Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5512 No. 4: 23 Sept. 2024
Type: Article
Published: 2024-09-23
DOI: 10.11646/zootaxa.5512.4.2
Page range: 491-511
Abstract views: 2653
PDF downloaded: 823

Sphyrna alleni sp. nov., a new hammerhead shark (Carcharhiniformes, Sphyrnidae) from the Caribbean and the Southwest Atlantic.

Predator Ecology and Conservation Lab; Biological Sciences Department; Florida International University; 3000 NE 151 Street; MSB 350; North Miami; FL; 33181; USA
Institut des Sciences de la Forêt Tempérée; Université de Quebec en Outaouais; Ripon; Québec; Canada. 58 Rue Principale; Ripon; QC J0V 1V0; Canada
National Oceanic and Atmospheric Administration; National Marine Fisheries Service; Southeast Fisheries Science Center; Mississippi Laboratories; P.O. Drawer 1207; Pascagoula; MS 39567; USA
Department of Marine and Environmental Sciences; Halmos College of Arts and Sciences; Nova Southeastern University; Fort Lauderdale; FL 33328-2004; USA
Predator Ecology and Conservation Lab; Biological Sciences Department; Florida International University; 3000 NE 151 Street; MSB 350; North Miami; FL; 33181; USA; Sharks and Rays Conservation Research Program; Mote Marine Laboratory & Aquarium; 1600 Ken Thompson Parkway; Sarasota; FL 34236; USA
Pisces Shovelbill shark morphology mtDNA nDNA phylogenetics species complex taxonomy

Abstract

Hammerhead sharks (Family Sphyrnidae) comprise a monophyletic Miocene radiation of carcharhiniform sharks characterized by their laterally expanded and dorsoventrally compressed head (‘cephalofoil’). The bonnethead shark (Sphyrna tiburo) is currently described as a single amphi-American hammerhead species composed of the subspecies Sphyrna tiburo tiburo in the Western Atlantic Ocean (WA) and S. tiburo vespertina in the Eastern Pacific Ocean (EP). Variation in mitochondrial DNA and cephalofoil shape suggest a species complex, with S. tiburo occurring in the U.S., Mexico, and Bahamas; S. aff. tiburo occurring from Belize to Brazil; and S. vespertina occurring in the EP. Morphometric, meristic, and genetic variation was used to resolve the bonnethead shark complex in the Western Atlantic. Twenty-three specimens (12 S. aff. tiburo from Belize and 11 S. tiburo from U.S.) were subject to sixty-one morphometric measurements and three meristic characters (counts of the number of precaudal vertebrae, lower and upper rows of functional teeth). An allometric formula was used to standardize any effect caused by differences in size of the individuals and data were analyzed with univariate and multivariate statistics. Sphyrna aff. tiburo and S. tiburo have non-overlapping vertebral counts (80-83 and 71-74 respectively) but no morphometric differences were detected. Although not captured in morphometric analysis, the cephalofoil of S. aff. tiburo has a more pointed anterior margin than S. tiburo that together with lobule shaped posterior margins gives the cephalofoil a distinctive shovel-shaped appearance. Concatenated mitochondrial sequences and 12 nuclear microsatellite markers clearly separated S. aff. tiburo and S. tiburo. We conclude that this complex comprises two species in the Western Atlantic, S. tiburo and S. alleni sp. nov., and we provide a description of the latter, which is distinguished by precaudal vertebral counts (80-83), a shovel-shaped cephalofoil with rounded posterior margins, and robust differences in mitochondrial and nuclear genetic markers. We suggest nuclear genetic and meristic examination of EP bonnetheads is needed to update the taxonomical status and redescribe S. vespertina.

