readings> do spiders have a mind?

Looking like a crusty flake of bark on the branch, Portia labiata, a thumbnail-sized jumping spider, stops to have a think. Portia is a spider that hunts other spiders – a risky business at the best of times.

Luckily Portia has brains. In fact it is the veritable Einstein of the arthropod world. Which is just as well as right now it has its beady eyes on Scytodes pallidus, a “spitting” spider that also specialises in hunting spiders – jumping spiders like Portia! And Scytodes has a secret weapon. From mouth glands it can squirt zig-zag jets of poison-coated silk that would snare Portia in a blink of an eye.

In evolutionary terms, it is like two high rolling gamblers about to shove all their chips on a single turn of a hand. Fortunately Scytodes has weak eyes. It is content to lurk in its silken lair, deep in the tangles of the forest floor of the Philippine island of Luzon, until some passer-by is fool enough to stumble across its web. Portia, on the other hand, has the most efficient eyes ever discovered in an animal.

Portia may be about the size of a fat raisin, with eyes no larger than sesame seeds, yet it has a visual acuity that beats a cat or a pigeon. The human eye is better, but only about five times better. So from a safe distance a foot or two away, Portia sits scanning Scytodes, looking to see if it is carrying an egg sac in its fangs.

This is how Scytodes protects its eggs. And to do any spitting, it has to drop them first. Spotting a Scytodes with eggs, Portia would simply mount a frontal assault. It would creep to the edge of the web, making use of its camouflage, and gently tickle the threads. By pretending to be a bumbling intruder, Portia would lure Scytodes into the open for the pounce.

However on this occasion Portia is out of luck. No eggs. Worse still, there is no easy way to execute plan B – to crawl around the web edge and jump Scytodes from behind. So perched on a branch, Portia begins to plot. For a good quarter hour it scans the surrounding undergrowth, it’s pin-head sized brain working out possible pathways across boulders and branches.

The retinas of its principle eyes have only about a thousand receptors compared to the 200 million or so of the human eyeball. But Portia can swivel these tiny eyes across the scene in systematic fashion, patiently building up an image point by point. Having rejected a few alternatives routes, Portia makes up its mind and disappears from sight. A couple of hours later, the silent assassin is back, dropping straight down on Scytodes from a convenient rock overhang on a silk dragline – looking like something out of the movie, Mission Impossible. Once again, Portia’s guile wins the day.

Back in the lab, the story has a different ending. “Oh, that wasn’t meant to happen!” cries Simon Pollard, a spider researcher at Canterbury University in Christchurch, New Zealand. A Portia specimen in its little plastic flask has just been chomped by the local White Tailed spider that was supposed to be its supper.

White Tails are yet another species of spider-eating spider. However they are all brawn, no brains. Many a New Zealand home is fumigated for fear of the painful nip of these sturdy hunters. “Well, I guess a bottle isn’t a very complex environment so Portia doesn’t really get the advantage of its greater intelligence,” says Pollard a little aggrieved.

It truly is a dog eat dog life for spiders it seems. Or araneophagic, to use the technical term. Yet the Portia family, which makes up about 15 of the 4,000 known jumping spider species, is fast becoming a celebrity in the field of animal cognition. The honey bee, with its intricate social behaviour and waggling dance telling of nectar-laden blooms, has long been considered a smart wee beastie.

But generally mind scientists have been dismissive of creepy crawlies. The nervous systems of invertebrates were supposed to be no more than a bundle of hardwired reflexes. Certainly you could not talk in terms of thinking, planning, trial and error learning, attention, states of expectation or – shudder – consciousness. Insects and spiders could never have anything approaching a mind. Yet Portia does stuff that just doesn’t fit with the idea that invertebrates function as blind automatons.

Undoubtedly many of Portia’s cognitive abilities are genetic. Laboratory tests carried out by Robert Jackson, chief of Canterbury’s spider unit, have shown that only Portia from the particular area where Scytodes is common can recognise the difference between an egg sac carrying and non-egg sac carrying specimen. And it is a visual skill they are born with. The same species of Portia trapped a few hundred miles away doesn’t show any evidence of seeing the egg sac.

