Environmental fluctuations restrict eco-evolutionary dynamics in predator–prey system

Environmental fluctuations, species interactions and rapid evolution are all predicted to affect community structure and their temporal dynamics. Although the effects of the abiotic environment and prey evolution on ecological community dynamics have been studied separately, these factors can also have interactive effects. Here we used bacteria–ciliate microcosm experiments to test for eco-evolutionary dynamics in fluctuating environments. Specifically, we followed population dynamics and a prey defence trait over time when populations were exposed to regular changes of bottom-up or top-down stressors, or combinations of these. We found that the rate of evolution of a defence trait was significantly lower in fluctuating compared with stable environments, and that the defence trait evolved to lower levels when two environmental stressors changed recurrently. The latter suggests that top-down and bottom-up changes can have additive effects constraining evolutionary response within populations. The differences in evolutionary trajectories are explained by fluctuations in population sizes of the prey and the predator, which continuously alter the supply of mutations in the prey and strength of selection through predation. Thus, it may be necessary to adopt an eco-evolutionary perspective on studies concerning the evolution of traits mediating species interactions.     

Impacts of predator-mediated interactions along a climatic gradient on the population dynamics of an alpine bird

According to classic theory, species'' population dynamics and distributions are less influenced by species interactions under harsh climatic conditions compared to under more benign climatic conditions. In alpine and boreal ecosystems in Fennoscandia, the cyclic dynamics of rodents strongly affect many other species, including ground-nesting birds such as ptarmigan. According to the ‘alternative prey hypothesis’ (APH), the densities of ground-nesting birds and rodents are positively associated due to predator–prey dynamics and prey-switching. However, it remains unclear how the strength of these predator-mediated interactions change along a climatic harshness gradient in comparison with the effects of climatic variation. We built a hierarchical Bayesian model to estimate the sensitivity of ptarmigan populations to interannual variation in climate and rodent occurrence across Norway during 2007–2017. Ptarmigan abundance was positively linked with rodent occurrence, consistent with the APH. Moreover, we found that the link between ptarmigan abundance and rodent dynamics was strongest in colder regions. Our study highlights how species interactions play an important role in population dynamics of species at high latitudes and suggests that they can become even more important in the most climatically harsh regions.     

Rapid prey evolution and the dynamics of two-predator food webs

Traits affecting ecological interactions can evolve on the same time scale as population and community dynamics, creating the potential for feedbacks between evolutionary and ecological dynamics. Theory and experiments have shown in particular that rapid evolution of traits conferring defense against predation can radically change the qualitative dynamics of a predator–prey food chain. Here, we ask whether such dramatic effects are likely to be seen in more complex food webs having two predators rather than one, or whether the greater complexity of the ecological interactions will mask any potential impacts of rapid evolution. If one prey genotype can be well-defended against both predators, the dynamics are like those of a predator–prey food chain. But if defense traits are predator-specific and incompatible, so that each genotype is vulnerable to attack by at least one predator, then rapid evolution produces distinctive behaviors at the population level: population typically oscillate in ways very different from either the food chain or a two-predator food web without rapid prey evolution. When many prey genotypes coexist, chaotic dynamics become likely. The effects of rapid evolution can still be detected by analyzing relationships between prey abundance and predator population growth rates using methods from functional data analysis.     

