Phenotypic plasticity and the effects of thermal fluctuations on specialists and generalists.

Classical theories predict that relatively constant environments should generally favour specialists, while fluctuating environments should be selected for generalists. However, theoretical and empirical results have pointed out that generalist organisms might, on the contrary, perform poorly under fluctuations. In particular, if generalism is underlaid by phenotypic plasticity, performance of generalists should be modulated by the temporal characteristics of environmental fluctuations. Here, we used experiments in microcosms of Tetrahymena thermophila ciliates and a mathematical model to test whether the period or autocorrelation of thermal fluctuations mediate links between the level of generalism and the performance of organisms under fluctuations. In the experiment, thermal fluctuations consistently impeded performance compared with constant conditions. However, the intensity of this effect depended on the level of generalism: while the more specialist strains performed better under fast or negatively autocorrelated fluctuations, plastic generalists performed better under slow or positively autocorrelated fluctuations. Our model suggests that these effects of fluctuations on organisms' performance may result from a time delay in the expression of plasticity, restricting its benefits to slow enough fluctuations. This study points out the need to further investigate the temporal dynamics of phenotypic plasticity to better predict its fitness consequences under environmental fluctuations.

Unclear relationships between mean survival rate and its environmental variance in vertebrates.

Current environmental changes may increase temporal variability of life history traits of species thus affecting their long-term population growth rate and extinction risk. If there is a general relationship between environmental variances (EVs) and mean annual survival rates of species, that relationship could be used as a guideline for analyses of population growth and extinction risk for populations, where data on EVs are missing. For this purpose, we present a comprehensive compilation of 252 EV estimates from 89 species belonging to five vertebrate taxa (birds, mammals, reptiles, amphibians and fish) covering mean annual survival rates from 0.01 to 0.98. Since variances of survival rates are constrained by their means, particularly for low and high mean survival rates, we assessed whether any observed relationship persisted after applying two types of commonly used variance stabilizing transformations: relativized EVs (observed/mathematical maximum) and logit-scaled EVs. With raw EVs at the arithmetic scale, mean-variance relationships of annual survival rates were hump-shaped with small EVs at low and high mean survival rates and higher (and widely variable) EVs at intermediate mean survival rates. When mean annual survival rates were related to relativized EVs the hump-shaped pattern was less distinct than for raw EVs. When transforming EVs to logit scale the relationship between mean annual survival rates and EVs largely disappeared. The within-species juvenile-adult slopes were mainly positive at low (<0.5) and negative at high (>0.5) mean survival rates for raw and relativized variances while these patterns disappeared when EVs were logit transformed. Uncertainties in how to interpret the results of relativized and logit-scaled EVs, and the observed high variation in EV's for similar mean annual survival rates illustrates that extrapolations of observed EVs and tests of life history drivers of survival-EV relationships need to also acknowledge the large variation in these parameters.

Adaptive responses of eelgrass (Zostera marina L.) to ocean warming and acidification.

Ocean warming (OW) and ocean acidification (OA), driven by rapid global warming accelerating at unprecedented rates, are profoundly impacting the stability of seagrass ecosystems. Yet, our current understanding of the effects of OW and OA on seagrass remains constrained. Herein, we investigated the response of eelgrass (Zostera marina L.), a representative seagrass species, to OW and OA through comprehensive transcriptomic and metabolomic analyses. The results showed notable variations in plant performance under varying conditions: OW, OA, and OWA (a combination of both conditions). Specifically, under average oceanic temperature conditions for eelgrass growth over the past 20 years -from May to November-OA promoted the production of differentially expressed genes and metabolites associated with alanine, aspartate, and glutamate metabolism, as well as starch and sucrose metabolism. Under warming condition, eelgrass was resistant to OA by accelerating galactose metabolism, along with glycine, serine, and threonine metabolism, as well as the tricarboxylic acid (TCA) cycle. Under the combined OW and OA condition, eelgrass stimulated fructose and mannose metabolism, glycolysis, and carbon fixation, in addition to galactose metabolism and the TCA cycle to face the interplay. Our findings suggest that eelgrass exhibits adaptive capacity by inducing different metabolites and associated genes, primarily connected with carbon and nitrogen metabolism, in response to varying degrees of OW and OA. The data generated here support the exploration of mechanisms underlying seagrass responses to environmental fluctuations, which hold critical significance for the future conservation and management of these ecosystems.

Resistance and resilience to invasion is stronger in synchronous than compensatory communities.

