Abstract
This paper concisely summarizes major aspects of cephalopod biology, behavior, and ecology providing a backdrop against which neurobiology of these animals can be interpreted. Reproduction, camouflage, motor control, memory, learning, and behavioral ecology are introduced, and thorough literature reviews of these subjects are cited for further reading. The aim of this paper is to provide a general introduction to cephalopods for use by workers currently focused on other model systems.
This is a preview of subscription content, access via your institution.
References
Aitken JP, O’Dor RK, Jackson GD (2005) The secret life of the giant Australian cuttlefish Sepia apama (Cephalopoda): behaviour and energetics in nature revealed through radio acoustic positioning and telemetry (RAPT). J Exp Mar Biol Ecol 320:77–91
Allen JJ, Mäthger LM, Barbosa A, Buresch KC, Sogin E, Schwartc J et al (2010) Cuttlefish dynamic camouflage: responses to substrate choice and integration of multiple visual cues. Proc Royal Soc B 277:1031–1039
Alves C, Boal JG, Dickel L (2008) Short-distance navigation in cephalopods: a review and synthesis. Cogn Process. doi:10.1007/s10339-007-0192-9
Anderson RC, Wood JB, Byrne RA (2002) Octopus senescence: the beginning of the end. J Appl Anim Welf Sci 5:275–283
Bauer B (1998) Sperm competition in Molluscs. In: Birkhead TR, Moller AP (eds) Sperm competition and sexual selection. Academic Press Ltd, San Diego, pp 255–305
Bazzino B, Gilly WF, Markaida U, Salinas-Zavala CA, Ramos-Castillejos J (2010) Horizontal movements, vertical-habitat utilization and diet of the jumbo squid (Dosidicus gigas) in the Pacific Ocean off Baja California Sur, Mexico. Prog Oceanogr 86:59–71
Bellanger C, Dauphin F, Chichery MP, Chichery R (2003) Changes in cholinergic enzyme activities in the cuttlefish brain during memory formation. Physiol Behav 79:749–756
Biederman GB, Davey VA (1993) Social learning in invertebrates. Science 259:1627–1628
Boal JG (2006) Social recognition: a top down view of cephalopod behaviour. Vie et Milieu 56:69–79
Boal JG, Gonzalez SA (1998) The social behavior of individual oval squids (Cephalopoda, Teuthoidea, Loliginidae, Sepioteuthis lessoniana) within a captive school. Ethology 104:161–178
Boal JG, Wittenberg KM, Hanlon RT (2000) Observational learning does not explain improvement in predation tactics by cuttlefish (Mollusca: Cephalopoda). Behav Process 52:141–153
Boletsky SV (2003) A lower limit to adult size in coleoid cephalopods. Berliner Palaobiologie Abhandlung 3:19–28
Boletzky SV (1994) Embryonic development of cephalopods at low temperatures. Antarct Sci 6:139–142
Brady B (2008) Long-term changes in biological characteristics and fishery of Loligo opalescens. Masters thesis, San Jose State University, USA
Budelmann BU (1995) The cephalopod nervous system: what evolution has made of the molluscan design. In: Breidbach O, Kutsuch W (eds) The nervous system of invertebrates: an evolutionary and comparative approach. Birkhauser Verlag, Basel, pp 115–138
Bullock TH, Budelmann BU (1991) Sensory evoked potentials in unanesthetized unrestrained cuttlefish: a new preparation for brain physiology in cephalopods. J Comp Physiol Ser A 168:141–150
Buresch KM, Hanlon RT, Maxwell MR, Ring S (2001) Microsatellite DNA markers indicate a high frequency of multiple paternity within individual field-collected egg capsules of the squid Loligo pealeii. Mar Ecol Prog Ser 210:161–165
Bush SL, Hoving HJT, Huffard CL, Robison BH, Zeidberg LD (2012) Brooding and sperm storage by the deep-sea squid Bathyteuthis berryi (Cephalopoda: Decapodiformes). J Mar Biol Assoc UK. doi:10.1017/S0025315411002165
Chen DS, Van Dykhuizen G, Hodge J, Gilly WF (1996) Ontogeny of copepod predation in juvenile squid (Loligo opalescens). Biol Bull 190:69–81
Cheng MW, Caldwell RL (2000) Sex identification and mating in the blue-ringed octopus, Hapalochlaena lunulata. Anim Behav 60:27–33
