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Feature

What is that Spider Thinking?

Despite their small size, some spiders are disquietingly intelligent.

Robert Jackson

Animal thinking, intelligent computers and similar topics have acquired a certain respectability in recent years, yet the notion of a thinking spider probably seems ludicrous to most people. We might concede that questions about thinking, intelligence and perhaps even consciousness are relevant with regard to some of the large-brained mammals, such as dolphins and chimpanzees, and perhaps, at least in science fiction, very sophisticated computers.

Conventional wisdom about spiders seems to be that these are basically eight-legged automatons, having behaviour ruled largely by instinct. A spider's brain would fit comfortably on a pin head and seems to vanish into insignificance when compared to the much larger brain of any mammal. A small brain means few neurones, and there would seem to be an elementary engineering problem working against the spider. With so few components, how could the spider's brain organize especially complex and flexible behaviour?

The humble spider has long been a favourite study animal in my laboratory at the University of Canterbury, and the practical advantages of using spiders are compelling. These are cooperative animals for experimental studies, compared to generally more temperamental birds and mammals, and the large numbers of spiders that can be maintained conveniently in the laboratory enable research based on sample sizes normally only dreamed about in bird and mammal studies. However, I have often heard that the trade-off in choosing a spider is that this limits the researcher to investigating primarily instinctive behaviour instead of "higher" processes such as cognition. Recent work on salticids, or jumping spiders, has forced me to revise my attitude towards spiders.

Complex Eyes, Complex Thought?

True to their name, jumping spiders can jump, but more importantly they see well. The eyes of other spiders lack the structural complexity required for acute vision, but we know, especially from the work of Michael Land at Sussex University in England and David Blest at the Australian National University, that salticids have unique, complex eyes with resolution abilities unparalleled in other animals of comparable size.

A simple key can be used to identify a salticid. When you see a spider, stare at it. If it stares back with large front eyes, it is a salticid. Otherwise, it must be something else. Because of those big eyes, many people find it easier to relate to a salticid than to other spiders. The feeling that eyes, even spider eyes, are the windows to the soul can be compelling, but scientists want objective knowledge of what goes on inside. Is there anything especially complex going on behind the salticid's eyes? To get a handle on this question, let's have a look at an unconventional salticid named Portia which lives in tropical regions of Africa, Asia and Australia.

Not surprisingly, most species of jumping spiders prey primarily on insects caught by actively hunting instead of by building webs. Having good vision, why should a salticid need a web? Portia, though, is an oddball that not only hunts out in the open but also builds a prey-catching web of its own, and also invades the webs of other spiders where it feeds on the other spider's eggs, on insects caught in the web, and on the other spider. On top of all this, Portia is unusual in appearance. In nature, it doesn't really look like a spider at all, or even an animal, but instead, like detritus in a web.

After entering the other spider's web, Portia does not simply stalk or chase down its victim, but instead sends vibratory signals across the silk. The victim spider may respond to these signals from Portia in a way that is indistinguishable from how it would respond to a small insect ensnared in the web, but when the duped spider gets close, Portia lunges out and catches it. A system in which a predator (here Portia) deceives its victim (here a web-building spider) by imitating a something of positive interest to the victim (in this example, a small insect ensnared in a web) is called "aggressive mimicry".

Portia makes its vibratory signals by manipulating, plucking and slapping the silk with any one or any combination of its eight legs and two palps. Each appendage can be moved in a great variety of different ways, and the movements of any one appendage, however complex, can be combined with different movements of any number of the other appendages. On top of all the signals made possible by legs and palps, Portia also makes signals by flicking its abdomen up and down, and abdomen movements can also be combined in various ways with virtually any of the appendage movements. The net effect is that Portia seems to have at its disposal virtually an unlimited array of different signals to use on the webs of other spiders.

In this game of deceit Portia can see its victim, but the victim, instead of relying on vision, has acute abilities to detect and discriminate between vibratory signals transmitted over the web's silk. Being able to make many different kinds of signals is important for Portia because how the other spider interprets web-borne vibrations appears to vary considerably between spider species. It may also vary with the sex, age, previous experience and feeding state of the spider. Yet Portia has been observed using aggressive mimicry against, and catching, just about every kind of web-building spider imaginable, as long as it is in a size range of from about 1/10th to two times Portia's size.

