Abstract
The life histories of cephalopods are still not well described. Stable isotopic analysis of cephalopod beaks is an effective method to study the habitat and trophic ecology of this group of organisms. As beaks grow continuously throughout squid’s life without replacement, we hypothesised that analysing different sections along the beak will provide information on the ontogenetic shifts during the individual’s lifetime. Here we used the Southern Ocean squid Kondakovia longimana as a model species to test the reliability of this method along the beaks of Antarctic species. Growing patterns show that beaks grow throughout the squid lifetime by a continuous deposition of material. This new material can influence the results of the stable isotopic analysis. δ13C and δ15N values (from − 26.3 to − 20.6‰ and from + 3.2 to + 8.2‰, respectively) from different beak regions indicated that K. longimana inhabits regions spanning a wide latitudinal range, and the trophic level at which it feeds increases throughout its lifetime. Stable isotopic analysis of different sections of the cephalopod beak is a reliable technique to study habitat and trophic ecology throughout Antarctic squid’s lifetime. Stable isotopic results showed an increase in δ15N values from the tip of the rostrum to the end of the hood and crest, in the upper beak, and to the free corner of lateral wall and wing in the lower beak. Our results also suggested that the upper beak is the best beak to study ontogenetic shifts, mainly in initial stages of the cephalopods’ life, presenting lower values of δ15N than the lower beak.
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References
Alvito PM, Rosa R, Phillips RA, Cherel Y, Ceia F, Guerreiro M, Seco J, Baeta A, Vieira RP, Xavier JC (2015) Cephalopods in the diet of nonbreeding black-browed and grey-headed albatrosses from South Georgia. Polar Biol 38:631–641. https://doi.org/10.1007/s00300-014-1626-3
Arkhipkin AI (2005) Statoliths as black boxes (life recorders) in squid. Mar Freshw Res 56:573–583. https://doi.org/10.1071/MF04158
Barquete V, Strauss V, Ryan PG (2013) Stable isotope turnover in blood and claws: a case study in captive African Penguins. J Exp Mar Biol Ecol 448:121–127. https://doi.org/10.1016/j.jembe.2013.06.021
Brault EK, Koch PL, McMahon KW, Broach KH, Rosenfield AP, Sauthoff W, Loeb VJ, Arrigo KR, Smith WO (2018) Carbon and nitrogen zooplankton isoscapes in West Antarctica reflect oceanographic transitions. Mar Ecol Prog Ser 593:29–45. https://doi.org/10.3354/meps12524
Brown CR, Klages NT (1987) Seasonal and annual variation in diets of Macaroni (Eudyptes chrysolophus chrysolophus) and Southern rockhopper (E. hrysocome chrysocome) penguins at sub-Antarctic Marion Island. J Zool 212:7–28. https://doi.org/10.1111/j.1469-7998.1987.tb05111.x
Ceia FR, Paiva VH, Fidalgo V, Morais L, Baeta A, Crisóstomo P, Mourato E, Garthe S, Marques JC, Ramos JA (2014) Annual and seasonal consistency in the feeding ecology of an opportunistic species, the yellow-legged gull Larus michahellis. Mar Ecol Prog Ser 497:273–284. https://doi.org/10.3354/meps10586
Ceia FR, Ramos JA, Phillips RA, Cherel Y, Jones DC, Vieira RP, Xavier JC (2015) Analysis of stable isotope ratios in blood of tracked wandering albatrosses fails to distinguish a δ 13C gradient within their winter foraging areas in the southwest Atlantic Ocean. Rapid Commun Mass Spectrom 29:2328–2336. https://doi.org/10.1002/rcm.7401
Cherel Y, Hobson KA (2005) Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proc R Soc Lond B Biol Sci 272:1601–1607. https://doi.org/10.1098/rspb.2005.3115
Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287. https://doi.org/10.3354/meps329281
Cherel Y, Weimerskirch H (1999) Spawning cycle of onychoteuthidae squids in the southern Indian Ocean: new information from seabird predators. Mar Ecol Prog Ser 188:93–104
Cherel Y, Fontaine C, Jackson GD, Jackson CH, Richard P (2009) Tissue, ontogenic and sex-related differences in δ 13C and δ 15N values of the oceanic squid Todarodes filippovae (Cephalopoda: Ommastrephidae). Mar Biol 156:699–708. https://doi.org/10.1007/s00227-008-1121-x
