High levels of mislabelling of shark flesh in Australian fish markets and seafood shops
Teagan J. Parker Kielniacz
A B , Adam J. Stow A B * and Nicolette C. Armansin A B
A
B
Abstract
Overfishing is a major cause of decline for many shark species globally, which can be largely offset by shifting consumer demand to sustainable harvests. The inherent difficulty identifying shark species after processing makes informative labelling fundamental to achieving a sustainable market.
We evaluated the level of mislabelling in Australia from shark flesh samples obtained from seafood suppliers across the country.
We used sequence data from the cytochrome oxidase subunit one gene (COI) and the 12S mitochondrial RNA gene (12S) to identify genera and likely species.
We used genetic sequence data to identify species from tissue samples from 91 fillets labelled as shark. Of these, 64 (70%) were mislabelled, and 9 comprised three species listed as threatened in Australia, the scalloped hammerhead (Sphryna lewini), greeneye spurdog (Squalus chloroculus) and school shark (Galeorhinus galeus). The scalloped hammerhead and greeneye spurdog were being sold under the label ‘flake’. Overall, 70% of samples were mislabelled and the proportion of mislabelling was significantly greater in takeaways compared with fish markets and wholesalers.
High levels of mislabelling of shark product in Australian fish markets and seafood shops was apparent both with respect to the genetically identified shark sample not matching the label and the use of ambiguous labels that do not adhere to the Australian Fish Names Standard. Mislabelling masked the presence of threatened species.
Our results reveal labelling practices that are not providing consumers with reliable information to identify shark products, and we demonstrate the utility of molecular methods in seafood trade monitoring.
Keywords: forensic identification, genetic identification, mislabelling, seafood monitoring, shark conservation, shark trade, sustainable seafood, threatened species.
Introduction
Fish are currently one of the most traded food commodities globally, with consumption having doubled in the past 50 years (Food and Agriculture Organization of the United Nations 2018, 2022). An estimated ~750,000 tonnes (Mg) of cartilaginous fishes (sharks, rays, skates and chimaeras) are listed in catch reports around the world each year as both targeted and bycatch species (Oliver et al. 2015; Food and Agriculture Organization of the United Nations 2022). Although estimating the global catch rate for all sharks is challenging, it is clear that overfishing is among the most damaging of threats to sharks (Braccini 2015; Davidson et al. 2016; Dulvy et al. 2021). Currently, approximately one-third of all shark, ray and skate species are threatened with extinction (Dulvy et al. 2021) and the abundance of some species of oceanic sharks has declined by more than 70% in the past half century, coinciding with an 18-fold increase in fishing pressures (Roff et al. 2018; Pacoureau et al. 2021).
Effective management of fisheries involves regular stock assessment and regulation of catch levels to maintain biomass at sustainable and productive levels or to allow stocks to rebuild to productive levels (Melnychuk et al. 2021; Pacoureau et al. 2023). Regulation that aims to prevent population declines is either applied at the stock-level or more broadly through international and regional agreements and country-level regulations (Gilman et al. 2014; Vincent et al. 2014; Melnychuk et al. 2021). However, the continued decline of shark populations suggests that regulatory control remains inadequate, and this seems to be for myriad reasons (Davidson et al. 2016; Cardeñosa et al. 2018; Dulvy et al. 2021). Sustainable management of shark populations is complicated by incidental bycatch, which is a key driver of population declines and is inherently difficult to monitor (Dulvy et al. 2021). Moreover, regulations aiming to reverse population declines can be difficult to enforce where resources are limited and in regions where shark fisheries are important to food security and livelihoods (McClenachan et al. 2016; Dulvy et al. 2017; Simpfendorfer and Dulvy 2017). Monitoring catch rates is critical for effective management, yet formal stock assessments exist for only 3% of all chondrichthyan species worldwide (Pacoureau et al. 2023). Managing catch rates is further hampered by poor traceability (Palin et al. 2013; Bellmann et al. 2016; Cundy et al. 2023), under-reported catch size and composition, and product mislabelling along the supply chain (Xiong et al. 2016; Dulvy et al. 2017; Shea and To 2017; Fox et al. 2018; Hellberg et al. 2019; Pazartzi et al. 2019).
Internationally, seafood mislabelling is common (Pardo et al. 2016), and is particularly high in the shark and ray trade, with reports of up to 94% of shark fillets sold being mislabelled (Griffiths et al. 2013; Agyeman et al. 2021). Poor labelling can arise at several stages along the supply chain, including at landing, wholesale or retail. Many closely related species are difficult to distinguish by sight even when fully intact at landing; for example, those in the commonly targeted Squalus and Carcharhinus genera (Miller and Mariani 2010; Hanner et al. 2011; Cardeñosa et al. 2018). Catch reports often rely on species aggregate or umbrella terms for this reason (Tillett et al. 2012). Unreliable identification is exacerbated because distinguishing features are removed during processing such as skin and fins, or from changes to fillet texture and colour from freezing or cooking. Furthermore, at the point of sale, standardised labelling conventions or standards can be lacking, poorly regulated or misplaced (Pazartzi et al. 2019; Agyeman et al. 2021; Cundy et al. 2023).
