Ants in Your Pants

January 31, 2020August 13, 2023 / creaturefact / Leave a comment

Ants. Can’t live with them, can’t live without them. They’ve been around for ages and outnumber us by over a million to one. They’re not just home invaders and picnic crashers; they’re the only other animal known to have sophisticated agriculture and manage herds of livestock. With more than ten thousand species to choose from, there’s an ant for every occasion. Did you rip your favorite shirt? Make friends with some weaver ants. Are you looking for someone to mow your lawn? Hire an army of grass cutter ants. Is life dull and you just want a thrill? Try bothering a stampede of African driver ants and get the adrenaline rush of a lifetime. I’ve mentioned ants before, but now is their time to have the spotlight.

African driver ants, or Siafu, are infamous for their nomadic colonies that devour anything and everything in their path. Blind soldiers with massive jaws guard the perimeters as the workers march on, carrying the young and the queen. Photo by Peter Steward on Flickr.

I couldn’t possibly cover every ant I would like to in this article, but I did manage to choose a select few, starting with the infamous bullet ant (Paraponera clavata). This ant is well known to have the most painful known insect sting in the world. As its name infers, the sting is likened to having a bullet wound. Justin Schmidt, a dedicated and somewhat eccentric entomologist, has painstakingly (pun intended) stung himself with as many insects as possible to compile the Schmidt Sting Pain Index. The pain of various insect stings, which he describes in wildly imaginative detail, are ranked from 1 to 4 (with 4 being the most painful). Can you guess who won that coveted number 4 on the scale? Take a moment. I’ll wait. Okay, now that you’ve guessed I can confidently assume that you thought about the bullet ant. After all, it is the star of this section. If you did choose the bullet ant, you’re wrong. That honor actually goes to the tarantula hawk wasp. No, the bullet ant doesn’t play by the rules. It has a sting so awful that it got its very own ranking of 4 plus. Not even the scale could contain the pain. As with many other animal toxins, bullet ant stings affect voltage gated sodium channels on cell membranes. This can wreak havoc on a cell’s ability to transmit signals, especially in the central nervous system (CNS). The blocked signals in nociceptors and skeletal muscles are what leads to the intense pain, paralysis, uncontrollable shaking, nausea, and more. The legendary sting of P. clavata is the reason it has become the gatekeeper of boys on their way to becoming warriors. The Sateré-Mawé tribe of Brazil has used this ant for years as part of a culturally important initiation rite. One sting is more than enough to cope with, but Mawé boys must endure multiple stings. Bullet ants are collected and dipped into a natural sedative to be safely woven into large gloves made from palm leaves. At the start of the initiation, a young man must slip both his hands into gloves filled with, now irate, immobilized ants. Only a thin layer of charcoal protects his hands and he must wear these gloves for five minutes straight and take the pain. What’s worse is the effects of the venom last well beyond these five excruciating minutes and boys hoping to become warriors must undergo this nightmare a total of twenty times before they are fully initiated. Forget jaguars, caimans, and anacondas. The Mawé people consider this humble ant to be the worst their rainforest home has to offer.

Great bullet ant photo by Graham Wise on Flickr.

Despite the potency of the venom delivered by the ant itself, one component may have medical significance. This compound of P. clavata, known as poneratoxin (PoTX), can have an analgesic effect in rats if administered in a small, controlled amount. Not only that, but it could potentially serve as a biological insecticide thanks to its ability to block transmission in the insect CNS.

