We live on a planet graced with many diverse ecosystems. Variety can be found at many sites, and at many spatial scales. We can enter a forest and look at the leaves on a branch and the insects feeding on that branch. We can also study the tree itself, or a stand of trees. Similarly, we can study biodiversity at the level of the local landscape, whether forest or prairie. Diversity at this scale has been called alpha diversity. In contrast, diversity over larger regions has been called gamma diversity. In this chapter, we will be considering how diversity is maintained at the local, or alpha, scale.
Many local biomes support large numbers of plants and animals living together, in what appear to be stable communities. Whether we are speaking of a tundra-like mountain top, a deciduous forest, or tropical evergreen forest, hundreds of species live together over what appears to have been thousands of years. This confronts us with some serious questions. Why haven't a few dominating species wiped out most all the others? Why hasn't the world's greenery been devoured by hungry herbivores? These questions have been central issues in ecology over many decades, and a variety of ideas have been put forward to understand the marvel of continuing local diversity.
THE CONCEPT OF THE NICHE
For zoologists, an answer to the puzzle of animal diversity has been the concept of the niche. Each species, it is assumed, has its own specific niche: an environment or lifestyle in which that species is most comfortable and most successful. Recall the two species of lice living on humans. One prefers to live amongst the hairs of our head; the other, apparently, requires the greater warmth and moisture of our private parts. By specializing on these very specific niches, two lice species share a larger environment (our hairy parts) without getting in each other's way. Similarly, four species of Hispine beetles feed on Heliconia latispatha plants in Costa Rica, but each species feeds on different parts of the plant.1 (Heliconia is the banana-like genus with “lobster claw” inflorescences we see in floral arrangements.) These beetles are related species, living on the same host but with slightly different feeding preferences. We call this niche division.
On the savannas of Africa, we can witness a clear separation of hunting niches among the larger mammals. Here, lions are the largest carnivores, fully twice the weight of a leopard. Hunting in packs, they can bring down the largest herbivores, even elephants. The next smaller guild of carnivores includes leopards, cheetahs, hyenas, and hunting dogs. Each of these species hunt in a distinctly different way. Hyenas and leopards hunt mostly at night, hyenas hunt in groups and also scavenge, while leopards are mostly solitary and can climb trees to pursue monkeys. Packs of hunting dogs and solitary cheetahs hunt on the open grassy plains during the light of day. Using speed, cheetahs run down their prey; using relays, hunting dogs wear down their prey. Smaller carnivores also share this same landscape: the coyote-like jackal, the feline serval, and several species of mongoose. The desert cat of Africa is about the size of our domestic cat. Living in a dry environment with few prey, the desert cat is a solitary hunter. Like many other desert mammals, the desert cat conserves moisture by being active only in the cool of night. Clearly, Africa's carnivores achieve their diversity by coming in a variety of sizes and using different hunting strategies.
Ecologists tried to embellish the concept of the niche with precise and imaginative qualities. Every animal species, they proclaimed, has a “fundamental niche” in which that species prospers. Two species with the same fundamental niche must inevitably compete, they declared, with one eliminating the other. Others proclaimed that the niche existed as a “multidimensional hypervolume bounded by the species’ tolerance factors for many different environmental factors.”2 Popular in the 1970s, these discussions produced few insights, nor did they help us understand plant life.
PLANTS AND THEIR NICHES
Botanists, in particular, had problems with the niche concept. Green plants all use the same basic resources—sunlight, water, and carbon dioxide—to build their tissues. Also, many species seem to grow together amicably, and it is often difficult to see where their niches differ. Ecologist P. J. Grubb suggested that, for plants, we should consider four component niches.3 First is the habitat niche: the particular ecological factors necessary to each species. The second is the life-form niche: the size, three dimensional structure, and annual productivity of each species. The third is the phenological niche: determining the timing of seasonal growth, flowering, and fruiting of each plant species. Finally, the regeneration niche determines how the species replaces itself in the landscape.
