An ecomorphological framework for the coexistence of two cyprinid fish and their hybrids in a novel environment

Biological Journal of the Linnean Society

Volumn 99, Issue 4, 2010, Pages 768-783

  Toscano, Benjamin J ^a,b   Pulcini, Domitilla ^a,c   Hayden, Brian ^b   Russo, Tommaso ^c   Kelly Quinn, Mary ^b   Mariani, Stefano ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Abramis brama; Adaptation; Freshwater; Hybridization; Rutilus rutilus

Indexed keywords

ADAPTATION; AGE CLASS; BODY SHAPE; COEXISTENCE; CYPRINID; DIET; ECOMORPHOLOGY; GENETIC ANALYSIS; HYBRID; HYBRIDIZATION; LIFE HISTORY; NICHE BREADTH; PHENOTYPIC PLASTICITY; TROPHIC ENVIRONMENT;

IRELAND;

ABRAMIS BRAMA; CYPRINIDAE; HYPEROGLYPHE POROSA; RUTILUS RUTILUS;

EID: 77952822559     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2010.01383.x     Document Type: Article

References (100)

1. Appelberg M. Swedish standard methods for sampling freshwater fish with multi-mesh gillnets. Fiskeriverket Information 2000, 1:3-32.
2. Arnold ML. Natural hybridization and evolution 1997, New York, NY, Oxford University Press
3. Arnold ML, Hodges SA. Are natural hybrids fit or unfit relative to their parents? Trends in Ecology and Evolution 1995, 10:67-71.
4. Bagenal TB, Telsch FW. Age and growth. Methods for assessment of fish production in fresh waters 1978, 101-136. Bagenal TB, In, ed., London, Blackwell Scientific
5. Barton NH. The role of hybridization in evolution. Molecular Ecology 2001, 10:551-568.
6. Barton NH, Hewitt GM. Analysis of hybrid zones. Annual Review of Ecology and Systematics 1985, 16:113-148.
7. Bearhop S, Adams CE, Waldron S, Fuller RA, Macleod H. Determining trophic niche width: a novel approach using stable isotope analysis. Journal of Animal Ecology 2004, 73:1007-1012.
8. Bianco PG. Hybridization between Alburnus albidus and Leuciscus cephalus cabeda in Italy. Journal of Fish Biology 1982, 21:593-603.
9. Bolnick DI, Yang LH, Fordyce JA, Davis JM, Svanback R. Measuring individual-level resource specialization. Ecology 2002, 83:2936-2941.
10. Bookstein FL. Morphometric tools for landmark data: geometry and biology 1991, Cambridge, Cambridge University Press
11. Bookstein FL, Gunz P, Mitteroecker P, Prossinger H, Schaefer K, Seidler H. Cranial integration in Homo: singular warps analysis of the midsagittal plane in ontogeny and evolution. Journal of Human Evolution 2003, 44:167-187.
12. Brassington R, Ferguson A. Electrophoretic identification of roach (Rutilus rutilus L.), rudd (Scardinim erythrophthalmus L.), bream (Abramis brama L.) and their natural hybrids. Journal of Fish Biology 1976, 9:471-477.
13. Buerkle CA, Morris RJ, Asmussen MA, Rieseberg LH. The likelihood of homoploid hybrid speciation. Heredity 2000, 84:441-451.
14. Burke JM, Arnold ML. Genetics and the fitness of hybrids. Annual Review of Genetics 2001, 35:31-52.
15. Burke JM, Carney SE, Arnold ML. Hybrid fitness in the Louisiana irises: analysis of parental and F1 performance. Evolution 1998, 52:37-43.
16. Caffrey J. Fish stock assessment of lough ramor 2005, Dublin, Central Fisheries Board
17. Child AR, Solomon DJ. Observations on morphological and biochemical features of some cyprinid hybrids. Journal of Fish Biology 1977, 11:125-131.
18. Clarke KR. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 1993, 18:117-143.
19. Cowx IG. The biology of bream, Abramis brama (L), and its natural hybrid with roach, Rutilus rutilus (L), in the River Exe. Journal of Fish Biology 1983, 22:631-646.
20. Cowx IG. Factors influencing coarse fish populations in rivers 2001, Bristol, R&D Publication 18, Environment Agency
21. Cragg-Hine D, Jones JW. Growth of dace Leuciscus leuciscus (L), roach Rutilus rutilus (L), and chub Squaliuscephalus (L) in Willow Brook, Northamptonshire. Journal of Fish Biology 1969, 1:59-82.
22. Cross TF. Isozymes of interspecific hybrids of the fish family Cyprinidae. Proceedings of the Royal Irish Academy 1978, 78B:323-334.
