Abstract
Cephalopods are well-documented for voracious and opportunistic feeding behaviors, but knowledge about individual niche partitioning in energy acquisition is still scarce. Here, we applied the stable isotope analysis to evaluate the individual diet specialization of female jumbo squid (Dosidicus gigas), which is an important pelagic commercial cephalopod and also acts as a vector of energy and nutrient transfer in the marine ecosystem. We detected the δ15N and δ13C values of each squid’s paired tissues; the digestive gland and mantle tissue were sampled from three regions (the Equatorial waters, waters off north and south Peruvian Exclusive Economic Zone) in the southeast Pacific. We found that the squid spanned more than one trophic level variation in the ranges of δ15N and δ13C values and consistently increased isotopic niche as they grew in each sampling region. Conversely, the variations between the paired tissues for each individual typically averaged from 0.82‰ to 1.92‰ for the δ15N values, and for the δ13C values, averaged from 1.18‰ to 1.65‰; the isotopic individuality index was close to 0. The inter-individual difference metrics (isotopic evenness and isotopic uniqueness) showed a variability of 1.1–1.7 factor when using the gonadosomatic index as a weight factor, and negligible change when weighed by mantle length, compared to the metrics without a weight factor added. The results indicate that the female jumbo squid is a diet generalist that is composed of individual specialization and that the individual diet specialization may be linked to energy acquisition for reproduction.
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Data availability
All data that support the findings of this study are included in the manuscript and supplementary material (Table S6). Data are, however, used under license from the Distant Squid Fisheries Sci-Tech Group (SHOU), and the usage is only permitted from the corresponding authors upon reasonable request.
References
Alegre A, Ménard F, Tafur R, Espinoza P, Argüelles J, Maehara V, Flores O, Simier M, Bertrand A (2014) Comprehensive model of jumbo squid dosidicus gigas trophic ecology in the northern humboldt current system. PLoS ONE 9:e85919. https://doi.org/10.1371/journal.pone.0085919
Anderson RC, Wood JB, Mather JA (2008) Octopus vulgaris in the Caribbean is a specializing generalist. Mar Ecol Prog Ser 371:199–202. https://doi.org/10.3354/meps07649
Arkhipkin A (1992) Reproductive system structure, development and function in cephalopods with a new general scale for maturity stages. J Northwest Atl Fish Sci 12:63–74
Arkhipkin A, Argüelles J, Shcherbich Z, Yamashiro C (2015) Ambient temperature influences adult size and life span in jumbo squid (Dosidicus gigas). Can J Fish Aquat Sci 72:400–409. https://doi.org/10.1139/cjfas-2014-0386
Barton MB, Litvin SY, Vollenweider JJ, Heintz RA, Norcross BL, Boswell KM (2019) Experimental determination of tissue turnover rates and trophic discrimination factors for stable carbon and nitrogen isotopes of Arctic Sculpin (Myoxocephalus scorpioides): A common Arctic nearshore fish. J Exp Mar Bio Ecol 511:60–67. https://doi.org/10.1016/j.jembe.2018.11.005
Bolnick DI, Yang LH, Fordyce JA, Davis JM, Svanbäck R (2002) Measuring individual-level resource specialization. Ecology 83:2936–2941. https://doi.org/10.1890/0012-9658(2002)083[2936:MILRS]2.0.CO;2
Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. https://doi.org/10.1086/343878
Bolnick DI, Ingram T, Stutz William E, Snowberg Lisa K, Lau On L, Paull Jeff S (2010) Ecological release from interspecific competition leads to decoupled changes in population and individual niche width. Proc Royal Soc B 277:1789–1797. https://doi.org/10.1098/rspb.2010.0018
