Linking vertical movements of large pelagic predators with distribution patterns of biomass in the open ocean.

Many predator species make regular excursions from near-surface waters to the twilight (200 to 1,000 m) and midnight (1,000 to 3,000 m) zones of the deep pelagic ocean. While the occurrence of significant vertical movements into the deep ocean has evolved independently across taxonomic groups, the functional role(s) and ecological significance of these movements remain poorly understood. Here, we integrate results from satellite tagging efforts with model predictions of deep prey layers in the North Atlantic Ocean to determine whether prey distributions are correlated with vertical habitat use across 12 species of predators. Using 3D movement data for 344 individuals who traversed nearly 1.5 million km of pelagic ocean in [Formula: see text]42,000 d, we found that nearly every tagged predator frequented the twilight zone and many made regular trips to the midnight zone. Using a predictive model, we found clear alignment of predator depth use with the expected location of deep pelagic prey for at least half of the predator species. We compared high-resolution predator data with shipboard acoustics and selected representative matches that highlight the opportunities and challenges in the analysis and synthesis of these data. While not all observed behavior was consistent with estimated prey availability at depth, our results suggest that deep pelagic biomass likely has high ecological value for a suite of commercially important predators in the open ocean. Careful consideration of the disruption to ecosystem services provided by pelagic food webs is needed before the potential costs and benefits of proceeding with extractive activities in the deep ocean can be evaluated.

Building use-inspired species distribution models: Using multiple data types to examine and improve model performance.

Species distribution models (SDMs) are becoming an important tool for marine conservation and management. Yet while there is an increasing diversity and volume of marine biodiversity data for training SDMs, little practical guidance is available on how to leverage distinct data types to build robust models. We explored the effect of different data types on the fit, performance and predictive ability of SDMs by comparing models trained with four data types for a heavily exploited pelagic fish, the blue shark (Prionace glauca), in the Northwest Atlantic: two fishery dependent (conventional mark-recapture tags, fisheries observer records) and two fishery independent (satellite-linked electronic tags, pop-up archival tags). We found that all four data types can result in robust models, but differences among spatial predictions highlighted the need to consider ecological realism in model selection and interpretation regardless of data type. Differences among models were primarily attributed to biases in how each data type, and the associated representation of absences, sampled the environment and summarized the resulting species distributions. Outputs from model ensembles and a model trained on all pooled data both proved effective for combining inferences across data types and provided more ecologically realistic predictions than individual models. Our results provide valuable guidance for practitioners developing SDMs. With increasing access to diverse data sources, future work should further develop truly integrative modeling approaches that can explicitly leverage the strengths of individual data types while statistically accounting for limitations, such as sampling biases.

Mesoscale eddies release pelagic sharks from thermal constraints to foraging in the ocean twilight zone.

Mesoscale eddies are critical components of the ocean's "internal weather" system. Mixing and stirring by eddies exerts significant control on biogeochemical fluxes in the open ocean, and eddies may trap distinctive plankton communities that remain coherent for months and can be transported hundreds to thousands of kilometers. Debate regarding how and why predators use fronts and eddies, for example as a migratory cue, enhanced forage opportunities, or preferred thermal habitat, has been ongoing since the 1950s. The influence of eddies on the behavior of large pelagic fishes, however, remains largely unexplored. Here, we reconstruct movements of a pelagic predator, the blue shark (Prionace glauca), in the Gulf Stream region using electronic tags, earth-observing satellites, and data-assimilating ocean forecasting models. Based on >2,000 tracking days and nearly 500,000 high-resolution time series measurements collected by 15 instrumented individuals, we show that blue sharks seek out the interiors of anticyclonic eddies where they dive deep while foraging. Our observations counter the existing paradigm that anticyclonic eddies are unproductive ocean "deserts" and suggest anomalously warm temperatures in these features connect surface-oriented predators to the most abundant fish community on the planet in the mesopelagic. These results also shed light on the ecosystem services provided by mesopelagic prey. Careful consideration will be needed before biomass extraction from the ocean twilight zone to avoid interrupting a key link between planktonic production and top predators. Moreover, robust associations between targeted fish species and oceanographic features increase the prospects for effective dynamic ocean management.

