Zombie fungi and ant graveyards

by JJ

It is not unusual for parasites to control the behavior of their hosts, sometimes causing dramatic changes in their behavior: Nematode worms have been shown to cause their insect hosts to drown themselves so that their adult stages can reproduce in water ¹. Some parasitic wasp larvae can drive bumblebees to bury themselves alive to provide a better environment for the developing larvae². Similarly, the parasitic fungus Ophiocordyceps unilateralis affects its insect host’s brain, effectively turning the insect into a ‘zombie’ whose only purpose is to serve as food for the fungus and a vehicle to carry it to more favorable environments.

O. unilateralis was first described by English scientist Tom Petch in 1931 as a top-shaped fungus found on dead aphids³(A common sap-sucking insect pest). He also noted how all dead aphids infected by the fungus were found ‘glued’ to leaves by fungal protrusions³. Since then, O. unilateralis has been shown to infect many species of insects, but especially ants in tropical forests around the world. There are even distinct species found in China, South America, and Africa^4,5. These fungi are thought to help keep insect populations in check. They have also been used in ancient Chinese medicine for hundreds of years, although they have only recently been investigated for the production of therapeutic compounds⁶.

When an ant is infected by O. unilateralis while foraging, it will eventually abandon all ant-like behavior, its mind seemingly under the control of the fungus: hence the term ‘zombie fungus’. When the ant walks over fungal spores, the spores cling to the exoskeleton (a hard shell-like outer layer) of the ant. Within 3 days, the spores germinate and reproduce within the ant⁷. In the meantime, the ant’s behavior starts to change. It stops foraging and following scent trails altogether and starts to climb to locations close to the forest floor, such as leaves. Once it reaches a leaf, the ant uses its mandibles (mouthparts) to clamp on to the leaf and stays put until it eventually dies of starvation, the fungus having used its body to reproduce. It is not clear how the ant’s colleagues feel about this.

Once the ant dies, the fungus produces a long stalk emerging from the back of the ant’s head (Fig. 1). This stalk bears a structure filled with new fungal spores. Eventually, these spores drop to the forest floor, where they can infect new insects and continue the cycle. The spread of spores in this manner means infected insects are often found clustered around the same area, forming ‘graveyards’⁷. Researchers have undertaken the grim task of studying different conditions surrounding these graveyards over time and have found that they are more likely to be present where humidity is high and foliage is dense- conditions that would give the fungus a better chance to reproduce. The number of graveyards has also been found to increase during the monsoons, and decrease in the summers⁷. More importantly, other insects have been shown to actively avoid these graveyards, and ant trails very rarely cut across graveyards⁷. Ant colonies prefer foraging up the treetops and minimize time spent on the forest floor⁷. They are also known to groom each other, which is thought to help remove spores and keep the colony immune to infection⁸. These behaviors have probably evolved as defense mechanisms against fungal infection, and suggest that the fungus has co-evolved with insects, with insects being evolutionarily selected for avoiding the fungus, and the fungus evolving to more efficiently disperse its spores⁵.

There are other aspects of O. unilateralis infection that are yet to be fully understood. For example, the interactions between the parasite and the host at the molecular level are not yet clear⁹. These are important because they would give us a clearer picture of how the fungus proceeds from the spore to the stalk-forming stage during infection. Next, the effect that the fungus has on the insect nervous system also needs to be described, aside from just behavioral changes. The full range of behavioral changes induced in ants is also not clear: some researchers suspect that the fungus induces aggressive behavior in ants, which could help the spores spread to other workers in the ant colony⁹. Using large indoor ant colonies for observational studies (Fig. 2) would allow researchers to manipulate ants and isolate each of these behavioral and physiological changes, helping to paint a more complete picture of the zombie fungus.

References                                                                                          

1.         Sato, T., Watanabe, K., Tamotsu, S., Ichikawa, A. & Schmidt-Rhaesa, A. Diversity of nematomorph and cohabiting nematode parasites in riparian ecosystems around the Kii Peninsula, Japan. Can. J. Zool. 90, 829–838 (2012).

2.         Müller, C. B. Parasitoid induced digging behaviour in bumblebee workers. Anim. Behav. 48, 961–966 (1994).

3.         Petch, T. Notes on entomogenous fungi. Trans. Br. Mycol. Soc. 16, 55–75 (1931).

4.         Evans, H. C., Elliot, S. L. & Hughes, D. P. Hidden Diversity Behind the Zombie-Ant Fungus Ophiocordyceps unilateralis : Four New Species Described from Carpenter Ants in Minas Gerais, Brazil. PLOS ONE 6, e17024 (2011).

5.         Kobmoo, N., Mongkolsamrit, S., Tasanathai, K., Thanakitpipattana, D. & Luangsa-Ard, J. J. Molecular phylogenies reveal host-specific divergence of Ophiocordyceps unilateralis sensu lato following its host ants. Mol. Ecol. 21, 3022–3031 (2012).

6.         Isaka, M., Kittakoop, P., Kirtikara, K., Hywel-Jones, N. L. & Thebtaranonth, Y. Bioactive substances from insect pathogenic fungi. Acc. Chem. Res. 38, 813–823 (2005).

7.         Pontoppidan, M.-B., Himaman, W., Hywel-Jones, N. L., Boomsma, J. J. & Hughes, D. P. Graveyards on the Move: The Spatio-Temporal Distribution of Dead Ophiocordyceps-Infected Ants. PLOS ONE 4, e4835 (2009).

8.         Schmid-Hempel, P. Parasites in Social Insects. (Princeton University Press, 1998).

9.         Bekker, C. de, Merrow, M. & Hughes, D. P. From Behavior to Mechanisms: An Integrative Approach to the Manipulation by a Parasitic Fungus (Ophiocordyceps unilateralis s.l.) of Its Host Ants (Camponotus spp.). Integr. Comp. Biol. icu063 (2014). doi:10.1093/icb/icu063