While community synchrony is a key framework for predicting ecological constancy, the interplay between community synchrony and ecological invasions remains unclear. Yet the degree of synchrony in a resident community may influence its resistance and resilience to the introduction of an invasive species. Here we used a generalizable mathematical framework, constructed with a modified Lotka-Volterra competition model, to first simulate resident communities across a range of competitive strengths and species' responses to environmental fluctuations, which yielded communities that ranged from strongly synchronous to compensatory. We then invaded these communities at different timesteps with invaders of varying demographic traits, after which we quantified the resident community's susceptibility to initial invasion attempts (resistance) and the degree to which community synchrony was altered after invasion (resiliency of synchrony). We found that synchronous communities were not only more resistant but also more resilient to invasion than compensatory communities, likely due to stronger competition between resident species and thus lower cumulative abundances in compensatory communities, providing greater opportunities for invasion. The growth rate of the invader was most influenced by the resident and invader competition coefficients and the growth rate of the invader species. Our findings support prioritizing the conservation of compensatory and weakly synchronous communities which may be at increased risk of invasion.

Dephasing Dynamics in a Non-Equilibrium Fluctuating Environment.

We performed a theoretical study of the dephasing dynamics of a quantum two-state system under the influences of a non-equilibrium fluctuating environment. The effect of the environmental non-equilibrium fluctuations on the quantum system is described by a generalized random telegraph noise (RTN) process, of which the statistical properties are both non-stationary and non-Markovian. Due to the time-homogeneous property in the master equations for the multi-time probability distribution, the decoherence factor induced by the generalized RTN with a modulatable-type memory kernel can be exactly derived by means of a closed fourth-order differential equation with respect to time. In some special limit cases, the decoherence factor recovers to the expression of the previous ones. We analyzed in detail the environmental effect of memory modulation in the dynamical dephasing in four types of dynamics regimes. The results showed that the dynamical dephasing of the quantum system and the conversion between the Markovian and non-Markovian characters in the dephasing dynamics under the influence of the generalized RTN can be effectively modulated via the environmental memory kernel.

Controlling the Mean Time to Extinction in Populations of Bacteria.

Populations of ecological systems generally have demographic fluctuations due to birth and death processes. At the same time, they are exposed to changing environments. We studied populations composed of two phenotypes of bacteria and analyzed the impact that both types of fluctuations have on the mean time to extinction of the entire population if extinction is the final fate. Our results are based on Gillespie simulations and on the WKB approach applied to classical stochastic systems, here in certain limiting cases. As a function of the frequency of environmental changes, we observe a non-monotonic dependence of the mean time to extinction. Its dependencies on other system parameters are also explored. This allows the control of the mean time to extinction to be as large or as small as possible, depending on whether extinction should be avoided or is desired from the perspective of bacteria or the perspective of hosts to which the bacteria are deleterious.

Response of coral bacterial composition and function to water quality variations under anthropogenic influence.

Microbial communities play key roles in the adaptation of corals living in adverse environments, as the microbiome flexibility can enhance environmental plasticity of coral holobiont. However, the ecological association of coral microbiome and related function to locally deteriorating water quality remains underexplored. In this work, we used 16S rRNA gene sequencing and quantitative microbial element cycling (QMEC) to investigate the seasonal changes of bacterial communities, particularly their functional genes related to carbon (C), nitrogen (N), phosphorus (P) and sulfur (S) cycle, of the scleractinian coral Galaxea fascicularis from nearshore reefs exposed anthropogenic influence. We used nutrient concentrations as the indicator of anthropogenic activities in coastal reefs, and found a higher nutrient pressure in spring than summer. The bacterial diversity, community structure and dominant bacteria of coral shifted significantly due to seasonal variations dominated by nutrient concentrations. Additionally, the network structure and nutrient cycling gene profiles in summer under low nutrient stress was distinct from that under poor environmental conditions in spring, with lower network complexity and abundance of CNPS cycling genes in summer compared with spring. We further identified significant correlations between microbial community (taxonomic composition and co-occurrence network) and geochemical functions (abundance of multiple functional genes and functional community). Nutrient enrichment was proved to be the most important environmental fluctuation in controlling the diversity, community structure, interactional network and functional genes of the coral microbiome. These results highlight that seasonal shifts in coral-associated bacteria due to anthropogenic activities alter the functional potentials, and provide novel insight about the mechanisms of coral adaptation to locally deteriorating environments.

Marine heatwaves and upwelling shape stress responses in a keystone predator.

