Schooling of light reflecting fish.

One of the hallmarks of the collective movement of large schools of pelagic fish are waves of shimmering flashes that propagate across the school, usually following an attack by a predator. Such flashes arise when sunlight is reflected off the specular (mirror-like) skin that characterizes many pelagic fishes, where it is otherwise thought to offer a means for camouflage in open waters. While it has been suggested that these 'shimmering waves' are a visual manifestation of the synchronized escape response of the fish, the phenomenon has been regarded only as an artifact of esthetic curiosity. In this study we apply agent-based simulations and deep learning techniques to show that, in fact, shimmering waves contain information on the behavioral dynamics of the school. Our analyses are based on a model that combines basic rules of collective motion and the propagation of light beams in the ocean, as they hit and reflect off the moving fish. We use the resulting reflection patterns to infer the essential dynamics and inter-individual interactions which are necessary to generate shimmering waves. Moreover, we show that light flashes observed by the school members themselves may extend the range at which information can be communicated across the school. Assuming that fish pay heed to this information, for example by entering an apprehensive state of reduced response-time, our analysis suggests that it can speed up the propagation of information across the school. Further still, we use an artificial neural network to show that light flashes are, on their own, indicative of the state and dynamics of the school, and are sufficient to infer the direction of attack and the shape of the school with high accuracy.

Evidence for a consistent use of external cues by marine fish larvae for orientation.

The larval stage is the main dispersive process of most marine teleost species. The degree to which larval behavior controls dispersal has been a subject of debate. Here, we apply a cross-species meta-analysis, focusing on the fundamental question of whether larval fish use external cues for directional movement (i.e., directed movement). Under the assumption that directed movement results in straighter paths (i.e., higher mean vector lengths) compared to undirected, we compare observed patterns to those expected under undirected pattern of Correlated Random Walk (CRW). We find that the bulk of larvae exhibit higher mean vector lengths than those expected under CRW, suggesting the use of external cues for directional movement. We discuss special cases which diverge from our assumptions. Our results highlight the potential contribution of orientation to larval dispersal outcomes. This finding can improve the accuracy of larval dispersal models, and promote a sustainable management of marine resources.

Toward Naturalistic Neuroscience of Navigation: Opportunities in Coral Reef Fish.

The ability to navigate in the world is crucial to many species. One of the most fundamental unresolved issues in understanding animal navigation is how the brain represents spatial information. Although navigation has been studied extensively in many taxa, the key efforts to determine the neural basis of navigation have focused on mammals, usually in lab experiments, where the allocated space is typically very small; e.g., up to one order of magnitude the size of the animal, is limited by artificial walls, and contains only a few objects. This type of setting is vastly different from the habitat of animals in the wild, which is open in many cases and is virtually limitless in size compared to its inhabitants. Thus, a fundamental open question in animal navigation is whether small-scale, spatially confined, and artificially crafted lab experiments indeed reveal how navigation is enacted in the real world. This question is difficult to study given the technical problems associated with in vivo electrophysiology in natural settings. Here, we argue that these difficulties can be overcome by implementing state of the art technology when studying the rivulated rabbitfish, Siganus rivulatus as the model animal. As a first step toward this goal, using acoustic tracking of the reef, we demonstrate that individual S. rivulatus have a defined home range of about 200 m in length, from which they seldom venture. They repeatedly visit the same areas and return to the same sleeping grounds, thus providing evidence for their ability to navigate in the reef environment. Using a clustering algorithm to analyze segments of daily trajectories, we found evidence of specific repeating patterns in behavior within the home range of individual fish. Thus, S. rivulatus appears to have the ability to carry out its daily routines and revisit places of interest by employing sophisticated means of navigation while exploring its surroundings. In the future, using novel technologies for wireless recording from single cells of fish brains, S. rivulatus can emerge as an ideal system to study the neural basis of navigation in natural settings and lead to "electrophysiology in the wild."

A new theoretical performance landscape for suction feeding reveals adaptive kinematics in a natural population of reef damselfish.

