Genetic diversity of an undescribed cryptic maskray (Neotrygon sp.) species from Fiji

Kerstin Glaus; Epeli Loganimoce; Gauthier Mescam; Sharon A. Appleyard

doi:10.1071/PC23064

RESEARCH ARTICLE (Open Access)

Previous Next Contents Vol 30(5)

Genetic diversity of an undescribed cryptic maskray (Neotrygon sp.) species from Fiji

Kerstin Glaus

^A ^* , Epeli Loganimoce

^A , Gauthier Mescam

^B and Sharon A. Appleyard

^C

+ Author Affiliations

- Author Affiliations

^A School of Agriculture, Geography, Environment, Ocean and Natural Sciences, SAGEONS, The University of the South Pacific, Laucala Campus, Suva, Fiji.

^B Projects Abroad UK, Limited Telecom House, 125-135 Preston Road, Brighton BN1 6AF, England.

^C CSIRO Australian National Fish Collection, National Research Collections Australia, Hobart, Tas, Australia.

^* Correspondence to: kerstin.glaus@usp.ac.fj

Handling Editor: Karissa Lear

Pacific Conservation Biology 30, PC23064 https://doi.org/10.1071/PC23064

Submitted: 22 December 2023 Accepted: 18 August 2024 Published: 12 September 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

The extinction risk of sharks and rays exceeds that of most other vertebrates. Genetic analyses can help identify conservation risks.

Aims

Identification of Fiji’s maskray and testing the null hypothesis of no genetic differentiation within the species over time.

Methods

Mitochondrial DNA cytochrome oxidase subunit 1 (COI) barcoding was used for species identification, and DArT-seq technology to monitor the genetic diversity. Cohort samples were collected in 2015 and 2022. A subset from each cohort was barcoded. The genetic survey was complemented by a size comparison between the two cohorts.

Key results

Barcoding of the COI gene showed a maximum similarity of 97.84% to Kuhl’s maskray (Neotrygon kuhlii) and 96.83% to the Coral Sea maskray (Neotrygon trigonoides), but no higher-level distinct species match to reference sequences in the Barcode of Life Datasystem. Genotyping of 56 individuals in two cohorts yielded 21,293 single nucleotide polymorphisms (SNPs), and 3871 SNPs per individual were retained. The neutral genetic diversity remained stable over time. The 2015 cohort showed positive inbreeding, with one full-sibling pair identified in each cohort. Body size comparisons indicated a significant reduction in disc length and width in the 2022 cohort.

Conclusions

The smaller body size of the 2022 cohort may hint at increased fishing pressure, but genetic diversity has not been affected. Thus, the null hypothesis is accepted.

Implications

These findings provide insights into the genetic diversity of Fiji’s maskray and enable a genetic comparison with current Neotrygon species known in the region. Taxonomy confirmation is needed, but the presence of a cryptic or potentially new maskray in Fiji seems plausible.

Keywords: batoids, COI barcoding, Dasyatidae, elasmobranchs, morphology, Oceania, single nucleotide polymorphisms, taxonomy.

References

Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends in Ecology & Evolution 23(6), 327-337.
| Crossref | Google Scholar | PubMed |

Allendorf FW, Luikart GH, Aitken SN (2012) ‘Conservation and the genetics of populations.’ (John Wiley & Sons)

Arlyza IS, Shen K-N, Durand J-D, Borsa P (2013) Mitochondrial haplotypes indicate parapatric-like phylogeographic structure in blue-spotted maskray (Neotrygon kuhlii) from the Coral Triangle region. Journal of Heredity 104(5), 725-733.
| Crossref | Google Scholar | PubMed |

Aschliman NC, Claeson KM, McEachran JD (2012) Phylogeny of batoidea. In ‘Biology of Sharks and their relatives’. 2nd edn. (Eds JC Carrier, JA Musick, MR Heithaus) pp. 57–96. (CRC Press)

Awruch CA (2015) Reproduction strategies. In ‘Fish physiology, Vol. 34.’ pp. 255–310. (Academic Press)

Beheregaray LB (2008) Twenty years of phylogeography: the state of the field and the challenges for the Southern Hemisphere. Molecular Ecology 17(17), 3754-3774.
| Crossref | Google Scholar | PubMed |

