Fish Physiology and Biochemistry 26: 171–175, 2002.© 2003 Kluwer Academic Publishers. Printed in the Netherlands.

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The liver lipid fatty acid profiles of seven Indian Ocean shark species

Bruce Davidson1 and Geremy Cliff2

1Department of Physiology, Wits Medical School, University of the Witwatersrand, Johannesburg, South Africa(Phone: +27 11 717 2464; Fax: +27 11 643 2765; E-mail: davidsonbc@physiology.wits.ac.za) 2Natal SharksBoard, Umhlanga, South Africa

Accepted: June 6, 2003

Key words: elasmobranch, hepatic oils

Abstract

We have assessed the fatty acid profiles of the livers from seven shark species (Carcharias taurus (raggedtooth/greynurse), Carcharhinus limbatus (blacktip), Carcharhinus obscurus (dusky), Carcharhinus leucas (Zambezi/bull),Sphyrna lewini (scalloped hammerhead), Carcharhinus brevipinna (spinner), and Galeocerdo cuvieri (tiger)) foundoff the east coast of South Africa. While there was generally little variation between the species, Carcharias taurusshowed fatty acid profiles that would be most favourable in human nutrition, in that it showed both low saturated(SFA) (37.1%) and high polyunsaturated fatty acid (PUFA) (26.6%) levels. However, all species showed profilesrich in PUFA, thus utilising the liver oil from sharks caught as part of the bycatch when fishing for teleost specieswould avoid unnecessary wastage of a potentially valuable resource.

Introduction

In many instances, commercial fishing for teleost spe-cies also produces a bycatch of sharks, most of whichare discarded after removal of the fins for sale on theoriental market. However, there is evidence that sharkliver is rich in oil (Nichols et al. 1998, 2001; Weth-erbee and Nichols 2000), which may be suitable as asource of the n3 polyunsaturates (n3 PUFA) reputedto be beneficial in the prevention of cardiac diseasein humans (al Makdessi et al. 1994; Murphy et al.1997). To date the data available on the liver fattyacids of the sharks that occur in coastal waters aroundAfrica is scant (Banjo, 1979; Peyronel et al. 1984),although the liver oil from West African sharks hasbeen shown to be composed largely of triacylglycer-ols, alkyldiacylglycerols and hydrocarbons (Sargentet al. 1973).

The Indian Ocean coastline of South Africa isunique in several respects. Firstly, the waters are sub-tropical to tropical; secondly, the continental shelf isnarrow, compressing nearshore fish species into a nar-row coastal strip; third, the infrastructure along thecoast is highly developed in some places while still

undeveloped in others, allowing for a natural ecologyto predominate, but with easy access to the facilitiesnecessary for research. This coastline is the home tomany species of shark, and some of these have thereputation of being dangerous to humans (Cliff andWilson 1986). As a direct result of shark attack theNatal Sharks Board (NSB) was established to protectthe tourism industry, and the main mechanism em-ployed to reduce the incidence of shark attack was theplacing of nets off the coastline to catch large sharks(Cliff and Wilson 1986). This practice has been inplace since 1952 and the NSB have developed data-bases for the sharks most commonly found off theKwaZuluNatal coast, and data reflecting the averageannual catch, body mass and liver mass is shown inTable 1. At the same time, it routinely collects samplematerial from sharks caught in the nets, and makesthese available to investigators wishing to carry outanalyses.

In this study we report the results of analysisof the fatty acids found in the total lipid fractionsfrom the livers of shark species found in this coastalregion and commonly caught in the nets. The spe-cies selected for inclusion were those where sample

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Table 1. Average annual catch, body mass and liver mass for the seven shark species during 1997–2001

Species Average annual catch Average body mass (kg) Average liver mass (kg)

Raggedtooth(grey nurse) 124 124 12

Blacktip 67 60 4

Dusky 192 89 10

Zambezi(bull) 26 80 9

Scalloped hammerhead 70 38 3

Spinner 115 80 8

Tiger 38 112 16

numbers allowed for statistical analysis of the data,namely Carcharias taurus (raggedtooth/grey nurse),Carcharhinus limbatus (blacktip), Carcharhinus ob-scurus (dusky), Carcharhinus leucas (Zambezi/bull),Sphyrna lewini (scalloped hammerhead), Carchar-hinus brevipinna (spinner), and Galeocerdo cuvieri(tiger). This study was an initial attempt to assess thevalue of the livers from a range of species of sharksrelatively common off the east coast of South Africa.

