Ecomorphological disparity in an adaptive radiation: Opercular bone shape and stable isotopes in Antarctic icefishes

Ecology and Evolution

Volumn 3, Issue 9, 2013, Pages 3166-3182

  Wilson, Laura A B ^a,b   Colombo, Marco ^c   Hanel, Reinhold ^d   Salzburger, Walter ^c   Sánchez Villagra, Marcelo R ^a  

^a PALÄONTOLOGISCHES INSTITUT UND MUSEUM   (Switzerland)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c UNIVERSITY OF BASEL   (Switzerland)

^d INSTITUT FÜR SEEFISCHEREI   (Germany)

Author keywords

Craniofacial bone; Ecology; Geometric morphometrics; Phylogeny; Stable isotopes

Indexed keywords

EID: 84887014215     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.708     Document Type: Article

References (130)

1. Adams, D. C., F. J. Rohlf, and D. E. Slice. 2004. Geometric morphometrics: ten years of progress following the 'revolution'. Ital. J. Zool. 71:5-16.
2. Akaike, H. 1974. A new look at the statistical model identification. IEEE Trans. Automat. Contr. 19:716-723.
3. Anker, G. Ch. 1974. Morphology and kinetics of the head of the stickleback, Gasterosteus aculeatus. Trans. Zool. Soc. Lond. 32:311-416.
4. Arif, S., W. E. Aguirre, and M. A. Bell. 2009. Evolutionary diversification of opercle shape in Cook Inlet threespine stickleback. Biol. J. Linn. Soc. 97:832-844.
5. Arnqvist, G., and T. Martensson. 1998. Measurement error in geometric morphometrics: empirical strategies to assess and reduce its impact on measures of shape. Acta Zool. Academ. Sci. Hung. 44:73-96.
6. Arthur, W. 2004. The effect of development on the direction of evolution: toward a twenty-first century consensus. Evol. Dev. 6:282-288.
7. Astrop, T. I. 2011. Phylogeny and evolution of Mecochiridae (Decapoda: Reptantia: Glypheoidea): an integrated morphometric and cladistic approach. J. Crustacean Biol. 31:114-125.
8. Barluenga, M., K. N. Stölting, W. Salzburger, M. Muschick, and A. Meyer. 2006. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439:719-723.
9. Bemis, W. E., and G. V. Lauder. 1986. Morphology and function of the feeding apparatus of the lungfish, Lepidosiren paradoxa (Dipnoi). J. Morphol. 187:81-108.
10. Berner, D., M. Roesti, A. P. Hendry, and W. Salzburger. 2010. Constraints on speciation suggested by comparing lake-stream stickleback divergence across two continents. Mol. Ecol. 19:4963-4978.
11. Blomberg, S. P., J. G. Lefevre, J. A. Wells, and M. Waterhouse. 2012. Independent contrasts and PGLS regression estimators are equivalent. Syst. Biol. 61:382-391.
12. Bookstein, F. L. 1991. P. 435 inMorphometric tools for landmark data. Cambridge Univ. Press, Cambridge 435 pp.
13. Brakefield, P. M. 2006. Evo-devo and constraints on selection. Trends Ecol. Evol. 21:362-368.
14. Brenner, M., B. H. Buck, S. Cordes, L. Dietrich, U. Jacob, K. Mintenbeck, et al. 2001. The role of iceberg scours in niche separation within the Antarctic fish genus Trematomus. Polar Biol. 24:502-507.
15. Burbrink, F. T., and R. A. Pyron. 2010. How does ecological opportunity influence rates of speciation, extinction, and morphological diversification in New World rat snakes (Tribe Lampropeltini)? Evolution 64:934-943.
16. Burchett, M. S. 1983. Food, feeding and behaviour of Notothenia rossii nearshore at South Georgia. Brit. Antarct. Surv. Bull. 61:45-51.
17. Burnham, K. P., and D. R. Anderson. 2010. Model selection and multimodel inference. Springer, New York, NY.
18. Butler, M. A., and A. King. 2004. Phylogenetic comparative analysis: a modelling approach for adaptive evolution. Am. Nat. 164:683-695.
