Skip to main content

Advertisement

Log in

Factors affecting the importance of myctophids in the diet of the world’s seabirds

  • Review, concept, and synthesis
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Mesopelagic myctophid fish are a key component of the world’s ocean food webs, linking primary consumers and predators. Among marine predators, seabirds are globally significant consumers, but the extent to which they feed on myctophids has been investigated only at the regional scale. This global-scale review of analyses of the stomach contents of 228 seabird species reveals that the occurrence of myctophids in seabird diets is extremely variable. However, myctophids do constitute a considerable amount of the food of penguins, the Procellariidae (shearwaters/petrels, etc.), and storm-petrels; in locations where birds are foraging in oceanic basin/shelf slope habitat; and among birds that feed at night. Recent analyses of the fatty acid signature of stomach oil emphasize that myctophids can be important prey also for seabirds exploiting oceanic habitats. Current efforts to survey seabirds’ distribution outside the breeding period, when they often become more oceanic, and their circadian activity may further support the global importance of myctophids as a pathway for carbon advection between marine compartments.

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

Similar content being viewed by others

References

  • Ainley DG, Fraser WR, Sullivan CW, Torres JJ, Hopkins TL, Smith WO (1986) Antarctic mesopelagic micronekton: evidence from seabirds that pack ice affects community structure. Science 232:847–849

    Article  CAS  PubMed  Google Scholar 

  • Ainley DG, Fraser WR, Smith WO, Hopkins TL, Torres JJ (1991) The structure of upper level pelagic food webs in the Antarctic: effects of phytoplankton distribution. J Mar Syst 2:111–122

    Article  Google Scholar 

  • Ainley DG, Ribic CA, Fraser WR (1992) Does prey preference affect habitat choice in Antarctic seabirds? Mar Ecol Prog Ser 90:207–221

    Article  Google Scholar 

  • Anthony JA, Roby DD (1996) Variation in lipid content of forage fishes and its effect on energy provisioning rates to seabird nestlings. In: Forage fishes in marine ecosystems, University of Alaska Sea Grant College Program, report no. 97–01, pp 725–730

  • Ashmole NP (1971) Seabird ecology and the marine environment. Avian Biol 1:223–286

    Google Scholar 

  • Barrett RT, Camphuysen K, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Huppop O, Leopold MF, Montevecchi WA, Veit RR (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691

    Article  Google Scholar 

  • Battaglia P, Andaloro F, Consoli P, Esposito V, Malara D, Musolino S, Pedà C, Romeo T (2013) Feeding habits of the Atlantic bluefin tuna, Thunnus thynnus (L. 1758), in the central Mediterranean Sea (Strait of Messina). Helgol Mar Res 67:97–107

    Article  Google Scholar 

  • Beamish RJ, Leask KD, Ivanov OA, Balanov AA, Orlov AM, Sinclair B (1999) The ecology, distribution, and abundance of midwater fishes of the Subarctic Pacific gyres. Prog Oceanogr 43:399–442

    Article  Google Scholar 

  • Bécares J, García-Tarrasón M, Villero D, Bateman S, Jover L, García-Matarranz V, Sanpera C, Arcos JM (2015) Modelling terrestrial and marine foraging habitats in breeding Audouin’s Gulls Larus audouinii: timing matters. PLoS ONE 10(4):e0120799. https://doi.org/10.1371/journal.pone.0120799

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bost CA, Georges JY, Guinet C, Cherel Y, Pütz K, Charrassin JB, Handrich Y, Zorn T, Lage J, Le Maho Y (1997) Foraging habitat and food intake of satellite-tracked king penguins during the austral summer at Crozet Archipelago. Mar Ecol Prog Ser 150:21–33

    Article  Google Scholar 

  • Bost CA, Zorn T, Le Maho Y, Duhamel G (2002) Feeding of diving predators and diel vertical migration of prey: King penguins’ diet versus trawl sampling at Kerguelen Islands. Mar Ecol Progr Ser 227:51–61

    Article  Google Scholar 

  • Bost CA, Thiebot JB, Pinaud D, Cherel Y, Trathan PN (2009) Where do penguins go during the inter-breeding period? Using geolocation to track the winter dispersion of the macaroni penguin. Biol Lett 5:473–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bridge ES, Thorup K, Bowlin MS, Chilson PB, Diehl RH, Fleron RW, Hartl P, Kays R, Kelly JF, Robinson WD, Wikelski M (2011) Technology on the move: recent and forthcoming innovations for tracking migratory birds. Bioscience 61:689–698

    Article  Google Scholar 

  • Catry P, Phillips RA, Phalan B, Silk JRD, Croxall JP (2004) Foraging strategies of grey-headed albatrosses Thalassarche chrysostoma: integration of movements, activity and feeding events. Mar Ecol Prog Ser 280:261–273