Genuine taxonomic confusion aside, commercial fraud is a widely acknowledged, but poorly understood driver of mislabelling (Luque and Donlan 2019; Chang et al. 2021; French and Wainwright 2022; Neo et al. 2022). Financial imperatives can exist for selling mislabelled fish, such as marketing a more valuable or appetising species, or to disguise catch that is protected (Pazartzi et al. 2019; Chang et al. 2021; Neo et al. 2022). Lax labelling regulations or poor enforcement result in a low risk of detection (Reilly 2018). This puts sustainable fisheries at a disadvantage and raises quality and sustainability concerns for both down-market vendors and consumers (Hanner et al. 2011; Fox et al. 2018). Although the extent of seafood fraud has not been sufficiently quantified (see Luque and Donlan 2019), a plethora of studies across more than 38 countries have found some level of mislabelling, and that the masking of threatened species is widespread (Pardo et al. 2016). Some evidence points to mislabelling being worse further along the supply chain; for example, at restaurants and takeaways (Liu et al. 2013; Vandamme et al. 2016; but see Luque and Donlan 2019).
Seafood mislabelling can also be problematic for food standards and public safety. There is evidence for both inter- and intraspecific variation in levels of heavy metals or pathogens (e.g. Biton-Porsmoguer et al. 2018), the presence of microplastics (Karami et al. 2017), or variation in nutritional value and allergic potential (Vandermeersch et al. 2015). This makes traceability of species and catch location important for quality control and safety.
The use of molecular genetics for taxonomic identification become an important method in food trade compliance monitoring (Hebert et al. 2003; e.g. Minhós et al. 2013; Sotelo et al. 2018, Pazartzi et al. 2019; Chen et al. 2020). Genetic identification by matching gene sequences with those in reference databases has been used extensively to identify elasmobranchs from raw, dried or degraded fins, and meat or gill plates (e.g. Cardeñosa et al. 2018; Fields et al. 2018; Hobbs et al. 2019; French and Wainwright 2022). It has been tested specifically for shark species in Australian waters (Ward et al. 2005, 2008; Holmes et al. 2009) but has had limited application in market surveys of traded sharks in Australia (Cundy et al. 2023).
It is estimated that over 5000 Mg of shark are landed each year in Australia (Woodhams and Harte 2018), part of the estimated 750,000 Mg of cartilaginous fish recorded globally each year (Food and Agriculture Organization of the United Nations 2022). Targeted fisheries occur in both the northern and southern states, and sharks are often sold at local fish markets and in takeaway shops. Mislabelling has already been identified across various states in Australia, where the label does not represent the taxonomy of the species sold or the label does not adhere to naming codes (Lamendin et al. 2015; Cundy et al. 2023; Sharrad et al. 2023).
The overarching code for food labelling in Australia is the Australia and New Zealand Food Standards Code (ANZFSC), which works in conjunction with state-based food standards to prevent deceptive conduct and protect consumers. These require labelling to be informative enough for purchasers to make informed decisions; however, consistency in the use of fish names is lacking. The Australian Fish Names Standard (AFNS) (AS SSA 5300–2019, Fisheries Research and Development Corporation 2024) aims to provide a consistent label for fish species traded within Australia, and as such has a designated name associated with each species or species group (currently ~250 for elasmobranchs). The AFNS cannot be enforced because it is not incorporated into the ANZFSC and standardised labelling is therefore only voluntary. Australian legislation does require that all raw seafood sold has a mandatory country of origin label, but this does not include adhering to the AFNS (Australian Government 2017). Retailers are instead encouraged to display species labels by the Fisheries Research and Development Corporation, as well as certification labels from private organisations (e.g. the blue Marine Stewardship Council label; Agnew et al. 2014). Despite these initiatives, in the absence of mandatory species labelling and the concurrent accountability, the ability for consumers to make sustainable choices is inhibited.
In Australia, shark meat is sold under a variety of terms, including ‘flake’, which is listed under the AFNS to describe two species of the genus Mustelus. Recent seafood market authentication studies of Australian seafood showed high rates of mislabelling, especially for sharks and rays (Cundy et al. 2023; Sharrad et al. 2023). Here, we investigate whether shark meat is accurately labelled across six states and territories in Australia, using genetic identification of fillets sold by wholesalers, fish markets and takeaway shops. We look at mislabelling both taxonomically and under the AFNS and compare data collected at the wholesale and ‘take away shop’ stages of the supply chain.
Materials and methods
Sample collection and storage
Between February and June 2019, we collected a total of 91 shark meat products (fresh and frozen, cooked and uncooked) from 28 Australian suppliers. These included 20 seafood retailers and wholesalers (both termed ‘markets’) selling fresh seafood, and 8 takeaway shops (‘takeaways’), which mostly sold cooked fillets. We approached venues that identified as ‘seafood markets’, ‘fish markets’, ‘fish and chips shops’, ‘fish or seafood takeaway shops’ or large wholesalers. We purchased Australian-sourced shark products, identified by lacking the mandatory country of origin label for imported raw fish (Australian Government 2017). A maximum of four fillets were taken from each vendor on the same day to minimise the chance of duplication of individual sharks. A tissue sample from each fillet was preserved in 95% ethanol and stored at room temperature. For each sample we recorded the retailer, location, date, product label and, where possible, verbal confirmation of the species from the staff on the day.
