On this typical sunny morning on this southeastern Florida beach, holidaymakers loll on their blankets and splash in the waves. Walking among them are two rather atypical beachcombers: Robert Higgins, 62 years old, dressed in a T-shirt and shorts and a floppy hat that covers his close- cropped hair; and Marie Wallace, a dark-eyed woman in her mid-forties in similar garb. They carry with them a shovel, buckets, plastic bottles, a fine-mesh screen, and a supply of freshwater--all the tools they’ll need for today’s scientific expedition.
Although the other people on the beach are completely unaware of it, beneath their feet, in the seemingly sterile sand, there exists a microscopic jungle of surreal animals waiting to be discovered. Some of these minuscule invertebrates spend their lives slithering between the sand grains. Others flutter along by whirling hairlike propellers on their heads. Still others, as waves crash over them, hold tight to the sand grains with tiny claws, as if clinging desperately to giant beach balls. Some of these tiny creatures graze on algae. Some of the grazers are themselves food for predators who insert lancelike tubes through their bodies and suck out their innards.
The dynamic, abrasive environment of a sandy beach might seem an impossibly inhospitable place to call home. Yet some of the greatest diversity of life on Earth hides here, on and between the grains of sand. It’s even richer, in taxonomy’s broadest terms, than the Amazon rain forest, says Higgins, one of the world’s experts on this hidden ecology. Those broad terms he is referring to are phyla--the 40 major groups into which all animals are divided. Humans, for example, belong to the phylum Chordata, which comprises all the animals that have backbones and thus includes birds, reptiles, fish, and lampreys. To fall into another phylum, you’ve got to be a radically different beast, yet so far 22 phyla of animals have been discovered living in sand.
Higgins has searched far and wide for such life, from the frigid beaches of Greenland to the rugged coast of southern Chile. But this tame Florida shore is prime hunting ground. The animals he has his eye out for are known collectively as meiofauna. The word means lesser animals, which is not a slight to the animals but a reference to the tools that zoologists use to collect them. Meiofauna describes animals that fall between two sizes of collecting screens, Higgins explains. The larger screens are made with 1-millimeter mesh, and scientists use them to winnow out big sand dwellers such as sea urchins and sea anemones. Meiofauna readily pass through such sieves, but scientists can gather them by using the 42- micrometer (.042 mm) screen--a mesh finer than a silk stocking. (Those who want to catch smaller game such as bacteria use an even finer mesh, with just 2-micrometer openings.)
Despite their small size, meiofauna are far from insignificant: they are as common and abundant as the grains of sand they call home. One study calculated that a single handful of wet sand contains 10,000 of these animals. Yet although meiofauna inhabit every seashore, as well as the sands and gravel far out at sea, they remain virtually unknown and poorly understood. Only within the past decade have ecologists begun to realize the important role they play in the health of the marine ecosystem, consuming detritus and pollutants that filter into the sands and serving as the primary food source for shrimp and bottom-feeding fish.
Very few people, including some scientists who study the larger invertebrates, know anything about them, says Higgins. Consequently, the achievements of meiofauna specialists often go unnoticed. Higgins, for example--who recently retired as a curator and researcher at the Smithsonian Institution in Washington, D.C., and is now an adjunct professor at three North Carolina universities--has discovered scores of new species, genera, and families of meiofauna over the past 39 years. With fellow zoologist Reinhardt Kristensen of the University of Copenhagen, he is responsible for the creation of the newest phylum of animals. Only two other new phyla have been created this century, simply because the existing categories are so broad and all-encompassing. But although 12 years have passed since Higgins and Kristensen named their new sand-dwelling phylum, the word--Loricifera--has yet to make it into Webster’s. Most meiofauna are what I call bibliocryptozoans, says Higgins, an amused smile lighting up his hazel eyes. They are animals that are extremely common on Earth but seldom found in our books.
Common though they may be, it still takes effort and expertise to find them. Today, on this Florida beach, Higgins knows exactly where to look. He chooses a spot three feet from last night’s high-tide mark and scrapes away the dry surface sand. He then begins digging a hole--a scientific skill that he says he perfected as a young Marine.
