Evolutionary ecomorphology of select species of rays distributed in the Gulf of Mexico
DOI:
https://doi.org/10.22201/ib.20078706e.2022.93.4032Keywords:
Bathomorphi, Feeding, Locomotion, Phylogenetic regression, Sexual dimorphismAbstract
Bathomorphi is a diverse lineage, accounting for more than half of the chondrichthyan diversity. Yet, more than 12.3% of the species are in the “deficient data” category of the IUCN Red List of Threatened Species, indicating a gap in the knowledge of this group. In the present study, the diet and morphological variation associated with locomotion
(disc) and feeding (Meckel’s cartilage and teeth) of 9 species of batomorphs were analyzed to assess trophic and morphological diversity, size, and sexual dimorphism. Comparative phylogenetic methods were used to determine the evolutionary relationship between variables. According to our results, the species selected showed a wide and
intricate morphological variation. Sexual dimorphism was mainly observed in tooth morphology, where males tended to have more pointed teeth than females. Disc allometry was recorded for most species; small specimens presented a longer snout than larger specimens. Only the Meckel’s cartilage was related to the diet of the species. However, the morphological variation of the disc, Meckel’s cartilage, and teeth of the batomorphs were correlated through the
evolution of the group and responded to functional patterns such as swimming and feeding, which finally, determined the ecology of the species.
References
Aguilar-Medrano, R. (2017). Ecomorphology and evolution of the pharyngeal apparatus of benthic damselfishes (Pomacentridae, subfamily Stegastinae). Marine Biology, 164, 21. https://doi.org/10.1007/s00227-016-3051-3
Aguilar-Medrano, R., Durand, J. R., Cruz-Escalona, V. H., & Moyle, P. B. (2019). Fish functional groups in the San Francisco Estuary: Understanding new fish assemblages in a highly altered estuarine ecosystem. Estuarine, Coastal and Shelf Sciences, 227, 106331. https://doi.org/10.1016/J.ECSS.2019.106331
Aguilar-Medrano, R., Frederich, B., Balart, E. F., & De Luna, E. (2013). Diversification of the pectoral fin shape in damselfishes (Perciformes, Pomacentridae) of the Eastern Pacific. Zoomorphology, 132, 197–213. https://doi.org/10.1007/s00435-012-0178-8
Albo-Puigserver, M., Navarro, J., Coll, M., Aguzzi, J., Cardona, L., & Sáez-Liante, R. (2015). Feeding ecology and trophic position of three sympatric demersal chondrichthyans in the northwestern Mediterranean. Marine Ecology Progress Series, 524, 255−268. https://doi.org/10.3354/meps11188
Aschliman, N. C. (2014). Interrelationships of the durophagous stingrays (Batoidea: Myliobatidae). Environmental Biology of Fish, 97, 967–979. https://doi.org/10.1007/s10641-014-0261-8
Bigelow, H. B., & Schroeder, W. C. (1950). New and little known cartilaginous fishes from the Atlantic. Museum of Comparative Zoology, 103, 385–408.
Bigelow, H. B., & Schroeder, W. C. (1951). A new genus and species of anacanthobatid skate from the Gulf of Mexico. Journal of the Washington Academy of Science, 41, 110–113.
Braga, R. R., Bornatowski, H., & Vitule, J. R. S. (2012). Feeding ecology of fishes: an overview of worldwide publications. Reviews of Fish Biology and Fisheries, 22, 915–929. https://doi.org/10.1007/s11160-012-9273-7
Bookstein, F. L. (1991). Morphometric tools for landmark data geometry and biology. Cambridge: Cambridge University Press.
Burress, E. D., Duarte, A., Serra, W. S., & Loureiro, M. (2015). Rates of piscivory predict pharyngeal jaw morphology in a piscivorous lineage of cichlid fishes. Ecology of Freshwater Fish, 25, 590–598. https://doi.org/10.1111/eff.12236
Chandler, A. C. (1921). A new species of ray from the Texas coast, and report of the occurrence of a top minnow new to the fauna of eastern Texas. Proceedings of the United States National Museum, 59, 657–658.
Collar, D. C., Wainwright, P. C., & Alfaro, M. E. (2008). Integrated diversification of locomotion and feeding in labrid fishes. Biological Letters, 4, 84–86. https://doi.org/10.1098/rsbl.2007.0509
Compagno, L. J. V. (1999). Batoid fishes. In K. E. Carpenter, & V. H. Niem, (Eds.), The living marine resources of the western central Pacific, Vol. 3. Batoid fishes, Chimaeras and bony fishes Part 1 (Elopidae to Linophrynidae) (pp. 1397–2068). Rome: FAO species Identification Guide for Fishery Purposes.
