Abstract
Fish populations are increasingly being subjected to anthropogenic changes to their sensory environments. The impact of these changes on inter- and intra-specific communication, and its evolutionary consequences, has only recently started to receive research attention. A disruption of the sensory environment is likely to impact communication, especially with respect to reproductive interactions that help to maintain species boundaries. Aquatic ecosystems around the world are being threatened by a variety of environmental stressors, causing dramatic losses of biodiversity and bringing urgency to the need to understand how fish respond to rapid environmental changes. Here, we discuss current research on different communication systems (visual, chemical, acoustic, electric) and explore the state of our knowledge of how complex systems respond to environmental stressors using fish as a model. By far the bulk of our understanding comes from research on visual communication in the context of mate selection and competition for mates, while work on other communication systems is accumulating. In particular, it is increasingly acknowledged that environmental effects on one mode of communication may trigger compensation through other modalities. The strength and direction of selection on communication traits may vary if such compensation occurs. However, we find a dearth of studies that have taken a multimodal approach to investigating the evolutionary impact of environmental change on communication in fish. Future research should focus on the interaction between different modes of communication, especially under changing environmental conditions. Further, we see an urgent need for a better understanding of the evolutionary consequences of changes in communication systems on fish diversity.
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References
Albert AYK, Millar NP, Schluter D (2007) Character displacement of male nuptial colour in threespine sticklebacks (Gasterosteus aculeatus). Biol J Linnean Soc 91:37–48
Amorim MCP (2006) Diversity of sound production in fish. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers, Enfield, pp 71–105
Amorim MCP, Knight ME, Stratoudakis Y, Turner GF (2004) Differences in sounds made by courting males of three closely related Lake Malawi cichlid species. J Fish Biol 65:1358–1371
Amorim MCP, Simoes 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
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Arnegard ME, Bogdanowicz SM, Hopkins CD (2005) Multiple cases of striking genetic similarity between alternate electric fish signal morphs in sympatric. Evolution 59:324–343
Arnegard ME, Jackson BS, Hopkins CD (2006) Time-domain signal divergence and discrimination without receptor modification in sympatric morphs of electric fishes. J Exp Biol 209:2182–2198
Baatrup E, Junge M (2001) Antiandrogenic pesticides disrupt sexual characteristics in the adult male guppy (Poecilia reticulata). Environ Health Perspect 109:1063–1070
Baier B (2008) Effect of conductivity changes on the stability of electric signal waveforms in dwarf stonebashers (Mormyridae; Pollimyrus castelnaui, P. marianne). J Comp Physiol A 194:915–919
Barber I, Nairn D, Huntingford FA (2001) Nests as ornaments: revealing construction by male sticklebacks. Behav Ecol 12:390–396
Bell AM (2001) Effects of an endocrine disrupter on courtship and aggressive behaviour of male three-spined stickleback, Gasterosteus aculeatus. Anim Behav 62:775–780
Boughman JW (2001) Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411:944–948
Brooks R, Couldridge V (1999) Multiple sexual ornaments coevolve with multiple mating preferences. Am Nat 154:37–45
Bullock TH, Hopkins CD, Popper AN, Fay RR (2005) Electroreception. Springer, New York
Candolin U (2003) The use of multiple cues in mate choice. Biol Rev 78:575–595
Candolin U, Salesto T, Evers M (2007) Changed environmental conditions weaken sexual selection in sticklebacks. J Evol Biol 20:233–239
Cheng CL, Flamarique IN (2004) Opsin expression: New mechanism for modulating colour vision—Single cones start making a different opsin as young salmon move to deeper waters. Nature 428:279
