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Ethology

Tricks of a seducer

Relatives of spiders, male harvestmen that take care of the eggs and attract the attention of females

Bruno A. BuzattoAcutisoma longipes: yellow secretion with an unpleasant odor repels predatorsBruno A. Buzatto

At the farm where he spent most of his childhood, in the hills around the town of Petrópolis, state of Rio de Janeiro, Glauco Machado used to find in every corner of the house small and inoffensive harvestmen [also known as daddy-longlegs], a close relatives of spiders and very common in the Atlantic Coastal Rainforest region, which provides them with a high level of moisture and mild temperatures. This was back in the early 80’s and Glauco could not imagine that later in life he would encounter these arachnids with very long and slim legs again during his undergraduate studies in biology at the State University of Campinas (Unicamp). Much less did he suspect that someday he would become one of the leading Brazilian experts in their behavior, which may help us understand the behavior of other living beings. “Harvestmen’s behavior can serve as a model to understand other animals where courting, reproduction and family relationships are concerned,” states the biologist, currently a professor at the School of Bioscience at the University of São Paulo (USP); his recent studies have shown that female care of their offspring is essential for the reproductive success of harvestmen.

Often mistaken for spiders, harvestmen have eight legs. However, two of them, i.e., the second pair of legs, are used as antennae to become familiar with their environment by touch. In fact, it is precisely because of their long legs that they probably received their [scientific] name, opiliones, which in Latin means shepherd. In Ancient Rome shepherds walked on wooden stilts to control their flocks better. As opposed to the bodies of spiders, separated into two parts (the abdomen and the cephalothorax, which unites the head and thorax), the harvestman’s body does is not divided: cephalothorax and abdomen are joined together in a single unit. Its strongest trait, however, which enables anyone to distinguish a harvestman from a spider, is that the former has odor glands: when threatened, it releases a strong, stinking secretion, which has given it the nickname aranha-bode in Portuguese, i.e., goat-spider or stinky spider. Based on chemical compounds such as quinones, phenols and ketones, this secretion allows several different species of harvestmen – approximately six thousand worldwide and almost a thousand in Brazil alone – to fend off predators such as frogs and ants, a fact recently corroborated by Machado.

For one full year, in a study coordinated by Machado on the  Island of Cardoso off  the southern coast of the state of São Paulo, Francini Osses, a biologist, monitored where females of the Bourguyia hamata species chose to build their nest. With an orange colored body and legs as long as 10 cm, these harvestmen almost always look for the long leaves of the Aechmea nudicaulis bromeliad to deposit their eggs, although there are 36 other bromeliad species right in the region where the research was being conducted. Francini assessed the volume of water and cleanliness of the bromeliads that this harvestmen species selected for its offspring. He found that there was a preference for larger bromeliads that accumulated more water, which prevents drastic variation in humidity, and where there was less debris from the trees, as described in the article soon to be published in the Journal of Ethology. “The selection of this bromeliad, which usually grows on trees, is that it protects against predators and provides an ideal level of cleanliness for the delivery of offspring,” explains Francini.

Maternal care is not restricted to choosing the most suitable place for procreation. After laying their eggs, females often dismiss their daily activities – such as their own nutrition, based on insects and fruits or even dead harvestmen of other species – to dedicate their time to their offspring. They practically spend a month on top of the eggs to protect them from predators. “It’s a very tough job. The female has to give up many things to ensure the birth of her offspring, but in the end she is rewarded,” states Machado, who had observed this behavior back in 1998, during his initial scientific studies. Recently the zoologist Bruno Buzatto and Machado decided to analyze the importance of protecting the eggs in an experiment carried out in nature.

BRUNO A. BUZATTOHarvestmen from the Gagrellinae subfamily, commonly found in the Mata Atlântica, the Atlantic coastal rainforestBRUNO A. BUZATTO

Mother care
At the Intervales State Park, located in the Vale do Ribeira valley, south of the state of São Paulo, Buzatto found 144 females of the Acutisoma proximum species, with a green body of the size of a 10-cent coin and that usually lay their eggs on rocks and leaves near the banks of streams, marking them with an ink that remains on the body for as long as two years. He then separated them into two groups: half of them spent the entire time taking care of the eggs, while the eggs from the other group of females were removed from the nests for two weeks. Buzatto found that the unprotected nests were attacked by crickets, wasps or harvestmen, which devoured 75% of the eggs on average. In an article published in the September 2007 edition of the Journal of Animal Ecology, Buzatto, Machado, Gustavo Requena and Eduardo Martins reported that the females whose eggs were experimentally removed from the nests soon looked for another male to copulate and began to lay eggs more often – on average they deposited 18% more eggs than the ones that cared for their offspring. Laying more eggs, however, only provided one apparent advantage, according to the researchers. When they quantified the burden on the females, they found that the best alternative would be to take care of their offspring. “There is no use in laying more eggs if most of the offspring will die if they do not receive their mother’s care,” explains Machado.

