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.

Artificial light at night interacts with predatory threat to alter reef fish metabolite profiles.

Light cycles and predatory threat define activity patterns (e.g. feeding/sleeping, activity/rest) in most diurnal fish species. Artificial light at night (ALAN) may disrupt natural cycles and biochemical processes, a mismatch which can eventually reduce condition and fitness. We evaluate the separate and joint effects of ALAN and predator threat on metabolism within brain, liver and muscle tissue of a common, wild caught damselfish, blue green chromis (Chromis viridis). The effects of ALAN varied according to tissue type and predator exposure. In all tissues we observed changes in metabolic pathways associated with increased activity under continuous light (despite provision of shelter), specifically those associated with energy metabolism, cell signalling, responses to oxidative stress and markers of cellular damage. In both the brain and liver tissues, predator threat served to moderate the influence of ALAN on metabolic change, likely due to increased sheltering behaviour. However, no interaction of predator threat with ALAN was observed in metabolism of the muscle tissue. Our results highlight complex sub-acute effects of ALAN exposure on tissue specific and whole organism energy metabolism. Collectively these effects indicate that ALAN has significant scope to reduce fitness of coastal fishes and potentially threaten ecosystem services, but that these changes are highly complex and may be altered by biotic drivers of activity.

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.

Moonlight enhances growth in larval fish.

Moonlight mediates trophic interactions and shapes the evolution of life-history strategies for nocturnal organisms. Reproductive cycles and important life-history transitions for many marine organisms coincide with moon phases, but few studies consider the effects of moonlight on pelagic larvae at sea. We evaluated effects of moonlight on growth of pelagic larvae of a temperate reef fish using "master chronologies" of larval growth constructed from age-independent daily increment widths recorded in otoliths of 321 individuals. We found that daily growth rates of fish larvae were enhanced by lunar illumination after controlling for the positive influence of temperature and the negative influence of cloud cover. Collectively, these results indicate that moonlight enhances growth rates of larval fish. This pattern is likely the result of moonlight's combined effects on foraging efficiency and suppression of diel migrations of mesopelagic predators, and has the potential to drive evolution of marine life histories.

Patterns of selective predation change with ontogeny but not density in a marine fish.

Phenotypic variation is prevalent in the early life-history stages of many organisms and provides the basis for selective mortality on size and growth-related traits of older life stages. Densities of organisms can vary widely at important life-history transitions, raising additional questions about the interplay between selection and density-dependent processes. We evaluate density dependence in patterns of selective mortality for a temperate reef fish. Specifically, we exposed pre-settlement and post-settlement stages of the common triplefin (Forsterygion lapillum) to a natural predator and evaluated patterns of selective mortality on early life-history traits as a function of ontogenetic stage and density. We used otoliths to reconstruct the traits of fish that survived versus fish that were consumed (i.e., we recovered otoliths from the guts of predators), and we estimated selection by analysing the relationship between absolute fitness and standardised traits. Absolute fitness was negatively correlated with size and larval growth rate for pre-settlement fish (i.e., larger and faster growing individuals were more likely to be consumed by predators), and this was consistent across the range of densities evaluated. Post-settlement fish experienced no selective mortality. Additionally, absolute fitness was equal across density treatments, suggesting mortality was density-independent. Collectively, these results suggest that patterns of selection change with ontogeny, but may be stable across densities when mortality is density-independent. Shifts in selective mortality for species with distinct life-stages can mask and complicate relationships between traits and fitness, and the importance of such traits may be underappreciated for earlier life stages.

Interactive effects of shelter and conspecific density shape mortality, growth, and condition in juvenile reef fish.

How landscape context influences density-dependent processes is important, as environmental heterogeneity can confound estimates of density dependence in demographic parameters. Here we evaluate 19 populations in a shoaling temperate reef fish (Trachinops caudimaculatus) metapopulation within a heterogeneous seascape (Port Phillip Bay, Australia) to show empirically that shelter availability and population density interact to influence juvenile mortality, growth and condition. Although heterogeneity in shelter availability obscured the underlying patterns of density dependence in different ways, the combination of habitat and its interaction with density were two to six times more important than density alone in explaining variation in demographic parameters for juveniles. These findings contradict many small-scale studies and highlight the need for landscape-scale observations of how density dependence interacts with resource availability and competition to better understand how demographic parameters influence the dynamics of metapopulations in heterogeneous environments.

Evidence and population consequences of shared larval dispersal histories in a marine fish.

