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Mozambique Diary: Snug as a bug

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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 very 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)


Filed under: Bats, Behavior, Gorongosa, Hemiptera, Mammals, Mozambique

Ghost hunting

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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.

 

 


Filed under: Gorongosa, Macrophotography, Mozambique, Praying mantids

Lungless and happy about it

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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).


Filed under: Amphibians, Behavior, Costa Rica, Macrophotography, New England

Mozambique Diary: Coconut crabs of Vamizi

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The coconut crab (Birgus latro), the coolest, most awesome, most beautiful inhabitant of the Vamizi Island. These animals have adapted to live around humans and the conservation group on the island does a good job of protecting them.

In July 1937 Amelia Earhart’s plane vanished somewhere over the southern Pacific in the general vicinity of New Guinea. Neither the plane nor her and her co-pilot’s bodies were found during the massive search operation that followed. But two years after her disappearance scattered skeletal remains, later identified as those of a tall woman of European descent, were found on the (then) desert island of Nikumaroro, one of the possible crash sites of Earhart’ aircraft. The skeleton was far from complete and many bones were missing, and the suspicion immediately fell on coconut crabs, common on the island. They were accused of carrying the bones and squirreling them away. But recently a group of history buffs called TIGHAR came to the crustaceans’ defense, claiming that these animals did not customarily carry away food into their burrows. They even conducted an experiment by placing a pig carcass on the beach of Nikumaroro and recorded a fascinating time lapse video of the crabs stripping it of its flesh. Crucially, though, no bones were carried away by the coconut crabs. But it still showed very convincingly that, had the crabs found Amelia Earhart’s body, they would have eaten her completely in a matter of days. I certainly find this explanation far more compelling and easier to think about than the alternative proposed by the authors of the pig experiment – that her body was eaten not by the crabs but by her starving co-pilot who might have survived the crash. Why the hell would he ever resort to cannibalism on an island full of large, delicious crustaceans and coconuts? (And what happened to him? Two years after the crash people arrived on the island and, if movies are any indication, they should have found a muscular demigod who had a meaningful relationship with a volleyball.)

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Coconut crabs prefer to be active at night and during the dusk. That is when they emerge from their burrows to look for food.

These thoughts ran through my head as I squeezed it into holes in the rugged karst rocks of Vamizi, an island off the coast of northern Mozambique, looking for coconut crabs. Their burrows turned out to be full of coconut shells and other food remains, indicating that a single experiment good science makes not. I had been dreaming of visiting Vamizi ever since my friend Harith showed me a cell phone photo of himself on the island, holding two coconut crabs. All my life I had been fascinated with those magnificent creatures, the largest, heaviest, most awesome of invertebrates that grace the terrestrial surface of the planet. Some years ago I was lucky enough to see these animals alive, first on Guadalcanal, later on Japan’s Okinawa Island, but in both cases they were individuals already captured by somebody else. In those places coconut crabs are on the brink of disappearance due to habitat loss and overharvesting, and I never had a chance to observe them in their natural habitat. Vamizi, however, a tiny speck of paradise in the Quirimbas Archipelago, still appears to have a healthy population of these animals.

Birgus_Vamizi2

Coconut crabs come in two main color forms, a blue and a red one, both of which can be found in the same population.

Coconut crabs survive on Vamizi thanks to a clever campaign developed by the good people of the Vamizi Marine Conservation Research Centre. If, they say to the locals who traditionally used to hunt the crabs, you kill one, a terrible spell will never let you leave the island. In a country that is full of many ridiculous colorful myths, this scary thought has apparently kept many from falling to the temptation of the coconut crab’s meat. How many crabs survive on the island is unknown but apparently during the wet season it is possible to see a dozen or more coconut crabs on a single stroll through the coastal woodland.

I arrived on Vamizi in June, during the cool, dry season, and the locals were not too optimistic about my chances of finding one. (“They sleep now.”) But I didn’t fly to northern Mozambique on the thieving (camera gear was stolen from our checked-in luggage) and occasionally suicidal LAM airlines (go ahead, google it) to leave without seeing a coconut crab. According to Harith the best chance of finding one would be at a place that reliably provides the crabs with their favorite food. No, not coconuts. They prefer something else – fresh garbage.

“Take me to the dump”, I asked Harith as soon as it started getting dark. As we approached the island’s refuse disposal site we heard a sound that I would have never associated with coconut crabs – loud clicking of empty bottles. And there they were. Two giant, surprisingly colorful animals, moving among a big pile of glass, looking for edible bits of organic matter. The setting was not natural, it certainly wasn’t beautiful, but I almost choked up when I saw them. It was at the same time a fulfillment of a life-long dream, to see coconut crabs in the wild, and a sad, disappointing realization that “wild” is a big pile of junk and rubbish, reeking of rotten food and overrun by rats. The Anthropocene, in its full splendor and glory.

Birgus_Vamizi4

The Anthropocene – is this what a “wild” habitat should be?

Over the next few days my outlook had improved as I counted and photographed the crabs, looking for an indication that the population was breeding on the island. A large part of the island is a well-protected nature reserve, full of gorgeous tropical life, including thousands of land crustaceans, small mammals, breathtaking birds, and cool reptiles (including two species new to science, which Harith will soon be describing.) And I won’t even mention the marine life, which puts Vamizi at the top of the list of the most spectacular diving sites of the world. The most reliable proof of the crabs breeding there would have been finding juveniles still in their shells. Coconut crabs (Birgus latro) are oversized, fully terrestrial hermit crabs, that, just like other members of the hermit crab family Coenobitidae, develop as microscopic planktonic larvae in the ocean, and must don an empty snail shell during the first months of their life on land to protect the still soft and fragile abdomen. Only after reaching the size of about 10 mm do they abandon the shell and assume the symmetrical appearance that differentiates them from other hermits (in all other species the abdomen remains asymmetrically twisted throughout their life.)

Birgus_Vamizi

Coconut crabs are excellent climbers. Also known as robber crabs, they are known to raid bird nests.

I must have picked up and examined about a thousand hermit crabs but, alas, they all turned out to be one of the two local species of Coenobita. A trip to a coconut grove at the opposite end of the island to look for juveniles hiding in the fallen fronds and coconut husks underneath the palm trees was similarly fruitless. That was worrisome. Rats are known to kill juvenile coconut crabs and the island was full of them. We saw rats not only around the houses but also in the most remote, virtually unspoiled natural habitats of Vamizi. One night my friend Max was startled by a gecko that hurled itself towards his head from the very top of a tall tree to escape a rat chasing it on the thin branches. Adult coconut crabs can and will kill a rat, but younger ones don’t stand a chance. Thankfully, the tourism company &Beyond, which operates the phenomenal eco-resort on the island, has been working diligently to improve the situation. To remove invasive species from Vamizi without harming its native populations of samango monkeys and other small mammals they use specially designed rat-only traps, ultrasonic repellents, and other tools to get rid of the nasty aliens.