Molecular analysis and species identification
Genomic DNA was extracted using the spin column Isolate II Genomic DNA kit from Bioline (Bioline Meridian Bioscience, Australia). Two pairs of universal primers were chosen for amplification of approximately 655 bp from the mitochondrial gene cytochrome c oxidase 1 (COI) (Ward et al. 2005; Table 1). COI is widely used to distinguish species, being usually sufficiently variant among, but largely similar within species (Hebert et al. 2003; Ward et al. 2005, 2008). These primers have been frequently used to distinguish shark species effectively (e.g. Almerón-Souza et al. 2018; Pazartzi et al. 2019). Amplification was carried out in 10-μL reactions containing 1 μM of each primer, 200 μM of each DNTP, 2 mM of MgCl and 1 unit of Taq polymerase. The polymerase chain reaction (PCR) conditions for the amplification of COI were the same for each primer pair and were as follows: an initial denaturation at 95°C for 10 min, followed by 45 cycles at 94°C for 30 s, 54°C for 30 s, 72°C for 1 min, and a final elongation phase of 72°C for 10 min. A primer pair targeting the 12S RNA gene region was also chosen to amplify ~171 bp (Taberlet et al. 2018), carried out in 10-μL reactions containing 1 μM of each primer, 200 μM of each DNTP, 2 mM of MgCl and 1 unit of Taq polymerase. PCR cycling conditions were as follows: initial denaturation at 95°C for 10 min, followed by 35 cycles at 95°C for 30 s, 59°C for 30 s, 72°C for 1 min and a final elongation phase of 72°C for 7 min.
| Target gene | Primer name | Primer sequence (5′−3′) | Primer length (bp) | Amplicon length (bp) | Reference | |
|---|---|---|---|---|---|---|
| COI | FishF1 | 5′-TCAACCAACCACAAAGACATTGGCAC-3′ | 26 | 655 | Ward et al. (2005) | |
| FishR1 | 5′-TAGACTTCTGGGTGGCCAAAGAATCA-3′ | 26 | 655 | Ward et al. (2005) | ||
| FishF2 | 5′- TCGACTAATCATAAAGATATCGGCAC-3′ | 26 | 655 | Ward et al. (2005) | ||
| FishR2 | 5′- ACTTCAGGGTGACCGAAGAATCAGAA-3′ | 26 | 655 | Ward et al. (2005) | ||
| 12S | Elas02-F | 5′-GTTGGTAAATCTCGTGCCAGC-3′ | 21 | 171 | Taberlet et al. (2018) | |
| Elas02-R | 5′-CATAGTAGGGTATCTAATCCTAGTTTG-3′ | 26 | 171 | Taberlet et al. (2018) |
Polymerase chain reaction purification and Sanger sequencing in the forward direction was conducted by Macrogen (Seoul, South Korea). All samples were re-sequenced three times, as a number of poor quality sequences were returned, indicative of contamination. Sequences were aligned and trimmed using MEGA software (ver. 11.0.13, see https://www.megasoftware.net; Tamura et al. 2021). To identify species and genera, individual COI sequences were matched to reference sequences in the NCBI’s GenBank database using the BLASTn (see https://blast.ncbi.nlm.nih.gov) program with the Megablast algorithm (Altschul et al. 1990; Zhang et al. 2000). We confirmed species identification when the following conditions were met: the highest percentage identity (PI) was ≥98%, which ensures that the sample is well matched to the reference sequence (Wong et al. 2009), and query cover ≥90% (i.e. the extent of overlap between the homologous sequences). Assignments were accepted at e-values at 0–0.00001, which gives a likelihood estimate of matches by chance in the database. We cross-referenced these assignments with the Barcode of Life Data System (BOLD, see www.boldsystems.org; Ratnasingham and Herbert 2007) for the species where sequences matched with a PI ≥ 98%. To further confirm identification at the taxonomic level of genus we searched the NCBI database for matches with our 12S sequence data using BLASTn. We assigned the genus where all matches with PI ≥ 97% were from the same genus.
Threatened species identification
Species of shark that are threatened in Australia (local status) refers to any listing under the national Environmental Protection and Biodiversity Conservation Act 1999 (EPBC Act) and state-based protections. Threatened species listed as ‘Conservation Dependent’ under the EPBC Act have management plans in place and can continue to be taken in fisheries. We also acknowledge that these listings may lag behind real conservation concern, we therefore also refer to threatened status according to the Shark Action Plan (SAP; Kyne et al. 2021), which applied IUCN criteria to local shark stocks and recommends protection gaps not currently reflected under the Australian system. Global status includes listing as CR (Critically Endangered), EN (Endangered), VU (Vulnerable), NT (Near Threatened) on the IUCN Red List for global assessments (see https://www.iucnredlist.org), as well as listing on the Convention on Migratory Species (CMS) and Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES).
