The African cichlid fish astatotilapia burtoni uses acoustic communication for reproduction: Sound production, hearing, and behavioral significance

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Maruska, Karen P ^a   Ung, Uyhun S ^a   Fernald, Russell D ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SEX HORMONE;

ACOUSTICS; AFRICA; ANIMAL COMMUNICATION; ANIMAL EXPERIMENT; ARTICLE; ASTATOTILAPIA BURTONI; AUDITORY THRESHOLD; CICHLID; CONTROLLED STUDY; COURTSHIP; EVOKED AUDITORY RESPONSE; FEMALE; MALE; MATE CHOICE; NOISE REDUCTION; NONHUMAN; PLASTICITY; REPRODUCTION; SEXUAL BEHAVIOR; SEXUAL SELECTION; SIGNAL DETECTION; SOCIAL STATUS; SOUND ANALYSIS; SOUND INTENSITY; SOUND TRANSMISSION; ANIMAL; BLOOD; BODY SIZE; HEARING; LAKE; PHYSIOLOGY; SEX DIFFERENCE; SOCIAL DOMINANCE; SOUND; STATISTICAL MODEL;

AFRICAN CICHLIDS; ANIMALIA; ASTATOTILAPIA BURTONI; CICHLIDAE; PISCES; VERTEBRATA;

AFRICA, EASTERN; ANIMAL COMMUNICATION; ANIMALS; AUDITORY THRESHOLD; BODY SIZE; CICHLIDS; EVOKED POTENTIALS, AUDITORY; FEMALE; GONADAL STEROID HORMONES; HEARING; LAKES; LINEAR MODELS; MALE; MATING PREFERENCE, ANIMAL; SEX FACTORS; SOCIAL DOMINANCE; SOUND;

EID: 84862107183     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037612     Document Type: Article

References (91)

