Behavior manipulators. The organisms capable of breaking the will

Behavior manipulators. The organisms capable of breaking the will

Behavioral control has always aroused deep fears. For instance, the mere idea of the existence of institutions and projects that have tried to manipulate the most private and apparently untouchable aspects of an individual arouses evident uneasiness. However, human being is not pioneer in behavioral control techniques. In nature, several species have been practicing these strategies for billions of years. In this article, we expose some of the most fascinating cases.

It is logical to think that members of the ruling classes have tried to facilitate their government over others in different ways, possibly since the first hierarchies in human societies were formed. One of these ways is through behavior manipulation and redirection of social groups located at lower levels. There have been many techniques and procedures we have tried to achieve this goal. From the most relatively moderate, such as the propagation of toxic propaganda, to the most invasive. In the latter case, the inhumane experiments carried out in the framework of the MK-Ultra project, an operation led by the CIA during the 1950s and 1960s whose objectives were to break the will through electroshock, drug inoculation, hypnosis and other methods, are noteworthy.

Nevertheless, we were not the first. In fact, a wide variety of cases can be found in the animal kingdom, in which an organism is able to modify the behavior of another at will in order to obtain a series of benefits. In general, these kind of relationships happen in the field of parasitism, one of the many relationships between species or interspecifics that can develop under certain evolutionary conditions.

First of all… What is parasitism?

Broadly speaking, parasitism is a relationship between different species in which one of them is able to benefit to the detriment of the other. We call a parasite to the organism that obtains the benefit at the expense of the host, that is, the organism that suffers from the parasite and its damages. Even if we do not take into account, parasitism is one of the most important ecological relationships that exists in nature and that largely determines the survival of species and individuals. As a typical example of this interaction, we could imagine the relationship that is established when a tapeworm of the genus Taenia reaches the intestinal tract of a human being: the tapeworm steals the necessary nutrients to feed and reproduce in its host while the infected individual suffers the consequencies, which in some cases result in abdominal pain, appetite loss, etc…

taenia
Escolex or heads of three species of the genus Taenia seen with a microscope. CDC

Moreover, the development of a relationship of parasitism may be compared to a sort of arms race led by evolution. Both host and parasite are constantly trying to overtake each other through the development of different strategies. Biologists call this event the “Red Queen hypothesis”. Nowadays we know a great variety of strategies that parasites develop to ensure their survival, and one of them is the one we are going to expose in this article: the manipulation of behavior.

Malaria, an expert manipulator

A paradigmatic case of manipulation is that of the malaria causing agent: the protozoan of the genus Plasmodium sp. It is difficult to imagine that such a small being could trigger such impressive physiological effects. To understand how this parasite works, firstly it is necessary to remember what malaria is.

Malaria is a fatal and dangerous disease that principally strikes tropical and sub-tropical countries with limited health resources. Without treatment, it can become a deadly disease. In fact, in these countries is one of the leading causes of mortality. Only in 2016, malaria caused nearly 445000 deaths, mostly in tropical African countries. Mosquitoes of the genus Anopheles sp. are the main reason why malaria infects so many people. Through this invertebrate, malaria is able to pass on from one mammal to another. And behavioral control happens in this stage.

mosquito-anopheles
The Malaria parasite is capable of physiliogically manipulating the Anopheles mosquito to reach a great number of hosts. Insuficiencia renal crónica El Salvador

Under normal conditions, mosquitoes are usually satisfied with the blood of their victims by biting as little as possible. It is logical, since the more times they try to bite, the more is the risk of being hit. Additionally, to facilitate blood intake, their salivary glands secrete a substance that causes their victims’ blood to remain fluid and not to coagulate. The problem is that this behavior is counterproductive to Plasmodium, as it seeks to reach more hosts to maximize the dispersal of its populations. Therefore, the parasite has to do something. It is known that when Plasmodium infects the mosquito, it ends up in the salivary glands of the insect. This is where the protozoan exerts its influence preventing the anticoagulant substance from  forming correctly and thus not functioning properly. Therefore, the mosquito cannot prevent the coagulation of its victim’s blood and cannot absorb the vital fluid. Then, the insect is forced to visit more hosts until it is completely satisfied and, in the process, it leaves the malaria parasite in more stops.

However, Plasmodium is capable of manipulating the insect in reverse. Keeping in mind that the mosquito is essential for the protozoan to complete its life cycle, Plasmodium needs somehow to return to a mosquito from the mammal it is in. To this end, Plasmodium emits a series of substances that difficult blood coagulation. This favors the mosquito to stay longer feeding on the individual infected by Plasmodium. In consequence, the protozoan has more probabilities to arrive to the invertebrate.

