Behaviour drives morphology: Voluntary emersion patterns shape gill structure in genetically identical mangrove rivulus

Animal Behaviour

Volumn 82, Issue 1, 2011, Pages 39-47

  Turko, A J ^a   Earley, R L ^b   Wright, P A ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF ALABAMA   (United States)

Author keywords

Amphibious fish; Gill lamellae; Phenotypic plasticity; Rivulus

Indexed keywords

ADAPTATION; CYPRINID; EVOLUTIONARY BIOLOGY; HYPOTHESIS TESTING; MARINE ECOSYSTEM; MORPHOLOGY; PHENOTYPIC PLASTICITY; SKIN; SURFACE AREA; VOLUNTARY APPROACH;

KRYPTOLEBIAS MARMORATUS; RIVULUS;

EID: 79958784149     PISSN: 00033472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anbehav.2011.03.001     Document Type: Article

References (56)

1. Abel D.C., Koenig C.C., Davis W.P. Emersion in the mangrove forest fish Rivulus marmoratus: a unique response to hydrogen sulfide. Environmental Biology of Fishes 1987, 18:67-72.
2. Auld J.R., Agrawal A.A., Relyea R.A. Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proceedings of the Royal Society B 2010, 277:503-511. 10.1098/rspb.2009.1355.
3. Bolnick D.I., Svanback R., Fordyce J.A., Yang L.H., Davis J.M., Hulsey C.D., Forister M.L. The ecology of individuals: incidence and implications of individual specialization. American Naturalist 2003, 161:1-28.
4. Browman H.I. Embryology, ethology and ecology of ontogenetic critical periods in fish. Brain, Behavior, and Evolution 1989, 34:5-12. 10.1159/000116486.
5. Chapman B.B., Morrell L.J., Benton T.G., Krause J. Early interactions with adults mediate the development of predator defenses in guppies. Behavioral Ecology 2008, 19:87-93. 10.1093/beheco/arm111.
6. Costa W., Lima S., Bartolette R. Androdioecy in Kryptolebias killifish and the evolution of self-fertilizing hermaphroditism. Biological Journal of the Linnean Society 2010, 99:344-349. 10.1111/j.1095-8312.2009.01359.x.
7. Darwin C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life 1859, J. Murray, London.
8. Davis W.P., Taylor D.S., Turner B.J. Field observations of the ecology and habits of mangrove rivulus (Rivulus marmoratus) in Belize and Florida. Ichthyological Explorations of Freshwaters 1990, 1:123-134.
9. DeWitt T.J., Scheiner S.M. Phenotypic Plasticity: Functional and Conceptual Approaches 2004, Oxford University Press, New York.
10. DeWitt T.J., Sih A., Wilson D.S. Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution 1998, 13:77-81.
11. Dunson W.A., Dunson D.B. Factors influencing growth and survival of the killifish, Rivulus marmoratus, held inside enclosures in mangrove swamps. Copeia 1999, 1999:661-668.
12. Frick N.T., Wright P.A. Nitrogen metabolism and excretion in the mangrove killifish, Rivulus marmoratus. I. The influence of environmental salinity and external ammonia. Journal of Experimental Biology 2002, 205:79-89.
13. Frick N.T., Wright P.A. Nitrogen metabolism and excretion in the mangrove killifish Rivulus marmoratus II. Significant ammonia volatilization in a teleost during air-exposure. Journal of Experimental Biology 2002, 205:91-100.
14. Ghalambor C.K., Angeloni L.M., Carroll S.P. Behavior as phenotypic plasticity. Evolutionary Behavioral Ecology 2010, 90-107. Oxford University Press, Oxford. D.F. Westneat, C.W. Fox (Eds.).
15. Grageda V.C., Sakakura Y., Minamimoto M., Hagiwara A. Differences in life-history traits in two clonal strains of the self-fertilizing fish, Rivulus marmoratus. Environmental Biology of Fishes 2005, 73:427-436.
16. Graham J.B. Air-breathing Fishes: Evolution, Diversity, and Adaptation 1997, Academic Press, San Diego.
17. Grizzle J.M., Thiyagarajah A. Skin histology of Rivulus ocellatus marmoratus: apparent adaptation for aerial respiration. Copeia 1987, 1987:237-240.
