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From where I belong: using mitochondrial DNA analysis to investigate the origin of a white shark (Carcharodon carcharias) captured in Indonesian waters

Published online by Cambridge University Press:  20 September 2024

C. P. O'Connell Open the ORCID record for C. P. O'Connell [Opens in a new window] ,
A. P. Prasetyo ,
M. Stewart  and
Fahmi
C. P. O'Connell*
Affiliation:
O'Seas Conservation Foundation, Inc., Yonkers, NY, 10701, USA School for Marine Science and Technology, University of Massachusetts Dartmouth, New Bedford, MA 02740, USA
A. P. Prasetyo
Affiliation:
Research Center for Conservation of Marine and Inland Water Resources, National Research and Innovation Agency, Cibinong 16911, Bogor, Indonesia
M. Stewart
Affiliation:
Project Hiu, Brisbane, QLD 4001, Australia
Fahmi
Affiliation:
Research Center for Oceanography, National Research and Innovation Agency, Pademangan 14430, Jakarta, Indonesia
*
Corresponding author: C. P. O'Connell; Email: oseasfdn@gmail.com
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Abstract

In 2013 and 2019, two separate encounters with a white shark (Carcharodon carcharias) were documented within Indonesian waters. Of particular importance was ca. 6.0 m male C. carcharias that was captured in Lombok, Indonesia in 2013, where an upper lateral tooth was retained. Using the D-loop sequences of the mitochondrial DNA (mtDNA) associated with this captured white shark, the mtDNA was compared to the available mtDNA sequences in GenBank® associated with the Northwest Pacific and Australian (i.e. Southern-Western and Eastern) C. carcharias subpopulations to determine its point of origin. Results from the mtDNA analyses suggest that the point of origin for this captured C. carcharias is from one of the Australian subpopulations. When compared to primary literature, this migration presents a northerly range extension for this species; however, since it is unclear what Australian subpopulation this shark was from it is uncertain what subpopulation this range extension applies to. Although C. carcharias presence within Indonesian waters is likely a rare occurrence, being that Indonesia represents the largest shark fin exporter in the world, the utilization of these waters and potential unsustainable exploitation poses a definitive threat to this highly migratory top predator. Therefore, further research investigating the purpose and site fidelity of C. carcharias within these waters is critical to future multijurisdictional protection of this top predator.

Keywords

Carcharodon carchariasD-loop sequencesIndonesiamtDNAwhite shark
Type
Marine Record
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 104 , 2024 , e75
Copyright
Copyright © The Author(s), 2024. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

Introduction

Top predators, such as some shark species, play a critical role and have been demonstrated to help maintain the balance within their respective food webs (Burkholder et al., Reference Burkholder, Heithaus, Fourqurean, Wirsing and Dill2013; Hussey et al., Reference Hussey, MacNeil, Siple, Popp, Dudley and Fisk2015). In some locations or even on a global scale, the retention of certain shark species is prohibited (e.g. Convention on International Trade in Endangered Species of Wild Fauna and Flora; Tolotti et al., Reference Tolotti, Filmalter, Bach, Travassos, Seret and Dagorn2015); however, in other locations, the increased demand and exploitation rates, both legal and illegal, raise concern about the health of certain shark populations (Shivji et al., Reference Shivji, Chapman, Pikitch and Raymond2005). Understanding the population structure, range, and abundance of a particular shark population can provide fisheries managers with essential information regarding the sustainable or unsustainable exploitation of that particular population (e.g. Chapman et al., Reference Chapman, Feldheim, Papastamatiou and Hueter2015; Pérez-Jiménez and Mendez-Loeza, Reference Pérez-Jiménez and Mendez-Loeza2015) and consequently can provide regulations to help restore the population to pre-existing levels (Hoffmann et al., Reference Hoffmann, Hilton-Taylor, Angulo, Böhm, Brooks, Butchart, Carpenter, Chanson, Collen, Cox, Darwall, Dulvy, Harrison, Katariya, Pollock, Quader, Richman, Rodrigues, Tognelli, Vié, Aguiar, Allen, Allen, Amori, Ananjeva, Andreone, Andrew, Ortiz, Baillie, Baldi, Bell, Biju, Bird, Black-Decima, Blanc, Bolaños, Bolivar-G, Burfield, Burton, Capper, Castro, Catullo, Cavanagh, Channing, Chao, Chenery, Chiozza, Clausnitzer, Collar, Collett, Collette, Fernandez, Craig, Crosby, Cumberlidge, Cuttelod, Derocher, Diesmos, Donaldson, Duckworth, Dutson, Dutta, Emslie, Farjon, Fowler, Freyhof, Garshelis, Gerlach, Gower, Grant, Hammerson, Harris, Heaney, Hedges, Hero, Hughes, Hussain, Icochea M, Inger, Ishii, Iskandar, Jenkins, Kaneko, Kottelat, Kovacs, Kuzmin, La Marca, Lamoreux, Lau, Lavilla, Leus, Lewison, Lichtenstein, Livingstone, Lukoschek, Mallon, McGowan, McIvor, Moehlman, Molur, Alonso, Musick, Nowell, Nussbaum, Olech, Orlov, Papenfuss, Parra-Olea, Perrin, Polidoro, Pourkazemi, Racey, Ragle, Ram, Rathbun, Reynolds, Rhodin, Richards, Rodríguez, Ron, Rondinini, Rylands, Sadovy de Mitcheson, Sanciangco, Sanders, Santos-Barrera, Schipper, Self-Sullivan, Shi, Shoemaker, Short, Sillero-Zubiri, Silvano, Smith, Smith, Snoeks, Stattersfield, Symes, Taber, Talukdar, Temple, Timmins, Tobias, Tsytsulina, Tweddle, Ubeda, Valenti, Paul van Dijk, Veiga, Veloso, Wege, Wilkinson, Williamson, Xie, Young, Akçakaya, Bennun, Blackburn, Boitani, Dublin, da Fonseca, Gascon, Lacher, Mace, Mainka, McNeely, Mittermeier, Reid, Rodriguez, Rosenberg, Samways, Smart, Stein and Stuart2010).

