Time is of the essence: A general framework for uncovering temporal structures of communities.

Ecological communities are inherently dynamic: species constantly turn over within years, months, weeks or even days. These temporal shifts in community composition determine essential aspects of species interactions and how energy, nutrients, information, diseases and perturbations 'flow' through systems. Yet, our understanding of community structure has relied heavily on static analyses not designed to capture critical features of this dynamic temporal dimension of communities. Here, we propose a conceptual and methodological framework for quantifying and analysing this temporal dimension. Conceptually, we split the temporal structure into two definitive features, sequence and duration, and review how they are linked to key concepts in ecology. We then outline how we can capture these definitive features using perspectives and tools from temporal graph theory. We demonstrate how we can easily integrate ongoing research on phenology into this framework and highlight what new opportunities arise from this approach to answer fundamental questions in community ecology. As climate change reshuffles ecological communities worldwide, quantifying the temporal organization of communities is imperative to resolve the fundamental processes that shape natural ecosystems and predict how these systems may change in the future.

Time-dependent interaction modification generated from plant-soil feedback.

Pairwise interactions between species can be modified by other community members, leading to emergent dynamics contingent on community composition. Despite the prevalence of such higher-order interactions, little is known about how they are linked to the timing and order of species' arrival. We generate population dynamics from a mechanistic plant-soil feedback model, then apply a general theoretical framework to show that the modification of a pairwise interaction by a third plant depends on its germination phenology. These time-dependent interaction modifications emerge from concurrent changes in plant and microbe populations and are strengthened by higher overlap between plants' associated microbiomes. The interaction between this overlap and the specificity of microbiomes further determines plant coexistence. Our framework is widely applicable to mechanisms in other systems from which similar time-dependent interaction modifications can emerge, highlighting the need to integrate temporal shifts of species interactions to predict the emergent dynamics of natural communities.

Priority Effects Determine How Dispersal Affects Biodiversity in Seasonal Metacommunities.

AbstractThe arrival order of species frequently determines the outcome of their interactions. This phenomenon, called the priority effect, is ubiquitous in nature and determines local community structure, but we know surprisingly little about how it influences biodiversity across different spatial scales. Here, we use a seasonal metacommunity model to show that biodiversity patterns and the homogenizing effect of high dispersal depend on the specific mechanisms underlying priority effects. When priority effects are driven only by positive frequency dependence, dispersal-diversity relationships are sensitive to initial conditions but generally show a hump-shaped relationship: biodiversity declines when dispersal rates become high and allow the dominant competitor to exclude other species across patches. When spatiotemporal variation in phenological differences alters species' interaction strengths (trait-dependent priority effects), local, regional, and temporal diversity are surprisingly insensitive to variation in dispersal, regardless of the initial numeric advantage. Thus, trait-dependent priority effects can strongly reduce the effect of dispersal on biodiversity, preventing the homogenization of metacommunities. Our results suggest an alternative mechanism that maintains local and regional diversity without environmental heterogeneity, highlighting that accounting for the mechanisms underlying priority effects is fundamental to understanding patterns of biodiversity.

Stage-mediated priority effects and season lengths shape long-term competition dynamics.

The relative arrival time of species can affect their interactions and thus determine which species persist in a community. Although this phenomenon, called priority effect, is widespread in natural communities, it is unclear how it depends on the length of growing season. Using a seasonal stage-structured model, we show that differences in stages of interacting species could generate priority effects by altering the strength of stabilizing and equalizing coexistence mechanisms, changing outcomes between exclusion, coexistence and positive frequency dependence. However, these priority effects are strongest in systems with just one or a few generations per season and diminish in systems where many overlapping generations per season dilute the importance of stage-specific interactions. Our model reveals a novel link between the number of generations in a season and the consequences of priority effects, suggesting that consequences of phenological shifts driven by climate change should depend on specific life histories of organisms.

Exploring Conditions That Strengthen or Weaken the Ecological and Evolutionary Consequences of Phenological Synchrony.

AbstractClimate change-driven phenological shifts alter the temporal distributions of natural populations and communities, but we have little understanding of how these shifts affect natural populations. Using agent-based models, we show that the interaction of within-population synchrony (individual variation in timing) and timing of interspecific interactions shapes ecological and evolutionary dynamics of populations within a seasonal cycle. Low-synchrony populations had lower survival and biomass but relatively stronger individuals. These effects were surprisingly robust and did not require size-based competitive asymmetries. However, reducing population synchrony could either negatively or positively affect population demography depending on whether the phenology of the focal species was advanced or delayed relative to its competitor. Furthermore, selection for earlier hatching increased when the interspecific competitor arrived earlier and when population synchrony was high. These results emphasize the importance of variation in the phenology of individuals within populations to better understand species interactions and predict ecological and evolutionary outcomes of phenological shifts.

