Skip to main content

Advertisement

Log in

Trophic ecology of a deep-sea fish assemblage in the Northwest Atlantic

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

Abstract

Understanding the trophic ecology of deep-sea communities provides valuable insight into deep-water ecosystem functioning, and can help inform fisheries management and conservation initiatives. However, few deep-sea food webs have been studied so far in the Northwest Atlantic. Here, stable isotope, gut content, and morphometric analyses were combined to explore trophic relationships in a deep-water fish assemblage off eastern Canada. While a weak depth effect was found on the isotopic composition of the species analyzed, isotopic and dietary records revealed the existence of two main, strongly coupled trophic pathways. The pelagic pathway either comprised pelagic fishes (e.g., meso- and bathypelagic species), primarily feeding on zooplankton and fish, or benthopelagic predators that showed a more pelagic-oriented diet. Such fishes displayed the lowest values of stable N and C isotope ratios. In contrast, demersal fishes representing the benthic trophic pathway had significantly higher values of δ15N and δ13C, and a taxonomically more benthic-oriented and diverse diet. Furthermore, smaller body sizes, larger mouths, and adaptations (e.g., bioluminescent structures and lures) prevailed in the pelagic species, consistent with living in a relatively food-poor environment. The largest average body sizes were found in the demersal fishes suggesting enhanced food intake and growth investment for the species. Only juvenile individuals of threatened species, such as Coryphaenoides rupestris and Rajella fyllae were caught, providing evidence of the vulnerability of such species to commercial fishing.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altabet MA, Pilskaln CP, Thunell R, Pride C, Sigman D, Chavez F, Francois R (1999) The nitrogen isotope biogeochemistry of sinking particles from the margin of the Eastern North Pacific. Deep Sea Res I 46(4):655–679. doi:10.1016/S0967-0637(98)00084-3

    Article  CAS  Google Scholar 

  • Badalamenti F, D’Anna G, Pinnegar JK, Polunin NVC (2002) Size-related trophodynamic changes in three target fish species recovering from intensive trawling. Mar Biol 141:561–570. doi:10.1007/s00227-002-0844-3

    Article  Google Scholar 

  • Bailey DM, King NJ, Priede IG (2007) Cameras and carcasses: historical and current methods for using artificial food falls to study deep-water animals. Mar Ecol Prog Ser 350:179–191

    Article  Google Scholar 

  • Bailey DM, Collins MA, Gordon JDM, Zuur AF, Priede IG (2009) Long-term changes in deep-water fish populations in the Northeast Atlantic: a deeper reaching effect of fisheries? Proc R Soc B 276:1965–1969. doi:10.1098/rspb.2009.0098

    Article  CAS  Google Scholar 

  • Baillon S, Hamel J-F, Wareham VE, Mercier A (2012) Deep cold-water corals as nurseries for fish larvae. Front Ecol Environ 10(7):351–356. doi:10.1890/120022

    Article  Google Scholar 

  • Baillon S, Hamel J-F, Mercier A (2014) Diversity, distribution and nature of faunal associations with deep-sea pennatulacean corals in the Northwest Atlantic. PLoS One 9:e111519. doi:10.1371/journal.pone.0111519

    Article  Google Scholar 

  • Baker KD, Devine JA, Haedrich RL (2009) Deep-sea fishes in Canada’s Atlantic: population declines and predicted recovery times. Environ Biol Fish 85:79–88. doi:10.1007/s10641-009-9465-8

    Article  Google Scholar 

  • Baker KD, Haedrich RL, Snelgrove PVR, Wareham VE, Edinger EN, Gilkinson KD (2012) Small-scale patterns of deep-sea fish distributions and assemblages of the Grand Banks, Newfoundland continental slope. Deep Sea Res I 65:171–188. doi:10.1016/j.dsr.2012.03.012

    Article  Google Scholar 

  • Baker R, Buckland A, Sheaves M (2014) Fish gut content analysis: robust measures of diet composition. Fish Fish 15(1):170–177. doi:10.1111/faf.12026

    Article  Google Scholar 

  • Bergmann M, Dannheim J, Bauerfeind E, Klages M (2009) Trophic relationships along a bathymetric gradient at the deep-sea observatory HAUSGARTEN. Deep Sea Res I 56(3):408–424. doi:10.1016/j.dsr.2008.10.004

    Article  CAS  Google Scholar 

  • Bowering WR, Lilly GR (1992) Greenland halibut (Reinhardtius hippoglossoides) off southern Labrador and northeastern Newfoundland (Northwest Atlantic) feed primarily on capelin (Mallotus villosus). Neth J Sea Res 29(1–2):211–222. doi:10.1016/0077-7579(92)90021-6

