By Elton Alisson
Agência FAPESP – The hard thick carapace or outer covering worn by some arthropods (such as insects, crustaceans and arachnids) is not sufficient armor for the harvestman Mischonyx cuspidatus to escape attack by the Brazilian recluse spider or brown spider (Loxosceles gaucho).
A study performed by researchers at the University of São Paulo’s School of Arts, Sciences and Humanities (EACH-USP), in collaboration with colleagues at the Federal University of Uberlândia (UFU), in Minas Gerais State, shows that the spider is capable of identifying points on the body of M. cuspidatus where its exoskeleton is flexible and, hence, vulnerable, using this skill to prey on the harvestman.
Findings from the study, which was part of the project “Chemical communication in harvestmen (Arachnida, Opiliones): morphology, behavior and chemistry” and supported by FAPESP, are described in a recent paper in the online version of the journal Animal Behaviour, published by Elsevier.
“We found that the recluse spider is able to avoid the armoring of M. cuspidatus by pinpointing vulnerable parts of the harvestman’s body and piercing its prey there,” said Rodrigo Hirata Willemart, a professor at EACH-USP and lead investigator for the project.
Harvestmen are arachnids of the order Opiliones. The most widespread suborder in Brazil is Laniatores, to which the species M. cuspidatus belongs.
Willemart told Agência FAPESP that harvestmen use different strategies to ward off attacks by the recluse spider, one of their predators in addition to certain birds, mammals and amphibians, among other animals. One such strategy is the discharge of odorous secretions in the form of droplets or spray to repel a predator.
However, the researchers discovered that this chemical defense strategy is rarely used by some harvestmen of the suborder Laniatores against banana (or wandering) spiders such as Enoploctenus cyclothorax and Ctenus ornatus.
The initial hypothesis was that Laniatores harvestmen are protected against spiders by their rigid exoskeleton. Using secretions to defend themselves from these predators despite having this “armor” would waste a “chemical weapon” that most likely cost them a great deal to produce, the researchers assumed.
“Although these two species of spider are far stronger and larger, they’re usually unable to penetrate the harvestman’s armor because the fangs on their chelicerae, the pincer-like mouthparts they use to bite prey, slip on the exoskeleton, and they abandon the attack,” Willemart told. “The spider jumps onto the harvestman, tries to bite it and quickly loses interest because the harvestman’s armor is too hard.”
Field research showed, however, that the recluse spider can kill and eat harvestmen even though its body and chelicerae are more delicate.
“We frequently found carcasses of Laniatores trapped in recluse spiders’ webs in the wild,” Willemart said. “For this reason, it seemed to us to be the perfect species to help us understand how the harvestman’s armor could be circumvented.”
To discover how these spiders prey on harvestmen and evaluate their hunting strategy in detail, the researchers performed three laboratory experiments with pairs of L. gaucho spiders and M. cuspidatus harvestmen.
The first experiment was designed to see whether, when hunting and capturing its prey, the spider follows the trail of chemical cues left by harvestmen as they move over a surface.
Harvestmen were left on filter paper for 24 hours, during which time they moved over the surface and impregnated the paper with chemical compounds. The paper impregnated with chemical compounds from harvestmen was then introduced into half the area of the terrarium used as a test arena; the other half was lined with blank paper containing no chemical cues to see whether the spider would remain longer on one side or the other.
The time spent by the spider on the sides with and without chemical cues left by harvestmen did not differ significantly.
“The spider didn’t use chemical cues left by harvestmen when deciding where to forage,” Willemart said.
In the second experiment, the researchers wanted to find out whether substrate-borne vibrations from harvestmen were important for the recluse spider to locate this particular prey. Spiders typically use vibratory cues to hunt and capture their prey – and L. gaucho does not have good eyesight.
Spiders and harvestmen were placed on a substrate that transmits vibration (filter paper) and on a vibration-dampening surface (granite). The researchers measured the time taken by spiders to attack harvestmen on each substrate.
The results showed that the spiders were equally successful in capturing their prey on both substrates.
“What this means is not that L. gaucho doesn’t use the vibrations transmitted by a substrate to locate its prey but that it can capture harvestmen with or without this sensory modality,” Willemart said.
The third experiment was designed to find out whether the recluse spider uses the web that it spins on the ground, and that resembles a sheet of silk, to capture and kill its prey by biting vulnerable areas of the harvestman’s body.
Spiders were tested with and without webs. Predation rates and handling times were the same, showing that the presence of a web is not decisive.
“We thought spiders using webs would be more successful, but, surprisingly, that wasn’t the case,” Willemart said.
Fifty-one of the 68 recluse spiders used by the researchers in these tests found a way to capture harvestmen, later killing and eating them, he added.
To understand how recluse spiders breach the protection afforded by the harvestman’s hard exoskeleton, the researchers recorded videos and described the predators’ attack behavior.
According to Willemart, a recluse spider begins by approaching its prey slowly and carefully, always trying to place itself in front of the prey to prevent escape. It then repeatedly touches the harvestman with its legs, possibly in search of vulnerable areas. It avoids excessive proximity, as the harvestman also has chelicerae as well as needle-sharp leg spikes.
If the harvestman remains immobile or fairly static, the spider may make a move Willemart likens to an ippon, the game-ending judo throw, flipping the harvestman over and pinning its back to the ground. The predator then delivers a series of poisonous bites to the joints and distal (outer) parts of the harvestman’s legs, precisely the areas where the exoskeleton is softer or more flexible to allow the harvestman to move.
“We analyzed 176 bites delivered by recluse spiders to harvestmen during the study,” Willemart said. “In 100% of cases, they bit joints or distal parts of legs.” None of the harvestmen resorted to chemical secretions to defend themselves from the predators’ attacks.
A hypothetical explanation for this is that harvestmen avoid using chemical defense against spiders in general, apparently because their hard exoskeleton is sufficient to protect them from most spider attacks.
They evidently do not anticipate the recluse spider’s ability to pinpoint the weaknesses in this armor, however.
“The recluse spider’s strategy for hunting harvestmen works much better than those of other species, such as banana or wandering spiders,” Willemart said.
“It’s as if recluse spiders were war strategists that exploit their opponent’s weaknesses, and banana spiders were street fighters that attack harvestmen using the wrong technique.”
Now the researchers plan to investigate whether other arthropods with rigid exoskeletons respond similarly to attack both by hunter predators such as banana or wandering spiders, and by recluse spiders.
The results of the study, published in the paper “Delicate fangs, smart killing: the predation strategy of the recluse spider” (doi: 10.1016/j.anbehav.2014.12.025), by Willemart et al., can be read in the journal Animal Behaviour at www.sciencedirect.com/science/article/pii/S0003347214004783.