Context Dependency of Community Dynamics: Predator-Prey Interactions Under Ecological Disturbances

Numerous studies have focused on the drivers of diversity and stability of communities, especially under global change. However, multi-dimensionality of ecosystems due to biotic components (e.g predation, competition and adaptive dynamics) and abiotic factors (e.g. disturbances, resource dynamics and their distinct attributes) cause context-dependent outcomes and challenge the predictions. There are still controversies around complex community dynamics under varying regimes, however, finding mechanistical explanations will illuminate the fate of multispecies assemblages. Using model microbial communities, consisting of bacterial prey and protist predator, combined with simulation modelling and advanced statistics, this thesis investigated the impact of imposed disturbances (i.e. increased dilution rates that simulate density-independent mortality as press or pulse disturbances) (i) on transient recovery dynamics of a simple microbial food web, and (ii) on bacterial abundance, diversity and community structure in the absence or presence of a protist predator. In addition, this thesis questioned the impacts of species interactions and rapid trait shifts, as a response to predation and competition, on the community dynamics and stability. Our results revealed that the predator suffered more from disturbances over longer time periods. Reduced predation pressure caused a transient phase of prey release during and even after disturbances. Recovery time depended on the strength and duration of disturbances, however, coupling to an alternative resource increased the chance of fast recovery and stabilized the communities. In multi-species prey communities, bacterial abundance, diversity, and community composition were more affected by predation than by the disturbances and resource dynamics. Predator abundance, on the other hand, was strongly affected by the type of disturbance imposed. Importantly, community attributes had differential sensitivities, as reflected by their different response and recovery dynamics. Prey community dynamics varied more temporally andwere less stable under predation stress, while prey diversity increased significantly. Predation rapidly induced anti-predation traits, which altered population dynamics of both prey and predator. More importantly, predator and the resistant prey, in turn, elevated the number of direct cause-effect relationships between the community members. Our findings are not limited to the studied system and can be used to understand the dynamic response and recovery potential of many natural predator-prey or host-pathogen systems. They can be used as a base for future studies to illuminate the debates on the future communities.:Summary Zusammenfassung 1 Scope and Outline 2 General Introduction 2.1 Context dependency of community dynamics 2.2 Ecological disturbances 2.2.1 Transient dynamics and stability 2.2.2 Catastrophic shifts 2.3 Species interactions and evolutionary dynamics under environmental change 2.3.1 Species interactions and coexistence 2.4 Eco-evolutionary dynamics 2.5 Community assembly mechanisms 2.6 Dealing with complexities 2.6.1 Microbial model systems as a tool in ecology 2.6.2 Correlation, causation and the future of predictions 2.7 Aims of this study 3 Community Dynamics under Disturbances 3.1 Transient recovery dynamics of a predator-prey system 4 Interactions of Community Drivers 4.1 Interactions between predation and disturbances shape prey communities 5 Species Interactions and Evolutionary Dynamics Shaping Communities 5.1 Summary 5.2 Introduction 5.2.1 Predator-Prey Dynamics and Community Stability 5.2.2 Causal inferences 5.3 Aim of the study 5.4 Methods 5.4.1 Organisms 5.4.2 Microcosm experiments and estimation of species abundances 5.4.3 Statistical analysis 5.5 Results 5.5.1 Community dynamics 5.5.2 Dynamics of prey diversity and community stability 5.5.3 Causal links between the species dynamics 5.6 Discussion 5.7 Synopsis 6 General Discussion 6.1 Communities under disturbances: Predator{ prey dynamics 6.2 Temporal species dynamics and community assembly Synthesis and Outlook 7.1 Increasing complexity of species interactions 7.2 Going further from causal links 7.3 Metacommunities References 8 Appendix 8.1 Declaration of the authorship 8.2 Author contributions of published articles 8.3 List of publications and conference contributions 8.4 Acknowledgments 8.5 Supplementary material for Chapter 3 8.6 Supplementary material for Chapter 4 8.7 Supplementary material for Chapter

Mining Synergistic Microbial Interactions: A Roadmap on How to Integrate Multi-Omics Data

Mining interspecies interactions remain a challenge due to the complex nature of microbial communities and the need for computational power to handle big data. Our meta-analysis indicates that genetic potential alone does not resolve all issues involving mining of microbial interactions. Nevertheless, it can be used as the starting point to infer synergistic interspecies interactions and to limit the search space (i.e., number of species and metabolic reactions) to a manageable size. A reduced search space decreases the number of additional experiments necessary to validate the inferred putative interactions. As validation experiments, we examine how multi-omics and state of the art imaging techniques may further improve our understanding of species interactions’ role in ecosystem processes. Finally, we analyze pros and cons from the current methods to infer microbial interactions from genetic potential and propose a new theoretical framework based on: (i) genomic information of key members of a community; (ii) information of ecosystem processes involved with a specific hypothesis or research question; (iii) the ability to identify putative species’ contributions to ecosystem processes of interest; and, (iv) validation of putative microbial interactions through integration of other data sources