Mixed interactions among life history stages of two harvested related species

Climate change and harvesting can affect the ecosystems'' functioning by altering the population dynamics and interactions among species. Knowing how species interact is essential for better understanding potentially unintended consequences of harvest on multiple species in ecosystems. I analyzed how stage‐specific interactions between two harvested competitors, the haddock (Melanogrammus aeglefinus) and Atlantic cod (Gadus morhua), living in the Barents Sea affect the outcome of changes in the harvest of the two species. Using state‐space models that account for observation errors and stochasticity in the population dynamics, I run different harvesting scenarios and track population‐level responses of both species. The increasing temperature elevated the number of larvae of haddock but did not significantly influence the older age‐classes. The nature of the interactions between both species shifted from predator‐prey to competition around age‐2 to ‐3. Increased cod fishing mortality, which led to decreasing abundance of cod, was associated with an increasing overall abundance of haddock, which suggests compensatory dynamics of both species. From a stage‐specific approach, I show that a change in the abundance in one species may propagate to other species, threatening the exploited species'' recovery. Thus, this study demonstrates that considering interactions among life history stages of harvested species is essential to enhance species'' co‐existence in harvested ecosystems. The approach developed in this study steps forward the analyses of effects of harvest and climate in multi‐species systems by considering the comprehension of complex ecological processes to facilitate the sustainable use of natural resources.     

Community structure and stability analysis for intraguild interactions among host, parasitoid, and predator

Intraguild predation (IGP) occurs when one species preys on a competitor species that shares a common resource. Modifying a prey–predator model with prey infection, we propose a model of IG interactions among host, parasitoid, and predator, in which the predator eats parasitized and unparasitized hosts, and the adult parasitoid density is explicitly expressed. Parameter dependences of community structure, including stability of the system, were analytically obtained. Depending on interaction strength (parasitization and predation on unparasitized and parasitized hosts), the model provides six types of community structure: (1) only the host exists, (2) the host and predator coexist stably, (3) the host and parasitoid coexist stably, (4) the host–parasitoid population dynamics are unstable, (5) the three species coexist stably, and (6) the population dynamics of the three species are unstable. In contrast to a traditional prey–predator model with prey infection, which predicts that population dynamics are always locally stable, our model predicts that they are unstable when the parasitization rate is high.     

Eco-evolutionary feedbacks drive species interactions

In the biosphere, many species live in close proximity and can thus interact in many different ways. Such interactions are dynamic and fall along a continuum between antagonism and cooperation. Because interspecies interactions are the key to understanding biological communities, it is important to know how species interactions arise and evolve. Here, we show that the feedback between ecological and evolutionary processes has a fundamental role in the emergence and dynamics of species interaction. Using a two-species artificial community, we demonstrate that ecological processes and rapid evolution interact to influence the dynamics of the symbiosis between a eukaryote (Saccharomyces cerevisiae) and a bacterium (Rhizobium etli). The simplicity of our experimental design enables an explicit statement of causality. The niche-constructing activities of the fungus were the key ecological process: it allowed the establishment of a commensal relationship that switched to ammensalism and provided the selective conditions necessary for the adaptive evolution of the bacteria. In this latter state, the bacterial population radiates into more than five genotypes that vary with respect to nutrient transport, metabolic strategies and global regulation. Evolutionary diversification of the bacterial populations has strong effects on the community; the nature of interaction subsequently switches from ammensalism to antagonism where bacteria promote yeast extinction. Our results demonstrate the importance of the evolution-to-ecology pathway in the persistence of interactions and the stability of communities. Thus, eco-evolutionary dynamics have the potential to transform the structure and functioning of ecosystems. Our results suggest that these dynamics should be considered to improve our understanding of beneficial and detrimental host–microbe interactions.     

The interaction between plant competition and disease

It is well documented that pathogens can affect the survival, reproduction, and growth of individual plants. Drawing together insights from diverse studies in ecology and agriculture, we evaluate the evidence for pathogens affecting competitive interactions between plants of both the same and different species. Our objective is to explore the potential ecological and evolutionary consequences of such interactions. First, we address how disease interacts with intraspecific competition and present a simple graphical model suggesting that diverse outcomes should be expected. We conclude that the presence of pathogens may have either large or minimal effects on population dynamics depending on many factors including the density-dependent compensatory ability of healthy plants and spatial patterns of infection. Second, we consider how disease can alter competitive abilities of genotypes, and thus may affect the genetic composition of populations. These genetic processes feed back on population dynamics given trade-offs between disease resistance and other fitness components. Third, we examine how the effect of disease on interspecific plant interactions may have potentially far-reaching effects on community composition. A host-specific pathogen, for example, may alter a competitive hierarchy that exists between host and non-host species. Generalist pathogens can also induce indirect competitive interactions between host species. We conclude by highlighting lacunae in our current understanding and suggest that future studies should (1) examine a broader taxonomic range of pathogens since work to date has largely focused on fungal pathogens; (2) increase the use of field competition studies; (3) follow interactions for multiple generations; (4) characterize density-dependent processes; and (5) quantify pathogen, as well as plant, population and community dynamics.     