19. Carroll, S. B. 2005. Endless forms most beautiful: the new science of Evo Devo and the making of the Animal Kingdom. W. W. Norton and Company Inc, New York, NY.
20. Chen, L., A. L. De Vries, and C.-H. C. Cheng. 1997. Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proc. Natl. Acad. Sci. USA 94:3811-3816.
21. Cheng, C.-H. C., P. A. Cziko, and C. W. Evans. 2006. Nonhepatic origin of notothenioid antifreeze reveals pancreatic synthesis as common mechanism in polar fish freezing avoidance. Proc. Natl Acad. Sci. 103:10491-10496.
22. Clabaut, C., P. M. E. Bunje, W. Salzburger, and A. Meyer. 2007. Geometric morphometric analyses provide evidence for the adaptive character of the Tanganyikan cichlid fish radiation. Evolution 61:560-578.
23. Collar, D. C., and P. C. Wainwright. 2006. Discordance between morphological and mechanical diversity in the feeding mechanism of centrarchid fishes. Evolution 60: 2575-2584.
24. Colosimo, P. F., K. E. Hosemann, S. Balabhadra, G. Villareal, M. Dickson, J. Grimwood, et al. 2005. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307:1928-1933.
25. Cooper, W. J., and M. W. Westneat. 2009. Form and function of damselfish skulls: rapid and repeated evolution into a limited number of tropic niches. BMC Evol. Biol. 9:24.
26. Cooper, W. J., K. Parsons, A. McIntyre, B. Kern, A. McGee-Moore, R. C. Albertson, et al. 2010. Bentho-pelagic divergence of cichlid feeding architecture was prodigious and consistent during multiple adaptive radiations within African rift lakes. PLoS One 5:e9551.
27. Cubbage, C. C., and P. M. Mabee. 1996. Development of the cranium and paired fins in the zebrafish Danio rerio (Ostariophysi, Cyprinidae). J. Morphol. 229:121-160.
28. Day, J. J., C. R. Peart, K. J. Brown, J. P. Friel, R. Bills, and T. Moritz. 2013. Continental diversification of an African catfish radiation (Mochokidae: Synodontis). Syst. Biol. 62:351-365.
29. Dayton, P. K., G. A. Robillia, and A. L. Devries. 1969. Anchor ice formation in McMurdo Sound Antarctica and its biological effects. Science 163:273-274.
30. DeVries, A. L., and J. T. Eastman. 1978. Lipid sacs as a buoyancy adaptation in an Antarctic fish. Nature 271: 352-353.
31. DeWitt, H. H. 1985. Reports on fishes of the University of Southern California Antarctic Research Program, 1962-1968. I. A review of the genus Bathydraco Günther (family Bathydraconidae). Cybium 9:295-314.
32. Dyreson, E., and W. P. Maddison. 2003. Rhetenor package for morphometrics for the Mesquite system.
33. Eakin, R. R., J. T. Eastman, and T. J. Near. 2009. A new species and a molecular phylogenetic analysis of the Antarctic fish genus Pogonophryne (Notothenioidei: Artedidraconidae). Copeia 4:705-713.
34. Eastman, J. T. 1993. Antarctic fish biology: evolution in a unique environment. Academic Press, San Diego.
35. Eastman, J. T. 2005. The nature of the diversity of Antarctic fishes. Polar Biol. 28:93-107.
36. Eastman, J. T., and A. L. DeVries. 1982. Buoyancy studies of notothenioid fishes in McMurdo Sound, Antarctica. Copeia 2:385-393.
37. Eastman, J. T., and A. R. McCune. 2000. Fishes on the Antarctic continental shelf: evolution of a marine species flock? J. Fish Biol. 57:84-102.
38. Ekau, W. 1991. Morphological adaptations and mode of life in high Antarctic fish. Pp. 23-39 in G. di Prisco, B. Maresca and B. Tota, eds. Biology and Antarctic fish. Springer, Berlin.
39. Erwin, D. H. 2007. Disparity: morphological pattern and developmental context. Palaeontology 50:57-73.
