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July | August 2012 Noise a source of stress for farmed fish

International Aquafeed is published five times a year by Perendale Publishers Ltd of the United Kingdom. All data is published in good faith, based on information received, and while every care is taken to prevent inaccuracies, the publishers accept no liability for any errors or omissions or for the consequences of action taken on the basis of information published. Copyright 2012 Perendale Publishers Ltd. All rights reserved. No part of this publication may be reproduced in any form or by any means without prior permission of the copyright owner. Printed by Perendale Publishers Ltd. ISSN: 1464-0058

The International magazine for the aquaculture feed industry

FEATURE

a source of stress for farmed fish


By Rogelio Sierra Flores1 2, Andrew Davie1, Tim Atack2 and Herve Migaud1, Institute of Aquaculture, University of Stirling, UK and Ardtoe Marine Laboratory, UK t is widely recognised that fish welfare and stress are inextricably linked. When welfare is compromised and fish are under stressful conditions there are a wide range of negative effects that have been reported. These include a reduction in feed intake, growth, food conversion efficiency and flesh quality; an increase in disease susceptibility and aggression; disruption of the reproductive axis and ultimately, in extreme cases mortality. Research has focused on numerous different potential stressors including environmental factors such as light, temperature and water quality as well as physical stressors like crowding, handling and transportation. However, the potential for sound to act as a stressor has been largely overlooked in aquaculture.

Noise

involves a series of complex terms but essentially sound is energy traveling as a mechanical wave caused by changes in the medium pressure. Detection of those variations is known as the audible sound and its loudness depends on the specific sensitivity to the frequencies. The colloquial term sound volume often confounds the definitions of sound pressure and sound intensity: sound intensity is the rate of flow of energy through an area (W/m), while sound pressure is the strength of the sound wave (Pa). Sound pressure levels (SPL) are the logarithmic expression in the relative scale decibel (dB) of the root mean square (RMS) compared to a reference value. Thus, to quantify anthropogenic sounds in the culture environment, we use the SPL of a given noise over the background reference.

or tissues and specialised cells distributed throughout the animal body, giving the fish the ability to sense and discriminate sounds based on their direction, distance and source. Fish auditory thresholds are believed to be primarily in the range of 20 to 3,000 Hz. However sensitivity does clearly vary with species (Figure 1) and stage of development. Reports have indicated that some fish species could even detect very low frequencies in the infrasound range (<20 Hz) as well as possibly in the ultrasound range (>20 kHz) although this may depend on sound levels fish are exposed to. Whether fish perception of these sound frequencies is functional hearing or an artefact of past auditory requirements needs further clarification.

Fish do not only passively perceive sounds generated in their environment, they can also be vocally active as shown in many Sound plays an important role in the life species. The swim bladder has an audiof terrestrial and aquatic animals as a means tory accessory function reflecting sound and of communication as well as its role in echoamplifying their communications. Some fish location, predator avoidance, or even just the also use this sound box to generate vocaliperception of changes in the environment. sations for a variety of potential reasons As such it deserves greater attention than including maintenance of contact, warning it has received so far as a parameter to be of predators, aggression or mate choice. monitored/managed in culture settings. Atlantic cod (Gadus morhua) is a particularly It must be acknowledged that air and water vocal species which produces sounds during are two completely different acoustic environaggression, chasing, escaping ments. With water being a but mainly during courtship. thousand times denser than Cod vocalisations are air, a greater energy input named grunts and clicks is required to initiate sound based on the human perceppropagation which results tion of the sound. The grunts in sound underwater havare produced by repeatedly ing a greater velocity with contracting the drum muscle less attenuation. In practical sending vibrations to the swim terms this means that greatbladder. One grunt is a repetier energy is required to cast tion of single pulses of 60 to a noise underwater although 200 ms in frequencies ranging water is less restrictive to a from 30 to 250 Hz (Figure 2). spreading sound wave, and Figure 1: Hearing thresholds comparison of humans, dogs, bats It is believed that during thus aquatic fields can be and fish. Hearing thresholds for five selected fish species (Atlantic cod, Atlantic salmon, Common carp, Tunids, and goldfish) courtship females will assess very noisy environments. Adapted from Popper et al., 2008 the fitness of the males based The concept of sound

The importance of sound

Sound perception

Grunts and clicks

Aquatic animals are provided with a wide range of sensory organs and systems to perceive and filter relevant environmental signals. The capability of fish to cast and recognise sound is well documented for some species, showing significant variability among them. In general, sound perception in fish is localised to three interconnected systems: the auditory, the equilibrium and the lateral line. They involve a series of complex organs

