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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.

Footprint Cave, Belize

Africa in Mesoamerica – a beautiful, little pool on the floor of the upper chamber of the Footprint Cave; it even has an adjoining pool that looks like the Arabian Peninsula.

Africa in Mesoamerica – a beautiful, little pool on the floor of the upper chamber of the Footprint Cave; it even has an adjoining pool that looks like the Arabian Peninsula.

It has been a long while since the last update to this blog, mostly because of my hectic travel schedule (in fact, I am typing this on a shaky train ride). But it has been an interesting time, with lots of great photo ops. Last week I joined Alex Wild, John Abbott and Thomas Shahan in Belize to teach BugShot 2013, an intense course in tropical insect macrophotography. Aside from working with a friendly group of photography masters and enthusiastic students it was my first exposure to some of the most interesting members of the troglobitic Mesoamerican fauna as the workshop was held at the Caves Branch Lodge in central Belize, an area famous for its karst formations, replete with deep limestone caves.

The most famous cave in the area is the Footprint Cave, named after calcified Mayan footprints found in the deeper section of the cave, along with a number of artifacts and skeletal remains. The cave was looted in 1994, and many artifacts and remains are now gone, but you can still see there ancient fire places and shards of Mayan pottery. It was quite an unreal and humbling experience to sit next to a pile of ash that might be over 2,000 years old but still looks warm. The cave itself is stunningly beautiful, cathedral-like, with massive stalactites that shimmer in the light of the headlamp. The shallow Caves Branch River flows through it, and as you walk along its bed large catfish and shrimp follow your every step, looking for small aquatic invertebrates flushed from under the sand.

Female cave cricket Mayagryllus apterus, a species endemic to the Caves Branch system of Belize.

Female cave cricket Mayagryllus apterus, a species endemic to the Caves Branch system of Belize.

As we walked deeper into the cave, leaving behind its large opening and eventually all traces of natural light, we began to discover a multitude of life forms that call this cave their home. Biologists explored Footprint Cave in early 1970’s, but little work has been done since. Many animal species found in the Caves Branch system are likely endemic, and some still await their formal scientific description. I was thrilled to see dozens of long-legged cave crickets Mayagryllus apterus, described only in 1993 from specimens collected in these caves. They were often accompanied by large, equally spindly amblypygids Paraphrynus raptator (Phrynidae), and apparently another, yet undescribed species of the family Charontidae is also present in the cave (and Gil Wizen might have found a third, possibly new amblypygid species). I was hoping to find some dinospiders (Ricinulei) there, alas, no such luck, but flipping rocks on the banks of Caves Branch River revealed a tiny, equally interesting arachnid, a pygmy vinegaroon (Schizomida). The species found in the Footprint Caves is a yet undescribed species of Schizomus, and I would love to be able to collect some specimens and describe them (I need to look into getting some permits for Belize).

A troglobitic isopod crustacean Troglophiloscia sp.; note its lack of pigmentation and eyes, characteristics typical of cave-dwelling organisms.

A troglobitic isopod crustacean Troglophiloscia sp.; note its lack of pigmentation and eyes, characteristics typical of cave-dwelling organisms.

Silk strands on the cave ceiling, produced by the larvae of predaceous fungus gnats (Keroplatidae: ?Macrocera sp.)

Silk strands on the cave ceiling, produced by the larvae of predaceous fungus gnats (Keroplatidae: ?Macrocera sp.)

Yet the most interesting organism in the cave was a fly. When we shone the light at the low celling of the cave we could see curtains of thin, glistening strands of sticky silk produced by larvae of predaceous fungus gnats of the family Keroplatidae; I have not been able to identify the species that lives in the Footprint Cave, but it is possibly a member of the genus Macrocera (Macrocerinae). The strands spun by the larvae are covered with droplets of oxalic acid, which trap and kill tiny flying insects, mayflies mostly, found in the cave. Members of a related subfamily Arachnocampinae found in Australia and New Zealand are famous for their bioluminescence, but the ones found in Belize are of the non-glowing variety. Still, it was a beautiful spectacle to see thousands of hair-like strands undulate gently in the breeze caused by a person walking several meters away.

The strands are covered with droplets of oxalic acid, which trap and kill unlucky insects, such as this mayfly, that brush against them in flight.

The strands are covered with droplets of oxalic acid, which trap and kill unlucky insects, such as this mayfly, that brush against them in flight.

Everybody was sad to leave the cave, which turned out to be the highlight of our photographic workshop, although the fauna of the rainforest that surrounded the lodge where we stayed was equally interesting. Not being able to collect anything was torture for me, but I hope that some day soon I will be able to come back to Caves Branch, this time wearing only my entomologist’s hat.

