How moonlight shapes environments, life histories, and ecological interactions on coral reefs.

The lunar cycle drives variation in nocturnal brightness. For the epipelagic larvae of coral reef organisms, nocturnal illumination may have widespread and underappreciated consequences. At sea, the onset of darkness coincides with an influx of mesopelagic organisms to shallow water (i.e. 'diel vertical migrants') that include predators (e.g. lanternfishes) and prey (zooplankton) of zooplanktivorous coral reef larvae. Moonlight generally suppresses this influx, but lunar periodicity in the timing and intensity of nocturnal brightness may affect vertically migrating predators and prey differently. A major turnover of species occurs at sunset on the reef, with diurnal species seeking shelter and nocturnal species emerging to hunt. The hunting ability of nocturnal reef-based predators is aided by the light of the moon. Consequently, variation in nocturnal illumination is likely to shape the timing of reproduction, larval development, and settlement for many coral reef organisms. This synthesis underscores the potential importance of trophic linkages between coral reefs and adjacent pelagic ecosystems, facilitated by the diel migrations of mesopelagic organisms and the ontogenetic migrations of coral reef larvae. Research is needed to better understand the effects of lunar cycles on life-history strategies, and the potentially disruptive effects of light pollution, turbidity, and climate-driven changes to nocturnal cloud cover. These underappreciated threats may alter patterns of nocturnal illumination that have shaped the evolutionary history of many coral reef organisms, with consequences for larval survival and population replenishment that could rival or exceed other effects arising from climate change.

Lunar rhythms in growth of larval fish.

Growth and survival of larval fishes is highly variable and unpredictable. Our limited understanding of this variation constrains our ability to forecast population dynamics and effectively manage fisheries. Here we show that daily growth rates of a coral reef fish (the sixbar wrasse, Thalassoma hardwicke) are strongly lunar-periodic and predicted by the timing of nocturnal brightness: growth was maximized when the first half of the night was dark and the second half of the night was bright. Cloud cover that obscured moonlight facilitated a 'natural experiment', and confirmed the effect of moonlight on growth. We suggest that lunar-periodic growth may be attributable to light-mediated suppression of diel vertical migrations of predators and prey. Accounting for such effects will improve our capacity to predict the future dynamics of marine populations, especially in response to climate-driven changes in nocturnal cloud cover and intensification of artificial light, which could lead to population declines by reducing larval survival and growth.

Asymmetric competition and floater dynamics.

In territorial species, nonterritorial floaters may be critical to population dynamics. One theoretical framework, based on the assumption that floating is a strategic decision to forego reproduction, predicts that selection maintains an abundant floater population even if low-quality territories are available. However, existing models make two critical assumptions: all individuals have equal competitive ability, and every individual in a population has access to every available territory. We assess the consequences of relaxing these assumptions in a model of asymmetric competition with a trade-off between investment in competitiveness and reproductive success. Our results demonstrate that selection for greater competitiveness eliminates floater production unless the outcome of territorial contests has a strong stochastic component. Next, we suppose individuals can compete for territories only within a fixed neighborhood. If this constraint is sufficiently strong, our model predicts that a population will produce floaters. Finally, we show that our model makes novel predictions regarding the maintenance of trait variation and the relationship between this variation and the distribution of competitors among unequal territories.

Reproductive phenology across the lunar cycle: parental decisions, offspring responses, and consequences for reef fish.

Most organisms reproduce in a dynamic environment, and life-history theory predicts that this can favor the evolution of strategies that capitalize on good times and avoid bad times. When offspring experience these environmental changes, fitness can depend strongly upon environmental conditions at birth and at later life stages. Consequently, fitness will be influenced by the reproductive decisions of parents (i.e., birth date effects) and developmental decisions (e.g., adaptive plasticity) of their offspring. We explored the consequences of these decisions using a highly iteroparous coral reef fish (the sixbar wrasse, Thalassoma hardwicke) and in a system where both parental and offspring environments vary with the lunar cycle. We tested the hypotheses that (1) reproductive patterns and offspring survival vary across the lunar cycle and (2) offspring exhibit adaptive plasticity in development time. We evaluated temporal variation in egg production from February to June 2017, and corresponding larval developmental histories (inferred from otolith microstructure) of successful settlers and surviving juveniles that were spawned during that same period. We documented lunar-cyclic variation in egg production (most eggs were spawned at the new moon). This pattern was at odds with the distribution of birth dates of settlers and surviving juveniles-most individuals that successfully survived to settlement and older stages were born during the full moon. Consequently, the probability of survival across the larval stage was greatest for offspring born close to the full moon, when egg production was at its lowest. Offspring also exhibited plasticity in developmental duration, adjusting their age at settlement to settle during darker portions of the lunar cycle than expected given their birth date. Offspring born near the new moon tended to be older and larger at settlement, and these traits conveyed a strong fitness advantage (i.e., a carryover effect) through to adulthood. We speculate that these effects (1) are shaped by a dynamic landscape of risk and reward determined by moonlight, which differentially influences adults and offspring, and (2) can explain the evolution of extreme iteroparity in sixbars.

