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Between Antagonism and Mutualism Between antagonism and mutualism Costs and benefits in a nursery pollination system Carmen Villacañas de Castro Between antagonism and mutualism Costs and benefits in a nursery pollination system Carmen Villacañas de Castro S UMMARY Thesis Committee Supervisor Prof. Dr. Thomas S. Hoffmeister Population and Evolutionary Ecology Institute of Ecology, University of Bremen Reviewers Prof. Dr. Thomas S. Hoffmeister Prof. Dr. Luis Giménez Benavides Evolutionary Ecology University Rey Juan Carlos (Madrid, Spain) Examination Board Prof. Dr. Thomas S. Hoffmeister Prof. Dr. Martin Diekmann Vegetation Ecology and Conservation Biology Institute of Ecology, University of Bremen Prof. Dr. Christian Wild Marine Ecology University of Bremen Dr. Annette Kolb Hochschule Bremen Inae Kim-Frommherz, University of Bremen Thalea Stuckenberg, University of Bremen Between antagonism and mutualism Costs and benefits in a nursery pollination system Carmen Villacañas de Castro Doctoral Thesis for the attainment of the academic degree Doktor der Naturwissenschaften (Dr. rer. nat.) submitted to the Faculty of Biology and Chemistry at the University of Bremen Bremen, June 2020 Promotionskolloquium am 16. Juli 2020 S UMMARY TABLE OF CONTENTS List of Figures vii List of Tables x SUMMARY Summary in English 13 Summary in German (Zusammenfassung) 16 Summary in Spanish (Resumen) 20 CHAPTER 1: General Introduction 26 CHAPTER 2: Cost/benefit ratio of a nursery pollination system in natural populations: a model application 68 CHAPTER 3: Friend or Foe? A parasitic wasp shifts the cost/benefit ratio in a nursery pollination system impacting plant fitness 106 CHAPTER 4: General Discussion 138 ANNEX Supporting Information 157 List of Image Sources 159 Acknowledgements 162 Declaration of Contribution 167 Affirmation in lieu of oath (Versicherung an Eides Statt) 168 Curriculum Vitae 169 vi S UMMARY LIST OF FIGURES CHAPTER 1 Figure 1 Darwin’s mechanistic model for the coevolution of Angraecum 28 sesquipedale and its pollinator. Figure 2 The interaction grid. 30 Figure 3 Depiction of different examples of interspecific interactions. 31 Figure 4 The interaction compass. 36 Figure 5 A variety of pollination syndromes. 41 Figure 6 Adult Seres rotundus fig wasps emerging from the syconium of a 43 larged-leaved rock fig, Ficus abutilifolia. Figure 7 The Silene latifolia–Hadena bicruris–Bracon variator multitrophic 50 system. Figure 8 Silene latifolia infested seed capsule about to be abscised from the 53 plant. CHAPTER 2 Figure 1 The model system: Silene latifolia–Hadena bicruris–Bracon variator 74 interaction. Figure 2 Experimental set up for the observation assays. 77 Figure 3 Map of the sampling area with the five different populations. 80 Figure 4 Number of visits to male and female Silene latifolia flowers by female 82 and male Hadena bicruris moths. vii Figure 5 Percentage of ovules fertilised by Hadena bicruris male and female 82 moths. Figure 6 Pollination rates of Silene latifolia female flowers, with significant 83 differences between fields. Figure 7 Infestation rates of Silene latifolia female flowers by Hadena bicruris 83 larva, with significant differences among populations. Figure 8 Infestation rates by Hadena bicruris as a function of the number of 84 female Silene latifolia plants in the population, represented by the best fitting line. Figure 9 Parasitism rates of Hadena bicruris larvae by the parasitoid wasp 86 Bracon variator with significant differences between populations. Figure 10 Number of Silene latifolia seeds per infested and intact capsules in 86 different field populations. CHAPTER 3 Figure 1 Hadena bicruris larva at a late developmental stage feeding on a Silene 112 latifolia secondary seed capsule. Figure 2 Seed output per capsule in Silene latifolia plants under different 119 treatments: “control” (negative control, no presence of the larvae and hence no predation), “herbivore” (larva is present and allowed to feed freely on seed capsules) and “herbivore + parasitoid” treatment (the predating larva is attacked by the parasitoid Bracon variator). Figure 3 Total seed output per plant for Silene latifolia plants under different 119 treatments: “control” (negative control, no presence of the larvae and hence no predation), “herbivore” (larva is present and allowed to feed freely on the plant) and “herbivore + parasitoid” (treatment, the predating larva is attacked by the parasitoid Bracon variator). viii Figure 4 Early germination for Silene latifolia seeds under different treatments: 120 “control” (seeds from capsules from pollinated plants without herbivore attack), “damaged” (seeds from damaged capsules from plants with herbivore attack) and “undamaged” (seeds from undamaged capsules from plants with herbivore attack). Figure 5 Germination (a) and survival (b) probability of Silene latifolia plants as 122 a function of initial seed density, represented by the best fitting lines. Figure 6 Total flower anthesis per plant in Silene latifolia as a function of initial 123 seed density and sex, represented by the best fitting lines. CHAPTER 4 Figure 1 Conceptual diagram of the Silene latifolia–Hadena bicruris system. 