Abstract
Caiman crocodilus is an alligatoroid broadly distributed in the neotropics from Mexico to Brazil, where Colombia is the only country that has the complete subspecies complex distributed in its territory. This species has been the focus of many genetic, ecological and morphological studies. However, these studies are limited to traditional morphology methods or have limitations to examine interspecific variation among the four subspecies reported in Colombia. This is the first study of intraspecific variation in the skull of Caiman crocodilus complex distributed in Colombia, using a two-dimensional approach of geometric morphometric on 122 post-hatching ontogenetic cranial series. Morphological differences between species and changes during ontogeny (snout increases its length and, skull roof and orbits decrease their proportions) that represents part of morphological changes in the cranial ontogeny of crocodilians were found. In the morphospace, there was a significant differentiation of C. crocodilus apaporiensis and C. crocodilus crocodilus from C. crocodilus fuscus and C. crocodilus chiapasius. Results from this study revealed that C. crocodilus apaporiensis is a differentiated group from the global complex as well as that the specimens of C. crocodilus chiapasius collected from Medem in Colombia may be showing cryptic morphology in some traits.
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References
Amavet P, Vilardi JC, Rosso E, Saidman B (2009) Genetic and morphometric variability in caiman latirostris (broad-snouted caiman), reptilia, alligatoridae. J Exp Zool Part A Ecol Genet Physiol 311:258–269. https://doi.org/10.1002/jez.523
Böhmer C, Rauhut OWM, Wörheide G (2015) Correlation between Hox code and vertebral morphology in archosaurs. Proc R Soc B Biol Sci 282:20150077
Brochu CA (1999) Phylogenetics, taxonomy, and historical biogeography of Alligatoroidea. J Vertebr Paleontol 19:9–100. https://doi.org/10.1080/02724634.1999.10011201
Busack SD, Pandya S (2001) Geographic variation in Caiman crocodilus and Caiman yacare (Crocodylia: Alligatoridae): systematic and legal implications. Herpetologica 57:294–312
Busbey AB (1995) Structural consequences of skull flattening in crocodilians. In: Thomason JJ (ed) Functional morphology in vertebrate paleontology. Cambridge University Press, New York, pp 173–192
Cooke SB, Terhune CE (2015) Form, function, and geometric morphometrics. Anat Rec 298:5–28. https://doi.org/10.1002/ar.23065
Drake AG, Klingenberg CP (2008) The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc B Biol Sci 275:71–76. https://doi.org/10.1098/rspb.2007.1169
Dryden IL, Mardia KV (1998) Statistical shape analysis. John Willey, London
Escobedo-Galvan AH, Velasco JA, Gonzalez-Maya JF, Resetar A (2015) Morphometric analysis of the Rio Apaporis Caiman (Reptilia, Crocodylia, Alligatoridae). Zootaxa 4059:541–554
Fernandez Blanco MV, Cassini GH, Bona P (2018) Skull ontogeny of extant caimans: a three-dimensional geometric morphometric approach. Zoology 129:69–81. https://doi.org/10.1016/j.zool.2018.06.003
Foth C, Bona P, Desojo JB (2015) Intraspecific variation in the skull morphology of the black caiman Melanosuchus niger (Alligatoridae, Caimaninae). Acta Zool 96:1–13. https://doi.org/10.1111/azo.12045
Foth AC, Rauhut OWM, Foth C, Rauhut OWM (2019) A Morphometric approach macroevolutionary and morphofunctional patterns in theropod skulls: a morphometric approach. Acta Palaeontol Pol 58:1–16
Iordansky NN (1973) The skull of the crocodilia. Biol Reptil 4:201–261
Klingenberg CP (2010) Evolution and development of shape: integrating quantitative approaches. Nat Rev Genet 11:623–635. https://doi.org/10.1038/nrg2829
Klingenberg CP (2011) MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour 11:353–357. https://doi.org/10.1111/j.1755-0998.2010.02924.x
McNulty KP, Vinyard CJ (2015) Morphometry, geometry, function, and the future. Anat Rec Integr Anat Evol Biol 298:328–333. https://doi.org/10.1002/ar.23064
Medem F (1955) A new subspecies of Caiman sclerops from Colombia. Fieldiana Zool 37:339–344
Medem F (1960) Datos zoo-geográficos y ecológicos sobre los Crocodylia y Testudinata de los ríos Amazonas, Putumayo y Caquetá. Caldasia 8:341–351
