Pathogen dynamics and tolerance behavior of the bee, Apis mellifera unicolor, following the introduction of Varroa destructor in La Réunion

L'abeille mellifère (Apis mellifera) est confrontée à une multitude de facteurs de stress biotiques et abiotiques qui ont induit à un déclin de ses populations au niveau mondial. La pathosphère de l'abeille et les interactions qui en découlent sont de mieux en mieux connues chez les sous-espèces européennes en zone tempérée. Il existe peu de données dans les zones tropicales et sur des sous-espèces d'autres lignées d'A. mellifera. La sous-espèce de lignée africaine A. m. unicolor est présente dans le Sud-Ouest de l’Océan Indien. Elle est indigène et endémique à la Réunion. L’introduction de l’ectoparasite Varroa destructor en 2017 a fortement impacté les colonies d’abeilles à La Réunion. Cet acarien affaiblit les abeilles et augmente leur vulnérabilité face aux pathogènes. De plus, il transporte des virus de l'abeille. La lutte chimique est le principal moyen de lutte contre le parasite. Toutefois, des mécanismes héritables de résistance ont été identifiés. Le premier objectif de la thèse était de mieux comprendre le cycle biologique d’A. m. unicolor en zone tropicale, en se concentrant sur la production de couvain et la durée d’operculation des nymphes. En effet, une réduction de cette durée pourrait réduire la reproduction de Varroa. Les colonies à La Réunion ont été capables d’élever du couvain toute l’année, avec une variation saisonnière. La durée d'operculation des nymphes d’A. m. unicolor est de 280 h. Une étude comparative a montré que les populations africaines avaient une durée d’operculation plus courte que les populations européennes. A. m. unicolor se situe parmi les populations hybrides, qui constituent un groupe intermédiaire. Un deuxième objectif était d'observer l’installation de Varroa destructor dans les colonies et de suivre sa dynamique, ainsi que celle de deux virus, le Deformed Wing Virus (DWV) et le Chronic Bee Paralysis Virus (CBPV). Des colonies ont été suivies sur deux périodes d’un an et sur deux ruchers expérimentaux. L'installation du parasite à induit une forte mortalité, jusqu’à 85% des colonies au bout d'un an, et des taux d'infestation élevés, jusqu’à 52 acariens pour cent abeilles. Le DWV a suivi l'établissement de Varroa dans les colonies et le taux d'infestation du parasite a eu un effet significatif sur sa prévalence et sa charge virale. Le CBPV n'est apparu que de manière transitoire au long des suivis. Les données ont montré que, dans les colonies tropicales qui élèvent du couvain toute l'année, Varroa et le DWV sont néanmoins soumis à une dynamique saisonnière qui semble influencée par les conditions environnementales. Le troisième objectif du travail était de mesurer deux mécanismes de résistances d’A. m. unicolor à Varroa, le Varroa Sensitive Hygiene (VSH), qui correspond à la capacité des ouvrières à détecter et retirer le couvain parasité, et le Mite Non-Reproduction (MNR), qui correspond à la capacité à réduire le succès reproducteur des Varroa fondatrices dans le couvain operculé. Les colonies ont montré une capacité à retirer les nymphes infestées (VSH) modérée et similaire à celles retrouvées dans des colonies d’abeilles européennes ou chez A. m. scutellata de lignée africaine. Elles ont par contre montré une proportion de MNR élevée, la moitié des fondatrices ayant une diminution de leur succès reproducteur, ce qui indiquerait une potentielle résistance. L'ensemble de ces résultats apporte de nouvelles connaissances sur une abeille de lignée africaine en milieu tropical. Ces résultats peuvent influencer les pratiques apicoles locales, notamment en terme de gestion des transhumances, mais aussi dans la mise en place de programmes de sélection d’abeilles résistantes à Varroa, tels qu'ils ont été réalisés sur des populations européennes. En effet, les variabilités observées dans les mesures de VSH et MNR suggèrent une possibilité de sélection de colonies résistantes d'A. m. unicolor à La Réunion.The honeybee (Apis mellifera) has been facing a multitude of biotic and abiotic stressors that have led to a decline in its populations worldwide. The pathogens of the honeybee and the resulting interactions are best known in European subspecies in temperate climates. There is few data in tropical areas and on subspecies of other lineages of A. mellifera. The African lineage subspecies A. m. unicolor is present in the South Western Indian Ocean. It is indigenous and endemic to La Réunion. The introduction of the ectoparasite Varroa destructor in 2017 had a major impact on bee colonies in La Réunion. The mite weakens bees and increases their vulnerability to other pathogens. In addition, it may carry honeybee viruses. Chemical treatments is the main means of controlling the parasite. However, heritable resistance mechanisms have been identified in the honeybee. The first objective of the thesis was to better understand the life cycle of A. m. unicolor, focusing on brood production and the capping period of pupae. Indeed, a reduction of this duration could reduce the reproduction of Varroa. Colonies were able to rear brood all year long, with seasonal variations. The capping period of A. m. unicolor is 280 h. A comparative study showed that African populations had a shorter capping period than European populations. A. m. unicolor is among the hybrid populations, which constitute an intermediate group. A second objective was to observe the establishment of V. destructor in the colonies and to follow its dynamics, as well as the dynamics of two viruses, the Deformed Wing Virus (DWV) and the Chronic Bee Paralysis Virus (CBPV). Colonies were monitored over two one-year periods in two experimental apiaries. The establishment of the parasite resulted in high mortality, up to 85% of colonies after one year, and high infestation rates, up to 52 mites per hundred bees. DWV followed the establishment of Varroa in the colonies and the infestation rate of the parasite had a significant effect on its prevalence and loads. CBPV appeared only transiently during the monitoring. The data showed that, in tropical colonies with permanent brood rearing, Varroa and DWV are nevertheless subjected to seasonal dynamics that could be influenced by environmental conditions. The third objective was to measure two resistance mechanisms of A. m. unicolor towards mites, Varroa Sensitive Hygiene (VSH), which corresponds to the ability of workers to detect and remove parasitized pupae, and Mite Non-Reproduction (MNR), which corresponds to the ability to reduce the reproductive success of Varroa foundresses in capped cells. The colonies showed a moderate ability to remove infested pupae (VSH), similar to those found in European subspecies or in A. m. scutellata (African lineage). However, they showed a high proportion of MNR, with half of the foundresses with a decreased reproductive success, which would indicate potential resistance. All these results provide new knowledge on an African lineage honeybee in a tropical environment. These results may influence local beekeeping practices, particularly transhumance management, but also the development of selection programs of Varroa resistant honeybees, such as those carried out on European populations. Indeed, the variabilities observed in the VSH and MNR measures suggested a possibility of selection of resistant colonies of A. m. unicolor in La Réunion

