Selection of landmarks and semilandmarks in fishes for geometric morphometric analyses: a comparative study based on analytical methods
DOI:
https://doi.org/10.3989/scimar.04280.15AKeywords:
morphological traits, landmarks, geometric morphometrics, diversity, point pattern, morphospace, marine fishesAbstract
We applied and compared three different sets of landmarks and semilandmarks commonly used in studies of fish assemblages to identify a standardized method of landmark selection that includes the maximum amount of morphological information of species. The different landmark-based methods used produced differences regarding the distribution of case-study species within the morphospace. We suggest that adding landmarks and semilandmarks that provide more specific information about anatomical structures with important roles in the biology of species, such as transformed fins or sensory organs, contributes to a clearer differentiation of species within the morphospace and a better interpretation of their occupancy. In addition, three types of method were used to establish how species are distributed within morphospace. The results demonstrated that aggregation points methods, including analyses based on quadrants or distances, are more appropriate for this purpose than indices of morphological disparity. The results also confirmed that although numerical methods are needed to test the statistical significance of outcomes, graphical methods provide a more intuitive interpretation of morphospace occupancy. The kernel density and Gabriel graph were useful to infer the morphospace zone where species are more densely grouped, improving the knowledge of space occupancy and structural complexity of fish assemblages.
Downloads
References
Adams D.C., Rohlf F.J., Slice D.E. 2013. A field comes of age: geometric morphometrics in the 21st century. Hystrix It. J. Mamm. 24: 7-14.
Anderson R.M., Gordon D.M., Crawley M.J., et al. 1982. Variability in the abundance of animal and plant species. Nature 296: 245-248. http://dx.doi.org/10.1038/296245a0
Angeles A.D.J., Gorospe J.G., Torres M.A.J., et al. 2014. Length-weight relationship, body shape variation and asymmetry in body morphology of Siganus guttatus from selected areas in five Mindanao bays. Int. J. Aqu. Sci. 5: 40-57.
Azzurro E., Tuset V.M., Lombarte A., et al. 2014. External morphology explains the success of biological invasions. Ecol. Lett. 17: 1455-1463. http://dx.doi.org/10.1111/ele.12351 PMid:25227153
Bellwood D.R., Wainwright P.C., Fulton C.J., et al. 2006. Functional versatility supports coral reef biodiversity. Proc. R. Soc. B 273: 101-107. http://dx.doi.org/10.1098/rspb.2005.3276 PMid:16519241 PMCid:PMC1560014
Bookstein F.L. 1991. Morphometric Tools for Landmark Data. Geometry and Biology. Cambridge University Press, New York.
Cadrin S.X. 2000. Advances in morphometric identification of fishery stocks. Rev. Fish Biol. Fish. 10: 91-112. http://dx.doi.org/10.1023/A:1008939104413
Cavalcanti M.J., Monteiro L.R., Lopes P.R.D. 1999. Landmark-based morphometric analysis in selected species of serranid fishes (Perciformes: Teleostei). Zool. Stud. 38: 287-294.
Chakrabarty P. 2005. Testing conjectures about morphological diversity in cichlids of lakes Malawi and Tanganyika. Copeia 2005: 359-373. http://dx.doi.org/10.1643/CG-04-089R2
Ciampaglio C.N., Kemp M., McShea D.W. 2001. Detecting changes in morphospace occupation patterns in the fossil record: characterization and analysis of measures of disparity. Paleobiology 27: 695-715. http://dx.doi.org/10.1666/0094-8373(2001)027<0695:DCIMOP>2.0.CO;2
Clabaut C., Bunje P.M.E., Salzburger W., et al. 2007. Geometric morphometric analyses provide evidence for the adaptative character of the Tanganyikan cichlid fish radiations. Evolution 61: 560-578. http://dx.doi.org/10.1111/j.1558-5646.2007.00045.x PMid:17348920
Clark P.J., Evans F.C. 1954. Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35: 445-453. http://dx.doi.org/10.2307/1931034
Cooper W.J., Westneat M.W. 2009. Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches. BMC Evol. Biol. 9: 24. http://dx.doi.org/10.1186/1471-2148-9-24 PMid:19183467 PMCid:PMC2654721
Cornwell W.K., Schwilk D.W., Ackerly D.D. 2006. A trait-based test for habitat filtering: convex hull volume. Ecology 87: 1465-1471. http://dx.doi.org/10.1890/0012-9658(2006)87[1465:ATTFHF]2.0.CO;2
Costa C., Cataudella S. 2007. Relationship between shape and trophic ecology of selected species of Sparids of the Caprolace coastal lagoon (Central Tyrrhenian sea). Environ. Biol. Fish. 78: 115-123. http://dx.doi.org/10.1007/s10641-006-9081-9
Dale M.R.T., Fortin M.J. 2010. From graphs to spatial graphs. Annu. Rev. Ecol. Evol. Syst. 41: 21-38. http://dx.doi.org/10.1146/annurev-ecolsys-102209-144718
Davenport J. 1994. How and why do flying fish fly? Rev. Fish Biol. Fish. 40: 184-214. http://dx.doi.org/10.1007/BF00044128
Davis J.C. 1986. Statistics and data analysis in geology. John Wiley & Sons, New York.
