Context-dependent multimodal behaviour in a coral reef fish.

Animals are expected to respond flexibly to changing circumstances, with multimodal signalling providing potential plasticity in social interactions. While numerous studies have documented context-dependent behavioural trade-offs in terrestrial species, far less work has considered such decision-making in fish, especially in natural conditions. Coral reef ecosystems host 25% of all known marine species, making them hotbeds of competition and predation. We conducted experiments with wild Ambon damselfish (Pomacentrus amboinensis) to investigate context-dependent responses to a conspecific intruder; specifically, how nest defence is influenced by an elevated predation risk. We found that nest-defending male Ambon damselfish responded aggressively to a conspecific intruder, spending less time sheltering and more time interacting, as well as signalling both visually and acoustically. In the presence of a model predator compared to a model herbivore, males spent less time interacting with the intruder, with a tendency towards reduced investment in visual displays compensated for by an increase in acoustic signalling instead. We therefore provide ecologically valid evidence that the context experienced by an individual can affect its behavioural responses and multimodal displays towards conspecific threats.

Respiratory acidosis and O2 supply capacity do not affect the acute temperature tolerance of rainbow trout (Oncorhynchus mykiss).

The mechanisms that determine the temperature tolerances of fish are poorly understood, creating barriers to disentangle how additional environmental challenges-such as CO2-induced aquatic acidification and fluctuating oxygen availability-may exacerbate vulnerability to a warming climate and extreme heat events. Here, we explored whether two acute exposures (~0.5 hours or ~72 hours) to increased CO2 impact acute temperature tolerance limits in a freshwater fish, rainbow trout (Oncorhynchus mykiss). We separated the potential effects of acute high CO2 exposure on critical thermal maximum (CTmax), caused via either respiratory acidosis (reduced internal pH) or O2 supply capacity (aerobic scope), by exposing rainbow trout to ~1 kPa CO2 (~1% or 10 000 µatm) in combination with normoxia or hyperoxia (~21 or 42 kPa O2, respectively). In normoxia, acute exposure to high CO2 caused a large acidosis in trout (blood pH decreased by 0.43 units), while a combination of hyperoxia and ~1 kPa CO2 increased the aerobic scope of trout by 28%. Despite large changes in blood pH and aerobic scope between treatments, we observed no impacts on the CTmax of trout. Our results suggest that the mechanisms that determine the maximum temperature tolerance of trout are independent of blood acid-base balance or the capacity to deliver O2 to tissues.

Metagenomics for Pathogen Detection During a Mass Mortality Event in Songbirds.

Mass mortality events in wildlife can be indications of an emerging infectious disease. During the spring and summer of 2021, hundreds of dead passerines were reported across the eastern US. Birds exhibited a range of clinical signs including swollen conjunctiva, ocular discharge, ataxia, and nystagmus. As part of the diagnostic investigation, high-throughput metagenomic next-generation sequencing was performed across three molecular laboratories on samples from affected birds. Many potentially pathogenic microbes were detected, with bacteria forming the largest proportion; however, no singular agent was consistently identified, with many of the detected microbes also found in unaffected (control) birds and thus considered to be subclinical infections. Congruent results across laboratories have helped drive further investigation into alternative causes, including environmental contaminants and nutritional deficiencies. This work highlights the utility of metagenomic approaches in investigations of emerging diseases and provides a framework for future wildlife mortality events.

Predatory trumpetfish conceal themselves from their prey by swimming alongside other fish.

Many animals use camouflage to avoid detection by others, yet even the most inconspicuous objects become detectable against the background when moving1,2. One way to reduce detection while moving would be to 'hide' behind the movements of objects or other animals3. Here, we demonstrate experimentally that a common marine predator, the trumpetfish (Aulostomus maculatus), can conceal its approach from its prey by performing a behaviour known as 'shadowing' - swimming closely next to another, larger and non-predatory fish3,4,5. Our findings reveal how predators can actively use another animal as a form of concealment to reduce detection by prey.

Sea temperature is the primary driver of recent and predicted fish community structure across Northeast Atlantic shelf seas.