Tri‐trophic interactions among <i>Fopius arisanus</i> , Tephritid species and host plants suggest apparent competition

Data are available on CIRAD Dataverse https://doi.org/10.18167/DVN1/NYZ2NR (https://dataverse.cirad.fr).International audienceWhen several polyphagous herbivore species share a parasitoid, the tri-trophic interaction networks can be difficult to predict. In addition to direct effects, the parasitoid may influence the herbivore community by mediating indirect interactions among hosts. The plant species can also modulate the parasitoid preference for a specific host. One of the indirect effects is apparent competition, a negative interaction between individuals as a result of the action of shared natural enemies. Here, we focus on the interactions between the parasitoid Fopius arisanus (Braconidae) and two generalist fruit fly pests: Bactrocera dorsalis and Bactrocera zonata (Tephritidae). This parasitoid was introduced into La Reunion in 2003 to control populations of B. zonata and can also interact with B. dorsalis since its invasion in 2017. Our main objective is to characterize the tri-trophic interactions between F. arisanus, fruit fly and host plant species. We developed a long-term field database of fruit collected before and after the parasitoid introduction and after the B. dorsalis invasion in order to compare parasitism rate and fruit fly infestation for the different periods. In laboratory assays, we investigated how the combination of fruit fly species and fruit can influence the preference of F. arisanus. In the field, before the invasion of B. dorsalis, the parasitism rate of F. arisanus was low and had a little impact on the fruit fly infestation rate. After the B. dorsalis invasion, we observed an increase in parasitism rate from 5% to 17%. A bioassay showed that females of F. arisanus could discriminate between eggs of different fruit fly and host plant species. The host plant species preference changed in relation to the fruit fly species inoculated. Field observations and laboratory experiments suggest the possible existence of apparent competition between B. dorsalis and B. zonata via F. arisanus

