Feeding in the dark: Lateral-line-mediated prey detection in the peacock cichlid Aulonocara stuartgranti

Journal of Experimental Biology

Volumn 215, Issue 12, 2012, Pages 2060-2071

  Schwalbe, Margot A B ^a   Bassett, Daniel K ^a,b   Webb, Jacqueline F ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

^b MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

Cichlid; Lateral line; Neuromast; Prey detection

Indexed keywords

COBALT; COBALT CHLORIDE;

ANIMAL; ARTICLE; CICHLID; HISTOLOGY; HYDRODYNAMICS; LIGHT; MECHANORECEPTOR; METABOLISM; PHYSIOLOGY; PREDATION;

ANIMALS; CICHLIDS; COBALT; HYDRODYNAMICS; LIGHT; MECHANORECEPTORS; PREDATORY BEHAVIOR;

EID: 84862562803     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.065920     Document Type: Article

References (85)

1. Albertson, R. C., Streelman, J. T., Kocher, T. D. and Yelick, P. C. (2005). Integration and evolution of the cichlid mandible: molecular basis of alternate feeding strategies. Proc. Natl. Acad. Sci. USA 102, 16287-16292. (Pubitemid 41688906)
2. Bassett, D. K. (2008). Predatory behaviour of nocturnal reef fish. PhD dissertation, University of Auckland.
3. Bassett, D. K. and Montgomery, J. C. (2011). The feeding response of Pseudophycas barbata to multisensory prey cues in a low light environment. J. Fish Biol. 79, 526-532.
4. Bassett, D. K., Carton, A. G. and Montogmery, J. C. (2006). Flowing water decreases hydrodynamic signal detection in a fish with an epidermal lateral-line system. Mar. Freshw. Res. 57, 611-617. (Pubitemid 44357691)
5. Bassett, D. K., Carton, A. G. and Montgomery, J. C. (2007). Saltatory search in a lateral line predator. J. Fish Biol. 70, 1148-1160. (Pubitemid 46606762)
6. Bergman, E. (1991). Changes in abundance of two percids, Perca fluviatilis and Gymnocephalus cernuus, along a productivity gradient: relations to feeding strategies and competitive abilities. Can. J. Fish. Aquat. Sci. 48, 536-545.
7. Bergstrom, M. A. and Mensinger, A. F. (2009). Interspecific resource competition between the invasive round goby and three native species: logperch, slimy sculpin, and spoonhead sculpin. Trans. Am. Fish. Soc. 138, 1009-1017.
8. Blaxter, J. H. S. (1988). Sensory performance, behavior and ecology of fish. In Sensory Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp. 203-232. New York: Springer-Verlag.
9. Brown, A. D., Mussen, T. D., Sisneros, J. A. and Coffin, A. B. (2011). Reevaluating the use of aminoglycoside antibiotics in behavioral studies of the lateral line. Hearing Res. 272, 1-4.
10. Carleton, K. L. (2009). Cichlid fish visual systems: mechanisms of spectral tuning. Integr. Zool. 4, 75-86.
11. Carleton, K. L., Spady, T. C. and Kocher, T. D. (2006). Visual communication in East African cichlid fishes. In Communication in Fishes (ed. F. Ladich, S. P. Collin, P. Moller and B. G. Kapoor), pp. 485-515. Enfield, NH: Science Publisher Inc.
12. Coombs, S. (1994). Nearfield detection of dipole sources by the goldfish (Carassius auratus) and the mottled sculpin (Cottus bairdi). J. Exp. Biol. 190, 109-129. (Pubitemid 2076402)
13. Coombs, S. (1999). Signal detection theory, lateral-line excitation patterns and prey capture behaviour of mottled sculpin. Anim. Behav. 58, 421-430. (Pubitemid 29400932)