De Schepper N., De Kegel B., Adriaens D. 2007. Morphological specializations in Heterocongrinae (Anguilliformes: Congridae) related to burrowing and feeding. J. Morphol. 268: 343-356. http://dx.doi.org/10.1002/jmor.10525 PMid:17351957
Dixon P.M. 2002. Ripley's K function. In: El-Shaarawi A.H., Piergorsch W.W. (eds), Encyclopedia of Environmetrics, vol. 3, John Wiley & Sons, New York, USA, pp. 1796-1803.
Dornburg A., Sidlauskas B., Santini F., et al. 2011. The influence of an innovative locomotor strategy on the phenotypic diversification of triggerfish (Family: Balistidae). Evolution 65: 1912-1926. http://dx.doi.org/10.1111/j.1558-5646.2011.01275.x PMid:21729047
Douglas M.E., Matthews W.J. 1992. Does morphology predict ecology? Hypothesis testing within a freshwater stream fish assemblage. Oikos 65: 213-224. http://dx.doi.org/10.2307/3545012
Dryden I.L., Mardia K.V. 1998. Statistical shape analysis. John Wiley & Sons, New York, 376 pp.
Farré M., Tuset V.M., Maynou F., et al. 2013. Geometric morphology as an alternative for measuring the diversity of fish assemblages. Ecol. Indic. 29: 159-166. http://dx.doi.org/10.1016/j.ecolind.2012.12.005
Farré M., Lombarte A., Recasens L., et al. 2015. Habitat influence in the morphological diversity of coastal fish assemblages. J. Sea Res. 99: 107-117. http://dx.doi.org/10.1016/j.seares.2015.03.002
Foote M. 1997. The evolution of morphological diversity. Annu. Rev. Ecol. Syst. 28: 129-152. http://dx.doi.org/10.1146/annurev.ecolsys.28.1.129
Fortin M.J., Keitt T.H., Maurer B.A., et al. 2005. Species' geographic ranges and distributional limits: pattern analysis and statistical issues. Oikos 108: 7-17. http://dx.doi.org/10.1111/j.0030-1299.2005.13146.x
Friedman M. 2010. Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction. Proc. R. Soc. B 277: 1675-1683. http://dx.doi.org/10.1098/rspb.2009.2177 PMid:20133356 PMCid:PMC2871855
Gabriel K.R., Sokal R.R. 1969. A new statistical approach to geographic variation analysis. Syst. Biol. 18: 259-278. http://dx.doi.org/10.2307/2412323
Gatz Jr. A.J. 1979. Community organization in fishes as indicated by morphological features. Ecology 60: 711-718. http://dx.doi.org/10.2307/1936608
Gosline W.A. 1994. Function and structure in the paired fins of scorpaenifom fishes. Environ. Biol. Fish. 40: 219-226. http://dx.doi.org/10.1007/BF00002508
Hutchings K., Griffiths M.H. 2005. Identity and distribution of southern African sciaenid fish species of the genus Umbrina. Afr. J. Mar. Sci. 27: 1-21. http://dx.doi.org/10.2989/18142320509504064
Jamon M., Renous S., Gasc J.P., et al. 2007. Evidence of force exchanges during the six-legged walking of the bottom-dwelling fish, Chelidonichthys lucerna. J. Exp. Zool. 307A: 542-547. http://dx.doi.org/10.1002/jez.401 PMid:17620306
Kassam D.D., Adams D.C., Ambali A.J.D., et al. 2003. Body shape variation in relation to resource partitioning within cichlid trophic guilds coexisting along the rocky shore of Lake Malawi. Anim. Biol. 53: 59-70. http://dx.doi.org/10.1163/157075603769682585
Kasumyan A.O. 2011. Tactile reception and behavior of fish. J. Ichthyol. 51: 1035-1103. http://dx.doi.org/10.1134/S003294521111004X