Every night I spent hours looking for juvenile crabs along the paths in the forest but all I was seeing were very mature adults. On the last night, dispirited by not finding any proof of new blood in the population, I walked further than usual and ended up being out in the field well past 2 AM. Tired and despondent, I decided to have one last tour of the resort staff houses, the most reliable spot for finding coconut crabs at that time of year. There were a few adults milling around but they soon left for their burrows in the forest. That was it. During my four days on the island I did not see any evidence that the animals were breeding. A similar pattern has been seen in other places inhabited by coconut crabs, where the pressure from invasive species, overharvesting, and habitat loss either prevents the animals from breeding or leads to unnaturally high mortality of juveniles. Despite coconut crabs’ longevity (they can live to be 60), with no young crabs surviving the population eventually dies out.

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All I can say is that I am glad that I am taller than a coconut crab (albeit not by much!)

I swept the light of my headlamp around, noticing for the first time the fence at the far end of the compound, overgrown with tall, spiky weeds. It occurred to me that I had never checked what lived among them. If I were a young coconut crab, would I want to compete with the adults, and risk being eaten, by feeding at the same spot, at the same time of night? I climbed the fence and crawled through the thicket, long, thorny branches ripping my shirt and cutting my skin. The ground below the weeds was covered with Coenobita hermit crabs, frantically gorging on discarded scraps of food. And there, among the hermits, were the juvenile coconut crabs. They weren’t much bigger than the large hermit crabs C. brevimanus common on the island, about 5-7 cm long. I let out a sigh of relief. The presence of young coconut crabs made it clear that the population was thriving, or at least not dying out. And the help they get from the conservation group working on the island will certainly improve their chances.

The next morning Harith, Max, and I left the island, having learned not only that it had a good population of coconut crabs, but also that eating oysters directly off the sun baked rocks exposed by the low tide really helps you purge your digestive system. I hope to go back to Vamizi sometime soon and do a more thorough assessment of the crabs’ population. And if I ever perish somewhere near to where these gorgeous animals live, I hope that they find me.

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The underside of a blue coconut crab.

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The edge of the underside of a coconut crab’s thorax looks very reptilian.


Filed under: Crustaceans, Invertebrates, Macrophotography, Mozambique

Travels in the Meddle Earth

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Tuatara (Sphenodon punctatus)

“Go!” is the last word I hear, and then it’s only the swish of air, panic in my heart, and the river getting closer with every nanosecond. Right at the moment I am ready to have my skull crushed, something pulls me up, and I am flying towards the top of the canyon again. Ah, bungee jumping, the sport of the brave and the insane. But this is New Zealand, home of crazy adrenaline addicts who first inflicted this exercise on the world, and I would have never forgiven myself if I did not make myself try it. “Yeah, it was all right,” I say nonchalantly when back on the bridge, hands deep in my pockets to hide the shakes (from the cold, I think.) Then I get into the car, and drive away without looking back.

Two things had always attracted me to New Zealand. One was bungee jumping, which I had always seen as a sort of a dry run for a suicide. The other was a burning desire to see a beast that I had first read about when still a young boy. Tuatara, a unique reptile whose pedigree goes back over 230 million years, is the only surviving member of the reptilian order Sphenodontia, now found only in New Zealand. In books and articles that I read about the tuatara it was portrayed as the closest thing to a living dinosaur the human race would ever have a chance to see. Even its very name sounded mesmerizing – tuatara, a Maori word for “spiny back” – and I envisioned a gargantuan monster, perhaps a real life dragon.

But it quickly becomes apparent to anybody interested in tuataras that the appeal of these remarkable reptiles lies not in their rather underwhelming physique (although I strongly disagree with the assessment presented by an Auckland newspaper in the late 1870’s, which called them “…the ugliest of all creeping things, with the exception of frogs.”) At first glance a tuatara can be confused with a large, thick-legged lizard. Not surprisingly, the first tuatara, in the form of a single skull sent from New Zealand to the College of Surgeons in London, was formally described in 1831 as such. Its descriptor, John Edward Grey, then an assistant in the British Museum’s reptile collection, coined the name Sphenodon, and placed it, incorrectly, as it later turned out, among the lizards of the family Agamidae. Eleven years later, not realizing that he was looking at the same, but far more complete animal, Grey described another New Zealand “lizard,” Hatteria punctata, based on a tuatara preserved in alcohol (the name he later changed to the now accepted, and “less barbarous,” Sphenodon punctatus). But it was the paleontologist Sir Richard Owen, the man who famously coined the term “dinosaur,” who first noticed a strong similarity of the New Zealand “lizard” to certain Mesozoic reptiles excavated in South Africa. His suspicion of the ancient origin of the tuatara, published by Albert Günther 150 years ago this month, was later confirmed by other zoologists, who placed the species and its fossil relatives in a separate order of reptiles. At the end of his life, after it became clear that tuatara was not a lizard, but rather a unique animal close to extinct Mesozoic reptiles Grey published a self exculpatory paper, explaining that he did notice its unusual features, but “[…] it would have required more than usual hardihood in 1831, when the genus was described, to venture to form for it even a family; while an order may now be suggested for the single genus, with every probability of it being adopted – a decided proof of the progress of science in a few years.” While Grey’s definition of the progress of science may sound antiquated, he was right predicting the fact that nobody now questions the singular status of the tuatara amongst modern reptiles.

A portrait of a tuatara.

Superficially, a modern tuatara’s 40-70 cm long body resembles a chunky iguana, with soft, grey or sometimes greenish skin covered with small, non-overlapping scales. A low crest runs along its back, eventually turning into stout, conical pegs on the thick, muscular tail. The head is also covered with small scales, but unlike lizards, tuataras do not have external ear openings, or even functional tympanic membranes. Nonetheless they can hear surprisingly well, albeit their sound perception is restricted to low frequencies, such as the low, grumbling noises these animals produce when distressed. Incidentally, their ability to hear only low frequencies makes them strangely intrigued by human voices, which also span the lower registers of the sound spectrum. The strongest indication of tuatara’s ancient provenance lies in the structure of their skull, which still bears two pairs of large openings connected by strong, bony arches, features that have long been lost in all modern reptiles. The upper jaw is fully fused with the rest of the skull, making it inflexible, and severely limiting the speed with which tuataras can open their mouth, and how wide they can do it. Rather than snatching things directly with their jaws tuataras must rely on their thick, sticky tongue to catch their prey, a lingual ingestion is the technical term for this behavior, and ingest they do. Tuataras are known to eat pretty much anything they can catch, and this includes beetles, crickets, earthworms, lizards, other tuataras, and even birds. Once in tuatara’s mouth, the prey is quickly cut into pieces by the shearing action of a single row of teeth on the lower jaw against two rows of teeth at the base of the upper one. And while tuataras’ disposition is rather docile, if sufficiently annoyed they will bite, and the sensation this produces has been repeatedly described as similar to being gripped by a powerful vise, which will only tighten its clasp if one attempts to dislodge it.