14. Coombs, S. and Conley, R. A. (1997). Dipole source localization by mottled sculpin, I. Approach strategies. J. Comp. Physiol. A 180, 387-399. (Pubitemid 27161761)
15. Coombs, S. and Janssen, J. (1990). Behavioral and neurophysiological assessment of lateral line sensitivity in the mottled sculpin, Cottus bairdi. J. Comp. Physiol. A 167, 557-567. (Pubitemid 20329606)
16. Coombs, S. and Montgomery, J. C. (1999). The enigmatic lateral line system. In Comparative Hearing: Fish and Amphibians (ed. R. R. Fay and A. N. Popper), pp. 319-362. New York: Springer-Verlag.
17. Coombs, S. and Patton, P. (2009). Lateral line stimulation patterns and prey orienting behavior in the Lake Michigan mottled sculpin (Cottus bairdi). J. Comp. Physiol. A 195, 279-297.
18. Coombs, S. and van Netten, S. (2006). The hydrodynamics and structural mechanics of the lateral line system. In Fish Biomechanics (ed. R. E. Shadwick and G. V. Lauder), pp. 103-139. San Diego, CA: Elsevier Academic Press.
19. Coombs, S., Janssen, J. and Webb, J. F. (1988). Diversity of lateral line systems: evolutionary and functional considerations. In Sensory Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp. 553-593. New York: Springer-Verlag.
20. Coombs, S., Janssen, J. and Montgomery, J. (1992). Functional and evolutionary implications of peripheral diversity in lateral line systems. In The Evolutionary Biology of Hearing (ed. D. B. Webster, R. R. Fay and A. N. Popper), pp. 267-294. New York: Springer-Verlag.
21. Coombs, S., Braun, C. and Donovan, B. (2001). The orienting response of Lake Michigan mottled sculpin is mediated by canal neuromasts. J. Exp. Biol. 204, 337-348. (Pubitemid 32116909)
22. Couldridge, V. C. K. and Alexander, G. J. (2002). Colour patterns and species recognition in four closely related species of Lake Malawi cichlids. Behav. Ecol. 13, 59-64. (Pubitemid 34134629)
23. Ćurčić-Blake, B. and van Netten, S. M. (2006). Source location encoding in the fish lateral line canal. J. Exp. Biol. 209, 1548-1559.
24. Denton, E. J. and Gray, J. A. B. (1988). Mechanical factors in the excitation of the lateral lines of fish. In Sensory Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp. 595-617. New York: Springer-Verlag.
25. Denton, E. J. and Gray, J. A. B. (1989). Some observations on the forces acting on neuromasts in fish lateral line canals. In The Mechanosensory Lateral Line: Neurobiology and Evolution (ed. S. Coombs, P. Gorner and H. Münz), pp. 229-246. New York: Springer-Verlag.
26. Engelmann, J., Hanke, W., Mogdans, J. and Bleckmann, H. (2000). Hydrodynamic stimuli and the fish lateral line. Nature 408, 51-52.
27. Engelmann, J., Hanke, W. and Bleckmann, H. (2002). Lateral line reception in stilland running water. J. Comp. Physiol. A 188, 513-526. (Pubitemid 36251063)
28. Evans, B. I. (2004). A fish's eye view of habitat change. In The Senses of Fish Adaptations for the Reception of Natural Stimuli (ed. G. von der Emde, J. Mogdans and B. G. Kapoor), pp. 1-30. Boston, MA: Kluwer Academic Publisher.
29. Fernald, R. D. and Liebman, P. A. (1980). Visual receptor pigments in the African cichlid fish, Haplochromis burtoni. Vision Res. 20, 857-864. (Pubitemid 10007705)
