Changes in the acoustic environment alter the foraging and sheltering behaviour of the cichlid Amititlania nigrofasciata

Behavioural Processes 116 (2015) 75–79

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Changes in the acoustic environment alter the foraging and sheltering behaviour of the cichlid Amititlania nigrofasciata Kirsty Elizabeth McLaughlin, Hansjoerg P. Kunc ∗ Queen’s University Belfast, Institute for Global Food Security, School of Biological Sciences, Medical Biology Centre, 97 Lisburn Road, Belfast BT9 7BL, UK

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Article history: Received 31 January 2015 Received in revised form 17 April 2015 Accepted 25 April 2015 Available online 29 April 2015 Keywords: Behaviour Environmental stressor Fish Noise pollution Underwater

a b s t r a c t Anthropogenic noise can affect behaviour across a wide range of species in both terrestrial and aquatic environments. However, behaviours might not be affected in isolation. Therefore, a more holistic approach investigating how environmental stressors, such as noise pollution, affect different behaviours in concert is necessary. Using tank-based noise exposure experiments, we tested how changes in the acoustic environment affect the behaviour of the cichlid Amatitlania nigrofasciata. We found that exposure to anthropogenic noise affected a couple of behaviours: an increase in sheltering was accompanied by a decrease in foraging. Our results highlight the multiple negative effects of an environmental stressor on an individual’s behaviour. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Many species are currently experiencing environmental changes caused by humans. Among these is a change in the acoustic environment, through an increase in anthropogenic noise (Hildebrand, 2009; Slabbekoorn et al., 2010). The resulting noise pollution is caused by human activities, such as those involved in the transport and energy sectors (Barber et al., 2010). Consequently, anthropogenic noise has become omnipresent in both terrestrial and aquatic environments, and is considered a major environmental stressor and a significant global pollutant (Wright et al., 2007; European Union, 2008). The effects of anthropogenic noise in terrestrial and aquatic environments can be seen on both the ecosystem and the individual level. On the ecosystem level, noise can affect biodiversity by changing species composition and predator-prey interactions (Bayne et al., 2008; Francis et al., 2009). Whereas on the individual level, noise can affect a variety of different behaviours (Popper, 2003; Brumm and Slabbekoorn, 2005; Tyack, 2008; Barber et al., 2010; Kight and Swaddle, 2011; Radford et al. 2014). Understanding behavioural changes in response to novel environmental stressors is crucial, since the initial responses of individuals to anthropogenic changes are often behavioural

∗ Corresponding author. Tel.: +44 28 9097 2104. E-mail addresses: [email protected] (K.E. McLaughlin), [email protected] (H.P. Kunc). http://dx.doi.org/10.1016/j.beproc.2015.04.012 0376-6357/© 2015 Elsevier B.V. All rights reserved.

(Tuomainen and Candolin, 2011). Environmental stressors can affect a single behaviour in isolation, but may also affect behaviours in concert (McEwen and Wingfield, 2003; Wingfield, 2005). For example, if common behavioural responses to stressors are correlated, such as sheltering and an individuals’ activity (Metcalfe et al., 1987) an increase in one behaviour may decrease the other. Changes in either of these behaviours may also negatively affect foraging and as a consequence energy intake (Kight and Swaddle, 2011; Marentette and Balshine, 2012; Purser and Radford, 2011). Therefore, examination of such potential behavioural cascades in response to anthropogenic noise is important. Convict cichlids (Amatitlania nigrofasciata) are a highly territorial freshwater fish native to Central and South America, where they occupy rocky habitats within streams, rivers and lakes (Conkel, 1993). Like many other fish species, convict cichlids shelter to avoid environmental stressors (Ferrari et al., 2010; Holmes and McCormick, 2010). Whilst occupying confined systems, e.g. lakes, individuals are unable to escape anthropogenic noise by large scale avoidance behaviour, making other behavioural changes, e.g. alteration to foraging rate, more biologically relevant. Convict cichlids are used extensively in behavioural studies, as their behaviour in captivity is comparable to that in the wild (Gagliardi-Seeley and Itzkowitz, 2009). Thus, convict cichlids are a good model system for understanding how changes in the acoustic environment might affect fitness enhancing behaviours. Tank-based experiments examining the impact of environmental stressors on behaviour are a valuable and commonly used first step, as they allow for tightly controlled experimental conditions