The strongest indication of tuatara’s ancient provenance lies in the structure of their skull, which still bears two pairs of large openings connected by strong, bony arches, features that have long been lost in all modern reptiles (with the exception of turtles, whose ancestors never had those openings to begin with.)

Like so many still surviving relict lineages of organisms, tuataras relish the cold. They are, like all reptiles, ectothermic. This means that their body temperature is dependent on the ambient temperature of the environment, and while they can regulate the amount of energy that reaches their body through basking or hiding in the shade, they cannot generate their own heat. Unlike most reptiles who prefer warm or truly hot weather, tuataras optimal body temperature is 16-21°C, the lowest of any reptile, and they remain active even when the temperature drops to decidedly nippy 7°C. Although this adaptation to the cool, temperate climate of the present day New Zealand is probably a relatively recent phenomenon, it allowed tuataras to outlive all their Mesozoic relatives from other parts of the globe, and withstand the competition from lizards they have been sharing New Zealand with since its separation from the old supercontinent Gondwana.

But the more I was learning about tuataras, the more obvious it was becoming that my chances of seeing one in its natural habitat were slim to none. Although recent conservation assessments of tuataras sounded optimistic, the overall picture was far from rosy. The numbers of surviving individuals were impressive, and between 30 and 50 thousand individuals are said to live in New Zealand. Unfortunately, most of them are concentrated on the small, offshore Stephens Island. Thirty-four additional tiny islands have tightly monitored populations that vary in size from a few to a few hundred individuals, but the mainland New Zealand has not seen free-living tuataras since the arrival of the Maori ancestors and their accompanying menagerie of dogs, rats, and pigs, which quickly did away with the slow, tasty reptiles and their eggs (not to mention the many now extinct native bird species.) By the time the English came in the late 1700’s, tuatara, or ngarara as it was also called, was considered on the mainland an almost mythical creature, remembered only by the oldest of the Maori, and even by them only as something that their grandfathers hunted (and, apparently, really feared.) Luckily, some of the animals survived on a few small islands in the Bay of Plenty and the Cook Strait where rats and other introduced species never managed to get to. Only within the last twenty years, following massive rat eradication efforts and great advances in captive rearing of tuataras, the downward trend has been reversed, and new populations have been reintroduced to several additional islands.  On the mainland, however, tuataras seem to be a lost cause. And yet, some people just refuse to give up.

On the outskirts of the capitol Wellington, on the southernmost tip of the North Island lies a valley called Karori. Until the mid-1800’s its entire area was covered with nearly pristine, primeval woods, but after the arrival of English settlers most of the forest was cut down or burned and, following the construction of two dams, a lake appeared at the bottom of the valley. But about twenty years ago, after both dams were finally decommissioned, and nobody really knew what to do next with the place, a group of conservationists came up with an audacious plan to turn Karori into a sanctuary, to recreate a piece of a piece of the old fragment of Gondwanaland known as Zealandia, and return to it its rightful, native inhabitants, including the tuatara. The problem was, that like nearly all of the country, Karori was overrun with invasive plants, and introduced mammals and birds thrived there in place of the indigenous fauna. At least 30 mammal, 34 birds, over 2,000 invertebrates, and 2,200 alien plant species are fully naturalized in New Zealand; in fact, the number of exotic, invasive seed plant species now exceeds that of the native ones. And although only a portion of the New Zealand’s aliens lived in Karori, their dominance over the natives was overwhelming.

The most serious predicament the Karori project faced was the alien mammals. By a strange bit of luck, the landmass that broke off the eastern part of Gondwana in the late Cretaceous about 80 million years ago to later become New Zealand just happened not to invite any land mammals for its oceanic voyage. The only furry, native inhabitants of New Zealand were a handful of bat and seal species. This left many potential ecological niches vacant, niches that were promptly filled by other, rather unexpected groups. Birds took upon themselves to become giant grazers (the now extinct moa), sprightly, flightless insectivores (the now mostly extinct wrens), or nocturnal, scent-guided predators of soft-bodied invertebrates (the now highly endangered kiwis.) In the absence of wily mammalian predators many lineages of birds forwent flight, as there no longer existed a pressure to quickly take up to the air to escape. The role of mice and other rodents was filled by seed-feeding, cricket-like wetas, and since few birds were interested in these insects, they grew huge and sluggish. And so, when the mammalian invasion began, probably as early as 2,000 years ago with the arrival of the first Polynesian sailors, this vulnerable, insular fauna did not stand a chance. The first to go were flightless moas, massive birds nearly twice the size of present-day ostriches – they fell victim to the worst mammalian offender, man. With the first human settlers came other mammals, most notably pigs, dogs, and the Pacific rat (Rattus exulans). The last one was of course brought in accidentally, but that did not diminish the bloodshed this species has caused. Rats are probably the main cause of the extinction of a number of birds, a severe decline in the populations of wetas, and wiping out tuataras on the mainland. Not to be outdone by the natives, the early English settlers rolled up their sleeves and went about turning this singular, exotic land into a South Pacific version of their northern homeland. Deer and foxes were introduced for their hunting pleasure, followed by hedgehogs, cats, and a number of other furry species. Rats and mice brought by both the Maori and Europeans flourished and wreaked havoc among planted crops in the lack of competition of any kind, which finally attracted the attention of the colonists. In one of the most disastrous decisions in New Zealand’s history, stoats, a kind of a weasel, were brought in from Europe to control the outbreaks. But why should stoats bother trying to catch fast and elusive rodents, which over millions of years of coevolution with mammalian predators had developed great skills at avoiding being eaten, when the islands were full of naïve, slow or flightless birds and their tasty eggs? Unsurprisingly, an avian carnage ensued.