A new, yet unnamed species of the pygmy vinegaroon (Schizomus sp.) from the Footprint Cave.

A new, yet unnamed species of the pygmy vinegaroon (Schizomus sp.) from the Footprint Cave.

Blue land crab

Males of the blue land crab (Cardisoma guanhumi) from the Dominican Republic sport giant claws used in territorial display and combat. [Nikon D1x, Nikkor 17-35mm]

Males of the blue land crab (Cardisoma guanhumi) from the Dominican Republic sport giant claws used in territorial display and combat. [Nikon D1x, Nikkor 17-35mm]

Unable to break her ties to the sea, a female blue land crab cautiously approaches the edge of the beach to release her eggs during the full moon. Shecannot swim, thus she must be careful not to be swept away by the waves, and soon she runs back to her burrow in the forest. Her planktonic larvae will develop into tiny crabs in less than two months and then will leave the ocean to begin terrestrial life. [Nikon D1x, Nikkor 17-35mm, flash Nikon SB-28DX]

Unable to break her ties to the sea, a female blue land crab cautiously approaches the edge of the beach to release her eggs during the full moon. She
cannot swim, thus she must be careful not to be swept away by the waves, and soon she runs back to her burrow in the forest. Her planktonic larvae will develop into tiny crabs in less than two months and then will leave the ocean to begin terrestrial life. [Nikon D1x, Nikkor 17-35mm, flash Nikon SB-28DX]

[An excerpt from the book “The Smaller Majority.”]

A giant among the smaller majority

Coconut crab (Birgus latro) on Guadalcanal, Solomon Islands [Canon 1D MKII, Canon 16-35mm, speedlight Canon 580EX]

While I can honestly say that there is no animal that I find uninteresting, none is higher on my list of the most amazing animals than the coconut crab (albeit this top place in my ranking is shared by many.) The first thing that you will notice about this crustacean is of course its size – it is huge. In fact, with the maximum leg span of 1 m (~3 ft) and weight of 3 kg (6.6 lb), it is the largest invertebrate animal you will find on land. There exist larger marine crustaceans, and there are many much larger cephalopods, but on dry land the coconut crab is the undisputed champion. It is also incredibly long-lived, for a terrestrial invertebrate, reputedly capable of reaching the ripe age of 40 years.

The chelae (“claws”) of coconut crabs are incredibly powerful, capable of cracking open a coconut shell [Canon 1D MKII, Canon 16-35mm, speedlight Canon 580EX]

From the taxonomic point of view, coconut crab (Birgus latro) is more closely related to hermit crabs (infraorder Anomura) than true crabs (infraorder Brachyura), and you can tell that by, among other things, the presence of only 4 pairs of walking legs (true crabs have 5 pairs.) Another giveaway is its life cycle – following a brief period as pelagic larvae, young coconut crabs carry a shell, just like other hermits. Only after reaching the size of about 10 mm the young abandon the shell, and begin to resemble the adults.

Legs of coconut crabs are of different length, perfectly adapted for climbing coconut trees [Canon 1D MKII, Canon 16-35mm, speedlight Canon 580EX]

The transition to the terrestrial lifestyle is more complete in the coconut crab than in any other land hermit. Not only did this species eschew a protective shell of a snail, thanks to its hard, resistant to water loss abdomen, but its senses are more akin to those of insects than crustaceans. All other terrestrial hermit crabs can only detect smells if the air humidity is very high – their olfactory organs are still those of an aquatic animal, and can only respond to chemical cues if they are dissolved in water. Coconut crabs, on the other hand, can smell things in dry air, indicating the development of land-adapted olfaction.

Like all arthropods, coconut crabs need to molt periodically, and the process takes place in a deep underground burrow [Canon 1D MKII, Canon 100mm, speedlight Canon 580EX]

Despite the common name, coconut crabs don’t feed only on coconuts. Like many decapod crustaceans, they are opportunists and will eat anything organic that they can put their powerful claws on (so powerful are their claws that you can easily lose a finger if you are not careful when playing with one.) In addition to cracking coconuts, they have been known to hunt shore birds sitting on their nests at night, steal dog food from people’s backyards, and will gladly eat any kind of carrion. This last habit had them implicated in the disappearance of the famed pilot Amelia Earhart, and you can sometimes hear speculations that her body might have been dismembered and eaten by coconut crabs somewhere around the archipelago of Kiribati after her plane’s crash.
Even if true, it is the crabs that suffer more from our appetite for crustacean flesh than the other way around. Their meat is purportedly deliciously coconutty, and there is plenty of it in an animal of their size. Nor surprisingly, they have been overharvested within most of their range around tropical islands of the Pacific and Indian Ocean, and have virtually disappeared from many places where they used to be common. Many countries that still have these magnificent animals now have laws protecting them, or at least limiting their harvest (one of them is the United States, which protects the crabs on the island of Guam), but an official conservation assessment of this species across its entire range has never been done. Therefore, the coconut crab is still listed as Data Deficient by the IUCN Red List, and its trade is not regulated by CITES. Hopefully this will change in the near future, it would be an unforgivable tragedy to lose this wonder of crustacean evolution.