 

References

  1. Aroca, A.K., Tavera, J. & Torres, Y. (2022) Molecular and morphological evaluation of the bonnethead shark complex Sphyrna tiburo (Carcharhiniformes: Sphyrnidae). Environmental Biology of Fishes, 105, 1643–1658. https://doi.org/10.1007/s10641-022-01358-x DOI: https://doi.org/10.1007/s10641-022-01358-x
  2. Barker, A.M., Adams, D.H., Driggers, W.B., Frazier, B.S. & Portnoy, D.S. (2019) Hybridization between sympatric hammerhead sharks in the western North Atlantic Ocean. Biology Letters, 15 (4). [published online] https://doi.org/10.1098/rsbl.2019.0004 DOI: https://doi.org/10.1098/rsbl.2019.0004
  3. Briggs, J.C. & Bowen, B.W. (2013) Marine shelf habitat: Biogeography and evolution. Journal of Biogeography, 40, 1023–1035. https://doi.org/10.1111/jbi.12082 DOI: https://doi.org/10.1111/jbi.12082
  4. Cardeñosa, D., Fields, A.T., Babcock, E.A., Shea, S.K.H., Feldheim, K.A. & Chapman, D.D. (2020) Species composition of the largest shark fin retail-market in mainland China. Scientific Reports, 10, 1–10. https://doi.org/10.1038/s41598-020-69555-1 DOI: https://doi.org/10.1038/s41598-020-69555-1
  5. Compagno, L.J. V (1984a) Fao Fisheries Synopsis. Fao Species Catalogue. Vol . 4. Sharks of the World. Part 2 - Carcharhiniformes. United Nations Development Programme Food And Agriculture Organization Of The United Nations, Rome, 249 pp.
  6. Compagno, L.J. V (1984b) 4 FAO Fisheries Synopsis Sharks of the world. An annotated and illustrated catalouge of shark species to date, Part II (Carcharhiniformes), 250–655.
  7. Díaz-Jaimes, P., Bayona-Vásquez, N.J., Escatel-Luna, E., Uribe-Alcocer, M., Pecoraro, C., Adams, D.H., Frazier, B.S., Glenn, T.C. & Babbucci, M. (2021) Population genetic divergence of bonnethead sharks Sphyrna tiburo in the western North Atlantic: Implications for conservation. Aquatic Conservation: Marine and Freshwater Ecosystems, 31, 83–98. https://doi.org/10.1002/aqc.3434 DOI: https://doi.org/10.1002/aqc.3434
  8. Domingues, R.R., Bruels, C.C., Gadig, O.B.F., Chapman, D.D., Hilsdorf, A.W.S. & Shivji, M.S. (2019) Genetic connectivity and phylogeography of the night shark (Carcharhinus signatus) in the western Atlantic Ocean: Implications for conservation management. Aquatic Conservation: Marine and Freshwater Ecosystems, 29, 102–114. https://doi.org/10.1002/aqc.2961 DOI: https://doi.org/10.1002/aqc.2961
  9. Domingues, R.R., Hilsdorf, A.W.S., Shivji, M.M., Hazin, F.V.H. & Gadig, O.B.F. (2018) Effects of the Pleistocene on the mitochondrial population genetic structure and demographic history of the silky shark (Carcharhinus falciformis) in the western Atlantic Ocean. Reviews in Fish Biology and Fisheries, 28, 213–227. https://doi.org/10.1007/s11160-017-9504-z DOI: https://doi.org/10.1007/s11160-017-9504-z
  10. Earl, D.A. & vonHoldt, B.M. (2012) STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359–361. https://doi.org/10.1007/s12686-011-9548-7 DOI: https://doi.org/10.1007/s12686-011-9548-7
  11. Ebert, D.A. & Compagno, L.J.V. (2009) Chlamydoselachus africana, a new species of frilled shark from southern Africa (Chondrichthyes, Hexanchiformes, Chlamydoselachidae). Zootaxa, 2173 (1), 1–18. https://doi.org/10.11646/zootaxa.2173.1.1 DOI: https://doi.org/10.11646/zootaxa.2173.1.1
  12. Elliott, N.G., Haskard, K. & Koslow, J.A. (1995) Morphometric analysis of orange roughy (Hoplostethus atlanticus) off the continental slope of southern Australia. Journal of Fish Biology, 46, 202–220. https://doi.org/10.1111/j.1095-8649.1995.tb05962.x DOI: https://doi.org/10.1111/j.1095-8649.1995.tb05962.x
