Journal of Oceanology and Limnology

, Volume 37, Issue 4, pp 1440–1448 | Cite as

Impacts of El Niño on the somatic condition of Humboldt squid based on the beak morphology

  • Guanyu Hu
  • Wei Yu
  • Bai Li
  • Dongyan Han
  • Xinjun ChenEmail author
  • Yong Chen
  • Jianhua Li
Aquaculture and Fisheries


The Humboldt squid Dosidicus gigas has a short life span, and environmental variability plays a significant role in regulating its population dynamics and distribution. An analysis of 1 096 samples of D. gigas collected by the Chinese commercial fishing vessels during 2013, 2014, and 2016 off the Peruvian Exclusive Economic Zone, was conducted to evaluate the impacts of El Niño events on the somatic condition of D. gigas. This study indicates that the slopes of all beak variables in relation to ML for females were greater than those of males during 2013, 2014, and 2016, and slopes of the upper crest length and the lower rostrum length significantly differed between females and males in 2013 ( P <0.05). Variation in the slopes for beak variables among years was studied; no significant difference was observed (ANCOVA, P >0.05). The Fulton’s condition coefficients ( K ) of females and males in 2013 and 2014 were significantly greater than those in 2016 ( P < 0.01). The K values of females were greater than those of males in 2013, 2014, and 2016, and K values significantly differed between females and males in 2013. In normal years, the chlorophyll a (Chl a ) concentration showed an N-shaped variability from January to December. However, in the El Niño period, it tended to weaken the upwelling coupled with warm and low Chl a concentration waters. We suggest that the poor somatic condition of D. gigas during the El Niño year was resulted from the low Chl a concentration in the waters, and the abundance of D. gigas would decrease due to the unfavourable environment and the lack of prey items in the El Niño year.


El Niño event Dosidicus gigas somatic condition abundance beak morphology 


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The data analysis and paper writing were done mainly when the senior author studied in Dr. CHEN Yong’s lab in the School of Marine Sciences, the University of Maine, which is supported by Shanghai Ocean University and the University of Maine. We thank XING Lei (Ocean University of China) for statistical consultancy and advice on the figures.


  1. Argüelles J, Tafur R. 2010. New insights on the biology of the jumbo squid Dosidicus gigas in the Northern Humboldt Current System: size at maturity, somatic and reproductive investment. Fisheries Research, 106(2): 185–192.CrossRefGoogle Scholar
  2. Arkhipkin A I, Rodhouse P G K, Pierce G J, Sauer W, Sakai M, Allcock L, Arguelles J, Bower J R, Castillo G, Ceriola L, Chen C S, Chen X J, Diaz–Santana M, Downey N, González A F, Amores J G, Green C P, Guerra A, Hendrickson L C, Ibáñez C, Ito K, Jereb P, Kato Y, Katugin O N, Kawano M, Kidokoro H, Kulik V V, Laptikhovsky V V, Lipinski M R, Liu B L, Mariátegui L, Marin W, Medina A, Miki K, Miyahara K, Moltschaniwskyj N, Moustahfid H, Nabhitabhata J, Nanjo N, Nigmatullin C M, Ohtani T, Pecl G, Perez J A A, Piatkowski U, Saikliang P, Salinas–Zavala C A, Steer M, Tian Y J, Ueta Y, Vijai D, Wakabayashi T, Yamaguchi T, Yamashiro C, Yamashita N, Zeidberg L D. 2015b. World squid fisheries. Reviews in Fisheries Science & Aquaculture, 23(2): 92–252.CrossRefGoogle Scholar
