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HU Guanyu, YU Wei, LI Bai, HAN Dongyan, CHEN Xinjun, CHEN Yong, LI Jianhua. Impacts of El Niño on the somatic condition of Humboldt squid based on the beak morphology[J]. HaiyangYuHuZhao, 2019, 37(4): 1440-1448

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

HU Guanyu1,4, YU Wei1,5, LI Bai4, HAN Dongyan4,6, CHEN Xinjun1,2,3,5, CHEN Yong4,5, LI Jianhua1,2,3,5
1 College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China;
2 National Distant-water Fisheries Engineering Research Center, Shanghai Ocean University, Shanghai 201306, China;
3 Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, Shanghai Ocean University, Shanghai 201306, China;
4 School of Marine Sciences, University of Maine, Orono, Maine 04469, USA;
5 Collaborative Innovation Center for National Distant-water Fisheries, Shanghai 201306, China;
6 College of Fisheries, Ocean University of China, Qingdao 266003, China
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 mantle length (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.
Key words:    El Niño event|Dosidicus gigas|somatic condition|abundance|beak morphology   
Received: 2018-06-16   Revised: 2018-07-22
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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.
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.
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.
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 1991-1992 El Niño. Deep Sea Research Part Ⅱ:Topical Studies in Oceanography, 43(4-6):933-969.
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.
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.
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 (Ommastrephes bartramii)in the Northwest Pacific Ocean. Fishery Bulletin, 108(1):1-14.
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.
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,
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.
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.
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.
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.
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.
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.
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.
Froese R. 2006. Cube law, condition factor and weight-length relationships:history, meta-analysis and recommendations.Journal of Applied Ichthyology, 22(4):241-253.
García V H. 2003. Growth and pigmentation process of the beaks of Todaropsis eblanae (Cephalopoda:ommastrephidae). Berliner Paläobiologische Abhandlungen, Berlin, 3:131-140.
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.
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.
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.
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.
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)
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.
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)
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.
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.
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.
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.
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.
Lipiński M R, Underhill L G. 1995. Sexual maturation in squid:quantum or continuum? South African Journal of Marine Science, 15(1):207-223.
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.
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.
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.
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.
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.
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 Reports, 49:256-262.
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.
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.
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.
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.
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,
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.
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.
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.
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.
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.
Schwing F B, Moor C S, Ralston S, Sakuma K M. 2000.Record coastal upwelling in the California Current in 1999. CalCOFI Reports, 41:148-160.
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.
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.
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.
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.
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.
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.
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.
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.
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.