Lungless and happy about it

It is rather amazing that a terrestrial animal as big as this Ringtail salamander (Bolitoglossa robusta) from Costa Rica can spend its entire life without taking a single breath and rely entirely on gas exchange through its skin.

It is rather amazing that a terrestrial animal as big as this Ringtail salamander (Bolitoglossa robusta) from Costa Rica can spend its entire life without taking a single breath and instead relies entirely on gas exchange through its skin.

Of all the organs in my body, the one that I would be most reluctant to part with (perhaps with the exception of my eyes) are the lungs. It seems that we need them more than anything else. True, we need all the other bits, but lungs seem particularly useful. Without them the brain stops working in a matter of minutes, the vascular system loses its main reason to exist, and the biochemical processes in pretty much every cell come to a grinding halt. Like the hideous inflatable Santa in front of my neighbor’s house, the complex edifice of the human body would immediately collapse if the air supply were to be shut off. It seems that if you are a land-dwelling vertebrate you better have lungs, or you are not going to last very long. And yet, defying common sense, there is a group of terrestrial animals that got rid of their lungs altogether, and in doing so have become widely successful, outcompeting their lunged relatives in both the number of species and their collective biomass. They are the lungless salamanders of the family Plethodontidae.

The Redback salamander (Plethodon cinereus), a small, unassuming animal common in the eastern United States, is a marvel of evolution, with physiology that makes our own appear laughably inefficient.

The Redback salamander (Plethodon cinereus), a small, unassuming animal, common in the eastern United States, is a marvel of evolution, with physiology that makes our own appears laughably inefficient.

I thought of them last month, when freakishly warm weather in Boston forced me to clean up the accumulation of dog poop from the front lawn, which in any other year the snow would have mercifully covered up until spring. The unseasonal warmth also woke up a multitude of creatures that should have been fast asleep, including a couple of Redback salamanders (Plethodon cinereus), which I found under a wooden plank in the garden. Despite the ice crystals glistening in the half-frozen soil, they were surprisingly agile. “Agile” is of course a relative term, especially when talking about an animal whose metabolism is entirely dependent on oxygen passively permeating the skin. Nearly 100% of the oxygen intake and excretion of the carbon dioxide takes place on the surface of the skin of these salamanders, with the throat (buccopahryngeal cavity) accounting for an additional, small proportion of the gas exchange (perhaps for this reason lungless salamanders still retain well-developed nostrils.) Clearly, animals that are incapable of taking active breaths, and thus accelerating or decelerating gas exchange at will, cannot be marathon runners, or runners of any kind. And somehow, by employing various degrees of toxicity and the ability to subsist on low-nutrition diet of springtails and mites, lungless salamanders have managed to become the dominant family of amphibians of the Western hemisphere. Nearly 400 species have already been described and new ones are being discovered every year in both the cool, temperate forests of North America, and in the rainforest canopy of the Neotropics. In some places their numbers are staggering. A recent analysis of the population of the Southern Redneck salamander (P. serratus) of the Ozark Highlands in Missouri put their numbers at 1.88 billion (!) individuals, with the biomass equivalent to that of most whitetail deer in that region – that’s 1,400,000 kg (3,086,471 lb) of amphibian flesh.

Among many adaptations to the arboreal lifestyle are the lungless salamanders' pad-like feet. Despite of the overall similarity, this foot shape has evolved independently in different species of the genus Bolitoglossa.

Among many adaptations to the arboreal lifestyle are the lungless salamanders’ pad-like feet. Despite the overall similarity, this foot shape has evolved independently in different species of the genus Bolitoglossa.

Although all members of the family Plethodontidae are entirely lungless, their ancestors were not. What prompted the loss is still a mystery, and two competing theories, neither particularly compelling, try to explain it. According to the older of the two, lungless salamanders originated from a lineage that inhabited cold, fast flowing and well-oxygenated streams of the Cretaceous Appalachia (lungless salamanders still dominate the amphibian fauna of that region). The loss of lungs made them less buoyant and thus more capable of maintaining their position at the bottom of the stream while hunting for prey. But some researchers pointed out the lack of geological evidence for cold, upland environments in the Mesozoic Appalachia. Instead, they argue, lungless salamanders come from oxygen-poor tropical waters, where highly humid terrestrial environment proved to be a better alternative. Once on land, dense vegetation exerted adaptive pressure to evolve small, narrow heads, which in turn prevented the animals from filling their lungs effectively, and leading to the reliance on respiration through the skin. If this sounds sketchy to you, you are not alone. Most herpetologists today lean towards the first explanation, with the added argument that the loss of lungs happened early on in the larval development of the aquatic ancestors of the plethodontids. But the truth is, nobody really knows.

The ability to use a prehensile tail, a rarity in the animal kingdom, is one of the most amazing characteristics of the large, arboreal Ringtail salamander (Bolitoglossa robusta) from Costa Rica.