Assessment of labelling accuracy
We identified cases of mislabelling using three definitions: (1) cases where vendor labels were not consistent with the AFNS (‘AFNS non-compliant’); (2) where either the species or genus described by the vendors or label did not match with those from the genetic analysis (‘taxonomically incorrect’); and (3) both measures under both definition (1) and (2) were combined as an overall measure of mislabelling. We applied a lenient interpretation for label discrepancies that were close to the AFNS though not strictly the same, or that were recently obsolete; for example, we included ‘gummy flake’ as correctly labelled under the category of flake. Where taxa can be used interchangeably in the common vernacular (e.g. ‘carpet shark’ for wobbegong), we considered this taxonomically correct but not under the AFNS. Where possible, we asked staff whether the labels were accurate and recorded the descriptions they provided to compare against the labels. We do not make claims as to the vendors intention in any of the cases of mislabelling that we found.
To assess whether the prevalence of mislabelling varies along the supply chain, we compared the number of mislabelled samples at markets with that at takeaways using a Fisher’s exact test.
Results
DNA and sequencing evaluation
We obtained sequence matches for 71 of the 91 tissue samples (Table 2). Of these, 46 were identified to species level (COI region, PI ≥ 98% from Genbank and BOLD) and 25 to genus only (24 using 12S region, PI ≥ 97% on Genbank, and 1 using COI as above; see Table S1 of the Supplementary material). Matches were inconclusive for 20 samples due to either a low identity match or a high match to a bacterial taxon (suggesting potential sample contamination).
| Location | Markets | Takeaways | Samples collected | Successfully matched | |
|---|---|---|---|---|---|
| Canberra, Australian Capital Territory (ACT) | 15 | – | 15 | 14 | |
| Sydney and South Coast, New South Wales (NSW) | 12 | 2 | 14 | 10 | |
| Brisbane, Queensland (Qld) | 10 | 15 | 25 | 19 | |
| Adelaide, South Australia (SA) | 1 | 4 | 5 | 4 | |
| Melbourne, Victoria (Vic.) | 16 | 4 | 20 | 14 | |
| Perth, Western Australia (WA) | 12 | – | 12 | 10 | |
| Total | 91 | 71 |
For 16 samples, several congeneric species from 4 genera were in the clusters of matches where PI ≥ 98% (Carcharhinus, n = 4; Orectolobus, n = 4; Squalus, n = 4; and Mustelus, n = 4; Table S1). In these cases, we assigned the species with the highest match probability but recorded the congenerics (Table S1). We excluded reads of PI ≥ 98% for less related species if they represented <3% of the top 100 reads, as these were most likely errors in the databases (Tables S1–S2 of the Supplementary material). We believe a lack of resolution with COI for distinguishing Orectolobus, Squalus and Mustelus species to be the likely cause of errors. All samples were confirmed to be from shark species, except for four samples from two teleost species (Mugil cephalus, n = 3; and Lates calcarifer, n = 1); however these genera were not confirmed using 12S.
Overall, we identified 14 species, 12 genera and assigned these to 10 families (Table 3). The most common genera in terms of sample numbers were Carcharhinus (n = 29) followed by Pristiophorus (n = 12), and the most common in terms of species diversity was also Carcharhinus (n = 3) and Orectolobus (n = 3). The most commonly identified species were the common sawshark (Pristiophorus cirratus, n = 12), followed by school shark (Galeorhinus galeus, n = 4), gummy shark (Mustelus antarcticus, n = 4), dusky whaler (Carcharhinus obscurus, n = 4) and western wobbegong (n = 4).
| Family | Genus | Species | Common name | Number of samples | Sample origin | |
|---|---|---|---|---|---|---|
| Callorhinchidae | Callorhinchus | C. milii | Elephantfish | 1 | Qld | |
| Carcharhinidae | Carcharhinus | C. brevipinna | Spinner shark | 3 | Qld | |
| C. leucus | Bull shark | 1 | ACT | |||
| C. obscurus | Dusky whaler | 4 | WA | |||
| – | – | 21 | ACT, NSW, Qld, SA, WA | |||
| Centrophoridae | Centrophorus | – | Dogfish spp. | 1 | Vic. | |
| Deania | – | Dogfish spp. | 1 | Vic. | ||
| Latidae | Lates | L. calcarifer | Barramundi | 1 | NSW | |
| Mugilidae | Mugil | M. cephalus | Mullet | 3 | NSW | |
| Orectolobidae | Orectolobus | O. halei | Gulf wobbegong | 3 | NSW, Vic. | |
| O. hutchinsi | Western wobbegong | 4 | WA | |||
| O. maculatus | Spotted wobbegong | 1 | NSW | |||
| Pristiophoridae | Pristiophorus | P. cirratus | Common sawshark | 12 | ACT, NSW | |
| Sphyrnidae | Sphyrna | S. lewini | Scalloped hammerhead | 3 | Qld | |
| Squalidae | Squalus | S. chloroculus | Greeneye spurdog | 2 | Vic. | |
| – | – | 2 | Vic. | |||
| Triakidae | Galeorhinus | G. galeus | School shark | 4 | Vic. | |
| Mustelus | M. antarcticus | Gummy shark | 3 | Vic. | ||
| Mustelus | M. antarcticus | Gummy shark | 1 | SA | ||
| Inconclusive | – | – | – | 20 | ACT, NSW, Qld, SA, Vic., WA | |
| Total | 91 |
Threatened species identification
Genetic analysis confirmed 17 (23.9%) samples from 6 globally threatened species listed by the IUCN (Table 4), 2 that are Critically Endangered (Sphryna lewini, Rigby et al. 2019a and G. galeus, Walker et al. 2020), 2 Endangered (C. obscurus, Rigby et al. 2019b; and Squalus chloroculus, Walker and Rochowski 2019) and 2 Vulnerable (Carcharhinus leucas, Rigby et al. 2021; and Carcharhinus brevipinna, Rigby et al. 2020). In Australia, two of these species (S. lewini and G. galeus) meet the criteria for Endangered under the EPBC Act and are listed as Conservation Dependent (Kyne et al. 2021), whereas S. chloroculus is endemic to Australia and listed as Endangered under the IUCN Red List criteria (Kyne et al. 2021; Fisheries Research and Development Corporation 2024). The remaining globally threatened species (C. brevipinna, C. obscurus and C. leucas) are not listed as threatened in Australian waters under the EPBC Act nor meet the IUCN Red List criteria for threatened according to the SAP (Kyne et al. 2021).
