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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).

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.

Hugewings

The enormous mandibles of a male dobsonfly (Corydalus)look like formidable weapons, but they are not. The males use them only in ritualized combat with other males and are too weak to use them to pinch or hurt anybody.

The enormous mandibles of a male dobsonfly (Corydalus) look like formidable weapons, but they are not. The males use them only in ritualized combat with other males, and are too weak to use them to pinch or hurt anybody (Barbilla N.P., Costa Rica).

As somebody who grew up in Europe I was really hoping that enrolling in a graduate school in the US would give me a chance to see many organisms that are rare or completely absent from the Old Continent. And, sure enough, as soon as I arrived in New England I almost got into a car accident after spotting my first Virginia possum, I giggled like a little girl at the sight of Black vultures feasting on a roadkill (probably a possum), and almost had a heart attack from the excitement of finding my first horseshoe crab on a beach in Connecticut. But nothing could prepare me for what one evening came to the light of the house that I shared with my then girlfriend. It was a creature so spectacular and unlike anything I had ever seen before that it took me a while to even put it in a broad taxonomic context. “It’s a megalopteran!”, I finally managed to exhale. “Oh yeah, a dobsonfly”, said Kristin, “They are pretty neat.”

Female dobsonfly in her natural habitat along a stream in Tapanti National Park in Costa Rica.

Female dobsonfly in her natural habitat along a stream in Tapanti National Park in Costa Rica.

That was my first introduction to the genus Corydalus, a massive creature that fully deserves to be a member of an insect order christened Megaloptera, or Hugewings (I just made this name up, but I think it’s fitting; as far as I know Megaloptera do not have a single-word common name despite being a well-recognized monophyletic lineage). They easily attain a wingspan of 140 mm (5.5″) and in flight are more akin to bats than insects. The dobsonfly that came to our light was a male and thus carried enormous, tusk-like mandibles that gave him a menacing look.

One of the few colorful members of the order Megaloptera, a Costa Rican dobsonfly Chloronia sp.

One of the few colorful members of the order Megaloptera, a Costa Rican dobsonfly Chloronia sp.

But, like so many seemingly dangerous invertebrates, a male dobsonfly could not hurt anybody even if he really tried. The gigantic mandibles are for show only, and the animal barely has enough muscle power to open and close them; actually biting is completely out of the question. Males use these ridiculous implements in largely ritualized combat with their rivals, a slower, weaker version of the jostling display seen in stag beetles. But be careful with dobsonfly females – while the males carry a pair of chopsticks, these have a pair of powerful wire cutters that can easily draw blood from careless fingers. Dobsonflies don’t live long as adults and, other than drinking water or an occasional visit to a flower to sip some nectar, don’t feed, and die within a few days.

A female dobsonfly taking off from a leaf at night in Tapanti National Park in Costa Rica.

A female dobsonfly taking off from a leaf at night in Tapanti National Park in Costa Rica.

The genus Corydalus is represented by 34 species, found mostly in the tropical regions of the Americas, and only the Eastern dobsonfly (C. cornutus) reaches as far North as Canada, while two additional species can be found in the southernmost parts of the US. The mandibles are enlarged in males of most species in this and in a closely related genus Acanthacorydalis from E Asia, although in Costa Rica I once caught a male of another dobsonfly with exaggerated sexual traits, Platyneuromus soror. His head carried two strange plates that reminded me of the facial lobes seen in an old male orangutan. Why they have them is unknown as they do not appear to use them in any way during courtship or mating.

The function of the large lobes on the head of Central American dobsonfly Platyneuromus soror is a complete mystery.

The function of the large lobes on the head of Central American dobsonfly Platyneuromus soror is a complete mystery.

The larvae of dobsonflies are aquatic and are well known to fishermen as hellgrammites (or helgies) – large, wiggly insects that make excellent bait for bass and trout. They are predators of other aquatic insects, such as caddis flies. Interestingly, while most species prefer large, well-oxygenated bodies of water (and thus make good indicator species of water quality), larvae of some hugewing species are capable of developing in such unusual habitats as water accumulated in tree holes or the digestive liquid at the bottom of pitcher plants. Those species that live in seasonal bodies of water are capable of aestivation, burying themselves is mud cocoons to await the return of water (very much like the lungfish). Interestingly, dried larvae of Megaloptera are used in Japanese traditional medicine to treat emotional problems in children, they are also consumed as a snack Zazamushi (not very tasty, according to my friend Kenji).

Hugewings give the impression of being ancient and primordial, and for good reason. They date back to the Permian, and are probably direct descendants of some of the earliest holometabolan insect (insects with the complete metamorphosis). They used to be lumped with the Neuroptera (netwings), but there is good evidence for their status as a monophyletic sister group to the Neuroptera.

Three species of hugewings common in New England.

Three species of hugewings common in New England.

The amazing Glass katydid

A young nymph of Glass katydid (Phlugis teres) from Suriname sitting on the tip of my finger.

A young nymph of Glass katydid (Phlugis teres) from Suriname sitting on the tip of my finger.

Once again things have been slow on my blog as I am trying to finish a million little things before my upcoming departure for Mozambique. I will be arriving there at the beginning of the rainy season, which means tons of insects and other invertebrates, a multitude of frogs, and hopefully some great new stories for this blog.