Cherel Y, Gasco N, Duhamel G (2011) Top predators and stable isotopes document the cephalopod fauna and its trophic relationships in Kerguelen waters. In: The Kerguelen Plateau: marine ecosystem and fisheries. Société Française d’Ichtyologie, Paris, pp 99–108
Clarke MR (1986) A handbook for the identification of cephalopod beaks. Clarendon Press, Oxford
Collins MA, Rodhouse PGK (2006) Southern Ocean Cephalopods. In: Southward AJ, Young CM, Fuiman LA (eds) Advances in marine biology, vol 50. Academic Press–Elsevier, England, pp 191–265. https://doi.org/10.1016/s0065-2881(05)50003-8
Croxall JP, Prince PA (1994) Dead or alive, night or day: how do albatrosses catch squid? Antarct Sci 6:155–162
Filippova JA (1972) New data on the squids (Cephalopoda: Oegopsida) from the Scotia Sea (Antarctic). Malacologia 11:391–406
Guerra A, Rodríguez-Navaroo AB, González AF, Romanek CS, Álvarez-Lloret P, Pierce GJ (2010) Life-history traits of the giant squid Architeuthis dux revealed from stable isotope signatures recorded in beaks. ICES J Mar Sci 67:1425–1431. https://doi.org/10.1093/icesjms/fsq091
Guerreiro M, Phillips RA, Cherel Y, Ceia FR, Alvito P, Rosa R, Xavier JC (2015) Habitat and trophic ecology of Southern Ocean cephalopods from stable isotope analyses. Mar Ecol Prog Ser 530:119–134. https://doi.org/10.3354/meps11266
Hobson KA, Cherel Y (2006) Isotopic reconstruction of marine food webs using cephalopod beaks: new insight from captively raised Sepia officinalis. Can J Zool 84:766–770. https://doi.org/10.1139/z06-049
Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic marine food web using δ 13C and δ 15N analysis. Mar Ecol Prog Ser 84:9–18
Jackson GD, Bustamante P, Cherel Y, Fulton EA, Grist EPM, Jackson CH, Nichols PD, Pethybridge H, Phillips K, Ward RD, Xavier JC (2007) Applying new tools to cephalopod trophic dynamics and ecology: perspectives from the Southern Ocean Cephalopod Workshop, February 2–3, 2006. Rev Fish Biol Fish 17:79–99. https://doi.org/10.1007/s11160-007-9055-9
Jaeger A, Lecomte VJ, Weimerskirch H, Richard P, Cherel Y (2010) Seabird satellite tracking validates the use of latitudinal isoscapes to depict predators’ foraging areas in the Southern Ocean. Rapid Commun Mass Spectrom 24:3456–3460. https://doi.org/10.1002/rcm.4792
Laptikhovsky V, Arkhipkin A, Bolstad KS (2009) A second species of the squid genus Kondakovia (Cephalopoda: Onychoteuthidae) from the sub-Antarctic. Polar Biol 32:21–26. https://doi.org/10.1007/s00300-008-0497-x
Laptikhovsky V, Collins MA, Arkhipkin A (2013) First case of possible iteroparity among coleoid cephalopods: the giant warty squid Kondakovia longimana. J Molluscan Stud 79:270–272. https://doi.org/10.1093/mollus/eyt014
Lipinski MR (2001) Statoliths as archives of cephalopod life cycle: a search for universal rules. Folia Malacol 9:115–123. https://doi.org/10.12657/folmal.009.014
Lowther AD, Fisk A, Kovacs KM, Lydersen C (2017) Interdecadal changes in the marine food web along the west Spitsbergen coast detected in the stable isotope composition of ringed seal (Pusa hispida) whiskers. Polar Biol 40:2027–2033. https://doi.org/10.1007/s00300-017-2122-3
Lu CC, Ickeringill R (2002) Cephalopod beak identification and biomass estimation techniques: tools for dietary studies of southern Australian finfishes. Museum Victoria Science Reports No. 6. Museum Victoria, Melbourne
Lynnes AS, Rodhouse PG (2002) A big mouthful for predators: the largest recorded specimen of Kondakovia longimana (Cephalopoda: Onychoteuthidae). Bull Mar Sci 71:1087–1090
McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102:378–390. https://doi.org/10.1034/j.1600-0706.2003.12098.x
Mendes S, Newton J, Reid RJ, Zuur AF, Pierce GJ (2007) Stable carbon and nitrogen isotope ratio profiling of sperm whale teeth reveals ontogenetic movements and trophic ecology. Oecologia 151:605–615. https://doi.org/10.1007/s00442-006-0612-z
