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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)

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.

Mozambique Diary: How to kill an assassin

The African assassin bug (Glymmatophora sp.) from Gorongosa, Mozambique

The African assassin bug (Glymmatophora sp.) from Gorongosa, Mozambique

I often lament the fact that humans are freakishly gargantuan next to nearly all other animals, and thus unable to appreciate the beauty and complexity of the majority of smaller life forms that share the world with us. Yet, at the same time I am thankful that we do not need to contend with the likes of tiger beetles or solifugids, and that ambush bugs will never succeed in luring us into their deadly grip with their imitation of the sounds that humans make. Compared to even the most vicious and dangerous mammals, the world of arthropods is orders of magnitude more advanced in the art of killing – if a lion were to be shrunk to the size of an average insect it would last no more than a few minutes before being dismembered by the first praying mantis or a spider, who would laugh at its puny claws, soft and squishy body, and the complete lack of any real weapons.

The hunt begins –the assassin bug notices the millepede and begins to approach it.

The hunt begins –the assassin bug notices the millepede and begins to approach it.

And although I prefer to study the more peaceful aspects of invertebrate behavior, such as their courtship and love songs, I cannot help but be impressed by the sophistication of weaponry used by arthropods to kill, or exact revenge on those who try.

On my last night in Mozambique, when I should have been packing and getting some sleep before a long journey home, I suddenly realized that I had almost missed the opportunity to solve the mystery of how ectrichodiine assassin bugs hunt their favorite prey, the giant African millipedes. I had caught a beautifully metallic, wingless assassin bug (Glymmatophora sp.) a few days earlier, and now all I needed was its prey. Luckily, I was still in Gorongosa, where most biological questions can be answered by taking a slow walk and paying attention, and within a few minutes I managed to find a large millipede.

Without the millepede being aware of it, the assassin bug slowly crawls on top.

Without the millepede being aware of it, the assassin bug slowly crawls on top.

For a docile, seemingly harmless animal, millipedes (Diplopoda) have surprisingly few enemies. As is often the case among small animals, an innocent demeanor hides powerful and quite unexpected defensive strategies. Millipedes have two major lines of defense, both effective enough to deter virtually all predators. First, the chitinous base of their exoskeleton is composed of up to 70 percent calcium and magnesium carbonate, making it much harder than that of most terrestrial arthropods. Few predators are strong enough to crack it, although mongooses have been reported to toss  millipedes against rocks to break their shells. For smaller predators such as spiders, the hard exoskeleton is an almost impenetrable barrier. But if one tries its luck anyway, a rich arsenal of chemical warfare stops the predator in its tracks, literally. Some millipedes produce substances that act as sedatives, forcing the spider into a state of suspended animation that lasts for many hours. Interestingly, this substance is virtually identical to the drug quaalude, a synthetic sedative once widely used in medicine and as a recreational drug. But licking millipedes to get high is not a good idea as many species produce cyanide, the most powerful inorganic poison known to man.

The assassin bug positions itself so that its rostrum can be inserted between the millepede's legs.

The assassin bug positions itself so that its rostrum can be inserted between the millepede’s legs.

Others exude substances that cause vomiting, headaches, and other unpleasant effects. And yet, few millipede species have warning coloration, which is typical of organisms that produce repellant chemicals. It is believed that the extreme effectiveness of their chemical weapons, combined with the very long time they have been around (terrestrial millipedes date back to the Carboniferous), made predators develop a genetically based aversion to these animals, and the millipede’s shape alone is a sufficient warning.

Once in place, the assassin bug delivers the deadly bite.

Once in place, the assassin bug delivers the deadly bite.

Assassin bugs (Reduviidae: Ectrichodiinae) are some of the very few animals that are able to hunt millipedes. They overcome the millipedes’ mechanical defenses by injecting them with a fast acting venom through a soft membrane between the calcified plates that cover their body. They also avoid being poisoned by their prey’s chemical defenses thanks to the way they feed – rather than chewing food, and thus potentially ingesting some of the toxic compounds, they inject their prey with digestive enzymes and then drink the liquified tissue through a long, sharp rostrum. All this is well known to biologists, of course, but surprisingly there exist very few documented observations of how the hunt unfolds, and what part of the millipede’s body is targeted by the assassin bug. On my last night in Gorongosa I had a chance to find out.

The assassin bug's bite makes the millipede convulse and exude yellow droplets of toxic benzoquinones.

The assassin bug’s bite makes the millipede convulse and exude yellow droplets of toxic benzoquinones.

I placed the two animals on the white stage of my field photo studio and waited. After a few minutes the assassin bug noticed the millipede and started to approach it stealthily. With imperceptibly slow steps it climbed the millipede’s body and positioned itself almost upside down, with the head and rostrum facing the ventral side between the millipede’s legs. It was clearly aiming for the softest part of the body. And then, with an amazing speed, it pierced the millipede with its stiletto-like rostrum. The millipede’s reaction was dramatic – its body twisted and uncoiled like a spring, nearly sending it up into the air. After a few seconds the body relaxed, and yellow, acrid droplets started oozing from between its plates. This was the moment when the assassin bug decided to walk away.

After a few minutes the millipede is dead (but read the entire story to see what happened next).