In the instance of white sharks (Carcharodon carcharias), there are nine known C. carcharias subpopulations: Southern-Western Australia (Bruce, Reference Bruce2016; McAuley et al., Reference McAuley, Bruce, Keay, Mountford, Pinnell and Whoriskey2017), Western North Atlantic (WNA, Skomal et al., Reference Skomal, Braun, Chisholm and Thorrold2017), Northeastern Pacific (NEP, Domeier and Nasby-Lucas, Reference Domeier and Nasby-Lucas2013), Eastern Australian and New Zealand (Bruce et al., Reference Bruce, Harasti, Lee, Gallen and Bradford2019), Mediterranean (Leone et al., Reference Leone, Puncher, Ferretti, Sperone, Tripepi, Micarelli and Tinti2020), South African (Kock et al., Reference Kock, O'Riain, Mauff, Meÿer, Kotze and Griffiths2013), Northwest Pacific (Tanaka et al., Reference Tanaka, Kitamura, Mochizuki and Kofuji2011), South American Atlantic (Cione and Barla, Reference Cione and Barla2008), and South American Pacific (Bustamante et al., Reference Bustamante, Vargas-Caro and Bennett2014; Figure 1). Due to its low rebound potential and current estimated population status, C. carcharias is listed as vulnerable on a global scale (Rigby et al., Reference Rigby, Barreto, Carlson, Fernando, Fordham, Francis, Jabado, Liu, Marshall, Pacoureau, Romanov, Sherley and Winker2019) according to the International Union for the Conservation of Nature Red List. The white shark is particularly vulnerable to exploitation since this species is characterized by having low fecundity, producing an average of 2–14 pups per litter (Francis, Reference Francis, Klimley and Ainley1996; Uchida et al., Reference Uchida, Toda, Teshima, Yano, Klimley and Ainley1996), slow growth (Wintner and Cliff, Reference Wintner and Cliff1999; Natanson and Skomal, Reference Natanson and Skomal2015), and late sexual maturity (Natanson and Skomal, Reference Natanson and Skomal2015), which is estimated to be >3.80 m total length (TL) for males and >4.50 m TL for females (Francis, Reference Francis, Klimley and Ainley1996; Pratt, Reference Pratt, Klimley and Ainley1996; Wintner and Cliff, Reference Wintner and Cliff1999). However, despite international protection of C. carcharias, this species exhibits transoceanic movements, making it susceptible to a variety of anthropogenic sources of mortality (e.g. Bonfil et al., Reference Bonfil, Meÿer, Scholl, Johnson, O'Brien, Oosthuizen, Swanson, Kotze and Paterson2005). While extensive tagging efforts have provided a baseline understanding of the movements of most C. carcharias populations (e.g. Skomal et al., Reference Skomal, Braun, Chisholm and Thorrold2017; Bruce et al., Reference Bruce, Harasti, Lee, Gallen and Bradford2019), there remains uncertainty as to the structure, size, and range of most subpopulations, particularly in the Northwest Pacific population (Christiansen et al., Reference Christiansen, Lin, Tanaka, Velikanov, Mollet, Wintner, Fordham, Fisk and Hussey2014).

Figure 1. (A) Map illustrating the relative locations of white shark (C. carcharias) populations (modified from Huveneers et al., Reference Huveneers, Apps, Becerril-García, Bruce, Butcher, Carlisle, Chapple, Christiansen, Cliff, Curtis and Daly-Engel2018). The populations are: Northeastern Pacific (NEP), Western North Atlantic (WNA), Mediterranean (MED), South African (SA), Northwest Pacific (NWP), Southern-Western Australian (SWA), Eastern Australian and New Zealand (EA), South American Pacific (SAP), and South American Atlantic (SAA). The rectangular region highlights the location of Indonesia. (B) Map representing Indonesia (area in black), as well as the white shark (C. carcharias) sightings within the region: (A) Nusa Penida in Bali, Indonesia (8°44′S; 115°32′E; 5.0 m female) and (B) Lombok, Indonesia (08°51′S; 118°18′E; 6.0 m male).