Micheli-Campbell MA, Connell MJ, Dwyer RG, Franklin CE, Fry B, Kennard MJ, Tao J, Campbell HA (2017) Identifying critical habitat for freshwater turtles: integrating long-term monitoring tools to enhance conservation and management. Biodivers Conserv 26:1675–1688. https://doi.org/10.1007/s10531-017-1325-9
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ 15N and animal age. Geochim Cosmochim Acta 48:1135–1140. https://doi.org/10.1016/0016-7037(84)90204-7
Miserez A, Schneberk T, Sun C, Zok FW, Waite JH (2008) The transition from stiff to compliant materials in squid beaks. Science 319:1816–1819. https://doi.org/10.1126/science.1154117
Miserez A, Rubin D, Waite JH (2010) Cross-linking chemistry of squid beak. J Biol Chem 285:38115–38124. https://doi.org/10.1074/jbc.M110.161174
Nemoto T, Okiyama M, Takahashi M (1985) Aspects of the roles of squid in food chains of Marine Antarctic Ecosystems. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 415–420. https://doi.org/10.1007/978-3-642-82275-9_58
Paiva VH, Ramos JA, Nava C, Neves V, Bried J, Magalhaes M (2017) Inter-sexual habitat and isotopic niche segregation of the endangered Monteiro’s storm-petrel during breeding. Zoology 126:29–35. https://doi.org/10.1016/j.zool.2017.12.006
Perales-Raya C, Bartolomé A, García-Santamaría MT, Pascual-Alayón P, Almansa E (2010) Age estimation obtained from analysis of octopus (Octopus vulgaris Cuvier, 1797) beaks: improvements and comparisons. Fish Res 106:171–176. https://doi.org/10.1016/j.fishres.2010.05.003
Perales-Raya C, Almansa E, Bartolomé A, Felipe BC, Iglesias J, Sánchez FJ, Carrasco JF, Rodríguez C (2014) Age validation in Octopus vulgaris beaks across the full ontogenetic range: beaks as recorders of life events in octopuses. J Shellfish Res 33:481–493. https://doi.org/10.2983/035.033.0217
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320. https://doi.org/10.1146/annurev.es.18.110187.001453
Ramos R, González-Solís J (2012) Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front Ecol Environ 10:258–266. https://doi.org/10.1890/110140
Raya CP, Hernández-González CL (1998) Growth lines within the beak microstructure of the octopus Octopus vulgaris Cuvier, 1797. S Afr J Mar Sci 20:135–142. https://doi.org/10.2989/025776198784126368
Roberts J, Xavier JC, Agnew DJ (2011) The diet of toothfish species Dissostichus eleginoides and Dissostichus mawsoni with overlapping distributions. J Fish Biol 79:138–154. https://doi.org/10.1111/j.1095-8649.2011.03005.x
Rodhouse PG (1998) Physiological progenesis in cephalpod molluscs. Biol Bull 195:17–20. https://doi.org/10.2307/1542771
Rodhouse PGK (2013) Role of squid in the Southern Ocean pelagic ecosystem and the possible consequences of climate change. Deep Sea Res II Top Stud Oceanogr 95:129–138. https://doi.org/10.1016/j.dsr2.2012.07.001
Rodhouse PGK, Griffiths HJ, Xavier JC (2014) Southern Ocean Squid. In: De Broyer C et al (eds) The biogeographic atlas of the Southern Ocean. The Scientific Committee on Antarctic Research, Cambridge, pp 284–289
Rosas-Luis R, Navarro J, Martínez-Baena F, Sánchez P (2017) Differences in the trophic niche along the gladius of the squids Illex argentinus and Doryteuthis gahi based on their isotopic values. Reg Stud Mar Sci 11:17–22. https://doi.org/10.1016/j.rsma.2017.02.003
Ruiz-Cooley RI, Villa EC, Gould WR (2010) Ontogenetic variation of δ 13C and δ 15N recorded in the gladius of the jumbo squid Dosidicus gigas: geographic differences. Mar Ecol Prog Ser 399:187–198. https://doi.org/10.3354/meps08383
Seco J, Roberts J, Ceia FR, Baeta A, Ramos JA, Paiva VH, Xavier JC (2016) Distribution, habitat and trophic ecology of Antarctic squid Kondakovia longimana and Moroteuthis knipovitchi: inferences from predators and stable isotopes. Polar Biol 39:167–175. https://doi.org/10.1007/s00300-015-1675-2
Takai N, Onaka S, Ikeda Y, Yatsu A, Kidokoro H, Sakamoto W (2000) Geographical variations in carbon and nitrogen stable isotope ratios in squid. J Mar Biol Assoc UK 80:675–684. https://doi.org/10.1017/S0025315400002502
