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External Articles - Behavior and Intelligence Experiments/Observations

DWhatley

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#2
Navigation by spatial memory and use of visual landmarks in octopuses

Navigation by spatial memory and use of visual landmarks in octopuses Jennifer A. Mather Journal of Comparative Biology January 1991

Abstract:
This study begins to evaluate how octopuses navigate, and whether they can use visual landmarks. Paths ofOctopus vulgaris were observed in the field as they foraged and responded to displacements.Octopus rubescens were trained to orient to a beacon in the laboratory, and response to its displacement was monitored.
2. Octopuses foraged using chemotactile exploration but did not retrace their outgoing paths.
3. Octopuses learned to orient to a beacon for a food reward, and oriented directly to it when it was moved 90° each day.
4. When a three-landmark array was presented to one octopus it oriented first to the largest landmark, then to the beacon. It responded to movement of one or more landmarks suggesting both orienting to this conspicuous landmark and going to where the beacon ought to have been.
5. The lack of disruption of octopuses' return home in the field by movement of an artificial landmark, the significant prediction of whether they would eat away from home by distance from the home, and their ease of return home when they were displaced by territorial fish, in combination with the lab data, suggested that octopuses can and do use a long-term memory of a visual landmark array.

The full article is available (for a fee) through SpringerLink. A recent news/press release with more information than the abstract can be found in the Scientific American Blog, The Thoughtful Animal
 

DWhatley

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#3
Octopus vulgaris Uses Visual Information to Determine the Location of Its Arm

Octopus vulgaris Uses Visual Information to Determine the Location of Its Arm
Tamar Gutnick,Ruth A. Byrne,Binyamin Hochner,Michael Kuba Science Direct March 2011

Full article, PDF and video.


Octopuses are intelligent, soft-bodied animals with keen senses that perform reliably in a variety of visual and tactile learning tasks [1,2,3,4,5,6]. However, researchers have found them disappointing in that they consistently fail in operant tasks that require them to combine central nervous system reward information with visual and peripheral knowledge of the location of their arms [6,7,8]. Wells [6] claimed that in order to filter and integrate an abundance of multisensory inputs that might inform the animal of the position of a single arm, octopuses would need an exceptional computing mechanism, and There is no evidence that such a system exists in Octopus, or in any other soft bodied animal. Recent electrophysiological experiments, which found no clear somatotopic organization in the higher motor centers, support this claim [9]. We developed a three-choice maze that required an octopus to use a single arm to reach a visually marked goal compartment. Using this operant task, we show for the first time that Octopus vulgaris is capable of guiding a single arm in a complex movement to a location. Thus, we claim that octopuses can combine peripheral arm location information with visual input to control goal-directed complex movements
 

DWhatley

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#4
A perspective on the study of cognition and sociality of cephalopod mollusks, a group of intelligent marine invertebrates http://onlinelibrary.wiley.com/doi/10.1111/j.1468-5884.2009.00401.x/abstract 2009 YUZURU IKEDA (subscription required)

Abstract
Cephalopod mollusks are found virtually everywhere throughout the world's oceans. They are highly mobile invertebrates that have evolved behavioral and morphological defenses against vertebrate predators. Unlike other mollusks, the coleoid cephalopods (octopus, cuttlefish, and squid) possess highly developed nervous systems with huge brains equivalent in size to some vertebrate brains. Cephalopod intelligence is also exhibited by their impressive memory and learning abilities. Why have cephalopods developed such huge brains and cognitive ability? One of the keys to answering this question lies in understanding the social interactions of cephalopods, which have thus far not been well documented. In this paper, I will outline our recent behavioral experiments using mirrors with some cephalopods and discuss these experiments in light of the diversity of social and cognitive behaviors of cephalopods.
 

