Skip to main content

Advertisement

Log in

New insights in Southwestern Atlantic Ocean Oegopsid squid distribution based on juvenile green turtle (Chelonia mydas) diet analysis

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

A total of 52 cephalopod beaks were found in the stomachs and intestines of 17 out of 54 green turtles, Chelonia mydas, stranded on the Uruguayan coast between 2009 and 2013 (frequency of occurrence = 31.5 %). Upper and lower beaks were assigned to at least six Oegopsid species of four different genera, Chiroteuthis, Histioteuthis, Onykia (= Moroteuthis) and Mastigoteuthis. Although the presence of cephalopods in the diet of green turtles has been reported previously, it has been quoted as a sporadic or less important diet category. Our findings suggest that this intake of cephalopods by juvenile green turtles during their oceanic stages may be more common in the Southwestern Atlantic Ocean waters than previously thought. According to our records, two of the six Oegopsid squid species found would have a more extended distribution than previously reported, ranging from circumpolar sub-Antarctic areas to the Brazil-Malvinas confluence zone. We highlight the potential of diet analysis of pelagic predators as a tool to enhance our knowledge of the diversity and distribution of poorly known cephalopod species.

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
Fig. 3

Similar content being viewed by others

References

  • Amorocho D, Reina RD (2007) Feeding ecology of the East Pacific green sea turtle Chelonia mydas agassizii at Gorgona National Park, Colombia. Endanger Species Res 3:43–51

    Article  Google Scholar 

  • Arthur KE, Balazs GH (2008) A comparison of immature green turtle (Chelonia mydas) diets among seven sites in the Main Hawaiian Islands. Pac Sci 62:205–217

    Article  Google Scholar 

  • Ayçaguer CB, Nieddu MA (2014) (In press) New records of Histioteuthis macrohista N. Voss, 1969 (Cephalopoda: Teuthida) from the South Western Atlantic. Comunicaciones de la Sociedad Malacológica del Uruguay

  • Balazs GH, Chaloupka M (2004) Spatial and temporal variability in somatic growth of green sea turtles (Chelonia mydas) resident in the Hawaiian Archipelago. Mar Biol 145:1043–1059. doi:10.1007/s00227-004-1387-6

    Article  Google Scholar 

  • Bjorndal K (1997) Foraging ecology and nutrition of the sea turtles. In: Lutz P, Music J (eds) The biology of sea turtles. CRC Press, New York, pp 199–231

    Google Scholar 

  • Bjorndal KA, Bolten AB, Moore JE (1990) Digestive fermentation in herbivores: effect of food particle size. Physiol Zool 63:710–721

    Google Scholar 

  • Blumenthal JM, Austin TJ, Bothwell JB, Broderick AC et al (2010) Life in (and out of) the lagoon: fine-scale movements of green turtles tracked using time-depth recorders. Aquat Biol 9:113–121

    Article  Google Scholar 

  • Bolstad KSR (2010) Systematics of the Onychoteuthidae Gray, 1847 (Cephalopoda: Oegopsida). Zootaxa 2696:1–186

    Google Scholar 

  • Boyle MC, Limpus CJ (2008) The stomach contents of post-hatchling green and loggerhead sea turtles in the South-west Pacific: an insight into habitat association. Mar Biol 155:233–241

    Article  Google Scholar 

  • Brand SJ, Lanyon JM, Limpus CJ (1999a) Diet selection by immature green turtles, Chelonia mydas, in subtropical Moreton Bay, south-east Queensland. Aust J Zool 47:181–191

    Article  Google Scholar 

  • Brand SJ, Lanyon JM, Limpus CJ (1999b) Digesta composition and retention times in wild immature green turtles, Chelonia mydas: a preliminary investigation. Mar Freshwat Res 50:145–147

    Article  Google Scholar 

  • Campos EJD, Piola AR, Matano RP, Miller JL (2008) PLATA: a synoptic characterization of the southwest Atlantic shelf under influence of the Plata River and Patos Lagoon outflows. Cont Shelf Res 28:1551–1555