    Article  Google Scholar 

  • Catul V, Gauns M, Karuppasamy PK (2011) A review on mesopelagic fishes belonging to family Myctophidae. Rev Fish Biol Fish 21:339–354

    Article  Google Scholar 

  • Chaurand T, Weimerskirch H (1994) The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea: a previously undescribed strategy of food provisioning in a pelagic seabird. J Anim Ecol 63:275–282

    Article  Google Scholar 

  • Cherel Y, Ridoux V (1992) Prey species and nutritional value of food fed during summer to King Penguin Aptenodytes patagonicus chicks at Possession Island, Crozet Archipelago. Ibis 134:118–127

    Article  Google Scholar 

  • Cherel Y, Verdon C, Ridoux V (1993) Seasonal importance of oceanic myctophids in king penguin diet at Crozet Islands. Polar Biol 13:355–357

    Google Scholar 

  • Cherel Y, Hobson KA, Guinet C, Vanpe C (2007) Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. J Anim Ecol 76:826–836

    Article  PubMed  Google Scholar 

  • Cherel Y, Fontaine C, Richard P, Labat JP (2010) Isotopic niches and trophic levels of myctophid fishes and their predators in the Southern Ocean. Limnol Oceanogr 55:324–332

    Article  CAS  Google Scholar 

  • Clarke A, Prince PA (1976) The origin of stomach oil in marine birds: analyses of the stomach oil from six species of subantarctic procellariiform seabirds. J Exp Mar Biol Ecol 23:15–30

    Article  CAS  Google Scholar 

  • Clarke MR, Prince PA (1980) Chemical composition and calorific value of food fed to mollymauk chicks Diomedea melanophris and D. chrysostoma at Bird Island, South Georgia. Ibis 122:488–494

    Article  Google Scholar 

  • Cleeland JB, Lea M-A, Hindell MA (2014) Use of the southern ocean by breeding short-tailed shearwaters (Puffinus tenuirostris). J Exp Mar Biol Ecol 450:109–117

    Article  Google Scholar 

  • Collins MA, Xavier JC, Johnston NM, North AW, Enderlein P, Tarling GA, Waluda CM, Hawker EJ, Cunningham NJ (2008) Patterns in the distribution of myctophid fish in the northern Scotia Sea ecosystem. Polar Biol 31:837–851

    Article  Google Scholar 

  • Connan M, Mayzaud P, Boutoute M, Weimerskirch H, Cherel Y (2005) Lipid composition of stomach oil in a procellariiform seabird Puffinus tenuirostris: implications for food web studies. Mar Ecol Prog Ser 290:277–290

    Article  CAS  Google Scholar 

  • Connan M, Cherel Y, Mabille G, Mayzaud P (2007a) Trophic relationships of white-chinned petrels from Crozet Islands: combined stomach oil and conventional dietary analyses. Mar Biol 152:95–107

    Article  CAS  Google Scholar 

  • Connan M, Cherel Y, Mayzaud P (2007b) Lipids from stomach oil of procellariiform seabirds document the importance of myctophid fish in the Southern Ocean. Limnol Oceanogr 52(2007):2445–2455

    Article  CAS  Google Scholar 

  • Connan M, Mayzaud P, Trouvé C, Barbraud C, Cherel Y (2008) Interannual dietary changes and demographic consequences in breeding blue petrels from Kerguelen Islands. Mar Ecol Prog Ser 373:123–135

    Article  CAS  Google Scholar 

  • Croxall JP, Lishman GS (1987) The food and feeding ecology of penguins. In: Croxall JP (ed) Seabirds, feeing ecology and role in marine ecosystems. Cambridge University Press, Cambridge, pp 101–133

    Google Scholar 

  • Croxall JP, McCann TS, Prince PA, Rothery P (1988) Reproductive performance of seabirds and seals at South Georgia and Signy Island, South Orkney Islands, 1976–1987: implications for Southern Ocean monitoring studies. In: Sahrhage D (ed) Antarctic Ocean and resources variability. Springer, Berlin, pp 261–285

    Chapter  Google Scholar 

  • Croxall JP, Prince PA, Reid K (1997) Dietary segregation of krill-eating South Georgian seabirds. J Zool Lond 242:531–556

    Article  Google Scholar 

  • Daly KL (1990) Overwintering development, growth, and feeding of larval Euphausia superba in the Antarctic marginal ice zone. Limnol Oceanogr 35:1564–1576. https://doi.org/10.4319/lo.1990.35.7.1564

