Acoustic communication in a noisy world: Can fish compete with anthropogenic noise?

Behavioral Ecology

Volumn 25, Issue 5, 2014, Pages 1022-1030

  Radford, Andrew N ^a   Kerridge, Emma ^a   Simpson, Stephen D ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

acoustic signaling; adaptation; anthropogenic noise; behavioral plasticity; fitness benefits; hearing; masking; pollution

Indexed keywords

ACOUSTICS; ANTHROPOGENIC EFFECT; BEHAVIORAL RESPONSE; BIRD; COMMUNICATION BEHAVIOR; FISH; MARINE MAMMAL; NOISE POLLUTION; PHENOTYPIC PLASTICITY; PROTEIN; SIGNALING;

EID: 84907708238     PISSN: 10452249     EISSN: 14657279     Source Type: Journal    
DOI: 10.1093/beheco/aru029     Document Type: Review

References (121)

1. Amorim MCP, Neves ASM. 2008. Male painted gobies vocalise to defend territories. Behaviour. 145:1065-1083.
2. Amorim MCP, Simões JM, Almada VC, Fonseca PJ. 2011. Stereotypy and variation of the mating call in the Lusitanian toadfish, Halobatrachus didactylus. Behav Ecol Sociobiol. 65:707-716.
3. Amorim MCP, Simões JM, Fonseca PJ, Turner GF. 2008. Species differences in courtship acoustic signals among five Lake Malawi cichlid species (Pseudotropheus spp.). J Fish Biol. 72:1355-1368.
4. Amoser S, Wysocki LE, Ladich F. 2004. Noise emission during the first powerboat race in an Alpine lake and potential impact on fish communities. J Acoust Soc Am. 116:3789-3797.
5. Barber JR, Crooks KR, Fristrup KM. 2009. The costs of chronic noise exposure for terrestrial organisms. Trends Ecol Evol. 25:180-189.
6. Bass AH, Ladich F. 2008. Vocal-acoustic communication: from neurons to behavior. In: Webb JF, Fay RR, Popper AN, editors. Springer handbook of auditory research. Vol. 32. New York: Springer. p. 253-278.
7. Bejder L, Samuels A, Whitehead H, Gales N. 2006. Interpreting short-term behavioural responses to disturbance within a longitudinal perspective. Anim Behav. 72:1149-1158.
8. Bermudez-Cuamatzin E, Ros-Chelén AA, Gil D, Garcia CM. 2011. Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird. Biol Lett. 7:36-38.
9. Bone Q, Moore RH. 2008. Biology of fishes. 3rd ed. New York: Taylor & Francis Group.
10. Brumm H. 2004. The impact of environmental noise on song amplitude in a territorial bird. J Anim Ecol. 73:434-440.
11. Brumm H, Schmidt R, Schrader L. 2009. Noise-dependent vocal plasticity in domestic fowl. Anim Behav. 78:741-746.
12. Brumm H, Slabbekoorn H. 2005. Acoustic communication in noise. Adv Study Behav. 35:151-209.
13. Brumm H, Todt D. 2002. Noise-dependent song amplitude regulation in a territorial songbird. Anim Behav. 63:891-897.
14. Brumm H, Voss K, Köllmer I, Todt D. 2004. Acoustic communication in noise: regulation of call characteristics in a New World monkey. J Exp Biol. 207:443-448.
15. Brumm H, Zollinger SA. 2011. The evolution of the Lombard effect: 100 years of psychoacoustic research. Behaviour. 148:1173-1198.
16. Candolin U. 2003. The use of multiple cues in mate choice. Biol Rev. 78:575-595.
17. Catchpole CK, Slater PJB. 2008. Bird song: biological themes and variations. Cambridge (MA): Cambridge University Press.
18. Chan AAY-H, Blumstein DT. 2011. Attention, noise, and implications for wildlife conservation and management. App Anim Behav Sci. 131:1-7.