| Species | Global IUCN, CITES, CMS | Local EPBC Act, SAP, State | Australian distribution | Number of samples | Sample origin | |
|---|---|---|---|---|---|---|
| Bull shark (C. leucus) | VU ↓ (IUCN) | NL (EPBC Act) LC (SAP) | WA, NT, Qld, NSW | 1 | ACT | |
| Dusky shark (C. obscurus) | EN ↓ IUCN A2 CMS A | NL (EPBC Act) NT (SAP) | All – western delineated | 4 | WA | |
| Greeneye spurdog (S. chloroculus) | EN ↓ IUCN | NL (EPBC Act) EN (EPBC Act) | NSW, Vic., Tas., SA | 2 | Vic. | |
| Scalloped hammerhead (S. lewini) | CR ↓IUCN A2 CITES A2 CMS A | CD (EPBC Act) EN (SAP) EN (NSW FMA) B | NSW, Qld, NT, WA | 3 | Qld | |
| School shark (G. galeus) | CR ↓ IUCN A2 CMS A | EN (SAP) CD (EPBC Act) | All, excl. NT | 4 | Vic. | |
| Spinner shark (C. brevipinna) | VU ↓ IUCN | LC but Aust is global refuge (SAP) NL (EPBC Act) | WA, NT, Qld, NSW | 3 | Qld |
IUCN, International Union for Conservation of Nature and Natural Resources; CITES, Convention on International Trade in Endangered Species of Wild Fauna and Flora; CMS, Convention on Migratory Species; EPBC, the Environmental Protection and Biodiversity Conservation Act 1999; SAP, Shark Action Plan; CR, Critically Endangered; EN, Endangered; VU, Vulnerable; NT, Near Threatened; LC, Least Concern; CD, Conservation Dependent; NL, Not Listed. ↓ indicates declining populations in IUCN assessment. Globally threatened but important stocks well-managed in Australia under SAP; A2, CITES Appendix 2 (Kyne et al. 2021; Department of Climate Change, Energy, the Environment and Water 2024; also see the Red List at https://www.iucnredlist.org).
Labelling analysis
Overall, 64 of the 91 samples (70%) were mislabelled, either because the label was not AFNS compliant (17 of 91 samples) or genetic sequence matching indicated that the wrong species was designated to the AFNS compliant label (47 of 71 samples). Fourteen samples were both AFNS compliant and taxonomically correct (Table 5).