Adaptive foraging behaviour of individual pollinators and the coexistence of co-flowering plants

Although pollinators can play a central role in determining the structure and stability of plant communities, little is known about how their adaptive foraging behaviours at the individual level, e.g. flower constancy, structure these interactions. Here, we construct a mathematical model that integrates individual adaptive foraging behaviour and population dynamics of a community consisting of two plant species and a pollinator species. We find that adaptive foraging at the individual level, as a complementary mechanism to adaptive foraging at the species level, can further enhance the coexistence of plant species through niche partitioning between conspecific pollinators. The stabilizing effect is stronger than that of unbiased generalists when there is also strong competition between plant species over other resources, but less so than that of multiple specialist species. This suggests that adaptive foraging in mutualistic interactions can have a very different impact on the plant community structure from that in predator–prey interactions. In addition, the adaptive behaviour of individual pollinators may cause a sharp regime shift for invading plant species. These results indicate the importance of integrating individual adaptive behaviour and population dynamics for the conservation of native plant communities.     

Adaptive genetic variation mediates bottom-up and top-down control in an aquatic ecosystem

Research in eco-evolutionary dynamics and community genetics has demonstrated that variation within a species can have strong impacts on associated communities and ecosystem processes. Yet, these studies have centred around individual focal species and at single trophic levels, ignoring the role of phenotypic variation in multiple taxa within an ecosystem. Given the ubiquitous nature of local adaptation, and thus intraspecific variation, we sought to understand how combinations of intraspecific variation in multiple species within an ecosystem impacts its ecology. Using two species that co-occur and demonstrate adaptation to their natal environments, black cottonwood (Populus trichocarpa) and three-spined stickleback (Gasterosteus aculeatus), we investigated the effects of intraspecific phenotypic variation on both top-down and bottom-up forces using a large-scale aquatic mesocosm experiment. Black cottonwood genotypes exhibit genetic variation in their productivity and consequently their leaf litter subsidies to the aquatic system, which mediates the strength of top-down effects from stickleback on prey abundances. Abundances of four common invertebrate prey species and available phosphorous, the most critically limiting nutrient in freshwater systems, are dictated by the interaction between genetic variation in cottonwood productivity and stickleback morphology. These interactive effects fit with ecological theory on the relationship between productivity and top-down control and are comparable in strength to the effects of predator addition. Our results illustrate that intraspecific variation, which can evolve rapidly, is an under-appreciated driver of community structure and ecosystem function, demonstrating that a multi-trophic perspective is essential to understanding the role of evolution in structuring ecological patterns.     

Revealing the role of predator interference in a predator–prey system with disease in prey population

Predation on a species subjected to an infectious disease can affect both the infection level and the population dynamics. There is an ongoing debate about the act of managing disease in natural populations through predation. Recent theoretical and empirical evidence shows that predation on infected populations can have both positive and negative influences on disease in prey populations. Here, we present a predator–prey system where the prey population is subjected to an infectious disease to explore the impact of predator on disease dynamics. Specifically, we investigate how the interference among predators affects the dynamics and structure of the predator–prey community. We perform a detailed numerical bifurcation analysis and find an unusually large variety of complex dynamics, such as, bistability, torus and chaos, in the presence of predators. We show that, depending on the strength of interference among predators, predators enhance or control disease outbreaks and population persistence. Moreover, the presence of multistable regimes makes the system very sensitive to perturbations and facilitates a number of regime shifts. Since, the habitat structure and the choice of predators deeply influence the interference among predators, thus before applying predators to control disease in prey populations or applying predator control strategy for wildlife management, it is essential to carefully investigate how these predators interact with each other in that specific habitat; otherwise it may lead to ecological disaster.     