  3. Arkhipkin A, Argüelles J, Shcherbich Z, Yamashiro C. 2015a. Ambient temperature influences adult size and life span in jumbo squid( Dosidicus gigas ). Canadian Journal of Fisheries and Aquatic Sciences, 72(3): 400–409.CrossRefGoogle Scholar
  4. Barber R T, Sanderson M P, Lindley S T, Chai F, Newton J, Trees C C, Foley D G, Chavez F P. 1996. Primary productivity and its regulation in the equatorial Pacific during and following the 1991–199. El Niño. Deep Sea Research Part II: Topical Studies in Oceanography, 43(4–6): 933–969.CrossRefGoogle Scholar
  5. Bazzino Ferreri G A. 2014. Length–weight relationships and condition factors of the humboldt squid( Dosidicus gigas ) from the gulf of california and the pacific ocean. Journal of Shellfish Research, 33(3): 769–780.CrossRefGoogle Scholar
  6. Castro J J, Hernández–García V. 1995. Ontogenetic changes in mouth structures, foraging behaviour and habitat use of Scomber japonicus and Illex coindetii. Scientia Marina, 59(3–4): 347–355.Google Scholar
  7. Chen X J, Tian S Q, Chen Y, Liu B L. 2010. A modeling approach to identify optimal habitat and suitable fishing grounds for neon flying squid( Omm a strephes bartramii ) in the Northwest Pacific Ocean. Fishery Bulletin, 108(1): 1–14.Google Scholar
  8. Clarke M R. 1962. The identification of cephalopod "beaks" and the relationship between break size and total body weight. Bulletin of the British Museum( Natural History )( Zoology ), 8: 419–480.Google Scholar
  9. Espinoza–Morriberón D, Echevin V, Colas F, Tam J, Ledesma J, Vásquez L, Graco M. 2017. Impacts of El Niño events on the Peruvian upwelling system productivity. Journal of Geophysical Research: Oceans, 122(7): 5 423–5 444, Scholar
  10. Fang Z, Chen X J, Su H, Thompson K, Chen Y. 2017. Evaluation of stock variation and sexual dimorphism of beak shape of neon flying squid, Ommastrephes bartramii, based on geometric morphometrics. Hydrobiologia, 784(1): 367–380.CrossRefGoogle Scholar
  11. Fang Z, Liu B L, Chen X J, Jin Y, Li J H, Chen Y. 2016. Sexual asynchrony in the development of beak pigmentation for the neon flying squid Ommastrephes bartramii in the North Pacific Ocean. Fisheries Science, 82(5): 737–746.CrossRefGoogle Scholar
  12. Fang Z, Liu B L, Li J H, Su H, Chen X J. 2014. Stock identification of neon flying squid( Ommastrephes bartramii ) in the North Pacific Ocean on the basis of beak and statolith morphology. Scientia Marina, 78(2): 239–248.CrossRefGoogle Scholar
  13. Fang Z, Xu L L, Chen X J, Liu B L, Li J H, Chen Y. 2015. Beak growth pattern of purpleback flying squid Sthenoteuthis oualaniensis in the eastern tropical Pacific equatorial waters. Fisheries Science, 81(3): 443–452.CrossRefGoogle Scholar
  14. Field J C, Baltz K, Phillips A J, Walker W A. 2007. Range expansion and trophic interactions of the jumbo squid, Dosidicus Gigas, in the California Current. California Cooperative Oceanic Fisheries Investigations Report, 48: 131–146.Google Scholar
  15. Franco–Santos R M, Iglesias J, Domingues P M, Vidal E A G. 2014. Early beak development in Argonauta nodosa and Octopus vulgaris(Cephalopoda: incirrata) paralarvae suggests adaptation to different feeding mechanisms. Hydrobiologia, 725(1): 69–83.CrossRefGoogle Scholar
  16. Franco–Santos R M, Vidal E A G. 2014. Beak development of early squid paralarvae(Cephalopoda: teuthoidea) may reflect an adaptation to a specialized feeding mode. Hydrobiologia, 725(1): 85–103.CrossRefGoogle Scholar