Costa, C., & Cataudella, S. (2007). Relationship between shape and trophic ecology of selected species of Sparids of the Caprolace coastal lagoon (Central Tyrrhenian Sea). Environmental Biology of Fishes, 78, 115–123. https://doi.org/10.1007/s10641-006-9081-9
Cuvier, G. (1816). Le Règne Animal distribué d'après son organisation pour servir de base à l'histoire naturelle des animaux et d'introduction à l'anatomie comparée. Les reptiles, les poissons, les mollusques et les annélides. Paris: Chez Déterville.
Dean, M. N., & Motta, P. J. (2004). Anatomy and functional morphology of the feeding apparatus of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea). Journal of Morphology, 262, 462–483. https://doi.org/10.1002/jmor.10245
Dean, M. N., Bizzarro, J. J., & Summers, A. P. (2007). The evolution of cranial design, diet, and feeding mechanisms in batoid fishes. Integrative and Comparative Biology, 47, 70–81. https://doi.org/10.1093/icb/icm034
Dean, M. N., Ramsay, J. B., & Schaefer, J. T. (2008). Tooth reorientation affects tooth function during prey processing and tooth ontogeny in the lesser electric ray, Narcine brasiliensis. Zoology, 111, 123–134. https://doi.org/10.1016/j.zool.2007.05.004
Di Santo, V., & Kenaley, C. P. (2016). Skating by: low energetic costs of swimming in a batoid fish. Journal of Experimental Biology, 219, 1804–1807. https://doi.org/10.1242/jeb.136358
Dulvy, N. K., & Reynolds, J. D. (2002). Predicting extinction vulnerability in skates. Conservation Biology, 16, 440–450. https://doi.org/10.1046/j.1523-1739.2002.00416.x
Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R. et al. (2014). Extinction risk and conservation of the world's sharks and rays. eLife, 3, e00590. https://doi.org/:10.7554/eLife.
Dulvy, N. K., Pacoureau, N., Rigby, C. L., Pollom, R. A., Jabado, R. W., Ebert, D. A. et al. (2021). Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Current Biology, 31, 4773–4787. https://doi.org/10.1016/j.cub.2021.08.062
Ebert, D. A., & Winton, M. V. (2010). Chondrichthyans of high latitude seas. In J. Carrier, J.A. Musick, & M. Heithaus (Eds.) Sharks and their relatives II: Biodiversity, adaptive physiology and conservation (pp. 115–158). Boca Raton, FL: CRC Press. https://doi.org/10.1201/9781420080483
Ehemann, N. R., González-González, L.V., Chollet-Villalpando, J. G., & De La Cruz-Agüero, J. (2018). Updated checklist of the extant Chondrichthyes within the Exclusive Economic Zone of Mexico. Zookeys, 774, 17–39. https://doiorg/10.3897/zookeys.774.25028
Ekstrom, L. J., & Kajiura, S. M. (2013). Pelvic girdle shape predicts locomotion and phylogeny in batoids. Journal of Morphology, 275, 100–110. https://doi.org/10.1002/jmor.20201
Fabre, A. C., Bickford, D., Segall, M., & Herrel, A. (2016). The impact of diet, habitat use, and behaviour on head shape evolution in homalopsid snakes. Biological Journal of the Linnean Society, 118, 634–647. https://doi.org/10.1111/bij.12753
Feduccia, A., & Slaughter, B. (1974). Sexual dimorphism in Skates (Rajidae) and its possible role differential niche utilization. Evolution, 28, 164–168. http://dx.doi.org/10.1111/j.1558-5646.1974.tb00737.x
Felsenstein, J. (1973). Maximum‐likelihood estimation of evolutionary trees from continuous characters. American Journal of Human Genetics, 25, 471– 492.
