Pl. VI

Part III · Intelligence in Action · Chapter 6

Play Behavior and Individual Personality in Octopuses

Octopuses hold a peculiar place in comparative psychology: solitary, short-lived molluscs that nonetheless became the first invertebrates credited with both individual personality and play. Both claims originated in a single collaboration between Jennifer Mather (University of Lethbridge) and aquarist Roland Anderson (Seattle Aquarium).

Personality/temperament. Mather & Anderson (1993, Journal of Comparative Psychology 107:336–340) tested 44 Octopus rubescens in three standardized situations—alerting (opening the tank lid), threat (touching with a test brush), and feeding (a crab). Factor analysis of the resulting behaviors extracted three orthogonal dimensions—Activity, Reactivity, and Avoidance—explaining ≈45% of variance. This was explicitly framed as analogous to temperament dimensions in human infants, a bold cross-phylum move. Crucially, individual behavior was consistent enough across situations to be called personality, not noise. The framework was extended developmentally by Sinn, Perrin, Mather & Anderson (2001, J. Comp. Psychol. 115:351–364), who observed 73 juvenile O. bimaculoides in week 3 of life; PCA yielded four components (active engagement, arousal/readiness, aggression, avoidance/disinterest, ≈53% variance), and profile analysis of 37 animals showed temperament traits shift significantly from week 3 to week 6, with a detectable effect of relatedness (a genetic signal). Sinn and colleagues later probed the boldness–shyness axis and behavioral syndromes, largely in the related dumpling squid Euprymna tasmanica, finding that bold-in-threat did not predict bold-in-feeding—shy/bold behavior was context-specific and even genetically/phenotypically uncoupled across contexts (Sinn & Moltschaniwskyj 2005; Sinn et al. 2008, 2010). This is an important caveat: cephalopod "personality" is real and repeatable, but the tidy idea of a single bold–shy type that generalizes across all situations does not hold up well.

Play. Mather & Anderson (1999, J. Comp. Psychol. 113:333–338) gave eight Enteroctopus (Octopus) dofleini ten trials with a floating pill bottle. Initial responses were exploration (arm palpation) and habituation, but two of eight octopuses did something else: they repeatedly used their funnel to shoot jets of water at the bottle, pushing it across the tank against the aquarium's intake current so it drifted back—then blowing it away again, "like bouncing a ball." Because this was repeated, non-functional, directed at an already-familiar object (i.e., after exploration was exhausted), and idiosyncratic to particular individuals, it was interpreted as exploratory play. This is often cited as the first experimental evidence of play in any invertebrate.

The most rigorous follow-up is Kuba, Byrne, Meisel & Mather (2006, J. Comp. Psychol. 120:184–190), "When do octopuses play?" Fourteen O. vulgaris (7 subadults, 7 adults) were presented Lego blocks and food items over seven days under differing food-deprivation states. Behavior was scored on a five-level scale (0–4), where the highest level—sustained, varied manipulation not explained by feeding—counted as play-like. Nine of 14 octopuses reached play-like behavior, concentrated on days 3–6, i.e., after the exploratory/habituation phase, supporting the key theoretical claim that play follows exploration developmentally. Notably, play did not differ by food deprivation, age, or sex, arguing against a purely foraging-motivated account. The companion study (Kuba et al., exploration/habituation) distinguished visual-only exploration of a prey-shaped object from tactile manipulation of Lego vs. food.

How "play" is judged and why it's contested. Modern claims are disciplined by Burghardt's (2005) five criteria: behavior is (1) not fully functional in context, (2) voluntary/spontaneous/autotelic, (3) structurally or temporally distinct from serious behavior, (4) repeated but not stereotyped, and (5) performed in a relaxed, unstressed state. A recent PLOS ONE study (Jarmoluk & Pelled 2025) began with nine O. bimaculoides, but only the three animals that learned to unscrew a test tube were subsequently given access to its free-floating cap; all three performed a repeated "release–grasp" sequence (releasing the cap into the current, retrieving it, and releasing it again), meeting the study's Level-4 threshold. Those animals were also active during daytime and engaged with handlers, but because the other six never received the cap, the design cannot establish that play propensity itself was restricted to a personality type. Skeptics further note that extended exploration or arousal can be hard to exclude and sample sizes remain tiny. What is robust: some octopuses repeatedly produce apparently non-functional object manipulation under controlled conditions—rare and remarkable in an invertebrate—but its prevalence and relationship to personality remain uncertain.