40. Fanta, E., F. S. Rios, L. Donatti, and W. E. Cardoso. 2003. Spatial and temporal variation in krill consumption by the Antarctic fish Notothenia coriiceps, in Admiralty Bay, King George Island. Antarct. Sci. 15:458-462.
41. Fischer, W., and J. C. Hureau. 1985. FAO species identification sheets for fishery purposes. South Ocean: fishing areas 48, 58 and 88 (CCAMLR convention area). Vol. 1. Food and agriculture organization of the United Nations, Rome.
42. Foster, B. A., and J. C. Montgomery. 1993. Planktivory in benthic nototheniid fish in McMurdo Sound, Antarctica. Environ. Biol. Fishes 35:313-318.
43. Gavrilets, S., and J. B. Losos. 2009. Adaptive radiation: contrasting theory with data. Science 323:732-737.
44. Gavrilets, S., and A. Vose. 2005. Dynamic patterns of adaptive radiation. Proc. Natl. Acad. Sci. USA 102:18040-18045.
45. Gerking, S. D. 1994. Feeding ecology of fish. Academic Press, San Diego.
46. Glor, R. E. 2010. Phylogenetic insights on adaptive radiation. Annu. Rev. Ecol. Evol. Syst. 41:251-270.
47. Gon, O., and P. C. Heemstra. 1990. Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown.
48. Gould, S. J. 1989. Wonderful life: the burgess shale and the nature of history. W. W. Norton and Co, New York, NY.
49. Grant, P. R., and B. R. Grant. 2006. Evolution of character displacement in Darwin's finches. Science 313:224-226.
50. Grubich, J. R., A. N. Rice, and M. W. Westneat. 2008. Functional morphology of bite mechanics in the great barracuda (Sphyraena barracuda). Zoology 111:16-29.
51. Hansen, T. F., J. Pienaar, and S. H. Orzack. 2008. A comparative method for studying adaptation to a randomly evolving environment. Evolution 62:1965-1977.
52. Harder, L. D. 2001. Mode and tempo of species diversification. Am. J. Bot. 88:1707-1710.
53. Harmon, L. J., J. A. Schulte, A. Larson, and J. B. Losos. 2003. Tempo and mode of evolutionary radiation in iguanian lizards. Science 301:961-964.
54. Harmon, L. J., J. T. Weir, C. D. Brock, R. E. Glor, and W. Challenger. 2008. GEIGER: investigating evolutionary radiations. Bioinformatics 24:129-131.
55. Harmon, L. J., J. B. Losos, T. J. Davies, R. G. Gillespie, J. L. Gittleman, W. B. Jennings, et al. 2010. Early burst of body size and shape evolution are rare in comparative data. Evolution 64:2385-2396.
56. Harrod, C., J. Mallela, and K. K. Kahilainen. 2010. Phenotype-environment correlations in a putative whitefish adaptive radiation. J. Anim. Ecol. 79:1057-1068.
57. Hobson, K. A., J. F. Piatt, and J. Pitocchelli. 1994. Using stable isotopes to determine seabird trophic relationships. J. Anim. Ecol. 63:786-798.
58. Hofmann, G. E., S. G. Lund, S. P. Place, and A. C. Whitmer. 2005. Some like it hot, some like it cold: the heat shock response is found in New Zealand but not Antarctic notothenioid fishes. J. Exp. Mar. Biol. Ecol. 316:79-89.
59. Holzman, R., and P. C. Wainwright. 2009. How to surprise a copepod: strike kinematics reduce hydrodynamic disturbance and increase stealth of suction-feeding fish. Limnol. Oceanogr. 54:2201-2212.
60. Holzman, R., D. C. Collar, S. A. Price, C. D. Hulsey, R. C. Thomson, and P. C. Wainwright. 2012. Biomechanical trade-offs bias rates of evolution in the feeding apparatus of fishes. Proc. Biol. Sci. 279:1287-1292.
61. Hughes, G. M. 1960. A comparative study of gill ventilation in marine teleosts. J. Exp. Biol. 37:28-45.
62. Hunt, G., and M. T. Carrano. 2010. Models and methods for analysing phenotypical evolution in lineages and clades. Pp. 245-269 in J. Alroy and G. Hunt, eds. Quantitative methods in paleobiology. Paleontological Society Short Course, 30 October 2010. Vol. 16. The Paleontological Society Papers, Boulder, CO.