Experimental evidence that local interactions select against selfish behaviour.

How social behaviours evolve remains one of the most debated questions in evolutionary biology. An important theoretical prediction is that when organisms interact locally due to limited dispersal or strong social ties, the population structure that emerges may favour cooperation over antagonism. We carry out an experimental test of this theory by directly manipulating population spatial structure in an insect laboratory model system and measuring the impact on the evolution of the extreme selfish behaviour of cannibalism. We show that, as predicted by the theory, Indian meal moth larvae that evolved in environments with more limited dispersal are selected for lower rates of cannibalism. This is important because it demonstrates that local interactions select against selfish behaviour. Therefore, the ubiquitous variation in population structure that we see in nature is a simple mechanism that can help to explain the variation in selfish and cooperative behaviours that we see in nature.

Developmental Change in Predators Drives Different Community Configurations.

AbstractTheoreticians who first observed alternative stable states in simple ecological models warned of grave implications for unexpected and irreversible collapses of natural systems (i.e., regime shifts). Recent ecosystem-level shifts engendering considerable economic losses have validated this concern, positioning bistability at the vanguard of coupled human-environment systems management. While the perturbations that induce regime shifts are known, the ecological forces that uphold alternative stable states are often unresolved or complex and system specific. Thus, the search continues for general mechanisms that can produce alternative stable states under realistic conditions. Integrating model predictions with long-term zooplankton community experiments, we show that the core feature of ontogenetic development, food-dependent maturation, enables a single community to reach different configurations within the same constant environment. In one configuration, predators regulate prey to foster coexistence, while in the other, prey counterintuitively exclude their predators via maturation-limiting competition. The concordance of these findings with the unique outcome and underlying mechanism of a general model provides empirical evidence that developmental change, a fundamental property of life, can support bistability of natural systems.

Ontogenetic diversity buffers communities against consequences of species loss.

Biodiversity can be measured at multiple organizational scales. While traditional studies have focused at taxonomic diversity, recent studies have emphasized the ecological importance of diversity within populations. However, it is unclear how these different scales of diversity interact to determine the consequence of species loss. Here we asked how predator diversity and presence of ontogenetic diversity within predator populations influences community structure. Ontogenetic diversity arises from shifts in the traits and ecology of individuals during ontogeny and it is one of the biggest sources of intraspecific diversity. However, whether it dampens or strengthens the negative consequences of with species loss is poorly understood. To study the interaction of species diversity and ontogenetic diversity, we experimentally manipulated predator species diversity and diversity of developmental stages within focal predator species and analysed their joint effect on predator and prey survival, biomass and prey community structure in experimental pond systems. While individual effects of ontogenetic diversity were often species specific, losing predator species from the community often had a much smaller or no effect on prey survival, biomass or community structure when all predator populations had high ontogenetic diversity. Thus, ontogenetic diversity within populations buffered against some of the consequences of biodiversity loss at higher organizational levels. Because the experiment controlled mean per capita size and biomass across structured versus unstructured populations, this pattern was not driven by differences in biomass of predators. Instead, results suggest that effects were driven by changes in the functional roles and indirect interactions across and within species. This indicates that even if all environmental conditions are similar, differences in the intrinsic structure of populations can modify the consequences of biodiversity loss. Together, these results revealed the importance of ontogenetic diversity within species for strengthening the resilience of natural communities to consequences of biodiversity loss and emphasize the need to integrate biodiversity patterns across organizational scales.

Within-host priority effects and epidemic timing determine outbreak severity in co-infected populations.