Belkhir K (1999) GENETIX, logiciel sous WindowsTM pour la génétique des populations. Available at http://www.univmontp2.fr/~genetix

Borsa P, Arlyza IS, Laporte M, Berrebi P (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.
| Crossref | Google Scholar |

Bradley D, Conklin E, Papastamatiou YP, McCauley DJ, Pollock K, Kendall BE, Gaines SD, Caselle JE (2017) Growth and life history variability of the grey reef shark (Carcharhinus amblyrhynchos) across its range. PLoS ONE 12(2), e0172370.
| Crossref | Google Scholar |

Carson AR, Smith EN, Matsui H, Brækkan SK, Jepsen K, Hansen J-B, Frazer KA (2014) Effective filtering strategies to improve data quality from population-based whole exome sequencing studies. BMC Bioinformatics 15(1), 125.
| Crossref | Google Scholar |

Chapman DD, Feldheim KA, Papastamatiou YP, Hueter RE (2015) There and back again: a review of residency and return migrations in sharks, with implications for population structure and management. Annual Review of Marine Science 7, 547-570.
| Crossref | Google Scholar | PubMed |

Chevolot M, Hoarau G, Rijnsdorp AD, Stam WT, Olsen JL (2006) Phylogeography and population structure of thornback rays (Raja clavata L., Rajidae). Molecular Ecology 15(12), 3693-3705.
| Crossref | Google Scholar | PubMed |

Connell J (2021) COVID-19 and tourism in Pacific SIDS: lessons from Fiji, Vanuatu and Samoa? The Round Table 110(1), 149-158.
| Crossref | Google Scholar |

Cortés E (2000) Life history patterns and correlations in sharks. Reviews in Fisheries Science 8(4), 299-344.
| Crossref | Google Scholar |

Davila F, Bourke RM, McWilliam A, Crimp S, Robins L, Van Wensveen M, Alders RG, Butler JRA (2021) COVID-19 and food systems in Pacific Island Countries, Papua New Guinea, and Timor-Leste: opportunities for actions towards the sustainable development goals. Agricultural Systems 191, 103137.
| Crossref | Google Scholar |

Devloo-Delva F, Maes GE, Hernández SI, Mcallister JD, Gunasekera RM, Grewe PM, Thomson RB, Feutry P (2019) Accounting for kin sampling reveals genetic connectivity in Tasmanian and New Zealand school sharks, Galeorhinus galeus. Ecology and Evolution 9(8), 4465-4472.
| Crossref | Google Scholar | PubMed |

Devloo-Delva F, Burridge CP, Kyne PM, Brunnschweiler JM, Chapman DD, Charvet P, Chen X, Cliff G, Daly R, Drymon JM, Espinoza M, Fernando D, Barcia LG, Glaus K, González-Garza BI, Grant MI, Gunasekera RM, Hernandez S, Hyodo S, Jabado RW, Jaquemet S, Johnson G, Ketchum JT, Magalon H, Marthick JR, Mollen FH, Mona S, Naylor GJP, Nevill JEG, Phillips NM, Pillans RD, Postaire BD, Smoothey AF, Tachihara K, Tillet BJ, Valerio-Vargas JA, Feutry P (2023) From rivers to ocean basins: the role of ocean barriers and philopatry in the genetic structuring of a cosmopolitan coastal predator. Ecology and Evolution 13(2), e9837.
| Crossref | Google Scholar |

DiBattista JD (2008) Patterns of genetic variation in anthropogenically impacted populations. Conservation Genetics 9, 141-156.
| Crossref | Google Scholar |

Domingues RR, Hilsdorf AWS, Gadig OBF (2018) The importance of considering genetic diversity in shark and ray conservation policies. Conservation Genetics 19, 501-525.
| Crossref | Google Scholar |

Dudgeon CL, Blower DC, Broderick D, Giles JL, Holmes BJ, Kashiwagi T, Krück NC, Morgan JAT, Tillett BJ, Ovenden JR (2012) A review of the application of molecular genetics for fisheries management and conservation of sharks and rays. Journal of Fish Biology 80(5), 1789-1843.
| Crossref | Google Scholar | PubMed |