19. Clark CW, Ellison WT, Southall BL, Hatch L, van Parijs SM, Frankel A, Ponikaris D. 2009. Acoustic masking in marine ecosystems: intuitions, analyses and implication. Mar Ecol Prog Ser. 395:201-222.
20. Codarin A, Wysocki LE, Ladich F, Picciulin M. 2009. Effects of ambient and boat noise on hearing and communication in three fish species living in a marine protected area (Miramare, Italy). Mar Pollut Bull. 58:1880-1887.
21. Diaz M, Parra A, Gallardo C. 2011. Serins respond to anthropogenic noise by increasing vocal activity. Behav Ecol. 22:332-336.
22. Di Iorio L, Clark CW. 2010. Exposure to seismic survey alters blue whale acoustic communication. Biol Lett. 6:51-54.
23. Dooling RJ, West, EW, Leek MR. 2009. Conceptual and computation models of the effects of anthropogenic sound on birds. Proc Inst Acoust. 31 (part 1).
24. Dubois A, Martens J. 1984. A case of possible vocal convergence between frogs and a bird in Himalayan torrents. J Ornithol. 125:455-463.
25. Engas A, Løkkeborg S, Ona E, Soldal AV. 1996. Effects of seismic shooting on local abundance and catch rates of cod (Gadus morhua) and haddock (Melanogrammus aeglefinus). Can J Fish Aquat Sci. 53:2238-2249.
26. FAO. 2012. The State of World Fisheries and Aquaculture 2012. Rome (Italy): FAO.
27. Fay RR, Edds-Walton PL. 1997. Directional response properties of saccular afferents of the toadfish, Opsanus tau. Hear Res. 111:1-21.
28. Fay RR, Megela-Simmons A. 1999. The sense of hearing in fishes and amphibians. In: Fay RR, Popper, AN, editors. Comparative hearing: fish and amphibians. New York: Springer Verlag. p. 269-318.
29. Fay RR, Popper AN. 2012. Fish hearing: new perspectives from two senior bioacousticians. Brain Behav Evol. 79:215-217.
30. Fernandez-Juricic E, Poston R, De Collibus K, Morgan T, Bastain B, Martin C, Jones K, Treminio R. 2005. Microhabitat selection and singing behavior patterns of male house finches (Carpodacus mexicanus) in urban parks in a heavily urbanized landscape in the western U.S. Urban Habitats. 3:49-69.
31. Fine ML, Thorson RF. 2008. Use of passive acoustics for assessing behavioral interactions in individual toadfish. Trans Am Fish Soc. 137:627-637.
32. Foote AD, Osborne RW, Hoelzel AR. 2004. Whale-call response to masking boat noise. Nature. 428:910.
33. Francis CD, Ortega CP, Cruz A. 2009. Noise pollution changes avian communities and species interactions. Curr Biol. 19:1415-1419.
34. Francis CD, Ortega CP, Cruz A. 2011. Vocal frequency change reflects different responses to anthropogenic noise in two suboscine tyrant flycatchers. Proc Biol Sci. 278:2025-2031.
35. Fristrup KM, Hatch LT, Clark CW. 2003. Variation in humpback whale (Megaptera novaeangliae) song length in relation to low-frequency sound broadcasts. J Acoust Soc Am. 113:3411-3424.
36. Fuller RA, Warren PH, Gaston KJ. 2007. Daytime noise predicts nocturnal singing in urban robins. Biol Lett. 3:368-370.
37. Gerhardt H, Huber F. 2002. Acoustic communication in insects and anurans. Chicago (IL): The University of Chicago Press.
38. Halfwerk W, Holleman LJM, Lessells CM, Slabbekoorn H. 2011. Negative impact of traffic noise on avian reproductive success. J Appl Ecol. 48:210-219.
39. Halvorsen MB, Casper BM, Matthews F, Carlson TJ, Popper AN. 2012. Effects of exposure to pile-driving sounds on the lake sturgeon, Nile tilapia and hogchoker. Proc Biol Sci. 279:4705-4714.