  13. Excoffier, L. & Heckel, G. (2006) Computer programs for population genetics data analysis: a survival guide. Nature Reviews Genetics, 7, 745–758. https://doi.org/10.1038/nrg1904 DOI: https://doi.org/10.1038/nrg1904
  14. Excoffier, L. & Lischer, H.E.L. (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x DOI: https://doi.org/10.1111/j.1755-0998.2010.02847.x
  15. Fields, A.T., Feldheim, K.A., Gelsleichter, J., Pfoertner, C. & Chapman, D.D. (2016) Population structure and cryptic speciation in bonnethead sharks Sphyrna tiburo in the south-eastern U.S.A. and Caribbean. Journal of Fish Biology, 89, 2219–2233. https://doi.org/10.1111/jfb.13025 DOI: https://doi.org/10.1111/jfb.13025
  16. Gilbert, R. (1967) A Revision of the Hammerhead Sharks. Proceedings of the United States National Museum, 119 (3539), 1–88, 22 figs., 10 pls., 5 maps, 9 tables. https://doi.org/10.5479/si.00963801.119-3539.1 DOI: https://doi.org/10.5479/si.00963801.119-3539.1
  17. Gonzalez, C., Gallagher, A.J. & Caballero, S. (2019) Conservation genetics of the bonnethead shark Sphyrna tiburo in Bocas del Toro, Panama: Preliminary evidence of a unique stock. PLoS ONE, 14, 1–17. https://doi.org/10.1371/journal.pone.0220737 DOI: https://doi.org/10.1371/journal.pone.0220737
  18. Gonzalez, C., Postaire, B., Domingues, R.R., Feldheim, K.A., Caballero, S. & Chapman, D. (2021) Phylogeography and population genetics of the cryptic bonnethead shark Sphyrna aff. tiburo in Brazil and the Caribbean inferred from mtDNA markers. Journal of Fish Biology, 99, 1899–1911. https://doi.org/10.1111/jfb.14896 DOI: https://doi.org/10.1111/jfb.14896
  19. Harper, S., Guzmán, H.M., Zylich, K. & Zeller, D. (2014) Reconstructing Panama’s Total Fisheries Catches from 1950 to 2010: Highlighting Data Deficiencies and Management Needs. Marine Fisheries Review, 76, 51–65. https://doi.org/10.7755/MFR.76.1_2.3 DOI: https://doi.org/10.7755/MFR.76.1_2.3
  20. IUCN (2021) The IUCN Red List of Threatened Species. Version 2020-3. Available from: https://www.iucnredlist.org/ (accessed 24 July 2024)
  21. Jakobsson, M. & Rosenberg, N.A. (2007) CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23, 1801–1806. https://doi.org/10.1093/bioinformatics/btm233 DOI: https://doi.org/10.1093/bioinformatics/btm233
  22. Jawad, L. a. (2013) Sharks of the world: A fully illustrated guide. Edited by D. A. Ebert, S. Fowler & L. Compagno. Journal of Fish Biology, 83, 1487–1488. https://doi.org/10.1111/jfb.12250 DOI: https://doi.org/10.1111/jfb.12250
  23. Jost, L., Archer, F., Flanagan, S., Gaggiotti, O., Hoban, S. & Latch, E. (2018) Differentiation measures for conservation genetics. Evolutionary Applications, 11, 1139–1148. https://doi.org/10.1111/eva.12590 DOI: https://doi.org/10.1111/eva.12590
  24. Keeney, D.B., Heupel, M., Hueter, R.E. & Heist, E.J. (2003) Genetic heterogeneity among blacktip shark, Carcharhinus limbatus, continental nurseries along the U.S. Atlantic and Gulf of Mexico. Marine Biology, 143, 1039–1046. https://doi.org/10.1007/s00227-003-1166-9 DOI: https://doi.org/10.1007/s00227-003-1166-9
  25. Lim, D.D., Motta, P., Mara, K. & Martin, A.P. (2010) Phylogeny of hammerhead sharks (Family Sphyrnidae) inferred from mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution, 55, 572–579. https://doi.org/10.1016/j.ympev.2010.01.037 DOI: https://doi.org/10.1016/j.ympev.2010.01.037
  26. Maddison, D. & Maddison, W. (2000) MacClade: Analysis of Phylogeny and Character Evolution. Manual. Sinauer, Sunderland, Massachusetts, 492 pp.
