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ethology

The webs of intelligence

Capacity for memorizing information enables spiders to perfect their instinctive hunting habits

EDUARDO CESARThe female orb-web spider (Nephilengys cruentata), with the male on its back: similar behaviors help to define kinshipEDUARDO CESAR

Indifferent to the girls running around in the garden, a 13-year-old boy observes the delicate movements of a spider in a web built amongst the leaves of a bush. He is so engrossed that he does not even let himself be perturbed by the intense heat of the summer in Alexandria, a city in the north of Egypt, on the Mediterranean coast. For the sake of curiosity, the teenager catches a grasshopper and puts it onto the web, and then picks up his notebook and jots down in detail what the spider does with the insect that is turning itself into its meal. It was that afternoon that a passion was born that was to remain latent for almost two decades before its realization: the Egyptian boy of those days, César Ades, today 60 years old, turned into one of the greatest Brazilian authorities in ethology, or the study of animal behavior.The desire to understand animal behavior led him to prove, by means of experiments in the laboratory, that spiders are capable of learning and of perfecting basic instincts, like those linked to hunting and building webs, usually seen as an innate and unchangeable skill.

“Certainly, instincts work like a sort of pre-programming of the mind”, explains Ades, a director of the Psychology Institute of the University of São Paulo (USP). “But there are also windows for learning in this pre-program.” According to him, the capacity for learning may perhaps be a particular characteristic of the nervous system, which, by means of experience, makes it possible to adapt to the challenges of the environment. Ades is not alone in advocating this idea, which can even alter the way one thinks of human intelligence, besides attesting to the flexibility of the instincts of – at least – spiders. If these eight-legged animals are really capable of learning, they may perhaps stop being just repugnant animals that awaken fear and terror. It may be that not everyone will be able to set themselves free of prejudices and recognize the delicacy and elegance of a trapdoor spider or of a black widow spider, but maybe it will be possible to think twice before squashing the daring one that has comeout from behind the curtain.

Miniature lions
In a line of work that runs parallel to Ades, American biologist Robert Jackson, from the University of Canterbury, in New Zealand, arrived at other discoveries about the spiders capacity for learning. Jackson investigated the hunting habits of a group of fly-catching tropical spiders of the Portia genus, common in Africa and in Oceania. These spiders, which rarely reach 1 centimeter in length, are cleverer than their size makes one suppose. With four pairs of eyes, larger and more efficient than those of other species of spiders, these fly-catchers gather some very precise visual information on the environment and draw up strategies for hunting that are worthy of a lion, a hunter par excellence. They are also skillful to the point of altering their hunting strategy when faced by prey that offers them greater danger – for example, a more aggressive spider, like the spitting spider of the Scytodes genus.

Instead of attacking the spitting spider in a straight line, which could be fatal, the Portia retreats, goes round, and then takes its prey by assault from behind, like a general faced by a more powerful army. The most recent results of Jackson’s research attracted the attention of about 450 specialists, who in August took part in the International Ethology Conference, held in Florianópolis, Santa Catarina.The research of Ades and Jackson complement each other. And they make it clear: spiders are capable of memorizing information and of learning from experiences they have lived through. There is hardly going to be any success in training a spider to press a bar to get a drop of water, as rats in the laboratory do. Learning by spiders – and by any animal, in short – seems to occur within certain limits, determined by the number and organization of the nerve cells (neurons). The nervous system of spiders has only a few thousand cells, not enough to cover a pinhead, while the human being boasts some 100 billion neurons.

Experiments about the capacity of spiders for learning clash with a common view, even in scientific circles, which makes a radical separation into watertight categories, of what is innate or instinctive from the fruits of learning. One clear example of instinct is the behavior of the queen of the leafcutter ants called “içá”. After flying around and mating, the içá pulls its wings off , with a movement of its feet, and digs an underground nest: the act of pulling the wings off occurs at the appropriate movement, without any need for training. At the other extreme, flexible behaviors appear, like the chimpanzees of the Ivory Coast, in Africa, cracking nuts: they take years to acquire – perhaps by imitation – the ability to hold the nut with one hand while striking it with the other, using a stone or a stick as a hammer. “This form of assessing behavior regarded instinct as a sort of pre-program, unalterable and isolated from the capacity for learning”, Ades explains.