Effects of epibiosis on consumer–prey interactions

In many benthic communities predators play a crucialrole in the population dynamics of their prey. Surfacecharacteristics of the prey are important forrecognition and handling by the predator. Because theestablishment of an epibiotic assemblage on thesurface of a basibiont species creates a new interfacebetween the epibiotized organism and its environment,we hypothesised that epibiosis should have an impacton consumer–prey interactions. In separateinvestigations, we assessed how epibionts onmacroalgae affected the susceptibility of the latterto herbivory by the urchin Arbacia punctulataand how epibionts on the blue mussel Mytilusedulis affected its susceptibility to predation bythe shore crab Carcinus maenas.Some epibionts strongly affected consumer feedingbehavior. When epibionts were more attractive thantheir host, consumer pressure increased. Whenepibionts were less attractive than their host or whenthey were repellent, consumer pressure decreased. Insystems that are controlled from the top-down,epibiosis can strongly influence community dynamics.For the Carcinus/Mytilus system that westudied, the in situ distribution of epibiontson mussels reflected the epibiosis-determinedpreferences of the predator. Both direct and indirecteffects are involved in determining theseepibiont-prey–consumer interactions.     

When phenology matters: age–size truncation alters population response to trophic mismatch

Climate-induced shifts in the timing of life-history events are a worldwide phenomenon, and these shifts can de-synchronize species interactions such as predator–prey relationships. In order to understand the ecological implications of altered seasonality, we need to consider how shifts in phenology interact with other agents of environmental change such as exploitation and disease spread, which commonly act to erode the demographic structure of wild populations. Using long-term observational data on the phenology and dynamics of a model predator–prey system (fish and zooplankton in Windermere, UK), we show that age–size truncation of the predator population alters the consequences of phenological mismatch for offspring survival and population abundance. Specifically, age–size truncation reduces intraspecific density regulation due to competition and cannibalism, and thereby amplifies the population sensitivity to climate-induced predator–prey asynchrony, which increases variability in predator abundance. High population variability poses major ecological and economic challenges as it can diminish sustainable harvest rates and increase the risk of population collapse. Our results stress the importance of maintaining within-population age–size diversity in order to buffer populations against phenological asynchrony, and highlight the need to consider interactive effects of environmental impacts if we are to understand and project complex ecological outcomes.     

Sensory-based niche partitioning in a multiple predator–multiple prey community

Many predators and parasites eavesdrop on the communication signals of their prey. Eavesdropping is typically studied as dyadic predator–prey species interactions; yet in nature, most predators target multiple prey species and most prey must evade multiple predator species. The impact of predator communities on prey signal evolution is not well understood. Predators could converge in their preferences for conspicuous signal properties, generating competition among predators and natural selection on particular prey signal features. Alternatively, predator species could vary in their preferences for prey signal properties, resulting in sensory-based niche partitioning of prey resources. In the Neotropics, many substrate-gleaning bats use the mate-attraction songs of male katydids to locate them as prey. We studied mechanisms of niche partitioning in four substrate-gleaning bat species and found they are similar in morphology, echolocation signal design and prey-handling ability, but each species preferred different acoustic features of male song in 12 sympatric katydid species. This divergence in predator preference probably contributes to the coexistence of many substrate-gleaning bat species in the Neotropics, and the substantial diversity in the mate-attraction signals of katydids. Our results provide insight into how multiple eavesdropping predator species might influence prey signal evolution through sensory-based niche partitioning.     