The ability to use a prehensile tail, a rarity in the animal kingdom, is one of the most amazing characteristics of the large, arboreal Ringtail salamander (Bolitoglossa robusta) from Costa Rica.

What is not in question is the fact that lungless salamanders rule the forests of North, Central, and parts of South America. Larger species tend to be ground-dwelling, whereas smaller ones live high in the canopy. The arboreal salamanders have evolved a number of cool adaptations to such a lifestyle. The Central American genus Bolitoglossa is famous for its lack of distinct fingers. Instead, these salamanders have pad-like feet that help them move on smooth, wet surfaces of rainforest trees. And although feet in all species of Bolitoglossa look similar, they are the result of two very different evolutionary processes. In smaller species, such as the colorful (and toxic) B. mexicana, the digit-less foot is the result of paedomorphosis – a developmental mechanism during which juvenile characters are retained in adult, reproductive animals. In other words, they have baby feet, and they rely on simple surface adhesion to cling to leaves and branches.

Larger species, such as the Costa Rican B. robusta, also have pad-like feet, but underneath the webbing sit fully developed digits and a complex musculature. The central part of the foot can be lifted, thus creating suction, a mechanism similar to that used by marine cephalopods. But wait, there is more. In addition to having suction cups for feet, this salamander has a prehensile, chameleon-like tail, which it uses to save itself from falling off trees. When I first saw one of these animals a few years ago pull this trick high in the branches in Tapanti National Park, I thought I was hallucinating. And the similarity to chameleons does not end there – just like those reptiles, lungless salamanders sport a long, projectile tongue (in one species the tongue is 80% as long as the body, and salamanders are pretty long animals!) They can eject it with an amazing speed, a mere 117 ms, to catch fast moving prey. And this ballistic tongue projection is an order of magnitude more powerful than that of any muscle in any other living vertebrate species.

All this to say that the next time you find a small, curled up salamander under a rock, look at it with a little more respect. This ancient animal can pull off tricks that would put many Marvel Comics characters to shame. Without taking a breath. Ever.

Ringtail salamander (Bolitoglossa robusta) on a tree branch in Tapanti National Park, Costa Rica.

Ringtail salamander (Bolitoglossa robusta) on a tree branch in Tapanti National Park, Costa Rica.

A really cool sequence of a lungless salamander (Hydromantes) using its projectile tongue (BBC).

Ghost hunting

A silhouette of the first ghost mantis recorded from Gorongosa National Park in Mozambique.

A silhouette of the first ghost mantis (Phyllocrania paradoxa) recorded from Gorongosa National Park in Mozambique.

I have been working in Africa for quite a while and during this time I have seen my share of iconic animals that epitomize the awesome continent’s fauna. There are still, of course, many that I yet need to meet in person – aardvark, “hairy” Trichobatrachus frog, Acridoxena katydid, to name a few – but luck or stubbornness allowed me to witness others. Few things can match the elation of meeting the gaze of a foraging chimpanzee, discovering a toy-like primate poto in the forest canopy over my head, or running into a fight between a hyena and a leopard over a freshly killed kudu. But my first encounter with one of the less known species, the ghost mantis (Phyllocrania paradoxa), was at least as memorable.

A female ghost mantis (Phyllocrania paradoxa) – these insects are such superb mimimcs of dry vegetation that it is often difficult to tell which part belongs to the plant and which to the insect.

A female ghost mantis (Phyllocrania paradoxa) – these insects are such superb mimimcs of dry vegetation that it is often difficult to tell which part belongs to the plant and which to the insect.

It happened during my first trip to Zimbabwe, at the time when the tumor in Robert Mugabe’s brain was still semi-dormant and the country, “Africa’s bread basket”, was experiencing its first and only period of relative political freedom and economic prosperity. I was staying with a group of friends in the suburbs of the recently re-christened capital Harare, vaguely intrigued with, but blissfully ignorant of why so many houses were standing empty, their gauged windows bordered with the mascara of freshly extinguished flames. Africa was new to me, and I inhaled its intoxicating atmosphere and devoured the sights of alien landscapes and even more alien fauna. But I came prepared – for years before my first visit I had been voraciously reading all that I could find about insects and other members of Africa’s smaller majority. The ghost mantis was one of my most desired quarries and I started looking for it the moment I landed. Alas, a month on and with no trace of the animal, it was beginning to feel as if I were really hunting a ghost. I had spent countless hours sifting through the leaf litter, scanning bushes and trees, sweeping my net through all kinds of vegetation – nothing.

One day I stood on the platform of a railway station, waiting for a train to take me to Bulawayo. It was late October, the peak of the dry season, and shriveled leaves were falling from trees onto my head in a rare, merciful breeze. One, fairly large and twisted brown leaf landed on my shoulder. I tried to brush it off but it just sat there, trembling in the wind. I flicked it again. It landed lower on my sleeve. And then the leaf started to climb up my arm. I looked, still not believing. Could it be? No, this is just a piece of withered plant. But it was, finally, a ghost mantis.

