Parasite manipulates host’s sense of smell

Parasites employ various strategies to increase their chances of reproducing. Some do so by manipulating the behaviour of their hosts. For example, when ready to sporulate, fungi of the genus Cordyceps synthesize chemicals which induce their ant hosts to climb the nearest plant, so that the area over which the fungal spores are distributed is maximized; similarly, gordian worms synthesize neuropeptides which mimic those produced by the host (a terrestrial insect), and which interfere with the host’s geotactic senses, causing it to jump into water so that the aquatic adult worm can emerge; and the platyhelminth worm Leuchchloridium macrosto- mum infects snails, turning their eye stalks into colourful blinkers, which makes the host more conspicuous to the molluscs which prey on them, and which are hosts for the remaining part of the parasites’ life cycle.

Acanthocephala is a phylum containing approximately 1,150 species of manipulative parasitic worm. The word Acanthocephala comes from the Greek roots Acantha, meaning ‘thorn’, and Kephale, meaning ‘head’; acanthocephalan worms, commonly known as spiny-headed or thorny-headed worms, are so named because one of their characteristic features is a retractable proboscis covered with tiny hooks. Acanthocephalans have a highly complex life cycle, involving the infection of one or more intermediate hosts. The intermediate hosts are always arthropods, and are usually the preferred food of the predator which acts as the worm’s definitive, or final, host.

Upon infection, the juvenile worm takes residence within the host’s body cavities. Because it lacks a digestive tract, the worm uses its proboscis to attach itself to the host’s intestinal wall, from which it absorbs nutrients. But acanthocephalans can only reach sexual maturity in the final host. The worms therefore manipulate the behaviour and physiology of their intermediate hosts, making them more conspicuous to the predatory fish; this increases the probability that the worms will complete their life cycle. The definitive host is always a vertebrate – a mammal, amphibian or bird; of the latter, ducks, geese and swans are common.

The intermediate hosts of the Pomphorhynchus laevis species are small (approx. 1 cm-long) freshwater crustaceans called amphi- pods. Previous studies have shown that amphipods infected with P. laevis are more susceptible to predation. Normally, amphipods remain in the dark areas to avoid capture by predators. This behaviour is mediated by a photophobic response, which causes the amphipods to be repulsed by light. But a P. laevis infection abolishes this photophobic response, and the amphipod’s response to light changes dramatically as a result. Rather than swimming away from a light source, infected shrimp move towards it. By swimming into open waters, they are much more visible to their predators. P. laevis infection also leads to increased production of haemocyanin, the invertebrate equivalent of haemoglobin, which carries oxygen around the body. The increased haemocyanin concentration produces a colour change, which further increases the conspicuousness of the infected shrimp, and facilitates the transmission of the parasite to the predatory fish, its definitive host.

An amphipod (left) and the retractable proboscis of Pomphorhynchus laevis (right).

Sebastian Baldauf and his colleagues at the University of Bonn’s Animal Ecology Research Group have now discovered another trick that P. laevis carries up its sleeve. They have found that the worm manipulates the sense of smell of its intermediate host, the amphipod. As a result, the infected shrimp is attracted to the odour of fish that prey on it.

From a brook near their laboratory in Lucerne, Switzerland, Baldauf and his colleagues collected several hundred amphipods of the Gammarus pulex species (also known as the freshwater shrimp, or river shrimp), and 10 perch fish, which are known to prey on amphipods. Compartmentalized tanks containing separate sections were used to subject the amphipods to a series of choice tests. In each trial, an amphipod was placed in the middle of the lower section, which ran the entire length of the tank. After 5 minutes, a transparent net was placed 3 cm from the bottom of the tank, and a transparent divider was placed on top of the net, to divide the top section into two compartments of equal size. A perch was then placed in one of the two upper compartments, and the preference of the amphipod to one side of the tank or the other was observed.

In one experiment, the transparent net was glued to a transparent divider, so that only visual cues were available to the amphipods. In this set up, neither infected nor uninfected amphipods showed any preference for which side of the tank they stayed in. In another set up, uninfected amphipods were separated from the fish by jsut the transparent net, so that chemical signals could diffuse between the upper and lower sections of the tank. In this trial, the amphipods preferred the side without fish, and tried to escape from the fish by moving into the opposite side of the tank. When this trial was repeated with infected amphipods, it was found that they actually preferred the side of the tank containing the fish, and moved towards it.

The researchers could not determine the nature odour detected by the amphipods. The escape behaviour of uninfected shrimp, and the approach behaviour of infected shrimp, may be elicited by the odour of the predatory fish, or, possibly, by the odour of decom- posing products of shrimp already eaten by the fish. Nevertheless, the trials provide evidence that chemical cues are important for the recognition of predators by amphipods, and that P. laevis manipulates the amphipod olfactory system, such that infected shrimp are attracted to, rather than repulsed by, the odour of its predators. How it does so is, however, unclear. The researchers believe this to be the first example of a parasite manipulating its host’s olfactory system. The findings have been published in the International Journal of Parasitology.

References:

Baldauf, S., et al. (2007). Infection with acanthocephalan manipulates an amphipod’s reaction to a fish predator’s odours. Int. J. Parasit. 37: 61-65.

Bakker, T. C. M., et al. (1997). Parasite-induced changes in behavior and color make Gammarex pulex more prone to fish predation. Ecology 78: 1098-1104.

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