Lipids

, Volume 48, Issue 10, pp 1029–1034

Unusually High Levels of n-6 Polyunsaturated Fatty Acids in Whale Sharks and Reef Manta Rays

  • L. I. E. Couturier
  • C. A. Rohner
  • A. J. Richardson
  • S. J. Pierce
  • A. D. Marshall
  • F. R. A. Jaine
  • K. A. Townsend
  • M. B. Bennett
  • S. J. Weeks
  • P. D. Nichols
Open Access
Communication

Abstract

Fatty acid (FA) signature analysis has been increasingly used to assess dietary preferences and trophodynamics in marine animals. We investigated FA signatures of connective tissue of the whale shark Rhincodon typus and muscle tissue of the reef manta ray Manta alfredi. We found high levels of n-6 polyunsaturated fatty acids (PUFA), dominated by arachidonic acid (20:4n-6; 12–17 % of total FA), and comparatively lower levels of the essential n-3 PUFA—eicosapentaenoic acid (20:5n-3; ~1 %) and docosahexaenoic acid (22:6n-3; 3–10 %). Whale sharks and reef manta rays are regularly observed feeding on surface aggregations of coastal crustacean zooplankton during the day, which generally have FA profiles dominated by n-3 PUFA. The high levels of n-6 PUFA in both giant elasmobranchs raise new questions about the origin of their main food source.

Keywords

n-3 Fatty acids Arachidonic acid Planktivores Zooplankton Elasmobranch 

Abbreviations

ARA

Arachidonic acid

DHA

Docosahexaenoic acid

EPA

Eicosapentaenoic acid

FA

Fatty acid(s)

GC

Gas chromatography

LA

Linoleic acid

LC-PUFA

Long chain- polyunsaturated fatty acid(s)

MUFA

Monounsaturated fatty acid(s)

PUFA

Polyunsaturated fatty acid(s)

SEM

Standard error of the mean

SFA

Saturated fatty acid(s)

Introduction

The whale shark Rhincodon typus and the reef manta ray Manta alfredi are giant planktivorous elasmobranchs that are presumed to feed predominantly on aggregations of zooplankton in highly productive areas [1, 2]. Direct studies on the diet of these elasmobranchs are limited to examination of a few stomach contents, faecal material and stable isotope analyses [3, 4, 5, 6], while recent field observations suggest that their diets are mostly composed of crustacean zooplankton [1, 7]. It is unknown, however, whether near-surface zooplankton are a major or only a minor part of their diets, whether these large elasmobranchs target other prey, or whether they feed in areas other than surface waters along productive coastlines.

Here we used signature fatty acid (FA) analysis to assess dietary preferences of R. typus and M. alfredi. The essential long-chain (≥C20) polyunsaturated fatty acids (LC-PUFA) of fishes are most likely derived directly from the diet, as higher consumers generally lack the ability to biosynthesise these FA de novo [8, 9]. The fatty acid profile of zooplankton is usually dominated by PUFA with a high n-3/n-6 ratio, and generally contains high levels of eicosapentaenoic acid (EPA, 20:5n-3) and/or docosahexaenoic acid (DHA, 22:6n-3) [8, 10, 11]. Considering this, it was expected that FA profiles of R. typus and M. alfredi tissues would be similarly n-3 PUFA dominated.

Materials and Methods

Tissue samples were collected from live, unrestrained specimens in southern Mozambique (14 R. typus and 12 M. alfredi) and eastern Australia (9 M. alfredi) using a modified Hawaiian hand-sling with a fitted biopsy needle tip between June–August 2011. Biopsies of R. typus were extracted laterally between the 1st and 2nd dorsal fin and penetrated ~20 mm deep from the skin into the underlying connective tissue. Biopsies of M. alfredi were of similar size, but were mainly muscle tissue, extracted from the ventro-posterior area of the pectoral fins away from the body cavity. Biopsies were immediately put on ice in the field and then stored at −20 °C for up to 3 months before analysis.

Lipids were extracted overnight using the modified Bligh and Dyer [12] method with a one-phase methanol:chloroform:water (2:1:0.8 by volume) mixture. Phases were separated by adding water and chloroform, followed by rotary evaporation of the chloroform in vacuo at ~40 °C. Total lipid extracts were concentrated by application of a stream of inert nitrogen gas and samples were stored in chloroform at −20 °C before FA analysis.