1. Partan SR, Marler P, (1999) Communication goes multimodal. Science 283: 1272-1273.
2. Partan SR, Marler P, (2005) Issues in the classification of multimodal communication signals. The American Naturalist 166: 231-245.
3. Taylor RC, Klein BA, Stein J, Ryan MJ, (2011) Multimodal signal variation in space and time: how important is matching a signal with its signaler? J Exp Biol 214: 815-820.
4. Bradbury JW, Vehrencamp SL, (1998) Principles of Animal Communication Sunderland, MA Sinauer Associates, Inc.
5. Candolin U, (2003) The use of multiple cues in mate choice. Biol Rev Camb Philos Soc 78: 575-595.
6. Coleman SW, (2009) Taxonomic and sensory biases in the mate-choice literature: there are far too few studies of chemical and multimodal communication. Acta Ethol 12: 45-48.
7. Mclennan DA, (2003) The importance of olfactory signals in the gasterosteid mating system: sticklebacks go multimodal. Biol J Linnean Soc 80: 555-572.
8. Hankison SJ, Morris MR, (2003) Avoiding a compromise between sexual selection and species recognition: female swordtail fish assess multiple species-specific cues. Behav Ecol 14: 282-287.
9. Van Staaden MJ, Smith AR, (2011) Cutting the Gordian knot: complex signaling in African cichlids is more than multimodal. Curr Zool 57: 237-252.
10. Sturmbauer C, Husemann M, Danley PD, (2011) Explosive speciation and adaptive radiation of East African cichlid fishes. In: Zachos FE, Habel JC, editors. Biodiversity hotspots Berlin Springer-Verlag pp. 333-362.
11. Turner GF, (1999) Explosive speciation of African cichlid fishes. In: Magurran AE, May RM, editors. Evolution of Biological Diversity Oxford Oxford University Press pp. 217-229.
12. Salzburger W, Niederstatter H, Brandstatter A, Berger B, Parson W, et al. (2006) Colour-assortative mating among populations of Tropheus moorii, a cichlid fish from Lake Tanganyika, East Africa. Proc Biol Sci 273: 257-266.
13. Hofmann CM, O'Quin KE, Marshall NJ, Cronin TW, Seehausen O, et al. (2009) The eyes have it: regulatory and structural changes both underlie cichlid visual pigment diversity. PLoS Biol 7: e1000266.
14. Maan ME, Hofker KD, van Alphen JJ, Seehausen O, (2006) Sensory drive in cichlid speciation. Am Nat 167.
15. Egger B, Klaefiger Y, Theis A, Salzburger W, (2011) A sensory bias has triggered the evolution of egg-spots in cichlid fishes. PLoS One 6: e25601.
16. Lehtonen TK, Meyer A, (2011) Heritability and adaptive significance of the number of egg-dummies in the cichlid fish Astatotilapia burtoni. Proc Biol Sci 278: 2318-2324.
17. 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.
18. Blais J, Plenderleith M, Rico C, Taylor MI, Seehausen O, et al. (2009) Assortative mating among Lake Malawi cichlid fish populations is not simply predictable from male nuptial colour. BMC Evol Biol 9: 53.
19. Lobel PS, (1998) Possible species specific courtship sounds by two sympatric cichlid fishes in Lake Malawi, Africa. Environmental Biology of Fishes 52: 443-452.
20. Danley PD, Husemann M, Chetta J, (2011) Acoustic diversity in Lake Malawi's rock-dwelling cichlids. Environ Biol Fish.
21. Amorim M, (2006) Diversity of sound production. In: Ladich F, Collin SP, Moller P, Kapoor BG, editors. Communication in Fishes Enfield, N.H. Science Publishers pp. 71-105.
22. Lobel PS, (2001) Acoustic behavior of cichlid fishes. Journal of Aquariculture and Aquatic Sciences IX: 167-185.
23. Nelissen MHJ, (1978) Sound production by some Tanganyikan cichlid fishes and a hypothesis for the evolution of their communication mechanisms. Behaviour LXIV1-2: 137-147.
24. Amorim MCP, Fonseca PJ, Almada VC, (2003) Sound production during courtship and spawning of Oreochromis mossambicus: male-female and male-male interactions. Journal of Fish Biology 62: 658-672.
25. Verzijden MN, van Heusden J, Bouton N, Witte F, ten Cate C, et al. (2010) Sounds of Lake Victoria cichlids vary within and between species and affect female mate preferences. Behav Ecol 21.
26. Sisneros JA, Forlano PM, Deitcher DL, Bass AH, (2004) Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305: 404-407.
27. Al-Mana D, Ceranic B, Djahanbakhch O, Luxon LM, (2008) Hormones and the auditory system: a review of physiology and pathophysiology. Neuroscience 153: 881-900.
28. Maruska KP, Tricas TC, (2011) Gonadotropin-releasing hormone (GnRH) modulates auditory processing in the fish brain. Horm Behav 59: 451-464.
29. Arch VS, Narins PM, (2009) Sexual hearing: The influence of sex hormones on acoustic communication in frogs. Hear Res.
30. Tremere LA, Pinaud R, (2011) Brain-generated estradiol drives long-term optimization of auditory coding to enhance the discrimination of communication signals. J Neurosci 31: 3271-3289.
31. Canlon B, Meltser I, Johansson P, Tahera Y, (2007) Glucocorticoid receptors modulate auditory sensitivity to acoustic trauma. Hear Res 226: 61-69.
32. Fernald RD, Hirata NR, (1977) Field study of Haplochromis burtoni: quantitative behavioral observations. Animal Behavior 25: 964-975.