There are fewer animals in these upper, drier sands, Higgins explains as he shovels, noting that most meiofauna require at least a thin film of water around their grain of sand to survive and that they thrive best where the sands are always wet. Out at sea Higgins can get plenty of meiofauna by dredging the top few inches of the ocean floor, but here on the beach he has to dig six feet down to reach slushy gravel. He shovels this prime meiofauna habitat into a bucket, then tops it with seawater to keep the tiny creatures alive. To look at the stuff--wet, sloppy sand-- you’d never guess that anything other than humble protozoans lives there.
Many of the meiofauna cling in various tenacious ways to the sand grains, and so, Higgins says, people have invented a variety of collecting techniques, depending on what animal they’re trying to catch. The most common method is to wash the samples of sand and gravel with magnesium chloride, which stuns the animals and causes them to loosen their grip. But a bath of freshwater, Higgins has found, seems to work just as well, causing the creatures to lose control of their salt balance and thus their bodily functions. If they’re exposed to the freshwater for only 20 seconds, the bath seldom kills them, he says, so they’re still in pretty good shape when you get them to the lab.
Accordingly, Higgins puts handfuls of the sand into a bucket of freshwater, then swirls the mixture into a slurry. Incapacitated, the meiofauna surrender their grasp on the sand grains, which settle to the bottom of the bucket as the animals continue to whirl. Wallace, Higgins’s assistant, kneels next to him, holding the sieve over another bucket. Higgins deftly pours the slurry through the sieve, leaving most of the sand behind. Wallace’s bucket fills with water; trapped in the sieve is a frothy residue that contains the meiofauna. Wallace rinses it into a bottle with squirts of filtered seawater. In this way she and Higgins fill several bottles, holding, Higgins promises, thousands of meiofauna.
The idea of looking for animals among the seas’ sands didn’t occur to biologists until this century. Scientists wanted to know what lived in the oceans, so they dredged the seafloor, then washed the gravel through their 1-millimeter mesh screens, says Higgins. That way they collected the macrofauna: the sea slugs and starfish. But they never thought to look for animals in the material--the sands and gravel--that was washed through the screens. In the 1920s zoologist Adolf Remane began using a finer screen to study the beach sands of Germany’s North Sea. He revealed a profusion of creatures previously unknown to science, and not a year has passed since without the discovery of at least a dozen new meiofaunal species. It’s a rich, complex world, says Higgins, but it’s one we’ve barely scratched the surface of. It’s impossible to say how many more species are left to be found and identified; I’ve got hundreds of new ones waiting right now to be described.
Higgins transports the collecting equipment and bottles of meiofauna back to the Smithsonian Marine Station at Link Port, Florida, where he has spent numerous field seasons. Only there, with the aid of a dissecting microscope, does this lilliputian world become visible. Even when enlarged 50 times, the animals are minuscule. But now you can see that they’re busy. Swimming, crawling, flailing, and writhing among the shiny chips of sand (some of which, when magnified, look as grand as Yosemite’s El Capitan) are the flat, segmented worms known as gastrotrichs, bristling with spines. There are pear-shaped rotifers, their heads awhirl with spinning cilia; wormlike turbellarians that are so protean they can transform their fat sausage bodies into slender threads as they maneuver between the sands; and rigid, boxy tardigrades. Elsewhere there are shrimplike mystacocarids and copepods, mitelike halacarids, and wormlike nematodes--all of which look as alien as their names sound.
Around them glint the plants that also grow in this world-- emerald strands of algae, star-shaped radiolarians, golden foraminifera, octagonal diatoms--as well as odd bits of detritus and cast-off body parts: here a silvery piece of a sponge’s internal skeleton, there a sea urchin’s glassy spine. Occasionally, a dinoflagellate (a one-celled alga), shaped like a speedboat, zooms past as if on an urgent errand, while ciliated protozoans glide about with the elegance of swans.