23. Dalerum F, Angerbjorn A. Resolving temporal variation in vertebrate diets using naturally occurring stable isotopes. Oecologia 2005, 144:647-658.
24. DeMarais BD, Dowling TE, Douglas ME, Minckley WL, Marsh PC. Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive hybridisation: implications for evolution and conservation. Proceedings of the National Academy of Sciences of the United States of America 1992, 89:2747-2751.
25. DeNiro MJ, Epstein S. Mechanism of carbon isotope fractionation associated with lipid synthesis. Science 1977, 197:261-263.
26. Diamond M. Some observations of spawning by roach, Rutilus rutilus L., and bream, Abramis brama L., and their implications for management. Aquaculture Research 1985, 16:359-367.
27. Dobzhansky T. Genetics and the origin of species 1951, New York, NY, Columbia University Press
28. Dobzhansky T. The genetics of the evolutionary process 1970, New York, NY, Columbia University Press
29. Dowling TE, Secor CL. The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics 1997, 28:593-619.
30. Ehlinger TJ. Habitat choice and phenotype-limited feeding efficiency in bluegill: individual differences and trophic polymorphisms. Ecology 1990, 71:886-896.
31. Emms SK, Arnold ML. The effect of habitat on parental and hybrid fitness: transplant experiments with Louisiana irises. Evolution 1997, 51:1112-1119.
32. Fadda C, Corti M. Three-dimensional geometric morphometrics of Arvicanthis: implications for systematics and taxonomy. Journal of Zoological Systematics & Evolutionary Research 2001, 39:235-245.
33. Fahy E, Martin S, Mulrooney M. Interactions of roach and bream in an Irish Reservoir. Archive für Hydrobiologie 1988, 114:291-309.
34. Fitzmaurice P. The spread of roach Rutilus rutilus (L.) in Irish waters. Second British Freshwaters Fisheries Conference 1981, 154-161. In, Liverpool, University of Liverpool
35. Fitzsimons M, Igoe F. Freshwater fish conservation in the Irish Republic: A review of pressures and legislation impacting on conservation efforts. Biology and Environment 2004, 104B:17-32.
36. Francis RICC. Back-calculation of fish length - a critical review. Journal of Fish Biology 1990, 36:883-902.
37. Frear PA. Hydroacoustic target strength validation using angling creel census data. Fisheries Management and Ecology 2002, 9:343-350.
38. Giessler S, Mader E, Schwenk K. Morphological evolution and genetic differentiation in Daphnia species complexes. Journal of Evolutionary Biology 1999, 12:710-723.
39. Goldspink CR. Comparative observations on growth-rate and year class strength of roach Rutilus rutilus L. in two Cheshire lakes, England. Journal of Fish Biology 1978, 12:421-433.
40. Goldspink CR. The population density, growth rate and reproduction of roach Rutilus rutilus (L.) in Tjeukemeer, The Netherlands. Journal of Fish Biology 1979, 15:473-498.
41. Goldspink CR. A note on the growth-rate and year-class strength of bream, Abramis brama (L.), in three eutrophic lakes, England. Journal of Fish Biology 1981, 19:665-673.
42. Hammer O, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 2001, 4.
43. Hänfling B. Understanding the establishment success of non-indigenous fishes: lessons from population genetics. Journal of Fish Biology 2007, 71D:115-135.
44. Hänfling B, Bolton P, Harley M, Carvalho GR. A molecular approach to detect hybridisation between crucian carp (Carassius carassius) and non-indigenous carp species (Carassius spp. and Cyprinus carpio). Freshwater Biology 2005, 50:403-417.
45. Harrod C, Grey J. Isotopic variation complicates analysis of trophic relations within the fish community of Plu beta see: a small, deep, stratifying lake. Archiv Fur Hydrobiologie 2006, 167:281-299.
46. Hatfield T, Schluter D. Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution 1999, 53:866-873.
47. Holmgren K, Appelberg M. Size structure of benthic freshwater fish communities in relation to environmental gradients. Journal of Fish Biology 2000, 57:1312-1330.