The total lipid extract from each sample was spotted on chromarods that were developed for 25 min in a polar solvent system (hexane:diethyl-ether:acetic acid, 60:17:0.1 by volume). The chromarods were then dried in an oven for 10 min at 100 °C and analysed immediately. Lipid class composition was determined for each sample using an Iatroscan Mark V TH10 thin layer chromatograph combined with a flame ionisation detector. A standard solution containing wax esters, triacylglycerol, free FA, sterols and phospholipids (Nu-Chek Prep. Inc., MN, USA) was run with the samples. Each peak was identified by comparison of Rf with the standard chromatogram. Peak areas were measured using SIC-480II Iatroscan™ Integrating Software v.7.0-E (System Instruments Co., Mitsubishi Chemical Medicine Corp., Japan) and quantified to mass per μL spotted using predetermined linear regressions.

An aliquot of the total extracted lipids was treated with methanol:hydrochloric acid:chloroform (10:1:1), heated at ~80 °C for 2 h and the resulting fatty acid methyl esters were extracted into hexane:chloroform (4:1). Samples were analysed using an Agilent Technologies 7890 B gas chromatography (GC) (Palo Alto, California, USA) equipped with a non-polar Equity™-1 fused silica capillary column (15 m × 0.1 mm i.d., 0.1 μm film thickness), a flame ionisation detector, a split/split-less injector and an Agilent Technologies 7683 B Series auto sampler. Helium was the carrier gas. Samples were injected in split-less mode at an oven temperature of 120 °C. After injection, oven temperature was raised to 270 °C at 10 °C/min and finally to 300 °C at 5 °C/min. Peaks were quantified with Agilent Technologies ChemStation software (Palo Alto, California, USA). Sterols were also separated under the GC conditions used, and largely comprised cholesterol. GC results typically have an error of up to ±5 % of individual component area. Peak identities were confirmed with a Finnigan ThermoQuest GCQ GC mass-spectrometer (GC-MS) system (Finnigan, San Jose,CA) [13]. Percentage FA data were calculated from the areas of chromatogram peaks. All FA are expressed as mole percentage of total FA.

Results and Discussion

Fatty acids of both M. alfredi muscle tissue and R. typus connective tissue were predominantly derived from phospholipids (Table 1). The classes of phospholipids were not distinguished in this study, but should be examined in future studies where phospholipids are found to be the dominant lipid class of these two giant elasmobranchs. The FA profile of M. alfredi was dominated by PUFA (34.9 % of total FA), while saturated FA were most abundant in R. typus (39.1 % of total FA) (Table 2). The main FA in both species included 18:0, 18:1n-9, 16:0 and 20:4n-6. Arachidonic acid (AA; 20:4n-6) was the most abundant FA in R. typus (16.9 %) whereas 18:0 was most abundant in M. alfredi (16.8 %). Both species had a relatively low level of EPA (1.1 and 1.2 %) and M. alfredi had a relatively high level of DHA (10.0 %) compared to R. typus (2.5 %). Fatty acid signatures of R. typus and M. alfredi were different to expected profiles of species that feed predominantly on crustacean zooplankton, which are typically dominated by n-3 PUFA and have high levels of EPA and/or DHA [8, 10, 11]. Instead, profiles of both large elasmobranchs were dominated by n-6 PUFA (>20 % total FA), with an n-3/n-6 ratio <1 and markedly high levels of AA (Table 2). The FA profiles of M. alfredi were broadly similar between the two locations, although some differences were observed that are likely due to dietary differences. Future research should aim to look more closely at these differences and potential dietary contributions.
Table 1

Means ± SE (standard error) lipid class compositions of whale shark (n = 14) and reef manta ray (n = 15) tissue samples, expressed as % of total lipid

Lipid class

Whale shark (n = 14)

Reef manta ray (n = 15)

% Total lipid ± SE

% Total lipid ± SE

WE

2.8 ± 1.3

0.6 ± 0.4

TAG

3.3 ± 1.4

3.4 ± 0.7

FFA

5.3 ± 1.0

2.1 ± 0.3

ST

20.5 ± 0.8

10.8 ± 1.1

PL

68.1 ± 3.5

83.0 ± 1.5

Total lipid content (mg g−1)

1.8 ± 1.1

3.8 ± 0.3

Total lipid content is expressed as mg g−1 of tissue wet mass

WE wax esters, TAG triacylglycerols, FFA free fatty acids, ST sterols (comprising mostly cholesterol), PL phospholipids