    Article  Google Scholar 

  • Davis ND, Myers KW, Ishida Y (1998) Caloric value of high-seas salmon prey organisms and simulated salmon ocean growth and prey consumption. N Pac Anadr Fish Comm Bull 1:146–162

    Google Scholar 

  • de Brooke ML (2004a) The food consumption of the world’s seabirds. Proc R Soc B 271:S246–S248

    Article  PubMed Central  Google Scholar 

  • de Brooke ML (2004b) Albatrosses and petrels across the world. Oxford University Press, Oxford, p 499

    Google Scholar 

  • Development Core Team R (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Dias MP, Granadeiro JP, Catry P (2012) Working the day or the night shift? Foraging schedules of Cory’s shearwaters vary according to marine habitat. Mar Ecol Prog Ser 467:245–252. https://doi.org/10.3354/meps09966

    Article  Google Scholar 

  • Donnelly J, Torres JJ, Sutton TT, Simoniello C (2004) Fishes of the eastern Ross Sea, Antarctica. Polar Biol 27:637–650

    Article  Google Scholar 

  • Egevang C, Stenhouse IJ, Phillips RA, Petersen A, Fox JW, Silk JR (2010) Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proc Natl Acad Sci USA 107:2078–2081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Einoder LD, Page B, Goldsworthy SD, De Little SC, Bradshaw CJA (2010) Exploitation of distant Antarctic waters and close neritic waters by Short-tailed Shearwaters breeding in South Australia. Austral Ecol 36:461–475

    Article  Google Scholar 

  • Einoder L, Page B, Goldsworthy SD (2013) Feeding strategy of the short-tailed shearwater vary by year and sea-surface temperature but do not affect breeding success. Condor 115:777–787

    Article  Google Scholar 

  • Frederiksen M, Moe B, Daunt F, Phillips RA, Barrett RT, Bogdanova MI, Boulinier T, Chardine JW, Chastel O, Chivers LS, Christensen-Dalsgaard S, Clément-Chastel C, Colhoun K, Freeman R, Gaston AJ, González-Solís J, Goutte A, Grémillet D, Guilford T, Jensen GH, Krasnov Y, Lorentsen SH, Mallory ML, Newell M, Olsen B, Shaw D, Steen H, Strøm H, Systad GH, Thórarinsson TL, Anker-Nilssen T (2012) Multicolony tracking reveals the winter distribution of a pelagic seabird on an ocean basin scale. Divers Distrib 18:530–542

    Article  Google Scholar 

  • Gaston AJ, Jones IL (1998) The Auks. Oxford University Press, Oxford, p 340

    Google Scholar 

  • Gjøsaeter J, Kawaguchi K (1980) A review of the world resources of mesopelagic fish. FAO Fish Tech Paper 193:1–151

    Google Scholar 

  • Hamer KC, Schreiber EA, Burger J (2002) Breeding biology, life histories, and life history environment interactions in seabirds. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, pp 217–261

    Google Scholar 

  • Harper P (1987) Feeding behaviour and other notes on 20 species of Procellariiformes at sea. Notornis 34:169–192

    Google Scholar 

  • Harrison CS, Hida TS, Seki MP (1983) Hawaiian seabird feeding ecology. Wildl Monogr 85:1–71

    Google Scholar 

  • Hayes BP, de Brooke ML (1990) Retinal ganglion cell distribution and behaviour in procellariiform seabirds. Vision Res 30:1277–1289

    Article  CAS  PubMed  Google Scholar 

  • Hedd A, Gales R, Brothers N (2001) Foraging strategies of shy albatross Thalassarche cauta breeding at Albatross Island, Tasmania, Australia. Mar Ecol Prog Ser 224:267–282

    Article  Google Scholar 

  • Hill SL, Murphy EJ, Reid K, Trathan PN, Constable AJ (2006) Modelling Southern Ocean ecosystems: krill, the food-web, and the impacts on harvesting. Biol Rev 81:581–608

    Article  CAS  PubMed  Google Scholar 

  • Hilton GM, Furness W, Houston DC (2000) A comparative study of digestion in North Atlantic seabirds. J Avian Biol 31:36–46

    Article  Google Scholar 

  • Hopkins T, Sutton TT, Lancraft TM (1996) The trophic and predation impact of a low latitude midwater fish assemblage. Prog Oceanogr 38:205–239

    Article  Google Scholar 

  • Hudson JM, Steinberg DK, Sutton TT, Graves JE, Latour RJ (2014) Myctophid feeding ecology and carbon transport along the northern Mid-Atlantic Ridge. Deep-Sea Res Part I 93:104–116

    Article  Google Scholar 

  • Hulley PA (1995) Lanternfishes. In: Paxton JR, Eschmeyer WN (eds) Encyclopedia of fishes. Academic Press, San Diego, pp 127–128

