External Articles - Behavior and Intelligence Experiments/Observations

[DWhatley]

The "intelligent" Octopus, Personality, self-awareness, & the need for environmental enrichment
A collection of six short summaries reviewing studies on forms of octopus behavior


The "intelligent" octopusBrain Behavior and Learning
A collection of 4 short summaries reviewing research on octopus intelligence

There has been much study of the neural control of behaviour, including learning, in octopuses. Little comparable work has been done with squids, mainly owing to their mostly pelagic life style and to the difficulty of maintaining them in enclosed spaces. Only a few learning and related studies have been published on west-coast octopuses.

 

[DWhatley]

Behavior Inconsistent with having "personality"
Video playback demonstrates episodic personality in the gloomy octopus R. Pronk, D. R. Wilson,R. Harcourt 2010 (pdf)

Behavior Consistent with having "personality"
Personalities of Octopuses (Octopus rubensens) Roland C. Anderson, Jennifer A. Mather 1993 (pdf)

 

[DWhatley]

Nautilus Rising: A Living Fossil’s Unexpected Renaissance

Curiosity Seeds Blog summary on Nautilus behavior siting professional articles from @robyn and @gjbarord

 

[DWhatley]

Long-term high-density occupation of a site by Octopus tetricus and possible site modification due to foraging behavior
Peter Godfrey-Smith, Matthew Lawrence

Abstract
We report observations of wild octopuses (Octopus tetricus) living in close proximity at a site centered on a single den that has been occupied since at least November 2009. Numbers observed on survey dives range from 2 to 11 (average of 5.48). We hypothesize that long-term occupation of the site has led to its physical modification through the accumulation of shells brought in during foraging, and that this “ecosystem engineering” has in turn resulted in higher densities being viable at the site.

 

[neurobadger]

From my frighteningly large Mendeley library (I have not included links to articles of TONMO members that I know of; you can find them on the Member Publications page):

Alupay, J. S., Hadjisolomou, S. P., & Crook, R. J. (2014). Arm injury produces long-term behavioral and neural hypersensitivity in octopus. Neuroscience Letters, 558, 137–42. doi:10.1016/j.neulet.2013.11.002

Anderson, R. C., Wood, J. B., & Byrne, R. A. (2002). Octopus senescence: the beginning of the end. Journal of Applied Animal Welfare Science, 5(4), 275–83. doi:10.1207/S15327604JAWS0504_02

Andrews, P. L. R., Darmaillacq, A.-S., Dennison, N., Gleadall, I. G., Hawkins, P., Messenger, J. B., … Smith, J. A. (2013). The identification and management of pain, suffering and distress in cephalopods, including anaesthesia, analgesia and humane killing. Journal of Experimental Marine Biology and Ecology, 447, 46–64. doi:10.1016/j.jembe.2013.02.010

Basil, J. A., Barord, G., Crook, R. J., Derman, R., Hui Ju, C., Travis, L., & Vargas, T. (2011). A SYNTHETIC APPROACH TO THE STUDY OF LEARNING AND MEMORY IN CHAMBERED NAUTILUS L.(CEPHALOPODA, NAUTILOIDEA). Vie et Milieu-Life and Environment, 61(4), 231–242.

Brown, E. R., & Piscopo, S. (2013). Synaptic plasticity in cephalopods; more than just learning and memory? Invertebrate Neuroscience, 13(1), 35–44. doi:10.1007/s10158-013-0150-4

Crook, R. J., & Basil, J. a. (2008a). A role for nautilus in studies of the evolution of brain and behavior. Communicative & Integrative Biology, 1(1), 18–9.

Crook, R. J., & Basil, J. A. (2008b). A biphasic memory curve in the chambered nautilus, Nautilus pompilius L. (Cephalopoda: Nautiloidea). The Journal of Experimental Biology, 211(Pt 12), 1992–8. doi:10.1242/jeb.018531

Crook, R. J., & Basil, J. A. (2013). Flexible Spatial Orientation and Navigational Strategies in Chambered Nautilus. Ethology, 119(1), 77–85. doi:10.1111/eth.12040

Crook, R. J., Dickson, K., Hanlon, R. T., & Walters, E. T. (2014). Nociceptive Sensitization Reduces Predation Risk. Current Biology, 24, 1121-1125. doi:10.1016/j.cub.2014.03.043

Grasso, F. W., & Basil, J. A. (2009). The evolution of flexible behavioral repertoires in cephalopod molluscs. Brain, Behavior and Evolution, 74(3), 231–45. doi:10.1159/000258669

Hanlon, R. T. (2007). Cephalopod dynamic camouflage. Current Biology, 17(11), R400–R404. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2674088&tool=pmcentrez&rendertype=abstract