The effect of dilution on eco‐evolutionary dynamics of experimental microbial communities

Changing environmental conditions can infer structural modifications of predator‐prey communities. New conditions often increase mortality which reduces population sizes. Following this, predation pressure may decrease until populations are dense again. Dilution may thus have substantial impact not only on ecological but also on evolutionary dynamics because it amends population densities. Experimental studies, in which microbial populations are maintained by a repeated dilution into fresh conditions after a certain period, are extensively used approaches allowing us to obtain mechanistic insights into fundamental processes. By design, dilution, which depends on transfer volume (modifying mortality) and transfer interval (determining the time of interaction), is an inherent feature of these experiments, but often receives little attention. We further explore previously published data from a live predator‐prey (bacteria and ciliates) system which investigated eco‐evolutionary principles and apply a mathematical model to predict how various transfer volumes and transfer intervals would affect such an experiment. We find not only the ecological dynamics to be modified by both factors but also the evolutionary rates to be affected. Our work predicts that the evolution of the anti‐predator defense in the bacteria, and the evolution of the predation efficiency in the ciliates, both slow down with lower transfer volume, but speed up with longer transfer intervals. Our results provide testable hypotheses for future studies of predator‐prey systems, and we hope this work will help improve our understanding of how ecological and evolutionary processes together shape composition of microbial communities.     

Are multiple predator effects directed by prey availability?

Antagonistic/synergistic interactions among predators foraging on the same prey have been assumed to play a major role in shaping community structure. Studies in systems with multiple predator species have shown that the strength of these interactions may not be predictable and is largely dependent on individual behavioural traits, species density and habitat complexity. Although the association of prey consumption and satiation of a foraging predator has long been recognized, there has been relatively little research on how prey availability affects multiple predators’ effects. In this work, we present a framework to investigate the variation in two coexisting/competing predators’ effects on prey risk as affected by the prey availability rate. Functional responses by each predator species were first studied in single-predator treatments. Then, the intra- and inter-specific competition was investigated by employing additive and substitutative experimental designs to highlight the nature of multiple effects. Intra- and interspecific interactions were found to be similar and there was risk reduction, and risk enhancement for the prey at intermediate and high levels, respectively, according to the multiplicative risk model (MRM). The results indicated that when similar predators are concerned, the outcomes of MRM may vary according to the functional response curve of these predators. Thus, studies involving a wide range of prey densities are required to explore the nature of interactions. Moreover, this kind of experimental data can contribute to unravelling complexities in theoretical approaches by earlier studies and ultimately promote understanding the effect of multiple predators on prey population regulation.     

The long‐term impacts of predators on prey: inducible defenses,population dynamics,and indirect effects

Despite the amount of research on the inducible defenses of prey against predators, our understanding of the long‐term significance of non‐lethal predators on prey phenotypes, prey population dynamics, and community structure has rarely been explored. Our objectives were to assess the effects of predators on prey defenses, prey population dynamics, and the relative magnitude of density‐ versus trait‐mediated indirect interactions (DMIIs and TMIIs) over multiple prey generations. Using a freshwater snail and three common snail predators, we constructed a series of community treatments with pond mesocosms that manipulated trophic structure, the identity of the top predator, and whether predators were caged or uncaged. We quantified snail phenotypes, snail population size, and resource abundance over multiple snail generations. We found that snails were expressing inducible defenses in our system although the magnitude of the responses varied over time and across predator species. Despite the expression of inducible defenses, caged predators did not reduce snail population size. There also was no evidence of TMIIs throughout the experiment suggesting that TMIIs have a minimal role in the long‐term structure of our communities. The absence of TMIIs was largely driven by the lack of predator‐induced reductions in resource consumption and the lack of consistent reductions in population size with predator cues. In contrast, we detected strong DMIIs associated with lethal predators suggesting that DMIIs are the dominant long‐term mechanism influencing community structure. Our results demonstrate that although predators can have significant effects on prey phenotypes and sometimes cause short‐term TMIIs, there may be few long‐term consequences of these responses on population dynamics and indirect interactions, at least within simple food webs. Research directed towards addressing the long‐term consequences of predator–prey interactions within communities will help to reveal whether the conclusions and predictions generated from short‐term experiments are applicable over ecological and evolutionary timescales.     

