Low genetic variability in Prochilodus lacustris and Prochilodus nigricans from river basins of northern and northeastern Brazil
DOI:
https://doi.org/10.20950/1678-2305/bip.2026.52.e974Keywords:
Maranhão, Neotropical region, Taxonomic, Migratory fishes, Hydrographic basinAbstract
The genus Prochilodus is an important fish resource. The various species within this genus are morphologically very similar, making reliable taxonomic identification difficult and creating uncertainty regarding the exact status of the different forms. This study aimed to evaluate the genetic differentiation between two species of Prochilodus belonging to the same lineage from the Maranhão and Amazon River basins based on mitochondrial DNA markers (16S rRNA, COI, Cyt b) and nuclear (TROP) DNA sequences. A total of 151 samples were collected from the Maranhão and Amazon rivers, followed by DNA extraction, polymerase chain reaction, sequencing, and data analysis, with the gene fragments analyzed separately and concatenated. The results revealed a strong genetic similarity between the species, with low genetic divergence values (0 to 0.35%) for the genes under study.
References
Abreu, J. M. S., Craig, J. M., Albert, J. S., & Piorski, N. M. (2019). Historical biogeography of fishes from coastal basins of Maranhão State, northeastern Brazil. Neotropical Ichthyology, 17(2), e180156. https://doi.org/10.1590/1982-0224-20180156
Abreu, J. M. S., Saraiva, A. C. S., Albert, J. S., & Piorski, N. M. (2020). Paleogeographic influences on freshwater fish distributions in northeastern Brazil. Journal of South American Earth Sciences, 102, 102692. https://doi.org/10.1016/j.jsames.2020.102692
Albert, J. S., Val, P., & Hoorn, C. (2018). The changing course of the Amazon River in the Neogene: Center stage for Neotropical diversification. Neotropical Ichthyology, 16(3), e180033. https://doi.org/10.1590/1982-0224-20180033
Ashley, P. J. (2007). Fish welfare: current issues in aquaculture. Applied Animal Behaviour Science, 104(3-4), 199-235. https://doi.org/10.1016/j.applanim.2006.09.001
Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Barros, M. C., Fraga, E. C., & Birindelli, J. L. (2011). Peixes da bacia do rio Itapecuru, no estado do Maranhão, Nordeste do Brasil. Journal of Biology, 71(2), 375-380. https://doi.org/10.1590/S1519-69842011000300006
Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K., Meier, R., Winker, K., Ingram, K. K., Das, I. (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution, 22(3), 148-155. https://doi.org/10.1016/j.tree.2006.11.004
Britski, H. A., Silimon, K. Z. S., & Lopes, B. S. (1999). Peixes do Pantanal: manual de Identificação Embrapa.
Calcagnotto, D., Schaefer, S. A., & Desalle, R. (2005). Relationships among characiform fishes inferred from analysis of nuclear and mitochondrial gene sequences. Molecular Phylogenetic and Evolution, 36(1), 135-153. https://doi.org/10.1016/j.ympev.2005.01.004
Cardoso, R. L., Silva, M. H. L., Carvalho-Neta, R. N. F., Castro, A. C. L., Ferreira, C. F. C., Ferreira, H. R. S., & Santos, D. M. S. (2019). Aspects of reproductive biology of curimba Prochilodus lacustris (Pisces, Prochilodontidae) in a tropical lake in Northeastern Brazil. Journal of Applied Ichthyology, 1-13. https://doi.org/10.1111/jai.13868
Carvalho, A. P. C., Collins, R. A., Martínez, J. G., Farias, L. P., & Hrbek, T. (2019). From shallow to deep divergences: mixed messages from Amazon Basin cichlids. Hydrobiologia, 832, 317-329. https://doi.org/10.1007/s10750-018-3790-x
