Zombies Pt 2 (or how I distracted my students)

Last week I mentioned how my students sidetracked me in a tute regarding introductions to the origins of life and in particular the acronym HOMR standing for Homeostasis, Organisation, Metabolism and Replication by initiating a discussion of whether or not zombies technically were alive. Well, the following week they had a test that occupied half the allocated tutorial time so instead of letting them out early I extended the discussion to real world zombies.

After a little investigation it became clear that ‘zombism’ is a lot more common in nature than I expected. While not true zombies the examples I have below represent some of natures best approximation of living dead.

The first one I quite liked was The North American Wood Frog (Rana sylvatica), which undergoes an extreme return from the dead each year.

Sup? I'm just defrosting.

The winter hibernation in northern North America is very important because of how long and extreme it can be. To up the challenge the wood frog hibernates in the leaf litter and consequently freezes solid during winter. By solid I mean properly solid. The frogs can survive multiple freeze/thaw events as long as less than 65% of their water remains unfrozen. Freeze/thaw stops my experiments on bacteria from working but apparently these frogs are just fine. To survive the big freeze the frogs accumulate urea in the tissues and build enormous glycogen stores which breaks into glucose upon ice formation in the tissues. The soluble urea and glucose prevent ice formation and save the frogs. This phenomenal life cycle enables easier and early access to the natal ponds where eggs are laid and tadpoles develop and must leave before the thawing dries up the pools. So the question was posed, is a wood frog alive during winter hibernation? Technically it's dead, no heartbeat, no metabolism and yet it survives. Does this make it a reanimated corpse? Very spooky.

There are lots of zombie ant variations that I could go to but my two favourites are zombifying fungi Ophiocordyceps unilaterius, which zombifies Camponotus leonardi ants and Dicrocoelium dendriticum which zombifies Formic fusca (the European common black ant).

All ants are creepy up close (Photo Credit: D. S. Sikes)

O. unilaterius infects the worker ants via its respiratory system and quickly spreads throughout the ant's body. Importantly the fungus spreads into the brain and the result is the ant alters the way it responds the pheromone messengers.

The zombieness of this interaction does not come from the death of the ant but instead the ant’s loss of ant-ness. Infected ants leave the colony (and in some cases are removed by the colony members directly) and climb. The climbing is very important as the fungus can only grow at a particular temperature and humidity. The ant must locate these conditions based on the chemical instructions of the fungal controller. Once a suitable environment has been found the ant performs its final act, it climbs underneath a leaf and grips with its mandibles, never to let go. Why the underneath? Because the fungus is sensitive to UV light. The fungus continues to grow and kills the ant in the process eventually resulting in the emergence of fungal stalks covered in spores that are sprinkled on the ground near the ant colony that provided the last victim.  Is the ant, which continues to satisfy HOMR (except for the ‘R’ that it never did that anyway), actually alive when the fungus takes over? Or is it an animated corpse?

Not as creepy as when they look like this though.

Similarly the Formica fusca have to deal with the mind-controlling pathogen Dicrocoelium dendriticum also known as the Lancet Liver Fluke. The adult flukes reside in the livers of cattle and other grazing mammals and its eggs are released in the faeces of that animal. The eggs sit happily in the poo until consumed by snails. Once eaten the flukes drill into digestive tract of the snail where they develop into juvenile flukes. Obviously the snail would prefer that this didn’t happen and so attempts to wall the flukes of in cysts. It is these cysts that are eventually released by the snail.

The cysts are left behind in the snail trails, which are harvested by the F. fusca and as such this is how they get infected. Similarly to the activity in the snail most flukes get caught up in cyst but one fluke navigates to a bundle of nerves in the ants oesophagus and from there it controls the ants activity.

As the night air cools the infected ants leave the colony and ascend the grass blades and clamp down on the tops with their mandibles and waits. If nothing happens during the night the ant decends in the morning as the temperature rises and it rejoins the colony. However, occasionally a grazing animal will eat the ants along with the grass allowing the infective process to start all over again. Again is this ant alive during the day but a reanimated corpse at night?

