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.

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.

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.

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.

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.

Multi-method assessment of whale shark (Rhincodon typus) residency, distribution, and dispersal behavior at an aggregation site in the Red Sea.

Whale sharks (Rhincodon typus) are typically dispersed throughout their circumtropical range, but the species is also known to aggregate in specific coastal areas. Accurate site descriptions associated with these aggregations are essential for the conservation of R. typus, an Endangered species. Although aggregations have become valuable hubs for research, most site descriptions rely heavily on sightings data. In the present study, visual census, passive acoustic monitoring, and long range satellite telemetry were combined to track the movements of R. typus from Shib Habil, a reef-associated aggregation site in the Red Sea. An array of 63 receiver stations was used to record the presence of 84 acoustically tagged sharks (35 females, 37 males, 12 undetermined) from April 2010 to May 2016. Over the same period, identification photos were taken for 76 of these tagged individuals and 38 were fitted with satellite transmitters. In total of 37,461 acoustic detections, 210 visual encounters, and 33 satellite tracks were analyzed to describe the sharks' movement ecology. The results demonstrate that the aggregation is seasonal, mostly concentrated on the exposed side of Shib Habil, and seems to attract sharks of both sexes in roughly equal numbers. The combined methodologies also tracked 15 interannual homing-migrations, demonstrating that many sharks leave the area before returning in later years. When compared to acoustic studies from other aggregations, these results demonstrate that R. typus exhibits diverse, site-specific ecologies across its range. Sightings-independent data from acoustic telemetry and other sources are an effective means of validating more common visual surveys.

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.

Evidence and patterns of tuna spawning inside a large no-take Marine Protected Area.

The Phoenix Islands Protected Area (PIPA), one of the world's largest marine protected areas, represents 11% of the exclusive economic zone of the Republic of Kiribati, which earns much of its GDP by selling tuna fishing licenses to foreign nations. We have determined that PIPA is a spawning area for skipjack (Katsuwonus pelamis), bigeye (Thunnus obesus), and yellowfin (Thunnus albacares) tunas. Our approach included sampling larvae on cruises in 2015-2017 and using a biological-physical model to estimate spawning locations for collected larvae. Temperature and chlorophyll conditions varied markedly due to observed ENSO states: El Niño (2015) and neutral (2016-2017). However, larval tuna distributions were similar amongst years. Generally, skipjack larvae were patchy and more abundant near PIPA's northeast corner, while Thunnus larvae exhibited lower and more even abundances. Genetic barcoding confirmed the presence of bigeye (Thunnus obesus) and yellowfin (Thunnus albacares) tuna larvae. Model simulations indicated that most of the larvae collected inside PIPA in 2015 were spawned inside, while stronger currents in 2016 moved more larvae across PIPA's boundaries. Larval distributions and relative spawning output simulations indicated that both focal taxa spawned inside PIPA in all 3 study years, demonstrating that PIPA is protecting viable tuna spawning habitat.

Mesoscale eddies influence the movements of mature female white sharks in the Gulf Stream and Sargasso Sea.

Satellite-tracking of mature white sharks (Carcharodon carcharias) has revealed open-ocean movements spanning months and covering tens of thousands of kilometers. But how are the energetic demands of these active apex predators met as they leave coastal areas with relatively high prey abundance to swim across the open ocean through waters often characterized as biological deserts? Here we investigate mesoscale oceanographic variability encountered by two white sharks as they moved through the Gulf Stream region and Sargasso Sea in the North Atlantic Ocean. In the vicinity of the Gulf Stream, the two mature female white sharks exhibited extensive use of the interiors of clockwise-rotating anticyclonic eddies, characterized by positive (warm) temperature anomalies. One tagged white shark was also equipped with an archival tag that indicated this individual made frequent dives to nearly 1,000 m in anticyclones, where it was presumably foraging on mesopelagic prey. We propose that warm temperature anomalies in anticyclones make prey more accessible and energetically profitable to adult white sharks in the Gulf Stream region by reducing the physiological costs of thermoregulation in cold water. The results presented here provide valuable new insight into open ocean habitat use by mature, female white sharks that may be applicable to other large pelagic predators.

