Artificial sound impact could put at risk hermit crabs and their symbiont anemones.

The sea anemone Calliactis parasitica, which is found in the East Atlantic (Portugal to Senegal) and the Mediterranean Sea, forms a symbiotic relationship with the red hermit crab, Dardanus calidus, in which the anemone provides protection from predators such as the octopus while it gains mobility, and possibly food scraps, from the hermit crab. Acoustic pollution is recognised by the scientific community as a growing threat to ocean inhabitants. Recent findings on marine invertebrates showed that exposure to artificial sound had direct behavioural, physiological and ultrastructural consequences. In this study we assess the impact of artificial sound (received level 157 ± 5 dB re 1 µPa2 with peak levels up to 175 dB re 1 µPa2) on the red hermit crab and its symbiotic sea anemone. Scanning electron microscopy analyses revealed lesions in the statocyst of the red hermit crab and in the tentacle sensory epithelia of its anemone when exposed to low-intensity, low-frequency sounds. These ultrastructural changes under situations of acoustic stress in symbiotic partners belonging to different phyla is a new issue that may limit their survival capacity, and a new challenge in assessing the effects of acoustic disturbance in the oceanic ecosystem. Despite the lesions found in the red hermit crab, its righting reflex time was not as strongly affected showing only an increase in the range of righting times. Given that low-frequency sound levels in the ocean are increasing and that reliable bioacoustic data on invertebrates is very scarce, in light of the results of the present study, we argue that anthropogenic sound effects on invertebrates species may have direct consequences in the entire ecosystem.

Towards automated long-term acoustic monitoring of endangered river dolphins: a case study in the Brazilian Amazon floodplains.

Using passive acoustic monitoring (PAM) and convolutional neural networks (CNN), we monitored the movements of the two endangered Amazon River dolphin species, the boto (Inia geoffrensis) and the tucuxi (Sotalia fluviatilis) from main rivers to floodplain habitats (várzea) in the Mamirauá Reserve (Amazonas, Brazil). We detected dolphin presence in four main areas based on the classification of their echolocation clicks. Using the same method, we automatically detected boat passages to estimate a possible interaction between boat and dolphin presence. Performance of the CNN classifier was high with an average precision of 0.95 and 0.92 for echolocation clicks and boats, respectively. Peaks of acoustic activity were detected synchronously at the river entrance and channel, corresponding to dolphins seasonally entering the várzea. Additionally, the river dolphins were regularly detected inside the flooded forest, suggesting a wide dispersion of their populations inside this large area, traditionally understudied and particularly important for boto females and calves. Boats overlapped with dolphin presence 9% of the time. PAM and recent advances in classification methods bring a new insight of the river dolphins' use of várzea habitats, which will contribute to conservation strategies of these species.

Cross-sensory interference assessment after exposure to noise shows different effects in the blue crab olfactory and sound sensing capabilities.

Underwater noise pollution is an increasing threat to marine ecosystems. Marine animals use sound in communication and orientation processes. The introduction of anthropogenic noise in their habitat can interfere with sound production and reception as well as with the acquisition of vital information through other sensory systems. In the blue crab (Callinectes sapidus), the statocyst is responsible for acoustic perception, and it is housed at the base of its first pair of antennae (antennule). The sensilla of the distal part of these antennule hosts the olfactory system, which is key for foraging. Given the anatomical proximity of the two sensory regions, we evaluated the possible interference of sound exposure with the crab ability to find food, by using an aquatic maze, and looked at the potential impairment of the righting reflex as well as at ultrastructural damages in statocysts. Although a significant effect was observed when looking at the time used by the animal to recover its habitual position ("righting reflex"), which was associated to lesions in the statocyst sensory epithelia, the time required to find food did not increase after the exposure to sound. When the crabs were exposed to natural sounds (marine background noise and sounds of their predators: Micropogonias undulates and Sciaenops ocellatus) they did not show significant differences in foraging behaviour. Although we found no unequivocal evidence of a negative impact of sound on olfactory capabilities, the study showed a clear righting reflex impairment correlated with ultrastructural damages of the statocysts. We argue that crab populations that cannot easily avoid noise sources due to their specific coastal distributions may incur in significant direct fitness costs (e.g. impairment of complex reflexes). This integrated approach to sound effect assessment could be used as a model for other invertebrate species to effectively monitor noise impact in marine environments.

Commercial cuttlefish exposed to noise from offshore windmill construction show short-range acoustic trauma.