Careful analyses of tree distributions within three neotropical rain forests recently discovered that about 40 percent of the species were associated with specific soil qualities. This study examined 1,400 tree species and ten essential soil nutrients in Panama, Colombia, and Ecuador. Even though most of the trees appeared to be similar in habitat preference, more than a third of the species had germinated in soil with specific nutrient characteristics.4 Here is an aspect of their habitat niche we hadn't been aware of earlier. Similarly, though altitude proved to be the most important factor determining local tree diversity in Borneo, soil characteristics were also significant.5
Surely, one of the easiest ways to pack more species into a single habitat is by varying their sizes. Little cats, whether on the savanna or in the desert, are busy looking for little rodents; they are not competing with either lions or leopards. Also, cats are much too large to make insects an important item in their diets; bugs don't contain a lot of energy. Smaller mammals, predatory insects, and nimble little birds are the primary hunters of insects. And just as there are advantages to being large, there are advantages to being small. Smaller animals can accelerate quickly, manoeuver nimbly, and find many places to hide.6 Best of all, they don't need a lot of food to keep themselves going. Similarly, little plants can live in places where the big ones can't. Epiphytes are a fine example. Leafy liverworts, small ferns, and orchids less than ten centimeters (four inches) tall can festoon the branches of trees in misty cloud forests. In deserts, short-lived ephemerals can sprout, flower, and fruit in a rainy season of only two months. For any species, size at maturity plays a big part of determining its role in the environment: the life-form niche.
Even when the same size, similar species can share the same landscape by timing their life activities differently: the phenological niche. A colorful example of differential timing can be seen in our Midwestern prairies. After a long and cold winter, growth on the prairie begins in early May. The first to flower are small plants, less than a foot (30 cm) high. These include lousewort, Indian paintbrush, toadflax, Hypoxis, and the white lady slipper. By June there's been more time to grow, and plants are two to three feet (60–90 cm) tall. These include golden Alexanders, the pink pasture rose, bluish lupines, and spiderworts. In early July, the prairie is in full flowering mode. This is when phlox, wild quinine, leadplant, prairie coreopsis, wild lilies, and many others are blooming. In August there are broad swaths of brilliant purple blazing star across the prairie, while flowering spurge sprinkles the view with little white inflorescences and early goldenrod adds a dash of yellow to the show. In August, and after sufficient rainfall, taller species reach over six feet (180 cm) high. By September, brilliantly yellow goldenrod species are going full blast, complemented by white and bluish asters and, hidden in the undergrowth, the elegant gentians. All the while, the less colorful—wind-pollinated—grasses and sedges have also gone through their species-specific sequence of flowering.
A prairie is rather like a grand stage on which different groups of dancers replace each other as the flowering season progresses. Perhaps this is more than the random seasonality of different species. If pollinators are in limited supply, sequential flowering reduces competition for pollinators, allowing more species to share the landscape. By avoiding competition through lifestyle adjustments, niche differentiation helps maintain local species richness throughout the world.
PLANT SUCCESSION
There's another important way in which plants divide the landscape along the gradient of time, but this is not within the cadence of a single year. Rip off the side of a mountain with a landslide, or scour a flood plain with a nasty flood, and you have bare land. Smaller weedy species can prosper in this open, sunny, windswept setting. These plants must be able to disperse their disseminules far and wide in order to “find” open space, and then grow quickly. Called plant pioneers, they are the first to colonize open ground. Once a short cover of greenery is in place, other seeds can settle in and produce taller plants. After a few years, the vegetation becomes tall enough and dense enough for the seeds of shade-loving trees to germinate and begin their lives. This process is called plant succession: the gradual transformation of bare ground to pioneering weeds and seedlings, then young forest and, finally, mature tall forest (where the rainfall is sufficient). In a sense, the pioneer plants prepare the site for the secondary invaders and these, in turn, set the stage for developing a “mature” vegetation.
After disruption and calamity, plant succession rebuilds the local vegetation. Insight into this process is evident at Peru's Manu National Park. Situated on the eastern flank of the Andes, and as these mountains continue to rise, the Manu River gradually gains in elevation, and its flood plain shifts. (The Andes Mountains are said to be rising “about as fast as your fingernails grow.”) Consequently, older terraces are found along one side of the Manu River, as the river slowly moves eastward in response to increasing elevation. Because the shifting river is moving in only one direction, researchers can compare both younger and older floodplain forests adjacent to the river. Weeds and grasses are the first to colonize the river's edge. Soon, Ceiba and Cecropia trees, together with other early pioneers, begin their lives in the open sunlit greenery along the river's edge. As they begin to form a canopy, a new forest grows around them, reaching a stature of about 100 feet (30 m) within a hundred years. Plant succession has demonstrated what it can do with bare ground, and it doesn't stop there.