  17. Froese R. 2006. Cube law, condition factor and weight–length relationships: history, meta–analysis and recommendations. Journal of Applied Ichthyology, 22(4): 241–253.CrossRefGoogle Scholar
  18. García V H. 2003. Growth and pigmentation process of the beaks of Todaropsis eblanae(Cephalopoda: ommastrephidae). Berliner Pal ä obiologische Abh andlungen, Berlin, 3: 131–140.Google Scholar
  19. Gröger J, Piatkowski U, Heinemann H. 2000. Beak length analysis of the Southern Ocean squid Psychroteuthis glacialis(Cephalopoda: psychroteuthidae) and its use for size and biomass estimation. Polar Biology, 23(1): 70–74.CrossRefGoogle Scholar
  20. Guerra Á, Rodríguez–Navarro A B, González Á F, Romanek C S, Álvarez–Lloret P, 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: Journal du Conseil, 67(7): 1 425–1 431.CrossRefGoogle Scholar
  21. Hernańdez–García V, Piatkowski U, Clarke M R. 1998. Development of the darkening of Todarodes sagittatus beaks and its relation to growth and reproduction. South African Journal of Marine Science, 20(1): 363–373.CrossRefGoogle Scholar
  22. Hoving H J T, Gilly W F, Markaida U, Benoit–Bird K J, Brown Z W, Daniel P, Field J C, Parassenti L, Liu B L, Campos B. 2013. Extreme plasticity in life–history strategy allows a migratory predator(jumbo squid) to cope with a changing climate. Global Change Biology, 19(7): 2 089–2 103.CrossRefGoogle Scholar
  23. Hu G Y, Chen X J, Fang Z. 2016a. Effect of individual growth on beak morphometry of jumbo flying squid, Dosidicus gigas off the Peruvian Exclusive Economic Zone. Journal of Fisheries of China, 40(1): 36–44(in Chinese with English abstract)Google Scholar
  24. Hu G Y, Fang Z, Liu B L, Yang D, Chen X J, Chen Y. 2016b. Age, growth and population structure of jumbo flying squid Dosidicus gigas off the Peruvian Exclusive Economic Zone based on beak microstructure. Fisheries Science, 82(4): 579–604.CrossRefGoogle Scholar
  25. Hu G Y, Jin Y, Chen X J. 2017. Beak morphological characteristics of Dosidicus gigas off the Peruvian Exclusive Economic Zone(EEZ) and their relationship with body size and daily age. Marine Fisheries, 39(4): 361–371.(in Chinese with English abstract)Google Scholar
  26. Ikica Z, Vuković V, Đurović M, Joksimović A, Krstuluvić Šifner S. 2014. Analysis of beak morphometry of the horned octopus Eledone cirrhosa, Lamarck 1798(Cephalopoda: octopoda), in the south–eastern Adriatic Sea. Acta Adriatica, 55(1): 43–56.Google Scholar
  27. Jackson G D, McKinnon J F. 1996. Beak length analysis of arrow squid Nototodarus sloanii(Cephalopoda: ommastrephidae) in southern New Zealand waters. Polar biology, 16(3): 227–230.CrossRefGoogle Scholar
  28. Keyl F, Argüelles J, Mariátegui L, Tafur R, Wolff M, Yamashiro C. 2008. A hypothesis on range expansion and spatiotemporal shifts in size–at–maturity of jumbo squid( Dosidicus gigas ) in the Eastern Pacific Ocean. CalCOFI Report, 49: 119–128.Google Scholar
  29. Lalas C. 2009. Estimates of size for the large octopus Macroctopus maorum from measures of beaks in prey remains. New Zealand Journal of Marine and Freshwater Research, 43(2): 635–642.CrossRefGoogle Scholar
  30. Lefkaditou E, Bekas P. 2004. Analysis of beak morphometry of the horned octopus Eledone cirrhosa(Cephalopoda: octopoda) in the Thracian Sea(NE Mediterranean). Mediterranean Marine Science, 5(1): 143–149.CrossRefGoogle Scholar
  31. Lipiński M R, Underhill L G. 1995. Sexual maturation in squid: quantum or continuum? South African Journal of Marine Science, 15(1): 207–223.CrossRefGoogle Scholar
