Translator Disclaimer
18 March 2013 Heavy metal concentrations of Two highly migratory sharks (Prionace glauca and Isurus Oxyrinchus) in the southeastern Pacific waters: comments on public health and conservation
Sebastián A. Lopez, Nicole L. Abarca, Roberto C. Meléndez
Author Affiliations +
Abstract

Despite the importance of sharks in structuring the marine food web, their biomass is declining dramatically throughout the world's oceans due to fishing pressures. Sharks caught as by-catch in long-line fisheries are sold for shark fins in the Asian fish market and secondarily as trunk sales for local consumption and fish meal. In order to determine the levels of heavy metals (mercury and lead) in oceanic shark populations in South Pacific waters, analyses of 39 Prionace glauca and 69 Isurus oxyrinchus were conducted. Mercury (Hg) and lead (Pb) were measured by cold vapor and via acetylene flame techniques, respectively. Mercury concentrations were similar in the studied sharks (p=0.1516), with 0.048 ± 0.03 µg·g−1 w/w for P. glauca and 0.034 ± 0.023 µg·g−1 w/w for I. oxyrinchus. P. glauca showed greater values of lead than I. oxyrinchus (p<0.001). Large specimens of both species showed high heavy metal concentration, while sexes showed no statistical differences (p>0.05). The metal concentrations reported in this work constitute a risk for human health, mainly from the high contributions of lead in tissues of P. glauca and I. oxyrinchus.

Introduction

Blue shark (Prionace glauca) and mako short fin shark (Isurus oxyrinchus) are pelagic, oceanic and highly migratory species [1]. These fishes have a wide geographic range and play an important role in marine food webs as apex predators, feeding on squid, tuna and other fishes [234567]. The importance of these sharks in structuring marine food webs has been demonstrated, thus their biomass decrease throughout the world's oceans is a concern [8,9]. Acuña [10] reported that sharks comprise over 70% of the total catch in the swordfish long-line fisheries. Sharks caught as by-catch in long-line fisheries are sold for shark fins in the Asian market and as trunk sales for local meat consumption and fish meal [11].

Sharks accumulate trace elements in their tissues such as mercury (Hg), arsenic (As) and lead (Pb)[12,13], largely through the diet [12]. Although blue and mako short fin sharks are the most abundant and are highly exploited throughout the oceans, knowledge of their heavy metal concentrations is very poor. The mercury and lead concentration of P. glauca and I. oxyrinchus tissues since 1974 in different oceans is summarized in Appendix 1. Mercury is the most studied element, principally in the Northern Hemisphere; in contrast lead is the least studied. Mercury and lead are volatile and highly toxic environmental contaminants present in marine ecosystems [13] where sharks are more susceptible to uptake and biomagnification of these heavy metals, because they incorporate the metals very efficiently and eliminate them slowly.

In the southeastern Pacific Ocean concentrations of mercury and Lead in fresh fish tissues for human consumption are not regulated, but international agencies (European Union and Food and Agriculture Organization/World Health Organization) have established limits for these heavy metals, which are 1.0 µg·g−1 and 0.3 µg·g−1 wet weight for mercury and lead, respectively [15161718]. In addition, since well-documented incidents of heavy metal exposure of human communities in Japan and Iraq have resulted in severe toxic effects [19], there has been widespread public concern over the bioaccumulation of heavy metals through consumption of shark meat by humans as well as by animals. The main goal of this study was to determine the mercury and lead concentrations in different tissues of two highly migratory sharks that are consumed by humans.

Methods

During March 2011 and December of 2011 one hundred and eight sharks (n=69 I. oxyrinchus and n=39 P. glauca) were collected as by-catch from industrial long-line swordfish (Xiphias gladius) fisheries off Chile, in a geographic range between 21°– 35°S and 78°– 118°W. The total length (TL) was measured and sex determined on board. Muscles from the dorsal part and liver samples (1.0 g) were taken from both species of sharks; however, stomach tissue was obtained only from mako shark specimens. All tissue samples were stored at −80 °C until processing in the laboratory.