Table 2

FA composition (mol% of total FA) of the whale shark R. typus (n = 14) and the reef manta ray M. alfredi (n = 21) [minor fatty acids (≤1 %) are not shown]

 

R. typus

M. alfredi

Mean (±SEM)

Mean (±SEM)

∑SFA

39.1 (0.7)

35.1 (0.7)

 16:0

13.8 (0.5)

14.7 (0.4)

 17:0

1.6 (0.1)

0

 i18:0

1.1 (0.1)

0.3 (0.1)

 18:0

17.8 (0.5)

16.8 (0.4)

∑MUFA

31.0 (0.9)

29.9 (0.7)

 16:1n-7c

2.1 (0.3)

2.7 (0.3)

 17:1n-8ca

1.8 (0.3)

0.7 (0.1)

 18:1n-9c

16.7 (0.7)

15.7 (0.4)

 18:1n-7c

4.6 (0.5)

6.1 (0.2)

 20:1n-9c

0.7 (0.02)

1.0 (0.03)

 24:1n-9c

1.9 (0.1)

1.1 (0.1)

∑PUFA

29.9 (0.9)

34.9 (1.2)

∑n-3

6.1 (0.3)

13.4 (0.6)

 20:5n-3 (EPA)

1.1 (0.1)

1.2 (0.1)

 22:6n-3 (DHA)

2.5 (0.2)

10.0 (0.5)

 22:5n-3

2.1 (0.1)

2.0 (0.1)

∑n-6

23.8 (0.8)

21.0 (1.4)

 20:4n-6 (AA)

16.9 (0.6)

11.7 (0.8)

 22:5n-6

0.9 (0.1)

3.3 (0.3)

 22:4n-6

5.5 (0.3)

5.1 (0.5)

n-3/n-6

0.3 (0.02)

0.7 (0.1)

SFA saturated fatty acids, MUFA monounsaturated fatty acids, PUFA polyunsaturated fatty acids, EPA eicosapentaenoic acid, DHA docosahexaenoic acid, AA arachidonic acid

aIncludes a17:0 coeluting

The n-6-dominated FA profiles are rare among marine fishes. Most other large pelagic animals and other marine planktivores have an n-3-dominated FA profile and no other chondrichthyes investigated to date has an n-3/n-6 ratio <1 [14, 15, 16] (Table 3, literature data are expressed as wt%). The only other pelagic planktivore with a similar n-3/n-6 ratio (i.e. 0.9) is the leatherback turtle, that feeds on gelatinous zooplankton [17]. Only a few other marine species, such as several species of dolphins [18], benthic echinoderms and the bottom-dwelling rabbitfish Siganus nebulosus [19], have relatively high levels of AA, similar to those found in whale sharks and reef manta rays (Table 3).
Table 3

Polyunsaturated fatty acid composition of chondrichthyan, planktivore, large pelagic and detrivore species

Species

Feeding habitat

Tissue

∑n-3

∑n-6

AA

EPA

DHA

n-3/n-6

Reference

Whale shark—R. typus (mol%)

Epipelagic—planktivore

Skin

6.1

23.8

16.9

1.1

2.5

0.3

This study

Whale shark—R. typus (wt%)

Epipelagic—planktivore

Skin

6.7

25.4

17.8

1.2

2.8

0.3

This study

Reef manta ray—M. alfredi (mol%)

Epipelagic—planktivore

Muscle

13.4

21.0

11.7

1.2

10.0

0.7

This study

Reef manta ray—M. alfredi (wt%)

Epipelagic—planktivore

Muscle

14.9

21.6

11.8

1.2

11.3

0.7

This study

Other chondrichthyes

 Port Jackson shark—Heterodontus portusjacksoni

Demersal—carnivore

Muscle

23.6

19.4

13.8

3.7

15.4

1.2

[45]

 Sandy-backed stingaree—Urolophus bucculentus

Demersal—carnivore

Muscle

32.9

16.5

12.6

3.1

27.9

2.0

[45]

 Southern chimaera—Chimaera fulva

Deep sea—carnivore

Muscle

30.4

11.2

4.7

3.4

23.3

2.7

[46]

 Angel shark—Squatina australis

Demersal—carnivore

Muscle

45.2

10.5

7.6

6.1

36.5

4.3

[45]

