Article

Grooming by honey bees as a component of varroa resistant behavior

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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.

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... 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). ...
Article
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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.
... Grooming behavior and Varroa sensitive hygiene are two specific traits in honey bee families that may significantly reduce the infection by Varroa mite (Büchler et al., [7]). Grooming behavior which involves removal and destruction of adult mites on the external surfaces of the adult bees may be exhibited as autogrooming or allogrooming (Ruttner and Hänel,[8]; reviewed by Pritchard, [9]). It may result in death of the mite or its relocation (Büchler et al., [7]). ...
... Varroa mite count showed that control hive was less burdened with the mite from the beginning. After the insertion of CheckMite, a peak in mite count (9) was observed in the same day; count dropped back to daily count between 0 and 1 (data not shown). Because of such a substantial increase in the number of grooming dances after the insertion of cHBA in comparison to control group we made visual inspection of the fallen mites searching for signs of damage on mites' body. ...
... On the other hand, it was noted that in certain colonies Varroa induces greater rate of antennation and aggressive behavior of individual workers (Martin et al., [49]). Besides, it seems that various species of genus Apis and also various subspecies of A. mellifera show different responses to encountered Varroa (Pritchard, [9]). Aumeier, ( [50]) observed that damages on Varroa are not necessarily a consequence of allogrooming. ...
Article
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Honey bees (Apis mellifera) are important component of global food production. Parasitic mite Varroa destructor (Varroa) poses serious threat to health of honey bee colonies worldwide. In past years there have been increased need for natural products that suppress the mite in honey bee population without negative impacts on honey bees and their products in order to substitute more toxic conventionally used acaricides. Hops beta acids (HBA) were suggested to have potential in suppression of Varroa. We tested HBA toxicity on honey bees in different concentrations and whether they have any influence on the grooming behavior of worker bees. For the purpose of the study toxicological tests were made on caged bees. HBA of different concentrations were tested per os (0.05%, 0.25% HBA) and topically (0.1%, 0.25%, 1% and 2% HBA, application of 0.5 µl of each directly on the thorax of a bee). Additionally every hour three bees from each tested group were sacrificed for histological examination of intestines. Two observation hives to monitor the effect of HBA on behavior of worker bees were setup. The allogrooming dances were video-documented before, in-between, and after the insertion of cellulose carrier containing 16% HBA, and mite fall during the experiments was counted in parallel. To evaluate behavior, selected comb was divided into six equal fields, on 2 x 3 grid. Grooming dances were counted in top-left field in the selected time interval and computed to dances per hour. In experiments with caged bees the HBA proved to be toxic for bees regardless the mode of application and the concentration of HBA tested, which was highly unexpected. The number of allogrooming dances after insertion of cellulose carrier with HBA almost doubled on the first day and dropped sharply the next day. A peak in mite fall and a quick drop afterwards was also observed. No such change was observed neither in number of fallen mites nor in number of grooming dances in the control hive. Our results suggest that the mechanism of HBA action may not be through the haemolimph ingested by a mite but may be either contact-toxic to Varroa or may stimulate bees into performing allogrooming which is one of the successful mechanisms of Varroa mite resistance in bee colonies. This preliminary study is a stepping stone for further research on toxicity, suitable concentrations and applications of HBA as natural alternatives of suppression of Varroa in the future.
... Understanding the mechanisms behind resistance to varroa contributes to the understanding of this relatively new host-parasite relationship and ultimately helps to prevent colony losses. Since grooming behavior is a typical resistance trait of A. cerana and also occurs in A. mellifera, but with different mite removal success (Aumeier, 2001;Currie & Tahmasbi, 2008; for a review see Pritchard, 2016), we compared the grooming behavior between colonies of these two populations and control colonies. ...
... Besides environmental factors, the bees' genetic make-up affects the ability to groom (Bąk & Wilde, 2015). Although different heritabilities have been reported, it is not clear how high the degree is to which grooming is heritable (Pritchard, 2016;Zakar, Jávor, & Kusza, 2014). ...
... The idea of mite injury as a proxy for grooming behavior is indeed controversial (Bienefeld, Zautke, Pronin, & Mazeed, 1999;Boecking & Spivak, 1999;Fries, Huazhen, Wei, & Jin, 1996;Rinderer, De Guzman, & Frake, 2013). However, mite injury is thought to occur due to allo-grooming (Pritchard, 2016) and the group size in our cage experiment and individual grooming experiment may be too small to trigger allo-grooming and could thus explain the absence of mite injuries. ...
Article
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The ectoparasitic mite Varroa destructor is an important cause of high colony losses of the honey bee Apis mellifera. In The Netherlands, two resistant A. mellifera populations developed naturally after ceasing varroa control. As a result, mite infestation levels of the colonies of these populations are generally between 5–10%. However, the mechanisms behind mite resistance are still unclear. Since grooming behavior is a typical resistance trait that occurs in A. mellifera, we compared grooming between colonies of these two resistant populations and control colonies that had been treated against varroa twice a year in previous years. Grooming was investigated by measuring mite fall in broodless colonies in the field and in small cages with a fixed number of mites and bees in the lab. Furthermore, grooming was investigated at the individual level by measuring the effectiveness to remove dust by individual bees from the resistant and control colonies. We found that the grooming behavior of resistant colonies was unexpectedly equally or even less effective than that of control colonies. These results were supported by the effectiveness of individual bees to remove dust. Based on our results, we discuss that the trigger for grooming behavior may be density-dependent: grooming may be only beneficial at high mite infestation levels. Other resistance mechanisms than grooming are more likely to explain the varroa resistance of our two populations.
... 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). ...
Article
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]. ...
Article
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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. ...
Article
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). ...
Article
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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. ...
Article
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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.