  27. Mazzullo, S.J. (2006) Late Pliocene to Holocene platform evolution in northern Belize, and comparison with coeval deposits in southern Belize and the Bahamas. Sedimentology, 53, 1015–1047. https://doi.org/10.1111/j.1365-3091.2006.00800.x DOI: https://doi.org/10.1111/j.1365-3091.2006.00800.x
  28. Meirmans, P.G. & Van Tienderen, P.H. (2004) GENOTYPE and GENODIVE: Two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes, 4, 792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x DOI: https://doi.org/10.1111/j.1471-8286.2004.00770.x
  29. Montes, C., Cardona, A., Jaramillo, C., Pardo, A., Silva, J.C., Valencia, V., Ayala, C., Pérez-Angel, L.C., Rodriguez-Parra, L.A., Ramirez, V. & Niño, H. (2015) Middle Miocene closure of the Central American Seaway. Science, 348, 226–229. https://doi.org/10.1126/science.aaa2815 DOI: https://doi.org/10.1126/science.aaa2815
  30. Morgan, J.A.T., Harry, A. V., Welch, D.J., Street, R., White, J., Geraghty, P.T., Macbeth, W.G., Tobin, A., Simpfendorfer, C.A. & Ovenden, J.R. (2012) Detection of interspecies hybridisation in Chondrichthyes: Hybrids and hybrid offspring between Australian (Carcharhinus tilstoni) and common (C. limbatus) blacktip shark found in an Australian fishery. Conservation Genetics, 13, 455–463. https://doi.org/10.1007/s10592-011-0298-6 DOI: https://doi.org/10.1007/s10592-011-0298-6
  31. Naylor, G.J.P. (1992) the Phylogenetic Relationships Among Requiem and Hammerhead Sharks: Inferring Phylogeny When Thousands of Equally Most Parsimonious Trees Result. Cladistics, 8, 295–318. https://doi.org/10.1111/j.1096-0031.1992.tb00073.x DOI: https://doi.org/10.1111/j.1096-0031.1992.tb00073.x
  32. Naylor, G.J.P., Caira, J.N., Jensen, K., Rosana, K.A.M., White, W.T. & Last, P.R. (2012) A DNA Sequence–Based Approach To the Identification of Shark and Ray Species and Its Implications for Global Elasmobranch Diversity and Parasitology. Bulletin of the American Museum of Natural History, 367, 1–262. https://doi.org/10.1206/754.1 DOI: https://doi.org/10.1206/754.1
  33. O’Dea, A., Lessios, H.A., Coates, A.G., Eytan, R.I., Restrepo-Moreno, S.A., Cione, A.L., Collins, L.S., De Queiroz, A., Farris, D.W., Norris, R.D., Stallard, R.F., Woodburne, M.O., Aguilera, O., Aubry, M.P., Berggren, W.A., Budd, A.F., Cozzuol, M.A., Coppard, S.E., Duque-Caro, H., Finnegan, S., Gasparini, G.M., Grossman, E.L., Johnson, K.G., Keigwin, L.D., Knowlton, N., Leigh, E.G., Leonard-Pingel, J.S., Marko, P.B., Pyenson, N.D., Rachello-Dolmen, P.G., Soibelzon, E., Soibelzon, L., Todd, J.A., Vermeij, G.J. & Jackson, J.B.C. (2016) Formation of the Isthmus of Panama. Science Advances, 2, 1–12. https://doi.org/10.1126/sciadv.1600883 DOI: https://doi.org/10.1126/sciadv.1600883
  34. Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x DOI: https://doi.org/10.1111/j.1471-8286.2004.00684.x
  35. Pérez-Jiménez, J.C. (2014) Historical records reveal potential extirpation of four hammerhead sharks (Sphyrna spp.) in Mexican Pacific waters. Reviews in Fish Biology and Fisheries, 24, 671–683. https://doi.org/10.1007/s11160-014-9353-y DOI: https://doi.org/10.1007/s11160-014-9353-y
  36. Pollom, R., Carlson, J., Charvet, P., Avalos, C., Bizzarro, J., Blanco-Parra, MP, Briones Bell-lloch, A., Burgos-Vázquez, M.I., Cardenosa, D., Cevallos, A., Derrick, D., Espinoza, E., Espinoza, M., Mejía-Falla, P.A., Morales-Saldaña, J.M., Navia, A.F. & Mo, O. (2021) Sphyrna tiburo (amended version of 2020 assessment). The IUCN Red List of Threatened Species, 2021, e.T39387A205765567.
