Stephanie Stiegel MICROCLIMATIC EFFECTS ON CENTRAL EUROPEAN DECIDUOUS TREE SPECIES AND THEIR INTERACTIONS WITH ARTHROPOD HERBIVORY MICROCLIMATIC EFFECTS ON CENTRAL EUROPEAN DECIDUOUS TREE SPECIES AND THEIR INTERACTIONS WITH ARTHROPOD HERBIVORY Stephanie Stiegel Hildesheim 2018 Kumulative Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften (Dr. rer. nat.) (Schwerpunkt Biologie) im Fachbereich 4 – Institut für Biologie und Chemie – Stiftung Universität Hildesheim Vorgelegt von: Stephanie Stiegel (Dipl.-Biol.) Geboren am 17.12.1984 in Dresden Abgabe der Dissertation: 21.06.2018 Tag der mündlichen Prüfung: 24.09.2018 Betreuung: Prof. Jasmin Mantilla-Contreras Prof. Martin H. Entling Gutachten: Prof. Jasmin Mantilla-Contreras Prof. Martin H. Entling Prüfungskommission: Prof. Horst Kierdorf Prof. Jasmin Mantilla-Contreras Prof. Martin H. Entling Dr. Torsten Richter Für Thomas, Jona und Malea Impressum Die Deutsche Natonalbibliothek verzeichnet diese Publikaton in der Deutschen Natonalbibliografe; detaillierte bibliografsche Daten sind im Internet über htp://dnb.d-nb.de abrufar. Diese elektronische Publikaton ist mit der Creatve-Commons-Nutzungslizenz BY-NC-ND 4.0 Internatonal (Namensnennung – Nicht kommerziell – Keine Bearbeitung) versehen. Weitere Informatonen unter: htps://creatvecommons.org/licenses/by-nc-nd/4.0/legalcode.de Universitätsverlag Hildesheim Universitätsplatz 1 31141 Hildesheim htps://www.uni-hildesheim.de/bibliothek/publizieren/open-access-universitaetsverlag/ Erstausgabe Hildesheim 2018 Redakton und Satz: Stephanie Stegel Titelblatgestaltung: Mario Müller, Universitätsverlag Hildesheim Der Beitrag steht als elektronische Publikaton im Internet kostenfrei (Open Access) zur Verfügung: htp://dx.doi.org/10.18442/014 Ziterempfehlung: Stegel, Stephanie (2018). Microclimatc efects on Central European deciduous tree species and their interactons with arthropod herbivory. Hildesheim: Universitätsverlag Hildesheim. E-Publikaton (Open Access) htp://dx.doi.org/10.18442/014 TABLE OF CONTENTS TABLE OF CONTENTS SUMMARY ZUSAMMENFASSUNG 7 GRAPHICAL ABSTRACT 9 CHAPTER 1 11 13 GENERAL INTRODUCTION 1.1 Arthropod herbivory in forest ecosystems 14 1.2 Leaf traits affecting arthropod herbivory 17 1.3 Environmental effects on arthropod herbivory 20 CHAPTER1.4 Research2 question 22 25 METHODOLOGICAL RESEARCH CONCEPTION 2.1 Introduction 26 2.2 Field study 27 CHAPTER2.3 Experimental3 study 30 31 READING THE LEAVES’ PALM: LEAF TRAITS AND HERBIVORY ALONG THE MICROCLIMATIC GRADIENT OF FOREST LAYERS 3.1 Abstract 32 3.2 Introduction 32 3.3 Materials and methods 35 3.4 Results 39 CHAPTER3.5 Discussion4 43 51 ENVIRONMENT VS. PLANT ONTOGENY: ARTHROPOD HERBIVORY PATTERNS ON EUROPEAN BEECH LEAVES ALONG THE VERTICAL GRADIENT OF TEMPERATE FORESTS IN CENTRAL GERMANY 4.1 Abstract 52 4.2 Introduction 52 4.3 Materials and methods 55 3.4 Results 61 4.5 Discussion 67 4.6 Conclusions 70 5 TABLE OF CONTENTS CHAPTER 5 73 EFFECTS OF PHYTODIVERSITY ON INSECT DIVERSITY AND HERBIVORY 5.2 Introduction 74 5.3 Materials and methods 75 5.4 Results 79 CHAPTER5.5 Discussion6 83 87 FAGUS SYLVATICA ACER PSEUDOPLATANUS CARPINUS BETULUS EXPERIMENTAL STUDY OF ENVIRONMENTAL EFFECTS: LEAF TRAITS OF JUVENILE , , AND ARE COMPARABLE TO LEAVES OF MATURE TREES IN UPPER CANOPIES 6.1 Abstract 88 6.2 Introduction 88 6.3 Materials and methods 90 6.4 Results 93 6.5 Discussion 96 CHAPTER6.6 Conclusions7 98 99 SYNOPSIS 7.1 Environmental and plant ontogenetic effects on herbivory along the vertical forest gradient 99 7.2 Explanations for contradictory results on herbivory 107 7.3 Bottom-up and top-down processes affecting herbivory 110 7.4 Importance of herbivory for nature conservation and forestry 116 REFERENCES7.5 Conclusions 119 APPENDICES 121 143 Appendix A 144 Appendix B 145 Appendix C 146 Appendix D 150 Appendix E 166 ACKNOWLEDGEMENTSAppendix F 174 181 6 SUMMARY SUMMARY Arthropod herbivores act as mediators for effects that cascade up and down the trophic chain. Therefore, herbivory plays an important role for driving ecosystem processes and influencing ecosystem structures and functions. Generally, ecosystem processes are mediated by interactions between organisms. The plant community composition is influenced by competitive interactions among plants, which is affected by herbivore species. Leaf area loss to insects can reduce tree growth, but alters material flows from canopies to forest soils. Therefore, the chemical quality of litter is changed (increases in nitrogen content) through enhanced nutrient cycling rates caused by herbivory. Climate and microclimate can affect insect physiology and behaviour directly or indirectly through climate-induced changes of host plants. Temperature determines the geographical range, site and timing of activities, success