Multitrophic interactions in oak Dissertation von Michael Bacht Philipps-Universtität Marburg Juli 2015 Multitrophic interactions in oak Dissertation zur Erlangung des Doktrogrades der Naturwissenschaften (Dr. rer. nat.) dem Fachbereich Biologie der Philipps-Universität Marburg vorgelegt von Michael Bacht aus Essen Marburg an der Lahn, Juli 2015 ________________________________________________________________________________ Vom Fachbereich Biologie der Philipps-Universität Marburg als Dissertation am angenommen. Erstgutachter: Dr. habil. Martin Schädler Zweitgutachter: Prof. Dr. Roland Brandl Tag der mündlichen Prüfung am: Table of contents Chapter I – General introduction Interactions between mycorrhizal fungi and herbivores................................................................. 3 Mycorrhization and plant defenses................................................................................................. 5 The role of plant growth stages....................................................................................................... 6 Aims of the thesis............................................................................................................................ 7 Chapter II Introduction..................................................................................................................................... 13 Materials and methods..................................................................................................................... 16 Results............................................................................................................................................. 20 Discussion........................................................................................................................................ 23 Chapter III Introduction..................................................................................................................................... 35 Materials and methods..................................................................................................................... 38 Results............................................................................................................................................. 44 Discussion........................................................................................................................................ 49 Chapter IV Introduction..................................................................................................................................... 57 Materials and methods..................................................................................................................... 61 Results............................................................................................................................................. 65 Discussion........................................................................................................................................ 68 Chapter V – Summary and outlook 77 Deutsche Zusammenfassung 85 Appendix chapter II 91 Appendix chapter III 113 References 119 Danksagung/ Acknowledgments 137 Chapter I General introduction General introduction Plant-insect interactions are played out in an ecological arena that is larger than the plant itself. Dicke and Takken 2006 In natural ecosystems species interaction play an substantially (Schenk et al. 2008). However, our important role for the dynamics and structure of knowledge of such interacting effects and the communities. Species are continually exposed to a underlying genetic and physiological mechanisms variety of interacting species, both above- and within plants as the central partner and the ecological belowground (Ehrlich & Raven, 1964; Thomson 2009). consequences is still very sketchy (Gehring & Whitham These interactions may have both detrimental (e.g. 2002). Moreover, these interacting effects can not be herbivores, pathogens) as well as beneficial (e.g. expected to be predictable from the separate effects of symbionts) for plant performance. The separate effects single interactors. Consequently, an understanding of of single interacting organisms on plant physiology and the separate and simultaneous influences of these effects performance are known to have important consequences on the plant and their reciprocal interactions is needed. on the performance of plants as well as the dynamics of Interactions between mycorrhizal fungi and populations and communities of plants (for root herbivores symbionts see Smith & Read 2007, van de Heijden & Amongst the most ubiquitous partners are mycorrhizal Sanders 2002). However, several types of interaction fungi and herbivorous insects which are associated with usually simultaneously affect plant growth and virtually all trees. The separate effects of these two physiology under natural conditions. By altering the groups of organisms on plant physiology and plant’s quality and quantity these interactors further performance are known to have important consequences affect each other, resulting in potentially complex for the performance of plants as well as the dynamics of feedback loops (Wardle et al., 2004). Recent evidence populations and communities of plants (e.g., accumulated that the underlying genetic and mycorrhiza: Smith & Read 2007, van de Heijden & physiological pathways induced by and involved in the Sanders 2002; herbivores: Crawley 1997). Moreover, different above- and below-ground interactions overlap insect herbivores and mycorrhizal fungi are known to 3 Chapter I affect each other, resulting in feedback effects on plant moth Lymantria dispar decreased C-allocation to the performance. Firstly, by providing nutrients mycorrhizal root system (Babst et al. 2008). Further, herbivory fungi may increase the vigor and nutritional quality of affects the balance between the important C-pools host plants with positive effects on the performance of starch and soluble sugars in leaf tissue (Babst et al., insect herbivores as well as positive effects on the ability 2005) and roots of trees (Kosola et al., 2002). of the plant to tolerate herbivory (Gehring & Whitham Therefore, herbivory is an important trigger of the C- 1994a, Borowicz 1997, Halldorsson et al. 2000). allocation patterns within plants with possibly Secondly, the resource supply by mycorrhizal fungi may important consequences on feedbacks with other allow plants to increase the investment into resistance associated organisms. However, the importance of against generalist insect herbivores (Jones & Last 1991, herbivory induced changes in allocation patterns for Gange & West, 1994; Bi et al., 2007; Yao et al., 2007). In plant-mycorrhiza symbioses remained unexplored turn, herbivory may importantly feed back on the until now. However, evidence accumulated that this interactions between plants and mycorrhiza. Herbivory stimulation of plant resistance is not only due to the may have a negative effect on mycorrhizal fungi because well-known effects of the mycorrhiza on plant defoliation by herbivores decreases photosynthesis and nutrition, but also to changes in the pathways of therefore the allocation of resources to the mycorrhizal signals that trigger the defence systems (Bi et al., fungi (Smith & Read, 1997; Gehring & Whitham, 2002). 2007; Yao et al., 2007; Pozo & Azcón- Aguilar, 2007). Ectomycorrhizal fungi may use between 10 to 50 % of the Thus, the ability of the plant to use these additional photosynthesis products of host plants (Simard et al., resources made available by mycorrhization for anti- 2002; Hobbie & Hobbie, 2006) and therefore EM fungi herbivore defence determines the direction of the may react very sensitively to herbivory induced changes effects on herbivore performance. Kempel et al. in C-allocation (Markkola et al., 2004; Stark & Kytöviita, (2009) demonstrated a central role of defence 2005). After feeding by herbivores, Frost & Hunter (2008) induction for the outcome of mycorrhiza-herbivore investigated a by 63% decreased allocation of carbon interactions what highlights the importance of belowground in red oak and an increased allocation to signalling pathways within the plant for this tri-partite new foliage. Similarly, herbivory by caterpillars of the relationship. 4 General introduction In addition, soil detritivores alter plant nutrient of secondary compounds like e.g. flavonoide and supply and therefore plant growth performance and isoflavonoide by arbuscular mycorrhizal fungi. Further, vitality. For instance Collembola recycle plant litter the impact of secondary metabolites on insect thereby increasing nutrient availability of plants, but herbivores has been shown by Gange and West (1994), they also alter plant growth via changing plant – who found increased levels of aucubin and catalpol in microbial interactions, in particular that between plants plants of Plantago laureolata inoculated with an and fungi (Chamberlain et al., 2006). Furthermore, arbuscular mycorrhizal fungus. Furthermore, Collembola affect plant performance not only through mycorrhizal colonisation also increases phenolic provisioning of nutrients but also influence their growth contents in Cynara cardunculus (Ceccarelli et al., 2010) and survivability by a number of other indirect Further, indirect defense mechanisms are an mechanisms like grazing on rhizosphere effective way of reducing herbivory (Baldwin et al., microorganisms and modifying the soil structure 2001). Often this involves the induced release of (Scheu, 2001; Gormsen