144 SUPPORTING INFORMATION Figure S1 Proportion of undamaged capsules for Silene latifolia plants as a 156 function of treatment: “herbivore” (control, larva is present and allowed to feed freely on seed capsules) and “herbivore + parasitoid” treatment (the predating larva is attacked by the parasitoid Bracon variator). Figure S2 Mean weight of seeds in Silene latifolia capsules under different 161 treatments: “control” (negative control, no presence of the larvae and hence no predation), “herbivore” (control, larva is present and allowed to feed freely on seed capsules) and “herbivore + parasitoid” treatment (the predating larva is attacked by the parasitoid Bracon variator). Figure S3 Total seed output per plant for Silene latifolia plants as a function of 161 treatment and total number of capsules produced, represented by the best fitting lines. ix LIST OF TABLES CHAPTER 2 Table 1 Description of the parameters from the model. 72 Table 2 Description of the behaviours recorded in the observation essays. 78 Table 3 Paired samples t-tests for differences in pollination rates between all 87 fields, with a “Benjamini–Hochberg” adjustment method. Table 4 Paired samples t-tests for differences in infestation rates between all 87 fields, with a “Benjamini–Hochberg” adjustment method. Table 5 Paired samples t-tests for differences in parasitism rates by the 88 parasitoid between all fields, with a “Benjamini–Hochberg” adjustment method. Table 6 Bonferroni-adjusted pairwise comparisons for the number of seeds per 88 capsule with the interaction term field*status. Table 7 Direct observations of Hadena bicruris activity behaviour. 89 Table 8 Data collected from field populations. Number of flowers/capsules 89 infested with Hadena bicruris, intact flowers/capsules, and the total flowers/capsules found in the population. Table 9 Data collected from field populations. Number of Hadena bicruris larvae 90 that died at a young stage and number of infested flowers/capsules found in the population. Table 10 Model parameters calculated for the different field populations. 90 Table 11 Model outcome calculated for the different field populations. 92 CHAPTER 3 Table 1 Contrast tests following the close test principal for seed output per 118 capsule between all pairs of categories. x S UMMARY SUMMARY 12 SUMMARY SUMMARY A hundred years after Darwin predicted the existence of a specific hawkmoth that could drink the nectar and pollinate the Malagasy star orchid, coevolution was defined as “an evolutionary change in a trait of the individuals in one population in response to a trait of the individuals of a second population, followed by an evolutionary response by the second population to the change in the first”. Since then, the demonstration that adaptations in both partner species are a result of reciprocal selection became a requirement to associate a certain pattern to coevolution. These relationships between species are dynamic and continually evolve as natural selection reshapes them. In this way, natural selection and coevolution have led to different types of interactions between species, depending on the effects on fitness of the partners involved. When the net effect is negative to one or both partners the relationship is an antagonism. Antagonisms are diverse and include predation and parasitism, among others. In commensalistic interactions, one species benefits and the other remains unaffected, while in mutualistic interactions both species benefit. Mutualisms vary greatly in the degree of obligacy and specificity, even between mutualistic partners. The study of mutualisms has gained popularity among ecologists, and they are now recognised as providing essential ecosystem services. Several ecological and evolutionary patterns that are shared between diverse forms of mutualisms have been identified. First of all, one of the partners performs a service that benefits its associate, and in turn it receives a reward. However, services provided and rewards produced can also be costly. Hence, natural selection will favour traits that minimise such costs without interfering with the mutualism itself. As long as the benefits outweigh the costs, the association will last. The second pattern observed is conditionality: a change in the outcome of the interaction as a result of variations in the given local biotic or abiotic conditions. Such variation can
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