Laboratory analysis

All laboratory material was previously decontaminated for two days with HNO3 (20%) [20] and washed with mili-Q water. Tissue samples were digested with 65% HNO3 using a microwave system [21,22] and analyzed with a Shimadzu AA-6200 atomic absorption spectrophotometer (AAS). Mercury was analyzed by a hydride vapor system HV-1 (cold vapor technique), and lead was measured by acetylene flame [21,22]. The AAS was calibrated using Custom Grade standards, with detection limits of 0.007 µg·g−1 for mercury (Certipur Merck 1000 mg/L) and 0.0088 µg·g−1 for lead (PbCl2). Further quality control included periodic blind analysis of an aliquot from a large sample of known concentration, and blind runs of duplicate samples (± 15%) during the analysis for each metal.

Data analyses

Based on size, studied specimens of blue shark were assigned into groups according to Lopez [2] as small (Ss): TL ≤ 195 cm, and large (Ls): TL > 195 cm. Similarly, individuals of Mako short fin sharks with TL ≤ 285 cm were considered small, and specimens above 285 cm of TL were large. The Shapiro-Wilks test was used to test the normality of data of concentrations of mercury and lead in blue and mako shark tissues, and a one-way ANOVA followed by a Tukey's post hoc test was used to compare heavy metal concentrations in different species, groups, sexes and type of tissues. All statistical analyses were performed using R software [23].

Results

Tissue/organ concentrations

Considering all tissues analyzed (muscle, liver and stomach), P. glauca showed 0.048 ± 0.03 (mean ± standard deviation) µg·g−1 of Hg and 1.996 ± 0.67 µg·g−1 of lead, while I. oxyrinchus presented 0.034 ± 0.023 and 0.922 ± 0.44 µg·g−1 of mercury and lead, respectively. The statistical test did not find differences in the mercury concentration of specimens of blue and mako sharks (F=2.08; p=0.1516) (Fig 1a). However, blue sharks exhibited a significantly higher accumulation of lead than mako sharks (F=24.7; p<0.001) (Fig. 1b).

Fig. 1.

Mercury and lead concentration comparison of blue sharks and mako shortfin sharks off Chile in 2011. a) mercury and b) lead concentration. p-value corresponding to one way ANOVA.

10.1177_194008291300600103-fig1.tif

Analyzing metal concentrations separately, blue shark mercury concentrations in the liver (0.104 ± 0.03 µg·g−1) were greater than in muscle tissues (0.014± 0.09 µg·g−1), and significantly different (F=40.6; p < 0.001). In contrast, lead concentration was greater in muscle tissue (2.244 ± 0.81 µg·g−1) than in liver (1.602 ± 0.298 µg·g−1) but statistically similar (F=2.17; p = 0.1491).

In mako shark individuals, mercury concentrations were highest in the liver, followed by stomach tissue and muscle tissue with 0.108 ± 0.02, 0.06 ± 0.01 and 0.006 ± 0.001 µg·g−1, respectively. Lead concentration was greater in liver (1.67 ± 0.28 µg·g−1) than in muscle (0.848 ± 0.47 µg·g−1) and stomach tissues (0.448 ± 0.16 µg·g−1); the statistical analysis also revealed that differences in levels of mercury and lead were highly significant (p <0.001).

Concentration by sexes and size

Male blue sharks had the highest concentration of mercury with 0.07 ± 0.03 µg·g−1, followed by female mako sharks with 0.04 ± 0.02 µg·g−1 (Appendix 2). Male blue sharks had statistically significant (p=0.012) greater mercury values than females. No differences were found in mercury concentration in males and females of mako shark (p=0.2969) (Appendix 3). In contrast to blue sharks, female mako sharks had higher mercury concentrations than males (Appendix 2). In comparison with individuals of mako shark, females and males of blue sharks had higher concentrations of lead with 2.07 ± 0.84 and 1.9 ± 0.4 µg·g−1, respectively (Appendix 3). Nevertheless, it should be noted that female blue and mako sharks had higher concentrations of lead than males.

