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.

The effect of biological and anthropogenic sound on the auditory sensitivity of oyster toadfish, Opsanus tau.

Many aquatic organisms use vocalizations for reproductive behavior; therefore, disruption of their soundscape could adversely affect their life history. Male oyster toadfish (Opsanus tau) establish nests in shallow waters during spring and attract female fish with boatwhistle vocalizations. Males exhibit high nest fidelity, making them susceptible to anthropogenic sound in coastal waters, which could mask their vocalizations and/or reduce auditory sensitivity levels. Additionally, the effect of self-generated boatwhistles on toadfish auditory sensitivity has yet to be addressed. To investigate the effect of sound exposure on toadfish auditory sensitivity, sound pressure and particle acceleration sensitivity curves were determined using auditory evoked potentials before and after (0-, 1-, 3-, 6- and 9-day) exposure to 1- or 12-h of continuous playbacks to ship engine sound or conspecific vocalization. Exposure to boatwhistles had no effect on auditory sensitivity. However, exposure to anthropogenic sound caused significant decreases in auditory sensitivity for at least 3 days, with shifts up to 8 dB SPL and 20 dB SPL immediately following 1- and 12-h anthropogenic exposure, respectively. Understanding the effect of self-generated and anthropogenic sound exposure on auditory sensitivity provides an insight into how soundscapes affect acoustic communication.

Reproductive state-dependent plasticity in the visual system of an African cichlid fish.

Visual communication is used widely across the animal kingdom to convey crucial information about an animals' identity, reproductive status, and sex. Although it is well-demonstrated that auditory and olfactory sensitivity can change with reproductive state, fewer studies have tested for plasticity in the visual system, a surprising detail since courtship and mate choice behaviors in many species are largely dependent on visual signals. Here, we tested for reproductive state-dependent plasticity in the eye of the cichlid fish Astatotilapia burtoni using behavioral, gene expression, neural activation, and electrophysiology techniques. Males court ovulated females more intensely than gravid females, and ovulated females were more responsive to male courtship behaviors than gravid females. Using electroretinography to measure visual sensitivity in dark-adapted fish, we revealed that gravid, reproductively-ready females have increased visual sensitivity at wavelengths associated with male courtship coloration compared to non-gravid females. After ovulation was hormonally induced, female's spectral sensitivity further increased compared to pre-injection measurements. This increased sensitivity after hormone injection was absent in non-gravid females and in males, suggesting an ovulation-triggered increase in visual sensitivity. Ovulated females had higher mRNA expression levels of reproductive neuromodulatory receptors (sex-steroids; gonadotropins) in the eye than nonovulated females, whereas males had similar expression levels independent of reproductive/social state. In addition, female mate choice-like behaviors positively correlated with expression of gonadotropin system receptors in the eye. Collectively, these data provide crucial evidence linking endocrine modulation of visual plasticity to mate choice behaviors in females.

Ecology of fish hearing.

Underwater sound is directional and can convey important information about the surrounding environment or the animal emitting the sound. Therefore, sound is a major sensory channel for fishes and plays a key role in many life-history strategies. The effect of anthropogenic noise on aquatic life, which may be causing homogenisation or fragmentation of biologically important signals underwater is of growing concern. In this review we discuss the role sound plays in the ecology of fishes, basic anatomical and physiological adaptations for sound reception and production, the effects of anthropogenic noise and how fishes may be coping to changes in their environment, to put the ecology of fish hearing into the context of the modern underwater soundscape.

Barking mad: The vocalisation of the John Dory, Zeus faber.

Studies on the behavioural function of sounds are very rare within heterospecific interactions. John Dory (Zeus faber) is a solitary, predatory fish that produces sound when captured, but has not been documented to vocalize under natural conditions (i.e. in the wild). The present study provides the first in-situ recordings of John Dory vocalisations and correlates them to behavioural response of snapper (Pagrus auratus) a common species found through New Zealand. Vocalisations or 'barks', ranged between 200-600 Hz, with a peak frequency of 312 ± 10 Hz and averaged 139 ± 4 milliseconds in length. Baited underwater video (BUV) equipped with hydrophones determined that under natural conditions a John Dory vocalization induced an escape response in snapper present, causing them to exit the area opposite to the position of the John Dory. We speculate that the John Dory vocalisation may be used for territorial display towards both conspecifics and heterospecifics, asserting dominance in the area or heightening predatory status.

The effect of motorboat sound on Australian snapper Pagrus auratus inside and outside a marine reserve.

Human-generated sound affects hearing, movement, and communication in both aquatic and terrestrial animals, but direct natural underwater behavioral observations are lacking. Baited underwater video (BUV) were deployed in near shore waters adjacent to Goat Island in the Cape Rodney-Okakari Point Marine Reserve (protected) or outside the reserve approximately four km south in Mathesons Bay (open), New Zealand to determine the natural behavior of Australian snapper Pagrus auratus exposed to motorboat sound. BUVs worked effectively at bringing fish into video range to assess the effects of sound. The snapper inhabiting the protected area showed no behavioral response to motorboat transits; however, fish in the open zones either scattered from the video frame or decreased feeding activity during boat presence. Our study suggests that motorboat sound, a common source of anthropogenic activity in the marine environment can affect fish behavior differently depending on the status of their habitat (protected versus open).

Vessel noise cuts down communication space for vocalizing fish and marine mammals.

Anthropogenic noise across the world's oceans threatens the ability of vocalizing marine species to communicate. Some species vocalize at key life stages or whilst foraging, and disruption to the acoustic habitat at these times could lead to adverse consequences at the population level. To investigate the risk of these impacts, we investigated the effect of vessel noise on the communication space of the Bryde's whale Balaenoptera edeni, an endangered species which vocalizes at low frequencies, and bigeye Pempheris adspersa, a nocturnal fish species which uses contact calls to maintain group cohesion while foraging. By combining long-term acoustic monitoring data with AIS vessel-tracking data and acoustic propagation modelling, the impact of vessel noise on their communication space was determined. Routine vessel passages cut down communication space by up to 61.5% for bigeyes and 87.4% for Bryde's whales. This influence of vessel noise on communication space exceeded natural variability for between 3.9 and 18.9% of the monitoring period. Additionally, during the closest point of approach of a large commercial vessel, <10 km from the listening station, the communication space of both species was reduced by a maximum of 99% compared to the ambient soundscape. These results suggest that vessel noise reduces communication space beyond the evolutionary context of these species and may have chronic effects on these populations. To combat this risk, we propose the application or extension of ship speed restrictions in ecologically significant areas, since our results indicate a reduction in sound source levels for vessels transiting at lower speeds.