Global COVID-19 lockdown highlights humans as both threats and custodians of the environment.

The global lockdown to mitigate COVID-19 pandemic health risks has altered human interactions with nature. Here, we report immediate impacts of changes in human activities on wildlife and environmental threats during the early lockdown months of 2020, based on 877 qualitative reports and 332 quantitative assessments from 89 different studies. Hundreds of reports of unusual species observations from around the world suggest that animals quickly responded to the reductions in human presence. However, negative effects of lockdown on conservation also emerged, as confinement resulted in some park officials being unable to perform conservation, restoration and enforcement tasks, resulting in local increases in illegal activities such as hunting. Overall, there is a complex mixture of positive and negative effects of the pandemic lockdown on nature, all of which have the potential to lead to cascading responses which in turn impact wildlife and nature conservation. While the net effect of the lockdown will need to be assessed over years as data becomes available and persistent effects emerge, immediate responses were detected across the world. Thus, initial qualitative and quantitative data arising from this serendipitous global quasi-experimental perturbation highlights the dual role that humans play in threatening and protecting species and ecosystems. Pathways to favorably tilt this delicate balance include reducing impacts and increasing conservation effectiveness.

Strong habitat and weak genetic effects shape the lifetime reproductive success in a wild clownfish population.

The relative contributions of environmental, maternal and additive genetic factors to the Lifetime reproductive success (LRS) determine whether species can adapt to rapid environmental change. Yet to date, studies quantifying LRS across multiple generations in marine species in the wild are non-existent. Here we used 10-year pedigrees resolved for a wild orange clownfish population from Kimbe Island (PNG) and a quantitative genetic linear mixed model approach to quantify the additive genetic, maternal and environmental contributions to variation in LRS for the self-recruiting portion of the population. We found that the habitat of the breeder, including the anemone species and geographic location, made the greatest contribution to LRS. There were low to negligible contributions of genetic and maternal factors equating with low heritability and evolvability. Our findings imply that our population will be susceptible to short-term, small-scale changes in habitat structure and may have limited capacity to adapt to these changes.

First genealogy for a wild marine fish population reveals multigenerational philopatry.

Natal philopatry, the return of individuals to their natal area for reproduction, has advantages and disadvantages for animal populations. Natal philopatry may generate local genetic adaptation, but it may also increase the probability of inbreeding that can compromise persistence. Although natal philopatry is well documented in anadromous fishes, marine fish may also return to their birth site to spawn. How philopatry shapes wild fish populations is, however, unclear because it requires constructing multigenerational pedigrees that are currently lacking for marine fishes. Here we present the first multigenerational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (Amphiprion percula) at Kimbe Island (Papua New Guinea) during a 10-y period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. Progeny tended to settle close to their parents, with related individuals often sharing the same colony. However, successful inbreeding was rare, and genetic diversity remained high, suggesting occasional inbreeding does not impair local population persistence. Local reproductive success was dependent on the habitat larvae settled into, rather than the habitat they came from. Our study suggests that longitudinal philopatry can influence both population replenishment and local adaptation of marine fishes. Resolving multigenerational pedigrees during a relatively short period, as we present here, provides a framework for assessing the ability of marine populations to persist and adapt to accelerating climate change.

Stable isotope analyses of feather amino acids identify penguin migration strategies at ocean basin scales.

Identifying the at-sea distribution of wide-ranging marine predators is critical to understanding their ecology. Advances in electronic tracking devices and intrinsic biogeochemical markers have greatly improved our ability to track animal movements on ocean-wide scales. Here, we show that, in combination with direct tracking, stable carbon isotope analysis of essential amino acids in tail feathers provides the ability to track the movement patterns of two, wide-ranging penguin species over ocean basin scales. In addition, we use this isotopic approach across multiple breeding colonies in the Scotia Arc to evaluate migration trends at a regional scale that would be logistically challenging using direct tracking alone.

