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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)

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.

Mozambique Diary: Not all flies fly

Tsetse fly (Glossina sp.) from Gorongosa feeding on my blood. Luckily, tsetses in this area do not carry the dreaded sleeping sickness (but it does not make it any less painful).

Tsetse fly (Glossina sp.) from Gorongosa feeding on my blood. Luckily, tsetses in Gorongosa do not carry the dreaded sleeping sickness.

After a long hike in the scorching heat of the African savanna the cool, shady patch of tall miombo forest looked like heaven to us. I was in the southern part of Gorongosa, looking with a few friends for some elusive species of arthropods. But we were having little luck finding any and after several hours of strenuous walking the morale was low. As we stepped under the dark, inviting canopy of the forest, the drop in the temperature was palpable and we all relaxed, slowed down the pace, and the mood in the group immediately improved. But then, suddenly, somebody yelped “Ouch!” and at the same moment I felt a painful pin-prick at the back of my neck. Crap, tsetse flies! We looked around – they were everywhere. Clouds of them. We could see groups of dozens clumping on vegetation, taking into the air the instant they noticed the movement of our bodies. We ran.

A painting (undoubtedly the first and only) of a bat fly (Penicillidia sp.) burrowing in the fur of a Long-winged bat (Miniopterus).

A painting (undoubtedly the first and only) of a bat fly (Penicillidia sp.) burrowing in the fur of a Long-winged bat (Miniopterus).

Tsetse flies have long had a reputation for being one of the scourges of Africa, alongside malaria, crocodiles, and the plague of locusts. And deservedly so – some species of tsetses, all members of the genus Glossina, are vectors of nasty protozoans, including Trypanosoma brucei, the cause of the deadly sleeping sickness. Luckily for us, Gorongosa tsetses carry a different Trypanosoma species, T. congolense. This protozoan does not affect humans but unfortunately causes the chronic Nagana disease in cattle and horses, which explains the nearly complete absence of these animals around the park and in almost the entire region of central Mozambique. But knowing that tsetse bites are not going to kill us did not make them any more pleasant. Tsetses are large flies, about the size of a bee, and their skin-piercing mouthparts are much thicker than those of a mosquito. In other words, it hurts like hell when one jabs you with its proboscis, and you flail your arms like a madman to shoo it away while the fly escapes unharmed.

Members of the family Streblidae, such as this Raymondia sp., collected from the Hildebrandt's horseshoe bat (Rhinolophus hildebrandtii), often exhibit interesting adaptations in their wing morphology, such as the ability to fold them longitudinally along the back. This presumably helps them move swiftly in the pelage of their hosts.

Members of the family Streblidae, such as this Raymondia sp., collected from the Hildebrandt’s horseshoe bat (Rhinolophus hildebrandtii), often exhibit interesting adaptations in their wing morphology, such as the ability to fold them longitudinally along the back. This presumably helps them move swiftly in the pelage of their hosts.

But count yourself lucky. Imagine instead that you cannot shoo them away. You try to smack one but it runs, hides in your hair or some place where you are not able to reach, and it continues to bite. It only leaves your body to give birth somewhere in your house but then immediately runs back, guided by your scent and body heat. Oh, and imagine that this fly is the size of your fist (or a small puppy). Welcome to the world that bats are forced to live in.

Tsetses are members of a large group of flies, the superfamily Hippoboscoidea, all of which are exclusively hematophagous – blood is the only food that they are interested in. The tsetse family (Glossinidae) is the most basal (unsophisticated, one might say) member of this lineage of insects – they are always looking for a blood meal but never evolved the ability to stay with their tasty host. Bats are unlucky to have been colonized by two much savvier families of flies, the Nycteribiidae and Streblidae. These insects know the value of a good host and, once they landed on the furry back of a bat, they never leave it again. Over millions of years of coevolution with their mammalian hosts the bat flies have undergone a remarkable transition. From a free-flying ancestor, most likely very similar to today’s tsetse flies, emerged several lineages of highly modified, often completely wingless, spider-like creatures. Their body became flattened and very hard, making it almost impossible to squash them against the skin. In the family Nyctiberiidae the head turned into a small appendage that can be safely tucked away in a protective groove on the back and all traces of wings completely disappeared. These flies cannot survive for long outside of their host’s body and only feel at home when scurrying at an alarming speed in its dense fur. Their feet are armed with large claws that make it almost impossible to dislodge them from the hair of their host. They really don’t look like flies and when a friend spotted one on the body of a bat she called me to collect the bat’s “pet spider.”

