SpringerLink
Log in

Multilocus phylogeography of the endemic and endangered angular angelshark (Squatina guggenheim) in the Southwest Atlantic Ocean

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

The angular angelshark (Squatina guggenheim) is a coastal endangered angel shark from the Southwest Atlantic Ocean and one of the major bycatch victims. Despite major concerns about this species, little is known about its evolutionary connectivity across its whole geographic distribution. Here, genetic connectivity and phylogeographic patterns of S. guggenheim for 122 individuals were assessed across the Southwest Atlantic Ocean regions based on a multilocus mitochondrial DNA approach to support conservation strategies. The concatenated mitochondrial dataset (control region, cytochrome b and cytochrome c oxidase I) showed high levels of haplotype diversity and low nucleotide diversity in S. guggenheim, with distinct genetic diversity patterns among populations. Although signs of step**-stone gene flow were observed, a strong and statistically significant genetic structure into at least two populations was detected, matching with the species’ biological traits and region’s oceanographic particularities. Contrasting demographic patterns were detected, in which only southernmost Atlantic populations showed signs of population expansion. Despite the existence of connectivity among regions, our results suggest that conservation plans should be carried out following the uniqueness of each management unit.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

DNA sequences of all molecular markers have been submitted to GenBank (https://www.ncbi.nlm.nih.gov/genbank), accession numbers: MW456691- MW456735.

Code availability

Not applicable.

References

  • Acha, E. M., H. W. Mianzan, R. A. Guerrero, M. Favero & J. Bava, 2004. Marine fronts at the continental shelves of austral South America: physical and ecological processes. Journal of Marine Systems 44: 83–105.

    Article  Google Scholar 

  • Allendorf, F. W., G. Luikart & S. N. Aitken, 2013. Conservation and the genetics of population, Blackwell, Oxford:

    Google Scholar 

  • Almerón-Souza, F., C. Sperb, C. L. Castilho, P. I. Figueiredo, L. T. Goncalves, R. Machado, et al., 2018. Molecular identification of shark meat from local markets in Southern Brazil based on DNA barcoding: Evidence for mislabeling and trade of Endangered species. Frontiers in Genetics. https://doi.org/10.3389/fgene.2018.00138.

    Article  PubMed  PubMed Central  Google Scholar 

  • Alves, D. P. & M. M. de Mahiques, 2019. Deposition and sea-level evolution models for Upper Pleistocene/Holocene in the São Sebastião Channel (SE Brazilian coast) inferred from 5th order seismic stratigraphy. Journal of South American Earth Sciences 93: 382–393.

    Article  Google Scholar 

  • Araújo, F. G., T. P. Teixeira, A. P. P. Guedes, M. C. C. de Azevedo & A. L. M. Pessanha, 2018. Shifts in the abundance and distribution of shallow water fish fauna on the southeastern Brazilian coast: a response to climate change. Hydrobiologia 814: 205–218.

    Article  Google Scholar 

  • Avise, J. C., 2000. Phylogeography –the history and formation of species, Harvard University Press:

    Book  Google Scholar 

  • Avise, J. C., 2009. Phylogeography: retrospect and prospect. Journal of Biogeography 36: 3–15.

    Article  Google Scholar 

  • Beerli, P. & J. Felsenstein, 2001. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences 98: 4563–4568.

    Article  CAS  Google Scholar 

  • Beerli, P. & M. Palczewski, 2010. Unified framework to evaluate panmixia and migration direction among multiple sampling locations. Genetics 185: 313–326.

    Article  PubMed  PubMed Central  Google Scholar 

  • Beheregaray, L. B., P. Sunnucks & D. A. Briscoe, 2002. A rapid fish radiation associated with the last sea-level changes in southern Brazil: the silverside Odontesthes perugiae complex. Proceedings of the Royal Society of London Series B: Biological Sciences 269: 65–73.

    Article  PubMed  PubMed Central  Google Scholar 

  • Belgrano, A. & C. W. Fowler, 2013. How fisheries affect evolution. Science 342: 1176–1177.

    Article  PubMed  Google Scholar 

  • Benjamini, Y. & Y. Hochberg, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (methodological) 57: 289–300.