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(Munday et al., 2009; Dixson et al., 2010; Simpson et al., 2011; Bruintjes and Radford, 2014). However, the ability to control for confounding factors must be traded off against the experimental set-up not fully mimicking real-world circumstances (Simpson et al., 2014). Using tank-based experiments, we assessed the impact of a changing acoustic environment on a couple behaviours of fish. We predicted that if noise affects behaviour, fish exposed to increased noise will increase sheltering and decrease their activity, leading to a decrease in foraging.

2. Materials and methods 2.1. Study species and husbandry Convict cichlids were sourced from a local supplier (Carrick Pet Stores, Carrickfergus, Northern Ireland) and fed once daily with Higrow (JMC) granules. Fish were housed in 90-l stock tanks in same sex groups for a seven day acclimation period at a stocking density of no greater than thirteen per tank (c.f. Arnott and Elwood, 2009). Stock tanks contained 2 cm gravel substrate, plastic plants and 9 cm diameter terracotta flower pots, a water heater, biological and chemical filtration and aeration. Fish were maintained on a 13:11 light: dark cycle and water temperature was 25 ± 1 ◦ C.

2.2. Noise stimuli For the noise exposure, we used playbacks of ferry noise (MV Portaferry II, 312 GT) because ship noise is the most common source of underwater noise pollution (Vasconcelos et al., 2007). Stimuli were recorded using a calibrated hydrophone with a preamplifier (HTI-96-MIN; manufacturers calibrated sensitivity −165 dB re 1 v/␮Pa; frequency range 2 Hz–30 kHz) connected to a Marantz PMD660 recorder (44.1 kHz sampling rate; 0.3 Vrms input sensitivity). Stimuli were recorded on different days with the hydrophone being placed and remaining 1 m from the ferry for the entirety of all recordings, (c.f. Kunc et al., 2014). All noise recordings were analysed in Avisoft-SASLab Pro software version 5.1.17 (Avisoft Bioacoustics, Berlin, Germany). All sound pressure levels (SPL) are expressed as root mean squared (RMS (5 s)) values, which allows a good representation of a complex noise source consisting of many frequencies (Davidson et al., 2007). Acoustic analysis was carried out in the 0–4 kHz frequency range. To generate the noise treatment (mean SPL RMS (5 s) 170 dB re 1 ␮Pa), the SPL of the stimuli was adjusted in Avisoft (SASLAB Pro). The control period consisted of ambient tank conditions (mean SPL RMS (5 s) 129 dB re 1 ␮Pa). A mean SPL RMS for the original ship recording (mean SPL RMS (5 s) 176 dB re 1 ␮Pa) was also generated to compare the original recording with the treatment (see Fig. 1). Mean SPL RMS for the noise treatment, ambient control conditions and the original ship recording were attained from 5 s segments of 20 separate tank and ship recordings. Underwater sound waves consist of two components: particle motion and sound pressure, both of which can provide individuals with information (Radford et al., 2012). Most fish species are able to detect particle motion of an acoustic wave and some species are able to detect the pressure component as well (Popper and Fay, 2011). The hearing capabilities of our study species, convict cichlids, have not yet been defined. However, the cichlid family contains species whose hearing is mainly based on particle motion and species whose hearing is mainly based on sound pressure (Ladich and Schulz-Mirbach, 2013; Yan and Popper, 1992). The noise stimuli experienced by the fish will differ from the original ferry recording as tank-based acoustics are complex and occur within the near-field. Thus, the relationship between sound pressure and particle motion will be different than with the original

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Power spectral density (dB re 1µPa2 Hz-1)

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Frequeny (Hz) Fig. 1. Averaged power spectral density (dB re 1 ␮Pa2 Hz−1 ) generated using Fast Fourier Transform (FFT) analysis of 5 s segments from 20 separate recordings of each noise type (original ship, noise treatment and control period) (FFT size 32,768; Hann evaluation window; bandwidth 2 Hz; resolution 1.4 Hz; frequency range analysed 0–4 kHz) (control: bottom line dark grey, noise: 2nd line mid grey, original ship: top line black, stock tank: 3rd line light grey).

