Predation landscapes influence migratory prey ecology and evolution.

Migratory prey experience spatially variable predation across their life cycle. They face unique challenges in navigating this predation landscape, which affects their perception of risk, antipredator responses, and resulting mortality. Variable and unfamiliar predator cues during migration can limit accurate perception of risk and migrants often rely on social information and learning to compensate. The energetic demands of migration constrain antipredator responses, often through context-dependent patterns. While migration can increase mortality, migrants employ diverse strategies to balance risks and rewards, including life history and antipredator responses. Humans interact frequently with migratory prey across space and alter both mortality risk and antipredator responses, which can scale up to affect migratory populations and should be considered in conservation and management.

Trophic cascades alter eco-evolutionary dynamics and body size evolution.

Trait evolution in predator-prey systems can feed back to the dynamics of interacting species as well as cascade to impact the dynamics of indirectly linked species (eco-evolutionary trophic cascades; EETCs). A key mediator of trophic cascades is body mass, as it both strongly influences and evolves in response to predator-prey interactions. Here, we use Gillespie eco-evolutionary models to explore EETCs resulting from top predator loss and mediated by body mass evolution. Our four-trophic-level food chain model uses allometric scaling to link body mass to different functions (ecological pleiotropy) and is realistically parameterized from the FORAGE database to mimic the parameter space of a typical freshwater system. To track real-time changes in selective pressures, we also calculated fitness gradients for each trophic level. As predicted, top predator loss generated alternating shifts in abundance across trophic levels, and, depending on the nature and strength in changes to fitness gradients, also altered trajectories of body mass evolution. Although more distantly linked, changes in the abundance of top predators still affected the eco-evolutionary dynamics of the basal producers, in part because of their relatively short generation times. Overall, our results suggest that impacts on top predators can set off transient EETCs with the potential for widespread indirect impacts on food webs.

Trade-offs between morphology and thermal niches mediate adaptation in response to competing selective pressures.

The effects of climate change-such as increased temperature variability and novel predators-rarely happen in isolation, but it is unclear how organisms cope with multiple stressors simultaneously. To explore this, we grew replicate Paramecium caudatum populations in either constant or variable temperatures and exposed half to predation. We then fit thermal performance curves (TPCs) of intrinsic growth rate (r max) for each replicate population (N = 12) across seven temperatures (10°C-38°C). TPCs of P. caudatum exposed to both temperature variability and predation responded only to one or the other (but not both), resulting in unpredictable outcomes. These changes in TPCs were accompanied by changes in cell morphology. Although cell volume was conserved across treatments, cells became narrower in response to temperature variability and rounder in response to predation. Our findings suggest that predation and temperature variability produce conflicting pressures on both thermal performance and cell morphology. Lastly, we found a strong correlation between changes in cell morphology and TPC parameters in response to predation, suggesting that responses to opposing selective pressures could be constrained by trade-offs. Our results shed new light on how environmental and ecological pressures interact to elicit changes in characteristics at both the individual and population levels. We further suggest that morphological responses to interactive environmental forces may modulate population-level responses, making prediction of long-term responses to environmental change challenging.

Phenotypically plastic responses to predation risk are temperature dependent.

Predicting how organisms respond to climate change requires that we understand the temperature dependence of fitness in relevant ecological contexts (e.g., with or without predation risk). Predation risk often induces changes to life history traits that are themselves temperature dependent. We explore how perceived predation risk and temperature interact to determine fitness (indicated by the intrinsic rate of increase, r) through changes to its underlying components (net reproductive rate, generation time, and survival) in Daphnia magna. We exposed Daphnia to predation cues from dragonfly naiads early, late, or throughout their ontogeny. Predation risk increased r differentially across temperatures and depending on the timing of exposure to predation cues. The timing of predation risk likewise altered the temperature-dependent response of T and R0. Daphnia at hotter temperatures responded to predation risk by increasing r through a combination of increased R0 and decreased T that together countered an increase in mortality rate. However, only D. magna that experienced predation cues early in ontogeny showed elevated r at colder temperatures. These results highlight the fact that phenotypically plastic responses of life history traits to predation risk can be strongly temperature dependent.