Dulvy NK, Pacoureau N, Rigby CL, Pollom RA, Jabado RW, Ebert DA, Finucci B, Pollock CM, Cheok J, Derrick DH, Herman KB, Sherman CS, VanderWright WJ, Lawson JM, Walls RHL, Carlson JK, Charvet P, Bineesh KK, Fernando D, Ralph GM, Matsushiba JH, Hilton-Taylor C, Fordham SV, Simpfendorfer CA (2021) Overfishing drives over one-third of all sharks and rays toward a global extinction crisis. Current Biology 31(21), 4773-4787.e8.
| Crossref | Google Scholar | PubMed |

Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14(8), 2611-2620.
| Crossref | Google Scholar | PubMed |

Excoffier L (2015) Arlequin ver 3.5 22. Institute of Ecology and Evolution, University of Berne. Swiss Institute of Bioinformatics.

Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10(3), 564-567.
| Crossref | Google Scholar | PubMed |

Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4), 1567-1587.
| Crossref | Google Scholar | PubMed |

Feldheim KA, Gruber SH, Ashley MV (2001) Population genetic structure of the lemon shark (Negaprion brevirostris) in the western Atlantic: DNA microsatellite variation. Molecular Ecology 10(2), 295-303.
| Crossref | Google Scholar | PubMed |

Ferretti F, White WT (2015) Neotrygon ningalooensis. The IUCN Red List of Threatened Species 2015: e.T195463A68636829. Available at https://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T195463A68636829.en [accessed 30 August 2024]

Finucci B, White WT, Kemper JM, Naylor GJP (2018) Redescription of Chimaera ogilbyi (Chimaeriformes; Chimaeridae) from the Indo-Australian region. Zootaxa 4375(2), 191-210.
| Crossref | Google Scholar | PubMed |

Foll M (2012) BayeScan v2. 1 user manual. Ecology 20(10), 1450-1462.
| Google Scholar |

Foll M, Gaggiotti O (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180(2), 977-993.
| Crossref | Google Scholar | PubMed |

Francis MP (1996) Observations on a pregnant white shark with a review of reproductive biology. In ‘Great white sharks: the biology of Carcharodon carcharias’. (Eds AP Klimley, DG Ainley) pp. 157–172. (Academic Press)

Frankham R (2003) Genetics and conservation biology. Comptes Rendus. Biologies 326, 22-29.
| Crossref | Google Scholar |

Glaus K (2019) Biology and conservation of the bull shark (Carcharhinus leucas) in Fiji. PhD. Thesis. The University of the South Pacific, Suva.

Glaus K, Appleyard S (2024) Genetic diversity, kinship, and polychromatism in the spotted eagle ray Aetobatus ocellatus of Fiji. Diversity in press.
| Google Scholar |

Glaus KBJ, Appleyard SA, Stockwell B, Brunnschweiler JM, Shivji M, Clua E, Marie AD, Rico C (2020) Insights into insular isolation of the Bull Shark, Carcharhinus leucas (Müller and Henle, 1839), in Fijian Waters. Frontiers in Marine Science 7, 586015.
| Crossref | Google Scholar |

Glaus K, Savou R, Brunnschweiler JM (2024a) Characteristics of Fiji’s small-scale ray fishery and its relevance to food security. Marine Policy 163, 106082.
| Crossref | Google Scholar |

Glaus K, Gordon L, Vierus T, Marosi ND, Sykes H (2024b) Rays in the shadows: batoid diversity, occurrence, and conservation status in Fiji. Biology 13(2), 73.
| Crossref | Google Scholar |

Goldman KJ, Cailliet GM, Andrews AH, Natanson LJ (2012) ‘Age determination and validation in chondrichthyan fishes. Biology of sharks and their relatives,’ 2nd edn. pp. 423–451. (CRC Press: Boca Raton, Florida)

Gondro C, Lee SH, Lee HK, Porto-Neto LR (2013) Quality control for genome-wide association studies. In ‘Genome-wide association studies and genomic prediction’, (Eds C Gondro, J van der Werf, B Hayes) pp. 129–147. (Humana Press)

Hasegawa M, Kishino H, Yano T-A (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160-174.
| Crossref | Google Scholar | PubMed |