One of the animals that I hope to see there is a pretty, yet unnamed katydid from Mt. Gorongosa, which I first found last year in the mid-elevation rainforest on the mountain slopes. I am now working on its formal description and will post its photos as soon as the paper is out. In the meantime I thought I would present one of its close relatives, the amazing Glass katydid from Central and South America, a member of the genus Phlugis (Listroscelidinae).

As they age, Glass katydids begin to lose their transparency, and older nymphs and aduls acquire pale green coloration.

As they age, Glass katydids begin to lose their transparency, and older nymphs and aduls acquire pale green coloration.

I coined the name Glass katydid after seeing for the first time young nymphs of Phlugis teres, a species found in Suriname, who display remarkable, nearly complete transparency of their bodies. These minute insects truly look as if they were made of glass and, peering closely, it is possible to see most of their internal organs, including the entire tracheal system. Unfortunately, these katydids lose most of the transparency as they get older, and eventually acquire pale green coloration, occasionally marked with brown accents.

It would seem that something so seemingly fragile cannot feed on anything other than dew and rose petals, but in fact Glass katydids are agile, powerful predators. Unlike most of neotropical katydids, the genus Phlugis includes many diurnal species that use their excellent vision to find prey, and their hunting technique is very clever. Glass katydids are sit-and-wait predators who spend most of the day sitting upside down on the underside of large, thin leaves, usually at the edge of the rainforest or in open, shrubby habitats. They prefer leaves that are fully exposed to the sun so that any insect landing on its upper surface will cast a dark, sharply defined shadow. And that shadow is what Glass katydids are waiting for – it tells them whether the insect is a hard beetle (not good) or a soft fly (excellent), and if the insect looks like a good meal they launch themselves from under the leaf and onto its surface, and capture the victim with their long, very spiny legs in a blink of an eye.

In addition to being some of the most sophisticated and fastest orthopteran predators, Glass katydids are famous for the sound they produce – their call exceeds the frequency of 55 kHz, which is about three times the frequency a human ear is capable of hearing. A closely related genus Archnoscelis holds the record of producing the highest frequency call among all invertebrates – a whopping 129 kHz, twice the frequency of echolocation of most bats, and about 10 times more than the hearing ability of most adult humans. Another reminder that the ability to look cool and do amazing things seems to be inversely correlated with the body size.

Their huge eyes are a good indication of Glass katydids’ mode of hunting – they are diurnal sit-and-wait predators of small flies and other soft insects. This newly discovered, yet unnamed species from Costa Rica hunts small flying insects along the edges of mid-elevation rainforest.

Their huge eyes are a good indication of Glass katydids’ mode of hunting – they are diurnal sit-and-wait predators of small flies and other soft insects. This newly discovered, yet unnamed species of Phlugis from Costa Rica hunts small flying insects along the edges of mid-elevation rainforest.

The miracle of parallel evolution

Herpetologists, can you tell which is which? Left: Centrolenella spinosa from Costa Rica, right: Hyperolius cf. pusillus from Mozambique.

Herpetologists, can you tell which is which? Left: Centrolenella spinosa from Costa Rica, right: Hyperolius cf. pusillus from Mozambique.

I have been going through photos taken during a recent trip to Mozambique, and every now and then I am struck by the similarity of some of the African organisms to their counterparts on other continents. One of the best such examples is that of Neotropical glass frogs (Centrolenidae) and some African reed frogs (Hyperoliidae). Their resemblance to each other is uncanny – the two animals display a virtually identical, nearly translucent body, and only the shape of their toe pads reveals which is which. And yet these two lineages of frogs are separated by at least 150 million years of evolution, with many forms that look nothing like them in between, but ended up evolving the same, homologous morphology.*) These two groups differ quite significantly in their biology, however. The South and Central American glass frogs are forest animals, spending most of their life in the trees, often high in the rainforest canopy. They lay their eggs on the underside of leaves that hang over fast flowing streams. Males of these frogs often guard multiple egg clutches, until hatching tadpoles are washed off by rain into the stream below. The African “glass frogs”, members of the Hyperolius nasutus species complex and a few others, have a very different lifestyle, and are found in open, grassy areas of the southern part of the continent. They lay eggs underwater in big clumps attached to submerged plant stems, and exhibit no parental care.

Seems to me that parallel evolution is another argument against the existence of a magical intelligent designer – if the designer is intelligent enough to invent loa loa and the HIV virus, why are so many of its designs so incredibly repetitive? (I say “its” because if this omnipotence exists, I cannot imagine that it sports a set of male, or any other, genitalia.) If I could create anything I would at least give some frogs laser eyes. Or make tiny dragons with wings. Oh, wait.

One distinguishing feature of true glass frogs is the position of their eyes, which point forward, giving them more human-like appearance.

One distinguishing feature of true glass frogs is the position of their eyes, which point forward, giving them more human-like appearance.

African reed frogs have more typical eyes, positioned on the sides of the skull.

African reed frogs, like this Hyperolius cf. pusillus from Gorongosa National Park in Mozambique, have more typical eyes, positioned on the sides of the skull.

*) Parallel evolution is different from convergent evolution in that in the former similar structures evolve independently but use homologous elements e.g., pterodactyl and bat wings, whereas in the latter similar solutions are developed by using unrelated, non-homologous elements e.g., shells of ostracod crustaceans and clams.