28 | InternAtIonAl AquAFeed | July-August 2012

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FEATURE EXPERT TPIC In captivity sound sources are more spe- tank walls all create obvious perceptible on their grunting. As such, male grunting project included four tilapia farms in China. These identify the key problems and causes related to in April, 2011. Over 40 farmers, processors, techvigour has been related to the volume of the cific, being related to the general operation noise (Figure 3). Some basic activities farms represented both small- and commercial- water management. like hand feeding officers a low the drum muscle mass as well as the individuals of an aquaculture facility including equipment nicians and government showed attended sound The second husbandry assessment of the scale production facilities utilising two different level increase of 8-11 dB re Pa very specific immune condition. During mating the and general project is an activities. Literature workshop. Participants found the workshop above production systems (pond and cages). Aside from regional environmental impacts of fish farm clusters, informative and helpful. This enhanced the producfemale will settle on the ground, while males suggests that general activity and farm noise background noise. identifying similarities and differences among criteria which will be jointly conducted by SFP and Hainan ers awareness of increasing demands for certified However, the analysis showed that other perform a courtship characterised by both will generate low frequency vibrations i.e. and requirements used by the three standards, Research Academy of Environmental Sciences, the sustainable seafood from reach worrying thus vocalisations and a swimming pattern around <1kHz which is within the auditory sensi- daily activities can overseas markets, levels. this project also identified outstanding issues in the leading environmental research institute in Hainan. further facilitating the engagement of Chinese tivity of fish. Thus, the female. farms, which most producers were able to address The study will examine the potential for regional stakeholders into a supply-chain dialogue around In enclosed aquaculture systems it is very prior to quantifying as a result of the trial audit. To date, all four farms scale improvement by looking at carrying capacity sustainability. likely that mating performance/mate choice how sound could SFP is currently working with local institutes of are now certified under one or more of the com- and the potential for zoning in a specific area. could be impaired if the males singing and act as a stressor, As more first-hand mercial aquaculture standards. somehow restrained it was felt impor- data becomes available aquaculture and environmental sciences to identify dancing performance is SFP is widely acknowledged for its expertise tant to a more in-depth understanding of and evaluate both qualitatively and quantitatively by the physical conditions. While every effort (along with more preby has been directed to optimising broodstock existing policies and management measures), the the environmental impacts of tilapia farming in stakeholders in Chinese tilapia, including key cisely catalogue the US and European buyers and retailers, as well as AIP will establish a working group that convenes Hainan. This includes an ecological study as well as holding tanks to ensure enough space and sound-scape in a producers and processors in China, aquaculture the key buyers, suppliers and producers along the socio-political analysis to advise local governments low turbulences to allow paired mating, little typical land-based institutes, industry associations, and local Chinese Chinese tilapia supply-chain to share the scientific and industrial associations about how to efficiently thought has been put into the acoustic condi- aquaculture facility. governments. Given the high level of trust that SFP findings. The AIP will then form a multi-stakeholder address the environmental issues associated with A sound maptions experienced by fish in culture. enjoys with the tilapia supply chain it was appropri- policy roundtable to further discuss the problems tilapia farming in Hainan. The preliminary results will ping exercise ate that a tilapia Aquaculture Improvement Project and solutions. The AIP participants will eventually be shared with key stakeholders at the Aquaculture was performed Negative effects of sound Figure 2. Waveform and spectrogram of four different (AIP) was officially launched in 2011. anthropogenic agree on the actions and timetables necessary to Policy Roundtable this fall in China. in the facilities of The negative effects of cod grunts recorded in SFP facilities of Ardtoe Marine the is also developing partnerships with SFP has now initiated two research projects Ardtoe Marine sound are well documented in the natural achieve the sustainability objectives defined by Laboratory, Scotland during Spring 2010. to environment where a wide farming on the the group. SFP will play a leading role in engaging Chinese universities and large feed manufacturers assess the impact of tilapia range of species Laboratory in external environment. The first project, started stakeholders, providing scientific advice and facilitat- to improve feed sourcing for tilapia farming in have been shown to alter their natural com- Scotland which in April 2011, involves monitoring water qual- ing communication. Accidental and/or intentional knocks against a munication and behaviour with there even revealed a surprisingly quiet background China. This work is to be undertaken through ity on selected farms in Hainan province, and in sound level in the rearing tanks as com- research projects on improving feeding efficientank wall, which can cause strong behavioural being evidence of panic and confusion and developing alternative feeds with fewer was undertaken different Hainan Institute of Up-to-date progress response to by the anthropogenic sound pared to what would be expected in cy reactions in the fish stocks, generates low Aquaculture. Dozens of water quality paramSFP has worked closely with local tilapia associafrequency sounds with volumes ranging from stimuli. In the natural marine environment shallow coastal waters. That said, sound impacts on wild fisheries. eters such as chemical oxygen demand (COD), tions to assess different tilapia standards that are these sound sources are diverse and include disturbances were evident. Common hus- 21-39 dB depending on the vigour/cause of nitrogen and phosphorus content, and heavy available in activities like workshop introducing More InforMatIon: Such SPL are clearly peroffshore engineering, pile driving, seismic sur- bandry the market. A hand feeding, walk- the perturbation. metals were analysed for five farms over two three international standards for tilapia farming, i.e. Sustainable Fisheries Partnership veying, busy shipping areas as well as naval ing, hand netting, talking, water inflow, ceived by the fish and could possibly trigger a croppings (10 months). The study helped 20/02/2012 bubbles, and knocks in Haikou Website: www.sustainablefish.org _OffshoreMaric_Quarter_SplitAd_OMC_Quarter BAP, GlobalGAP, and ASC, was held against the stress reaction. aeration 07:53 Page 1 activity.