 Longnose velvet dogfish—Centroselachus crepidater

Deep sea—carnivore

Muscle

39.1

6.6

4.4

2.3

32.2

5.9

[46]

 Shortnose spurdog—Squalus megalops

Deep sea—carnivore

Muscle

37.5

6.4

3.6

1.2

32.3

5.9

[46]

 South China catshark—Apristurus sinensis

Deep sea—carnivore

Muscle

38.5

6.4

3.4

2.9

28.9

6

[46]

 Broadnose sevengill shark—Notorynchus cepedianus

Deep sea—carnivore

Liver

23.2

3.2

1.7

3.4

16.6

7.2

[46]

Planktivores

 Leatherback turtle—Dermochelys coriacea

Epipelagic—planktivore

Muscle

15.5

17.3

15.5

6.1

5.7

0.9

[17]

 Jellyfish—Aurelia sp.

Epipelagic—planktivore

Whole

34.5

12.2

9.9

14.1

9.8

2.8

[25]

 Finwhale—Balaenoptera physalus

Pelagic—planktivore

Blubber oil

6.7

2.3

0.3

1.8

2.74

2.9

[47]

 Anchovies—Engraulis mordax mordax

Pelagic—planktivore

Whole

22.9

4.9

0.4

13.5

8.8

27.8

[48]

Large pelagics

 Dolphin—mixed species

Epipelagic—carnivore

Muscle

16.3

18.6

14.2

6.4

7.6

0.9

[18]

Gray whale—E. robustus

Pelagic—planktivore

Muscle

4.7

7.5

1.2

~1.8

[49]

 Ocean sunfish—Mola mola

Pelagic—carnivore

Muscle

29.4

10.8

7.73

8.8

17.0

2.7

[50]

Benthic feeders

 Sea cucumber—Holothuria scabra

Benthic—deposit feeder

Whole

10.7

22.6

19.1

8.2

1.5

0.5

[19]

 Sea urchin—Heliocidaris erythrogramma

Benthic—deposit feeder

Whole

10.7

14.6

6.1

8.3

0.4

0.7

[19]

 Dusky rabbitfish—Siganus nebulosus

Benthic—deposit feeder

Muscle

18.5

20.5

12.4

1.3

14.6

0.9

[19]

Data from this study for Rhincodon typus and Manta alfredi are expressed in both mol% and wt% format, with all literature data as wt%

EPA eicosapentaenoic acid, DHA docosahexaenoic acid, AA arachidonic acid

The trophic pathway for n-6-dominated FA profiles in the marine environment is not fully understood. Although most animal species can, to some extent, convert linoleic acid (LA, 18:2n-6) to AA [8], only traces of LA (<1 %) were present in the two filter-feeders here. Only marine plant species are capable of biosynthesising long-chain n-3 and n-6 PUFA de novo, as most animals do not possess the enzymes necessary to produce these LC-PUFA [8, 9]. These findings suggest that the origin of AA in R. typus and M. alfredi is most likely directly related to their diet.

Although FA are selectively incorporated into different elasmobranch tissues, little is known on which tissue would best reflect the diet FA profile. McMeans et al. [14] recently showed that FA profile of muscle in the Greenland shark is the most representative of its prey FA profiles. It is thus assumed here that the muscle tissue of M. alfredi is representative of its diet, but the extent to which the FA profile of the subdermal connective tissue of R. typus reflects its diet is unknown.

Certain species of phytoplankton including diatoms, and some macro algae such as Rhodophyta can biosynthesise n-6 PUFA, with levels of over 40 % (as wt%) of AA recorded [20, 21]. Although phytoplankton and macro algae have been reported in R. typus stomach contents, they are assumed to be incidentally ingested [22]. The feeding apparatus and feeding strategy of R. typus and M. alfredi are adapted for targeting larger prey [23, 24]. There is no observational evidence of either species targeting phytoplankton, but there are frequent observations of feeding on zooplankton patches. More plausibly, n-6 LC-PUFA from phytoplankton could enter the food chain when consumed by zooplankton and subsequently be transferred to higher-level consumers. It is unclear what type of zooplankton is likely to feed on AA-rich algae. To date, only a few jellyfish species are known to contain high levels of AA (2.8–9.9 % of total FA as wt%), but they also have high levels of EPA, which are low in R. typus and M. alfredi [17, 25, 26].