Understanding how organismal traits determine performance and, ultimately, fitness is a fundamental goal of evolutionary eco-morphology. However, multiple traits can interact in non-linear and context-dependent ways to affect performance, hindering efforts to place natural populations with respect to performance peaks or valleys. Here, we used an established mechanistic model of suction-feeding performance (SIFF) derived from hydrodynamic principles to estimate a theoretical performance landscape for zooplankton prey capture. This performance space can be used to predict prey capture performance for any combination of six morphological and kinematic trait values. We then mapped in situ high-speed video observations of suction feeding in a natural population of a coral reef zooplanktivore, Chromis viridis, onto the performance space to estimate the population's location with respect to the topography of the performance landscape. Although the kinematics of the natural population closely matched regions of high performance in the landscape, the population was not located on a performance peak. Individuals were furthest from performance peaks on the peak gape, ram speed and mouth opening speed trait axes. Moreover, we found that the trait combinations in the observed population were associated with higher performance than expected by chance, suggesting that these combinations are under selection. Our results provide a framework for assessing whether natural populations occupy performance optima.

Shift and homogenization of gut microbiome during invasion in marine fishes.

Biological invasion is one of the main components of global changes in aquatic ecosystems. Unraveling how establishment in novel environments affects key biological features of animals is a key step towards understanding invasion. Gut microbiome of herbivorous animals is important for host health but has been scarcely assessed in invasive species. Here, we characterized the gut microbiome of two invasive marine herbivorous fishes (Siganus rivulatus and Siganus luridus) in their native (Red Sea) and invaded (Mediterranean Sea) ranges. The taxonomic and phylogenetic diversity of the microbiome increased as the fishes move away from the native range and its structure became increasingly different from the native microbiome. These shifts resulted in homogenization of the microbiome in the invaded range, within and between the two species. The shift in microbial diversity was associated with changes in its functions related with the metabolism of short-chain fatty acids. Altogether, our results suggest that the environmental conditions encountered by Siganidae during their expansion in Mediterranean ecosystems strongly modifies the composition of their gut microbiome along with its putative functions. Further studies should pursue to identify the precise determinants of these modifications (e.g. changes in host diet or behavior, genetic differentiation) and whether they participate in the ecological success of these species.

Light flashes and the geometry of specular fish schools.

The risk of predation presents a difficult challenge in environments that offer no physical shelter, such as the open waters of the world's seas. In the absence of hiding places, many marine fishes turn to two main anti-predator strategies: aggregation and camouflage, which, mostly, have been studied separately. Here, we consider both aspects together and examine the visual imprint of fish schools of different sizes and geometries, given that camouflage is attained by specular (mirror-like) skin texture. To do so, we developed ray-tracing simulations that model the passage of sunbeams as they go through an optically realistic aquatic environment and reflect off the skins of the fish. We find that due to frequent high-intensity specular reflections (light flashes), the marginal increase in detectability with increasing school size is significantly higher than previously estimated under the assumption of diffusive reflection. However, we also find that by increasing density and alignment the fish can mitigate the detectability of individuals, albeit at the expense of the detectability of the school as a whole. Our findings provide a new perspective on documented responses to threat by schooling pelagic fishes and underscore the importance of the optical signature of animals in structuring their behaviour.

Treatment-level impacts of microplastic exposure may be confounded by variation in individual-level responses in juvenile fish.

Microplastic (MP) pollution is a key global environmental issue and laboratory exposure studies on aquatic biota are proliferating at an exponential rate. However, most research is limited to treatment-level effects, ignoring that there may be substantial within-population variation in responses to anthropogenic stressors. MP exposure experiments often reveal considerable, yet largely overlooked, inter-individual variation in particle uptake within concentration treatments. Here, we investigated to what degree treatment-level responses to MP exposure may be affected by variation in MP ingestion rates in the early life stages of a marine fish, the Gilt-head seabream, Sparus aurata. First, we tested whether MP ingestion variation is repeatable. Second, we assessed to what degree this variation may determine individual-level effects of MP exposure on fitness-related behavioural performance (i.e., escape response). We found that consistent inter-individual variation in MP ingestion was prevalent and led to differential impacts within exposure treatments. Individuals with high MP ingestion rates exhibited markedly inferior escape responses, a result that was partially concealed in treatment-level analyses. Our findings show that the measured response of populations to environmental perturbations could be confounded by variation in individual-level responses and that the explicit integration of MP ingestion variation can reveal cryptic patterns during exposure experiments.

Quantitative species-level ecology of reef fish larvae via metabarcoding.