Cigliano JA (1993) Dominance and den use in Octopus bimaculoides. Anim Behav 46:677–684
Cigliano JA (1995) Assessment of the mating history of female pygmy octopuses and a possible sperm competition mechanism. Anim Behav 49:849–851
Corner BD, Moore HT (1980) Field observations on the reproductive behavior of Sepia latimanus. Micronesica 16:235–260
Crook RJ, Basil J (2008a) A biphasic memory curve in the chambered nautilus, Nautilus pompilius L. (Cephalopoda: Nautiloidea). J Exp Biol 211:1992–1998
Crook RJ, Basil J (2008b) A role for nautilus in studies of the evolution of brain and behaviour. Commun Integr Biol 1:61–62
Crook RJ, Walters ET (2011) Nociceptive behavior and physiology in molluscs: animal welfare implications. Inst Lab Anim Res J 52:185–195
Crook RJ, Hanlon RT, Basil JA (2009) Memory of visual and topographical features suggests spatial learning in the ancient cephalopod, nautilus (Nautilus pompilius L.). J Comp Psychol 3:264–274
Cummins SF, Boal JG, Buresch KC, Kuanpradit C, Sobhon P, Holm JB, Degnan BM, Nagle GT, Hanlon RT (2011) Extreme aggression in male squid Induced by a β-MSP-like pheromone. Curr Biol 21:322–327
Di Cosmo A, Di Cristo C (1998) Neuropeptidergic control of the optic gland of Octopus vulgaris: FMRF-amide and GnRH immunoreactivity. J Comp Neurol 398:1–12
Dodson JJ (1998) The nature and role of learning in the orientation and migratory behavior of fishes. Environ Biol Fishes 23:161–182
Fiorito G, Chichery R (1995) Lesions of the vertical lobe impair visual discrimination learning by observation in Octopus vulgaris. Neurosci Lett 192:117–120
Fiorito G, Scotto P (1992) Observational learning in Octopus vulgaris. Science 256:545–547
Forsythe JW (2004) Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Mar Freshw Res 55:331–339
Frank MG, Waldrop RH, Dumoulin M, Aton S, Boal JG (2012) A preliminary analysis of sleep-like states in the cuttlefish Sepia officinalis. PLoS ONE. doi:10.1371/journal.pone.0038125
Grant P, Zheng Y, Pant HC (2006) Squid (Loligo pealei) giant fiber system: a model for studying neurodegeneration and dementia? Biol Bull 210:318–333
Grasso FW, Basil JA (2009) The evolution of flexible behavioral repertoires in cephalopods molluscs. Brain Behav Evol 74:231–245
Gutfreund Y, Flash T, Fiorito G, Hochner B (1998) Patterns of arm muscle activation involved in octopus reaching movements. J Neurosci 18:5976–5987
Hall KC, Hanlon RT (2002) Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Mar Biol 140:533–545
Hanlon RT (1988) Behavioral and body patterning characters useful in taxonomy and field identification of Cephalopods. Malacologia 29:247–266
Hanlon RT (2007) Cephalopod dynamic camouflage. Curr Biol 17:400–404
Hanlon RT, Forsythe J (2008) Sexual cannibalism by Octopus cyanea on a Pacific coral reef. Mar Freshw Behav Physiol 41:19–28
Hanlon RT, Hixon RF (1980) Body patterning and field observations of Octopus burryi. Bull Mar Sci 30:749–755
Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, Cambridge
Hanlon RT, Forsythe JW, Joneschild DE (1999) Crypsis, conspicuousness, mimicry and polyphenism as antipredator defenses of foraging octopuses on Indo-Pacific coral reefs, with a method of quantifying crypsis from video tapes. Biol J Linn Soc 66:1–22
Hanlon RT, Smale MJ, Sauer WHH (2002) The mating system of the squid Loligo vulgaris reynaudii (Cephalopoda, Mollusca) off South Africa: fighting, guarding, sneaking, mating and egg laying behavior. Bull Mar Sci 71:331–345
Hanlon RT, Chiao C–C, Mäthger LM, Buresch KC, Barbosa A, Allen JJ et al (2011) Rapid adaptive camouflage in cephalopods. In: Stevens M, Merilaita S (eds) Animal camouflage: mechanisms and functions. Cambridge University Press, Cambridge, pp 145–163
Heithaus MR, Frid A, Wirsing AJ, Worm B (2008) Predicting ecological consequences of marine top predator declines. Trends Ecol Evol 23:202–210
Hochner B (2008) Octopuses. Curr Biol 18:R897–R898
Hochner B (2012) An embodied view of octopus neurobiology. Curr Biol 22:R887–R892