Colman JR, Baldwin D, Johnson LL, Scholz NL (2009) Effects of the synthetic estrogen, 17 alpha-ethinylestradiol, on aggression and courtship behavior in male zebrafish (Danio rerio). Aquat Toxicol 91:346–354
Crampton WGR, Albert JS (2006) Evolution of electric signal diversity in Gymnotiform fishes. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers, Enfield, pp 647–731
Cummings ME (2007) Sensory trade-offs predict signal divergence in surfperch. Evolution 61:530–545
Darimont CT, Carlson SM, Kinnison MT, Paquet PC, Reimchen TE, Wilmers CC (2009) Human predators outpace other agents of trait change in the wild. Proc Natl Acad Sci USA 106:952–954
Darwall WRT, Vié JC (2005) Identifying important sites for conservation of freshwater biodiversity: extending the species-based approach. Fisheries Manag Ecol 12:287–293
DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81
Domenici P, Claireaux G, McKenzie DJ (2007) Environmental constraints upon locomotion and predator-prey interactions in aquatic organisms: an introduction. Philos Trans R Soc Lond Ser B-Biol Sci 362:1929–1936
Donohue I, Molinos JG (2009) Impacts of increased sediment loads on the ecology of lakes. Biol Rev 84:517–531
Dunlap KD, Smith GT, Yekta A (2000) Temperature dependence of electrocommunication signals and their underlying neural rhythms in the weakly electric fish, Apteronotus leptorhynchus. Brain Behav Evol 55:152–162
Dunlop ES, Heino M, Dieckmann U (2009) Eco-genetic modeling of contemporary life-history evolution. Ecol Appl 19:1815–1834
Enberg K, Jorgensen C, Dunlop ES, Heino M, Dieckmann U (2009) Implications of fisheries-induced evolution for stock rebuilding and recovery. Evol Appl 2:394–414
Endler JA (1980) Natural selection on colour patterns in Poecilia reticulata. Evolution 34:76–91
Endler JA (1983) Natural and sexual selection on colour patterns in poeciliid fishes. Env Biol Fish 9:173–190
Endler JA (1992) Signals, signal condition, and the direction of evolution. Am Nat 139:S125–S153
Endler JA, Westcott DA, Madden JR, Robson T (2005) Animal visual systems and the evolution of colour patterns: sensory processing illuminates signal evolution. Evolution 59:1795–1818
Evans CD, Monteith DT, Cooper DM (2005) Long-term increases in surface water dissolved organic carbon: observations, possible causes and environmental impacts. Environ Pollut 137:55–71
Fay RR, Popper AN (2000) Evolution of hearing in vertebrates: the inner ears and processing. Hear Res 149:1–10
Feulner PGD, Kirschbaum F, Tiedemann R (2008) Adaptive radiation in the Congo River: an ecological speciation scenario for African weakly electric fish (Teleostei; Mormyridae; Campylomormyrus). J Physiology-Paris 102:340–346
Feulner PGD, Plath M, Engelmann J, Kirschbaum F, Tiedemann R (2009) Electrifying love: electric fish use species-specific discharge for mate recognition. Biol Lett 5:225–228
Fisher HS, Wong BBM, Rosenthal GG (2006) Alteration of the chemical environment disrupts communication in a freshwater fish. Proc R Soc Lond Ser B-Biol Sci 273:1187–1193
Fugère V, Krahe R (2010) Electric signals and species recognition in the wave-type gymnotiform fish Apteronotus leptorhynchus. J Exp Biol 213:225–236
Fuller RC, Houle D, Travis J (2005) Sensory bias as an explanation for the evolution of mate preferences. Am Nat 166:437–446
Gray SM, McKinnon JS (2007) Linking colour polymorphism maintenance and speciation. Trends Ecol Evol 22:71–79
Gray SM, Dill LM, Tantu FY, Loew ER, Herder F, McKinnon JS (2008) Environment-contingent sexual selection in a colour polymorphic fish. Proc R Soc Lond Ser B-Biol Sci 275:1785–1791
Grether GF (2000) Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata). Evolution 54:1712–1724
Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond Ser B-Biol Sci 266:1317–1322
Hendry AP, Farrugia TJ, Kinnison MT (2008) Human influences on rates of phenotypic change in wild animal populations. Molec Ecol 17:20–29
Heuschele J, Candolin U (2007) An increase in pH boosts olfactory communication in sticklebacks. Biol Lett 3:411–413
Heuschele J, Mannerla M, Gienapp P, Candolin U (2009) Environment-dependent use of mate choice cues in sticklebacks. Behav Ecol 20:1223–1227
