Skip to main content
Log in

Tissue-specific fatty acid profiles of vent-obligate tonguefishes (Symphurus spp.) on volcanic arcs in the western Pacific Ocean

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Symphurine tonguefishes (Pleuronectiformes: Cynoglossidae) have been found at hydrothermal vents on several submarine volcanoes in the western Pacific Ocean, often in great numbers. Marine fishes require dietary polyunsaturated fatty acids (PUFA) for growth and development, but it is unclear how this need is met in environments based on chemosynthetic production. Furthermore, the trophic ecology and nutritional requirements of symphurine tonguefishes at vents are generally unknown. To address these knowledge gaps, fatty acid composition was determined in muscle, liver, gonad and eyes of Symphurus thermophilus (Mariana Arc; 21°–23°N, 142°–144°E) and Symphurus sp. A (Tonga Arc; 21°09′S, 175°45′W) sampled in October 2005 and May 2007, respectively. All tissues of Symphurus spp. contained substantial levels of PUFA. Relative amounts of most PUFA in muscle tissues of Symphurus spp. were similar to levels measured in non-vent demersal fishes from temperate waters worldwide. Principal components analysis using fatty acid profiles of Symphurus sp. A from the Tonga Arc revealed three distinct clusters of samples that were related to tissue type. Similar trends could not be discerned for S. thermophilus (Mariana Arc). The fatty acid composition of Symphurus spp. suggests that PUFA-rich prey were not limiting at the sampled vents, although we lack information about how these fishes metabolize lipid. Stable carbon isotope ratios (δ13C) of several individual fatty acids in fish from Nikko and Daikoku suggest a photic zone origin. Benthic–pelagic coupling on intra-oceanic volcanic arcs may strongly influence the presence and persistence of resident vertebrates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahlgren G, Vrede T, Goedkoop W (2009) Fatty acid ratios in freshwater fish, zooplankton and zoobenthos—are there specific optima? In: Arts MT, Bret MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, London, pp 147–178. doi:10.1007/978-0-387-89366-2_7

    Chapter  Google Scholar 

  • Bakes MJ, Elliott NG, Green GJ, Nichols PD (1995) Variation in lipid composition of some deep-sea fish (Teleostei: Oreosomatidae and Trachichthyidae). Comp Biochem Physiol B 111:633–642. doi:10.1016/0305-0491(95)00024-3

    Article  Google Scholar 

  • Bell MV, Batty RS, Dick JR, Fretwell K, Navarro JC, Sargent JR (1995) Dietary deficiency of docosahexaenoic acid impairs vision at low light intensities in juvenile herring (Clupea harengus L.). Lipids 30:443–449. doi:10.1007/BF02536303

    Article  CAS  Google Scholar 

  • Bell JG, McEvoy LA, Estevez A, Shields RJ, Sargent JR (2003) Optimising lipid nutrition in first-feeding flatfish larvae. Aquaculture 227:211–220. doi:10.1016/S0044-8486(03)00504-0

    Article  CAS  Google Scholar 

  • Body DR (1983) The nature and fatty acid composition of the oils from deep sea fish species from New Zealand waters. J Sci Food Agric 34:388–392. doi:10.1002/jsfa.2740340411

    Article  CAS  Google Scholar 

  • Christie WW (2003) Lipid analysis. Isolation, separation, identification and structural analysis of lipids, 3rd edn. The Oily Press, Bridgwater, UK

  • Cohen DM, Rosenblatt RH, Moser HG (1990) Biology and description of a bythitid fish from deep-sea thermal vents in the tropical eastern Pacific. Deep Sea Res 37:267–283. doi:10.1016/0198-0149(90)90127-H

    Article  Google Scholar 

  • Comeault A, Stevens CJ, Juniper SK (2010) Mixed photosynthetic-chemosynthetic diets in vent obligate macroinvertebrates at shallow hydrothermal vents on Volcano 1, South Tonga Arc—evidence from stable isotope and fatty acid analyses. Cah Biol Mar 51:351–359

  • Copeman LA, Parrish CC, Brown JA, Harel M (2002) Effects of docosahexaenoic, eicosapentaenoic, and arachidonic acids on the early growth, survival, lipid composition and pigmentation of yellowtail flounder (Limanda ferruginea): a live food enrichment experiment. Aquaculture 210:285–304. doi:10.1016/S0044-8486(01)00849-3