But as Jackson points out, this just deepens the mystery. First there is the fact that such a specific mental behaviour as looking for an egg sac could be wired into a spider’s genome. And then there is the realisation that this is a population-specific, not species-specific, trait! It is a bit of locally acquired genetic knowledge. How does any simple hardwiring story account for that?

Watching Portia crouched in its flask, it is easy to understand why its exceptional abilities have been overlooked for so long. Ragged, hairy and drab, it wouldn’t attract a second glance in its jungle habitat when there are so many other, much more flashy and fiercesomely fanged, jumping spiders scuttling about. Even the fact that it is a spider-eating spider is not a big deal. Yet once researchers woke up to the fact that Portia had exceptional eye-sight and was unusually flexible in its behaviour, the surprises have just kept coming.

One of Portia’s principal skills is to be able to lure another spider out of its web. Portia will pluck out rhythms at the edge of a web to mimic a trapped insect or other intruder. In some cases it can recognise the resident spider and will know what rhythm use – a remarkable ability in itself. But Portia has the flexibility to try out various patterns in trial and error fashion. It can tickle the web lightly, strum it vigorously, bob up and down as if on a trampoline – whatever it takes to move the other spider into position for an attack.

Often the foe will be two to three times Portia’s size and the trick is to arouse its curiosity without provoking a full blooded rush. Portia will also take advantage of any kind of cover. If it is a windy day, or the resident spider is busy wrapping up a recent capture, Portia will time its advance to match.

Duane Harland, another researcher affiliated with the Canterbury University spider lab, says this web plucking reveals all sorts of cognitive skills that were thought to be beyond such a small creature. He contrasts Portia with other web invaders like the local bully, the White Tail.

“The White Tail can pluck, but only in a programmed, stereotyped, way. It doesn’t bother with tactics, or experimenting, or looking to see which way the other spider is facing. It just charges in and overpowers its prey with its size. Portia is a really weedy little spider and has to spend ages planning a careful attack. But its eyesight and trial and error approach means it can tackle any sort of web spider it comes across, even ones it has never met before in the history of its species,” says Harland.

While Portia’s deception skills are impressive, the real admiration is reserved for its ability to plot a path to its victim. For an instinctive animal, out of sight is supposed to be out of mind. But Portia can take several hours to get into the right spot, even if it means losing sight of its prey for long periods.

This capacity has been tested with mazes in the lab, both at Canterbury and at the University of Sussex. In a typical experiment, a choice of two paths is created with kinked coat hanger wire. The set-up simulates a pair of branches growing out of the forest floor and crossing over each other in a visually confusing way. Dangling at the end of each wire branch is an identical prey-holding dish. Into one is placed a dead spider (preserved and spray-coated to remove any odour cues). To make this bait jiggle attractively, it is jolted with a magnetic coil contraption.

A Portia that has been starved a few days is then released onto a platform in the middle of the maze – actually a tall wooden dowel that gives a view across the whole apparatus. To get to the dangling bait, the Portia has to work out which wire branch to take. The arrangement is such that once down on the ground, and even while climbing back across the wires, the spider is beneath the level of the dishes and so must rely on its memory of where it should be heading.

As a maze to be worked out from a single viewing – and with no previous experience of such mazes – this would be a tall order even for a rat or monkey. Yet more often than not, Portia could identify the right path. There was nothing quick about it. Portia would sit on top of the dowel for up to an hour, twisting to and fro as it appeared to track its eyes across the various possible routes.

Sometimes it couldn’t decide and would just give up. However, once it had a plan, it would clamber down and pick the correct wire, even if this meant at first heading back behind where it had been perched. And walking right past the other wire.

Harland says it seems that Portia can see where it has to get to in order to start its journey and ignore distractions along the way. This impression was strengthened by the fact that on trials where Portia made a wrong choice, it often gave up on reaching the first high bend of the wire – even though the bait was not yet in sight. It was as if Portia knew where it should be in the apparatus and could tell straight away when it had made a dumb mistake.