In large-sized sharks (Fig. 2 and 3), the highest concentrations of mercury were found in blue sharks with 0.05 ± 0.03 µg·g−1, and 0.04 ± 0.02 µg·g−1 for mako sharks. In contrast, the highest lead concentrations were encountered in small sized blue sharks and mako sharks (Appendix 2). Statistical differences were not found for mercury (p=0.986) or lead concentrations (p=0.835) between small and large blue shark specimens. A similar situation was found in mako sharks (Appendix 4).

Fig. 2.

Mercury and lead concentration found in different length individuals of blue shark off Chile, in 2011.

10.1177_194008291300600103-fig2.tif

Fig. 3.

Mercury and lead concentration found in different length individuals of Mako shortfin shark off Chile in 2011.

10.1177_194008291300600103-fig3.tif

Discussion

The significant differences of mercury and lead found in tissues/organs between blue and mako sharks are due to an organotropism phenomenon in which mercury or lead are distributed differentially in shark organs[13]. In fact, organotropism in some marine species is related to the uptake (gill, stomach, intestine) or excretion rate (liver, kidney)[24], but in sharks it is well known that heavy metals are incorporated by dietary habits in a dose-dependent manner and consequently they accumulate in the internal organs (through the blood)[13], producing the organotropism phenomenon in these predators.

All tissues of blue and mako sharks showed lower concentration of mercury and were below the limit value proposed by international organizations (1 µg·g−1) and also with other reports [151617]. In contrast, the mean lead concentration in both sharks was greater than the limit proposed by WHO/FAO and European commission (0.3 µg·g−1). A similar situation occurred in females and males of the studied sharks, with a lower mercury concentration than lead. The differences in mercury concentration found between female and male blue shark may be due to the type of food they consume, as suggested by Barrera-Garcia[12], who attributed these parameters to the differences between sexes and maturity stages, where females consume more invertebrates and males feed on fish such as mackerel.

Large size individuals of P. glauca had greater mercury and lead concentrations than small individuals. This is a well-documented process [12,13,20,25262728293031323334] known as bioaccumulation [25,28,35]. The bioaccumulation process can take different pathways, one of which is through the diet (biomagnification). Thus, the prey of small or large P. glauca and I. oxyrinchus individuals play an important role in size concentrations. In fact, the diet of these predators consists mainly of bony fishes in small individuals and squid in large specimens [3,4]; moreover, Maz-Courrau [28] found that different prey produced variable concentrations of heavy metals in blue sharks.

Risk for human consumption

Recently, the concentration of heavy metals in marine predators has been investigated because they form part of the diet of humans. In the last ten years sharks have been exploited in this region of the Pacific as target-species or by-catch [11]. Lamilla [11] identified the final destination of sharks caught in the fisheries as: sale of fins, local consumption and fishmeal. Thus the concentration of heavy metals reported in this study will constitute a risk for human health. Apparently, following the proposal by WHO/FAO, the mercury concentration will be not a problem for human consumption because it does not exceed the limit level, while lead concentration exceeded the limit value proposed by international organisms, which is 0.3 µg·g−1 wet weight, thus indicating a risk for human health. However, recent studies [44454647] showed that even though the mercury concentration is low and in an acceptable range, there are synergistic effects of mercury and lead combined in tissues. Thus the mercury may be masked by another metal, which is probably cadmium because it presents a simultaneous synergism in tissues [44,45].

Another problem detected is the indirect consumption of sharks as fish meal [11]; its principal component is the internal organs such liver or stomach. This fish meal is used to make pellet food for farm fish, which are an important item in human diet. For example, Vizzini [48] compared the levels of heavy metals between wild and farmed tuna, finding no differences in both mercury and lead concentrations. It is well known that wild tuna accumulate high concentrations of these trace metals, thus for tuna from farms we would have expected lower concentrations. The unexpectedly high metal concentrations of farm fish may be due to pellet food, which is probably made with shark internal organs. Finally, possible risks to humans from lead and its synergistic effects with mercury due to fish consumption are poorly known; they probably involve cancer (mainly gastrointestinal), neurotoxicity, immunotoxicity, cardiotoxicity, reproductive toxicity, teratogenesis and genotoxicity [36].

