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Alma Mater Studiorum – Università Di Bologna Allma Mater Studiiorum – Uniiversiità dii Bollogna DOTTORATO DI RICERCA IN Biodiversità ed Evoluzione Ciclo 28 Settore Concorsuale di afferenza: 05/B1 Settore Scientifico disciplinare: BIO/05 Exploring Plant-Pollinator interactions: critical studies for the safeguard of wild Apoidea and spontaneous plant populations Presentata da: Gherardo Bogo Coordinatore Dottorato Relatore Prof.ssa Barbara Mantovani Prof.ssa Marta Galloni Co-relatore Dott.ssa Laura Bortolotti Esame finale anno 2016 “According to the laws of aerodynamics, the bumblebee can’t fly, but bumblebee doesn’t know anything about the laws of aerodynamics, so it goes ahead and flies anyway” Mary Kay Ash To my wonderful parents Contents CONTENTS 1. General introduction .................................................................................................. 1 1.1. Plant-pollinators relationship ................................................................................. 1 1.2. Global decline of bees ........................................................................................... 2 1.3. Eusocial Apidae: bumble bees and honey bees ..................................................... 4 1.3.1. Caste differentiation ....................................................................................... 5 1.3.2. Life cycle ........................................................................................................ 6 1.4. References ............................................................................................................. 9 2. General purposes ...................................................................................................... 14 2.1. References ........................................................................................................... 15 3. Evaluation and enhancement of wild Apoidea populations: pollinator community of Dictamnus albus .................................................................................... 17 3.1. LIFE+ PP-ICON project ...................................................................................... 17 3.2. Dictamnus albus .................................................................................................. 18 3.3. Aim of the study .................................................................................................. 20 3.4. References ........................................................................................................... 21 3.5. Integrated conservation of bee pollinators of a rare plant in a protected area near Bologna (Italy) ............................................................................................................ 23 3.6. Seasonal and annual variations in the pollination efficiency of a pollinator community of Dictamnus albus L. ............................................................................. 39 3.7. Temporal activity patterns in a pollination community of Dictamnus albus L. in relation to some biotic and abiotic factors .................................................................. 51 4. Role of nectar amino acids in plant-pollinator relationship: Gentiana lutea and social Apidae ................................................................................................................. 74 4.1 Gentiana lutea ...................................................................................................... 74 4.1.1 Protection and conservation .......................................................................... 76 4.1.2 Plant-pollinators relationship ......................................................................... 76 4.2. Nectar as floral rewards ....................................................................................... 77 4.2.1. Sugars ........................................................................................................... 78 i Contents 4.2.2. Amino acids .................................................................................................. 79 4.2.3. Non-protein amino acids .............................................................................. 80 4.2.4. Toxic nectar .................................................................................................. 81 4.3. Aim of the study .................................................................................................. 82 4.4. References ........................................................................................................... 84 4.5. Role of nectar amino acid composition in pollinator preference (Bombus terrestris L.) ................................................................................................................ 91 4.6. Role of nectar chemical composition in plant-pollinator interactions: Gentiana lutea L. as model species .......................................................................................... 114 4.7. Role of non protein amino acids in nectar: effects on bees behaviour .............. 131 5. Improvement of bumble bee colonies rearing through biological and technical measures ...................................................................................................................... 149 5.1. Inbreeding .......................................................................................................... 149 5.1.1. Inbreeding in social Hymenoptera .............................................................. 150 5.1.2. Diploid males in Bombus terrestris ............................................................ 152 5.2. Commercial rearing ........................................................................................... 152 5.3. Aim of the study ................................................................................................ 153 5.4. References ......................................................................................................... 155 5.5. Lab rearing applied method – Bumble bees colony rearing and release. .......... 159 5.6. Lack of partner preference system for incest avoidance in the bumble bee Bombus terrestris ...................................................................................................... 164 5.7. Inbreeding risk in the reproductive strategies of the bumble bee Bombus terrestris ................................................................................................................... 182 5.8. Effects of pre-diapause queens’ weight and pupae’s gender on colony initiation in artificially reared Bombus terrestris L. (Hymenoptera: Apidae) ......................... 198 6. General conclusions ................................................................................................ 218 Acknowledgements ..................................................................................................... 220 ii 1. General introduction CHAPTER 1 General introduction 1.1. Plant-pollinators relationship Plant-pollinators interactions are considered essential in the evolutionary process of Angiosperms and several mutual relations developed due to this connection (Biernaskie et al., 2005; Brunet, 2005). This co-evolution led entomophilous plant species to evolve lure and reward mechanisms that guarantee visits and fidelity of pollinator insects. Pollinators, in their turn, developed specific adaptations to interact with different types of flowers, ensuring plant pollen transfer from one individual to another, favouring allogamy and the fitness of the plant population (Richards, 1997). Even in some cases in which pollination is triggered by other vectors, pollinators can facilitate it and make it more effective. This relationship sometimes reached an extreme specialization level, in which the plant totally depends from a specific animal taxon for its reproduction. Plant-pollinator interactions can be very complex, since pollinators behaviour is influenced by many factors, such as flowers’ morphology, their arrangement, the plant density within the population, the plant population size, in addition to other biotic and abiotic factors (Kunin, 1993; Routley et al., 1999; Mitchell et al., 2004; Brunet, 2005). Pollination is the first step in sexual reproduction: pollen carriage is essential to preserve biodiversity of terrestrial ecosystems (Kevan, 1999). In case of zoophilous plants, especially if rare, threatened or particularly sensitive to environmental changes, the interaction network with pollinators plays a primary role. Pollinators are therefore extremely important, both from ecological and economical point of view. The delicate balance between plants and pollinators is constantly jeopardized by a whole series of anthropogenic factors, including fragmentation of habitat, land-use changes, modern agricultural practices, use of chemicals such as pesticides and herbicides and invasions of non-native plants and animals (Kearns et al., 1998). The need for active conservation of pollinators, with the aim of preserving plant-pollination interactions, is being appreciated only in the last few years. 1 1. General introduction 1.2. Global decline of bees In the whole spectrum of animal pollinators, bees (both managed and wild) are among the best ones. There are many potential threats that affect bee biodiversity in general and their abundance and diversity in particular (National Research Council, 2007). It is important to consider that these drivers are not independent factors (Brook et al., 2008), but they can interact with each other (Didham et al., 2007). Decline factors (Tab. 1) are
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