Climate change has strongly influenced the distribution and abundance of marine fish species, leading to concern about effects of future climate on commercially harvested stocks. Understanding the key drivers of large-scale spatial variation across present-day marine assemblages enables predictions of future change. Here we present a unique analysis of standardised abundance data for 198 marine fish species from across the Northeast Atlantic collected by 23 surveys and 31,502 sampling events between 2005 and 2018. Our analyses of the spatially comprehensive standardised data identified temperature as the key driver of fish community structure across the region, followed by salinity and depth. We employed these key environmental variables to model how climate change will affect both the distributions of individual species and local community structure for the years 2050 and 2100 under multiple emissions scenarios. Our results consistently indicate that projected climate change will lead to shifts in species communities across the entire region. Overall, the greatest community-level changes are predicted at locations with greater warming, with the most pronounced effects at higher latitudes. Based on these results, we suggest that future climate-driven warming will lead to widespread changes in opportunities for commercial fisheries across the region.

Limiting motorboat noise on coral reefs boosts fish reproductive success.

Anthropogenic noise impacts are pervasive across taxa, ecosystems and the world. Here, we experimentally test the hypothesis that protecting vulnerable habitats from noise pollution can improve animal reproductive success. Using a season-long field manipulation with an established model system on the Great Barrier Reef, we demonstrate that limiting motorboat activity on reefs leads to the survival of more fish offspring compared to reefs experiencing busy motorboat traffic. A complementary laboratory experiment isolated the importance of noise and, in combination with the field study, showed that the enhanced reproductive success on protected reefs is likely due to improvements in parental care and offspring length. Our results suggest noise mitigation could have benefits that carry through to the population-level by increasing adult reproductive output and offspring growth, thus helping to protect coral reefs from human impacts and presenting a valuable opportunity for enhancing ecosystem resilience.

Uptake of microplastics by the snakelocks anemone (Anemonia viridis) is commonplace across environmental conditions.

Microplastics (<1 mm) are ubiquitous in our oceans and widely acknowledged as concerning contaminants due to the multi-faceted threats they exert on marine organisms and ecosystems. Anthozoans, including sea anemones and corals, are particularly at risk of microplastic uptake due to their proximity to the coastline, non-selective feeding mechanisms and sedentary nature. Here, the common snakelocks anemone (Anemonia viridis) was used to generate understanding of microplastic uptake in the relatively understudied Anthozoa class. A series of microplastic exposure and multi-stressor experiments were performed to examine particle shape and size selectivity, and to test for the influence of food availability and temperature on microplastic uptake. All A. viridis individuals were found to readily take up microplastics (mean 142.1 ± 83.4 particles per gram of tissue) but exhibited limited preference between different particle shapes and sizes (n = 32). Closer examination identified that uptake involved both ingestion and external tissue adhesion, where microplastics were trapped in secreted mucus. Microplastic uptake in A. viridis was not influenced by the presence of food or elevated water temperature (n = 40). Furthermore, environmental sampling was performed to investigate microplastic uptake in A. viridis (n = 8) on the coast of southwest England, with a mean of 17.5 ± 4.0 particles taken up per individual. Fibres represented the majority of particles (91%) followed by fragments (9%), with 87% either clear, blue or black in colour. FTIR analysis identified 70% of the particles as anthropogenic cellulosic or plastic polymers. Thus, this study provides evidence of microplastic uptake by A. viridis in both laboratory exposures experiments and in the marine environment. These findings support recent literature suggesting that external adhesion may be the primary mechanism in which anthozoans capture microplastics from the water column and highlights the potential role anemones can play as environmental microplastic bioindicators.

Rapid blood acid-base regulation by European sea bass (Dicentrarchus labrax) in response to sudden exposure to high environmental CO2.