The installation of marine renewable energy devices (MREDs, wind turbines and converters of wave, tidal and ocean thermal energy) has increased quickly in the last decade. There is a lack of knowledge concerning the effects of MREDs on benthic invertebrates that live in contact with the seabed. The European common cuttlefish (Sepia officinalis) is the most abundant cephalopod in the Northeast Atlantic and one of the three most valuable resources for English Channel fisheries. A project to build an offshore wind farm in the French bay of Saint-Brieuc, near the English Channel, raised concern about the possible acoustic impact on local cuttlefish communities. In this study, consisting of six exposure experiments, three types of noise were considered: 3 levels of pile-driving and 3 levels of drilling. The objectives were to assess possible associated changes in hatching and larva survival, and behavioural and ultrastructural effects on sensory organs of all life stages of S. officinalis populations. After exposure, damage was observed in the statocyst sensory epithelia (hair cell extrusion) in adults compared to controls, and no anti-predator reaction was observed. The exposed larvae showed a decreased survival rate with an increasing received sound level when they were exposed to maximum pile-driving and drilling sound levels (170 dB re 1 µPa2 and 167 dB re 1 µPa2, respectively). However, sound pressure levels's lower than 163 dB re 1 µPa2 were not found to elicit severe damage. Simulating a scenario of immobile organisms, eggs were exposed to a combination of both pile driving and drilling as they would be exposed to all operations without a chance to escape. In this scenario a decrease of hatching success was observed with increasing received sound levels.

Seagrass Posidonia is impaired by human-generated noise.

The last hundred years have seen the introduction of many sources of artificial noise in the sea environment which have shown to negatively affect marine organisms. Little attention has been devoted to how much this noise could affect sessile organisms. Here, we report morphological and ultrastructural changes in seagrass, after exposure to sounds in a controlled environment. These results are new to aquatic plants pathology. Low-frequency sounds produced alterations in Posidonia oceanica root and rhizome statocysts, which sense gravity and process sound vibration. Nutritional processes of the plant were affected as well: we observed a decrease in the number of rhizome starch grains, which have a vital role in energy storage, as well as a degradation in the specific fungal symbionts of P. oceanica roots. This sensitivity to artificial sounds revealed how sound can potentially affect the health status of P. oceanica. Moreover, these findings address the question of how much the increase of ocean noise pollution may contribute in the future to the depletion of seagrass populations and to biodiversity loss.

Morphological Evidence for the Sensitivity of the Ear Canal of Odontocetes as shown by Immunohistochemistry and Transmission Electron Microscopy.

The function of the external ear canal in cetaceans is still under debate and its morphology is largely unknown. Immunohistochemical (IHC) analyses using antibodies specific for nervous tissue (anti-S100, anti-NSE, anti-NF, and anti-PGP 9.5), together with transmission electron microscopy (TEM) and various histological techniques, were carried out to investigate the peripheral nervous system of the ear canals of several species of toothed whales and terrestrial Cetartiodactyla. This study highlights the innervation of the ear canal with the presence of lamellar corpuscles over its entire course, and their absence in all studied terrestrial mammals. Each corpuscle consisted of a central axon, surrounded by lamellae of Schwann receptor cells, surrounded by a thin cellular layer, as shown by IHC and TEM. These findings indicate that the corpuscles are mechanoreceptors that resemble the inner core of Pacinian corpuscles without capsule or outer core, and were labelled as simple lamellar corpuscles. They form part of a sensory system that may represent a unique phylogenetic feature of cetaceans, and an evolutionary adaptation to life in the marine environment. Although the exact function of the ear canal is not fully clear, we provide essential knowledge and a preliminary hypothetical deviation on its function as a unique sensory organ.

Marine mammal acoustic detections in the Greenland and Barents Sea, 2013 - 2014 seasons.

While the Greenland and Barents Seas are known habitats for several cetacean and pinniped species there is a lack of long-term monitoring data in this rapidly changing environment. Moreover, little is known of the ambient soundscapes, and increasing off-shore anthropogenic activities can influence the ecosystem and marine life. Baseline acoustic data is needed to better assess current and future soundscape and ecosystem conditions. The analysis of a year of continuous data from three passive acoustic monitoring devices revealed species-dependent seasonal and spatial variation of a large variety of marine mammals in the Greenland and Barents Seas. Sampling rates were 39 and 78 kHz in the respective locations, and all systems were operational at a duty cycle of 2 min on, 30 min off. The research presents a description of cetacean and pinniped acoustic detections along with a variety of unknown low-frequency tonal sounds, and ambient sound level measurements that fall within the scope of the European Marine Strategy Framework (MSFD). The presented data shows the importance of monitoring Arctic underwater biodiversity for assessing the ecological changes under the scope of climate change.

A critical period of susceptibility to sound in the sensory cells of cephalopod hatchlings.

The cephalopod statocyst and lateral line systems are sensory organs involved in orientation and balance. Lateral lines allow cephalopods to detect particle motion and are used for locating prey or predators in low light conditions. Here, we show the first analysis of damaged sensory epithelia in three species of cephalopod hatchlings (Sepia officinalis, Loligo vulgaris and Illex coindetii) after sound exposure. Our results indicate lesions in the statocyst sensory epithelia, similar to what was found in adult specimens. The novelty is that the severity of the lesions advanced more rapidly in hatchlings than in adult animals; i.e. the degree of lesions seen in hatchlings immediately after noise exposure would develop within 48 h in adults. This feature suggests a critical period of increased sensitivity to acoustic trauma in those species as has been described in developing mammalian cochlea and avian basilar papilla. The hair cells in the lateral lines of S. officinalis followed the same pattern of damage occurrence, while those of L. vulgaris and I. coindetii displayed a decreasing severity of damage after 24 h. These differences could be due to dissimilarities in size and life stages between the three species.

