A sound beginning of life starts before birth.

Long-term impact from prenatal noise exposure in birds should raise general concern.

An experimental sound exposure study at sea: No spatial deterrence of free-ranging pelagic fisha).

Acoustic deterrent devices are used to guide aquatic animals from danger or toward migration paths. At sea, moderate sounds can potentially be used to deter fish to prevent injury or death due to acoustic overexposure. In sound exposure studies, acoustic features can be compared to improve deterrence efficacy. In this study, we played 200-1600 Hz pulse trains from a drifting vessel and investigated changes in pelagic fish abundance and behavior by utilizing echosounders and hydrophones mounted to a transect of bottom-moored frames. We monitored fish presence and tracked individual fish. This revealed no changes in fish abundance or behavior, including swimming speed and direction of individuals, in response to the sound exposure. We did find significant changes in swimming depth of individually tracked fish, but this could not be linked to the sound exposures. Overall, the results clearly show that pelagic fish did not flee from the current sound exposures, and we found no clear changes in behavior due to the sound exposure. We cannot rule out that different sounds at higher levels elicit a deterrence response; however, it may be that pelagic fish are just more likely to respond to sound with (short-lasting) changes in school formation.

Separate and combined effects of boat noise and a live crab predator on mussel valve gape behavior.

Noisy human activities at sea are changing the acoustic environment, which has been shown to affect marine mammals and fishes. Invertebrates, such as bivalves, have so far received limited attention despite their important role in the marine ecosystem. Several studies have examined the impact of sound on anti-predator behavior using simulated predators, but studies using live predators are scarce. In the current study, we examined the separate and combined effects of boat sound playback and predator cues of shore crabs (Carcinus maenas) on the behavior of mussels (Mytilus spp.). We examined the behavior of the mussels using a valve gape monitor and scored the behavior from the crabs in one of two types of predator test conditions from video footage to control for effects from potential, sound-induced variation in crab behavior. We found that mussels closed their valve gape during boat noise and with a crab in their tank, but also that the stimulus combination did not add up to an even smaller valve gape. The sound treatment did not affect the stimulus crabs, but the behavior of the crabs did affect the valve gape of the mussels. Future research is needed to examine whether these results stand in situ and whether valve closure due to sound has fitness consequences for mussels. The effects on the well-being of individual mussels from anthropogenic noise may be relevant for population dynamics in the context of pressure from other stressors, their role as an ecosystem engineer, and in the context of aquaculture.

Anthropogenic noise pollution and wildlife diseases.

There is a global rise in anthropogenic noise and a growing awareness of its negative effects on wildlife, but to date the consequences for wildlife diseases have received little attention. In this paper, we discuss how anthropogenic noise can affect the occurrence and severity of infectious wildlife diseases. We argue that there is potential for noise impacts at three main stages of pathogen transmission and disease development: (i) the probability of preinfection exposure, (ii) infection upon exposure, and (iii) severity of postinfection consequences. We identify potential repercussions of noise pollution effects for wildlife populations and call for intensifying research efforts. We provide an overview of knowledge gaps and outline avenues for future studies into noise impacts on wildlife diseases.

A decade of underwater noise research in support of the European Marine Strategy Framework Directive.

Underwater noise from human activities is now widely recognised as a threat to marine life. Nevertheless, legislation which directly addresses this source of pollution is lacking. The first (and currently only) example globally is Descriptor 11 of the Marine Strategy Framework Directive (MSFD), adopted by the European Union in 2008, which requires that levels of underwater noise pollution do not adversely affect marine ecosystems. The MSFD has stimulated a concerted research effort across Europe to develop noise monitoring programmes and to conduct research towards specifying threshold values which would define 'Good Environmental Status' (GES) for underwater noise. Here, we chart the progress made during the first decade of Descriptor 11's implementation: 2010-2020. Several international joint monitoring programmes have been established for impulsive and continuous noise, enabling ecosystem-scale assessment for the first time. Research into the impact of noise on individual animals has grown exponentially, demonstrating a range of adverse effects at various trophic levels. However, threshold values for GES must be defined for 'populations of marine animals.' Population-level consequences of noise exposure can be modelled, but data to parameterise such models are currently unavailable for most species, suggesting that alternative approaches to defining GES thresholds will be necessary. To date, the application of measures to reduce noise levels (quieting/noise abatement) has been limited. To address this, the EU in 2021 identified an explicit need to reduce underwater noise pollution in its waters. Delivering on this ambition will require further research focused on the development and implementation of quieting measures.