Implications for conservation

Sharks are apex predators in all oceans; they play an important role structuring the ecosystems which they inhabit [234]. The ecological impacts of eliminating these top predators are already indicated in the literature [49], such as predator control and induction of subsequent cascades of indirect trophic interactions [50]. Fishing pressure has disproportionately reduced abundances of these predators mainly near the coast [51], which in turn could produce the above-mentioned effects. Despite a rich ecological and fishery literature on trophic cascades, consequences of removing oceanic apex predators remain uncertain. Moreover, exploitation of large sharks (principally P. glauca and I. oxyrinchus) has been intensified worldwide in recent decades, driven by an upsurge in demand for shark fins and meat [11] and in by-catch in many fisheries. Also, data to assess direct impacts of exploitation on these large sharks are limited, but consistently indicate that they have been driven to low levels of abundance [49,50]. In fact, when fisheries affect indirectly the mean trophic levels of the large sharks, an increase begins because they feed on high trophic level prey, which produce a major accumulation of the trace metals in their tissues, which is finally consumed by human as meat and fins or indirectly as fish meal.

Acknowledgments

The authors are grateful to José Luis Vega and Dr. Mario Duque from Chemistry lab of Andres Bello University for assisting with the atomic absorption spectrophotometer, and also to Sinjun De Aguiar from the University of Nottingham for the assertive suggestions to this manuscript.

References

1.

Camhi, M., Pikitch, E.K., and Babcock, E., (2008). Sharks of the Open Ocean Biology, Fisheries and Conservation. First Edition. Oxford, UK: Blackwell. 356 pp. Google Scholar

2.

Lopez, S., Barría, P., and Meléndez, R., (2012). Feeding and trophic relationships of two highly migratory sharks in the eastern south Pacific Ocean. Pan-American Journal of Aquatic Science 7: 50–56. Google Scholar

3.

Lopez, S., Meléndez, R., and Barría, P., (2009). Feeding of the shortfin mako shark Isurus oxyrinchus Rafinesque, 1810 (Lamniformes:Lamnidae) in the Southeastern Pacific. Revista de Biología Marina y Oceanografía 44: 439–451. Google Scholar

4.

Lopez, S., Meléndez, R., and Barría, P., (2010). Preliminary diet analysis of the blue shark Prionace glauca in the eastern South Pacific. Revista de Biología Marina y Oceanografía 45: 745–749. Google Scholar

5.

Maia, A., Queiroz, N., Correia, J.P., and Cabral, H., (2006). Food habits of the shortfin mako, Isurus oxyrinchus, off the southwest coast of Portugal. Environmental Biology of Fishes 77: 157–167. Google Scholar

6.

Vaske-Júnior, T., and Rincón-Filho, G., (1998). Conteúdo estomacal dos tubarões azul (Prinace glauca) e anequim (Isurus oxyrinchus) em águas oceânicas no sul do Brasil. Revista Brasileira de Biologia 58: 445–452. Google Scholar

7.

Estrada, J., Rice, A., Lutcavage, M.E., and Skomal, G.B., (2003). Predicting trophic position in sharks of the north-west Atlantic Ocean using stable isotope analysis. Journal of the Marine Biological Association of the UK 83: 1347–1350. Google Scholar

8.

Clarke, S.C., McAllister, M.K., Milner-Gulland, E.J., Kirkwood, G.P., Michielsens, C.G., , (2006). Global estimates of shark catches using trade records from commercial markets. Ecology letters 9: 1115–1126. Google Scholar

9.

Stevens, J., (2000). The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57: 476–494. Google Scholar

10.

Acuña, E., Villarroel, J.C., and Grau, R., (2002). Fauna íctica asociada a la pesquería de pez espada (Xiphias gladius Linnaeus). Gayana 66: 263–267. Google Scholar

11.

Lamilla, J., Bustamante, C., Roa, R., Acuña, E., Concha, F., , et al. (2010). Estimación del descarte de condrictios en pesquerías artesanales. Final Report Fishery research fund number:2002-07. pp 246. Google Scholar

12.