Boyle P, Rodhouse P (2005) Cephalopods: ecology and fisheries. Wiley-Blackwell, Oxford, UK
Bruno C, Cornejo CF, Riera R, Ibáñez CM (2021) What is on the menu? Feeding, consumption and cannibalism in exploited stocks of the jumbo squid Dosidicus gigas in south-central Chile. Fish Res 233:105722. https://doi.org/10.1016/j.fishres.2020.105722
Buchheister A, Latour RJ (2010) Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Can J Fish Aquat Sci 67:445–461. https://doi.org/10.1139/F09-196
Busst GMA, Britton JR (2018) Tissue-specific turnover rates of the nitrogen stable isotope as functions of time and growth in a cyprinid fish. Hydrobiologia 805:49–60. https://doi.org/10.1007/s10750-017-3276-2
Chen XJ, Liu BL, Fang Z, Li JH (2019) Tou Zu Gang. China Ocean Press, Beijing
Chen X, Han F, Zhu K, Punt AE, Lin D (2020) The breeding strategy of female jumbo squid Dosidicus gigas: energy acquisition and allocation. Sci Rep 10:9639. https://doi.org/10.1038/s41598-020-66703-5
Chong J, Oyarzún C, Galleguillos R, Tarifeño E, Sepúlveda R, Ibáñez C (2005) Parámetros biológico-pesqueros de la jibia Dosidicus gigas (Orbigny, 1835) (Cephalopoda: Ommastrephidae) frente a la costa de Chile central (29°S-40°S) durante 1993–1994. Gayana (concepción) 69:319–328. https://doi.org/10.4067/S0717-65382005000200012
Clarke A (2019) Energy Flow in Growth and Production. Trends Ecol Evol 34:502–509. https://doi.org/10.1016/j.tree.2019.02.003
Costa-Pereira R, Araújo MS, Souza FL, Ingram T (2019) Competition and resource breadth shape niche variation and overlap in multiple trophic dimensions. Proc Royal Soc B 286:20190369. https://doi.org/10.1098/rspb.2019.0369
Cucherousset J, Villéger S (2015) Quantifying the multiple facets of isotopic diversity: New metrics for stable isotope ecology. Ecol Indic 56:152–160. https://doi.org/10.1016/j.ecolind.2015.03.032
DeSantis LRG, Pardi MI, Du A, Greshko MA, Yann LT, Hulbert RC, Louys J (2022) Global long-term stability of individual dietary specialization in herbivorous mammals. Proc Royal Soc B 289:20211839. https://doi.org/10.1098/rspb.2021.1839
Eddy TD, Bernhardt JR, Blanchard JL, Cheung WWL, Colléter M, du Pontavice H, Fulton EA, Gascuel D, Kearney KA, Petrik CM, Roy T, Rykaczewski RR, Selden R, Stock CA, Wabnitz CCC, Watson RA (2021) Energy flow through marine ecosystems: confronting transfer efficiency. Trends Ecol Evol 36:76–86. https://doi.org/10.1016/j.tree.2020.09.006
FAO (2022) The state of world fisheries and aquaculture 2022. Towards Blue Transformation, FAO, Rome, Italy
Field JC, Elliger C, Baltz K, Gillespie GE, Gilly WF, Ruiz-Cooley RI, Pearse D, Stewart JS, Matsubu W, Walker WA (2013) Foraging ecology and movement patterns of jumbo squid (Dosidicus gigas) in the California Current System. Deep-Sea Res II 95:37–51. https://doi.org/10.1016/j.dsr2.2012.09.006
Gallagher CA, Chimienti M, Grimm V, Nabe-Nielsen J (2022) Energy-mediated responses to changing prey size and distribution in marine top predator movements and population dynamics. J Anim Ecol 91:241–254. https://doi.org/10.1111/1365-2656.13627
Gao X, Gong Y, Chen X, Li Y (2022) Dietary shifts and niche partitioning throughout ontogeny reduce intraspecific competition in a pelagic generalist predator. Mar Ecol Prog Ser 692:81–97. https://doi.org/10.3354/meps14079
Golikov AV, Ceia FR, Sabirov RM, Zaripova ZI, Blicher ME, Zakharov DV, Xavier JC (2018) Ontogenetic changes in stable isotope (δ13C and δ15N) values in squid Gonatus fabricii (Cephalopoda) reveal its important ecological role in the Arctic. Mar Ecol Prog Ser 606:65–78. https://doi.org/10.3354/meps12767