    Google Scholar 

  • Ichii T, Bengston JL, Boveng PL, Takao Y, Jansen JK, Hiruki-Raring LM, Cameron MF, Okamura H, Hayashi T, Naganobu M (2007) Provisioning strategies of Antarctic fur seals and chinstrap penguins produce different responses to distribution of common prey and habitat. Mar Ecol Prog Ser 344:277–297

    Article  Google Scholar 

  • Imber M (1976) The origin of petrel stomach oils—a review. Condor 78:366–369

    Article  Google Scholar 

  • Irigoien X, Klevjer TA, Røstad A, Martinez U, Boyra G, Acuña JL, Bode A, Echevarria F, Gonzalez-Gordillo JI, Hernandez-Leon S, Agusti S, Aksnes DL, Duarte CM, Kaartvedt S (2014) Large mesopelagic fishes biomass and trophic efficiency in the open ocean. Nat Commun 5:3271. https://doi.org/10.1038/ncomms4271

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diet. Ecol Monogr 74:211–235

    Article  Google Scholar 

  • Iverson SJ, Springer AM, Kitaysky AS (2007) Seabirds as indicators of food web structure and ecosystem variability: qualitative and quantitative diet analyses using fatty acids. Mar Ecol Prog Ser 352:235–244

    Article  CAS  Google Scholar 

  • Jackson S, Ryan PG (1986) Differential digestion rates of prey by white-chinned petrels (Procellaria aequinoctialis). Auk 103:617–619

    Google Scholar 

  • Jacob J (1982) Stomach oils. In: Fraser DS, King JR, Parkes KC (eds) Avian biology, vol VI. Academic Press Inc, Orland, pp 325–340

    Chapter  Google Scholar 

  • Jessopp MJ, Cronin M, Doyle TK, Wilson M, McQuatters-Gollop A, Newton S, Phillips RA (2013) Transatlantic migration by post-breeding puffins: a strategy to exploit a temporarily abundant food resource? Mar Biol 160:2755–2762

    Article  Google Scholar 

  • Käkelä R, Käkelä A, Martínez-Abraín A, Sarzo B, Louzao M, Gerique C, Villuendas E, Strandberg U, Furness RW, Oro D (2010) Fatty acid signature analysis confirm foraging resources of globally endangered Mediterranean seabird species: calibration test and application to the wild. Mar Ecol Prog Ser 398:245–258

    Article  CAS  Google Scholar 

  • Karnovsky NJ, Hobson KA, Iverson SJ (2012) From lavage to lipids: estimating diets of seabirds. Mar Ecol Prog Ser 451:263–284

    Article  CAS  Google Scholar 

  • Kirkwood R, Robertson G (1997) The foraging ecology of female emperor penguins in winter. Ecol Monogr 67:155–176

    Article  Google Scholar 

  • Klevjer TA, Irigoien X, Røstad A, Fraile-Nuez E, Benítez-Barrios VM, Kaartvedt S (2016) Large scale patterns in vertical distribution and behaviour of mesopelagic scattering layers. Sci Rep 6:19873. https://doi.org/10.1038/srep19873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klomp NI, Schultz MA (2000) Short-tailed shearwaters breeding in Australia forage in Antarctic waters. Mar Ecol Prog Ser 194:307–310

    Article  Google Scholar 

  • Kokubun N, Yamamoto T, Kikuchi DM, Kitaysky A, Takahashi A (2016) Nocturnal foraging by red-legged kittiwakes, a surface feeding seabird that relies on deep water prey during reproduction. PLoS ONE 10:e0138850. https://doi.org/10.1371/journal.pone.0138850

    Article  CAS  Google Scholar 

  • Kooyman GL (1989) Divers divers. Springer, Berlin, p 200

    Book  Google Scholar 

  • Kubodera T, Watanabe H, Ichii T (2007) Feeding habits of the blue shark, Prionace glauca, and salmon shark, Lamna ditropis, in the transition region of the Western North Pacific. Rev Fish Biol Fisheries 17:111–124

    Article  Google Scholar 

  • Kurasawa K, Itabashi Y, Yamamoto M, Watanuki Y (2012) Prey of streaked shearwaters during long foraging trips estimated by fatty acid composition of the stomach oil. Jpn J Ornithol 61:137–141

    Article  Google Scholar 

  • Le Corre M, Jaeger A, Pinet P, Kappes MA, Weimerskirch H, Catry T, Ramos JA, Russell JC, Shah N, Jaquemet S (2012) Tracking seabirds to identify potential marine protected areas in the tropical Indian Ocean. Biol Cons 156:83–93