Hofmann Cv, O’Quin KE, Marshall NJ, Cronin TW, Seehausen O, Carleton KL (2009) The eyes have it: regulatory and structural changes both underlie cichlid visual pigment diversity. Plos Biol 7:e1000266
Hopkins CD (1976) Stimulus filtering and electroreception: tuberous electroreceptor’s in three species of gymnotoid fish. J Comp Physiol 111:171–207
Jaensson A, Scott AP, Moore A, Kylin H, Olsen KH (2007) Effects of a pyrethroid pesticide on endocrine responses to female odours and reproductive behaviour in male parr of brown trout (Salmo trutta L.). Aquat Toxicol 81:1–9
Järvenpää M, Lindström K (2004) Water turbidity by algal blooms causes mating system breakdown in a shallow-water fish, the sand goby Pomatoschistus minutus. Proc R Soc Lond Ser B-Biol Sci 271:2361–2365
Jeffery WR (2005) Adaptive evolution of eye degeneration in the Mexican blind cavefish. J Hered 96:185–196
Jordan R, Kellogg K, Juanes F, Stauffer J (2003) Evaluation of female mate choice cues in a group of Lake Malawi mbuna (Cichlidae). Copeia 16:181–186
Karim N, Gordon SP, Schwartz AK, Hendry AP (2007) This is not deja vu all over again: male guppy colour in a new experimental introduction. J Evol Biol 20:1339–1350
Kemp DJ, Reznick DN, Grether GF (2008) Ornamental evolution in Trinidadian guppies (Poecilia reticulata): insights from sensory processing-based analyses of entire colour patterns. Biol J Linnean Soc 95:734–747
Kidd MR, Danley PD, Kocher TD (2006) A direct assay of female choice in cichlids: all the eggs in one basket. J Fish Biol 68:373–384
Kodric-Brown A, Nicoletto PF (2005) Courtship behaviour, swimming performance, and microhabitat use of Trinidadian guppies. Env Biol Fish 73:299–307
Kramer B, Kuhn B (1993) Electric signalling and impedance matching in a variable environment—the electric organ of mormyrid fish actively adapts to changes in water conductivity. Naturwissenschaften 80:43–46
Ladich F (2007) Females whisper briefly during sex: context- and sex-specific differences in sounds made by croaking gouramis. Anim Behav 73:379–387
Ladich F, Fine ML (2006) Sound-generating mechanisms in fishes: a unique diversity in vertebrates. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers, Enfield, pp 1–43
Lande R (2009) Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J Evol Biol 22:1435–1446
Landsberger M, von der Emde G, Haverkate D, Schuster S, Gentsch J, Ulbricht E, Reichenbach A, Makarov F, Wagner HJ (2008) Dim light vision—morphological and functional adaptations of the eye of the mormyrid fish, Gnathonemus petersii. J Physiology-Paris 102:291–303
Lavoué S, Sullivan JP, Arnegard ME, Hopkins CD (2008) Differentiation of morphology, genetics and electric signals in a region of sympatric between sister species of African electric fish (Mormyridae). J Evol Biol 21:1030–1045
Law R (2007) Fisheries-induced evolution: present status and future direction. Mar Ecol-Prog Ser 335:271–277
Levine JS, MacNichol EF (1982) Colour vision in fishes. Sci Am 246:140–149
Lewandowski E, Boughman JW (2008) Effects of genetics and light environment on colour expression in three spine sticklebacks. Biol J Linnean Soc 27:663–673
Lim MLM, Sodhi NS, Endler JA (2008) Conservation with sense. Science 319:281
Lobel PS (1998) Possible species specific courtship sounds by two sympatric cichlid fishes in Lake Malawi, Africa. Env Biol Fish 52:443–452
Loew ER, Lythgoe JN (1978) Ecology of cone pigments in teleost fishes. Vis Res 18:715–722
Maan ME, Seehausen O, van Alphen JJM (2010) Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish. Biol J Linnean Soc 99:398–406
Malmqvist B, Rundle S (2002) Threats to the running water ecosystems of the world. Environ Conserv 29:134–153
McLennan DA (2003) The importance of olfactory signals in the gasterosteid mating system: sticklebacks go multimodal. Biol J Linnean Soc 80:555–572
Milinski M (2006) The major histocompatibility complex, sexual selection, and mate choice. Annu Rev Ecol Evol S 37:159–186
Moller P (2002) Multimodal sensory integration in weakly electric fish: a behaviorial account. J Physiology-Paris 96:547–556
