Abstract
To improve limited knowledge of the predation behaviour of the loliginid species, this study is the first to examine the hunting and feeding behaviour of Loligo vulgaris. Hunting and feeding strategy, as well as body patterning of the squid were described in laboratory experiments during which, two prey types, characterised by different size and mobility (prawn and fish), were offered to the squid. According to the type and distance of the prey, three hunting strategies were observed: to seize larger, farthest and high-mobility prey (fish), squid used tentacles as the main predatory tool (tentacular lunge attack); squid conducted an arm-opening attack to capture smaller and less mobile prey (prawn), but a mixed-strategy using both arms and tentacles was executed when the prawn was further away. Once captured, prawns were consumed alive, while the squid administered a lethal bite to the fish prior to consumption. Fish were always eaten in head-caudal fin direction. Size-feeding strategy differences were also observed. Largest squid ate faster and consumed the entire prey, while smaller squid rejected certain parts of the fish prey. Better prey-handling skills and larger feeding apparatus (e.g., beak) of larger squid (older/experienced individuals) are the likely causes. Finally, a prey-specific body pattern was performed depending on the prey exigency levels.
Similar content being viewed by others
References
Abrams PA (2000) The evolution of predator–prey interactions: theory and evidence. Annu Rev Ecol Syst 31:79–105
Bailey PCE (1986) The feeding behaviour of a sit-and wait-predator, Ranatra dispar (Heteroptera: Nepidae): optimal foraging and feeding dynamics. Oecologia 68:291–297
Barbosa P, Castellanos I (2005) Ecology of predator–prey interactions. Oxford University Press, Nueva York
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bidder AM (1950) The Digestive Mechanism of the European Squids Loligo vulgaris, Loligo forbesii, Alloteuthis media and Alloteutihis subulata. Q J Microsc Sci 3–91:1–43
Borrelli L, Gherardi F, Fiorito G (2006) A catalogue of body patterning in Cephalopoda. Firenze University Press, Firenze
Boycott B (1958) The cuttlefish—Sepia. New Biol 25:98–118
Brown AEX, de Bivort B (2018) Ethology as a physical science. Nat Phys 14:653–657
Cabanellas-Reboredo M, Alós J, Palmer M et al (2012) Movement patterns of the European squid Loligo vulgaris during the inshore spawning season. Mar Ecol Prog Ser 466:133–144
Cabanellas-Reboredo M, Alós J, Palmer M et al (2011) Simulating the indirect handline jigging effects on the European squid Loligo vulgaris in captivity. Fish Res 110:435–440
Cabanellas-Reboredo M, Calvo-Manazza M, Palmer M et al (2014) Using artificial devices for identifying spawning preferences of the European squid: usefulness and limitations. Fish Res 157:70–77
Chabala LD, Morello RS, Busath D et al (1986) Capture, transport, and maintenance of live squid (Loligo pealei) for electrophysiological studies. Pflugers Arch Eur J Physiol 407(1):105–108
Cole PD, Adamo SA (2005) Cuttlefish (Sepia officinalis: Cephalopoda) hunting behavior and associative learning. Anim Cogn 8:27–30
Curio E (1976) Hunting for prey. The ethology of predation. Springer, Berlin Heidelberg, pp 132–210
Dinets V, Brueggen JC, Brueggen JD (2015) Crocodilians use tools for hunting. Ethol Ecol Evol 27:74–78
Duval P, Chichery M-P, Chichery R (1984) Prey capture by the cuttlefish (Sepia officinalis L): an experimental study of two strategies. Behav Process 9:13–21
Fields WG (1965) The structure, development, food relations, reproduction, and life history of the squid Loligo opalescens Berry. Calif Dep Fish Game Fish Bull 131:108
Fiorito G, Affuso A, Basil J et al (2015) Guidelines for the care and welfare of Cephalopods in research—a consensus based on an initiative by CephRes, FELASA and the Boyd Group. Lab Anim 49:1–90
Fiorito G, Gherardi F (1999) Prey-handling behaviour of Octopus vulgaris (Mollusca, Cephalopoda) on Bivalve preys. Behav Process 46:75–88
Fuentes L, Iglesias J, Villanueva R (2014) Cephalopod culture. Springer, The Netherlands
Ghiretti F (1959) Cephalotoxin: the crab-paralysing agent of the posterior salivary glands of cephalopods. Nature 183:1192–1193