    Article  Google Scholar 

  • Borsa, P., I. S. Arlyza, M. Laporte & P. Berrebi, 2012. Population genetic structure of blue-spotted maskray Neotrygon kuhlii and two other Indo-West Pacific stingray species (Myliobatiformes: Dasyatidae), inferred from size-polymorphic intron markers. Journal of Experimental Marine Biology and Ecology 438: 32–40.

    Article  Google Scholar 

  • Bouckaert, R., J. Heled, D. Kühnert, T. Vaughan, C. H. Wu, D. **e, et al., 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10: e1003537.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bouckaert, R. R. & A. J. Drummond, 2017. bModelTest: Bayesian phylogenetic site model averaging and model comparison. BMC Evolutionary Biology 17(1): 1–11.

    Article  Google Scholar 

  • Bowen, B. W., K. Shanker, N. Yasuda, M. Celia, M. C. M. D. Malay, S. von der Heyden, et al., 2014. Phylogeography unplugged: comparative surveys in the genomic era. Bulletin of Marine Science 90: 13–46.

    Article  Google Scholar 

  • Bunholi, I. V., B. L. S. Ferrette, J. B. De Biasi, C. O. Magalhães, M. M. Rotundo, C. Oliveira, et al., 2018. The fishing and illegal trade of the angelshark: DNA barcoding against misleading identifications. Fisheries Research 206: 193–197.

    Article  Google Scholar 

  • Chapman, D. D., K. A. Feldheim, Y. P. Papastamatiou & R. E. Hueter, 2015. There and back again: A review of residency and return migration in sharks, with implication for populations structure and management. Annual Review of Marine Science 7: 547–570.

    Article  PubMed  Google Scholar 

  • Chevolot, M., G. Hoarau, A. D. Rijnsdorp, W. T. Stam & J. L. Olsen, 2006. Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Molecular Ecology 15: 3693–3705.

    Article  CAS  PubMed  Google Scholar 

  • Chiaramonte, G. E., 1998. Shark fisheries in Argentina. Marine and Freshwater Research 49: 601–609.

    Article  Google Scholar 

  • Colonello, J. H., L. O. Lucifora & A. M. Massa, 2007. Reproduction of the angular angelshark (Squatina guggenheim): geographic differences, reproductive cycle, and sexual dimorphism. ICES Journal of Marine Science 64: 131–140.

    Article  Google Scholar 

  • Corrêa, I. C. S., 1996. Les variations du niveau de la mer durant les derniers 17.500 ans BP: l’exemple de la plate-forme continentale du Rio Grande do Sul-Brésil. Marine Geology 130: 163–178.

    Article  Google Scholar 

  • Cortinhas, M. C. S., R. Kersanach, M. Proietti, L. F. C. Dumont, F. D’Incao, A. L. F. Lacerda & M. M. Cestari, 2016. Genetic structuring among silverside fish (Atherinella brasiliensis) populations from different Brazilian regions. Estuarine, Coastal and Shelf Science 178: 148–157.

    Article  CAS  Google Scholar 

  • Cousseau, M. B. & D. E. Figueroa, 2001. Las especies del género Squatina en aguas de Argentina (Pisces: Elasmobranchii: Squatinidae). Neotrópica 47: 85–86.

    Google Scholar 

  • Cruz, V. P., A. M. Adachi, P. H. Oliveira, G. S. Ribeiro, F. G. Paim, B. C. Souza, et al., 2021. Genetic diversity in two threatened species of guitarfish (Elasmobranchii: Rhinobatidae) from the Brazilian and Argentinian coasts: an alert for conservation. Neotropical Ichthyology. https://doi.org/10.1590/1982-0224-2021-0012.

    Article  Google Scholar 

  • Cuevas, J. M., V. García, S. Montealegre-Quijano, L. Paesch, M. Estalles, V. Falabella, et al., 2020. Report of the IUCN Regional Red List Workshop for Species of the Patagonian Sea: Chondrichthyans. Forum for the Conservation of the Patagonian Sea. 302 pp.

