Acoustic stress responses in juvenile sea bass Dicentrarchus labrax induced by offshore pile driving
Introduction
Anthropogenic sound research has been mostly conducted in the terrestrial environment, although aquatic environments also suffer from noise pollution (Broucek, 2014, Kight and Swaddle, 2011, Slabbekoorn et al., 2010). Marine organisms rely on sound for survival, communication, detection of prey and predators, individual recognition, orientation, navigation, mate selection, shoaling, and even larval settlement (Caltrans, 2009, Clark et al., 2009, Popper et al., 2014, Slabbekoorn and Bouton, 2008, Slabbekoorn et al., 2010, Stanley et al., 2012, Wartzok and Ketten, 1999). During several decades, a variety of anthropogenic sounds have been introduced into the marine environment. Sound is generated from shipping, seismic surveys, sonar equipment, underwater explosions and offshore construction. In addition to these anthropogenic noises, sound is naturally present in the ambient marine environment and marine animals also produce sounds. This mixture of biotic and abiotic noise creates a highly complex acoustic environment (De Jong et al., 2011) that affects marine organisms in different ways (Popper and Hastings, 2009b). Underwater noise travels faster and further from the sound source compared to air-borne sound, and the frequency of anthropogenic generated underwater sound largely overlaps with the range of biologically relevant sounds (Hastings and Popper, 2005, Slabbekoorn et al., 2010). This combination makes artificial sound a potential threat to marine life. Human-generated underwater sound has been classified as a pollutant worldwide and must be therefore be monitored. Within the EU Marine Strategy Framework Directive (MSFD) (2010/477/EU European Commission Decision), two indicators have been proposed, i.e. impulsive and ambient (continuous) noise. Empirical data to assign thresholds are lacking, however (Van der Graaf et al., 2012).
To meet renewable energy targets, the number of constructed and planned offshore wind farms (OWFs) is rapidly increasing in the North Sea, with pile driving as the most commonly used method to anchor the piles. This activity is characterized by high-intensity impulsive sounds, with sound pressure levels (from zero to peak, SPLz–p) up to 210 dB re 1 μPa (e.g. Debusschere et al., 2014). Although OWFs are being constructed all over the North Sea, quantitative data on the impact of pile driving on fish are largely lacking. Recently, a number of acoustically controlled chamber experiments have been carried out, mainly focusing on mortality and injuries (Bolle et al., 2012, Casper et al., 2013a, Casper et al., 2012, Halvorsen et al., 2012a, Halvorsen et al., 2012b). These studies found that after exposure to pile driving sound levels, fish without a swim bladder (e.g. flatfish) are not susceptible to barotrauma injuries. In contrast, injuries were quite often noticed and were more severe in physoclistous fish (closed swim bladder) compared to physostomous fish (open swim bladder), with most of the injuries noted in tissues close to the swim bladder. These studies also revealed that most injuries did not lead to mortality under optimal lab conditions. Mortal injuries in round fish were observed, but only after exposure to sound level thresholds above 180–187 dB re 1 μPa2 s for SELss (single strike sound exposure level) and 210–220 dB re 1 μPa2 s for SELcum (cumulative sound exposure level).
The behavioural responses in fish related to acoustic stress induced by pile driving have received much less attention than physical injury or mortality (Barton, 2002, Popper and Hastings, 2009a). Pile driving noise can be categorized as a ‘type 1’ stressor: it leads to spatially localised stress that is detectable in individual organisms (Shuter, 1990). To re-establish homeostasis after being exposed to a stressor, three main compensatory physiological stress responses are of importance in fish (Wedemeyer et al., 1990). The primary response is a combination of stimulating the sympathetic nervous system, a release of catecholamines and activation of the hypothalamic-pituitary-interrenal axis, which incites the release of steroid glucocorticoid hormones such as cortisol (Barton, 2002, Schulte, 2014). The corticosteroids and catecholamines mediate a secondary response, covering an adjustment of the physiological metabolism (glucose, lactate, adenylate energy charge), haematological and immune features, and changes in respiration (Iwama, 1998, Pickering, 1981, Rotllant and Tort, 1997, Simontacchi et al., 2008). The tertiary response is related to whole-animal performance, including growth, condition, behaviour, fecundity, disease resistance and survival (Wedemeyer et al., 1990), and is only observed when the initial responses failed to re-establish homeostasis (Pavlidis et al., 2011).