After two hundred years, this same tall forest exhibits the full grandeur we expect, rich in large, thick-trunked trees and vining woody lianas. By three hundred years, however, the early pioneers are collapsing; the forest is losing its stature. And by five hundred years, forest structure has changed dramatically. Most all of the early giants are gone, replaced by tall and spindly younger trees. Forest dynamics may have made a mess of the forest, but it has become an extravagant mess, richer in species with the passing of time.7
LIFE-HISTORY STRATEGIES
The temporal sequence of vegetation succession introduces us to another important niche dimension: life span. The little weed growing at the edge of a tropical river may be able to flower and produce seeds within two months. On that same river bank, a young Ceiba seedling may have just begun its life trajectory. If this plant can survive the tribulations of its riverside home, it may become a forest giant, producing flowers and fruits for over two hundred years. Some plants live quickly and die young; others bide their time, waiting decades before producing flowers and seeds. Dayflies may have only a few hours for their reproductive maturity, while elephants live for more than half a century. Biologists who study differing lifestyles call their subject life-history strategies.8
An especially revealing comparison focused on rabbits and small monkeys. Here we had two mammalian species of the same body mass, yet living very different lives. Rabbit females produce more offspring more often than do monkeys of similar weight. Fundamentally, rabbits aren't very smart, but they're cheap to build. Baby rabbits do not require as much energy and mothering as do baby monkeys. The reason is simple; rabbits have brains only half the size of monkeys of similar weight. Brains are expensive, requiring a lot of energy in construction, nurturing, and ongoing maintenance. With smaller brains, rabbit mothers have larger litters more often. The little monkeys give birth to only one or two babies, and these babies take much longer to mature. Especially significant in this comparison is life span. On average, these monkeys live more than twice as long as the rabbits! For the monkeys, a lower reproductive rate finds compensation in a longer life trajectory. Clever monkeys, living in treetops, produce fewer but smarter babies, and live a longer life. Rabbits have more babies more often, but with a shorter life span. Forged by natural selection, both strategies have proven successful over time.
How might natural selection have determined the length of life, both for us and all other species? The logic is quite simple. Once we—or any other species—reach an age where we no longer contribute to the well-being of our offspring, natural selection no longer applies. For example, if we carry genes that shorten our early lives and keep us from provisioning our children, those children are less likely to survive. Consequently, genes causing early-onset disease are less likely to be carried into the next generation. That's strong negative selection. However, if we carry genes making us susceptible to diseases when we are in our seventies and no longer helping our children or their children, such genes are invisible to natural selection! If the late-acting genes have no effect on the success of further generations there is no way they can be subject to positive selection! And thus we, and all the other species on this planet, are stuck with a life span appropriate to our lifestyle and our niche.
TROPHIC LEVELS
Niche differentiation can also be viewed from a broader perspective: that of trophic levels in the ecosystem. Here we have a pyramid of species, the base of which is made up by the primary producers—mostly green plants using sunlight to build new tissues. The next trophic level is that of herbivores, or primary consumers: species feeding directly on the greenery. The next level is made up of those species that feed directly on the herbivores; this crowd of secondary consumers includes carnivores, insectivores, and others. Finally, a third trophic level of parasites and pathogens feeds on all trophic levels. In addition, a large number of organisms consume dead organic matter; these include bacteria, fungi, and a variety of small animals. Taken together, these trophic levels form a pyramid, with each higher level having less biomass than those they feed on, since there is energy loss as one moves up the food chain. Nevertheless, higher tropic levels may have many more species than lower levels, as when many little herbivores are feasting on a single large tree.
