Why are there no lobsters on lands or bats at sea? The answer appears to be a biological version of beginner's luck

Geerat J. Vermeij

I can't help noticing them. With every sweaty step I take along a trail in the magnificent rainforest on Panama's Barro Colorado Island, insects of every description make their presence known. The piercing shrieks of cicadas high overhead drown out the territorial calls of birds. To one side of the trail, a pair of orchid bees, wings vibrating in a low, almost threatening pulsating buzz, engage in an elaborate aerial mating dance. The leaves of the understory shrubs, lianas, and sapling trees bear the unmistakable signs of damage by hungry insects. Some are mere skeletons of veins, all the intervening leaf tissue having been nibbled away by caterpillars. Ants burdened with loads of leaf fragments march toward their underground fungal gardens. And the insects are hardly alone. Lizards scurry in the leaf litter at my feet, monkeys feed noisily in the branches above nay head, a vine snake makes its sinuous way toward an unsuspecting small bird. Like the insects and plants, all these creatures are occupied with the business of extracting a living from the land.

Just a few miles away, on the warm rocky shores and mudflats of the Bay of Panama, life-forms are markedly different. There--where the sea has as much influence on living organisms as terra firma does--barnacles and bivalves and bryozoans filter food particles out of the water, snails and sea urchins and octopuses and crabs consume everything from decaying matter to other animals, and tiny corals and seaweeds photosynthesize on tide pool rocks.

Offshore, of course, the contrast with life on land is even greater. All photosynthesis in the sea is carried out by microscopic plants that drift near the surface and find their way up the food chain not only to such typically marine animals as sharks and squid but ultimately also to air-breathing whales and albatrosses.

That the cast of characters living on land is so different from the one inhabiting the sea is such a familiar observation that we rarely stop to ask why this is so or how the differences are maintained. Yet such everyday questions provide some of the most interesting puzzles to the naturalist, and the answers can yield deep insight into how nature works.

A little history puts the problem in perspective. All the available evidence--derived from studying the evolutionary relationships of all kinds of extinct and living organisms--indicates that plants and animals originated in the sea. Multicellular marine organisms may have existed as early as 1.7 billion years ago, and plants identifiable as red algae were certainly growing 1.2 billion years ago. When marine animals appeared remains a matter of controversy, but an estimate of 700-800 million years ago seems reasonable. By Middle Ordovician times, about 460 million years ago, fungi (the oldest recognized multicellular terrestrial organisms) had colonized the land. During the next 140 million years, other types of organisms invaded terra firma and gave rise to vascular plants, millipedes, mites, insects, spiders, scorpions, land snails, and early amphibians and reptiles.

A look at the distribution of the major groups of plants and animals alive today is instructive. (By "group," I mean a clade, an evolutionary branch consisting of an ancestor and all its descendants. A major group is a large and typically old clade, such as insects or vertebrates.) Most of these groups live either in the sea or on dry land, but not in both. A small minority occupy freshwater habitats. Very few groups have made the transition from water to land or from land back to water, and groups that have moved between marine and terrestrial habitats are especially rare. This may seem surprising, since land and sea are both so full of life, but the facts bear out the statement. Mollusks, for example, have occupied the sea for more than 500 million years--seemingly ample time to make the move--but only nine groups of snails, and no clams or cephalopods (the group containing squid and octopuses), have ventured onto dry land. With an equally long history in the sea, arthropods (a huge group of invertebrates including insects, crustaceans, and spiders) have made the transition to land at most nine times. Green plants may have done it only once. Lobsters, sea stars, corals, bryozoans, brown algae, and a host of other marine groups never made it.

Once on shore, of course, some colonizers were spectacularly successful. All the plants in your neighborhood, for example--from the loftiest tree to little spring pansies--may have evolved from a single ancestor. Groups of animals and plants that made it to land prior to about 300 million years ago were especially prolific in their new surroundings. There are now hundreds of thousands of species of insects and green plants, and tens of thousands of mites, spiders, and pulmonate land snails (those endowed with lungs). Later arrivals, such as sowbugs, crabs, hermit crabs, and some other land snail groups, have remained minor elements of the terrestrial fauna.