Zombie ants

Among the great diversity of examples of behavioral manipulation, ants are often tragic protagonists of many of them. This is the case of the ant species Formica fusca, which can be parasitized by the flatworm Dicrocoelium dendriticum. This worm reaches its victim through a snail, another host necessary for this parasite to complete its life cycle. The snail’s mucus is an irresistible food for these ants, but also a very effective transmission route for the parasite. The end of the cycle is a mammal, usually a bovine. However, to transfer from an ant to a cow for example is very complicated, since cows do not feed on ants and it is very difficult to accidentally ingest any when they live at ground level. Nevertheless, the worm has little concern about this obstacle and has developed a spectacular strategy.

When the worm reaches an ant, it goes through a series of phases at the same time as it migrates towards the proto-brain of the insect, where it ends up becoming deeply embedded. From then on, the ant behaves in an extravagant way. At certain times of the day, the ant breaks its routine against its will and does something very strange: it climbs to the top of a blade of grass or a plant, gets hooked with its strong jaws and lifts its abdomen to the heights. Like a born gymnast, he does a handstand. In this peculiar way, the parasite has managed to considerably increase the chances of a cow to ingest the ant it has infected.

Ciclo_Dicrocoelium_dendriticum
Life cycle of the parasite flatworm Dicrocoelium dendriticum. CDC

Another similar case occurs when ants of the genus Camponotus sp. are invaded by the spores of a fungus of the Ophiocordyceps unilateralisgroup. Similar to the previous case, infected ants behave erratically, climb to the tops of grass blades or other plants and become strongly attached with their jaws. However, unlike the previous case, the ant ends up dying shortly after and like a gargoyle, it remains motionless at high altitudes. Thus, the fungus is able to be located at a higher and more favorable height for the dissemination of its spores.

hormiga_infectada
A fungus emerges from the corpse of its host to disperse its spores. Un paseo por la zoología

Signals for calling the attention

If the above examples are fascinating, the following are no less so. Because another of the strategies of some parasites is to attract the attention of their next host by emitting visual signals.

In this regard, snails of the genus Succinea sp. have very bad luck. Obviously, like any other species, they try their best to survive and avoid predation. But many times they can’t. And all because of the fungus Leucochloridium paradoxum, which is capable of infecting them. To complete its life cycle, this fungus needs, in addition to the affected snails, some species of birds. And as in other situations, it is difficult to move from a snail to a bird. However, the fungus has its tricks. When it infects a snail, the parasite develops a series of elongations that extend to the tentacles of the mollusk. What is most striking is that these extensions emit color pulses during the daylight hours. Several researchers have suggested that these color pulsations (which change between black, green-yellow and white, all of which are very striking colors) would mimic the movement and color of some very appetizing caterpillar for certain birds that would serve as the final host to the fungus. To make matters worse, the fungus can also force the snail to expose itself to its predators as much as possible, encouraging it to climb to high places, to leave dark or shaded areas, etc.

Cephalotes_atratus_parasitada
Comparison between a non-parasitized ant of the species Cephalotes atratus with a parasitized ant. Science Daily

And going back to ants, there is a species that can change the color of their cuticle… involuntarily. And this is due to infection by a worm known as Myrmeconema neotropicum. Its hosts are the already mentioned ants (of the species Cephalotes atratus) and birds. Nowadays it is known that when the worm infects these ants, the color of the upper abdomen (which in normal conditions is black) turns red. This is due to the fungus ability to cause a thinning of the cuticle in this area, exposing the striking red. Not only that, but the manipulation of behavior also includes that infected individuals roam through areas with an abundance of red berries with a color similar to that of their modified abdomen. Birds are likely to confuse the berries with the ant and hopefully the parasite will end its life cycle in the winged host.

Loss of fear

The outcome of the parasitized host depends largely on the form of spread of the parasite and the habits of the next hosts that the parasite needs to invade. Obviously, the parasite will do its best to showcase its adaptive success. And to this end, any action is valid, including the inducement to commit suicide.