Now it’s time for an ant that poses no threat to people, but is an amazing survivor. Meet the Saharan silver ant (Cataglyphis bombycina). This ant is capable of surviving conditions that would cook virtually any other living creature. In the Sahara desert, the surface of the sand can reach temperatures of up to 158℉ under the brutal midday sun. Several ingenious evolutionary adaptations give C. bombycina the ability to cope with this unforgiving environment while all others must either hide or perish. One strategy is to limit the time of exposure. Even these hardy ants will die if they are out on the scorching sands for long enough. That’s why they turn their foraging trips into a mad dash for their lives. Groups of ants leave their nest in a frantic search for other arthropods, such as desert beetles, that were too slow to escape the sun’s deadly rays. Once located, prey is dragged back to the nest as fast as possible via extraordinary teamwork. The poor animals that die and end up providing for these ants have succumbed to what is known as heat shock. Every living organism produces substances called heat shock proteins (HSPs). HSPs are tied to specific genes (heat shock genes) that, when activated by high temperature, are expressed and direct synthesis of HSPs by the cells. The purpose of these proteins is to protect the body from severe heat shock. Normally they are not produced until there is an environmental trigger, but Saharan silver ants start to produce them before leaving their nests. HSPs are synthesized preemptively to give the ants protection so they don’t die upon exiting their nest. This is because their foraging trips are usually too short to trigger synthesis of HSPs the normal way and the temperature rise would kill them before they got the chance. Not only are these HSPs produced before exposure, they continue to be synthesized beyond temperatures that would kill other animals, giving silver ants an even greater edge.

Another advantage over everyone else is long legs and a fast gate. Even though the sand itself may reach temperatures past what C. bobmbycina can tolerate, it is significantly cooler just a few millimeters off the surface. The long, stilt-like legs of this ant raise it off the sand just enough to keep its body below its critical maximum of 128.5℉. Long legs generally mean an animal can run faster, and C. bombycina is no exception. Its gait is a frenzied sprint that, at top speed, becomes quadrupedal. That’s right, these ants will actually lift their front legs off the ground completely to pelt forward as quickly as they can, and to minimize exposure to the sand. Running fast and limiting each foot’s contact with the ground allows them to go farther and keep cooler in their short bursts of foraging. They use the sun to navigate so that they can keep track of where they are in relation to their nest and how long they have been out.

Unfortunately, special proteins, great legs, and excellent navigational ability aren’t enough to beat the heat. Silver ants actually spend the majority of their scavenging forays offloading heat while sitting atop dry vegetation or stones. What allows them to do this so efficiently is the hair that gives them their name. These gleaming, silvery coats are what put them above and beyond everyone else when it comes to desert survival. Each individual hair is a triangular shape with two ridged surfaces and one smooth surface. The smooth surface sits against the body and the ridged surfaces face outward. When solar radiation hits the surfaces of these hairs, the ridges trap it and scatter that radiation back out in all directions. This is called “Mie scattering” and enhances the hairs’ reflectivity in the visible and near infrared range where solar radiation is at its strongest. In the mid infrared, the silvery hairs become antireflective and help the ants offload heat through emissivity. But what about the heat radiating off the ground? C. bombycina is prepared for that too. The undersides of their bodies are bare and reflect the mid infrared radiation from the sand better than if they were covered in hairs. All of these features, and more, combine to optimize survival and allow silver ants to be the lean, mean, foraging machines that they are.

There are countless ways to protect yourself from all kinds of threats if you’re an ant. Wearing what is essentially a heat shield or having a sting that will cripple your attacker with pain are just two. How about being heavily armored and using your head as a door to seal everyone out of your house? Using your own body as a barrier is called phragmosis and it’s what several genera of ants choose to do. Ants, as colonial animals, all have specific jobs to help their family. For ants in these phragmotic genera, usually the soldiers, that job is protecting the nest with their heads when the colony is threatened. The head structures, or cranial discs, that aid this can come in a variety of shapes and sizes that match their purpose. Some are even covered with sticky, fibrous secretions that accumulate environmental debris to help escape detection (cryptic phragmosis). Not only can they be used for blocking entrances, they can also be used like bulldozers to physically push intruders out of the nest. In one species of ant, Blepharidatta conops, it is the queen who possesses a head disc that she uses to block her nest chamber. The diameter is much too small to be of use blocking the nest entrance, but it certainly gets the job done when it comes to protecting her young. Perhaps one of the most diverse phragmotic genera is Cephalotes, also called turtle ants. In Cephalotes, generally all castes from workers to queens possess some kind of highly adapted head shield. These arboreal ants dwell high in the canopies of neotropical forests and use their heads to plug the holes of their wood cavity nests. They are also capable of gliding down from the canopy using what is known as Directed Aerial Descent, which is pretty cool. These ants are basically weird insect superheroes. Anyway, the morphology of the cranial discs prevents exposure of eyes, antennae, and mandibles to predators, just leaving them with a perfectly fitted, armored door to deal with. As mentioned before, these discs can be covered in organic material that sticks to glandular secretions, making entrances hard to locate in the first place.