63. Hunt, B. M., K. Hoefling, and C.-H. Cheng. 2003. Annual warming episodes in seawater temperatures in McMurdo Sound in relationship to endogenous ice in notothenioid fish. Antarct. Sci. 15:333-338.
64. Iken, K., E. R. Barrera-Oro, M. L. Quartino, R. J. Casaux, and T. Brey. 1997. Grazing by the Antarctic fish Notothenia coriiceps: evidence for selective feeding on macroalgae. Antarcti. Sci. 9:386-391.
65. Ingram, T., L. J. Harmon, and J. B. Shurin. 2012. When should we expect early bursts of trait evolution in comparative data? Predictions from an evolutionary food web model. J. Evol. Biol. 25:1902-1910.
66. Jackson, D. A. 1993. Stopping rules in principal components analysis: a comparison of heuristical and statistical approaches. Ecology 74:2204-2214.
67. Jones, F. C., M. G. Grabherr, Y. F. Chan, P. Russell, E. Mauceli, J. Johnson, et al. 2012a. The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484:55-61.
68. Jones, F. C., Y. F. Chan, J. Schmutz, J. Grimwood, S. Brady, A. M. Southwick, et al. 2012b. A genome-wide SNP genotyping array reveals patterns of global and repeated species pair divergence in sticklebacks. Curr. Biol. 22:83-90.
69. Kimmel, C. B., A. DeLaurier, B. Ullmann, J. Dowd, and M. McFadden. 2010. Modes of developmental outgrowth and shaping of a craniofacial bone in zebrafish. PLoS ONE 5:e9475.
70. Kimmel, C. B., B. Ullmann, C. Walker, C. Wilson, M. Currey, P. C. Phillips, et al. 2005. Evolution and development of facial bone morphology in threespine sticklebacks. Proc. Natl. Acad. Sci. USA 102:5791-5796.
71. Kimmel, C. B., W. E. Aguirre, B. Ullmann, M. Currey, and W. A. Cresko. 2008. Allometric change accompanies opercular shape evolution in Alaskan threespine sticklebacks. Behaviour 145:669-691.
72. Kimmel, C. B., W. A. Cresko, P. C. Phillips, B. Ullmann, M. Currey, F. von Hippel, et al. 2011. Independent axes of genetic variation and parallel evolutionary divergence of opercle bone shape in threespine stickleback. Evolution 66:419-434.
73. Klingenberg, C. P. 2010. Evolution and development of shape: integrating quantitative approaches. Nat. Rev. Genet. 11:623-635.
74. Klingenberg, C. P., and E. Ekau. 1996. A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae). Biol. J. Linn. Soc. 59:143-177.
75. Kocher, T. D. 2004. Adaptive evolution and explosive speciation: the cichlid fish model. Nat. Rev. Genet. 5:288-298.
76. Kock, K. H. 2005. Antarctic fishes (Channichthyidae): a unique family of fishes. A review, part I. Polar Biol. 28:862-895.
77. Krieger, J. D., R. P. Guralnick, and D. M. Smith. 2007. Generating empirically determined continuous measures of leaf shape for paleoclimate reconstruction. Palaios 22:212-219.
78. La Mesa, M., J. T. Eastman, and M. Vacchi. 2004. The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol. 27:321-338.
79. Lau, Y.-T., S. K. Parker, T. J. Near, and H. W. III Detrich. 2012. Evolution and function of the globin intergenic regulatory regions of the Antarctic dragonfishes (Notothenioidei: Bathydraconidae). Mol. Biol. Evol. 29:1071-1080.
80. Lauder, G. 1979. Feeding mechanics in primitive teleosts and in the halecomorph fish Amia calva. J. Zool. 187:543-578.
81. Lauder, G. V. 1983. Functional design and evolution of pharyngeal jaw apparatus in Euteleostean fishes. Zool. J. Linn. Soc. 77:1-38.
82. Losos, J. B. 2009. Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. Univ. of California Press, Berkley.