Co-infections of hosts by multiple pathogen species are ubiquitous, but predicting their impact on disease remains challenging. Interactions between co-infecting pathogens within hosts can alter pathogen transmission, with the impact on transmission typically dependent on the relative arrival order of pathogens within hosts (within-host priority effects). However, it is unclear how these within-host priority effects influence multi-pathogen epidemics, particularly when the arrival order of pathogens at the host-population scale varies. Here, we combined models and experiments with zooplankton and their naturally co-occurring fungal and bacterial pathogens to examine how within-host priority effects influence multi-pathogen epidemics. Epidemiological models parametrized with within-host priority effects measured at the single-host scale predicted that advancing the start date of bacterial epidemics relative to fungal epidemics would decrease the mean bacterial prevalence in a multi-pathogen setting, while models without within-host priority effects predicted the opposite effect. We tested these predictions with experimental multi-pathogen epidemics. Empirical dynamics matched predictions from the model including within-host priority effects, providing evidence that within-host priority effects influenced epidemic dynamics. Overall, within-host priority effects may be a key element of predicting multi-pathogen epidemic dynamics in the future, particularly as shifting disease phenology alters the order of infection within hosts.

The role of seasonal timing and phenological shifts for species coexistence.

Shifts in the phenologies of coexistence species are altering the temporal structure of natural communities worldwide. However, predicting how these changes affect the structure and long-term dynamics of natural communities is challenging because phenology and coexistence theory have largely proceeded independently. Here, I propose a conceptual framework that incorporates seasonal timing of species interactions into a well-studied competition model to examine how changes in phenologies influence long-term dynamics of natural communities. Using this framework I demonstrate that persistence and coexistence conditions strongly depend on the difference in species' mean phenologies and how this difference varies across years. Consequently, shifts in mean and interannual variation in relative phenologies of species can fundamentally alter the outcome of interactions and the potential for persistence and coexistence of competing species. These effects can be predicted by how per-capita effects scale with differences in species' phenologies. I outline how this approach can be parameterized with empirical systems and discuss how it fits within the context of current coexistence theory. Overall, this synthesis reveals that phenology of species interactions can play a crucial yet currently understudied role in driving coexistence and biodiversity patterns in natural systems and determine how species will respond to future climate change.

Phenotype-Environment Matching Predicts Both Positive and Negative Effects of Intraspecific Variation.

Natural populations can vary considerably in their genotypic and/or phenotypic diversity. Differences in this intraspecific diversity can have important consequences for contemporary ecological dynamics, but the direction and magnitude of these effects appear inconsistent across studies and systems. Here we proposed and tested the hypothesis that context-dependent ecological effects of altering phenotypic variance are predictable and arise from the relationship between a population's mean phenotype and the local environmental optimum. By factorially manipulating the mean and variance of a key host trait in environments with and without a lethal parasite, we demonstrate that increasing phenotypic variance can have beneficial effects for host populations (e.g., smaller disease epidemics) but only when the population's initial phenotype was poorly matched to the local environment. When phenotypes were initially well suited to environmental conditions, in contrast, greater phenotypic variance led to larger disease epidemics. Significant reductions in individual susceptibility occurred in both contexts over time, but the mechanisms leading to those reductions differed; strong selection was caused by either a suboptimal trait mean and insufficient trait variance or a near-optimal trait mean and too much trait variance. Increasing intraspecific variation is clearly not always beneficial for populations, instead producing predictable ecological and evolutionary effects that depend on environmental context and biological interactions.

Within-Host Priority Effects Systematically Alter Pathogen Coexistence.

Coinfection of host populations alters pathogen prevalence, host mortality, and pathogen evolution. Because pathogens compete for limiting resources, whether multiple pathogens can coexist in a host population can depend on their within-host interactions, which, in turn, can depend on the order in which pathogens infect hosts (within-host priority effects). However, the consequences of within-host priority effects for pathogen coexistence have not been tested. Using laboratory studies with a coinfected zooplankton system, we found that pathogens had increased fitness in coinfected hosts when they were the second pathogen to infect a host, compared to when they were the first pathogen to infect a host. With these results, we parameterized a pathogen coexistence model with priority effects, finding that pathogen coexistence (1) decreased when priority effects increased the fitness of the first pathogen to arrive in coinfected hosts and (2) increased when priority effects increased the fitness of the second pathogen to arrive in coinfected hosts. We also identified the natural conditions under which we expect within-host priority effects to foster coexistence in our system. These outcomes were the result of positive or negative frequency dependence created by feedback loops between pathogen prevalence and infection order in coinfected hosts. This suggests that priority effects can systematically alter conditions for pathogen coexistence in host populations, thereby changing pathogen community structure and potentially altering host mortality and pathogen evolution via emergent processes.

Opportunities for behavioral rescue under rapid environmental change.