For some really breathtaking photography of Cephalotes, please check out Alex Wild.

In a fantastic example of convergent evolution, there is a genus of Old World ant, Carebara, that has independently developed a very similar head shape to that seen in Cephalotes. The convex, shield-like head disc shape may have evolved independently even among separate species of Carebara. As ground nesting ants found in the leaf litter of African forests, Carebara workers have cephalic discs that collect soil and other debris, thereby camouflaging the nest entrances. They do not possess the sticky secretions of Cephalotes, but litter and soil easily collect on small hairs. When threatened by an intruder, they lock their heads down, making them both harder to see and the nest more difficult to invade.

Figure 1. from Fischer et al. 2015. The phragmotic workers of two Carebara species.

Reverse phragmosis has also been hypothesized, but as of now not proven, in the queens of the species Pheidole embolopyx. This is when the ant has a truncated (shortened), shield-like abdomen. So basically it’s a butt door. Or it would be if it was used to block nest tunnels. In the numerous experiments performed by E.O. Wilson and B. Hölldobler, not once did the study queen use her abdomen defensively. She always went on the attack, using her mandibles to nip at any threat they presented her with. She even turned completely around in her tunnel to attack the dissecting needle approaching her from behind rather than using her abdomen as a shield. It’s still a mystery what purpose this flat and potentially phragmotic abdomen serves. However, it does really reinforce the saying “Don’t judge a book by its cover.”

That goes for any of the ants in this article or anywhere in the world. Ants have a bad reputation and we’re all too quick to judge them and make assumptions based on the bad experiences we’ve had with a handful of species. In reality, there are trillions more ants out there that are just going about their own business, often in a truly fascinating manner, and want nothing to do with us. Let’s appreciate and think about those ants before we go judging any ant we see.

The wonderful Justin O. Schmidt sadly left us in February of 2023. He was an invaluable and pioneering contributor to the scientific community and will be dearly missed.

The “King of Sting”

References:

1. Rykaczewska-Czerwinska, Monika, et al. “Antinociceptive Effect of Poneratoxin (PoTX) in Rats.” Pestycydy, no. 1-2, 2008, pp. 135–141.

2. “Sateré-Mawé Initiation.” Culture and Customs, Penn State and WordPress, 16 Nov. 2015, 1:15pm, sites.psu.edu/mgeitnerrcl/2013/11/16/satere-mawe-initiation/.

3. Torres, A.f.c., et al. “Molecular Pharmacology and Toxinology of Venom from Ants.” An Integrated View of the Molecular Recognition and Toxinology – From Analytical Procedures to Biomedical Applications, 2013, doi:10.5772/53539

4. Palma, Mario Sergio. “Insect Venom Peptides.” Handbook of Biologically Active Peptides, 2006, pp. 389–396., doi:10.1016/b978-012369442-3/50059-3.

5. el-Showk, Sedeer. “Agriculture in Ants and Humans.” Scitable, Nature Publishing Group, 17 June 2013, http://www.nature.com/scitable/blog/accumulating-glitches/ant_agriculture.

6. Moore, Hannah. “Are All the Ants as Heavy as All the Humans?” BBC News, BBC, 22 Sept. 2014, http://www.bbc.com/news/magazine-29281253.