Hochner, B. (2010). Functional and comparative assessments of the octopus learning and memory system. Front Biosci (Schol Ed), 2, 764–771. Retrieved from http://www.octopus.huji.ac.il/site/articles/Hochner-2010.pdf

Hochner, B., Brown, E. R., & Langella, M. (2003). A learning and memory area in the octopus brain manifests a vertebrate-like long-term potentiation. Journal of Neurophysiology, 90(5), 3547–3554. Retrieved from http://jn.physiology.org/content/90/5/3547.short

Hochner, B., Shomrat, T., & Fiorito, G. (2006). The octopus: a model for a comparative analysis of the evolution of learning and memory mechanisms. The Biological Bulletin, 210(3), 308–317. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/16801504

Moriyama, T., & Gunji, Y.-P. (1997). Autonomous Learning in Maze Solution by Octopus. Ethology, 103(6), 499–513. doi:10.1111/j.1439-0310.1997.tb00163.x

Niven, J. E. (2011). Invertebrate neurobiology: visual direction of arm movements in an octopus. Current Biology, 21(6), R217–R218. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/21419985

Shomrat, T., Feinstein, N., Klein, M., & Hochner, B. (2010). Serotonin is a facilitatory neuromodulator of synaptic transmission and “reinforces” long-term potentiation induction in the vertical lobe of Octopus vulgaris. Neuroscience, 169(1), 52–64. doi:10.1016/j.neuroscience.2010.04.050

Shomrat, T., Graindorge, N., Bellanger, C., Fiorito, G., Loewenstein, Y., & Hochner, B. (2011). Alternative sites of synaptic plasticity in two homologous “fan-out fan-in” learning and memory networks. Current Biology, 21(21), 1773–82. doi:10.1016/j.cub.2011.09.011

 

[DWhatley]

Recognizing cephalopod boreholes in shells and the northward spread of Octopus vulgaris Cuvier, 1797 (Cephalopoda, Octopodoidea)
Auke-Florian HIEMSTRA 2015 full article.

INTRODUCTION Aristotle was the first to observe octopuses feed on molluscs (see D’Arcy Thompson, 1910), but it was Fujita who discovered in 1916 that a hole was bored in the shell of cultured pearl oysters prior to its owner being eaten; a behaviour independently discovered by Pilson & Taylor (1961) in laboratory tanks. Octopuses are versatile carnivores with a diverse array of prey, ranging from soft bodied to heavily armoured organisms, such as bivalves, gastropods and crustacean (Nixon, 1987). There are different techniques of penetrating a shell to gain the meat inside (Steer & Semmens, 2003). Enteroctopus dofleini (Wülker, 1910), for example, has four techniques of getting into a clam. If possible, they use the easiest way, according to the optimal foraging model, resorting to drilling only when other methods are unsuccessful (Mather & Anderson, 2007). Regardless of their prey size, Octopus will always try the pulling method first (Fiorito & Gherardi, 1999), but if unsuccessful, it changes its tactics and initiates a drilling response (Hartwick et al., 1978). ...

This article is particularly interesting because it notes that drilling may NOT be solely by the radula.

The drilling activities seem to be carried out by another structure within the buccal mass, namely the small conical teeth on the tip of the muscular salivary papilla (Nixon, 1979a), as not one out of ten octopuses drilled again after surgical removal of their salivary papilla (Nixon 1979a; 1979b). Since the discovery of octopus drillings there has been speculation about possible chemical action on the shell (Fujita, 1916; Pilson & Taylor, 1961; Arnold & Arnold, 1969; Wodinsky 1969; 1973). After comparison of the shell surface it was indeed concluded that some chemical dissolution during drilling may occur (Nixon et al., 1980; Ambrose, 1988).

 

[DWhatley]

Signal Use by Octopuses in Agonistic Interactions
David Scheel, Peter Godfrey-Smith (pgs), Matthew Lawrence (jugglematt) 2016

Summary
Cephalopods show behavioral parallels to birds and mammals despite considerable evolutionary distance [1 and 2]. Many cephalopods produce complex body patterns and visual signals, documented especially in cuttlefish and squid, where they are used both in camouflage and a range of interspecific interactions [1, 3, 4 and 5]. Octopuses, in contrast, are usually seen as solitary and asocial [6 and 7]; their body patterns and color changes have primarily been interpreted as camouflage and anti-predator tactics [8, 9,10, 11 and 12], though the familiar view of the solitary octopus faces a growing list of exceptions. Here, we show by field observation that in a shallow-water octopus, Octopus tetricus, a range of visible displays are produced during agonistic interactions, and these displays correlate with the outcome of those interactions. Interactions in which dark body color by an approaching octopus was matched by similar color in the reacting octopus were more likely to escalate to grappling. Darkness in an approaching octopus met by paler color in the reacting octopus accompanied retreat of the paler octopus. Octopuses also displayed on high ground and stood with spread web and elevated mantle, often producing these behaviors in combinations. This study is the first to document the systematic use of signals during agonistic interactions among octopuses. We show prima facie conformity of our results to an influential model of agonistic signaling [ 13]. These results suggest that interactions have a greater influence on octopus evolution than has been recognized and show the importance of convergent evolution in behavioral traits.