sound source (Akamatsu et al., 2002). Therefore the noise stimuli used in this study shall be referred to as noise, not ship-noise. To characterise the noise fish were experiencing, sound recordings of the control period and the noise treatment were made from the middle of the experimental tanks. Using Avisoft (SASLAB Pro), power spectral densities from 20 separate recordings for each treatment and the original ship noise were generated using Fast Fourier Transform analysis (FFT size 32,768; Hann evaluation window; bandwidth 2 Hz, resolution 1.37 Hz) of 5 s segments. To illustrate frequency and SPL over time a spectrogram and oscillogram of the noise stimuli were generated (Figs. A1 and A2). All recordings were made using the same equipment as described above. We acknowledge that the exact SPL RMS received by fish changes throughout the tank. However, the aim of our study was to test whether behaviour differs in relation to increased noise. 2.3. Experimental procedure For the playback experiments, each fish was placed into a 28-l glass tank (45 × 24.5 × 25.5 cm with 5 mm thick walls), with 2 cm gravel, air driven filter, heater and a 9 cm diameter terracotta flower pot. Fish were given 24 h to acclimate to the tank and were not fed during this period to control for differing levels of hunger prior to the experiment. Five experimental tanks were set-up to run simultaneously, and each experimental tank was placed on an individual 2 cm thick polystyrene slab, 61 cm apart on top of a wooden bench. Noise transfer during noise playback from one tank to another was 3 dB RMS (averaged from 5 s segments of 10 separate recordings). After the 24 h acclimation period, an underwater speaker (AQ SUBAQUA 30) connected to an amplifier (Denon Professional integrated amplifier DN-A100) and a CD player (Sony BDP-S1100) was placed in each tank, behind an opaque divider and the air driven filter was switched off. The speaker compartment measured 15 × 24.5 cm and the experimental arena measured 30 × 24.5 cm. Prior to the beginning of the experiment a food source (3 × 3 cm block of Tetra goldfish holiday food) was fixed on the bottom of each tank 30 cm from the speaker and a video camera (Canon Legria FS306, Canon, Japan) was positioned in front of each tank. No fish consumed all the food during the experiment. After the food source and speaker

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a 1.0

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were added to the tank and the camera was switched on fish were given 40 min to recover from any disturbance before the experiment began. To avoid any effect of the observer, from this point onwards fish were visually isolated from the experimenter. After the 40 min recover period each fish was exposed to two conditions an ambient control (ambient tank conditions) and a noise treatment. To rule out that the presence of the speaker or the electromagnetic field produced by the speaker had an effect on the behaviour of fish, the speaker was not removed during the control treatment and remained switched-on throughout the entire experiment. Each treatment lasted for 5 min during which the individual was video-taped. There was a 10 min period between the noise and the control treatment, during which time the food source was not removed. Treatment order was randomised and each fish received both treatments. The experiment began regardless of where the fish was positioned within the tank and the tank was cleaned after each fish was removed.

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Fig. 2. Proportion of time fish spent in shelter (a) and count of foraging activity of fish (b) during the control period and noise treatment. Box plots indicate median, 25% and 75% quartiles (box), interquartile ranges (whiskers) and outliers (dots). N = 15.

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2.6. Statistical analysis

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Statistical analysis was carried out in SPSS 17 (SPSS Inc., Chicago, IL, U.S.A.) and R (Development Core Team, 2013). To test whether noise had an overall effect on activity, sheltering and foraging, we used a Wilcoxon test on each behaviour. To test whether differences in behaviour were due to a change in the number of individuals adjusting their behaviour we used a chi-squared test. To test whether behaviours were correlated in both the control and the noise treatment we used a Spearman rank correlations.

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2.5. Ethical note All work was carried out under a UK Home Office License (PPL2742), and adhered to the ASAB/ABS guidelines. To reduce aggression in stock tanks fish were provided with environmental enrichment (Barley and Coleman, 2010). During the experiments, fish were socially isolated for a minimal time to limit isolation stress (Pottinger and Pickering, 1992). We designed the experiment in accordance with the reduction principle of the 3Rs (HMSO, 1986).

