Interspecific differences in hypoxia-induced gill remodeling in carp

Physiological and Biochemical Zoology

Volumn 86, Issue 6, 2013, Pages 727-739

  Dhillon, Rashpal S ^a   Yao, Lili ^a   Matey, Victoria ^b   Chen, Bo Jian ^c   Zhang, An Jie ^c   Cao, Zhen Dong ^c   Fu, Shi Jian ^c   Brauner, Colin J ^a   Wang, Yuxiang S ^d   Richards, Jeffrey G ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b SAN DIEGO STATE UNIVERSITY   (United States)

^c CHONGQING NORMAL UNIVERSITY   (China)

^d QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYPRINID; DEVELOPMENTAL BIOLOGY; ECOLOGICAL MODELING; HYPOXIA; INTERSPECIFIC VARIATION; MAGNITUDE; MORPHOLOGY; NUMERICAL MODEL; OXYGEN; PHYLOGENETICS;

CYTOCHROME B; DNA; OXYGEN;

ANIMAL; ANIMAL DISEASE; ANOXIA; ARTICLE; CARP; CHEMISTRY; GENETICS; GILL; METABOLISM; PHYLOGENY; POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANIMALS; ANOXIA; CARPS; CYTOCHROMES B; DNA; GILLS; MICROSCOPY, ELECTRON, SCANNING; OXYGEN; PHYLOGENY; POLYMERASE CHAIN REACTION;

EID: 84887731263     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/673180     Document Type: Article

References (59)