48. Horppila J. The effect of length frequency ranges on the back-calculated lengths of roach, Rutilus rutilus (L.). Fisheries Research 2000, 45:21-29.
49. Horppila J, Nyberg K. The validity of different methods in the backcalculation of the lengths of roach - a comparison between scales and cleithra. Journal of Fish Biology 1999, 54:489-498.
50. Kennedy M, Fitzmaurice P. The biology of the bream Abramis brama (L.) in Irish waters. Proceedings of the Royal Irish Academy 1968, 67:95-157.
51. Kennedy M, Fitzmaurice P. Occurrence of cyprinid hybrids in Ireland. Irish Naturalists Journal 1973, 17:349-351.
52. Kiljunen M, Grey J, Sinisalo T, Harrod C, Immonen H, Jones RI. A revised model for lipid-normalizing delta C-13 values from aquatic organisms, with implications for isotope mixing models. Journal of Applied Ecology 2006, 43:1213-1222.
53. Kruskal JB. Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 1964a, 29:1-27.
54. Kruskal JB. Nonmetric multidimensional scaling: a numerical method. Psychometrika 1964b, 29:115-129.
55. Lammens EHRR, Geursen J, McGillavry J. Diet shifts, feeding efficiency and coexistence of bream (Abramis brama), roach (Rutilus rutilus) and white bream (Blicca bjoerkna) in hypertrophic lakes: Proceedings of the Fifth Congress of European Ichthyologists. 1985, 153-162.
56. Lammens EHRR, Hoogenboezem W. Diets and feeding behaviour. Cyprinid fishes: systematics, biology and exploitation 1991, 353-376. Winfield IJ, Nelson JS. In, eds., London, Chapman and Hall
57. Lauder GV. Form and function: structural analysis in evolutionary morphology. Paleobiology 1981, 7:430-442.
58. Lauder GV, Drucker EG. Morphology and experimental hydrodynamics of fish fin control surfaces. IEEE Journal of Oceanic Engineering 2004, 29:556-571.
59. Layman CA, Arrington DA, Montana CG, Post DM. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 2007, 88:42-48.
60. Lexer C, Welch M, Durphy J, Rieseberg L. Natural selection for salt tolerance quantitative trait loci (QTLs) in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid hybrid species. Molecular Ecology 2003, 12:1225-1235.
61. Martinez del Rio C, Wolf BO. Mass-balance models for animal-isotopic ecology. Physiological and ecological adaptations to feeding in vertebrates 2005, 141-174. Stack M, Wand T. In, eds., Enfield, Science Publishers
62. Mayr E. Animal species and evolution 1963, Cambridge, MA, Belknap Press
63. McCarthy EM, Asmussen MA, Anderson WW. A theoretical assessment of recombinational speciation. Heredity 1995, 74:502-509.
64. Mehner T, Holmgren K, Lauridsen TL, Jeppesen E, Diekmann M. Lake depth and geographical position modify lake fish assemblages of the European 'Central Plains' ecoregion. Freshwater Biology 2007, 52:2285-2297.
65. Mulrooney M, Fahy E. Hybridisation among three cyprinid species in a Co. Dublin reservoir. Irish Naturalists Journal 1985, 21:470-472.
66. Newsome SD, Martinez del Rio C, Bearhop S, Phillips DL. A niche for isotopic ecology. Frontiers in Ecology and the Environment 2007, 5:429-436.
67. Nzau Matondo B, Ovidio M, Philippart JC, Poncin P. Hybridization behaviour between two common European cyprinid fish species - silver bream, Blicca bjoerkna and common bream, Abramis brama- in a controlled environment. Animal Biology 2009, 59:97-108.
68. Olin M, Rask M, Ruuhijarvi J, Kurkilahti M, Ala-Opas P, Ylonen O. Fish community structure in mesotrophic and eutrophic lakes of southern Finland: the relative abundances of percids and cyprinids along a trophic gradient. Journal of Fish Biology 2002, 60:593-612.
69. Perez SI, Bernal V, Gonzalez PN. Differences between sliding semi-landmark methods in geometric morphometrics, with an application to human craniofacial and dental variation. Journal of Anatomy 2006, 208:769-784.
70. Pfennig KS. Facultative mate choice drives adaptive radiation. Science 2007, 318:965-967.
71. Phillips DL, Gregg JW. Uncertainty in source partitioning using stable isotopes. Oecologia 2001, 127:171-179.
72. Pitts CS. Hybridisation in the fish family Cyprinidae. 1994, DPhil. Thesis, University of Hull
