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Almost mammals

A female ball blattodean (Perisphaerus lunatus) from northern Cambodia begins to unfurl to reveal long, powerful legs.

A female ball blattodean (Perisphaerus semilunatus) from northern Cambodia begins to unfurl to reveal long, powerful legs.

I was rummaging one day through the leaf litter on the forest floor in northern Cambodia, looking for insects, when a small, perfectly round ball rolled from a leaf above, bounced off my head, and landed on the ground in front of me. I picked it up to have a closer look, not sure if the object was an animal or a plant. It was about the size of a pea, but black, and very hard. It was an animal, as betrayed by the clearly visible segmentation of its body, but several groups (crustaceans, millipedes, and armadillos, to name a few) use a very similar tactic, and I was not sure which one I was holding (I quickly ruled out armadillos.) After a few seconds a pair of big eyes with two short antennae between them cautiously peeked from a crack that opened on the mysterious sphere. It was a blattodean, but one I had never seen before. Later I identified it as the ball blattodean (Perisphaerus), an interesting animal that experiments revealed to be, thanks to its tight armor, virtually impervious to attacks by ants and other small predators. In fact, the combination of the hard cuticle that forms its exoskeleton with its powerful muscles makes it impossible to unroll the animal without damaging it.

Ball blattodeans of the genus Perisphaerus and several related genera are probably the only organisms other than mammals that exhibit suckling behavior. Young nymphs of these insects have long, almost proboscis-like mouthparts that allow them to access a series of special “mammary” glands on their mother’s underside and suck nutritious fluids.

Ball blattodeans of the genus Perisphaerus and several related genera are probably the only organisms other than mammals that exhibit suckling behavior. Young nymphs of these insects have long, almost proboscis-like mouthparts that allow them to access a series of special “mammary” glands on their mother’s underside and suck nutritious fluids.

Rolling your body into a tight, hard ball is a neat trick, perfected by only a few other insects, but there is something else about Perisphaerus that makes it unique among not only insects, but also almost all other animals. Blattodeans, a large, ancient lineage, represented by nearly 5,000 species, is a truly fascinating example of the evolution of parental care and social behavior. Within insects, where good parenting usually amounts to not eating your young, blattodeans display levels of devotion and parental sophistication otherwise found only in birds and mammals. Dr. Louis M. Roth, the late Harvard entomologist who during his long and productive life uncovered many secrets of blattodean biology, was the first to realize the unusual nature of Perisphaerus. While studying these insects he noticed that females were often accompanied by nymphs clinging to their legs, and some of these youngsters had their heads stuck to the underside of their mother’s body. Careful examination revealed something strange – the mouthparts of the nymphs were very long, almost proboscis-like, a trait unknown in blattodeans, whose mouthparts are of a simple, biting type. Looking carefully at the female Roth also noticed that between the bases of her legs were small, glandular openings, and that’s where the young ones were sticking their heads. Could it be that the mother were actually suckling her young? Up to that point only mammals were known to display this type of behavior, but suddenly it appeared that a similar one might have evolved at least one more time in the history of the animal kingdom. The evidence for this is still largely circumstantial, but what we know about blattodeans certainly supports such a possibility. Many species of these insects give birth to live young, and in a few cases the female feeds them until they are ready to start foraging on their own. In the case of the Pacific blattodean (Diploptera punctata) the female develops an equivalent of the mammalian placenta, and feeds the embryos growing inside her abdomen with a rich mix of proteins, lipids, and carbohydrates. But a female with “mammary glands” and nymphs with sucking mouthparts take the maternal care among blattodeans to a completely new level.

North American forest blattodean (Parcoblatta penssylvanica) carrying an ootheca – a hard, nearly indestructible purse that protects the eggs from predators, parasitoids, and desiccation.

North American forest blattodean (Parcoblatta penssylvanica) carrying an ootheca – a hard, nearly indestructible purse that protects the eggs from predators, parasitoids, and desiccation.

A couple of years after my first encounter with Perisphaerus I found myself, in the middle of the night, following through a bamboo thicket a group of fanatical herpetologists who were intent on catching a particularly elusive, possibly new to science frog. We were in New Britain, a large island that is a part of Papua New Guinea, and I knew that I had a good chance to run across Perisphaerus again. Sure enough, the very moment I heard a triumphant scream that announced the capture of the unfortunate amphibian, I saw the mysterious blattodean scurrying around my feet. And it was a pregnant female. She gave birth to about 10 young a few days later, and during the two weeks when I kept her in a small container the nymphs always stayed with her, hidden under her body, their mouthparts firmly between her legs. Every now and then she would have a bite of a fruit, but the young ones never left her side or fed independently. And yet they grew. I separated a couple of nymphs from their mother and offered them the same conditions and food I was providing her with – they were dead within three days, while their siblings continued to thrive. This short observation convinced me that the female feeds her young with something secreted by her body, and that they completely depended on it, just like mammalian offspring does. My admiration for insects ratcheted up yet another notch.