    Article  Google Scholar 

  • Cabana G, Rasmussen JB (1996) Comparison of aquatic food chain using nitrogen isotopes. Proc Natl Acad Sci USA 93(20):10844–10847

    Article  CAS  Google Scholar 

  • Campbell N, Neat F, Burns F, Kunzlik P (2011) Species richness, taxonomic diversity, and taxonomic distinctness of the deep-water demersal fish community on the Northeast Atlantic continental slope (ICES Subdivision VIa). ICES J Mar Sci 68(2):365–376. doi:10.1093/icesjms/fsq070

    Article  Google Scholar 

  • Churchill DA, Heithaus MR, Vaudo JJ, Grubbs RD, Gastrich K, Castro JI (2015) Trophic interactions of common elasmobranchs in deep-sea communities of the Gulf of Mexico revealed through stable isotope and stomach content analysis. Deep Sea Res II 115:92–102. doi:10.1016/j.dsr2.2014.10.011

    Article  CAS  Google Scholar 

  • Clarke MW, Kelly CJ, Connolly PL, Molloy JP (2003) A life history approach to the assessment and management of deepwater fisheries in the Northeast Atlantic. J Northwest Atl Fish Sci 31:401–411

    Google Scholar 

  • Clarke J, Milligan RJ, Bailey DM, Neat FC (2015) A scientific basis for regulating deep-sea fishing by depth. Curr Biol 25:2425–2429. doi:10.1016/j.cub.2015.07.070

    Article  CAS  Google Scholar 

  • Coad BW, Reist JD (2004) Annotated list of the Arctic marine fishes of Canada. Can Manuscr Rep Fish Aquat Sci 2674:112

  • Conley WJ, Hopkins TL (2004) Feeding ecology of lanternfish (Pisces: Myctophidae) larvae: prey preferences as a reflection of morphology. Bull Mar Sci 75(3):361–379

    Google Scholar 

  • COSEWIC (Committee on the Status of Endangered Wildlife in Canada) (2016) Canadian species at risk. https://www.registrelep-sararegistry.gc.ca/sar/assessment/status_e.cfm. Accessed Mar 2017

  • Devine JA, Baker KD, Haedrich RL (2006) Fisheries: deep-sea fishes qualify as endangered. Nature 439:29. doi:10.1038/439029a

    Article  CAS  Google Scholar 

  • Drazen JC, Haedrich RL (2012) A continuum of life histories in deep-sea demersal fishes. Deep Sea Res I 61:34–42. doi:10.1016/j.dsr.2011.11.002

    Article  Google Scholar 

  • Drazen JC, Sutton TT (2017) Dining in the deep: the feeding ecology of deep-sea fishes. Annu Rev Mar Sci 9:337–366. doi:10.1146/annurev-marine-010816-060543

    Article  Google Scholar 

  • Drazen JC, Popp BN, Choy AC, Clemente T, De Forest L, Smith KL Jr (2008) Bypassing the abyssal benthic food web: macrourid diet in the eastern North Pacific inferred from stomach content and stable isotope analyses. Limnol Oceanogr 53(6):2644–2654. doi:10.4319/lo.2008.53.6.2644

    Article  Google Scholar 

  • Ebeling AW, Cailliet GM (1974) Mouth size and predator strategy of midwater fishes. Deep Sea Res Oceanogr Abstr 21(11):959–968. doi:10.1016/0011-7471(74)90028-X

    Article  Google Scholar 

  • Eliassen J-E, Jobling M (1985) Food of the roughhead grenadier, Macrourus berglax, Lacepede in North Norwegian waters. J Fish Biol 26(3):367–376. doi:10.1111/j.1095-8649.1985.tb04276.x

    Article  Google Scholar 

  • Froese R, Pauly D (2016) FishBase. http://www.fishbase.org. Accessed Mar 2017

  • Gale KSP, Hamel J-F, Mercier A (2013) Trophic ecology of deep-sea Asteroidea (Echinodermata) from eastern Canada. Deep Sea Res I 80:25–36. doi:10.1016/j.dsr.2013.05.016

    Article  CAS  Google Scholar 

  • Galván DE, Sweeting CJ, Reid WDK (2010) Power of stable isotope techniques to detect size-based feeding in marine fishes. Mar Ecol Prog Ser 407:271–278. doi:10.3354/meps08528