In Debusschere et al. (2014) the results on mortality in juvenile sea bass Dicentrarchus labrax after exposure to pile driving sounds were presented based on a number of in situ experiments. To date, no other offshore in situ experiments have been published, mainly because of the logistical challenges related to conducting experiments that combine fish and sound near OWF construction sites. The aim of the current study was to determine whether pile driving is perceived as an acoustic stressor in fish, more specifically in young sea bass, based on the same four in situ field experiments. The primary response level was determined by the biochemical parameter whole-body cortisol; the secondary response level by respiration (oxygen consumption rate) and whole-body lactate; the tertiary response level by growth, weight, condition and skeletal deformation.
Section snippets
Juvenile sea bass
For this experimental study young European sea bass D. labrax were used as model organism. Sea bass is an important fish species, both for commercial fisheries and in aquaculture. It is a euryhaline and eurythermic species, distributed throughout the North Atlantic, Mediterranean and Black Sea, and inhabiting several demersal (benthic) habitats down to 100 m (Varsamos et al., 2001). Young sea bass of 45 days post hatching (dph) were collected from the Ecloserie Marine de Gravelines (France) and
Sound pressure
Detailed results on the measured sound pressure parameters during the four in situ experiments have been published in Debusschere et al. (2014). In summary, the ambient background SPL (as measured during the in situ control treatments) ranged from 128 to 145 dB re 1 μPa. The impulsive sound pressure generated during the pile driving activity itself (in situ exposure treatment) was much higher, with SELss ranging from 181 to 188 dB re 1 μPa2 s, SPLz–p of 210 dB re 1 μPa, the number of strikes
Discussion
Debusschere et al. (2014) based on the same in situ experiments, showed that impulsive sound generated by pile driving did not invoke significant increases in immediate or delayed mortality in young sea bass D. labrax. Furthermore, various lab studies have revealed that under optimal conditions strong impulsive sounds may cause fish injuries, but these normally do not lead to mortality (e.g. Bolle et al., 2012, Casper et al., 2013a, Casper et al., 2013b, Halvorsen et al., 2012a, Halvorsen
Conclusions
Although the in situ experiments on the pile driving vessel were logistically demanding, they provide important insights into the acoustic stress response in juvenile fish. Strong and acute secondary stress responses were revealed when young sea bass D. labrax were exposed to impulsive sounds as close as 45 m from a pile driving activity. Especially oxygen consumption rate, and to a lesser extent whole-body lactate proved to be robust parameters. The stress reaction seems to be anxiety related,
Acknowledgements
The authors would like to thank Northwind NV and its contractor GeoSea NV for their collaboration and support during the field experiments. Jyotsna Shrivastava, Naomi Breine, Steven Joosens, Jan Ranson, Karl Van Ginderdeuren, Robin Brabant and Dirk Van Gansbeke are acknowledged for their technical support. Miriam Levenson is to be thanked for proofreading the manuscript. Elisabeth Debusschere is supported by an IWT predoctoral grant (Agency for Innovation by Science and Technology, 111217).
References (74)
- et al.
Behavioral characterization of the alarm reaction and anxiolytic-like effect of acute treatment with fluoxetine in piaucu fish
Physiol. Behav.
(2012) - et al.
Changes in plasma-cortisol during stress and smoltification in Coho Salmon, Oncorhynchus-Kisutch
General Comp. Endocrinol.
(1985) - et al.
Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids
Annu. Rev. Fish Dis.
(1991) The corticotropin-releasing factor system as a mediator of the appetite-suppressing effects of stress in fish
Gen. Comp. Endocrinol.