Seascape and life-history traits do not predict self-recruitment in a coral reef fish.

The persistence and resilience of many coral reef species are dependent on rates of connectivity among sub-populations. However, despite increasing research efforts, the spatial scale of larval dispersal remains unpredictable for most marine metapopulations. Here, we assess patterns of larval dispersal in the angelfish Centropyge bicolor in Kimbe Bay, Papua New Guinea, using parentage and sibling reconstruction analyses based on 23 microsatellite DNA loci. We found that, contrary to previous findings in this system, self-recruitment (SR) was virtually absent at both the reef (0.4-0.5% at 0.15 km(2)) and the lagoon scale (0.6-0.8% at approx. 700 km(2)). While approximately 25% of the collected juveniles were identified as potential siblings, the majority of sibling pairs were sampled from separate reefs. Integrating our findings with earlier research from the same system suggests that geographical setting and life-history traits alone are not suitable predictors of SR and that high levels of localized recruitment are not universal in coral reef fishes.

Tracing carbon flow through coral reef food webs using a compound-specific stable isotope approach.

Coral reefs support spectacularly productive and diverse communities in tropical and sub-tropical waters throughout the world's oceans. Debate continues, however, on the degree to which reef biomass is supported by new water column production, benthic primary production, and recycled detrital carbon (C). We coupled compound-specific stable C isotope ratio (δ(13)C) analyses with Bayesian mixing models to quantify C flow from primary producers to coral reef fishes across multiple feeding guilds and trophic positions in the Red Sea. Analyses of reef fishes with putative diets composed primarily of zooplankton (Amblyglyphidodon indicus), benthic macroalgae (Stegastes nigricans), reef-associated detritus (Ctenochaetus striatus), and coral tissue (Chaetodon trifascialis) confirmed that δ(13)C values of essential amino acids from all baseline C sources were both isotopically diagnostic and accurately recorded in consumer tissues. While all four source end-members contributed to the production of coral reef fishes in our study, a single-source end-member often dominated dietary C assimilation of a given species, even for highly mobile, generalist top predators. Microbially reworked detritus was an important secondary C source for most species. Seascape configuration played an important role in structuring resource utilization patterns. For instance, Lutjanus ehrenbergii showed a significant shift from a benthic macroalgal food web on shelf reefs (71 ± 13 % of dietary C) to a phytoplankton-based food web (72 ± 11 %) on oceanic reefs. Our work provides insights into the roles that diverse C sources play in the structure and function of coral reef ecosystems and illustrates a powerful fingerprinting method to develop and test nutritional frameworks for understanding resource utilization.

Coral reef fish populations can persist without immigration.

Determining the conditions under which populations may persist requires accurate estimates of demographic parameters, including immigration, local reproductive success, and mortality rates. In marine populations, empirical estimates of these parameters are rare, due at least in part to the pelagic dispersal stage common to most marine organisms. Here, we evaluate population persistence and turnover for a population of orange clownfish, Amphiprion percula, at Kimbe Island in Papua New Guinea. All fish in the population were sampled and genotyped on five occasions at 2-year intervals spanning eight years. The genetic data enabled estimates of reproductive success retained in the same population (reproductive success to self-recruitment), reproductive success exported to other subpopulations (reproductive success to local connectivity), and immigration and mortality rates of sub-adults and adults. Approximately 50% of the recruits were assigned to parents from the Kimbe Island population and this was stable through the sampling period. Stability in the proportion of local and immigrant settlers is likely due to: low annual mortality rates and stable egg production rates, and the short larval stages and sensory capacities of reef fish larvae. Biannual mortality rates ranged from 0.09 to 0.55 and varied significantly spatially. We used these data to parametrize a model that estimated the probability of the Kimbe Island population persisting in the absence of immigration. The Kimbe Island population was found to persist without significant immigration. Model results suggest the island population persists because the largest of the subpopulations are maintained due to having low mortality and high self-recruitment rates. Our results enable managers to appropriately target and scale actions to maximize persistence likelihood as disturbance frequencies increase.