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39, 783–791. http://www.jstor.org/stable/2408678
Franklin, O., Palmer, C., & Dyke, G. (2014). Pectoral fin morphology of Batoid fishes (Chondrichthyes: Batoidea): Explaining phylogenetic variation with geometric morphometrics. Journal of Morphology, 275, 1173–1186. https://doi.org/10.1002/jmor.20294
Freckleton, R. P. (2012). Fast likelihood calculations for comparative analyses. Methods in Ecology and Evolution, 3, 940–947. https://doi.org/10.1111/j.2041-210X.2012.00220.x
Froese, R., & Pauly, D. (2019). FishBase. World Wide Web electronic publication version (11/2021). www.fishbase.org
Fulton, C. J. (2007). Swimming speed performance in coral reef fishes: Field validations reveal distinct functional groups. Coral Reefs, 26, 217–228. http://dx.doi.org/10.1007/s00338-007-0195-0
Garman, S. (1880). Synopsis and descriptions of the American Rhinobatidae. Proceedings of the Unites States National Museum, 3, 516–523. https://doi.org/10.5479/si.00963801.180.516
Garman, S. (1881). Reports on the results of dredging, under the Supervision of Alexander Agassiz, along the Atlantic coast of the United States during the summer of 1880, by the U. S. Coast Survey Steamer "Blake," Commander J. R. Bartlett, U. S. N., commanding Part XII. Report on the Selachians. Bulletin of the Museum of Comparative Zoology, 8, 231–237
Graham, K. J., Andrew, N. L., & Hodgson, K. E. (2001). Changes in relative abundance of sharks and rays on Australian South East Fishery trawl grounds after twenty years of fishing. Marine Freshwater Research, 52, 549–561. http://dx.doi.org/10.1071/MF99174
Griffith, E., & Smith, C.H. (1834). The class Pisces, arranged by the Baron Cuvier, with supplementary additions, by Edward Griffith and Charles Hamilton Smith. In G. Cuvier (Ed.) The Animal Kingdom. London: Whittaker and Co.
Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Paleontologia Electronica, 4, 1–9
Harmon, L., Weir, J., Brock, C., Glor, R., & Challenger, W. (2008). GIEGER: Investigating evolutionary radiations. Bioinformatics, 24, 129–131. https://doi.org/10.1093/bioinformatics/btm538
Hildebrand, S. F., & Schroeder, W.C. (1928). Fishes of Chesapeake Bay. Bulletin of the U.S. Bureau of Fisheries, 43, 1–366.
IUCN (International Union for Conservation of Nature). (2020). The IUCN Red List of Threatened Species. Version 2020-1. Downloaded in November 2021 from: https://www.iucnredlist.org
Jargowsky, M. B., Cooper, P. T., Ajemian, M. J., Colvin, M. E., & Drymon, J. M. (2019). Discerning the dietary habits of the smooth butterfly ray Gymnura lessae using two distinct methods, otolith identification and metagenetics. Journal of Fish Biology, 96, 1–10. http://dx.doi.org/10.1111/jfb.14221
Kajiura, S. M., & Tricas, T. C. (1996). Seasonal dynamics of dental sexual dimorphism in the Atlantic stingray Dasyatis Sabina. The Journal of Experimental Biology, 199, 2297–2306.
Kumar, S., Stecher, G., Li, M., Knyaz, C., & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Molecular Biology and Evolution, 35, 1547–1549. http://dx.doi.org/10.1093/molbev/msy096
Langerhans, R. B., & Reznick, D. N. (2010). Ecology and evolution of swimming performance in fishes: predicting evolution with biomechanics (pp. 200–248). In P. Domenici, & B. G. Kapoor (Eds.) Fish locomotion. Enfield, Oxford: Science Publishers.
Last, P. R., White, W. T., de Carvalho, M. R., Séret, B., Stehmann, M. F. W., & Naylor, G. J. P. (2016). Rays of the world. Australia: CSIRO Publishing, Comstock Publishing Associates.
Lobato, F. L., Barneche, D. R., Siqueira, A. C., Liedke, A. M. R., Lindner, A., Pie, M. R. et al. (2014). Diet and diversification in the evolution of coral reef fishes. Plos One, 9, e102094. https://doi.org/10.1371/journal.pone.0102094
Losos, J. B. (2009). Lizards in an evolutionary tree: ecology and adaptive radiation of anoles. Berkeley, California: University of California Press.
Michael, S. W. (1993). Reef sharks and rays of the world. A guide to their identification, behavior, and ecology. Monterey, California: Sea Challengers.
McEachran, J. D., & de Carvalho, M. R. (2002). Batoids fishes In K. E. Carpenter (Ed.), The living marine resources of the Western Central Atlantic. Introduction, mollusks, crustaceans, hagfishes, sharks, batoid fishes, and chimaeras No. 5 (pp. 507–589). Rome: FAO, Special Publication.