(2006)- et al.
The hypothalamic-pituitary-interrenal axis and the control of food intake in teleost fish
Comp. Biochem. Physiol. B Biochem. Mol. Biol.
(2001) - et al.
Whole body cortisol and expression of HSP70, IGF-I and MSTN in early development of sea bass subjected to heat shock
Gen. Comp. Endocrinol.
(2011) - et al.
Behavioral measures of anxiety in zebrafish (Danio rerio)
Behav. Brain Res.
(2010) - et al.
Impact of an acoustic stimulus on the motility and blood parameters of European sea bass (Dicentrarchus labrax L.) and gilthead sea bream (Sparus aurata L.)
Mar. Environ. Res.
(2010) - et al.
Effects of exposure to pile driving sounds on fish inner ear tissues
Comp. Biochem. Physiol. A Mol. Integr. Physiol.
(2013) - et al.
Oxygen consumption in sea bass fingerling Dicentrarchus labrax exposed to acute salinity and temperature changes: metabolic basis for maximum stocking density estimations
Aquaculture
(1998)
Understanding behavioral and physiological phenotypes of stress and anxiety in zebrafish
Behav. Brain Res.
The effect of temperature and fish size on growth, feed intake, food conversion efficiency and stomach evacuation rate of Atlantic salmon post-smolts
Aquaculture
The effect of dietary carbohydrate on the stress response in cod (Gadus-Morhua)
Aquaculture
UGCT: new X-ray radiography and tomography facility
Nucl. Instrum. Methods Phys. Res. Sect. A Accel. Spectrom. Detect. Assoc. Equip.
Temporal structure of sound affects behavioural recovery from noise impact in European seabass
Biol. Conserv.
Onset of the primary stress in European sea bass Dicentrarhus labrax, as indicated by whole body cortisol in relation to glucocorticoid receptor during early development
Aquaculture
Growth and stress in fish production
Aquaculture
Rethinking sound detection by fishes
Hear. Res.
Whole-body cortisol is an indicator of crowding stress in adult zebrafish, Danio rerio
Aquaculture
The adrenergic stress response in fish: control of catecholamine storage and release
Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol.
Residency, site fidelity and habitat use of Atlantic cod (Gadus morhua) at an offshore wind farm using acoustic telemetry
Marine Environ. Res.
Differences between rainbow trout and brown trout in the regulation of the pituitary-interrenal axis and physiological performance during confinement
General Comp. Endocrinol.
Biochemical responses of European sea bass (Dicentrarchus labrax L.) to the stress induced by off shore experimental seismic prospecting
Mar. Pollut. Bull.
A noisy spring: the impact of globally rising underwater sound levels on fish
Trends Ecol. Evol.
Software tools for quantification of X-ray microtomography
Nucl. Instrum. Methods Phys. Res. Sect. A Accel. Spectrom. Detect. Assoc. Equip.
Ship noise and cortisol secretion in European freshwater fishes
Biol. Conserv.
Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids
Integr. Comp. Biol.
Effects of chronic cortisol administration and daily acute stress on growth, physiological conditions, and stress responses in juvenile rainbow-trout
Dis. Aquatic Org.
Multiple acute disturbances evoke cumulative physiological stress responses in juvenile Chinook salmon
Trans. Am. Fish. Soc.
Underwater construction and operational noise at alpha ventus
Common sole larvae survive high levels of pile-driving sound in controlled exposure experiments
Plos One
The stress response in fish
Physiol. Rev.
The Acoustic Impedance (pc) of Sea Water Is Presented as a Function of Temperature, Pressure and Salinity
Effect of noise on performance, stress, and behaviour of animals
Slovak J. Anim. Sci.
Differential stress responses in fish from areas of high- and low-predation pressure
J. Comp. Physiol. B Biochem. Syst. Environ. Physiol.
Measuring behavioral and endocrine responses to novelty stress in adult zebrafish
Nat. Protoc.
Final technical guidance for assessment & mitigation of the hydroacoustic effects of pile driving on fish
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