Moller P (2006) Electrocommunication: history, insights, and new questions. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers, Enfield, pp 579–598
Moore A, Waring CP (2001) The effects of a synthetic pyrethroid pesticide on some aspects of reproduction in Atlantic salmon (Salmo salar L.). Aquat Toxicol 52:1–12
Myrberg AAJ, Spanier E, Ha SJ (1978) Temporal patterning in acoustical communication. In: Reese ES, Lighter FJ (eds) Contrasts in behaviour. Wiley, New York, pp 137–179
Myrberg AA, Mohler M, Catala J (1986) Sound production by males of a coral reef fish (Pomacentrus partitus): its significance to females. Anim Behav 34:923–933
Östlund-Nilsson S, Holmlund M (2003) The artistic three-spined stickleback (Gasterosteous aculeatus). Behav Ecol Sociobiol 53:214–220
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42
Pauers MJ, McKinnon JS, Ehlinger TJ (2004) Directional sexual selection on chroma and within-pattern colour contrast in Labeotropheus fuelleborni. Proc R Soc Lond Ser B-Biol Sci 271:S444–S447
Plath M, Blum D, Tiedemann R, Schlupp I (2008) A visual audience effect in a cavefish. Behaviour 145:931–947
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
Popper AN, Hastings MC (2009) The effects of anthropogenic sources of sound on fishes. J Fish Biol 75:455–489
Price TD (2006) Phenotypic plasticity, sexual selection and the evolution of colour patterns. J Exp Biol 209:2368–2376
Raeymaekers JAM, Boisjoly M, Delaire L, Berner D, Räsäene K, Hendry AP (2010) Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback. J Evol Biol 23:2694–2708
Ricciardi A, Rasmussen JB (1999) Extinction rates of North American freshwater fauna. Cons Biol 13:1220–1222
Rosenthal GG, De La Rosa Reyna XF, Kazianis S, Stephens MJ, Morizot DC, Ryan MJ, De Leon FJG (2003) Dissolution of sexual signal complexes in a hybrid zone between the swordtails Xiphophorus birchmanni and Xiphophorus malinche (Poeciliidae). Copeia 47:299–307
Rushbrook BJ, Head ML, Katsiadaki I, Barber I (2010) Flow regime affects building behavior and nest structure in sticklebacks. Behav Ecol Sociobiol 64:1927–1935
Schuster S (2006) Integration of the electrosense with other senses: implications for communication. In: Ladich F, Collin SP, Moller P, Kapoor BG (eds) Communication in fishes. Science Publishers, Enfield, pp 781–804
Schwartz AK, Hendry AP (2009) Testing the influence of local forest canopy clearing on phenotypic variation in Trinidadian guppies. Funct Ecol 24:354–364
Seehausen O, van Alphen JJM, Witte F (1997) Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277:1808–1811
Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, van der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N (2008) Speciation through sensory drive in cichlid fish. Nature 455:620–627
Shand J, Davies WL, Thomas N, Balmer L, Cowing JA, Pointer M, Carvalho LS, Trezise AEO, Collin SP, Beazley LD, Hunt DM (2008) The influence of ontogeny and light environment on the expression of visual pigment opsins in the retina of the black bream, Acanthopagrus butcheri. J Exp Biol 211:1495–1503
Sharpe DMT, Hendry AP (2009) Life history change in commercially exploited fish stocks: an analysis of trends across studies. Evol Appl 2:260–275
Siepeilski AM, DiBattista JD, Carlson SM (2009) It’s about time: the temporal dynamics of phenotypic selection in the wild. Ecol Lett 12:1261–1276
Silva A, Perrone R, Macadar O (2007) Environmental, seasonal, and social modulations of basal activity in a weakly electric fish. Physiol Behav 90:525–536
Simões JM, Fonseca PJ, Turner GF, Amorim MCP (2008) African cichlid Pseudotropheus spp. males moan to females during foreplay. J Fish Biol 72:2689–2694
Slabbekoorn H, Peet M (2003) Ecology: birds sing at a higher pitch in urban noise—great tits hit the high notes to ensure that their mating calls are heard above the city’s din. Nature 424:267
Slabbekoorn H, Bouton N, van Opzeeland I, Cours 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
Smadja C, Butlin RK (2009) On the scent of speciation: the chemosensory system and its role in pre mating isolation. Heredity 102:77–97
Smith AR, van Staaden MJ (2009) The association of visual and acoustic courtship behaviour in African cichlid fishes. Mar Freshw Behav Physiol 42:211–216