Ghost mantids are extremely polymorphic in both their coloration and the shape of the strange processes on their heads.

No two individuals of ghost mantids are alike, which prevents their principal predators, birds and primates, from learning how to tell them apart from real leaves.

That was 25 years ago and it took me this long to run across another one. In fact, I had more run-ins with the notoriously elusive leopards than with this incredible insect. But this year, in April, I was finally able to confirm ghost mantids’ presence in Mozambique’s Gorongosa National Park (something that I have always suspected), when my friend, entomologist Marek Bakowski, found the first individual during our annual biodiversity survey. Since then I have encountered a few more ghost mantids in the park.

A Gorongosa ghost mantis with a freshly laid ootheca.

A Gorongosa ghost mantis with a freshly laid ootheca.

A molting ghost mantis.

A molting ghost mantis.

Thanks to their otherworldly appearance ghost mantids have long been the favorite of amateur insect collectors and, since they can be easily bred in captivity, they have recently become very popular in the pet trade. Now all you need to do to see a live ghost mantis is to pay a few bucks online and one will be delivered to your door. But for an animal so widely kept, shockingly little is known about its biology and behavior in its natural habitat. Nobody is even sure how many species of ghost mantids there are. Three species of the genus Phyllocrania have been described, only to be synonymized a few years ago. All three were recognized as separate species based on the differences in the shape of the leaf-like process on the head, which can vary wildly within the same population. Ghost mantids, like many other insects that rely on leaf-like camouflage, display an ungodly degree of polymorphism, and no two specimens are alike. But the species’ distribution, throughout sub-Saharan Africa and Madagascar, hints at the possibility of distinct, genetically isolated lineages.

Like most praying mantids, the ghost mantis is an ambush predator, a truly superb one. But unlike many others, it is not inclined to attack members of its own species, and I know of no case of the female devouring a male during copulation, as it is often the case in some other lineages of these insects. In Gorongosa ghost mantids are found mostly in the understory of miombo and mopane woodland, and the only time I witnessed one feeding, it was chomping on a grasshopper. Females produce strange, caterpillar-like oothecae, and newly hatched nymphs look and behave like black ants; after the first molt they turn into perfect replicas of dried-up chaff. How males and females find each other, however, is a mystery to me. It is likely that females, like in other highly cryptic mantids, produce sex pheromones to attract their mates.

Next on the list of African biodiversity icons to confirm in Gorongosa, the Devil mantis. I know you are there and I will find you.

No two individuals of ghost mantids are alike, which prevents their principal predators, birds and primates, from learning how to tell them apart from real leaves.

Ghost mantids are extremely polymorphic in both their coloration and the shape of the strange processes on their heads.

 

 

Mozambique Diary: Snug as a bug

A cute African bat bug (Cacodmus villosus), snuggly nestled on the tail membrane of the Banana bat (Neoromicia nana) (Gorongosa National Park, Mozambique)

A cute African bat bug (Cacodmus villosus), snuggly nestled on the tail membrane of the Banana bat (Neoromicia nana) (Gorongosa National Park, Mozambique)

“There is a strange ecto on this vesper”, said Jen, a sentence that only recently would have been difficult for me to comprehend. But now, after a few years of rubbing shoulders with mammalogists in Gorongosa I osmotically absorbed enough jargon to understand that she had noticed an interesting parasitic insect on a bat of the family Vespertilionidae. My ears perked up. Jen skillfully disentangled the screeching animal from the mist net and gently stretched the leg of the bat to reveal a small, fuzzy insect snuggly nestled between its fur and the naked tail membrane. Although the circumstances were unusual, considering that we were in the middle of a montane rainforest in Mozambique, and the insect was sitting on a flying mammal, a neural circuit that develops very early on during every entomologist’s training immediately fired a signal – it’s a bed bug!

To be precise the insect sitting on the bat’s body was a bat bug (Cacodmus villosus), a species common in sub-Saharan Africa and associated mostly with bats of the genus Neoromicia. These insects are indeed close relatives of the infamous human bed bugs (Cimex lectularius and C. hemipterus) and share a nearly identical morphology. Until recently entomologists thought that bat bugs spend all of their time in caves and other bat roosting sites, and only briefly visit their hosts’ bodies to feed when the bats are resting. But recent observations, supported by our find, indicate that members of at least this species of bat bugs live permanently on their host. And this is surprisingly interesting.

Bats of the family Vespertilionidae, such as this Neoromicia nana, are frequent hosts of bat bugs, possibly because of these mammals' low hematocrit, which makes drinking of their blood easier for parasites.

Bats of the family Vespertilionidae, such as these Neoromicia nana, are frequent hosts of bat bugs, possibly because of these mammals’ low hematocrit, which makes drinking of their blood easier for parasites.

