Magazine R621 would be difficult to disentangle this (MSC) as sustainably harvested is the from the effects of age that may also Correspondence South Georgia/Shag Rocks population increase grey-matter density. (SGSR) fishery[3,4] . Understanding the neural basis Our primary goal was to investigate of mathematical processes could Genetic detection supply-chain reliability for Chilean play an important role in improving bass with respect to MSC certification. mathematical education. This would of mislabeled fish Although species substitutions help individuals struggling to learn from a certified (labeling less expensive species about numbers and arithmetic, such as more expensive species) are as dyscalculics, but it would also sustainable fishery relatively easy to detect, resolving the have a wider impact. Poor numeracy geographic origin of samples within affects not only the life chance of Peter B. Marko1,*, Holly A. Nance1,2, a single species requires genetic individuals, it is a significant cost to and Kimberly D. Guynn3 characterization of source populations. society (about £2.4 billion per year in Therefore, we analyzed mitochondrial the UK, for example). Moreover, the The decline and collapse of many of DNA (mtDNA) from retail-acquired level of mathematical competence the world’s fisheries has led to the fish using the same methods as a in a society plays a causal role in its implementation of social marketing previous study [7] that revealed SGSR economic performance, as a recent that promotes the consumption of to be genetically highly distinct from OECD report demonstrates. However, sustainably harvested seafood [1,2]. populations north of the Antarctic for neuroscience to have a practical Because the success of this strategy Polar Front (APF), an oceanographic impact, we will need to know more depends on supply chain integrity, we discontinuity separating the Southern about the neural networks underlying investigated the accuracy of eco-labels from warmer water to the north mathematical skills more complex than for Patagonian toothfish, marketed (Figure 1). Briefly, we characterized simple arithmetic, and in other areas of as ‘Chilean sea bass’ (Dissostichus fish by amplifying ~1200 nucleotides mathematics, including geometry and eleginoides), by genetically analyzing of mtDNA (control flanked by algebra. retail fish bearing certification labels tRNA proline and 12S rRNA) followed from the Marine Stewardship Council by digestion with a single restriction Further reading (MSC). For Chilean sea bass, MSC enzyme (BstNI) and visualization with Butterworth, B., Varma, S., and Laurillard, D. (2011). certification labels indicate that agarose electrophoresis (Supplemental Dyscalculia: From brain to education. Science, 332, 1049–1053. fish were harvested from the only information). Using the same method Castelli, F., Glaser, D.E., and Butterworth, B. (2006). sustainable fishery[3,4] , a population as the previous study [7] allowed us Discrete and analogue quantity processing in in waters surrounding the sub- to compare retail MSC-certified fish to the parietal lobe: a functional MRI study. Proc. Natl. Acad. Sci. USA 103, 4693–4698. Antarctic island of South Georgia and the only stock from which they could Cohen Kadosh, R., and Walsh, V. (2009). Numerical the nearby plateau at Shag Rocks [3]. have been caught and validly labeled representation in the parietal lobes: Abstract or not abstract? Behav. Brain Sci. 32, 313–328. We found that not all MSC-certified as MSC-certified. For comparison, we Dehaene, S., Bossini, S., and Giraux, P. (1993). The fish were Chilean sea bass from the applied the same methods to a sample mental representation of parity and numerical certified stock: some were simply of uncertified fish, most of which were magnitude. J. Experimental Psychol. Gen. 122, 371–396. not D. eleginoides, but among those labeled with Chile as the country of Ischebeck, A., Zamarian, L., Siedentopf, C., that were, we found significant origin. Koppelstatter, F., Benke, T., Felber, S., and Delazer, M. (2006). How specifically do we genetic differences between the retail We found that not all MSC-certified learn? Imaging