 

[DWhatley]

Pull or Push? Octopuses Solve a Puzzle Problem
Jonas N. Richter, Binyamin Hochner, Michael J. Kuba 2016 (PLOS One full article)

Abstract
Octopuses have large brains and exhibit complex behaviors, but relatively little is known about their cognitive abilities. Here we present data from a five-level learning and problem-solving experiment. Seven octopuses (Octopus vulgaris) were first trained to open an L shaped container to retrieve food (level 0). After learning the initial task all animals followed the same experimental protocol, first they had to retrieve this L shaped container, presented at the same orientation, through a tight fitting hole in a clear Perspex partition (level 1). This required the octopuses to perform both pull and release or push actions. After reaching criterion the animals advanced to the next stage of the test, which would be a different consistent orientation of the object (level 2) at the start of the trial, an opaque barrier (level 3) or a random orientation of the object (level 4). All octopuses were successful in reaching criterion in all levels of the task. At the onset of each new level the performance of the animals dropped, shown as an increase in working times. However, they adapted quickly so that overall working times were not significantly different between levels. Our findings indicate that octopuses show behavioral flexibility by quickly adapting to a change in a task. This can be compared to tests in other species where subjects had to conduct actions comprised of a set of motor actions that cannot be understood by a simple learning rule alone.

 

[DWhatley]

Peripheral injury alters schooling behavior in squid, Doryteuthis pealeii
Megumi Oshima,Theodor Di Pauli von Treuheim, Julia Carroll,Roger T Hanlon,Edgar T Walters,Robyn J Crook 2016 (subscription Science Direct)

Abstract
Animals with detectable injuries are at escalated threat of predation. The anti-predation tactic of schooling reduces individual predation risk overall, but it is not known how schooling behavior affects injured animals, or whether risks are reduced equally for injured animals versus other school members. In this laboratory study we examined the effects of minor fin injury on schooling decisions made by squid. Schooling behavior of groups of squid, in which one member was injured, was monitored over 24 hours. Injured squid were more likely to be members of a school shortly after injury (0.5–2 h), but there were no differences compared with sham-injured squid at longer time points (6–24 h). Overall, the presence of an injured conspecific increased the probability that a school would form, irrespective of whether the injured squid was a member of the school. When groups containing one injured squid were exposed to a predator cue, injured squid were more likely to join the school, but their position depended on whether the threat was a proximate visual cue or olfactory cue. We found no evidence that injured squid oriented themselves to conceal their injury from salient threats. Overall we conclude that nociceptive sensitization after injury changes grouping behaviors in ways that are likely to be adaptive.

 

[DWhatley]

Number sense and state-dependent valuation in cuttlefish
Tsang-I Yang, Chuan-Chin Chiao 2016 (Subscription Proceedings of the Royal Society B)

Editorial summary on Physics.org

Abstract
Identifying the amount of prey available is an important part of an animal's foraging behaviour. The risk-sensitive foraging theory predicts that an organism's foraging decisions with regard to food rewards depending upon its satiation level. However, the precise interaction between optimal risk-tolerance and satiation level remains unclear. In this study, we examined, firstly, whether cuttlefish, with one of the most highly evolved nervous system among the invertebrates, have number sense, and secondly, whether their valuation of food reward is satiation state dependent. When food such as live shrimps is present, without training, cuttlefish turn toward the prey and initiate seizure behaviour. Using this visual attack behaviour as a measure, cuttlefish showed a preference for a larger quantity when faced with two-alternative forced choice tasks (1 versus 2, 2 versus 3, 3 versus 4 and 4 versus 5). However, cuttlefish preferred the small quantity when the choice was between one live and two dead shrimps. More importantly, when the choice was between one large live shrimp and two small live shrimps (a prey size and quantity trade-off), the cuttlefish chose the large single shrimp when they felt hunger, but chose the two smaller prey when they were satiated. These results demonstrate that cuttlefish are capable of number discrimination and that their choice of prey number depends on the quality of the prey and on their appetite state. The findings also suggest that cuttlefish integrate both internal and external information when making a foraging decision and that the cost of obtaining food is inversely correlated with their satiation level, a phenomenon similar to the observation that metabolic state alters economic decision making under risk among humans.