Update (09/14/10): After a few months of blogging on my own, I’m proud to say that Laelaps has made the jump over to the new WIRED Science blogging network. Click here to check it out.

By now you have probably heard about my new neighbor here on ScienceBlogs, a nutrition blog called Food Frontiers. It is a corporate blog run by PepsiCo. I wish I were kidding.

The offending blog, which has already been operating for some time on the PepsiCo website, greatly diminishes the credibility of ScienceBlogs by providing a corporation with a platform to advertise to readers without actually calling it advertising. A newspaper or magazine would not allow PepsiCo to write articles about global health or nutrition – there is a very clear conflict of interest there – so I am absolutely dumbfounded as to why the SEED management team thought it acceptable to give the corporation space here. If PepsiCo wants to have their R&D scientists blog on their own site, that’s fine, but in moving Food Frontiers to ScienceBlogs, the company is trying to trade in on the reputation I and other Sb bloggers have built while simultaneously tarnishing that reputation.

The launch of the PepsiCo blog sharply underscores my mounting frustration with SEED. The SEED management team has repeatedly failed to treat me and my fellow bloggers with courtesy and respect, and this latest event goes beyond disrespect into actively undermining our credibility. Hence I am putting Laelaps on hiatus until I determine what is best for my writing. This is not the end of Laelaps – I will keep writing somewhere, and you can always check out my blog Dinosaur Tracking on the Smithsonian website – but if SEED insists on valuing corporate money over creativity, honesty, and integrity, then I will have no choice but to move elsewhere.

For more on this controversy, see these posts from PalMD, Abel, Isis, Janet, Zuska, Blake, Christie, Sharon, Jason, Greg, Orac, PZ, Mark, and GrrlScientist, as well as the notes from James H., Alex Wild, Scicurious. I am also sad to say that Blake and David Dobbs have left Sb, but I am glad that they will both continue to write at their respective blogs.

In one of my favorite episodes of the animated TV show Futurama, the chief protagonist – delivery boy Philip J. Fry – becomes infested with worms after eating a dodgy egg-salad sandwich purchased from the restroom of an interstellar truck stop. Lucky for Fry, the parasites are beneficial – they repair his injuries and greatly enhance his cognitive abilities. (“Of all the parasites I’ve had over the years,” Fry explains to his coworkers, “these worms are among the… – hell! They are the best!”) The giant gliding ants (Cephalotes atratus) of Central and South American rainforests are not so fortunate. They, too, often become infested with a peculiar kind of worm, but these worms trigger a startling metamorphosis which transforms the ants into walking transports for the next generation of nematodes.

Naturalists have long recognized the ability of parasites to influence the behavior of their hosts. Among ants, especially, almost everyone has heard of the fungus Cordyceps unilateralis which causes “zombie” ants to climb up high and clamp down on a branch before the fungal stalk erupts from the back of the ant’s head. A previously unknown species of nematode worm – mentioned by scientists S.P. Yanoviak, M. Kaspari, R. Dudley, and G. Poinar Jr. in the April 2008 issue of The American Naturalist – also changes the attributes of its ant hosts, but in a very different way.

While studying giant gliding ants in the forests of Panama in May of 2005, the authors of the study noticed that the gasters (the bulbous, terminal part of the ant abdomen) of some individuals were bright red in color and held conspicuously high. This condition was first described in these ants over a century ago – they were even proposed to be a distinct type of ant in 1894 because of it – but no one knew what caused it. Yanoviak and colleagues found the answer. When they opened up the gasters of these ants they found hundreds of tiny, transparent eggs with tiny nematode worms inside. Closer inspection showed that the worms were a species hitherto unknown to science – a tetradonematid nematode similar to species which infest flies and beetles, but causing physical changes never before seen in an arthropod.

Through observations of four infested colonies in the field and tests in the lab, the scientists were able to determine that the worms were using the ants to further their life cycle. As the researchers initially observed, the gaster of an infested ant will turn red (due to a thinning of the exoskeleton which looks red when combined with the nematode eggs), be held high almost constantly, and is easily detached from the rest of the body. The ants are also docile and sluggish; they fail to bite or give off alarm pheromones when faced by a threat.

The docility of the ants and their bright-red gasters make them easy targets for birds, the next essential part of the nematode life cycle. Birds have not been directly observed to consume these ants, but as the researchers found when they presented infected ant gasters and different colored clay balls to birds in the field, birds were highly attracted to what they perceived to be red or pink colored berries, and a test with a captive chicken showed that the nematode eggs could survive going through the bird digestive system. This was important, as the ants regularly pick up bird feces as they forage, making it relatively easy for an avian carrier to leave feces at a distant site where a different ant nest will pick up the feces (and hence the parasites).