In recent years, sparse sightings of C. carcharias have occurred within Indonesian waters (Fahmi and Dharmadi, Reference Fahmi and Dharmadi2014; Coleman, personal communication, 2019). More specifically, in 2019 within Nusa Penida in Bali, Indonesia (8°44′S; 115°32′E; Figure 1A), scuba divers encountered an approximately 5.0 m TL female C. carcharias (Figure 2A). In 2013, a ca. 6.0 m TL male C. carcharias (Figure 2B) was captured by demersal longline fishermen off Dompu in West Nusa Tenggara, Indonesia (08°51′S; 118°18′E; Figure 1B). Although multiple C. carcharias subpopulations have been identified in the waters surrounding Indonesia, including the Northwest Pacific, the Southern-Western Australian, and Eastern Australian and New Zealand, there exists no record of any tagged sharks associated with these stocks travelling into these tropical waters. Therefore, using a sample collected from the upper lateral tooth of the C. carcharias captured in the Lesser Sunda region and comparing it to the publicly available mitochondrial DNA (mtDNA) database (GenBank®; Bethesda, MD, USA), the present study aimed to determine which subpopulation this C. carcharias may be most closely related to, thus suggesting site of origin.

Figure 2. Recent and documented white shark (C. carcharias) sightings within Indonesian waters. (A) An estimated 5.0 m TL female C. carcharias sighted by divers at Nusa Penida in Bali, Indonesia in 2019 © Two Fish Divers. (B) A 6.0 m TL male C. carcharias captured by fishermen in eastern Lombok, Indonesia in 2013 © Fahmi and Dharmadi (Reference Fahmi and Dharmadi2014). (C) Upper lateral tooth collected from the white shark C. carcharias landed in eastern Lombok, Indonesia in 2013. © Fahmi and Dharmadi (Reference Fahmi and Dharmadi2014).

Methods

In 2013, a C. carcharias was captured by demersal longline fishermen and brought to a fishing market where scientists were able to collect both photographic evidence and one upper lateral tooth (Fahmi and Dharmadi, Reference Fahmi and Dharmadi2014; Figure 2C). At the Centre Laboratory of Sequencing, National Research and Innovation Agency in West Java, Indonesia from February to April 2023, DNA was extracted from the 10-year-old upper lateral tooth using a DNeasy Tissue Kit (Qiagen™) and the addition of ethylenediaminetetraacetic acid to the incubation stage (modified from Swig and Collier, Reference Swig and Collier2021). A polymerase chain reaction (PCR) was used to amplify about 500 bp of the mtDNA D-loop region. The two primers for the D-loop region were: GWDL-L (TTG ACG CGA TCA AGG ACG AA) and GWDL-H (CAA ACA TCC ATT TGG CCT TC) (Pardini et al., Reference Pardini, Jones, Scholl and Noble2000). A total volume of 24 μl included 12.5 μl MyTaq™ HS Red Mix PCR kit, 1 μl of the 5 μM pre-mixed forward and reverse primers (IDT™), 3 μl of a standardized amount (10–15 ng μl−1) of DNA, and 7.5 μl of sterile water. The PCR profile included a 1 min initial denaturing step at 95°C, 40 cycles at 95°C for 15 s, 55°C for 30 s, 72°C for 1 min, and a 5 min final extension step at 72°C (Tanaka et al., Reference Tanaka, Kitamura, Mochizuki and Kofuji2011). The negative control (Borneo river shark [Glyphis fowlerae]) was used to validate the GWS primer. To confirm species, two additional primers were run (i.e. Elas02; Taberlet et al., Reference Taberlet, Coissac, Hajibabaei and Rieseberg2012 and Leray-XT; Wangensteen et al., Reference Wangensteen, Palacín, Guardiola and Turon2018) by following the PCR mix and PCR profile (Prasetyo et al., Reference Prasetyo, Murray, Agung, Sales, McDevitt and Mariani2023). After PCR, each replicate was visually examined on a 1.2% agarose gel and stained with GelRed® Nucleic Acid Gel Stain. Each well received 2 μl of the sample and a 100 bp ladder from Invitrogen™ was included in the gel for reference.

PCR products are then purified using a QIAquick PCR Purification Kit (Qiagen). The purification products were then Sanger sequenced using the Genetic Analyzer 3500 (ABI™) at the Sequencing Centre, Genomic Laboratory, National Research and Innovation Agency, Bogor, Indonesia. All positions containing gaps and missing data were eliminated from the dataset (‘Complete deletion’ option). After trimming and quality control have been conducted, the sequences (GenBank accession no. PP078820) were then aligned using software UGENE (Okonechnikov et al., Reference Okonechnikov, Golosova, Fursov and Team2012) and compared with the National Center for Biotechnology Information (NCBI) sequences for the Japanese (GenBank accession nos. AB598394–AB598397) (Tanaka et al., Reference Tanaka, Kitamura, Mochizuki and Kofuji2011) and Australian–New Zealand (GenBank accession nos. KY067571–KY067590) subpopulations. To further examine the phylogenetic tree, maximum-likelihood was constructed using the neighbour-joining method with the Kimura-2 model for 1000 bootstrap replications in MEGA-X with default parameters. To improve the clarity of the phylogenetic tree, FigTree v1.4.4 and Inkscape were used.

