In 1972, Holmes and Bethel outlined four ways in which a change in the behaviour of the intermediate host would increase the rate of transmission. These changes are a decrease in stamina, an increase in conspicuousness, disorientation and altered responses to environmental stimuli. These include changes in colour, size, foraging ability, preferences for high/light places, changes to social behaviour, mating behaviour and competitive interactions to name but a few. The activity of the host may be decreased or increased due to a parasite and different examples will be discussed showing that both extremes can increase predation and therefore transmission. It can therefore by appreciated that the different alterations of host behaviour due to parasites are extensive and widespread. Many scientists have become increasingly interested in the mechanisms and ways that behaviour is altered due to parasitic infection and their experiments and investigations illustrate the phenomenon of how different species which would naturally avoid predation can be manipulated by the action of parasites to go against their natural behavioural pattern. The hypothesis that these scientists use to carry out their investigations is known as the manipulation hypothesis which is used to test how the parasite manipulates its host to benefit itself.
Wild brown rats, Rattus norvegicus, are the intermediate hosts for Toxoplasma gondii: a parasitic protozoan. The protozoan’s definite host are cats and an experiment was performed which showed that once the rat had been infected with the protozoa its behaviour changed with respect to activity with the infected rats having notably higher levels of activity than the uninfected ones. This higher activity made the parasitised rats significantly less timid which meant that they were caught more easily by the cats and in turn the protozoa were able to reach their definitive host and complete their life cycle. Using the same species, another experiment was carried out to investigate the rat’s awareness of its predator. It was found that when both infected and non-infected rats where exposed to the scents of cats (their natural predators) and rabbits (which acted as a control scent); non-infected rats avoided the cat scented areas whereas infected rats had no such predisposition and actually showed preference to the cat scent over that of the rabbit. From this experiment is seems likely that rats behaviour was altered by the protozoa in order to benefit the parasite itself by increasing transmission to the definite host: the cat.
Increased energy levels have also been shown to be the altered behaviour in parasite infected lemmings. When exploring, the infected lemmings with higher energy levels were more noticeable to their predators, the snowy owls which are the definite hosts of the protozoan parasite. The parasite infected lemmings also seemed to carry out less grooming which signifies reduced fear of their natural predators.
As well as alterations to energy which increase levels, many instances have been found where the parasite benefits when it causes a reduction in its hosts energy levels. When ants where infected with parasites of cestodes and trematodes their behaviour in comparison to ants with no parasites was found to be much slower, sluggish or even stationary. This behaviour was seen to increase the chances of the ants being eaten by their predators which allowed the parasites to reach their definitive host and complete their life cycle. Activity levels can therefore be of benefit to the parasite in conjunction with predation where if they are decreased, a reduction in the stamina of the intermediate host increases the chance of predation and if they are increased, the animal becomes more noticeable and exposed which also increases chances of predation.
Behaviour resulting in the intermediate host being more conspicuous to its predator can also be achieved in a number of ways other than altering activity levels. Parasite - altered behaviour may mean that the animal prefers higher places or swims closer to the surface and is therefore at a greater risk of being preyed upon. This has been shown with aquatic animals such as gammarids which where found to float up to the surface once infected with plerocercoids. Burrowing bivalves which are infected with a trematode have been found to reside nearer the surface and are therefore more conspicuous to the birds which prey on them.
An investigation involving the action of the tapeworm Schistocephalus solidus on the three spined stickleback Gasterosteus has shown some interesting results. In order for the tapeworm to progress from its larval stage and be capable of reproduction; fish eating birds must ingest the tapeworm’s stickleback host. Once infected, it was observed that sticklebacks swum closer to the surface. Different scientists had different ideas to the reason behind this with suggestions of increased oxygen, food and temperature requirements but whatever the reason, parasite infected sticklebacks were more visible and more likely to be preyed upon.
In 2001 another investigation was performed to see the correlation between the growth and development of the parasite and the behaviour of the sticklebacks which were and were not infected. The methodology of the experiment was as follows. 30 sticklebacks where fed experimentally - infected copepods and where therefore exposed to the tapeworm S. solidus. Every two weeks the behaviour of the fish were recorded in three different areas: shelter use, escaping response when exposed to a model heron and swimming performance in a miniature ’flume’ tank. Out of the 30 sticklebacks, 5 developed infections and within 16 weeks the tapeworms had occupied 17-26% of the stickleback’s body weight. The conclusion from the results was that shelter use of the sticklebacks was significantly decreased but only when the parasites had grown to a weight of 100mg. When the sticklebacks where experimentally attacked by a model heron, the number reaching cover decreased with respect to the time after infection. Also, paratisised fish where slower at gaining weight than those which where uninfected. These results tend to the assumption that tapeworm infection of sticklebacks make sticklebacks more vulnerable to predation.
Conspicuousness may also be increased not only by behaviour but also by appearance. Many parasitic infections have the side effect of weight loss but a few have the opposite effect; making the host larger and therefore more noticeable. When rats are infected with plerocercoids, the parasite releases a hormone which results in the rats becoming large and fat. Colour changes can also increase conspicuousness and some parasites have the ability to be seen through the parasitised animal which makes them more noticeable in comparison to their uninfected counterparts.
Changes to behaviour due to parasites has also been found with respect to mating behaviour and social behaviour. Some changes such as the disruption of fish schooling which would leave the parasitised fish more exposed and therefore in danger of predation can be appreciated as ways to increase transmission. However, in most instances where mating and social behaviour is changed, it is unclear what the relationship is between these alterations and increased chances of transmission.
It can therefore be seen that the ways in which a host’s behaviour can be altered are very varied and broad and that they generally seem to be adaptations which mean that the parasite’s transmission is increased. However, it is still not clear that the changes in behaviour are always of benefit to the parasite. This is because some experiments have shown that altered behaviour of parasitised intermediate hosts has lead to predation by an animal other than the parasite’s definitive host. Also, occasionally the altered behaviour seems to have no effect or may even be harmful to the parasite, sometimes benefiting the host to a greater degree. Some experiments have involved several altered behaviours and in these cases there is very little way of knowing to what extent each individual behavioural change contributes to benefiting the parasite.
Despite the vast number of experiments which have been carried out, most experiments have been laboratory based with little thought to what would happen if the same situation occurred in the wild. Different methods have been used which means that many experiments are not suitable for comparative analysis. There is also a significant lack of statistical methods which have been used. Furthermore, hypothesises testing that parasite - altered behaviour is not advantageous to the parasite are rarely carried out which results in slightly biased and uncertain results.
In conclusion, parasite - altered behaviour is the understanding that a parasite is able to modify the behaviour of its host in order to benefit itself which is often in conjunction with it reaching a second host. Many different ways in which this can be achieved have been illustrated through scientific experiments, however more extensive work needs to be carried out before we can be sure that the ultimate reason for parasite - altered behaviour is to benefit only the parasite.
References:
Parasitism and Host behaviour - A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis
Barnard C.J and Behnke J.M
Taylor and Frances, London, 1990
Introduction to Animal Parasitology (3rd Edition)
Smyth J.D
Hodder & Stoughton, 1996
Medical Microbiology
Mims C.A et al.
Mosby - Year Book Europe Ltd. 2002
