Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Inter- and intra-regional patterns of stable isotopes in Dosidicus gigas beak: biological, geographical and environmental effects

Bi Lin Liu A B C , Jing Yuan Lin A , Xin Jun Chen A B C D , Yue Jin A and Jin Tao Wang A
+ Author Affiliations
- Author Affiliations

A College of Marine Sciences, Shanghai Ocean University, 999 Hucheng Ring Road, Lingang New City, Shanghai, 201306, P.R. China.

B The Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, 999 Hucheng Ring Road, Lingang New City, Shanghai, 201306, P.R. China.

C National Engineering Research Center for Oceanic Fisheries, 999 Hucheng Ring Road, Lingang New City, Shanghai, 201306, P.R. China.

D Corresponding author. Email: xjchen@shou.edu.cn

Marine and Freshwater Research 69(3) 464-472 https://doi.org/10.1071/MF17144
Submitted: 22 May 2017  Accepted: 9 October 2017   Published: 12 January 2018

Abstract

We analysed stable carbon (δ13C) and nitrogen (δ15N) isotopes of 478 Dosidicus gigas specimens collected outside the Ecuadorian, Peruvian and Chilean exclusive economic zones in the south-eastern Pacific Ocean during 2009 to 2013. There were significant spatial differences both in δ13C and δ15N values across regions, with the lowest values off Ecuador and the highest values off Chile. A small intra-regional range of isotope values indicates that squid off Ecuador feed at the same trophic level with similar primary production. In contrast, a large intra-regional range of isotope values suggests that squid off Chile, especially Peru, migrate over a large geographic range and occupy a wide range of trophic levels. A generalised additive model was used to estimate the biological (mantle length and age), geographical (latitude, and distance to the shelf break) and environmental (sea-surface temperature and chlorophyll-a) effects on isotope values. Best fitted generalised additive models explained 54.0% of the variability in δ13C and 93.1% of the variability in δ15N. The yield relationships between isotopes and explanatory variables increase our understanding of D. gigas habitats, movement and feeding ecology in the south-eastern Pacific Ocean.

Additional keywords: baseline, δ13C, δ15N, feeding, movement, south-eastern Pacific Ocean.


References

Argüelles, J., Lorrain, A., Cherel, Y., Graco, M., Tafur, R., Alegre, A., Espinoza, P., Taipe, A., Ayón, P., and Bertrand, A. (2012). Tracking habitat and resource use for the jumbo squid Dosidicus gigas: a stable isotope analysis in the Northern Humboldt Current System. Marine Biology 159, 2105–2116.
Tracking habitat and resource use for the jumbo squid Dosidicus gigas: a stable isotope analysis in the Northern Humboldt Current System.Crossref | GoogleScholarGoogle Scholar |

Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: a Practical Information–Theoretic Approach’, 2nd edn. (Springer-Verlag: New York, NY, USA.)

Carscallen, W. M. A., Vandenberg, K., Lawson, J. M., Martinez, N. D., and Romanuk, T. N. (2012). Estimating trophic position in marine and estuarine food webs. Ecosphere 3, art25.
Estimating trophic position in marine and estuarine food webs.Crossref | GoogleScholarGoogle Scholar |

Chen, X. J., Liu, B. L., Qian, W. G., Tian, S. Q., and Zhao, X. H. (2007). Fishery biology of purpleback squid, Sthenoteuthis oualaniensis, in the northwest Indian Ocean. Fisheries Research 83, 98–104.
Fishery biology of purpleback squid, Sthenoteuthis oualaniensis, in the northwest Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Cherel, Y., and Hobson, K. A. (2005). Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids. Proceedings of the Royal Society of London – B. Biological Sciences 272, 1601–1607.
Stable isotopes, beaks and predators: a new tool to study the trophic ecology of cephalopods, including giant and colossal squids.Crossref | GoogleScholarGoogle Scholar |

Cherel, Y., and Hobson, K. A. (2007). Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Marine Ecology Progress Series 329, 281–287.
Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXislChtLc%3D&md5=b39bdb5e83bcabc19ca41a8ef05845f2CAS |

Cherel, Y., Fontaine, C., Jackson, G. D., Jackson, C. H., and Richard, P. (2009). Tissue, ontogenic and sex-related differences in δ13C and δ15N values of the oceanic squid Todarodes filippovae (Cephalopoda: Ommastrephidae). Marine Biology 156, 699–708.
Tissue, ontogenic and sex-related differences in δ13C and δ15N values of the oceanic squid Todarodes filippovae (Cephalopoda: Ommastrephidae).Crossref | GoogleScholarGoogle Scholar |

Chong, J., Oyarzun, C., Galleguillos, R., Tarifeño, E., Sepúlveda, R., and Ibáñez, C. (2005). Fishery biology parameters of jumbo squid, Dosidicus gigas (d’Orbigny, 1835) (Cephalopoda: Ommastrephidae), in central Chile coast (29°S–40°S) during 1993–1994. Gayana 69, 319–328.