... During grooming, workers brush mites off their bodies or those of their nest mates using their legs, and they may also bite them with their mandibles, thereby causing injuries to the mites, especially to their legs (Pritchard, 2016). A high propensity for grooming may partly explain the resistance of A. cerana (Büchler et al, 1992;Peng et al, 1987). ...
... SMR has also shown between-year variation (Kulincevic et al, 1988), potentially due to temperature fluctuations affecting the number of viable offspring produced per female mite (Bienefeld et al, 1995). Similarly, grooming is affected by environmental factors (Pritchard, 2016), varying according to the season, with less grooming being performed in spring than in summer (Büchler, 1993). It has been shown that the impact of grooming on mite mortality is reduced at lower temperatures (Currie and Tahmasbi, 2008;Tahmasbi, 2009) and at higher humidity (Tahmasbi, 2009), meaning that this trait in particular could be less efficient in terms of limiting the mite population during wintertime. ...
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Despite the implementation of control strategies, the invasive parasitic mite Varroa destructor remains one of the principal causes of honey bee (Apis mellifera) colony losses in numerous countries. For this reason, the parasite represents a serious threat to beekeeping and to agro-ecosystems that benefit from the pollination services provided by honey bees. Numerous selection programmes have been initiated over the last three decades with the aim of promoting the establishment of balance in the host–parasite relationship and, thus, helping European honey bees to survive in the presence of the parasite without the need for acaricide treatments. Such programmes have focused on either selective breeding for putative resistance traits or natural selection. To date, no clear overview of these attempts has been available, which has prevented building on past successes or failures and, therefore, hindered the development of a sustainable strategy for solving the V. destructor problem. In the present study, we review past and current selection strategies, report on their outcomes and discuss their limitations. Based on this state-of-the-art knowledge, we propose a strategy for increasing response to selection and colony survival against V. destructor infestations. Developing in-depth knowledge regarding the selected traits, optimising selection programmes and communicating their outcomes are all crucial to our efforts to establish a balanced relationship between the invasive parasite and its new host.
... Causing damages to Varroa mites (i.e. GB) is a heritable character in A. mellifera (Pritchard, 2016). Phoretic Varroa mites; foundress, gravid or daughter mites are exposed to grooming by bees especially daughter mites (Kirrane et al., 2012). ...
... The GB is differed among bee species, subspecies and hybrids (Balhareth et al., 2012;Bąk and Wilde, 2015;Pritchard, 2016). GB can be evaluated under filed conditions by calculating the percentage of damaged mites from the total number of fallen mites (Stanimirovic et al., 2010). ...
Article
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Extracts of drone larvae and propolis as safe materials are anticipated to boost the grooming behavior of honey bees against Varroa mites. It is also expected that grooming behavior of bees and morphology of Varroa are stable during the least active period of the year to bee colonies (i.e winter). Sugar syrup alone or mixed with drone larvae extract or propolis extract were examined as potential Varroa control materials to test these hypothesizes. Moreover, percentages of groomed mites along with body lengths and widths of Varroa were studied on weekly basis during winter. The results showed that propolis extract was able to increase the number of fallen mites under field conditions but with lethal impacts on bee workers in the laboratory than extract of drone larvae or sugar syrup. All the treatments were not able to boost the grooming behavior of bees. The results proved that grooming behavior was stable during winter. Therefore, it is better to select colonies with grooming potential against Varroa during winter in selection programs. December was significantly the minimal month in percentage of groomed mites based on the overall means. Means of measured characteristics of Varroa declined significantly over the study period. For beekeepers, using sugar syrup as spray on bees during regularly colony inspection can help managing Varroa populations without harming the bees.
... 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). ...
Article
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. ...
Article
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). ...
Article
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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. ...
Article
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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. Clinical Trials Registration: Not applicable
... 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). ...
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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 ppm 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). ...
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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). ...
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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]. ...
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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. ...
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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). ...
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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. ...
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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.
... contains supplementary material, which is available to authorized users. and (5) grooming behavior (Guzman-Novoa et al. 2012;Invernizzi et al. 2016;Pritchard 2016). ...
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The present study was conducted to quantify at the individual level the grooming behavior of bees from resistant colonies and susceptible colonies. Experienced and naive bees from resistant colonies were compared to experienced and naive bees from susceptible colonies at the age of 4, 7, 15 and 21 days. In a total of 480 assays, resistant bees successfully groomed off 10 times more mites placed than susceptible bees. Worker of different ages are involved but the lowest percentage of grooming was observed in 21-day-old bees. The experienced bees from resistant colonies bees that have evolved in a natural environment removed significantly more mites (69.2%) compared to naive bees (51.7%) who had no contact with other older bees.
... Resistance or tolerance to V. destructor mites is a typical characteristic of Africanized bees from South and Central America (e.g., Martin and Medina, 2004;Mondragón et al., 2005;Rivera-Marchand et al., 2012). There are also accounts of Varroa resistant and tolerant European-derived A. mellifera populations from North America, Europe, and other parts of the world (e.g., Fries et al., 2006;Le Conte et al., 2007;Seeley, 2007;Pritchard, 2016). Specific adaptive behaviors have evolved in these honey bee populations, mainly related to resistance mechanisms, such as hygienic behavior specifically targeting Varroa-infested capped brood cells (VSH), recapping, and grooming (reviewed by Mondet et al., 2020). ...