7. Gough, Zoe. “The World’s Most Painful Insect Sting.” BBC Earth, BBC, 13 Mar. 2015, www.bbc.com/earth/story/20150312-the-worlds-most-painful-insect-sting.

8. Gehring, Walter J., and Rüdiger Wehner. “Heat Shock Protein Synthesis and Thermotolerance in Cataglyphis, an Ant from the Sahara Desert.” Proceedings of the National Academy of Sciences, vol. 92, no. 7, 28 Mar. 1995, pp. 2994–2998., doi:10.1073/pnas.92.7.2994.

9. Zollikofer, Christoph P. E. “Stepping Patterns in Ants II. Influence of Body Morphology.” Journal of Experimental Biology, vol. 192, no. 1, 15 July 1994, pp. 107–118.

10. Shi, Norman N., et al. “Keeping Cool: Enhanced Optical Reflection and Radiative Heat Dissipation in Saharan Silver Ants.” Science, vol. 349, no. 6245, 18 June 2015, pp. 298–301., doi:10.1126/science.aab3564.

11. Alonso, José Ramón. “Flat Heads.” Mapping Ignorance, Dinahosting, 8 Jan. 2016, mappingignorance.org/2016/01/08/flat-heads/.

12. Brandão, C. R. F., et al. “The First Case of Intranidal Phragmosis in Ants. The Ergatoid Queen of Blepharidatta Conops (Formicidae, Myrmicinae) Blocks the Entrance of the Brood Chamber.” Insectes Sociaux, vol. 48, no. 3, Sept. 2001, pp. 251–258., doi:10.1007/pl00001774.

13. Fischer, Georg, et al. “Two New Phragmotic Ant Species from Africa: Morphology and next-Generation Sequencing Solve a Caste Association Problem in the Genus Carebara Westwood.” ZooKeys, vol. 525, 2015, pp. 77–105., doi:10.3897/zookeys.525.6057.

14. Yanoviak, Stephen P., et al. “Evolution and Ecology of Directed Aerial Descent in Arboreal Ants.” Integrative and Comparative Biology, vol. 51, no. 6, 2011, pp. 944–956., doi:10.1093/icb/icr006.

15. Wilson, E. O., and B. Hölldobler. “Caste-Specific Techniques of Defense in the Polymorphic AntPheidole Embolopyx (Hymenoptera: Formicidae).” Insectes Sociaux, vol. 32, no. 1, 1985, pp. 3–22., doi:10.1007/bf02233223.

Photo and Video Links:

1. Guarding the empire’s treasure by Peter Steward

2. Paraponera clavata by Graham Wise

3. https://www.youtube.com/watch?v=VbkgNDERlpU

4. Texas Turtle Ant, solider (Formicidae, Cephalotes texanus) by Alejandro Santillana

5. Figure 1

6. https://www.chemistryworld.com/careers/the-man-who-gets-stung-by-insects/2500173.article

Could “The Last of Us” Really Happen?

October 9, 2015August 25, 2023 / creaturefact / 3 Comments

UPDATE 4/19/22: Newer research has suggested that the ants that are infected with O. unilateralis are not in fact controlled via manipulation of the brain. Rather, there seems to be a chemical means by which the fungus forces the ant to bite the leaf vein. The study found no evidence of fungal cells inside the actual brain. However, hyphae were abundant throughout the head of the ant and the rest of its body, including inside the muscle fibers themselves, creating a complex network. The exact mechanisms behind the behavioral manipulation are still not known and more studies need to be done. With that in mind, please know that I am discussing the structure and function of ant brains in this article, as it helps exemplify the differences between an insect and vertebrate brain for the purpose of speculation.