Materials and methods

Details of the netting operation to protect the pop-ular swimming beaches of KwaZuluNatal are givenby Cliff and Dudley (1992). Sharks caught in thenets were taken to the laboratories of the NSB, wherethe carcasses were dissected and approximately 20 gsamples collected from the livers, placed into labelledglass vials and frozen at −20 ◦C. For this study freshmaterial was needed to avoid the possible deteriorationof the lipids, especially the PUFA, hence only newlycaught sharks were sampled.

The samples were taken to the University of theWitwatersrand where the lipids were extracted (Blighand Dyer 1959). A 1ml aliquot of each extract wasthen used to determine the lipid dry weight, and a fur-ther aliquot approximating to 20 mg of lipid was trans-methylated using 10% boron trifluoride in methanolto prepare methyl esters of the fatty acids (Moscatelli1972). These were then extracted into hexane, and themethyl esters separated using a Varian 3400 gas chro-matograph, with a 10% SP2330 packed column andFID detection, and quantitated using a Varian 4270integrator.

Results

The results of the analyses are shown in Table 2.In general there was a high degree of conformitybetween the species, both at the level of the indi-vidual fatty acids and when these were summed intoclasses of fatty acids. However, there were some dif-ferences between the species. The raggedtooth (greynurse) and scalloped hammerhead showed the low-est total saturated fatty acids (SFA) (37.1%, 36.2%),while the blacktip showed the highest (43.8%). Theraggedtooth, blacktip and dusky also showed thehighest levels of both arachidonic acid (20:4n6) (5.2%,4.8%, 4.9%) and total n6 polyunsaturates (n6 PUFA)(8.7%, 9.0%, 8.6%), while the scalloped hammer-head showed the lowest total n6 PUFA (4.4%). Boththe raggedtooth and the spinner showed the greatestamounts of total n3 PUFA (17.9%, 19.0%), withthe least amounts found in the tiger and the Zam-bezi (bull) livers (9.8%, 11.3%). Within the n3 PUFAthe raggedtooth, blacktip and scalloped hammerheadshowed high levels of docosahexaenoic acid (22:6n3)(10.9%, 9.4%, 10.1%), while high levels of eicos-apentaenoic acid (20:5n3) were found in the duskyand spinner(5.3%, 5.3%), and low levels in the tiger(1.7%). The total PUFA fractions were present in thegreatest amounts in the raggedtooth (26.6%) and thespinner (26.9%). The ratio of n6 to n3 PUFA wasgreatest in the tiger (0.86:1) and least in the scallopedhammerhead (027:1), while the ratio of SFA to PUFAwas least in the raggedtooth (1.39:1) and greatest inthe Zambezi (2.31:1) and tiger (2.14:1).

Discussion

While a major function of shark liver lipids is to main-tain buoyancy (Baldridge 1970; Bone and Roberts

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Table 2. The percentage composition of the liver lipid fatty acids from the seven shark species sampled

Fatty Acid Raggedtooth/Grey Nurse Blacktip Dusky Zambezi/Bull Spinner Scalloped Hammerhead Tiger

(n=13) (n=8) n=7) (n=8) (n=6) (n=6) (n=9)

14:0 3.8 ± 1.1 4.1 ± 0.7 5.4 ± 1.2 8.0 ± 1.9 6.4 ± 0.9 3.7 ± 0.5 2.5 ± 0.8

16:0 27.7 ± 3.3 28.4 ± 3.5 26.8 ± 2.7 21.3 ± 2.6 26.9 ± 2.7 21.4 ± 3.3 27.6 ± 1.8

18:0 5.6 ± 1.6 11.3 ± 1.9 7.1 ± 0.8 12.2 ± 2.1 10.0 ± 1.8 11.1 ± 1.6 8.9 ± 2.1

Tot SFA 37.1 ± 4.2 43.8 ± 5.0 39.3 ± 2.9 41.5 ± 3.0 43.3 ± 2.9 36.2 ± 3.9 39.0 ± 2.5

14:1n9 0.7 ± 0.2 0.8 ± 0.4 0.4 ± 0.1 0.3 ± 0.2 0.4 ± 0.1 0.3 ± 0.2 0.7 ± 0.3

16:1n9 9.8 ± 1.8 7.5 ± 1.3 14.0 ± 1.7 10.4 ± 1.8 7.9 ± 1.0 14.2 ± 1.9 11.3 ± 1.6

18:1n9 24.2 ± 2.3 23.2 ± 2.6 23.1 ± 2.5 29.1 ± 2.1 21.2 ± 1.9 24.9 ± 2.0 29.9 ± 2.5