Article
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The Western honey bee, Apis mellifera, is an important species in providing honey and pollination services globally. The mite Varroa destructor is the major threat to A. mellifera, and it is associated with the severe colony winter mortality reported in recent decades. However, Varroa mite tolerant or resistant populations of A. mellifera have been detected around the world. A proposed mechanism responsible for limiting mite population growth in the colonies is grooming behavior, the physical removal and injury of mites from the adult bee bodies by individual workers or by their nest-mates. This behavioral strategy has been poorly studied in V. destructor-resistant colonies worldwide, especially in honey bee populations of European origin. In Argentina, honey bee stocks showing survival without mite treatment have been reported. In the present study, European-derived A. mellifera populations established in the Transition Chaco eco-region (Santa Fe province), with a subtropical climate, were characterized at the colony level. A honey bee stock showing natural Varroa-resistance (M) was compared to a Varroa-susceptible stock (C) for parameters of colony status (colony strength, percentage of Varroa infestation in adults and brood, hygienic behavior) and for indirect measures of grooming (percentage of fallen mites and damaged mites). M colonies showed lower phoretic and brood infestation and higher hygienic behavior in early autumn, and higher survival and population strength after wintering, in comparison with C colonies. The mean percentages of fallen mites and of damaged mites, and the injury to mites were higher in M than in C colonies. Our results suggest that, by modulating the parasitization dynamics in colonies, grooming behavior would be associated with the higher survival of Varroa-resistant stock. This study sheds light on how honey bee colonies can adaptively respond to mite pressure by modeling their behavior to resist Varroosis and provides evidence for grooming as an emerging factor evolving by natural selection. Percentage of damaged mites appears to be a reliable measure to enhance this behavior in honey bee colonies by selective breeding. Finally, the importance of improving and protecting locally adapted honey bee populations with natural Varroa resistance for regional apiculture is discussed.
... Our model also shows that grooming is an effective mechanism for controlling the growth of mites. The absence of grooming in the model can lead to very high populations of mites and the importance of grooming to bee survival has been noted by other authors [13,36,37]. ...
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The Varroa destructor mite has been associated with the recent decline in honey bee populations. While experimental data are crucial in understanding declines, insights can be gained from models of honey bee populations. We add the influence of the V. destructor mite to our existing honey bee model in order to better understand the impact of mites on honey bee colonies. Our model is based on differential equations which track the number of bees in each day in the life of the bee and accounts for differences in the survival rates of different bee castes. The model shows that colony survival is sensitive to the hive grooming rate and reproductive rate of mites, which is enhanced in drone capped cells.
... Allogrooming and autogrooming contribute to varroa resistance by removing mites from adult bees and also by physically damaging the mites, preventing them from seeking a new brood cell to infest [72]. Honey bees can initiate allogrooming via a 'grooming invitation signal'a whole-body vibrational dance lasting several secondswhich stimulates other workers to groom the dancer. ...
Article
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The parasitic mite, Varroa destructor, has shaken the beekeeping and pollination industries since its spread from its native host, the Asian honey bee (Apis cerana), to the naïve European honey bee (Apis mellifera) used commercially for pollination and honey production around the globe. Varroa is the greatest threat to honey bee health. Worrying observations include increasing acaricide resistance in the varroa population and sinking economic treatment thresholds, suggesting that the mites or their vectored viruses are becoming more virulent. Highly infested weak colonies facilitate mite dispersal and disease transmission to stronger and healthier colonies. Here, we review recent developments in the biology, pathology, and management of varroa, and integrate older knowledge that is less well known.
... 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 [72]. Honey bees can initiate allo-grooming via a "grooming invitation signal" -a wholebody vibrational dance lasting several seconds -which stimulates other workers to groom the dancer. ...
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The parasitic mite, Varroa destructor, has shaken the beekeeping and pollination industries since its spread from its native host, the Asian honey bee (Apis cerana), to the naïve European honey bee (A. mellifera) used commercially for pollination and honey production around the globe. Varroa is the greatest threat to honey bee health. Worrying observations include increasing acaricide resistance in the varroa population and sinking economic treatment thresholds, suggesting that the mites or their vectored viruses are becoming more virulent. Highly infested weak colonies facilitate mite dispersal and disease transmission to stronger and healthier colonies. Here, we review recent developments in the biology, pathology and management of varroa, and integrate older knowledge that is less well known.
... Hygienic behavior has been shown to be an effective behavioral mechanism against many diseases and Varroa parasites (Laidlaw and Page, 1997). Grooming behavior is relatively simple, involving removal or destruction of adult mites on the external surfaces of adult bees (Pritchard, 2016). ...
Article
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Grooming behavior, which is one of the behavioral resistance mechanisms based on the genetic basis in honeybees, is a defense response against parasitic mites, especially Varroa mite. In recent years, scientists and beekeepers have focused on bee breeding in terms of grooming behavior, because honey bees showing grooming behavior have the potential to can protect themselves against Varroa destructor. It is of great importance to determine the genes and gene regions related to this behavior before starting the breeding studies in terms of grooming behavior. In this respect, the right honey bee species or races can be selected and the success rate will increase. In researches, it was found that bees exhibit different grooming behaviors level according to species and races. Therefore, some species and races were found to be more successful than others. Especially in neural, developmental, detoxification and health-related gene expression studies, it has been shown that some gene expression is in direct proportion to the intensity of grooming behavior. While the genes responsible for grooming behavior are not known exactly, studies are underway to solve the genetic mechanism of this behavior. In this study, we reviewed the effects of neural gene expression on grooming behavior.
... 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 [80]. Honeybees can initiate allo-grooming via a "grooming invitation signal" -a wholebody vibrational dance lasting several seconds -which stimulates other workers to groom the dancer. ...
Preprint
Full-text available
The parasitic mite, Varroa destructor, has shaken the beekeeping and pollination industries since its spread from its native host, the Asian honeybee (Apis cerana), to the naïve European honeybee (A. mellifera) used commercially for pollination and honey production around the globe. Varroa is the greatest threat to honeybee health. Worrying observations include increasing acaricide resistance in the varroa population and sinking economic treatment thresholds, suggesting that the mites or their vectored viruses are becoming more virulent. Highly infested weak colonies, popularly dubbed “mite bombs”, facilitate mite dispersal and disease transmission to stronger and healthier colonies. Here, we review recent developments in the biology, pathology and management of varroa, and unearth old knowledge that was lost in the archives.