Carvalho-Costa, L. F., Piorski, N. M., Willis, S. C., Galetti Jr., P. M., & Ortí, G. (2011). Molecular systematics of the neotropical shovelnose catfish genus Pseudoplatystoma Bleeker 1862 based on nuclear and mtDNA markers. Molecular Phylogenetic and Evolution, 59(1), 177-194. https://doi.org/10.1016/j.ympev.2011.02.005
Castro, R. M. C., & Vari, R. (2004). Detritivores of the South American fish family Prochilodontidae (Teleostei: Ostariophysi: Characiformes): a phylogenetic and revisionary study (Smithsonian Contributions to Zoology, vol. 622). Smithsonian Books. https://doi.org/10.5479/si.00810282.622
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). JModelTest2: more models, new heuristics and parallel computing. Nature Methods, 9, 772. https://doi.org/10.1038/nmeth.2109
Da Silva, R., Peloso P. L. V., Sturaro, M. J., Veneza, I., Sampaio, I., Schneider, H., & Gomes, G. (2017). Comparative analyses of species delimitation methods with molecular data in snappers (Perciformes: Lutjaninae). Mitochondrial DNA Part A, 29(7), 1108-1114. https://doi.org/10.1080/24701394.2017.1413364
Dinno, A. (2009). Exploring the sensitivity of horn’s parallel analysis to the distributional form of simulated data. Multivariate Behavioral Research, 44(3), 362-388. https://doi.org/10.1080/00273170902938969
Drummond, A. J., Suchard, A. M., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution, 29(8), 1969-1973. https://doi.org/10.1093/molbev/mss075
Ezard, T., Fujisawa, T., & Barraclough, T. G. (2009). SPLITS: Species’ limits by threshold statistics R package version 1.0-18/r45. Retrieved from https://r-forge.r-project.org/projects/splits/
Farias, I. P., Ortí, G., Sampaio, I., Schneider, H., & Meyer, A. (2001). Mitochondrial DNA phylogeny of the family Cichlidae: monophyly and fast molecular evolution of neotropical assemblage. Journal of Molecular Evolution, 48, 703-711. https://doi.org/10.1007/pl00006514
Ferreira, D. G., Souza-Shibatta, L., Shibatta, O. A., Sofia, S. H., Carlsson, J., Dias, J. H. P., Makrakis, S., & Makrakis, M. C. (2016). Genetic structure and diversity of migratory freshwater fish in a fragmented Neotropical River system. Reviews in Fish Biology and Fisheries, 27, 209-231. https://link.springer.com/article/10.1007/s11160-016-9441-2
Fonseca, F. S., Domingues, R. R., Hallerman, E. M., & Hilsdorf, A. W. S. (2017). Genetic diversity of an imperiled neotropical catfish and recommendations for its restoration. Frontiers in Genetics, 8, 196. https://doi.org/10.3389/fgene.2017.00196
Frable, B. W., Melo, B. F., Sidlauskas, B. L., Hoekzema, K., Vari, R. P., & Oliveira, C. (2016). Data on the multilocus molecular phylogenies of the Neotropical fish family Prochilodontidae (Teleostei: Characiformes). Data in Brief, ., 128-142. https://doi.org/10.1016/j.dib.2016.08.015
Fraga, E., Schneider, H., Nirchio, M., Santa-Brigida, E., Rodrigues-Filho, L. F., & Sampaio, I. (2007). Molecular phylogenetic analyses of mullets (Mugilidae, Mugiliformes) based on two mitochondrial genes. Jornal of Applied Ichthyology, 23, 598-604. https://doi.org/10.1111/j.1439-0426.2007.00911.x
Fraga, E., Silva, L. M. M., Schneider, H., Sampaio, I., & Barros, M. C. (2014). Variabilidade genética em populações naturais de Leporinus piau (Anostomidae, Characiformes) da bacia do Rio Itapecuru. Revista Trópica, 8(2), 28-40. https://doi.org/10.0000/rtcab.v8i2.1121
Friesen, V. L., Congdon, B. C., Kidd, M. G., & Birt, T. P. (1999). Polymerase chain reaction (PCR) primers for the amplification of five nuclear introns in vertebrates. Molecular Ecology, 8(12), 2147-2149. https://doi.org/10.1046/j.1365-294x.1999.00802-4.x
Fujisawa, T., & Barraclough, T. G. (2013). Delimiting species using single-locus data and the generalized mixed yule coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Systematic Biology, 62(5), 707-724. https://doi.org/10.1093/sysbio/syt033