Producing and scrounging can have stabilizing effects at multiple levels of organization

This study shows, for the first time, that the evolution of a simple behavior, scrounging, at the individual level can have effects on populations, food chains, and community structure. In particular, the addition of scrounging in consumer populations can allow multiple consumers to coexist while exploiting a single prey. Also, scrounging in the top predator of a tritrophic food chain can stabilize interactions between the top predator, its prey, and its prey's prey. This occurs because the payoffs to scrounging for food in a population are negative frequency dependent, allowing scroungers to invade a population and to coexist with producers at a frequency which is density‐dependent. The presence of scroungers, who do not search for resources but simply use those found by others (producers) reduces the total amount of resource acquired by the group. As scrounging increases with group size, this leads to less resource acquired per individual as the group grows. Ultimately, this limits the size of the group, its impact on its prey, and its ability to outcompete other species. These effects can promote stability and thus increase species diversity. I will further suggest that prey may alter their spatial distribution such that scrounging will be profitable among their predators thus reducing predation rate on the prey.     

Bacterial predator–prey dynamics in microscale patchy landscapes

Soil is a microenvironment with a fragmented (patchy) spatial structure in which many bacterial species interact. Here, we explore the interaction between the predatory bacterium Bdellovibrio bacteriovorus and its prey Escherichia coli in microfabricated landscapes. We ask how fragmentation influences the prey dynamics at the microscale and compare two landscape geometries: a patchy landscape and a continuous landscape. By following the dynamics of prey populations with high spatial and temporal resolution for many generations, we found that the variation in predation rates was twice as large in the patchy landscape and the dynamics was correlated over shorter length scales. We also found that while the prey population in the continuous landscape was almost entirely driven to extinction, a significant part of the prey population in the fragmented landscape persisted over time. We observed significant surface-associated growth, especially in the fragmented landscape and we surmise that this sub-population is more resistant to predation. Our results thus show that microscale fragmentation can significantly influence bacterial interactions.     

Effects of evolutionary changes in prey use on the relationship between food web complexity and stability

The relationship between food web complexity and stability has been the subject of a long-standing debate in ecology. Although rapid changes in the food web structure through adaptive foraging behavior can confer stability to complex food webs, as reported by Kondoh (Science 299:1388–1391, 2003), the exact mechanisms behind this adaptation have not been specified in previous studies; thus, the applicability of such predictions to real ecosystems remains unclear. One mechanism of adaptive foraging is evolutionary change in genetically determined prey use. We constructed individual-based models of evolution of prey use by predators assuming explicit population genetics processes, and examined how this evolution affects the stability (i.e., the proportion of species that persist) of the food web and whether the complexity of the food web increased the stability of the prey–predator system. The analysis showed that the stability of food webs decreased with increasing complexity regardless of evolution of prey use by predators. The effects of evolution on stability differed depending on the assumptions made regarding genetic control of prey use. The probabilities of species extinctions were associated with the establishment or loss of trophic interactions via evolution of the predator, indicating a clear link between structural changes in the food web and community stability.     

Predator-prey coevolution driven by size selective predation can cause anti-synchronized and cryptic population dynamics

Population dynamics and evolutionary dynamics can occur on similar time scales, and a coupling of these two processes can lead to novel population dynamics. Recent theoretical studies of coevolving predator-prey systems have concentrated more on the stability of such systems than on the characteristics of cycles when they are unstable. Here I explore the characteristics of the cycles that arise due to coevolution in a system in which prey can increase their ability to escape from predators by becoming either significantly larger or significantly smaller in trait value (i.e., a bidirectional trait axis). This is a reasonable model of body size evolution in some systems. The results show that antiphase population cycles and cryptic cycles (large population fluctuation in one species but almost no change in another species) can occur in the coevolutionary system but not systems where only a single species evolves. Previously, those dynamical patterns have only been theoretically shown to occur in single species evolutionary models and the coevolutionary model which do not involve a bi-directional axis of adaptation. These unusual dynamics may be observed in predator-prey interactions when the density dependence in the prey species is strong.