Varroa destructor is a real challenger for beekeepers and scientists: fragile out of the hive, tenacious inside a bee colony. From all the research done on the topic, we have learned that a better understanding of this organism in its relationship with the bee but also for itself is necessary. Its biology relies mostly on semiochemicals for reproduction, nutrition, or orientation. Many treatments have been developed over the years based on hard or soft acaricides or even on biocontrol techniques. To date, no real sustainable solution exists to reduce the pressure of the mite without creating resistances or harming honeybees. Consequently, the development of alternative disruptive tools against the parasitic life cycle remains open. It requires the combination of both laboratory and field results through a holistic approach based on health biomarkers. Here, we advocate for a more integrative vision of V. destructor research, where in vitro and field studies are more systematically compared and compiled. Therefore, after a brief state-of-the-art about the mite’s life cycle, we discuss what has been done and what can be done from the laboratory to the field against V. destructor through an integrative approach.

Varroa destructor, a major ectoparasite of the Western honey bee Apis mellifera, is a widespread pest that damages colonies in the Northern Hemisphere. Throughout their lifecycle, V. destructor females feed on almost every developmental stage of their host, from the last larval instar to the adult. The parasite is thought to feed on hemolymph and fat body, although its exact diet and nutritional requirements are poorly known. Using artificial Parafilm™ dummies, we explored the nutrition of V. destructor females and assessed their survival when fed on hemolymph from bee larvae, pupae, or adults. We compared the results with mites fed on synthetic solutions or filtered larval hemolymph. The results showed that the parasites could survive for several days or weeks on different diets. Bee larval hemolymph yielded the highest survival rates, and filtered larval plasma was sufficient to maintain the mites for 14 days or more. This cell-free solution therefore theoretically contains all the necessary nutrients for mite survival. Because some bee proteins are known to be hijacked without being digested by the parasite, we decided to run a proteomic analysis of larval honey bee plasma to highlight the most common proteins in our samples. A list of 54 proteins was compiled, including several energy metabolism proteins such as Vitellogenin, Hexamerin, or Transferrins. These molecules represent key nutrient candidates that could be crucial for V. destructor survival.

Varroa destructor (Anderson and Trueman) is known as a major pest of Apis mellifera L, especially in the Northern Hemisphere where its effects can be deleterious. As an obligate parasite, this mite relies entirely on its host to reproduce and complete its cycle. Studies focusing on isolated organs are needed to better comprehend this organism. To conduct such targeted molecular or physiological studies, the dissection of V. destructor mites is crucial as it allows the extraction of specific organs. Here, we propose a technical article showing detailed steps of females V. destructor dissection, illustrated with pictures and videos. These illustrated guidelines will represent a helpful tool to go further in V. destructor research.

Beekeepers can use a variety of treatments against Varroa destructor, the parasitic mite of Apis mellifera. However, sustainable and easy-to-use solutions are still scarce, considering the complexity of reaching the parasite alone. Current treatments involve soft acaricides, although their mechanism of action is not well understood. We investigated the effects of organic acids such as tartaric, lactic, formic, and citric acids on the attachment abilities of V. destructor under laboratory conditions. Preventing parasites from gripping or holding on to their hosts is a crucial target for mite control strategies. We challenged grip skills through the Rotavar setup after the direct application of acids to mites’ arolia. We also tested the potential for mites to fall off honeybees after bee treatment. We found that tartaric, citric, and lactic acids were good candidates to impair the attachment of V. destructor twenty-four hours post-treatment. However, lactic acid remained the only candidate at a reasonable concentration to destabilise mites after the honey bee’s treatment without reducing their lifespan. While we conducted these experiments under artificial conditions, our results improved our comprehension of the organic acids’ potential impact on V. destructor. They can also help with the development of new methods for hive application for beekeepers worldwide.

Olfaction is a major sense in Varroa destructor. In natural conditions, it is known that this honey bee parasite relies on kairomones to detect its host or to reproduce. Yet, in artificial conditions, the parasite is able to feed and survive for a few days even though most honey bee pheromones are lacking. Other key cues are thus probably involved in V. destructor perception of its close environment. Here, we used several artificial feeding designs to explore the feeding behaviour of the parasite when it is deprived of olfactory cues. We found that V. destructor is still able to feed only guided by physical cues. The detection of the food source seems to be shape-related as a 3D membrane triggers arrestment and exploration more than a 2D membrane. The tactile sense of V. destructor could thus be essential to detect a feeding site, although further studies are needed to assess the importance of this sense combined with olfaction in natural conditions.

Effets de l'acide lactique sur les fonctions biologiques et le comportement de Varroa destructor : vers une meilleure compréhension du parasite pour le développement de solutions de lutte par biocontrôle: Varroa destructor est l'un des principaux facteurs d'affaiblissement des colonies d'abeilles domestiques. Cependant, les solutions de lutte durables sont peu nombreuses du fait de la proximité entre l'hôte et le parasite. Depuis des années, de nombreux traitements sont exploités dont les acides organiques présents naturellement dans le miel. Bien qu'employé à l'échelle mondiale, le mode d'action de ces acaricides naturels reste très peu décrit, et notamment leurs potentiels effets sur l'agrippement. Parmi les principales stratégies de contrôle, l'interférence des acides organiques avec les capacités d'agrippement, vitales pour un ectoparasite tel que V. destructor, reste peu étudiée. En effet, l'acarien utilise des coussinets adhésifs appelés les arolia afin de s'accrocher sur l'abeille. Parmi ces acides naturels, l'acide lactique est utilisé comme acaricide depuis trente ans sans connaissances détaillées des mécanismes d'action impliqués et reste encore aujourd'hui peu investigué. L'objectif de ma thèse était d'étudier le mode d'action de l'acide lactique sur V. destructor dans le but de développer un traitement durable. J'ai d'abord créé des dispositifs dédiés aux études comportementales et adaptés à la taille de l'acarien dont le Rotavar spécifiquement construit pour tester ses capacités d'agrippement. J'ai souligné pour la première fois l'existence d'un fluide sous les arolia de V. destructor. Par ailleurs, j'ai démontré que l'acide lactique n'était pas un acaricide mais qu'il interférait plutôt avec les capacités d'agrippement du parasite lorsqu'il était mis en contact directement, mais aussi indirectement via le traitement des abeilles. J'ai comparé ces effets à ceux obtenus à la suite d'une exposition aux acides formique, citrique ou tartrique et observé un effet spécifique de l'acide lactique sur les capacités d'agrippement de l'acarien. En particulier, j'ai démontré des altérations de la forme des arolia dans le temps, ainsi qu'une accumulation de fluide, induites par le traitement à l'acide lactique. J'ai aussi analysé les coûts adaptatifs d'un déficit d'agrippement, et noté des capacités de locomotion et de reproduction réduites chez le parasite. Je me suis ensuite intéressée aux potentiels effets sublétaux sur l'hôte en exposant de manière chronique les abeilles à l'acide lactique, ce qui n'a pas engendré d'accumulation dans les organes. Ainsi, mes résultats suggèrent que l'acide lactique semble opérer localement même si un mode d'action systémique ne peut être totalement rejeté. Mes travaux de thèse sont les premiers à décrire l'activité de l'acide lactique sur V. destructor ainsi que les potentiels effets sublétaux sur les abeilles. Ils visent à encourager de futures études utilisant une approche centrée sur l'acarien afin d'appliquer de manière adéquate les traitements tout en préservant la santé des abeilles, de la faune et finalement humaine.