A robin flying over a field sees a juicy caterpillar on a leaf. It dives in for a closer look but it notices something strange: this larva is bright red and glowing slightly. Red means danger – this caterpillar is probably toxic and is best avoided. The robin leaves; the caterpillar apparently lives. But this particular caterpillar is already dead, and its corpse has been protected by two unseen and unlikely partners. Its warning colours are not its own – they were painted on by parasites.

The caterpillar has been infected by nematode worms, which burrowed into its mouth, skin or anus. Once inside, they released thousands of glowing bacteria (Photorhabdus luminescens). These will soon kill the caterpillar, breaking down its tissues into a nutritious soup, which the worms will gorge upon. Several generations of worms will live, feed, mate and die in a single dead caterpillar, before bursting forth, ready to infect again with bacteria in tow.

The worms (from the Heterorhabditis group) and the bacteria are partners in infection – one infiltrates, the other kills, and neither can survive without the other. But their efforts are all for naught if their host gets eaten in the meantime. If that happens, they die too; the worms can’t survive a trip through the gut of a bird. And to avoid that happening, they conspire to make the caterpillar look as unpalatable as possible. They save it from being eaten from the outside so that they have enough time to eat it from the inside.

Andy Fenton from the University of Liverpool discovered this tactic by offering a variety of caterpillars – both infected and uninfected – to wild robins. He found that the birds hardly ever eat infected caterpillars but they’ll certainly chomp down on healthy ones that had been dead for the same time.

As the infection continues, the red colour deepens, ultraviolet reflections dim, and the parasitized caterpillars become even more distinct from their uninfected kin. As a result, the robins’ revulsion grew. By the end, they even became reticent to approach the larvae for an exploratory peck.

It’s possible that the birds were using other cues, such as smell, to tell between the infected and healthy caterpillars. However, Fenton notes that he pinned all the larvae on a board and offered them to the robins, who probably don’t have a keen enough sense of smell to discriminate between such close sources. Instead, they were probably relying on their keen eyesight, and the fact that the infected caterpillars look ever more bizarre with time.

Fenton notes that the painted warnings would only work if they were honest ones. If a robin took a peck and found that the bright red morsels were actually quite pleasant to the taste, it would soon learn to eat them anyway. So it’s probable that the parasites also produce some sort of distasteful chemical and indeed, some of the birds that did peck at their hosts’ carcasses decided to leave them alone.

Parasites often change the behaviour and the bodies of their hosts and often, they make them more likely to be eaten. Flukes drive snails to visible leaves and extend pulsating sacs into their antennae, drawing the attention of birds. Rats infected with Toxoplasma develop a fatal attraction for cat urine. Crustaceans infected by the spiny-headed worm Polymorphus paradoxus spend more time at the water surface, making them easy prey for ducks.

In all of these cases, the parasites have complex life cycles involving many hosts. By triggering kamikaze behaviour, it ensures that its current host (snail, rat or crustacean) will be eaten by the next one (bird, cat or duck). But the worm and bacteria are less complicated. Although they infect a wide range of insects, their life cycle only involves one host. For them, being eaten would be a disaster and it’s no surprise that they have evolved strategies to avoid that fate.

This particular partnership has been studied for some time. The bacteria are responsible for a phenomenon called “angel glow”, a mysterious blue glow coming from the wounds of soldiers as far back as the US Civil War. Bizarrely, these soldiers were less prone to blood poisoning and infections. Why? The luminous bacteria typically secrete antibiotics that keep their worm partners free from other infections; these same antibiotics protected human soldiers too. Today, the parasitic partners are helping humans in another way too. They’re used as a convenient form of biological control, to cull insect pests without having to resort to chemical agents.

Reference: Fenton, A., Magoolagan, L., Kennedy, Z., & Spencer, K. (2010). Parasite-induced warning coloration: a novel form of host manipulation Animal Behaviour DOI: 10.1016/j.anbehav.2010.11.010

Photo by Penny Greb

More on parasites:

• Attack of the cloned soldier worms
• Parasitic wasps hitchhike on butterflies by smelling for chemical chastity belts
• One parasite to rule them all – Wolbachia protects against mosquito-borne diseases
• The plague of tyrants – a common bird parasite that infected Tyrannosaurus
• Wasps use genes stolen from ancient viruses to make biological weapons
• Toxoplasma – the brain parasite that influences human culture

If the citation link isn’t working, read why here

December 17th, 2010 by Ed Yong in Animal behaviour, Animal communication, Animal defences, Animals, Parasites | 9 comments | RSS feed | Trackback >