40. Hanna D, Blouin-Demers G, Wilson DR, Mennill DJ. 2011. Anthropogenic noise affects song structure in red-winged blackbirds (Agelaius phoeniceus). J Exp Biol. 214:3549-3556.
41. Hawkins AD, Amorim MCP. 2000. Spawning sounds of the male haddock, Melanogrammus aeglefinus. Environ Biol Fish. 59:29-41.
42. Hawkins AD, Chapman CJ. 1975. Masked auditory thresholds in the cod (Gadus morhua L.). J Comp Physiol. 103:209-226.
43. Hawkins AD, Myrberg AA. 1983. Hearing and sound communication underwater. In: Lewis B, editor. Bioacoustics, a comparative approach. London: Academic Press. p. 347-405.
44. Hawkins AD, Rasmussen K. 1978. The calls of galoid fish. J Mar Biol Ass Lond. 58:891-911.
45. Henglmuller SM, Ladich F. 1999. Development of agonistic behaviour and vocalization in croaking gouramis. J Fish Biol. 54:380-395.
46. Heuschele J, Mannerla M, Gienapp P, Candolin U. 2009. Environmentdependent use of mate choice cues in sticklebacks. Behav Ecol. 20:1223-1227.
47. Hildebrand JA. 2009. Anthropogenic and natural sources of ambient noise in the ocean. Mar Ecol Prog Ser. 395:4-20.
48. Holles S, Simpson SD, Radford AN, Berten L, Lecchini D. 2013. Boat noise disrupts orientation behaviour in a coral reef fish. Mar Ecol Prog Ser. 485:295-300.
49. Holt MM, Noren DP, Veirs V, Emmons CK, Veirs S. 2009. Speaking up: killer whales (Orcinus orca) increase their call amplitude in response to vessel noise. J Acoust Soc Am. 125:EL27-EL32.
50. Johnstone RA. 1996. Multiple displays in animal communication: "Backup signals" and "multiple messages". Phil Trans R Soc B. 351:329-338.
51. Kaiser K, Hammers JL. 2009. The effect of anthropogenic noise on male advertisement call rate in the neotropical treefrog, Dendropsophus triangulum. Behaviour. 146:1053-1069.
52. Keevin TM, Hempen GL. 1997. The environmental effects of underwater explosions with methods to mitigate impacts. St. Louis (MO): U.S. Army Corps of Engineers. Available from: http://www.denix.osd. mil/nr/upload/underwaterexplosions.pdf, last accessed on 20 January 2014.
53. Kight CR, Saha MS, Swaddle JP. 2012. Anthropogenic noise is associated with reductions in the productivity of breeding Eastern Bluebirds (Sialia sialis). Ecol Appl. 22:1989-1996.
54. Kight CR, Swaddle JP. 2011. How and why environmental noise impacts animals: an integrative, mechanistic review. Ecol Lett. 14:1052-1061.
55. La VT. 2012. Diurnal and nocturnal birds vocalize at night: a review. Condor. 114:245-257.
56. Ladich F, Collin SP, Moller P, Kapoor BG. 2006. Fish communication. Enfield (CT): Science Publisher.
57. Lampe U, Schmoll T, Franzke A, Reinhold K. 2012. Staying tuned: grasshoppers from noisy roadside habitats produce courtship signals with elevated frequency components. Funct Ecol. 26:1348-1354.
58. Leonard ML, Horn AG. 2012. Ambient noise increases missed detections in nestling birds. Biol Lett. 8:530-532.
59. Le Prell CG, Henderson D, Fay RR, Popper AN, editors. 2012. Noiseinduced hearing loss: scientific advances. New York: Springer Science + Business Media, LLC.
60. Lesage V, Kingsley MCS, Sjare B. 1999. The effect of vessel noise on the vocal behavior of belugas in the St. Lawrence River estuary, Canada. Mar Mamm Sci. 15:65-84.
61. Lohr B, Wright TF, Dooling RJ. 2003. Detection and discrimination of natural calls in masking noise by birds: estimating the active space of a signal. Anim Behav. 65:763-777.