20:1n9 1.7 ± 0.3 0.6 ± 0.2 0.9 ± 0.4 0.8 ± 0.2 0.3 ± 0.2 3.7 ± 1.0 0.9 ± 0.5

Tot MUFA 36.4 ± 2.5 32.1 ± 2.9 38.4 ± 2.9 40.6 ± 2.5 29.8 ± 2.3 43.1 ± 2.6 42.8 ± 2.9

18:2n6 1.4 ± 0.3 1.1 ± 0.7 1.0 ± 0.2 1.4 ± 0.2 1.7 ± 0.4 0.5 ± 0.2 1.9 ± 0.4

20:4n6 5.2 ± 0.9 4.8 ± 1.9 4.9 ± 1.3 2.6 ± 1.1 3.0 ± 0.8 2.4 ± 0.8 4.3 ± 1.2

22:4n6 1.3 ± 0.5 1.0 ± 0.4 1.6 ± 0.6 1.0 ± 0.5 1.3 ± 0.6 0.7 ± 0.4 1.5 ± 0.3

22:5n6 0.8 ± 0.4 2.1 ± 0.6 1.1 ± 0.3 1.7 ± 0.5 1.3 ± 0.7 0.8 ± 0.4 1.5 ± 0.6

Tot n6 PUFA 8.7 ± 1.0 9.0 ± 2.0 8.6 ± 1.1 6.7 ± 1.6 7.9 ± 1.8 4.4 ± 1.0 8.4 ± 1.9

20:5n3 3.8 ± 0.6 3.2 ± 1.1 5.3 ± 1.0 2.5 ± 0.9 5.3 ± 1.1 2.9 ± 1.1 1.7 ± 0.2

22:5n3 3.2 ± 0.9 2.5 ± 1.2 2.2 ± 1.5 1.4 ± 0.7 4.9 ± 1.6 3.4 ± 0.7 1.3 ± 0.4

22:6n3 10.9 ± 2.0 9.4 ± 2.2 6.5 ± 0.9 7.4 ± 1.3 8.8 ± 2.3 10.1 ± 2.0 6.8 ± 1.2

Tot n3 PUFA 17.9 ± 2.2 15.1 ± 2.3 14.0 ± 2.2 11.3 ± 1.8 19.0 ± 2.6 16.4 ± 2.4 9.8 ± 1.6

Tot PUFA 26.6 ± 2.4 24.4 ± 2.3 22.6 ± 2.6 18.0 ± 2.4 26.9 ± 2.8 20.8 ± 2.7 18.2 ± 2.1

n6:n3 0.48:1 0.60:1 0.61:1 0.59:1 0.42:1 0.27:1 0.86:1

SFA:PUFA 1.39:1 1.80:1 1.74:1 2.31:1 1.61:1 1.74:1 2.14:1

Tot SFA = Total saturated fatty acids, Tot MUFA = Total monounsaturated fatty acids, Tot n6 PUFA = Total n6 polyunsaturated fattyacids, Tot n3 PUFA = Total n3 polyunsaturated fatty acids, Tot PUFA = Total polyunsaturated fatty acids.Data shown as mean ± 1 SD.There were no significant differences between the species as assessed using the ‘t’ test. Smallest value for ‘p’ was >0.1.

1969; Phleger 1998), sharks also utilise fatty acids,stored in their livers, as sources of ketones for en-ergy metabolism in other tissues (Watson and Dickson2001). Much of the liver fatty acids are likely to be areservoir of substrates for this process, especially dur-ing times of dietary shortage, although some will alsobe structural components of liver cell membrane phos-phoglycerides. Most vertebrates preferentially utiliseSFA as fuel molecules, hence the relatively high levelsof these moieties across all the species analysed. How-ever, membrane phosphoglyceride structure requires abalance between SFA, monounsaturates (MUFA) andPUFA to maintain an appropriate degree of mem-brane fluidity, which may partially explain the levelsof PUFA detected in this study and others from westAfrica (Banjo 1979; Peyronel et al. 1984).

The blacktip, dusky, Zambezi and spinner areall member of the genus Carcharhinus, while theraggedtooth is a member of the Order Lamniformes.But the liver fatty acid results do not show any cor-relation with the genus or Order of the shark spe-cies, except for slight but non-significant differences

(P > 0.1) for the SFA between the four Carchar-hinus species and the other three species, and thescalloped hammerhead and tiger showing higher levelsof MUFA, but again not significant (P > 0.1) whencompared to the other species.