For those who don’t know, The Last of Us is a dark, yet beautifully crafted survival horror game that explores what the world would be like if the majority of the human population were infected by a mutated strain of Ophiocordyceps unilateralis. This video game is critically acclaimed for its storytelling, graphics, and gameplay. It is considered a masterpiece by most of its reviewers and by its players. From the little bit I have played, I would absolutely agree. There are few developers that are able to take a real world scientific event, such as an insect being manipulated by a parasitic fungus, and implement the core concept realistically in a video game. Naughty Dog, the developer of The Last of Us, does this fantastically well.

Joel and Ellie are the game’s core characters

Ophiocordyceps unilateralis is in fact a real fungus. This species (actually a whole complex of species referred to collectively as Ophiocordyceps unilateralis sensu lato, meaning “in a broad sense” – I will refer to this species complex just as O. unilateralis from here) specifically targets ants, generally of the Camponotus genus, and takes over their bodies in order to move them to a location with ideal conditions for its reproduction. One of the most interesting things about this fungus is how precisely it manipulates its host. A 2009 study by Andersen et al. in The American Naturalist found that ants infected with O. unilateralis almost always died gripping a vein on the underside of a leaf (98%) and that this location was significantly more towards the north-northwest side of the plant than any other direction. Camponotus ants were found almost exclusively at a height of 25 centimeters from the forest floor, while closely related Polyrhachis ants were seen at a mean height of 78.43 centimeters. This kind of behavioral control is known as an extended phenotype. The gene expression of a parasite within a host’s tissue causes aberrant host behavior that increases the parasite’s fitness. Keep in mind that the ant species in the study colonize the canopy, not the forest floor, so this is extremely complex behavioral manipulation. Under the fungus’s control, these infected ants are traveling very far from their initial location. Many infected ants will often die in areas where others already have because the conditions in these places are favorable for O. unilateralis. This leads to places, called graveyards, that have a high density of corpses. Any healthy ant happening to walk through such an area will likely become infected by the deadly spores.

An ant with its jaws locked in a “death grip”.

When O. unilateralis spores come into contact with an ant, they adhere to it and start to penetrate its cuticle. After this, fungal cells start to infest the ant’s entire body and begin to alter its behavior. The infected ant then leaves the colony and starts the trek down toward the forest floor. Once a perfect spot is reached, the ant will bite the vein of a leaf and die with its jaws locked in place. This is known as the “death grip”, and keeps the ant from falling off the leaf. Any ants that end up dying within the colony due to infection will be carried far away by other workers. Within a few days, the stroma, or stalk, of the fungus will erupt from the back of its host’s head and develop a stromal plate that releases spores when mature. By this point, most of the ant’s original tissue has been replaced by fungus.

Saggital section of a dead Camponotus ant filled with fungus from The American Natrualist – W = white, Bl = black, O = orange, and P = pareithecial plate, which is where the spores originate. (The life of a dead ant: the expression of an adaptive extended phenotype. Andersen et al. 2009)

The ants in the video below are not Camponotus or Polyrhachis ants, and the fungus is not O. unilateralis so the hosts show a different behavior. However, it still illustrates the process well.

What a horror it would be if humans were susceptible to such a fate! The question is, could this actually happen? Let’s consider the ant brain for a moment. It has all the general features of a typical insect brain and is very simple compared to a vertebrate brain. However, ants have more well developed areas associated with memory and learning. These “higher” functions are controlled by the mushroom bodies. Mushroom bodies are much larger in worker ants than they are in the male soldiers. Workers must navigate varying spacio-temporal environments using multiple cues and also remember where food is and where home is. For ants, workers are the most “intelligent”. Still, one lone worker is of no use. It takes the whole colony to have a properly functioning and flourishing nest. An entire colony of ants, which can be up to millions of individuals, does not even come close to matching the complexity of a single human brain. If a fungus were to develop an ability to infect and alter the behavior of humans, this would probably take a ridiculously long time to evolve. Human beings would most likely not even be around any longer. But, let’s just roll with it and say that this could happen. What would it be like and how does The Last of Us compare?

Simplified ant brain from Recognition of social identity in ants (Bos and d’Ettorre, 2012).