As it turns out, repeated feeding on the same host and in the same spot on the body can be deadly. Not only because the host is more likely to find and kill the annoying parasite, but also because the immune response from the host gets cumulatively stronger over time and greatly increases the mortality of the blood suckers. A few groups of arthropods have successfully managed to adapt (ticks, ceratopogonid and nycteribiid flies, lice, to name a few) but the initial stage of the transformation from a visiting to resident parasite must surely be difficult. This change also requires a great deal of morphological adaptation to become harder to locate and remove by the host. And the bat bug that we saw, despite being very similar in its overall form to the human bed bug, was already displaying some indication of this transition. Its body was harder and smaller than that of the bed bug, which only visits its human hosts for a few minutes every few days. The animal was also covered with long hair, which probably makes it more difficult to be grasped by a bat grooming itself; similar long setae covering the body are the characteristic of another group of ectoparasites, the bat flies (Nycteribiidae).

All members of the family Cimicidae have a similar morphology, and all are obligate hemophages of mammals and birds.

All members of the family Cimicidae have a similar morphology, and all are obligate hemophages of mammals and birds.

Bed, bat, and bird bugs, members of the family Cimicidae, are obligate hematophages – they must drink animal blood to live. It does not matter much to them whose blood they are drinking. Bat bugs will happily drink human blood, and bed bugs love to feed on chickens. Blood, regardless of its origin, appears to be uniformly nutritious. The reason these insects specialize on particular hosts has to do with the morphology of the red blood cells (erythrocytes) as their sizes vary among animals. For example, chicken erythrocytes are 11.2 µm in diameter, whereas human ones are only 6-7 µm. Since bat and bed bugs drink blood through a needle-like stylet, its diameter has to match that of the erythrocytes of their host and the viscosity of the blood. If you ever had a really good, thick strawberry frap then you know what I am talking about – the pieces of fruit clog the straw and you end up scooping them out of the cup with your fingers (everybody does it, right?) The point is that human blood is easier to drink than that of birds, which might have been the reason why these insects switched hosts sometime during the early stages of human social evolution, from birds or bats that inhabited the same dwellings (swallows are highly probable original hosts). Blood morphology also explains why some bats have and others do not have bat bugs. Bats of the family Vespertilionidae, like the one we caught in Gorongosa, have really low hematocrit (the percentage of red cells in blood) compared to other bats, which makes their blood “thinner” and easier to drink. Not surprisingly they are the most common hosts of bat bugs.

Bed bug (Cimex lectularius) feeding on my blood.

Bed bug (Cimex lectularius) feeding on this human’s blood.

The recent upsurge in bed bug infestations across the world, caused in all likelihood by the sudden availability of cheap airfare and thus a dramatic increase in mixing up of the human population (damn you, JetBlue!), has put these insects into the spotlight. But bed bugs have always been the darlings of behavioral biologists, primarily because of their unusual reproductive behavior. Bat and bed bugs are practitioners of traumatic insemination – males in these insects don’t bother finding the proper opening in the female’s body, but simply jab their sharp copulatory organ into the side of her abdomen and ejaculate directly into the body cavity. This cannot possibly be pleasant. In fact, females who were inseminated in this way show 20-30% decrease in their lifespan due to injuries, and some die immediately after the mating. For this reason female bed bugs had to evolve separate paragenital structures that channel sperm injected into their body cavity into the true reproductive organs. Unfortunately, male bed bugs are particularly horny creatures that will attack anything that moves, including other males, and mate with it. In most bed bug species such intrasexual rape results in the death of the victim male due to ruptured intestines. So severe is the risk of dying from misplaced mating attempts that in the African bat bug Afrocimex constrictus males have developed paragenital structures similar to those of females, just to protect themselves from other lusty males.

Why such bizarre mating strategy has evolved in bed bugs (and a few other invertebrate groups) is still a mystery. Most explanations center around sperm competition – by injecting sperm directly into the body of the female the males bypass mating plugs that females of many animals develop to stop future matings. It may also give males a chance to send sperm closer to the ovaries, or simply avoid having to perform some ridiculous dance or other display in order to be accepted by the female as a mating partner. There is also a theory that by injecting sperm directly into the gut the male bed bug feeds the female (his sperm is indeed partially digested), a form of a nuptial gift. Thanks, but no thanks!

African bat bug (Cacodmus villosus) on the wing membrane of the Banana bat (Neoromicia nana) (Gorongosa National Park, Mozambique)

African bat bug (Cacodmus villosus) on the wing membrane of the Banana bat (Neoromicia nana) (Gorongosa National Park, Mozambique)

Mozambique Diary: Photoshop or not?

Rock scorpion (Hadogenes granulatus) from Bunga Inselberg in Gorongosa, one of the largest scorpions in the world.

Rock scorpion (Hadogenes granulatus) from Bunga Inselberg in Gorongosa, one of the largest scorpions in the world.