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July-August 2012 | InternAtIonAl AquAFeed | 29 July-August 2012 | InternAtIonAl AquAFeed | 27

FEATURE

Fish reaction
Stress reactions in fish in response to sound perturbations can be behavioural, acoustic and/or physiological. Behavioural responses are the apparent avoidance or freezing reaction. Acoustic responses are more difficult to

ly correlated to peak cortisol concentrations. Tested sound levels were comparable to those encountered during the site sound mapping, which suggests that a perturbation as simple as knocking a tank wall can be strong enough to trigger a significant increase of cortisol.

of elevated cortisol to the oocytes reducing their viability. Another possibility is that the courtship ritual could have been disrupted by the randomised sound exposure masking the grunts and interrupting the mating behaviour explaining the reduction in fertilisation rate. Regardless of the causative mechanism, the fact that fertilisation success and egg quality were so clearly affected in sound stressed broodstock should be taken as a clear indication the acoustic conditions in culture deserve more attention.

Implications for other species


While evidence suggests that Atlantic cod is one of the more acoustically sensitive fish we firmly believe that there are implications for this work in most other cultured species. Future work should focus on the long-term effects of noise as a stressor including temporary auditory thresholds adaptation as coping strategies. Acclimatisation to noise might be possible, although negative physiological responses could be present even without a clear behavioural response. In terms of the culture facilities we use, clearly more attention has to be paid in reducing the noise caused around land-based aquaculture facilities and, by doing so, making aquaculture production more reliable and predictable possibly helping to reduce the commonly reported variability in fish performances in most aquaculture facilities. Instituting some routine simple and cheap sound measurements on a farm could mitigate many unnecessary disturbances that might be acting as stressors affecting the welfare and thus performance of the fish. The results of doing so may well be seen in the bottom line.

Figure 3: Noise disturbances monitored in an aquaculture on-growing tank. Waveform and spectrogram representations: A) Background sound level; B) Hand feeding commercial dry pellets of 4.5 mm two times five pellets at the time; C) Knocks against the tank wall. Three sets of three knocks caused with the bare fingers.

characterise, however evidence suggests that fish may attempt to alter their vocalisation form and structure (length, frequencies and amplitude) to increase transmission probability as has been reported in other vertebrates. Finally, the physiological responses are varied as a stress activation of the sympathetic nervous system (SNS) and the hypothalamicpituitary-interrenal (HPI) axis can impact on many processes however evidence of sound stimulating these processes is lacking to date. Buscaino et al. (2009) demonstrated in sea bass and sea bream that sound perturbations above a threshold can result in an increase in blood glucose levels and haematocrit which confirms the involvement of the HPI axis in this species.

Recovery from the sound perturbation was also rapid indicating it to be an acute stress response that fish should be able to cope and adapt to. This would in turn suggest a minor impact in the long-term performance of the fish stocks although, in fish farm facilities, those acute sudden noises are common and frequent. Thus, the second phase of the work considered how short acute sound stressors applied over a long time frame can impact on fish performances.

Sound stressors over time: a significant impact


We discovered that cod broodstock exposed to six hours of daily randomised noise at a SPL of 34 dB re Pa (comparable to a loud knock on a tank wall) significantly impacted on the their spawning performance. Egg production in terms of volume of eggs and egg size was comparable between broodstocks that were both exposed, and not exposed, to sound though in the sound exposed population fertilisation rates were reduced by almost half. Work is currently underway to investigate why sound perturbations result in such a significant reduction in fertilisation success with one possibility being the maternal transfer
30 | InternAtIonAl AquAFeed | July-August 2012

Acknowledgments
This project was co-funded by the Mexican Council for Science and Technology (CONACYT) and EU FP7 project 232305 PROSPAWN.

Acute stress response


Our studies have shown that noise does elicit an acute stress response in Atlantic cod (Gadus morhua) juveniles. Fish exposed to sound in the 100-1000Hz range for 10 minutes, using suspended underwater loudspeakers, showed a significant increase of plasma cortisol concentrations within 10 minutes of exposure. Furthermore, the response was dose dependent as sound pressure levels were direct-

References
Buscaino, G., F. Filiciotto, et al. (2010). "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.)." Marine Environmental Research 69(3): 136142.

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