  • Darriba, D., G. L. Taboada, R. Doallo & D. Posada, 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9: 772–772.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • DiBattista, J. D., C. Wilcox, M. T. Craig, L. A. Rocha & B. W. Bowen, 2011. Phylogeography of the Pacific Blueline Surgeonfish, Acanthurus nigroris, reveals high genetic connectivity and a cryptic endemic species in the Hawaiian Archipelago. Journal of Marine Biology 2011: 1–17.

    Article  Google Scholar 

  • Domingues, R. R., A. W. S. Hilsdorf & O. B. F. Gadig, 2018. The importance of considering genetic diversity in shark and ray conservation policies. Conservation Genetics 19: 501–525.

    Article  CAS  Google Scholar 

  • Drummond, A. J., A. Rambaut, B. Shapiro & O. G. Pybus, 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22: 1185–1192.

    Article  CAS  PubMed  Google Scholar 

  • Dudgeon, C. L., D. C. Blower, D. Broderick, J. L. Giles, B. J. Holmes, T. Kashiwagi, et al., 2012. A review of the application of molecular genetics for fisheries management and conservation of sharks and rays. Journal of Fish Biology 80: 1789–1843.

    Article  CAS  PubMed  Google Scholar 

  • Dulvy, N. K., J. K. Baum, S. Clarke, L. J. Compagno, E. Cortés, A. Domingo, et al., 2008. You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquatic Conservation 18: 459–482.

    Article  Google Scholar 

  • Drummond, A. J., & Bouckaert, R. R. (2015). Bayesian evolutionary analysis with BEAST. Cambridge University Press.

  • Dulvy, N. K., S. L. Fowler, J. A. Musickm, R. D. Cavanagh, P. M. Kyne, L. R. Harrison, et al., 2014. Extinction risk and conservation of the world’s sharks and rays. eLife 3: e00590.

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebert, D. A., S. L. Fowler & L. J. Compagno, 2013. Sharks of the world: a fully illustrated guide, Wild Nature Press, Plymouth:

    Google Scholar 

  • Ellis, J. R., J. Barker, S. R. M. Phillips, E. K. Meyers & M. Heupel, 2020. Angel sharks (Squatinidae): a review of biological knowledge and exploitation. Journal of Fish Biology. https://doi.org/10.1111/jfb.14613.

    Article  PubMed  Google Scholar 

  • Excoffier, L. & H. E. Lischer, 2010. Arlequin suite version 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.

    Article  PubMed  Google Scholar 

  • Excoffier, L., P. E. Smouse & J. M. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein, J., 1982. How can we infer geography and history from gene frequencies? Journal of Theoretical Biology 96: 9–20.

    Article  CAS  PubMed  Google Scholar 

  • Franco, B. C., O. Defeo, A. R. Piola, M. Barreiro, H. Yang, L. Ortega & O. O. Moller, 2020. Climate change impacts on the atmospheric circulation, ocean, and fisheries in the southwest South Atlantic Ocean: a review. Climatic Change 162: 2359–2377.

    Article  Google Scholar 

  • Fruet, P. F., E. R. Secchi, J. C. Di Tullio, P. C. Simões-Lopes, F. Daura-Jorge, A. P. Costa, et al., 2017. Genetic divergence between two phenotypically distinct bottlenose dolphin ecotypes suggests separate evolutionary trajectories. Ecology and Evolution 7(21): 9131–9143.

    Article  PubMed  PubMed Central  Google Scholar 

  • Fu, Y. X., 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaida, I. H., 1997. Population structure of the Pacific angelshark, Squatina californica (Squatiniformes: Squatinidae), around the California Channel Islands. Copeia 1997: 738–744.

    Article  Google Scholar 

  • García, G., S. Pereyra, V. Gutierrez, S. Oviedo, P. Miller & A. Domingo, 2014. Population structure of Squatina guggenheim (Squatiniformes, Squatinidae) from the south-wester Atlantic Ocean. Journal of Fish Biology 86: 186–202.

    Article  PubMed  Google Scholar 

  • Grant, W. A. S. & B. W. Bowen, 1998. Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. Journal of Heredity 89: 415–426.

    Article  Google Scholar 

  • Grant, W. S., 2015. Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. Journal of Heredity 106: 333–346.