of oviposition and hatching, and the duration of developmental stages of arthropod herbivores. The activity of poikilothermic insects increases with temperature, and therefore growth and consumption rates are enhanced. However, morphological and functional leaf traits that determine host plant palatability often mediate indirect environmental effects on herbivory. Leaf palatability is determined by leaf toughness, nutrients, and defence compounds. In warm environments, expected high rates of arthropod herbivory can then be suppressed by negative changes of leaf traits. Microclimate gradients are found across the different strata of forest ecosystems. Abiotic factors change vertically between forest layers due to a micro- environmental gradient. Along the vertical gradient, microclimate is affected by the light regime, with increasing temperatures and decreasing humidity from understorey to upper canopies. Various organisms are distributed along the vertical forest gradient based on changes in environmental conditions and in the quality and quantity of available resources. Temperate deciduous forests reveal highly stratified arthropod communities with vertical and horizontal distribution patterns. Microclimatic requirements and the availability of food resources along the vertical forest gradient can reflect spatial distributions and preferences of arthropods. This research study investigated arthropod herbivory on leaves of deciduous tree species along the vertical gradient of temperate forests. A field study with ten forests sites in Central Germany and an experimental study in greenhouses were 7 SUMMARY conducted, addressing effects of microclimate and leaf traits on arthropod herbivory. Juvenile and adult individuals of Fagus sylvatica L. (European beech), the dominant deciduous tree species in Central Europe, were chosen as main research subjects. Furthermore, Acer pseudoplatanus L. (Sycamore maple) and Carpinus betulus L. (hornbeam), two frequent tree species in the forest understorey, were also surveyed. The aim of the study was to detect patterns of herbivory along the vertical forest gradient, and if they are dependent on different feeding guilds like leaf-chewing, sap-sucking, leaf-mining, and gall-inducing. Herbivory patterns were tried to link to microclimate and leaf trait factors. Leaf damaged on F. sylvatica, caused by leaf-chewing insects, decreased from the understorey to upper canopies, along with changes towards unfavourable leaf trait characteristics for insect herbivores (tough leaves, low nitrogen and high carbon content). Changes of leaf traits along the vertical forest gradient were in accordance with effects of the light-induced microclimatic gradient of forest stands. Furthermore, herbivory differences between juvenile tree species in the understorey, with highest levels found on A. pseudoplatanus and C. betulus compared to F. sylvatica, seemed to be in accordance with patterns of defensive traits (indicated by carbon content). In addition, arthropod herbivores also showed variability in their preferences for plant ontogenetic stages, because the distribution of identified feeding traces revealed distinct patterns with differences between juvenile and adult F. sylvatica individuals. Herbivory of gall-inducing species was increased on adult compared to juvenile trees. The distribution of galls is strongly linked to the theory of harsh environment, which is based on top-down control through predation. Further impact on arthropod herbivores was detected for decreasing herbivory with an increase in phytodiversity. In conclusion, the choice of quantitative measure is essential for determining and comparing herbivory, and differs between distinct feeding guilds. Along the vertical forest gradient, herbivory patterns can be linked to environmental and ontogenetic processes, and microclimate essentially affects herbivory intensities, patterns, and processes. Despite direct impacts on arthropod herbivores, the environment influences herbivory through effects on leaf traits and the top-down control by predators. In addition, plant ontogeny affects herbivory indirectly through alterations of leaf traits and top-down processes of predation. 8 ZUSAMMENFASSUNG ZUSAMMENFASSUNG Herbivore Arthropoden fungieren als Mediatoren für Effekte entlang der Nahrungskette (trophische Kaskade). Daher spielt Herbivorie eine wichtige Rolle für die Lenkung von Ökosystemprozessen und beeinflusst Struktur sowie Funktionen von Ökosystemen. Die Zusammensetzung der Pflanzengesellschaft entsteht beispielsweise durch kompetitive Interaktion zwischen Pflanzen, die wiederum von herbivoren Arten beeinflusst wird. Der Blattflächenverlust durch Insekten kann einerseits das Wachstum der Bäume reduzieren. Andererseits verändert