    Article  Google Scholar 

  • Lorrain A, Arguelles J, Alegre A, Bertrand A, Munaron J-M, Richard P, Cherel Y (2011) Sequential isotopic signature along gladius highlights contrasted individual foraging strategies of Jumbo squid (Dosidicus gigas). PLoS ONE 6(7):e22194. https://doi.org/10.1371/journal.pone.0022194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lubimova T, Shust K, Popkov V (1987) Specific features in the ecology of Southern Ocean mesopelagic fish of the family Myctophidae. Biological resources of the Arctic and Antarctic (collected papers), vol 320. Nauka Press, Moscow, p 337

    Google Scholar 

  • Mackley EK, Phillips RA, Silk JRD, Wakefield ED, Afanasyev V, Furness RW (2011) At-sea activity patterns of breeding and non-breeding white-chinned petrels Procellaria aequinoctialis from South Georgia. Mar Biol 158:429–438

    Article  Google Scholar 

  • Markaida U, Sosa-Nishizaki O (2010) Food and feeding habits of the blue shark Prionace glauca caught off Ensenada, Baja California, Mexico, with a review on its feeding. J Mar Biol Assoc UK 90:977–994

    Article  Google Scholar 

  • Marra PP, Cohen EB, Loss SR, Rutter JE, Tonra CM (2015) A call for full annual cycle research in animal ecology. Biol Lett 11:20150552

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Matsumoto K, Oka N, Ochi D, Muto F, Satoh TP, Watanuki Y (2012) Foraging behavior and diet of Streaked Shearwaters (Calonectris leucomelas) rearing chicks at Mikura I. Ornithol Sci 11:9–19

    Article  Google Scholar 

  • Moku M, Kawaguchi K, Watanabe H, Ohno A (2000) Feeding habits of three dominant myctophid fishes, Diaphus theta, Stenobrachius leucopsarus and S. mannochir, in the subarctic and transitional waters of the western North Pacific. Mar Ecol Prog Ser 207:129–140

    Article  Google Scholar 

  • Moseley C, Grémillet D, Connan M, Ryan PG, Mullers RHE, van der Lingen CD, Miller TW, Coetzee JC, Crawford RJM, Sabarros P, McQuaid CD, Pichegru L (2012) Foraging ecology and ecophysiology of Cape gannets from colonies in contrasting feeding environments. J Exp Mar Biol Ecol 422–423:29–38

    Article  Google Scholar 

  • Moteki M, Koubbi P, Pruvost P, Tavernier E, Hulley PA (2011) Spatial distribution of pelagic fish off Adélie and George V Land, East Antarctica in the austral summer 2008. Polar Sci 5:211–224

    Article  Google Scholar 

  • Murphy EJ, Watkins JL, Trathan PN, Reid K, Meredith MP, Thorpe SE, Johnston NM, Clarke A, Tarling GA, Collins MA, Forcada J, Shreeve RS, Atkinson A, Korb R, Whitehouse MJ, Ward P, Rodhouse PG, Enderlein P, Hirst AG, Martin AR, Hill SL, Staniland IJ, Pond DW, Briggs DR, Cunningham NJ, Fleming AH (2007) Spatial and temporal operation of the Scotia Sea ecosystem: a review of large-scale links in a krill centred food web. Phil Trans R Soc B 362:113–148

    Article  CAS  PubMed  Google Scholar 

  • Navarro J, Cardador L, Brown R, Phillips RA (2015) Spatial distribution and ecological niches of non-breeding planktivorous petrels. Sci Rep 5:12164

    Article  PubMed  PubMed Central  Google Scholar 

  • Nelson JB (2005) Pelicans, cormorants and their relatives. Oxford University Press, Oxford, p 661

    Google Scholar 

  • Neves VC, Bried J, González-Solís J, Roscales JL, Clarke MR (2012) Feeding ecology and movements of the Barolo shearwater Puffinus baroli baroli in the Azores, NE Atlantic. Mar Ecol Prog Ser 452:269–285. https://doi.org/10.3354/meps09670

    Article  Google Scholar 

  • Ohizumi H, Yoshioka M, Mori K, Miyazaki N (1998) Stomach contents of common dolphins (Delphinus delphis) in the pelagic western North Pacific. Mar Mammal Sci 14:835–844

    Article  Google Scholar 

  • Ohizumi H, Kuramochi T, Amano M, Miyazaki N (2000) Prey switching of Dall’s porpoise Phocoenoides dalli with population decline of Japanese pilchard Sardinops melanostictus around Hokkaido, Japan. Mar Ecol Prog Ser 200:265–275

