The purpleback flying squid Sthenoteuthis oualaniensis (Lesson, 1830) is landed in small quantities along the northwest coast of India. Keeping in view the possibility of utilization of this species for domestic and export markets, the cadmium accumulation in the body tissues, which often causes concern, was studied. The dorsal mantle length of male and female observed during the study ranged from 34 to 47 cm and 30 to 32 cm respectively. The highest mean concentration of 435.22 ± 61.27 μg g-1 (mean ± S.E.) of Cd was found in the liver. Accumulation of Cd was also prominent in the gut, gills and skin. Moderate concentration

of Cd (1 to 4 μg g-1) was observed in the nidamental gland, accessory nidamental gland, eyes, tentacles and muscle. In the gonads and arms, the concentration was below the acceptability level of 1.0 μg g-1. Higher accumulation in most of the organs/tissues of larger squids was observed. Significantly higher accumulation (p < 0.05) was noticed in the liver of larger specimens, indicating bioaccumulation. As the mean Cd content in the edible part was more than 1.0 μg g-1, this study highlights the need for detailed

investigations to understand the bioaccumulation of Cd in Sthenoteuthis oualaniensi

Asokan, P K

Badonia, Rajendra

Das, Shibsankar

Ghosh, Shubhadeep

Madhu, V R

Murthy, Narasimha L

Panda, Satyen Kumar

CMFRI Digital Repository

191Journal of the Marine Biological Association of India (2008)Cadmium content in the purpleback flying squidJ. Mar. Biol. Ass. India, 50 (2) : 191 - 195, July - December 2008IntroductionOceanic squids belonging to the familyOmmastrephidae are large nektonic predators foundmostly in the tropical seas. The Indo-Pacificpurpleback squid Sthenoteuthis oualaniensis(Lesson, 1830) representing this family is widelydistributed in the tropical Indian and Pacific oceanswith the productive areas located in 18–22oSnorthward of Indian Ocean and between 20–25oNand 16–20oS of Pacific Ocean (Aravindakshan andSakthivel, 1973; Zuyev et al., 2002). Due to theirhuge biomass and nutritional value, they areprospective subject for open ocean fisheriesinvestigations. This species appears to have aplastic phenotype and has adapted to the ArabianSea conditions by evolving the capacity to grow toa giant size (Snÿder, 1998). The population densityin this region is estimated to be about 0.9-1.6 x106 t (Zuyev et al., 2002). Soviet investigations oncephalopod resources in the Arabian Sea haverevealed absolute dominance in numbers andbiomass of this species in the epipelagic region(Chesalin and Zuyev, 2002).In recent years, with the expansion of fishingto the deeper waters, gradual increase in thelandings of this species is observed along thenorthwest coast of India, especially in the Gujaratregion. Raje and Savaria (1987) have reportedlanding of S. oualaniensis from Saurashtra coast ofGujarat. Recently, Mohamed et al. (2006) havedescribed the population characteristics and someaspects of biology of the purpleback squid landedCadmium in the purpleback flying squid Sthenoteuthis oualaniensis (Lesson,1830) along northwest coast of India*L.  Narasimha Murthy, Satyen Kumar Panda, V. R. Madhu, 1P. K. Asokan,1Shubhadeep Ghosh, Shibsankar Das and Rajendra BadoniaVeraval Research Centre of Central Institute of Fisheries Technology, MatsyaBhavan,Bhidia, Veraval-362 269, Gujarat, India.1Veraval Regional Centre of Central Marine Fisheries Research Institute, Matsya Bhavan, Bhidia, Veraval-362 269, Gujarat, India.* E-mail: murthycift@gmail.comAbstractThe purpleback flying squid Sthenoteuthis oualaniensis (Lesson, 1830) is landed in small quantities alongthe northwest coast of India. Keeping in view the possibility of utilization of this species for domestic andexport markets, the cadmium accumulation in the body tissues, which often causes concern, was studied.The dorsal mantle length of male and female observed during the study ranged from 34 to 47 cm and 30 to32 cm respectively. The highest mean concentration of 435.22 ± 61.27 µg g-1 (mean ± S.E.) of Cd wasfound in the liver. Accumulation of Cd was also prominent in the gut, gills and skin. Moderate concentra-tion of Cd (1 to 4 µg g-1) was