Hochner B, Shomrat T, Fiorito G (2006) The octopus: a model for a comparative analysis of the evolution and memory mechanisms. Biol Bull 210:308–317
Houck BA (1982) Temporal spacing in the activity patterns of 3 Hawaiian USA shallow water octopods. Nautilus 96:152–156
Hoving HJT, Roeleveld MAC, Lipinski MR, Videler JJ (2006) Nidamental glands in males of the oceanic squid Ancistrocheirus lesueurii (Cephalopoda: Ancistrocheiridae)—sex change or intersexuality? J Zool 269:341–348
Hoving HJT, Bush SL, Robison BH (2011) A shot in the dark: same-sex sexual behaviour in a deep-sea squid. Biol Lett. doi:10.1098/rsbl.2011.0680
Huffard CL (2006) Locomotion by Abdopus aculeatus: walking the line between primary and secondary defenses. J Exp Biol 209:3697–3707
Huffard CL (2007) Ethogram of Abdopus aculeatus (d’Orbigny, 1834) (Cephalopoda: Octopodidae): can behavioral characters inform octopodid taxonomy and systematics? J Molluscan Stud 73:185–193
Huffard CL, Godfrey-Smith P (2010) Field observations of mating in Octopus tetricus Gould 1852 and Amphioctopus marginatus (Taki, 1964). Molluscan Res 30:81–86
Huffard CL, Boneka F, Full RJ (2005) Underwater bipedal locomotion by octopuses in disguise. Science 307:1927
Huffard CL, Caldwell RL, Boneka F (2008) Mating behavior of Abdopus aculeatus (d’Orbigny 1834) (Cephalopoda: Octopodidae) in the wild. Mar Biol 154:353–362
Huffard CL, Caldwell RL, Boneka F (2010) Male-male and male-female aggression may influence mating associations in wild octopuses (Abdopus aculeatus). J Comp Psychol 124:38–46
Hvorecny LM, Grudowski JL, Blakeslee CJ, Simmons TL, Roy PR, Brooks JA et al (2007) Octopuses (Octopus bimaculoides) and cuttlefishes (Sepia pharaonis, S. officinalis) can conditionally discriminate. Anim Cogn 10:449–459
Hylleberg J, Nateewathana A (1991) Morphology, internal anatomy, and biometrics of the cephalopod Idiosepius biserialis Voss, 1962. A new record for the Andaman Sea. Phuket Mar Biol Cent Res Bull 56:1–9
Ibáñez CM, Keyl F (2010) Cannibalism in cephalopods. Rev Fish Biol Fish 20:123–136
Itami K, Izawa Y, Maeda S, Nakai K (1963) Notes on the laboratory culture of octopus larvae. Bull Jpn Soc Sci Fish 29:514–520
Itawa Y, Munehara H, Sakurai Y (2005) Dependence of paternity rates on alternative reproductive behaviors in the squid Loligo bleekeri. Mar Ecol Prog Ser 298:219–228
Jozet-Alves C, Mode’ran J, Dickel L (2008) Sex differences in spatial cognition in an invertebrate: the cuttlefish. Proc Royal Soc B 275:2049–2054
Kanda A, Takahasi T, Satake H, Minakata H (2006) Molecular and functional characterization of a novel gonadotropin releasing-hormone receptor isolated from the common octopus (Octopus vulgaris). Biochem J 395:125–135
Kier WM, Smith KK (1985) Tongues, tentacles and trunks-the biomechanics of movement in muscular-hydrostats. Zool J Linn Soc 83:307–324
Kier WM, Stella MP (2007) The arrangement and function of octopus arm musculature and connective tissue. J Morphol 268:831–843
Leite TS, Haimovici M, Mather J, Lins Oliveira JE (2009) Habitat, distribution, and abundance of the commercial octopus (Octopus insularis) in a tropical oceanic island, Brazil: information for management of an artisanal fishery inside a marine protected area. Fish Res 98:85–91
Lutz RA, Voight JR (1994) Close encounter in the deep. Nature 371:563
Mangold K (1987) Reproduction. In: Boyle PR (ed) Cephalopod life cycles: volume II comparative reviews. Academic Press, London, pp 157–200
Marshall NJ, Messenger JB (1996) Colour-blind camouflage. Nature 382:408–409
Mather JA (1991) Navigation by spatial memory and use of visual landmarks in octopuses. J Comp Physiol Ser A 168:491–497
Mather JA, Anderson RC (2007) Ethics and invertebrates: a cephalopod perspective. Dis Aquat Org Special Issue 75:119–129
Mäthger LM, Barbosa A, Miner S, Hanlon RT (2006) Color blindness and contrast perception in cuttlefish (Sepia officinalis) determined by a visual sensorimotor assay. Vis Res 46:1746–1753