| Barcoding result | AFNS name | Vendor label | Mislabelled | Origin | Venue | n | |
|---|---|---|---|---|---|---|---|
| Callorhinchus milii (elephantfish) | Elephantfish | Flake A | Yes | Qld | Takeaway | 1 | |
| Carcharhinus brevipinna (spinner shark) | Spinner shark | Flake A | Yes | Qld | Takeaway | 3 | |
| Carcharhinus leucas (bull shark) | Bull shark | Flake A | Yes | ACT | Market | 1 | |
| Carcharhinus obscures (dusky whaler) | Dusky whaler or bronze whaler sharks | Bronze A whaler | No | WA | Market | 6 | |
| Carcharhinus sp. | By species common name, or congeneric group | Flake A | Yes | ACT | Market | 3 | |
| Qld | Takeaway | 6 | |||||
| SA | Takeaway | 3 | |||||
| Large boneless fillet | Yes | NSW | Market | 1 | |||
| Shark barrel | Yes | Qld | Market | 2 | |||
| Aust. shark | Yes | Qld | Market | 4 | |||
| Centrophorus sp. | By species common name, or congeneric group | Flake A | Yes | Vic. | Takeaway | 1 | |
| Deania sp. | By species common name | Flake A | Yes | Vic. | Takeaway | 1 | |
| Galeorhinus galeus (school shark) | School Shark | School A shark | No | Vic. | Market | 4 | |
| Lates calcarifer (barramundi) | Barramundi | Boneless fillet: roughskin shark | Yes | NSW | Market | 1 | |
| Mugil cephalus (mullet) | Sea mullet or mullet | Flake A | Yes | NSW | Market | 3 | |
| Mustelus antarcticus (gummy shark) | Flake or gummy shark | Gummy A flake | No | Vic. | Market | 3 | |
| Flake A | No | SA | Market | 1 | |||
| Orectolobus halei (gulf wobbegong) | Wobbegong | Flake A | Yes | NSW | Takeaway | 2 | |
| Gummy A flake | Yes | Vic. | Market | 1 | |||
| Orectolobus hutchinsi (western wobbegong) | Wobbegong | Carpet shark | Yes | WA | Market | 4 | |
| Orectolobus maculates (spotted wobbegong) | Wobbegong or spotted wobbegong | Boneless fillet | Yes | NSW | Market | 1 | |
| Pristiophorus cirratus (common sawshark) | Common sawshark or sawshark | Gummy A shark | Yes | ACT | Market | 3 | |
| Flake A | Yes | ACT | Market | 7 | |||
| Boneless sweetfish | Yes | NSW | Market | 1 | |||
| Flake fillet A | Yes | NSW | Market | 1 | |||
| Sphyrna lewini (scalloped hammerhead) | Scalloped hammerhead | Flake A | Yes | Qld | Market | 3 | |
| Squalus chloroculus (greeneye spurdog) | Greeneye dogfish | Flake A | Yes | Vic. | Market | 2 | |
| Squalus sp. | Flake A | Yes | Vic. | Market | 2 |
AFNS compliance
Across the 91 samples, vendors used 13 labels; however, we counted ‘flake fillet’ and the now obsolete ‘gummy flake’ as being labelled ‘flake’ leaving 11 labels available for analysis. A total of 4 of the 11 labels were AFNS compliant: ‘flake’, ‘gummy shark’, ‘bronze whaler’ and ‘school shark’. Flake (and its derivatives) was by far the most common label (n = 59). Five labels were taxonomically specific (n = 78), these being ‘flake’ and ‘gummy shark’ (Mustelus spp.), ‘carpet shark’ (Orectolobidae spp.), ‘bronze whaler’ (either bronze or dusky whaler under AFNS) and ‘school shark’ (G. galeus). The remaining seven non-compliant labels (n = 13) were: ‘Aus. shark’, ‘boneless fillet’, ‘boneless fillet: roughskin shark’, ‘boneless sweetfish’, ‘large boneless fillet’ and, ‘shark barrel’.
From 19 venues, we received a verbal description from the staff of the species being sold and found that 16 of these did not match the vendor’s label and 7 responses were not taxon-specific (Table 6). Two species descriptions given verbally matched the genetic identification, but not their shop labels (NSW-06: labelled as ‘flake’ but the vendor said it was wobbegong and the genetic sequences confirmed it as Orectolobus halei; VIC-05: fillet labelled as ‘flake’, the vendor said it was dogfish, which was confirmed as the green-eyed spurdog (S. chloroculus).
| Sample | Vendor label | Vendor response | Genetic identification | |
|---|---|---|---|---|
| ACT-01, 03 | Flake | Mako shark | Carcharhinus sp. | |
| ACT-02 | Flake | Mako shark | Carcharhinus leucus | |
| ACT-04, 05, 06, 07 | Flake | Gummy shark | Pristiophorus cirratus | |
| ACT-08 | Flake | Just shark | Carcharhinus sp. | |
| ACT-09 | Flake | Just shark | Inconclusive | |
| ACT-10, 11, 12 | Flake | Gummy shark | Pristiophorus cirratus | |
| ACT-13, 14, 15 | Gummy shark | Flake is big shark, gummy is small shark | Pristiophorus cirratus | |
| NSW-01 | Boneless fillet | Shark | Inconclusive | |
| NSW-02 | Boneless fillet | Angel shark | Orectolobus maculatus | |
| NSW-03, 04, 05 | Flake | School shark, caught local | Mugil cephalus | |
| NSW-06, 07 | Flake | Carpet shark–wobbegong | Orectolobus halei | |
| NSW-08 | Large boneless fillet | Toothed shark but unsure | Carcharhinus sp. | |
| NSW-11 | Boneless sweetfish | Baby shark | Pristiophorus cirratus | |
| NSW-12, 13 | Flake fillet | Sawfish | Inconclusive | |
| QLD-01, 02, 03 | Flake | Blacktip reef shark. We also sell Mako shark when it’s available. | Sphyrna lewini | |
| QLD-04, 05, 06, 07 | Flake | Blacktip reef shark | Carcharhinus brevipinna | |
| QLD-08, 09 | Flake | Imported from Taiwan. The only shark species you can eat. | Inconclusive | |
| QLD-10 | Flake | Imported from Taiwan. The only shark species you can eat. | Callorhinchus capensis | |
| QLD-11, 12 | Flake | The Melbourne species. | Inconclusive | |
| QLD-17 | Flake | Blacktip shark | Inconclusive | |
| VIC-05, 06 | Flake | Dogfish shark | Squalus chloroculus | |
| VIC-09, 10, 11, 12 | Flake | Angelshark | Inconclusive |
Mislabelling by taxon
Five taxon-specific labels were recorded, including ‘bronze whaler’, ‘carpet shark’, ‘gummy shark’, ‘roughskin shark’, ‘school shark’ and ‘flake’ (including its derivatives). Overall, we found taxa (species or genus only) were mislabelled in 47 cases (66%). Matching barcoded taxa to species-specific vendor labels was not possible for 31 samples because of insufficient genetic resolution or uninformative labelling. Two samples were labelled as Bronze whaler but could only be genetically identified to genus level (Carcharhinus). A further nine samples were labelled using one of five taxonomically unspecified terms including ‘Aus. shark’, ‘boneless fillet’, ‘boneless sweetfish’, ‘large boneless fillet’ and ‘shark barrel’, and therefore matching the genetic sequences with vendor labels was not possible for these. Carcharhinus species were the most commonly mislabelled (C. obscurus, n = 4, C. brevipinna, n = 3, C. leucas, n = 1, Carcharhinus genus only, n = 12) followed by P. cirratus (n = 11).