    Article  PubMed  Google Scholar 

  • Heath, T. A., J. P. Huelsenbeck & T. Stadler, 2014. The fossilized birth–death process for coherent calibration of divergence-time estimates. Proceedings of the National Academy of Sciences 111(29): E2957–E2966.

    Article  CAS  Google Scholar 

  • Hellberg, M. E., R. S. Burton, J. E. Neigel & S. R. Palumbi, 2002. Genetic assessment of connectivity among marine populations. Bulletin of Marine Science 70: 273–290.

    Google Scholar 

  • Heled, J., 2010. Extended Bayesian skyline plot tutorial. http://beast-mcmc.googlecode.com/svn-history/r3936/trunk/doc/tutorial/EBSP/ebsp-tut.pdf. Accessed 24 August 2020.

  • Heled, J. & A. J. Drummond, 2008. Bayesian inference of population size history from multiple loci. BMC Evolutionary Biology 8: 289.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Herbert, T. D., K. T. Lawrence, A. Tzanova, L. C. Peterson, R. Caballero-Gill & C. S. Kelly, 2016. Late Miocene global cooling and the rise of modern ecosystems. Nature Geoscience 9: 843–847.

    Article  CAS  Google Scholar 

  • Hewitt, G., 2000. The genetic legacy of the Quaternary ice ages. Nature 405: 907–913.

    Article  CAS  PubMed  Google Scholar 

  • Hirschfeld, M., C. Dudgeon, M. Sheaves & A. Barnett, 2021. Barriers in a sea of elasmobranchs: From fishing for populations to testing hypotheses in population genetics. Global Ecology and Biogeography 00: 1–17.

    Google Scholar 

  • Instituto Chico Mendes de Conservação da Biodiversidade, 2018. Volume VI - Peixes. In: Instituto Chico Mendes de Conservação da Biodiversidade (org) Livro Vermelho da Fauna Brasileira Ameaçada de Extinção. ICMBio, Brasília

  • Iriarte, P. J. F., M. P. Alonso, D. E. Sabadin, P. A. Arauz & C. M. Iudica, 2011. Phylogeography of weakfish Cynoscion guatucupa (Perciformes: Sciaenidae) from the southwestern Atlantic. Scientia Marina 75: 701–706.

    Article  Google Scholar 

  • Karl, S. A., A. L. Castro & R. C. Garla, 2012. Population genetics of the nurse shark (Ginglymostoma cirratum) in the western Atlantic. Marine Biology 159: 489–498.

    Article  Google Scholar 

  • Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock & A. Drummond, 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.

    Article  PubMed  PubMed Central  Google Scholar 

  • Leigh, J. W. & D. Bryant, 2015. POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6: 1110–1116.

    Article  Google Scholar 

  • Lucifora, L. O., V. B. García, R. C. Menni & B. Worm, 2012. Spatial patterns in the diversity of sharks, rays, and chimaeras (Chondrichthyes) in the Southwest Atlantic. Biodiversity and Conservation 21: 407–419.

    Article  Google Scholar 

  • Ludt, W. B. & L. A. Rocha, 2015. Shifting seas: the impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. Journal of Biogeography 42: 25–38.

    Article  Google Scholar 

  • Lutz, V. A., V. Segura, A. I. Dogliotti, D. A. Gagliardini, A. A. Bianchi & C. F. Balestrini, 2010. Primary production in the Argentine Sea during spring estimated by field and satellite models. Journal of Plankton Research 32: 181–195.

    Article  CAS  Google Scholar 

  • Machado, L. F., J. de Souza Damasceno, A. A. Bertoncini, A. P. C. Farro, M. Hostim-Silva & C. Oliveira, 2017. Population genetic structure and demographic history of the spadefish, Chaetodipterus faber (Ephippidae) from Southwestern Atlantic. Journal of Experimental Marine Biology and Ecology 487: 45–52.

    Article  Google Scholar 

  • Machado, R. C., M. C. da Silva Cortinhas, M. C. Proietti & M. Haimovici, 2020. Genetic connectivity of black drum (Pogonias courbina) stocks in the southwestern Atlantic Ocean. Environmental Biology of Fishes 103(8): 913–926.