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To avoid observer bias, video recordings were assigned a code and analysed without sound so that the observer (KEMcL) was unaware of which treatment was being analysed. Using JWatcher version 1.0 event recording software (Blumstein and Daniel, 2007), we analysed the following behaviours for each individual: (i) the proportion of time sheltering; defined as half a body length inside the flower pot, (ii) the proportion of time moving, as a measure of activity; defined as a vertical or horizontal movement of a full body length, and (iii) foraging activity; defined as the number of pecks at the substrate, or food (Bracciali et al., 2012). Our initial plan was to expose 32 fish to noise. However, 17 fish spent the entire control period inside their shelter and thus the data from these fish were excluded from further analysis (N = 15). Following the principle of the 3Rs we abstained from using more individuals (see Section 2.5).

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The presence of noise elicited behavioural changes: fish increased the time they spent sheltering (Wilcoxon test: Z = −2.32, p = 0.019; Fig. 2a), decreased their foraging (Wilcoxon test: Z = −2.31, p = 0.02; Fig. 2b), but did not alter their activity (Wilcoxon test: Z = −0.52, p = 0.6). The noise-induced decrease in foraging was due to a decrease in the number of individuals that foraged (chisquared test: 2 1 = 3.96, p = 0.046; Fig. 3), but the noise-induced increase in sheltering was not (chi-squared test: 2 1 = 45, p > 0.9;

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Fig. 3. Number of individuals sheltering (white bars) and foraging (black bars) during the control period and noise treatment.

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Fig. 3). Sheltering and foraging were negatively correlated (control treatment Spearman correlation: rs = −0.593, df = 15, p = 0.02; noise treatment Spearman correlation: rs = −0.595, df = 15, p = 0.019).

4. Discussion Through tank-based noise exposure experiments, we show that increased noise can affect the behaviour of the cichlid A. nigrofasciata. Fish exposed to noise increased time spent sheltering and decreased foraging. The number of individuals sheltering did not change with noise exposure. However, when noise was broadcast fewer individuals foraged than during the ambient control. A change in one behaviour may negatively impact other behaviours by diverting available time away from their expression (Lima and Dill, 1990; Kight and Swaddle, 2011; Picciulin et al., 2010). In our study, fish increased time spent sheltering and decreased foraging during noise exposure, suggesting that a change in one behaviour can result in a behavioural cascade. Additional underwater noise has been found to affect foraging behaviour in other fish species and also invertebrates (e.g. Wale et al., 2013; Voellmy et al., 2014; Bracciali et al., 2012). Behavioural responses may also be influenced by the structure of the environment, for example whether individuals can make use of shelters. In a previous study examining the effect of noise on stickleback behaviour, foraging decreased with increasing noise but hiding was not affected (Purser and Radford, 2011); however, designated shelters that allowed individuals to retreat completely were not provided. Sheltering is a common behavioural response to an environmental stressor (Metcalfe et al., 1987). Thus, only when a designated shelter is provided may the full consequences of increasing noise levels on an individual’s behaviour be seen. Our results suggest that the structure of the environment may be crucial, because individuals in our study sheltered more during noise when designated shelters were provided. As sheltering time increased with additional noise fewer individuals foraged, suggesting a switch occurred from foraging to sheltering during the noise exposure. If not compensated for, a cessation of foraging could lead to reduced energy intake (Kight and Swaddle, 2011; Purser and Radford, 2011), ultimately negatively affecting individual survival. Moreover, an increase in the time fish spend sheltering could result in a decrease in the time available for other behaviours such as territory defence and courtship. It remains to be shown whether long-term exposure to noise has the same effects as our short-term noise exposure experiment. The experimental increase in noise created a novel environment. In many species, the behaviour of individuals consistently differs in response to novel environments (Wilson et al., 1994; Gosling, 2001; Dingemanse and de Goede, 2004). Movement of individuals exposed to a novel environment is a measure of exploratory behaviour and correlates with boldness, making movement a component of personality (Verbeek et al., 1994; Sih et al., 2003; Bell, 2005; Brown et al., 2007). Shy individuals have been found to decrease their activity levels in response to novelty, whereas bold individuals increase their activity (Brown et al., 2007). Therefore, personality may have acted as a confounding factor, masking any potential effects of noise on movement. How relevant are our results to assessing the impact of noise on aquatic environments? Our study was conducted within a confined system, i.e. a tank, in which fish were unable to respond to noise with avoidance. However, tank experiments mimic common ecological circumstances faced by many species where individuals cannot avoid noise polluted areas. For example, species that either inhabit confined habitats, defend territories (Bruintjes and Radford, 2013), or which rely upon seasonal, or patchy resources may be among those affected (Eikenaar et al., 2009). These constraints can