In the closely related family Streblidae the wings may or may not be present, but even in the winged species the body is modified for squeezing through the fur, and members of the subfamily Ascodipterinae go even further in their commitment to the host. Much further. Once a female lands on a bat she sheds her wings and legs (yes, legs) and burrows head-first into the skin. Once there, her head and thorax sink into her own abdomen, and the skin of the bat overgrows her body. She becomes one with her host.

Penicillidia bat flies (Nycteribiidae) are some of the most unusual members of the order Diptera and hardly resemble their winged relatives. This individual was collected from a Long-winged bat (Miniopterus natalensis) in Gorongosa, Mozambique.

Penicillidia bat flies (Nycteribiidae) are some of the most unusual members of the order Diptera and hardly resemble their winged relatives. This individual was collected from a Long-winged bat (Miniopterus natalensis) in Gorongosa, Mozambique.

Female bat flies, like their relatives tsetse flies, are remarkably good mothers. The great majority of insects relies on what ecologist call “r-selection” in their reproduction – they lay hundreds or thousands of eggs, betting on one or two of them making it to adulthood. Bat flies, on the other hand, rely on “K-selection” – like humans, they prefer to invest a lot in a much smaller number of offspring, hoping that they will all make it to the reproductive age. They are larviparous – instead of laying eggs the female gives birth to a single, fully developed larva, which immediately turns into a pupa. While in her mother’s body, the larva feeds on “milk glands”, analogous to the mammalian mammary glands (if they were located in the uterus), and develops safely protected from the elements and predators. When the time comes for the mother to give birth she walks off the bat’s body and attaches the larva to the wall of the bat’s roosting place, usually a cave (which explains why bats that roost in rolled-up leaves and other less permanent places have fewer ectoparasites). Then she turns back and runs towards her host, guided by the smell and the heat of its body.

The recent Ebola crisis brought back the attention of the medical community to bats as potential reservoirs of the virus. Although there is no evidence that bats are in fact harboring the virus, there seems to be some correlation between instances of the outbreak and the presence of large numbers of bats in the affected areas. While reading the literature on both Ebola and bat flies I found it rather curious that nobody has tested bat flies for the presence of the virus – these are relatively very long lived (195 days on average) insects, who always stay (as pupae) at the roosting sites of bats, even when the hosts leave to forage elsewhere. They often move from one host species to another and, this point makes me really wonder why nobody has seriously looked at these flies as potential vectors, occasionally drop on and bite people. We know that they harbor a slew of pathogens – a recent study conducted in Gorongosa National Park on bats Rhinolophus landeri and Hipposideros caffer showed that flies living on these animals are vectors of Trypanosoma species that are ancestral to those that cause Chagas disease. Add to this the fact that one of the first cases of Marburg disease in Zimbabwe (caused by a virus related to Ebola) was caused by a bite of an arthropod (by default all unidentified bites seem to be classified by the medical community as “spider bites” and spiders in the area were tested, predictably unsuccessfully, for Marburg). It is far more likely that the bite was caused by a fly that fell off a bat.

A friend of mine recently expressed her dismay at “lowly” parasites. I beg to differ – if anything, parasites, including bat flies, are incredible examples of evolution at its best, organisms capable of both adapting to life in the most hostile of environments (the very substrate you live on wants you dead!) and resisting diseases that live inside your body. I cannot promise that I will not try to smack the next tsetse fly that lands on me but at least I promise that I will do it in the most respectful, considerate way.

Louse flies (Hippoboscidae) are close, equally modified for ectoparasitic lifestyle family of flies. This Lipoptena sp. was collected from a Nyala antelope while it was fitted with a GPS collar. Louse flies are parasites of large mammals and birds, and some are considered serious pests of sheep.