    Article  Google Scholar 

  • Orben RA, Irons DB, Paredes R, Roby DD, Phillips RA, Shaffer SA (2015) North or south? Niche separation of endemic red-legged kittiwakes and sympatric black-legged kittiwakes during their non-breeding migrations. J Biogeogr 42:401–412

    Article  Google Scholar 

  • Pakhomov EA, Perissinotto R, McQuaid CD (1996) Prey composition and daily rations of myctophid fishes in the Southern Ocean. Mar Ecol Prog Ser 134:1–14

    Article  Google Scholar 

  • Paredes R, Orben RA, Suryan RM, Irons DB, Roby DD, Harding AMA, Young RC, Benoit-Bird K, Ladd C, Renner H, Heppell S, Phillips RA, Kitaysky A (2014) Foraging responses of Black-legged Kittiwakes to prolonged food-shortages around colonies on the Bering Sea shelf. PLoS ONE 9(3):e92520. https://doi.org/10.1371/journal.pone.0092520

    Article  PubMed  PubMed Central  Google Scholar 

  • Pepin P (2013) Distribution and feeding of Bethosema glaciale in the western Labrador Sea: Fish-zooplankton interaction and the consequence to calanoid copepod populations. Deep-Sea Res Part I 75:119–134

    Article  Google Scholar 

  • 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 409:290–299

    Article  Google Scholar 

  • Pethybridge H, Virtue P, Casper R, Yoshida T, Green CP, Jackson G, Nichols PD (2012) Seasonal variations in diet of arrow squid (Nototodarus gouldi): stomach content and signature fatty acid analysis. J Mar Biol Assoc UK 92:187–196

    CAS  Google Scholar 

  • Phalan B, Phillips RA, Silk JRD, Afanasyev V, Fukuda A, Fox J, Catry P, Higuchi H, Croxall JP (2007) Foraging behaviour of four albatross species by night and day. Mar Ecol Prog Ser 340:271–286

    Article  Google Scholar 

  • Phillips RA, Catry P, Silk JRD, Bearhop S, McGill R, Afanasyev V, Strange IJ (2007) Movements, winter distribution and activity patterns of Falkland and brown skuas: insights from loggers and isotopes. Mar Ecol Prog Ser 345:281–291

    Article  Google Scholar 

  • Pollet IL, Hedd A, Taylor PD, Montevecchi WA, Shutler D (2014) Migratory movements and wintering areas of Leach’s Storm-Petrels tracked using geolocators. J Field Ornithol 85:321–328

    Article  Google Scholar 

  • Prince PA, Morgan RA (1987) Diet and feeding ecology of Procellariiformes. In: Croxall JP (ed) Seabirds, feeing ecology and role in marine ecosystems. Cambridge University Press, Cambridge, pp 135–171

    Google Scholar 

  • Pusch C, Hulley PA, Kock KH (2004) Community structure and feeding ecology of mesopelagic fishes in the slope waters of King George Island (South Shetland Island, Antarctica). Deep-Sea Res Part 1(51):1685–1708

    Article  Google Scholar 

  • Quillfeldt P, Masello JF, Brickle P, Martin-Creuzburg D (2011) Fatty acid signatures of stomach contents reflect inter- and intra-annual changes in diet of a small pelagic seabird, the Thin-billed prion Pachyptila belcheri. Mar Biol 158:1805–1813

    Article  CAS  Google Scholar 

  • Raclot T, Groscolas R, Cherel Y (1998) Fatty acid evidence for the importance of myctophid fishes in the diet of King Penguins, Aptenodytes patagonicus. Mar Biol 132:523–533

    Article  Google Scholar 

  • Ranconi RA, Koopman HN, McKinstry CAE, Wong SNP, Westgate AJ (2010) Inter-annual variability in diet of non-breeding pelagic seabirds Puffinus spp. at migratory staging areas: evidence from stable isotope and fatty acids. Mar Ecol Prog Ser 419:267–282

    Article  Google Scholar 

  • Ratcliffe N, Trathan P (2011) A review of the diet and at-sea distribution of penguins breeding within the CAMLR convention area. CCAMLR Sci 18:75–114

    Google Scholar 

  • Rau GH, Ainley DG, Bengtson JL, Torres JJ, Hopkins TL (1992) 15N/14N and 13C/12C in Weddell Sea birds, seals, and fish: implications for diet and trophic structure. Mar Ecol Prog Ser 84:1–8

    Article  CAS  Google Scholar 

  • Raya Rey A, Trathan PN, Pütz K, Schiavini A (2007) Effect of oceanographic conditions on the winter movements of rockhopper penguins Eudyptes chrysocome chrysocome from Staten Island, Argentina. Mar Ecol Prog Ser 330:285–295