Tri‐trophic interactions among <i>Fopius arisanus</i> , Tephritid species and host plants suggest apparent competition

Data are available on CIRAD Dataverse https://doi.org/10.18167/DVN1/NYZ2NR (https://dataverse.cirad.fr).International audienceWhen several polyphagous herbivore species share a parasitoid, the tri-trophic interaction networks can be difficult to predict. In addition to direct effects, the parasitoid may influence the herbivore community by mediating indirect interactions among hosts. The plant species can also modulate the parasitoid preference for a specific host. One of the indirect effects is apparent competition, a negative interaction between individuals as a result of the action of shared natural enemies. Here, we focus on the interactions between the parasitoid Fopius arisanus (Braconidae) and two generalist fruit fly pests: Bactrocera dorsalis and Bactrocera zonata (Tephritidae). This parasitoid was introduced into La Reunion in 2003 to control populations of B. zonata and can also interact with B. dorsalis since its invasion in 2017. Our main objective is to characterize the tri-trophic interactions between F. arisanus, fruit fly and host plant species. We developed a long-term field database of fruit collected before and after the parasitoid introduction and after the B. dorsalis invasion in order to compare parasitism rate and fruit fly infestation for the different periods. In laboratory assays, we investigated how the combination of fruit fly species and fruit can influence the preference of F. arisanus. In the field, before the invasion of B. dorsalis, the parasitism rate of F. arisanus was low and had a little impact on the fruit fly infestation rate. After the B. dorsalis invasion, we observed an increase in parasitism rate from 5% to 17%. A bioassay showed that females of F. arisanus could discriminate between eggs of different fruit fly and host plant species. The host plant species preference changed in relation to the fruit fly species inoculated. Field observations and laboratory experiments suggest the possible existence of apparent competition between B. dorsalis and B. zonata via F. arisanus

Quantitative virus dynamics in Apis mellifera unicolor colonies after a new invasion of Varroa destructor in La Réunion Island

International audienc

A better understanding of biological traits of the tropical honeybee subspecies Apis mellifera unicolor

International audienc

The post-capping period of the tropical honey bee subspecies Apis mellifera unicolor in La Réuion

The honey bee Apis mellifera has shown a great intraspecific diversity, together with a variability of its life history traits. The development of the brood has been well documented in temperate but much less in tropical subspecies, but a limited number of studies focused on tropical subspecies. This study measures the post-capping period of A. mellifera unicolor, an African lineage subspecies living in a tropical and insular environment. The post-capping period was measured on 15 colonies distributed on two apiaries located at different altitudes (150 m and 900 m) in La Réunion. The mean post-capping period of A. mellifera unicolor was 280.1 ± 0.12 h and was significantly shorter in colonies at low altitude. A comparative analysis of the literature on the post-capping period for different subspecies showed that the post-capping period of the African lineage was significatively shorter than that of European lineage. A. mellifera unicolor post-capping period belonged to the hybrid cluster between them. Knowledge of such life history traits of A. mellifera unicolor may have implications for beekeeping practices and should be considered as one of the potential resistance traits to be evaluated in Varroa destructor breeding programmes

Quantitative virus dynamics in Apis mellifera unicolor colonies after a new invasion of Varroa destructor in La Réunion Island

International audienc

A better understanding of biological traits of the tropical honeybee subspecies Apis mellifera unicolor

International audienc

An overview of the honeybee genetic diversity and health in the Indian Ocean Islands

International audienc