Golikov AV, Ceia FR, Sabirov RM, Ablett JD, Gleadall IG, Gudmundsson G, Hoving HJ, Judkins H, Pálsson J, Reid AL, Rosas-Luis R, Shea EK, Schwarz R, Xavier JC (2019) The first global deep-sea stable isotope assessment reveals the unique trophic ecology of Vampire Squid Vampyroteuthis infernalis (Cephalopoda). Sci Rep 9:19099. https://doi.org/10.1038/s41598-019-55719-1
Gong Y, Ruiz-Cooley RI, Hunsicker ME, Li Y, Chen X (2018) Sexual dimorphism in feeding apparatus and niche partitioning in juvenile jumbo squid Dosidicus gigas. Mar Ecol Prog Ser 607:99–112. https://doi.org/10.3354/meps12768
Gong Y, Li Y, Chen X, Yu W (2020) Trophic niche and diversity of a pelagic squid (Dosidicus gigas): A comparative study using stable isotope, fatty acid, and feeding apparatuses morphology. Front Mar Sci 7:642. https://doi.org/10.3389/fmars.2020.00642
Han F, Chen X, Lin D (2020) Energy accumulation and its relation to sea surface environments in Dosidicus gigas from the equatorial water of the Eastern Pacific. J Fish Sci China 27:427–437. https://doi.org/10.3724/SP.J.1118.2020.19224
Ibáñez CM, Arancibia H, Cubillos LA (2008) Biases in determining the diet of jumbo squid Dosidicus gigas (D’ Orbigny 1835) (Cephalopoda: Ommastrephidae) off southern-central Chile (34°S–40°S). Helgol Mar Res 62:331–338. https://doi.org/10.1007/s10152-008-0120-0
Ibáñez CM, Riera R, Leite T, Díaz-Santana-Iturrios M, Rosa R, Pardo-Gandarillas MC (2021) Stomach content analysis in cephalopods: past research, current challenges, and future directions. Rev Fish Biol Fish 31:505–522. https://doi.org/10.1007/s11160-021-09653-z
ICES (2010) Report of the Workshop on Sexual Maturity Staging of Cephalopods, 8–11 November 2010. Livorno, Italy
Ivanovic ML (2010) Alimentación del calamar Illex argentinus en la región patagónica durante el verano de los años 2006, 2007 y 2008. Revista De Invest Desarrollo Pesquero 20:51–63
Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER – stable isotope bayesian ellipses in R. J Anim Ecol 80:595–602. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Jereb P, Roper CFE, Norman MD, Finn JK (2016) Cephalopods of the world. In: Jereb P (ed) An annotated and illustrated catalogue of cephalopod species known to date, vol 3. Octopods and Vampire Squids, Rome
Kessler WS (2006) The circulation of the eastern tropical Pacific: A review. Prog Oceanogr 69:181–217. https://doi.org/10.1016/j.pocean.2006.03.009
Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S (2012) Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87:545–562. https://doi.org/10.1111/j.1469-185X.2011.00208.x
Leite TS, Batista AT, Lima FD, Barbosa JC, Mather J (2016) Geographic variability of Octopus insularis diet: from oceanic island to continental populations. Aquat Biol 25:17–27
Li YK, Feng D, Gao XD, Chen XJ, Gong Y (2021) Comparative study on the feeding habits of Sthenoteuthis oualaniensis and Dosidicus gigas in the eastern equatorial pacific ocean. Oceanol Limnol Sin 52:1303–1314. https://doi.org/10.11693/hyhz20210300062
Lian J, Feng Y, Lin D (2022) Relative energy accumulation in soma and gonad tissues of female Dosidicus gigas and relation to environmental effects. South China Fish Sci 18:34–43. https://doi.org/10.12131/20210219
Lin D, Chen X, Chen Y, Fang Z (2015) Sex-specific reproductive investment of summer spawners of Illex argentinus in the southwest Atlantic. Invertebr Biol 134:203–213. https://doi.org/10.1111/ivb.12088
Lin D, Xuan S, Chen Z, Chen X (2019) The ovarian development, fecundity and hypothesis on spawning pattern of common cuttlefish Sepia officinalis off Mauritania. Fish Res 210:193–197. https://doi.org/10.1016/j.fishres.2018.08.003
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. Fish Res 79:16–27. https://doi.org/10.1016/j.fishres.2006.02.016