... En el acicalamiento las abejas se defienden de la varroa que tiene adheridas con sus patas, mandíbulas o movimientos, mordiéndola, dañándola y quitándosela de encima o al frotarse con otra superficie (Pritchard, 2016). ...
Article
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Antecedentes: La abeja melífera se encuentra amenazada por varios factores que provocan lo que hoy en día se conoce a nivel mundial como el Síndrome de Colapso de las colmenas, entre los cuales destaca la presencia del ácaro Varroa destructor. El objetivo de la reseña es actualizar la información sobre la Varroasis en Apis mellifera y de algunos mecanismos de defensa de las abejas en su coevolución con el parásito. Métodos: Se revisaron las bases de datos de Sciencedirect, Google-scholar, Scopus y NCBI con el empleo de las palabras claves: Varroa destructor, ciclo biológico, abejas, Apis, abejas africanizadas, apicultura y Apis mellifera. Se enfatizó en los artículos de los últimos cinco años. Resultados: Se describen las características del ácaro y su ciclo biológico, así como sus efectos sobre las colonias de abejas y los factores que influyen en la prevalencia del parásito. Además, se refieren los mecanismos como el comportamiento higiénico, acicalamiento, supresión de la reproducción del ácaro. Se actualiza sobre el impacto de la Varroasis a nivel mundial. Conclusiones: Ciertas poblaciones de abejas logran convivir con el ácaro varroa, pues sus mecanismos de defensa les permiten mantener tasas de infestación en rangos permisibles. En la actualidad existe la tendencia a incluir estos mecanismos en planes de mejoramiento.
... Apis cerana damages varroa mites with autogrooming and allogrooming and in so doing frequently removes them (Peng et al. 1987;Büchler et al. 1992). By contrast, similar behavior has rarely been seen in A. mellifera (Pritchard 2016). ...
Article
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The infestation of honey bees by the endoparasitic tracheal mite Acarapis woodi was first discovered in Apis mellifera on the Isle of Wight, England, and the mite has since spread to all continents except Australia. Since 2010, this tracheal mite has spread rapidly in the Japanese honey bee, Apis cerana japonica, of mainland Japan, causing considerable colony mortality. In contrast, infestations by the mites in the imported and managed European honey bee, A. mellifera, have rarely been observed in Japan. A previous laboratory experiment revealed a difference in susceptibility by demonstrating that the tracheal mite more frequently enters tracheae of A. cerana than those of A. mellifera. In this study, we compared autogrooming responses of A. cerana and A. mellifera by depositing a mite on each honey bee’s mesoscutum, and we then assessed the efficacy of autogrooming to remove the mite. The bees that received mites more frequently showed an autogrooming response compared to unchallenged bees in both bee species. However, a significantly greater proportion of A. mellifera individuals autogroomed compared to A. cerana. In addition, when bees autogroomed, A. mellifera removed the tracheal mite more effectively than A. cerana. When considering all bees in the mite-deposited group, the proportion of mite removal in A. mellifera was almost twice as high as that in A. cerana. Thus, the difference in susceptibility to the tracheal mite between these two bee species is attributed to the difference in the behavioral response threshold to mites and the effectiveness of mite removal by grooming.
... Autogrooming stimulates the allogrooming, which starts when bees perceive another bee performing the grooming dance, and generally involves several nestmates acting collaboratively. Both autogrooming and allogrooming could be useful in detecting and removing parasites [27]. ...
Article
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The high annual losses of managed honey bees (Apis mellifera) has attracted intensive attention, and scientists have dedicated much effort trying to identify the stresses affecting bees. There are, however, no simple answers; rather, research suggests multifactorial effects. Several works have been reported highlighting the relationship between bees' immunosuppression and the effects of malnutrition, parasites, pathogens, agrochemical and beekeeping pesticides exposure, forage dearth and cold stress. Here we analyze a possible connection between immunity-related signaling pathways that could be involved in the response to the stress resulted from Varroa-virus association and cold stress during winter. The analysis was made understanding the honey bee as a superorganism, where individuals are integrated and interacting within the colony, going from social to individual immune responses. We propose the term "Precision Nutrition" as a way to think and study bees' nutrition in the search for key molecules which would be able to strengthen colonies' responses to any or all of those stresses combined.
... El acicalamiento es la habilidad de las abejas obreras de remover ectoparásitos de sus cuerpos usando sus mandíbulas y sus patas (36,64) . Existen dos tipos de acicalamiento, auto acicalamiento y acicalamiento grupal, que incluye la participación de varias compañeras de la colonia que actúan en colaboración (65) , este último, es menos común que el auto-acicalamiento (66) . Las colonias de abejas que expresan esta habilidad en una alta proporción de sus obreras, son más resistentes a las infestaciones del ácaro Varroa destructor en comparación con colonias que lo expresan en una baja proporción de sus integrantes. ...
Article
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Resumen: Las abejas melíferas (Apis mellifera) polinizan plantas tanto de sistemas naturales como manejados para la agricultura, contribuyendo a la producción de alimentos y a sostener y aumentar la biodiversidad. Desafortunadamente, en la actualidad ocurren casos de despoblación y pérdida de colonias de abejas en todo el mundo. Diferentes factores contribuyen a la disminución de poblaciones de abejas, entre ellos, patógenos (parásitos, hongos, bacterias y virus), alteración o pérdida de ecosistemas, o el uso de agroquímicos. Todos estos factores alteran los mecanismos de defensa del sistema inmune de las abejas. Las abejas melíferas poseen un sistema inmune innato que incluye barreras físicas, así como respuestas celulares y humorales, que son generalizadas y que les permite defenderse contra organismos infecciosos y parasitarios. Además de los agentes patógenos, acaricidas, fungicidas, herbicidas y otros plaguicidas, han demostrado tener efectos sobre su salud y sistema inmune. Los mecanismos involucrados en la defensa están representados por vías de
... Slightly different duration of capping period has been seen in different honey bee species which can be considered as a resistance mechanism against Varroa mites (Table 1). Other resistance mechanisms are grooming and hygienic behaviors which have been comprehensively studied in the literature (Peng et al. 1987;Boecking 1992;Ardestani et al. 2002;Mondragón et al. 2005;Büchler et al. 2010;Ardestani et al. 2011;Kirrane et al. 2012;Pritchard 2016;Invernizzi et al. 2016;Nganso et al. 2017). ...