18. Harrington R.W. Oviparous hermaphroditic fish with internal self-fertilization. Science 1961, 134:1749-1750.
19. Harrington R.W. Twenty-four hour rhythms of internal self-fertilization and of oviposition by hermaphrodites of Rivulus marmoratus. Physiological Zoology 1963, 36:325-341.
20. Huehner M.K., Schramm M.E., Hens M.D. Notes on the behavior and ecology of the killifish Rivulus marmoratus Poey 1880 (Cyprinodontidae). Florida Scientist 1985, 48:1-7.
21. King J.A.C., Abel D.C., DiBona R. Effects of salinity on chloride cells in the euryhaline cyprinodontid fish Rivulus marmoratus. Cell and Tissue Research 1989, 257:367-377.
22. Laughlin T.F., Lubinski B.A., Park E.-H., Taylor D.S., Turner B.J. Clonal stability and mutation in the self-fertilizing hermaphroditic fish, Rivulus marmoratus. Journal of Heredity 1995, 86:399-402.
23. LeBlanc D.M., Wood C.M., Fudge D.S., Wright P.A. A fish out of water: gill and skin remodeling promotes osmo- and ionoregulation in the mangrove killifish Kryptolebias marmoratus. Physiological and Biochemical Zoology 2010, 83:932-949. 10.1086/656307.
24. Lin H.-C., Dunson W.A. An explanation of the high strain diversity of a self-fertilizing hermaphroditic fish. Ecology 1995, 76:593-605.
25. Lin H.-C., Dunson W.A. Phenotypic plasticity in the growth of the self-fertilizing hermaphroditic fish Rivulus marmoratus. Journal of Fish Biology 1999, 54:250-266.
26. Litwiller S.L., O'Donnell M.J., Wright P.A. Rapid increase in the partial pressure of NH3 on the cutaneous surface of air-exposed mangrove killifish, Rivulus marmoratus. Journal of Experimental Biology 2006, 209:1737-1745. 10.1242/jeb.02197.
27. Mackiewicz M., Tatarenkov A., Perry A., Martin J.R., Elder J.F., Bechler D.L., Avise J.C. Microsatellite documentation of outcrossing between inbred laboratory strains of the self-fertilizing mangrove killifish (Kryptolebias marmoratus). Journal of Heredity 2006, 97:508-513. 10.1093/jhered/es1017.
28. Mackiewicz M., Tatarenkov A., Taylor D.S., Turner B.J., Avise J.C. Extensive outcrossing and androdioecy in a vertebrate species that otherwise reproduces as a self-fertilizing hermaphrodite. Proceedings of the National Academy of Sciences, U.S.A. 2006, 103:9924-9928. 10.1073/pnas.0603847103.
29. Marks C., West T.N., Bagatto B., Moore F.B.G. Developmental environment alters conditional aggression in zebrafish. Copeia 2005, 2005:901-908.
30. Matey V., Richards J.G., Wang Y., Wood C.M., Rogers J., Davies R., Murray B.W., Chen X., Du J., Brauner C.J. The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. Journal of Experimental Biology 2008, 211:1063-1074. 10.1242/jeb.010181.
31. Mitrovic D., Perry S.F. The effects of thermally induced gill remodeling on ionocyte distribution and branchial chloride fluxes in goldfish (Carassius auratus). Journal of Experimental Biology 2009, 212:843-852. 10.1242/jeb.025999.
32. Nilsson G.E. Gill remodeling in fish: a new fashion or an ancient secret?. Journal of Experimental Biology 2007, 210:2403-2409. 10.1242/jeb.000281.
33. Ong K.J., Stevens E.D., Wright P.A. Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure. Journal of Experimental Biology 2007, 210:1109-1115. 10.1242/jeb.002238.
34. Petrie M.E., Ryer C.H. Hunger, light level and body size affect refuge use by post-settlement lingcod Ophiodon elongates. Journal of Fish Biology 2006, 69:957-969. 10.1111/j.1095-8649.2006.01165.x.
35. Sakakura Y., Soyano K., Noakes D.L.G., Hagiwara A. Gonadal morphology in the self-fertilizing mangrove killifish, Kryptolebias marmoratus. Ichthyological Research 2006, 53:427-430. 10.1007/s10228-006-0362-2.
36. Sayer M.D.J. Adaptations of amphibious fish for surviving life out of water. Fish and Fisheries 2005, 6:186-211.