Crazy talk, obviously. There just ain’t room in Portia’s tiny head for anything approaching a plan, an expectation, or any other kind of inner life. The human brain has some 100 billion neurons, or brain cells, and even a mouse has around 70 million. Harland says no one has done a precise count on Portia but it is reckoned to have about 600,000 neurons, putting it midway between the quarter million of a housefly and the one million of a honey bee. Yet in the lab over the past few years, Portia has kept on surprising.

Recent experiments by Daiqin Li at the National University of Singapore have demonstrated selective attention and priming effects. The smell of a particular kind of prey not only puts Portia on the alert for that prey – Portia immediately finds it much easier to spot – but it also dulls Portia’s ability to detect other prey types.

Rather controversially, Li calls this the forming of a search image. Yet even if this mental priming is reduced to some thoroughly robotic explanation, such as an enhanced sensitivity of certain prey-recognising circuits and a matching damping of others, it still says that there is a general shift in the running state of Portia’s nervous system. Portia is responding in a globally cohesive fashion and is not just a loose bundle of automatic routines.

In another experiment to explore its ability to learn, Portia was stranded on an island in the middle of a water filled tray. The distance was far enough that Portia had to decide whether to leap as far as it could or just swim. On some trials, the experimenters would make waves to push Portia back. On others they would help wash Portia to the other side. Portia would remember what had happened on the first trial and either make the same choice again if it had been successful, or switch tactics if it had been frustrated. Again this seems a rather dynamic, unprogrammed, response for such a small brain.

So what do the researchers conclude? Does Portia have a mind, some inkling of an inner mental life? Or can every behaviour eventually be explained away in terms of simple cues and instinctive responses? Harland replies that what would be exciting would be if science could recognise some halfway position between the two conventional extremes of conscious and mindless behaviour.

Harland says Portia’s eyesight is the place to start. Jumping spiders already have excellent vision and Portia’s is ten times as good, making it sharper than most mammals. However being so small, there is a trade-off in that Portia can only focus its eyes on a tiny spot. It has to build up a picture of the world by scanning almost pixel by pixel across the visual scene. Whatever Portia ends up seeing, the information is accumulated slowly, as if peering through a keyhole, over many minutes. So there might be something a little like visual experience, but nothing like a full and “all at once” experience of a visual field. 

Harland feels that the serial nature of this scanning vision also makes it easier to imagine how prey recognition and other such decision processes could be controlled by some quite stereotyped genetic programs. When Portia is looking for an egg sac obscuring the face of Scytodes, it wouldn’t need to be representing the scene as a visual whole. Instead it could be checking a template, ticking off critical features in a sequence of fixations.

In such a case, the less the eye sees with each fixation, perhaps the better. The human brain has to cope with a flood of information. Much of the work lies in discovering what to ignore about any moment. So the laser-like focus of Portia’s eyes might do much of this filtering by default.

Harland hopes soon to use eye-tracking equipment to check this idea. The lessons learnt could help crack the problem of robot vision: “Being able to reverse engineer what Portia can do with just a few photocells and a few neurons would be huge,” he enthuses.

Yet while much of Portia’s mental abilities may reduce to the way its carefully designed eyes are coupled to largely reflexive motor patterns, Harland says there is still a disconcerting plasticity in its gene-encoded knowledge of the world. If one population of Portia can recognise an egg-carrying Scytodes but specimens from another region can’t, then this seems something quite new – a level of learning somewhere in-between the brain of an individual and the genome of a species.

The Canterbury researchers have found other examples of this population level learning. An Australian species of Portia shows regional variation in its ability to recognise the jumping spider, Jacksonoides queenslandicus. It is only those Portia which live in the same locality that know to freeze whenever Jacksonoides turns a hungry eye in their direction.

So either way, Portia looks set to stir debate. Perhaps some will say that creepy crawlies are a jump closer to being able to claim status as mental beings. Look into the eyes of a spider and who is to say it is not looking back? Yet even if it is still all merely instinct and hardwiring, genes are somehow much better at capturing locally-useful information than ever suspected. As Harland says, Portia just doesn’t fit anyone’s theories right at the moment.

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