    Article  Google Scholar 

  • Caraccio MN (2008) Análisis de la composición genética de Chelonia mydas (tortuga verde) en el área de alimentación y desarrollo de Uruguay. Tesis de Maestría del Programa de Desarrollo de las Ciencias Básicas (PEDECIBA), Área Biología-Subárea Genética, Facultad de Ciencias, Universidad de la República, Montevideo

  • Cardona L, Pazos L, Aguilar L (2009) Delayed ontogenic dietary shift and high levels of omnivory in green turtles (Chelonia mydas) from the NW coast of Africa. Mar Biol 156:1487–1495

    Article  CAS  Google Scholar 

  • Carrión-Cortez JA, Zárate P, Sminoff JA (2010) Feeding ecology of the green sea turtle (Chelonia mydas) in the Galapagos Islands. J Mar Biol Assoc UK 90:1005–1013. doi:10.1017/S0025315410000226

    Article  Google Scholar 

  • Chaloupka M, Limpus CJ (2001) Trends in the abundance of sea turtles resident in southern Great Barrier Reef waters. Biol Conserv 102:235–249

    Article  Google Scholar 

  • Chaloupka M, Limpus C, Miller J (2004) Green turtle somatic growth dynamics in a spatially disjunct Great Barrier reef metapopulation. Coral Reefs 23:325–335. doi:10.1007/s00338-004-0387-9

    Article  Google Scholar 

  • Cherel Y, Klages N (1998) A review of the food of albatrosses. In: Robertson G, Gales R (eds) Albatross biology and conservation. Surrey Beatty & Sons, Chipping Norton, pp 113–136

    Google Scholar 

  • Cherel Y, Weimerskirch H (1995) Seabirds as indicators of marine resources: black-browed albatrosses feeding on ommastrephid squids in Kerguelen waters. Mar Ecol Prog Ser 129:295–300

    Article  Google Scholar 

  • Cherel Y, Weimerskirch H (1999) Spawning cycle of onychoteuthid squids in the southern Indian Ocean: new information from seabird predators. Mar Ecol Prog Ser 188:93–104. doi:10.3354/meps188093

    Article  Google Scholar 

  • Cherel Y, Duhamel G, Gasco N (2004) Cephalopod fauna of subantarctic islands: new information from predators. Mar Ecol Prog Ser 266:143–156

    Article  Google Scholar 

  • Clarke MR (1986) A handbook for the identification of cephalopod beaks. Claredon Press, Oxford, 273 pp

    Google Scholar 

  • Collins MA, Rodhouse PGK (2006) Southern ocean cephalopods. Adv Mar Biol 50:191–265

    Article  PubMed  Google Scholar 

  • Croxall JP, Prince PA (1994) Dead or alive, night or day: how do albatrosses catch squid? Antarct Sci 6:155–162

    Article  Google Scholar 

  • Croxall JP, Prince PA (1996) Cephalopods as prey: seabirds. Philos Trans R Soc B 351:1023–1043

    Article  Google Scholar 

  • Csirke J (1987) The Patagonian fishery resources and the offshore fisheries in the Southwest Atlantic. Fish Tech Pap 286. FAO, Rome, p 75

    Google Scholar 

  • Domingo A, Bugoni L, Prosdocimi L, et al (2006) The impact generated by fisheries on Sea Turtles in the Southwestern Atlantic. Tech. Rep. WWF Programa Marino para Latinoamérica y el Caribe, San José, Costa Rica: 71 pp

  • Ferreira B, Garcia M, Jupp BP, Al-Kryumi A (2006) Diet of the green turtle (Chelonia mydas) at Ra’s Hadd, Sultanate of Oman. Chelon Conserv Biol:141–145

  • Field I, Bradshaw C, Van Den Hoff J, Burton H, Hindell M (2007) Age-related shifts in the diet composition of southern elephant seals expand overall foraging niche. Mar Biol 150:1441–1452

    Article  CAS  Google Scholar 

  • Godley BJ, Thompson DR, Waldron S, Furness RW (1998) The trophic status of marine turtles as determined by stable isotope analysis. Mar Ecol Prog Ser 166:277–284