    Article  CAS  Google Scholar 

  • Drazen JC, Phleger CF, Guest MA, Nichols PD (2009) Lipid composition and diet inferences in abyssal macrourids of the eastern North Pacific. Mar Ecol Prog Ser 387:1–14. doi:10.3354/meps08106

    Article  CAS  Google Scholar 

  • Dwyer KS, Parrish CC, Brown JA (2003) Lipid composition of yellowtail flounder (Limanda ferruginea) in relation to dietary lipid intake. Mar Biol 143:659–667. doi:10.1007/s00227-003-1101-0

    Article  CAS  Google Scholar 

  • El Razak AA, Ward AC, Glassey J (2014) Screening of marine bacterial producers of polyunsaturated fatty acids and optimisation of production. Microb Ecol 67:454–464. doi:10.1007/s00248-013-0332-y

    Article  Google Scholar 

  • Estévez A, Kanazawa A (1996) Fatty acid composition of neural tissues of normally pigmented and unpigmented juveniles of Japanese flounder using rotifer and Artemia enriched in n-3 HUFA. Fish Sci 62:88–93

    Google Scholar 

  • Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  Google Scholar 

  • Gebruk AV, Southward EC, Kennedy H, Southward AJ (2000) Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J Mar Biol Assoc UK 80:485–499

    Article  CAS  Google Scholar 

  • Geistdoerfer P (1999) Thermarces pelophilum, espèce nouvelle de Zoarcidae associée à l’émission de fluides froids au niveau du prisme d’accrétion de la barbade, Océan Atlantique Nord-Ouest. Cybium 23:5–11

    Google Scholar 

  • Guerreiro V, Narciso L, Almeida AJ, Biscoito M (2004) Fatty acid profiles of deep-sea fishes from the Lucky Strike and Menez Gwen hydrothermal vent fields (Mid-Atlantic ridge). Cybium 28:33–44

    Google Scholar 

  • Hamre K, Holen E, Moren M (2007) Pigmentation and eye migration in Atlantic halibut (Hippoglossus hippoglossus L.) larvae: new findings and hypotheses. Aquac Nutr 13:65–80. doi:10.1111/j.1365-2095.2007.00467.x

    Article  CAS  Google Scholar 

  • Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227. doi:10.1016/0163-7827(90)90002-3

    Article  CAS  Google Scholar 

  • Holmes WN, Donaldson EM (1969) The body compartments and the distribution of electrolytes. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol 1. Academic Press, New York, pp 1–89

    Google Scholar 

  • Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecol Monograph 74:211–235. doi:10.1890/02-4105

    Article  Google Scholar 

  • Kelly JR, Scheibling RE (2012) Fatty acids as dietary tracers in benthic food webs. Mar Ecol Prog Ser 446:1–22. doi:10.3354/meps09559

    Article  CAS  Google Scholar 

  • Legendre P, Legendre L (2012) Numerical ecology, 3rd English edition. Elsevier, Amsterdam

  • Levesque C, Limén H, Juniper SK (2005) Origin, composition and nutritional quality of particulate matter at deep-sea hydrothermal vents on Axial Volcano, NE Pacific. Mar Ecol Prog Ser 289:43–52. doi:10.3354/meps289043

    Article  Google Scholar 

  • Mayor DJ, Sharples CJ, Webster L, Walsham P, Lacaze J-P, Cousins NJ (2013) Tissue and size-related changes in the fatty acid and stable isotope signatures of the deep sea grenadier fish Coryphaenoides armatus from the Charlie-Gibbs Fracture Zone region of the Mid-AtlanticRidge. Deep Sea Res II 98:421–430. doi:10.1016/j.dsr2.2013.02.030

    Article  CAS  Google Scholar 

  • Meglen RR (1992) Examining large databases: a chemometric approach using principal component analysis. Mar Chem 39:217–237. doi:10.1016/0304-4203(92)90103-H

    Article  CAS  Google Scholar 

  • Munroe TA, Hashimoto J (2008) A new Western Pacific tonguefish (Pleuronectiformes: Cynoglossidae): the first pleuronectiform discovered at active hydrothermal vents. Zootaxa 1839:43–59

    Google Scholar 

  • Munroe TA, Tyler J, Tunnicliffe V (2011) Description and biological observations on a new species of deepwater symphurine tonguefish (Pleuronectiformes: Cynoglossidae: Symphurus) collected at Volcano 19, Tonga Arc, West Pacific Ocean. Zootaxa 3061:53–66