Article
The aim of this study was to assess the potential harmful effects of neonicotinoids inside honey bee colonies and especially on the honey bee pest, Varroa destructor. This paper shortly summarized previous studies which investigated the toxicity of neonicotinoids to honey bees. The possible exposure routes of these insecticides to Varroa mites inside and outside bee colonies were studied. And finally, the link between the adverse effects of neonicotinoids and Varroa mite life cycle in the brood cells and the influence of these chemicals on the mites inside bee colonies were investigated. It was concluded that the application of neonicotinoid insecticides on a variety of agricultural crops may result in the exposure of honey bees to these chemicals and as a consequence, Varroa mites (parasites living inside bee colonies) also got exposed to these insecticides indirectly. The present study re-emphasized on ecotoxicological attempts assessing the risk of these insecticides to honey bees as well as on ecological and behavioral aspects of their application inside bee colonies.
... Cognition is not mandatory though for the evolution of medication. previously shown that ants disinfect fungus-exposed brood through allogrooming (Tragust et al. 2013) and that grooming overall leads to parasite reduction on treated individuals (Pritchard 2016, Hughes et al. 2002. Our observations are the first, to our knowledge, to ...
Thesis
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An efficient foraging strategy is one of the most important traits for the fitness of animals. The theory of optimal foraging tries to predict foraging behaviour through the overarching question: how animals should forage so as to minimize costs while maximizing profits? Social insects, having occupied nearly every natural niche through widely different strategies, offer themselves as an ideal group to study how well optimal foraging theory can explain their behaviour and success. Specialization often leads to unique adaptations in morphology and behaviour. I therefore decided to investigate the behaviour of Megaponera analis. This ponerine ant species is specialized on hunting only termites of the subfamily Macrotermitinae at their foraging sites. Their foraging behaviour is regulated by a handful of individual scouts (10-20) that search for termite foraging sites before returning to the nest to recruit a large number of nestmates (200-500 ants). These ants then follow the scout in a column formation to the termites and after the hunt return together to the nest, these raids occur two to five times per day. Predators of highly defensive prey likely develop cost reducing adaptations. The evolutionary arms race between termites and ants led to various defensive mechanisms in termites, e.g. a caste specialized in fighting predators. As M. analis incurs high injury/mortality risks when preying on termites, some risk mitigating adaptations have evolved. I show that a unique rescue behaviour in M. analis, consisting of injured nestmates being carried back to the nest, reduces combat mortality. These injured ants “call for help” with pheromones present in their mandibular gland reservoirs. A model accounting for this rescue behaviour identifies the drivers favouring its evolution and estimates that rescuing allows for maintaining a 29% larger colony size. Heavily injured ants that lost too many legs during the fight on the other hand are not helped. Interestingly, this was regulated not by the helper but by the uncooperativeness of the injured ant. I further observed treatment of the injury by nestmates inside the nest through intense allogrooming directly at the wound. Lack of treatment increased mortality from 10% to 80% within 24 hours, with the cause of death most likely being infections. Collective decision-making is one of the main mechanisms in social insects through which foraging is regulated. However, individual decision-making can also play an important role, depending on the type of foraging behaviour. In M. analis only a handful of individuals (the scouts) hold all the valuable information about foraging sites. I therefore looked at predictions made by optimal foraging theory to better understand the interplay between collective and individual decision-making in this obligate group-raiding predator. I found a clear positive relation between raid size and termite abundance at the foraging site. Furthermore, selectivity of the food source increased with distance. The confirmation of optimal foraging theory suggests that individual scouts must be the main driver behind raid size, choice and raiding behaviour. Therefore most central place foraging behaviours in M. analis were not achieved by collective decisions but rather by individual decisions of scout ants. Thus, 1% of the colony (10–20 scouts) decided the fate and foraging efficiency of the remaining 99%. Division of labour is one of the main reasons for the success of social insects. Worker polymorphism, age polyethism and work division in more primitive ants, like the ponerines, remain mostly unexplored though. Since M. analis specializes on a defensive prey, adaptations to reduce their foraging costs can be expected. I found that the work division, task allocation and column-formation during the hunt were much more sophisticated than was previously thought. The column-formation was remarkably stable, with the same ants resuming similar positions in subsequent raids and front ants even returning to their positions if displaced in the same raid. Most of the raid tasks were not executed by predetermined members of the raid but were filled out as need arose during the hunt, with a clear preference for larger ants to conduct most tasks. I show that specialization towards a highly defensive prey can lead to very unique adaptations in the foraging behaviour of a species. I explored experimentally the adaptive value of rescue behaviour focused on injured nestmates in social insects. This was not only limited to selective rescuing of lightly injured individuals by carrying them back (thus reducing predation risk) but moreover includes a differentiated treatment inside the nest. These observations will help to improve our understanding of the evolution of rescue behaviour in animals. I further show that most optimal foraging predictions are fulfilled and regulated by a handful of individuals in M. analis. Lastly, I propose that the continuous allometric size polymorphism in M. analis allows for greater flexibility in task allocation, necessary due to the unpredictability of task requirements in an irregular system such as hunting termites in groups. All of my observations help to further understand how a group-hunting predator should forage so as to minimize costs while maximizing profits.