In this regard, it is worth mentioning the parasitosis that some insects that avoid water can suffer from certain species of very fine and long worms: the nematomorphs or hairworms. These animals begin their reproductive cycle inside aquatic insect larvae. When the parasite gets out of the water together with its host (already metamorphosed in some terrestrial phase), it looks for a terrestrial insect to continue its cycle, for example a cricket. However, this parasite needs to re-colonize an aquatic larva to complete its cycle, while the cricket escape from water to avoid death. Even so, the will of the parasite prevails over the will of the insect and finally gets its host to throw itself fearlessly into the water, where it will drown while the parasite leaves the body of the corpse in search of its new host.

parasito_Paragordius-tricuspidatus
A hairworm emerges such as a Ridley Scott’s alien from the corpse of its drown host. Muy Interesante Spain

There are also several cases of this type of lethal manipulation in animals with a more complex nervous system. A paradigmatic example is that of the toxoplasmosis causing agent: the protozoan Toxoplasma gondii. It is well known for its dangerousness to pregnant women, because if they become infected during pregnancy the parasite can infect the fetus and cause him serious harm. It is also often related to cats, and in fact our feline friends are hosts of this protozoan. The other hosts that protozoan needs to complete their life cycle are rodents or some species of birds, while humans can be an accidental host in case they come into contact with cat faeces containing the parasite. Among all of them, rodents are the mainly that suffer from behavioral changes. It is well known that a mouse runs away from a cat for survival. However when mice are infected with Toxoplasma gondii, which colonizes certain regions of the brain, mice lose their sense of fear and even are attracted to stimuli such as the smell of cat urine, inevitably precipitating them to their end and the parasite to a new beginning.

gato_roeador_toxoplasma
Rodents infected by Toxoplasma gondii lose the fear to their predators. Vix Explora

Unfortunately, we cannot get away and we can also be victims of behavioral manipulation by beings infinitely smaller than ourselves. Following the previous example, Toxoplasma gondii is also capable of manipulating us. In fact, strong correlations have been found between parasitized men and certain behaviors, such as being more introspective, susceptible and emotionally unstable. Also, some researchers have suggested that there is a link between being parasitized by Toxoplasma and being more predisposed to car crashes. In addition, several authors have suggested that some cases of schizophrenia and epilepsy may be due to brain damage caused by the protozoa. Even so, there aren’t solid conclusions about what benefits the parasite might gain from these strategies.

Parasitology opens up a wide range of research pathways and questions that are worth answering. More research is needed to answer these questions, but one thing is clear: in behavior control, as in so many other areas, nature is one step ahead.

REFERENCES

  • Berenreiterová, M., Flegr, J., Kubena, A.A. & Nemec, P. (2011). The distribution of Toxoplasma gondii cysts in the brain of a mouse with latent toxoplasmosis: Implications for the behavioral manipulation hypothesis. PLOS ONE 6(12), e28925.

  • Center for Disease Control and Prevention CDC (2018). Parasites[online] available in: https://www.cdc.gov/parasites/index.html

  • Da Silva, R.C. & Langoni, H. (2009). Toxoplasma gondii: host-parasite interaction and behavior manipulation. Parasitology Research 105, 893-898.

  • De Bekker, C., Will, I., Hughes, D.P., Brachmann, A. & Merrow, M. (2017). Daily rhythms and enrichment patterns in the transcriptome of the behavior-manipulating parasite Ophiocordyceps kimflemingiaePLOS ONE 12(11), e0187170.

  • Flegr, J., Havlícek, J., Kodym, P., Malý, M. & Smahel, Z. (2002). Increased risk of traffic accidents in subjects with latent toxoplasmosis: a retrospective case-control study. BMC Infectious Diseases 2, 11.

  • Merino, S. (2013). Diseñados por la enfermedad. El papel del parasitismo en la evolución de los seres vivos. Madrid: Síntesis.

  • New York Times (2018). Project MKUltra, the CIA’s program of research in behavioral modification [online] available in: http://www.nytimes.com/packages/pdf/national/13inmate_ProjectMKULTRA.pdf

  • Poinar Jr, G. & Yanoviak S.P. (2008). Myrmeconema neotropicum g., n. sp., a new tetradonematid nematode parasiting South American populations of Cephalotes atratus (Hymenoptera: Formicidae), with the discovery of an apparent parasite-induced host morph. Systematic Parasitology 69, 145-153.

  • RBM Partnership (2017). About Malaria [online] available in: https://rollbackmalaria.com/about-malaria/

  • Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P & Renaud, F. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behavior of their terrestrial hosts? Journal of Evolutionary Biology 15, 358-361.

  • Verble, R.M., Meyer, A.D., Kleve, M.G. & Yanoviak, S.P. (2012). Exoskeletal thinning in Cephalotes atratusants (Hymenoptera: Formicidae) parasitized by Myrmeconema neotropicum (Nematoda: Tetradonematidae). Journal of Parasitology, 98(1), 226-228.

  • Wesolowska, W. & Wesolowski, T. (2013). Do Leucochloridiumsporocysts manipulate the behavior of their snail hosts? Journal of Zoology 292, 151-155.

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