Of the 59 samples labelled as ‘flake’, 88% were not the AFNS-designated species (Mustelus mustelus and Mustelus lenticulatus) and consisted of 10 genera and 9 species. These included 40 samples where sequences did not match to the AFNS-designated species (Table 5) and 12 samples where sequence matching was inconclusive but the vendor identified a species (Table 6). Three samples labelled as ‘flake’ were not identified by the vendor and sequence matching was also inconclusive (Table S1). The four samples correctly labelled were all sold as pre-packed fillets. The four verifiable samples labelled ‘bronze whaler’ were C. obscurus, which is compliant as that label can be used for both Carcharhinus brachyurus and C. obscurus. All fillets labelled ‘school shark’ were compliant and sequences matched with G. galeus.
For the non-compliant labels, ‘carpet shark’ was used for species of wobbegong (Orectolobidae spp.). This is not compliant because standard advises the label ‘wobbegong’ should be applied to Orectolobidae spp. However, we counted these as taxonomically correct as ‘carpet shark’ is a common term for this genus. Other Orectolobidae were labelled as ‘flake’ or ‘boneless fillet’. ‘Roughskin shark’ most likely refers to the standard name ‘roughskin dogfish’ but was sequenced as the finfish (L. calcarifer) or sequence matching was inconclusive.
Threatened species labelling
We identified nine samples from three species listed as threatened in Australia (Table 4). Only the school shark (G. galeus) was correctly labelled with the other two species (S. lewini and S. chloroculus) incorrectly labelled as ‘flake’ (Table 5).
Markets v. takeaways
Labelling inaccuracies occurred at markets and takeaway venues. In total, 47 of the 66 samples from markets were mislabelled, either taxonomically (n = 31 of 52 barcoded samples) or under the AFNS (n = 17 of 66 label observations). Labels using the term ‘flake’ (either ‘flake’, ‘flake fillet’ or ‘gummy flake’) comprised 44% of labels at fish markets. All samples from takeaways were labelled as ‘flake’, and of those that could be confirmed with genetic sequence matching (n = 17; the other 8 were inconclusive), none were Mustelus species. All of the labels with correct taxon (n = 14) were from fish markets. Takeaways showed significantly higher taxonomic mislabelling than markets (Fisher’s exact statistic = 0; d.f. = 1, P < 0.05) and a greater use of non-compliant AFNS labels (Fisher’s exact statistic <0.0001, d.f. = 1, P < 0.05).
Discussion
The labelling used by vendors of shark flesh frequently did not adhere to guidelines, and a high proportion of labels were not compatible with the species of shark being sold. Data from 91 shark flesh samples collected from 28 vendors in five Australian states reveal that more than half of the labels were non-compliant with the AFNS, and genetic identification showed that the majority of the five species-specific labels incorrectly represented the species being sold. The most misused label for shark flesh was ‘flake’, which is supposed to be used for product derived from the sustainable gummy shark fishery (Simpfendorfer et al. 2019). Furthermore, product incorrectly labelled as ‘flake’ was shown to mask the presence of three species listed as threatened in Australian waters, two listed under the EPBC Act and another listed in the Shark Action Plan as meeting the IUCN Red List criteria. Although our findings are based on modest sample sizes, they are consistent with other recent analyses of mislabelling with Australian shark product.
Recent genetic barcoding analyses of Australian seafood, including sharks and rays, are compatible with our results. We found that 70% of samples were mislabelled under the AFNS guidelines, compared with 78% reported by Cundy et al. (2023) and the 89% of retailers mislabelling shark product in South Australia (Sharrad et al. 2023). Globally, averaged levels of seafood mislabelling were at 5–30%, and generally higher in the elasmobranch trade ranging from 2% (Griffiths et al. 2013) to 94% (Agyeman et al. 2021) with a 2016 average of ~50% (Pardo et al. 2016).