Bad neighbors: how spatially disjunct habitat degradation can cause system-wide population collapse.

Movement of individuals links the effects of local variation in habitat quality with growth and persistence of populations at the landscape scale. When the populations themselves are linked by interspecific interactions, such as predation, differential movement between habitats may lead to counterintuitive system-wide dynamics. Understanding the interaction between local drivers and dynamics of widely dispersed species is necessary to predict the impacts of habitat fragmentation and degradation, which may be transmitted across habitat boundaries by species' movements. Here we model predator-prey interactions across unaltered and degraded habitat areas, and we explore the additional effects of adaptive habitat choice by predators on the resilience of prey populations. We show how movement between habitats can produce the "bad neighbor effect," in which predators' response to localized habitat degradation causes system-wide loss of prey populations. This effect arises because adaptive foraging results in the concentration of predators in the more productive unaltered habitat, even when this habitat can not support the increased prey mortality. The mechanisms underlying this effect are especially sensitive to prey dispersal rate and adaptive predator behavior.

Alternative Stable States, Coral Reefs, and Smooth Dynamics with a Kick.

We consider a computer simulation, which was found to be faithful to time series data for Caribbean coral reefs, and an analytical model to help understand the dynamics of the simulation. The analytical model is a system of ordinary differential equations (ODE), and the authors claim this model demonstrates the existence of alternative stable states. The existence of an alternative stable state should consider a sudden shift in coral and macroalgae populations, while the grazing rate remains constant. The results of such shifts, however, are often confounded by changes in grazing rate. Although the ODE suggest alternative stable states, the ODE need modification to explicitly account for shifts or discrete events such as hurricanes. The goal of this paper will be to study the simulation dynamics through a simplified analytical representation. We proceed by modifying the original analytical model through incorporating discrete changes into the ODE. We then analyze the resulting dynamics and their bifurcations with respect to changes in grazing rate and hurricane frequency. In particular, a "kick" enabling the ODE to consider impulse events is added. Beyond adding a "kick" we employ the grazing function that is suggested by the simulation. The extended model was fit to the simulation data to support its use and predicts the existence cycles depending nonlinearly on grazing rates and hurricane frequency. These cycles may bring new insights into consideration for reef health, restoration and dynamics.

Demographic heterogeneity and the dynamics of open populations.

Individuals vary in their phenotype and propensity for growth and survival, but the demographic consequences of this remain poorly understood. We extend previous theoretical work on benthic marine populations and formulate a new model to evaluate how demographic heterogeneity among newly settled reef fish affects population stability. We simulated settlement, growth, and mortality of a small reef fish, the common triplefin (Forsterygion lapillurn) in an open "subpopulation" using a delay-differential equation model framework. We modeled demographic heterogeneity with a discrete number of "quality" types, motivated by our previous empirical observations: individuals were either "high quality" (immigrants from nearby subpopulations) or "low quality" (immigrants from distant subpopulations); in our model, quality influences how quickly individuals develop at a given competitor density. Our results demonstrate how demographic heterogeneity and juvenile competition interact to qualitatively alter the effects of settlement on population stability. Specifically, our model suggests that a mixture of quality types can stabilize the equilibrium even when equal settlement of either type alone would result in an unstable equilibrium. These results highlight the importance of among-individual variation in a metapopulation context, and suggest that in systems where dispersal influences individual quality, connectivity may serve to stabilize local populations.

Linking Dynamic Habitat Selection with Wading Bird Foraging Distributions across Resource Gradients.