Table Mountain blattodean (Aptera fusca) from South Africa is a species that exhibits an extended maternal care.

Table Mountain blattodean (Aptera fusca) from South Africa is a species that exhibits an extended maternal care.

Of course, not all blattodeans display the same degree of nurturing and maternal sacrifice, but there is not a single species in this group that does not at least try to give its children a safe start in life. The least the female blattodean can, and most do for their eggs is to encase them in a hard, chitinous purse that protects the eggs not only from physical injuries and desiccation, but also creates a very effective barrier to predators and parasitoids. Usually such a container, known as the ootheca, is carried by the female until the eggs are almost ready to hatch. She will then burry or glue it close to the source of food, usually a fruit or some particularly tasty leaf, and the young hatch a few days or weeks later, ready to start independent life. In more advanced species the female never lets her eggs go, and while she still protects them in an ootheca, she carries it until the very day the young ones are going to hatch. Others take it a step further and, after forming the ootheca and filling it with eggs, suck it back into their abdomen. There, protected by both the ootheca and their mother’s belly the young ones complete their development. Their hatching takes place inside the mother’s abdomen, giving the impression of live birth (such false live birth is known as ovoviviparity.) And finally, there are species, such as the Pacific Diploptera punctata that are truly live bearing.

A large, shield-like pronotum protects the head and front legs of the giant blattodean (Blaberus giganteus) from Guyana.

A large, shield-like pronotum protects the head and front legs of the giant blattodean (Blaberus giganteus) from Guyana. This species is ovoviviparous, which means that eggs are carried by the mother until they are ready to hatch and the nymphs are ready to start independent life.

I have always been fascinated by these animals: the simple elegance of their bodies, their devotion as parents, their dominance in tropical ecosystems, their ancient origin, all this made me want to learn more. But for a group so rich in species and so abundant in many terrestrial ecosystems, we know shockingly little about blattodeans. There are probably no more than 20-30 scientists worldwide who study the 5 thousand or so species we already know about (an equal number of new species of blattodeans most likely still awaits discovery.) At the same time thousands of students and researchers around the world work on mammals, a group with a comparable number of species. As it turns out, the two may have a number of astonishing similarities in their reproductive behavior. Perhaps some of the mammal specialists could be enticed to broaden their taxonomic horizons, and help us learn more about one of the most intriguing groups of animals that ever walked the Earth? Entomologists could really use some help here.

Wood blattodeans (Cryptocercus) took their family life to the next level, and these insects live in small, multi-generational societies. Females feed their offspring symbiotic protozoans, which these insects need to be able to digest cellulose, their main source of food. From here it took only a small evolutionary step towards eusociality, which we see in a lineage of blattodeans known as termites.

Wood blattodeans (Cryptocercus) took their family life to the next level, and these insects live in small, multi-generational societies. Females feed their offspring symbiotic protozoans, which these insects need to be able to digest cellulose, their main source of food. From here it took only a small evolutionary step towards eusociality, which we see in a lineage of blattodeans known as termites.

Tough as nails

Vernal pools are unique aquatic ecosystems, fleeting and unpredictable, but rich in animal life.

Vernal pools are unique aquatic ecosystems, fleeting and unpredictable, but rich in animal life.

Last night I finally managed to see the movie “Gravity”, which proves to me incontrovertibly that humans are not meant to stick their noses outside the protective layer of Earth’s atmosphere, despite having developed all kinds of high tech space gear (which, incidentally, seemed to have been designed primarily to kill Sandra Bullock’s character.) But this unexpectedly beautiful movie also made me think of a certain creature, whose amazing survival skills had lead NASA to use it to test the limits of life’s perseverance in outer space, long before somebody finally realized that people floating aimlessly in the cosmic void make for much better television.

To photograph fairy shrimp and other inhabitants of vernal pools directly in their habitat I used a complicated underwater setup with live video feed that allowed me to see what was in front of the lens. When I turned it on I was amazed how much life was there, it was almost as if I suddenly looked at a tiny coral reef.

To photograph fairy shrimp and other inhabitants of vernal pools directly in their habitat I used a complicated underwater setup with live video feed that allowed me to see what was in front of the lens. When I turned it on I was amazed how much life was there, it was almost as if I suddenly looked at a tiny coral reef.