Klingenberg C.P. 2010. Evolution and development of shape: integrating quantitative approaches. Nat. Rev. Genet. 11: 623-635. http://dx.doi.org/10.1038/nrg2829
Klingenberg C.P., Ekau W. 1996. A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae). Biol. J. Linn. Soc. 59: 143-177. http://dx.doi.org/10.1111/j.1095-8312.1996.tb01459.x
Korn D., Hopkins M.J., Walton S.A. 2013. Extinction space – A method for the quantification and classification of changes in morphospace across extinction boundaries. Evolution 67: 2795-2810. http://dx.doi.org/10.1111/evo.12162
Laurenson C.H., Hudson I.R., Jones D.O.B., et al. 2004. Deep water observations of Lophius piscatorius in the north-eastern Atlantic Ocean by means of a remotely operated vehicle. J. Fish Biol. 65: 947-960. http://dx.doi.org/10.1111/j.0022-1112.2004.00496.x
Layman C.A., Langerhans R.B., Winemiller K.O. 2005. Body size, not other morphological traits, characterizes cascading effects in fish assemblage composition following commercial netting. Can. J. Fish. Aquat. Sci. 62: 2802-2810. http://dx.doi.org/10.1139/f05-183
Liao J.C. 2002. Swimming in needlefish (Belonidae): anguilliform locomotion with fins. J. Exp. Biol. 205: 2875-2884. PMid:12177151
Lombarte A., Aguirre H. 1997. Quantitative differences in the chemoreceptor systems in the barbels of two species of Mullidae (Mullus surmuletus and M. barbatus) with different bottom habitats. Mar. Ecol. Prog. Ser. 150: 57-64. http://dx.doi.org/10.3354/meps150057
Lombarte A., Gordoa A., Whitfield A.K., et al. 2012. Ecomorphological analysis as a complementary tool to detect changes in fish communities following major perturbations in two South African estuarine systems. Environ. Biol. Fish. 94: 601-614. http://dx.doi.org/10.1007/s10641-011-9966-0
Loy A., Boglione C., Cataudella S. 1999. Geometric morphometrics and morpho-anatomy: a combined tool in the study of seabream (Sparus aurata, Sparidae) shape. J. Appl. Ichthyol. 15: 104-110. http://dx.doi.org/10.1046/j.1439-0426.1999.00116.x
Loy A., Bertelletti M., Costa C., et al. 2001. Shape changes and growth trajectories in the early stages of three species of the genus Diplodus (Perciformes, Sparidae). J. Morphol. 250: 24-33. http://dx.doi.org/10.1002/jmor.1056 PMid:11599013
McClain C.R., Johnson N.A., Rex M.A. 2004. Morphological disparity as a biodiversity metric in lower bathyal and abyssal gastropod assemblages. Evolution 58: 338-348. http://dx.doi.org/10.1554/03-237
Mercader L., Lloris D., Rucabado J.A. 2001. Tots els peixos del mar Català: Diagnosis i claus d'identificació. Institut d'Estudis Catalans, Barcelona.
Nelson J.S. 2006. Fishes of the World, 4rth edition. Wiley and Sons, New Jersey.
Perry G.L.W., Miller B.P., Enright N.J. 2006. A comparison of methods for the statistical analysis of spatial point patterns in plant ecology. Plant Ecol. 187: 59-82. http://dx.doi.org/10.1007/s11258-006-9133-4
Pie M.R., Traniello J.F.A. 2007. Morphological evolution in a hyperdiverse clade: the ant genus Pheidole. J. Zool. 271: 99-109. http://dx.doi.org/10.1111/j.1469-7998.2006.00239.x
Recasens L., Lombarte A., Sánchez P. 2006. Teleostean fish composition and structure of an artificial reef and a natural rocky area in Catalonia (North Western Mediterranean). Bull. Mar. Sci. 78: 71-82.