Some protozoans and microeukaryotes, including heterotrophic thraustochytrids in marine sediments are rich in AA [27, 28, 29, 30] and could be linked with high n-6 LC-PUFA and AA levels in benthic feeders (n-3/n-6 = 0.5–0.9; AA = 6.1–19.1 % as wt%; Table 3), such as echinoderms, stingrays and other benthic fishes. However, the pathway of utilisation of AA from these micro-organisms remains unresolved. R. typus and M. alfredi may feed close to the sea floor and could ingest sediment with associated protozoan and microeukaryotes suspended in the water column; however, they are unlikely to target such small sediment-associated benthos. The link to R. typus and M. alfredi could be through benthic zooplankton, which potentially feed within the sediment on these AA-rich organisms and then emerge in high numbers out of the sediment during their diel vertical migration [31, 32]. It is unknown to what extent R. typus and M. alfredi feed at night when zooplankton in shallow coastal habitats emerges from the sediment.

The subtropical/tropical distribution of R. typus and M. alfredi is likely to partly contribute to their n-6-rich PUFA profiles. Although still strongly n-3-dominated, the n-3/n-6 ratio in fish tissue noticeably decreases from high to low latitudes, largely due to an increase in n-6 PUFA, particularly AA (Table 3) [33, 34, 35]. This latitudinal effect alone does not, however, explain the unusual FA signatures of R. typus and M. alfredi.

We found that M. alfredi contained more DHA than EPA, while R. typus had low levels of both these n-3 LC-PUFA, and there was less of either n-3 LC-PUFA than AA in both species. As DHA is considered a photosynthetic biomarker of a flagellate-based food chain [8, 10], high levels of DHA in M. alfredi could be attributed to crustacean zooplankton in the diet, as some zooplankton species feed largely on flagellates [36]. By contrast, R. typus had low levels of EPA and DHA, and the FA profile showed AA as the major component.

Our results suggest that the main food source of R. typus and M. alfredi is dominated by n-6 LC-PUFA that may have several origins. Large, pelagic filter-feeders in tropical and subtropical seas, where plankton is scarce and patchily distributed [37], are likely to have a variable diet. At least for the better-studied R. typus, observational evidence supports this hypothesis [38, 39, 40, 41, 42, 43]. While their prey varies among different aggregation sites [44], the FA profiles shown here suggest that their feeding ecology is more complex than simply targeting a variety of prey when feeding at the surface in coastal waters. Trophic interactions and food web pathways for these large filter-feeders and their potential prey remain intriguingly unresolved. Further studies are needed to clarify the disparity between observed coastal feeding events and the unusual FA signatures reported here, and to identify and compare FA signatures of a range of potential prey, including demersal and deep-water zooplankton.

Notes

Acknowledgments

We thank P. Mansour for his assistance with laboratory techniques and equipment, D. Holdsworth for management of the CSIRO GC-MS facility and C. F. (Rick) Phleger for early comments on this study. We thank E. Murphy, the Associate Editor and two anonymous reviewers for providing constructive comments that improved the quality of the manuscript. This study was supported by the ARC Linkage Grant LP110100712, Earthwatch Institute Australia and Sibelco Pty Ltd. Field work was supported by Casa Barry Lodge, Peri-Peri Divers, Lady Elliot Island Eco Resort and Manta Lodge and Scuba Centre and was conducted under Great Barrier Reef Marine Park permit (G09/29853.1) and Ethics approval (SBMS/071/08/SEAWORLD).