Linking habitat mosaics and connectivity in a coral reef seascape.

Tropical marine ecosystems are under mounting anthropogenic pressure from overfishing and habitat destruction, leading to declines in their structure and function on a global scale. Although maintaining connectivity among habitats within a seascape is necessary for preserving population resistance and resilience, quantifying movements of individuals within seascapes remains challenging. Traditional methods of identifying and valuing potential coral reef fish nursery habitats are indirect, often relying on visual surveys of abundance and correlations of size and biomass among habitats. We used compound-specific stable isotope analyses to determine movement patterns of commercially important fish populations within a coral reef seascape. This approach allowed us to quantify the relative contributions of individuals from inshore nurseries to reef populations and identify migration corridors among important habitats. Our results provided direct measurements of remarkable migrations by juvenile snapper of over 30 km, between nurseries and reefs. We also found significant plasticity in juvenile nursery residency. Although a majority of individuals on coastal reefs had used seagrass nurseries as juveniles, many adults on oceanic reefs had settled directly into reef habitats. Moreover, seascape configuration played a critical but heretofore unrecognized role in determining connectivity among habitats. Finally, our approach provides key quantitative data necessary to estimate the value of distinctive habitats to ecosystem services provided by seascapes.

Experimental evaluation of imprinting and the role innate preference plays in habitat selection in a coral reef fish.

When facing decisions about where to live, juveniles have a strong tendency to choose habitats similar to where their parents successfully bred. Developing larval fishes can imprint on the chemical cues from their natal habitat. However, to demonstrate that imprinting is ecologically important, it must be shown that settlers respond and distinguish among different imprinted cues, and use imprinting for decisions in natural environments. In addition, the potential role innate preferences play compared to imprinted choices also needs to be examined. As environmental variability increases due to anthropogenic causes these two recognition mechanisms, innate and imprinting, could provide conflicting information. Here we used laboratory rearing and chemical choice experiments to test imprinting in larval anemonefish (Amphiprion percula). Individuals exposed to a variety of benthic habitat or novel olfactory cues as larvae either developed a preference for (spent >50% of their time in the cue) or increased their attraction to (increased preference but did not spend >50% of their time in the cue) the cue when re-exposed as settlers. Results indicate not only the capacity for imprinting but also the ability to adjust innate preferences after early exposure to a chemical cue. To test ecological relevance in the natural system, recruits were collected from anemones and related to their parents, using genetic parentage analysis, providing information on the natal anemone species and the species chosen at settlement. Results demonstrated that recruits did not preferentially return to their natal species, conflicting with laboratory results indicating the importance imprinting might have in habitat recognition.

Like a rolling stone: Colonization and migration dynamics of the gray reef shark (Carcharhinus amblyrhynchos).

Designing appropriate management plans requires knowledge of both the dispersal ability and what has shaped the current distribution of the species under consideration. Here, we investigated the evolutionary history of the endangered gray reef shark (Carcharhinus amblyrhynchos) across its range by sequencing thousands of RADseq loci in 173 individuals in the Indo-Pacific (IP). We first bring evidence of the occurrence of a range expansion (RE) originating close to the Indo-Australian Archipelago (IAA) where two stepping-stone waves (east and westward) colonized almost the entire IP. Coalescent modeling additionally highlighted a homogenous connectivity (Nm ~ 10 per generation) throughout the range, and isolation by distance model suggested the absence of barriers to dispersal despite the affinity of C. amblyrhynchos to coral reefs. This coincides with long-distance swims previously recorded, suggesting that the strong genetic structure at the IP scale (F ST ~ 0.56 between its ends) is the consequence of its broad current distribution and organization in a large number of demes. Our results strongly suggest that management plans for the gray reef shark should be designed on a range-wide rather than a local scale due to its continuous genetic structure. We further contrasted these results with those obtained previously for the sympatric but strictly lagoon-associated Carcharhinus melanopterus, known for its restricted dispersal ability. Carcharhinus melanopterus exhibits a similar RE dynamic but is characterized by a stronger genetic structure and a nonhomogeneous connectivity largely dependent on local coral reefs availability. This sheds new light on shark evolution, emphasizing the roles of IAA as source of biodiversity and of life-history traits in shaping the extent of genetic structure and diversity.