    Article  Google Scholar 

  • González Carman V, Falabella V, Maxwell S, Albareda D, Campagna C, Mianzan H (2012) Revisiting the ontogenetic shift paradigm: the case of juvenile green turtles in the SW Atlantic. J Exp Mar Biol Ecol 429:64–72. doi:10.1016/j.jembe.2012.06.007

    Article  Google Scholar 

  • González Carman V, Botto F, Gaitán E, Albareda D, Campagna C, Mianzan H (2013) A jellyfish diet for the herbivorous green turtle Chelonia mydas in the temperate SW Atlantic. Mar Biol. doi:10.1007/s00227-013-2339-9

    Google Scholar 

  • Guebert-Bartholo FM, Barletta M, Costa MF, Monteiro-Filho ELA (2011) Using gut contents to assess foraging patterns of juvenile green turtles Chelonia mydas in the Paranaguá Estuary, Brazil. Endanger Species Res 13:131–143

    Article  Google Scholar 

  • Hatase H, Sato K, Yamaguchi M, Takahashi K, Tsukamoto K (2006) Individual variation in feeding habitat use by adult female green sea turtles (Chelonia mydas): are they obligately neritic herbivores? Oecologia 149:52–64

    Article  PubMed  Google Scholar 

  • Hatfield EMC, Rodhouse PG (1991) Biology and fishery of the Patagonian squid Loligo gahi (d’Orbigny, 1835): a review of current knowledge. J Ceph Biol 2:41–79

    Google Scholar 

  • Hernández-García V (1995) The diet of the swordfish Xiphias gladius Linnaeus, 1758, in the central east Atlantic, with emphasis on the role of cepahlopods. Fish Bull 93:403–411

    Google Scholar 

  • Hirth HF (1997) Synopsis of the biological data on the green turtle, Chelonia mydas (Linnaeus 1758). United States Fish and Wildlife Service Biological Report 97–1:120 pp

  • Horta S, Defeo O (2012) The spatial dynamics of the white mouth croaker artisanal fishery in Uruguay and interdependencies with the industrial fleet. Fish Res 125–126(1):21–128. doi:10.1016/ j.fishres.2012.02.007

    Google Scholar 

  • Hoving HJT, Perez JAA, Bolstad K, Braid H, Evans AB, Fuchs D, Judkins H, Kelly JT, Marian JEAR, Nakajima R, Piatkowski U, Reid A, Vecchione M, Xavier JC (2014) The study of deep-sea cephalopods. Adv Mar Biol (in press)

  • Imber MJ (1992) Cephalopods eaten by wandering albatrosses (Diomedea exulans L.) breeding at six circumpolar localities. J R Soc N Z 22:243–263

    Article  Google Scholar 

  • International Union for Conservation of Nature and Natural Resources (2013) Red list of threatened species, version 2013.2. www.iucnredlist.org

  • Limpus CJ, Couper PJ, Read MA (1994) The green turtle, Chelonia mydas, in Queensland: Population structure in a warm temperate feeding area. Mem Queensland Mus 35:139

    Google Scholar 

  • López-Mendilaharsu M, Estrades A, Caraccio M et al (2006) Biología y ecología de las tortugas marinas en la zona costera uruguaya. In: Menafra R, Rodríguez-Gallego L, Scarabino F, Conde D (eds) Bases para la Conservación y el Manejo de la Costa Uruguaya. VIDA SILVESTRE, Montevideo, pp 247–258

  • López-Mendilaharsu M, Gardner S, Riosmena-Rodríguez R, Seminoff JA (2008) Diet selection by immature green turtles (Chelonia mydas) at Bahía Magdalena foraging ground in the Pacific Coast of the Baja California Peninsula, México. J Mar Biol Assoc UK 88:1–7

    Article  Google Scholar 

  • Lu CC, Williams R (1994) Contribution to the biology of squid in the Prydz Bay region, Antarctica. Antarct Sci 6:223–229