Strategy and Tactics

Being able to make so many different signals is one thing, but how does Portia derive from this repertoire the appropriate signal for each of its diverse victims? This question was the impetus for a research programme at the University of Canterbury, much of which was carried out in collaboration with Dr Stimson Wilcox from the State University of New York. We developed a computer-based system for recording and playing back signals on webs, which is rather like listening and talking to spiders in their own language.

From this work, which is still in progress, the key to Portia's success at victimizing so many different types of spiders appears to be an interplay of two basic ploys: 1) using specific pre-programmed signals when cues from some of its more common prey species are detected; and 2) adjusting signals to different prey species in a flexible fashion, as a consequence of feedback from the victims.

The first ploy, using pre-programmed tactics, is consistent with the popular portrayal of spiders as animals governed by instinct. Building a spider this way appears analogous to inserting separate instructions for different prey into a computer, but commonsense tells us there must be a limit set by the "disk size", i.e., the spider's brain size. Accordingly, we started out expecting to find only a few hardwired prey-specific tactics, but we keep finding more and more -- ten, twenty where it will end is unclear. Surely at some point the small brain of the spider must set limits on the expansion of repertoire size for instinctive behaviour, but where this point lies is far from obvious.

The second ploy, flexible derivation of signals by trial and error, is an unexpected style of behaviour for a spider, as it indicates that Portia solves problems. It figures out, by trial and error, what to do with different victims. Evidently, having a small brain does not limit Portia to pre-programmed tactics.

To illustrate the trial-and-error tactic, let us first look at what happens when Portia goes into the web of a species of web-building spider for which it does not have a pre-programmed tactic. Portia begins by presenting the resident spider with a kaleidoscope of different vibratory signals. When one of these signals elicits an appropriate response from the victim, Portia ceases to vary its signals and, instead, concentrates on producing the signal that worked. If Portia is more powerful than its intended victim, an appropriate response might be that the resident spider approaches as though Portia were a small insect in a web, but the appropriate response can be more subtle than this.

Aggressive mimicry for Portia is a dangerous way to make a living. When facing a large and powerful spider in a web, it would be foolhardy for Portia simply to pretend to be prey and provoke a full-scale predatory attack. Instead, in these instances, Portia appears to strive for fine control over the victim's behaviour. This may be by making signals that draw the victim in slowly. Alternatively, signals may keep the victim calm while Portia moves in slowly for the kill. Calming effects appear to be achieved by monotonous repetition of a habituating signal, as though Portia were putting its victim to sleep with a vibratory lullaby derived by trial and error.

Sometimes Portia manipulates its victim into a particular orientation before attacking. Interactions with pholcids, spiders with very long legs, illustrate this. The best way for Portia to catch a pholcid is to grab hold of its body without hitting a leg first, because once a leg is contacted, the pholcid defends itself and sometimes kills the Portia. However, by trial and error, Portia can coax the pholcid into a position from which a clear shot at the body is possible.

Even when Portia has a pre-programmed tactic for a spider species, trial and error may still be relevant. In fact, it often appears that the role of the pre-programmed signal is not so much to provide a solution, all by itself, for the problem of how to catch a particular spider but, instead, to get the predatory sequence off to a good start, after which Portia finishes the job by trial and error. The victim spider may, for instance, start approaching slowly, then lose interest, become distracted, or begin approaching too fast. When, for any reason, pre-programmed signals do not work, Portia switches to trial and error.

When using trial and error, Portia associates success with a particular signal and remembers to keep using it, which is at least a simple kind of learning. What may be more important is that Portia figures out how to catch the spider, and being able to figure things out must be at least close to what is meant by thinking. Is there any good reason not to call Portia a thinking animal?

There are other examples of flexibility in Portia's predatory strategy. For example, there is what we call the "smokescreen" tactic. We discovered this when trying to record Portia's signals in the field. One problem we had was that whenever the wind blew, movement of the web masked out just about any other signal going across the silk. However, we noticed that it was especially when the wind blew that Portia walked rapidly toward the spider in the web. Later, in laboratory experiments using fans to generate artificial wind we could control, we demonstrated that Portia deliberately chooses to approach its victim when a breeze opportunistically provides a vibratory "smokescreen" to hide behind.