... In fact, a certain percentage of mites in a colony simply lose their grip and fall to the bottom of the hive over time. Moreover, in order to avoid parasitism by V. destructor, honey bees often exhibit defensive behaviors such as "grooming" which involves self-removal of phoretic Varroa mites on the body of adult bees [58]. When effective, this behavior leads to the removal of the parasite which is more likely to fall on the hive floor. ...
Article
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The biocontrol of the honey bee ectoparasite Varroa destructor is an underexploited but promising avenue that would benefit from being integrated in a Varroa management program. Our study aimed to investigate the potential of the predatory mite Stratiolaelaps scimitus to control Varroa infestations in honey bees. Tests on safety and predation were carried out to: (1) assess the risk of predation of the honey bee brood by S. scimitus under laboratory conditions and within the colony, and (2) evaluate the predation potential of S. scimitus on phoretic Varroa mites. Under laboratory conditions, S. scimitus was able to feed upon free Varroa mites, but also attacked every unprotected honey bee brood stages with a strong preference for bee eggs. When introduced inside colonies, however, S. scimitus does not have negative effects on the survival of the bee brood. Moreover, observations made in the laboratory revealed that S. scimitus does not attack Varroa mites when they are attached to the body of bees. However, all Varroa mites that had naturally fallen from the bees were predated upon by S. scimitus and died in less than 24h. This study provides evidence that S. scimitus does not represent a significant threat to the bee brood, but also suggests that its effect in Varroa control will probably be limited as it does not attack phoretic Varroa mites. Our results represent a first step in assessing the potential of S. scimitus to control V. destructor and provide novel information about the predator’s behavior inside the honey bee colony.
... (1) Targeted selection: We seek and choose (select) properties that coun- teract the development of varroa, and breed them into our bee stocks. For example, it could be breeding for hygienic behavior against the varroa mite (VSH) (Leclercq, Pannebakker, Gengler, Nguyen, & Francis, 2017;Wilson-Rich et al., 2009), or groom- ing of mites (Pritchard, 2016). Such breeding requires a highly coor- dinated approach and controlled mating of the queens with selected drones. ...
Article
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The honey bee is in Europe an endemic and wild species, with regional subspecies and many local adaptations. Although subspecies and populations have been hybridized, and despite some selective breeding, the honey bee still behaves naturally and increases its fitness through continuous local adaptation. In order to evolve more resilience against the varroa mite, a major threat, two ways are open: (1) targeted selection and breeding on a large or regional scale, and (2) natural selection for fitness in the presence of the varroa mite. While the success score for selective breeding is still scant, natural selection has delivered a few described cases of resistance, all in relatively short time periods. Resilience of an organism towards parasites and diseases can be obtained by resistance (the disease / parasite is hampered in its development and fitness) and by tolerance (the damage caused by the disease or parasite is avoided or restraint). Resistance and tolerance can act concurrently. A balanced relationship between host and parasite can develop through resistance and tolerance, and an important condition to reach such a balance is that the disease or parasite is vertically transmitted: from mother to offspring. When a parasite is transmitted horizontally, such a balanced relationship struggles to develop. With natural reproduction of honey bee colonies, parasites are transmitted vertically onto the new generation. Method (2) of natural selection does not interfere with this transmission route. By replication or rejuvenation of colonies with the introduction of foreign queens (method (1)), the transmission is largely horizontal. This applies as well for the transmission of beneficial organisms (symbionts) in the colony. In addition to reproduction of colonies and selective breeding, many other methods applied by beekeepers conflict with the bee colonies’ behaviours and resilience traits against parasites and diseases. Aligning methods to the natural traits of the bees, as well as the decision to start selection, targeted or natural, should be done with prudence to avoid evitable collateral damage.
... There are many more examples of colony responses and organization to parasite infections on a colony level [16,47], but our observations are more focused on the level of the individual. It has been previously shown that ants disinfect fungus-exposed brood through allogrooming [48] and that grooming overall leads to parasite reduction on treated individuals [49,50]. Our observations are the first, to our knowledge, to show this type of treatment to be directed towards a high-risk infection zone of an individual (open wounds). ...
Article
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Open wounds are a major health risk in animals, with species prone to injuries likely developing means to reduce these risks. We therefore analysed the behavioural response towards open wounds on the social and individual level in the termite group-hunting ant Megaponera analis. During termite raids, some ants get injured by termite soldiers (biting off extremities), after the fight injured ants get carried back to the nest by nest-mates. We observed treatment of the injury by nest-mates inside the nest through intense allogrooming at the wound. Lack of treatment increased mortality from 10% to 80% within 24 h, most likely due to infections. Wound clotting occurred extraordinarily fast in untreated injured individuals, within 10 min. Furthermore, heavily injured ants (loss of five extremities) were not rescued or treated; this was regulated not by the helper but by the unresponsiveness of the injured ant. Interestingly, lightly injured ants behaved ‘more injured’ near nest-mates. We show organized social wound treatment in insects through a multifaceted help system focused on injured individuals. This was not only limited to selective rescuing of lightly injured individuals by carrying them back (thus reducing predation risk), but, moreover, included a differentiated treatment inside the nest.
... Alleen de weg er naar toe is wel omstreden: gaan we via de (gangbare) weg van veredeling en imkerij (met behoud van de door de imker gewaardeerde eigenschappen), of volgen we de bijen in hun harde strijd om te overleven 'in de natuur'? 1. Gerichte selectie: we zoeken en kiezen (selecteren) eigenschappen die (de ontwikkeling van) varroamijten tegengaan, en kruisen deze gericht in onze bijenvolken in. Het zou bijvoorbeeld om hygiënisch uitruim gedrag tegen de Varroamijt (VSH) kunnen gaan (LeClerc et al. 2017;Wilson-Rich et al., 2009), of om grooming van mijten (Pritchard 2016). Dit vereist een zeer gecoördineerde aanpak en gecontroleerde paring van de koninginnen met darren. ...