Fish in coastal ecosystems can be exposed to acute variations in CO2 of between 0.2 and 1 kPa CO2 (2000-10,000 µatm). Coping with this environmental challenge will depend on the ability to rapidly compensate for the internal acid-base disturbance caused by sudden exposure to high environmental CO2 (blood and tissue acidosis); however, studies about the speed of acid-base regulatory responses in marine fish are scarce. We observed that upon sudden exposure to ∼1 kPa CO2, European sea bass (Dicentrarchus labrax) completely regulate erythrocyte intracellular pH within ∼40 min, thus restoring haemoglobin-O2 affinity to pre-exposure levels. Moreover, blood pH returned to normal levels within ∼2 h, which is one of the fastest acid-base recoveries documented in any fish. This was achieved via a large upregulation of net acid excretion and accumulation of HCO3- in blood, which increased from ∼4 to ∼22 mmol l-1. While the abundance and intracellular localisation of gill Na+/K+-ATPase (NKA) and Na+/H+ exchanger 3 (NHE3) remained unchanged, the apical surface area of acid-excreting gill ionocytes doubled. This constitutes a novel mechanism for rapidly increasing acid excretion during sudden blood acidosis. Rapid acid-base regulation was completely prevented when the same high CO2 exposure occurred in seawater with experimentally reduced HCO3- and pH, probably because reduced environmental pH inhibited gill H+ excretion via NHE3. The rapid and robust acid-base regulatory responses identified will enable European sea bass to maintain physiological performance during large and sudden CO2 fluctuations that naturally occur in coastal environments.

Anthropogenic underwater vibrations are sensed and stressful for the shore crab Carcinus maenas.

Acoustic pollution in aquatic environments has increased with adverse effects on many aquatic organisms. However, little work has been done considering the effects of the vibratory component of acoustic stimuli, which can be transmitted in the substrate and propagated into the aquatic medium. Benthic marine organisms, including many invertebrates, are capable of sensing seabed vibration, yet the responses they trigger on organism have received little attention. This study investigates the impact of underwater vibration on the physiology and behaviour of a ubiquitous inhabitant of coastal areas of the northern hemisphere, the shore crab Carcinus maenas. We developed a novel vibratory apparatus with geophones supported on a softly sprung frame to induce a seabed vibration of 20 Hz frequency, as observed during dredging, piling and other anthropogenic activities. The geophone internal mass caused the frame to vibrate in a controlled manner. Our results show that transition from ambient to anthropogenic vibrations induced an increase in activity and antennae beats in shore crabs, indicating perception of the vibratory stimulus and a higher stress level. There was also a trend on sex-specific responses to anthropogenic vibration, with males showing a higher activity level than females. However, no effect of anthropogenic vibrations was found upon oxygen consumption. These results show that anthropogenic underwater vibration induces behavioural responses in Carcinus maenas. This highlights the importance of evaluating man-made vibratory activities on coastal invertebrates and the necessity of evaluating anthropogenic effects on both sexes.

The soundscape of the Anthropocene ocean.

Oceans have become substantially noisier since the Industrial Revolution. Shipping, resource exploration, and infrastructure development have increased the anthrophony (sounds generated by human activities), whereas the biophony (sounds of biological origin) has been reduced by hunting, fishing, and habitat degradation. Climate change is affecting geophony (abiotic, natural sounds). Existing evidence shows that anthrophony affects marine animals at multiple levels, including their behavior, physiology, and, in extreme cases, survival. This should prompt management actions to deploy existing solutions to reduce noise levels in the ocean, thereby allowing marine animals to reestablish their use of ocean sound as a central ecological trait in a healthy ocean.

Assessing and mitigating impacts of motorboat noise on nesting damselfish.

Motorboats are a pervasive, growing source of anthropogenic noise in marine environments, with known impacts on fish physiology and behaviour. However, empirical evidence for the disruption of parental care remains scarce and stems predominantly from playback studies. Additionally, there is a paucity of experimental studies examining noise-mitigation strategies. We conducted two field experiments to investigate the effects of noise from real motorboats on the parental-care behaviours of a common coral-reef fish, the Ambon damselfish Pomacentrus amboinensis, which exhibits male-only egg care. When exposed to motorboat noise, we found that males exhibited vigilance behaviour 34% more often and spent 17% more time remaining vigilant, compared to an ambient-sound control. We then investigated nest defence in the presence of an introduced conspecific male intruder, incorporating a third noise treatment of altered motorboat-driving practice that was designed to mitigate noise exposure via speed and distance limitations. The males spent 22% less time interacting with the intruder and 154% more time sheltering during normal motorboat exposure compared to the ambient-sound control, with nest-defence levels in the mitigation treatment equivalent to those in ambient conditions. Our results reveal detrimental impacts of real motorboat noise on some aspects of parental care in fish, and successfully demonstrate the positive effects of an affordable, easily implemented mitigation strategy. We strongly advocate the integration of mitigation strategies into future experiments in this field, and the application of evidence-based policy in our increasingly noisy world.