observed in the nidamental gland, accessory nidamental gland, eyes, tentaclesand muscle. In the gonads and arms, the concentration was below the acceptability level of 1.0 µg g-1.Higher accumulation in most of the organs/tissues of larger squids was observed. Significantly higheraccumulation (p < 0.05) was noticed in the liver of larger specimens, indicating bioaccumulation. As themean Cd content in the edible part was more than 1.0 µg g-1, this study highlights the need for detailedinvestigations to understand the bioaccumulation of Cd in Sthenoteuthis oualaniensis.Keywords:  Purpleback flying squid, cadmium, tissue, liver192Journal of the Marine Biological Association of India (2008)L. Narasimha Murthy et al.at Cochin. As there is lack of knowledge onprocessing, this oceanic squid remains under-utilized.In the last decade, there has been a concern onthe cadmium accumulation in cephalopods andthere are instances of rejection of seafoodconsignments exported from India because of Cdlevels beyond the EU prescribed limit. Squids areknown to accumulate Cd from water and foodsources and hence constitute an important sourceof Cd for cephalopod predators and act as vectorin the biomagnification process (Bustamante etal., 1998). In squids such as Loligo duvauceli andDoryteuthis sibogae harvested from Indian waters,the mean Cd concentration in the edible parts isfound to be within the maximum residual levelsprescribed by the EU and USFDA (Prafulla et al.,2001; Sivaperumal et al., 2007). In cephalopods adifferential accumulation of heavy metals indifferent tissues is reported (Martin and Flegel,1975; Finger and Smith, 1987). In S. oualaniensisfrom Japanese waters, high cadmium content of1106 µg. g dry weight-1 has been reported from thedigestive glands (Kurihara et al., 1993). There isno data on the cadmium content of S. oualaniensis,which is now emerging as a fishery along thenorthwest coast of India. This study attempts tounderstand the organ/tissue specific accumulationof cadmium in S. oualaniensis landed at Veraval,India.Material and methodsSquid samples: The purpleback flying squid islanded by multiday trawlers along the northwestcoast of India, especially by those venturing to themid-Arabian Sea or closer to the Oman coast. Squidsamples were collected from fishing boats operatingfrom Veraval, Gujarat during September 2007 –February 2008. Species identification was basedon descriptions of Roper et al. (1984) and Silas(1986). Biometric measurements such as dorsalmantle length (DML; in cm) and weight (g) forindividual squids were recorded and a total of 30individuals were used for this study. After initialrinsing with seawater, the samples were sealed inpolyethylene bags and kept frozen at -20°C untilfurther analyses. The samples were thawed anddissected on a clean polypropylene board and allindividual organs were separated and storedseparately. Muscle (edible part), tentacles, arms,gills, accessory nidamental gland, nidamentalglands, skin, liver, eyes, gut and gonads were usedfor studying the cadmium concentration.Cadmium content analysis: Samples weredigested in teflon containers using a microwavedigester (Ethos plus High Performance MicrowaveLabstation, Milestone, USA). Tissues werehomogenized, 3g of wet tissue was weighed into100 ml teflon vials and digested overnight with 7ml of pure nitric acid (AR grade, specific gravity:1.38, Qualigens, India) and 3ml of hydrogenperoxide. The microwave parameters were 700Wpower for one hour (40 minute heating and 20minute ventilation). The digested contents weretransferred to acid washed polypropylene bottlesand made up to 25 ml with double distilled waterand subjected to Cd analysis in Atomic AbsorptionSpectrophotometer (GBC 932AA, GBC ScientificInstruments, Australia) by following the AOACmethod (AOAC, 2000).Statistical analyses: One way ANOVA wascarried out on log-transformed data onconcentration of Cd in the tissues and thesignificance was tested at 95% confidence level.Whenever significant differences were found,Tukey’s posthoc test was used to differentiatebetween the tissue/organs. Regression analysis wascarried out between cadmium concentrations andorgan/tissue and for