    Google Scholar 

  • Marcovaldi M, Marcovaldi G (1999) Marine turtles of Brazil: the history and structure of Projeto TAMAR-IBAMA. Biol Conserv 91:35–41

    Article  Google Scholar 

  • Martinez-Souza G, Vélez-Rubio GM, Techera B, Russomagno M, Berrondo L, Kinas P (2012) Cerro Verde, Uruguay: a year-round feeding area for juveniles green turtles? In: Jones TT, Wallace BP (eds) Proceedings of the 31st symposium on sea turtle biology and conservation. International Sea Turtle Society, NOAA Techincal Memorandum NOAA NMFS-SEFSC, pp 148–149

  • Morais RA, Longo GO, Yoshida ETE, Stahelin GD, Horta PA (2012) Cephalopod ingestion by juvenile green sea turtles (Chelonia mydas): Predatory or scavenging behavior? Herpetol Rev 43:47–50

    Google Scholar 

  • Nagoaka S, Martins A, Santos R et al (2012) Diet of juvenile green turtles (Chelonia mydas) associating with artisanal fishing traps in a subtropical estuary in Brazil. Mar Biol 159:573–589

    Article  Google Scholar 

  • Nesis KN (1987) Cephalopods of the world. T.F.H. Publications, Neptune City

    Google Scholar 

  • Ohizumi H, Kuramochi T, Kubodera T, Yoshioka M, Miyazaki N (2003) Feeding habits of Dall’s porpoises (Phocoenoides dalli) in the subarctic North Pacific and the Bering Sea basin and the impact of predation on mesopelagic micronekton. Deep Sea Res (I Oceanogr Res Pap) 50:593–610

    Article  Google Scholar 

  • Okutani T (1994) The importance of the Southern Ocean cephalopod fauna. Antarct Sci 6:2

    Article  Google Scholar 

  • Ortega L, Martínez A (2007) Multi annual and seasonal variability of water masses and fronts over the Uruguayan shelf. J Coast Res 23:618–629. doi:10.2112/04-0221.1

    Article  Google Scholar 

  • Parker DM, Dutton PH, Balazs GH (2011) Oceanic diet and distribution of haplotypes for the green turtle, Chelonia mydas, in the central North Pacific. Pac Sci 65(4):419–431. doi:10.2984/65.4.419

    Article  Google Scholar 

  • Perez JAA, Martins RS, Santos RA (2004) Cefalópodes capturados pela pesca commercial de talude no sudeste e sul do Brasil. Not Téc FACIMAR 8:65–74

    Google Scholar 

  • R Development Team (2008) R statistcs. Available at: http://www.r-project.org/

  • Read MA, Limpus CJ (2002) The green turtle, Chelonia mydas, in Queensland: feeding ecology of immature turtles in Moreton Bay, southeastern Queensland. Mem Queensland Mus 48:207–214

    Google Scholar 

  • Reich KJ, Bjorndal KA, Bolten AB (2007) The ‘lost years’ of green turtles: using stable isotopes to study cryptic life-stages. Biol Lett 3:712–714

    Article  PubMed Central  PubMed  Google Scholar 

  • Reisser J, Proietti M, Sazima I, Kinas P, Horta P, Secchi E (2013) Feeding ecology of the green turtle (Chelonia mydas) at rocky reefs in western South Atlantic. Mar Biol 160:3169–3179

    Article  Google Scholar 

  • Rodhouse PG, Lu CC (1998) Chiroteuthis veranyi from the Atlantic sector of the Southern Ocean (Cephalopoda: Chiroteuthidae). S Afr J Mar Sci 20:311–322. doi:10.2989/025776198784126593

    Article  Google Scholar 

  • Rodhouse PG, Nigmatullin ChM (1996) Role as consumers. Phil Trans R Soc Lond B 351. doi: 10.1098/rstb.1996.0090

  • Rodhouse PG, White MG (1995) Cephalopods occupy the ecological niche of epipelagic fish in the Antarctic Polar frontal zone. Biol Bull 189:77–80