Climate change increases the frequency and intensifies the magnitude and duration of extreme events in the sea, particularly so in coastal habitats. However, the interplay of multiple extremes and the consequences for species and ecosystems remain unknown. We experimentally tested the impacts of summer heatwaves of differing intensities and durations, and a subsequent upwelling event on a temperate keystone predator, the starfish Asterias rubens. We recorded mussel consumption throughout the experiment and assessed activity and growth at strategically chosen time points. The upwelling event overall impaired starfish feeding and activity, likely driven by the acidification and low oxygen concentrations in the upwelled seawater. Prior exposure to a present-day heatwave (+5°C above climatology) alleviated upwelling-induced stress, indicating cross-stress tolerance. Heatwaves of present-day intensity decreased starfish feeding and growth. While the imposed heatwaves of limited duration (9 days) caused slight impacts but allowed for recovery, the prolonged (13 days) heatwave impaired overall growth. Projected future heatwaves (+8°C above climatology) caused 100% mortality of starfish. Our findings indicate a positive ecological memory imposed by successive stress events. Yet, starfish populations may still suffer extensive mortality during intensified end-of-century heatwave conditions.

Cellular memory of rapid growth is sensitive to nutrient depletion during starvation.

Bacteria frequently encounter nutrient fluctuations in natural environments, yet we understand little about their ability to maintain physiological memory of previous food sources. Starvation is a particularly acute case, in which cells must balance adaptation to stresses with limited nutrient supply. Here, we show that Escherichia coli cells immediately accelerate and decelerate in growth upon transitions from spent to fresh media and vice versa, respectively, and memory of rapid growth can be maintained for many hours under constant flow of spent medium. However, after transient exposure of stationary-phase cells to fresh medium, subsequent aerobic incubation in increasingly spent medium led to lysis and limited growth when rejuvenated in fresh medium. Growth defects were avoided by incubation in anaerobic spent medium or water, suggesting that defects were caused by respiration during the process of nutrient depletion in spent medium. These findings highlight the importance of respiration for stationary phase survival and underscore the broad range of starvation outcomes depending on environmental history.

Spatial correlation reverses the compound effect of multiple stressors on rocky shore biofilm.

Understanding how multifactorial fluctuating environments affect species and communities remains one of the major challenges in ecology. The spatial configuration of the environment is known to generate complex patterns of correlation among multiple stressors. However, to what extent the spatial correlation between simultaneously fluctuating variables affects ecological assemblages in real-world conditions remains poorly understood. Here, we use field experiments and simulations to assess the influence of spatial correlation of two relevant climate variables - warming and sediment deposition following heavy precipitation - on the biomass and photosynthetic activity of rocky intertidal biofilm. First, we used a response-surface design experiment to establish the relation between biofilm, warming, and sediment deposition in the field. Second, we used the response surface to generate predictions of biofilm performance under different scenarios of warming and sediment correlation. Finally, we tested the predicted outcomes by manipulating the degree of correlation between the two climate variables in a second field experiment. Simulations stemming from the experimentally derived response surface showed how the degree and direction (positive or negative) of spatial correlation between warming and sediment deposition ultimately determined the nonlinear response of biofilm biomass (but not photosynthetic activity) to fluctuating levels of the two climate variables. Experimental results corroborated these predictions, probing the buffering effect of negative spatial correlation against extreme levels of warming and sediment deposition. Together, these results indicate that consideration of nonlinear response functions and local-scale patterns of correlation between climate drivers can improve our understanding and ability to predict ecological responses to multiple processes in heterogeneous environments.

Maintenance of community function through compensation breaks down over time in a desert rodent community.

Understanding the ecological processes that maintain community function in systems experiencing species loss, and how these processes change over time, is key to understanding the relationship between community structure and function and predicting how communities may respond to perturbations in the Anthropocene. Using a 30-year experiment on desert rodents, we show that the impact of species loss on community-level energy use has changed repeatedly and dramatically over time, due to (1) the addition of new species to the community, and (2) a reduction in functional redundancy among the same set of species. Although strong compensation, initially driven by the dispersal of functionally redundant species to the local community, occurred in this system from 1997 to 2010, since 2010, compensation has broken down due to decreasing functional overlap within the same set of species. Simultaneously, long-term changes in sitewide community composition due to niche complementarity have decoupled the dynamics of compensation from the overall impact of species loss on community-level energy use. Shifting, context-dependent compensatory dynamics, such as those demonstrated here, highlight the importance of explicitly long-term, metacommunity, and eco-evolutionary perspectives on the link between species-level fluctuations and community function in a changing world.

A simple adaptive difference algorithm with CO2 measurements for evaluating plant growth under environmental fluctuations.