Barrera-García, A., O'Hara, T., Galván-Magaña, F., Méndez-Rodríguez, L.C., Castellini, J.M., , et al. (2012). Oxidative stress indicators and trace elements in the blue shark (Prionace glauca) off the east coast of the Mexican Pacific Ocean. Comparative Biochemistry and Physiology Toxicology & Pharmacology 156: 59–66. Google Scholar

13.

Pethybridge, H., Cossa, D., and Butler, E., (2010). Mercury in 16 demersal sharks from southeast Australia: Biotic and abiotic sources of variation and consumer health implications. Marine Environmental Research 69: 18–26. Google Scholar

14.

Cortés, E., (2004). Life history patterns, demography, and populations dynamics. In: Biology of sharks and their relatives. Carrier, J., Musick, J., and Heithaus, M., (Eds). pp 449–469. CRC press. Florida. U.S.A. Google Scholar

15.

Official Journal of the European Communities. (2006). Commission regulation (EC) Number 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. L 364/5 Google Scholar

16.

Official Journal of the European Communities. (2008). Commission regulation (EC) Number 629/2008 of 2 July 2008 setting maximum levels for certain contaminants in foodstuffs. L 173/6 Google Scholar

17.

WHO World Health Organization. (2003). Summary and conclusions. Presented at the 61st Meeting of the Joint FAO/WHO expert committee on Food additives, Rome 10-19 June 2003. Google Scholar

18.

Storelli, M., Garofalo, R., Giungato, D., and Giacominelli-Stuffler, R., (2010). Intake of essential and nonessential elements from consumption of octopus, cuttlefish and squid. Food Additives and Contaminants: Part B 3: 14–18. Google Scholar

19.

Harada, M., (1995). Minamata disease: methylmercury poisoning in Japan caused by environmental pollution. Critical Reviews in Toxicology 25: 1–24. Google Scholar

20.

Branco, V., Vale, C., Canário, J., and Santos, M., (2007). Mercury and selenium in blue shark (Prionace glauca, L. 1758) and swordfish (Xiphias gladius, L. 1758) from two areas of the Atlantic Ocean. Environmental Pollution 150: 373–380. Google Scholar

21.

Gutleb, A., Kranz, A., Nechay, G., and Toman, A., (1998). Heavy metal concentrations in livers and kidneys of the otter (Lutra lutra) from Central Europe. Bulletin of environmental contamination and toxicology 60: 273–279. Google Scholar

22.

Gutleb, A., Helsberg, A., and Mitchell, C., (2002). Heavy metal concentrations in fish from a pristine rainforest valley in Peru: a baseline study before the start of oil-drilling activities. Bulletin of Environmental Contamination and Toxicology 69: 523–529. Google Scholar

23.

R development core team.(2011) R: A language and environment for statistical computing. R foundation for statistical computing. Vienna, Austria. Google Scholar

24.

Boening, D.W., (2000). Ecological effects, transport, and fate of mercury: a general review. Chemosphere 40: 1335–1351. Google Scholar

25.

Escobar-Sánchez, O., Galván-Magaña, F., and Rosíles-Martínez, R., (2011). Biomagnification of mercury and selenium in blue shark Prionace glauca from the Pacific Ocean off Mexico. Biological Trace Element Research 144: 550–559. Google Scholar

26.

Endo, T., Hisamichi, Y., Haraguchi, K., Kato, Y., Ohta, C., , et al. (2008). Hg, Zn and Cu levels in the muscle and liver of tiger sharks (Galeocerdo cuvier) from the coast of Ishigaki Island, Japan: relationship between metal concentrations and body length. Marine Pollution Bulletin 56: 1774–1780. Google Scholar

27.

Hurtado-Banda, R., Gomez-Alvarez, A., Márquez-Farías, J.F., Cordoba-Figueroa, M., Navarro-García, G., , et al. (2012). Total mercury in liver and muscle tissue of two coastal sharks from the northwest of Mexico. Bulletin of Environmental Contamination and Toxicology 88: 971–975. Google Scholar

28.

