Cephalove

Most species of shallow water octopuses appear to be pretty solitary animals. They live in dens and venture out from them to hunt or find mates; defending these dens and getting busy are the only social interaction that many species of octopuses are observed to have in the wild. I like to think of them as the curmudgeons of the reef environment, keeping to themselves because that’s just the way they like it.

Keep movin', buddy; there's nothing to see here. (Photo by algaedoc)

It might surprise us, then, to learn that Elena Tricarico and her coworkers, working out of the Stazione Zoologica in Naples, just published a paper arguing the octopuses (of the species Octopus vulgaris), can recognize other individual octopuses. While it’s clear that this ability might be important to more social cephalopods (like squids, which form schools), what good could it do for a species with such a hermit-like existence?

It turns out that keeping to one’s self in an area where there are lots of other organisms around requires some social skills – you have to know a little about the folks around you and what behavior to expect from them. For example, if you see the same animal patrolling an adjacent territory each day, it doesn’t do much good to make a huge fuss over it all the time. If you have your territory, and she has hers, it behooves you both to be able to recognize each other so that you don’t waste time and energy chasing off somebody who isn’t actually going to cause you any problems (this is called the “dear enemy” effect.) On the other hand, if a wandering octopus comes through looking for a good nesting site, it would be useful to be able to tell that he’s a stranger so that you could drive him away and keep him from taking over your territory. Thinking about it in these terms, it makes sense that the ability to recognize other octopuses could be a useful ability to have.

To test whether octopuses could do this, Tricarico and coworkers divided up their experimental octopuses into two groups; in one group, pairs of octopuses were housed with a clear divider between them, so that they could see their partner, while in the other group the octopuses had an opaque divider. After letting the octopuses either see or not see each other for 3 days, they watched how these pairs interacted with each other when they were put into the same test tank for 15 minutes. It turns out that pairs that had seen each other before avoided each other more, touched each other less, and spent a longer time ignoring each other when they were placed in the same tank than pairs that had been separated by the opaque divider.

This alone isn’t enough evidence to conclude that octopuses can recognize other individual octopuses – after all, the pairs that could see each other might just be getting used to being around any octopus. To test whether the octopuses had learned to recognize their specific partner or just gotten used to the presence of other octopuses, the researchers did one more test – they put the octopuses back in the test tank, but this time, they put some of them in with the familiar octopus they had been seeing throughout the experiment, and some of them in with an octopus they had never seen before. What they saw was this: when octopuses were placed with another octopus that they were familiar with, they touched each other less, avoided each other more, and their interactions were shorter than when they were placed with unfamiliar octopuses. It looked as if the octopuses had learned to recognize their partner, and responded differently to them than to a strange octopus.

Like all good experiments, this one begs plenty of questions: can octopuses tell who individuals are, or do they just categorize other octopuses as familiar or unfamiliar? Does their ability to discriminate other individuals imply some sort of social cognition, and of what sort (I’d argue that it suggests only very basic social cognitive skills, but opens the door for more investigation,) and, finally, do I need to worry that someday, the octopuses will learn to recognize ME?

That's right, buddy, I'm looking at YOU. (photo by Rowland Cain)

Thanks for reading! I’d like to point out that I took the title of this post directly from the paper it discusses; it was such a good title that I couldn’t think of anything more fitting.

Elena Tricarico, Luciana Borrelli, Francesca Gherardi, Graziano Fiorito (2011). I Know My Neighbour: Individual Recognition in Octopus vulgaris PLOS One : 10.1371/journal.pone.0018710

A story about squid has been making the rounds in news sources and blogs this weekend. Just two days ago, a paper came out showing that male squid (loligo peleii) react with extreme agression to a certain protein found on the surface of squid eggs. The paper was written by a group of researchers (including the illustrious cephalopod biologists Jean Boal and Roger Hanlon) from all over the world.

The authors of the study noted that, when this species of squid get together in big groups, the males interact with the eggs that the female attach to the sea floor in a curious way – they approach eggs that are already attached to the sea floor, blow water on them, and then touch the eggs with their head and arms. This occurs before and in-between fights that the males have with each other, in which they compete over the opportunity to mate with females.

To confirm that some component of the eggs was causing the squid’s aggression, the experimenters put pairs of male squids into tanks with eggs. Sure enough, touching the eggs made the squids more aggressive.

Squid eggs attached to the seafloor, by Debby Ng

The authors then made an extract of the squid eggs, and used a technique called high-performance liquid chromatography to separate their extract into different parts. HPLC works by forcing a solution through a tube (called an HPLC column) that the various substances in the solution stick to in some way. Depending on the specific conditions, different substances will get stuck in the column for longer or shorter times. Substances that don’t stick to the column very well come out the other side quickly, and substances that stick to the column very well will come out more slowly. The solution coming out of the column at a certain time will contain only some of the substances that were in the original solution, and so it is a useful way to separate a complex mixture up into parts, called fractions.

After the egg extract was divided up into fractions, the various fractions were tested to see if they made males aggressive. After finding which fraction was responsible for this effect, the authors purified it further and identified a specific protein within it and figured out its amino acid sequence.

The culpit, it turns out, is a small protein that is related to a family of proteins called the Beta-microseminoproteins, which have been found in species from humans to scallops to ostriches. The female squid’s reproductive tract secretes this protein as part of the coating of the eggs she lays.

In humans, this group of proteins is found in the male reproductive tract, where it attaches to the outside of sperm cells and may be related to a man’s level of fertility. Nobody has asked whether it also makes males of mammalian species more aggressive, although I suppose it is only a matter of time now.