Markaida U, Sosa-Nishizaki O (2003) Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the gulf of california, Mexico. J Mar Biol Assoc UK 83:507–522. https://doi.org/10.1017/S0025315403007434h
Martínez-Baena F, Navarro J, Albo-Puigserver M, Palomera I, Rosas-Luis R (2016) Feeding habits of the short-finned squid Illex coindetii in the western Mediterranean Sea using combined stomach content and isotopic analysis. J Mar Biol Assoc UK 96:1235–1242. https://doi.org/10.1017/S0025315415001940
Mather JA, Leite TS, Batista AT (2012) Individual prey choices of octopuses: Are they generalist or specialist? Current Zool 58:597–603. https://doi.org/10.1093/czoolo/58.4.597
Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305. https://doi.org/10.1111/j.1365-2656.2010.01753.x
McCutchan JH Jr, Lewis WM Jr, 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
McInturf AG, Pollack L, Yang LH, Spiegel O (2019) Vectors with autonomy: what distinguishes animal-mediated nutrient transport from abiotic vectors? Biol Rev 94:1761–1773. https://doi.org/10.1111/brv.12525
Navarro J, Coll M, Somes CJ, Olson RJ (2013) Trophic niche of squids: Insights from isotopic data in marine systems worldwide. Deep-Sea Res II 95:93–102. https://doi.org/10.1016/j.dsr2.2013.01.031
Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, Fogel ML, Estes JA (2009) Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974. https://doi.org/10.1890/07-1812.1
Newsome SD, Yeakel JD, Wheatley PV, Tinker MT (2012) Tools for quantifying isotopic niche space and dietary variation at the individual and population level. J Mammal 93:329–341. https://doi.org/10.1644/11-mamm-s-187.1
Nigmatullin CM, Markaida U (2009) Oocyte development, fecundity and spawning strategy of large sized jumbo squid Dosidicus gigas. J Mar Biol Assoc UK 89:789–801. https://doi.org/10.1017/S0025315408002853
Nigmatullin CM, Nesis K, Arkhipkin A (2001) A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae). Fish Res 54:9–19
Pennington JT, Mahoney KL, Kuwahara VS, Kolber DD, Calienes R, Chavez FP (2006) Primary production in the eastern tropical Pacific: A review. Prog Oceanogr 69:285–317. https://doi.org/10.1016/j.pocean.2006.03.012
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 Bio Ecol 409:290–299. https://doi.org/10.1016/j.jembe.2011.09.009
Pethybridge HR, Nichols PD, Virtue P, Jackson GD (2013) The foraging ecology of an oceanic squid, Todarodes filippovae: The use of signature lipid profiling to monitor ecosystem change. Deep-Sea Res II 95:119–128. https://doi.org/10.1016/j.dsr2.2012.07.025
Portner EJ, Markaida U, Robinson CJ, Gilly WF (2020) Trophic ecology of Humboldt squid, Dosidicus gigas, in conjunction with body size and climatic variability in the Gulf of California, Mexico. Limnol Oceanogr 65:732–748. https://doi.org/10.1002/lno.11343
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
Quirós-Collazos L, Calvo E, Schouten S, van der Meer MTJ, Rodrigo-Gámiz M, Pena LD, Cacho I, Pelejero C (2020) Controls on primary productivity in the eastern equatorial pacific, east of the galapagos Islands, during the penultimate deglaciation. Paleoceanogr Paleoclimatol 35:003777. https://doi.org/10.1029/2019PA003777
Quispe-Machaca M, Guzmán-Rivas FA, Ibáñez CM, Urzúa Á (2021) Intra-individual variability in biochemical constituents and fatty acid composition of adult jumbo squid (Dosidicus gigas) in the southeastern Pacific Ocean. J Sea Res 174:102082. https://doi.org/10.1016/j.seares.2021.102082
Quispe-Machaca M, Guzmán-Rivas FA, Ibáñez CM, Urzúa Á (2022) Trophodynamics of the jumbo squid Dosidicus gigas during winter in the Southeast Pacific Ocean off the coast of Chile: Diet analyses and fatty acid profile. Fish Res 245:106154. https://doi.org/10.1016/j.fishres.2021.106154
