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Sustainable Agriculture Through Protection of Wild Bee Health

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Sustainable Agriculture Through Protection of Wild Bee Health Sustainable agriculture through protection of wild bee health: Investigation of transmission risk of the honey bee pathogen Nosema ceranae Inaugural-Dissertation to obtain the academic degree Doctor rerum naturalium (Dr. rer. nat.) submitted to the Department of Biology, Chemistry and Pharmacy of Freie Universität Berlin by Uta Müller 2019 This thesis was conducted between January 2015 and December 2018, under the supervision of Prof. Dr. Jens Rolff (Freie Universität Berlin) and Prof. Dr. Dino McMahon (Bundesanstalt für Materialforschung Berlin & Freie Universität Berlin). The work was carried out at Freie Universität Berlin. 1 st Reviewer: Prof. Dr. Jens Rolff 2 nd Reviewer: Prof. Dr. Dino McMahon Date of defense: 02.05.2019 1 Table of contents Table of contents 2 Acknowledgements 4 Summary 5 Zusammenfassung 7 Thesis Outline 9 List of Figures 10 List of Tables 12 General Introduction 13 Chapter 1: Associations between wild bee communities and Nosema ceranae in honey bees 31 1.1 Abstract 31 1.2 Introduction 32 1.3 Materials and Methods 33 1.4 Results 37 1.5 Discussion 46 1.6 Conclusion 49 1.7 Acknowledgements 49 1.8 References 50 Chapter 2: Susceptibility of the wild bee Osmia bicornis to the honey bee pathogen Nosema ceranae 55 2.1 Abstract 55 2.2 Introduction 56 2.3 Materials and Methods 57 2.4 Results 61 2 2.5 Discussion 66 2.6 Conclusion 69 2.7 Acknowledgements 69 2.8 References 70 Chapter 3: Life history effects in the solitary bee Osmia bicornis after larval exposure to the honey bee pathogen Nosema ceranae 74 3.1 Abstract 74 3.2 Introduction 75 3.3 Materials and Methods 76 3.4 Results 81 3.5 Discussion 87 3.6 Conclusion 90 3.7 Acknowledgements 90 3.8 References 90 General Discussion 97 Conclusion 105 References (Introduction and Discussion) 106 Declaration of Authorship 133 Appendix 134 Supplementary Material General Introduction 134 Supplementary Material Chapter 3 134 3 Acknowledgements I am thankful for the Deutsche Bundesstiftung Umwelt for providing funding and a valuable network for my thesis. I very much thank Prof. Jens Rolff and Prof. Dino McMahon for their engaged support and supervision of the thesis. I am very greatful to the Bachelorstudents Julia Lorenz and Lorin Schellenberg and the Masterstudent Kathrin Bramke for their contribution. I thank Dr. Christoph Saure for identification of collected bee sample and valuable professional advice, Dr. Erhard Strohm on sharing expertise on Osmia bicornis, the Deutsche Bieneninstitut for providing data on distribution of N. ceranae in honey bees and laboratory training, Dr. Lena Wilfert for exchange of information and skills in virus detection, Marika Harz and Benedickt Polacez for providing honey bees for laboratory experiments. I appreciate the cooperativeness of numerous beekeepers in providing honey bee samples and field sides for collection, the Landschaftspflegeverein Nuthe-Nieplitz for allowing the establishment of nesting resources on their orchards. I thank the Departments for Environment of Berlin and Brandenburg for granting their permission to sample wild bees. I thoroughly thank my working group members for all their support, in professional questions and discussions, motivation, laughing and the great office atmosphere. Many, many thanks go to my friends and family who have always been there with great encouragement. 4 Summary Pollinators are declining globally and emerging pathogens are among the causative factors. Pathogens are shared between domesticated honey bees and wild pollinators with flowers as transmission hubs. In contrast to honey bees, pathogen impacts in wild bees remain mostly unstudied. This thesis aimed to investigate associations between honey bees infected with Nosema ceranae and wild bees in the field as well as direct effects in a solitary wild bee experimentally inoculated with N. ceranae. Chapter 1 used a field survey approach to test how the presence of honey bees infected with N. ceranae affects the community composition of wild bees sharing the habitat. The results demonstrate a negative correlation between functional diversity of wild bees and the presence of infected honey bees. However, this relationship differs between functional groups. The occurrence of the rare parasitic, the cavity-nesting ones and also the Red List species is negatively associated with pathogen presence in the surrounding honey bee hives whereas the opposite is shown for common social-polylectic species. Furthermore, a habitat analysis revealed that both the highly specialized solitary-oligolectic and the threatened Red List species were particularly dependent on high coverage of suitable foraging and nesting habitat. In conclusion, sensitivity to