It soon became obvious that the only way to keep invasive mammals out of Karori was to surround it with an impenetrable fence, and then eliminate all the invaders inside the fence with a combination of traps and poisons. At the cost of slightly over 2 million NZ$ (approx 1.5 mln US$) a tall, metal mesh fence was erected around an area of about 1 square mile, capped with a wide, slippery metal ledge, impassable to all mammals. Or at least that was the idea – accidental damage to the mesh, designed to be fine enough to prevent even baby mice to slip through, allowed some mice to re-enter the reserve, and establish a population that still seems to be thriving. There was not much that could be done about invasive bird species – even if all alien birds were exterminated in Karori, new ones would simply fly in from surrounding areas – and getting rid off invasive plants turned out to be easier said than done. But, in the end, a remarkable progress has been made in replacing some alien plants with native vegetation, and a number of indigenous bird species as well as 200 tuataras were released in Karori. I decided that if I were ever to see one of these animals living free in something akin to a natural habitat, this was the place.

A big, beautiful wall — and nobody builds walls better than NZ, believe me — but still some rodents were able to get through and are now present in Karori. Seems that walls rarely solve anything.

I took a walk to Karori from downtown Wellington on a cold and windy October morning, and was met by a friendly volunteer who gave me a quick introduction to the history and the layout of the sanctuary. The place was undeniably impressive, although my introduction was constantly being interrupted by mallard ducks begging us for food. As we strolled along a wall of tall, imposing pine trees, I tried to spot a plant, any plant, that was not an introduced alien (“No, not that bush,” “No, not this either,” “No, that’s European Plantain,” “But look, here is native flax!”) We flushed a group of California quails, and a few European blackbirds flew over our heads as we approached the tuataras’ inner sanctum, a smaller area surrounded by another fence, which keeps out wekas – native, flightless birds known to attack and eat the reptiles. Behind it, to my surprise, was yet another, shorter fence. Its purpose was to separate a part of the Karori tuatara population (60 individuals) from mice that roamed its terrain. The terms “free-living” and “natural” were quickly becoming more and more relative. Unfortunately, by the time I reached the enclosure freezing rain was pouring and, understandably, no sane tuatara would stick its head out of the burrow in such weather. In the days that followed I visited the sanctuary every day, but the capricious Wellington spring kept tuataras underground. Only after a week, when I stopped there for the last time on my way to the airport, was I greeted with beautiful sunshine, and several tuataras basking in front of their dens.

But for the time being I had no choice but to move to the plan B, and visit Victoria University in Wellington, which maintains a small colony of the ancient reptiles. One of New Zealand’s most knowledgeable tuatara specialists is Dr. Nicky Nelson who for many years has lead the efforts in their conservation, and made some remarkable discoveries about their reproduction and sex determination. We met at the university cafeteria, a place with a stunning view of the Wellington harbor and the Matiu Island, which has a small population of repatriated tuataras. I had originally planned to visit the island as well, but became too entangled in bureaucratic red tape to make it worthwhile. Nicky filled me in on some of the latest research, including a genetic study that unequivocally demonstrated that all tuataras are members of one species, rather than two, Sphenodon punctatus and S. guntheri, as dictated by the traditionally accepted taxonomy. The latter, thought to be restricted in its original distribution to the miniscule Brothers Island in the Cook Strait, appears to be nothing more than a somewhat stunted by limited food availability, and marginally differentiated by genetic drift form of the widely distributed species.

This young, captive-raised tuatara hatchling will soon be released to augment one of the tightly controlled wild populations. There, it will lead a mostly diurnal life, trying to avoid being devoured by the nocturnal adults. It will take thirteen to twenty years before this individual is ready to reproduce.

After a chat and a cup of coffee I was finally standing in front of a large, glass-walled pen that held the animals. Each pane of glass was connected to a sensitive security system, and the door to the enclosure had two massive locks. None of it surprised me, of course, considering the US$20-30,000 asking price for a single tuatara on the black market of exotic pets. Nicky climbed inside and quickly located Spike, a 22 year old male, a captive-raised youngster (tuataras easily live to be a hundred, although reports of a 300 year old individual could not be substantiated.) He was a gorgeous specimen, and I really wanted to spend more time photographing him, preferably in a setting other than an enclosure inside a building. We agreed for Spike to meet me (with a couple of handlers) the next day in the cemetery adjacent to the university, where some semi-natural vegetation could be found. I found the arrangement somewhat peculiar, but at the same time strangely symbolic. As I stood on the following day among the graves of early Wellington settlers, watching the native New Zealander basking himself in the specks of early spring sun among seedlings of American maples and clumps of African grasses, his two caretakers vigilant over his every move, I could not help but feel extremely pessimistic about the fate of this island’s biodiversity. Tuatara, this magnificent animal, a Mesozoic relic if there ever was one, survives only thanks to the complete devotion of people like Nicky Nelson, surrounded by one of the greatest biodiversity disasters in the history of the human conquest of Nature. If left to its own devices, the entire population of these reptiles would probably disappear within a few decades, devoured by rats or pigs, or simply driven to extinction by their vanishing natural habitats. To add insult to injury, since sex in tuataras is not determined genetically as in it is in mammals or birds, but by the temperature in which their eggs develop, climate change can potentially accelerate their decline (if the temperature of incubation exceeds 21°C all hatchlings will be male.) Recent climatic models developed for the North Brother Island tuatara population suggest that by 2085 no females will be able to develop, thus spelling the end to that group of animals.

To help keep track of the movement of individual tuataras, each animal of the first batch of 70 released in Karori is marked with a unique combination of small color beads. Depending on the size of the animal, they may carry between 2 and 6 beads attached to their crest at the base of the head. Although the presence of beads somehow spoils the illusion of the animal being “wild,” a traditional alternative would have been to clip a toe or a combination of toes—a far more painful and risky procedure.