Context Dependency of Community Dynamics: Predator-Prey Interactions Under Ecological Disturbances

Numerous studies have focused on the drivers of diversity and stability of communities, especially under global change. However, multi-dimensionality of ecosystems due to biotic components (e.g predation, competition and adaptive dynamics) and abiotic factors (e.g. disturbances, resource dynamics and their distinct attributes) cause context-dependent outcomes and challenge the predictions. There are still controversies around complex community dynamics under varying regimes, however, finding mechanistical explanations will illuminate the fate of multispecies assemblages. Using model microbial communities, consisting of bacterial prey and protist predator, combined with simulation modelling and advanced statistics, this thesis investigated the impact of imposed disturbances (i.e. increased dilution rates that simulate density-independent mortality as press or pulse disturbances) (i) on transient recovery dynamics of a simple microbial food web, and (ii) on bacterial abundance, diversity and community structure in the absence or presence of a protist predator. In addition, this thesis questioned the impacts of species interactions and rapid trait shifts, as a response to predation and competition, on the community dynamics and stability. Our results revealed that the predator suffered more from disturbances over longer time periods. Reduced predation pressure caused a transient phase of prey release during and even after disturbances. Recovery time depended on the strength and duration of disturbances, however, coupling to an alternative resource increased the chance of fast recovery and stabilized the communities. In multi-species prey communities, bacterial abundance, diversity, and community composition were more affected by predation than by the disturbances and resource dynamics. Predator abundance, on the other hand, was strongly affected by the type of disturbance imposed. Importantly, community attributes had differential sensitivities, as reflected by their different response and recovery dynamics. Prey community dynamics varied more temporally andwere less stable under predation stress, while prey diversity increased significantly. Predation rapidly induced anti-predation traits, which altered population dynamics of both prey and predator. More importantly, predator and the resistant prey, in turn, elevated the number of direct cause-effect relationships between the community members. Our findings are not limited to the studied system and can be used to understand the dynamic response and recovery potential of many natural predator-prey or host-pathogen systems. They can be used as a base for future studies to illuminate the debates on the future communities.:Summary Zusammenfassung 1 Scope and Outline 2 General Introduction 2.1 Context dependency of community dynamics 2.2 Ecological disturbances 2.2.1 Transient dynamics and stability 2.2.2 Catastrophic shifts 2.3 Species interactions and evolutionary dynamics under environmental change 2.3.1 Species interactions and coexistence 2.4 Eco-evolutionary dynamics 2.5 Community assembly mechanisms 2.6 Dealing with complexities 2.6.1 Microbial model systems as a tool in ecology 2.6.2 Correlation, causation and the future of predictions 2.7 Aims of this study 3 Community Dynamics under Disturbances 3.1 Transient recovery dynamics of a predator-prey system 4 Interactions of Community Drivers 4.1 Interactions between predation and disturbances shape prey communities 5 Species Interactions and Evolutionary Dynamics Shaping Communities 5.1 Summary 5.2 Introduction 5.2.1 Predator-Prey Dynamics and Community Stability 5.2.2 Causal inferences 5.3 Aim of the study 5.4 Methods 5.4.1 Organisms 5.4.2 Microcosm experiments and estimation of species abundances 5.4.3 Statistical analysis 5.5 Results 5.5.1 Community dynamics 5.5.2 Dynamics of prey diversity and community stability 5.5.3 Causal links between the species dynamics 5.6 Discussion 5.7 Synopsis 6 General Discussion 6.1 Communities under disturbances: Predator{ prey dynamics 6.2 Temporal species dynamics and community assembly Synthesis and Outlook 7.1 Increasing complexity of species interactions 7.2 Going further from causal links 7.3 Metacommunities References 8 Appendix 8.1 Declaration of the authorship 8.2 Author contributions of published articles 8.3 List of publications and conference contributions 8.4 Acknowledgments 8.5 Supplementary material for Chapter 3 8.6 Supplementary material for Chapter 4 8.7 Supplementary material for Chapter

Interactions between predation and disturbances shape prey communities

Abstract Ecological disturbances are important drivers of biodiversity patterns. Many biodiversity studies rely on endpoint measurements instead of following the dynamics that lead to those outcomes and testing ecological drivers individually, often considering only a single trophic level. Manipulating multiple factors (biotic and abiotic) in controlled settings and measuring multiple descriptors of multi-trophic communities could enlighten our understanding of the context dependency of ecological disturbances. Using model microbial communities, we experimentally tested the effects of imposed disturbances (i.e. increased dilution simulating density-independent mortality as press or pulse disturbances coupled with resource deprivation) on bacterial abundance, diversity and community structure in the absence or presence of a protist predator. We monitored the communities immediately before and after imposing the disturbance and four days after resuming the pre-disturbance dilution regime to infer resistance and recovery properties. The results highlight that bacterial abundance, diversity and community composition were more affected by predation than by disturbance type, resource loss or the interaction of these factors. Predator abundance was strongly affected by the type of disturbance imposed, causing temporary relief of predation pressure. Importantly, prey community composition differed significantly at different phases, emphasizing that endpoint measurements are insufficient for understanding the recovery of communities