Also, if the wind does not blow, Portia can make its own vibratory smokescreen. That is, while walking across the web, Portia can mask the faint vibrations it makes while stepping by adding large-scale vibrations that simulate a breeze. Portia is selective, using opportunistic and self-generated smokescreens against spiders, but not when stalking, for instance, insects caught in webs or the egg sacs of the other spider -- targets for which masking is irrelevant.

Although trial-and-error and smokescreen behaviour illustrate that Portia is flexible in behaviour, it may still be tempting to envisage Portia as being more or less machine-like in behaviour. After all, we can readily envisage building a mindless robot capable of trial-and-error and smokescreen behaviour. Perhaps only a "higher" animal with a big brain, such as a chimpanzee, can make up its mind and plan ahead, but we had better have another look at Portia.

A Sneaky Spider

For Dr Wilcox and myself, the wind was not the only problem in the field. Sometimes Portia would stop, look at a web, then turn and walk away. This used to happen especially in Queensland when working with Argiope appensa, a spider that builds orb webs on tree trunks. Although it would appear easy for Portia simply to walk straight from the tree into the web, A. appensa has this problem covered. Being exceedingly sensitive to anything foreign touching the web, A. appensa rarely gives Portia time to enter the web and start signalling. If A. appensa is sure the intruder is an insect prey, it attacks; otherwise, it uses a specialized defence called "pumping". When pumping, A. appensa rapidly flexes its legs over and over again, setting the web into motion and either driving or throwing Portia out of the web.

In the field, we eventually realized that our seemingly uncooperative Portia was walking up the tree trunk toward A. appensa, stopping, looking around, then going off in a different direction, only later to come out above the web. This was in rain forest, and there were usually vines and other vegetation near the tree. There might be a vine that extended out above the web, for example. After looking at the web, the vine and the neighbouring vegetation, Portia would move away, perhaps going to where the web was completely out of view, cross the vegetation, and come out on the vine above the web. Next, from above the web, Portia would drop on its own silk line alongside, but without touching, the web of the A. appensa. Then, when parallel with the spider in the web, Portia would swing in to make a kill.

We realized that Portia might be making deliberate detours to reach a point for a more effective attack on this special prey. Subsequently, with another collaborator, Michael Tarsitano, we got experimental evidence that Portia makes deliberate detours which are planned ahead. For example, if presented with a choice of two routes on artificial vegetation in the laboratory, only one of which leads to a prey spider, Portia consistently takes the appropriate path even when this means initially going away from the prey, going to where the prey is temporarily out of view, and going past where the inappropriate path begins.

It is tempting to say that an animal that plans ahead is making up its mind, which might be a metaphor for saying Portia is conscious in some sense. However, even if words such as "thinking", much less "consciousness", are legitimate in reference to a spider, this need not, and should not, imply that what we as people experience subjectively when we think and make conscious decisions has this precise subjective parallel in a spider.

Not so long ago, topics such as animal thinking and animal awareness were widely viewed by scientists as somehow disreputable, but now these topics are coming into fashion. However, recognizing the problem of anthropomorphism was one of the reasons these topics went out of fashion in the first place, and this problem has not simply gone away. Indeed, progress in the scientific study of animal thinking and consciousness probably depends on our ability to de-mystify these expressions and free them of their anthropomorphic baggage.

Alien Minds

If pressed, I would probably say that Portia thinks and even, perhaps, that it is conscious, but I am not especially interested in debating the point if this means worrying about definitions for these terms. Studying the mechanisms underlying complex behaviour is more interesting. I would like to know, for example, specific things about the processes by which different animals solve problems and behave flexibly.

It is tempting to call Portia the chimpanzee of the spider world but, of course, Portia is not really a chimpanzee, which may be one of the biggest advantages in using Portia as a study animal. Spiders have had a long evolutionary history separate from our own, and from that of chimpanzees, dolphins and other vertebrates. People react subjectively to spiders as somehow alien, whereas there tends to be more of an emotional bond to the dolphin and the chimpanzee. Perhaps there is no better way to de-mystify the topics of animal thinking and animal consciousness than to discuss them in reference to the more alien animal -- the spider.

Robert Jackson is senior lecturer in zoology at the University of Canterbury.