The larval pool of coral reef fish has a crucial role in the dynamics of adult fish populations. However, large-scale species-level monitoring of species-rich larval pools has been technically impractical. Here, we use high-throughput metabarcoding to study larval ecology in the Gulf of Aqaba, a region that is inhabited by >500 reef fish species. We analysed 9,933 larvae from 383 samples that were stratified over sites, depth and time. Metagenomic DNA extracted from pooled larvae was matched to a mitochondrial cytochrome c oxidase subunit I barcode database compiled for 77% of known fish species within this region. This yielded species-level reconstruction of the larval community, allowing robust estimation of larval spatio-temporal distributions. We found significant correlations between species abundance in the larval pool and in local adult assemblages, suggesting a major role for larval supply in determining local adult densities. We documented larval flux of species whose adults were never documented in the region, suggesting environmental filtering as the reason for the absence of these species. Larvae of several deep-sea fishes were found in shallow waters, supporting their dispersal over shallow bathymetries, potentially allowing Lessepsian migration into the Mediterranean Sea. Our method is applicable to any larval community and could assist coral reef conservation and fishery management efforts.

Auto-correlated directional swimming can enhance settlement success and connectivity in fish larvae.

Larvae of coastal-marine fishes have been shown repeatedly to swim directionally in the pelagic environment. Yet, biophysical models of larval dispersal typically impose a Simple Random Walk (SRW) algorithm to simulate non-directional movement in the open ocean. Here we investigate the use of a Correlated Random Walk (CRW) algorithm; imposing auto-correlated directional swimming onto simulated larvae within a high-resolution 3D biophysical model of the Gulf of Aqaba, the Red Sea. Our findings demonstrate that implementation of auto-correlated directional swimming can result in an increase of up to ×2.7 in the estimated success rate of larval-settlement, as well as an increase in the extent of connectivity. With accumulating empirical support for the capacity for directional-swimming during the pelagic phase, we propose that CRW should be applied in biophysical models of dispersal by coastal marine fish-larvae.

Large but uneven reduction in fish size across species in relation to changing sea temperatures.

Ectotherms often attain smaller body sizes when they develop at higher temperatures. This phenomenon, known as the temperature-size rule, has important consequences for global fisheries, whereby ocean warming is predicted to result in smaller fish and reduced biomass. However, the generality of this phenomenon and the mechanisms that drive it in natural populations remain unresolved. In this study, we document the maximal size of 74 fish species along a steep temperature gradient in the Mediterranean Sea and find strong support for the temperature-size rule. Importantly, we additionally find that size reduction in active fish species is dramatically larger than for more sedentary species. As the temperature dependence of oxygen consumption depends on activity levels, these findings are consistent with the hypothesis that oxygen is a limiting factor shaping the temperature-size rule in fishes. These results suggest that ocean warming will result in a sharp, but uneven, reduction in fish size that will cause major shifts in size-dependent interactions. Moreover, warming will have major implications for fisheries as the main species targeted for harvesting will show the most substantial declines in biomass.

Correlations between Circadian Rhythms and Growth in Challenging Environments.

In plants, the circadian system controls a plethora of processes, many with agronomic importance, such as photosynthesis, photoprotection, stomatal opening, and photoperiodic development, as well as molecular processes, such as gene expression. It has been suggested that modifying circadian rhythms may be a means to manipulate crops to develop improved plants for agriculture. However, there is very little information on how the clock influences the performance of crop plants. We used a noninvasive, high-throughput technique, based on prompt chlorophyll fluorescence, to measure circadian rhythms and demonstrated that the technique works in a range of plants. Using fluorescence, we analyzed circadian rhythms in populations of wild barley (Hordeum vulgare ssp. spontaneum) from widely different ecogeographical locations in the Southern Levant part of the Fertile Crescent, an area with a high proportion of the total genetic variation of wild barley. Our results show that there is variability for circadian traits in the wild barley lines. We observed that circadian period lengths were correlated with temperature and aspect at the sites of origin of the plants, while the amplitudes of the rhythms were correlated with soil composition. Thus, different environmental parameters may exert selection on circadian rhythms.

Heterogeneous 'proportionality constants' - A challenge to Taylor's Power Law for temporal fluctuations in abundance.