Unfortunately, being at the top of the trophic pyramid can be precarious, as occurred when American populations of bald eagles collapsed. Aquatic plants had absorbed the insecticide DDT from water draining agricultural fields, and following mosquito-control operations. Little fish fed on these aquatic plants and accumulated DDT in their fatty tissues. Larger fish ate the little fish and further amplified DDT residues. Bald eagles, feeding on the larger fish, inevitably acquired high concentrations of DDT—and their reproduction fell drastically. Other raptors suffered similarly, making clear that DDT use had to be curtailed. Everyone had thought that pesticides would simply diffuse into the landscape and, to all intents and purposes, disappear. DDT contradicted this assumption, showing that physiological processes could sequester such chemicals, and the food chain could concentrate them, in a process called biomagnification or bioaccumulation. We humans are vulnerable to this same process with mercury, arsenic, lead, and cadmium, as we burn fossil fuels and mine for gold.
Niche division, together with a pyramid of trophic levels, gives rise to complex interconnected food webs. A recent study of aphids illustrates some of the complexities within a simple food web. Aphids are small (1–4 mm) insects that suck sap from herbaceous plant stems. You often find a cluster of aphids, busy sucking on a weedy stem, attended by ants. Since plant sap is deficient in some nutrients essential for aphid growth and survival, aphids have a problem. One solution is sucking up a lot of sap and sending most of it out their rear ends—while extracting the special nutrients they need. Because the sap they expel is rich in sugars, ants often tend and protect the aphids to get the sugary exudate. But aphids attract parasites as well as protectors. Little parasitic wasps attacking aphids are called parasitoids. The wasp injects an egg into the body of the aphid; this egg becomes a larva feeding on the insides of the doomed aphid, finally pupating and emerging as a new wasp. But things aren't really that simple. The parasitic wasps are themselves parasitized! These secondary parasitoids—also little wasps—come in two strategies: those that parasitize the primary parasitoid larva, and those that parasitize the parasitoid pupa. And that's not all—the host plants play a role as well. Using brussels sprouts and their wild relative Brassica oleracea, together with two aphid species and a number of parasitoids, this study showed how the quality of the host plants affected the numbers and diversity within this little network. Here the two species of aphids were subjected to five species of primary parasitoids, and these to ten species of secondary parasitoids. The result of these experiments was clear: the quality of the primary food affected the numbers and diversity in the aphid-parasitoid system. Turns out, the wild plants supported more aphids and a more diverse parasitoid community than did the brussels sprouts.9 Since this study included only two plant hosts and two herbivorous species, imagine what's going on in rain forests!
DISRUPTION AND DIVERSITY
Niche differentiation may help us understand local species diversity, but it does not deal with the question we asked earlier: Why haven't superior competitors taken over the landscape? How is local diversity maintained over time? Why are there three hundred co-occurring tree species in some tropical rain forests? To answer these questions, biologists have looked at environmental variables that disturb the status-quo. These come in two general classes: physical phenomena such as storms, drought, and earthquakes; or biological factors such as predators, parasites, and pathogens. Let's begin with the physical.
While most tree species in a tropical rain forest are scattered about, it was discovered that some species were found in close groups. Not only were they the same species, they were the same age. For some clumps, the reason was easy to see. There was evidence of a landslide or large tree fall, with seeds or saplings of the clumped trees having been in the right place at just the right time to take advantage of the new clearing. Plants need sunlight for growth, and sunlight is in short supply on the floor of the rain forest. Any disturbance that allows more light to enter through a gap in the canopy will change the dynamics of the understory. In fact, some understory species are specialists on particular gap sizes. Three species of understory palms were studied in Costa Rica; all are specialists on a particular size of light gap. Too small a gap, and the palms do not have enough light to survive, but if the gap is too large other species overgrow them.10 This is niche specialization for a very particular kind of forest disturbance. How might these palms manage to find the right tree gap, you ask? By producing a multitude of seeds and having a few of these many seeds germinate in just the right spot.
Whether the collapse of a giant forest tree, a river changing its course, or landslides opening new space, such processes disturb the status quo, allowing new immigrants to gain a foothold and begin their life trajectory. Driving through Central America, we were annoyed by the landslides delaying our progress along the Inter-American Highway. At first, I had thought: “Lousy engineers!” But after a few years of field work it became clear: the roads and the engineers weren't the problem, it was the mountains! These young, unstable mountains are constantly collapsing and producing landslides. In Central America, in the Andes, and along mountains round the world, ongoing geological uplift has created elevated highlands with steep unconsolidated soils. Throw in earthquakes, and you've got an unstable geology constantly opening up new ground, supporting high species turnover, and high species richness. Thank you, plate tectonics!
