Photo of a giant Pacific octopus. Copyright Greg Dombowsky and Dive BC Publications.
Taxonomy and comparative anatomy
Cephalopods are a class of the phylum Mollusca (molluscs) and are therefore related to bivalves scallops, oysters, clams, snails and slugs, tusk shells and chitons. Cephalopods include the pelagic, shelled nautiloids and the coeleoids (cuttlefish, squid and octopods, the group to which octopuses belong). (Authorities agree that the plural of octopus cannot be octopi, as the word is Greek, not Latin.)
The design of a mollusc's nervous system is quite different from that of a vertebrate, despite fundamental similarities at the neuronal level:
The vertebrate central nervous system comprises one main nerve cord that has swollen at one end to create a brain. Most molluscs, on the other hand, have dual nerve cords running like a set of railway tracks along the length of the body (Hamilton, 1997, p. 32).
Among the molluscs, there is an enormous degree of variability in the complexity of the nervous system. Cephalopods are renowned for their large brains, while other molluscs (e.g. bivalves) lack even a head, let alone a proper brain. Most molluscs have a relatively "simple" central nervous system, with five or six pairs of ganglia.
In the cephalopods alone among the molluscs, evolution has also constructed a brain. It has greatly expanded the forwardmost pairs of ganglia and moved them closer together to create a tightly packed mass of lobes that lies between the eyes and encircles the oesophagus (Hamilton, 1997, p. 32).
The brain-to-body weight ratios of cephalopods exceed those of other invertebrates, as well as most fish and reptiles. Additionally, their brains are anatomically complex. However, mammals and birds far outstrip cephalopods in the complexity of their brains (Anderson and Wood, 2001; Hamilton, 1997).
In contrast with molluscs such as clams and oysters, which are passive filter feeders, cephalpods live in a challenging environment, where they have to hunt down mobile prey and avoid predators. They have sophisticated sense organs, a complex rapid movement system, an ability to rapidly change colour and (in the case of cuttlefish and squid) a wide range of social signals (Broom, 2001).
What do cephalopods think with?
So far, we have assumed that cephalopods think with their brains.
...[A]n octopus moves its arms simply by sending a "move" command from its brain to its arm and telling it how far to move.The arm does the rest, controlling its own movement as it extends.
"There appears to be an underlying motor program... which does not require continuous central control," the researchers write (Noble, 2001).
When discussing insects, I argued that there is no reason why intelligence should be tied to a brain. We should be open to the possibility of creatures who think with their arms, especially when "each arm is controlled by an elaborate nervous system consisting of around 50 million neurons" (Noble, 2001).
The learning abilities and adaptive behaviour of cephalopods compare favourably with those of insects and some vertebrates. The following discussion focuses principally on the well-studied common octopus, Octopus vulgaris.
Spatial learning
Cephalopods find their way around by remembering landmarks, as well as the distances they have travelled:
Cephalopods are certainly adept at navigation. Mather and a team of volunteers have mapped the travels of fist-sized O[ctopus] vulgaris as they forage off the coast of Bermuda. The animals venture from their dens on complicated trips lasting up to three hours, and return by different, more direct routes. Although O. vulgaris usually ends up no more than 9 metres from home, other species of octopus can find their dens after journeys of up to 120 metres - over a landscape that easily disorients human scuba divers (Hamilton, 1997, p. 35).
Like some insects, octopuses can navigate flexibly:
A series of disruptions of the foraging trail showed that they could make detours and suggested they were using vision to follow prominent features of the landscape of the rocky bottom (Mather and Anderson, 1998).
The ability of insects to navigate using landmarks has already been identified as indicative of cognitive mental states (see above), irrespective of whether they use allocentric cognitive maps.
Additionally, laboratory tests have shown that octopuses are fast learners that adapt quickly to reversals. They can rapidly learn the location of an escape burrow in an arena and retain this information for a week. When the burrow location is rotated 180 degrees, they display relearning (Langley, 2002).
Octopuses can navigate simple mazes. Lauren Hvorecny and Jessica Grudowski are currently researching learning in octopuses, to determine if they can solve a conditional discrimination maze problem (in maze configuration A, go to hole A; in maze configuration B, go to hole B). The results are still being analysed. The only invertebrate that has demonstrated this type of complex learning is the honeybee.
Conceptual Learning
Experiments on octopuses performed by J. Z. Young in the 1950s and 1960s showed that they can learn to distinguish between shapes, orientations, sizes and degrees of brightness:
In one experiment, Young trained octopuses to select between large and small squares, horizontal and vertical stripes, and black and white circles. He found that the animals could retain all three preferences at once (Hamilton, 1997, p. 34).
However, discrimination is not the same as conceptualisation. Evidence for the latter would be more convincing if it could be demonstrated that octopuses, like honey bees, were able to make distinctions at a more abstract level - e.g. between symmetrical and asymmetrical, or same and different. Research to date on whether octopuses get "the oddity concept" is inconclusive (Mather, personal email, 8 September 2003).