Louse flies (Hippoboscidae) are closely related to bat flies and equally modified for ectoparasitic lifestyle. This Lipoptena sp. was collected from a Nyala antelope while it was being fitted with a GPS collar. Louse flies are parasites of large mammals and birds, and some are considered serious pests of sheep.

Treehoppers

Nobody really knows what the strange structures on the head of the Bocydium treehopper are for. They don't use them in courtship and seem pretty ineffective for defense.

Nobody really knows what the strange structures on the head of the Bocydium treehopper are for. They don’t use them in courtship and seem pretty ineffective for defense.

“I need to have my vision checked” was the first thought that popped into my head when my eyes met a treehopper of the genus Bocydium sitting on a thin branch in the Braulio Carillo National Park in Costa Rica, where I was researching several newly discovered katydid species. I had seen many mind-boggling organisms during my years as a tropical entomologist, but this thing looked like something that had just disembarked from a tiny interstellar spaceship. All the parts expected of a self-respecting insect were there – six legs, compound eyes, two pairs of wings – but what was the deal with the huge modernist sculpture on the head?

An ant can elicit the production of a droplet of honeydew by gently stroking the treehopper (Harmonides sp.) with her antennae.

For ants, a colony of treehoppers is like a pasture full of cattle. They protect the insects and collect their nutritious honeydew. An ant can elicit the production of a droplet of honeydew by gently stroking a treehopper (in this case a Costa Rican Harmonides sp.) with her antennae.

Treehoppers, members of the family Membracidae, are distant relatives of cicadas and aphids, and just like them they feed on liquids that flow through vascular tissues of plants. Such diet is extremely rich in carbohydrates, to the point that the excess must be expelled by the treehoppers. They do so in the form of honeydew, sugary water, dripping off the end of their abdomen, a substance that other organisms, ants mostly, find both delectable and worthy of fighting for. For this reason ants frequently form mutualistic relationships with treehopers, and defend them against potential predators in exchange for nutritious droplets. Some ants are even capable of asking for honeydew by gently tapping or stroking the treehopper’s abdomen, to which the insect responds by dispensing the drink. In addition to ants, certain wasps and flies also take advantage of this resource, but do not seem to repay in any way.

This mutualistic relationship with ants can influence the maternal behavior of some species. In many treehoppers the female guards the eggs and newly hatched brood, shielding them with her body and fending off predators. But if ants are constantly present, assuming the role of the brood’s guardians, then there is no need for her to stick around and protect her children. Instead, she can move on and lay another clutch of eggs on a different part of the host plant. Treehopper species that lead solitary life and don’t display maternal guarding of the brood are unlikely to attract ants’ protective interest as it is simply uneconomical for the ants to travel long distances to collect honeydew from a single insect. Thus, in some cases, developing nymphs of solitary species join “herds” of communal treehoppers, thus gaining the benefit of ants’ services.

Treehoppers are excellent parents – this female Thorn treehopper (Umbonia sp.) is shielding her eggs with her body; if necessary she can also use her powerful legs to kick potential predators.

Treehoppers are excellent parents – this female Thorn treehopper (Umbonia sp.) is shielding her eggs with her body; if necessary she can also use her powerful legs to kick and ward off potential predators.

But treehoppers are by no means helpless and, in the absence of ants, can defend themselves quite effectively using deceit, amazing body armor, and kickboxing (or at least an insect version of it). Nearly all species of treehoppers carry a massive, often intricately shaped and beautifully colored shield-like thoracic structure known as the helmet. In most cases its function is that of crypsis – many species resemble thorns, tiny leaves, or random bits of vegetation. Others use their helmet and bright coloration to turn into perfect replicas of stinging wasps, albeit they of course remain completely harmless.

Members of the tribe Hoplophorionini, however, go beyond such passive defense and have evolved powerfully muscled, spiny legs, which they are not shy to use on a wasp or any other predator that makes a mistake of straying too close. They kick and flap their wings, which is usually enough to drive away a predator several times their size. In those species where the female guards a large group of children, who usually position themselves in a long line all along a branch of their favorite plant, the insects employ a complicated language of acoustic signals – the nymphs can “talk” to the mother by sending substrate-borne vibrations, alerting her to an approaching enemy so that she can come running and ward the predator off. Acoustic communication is also used among adults to find mates, stake territories, or warn others about predators. Some species eavesdrop on other treehoppers to look for richer or safer pastures.

