Paternal care regulates the timing, synchrony and success of hatching in a coral reef fish.

In oviparous species, the timing of hatching is a crucial decision, but for developing embryos, assessing cues that indicate the optimal time to hatch is challenging. In species with pre-hatching parental care, parents can assess environmental conditions and induce their offspring to hatch. We provide the first documentation of parental hatching regulation in a coral reef fish, demonstrating that male neon gobies (Elacatinus colini) directly regulate hatching by removing embryos from the clutch and spitting hatchlings into the water column. All male gobies synchronized hatching within 2 h of sunrise, regardless of when eggs were laid. Paternally incubated embryos hatched later in development, more synchronously, and had higher hatching success than artificially incubated embryos that were shaken to provide a vibrational stimulus or not stimulated. Artificially incubated embryos displayed substantial plasticity in hatching times (range: 80-224 h post-fertilization), suggesting that males could respond to environmental heterogeneity by modifying the hatching time of their offspring. Finally, paternally incubated embryos hatched with smaller yolk sacs and larger propulsive areas than artificially incubated embryos, suggesting that paternal effects on hatchling phenotypes may influence larval dispersal and fitness. These findings highlight the complexity of fish parental care behaviour and may have important, and currently unstudied, consequences for fish population dynamics.

An integrative investigation of sensory organ development and orientation behavior throughout the larval phase of a coral reef fish.

The dispersal of marine larvae determines the level of connectivity among populations, influences population dynamics, and affects evolutionary processes. Patterns of dispersal are influenced by both ocean currents and larval behavior, yet the role of behavior remains poorly understood. Here we report the first integrated study of the ontogeny of multiple sensory systems and orientation behavior throughout the larval phase of a coral reef fish-the neon goby, Elacatinus lori. We document the developmental morphology of all major sensory organs (lateral line, visual, auditory, olfactory, gustatory) together with the development of larval swimming and orientation behaviors observed in a circular arena set adrift at sea. We show that all sensory organs are present at hatch and increase in size (or number) and complexity throughout the larval phase. Further, we demonstrate that most larvae can orient as early as 2 days post-hatch, and they swim faster and straighter as they develop. We conclude that sensory organs and swimming abilities are sufficiently developed to allow E. lori larvae to orient soon after hatch, suggesting that early orientation behavior may be common among coral reef fishes. Finally, we provide a framework for testing alternative hypotheses for the orientation strategies used by fish larvae, laying a foundation for a deeper understanding of the role of behavior in shaping dispersal patterns in the sea.

A portfolio of climate-tailored approaches to advance the design of marine protected areas in the Red Sea.

Intensified coastal development is compromising the health and functioning of marine ecosystems. A key example of this is the Red Sea, a biodiversity hotspot subjected to increasing local human pressures. While some marine-protected areas (MPAs) were placed to alleviate these stressors, it is unclear whether these MPAs are managed or enforced, thus providing limited protection. Yet, most importantly, MPAs in the Red Sea were not designed using climate considerations, likely diminishing their effectiveness against global stressors. Here, we propose to tailor the design of MPAs in the Red Sea by integrating approaches to enhance climate change mitigation and adaptation. First, including coral bleaching susceptibility could produce a more resilient network of MPAs by safeguarding reefs from different thermal regions that vary in spatiotemporal bleaching responses, reducing the risk that all protected reefs will bleach simultaneously. Second, preserving the basin-wide genetic connectivity patterns that are assisted by mesoscale eddies could further ensure recovery of sensitive populations and maintain species potential to adapt to environmental changes. Finally, protecting mangrove forests in the northern and southern Red Sea that act as major carbon sinks could help offset greenhouse gas emissions. If implemented with multinational cooperation and concerted effort among stakeholders, our portfolio of climate-tailored approaches may help build a network of MPAs in the Red Sea that protects more effectively its coastal resources against escalating coastal development and climate instability. Beyond the Red Sea, we anticipate this study to serve as an example of how to improve the utility of tropical MPAs as climate-informed conservation tools.