It is not the adult ants which initially become infested, though. An internal filter-like organ prevents the nematode eggs from passing far enough to become established in their bodies. Instead, the colonies become infested when workers feed the bird feces to larvae in the nest. The juvenile nematodes take up residence inside the larvae, stunting the young ant’s growth (infested ants are about 10% smaller than healthy ones), and from there the worms grow and mate. The male worms die, but the females lay eggs in the gaster of the ant, and it is about this time that the host ants are switching from working in the nest to foraging outside the nest, a time when the ants will be susceptible to predation by birds.

As the authors note, there are at least two alternatives to this scenario.

1) It may be that the bodies of dead infested ants are being fed back to the colony, thereby continuing the nematode lifecycle. For the parasite to spread to new colonies, however, queens carrying the nematodes would have to successfully establish nests in new areas (unlikely if the nematodes suck resources from the ant and weaken them), or infested ants would have to be enslaved by neighboring colonies. The authors did not find direct evidence to support either idea.

2) The parasite may cause infested ants to be more conspicuous to animals which are already consuming ants on a regular basis. Birds seem to avoid healthy giant gliding ants because of their spiny armor and strong pheromones, but lizards and anteaters may not be so picky. In this case, these other vertebrates may pick out the infested ants as these individuals would be easier to spot, but this creates a problem with droppings. The feces of lizards and anteaters would be more likely to drop to the forest floor where they would be picked over by other species of ants, and so deprive the parasite of getting back into a giant gliding ant nest.

Further laboratory and field observations will be required to test the hypothesis presented in the American Naturalist paper, but, at present, predation by birds appears to best explain the modifications to the ants, the infestation of larvae by the parasite, and the dispersal of the nematode to new colonies. The details of how this two-host system evolved and the physiological mechanisms which trigger the changes in the ants are as yet unknown, but hopefully further research will help to explain how a tiny worm can so drastically change the appearance and behavior of an organism.

Yanoviak, S., Kaspari, M., Dudley, R., & Poinar, G. (2008). Parasite‐Induced Fruit Mimicry in a Tropical Canopy Ant The American Naturalist, 171 (4), 536-544 DOI: 10.1086/528968

HUGHES, D., KRONAUER, D., & BOOMSMA, J. (2008). Extended Phenotype: Nematodes Turn Ants into Bird-Dispersed Fruits Current Biology, 18 (7) DOI: 10.1016/j.cub.2008.02.001

I have been writing here at ScienceBlogs.com for about two years and nine months now. Some of you have been reading my posts since I started here (thank you for sticking with me!), but readers come and go over time, and so I am jumping on board with the “Who are you?” meme recently restarted by DrugMonkey, Pal, Janet, Bora, and Jason.

Everyone is asking different questions of their readers – some more detailed ones than others – but I think I’ll keep it relatively simple: who are you (feel free to comment anonymously or under a pseud, and be as specific [or not] as you prefer), what do you like about this blog, and is there anything you would like to see here in the future? I admit, straight-up asking for positive feedback might seem a little self-serving, but I am hoping that by doing so I can foster the community of regular readers here and further improve my writing. (Even if you don’t want to comment here, please send me an e-mail.) As Pal noted in his own post on this, “As bloggers we can get an idea of how many people are reading us, but not that much else”, so getting some good feedback from readers can be both helpful and encouraging.

Not all zombies are created equal. The most popular zombie archetype is a shambling, brain-eating member of the recently deceased, but, in recent films from 28 Days Later to Zombieland, the definition of what a zombie is or isn’t has become more complicated. Does a zombie have to be a cannibal corpse, or can a zombie be someone infected with a virus which turns them into a blood-crazed, fast-running monster?

For my own part, I have always preferred the classic George Romero zombies from the original Dawn of the Dead and Day of the Dead films (as well as my most favorite of zombie films, Shaun of the Dead). The shuffling, groaning masses not only deliver social commentary in spades – i.e. our transformation into mindless consumers inextricably drawn to shopping malls – but the prospect of slowly being closed in by a seemingly unstoppable horde is far more frightening than any sprinting zombie. Nevertheless, there is one thing that bugs me about zombie movies in the classic vein – where are all the flesh-eating insects?

Zombies are often the star antagonists of horror films, but there is another array of flesh eaters which are usually ignored. For bacteria, flies, and other organisms which typically set to work on cadavers soon after death, a zombocalypse would be a smorgasbord of epic proportions. So, in order to figure out what might happen to the living dead in the days after their horrifying resurrection, I turned to forensic science and taphonomy to see what might worry the zombies themselves.

As outlined by forensic scientist Arpad Vass in a brief overview called “Beyond the grave – understanding human decomposition“, it doesn’t take long for the human body to break down. Just four minutes after death, oxygen deprived cells begin to digest themselves and spill their contents. This is not visible at first, but after a few days fluid-filled blisters appear on the skin and large parts of the skin begin to slough off. By this time, with the onset of putrefaction and bloating of the corpse, the work of bacteria, fungi, and other microorganisms begins to become apparent.