    Article  Google Scholar 

  • Gartner JV Jr, Crabtree RE, Sulak KJ (1997) Feeding at depth. In: Randall DJ, Farrell AP (eds) Deep sea fishes. Academic Press, New York, pp 115–194

    Chapter  Google Scholar 

  • Gerringer ME, Popp BN, Linley TD, Jamieson AJ, Drazen JC (2017) Comparative feeding ecology of abyssal and hadal fishes through stomach content and amino acid isotope analysis. Deep Sea Res II 121:110–120. doi:10.1016/j.dsr.2017.01.003

    Article  CAS  Google Scholar 

  • Godbold JA, Bailey DM, Collins MA, Gordon JDM, Spallek WA, Priede IG (2013) Putative fishery-induced changes in biomass and population size structures of demersal deep-sea fishes in ICES Sub-area VII, Northeast Atlantic Ocean. Biogeosciences 10:529. doi:10.5194/bg-10-529-2013

    Article  Google Scholar 

  • Gonzáles C, Román E, Paz X, Ceballos E (2006) Feeding habits and diet overlap of skates (Amblyraja radiata, A. hyperborea, Bathyraja spinicauda, Malacoraja senta and Rajella fyllae) in the North Atlantic. Report, NAFO SCR Doc 06/53, Ser N5285

  • Gordon JDM, Mauchline J (1996) The distribution and diet of the dominant, slope-dwelling eel, Synaphobranchus kaupi, of the Rockall Trough. J Mar Biol Assoc UK 76(2):493–503. doi:10.1017/S0025315400030691

    Article  Google Scholar 

  • Haedrich RL (1996) Deep-water fishes: evolution and adaptation in the earth’s largest living spaces. J Fish Biol 49:40–53. doi:10.1111/j.1095-8649.1996.tb06066.x

    Article  Google Scholar 

  • Hoffman JC, Sutton TT (2010) Lipid correction for carbon stable isotope analysis of deep-sea fishes. Deep Sea Res I 57(8):956–964. doi:10.1016/j.dsr.2010.05.003

    Article  CAS  Google Scholar 

  • Hulley P (2015) Alepocephalus bairdii. The IUCN Red List of Threatened Species 2015: e.T15147740A15147743. http://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T15147740A15147743.en. Accessed Mar 2017

  • Hussey NE, MacNeil MA, Olin JA, McMeans BC, Kinney MJ, Chapman DD, Fisk AT (2012) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. J Fish Biol 80(5):1449–1484. doi:10.1111/j.1095-8649.2012.03251.x

    Article  CAS  Google Scholar 

  • Hussey NE, Macneil MA, McMeans BC, Olin JA, Dudley SFJ, Cliff G, Wintner SP, Fennessy ST, Fisk AT (2014) Rescaling the trophic structure of marine food webs. Ecol Lett 17(2):239–250. doi:10.1111/ele.12226

    Article  Google Scholar 

  • Hynes HBN (1950) The food of fresh-water sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius), with a review of methods used in studies of the food of fishes. J Anim Ecol 19:36–58

    Article  Google Scholar 

  • Iken K, Brey T, Wand U, Voigt J, Junghans P (2001) Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Prog Oceanogr 50:383–405. doi:10.1016/S0079-6611(01)00062-3

    Article  Google Scholar 

  • Iken K, Bluhm BA, Gradinger R (2005) Food web structure in the high Arctic Canada Basin: evidence from δ13C and δ15N analysis. Polar Biol 28(3):238–249. doi:10.1007/s00300-004-0669-2

    Article  Google Scholar 

  • Iwamoto T (2015) Coryphaenoides rupestris. The IUCN Red List of Threatened Species 2015: e.T15522149A15603540. http://dx.doi.org/10.2305/IUCN.UK.2015-4.RLTS.T15522149A15603540.en. Accessed Mar 2017

  • Kim SL, Koch PL (2012) Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environ Biol Fish 95(1):53–63. doi:10.1007/s10641-011-9860-9

    Article  Google Scholar 

  • Kulka DW, Barker AS, Orlov A, Pasolini P (2009) Rajella fyllae. The IUCN Red List of Threatened Species 2009: e.T161587A5458368. http://dx.doi.org/10.2305/IUCN.UK.2009-2.RLTS.T161587A5458368.en. Accessed Mar 2017

  • Layman CA, Albrey Arrington D, Montana CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88(1):42–48

    Article  Google Scholar 

  • Mauchline J, Gordon JDM (1983) Diets of clupeoid, stomiatoid and salmonoid fish of the Rockall Trough, northeastern Atlantic Ocean. Mar Biol 77(1):67–78. doi:10.1007/BF00393211