One of the more entertaining consequences of posting images of obscure, rarely seen animals on this blog or on my Facebook page is that I am sometimes accused of faking them, especially if a Google search by those who doubted the veracity of my photos did not produce similar pictures taken by other photographers. This happens particularly often with animals that are the largest of their kind, be it a giant land crab or, more recently, a parasitic bat fly. I wonder if the photos in this post will be met with similar incredulity.

Bunga Inselbergs in Gorongosa National Park, Mozambique

Bunga Inselbergs in Gorongosa National Park, Mozambique

Last month I lead (lured) a group of researchers to a remote corner of Gorongosa National Park to continue the documentation of the biological richness of this remarkable place. Our camp was at the foothills of the Bunga inselberg, one of several small, isolated mountains in the western part of the park. These inselbergs have never been biologically explored and although we did not expect to find any endemic species there was always a chance of encountering rare or new to science organisms. These inselbergs are, in an essence, giant piles of volcanic rock, covered with a very thin layer of topsoil and a dense carpet of woody vegetation. Such a habitat is heaven for a lot of animals but, to my great relief, not lions and elephants. This meant that we could roam freely around the inselbergs in a relative safety, not constrained by the need to be always accompanied by armed park rangers. I say “relative” because Africa is rich in things that can get you, and Bunga inselbergs were no different – on my first visit there my friends and I were attacked by a cloud of wild honey bees, and on the following day I pulled nearly 150 stingers from my arms and neck. (It was a close call – I remember thinking “At least this is the end fit for an entomologist,” before losing consciousness.) Thankfully there were no similar incidents during this survey, although I did make sure that every person carried an Epipen kit to treat potential anaphylactic shock.

The median ocelli of the rock scorpion (Hadogenes granulatus) are protected from scratching against rocks by elevated ridges (green arrow). These are absent in species that live in equally constrained but softer environments, such as this Opistacanthus (below) found under tree bark.

The median ocelli of the rock scorpion (Hadogenes granulatus) are protected from scratching against rocks by elevated ridges (green arrow). These are absent in species that live in equally constrained but softer environments, such as this Opistacanthus (below) found under tree bark.

Lifting heavy volcanic rocks to look for animals during the survey was hard work, but it was also immensely rewarding. Each flat piece of basalt could have been hiding a cool gecko, a snake, a family of crickets, some awesome beetles, or a scorpion, and it was the last one that gave me the biggest surprise. Rock scorpions of the genus Hadogenes are considered the largest, or at least the longest, scorpions in the world. Some species can reach the length of 22 cm and several individuals from Bunga were at least this big. Granted, a large portion of the body is the long and thin telson (“tail”) of the animal, but it is still a spectacular beast, which will make you pause when you see it scurrying around your fingers. All species of Hadogenes are obligate lithophiles; in other words, they love rocks. Their bodies are perfectly adapted to squeezing into narrow crevices, and their feet carry stiff setae and strongly curved claws that allow them to cling to even the smoothest rocks (and hang from rocks upside down, something that few other scorpions can do). Their median ocelli – the main pair of eyes – are protected by elevated ridges that prevent them from scratching against the rocks, and the entire body is flatter than in any other scorpion of similar size.

Like many scorpions, members of the genus Hadogenes display a beautiful, blue fluorescence if exposed to ultraviolet light. A recent study suggests that this helps these nocturnal animals detect and avoid light.

Like many scorpions, members of the genus Hadogenes display a beautiful, blue fluorescence if exposed to ultraviolet light. A recent study suggests that this helps these nocturnal animals detect and avoid light.

But, as it is often the case, a large size and a scary appearance do not necessarily translate into true ability to inflict harm. The giveaway is the telson, which in rock scorpions is long and thin, betraying the presence of weak muscles and a small venom gland, and thus the lack of reliance on venom for capturing prey and defense. They can and do sting, of course, but the strength of their venom is no greater than that of a bee (and, thankfully, scorpions do not move in large swarms and are far more friendly than those pissy little bits of flying pain). A few species of Hadogenes have the ability to spray venom towards the attacker, which can cause painful irritation if the droplets get into your eyes, but otherwise they are harmless. In fact, an article (pdf) describing the medical importance of rock scorpions puts more emphasis on their ability to pinch your fingers then to envenomate.

Scorpions of the genus Hadogenes occur in rocky habitats across southern and East Africa, often on isolated mountains, leading to frequent allopatric speciation and a high number of endemic species. When I first found rock scorpions on Bunga I was hoping for a new, undescribed species but, alas, this turned out not to be the case as they were all members of H. granulatus, a species known from other places in Mozambique.

I photographed one of the individuals sitting on a vertical rock next to my hand. I knew that the animal was pretty harmless but I still was not looking forward to comparing its venom to that of a bee, and decided not to shoot it sitting directly on my hand. And, of course, it made it much easier to manipulate the image in Photoshop to make the scorpion appear bigger. (Kidding!)

Rock scorpions’s body is strongly flattened, perfectly adapted to squeezing into the narrowest crevices.