Cosgrove, J. A. (2005). The first specimens of Humboldt squid in British Columbia. PICES Press 13, 30–31.

Dilly, P. N., and Nixon, M. (1976). The cells that secrete the beaks in octopods and squids (Mollusca, Cephalopoda). Cell and Tissue Research 167, 229–241.
The cells that secrete the beaks in octopods and squids (Mollusca, Cephalopoda).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE287mtlaqsg%3D%3D&md5=e313d2600eef3b0b9d03216a00b16d3dCAS |

Fang, Z., Thompson, K., Jin, Y., Chen, X. J., and Chen, Y. (2016). Preliminary analysis of beak stable isotopes (δ13C andδ15N) stock variation of neon flying squid, Ommastrephes bartramii, in the North Pacific Ocean. Fisheries Research 177, 153–163.
Preliminary analysis of beak stable isotopes (δ13C andδ15N) stock variation of neon flying squid, Ommastrephes bartramii, in the North Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Field, J. C., Baltz, K., Phillips, A. J., and Walker, W. A. (2007). Range expansion and trophic interactions of the jumbo squid, Dosidicus gigas, in the California Current. California Cooperative Oceanic Fisheries Report 48, 131–146.

Field, J. C., Elliger, C., Baltz, K., Gillespie, G., Gilly, W. F., Ruiz-Cooley, I., Pearse, D., Stewart, J. S., Matsubu, W., and Walker, W. (2013). Foraging ecology and movement patterns of the Humboldt squid in the California Current. Deep Sea Research – II. Topical Studies in Oceanography 95, 37–51.
Foraging ecology and movement patterns of the Humboldt squid in the California Current.Crossref | GoogleScholarGoogle Scholar |

Fry, B. (2007). ‘Stable Isotope Ecology.’ (Springer: New York, NY, USA.)

Gilly, W. F., and Markaida, U. (2007). Perspectiveson Dosidicus gigas in a changing world. In ‘The Role of Squid in Open Ocean Ecosystems. Report of a GLOBEC-CLIOTOP/PFRP Workshop’, 16–17 November 2006, Honolulu, HI, USA. (Eds R. J. Olson and J. W. Young.) pp. 81–90. (GLOBEC International Project Office, Plymouth Marine Laboratory: Plymouth UK.)

Guerra, Á., Rodríguez-Navarro, A. B., González, Á. F., Romanek, C. S., Álvarez-Lloret, P., and Pierce, G. J. (2010). Life-history traits of the giant squid Architeuthis dux revealed from stable isotope signatures recorded in beaks. ICES Journal of Marine Science 67, 1425–1431.

Hunsicker, M. E., Essington, T. E., Aydin, K. Y., and Ishida, B. (2010). Predatory role of the commander squid Berryteuthis magister in the eastern Bering Sea: insights from stable isotopes and food habits. Marine Ecology Progress Series 415, 91–108.
Predatory role of the commander squid Berryteuthis magister in the eastern Bering Sea: insights from stable isotopes and food habits.Crossref | GoogleScholarGoogle Scholar |

Hunt, S., and Nixon, M. (1981). A comparative study of protein composition in the chitin–protein complexes of the beak, pen, sucker disc, radula and oesophageal cuticle of cephalopods. Comparative Biochemistry and Physiology 68B, 535–546.
| 1:CAS:528:DyaL3MXktl2gtLw%3D&md5=9a2e11854b272dac9c1953f3b6c3e2beCAS |

Jackson, A. L., Inger, R., Parnell, A. C., and Bearhop, S. (2011). Comparing isotopic niche widths among and within communities: SIBER: stable isotope Bayesian ellipses in R. Journal of Animal Ecology 80, 595–602.
Comparing isotopic niche widths among and within communities: SIBER: stable isotope Bayesian ellipses in R.Crossref | GoogleScholarGoogle Scholar |

Jaquet, N., Gendron, D., and Coakes, A. (2003). Sperm whales in the Gulf of California: Residency, movements, behavior, and the possible influence of variation in food supply. Marine Mammal Science 19, 545–562.
Sperm whales in the Gulf of California: Residency, movements, behavior, and the possible influence of variation in food supply.Crossref | GoogleScholarGoogle Scholar |