83. MacLeod, N. 1999. Generalizing and extending the eigenshape method of shape space visualization and analysis. Paleobiology 25:107-138.
84. Maddison, W. P., and D. R. Maddison. 2011. Mesquite: a modular system for evolutionary analysis. Version 2.75. Available at http://mesquiteproject.org.
85. Makinen, H. S., and J. Merila. 2008. Mitochondrial DNA phylogeography of the three spined stickleback (Gasterosteus aculeatus) in Europe - evidence for multiple glacial refugia. Mol. Phylogenet. Evol. 46:167-182.
86. Marroig, G., and J. M. Cheverud. 2005. Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in new world monkeys. Evolution 59:1128-1142.
87. Marroig, G., and J. M. Cheverud. 2010. Size as a line of least resistance II: direct selection on size or correlated response due to constraints? Evolution 64:1470-1488.
88. Matschiner, M., R. Hanel, and W. Salzburger. 2011. On the origin and trigger of the notothenioid adaptive radiation. PLoS One 6:18911.
89. McPeek, M. A. 2008. The ecological dynamics of clade diversification and community assembly. Am. Nat. 172:E270-E284.
90. Mehta, R. S., and P. C. Wainwright. 2008. Functional morphology of the pharyngeal jaw apparatus in moray eels. J. Morphol. 269:604-619.
91. Mitteroecker, P., and P. Gunz. 2009. Advances in geometric morphometrics. Evol. Biol. 36:235-247.
92. Muschick, M., M. Barluenga, W. Salzburger, and A. Meyer. 2011. Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evol. Biol. 11:116.
93. Muschick, M., A. Indermaur, and W. Salzburger. 2012. Convergent evolution within an adaptive radiation of cichlid fishes. Curr. Biol. 22:1-7.
94. Near, T. J., A. Dornburg, K. L. Kuhn, J. T. Eastman, J. N. Pennington, T. Patarnello, et al. 2012. Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc. Natl. Acad. Sci. USA 109:3434-3439.
95. Olson, M. E., and A. Arroyo-Santos. 2009. Thinking in continua: beyond the "adaptive radiation" metaphor. Bioessays 31:1337-1346.
96. Pigliucci, M. 2008. Sewall Wright's adaptive landscapes: 1932 vs. 1988. Biol. Philos. 23:591-603.
97. Polly, P. D. 2003. Paleophylogeography: the tempo of geographic differentiation in marmots (Marmota). J. Mammal. 84:369-384.
98. Post, D. M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703-718.
99. Raff, R. A. 2007. Written in stone: fossils, genes and evo-devo. Nat. Rev. Genet. 8:911-920.
100. Reid, W. D. K., S. Clarke, M. A. Collins, and M. Belchier. 2007. Distribution and ecology of Chaenocephalus aceratus (Channichthyidae) around South Georgia and Shag Rocks (Southern Ocean). Polar Biol. 30:1523-1533.
101. Rohlf, F. J. 2001. Comparative methods for the analysis of continuous variables: geometric interpretations. Evolution 55:2143-2160.
102. Rohlf, F. J. 2010. tpsDig Version 2.16. Department of Ecology and Evolution, State University of New York at Stony Brook, New York, NY.
103. Rutschmann, S., M. Matschiner, M. Damerau, M. Muschick, M. F. Lehmann, R. Handel, et al. 2011. Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation. Mol. Ecol. 20:4707-4721.
104. Salazar-Ciudad, I. 2006. On the origins of morphological disparity and its diverse developmental bases. Bioessays 28:1112-1122.
105. Sallan, L. C., and M. Friedman. 2012. Heads or tails: staged diversification in vertebrate evolutionary radiations. Proc. Biol. Sci. 279:2025-2032.
106. Salzburger, W. 2009. The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol. Ecol. 18:169-185.