Tool Use
Beck proposes that in order to qualify as a tool user, an animal must be able to modify, carry or manipulate an item external to itself, before using it to effect some change in the environment (Mather and Anderson, 1998). According to this criterion, octopuses use both rocks and water jets from their siphons as tools to modify their environment. After selecting a place for a home, an octopus usually has to modify it extensively to render it suitable for habitation, as it is usually clogged with sand and the shape may not be appropriate. The octopus gathers up excess sand and small rocks and carries them out to the entrance of its new home. Once there, it lets go of the rocks and blasts them all away with a jet of water from its siphon. After removing sand and small rocks from its burrow, an octopus may be left with a large entrance, so it goes outside, picks up some some small rocks and brings them back to the home, piling them up at the entrance.
Octopuses also use water jets to get rid of nuisances:
After capturing crab prey, the octopus will usually kill them and hold one or several under the arm web, dissolve the cartilage holding the joints together, digest out the meat, and keep the exoskeleton bits. When it's finished, it will take the remains to the den entrance and jet the lot out into what becomes a midden. If a scavenging Serranid fish comes by to eat these remains, the octopus may jet a blast of water to remove the 'pest' from the vicinity (Mather and Anderson, 1998).
The problem with Beck's yardstick is that the tool-using behaviour it describes may be either fixed or flexible. The behaviour described above may turn out to be a fixed action pattern, and even Mather and Anderson (1998) admit that octopuses use tools "in a very simple way".
Although octopuses do not appear to fine-tune their behaviour when cleaning their dens, they aim their jets carefully at passing scavengers or human observers - rather like a water gun (Mather and Anderson, 2000). This could be an instance of bona fide agency.
Mather and Anderson (1998) also describe a recent experiment (discussed below) where two octopuses were able to fine-tune the force of their water jets to control the movement of some coloured toys floating in their tank. The octopuses did not manipulate the toys in a stereotypical fashion; indeed, their behaviour seemed spontaneous, even playful. This tool-using behaviour by octopuses appears to have been both flexible and fine-tuned, but follow-up studies are warranted.
At present, then, there are promising leads, but the evidence is insufficient to determine whether tool use in octopuses is accompanied by cognitive mental states.
The ability to change bodily appearance: camouflage, mimicry, signaling and deceit
Cephalopods have an ability to change their appearance which is unrivalled among other animals, thanks to the presence of thousands or even millions of rapidly migrating chromatophores (multi-celled organs containing pigment sacs of various colours) in their skin, which allow them to blend in with their background. It takes less than a second for cephalopods to adopt a new colour pattern, as the process is controlled by the brain through nervous impulses to the muscles. Additionally, cephalopods have soft, flexible bodies and muscles that allow them to change the texture of their skin (Hamilton, 1997; Langley, 2002; Milius, 2001).
Cephalopods use their ability to change their colour patterns and skin texture for various purposes. To avoid being eaten by a predator, they may either blend in with their backgound, or mimic animals that taste bad to the predator, or even mimic animals which feed on the predator (Hamilton, 1997; Langley, 2002; Milius, 2001).
Sometimes, the octopus fled with its arms aligned in a flattened, striped oval, looking much like a common poisonous flatfish. On four occasions when damselfish pestered an octopus, Norman saw it poke six of its legs down a burrow and spread the other two. They sported bands and waved gently, resembling the sea snakes that prey on damselfish.When Norman saw a mimic octopus chugging along well above the seafloor, extended arms colored in stripes, he thought of the sunburst of striped, poisonous spines that lionfish flare (Milius, 2001).
Cephalopods also change their colour patterns and texture to camouflage themselves while hunting prey, to signal (or disguise) their intentions during courtship, and to deceive or ward off attacks by rival males (Hamilton, 1997).
The Caribbean reef squid affords a spectacular example of this behaviour:
[It] has at least 35 patterns in addition to its almost magical ability to blend in with its background. It can flash a different display on each side of its body when positioned between a potential mate, which sees a uniform light grey, and a rival male, which sees tiger striping called the "intense zebra display". If the positions change, so do the patterns (Hamilton, 1997, p. 33).
Similarly, male cuttlefish adopt female colouring, patterns, and shape, to gain access to females guarded by larger rivals (Scigliano, 2003).
The behaviour described here can easily be interpreted in intentional terms: mimicry, disguise, strategic planning and deception. A useful question to ask might be: do we need to adopt an agent-centred stance in order to account for the behaviour? To answer this question, we need to do three things. First, we need to discover what causes these colour and texture changes in cephalopods. Are they triggered by simple reflexes, or is there at least some scope for fine motor control, as we observed in Drosophila, which would allow us to speak of agency here? Unfortunately, the sheer rapidity of the changes makes it difficult to investigate their etiology.
Second, we have to find out whether cephalopods are physically capable of controlling (i.e. fine-tuning) their color and texture changes. In my discussion of agency in Drosophila, I suggested that fine motor control required an interaction between an animal's feedforward and feedback mechanisms, and that efferent copy played a vital role. Certainly, the body movements of the Indonesian mimic octopus appear fine-tuned to the circumstances.