Results

The modified DNA extraction protocol successfully resulted in the DNA extraction from the 10-year-old upper lateral tooth. However, the DNA concentration was very low by 7.75 ng μl−1. Despite the low DNA concentration, the three primer sets successfully amplified the targeted sequence. A short-targeted sequence was chosen to anticipate fragmented DNA extracted from the tooth (GenBank accession no. PP078820; Figure 3).

Figure 3. Gel electrophoresis image of the amplified sequence associated with the 6.0 m TL white shark (C. carcharias) captured in 2013 by demersal longline fishermen off of eastern Lombok, Indonesia. The 100 bp DNA Ladder by Geneaid™ was used (lane 1). Experiments were conducted using three distinct primer sets: Leray-XT (Wangensteen et al., Reference Wangensteen, Palacín, Guardiola and Turon2018), Elas02 (Taberlet et al., Reference Taberlet, Coissac, Hajibabaei and Rieseberg2012), and GWS (Pardini et al., Reference Pardini, Jones, Scholl and Noble2000). Each primer set was designed to target specific regions, namely cytochrome c oxidase I region (COI; lane 2), 12S ribosomal RNA region (12S; lane 3), and D-loop region (D-loop; lane 4), respectively. The Leray-XT and 12S primers amplified sequences were used to confirm the identification of species, whereas the GWS primer sequences were utilized for further investigation. The negative control (Borneo river shark [G. fowlerae]) was used to validate GWS primer (lane 5).

Sanger sequencing confirmed that the tooth was from a C. carcharias based on three different primers (Table 1). Moreover, the neighbour-joining tree associated with the mtDNA in the D-loop region (about 400–500 bp) revealed that the shark has a closer or nested clade with the Australian subpopulations rather than the Japanese subpopulation (Figure 4) with a bootstrap value at 93%. Although these results suggest the site of origin for this individual C. carcharias is from the Australian subpopulations, the available GenBank database does not differentiate between the two subpopulations (i.e. Southern-Western and Eastern Australian and New Zealand). Therefore, determining the specific Australian subpopulation that this C. carcharias was most closely associated with was not possible.

Table 1. BLAST result using the NCBI for the 6.0 m TL male white shark (C. carcharias) captured in eastern Lombok, Indonesia

Figure 4. Genetic relationship of 29 white sharks (C. carcharias) from the Northwest Pacific (Japan) and Australia–New Zealand subpopulations in comparison to the Indonesian specimen using the D-loop region inferred using the neighbour-joining method with the Kimura-2 model for 1000 bootstrap replications. There was a total of 412 positions in the final dataset. Bootstrap support values are shown near internal nodes.

Discussion

Understanding the migratory habits of marine top predators is important as it provides critical information about stock structure and potential threats that may negatively impact population health and abundance. Using the present mtDNA analysis of the D-loop region, this study is the first to demonstrate at least one site of origin (e.g. from Australia) for C. carcharias that enter Indonesian waters. While it is currently uncertain as to whether this shark came from the Southern-Western Australian (e.g. Bradford et al., Reference Bradford, Patterson, Rogers, McAuley, Mountford, Huveneers, Robbins, Fox and Bruce2020) or Eastern Australian and New Zealand (e.g. Spaet et al., Reference Spaet, Butcher, Manica and Lam2022) C. carcharias subpopulation, this study provides an initial step to further understanding the true range of this highly migratory top predator. Presently the range associated with both Australian subpopulations has not been demonstrated to extend into Indonesian waters (e.g. Spaet et al., Reference Spaet, Patterson, Bradford and Butcher2020); however, the Eastern Australian and New Zealand subpopulation has been documented as far north as Papua New Guinea (PNG; Spaet et al., Reference Spaet, Patterson, Bradford and Butcher2020). Therefore, the present study suggests a range extension for Australia-associated C. carcharias. Although it is likely that the documented C. carcharias encounters from the present study are associated with the Eastern Australian and New Zealand subpopulation due to the proximity of Indonesia to PNG, due to the lack of tangible satellite telemetry or genetic data it is uncertain which subpopulation this range extension pertains to.

Furthermore, while little is known about the migratory patterns of the Northwest Pacific C. carcharias stock (Christiansen et al., Reference Christiansen, Lin, Tanaka, Velikanov, Mollet, Wintner, Fordham, Fisk and Hussey2014), DNA analyses suggest that this is a reproductively isolated stock (Tanaka et al., Reference Tanaka, Kitamura, Mochizuki and Kofuji2011). More specifically, Tanaka et al. (Reference Tanaka, Kitamura, Mochizuki and Kofuji2011) demonstrated through the use of mtDNA analyses that the Northwest Pacific C. carcharias form a monophyletic clade and exhibit unique life-history characteristics in comparison to other C. carcharias stocks. Therefore, although likely a rare occurrence, C. carcharias that utilize Indonesian waters are likely only from one or both of the Australia-associated stock (i.e. Southern-Western Australian and Eastern Australian and New Zealand) or if they are from the Northwest Pacific, they are not utilizing this region for mating purposes as this would be evidenced through previous DNA analyses (e.g. Tanaka et al., Reference Tanaka, Kitamura, Mochizuki and Kofuji2011).