    Article  Google Scholar 

  • Mauchline J, Gordon JDM (1984a) Occurrence and feeding of berycomorphid and percomorphid teleost fish in the Rockall Trough. ICES J Mar Sci 41(3):239–247. doi:10.1093/icesjms/41.3.239

    Article  Google Scholar 

  • Mauchline J, Gordon JDM (1984b) Diets and bathymetric distributions of the macrourid fish of the Rockall Trough, northeastern Atlantic Ocean. Mar Biol 81(2):107–121. doi:10.1007/BF00393109

    Article  Google Scholar 

  • Mauchline J, Gordon JDM (1985) Trophic diversity in deep-sea fish. J Fish Biol 26(5):527–535. doi:10.1111/j.1095-8649.1985.tb04293.x

    Article  Google Scholar 

  • McConnaughey T, McRoy CP (1979) Food-web structure and the fractionation of carbon isotopes in the Bering sea. Mar Biol 53:257–262. doi:10.1007/BF00952434

    Article  CAS  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48(5):1135–1140

    Article  CAS  Google Scholar 

  • Mindel BL, Webb TJ, Neat FC, Blanchard JL (2015) A trait-based metric sheds new light on the nature of the body size–depth relationship in the deep-sea. J Anim Ecol 85(2):427–436. doi:10.1111/1365-2656.12471

    Article  Google Scholar 

  • Mindel BL, Neat FC, Trueman CN, Webb TJ, Blanchard JL (2016) Functional, size and taxonomic diversity of fish along a depth gradient in the deep sea. PeerJ 4:e2387. doi:10.7717/peerj.2387

    Article  Google Scholar 

  • Mintenbeck K, Jacob U, Knust R, Arntz WE, Brey T (2007) Depth-dependence in stable isotope ratio δ15N of benthic POM consumers: the role of particle dynamics and organism trophic guild. Deep Sea Res I 54(6):1015–1023. doi:10.1016/j.dsr.2007.03.005

    Article  Google Scholar 

  • Murillo FJ, Muñoz PD, Altuna A, Serrano A (2011) Distribution of deep-water corals of the Flemish Cap, Flemish Pass, and the Grand Banks of Newfoundland (Northwest Atlantic Ocean): interaction with fishing activities. ICES J Mar Sci 68(2):319–332. doi:10.1093/icesjms/fsq071

    Article  Google Scholar 

  • Murillo FJ, Muñoz PD, Cristobo J, Ríos P, González C, Kenchington E, Serrano A (2012) Deep-sea sponge grounds of the Flemish Cap, Flemish Pass and the Grand Banks of Newfoundland (Northwest Atlantic Ocean): distribution and species composition. Mar Biol Res 8:842–854. doi:10.1080/17451000.2012.682583

    Article  Google Scholar 

  • Polunin NVC, Morales-Nin B, Pawsey WE, Cartes JE, Pinnegar JK, Moranta J (2001) Feeding relationships elucidated by stable nitrogen and carbon isotope data. Mar Ecol Prog Ser 220:13–23. doi:10.3354/meps220013

    Article  CAS  Google Scholar 

  • Post DM, Layman CA, Albrey Arrington D, Takimoto G, Quattrochi J, Montaña CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. doi:10.1007/s00442-006-0630-x

    Article  Google Scholar 

  • Reece JS, Metha RS (2013) Evolutionary history of elongation and maximum body length in moray eels (Anguilliformes: Murenidae). Biol J Linn Soc 109(4):861–875. doi:10.1111/bij.12098

    Article  Google Scholar 

  • Reid WDK, Wigham BD, McGill RAR, Polunin NVC (2012) Elucidating trophic pathways in benthic deep-sea assemblages of the Mid-Atlantic Ridge north and south of the Charlie–Gibbs Fracture Zone. Mar Ecol Prog Ser 463:89–103. doi:10.3354/meps09863

    Article  Google Scholar 

  • Reid WDK, Sweeting CJ, Wigham BD, McGill RAR, Polunin NVC (2013) High variability in spatial and temporal size-based trophodynamics of deep-sea fishes from the Mid-Atlantic Ridge elucidated by stable isotopes. Deep Sea Res II 98:412–420. doi:10.1016/j.dsr2.2013.01.020

    Article  CAS  Google Scholar 

  • Reiner F (1996) Catálogo dos peixes do arquipélago de Cabo Verde. Instituto Português de Investigação Marítima, Publicações Avulsas do IPIMAR, Lisbon, p 339