The characteristic bad odors and greenish skin of zombies are signs of the busy activity of the microorganisms. Slowly but surely, the bacteria and fungi (such as species of Staphylococcus, Candida, Malasseria, Bacillus and Streptococcus) transform tissue into gases and liquids – unless zombies take steps to preserve themselves, their decomposition is inevitable. (Interestingly, in warm, moist environments, zombies would make their own soap through a process called saponification in which fat in the body is transformed under high pH conditions. Cadaver lather, anyone?) Eventually the internal organs will all be broken down leaving the skin as little more than a thin bag around the bones, and soon after that body will become nothing more than a skeleton. Rate of decomposition varies due to temperature and moisture, but, to provide some measure of the speed at which these transformations take place, Vass figured that – at about 50 degrees Fahrenheit – it takes about 128 days for a corpse to be entirely skeletonized.

But what about insects? Naturalists since the time of Carolus Linnaeus have recognized that these little “death workers”, too, play important roles in decomposition, and the more insects tuck into a corpse, the faster it falls apart. Of these, an array of Diptera flies are among the most frequent arthropod visitors to corpses, and their time of arrival has been used to figure out how long a body has been dead. As stated by scientists Carlo Campobasso, Giancarlo Di Vella, and Francesco Introna in their review of flies and decomposition, among the first flies to arrive are species belonging to the Calliphoridae (blow flies), the Sarcophagidae (flesh flies), and the Muscidae (house flies), later followed by members of the Sphaeroceridae (lesser dung flies), Piophilidae (cheese flies), Fanniidae, and Phoridae. They typically lay their eggs around whatever open orifices they can find – especially on the head – with 6 to 10 days between the time they lay their eggs and the time the new adult flies emerge, and the warmer it is, the more species you will find. Beetles do their part, too. Members of the Silphidae (carrion beetles) are early visitors to corpses, while species among the Nitidulidae (sap beetles), Cleridae (checkered beetles), Scarabaeidae (scarabs), and, those most famous of all cadaver beetles, Dermestidae arrive later. (Staphylinidae (rove beetles) and Histeridae (clown beetles) can be found on corpses, too, but these often eat other insects rather than the body itself.)

While zombies would not be quite as easy to prey upon as a stone-still cadaver, I can imagine that at least some of these insects would still try to feed and breed on them, further speeding along decomposition. In fact, unburied bodies often undergo a drastic decline in mass during just a few days, thanks in large part to scavengers, and so it is not unreasonable to speculate that – as much as the living would have reason to fear zombies – bacteria, flies, and even vertebrate scavengers would give zombies something to worry about. As for mammalian and avian scavengers, these animals might be more skittish of zombies than they would be of cadavers, but I have to wonder if some of them might try to take a bite here or there, especially during the time between death and ‘zombification’ as the putrefaction which soon comes about is more of a deterrent than attractant for everything other than insect scavengers.

Despite horror film scenarios of long-lasting zombie horror, the bodies of the undead would not last very long. Between the natural breakdown of the body following death, the activities of scavengers, the colonization of microorganisms, and the habits of arthropods, any given zombie might only be able to last few a few days, weeks, or months before decomposing so much that they are unable to move. Granted, the beginning of a zombocalypse – when the public remains unaware – would probably be marked by many hapless victims being turned into zombies themselves, but given enough time the epidemic would simply rot itself away. As with H.G. Wells’ classic story about alien invasion – War of the Worlds – our greatest assets in confronting the zombie menace would not be guns or chainsaws, but the small organisms which rely on decomposing flesh to make their living.

Campobasso, C. (2001). Factors affecting decomposition and Diptera colonization Forensic Science International, 120 (1-2), 18-27 DOI: 10.1016/S0379-0738(01)00411-X

Carter, D., Yellowlees, D., & Tibbett, M. (2006). Cadaver decomposition in terrestrial ecosystems Naturwissenschaften, 94 (1), 12-24 DOI: 10.1007/s00114-006-0159-1

DeVault, T., Brisbin, Jr., I., & Rhodes, Jr., O. (2004). Factors influencing the acquisition of rodent carrion by vertebrate scavengers and decomposers Canadian Journal of Zoology, 82 (3), 502-509 DOI: 10.1139/Z04-022

Anyway, I hope you like the stories, and, if you do, be sure to check out my forthcoming book on paleontology and evolution, Written in Stone (pardon the shameless plug).

Out on the grassy plains of Kenya’s Masai Mara National Reserve, a group of six female topi antelope (Damaliscus lunatus) walk across the savanna. It is the time of the annual rut – a one and a half month period in which most males control small patches of land and try to attract adult females which, for one day, are in estrus. The small group walks by one of the lone males, but just as they reach the edge of his territory he snorts an alarm. It means that somewhere, out ahead of them, a predator waits to pounce on any topi foolish enough to blunder towards it, and so the females stay close. What the females don’t know, however, is that the alarm call was a lie.