How could the behavior we’re looking at (that is, the fact that males of the species L. pealeii just flip out when they sense this protein) be good for the squid? Behaviors have to evolve, and so they need to help the individual to reproduce in some way.

It’s easy to see how being aggressive and competitive would help a male mate. The real question is: why use a pheronome? And why on the eggs? In a squid mating frenzy, there is ample stimulation – why don’t male squids simply become intensely aggressive at the site of a large group of other squid? That would seem to involve less energy (and less evolutionary backflips) than first seeing the mating frenzy, then seeing the eggs on the seafloor, then approaching and touching them, and only then being spurred into super-aggression.

For starters, it’s good to remind ourselves that none of the components of that behavioral sequence, odd as it is, evolved specifically for that purpose. Because the type of protein that is used as a pheremone in this case is found in many animals, it very clearly has been around for a long time before squid evolved specific mating habits, filling other necessary (and currently unknown) functions. Similarly, squid were probably spawning in groups and competing for mates before they developed the ability to respond to this protein with aggression.

Of course, this could be wrong – if it turns out that beta-microseminoproteins is used as a pheremone in lots of different species, then it may have evolved this function very long ago. Only more research will tell.

Functionally speaking, though, why would a pheremone evolve as a cue for aggression, even when there are plenty of other cues in the environment for the male squid to respond to (the sight of eggs and other squids being the easiest to think of)? My thought is that, in a system that can change as quickly and as unpredictably as an ecosystem, it always helps to have reduntancy. Having two seperate senses that both cause the right behavior in the right context is better than having just one, because either one might fail at an inopportune time and leave the animal (figuratively) screwed.

The other idea that I came up with is that it might help the squids recognize when a spawning group is made up of the right kind of squid – squids of their own species or sub-species. There are many types of squid that look alike to me, and while I’m sure that squid are better at telling the difference between their own kind than I am, it seems like a relatively easy mistake to make in poor conditions (dark or murky water, or the added confusion of predators being present.) Any squid who couldn’t clearly tell when the squids available for mating were squid they could actually produce offspring with would be at a huge disadvantage in terms of making babies. Again, this question could only be answered with more research.

Thanks for reading!

Scott F. Cummins, Jean G. Boal, Kendra C. Buresch,, Chitraporn Kuanpradit, Prasert Sobhon,, Johanna B. Holm, Bernard M. Degnan, Gregg T. Nagle,, & and Roger T. Hanlon (2011). Extreme Aggression in Male Squid Induced by a b-MSP-like Pheromone Current Biology : 10.1016/j.cub.2011.01.038

Anahí Franchi N, Avendaño C, Molina RI, Tissera AD, Maldonado CA, Oehninger S, & Coronel CE (2008). beta-Microseminoprotein in human spermatozoa and its potential role in male fertility. Reproduction (Cambridge, England), 136 (2), 157-66 PMID: 18469041

Everybody likes cuttlefish, it seems. They’re neat-looking, sociable, and display lots of entertaining behavior. I think it’s about time, then, to start talking about what cuttlefish do best: change color! I’ll start at what is, as far as I can tell, the beginning.

In 1988, Roger Hanlon and John Messenger published a paper called “Adaptive Coloration in Young Cuttlefish (Sepia Officinalis L.): The Morphology and Development of Body Patterns and Their Relation to Behaviour.” This paper lays out a description of the body-patterning behavior of young cuttlefish (S. officinalis), paving the way for many future studies on this behavior and the environmental features mediating it. The authors hatched and raised “more than 50″ cuttlefish, recording their behavior while they were in the laboratory, and then releasing them into the sea and videotaping them. From this (very large) set of data, they developed a systematic description of the various components of cuttlefish body patterns, as well as some ideas about what adaptive function they serve to the cuttlefish to use them. In addition, they did some microscopic analyses of the animal’s brains and skins, which I will spend less time on here.

The authors decided, based on precident as well as their own ingenuity, to describe the body patterns of cuttlefish (that is, the patterns of postures and colors that cuttlefish display) using a hierarchical scheme. In this scheme, each body pattern corresponds to one or a few behaviors, during which it is expressed. The body pattern is itself composed of multiple components – it has chromatic components (specific patterns of coloration,) textural components (specific patterns of skin texture,) postural components ( specific ways the cuttlefish holds its body,) and locomotor components (the ways the cuttlefish moves its body during the display.) Each of these components is made up of several units. The term “unit” as used here refers to a group of muscles that acts together to produce a local effect, many of which add up to become a body pattern component. For example, the group of muscles in each arm that hold that arm in a certain position make up a postural unit, and all of the postural units (that is, all of the arm and mantle muscle groups) together make up a postural body pattern component. Each unit is in turn made up of a number of elements, which are the smallest possible pieces that can display a particular tiny piece of a body pattern – for example, a single arm or skin muscle, or a single chromatophore. If that confused you, just take a look at their first figure, diagramming this concept:

Click through for a larger version.

The authors identify 54 components in all: 34 chromatic components, 6 textural components, 8 postural components, and 6 locomotor components. They also identify 13 distinct body patterns that are made out of these components: 6 chronic patterns (those expressed stably for a long time) and 7 acute patterns (those expressed transiently, usually in reaction to some significant or disturbing event.)

As an aside, I’d like take a moment to throw around a few counter-arguments to a common abuse of this line of research – namely, the claim that people like to throw around that cuttlefish and squid have a “language” that they express with their skin.