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#5
Cephalopod cognition in an evolutionary context: implications for ethology - Joseph J Vitti


Abstract:
What is the distribution of cognitive ability within the animal kingdom? It would be egalitarian to assume that variation in intelligence is everywhere clinal, but examining trends among major phylogenetic groups, it becomes easy to distinguish high--performing ‘generalists’ – whose behavior exhibits domain--flexibility – from ‘specialists’ whose range of behavior is limited and ecologically specific. These generalists include mammals, birds, and, intriguingly, cephalopods. The apparent intelligence of coleoid cephalopods (squids, octopuses, and cuttlefish) is surprising – and philosophically relevant – because of our independent evolutionary lineages: the most recent common ancestor between vertebrates and cephalopods would have been a small wormlike organism, without any major organizational structure to its nervous system. By identifying the cognitive similarities between these organisms and vertebrates, we can begin to derive some general principles of intelligence as a biological phenomenon. Here, I discuss trends in cephalopod behavior and surrounding theory, and suggest their significance for our understanding of domain--general cognition and its evolution.
 

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#6
The Octopus Vertical Lobe Modulates Short-Term Learning Rate and Uses LTP to Acquire Long-Term Memory 2008
Tal Shomrat1, Ilaria Zarrella2, Graziano Fiorito2, Binyamin Hochner
Full PDF available at link
Summary
Analyzing the processes and neuronal circuitry involved in complex behaviors in phylogenetically remote species can help us understand the evolution and function of these systems. Cephalopods, with their vertebrate-like behaviors 1, 2, 3, 4 and 5 but much simpler brains [6], are ideal for such an analysis. The vertical lobe (VL) of Octopus vulgaris is a pivotal brain station in its learning and memory system [7]. To examine the organization of the learning and memory circuitry and to test whether the LTP that we discovered in the VL [8] is involved in behavioral learning, we tetanized the VL to induce a global synaptic enhancement of the VL pathway. The effects of tetanization on learning and memory of a passive avoidance task were compared to those of transecting the same pathway. Tetanization accelerated and transection slowed short-term learning to avoid attacking a negatively reinforced object. However, both treatments impaired long-term recall the next day. Our results suggest that the learning and memory system in the octopus, as in mammals [9], is separated into short- and long-term memory sites. In the octopus, the two memory sites are not independent; the VL, which mediates long-term memory acquisition through LTP, also modulates the circuitry controlling behavior and short-term learning.
 

DWhatley

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#7
Cognition and Recognition in the Cephalopod Mollusc Octopus vulgaris: Coordinating Interaction with Environment and Conspecifics Elena Tricarico, Piero Amodio, Giovanna Ponte, Graziano Fiorito

If anyone has access to this paper, I would love to read a "free" copy. Unfortunately, the abstract does provide even a hint on how the article relates to the title.

Abstract
Cephalopods provide numerous examples of behavioral and neural plasticity and richness of the behavioral repertoire that has been claimed in favour of cognitive capabilities. Here we revise the most recent knowledge on octopus cognition and recognition processes. The examination of data and observations available provide the basis for asking new stimulating questions about the cognitive abilities of octopuses and their allies and open novel scenarios for future comparative research.
 

DWhatley

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#8
Cephalopod Consciousness
2010 Cephalove Mike Lisieski
I (Mike Lisieski) am an undergraduate student in Psychology and Pharmacology. I plan to pursue an M.D. and a Ph.D in behavioral neuroscience after finishing my undergraduate degrees. Cephalove is a project I started in May 2010 to make science related to cephalopods more accessible on the internet. Conveniently enough, it also gives me something entertaining to do that (hopefully) keeps my mind sharp. My background is in neuroscience and psychology, and so I tend to focus on these topics when discussing cephalopod research – though I try to give all disciplines a fair shake. I blogged for a few months at blogger, and then moved to the Southern Fried Science network, where I’m looking forward to blogging in a more visible location!