The AFNS prescribes standard fish names for production or trade by retailers and restaurants (i.e. consumer trade) but is not mandated in the ANZFSC. We found non-compliance with the AFNS at takeaways and mislabelling at 26% at markets. The level of taxonomic mislabelling was also significantly higher at takeaways than markets (68 v. 47% respectively). Our findings are compatible with previous work showing that mislabelling is generally more prevalent further along the supply-chain, with restaurants and takeaways generally showing lower compliance than retailers (Pardo et al. 2016).
The most misused label was ‘flake’ with 14 vendors misrepresenting 9 species and 10 genera with this label. Under the AFNS, ‘flake’ is the designated label for gummy shark (M. antarcticus) and rig (M. lenticulatus) both of which are considered sustainably harvested in Australia (Simpfendorfer and Dulvy 2017; Patterson et al. 2019; Simpfendorfer et al. 2019). The high level of misuse of the label ‘flake’ in Australia was also found by Cundy et al. (2023) who reported that 67% of samples were incorrectly labelled as ‘flake’ as opposed to 88% found here. In the past 5 years, commercial take of M. antarcticus in the SESSF has not exceeded the annual RBC quota limit (Woodhams and Harte 2018; Petrolo et al. 2021). These results highlight the need for accurate labelling to allow for consumer confidence when selecting flake because it is sustainably harvested.
Misuse of the term ‘flake’ was shown to mask the presence of five species listed as threatened at a global scale by the IUCN: G. galeus, S. lewini, C. brevipinna, C. leucas and S. chloroculus. Three of these species are listed as threatened in Australia. The scalloped hammerhead shark (S. lewini) and school shark (G. galeus) are listed as ‘Conservation Dependent’ under the EPBC Act and population numbers in Australian waters have declined by more than 50% in the last 70–80 years (Kyne et al. 2021). In 2022, the green-eye spurdog (S. chloroculus) was nominated to receive threatened species listing under the EPBC Act and is currently under assessment, after inferred population declines of >50% over the last 63 years (Kyne et al. 2021). Both S. lewini and G. galeus are listed as Critically Endangered, and S. chloroculus, an Australian endemic, is listed as Endangered on the global IUCN Red List of Threatened Species. S. lewini has also been listed under CITES Appendix II, which allows for regulated trade, though monitoring may be hampered by frequent mislabelling of this species (e.g. Hobbs et al. 2019; Biffi et al. 2020; Munguia-Vega et al. 2022).
Each of the species listed as threatened in Australia and mislabelled as ‘flake’ are morphologically distinct from gummy sharks or rig and are unlikely to have been misidentified at capture. However, there are species that are difficult to distinguish from each other using morphological features, and this also contributes to mislabelling. Carcharhinids or requiem sharks are an example of a group threatened by overfishing that may be difficult to distinguish (see the Red List at https://www.iucnredlist.org). This issue is compounded by the current AFNS allowing for umbrella terms for groups of species; for example, both C. obscurus and C. brachyurus have been assigned the label ‘bronze whaler’. Morphological identification is also notoriously difficult for dogfish of Squalus spp. In south-east Australia, there have been population declines of up to 97% from 1970 to 1990 mainly due to bottom trawling (Graham et al. 2001; Australian Fisheries Management Authority 2012). However, dogfish catch records have been only specified to genera, which presents problems for down-market labelling. Informative labels are crucial to the maintenance of species-specific catch data and the development of more effective protective measures (Barbuto et al. 2010; Liu et al. 2013; Almerón-Souza et al. 2018; Bunholi et al. 2018; Pazartzi et al. 2019).
Accurate labelling is essential to ensure the authenticity of seafood products, prevent commercial fraud and allow for the sustainable management of fish stocks. Our results demonstrate that the Australian shark trade is consistent with the global problem of product mislabelling, and consequently with the monitoring of sharks being traded and consumed, including threatened species. Australia is signatory to several international agreements and has obligations to manage the trade in protected species. In the absence of standardised and enforced labelling, not only are these obligations difficult to meet, but wider conservation efforts by fisheries, responsible vendors and consumers are negated. We demonstrate how genetic-based identification can be used for market surveys to highlight the hidden trade in shark meat, which can contribute to more effective shark management.
Data availability
The authors confirm that the raw data supporting the findings of this study will be available in DRYAD.
Conflicts of interest
The authors declare that they have no known conflicts of interest associated with this publication and have received no financial support or personal benefits that could have influenced the research presented in this article.
Declaration of funding
The authors thank the SeaLife Trust and the Linnean Society of New South Wales for providing funding for sequencing.
Acknowledgements
We thank Johan Pansu, Christine Chivas and Natalie Caulfield for assistance with laboratory work, and Leonardo Guida, Ingrid Neilson, Shannon Hurley and others from the Australian Marine Conservation Society, Kerstin Bilgman, Natalie Caulfield, Philippa Moore, Evie Parker Kielniacz, Aleksie Villis, Ryan Anderson and Jo MacKellar for assistance with sample collection.
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