    Google Scholar 

  • Ribeiro MDO, Barreto Teresa F, Casatti L (2016) Use of functional traits to assess changes in stream fish assemblages across a habitat gradient. Neotrop Ichthyol 14:e140185. doi:10.1590/1982-0224-20140185

    Article  Google Scholar 

  • Rombouts I, Beaugrand G, Fizzala X, Gaill F, Greenstreet SPR, Lamare S, Le loc’h F, McQuatters-Gollop A, Mialet B, Niquil N (2013) Food web indicators under the Marine Strategy Framework Directive: from complexity to simplicity? Ecol Indic 29:246–254. doi:10.1016/j.ecolind.2012.12.021

    Article  Google Scholar 

  • Scharf FS, Juanes F, Rountree RA (2000) Prey size relationships of marine fish predators: interspecific variation and effects of ontogeny and body size on trophic-niche breadth. Mar Ecol Prog Ser 208:229–248. doi:10.3354/meps208229

    Article  Google Scholar 

  • Sherwood GD, Rose GA (2005) Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web. Estuar Coast Shelf Sci 63(4):537–549. doi:10.1016/j.ecss.2004.12.010

    Article  CAS  Google Scholar 

  • Sherwood OA, Jamieson RE, Edinger EN, Wareham VE (2008) Stable C and N isotopic composition of cold-water corals from the Newfoundland and Labrador continental slope: examination of trophic, depth and spatial effects. Deep Sea Res I 55(10):1392–1402. doi:10.1016/j.dsr.2008.05.013

    Article  CAS  Google Scholar 

  • Smith D, Gordon JDM, Priede IG (2010) Synaphobranchus kaupii. The IUCN Red List of Threatened Species 2010: e.T155246A4756653. http://dx.doi.org/10.2305/IUCN.UK.2010-4.RLTS.T155246A4756653.en. Accessed Mar 2017

  • Snelgrove P, Haedrich R (1985) Structure of the deep demersal fish fauna off Newfoundland. Mar Ecol Prog Ser 27:99–107. doi:10.3354/meps027099

    Article  Google Scholar 

  • Trueman CN, Johnston G, O’Hea B, MacKenzie KM (2014) Trophic interactions of fish communities at midwater depths enhance long-term carbon storage and benthic production on continental slopes. Proc R Soc B 281:20140669. doi:10.1098/rspb.2014.0669

    Article  Google Scholar 

  • Valls M, Sweeting CJ, Olivar MP, Fernández de Puelles ML, Pasqual C, Polunin NVC, Quetglas A (2014) Structure and dynamics of food webs in the water column on shelf and slope grounds of the western Mediterranean. J Mar Syst 138:171–181. doi:10.1016/j.jmarsys.2014.04.002

    Article  Google Scholar 

  • Walsh SJ, McCallum BR (1997) Performance of the Campelen 1800 shrimp trawl during the 1995 Northwest Atlantic Fisheries Centre autumn groundfish survey. NAFO Sci Coun Stud 29:105–116

    Google Scholar 

  • Ward AB, Mehta RS (2010) Axial elongation in fishes: using morphological approaches to elucidate developmental mechanisms in studying body shape. Integr Comp Biol 50(6):1106–1119. doi:10.1093/icb/icq029

    Article  Google Scholar 

Download references

Acknowledgements

The authors acknowledge financial support from the Natural Science and Engineering Research Council of Canada (NSERC) Discovery Grant (Grant no. 311406 to A. Mercier and 105379 to C.C. Parrish) and Canada Foundation for Innovation (CFI) Leaders Opportunity Fund (Grant no. 11231 to A. Mercier). The authors also want to thank the associate editor C. Harrod and the reviewers for their insightful comments and great contributions to this manuscript; the DFO staff, in particular D. Stansbury, K. Tipple, D. Pittman, V.E. Wareham, and M. Koen-Alonso for help with logistics and species identification; E. Montgomery for sample collection; A. Pye, J. Wells, U. Tilves, N. Ӧzdemír, K.S.P. Gale, L. Cárreon-Palau, R. Belley, and J. Ammendolia for technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Camilla Parzanini.

Ethics declarations

Conflict of interest

All the authors, CP, CCP, J-FH, AM, have approved the manuscript submitted and declared they have no conflicts of interest in regard to this work.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: C. Harrod.

Reviewed by C. Trueman and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Parzanini, C., Parrish, C.C., Hamel, JF. et al. Trophic ecology of a deep-sea fish assemblage in the Northwest Atlantic. Mar Biol 164, 206 (2017). https://doi.org/10.1007/s00227-017-3236-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3236-4

Navigation