    Google Scholar 

  • Økland HMW, Stoknes IS, Remme JF, Kjerstad M, Synnes M (2005) Proximate composition, fatty acid and lipid class composition of the muscle from deep-sea teleosts and elasmobranchs. Comp Physiol Biochem B 140:437–443. doi:10.1016/j.cbpc.2004.11.008

    Article  Google Scholar 

  • Parrish CC, Deibel D, Thompson RJ (2009) Effect of sinking spring phytoplankton blooms on lipid content and composition in suprabenthic and benthic invertebrates in a cold ocean coastal environment. Mar Ecol Prog Ser 391:33–51. doi:10.3354/meps08148

    Article  CAS  Google Scholar 

  • Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Rešek E, Engelen A, Varela J (2012) Polyunsaturated fatty acids of marine macroalgae: potential for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935. doi:10.3390/md10091920

    Article  CAS  Google Scholar 

  • Pethybridge H, Bodin N, Arsenault-Pernet EJ, Bourdeix J-H, Brisset B, Bigot J-L, Roos D, Peter M (2014) Temporal and inter-specific variations in forage fish feeding conditions in the NW Mediterranean: lipid content and fatty acid compositional changes. Mar Ecol Prog Ser 512:39–54. doi:10.3354/meps10864

    Article  Google Scholar 

  • Petursdottir H, Gislason H, Falk-Petersen S (2008) Lipid classes and fatty acid compositions of muscle, liver and skull oil in deep-sea redfish Sebastes mentella over the Reykjanes Ridge. J Fish Biol 73:2485–2496. doi:10.1111/j.1095-8649.2008.02100.x

    Article  CAS  Google Scholar 

  • Phleger CF, Nelson MM, Groce AK, Cary SC, Coyne K, Gibson JAE, Nichols PD (2005) Lipid biomarkers of deep-sea hydrothermal vent polychaetes—Alvinella pompejana, A. caudata, Paralvinella grasslei and Hesiolyra bergii. Deep Sea Res I 52:2333–2352. doi:10.1016/j.dsr.2005.08.001

    Article  Google Scholar 

  • Pond DW, Segonzac M, Bell MV, Dixon DR, Fallick AE, Sargent JR (1997) Lipid and lipid carbon stable isotope composition of the hydrothermal vent shrimp Mirocaris fortunata: evidence for nutritional dependence on photosynthetically fixed carbon. Mar Ecol Prog Ser 157:221–231. doi:10.3354/meps157221

    Article  CAS  Google Scholar 

  • Pond DW, Pond DW, Bell MV, Dixon DR, Fallick AE, Segonzac M, Sargent JR (1998) Stable-carbon-isotope composition of fatty acids in hydrothermal vent mussels containing methanotrophic and thiotrophic bacterial endosymbionts. Appl Environ Microbiol 64:370–375

    CAS  Google Scholar 

  • Pond DW, Allen CE, Bell MV, Van Dover CL, Fallick AE, Dixon DR, Sargent JR (2002) Origins of long-chain polyunsaturated fatty acids in the hydrothermal vent worms Ridgeia piscesae and Protis hydrothermica. Mar Ecol Prog Ser 225:219–226. doi:10.3354/meps225219

    Article  CAS  Google Scholar 

  • Pond DW, Fallick AE, Stevens CJ, Morrison DJ, Dixon DR (2008) Vertebrate nutrition in a deep-sea hydrothermal vent ecosystem: fatty acid and stable isotope evidence. Deep Sea Res I 55:1718–1726. doi:10.1016/j.dsr.2008.07.006

    Article  Google Scholar 

  • Reñones O, Polunin NVC, Goni R (2002) Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis. J Fish Biol 61:122–137. doi:10.1111/j.1095-8649.2002.tb01741.x

    Article  Google Scholar 

  • Rosenblatt RH, Cohen DM (1986) Fishes living in deep-sea hydrothermal vents in the tropical eastern Pacific with description of a new genus and two new species of eelpout (Zoarcidae). Trans San Diego Soc Nat Hist 21:71–79

    Article  Google Scholar 

  • Saito H, Ishihara K, Murase T (1997) The fatty acid composition in tuna (Bonito, Euthynnus pelamis) caught at three different localities from tropics to temperate. J Sci Food Agric 73:53–59. doi:10.1002/(SICI)1097-0010(199701)73:1<53:AID-JSFA707>3.0.CO;2-5