Male song stability shows cross-year repeatability but does not affect reproductive success in a wild passerine bird.

Predictable behaviour (or 'behavioural stability') might be favoured in certain ecological contexts, for example when representing a quality signal. Costs associated with producing stable phenotypes imply selection should favour plasticity in stability when beneficial. Repeatable among-individual differences in degree of stability are simultaneously expected if individuals differ in ability to pay these costs, or in how they resolve cost-benefit trade-offs. Bird song represents a prime example, where stability may be costly yet beneficial when stable singing is a quality signal favoured by sexual selection. Assuming energetic costs, ecological variation (e.g. in food availability) should result in both within- and among-individual variation in stability. If song stability represents a quality signal, we expect directional selection favouring stable singers. For a 3-year period, we monitored 12 nest box plots of great tits Parus major during breeding. We recorded male songs during simulated territory intrusions, twice during their mate's laying stage and twice during incubation. Each preceding winter, we manipulated food availability. Assuming that stability is costly, we expected food-supplemented males to sing more stable songs. We also expected males to sing more stable songs early in the breeding season (when paternity is not decided) and stable singers to have increased reproductive success. We found strong support for plasticity in stability for two key song characteristics: minimum frequency and phrase length. Males were plastic because they became more stable over the season, contrary to expectations. Food supplementation did not affect body condition but increased stability in minimum frequency. This treatment effect occurred only in 1 year, implying that food supplementation affected stability only in interaction with (unknown) year-specific ecological factors. We found no support for directional, correlational or fluctuating selection on the stability in minimum frequency (i.e. the song trait whose stability exhibited cross-year repeatability): stable singers did not have higher reproductive success. Our findings imply that stability in minimum frequency is not a fitness quality indicator unless males enjoy fitness benefits via pathways not studied here. Future studies should thus address the mechanisms shaping and maintaining individual repeatability of song stability in the wild.

An experimental test of chronic traffic noise exposure on parental behaviour and reproduction in zebra finches.

Chronic traffic noise is increasingly recognised as a potential hazard to wildlife. Several songbird species have been shown to breed poorly in traffic noise exposed habitats. However, identifying whether noise is causal in this requires experimental approaches. We tested whether experimental exposure to chronic traffic noise affected parental behaviour and reproductive success in zebra finches (Taeniopygia guttata). In a counterbalanced repeated-measures design, breeding pairs were exposed to continuous playback of one of two types of highway noise previously shown to be either neutral (control) or aversive. Parental nest attendance positively correlated with feeding effort and was higher for the aversive than the control sound and this effect was more pronounced for parents attending larger broods. However, neither noise condition affected offspring number, growth or body mass. The absence of an effect held when we combined our data with data from two other comparable studies into a meta-analysis. We discuss whether the increased nest attendance could be a compensatory strategy that alleviated detrimental noise effects on the chicks, and whether it could be caused by impaired parent-offspring or within-pair communication. Future work should test these hypotheses and investigate potential long-term costs of increased parental engagement.

Effects of pile driving sound on local movement of free-ranging Atlantic cod in the Belgian North Sea.