Species distribution models (SDM) link species occurrence with a suite of environmental predictors and provide an estimate of habitat quality when the variable set captures the biological requirements of the species. SDMs are inherently more complex when they include components of a species' ecology such as conspecific attraction and behavioral flexibility to exploit resources that vary across time and space. Wading birds are highly mobile, demonstrate flexible habitat selection, and respond quickly to changes in habitat quality; thus serving as important indicator species for wetland systems. We developed a spatio-temporal, multi-SDM framework using Great Egret (Ardea alba), White Ibis (Eudocimus albus), and Wood Stork (Mycteria Americana) distributions over a decadal gradient of environmental conditions to predict species-specific abundance across space and locations used on the landscape over time. In models of temporal dynamics, species demonstrated conditional preferences for resources based on resource levels linked to differing temporal scales. Wading bird abundance was highest when prey production from optimal periods of inundation was concentrated in shallow depths. Similar responses were observed in models predicting locations used over time, accounting for spatial autocorrelation. Species clustered in response to differing habitat conditions, indicating that social attraction can co-vary with foraging strategy, water-level changes, and habitat quality. This modeling framework can be applied to evaluate the multi-annual resource pulses occurring in real-time, climate change scenarios, or restorative hydrological regimes by tracking changing seasonal and annual distribution and abundance of high quality foraging patches.

Consequences of variable larval dispersal pathways and resulting phenotypic mixtures to the dynamics of marine metapopulations.

Larval dispersal can connect distant subpopulations, with important implications for marine population dynamics and persistence, biodiversity conservation and fisheries management. However, different dispersal pathways may affect the final phenotypes, and thus the performance and fitness of individuals that settle into subpopulations. Using otolith microchemical signatures that are indicative of 'dispersive' larvae (oceanic signatures) and 'non-dispersive' larvae (coastal signatures), we explore the population-level consequences of dispersal-induced variability in phenotypic mixtures for the common triplefin (a small reef fish). We evaluate lipid concentration and otolith microstructure and find that 'non-dispersive' larvae (i) have greater and less variable lipid reserves at settlement (and this variability attenuates at a slower rate), (ii) grow faster after settlement, and (iii) experience similar carry-over benefits of lipid reserves on post-settlement growth relative to 'dispersive' larvae. We then explore the consequences of phenotypic mixtures in a metapopulation model with two identical subpopulations replenished by variable contributions of 'dispersive' and 'non-dispersive' larvae and find that the resulting phenotypic mixtures can have profound effects on the size of the metapopulation. We show that, depending upon the patterns of connectivity, phenotypic mixtures can lead to larger metapopulations, suggesting dispersal-induced demographic heterogeneity may facilitate metapopulation persistence.

Determining habitat quality for species that demonstrate dynamic habitat selection.

Determining habitat quality for wildlife populations requires relating a species' habitat to its survival and reproduction. Within a season, species occurrence and density can be disconnected from measures of habitat quality when resources are highly seasonal, unpredictable over time, and patchy. Here we establish an explicit link among dynamic selection of changing resources, spatio-temporal species distributions, and fitness for predictive abundance and occurrence models that are used for short-term water management and long-term restoration planning. We used the wading bird distribution and evaluation models (WADEM) that estimate (1) daily changes in selection across resource gradients, (2) landscape abundance of flocks and individuals, (3) conspecific foraging aggregation, and (4) resource unit occurrence (at fixed 400 m cells) to quantify habitat quality and its consequences on reproduction for wetland indicator species. We linked maximum annual numbers of nests detected across the study area and nesting success of Great Egrets (Ardea alba), White Ibises (Eudocimus albus), and Wood Storks (Mycteria americana) over a 20-year period to estimated daily dynamics of food resources produced by WADEM over a 7490 km(2) area. For all species, increases in predicted species abundance in March and high abundance in April were strongly linked to breeding responses. Great Egret nesting effort and success were higher when birds also showed greater conspecific foraging aggregation. Synthesis and applications: This study provides the first empirical evidence that dynamic habitat selection processes and distributions of wading birds over environmental gradients are linked with reproductive measures over periods of decades. Further, predictor variables at a variety of temporal (daily-multiannual) resolutions and spatial (400 m to regional) scales effectively explained variation in ecological processes that change habitat quality. The process used here allows managers to develop short- and long-term conservation strategies that (1) consider flexible behavioral patterns and (2) are robust to environmental variation over time.

Life history and matrix heterogeneity interact to shape metapopulation connectivity in spatially structured environments.