Kurle, C. M., and Worthy, G. A. J. (2002). Stable nitrogen and carbon isotope ratios in multiple tissues of the northern fur seal Callorhinus ursinus: implications for dietary and migratory reconstructions. Marine Ecology Progress Series 236, 289–300.
Stable nitrogen and carbon isotope ratios in multiple tissues of the northern fur seal Callorhinus ursinus: implications for dietary and migratory reconstructions.Crossref | GoogleScholarGoogle Scholar |

Kurle, C. M., Sinclair, E. H., Edwards, A. E., and Gudmundson, C. J. (2011). Temporal and spatial variation in the δ15N and δ13C values of fish and squid from Alaskan waters. Marine Biology 158, 2389–2404.
Temporal and spatial variation in the δ15N and δ13C values of fish and squid from Alaskan waters.Crossref | GoogleScholarGoogle Scholar |

Layman, C. A., Arrington, D. A., Montaña, C. G., and Post, D. M. (2007). Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88, 42–48.
Can stable isotope ratios provide for community-wide measures of trophic structure?Crossref | GoogleScholarGoogle Scholar |

Layman, C. A., Araujo, M. S., Boucek, R., Hammerschlag-peyer, C. M., Harrison, E., Jud, Z. R., Matich, P., Rosenblatt, A. E., Vaudo, J. J., Yeager, L. A., Post, D. M., and Bearhop, S. (2012). Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biological Reviews of the Cambridge Philosophical Society 87, 545–562.
Applying stable isotopes to examine food-web structure: an overview of analytical tools.Crossref | GoogleScholarGoogle Scholar |

Liu, B. L., Chen, X. J., and Yi, Q. (2013). A comparison of fishery biology of the jumbo flying squid, Dosidicus gigas, outside EEZ waters in the eastern Pacific Ocean. Chinese Journal of Oceanology and Limnology 31, 523–533.
A comparison of fishery biology of the jumbo flying squid, Dosidicus gigas, outside EEZ waters in the eastern Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Liu, B. L., Chen, X. J., Chen, Y., and Hu, G. Y. (2015). Determination of squid age using upper beak rostrum sections: technique improvement and comparison with statolith. Marine Biology 162, 1685–1693.
Determination of squid age using upper beak rostrum sections: technique improvement and comparison with statolith.Crossref | GoogleScholarGoogle Scholar |

Liu, B. L., Cao, J., Truesdell, S. B., Chen, Y., Chen, Y. J., and Tian, S. Q. (2016). Reconstructing cephalopod migration with statolith elemental signatures a case study using Dosidicus gigas. Fisheries Science 82, 425–433.
Reconstructing cephalopod migration with statolith elemental signatures a case study using Dosidicus gigas.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XkvFGksrw%3D&md5=8a359f15357cf8f28a9ab9063770d7cfCAS |

Lorrain, A., Argüelles, J., Alegre, A., Bertrand, A., Munaron, J. M., Richard, P., and Cherel, Y. (2011). Sequential isotopic signature along gladius highlights contrasted individual foraging strategies of jumbo squid (Dosidicus gigas). PLoS One 6, e22194.
Sequential isotopic signature along gladius highlights contrasted individual foraging strategies of jumbo squid (Dosidicus gigas).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVSlt77L&md5=40243f1cd9a73fabc8ad71f6a3bc67d9CAS |

Lorrain, A., Graham, B. S., Popp, B. N., Allain, V., Olson, R. J., Hunt, B. P., Allain, V., Olson, R. J., Hunt, B. P. V., Potier, M., Fry, B., Galván-Magaña, F., Menkes, C. E. R., Kaehler, S., and Ménard, F. (2015). Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans. Deep-sea Research – II. Topical Studies in Oceanography 113, 188–198.
Nitrogen isotopic baselines and implications for estimating foraging habitat and trophic position of yellowfin tuna in the Indian and Pacific Oceans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlt1Slt70%3D&md5=aab3b8273cba6da8cbdf5d1060950316CAS |

Markaida, U. (2006). Food and feeding of jumbo squid Dosidicus gigas in the Gulf of California and adjacent waters after the 1997–98 El Niño event. Fisheries Research 79, 16–27.
Food and feeding of jumbo squid Dosidicus gigas in the Gulf of California and adjacent waters after the 1997–98 El Niño event.Crossref | GoogleScholarGoogle Scholar |

Markaida, U., and Hochberg, F. G. (2005). Cephalopods in the diet of swordfish (Xiphias gladius) caught off the west coast Baja California, Mexico. Pacific Science 59, 25–41.
Cephalopods in the diet of swordfish (Xiphias gladius) caught off the west coast Baja California, Mexico.Crossref | GoogleScholarGoogle Scholar |

