Host Parasite Interactions: Cricket Suicide

By Stephanie Kolodij

 

In the summer of 2000, a group of scientists stood around a private pool in the south of France. Amid the drinking and socializing, Dr. F. Thomas from the Centre d’Etude sur le Polymorphisme des Micro-Organismes noticed something odd. Crickets from the neighbouring forest hopped across the concrete patio and into the pool. Once there, the crickets promptly drowned. Thin, white worms more than three times the length of the crickets wriggled free of the water-logged corpses.

Dr. Thomas decided to investigate.

The Worm

The scientists fished the dead crickets from the pool along with their apparent parasite. They determined that the infestation occurred because of a Nematomorpha, a large group (or taxon) of worm species commonly known as horsehair worms.

The adults of this taxon live freely in bodies of water. They mate in large, tight clusters of worms. This can only occur in their natural aquatic environment. However, the juvenile horsehair worms must first parasitize insects such as crickets in order to grow to their adult stage.

How Do They Get There?

The insect host, a cricket in this case, gains the parasite by consuming the microscopic larvae of a horsehair worm. The worm then grows until it takes up the majority of the body cavity of the host. The parasite invades every part of the cricket, except for the head and legs. Once the worm has grown to full size, it can exit the cricket and move on to the reproductive stage of its life cycle.

The worm needs water, and the forest dwelling cricket cannot swim. Thomas and colleagues thought this conflict could account for the strange behaviour seen at the pool in France. They created an experiment to determine whether or not the horsehair worm manipulated its insect host to leap to its death.

Field Cricket with Horsehair WormThe horsehair worm grows until it takes up the entire body cavity of the host insect.
Source: University of Nebraska-Lincoln, Soni Cochran, 2011.

The Field Observations

Over the summers of 2000 and 2001, Thomas conducted field observations of the crickets from the forest adjacent to the private pool. They sat and watched crickets arriving in the area. If the crickets jumped to their watery graves, the scientists collected both the empty cricket shell and the horsehair worm that emerged.

During those summers, the researchers observed several crickets jumping into the pool and releasing parasites. Two strange behaviours emerged. First, when the worm left the host body, some of the crickets lived. Five individuals managed to escape the pool after depositing the infection, despite the evisceration caused by the parasite. Second, 100% of the 10 crickets the researchers rescued from the pool immediately jumped back in. Does this behaviour only occur in infected crickets?

The Field Experiment

Also in 2000, Thomas took a more experimental approach. He wanted to look at the difference in behaviour between the infected and uninfected crickets. Scientists collected crickets from both the edge of the pool and the forest interior. The researchers kept the crickets overnight in the laboratory as a geographical control. Thomas placed the collected subjects two metres from the edge of a pool. He watched their behaviour for 15 minutes. The researchers then preserved and dissected each insect to determine their infection status.

Thomas and colleagues found a difference in horsehair infection rates between the crickets collected at the edge of the pool and the crickets collected from the forest. Of the forest crickets, 15% had a horsehair parasite. Of the pool-edge crickets, 95% had a horsehair parasite.

The scientists reorganized the crickets into two groups based on whether or not they possessed a parasite. Another difference emerged once the researchers placed the crickets near the pool. Only 13% of the uninfected crickets entered the water. Forty-nine percent of the infected subjects entered the water within 15 minutes.

The Lab Experiment

Thomas and colleagues also wanted to see if the crickets responded to the presence of water as the inciting factor. They set up a Y-shaped arena with one humid arm, culminating in a water trough. The other arm, a dry control, ended in an empty trough. The scientists left both infected and uninfected cricket subjects at the base of the Y then allowed them free reign of the arena for 30 minutes. The researchers documented which trough each cricket ended up in. They also recorded which arm of the arena the crickets chose, if the subjects did not reach either trough.

The Y-arena test showed no difference between the infected and uninfected crickets for preference of humid over dry conditions. The behaviours differed when the subjects reached the end of either branch.

Every cricket that reached the end of the dry arm, regardless of infection status, entered the dry trough within minutes. Once the crickets encountered water in the humid arm, all of the infected crickets leapt in immediately. Only 1 in 12 of the uninfected crickets jumped into the water trough.

The researchers indicate that the presence of water has no effect on the crickets until they physically encounter it.

What Does This Mean?

Thomas and colleagues suggest that the parasite manipulation system occurs, but not in a sophisticated way. Given that crickets have terrestrial (i.e., dry, earthy) habitats, natural selection acts on the horsehair worms that can manipulate the host to water.

The insects do not seem to have any sense of travelling to water. The researchers speculate that in nature, the behavioural modification would present erratically. The cricket leaves its normal habitat, but not in any particular direction. The scientists go on to say that the forest near the field site has a large number of small streams criss-crossing through. The wandering of the sick cricket would likely land it in water before long.

The study proves the behavioural difference between infected and uninfected crickets. The scientists found that the uninfected crickets displayed great reluctance to enter any kind of water while the infected crickets dove in without hesitation. They do not know whether this behaviour relates to an attraction to water, or simply ignorance on the part of the infected host to the dangers of water.

The researchers conclude that an alteration takes place in the infected crickets, regardless of the sophistication or inciting factor.

The horsehair worm parasite manipulates the infected cricket host into “suicide” by drowning, in order to complete its own life cycle.

Sources

Cochran, S. [Photograph of a field cricket and a horsehair worm]. (2011). Retrieved from http://lancaster.unl.edu/pest/resources/horsehairworm.shtml.Gwynne, Darryl. “Manipulation of Host Phenotypes by Parasites” BIO406. University of Toronto, Mississauga Campus. Mississauga, Ontario. 27 September 2012. Lecture.Ogg, B. (2011). Horsehair worms. Retrieved October/23, 2012, from http://lancaster.unl.edu.myaccess.library.utoronto.ca/pest/resources/horsehairworm.shtml
Gwynne, Darryl. “Manipulation of Host Phenotypes by Parasites” BIO406. University of Toronto, Mississauga Campus. Mississauga, Ontario. 27 September 2012. Lecture.
Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P., & Renaud, F. (2002). Do hairworms (nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology, 15(3), 356-361. doi: 10.1046/j.1420-9101.2002.00410.x