Monteiro, L. R., Bonato, V., & dos Reis, S. F. (2005). Evolutionary integration and morphological diversification in complex morphological structures: Mandible shape divergence in spiny rats (Rodentia, Echimyidae). Evolution and Development, 7, 429–439. https://doi.org/10.1111/j.1525-142X.2005.05047.x
Navarro-González, J. A., Rubio-Rodríguez, U., Mejía-Falla, P. A., & Cruz-Escalona, V. H. (2018). Descripción morfológica del aparato bucal de adultos de Urotrygon nana y U. rogersi (Urotrygonidae): diferencias intraespecíficas e interespecíficas. Hidrobiológica, 28, 219–222. https://doi.org/10.24275/uam/izt/dcbs/hidro/2018v28n2/navarro
Nelson, J. S., Grande, T. C., & Wilson, M. V. H. (2016). Fishes of the world, 5th Ed. New York: John Wiley & Sons.
O’Shea, O. R., Wueringer, B. E., Winchester, M. M., & Brooks, E. J. (2017). Comparative feeding ecology of the yellow ray Urobatis jamaicensis (Urotrygonidae) from The Bahamas. Journal of Fish Biology, 2, 73–84. https://doi.org/10.1111/jfb.13488
Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290. http://dx.doi.org/10.1093/bioinformatics/btg412
Parson, J., Fish, F. E., & Nicastro, A. J. (2011). Turning performance of batoid rays: limitations of a rigid body. Journal of Experimental Marine Biology and Ecology, 402, 12–18. http://dx.doi.org/10.1016/j.jembe.2011.03.010
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2014). nlme: Linear and nonlinear mixed effects models. R package version 3.1–117. http://cran.r-project.org/package=nlme
Platell, M., Potter, I. C, & Clarke, K. R. (1998). Resource partitioning by four species of elasmobranchs (Batoidea: Urolophidae) in coastal waters of temperate Australia. Marine Biology, 131, 719−734. http://dx.doi.org/10.1007/s002270050363
Price, S. A., Wainwright, P. С., Bellwood, D. R., Kazancioglu, E., Collar, D. C., & Near, T. J. (2010). Functional innovations and morphological diversification in parrotfishes. Evolution, 64, 3057–3068. http://dx.doi.org/10.1111/j.1558-5646.2010.01036.x
Queiroz, A. P. N., Araújo, M. L. G., & Lessa, R. P. T. (2019). Dietary composition and trophic level of Hypanus marianae (Myliobatiformes: Dasyatidae), captured off Pernambuco coast, Brazil. Latin American Journal of Aquatic Research, 47, 808–817. https://doi.org/10.3856/vol47-issue5-fulltext-10
R Development Core Team (2011). R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. http://www.R-project.org
Radinsky, L. (1961). Tooth histology as a taxonomic criterion for cartilaginous fishes. Journal of Morphology, 109, 73–92. https://doi.org/10.1002/jmor.1051090106
Rastgoo, A. R., Navarro, J., & Valinassab, T. (2018). Comparative diets of sympatric batoid elasmobranchs in the Gulf of Oman. Journal of Aquatic Biology, 27, 35–41. http://dx.doi.org/10.3354/ab00694
Revell, L. J. (2012). phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Revell, L. J. (2013). Two new graphical methods for mapping trait evolution on phylogenies. Methods of Ecology and Evolution, 4, 754–759. https://doi.org/10.1111/2041-210X.12066
Robertson, D. R., & Van Tassell, J. (2019). Shorefishes of the Greater Caribbean: online information system. Version 2.0. Smithsonian Tropical Research Institute, Balboa, Panamá.
Rohlf, F. J. (1993). Relative warps analysis and an example of its application to mosquito wings. In L. F. Marcus, E. Bello, & A. Garcia-Valdecasas (Eds.), Contributions to morphometrics (pp. 131–159). Madrid: Monografias del Museo Nacional de Ciencias Naturales, CSIC.
Rohlf, F. J. (1999). Shape statistics: Procrustes superimpositions and tangent spaces. Journal of Classification, 16, 197–223.