    Article  Google Scholar 

  • Raymond B, Lea M-A, Patterson T, Andrew-Goff V, Sharples R, Charrassin JB, Cottin M, Emmerson L, Gales N, Gales R, Goldsworthy SD, Harcourt R, Kato A, Kirkwood R, Lawton K, Ropert-Coudert Y, Southwell C, van den Hoff J, Wienecke B, Woehler EJ, Wotherspoon S, Hindell MA (2016) Important marine habitat off east Antarctica revealed by two decades of multi-species predator tracking. Ecography 38:121–129

    Article  Google Scholar 

  • Renner HM, Mueter F, Drummond BA, Warzybok JA, Sinclair EH (2012) Patterns of change in diets of two piscivorous seabird species during 35 years in the Pribilof Islands. Deep-Sea Res Part II 65–70:273–291

    Article  Google Scholar 

  • Ridoux V (1994) The diets and dietary segregation of seabirds at the subantarctic Crozet Islands. Mar Ornithol 22:1–192

    Google Scholar 

  • Rodhouse PG, Nigmatullin CM (1996) Role as consumers. Phil Trans R Soc B 351:1003–1022

    Article  Google Scholar 

  • Rubolini D, Maggini I, Ambrosini R, Imperio S, Paiva VH, Gaibani G, Saino N, Cecere JG (2015) The effect of moonlight on Scopoli’s shearwater Calonectris diomedea colony attendance patterns and nocturnal foraging: a test of the foraging efficiency hypothesis. Ethology 121:284–299

    Article  Google Scholar 

  • Sabourenkov EN (1991) Mesopelagic fish of the Southern Ocean—summary results of recent Soviet studies. CCAMLR Sel Sci Papers 1990:433–457

    Google Scholar 

  • Sassa C, Kawaguchi K (2004) Larval feeding habits of Diaphus garmani and Myctophum asperum (Pisces: Myctophidae) in the transition region of the western North Pacific. Mar Ecol Progr Ser 278:279–290

    Article  Google Scholar 

  • Saunders RA, Collins MA, Ward P, Stowasser G, Hill SL, Shreeve R, Tarling GA (2015) Predatory impact of the myctophid fish community on zooplankton in the Scotia Sea (Southern Ocean). Mar Ecol Prog Ser 541:45–64

    Article  CAS  Google Scholar 

  • Saunders RA, Collins MA, Stowasser G, Tarling GA (2017) Southern Ocean mesopelagic fish communities in the Scotia Sea are substained by mass immigration. Mar Ecol Prog Ser 569:173–185

    Article  Google Scholar 

  • Schealer DA (2002) Foraging behavior and food of seabirds. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, pp 137–177

    Google Scholar 

  • Schneider D, Hunt GL Jr (1984) A comparison of seabird diets and foraging distribution around the Pribilof Islands, Alaska. In: DN Nettleship, GA Sanger, PF Springer (eds) Marine birds: their feeding ecology and commercial fisheries relationships. Can Wildl Serv Spec Publ 86–95

  • Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358

    Article  Google Scholar 

  • Schreiber EA, Burger J (2001) Biology of marine birds, vol Appendix 2. CRC Press, Boca Raton, pp 665–685

    Google Scholar 

  • Sinclair EH, Vlietstra LS, Johnson DS, Zeppelin TK, Byrd GV, Springer AM, Ream RR, Hunt GL Jr (2008) Patterns in prey use among fur seals and seabirds in the Pribilof Islands. Deep-Sea Res II 55:1897–1918

    Article  Google Scholar 

  • Spear LB, Ainley DG, Walker WA (2007) Foraging dynamics of seabirds in the eastern tropical Pacific Ocean. Stud Avian Biol 35:1–99

    Google Scholar 

  • Storer RW (1987) The possible significance of large eyes in the red-legged kittiwake. Condor 89:192–194

    Article  Google Scholar 

  • Thiebot JB, Lescroël A, Pinaud D, Trathan PN, Bost CA (2011) Larger foraging range but similar habitat selection in non-breeding versus breeding sub-Antarctic penguins. Antarct Sci 23:117–126

    Article  Google Scholar 

  • Thiebot JB, Delord K, Marteau C, Weimerskirch H (2014) Stage-dependent distribution of the critically endangered Amsterdam albatross in relation to economic exclusive zones. Endang Spec Res 23:263–276

    Article  Google Scholar 

  • Thiers L, Delord K, Barbraud C, Phillips RA, Pinaud D, Weimerskirch H (2014) Foraging zones of the two sibling species of giant petrels in the Indian Ocean throughout the annual cycle: implication for their conservation. Mar Ecol Prog Ser 499:233–248