Firstly, cuttlefish displays are not symbolic – a cuttlefish who displays (for example) a pattern associated with mating is symoblizing sex, or the desire to have sex – the fact is that cuttlefish that want to have sex behave in a particular way. Calling this language is like saying that your dog is speaking to you when he humps your leg. He’s not telling you that he wants to have sex – he’s just doing what amorous dogs do.

Secondly, cuttlefish displays do not seem to have syntax. One of the things that makes language useful, and indeed defines language, is the ability to use various components of that language in novel ways, to communicate novel ideas. Related to this is the fact that the meanings of symbols are arbitrary – they can change, and do not neccessarily resemble or otherwise relate to whatever is being symbolized. There is simply no evidence that cuttlefish body patterns are this flexible, or ever mean anything besides making the behaviors they are part of more distinctive or effective. They may serve as an avenue of communication between conspecifics in some instances (in fact, they almost certainly do) but it is woefully inaccurate to describe them as language, especially without any further qualification.

Even if cuttlefish body patterning were a language, it would be a poor one. In most languages, a small number of symbols are used in various combinations to make a variety of units of meaning. For example, letters combine to form words, which combine to form short phrases. In english, there are 26 letters and many thousands of words and short phrases. Combining letters generates new information, not contained in the individual letters. The transition from components to body patterns in cuttlefish, on the other hand, causes information to be lost. Out of many components, cuttlefish put together only a few units of meaning.

So dear internet: I know how much you love cuttlefish, and I know that you want everybody else to love them, too. Exaggerating the evidence to make them seem more “intelligent” is not a valid way to do this, and makes you look unintelligent, dishonest, or both. Please, for your own good and the good of cephalopods everywhere, stop.

Anyways, back to the paper:

What do cuttlefish use these body patterns for? Most of the chronic body patterns are used for crypsis, or camoflage. A cuttlefish will use these patterns to blend into whatever is around them, so that they don’t get eaten. The plate below shows three cuttlefish in different developmental stages blending into the same substrate. The youngest one (towards the bottom of the photograph) is showing (as well as I can tell) a “strong disruptive” pattern, made up of highly contrasting dark and light components. The next oldest one (towards the top of the photograph) is showing a “weak disruptive” pattern, with the same basic scheme but with less contrast. The oldest one (right in the middle) is showing a “dark mottle” pattern, which is just what it sounds like:

When hiding fails, cuttlefish will show a variety of acute patterns in defense. Included among these are “uniform blanching” and “uniform darkening”, both of which are used to confuse would predators. A posture called “flamboyant”, where the cuttlefish waves its arms in the water, is used to startle predators. Adult cuttlefish use a pattern called the “deimatic” pattern, where the cuttlefish flattens and turns completely white except for a few dark markings on the mantle is theorized to be a sort of bluff: it makes the cuttlefish look bigger, and (hopefully) frightenes whatever predator is pursuing the cuttlefish enough to drive it off.

Patterns called “zebra” and “intense zebra” are used in social behavior, which primarily consists of sexual behavior and agonistic behavior (fighting or aggressive displays.) Variations on these patterns are used to distinguish between males and females. The picture below shows a male displaying the “intense zebra” pattern to a female. The authors note the critical inclusion of the extended and densely patterned fourth arm (the one most towards the bottom of the photograph,) the absence of which is one of the things that distinguishes the female “zebra” display from the male “zebra” display.

Click through for a larger version.

Finally, (and this is what I like best about this paper,) the authors close with a call for work “towards a comparative cephalopod ethology.” I can’t say it any better than they did:

It is clear from our work and [others] that cephalopod body patterns are inextricably linked with cephalopod behaviour so that study of body patterns becomes central to cephalopod ethology…

Recently there has been increased interest in ecological studies of cephalopods and we hope field researchers will begin to record systematically ethological data such as adaptive coloration, with the long-term goal of providing a more comprehensive view of their behaviour and life style.

Thanks for reading! I only covered this paper in the roughest way, so I urge those who want to know more to check it out – it’s available from Royal Society Publishing.

Hanlon, R., & Messenger, J. (1988). Adaptive Coloration in Young Cuttlefish (Sepia Officinalis L.): The Morphology and Development of Body Patterns and Their Relation to Behaviour Philosophical Transactions of the Royal Society B: Biological Sciences, 320 (1200), 437-487 DOI: 10.1098/rstb.1988.0087

In this second post of the series “Cephalopod Consciousness”, I’ll talk about the methods that scientists have used to attempt to study consciousness in animals. For perhaps the first time in the history of this blog, I’ll write about science without making any specific reference to cephalopods – I’m saving that for part 3. Here I’ll just cover enough background get a basic handle on the study of consciousness in non-humans, so that I can talk all about its application to cephalopods next time.

I’ll refer primarily to three review articles as I move through the various paradigms used to argue for or against non-human consciousness. These articles are Animal consciousness: a synthetic approach by Edelman and Seth (2009), Subjective experience is probably not limited to humans: The evidence from neurobiology and behavior by Baars (2005), and Affective consciousness: Core emotional feelings in animals and humans by Panksepp (2005). There are many good articles and books on the topic that I am not covering here, so feel free to point out what might be better/useful sources in the comments if you think I’ve missed something important.

In any case, let’s dive right in!

We have to start out assuming that the question of consciousness in non-human animals is worth investigating (eg. that my last post in the series contained at least one valid argument – I might be pushing my luck, but bear with me!) Where do we start?