Gonçalves JM, Porteiro FM, Cardigos F et al (2009) The Azorean Loligo forbesi (Cephalopoda: Loliginidae) in captivity: transport, handling, maintenance, tagging and survival. Mar Biodivers Rec 2:e120
Grisley MS, Boyle PR, Pierce GJ, Key LN (1999) Factors affecting prey handling in lesser octopus (Eledone cirrhosa) feeding on crabs (Carcinus maenas). J Mar Biol Assoc UK 79:1085–1090
Hanlon R (2007) Cephalopod dynamic camouflage. Curr Biol 17:400–404
Hanlon RT (1990) Maintenance, rearing and culture of teuthoid and sepioid squids. In: Gilbert DL, Adelman WJ, Arnold JM (eds) Squid as experimental animals. Springer, Boston, pp 35–62
Hanlon RT, Maxwell MR, Shashar N et al (1999) An ethogram of body patterning behavior in the biomedically and commercially valuable squid Loligo pealei off Cape Cod, Massachusetts. Biol Bull 197:49–62
Hanlon RT, Messenger JB (2018) Cephalopod behaviour, 2nd edn. Cambridge University Press, Cambridge
Hanlon RT, Messenger JB, Young JZ (1988) Adaptive coloration in young cuttlefish (Sepia officinalis L.): the morphology and development of body patterns and their relation to behaviour. Philos Trans R Soc London B Biol Sci 320:437–487
Hanlon RT, Smale MJ, Sauer WHH (1994) An ethogram of body patterning behavior in the squid Loligo vulgaris reynaudii on spawning grounds in South Africa. Biol Bull 187:363–372
How MJ, Norman MD, Finn J et al (2017) Dynamic skin patterns in Cephalopods. Front Physiol 8:393
Hunt JC, Zeidberg LD, Hamner WM, Robison BH (2000) The behaviour of Loligo opalescens (Mollusca: Cephalopoda) as observed by a remotely operated vehicle (ROV). J Mar Biol Assoc UK 80:873–883
Hurley AC (1976) Feeding behavior, food consumption, growth, and respiration of the squid Loligo opalescens raised in the laboratory. Fish Bull 74(1)
Jastrebsky RA, Bartol IK, Krueger PS (2017) Turning performance of brief squid Lolliguncula brevis during attacks on shrimp and fish. J Exp Biol 220:908–919
Kaspari M (1991) Prey preparation as a way that grasshopper sparrows (Ammodramus savannarum) increase the nutrient concentration of their prey. Behav Ecol 2:234–241
Kier WM (1982) The functional morphology of the musculature of squid (Loliginidae) arms and tentacles. J Morphol 172:179–192
Koueta N, Boucaud-Camou E (1989) Comparative study of the secretion of the posterior salivary gland of decapod cephalopods. II. Processus of secretion in the squids Loligo vulgaris L. and Loligo forbesi Steenstrup
LaRoe ET (1971) The culture and maintenance of the loliginid squids Sepioteuthis sepioidea and Doryteuthis plei. Mar Biol 9:9–25
Lloyd FE (1942) The carnivorous plants. Chronica Botanica Company, Waltham, Massachusetts, USA
Mather JA, Kuba MJ (2013) The cephalopod specialties: complex nervous system, learning, and cognition. Can J Zool 91:431–449
Mather JA, Mather DL (2004) Apparent movement in a visual display: the ‘passing cloud’ of Octopus cyanea (Mollusca: Cephalopoda). J Zool 263:89–94
Messenger JB (1968) The visual attack of the cuttlefish, sepia officinalis. Anim Behav 16(342):357
Messenger JB, Nixon M, Ryan KP (1985) Magnesium chloride as an anaesthetic for cephalopods. Comp Biochem Physiol C 82:203–205
Moltschaniwskyj NA, Hall K, Lipinski MR et al (2007) Ethical and welfare considerations when using cephalopods as experimental animals. In: Reviews in fish biology and fisheries. pp 455–476
Nicol S, O’dor RK (1985) Predatory behaviour of squid (Illex illecebrosus) feeding on surface swarms of euphausiids. Can J Zool 63:15–17
O’Dor RK, Hoar JA, Webber DM et al (1994) Squid (Loligo forbesi) performance and metabolic rates in nature. Mar Freshw Behav Physiol 25:163–177
Packard A, Hochberg FG (1977) Skin patterning in Octopus and other genera. Symp Zool Soc London 38:191–231
Pierce GJ, Allcock L, Bruno I et al (2010) Cephalopod biology and fisheries in Europe. ICES Coop Res Rep 303:175
Pierce GJ, Boyle PR, Hastie LC, Santos MB (1994) Diets of squid Loligo forbesi and Loligo vulgaris in the northeast Atlantic. Fish Res 21:149–163
Plaut I (2001) Critical swimming speed: its ecological relevance. Comp Biochem Physiol A Mol Integr Physiol 131:41–50
Porteiro FM, Martins HR, Hanlon RT (1990) Some observations on the behavior of adult squids, Loligo forbesi, in captivity. J Mar Biol Assoc UK 70:459–472