Colour changes in cephalopods are more problematic. Although they are directed by the brain via the nervous system, no muscular movements appear to be involved. Can there be trying wihout muscular activity? It is hard to see how we can speak of a cephalopod as trying to turn black unless it can compare its current colour with that of its surroundings and adjust its bodily movements accordingly. On the other hand, processes which are involuntary in vertebrate nervous systems may not be so in cephalopods.
Third, we need to investigate whether the behaviour observed is a fixed action pattern or whether it is truly flexible, as defined in this thesis. For instance, is there any evidence of learning? Do young cephalopods display a "learning curve" when camouflaging their appearance, mimicking other animals or signaling to mates? And can they learn by watching their peers? (The answer to the last question is probably negative.)
Flexible behaviour in octopuses?
Mather and Anderson (2000) describe how octopuses will use a variety of techniques to open a clam shell, switching readily from one to another in the event of failure. Giant Pacific octopuses switch strategies to open different shellfish - smashing thin mussels, prying open clams, and drilling tougher-shelled clams. When clams were wired shut with stainless steel wire, the octopuses couldn't pull them apart, so they switched to drilling and chipping. The authors comment:
They were intelligently adapting the penetration technique to the clam species presented and the situation in which they were placed.
The above interpretation is reasonable. Unfortunately, the range of behaviours involved here is too narrow to decide whether the octopuses were acting intentionally or in a hit-and-miss fashion.
Observational learning in cephalopods?
Fiorito and Scotto (1992) reported that an octopus in a research laboratory in Naples learned to choose a red ball instead of a white one, simply by watching another octopus. (Actually, octopuses prefer red over white, but the opposite preference has also been induced in recent experiments.) The discovery of observational learning, if confirmed, would be remarkable, as octopuses are short-lived, solitary creatures that usually meet only to copulate, and as even some mammals are incapable of this learning feat (Hamilton, 1997). However, other researchers, including Jean Boal, have tried without success to replicate the results (Mather, personal email, 8 September 2003). Commenting on the original experiment, Woods (2003) writes:
A critique by Biederman and Davey of the Fiorito and Scotto experiment can be found in Science vol 259 (March 12, 1993). The critique questions: if the observational octopuses attacked the ball more often since it was a familiar item (i.e. octopuses are hesitant to attack novel stimuli), [and] if observational learning or rapid imitation occurred (what was the role of the stimuli and the role of the demonstrator octopus - why were these not controlled for?). I should mention that Fiorito defends the experiment in the same issue of Science. The bottom line, at least in my mind, is that the Fiorito and Scotto experiment failed to prove observational learning since other factors were not controlled for. I certainly would not rule out the possibility of observational learning in cephalopods - after all they are the most advanced invertebrates. On the other hand, octopuses are not very social so there may not be much of a chance for them to evolve the ability to learn by observing other octopuses.
On methodological grounds alone, it would be imprudent to ascribe observational learning to cephalopods. There is another reasons to question the cognitive interpretation of the octopuses' behaviour: learning can also be triggered by events that convey no technical (means-end) information, suggesting that the skills are latent within the octopus and not learned.
Late last year at Woods Hole, Boal, Hanlon and graduate student Kim Wittenberg allowed animals to observe trained cuttlefish attack and eat a crab, and then compared their performance in the same situation with a naive animal. The observers did learn more quickly how to hunt down a crab. But they also hunted better if they had previously seen only a crab without a predation event, or even if they had simply smelt that a crab was kept hidden behind a partition. 'If smelling a crab means you perform better than if you hadn't smelled one before, and watching a predation event is no better than simply smelling a crab,' says Boal, 'then we're talking [about] some kind of releaser of an innate behavior' (Hamilton, 1997, p. 35).
Play in octopuses
Mather and Anderson (1999) define play as "activity having no immediate benefits and structurally including repetitive or exaggerated actions that may be out of sequence or disordered", and reported observing some octopuses playing with objects. Scigliano (2003) describes their experiment:
Anderson tested for play by presenting eight giant Pacific octopuses with floating pill bottles in varying colors and textures twice a day for five days. Six octopuses examined the bottles and lost interest, but two blew them repeatedly into their tanks' jets. One propelled a bottle at an angle so it circled the tank; the other shot it so it rebounded quickly and on three occasions shot it back at least 20 times, as if it were bouncing a ball.
However, Boal questions the authors' interpretation, and suggests that the behaviour may reflect boredom (like a cat pacing), rather than creativity. More recently, another researcher, Ulrike Griebel, offered common octopuses a variety of objects, from Lego assemblies to floating bottles on strings. Some octopuses took toys into their nests and toted them along while fetching food. Griebel suggests that this "might be an early stage of object play" (Scigliano, 2003).
Mather and Anderson (2000) argue that "[p]lay involves the detachment of actions from their primary context, and such flexibility is both a basis and a sign of intelligence, whether it be shown in a person or a fish or an octopus." The key insight here is that the player self-selects a new goal and performs the actions to achieve this goal rather than the natural end of the behaviour. Genuine play is therefore cognitive.
The upshot of our overview is that although we cannot be as certain as for insects, cephalopods also appear to be creatures with minds of their own, possibly rivalling those of some vertebrates.
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