Rock scorpions’s body is strongly flattened, perfectly adapted to squeezing into the narrowest of crevices.


Flavio Artur, Ricardo Guta, and I, 24 hours after being attacked by a swarm of wild African honey bees. On that morning I pulled out nearly 150 stingers from my skin.

Flavio Artur, Ricardo Guta, and I, 24 hours after being attacked by a swarm of wild African honey bees. On that morning I pulled out nearly 150 stingers from my skin.

 

Mozambique Diary: Red-headed flies

Red-headed flies (Bromophila caffra) are striking and common animals in East and southern Africa, but little is known about their biology.

Red-headed flies (Bromophila caffra) are striking and common animals in East and southern Africa, but little is known about their biology.

Two months, that’s how long I have been neglecting this blog. Some people had even sent me messages to check if I were still alive. But I am alive and the reasons for my silence were good – until last week I was in Mozambique, working at the Wilson Lab and busily preparing for the next biodiversity survey of Gorongosa National Park. While there I had precious little time to write or take photos, but I did manage to take some shots of a few interesting critters. It is the rainy season in Gorongosa now and insect life is exploding. I had set up an ultraviolet light in front of my office to collect all members of my target groups (orthopteroid and dictyopteroid insects) and to cherry-pick the more interesting species from orders that we don’t yet collect systematically. On some nights the sheet was sagging under the weight of hundreds of species of insects and for a while mysterious redheads kept coming to the light.

Red-headed flies, which in Mozambique emerge at the end of the rainy season, like to hang in clusters on leaves.

Red-headed flies, which in Mozambique emerge at the end of the rainy season, like to hang in clusters on leaves.

I recognized them from my earlier trips to Gorongosa as Red-headed flies (Bromophila caffra) – large, slow moving insects, reluctant to take to the air, and much happier to hang in clusters from low tree branches. They are truly striking animals, showy and clearly unconcerned about attracting anybody’s attention, including that of potential predators. There were many birds and grabby vervet monkeys in the camp, who not so much as looked in the direction of the flies who slowly spun in clusters on leaves.

Adult Red-headed flies feed on dung and other decaying organic matter.

Adult Red-headed flies feed on dung and other decaying organic matter.

But for an insect as conspicuous and common as the Red-headed fly, shockingly little is known about its biology. In fact, the last scientific paper that mentions it by name (according to an extensive MetaLib cross-database search) is from 1915, and it does so only to compare the fly’s strikingly red head to another species. As already pointed out in an excellent post about this species by Ted C. MacRae, there exists only anecdotal evidence that the larvae of this species might be feeding on the roots of Terminalia trees, potentially sequestering toxic cyclic triterpenes, which would explain the adult flies’ aposematic coloration. But, as is the case with so many African invertebrates, nobody really knows.

There is also another possibility. One morning while in Gorongosa I woke up to find my arms covered with big, painful blisters. The night before I had spent a couple of hours searching for insects in tall grass and remembered seeing many contrastingly colored, red and black beetles of the genus Mylabris. “Oh, that’s why they are called blister beetles!”, it dawned on me, a little too late. While walking through the grass I must have brushed against some of these insects, and a mere touch against my skin caused the blisters, which lasted for over a week, to appear. The beetles themselves are highly toxic, deadly even, and no bird or other vertebrate will try to eat them. It is therefore quite possible that the flies are fakers – not toxic at all but simply counting on predators’ reluctance to try a potentially harmful meal. This phenomenon, known as Batesian mimicry, is common in the animal kingdom and I strongly suspect that the flies are an example of it.

I strongly suspect that Red-headed flies are Batesian mimics of blister beetles of the genus Mylabris. These beetles not only cause painful, long-lasting blisters but are also potentially deadly toxic.

I strongly suspect that Red-headed flies are Batesian mimics of blister beetles of the genus Mylabris. These beetles not only cause painful, long-lasting blisters but are also potentially deadly toxic.

When I return to Gorongosa next month the flies should still be around. It will also be the time when many young house geckos (Hemidactylus mabouia) are hanging around the lights of the camp, having hatched in January and February. It might be a bit evil on my part, but I think I will do some feeding experiments to see if the lizards, which at that point should still be naive about the flies, have any adverse reaction to eating them. Watch this space.

One peculiar morphological characteristic of the Red-headed flies is the absence of the ocelli, which are typically found on the head of other flies.

One peculiar morphological characteristic of the Red-headed flies is the absence of the ocelli, which are typically found on the head of other flies.

Dermatobia Redux

Raising two dipteran children was an interesting experience. It was embarrassing on a few occasions, when both of my arms started bleeding profusely in public; painful at times, to the point of waking me up in the middle of the night; and inconvenient during the last stages of the flies’ development, when I had to tape plastic containers to my arms to make sure that I will not lose the emerging larvae. But other than those minor discomforts it was really not a big deal. Perhaps my opinion would have been different had the bot flies decided to develop in my eyelids, but I actually grew to like my little guests, and watched their growth with the same mix of pleasure and apprehension as when I watch the development of any other interesting organism under my care.