Postuma FA, Gasalla MA (2015) Ethogram analysis reveals new body patterning behavior of the tropical arrow squid Doryteuthis plei off the São Paulo coast. Biol Bull 229:143–159
Rocha F, Castro B, Gil M, Guerra Á (1994) The diets of Loligo vulgaris and L. forbesi (Cephalopoda: Loliginidae) in northwestern Spanish Atlantic waters. Sarsia 79:119–126
Rocha F, Guerra A (1999) Age and growth of two sympatric squid Loligo vulgaris and Loligo forbesi, in Galician waters (north-west Spain). J Mar Biol Assoc UK 79:697–707
Rocha F, Guerra Á, González ÁF (2001) A review of reproductive strategies in cephalopods. Biol Rev 76:291–304
Schaeffel F, Murphy CJ, Howland HC (1999) Accommodation in the cuttlefish (Sepia officinalis). J Exp Biol 202:3127–3134
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Syst 2:369–404
Sherr EB, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek 81:293–308
Smale M, Sauer W, Roberts M (2001) Behavioural interactions of predators and spawning chokka squid off South Africa: towards quantification. Mar Biol 139:1095–1105
Smith TG, Siniff DB, Reichle R, Stone S (1981) Coordinated behavior of killer whales, Orcinus orca, hunting a crabeater seal, Lobodon carcinophagus. Can J Zool 59:1185–1189
Staudinger MD, Hanlon RT, Juanes F (2011) Primary and secondary defences of squid to cruising and ambush fish predators: variable tactics and their survival value. Anim Behav 81:585–594
Stevens A (2010) Predation, herbivory, and parasitism. Nat Educ Knowl 3:36
Stewart WJ, Bartol IK, Krueger PS (2010) Hydrodynamic fin function of brief squid, Lolliguncula brevis. J Exp Biol 213:2009–2024
Sugimoto C, Ikeda Y (2013) Comparison of the ontogeny of hunting behavior in pharaoh cuttlefish (Sepia pharaonis) and oval squid (Sepioteuthis lessoniana). Biol Bull 225:50–59
Sykes AV, Gestal C (2014) Welfare and diseases under culture conditions. In: Iglesias J, Fuentes L, Villanueva R (eds) Cephalopod culture. Springer, Netherlands, pp 97–112
Vailati A, Zinnato L, Cerbino R (2012) How archer fish achieve a powerful impact: hydrodynamic instability of a pulsed jet in toxotes jaculatrix. PLoS ONE 7:e47867
Valls M, Cabanellas-Reboredo M, Uranga I, Quetglas A (2015) Feeding ecology of two squid species from the western Mediterranean. Mar Ecol Prog Ser 531:207–219
Verrill AE (1882) Report on the cephalopods of the northeastern coast of America. Govt. print. off, Washington, extracted from the annual report of the Commissioner of Fish and Fisheries (1879)
Villanueva R, Perricone V, Fiorito G (2017) Cephalopods as predators: a short journey among behavioral flexibilities, adaptions, and feeding habits. Front Physiol 8:598
Wallace IC, O’Dor RK (1980) Sequential observations on the digestive process in the squid, Illex illecebrosus. NAFO Sci Counc Stud 1:65–69
Willard DE (1977) Constricting methods of snakes. Copeia 1977:379–382
Wolff GA (1984) Identification and estimation of size from the beaks of 18 species of cephalopods from the Pacific Ocean. NOAA/National Marine Fisheries Service, (NOAA Technical Report NMFS, 17)
Yu X, Zhang X, Duan Y et al (2010) Effects of temperature, salinity, body length, and starvation on the critical swimming speed of whiteleg shrimp, Litopenaeus vannamei. Comp Biochem Physiol Mol Integr Physiol 157:392–397
Acknowledgments
We especially thank the logistic support of Palma Aquarium, as well as the cooperation of all staff from Palma Aquarium (especially, R. Grädel and C. Keller) that provided us his experience in the captivity experiments. Moreover, we thanks to D. Villegas, S. Sardu, J. Maimó, M. Carrió and R. Padillo for their collaboration in collecting the squid. Jorge Hernández-Urcera is supported by a Juan de la Cierva’s post-doc research grants (#FJCI-2016-30990) funded by the Spanish Ministry of Science, Innovation and Universities. Miguel Cabanellas-Reboredo is supported by a postdoctoral contract co-funded by the Regional Government of the Balearic Islands and the European Social Fund 2014–2020.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Carreño Castilla, A., Hernández-Urcera, J., Gouraguine, A. et al. Predation behaviour of the European squid Loligo vulgaris. J Ethol 38, 311–322 (2020). https://doi.org/10.1007/s10164-020-00652-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10164-020-00652-4