Maz-Courrau, A., López-Vera, C., Galván-Magaña, F., Escobar-Sánchez, O., Rosíles-Martínez, R., , et al. (2012). Bioaccumulation and biomagnification of total mercury in four exploited shark species in the Baja California Peninsula, Mexico. Bulletin of Environmental Contamination and Toxicology 88: 129–134. Google Scholar

29.

Burger, J., Campbell, K.R., Murray, S., Campbell, T.S., Gaines, K.F., , et al. (2007). Metal levels in blood, muscle and liver of water snakes (Nerodia spp.) from New Jersey, Tennessee and South Carolina. The Science of the total environment 373: 556–563. Google Scholar

30.

Stevens, J.D., and Brown, B.E., (1974). Occurrence of heavy metals in the blue shark Prionace glauca and selected pelagic in the N.E. Atlantic Ocean. Marine Biology 293: 287–293. Google Scholar

31.

Branco, V., Canário, J., Vale, C., Raimundo, J., and Reis, C., (2004). Total and organic mercury concentrations in muscle tissue of the blue shark (Prionace glauca L.1758) from the Northeast Atlantic. Marine pollution bulletin 49: 871–874. Google Scholar

32.

Kaneko, J.J., and Ralston, N.V., (2007). Selenium and mercury in pelagic fish in the central north pacific near Hawaii. Biological trace element research 119: 242–254. Google Scholar

33.

Nam, D-H., Adams, D.H., Reyier, E.A., and Basu, N., (2011). Mercury and selenium levels in lemon sharks (Negaprion brevirostris) in relation to a harmful red tide event. Environmental monitoring and assessment 176: 549–559. Google Scholar

34.

Lozano, G., Brito, A., Hardisson, A., Gutiérrez, A., González-Weller, D., , et al. (2009). Content of lead and cadmium in barred hogfish, Bodianus scrofa, island grouper, Mycteroperca fusca, and Portuguese dogfish, Centroscymnus coelolepis, from Canary Islands, Spain. Bulletin of environmental contamination and toxicology 83: 591–594. Google Scholar

35.

Maz-Courrau, A., and López-Vera, C., (2006). Biomagnificación y bioacumulación de mercurio en cuatro especies de tiburón de la península de Baja California Sur, Mexico. Bachelor's thesis. Jorge Tadeo Lozano University, Bogotá Colombia. pp 77. Google Scholar

36.

González, M.A., Vivanco, M.G., Palomino, I., Garrido, J.L., Santiago, M., , et al. (2012). Modelling Some Heavy Metals Air Concentration in Europe. Water, Air, & Soil Pollution in press. Google Scholar

37.

Vas, P., (1991). Trace metal levels in sharks from British and Atlantic waters. Marine pollution bulletin 22: 67–72. Google Scholar

38.

Storelli, M.M., Stuffler, R., and Marcotrigiano, G.O., (2001) Total mercury and methylmercury in tuna fish and sharks from the South Adriatic Sea. Italian Journal of Food Science 1: 101–106. Google Scholar

39.

Davenport, S.R., (1995). Mercury in blue sharks and deepwater dogfish from around Tasmania. Australian Fish 54: 20–24. Google Scholar

40.

Dias, A., Guimaraes, J., Malm, O., and Costa, P., (2008). Total mercury in muscle of the shark Prionace glauca (Linnaeus, 1758) and swordfish Xiphias gladius Linnaeus, 1758, from the South-Southeast coast of Brazil and the implications from public health. Cadernos de Saude Publica 24: 2063–2070. Google Scholar

41.

Velez, M., (2009). Indicadores de estrés oxidativo relacionados con la presencia de elementos traza (plomo, cadmio, mercurio y arsénico) en diferentes tejidos del tiburón mako (Isurus oxyrinchus). Masther thesis. CIBNOR, La Paz, Mexico. pp 76. Google Scholar

42.

Vlieg, P., Murray, T., and Body, D., (1993). Nutritional data on six oceanic pelagic fish species from New Zealand waters. Journal of Food Composition and Analysis 6: 45–54. Google Scholar

43.