Having two bot fly larvae embedded in my skin have also made me ponder once again the perplexing element of the human psyche that makes us abhor parasites but revere predators. Why is it that an animal that is actively trying to kill us, such as a lion, gets more respect than one that is only trying to nibble on us a little, without causing much harm? I strongly suspect that it has to do with our genetically encoded sense of “fairness” – we perceive parasites as sneaky and underhanded, whereas predators attack us head-on and thus expose themselves to our retaliation. They are brave, or so we think. This, of course, is a very naive and anthropomorphic interpretation of nature. A lion is no “braver” than a bot fly, who has to skillfully hunt mosquitos to assure the dispersal of her eggs and risk more dangers than a lion, a top predator with no natural enemies. Most importantly, to a bot fly we, humans, are a renewable resource – it is in the bot fly’s best interest that we live a very long life and thus can be “reused” – hence the minimum amount of suffering that this species causes. To a lion we are nothing more than a one-time meal. But we should not judge either species for their actions – there is no “good” or “bad” in nature – nature is amoral.

I am saying this to prepare you for a short video that I have made about my experience of raising a bot fly. I don’t want you to think that it is “creepy” or “weird”. It is simply a documentation of an interesting organism, who happens to develop in the skin of large mammals. But please be forewarned that this video includes a few sequences that some viewers may find disturbing. If you don’t want to have nightmares about things living inside you (which they already do, by the way), please don’t watch it. But if you are prepared to be open-minded and appreciate God’s wonderful creations in all their amazing glory, enjoy the show!

Puppy-killing scientist smuggles rainforest babies in body cavity

I am pretty sure that taking this very photo in Belize was the beginning of my adventure with the Human bot flies.

I am pretty sure that taking this very photo in Belize was the beginning of my adventure.

I almost got away with it – for five days I had covered my body and slathered insect repellant onto my skin with an almost religious zeal, but on the last day I faltered. I was in Belize, teaching macrophotography at the Bugshot workshop. The course was almost over, and so I relaxed and decided to shoot some red-eyed tree frogs in the rainforest around the lodge. I rolled up my sleeves but, because I had misplaced my insect repellant and was too lazy to look for it, I did not put any DEET on. Big mistake. As I photographed the frogs, clouds of mosquitos, perhaps sensing a new, unprotected warm body, went to town on my arms and face. But, this being my last day in Belize, I decided to ignore the little vampires and kept taking pictures. Later that day my arms were quite itchy, but it was nothing new or unusual.

That's a nice-looking butt – I knew that something was amiss when a strange tube started poking out of my skin. This turned out to be a bot fly's breathing tube.

That’s a nice-looking butt – I knew that something was amiss when a strange tube started poking out of my skin. This turned out to be a bot fly’s breathing tube.

Things started veering off course after I got home. Some of the mosquito bites kept itching and, rather than disappearing, started to get bigger. It didn’t take me long to realize that I had brought with me, embedded in tiny holes in my skin, larvae of the Human bot fly (Dermatobia hominis). This was not the first time for me to have this parasite. What was new was the number of these animals that had made my body their home – at least six of them were feeding on both my arms, with four spaced only a millimeter apart on my right forearm. In the end, only three of them survived the first week. One of the surviving larvae was on my elbow. It was a nasty little thing, very active and painful. It had to go. But I decided to keep the two remaining larvae. As strange as it sounds, I felt bad about killing them, but I also had never seen an adult bot fly, and this was my chance.

Human bot flies are well known to entomologists and people living in warm, tropical parts of Central and South America. I cannot think of any of my biologist friends working there who didn’t have a torsalo living in their skin at some point or another, often in such very inconvenient places as the eyelid, the upper lip, or the top of the head. These get extracted through a variety of methods that often involve suffocating the larva with glycerine jelly, raw steak, or duct tape, and then pulling or squeezing the larva out of the skin. These methods usually work, but there is always a risk of leaving a part of the bot’s body in the wound, which may lead to infection. On those occasions where I needed to remove a larva, I preferred to use a suction venom extractor, which enlarges the opening of the wound (warble) and pulls the larva out, still alive and in one piece. I only discovered this method, first described 13 years ago (Boggild et al. 2002. Clin. Infect. Dis. 35: 336-8), after a visit to my doctor. Her solution was to perform a surgery by cutting my arm open. I said “thanks, but no thanks” and did my own research on furuncular myasis.

A mature larva of the Human bot fly (Dermatobia hominis) is an impressively armored animal. And yet it caused relatively little discomfort when feeding, deeply embedded in the skin of its host, me.

A mature larva of the Human bot fly (Dermatobia hominis) is an impressively armored animal. And yet it caused relatively little discomfort when feeding, deeply embedded in the skin of its host, me.