all the samples to find outtrend in the accumulation pattern with increase inthe size of the individuals. All the statisticalanalyses were carried out using SPSS software(Version 16.0) (SPSS Inc., USA).Results and DiscussionThe dorsal mantle length ranged between 34-47 cm for males and 30-32 cm for females of S.oualaniensis. In earlier studies, the maximum DMLfor this species has been reported to be 35.0 cm forunsexed specimens (Roper et al., 1984), 62.0 cmfor female and 32.0 cm for male (Zuyev et al.,2002). The DML ranges reported by Mohamed etal. (2006) from the southern Arabian Sea was 22-47 mm. Chesalin et al. (1995) reported giant193Journal of the Marine Biological Association of India (2008)Cadmium content in the purpleback flying squidArabian form with mantle length (ML) 24–32 cm(male) and 30–63 cm (female). Xinjun et al. (2007)observed mean mantle length of 30 cm for males(range: 10.6–46.2 cm) and 35 cm for females (range:10.6–61.2 cm).The concentration of Cd in different organs/tissue of S. oualaniensis is presented in Table 1.The highest mean Cd concentration of 435.22 µgg-1 was found in the liver, which ranged from110.42 to 900.76 µg g-1. High concentrations ofheavy metals in the liver (also known as digestivebody burden at the end of the exposure period of14 days. The liver of Sthenoteuthis oualaniensisaccumulating 79 µg. g wet weight-1 (Ichihashi etal., 2001) and 780 µg. g dry weight-1 (Martin andFlegal, 1975) of Cd has been reported. The protein-bound Cd   has been reported to accumulate in theliver of the squid, T. pacificus (Tanaka et al., 1983;Dohi et al., 1986). The protein-bound nature ofCd, as reported in the earlier studies, may be thereason for the high concentration of the metal inthe liver.Table 1. Cadmium concentration in the organ tissue of  Sthenoteuthis oualaniensis (n = 30)Organ/Tissue Concentration (µg/g wet weight)Mean ± SD Minimum MaximumMuscle (edible part) 1.44 ± 0.29a,b,c 0.26 5.26Tentacles 1.48 ± 0.30b,c,d 0.50 4.17Arms 0.84 ± 0.22a,b 0.27 4.32Gills 8.92 ± 0.95e 2.95 18.42Accessory nidamental gland 1.17 ± 0.24a,b 0.15 4.57Nidamental gland 3.67 ± 0.76d 0.95 12.71Skin 7.96 ± 0.46e 4.62 13.95Liver 435.22 ± 61.27f 110.42 900.76Eyes 2.94 ± 0.60c,d 0.47 8.74Gut 18.66 ± 3.91e 1.16 47.14Gonads 0.86 ± 0.24a 0.04 1.86a,b,c,d,e,f Values with different superscripts are significantly different at P<0.05gland, hepatopancreas or mid-gut gland) ofommastrephid squids have been reported earlier(Martin and Flegal, 1975; Smith et al., 1984). Inother cephalopods, such as the cuttlefish Sepiaofficinalis and the octopus, Eledone cirrhosa,caught along the French coast, the liver containedthe highest Cd concentration among the organs(Miramand and Bently, 1992). In a recent study,the highest mean cadmium concentration of 1002.9µg g-1 (wet weight) was observed in the digestivegland of sexually mature Argentine short-finnedsquids (Illex argentinus) (Dornless et al., 2007). Ina bioaccumulation study, Koyama et al. (2000)observed that the liver of the oval squidSepioteuthis lessoniana exhibited the highest Cdconcentration (49.3 µg. g ww-1) and had the highestproportion of Cd content (42.8%) to the whole-The mean Cd concentration in the gut ofSthenoteuthis oualaniensis was 18.66 ± 3.91 µgg-1. Higher concentration of Cd in the intestinemay be due to the occurrence of organisms withhigh Cd level in the diet and also may be due tofrequent cannibalistic tendency of this species(Chesalin, 1994).In the UK waters, the concentration of Cd wasgenerally higher in the ommastrephids in all thetissues except the muscle (Pierce et al., 2008). Inour study, the maximum Cd content in the musclewas 5.26 µg g-1, which is above the prescribedlimit for export to EU (EC, 2006) and USA.Posthoc comparison by one-way ANOVA indifferent organs of Sthenoteuthis oualaniensisshowed that the concentration of Cd in the liver194Journal of the Marine Biological Association of India (2008)L. Narasimha Murthy et al.was significantly different from other organs (p <0.05). Skin, gills and gut accumulated moderate tohigh levels of Cd which was significantly higherthan the rest of the organs/tissues.Regression analysis of Cd concentration