The first thing to do is to operationalize consciousness. We have to determine how we will identify consciousness in non-human animals, if it exists. The classic way of studying consciousness in humans is through “accurate report”, which Edelman and Seth (2009) define as “a first-person account of what an individual is experiencing, made without the attempt to mislead.” Assuming that you believe that other humans are actually conscious (which can be argued; I won’t get into that here, though,) this is as direct a way as any to study consciousness. It is, however, very difficult to do with animals, as we for the most part lack any reliable form of verbal communication with non-humans. Notable possible exceptions to this include parrots (like Alex the Grey Parrot, who learned language well enough to pretty unambiguously demonstrate cognitive capacities such as numerical representation and the ability to categorize objects) and some chimpanzees who have been taught to use simple language (for example, Washoe, who was taught to use American Sign Language to communicate with her keepers.) Despite these exceptions, linguistic reports remain a rare and difficult-to-use tool for studying consciousness in animals.

One way of working around the inability of most animals to use language (and our inability to interpret the other ways they might be projecting information) is to allow the animals to report on their experience through some sort of trained response, such as by pressing a lever, pushing a button, or another physical activity. For example, Baars (2005) describes a study (Cowey and Stoerig, 1995) in which Macaques were trained to touch a screen where a target stimulus appeared, and then also to indicate (by pressing a button) whether they had perceived any stimulus on the screen (known as a “signal-detection task”, this is a pretty standard way to determine whether an intact animal can sense something.) After damaging parts of the cortex that process visual information in these monkeys, the experimenters found that they continued to point to the correct spot, but they not longer reported seeing a stimulus when the stimulus was in a certain part of the visual field. This parallels a phenomenon known as “blindsight” in humans, where a subject will claim not to perceive anything in a part of the visual field but will otherwise show basically normal behavioral responses to objects in that portion of the visual field. By training the monkeys in this study to report on their experience, the authors of this study were able to show that their awareness of their sensory world is separable from the at least some of the basic functionality of their sensory world, arguing that they have some sort of conscious perception of the world on top of the ability to make motor responses to sensory stimuli. By providing a way for animals to make “commentary” on their experience, Baars claims, methods like this provide a method of studying consciousness that is functionally equivalent to the method of accurate report in humans.

In some cases, animals do not need to be trained to show behavioral evidence of complex cognitive processes, which suggest (but importantly do not prove) the existence of consciousness. For example, as part of their arguments for the possibility of consciousness in birds, Edelman and Seth (2009) cite observations of birds exhibiting object constancy (which is the ability to attend to an object even though it leaves the visual field, such as when it is hidden behind another object – for example, peek-a-boo is fun because young babies do not have object constancy, and so they act as if you disappear when you are hidden from sight,) using and modifying tools, and changing their behavior based on their perceptions of being watched by other birds. They argue that these behaviors show that birds have a working memory and spatial cognition as well as “the ability to make sophisticated discriminations and to plan behaviors before executing them.”

Other behavioral experiments get at the question of whether animals have “selfhood” – that is, do animals have a sense of identity? Such a distinction between self and other is considered key to the sort of “higher-order” consciousness that humans have. The most classical method of doing this in humans and apes is by testing to see if they can recognize themselves in a mirror. This ability is rather straightforwardly called Mirror Self-Recognition (or MSR.) It has been used on many animals, and some that appear to have the ability to recognize themselves include dolphins, chimpanzees, gorillas, and (in one of my new personal favorite behavioral studies by Plotnik et al., 2006) elephants.

If you’re like me, you’re a bit troubled right now. These behavioral methods fall short of actually addressing consciousness per se, and they would never fly as an argument for consciousness in animals in and of themselves (actually, the results with macaques are a veritable one-hit KO in this argument, but only because they involve a species so closely related to humans – arguments from analogy to more distant evolutionary relatives require correspondingly more evidence to make.) Behavioral experiments do not solve the problem of identifying the internal states of animals, which is what we mean when we say “consciousness.” In a particularly lucid explanation of how this problem might be solved despite the shortcomings of behavioral evidence to inform us about internal states, Panksepp (2005) argues for a “psycho-neuro-ethological triangulation” strategy to address the problem of animal consciousness. According to this strategy, we should use neurological processes (some well-studied ones are the mobilization or production of neuroactive chemicals in the body and changes in EEG patterns) as a link between the behaviors we know to be associated with conscious states in humans (in his argument, emotional states in particular) and analogous behaviors in animals. For example, we know that humans feel pain when they are burned by a hot stove (the “psycho-” component of the strategy), and they then withdrawal from the stove and attend to the site of injury. If we watch a rat touch its paw to a hot piece of metal and get burned, we can observe the same sort of reaction (the “ethological” component of the strategy.) Finally, we can attempt to identify neural processes in the rat that correspond with this behavioral reaction in the rat and in humans, as well as neural processes that correspond specifically with the perception of the event (in this case, pain) in humans. If we find that homologous neural processes and behaviors occur in both cases, we have a good case for suggesting that analogous subjective experiences also occur.

In apparent agreement with this idea, both Baars (2005) and Edelman and Seth (2009) make a case for the identification of consciousness in non-humans through the study of neural processes that resemble those associated with human consciousness. The latter authors, in their argument for the possibility of consciousness in birds, identify the presence of human-like (or conscious-like) EEG patterns in birds and the presence of a neural circuit analogous to the thalamocortical circuit of humans (which has been shown through studies of brain-damaged patients and neuroimaging studies to be closely associated with consciousness) as evidence supporting the interpretation of bird behavior as indicative of consciousness. Baars argues that the apparent evolution of these brain structures suggests that consciousness is universal at least among all mammals. Because conscious states and phenomena (for example, wakefulness, REM sleep, and sensory perceptions) are modulated by brainstem structures and “seated in” the thalamocortical circuit, structures which have not undergone much overall structure change throughout mammalian evolution, they are likely to be conserved across all mammals. This is what he claims – I regrettably do not have the expertise in paleobiology or comparative anatomy to agree with or dispute his claims about brain evolution, but they sound like they could be disputed.