Although it is uncertain if all C. carcharias that utilize Indonesian waters are from the Australian subpopulations (e.g. Southern-Western Australian and Eastern Australian and New Zealand) or from the Northwest Pacific subpopulation, it is further uncertain as to why, how frequently, and for what duration they are utilizing these tropical waters. It is not uncommon for C. carcharias to utilize tropical waters as they have a global distribution in temperate, subtropical, and tropical seas (Bonfil et al., Reference Bonfil, Meÿer, Scholl, Johnson, O'Brien, Oosthuizen, Swanson, Kotze and Paterson2005, Reference Bonfil, Francis, Duffy, Manning and O'Brien2010; Duffy et al., Reference Duffy, Francis, Manning, Bonfil and Domeier2012; Skomal et al., Reference Skomal, Braun, Chisholm and Thorrold2017). However, research illustrates that C. carcharias movement patterns have been suggested to be correlated with a variety of both biotic and abiotic variables, including reproductive behaviour (e.g. mating or parturition; Domeier, Reference Domeier and Domeier2012), water temperature (e.g. Skubel et al., Reference Skubel, Kirtman, Fallows and Hammerschlag2018), and prey (Nasby-Lucas et al., Reference Nasby-Lucas, Dewar, Lam, Goldman and Domeier2009). While all three are plausible explanations for their presence within Indonesian waters, insufficient data make it difficult to make any sound conclusions.

Indonesia is considered one of the world's largest shark fin exporters in the world (Okes and Sant, Reference Okes and Sant2019; FAO, Reference FAO2022) with serious challenges on managing fisheries and its trade (Prasetyo et al., Reference Prasetyo, McDevitt, Murray, Barry, Agung, Muttaqin and Mariani2021). While C. carcharias may not be commonly utilizing these waters, the potential anthropogenic threats are a cause for concern. Therefore, future research should aim at distinguishing what subpopulation(s) these Indonesian C. carcharias originated from, with a focus on satellite tagging efforts that may shed light on the potential ecological importance of Indonesia's waters to this top predator.

Acknowledgements

We acknowledge the facilities, scientific, and technical support from the Sequencing Centre, Genomic Laboratory at the National Research and Innovation Agency (BRIN).

Author contributions

C. P. O., A. P. P., M. S., and Fahmi all formulated the research question and assisted with writing the manuscript. Fahmi provided the white shark sample. C. P. O., A. P. P., and Fahmi helped design the study, whereas A. P. P. carried out the study, analysed the data, and interpreted the findings.

Financial support

This work was partially supported by O'Seas Conservation Foundation, Inc.; Discovery Channel, Inc. and Talesmith TV; and Mrs. Uli Pandjaitan.

Competing interests

None.