References

  1. 1.
    Nelson JD, Eckert SA (2007) Foraging ecology of whale sharks (Rhincodon typus) within Bahía De Los Angeles, Baja California Norte, México. Fish Res 84:47–64CrossRefGoogle Scholar
  2. 2.
    Anderson RC, Adam MS, Goes JI (2011) From monsoons to mantas: seasonal distribution of Manta alfredi in the Maldives. Fish Oceanogr 20:104–113CrossRefGoogle Scholar
  3. 3.
    Jarman S, Wilson S (2004) DNA-based species identification of krill consumed by whale sharks. J Fish Biol 65:586–591CrossRefGoogle Scholar
  4. 4.
    Silas E, Rajagopalan M (1963) On a recent capture of a whale shark (Rhincodon typus Smith) at Tuticorin, with a note on information to be obtained on whale sharks from Indian waters. J Mar Biol Ass India 5:153–157Google Scholar
  5. 5.
    Borrell A, Cardona L, Kumarran RP, Aguilar A (2011) Trophic ecology of elasmobranchs caught off Gujarat, India, as inferred from stable isotopes. ICES J Mar Sci 68:547–554CrossRefGoogle Scholar
  6. 6.
    Whitley GP (1936) The Australian devil ray, Daemomanta alfredi (Krefft), with remarks on the superfamily Mobuloidae (order Batoidei). Aust Zool 8:164–188Google Scholar
  7. 7.
    Papastamatiou YP, DeSalles PA, McCauley DJ (2012) Area-restricted searching by manta rays and their response to spatial scale in lagoon habitats. Mar Ecol Prog Ser 456:233CrossRefGoogle Scholar
  8. 8.
    Dalsgaard J, St John M, Kattner G, Müller-Navarra D, Hagen W (2003) Fatty acid trophic markers in the pelagic marine environment. Adv Mar Biol 46:225–340PubMedCrossRefGoogle Scholar
  9. 9.
    Iverson SJ (2009) Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. In: Arts MT, Brett MT, Kainz M (eds) Lipids in aquatic ecosystems. Springer Science, New YorkGoogle Scholar
  10. 10.
    Brett MT, Müller-Navarra DC, Persson J (2009) Crustacean zooplankton fatty acid composition. In: Arts MT, Bakes MJ, Kainz M (eds) Lipids in aquatic ecosystems. Springer Science, New YorkGoogle Scholar
  11. 11.
    Sargent J, Falk-Petersen S (1988) The lipid biochemistry of calanoid copepods. Hydrobiologia 167:101–114CrossRefGoogle Scholar
  12. 12.
    Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedCrossRefGoogle Scholar
  13. 13.
    Phleger CF, Nelson MM, Mooney BD, Nichols PD, Ritar AJ, Smith GG, Hart PR, Jeffs AG (2001) Lipids and nutrition of the southern rock lobster, Jasus edwardsii, from hatch to Puerulus. Mar Freshw Res 52:1475–1486CrossRefGoogle Scholar
  14. 14.
    McMeans BC, Arts MT, Fisk AT (2012) Similarity between predator and prey fatty acid profiles is tissue dependent in Greenland sharks (Somniosus microcephalus): implications for diet reconstruction. J Exp Mar Biol Ecol 429:55–63CrossRefGoogle Scholar
  15. 15.
    Pethybridge H, Daley RK, Nichols PD (2011) Diet of demersal sharks and chimaeras inferred by fatty acid profiles and stomach content analysis. J Exp Mar Biol Ecol 409:290–299CrossRefGoogle Scholar
  16. 16.
    Schaufler L, Heintz R, Sigler M, Hulbert L (2005) Fatty acid composition of sleeper shark (Somniosus pacificus) liver and muscle reveals nutritional dependence on Planktivores. ICES CM, Elasmobranch Fisheries Science, p 19Google Scholar
  17. 17.
    Holland D, Davenport J, East J (1990) The fatty acid composition of the leatherback turtle Dermochelys coriacea and its jellyfish prey. J Mar Biol Assoc UK 70:761–770CrossRefGoogle Scholar
  18. 18.
    Williams G, Crawford M, Perrin W (1987) Comparison of the fatty acid component in structural lipids from dolphins, zebra and giraffe: possible evolutionary implications. J Zool 213:673–684CrossRefGoogle Scholar
  19. 19.
    Nichols PD, Mooney BD, Elliott NG (2002) Nutritional value of Australian seafood ii., Factors affecting oil composition of edible species. A.F. R. D. C. F. CSIRO Marine ResearchCSIRO Marine Research, Australia, pp 1–195Google Scholar
  20. 20.
    Dunstan GA, Volkman JK, Barrett SM, Leroi JM, Jeffrey S (1994) Essential polyunsaturated fatty acids from 14 species of diatom (Bacillariophyceae). Phytochem 35:155–161CrossRefGoogle Scholar
  21. 21.
    Johns R, Nichols P, Perry G (1979) Fatty acid composition of ten marine algae from Australian waters. Phytochemistry 18:799–802CrossRefGoogle Scholar
  22. 22.
    Colman JG (1997) A review of the biology and ecology of the whale shark. J Fish Biol 51:1219–1234CrossRefGoogle Scholar
  23. 23.
    Motta PJ, Maslanka M, Hueter RE, Davis RL, De La Parra R, Mulvany SL, Habegger ML, Strother JA, Mara KR, Gardiner JM (2010) Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico. Zoology 113:199–212PubMedCrossRefGoogle Scholar
  24. 24.
    Paig-Tran EWM, Bizzarro JJ, Strother JA, Summers AP (2011) Bottles as models: predicting the effects of varying swimming speed and morphology on size selectivity and filtering efficiency in fishes. J Exp Biol 214:1643–1654PubMedCrossRefGoogle Scholar
  25. 25.
    Nichols PD, Danaher KT, Koslow JA (2003) Occurrence of high levels of tetracosahexaenoic acid in the jellyfish Aurelia sp. Lipids 38:1207–1210PubMedCrossRefGoogle Scholar
  26. 26.