Messenger JB (2001) Cephalopod chromatophores: neurobiology and natural history. Biol Rev 76:473–528
Nabhitabhata J, Suwanamala J (2008) Reproductive behaviour and cross-mating of two closely related pygmy squids Idiosepius biserialis and Idiosepius thailandicus (Cephalopoda: Idiosepiidae). J Mar Biol Assoc UK 88:987–993
Nishioka RS, Yasumasu I, Packard A, Bern HA, Young JZ (1966) Nature of vesicles associated with nervous system of cephalopods. Zeitschrift für Zellforschung 75:301–316
Norman MD (2000) Cephalopods: a world guide. ConchBooks, Hackenheim
Norman MD, Hochberg FG, Boucher R (2005) A revision of the deep-water octopus genus Scaeurgus (Cephalopoda: Octopodidae) with description of three new species from the Southwest Pacific Ocean. J Molluscan Stud 71:319–337
O’Dor RK, Macalaster EG (1983) Bathypolypus arcticus. In: Boyle PR (ed) Cephalopod life cycles: volume I species accounts. Academic Press, London, pp 401–410
Packard A (1961) Sucker display of Octopus. Nature 190:736–737
Packard A (1972) Cephalopods and fish: the limits of convergence. Biol Rev Camb Philos Soc (Lond) 47:241–307
Packard A, Hochberg FG (1977) Skin patterning in Octopus and other genera. Symp Zool Soc Lond 38:191–231
Packard A, Sanders GD (1971) Body patterns of Octopus vulgaris and maturation of the response to disturbance. Anim Behav 19:780–790
Pickford GE (1964) Octopus dofleini (Wülker). Bull Bingham Oceanogr Collect Yale Univ 19:1–54
Pronk R, Wilson DR, Harcourt R (2010) Video playback demonstrates episodic personality in the gloomy octopus. J Exp Biol 213:1035–1041
Richard A, Lemaire J (1975) Determination et differenciation sexualles chez la Seiche, Sepia officinalis L. (Mollusque: Cephalopode). C R Acad Sci Paris D 277:2185–2188
Robson GC (1929) A monograph of the recent Cephalopoda based on the collections in the British Museum (Natural History). Part I. Octopodinae. British Museum Natural History, London
Rocha F, Guerra A, Gonzalez AF (2001) A review of reproductive strategies in cephalopods. Biol Rev 76:291–304
Sauer WHH, Smale MJ, Lipinski MR (1992) The location of spawning grounds, spawning and schooling behaviour of the squid Loligo vulgaris reynaudii (Cephalopoda: Myopsida) of the Eastern Cape Coast, South Africa. Mar Biol 114:97–107
Scheel D, Bisson L (2012) Movement patterns of giant Pacific octopuses, Enteroctopus dofleini (Wülker, 1910). J Exp Mar Biol Ecol 416–417:21–31
Seibel BA, Robison BH, Haddock SHD (2005) Post-spawning egg care by a squid. Nature 438:929
Semmens JM, Pecl GT, Villanueva R, Jouffre D, Sobrino I, Wood JB et al (2004) Understanding octopus growth: patterns, variability and physiology. Mar Freshw Res 55:367–377
Semmens JM, Pecl GT, Gillanders BM, Waluda CM, Shea E, Jouffre D et al (2007) Approaches to resolving cephalopod movement and migration patterns. Rev Fish Biol Fish 17:401–423
Shigeno S, Kidokoro H, Tsuchiya K, Segawa S, Yamamoto M (2001) Development of the brain in the Oegopsid Squid, Todarodes pacificus: an atlas up to the hatching stage. Zoolog Sci 18:527–541
Shomrat T, Zarrella I, Fiorito G, Hochner B (2008) The octopus vertical lobe modulates short-term learning rate and uses LTP to acquire long-term memory. Curr Biol 18:337–342
Sinn DL, Moltschaniwskyj NA (2005) Personality traits in dumpling squid (Euprymna tasmanica): context-specific traits and their correlation with biological characteristics. J Comp Psychol 119:99
Sinn DL, Perrin NA, Mather JA, Anderson RC (2001) Early temperamental traits in an octopus (Octopus bimaculoides). J Comp Psychol 115:351–364
Squires ZE, Wong BBM, Norman MD, Stuart-Fox D (2012) Multiple fitness benefits of polyandry in a cephalopod. PLoS ONE 7:e37074. doi:10.1371/journal.pone.0037074
Staaf DJ, Camarillo-Coop S, Haddock SHD, Nyack AC, Payne J, Salinas-Zavala CA et al (2008) Natural egg mass deposition by the Humboldt squid (Dosidicus gigas) in the Gulf of California and characteristics of hatchlings and paralarvae. J Mar Biol Assoc UK 88:759–770