In essence, the argument for consciousness in animals remains an argument by analogy from the easily acceptable existence of consciousness in humans. It uses both behavioral and neural evidence to build this case. Critically, though, it makes use of comparative neuroscience to support the existence of consciousness in non-human vertebrates. Remember, though, that non-human mammals and birds are relatively closely related to people, and so their neuroanatomy is (arguably) suitably homologous to human neuroanatomy to make such an argument. What can we make of this line of inquiry when we try to apply it to an animal that is, evolutionarily speaking, much more distantly related to humans – say, an octopus?

Tune in next time to find out!

(For those who are interested in the topic, the journal Consciousness and Cognition put out an issue dedicated to animal consciousness in 2005. It’s very worth checking out.)

BAARS, B. (2005). Subjective experience is probably not limited to humans: The evidence from neurobiology and behavior Consciousness and Cognition, 14 (1), 7-21 DOI: 10.1016/j.concog.2004.11.002

Edelman, D., & Seth, A. (2009). Animal consciousness: a synthetic approach Trends in Neurosciences, 32 (9), 476-484 DOI: 10.1016/j.tins.2009.05.008

PANKSEPP, J. (2005). Affective consciousness: Core emotional feelings in animals and humans Consciousness and Cognition, 14 (1), 30-80 DOI: 10.1016/j.concog.2004.10.004

Plotnik JM, de Waal FB, & Reiss D (2006). Self-recognition in an Asian elephant. Proceedings of the National Academy of Sciences of the United States of America, 103 (45), 17053-7 PMID: 17075063

Cowey, A., & Stoerig, P. (1995). Blindsight in monkeys Nature, 373 (6511), 247-249 DOI: 10.1038/373247a0

         I was recently pointed to this article on “octopus intelligence”.  I like the article (which features quotes from such cephalopod research all-stars as Roger Hanlon and Jennifer Mather,) although I am a bit let down by the brief, incomplete explanation that is given to the various “intellectual” abilities of the octopus such as “problem solving” and “play”.  Both of these behaviors are difficult to define precisely, and are often understood in vertebrates by analogy to human experience.  For example, one of the criteria that is used to define play in animals (as stated in Kuba et al. 2003, a study on play-like behavior in octopuses) is that it is “spontaneous and pleasurable (‘done for its own sake’)”.  This is one of the central features of play – that it appears to serve no other immediate purpose than to entertain or occupy the animal expressing the behavior.  I take some issue with the use of the term “play
 to describe octopus behavior, at the very least because the implications of play-like behavior in the octopus are not very well studied yet.  It’s much harder to determine the motivational significance of an activity in an octopus than it is in, say, a rat.  This is because we know the brain and behavior of the rat much more thoroughly than we know those of octopuses, and since they are structurally similar to ours we can relatively easily design valid measures of motivation in rats.  In contrast to the vast (though still incomplete) neurological and behavioral description of pleasurable and aversive states in the rat that we have generated, we have only a very crude measure of the possible hedonic characteristics of an activity in the octopus; that is, we can assume that the octopus will do “pleasurable” things and will avoid aversive things, but we have little more to go on when we are talking about the motivation of an octopus.  Because of this limitation, I think that it may be too early to say for sure what processes play-like behaviors in the octopus actually represent, and so the touting of play as evidence of the impressive mental powers of the octopus also seems premature.

         Whoa, now!  Before I go making assertions like this, I should look at the research, right?  Good call.  Let’s see what the vast scientific library that is the internet can teach us about the play-like behavior of octopuses.

         I’ll focus on Kuba et al. (2006), a recent study that was done to examine putative play behavior in O. vulgaris.  In this study, the authors exposed octopuses to stimuli made out of Lego blocks for half an hour at a time repeatedly over a period of 7 days and scored the octopuses reactions to the objects.  The authors’ scoring system is illustrated below (this if Figure 1 from the paper.)

         As you can see, level 3 (which the authors describe as “play-like”) and level 4 (which the authors call “play”) involve repeatedly manipulating non-food objects in complex, non-stereotyped ways for a significant amount of time.  Out of 14 (wild-caught) subjects, object manipulation that was scored at level 3 was observed in 9 subjects, and object manipulation that was scored at level 4 was observed in one subject.  There was no difference of age or hunger state in this behavior (young and old octopuses showed the same sorts of behavior, as did hungry and sated octopuses.)  Play-like behaviors tended to occur after several days of presentation of the stimulus, suggesting that this was not merely exploratory behavior, which appeared to decrease during the first few days of exposure (as the octopuses presumably got used to the presence of the stimuli in their tanks.)

         By this point, I tentatively buy the characterization of these behaviors as “play” – they don’t appear to serve any purpose for the octopus, who is clearly not simply confusing the objects with food.  They are exhibited after the octopus has presumably had ample time to learn that they do not represent a threat.  The behaviors do not appear to clearly belong to any other class of behavior (except perhaps tactile exploratory behavior.)  As I said before, however, using the existence of these behaviors to argue for the intelligence of the octopus seems premature to me.  For one, the significance of these behaviors in the wild is not well understood – they must confer some survival utility, but they do not appear to be disproportionately expressed in young, rapidly developing octopuses as they are in mammalian young, and so are unlikely to contribute to neurodevelopment in the same way that play in mammals (especially social mammals) is thought to.  We know that play in social mammals (like humans, some apes, and rats) serves a variety of functions in development – to establish dominance hierarchies, to develop skills for living within social organizations, to learn hunting and food-gathering behaviors, to help develop motor coordination, etc.  We have comparatively little sense of the importance of play in the life of an octopus, and so it is hard to know what play-like behavior means in the context of octopus cognition.