Probability of successful larval dispersal declines fivefold over 1 km in a coral reef fish.

A central question of marine ecology is, how far do larvae disperse? Coupled biophysical models predict that the probability of successful dispersal declines as a function of distance between populations. Estimates of genetic isolation-by-distance and self-recruitment provide indirect support for this prediction. Here, we conduct the first direct test of this prediction, using data from the well-studied system of clown anemonefish (Amphiprion percula) at Kimbe Island, in Papua New Guinea. Amphiprion percula live in small breeding groups that inhabit sea anemones. These groups can be thought of as populations within a metapopulation. We use the x- and y-coordinates of each anemone to determine the expected distribution of dispersal distances (the distribution of distances between each and every population in the metapopulation). We use parentage analyses to trace recruits back to parents and determine the observed distribution of dispersal distances. Then, we employ a logistic model to (i) compare the observed and expected dispersal distance distributions and (ii) determine the relationship between the probability of successful dispersal and the distance between populations. The observed and expected dispersal distance distributions are significantly different (p < 0.0001). Remarkably, the probability of successful dispersal between populations decreases fivefold over 1 km. This study provides a framework for quantitative investigations of larval dispersal that can be applied to other species. Further, the approach facilitates testing biological and physical hypotheses for the factors influencing larval dispersal in unison, which will advance our understanding of marine population connectivity.

Patterns and persistence of larval retention and connectivity in a marine fish metapopulation.

Connectivity, the demographic linking of local populations through the dispersal of individuals, is one of the most poorly understood processes in population dynamics, yet has profound implications for conservation and harvest strategies. For marine species with pelagic larvae, direct estimation of connectivity remains logistically challenging and has mostly been limited to single snapshots in time. Here, we document seasonal and interannual patterns of larval dispersal in a metapopulation of the coral reef fish Amphiprion polymnus. A 3-year record of larval trajectories within and among nine discrete local populations from an area of approximately 35 km was established by determining the natal origin of settled juveniles through DNA parentage analysis. We found that spatial patterns of both self-recruitment and connectivity were remarkably consistent over time, with a low level of self-recruitment at the scale of individual sites. Connectivity among sites was common and multidirectional in all years and was not significantly influenced by seasonal variability of predominant surface current directions. However, approximately 75% of the sampled juveniles could not be assigned to parents within the study area, indicating high levels of immigrations from sources outside the study area. The data support predictions that the magnitude and temporal stability of larval connectivity decreases significantly with increasing distance between subpopulations, but increases with the size of subpopulations. Given the considerable effort needed to directly measure larval exchange, the consistent patterns suggest snapshot parentage analyses can provide useful dispersal estimates to inform spatial management decisions.

Larval dispersal connects fish populations in a network of marine protected areas.

Networks of no-take marine protected areas (MPAs) have been widely advocated for the conservation of marine biodiversity. But for MPA networks to be successful in protecting marine populations, individual MPAs must be self-sustaining or adequately connected to other MPAs via dispersal. For marine species with a dispersive larval stage, populations within MPAs require either the return of settlement-stage larvae to their natal reserve or connectivity among reserves at the spatial scales at which MPA networks are implemented. To date, larvae have not been tracked when dispersing from one MPA to another, and the relative magnitude of local retention and connectivity among MPAs remains unknown. Here we use DNA parentage analysis to provide the first direct estimates of connectivity of a marine fish, the orange clownfish (Amphiprion percula), in a proposed network of marine reserves in Kimbe Bay, Papua New Guinea. Approximately 40% of A. percula larvae settling into anemones in an island MPA at 2 different times were derived from parents resident in the reserve. We also located juveniles spawned by Kimbe Island residents that had dispersed as far as 35 km to other proposed MPAs, the longest distance that marine larvae have been directly tracked. These dispersers accounted for up to 10% of the recruitment in the adjacent MPAs. Our findings suggest that MPA networks can function to sustain resident populations both by local replenishment and through larval dispersal from other reserves. More generally, DNA parentage analysis provides a direct method for measuring larval dispersal for other marine organisms.