Human bot flies (D. hominis), despite their name, are not interested in our species only. They will gladly feed on other primates, as well as ungulates and other large mammals. Similarly, other members of the bot fly family (Oesteridae), who preferentially target small mammals, will occasionally find themselves on humans. But we get infected with D. hominis more often than with other bot flies because of this species’ unusual strategy of dispersing its eggs. Rather than laying them on the ground in the vicinity of mammalian burrows, the way other bot flies do, the D. hominis female catches and lays her eggs on other exoparasites: mosquitos, ticks, and deer flies. The eggs hatch while on the intermediate host and drop onto the skin of the ultimate host, often a human, when they sense its body heat. Frequently they will use the hole made by the mosquito to enter the skin but they can also use a hair follicle to get inside. Even the newly hatched larvae are covered with spines that point up, which makes pulling them out from the warble very difficult.

The puparium of the Human bot fly. The tufts on the front of the body are anterior spiracles that allow the animal to breathe when it matures in this stage underground. As the puparium ages it changes color from light brown to black. Remarkably, the spiracles stay the same, orange color.

The puparium of the Human bot fly. The tufts on the front of the body are the anterior spiracles that allow the animal to breathe as it matures  underground. As the puparium ages it changes color from light brown to black. Remarkably, the spiracles stay the same, orange color.

Once in the skin, the larva undergoes three molts and in 7-10 weeks grows from the size of a grain of sugar to that of a peanut. Throughout this time the warble enlarges and occasionally bleeds, but otherwise it is relatively painless, unless the larva decides to munch on nerve endings. These wounds rarely get infected as the larva very likely produces antibiotic secretions. Once fully grown, the larva crawls out of the warble and falls to the ground, where it quickly buries itself and turns into a puparium. The wound usually heals completely within a couple of days. All in all, not a big deal. But some people, for whatever reason, don’t like to have a squishy, almost harmless animal living in their skin.

Although we don’t think about them as such, Human bot flies are beautiful rainforest animals, as much a part of that ecosystem as howler monkeys and Morpho butterflies.

A mature Human bot fly (Dermatobia hominis). Although we don’t think about them as such, these flies are beautiful rainforest animals, as much a part of that ecosystem as howler monkeys and Morpho butterflies.

A mounting body of research indicates that many parasites have evolved a way of manipulating the behavior of their hosts. A parasitic horsehair worm will make its otherwise terrestrial grasshopper jump into the water, where it then ruptures the grasshopper’s body and swims away. Parasitoid wasps who have just left the emaciated body of a caterpillar will be actively protected by their brain-washed host. Humans also fall victim to parasitic manipulation – there is evidence that toxoplasmosis, a disease caused by protozoan Toxoplasma gondii, makes men less intelligent and prone to take greater risks (it has to do with increasing the likelihood of ending up as food for large cats, Toxoplasma’s ultimate host; inexplicably, the effect on women is a statistically significant increase in their intelligence.)

After I had decided to keep two of my botflies and let them reach maturity, I began to wonder – have the generations of entomologists, who let these flies live in their skin as a kind of geeky right of passage, inadvertently selected for a strain of bot flies that manipulate human behavior towards letting the flies live? Or do I just have toxoplasmosis?

A newly eclosed Human bot fly, with traces of the ptilinum on its head, a reversible pouch that gets inflated with hemolymph to help the young fly break free from the puparium.

A newly eclosed Human bot fly, with traces of the ptilinum on its head, a reversible pouch that gets inflated with hemolymph to help the young fly break free from the puparium.

In any case, the flies survived in my skin for nearly 10 weeks, successfully emerged, pupated, and are now enjoying a brief life as adults. Brief, because adult bot flies have no functional mouthparts and cannot feed, which means that they only live for a few days. They are quite pretty – I would go as far as to say that, among insects, they undergo one of the most dramatic transitions from ugly to cute during their development.

It was an interesting experience and I am glad that I managed to bring these insects to maturity. But rest assured that the next time I am in Belize my bottle of DEET will never leave my pocket.

Stay tuned for a video with some awesome sequences showing the development of my bot fly!

Update: The video is now available.

A composite photo showing the stages of the Human bot fly’s development. The size difference between the first and the third larval instal is particularly striking.

A composite photo showing the stages of the Human bot fly’s development. The size difference between the first and the third larval instars is particularly striking.

Postscript
I let my bot flies live and I went to great pains to make sure that they survived their inadvertent exodus from their native land of Belize. Will this endear me to people who wanted to crucify me for killing a puppy-sized spider a few months ago? I am guessing, no. Do I give a crap? Take a guess. Incidentally, now that the dust has mostly settled, I can repeat that I did not kill the puppy-sized spider – another scientist collected and preserved it – although this bit of information somehow didn’t register with the online media. There was no point in clarifying this because it is completely irrelevant to the issue of scientific collecting – I have killed and preserved my share of specimens, and I will always defend biologists who have the unpleasant duty to do so.

Postscript 2
Gil Wizen has written about his experience of raising a dipteran child on his blog.