Garavello, J. C., Garavello, J. P., & Oliveira, A. K. (2010). Ichthyofauna, fish supply and fishermen activities on the mid-Tocantins River, Maranhão State, Brazil. Brazilian Journal of Biology, 70(3), 575-585. https://doi.org/10.1590/S1519-69842010000300014
Godinho, A. L., & Kynard, B. (2006). Migration and spawning of radio-tagged Zulega Prochilodus argenteus in a dammed Brazilian river. Transactions of the American Fisheries Society, 135(3), 811-824. https://doi.org/10.1577/T04-176.1
Gouy, M., Guindon S., & Gascuel, O. (2010). SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution, 27(2), 221-224. https://doi.org/10.1093/molbev/msp259
Guimarães, K. L. A., Lima, M. P., Santana, D. J., Souza, M. F. B., Barbosa, R. S., & Rodrigues, L. R. R. (2022). DNA barcoding and phylogeography of the Hoplias malabaricus species complex. Scientific Reports, 12(1), 5288. https://doi.org/10.1038/s41598-022-09121-z
Guimarães, K. L. A., Rosso, J. J., González‐Castro, M., Souza, M. F., Díaz de Astarloa, J. M., & Rodrigues, L. R. (2022). A new species of Hoplias malabaricus species complex (Characiformes: Erythrinidae) from the Crepori River, Amazon basin, Brazil. Journal of Fish Biology, 100(2), 425-443. https://doi.org/10.1111/jfb.14953
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59(3), 307-321. https://doi.org/10.1093/sysbio/syq010
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium, 41, 95-98.
Hebert, P. D. N., Cywinska, A., Ball, S. L., & Ward, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society B, 270(1512), 313-321. https://doi.org/10.1098/rspb.2002.2218
Hubert, N., Duponchelle, F., Nuñez, J., Garcia-Davila, C., Paugy, D., & Renno, J. F. (2007). Phylogeography of the piranha genera Serrasalmus and Pygocentrus: implications for the diversification of the Neotropical ichthyofauna. Molecular Ecology, 16(10), 2115-2136. https://doi.org/10.1111/j.1365-294x.2007.03267.x
Hubert, N., Hanner, R., Holm, E., Mandrak, N. E., Taylor, E., Burridge, M., Watkinson, D., Dumont, P., Curry, A., Bentzen, P., Zhang, J., April, J., Bernatchez, L. (2008). Identifying Canadian freshwater fishes through DNA barcodes. PLoS One, 3(6), e2490. https://doi.org/10.1371/journal.pone.0002490
Kress, W. J., García-Robledo, C., Uriarte, M., & Erickson, D. L. (2015). DNA barcodes for ecology, evolution, and conservation. Trends in Ecology & Evolution, 30(1), 25-35. https://doi.org/10.1016/j.tree.2014.10.008
Kumar, S., Stecher, G., Li, M., Knyar, C., & Tamura, K. (2018). MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution, 35(6), 1547-1549. https://doi.org/10.1093/molbev/msy096
Limeira-Filho, D., Moraes, P. S. S., Almeida, M. S., Silva, A. C. C., Silva, J. L. N., Farias-Rodrigues, L., Teixeira, B. R. S., Anjos, J. V. X., Birindelli, J. L. O., Barros, M. C., & Fraga, E. C. (2023). Fish diversity in the rivers that drain the Baixada Maranhense and the Mearim basin in northeastern Brazil. Brazilian Journal of Biology, 83, e273525. https://doi.org/10.1590/1519-6984.273525
Lopes, U., Galetti Jr., P. M., & Freitas, P. D. (2020). Hidden diversity in Prochilodus nigricans: A new genetic lineage within the Tapajós River basin. PLoS One, 15(8), e0237916. https://doi.org/10.1371/journal.pone.0237916
Lundberg, J. G., Marshall, L. G., Guerrero, J., Horton, B., Malabarba, M. C. S. L., & Wesselingh, F. (1998). The stage for neotropical fish diversification: a history of tropical South American rivers. In: Malabarba, L. R., Reis, R. E., Vari, R. P., Lucena, Z. M. S., & Lucena, C. A. S. (editors), Phylogeny and classification of Neotropical fishes (pp. 13-48). EDUPUCRS.