Larval dispersal is disproportionately important for marine population ecolgy and evolution, yet our inability to track individuals severely constrains our understanding of this key process. We analyze otoliths of a small reef fish, the common triplefin (Forsterygion lapillum), to reconstruct individual dispersal histories and address the following questions: (1) How many discrete sets of dispersal histories (dispersal cohorts) contribute to replenishment of focal populations; (2) When do dispersal cohorts converge (a metric of shared dispersal histories among cohorts); and (3) Do these patterns predict spatiotemporal variation in larval supply? We used light traps to quantify larval supply, and otolith microstructure and microchemistry (using laser ablation inductively coupled plasma mass spectrometry; LA-ICP-MS) to reconstruct daily environmental histories of individuals in their 30-d lead-up to settlement. Our results indicate that a variable number of dispersal cohorts replenish focal populations (range of 2-8, mean of 4.3, standard deviation of 2.8). Convergence times varied (from 0 to > 30 d prior to settlement), and larval supply was negatively correlated with cohort evenness but not with the number of cohorts, or when they converged, indicating disproportionately large contributions from some cohorts (i.e., sweepstakes events). Collectively, our results suggest that larval reef fishes may variably disperse in shoals, to drive local replenishment and connectivity within a metapopulation.

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.

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.

The legacy of dispersal: larval experience shapes persistence later in the life of a reef fish.

1. Movement pathways of individuals can be shaped by heterogeneity in the dispersal environment that separates origin and destination patches. However, effects of the dispersal environment on the phenotype (or future fitness) of dispersers is poorly known; individual experiences during dispersal may have latent effects on the performance or persistence of later life-stages. 2. We evaluated such 'legacy effects' for dispersing reef fish larvae using (i) otolith (ear stone) microchemistry to characterize two distinct dispersal pathways and (ii) otolith microstructure to estimate 'larval quality' (a composite of five measured larval phenotypes). We conducted a reciprocal transplant field experiment to evaluate selective mortality after dispersal as a function of larval quality. We conducted longitudinal sampling of natural cohorts of reef fish through to adulthood to quantify shifts in the distribution of larval quality in local populations. 3. We found the quality of dispersers to be variable and determined by their experience in the larval dispersal environment. Larval quality of successful dispersers predicted their subsequent survival after dispersal in reciprocal transplant experiments. Longitudinal sampling was consistent with short-term field experiments, and revealed that survivors to adulthood were disproportionately comprised of high quality larval dispersers. 4. Overall, our results suggest that conditions in the dispersal environment shape future fitness of individuals after successful dispersal, and that this can indirectly mediate dispersal patterns and connectivity in a metapopulation.

The vermetid gastropod Dendropoma maximum reduces coral growth and survival.

Coral reefs are one of the most diverse systems on the planet; yet, only a small fraction of coral reef species have attracted scientific study. Here, we document strong deleterious effects of an often overlooked species-the vermetid gastropod, Dendropoma maximum-on growth and survival of reef-building corals. Our surveys of vermetids on Moorea (French Polynesia) revealed a negative correlation between the density of vermetids and the per cent cover of live coral. Furthermore, the incidence of flattened coral growth forms was associated with the presence of vermetids. We transplanted and followed the fates of focal colonies of four species of corals on natural reefs where we also manipulated presence/absence of vermetids. Vermetids reduced skeletal growth of focal corals by up to 81 per cent and survival by up to 52 per cent. Susceptibility to vermetids varied among coral species, suggesting that vermetids could shift coral community composition. Our work highlights the potential importance of a poorly studied gastropod to coral dynamics.

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.

Larval quality is shaped by matrix effects: implications for connectivity in a marine metapopulation.