33. Fernald RD, (2009) Social regulation of reproduction: what changes and why? Hormones, Brain and Behavior 1: 683-691.
34. Maruska KP, Fernald RD, (2011) Social regulation of gene expression in the hypothalamic-pituitary-gonadal axis. Physiology 26: 412-423.
35. Renn SC, Carleton JB, Magee H, Nguyen ML, Tanner AC, (2009) Maternal care and altered social phenotype in a recently collected stock of Astatotilapia burtoni cichlid fish. Integr Comp Biol 49: 660-673.
36. White SA, Fernald RD, (1993) Gonadotropin-releasing hormone-containing neurons change size with reproductive state in female Haplochromis burtoni. J Neurosci 13: 434-441.
37. Heiligenberg W, Kramer U, Schulz V, (1972) The angular orientation of the black eye-bar in Haplochromis burtoni (Cichlidae, Pisces) and its relevance for aggressivity. Z Vergl Physiol 76: 168-176.
38. Maruska KP, Fernald RD, (2012) Contextual chemosensory urine signaling in an African cichlid fish. J Exp Biol 215: 68-74.
39. Maruska KP, Fernald RD, (2010) Steroid receptor expression in the fish inner ear varies with sex, social status, and reproductive state. BMC Neurosci 11: 58.
40. Nelissen MHJ, (1977) Sound production by Haplochromis burtoni (Gunther) and Tropheus moorii Boulenger (Pisces, Cichlidae). Annales Soc R Zool Belg 106: 155-166.
41. Crapon de Caprona MD, (1980) Olfactory communication in a cichlid fish, Haplochromis burtoni. Z Tierpsychol 52: 113-134.
42. Hirata NR, Fernald RD, (1975) Non-intentional sound production in a Cichlid fish (Haplochromis burtoni, Gunther). Experientia 31: 299-300.
43. Maruska KP, Fernald RD, (2010) Behavioral and physiological plasticity: Rapid changes during social ascent in an African cichlid fish. Horm Behav 58: 230-240.
44. Fernald RD, (1977) Quantitative behavioral observations of Haplochromis burtoni under semi-natural conditions. Animal Behavior 25: 643-653.
45. Kenyon T, Ladich F, Yan HY, (1998) A Comparative Study of Hearing Ability in Fishes: The Auditory Brainstem Response Approach. Journal of Comparative Physiology A 182: 307-318.
46. Maruska KP, Boyle KS, Dewan LR, Tricas TC, (2007) Sound production and spectral hearing sensitivity in the Hawaiian sergeant damselfish, Abudefduf abdominalis. Journal of Experimental Biology 210: 3990-4004.
47. Horodysky AZ, Brill RW, Fine ML, Musick JA, Latour RJ, (2008) Acoustic pressure and particle motion thresholds in six sciaenid fishes. J Exp Biol 211: 1504-1511.
48. Ripley JL, Lobel PS, Yan HY, (2002) Correlation of sound production with hearing sensitivity in the Lake Malawi cichlid Tramitichromis intermedius. Bioacoustics 12: 238-240.
49. Wysocki LE, Codarin A, Ladich F, Picciulin M, (2009) Sound pressure and particle acceleration audiograms in three marine fish species from the Adriatic Sea. J Acoust Soc Am 126: 2100-2107.
50. Lechner W, Heiss E, Schwaha T, Glosmann M, Ladich F, (2011) Ontogenetic development of weberian ossicles and hearing abilities in the African bullhead catfish. PLoS One 6: e18511.
51. Mann DA, Higgs DM, Tavolga WN, Souza MJ, Popper AN, (2001) Ultrasound detection by clupeiform fishes. Journal of Acoustical Society of America 109: 3048-3054.
52. Davidson J, Frankel AS, Ellison WT, Summerfelt S, Popper AN, et al. (2007) Minimizing noise in fiberglass aquaculture tanks: noise reduction potential of various retrofits. Aquacultural Engineering 37: 125-131.
53. Fay RR, (1974) Sound reception and processing in the carp: Saccular potentials. Comp Biochem Physiol 46: 29-42.
54. Akamatsu T, Okumura T, Novarini N, Yan HY, (2002) Empirical refinements applicable to the recording of fish sounds in small tanks. Journal of Acoustical Society of America 112: 3073-3082.
55. Myrberg AA Jr, Lugli M, (2006) Reproductive behavior and acoustical interactions. In: Ladich F, Collin SP, Moller P, Kapoor BG, editors. Communication in Fishes, Volume 1 Enfield, N.H. Science Publishers pp. 149-176.
56. Amorim MCP, Knight ME, Stratoudakis Y, Turner GF, (2004) Differences in sounds made by courting males of three closely related Lake Malawi cichlid species. Journal of Fish Biology 65: 1358-1371.
57. Rice AN, Lobel PS, (2003) The pharyngeal jaw apparatus of the Cichlidae and Pomacentridae: function in feeding and sound production. Reviews in Fish Biology and Fisheries 13: 433-444.
58. Longrie N, Van Wassenbergh S, Vandewalle P, Mauguit Q, Parmentier E, (2009) Potential mechanism of sound production in Oreochromis niloticus (Cichlidae). J Exp Biol 212: 3395-3402.
59. Simoes JM, Duarte IG, Fonseca PJ, Turner GF, Amorim MC, (2008) Courtship and agonistic sounds by the cichlid fish Pseudotropheus zebra. J Acoust Soc Am 124.
60. Ripley JL, Lobel PS, (2004) Correlation of acoustic and visual signals in the cichlid fish Tramitichromis intermedius. Environ Biol Fish 71: 389-394.
61. Myrberg AA Jr, Kramer E, Heinecke P, (1965) Sound production by cichlid fishes. Science 149: 555-558.