Physical disturbance is usually random; landslides, storms, or sudden tree-falls are a matter of chance. Most plants deal with this problem by constantly dispersing seeds; hopeful (so to speak) that a few will find themselves in an appropriate site. Some species play a waiting game. In carefully monitored Malaysian forests, it was observed that some immature understory trees, around thirty feet (10 m) tall, remained at that height over more than twenty years. Failing to grow further, these trees did not flower or fruit; they seemed to have a “wait-and-hope” strategy. If a nearby canopy tree does come down, our waiting tree will have the illumination needed to grow into the canopy where it can flower and fruit. Surely, unpredictable disruption is a major factor in supporting the species richness of many habitats, even allowing the lucky seed from a new species to join a plant community that is already populated by hundreds of other species! In a review of their studies of tree dynamics at Barro Colorado Island in Panama, Stephen Hubbell and Robin Foster concluded that “chance and biological uncertainty may play a major role in shaping the population biology and community ecology of tropical tree communities.”11
Unpredictable variation in weather is another disruptive force helping keep plant communities diverse. One of the surprises of visiting our Midwestern prairies is how different they can appear from year to year. And it is not just rainfall; the severity and length of the previous winter can play a role. A very dry spring can alter the growth and flowering of different species. A good year for one species may be a bad year for another. For plants, the ability to produce seeds will rise and fall with varying environmental conditions. A recent prairie study in Kansas showed how inter-annual climate variability contributed to the coexistence of three very similar grass species. Seed storage in the soil, together with the overlap of generations—and climate variability—prevented any one of these grass species from dominating the landscape.12
Another important factor in our Midwestern prairies is fire! After witnessing a brilliant display of prairie flowering, I decided to share this phenomenon with friends. The following year, I filled my car with visitors and drove off to see the flowering extravaganza at the same prairie and the same time as the year before. Sad to say, but the flowering extravaganza wasn't there. There were flowers, of course, but nothing like the profusion of the previous year. My “Flower Tour” had nowhere near the impact that I'd been hoping for. Robert Betz, having studied these prairies over many years, noted that fires played a major role in the intensity of floral displays. When many nutrients are returned to the soil after a burn, the following summer is likely to produce a burst of flowering and fruiting. Similarly, fire is an important dynamic in many seasonally dry biomes around the world.
Moderate disruption is an important factor in maintaining local species richness. Of course, we need to distinguish moderate from severe disruption. Forests in Southeast Asia that are regularly subjected to destructive typhoons do not have as many tree species as forests outside the paths of these powerful storms. Similarly, a long cold winter or many months of drought are challenges only well-adapted species can survive.13
DIVERSITY PROMOTERS: PREDATORS, PARASITES, AND PATHOGENS
In addition to physical disruptions maintaining species richness, there are biological factors as well. After studying bruchid beetles in Central American lowland forests for many years, Daniel Janzen suggested that these beetles had a definite effect on the distribution of their host trees. Bruchids feed on the seeds of specific species of leguminous trees and are most numerous under such trees, “waiting” for fruit to ripen and seeds to fall. The beetles and their larvae feast upon the fallen seeds and destroy the seeds’ ability to germinate. It was from such observations that Janzen and others proposed survival and regrowth of seeds to be inversely proportional to the distance from their mother tree. Seed survival and growth was more likely further from the mother tree.14 Others have found that seedlings near a parent tree die off more readily than those more distant, because of pathogenic fungi in the soil surrounding the mother tree. Indeed, some tree species exhibit a so-called “hyperdispersed” pattern of occurrence within the forest.
But things aren't that simple. Seed-eating rodents, busy on the forest floor, seek out infested seeds with tasty grubs inside, adding another element to the story of seed success. Unlike the “clumped trees” we mentioned earlier, these trees of the same species simply don't grow near each other. Unfortunately, the seed predation hypothesis explains the distribution patterns of some species but not a whole lot of other species.15 Nevertheless, specialized predators and pathogens can keep their host species from becoming too numerous. Even grazing animals can help maintain diversity. Careful studies in English meadowlands have shown that meadows grazed by sheep had twice as many plant species as those same meadows in the absence of grazing!