Taylor's Power Law for the temporal fluctuation in population size (TL) posits that the variance in abundance scales according to aM(b); where M is the mean abundance and a and b are the 'proportionality' and 'scaling' coefficients. As one of the few empirical rules in population ecology, TL has attracted substantial theoretical and empirical attention. Much of this attention focused on the scaling coefficient; particularly its ubiquitous deviation from the null value of 2. Here we present a line of reasoning that challenges the power-law interpretation of the empirical log-linear relationship between the mean and variance of population size. At the core of our reasoning is the proposition that populations vary not only with respect to M but also with respect to a; which leaves the log-linear relationship intact but forfeits its power-law interpretation. Using the stochastic logistic-growth model as an example, we show that ignoring among-population variation in a is akin to ignoring the variation in the intrinsic rate of growth (r). Accordingly, we show that the slope of the log-linear relationship (b) is a function of the among-population (co)variation in r and the carrying-capacity. We further demonstrate that local environmental stochasticity is sufficient to generate the full range of observed values of b, and that b can in fact be insensitive to substantial differences in the balance between variance-generating and stabilizing processes.

Social foraging with partial (public) information.

Group foragers can utilize public information to better estimate patch quality and arrive at more efficient patch-departure rules. However, acquiring such information may come at a cost; e.g. reduced search efficiency. We present a Bayesian group-foraging model in which social foragers do not require full awareness of their companions' foraging success; only of their number. In our model, patch departure is based on direct estimates of the number of remaining items. This is achieved by considering all likely combinations of initial patch-quality and group foraging-success; given the individual forager's experience within the patch. Slower rates of information-acquisition by our 'partially-aware' foragers lead them to over-utilize poor patches; more than fully-aware foragers. However, our model suggests that the ensuing loss in long-term intake-rates can be matched by a relatively low cost to the acquisition of full public information. In other words, we suggest that group-size offers sufficient information for optimal patch utilization by social foragers. We suggest, also, that our model is applicable to other situations where resources undergo 'background depletion', which is coincident but independent of the consumer's own utilization.

Polarized light sensitivity and orientation in coral reef fish post-larvae.

Recent studies of the larvae of coral-reef fishes reveal that these tiny vertebrates possess remarkable swimming capabilities, as well as the ability to orient to olfactory, auditory, and visual cues. While navigation according to reef-generated chemicals and sounds can significantly affect dispersal, the effect is limited to the vicinity of the reef. Effective long-distance navigation requires at least one other capacity-the ability to maintain a bearing using, for example, a sun compass. Directional information in the sun's position can take the form of polarized-light related cues (i.e., e-vector orientation and percent polarization) and/or non-polarized-light related cues (i.e., the direct image of the sun, and the brightness and spectral gradients). We examined the response to both types of cues using commercially-reared post-larvae of the spine-cheeked anemonefish Premnas biaculeatus. Initial optomotor trials indicated that the post-larval stages are sensitive to linearly polarized light. Swimming directionality was then tested using a Drifting In-Situ Chamber (DISC), which allowed us to examine the response of the post-larvae to natural variation in light conditions and to manipulated levels of light polarization. Under natural light conditions, 28 of 29 post-larvae showed significant directional swimming (Rayleigh's test p<0.05, R = 0.74±0.23), but to no particular direction. Swimming directionality was positively affected by sky clarity (absence of clouds and haze), which explained 38% of the observed variation. Moreover, post-larvae swimming under fully polarized light exhibited a distinct behavior of tracking the polarization axis, as it rotated along with the DISC. This behavior was not observed under partially-polarized illumination. We view these findings as an indication for the use of sun-related cues, and polarized light signal in specific, by orienting coral-reef fish larvae.

Evidence for cohesive dispersal in the sea.

As with many marine species, the vast majority of coral-reef fishes have a bipartite life cycle consisting of a dispersive larval stage and a benthic adult stage. While the potentially far-reaching demographic and ecological consequences of marine dispersal are widely appreciated, little is known of the structure of the larval pool and of the dispersive process itself. Utilizing Palindrome Sequence Analysis of otolith micro-chemistry (PaSA;) we show that larvae of Neopomacentrus miryae (Pomacentridae) appear to remain in cohesive cohorts throughout their entire pelagic larval duration (PLD; ~28 days). Genetically, we found cohort members to be maternally (mtDNA) unrelated. While physical forcing cannot be negated as contributing to initial cohort formation, the small scale of the observed spatial structure suggests that some behavioral modification may be involved from a very early age. This study contributes to our ongoing re-evaluation of the processes that structure marine populations and communities and the spatial scales at which they operate.

Functional changes of the visual system of the damselfish Dascyllus marginatus along its bathymetric range.