OBJECTIVE: The aim of this study is to demonstrate an adaptive method that is robust toward environmental fluctuations and provides a real-time measure of plant growth by measuring CO2 consumption. To verify the validity of the proposed method, the relation between the plant growth and variation in light conditions with a closed experimental system was investigated. RESULTS: The proposed method was used to measure the photosynthetic rate induced by photosynthetic photon flux density (PPFD) and to evaluate plant growth under continuous and pulsed light in arugula plants. The PPFD-dependent change in photosynthetic rate was measured. And in the condition range of 200-10,000 µs pulse period and 50% duty ratio of pulsed light, there was no change in the growth rate of plants assuming the same PPFD as continuous light. These experiments showed the validity of the adaptive method in removing environmental fluctuations without precise control of temperature and humidity.

The long and the short of it: Mechanisms of synchronous and compensatory dynamics across temporal scales.

Synchronous dynamics (fluctuations that occur in unison) are universal phenomena with widespread implications for ecological stability. Synchronous dynamics can amplify the destabilizing effect of environmental variability on ecosystem functions such as productivity, whereas the inverse, compensatory dynamics, can stabilize function. Here we combine simulation and empirical analyses to elucidate mechanisms that underlie patterns of synchronous versus compensatory dynamics. In both simulated and empirical communities, we show that synchronous and compensatory dynamics are not mutually exclusive but instead can vary by timescale. Our simulations identify multiple mechanisms that can generate timescale-specific patterns, including different environmental drivers, diverse life histories, dispersal, and non-stationary dynamics. We find that traditional metrics for quantifying synchronous dynamics are often biased toward long-term drivers and may miss the importance of short-term drivers. Our findings indicate key mechanisms to consider when assessing synchronous versus compensatory dynamics and our approach provides a pathway for disentangling these dynamics in natural systems.

The role of phenotypic plasticity in the establishment of range margins.

It has been argued that adaptive phenotypic plasticity may facilitate range expansions over spatially and temporally variable environments. However, plasticity may induce fitness costs. This may hinder the evolution of plasticity. Earlier modelling studies examined the role of plasticity during range expansions of populations with fixed genetic variance. However, genetic variance evolves in natural populations. This may critically alter model outcomes. We ask: how does the capacity for plasticity in populations with evolving genetic variance alter range margins that populations without the capacity for plasticity are expected to attain? We answered this question using computer simulations and analytical approximations. We found a critical plasticity cost above which the capacity for plasticity has no impact on the expected range of the population. Below the critical cost, by contrast, plasticity facilitates range expansion, extending the range in comparison to that expected for populations without plasticity. We further found that populations may evolve plasticity to buffer temporal environmental fluctuations, but only when the plasticity cost is below the critical cost. Thus, the cost of plasticity is a key factor involved in range expansions of populations with the potential to express plastic response in the adaptive trait. This article is part of the theme issue 'Species' ranges in the face of changing environments (part I)'.

A general theory of coexistence and extinction for stochastic ecological communities.

We analyze a general theory for coexistence and extinction of ecological communities that are influenced by stochastic temporal environmental fluctuations. The results apply to discrete time (stochastic difference equations), continuous time (stochastic differential equations), compact and non-compact state spaces and degenerate or non-degenerate noise. In addition, we can also include in the dynamics auxiliary variables that model environmental fluctuations, population structure, eco-environmental feedbacks or other internal or external factors. We are able to significantly generalize the recent discrete time results by Benaim and Schreiber (J Math Biol 79:393-431, 2019) to non-compact state spaces, and we provide stronger persistence and extinction results. The continuous time results by Hening and Nguyen (Ann Appl Probab 28(3):1893-1942, 2018a) are strengthened to include degenerate noise and auxiliary variables. Using the general theory, we work out several examples. In discrete time, we classify the dynamics when there are one or two species, and look at the Ricker model, Log-normally distributed offspring models, lottery models, discrete Lotka-Volterra models as well as models of perennial and annual organisms. For the continuous time setting we explore models with a resource variable, stochastic replicator models, and three dimensional Lotka-Volterra models.

Stationary distributions of persistent ecological systems.

We analyze ecological systems that are influenced by random environmental fluctuations. We first provide general conditions which ensure that the species coexist and the system converges to a unique invariant probability measure (stationary distribution). Since it is usually impossible to characterize this invariant probability measure analytically, we develop a powerful method for numerically approximating invariant probability measures. This allows us to shed light upon how the various parameters of the ecosystem impact the stationary distribution. We analyze different types of environmental fluctuations. At first we study ecosystems modeled by stochastic differential equations. In the second setting we look at piecewise deterministic Markov processes. These are processes where one follows a system of differential equations for a random time, after which the environmental state changes, and one follows a different set of differential equations-this procedure then gets repeated indefinitely. Finally, we look at stochastic differential equations with switching, which take into account both the white noise fluctuations and the random environmental switches. As applications of our theoretical and numerical analysis, we look at competitive Lotka-Volterra, Beddington-DeAngelis predator-prey, and rock-paper-scissors dynamics. We highlight new biological insights by analyzing the stationary distributions of the ecosystems and by seeing how various types of environmental fluctuations influence the long term fate of populations.