Other than apocalyptic annihilation of all life on Earth following an international spat about whether God’s word should be read from left to right or the other way around, one of the most frightening possible future scenarios for our planet is the arrival of a period that some scientists chose to call the Homogenocene – the Age of Uniformity. What they envision is a time when, thanks to voluntary and involuntary transfer and exchange of organisms between nearly all possible points of the globe, a feat well nigh impossible a thousand years ago but now trifling, all continents and smaller geographic regions will lose their biological identity. Nearly indistinguishable, relatively small suites of species will be present across climatically and physically similar areas, whereas the original, local ecosystems and associated, endemic and native species of those environments will be gone, replaced by more resilient, unfairly advantaged alien invaders (or invitees.) Regrettably, as tragically exemplified by New Zealand, it seems that the dawn of this new age is already on the horizon. Global commerce, tourism, migration, biological control, and plain, human stupidity have already done a splendid job of mixing things up, shuffling organisms from one continent to the next, opening the gates for barbarians to slaughter the unsuspecting natives. Virtually any place on Earth where humans have ever set foot is left with the trail of our inseparable biological satellites – rats, houseflies, clover – the list is thousands of species long. Each of them is likely to displace some local equivalent or, if there is none, carve for itself a deep and permanent niche in the new environment, and never without harming the existing balance of things. None rivals our own species in its thirst for destruction, but there are a few impressively accomplished contenders. Mice and rats now feel at home anywhere from Polar research stations to equatorial villages, and the list of local species they have extinguished may be even longer than that of species that humans speared and clubbed to extinction (there exists poor record of plant species we have picked or trampled to death, but there are some known cases.) Japanese beetles, Argentine fire ants, European earwigs, German yellow jackets, American cockroaches, Canadian waterweed, their names tellingly prefaced with the (presumed) point of origin, are wrecking havoc in places they would have never gotten to if it wasn’t for the convenience of ships and planes. But while these stowaways arrived to where they are now without our expressed consent, most invasive species that now reign supreme were lovingly carried across the oceans, nurtured and cared for upon the arrival, and let loose with a blessing (or at least their cages had locks that needed some work.) Goats, foxes, cats, pigs, horses, sparrows, starlings, pigeons, oaks, pines, ivy, kudzu, prickly pear, eucalypts, aloes, carp, trout, honey bees, bullfrogs, cane toads, the list goes on and on, are all united in their status as legal, consciously invited immigrants in places where they should have never gone to. In many cases the decision to bring in the alien species was well intentioned, but in the end nearly always with devastating consequences to the local ecosystems. Alien species, if introduced into an area that matches the physical aspects of their home turf, instantly gain the upper hand over the natives by the simple fact that they left behind an army of predators, parasites, and diseases that over thousands or millions of years had evolved along their side, and kept their populations in check. In the new place all these restraints are suddenly gone. The locals, however, still need to deal with their nemeses, but now these limiting factors are combined with the competition from the new arrivals. Not surprisingly, it often takes only one or two generations before local species are completely overwhelmed by the aliens, and either undergo a dramatic decline, or disappear completely.

The New Zealand Department of Conservation is doing a truly splendid job working on the restoration of natural habitats around the country, and nearly a third of its surface is at least partially protected. But it may take a long time to reverse the effects of the horrible devastation caused by the original settlers’ idea to convert New Zealand into a South Pacific version of England. Thousands of square miles have been turned in “green deserts,” where no native plants or animals are able to survive.

New Zealand, because of its geological and biogeographic history, exhibits a notable absence of many taxonomic and functional groups that dominate other lands (snakes, woodpeckers, mammals, to name just a few.) Alien species fill those gaps, and in the process profoundly alter the natural ecosystems. For example, New Zealand had no animals that specialized in stealing bird eggs or chicks. Brushtail possums, introduced to New Zealand 150 years ago to establish fur trade, and now roaming in numbers in excess of 60 million of free living animals, have become major bird nest predators, although in their native Australia they feed mostly on flowers and other plant material. The saturation with non-native organisms is now so complete that, according to a recent, comprehensive review of New Zealand invasive species, even a small patch of seemingly unmodified, native forest in the most remote corner of the country has on average 6 alien mammal herbivores, 5 alien mammal predators, 2 alien fish, numerous alien plants, and an unknown number of alien invertebrates, fungi and bacteria species.

It is painfully obvious that our understanding of the complexities and multilayered organismal co-dependencies within even the simplest of ecosystems is not comprehensive enough to predict the outcome of the introduction of even a single, foreign species to the mix. One would think that New Zealanders have learnt their lesson, and no more alien species will ever be willingly introduced. I was therefore positively shocked to learn that at Karori sanctuary, the very place that epitomizes the most heartfelt attempt to reverse the effects of human meddling with nature, an Australian, non-native plant known as Banksia integrifolia is purposefully introduced to the reserve in an effort to increase the availability of nectar to local birds. To add to the mystery, this particular species is one of the few banksias that do not require fire to disperse and germinate their seeds, which makes it a more likely candidate to escape from Karori and establish itself elsewhere. “Mistakes have been made,” the keepers of Karori seem to be saying, “but now we know what we are doing,” and let’s hope that they are right. Returning Karori to its former, pre-human glory is going to be a long process, estimated to take at least 500 years if everything goes as planned. It is a daring experiment, not unlike trying to keep an iceberg frozen in the middle of a scorching desert, one that will require constant care, significant financial resources, and an army of devotees. And this is for an area of about 1 square mile, or less than 0.001% of New Zealand’s surface.

To protect the country from additional invasions, the New Zealand government has created MAF Biosecurity, one of the most sophisticated and effective biological quarantine systems in the world. It screens all goods and passengers arriving in New Zealand, and every day uncovers about 240 cases of high risk items (potential weed plants, contaminated food etc.) being brought by people into the country. Unfortunately, for much of the islands’ biodiversity this noble effort came too late – 42% of native New Zealand birds are now extinct, as are numerous amphibians, reptiles, fish, insects, and an unknown number of other invertebrates and many plant species. The survival of the remaining native organisms hinges on the effectiveness of the quarantine and conservation as well as the good will of people who devote their lives to saving the remains of the old Zealandia, and it was only thanks to them that I was finally able to meet the tuatara. But with Homogenocene already at the door of this otherwise beautiful island country, the world’s attention should probably focus on other places that may soon be met with a similar fate. Other Pacific islands, New Guinea, Fiji, Solomon Islands, should become the targets of the most stringent quarantine efforts; it is not too late for them to save most of their native fauna and flora from the impact of alien species. And yet, if history has taught us anything, it is that we don’t need no stinkin’ history to teach us anything, thank you very much, and New Zealand’s mistakes will be promptly repeated in all those places. I really hope that I am wrong.

In 2005 the Karori Sanctuary near Wellington became the first site on the mainland New Zealand to see free-living tuataras in over 300 years. Seventy individuals, translocated from the Stephens Island in the Cook Strait were released, 60 of which were placed behind an additional enclosure that protected them from mice that unfortunately still roam in Karori. But as it turned out, animals outside the fence actually did better than the ones inside, and gained significantly more weight. A subsequent batch of 130 individuals was released two years later outside the mice-proof fence (but still inside a very large enclosure that protects them from wekas, flightless, predatory birds that like to eat the reptiles.) After five years the survival rate of the released animals was 33%, which may seem low, but these cryptic animals are notoriously difficult to spot, and the actual survival rate is almost certainly much higher (within the smaller, mice-proof area the survival rate was 89%.) But the ultimate proof that the translocation was a success came from the discovery of clutches of viable eggs and, in March 2009, the first born-free hatching.


