) than those collected on the bottom boards (26.1%).
The removal and grooming behaviour of Apis mellifera intermissa against Varroa jacobsoni was investigated in Tunisia. Workers in 15 test colonies detected and removed up to 75% of artificially infested brood and removed up to 97%-99% of freeze-killed brood in each of two trials. Likewise, A. m. intermissa actively groomed off V. jacobsoni, as shown by a great number of injured mites dropping from naturally infested colonies. Both grooming and removal activities of A. m. intermissa provide evidence for active mechanisms of resistance against V. jacobsoni.
A behavioral and physiological resistance mechanism of the Asian honey bee (Apis cerana) to an ectoparasitic mite, Varroa jacobsoni, which causes severe damage to the European honey bee (Apis mellifera) in the beekeeping industry worldwide, is reported here for the first time. Parasitism by the mite induced Asian worker bees to perform a series of cleaning behaviors that effectively removed the mites from the bodies of the adult host bees. The mites were subsequently killed and removed from the bee hives in a few seconds to a few minutes. The grooming behavior consists of self-cleaning, grooming dance, nestmate cleaning, and group cleaning. Worker bees can also rapidly and effectively remove the mites from the brood. The European bee showed cleaning behavior at low frequency and generally failed to remove the mites from both the adult bees and the brood.
Adult females (n = 518) of Varroa destructor from Apis mellifera prepupae were examined by scanning electron microscopy without prior fluid fixation, dehydration and critical-point drying.
Fifty-five (10.6%) mites had one (8.1%) or two (2.5%) diagonal dimples positioned symmetrically on the idiosoma’s dorsum.
Where one such regular dorsal dimple existed per mite body, it occurred on the left or right side, equally. Mites with at
least one regular dorsal dimple were 3.4% longer, but neither idiosomal width nor elliptical area differed significantly from
mites lacking dimples. Dimple length was normally distributed in the population, and averaged 462 ± 9.2 μm (s.e.; n = 68 dimples).
Internally, each regular dorsal dimple aligns with a series of obliquely-situated, dorso-ventral muscles in the opisthosoma.
It is concluded that regular dorsal dimples are faults originating during mite ontogeny and should be considered separately
from damage to Varroa destructor inflicted by honeybees or predatory arthropods.
The research on bee and mite biology over the past 20 years has uncovered numerous details of the A. cei-ann-li. jacobsoni co-adaptation which are systematically summarized here. A. cerana acquired a high degree of hygienic efficiency with a differentiated set of behavioural traits that we describe in this review in a broad sense to include grooming of mites by adult bees, uncapping and removal of infested brood and entombing of infested brood. Approximately 20 % of the reproducing mite population can be eliminated by entombing of lethally parasitized drone pupae. In their equally effective infesting behaviour the parasites explore the most suitable adult and larval host individuals for safe phoretic positions, the favourable caste and suitable age. A. cerana compel V. jacobsoni to reproduce exclusively on drone brood hosts. This limited reproduction, in combination with characteristics of the population dynamics of the host, are key factors which limit mite populations to tolerable levels. (C) Inra/DIB/AGIB/Elsevier, Paris.
This study examines changes in reproduction and mortality of Varroa destructor when queens from stocks of honey bees (Apis mellifera L.) that differ in susceptibility to the mites were exchanged between colonies. Queens were selected for suppression of mite reproduction (SMRD). In two experiments uniform colonies of bees were established; half the colonies were given queens selected for SMRD, and half were given unselected queens. Queens were exchanged after 7 (experiment 1) and 13 weeks (experiment 2). The percentage of mites that had no progeny was determined for each colony at 5 times (2 before and 3 after exchanging queens). Mites that had no progeny included live and dead mites. Results showed (1) that reproduction of mites is suppressed by adding a queen selected for SMRD, and (2) that a mite population recovers its reproduction when a SMRD queen is replaced by an unselected queen. Selection of the SMRD trait can be reduced to counting only live mites that laid no eggs and dead mites.