hinder avoidance of noise, requiring individuals to adjust their behaviour within their ecological and physical boundaries. The particle motion generated from tank-based playback experiments will not closely mimic real-world situations and the repeated exposure of individuals to increased noise may lead to habituation or even sensitisation (Bejder et al., 2009; Bruintjes and Radford, 2013). However, our results show that changes in the acoustic environment affected a couple behaviours in the convict cichlid. In conclusion, fish adjusted their behaviour in response to a novel environmental stressor. Exposure to noise did not only affect a single behaviour in isolation, because an increase in time spent sheltering was accompanied by a decrease in foraging. Our results show how underwater noise pollution affects a couple behaviours within an individual, highlighting the potential consequences of an environmental stressor on individual fish. Acknowledgements We thank R. Elwood, C. Ijichi, M. Montague and E. Walsh and the reviewers for their helpful comments on an earlier draft; G. Lyons for providing recordings of the stimuli and DARD for funding. Appendix A.

Fig. A1. Frequency content of noise stimuli (15 s segment of noise).

Fig. A2. Amplitude content of noise stimuli (15 s segment of noise).

References Akamatsu, T., Okumura, T., Novarini, N., Yan, H., 2002. Empirical refinements applicable to the recording of fish sounds in small tanks. J. Acoust. Soc. Am. 112, 3073–3082. Arnott, G., Elwood, R., 2009. Probing aggressive motivation in a cichlid fish. Biol. Lett. 5, 762–764. Barber, J.R., Crooks, K.R., Fristrup, K.M., 2010. The costs of chronic noise exposure for terrestrial organisms. Trends Ecol. Evol. 25, 180–189. Barley, A.J., Coleman, R.M., 2010. Habitat structure directly affects aggression in convict cichlids Archocentrus nigrofasciatus. Curr. Zool. 56, 52–56.

