Animal behaviorists study the evolutionary and ecological underpinnings of animal behavior. We jot down details about the particular behavioral quirks of an animal and code an ethogram to catalogue these traits. What if some of these animals had no control over their behavior and are in fact being manipulated by other creatures nestled deep within their brains? Does this sound like the start of a bad zombie movie trailer? Well, we don’t need to turn to science fiction for our fix of blood and gore! There are a host of creatures (pun very much intended!) that live out their entire lives inside other animals and often manipulate their hosts’ behaviors1. Some of these parasites even require multiple species of hosts at different stages of their life cycle, and a particularly fascinating example is the parasitic helminth, Euhaplorchis californiensis. Funnily enough, many parasite species are known only by their scientific name which makes them sound even more alien than they already are. Let’s refer to this particular parasitic worm as “Euha”, to avoid alienating an already under-appreciated taxonomic class of animals.
Check out the dark eye-spots on this Euhaplorchis californiensis cercarial trematode. Perhaps our brains are primed to associate more readily with animals that have eyes, but this cute-looking creature is actually a deadly mind-controlling agent par excellence. [Source, taken by Todd Huspeni]
Euha lives an incredibly complex life; scientists have described it as a tropically-transmitted parasite (TTP). TTP’s are parasites that are transmitted through the trophic or food web. Think back to your first or second grade science class: remember those fun food webs with plants, herbivores, carnivores, and arrows linking these different types of animals? Well, TTP’s basically use those “links” between different trophic levels as highways for their own development. Euha eggs are released in the environment in the droppings of an infected host animal, usually a piscivorous (i.e. fish-eating) bird. These eggs are then ingested by unwary mud snails (Cerithidea californica) which develop and leave the snail only to infect the Pacific killifish (Fundulus parvipinnis) which in turn are snatched up by a hungry bird, and so the life cycle continues2. That’s three different host animals: talk about a long-distance migration!
Life cycle of the trophically-transmitted Euhaplorchis californiensis trematode. [Source images 1, 2, 3, 4]
Euha has fascinated scientists for decades, but what is particularly astonishing is their ability to control the behavior of the host species they are infecting. Experimental studies have demonstrated that killifish infected by Euha exhibit…unusual behaviors compared to uninfected fish. The scientists who first described this parasite manipulation coded weird behaviors in killifish that were engaging in “surfacing, flashing, contorting, shimmying, and jerking”2. While it might sound like Euha was just the dance-instructor equivalent of a Babel fish, the repercussions are actually quite severe. Flash-dancing killifish exposed the lateral and ventral surfaces of their bodies far more frequently: these surfaces are a lighter color and make the killifish more conspicuous (see details on countershading and why fish are colored this way). In addition, infected fish spent more time at the surface of the water compared to uninfected fish. This makes them a much easier target for predators like fish-eating birds.
Researchers from the University of California Santa Barbara (UCSB) discuss Euhaplorchis californiensis and its ability to manipulate Pacific killifish behavior.
How does Euha actually control its hosts’ behaviors? Euha has an immediate reproductive cost on its intermediate snail host: it castrates the snail and takes over its energy reserves to produce multiple copies of infective cercariae2. These cercariae leave the snail and swim in search of their next intermediate host, the killifish. Once inside the fish, Euha migrates to the brain and encysts in a dormant stage known as the metacercariae. The Euha metacercariae themselves do not appear to prevent growth or reproduction in infected killifish3. Instead, the parasite appears to selectively control the locomotor behaviors of its host. Those jerky dance moves can be attributed to an increase in monoaminergic activity in the hippocampus and the raphe nuclei3. These specific brain-regions have high densities of serotonin-producing neurons. Fish that had more metacercariae (per body mass) thus had less serotonergic activity, which has been associated with a stress response in other fish species3. High serotongeric activity is associated with predatory-avoidance behaviors by inhibiting movement in the animal. Thus, an infected brain may not respond to this “freeze” switch, which might otherwise protect a threatened fish.
Note in the bottom image the conspicuous black circles that represent individual Euhaplorchis californiensis metacercariae in a cross-section of a killifish brain. An unparasitized kilifish brain is shown above for comparison. [Source]
However, the experimenters who determined that this control-mechanism might be at play in Euha-infected killifish are cautious. They could not conclude that the aforementioned conspicuous movements were attributed to this modified brain activity, as they were unable to conduct behavioral observations in the field3. Their work and work by others underlines the need for more field and experimental studies that examine parasite-mediated behavioral modification, which may exert an important selective pressure on animal behavior. For example, infection of the closely-related banded killifish (Fundulus diaphanus) by a different trematode worm species results in darkened spots on parasitized fish. This phenotypic trait is potentially used by unparasitized fish as a marker for shoal preference: fish may evaluate whether or not to join a particular shoal depending on the parasite load of the members in these shoals4. Lowly parasites like Euha, that tend to elicit a slew of negative reactions, might in fact have important consequences on the survival and reproduction of many of the more charismatic animal species we know and love.
[By: Neetha Iyer]
References:
- Klein, S. L. (2003). Parasite manipulation of the proximate mechanisms that mediate social behavior in vertebrates. Physiology & behavior, 79(3), 441-449.
- Lafferty, K. D., & Morris, A. K. (1996). Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology, 77(5), 1390-1397.
- Shaw, J. C., Korzan, W. J., Carpenter, R. E., Kuris, A. M., Lafferty, K. D., Summers, C. H., & Øverli, Ø. (2009). Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proceedings of the Royal Society of London B: Biological Sciences, 276(1659), 1137-1146.
- Krause, J., & Godin, J. G. J. (1996). Influence of parasitism on shoal choice in the banded killifish (Fundulus diaphanus, Teleostei, Cyprinodontidae). Ethology, 102(1), 40-49.
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