Live young coconut crabs for sale at a seafood market on Okinawa, Japan [Canon PowerShot SX100 IS]

The benefits of constant rain

Even in the middle of the day, forests of New Guinea can appear dark, saturated with water and engulfed in a perpetual mist. [Canon 1Ds MkII, Canon 16-25mm]

I am not a big fan of cold, rainy days, like the one we are having today in Boston, and so I need to remind myself that this type of weather actually produces one of the richest, life-friendly environments imaginable. Not in Massachusetts, however, but in the mountains of Papua New Guinea.

In 2009 I spent a couple of months on the islands of New Guinea and New Britain, conducting a survey of katydids and related insects, which revealed that over 60% of katydid species there were new to science. This blew my mind, but I was also astounded by the preponderance of organisms and behaviors that I always thought of as quintessentially aquatic, which I nonetheless found on land.

Male of a yet unnamed, new species of tree frog (Oreophryne sp. n.) guarding a clutch of eggs in the Muller Range of PNG [Canon 1Ds MkII, Canon 100mm macro, 2 speedlights 580EX]

Few places are more humid than rainforests of New Guinea. Annual rainfall in some areas reaches seven thousand millimeters, or even a staggering twelve thousand millimeters (or nearly forty feet) per year! The atmosphere is saturated with moisture, and thick mats of mosses and lichens trap and store huge amounts of water. Yet at the same time many parts of the island are virtually devoid of streams, rivers, or any large bodies of standing water. This is due to the geological composition of its surface, which in many places consists of karst, a formation in which the underlying limestone layers have been dissolved, forming countless sinkholes and fissures. This prevents the accumulation of surface water, forcing organisms that rely on its presence for their reproduction and development to find other solutions.

A semi-terrestrial naiad (nymph) of a damselfly (Papuagrion sp.) on a Pandanus leaf. [Canon 40D, Canon MP-E 65mm, 2 speedlights 580EX]

Frogs are organisms whose early development requires an aquatic habitat, an inconvenient remnant of their early evolutionary history. In most species females lay their eggs in streams and ponds, and developing tadpoles use their gills to breathe under water. But on New Guinea, where surface water is scarce, many species have evolved strategies that allow them to bypass a free-living tadpole stage entirely. Rather than laying hundreds or thousands of small eggs and leaving them to their own devices in the water, they produce a handful of very large eggs and take care of them until they are ready to hatch. Each egg contains enough nutrients, in the form of a large yolk reserve, that allows the embryo inside to complete its development into a tiny, independent froglet. Unlike reptile or bird eggs, frog eggs lack a hard, water-impermeable shell, and risk their desiccation if not protected and moistened regularly. For this reason, one of the parents stays with the eggs and safeguards them throughout their development. In frogs of the genus Oreophryne, the male guards the eggs suspended in a clutch underside a leaf, and leaves them during the day to go hunting for insects, but comes back every evening to moisten them with water and shield them from harm. After a few weeks, young frogs are ready to become independent, and break the walls of their miniature aquatic cradles.

Pink, terrestrial amphipod crustacean from the Muller Range of PNG [Canon 40D, Canon MP-E 65mm, 2 speedlights 580EX]

But tadpoles with terrestrial development were not the only animals that seemed out of place on the forest floor of New Guinea. High in the mountains of the Muller Range we found damselfly nymphs crawling on leaves of Pandanus trees, and below, in the leaf litter, pink amphipod crustaceans mingled with ants and beetles. I also saw in those forests land crabs, flatworms, and sea anemones. Well, the last ones turned out to be strange mushrooms of the genus Aseroë, but for a second I almost believed in the existence of terrestrial sea anemones – if they were to live on land, rainforests of New Guinea would probably come closest to their underwater habitat.

Ok, now I feel a little better about the rain behind the window.

(You can read more about the amazing life forms on New Guinea in my book “Relics: Travels in Nature’s Time Machine”, from which I took a fragment of this text.)