Offshore exposure experiments on cuttlefish indicate received sound pressure and particle motion levels associated with acoustic trauma.

Recent findings on cephalopods in laboratory conditions showed that exposure to artificial noise had a direct consequence on the statocyst, sensory organs, which are responsible for their equilibrium and movements in the water column. The question remained about the contribution of the consequent near-field particle motion influence from the tank walls, to the triggering of the trauma. Offshore noise controlled exposure experiments (CEE) on common cuttlefish (Sepia officinalis), were conducted at three different depths and distances from the source and particle motion and sound pressure measurements were performed at each location. Scanning electron microscopy (SEM) revealed injuries in statocysts, which severity was quantified and found to be proportional to the distance to the transducer. These findings are the first evidence of cephalopods sensitivity to anthropogenic noise sources in their natural habitat. From the measured received power spectrum of the sweep, it was possible to determine that the animals were exposed at levels ranging from 139 to 142 dB re 1 µPa2 and from 139 to 141 dB re 1 µPa2, at 1/3 octave bands centred at 315 Hz and 400 Hz, respectively. These results could therefore be considered a coherent threshold estimation of noise levels that can trigger acoustic trauma in cephalopods.

Evidence of Cnidarians sensitivity to sound after exposure to low frequency underwater sources.

Jellyfishes represent a group of species that play an important role in oceans, particularly as a food source for different taxa and as a predator of fish larvae and planktonic prey. The massive introduction of artificial sound sources in the oceans has become a concern to science and society. While we are only beginning to understand that non-hearing specialists like cephalopods can be affected by anthropogenic noises and regulation is underway to measure European water noise levels, we still don't know yet if the impact of sound may be extended to other lower level taxa of the food web. Here we exposed two species of Mediterranean Scyphozoan medusa, Cotylorhiza tuberculata and Rhizostoma pulmo to a sweep of low frequency sounds. Scanning electron microscopy (SEM) revealed injuries in the statocyst sensory epithelium of both species after exposure to sound, that are consistent with the manifestation of a massive acoustic trauma observed in other species. The presence of acoustic trauma in marine species that are not hearing specialists, like medusa, shows the magnitude of the problem of noise pollution and the complexity of the task to determine threshold values that would help building up regulation to prevent permanent damage of the ecosystems.

Contribution to the Understanding of Particle Motion Perception in Marine Invertebrates.

Marine invertebrates potentially represent a group of species whose ecology may be influenced by artificial noise. Exposure to anthropogenic sound sources could have a direct consequence on the functionality and sensitivity of their sensory organs, the statocysts, which are responsible for their equilibrium and movements in the water column. The availability of novel laser Doppler vibrometer techniques has recently opened the possibility of measuring whole body (distance, velocity, and acceleration) vibration as a direct stimulus eliciting statocyst response, offering the scientific community a new level of understanding of the marine invertebrate hearing mechanism.

The Use of Deep Water Berths and the Effect of Noise on Bottlenose Dolphins in the Shannon Estuary cSAC.

The Shannon Estuary on the west coast of Ireland is one of Europe's premier deepwater berths catering for ships up to 200,000 deadweight tonnage. It is also Ireland's only designated candidate special area of conservation for bottlenose dolphins under the EU Habitats Directive. Long-term static acoustic monitoring was carried out at a number of intensive shipping sites. In 2012, noise monitoring took place over a 6-month period (at 1 site) as part of Ireland's requirements under the Marine Strategy Framework Directive (MSFD). This is the first assessment of the potential effect of vessel traffic on the behavior of this discrete dolphin population.

Extraction of pulse repetition intervals from sperm whale click trains for ocean acoustic data mining.

The analysis of acoustic data from the ocean is a valuable tool to study free ranging cetaceans and anthropogenic noise. Due to the typically large volume of acquired data, there is a demand for automated analysis techniques. Many cetaceans produce acoustic pulses (echolocation clicks) with a pulse repetition interval (PRI) remaining nearly constant over several pulses. Analyzing these pulse trains is challenging because they are often interleaved. This article presents an algorithm that estimates a pulse's PRI with respect to neighboring pulses. It includes a deinterleaving step that operates via a spectral dissimilarity metric. The sperm whale (SW) produces trains with PRIs between 0.5 and 2 s. As a validation, the algorithm was used for the PRI-based identification of SW click trains with data from the NEMO-ONDE observatory that contained other pulsed sounds, mainly from ship propellers. Separation of files containing SW clicks with a medium and high signal to noise ratio from files containing other pulsed sounds gave an area under the receiver operating characteristic curve value of 0.96. This study demonstrates that PRI can be used for the automated identification of SW clicks and that deinterleaving via spectral dissimilarity contributes to algorithm performance.