A large-scale experiment finds no consistent evidence of change in mortality or commercial productivity in silverlip pearl oysters (Pinctada maxima) exposed to a seismic source survey.

High-intensity, impulsive sounds are used to locate oil and gas reserves during seismic exploration of the seafloor. The impacts of this noise pollution on the health and mortality of marine invertebrates are not well known, including the silverlip pearl oyster (Pinctada maxima), which comprises one of the world's last remaining significant wildstock pearl oyster fisheries, in northwestern Australia. We exposed ≈11,000 P. maxima to a four-day experimental seismic survey, plus one vessel-control day. After exposure, survival rates were monitored throughout a full two-year production cycle, and the number and quality of pearls produced at harvest were assessed. Oysters from two groups, on one sampling day, exhibited reduced survival and pearl productivity compared to controls, but 14 other groups receiving similar or higher exposure levels did not. We therefore found no conclusive evidence of an impact of the seismic source survey on oyster mortality or pearl production.

Wearable sensors for monitoring marine environments and their inhabitants.

Human societies depend on marine ecosystems, but their degradation continues. Toward mitigating this decline, new and more effective ways to precisely measure the status and condition of marine environments are needed alongside existing rebuilding strategies. Here, we provide an overview of how sensors and wearable technology developed for humans could be adapted to improve marine monitoring. We describe barriers that have slowed the transition of this technology from land to sea, update on the developments in sensors to advance ocean observation and advocate for more widespread use of wearables on marine organisms in the wild and in aquaculture. We propose that large-scale use of wearables could facilitate the concept of an 'internet of marine life' that might contribute to a more robust and effective observation system for the oceans and commercial aquaculture operations. These observations may aid in rationalizing strategies toward conservation and restoration of marine communities and habitats.

Diving into the vertical dimension of elasmobranch movement ecology.

Knowledge of the three-dimensional movement patterns of elasmobranchs is vital to understand their ecological roles and exposure to anthropogenic pressures. To date, comparative studies among species at global scales have mostly focused on horizontal movements. Our study addresses the knowledge gap of vertical movements by compiling the first global synthesis of vertical habitat use by elasmobranchs from data obtained by deployment of 989 biotelemetry tags on 38 elasmobranch species. Elasmobranchs displayed high intra- and interspecific variability in vertical movement patterns. Substantial vertical overlap was observed for many epipelagic elasmobranchs, indicating an increased likelihood to display spatial overlap, biologically interact, and share similar risk to anthropogenic threats that vary on a vertical gradient. We highlight the critical next steps toward incorporating vertical movement into global management and monitoring strategies for elasmobranchs, emphasizing the need to address geographic and taxonomic biases in deployments and to concurrently consider both horizontal and vertical movements.

The power of national acoustic tracking networks to assess the impacts of human activity on marine organisms during the COVID-19 pandemic.

COVID-19 restrictions have led to an unprecedented global hiatus in anthropogenic activities, providing a unique opportunity to assess human impact on biological systems. Here, we describe how a national network of acoustic tracking receivers can be leveraged to assess the effects of human activity on animal movement and space use during such global disruptions. We outline variation in restrictions on human activity across Australian states and describe four mechanisms affecting human interactions with the marine environment: 1) reduction in economy and trade changing shipping traffic; 2) changes in export markets affecting commercial fisheries; 3) alterations in recreational activities; and 4) decline in tourism. We develop a roadmap for the analysis of acoustic tracking data across various scales using Australia's national Integrated Marine Observing System (IMOS) Animal Tracking Facility as a case study. We illustrate the benefit of sustained observing systems and monitoring programs by assessing how a 51-day break in white shark (Carcharodon carcharias) cage-diving tourism due to COVID-19 restrictions affected the behaviour and space use of two resident species. This cessation of tourism activities represents the longest break since cage-diving vessels started day trips in this area in 2007. Long-term monitoring of the local environment reveals that the activity space of yellowtail kingfish (Seriola lalandi) was reduced when cage-diving boats were absent compared to periods following standard tourism operations. However, white shark residency and movements were not affected. Our roadmap is globally applicable and will assist researchers in designing studies to assess how anthropogenic activities can impact animal movement and distributions during regional, short-term through to major, unexpected disruptions like the COVID-19 pandemic.