Offshore energy acquisition through the construction of wind farms is rapidly becoming one of the major sources of green energy all over the world. The construction of offshore wind farms contributes to the ocean soundscape as steel monopile foundations are commonly hammered into the seabed to anchor wind turbines. This pile driving activity causes repeated, impulsive, low-frequency sounds, reaching far into the environment, which may have an impact on the surrounding marine life. In this study, we investigated the effect of the construction of 50 wind turbine foundations, over a time span of four months, on the presence and movement behaviour of free-swimming, individually tagged Atlantic cod. The turbine foundations were constructed at a distance ranging between 2.3 and 7.1 km from the cod, which resided in a nearby, existing wind farm in the southern North Sea. Our results indicated that local fish remained in the exposed area during and in-between pile-driving activities, but showed some modest changes in movement patterns. The tagged cod did not increase their net movement activity, but moved closer to the scour-bed (i.e. hard substrate), surrounding their nearest turbine, during and after each piling event. Additionally, fish moved further away from the sound source, which was mainly due to the fact that they were positioned closer to a piling event before its start. We found no effect of the time since the last piling event. Long-term changes in movement behaviour can result in energy budget changes, and thereby in individual growth and maturation, eventually determining growth rate of populations. Consequently, although behavioural changes to pile driving in the current study seem modest, we believe that the potential for cumulative effects, and species-specific variation in impact, warrant more tagging studies in the future, with an emphasis on quantification of energy budgets.

North Sea soundscapes from a fish perspective: Directional patterns in particle motion and masking potential from anthropogenic noise.

The aquatic world of animals is an acoustic world as sound is the most prominent sensory capacity to extract information about the environment for many aquatic species. Fish can hear particle motion, and a swim bladder potentially adds the additional capacity to sense sound pressure. Combining these capacities allows them to sense direction, distance, spectral content, and detailed temporal patterns. Both sound pressure and particle motion were recorded in a shallow part of the North Sea before and during exposure to a full-scale airgun array from an experimental seismic survey. Distinct amplitude fluctuations and directional patterns in the ambient noise were found to be fluctuating in phase with the tidal cycles and coming from distinct directions. It was speculated that the patterns may be determined by distant sources associated with large rivers and nearby beaches. Sounds of the experimental seismic survey were above the ambient conditions for particle acceleration up to 10 km from the source, at least as detectable for the measurement device, and up to 31 km for the sound pressure. These results and discussion provide a fresh perspective on the auditory world of fishes and a shift in the understanding about potential ranges over which they may have access to biologically relevant cues and be masked by anthropogenic noise.

An echosounder view on the potential effects of impulsive noise pollution on pelagic fish around windfarms in the North Sea.

Anthropogenic noise in the oceans is disturbing marine life. Among other groups, pelagic fish are likely to be affected by sound from human activities, but so far have received relatively little attention. Offshore wind farms have become numerous and will become even more abundant in the next decades. Wind farms can be interesting to pelagic fish due to food abundance or fisheries restrictions. At the same time, construction of wind farms involves high levels of anthropogenic noise, likely disturbing and/or deterring pelagic fish. Here, we investigated whether bottom-moored echosounders are a suitable tool for studying the effects of impulsive - intermittent, high-intensity - anthropogenic noise on pelagic fish around wind farms and we explored the possible nature of their responses. Three different wind farms along the Dutch and Belgian coast were examined, one with exposure to the passing by of an experimental seismic survey with a full-scale airgun array, one with pile driving activity in an adjacent wind farm construction site and one control site without exposure. Two bottom-moored echosounders were placed in each wind farm and recorded fish presence and behaviour before, during and after the exposures. The echosounders were successful in detecting variation in the number of fish schools and their behaviour. During the seismic survey exposure there were significantly fewer, but more cohesive, schools than before, whereas during pile driving fish swam shallower with more cohesive schools. However, the types and magnitudes of response patterns were also observed at the control site with no impulsive sound exposure. We therefore stress the need for thorough replication beyond single case studies, before we can conclude that impulsive sounds, from either seismic surveys or pile driving, are a disturbing factor for pelagic fish in otherwise attractive habitat around wind farms.

The importance of individual variation for the interpretation of behavioural studies: ethanol effects vary with basal activity level in zebrafish larvae.