30. Fryer, G. (1959). The trophic interrelationships and ecology of some littoral communities of Lake Nyasa with especial reference to the fishes, and a discussion of the evolution of a group of rock-frequenting Cichlidae. Proc. Zool. Soc. Lond. 132, 153-281.
31. Fryer, G. and Iles, T. D. (1972). The Cichlid Fishes of the Great Lakes of Africa: Their Biology and Evolution. Edinburgh: Oliver and Boyd.
32. Gardiner, J. M. and Atema, J. (2007). Sharks need the lateral line to locate odor sources: rheotaxis and eddy chemotaxis. J. Exp. Biol. 210, 1925-1934. (Pubitemid 46998737)
33. Grant, S. M., Dieckhoff, H. W., Mayland, H. J. and Meyer, M. K. (1987). Ecology of Aulonocara Regan, 1922 in Lake Malawi. Cour. Forsch.-Inst. Senckenberg 94, 131-139.
34. Gray, J. A. B. and Best, A. C. G. (1989). Patterns of excitation of the lateral line of the ruffe. J. Mar. Biol. Assoc. UK 69, 289-306.
35. Greenwood, P. H. (1981). The Haplochromine Fishes of the East African Lakes. Ithaca, NY: Cornell University Press.
36. Guthrie, D. M. and Muntz, W. R. A. (1993). Role of vision in fish behaviour. In Behaviour of Teleost Fishes, 2nd edn (ed. T. Pitcher), pp. 89-128. London: Chapman and Hall.
37. Hara. T. (1993). Role of olfaction in fish behavior. In Behaviour of Teleost Fishes, 2nd edn (ed. T. J. Pitcher), pp. 171-200. London: Chapman and Hall.
38. Helfman, G. S. (1993). Fish behaviour by day, night and twilight. In Behaviour of Teleost Fishes, 2nd edn (ed T. J. Pitcher), pp. 479-512. London: Chapman and Hall.
39. Hoekstra, D. and Janssen, J. (1985). Non-visual feeding behavior of the mottled sculpin, Cottus bairdi, in Lake Michigan. Environ. Biol. Fish. 12, 111-117. (Pubitemid 16275053)
40. Hoekstra, D. and Janssen, J. (1986). Lateral line receptivity in the mottled sculpin (Cottus bairdi). Copeia 1986, 91-96.
41. Holland, K. (1978). Chemosensory orientation to food by a Hawaiian goatfish (Parupeneus porphyreus, Mullidae). J. Chem. Ecol. 4, 173-186.
42. Janssen, J. (1997). Comparison of response distance to prey via the lateral line in the ruffe and yellow perch. J. Fish Biol. 51, 921-930. (Pubitemid 27503124)
43. 2+: implications for lateral line studies. J. Comp. Physiol. A 186, 957-960.
44. Kalmijn, A. J. (1988). Hydrodynamic and acoustic field detection. In Sensory Biology of Aquatic Animals (ed. J. Atema, R. R. Fay, A. N. Popper and W. N. Tavolga), pp. 83-130. New York: Springer-Verlag.
45. Kanter, M. and Coombs, S. (2003). Rheotaxis and prey detection in uniform currents by Lake Michigan mottled sculpin (Cottus bairdi). J. Exp. Biol. 206, 59-70. (Pubitemid 36108150)
46. Karlsen, H. E. and Sand, O. (1987). Selective and reversible blocking of the lateral line in freshwater fish. J. Exp. Biol. 133, 249-262.
47. Konings, A. (1990). Koning's Book of Cichlids and Other Fishes of Lake Malawi. Neptune City, NJ: TFH Publications Inc.
48. Konings, A. (2007). Malawi Cichlids in Their Natural Habitat, 4th edn. El Paso, TX: Cichlid Press.
49. Liao, J. (2006). The role of the lateral line and vision on body kinematics and hydrodynamic preference of rainbow trout in turbulent flow. J. Exp. Biol. 209, 4077-4090. (Pubitemid 44769377)
50. Livingston, M. E. (1987). Morphological and sensory specializations of five New Zealand flatfish species, in relation to feeding behaviour. J. Fish Biol. 31, 775-795.