Sorensen PW, Stacey NE (2004) Brief review of fish pheromones and discussion of their possible uses in the control of non-indigenous teleost fishes. New Zeal J Mar Fresh 38:399–417
Squire A, Moller P (1982) Effects of water conductivity on electrocommunication in the weak-electric fish Brienomyrus niger (Mormyriformes). Anim Behav 30:375–382
Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trends Ecol Evol 18:94–101
Sullivan JP, Lavoue S, Hopkins CD (2002) Discovery and phylogenetic analysis of a riverine species flock of African electric fishes (Mormyridae: Teleostei). Evolution 56:597–616
Sullivan JP, Lavoue S, Arnegard ME, Hopkins CD (2004) AFLPs resolve phylogeny and reveal mitochondrial introgression within a species flock of African electric fish (Mormyroidea: Teleostei). Evolution 58:825–841
Svanback R, Pineda-Krch M, Doebeli M (2009) Fluctuating population dynamics promotes the evolution of phenotypic plasticity. Am Nat 174:176–189
Temple SE, Veldhoen KM, Phelan JT, Veldhoen NJ, Hawryshyn CW (2008) Ontogenetic changes in photoreceptor opsin gene expression in coho salmon (Oncorhynchus kisutch, Walbaum). J Exp Biol 211:3879–3888
Tierney KB, Singh CR, Ross PS, Kennedy CJ (2007) Relating olfactory neurotoxicity to altered olfactory-mediated behaviours in rainbow trout exposed to three currently-used pesticides. Aquat Toxicol 81:55–64
Tricas TC, Michael SW, Sisneros JA (1995) Electro sensory optimization to conspecic phasic signals for mating. Neurosci Lett 202:129–132
Utne-Palm AC (2002) Visual feeding of fish in a turbid environment: physical and behavioural aspects. Mar Freshw Behav Physiol 35:111–128
Vasconcelos RO, Amorim MCP, Ladich F (2007) Effects of ship noise on the detectability of communication signals in the Lusitanian toadfish. J Exp Biol 210:2104–2112
Wagner HJ (2007) Bipolar cells in the “grouped retina” of the elephantnose fish (Gnathonemus petersii). Visual Neurosci 24:355–362
Wagner HJ, Kroger RHH (2005) Adaptive plasticity during the development of colour vision. Prog Retin Eye Res 24:521–536
Ward AJW, Duff AJ, Horsfall JS, Currie S (2008) Scents and scents-ability: pollution disrupts chemical social recognition and shoaling in fish. Proc R Soc Lond Ser B-Biol Sci 275:101–105
Webster DR, Weissburg MJ (2009) The hydrodynamics of chemical cues among aquatic organisms. Annu Rev Fluid Mech 41:73–90
Winn HE (1964) The biological significance of fish sounds. In: Tavolga WN (ed) Marine bio-acoustics. Oxford, Pergamon Press, pp 213–230
Wong BBM, Fisher HS, Rosenthal GG (2005) Species recognition by male swordtails via chemical cues. Behav Ecol 16:818–822
Wong BBM, Candolin U, Lindstrom K (2007) Environmental deterioration compromises socially enforced signals of male quality in three-spined sticklebacks. Am Nat 170:184–189
Wysocki LE, Dittami JP, Ladich F (2006) Ship noise and cortisol secretion in European freshwater fishes. Biol Cons 128:501–508
Zakon H, Oestreich J, Tallarovic S, Triefenbach F (2002) EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips. J Physiology-Paris 96:451–458
Zala SM, Penn DJ (2004) Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. Anim Behav 68:649–664
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The authors thank the editor and referees for their constructive criticisms. We also thank Ole Seehausen, Jenny Boughman, and the Lauren Chapman lab for stimulating discussions. Further, SMG and IS would like to thank the Fisheries Society of the British Isles for funding. SMG was supported by a NSERC Postdoctoral Fellowship, and BBMW by the Australian Research Council.
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Inke van der Sluijs and Suzanne M. Gray contributed equally to the paper.
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van der Sluijs, I., Gray, S.M., Amorim, M.C.P. et al. Communication in troubled waters: responses of fish communication systems to changing environments. Evol Ecol 25, 623–640 (2011). https://doi.org/10.1007/s10682-010-9450-x
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DOI: https://doi.org/10.1007/s10682-010-9450-x