... Evidence for this has been shown both at the colony level (Arechavaleta-Velasco & Guzmán-Novoa, 2001;Guzmán-Novoa, Emsen, Unger, Espinosa-Montaño, & Petukhova, 2012;Mondragó n, Spivak, & Vandame, 2005;Rinderer et al., 2001) and through assays inoculating individual bees with mites (Aumeier, 2001;Büchler, Drescher, & Tornier, 1992;Fries, Huazhen, Wei, & Jin, 1996;Guzmán-Novoa et al., 2012;Peng, Fang, Xu, & Ge, 1987). These are reviewed in detail by Rinderer et al. (2013), and also see Pritchard (2016). ...
Article
Grooming is a honey bee behavior that has the potential to minimize and manage the detrimental effects of $\textit{Varroa destructor}$. Here we tested the efficacy of the Bee Gym™, a device hypothesized to increase honey bee auto-grooming and increase mite removal from colonies. Natural mite fall from 20 colonies was counted for 14 days, after which half the colonies were fitted with a Bee Gym and half with a control object. Mite fall and the proportion of damaged mites were then recorded for another 14 days. Total mite fall was generally higher over the second 14 days, but this increase was not significantly higher for the Bee Gym colonies than for the control colonies. There was also no difference in the proportion of damaged mites between the two treatments. Mite fall and damage to mites may be influenced by other factors, and this is discussed; however, given that we found no effect of the Bee Gym, we conclude that there is no evidence from this study of its efficacy as a management strategy for $\textit{V. destructor}$. El aseo es un comportamiento de la abeja de la miel que tiene el potencial de minimizar y de manejar los efectos perjudiciales de $\textit{Varroa destructor}$. Aquí hemos probado la eficacia del Bee Gym ™, un dispositivo que hipotéticamente aumenta el auto-aseo en la abeja de la miel y aumentar la eliminación de ácaros de las colonias. La caída natural de ácaros de 20 colonias se contó durante 14 días, tras lo cual la mitad de las colonias fueron equipadas con un Bee Gym y la otra mitad con un objeto de control. La caída de ácaros y la proporción de ácaros dañados se registraron durante otros 14 días. La caída total de ácaros fue generalmente mayor durante los segundos 14 días, pero este aumento no fue significativamente mayor para las colonias con Bee Gym que para las colonias de control. Tampoco hubo diferencias en la proporción de ácaros dañados entre los dos tratamientos. La caída de ácaros y el daño a los ácaros pueden estar influidos por otros factores, lo cual se discute; sin embargo, dado que no encontramos ningún efecto del Bee Gym, concluimos que no hay evidencia en este estudio de su eficacia como estrategia de manejo para $\textit{V. destructor}$.
... Evidence for this has been shown both at the colony level (Arechavaleta-Velasco & Guzmán-Novoa, 2001;Guzmán-Novoa, Emsen, Unger, Espinosa-Montaño, & Petukhova, 2012;Mondragó n, Spivak, & Vandame, 2005;Rinderer et al., 2001) and through assays inoculating individual bees with mites (Aumeier, 2001;Büchler, Drescher, & Tornier, 1992;Fries, Huazhen, Wei, & Jin, 1996;Guzmán-Novoa et al., 2012;Peng, Fang, Xu, & Ge, 1987). These are reviewed in detail by Rinderer et al. (2013), and also see Pritchard (2016). ...
Article
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Grooming is a honey bee behavior that has the potential to minimize and manage the detrimental effects of Varroa destructor. Here we tested the efficacy of the Bee Gym™, a device hypothesized to increase honey bee auto-grooming and increase mite removal from colonies. Natural mite fall from 20 colonies was counted for 14 days, after which half the colonies were fitted with a Bee Gym and half with a control object. Mite fall and the proportion of damaged mites were then recorded for another 14 days. Total mite fall was generally higher over the second 14 days, but this increase was not significantly higher for the Bee Gym colonies than for the control colonies. There was also no difference in the proportion of damaged mites between the two treatments. Mite fall and damage to mites may be influenced by other factors, and this is discussed; however, given that we found no effect of the Bee Gym, we conclude that there is no evidence from this study of its efficacy as a management strategy for V. destructor.
Article
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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.
Article
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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.
Preprint
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.
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The significant risk of disease transmission has selected for effective immune-defense strategies in insect societies. Division of labour, with individuals specialized in immunity-related tasks, strongly contributes to prevent the spread of diseases. A trade-off, however, may exist between phenotypic specialization to increase task efficiency and maintenance of plasticity to cope with variable colony demands. We investigated the extent of phenotypic specialization associated with a specific task by using allogrooming in the honeybee, Apis mellifera, where worker behaviour might lower ectoparasites load. We adopted an integrated approach to characterize the behavioural and physiological phenotype of allogroomers, by analyzing their behavior (both at individual and social network level), their immunocompetence (bacterial clearance tests) and their chemosensory specialization (proteomics of olfactory organs). We found that allogroomers have higher immune capacity compared to control bees, while they do not differ in chemosensory proteomic profiles. Behaviourally, they do not show differences in the tasks performed (other than allogrooming), while they clearly differ in connectivity within the colonial social network, having a higher centrality than control bees. This demonstrates the presence of an immune-specific physiological and social behavioural specialization in individuals involved in a social immunity related task, thus linking individual to social immunity, and it shows how phenotypes may be specialized in the task performed while maintaining an overall plasticity.