the learning of multiplication sample of fish and the certified stock Chilean sea bass came from the and subtraction. Neuroimage 30, 1365–1375. population. Uncertified fish may not certified fishery. A combination of Nieder, A., and Dehaene, S. (2009). Representation of Number in the Brain. Annu. Rev. Neurosci. necessarily resemble stocks closest PCR, BstN1 digestion, and nucleotide 32, 185–208. to their country of origin because sequencing showed that 8% (3 of 36) Pesenti, M., Zago, L., Crivello, F., Mellet, E., Samson, D., Duroux, B., Seron, X., Mazoyer, capture and processing often occur at of fish labeled as MSC-certified Chilean B., and Tzourio-Mazoyer, N. (2001). Mental different places. However, significant sea bass were actually other species calculation expertise in a prodigy is sustained differences between MSC-certified (Supplemental information). Among by right prefrontal and medial-temporal areas. Nat. Neurosci. 4, 103–107. Chilean sea bass and the sole certified retail MSC-certified fish that were Pinel, P., and Dehaene, S. (2009). Beyond fishery for this species indicate that actually D. eleginoides (33 samples), hemispheric dominance: brain underlying the joint lateralization of language uncertified fish were inserted into the 15% (5 of 33 samples) had mtDNA and arithmetic to the left hemisphere. J. Cogn. MSC supply chain. haplotypes not present in SGSR Neurosci. 22, 48–66. Best known to consumers by its (haplotypes E, F, I, and J); haplotype Price, G.R., Holloway, I., Räsänen, P., Vesterinen, M., and Ansari, D. (2007). Impaired parietal market name, ‘Chilean sea bass’, the B was found at an elevated frequency magnitude processing in developmental Patagonian toothfish Dissostichus( in the retail sample, and haplotypes dyscalculia. Curr. Biol. 17, R1042–R1043. Walsh, V. (2003). A theory of magnitude: Common eleginoides) is a slow-growing, long- C and D were not found in the retail cortical metric of time, space and quantity. lived species found primarily in the sample (Figure 1). Overall, the haplotype Trends Cogn. Sci. 7, 483–488. surrounding Antarctica content of retail certifiedD. eleginoides Zago, L., Pesenti, M., Mellet, E., Crivello, F., Mazoyer, B., and Tzourio-Mazoyer, N. (2001). (Figure 1). Reported and unreported differed significantly from the SGSR Neural correlates of simple and complex mental catches of D. eleginoides increased stock (exact test for differentiation calculation. Neuroimage 13, 314–327. substantially in the 1990s [3,5] such P = 0.0026; Supplemental information). that D. eleginoides is now regarded as This discrepancy is likely caused by Institute of Cognitive Neuroscience, UCL, 17 Queen Square, London WC1N 3AR, UK. overfished[3–6] . At present, the only mislabeling of less desirable species E-mail: [email protected]; fishery where this species is considered and uncertified Chilean sea bass as [email protected] by the Marine Stewardship Council MSC-certified Chilean sea bass at Current Biology Vol 21 No 16 R622

towards sustainable fisheries, our 50ºW 41.3.1 study showed that retail labeling of MSC-certified Chilean sea bass was 41.3.3 inaccurate and that country-of-origin 80 labelling was highly misleading. South With respect to certified sustainable

87 50ºS fisheries, mislabeling ultimately results 39 in misplaced consumer demand 46 40 for uncertified fisheries, thereby 48.3484 undermining the most basic goal of this conservation strategy. 148 41.3.2413 .2 60ºS 48 4455 Supplemental information Supplemental information includes experi- 88.388.3 48.248.2 SSouthernouthern OOceancean mental procedures as well as supplemental 48.148.1 results and discussion and can be found with this article online at doi:10.1016/ j.cub.2011.07.006. 88.1, 88.2 33 Acknowledgements 48.5 K. Barr, B. Wilbur, J. McGuire, B. Sowers, C. Edwards and S. McAlister collected some Antarctica of the samples. P. Shaw provided comments A B F H C/D E/I/J on an earlier version of the manuscript. National Science Foundation Grant (OCE- 0961996) to P.B.M. supported this research. This is Technical Contribution No. 5943 of

Current Biology the Clemson University Experiment Station (USDA) under project SC-1700342.