After a few minutes the millipede is dead (but read the entire story to see what happened next).

I was already feeling bad for staging this drama, but the bug’s behavior made me feel even more guilty. “You ain’t going nowhere, buddy”, I thought as I placed a large container over the predator and its prey, “finish the job and eat it.” I simply could not understand why the assassin bug, which clearly must have been hungry, would suddenly abandon its dinner. And then, within a couple of minutes, the assassin bug was dead.

It all now made sense – the assassin bug was not abandoning its kill, it was just walking away to avoid being poisoned by the deadly benzoquinones dripping from the body of its victim. It would have undoubtedly come back to feed after the millipede had died and most of the volatile chemicals had blown away. By placing a container over the two animals I created a gas chamber that killed them both. I still feel awful about it but, alas, this is how biological mysteries are sometimes solved. I strongly suspect that the scent of benzoquinones, which are only emitted by an injured or dying millipede, acts as a long-range attractant to other assassin bugs that are often seen feeding communally on large millipedes, but at the same time the animal that made the kill must temporarily move away to avoid death from the same compounds. Aren’t invertebrates amazing?

Only in America

Only in America – both 13- and 17-year periodical cicadas are found mostly in the northeastern portion of the United States, with a few broods extending as far West as Kansas and as far South as Louisiana.

Only in America – both 13- and 17-year periodical cicadas are found mostly in the northeastern portion of the United States, with a few broods extending as far West as Kansas and as far South as Louisiana.

I first learned about the existence of periodical cicadas when I was a young boy, still living in z Old Country. The idea that an insect could develop underground for 17 years was crazy enough, but the fact that after all that time every individual within the population emerges at once in a synchronized, massive wave was almost too much to believe. Naturally, I became obsessed with this incredible phenomenon, which takes place only in the eastern half of the United States, and nowhere else in the world. To make it even more interesting, in addition to their unusual biology, these insects were reputedly quite tasty, thus combining my two greatest passions – entomology and exotic dining – into one, handy package. I very badly wanted to see them.

A nymph and an adult of a 17-year periodical cicada (Magicicada septemdecim) from Meriden, CT.

A nymph and an adult of a 17-year periodical cicada (Magicicada septendecim) from Meriden, CT.

My first opportunity came in 2004, when Brood X of the 17-year cicadas emerged in Washington DC and the surrounding states. Like the birds and dogs, which go crazy at the sight of such an unexpected bounty and stuff themselves with cicadas until they are ready to burst, I also went a little nuts. My friend Leeanne and I organized a cookout, daring others to try our fried, chocolate-covered, and roasted cicadas and, in the final stage of the entogastronomical orgy, live ones. Surprisingly, live, freshly molted (teneral) cicadas turned out to be absolutely delicious, combining a firm but yielding texture, with a creamy, delightfully nutty flavor. Now that I think about it, they might be considered a terrestrial equivalent of raw oysters. I wonder how they would taste with a drop of champagne mignonette and a touch of horseradish?

Nymphs of periodical cicadas spend 13 or 17 years underground, feeding on roots of trees. Their front legs are enlarged and perfectly adapted for digging.

Nymphs of periodical cicadas spend 13 or 17 years underground, feeding on roots of trees. Their front legs are enlarged and perfectly adapted for digging.

The opportunity to find out may be at hand. This June, for the first time since 1996, 17-year cicadas (Brood II) are emerging in central Connecticut, and thus not too far from my home in Massachusetts. Yesterday I took a drive to Connecticut to see if I can score some of the beautiful and delicious insects. With friends Derek and Melissa we arrived at a particular street corner in Meriden, CT, which we had carefully selected based on the latest reports of cicada sightings. The first thing I noticed after stepping out of the car was the persistent hum of cicadas calling from high in the trees. There were clearly thousands of them in this neighborhood, and soon we started seeing small clusters of cicadas sitting on trees and bushes. Alas, they were all mature adults.

When finally ready to molt, cicada nymphs climb trees and other tall objects, and transform into beautiful adults.

When finally ready to molt, cicada nymphs climb trees and other tall objects, and transform into beautiful adults. This individual is a member of the Brood X, which emerged in 2004.

To eat cicadas, one must collect them while they are still soft and lightly colored, before the chitin of their exoskeleton hardens and the wings fully expand. Still, it was great to be able to see these amazing insects again. Derek and I spent some time photographing the cicadas, although strong and gusty wind made it quite difficult. After my friends had left I stayed a bit longer, determined to find some teneral individuals. I did not find any, but after some digging in the soil I located cicada nymphs. I brought a few of them home, and now all I need to do is wait, and make some mignonette sauce.

Newly emerged (eclosed) periodical cicadas are almost snow white, but within a couple of hours their body darkens and their exoskeleton becomes hard.

Newly emerged (eclosed) periodical cicadas are almost snow white, but within a couple of hours their body darkens and their exoskeleton becomes hard.

An empty exuvia of a periodical cicada.

An empty exuvia of a periodical cicada.

Adult periodical cicadas live for only a couple of weeks, and during this time they feed on juices of plants.

Adult periodical cicadas live for only a couple of weeks, and during this time they feed on juices of plants.