Predators modify the temperature dependence of life-history trade-offs.

Although life histories are shaped by temperature and predation, their joint influence on the interdependence of life-history traits is poorly understood. Shifts in one life-history trait often necessitate shifts in another-structured in some cases by trade-offs-leading to differing life-history strategies among environments. The offspring size-number trade-off connects three traits whereby a constant reproductive allocation (R) constrains how the number (O) and size (S) of offspring change. Increasing temperature and size-independent predation decrease size at and time to reproduction which can lower R through reduced time for resource accrual or size-constrained fecundity. We investigated how O, S, and R in a clonal population of Daphnia magna change across their first three clutches with temperature and size-independent predation risk. Early in ontogeny, increased temperature moved O and S along a trade-off curve (constant R) toward fewer larger offspring. Later in ontogeny, increased temperature reduced R in the no-predator treatment through disproportionate decreases in O relative to S. In the predation treatment, R likewise decreased at warmer temperatures but to a lesser degree and more readily traded off S for O whereby the third clutch showed a constant allocation strategy of O versus S with decreasing R. Ontogenetic shifts in S and O rotated in a counterclockwise fashion as temperature increased and more drastically under risk of predation. These results show that predation risk can alter the temperature dependence of traits and their interactions through trade-offs.

Phylogenetic patterns of trait and trait plasticity evolution: Insights from amphibian embryos.

Environmental variation favors the evolution of phenotypic plasticity. For many species, we understand the costs and benefits of different phenotypes, but we lack a broad understanding of how plastic traits evolve across large clades. Using identical experiments conducted across North America, we examined prey responses to predator cues. We quantified five life-history traits and the magnitude of their plasticity for 23 amphibian species/populations (spanning three families and five genera) when exposed to no cues, crushed-egg cues, and predatory crayfish cues. Embryonic responses varied considerably among species and phylogenetic signal was common among the traits, whereas phylogenetic signal was rare for trait plasticities. Among trait-evolution models, the Ornstein-Uhlenbeck (OU) model provided the best fit or was essentially tied with Brownian motion. Using the best fitting model, evolutionary rates for plasticities were higher than traits for three life-history traits and lower for two. These data suggest that the evolution of life-history traits in amphibian embryos is more constrained by a species' position in the phylogeny than is the evolution of life history plasticities. The fact that an OU model of trait evolution was often a good fit to patterns of trait variation may indicate adaptive optima for traits and their plasticities.

Scaling from Metabolism to Population Growth Rate to Understand How Acclimation Temperature Alters Thermal Performance.

SYNOPSIS: The mean and variance of environmental temperature are changing as a consequence of human activities. Ectotherms are sensitive to these temperature changes in the short term, typically displaying a unimodal response of most biological rates to temperature (thermal performance curves; TPCs). Many organisms, however, may acclimate or evolve in response to new temperature regimes. In particular, population growth rate TPCs (r TPCs) reflect the ability to maintain positive growth under a range of temperatures, and therefore shifts in r TPCs due to acclimation are fundamental to our understanding of how ectotherms will respond to changes in climate. Here, we derive a model for r TPCs rooted in temperature dependent metabolic rate (through enzyme kinetics and activity). We then use this model to interpret the effects of acclimation to different temperatures on r TPCs of the protist Paramecium bursaria. Intermediate acclimation temperatures generally resulted in higher upper critical thermal limits, thermal optima, maximum population growth rate, and the area under the TPC. Lower critical thermal limits increased linearly with acclimation temperature, causing a decrease in thermal breadth with increased acclimation temperature. Thus, rather than showing improved performance at the acclimation temperature, P. bursaria appeared to pay a price at all temperatures for acclimating to higher temperatures. The fits of our data to our model also suggest that changes in the structure and function of metabolic enzymes may underlie the changes in the TPCs. Specifically, our results suggest that both the delta heat capacity and delta enthalpy of formation of metabolic enzymes may have increased with acclimation. Since these two factors are correlated across acclimation temperatures, our data also suggest potential trade-offs that may constrain changes in TPCs.