Striking / counterintuitive:

• Octopuses were the first invertebrates ever shown to have consistent individual personalities (Mather & Anderson 1993) and the first shown to play (1999) — both from the same aquarist-scientist duo.
• In the founding play study only 2 of 8 octopuses actually played, by jetting water to bounce a pill bottle against the tank current — play was individual, not species-typical.
• Play reliably appears only AFTER exploration is exhausted (days 3–6 in Kuba et al. 2006), supporting the idea that curiosity must be satisfied before an animal 'plays'.
• Play was unaffected by hunger, age, or sex — arguing it is not disguised foraging.
• The bold–shy axis is context-specific in cephalopods: an animal bold under threat is not necessarily bold when feeding, undermining the notion of a single generalizable personality type.
• Juvenile octopus temperament changes with age and carries a heritable (relatedness) signal, despite octopuses being essentially solitary with no parental care.

Open questions:

• Is octopus 'play' genuinely play, or prolonged exploration/arousal? The distinction rests on Burghardt's criteria and tiny samples (often 2–3 individuals).
• What is the neural basis of individual differences — do personality axes map onto identifiable circuits in the vertical lobe or elsewhere?
• How stable are personality traits across a single octopus's short (≈1–2 year) semelparous lifespan?
• Does play have any fitness function in a solitary, fast-growing animal, or is it a byproduct of large brains and manipulative arms (convergent with vertebrates)?
• Why do only a minority of individuals play, and is play propensity itself a stable personality trait linked to activity/boldness?
• Do the 1993 factors (activity, reactivity, avoidance) truly replicate across species and labs, or are the labels artifacts of specific test batteries?

Key researchers/labs: Jennifer A. Mather (University of Lethbridge) — pioneer of octopus personality and play, Roland C. Anderson (Seattle Aquarium, d. 2013) — co-originator of personality/play studies, Michael J. Kuba (Konrad Lorenz Institute / OIST) — object play and exploration experiments, Ruth A. Byrne — cephalopod cognition, arm use, exploration, David L. Sinn (Cal Poly Humboldt) — temperament ontogeny and behavioral syndromes, Natalie A. Moltschaniwskyj — boldness/shyness in cephalopods, Gordon M. Burghardt (Univ. Tennessee) — theorist of the five-criteria definition of play, Galit Pelled & Katarina Jarmoluk — recent O. bimaculoides play work.

Key papers #

• Mather, J.A. & Anderson, R.C. (1993). Personalities of octopuses (Octopus rubescens). Journal of Comparative Psychology 107(3):336–340 — First demonstration of personality in an invertebrate: three factors — Activity, Reactivity, Avoidance (≈45% variance) from 44 O. rubescens across alerting/threat/feeding.
• Mather, J.A. & Anderson, R.C. (1999). Exploration, play, and habituation in octopuses (Octopus dofleini). Journal of Comparative Psychology 113(3):333–338 — First experimental evidence of play in an invertebrate: 2 of 8 octopuses repeatedly jetted water to push a floating pill bottle after exploration was exhausted.
• Kuba, M.J., Byrne, R.A., Meisel, D.V. & Mather, J.A. (2006). When do octopuses play? Effects of repeated testing, object type, age, and food deprivation on object play in Octopus vulgaris. Journal of Comparative Psychology 120(3):184–190 — 9 of 14 O. vulgaris showed play-like behavior (five-level scale), peaking days 3–6 after exploration; unaffected by food deprivation, age, sex — play follows exploration.
• Sinn, D.L., Perrin, N.A., Mather, J.A. & Anderson, R.C. (2001). Early temperamental traits in an octopus (Octopus bimaculoides). Journal of Comparative Psychology 115(4):351–364 — 73 juveniles: four temperament components (≈53% variance); traits change from week 3 to 6 and show an effect of relatedness (genetic signal).
• Burghardt, G.M. (2005). The Genesis of Animal Play: Testing the Limits. MIT Press — Provides the five operational criteria used to adjudicate whether octopus object manipulation qualifies as genuine play.
• Sinn, D.L. & Moltschaniwskyj, N.A. (2005). Personality traits in dumpling squid (Euprymna tasmanica): context-specific traits and their correlation with biological characteristics. Journal of Comparative Psychology 119(1):99–110 — Boldness is context-specific in cephalopods — bold-in-threat does not predict bold-in-feeding, complicating single-axis boldness accounts.
• Jarmoluk, K. & Pelled, G. (2025). Evidence of play behavior in captive California two-spot octopuses (Octopus bimaculoides). PLOS ONE — 3 of 9 octopuses performed repeated release–grasp sequences with floating caps meeting Burghardt's criteria; players were the more active, handler-engaging individuals, linking play to personality.
• Kuba, M.J., Byrne, R.A., Meisel, D.V. & Mather, J.A. (2006). Exploration and habituation in intact free-moving Octopus vulgaris. International Journal of Comparative Psychology 19(4) — Documents non-associative learning (habituation) and the exploration phase that precedes play, using prey-shaped objects, Lego, and food.