Having made the switch to life on land, few groups of organisms returned to the sea. No marine snails or crustaceans can claim terrestrial ancestry. Of the million or so living species of insects, only about 1,400 are marine--the result of an estimated 122 separate invasions from the land, including those involving an intermediate phase in freshwater. Most of these insects colonized the margins of the sea: places such as mangrove forests, salt marshes, tide pools, sandy beaches, clumps of washed-up seaweed, and crevices at the upper reaches of rocky shores. The only insects that make a living in the open ocean are five species of water strider, which skate across the water's surface in warm seas.

Similarly, there are some 300,000 living species of land plants, compared with only sixty truly marine species that have terrestrial ancestors. All these marine plants are sea grasses, representing three separate invasions from the land, all by way of freshwater. Rooted in sand or sandy mud, sea grasses grow offshore--near continents and large islands--in water up to sixty feet deep. Salt-tolerant mangroves and salt-marsh and beach plants evolved into an additional thirty to forty groups of land plants.

Tetrapods (four-limbed vertebrates) are striking exceptions. They have been notably successful at returning from the land to exploit marine habitats. Including extinct groups, marine tetrapods evolved from terrestrial ancestors at least thirty-five times among reptiles (turtles, crocodiles, plesiosaurs, lizards, snakes), seven times among mammals (including whales, seals, and otters, as well as the extinct New England sea mink and a bizarre marine sloth that lived some 4 million years ago in the waters off the coast of modern-day Peru), and ten times among geese and ducks, plus numerous times among other groups of birds. (This adds up to fewer than the 122 insect invasions, but taking the total number of species in both groups into account, tetrapods have made the transition far more frequently.) We humans are the latest and, although atypical, certainly the most successful land animals to exploit the sea. Even with no special physical adaptations, Homo sapiens makes use of more marine resources and penetrates the ocean more extensively--from the poles to the equator and from the high-tide line to the deepest trenches--than does any other species.

Why has such a small proportion of all living things managed evolutionary leaps between land and sea? The most obvious explanation would seem to be the differing physical demands of air and water. Gravity, for example, is a pervasive force to be reckoned with on land but is greatly reduced in water, because the density of living matter is very close to that of water. Respiration--the uptake and release of gases such as oxygen and carbon dioxide--is much faster in air than in water. These and other physical realities mean that almost every aspect of life, from taking a simple breath or eating to finding a mate, requires different, often incompatible, adaptations in the two media.

But this explanation is not sufficient. If physical differences between air and water accounted for the difficulty, transitions between land and freshwater should be just as rare as those between land and sea. But the evidence suggests otherwise. Land plants have given rise to freshwater species at least 200 times, and the 45,000 or so species of insects in freshwater lakes and streams represent hundreds of separate invasions from the land. Mammals have made the move from land to freshwater at least twenty-four times. Even more telling are the insects that have successfully colonized surf-swept lakeshores but not the shores of wave-swept seacoasts, as well as the insects that live in inland saline lakes but not in coastal marine habitats. How can some dragonflies and caddis flies live in salt lakes but not in the sea?

Politicians might not readily come to mind as sources of scientific insight, but in this case they understand the basic principle better than almost anyone else. That principle is incumbency. Physical contrasts aren't the only factor that make it difficult to shift from one environment to another; the well-adapted organisms already living there prevent invaders from gaining a foothold.

How does such incumbency work? To succeed in a new environment, an invader must be able to compete effectively with resident species, which will typically, and not surprisingly, have the upper hand because they are already well suited to both their physical and biological surroundings. Before the Middle Ordovician, dryland ecosystems were fairly simple, dominated mainly by mat-forming microbes that would have been unable to compete with larger plant and animal invaders from the sea or from freshwater. But by the later Devonian (about 350 million years ago), terrestrial ecosystems--primarily forests and the many creatures living in them--were much more complex, with established communities of incumbents capable of preventing further invasions by most groups of marine organisms.

By the Permian Period, about 260 million years ago, the invasion tables had turned. Tetrapods had achieved metabolic levels equal to and often higher than those of marine fish. (Why does this matter? Given enough food, an animal with a high metabolic rate can grow faster, gather and safeguard more resources more quickly, and devote more energy to defense, including the defense of offspring, than can an animal with a low rate. Having a faster metabolism is like having more money: you may not be able to buy happiness, but you can acquire more of the things you need and can carry out more of the essential tasks of life more effectively.) These high-powered terrestrial species still, of course, had numerous obstacles to overcome before carving out a niche for themselves in the sea, but at least by Permian times they stood a fighting chance.