Stoichiometry and Life-History Interact to Determine the Magnitude of Cross-Ecosystem Element and Biomass Fluxes.

Ecosystems are linked through the transfer of materials and energy. Studies examining material fluxes across habitat boundaries frequently quantify unidirectional flows of nutrients and energy. However, material fluxes can be multidirectional, and we lack a conceptual framework to describe how their quantity and stoichiometry influence the net transfer of individual elements between ecosystems. Here we develop a zero net transfer isocline (ZNTI) framework that integrates the relative mass and stoichiometry of fluxes into and out of an ecosystem. We then use case studies with amphibians and salmon to elucidate how life history, ontogenetic shifts in stoichiometry, and trophic interactions shape relative fluxes of nutrients between aquatic and terrestrial ecosystems. Because they increase in both size and Ca content from ova to metamorphs, amphibian life histories strongly bias them toward net Ca export into the terrestrial environment. Because amphibian biomass, C, P, and Ca ZNTIs do not overlap, there is no value of survivorship where the net flux of biomass, C, P, and Ca are simultaneously balanced between terrestrial and aquatic habitats. The degree of iteroparity and semelparity in salmon strongly affects both the magnitude of net biomass and P flux between riverine and marine environments. While the net direction of biomass flux generally remains strongly biased toward import into the riverine system, net P flux can reach net export into the marine environment because of increasing adult breeding survival leading to reduced mass and %P of what they deposit in rivers (e.g., ova vs. whole carcasses). These examples highlight how ontogenetic shifts in body size and stoichiometry result in asymmetric fluxes of elements and biomass that can lead to simultaneous net imports and exports of different elements within the same system. Furthermore, they demonstrate how changes in life-history characteristics and stage-specific survivorship can lead to changes in net elemental transport between ecosystems.

Predation changes the shape of thermal performance curves for population growth rate.

Ectotherms generally demonstrate nonlinear changes in performance (e.g., movement speed, individual growth, population growth) as a function of temperature that are characterized by thermal performance curves (TPC). Predation risk elicits phenotypic and behavioral changes that likewise impact performance measures. We tested whether exposure to predation Orthocyclops modestus impacts the maximum population growth rate (rmax) TPC of the protist Paramecium aurelia. We fit predator and non-predator exposed P. aurelia population growth rates to a function previously shown to best describe Paramecium population growth rate TPC's (Lactin-2) and compared subsequent parameter estimates between curves. For Paramecium exposed to predation risk, maximum population growth increased more rapidly as temperatures rose and decreased more rapidly as temperatures fell compared to the initial temperature. The area under each TPC curve remained approximately the same, consistent with the idea of a trade-off in performance across temperatures. Our results indicate TPCs are flexible given variation in food web context and that trophic interactions may play an important role in shaping TPCs. Furthermore, this and other studies illustrate the need for a mechanistic model of TPCs with parameters tied to biologically meaningful properties.

Trade-offs between growth and maturation: the cost of reproduction for surviving environmental extremes.

Life-history trade-offs and the costs of reproduction are central concepts in evolution and ecology. Episodic climatic events such as drought and extreme temperatures provide strong selective pressures that can change the balance of these costs and trade-offs. We used size-structured matrix models parameterized from field and laboratory studies to examine the effect of periodic drought on two species of aquatic salamanders (greater siren, Siren lacertina; lesser siren, Siren intermedia) that differ in size at reproduction and maximum body size. Post-drought body size distributions of the larger species (S. lacertina) are consistent with size-dependent mortality. Smaller individuals were extirpated from the population during each drought while large animals persisted, a pattern that contrasted with that seen in several ectotherms. This appears to be largely explained by estivation proficiency and a positive relationship between body size and estivation potential. Increased body size, however, may come at the cost of fecundity and maturation rate compared to a closely related congener. The cost of somatic allocation in this case may manifest itself via reduced per-capita competitive ability, which (at least in simulation studies) allows the smaller, fast-maturing species to outcompete the larger, slow-maturing species when drought is minimal or nonexistent.