Rohlf, F. J. (2015). The tps series of software. Hystrix, 26, 1–4. http://dx.doi.org/10.4404/hystrix-26.1-11264
Rohlf, F. J., & Slice, D. (1990). Extension of the Procrustes method for the optimal superposition of landmarks. Systematic Zoology, 39, 40–59. https://doi.org/10.2307/2992207
Rolland, J., Condamine, F. L., Jiguet, F., & Morlon, H. (2014). Faster speciation and reduced extinction in the tropics contribute to the mammalian latitudinal diversity gradient. Plos Biology, 12, e1001775. http://dx.doi.org/10.1371/journal.pbio.1001775
Rosenberger, L. J. (2001). Pectoral fin locomotion in batoid fishes: Undulation versus oscillation. Journal of Experimental Biology, 204, 379–394. https://doi.org/10.1242/jeb.204.2.379
Ross, S. T. (1986). Resource partitioning in fish assemblages: a review of field studies. Copeia, 2, 352–388.
Rutledge, K. M., Summers, A. P., & Kolmann, M. A. (2019). Killing them softly: Ontogeny of jaw mechanics and stiffness in mollusk‐feeding freshwater stingrays. Journal of Morphology, 280, 796–808. https://do.org/10.1002/jmor.20984
Sáez, S., & Lamilla, J. (1997). Morfología y disposición de los dientes en una especie con heterodontía sexual: Raja (Dipturus) chilensis Guichenot, 1848. Biología Pesquera, 26, 25–41.
Sáez, S., & Laminilla, J. (2004). Sexual homodonty in Bathyraja griseocauda (Norman 1973) from the Southern Eastern Pacific (Chile) (Chondrichthyes, Rajidae: Arhynchobatinae). Journal of Applied Ichthyology, 20, 189–193. https://doi.org/10.1111/j.1439-0426.2004.00516.x
Sáez, S., & Laminilla, J. (2012). Claves taxonómicas para el reconocimiento dentario en taxa del superorden Rajomorphii de Chile (Chondrichthyes, Batoidea). Latin American Journal of Aquatic Research, 40, 282–291.
Serena, F., Abella, A. J., Bargnesi, F., Barone, M., Colloca, F., Ferretti, F. et al. (2020). Species diversity, taxonomy and distribution of Chondrichthyes in the Mediterranean and Black Sea. European Zoology Journal, 87, 497–536. https://doi.org/10.1080/24750263.2020.1805518
Stehmann, M., McEachran, J. D., & Vergara, R. (1978). Dasyatidae. In W. Fischer (Ed.), FAO species identification sheets for fishery purposes. Western Central Atlantic (Fishing Area 31). Vol. 1. Rome: FAO.
Summers, A. P. (2000). Stiffening the stingray skeleton – an investigation of durophagy in myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae). Journal of Morphology, 243, 113–126. https://doi.org/10.1002/(sici)1097-4687(200002)243:2%3C113::aid-jmor1%3E3.0.co;2-a
Tamura, K., & Nei, M. (1993). Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512–526. https://doi.org/10.1093/oxfordjournals.molbev.a040023
Taniuchi, T., & Shimizu, M. (1993). Dental sexual dimorphism and food habits in the stingray Dasyatis akajei from Tokyo Bay, Japan. Nippon Suisan Gakkaishi, 59, 53–60. https://doi.org/10.2331/SUISAN.59.53
Underwood, C. J., Johanson, Z., Welten, M., Metscher, B., Rasch, L. J., Fraser, G. J. et al. (2015). Development and evolution of dentition pattern and tooth order in the skates and rays (Batoidea; Chondrichthyes). Plos One, 10, e0122553. https://doi.org/10.1371/journal.pone.0122553
Wainwright, P. C., Bellwood, D. R., & Westneat, M. W. (2002). Ecomorphology of locomotion in labrid fishes. Environmental Biology of Fishes, 65, 47–62. http://dx.doi.org/10.1023/A:1019671131001
Weigmann, S. (2016). Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. Journal of Fish Biology, 88, 837–1037. https://doi.org/10.1111/jfb.12874
Wilga, C. D., & Lauder, G. V. (2000). Three-dimensional kinematics and wake structure of the pectoral fins during locomotion in leopard sharks, Triakis semifasciata. Journal of Experimental Biology, 203, 2261–2278. https://doi.org/10.1242/jeb.203.15.2261
Yokota, L., & De Carvalho, M.R. (2017). Taxonomic and morphological revision of butterfly rays of the Gymnura micrura (Bloch and Schneider 1801) species complex, with the description of two new species (Myliobatiformes: Gymnuridae). Zootaxa, 4332, 1–74. http://dx.doi.org/10.11646/zootaxa.4332.1.1
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric Morphometrics for biologists: a primer. New York and London: Elsevier Academic Press.