  37. Posada, D.J. (2008) ModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256. https://doi.org/10.1093/molbev/msn083 DOI: https://doi.org/10.1093/molbev/msn083
  38. Price, K.A., O’Bryhim, J.R., Jones, K.L. & Lance, S.L. (2014) Development of polymorphic microsatellite markers for the bonnethead shark, Sphyrna tiburo. Conservation Genetics Resources, 7, 69–71. https://doi.org/10.1007/s12686-014-0289-2 DOI: https://doi.org/10.1007/s12686-014-0289-2
  39. Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. https://doi.org/10.1093/genetics/155.2.945 DOI: https://doi.org/10.1093/genetics/155.2.945
  40. Quattro, J.M., Driggers, W.B., Grady, J.M., Ulrich, G.F. & Roberts, M.A. (2013) Sphyrna gilberti sp. nov., a new hammerhead shark (Carcharhiniformes, Sphyrnidae) from the western Atlantic Ocean. Zootaxa, 3702 (2), 159. https://doi.org/10.11646/zootaxa.3702.2.5 DOI: https://doi.org/10.11646/zootaxa.3702.2.5
  41. Reis-Filho, J.A., Sampaio, C.L.S., Leite, L., Oliveira, G.S.A., Loiola, M. & De Anchieta Nunes, J.C.C. (2014) Rediscovery of bonnethead shark Sphyrna tiburo after more than two decades of non-record on central coast of Brazil. Marine Biodiversity Records, 7, 1–8. https://doi.org/10.1017/S1755267214000487 DOI: https://doi.org/10.1017/S1755267214000487
  42. Rosenberg, N.A. (2004) DISTRUCT: A program for the graphical display of population structure. Molecular Ecology Notes, 4, 137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x DOI: https://doi.org/10.1046/j.1471-8286.2003.00566.x
  43. Rousset, F. (2008) GENEPOP’007: A complete re-implementation of the GENEPOP software for Windows and Linux. Molecular Ecology Resources, 8, 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x DOI: https://doi.org/10.1111/j.1471-8286.2007.01931.x
  44. Springer, S. (1940) Three new sharks of the genus Sphyrna from the Pacific coast of tropical America. Stanford Ichthyological Bulletin, 1, 161–172.
  45. Springer, V.G. & Garrick, J.A.F. (1964) A Survey of Vertebral Numbers in Sharks. Proceedings of the United States National Museum, 116, 73–96. https://doi.org/10.5479/si.00963801.116-3496.73 DOI: https://doi.org/10.5479/si.00963801.116-3496.73
  46. Ward, R.D., Zemlak, T.S., Innes, B.H., Last, P.R. & Hebert, P.D.N. (2005) DNA barcoding Australia’s fish species. Philosophical transactions of the Royal Society of London, Series B, Biological sciences, 360, 1847–1857. https://doi.org/10.1098/rstb.2005.1716 DOI: https://doi.org/10.1098/rstb.2005.1716