We’ll start with the mode of infection. In the video game, people seem to become infected by breathing in the spores of the mutant O. unilateralis strain. Those who wear a special breathing bask in spore filled areas do not become infected. This appears to check out. Human skin is likely to be much less susceptible to becoming invaded by spores, simply because it is so much thicker and has many more layers than insect cuticle. Other fungi are able to infect hosts via inhalation (like some molds), so it would be no different for a mutant fungus; the infection would just result in a different pathology. So getting infected by this fungus is not in question if you breathe the spores in, but you can also fall victim if there is an exchange of bodily fluids, such as from a bite. This is logical as well. If the fungus has infiltrated an infected person’s system as in ants, bodily fluids like saliva and blood may contain fungal cells. These could easily be passed on to a healthy human.

What about the behavioral and morphological alterations? In The Last of Us, any infected individual, even in the early stages, is being driven by the fungus’ gene expression and aims to spread the spores or cells to as many others as possible. There are four main stages of infection from this mutant O. unilateralis: Runners, Stalkers, Clickers, and Bloaters. All of these collectively are referred to as the Infected (noun) in the game. Individuals who have just been infected are classified as Runners. They still cling to a shred of their humanity, however small, and try to resist the fungus’ behavioral control. However, if they are startled or as the infection progresses, they will snap and attempt to attack anyone nearby who is healthy. Stalkers are fully controlled by O. unilateralis and start to show fungal growth on the face. This fungus strain attacks the eyes first, so they have poor vision and begin to exhibit primitive signs of echolocation. In Clickers, the face has been fully engulfed by fungal growth and rendered the host completely blind. These Infecteds use clicking and screeching to crudely survey their surroundings within a small radius. The growth on the head and face forms a roughly dish shaped plate that helps to direct the clicks. Bloaters are the final stage and can take 10-15 years to develop. The entire body of this Infected is now covered in fungus, some of it showing bioluminescence, and is therefore very physically hardy. Bloaters are also able to throw sacs of toxic powder both as a defense and an attack mechanism. Once the host finally dies, whatever tissue is left of the former person crumbles and is used by the parasite to complete its growth and release spores.

The remaining tissues of the victim begin to crumble as the fungus spreads its spores.

Now to analyze the behavior of the Infected. All stages appear to seek out specific locations and stay there, unless stimulated to pass on the infection when a healthy individual is sensed nearby. This reflects the behavior of O. unilateralis controlled ants that travel until they find the optimal conditions for the fungus’s reproduction and then fix themselves to that spot. However, infected ants will leave the colony and do not show any aggressive behavior whatsoever toward other ants. Why would the Infected exhibit such an aggressive drive to bite or kill? We actually have a disease in existence that does just this. It’s called rabies virus. If rabies can infiltrate the brains of mammals and stimulate this type of behavior, it would not be a stretch to think that a mutant fungus could affect humans this way. Rabies in humans doesn’t present the same way that it does in other mammals; it resembles a bad flu, followed by agitated behavior and cognitive deficits, sometimes with hallucinations, delirium, and insomnia. Perhaps our mutant O. unilateralis would be able to incite the aggressive behavior seen in the games by affecting the brain in a similar way to rabies in non-human mammals. This could explain the Infecteds’ responses to healthy humans.

Clickers use crude echolocation to detect the presence of nearby humans and then go into a full sprint toward anyone they sense.