Inherited habits
This simplistic interpretation bothered the researcher, and he found in spiders a model capable of demonstrating the existence of flexibility in supposedly fixed behaviors. Born predators, they have always been regarded as essentially instinctive. But one can now think that instinctive patterns are not always so rigid as used to be imagined, since the spiders like the ones that make their webs amongst the roses in the garden or stay unnoticed in the nooks of the walls are capable of modifying their behavior.Even so, spiders do not forget the past of their own species. At the same time that they are proving to be apt at modifying old habits, even today they seem to maintain some of the behaviors of their most distant ancestors. Even without any predators nearby, some species do not fail to construct a protection of silk around their eggs. It was biologist Hilton Ferreira Japyassú, a former pupil of Ades and nowadays one of his collaborators, who discovered the limits to the flexibility of some of some of the spiders behaviors. Besides these discoveries, the work resulted in the development of EthoSeq, a program that makes possible an evolutionary analysis of behavioral acts organized in a sequence – it not only works with spiders, but also with cats and birds.

In the Arthropod Laboratory at the Butantan Institute, Japyassú studied the hunting behavior of another spider found in the garden, the orb-web spider, or Nephilengys cruentata, which has long legs of up to 2 centimeters and a voluminous orange and black striped abdomen, three times larger than its trunk and head. He also assessed the reproductive habits of another species that is common in the south of Brazil, the brown spider (Loxosceles gaucho) – with its brown body only 1 centimeter in length, it is much smaller than the orb-web spider, but it produces a venom that is far more potent, lethal even for human beings.

Analyzing these habits provided the biologist from the Butantan data that was sufficiently robust for stating that similarities or differences in behavior reveal the degree of kinship between spiders. For this reason, more or less similar forms of hunting or taking care of offspring can be useful for defining with greater precision the link – not always clear – between the 44,000 species of spiders now identified. In addition, they reveal some very primitive habits, such as constructing a protection of silk fibers for the eggs, shared by some species since the first spiders arose, 400 million years ago. “It is the first time that it is shown that the behavior of present-day species can keep such strong signs of very ancient habits”, Japyassú comments, with the endorsement of the magazines, Behavior and Journal of Arachnology, which in the last two years have published the most recent results of his work.

Reconstructed history
By showing that spiders that descend from a common ancestor share – at least in part – a given habit, the researcher from the Butantan reinforces the experimental foundation of an idea put forward in the decade of 1930 by Konrad Lorenz, an Austrian physician and zoologist who began the study of animal behavior, or ethology. Recognized with the Nobel Prize in 1973 for revealing animals, individual and social behavioral patterns, Lorenz had said , at the beginning of last century, that some of these habits – such as scratching their heads, like dogs – could be transmitted from one generation to another. It was not such an original idea. The English naturalist Charles Darwin, the author of the Theory of Evolution, had already called attention to the possibility of behavior being inherited in his book The Expression of the Emotions in Man and Animals, of 1872. “Up until now, discussions have been theoretic only”, observes Japyassú, “and there was a lack of empirical data to show whether behavior could infact reveal kinship between species.”

In a broader fashion, the works of the biologist from the Butantan Institute reveal that the small units that make up behavior, or the actions, make it possible to reconstruct the evolutionary history of distant groups of spiders, as he stated in an article published in July in the Journal of Arachnology. They also prove that even more complex behaviors – made up of a sequence of simple actions and therefore more susceptible to the influence of the environment – keep traces of kinship between species, as verified in an article published in the April 2002 issue of Behavior. Accordingly, they create the possibility of adopting behavior as an auxiliary tool in classification and in the reconstruction of the evolutionary history of other groups of animals, such as birds, or even mammals – a complex scientific task, which began in the 18th century with Swedish botanist Linnaeus (Carl von Linné), using the study of the biological forms and structures (morphology), which in the last decade has won the support of genetics. As even so there is not a solution for everything, new methods that assist in the classification of living beings are always welcome.