Congruent Genetic and Demographic Dispersal Rates in a Natural Metapopulation at Equilibrium.

Understanding the functioning of natural metapopulations at relevant spatial and temporal scales is necessary to accurately feed both theoretical eco-evolutionary models and conservation plans. One key metric to describe the dynamics of metapopulations is dispersal rate. It can be estimated with either direct field estimates of individual movements or with indirect molecular methods, but the two approaches do not necessarily match. We present a field study in a large natural metapopulation of the butterfly Boloria eunomia in Belgium surveyed over three generations using synchronized demographic and genetic datasets with the aim to characterize its genetic structure, its dispersal dynamics, and its demographic stability. By comparing the census and effective population sizes, and the estimates of dispersal rates, we found evidence of stability at several levels: constant inter-generational ranking of population sizes without drastic historical changes, stable genetic structure and geographically-influenced dispersal movements. Interestingly, contemporary dispersal estimates matched between direct field and indirect genetic assessments. We discuss the eco-evolutionary mechanisms that could explain the described stability of the metapopulation, and suggest that destabilizing agents like inter-generational fluctuations in population sizes could be controlled by a long adaptive history of the species to its dynamic local environment. We finally propose methodological avenues to further improve the match between demographic and genetic estimates of dispersal.

Predicting community dynamics of antibiotic-sensitive and -resistant species in fluctuating environments.

Microbes occupy almost every niche within and on their human hosts. Whether colonizing the gut, mouth or bloodstream, microorganisms face temporal fluctuations in resources and stressors within their niche but we still know little of how environmental fluctuations mediate certain microbial phenotypes, notably antimicrobial-resistant ones. For instance, do rapid or slow fluctuations in nutrient and antimicrobial concentrations select for, or against, resistance? We tackle this question using an ecological approach by studying the dynamics of a synthetic and pathogenic microbial community containing two species, one sensitive and the other resistant to an antibiotic drug where the community is exposed to different rates of environmental fluctuation. We provide mathematical models, supported by experimental data, to demonstrate that simple community outcomes, such as competitive exclusion, can shift to coexistence and ecosystem bistability as fluctuation rates vary. Theory gives mechanistic insight into how these dynamical regimes are related. Importantly, our approach highlights a fundamental difference between resistance in single-species populations, the context in which it is usually assayed, and that in communities. While fast environmental changes are known to select against resistance in single-species populations, here we show that they can promote the resistant species in mixed-species communities. Our theoretical observations are verified empirically using a two-species Candida community.

Quantifying the relative importance of variation in predation and the environment for species coexistence.

Coexistence and food web theory are two cornerstones of the long-standing effort to understand how species coexist. Although competition and predation are known to act simultaneously in communities, theory and empirical study of these processes continue to be developed largely independently. Here, we integrate modern coexistence theory and food web theory to simultaneously quantify the relative importance of predation and environmental fluctuations for species coexistence. We first examine coexistence in a theoretical, multitrophic model, adding complexity to the food web using machine learning approaches. We then apply our framework to a stochastic model of the rocky intertidal food web, partitioning empirical coexistence dynamics. We find the main effects of both environmental fluctuations and variation in predator abundances contribute substantially to species coexistence. Unexpectedly, their interaction tends to destabilise coexistence, leading to new insights about the role of bottom-up vs. top-down forces in both theory and the rocky intertidal ecosystem.

The Nutritional Ecology of Marine Apex Predators.

Apex predators play pivotal roles in marine ecosystems, mediated principally through diet and nutrition. Yet, compared with terrestrial animals, the nutritional ecology of marine predators is poorly understood. One reason is that the field has adhered to an approach that evaluates diet principally in terms of energy gain. Studies in terrestrial systems, by contrast, increasingly adopt a multidimensional approach, the nutritional geometry framework, that distinguishes specific nutrients and calories. We provide evidence that a nutritional approach is likewise relevant to marine apex predators, then demonstrate how nutritional geometry can characterize the nutrient and energy content of marine prey. Next, we show how this framework can be used to reconceptualize ecological interactions via the ecological niche concept, and close with a consideration of its application to problems in marine predator research.