Thorny-headed worms make shrimps lose their sense to smell fish predators

Shrimps infected with thorny-headed worms lose their ability to smell the presence of predatory fish or injured shrimps and to perform anti-predator behavior. This may increase the likelihood that they will be eaten, thereby passing the parasite to its next host.

In common with many aquatic animals, fresh water shrimps can detect the presence of fish predators by their smell and take avoiding action. However, if a thorny-headed worm has taken up residence inside the shrimp this anti-parasite behavior is overridden, the shrimp is more likely to be eaten and the worm will then be delivered to the next host in its life cycle.

Charles Stone and Janice Moore have recently extended these observations and shown that shrimps also lose the ability to smell alarm signals from other shrimps in danger. These findings add to the fascinating suite of behavioral manipulations already known to occur when this group of parasites infect their arthropod hosts.

Thorny- (or spiny) headed worms get their name from the proboscis armed with rows of backwards pointing spines that that they use to punch into the gut of their vertebrate host to anchor them. They belong to the phylum Acanthocephala and are all parasitic, having a life cycle that also involves an invertebrate host.

The proboscis of a Rhadinorhynchus species of acanthocephalan. Image from wiki commons.
The proboscis of a Rhadinorhynchus species of acanthocephalan. Image from wiki commons.

Several species use shrimps (amphipods) as their intermediate host and either a fish or a mammal or bird that feeds in an aquatic environment as final host. The parasite’s eggs are shed with the faeces of the vertebrate host and, if eaten by a shrimp, they hatch and the embryo burrows through the wall of the intestine and develops in the body cavity. Here they mature to a juvenile called a cystacanth that can infect a fish if it’s shrimp host is eaten.

Amphipods feature in the diet of many fresh water fish and birds such as ducks. When they smell the presence of predatory fish they alter their behavior in response to fish odors (known as chemical signals or kairomones) in ways that decrease the likelihood of being caught.  For instance, they dive to find shelter in the substrate, are less active, aggregate together and are less likely to be found drifting in the water column. They respond to alarm chemicals (or pheromones) given off by other shrimps in a similar way.

In Stone and Moore’s study, infected shrimp’ responses to these odors were compared to those of uninfected ones. Individual shrimps were exposed to water alone, water in which a Green Sunfish had been swimming for 24 hours (containing kairomones) or to water containing a shrimp extract   that  simulated injured organisms (containing alarm pheromones).  In the test tank the researchers place a refuge made from a piece of opaque black glass, supported on legs, and placed in the center of the bottom of the tank.

Shrimps were observed for 5 mins and the amount of time spent crawling /swimming away from the refuge or on or under it was recorded. The test water was then introduced and the same behavior recorded for another 5 mins.  Shrimp behavior before and after the exposure to these odors was compared.

Leptorhynchiodes thecatus a parasite of fresh -water fish in the US. Image http://www.state.me.us/ifw/fishing/health/vol4issue9.htm
Leptorhynchiodes thecatus a parasite of fresh -water fish in the US. Image http://www.state.me.us/ifw/fishing/health/vol4issue9.htm

The presence of a cystacanth had no effect on the behavior of the shrimps in the untreated water, but the alarm pheromone from damaged shrimps significantly decreased their activity and double the time at the refuge. In contrast, alarm pheromone had no effect on infected shrimps.

Kairamones from the predator fish also caused the activity of uninfected shrimp to decrease and the time spent using the refuge to increase, though not to such a great extent as the alarm pheromone.  However, refuge use actually decreased slightly in infected fish. The authors concluded that infected shrimps did not sense the stimuli indicating danger.

Unfortunately the nature and concentration of fish kairomones and shrimp alarm pheromones produced in this study is unknown and they could well be complex mixtures of chemicals. This resulted in changes in behavior recordings being qualitative rather than quantitative. Isolation of the active ingredients would be desirable but no doubt challenging.

It is easy to predict that this loss of response to odors signalling danger would result in greater risk of predation and that this, in turn, would benefit the parasite. Experiments to test this hypothesis were unfortunately not conducted by Stone and Moore although investigation of similar responses to alarm pheromone by another uninfected amphipod showed that they do have an anti-predator effect; increasing the time taken for a Green Sunfish to attack the shrimps.

Conclusive demonstrations that parasite-induced changes in behavior increase the chances of transmission of parasites from the prey host to the predator host are rare. However, John Holmes and colleagues did this in the 1970s using this and another acanthocephalan that had ducks and muskrats as it’s final hosts. Mallard ducks and muskrats were shown to eat significantly more shrimps infected with the acanthocephalan Polymorphous paradoxus than uninfected shrimps.

The geotactic and phototactic responses of P. paradoxus are changed by the presence of a cystacanth. Unlike uninfected shrimps, they swim upwards and toward the light, bringing them in the vicinity of ducks or muskrats feeding in the surface waters. Furthermore they develop a “clinging response” which caused them to hold on to floating vegetation, thereby being eaten accidentally.

Janice Moore has published a thought provoking review of the development of the study of parasite-induced changes in host behavior that is recommended for further reading.

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