62. Løkkeborg S, Ona E, Vold A, Salthaug A. 2012. Effects of sounds from seismic air guns on fish behavior and catch rates. In: Popper AN, Hawkins AD, editors. The effects of noise on aquatic life. New York: Springer. p. 415-419.
63. Love EK, Bee MA. 2010. An experimental test of noise-dependent voice amplitude regulation in Copes grey treefrog (Hyla chrysoscelis). Anim Behav. 80:509-515.
64. Lowry H, Lill A, Wong BB. 2012. How noisy does a noisy miner have to be? Amplitude adjustments of alarm calls in an avian urban adapter. PLoS One. 7:e29960.
65. Luczkovich JJ, Daniel HJ, Hutchinson M, Jenkins T, Johnson SE, Pullinger RC, Sprague MW. 2000. Sounds of sex and death in the sea: bottlenose dolphin whistles suppress mating choruses of silver perch. Bioacoustics. 10:323-334.
66. Lugli M. 2010. Sounds of shallow water fishes pitch within the quiet window of the habitat ambient noise. J Comp Physiol A. 196:439-451.
67. Lugli M, Yan HY, Fine ML. 2003. Acoustic communication in two freshwater gobies: the relationship between ambient noise, hearing thresholds and sound spectrum. J Comp Phys A. 189:309-320.
68. Luther D, Baptista L. 2010. Urban noise and the cultural evolution of bird songs. Proc Biol Sci. 277:469-473.
69. Luther D, Gentry K. 2013. Sources of background noise and their influence on vertebrate acoustic communication. Behaviour. 150:1045-1068.
70. Mann DA. 2006. Propagation of fish sounds. In: Ladich F, Collin SP, Moller P, Kapoor BG, editors. Communication in fishes. Vol. 1. Enfield (CT): Science Publishers. p. 107-120.
71. Mann DA, Lobel PS. 1998. Acoustic behaviour of the damselfish Dascyllus albisella: behavioural and geographic variation. Environ Biol Fish. 51:421-428.
72. McDonald MA, Hildebrand JA, Wiggins SM. 2006. Increases in deep ocean ambient noise in the Northeast Pacific west of San Nicolas Island, California. J Acoust Soc Am. 120:711-718.
73. Miller PJ, Biassoni N, Samuels A, Tyack PL. 2000. Whale songs lengthen in response to sonar. Nature. 405:903.
74. Morley EL, Jones G, Radford AN. 2014. The importance of invertebrates when considering the impacts of anthropogenic noise. Proc Biol Sci. 281:20132683.
75. Myrberg AA. 1981. Sound communication and interception in fishes. In Tavolga WN, Popper, AN, Fay RR, editors. Hearing and sound communication in fishes. New York: Springer-Verlag. p. 395-426.
76. Myrberg AA, Ha SJ, Shamblott MJ. 1993. The sounds of bicolor damselfish (Pomacentrus partitus)-predictors of body size and a spectral basis for individual recognition and assessment. J Acoust Soc Am. 94:3067-3070.
77. Myrberg AA, Mohler M, Catala JD. 1986. Sound production by males of a coral reef fish (Pomacentrus partitus): its significance to females. Anim Behav. 34:913-923.
78. Myrberg AA, Spires JY. 1972. Sound discrimination by the bicolor damselfish (Eupomacentrus partitus). J Exp Biol. 57:727-735.
79. Naguib M. 2013. Living in a noisy world: indirect effects of noise on animal communication. Behaviour. 150:1069-1084.
80. Normandeau Associates, Inc. 2012. Effects of noise on fish, fisheries, and invertebrates in the U.S. Atlantic and Arctic from energy industry sound-generating activities. A literature synthesis for the U.S. Dept. of the Interior, Bureau of Ocean Energy Management. Contract #M11PC00031. Bedford (NH): U.S. Dept. of the Interior, Bureau of Ocean Energy Management. 153 pp. Available from: http://www.data.boem.gov/homepg/data-center/other/espis/espismaster.asp?appid=1, last accessed on 30 February 2014
81. Oberweger K, Goller F. 2001. The metabolic cost of birdsong production. J Exp Biol. 204:3379-3388.
82. Parks SE, Clark CW, Tyack PL. 2007. Short- and long-term changes in right whale calling behavior: the potential effects of noise on acoustic communication. J Acoust Soc Am. 122:3725-3731.