Markaida, U., and Sosa-Nishizaki, O. (2003). Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. Journal of the Marine Biological Association of the United Kingdom 83, 507–522.
Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico.Crossref | GoogleScholarGoogle Scholar |

Ménard, F., Lorrain, A., Potier, M., and Marsac, F. (2007). Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Marine Biology 153, 141–152.
Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean.Crossref | GoogleScholarGoogle Scholar |

Miserez, A., Li, Y., Waite, J. H., and Zok, F. (2007). Jumbo squid beaks: inspiration for design of robust organic composites. Acta Biomaterialia 3, 139–149.
Jumbo squid beaks: inspiration for design of robust organic composites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVektLvM&md5=98d480282ec4cc76e02c073e222b5e95CAS |

Navarro, J., Coll, M., Somes, C. J., and Olson, R. J. (2013). Trophic niche of squids: insights from isotopic data in marine systems worldwide. Deep-sea Research – II. Topical Studies in Oceanography 95, 93–102.
Trophic niche of squids: insights from isotopic data in marine systems worldwide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXisVOrtbg%3D&md5=3720932c17c8b92d2cf8ef3dbf74f93eCAS |

Nevárez-Martínez, M., Hernández-Herrera, A., Morales-Bojorquez, E., Balmori-Ramírez, A., Cisneros-Mata, M., and Morales-Azpeitia, R. (2000). Biomass and distribution of the jumbo squid (Dosidicus gigas; d’Orbigny, 1835) in the Gulf of California, Mexico. Fisheries Research 49, 129–140.
Biomass and distribution of the jumbo squid (Dosidicus gigas; d’Orbigny, 1835) in the Gulf of California, Mexico.Crossref | GoogleScholarGoogle Scholar |

Newsome, S., Clementz, M., and Koch, P. (2010). Using stable isotope biogeochemistry to study marine mammal ecology. Marine Mammal Science 26, 509–572.
| 1:CAS:528:DC%2BC3cXhtVaksrzJ&md5=6a83411bac3667749bc79ccb01bc967aCAS |

Nigmatullin, Ch. M., Nesis, K. N., and Arkhipkin, A. I. (2001). A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae). Fisheries Research 54, 9–19.
A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae).Crossref | GoogleScholarGoogle Scholar |

Ohkouchi, N., Tsuda, R., Chikaraishi, Y., and Tanabe, K. (2013). A preliminary estimate of the trophic position of the deep-water ram’s horn squid Spirula spirula based on the nitrogen isotopic composition of amino acids. Marine Biology 160, 773–779.
A preliminary estimate of the trophic position of the deep-water ram’s horn squid Spirula spirula based on the nitrogen isotopic composition of amino acids.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksF2ksbg%3D&md5=b96b316f9b69f2edb186e174c9aedc5fCAS |

Olson, R. J., and Watters, G. M. (2003). A model of the pelagic ecosystem in the eastern tropical Pacific Ocean. Inter-American Tropical Tuna Commission Bulletin 22, 135–218.

Parry, M. (2008). Trophic variation with length in two ommastrephid squids, Ommastrephes bartramii and Sthenoteuthis oualaniensis. Marine Biology 153, 249–256.
Trophic variation with length in two ommastrephid squids, Ommastrephes bartramii and Sthenoteuthis oualaniensis.Crossref | GoogleScholarGoogle Scholar |

Pethybridge, H. R., Young, J. W., Kuhnert, P. M., and Farley, J. H. (2015). Using stable isotopes of albacore tuna and predictive models to characterize bioregions and examine ecological change in the SW Pacific Ocean. Progress in Oceanography 134, 293–303.
Using stable isotopes of albacore tuna and predictive models to characterize bioregions and examine ecological change in the SW Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |

Rosas-Luis, R., Salinas-Zavala, C. A., Koch, V., del Monte-Luna, P., and Morales-Zárate, M. V. (2008). Importance of jumbo squid Dosidicus gigas (Orbigny, 1835) in the pelagic ecosystem of the central Gulf of California. Ecological Modelling 218, 149–161.
Importance of jumbo squid Dosidicus gigas (Orbigny, 1835) in the pelagic ecosystem of the central Gulf of California.Crossref | GoogleScholarGoogle Scholar |

Ruiz-Cooley, R. I., and Gerrodette, T. (2012). Tracking large-scale latitudinal patterns of δ13C and δ15N along the E Pacific using epi-mesopelagic squid as indicators. Ecosphere 3, art63.
Tracking large-scale latitudinal patterns of δ13C and δ15N along the E Pacific using epi-mesopelagic squid as indicators.Crossref | GoogleScholarGoogle Scholar |