Menasveta, P., and Siriyong, R., (1977). Mercury content of several predacious fish in the Andaman Sea. Marine pollution bulletin 8: 200–204. Google Scholar

44.

Wang, L., Jianji, L., Jingui, L., and Zongping, L., (2010). Effects of Lead/and/or Cadmium of the Oxidative damage of rat kindnay cortex mitochondria. Biological Trace Element Research 137: 69–78 Google Scholar

45.

Traoré, A., Bonini, M., and Creppy, E., (1999). Synergistic effects of some metals contaminating mussels on the cytotoxicity of the marine toxin okadaic acid. Archives of Toxicology 73: 289–295 Google Scholar

46.

Sá, I., da Costa, M.J.P., and Cunha, E.M., (2012). Lead hepatotoxicology: A study in an animal model. Toxicology and Industrial Health 28(2): 108–113 Google Scholar

47.

Papp, A., Pecze, L., Szabó, A., and Vezér, T., (2006). Effects on the central and peripheral nervous activity in rats elicited by acute administration of lead, mercury and manganese, and their combinations. Journal of Applied Toxicology 26: 374–380 Google Scholar

48.

Vizzini, S., Tramati, C., and Mazzola, A., (2010). Comparison of stable isotope composition and inorganic organic contaminant levels in wild and farmed bluefin tuna, Thunnus thynnus, in the Mediterrean Sea. Chemosphere 78: 1236–1243. Google Scholar

49.

Myers, R., Baum, J., Sheperd, T., Powers, S., and Peterson, Ch, . (2007). Cascading effects of the loss of apex predatory sharks from a coastal Ocean. Science 315: 1846–1850. Google Scholar

50.

Baum, J., and Worm, B., (2009). Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology 78: 699–714. Google Scholar

51.

Lack, M., and Sant, G., (2009). Trends in global shark catch and recent developments in management. TRAFFIC: the wildlife trade-monitoring network. Final report. pp 33. Google Scholar

Appendices

Appendix 1.

Summary data of heavy metal concentrations (µg·g−1 w.w.) in different tissues of blue and mako shortfin shark in different oceans. Mean ± standard deviation.

10.1177_194008291300600103-table1.tif

Appendix 2.

Mean concentration of Hg and Pb by sexes and size of Prionace glauca and Isurus oxyrinchus off Chile during 2011. BS: Blue shark (Prionace glauca) and MSf: Mako shortfin shark (Isurus oxyrinchus). Ss: Small size and Ls: Large size.

10.1177_194008291300600103-table2.tif

Appendix 3. Differences in mercury and lead between males-females of P. glauca and I. oxyrinchus off Chile in 2011. Above the diagonal are p-values for Hg and below the diagonal is Pb from one-way ANOVA analysis.

10.1177_194008291300600103-table3.tif

Appendix 4. Differences between small and large size of P. glauca and I. oxyrinchus individuals off Chile in 2011. Above the diagonal are p-values for Hg and below the diagonal is Pb from one-way ANOVA analysis.

10.1177_194008291300600103-table4.tif
© 2013 Sebastián A. Lopez, Nicole L. Abarca and Roberto Meléndez C. This is an open access paper. We use the Creative Commons Attribution 3.0 license http://creativecommons.org/licenses/by/3.0/ - The license permits any user to download, print out, extract, archive, and distribute the article, so long as appropriate credit is given to the authors and source of the work. The license ensures that the published article will be as widely available as possible and that the article can be included in any scientific archive. Open Access authors retain the copyrights of their papers. Open access is a property of individual works, not necessarily journals or publishers.
Sebastián A. Lopez, Nicole L. Abarca, and Roberto C. Meléndez "Heavy metal concentrations of Two highly migratory sharks (Prionace glauca and Isurus Oxyrinchus) in the southeastern Pacific waters: comments on public health and conservation," Tropical Conservation Science 6(1), 126-137, (18 March 2013). https://doi.org/10.1177/194008291300600103
Received: 28 September 2012; Accepted: 3 January 2013; Published: 18 March 2013
JOURNAL ARTICLE
12 PAGES


SHARE
ARTICLE IMPACT
Back to Top