A large-scale experiment finds no evidence that a seismic survey impacts a demersal fish fauna.

Seismic surveys are used to locate oil and gas reserves below the seabed and can be a major source of noise in marine environments. Their effects on commercial fisheries are a subject of debate, with experimental studies often producing results that are difficult to interpret. We overcame these issues in a large-scale experiment that quantified the impacts of exposure to a commercial seismic source on an assemblage of tropical demersal fishes targeted by commercial fisheries on the North West Shelf of Western Australia. We show that there were no short-term (days) or long-term (months) effects of exposure on the composition, abundance, size structure, behavior, or movement of this fauna. These multiple lines of evidence suggest that seismic surveys have little impact on demersal fishes in this environment.

Natural nutrient subsidies alter demographic rates in a functionally important coral-reef fish.

By improving resource quality, cross-ecosystem nutrient subsidies may boost demographic rates of consumers in recipient ecosystems, which in turn can affect population and community dynamics. However, empirical studies on how nutrient subsidies simultaneously affect multiple demographic rates are lacking, in part because humans have disrupted the majority of these natural flows. Here, we compare the demographics of a sex-changing parrotfish (Chlorurus sordidus) between reefs where cross-ecosystem nutrients provided by seabirds are available versus nearby reefs where invasive, predatory rats have removed seabird populations. For this functionally important species, we found evidence for a trade-off between investing in growth and fecundity, with parrotfish around rat-free islands with many seabirds exhibiting 35% faster growth, but 21% lower size-based fecundity, than those around rat-infested islands with few seabirds. Although there were no concurrent differences in population-level density or biomass, overall mean body size was 16% larger around rat-free islands. Because the functional significance of parrotfish as grazers and bioeroders increases non-linearly with size, the increased growth rates and body sizes around rat-free islands likely contributes to higher ecosystem function on coral reefs that receive natural nutrient subsidies. More broadly, these results demonstrate additional benefits, and potential trade-offs, of restoring natural nutrient pathways for recipient ecosystems.

Moray eels are more common on coral reefs subject to higher human pressure in the greater Caribbean.

Proximity and size of the nearest market ('market gravity') have been shown to have strong negative effects on coral reef fish communities that can be mitigated by the establishment of closed areas. However, moray eels are functionally unique predators that are generally not subject to targeted fishing and should therefore not directly be affected by these factors. We used baited remote underwater video systems to investigate associations between morays and anthropogenic, habitat, and ecological factors in the Caribbean region. Market gravity had a positive effect on morays, while the opposite pattern was observed in a predator group subject to exploitation (sharks). Environmental DNA analyses corroborated the positive effect of market gravity on morays. We hypothesize that the observed pattern could be the indirect result of the depletion of moray competitors and predators near humans.

Depth-dependent dive kinematics suggest cost-efficient foraging strategies by tiger sharks.

Tiger sharks, Galeocerdo cuvier, are a keystone, top-order predator that are assumed to engage in cost-efficient movement and foraging patterns. To investigate the extent to which oscillatory diving by tiger sharks conform to these patterns, we used a biologging approach to model their cost of transport. High-resolution biologging tags with tri-axial sensors were deployed on 21 tiger sharks at Ningaloo Reef for durations of 5-48 h. Using overall dynamic body acceleration as a proxy for energy expenditure, we modelled the cost of transport of oscillatory movements of varying geometries in both horizontal and vertical planes for tiger sharks. The cost of horizontal transport was minimized by descending at the smallest possible angle and ascending at an angle of 5-14°, meaning that vertical oscillations conserved energy compared to swimming at a level depth. The reduction of vertical travel costs occurred at steeper angles. The absolute dive angles of tiger sharks increased between inshore and offshore zones, presumably to reduce the cost of transport while continuously hunting for prey in both benthic and surface habitats. Oscillatory movements of tiger sharks conform to strategies of cost-efficient foraging, and shallow inshore habitats appear to be an important habitat for both hunting prey and conserving energy while travelling.

Synchronous biological feedbacks in parrotfishes associated with pantropical coral bleaching.

