National Geographic

Parasitic worms paint warning colours on their hosts using glowing bacteria

Glowing_bacteria_nematodes

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

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There are 9 Comments. Add Yours.

  1. Kat
    December 17, 2010

    Am I the only person who thought that was a photo of a croissant?
    I’m hungry now, you bastard :)

  2. Robert
    December 17, 2010

    Parasite-host behavior is a favorite conversational topic of mine, and this is yet another round of ammunition in my arsenal of intriguing examples. Most of the others I know of are listed here: the snail fluke and toxo, particularly.

    This one’s a doozy, though, and may not be suitable for dinner parties.

  3. Dan Bailey
    December 17, 2010

    I’ve heard the “angel glow” story before, but I always wondered, are the glowing bacteria pathogenic in humans? It seems like they’re certainly bad news for caterpillars and other insects, but could they also cause sickness in humans, or birds for that matter? If the bacteria can liquify the inside of a caterpillar, you’d think they could also do some damage while growing in an open wound.

  4. Ed Yong
    December 17, 2010

    Dan- No, no problems for birds or mammals. Birds in the study were unharmed if they were deliberately fed the infected larvae.

  5. James
    December 17, 2010

    It’s such an amazing story of symbiosis! I wrote something similar up at SciAm blogs as well. From what I have read the glow seems to act as a deterrent for birds and mammals but an attractant for other insects and larvae facilitating easy spread of the bacteria and nematodes between hosts.
    http://tinyurl.com/26v2767

    Also @Dan Bailey
    The secretions of the worms and bacteria are almost exclusively larvacidal but can cause minor infections if the bacteria get into the underlying skin layers, generally causing ulceration but are easily treated.

    Great piece Ed, always love your write ups :)

  6. Ed Yong
    December 17, 2010

    James, I actually linked to your piece above! See last paragraph. It was a *really* nice piece.

  7. James
    December 17, 2010

    lol, I was so eager to comment that I missed that link! I’m so glad you liked it. I’ve got some picks of infections but I don’t think I can post them in here. To Twitter!

  8. Don
    December 18, 2010

    Dear Ed: Heterorhabditis spp are soil dwellers, and their host insects aren’t normally exposed to the eyes of birds. I have studied these and related entomopathogenic nematodes for 15 years in the field and never seen a host exposed; all were underground. Happy to provide you with references.
    Regards, Don Strong

  9. Ed Yong
    January 6, 2011

    Don, I asked Andy Fenton about your point. His response:

    “It’s true that these are soil-dwelling nematodes, and that we would be unlikely to see infected insects exposed on the soil surface. However, many birds that feed on soil-based insects (eg starlings, blackbirds etc) do so by probing in the ground and looking for grubs. Starlings in particular open their beaks in the soil to create a hole which they examine for prey – and it is at this point the infected insect would be seen.

    It is a fair point though that the experimental set up we used was artificial, as an initial test of the idea that the colour change could be a deterrent, and it would be great to now test it under more realistic conditions.”

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