Japyassú decided to dedicate himself to studying the behavior of spiders after listening to a lecture by Ades, who has the reputation of packing the auditorium and of speaking passionately about his work. Ades, in turn, felt engrossed by spiders when he read La Vie des Araignées (The Life of Spiders), by French naturalist Jean-Henri Fabre, a present he was given months before his vacations in Alexandria from a friend in his native city, Cairo, who was not very fond of the subject. His interest for the world of the arachnids only reappeared much later, while carrying out his postgraduate studies in psychology at USP, with another present: a box with an elegant black-and-yellow garden spider (Argiope argentata), offered by Walter Hugo de Andrade Cunha, one of the pioneers in ethology in Brazil. With a brown belly with a yellow stripe, this spider is distinguished for having a shiny silver back, a feature that has earned it the name of silver argiope. Common all over Brazil, this garden spider builds its web in bushes exposed to the sun, close to the ground. It remains immobile in the middle of the web, until an insect gets caught in the viscous threads – this is the moment that the spider attacks with impressive speed. This was the species that brought Ades the most gratifying results in the following years.

The suspicion that a memory factor could be at work in the behavior of the garden spider arose with the observation that it would behave differently when it was catching insects quickly, one after the other. Founded on the studies by German ethologist Hans Peters, one of the first to talk about memory in spiders, back in the 30s, Ades thought: if it were absolutely instinctive and independent of experience, the hunting behavior ought to repeat itself, always in the same way, with every insect caught. But it was not like that. According to the experiments, as soon as an insect fell onto its web, the spider would leave the center in the direction of its prey and bite it, releasing a dose of the venom that would paralyze it. Sometimes, the spider would immobilize its prey, wrapping it in silk threads, before carrying it to the center of the web, where it would make it fast with a thread of silk. And then it would slowly devour it, soaking it in digestive juices.

Lost prey
The experiments that ensued made clear the importance of the thread that bound the prey to the web: with it, the spider would not lose the first prey if others fell onto the web. If Ades put another insect on the web during this meal, the Argiope would perceive the arrival of the prey, by the unexpected vibration, and would immediately run in its direction. But, this time, it would not take the captured fly to the center: it would leave it rolled up at the edge of the web, only to look for it later, after finishing the interrupted meal.

Other studies show that the capacity for recovering a stored prey – even if it were immobile and incapable of generating any signs that might indicate its presence – depends on the memory. For example, Dutch ethologist Nicholaas Tinbergen had already found, some 50 years ago, that foxes are capable of burying seagulls eggs and of recovering them days later, guided only by their recollections. To confirm that the same was happening with the spiders, the researcher removed the fly warehoused at the center or at the edge of the web. And he got a surprise: even after an interval of up to 15 minutes, the spider would look for the prey that ought to be there and was not any more: it would shake the threads, go round and round the middle of the web, then widen the search to the edges. Until giving up.

But there were two kinds of theft, which would generate different reactions. If it lost a prey held at the center of the web, the Argiope would concentrate its search right there, as if it knew that the food had originally been there. When a prey disappeared from the edges, its movements would take it round the edge of the web. It is not so obvious as all that: if it were not capable of memorizing where it had put the prey, the animal would not show this coherence and would look for the lost food, indistinctly, all over the web. A detail: the spider would spend more time looking for the larger preys. Evidently, to keep information in the memory facilitates survival. “A spider that remembers”, says Ades, “gets food more quickly and in greater quantity than another, which only reacts to present stimuli, without any notion of past facts.”Could spiders also learn to build their own webs? With this question, Ades was meddling with a taboo: even the most acclaimed reference books on arachnology stated that the construction of the web was independent of experience – it was a perfect model of instinct. To verify a possible effect of training, the researcher and his then pupil Selene da Cunha Nogueira put silver argiopes in horizontal boxes.