Biological feedbacks generated through patterns of disturbance are vital for sustaining ecosystem states. Recent ocean warming and thermal anomalies have caused pantropical episodes of coral bleaching, which has led to widespread coral mortality and a range of subsequent effects on coral reef communities. Although the response of many reef-associated fishes to major disturbance events on coral reefs is negative (e.g., reduced abundance and condition), parrotfishes show strong feedbacks after disturbance to living reef structure manifesting as increases in abundance. However, the mechanisms underlying this response are poorly understood. Using biochronological reconstructions of annual otolith (ear stone) growth from two ocean basins, we tested whether parrotfish growth was enhanced following bleaching-related coral mortality, thus providing an organismal mechanism for demographic changes in populations. Both major feeding guilds of parrotfishes (scrapers and excavators) exhibited enhanced growth of individuals after bleaching that was decoupled from expected thermal performance, a pattern that was not evident in other reef fish taxa from the same environment. These results provide evidence for a more nuanced ecological feedback system-one where disturbance plays a key role in mediating parrotfish-benthos interactions. By influencing the biology of assemblages, disturbance can thereby stimulate change in parrotfish grazing intensity and ultimately reef geomorphology over time. This feedback cycle operated historically at within-reef scales; however, our results demonstrate that the scale, magnitude, and severity of recent thermal events are entraining the biological responses of disparate communities to respond in synchrony. This may fundamentally alter feedbacks in the relationships between parrotfishes and reef systems.

Acoustic enrichment can enhance fish community development on degraded coral reef habitat.

Coral reefs worldwide are increasingly damaged by anthropogenic stressors, necessitating novel approaches for their management. Maintaining healthy fish communities counteracts reef degradation, but degraded reefs smell and sound less attractive to settlement-stage fishes than their healthy states. Here, using a six-week field experiment, we demonstrate that playback of healthy reef sound can increase fish settlement and retention to degraded habitat. We compare fish community development on acoustically enriched coral-rubble patch reefs with acoustically unmanipulated controls. Acoustic enrichment enhances fish community development across all major trophic guilds, with a doubling in overall abundance and 50% greater species richness. If combined with active habitat restoration and effective conservation measures, rebuilding fish communities in this manner might accelerate ecosystem recovery at multiple spatial and temporal scales. Acoustic enrichment shows promise as a novel tool for the active management of degraded coral reefs.

Can Fish and Cell Phones Teach Us about Our Health?

Biologging is a scientific endeavor that studies the environment and animals within it by outfitting the latter with sensors of their dynamics as they roam freely in their natural habitats. As wearable technologies advance for the monitoring of human health, it may be instructive to reflect on the successes and failures of biologging in field biology over the past few decades. Several lessons may be of value. Physiological sensors can "encode" for a wider number of states than the one explicitly targeted, although the limits of this are debatable. The combination of orthogonal sensors turns out to be critical to delivering a high value data set. Sensor fusion and engineering for longevity are also important for success. This Perspective highlights successful strategies for biologging that hold promise for human health monitoring.

Stable isotope analyses reveal unique trophic role of reef manta rays (Mobula alfredi) at a remote coral reef.

Stable isotope analyses provide the means to examine the trophic role of animals in complex food webs. Here, we used stable isotope analyses to characterize the feeding ecology of reef manta rays (Mobula alfredi) at a remote coral reef in the Western Indian Ocean. Muscle samples of M. alfredi were collected from D'Arros Island and St. Joseph Atoll, Republic of Seychelles, in November 2016 and 2017. Prior to analysis, lipid and urea extraction procedures were tested on freeze-dried muscle tissue in order to standardize sample treatment protocols for M. alfredi. The lipid extraction procedure was effective at removing both lipids and urea from samples and should be used in future studies of the trophic ecology of this species. The isotopic signatures of nitrogen (δ15N) and carbon (δ13C) for M. alfredi differed by year, but did not vary by sex or life stage, suggesting that all individuals occupy the same trophic niche at this coral reef. Furthermore, the isotopic signatures for M. alfredi differed to those for co-occurring planktivorous fish species also sampled at D'Arros Island and St. Joseph Atoll, suggesting that the ecological niche of M. alfredi is unique. Pelagic zooplankton were the main contributor (45%) to the diet of M. alfredi, combined with emergent zooplankton (38%) and mesopelagic prey items (17%). Given the extent of movement that would be required to undertake this foraging strategy, individual M. alfredi are implicated as important vectors of nutrient supply around and to the coral reefs surrounding D'Arros Island and St. Joseph Atoll, particularly where substantial site fidelity is displayed by these large elasmobranchs.