62. Longrie N, Fine ML, Parmentier E, (2008) Innate sound production in the cichlid Oreochromis niloticus. J Zool (London) 275: 413-417.
63. Yan HY, Popper AN, (1992) Auditory sensitivity of the cichlid fish Astronotus ocellatus (Cuvier). J Comp Physiol A 171: 105-109.
64. Kenyon TN, Ladich F, Yan HY, (1998) A comparative study of hearing ability in fishes: the auditory brainstem response approach. Journal of Comparative Physiology [A] 182: 307-318.
65. Tavolga WN, (1974) Signal/noise ratio and the critical band in fishes. J Acoust Soc Am 55: 1323-1333.
66. Fay RR, Popper AN, (1975) Modes of stimulation of the teleost ear. J Exp Biol 62: 370-387.
67. Ladich F, Wysocki LE, (2003) How does tripus extirpation affect auditory sensitivity in goldfish? Hear Res 182: 119-129.
68. Smith ME, Kane AS, Popper AN, (2004) Acoustical stress and hearing sensitivity in fishes: does the linear threshold shift hypothesis hold water? J Exp Biol 207: 3591-3602.
69. Wysocki LE, (2006) Detection of communication sounds. In: Ladich F, Collin SP, Moller P, Kapoor BG, editors. Communication in Fishes, Volume 1 Enfield Science Publishers pp. 177-205.
70. Schellart NAM, Popper AN, (1992) Functional aspects of the evolution of the auditory system of Actinopterygian fish. In: Webster DB, Fay RR, Popper AN, editors. The Evolutionary Biology of Hearing New York Springer Verlag pp. 295-322.
71. Fay RR, Simmons AM, (1999) The sense of hearing in fishes and amphibians. In: Fay RR, Popper AN, editors. Comparative hearing: fish and amphibians New York Springer pp. 269-318.
72. Maruska KP, Tricas TC, (2009) Encoding properties of auditory neurons in the brain of a soniferous damselfish: response to simple tones and complex conspecific signals. J Comp Physiol A Neuroethol Sens Neural Behav Physiol.
73. Rohmann KN, Bass AH, (2011) Seasonal plasticity of auditory hair cell frequency sensitivity correlates with plasma steroid levels in vocal fish. J Exp Biol 214: 1931-1942.
74. Sisneros JA, Bass AH, (2003) Seasonal plasticity of peripheral auditory frequency sensitivity. J Neurosci 23: 1049-1058.
75. Corwin JT, (1983) Postembryonic growth of the macula neglecta auditory detector in the ray, Raja clavata: continual increases in hair cell number, neural convergence, and physiological sensitivity. J Comp Neurol 217: 345-356.
76. Hultcrantz M, Simonoska R, Stenberg AE, (2006) Estrogen and hearing: a summary of recent investigatiosn. Acta Oto-Laryngologica 126: 10-14.
77. Kustan JM, Maruska KP, Fernald RD, (2011) Subordinate male cichlids retain reproductive competence during social suppression. Proc R Soc B.
78. McKibben JR, Bass A, (1998) Behavioral assessment of acoustic parameters relevant to signal recognition and preference in a vocal fish. Journal of Acoustical Society of America 104: 3520-3533.
79. Simoes JM, Duarte IG, Fonseca PJ, (2008) Courtship and agonistic sounds by the cichlid fish Pseudotropheus zebra. J Acoust Soc Am 124: 1332-1338.
80. Gerhardt HC, Tanner SD, Corrigan CM, Walton HC, (2000) Female preference functions based on call duration in the gray tree frog (Hyla versicolor). Behav Ecol 11: 663-669.
81. Araya-Ajoy YM, Chaves-Campos J, Kalko EK, Dewoody JA, (2009) High-pitched notes during vocal contests signal genetic diversity in ocellated antbirds. PLoS One 4: e8137.
82. Scheuber H, Jacot A, Brinkhof MW, (2004) Female preference for multiple condition-dependent components of a sexually selected signal. Proc Biol Sci 271: 2453-2457.
83. Magrath RD, Bennett TH, (2011) A micro-geography of fear: learning to eavesdrop on alarm calls of neighbouring heterospecifics. Proc Biol Sci.
84. Page RA, Ryan MJ, (2005) Flexibility in assessment of prey cues: frog-eating bats and frog calls. Proc Biol Sci 272: 841-847.
85. Amy M, Leboucher G, (2009) Effects of eavesdropping on subsequent signalling behaviors in male canaries. Ethology 115: 239-246.
86. Clement TS, Grens KE, Fernald RD, (2005) Female affiliative preference depends on reproductive state in the African cichlid fish, Astatotilapia burtoni. Behav Ecol 16: 83-88.
87. Crapon de Caprona MD, (1974) The effect of chemical stimuli from conspecifics on the behavior of Haplochromis burtoni (Cichlidae, Pisces) Experientia 30: 1394-1395.
88. Maruska KP, Fernald RD, (2010) Reproductive status regulates expression of sex steroid and GnRH receptors in the olfactory bulb. Behav Brain Res 213: 208-217.
89. Nosil P, Harmon LJ, Seehausen O, (2009) Ecological explanations for (incomplete) speciation. Trends Ecol Evol 24: 145-156.
90. Nosil P, Harmon LJ, (2009) Niche dimensionality and ecological speciation. In: Butlin R, Bridle J, Schluter D, editors. Speciation and patterns of diversity Cambridge Cambridge University Press pp. 127-154.
91. Greenwood PH, (1984) African cichlids and evolutionary theories. In: Echelle AA, Kornfield I, editors. Evolution of fish species flocks Orono, Maine University of Maine at Orono Press pp. 141-155.