Machado, V. N., Willis, S. C., Teixeira, A. S., Hrbek, T., & Farias, I. P. (2017). Population genetic structure of the Amazonian black flannelmouth characin (Characiformes, Prochilodontidae: Prochilodus nigricans Spix & Agassiz, 1829): contemporary and historical gene flow of a migratory and abundant fishery species. Environmental Biology of Fishes, 100(1), 1-16. https://doi.org/10.1007/s10641-016-0547-0
Melo, B. F., Dorini, B. F., Foresti, F., & Oliveira, C. (2018). Little divergence among mitochondrial lineages of Prochilodus (Teleostei, Characiformes). Frontiers in Genetics, 9, 107. https://doi.org/10.3389/fgene.2018.00107
Melo, B. F., Sidlauskas, B. L., Hoekzema, K., Frable, B. W., Vari, R. P., & Oliveira, C. (2016). Molecular phylogenetics of the Neotropical fish family Prochilodontidae (Teleostei: Characiformes). Molecular Phylogenetics and Evolution, 102, 189-201. https://doi.org/10.1016/j.ympev.2016.05.037
Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop, 1-8. https://doi.org/10.1109/GCE.2010.5676129
Mondin, L. A. D. C., Machado, C. B., Resende, E. K. D., Marques, D. K., & Galetti Jr., P. M. (2018). Genetic pattern and demographic history of Salminus brasiliensis: Population expansion in the Pantanal Region during the Pleistocene. Frontiers in Genetics, 9(1), 1. https://doi.org/10.3389/fgene.2018.00001
Mota, S. Q., & Ruffino, M. L. (1997). Biologia e pesca do curimatá (Prochilodus nigricans Agassiz, 1829) (Prochilodontidae) no Médio Amazonas. Revista Unimar, 19(2), 493-508.
Nascimento, M. H., Almeida, M. S., Veira, M. N., Limeira Filho, D., Lima, R. C., Barros, M. C., & Fraga, E. C. (2016). DNA barcoding reveals high levels of genetic diversity in the fishes of the Itapecuru Basin in Maranhão, Brazil. Genetics and Molecular Research, 15(3). https://doi.org/10.4238/gmr.15038476
Nogueira, A. F., Oliveira, C., Langeani, F., & Netto-Ferreira, A. L. (2021). Molecular species delimitation of the genera Anodus, Argonectes, Bivibranchia and Micromischodus (Ostariophysi: Characiformes). Neotropical Ichthyology, 19(4), e210005. https://doi.org/10.1590/1982-0224-2021-0005
Ochoa, L. E., Melo, B. F., García-Melo, J. E., Maldonado-Ocampo, J. A., Souza, C. S., Albornoz-Garzón, J. G., Conde-Saldaña, C. C., Villa-Navarro, F., Ortega-Lara, A., & Oliveira, C. (2020). Species delimitation reveals an underestimated diversity of Andean catfishes of the family Astroblepidae (Teleostei: Siluriformes). Neotropical Ichthyology, 18(4), e200048. https://doi.org/10.1590/1982-0224-2020-0048
Palumbi, S. (1991). The simple fool’s guide to PCR, version 2.0 University of Hawaii.
Palumbi, S. R. (1996). Nucleic acids II: the polymerase chain reaction. In: Hillis, D., Moritz, C., & Mable, B. (Eds.), Molecular Systematics (pp. 205-247). Sinauer Associates.
Papa, Y., Bail, P. Y. L., & Covain, R. (2021). Genetic landscape clustering of a large DNA barcoding data set reveals shared patterns of genetic divergence among freshwater fishes of the Maroni Basin. Molecular Ecology Resources, 21(6), 2109-2124. https://doi.org/10.1111/1755-0998.13402
Paradis, E., & Schliep, K. (2019). Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics, 35(3), 526-528. https://doi.org/10.1093/bioinformatics/bty633
Pauls, S. U., Nowak, C., Bálint, M., & Pfenninger, M. (2013). The impact of global climate change on genetic diversity within populations and species. Molecular Ecology, 22(4), 925-946. https://doi.org/10.1111/mec.12152
Piorski, N. M. (2010). Diversidade genética e filogeografia das espécies Hoplias malabaricus (Bloch, 1794) e Prochilodus lacustris Steindachner, 1907 no nordeste do Brasil [PhD Thesis, Universidade Federal de São Carlos, São Carlos).