indifferent size showed that the concentration waspositively correlated in the case of liver (p < 0.05,r2 = 0.71). Cd in other tissues did not showsignificant trend with increase in size. However,the concentration in most of the organs was higherin larger squids.Higher Cd content in most of the organs ofsquids of larger size may be due to the differentialfeeding pattern with growth. The juveniles mostlydevour upon meso and macroplanktonicinvertebrates such as the copepods, amphipods andeuphausiids, whereas the adults prey uponmicronektonic and nektonic organisms such as themyctophids, flyingfishes and squids that maycontain higher Cd level in their tissues (Zuyev etal., 2002). Ichihasi et al. (2001) reported a similartrend of higher Cd level in the liver of the adultSthenoteuthis oualaniensis (79.1 µg g-1) comparedto juveniles (20.8 µg g-1). The result of this studyalso shows higher concentrations of Cd in the liver(539.9 µg g-1) in 40-50 cm group, than the meanconcentrations in 30-40 cm group (185.9 µg g-1).The present study shows that the Cd is presentin the body parts of  S. oualaniensis and theconcentrations are above the maximum permissiblelimit of 1 ppm for export to the EU countries andUSA. Hence, the utilization of the purpleback flyingsquid landed along Gujarat coast for humanconsumption needs a cautious approach. Factorslike seasonality, metabolic and trophic changesduring different life stages, which may alter theaccumulation of cadmium, needs furtherinvestigations.AcknowledgementsThe authors wish to express their sincere thanksto the Director, CIFT, Cochin for accordingpermission to publish this paper. The technicalassistance rendered by the staff of Fish ProcessingSection, CIFT, Veraval and Regional Centre ofCMFRI is gratefully acknowledged.ReferencesAOAC. 2000. Determination of Lead, Cadmium, Copper,Iron and Zinc in foods. Association of OfficialAnalytical Chemists, Official Method 999.10. Ch. 9, p. 19.Aravindakshan, P. N. and M. Sakthivel. 1973. The locationof cephalopod nurseries in the Indian Ocean.International Indian Ocean Expedition, Handbook tothe International Zooplankton Collections. IndianOcean Biological Centre, 5: p. 70-75.Bustamante, P. C., F. S. W. Fowler and P. Miramand. 1998.Cephalopods as a vector for the transfer of cadmiumto top marine predators in the north-east AtlanticOcean. The Science of the Total Environment, 220(1): p. 71-80.Chesalin, M. V. 1994. Feeding of oceanic squids of genusSthenoteuthis and their role in trophic structure ofpelagic communities. Abstr. Can. Biol. Sci. Thesis.Institute of Biology of the Southern Seas, NationalUkrainian Academy of Sciences, Sevastopol, 24 pp.Chesalin, M. V., G. V. Zuyev and V. N. Nikolsky. 1995.Squid Sthenoteuthis oualaniensis (Cephalopoda:Ommastrephidae) is the “master” of the Arabian Sea.Abstr. Commun. 12th Int’l. Malacol. Congr., Vigo(Spain), 3–8 Sept. 1995: p.161–162.Table 2. Cadmium concentration (µg g-1) in the organ/tissue of Sthenoteuthis oualaniensis of differentlength class (n = 30); the values are mean ± SD.NA refers not availableOrgan/Tissue Length (cm)30-40 40-50Muscle (edible part) 1.38 ± 0.42 1.46 ± 0.37Tentacles 1.9 ± 1.07 1.38 ± 0.29Arms 0.65 ± 0.07 0.93 ± 0.32Gills 08.21 ± 0.44 9.20 ± 1.33Accessorynidamental gland 0.76 ± 0.07 1.33 ± 0.33Nidamental gland 2.04 ± 0.380 4.49 ± 1.07Skin 9.17 ± 1.19 7.47 ± 0.41Liver 185.98 ± 33.49 534.92 ± 69.74Eyes 2.62 ± 0.42 3.10 ± 0.89Gut 28.32 ± 4.08 13.82 ± 5.03Gonads NA 0.86 ± 0.24195Journal of the Marine Biological Association of India (2008)Cadmium content in the purpleback flying squidChesalin, M. V.  and G. V. Zuyev. 2002. Pelagiccephalopods of the Arabian Sea with an emphasis onSthenoteuthis oualaniensis. Bull. Mar. Sci., 71(1): 209-221.Dohi, Y., K. Kosaka, K. Ohba and Y. Yoneyama. 1986.Cadmium-binding proteins of three marine molluscsand characterization of two cadmium-bindingglycoproteins from the hepatopancreas of a whelk,Buccinum tenuissium. Environmental HealthPerspective, 65: 49-55.Dorneles, P. R.,  J. Lailson-Brito, R. A. dos Santos, P. A.S. da Costa, O. Malma, , A. F. Azevedo and J. P. M.Torres. 