K.E. McLaughlin, H.P. Kunc / Behavioural Processes 116 (2015) 75–79 Bayne, E.M., Habib, L., Boutin, S., 2008. Impacts of chronic anthropogenic noise from energy-sector activity on abundance of songbirds in the boreal forest. Conserv. Biol. 22, 1186–1193. Bell, A., 2005. Behavioural differences between individuals and two populations of stickleback (Gasterosteus aculeatus). J. Evol. Biol. 18, 464–473. Bejder, L., Samuels, A., Whitehead, H., Finn, H., Allen, S., 2009. Impact assessment research: use and misuse of habituation: sensitisation and tolerance in describing wildlife responses to anthropogenic stimuli. Mar. Ecol. Prog. Ser. 395, 177–185. Blumstein, D.T., Daniel, J.C., 2007. Quantifying Behaviour the JWatcher Way. Sinauer, Sunderland, MA, USA. Bracciali, C., Campobello, D., Giacoma, C., Sara, G., 2012. Effects of nautical traffic and noise on foraging patterns of mediterranean damselfish (Chromis chromis). PLoS One 7, e40582. Brown, C., Jones, F., Braithwaite, V.A., 2007. Correlation between boldness and body mass in natural populations of the poeciliid Brachyrhaphis episcopi. J. Fish Biol. 71, 1590–1601. Bruintjes, R., Radford, A.N., 2013. Context-dependent impacts of anthropogenic noise on individual and social behaviour in a cooperatively breeding fish. Anim. Behav. 85, 1343–1349. Bruintjes, R., Radford, A.N., 2014. Chronic playback of boat noise does not impact hatching success or post-hatching larval growth and survival in a cichlid fish. PeerJ 2, e594. Brumm, H., Slabbekoorn, H., 2005. Acoustic communication in noise. Adv. Study Behav. 35, 151–209. Conkel, D., 1993. Cichlids of North and Central America. TFH Publications, Neptune city, New Jersey. Davidson, J., Frankel, A.S., Ellison, W.T., Surnmerfelt, S., Popper, A.N., Mazik, P., Bebak, J., 2007. Minimizing noise in fiberglass aquaculture tanks: noise reduction potential of various retrofits. Aquacult. Eng. 37, 125–131. Dingemanse, N., de Goede, P., 2004. The relation between dominance and exploratory behavior is context-dependent in wild great tits. Behav. Ecol. 15, 1023–1030. Dixson, D.L., Munday, P.L., Jones, G.P., 2010. Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues. Ecol. Lett. 13, 68–75. Eikenaar, C., Richardson, D.S., Brouwer, L., Bristol, R., Komdeur, J., 2009. Experimental evaluation of sex differences in territory acquisition in a cooperatively breeding bird. Behav. Ecol. 20, 207–214. European Union, 2008. Marine Strategy Framework Directive. 2008/56/EC. Ferrari, M.C.O., Elvidge, C.K., Jackson, C.D., Chivers, D.P., Brown, G.E., 2010. The responses of prey fish to temporal variation in predation risk: sensory habituation or risk assessment? Behav. Ecol. 21, 532–536. Francis, C.D., Ortega, C.P., Cruz, A., 2009. Noise pollution changes avian communities and species interactions. Curr. Biol. 19, 1415–1419. Gagliardi-Seeley, J., Itzkowitz, M., 2009. Does being paired give male and female convict cichlids (Amatitlania nigrofasciata) an advantage when competing against same-sex individuals? Acta Ethol. 12, 115–120. Gosling, S., 2001. From mice to men: what can we learn about personality from animal research? Psychol. Bull. 127, 45–86. Hildebrand, J.A., 2009. Anthropogenic and natural sources of ambient noise in the ocean. Mar. Ecol. Prog. Ser. 395, 5–20. HMSO, 1986. Animals (Scientific Procedures) Act 1986. Amendment Regulations 2012. Holmes, T.H., McCormick, M.I., 2010. Smell, learn and live: the role of chemical alarm cues in predator learning during early life history in a marine fish. Behav. Process. 83, 299–305. Kight, C.R., Swaddle, J.P., 2011. How and why environmental noise impacts animals: an integrative, mechanistic review. Ecol. Lett. 14, 1052–1061. Kunc, H.P., Lyons, G.N., Sigwart, J.D., McLaughlin, K.E., Houghton, J.D.R., 2014. Anthropogenic noise affects behaviour across sensory modalities. Am. Nat. 184, E93–E100. Ladich, F., Schulz-Mirbach, T., 2013. Hearing in cichlid fishes under noise conditions. PLoS One 8, e57588. Lima, S.L., Dill, L.M., 1990. Behavioural decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619–640. Marentette, J.R., Balshine, S., 2012. Altered prey responses in round goby from contaminated sites. Ethology 118, 812–820. McEwen, B., Wingfield, J., 2003. The concept of allostasis in biology and biomedicine. Horm. Behav. 43, 2–15.