Piorski, N. M., Castro, A. C. L., & Sousa-Neto, M. A. S. (2007). Peixes do cerrado da região sul maranhense. In Barreto, L. N. (ed.), Cerrado Norte do Brasil (pp. 177-212). USEB.
Puillandre, N., Brouillet, S., & Achaz, G. (2020). ASAP: Assemble Species by Automatic Partitioning. Molecular Ecology Resources, 21(2), 609-620. https://doi.org/10.1111/1755-0998.13281
Puillandre, N., Lambert, A., Brouillet, S., & Achaz, G. (2012). ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology, 21(8), 1864-1877. https://doi.org/10.1111/j.1365-294x.2011.05239.x
Queiroz, L. J., Ohara, W. M., & Vari, R. P. (2013). Prochilodontidae. In: Queiroz, L. J. (ed.), Peixes do Rio Madeira (3 vols., pp. 140-146). Dialeto Latin American Documentary.
Rambaut, A. (2014). FigTree v1.4.2 Retrieved from http://tree.bio.ed.ac.uk/software/figtree/
Rambaut, A., Suchard, M. A., Xie, D., & Drummond, A. J. (2014). Tracer v1.6 Retrieved from http://tree.bio.ed.ac.uk/software/tracer
Ramirez, J. L., Birindelli, J. L., Carvalho, D. C., Affonso, P. R. A. M., Venere, P. C., Ortega, H., Carrillo-Avila, M., Rodríguez-Pulido, J. A., & Galetti Jr., P. M. J. R. (2017). Revealing Hidden diversity of the underestimated neotropical ichthyofauna: DNA barcoding in the recently described genus Megaleporinus (Characiformes: Anostomidae). Frontiers in Genetics, 8, 149. https://doi.org/10.3389/fgene.2017.00149
Ramos, T. P. A., Ramos, R. T. C., & Ramos, S. A. Q. A. (2014). Ichthyofauna of the Parnaiba river Basin. Northeastern Brazil. Biota Neotropica, 14(1), e20130039. https://doi.org/10.1590/S1676-06020140039
Rossini, B. C., Oliveira, C. A. M., Melo, F. A. G. D., Bertaco, V. D. A., Astarloa, J. M. D. D., Rosso, J. J., Foresti, F., & Oliveira, C. (2016). Highlighting Astyanax species diversity through DNA barcoding. PLoS One, 11(12), e0167203. https://doi.org/10.1371/journal.pone.0167203
Rozas, J., Sánchez-DelBarrio, J. C., Messeguer, X., & Rozas, R. (2018). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics, 19(8), 2496-2497. https://doi.org/10.1093/bioinformatics/btg359
Rueda, E. C., Carriquiriborde, P., Monzón, A. M., Somoza, G. M., & Ortí, G. (2013). Seasonal variation in genetic population structure of sábalo (Prochilodus lineatus) in the Lower Uruguay River. Genetica, 141, 401-407. https://doi.org/10.1007/s10709-013-9739-0
Sales, N. G., Pessali, T. C., Andrade Neto, F. R., & Carvalho, D. C. (2018). Introgression from non-native species unveils a hidden threat to the migratory Neotropical fish Prochilodus hartii Biological Invasion, 20, 555-566. https://doi.org/10.1007/s10530-017-1556-4
Sanger, F., Nicklen, S., & Coulson, A. R. (1977). DNA sequencing with chain-terminating inhibitors. Proceedings of the National Academy of Sciences, 74(12), 5463-5467. https://doi.org/10.1073/pnas.74.12.5463
Santos, G. S. A. (2007). Análise filogenética das espécies de Leporinus (Ostariophysi: Characiformes: Anostomidae) das Bacias do Prata e São Francisco [Masters thesis, Universidade Estadual Paulista “Júlio de Mesquita Filho”).
Santos, G. M., Mérona, B., Juras, A. A., & Jégu, M. (2004). Peixes do Baixo Rio Tocantins: 20 anos depois da Usina Hidrelétrica Tucuruí Eletronorte.