1. Bickler P.E. and L.T. Buck. 2007. Hypoxia tolerance in reptiles, amphibians, and fishes: life with variable oxygen availability. Annu Rev Physiol 69:145-170.
2. Blazka P. 1958. The anaerobic metabolism of fish. Physiol Zool 31:117-128.
3. Brauner C.J., V. Matey, W. Zhang, J.G. Richards, R. Dhillon, Z.-D. Cao, Y. Wang, and S.-J. Fu. 2011. Gill remodeling in crucian carp during sustained exercise and the effect on subsequent swimming performance. Physiol Biochem Zool 84: 535-542.
4. Brauner C.J., T. Wang, Y. Wang, J.G. Richards, R.J. Gonzalez, N.J. Bernier, W. Xi, M. Patrick, and A.L. Val. 2004. Limited extracellular but complete intracellular acid-base regulation during short-term environmental hypercapnia in the armoured catfish, Liposarcus pardalis. J Exp Biol 207:3381-3390.
5. Brett J.R. 1964. The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Board Can 21:1183-1226.
6. Burggren W.W. 1982. "Air gulping" improves blood oxygen transport during aquatic hypoxia in the goldfish Carassius auratus. Physiol Zool 55:327-334.
7. Diaz R.J. and D.L. Breitburg. 2009. The hypoxic environment. Pp. 1-23 in J.G. Richards, A.P. Farrell, and C.J. Brauner, eds. Hypoxia. Elsevier, San Diego, CA.
8. Felsenstein J. 1985. Phylogenies and the comparative method. Am Nat 125:1-15.
9. Fu S.-J., C.J. Brauner, Z.-D. Cao, J.G. Richards, J.-L. Peng, R. Dhillon, and Y.-X. Wang. 2011. The effect of acclimation to hypoxia and sustained exercise on subsequent hypoxia tolerance and swimming performance in goldfish (Carassius auratus). J Exp Biol 214:2080-2088.
10. Fu S.-J., Z. Peng, Z.-D. Cao, J.-L. Peng, X.-K. He, D. Xu, and A.-J. Zhang. 2012. Habitat-specific locomotor variation among Chinese hook snout carp (Opsariichthys bidens) along a river. PLoS ONE 7:e40791.
11. Garland T., Jr., and S.C. Adolph. 1994. Why not to do twospecies comparative studies: limitations on inferring adaptation. Physiol Zool 67:797-828.
12. Garland T., Jr., A.F. Bennett, and E.L. Rezende. 2005. Phylogenetic approaches in comparative physiology. J Exp Biol 208:3015-3035.
13. Garland T., Jr., P.H. Harvey, and A.R. Ives. 1992. Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18-32.
14. Gonzalez R.J. 2011. The osmorespiratory compromise. Pp. 1389-1394 in A.P. Farrell, E.D. Stevens, J.J. Cech, and J.G. Richards, eds. Encyclopedia of fish physiology: from genome to environment. Vol. 2. Academic Press, London.
15. Holopainen I. J, W.M. Tonn, and C.A. Paszkowski. 1997. Tales of two fish: the dichotomous biology of crucian carp (Carassius carassius (L.) in northern Europe. Ann Zool Fenn 34:1-22.
16. Hyvärinen H., I.J. Holopainen, and J. Piironen. 1985. Anaerobic wintering of crucian carp (Carassius carassius L.). I. Annual dynamics of glycogen reserves in nature. Comp Biochem Physiol A 82:797-803.
17. Johnston I.A. and L.M. Bernard. 1983. Utilization of the ethanol pathway in carp following exposure to anoxia. J Exp Biol 104:73-78.
18. Karnovsky M.J. 1965. A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137-138.
19. Kong X.H., X.Z. Wang, X.N. Gan, J.B. Li, and S.P. He. 2007. Phylogenetic relationships of Cyprinidae (Teleostei: Cypriniformes) inferred from the partial S6K1 gene sequences and implication of indel sites in intron 1. Sci China Ser C Life Sci 50:780-788.
20. Kramer D.L. 1987. Dissolved oxygen and fish behavior. Environ Biol Fishes 18:81-92.
21. Kumar S., K. Tamura, and M. Nei. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150-163.
22. Lomholt J.P. and K. Johansen. 1979. Hypoxia acclimation in carp: how it affects O2 uptake, ventilation, and O2 extraction from water. Physiol Zool 52:38-49.
23. Luo Y.L. 1990. A revision of fishes of the cyprinid genus Megalobrama. Acta Hydrobiol Sin 14:159-165.
24. MaddisonW.P. and D.R. Maddison. 2004. Mesquite: a modular system for evolutionary analysis. Version 1.02. http:// mesquiteproject.org.
25. Mandic M., K.A. Sloman, and J.G. Richards. 2009a. Escaping to the surface: a phylogenetically independent analysis of hypoxia-induced respiratory behaviors in sculpins. Physiol Biochem Zool 82:730-738.
26. Mandic M., B. Speers-Roesch, and J.G. Richards. 2013. Hypoxia tolerance in sculpins is associated with high anaerobic enzyme activity in brain but not in liver or muscle. Physiol Biochem Zool 86:92-105.
27. Mandic M., A.E. Todgham, and J.G. Richards. 2009b. Mechanisms and evolution of hypoxia tolerance in fish. Proc R Soc B 276:735-744.
28. Matey V., J.G. Richards, Y. Wang, C.M. Wood, J. Rogers, R. Davies, B.W. Murray, X.-Q. Chen, J. Du, and C.J. Brauner. 2008. The effect of hypoxia on gill morphology and ionoregulatory status in the Lake Qinghai scaleless carp, Gymnocypris przewalskii. J Exp Biol 211:1063-1074.
29. Midford P.E., T. Garland Jr., and W.P. Maddison. 2003. PDAP: PDTREE: a translation of the PDTREE application of Garland et al.'s phenotypic diversity analysis programs. http:// mesquiteproject.org/pdap_mesquite.
30. Muusze B., J. Marcon, G. van den Thillart, and V. Almeida-Val. 1998. Hypoxia tolerance of Amazon fish: respirometry and energy metabolism of the cichlid Astronotus ocellatus. Comp Biochem Physiol A120:151-156.