         Because we know that play is very important to the cognitive function of mammals I mentioned previously (more properly, we know that disrupting play behavior causes deficits in behaviors that depend on play to develop,) we can claim that play is part of a group of behaviors that make manifest the intelligence of these animals.  Without knowing what play-like behavior does for an octopus, it’s hard to say whether it implies an analogous intelligence in these animals.  It might be explained in many cases as a simple extension of exploratory behavior.  As a foraging predator, it makes sense that O. vulgaris would be served well by repeated, thorough explorations of the same object, which mobile and semi-mobile prey would presumably periodically be found on.  This behavior might be explained as part of a foraging strategy that is somewhat impervious to associative learning, and so violate the criteria that we use to classify a behavior as play all together.

         My discussion thus far has accepted the hypothesis that behavior classifiable as play occurs regularly in the octopus, and thus needs to be explained in terms of its adaptive utility to the animal.  Based on the previously summarized paper, however, clear play-like behavior in the octopus appears to be pretty rare.  On the 5th day of the experiment, when play-like behavior peaked, 444 interactions with the stimuli were observed.  Out of these, 13% qualified as level 2 (they involved manipulation beyond very basic exploration of the object with the arms,) 0.9% were scored as play-like, and a single observation (0.02% of the total observations) was scored as being definitively “play”.  I think this was a well-designed study, but the results don’t convince me that play (as defined by the authors) is terribly important in the lives of octopuses, and might just as well represent a rare, specific type of interac
tion that they have with unusual stimuli in a laboratory environment.

         I realize that I have been sort of hard on this study.  I don’t want to imply that octopuses are not remarkable animals that are capable of many things one wouldn’t expect from a mollusc.  I do think, however, that it pays to be very skeptical about the use of the terms “play” and “intelligence”.  Both of these are concepts that we understand primarily by analogy to our experience of them as humans.  We know that social play in vertebrates is indeed play (even the scientists among us) because we know what a play fight feels like, and understand intuitively how it differs from a real fight.  We can extend this to behaviors that we see in animals (with more or less accuracy, depending on the situation.)  We know what intelligence means (or we think we do) because we have expectations of how people should function, and we can draw analogies to other vertebrates who have the same sort of behavioral flexibility and environmental demands that we do.  One might dismiss this as unscientific, but we have pretty good evidence that the neural structures that are responsible for a variety of emotions and types of behaviors are conserved in some form across species (in mammals at least.)   Thus, we can be somewhat comfortable in our understanding of the role of play in a rat’s cognitive life because, at a pretty complex level of structure and function, they have essentially the same machinery in their head that we do.  It’s a bit less convincing to use the same anthropomorphic logic to justify associating what looks like play behavior in an octopus with the “intelligence” that we suspect goes along with play behavior in vertebrates.  This is because the existence of analogous neural substrates and their accompanying cognitive functions (emotions, hedonic value, etc.) is not clear.  It strikes me as somewhat mistaken that we would use psychological constructs that were created to describe human behavior such as “play” and “problem-solving” to describe cephalopod behavior, though we do it even when they appear to be a poor fit to the behavior in question.

         As Jennifer Mather points out in her quote in the Boston Globe article: “We’re smart and the octopus is smart, but octopus intelligence just can’t be related to our intelligence.”  This I have to agree with.  Just because we can call a behavior something that sounds familiar (in this case, “play”) doesn’t mean that we’ve explained it, even though it might appear this way.  I think that octopuses are fascinating and astounding creatures that exhibit very interesting behaviors; I’m just not quite convinced that they play.

Thanks for reading!

Kuba, M., Byrne, R., Meisel, D., & Mather, J. (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 DOI: 10.1037/0735-7036.120.3.184

M Kuba, D V Meisel, R A Byrne, U Griebel, & J A Mather (2003). Looking at Play in Octopus Vulgaris Coleoid cephalopods through time, 163-169

I recently got a request (thanks to arvindpillai at Fins to Feet) to do a post on the shoaling and predatory behavior of Humboldt squid, Dosidicus gigas (also known as the Jumbo squid, and by those who don’t know any better, the giant squid.)  I decided that this would be a good thing to do, because I hadn’t read much about the predatory behavior of D. gigas.  So I spent a week searching the literature for scientific studies on Humboldt squid predatory behavior, and guess what?  I still haven’t read much about it!

It turns out that there is very little known about the behavior of these squid.  The paucity of our ethological knowledge of them is shocking to me, given the disproportionate attention to this species in popular media.  I’ve seen at least one budding cephalopod enthusiast become intrigued by stories about this species to the extent of obsession, and it’s not hard to see why.  Somehow, these squid have gained a reputation as fierce predators that are so bloodthirsty as to be regularly deadly to humans.  As such, popular TV shows and news magazines have run numerous stories about them, usually finding one or two divers who have (presumably) had experience with these squids (or at least heard stories about them) to expound on just how ferocious and aggressive they are.  Invariably, some sensational quip (that is almost always unsupported by scientific literature because, well, that literature does not exist) is used to drive home just how scary these squid are:

“It has probing arms and tooth-lined tentacles, a raptor-like beak and an insatiable craving for flesh — any kind of flesh, even that of humans,” says Pete Thomas in “Warning lights of the sea“. 