    Article  Google Scholar 

  • Márquez, A., A. M. Solé-Cava, A. N. Pereira, A. Vasconcellos & E. P. Lessa, 2017. Deep genetic divergence in the Southern kingcroaker Menticirrhus americanus in its southernmost distribution. Brazilian Journal of Oceanography 65: 515–519.

    Article  Google Scholar 

  • Mendonça, F. F., C. Oliveira, O. B. F. Gadig & F. Foresti, 2011. Phylogeography and genetic population structure of Caribbean sharpnose shark Rhizoprionodon porosus. Reviews in Fish Biology and Fisheries 21: 799–814.

    Article  Google Scholar 

  • Mendonça, F. F., C. Oliveira, O. B. F. Gadig & F. Foresti, 2013. Diversity and genetic population structure of the Brazilian sharpnose shark Rhizoprionodon lalandii. Aquatic Conservation: Marine and Freshwater Ecosystems 23: 850–857.

    Article  Google Scholar 

  • Miranda, L. V. & M. Haimovici, 2007. Changes in the population structure, growth and mortality of striped weakfish Cynoscion guatucupa (Sciaenidae, Teleostei) of southern Brazil between 1976 and 2002. Hydrobiologia 589: 69–78.

    Article  Google Scholar 

  • O’Brien, S. M., V. F. Gallucci & L. Hauser, 2013. Effects of species biology on the historical demography of sharks and their implications for likely consequences of contemporary climate change. Conservation Genetics 14: 125–144.

    Article  Google Scholar 

  • Oddone, M., C. A. Awruch, R. Barreto, P. Charvet, G. E. Chiaramonte, J. M. Cuevas, et al., 2019. Squatina guggenheim. The IUCN Red List of Threatened Species 2019: e.T130393378A130393975.

  • Odebrecht, C. & J. P. Castello, 2001. The convergence ecosystem in the Southwest Atlantic. In Seeliger, U. & B. Kjerfve (eds), Coastal marine ecosystems of Latin America Springer, Berlin: 147–165.

    Chapter  Google Scholar 

  • Ovenden, J. R., 2013. Crinkles in connectivity: combining genetics and other types of biological data to estimate movement and interbreeding between populations. Marine and Freshwater Research 64(3): 201–207.

    Article  Google Scholar 

  • Piola, A. R., E. J. Campos, O. O. Möller Jr., M. Charo & C. Martinez, 2000. Subtropical shelf front off eastern South America. Journal of Geophysical Research: Oceans 105: 6565–6578.

    Article  Google Scholar 

  • R Core Team, 2020. R: A language and Environment for Statistical Computing, R Foundation For Statistical Computing, Vienna

    Google Scholar 

  • Rabassa, J., A. M. Coronato & M. Salemme, 2005. Chronology of the Late Cenozoic Patagonian glaciations and their correlation with biostratigraphic units of the Pampean region (Argentina). Journal of South America Earth Sciences 20: 81–103.

    Article  Google Scholar 

  • Rambaut, A., A. J. Drummond, D. **e, G. Baele & M. A. Suchard, 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67(5): 901.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramírez-Amaro, S., D. Ramírez-Macías, R. Vázquez-Juárez, S. Flores-Ramírez, F. Galván-Magaña & J. N. Gutiérrez-Rivera, 2017. Population structure of the Pacific angelshark (Squatina californica) along the northwestern coast of Mexico based on the mitochondrial DNA control region. Ciencias Marinas 43: 69–80.

    Article  CAS  Google Scholar 

  • Ramos-Onsins, S. E. & J. Rozas, 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19: 2092–2100.

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues, R., S. Santos, M. Haimovici, U. Saint-Paul, I. Sampaio & H. Schneider, 2014. Mitochondrial DNA reveals population structuring in Macrodon atricauda (Perciformes: Sciaenidae): a study covering the whole geographic distribution of the species in the southwestern Atlantic. Mitochondrial DNA 25(2): 150–156.