Filed under: Conservation, Reptiles

Mozambique Diary: Demons in the dust

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Translucent and motionless, the Gregarious antlions (Hagenomyia tristis) are virtually invisible as they form large aggregations, often a few hundred strong, in the grassy understory of Mozambican miombo woodlands.

When the fuel line under a car breaks and starts spewing a highly flammable liquid, the chances of something good coming out of such a situation are usually slim. And so I was not looking forward to having to crawl under my Landcruiser to try to fix the leak after the car had stalled again. I got out and after a few minutes of fiddling I was able to reattach the fuel line well enough for the engine to start. Wiping diesel off my arms and face I took a quick glance around, and what I saw made this unfortunate stop almost entirely worthwhile. At first I wasn’t quite sure what I was looking at – a diaphanous grey cloud seemed to have landed among the tall grass, shimmering ever so slightly, not allowing my eyes to pick out any discernible elements that constituted this strange apparition. I moved in closer and the cloud lifted, slowly and in complete silence, revealing itself to be composed of hundreds and hundreds of large, nearly translucent insects. Hagenomyia tristis, the Gregarious antlions!

Hagenomyia_tristis_1
When disturbed, the entire aggregation of antlions lifts off slowly and in complete silence. Unlike swarms of locusts or bees, which make quite a noise when they fly, the soft wings of antlions, fringed with very fine hair-like setae, a thousand flying antlions make almost no discernible sound.

I was traveling last week with a few companions across Coutada 12, a former hunting concession in central Mozambique. This area, no longer in use for hunting, will hopefully soon become a part of Gorongosa National Park, nearly doubling its size and, if all goes well, in a not too distant future will allow herds of buffalo and elephants to once again trek from the shores of the Indian Ocean to the slopes of Mt. Gorongosa. Our small party was there to scout for potential campsites for an upcoming biodiversity survey. The car problem was just part of the process, as annoying and almost as inevitable as the constant barrage of tse-tse flies that tested the limits of how much cursing is too much, even among friends.

Finding the Gregarious antlions was for me the highlight of our short trip. Not particularly rare and often congregating in huge numbers, these insects are nonetheless difficult to spot, and I had seen them only once before. Their wings are just the right shade of grey to make them disappear in the sun-dappled vegetation, and they lack the lustrous sheen that makes the wings of other antlions stand out in the sunlight. A bright spot on the wing draws your eye away from the body of the insect and makes it even more unlikely that a predator will recognize it as something good to eat. These are the only antlions that do not lead a solitary lifestyle that is typical of all other members of the family Myrmeleontidae.

Gregarious antlions (Hagenomyia tristis) carry bright, conspicuous spots on their wings that draw the attention of a potential predator away from the body of the insect and make it even more unnoticeable.

Why do they congregate in such large groups? The answer is likely the same as to the question of why birds flock and fish shoal – these insects are good statisticians. Simply put, the chances of any individual antlion being picked out by a predator are significantly lower in a dense group than if the same individuals were widely scattered. A more interesting question is, why don’t all antlions do the same? It appears that despite the lower risk of being eaten, living in a large group also lowers the chances of finding food for yourself as you must compete with all your shoulder-to-shoulder companions. This is particularly true for predators, such as these antlions that feed on small flying insects, since their food is unlikely to present itself in one huge cluster. For this reason herding behavior is seen more frequently in herbivores, especially those that feed on plants that cover extensive areas.

But there is at least one other antlion who wishes to be gregarious. Banyutus lethalis is a species remarkably similar to H. tristis in its appearance and living in the same habitat of African miombo woodland. And yet it never forms its own aggregations. Rather, individuals of B. lethalis sneak in among the masses of H. tristis, taking advantage of the protection bestowed by the herd, but probably not suffering the cost of the competition for food with other group members (it is likely that the two species hunt for different prey.) Another difference between these two species is in their larval behavior – while the larvae of H. tristis form the iconic funnel-shaped pits in the sand, those of B. lethalis simply wait for their victims while camouflaged under a thin layer of dust.

Banyutus lethalis is a solitary antlion that frequently sneaks in among the aggregations of H. tristis to benefit from the protection bestowed by the herd. Their appearance is nearly identical to that of their hosts. Like most antlions, their eggs are laid in sand and the larvae develop there, hunting small insect. This species does not build the funnel-shaped pitfalls that antlions are famous for.

Antlions, a fascinating group of insect christened “demons in the dust” by the entomologist William M. Wheeler, are still relatively poorly studied worldwide and virtually untouched in Mozambique. Southern Africa has a particularly rich fauna, with nearly 200 species, or 10% of the world’s antlion known species. In Gorongosa NP we have so far recorded about 20 of them, which means that there is still a lot of work ahead of us before we find them all. Leaky fuel lines and tse-tse flies be damned.

Gorongosa has a rich fauna of neuropteroid insects, including over 20 species of antlions.

Gladiator spiders

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In June 2006 I was in Ghana with a group of conservation biologists to gather data and arguments for the creation of a new national park around the spectacular and highly threatened Atewa Forest Reserve, a lofty goal that, alas, has still not been reached. Sweeping my insect net through the lush vegetation, I knocked down from an epiphyte-covered branch a strange, green spider. It had a fat, flattened body that resembled a piece of moss. Looking closer, I noticed its huge, forward-facing eyes and realized that it must be a net-casting spider, a member of the family Deinopidae, but one that did not resemble any of the species that I was used to seeing in the rainforests of Central and South America. Later that day I found another individual of the same species, this one holding its gladiator net, which confirmed my initial suspicion. It turned out to be Asianopis guineensis, a species known only from its holotype described in 1940.

I had since forgotten about this brief encounter but recently I ran across an interesting paper describing the behavior used by the net-casting spiders to catch flying insects, which made me think of it again. Net-casting spider, known also as gladiator or ogre-faced spiders, stand out among their silk-spinning kin thanks to an unusual way of catching prey. While most net-making spiders employ a passive, sit-and-wait hunting strategy, deinopids use a small “hand-held” net to actively capture their victims by casting it over them with a remarkable speed. The net is made of tightly packed, non-sticky silk that can be stretched many times over without breaking. Its densely coiled, thin strands work like a very fine, flexible mist-net that bird and bat biologists use to capture their animals. Each tiny loop catches on the spines and protuberances on the victim’s body, enveloping and immobilizing it, allowing the spider to deliver its kiss of death and further wrap it in a layer of silk. 