Here’s an epsilonematid nematode, Higgins announces triumphantly seconds after setting a petri dish of this morning’s catch under his microscope. It’s a habit of Higgins’s to search dishes quickly for the usual suspects (like nematodes) and for creatures he doesn’t recognize. After you’ve done this for a while, you develop a sense like a good bird-watcher, he explains. I’m just an amateur bird-watcher, so I’m always amazed at what a top-notch birder--or a native in the forest--is able to see. But here, searching for meiofauna, I’m that person in the forest. With only a glimpse of a moving creature or a broken piece of meiofaunal anatomy, Higgins can visualize the whole beast and name it.
The epsilonematid nematode that Higgins has spotted is one of the easier ones to recognize since, as its name implies, the thin, wormlike animal is shaped something like the Greek letter epsilon (e). It’s a shape perfectly suited for living in the crevices of the beach sands: slightly curved at both ends and nipped in at the waist. The nematode’s body is covered with tiny spines, which protect it from its abrasive home and enable it to wedge itself securely between the sandy particles. You want to be able to do that, says Higgins, if you live at the shore, where the incoming and outgoing tides can make it fairly turbulent.
Most of the meiofauna have some variation on these themes: a shape, or anatomic structure, that allows them to squeeze, like spelunkers, through the crevices between the sand grains, and a gripping mechanism to keep them in place when the going gets rough. A secure grip is particularly important since many meiofauna species cannot swim and so are in constant danger of being washed out of the sand and into the sea. The animals are also typically transparent (though they may take on a golden or greenish hue after feeding on diatoms and algae) and flat, elongated, or cylindrical. Nearly all have some kind of protection from abrasion and collision, such as spines, shells, scales, or even body walls that are padded like the bumpers of a car.
Searching his petri dish further, Higgins soon finds a tardigrade, another creature for whom a tight grip is crucial to survival. Tardigrades are also found in freshwater, where they have plump little bodies with stumpy legs, a configuration that has led to their popular name of water bear. But this marine tardigrade, all of half a millimeter in length, looks more like a piece of silver confetti equipped with legs and claws. It uses the claws to grip and move over the sands. Since these particular ones can’t swim, they really do have to hang on for dear life, says Higgins. Another tardigrade species has mechanical suction toes to keep itself in place; while a third, which also inhabits the Florida coast, boasts both suction toes and claws. Still another suction-toed species has a tear-shaped bubble on the end of a long tail, which gives it buoyancy. To feed, it lets go of its sandy particle and, with its tail aloft, hovers over the gravel, grazing like a zeppelin-towed cow on the thin layer of microscopic algae that covers the seafloor.
Other meiofauna, such as gastrotrichs and turbellarians, have mastered their dynamic habitat with the aid of special adhesive organs. Depending on the species, these tubes--which appear as small bumps--may be found near the animal’s mouth, along its sides, or near its tail. Some of the glands secrete a substance sticky enough to rival epoxy, while the others dispense a solvent. A gastrotrich, for example, can glue itself securely to a grain of sand with one squirt, then dissolve the bond with a second, freeing itself to swim by beating the hundreds of cilia that line its underbelly.
A kinorhynch, on the other hand, moves with a bit less grace. Higgins describes the creature as an umbrella in a canister. Its body is a hollow cylinder with a set of curved arms that emerge from the front end. Inside the cylinder is the animal’s head--the umbrella part-- which is armed with a ring of nine spines. The animal works its way through the world with a sort of breaststroke. As the arms come into contact with sand or mud, they push against it to drag the body forward. As they do so, the head emerges from the cylinder and unfolds its spines, grabbing on to whatever’s in front of it. Once it’s anchored in this fashion, the kinorhynch retracts its arms into the cylinder and repeats the sequence. Since sand grains are often much larger than the average kinorhynch, it may take the creature several minutes to explore each one.
Unfortunately, in the laboratory it is nearly impossible to see these animals move--or do anything else--as they normally would. After all, a petri dish of salt water is vastly different from the snug sandy matrix meiofauna call home. When you look through the microscope at tardigrades, for example, which normally live attached to a grain of sand, they appear to be searching for something to grasp: their clawed feet move back and forth, back and forth, but the animal makes little headway. Consequently, to get a better idea of how meiofauna usually live, zoologists sometimes place unfiltered samples under the scope. You can see them crawling over the sand grains, and that’s how we have some idea about how they move, explains Higgins.