    Article  CAS  PubMed  Google Scholar 

  • Rozas, J., A. Ferrer-Mata, J. C. Sánchez-DelBarrio, S. Guirao-Rico, P. Librado, S. E. Ramos-Onsins & A. Sánchez-Gracia, 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34: 3299–3302.

    Article  CAS  PubMed  Google Scholar 

  • Sandoval-Castillo, J., A. Rocha-Olivarez & E. F. Balford, 2004. Cryptic isolation of Gulf of California shovelnose guitarfish evidenced by mitochondrial DNA. Marine Biology 145: 983–988.

    Article  CAS  Google Scholar 

  • Santos, S., T. Hrbek, I. P. Farias, H. Schneider & I. Sampaio, 2006. Population genetic structuring of the king weakfish, Macrodon ancylodon (Sciaenidae), in Atlantic coastal waters of South America: deep genetic divergence without morphological change. Molecular Ecology 15: 4361–4373.

    Article  CAS  PubMed  Google Scholar 

  • Santos, T. P., D. O. Lessa, I. M. Venancio, C. M. Chiessi, S. Mulitza, H. Kuhnert, et al., 2017. Prolonged warming of the Brazil Current precedes deglaciations. Earth Planetary Science Letters 463: 1–12.

    Article  CAS  Google Scholar 

  • Stadler, T., 2010. Sampling-through-time in birth–death trees. Journal of Theoretical Biology 267(3): 396–404.

    Article  PubMed  Google Scholar 

  • Stelbrink, B., T. von Rintelen, G. Cliff & J. Kriwet, 2010. Molecular systematics and global phylogeography of angel sharks (genus Squatina). Molecular Phylogenetics and Evolution 54(2): 395–404.

    Article  PubMed  Google Scholar 

  • Toomey, L., D. Welsford, S. A. Appleyard,, A. Polanowski, C. Faux, B. E. Deagle, ... & S. Jarman, 2016. Genetic structure of Patagonian toothfish populations from otolith DNA. Antarctic Science 28(5): 347–360. https://doi.org/10.1017/S0954102016000183.

    Article  Google Scholar 

  • Vaidya, G., D. J. Lohman & R. Meier, 2011. SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics 27: 171–180.

    Article  PubMed  Google Scholar 

  • Vasconcellos, A. V., D. Lima, F. Bonhomme, M. Vianna & A. M. Solé-Cava, 2015. Genetic population structure of the commercially most important demersal fish in the Southwest Atlantic: the whitemouth croaker (Micropogonias furnieri). Fisheries Research 167: 333–337.

    Article  Google Scholar 

  • Vaz-dos-Santos, A. M., C. L. D. B. Rossi-Wongtschowski & J. L. D. Figueiredo, 2009. Merluccius hubbsi (Teleostei: Merlucciidae): stock identification based on reproductive biology in the South-Southeast Brazilian region. Brazilian Journal of Oceanography 57: 17–31.

    Article  Google Scholar 

  • Viñas, M. D., R. M. Negri, F. C. Ramírez & D. Hernández, 2002. Zooplankton assemblages and hydrography in the spawning area of anchovy (Engraulis anchoita) off Rio de la Plata estuary (Argentina–Uruguay). Marine and Freshwater Research 53: 1031–1043.

    Article  Google Scholar 

  • Vögler, R., A. C. Milessi & R. A. Quiñones, 2008. Influence of environmental variables on the distribution of Squatina guggenheim (Chondrichthyes, Squatinidae) in the Argentine-Uruguayan Common Fishing Zone. Fisheries Research 91: 212–221.

    Article  Google Scholar 

  • Vooren, C. M. & S. Klippel, 2005. Biologia e status de conservação dos cações-anjo Squatina guggenheim, S. occulta e S. argentina. In Vooren CM, Klippel S (ed) Ações para a conservação de tubarões e raias no sul do Brasil. Igaré, Porto Alegre: 262.

  • Vooren, C. M., S. Montealegre-Quijano, R. P. T. Lessa, R. R. P. Barreto, J. M. R. Soto, J. E. Kotas & R. A. dos Santos, 2018. Squatina guggenheim Marini, 1936. In Instituto Chico Mendes de Conservação da Biodiversidade (org) Livro Vermelho da Fauna Brasileira Ameaçada de Extinção: Volume VI – Peixes. ICMBio, Brasília: 1112–1116.