83. Parmentier E, Colleye O, Fine ML, Frédérich B, Vandewalle P, Herrel A. 2007. Sound production in the clownfish Amphiprion clarkii. Science. 316:1006.
84. Parmentier E, Kèver L, Casadevall M, Lecchini D. 2010. Diversity and complexity in the acoustic behaviour of Dascyllus flavicaudus (Pomacentridae). Mar Biol. 157:2317-2327.
85. Parmentier E, Lagardère JP, Vandewalle P, Fine ML. 2005. Geographical variation in sound production in the anemonefish Amphiprion akallopisos. Proc Biol Sci. 272:1697-1703.
86. Parvulescu A. 1964. Problems of propagation and processing. In: Tavolga WN, editor. Marine bioacoustics. Oxford: Pergamon. p. 87-100.
87. Picciulin M, Sebastianutto L, Codarin A, Calcagno G, Ferrero EA. 2012. Brown meagre vocalization rate increases during repetitive boat noise exposures: a possible case of vocal compensation. J Acoust Soc Am. 132:3118-3124.
88. Plenderleith M, van Oosterhout C, Robinson RL, Turner GF. 2005. Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish. Biol Lett. 1:411-414.
89. Popper AN, Fay RR. 1999. Comparative hearing: fish and amphibians. New York: Springer Verlag.
90. Popper AN, Halvorsen MB, Kane A, Miller DL, Smith ME, Song J, Stein P, Wysocki LE. 2007. The effects of high-intensity, low-frequency active sonar on rainbow trout. J Acoust Soc Am. 122:623-635.
91. Popper AN, Hastings MC. 2009. The effects of anthropogenic sources of sound on fishes. J Fish Biol. 75:455-489.
92. Popper AN, Schilt CR. 2008. Hearing and acoustic behavior (basic and applied). In: Webb JF, Popper AN, Fay RR, editors. Fish bioacoustics. New York: Springer. p. 17-48.
93. Popper AN, Smith ME, Cott PA, Hanna BW, MacGillivray AO, Austin ME, Mann DA. 2005. Effects of exposure to seismic airgun use on hearing of three fish species. J Acoust Soc Am. 117:3958-3971.
94. Purser J, Radford AN. 2011. Acoustic noise induces attention shifts and reduces foraging performance in three-spined sticklebacks (Gasterosteus aculeatus). PLoS One. 6:e17478.
95. Rabin LA, Coss RG, Owings DH. 2006. The effects of wind turbines on antipredator behaviour in California ground squirrels (Spermophilus beecheyi). Biol Conserv. 131:410-420.
96. Radford AN, Morley E, Jones G. 2012. The effects of noise on biodiversity. Defra report NO0235.
97. Radford AN, Purser J, Bruintjes R, Voellmy IK, Everley KA, Wale MA, Holles S, Simpson SD. Forthcoming 2014. Beyond a simple effect: variable and changing responses to anthropogenic noise. In: Popper AN, Hawkins AD, editors. Effects of noise on aquatic life II. New York: Springer.
98. Read J, Jones G, Radford AN. 2014. Fitness costs are as important as benefits when considering noise-induced behavioural responses. Behav Ecol. 25:4-7.
99. Remage-Healey L, Nowacek DP, Bass AH. 2006. Dolphin foraging sounds suppress calling and elevate stress hormone levels in a prey species, the Gulf toadfish. J Exp Biol. 209:4444-4451.
100. Rowe S, Hutchings JA, Skjaeraasen JE, Bezanson L. 2008. Morphological and behavioural correlates of reproductive success in Atlantic cod Gadus morhua. Mar Ecol Prog Ser. 354:257-265.