Sea anemone mushrooms (Aseroë sp.) from New Britain [Canon 1D MkII, Canon 24-105mm]

The rarity of blue

Blue poison arrow frog (Dendrobates azureus) from Guyana [Canon 5D, Canon 100mm macro, 2 speedlights 580EX]

The other day I was listening to Radiolab in my car (if you don’t know this program, give them a listen), and the topic of the episode was our perception of colors. I was struck by the statement that the color blue is exceptionally rare in nature and, as a consequence, philologists claim, this is the last color to enter human vocabulary in the course of the evolution of individual languages. This is simply because we rarely need (or needed, historically speaking) to describe things that are blue. I always knew that blue was relatively rare among terrestrial animals, albeit examples of blue species can be found in nearly every major group, and decided to see if the pattern of rarity of blueness is reflected in my photos.

I used the program Picasa, which allows you to filter images by their color information, to do a search for images with blue as the predominant color. I scanned only about 15,000 of my images, but they represented different geographic regions and groups of animals, and thus were representative of my entire image collection. Naturally, I got a lot of hits with blue sky or water, but also a few photos showing blue animals. The most surprising thing was that nearly all blue animals were from the New World: morpho butterflies, Coprophaneus dung beetles, blue crabs (Callinectes), and poison arrow frogs, to name a few. The only non-American species that came up in the search was a Japanese mud crab Ilyoplax pusillus.

Now, there are many animals in Europe, Africa, and Asia with blue colors (lycaenid butterflies, blue-winged Oedipoda grasshoppers, Blue Tits and other birds etc.), but I cannot think of anything that rivals North American bluebirds or morphos. This makes me wonder if the evolution of color classification schemes in human languages that was mentioned in the Radiolab program might have been different among Amerindian tribes that are routinely exposed to blue animals. The only examples of languages that lacked a specific word for blue came from Africa, and the historical examples of languages that coined this word late in their evolution came from Europe. I need to read up on this.

Male blue mud crab (Ilyoplax pusillus) from Kyushu, Japan performing a courtship display (make sure to click on the image to see the entire display) [Canon 1Ds MkII, Canon 180mm macro, 2 speedlights 580EX]

Galapagos in red and blue

All mature Sally Lightfoot crabs (Grapsus grapsus) display a wonderful combination of red, blue, and orange [Canon 7D, Canon 24-105mm]

The very first animal that I saw upon landing in the Galapagos was also one that I found to be the most beautiful of all the organisms I encountered in the archipelago. Every rock within the splash zone of the shore was dotted with vermilion red, large crabs that moved with a slow, deliberate gait of an animal always ready to sprint at the slightest provocation. These were the famous Galapagos Sally Lightfoot Crabs (Grapsus grapsus), which I soon discovered to be a permanent fixture on nearly every piece of volcanic rock throughout the islands.
Sally Lightfoot crabs are not endemic to the Galapagos, and they can be found along the Pacific shores from Baja California to Chile. They are also known from the tropical waters of the Atlantic, although some taxonomists suggest that the Atlantic populations represent different species. But it is in the Galapagos where they reach the highest density, and their flamboyant bodies are as emblematic of the islands as the iguanas and giant tortoises.

Sally Lightfoot crabs got their name from their ability to move with lightning-fast speed across the the surface of the water, without sinking under. They do it in a way similar to that of basilisk lizards, by using their strongly flattened legs to increase the area of contact with the surface of the water, and if there is a crab species that deserves to be called Jesus Christ Crabs, it is them.

Crabs on the volcanic rocks on the shores of Isabela [Canon 7D, Canon 24-105mm]

Sally Lightfoots feed mostly on algae growing within the splash zone, and only very reluctantly enter the ocean. I had caught one large individual while snorkeling along the shore and released it under water a few meters from the shore – the crab immediately ran towards the rocks and climbed above the surfaces. Because of their mostly vegetarian nature, their chelipeds (“pincers”) are rather weak and designed for grazing soft plant tissue, and only rarely do they resort to preying on other animals.

Their bright coloration has baffled zoologists for quite some time. Both males and females are equally brightly red and blue, which seems to preclude the use of these colors as sexual attractants. Young crabs are cryptically dark, and almost invisible on rocks, which is a typical kind of coloration found in grapsid crabs living above the water level. My personal suspicion is that their bright colors have a similar function to that of brightly colored hind wings seen in many otherwise cryptically colored insects, such as noctuid moths or oedipodine grasshoppers. These animals display flashy, bright patterns while flying away from a predator, but immediately hide them the moment they land, seemingly disappearing and confusing the predator. Crabs cannot fly, but they run towards narrow crevices in the volcanic rocks with such an amazing speed that the effect is quite similar; the presence of similarly colorful individuals all over the rocks is sure to make a bird hunting for crabs confused about which individual he was following.

These three individuals of different ages exemplify the color change that takes place during Sally Lightfoot crabs’ development [Canon 7D, Canon 100-400mm]