Standardization and reduction of variation is key to behavioural screening of animal models in toxicological and pharmacological studies. However, individual variation in behavioural and physiological phenotypes remains in each laboratory population and can undermine the understanding of toxicological and pharmaceutical effects and their underlying mechanisms. Here, we used zebrafish (ABTL-strain) larvae to explore individual consistency in activity level and emergence time, across subsequent days of early development (6-8 dpf). We also explored the correlation between these two behavioural parameters. We found inter-individual consistency over time in activity level and emergence time, but we did not find a consistent correlation between these parameters. Subsequently, we investigated the impact of variation in activity level on the effect of a 1% ethanol treatment, suitable for our proof-of-concept case study about whether impact from pharmacological treatments might be affected by inter-individual variation in basal locomotion. The inter-individual consistency over time in activity level did not persist in this test. This was due to the velocity change from before to after exposure, which turned out to be a dynamic individual trait related to basal activity level: low-activity individuals raised their swimming velocity, while high-activity individuals slowed down, yielding diametrically opposite response patterns to ethanol exposure. We therefore argue that inter-individual consistency in basal activity level, already from 6 dpf, is an important factor to take into account and provides a practical measure to improve the power of statistical analyses and the scope for data interpretation from behavioural screening studies.

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.

Effects of a seismic survey on movement of free-ranging Atlantic cod.

Geophysical exploration of the seabed is typically done through seismic surveys, using airgun arrays that produce intense, low-frequency-sound pulses1 that can be heard over hundreds of square kilometers, 24/7.2,3 Little is known about the effects of these sounds on free-ranging fish behavior.4-6 Effects reported range from subtle individual change in activity and swimming depth for captive fish7,8 to potential avoidance9 and changes in swimming velocity and diurnal activity patterns for free-swimming animals.10 However, the extent and duration of behavioral responses to seismic surveys remain largely unexplored for most fish species.4 In this study, we investigated the effect of a full-scale seismic survey on the movement behavior of free-swimming Atlantic cod (Gadus morhua). We found that cod did not leave the detection area more than expected during the experimental survey but that they left more quickly from 2 days to 2 weeks after the survey. Furthermore, during the exposure, cod decreased their activity, with time spent being "locally active" (moving small distances, showing high body acceleration) becoming shorter, and time spent being "inactive" (moving small distances, having low body acceleration) becoming longer. Additionally, diurnal activity cycles were disrupted with lower locally active peaks at dusk and dawn, periods when cod are known to actively feed.11,12 The combined effects of delayed deterrence and activity disruption indicate the potential for seismic surveys to affect energy budgets and to ultimately lead to population-level consequences.13.

Effects of seismic airgun playbacks on swimming patterns and behavioural states of Atlantic cod in a net pen.

Anthropogenic sound can affect fish behaviour and physiology which may affect their well-being. However, it remains a major challenge to translate such effects to consequences for fitness at an individual and population level. For this, energy budget models have been developed, but suitable data to parametrize these models are lacking. A first step towards such parametrization concerns the objective quantification of behavioural states at high resolution. We experimentally exposed individual Atlantic cod (Gadus morhua) in a net pen to the playback of seismic airgun sounds. We demonstrated that individual cod in the net pen did not change their swimming patterns immediately at the onset of the sound exposure. However, several individuals changed their time spent in three different behavioural states during the 1 h exposure. This may be translated to changes in energy expenditure and provide suitable input for energy budget models that allow predictions about fitness and population consequences.

The role of the Glucocorticoid Receptor in the Regulation of Diel Rhythmicity.

Virtually all organisms have adapted to the earth's day-night cycles by the evolution of endogenous rhythms that regulate most biological processes. Recent research has highlighted the role of glucocorticoids and the Glucocorticoid receptor (GR) in coordinating clock function across various levels of biological organisation. In the present study, we have explored the role of the GR in the rhythmicity of the biological clock, by comparing 5 day old wildtype zebrafish larvae (gr+) with mutant larvae with a non-functional GR (grs357). The mutants display a weaker rhythmicity in locomotor activity in wildtypes than in mutants, while the rhythmicity of the angular velocity was higher for wildtypes. The melatonin production of the mutants showed a weaker rhythmicity, but surprisingly, there were no differences in the rhythmicity of clock-related gene expression between genotypes that could explain a mechanism for GR functionality at the transcriptional level. Furthermore, our results show that grs357 larvae have a more erratic swimming path, and cover more distance during locomotor activity than wild type larvae, in line with previously described behaviour of this mutant. Therefore, these results suggest that GR affects the diel rhythmicity of zebrafish larvae at the behavioural and endocrine level, but that these effects are not mediated by changes in the expression of clock-related genes.

Population-level effects of acoustic disturbance in Atlantic cod: a size-structured analysis based on energy budgets.