2007. Cephalopods and cetaceans as indicatorsof offshore bioavailability of cadmium off CentralSouth Brazil Bight. Environmental Pollution, 148(1):352-359.EC, 2006. Commission regulation (EC) No. 1881/2006 of19 Dec. 2006 setting maximum levels for certaincontaminants in foodstuffs. Official Journal ofEuropean Union, L364: 5-24.Finger, J. M. and J. D. Smith. 1987. Molecular associationof Cu, Zn, Cd and 210 Po in the digestive gland ofsquid Notodarus gouldi. Mar. Biol., 95: 87-91.Ichihashi, H., Y. Nakamura, K. Kannan, A. Tsumura andS. Yamasaki. 2001. Multi-elemental concentrations intissues of Japanese common squid (Todarodespacificus).  Arch. Environ. Contam. Toxicol., 41: 483–490.Koyama, J., N. Nanamori, and S. Segawa. 2000.Bioaccumulation of waterborne and dietary cadmiumby oval squid, Sepioteuthis lessoniana, and itsdistribution among organs. Mar. Pollut. Bull., 40(11):961-967.Kurihara, H., H. Togawa and M. Hatano. 1993.Concentration of cadmium in livers of several kindsof squids and approach to its elimination. Bull. Fac.Fish, Hokkaido Univ., 44: 32-38.Martin, H. and A. R. Flegal. 1975. High copperconcentrations in squid livers in association withelevated levels of silver, cadmium and zinc. Mar.Biol., 30: 51-55.Miramand, P. and D. Bently. 1992. Concentration anddistribution of heavy metals in tissues of twocephalopods, Elodone cirrhosa and Sepia officinalisfrom the French coast of the English Channel. Mar.Biol., 114: 407-414.Mohamed, K. S., M. Joseph and P. S.Alloycious. 2006.Population characteristics and some biology of theoceanic squid  Sthenoteuthis oualaniensis Lesson,(1830). J. Mar. Biol. Ass. India, 48(2): 256-259.Pierce, G. J., G. Stowasser, L. C. Hastie and P.  Bustamante.2008. Geographic, seasonal and ontogenetic variationin cadmium and mercury concentrations in squid(Cephalopoda: Teuthoidea) from UK waters.Ecotoxicology and Environmental Safety, 70: 422-432.Prafulla, V., L. Francis and P. T. Lakshmanan. 2001.Concentrations of trace metals in the squids, Loligoduvauceli and Doryteuthis sibogae caught from thesouthwest coast of India. Asian Fisheries Science, 14:399-410.Raje, S. G. and Y. D. Savaria. 1987. Record of the oceanicsquid Symplectoteuthis oualaniensis (Lesson) caughtoff Mangrol, Saurashtra coast. Indian J. Fish., 34:233–235.Roper, C. F. E., M. J. Sweeney and C. E. Nauen. 1984.Cephalopods of the world. Food and AgricultureOrganization, Rome, Italy, 3: 277 pp.Silas, E. G. 1986. Cephalopod bionomics, fisheries andresources of the Exclusive Economic Zone of India.Bull. Cent. Mar. Fish. Res. Inst., 37: 195 pp.Sivaperumal, P., T. V. Sankar and P. G. V.  Nair. 2007.Heavy metal concentrations in fish, shellfish and fishproducts from internal markets of India vis-a-visinternational standards. Food Chemistry, 102 (3): 612-620.Smith, J. D., L. Plues, M. Heyraud and  R. D. Cherry.1984. Concentrations of the elements Ag, Al, Ca, Cd,Cu, Fe, Mg, Mn, Pb and Zn, and the radionuclides210Pb and 210Po in the digestive gland of the squid.Mar. Env. Res., 13: 55-68.Snÿder, R. 1998. Aspects of the biology of the giant formof Sthenoteuthis oualaniensis (cephalopoda:ommastrephidae) from the Arabian Sea. FisheriesResearch, 83 (1): 98-104.Tanaka, T., Y. Hayashi and M. Ishizawa.1983. Subcellulardistribution and binding of heavy metals in theuntreated liver of the squid, comparison with datafrom the liver of cadmium and silver-exposed rats.Experientia, 39: 746-748.Xinjun, C., L. Bilina, T. Siquana, Q. Weiguoa andZ. Xiaohua. 2007. Fishery biology of purplebacksquid, Sthenoteuthis oualaniensis, in the northwestIndian Ocean. Fisheries Research, 83 (1): 98-104.Zuyev, G., C. Nigmatullin, M. Chesalin and K. Nesis.2002. Main results of long-term worldwide studies ontropical nektonic oceanic squid genus Sthenoteuthis:An overview of the Soviet investigations. Bull. Mar.Sci., 71(2): 1019–1060.Received: 24 September 2008Accepted: 22 December 2008

Cadmium in the purpleback flying squid Sthenoteuthis oualaniensis (Lesson, 1830) along northwest coast of India

http://eprints.cmfri.org.in/2155/1/Murty_191-195.pdf

Cadmium in the purpleback flying squid Sthenoteuthis oualaniensis (Lesson, 1830) along northwest coast of India

Abstract

Similar works

Full text

Available Versions

CMFRI Digital Repository