Santos, S., Schneider, H., & Sampaio, I. (2003). Genetic differentiation of Macrodon ancylodon (Sciaenidae, Perciformes) populations in Atlantic coastal waters of South America as revealed by mtDNA analysis. Genetics and Molecular Biology, 26(2), 151-161. https://doi.org/10.1590/S1415-47572003000200008
Silva-Santos, R., Ramirez, J. L., Galetti Jr., P. M., & Freitas, P. D. (2018). Molecular evidences of a hidden complex scenario in Leporinus cf. friderici Frontiers in Genetics, 9, 47. https://doi.org/10.3389/fgene.2018.00047
Sivasundar, A., Bermingham, E., & Ortí, G. (2001). Population structure and biogeography of migratory freshwater fishes (Prochilodus: Characiformes) in major South American rivers. Molecular Ecology, 10(2), 407-417. https://doi.org/10.1046/j.1365-294x.2001.01194.x
Smith, M. F., & Patton, J. L. (1993). The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biological Journal of the Linnean Society, 50(3), 149-177. https://doi.org/10.1111/j.1095-8312.1993.tb00924.x
Soares, E. C. (2005). Peixes do Mearim Instituto Geia.
Soares Júnior, A. V., Hasui, Y., Costa, J. B. S., & Machado, F. B. (2011). Evolução do rifteamento e paleogeografia da margem atlântica equatorial do Brasil: Triássico ao Holoceno. Geociências, 30(4), 669-692.
Souza, C. R., Affonso, P. R. A. M., Bitencourt, J. A., Sampaio, I., & Carneiro, P. L. S. (2018). Species validation and cryptic diversity in the Geophagus brasiliensis Quoy & Gaimard, 1824 complex (Teleostei, Cichlidae) from Brazilian coastal basins as revealed by DNA analyses. Hydrobiologia, 809, 309-321. https://doi.org/10.1007/s10750-017-3482-y
Stamatakis, A. (2014). RAxML Version 8: a tool for phylogenetic analysis and postanalysis of large phylogenies. Bioinformatics, 30(9), 1312-1313. https://doi.org/10.1093/bioinformatics/btu033
Stanley, S. M. (1979). Macroevolution: pattern and process The John Hopkins University Press.
Suchard, M. A., Lemey, P., Baele, G., Ayres, D. L., Drummond, A. J., & Rambaut, A. (2018). Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution, 4(1), vey016. https://doi.org/10.1093/ve/vey016
Taphorn, D. C. (1992). The characiform fishes of the Apure River drainage, Venezuela. BioLlania.
Turner, T., McPhee, M. V., Campbell, P., & Winemiller, K. O. (2004). Phylogeography and intraspecific genetic variation of prochilodontid fishes’ endemic to rivers of northern South America. Journal of Fish Biology, 64(1), 186-201. https://doi.org/10.1111/j.1095-8649.2004.00299.x
Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). Springer. Retrieved from https://www.stats.ox.ac.uk/pub/MASS4/
Venables, W. N., & Smith, D. M. (2021). The R Core Team. R version 4.1.0 Patched R: A Programming Environment for Data Analysis and Graphics. Foundation for Statistical Computing.
Ward, R. D., Zemlbak, 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 B, 360(1462), 1847-1857. https://doi.org/10.1098/rstb.2005.1716
Wilkinson, M. J., Marshall, L. G., & Lundberg, J. G. (2006). River behavior on megafans and potential influences on diversification and distribution of aquatic organisms. Journal of South American Earth Sciences, 21(1-2), 151-172. https://doi.org/10.1016/j.jsames.2005.08.002
Zhang, J., Kapli, P., Pavlidis, P., & Stamatakis, A. (2013). A general species delimitation method with applications to phylogenetic placements. Bioinformatics, 29(22), 2869-2876. https://doi.org/10.1093/bioinformatics/btt499
Downloads
Published
Issue
Section
License
Copyright (c) 2026 Elidy Rayane de Rezende Franca, Jordânia Leticia do Nascimento Silva, Fernanda da Conceição Silva, Maria Histelle Sousa Nascimento, Fabiano Corrêa, Maria Claudene Barros, Elmary da Costa Fraga
This work is licensed under a Creative Commons Attribution 4.0 International License.