Medem F (1971) Situation report on Crocodilians from three South American countries. In: Crocodiles. Proceedings of the first working meeting of crocodile specialists sponsored by the New York Zoological Society and organized by the Survival Service Commission, lUCN, at the Bronx Zoo, New York 15–17 March 1971. l-191. lUCN Publication New Series, New York, p 32:152–158
Medem F (1981) Los Crocodylia de Sur América. Volumen 1 Los Crocodylia de Colombia. Ministerio de Educación Nacional, Colciencias, Bogotá
Monteiro LR, Soares M (1997) Allometric analysis of the ontogenetic variation and evolution of the skull in Caiman spix, 1825 (Crocodylia: Alligatoridae). Herpetologica 53:62–69
Monteiro LR, Cavalcanti MJ, Sommer HJSS (1997) Comparative ontogenetic shape changes in the skull of Caiman species (Crocodylia. Alligatoridae). J Morphol 231:53–62. https://doi.org/10.1002/(sici)1097-4687(199701)231:1%3c53:aid-jmor5%3e3.0.co;2-p
Mook CC (1921) Skull characters of recent crocodilia with notes on the affinities of the recent genera. Bull Am Museum Nat Hist XLIV:123–268
Morales-Betancourt MA, Lasso CA, De La Ossa VJ, Fajardo-Patiño A (2013) VIII. Biología y conservación de los Crocodylia de Colombia. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (IAvH)., Bogotá, DC, Colombia
Rodríguez Melo MA (2000) Estado y distribución de los Crocodylia en Colombia. Ministerio del Medio Ambiente, Bogotá
Rohlf FJ (2017) TpsDig, version 2.30. Department of Ecology and Evolution, State University of New York at Stony Brook, New York
Rohlf FJ, Slice D (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Soc Syst Biol 39:40–59
Sadleir RW, Makovicky PJ (2008) Cranial shape and correlated characters in crocodilian evolution. J Evol Biol 21:1578–1596. https://doi.org/10.1111/j.1420-9101.2008.01602.x
Velasco A, Ayarzagüena J, Manolis S, Stevenson C (2010) Spectacled caiman Caiman crocodilus. In: Crocodiles, status survey and conservation action plan, pp 10–15
Venegas-Anaya M, Crawford AJ, Galvan AHE et al (2008) Mitochondrial DNA phylogeography of Caiman crocodilus in Mesoamerica and South America. J Exp Zool Part A Ecol Genet Physiol 309A:614–627. https://doi.org/10.1002/jez.502
Watanabe A, Slice DE (2014) The utility of cranial ontogeny for phylogenetic inference: a case study in crocodylians using geometric morphometrics. J Evol Biol 27:1078–1092. https://doi.org/10.1111/jeb.12382
Zelditch ML, Swiderski DL, Sheets HD (2012) Chapter 1 - Introduction. Geometric morphometrics for biologists, 2nd edn. Academic Press, San Diego, pp 1–20
Acknowledgements
We thank Alan Resetar, Joshua Mata and John Bates for their amazing support with this project. We also thank to the Senckenberg, Forschungsinstitute und Naturmuseen for their help. MAB is a PhD student thanks to the grant program No 647, 2014, from COLCIENCIAS, Colombia. This project was partially supported by a Field Museum of Natural History’s Science Visiting Scholarship in 2018. HB thanks to the FONDECYT DE INCIACION No. 11180366 and Proyecto Redes de Investigación REDI170182 from CONICYT.
Funding
This project was partially funded by a Science Visiting Scholarship from the Field Museum of Natural History; by FONDECYT DE INCIACION No. 11180366 and Proyecto Redes de Investigación REDI170182 from CONICYT.
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MAB designed the study, collected the samples and performed morphometric measurements of sampled material and data analyses, MAB and HAB performed statistical analysis; MAB, SC and HAB wrote the manuscript; all authors contributed in improving the draft of the manuscript by adding valuable comments.
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No live animals were used in this study. The Field Museum of Natural History allowed MAB to use their collection for this project.
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Angulo-Bedoya, M., Correa, S. & Benítez, H.A. Unveiling the cryptic morphology and ontogeny of the Colombian Caiman crocodilus: a geometric morphometric approach. Zoomorphology 138, 387–397 (2019). https://doi.org/10.1007/s00435-019-00448-2
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DOI: https://doi.org/10.1007/s00435-019-00448-2