Hata E, Motomura H (2024) Neotrygon yakkoei, a new bluespotted maskray (Dasyatidae) from Japan. Ichthyological Research
| Crossref | Google Scholar |

Hedgecock D (1994) Temporal and spatial genetic structure of marine animal populations in the California Current. California Cooperative Oceanic Fisheries Investigations Reports 35, 73-81.
| Google Scholar |

Hernández S, Daley R, Walker T, Braccini M, Varela A, Francis MP, Ritchie PA (2015) Demographic history and the South Pacific dispersal barrier for school shark (Galeorhinus galeus) inferred by mitochondrial DNA and microsatellite DNA mark. Fisheries Research 167, 132-142.
| Crossref | Google Scholar |

Heupel MR, Carlson JK, Simpfendorfer CA (2007) Shark nursery areas: concepts, definition, characterization and assumptions. Marine Ecology Progress Series 337, 287-297.
| Crossref | Google Scholar |

Hirschfeld M, Dudgeon C, Sheaves M, Barnett A (2021) Barriers in a sea of elasmobranchs: from fishing for populations to testing hypotheses in population genetics. Global Ecology and Biogeography 30(11), 2147-2163.
| Crossref | Google Scholar |

Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Molecular Ecology Resources 9(5), 1322-1332.
| Crossref | Google Scholar | PubMed |

Jabado RW, Kyne PM, Pollom RA, Ebert DA, Simpfendorfer CA, Ralph GM, Al Dhaheri SS, Akhilesh KV, Ali K, Ali MH, Al Mamari TMS, Bineesh KK, El Hassan IS, Fernando D, Grandcourt EM, Khan MM, Moore ABM, Owfi F, Robinson DP, Romanov E, Soares A-L, Spaet JLY, Tesfamichael D, Valinassab T, Dulvy NK (2018) Troubled waters: threats and extinction risk of the sharks, rays and chimaeras of the Arabian Sea and adjacent waters. Fish and Fisheries 19(6), 1043-1062.
| Crossref | Google Scholar |

Jacobsen IP, Bennett MB (2010) Age and growth of Neotrygon picta, Neotrygon annotata and Neotrygon kuhlii from north-east Australia, with notes on their reproductive biology. Journal of Fish Biology 77(10), 2405-2422.
| Crossref | Google Scholar |

Jacobsen IP, Kyne PM, Last PR (2015) Neotrygon annotata. The IUCN Red List of Threatened Species 2015: e.T60150A68636040. Available at https://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T60150A68636040.en. [accessed 30 August 2024]

Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24(11), 1403-1405.
| Crossref | Google Scholar | PubMed |

Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27(21), 3070-3071.
| Crossref | Google Scholar | PubMed |

Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources 10(3), 551-555.
| Crossref | Google Scholar | PubMed |

Kalinowski ST, Wagner AP, Taper ML (2006) ML-RELATE: a computer program for maximum likelihood estimation of relatedness and relationship. Molecular Ecology Notes 6(2), 576-579.
| Crossref | Google Scholar |

Klimley AP (1987) The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environmental Biology of Fishes 18, 27-40.
| Crossref | Google Scholar |

Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across K. Molecular Ecology Resources 15(5), 1179-1191.
| Crossref | Google Scholar | PubMed |

Kornfield I, Sidell BD, Gagnon PS (1982) Stock definition in Atlantic herring (Clupea harengus harengus): genetic evidence for discrete fall and spring spawning populations. Canadian Journal of Fisheries and Aquatic Sciences 39(12), 1610-1621.
| Crossref | Google Scholar |

Kuguru G, Gennari E, Wintner S, Dicken ML, Klein JD, Rhode C, Bester-van der Merwe AE (2019) Spatio-temporal genetic variation of juvenile smooth hammerhead sharks in South Africa. Marine Biology Research 15(10), 568-579.
| Crossref | Google Scholar |

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(6), 1547-1549.
| Crossref | Google Scholar | PubMed |

Kyne PM, Finucci B (2018) Neotrygon kuhlii. The IUCN Red List of Threatened Species 2018: e.T116847578A116849874. Available at https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T116847578A116849874.en [accessed 30 August 2024]

Lacson JM, Morizot DC (1991) Temporal genetic variation in subpopulations of bicolor damselfish (Stegastes partitus) inhabiting coral reefs in the Florida Keys. Marine Biology 110, 353-357.
| Crossref | Google Scholar |