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

Bonfil, R, Francis, MP, Duffy, C, Manning, MJ and O'Brien, S (2010) Large-scale tropical movements and diving behavior of white sharks Carcharodon carcharias tagged off New Zealand. Aquatic Biology 8, 115–123.Google Scholar
Bonfil, R, Meÿer, M, Scholl, MC, Johnson, R, O'Brien, S, Oosthuizen, H, Swanson, S, Kotze, D and Paterson, M (2005) Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science (New York, N.Y.) 310, 100–103.Google Scholar
Bradford, R, Patterson, TA, Rogers, PJ, McAuley, R, Mountford, S, Huveneers, C, Robbins, R, Fox, A and Bruce, BD (2020) Evidence of diverse movement strategies and habitat use by white sharks, Carcharodon carcharias, off southern Australia. Marine Biology 167, 1–12.Google Scholar
Bruce, BD (2016) Determining the size and trend of the West Coast white shark population. Marine Biodiversity Hub, National Environmental Science Program report. Hobart: CSIRO. https://www.nespmarine.edu.au/document/determining-size-and-trend-west-coast-white-shark-populationGoogle Scholar
Bruce, BD, Harasti, D, Lee, K, Gallen, C and Bradford, R (2019) Broad-scale movements of juvenile white sharks Carcharodon carcharias in eastern Australia from acoustic and satellite telemetry. Marine Ecology Progress Series 619, 1–15.Google Scholar
Burkholder, DA, Heithaus, MR, Fourqurean, JW, Wirsing, A and Dill, LM (2013) Patterns of top-down control in a seagrass ecosystem: could a roving apex predator induce a behaviour-mediated trophic cascade? Journal of Animal Ecology 82, 1192–1202.Google Scholar
Bustamante, C, Vargas-Caro, C and Bennett, MB (2014) Not all fish are equal: functional biodiversity of cartilaginous fishes (Elasmobranchii and Holocephali) in Chile. Journal of Fish Biology 85, 1617–1633.Google Scholar
Chapman, DD, Feldheim, KA, Papastamatiou, YP and 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.Google Scholar
Christiansen, HM, Lin, V, Tanaka, S, Velikanov, A, Mollet, HF, Wintner, SP, Fordham, SV, Fisk, AT and Hussey, NE (2014) The last frontier: catch records of white sharks (Carcharodon carcharias) in the Northwest Pacific Ocean. PLoS ONE 9, e94407.Google Scholar
Cione, AL and Barla, MJ (2008) Causes and contrasts in current and past distribution of the white shark (Lamniformes: Carcharodon carcharias) off southeastern South America. Revista del Museo Argentino de Ciencias Naturales 10, 175–184.Google Scholar
Domeier, ML (2012) A new life-history hypothesis for white sharks, Carcharodon carcharias, in the Northeastern Pacific. In Domeier, ML (ed.), Global Perspectives on the Biology and Life History of the White Shark. Boca Raton, FL: CRC Press, pp. 199–224.Google Scholar
Domeier, ML and Nasby-Lucas, N (2013) Two-year migration of adult female white sharks (Carcharodon carcharias) reveals widely separated nursery areas and conservation concerns. Animal Biotelemetry 1, 1–9. https://doi.org/10.1186/2050-3385-1-2Google Scholar
Duffy, CAJ, Francis, MP, Manning, MJ and Bonfil, R (2012) Regional population connectivity, oceanic habitat, and return migration revealed by satellite tagging of white sharks, Carcharodon carcharias, at New Zealand aggregation sites. In Domeier, ML (ed.), Global Perspectives on the Biology and Life History of the White Shark. Boca Raton: CRC Press, pp. 301–318.Google Scholar
Fahmi, and Dharmadi, (2014) First confirmed record of the white shark Carcharodon carcharias (Lamniformes: Lamnidae) from Indonesia. Marine Biodiversity Records 7, e53.Google Scholar
FAO, (2022) Fishery and aquaculture statistics. Global capture production 1950–2020 (FishStatJ). In FAO Fisheries and Aquaculture Division [online]. Updated 2022. Rome, Italy: FAO UN. www.fao.org/fishery/statistics/software/fishstatj/en.Google Scholar
Francis, MP (1996) Observations on a pregnant white shark with a review in reproduction biology. In Klimley, AP, Ainley, DG (ed.), Great White Sharks: The Biology of Carcharodon carcharias. San Diego, CA: Academic Press, pp. 157–172.Google Scholar
Hoffmann, M, Hilton-Taylor, C, Angulo, A, Böhm, M, Brooks, TM, Butchart, SHM, Carpenter, KE, Chanson, J, Collen, B, Cox, NA, Darwall, WRT, Dulvy, NK, Harrison, LR, Katariya, V, Pollock, CM, Quader, S, Richman, NI, Rodrigues, ASL, Tognelli, MF, Vié, J-C, Aguiar, JM, Allen, DJ, Allen, GR, Amori, G, Ananjeva, NB, Andreone, F, Andrew, P, Ortiz, ALA, Baillie, JEM, Baldi, R, Bell, BD, Biju, SD, Bird, JP, Black-Decima, P, Blanc, JJ, Bolaños, F, Bolivar-G, W, Burfield, IJ, Burton, JA, Capper, DR, Castro, F, Catullo, G, Cavanagh, RD, Channing, A, Chao, NL, Chenery, AM, Chiozza, F, Clausnitzer, V, Collar, NJ, Collett, LC, Collette, BB, Fernandez, CFC, Craig, MT, Crosby, MJ, Cumberlidge, N, Cuttelod, A, Derocher, AE, Diesmos, AC, Donaldson, JS, Duckworth, JW, Dutson, G, Dutta, SK, Emslie, RH, Farjon, A, Fowler, S, Freyhof, J, Garshelis, DL, Gerlach, J, Gower, DJ, Grant, TD, Hammerson, GA, Harris, RB, Heaney, LR, Hedges, SB, Hero, J-M, Hughes, B, Hussain, SA, Icochea M, J, Inger, RF, Ishii, N, Iskandar, DT, Jenkins, RKB, Kaneko, Y, Kottelat, M, Kovacs, KM, Kuzmin, SL, La Marca, E, Lamoreux, JF, Lau, MWN, Lavilla, EO, Leus, K, Lewison, RL, Lichtenstein, G, Livingstone, SR, Lukoschek, V, Mallon, DP, McGowan, PJK, McIvor, A, Moehlman, PD, Molur, S, Alonso, AM, Musick, JA, Nowell, K, Nussbaum, RA, Olech, W, Orlov, NL, Papenfuss, TJ, Parra-Olea, G, Perrin, WF, Polidoro, BA, Pourkazemi, M, Racey, PA, Ragle, JS, Ram, M, Rathbun, G, Reynolds, RP, Rhodin, AGJ, Richards, SJ, Rodríguez, LO, Ron, SR, Rondinini, C, Rylands, AB, Sadovy de Mitcheson, Y, Sanciangco, JC, Sanders, KL, Santos-Barrera, G, Schipper, J, Self-Sullivan, C, Shi, Y, Shoemaker, A, Short, FT, Sillero-Zubiri, C, Silvano, DL, Smith, KG, Smith, AT, Snoeks, J, Stattersfield, AJ, Symes, AJ, Taber, AB, Talukdar, BK, Temple, HJ, Timmins, R, Tobias, JA, Tsytsulina, K, Tweddle, D, Ubeda, C, Valenti, SV, Paul van Dijk, P, Veiga, LM, Veloso, A, Wege, DC, Wilkinson, M, Williamson, EA, Xie, F, Young, BE, Akçakaya, HR, Bennun, L, Blackburn, TM, Boitani, L, Dublin, HT, da Fonseca, GAB, Gascon, C, Lacher, TE, Mace, GM, Mainka, SA, McNeely, JA, Mittermeier, RA, Reid, GM, Rodriguez, JP, Rosenberg, AA, Samways, MJ, Smart, J, Stein, BA and Stuart, SN (2010) The impact of conservation on the status of the world's vertebrates. Science 330, 1503–1509.Google Scholar