Mike Bear, an otherwise anonymous diver from San Diego is quoted in this article as saying “I wouldn’t go into the water with them for the same reason I wouldn’t walk into a pride of lions on the Serengeti.” 

“The Humboldt squid is a voracious predator that will eat anything it can get its tentacles on,” says Kelly Benoit-Bird, an oceanographer, quoted by Mark Floyd in this piece.

With all the hubbub, these guys must be pretty dangerous, right?  The stuff of nightmares, even!  I mean, just look at this bloodthirsty monster!

This is the myth of the Humboldt squid: that they are first and foremost dangerous, indiscriminate killing machines.  This is, frustratingly, the first (and often only) piece of information that is repeated about them in any given article.  But what’s the real story?

Let’s put this in perspective by considering the case of sharks, another predatory ocean-dweller that has been sensationalized as being imminently dangerous to humans (remember “Jaws”?  It was pretty silly, but a lot of people took that era’s shark scares seriously.)  Fatal shark attacks on humans are documented somewhat regularly, and are discussed (albeit infrequently) in the scientific and medical literature (ie. this study on fatal shark attacks.)  I cannot find a single verifiable record of a fatal squid attack on a human in the medical literature (admittedly, I have only searched 3 online databases and Google scholar – I might be missing something.)  The closest thing I can find are fisherman’s accounts in popular media of other fisherman’s stories about hearing about people being killed by Humboldt squid.  Keeping in mind the D. gigas is a rather common animal, is fished for sport by casual fishermen, and is usually encountered in large groups (the commonly cited size is 1000-1200 animals per shoal, but I can’t find anything peer reviewed to support this,) it looks like these squid are all but harmless, given how often it is encountered by lay-people and how few (if any) fatal encounters there have been.

This is not to say that I don’t think it’s possible that a Humboldt might kill a human someday; they are clearly aggressive, as several documented, non-fatal “attacks” on humans show.  I have to say, though, that the media attention that is payed to them (which is probably the reason why so many people are “interested” in them) is really a nuisance.  By making inflated claims about a species that we have little behavioral research about, media outlets encourage people to accept hearsay and horror stories as if they were biological fact.  These stories also draw attention away from other squid species whose behavior is very well characterized (ie. L. Pelalei) which might be better used to teach the public basic information about cephalopods.  Finally, by attempting to catch people’s eye using gorey stories, such articles serve to blind people to really learning about these animals by focusing on how “bloodthirsty” and “horrifying” they are – an effect that can’t be any good for conservation effforts.  I recognize that most people want an entertaining story rather than a dissertation out of their media, but this obvious bias in popular media coverage on this particular variety of cephalopods just bugs me because it is so pervasive and one-sided.

Now that I’m done ranting and raving, and have hopefully convinced you that D. gigas might not be the single-minded killers that they are often portrayed to be, I’ll try to get at the facts (that is, our very limited scientific knowledge) of this species.  Most of the research that has been done on them has been about their interactions with predator and prey species and their movement through their habitat, rather than their ethology.  This is because they are an important species in the study of ocean ecology.  They can be caught regularly in relatively large numbers throughout their range with little risk of damaging populations – this is uncommon among large predators, which tend to be much more rare than those lower on the food chain.  They are also suitable to be tracked using remotely monitored tags (as per Markaida et al. 2005) which are difficult to attach to less robust cephalopod species.  As such, they are convenient and informative to study when trying to learn about how oceanic food chains work.

So, what do we know about their feeding habits?  For one, we know that, as Dr. Benoit-Bird was trying to point out, that Humboldts are active, generalist predators, eating (according to Nigmatullin et al.) all manner of prey including “cepepods, hyperiid amphipods, euphausiids, pelagic shrimps and red crabs… heteropod molluscs, squid, pelagic octopods and various fishes.”  The authors also note that D. gigas is commonly cannibalistic, a facet of their predation that has probably contributed to their mythological status.  They are especially cannibalistic during squid jigging sessions, when they are excited by bright lights and surrounded by their injured conspecifics.  They feed near the surface mostly during the night, especially at dus
k and dawn, and spend their days deeper in the water column (200-400m deep), as was shown by a radio tracking study by Gilly et al. in 2006.  They can vary their diet depending on changes in their environment, showing an adaptability that no doubt contributes to their great abundance (Markaid and Sosa-Nishizaki, 2002).  Interestingly, recent ecological research has shown that their range has recently expanded from its historical locus in the equatorial Pacific ocean off of Central and South America to extend to the Pacific Northwest (as described by Cosgrove and Sendal, 2005, Zeidberg and Robison, 2007, and Field et al., 2007), possibly due to their unique ability to deal with hypoxic conditions that other predatory species cannot.   The squid can retreat into deep water with very little oxygen in between daily trips to feed at the surface, and thus avoid predation by other species such as Mako sharks (Vetter et al, 2008)..  On an unrelated note, if I were a squid researcher named Zeidberg, I’d just go ahead and change it to “Zoidberg”.  It’s too perfect.

There is dissappointingly little to say about the shoaling and predatory behavior of D. gigas.  If there are any glaring omissions in my coverage of the topic, please let me know; however, I think I found most of what’s in the scientific literature.  Basically, we know that they form large shoals, and that they are generalist predators.  More detailed information than that on the behavior of this species will have to wait for a new generation of adventurous ethologists.  Until then, I’ll be turning back to those species of cephalopod about which we have enough information to draw useful conclusions about behavior.  Perhaps someday the sort of experiments that have been done in smaller, more easily handled species will be done in D. gigas, but until that happens, I will probably stay mostly silent about them in favor of covering studies on less glamorous species in detail.