As the first sunny days of March begin to melt away frozen remainders of winter in the northeaster United States, members of an ancient lineage of animals are getting ready to spring back to life. Throughout most of the year their habitat was as dry as a bone, but when the last patches of snow turned into water, leaf-packed depressions on the forest floor suddenly transformed into small, ephemeral ponds. Known as vernal pools, these fleeting bodies of water will be gone again by the time summer comes, but for now they create a unique aquatic ecosystem. Soon, the water is filled with thousands of tiny animals, at first not much larger than the point at the end of this sentence, but within a few weeks reaching the length of nearly a half of a pinky finger. They are the fairy shrimp (Eubranchipus vernalis), members of a group of crustaceans known as branchiopods, animals that were already present in the Cambrian seas half a billion years ago, before any plants even considered leaving water for terrestrial habitats.

Male fairy shrimp have massive, highly modified antennae, which they use to grasp and hold the female during mating.

Male fairy shrimp (Eubranchipus vernalis) have massive, highly modified antennae, which they use to grasp and hold the female during mating.

Looking at the delicate, soft body of a fairy shrimp it is hard to imagine how a lineage of organisms so seemingly fragile could have survived for so long. Take one out of the water, and it is dead within seconds. Let the oxygen level in the pond drop, and the entire population is wiped out. Given a chance, a single fish could probably do away with them all in a day, but luckily fish don’t do well in ponds that last for only a few months of a year. But fairy shrimps’ frailty is an illusion because where it counts they are as tough as nails.

In the northeastern United States several species of salamanders, such as this Spotted salamander (Ambystoma maculatum) from Westfield MA, share vernal pools with the fairy shrimp.

In the northeastern United States several species of salamanders, such as this Spotted salamander (Ambystoma maculatum) from Westfield MA, share vernal pools with the fairy shrimp.

If you live in a place as transient as a vernal pool, here now but gone in a few months, an environment of unpredictable duration and often uncertain arrival, you better have a solid survival strategy to build your life around. First, once the right environment appears, you must develop very quickly and reach reproductive maturity before the changing conditions kill you. Second, you need a method to keep your genetic line alive, even when the only habitat in which you can survive is gone. And third, plan for the unforeseeable cataclysms, such as sudden evaporation of the pool before you are ready to produce a new generation. Because, if you fail on any of these accounts, your species will not last past the first generation. Fairy shrimp, despite their unassuming physique, are master survivalists in the most hostile and unstable of habitats, and execute the three-step action plan flawlessly.

Male fairy shrimp (Eubanchipus vernalis).

Male fairy shrimp (Eubanchipus vernalis) from Estabrook Woods, MA.

As soon as the vernal pool forms, cysts containing fully formed shrimp embryos from the year before break open, and minute, swimming larvae emerge. They immediately start feeding on microscopic algae and bacteria already present in the water, and grow like crazy. During the first few days of their lives, baby fairy shrimp, known as nauplii, increase their length by a third and nearly double their weight every day. In about a month the animals are fully grown. One pair of the males’ antennae develops into giant, antler-like projections that help them catch and grasp their mating partners, while females grow big egg pouches on their abdomens. A few days later females start to lay at the bottom of the pool large clutches of cysts, eggs with embryos already developing inside, and die shortly after. Soon the water level in the pool begins to drop, and by June all traces of the once vibrant aquatic habitat are usually gone.

The body of a fairy shrimp is nearly translucent, which makes them invisible to a predator looking from above.

The body of a fairy shrimp is nearly translucent, which makes them invisible to a predator looking from above.

But inside the cysts hidden under a thin layer of soil the embryos are very much alive. They slowly continue their development, but can remain in the dormant state, out of the water, baking in the sun or being frozen in ice, for many years. Their outer shell is nearly waterproof, and quite sticky. This stickiness explains the sudden appearance of fairy shrimp in the most unexpected places, including old tires filled with water, after hitching a ride on the legs of birds and other animals. These cysts can live through being dipped in boiling water and liquid air (-194.35 °C, or -317.83°F), which is one of the reasons why these organisms are being used by NASA to test the survival of life outside of Earth’s atmosphere.
The following spring, if everything goes as planned, water of the melting snow awakens the dormant embryos, and within a few days they break the shell of their tiny survival capsules. But not all of them. Only a portion of the cysts responds to the first appearance of water, while others continue their slumber. If the pool dries prematurely, as it sometimes happens during a particularly warm spring, all early hatchlings die, and a second batch of larvae will emerge only if the pool fills up with water again. It has been shown that some cysts in a clutch will wait through eight cycles of wetting and drying before finally deciding to hatch. Fairy shrimp have evolved this ingenious strategy of hedging their reproductive bets in response to the erratic nature of their habitat, and it clearly serves them very well.

Fairy shrimp swim upside down, using 10 pairs of legs to propel themselves and collect bits of algae to feed on.

Fairy shrimp swim upside down, using 10 pairs of legs to propel themselves and collect bits of algae to feed on.

Mozambique Diary: Pardalota

Pardalota reimeri, probably the most colorful and one of the rarest katydids in the world. The individuals I observed in Quirimbas are the first record of this species in 103 years.