  32. Liu B L, Chen X J, Chen Y, Tian S Q, Li J H, Fang Z, Yang M Z. 2013. Age, maturation, and population structure of the Humboldt squid Dosidicus gigas off the Peruvian Exclusive Economic Zones. Chinese Journal of Oceanology and Limnology, 31(1): 81–91.CrossRefGoogle Scholar
  33. Liu B L, Fang Z, Chen X J, Chen Y. 2015. Spatial variations in beak structure to identify potentially geographic populations of Dosidicus gigas in the Eastern Pacific Ocean. Fisheries Research, 164: 185–192.CrossRefGoogle Scholar
  34. Lu C C, Ickeringill R. 2002. Cephalopod beak identification and biomass estimation techniques: tools for dietary studies of southern Australian finfishes. Museum Victoria Science Reports, Victoria, Australia.Google Scholar
  35. Markaida U, Quiñónez–Velázquez C, Sosa–Nishizaki O. 2004. Age, growth and maturation of jumbo squid Dosidicus gigas(Cephalopoda: ommastrephidae) from the Gulf of California, Mexico. Fisheries Research, 66(1): 31–47.CrossRefGoogle Scholar
  36. Martínez P, Sanjuan A, Guerra A. 2002. Identification of Illex coindetii, I. illecebrosus and I. argentinus(Cephalopoda: ommastrephidae) throughout the Atlantic Ocean; by body and beak characters. Marine Biology, 141(1): 131–143.CrossRefGoogle Scholar
  37. Mejia–Rebollo A, Quiñónez–Velázquez C, Salinas–Zavala C A, Markaida U. 2008. Age, growth and maturity of jumbo squid( Dosidicus gigas d’Orbigny, 1835) off the western coast of the Baja California Peninsula. CalCOFI Rep orts, 49: 256–262.Google Scholar
  38. Miserez A, Li Y L, Waite J H, Zok F. 2007. Jumbo squid beaks: inspiration for design of robust organic composites. Acta Biomaterialia, 3(1): 139–149.CrossRefGoogle Scholar
  39. Miserez A, Schneberk T, Sun C J, Zok F W, Waite J H. 2008. The transition from stiff to compliant materials in squid beaks. Science, 319(5871): 1 816–1 819.CrossRefGoogle Scholar
  40. Nigmatullin C M, Nesis K N, Arkhipkin A. 2001. A review of the biology of the jumbo squid Dosidicus gigas(Cephalopoda: ommastrephidae). Fisheries Research, 54(1): 9–19.CrossRefGoogle Scholar
  41. Pecl G T, Moltschaniwskyj N A, Tracey S R, Jordan A R. 2004. Inter–annual plasticity of squid life history and population structure: ecological and management implications. Oecologia, 140(2): 380.CrossRefGoogle Scholar
  42. Radenac M H, Léger F, Singh A, Delcroix T. 2012. Sea surface chlorophyll signature in the tropical Pacific during eastern and central Pacific ENSO events. Journal of Geophysical Research: Oceans, 117(C4): C04007, 1029/2011JC007841.CrossRefGoogle Scholar
  43. Raya C P, Hernández–González C L. 1998. Growth lines within the beak microstructure of the octopus Octopus vulgaris Cuvier, 1797. South African Journal of Marine Science, 20(1): 135–142.CrossRefGoogle Scholar
  44. Robinson C J, Gómez–Gutiérrez J, de León D A S. 2013. Jumbo squid( Dosidicus gigas ) landings in the Gulf of California related to remotely sensed SST and concentrations of chlorophyll a(1998–2012). Fisheries Research, 137: 97–103.CrossRefGoogle Scholar
  45. Rodríguez–Domínguez A, Rosas C, Méndez–Loeza I, Markaida U. 2013. Validation of growth increments in stylets, beaks and lenses as ageing tools in Octopus maya. Journal of Experimental Marine Biology and Ecology, 449: 194–199.CrossRefGoogle Scholar
  46. Sandoval–Castellanos E, Uribe–Alcocer M, Díaz–Jaimes P. 2007. Population genetic structure of jumbo squid( Dosidicus gigas ) evaluated by RAPD analysis. Fisheries Research, 83(1): 113–118.CrossRefGoogle Scholar