Protection from illegal fishing and shark recovery restructures mesopredatory fish communities on a coral reef.

The recovery of communities of predatory fishes within a no-take marine reserve after the eradication of illegal fishing provides an opportunity to examine the role of sharks and other large-bodied mesopredatory fishes in structuring reef fish communities. We used baited remote underwater video stations to investigate whether an increase in sharks was associated with a change in structure of the mesopredatory fish community at Ashmore Reef, Western Australia. We found an almost fourfold increase in shark abundance in reef habitat from 0.64 hr-1 ± 0.15 SE in 2004, when Ashmore Reef was being fished illegally, to 2.45 hr-1 ± 0.37 in 2016, after eight years of full-time enforcement of the reserve. Shark recovery in reef habitat was accompanied by a two and a half-fold decline in the abundance of small mesopredatory fishes (≤50 cm TL) (14.00 hr-1 ± 3.79 to 5.6 hr-1 ± 1.20) and a concomitant increase in large mesopredatory fishes (≥100 cm TL) from 1.82 hr-1 ± 0.48 to 4.27 hr-1 ± 0.93. In contrast, near-reef habitats showed an increase in abundance of large mesopredatory fishes between years (2.00 hr-1 ± 0.65 to 4.56 hr-1 ± 1.11), although only smaller increases in sharks (0.67 hr-1 ± 0.25 to 1.22 hr-1 ± 0.34) and smaller mesopredatory fishes. Although the abundance of most mesopredatory groups increased with recovery from fishing, we suggest that the large decline of small mesopredatory fish in reef habitat was mostly due to higher predation pressure following the increase in sharks and large mesopredatory fishes. At the regional scale, the structure of fished communities at Ashmore Reef in 2004 resembled those of present day Scott Reefs, where fishing still continues today. In 2016, Ashmore fish communities resembled those of the Rowley Shoals, which have been protected from fishing for decades.

Demographic plasticity facilitates ecological and economic resilience in a commercially important reef fish.

Variation in life-history characteristics is evident within and across animal populations. Such variation is mediated by environmental gradients and reflects metabolic constraints or trade-offs that enhance reproductive outputs. While generalizations of life-history relationships across species provide a framework for predicting vulnerability to overexploitation, deciphering patterns of intraspecific variation may also enable recognition of peculiar features of populations that facilitate ecological resilience. This study combines age-based biological data from geographically disparate populations of bluespine unicornfish (Naso unicornis)-the most commercially valuable reef-associated species in the insular Indo-Pacific-to explore the magnitude and drivers of variation in life span and examine the mechanisms enabling peculiar mortality schedules. Longevity and mortality schedules were investigated across eleven locations encompassing a range of latitudes and exploitation levels. The presence of different growth types was examined using back-calculated growth histories from otoliths. Growth-type-dependent mortality (mortality rates associated with particular growth trajectories) was corroborated using population models that incorporated size-dependent competition. We found a threefold geographic variation in life span that was strongly linked to temperature, but not to anthropogenic pressure or ocean productivity. All populations consistently displayed a two-phase mortality schedule, with higher than expected natural mortality rates in earlier stages of post-settlement life. Reconstructed growth histories and population models demonstrated that variable growth types within populations can yield this peculiar biphasic mortality schedule, where fast growers enjoy early reproductive outputs at the expense of greater mortality, and benefits for slow growers derive from extended reproductive outputs over a greater number of annual cycles. This promotes population resilience because individuals can take advantage of cycles of environmental change operating at both short- and long-term scales. Our results highlight a prevailing, fundamental misperception when comparing the life histories of long-lived tropical ectotherms: the seemingly incongruent combination of extended life spans with high mortality rates was enabled by coexistence of variable growth types in a population. Thus, a demographic profile incorporating contrasting growth and mortality strategies obscures the demographic effects of harvest across space or time in N. unicornis and possibly other ectotherms with the combination of longevity and asymptotic growth.

Implanted Nanosensors in Marine Organisms for Physiological Biologging: Design, Feasibility, and Species Variability.