Anthropogenic underwater noise may negatively affect marine animals. Yet, while fishes are highly sensitive to sounds, effects of acoustic disturbances on fishes have not been extensively studied at the population level. In this study, we use a size-structured model based on energy budgets to analyse potential population-level effects of anthropogenic noise on Atlantic cod (Gadus morhua). Using the model framework, we assess the impact of four possible effect pathways of disturbance on the cod population growth rate. Through increased stress, changes in foraging and movement behaviour, and effects on the auditory system, anthropogenic noise can lead to (i) increased energy expenditure, (ii) reduced food intake, (iii) increased mortality, and (iv) reduced reproductive output. Our results show that population growth rates are particularly sensitive to changes in energy expenditure and food intake because they indirectly affect the age of maturation, survival and fecundity. Sub-lethal effects of sound exposure may thus affect populations of cod and fishes with similar life histories more than lethal effects of sound exposure. Moreover, anthropogenic noise may negatively affect populations when causing persistent increases of energy expenditure or decreases of food intake. Effects of specific acoustic pollutants on energy acquisition and expenditure should therefore be further investigated.

Diving apart together: call propagation in diving long-finned pilot whales.

Group-living animals must communicate to stay in contact. In long-finned pilot whales, there is a trade-off between the benefits of foraging individually at depth and the formation of tight social groups at the surface. Using theoretical modelling and empirical data of tagged pairs within a group, we examined the potential of pilot whale social calls to reach dispersed group members during foraging periods. Both theoretical predictions and empirical data of tag pairs showed a potential for communication between diving and non-diving group members over separation distances up to 385 m (empirical) and 1800 m (theoretical). These distances match or exceed pilot whale dive depths recorded across populations. Call characteristics and environmental characteristics were analysed to investigate determinants of call detectability. Longer calls with a higher sound pressure level (SPL) that were received in a quieter environment were more often detected than their shorter, lower SPL counterparts within a noisier environment. In a noisier environment, calls were louder and had a lower peak frequency, indicating mechanisms for coping with varying conditions. However, the vulnerability of pilot whales to anthropogenic noise is still of concern as the ability to cope with increasing background noise may be limited. Our study shows that combining propagation modelling and actual tag recordings provides new insights into the communicative potential for social calls in orientation and reunion with group members for deep-diving pilot whales.

Profound effects of glucocorticoid resistance on anxiety-related behavior in zebrafish adults but not in larvae.

Previously, adult zebrafish with a mutation in the gene encoding the glucocorticoid receptor (Gr) were demonstrated to display anxiety- and depression-like behavior that could be reversed by treatment with antidepressant drugs, suggesting that this model system could be applied to study novel therapeutic strategies against depression. Subsequent studies with zebrafish larvae from this grs357 line and a different gr mutant have not confirmed these effects. To investigate this discrepancy, we have analyzed the anxiety-like behavior in 5 dpf grs357 larvae using a dark/tapping stimulus test and a light/dark preference test. In addition, grs357 adult fish were subjected to an open field test. The results showed that in larvae the mutation mainly affected general locomotor activity (decreased velocity in the dark/tapping stimulus test, increased velocity in the light/dark preference test). However, parameters considered specific readouts for anxiety-like behavior (response to dark/tapping stimulus, time spent in dark zone) were not altered by the mutation. In adults, the mutants displayed a profound increase in anxiety-like behavior (time spent in outer zone in open field test), besides changes in locomotor activity (decreased velocity, increased angular velocity and freezing time). We conclude that the neuronal circuitry involved in anxiety- and depression-like behavior is largely affected by deficient Gr signaling in adult fish but not in larvae, indicating that this circuitry only fully develops after the larval stages in zebrafish. This makes the zebrafish an interesting model to study the ontology of anxiety- and depression-related pathology which results from deficient glucocorticoid signaling.

Noise pollution.

Noise pollution has spread over the entire globe: from the initial rumble in the Stone age, the invention of gun powder, and a steady rise during the industrial revolution, to a global acceleration in the second half of the 20th century. Hans Slabbekoorn highlights what we know about the impact of this acoustic climate change, on humans and animals alike.