The aim of this research was to investigate whether or not sugar dusting can stimulate the grooming behaviour in Apis mellifera L. (Hymenoptera: Apidae), an important defensive mechanism against Varroa destructor Anderson & Trueman (Acari: Varroidae), and to assess the most effective dose and frequency of treatment. The criterion for evaluation of grooming potential was the percentage of damaged mites (PDM) among the total number collected on the bottom boards of the hives. In each sugar‐treated group PDM was significantly higher in comparison both with the negative control (no treatment) and with the values preceding the treatment. The results point to a stimulating effect of sugar on the grooming behaviour at all doses and frequencies tested. Treatment frequency influenced the stimulating effect of sugar: treatments at 3‐ and 7‐day intervals with 30 and 40 g resulted in significantly higher PDMs than the least frequent treatment (every 14 days); dusting with 20 g influenced PDM only when repeated at 3‐day intervals. Because treatments at 3‐day intervals are time‐consuming, those with 40 or 30 g repeated every 7 days may be recommended. In the positive control (hives treated with amitraz), average PDM was significantly lower than in the negative control and all sugar‐treated groups. Possible causes of the stimulating effect of sugar dusting on bee grooming behaviour are discussed.
OneApis mellifera and oneApis cerana observation hive were used to test the response to individually introducedVarroa jacobsoni mites. Within 60s, 88.6% of the involved cerana worker bees (n=44) showed auto-grooming behaviour. Within 5 min, allo-grooming behaviour, involving up to four nestmates, was observed in 33.3% of the infested bees. Successful mite removal was observed in 75% of the not-prematurely discontinued observations (n=36); 32% of the mites removed were caught with the mandibles.For mellifera auto-grooming behaviour was observed in most cases but delayed in comparison to cerana, and allo-grooming behaviour was rarely observed. Within 5 min, 48% of the mites in notprematurely discontinued observations (n=25) were removed, but none of the mites was caught with the mandibles.ForApis dorsata auto-grooming behaviour in response to the infestation withTropilaelaps clareae andVarroa mites is reported for the first time.Varroa was removed at a higher rate thanTropilaelaps. The higher survival chance ofTropilaelaps seems to be due to differences in mite behaviour and the preference for certain parts of the bee-body.
Honey bees, Apis mellifera L., are polyandrous and several males simultaneously father offspring within a single colony. The relatedness of female colony members therefore varies with their paternity: workers encounter both patrilineal full sister (r¯=0·75) and non-patrilineal half-sister (r¯=0·25) nestmates. The impact of this intra-colony genetic variation on social grooming and trophallaxis (liquid food exchange) among workers in colonies consisting of two phenotypically-distinct worker patrilines was examined. Workers in these colonies groomed and fed a disproportionately large number of full sisters despite a tendency to encounter a disproportionately large number of half-sisters. Thus, workers actively discriminated between full and half-sisters. This patrilineal discrimination occurred both in colonies with laying queens and in a queenless colony rearing replacement queens. These results suggest that intracolony genetic variation may have a major effect on colony social organization.
We evaluated the difference in tracheal mite infestation between nestmate honey bees that were actively autogrooming and those that were not. Bees seen to be actively grooming themselves in an observation hive were immediately removed through a door, narcotized and searched for mites. Nearby bees that were not grooming also were taken and examined. A strong association was found between the act of autogrooming and the presence of tracheal mites, with mites found at a 4-fold greater frequency on the thoraxes of grooming bees (36/50 with mites) than on non-grooming bees. Mites were found most commonly on the metatergum and the propodeum, and near the wing bases.
Varroa mite mortality and mite damage in colonies of Apis cerana cerana Fabr and Apis mellifera ligustica Spin, where mites were added to observation hive bees and to full-sized colonies of both bee species, were studied. The results show grooming behavior in A cerana but the results also indicate that this behavior may be less effective than previously recorded. In A mellifera colonies, phoretic mites were also removed by the bees but less effectively than in A cerana colonies. The proportion of experimentally-added live mites in the debris that were visibly damaged in colonies of A cerana was 30% (n = 115). From A mellifera colonies, 12.5% of the introduced mites had visible injuries caused by the bees (n = 65). The mites recovered from both bee species showed reduced survival rate on bee pupae compared to control mites. Compared to A mellifera, A cerana is more effective in both removing mites and causing mite damage. However, in A mellifera phoretic mites are also removed by the bees, and some of them are injured. Since no reproduction of Varroa mites occurs in worker brood in A cerana, extremely effective grooming behavior may not be needed to explain the tolerance of A cerana to Varroa mite infestations. The results presented demonstrate that more research is needed to evaluate the importance of grooming behavior to Varroa mite tolerance in both A cerana and A mellifera.