Please excuse me if it seems like I’ve rained on the proverbial parade.  Excuse me also for not getting into the methods of the studies that I’ve cited.  I encourage you to peruse them, but I opted to cover a greater area of research superficially rather than getting in depth about any specific finding in this post, so that I could adequately sum up the state of scientific knowledge of the Humboldt squid.  To lighten the mood, I’ll leave you with one more quote about the Humboldtl, by the realtively famous undersea cameraman, Scott Cassell, who has spent much of his professional career filming these squid (including a documentary titled “Humboldt: the Man-Eating Squid”) and is quoted in this piece by Tim Zimmermann:  “They are one of the most beautiful creatures, and they just happen to be lethal… There is no life form on this planet more alien than a Humboldt squid.”  I guess I didn’t realize that any life form on this planet was “alien”, given that they all evolved here.  Oh well – what do I know?

Thanks for reading!

Gilly, W., Markaida, U., Baxter, C., Block, B., Boustany, A., Zeidberg, L., Reisenbichler, K., Robison, B., Bazzino, G., & Salinas, C. (2006). Vertical and horizontal migrations by the jumbo squid Dosidicus gigas revealed by electronic tagging Marine Ecology Progress Series, 324, 1-17 DOI: 10.3354/meps324001

JOHN C. FIELD, KEN BALTZ, A. JASON PHILLIPS, & WILLIAM A. WALKER (2007). RANGE EXPANSION AND TROPHIC INTERACTIONS OF THE JUMBO SQUID,
DOSIDICUS GIGAS, IN THE CALIFORNIA CURRENT CalCOFI Rep., 48 : http://swfsc.noaa.gov/publications/FED/00859.pdf

James A. Cosgrove, & Kelly A. Sendall (2005). First Records of Dosidicus gigas, the Humboldt Squid
in the Temperate North-eastern Pacific Archives of the British Columbia Royal Museum

Unai Markaida, Joshua J. C. Rosenthal, & William F. Gilly (2005). Tagging studies on the jumbo squid
(Dosidicus gigas) in the Gulf of California, Mexico Fisheriy Bulletin, 103, 219-226

Markaida, U., & Sosa-Nishizaki, O. (2003). Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico Journal of the Marine Biological Association of the UK, 83 (3), 507-522 DOI: 10.1017/S0025315403007434h

Nigmatullin, C. (2001). A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) Fisheries Research, 54 (1), 9-19 DOI: 10.1016/S0165-7836(01)00371-X

RUSS VETTER, SUZANNE KOHIN, ANTONELLA PRETI, SAM MCCLATCHIE AND HEIDI DEWAR (2008). PREDATORY INTERACTIONS AND NICHE OVERLAP BETWEEN MAKO SHARK,
ISURUS OXYRINCHUS, AND JUMBO SQUID, DOSIDICUS GIGAS, IN THE CALIFORNIA CURRENT CalCOFI Rep., 49

Zeidberg LD, & Robison BH (2007). Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proceedings of the National Academy of Sciences of the United States of America, 104 (31), 12948-50 PMID: 17646649

Byard RW, Gilbert JD, & Brown K (2000). Pathologic features of fatal shark attacks. The American journal of forensic medicine and pathology : official publication of the National Association of Medical Examiners, 21 (3), 225-9 PMID: 10990281

I know these citations are sloppy – for some reason, I’m having some trouble working with the ResearchBlogging citation generator.  I promise I’ll fix it before next time.

Having finished the last post with a short discussion of hunting/foraging behavior in the octopus, I figured I should do a lighter post with some fun video examples of cephalopod predatory behavior.

[youtube=http://www.youtube.com/watch?v=D2oc6HQ3rHQ]
This is a short video of an octopus hunting (I don’t know the species) by For the Sea Productions.  The octopus catches a fish, apparently by spreading its web and feeling around.  There’s some great color-changing behavior here, too.  It’s hard to know how typical this behavior is, though, as it’s obviously influenced by the presence of the person filming.

[youtube=http://www.youtube.com/watch?v=-hGfTy2faLo]
This is a clip from Deep Sea 3D (I think – I haven’t seen the IMAX film, but that’s what the caption says) showing a visually-provoked attack on a crab.  I believe that the octopus here is a Pacific giant octopus.

Let’s not leave out the other cephalopods!  In contrast to octopuses, cuttlefish are primarily visual predators, who shoot out two long tentacles (these are tentacles proper – they are distinct from arms, which octopuses also have) to grab their prey.

[youtube=http://www.youtube.com/watch?v=vSQrBayqcNA]
This video was made by the California Academy of Sciences, and shows some adorable cuttlefish attacking crabs.  I’m not sure what species they are.  Again, you can see dramatic color changes as the animals become aroused.

[youtube=http://www.youtube.com/watch?v=M7gLTlWCfzg]
This one, also by the CAS, shows a great slow-motion shot of the cuttlefish tentacular strike. 

I’ll end with one of my favorite videos of cephalopod predation:

[youtube=http://www.youtube.com/watch?v=mGMT99i00M4]
Notice how the octopus turns mostly white and spreads its arms when the cuttlefish (most likely Sepia apama, although I’m not sure) approaches.  This is called the deimatic display, and it’s a defensive behavior seen in adult octopuses.

I feel obligated to warn anyone reading this that when you search “octopus eating” or similar strings on youtube, you are much more likely to find videos of people eating octopuses than octopuses eating anything.  : (