Hussey, NE, MacNeil, MA, Siple, MC, Popp, BN, Dudley, SF and Fisk, AT (2015) Expanded trophic complexity among large sharks. Food Webs 4, 1–7.Google Scholar
Huveneers, C, Apps, K, Becerril-García, EE, Bruce, B, Butcher, PA, Carlisle, AB, Chapple, TK, Christiansen, M, Cliff, G, Curtis, TH and Daly-Engel, TS (2018) Future research directions on the “elusive” white shark. Frontiers in Marine Science 17, 455.Google Scholar
Kock, A, O'Riain, MJ, Mauff, K, Meÿer, M, Kotze, D and Griffiths, C (2013) Residency, habitat use and sexual segregation of white sharks, Carcharodon carcharias in False Bay, South Africa. PLoS ONE 8, 55048.Google Scholar
Leone, A, Puncher, GN, Ferretti, F, Sperone, E, Tripepi, S, Micarelli, P and Tinti, F (2020) Pliocene colonization of the Mediterranean by great white shark inferred from fossil records, historical jaws, phylogeographic and divergence time analyses. Journal of Biogeography 47, 1119–1129.Google Scholar
McAuley, RB, Bruce, BD, Keay, IS, Mountford, S, Pinnell, T and Whoriskey, FG (2017) Broad-scale coastal movements of white sharks off Western Australia described by passive acoustic telemetry data. Marine and Freshwater Research 68, 1518–1531.Google Scholar
Nasby-Lucas, N, Dewar, H, Lam, CH, Goldman, KJ and Domeier, ML (2009) White shark offshore habitat: a behavioral and environmental characterization of the Eastern Pacific shared offshore foraging area. PLoS ONE 4, e8163.Google Scholar
Natanson, LJ and Skomal, GB (2015) Age and growth of the white shark, Carcharodon carcharias, in the Western North Atlantic Ocean. Marine and Freshwater Research 66, 387–398.Google Scholar
Okes, N and Sant, G (2019) An Overview of Major Shark and Ray Catchers, Traders, and Species. Cambridge, UK: TRAFFIC.Google Scholar
Okonechnikov, K, Golosova, O, Fursov, M and Team, TU (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics (Oxford, England) 28, 1166–1167.Google Scholar
Pardini, AT, Jones, CS, Scholl, MC and Noble, LR (2000) Isolation and characterization of dinucleotide microsatellite loci in the great white shark, Carcharodon carcharias. Molecular Ecology 9, 1176–1178.Google Scholar
Pérez-Jiménez, JC and Mendez-Loeza, I (2015) The small-scale shark fisheries in the southern Gulf of Mexico: understanding their heterogeneity to improve their management. Fisheries Research 172, 96–104.Google Scholar
Prasetyo, AP, McDevitt, AD, Murray, JM, Barry, J, Agung, F, Muttaqin, E and Mariani, S (2021) Shark and ray trade in and out of Indonesia: addressing knowledge gaps on the path to sustainability. Marine Policy 133, 104714.Google Scholar
Prasetyo, AP, Murray, J, Agung, F, Sales, N, McDevitt, A and Mariani, S (2023) Shark-dust: application of high-throughput DNA sequencing of processing residues for trade monitoring of threatened sharks and rays. Conservation Letters 16, e12971. https://doi.org/10.1111/conl.12971Google Scholar
Pratt, HL (1996) Reproduction in the male white shark. In Klimley, AP and Ainley, DG (eds), Great White Sharks: The Biology of Carcharodon carcharias. San Diego, CA: Academic Press, pp. 131–138.Google Scholar
Rigby, CL, Barreto, R, Carlson, J, Fernando, D, Fordham, S, Francis, MP, Jabado, RW, Liu, KM, Marshall, A, Pacoureau, N, Romanov, E, Sherley, RB and Winker, H (2019) White shark (Carcharodon carcharias). IUCN Red List of Threatened Species.Google Scholar
Shivji, MS, Chapman, DD, Pikitch, EK and Raymond, PW (2005) Genetic profiling reveals illegal international trade in fins of the great white shark, Carcharodon carcharias. Conservation Genetics 6, 1035–1039.Google Scholar
Skomal, GB, Braun, CD, Chisholm, JH and Thorrold, SR (2017) Movements of the white shark Carcharodon carcharias in the North Atlantic Ocean. Marine Ecology Progress Series 580, 1–16.Google Scholar
Skubel, RA, Kirtman, BP, Fallows, C and Hammerschlag, N (2018) Patterns of long-term climate variability and predation rates by a marine apex predator, the white shark Carcharodon carcharias. Marine Ecology Progress Series 587, 129–139.Google Scholar
Spaet, JL, Butcher, PA, Manica, A and Lam, CH (2022) Spatial dynamics and fine-scale vertical behaviour of immature eastern Australasian white sharks (Carcharodon carcharias). Biology 11, 1689.Google Scholar
Spaet, JL, Patterson, TA, Bradford, RW and Butcher, PA (2020) Spatiotemporal distribution patterns of immature Australasian white sharks (Carcharodon carcharias). Scientific Reports 10, 10169.Google Scholar
Swig, B and Collier, RS (2021) Novel method for the extraction of DNA from Lamniformes tooth and denticle enamel suitable for PCR. Dental Research and Oral Health 6, 25–27. 2021.01.18.427093.Google Scholar
Taberlet, P, Coissac, E, Hajibabaei, M and Rieseberg, LH (2012) Environmental DNA. Molecular Ecology 21, 1789–1793.Google Scholar
Tanaka, S, Kitamura, T, Mochizuki, T and Kofuji, K (2011) Age, growth and genetic status of the white shark (Carcharodon carcharias) from Kashima-nada, Japan. Marine and Freshwater Research 62, 548–556.Google Scholar
Tolotti, MT, Filmalter, JD, Bach, P, Travassos, P, Seret, B and Dagorn, L (2015) Banning is not enough: the complexities of oceanic shark management by tuna regional fisheries management organizations. Global Ecology and Conservation 4, 1–7.Google Scholar
Uchida, S, Toda, M, Teshima, K and Yano, K (1996) Pregnant white sharks and full-term embryos from Japan. In Klimley, AP, Ainley, DG (eds), Great White Sharks: The Biology of Carcharodon carcharias. San Diego, CA: Academic Press, pp. 139–155.Google Scholar
Wangensteen, OS, Palacín, C, Guardiola, M and Turon, X (2018) DNA metabarcoding of littoral hard-bottom communities: high diversity and database gaps revealed by two molecular markers. PeerJ 6, e4705.Google Scholar
Wintner, SP and Cliff, G (1999) Age and growth determination of the white shark, Carcharodon carcharias, from the east coast of South Africa. Fisheries Bulletin 97, 153–169.Google Scholar
Figure 0