Used to building their webs on a plane close to the vertical, they found themselves under unprecedented conditions. To start with, they were totally lost: they would spin the threads at random and produce a chaotic web. Only after a few days did they begin to weave more orderly structures, with the spokes converging and attempted spirals. Weeks later, they were already succeeding in building complete and functional webs on the horizontal. The experiment was repeated with the same spiders after they had had the opportunity of constructing the web on the vertical. Afterwards, forced to work on the horizontal, they were more agile than in the previous attempt, an indication that they had learned to deal with the space available.

Eight-eyed cats
In New Zealand, Jackson is investigating the hunting habits of tropical spiders, particularly those belonging to the Portia genus. Known as fly-catchers, these spiders are veritable eight-eyed cats, on account of their appearance and sharp-sightedness. Up to 8 millimeters in length, these spiders live in trees and on walls and do not build webs. Instead of this, they invade the webs of others and feed on other spiders. In one of his first experiments, published in 1993 in the scientific magazine Behavior, Jackson analyzed how three species of Portia – P. fimbriata, from Australia; P. labiata, from Sri Lanka; and P. schultz, from Kenya – acted in catching some of their natural preys: the Philoponella variabilis spider, which reaches 4 millimeters in length when adult, and one other a bit bigger, the Stegodyphus sarasinorum, of 1 centimeter.

As soon as it reaches the web of its victim, the fly-catcher stops, facing the other spider. Next, it begins a series of movements with the body – it lowers and raises the abdomen or pushes the silk threads, simulating the agitation of some insect stuck to the web. As soon as it perceives that one of the almost 120 distinct movements has brought results and called the attention of the owner of the web, the fly-catcher starts repeating only the successful steps, until its ingenuous prey gets near enough to receive a deadly attack. But the Portia was to reveal itself even more inventive when faced by aggressive preys, like the spitting spider (Scytodes sp). With its front legs longer than the others, one of the characteristics that marks this tropical spider, with its bodies with patches of black, brown and yellow, is that it launches onto its prey a sticky saliva that immobilizes it.

Jackson’s team put four species of Portia up against the spitting spiders found in the Philippines. One of these species of fly-catchers – P. labiata, also originating in the Philippines – would come out better in the hunt, according to an article published in 1998, in the Journal of Insect Behavior. Although it was born in the laboratory, without any previous contact with the spitting spiders, the Philippine fly-catchers revealed themselves to be veritable strategists. Instead of calling the attention of their preys with movements in the web and next attacking them front on, the P. labiata would act differently: faced by an advancing spitting spider, it would retreat and go around the web, to attack from behind. In another test, Jackson found that the fly-catchers would more frequently attack the spitting spiders head on when the latter were holding eggs in their jaws and were therefore not able to launch the sticky saliva – a clear perfecting of an instinctive habit.

But not everything in instinctive behavior is altered by learning. In recent work, César Ades and two of his pupils, Mayra Dias Candido and Fausto Assumpção Fernandes, tried to ascertain whether the silver argiope would spend less time looking for its prey, if it were to lose one after the other. Up to this moment, the results indicate that the spiders do not desist from catching and warehousing their prey. Moreover, they always spent the same time in the search, even with a useless result, as the researchers have ten times running removed the prey that was being held. Ades realized that his pupils felt frustrated with this result, but he himself was not disheartened and consoled them with a positive point of view, reminding them that instinct could not be entirely molded, and that both flexibility and rigidity are equally important for the adaptation of any organism to the reality in which it lives.

The Projects
1. Psychoethological Studies on Animals; Modality Grant for Productivity in Research (CNPq); Coordinator César Ades – Psychology Institute-USP; Investment R$ 58,400.00
2. Behavior and Evolution in Spiders: Cladistic Analysis of Predation, Web Construction and Courting in Araneid Families; Modality Regular Line of Grants for Research Projects (FAPESP); Coordinator Hilton Ferreira Japyassú – Butantan Institute; Investment R$ 90,536.08

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