N. ceranae associated stressors has to be considered differentially for particular functional groups which argue for the support of a functionally diverse pollinator community and special arrangements for the most severely affected groups. In Chapter 2, the agriculturally managed wild bee Osmia bicornis was used as model for solitary bees in an inoculation experiment with N. ceranae. The results revealed that inoculation had negligible impacts only on male survival. Several different species of wild bees that shared floral resources with infected honey bees in the environment were screened for the pathogen and were shown to be widely positive for N. ceranae whereas the pathogen was not detected in wild bees collected at another field site with uninfected honey bees. O. bicornis could therefore be acting as a pathogen reservoir and vector enhancing the circulation of N. ceranae within the pollinator network which affects both managed and wild bees. Larvae of O. bicornis were exposed to spores of N. ceranae during development in Chapter 3. Exposed individuals were characterized by a greater mortality and a delay in the onset of pupation even though very few spores were detected in a few individuals. Exposure was also associated with a reduction in body size in males as well as an increase in head capsule width in both sexes. The individuals which were exposed to the pathogen as larvae 5 did not show any fitness costs after hatching. The results indicate that even without proliferation, N. ceranae can have sublethal effects on particular life history stages of O. bicornis and affect development in this solitary bee model. Collectively, the results suggest indirect and direct impacts of N. ceranae on solitary wild bees but have to be extrapolated with caution regarding species-specific differences in pathogen impacts. Furthermore, in the environment, multiple stressors are afflicting wild bees and can interact synergistically. The present thesis delivers useful starting points for further inoculation experiments with a suitable solitary wild bee model and important information regarding pathogen reservoir species within the pollinator community. In conservation management, special support for particularly sensitive functional groups and life stages is required. 6 Zusammenfassung Bestäuber sind weltweit von Rückgängen betroffen wobei neue Krankheitserreger eine der Ursachen sind. An Blüten als Übertragungspunkten treffen sowohl domestizierte Honigbienen als auch auf wildlebende Bestäuber auf die Erreger. Im Gegensatz zu Honigbienen sind die Auswirkungen der Pathogene in Wildbienen bisher kaum erforscht. Diese Arbeit untersucht Zusammenhänge zwischen Honigbienen, die mit Nosema ceranae infiziert sind, und Wildbienen im Freiland. Außerdem werden direkte Effekte einer experimentellen Infizierung mit N. ceranae in einer solitären Wildbienenart betrachtet. Im ersten Kapitel wurde mittels einer Feldstudie untersucht, wie sich das Vorhandensein von Honigbienen, die mit N. ceranae infiziert sind, auf die Gemeinschaft der Wildbienen im geteilten Habitat auswirkt. Die Ergebnisse zeigen, dass ein negativer Zusammenhang zwischen der funktionellen Diversität der Wildbienen und der Präsenz von infizierten Honigbienen besteht. Allerdings unterschied sich dieser Zusammenhang zwischen verschiedenen funktionellen Gruppen. Das Vorkommen von seltenen, von parasitischen und von in Hohlräumen nistenden sowie der Rote-Liste Arten stand in einem negativen Zusammenhang mit Pathogenbefall in umliegenden Bienenstöcken. In Hinblick auf die häufigen, die sozial lebenden und die polylektischen Arten zeigte sich eine gegenläufige Beziehung. Weiterhin legte eine Habitatanalyse offen, dass sowohl hochspezialisierte solitärlebende und oligolektische wie auch bedrohte Rote-Liste Arten besonders abhängig von einer hohen Deckung von Nahrungs- und Nisthabitaten sind. Schlussfolgernd muss die Anfälligkeit gegenüber mit N. ceranae assoziierten Stressfaktoren für verschiedene funktionelle Gruppen unterschiedlich bewertet werden. Dies spricht für die Unterstützung einer diversen Bestäubergesellschaft mit besonderen Maßnahmen für die am stärksten beeinträchtigten Gruppen. In Kapitel 2 wurde die landwirtschaftlich eingesetzte Wildbiene Osmia bicornis als ein Modell für Solitärbienen in einem Infektionsexperiment mit N. ceranae untersucht. Die Ergebnisse der Infizierung zeigten eine geringfügig negative Auswirkung ausschließlich auf das Überleben der behandelten Männchen. Verschiedene Wildbienenarten, die sich in ihrer natürlichen Umgebung Blüten mit infizierten Honigbienen teilten, wurden gefangen und auf N. ceranae untersucht. Dabei erwiesen sich viele von ihnen als Träger des Pathogens wohingegen es in Wildbienen, von einer anderen Probestelle mit uninfizierten Honigbienen, nicht gefunden wurde. Demnach kann O. bicornis ein Pathogenreservoir sowie
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