Figure 1. (A) Map illustrating the relative locations of white shark (C. carcharias) populations (modified from Huveneers et al., 2018). The populations are: Northeastern Pacific (NEP), Western North Atlantic (WNA), Mediterranean (MED), South African (SA), Northwest Pacific (NWP), Southern-Western Australian (SWA), Eastern Australian and New Zealand (EA), South American Pacific (SAP), and South American Atlantic (SAA). The rectangular region highlights the location of Indonesia. (B) Map representing Indonesia (area in black), as well as the white shark (C. carcharias) sightings within the region: (A) Nusa Penida in Bali, Indonesia (8°44′S; 115°32′E; 5.0 m female) and (B) Lombok, Indonesia (08°51′S; 118°18′E; 6.0 m male).

Figure 1

Figure 2. Recent and documented white shark (C. carcharias) sightings within Indonesian waters. (A) An estimated 5.0 m TL female C. carcharias sighted by divers at Nusa Penida in Bali, Indonesia in 2019 © Two Fish Divers. (B) A 6.0 m TL male C. carcharias captured by fishermen in eastern Lombok, Indonesia in 2013 © Fahmi and Dharmadi (2014). (C) Upper lateral tooth collected from the white shark C. carcharias landed in eastern Lombok, Indonesia in 2013. © Fahmi and Dharmadi (2014).

Figure 2

Figure 3. Gel electrophoresis image of the amplified sequence associated with the 6.0 m TL white shark (C. carcharias) captured in 2013 by demersal longline fishermen off of eastern Lombok, Indonesia. The 100 bp DNA Ladder by Geneaid™ was used (lane 1). Experiments were conducted using three distinct primer sets: Leray-XT (Wangensteen et al., 2018), Elas02 (Taberlet et al., 2012), and GWS (Pardini et al., 2000). Each primer set was designed to target specific regions, namely cytochrome c oxidase I region (COI; lane 2), 12S ribosomal RNA region (12S; lane 3), and D-loop region (D-loop; lane 4), respectively. The Leray-XT and 12S primers amplified sequences were used to confirm the identification of species, whereas the GWS primer sequences were utilized for further investigation. The negative control (Borneo river shark [G. fowlerae]) was used to validate GWS primer (lane 5).

Figure 3

Table 1. BLAST result using the NCBI for the 6.0 m TL male white shark (C. carcharias) captured in eastern Lombok, Indonesia

Figure 4

Figure 4. Genetic relationship of 29 white sharks (C. carcharias) from the Northwest Pacific (Japan) and Australia–New Zealand subpopulations in comparison to the Indonesian specimen using the D-loop region inferred using the neighbour-joining method with the Kimura-2 model for 1000 bootstrap replications. There was a total of 412 positions in the final dataset. Bootstrap support values are shown near internal nodes.