Shallow-water zooplanktivorous fish rely on their vision for foraging. In shallow water, feeding efficiency decreases in dim light and thus the fish cease foraging at crepuscular hours. Creatures living in the lower parts of their depth ranges are expected to be exposed to limited light levels for longer hours. However, observations of the zooplanktivore Dascyllus marginatus showed little change in foraging duration down to 40m deep. We asked whether the visual system's functionality changes with depth along the depth range of this damselfish; we examined eye and retina anatomy for changes in visual acuity and light sensitivity and used the optomotor response to test for spatial and temporal light summation. We found only minor changes in the anatomy of the eye that are not expected to affect visual sensitivity or acuity. However, behavioural experiments showed that the deeper water fish's test performance exceeded those of fish in shallow water under lower light levels. We found that deeper water fish responded to the optomotor test at lower light levels and also had more discriminating visual acuity in low light, which can increase their potential reactive distance. The plastic adaptive ability of the visual system to low light levels may explain the fish's ability to inhabit deeper reef habitats and thus expand their depth range limits.

The effect of adult aggression on habitat selection by settlers of two coral-dwelling damselfishes.

Coral-reef fishes experience a major challenge when facing settlement in a multi-threat environment, within which, using settlement cues, they need to select a suitable site. Studies in laboratories and artificial setups have shown that the presence of conspecific adults often serves as a positive settlement cue, whose value is explained by the increased survival of juveniles in an already proven fit environment. However, settlement in already inhabited corals may expose the recruits to adult aggression. Daily observations and manipulation experiments were used in the present study, which was conducted in the natural reef. We revealed differential strategies of settlers, which do not necessarily join conspecific adults. Dascyllus aruanus prefer to settle near (not with) their aggressive adults, and to join them only after gaining in size; whereas Dascyllus marginatus settlers in densely populated reefs settle independently of their adult distribution. Our results present different solutions to the challenges faced by fish recruits while selecting their microhabitat, and emphasize the complexity of habitat selection by the naïve settlers. Although laboratory experiments are important to the understanding of fish habitat selection, further studies in natural habitats are essential in order to elucidate the actual patterns of settlement and habitat selection, which are crucial for the survival of coral-reef fish populations.

Estimating the rate of biological introductions: Lessepsian fishes in the Mediterranean.

Sampling issues preclude the direct use of the discovery rate of exotic species as a robust estimate of their rate of introduction. Recently, a method was advanced that allows maximum-likelihood estimation of both the observational probability and the introduction rate from the discovery record. Here, we propose an alternative approach that utilizes the discovery record of native species to control for sampling effort. Implemented in a Bayesian framework using Markov chain Monte Carlo simulations, the approach provides estimates of the rate of introduction of the exotic species, and of additional parameters such as the size of the species pool from which they are drawn. We illustrate the approach using Red Sea fishes recorded in the eastern Mediterranean, after crossing the Suez Canal, and show that the two approaches may lead to different conclusions. The analytical framework is highly flexible and could provide a basis for easy modification to other systems for which first-sighting data on native and introduced species are available.

Oviposition habitat selection in response to risk of predation in temporary pools: mode of detection and consistency across experimental venue.

Natural selection should favor females that avoid ovipositing where risk of predation is high for their progeny. Despite the large consequences of such oviposition behavior for individual fitness, population dynamics, and community structure, relatively few studies have tested for this behavior. Moreover, these studies have rarely assessed the mode of detection of predators, compared responses in prey species that vary in vulnerability to predators, or tested for the behavior in natural habitats. In an outdoor artificial pool experiment, we tested the oviposition responses of two dipteran species, Culiseta longiareolata (mosquito) and Chironomus riparius (midge), to the hemipteran predator, Notonecta maculata. Both dipteran species have similar life history characteristics, but Culiseta longiareolata larvae are highly vulnerable to predation by Notonecta, while Chironomus riparius larvae are not. As their vulnerabilities would suggest, Culiseta longiareolata, but not Chironomus riparius, strongly avoided ovipositing in pools containing Notonecta. An experiment in natural rock pools assessing oviposition by Culiseta longiareolata in response to Notonecta maculata yielded an oviposition pattern highly consistent with that of the artificial pool experiment. We also demonstrated that the cue for oviposition avoidance by Culiseta longiareolata was a predator-released chemical: Notonecta water (without Notonecta replenishment) repelled oviposition for 8 days. Oviposition avoidance and mode of detection of the predator have important implications for how to assess the true impact of predators and for the use of commercially produced kairomones for mosquito control.