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.

Larval fish dispersal in a coral-reef seascape.

Larval dispersal is a critical yet enigmatic process in the persistence and productivity of marine metapopulations. Empirical data on larval dispersal remain scarce, hindering the use of spatial management tools in efforts to sustain ocean biodiversity and fisheries. Here we document dispersal among subpopulations of clownfish (Amphiprion percula) and butterflyfish (Chaetodon vagabundus) from eight sites across a large seascape (10,000 km2) in Papua New Guinea across 2 years. Dispersal of clownfish was consistent between years, with mean observed dispersal distances of 15 km and 10 km in 2009 and 2011, respectively. A Laplacian statistical distribution (the dispersal kernel) predicted a mean dispersal distance of 13-19 km, with 90% of settlement occurring within 31-43 km. Mean dispersal distances were considerably greater (43-64 km) for butterflyfish, with kernels declining only gradually from spawning locations. We demonstrate that dispersal can be measured on spatial scales sufficient to inform the design of and test the performance of marine reserve networks.

Marine Dispersal Scales Are Congruent over Evolutionary and Ecological Time.

The degree to which offspring remain near their parents or disperse widely is critical for understanding population dynamics, evolution, and biogeography, and for designing conservation actions. In the ocean, most estimates suggesting short-distance dispersal are based on direct ecological observations of dispersing individuals, while indirect evolutionary estimates often suggest substantially greater homogeneity among populations. Reconciling these two approaches and their seemingly competing perspectives on dispersal has been a major challenge. Here we show for the first time that evolutionary and ecological measures of larval dispersal can closely agree by using both to estimate the distribution of dispersal distances. In orange clownfish (Amphiprion percula) populations in Kimbe Bay, Papua New Guinea, we found that evolutionary dispersal kernels were 17 km (95% confidence interval: 12-24 km) wide, while an exhaustive set of direct larval dispersal observations suggested kernel widths of 27 km (19-36 km) or 19 km (15-27 km) across two years. The similarity between these two approaches suggests that ecological and evolutionary dispersal kernels can be equivalent, and that the apparent disagreement between direct and indirect measurements can be overcome. Our results suggest that carefully applied evolutionary methods, which are often less expensive, can be broadly relevant for understanding ecological dispersal across the tree of life.

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.

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.

Carbon and nitrogen isotope fractionation of amino acids in an avian marine predator, the gentoo penguin (Pygoscelis papua).

Compound-specific stable isotope analysis (CSIA) of amino acids (AA) has rapidly become a powerful tool in studies of food web architecture, resource use, and biogeochemical cycling. However, applications to avian ecology have been limited because no controlled studies have examined the patterns in AA isotope fractionation in birds. We conducted a controlled CSIA feeding experiment on an avian species, the gentoo penguin (Pygoscelis papua), to examine patterns in individual AA carbon and nitrogen stable isotope fractionation between diet (D) and consumer (C) (Δ(13)CC-D and Δ(15)NC-D, respectively). We found that essential AA δ (13)C values and source AA δ (15)N values in feathers showed minimal trophic fractionation between diet and consumer, providing independent but complimentary archival proxies for primary producers and nitrogen sources respectively, at the base of food webs supporting penguins. Variations in nonessential AA Δ(13)CC-D values reflected differences in macromolecule sources used for biosynthesis (e.g., protein vs. lipids) and provided a metric to assess resource utilization. The avian-specific nitrogen trophic discrimination factor (TDFGlu-Phe = 3.5 ± 0.4‰) that we calculated from the difference in trophic fractionation (Δ(15)NC -D) of glutamic acid and phenylalanine was significantly lower than the conventional literature value of 7.6‰. Trophic positions of five species of wild penguins calculated using a multi-TDFG lu-Phe equation with the avian-specific TDFG lu-Phe value from our experiment provided estimates that were more ecologically realistic than estimates using a single TDFG lu-Phe of 7.6‰ from the previous literature. Our results provide a quantitative, mechanistic framework for the use of CSIA in nonlethal, archival feathers to study the movement and foraging ecology of avian consumers.