    Sipos J, Ackman RG (1968) Jellyfish (Cyanea capillata) lipids: fatty acid composition. J Fish Res Board Can 25:1561–1569CrossRefGoogle Scholar
  27. 27.
    Bell M, Sargent J (1985) Fatty acid analyses of phosphoglycerides from tissues of the clam Chlamys Islandica (Muller) and the starfish Ctenodiscus crispatus (Retzius) from Balsfjorden, Northern Norway. J Exp Mar Biol Ecol 87:31–40CrossRefGoogle Scholar
  28. 28.
    Howell KL, Pond DW, Billett DSM, Tyler PA (2003) Feeding ecology of deep-sea seastars (Echinodermata: Asteroidea): a fatty-acid biomarker approach. Mar Ecol Prog Ser 255:193–206CrossRefGoogle Scholar
  29. 29.
    Nichols DS (2003) Prokaryotes and the input of polyunsaturated fatty acids to the marine food web. FEMS Microbiol Lett 219:1–7PubMedCrossRefGoogle Scholar
  30. 30.
    Lee Chang KJ, Dunstan GA, Abell GCJ, Clementson LA, Blackburn SI, Nichols PD, Koutoulis A (2012) Biodiscovery of new Australian thraustochytrids for production of biodiesel and long-chain omega-3 oils. Appl Microbiol Biotechnol 93:2215PubMedCrossRefGoogle Scholar
  31. 31.
    Hutchinson GE (1967) A treatise on limnology. Wiley, New YorkGoogle Scholar
  32. 32.
    Stoecker DK, Capuzzo JMD (1990) Predation on protozoa: its importance to zooplankton. J Plankton Res 12:891–908CrossRefGoogle Scholar
  33. 33.
    Armstrong SG, Wyllie SG, Leach DN (1994) Effects of season and location of catch on the fatty acid compositions of some Australian fish species. Food Chem 51:295–305CrossRefGoogle Scholar
  34. 34.
    Sinclair A, O’Dea K, Naughton J, Sutherland T, Wankowski J (1984) Polyunsaturated fatty acid types in some Australian and Antarctic fish. In: Proceedings of the nutrition society of Australia conference 9:188Google Scholar
  35. 35.
    Gibson R (1983) Australian fish—an excellent source of both arachidonic acid and n-3 polyunsaturated fatty acids. Lipids 18:743–752CrossRefGoogle Scholar
  36. 36.
    Kleppel GS (1993) On the diets of calanoid copepods. Mar Ecol Prog Ser 99:183–195CrossRefGoogle Scholar
  37. 37.
    Lalli CM, Parsons TR (1997) Biological oceanography: an introduction, 2nd edn. Butterworth-Heinemann Oxford, UKGoogle Scholar
  38. 38.
    de la Parra Venegas R, Hueter R, Cano JG, Tyminski J, Remolina JG, Maslanka M, Ormos A, Weigt L, Carlson B, Dove A (2011) An unprecedented aggregation of whale sharks, Rhincodon typus, in Mexican coastal waters of the Caribbean sea. PLoS One 6:e18994PubMedCrossRefGoogle Scholar
  39. 39.
    Duffy C (2002) Distribution, seasonality, lengths, and feeding behaviour of whale sharks (Rhincodon typus) observed in New Zealand waters. N Z J Mar Freshw Res 36:565–570CrossRefGoogle Scholar
  40. 40.
    Heyman WD, Graham RT, Kjerfve B, Johannes RE (2001) Whale sharks Rhincodon typus aggregate to feed on fish spawn in Belize. Mar Ecol Prog Ser 215:275–282CrossRefGoogle Scholar
  41. 41.
    Robinson DP, Jaidah MY, Jabado RW, Lee-Brooks K, El-Din NMN, Malki AAA, Elmeer K, McCormick PA, Henderson AC, Pierce SJ (2013) Whale sharks, Rhincodon typus, aggregate around offshore platforms in Qatari waters of the Arabian Gulf to feed on fish spawn. PLoS One 8:e58255PubMedCrossRefGoogle Scholar
  42. 42.
    Rowat D, Meekan M, Engelhardt U, Pardigon B, Vely M (2007) Aggregations of juvenile whale sharks (Rhincodon typus) in the Gulf of Tadjoura, Djibouti. Environ Biol Fishes 80:465–472CrossRefGoogle Scholar
  43. 43.
    Meekan M, Jarman S, McLean C, Schultz M (2009) DNA evidence of whale sharks (Rhincodon typus) feeding on red crab (Gecarcoidea Natalis) larvae at Christmas Island, Australia. Mar Freshw Res 60:607–609CrossRefGoogle Scholar
  44. 44.
    Rowat D, Brooks K (2012) A review of the biology, fisheries and conservation of the whale shark Rhincodon typus. J Fish Biol 80:1019–1056PubMedCrossRefGoogle Scholar
  45. 45.
    Dunstan GA, Sinclair AJ, O’Dea K, Naughton JM (1988) The lipid content and fatty acid composition of various marine species from southern Australian coastal waters. Comp Biochem Physiol B 91:165–169CrossRefGoogle Scholar
  46. 46.
    Pethybridge H, Daley R, Virtue P, Nichols P (2010) Lipid composition and partitioning of deepwater chondrichthyans: inferences of feeding ecology and distribution. Mar Biol 157:1367–1384CrossRefGoogle Scholar
  47. 47.
    Ackman RG, Epstein S, Eaton CA (1971) Differences in the fatty acid compositions of blubber fats from Northwestern Atlantic finwhales (Balaenoptera physalus) and harp seals (Pagophilus groenlandica). Comp Biochem Physiol B 40:683–697PubMedGoogle Scholar
  48. 48.
    Lewis R (1967) Fatty acid composition of some marine animals from various depths. J Fish Res Board Can 24:1101–1115CrossRefGoogle Scholar
  49. 49.
    Caraveo-Patiño J, Wang Y, Soto LA, Ghebremeskel K, Lehane C, Crawford MA (2009) Eco-physiological repercussions of dietary arachidonic acid in cell membranes of active tissues of the gray whale. Mar Ecol 30:437–447CrossRefGoogle Scholar
  50. 50.
    Hooper S, Paradis M, Ackman RG (1973) Distribution of trans-6-hexadecenoic acid, 7-methyl-7-hexadecenoic acid and common fatty acids in lipids of the ocean sunfish Mola mola. Lipids 8:509–516PubMedCrossRefGoogle Scholar