Measuring stability in ecological systems without static equilibria

Abstract Ecological stability refers to a range of concepts used to quantify how species and environments change over time and in response to disturbances. Most empirically tractable ecological stability metrics assume that systems have simple dynamics and static equilibria. However, ecological systems are typically complex and often lack static equilibria (e.g., predator–prey oscillations, transient dynamics, chaos). Failing to account for these factors can lead to biased estimates of stability, in particular, by conflating effects of observation error, process noise, and underlying deterministic dynamics. To distinguish among these processes, we combine three existing approaches: state space models; delay embedding methods; and particle filtering. Jointly, these provide something akin to a deterministically “detrended” version of the coefficient of variation, separately tracking variability due to deterministic dynamics versus stochastic perturbations. Moreover, these variability estimates can be used to forecast dynamics, classify underlying sources of stochastic dynamics, and estimate the “exit time” before a state change takes place (e.g., local extinction events). Importantly, the time‐delay embedding methods that we employ make very few assumptions about the functions governing deterministic dynamics, which facilitates applications in systems with limited data and a priori biological knowledge. To demonstrate how complex dynamics without static equilibria can bias ecological stability estimates, we analyze simulated time series of abundance dynamics in a system with time‐varying carrying capacity and empirically observed abundance dynamics of the green algae Chlamydomonas terricola grown in a diverse microcosm mixture under variable temperature conditions. We show that stability estimates based on raw observations greatly overestimate temporal variability and fail to accurately forecast time to extinction. In contrast, joint application of state space modeling, delay embedding, and particle filters were able to: (1) correctly quantify the contributions of deterministic versus stochastic variability; (2) successfully estimate “true” abundance dynamics; and (3) correctly forecast time to extinction. Our results therefore demonstrate the importance of accounting for effects of complex, nonstatic dynamics in studies of ecological stability and provide an empirically tractable and flexible toolkit for conducting these measurements

Growth Curves

Cell counts [cells/ml] of Escherichia coli JM109 (prey) and Tetrahymena pyriformis (predator) within 24 hours in monocultures and in combination

Data from: Transient recovery dynamics of a predator–prey system under press and pulse disturbances

Background: Species recovery after disturbances depends on the strength and duration of disturbance, on the species traits and on the biotic interactions with other species. In order to understand these complex relationships, it is essential to understand mechanistically the transient dynamics of interacting species during and after disturbances. We combined microcosm experiments with simulation modelling and studied the transient recovery dynamics of a simple microbial food web under pulse and press disturbances and under different predator couplings to an alternative resource. Results: Our results reveal that although the disturbances affected predator and prey populations by the same mortality, predator populations suffered for a longer time. The resulting diminished predation stress caused a temporary phase of high prey population sizes (i.e. prey release) during and even after disturbances. Increasing duration and strength of disturbances significantly slowed down the recovery time of the predator prolonging the phase of prey release. However, the additional coupling of the predator to an alternative resource allowed the predator to recover faster after the disturbances thus shortening the phase of prey release. Conclusions: Our findings are not limited to the studied system and can be used to understand the dynamic response and recovery potential of many natural predator–prey or host–pathogen systems. They can be applied, for instance, in epidemiological and conservational contexts to regulate prey release or to avoid extinction risk of the top trophic levels under different types of disturbances

Transient recovery dynamics of a predator–prey system under press and pulse disturbances

Abstract Background Species recovery after disturbances depends on the strength and duration of disturbance, on the species traits and on the biotic interactions with other species. In order to understand these complex relationships, it is essential to understand mechanistically the transient dynamics of interacting species during and after disturbances. We combined microcosm experiments with simulation modelling and studied the transient recovery dynamics of a simple microbial food web under pulse and press disturbances and under different predator couplings to an alternative resource. Results Our results reveal that although the disturbances affected predator and prey populations by the same mortality, predator populations suffered for a longer time. The resulting diminished predation stress caused a temporary phase of high prey population sizes (i.e. prey release) during and even after disturbances. Increasing duration and strength of disturbances significantly slowed down the recovery time of the predator prolonging the phase of prey release. However, the additional coupling of the predator to an alternative resource allowed the predator to recover faster after the disturbances thus shortening the phase of prey release. Conclusions Our findings are not limited to the studied system and can be used to understand the dynamic response and recovery potential of many natural predator–prey or host–pathogen systems. They can be applied, for instance, in epidemiological and conservational contexts to regulate prey release or to avoid extinction risk of the top trophic levels under different types of disturbances

Disturbance treatments

Cell counts of E. coli JM109 (prey) and Tetrahymena pyriformis (predator) in three experimental treatments: Undisturbed (control), press and pulse disturbance. All treatments were replicated three times