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Riverón S, Raoult V, Baylis AMM, Jones KA, Slip DJ, Harcourt RG (2021) Pelagic and benthic ecosystems drive differences in population and individual specializations in marine predators. Oecologia 196:891–904. https://doi.org/10.1007/s00442-021-04974-z
Rocha F, Guerra Á, González ÁF (2001) A review of reproductive strategies in cephalopods. Biol Rev 76:291–304. https://doi.org/10.1017/S1464793101005681
Rosa R, Yamashiro C, Markaida U, Rodhouse PGK, Waluda CM, Salinas-Zavala CA, Keyl F, O’Dor R, Stewart JS, Gilly WF (2013) Dosidicus gigas, Humboldt Squid. In: Rosa R, Pierce G, O’Dor R (eds) Advances in Squid Biology, Ecology and Fisheries Part II - Oegopsid squids. Nova Science Publishers, New York, pp 169–206
Rosas-Hernández MP, Aurioles-Gamboa D, Hernández-Camacho CJ (2019) Specialized foraging habits of adult female California sea lions Zalophus californianus. Mar Mamm Sci 35:1463–1488. https://doi.org/10.1111/mms.12603
Rosas-Luis R, Chompoy-Salazar L (2016) Description of food sources used by jumbo squid Dosidicus gigas (D’Orbigny, 1835) in Ecuadorian waters during 2014. Fish Res 173:139–144. https://doi.org/10.1016/j.fishres.2015.08.006
Rosas-Luis R, Tafur-Jimenez R, Alegre-Norza AR, Castillo-Valderrama PR, Cornejo-Urbina RM, Salinas-Zavala C, Sánchez P (2011) Trophic relationships between the jumbo squid (Dosidicus gigas ) and the lightfish (Vinciguerria lucetia) in the humboldt current system off Peru. Sci Mar 75:549–557. https://doi.org/10.3989/SCIMAR.2011.75N3549
Rosas-Luis R, Sánchez P, Portela JM, del Rio JL (2014) Feeding habits and trophic interactions of Doryteuthis gahi, Illex argentinus and Onykia ingens in the marine ecosystem off the Patagonian Shelf. Fish Res 152:37–44. https://doi.org/10.1016/j.fishres.2013.11.004
Rosas-Luis R, Navarro J, Sánchez P, Del Río JL (2016) Assessing the trophic ecology of three sympatric squid in the marine ecosystem off the Patagonian Shelf by combining stomach content and stable isotopic analyses. Mar Biol Res 12:402–411. https://doi.org/10.1080/17451000.2016.1142094
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, Markaida U, Gendron D, Aguíñiga S (2006) Stable isotopes in jumbo squid (Dosidicus gigas) beaks to estimate its trophic position: comparison between stomach contents and stable isotopes. J Mar Biol Assoc UK 86:437–445. https://doi.org/10.1017/S0025315406013324
Ruiz-Cooley RI, Villa EC, Gould WR (2010) Ontogenetic variation of δ13C and δ15N 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
Scheel D, Leite T, Mather J, Langford K (2017) Diversity in the diet of the predator Octopus cyanea in the coral reef system of Moorea, French Polynesia. J Nat Hist 51:2615–2633. https://doi.org/10.1080/00222933.2016.1244298
Shaner P-JL, Ke L-h (2022) Niche overlap in rodents increases with competition but not ecological opportunity: A role of inter-individual difference. J Anim Ecol 91:1679–1692. https://doi.org/10.1111/1365-2656.13750
Shero MR, Goetz KT, Costa DP, Burns JM (2018) Temporal changes in Weddell seal dive behavior over winter: Are females increasing foraging effort to support gestation? Ecol Evol 8:11857–11874. https://doi.org/10.1002/ece3.4643
Stowasser G, Pierce GJ, Moffat CF, Collins MA, Forsythe JW (2006) Experimental study on the effect of diet on fatty acid and stable isotope profiles of the squid Lolliguncula brevis. J Exp Mar Bio Ecol 333:97–114. https://doi.org/10.1016/j.jembe.2005.12.008
Winckler G, Anderson RF, Jaccard SL, Marcantonio F (2016) Ocean dynamics, not dust, have controlled equatorial Pacific productivity over the past 500,000 years. PNAS 113:6119–6124. https://doi.org/10.1073/pnas.1600616113