37. Schaefer J., Ryan A. Developmental plasticity in the thermal tolerance of zebrafish Danio rerio. Journal of Fish Biology 2006, 69:722-734. 10.1111/j.1095-8649.2006.01145.x.
38. Scheiner S.M. Genetics and evolution of phenotypic plasticity. Annual Review of Ecology and Systematics 1993, 24:35-68.
39. Sollid J., De Angelis P., Gundersen K., Nilsson G.E. Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. Journal of Experimental Biology 2003, 206:3667-3673. 10.1242/jeb.00594.
40. Sollid J., Weber R.E., Nilsson G.E. Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. Journal of Experimental Biology 2005, 208:1109-1116. 10.1242/jeb.01505.
41. Stoner A.W. Hunger and light level alter response to bait by Pacific halibut: laboratory analysis of detection, location and attack. Journal of Fish Biology 2003, 62:1176-1193. 10.1046/j.1095-8649.2003.00117.x.
42. Tatarenkov A., Lima S., Taylor D.S., Avise J.C. Long-term retention of self-fertilization in a fish clade. Proceedings of the National Academy of Sciences, U.S.A. 2009, 106:14456-14459. 10.1073/pnas.0907852106.
43. Tatarenkov A., Ring B.C., Elder J.F., Bechler D.L., Avise J.C. Genetic composition of laboratory stocks of the self-fertilizing fish Kryptolebias marmoratus: a valuable resource for experimental research. PLoS ONE 2010, 5. e12863. 10.1371/journal.pone.0012863.
44. Taylor D.S. Adaptive specializations of the cyprinodont fish Rivulus marmoratus. Florida Scientist 1990, 53:239-248.
45. Taylor D.S. Diet of the killifish Rivulus marmoratus collected from land crab burrows, with further ecological notes. Environmental Biology of Fishes 1992, 33:389-393.
46. Taylor D.S. Biology and ecology of Rivulus marmoratus: new insights and a review. Florida Scientist 2000, 63:242-255.
47. Taylor D.S., Davis W.P., Turner B.J. Groveling in the mangroves: 16 years in pursuit of the cyprinodont fish Rivulus marmoratus on the Belize Cays. Atoll Research Bulletin 2004, 525:1-14.
48. Taylor D.S., Turner B.J., Davis W.P., Chapman B.B. A novel terrestrial fish habitat inside emergent logs. American Naturalist 2008, 171:263-266. 10.1086/524960.
49. Tulley J.J., Huntingford F.A. Parental care and the development of adaptive variation in anti-predator responses in sticklebacks. Animal Behaviour 1987, 35:1570-1572.
50. Turner B.J., Elder J.F., Laughlin T.F., Davis W.P. Genetic variation in clonal vertebrates detected by simple-sequence DNA fingerprinting. Proceedings of the National Academy of Sciences, U.S.A. 1990, 87:5653-5657.
51. Turner B.J., Elder J.F., Laughlin T.F., Davis W.P., Taylor D.S. Extreme clonal diversity and divergence in populations of a selfing hermaphroditic fish. Proceedings of the National Academy of Sciences, U.S.A. 1992, 89:10643-10647.
52. Vehanen T. Adaptive flexibility in the behaviour of juvenile Atlantic salmon: short-term responses to food availability and threat from predation. Journal of Fish Biology 2003, 63:1034-1045. 10.1046/j.1095-8649.2003.00228.x.
53. Vogt G., Huber M., Thiemann M., van den Boogaart G., Schmitz O.J., Schubart C.D. Production of different phenotypes from the same genotype in the same environment by developmental variation. Journal of Experimental Biology 2008, 211:510-523. 10.1242/jeb.008755.
54. Vrijenhoek R.C. Homozygosity and interstrain variation in the self-fertilizing hermaphroditic fish, Rivulus marmoratus. Journal of Heredity 1985, 76:82-84.
55. West-Eberhard M.J. Developmental Plasticity and Evolution 2003, Oxford University Press, New York.
56. Widmer S., Moore F.B.G., Bagatto B. The effects of chronic developmental hypoxia on swimming performance in zebrafish. Journal of Fish Biology 2006, 69:1885-1891. 10.1111/j.1095-8649.2006.01242.x.