    Article  Google Scholar 

  • Rodhouse PG, Arnbom T, Fedak MA, Yeatman J, Murray AWA (1992) Cephalopod prey of the southern elephant seal, Mirounga leonina L. Can J Zool 70:1007–1015

    Article  Google Scholar 

  • Rodhouse PG, Robinson K, Gajdatsy SB, Daly HL, Ashmore MJS (1994) Growth, age structure and environmental history in the cephalopod Martialia hyadesi (Teuthoidea: Ommastrephidae) at the Antarctic Polar Frontal Zone and on the Patagonian Shelf Edge. Antarct Sci 6(2):259–267

    Google Scholar 

  • Rodhouse PG, Xavier JC, Griffiths H (2014) Southern Ocean squid. In: De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz C d’, Van de Putte AP, Danis B, David B, Grant S, Gutt J, Held C, Hosie G, Huettmann F, Post A, Ropert-Coudert Y (eds) Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, 400 pp

  • Roper CFE, Young RE (1974) Vertical distribution of pelagic cephalopods. Smithson Contrib Zool 209:1–59

    Google Scholar 

  • Russell DJ, Hargrove S, Balazs G (2011) Marine sponges, other animal food, and nonfood items found in digestive tracts of the herbivorous marine turtle Chelonia mydas in Hawai’i. Pac Sci 65(3):375–381

    Article  Google Scholar 

  • Salman A, Karakulak FS (2009) Cephalopods in the diet of albacore, Thunnus alalunga, from the eastern Mediterranean. J Mar Biol Assoc UK 89:635–640

    Article  Google Scholar 

  • Scarabino F (2003) Lista sistemática de los Cephalopoda vivientes de Uruguay. Comunicaciones de la Sociedad Malacológica del Uruguay 8(78–79):197–202

    Google Scholar 

  • Seminoff JA, Resendiz A, Nichols WJ (2002) Diet of East Pacific green turtles (Chelonia mydas) in the central Gulf of California, Mexico. J Herpetol 36:447–453

    Article  Google Scholar 

  • Tsuchiya K, Okutani T (1991) Growth stages of Moroteuthis robusta (Verrill, 1881) with the re-evaluation of the genus. Bull Mar Sci 49:137–147

    Google Scholar 

  • Vaske-junior T, Rincon-Filho G (1998) Conteúdo estomacal dos tubarões azul (Prinace glauca) e anequim (Isurus oxyrinchus) em águas oceânicas no sul do Brasil. Rev Bras Biol 58(3):445–452

    Article  Google Scholar 

  • Vélez-Rubio GM, Estrades A, Fallabrino A, Tomás J (2013) Marine turtle threats in Uruguayan waters: insights from 12 years of stranding data. Mar Biol 160:2797–2811

    Article  Google Scholar 

  • Voight JR, Portner HO, O’Dor RK (1994) A review of ammonia-mediated bouyancy in squids (Cephalopoda: Teuthoidea). Mar Freshw Behav Physiol 25:193–203

    Article  Google Scholar 

  • Voss NA, Nesis KN, Rodhouse PG (1998) The Cephalopod family Histioteuthidae (Oegopsida): systematics, biology, and biogeography. In: Voss NA, Vecchione M, Toll RB, Sweeney MJ (eds) Systematics and Biogeography of Cephalopods. Smithsonian Contributions to Zoology, Washington, pp 293–372

    Google Scholar 

  • Wainer I, Venegas SA (2002) South Atlantic multidecadal variability in the climate system model. J Clim 15:1408–1420

    Article  Google Scholar 

  • Wakabayashi T, Kubodera T, Sakai M, Ichii T, Chow S (2007) Molecular evidence for synonymy of the genera Moroteuthis and Onykia and identification of their paralarvae from northern Hawaiian waters. J Mar Biol Assoc UK 87:959–965

    Article  CAS  Google Scholar 

  • Xavier JC, Cherel Y (2009) Cephalopod Beak Guide for the Southern Ocean. British Antarctic Survey, Cambridge, 129 pp

