Abstract
Octopuses integrate visual, chemical and tactile sensory information while foraging and feeding in complex marine habitats. The respective roles of these modes are of interest ecologically, neurobiologically, and for development of engineered soft robotic arms. While vision guides their foraging path, benthic octopuses primarily search “blindly” with their arms to find visually hidden prey amidst rocks, crevices and coral heads. Each octopus arm is lined with hundreds of suckers that possess a combination of chemo- and mechanoreceptors to distinguish prey. Contact chemoreception has been demonstrated in lab tests, but mechanotactile sensing is less well characterized. We designed a non-invasive live animal behavioral assay that isolated mechanosensory capabilities of Octopus bimaculoides arms and suckers to discriminate among five resin 3D-printed prey and non-prey shapes (all with identical chemical signatures). Each shape was introduced inside a rock dome and was only accessible to the octopus’ arms. Octopuses’ responses were variable. Young octopuses discriminated the crab prey shape from the control, whereas older octopuses did not. These experiments suggest that mechanotactile sensing of 3D shapes may aid in prey discrimination; however, (i) chemo-tactile information may be prioritized over mechanotactile information in prey discrimination, and (ii) mechanosensory capability may decline with age.
Similar content being viewed by others
Data availability
The datasets used for the current study are available from the corresponding author upon reasonable request.
References
Al-Soudy AS, Maselli V, Galdiero S, Kuba MJ, Polese G, CosmoA Di (2021) Identification and characterization of a rhodopsin kinase gene in the suckers of Octopus vulgaris: looking around using arms? Biology 10:936. https://doi.org/10.3390/biology10090936
Altman JS (1971) Control of accept and reject reflexes in the octopus. Nature 229:204–206. https://doi.org/10.1038/229204a0
Ambrose RF, Nelson BV (1983) Predation by Octopus vulgaris in the Mediterranean. Mar Ecol 4:251–261. https://doi.org/10.1111/j.1439-0485.1983.tb00299.x
Borrelli L, Gherardi F, Fiorito G (2006) A catalog of body patterning in Cephalopoda. Firenze University Press, Firenze
Boycott BB, Young JZ (1956) The subpedunculate body and nerve and other organs associated with the optic tract of cephalopods. Bertil Hanström. Zoological papers in honour of his sixty-fifth birthday. Zoological Institute, Lund, pp 76–105
Boyle PR (1986) Responses to water-borne chemicals by the octopus Eledone cirrhosa (Lamarck, 1798). J Exp Mar Bio Ecol 104:23–30. https://doi.org/10.1016/0022-0981(86)90095-X
Buresch KC, Sklar K, Chen JY, Madden SR, Mongil AS, Wise GV, Boal JG, Hanlon RT (2022) Contact chemoreception in multi-modal sensing of prey by Octopus. J Comp Physiol A 208:435–442. https://doi.org/10.1007/s00359-022-01549-y
Byrne RA, Kuba MJ, Meisel DV, Griebel U, Mather JA (2006) Octopus arm choice is strongly influenced by eye use. Behav Brain Res 172:195–201. https://doi.org/10.1016/j.bbr.2006.04.026
Forsythe JW, Hanlon RT (1988) Effect of temperature on laboratory growth, reproduction and life span of Octopus bimaculoides. Mar Biol 98:369–379. https://doi.org/10.1007/BF00391113
Forsythe JW, Hanlon RT (1997) Foraging and associated behavior by Octopus cyanea Gray, 1849 on a coral atoll, French Polynesia. J Exp Mar Biol Ecol 209:15–31. https://doi.org/10.1016/S0022-0981(96)00057-3
Grasso FW (2008) Octopus sucker-arm coordination in grasping and manipulation. Am Malacol Bull 24:13–23. https://doi.org/10.4003/0740-2783-24.1.13
Graziadei P (1962) Receptors in suckers of Octopus. Nature 195:57–59. https://doi.org/10.1038/195057a0
Graziadei P (1964) Electron microscopy of some primary receptors in the sucker of Octopus vulgaris. Z Für Zellforsch Mik Ana 64:510–522. https://doi.org/10.1007/BF010
Graziadei PP, Gagne HT (1976) Sensory innervation in the rim of the octopus sucker. J Morphol 150:639–679. https://doi.org/10.1002/jmor.1051500304