    Article  Google Scholar 

  • Tierney M, Nichols PD, Wheatley KE, Hindell MA (2008) Blood fatty acids indicate inter- and intra-annual variation in the diet of Adélie penguins: comparison with stomach content and stable isotope analysis. J Exp Mar Biol Ecol 367:65–74

    Article  CAS  Google Scholar 

  • Vipin PM, Ravi R, Fernandez TJ, Pradeep K, Boopendranath MR, Remesan MP (2012) Distribution of myctophid resources in the Indian Ocean. Rev Fish Biol Fish 22:423–436. https://doi.org/10.1007/s11160-011-9244-4

    Article  Google Scholar 

  • Waluda CM, Hill SL, Peat HJ, Trathan PN (2012) Diet variability and reproductive performance of macaroni penguins Eudyptes chrysolophus at Bird Island, South Georgia. Mar Ecol Prog Ser 466:261–274

    Article  Google Scholar 

  • Wang SW, Hollmen TE, Iverson SJ (2010) Validating quantitative fatty acid signature analysis to estimate diets of spectacled and Steller’s eiders (Somateria fischeri and Polystica stelleri). J Comp Physiol B 180:125–139

    Article  CAS  PubMed  Google Scholar 

  • Watanabe H, Moku M, Kawaguchi K, Ishimaru K, Ohno A (1999) Diel vertical migration of myctophid fishes (family Myctophidae) in the transitional waters of the western North Pacific. Fish Oceanogr 8:115–127

    Article  Google Scholar 

  • Weimerskirch H, Cherel Y (1998) Feeding ecology of short-tailed shearwaters: breeding in Tasmania and foraging in Antarctica? Mar Ecol Prog Ser 167:261–274

    Article  Google Scholar 

  • Weimerskirch H, Guionnet T (2002) Comparative activity pattern during foraging of four albatross species. Ibis 144:40–50

    Article  Google Scholar 

  • Weimerskirch H, Wilson RP (2000) Oceanic respite for wandering albatrosses. Nature 406:955–956

    Article  CAS  PubMed  Google Scholar 

  • Weimerskirch H, Gault A, Cherel Y (2005) Prey distribution and patchiness: factors in foraging success and efficiency of wandering albatrosses. Ecology 86:2611–2622

    Article  Google Scholar 

  • Weimerskirch H, Borsa P, Cruz S, de Grissac S, Gardes L, Lallemand J, Le Corre M, Prudor A (2017) Diversity of migration strategies among great frigatebirds populations. J Avian Biol 48:103–113

    Article  Google Scholar 

  • Williams TD (1995) The penguins. Oxford University Press, Oxford, p 295

    Google Scholar 

  • Williams CT, Buck CL (2010) Using fatty acids as dietary tracers in seabird trophic ecology: theory, application and limitations. J Ornithol 151:531–543

    Article  Google Scholar 

  • Wilson RP, La Cock GD, Wilson MP, Mollagee F (1985) Differential digestion of fish and squid in Jackass penguins Spheniscus demersas. Ornis Scand 16:77–79

    Article  Google Scholar 

  • Wold A, Jaeger I, Hop H, Gabrielsen GW, Falk-Petersen S (2011) Arctic seabird food chains explored by fatty acid composition and stable isotopes in Kongsfjorden, Svalbard. Polar Biol 34:1147–1155

    Article  Google Scholar 

  • Yamamoto T, Takahashi A, Yoda K, Katsumata N, Watanabe S, Sato K, Trathan PN (2008) The lunar cycle affects at-sea behaviour in a pelagic seabird, the Streaked Shearwater, Calonectris leucomelas. Anim Behav 76:1647–1652

    Article  Google Scholar 

  • Young JW, Lansdell MJ, Campbell RA, Cooper SP, Juanes F, Guest MA (2010) Feeding ecology and niche segregation in oceanic top predators off eastern Australia. Mar Biol 157:2347–2368

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GG (2009) Mixed effects models and extensions in ecology with r. Springer, New York

    Book  Google Scholar 

Download references

Acknowledgements

The authors thank O. Yamamura for information on the global distribution of myctophids, B. Nishizawa for statistical advice, Drs. Yves Cherel, David Ainley and a anonymous reviewer for valuable and helpful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yutaka Watanuki.

Ethics declarations

Conflict of interest

The authors have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors. This article is a review paper and does not contain any studies with animals performed by any of the authors.

Additional information

Responsible Editor: Y. Cherel.

Reviewed by D. G. Ainley and an undisclosed expert.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 612 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Watanuki, Y., Thiebot, JB. Factors affecting the importance of myctophids in the diet of the world’s seabirds. Mar Biol 165, 79 (2018). https://doi.org/10.1007/s00227-018-3334-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-018-3334-y

Navigation