And there's more: competitive relationships are dynamic. We are all aware of the effect of predators on their prey, and we see the effects of arms races in many aspects of the living world. Horses are larger and run much faster today than their smaller ancestors of fifty million years ago. Many lineages of plants have developed specific toxins to defend themselves from herbivores. Though most herbivores cannot survive specific poisons, a few lineages have the ability to sequester the poison from the plant on which they feed, becoming poisonous themselves! Milkweed plants and monarch butterflies have such a relationship. Monarch caterpillars are one of only a few insect lineages that can feed on milkweeds (Asclepias spp.). Thanks to ingesting and sequestering the plant's toxin, both the monarch caterpillar and butterfly are quite poisonous, and both have distinctive, easily recognized colors. Over time, birds have developed the inherited wisdom to keep these butterflies and their caterpillars off their menu.
Plants of the rainforest and prairie may look like a pleasant arrangement of greenery, but they are much more than that. As in the milkweed example, plants are a veritable zoo of defensive chemistry. Cocaine in the coca leaf, caffeine in the coffee bean, morphine in the fruit wall of the opium poppy, and pungent aromatic oils in the mint family—all are defensive armaments against herbivory. Indigenous vegetation in New Zealand has no plants poisonous to mammals because non-flying mammals were absent in New Zealand before the arrival of humans. Over many millions of years there simply was no need for mammal-repelling toxins in mammal-free New Zealand.
An important way of avoiding predation for animals is to hide. This is one reason for being active only in the dark of night. Beetles are clumsy fliers; they fly at night to avoid more agile birds. A majority of mammals restrict their activities to the cover of night. Another way of avoiding your predators is to mimic your surroundings. Grasshoppers look like blades of grass; many caterpillars stop when disturbed and appear to be a dead twig; moths fold their wings and mimic bark or fallen leaves; all are difficult to see. These creatures are the products of selection—deceiving the keen eyes of those who would devour them. Mimicry takes other forms as well. There are tropical moths that resemble stinging wasps; caterpillars with two large eyespots at their ends to look like little snakes, and brightly colored orange butterflies that look just like brightly orange poisonous butterflies. These many mimics bear graphic witness to the dangers of the world in which they live.
ENEMIES OF ENEMIES ARE FRIENDS
For plants, predators of herbivores are friends! A very dramatic example of predator effects on vegetation came with the reintroduction of wolves into Yellowstone National Park. By 1926, wolves had been exterminated in the park, with herbivore populations, especially elk, rising to new levels. Quickly browse species, such as cottonwood, aspen, willows, and berry-producing shrubs declined. And though coyotes, bears, and cougars were present in the park, they were not sufficient to constrain elk numbers (which had to be culled over the years). With reintroduction of thirty-one wolves during the winter of 1995/1996, the scenery began to change! Cottonwoods and willows in the Lamar Valley were now growing six to twelve feet high, instead of being continuously browsed down to three feet. Regrowth was especially strong near streams, where denser vegetation made it easier for wolves to hide and ambush their prey.
Smart elk were changing their browsing patterns, staying clear of denser growth where wolves might lurk. Soon the landscape began to resemble photographs taken in the early 1900s.16 Yellowstone clearly demonstrated how top carnivores can help maintain higher levels of plant growth. All told, a dynamic habitat with a variety of predators supports greater plant species numbers. However, while large carnivores are highly visible factors in environmental dynamics, there are also many less visible “predators.”
Sad to say, but the natural world is rich in smaller, often invisible, microbial parasites and pathogens. Such agents, from viruses to microbes and slender worms, all play a role in maintaining biodiversity. These deadly adversaries regulate the numbers of both animals and plants, and they are often constrained by simple physical parameters. If their hosts are numerous and crowded, the pathogens have little difficulty spreading to new hosts, causing epidemics. If the host species is rare or scattered, infection is less likely, and the parasite must bide its time. Here again, we have density-dependent factors keeping population numbers in check. This same process constrained human numbers before modern medicine. More important, pathogens sustain biodiversity by giving rare species a slightly better chance of reproducing successfully than their more common neighbors.