Gutnick T, Byrne RA, Hochner B, Kuba M (2011) Octopus vulgaris uses visual information to determine the location of its arm. Curr Biol 21:460–462. https://doi.org/10.1016/j.cub.2011.01.052
Gutnick T, Zullo L, Hochner B, Kuba MJ (2020) Use of peripheral sensory information for central nervous control of arm movement by Octopus vulgaris. Curr Biol 30:4322–4327. https://doi.org/10.1016/j.cub.2020.08.037
Hanassy S, Botvinnik A, Flash T, Hochner B (2015) Stereotypical reaching movements of the octopus invlove both bend propagation and arm elongation. Bioinspir Biomim 10:035001. https://doi.org/10.1088/1748-3190/10/3/0350001
Hanlon RT, Messenger JB (2018) Cephalopod behaviour, 2nd edn. Cambridge University Press, Cambridge
Holst MM, Hauver CM, Stein RS, Milano BL, Levine LH, Zink AG, Watters JV, Crook RJ (2022) Behavioral changes in senescent giant Pacific octopus (Enteroctopus dofleini) are associated with peripheral neural degeneration and loss of epithelial tissue. Comp Biochem Physiol A 271:111263. https://doi.org/10.1016/j.cbpa.2022.111263
Ifere NO, Shidara H, Sato N, Ogawa H (2022) Spatial perception mediated by insect antenna mechanosensory system. J Exp Biol 225:jeb24376. https://doi.org/10.1242/jeb.243276
Kawashima S, Ikeda Y (2021) Evaluation of visual and tactile perception by plain-body Octopus (Callistoctopus aspilosomatis) of prey-like objects. Zool Sci 38:495–505. https://doi.org/10.2108/zs210037
Kawashima S, Yasumuro H, Ikeda Y (2021) Plain-body Octopus’s (Callistoctopus aspilosomatis) learning about objects via both visual and tactile sensory inputs: a pilot study. Zool Sci 38:383–396. https://doi.org/10.2108/zs210034
Kuba M, Byrne RA, Meisel DV, Mather JA (2006a) Exploration and habituation in intact free moving Octopus vulgaris. Int J Comp Psychol 19:426–438. https://doi.org/10.46867/ijcp.2006.19.04.02
Kuba MJ, Byrne RA, Meisel DV, Mather JA (2006b) When do octopuses play? Effects or repeated testing, object type, age, and food depravation on object play in Octopus vulgaris. J Comp Psychol 120:184–190. https://doi.org/10.1037/0735-7036.120.3.184
Lee PG (1992) Chemotaxis by Octopus maya Voss et Solis in a Y-maze. J Exp Mar Biol Ecol 153:53–67. https://doi.org/10.1016/0022-0981(92)90016-4
Leite TS, Haimovici M, Mather J (2009) Octopus insularis (Octopodidae), evidences of a specialized predator and a time-minimizing hunter. Mar Biol 156:2355–2367. https://doi.org/10.1007/S00227-009-1264-4
Maselli V, Al-Soudy AS, Buglione M, Aria M, Polese G, Di Cosmo A (2020) Sensorial hierarchy in Octopus vulgaris’s food choice: chemical vs. visual. Animals 10:457. https://doi.org/10.3390/ani10030457
Mather JA, Anderson RC (1999) Exploration, play and habituation in octopuses (Octopus dofleini). J Comp Psychol 113:333–338. https://doi.org/10.1037/0735-7036.113.3.333
Mather JA, O’Dor RK (1991) Foraging strategies and predation risk shape the natural history of juvenile Octopus vulgaris. Bull Mar Sci 49:256–269
Mellon D (2012) Smelling, feeling, tasting and touching: behavioral and neural integration of antennular chemosensory and mechanosensory inputs in the crayfish. J Exp Biol 215:2163–2172. https://doi.org/10.1242/jeb.069492
Messenger JB, Wilson AP, Hedge A (1973) Some evidence for colour-blindness in Octopus. J Exp Biol 59:77–94. https://doi.org/10.1242/jeb.59.1.77
Prescott TJ, Diamond ME, Wing AM (2011) Active touch sensing. Philos Trans R Soc Lond 366:2989–2995. https://doi.org/10.1098/rstb.2011.0167
Robertson JD, Bonaventura J, Kohm A (1995) Nitric-oxide synthase inhibition blocks octopus touch learning without producing sensory or motor dysfunction. Proc R Soc B Biol Sci 261:167–172. https://doi.org/10.1098/rspb.1995.0132
Rowell CHF (1966) Activity of interneurones in arm of octopus in response to tactile stimulation. J Exp Biol 44:589–605. https://doi.org/10.1242/jeb.44.3.589
