The Walking (Un)Dead: Zombie ants and the strange effects of parasitic fungi on ant behaviour​.

In the understorey of a tropical forest, a carpenter ant, of the species Camponotus leonardi, has descended from the canopy away from her regular foraging trails and staggers drunkenly along a branch. Her movements are jerky and conspicuous. She twitchily moves forwards and suddenly starts convulsing with such ferocity that she falls from the branch onto the ground before again taking up an erratic fitful path that zigzags and circles back on itself. Around noon, after several hours of climbing and aimless lurching (now no more than about twenty-five centimetres above the ground) the ant finds herself on the underside of a sapling leaf where, without warning, she forcefully sinks her mandibles into one of the leaf’s veins, gripping it firmly between her tightly locked jaws. Within six hours the ant is dead.  After two days, white hairs bristle from between her joints and a few days later these have become a brown mat covering the whole insect and a pinkish-white stalk has started to erupt from the base of the ant’s head. The stalk continues to grow and within two weeks it has reached twice the length of the ant’s body reaching towards the ground below.

This is a description of a “zombie-ant”, part of the life-cycle of a parasitic fungus, Ophiocordyceps unilateralis. This bizarre behaviour was first recorded by Alfred Russell Wallace in Sulawesi in 1859, but was not researched in much detail until quite recently. It has since been discovered that the fungus disrupts the normal behaviour of the ant through chemical interference in the brain, causing the infected ant to behave in ways that will improve the fungus’ opportunities to spread its spores and so reproduce. The fungus grows throughout the body cavity of the ant, using internal organs as food while the ant’s strong chitonous exoskeleton serves as a kind of capsule, protecting the fungus from drying out, being eaten, or further infection.

The earliest known record of a fungus visibly parasitizing an insect dates from about 105 million years ago, it is a male scale insect, preserved in amber, with two fungal stalks projecting from its head. But this fossil cannot tell us if the infected insect’s regular behaviour was changed or disrupted in any way.  Evidence of “Zombie-ant” behaviour dates from around 48 million years ago from fossilised leaves that show the distinct markings on either side of leaf veins left by the lock-jawed mandibles of Eocene epoch ants. This association is evidently ancient and seemingly very common, with about 1,000 species of fungal parasites of insects known to exist today. These fungal pathogens have evolved to become either strictly species-specific or more generalist in their target insects, with some able to infect hundreds of different species. The variety of fungal pathogens and potential hosts has created some peculiar behaviours in insects which have most likely co-evolved with the fungi.

It is sometimes difficult to know which of these insect behaviours are entirely involuntary and driven by the fungus to improve its own reproductive success; and which the insects have evolved as a form of defence against infection. One of these unresolved odd behaviours is when the ant host climbs to an elevated position in what is known as “summit disease”. This increases the area over which spores can spread through wind dispersal, and removes the ant from close proximity with its colony or relatives. It is unclear if this behaviour is a zombie state caused by the fungus or if it is an altruistic act of self-sacrifice by the ant. By moving to an area away from its relatives it might be saving the rest of the colony from the immediate spread of infection by what is sometimes called “adaptive suicide”.

cordyceps4-xlcordyceps2-xl

In this age-old struggle for survival the ants have developed adaptations to protect themselves and their nests from fungal infections. Grooming themselves and socially cleaning each other, allogrooming, they remove potentially harmful spores before these can penetrate the cuticle and take hold. Some ants spray poison in their nests to act as fungicides and if that fails to stop an infestation, they partition their nests by sealing off contaminated chambers. In some cases infected individuals are carried out of the nest by healthy workers; and as a last resort the entire colony relocates, abandoning the nest.

Zombie-like behaviour in insects is also caused by other types of parasites including bacteria and even other invertebrates. Such parasites are extreme versions of the multitudes of microscopic organisms that exist in and on all living things. This raises fascinating questions about the nature of any organism’s true independence in what are undoubtedly highly complex interrelated living systems. Zombie-ants provide us with a glimpse into this intricately tangled-web of molecular influences and behavioural adaptations – often leading us to wonder: who, ultimately, controls whom?

 

References:

  1. Andersen, S.B., Gerritsma, S., Yusah, K.M., Mayntz, D., Hywel-Jones, N.L., Billen, J., Boomsma, J.J. and Hughes, D.P. (2009) The Life of a Dead Ant: The Expression of an Adaptive Extended Phenotype. The American Naturalist, 174(3): 424-433.
  1. Hughes, D.P, Andersen, S.B., Hywel-Jones N.L., Himaman W., Billen, J. and Boomsma J.J. (2011) Behavioral Mechanisms and Morphological Symptoms of Zombie Ants Dying from Fungal Infection. BioMed Central: Ecology, 11(13).
  1. Pontoppidan M.-B., Himaman W., Hywel-Jones N.L., Boomsma J.J. and Hughes D.P. (2009) Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants. Public Library of Science: ONE, 4(3): e4835.
  1. Shang, Y., Feng, P. and Wang, C. (2015) Fungi That Infect Insects: Altering Host Behaviour and Beyond. Public Library of Sciences: Pathogens, 11(8): e1005037
  1. Hughes, D.P., Wappler, T. and Labandeira C.C. (2010) Ancient death-grip leaf scars reveal ant–fungal parasitism. Biology Letters, 7: 67-70.
  1. Roy, H.E., Steinkraus, D.C., Eilenberg, J., Hajek, A.E. and Pell, J.K. (2006) Bizarre Interactions and Endgames: Entomopathogenic Fungi and Their Arthropod Hosts. Annual Review of Entomology, 51: 331-57
  1. Bekker, C. de, Quevillon, L.E., Smith, P.B., Fleming, K.R., Ghosh, D., Patterson, A.D. and Hughes, D.P. (2014) Species-Specific Ant Brain Manipulation by a Specialized Fungal Parasite. BioMed Central: Evolutionary Biology, 14(166).

All images ©Alex Wild http://www.alexanderwild.com

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out / Change )

Twitter picture

You are commenting using your Twitter account. Log Out / Change )

Facebook photo

You are commenting using your Facebook account. Log Out / Change )

Google+ photo

You are commenting using your Google+ account. Log Out / Change )

Connecting to %s