Stewart JS, Field JC, Markaida U, William FG (2012) Behavioral ecology of jumbo squid (Dosidicus gigas) in relation to oxygen minimum zones. Deep Sea Res Part II Top Stud Oceanogr. doi:10.1016/j.dsr2.2012.06.005
Sumbre G, Gutfreund Y, Fiorito G, Flash T, Hochner B (2001) Control of octopus arm extension by a peripheral motor program. Science 293:1845–1848
Tricarico E, Borrelli L, Gherardi F, Fiorito G (2011) I know my neighbour: individual recognition in Octopus vulgaris. PLoS ONE 6:e18710
Van Heukelem W (1973) Growth and life-span of Octopus cyanea (Mollusca: Cephalopoda). J Zool 169:299–315
Vecchione M (1991) Observations on the paralarval ecology of a euryhaline squid, Lolliguncula brevis (Cephalopoda, Loliginidae). Fish Bull 89:515–521
Villanueva RA, Norman MD (2008) Biology of the planktonic stages of benthic octopuses. Oceanogr Mar Biol Annu Rev 46:105–202
Voight JR (1991) Enlarged suckers as an indicator of male maturity in Octopus. Bull Mar Sci 49:98–106
Voight JR (2005) Hydrothermal vent octopuses of Vulcanoctopus hydrothermalis, feed on bathypelagic amphipods of Halice hesmonectes. J Mar Biol Assoc UK 85:985–988
Voight JR (2009) Differences in spermatophore availability among octopodid species (Cephalopoda: Octopoda). Malacologia 51:143–153
Voight JR, Drazen JC (2004) Hatchlings of the deep-sea octopus Graneledone boreopacifica are the largest and most advanced known. J Molluscan Stud 70:406–408
Voight JR, Feldheim KA (2009) Microsatellite inheritance and multiple paternity in the deep-sea octopus Graneledone boreopacifica (Mollusca: Cephalopoda). Invertebr Biol 128:26–30
Wada T, Takegaki T, Mori T, Natsukari Y (2005) Sperm displacement behavior of the cuttlefish Sepia esculenta (Cephalopoda: Sepiidae). J Ethol 23:85–92
Warner RR (1988) Traditionality of mating-site preference in a coral reef fish. Nature 335:719–721
Wells MJ, Wells J (1972) Sexual displays and mating of Octopus vulgaris and Octopus cyanea and attempts to alter performance by manipulating the glandular condition of the animals. Anim Behav 20:29–308
Williamson R, Chrachri A (2004) Cephalopod neural networks. Neurosignals 13:87
Woodhams PL, Messenger JB (1974) A note on the ultrastructure of the octopus olfactory organ. Cell Tissue Res 152:253–258
Young JZ (1963) The number and sizes of nerve cells in Octopus. Proc Zool Soc Lond 140:229–254
Young JZ (1964) Paired centres for the control of attack by Octopus. Proc R Soc Lond B 159:565–588
Young JZ (1971) The anatomy of the nervous system of Octopus vulgaris. Clarendon Press, Oxford
Zullo L, Hochner B (2011) A new perspective on the organization of an invertebrate brain. Commun Integr Biol 4:26–29
Zullo L, Sumber G, Agnisola S, Flash T, Hochner B (2009) Nonsomatotopic organization of the higher motor centers in Octopus. Curr Biol 19:1632–1636
Zylinski S, Osorio D (2011) What can camouflage tell us about non-human visual perception? A case study of multiple cue use in the cuttlefish. In: Stevens M, Merilaita S (eds) Animal camouflage: mechanisms and function. Cambridge University Press, Cambridge, pp 164–185
Zylinski S, How MJ, Osorio D, Hanlon RT, Marshall NJ (2011) To be seen or to hide: visual characteristics of body patterns for camouflage and communication in the Australian giant cuttlefish Sepia apama. Am Nat 177:681–690
Zylinski S, Darmaillacq A-S, Shashar N (2012) Visual interpolation for contour completion by the European cuttlefish (Sepia officinalis) and its use in dynamic camouflage. Proc Royal Soc B 1471–2954. doi:10.1098/rspb.2012.0026
Acknowledgments
I thank Graziano Fiorito for the invitation to write this paper, and three anonymous reviewers for their constructive comments.
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Huffard, C.L. Cephalopod neurobiology: an introduction for biologists working in other model systems. Invert Neurosci 13, 11–18 (2013). https://doi.org/10.1007/s10158-013-0147-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10158-013-0147-z