Pardalota reimeri, probably the most colorful and one of the rarest katydids in the world. The individuals I observed in Quirimbas are the first record of this species in 103 years.

Ever since I can remember I have been having a recurring nightmare: I am in some incredible location – usually somewhere in the tropics, there are amazing insects everywhere, often those that I have been dying to find, but I need to leave immediately and have none of my collecting gear – not a single vial, no net, no camera (not everybody can relate, I realize, but entomologists know what I am talking about). And last month I finally got to live through this bad dream.

A defensive display of Pardalota reimeri – these katydids feed on highly toxic plants and is likely that their bodies are loaded with poisonous alkaloids.

A defensive display of Pardalota reimeri – these katydids feed on highly toxic plants and is likely that their bodies are loaded with poisonous alkaloids.

Before coming to Gorongosa I flew to the northern town of Pemba where a newly opened campus of the University of Lurió trains Mozambican students in biology and engineering. It was supposed to be a strictly-business trip, meeting lecturers and students, and for this reason I did not bring with me any collecting or sound recording equipment, and only the most basic photo gear. But my friend Harith had a better idea and decided to take me on a short trip to Quirimbas National Park, famous chiefly for its spectacular marine life. Some of his students were working on insect and amphibian faunas of the park, and I said, “Why the hell not.” The seemingly easy trip turned briefly into hell after our Mitsubishi truck decided to part ways with its clutch right in the middle of nowhere. After a long while a friendly driver in a passing car went to fetch a tow truck for us, and eventually we made it to the park.

An unidentified, aposemtically-colored tiger moth found on the same plants as Pardalota.

An unidentified, aposemtically-colored tiger moth found on the same plants as Pardalota.

The first thing that I noticed was the wall of insect sound. The lush miombo forest reverberated with loud katydid calls, ones that I did not recognize. They were unusual for a couple of reasons. One, it was the middle of a hot, African day, and katydids tend not to like it, preferring to call under the cover of the night. And two, the calls were continuous, low frequency, and very complex. They were telling everybody with ears, “Here I am, come and get me.” And when you do that you better have a good trick up your sleeve to protect yourself, as katydid ladies are not the only ones listening: birds, lizards, monkeys, they all love big, juicy insects.

The katydids were calling from high in the trees and I was afraid that I would not be able to catch, or even see them. But then one flew down from the canopy and landed right in front of me. When I saw what it was, my heart skipped a beat – it was Pardalota reimeri, the Holy Grail for katydid aficionados (there are a few of us out there). This species had been known only from the original type series, described in 1911 and preserved in a museum in Berlin. What is special about this species is that even those old, dried husks retained vivid, crazy colors, unlike those of any other known katydid species. And colors as awesome as this indicate an equally awesome biology.

I caught the katydid and he immediately went into a defensive mode: he opened his bright purple, black and white wings, and exposed his neon-orange abdomen and cervical membrane; he lifted his hind legs that had yellow and black markings, remarkably similar to those of toxic chrysomelid beetles. This was either a daring bluff, or this thing was seriously poisonous. All around me other males continued to sing.

A video of a P. reimeri nymph – although the insect is not feeding it gives the perfect illusion of the front end of a fuzzy caterpillar chewing on a leaf.

What to do? Here I was, surrounded by a remarkable entomological discovery, but with no way to collect, preserve, or record it. I decided to exploit Harith’s students and we fanned out looking for the insects. Soon we discovered where they sang – they were only calling from, and feeding on, two species of trees, both known to produce potent chemical defenses, including some powerful psychoactive alkaloids. This almost certainly explained their aposematic coloration. We also found nymphs of this species, which turned out to be incredibly hairy. In fact, when I first saw one I thought I was looking at a fuzzy caterpillar feeding on a toxic plant – its movements were an uncanny imitation of the front end of a caterpillar chewing on a leaf, even though I was looking at at the katydid’s butt. It wasn’t shocking then when a minute later I noticed very similar looking caterpillars feeding on the same plant and, also on the same plant, tiger moths (well known to be toxic) wearing colors very similar to those of the katydids’. Having nothing else at my disposal I pointed my Canon 6D at the canopy and used its video recording feature to record the sound of the singing males. I collected as many individuals as I could, stuffing them into Ziplock bags, hoping to be able to get decent photos and proper sound recordings later on.

In the end I managed to collect enough material and data to write a short note about the biology of this species. But not being able to do a very good job at data and specimen collecting in the field was not a pleasant experience. I have already learned never to go anywhere without my headlamp, a GPS, and a camera, and now I am adding to this list an ultrasonic sound recorder and a large set of vials with 96% ethanol. On the second thought, maybe also an extra clutch for a Mitsubishi and a satellite phone. And some beer, for emergencies.
Two nights later I had a nightmare about Quirimbas.

A female P. reimeri cleaning her foot.

A female P. reimeri cleaning her foot.