Tan Y, Hoon S, Guerette PA, Wei W, Ghadban A, Hao C, Miserez A, Waite JH (2015) Infiltration of chitin by protein coacervates defines the squid beak mechanical gradient. Nat Chem Biol 11:488–495. https://doi.org/10.1038/nchembio.1833
Trull TW, Armand L (2001) Insights into Southern Ocean carbon export from the δ 13C of particles and dissolved inorganic carbon during the SOIREE iron release experiment. Deep Sea Res II Top Stud Oceanogr 48:2655–2680. https://doi.org/10.1016/s0967-0645(01)00013-3
Xavier JC, Cherel Y (2009) Cephalopod beak guide for the Southern Ocean. British Antarctic Survey, Cambridge
Xavier JC, Peck LS (2015) Life beyond the ice. In: Liggett D, Storey B, Cook Y, Meduna V (eds) Exploring the last continent. Springer, Berlin, pp 229–252
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. https://doi.org/10.1017/S0954102099000097
Xavier JC, Wood AG, Rodhouse PG, Croxall J (2007) Interannual variations in cephalopod consumption by albatrosses at South Georgia: implications for future commercial exploitation of cephalopods. Mar Freshw Res 58:1136–1143. https://doi.org/10.1071/MF06237
Xavier JC, Allcock AL, Cherel Y, Lipinski MR, Pierce GJ, Rodhouse PGK, Rosa R, Shea EK, Strugnell JM, Vidal EAG, Villanueva R, Ziegler A (2015) Future challenges in cephalopod research. J Mar Biol Assoc UK 95:999–1015. https://doi.org/10.1017/s0025315414000782
Xavier JC, Ferreira S, Tavares S, Santos N, Mieiro CL, Trathan PN, Lourenco S, Martinho F, Steinke D, Seco J, Pereira E, Pardal M, Cherel Y (2016a) The significance of cephalopod beaks in marine ecology studies: can we use beaks for DNA analyses and mercury contamination assessment? Mar Pollut Bull 103:220–226. https://doi.org/10.1016/j.marpolbul.2015.12.016
Xavier JC, Raymond B, Jones DC, Griffiths H (2016b) Biogeography of cephalopods in the Southern Ocean using habitat suitability prediction models. Ecosystems 19:220–247. https://doi.org/10.1007/s10021-015-9926-1
Zimmer I, Piatkowski U, Brey T (2007) The trophic link between squid and the emperor penguin Aptenodytes forsteri at Pointe Géologie, Antarctica. Mar Biol 152:1187–1195. https://doi.org/10.1007/s00227-007-0766-1
Acknowledgements
This work has been supported by the British Antarctic Survey, providing laboratory space and equipment for shore-based sample processing at South Georgia. It also has the support of the Government of South Georgia and the South Sandwich Islands and the research programs CEPH, SCAR AnT-ERA, SCAR EGBAMM, PROPOLAR and ICED. JX is supported by the Investigator FCT program (IF/00616/2013) and FRC by the Foundation for Science and Technology (FCT—Portugal) and the European Social Fund (POPH, EU) through a post-doc grant (SFRH/BPD/95372/2013). We would also like to thank the reviewers of the manuscript Dr. Vecchioni and Dr. Lipínski and to the editor of the journal Dr. Dieter Piepenburg for the useful comments to improve the quality of the work. Further, we want to thank our friend Naomi Treble for the revision of the English language.
Funding
The author José C. Xavier is supported by Fundação para a Ciência e Tecnologia (PT) through the grant (IF/00616/2013). Filipe R. Ceia is supported by Fundação para a Ciência e Tecnologia (PT) and European Social Fund (POPH, EU) through the grant (SFRH/BPD/95372/2013). The scientific work was supported by British Antarctic Survey, Government of South Georgia, Government of South Sandwich Islands and by several research programs, i.e. CEPH, SCAR AnT-ERA, SCAR EGBAMM, PROPOLAR and ICED.
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This research uses beaks from squid. These beaks were obtained from the stomachs of fish captured in a Fishing Vessel for human consumption. No harm was made to any animal while performing this research.
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Queirós, J.P., Cherel, Y., Ceia, F.R. et al. Ontogenic changes in habitat and trophic ecology in the Antarctic squid Kondakovia longimana derived from isotopic analysis on beaks. Polar Biol 41, 2409–2421 (2018). https://doi.org/10.1007/s00300-018-2376-4
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DOI: https://doi.org/10.1007/s00300-018-2376-4