Ricklefs R.E. 2012. Species richness and morphological diversity of passerine birds. Proc. Natl. Acad. Sci. USA 109: 14482-14487. http://dx.doi.org/10.1073/pnas.1212079109 PMid:22908271 PMCid:PMC3437851
Ripley B.D. 1979. Tests of 'randomness' for spatial point patterns. J. Roy. Stat. Soc. B 41: 368-374.
Rohlf F.J. 2003a. TpsDig Version 2.16. Department of Ecology and Evolution, State University of New York at Stony Brook, New York.
Rohlf F.J. 2003b. TpsSmall Version 1.28. Department of Ecology and Evolution, State University of New York at Stony Brook, New York.
Rohlf F.J. 2003c. TpsRelw Version 1.49. Department of Ecology and Evolution, State University of New York at Stony Brook, New York.
Rohlf F.J., Marcus L.F. 1993. A Revolution in Morphometrics. Trends Ecol. Evol. 8: 129-132. http://dx.doi.org/10.1016/0169-5347(93)90024-J
Rüber L., Adams D.C. 2001. Evolutionary convergence of body shape and trophic morphology in cichlids from Lake Tanganyika. J. Evol. Biol. 14: 325-332. http://dx.doi.org/10.1046/j.1420-9101.2001.00269.x
Russell E.S. 1916. Form and function: a contribution to the history of animal morphology. American edition. EP Dutton and Co., New York. http://dx.doi.org/10.5962/bhl.title.3747
Schoenfuss H.L., Blob R.W. 2003. Kinematics of waterfall climbing in Hawaiian freshwater fishes (Gobiidae): vertical propulsion at the aquatic-terrestrial interface. J. Zool. 261: 191-205. http://dx.doi.org/10.1017/S0952836903004102
Shen B., Dong L., Xiao S., et al. 2008. The Avalon explosion: evolution of Ediacara morphospace. Science 319: 81-84. http://dx.doi.org/10.1126/science.1150279 PMid:18174439
Silverman B.W. 1986. Density estimation for statistics and data analysis. Monographs on Statistics and Applied Probability, Chapman and Hall, London. http://dx.doi.org/10.1007/978-1-4899-3324-9
Smith U.E., Hendricks J.R. 2013. Geometric morphometric character suites as phylogenetic data: extracting phylogenetic signal from gastropod shells. Syst. Biol. 62: 366-385. http://dx.doi.org/10.1093/sysbio/syt002 PMid:23325808
Strauss R.E., Bookstein F.L. 1982. The truss: body form reconstructions in morphometrics. Syst. Biol. 31: 113-135. http://dx.doi.org/10.1093/sysbio/31.2.113
Strogatz S.H. 2001. Exploring complex networks. Nature 410: 268-276. http://dx.doi.org/10.1038/35065725 PMid:11258382
Thompson D.W. 1915. Morphology and mathematics. T. Roy. Soc. Edin. 50: 857-895. http://dx.doi.org/10.1017/S0080456800017105
Tuset V.M., Farré M., Lombarte A., et al. 2014. A comparative study of morphospace occupation of mesopelagic fish assemblages from the Canary Islands (North-eastern Atlantic). Ichthyol. Res. 61: 152-158. http://dx.doi.org/10.1007/s10228-014-0390-2
Tytell E.D., Lauder G.V. 2004. The hydrodynamics of eel swimming I. Wake structure. J. Exp. Biol. 207: 1825-1841. http://dx.doi.org/10.1242/jeb.00968 PMid:15107438
Valentin A., Sévigny J.M., Chanut J.P. 2002. Geometric morphometrics reveals body shape differences between sympatric redfish Sebastes mentella, Sebastes fasciatus and their hybrids in the Gulf of St Lawrence. J. Fish. Biol. 60: 857-875. http://dx.doi.org/10.1006/jfbi.2002.1889
Van Bocxlaer B., Schultheiß R. 2010. Comparison of morphometric techniques for shapes with few homologous landmarks based on machine-learning approaches to biological discrimination. Paleobiology 36: 497-515. http://dx.doi.org/10.1666/08068.1