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Honey bees are agriculturally important, both as pollinators and by providing products such as honey. The sustainability of beekeeping is at risk through factors of global change such as habitat loss, as well as through the spread of infectious diseases. In China and other parts of Asia, beekeepers rely both on native Apis cerana and non-native Apis mellifera, putting bee populations at particular risk of disease emergence from multi-host pathogens. Indeed, two important honey bee parasites have emerged from East Asian honey bees, the mite Varroa destructor and the microsporidian Nosema ceranae. As V. destructor vectors viral bee diseases, we investigated whether another key bee pathogen, Deformed Wing Virus (DWV), may also have originated in East Asian honey bee populations. We use a large-scale survey of apiaries across China to investigate the prevalence and seasonality of DWV in managed A. mellifera and A. cerana colonies, showing that DWV-A prevalence was higher in A. mellifera, with a seasonal spike in prevalence in autumn and winter. Using phylogenetic and population genetic approaches, we show that while China and East Asian DWV isolates show comparatively high levels of genetic diversity, these bee populations are not a source for the current global DWV epidemic.
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This article provides a translation in German of the Open Access article in Bee World (2018): Tjeerd Blacquière & Delphine Panziera (2018) A Plea for Use of Honey Bees’ Natural Resilience in Beekeeping, Bee World, 95:2, 34-38, DOI: 10.1080/0005772X.2018.1430999 https://www.tandfonline.com/doi/full/10.1080/0005772X.2018.1430999 Zusammenfassung Die Honigbiene ist in Europa eine endemische und wilde Art, mit regionalen Unterarten und vielen lokalen Anpassungen. Obwohl Unterarten und Populationen hybridisiert wurden und trotz einiger selektiver Zucht, verhält sich die Honigbiene immer noch natürlich und erhöht ihre Fitness durch kontinuierliche lokale Anpassung. Um mehr Widerstandsfähigkeit gegen die Varroamilbe, eine große Bedrohung, zu entwickeln, gibt es zwei Möglichkeiten: (1) gezielte Selektion und Zucht im großen oder regionalen Maßstab und (2) natürliche Selektion für die Fitness in Gegenwart der Varroa-Milbe. Während die Erfolgsquote bei der selektiven Züchtung noch gering ist, hat die natürliche Selektion in relativ kurzer Zeit einige beschriebene Resistenzen hervorgebracht. Die Resilienz eines Organismus gegenüber Parasiten und Krankheiten kann durch Resistenz (die Krankheit / der Parasit wird in seiner Entwicklung und Fitness behindert) und durch Toleranz (der durch die Krankheit oder den Parasiten verursachte Schaden wird vermieden oder gehemmt) erreicht werden. Resistenz und Toleranz können gleichzeitig wirksam sein. Ein ausgewogenes Verhältnis zwischen Wirt und Parasit kann sich durch Resistenz und Toleranz entwickeln, und eine wichtige Voraussetzung für ein solches Gleichgewicht ist, dass die Krankheit oder der Parasit vertikal übertragen wird: von der Mutter auf den Nachwuchs. Wenn ein Parasit horizontal übertragen wird, wird sich ein solches ausgewogenes Verhältnis nur schwer entwickeln können. Bei der natürlichen Vermehrung von Honigbienenvölkern werden Parasiten vertikal auf die neue Generation übertragen. Die Methode (2) der natürlichen Selektion stört diesen Übertragungsweg nicht. Durch Replikation oder Verjüngung von Bienenvölkern mit der Einweiselung von fremden Königinnen (Methode (1)) erfolgt die Übertragung weitgehend horizontal. Die gleichen Prinzipien gelten auch für die Übertragung von Nützlingen (Symbionten) in einer Kolonie. Neben der Vermehrung der Bienenvölker und der selektiven Zucht stehen viele andere Methoden der Imker im Widerspruch zum Verhalten der Bienenvölker und ihren Eigenschaften der Resilienz gegen Parasiten und Krankheiten. Die Anpassung der imkerlichen Methoden an die natürlichen Eigenschaften und Fähigkeiten der Bienen sowie die Entscheidung, mit der Selektion - gezielte oder natürliche - zu beginnen, sollte mit Umsicht erfolgen, um unnötige Kollateralschäden zu vermeiden.
Article
In animals, self-grooming is an important component of their overall hygiene because it reduces the risk of disease and parasites. The European honey bee (Apis mellifera) exhibits hygienic behavior, which refers to the ability of the members of a colony to remove diseased or dead brood from the hive. Individual grooming behavior, however, is when a bee grooms itself to remove parasites. While both behaviors are critical for the mitigation of disease, hygienic behavior is overwhelmingly more studied because, unlike grooming behavior, it has a simple bioassay to measure its phenotype. Here, we develop a novel bioassay to expedite data collection of grooming behavior by testing different honey bee genotypes (stocks). Individual worker bees from different commercial stocks were coated in baking flour, placed in an observation arena, and digitally recorded to automatically measure grooming rates. The videos were analyzed in MATLAB, and an exponential function was fit to the pixel data to calculate individual grooming rates. While bees from the different commercial stocks were not significantly different in their grooming rates, the automation of grooming measurements may facilitate future research and stock selection for this important mechanism of social immunity.
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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.
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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.
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Tliisstudy was uiidetlakcn to dctcniiiiic whcllícr Italiaii aiid AfricaJiizcdnieilifera workcre can ridÜicitísclvcs ofÜic initc Varroa Jacobsoni aftcr artificial infcstation with adull fciiialcs oftlús parasite.
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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.
Book
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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.
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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.
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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.
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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.
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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)
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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.
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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.
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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.
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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.
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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.
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Keywordschewed mites– Varroa destructor – Apis mellifera
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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.
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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.
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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.
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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.
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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.
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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 ($r^2 = 0.38$). 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 ($r = -0.65$ and $r = -0.76$, 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.
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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
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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
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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.
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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.
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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.