Can we project changes in fish abundance and distribution in response to climate?

Large-scale and long-term changes in fish abundance and distribution in response to climate change have been simulated using both statistical and process-based models. However, national and regional fisheries management requires also shorter term projections on smaller spatial scales, and these need to be validated against fisheries data. A 26-year time series of fish surveys with high spatial resolution in the North-East Atlantic provides a unique opportunity to assess the ability of models to correctly simulate the changes in fish distribution and abundance that occurred in response to climate variability and change. We use a dynamic bioclimate envelope model forced by physical-biogeochemical output from eight ocean models to simulate changes in fish abundance and distribution at scales down to a spatial resolution of 0.5°. When comparing with these simulations with annual fish survey data, we found the largest differences at the 0.5° scale. Differences between fishery model runs driven by different biogeochemical models decrease dramatically when results are aggregated to larger scales (e.g. the whole North Sea), to total catches rather than individual species or when the ensemble mean instead of individual simulations are used. Recent improvements in the fidelity of biogeochemical models translate into lower error rates in the fisheries simulations. However, predictions based on different biogeochemical models are often more similar to each other than they are to the survey data, except for some pelagic species. We conclude that model results can be used to guide fisheries management at larger spatial scales, but more caution is needed at smaller scales.

Hormonal and behavioural effects of motorboat noise on wild coral reef fish.

Anthropogenic noise is an emergent ecological pollutant in both terrestrial and aquatic habitats. Human population growth, urbanisation, resource extraction, transport and motorised recreation lead to elevated noise that affects animal behaviour and physiology, impacting individual fitness. Currently, we have a poor mechanistic understanding of the effects of anthropogenic noise, but a likely candidate is the neuroendocrine system that integrates information about environmental stressors to produce regulatory hormones; glucocorticoids (GCs) and androgens enable rapid individual phenotypic adjustments that can increase survival. Here, we carried out two field-based experiments to investigate the effects of short-term (30 min) and longer-term (48 h) motorboat-noise playback on the behaviour, GCs (cortisol) and androgens of site-attached free-living orange-fin anemonefish (Amphiprion chrysopterus). In the short-term, anemonefish exposed to motorboat-noise playback showed both behavioural and hormonal responses: hiding and aggression increased, and distance moved out of the anemone decreased in both sexes; there were no effects on cortisol levels, but male androgen levels (11-ketotestosterone and testosterone) increased. Some behaviours showed carry-over effects from motorboat noise after it had ceased, and there was no evidence for a short-term change in response to subsequent motorboat-noise playback. Similarly, there was no evidence that longer-term exposure led to changes in response: motorboat noise had an equivalent effect on anemonefish behaviour and hormones after 48 h as on first exposure. Longer-term noise exposure led to higher levels of cortisol in both sexes and higher testosterone levels in males, and stress-responses to an additional environmental challenge in both sexes were impaired. Circulating androgen levels correlated with aggression, while cortisol levels correlated with hiding, demonstrating in a wild population that androgen/glucocorticoid pathways are plausible proximate mechanisms driving behavioural responses to anthropogenic noise. Combining functional and mechanistic studies are crucial for a full understanding of this global pollutant.

Climate Change Drives Poleward Increases and Equatorward Declines in Marine Species.

Marine environments have increased in temperature by an average of 1°C since pre-industrial (1850) times [1]. Given that species ranges are closely allied to physiological thermal tolerances in marine organisms [2], it may therefore be expected that ocean warming would lead to abundance increases at poleward side of ranges and abundance declines toward the equator [3]. Here, we report a global analysis of abundance trends of 304 widely distributed marine species over the last century, across a range of taxonomic groups from phytoplankton to fish and marine mammals. Specifically, using a literature database, we investigate the extent that the direction and strength of long-term species abundance changes depend on the sampled location within the latitudinal range of species. Our results show that abundance increases have been most prominent where sampling has taken place at the poleward side of species ranges, and abundance declines have been most prominent where sampling has taken place at the equatorward side of species ranges. These data provide evidence of omnipresent large-scale changes in abundance of marine species consistent with warming over the last century and suggest that adaptation has not provided a buffer against the negative effects of warmer conditions at the equatorward extent of species ranges. On the basis of these results, we suggest that projected sea temperature increases of up to 1.5°C over pre-industrial levels by 2050 [4] will continue to drive latitudinal abundance shifts in marine species, including those of importance for coastal livelihoods.