Laboratory measurements of physiological and demographic tolerances are important in understanding the impact of climate change on species diversity; however, it has been recognized that forecasts based solely on these laboratory estimates overestimate risk by omitting the capacity for species to utilize microclimatic variation via behavioral adjustments in activity patterns or habitat choice. The complex, and often context-dependent nature, of microclimate utilization has been an impediment to the advancement of general predictive models. Here, we overcome this impediment and estimate the potential impact of warming on the fitness of ectotherms using a benefit/cost trade-off derived from the simple and broadly documented thermal performance curve and a generalized cost function. Our framework reveals that, for certain environments, the cost of behavioral thermoregulation can be reduced as warming occurs, enabling behavioral buffering (e.g., the capacity for behavior to ameliorate detrimental impacts) and "behavioral rescue" from extinction in extreme cases. By applying our framework to operative temperature and physiological data collected at an extremely fine spatial scale in an African lizard, we show that new behavioral opportunities may emerge. Finally, we explore large-scale geographic differences in the impact of behavior on climate-impact projections using a global dataset of 38 insect species. These multiple lines of inference indicate that understanding the existing relationship between thermal characteristics (e.g., spatial configuration, spatial heterogeneity, and modal temperature) is essential for improving estimates of extinction risk.

Carryover effects drive competitive dominance in spatially structured environments.

Understanding how changes to the quality of habitat patches affect the distribution of species across the whole landscape is critical in our human-dominated world and changing climate. Although patterns of species' abundances across a landscape are clearly influenced by dispersal among habitats and local species interactions, little is known about how the identity and origin of dispersers affect these patterns. Because traits of individuals are altered by experiences in their natal habitat, differences in the natal habitat of dispersers can carry over when individuals disperse to new habitats and alter their fitness and interactions with other species. We manipulated the presence or absence of such carried-over natal habitat effects for up to eight generations to examine their influence on two interacting species across multiple dispersal rates and different habitat compositions. We found that experimentally accounting for the natal habitat of dispersers significantly influenced competitive outcomes at all spatial scales and increased total community biomass within a landscape. However, the direction and magnitude of the impact of natal habitat effects was dependent upon landscape type and dispersal rate. Interestingly, effects of natal habitats increased the difference between species performance across the landscape, suggesting that natal habitat effects could alter competitive interactions to promote spatial coexistence. Given that heterogeneity in habitat quality is ubiquitous in nature, natal habitat effects are likely important drivers of spatial community structure and could promote variation in species performance, which may help facilitate spatial coexistence. The results have important implications for conservation and invasive species management.

Shifts in phenological distributions reshape interaction potential in natural communities.

Climate change has changed the phenologies of species worldwide, but it remains unclear how these phenological changes will affect species interactions and the structure of natural communities. Using a novel approach to analyse long-term data of 66 amphibian species pairs across eight communities, we demonstrate that phenological shifts can significantly alter the interaction potential of coexisting competitors. Importantly, these changes in interaction potential were mediated by non-uniform, species-specific shifts in entire phenological distributions and consequently could not be captured by metrics traditionally used to quantify phenological shifts. Ultimately, these non-uniform shifts in phenological distributions increased the interaction potential for 25% of species pairs (and did not reduce interaction potential for any species pair), altering temporal community structure and potentially increasing interspecific competition. These results demonstrate the potential of phenological shifts to reshape temporal structure of natural communities, emphasising the importance of considering entire phenological distributions of natural populations.

Prey Limitation Drives Variation in Allometric Scaling of Predator-Prey Interactions.

Ecologists have long searched for a universal size-scaling constant that governs trophic interactions. Although this is an appealing theoretical concept, predator-prey size ratios (PPSRs) vary strikingly across and within natural food webs, meaning that predators deviate from their optimal prey size by consuming relatively larger or smaller prey. Here we suggest that this unexpected variation in allometric scaling of trophic interactions can be predicted by gradients of prey limitation consistent with predictions from optimal foraging theory. We analyzed >6,000 trophic interactions of 52 populations from four tropical frog species along a gradient of prey limitation. The mean of PPSR and its variance differed up to two orders of magnitude across and within food webs. Importantly, as prey availability decreased across food webs, PPSR and its variance became more size dependent. Thus, trophic interactions did not follow a fixed allometric scaling but changed predictably with the strength of prey limitation. Our results emphasize the importance of ecological contexts in arranging food webs and the need to incorporate ecological drivers of PPSR and its variance in food web and community models.

Nonlinear effects of phenological shifts link interannual variation to species interactions.