Variation in the phenotype or "quality" of dispersing individuals can shape colonization success and thus local dynamics and patterns of connectivity in a metapopulation. In marine reef systems, larval dispersal typically connects fragmented populations, and larval quality may be shaped by developmental history at the natal reef (e.g., parental effects) and/or by conditions in the pelagic environment (e.g., food, temperature, hydrodynamics, predator regime). We extract information recorded within the incremental bands of fish "ear stones" (otoliths) to reconstruct the early life histories of reef fish, to evaluate whether larval quality is a function of natal populations, dispersal histories, or both. We sampled sagittal otoliths from 282 common triplefins (Forsterygion lapillum) collected at approximately weekly, intervals between December 2003 and March 2004, from three sites within Wellington Harbor (New Zealand) and three sites along the adjacent Wellington South Coast. We used image analysis to quantify otolith traits and to reconstruct five larval phenotypes (pelagic larval duration, size-at-hatch, early larval growth, late larval growth, and an instantaneous larval growth rate), followed by a principal components analysis to derive a composite measure of larval quality. We used laser ablation-inductively coupled plasma-mass spectrometry to quantify otolith microchemistry, followed by a set of cluster analyses (based upon 13 statistical descriptors of time series for each of 11 elemental ratios) to identify and characterize two putative natal "source populations" and two putative "larval dispersal histories." We evaluated the relationship between larval quality, source populations, and dispersal histories using two-way ANOVA and MANOVA, and determined that larval quality of F. lapillum is a function of larval dispersal history and not source population identity. Specifically, larvae of F. lapillum with microchemical signatures consistent with retention and/or entrainment in the nutrient-enriched Wellington Harbor had traits associated with elevated larval quality (i.e., short pelagic larval durations, small size-at-hatch, fast larval growth, and fast instantaneous growth rates). Our results suggest that conditions in the pelagic larval environment shape larval quality and potentially mediate metapopulation connectivity. In the case of F. lapillum from Wellington Harbor, environmentally induced heterogeneity in larval quality may limit connectivity by favoring successful replenishment by locally retained larvae over long-distance dispersers.

Quantifying site quality in a heterogeneous landscape: recruitment of a reef fish.

Heterogeneity in site quality can play an important role in patterns of abundance and population dynamics. Yet, estimating site quality in natural systems can be problematic because site quality can (1) vary through ontogeny for a focal organism, leading to shifts in site quality with age, (2) be confounded with (or masked by) variation in traits of individuals populating the sites, and (3) be correlated with local density. For example, if high-quality sites attract more individuals but vital rates are density dependent, then observed vital rates will be relatively homogeneous in space despite strong heterogeneity in site quality. Here, we operationally define site quality for a reef fish as the mean survival time of juveniles transplanted to sites at a common density and size structure, with random assignment of individuals to sites to remove potential confounding effects of local variation in individual quality and density. Our assays using juvenile age classes of the six-bar wrasse (Thalassoma hardwicke) showed that site quality varied in space (i.e., among patch reefs) but was constant through time. Site quality increased with availability of the branching coral Pocillopora (which is used as a refuge), but decreased with density of a predator, the arc-eye hawkfish, Paracirrhites arcatus (which also uses Pocillopora). We experimentally added colonies of Pocillopora to reefs and (1) increased site quality, (2) enhanced natural settlement rates of six-bar wrasse, but (3) attracted more hawkfish predators, and (4) did not increase survival of juvenile fish under ambient densities. Our results suggest that Pocillopora increases site quality, but attracts greater densities of settlers and predators, resulting in increased density dependence and predation, which mask the underlying effects of Pocillopora on site quality (supporting the hypothesis of "cryptic density dependence"). Variation in site quality and the possible confounding effects of density and individual traits warrant more experimental study.

Regulation of local populations of a coral reef fish via joint effects of density- and number-dependent mortality.

Density-dependent mortality can regulate local populations - effectively minimizing the likelihood of local extinctions and unchecked population growth. It is considered particularly important for many marine reef organisms with demographically open populations that lack potential regulatory mechanisms tied to local reproduction. While density-dependent mortality has been documented frequently for reef fishes, few studies have explored how the strength of density-dependence varies with density, or how density-dependence may be modified by numerical effects (i.e., number-dependent mortality). Both issues can have profound effects on spatial patterns of abundance and the regulation of local populations. I address these issues through empirical studies in Moorea, French Polynesia, of the six bar wrasse (Thalassoma hardwicke), a reef fish that settles to isolated patch reefs. Per capita mortality rates of newly settled wrasse increased as a function of density and were well approximated by the Beverton-Holt function for both naturally formed and experimentally generated juvenile cohorts. Average instantaneous mortality rates were a decelerating function of initial densities, indicating the per capita strength of density-dependence decreased with density. Results of a factorial manipulation of density and group size indicate that per capita mortality rates were simultaneously density- and number-dependent; fish at higher densities and/or in groups had higher probabilities of disappearing from patch reefs compared with fish that were solitary and/or at lower densities. Mortality rates were ~30% higher for fish at densities of 0.5 fish/m2 than at 0.25 fish/m2. Similarly, mortality rates increased by ~45% when group size was increased from 1 to 2 individuals per patch, even when density was kept constant. These observations suggest that the number of interacting individuals, independent of patch size (i.e., density-independent effects) can contribute to regulation of local populations. Overall, this work highlights a greater need to consider numerical effects in addition to density effects when exploring sources of population regulation.