Two extreme examples of treehopper morphology – Membracis zonata, showing disruptive coloration that conceals the fact of being an insect, and Cladonota ridicula, a perfect imitator of a dead speck of vegetation.

Two extreme examples of treehopper morphology – Membracis zonata, showing disruptive coloration that conceals the fact of being an insect, and Cladonota ridicula, a perfect imitator of a dead speck of vegetation.

Entomologists had always assumed that trehoppers’ helmet was a simple outgrowth of the pronotum, or the dorsal plate of the first segment of the thorax. Pronotal modifications can be seen in other groups of insects (beetles or grasshoppers, for example), and thus it was only logical that treehoppers represented merely an extreme case of such a development. But a study published in 2011 by Benjamin Prud’homme and his colleagues (pdf) challenged this view. It provided tantalizing evidence that the awesome structures that treehoppers carry on their bodies are essentially a third pair of wings that had evolved to play a very different function. By carefully studying the embryonic development of treehoppers and mapping the expression of certain Hox genes (genes that control the development of serial structures, such as an insect’s body segments), they were able to show that the helmet of treehopers starts as a pair of tiny wing-like structures that later expand and fuse above the body. In some cases they even retain traces of hinges that are present at the base of normal insect wings.

And thus we know how, but not necessarily why. Some entomologists have suggested that the otherworldly shapes of Bocydium and other insane treehoppers are examples of ant mimicry, or simply serve to turn the body of an otherwise helpless insect into an equivalent of unpalatable fishhooks. But there might be another explanation – what if these structures are sophisticated satellite antennas and the treehoppers use them to stay in touch with the mothership? Probably not. Or maybe?

What possible function can these massive horns play in this Costa Rican treehopper Umbelligerus sp.?

What possible function can these massive horns play in this Costa Rican treehopper Umbelligerus woldai?

A portrait of a Costa Rican treehopper Poppea capricornis.

A portrait of a Costa Rican treehopper Poppea capricornis.

A new voice in the chorus

A pair of Jumping Bush Crickets (Orocharis saltator) from Massachusetts. Females have long, needle-like ovipositors, which they use to lay eggs deep into the stems of plants.

A pair of Jumping Bush Crickets (Orocharis saltator) from Massachusetts. Females have long, needle-like ovipositors, which they use to lay eggs deep into the stems of plants.

Yesterday evening, right before the weather turned nasty, as I stood on the deck over my garden I suddenly caught a sound wave, one that I immediately recognized but had never before heard around my house. I ran to grab my recorder and was able to capture a snippet of the call. Seeing me pointing my microphone towards his house, a neighbor approached me warily, inquiring if I am trying to find the property line. I explained what I was doing and he left, satisfied in his knowledge that I am just feeble minded, and not trying to sue him for his land.

The call was that of the Jumping Bush Cricket (Orocharis saltator), a species I first encountered a couple of years ago in Cambridge, MA. Since then I have been looking for other places where this pretty animal might live, but never expected to find it in my backyard. It is a species that belongs to the chiefly tropical subfamily Eneopterinae, and makes a fine addition to the chorus of crickets around my house, which now includes 12 species:

Jumping Bush Cricket (Orocharis saltator)
Handsome trig (Phyllopalpus pulchellus)
Say’s trig (Anaxipha exigua)
Carolina ground cricket (Eunemobius carolinus)
Allard’s ground cricket (Allonemobius allardi)
Striped ground cricket (Allonemobius fasciatus)
Two-spotted tree cricket (Neoxabea bipunctata)
Snowy tree cricket (Oecanthus fultoni)
Spring field cricket (Gryllus veletis)
Fall field cricket (Gryllus pennsylvanicus)
House cricket (Acheta domesticus) (introduced)
Eastern ant cricket (Myrmecophilus pergandei)

Sonogram of the Jumping Bush Cricket (Orocharis saltator); click here to listen to the recording.

Sonogram of the Jumping Bush Cricket (Orocharis saltator); click here to listen to the recording.

A male Jumping Bush Cricket (Orocharis saltator).

A male Jumping Bush Cricket (Orocharis saltator).