Vergara-Solana F.J., García-Rodriguez F.J., Tavera J.J., et al. 2014. Molecular and morphometric systematics of Diapterus (Perciformes, Gerreidae). Zool. Scripta 43: 338-350. http://dx.doi.org/10.1111/zsc.12054
Villéger S., Ramos Miranda J., Flores Hernandez D., et al. 2010. Contrasting changes in taxonomic and functional diversity of tropical fish communities after habitat degradation. Ecol. Appl. 20: 1512-1522. http://dx.doi.org/10.1890/09-1310.1 PMid:20945756
Wainwright P.C., Belwood D.R., Westneat M.W. 2002. Ecomorphology of locomotion in labrid fishes. Environ. Biol. Fish. 65: 47-62. http://dx.doi.org/10.1023/A:1019671131001
Walker J.A. 2010. An integrative model of evolutionary covariance: a symposium on body shape in fishes. Integr. Comp. Biol. 50: 1051-1056. http://dx.doi.org/10.1093/icb/icq014 PMid:21558259
Werdelin L., Lewis M.E. 2013. Temporal change in functional richness and evenness in the Eastern African Plio-Pleistocene carnivoran guild. PLoS ONE 8: e57944. http://dx.doi.org/10.1371/journal.pone.0057944 PMid:23483948 PMCid:PMC3590191
Wiegand T., Moloney K.A. 2004. Rings, circles, and null-models for point pattern analysis in ecology. Oikos 104: 209-229. http://dx.doi.org/10.1111/j.0030-1299.2004.12497.x
Willis S.C., Winemiller K.O., Lopez-Fernandez H. 2005. Habitat structural complexity and morphological diversity of fish assemblages in a Neotropical floodplain river. Oecologia 142: 284-295. http://dx.doi.org/10.1007/s00442-004-1723-z PMid:15655689
Wills M.A. 2001. Morphological disparity: a primer. In: Adrain J.M., Edgecombe G.D., Lieberman B.S. (eds), Fossils, phylogeny, and form: an analytical approach. Kluwer Academic/ Plenum Publishers, New York. pp 55-144. http://dx.doi.org/10.1007/978-1-4615-0571-6_4
Winemiller K.O. 1991. Ecomorphological diversification in lowland fresh-water fish assemblages from five biotic regions. Ecol. Monogr. 61: 343-365. http://dx.doi.org/10.2307/2937046
Worton B.J. 1989. Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70: 164-168. http://dx.doi.org/10.2307/1938423
Yamanoue Y., Setiamarga D.H.E., Matsuura K. 2010. Pelvic fins in teleosts: structure, function and evolution. J. Fish. Biol. 77: 1173-1208. http://dx.doi.org/10.1111/j.1095-8649.2010.02674.x PMid:21039499
Young K.A., Snoeks J., Seehausen O. 2009. Morphological diversity and the roles of contingency, chance and determinism in African cichlid radiations. PLoS ONE 4: e4740. http://dx.doi.org/10.1371/journal.pone.0004740 PMid:19270732 PMCid:PMC2648897
Zelditch M.L., Swidersky D.L., Sheeds H.D., et al. 2004. Geometric morphometrics for biologists: a primer. Elsevier Academic Press, London. PMCid:PMC1571426
Zuanon J., Bockmann F.A., Sazima I. 2006. A remarkable sand-dwelling fish assemblage from central Amazonia, with comments on the evolution of psammophily in South American freshwater fishes. Neotrop. Ichthyol. 4: 107-118. http://dx.doi.org/10.1590/S1679-62252006000100012
Published
How to Cite
Issue
Section
License
Copyright (c) 2016 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the print and online versions of this journal are the property of the Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.
All contents of this electronic edition, except where otherwise noted, are distributed under a Creative Commons Attribution 4.0 International (CC BY 4.0) licence. You may read here the basic information and the legal text of the licence. The indication of the CC BY 4.0 licence must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the final version of the work produced by the publisher, is not allowed.