Significantly, incumbents have always been less of a problem in freshwater ecosystems. Part of the reason for this may be that several important groups of marine predators--echinoderms and cephalopods, among others--are, and apparently always have been, absent from freshwater. In addition, many small bodies of freshwater, as well as inland salt lakes, lack fish and other potentially effective predators and competitors. Such safe places may therefore serve as staging areas, places to acquire and hone adaptations necessary for survival in water.

But what is it about tetrapods that has enabled them to return to a watery way of life--fresh or marine--so frequently and effectively? Unlike marine insects and other arthropods that endure submersion by taking refuge in rock crevices or in self-generated gas bubbles, once tetrapods take the plunge, they remain active. Although they may still need to come to the surface to breathe (or, as in the case of seals and seabirds, return to the land to breed), they are able to feed and carry out many of the other vital functions of life in their adopted medium. Perhaps in the distant past the newcomers, with their revved-up metabolism, thrived because the relatively sluggish incumbents--crustaceans, echinoderms, mollusks, and many fish--offered little resistance. Today the descendants of the invaders often occupy dominant positions in marine ecosystems. Depending on the species, whales are either major consumers of plankton or krill or they are major predators, feeding on seals, fish, and penguins. Seals and marine birds are also carnivores that dine at or near the top of the food chain (as did the extinct marine reptiles). Green sea turtles and sea cows are herbivores with large appetites, as was the Peruvian sloth, presumably. (Even among tetrapods, however, lineages that returned to the sea form a small minority. There are, for example, no marine bats, hoofed mammals, parrots, or songbirds.)

Issues of incumbency may also explain why carrying out a successful invasion of land from the sea is difficult. Most organisms in a position to make the attempt are like periwinkles and other shore snails--creatures that, when exposed to the air at low tide, spend long hours waiting passively behind closed doors until the tide returns. Only then can they begin feeding and moving around again. Such creatures are unlikely to compete successfully for resources with birds that energetically race around on the mudflats in search of nutritious tidbits or with raccoons that come to the water's edge to forage for food. Most of the more recent success stories involve snails, isopods, and other marine animals that have colonized leaf litter or remained in environments close to the seashore. One of the more notable recent invaders is the large coconut crab (Birgus latro), a hermit crab restricted to islands in the Pacific and Indian Oceans. Large and aggressive, as well as powerful when its shell is hard, this animal is defenseless when molting and would be an easy target for hungry ground-dwelling mammals. It may owe its success to the rarity or absence of major carnivorous vertebrates on islands.

Of course, incumbents and invaders don't live in a vacuum. Both are affected, often dramatically, by external forces, some of which may help topple an incumbent that would otherwise have been able to stand its ground. In nature, there is no such thing as a term limit for incumbents, but they are vulnerable nonetheless. Being well-adjusted to the status quo can be a liability if that adjustment comes at the cost of flexibility. Incumbents often prove to be most at risk during times of major disturbance, such as a sudden change in climate. The disturbance, together with pressure from predators and competitors, may enable upstart, imperfectly adapted invaders to gain a beachhead in a foreign place.

The principle of incumbency is widely applicable in biology and has important implications for our own relationships with the rest of the biosphere. By destroying or modifying most of the world's ecosystems and by exploiting most of the competitively superior animals and plants on land as well as in the sea, we humans are eliminating incumbents. This makes it even easier for the remaining species (many of which are often disparaged, perhaps unfairly, as "weeds" because of their ability to adapt to life in the disturbed environments we have fashioned) to spread to new habitats or regions. Now that humans are the most powerful of all incumbents, let's hope that we can govern wisely and compassionately.

Geerat J. Vermeij ("Why Are There No Lobsters on Land or Bats at Sea?" page 60) is a professor of geology at the University of California, Davis. Mollusks, living and extinct, are his first love. Praising their manageable size, varied textures, and great diversity, he says that "shells have just about everything a scientist could want." In 2000, Vermeij received the Daniel Giraud Elliot Medal from the National Academy of Sciences for "extracting major generalizations about biological evolution from the fossil record, by feeling details of shell anatomy that other scientists only see." Blind from age three, he is the author of A Natural History of Shells (Princeton University Press) and the autobiographical Privileged Hands: A Scientific Life (W. H. Freeman).

COPYRIGHT 2002 Natural History Magazine, Inc.
COPYRIGHT 2008 Gale, Cengage Learning