79

Metcalfe, N.B., Huntingford, F.A., Thorpe, J.E., 1987. The influence of predation risk on the feeding motivation and foraging strategy of juvenile Atlantic salmon. Anim. Behav. 35, 901–911. Munday, P.L., Dixson, D.L., Donelson, J.M., Jones, G.P., Pratchett, M.S., Devitsina, G.V., Doving, K.B., 2009. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. Proc. Natl. Acad. Sci. U. S. A. 106, 1848–1852. Picciulin, M., Sebastianutto, L., Codarin, A., Farina, A., Ferrero, E.A., 2010. In situ behavioural responses to boat noise exposure of Gobius cruentatus (Gmelin, 1789; fam. Gobiidae) and Chromis chromis (Linnaeus, 1758; fam. Pomacentridae) living in a marine protected area. J. Exp. Mar. Biol. 386, 125–132. Popper, A.N., 2003. Effects of anthropogenic sounds on fishes. Fisheries 28, 24–31. Popper, A.N., Fay, R.R., 2011. Rethinking sound detection by fishes. Hear. Res. 273, 25–36. Pottinger, T., Pickering, A., 1992. The influence of social-interaction on the acclimation of Rainbow-Trout, Oncorhynchus-Mykiss (Walbaum) to chronic stress. J. Fish Biol. 41, 435–447. Purser, J., Radford, A.N., 2011. Acoustic noise induces attention shifts and reduces foraging performance in three-spined sticklebacks (Gasterosteus aculeatus). PLoS One 6, e17478. Development Core Team, R., 2013. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria http://www.R-project.org/ Radford, A.N., Kerridge, E., Simpson, S.D., 2014. Acoustic communication in a noisy world: can fish compete with anthropogenic noise? Behav. Ecol. 25, 1022–1030. Radford, C.A., Montgomery, J.C., Caiger, P., Higgs, D.M., 2012. Pressure and particle motion detection thresholds in fish: a re-examination of salient auditory cues in teleosts. J. Exp. Biol. 215, 3429–3435. Sih, A., Kats, L., Maurer, E., 2003. Behavioural correlations across situations and the evolution of antipredator behaviour in a sunfish-salamander system. Anim. Behav. 65, 29–44. Simpson, S.D., Purser, J., Radford, A.N., 2014. Anthropogenic noise compromises antipredator behaviour in European eels. Global Change Biol., http://dx.doi.org/10.1111/gcb.12685. Simpson, S.D., Munday, P.L., Wittenrich, M.L., Manassa, R., Dixson, D.L., Gagliano, M., Yan, H.Y., 2011. Ocean acidification erodes crucial auditory behaviour in a marine fish. Biol. Lett. 7, 917–920. Slabbekoorn, H., Bouton, N., van Opzeeland, I., Coers, A., ten Cate, C., Popper, A.N., 2010. A noisy spring: the impact of globally rising underwater sound levels on fish. Trends Ecol. Evol. 25, 419–427. Tuomainen, U., Candolin, U., 2011. Behavioural responses to human-induced environmental change. Biol. Rev. Camb. Philos. Soc. 86, 640–657. Tyack, P.L., 2008. Implications for marine mammals of large-scale changes in the marine acoustic environment. J. Mammal. 89, 549–558. Vasconcelos, R.O., Amorim, M.C.P., Ladich, F., 2007. Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish. J. Exp. Biol. 210, 2104–2112. Verbeek, M., Drent, P., Wiepkema, P., 1994. Consistent individual-differences in early exploratory – behavior of male great tits. Anim. Behav. 48, 1113–1121. Voellmy, I.K., Purser, J., Flynn, D., Kennedy, P., Simpson, S.D., Radford, A.N., 2014. Acoustic noise reduces foraging success in two sympatric fish species via different mechanisms. Anim. Behav. 89, 191–198. Wale, M.A., Simpson, S.D., Radford, A.N., 2013. Noise negatively affects foraging and antipredator behaviour in shore crabs. Anim. Behav. 86, 111–118. Wilson, D., Clark, A., Coleman, K., Dearstyne, T., 1994. Shyness and boldness in humans and other animals. Trends Ecol. Evol. 9, 442–446. Wingfield, J.C., 2005. The concept of allostasis: coping with a capricious environment. J. Mammal. 86, 248–254. Wright, A.J., Aguilar Soto, N., Baldwin, A.L., Bateson, M., Beale, C.M., Clark, C., Deak, T., Edwards, E.F., Fernandez, A.F., Godinho, R., Hatch, L.T., Kakuschke, A., Lesseau, D., Martineau, D., Romero, L.M., Weilgart, L.S., Wintle, B.A., Notarbartolo-di-Sciara, G., Martin, V., 2007. Anthropogenic noise as a stressor in animals: a multidisciplinary perspective. Int. J. Comp. Psychol. 20, 250–273. Yan, H., Popper, A.N., 1992. Auditory-sensitivity of the cichlid fish Astronotus-Ocellatus (Cuvier). J. Comp. Physiol. Sens. Neural Behav. Physiol. 171, 105–109.