    Google Scholar 

  • Xavier JC, Rodhouse PG, Trathan PN, Wood AG (1999) A Geographical Information System (GIS) atlas of cephalopod distribution in the Southern Ocean. Antarct Sci 11:61–62

    Article  Google Scholar 

  • Xavier JC, Rodhouse PG, Purves MG, Daw TM, Arata J, Pilling GM (2002) Distribution of cephalopods recorded in the diet of Patagonian toothfish (Dissostichus eleginoides) around South Georgia. Polar Biol 25:323–330

    Google Scholar 

  • Xavier JC, Croxall JP, Cresswell KA (2005) Boluses: a simple, cost-effective diet method to assess the cephalopod prey of albatrosses? Auk 122:1182–1190

    Article  Google Scholar 

  • Xavier JC, Geraint GA, Croxall JP (2006) Determining large scale distribution of pelagic cephalopods, fish and crustaceans in the South Atlantic from wandering albatross (Diomedea exulans) foraging data. Ecography 29:260–272

    Article  Google Scholar 

  • Xavier JC, Phillips RA, Cherel Y (2011) Cephalopods in marine predator diet assessments: why identifying upper and lower beaks is important. ICES J Mar Sci 68(9):1857–1864. doi:10.1093/icesjms/fsr103

    Article  Google Scholar 

  • Xavier JC, Cherel Y, Roberts J, Piatkowski U (2013) How do cephalopods become available to seabirds: can fish gut contents from tuna fishing vessels be a major food source of deep-dwelling cephalopods? ICES J Mar Sci 70:46–49

    Article  Google Scholar 

  • Young RE, Vecchione M (2007) Cephalopoda Cuvier 1797. Octopods, squids, nautiluses, etc. The Tree of Life Web Project, version 10. http://tolweb.org/Cephalopoda/19386/2012.11.10

  • Zug GR, Glor RF (1999) Estimates of age and growth in a population of green seaturtles Chelonia mydas from the Indian River lagoon system, Florida: a skeletochronological analysis. Can J Zool 76:1497–1506. doi:10.1139/cjz-76-8-1497

    Article  Google Scholar 

  • Zug GR, Balazs GH, Wetherall JA, Parker DM, Murakawa SKK (2001) Age and growth of Hawaiian green seaturtles (Chelonia mydas): an analysis based on skeletochronology. Fish Bull 100:117–127

    Google Scholar 

Download references

Acknowledgments

We would like to thank the volunteers and Karumbe members, specially Andrés Estrades, Alejandro Fallabrino, Virginia Ferrando, Daniel González, Luciana Alonso, Virginia Borrat, and Natalia Teryda, for their collaboration in the study and green turtle diet analyses. We also thank the support of the Marine Zoology Unit of the Cavanilles Institute of Biodiversity and Evolutionary Biology (University of Valencia, Spain), specially Ohiana Revuelta, Natalia Fraija and Ana Born. The authors are really grateful to all the persons and institutions that collaborated in the Uruguay marine turtle stranding network: local fishermen, government institutions (DINARA and DINAMA), naval prefectures, lifeguard service, rangers, civil organizations (particularly SOCOBIOMA), citizens and tourist. We also acknowledge the financial support from IFAW and Rufford Small Grants to GVR and Agencia Nacional de Investigación e Innovación (ANII) to A.C. J.T. is supported by projects CGL2011-30413 of the Spanish Ministry of Economy and Competitiveness and Prometeo (UV-CI-12-151) of the Generalitat Valenciana. This research was conducted under license (No. 200/04, 073/08 and 323/11) from the Fauna Department-Ministry of Cattle, Agriculture and Fishing of Uruguay.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to G. M. Vélez-Rubio.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vélez-Rubio, G.M., Tomás, J., Míguez-Lozano, R. et al. New insights in Southwestern Atlantic Ocean Oegopsid squid distribution based on juvenile green turtle (Chelonia mydas) diet analysis. Mar Biodiv 45, 701–709 (2015). https://doi.org/10.1007/s12526-014-0272-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12526-014-0272-x

Keywords

Navigation