Last P, Naylor G, Séret B, White W, de Carvalho M, Stehmann M (2016a) ‘Rays of the World.’ (CSIRO publishing)

Last PR, Naylor GJP, Manjaji-Matsumoto BM (2016b) A revised classification of the family Dasyatidae (Chondrichthyes: Myliobatiformes) based on new morphological and molecular insights. Zootaxa 4139(3), 345-368.
| Crossref | Google Scholar | PubMed |

Last PR, White WT, Seret B (2016c) Taxonomic status of maskrays of the Neotrygon kuhlii species complex (Myliobatoidei: Dasyatidae) with the description of three new species from the Indo-West Pacific. Zootaxa 4083(4), 533-561.
| Crossref | Google Scholar | PubMed |

Le Port A, Lavery S (2012) Population structure and phylogeography of the short-tailed stingray, Dasyatis brevicaudata (Hutton 1875), in the Southern Hemisphere. Journal of Heredity 103(2), 174-185.
| Crossref | Google Scholar | PubMed |

Lieber L, Hall G, Hall J, Berrow S, Johnston E, Gubili C, Sarginson J, Francis M, Duffy C, Wintner SP, Doherty PD, Godley BJ, Hawkes LA, Witt MJ, Henderson SM, de Sabata E, Shivji MS, Dawson DA, Sims DW, Jones CS, Noble LR (2020) Spatio-temporal genetic tagging of a cosmopolitan planktivorous shark provides insight to gene flow, temporal variation and site-specific re-encounters. Scientific Reports 10(1), 1661.
| Crossref | Google Scholar |

Liu SYV, Chen Y-Y, Cheng C (2023) Genetic structure and relatedness of juvenile sicklefin lemon shark (Negaprion acutidens) at Dongsha Island. Scientific Reports 13(1), 988.
| Crossref | Google Scholar |

Lotterhos KE, Whitlock MC (2014) Evaluation of demographic history and neutral parameterization on the performance of F_ST outlier tests. Molecular Ecology 23(9), 2178-2192.
| Crossref | Google Scholar | PubMed |

Luikart G, Kardos M, Hand BK, Rajora OP, Aitken SN, Hohenlohe PA (2018) Population genomics: advancing understanding of nature. In ‘Population genomics: concepts, approaches and applications’. (Ed. O Rajora) pp. 3–79. (Springer)

Madden T (2003) The BLAST sequence analysis tool. In ‘The NCBI handbook’. (Ed. J McEntyre) pp. 425–436. (National Library of Medicine, National Center for Biotechnology Information)

Mangubhai S, Fox M, Nand Y (2017) Value chain analysis of the wild caught mud crab fishery in Fiji. Wildlife Conservation Society, Suva, Fiji.

Marie AD, Herbinger C, Fullsack P, Rico C (2019) First reconstruction of kinship in a scalloped hammerhead shark aggregation reveals the mating patterns and breeding sex ratio. Frontiers in Marine Science 6, 676.
| Crossref | Google Scholar |

Martin AP, Naylor GJP, Palumbi SR (1992) Rates of mitochondrial DNA evolution in sharks are slow compared with mammals. Nature 357(6374), 153-155.
| Crossref | Google Scholar | PubMed |

Momigliano P, Harcourt R, Robbins WD, Jaiteh V, Mahardika GN, Sembiring A, Stow A (2017) Genetic structure and signatures of selection in grey reef sharks (Carcharhinus amblyrhynchos). Heredity 119(3), 142-153.
| Crossref | Google Scholar | PubMed |

Naylor GJP, Caira JN, Jensen K, Rosana KAM, White WT, Last PR (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 2012(367), 1-262.
| Crossref | Google Scholar |

Osgood GJ, White ER, Baum JK (2021) Effects of climate-change-driven gradual and acute temperature changes on shark and ray species. Journal of Animal Ecology 90(11), 2547-2559.
| Crossref | Google Scholar | PubMed |

Ovenden JR, Dudgeon C, Feutry P, Feldheim K, Maes GE (2018) Genetics and genomics for fundamental and applied research on elasmobranchs. In Shark research: Emerging technologies and applications for the field and laboratory’. (Eds JC Carrier, MR Heithaus, CA Simpfendorfer) pp. 235–254. (CRC Press)

Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F, Jr. (1998) Fishing down marine food webs. Science 279(5352), 860-863.
| Crossref | Google Scholar | PubMed |

Pazmiño DA, Maes GE, Simpfendorfer CA, Salinas-de-León P, van Herwerden L (2017) Genome-wide SNPs reveal low effective population size within confined management units of the highly vagile Galapagos shark (Carcharhinus galapagensis). Conservation Genetics 18, 1151-1163.
| Crossref | Google Scholar |

Pierce SJ, Bennett MB (2009) Validated annual band-pair periodicity and growth parameters of blue-spotted maskray Neotrygon kuhlii from south-east Queensland, Australia. Journal of Fish Biology 75(10), 2490-2508.
| Crossref | Google Scholar | PubMed |

Pierce SJ, Kyne PM (2015) Neotrygon leylandi. The IUCN Red List of Threatened Species 2015: e.T60156A68636690. Available at https://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T60156A68636690.en [accessed 30 August 2024]

Pierce SJ, Pardo SA, Bennett MB (2009) Reproduction of the blue-spotted maskray Neotrygon kuhlii (Myliobatoidei: Dasyatidae) in south-east Queensland, Australia. Journal of Fish Biology 74(6), 1291-1308.
| Crossref | Google Scholar | PubMed |

Pierce SJ, White WT, Jacobsen IP, Barratt PJ, Last PR, Kyne PM (2015) Neotrygon picta. The IUCN Red List of Threatened Species 2015: e.T195464A68636975. Available at https://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T195464A68636975.en. [accessed 31 August 2024]

Plank SM, Lowe CG, Feldheim KA, Wilson RR, Jr, Brusslan JA (2010) Population genetic structure of the round stingray Urobatis halleri (Elasmobranchii: Rajiformes) in southern California and the Gulf of California. Journal of Fish Biology 77(2), 329-340.
| Crossref | Google Scholar | PubMed |

Postaire BD, Devloo-Delva F, Brunnschweiler JM, Charvet P, Chen X, Cliff G, Daly R, Drymon JM, Espinoza M, Fernando D, Glaus K, Grant MI, Hernandez S, Hyodo S, Jabado RW, Jaquemet S, Johnson G, Naylor GJP, Nevill JEG, Pathirana BM, Pillans RD, Smoothey AF, Tachihara K, Tillet BJ, Valerio-Vargas JA, Lesturgie P, Magalon H, Feutry P, Mona S (2024) Global genetic diversity and historical demography of the Bull Shark. Journal of Biogeography 51, 632-648.
| Crossref | Google Scholar |

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2), 945-959.
| Crossref | Google Scholar | PubMed |

Puckridge M, Last PR, White WT, Andreakis N (2013) Phylogeography of the Indo-West Pacific maskrays (Dasyatidae, Neotrygon): a complex example of chondrichthyan radiation in the Cenozoic. Ecology and Evolution 3(2), 217-232.
| Crossref | Google Scholar | PubMed |

Puechmaille SJ (2016) The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Molecular Ecology Resources 16(3), 608-627.
| Crossref | Google Scholar | PubMed |

Ratnasingham S, Hebert PDN (2007) BOLD: the barcode of life data system (http://www.barcodinglife.org). Molecular Ecology Notes 7(3), 355-364.
| Crossref | Google Scholar | PubMed |

Reynolds J, Weir BS, Cockerham CC (1983) Estimation of the coancestry coefficient: basis for a short-term genetic distance. Genetics 105(3), 767-779.
| Crossref | Google Scholar | PubMed |

Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4(1), 137-138.
| Crossref | Google Scholar |

Rus Hoelzel A, Shivji MS, Magnussen J, Francis MP (2006) Low worldwide genetic diversity in the basking shark (Cetorhinus maximus). Biology Letters 2(4), 639-642.
| Crossref | Google Scholar |

Schluessel V, Broderick D, Collin SP, Ovenden JR (2010) Evidence for extensive population structure in the white-spotted eagle ray within the Indo-Pacific inferred from mitochondrial gene sequences. Journal of Zoology 281(1), 46-55.
| Crossref | Google Scholar |