The Functional and Ecological Significance of Deep Diving by Large Marine Predators.

Many large marine predators make excursions from surface waters to the deep ocean below 200 m. Moreover, the ability to access meso- and bathypelagic habitats has evolved independently across marine mammals, reptiles, birds, teleost fishes, and elasmobranchs. Theoretical and empirical evidence suggests a number of plausible functional hypotheses for deep-diving behavior. Developing ways to test among these hypotheses will, however, require new ways to quantify animal behavior and biophysical oceanographic processes at coherent spatiotemporal scales. Current knowledge gaps include quantifying ecological links between surface waters and mesopelagic habitats and the value of ecosystem services provided by biomass in the ocean twilight zone. Growing pressure for ocean twilight zone fisheries creates an urgent need to understand the importance of the deep pelagic ocean to large marine predators.

Pieces in a global puzzle: Population genetics at two whale shark aggregations in the western Indian Ocean.

The whale shark Rhincodon typus is found throughout the world's tropical and warm-temperate ocean basins. Despite their broad physical distribution, research on the species has been concentrated at a few aggregation sites. Comparing DNA sequences from sharks at different sites can provide a demographically neutral understanding of the whale shark's global ecology. Here, we created genetic profiles for 84 whale sharks from the Saudi Arabian Red Sea and 72 individuals from the coast of Tanzania using a combination of microsatellite and mitochondrial sequences. These two sites, separated by approximately 4500 km (shortest over-water distance), exhibit markedly different population demographics and behavioral ecologies. Eleven microsatellite DNA markers revealed that the two aggregation sites have similar levels of allelic richness and appear to be derived from the same source population. We sequenced the mitochondrial control region to produce multiple global haplotype networks (based on different alignment methodologies) that were broadly similar to each other in terms of population structure but suggested different demographic histories. Data from both microsatellite and mitochondrial markers demonstrated the stability of genetic diversity within the Saudi Arabian aggregation site throughout the sampling period. These results contrast previously measured declines in diversity at Ningaloo Reef, Western Australia. Mapping the geographic distribution of whale shark lineages provides insight into the species' connectivity and can be used to direct management efforts at both local and global scales. Similarly, understanding historical fluctuations in whale shark abundance provides a baseline by which to assess current trends. Continued development of new sequencing methods and the incorporation of genomic data could lead to considerable advances in the scientific understanding of whale shark population ecology and corresponding improvements to conservation policy.

Connectivity dominates larval replenishment in a coastal reef fish metapopulation.

Direct estimates of larval retention and connectivity are essential to understand the structure and dynamics of marine metapopulations, and optimize the size and spacing of reserves within networks of marine-protected areas (MPAs). For coral reef fishes, while there are some empirical estimates of self-recruitment at isolated populations, exchange among sub-populations has been rarely quantified. Here, we used microsatellite DNA markers and a likelihood-based parentage analysis to assess the relative magnitude of self-recruitment and exchange among eight geographically distinct sub-populations of the panda clownfish Amphiprion polymnus along 30 km of coastline near Port Moresby, Papua New Guinea. In addition, we used an assignment/exclusion test to identify immigrants arriving from genetically distinct sources. Overall, 82 per cent of the juveniles were immigrants while 18 per cent were progeny of parents genotyped in our focal metapopulation. Of the immigrants, only 6 per cent were likely to be genetically distinct from the focal metapopulation, suggesting most of the connectivity is among sub-populations from a rather homogeneous genetic pool. Of the 18 per cent that were progeny of known adults, two-thirds dispersed among the eight sub-populations and only one-third settled back into natal sub-populations. Comparison of our data with previous studies suggested that variation in dispersal distances is likely to be influenced by the geographical setting and spacing of sub-populations.