Cephalopods are a somewhat tangential research interest to me; I am generally interested in neuroscience and psychology, and more specifically in the neuroscience and psychology of psychoactive drugs. My first introduction to cephalopods in scientific research was through Fioritio and Scotto’s 1992 paper on observational learning in O. vulgaris, after which I discovered J. Z. Young’s work on cephalopod neuroanatomy. After casually reading these, and a visit to the Pittsburgh Zoo where I saw a beautiful O. dofleini crawling about its tank, I decided to start this blog. Prior to writing this blog, I have very little background in marine biology per se, although I have been interested in biology as long as I can remember.
Cephalopod Consciousness Part 1: Who cares?
Cephalopod Consciousness Part 2: The Case for Animal Consciousness
Cephalopod Consciousness Part 3: The Case for Cephalopod Consciousness

 
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DWhatley

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#9
Octopuses (Enteroctopus dofleini) Recognize Individual Humans
Roland C. Anderson, Jennifer A. Mather, Mathieu Q. Monette, Stephanie R. M. Zimsen 2010 (subscription)

Abstract
This study exposed 8 Enteroctopus dofleini separately to 2 unfamiliar individual humans over a 2-week period under differing circumstances. One person consistently fed the octopuses and the other touched them with a bristly stick. Each human recorded octopus body patterns, behaviors, and respiration rates directly after each treatment. At the end of 2 weeks, a body pattern (a dark Eyebar) and 2 behaviors (reaching arms toward or away from the tester and funnel direction) were significantly different in response to the 2 humans. The respiration rate of the 4 larger octopuses changed significantly in response to the 2 treatments; however, there was no significant difference in the 4 smaller octopuses' respiration. Octopuses' ability to recognize humans enlarges our knowledge of the perceptual ability of this nonhuman animal, which depends heavily on learning in response to visual information. Any training paradigm should take such individual recognition into consideration as it could significantly alter the octopuses' responses
Playing “Good Cop, Bad Cop” with Octopuses, The Scorpion and the Frog editorial from the 2010 experiment.
 
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DWhatley

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#10
I Know My Neighbour: Individual Recognition in Octopus vulgaris
Elena Tricarico, Luciana Borrelli, Francesca Gherardi, Graziano Fiorito 2011 (full article)

Abstract
Background
Little is known about individual recognition (IR) in octopuses, although they have been abundantly studied for their sophisticated behaviour and learning capacities. Indeed, the ability of octopuses to recognise conspecifics is suggested by a number of clues emerging from both laboratory studies (where they appear to form and maintain dominance hierarchies) and field observations (octopuses of neighbouring dens display little agonism between each other). To fill this gap in knowledge, we investigated the behaviour of 24 size-matched pairs of Octopus vulgaris in laboratory conditions.

Methodology/Principal Findings
The experimental design was composed of 3 phases: Phase 1 (acclimatization): 12 “sight-allowed” (and 12 “isolated”) pairs were maintained for 3 days in contiguous tanks separated by a transparent (and opaque) partition to allow (and block) the vision of the conspecific; Phase 2 (cohabitation): members of each pair (both sight-allowed and isolated) were transferred into an experimental tank and were allowed to interact for 15 min every day for 3 consecutive days; Phase 3 (test): each pair (both sight-allowed and isolated) was subject to a switch of an octopus to form pairs composed of either familiar (“sham switches”) or unfamiliar conspecifics (“real switches”). Longer latencies (i.e. the time elapsed from the first interaction) and fewer physical contacts in the familiar pairs as opposed to the unfamiliar pairs were used as proxies for recognition.

Conclusions
Octopuses appear able to recognise conspecifics and to remember the individual previously met for at least one day. To the best of our knowledge, this is the first experimental study showing the occurrence of a form of IR in cephalopods. Future studies should clarify whether this is a “true” IR.
 

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#11
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

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#12

DWhatley

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#14
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.
 
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neurobadger

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#15
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

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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

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#17
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.
 

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#18
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.
 

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#19
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.
 

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#20
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.
 

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