101. Schaub A, Ostwald J, Siemers BM. 2009. Foraging bats avoid noise. J Exp Biol. 211:3174-3180.
102. Simpson SD, Meekan MG, Larsen NJ, McCauley RD, Jeffs A. 2010. Behavioural plasticity in larval reef fish: orientation is influenced by recent acoustic experiences. Behav Ecol. 21:1098-1105.
103. Simpson SD, Meekan M, Montgomery J, McCauley R, Jeffs A. 2005. Homeward sound. Science. 308:221.
104. Simpson SD, Radford AN, Tickle EJ, Meekan MG, Jeffs AG. 2011. Adaptive avoidance of reef noise. PLoS One. 6:e16625.
105. Slabbekoorn H. Forthcoming 2014. Aiming for progress in understanding underwater noise impact on fish: complementary need for indoor and outdoor studies. In: Popper AN, Hawkins AD, editors. Effects of noise on aquatic life II. New York: Springer.
106. Slabbekoorn H, Bouton N, van Opzeeland I, Coers A, ten Cate C, Popper AN. 2010. A noisy spring: the impact of globally rising underwater sound levels on fish. Trends Ecol Evol. 25:419-427.
107. Slabbekoorn H, Peet M. 2003. Birds sing at a higher pitch in urban noise: great tits hit the high notes to ensure their mating calls are heard above the citys din. Nature. 424:267.
108. Sun JWC, Narins PA. 2005. Anthropogenic sounds differentially affect amphibian call rate. Biol Cons. 121:419-427.
109. van der Sluijs I, Gray SM, Amorim MCP, Barber I, Candolin U, Hendry AP, Krahe R, Maan ME, Utne-Palm AC, Wagner H-J, et al. 2011. Communication in troubled waters: responses of fish communication systems to changing environments. Evol Ecol. 25:623-640.
110. Tavolga WN. 1971. Sound production and detection. In: Hoar WS, Randall DJ, editors. Fish physiology. New York: Academic Press. p. 135-205.
111. Tyack P. 2008. Implications for marine mammals of large-scale changes in the marine acoustic environment. J Mamm. 89:549-558.
112. United Nations. 2011. World urbanization prospects: the 2011 revision. New York: United Nations.
113. Vasconcelos RO, Amorim MC, Ladich F. 2007. Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish. J Exp Biol. 210:21042112.
114. Vasconcelos RO, Ladich F. 2008. Development of vocalization, auditory sensitivity and acoustic communication in the Lusitanian toadfish Halobatrachus didactylus. J Exp Biol. 211:502-509.
115. Verzijden MN, van Heusden J, Bouton N, Witte F, ten Cate C, Slabbekoorn H. 2010. Sounds of male Lake Victoria cichlids vary within and between species and affect female mate preferences. Behav Ecol. 21:548-555.
116. Watts RD, Compton RW, McCammon JH, Rich CL, Wright SM, Owens T, Ouren DS. 2007. Roadless space of the conterminous United States. Science. 316:736-738.
117. Winn H. 1964. The biological significance of fish sounds. In: Tavolga WN, editor. Marine bioacoustics. Oxford: Pergamon Press. p. 213-231.
118. World Health Organization. 2011. Burden of disease from environmental noise: quantification of healthy life years lost in Europe. Geneva (Switzerland): World Health Organization.
119. Wright AJ, Soto NA, Baldwin AL, Bateson M, Beale CM, Clark C, Deak T, Edwards EF, Fernández A, Godinho A, et al. 2007. Anthropogenic noise as a stressor in animals: a multidisciplinary perspective. Int J Comp Psychol. 20:250273.
120. Wysocki LE, Davidson JW, Smith ME, Frankel AS, Ellison WT, Mazik PM, Popper AN, Bebak J. 2007. Effects of aquaculture production noise on hearing, growth, and disease resistance of rainbow trout Oncohynchus mykiss. Aquaculture. 272:687-697.
121. Wysocki LE, Dittami JP, Ladich F. 2006. Ship noise and corticol secretion in European freshwater fishes. Biol Conserv. 128:501-508.