Still, most of Higgins’s work is the identification of new species, and for that he needs screened and filtered water to get an unobscured view of the animals. But even with a good view, it can take years to know what you’re really looking at, as Higgins discovered with his new phylum, the Loricifera.
In 1974, Higgins found an animal off the coast of North Carolina that sported feathery plumes on its head and seemed radically different from other meiofauna he had seen. He guessed it was a larval stage of some new species, but with only one sample, he wouldn’t venture naming or describing it formally.
Eight years later Reinhardt Kristensen brought some meiofauna for Higgins to examine. Reinhardt had collected some samples off the coast of Brittany and was rushing to catch a train, and so he hurriedly flushed these with freshwater, Higgins recalls. There were 50 adult specimens and even more larvae of a species that Kristensen had never seen before, and their feathery plumes told Kristensen that these were strange animals indeed. He wondered if Higgins could identify them for him.
He showed them to me, says Higgins, and I said, ‘Oh, I have one of those, too.’ What Higgins had thought was a larva from North Carolina actually turned out to be an adult of this bizarre new life-form. We knew what we had was a new, distinct animal. Over two years, Higgins and Kristensen cataloged and described the features that made their specimens unique. It was a great deal of work because the Loricifera are the most complex microscopic animals, says Higgins. The head segment alone, although only 50 micrometers long, is composed of nine overlapping rings with more than 200 feathery appendages--and all had to be counted, measured, drawn, and described. Most startling of all, Higgins and Kristensen discovered that these creatures had the smallest cells of any animal. An appendage only 40 micrometers in length, says Higgins, will have as many as seven specialized cells in it--cells for the muscles, nerves, epithelium.
Deciding that their new animal did not fit any existing taxonomic category, Higgins and Kristensen created a new phylum for it--in essence saying, Here is a new group of animals unlike any other on Earth. The name Higgins chose comes from the Latin lorica, meaning corset, and ferre, to bear, because the cuticle rings that sheathe the animals fit them like a girdle. Among the Loricifera, Higgins and Kristensen initially described 3 genera and 5 species. Today over 70 species have been identified from sites around the world--one was even found five miles below the surface of the North Pacific Ocean. The list keeps growing: Higgins himself has five new ones to describe from the Louisiana coast.
Despite their long labors, Higgins and Kristensen know next to nothing about the behavior of Loricifera. The organisms are difficult to find and once caught usually expire before reaching the lab. All the adults we’ve seen have been dead, says Higgins. Kristensen once saw a live larva; it had two appendages that it kicked like a scuba diver. But since the adults lack fins, these appendages are apparently lost as the animals, on their way to maturity, pass through several stages and shed successive exoskeletons. Higgins and Kristensen suspect that for locomotion the adults use their feathery head appendages. There are muscle cells in those plumes, says Higgins, but whether the Loricifera spin them or wave them about, we just don’t know.
The zoologists don’t know what the Loricifera eat, either, but guess that they may subsist as parasites because their narrow snouts appear designed for piercing and sucking. Equally mysterious are the Loricifera’s sex lives. The males have large, prominent testes that take up as much as 75 percent of the space in the abdomen, says Higgins, while the females produce one or two eggs at a time. The eggs too are large; a single egg can occupy half the female’s abdomen. Presumably the male transfers packets of sperm into the female’s body, but Higgins can’t say for sure. So many of these things depend on a chance sighting. You find them by doing what we’re doing now, going carefully through each sample, watching and searching.
Much more is known about the mating habits of some of the other meiofauna species. Like the Loricifera, many of these creatures produce only one egg at a time. Animals that lay hundreds of eggs (such as many species of fish) can afford to abandon their offspring, since it is likely that many of their young will survive the vagaries of nature. But these species of meiofauna, like humans, produce so few offspring that they must jealously guard them to be sure they survive their youth. Thus the hermaphroditic hydra, Otohydra vagans (which looks like a gelatinous oval with a dozen fat tentacles sprouting around its mouth), incubates its single egg in an internal pouch. Only when its young is close to maturity does the hydra release it into the sands. Many turbellarians (those protean flatworms) also produce a single egg at a time, and with a squirt of an adhesive from their reproductive system, they attach it to a grain of sand. They then cover the egg with a protective secretion, effectively sealing it in a cocoon.