  47. Sandoval–Castellanos E, Uribe–Alcocer M, Díaz–Jaimes P. 2010. Population genetic structure of the Humboldt squid( Dosidicus gigas d’Orbigny, 1835) inferred by mitochondrial DNA analysis. Journal of Experimental Marine Biology and Ecology, 385(1–2): 73–78.CrossRefGoogle Scholar
  48. Schwing F B, Moor C S, Ralston S, Sakuma K M. 2000. Record coastal upwelling in the California Current in 1999. CalCOFI Rep orts, 41: 148–160.Google Scholar
  49. Taipe A, Yamashiro C, Mariategui L, Rojas P, Roque C. 2001. Distribution and concentrations of jumbo flying squid( Dosidicus gigas ) off the Peruvian coast between 1991 and 1999. Fisheries Research, 54(1): 21–32.CrossRefGoogle Scholar
  50. Uyeno T A, Kier W M. 2007. Electromyography of the buccal musculature of octopus( Octopus bimaculoides ): a test of the function of the muscle articulation in support and movement. Journal of Experimental Biology, 210: 118–128.CrossRefGoogle Scholar
  51. Villegas Bárcenas G, Perales–Raya C, Bartolomé A, Almansa E, Rosas C. 2014. Age validation in Octopus maya(Voss and Solís, 1966) by counting increments in the beak rostrum sagittal sections of known age individuals. Fisheries Research, 152: 93–97.CrossRefGoogle Scholar
  52. Waluda C M, Rodhouse P G. 2006. Remotely sensed mesoscale oceanography of the Central Eastern Pacific and recruitment variability in Dosidicus gigas. Marine Ecology Progress, 310: 25–32.CrossRefGoogle Scholar
  53. Waluda C M, Yamashiro C, Rodhouse P G. 2006. Influence of the ENSO cycle on the light–fishery for Dosidicus gigas in the Peru Current: an analysis of remotely sensed data. Fisheries Research, 79(1–2): 56–63.CrossRefGoogle Scholar
  54. Wolff G A. 1984. Identification and estimation of size from the beaks of 18 species of cephalopods from the Pacific Ocean. NOAA Technical Report NMFS 17, US.Google Scholar
  55. Yu W, Yi Q, Chen X J, Chen Y. 2016. Modelling the effects of climate variability on habitat suitability of jumbo flying squid, Dosidicus gigas, in the Southeast Pacific Ocean off Peru. ICES Journal of Marine Science, 73(2): 239–249.CrossRefGoogle Scholar
  56. Yu W, Yi Q, Chen X J, Chen Y. 2017. Climate–driven latitudinal shift in fishing ground of jumbo flying squid( Dosidicus gigas ) in the Southeast Pacific Ocean off Peru. International Journal of Remote Sensing, 38(12): 3 531–3 550.CrossRefGoogle Scholar
  57. Zeidberg L D, Robinson B H. 2007. Invasive Range Expansion by the Humboldt Squid, Dosidicus gigas, in the Eastern North Pacific. Proceedings of the National Academy of Sciences of the United States of America, 104(31): 12 948–12 950.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Guanyu Hu
    • 1
    • 4
  • Wei Yu
    • 1
    • 5
  • Bai Li
    • 4
  • Dongyan Han
    • 4
    • 6
  • Xinjun Chen
    • 1
    • 2
    • 3
    • 5
    Email author
  • Yong Chen
    • 4
    • 5
  • Jianhua Li
    • 1
    • 2
    • 3
    • 5
  1. 1.College of Marine SciencesShanghai Ocean UniversityShanghaiChina
  2. 2.National Distant-water Fisheries Engineering Research CenterShanghai Ocean UniversityShanghaiChina
  3. 3.Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of EducationShanghai Ocean UniversityShanghaiChina
  4. 4.School of Marine SciencesUniversity of MaineOronoUSA
  5. 5.Collaborative Innovation Center for National Distant-water FisheriesShanghaiChina
  6. 6.College of FisheriesOcean University of ChinaQingdaoChina

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