107. Sánchez-Villagra, M. R. 2010. Developmental palaeontology in synapsids: the fossil record of ontogeny in mammals and their closest relatives. Proc. Biol. Sci. 277:1139-1147.
108. Santos, M. E., and W. Salzburger. 2012. How cichlids diversify. Science 338:619-621.
109. Schluter, D. 2000. The ecology of adaptive radiation. Oxford Univ. Press, New York, NY. 296 pp.
110. Schluter, D., and J. D. McPhail. 1992. Ecological character displacement and speciation in sticklebacks. Am. Nat. 140:85-108.
111. Seehausen, O. 2006. African cichlid fish: a model system in adaptive radiation research. Proc. Biol. Sci. 273:1987-1998.
112. Seehausen, O. 2007. Chance, historical contingency and ecological determinism jointly determine the rate of adaptive radiation. Heredity 99:361-363.
113. Shapiro, M. D., M. E. Marks, C. L. Peichel, B. K. Blackman, K. S. Nereng, B. Jonsson, et al. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428:717-723.
114. Sidlauskas, B. L. 2008. Continuous and arrested morphological diversification in sister clades of characiform fishes: a phylomorphospace approach. Evolution 62:3135-3156.
115. Simpson, G. G. 1953. The major features of evolution. Columbia Univ. Press, New York, NY.
116. 2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326:1394-1397.
117. Wagenmakers, E., and S. Farrel. 2004. AIC model selection using Akaike weights. Psychon. Bull. Rev. 11:192-196.
118. Wainwright, P. C. 1996. Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology 77:1336-1343.
119. Westneat, M. W. 2006. Skull biomechanics and suction feeding in fishes. Pp. 29-75 in G. V. Lauder and R. E. Shadwick, eds. Fish biomechanics. Elsevier Academic Press, San Diego, CA.
120. Westneat, M. W., M. E. Alfaro, P. C. Wainwright, D. R. Bellwood, J. R. Grubich, J. L. Fessler, et al. 2005. Local phylogenetic divergence and global evolutionary convergence of skull function in reef fishes of the family Labridae. Proc. Biol. Sci. 272:992-1000.
121. Willacker, J. J., F. A. Von Hippel, P. R. Wilton, and K. M. Walton. 2010. Classification of threespine stickleback along the benthic-limnetic axis. Biol. J. Linn. Soc. 101:595-608.
122. Wilson, L. A. B. 2013a. Geographic variation in the greater Japanese shrew-mole, Urotrichus talpoides: combining morphological and chromosomal patterns. Mamm. Biol. 78:267-275.
123. Wilson, L. A. B. 2013b. The contributions of developmental palaeontology to extensions of evolutionary theory. Acta Zool. 94:254-260.
124. Wilson, L. A., N. MacLeod, and L. T. Humphrey. 2008. Morphometric criteria for sexing juvenile human skeletons using the ilium. J. Forensic Sci. 53:269-278.
125. Wilson, L. A. B., H. F. V. Cardoso, and L. T. Humphrey. 2011. A blind test of six criteria of the juvenile ilium. Forensic Sci. Int. 206:35-42.
126. Wilson, L. A. B., H. Furrer, R. Stockar, and M. R. Sánchez-Villagra. 2013. A quantitative evaluation of evolutionary patterns in opercle bone shape in Saurichthys (Actinopterygii: Saurichthyidae). Palaeontology 56: 901-915.
127. Wright, S. 1932. The role of mutation, inbreeding, crossbreeding, and selection in evolution. Proc. 6th Internat. Congr. Genet.1:356-366
128. Young, K. A., J. Snoeks, and O. Seehausen. 2009. Morphological diversity and the roles of contingency, changes and determinism in African cichlid radiations. PLoS One 4:e4740.
129. Zahn, C. T., and R. Z. Roskies. 1972. Fourier shape descriptors for closed plane curves. IEEE T. Comput. C-21:269-281.
130. Zelditch, M. L., D. L. Swiderski, and H. D. Sheets. 2004. Geometric morphometrics for biologists: a primer. Elsevier Academic Press, London.