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.

Causes and consequences of intraspecific variation in animal responses to anthropogenic noise.

Anthropogenic noise is a recognized global pollutant, affecting a wide range of nonhuman animals. However, most research considers only whether noise pollution has an impact, ignoring that individuals within a species or population exhibit substantial variation in responses to stress. Here, we first outline how intrinsic characteristics (e.g., body size, condition, sex, and personality) and extrinsic factors (e.g., environmental context, repeated exposure, prior experience, and multiple stressors) can affect responses to environmental stressors. We then present the results of a systematic search of the anthropogenic-noise literature, identifying articles that investigated intraspecific variation in the responses of nonhuman animals to noise. This reveals that fewer than 10% of articles (51 of 589) examining impacts of noise test experimentally for intraspecific variation in responses; of those that do, more than 75% report significant effects. We assess these existing studies to determine the current scope of research and findings to-date, and to provide suggestions for good practice in the design, implementation, and reporting of robust experiments in this field. We close by explaining how understanding intraspecific variation in responses to anthropogenic noise is crucial for improving how we manage captive animals, monitor wild populations, model species responses, and mitigate effects of noise pollution on wildlife. Our aim is to stimulate greater knowledge and more effective management of the harmful consequences of this global pollutant.

Rising CO2 enhances hypoxia tolerance in a marine fish.

Global environmental change is increasing hypoxia in aquatic ecosystems. During hypoxic events, bacterial respiration causes an increase in carbon dioxide (CO2) while oxygen (O2) declines. This is rarely accounted for when assessing hypoxia tolerances of aquatic organisms. We investigated the impact of environmentally realistic increases in CO2 on responses to hypoxia in European sea bass (Dicentrarchus labrax). We conducted a critical oxygen (O2crit) test, a common measure of hypoxia tolerance, using two treatments in which O2 levels were reduced with constant ambient CO2 levels (~530 µatm), or with reciprocal increases in CO2 (rising to ~2,500 µatm). We also assessed blood acid-base chemistry and haemoglobin-O2 binding affinity of sea bass in hypoxic conditions with ambient (~650 µatm) or raised CO2 (~1770 µatm) levels. Sea bass exhibited greater hypoxia tolerance (~20% reduced O2crit), associated with increased haemoglobin-O2 affinity (~32% fall in P50) of red blood cells, when exposed to reciprocal changes in O2 and CO2. This indicates that rising CO2 which accompanies environmental hypoxia facilitates increased O2 uptake by the blood in low O2 conditions, enhancing hypoxia tolerance. We recommend that when impacts of hypoxia on aquatic organisms are assessed, due consideration is given to associated environmental increases in CO2.

A novel CRISPR/Cas9 associated technology for sequence-specific nucleic acid enrichment.

Massively parallel sequencing technologies have made it possible to generate large quantities of sequence data. However, as research-associated information is transferred into clinical practice, cost and throughput constraints generally require sequence-specific targeted analyses. Therefore, sample enrichment methods have been developed to meet the needs of clinical sequencing applications. However, current amplification and hybrid capture enrichment methods are limited in the contiguous length of sequences for which they are able to enrich. PCR based amplification also loses methylation data and other native DNA features. We have developed a novel technology (Negative Enrichment) where we demonstrate targeting long (>10 kb) genomic regions of interest. We use the specificity of CRISPR-Cas9 single guide RNA (Cas9/sgRNA) complexes to define 5' and 3' termini of sequence-specific loci in genomic DNA, targeting 10 to 36 kb regions. The complexes were found to provide protection from exonucleases, by protecting the targeted sequences from degradation, resulting in enriched, double-strand, non-amplified target sequences suitable for next-generation sequencing library preparation or other downstream analyses.