Ruiz-Cooley, R. I., Gendron, D., Aguíñiga, S., Mesnick, S., and Carriquiry, J. D. (2004). Trophic relationships between sperm whales and jumbo squid using stable isotope of C and N. Marine Ecology Progress Series 277, 275–283.
Trophic relationships between sperm whales and jumbo squid using stable isotope of C and N.Crossref | GoogleScholarGoogle Scholar |

Ruiz-Cooley, R. I., Markaida, U., Gendron, D., and Aguíñiga, S. (2006). Stable isotopes in jumbo squid (Dosidicus gigas) beaks to estimate its trophic position: comparison between stomach contents and stable isotopes. Journal of the Marine Biological Association of the United Kingdom 86, 437–445.
Stable isotopes in jumbo squid (Dosidicus gigas) beaks to estimate its trophic position: comparison between stomach contents and stable isotopes.Crossref | GoogleScholarGoogle Scholar |

Ruiz-Cooley, R. I., Villa, E. C., and Gould, W. R. (2010). Ontogenetic variation of δ13C and δ15N recorded in the gladius of the jumbo squid Dosidicus gigas: geographic differences. Marine Ecology Progress Series 399, 187–198.
Ontogenetic variation of δ13C and δ15N recorded in the gladius of the jumbo squid Dosidicus gigas: geographic differences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvFOmu7Y%3D&md5=76889cbfedefc04c42b999d16f1cacc7CAS |

Ruiz-Cooley, R. I., Ballance, L. T., and McCarthy, M. D. (2013). Range expansion of the jumbo squid in the NE Pacific: δ15N decrypts multiple origins, migration and habitat use. PLoS One 8, e59651.
Range expansion of the jumbo squid in the NE Pacific: δ15N decrypts multiple origins, migration and habitat use.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltFSnu7o%3D&md5=ca3b061552c5511004ee655e60f7bd2cCAS |

Stowasser, G., Pierce, G. J., Moffat, C. F., Collins, M. A., and Forsythe, J. W. (2006). Experimental study on the effect of diet on fatty acid and stable isotope profiles of the squid Lolliguncula brevis. Journal of Experimental Marine Biology and Ecology 333, 97–114.
Experimental study on the effect of diet on fatty acid and stable isotope profiles of the squid Lolliguncula brevis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkvVGjtb8%3D&md5=57c86a1c41e35fcfc98c9167b358e51dCAS |

Tam, J., Taylor, M. H., Blaskovic, V., and Volff, L. M. (2008). Trophic modeling of the Northern Humboldt Current ecosystem. Part I: comparing trophic linkages under La Niña and El Niño conditions. Progress in Oceanography 79, 352–365.
Trophic modeling of the Northern Humboldt Current ecosystem. Part I: comparing trophic linkages under La Niña and El Niño conditions.Crossref | GoogleScholarGoogle Scholar |

Wing, B. (2005). Unusual observations of fish and invertebrates from the Gulf of Alaska, 2004–05. AFSC Quarterly Research Reports July–Sept 2005. (Alaska Fisheries Science Center, Auke Bay Laboratory (ABL), Ocean Carrying Capacity Program.) Available at https://www.afsc.noaa.gov/quarterly/jas2005/divrptsABL1.htm [Verified 25 December 2017].

Wood, S. N. (2006). ‘Generalized Additive Models: an Introduction with R.’ (Chapman and Hall/CRC: Boca Raton, FL, USA.)

Wormuth, J. H. (1998). Workshop deliberations on the Ommastrephidae: a brief history of their systematics and a review of the systematics, distribution, and biology of the genera Martialia Rochebrune and Mabille, 1889, Todaropsis Girard, 1890, Dosidicus Steenstrup, 1857, Hyaloteuthis Gray, 1849, and Eucleoteuthis Berry, 1916. In ‘Systematics and Biogeography of Cephalopods. Vol. I. Smithsonian Contributions to Zoology 586(II)’. (Eds N. A. Voss, M. Vecchione, R. B. Toll, and M. J. Sweeney.) pp. 373–383. (Smithsonian Institution Press: Washington, DC, USA.)

Xavier, J. C., Allcock, A. L., Cherel, Y., Lipinski, M. R., Pierce, G. J., Rodhouse, P. G. K., Rosa, R., Shea, E. K., Strugnell, J. M., Vidal, E. A. G., Villanueva, R., and Ziegler, A. (2015). Future challenges in cephalopod research. Journal of the Marine Biological Association of the United Kingdom 95, 999–1015.
Future challenges in cephalopod research.Crossref | GoogleScholarGoogle Scholar |