The vast majority of species interactions are seasonally structured and depend on species' relative phenologies. However, differences in the phenologies of species naturally vary across years and are altered by ongoing climate change around the world. By combining experiments that shifted the relative hatching of two competing tadpole species across a productivity gradient with simulations of inter-annual variation in arrival times I tested how phenological variation across years can alter the strength and outcome of interspecific competition. Shifting the relative timing of hatching (phenology) of a species fundamentally altered interspecific competition, and the effect of shifting the timing on competition was highly non-linear for most demographic rates. Furthemore, this relationship varied with productivity of the system. As a consequence, (a) shifts in relative timing of phenologies had small or large effects depending on the average natural timing of interactions, and (b) changes in the inter-annual variation in onset of interaction alone can alter species interactions in simulations even when mean phenologies (timing) remain unchanged across years. Studies on phenologies traditionally focus on directional shifts in the mean of phenologies, but these results suggest that we also need to consider inter-annual variation in phenologies of interacting species to predict dynamics of natural communities and how they will be modified by climate change.

Drivers of individual niche variation in coexisting species.

Although neglected by classic niche theory, individual variation is now recognized as a prevalent phenomenon in nature with evolutionary and ecological relevance. Recent theory suggests that differences in individual variation across competitors can affect species coexistence and community patterns. However, the degree of individual variation is flexible across wild populations and we still know little about the ecological drivers of this variation across populations of single species and, especially, across coexisting species. Here, we aimed to (a) elucidate the major drivers of individual niche variation in natural communities and (b) to determine how consistent this variation is across coexisting species and communities. We analysed natural patterns of individual-level niche variation in four species of coexisting generalist frogs across a wide range of tropical communities. Specifically, we used gut contents and stable isotopes (δ13 C and δ15 N) from frog species and their prey to quantify individual niche specialization. Then, we combined data on local community structure, availability of prey, phylogenetic relationships and predator-prey size models to test how this variation is related to four ecological factors which are predicted to be key drivers of individual specialization: intraspecific competition, interspecific competition, ecological opportunity (i.e., diversity of resources) and predation. We found that the degree of individual trophic specialization varied by up to ninefold across populations within the same species. This sizable variation in trophic specialization across populations was at least partially explained by gradients of density of competitors (both conspecifics and heterospecifics) and intraguild predation. However, the specific relationships between individual specialization and these ecological gradients were strongly species-specific. As consequences, the identity of the species with more individual variation changed among sites and there was typically no spatial correlation in the degree of individual specialization across coexisting species. Our results show that individual niche specialization within and across species can be strongly context-dependent and that hierarchies of individual variation among coexisting species are not necessarily consistent across communities. Recent theory suggests that this pattern could lead to concurrent changes in competitive interactions across sites and thereby could play a key role in species coexistence at the landscape level. Our results suggest that individual variation across and within coexisting species has the potential to affect not only species coexistence at local communities, but also regional diversity patterns.

Queen presence mediates the relationship between collective behaviour and disease susceptibility in ant colonies.

The success of social living can be explained, in part, by a group's ability to execute collective behaviours unachievable by solitary individuals. However, groups vary in their ability to execute these complex behaviours, often because they vary in their phenotypic composition. Group membership changes over time due to mortality or emigration, potentially leaving groups vulnerable to ecological challenges in times of flux. In some societies, the loss of important individuals (e.g. leaders, elites and queens) may have an especially detrimental effect on groups' ability to deal with these challenges. Here, we test whether the removal of queens in colonies of the acorn ant Temnothorax curvispinosus alters their ability to execute important collective behaviours and survive outbreaks of a generalist entomopathogen. We employed a split-colony design where one half of a colony was maintained with its queen, while the other half was separated from the queen. We then tested these subcolonies' performance in a series of collective behaviour assays and finally exposed colonies to the entomopathogenic fungus Metarhizium robertsii by exposing two individuals from the colony and then sealing them back into the nest. We found that queenright subcolonies outperformed their queenless counterparts in nearly all collective behaviours. Queenless subcolonies were also more vulnerable to mortality from disease. However, queenless groups that displayed more interactions with brood experienced greater survivorship, a trend not present in queenright subcolonies. Queenless subcolonies that engage in more brood interactions may have had more resources available to cope with two physiological challenges (ovarian development after queen loss and immune activation after pathogen exposure). Our results indicate that queen presence can play an integral role in colony behaviour, survivorship and their relationship. They also suggest that interactions between workers and brood are integral to colonies survival. Overall, a social group's history of social reorganization may have strong consequences on their collective behaviours and their vulnerability to disease outbreaks.