    Article  CAS  Google Scholar 

  • Sancho G, Fisher CR, Mills S, Micheli F, Johnson GA, Lenihan HS, Peterson CH, Mullineaux LS (2005) Selective predation by the zoarcid fish Thermarces cerberus at hydrothermal vent sites. Deep Sea Res I 52:837–844. doi:10.1016/j.dsr.2004.12.002

    Article  Google Scholar 

  • Sargent JR, McEvoy LA, Bell JG (1997) Requirements, presentation and sources of polyunsaturated fatty acids in marine fish larval feeds. Aquaculture 155:117–127. doi:10.1016/S0044-8486(97)00122-1

    Article  CAS  Google Scholar 

  • Sargent JR, Bell G, McEvoy L, Tocher D, Estevez A (1999) Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177:191–199. doi:10.1016/S0044-8486(99)00083-6

    Article  CAS  Google Scholar 

  • Shields RJ, Bell JG, Luizi FS, Gara B, Bromage NR, Sargent JR (1999) Natural copepods are superior to enriched Artemia nauplii as feed for halibut larvae (Hippoglossus hippoglossus) in terms of survival, pigmentation and retinal morphology: relation to dietary essential fatty acids. J Nutr 129:1186–1194

    CAS  Google Scholar 

  • Stevens CJ, Limén H, Pond DW, Gélinas Y, Juniper SK (2008) Ontogenetic shifts in the trophic ecology of two alvinocaridid shrimp species at hydrothermal vents on the Mariana Arc, western Pacific Ocean. Mar Ecol Prog Ser 356:225–237. doi:10.3354/meps07270

    Article  CAS  Google Scholar 

  • Stevens CJ, Juniper SK, Limén H, Pond DW, Metaxas A, Gélinas Y (2015) Obligate hydrothermal vent fauna at East Diamante submarine volcano (Mariana Arc) exploit photosynthetic and chemosynthetic carbon sources. Mar Ecol Prog Ser 525:25–39. doi:10.3354/meps11229

    Article  CAS  Google Scholar 

  • Stowasser G, McAllen R, Pierce GJ, Collins MA, Moffat CF, Priede IG, Pond DW (2009) Trophic position of deep-sea fish—assessment through fatty acid and stable isotope analyses. Deep Sea Res I 56:812–826. doi:10.1016/j.dsr.2008.12.016

    Article  CAS  Google Scholar 

  • Tocher DR (2003) Metabolism and functions of lipids and fatty acids in teleost fish. Rev Fish Sci 11:107–184. doi:10.1080/713610925

    Article  CAS  Google Scholar 

  • Tunnicliffe V, Koop BF, Tyler J, So S (2010) Flatfish at seamount hydrothermal vents show strong genetic divergence between volcanic arcs. Mar Ecol 31:1–9. doi:10.1111/j.1439-0485.2010.00370.x

    Article  Google Scholar 

  • Tunnicliffe V, Tyler J, Dower J (2013) Population ecology of the tonguefish Symphurus thermophilus (Pisces; Pleuronectiformes; Cynoglossidae) at sulphur-rich hydrothermal vents on volcanoes of the northern Mariana Arc. Deep Sea Res II 92:172–182. doi:10.1016/j.dsr2.2013.01.026

    Article  Google Scholar 

  • Vlieg P, Body DR (1988) Lipid contents and fatty acid composition of some New Zealand freshwater finfish and marine finfish, shellfish, and roes. N Z J Mar Fresh Res 22:151–162. doi:10.1080/00288330.1988.9516287

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank the officers and crew of the R/V Sonne and R/V Natsushima, and the ROPOS and Hyper-Dolphin pilots for assistance with the collection of specimens. Dr. John Dower provided us with the specimens from Nikko and Daikoku submarine volcanoes. We appreciate the advice of Drs. Verena Tunnicliffe and Tom Munroe during the preparation of this manuscript. This work was supported by NSERC Canada grants to Dr. V. Tunnicliffe and SKJ, and an NSERC PDF fellowship to CJS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Catherine J. Stevens.

Additional information

Responsible Editor: C. Harrod.

Reviewed by Undisclosed experts.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stevens, C.J., Pond, D.W., Fallick, A.E. et al. Tissue-specific fatty acid profiles of vent-obligate tonguefishes (Symphurus spp.) on volcanic arcs in the western Pacific Ocean. Mar Biol 163, 164 (2016). https://doi.org/10.1007/s00227-016-2934-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-016-2934-7

Keywords

Navigation