And it is not only the females that are interested in taking care of the nests. Machado discovered that males of some species pretend to be good father figures as a courting strategy. In the past, Machado and his team identified six species of harvestmen in which the males are responsible for the eggs and they investigated this behavior in another six species – before they were  aware of three species in which the males cared for the eggs. Analyzing the Iporangaia pustolosa species, with the bright green body and black spots and just slightly larger than a pearl, Machado and Gustavo Requena discovered that the more females within a population of harvestmen, the longer males spend taking care of the eggs.

GLAUCO MACHADOProtimesius longipalpis, found in the Amazon; and a specimen of the Pristocnemis genus, sensitive to deforestationGLAUCO MACHADO

The right choice
At least among harvestmen, the strategy works. Taís Nazareth observed the copulating harvestmen of the Pseudopucrolia genus originally from the state of Espírito Santo. She placed two males in glass recipients – one cared for the eggs while the other remained alone with no offspring. Then the researcher placed a female in the environment. In less than two hours, she had already chosen the male that cared for the eggs and copulated with him. Subsequently, the roles were inverted. The male that previously had nothing to care for began to care for the eggs. The other had nothing to watch over. Again the female chose to copulate with the male with the offspring. Physical attributes such as body size and color did not influence the choice, observed Taís. This experiment also showed that, when the insect responsible for the eggs dies, another male takes over the responsibility to protect the offspring, which is the opposite of the behavior found in other species. “If females prefer caring males, the ones that pretend to be the owners of the eggs are ahead of the game,” suggests Machado.

Without venom and fangs, the apparently fragile harvestmen may become aggressive to protect themselves: they attack with their palps and they pinch with their chelicerae or with the thorns on their legs. But there is a weapon that only they possess that has enabled them to survive since their origin, 400 million years ago: the repulsive odor they release. Through a pair of scent glands, they release a yellow liquid with a strong acidic odor, capable of fending off many of their predators. In a series of tests carried out years ago at Unicamp, Machado confirmed the efficiency of the scent in saving harvestmen’s lives. Along with researchers Patrícia Carrera, Armando Pomini and Anita Marsaioli, he collected the stinking yellow liquid of the Acutisoma longipes species, common throughout the entire Southeast of Brazil, and extracted two types of benzoquinone.

In experiments with seven species of ants, Machado wet a piece of filter paper in water and sugar, then adding to this some secretion from the harvestmen. It was enough to keep ants away from the food for up to ten minutes, and gave the harvestmen more than enough time to escape an attack. The group repeated the same test with other harvestmen predators. To guarantee that it was really the stench – and not a different defense strategy – that was protecting the long-legged shepherds, Machado put some drops of yellow secretion on crickets and offered them to horned frogs and spiders. Most of the predators could not stand the stench. After eating the smelly cricket, the frog started to jump and shake until he coughed it up alive. The only predator that was able to eat the cricket, although with some difficulty, was the white-eared opossum, stated the researchers in an article published in the Journal of Chemical Ecology.

“We were careful to study animals that live in the same areas as the harvestmen and who eat them in their diet,” stated Machado, who in the beginning of last year published, along with Ricardo Pinto da Rocha, from USP, and Gonzalo Giribet, from Harvard University, the book Harvestmen: the biology of opiliones. With chapters written by 25 different authors, it sheds new light on the morphology, taxonomy, behavior and ecology of harvestmen, one of the oldest animal groups on Earth. Since they only travel short distances, it is likely that the species found in different regions all around the world have lived there for millions of years, a fact that helps scientists to understand our planet’s evolution. “Considering the current distribution and establishing relative relationships, we found that there are very similar species in Chile, South Africa and Australia,” reports Machado. Not by chance, these countries are located in continental blocks that were joined hundreds of millions of years ago in the supercontinent of Gondwana.

The Project
Parental care and evolution of the subsocial behavior in harvestmen of the Gonyleptidae family (arachnida: opiliones) (nº 05/50147-1); Type: Regular Research Grant Line – Young Researchers; Coordinator:
Glauco Machado – IB/USP; Investment: R$ 141,737.16