51. MacIver, M. A., Sharabash, N. M. and Nelson, M. E. (2001). Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. J. Exp. Biol. 204, 543-557. (Pubitemid 32176980)
52. Marshall, N. J. (1996). The lateral line system of three deep-sea fish. J. Fish Biol. 49 Suppl. A, 239-258. (Pubitemid 27093624)
53. Meyer, M. K., Riehl, R. and Zetzsche, H. (1987). A revision of the cichlid fishes of the genus Aulonocara Regan, 1922 from Lake Malawi, with descriptions of six new species (Pisces, Perciformes, Cichlidae). Cour. Forsch.-Inst. Senckenberg 94, 7-53.
54. Mogdans, J. and Nauroth, I. E. (2011). The oscar, Astronotus ocellatus, detects and discriminates dipole stimuli with the lateral line system. J. Comp. Physiol. A 197, 959-968.
55. Montgomery, J. C., Baker, C. F. and Carton, A. G. (1997). The lateral line can mediate rheotaxis in fish. Nature 389, 960-963. (Pubitemid 27485685)
56. New, J. (2002). Multimodal integration in the feeding behaviors of predatory teleost fishes. Brain Behav. Evol. 59, 177-189. (Pubitemid 34914027)
57. O'Brien, W. J., Evans, B. I. and Browman, H. I. (1989). Flexible search tactics and efficient foraging in saltatory searching animals. Oecologia 80, 100-110. (Pubitemid 20425986)
58. O'Quin, K. E., Smith, A. R., Sharma, A. and Carleton, K. L. (2011). New evidence for the role of heterochrony in the repeated evolution of cichlid opsin expression. Evol. Dev. 13, 193-203.
59. Ogle, D. H., Selgeby, J. H., Newman, R. M. and Henry, M. G. (1995). Diet and feeding periodicity of the ruffe in the St. Louis River estuary, Lake Superior. Trans. Am. Fish. Soc. 124, 356-369. (Pubitemid 26452159)
60. Palmer, L. M., Deffenbaugh, M. and Mensinger, A. F. (2005). Sensitivity of the anterior lateral line to natural stimuli in the oyster toadfish, Opsanus tau (Linnaeus). J. Exp. Biol. 208, 3441-3450. (Pubitemid 41463266)
61. Patton, P., Windsor, S. and Coombs, S. (2010). Active wall following by Mexican blind cave fish. J. Comp. Physiol. A 196, 853-867.
62. Phillips, R. R. and Swears, S. B. (1979). Social hierarchy, shelter use, and avoidance of predatory toadfish (Opsanus tau) by the striped blenny (Chasmodes bosquianus). Anim. Behav. 27, 1113-1121.
63. Price, N. N. and Mensinger, A. F. (1999). Predator-prey interactions of juvenile toadfish, Opsanus tau. Biol. Bull. 197, 246-247. (Pubitemid 29530561)
64. Reno, H. W. (1966). The infraorbital canal, its lateral-line ossicles and neuromasts, in the minnows Notropis volucellus and N. buchanani. Copeia 1966, 403-413.
65. Reno, H. W. (1971). The lateral-line system of the silverjaw minnow, Ericymba buccata Cope. Southwest Nat. 15, 347-358.
66. Richmond, H. E., Hrabik, T. R. and Mensinger, A. F. (2004). Light intensity, prey detection and foraging mechanisms of age 0 year yellow perch. J. Fish Biol. 65, 195-205. (Pubitemid 39040127)
67. Sand, O. and Bleckmann, H. (2008). Orientation to auditory and lateral line stimuli. In Fish Bioacoustics (ed. J. F. Webb, R. R. Fay and A. N. Popper), pp. 183-232. New York: Springer-Verlag.
68. Santos, F., MacDonald, G., Rubel, E. W. and Raible, D. W. (2006). Lateral line hair cell maturation is a determinant of aminoglycoside susceptibility in zebrafish (Danio rerio). Hearing Res. 213, 25-33. (Pubitemid 43356625)