Metapopulation models have historically treated a landscape as a collection of habitat patches separated by a matrix of uniformly unsuitable habitat. This perspective is still apparent in many studies of marine metapopulations, in which recruitment variation is generally assumed to be primarily the result of variability in ocean currents and interactions with disperser behavior, with little consideration of spatial structure that can affect disperser viability. We use a simple model of dispersal of marine larvae to demonstrate how heterogeneity in dispersal habitat (i.e., the matrix) can generate substantial spatial variation in recruitment. Furthermore, we show how this heterogeneity can interact with larval life-history variation to create alternative patterns of source-sink dynamics. Finally, we place our results in the context of spatially structured matrix population models, and we propose the damping ratio of the connectivity matrix as a general and novel measure of landscape connectivity that may provide conceptual unification to the fields of metapopulation biology and landscape ecology.

Effects of life history variation on vertical transfer of toxicants in marine mammals.

Toxicant bioaccumulation poses a risk to many marine mammal populations. Although individual-level toxicology has been the subject of considerable research in several species, we lack a theoretical framework to generalize the results across environments and life histories. Here we formulate a dynamic energy budget model to predict the effects of intra- and interspecific life history variation on toxicant dynamics in marine mammals. Dynamic energy budget theory attempts to describe the most general processes of energy acquisition and utilization in heterotrophs. We tailor the basic model to represent the marine mammal reproductive cycle, and we add a model of toxicant uptake and partitioning to describe vertical transfer of toxicants from mother to offspring during gestation and lactation. We first show that the model predictions are consistent with qualitative patterns reported in empirical studies and previous species-specific modeling studies. Next, we use this model to examine the dependence of offspring toxicant load on birth order, food density, and interspecific life history variation.

Poaching, enforcement, and the efficacy of marine reserves.

Marine reserves are promoted as an effective supplement to traditional fishery management techniques of harvest quotas and effort limitation. However, quantitative fishery models have ignored the impact of noncompliance (poaching). Here we link a model of a harvested fish population to a game-theoretic representation of fisherman behavior to quantify the effect of poaching on fishery yield and the enforcement effort required to maintain any desired level of reserve effectiveness. Although higher fish densities inside reserves will typically entice fishermen to poach, we show that the initial investment in enforcement efforts provides the greatest return on maintaining the benefits of the reserve to the fishery. Furthermore, we find that poaching eliminates the positive effect of fish dispersal on yield that is predicted by traditional models that ignore fisherman behavior. Our results broaden a fundamental insight from previous models of marine reserves, the effective equivalence of the harvest quota and reserve fraction, to the more realistic scenario in which fishermen attempt to maximize their economic payoffs.

Sequential decision-making in a variable environment: modeling elk movement in Yellowstone National Park as a dynamic game.

We develop a suite of models with varying complexity to predict elk movement behavior during the winter on the Northern Range of Yellowstone National Park (YNP). The models range from a simple representation of optimal patch choice to a dynamic game, and we show how the underlying theory in each is related by the presence or absence of state- and frequency-dependence. We compare predictions from each of the models for three variables that are of basic and applied interest: elk survival, aggregation, and use of habitat outside YNP. Our results suggest that despite low overall forage depletion in the winter, frequency-dependence is crucial to the predictions for elk movement and distribution. Furthermore, frequency-dependence interacts with mass-dependence in the predicted outcome of elk decision-making. We use these results to show how models that treat single movement decisions in isolation from the seasonal sequence of decisions are insufficient to capture landscape scale behavior.

Transient dynamics limit the effectiveness of keystone predation in bringing about coexistence.

We analyze the transient dynamics of simple models of keystone predation, in which a predator preferentially consumes the dominant of two (or more) competing prey species. We show that coexistence is unlikely in many systems characterized both by successful invasion of either prey species into the food web that lacks it and by a stable equilibrium with high densities of all species. Invasion of the predator-resistant consumer species often causes the resident, more vulnerable prey to crash to such low densities that extinction would occur for many realistic population sizes. Subsequent transient cycles may entail very low densities of the predator or of the initially successful invader, which may also preclude coexistence of finite populations. Factors causing particularly low minimum densities during the transient cycles include biotic limiting resources for the prey, limited resource partitioning between the prey, a highly efficient predator with relatively slow dynamics, and a vulnerable prey whose population dynamics are rapid relative to the less vulnerable prey. Under these conditions, coexistence of competing prey via keystone predation often requires that the prey's competitive or antipredator characteristics fall within very narrow ranges. Similar transient crashes are likely to occur in other food webs and food web models.