Scientia Marina, Vol 80, No 2 (2016)

Selection of landmarks and semilandmarks in fishes for geometric morphometric analyses: a comparative study based on analytical methods


https://doi.org/10.3989/scimar.04280.15A

Marc Farré
Institut de Ciències del Mar, CSIC , Spain

Víctor M. Tuset
Institut de Ciències del Mar, CSIC , Spain

Francesc Maynou
Institut de Ciències del Mar, CSIC , Spain

Laura Recasens
Institut de Ciències del Mar, CSIC , Spain

Antoni Lombarte
Institut de Ciències del Mar, CSIC , Spain

Abstract


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.

Keywords


morphological traits; landmarks; geometric morphometrics; diversity; point pattern; morphospace; marine fishes

Full Text:


HTML PDF XML

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




Copyright (c) 2016 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us scimar@icm.csic.es

Technical support soporte.tecnico.revistas@csic.es