As he gazes intently through his microscope, Higgins now spots one of these turbellarian capsules, recognizing the almost metallic golden hue and the delicate wine-cup shape. The young turbellarian inside, he realizes, is trying to get out, struggling like someone jammed into a down sleeping bag. Now, that’s something I’ve not seen before, Higgins says before he calls for others to admire his hatching turbellarian. I’ve seen these egg capsules hundreds of times, he adds, putting his own eye back to the microscope, but this is the first time I’ve ever seen one hatch.
Once the turbellarian is finally free, it hastily swims off in search of a meal. Turbellarians are predators, and many of them lance their prey with a dartlike structure in the mouth; after inserting the lance, they suck the animal dry. There are many other predators among the meiofauna, and some omnivores as well--nematodes will attack their fellow meiofauna, but they eat algae as well. One nematode is even something of an agriculturalist, as Higgins puts it. As it burrows through the sediments, it secretes a mucus that serves two purposes: it stiffens the tunnel to prevent it from collapsing and acts as a fertilizer on which algae thrive. When the nematode later comes slithering through this tunnel again, it will find a fresh crop of algae to browse on. Other forms of meiofauna, such as the rotifers and gastrotrichs, act like vacuum cleaners, sucking up bacteria, algae, and organic detritus from the sands. They really are the garbage collectors of the system, consuming all the dead bacteria and plankton left on the shore in the sands, says Higgins.
So vital a role do these tiny animals play in cleansing the marine sands that zoologists now say that the healthiest beaches and estuaries are those with a rich and diverse meiofaunal population. They are also particularly promising indicators of pollution since, as Higgins notes, they are in constant contact with the sediments. If those sediments are full of pollutants, the meiofaunal populations often feel the effects first. And because meiofauna are so far down the food chain, serving as the primary dinner item for shrimp, in particular, any drop in their numbers affects the many animals above them. It used to be thought that you could monitor the health of an estuary by studying the bottom- dwelling fish, says Higgins; many ecologists now think you get a better picture by keeping track of the meiofauna.
Although the day’s meiofauna hunt has not turned up any new species, Higgins is pleased to have seen a turbellarian hatch for the first time. It’s rare not to see something new, something you haven’t seen before, even in sands like these that I’ve studied many times. But it’s like I always tell people: ‘If you look where people haven’t looked before, you’ll find something new. Or if you look harder where people have looked before, you’ll find something new.’
For those hoping to catch a glimpse of this hidden world, Higgins notes that one needs only a few basic naturalist’s tools: a homemade sieve fashioned out of a nylon mesh net fastened over a funnel; a spray bottle for rinsing it out; a petri dish to place the samples in; and a stereomicroscope of at least 25 times magnification. Higgins encourages people to explore other poorly understood habitats with this gear as well, such as the moss on a river rock, or the small pools of water that form on ice fields. You’ll find animals in all of these, he says, and in some cases you’ll be the first person to see them. New animals are to be found everywhere--even, as Higgins’s colleague Kristensen recently discovered, in the filmy ooze on the back of a crab’s shell. He scraped off that film and found this strange, wormlike new animal. He’s still studying it and hasn’t named it yet; but it may very well prove to be another new phylum or at least a new class of animals, says Higgins.
None of the animals that live in such habitats will be big or sexy or bold, he admits. And they won’t solve the world’s economic problems. But we search for them because we need to know as much as we can about what is there; we need to understand the biodiversity that can exist even in the beach’s sands.
The world would, however, be a very different place without meiofauna. A beach without meiofauna would be like a forest without turkey vultures or other scavengers, says Higgins. All the dead material--fish, shellfish, seaweed--that washes up on shore would simply accumulate, and the bacteria would build up until the beach became anoxic [starved of oxygen]. Instead of a clean shore, there would be a sticky, stinking mudflat. But as the sparkling sands of that Florida beach testify, the world is not like that and meiofauna do exist--even though most of the human population never even know they are there.