31. Nilsson G.E., A. Dymowska, and J.A.W. Stecyk. 2012. New insights into the plasticity of gill structure. Resp Physiol Neurobiol 184:214-222.
32. Nilsson G.E. and S. Ostlund-Nilsson. 2008. Does size matter for hypoxia tolerance in fish? Biol Rev 83:173-189.
33. Nilsson G., S. Ostlund-Nilsson, R. Penfold, and A.S. Grutter. 2007. From record performance to hypoxia tolerance: respiratory transition in damselfish larvae settling on a coral reef. Proc R Soc B 274:79-85.
34. Nilsson G.E. and G.M.C. Renshaw. 2004. Hypoxic survival strategies in two fishes: extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. J Exp Biol 207:3131-3139.
35. Ong K.J., E.D. Stevens, and P.A. Wright. 2007. Gill morphology of the mangrove killifish (Kryptolebias marmoratus) is plastic and changes in response to terrestrial air exposure. J Exp Biol 210:1109-1115.
36. Perry S.F., C. Fletcher, S. Bailey, J. Ting, J. Bradshaw, V. Tzaneva, and K.M. Gilmour. 2012. The interactive effects of exercise and gill remodeling in goldfish (Carassius auratus). J Comp Physiol B 182:935-945.
37. Posada D. and K.A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
38. Shoubridge E.A. and P.W. Hochachka. 1980. Ethanol: novel end product of vertebrate anaerobic metabolism. Science 209: 308-309.
39. Sloman K.A., C.M. Wood, G.R. Scott, S. Wood, M. Kajimura, O.E. Johannsson, V.M. Almeida-Val, and A.L. Val. 2006. Tribute to R. G. Boutilier: the effect of size on the physiological and behavioural responses of oscar, Astronotus ocellatus, to hypoxia. J Exp Biol 209:1197-1205.
40. Sollid J., P. De Angelis, K. Gundersen, and G.E. Nilsson. 2003. Hypoxia induces adaptive and reversible gross morphological changes in crucian carp gills. J Exp Biol 206:3667-3673.
41. Sollid J., A. Kjernsli, P.M. De Angelis, A.K. Rohr, and G.E. Nilsson. 2005a. Cell proliferation and gill morphology in anoxic crucian carp. Am J Physiol 289:R1196-R1201.
42. Sollid J. and G.E. Nilsson. 2006. Plasticity of respiratory structures: adaptive remodeling of fish gills induced by ambient oxygen and temperature. Respir Physiol Neurobiol 154:241-251.
43. Sollid J., R.E. Weber, and G.E. Nilsson. 2005b. Temperature alters the respiratory surface area of crucian carp Carassius carassius and goldfish Carassius auratus. J Exp Biol 208:1109-1116.
44. Tzaneva V., S. Bailey, and S.F. Perry. 2011a. The interactive effects of hypoxemia, hyperoxia, and temperature on the gill morphology of goldfish (Carassius auratus). Am J Physiol 300:R1344-R1351.
45. Tzaneva V., K.M. Gilmour, and S.F. Perry. 2011b. Respiratory responses to hypoxia or hypercapnia in goldfish (Carassius auratus) experiencing gill remodelling. Respir Physiol Neurobiol 175:112-120.
46. Ultsch G.R., M.E. Ott, and N. Heisler. 1980. Standard metabolic rate, critical oxygen tension, and aerobic scope for spontaneous activity of trout (Salmo gairdneri) and carp (Cyprinus carpio) in acidified water. Comp Biochem Physiol A 67:329-335.
47. Val A.L., V.M.F. Almeida-Val, and D.J. Randall, eds. 2006. Fish physiology. Vol. 21. The physiology of tropical fishes. Elsevier/ Academic Press, London.
48. Van den Thillart G., F. Kesbeke, and A. van Waarde. 1976. Influence of anoxia on the energy metabolism of goldfish Carassius auratus (L.). Comp Biochem Physiol A 55:329-336.
49. 2 excretion rates and anoxia tolerance at 20, 10 and 5°C. Comp Biochem Physiol A 76:295-300.
50. Van Waversveld J., A.D.F. Addink, and G. Van den Thillart. 1989. Simultaneous direct and indirect calorimetry on normoxic and anoxic goldfish. J Exp Biol 142:325-335.
51. Walker R.M. and P.H. Johansen. 1977. Anaerobic metabolism in goldfish (Carassius auratus). Can J Zool 55:1304-1311.
52. Wang C., Q. Chen, G. Lu, J. Xu, Q. Yang, and S. Li. 2008. Complete mitochondrial genome of the grass carp (Ctenopharyngodon idella, Teleostei): insight into its phylogenic position within Cyprinidae. Gene 424:96-101.
53. Wang C., J. Wang, J. Yang, G. Lu, X. Song, Q. Chen, J. Xu, Q. Yang, and S. Li. 2012. Complete mitogenome sequence of black carp (Mylopharyngodon piceus) and its use for molecular phylogeny of leuciscine fishes. Mol Biol Rep 39:6337-6342.
54. Wang X., J. Wang, S. He, and R.L. Mayden. 2007. The complete mitochondrial genome of the Chinese hook snout carp Opsariichthys bidens (Actinopterygii: Cypriniformes) and an alternative pattern of mitogenomic evolution in vertebrate. Gene 399:11-19.
55. 2 on hemoglobin-oxygen affinity. J Comp Physiol B 128:127-137.
56. Yeager D.P. and G.R. Ultsch. 1989. Physiological regulation and conformation: a BASIC program for the determination of critical points. Physiol Zool 62:888-907.
57. Yi Y., Z. Wang, and Z. Yang. 2010. Impact of the Gezhouba and Three Gorges Dams on habitat suitability of carps in the Yangtze River. J Hydrol 387:283-291.
58. Yoshiyama R.M., C.J. Valpey, and L.L. Schalk. 1995. Differential propensities for aerial emergence in intertidal sculpins (Teleostei; Cottidae). J Exp Mar Biol Ecol 191:195-207.
59. Zhang W., Z.D. Cao, J.L. Peng, B.J. Chen, and S.J. Fu. 2010. The effects of dissolved oxygen level on the metabolic interaction between digestion and locomotion in juvenile southern catfish (Silurus meridionalis Chen). Comp Biochem Physiol A 157:212-219.