Sherman CS, Bin Ali A, Bineesh KK, Derrick D, Dharmadi, Fahmi, Fernando D, Haque AB, Maung A, Seyha L, Tanay D, Utzurrum JAT, Vo VQ, Yuneni RR (2021a) Neotrygon caeruleopunctata. The IUCN Red List of Threatened Species 2021: e.T104166988A175220257. Available at https://dx.doi.org/10.2305/IUCN.UK.2021-2.RLTS.T104166988A175220257.en [accessed 30 August 2024]

Sherman CS, Rigby CL, Derrick D (2021b) Neotrygon trigonoides. The IUCN Red List of Threatened Species 2021: e.T104167060A104167071. Available at https://dx.doi.org/10.2305/IUCN.UK.2021-2.RLTS.T104167060A104167071.en [accessed 31 August 2024]

Sherman CS, Rigby CL, Derrick D (2021c) Neotrygon australiae. The IUCN Red List of Threatened Species 2021: e.T104166970A104166982. Available at https://dx.doi.org/10.2305/IUCN.UK.2021-2.RLTS.T104166970A104166982.en. [accessed 30 August 2024]

Sherman CS, Bin Ali A, Bineesh KK, Derrick D, Dharmadi, Fahmi, Fernando D, Haque AB, Maung A, Seyha L, Tanay D, Utzurrum JAT, Vo VQ, Yuneni RR (2022a) Neotrygon orientalis (amended version of 2021 assessment). The IUCN Red List of Threatened Species 2022: e.T104167028A212575008. Available at https://dx.doi.org/10.2305/IUCN.UK.2022-1.RLTS.T104167028A212575008.en. [accessed 30 August 2024]

Sherman CS, Bin Ali A, Bineesh KK, Derrick D, Dharmadi, Fahmi, Fernando D, Haque AB, Maung A, Seyha L, Tanay D, Utzurrum JAT, Vo VQ, Yuneni RR (2022b) Neotrygon varidens (amended version of 2021 assessment). The IUCN Red List of Threatened Species 2022: e.T104167083A212575659. Available at https://dx.doi.org/10.2305/IUCN.UK.2022-1.RLTS.T104167083A212575659.en. [accessed 31 August 2024]

Tukana M, Prince J, Glaus KBJ, Marama K, Whippy-Morris C (2023) A baseline study of Fiji’s small-scale lobster fishery using value chain analysis and size at maturity thresholds. Marine Policy 149, 105513.
| Crossref | Google Scholar |

Venables WN, Smith DM, Team RDC (2009) ‘An introduction to R.’ (Network Theory Limited Bristol)

Waples RS, Punt AE, Cope JM (2008) Integrating genetic data into management of marine resources: how can we do it better? Fish and Fisheries 9(4), 423-449.
| Crossref | Google Scholar |

Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philosophical Transactions of the Royal Society B: Biological Sciences 360(1462), 1847-1857.
| Crossref | Google Scholar |

Ward RD, Holmes BH, White WT, Last PR (2008) DNA barcoding Australasian chondrichthyans: results and potential uses in conservation. Marine and Freshwater Research 59(1), 57-71.
| Crossref | Google Scholar |

West RM (2021) Best practice in statistics: use the Welch t-test when testing the difference between two groups. Annals of Clinical Biochemistry: International Journal of Laboratory Medicine 58(4), 267-269.
| Crossref | Google Scholar | PubMed |

White WT, O’Neill HL, Naylor GJ (2022) Taxonomy and diversity of extant elasmobranchs. In ‘Biology of sharks and their relatives.’ (Eds JC Carrier, CA Simpfendorfer, MR Heithaus, KE Yopak) pp. 31–57. (CRC Press)

Wickham H, Averick M, Bryan J, Chang W, McGowan LDA, François R, Grolemund G, Hayes A, Henry L, Hester J, Kuhn M, Pedersen TL, Miller E, Bache SM, Muller K, Ooms J, Robinson D, Seidel DP, Spinu V, Takahashi K, Vaughan D, Wilke C, Woo K, Yutani H (2019) Welcome to the Tidyverse. Journal of Open Source Software 4(43), 1686.
| Crossref | Google Scholar |