Download references

Acknowledgements

The authors are grateful to all fishermen from “Pró-Pesca Project: fishing the knowledge” for donating some specimens from Brazil, Dr. Luís Gustavo Cardoso (Instituto Oceanográfico, Universidade Federal do Rio Grande—FURG) and Me. Mariana Martins – FURG for sampling support. We are grateful to Fundação de Amparo a Pesquisa do Estado de São Paulo – FAPESP for financial support through the project granted to F. Mendonça #2017/17605-3. B.L.S.F. was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil, Finance Code 001.Fellowship for R.R.D was provided by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP 2017/02420-8). We also sincerely thank three anonymous reviewers and the editor whose suggestions helped improve and clarify this manuscript.

Funding

This study was supported by grants from the Fundação de Amparo a Pesquisa do Estado de São Paulo – FAPESP to F. Mendonça (#2017/17605-3) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES (Master’s degree fellowship to I. Bunholi).

Author information

Authors and Affiliations

  1. Laboratório de Genética Pesqueira e Conservação (GenPesC), Instituto do Mar, Universidade Federal de São Paulo (UNIFESP), Campus Baixada Santista, São Paulo, Brasil

    Ingrid Vasconcellos Bunholi, Bruno Lopes da Silva Ferrette, Rodrigo Rodrigues Domingues & Fernando Fernandes Mendonça

  2. Laboratório de Biologia e Genética de Peixes, Instituto de Biociências de Botucatu, Universidade Estadual Paulista Júlio de Mesquita Filho (UNESP), Bauru, Brasil

    Ingrid Vasconcellos Bunholi, Claudio Oliveira & Fausto Foresti

  3. Department of Biology, Indiana State University, Terre Haute, IN, USA

    Ingrid Vasconcellos Bunholi

  4. Laboratório de Genética da Conservação, Universidade Santa Cecília (UNISANTA), Santos, SP, Brasil

    Bruno Lopes da Silva Ferrette

  5. Laboratório de Pesquisas Biológicas (LAPEBio), Universidade Santa Cecília (UNISANTA), Acervo Zoológico, Santos, Brasil

    Matheus Marcos Rotundo

  6. Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina

    Juan Martín Cuevas, Mirta García & Sebastián Gómez

  7. Wildlife Conservation Society de Argentina, Amenábar 1595, P. 2, Of. 19, CABA, Argentina

    Juan Martín Cuevas

  8. Laboratório de Biologia de Teleósteos e Elasmobrânquios (LABITEL), Departamento de Ecologia e Zoologia, Universidade Federal de Santa Catarina (UFSC), Florianópolis, Brasil

    Renato Hajenius Aché de Freitas

Authors
  1. Ingrid Vasconcellos Bunholi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bruno Lopes da Silva Ferrette
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rodrigo Rodrigues Domingues
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matheus Marcos Rotundo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Juan Martín Cuevas
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mirta García
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sebastián Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Renato Hajenius Aché de Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudio Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Fausto Foresti
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Fernando Fernandes Mendonça
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

IVB, RRD and FFM conceived the ideas. MMR, JMC, MG, SG, RHAF provided sampling. IVB carried out laboratory work. IVB and BLSF analyzed the data. IVB led the writing of the first draft. All authors contributed to manuscript revision.

Corresponding author

Correspondence to Ingrid Vasconcellos Bunholi.

Ethics declarations

Conflict of interest

The authors have no conflict of interests.

Ethics approval

Not applicable.

Informed Consent

Not applicable.

Consent for publication

Not applicable.

Additional information

Handling Editor: Handling editor: Cécile Fauvelot

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2576 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bunholi, I.V., da Silva Ferrette, B.L., Domingues, R.R. et al. Multilocus phylogeography of the endemic and endangered angular angelshark (Squatina guggenheim) in the Southwest Atlantic Ocean. Hydrobiologia 849, 2177–2192 (2022). https://doi.org/10.1007/s10750-022-04855-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-022-04855-3

Keywords

Search

Navigation