To detect their prey deinoipids use two separate senses. Their huge eyes provide them with an unparalleled ability to see at night. The light-gathering ability of deinopid eyes is an astounding f/0.58. If you ever used a camera then you know that the “f” number, or the aperture of a lens typically starts at around f/3 and goes up to over f/20 – the lower the number, the greater the ability to gather light. Man-made lenses have high f numbers, which is why we need flashes, tripods, reflectors, and other implements to help the camera gather enough light to create a well-exposed picture. The human eye, with the iris that adjusts its diameter to adapt to different levels of light, spans the range of f/2.1 to f/8.3. The difference between the spider’s f/0.58 and a human’s f/2.1 seems deceptively small but it means that the deinopids’ sensitivity to light is 2,000 times greater than that of the human eye, and hundreds of times greater than that of a cat (f/0.9) or an owl (f/1.1). 

To achieve such an incredible sensitivity, which allows them to spot small insects in pitch black darkness, deinopids have evolved a unique eye structure that disintegrates every day, only to rebuild itself at night. Each of the spider’s big front eyes (technically, posterior-median eyes that moved to the frontal position) has six special light-sensitive structures called rhabdoms, connected with a membrane. The volume of that membrane dictates how much light an eye can gather. At night the membrane is rapidly synthesized, dramatically increasing the light sensitivity of the eye but when the day comes the membrane dissolves, leaving only enough for basic vision.  But why? Wouldn’t it be great to have super vision 24/7?

Several hypotheses have been proposed to explain this phenomenon and the most plausible one is that such an ultra-sensitive membrane ages very quickly, leading to a progressive loss of its sensitivity. It thus makes more sense to reabsorb it when it is not needed and synthesize it anew when it is.

The insects that deinopids catch are quite large compared to the spider’s body and one would think that a single cricket of nearly equal weight would be enough to satisfy it for the night. But no, as soon as the prey is captured the spider begins to eat it, while at the same time setting up its net for another strike. It is possible that the spider’s voracious appetite is driven by the energy-hungry physiology of its eyes, which might have caused some net-casting spiders (the genus Menneus) to forgo the fabulous night vision and reduce their eye size in a process known as regressive evolution.

Remarkably, net-casting spiders can catch insects without ever seeing them or, since spiders have no ears, hearing them. If a flying insect makes a mistake of coming too close behind the spider’s back, it will be met with a blindingly swift backwards strike of the net, deployed with the speed of 60 ms. (To use another photographic reference, the shutter-lag of an average camera, which is the time that elapses between you pressing the shutter button and the camera taking a picture, is between 50 to 200 ms. In other words, these spiders are freaking fast.) Experiments have shown that even blinded deinopids can detected flying prey from two meters away, solely by the sound of the beating wings and precisely direct the strike, all without having ears. It is still unclear how these animals detect sound, but it is likely that the structures responsible for it are trichobothria (“hair”) on the legs of the spider that respond to the movement of air molecules caused by sound waves. The tarsus, or the foot of the spider appears to be particularly sensitive to sound.

All of this is very cool but the thing that really impressed me about net-casting spiders is the incredible effort that females put into building the most beautiful protective shield around their eggs. Last year I was standing in front of my house in Costa Rica, listening to the night chorus of insects and frogs when I noticed a female building an egg sac. It was a perfect orb, suspended on a single strand of silk, and the female seemed to be continuously measuring its smoothness and size with her pedipalps, every few seconds applying a few microscopically thin strands of silk to make it even more perfect. I watched her for a while and took a few pictures, hoping to see over the next few days how she would combine her maternal duties with her hunting activity. Alas, the next morning both the spider and her beautiful maternal work of art were gone, and I will never know if she carried it to a safer location or if a bird swallowed both miracles of evolution. ✦

P. S. If you would like to read more about these spiders and see some really excellent photos and videos, visit Gil Wizen’s blog.

Bengalia

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The dilapidated remnants of Chironde, an old hunting camp near the town of Inhamitanga in Mozambique, don’t make for a particularly enticing location for visitors and most of the year the camp sits empty, looked after by a lone guard whose most exciting part of the day used to be cooking a pot of rice under a leaky roof of a small outdoor kitchen. But after years of neglect the roof collapsed entirely, and the guard had to find another place. The now abandoned structure was quickly colonized by various organisms, including a large colony of carpenter ants (Camponotus importunus), who found the cracked concrete floor of the kitchen absolutely perfect for building an extensive colony. 

I have been coming to Chironde frequently over the years with researchers and students since the surrounding pristine miombo woodland provides a fantastic environment for biological exploration and a couple of weeks ago I went there again with two visiting scientists. During the night it started to rain, and the water must have seeped into the underground ant colony because the following morning we were met with a sight of hundreds of ants frantically pulling their larvae and pupae to the surface in an apparent attempt to dry them. As we watched the ants, suddenly a few large flies appeared and started wresting with the ants over their precious cargo. Although the ants were quite large, in almost all cases the flies managed to overpower them and fly away with the larva or pupa in their grabby legs. The flies would land a few meters away and start sucking the content of their prey, within minutes leaving nothing but a shriveled shell. I recognized them instantly as members of the Old World genus Bengalia (Calliphoridae: Bengalinae), aptly known as highwayman flies.

A short video of Benagalia stealing ant brood that I filmed in Chironde, Mozambique.

It wasn’t my first encounter with highwayman flies. A few years earlier I was looking for inquilines of termites, animals that share their underground living spaces, and broke off a small section of the termite mound, exposing a group of pale and soft workers to the light. Within seconds highwayman flies showed up out of nowhere and started kidnapping the confused creatures. The flies would alight on a bush a few meters away, suck the poor termite dry, and come for more. At that time I had no idea of Bengalia’s existence and so I took a few photos and started searching entomological literature, looking for clues. It didn’t take me long to identify the flies but was quite surprised to discover how little was known about their biology, despite multiple studies on the flies’ taxonomy. In fact, most of what I found were old, anecdotal observations from SE Asia of the flies hunting termites or stealing larvae and pupae of ants, although recently a study in China shed additional light on the interactions between highwayman flies and ants.

Highwayman flies truly behave like their human namesakes. They target travelers, either termites marching towards their food source or ants carrying their brood or food from one place to another. On rare occasions they depart from their kleptoparasitic tendencies and attack small solitary creatures, such as nymphs of blattodeans, but they really prefer to rob or hunt social insects. It is not clear how highwayman flies locate ants carrying their brood or exposed termite workers but it is likely that they use a combination of vision and scent. There is some indication that they are attracted to the smell of fungal gardens grown underground by termites, a smell that usually indicates a damage to the mound and the possibility of exposed workers.