Teleosts, other elasmobranchs and squid make up alarge proportion of the sharks’ diets, although in vary-ing proportions, and these provide varying levels offatty acids from their tissues, partially dependent onthe prey species. Nelson et al. (2000, 2001), Nicholset al. (2001a), Phleger et al. (1997, 1999a, 1999b,2001) and Vlieg et al. 1993 have reported the fattyacid profiles of a wide range of marine organisms, andwhilst some of these may not necessarily be compon-ents of sharks dietary intakes, they illustrate the greatdiversity of fatty acid profiles found in the marine foodchain. In light of this, the results presented here maynot be a reflection of the taxonomic relationships, butmay rather reflect differences in dietary food sourceselection.

Nichols et al. (1998, 2001b) have published fattyacid profiles from several shark species in Australian

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waters, and included data on blacktip, tiger and ham-merhead. Their blacktip data seemed to vary consider-ably dependant on site of capture, and only concurredwith our data in some instances. Their results for tigershark agreed quite closely with the data in this study,except for 16:1n7, 20:4n6 and 22:6n3; while the dataon hammerhead sharks agreed very closely, althoughthey did not specify the species of hammerhead.

From the perspective of human health, a low ra-tio of SFA to PUFA (=<2:1) is considered beneficial.Long chain n3 moieties are present within the ter-restrial food chain at much lower levels than the n6 (n6to n3 ratio often greater than 10 to 1), while a ratio ofabout 2 to 1 is thought preferable. Thus oils rich in n3PUFA have the potential to be beneficial in redressingthis imbalance.

Excessive intake of SFA has been implicated inpredisposing towards hypercholesterolaemia, hyper-tension and myocardial infarction, amongst other con-ditions (Albert et al. 2002). Increased PUFA intake hasbeen suggested to ameliorate these effects, especiallyif there is a reasonable balance of n6 and n3 moieties(Hu et al. 2002). Increasing the n3 intake has also beensuggested to reduce the production of pro-aggregatorythromboxane A2 (Sinclair and Mann 1996) increasethe anti-inflammatory prostaglandins (Sanigorski et al.1994; Mann et al. 1994), and also shown to mitigateagainst clinical depression (Adams et al. 1996).

From this study, the best species for utilisationwould be the raggedtooth (low SFA, high PUFA, lowratio of SFA to PUFA), and a good n6 to n3 ratio(0.48:1). However, the raggedtooth also showed highlevels of both 20:4n6 (arachidonic acid) and 22:6n3(docosahexaenoic acid), both of which have signific-ance in human nutrition, but for largely contradict-ory reasons (Collier and Sinclair 1993). The spinnershowed a similar profile to the raggedtooth within thePUFA fraction, but the levels of SFA were higher.However, it must be borne in mind that the fatty acidcomposition of the liver oil may vary dramatically de-pending on the geographical location of the shark andpossibly also the diet and time of year (Nichols et al.1998, 2001b). It is also possible that the fatty acidcomposition may vary between the different classesof lipids (triacylglycerols, alkyldiacylglycerols, etc.).These fractions were not separated or analysed in thisstudy, but will be addressed in future expansion of thiswork.

There have been reports of shark liver oil stimulat-ing the immune system in humans, as well as showingbeneficial effects in ameliorating tissue damage res-

ulting from radiation therapy (Pugliese et al. 1998).At the same time, shark liver oil is also rich in the fatsoluble vitamins A, D and E (Nichols et al. 2001b).

For comparison, commercially available fish oils,MaxEPA and cod liver oil, provide 18% and 8%20:5n3 and 12% and 8% 22:6n3, respectively, whilethe mean for the shark livers reported here were 4%20:5n3 and 9% 22:6n3. Thus, shark liver would appearto be a good potential source of metabolically import-ant PUFA, and the harvesting of the livers from sharkscaught as part of the bycatch of teleost fisheries wouldprovide a good source of PUFA-rich oil, and this oilwould provide higher levels of n3 than n6 PUFA, thushelping to counterbalance the preponderance of n6provided by the terrestrial food chain.

Acknowledgements

The authors would like to recognise the support ofthe Natal Sharks Board operations and laboratory stafffor providing the shark liver samples without whichthis project would have been impossible. The authorswould like to thank the University of the Witwater-srand for financial and infrastructural support of thisproject.

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