Runners display behavioral tendencies that would be expected. Since the fungus has only just started infiltrating the brain, it is not surprising that the victim would be scared and confused by what is happening. It makes sense that a person in this state would be very volatile and dangerous to approach. Stalkers tend to hide out of sight and only engage when someone lets their guard down. This is presumably because their vision is extremely poor and they must wait until the opportune moment in order to successfully attack. Clickers are harder to explain realistically. It would be highly unlikely that an Infected would suddenly develop the ability to navigate using clicks. This is a skill that must utilize learning and memory, parts of the brain no longer accessible to the victim. Very few humans are able to echolocate and those who are have refined their technique over years. Real world O. unilateralis is not able to direct ants to do things they are not already capable of; it simply takes advantage of abilities the insect already possesses. The sense that would be most beneficial to a Clicker is touch. Of course, sound is still an effective way of interacting with surroundings, but it would not be used for spatial navigation as in The Last of Us. This can be extrapolated to the Bloaters in the game as well, because they also use echolocation. All of these Infected will attack to kill. This is presumably because the fungus cannot kill immediately on its own, but can reach maturity faster in a dead body. So, when controlling a living human, O. unilateralis uses that person to its advantage by driving them to help speed up reproduction through the provision of corpses. If the host fails to make a kill, but manages to penetrate the skin of a healthy human, then the fungus still benefits because that person will become another Infected.

Bloaters take 10 to 15 years to develop and have hard fungal growth all over their bodies, giving them great resistance to blunt and penetrating forces.

Overall, the concept of The Last of Us is scientifically plausible, given enough time for O. unilateralis or a different species of Ophiocordyceps fungus to evolve the traits explored here. The intelligence and thought put into this game has given it so much more than most other video games can offer. These things make it different from your standard zombie apocalypse. It is scary because it feels like it could really happen, and this realness comes from its grounding in actual science. The infection seen in it is already a reality for many insects and other arthropods. They may not show the aggressiveness displayed by the Infected, but the behavioral manipulation seen in these animals is extremely effective at fulfilling the fungus’s needs. Maybe at some point in the future, the fictional scenario of The Last of Us could come to be. Who knows? The natural world is continually revealing so many things previously thought impossible.

References:
1. Gronenberg, Wulfila. “Structure and function of ant (Hymenoptera: Formicidae) brains: strength in numbers.” Myrmecological News 11 (2008): 25-36.

2. Evans, Harry C., Simon L. Elliot, and David P. Hughes. “Ophiocordyceps unilateralis: A keystone species for unraveling ecosystem functioning and biodiversity of fungi in tropical forests?.” Communicative & integrative biology 4.5 (2011): 598-602.

3. Hughes, David P., et al. “Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection.” BMC ecology 11.1 (2011): 13.

4. Andersen, Sandra B., et al. “The life of a dead ant: the expression of an adaptive extended phenotype.” The American Naturalist 174.3 (2009): 424-433.

5. Pontoppidan, Maj-Britt, et al. “Graveyards on the move: the spatio-temporal distribution of dead Ophiocordyceps-infected ants.” PloS one 4.3 (2009): e4835.

6. “The Infected.” The Last of Us Wiki. Wikia, 2013. Web. 7 Oct. 2015. <http://thelastofus.wikia.com/wiki/The_Infected>.

7. “Signs and Symptoms – Rabies.” Centers for Disease Control and Prevention. Centers for Disease Control and Prevention, 15 Feb. 2012. Web. 08 Oct. 2015.

Photo and Video Links:
1.http://static.giantbomb.com/uploads/scale_large/9/93770/2419553-397060_386577108098888_427807760_n.jpg

2.https://i.guim.co.uk/img/static/sys-images/Guardian/Pix/pictures/2010/12/21/1292935214310/a-dead-worker-ant-004.jpg

3.http://ento.psu.edu/publications/DH1

4.https://www.youtube.com/watch?v=XuKjBIBBAL8

5.http://journal.frontiersin.org/article/10.3389/fpsyg.2012.00083/full

6.https://vignette.wikia.nocookie.net/thelastofus/images/3/3f/Infected_Final_Stage.jpg/revision/latest?cb=20130224030859&format=original

7.http://vignette4.wikia.nocookie.net/thelastofus/images/9/9d/Clicker.jpg/revision/latest?cb=20150928101722

8.http://vignette4.wikia.nocookie.net/thelastofus/images/8/8f/Bloater.jpg/revision/latest?cb=20150928101859