Figure 1. Chilean sea bass (Dissostichus eleginoides) mitochondrial DNA (mtDNA) haplotype References frequencies. 1. Kolter, P., and Zaltman, G. (1971). Social Pie diagrams (sample sizes within) show the frequencies of mtDNA haplotypes from locations marketing: an approach to planned social marked by yellow stars [7] and for the retail MSC sample which was ostensibly harvested from change. J. Marketing 53, 3–12. the South Georgia/Shag Rocks fishery (SGSR). The size of each pie is proportional to the sam- 2. Jacquet, J.L., and Pauly, D. (2007). The rise ple sizes, including the retail MSC sample. The heavy dashed blue line indicates the position of seafood awareness campaigns in an era of collapsing fisheries. Marine Policy 31, 308–313. of the Antarctic Polar Front; gray lines and italicized numbers denote United Nations Food and 3. Holt, T., Medley, P., Rice, J., Cooper, J., and Agriculture (FAO) fishing areas. Hough, A. (2001). Certification report for South Georgia Patagonian Toothfish Longline Fishery. Moody Marine, Ltd., Birkenhead. one or more steps in the supply chain ambiguity of country-of-origin labelling 4. Jacquet, J.L., Pauly, D., Ainley, D., Dayton, P., between fisher and consumer. Although [9] likely resulting from the large Holt, S., and Jackson, J.B.C. (2010). Seafood stewardship in crisis. Nature 467, 28–29. a significant difference between retail distances uncertified fish are often 5. Sovacool B.K., and Siman-Sovacool, K.E. fish (that were actuallyD. eleginoides) shipped after capture. Although 92% (2008). Creating legal teeth for toothfish: using and the SGSR stock could also have of uncertified fish that were actually the market to protect fish stocks in Antarctica. J. Environ. Law 20,15–33. been caused by recent migration, Chilean sea bass (13 of 19 samples or 6. National Environmental Trust, Black Market exchange on a scale that could 68%) were labeled as having originated for White Gold: The Illegal Trade in Chilean Sea Bass. (Report, Sept. 2004) NET, Washington alter haplotype frequencies seems from Chile, 46% (6 of 13) had haplotype DC. unlikely given the slow maturation A, which is not present north of the 7. Shaw, P.W., Arkhipkin, A.I., and Al-Khairulla, of D. eleginoides (>10 years) and the APF (Figure 1). Because haplotype A H. (2004). Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic short time between the population is common south of the APF, nearly Ocean: the effect of the Antarctic Polar Front genetic study (2001) and our retail half of the uncertified fish ‘originating’ and deep-water troughs as barriers to genetic exchange. Mol. Ecol. 13, 3293–3303. sampling (2008); additional evidence from Chile were most likely captured 8. Appleyard, S.A., Ward, R.D., and Williams, R. has also established SGSR as highly in Antarctic waters, but processed (2002). Population structure of the Patagonian distinct and likely isolated from other later in Chile. This result is qualitatively toothfish around Heard, McDonald and Macquarie Islands. Antarct. Sci. 14, 364–373. stocks (Supplemental information). consistent with recent catch records: 9. http://www.ams.usda.gov/AMSv1.0/cool. Genetic exchange with nearby stocks although most (91%) of the reported 10. CCAMLR. (2004). Statistical Bull., Vol. 22, also seems particularly unlikely given 2009 Chilean harvest originated from www.ccamlr.org/pu/e/e_pubs/sb/intro.htm that the nearest potential source north of the APF (FAO area 87, Figure 1Department of Biological Sciences, populations (South America) lack three 1), vessels also harvested south of Clemson University, Clemson, SC 29631, unusual haplotypes (E, I, and J) found the APF (FAO areas 41.3.2, 48.3, 88.1, USA. 2Harbor Branch Oceanographic in the retail sample (Figure 1); in fact, 88.2), plus 5% of exports to the United Institute at Florida Atlantic University, 5600 haplotype E has only been found at States were harvested by vessels from US 1 North, Fort Pierce, FL 34946, USA. 3 Heard Island, in the southern Indian other countries [10]. Fisheries National Seafood Inspection Lab, National Oceanic and Atmospheric Ocean [8]. Although social marketing has the Administration, 3209 Frederic Street, In contrast to certified fish, analysis potential to positively impact threatened Pascagoula, MS 39567, USA. of uncertified fish exposed the species by guiding consumers *E-mail: [email protected]