Wolf N, Webster SR, Welker JM, Harris BP (2019) Assessing the relationship between diet and size-at-age in Pacific halibut (Hippoglossus stenolepis) using δ13C and δ15N analysis. Can J Fish Aquat Sci 76:1–6. https://doi.org/10.1139/cjfas-2018-0380
Xavier J, Cherel Y (2021) Cephalopod beak guide for the Southern Ocean: An update on taxonomy, revised. British Antarctic Survey, Cambridge
Xavier JC, Cherel Y, Ceia FR, Queirós JP, Guimarães B, Rosa R, Cunningham DM, Moors PJ, Thompson DR (2018) Eastern rockhopper penguins Eudyptes filholi as biological samplers of juvenile and sub-adult cephalopods around Campbell Island, New Zealand. Polar Biol 41:1937–1949. https://doi.org/10.1007/s00300-018-2333-2
Xavier JC, Golikov AV, Queirós JP, Perales-Raya C, Rosas-Luis R, Abreu J, Bello G, Bustamante P, Capaz JC, Dimkovikj VH, González AF, Guímaro H, Guerra-Marrero A, Gomes-Pereira JN, Kubodera T, Laptikhovsky V, Lefkaditou E, Lishchenko F, Luna A, Liu B, Pierce GJ, Pissarra V, Reveillac E, Romanov EV, Rosa R, Roscian M, Rose-Mann L, Rouget I, Sánchez P, Sánchez-Márquez A, Seixas S, Souquet L, Varela J, Vidal EAG, Cherel Y (2022) The significance of cephalopod beaks as a research tool: An update. Front Physiol. https://doi.org/10.3389/fphys.2022.1038064
Zango L, Navarro-Herrero L, García-Vendrell M, Safi K, González-Solís J (2020) Niche partitioning and individual specialization among age, breeding status and sex classes in a long-lived seabird. Anim Behav 170:1–14. https://doi.org/10.1016/j.anbehav.2020.10.001
Zar JH (1999) Biostatistical Analysis, 4th edn. Prentice Hall, New Jersey
Acknowledgements
This work is a contribution of the Distant Squid Fisheries Sci-Tech Group, SHOU. We thank the staff members of the Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, Shanghai Ocean University for assisting at the laboratory. We are grateful to Dr. Kindong Richard for his help with editing the revised manuscript, and to the Editor Prof. Rui Rosa and the anonymous reviewers for their constructive comments and suggestions on the manuscript.
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This work was supported by the National Natural Science Foundation of China (41876144), Shanghai Talent Development Funding (2020107) and Project on the Survey and Monitor-Evaluation of Global Fishery Resources (Comprehensive Scientific Survey of Fishery Resources at the High Seas) to DL, and National Key Research and Development Project of China (2019YFD0901404), National Natural Science Foundation of China (41876141) and Shanghai Science and Technology Innovation Program (19DZ1207502) to XC.
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DL and XC devised the study. YF and KZ conducted the laboratory experiment. DL and YF performed the data analysis. DL, YF, K.Z, and XC interpreted the results. D.L, and Y.F wrote the first draft. All the authors edited and approved the final manuscript.
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Specimens were collected as dead squids from the commercial jigging fisheries landings, during the fishing season between 2017 and 2020. The specimens were analyzed in the laboratory using methods that are in line with current Chinese national standards, namely Laboratory Animals-General Requirements for Animal Experiment (GB/T 35823–2018). As all material sampled in this work was obtained from commercial jigging fisheries landings and already dead, there was no requirement for ethical approval of sampling protocols as it did not include live organisms.
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Feng, Y., Zhu, K., Lin, D. et al. Individual diet specialization in the female jumbo squid Dosidicus gigas. Mar Biol 170, 76 (2023). https://doi.org/10.1007/s00227-023-04227-y
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DOI: https://doi.org/10.1007/s00227-023-04227-y