69. Schleuter, D. and Eckmann, R. (2006). Competition between perch (Perca fluviatilis) and ruffe (Gymnocephalus cernuus): the advantage of turning night into day. Freshwater Biol. 51, 287-297.
70. Schwarz, J. S., Reichenbach, T. and Hudspeth, A. J. (2011). A hydrodynamic sensory antenna used by killifish for nocturnal hunting. J. Exp. Biol. 214, 1857-1866.
71. Seehausen, O. and van Alphen, J. J. M. (1998). The effect of male coloration on female mate choice in closely related Lake Victoria cichlids (Haplochromis hyererei complex). Behav. Ecol. Sociobiol. 42, 1-8. (Pubitemid 28189726)
72. Seehausen, O., Terai, Y., Magalhae, I. S., Carleton, K. L., Mrosso, H. D. J., Miyagi, R., van der Sluijs, I., Schneider, M. V., Maan, M. E., Tachida, H., Imai, H. and Okada, N. (2008). Speciation through sensory drive in cichlid fish. Nature 455, 620-627.
73. Song, J., Hong, Y. Y. and Popper, A. N. (1995). Damage and recovery of hair cells in fish canal (but not superficial) neuromasts after gentamicin exposure. Hearing Res. 91, 63-71. (Pubitemid 26046854)
74. Taplin, R. H. (2007). Experimental design and analysis to investigate predator preferences for prey. J. Mar. Biol. Ecol. 344, 116-122. (Pubitemid 46441194)
75. Trewavas, E. (1983). Tilapiine Fishes of the Genera Sarotherodon, Oreochromis, and Danakilia. London: British Museum (Natural History).
76. van Netten, S. M. and van Maarseveen, J. T. P. (1994). Mechanophysiological properties of the supraorbital lateral line canal in ruffe (Acerina cernua). Proc. R. Soc. Lond. B 256, 239-246. (Pubitemid 24209618)
77. Van Trump, W. J., Coombs, S., Duncon, K. and McHenry, M. J. (2010). Gentamicin is ototoxic to all hair cells in the fish lateral line system. Hearing Res. 261, 42-50.
78. Vinyard, G. L. and O'Brien, W. J. (1976). Effects of light and turbidity on the reactive distance of bluegill (Lepomis macrochirus). J. Fish. Res. Board Can. 33, 2845-2849.
79. Von der Emde, G. and Bleckmann, H. (1998). Finding food: senses involved in foraging for insect larvae in the electric fish Gnathonemus petersii. J. Exp. Biol. 201, 969-980. (Pubitemid 28203143)
80. Wallace, D. C. (1976). Feeding behavior and developmental, seasonal and diel changes in the food of the silverjaw minnow, Ericymba buccata Cope. Am. Midl. Nat. 95, 361-376.
81. Webb, J. F. (1989). Gross morphology and evolution of the mechanosensory lateral line system in teleost fishes. Brain Behav. Evol. 33, 34-53. (Pubitemid 19097508)
82. Webb, J. F. (1995). How do asymmetric cranial bones develop in the flatfish, Glyptocephalus zachirus? Am. Zool. 35, 106A.
83. Webb, J. F., Montgomery, J. C. and Mogdans, J. (2008). Bioacoustics and the lateral line system of fishes. In Fish Bioacoustics (ed. J. F. Webb, A. N. Popper and R. R. Fay), pp. 145-182. New York: Springer-Verlag.
84. Yoshii, K. and Kurihara, K. (1983). Role of cations in olfactory reception. Brain Res. 274, 239-248. (Pubitemid 13047064)
85. Yoshizawa, M., Gorički, S., Soares, D. and Jeffery, W. R. (2010). Evolution of a behavioral shift mediated by superficial neuromasts helps cavefish find food in darkness. Curr. Biol. 20, 1631-1636.