In recent decades, biologists have sought to tag animals with various sensors to study aspects of their behavior otherwise inaccessible from controlled laboratory experiments. Despite this, chemical information, both environmental and physiological, remains challenging to collect despite its tremendous potential to elucidate a wide range of animal behaviors. In this work, we explore the design, feasibility, and data collection constraints of implantable, near-infrared fluorescent nanosensors based on DNA-wrapped single-wall carbon nanotubes (SWNT) embedded within a biocompatible poly(ethylene glycol) diacrylate (PEGDA) hydrogel. These sensors are enabled by Corona Phase Molecular Recognition (CoPhMoRe) to provide selective chemical detection for marine organism biologging. Riboflavin, a key nutrient in oxidative phosphorylation, is utilized as a model analyte in in vitro and ex vivo tissue measurements. Nine species of bony fish, sharks, eels, and turtles were utilized on site at Oceanogràfic in Valencia, Spain to investigate sensor design parameters, including implantation depth, sensor imaging and detection limits, fluence, and stability, as well as acute and long-term biocompatibility. Hydrogels were implanted subcutaneously and imaged using a customized, field-portable Raspberry Pi camera system. Hydrogels could be detected up to depths of 7 mm in the skin and muscle tissue of deceased teleost fish ( Sparus aurata and Stenotomus chrysops) and a deceased catshark ( Galeus melastomus). The effects of tissue heterogeneity on hydrogel delivery and fluorescence visibility were explored, with darker tissues masking hydrogel fluorescence. Hydrogels were implanted into a living eastern river cooter ( Pseudemys concinna), a European eel ( Anguilla anguilla), and a second species of catshark ( Scyliorhinus stellaris). The animals displayed no observable changes in movement and feeding patterns. Imaging by high-resolution ultrasound indicated no changes in tissue structure in the eel and catshark. In the turtle, some tissue reaction was detected upon dissection and histopathology. Analysis of movement patterns in sarasa comet goldfish ( Carassius auratus) indicated that the hydrogel implants did not affect swimming patterns. Taken together, these results indicate that this implantable form factor is a promising technique for biologging using aquatic vertebrates with further development. Future work will tune the sensor detection range to the physiological range of riboflavin, develop strategies to normalize sensor signal to account for the optical heterogeneity of animal tissues, and design a flexible, wearable device incorporating optoelectronic components that will enable sensor measurements in moving animals. This work advances the application of nanosensors to organisms beyond the commonly used rodent and zebrafish models and is an important step toward the physiological biologging of aquatic organisms.

Temperature and the vertical movements of oceanic whitetip sharks, Carcharhinus longimanus.

Large-bodied pelagic ectotherms such as sharks need to maintain internal temperatures within a favourable range in order to maximise performance and be cost-efficient foragers. This implies that behavioural thermoregulation should be a key feature of the movements of these animals, although field evidence is limited. We used depth and temperature archives from pop-up satellite tags to investigate the role of temperature in driving vertical movements of 16 oceanic whitetip sharks, Carcharhinus longimanus, (OWTs). Spectral analysis, linear mixed modelling, segmented regression and multivariate techniques were used to examine the effect of mean sea surface temperature (SST) and mixed layer depth on vertical movements. OWTs continually oscillated throughout the upper 200 m of the water column. In summer when the water column was stratified with high SSTs, oscillations increased in amplitude and cycle length and sharks reduced the time spent in the upper 50 m. In winter when the water column was cooler and well-mixed, oscillations decreased in amplitude and cycle length and sharks frequently occupied the upper 50 m. SSTs of 28 oC marked a distinct change in vertical movements and the onset of thermoregulation strategies. Our results have implications for the ecology of these animals in a warming ocean.

Habitat degradation negatively affects auditory settlement behavior of coral reef fishes.