A peculiar aspect of the flies’ behavior is that they truly prefer to steal rather than earn an honest living. If offered the exact same prey item but without the ants present, an ant larva or pupa lying alone, they will simply ignore it. But the moment an ant picks it up, then the game is on. It’s almost as if they were unable to make their own judgement as to what is worth taking without someone telling them. They will even steal breadcrumbs from ants, something that they probably would never consider eating, if they see the insects carrying them. 

The development of Bengalia is nearly completely unknown. A larva of this fly (hatched from an egg laid under laboratory conditions) was described for the first time in 2016 and there is a single observation of a female lying eggs in the soil near an incipient colony of termites. Larvae of a closely related genus Verticia (Bengalinae) are parasitoids of termites, developing inside the head of termite soldiers, over time filling it completely, and eventually leaving the host by crawling through its neck, thorax, and abdomen, only to emerge at the posterior end (while the host is still alive). It is therefore quite likely that Bengalia larvae do something equally horrendous to termites. On a few occasions I found what looked like fly larvae in the termite colonies. I am now tempted to look for them again and attempt to rear them in hope of unraveling the mystery of Bengalia’s development. If I have any luck, you will be the first to know.


Silently speaking

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Crickets are some of the oldest and best studied singers of the animal world. Their ancestors were probably some of the first animals to break the silence of the dry land in the Permian and the Triassic (acoustic communication underwater had probably appeared long before that, albeit fossil evidence for that is scant.) The ubiquity of cricket calls is so pervasive that even people who live in colder climates where crickets are rare will immediately recognize the sound. Their calls are so ingrained into the human psyche that it is difficult to image a nocturnal soundscape without at least one species contributing to the ambience. The sound of the call is produced in the typical orthopteran fashion, by using one part of the body to rub against another (in this case, the underside of the right front wing against the top of the left one), a mechanism known as stridulation.

There are many advantages of using sound for communication. Unlike the size and color of sexually-selected ornaments (e.g., the claw used by fiddler crabs to attract females), which usually give a good indication of the male’s fitness but do not require a tremendous expenditure of energy, sound is considered an “honest signal” – females judge the males by both the loudness and duration of the call, and those cannot be easily faked. Sound is directional, which allows the recipient to locate the sender, which means that a female bird can quickly find a singing male by simply following the soundwaves. Sound also allows animals to draw boundaries, and a lone lion will know not to stray too close to a certain part of the savanna because another pride is already roaring there. The ability to communicate acoustically is a superpower that allows animals to send complex messages over long distances, without the need to be visible to the recipient. This is particularly important in settings where visibility is low, such as within a dense forest, at night, or in caves. 

Yet, there are drawbacks to acoustic communication. If a female can hear your call from afar, so can predators, and a high number of crickets have turned their evolutionary trajectory towards silence. Geckos, bats, even cats are known to eavesdrop on calling crickets to pinpoint and hunt them. The selective pressure of the parasitoid fly Ormia ochracea, which uses the call of singing males to locate and drop its deadly larvae on them has lead the cricket Teleogryllus oceanicus to eschew acoustic communication altogether. But in some cases, the reasons for the loss of the ability to produce sound are less clear.

Crickets of the genus Phaeophilacris are large, spindly-legged creatures, found deep in the caves across Africa. In Mozambique, I often see them on the walls of caves occupied by large bat colonies, whose droppings and carcasses provide an ample and steady supply of food for the insects. Unlike other members of the large cricket family Phalangopside, Phaeophilacris have no hearing organs (tympanum) on their front tibia and the males lack stridulatory organs on their wings. This seems odd, since the darkness of the cave should make sound the ideal medium for communication and finding each other. But perhaps millions of years of coexistence with bats, animals known to target singing insects, exerted enough selective pressure to eliminate the risk of being overheard by the winged predators by removing the sound-producing organs and, consequently, the organs needed to hear it. But then, how do these mute and deaf animals manage to find mating partners in the complete darkness? And even if they find each other, what criteria do they use to decide who is and who isn’t a good one to entangle their genes with? 

Phaeophilacris solved the first problem by overcoming the typically high levels of territoriality and aggression found in most crickets by becoming highly gregarious animals. Colonies of cave crickets often consist of dozens or hundreds of animals, squeezed together into crevices and holes in the walls of the cave. Even when out and about looking for food, their extremely long appendages covered with highly sensitive trichobothria (“hairs”) allow the crickets to be always in touch with other members of the group. In such tight settings, males can easily smell and detect females with their antennae as soon as the time for courtship comes.

How do females decide if a particular male has got what it takes to produce the best offspring? In acoustic species, the volume and duration of the call are good, honest indicators of the male’s fitness, but what if you can no longer sing? Luckily for the males, they still have the wings and they have evolved a way of using them in an ingenious way that provides a good proxy for the quality of their genes. When a male encounters an interested female, he lifts his wings up and holds them vertically and perpendicularly to the body axis. Then, he begins to flick them forward, with each movement sending a single vortex of compressed air towards the female. She cannot hear this, of course, but a series of specialized trichobothria on her cerci, the long appendages at the tip of her abdomen, immediately detect and measure the power of these puffs of air. The vortex travels with the speed of 40 cm/second and is detectable by her from 15 cm away. If she finds them convincing enough, the courtship moves on to the next stage, where the two partners caress each other with the antennae, while the male shakes his body seductively and occasionally touches the female with his legs. Eventually, if properly enticed, the female climbs on his back and the male transfers a small spermatophore into her genital opening, concluding the proceedings.

The silent communication of crickets, which allows them to conduct their love affairs undetected by bats and other predators is pretty neat in its own right but one researcher, inspired by the crickets’ behavior, decided to copy it and design a robot that communicates with other robots using air vortices (Russel, A. 2011. Air vortex ring communication between mobile robots. Robotics and Autonomous Systems 59: 65-73). His robots were able to transmit and receive 466 ASCII characters using nothing but puffs of air. While this may seem stupid to Republican politicians, such biomimicry matters because it opens avenues for the development of efficient communication in places where optical or radio transmission of signals is impossible (in low visibility or underwater, for example), or when other modes of communication can be jammed or intercepted by bad actors.  

Phaeophilacris crickets have been silently talking to each other in African caves for millions of years. Until now, nobody bothered them but recently those environments have found themselves under assault. Rampant habitat loss across the continent threatens the survival of bats, which may spell the end of the troglobitic communities, and the caves themselves are targeted by mining companies looking for limestone and bat guano. Cave crickets are just some of the countless unusual and poorly known cave inhabitants that may give us ideas for new and revolutionary technological solutions. Whether we will have a chance to be inspired by those other species is becoming less and less certain.✦

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