Hydrodynamic and biological constraints on group cohesion in plankton.

The dynamics of plankton in the ocean are determined by biophysical interactions. Although physics and biotic behaviors are known to influence the observed patchiness of planktonic populations, it is still unclear how much, and if, group behavior contributes to this biophysical interaction. Here, we demonstrate how simple rules of behavior can enhance or inhibit active group cohesion in plankton in a turbulent environment. In this study, we used coral-reef fish larvae as a model to investigate the interaction between microscale turbulence and planktonic organisms. We synthesized available information on the swimming speeds and sizes of reef fish larvae, and developed a set of equations to investigate the effects of viscosity and turbulence on larvae dispersion. We then calculated the critical dispersion rates for three different swimming strategies - cruise, random-walk, and pause-travel - to determine which strategies could facilitate group cohesion during dispersal. Our results indicate that swimming strategies and migration to low-turbulence regions are the key to maintaining group cohesion, suggesting that many reef fish species have the potential to remain together, from hatching to settlement. In addition, larvae might change their swimming strategies to maintain group cohesion, depending on environmental conditions and/or their ontogenic stage. This study provides a better understanding of the hydrodynamic and biological constraints on group formation and cohesion in planktonic organisms, and reveals a wide range of conditions under which group formation may occur.

Potential roles of smell and taste in the orientation behaviour of coral-reef fish larvae: insights from morphology.

An ontogenetic analysis of the olfactory organ and the number and distribution of internal taste buds was carried out in two neon gobies (Elacatinus lori and Elacatinus colini) with the goal of revealing morphological trends that might inform an understanding of the roles of olfaction and taste in larval orientation behaviour. The pattern of development of the olfactory organ is unremarkable and enclosure of the olfactory epithelium occurs concurrently with metamorphosis and settlement in both species. Like other gobies, juvenile and adult E. lori and E. colini lack complex olfactory lamellae, and lack the accessory nasal sacs present in some adult gobies that could facilitate active olfactory ventilation (i.e., sniffing). A small number of internal taste buds are present at hatch with most found in the caudal region of the buccal cavity (on gill arches, roof of buccal cavity). As taste bud number increases, they demonstrate an anterior spread to the lips, buccal valves and tongue (i.e., tissue covering the basihyal). In the absence of an active ventilatory mechanism for the olfactory organs, the water that moves through the buccal cavity with cyclic gill ventilation may provide chemical cues allowing the internal taste buds to play a role in chemical-mediated orientation and reef-seeking behavior in pelagic larval fishes.

Patterns, causes, and consequences of marine larval dispersal.

Quantifying the probability of larval exchange among marine populations is key to predicting local population dynamics and optimizing networks of marine protected areas. The pattern of connectivity among populations can be described by the measurement of a dispersal kernel. However, a statistically robust, empirical dispersal kernel has been lacking for any marine species. Here, we use genetic parentage analysis to quantify a dispersal kernel for the reef fish Elacatinus lori, demonstrating that dispersal declines exponentially with distance. The spatial scale of dispersal is an order of magnitude less than previous estimates-the median dispersal distance is just 1.7 km and no dispersal events exceed 16.4 km despite intensive sampling out to 30 km from source. Overlaid on this strong pattern is subtle spatial variation, but neither pelagic larval duration nor direction is associated with the probability of successful dispersal. Given the strong relationship between distance and dispersal, we show that distance-driven logistic models have strong power to predict dispersal probabilities. Moreover, connectivity matrices generated from these models are congruent with empirical estimates of spatial genetic structure, suggesting that the pattern of dispersal we uncovered reflects long-term patterns of gene flow. These results challenge assumptions regarding the spatial scale and presumed predictors of marine population connectivity. We conclude that if marine reserve networks aim to connect whole communities of fishes and conserve biodiversity broadly, then reserves that are close in space (<10 km) will accommodate those members of the community that are short-distance dispersers.