Coral reefs are increasingly degraded by climate-induced bleaching and storm damage. Reef recovery relies on recruitment of young fishes for the replenishment of functionally important taxa. Acoustic cues guide the orientation, habitat selection, and settlement of many fishes, but these processes may be impaired if degradation alters reef soundscapes. Here, we report spatiotemporally matched evidence of soundscapes altered by degradation from recordings taken before and after recent severe damage on Australia's Great Barrier Reef. Postdegradation soundscapes were an average of 15 dB re 1 µPa quieter and had significantly reduced acoustic complexity, richness, and rates of invertebrate snaps compared with their predegradation equivalents. We then used these matched recordings in complementary light-trap and patch-reef experiments to assess responses of wild fish larvae under natural conditions. We show that postdegradation soundscapes were 8% less attractive to presettlement larvae and resulted in 40% less settlement of juvenile fishes than predegradation soundscapes; postdegradation soundscapes were no more attractive than open-ocean sound. However, our experimental design does not allow an estimate of how much attraction and settlement to isolated postdegradation soundscapes might change compared with isolated predegradation soundscapes. Reductions in attraction and settlement were qualitatively similar across and within all trophic guilds and taxonomic groups analyzed. These patterns may lead to declines in fish populations, exacerbating degradation. Acoustic changes might therefore trigger a feedback loop that could impair reef resilience. To understand fully the recovery potential of coral reefs, we must learn to listen.

School is out on noisy reefs: the effect of boat noise on predator learning and survival of juvenile coral reef fishes.

Noise produced by anthropogenic activities is increasing in many marine ecosystems. We investigated the effect of playback of boat noise on fish cognition. We focused on noise from small motorboats, since its occurrence can dominate soundscapes in coastal communities, the number of noise-producing vessels is increasing rapidly and their proximity to marine life has the potential to cause deleterious effects. Cognition-or the ability of individuals to learn and remember information-is crucial, given that most species rely on learning to achieve fitness-promoting tasks, such as finding food, choosing mates and recognizing predators. The caveat with cognition is its latent effect: the individual that fails to learn an important piece of information will live normally until the moment where it needs the information to make a fitness-related decision. Such latent effects can easily be overlooked by traditional risk assessment methods. Here, we conducted three experiments to assess the effect of boat noise playbacks on the ability of fish to learn to recognize predation threats, using a common, conserved learning paradigm. We found that fish that were trained to recognize a novel predator while being exposed to 'reef + boat noise' playbacks failed to subsequently respond to the predator, while their 'reef noise' counterparts responded appropriately. We repeated the training, giving the fish three opportunities to learn three common reef predators, and released the fish in the wild. Those trained in the presence of 'reef + boat noise' playbacks survived 40% less than the 'reef noise' controls over our 72 h monitoring period, a performance equal to that of predator-naive fish. Our last experiment indicated that these results were likely due to failed learning, as opposed to stress effects from the sound exposure. Neither playbacks nor real boat noise affected survival in the absence of predator training. Our results indicate that boat noise has the potential to cause latent effects on learning long after the stressor has gone.

Genome-wide comparisons reveal a clinal species pattern within a holobenthic octopod-the Australian Southern blue-ringed octopus, Hapalochlaena maculosa (Cephalopoda: Octopodidae).

The southern blue-ringed octopus, Hapalochlaena maculosa (Hoyle, 1883) lacks a planktonic dispersal phase, yet ranges across Australia's southern coastline. This species' brief and holobenthic life history suggests gene flow might be limited, leaving distant populations prone to strong genetic divergence. This study used 17,523 genome-wide SNP loci to investigate genetic structuring and local adaptation patterns of H. maculosa among eight sampling sites along its reported range. Within sites, interrelatedness was very high, consistent with the limited dispersal of this taxon. However, inbreeding coefficients were proportionally lower among sites where substructuring was not detected, suggesting H. maculosa might possess a mechanism for inbreeding avoidance. Genetic divergence was extremely high among all sites, with the greatest divergence observed between both ends of the distribution, Fremantle, WA, and Stanley, TAS. Genetic distances closely followed an isolation by geographic distance pattern. Outlier analyses revealed distinct selection signatures at all sites, with the strongest divergence reported between Fremantle and the other Western Australian sites. Phylogenetic reconstructions using the described sister taxon H. fasciata (Hoyle, 1886) further supported that the genetic divergence between distal H. maculosa sites in this study was equivalent to that of between established heterospecifics within this genus. However, it is advocated that taxonomic delineations within this species should be made with caution. These data indicate that H. maculosa forms a clinal species pattern across its geographic range, with gene flow present through allele sharing between adjacent populations. Morphological investigations are recommended for a robust resolution of the taxonomic identity and ecotype boundaries of this species.