Loner ant waiting to be consumed.

Like the fungus and fluke before it the pathogenic barnacle Sacculina is a mind controller but this barnacle has an even more sinister side. Sacculina are castrating parasites of crabs and their lifecycle is as fascinating as it is weird. A female Sacculina will find and attach to a crab exoskeleton and then move around on its surface looking for a gap through which it can invade. It then ejects its own hard shell as it invades the crab’s interior. Once beneath the skeleton the Sacculina infiltrate all parts of the crab but specifically have activity at the genitals of the crab. The male crabs are castrated and rearranged to become females and the female’s egg sack is infiltrated and becomes Sacculina’s new home.

In its new home the parasite prevents the crabs natural molting and regrowing of limbs, as this is not nutritionally beneficial to the parasite, which prevents the crab from growing and repairing damage. Over time a male Sacculina finds the lady Sacculina in its crab host and fertilises her eggs inside the crab. The crab is further manipulated to develop nurturing characteristics and behaves exactly like a pregnant lady crab should. Once ready to be released the crab follows its normal birthing behaviour of climbing to a high rock, massaging her egg sack and swirling her claws to improve water flow except this time they are parasites and not crabs. Ultimately the crab dies as the parasite leaches nutrient faster than the crab can aquire it but in the mean time it has acted as a mindless vehicle for the construction or more zombifying parasites.

A double infection? Could this get any worse? Yeah actually, given the crab will eventually die.

The last one I wanted to mention is Toxoplasmosa gondii. A friend of mine wrote this little guy up here at little while ago but a quick summary of the facts wouldn’t go astray here I don’t think. T. gondii is a protozoan of cats spread primarily in their faeces but that doesn’t mean you wont get it. In fact estimates that as many as 16% of 12 year olds have previously been infected by T. gondii suggest that we eat more cat poo then we should. Having said that, eating poorly prepared meat is much more likely to give you the parasite.

In any case the cats are rarely significantly affected by the infection and even in humans the infections are often subclinical. Or are they?

Sustained infection of the human host has been linked to mental illness and, of all things, traffic incidents.

It also seems that we might be able to explain the ‘crazy cat lady’ on The Simpsons or any other TV show with a ‘scary old woman + cats’. Infected women apparently become generally more extroverted, show decreased inhibition and increased promiscuity while also exhibiting increased intelligence. Conversely men get the opposite, generally introverted and anti-social. Thus crazy cat ladies and crazy cat men rarely meet to produce crazy cat children.

Crazy cat lady and her kitteh quilt

Zombies seems more prevelant in nature than I ever expected it would be and while full zombification (rotting flesh and eating of brains) is not seen complete hijacking of organisms internal and external environments is performed routinely by nature’s little zombifiers, the parasites, and their actions are way to zombie-like for me to stay comfortable.

References

Costanzo JP, Lee RE Jr, & Lortz PH (1993). Glucose concentration regulates freeze tolerance in the wood frog Rana sylvatica. The Journal of experimental biology, 181, 245-55 PMID: 8409827
Andersen, S., Gerritsma, S., Yusah, K., Mayntz, D., Hywel‐Jones, N., Billen, J., Boomsma, J., & Hughes, D. (2009). The Life of a Dead Ant: The Expression of an Adaptive Extended Phenotype The American Naturalist, 174 (3), 424-433 DOI: 10.1086/603640
Jones JL, Kruszon-Moran D, & Wilson M (2003). Toxoplasma gondii infection in the United States, 1999-2000. Emerging infectious diseases, 9 (11), 1371-4 PMID: 14718078
PHILLIPS, W., & CANNON, L. (1978). Ecological observations on the commercial sand crab, Portunus pelagicus (L.), and its parasite, Sacculina granifera Boschma, 1973 (Cirripedia: Rhizocephala) Journal of Fish Diseases, 1 (2), 137-149 DOI: 10.1111/j.1365-2761.1978.tb00014.x
Tarry, D. (2009). Dicrocoelium dendriticum: The Life Cycle in Britain Journal of Helminthology, 43 (3-4) DOI: 10.1017/S0022149X00004971