Strobel SM, Sills JM, Tinker MT, Reichmuth CJ (2018) Active touch in sea otters: in-air and underwater texture discrimination thresholds and behavioral strategies for paws and vibrissae. J Exp Biol 221:jeb181347. https://doi.org/10.1242/jeb.181347
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. https://doi.org/10.1126/science.1060976
Sutherland NS (1962) Visual dsicrimination of shape by Octopus: squares and crosses. J Comp Physiol Psychol 55:939–943. https://doi.org/10.1037/h0040049
Sutherland NS (1963) Shape discrimination and receptive fields. Nature 197:118–122. https://doi.org/10.1038/197118a0
Ten Cate J (1928) L’innervation des ventouses chez Octopus vulgaris. Arch Néerl Physiol 13:407–422
van Giesen L, Kilian PB, Allard CAH, Bellono NW (2020) Molecular basis of chemotactile sensation in Octopus. Cell 183:594–604. https://doi.org/10.1016/j.cell.2020.09.008
Walderon MD, Nolt KJ, Haas RE, Prosser KN, Holm JB, Nagle GT, Boal JG (2011) Distance chemoreception and the detection of conspecifics in Octopus bimaculoides. J Molluscan Stud 77:309–311. https://doi.org/10.1093/mollus/eyr009
Wells MJ (1959) A touch learning centre in Octopus. J Exp Biol 36:590–612. https://doi.org/10.1242/jeb.36.4.590
Wells MJ (1961) Centres for tactile and visual learning in brain of Octopus. J Exp Biol 38:811–826. https://doi.org/10.1242/jeb.38.4.811
Wells MJ (1962) Brain and behaviour in Cephalopods. Heinemann, London
Wells MJ (1964) Tactile discrimination of surface curvature and shape by the octopus. J Exp Biol 41:433–445. https://doi.org/10.1242/jeb.41.2.433
Wells MJ (1978) Octopus—physiology and behaviour of an advanced invertebrate. Chapman and Hall, London
Wells MJ, Young JZ (1965) Split-brain preparations and touch learning in Octopus. J Exp Biol 43:565–579. https://doi.org/10.1242/jeb.43.3.565
Wells MJ, Young JZ (1970) Stimulus generalisation in the tactile system of Octopus. J Neurobiol 2:31–46. https://doi.org/10.1002/neu.480020104
Xie Z, Yuan F, Liu J, Tian L, Chen B, Fu Z, Mao S, Jin T, Wang Y, He X, Wang G, Mo Y, Ding X, Zhang Y, Laschi C, Wen L (2023) Octopus-inspired sensorized soft arm for environmental interaction. Sci Robot. https://doi.org/10.1126/scirobotics.adh7852
Yarnall JL (1969) Aspects of the behaviour of Octopus cyanea Gray. Anim Behav 17:747–754. https://doi.org/10.1016/S0003-3472(69)80022-9
Zullo L, Fossati SM, Benfenati F (2011) Transmission of sensory responses in the peripheral nervous system of the arm of Octopus vulgaris. Vie Milieu 61:197–201
Acknowledgements
We thank Eva Castagna, Tylar Morano, and Anna Krylova for help with animal care. Staff at the Marine Resources Center at MBL provided support with water quality, seawater system maintenance, and collection of food. Thanks to Chuck Winkler of Aquatic Research Consultants for collection and transport of octopuses to Massachusetts.
Funding
This research was supported by the Office of Naval Research Grant # N00014-22-1-2208.
Author information
Authors and Affiliations
Contributions
KCB, RTH, JBG: designed the study. NDH, LB, EYZ, ASL, CF, JH, ZS: conducted experiments, video analysis, and data collection. KB and JGB: analyzed the data. JH: drew Fig. 3. ZS: created Movie S1. KCB, RTH, JGB prepared the manuscript. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Ethical approval
In the United States, cephalopods are not included in federal regulations that govern the use of animals in research laboratories. Consequently, no protocol or approval number was required for this research; however, the care of the animals in this study adhered to The Marine Biological Laboratory’s Cephalopod Care Policy.
Additional information
Handling Editor: Uwe Homberg.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Supplementary file1 (MP4 196597 KB)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Buresch, K.C., Huget, N.D., Brister, W.C. et al. Evidence for tactile 3D shape discrimination by octopus. J Comp Physiol A (2024). https://doi.org/10.1007/s00359-024-01696-4
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00359-024-01696-4