In many natural history documentaries, mating among mammals is presented as a relatively straightforward affair. Males compete with each other for access to females – be it through the control of a territory, dominance in a social group, or some other route – with the biggest and most impressive males coming out on top. Not surprisingly, things are not as orderly in nature as they are on television, and this goes for the topi as for any other animal. Males lucky enough to hold down a mating territory are not content to simply let females choose who they are going to mate with. As Jakob Bro-Jorgensen and Wiline Pangle demonstrate in a new American Naturalist paper, deceitful males can enhance their chances of siring part of the next generation.

Detecting deception among non-human animals has been notoriously difficult. How can you tell if an animal is telling a lie? In the case of topi antelope, specifically, it would appear that males are emitting false alarm snorts in order to retain females in their territories, but what if these “false alarms” are really just mistakes which just happen to have a beneficial effect for those males?

In order to test these competing hypotheses, Bro-Jorgensen and Pangle observed 73 female topi (53 in estrus and 20 not in estrus) over several rut seasons between 2005 and 2009 for a total of 274 hours. The scientists recorded the salient details of how the females moved among male-controlled territories as well as the occurrence of alarm calls by males which were determined to be “true” or “false” on the basis of whether predators were actually present (which was possible to determine given the open habitat in which the topi live). Once they observed the occurrence of both true and false alarms in the field, they recorded these calls (along with a grunt, which they used as a control) and played them back a total of 20 times to 60 grazing female topi to see whether females could detect the difference between them. Furthermore, the researchers approached male topi on foot in order to see if they emitted alarm snorts. If so, this might mean that the snorts are more about communicating to a predator – “I see you. You have lost the element of surprise” – than to other topi.

When Bro-Jorgensen and Pangle looked at the acoustic breakdown of the alarm calls they could not find any difference between true and false alarms – the calls could only be distinguished by the context in which the males emitted them. Likewise, the playback experiments also failed to find a difference between true and false alarm snorts. Females reacted the same way to both, often standing vigilant before walking away since males typically snort from a place between females and the danger, meaning the females would – under normal circumstances – be headed back into the male’s territory. These observations were consistent with the natural behavior of these animals. Consistent with the female-retention hypothesis, the scientists observed that males emitted false snorts most often when a female in estrus was nearby. When females began to move away, the male would look in the direction she was going, with his ears alert, and snort.

Sex, of course, was the reason why the males were raising false alarms, and this strategy appeared to work well for them. On average, males who emitted false alarms mated two-to-three times with estrus females during the time those females remained in their territory, and in a few cases – 10% – males only succeeded in mating after snorting. Likewise, since a female topi is only in estrus for one day, the longer a male can keep a female in his territory, the better – every minute she is in one male’s territory is a minute that she’s not mating with another male. Even if a male does not mate very many times with a female that is in his territory, delaying her departure can still confer reproductive benefits.

Interestingly, the results of the “threat” experiment (in which researchers approached male topi standing alone) showed that true alarm snorts might have more to do with letting predators know that they have been spotted than communicating to other topi. Even though no other topi were nearby, the males still snorted when approached. If the primary purpose of the snorts was to warn other topi, then the male would have just drawn attention to himself for no good reason, and so it seems more plausible that alarm snorts are actually “deterrent snorts” meant to discourage predators which rely on stalking. Hence, since true alarms were elicited by lone males and false alarms were closely tied to the presence of females in estrus, it was unlikely that the male topi were making mistakes (i.e. thinking that they were warning females about a predator in the grass). They were using the alarm calls as a manipulative tool to gain more mating opportunities, and males which did so enjoyed enhanced mating success. As the authors state, males gain significant reproductive advantages from false alarm calls, but females cannot afford to ignore alarm calls – as there is no difference between false and true alarms, ignoring any alarm call may mean that they are walking right into the path of a predator.

Just what the male topis are thinking when they emit the false alarms is beyond our ability to discern, but the results of the observations are strong – male topis use alarm calls to manipulate females. Since there is no way to tell the difference between true and false alarms, and the cost to females for ignoring the alarms is potentially high, it is easy for the male topi to use the snorts as dishonest signals. In fact, alarm calls in general are probably susceptible to becoming used as manipulative signals for much the same reasons – perhaps deceit is more widespread among animals than has previously been appreciated.

[Photo of topi on an anthill (top) by Jakob Bro‐Jørgensen.]

Bro‐Jørgensen, J., & Pangle, W. (2010). Male Topi Antelopes Alarm Snort Deceptively to Retain Females for Mating The American Naturalist, 176 (1) DOI: 10.1086/653078