Copyright information

© The Author(s) 2013

Open AccessThis article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.

Authors and Affiliations

  • L. I. E. Couturier
    • 1
    • 2
  • C. A. Rohner
    • 2
    • 3
    • 4
  • A. J. Richardson
    • 2
    • 5
  • S. J. Pierce
    • 3
    • 6
  • A. D. Marshall
    • 3
    • 6
  • F. R. A. Jaine
    • 2
    • 4
  • K. A. Townsend
    • 7
  • M. B. Bennett
    • 1
  • S. J. Weeks
    • 4
  • P. D. Nichols
    • 8
  1. 1.School of Biomedical SciencesThe University of QueenslandSt LuciaAustralia
  2. 2.Climate Adaptation FlagshipCSIRO Marine and Atmospheric ResearchDutton ParkAustralia
  3. 3.Manta Ray and Whale Shark Research CentreMarine Megafauna FoundationInhambaneMozambique
  4. 4.Biophysical Oceanography Group, School of Geography, Planning and Environmental ManagementThe University of QueenslandSt LuciaAustralia
  5. 5.Centre for Applications in Natural Resource MathematicsThe University of QueenslandSt LuciaAustralia
  6. 6.Wild MeInhambaneMozambique
  7. 7.School of Biological SciencesThe University of QueenslandSt LuciaAustralia
  8. 8.Wealth from Oceans FlagshipCSIRO Marine and Atmospheric ResearchHobartAustralia

Personalised recommendations