73. Pitts CS, Jordan DR, Cowx IG, Jones NV. Controlled breeding studies to verify the identity of roach and common bream hybrids from a natural population. Journal of Fish Biology 1997, 51:686-696.
74. Post DM. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83:703-718.
75. Reyer HU. Mating with the wrong species can be right. Trends in Ecology and Evolution 2008, 23:289-292.
76. Rieseberg LH. Hybrid origins of plant species. Annual Review of Ecology and Systematics 1997, 28:359-389.
77. Rieseberg LH, Van Fossen C, Desrochers AM. Hybrid speciation accompanied by genomic reorganization in wild sunflowers. Nature 1995, 375:313-316.
78. Rohlf FJ. An overview of image processing and analysis techniques for morphometrics. Proceedings of the Michigan morphometrics workshop 1990, 37-60. Ann Arbor, MI, University of Michigan Museum of Zoology
79. Rohlf FJ. Comparitive methods for the analysis of continuous variables: geometric interpretations. Evolution 2001, 55:2143-2160.
80. Rohlf FJ. TPS dig 2006, http://life.bio.sunysb.edu/morph/, Stony Brook, NY, Department of Ecology and Evolution, State University of New York, Available at:
81. Rohlf FJ, Corti M. The use of two-block partial least-squares to study covariation in shape. Systematic Biology 2000, 49:740-753.
82. Rohlf FJ, Slice DE. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 1990, 39:40-59.
83. Russo T, Pulcini D, O'Leary A, Cataudella S, Mariani S. Relationship between body shape and trophic niche segregation in two closely related symparic fishes. Journal of Fish Biology 2008, 73:809-828.
84. Schiffman SS, Reynolds ML, Young FW. Introduction to multidimensional scaling: theory, methods, and applications 1981, New York, NY, Academic Press
85. Schluter D. Ecology and the origin of species. Trends in Ecology and Evolution 2001, 16:372-380.
86. Seehausen O. Hybridization and adaptive radiation. Trends in Ecology and Evolution 2004, 19:198-207.
87. Simons JHEJ, Bakker C, Schropp MHI, Jans LH, Kok FR, Grift RE. Man-made secondary channels along the river Rhine (the Netherlands); results of post-project monitoring. Regulated Rivers: Research and Management 2001, 17:473-491.
88. Smith PA. The relationship between stock and catch and the effect of bait on catch as determined for a UK recreational catch and release fishery. Fisheries Management and Ecology 2002, 9:261-266.
89. Templeton AR. Mechanisms of speciation - a population genetic approach. Annual Review of Ecology and Systematics 1981, 12:23-48.
90. Toner P, Bowman J, Clabby K, Lucey J, McGarrigle M, Concannon C, Clenaghan C, Cunningham P, Delaney J, O'Boyle S, MacCárthaigh M, Craig M, Quinn R. Water quality in Ireland 2001-2003 2005, Wexford, EPA
91. Waser NM, Price MV. Outcrossing distance effects in Delphinium nelsonii: pollen loads, pollen tubes, and seed set. Ecology 1991, 72:171-179.
92. Webb PW. Body form, locomotion and foraging in aquatic vertebrates. American Zoologist 1984, 24:107-120.
93. Went AEJ. Recent Irish records of rare fish. Nature 1950, 165:1025-1025.
94. Went AEJ. The Pike in Ireland. Irish Naturalists Journal 1957, 12:177-182.
95. Wheeler A. The fishes of the British Isles and North-West Europe 1969, London, McMillan
96. Wilson JG. Eutrophication in Irish waters 1998, Dublin, Royal Irish Academy
97. Winemiller KO. Ecomorphological diversification in lowland freshwater fish assemblages from five biotic regions. Ecological Monographs 1991, 61:343-365.
98. Wood AB, Jordan DR. Fertility of roach × bream hybrids, Rutilus rutilus (L.) × Abramis brama (L.), and their identification. Journal of Fish Biology 1987, 30:249-261.
99. Wyatt PMW, Pitts CS, Butlin RK. A molecular approach to detect hybridization between bream Abramis brama, roach Rutlius rutilus and rudd Scardinius erythrophthalmus. Journal of Fish Biology 2006, 69:52-71.
100. Zelditch ML, Swiderski DL, Sheets HD, Fink WL. Geometric morphometrics for biologists: a primer 2004, London, Elsevier Academic Press