Young plants and animals are especially vulnerable to disease. In a study of tree seedlings on Barro Colorado Island, it was found that fungal diseases killed many of the little plantlets during their first year of life.17 Earlier, we discusses how sexual reproduction kept a species’ genetic resources in constant flux. In fact, incessant genetic shuffling by sexual reproduction may be the only way to deal with the challenge of parasites and pathogens. Sexually reproducing populations, by remaining constantly variable, give pathogens and parasites a less uniform target. And though we may abhor disease and pestilence (as well as storm and flood), all these factors are vital to maintaining rich and diverse ecosystems. Nevertheless, Mother Nature also has positive ways of sustaining biodiversity.
WHEN COOPERATION PROMOTES BIODIVERSITY
The notion that cooperation between different species might be a potent force in maintaining biodiversity has always been met with skepticism. After all, natural selection is supposed to work on the reproductive effectiveness of individual plants and animals. If that's true, how can helping others be a product of natural selection? Perhaps, the cooperation we see so prominently in nature originated independently in the cooperating partners. Ancient flowers, visited by pollen-eating beetles, may have reproduced more effectively than flowers not visited. Later, adding colorful petals, nectar and aroma attracted a greater variety of insects. Slowly, there developed a loosely symbiotic system, with insects finding food as plants were being cross-pollinated more effectively. These plants and animals had simply been maximizing their own benefits independently, before becoming enmeshed in a mutually beneficial syndrome. Regardless of who has benefited more in these interactions, the results have been hugely important in the evolution of more diverse ecosystems.
Animal pollination is the primary reason that tropical rain forests can support as many as three hundred species of trees in the same small area. Wind pollination can be effective, as we see in our oak woodlands, among savanna grasses, and in conifer forests around the world. However, it is effective when plant species are surrounded by many others of their own kind. Wind pollination is not very effective for isolated plants, such as in a tropical rain forest. Sentient animals can seek and find plants of the same species over long distances. Without sentient pollinators, a rain forest with hundreds of co-occurring flowering plant species would be impossible.
Insects serve only those plants that attract their attention, provide them with somewhere to land when they arrive, guide them in the direction they should go and reward them for their efforts.
—Peter Thompson18
But why might a pollinating insect search for the flowers of another plant of the same species? Actually, the underlying logic is simple: conserve energy! Why spend time trying to figure out how to suck nectar out of a new and different flower when you've just tanked up from a nice purple-and-yellow one? The strategy is clear: “That was good, let's find another purple-and-yellow flower.” Even little insect brains can follow this protocol, resulting in what we call pollinator fidelity. In this way, pollinators tend to move between flowers of the same plant species. When the purple-and-yellow flowers run dry, the insect will initiate a new search.
The “loose symbiosis” of flowers and their animal pollinators has given rise to varying degrees of specific dependency. The bee family, with 20,000 species, is especially important. Bees are the only insect family feeding their young nectar and pollen. That's why you see honey bees and bumblebees visiting flowers so frequently. They are not just filling their own gas tanks, they are gathering sustenance for their little ones! And it's not just insects. Birds can also serve as pollinators, often attracted to bright red flowers. A signature feature of the New World tropics is the presence of bright red flowers with narrow floral tubes, and no landing sites! You will not find similar flowers among the native plants of the Old World. The reason is simple: hummingbirds are exclusive to the Americas. Because these little birds can hover in midair, they do not need a place to alight while sipping nectar. Pollinating birds in Africa, Asia, and Australia visit bright red flowers provided with nearby perches from which they sip nectar. No need for perches in flowers visited by hummingbirds. An estimated 8,000 species of flowering plants, in dozens of families, have evolved flowers specifically adapted to hummingbird pollination in the neotropics.
FIGS AND THEIR FIG-WASPS
An extreme—completely interdependent—pollination symbiosis is that of fig trees and their pollinating wasps. The fig tree's little flowers are enclosed within the spherical or urn-like fig. Though it looks like a fruit, the fig is actually a hollow inflorescence, with all its little flowers inside. Tightly overlapping bracts, covering the entry at the top of the fig, require that the flat-headed fig-wasp squeeze her way through this obstruction to enter the interior of the fig, usually losing her wings in the process. Once inside, she moves around among the female flowers of the fig with pollen collected from the fig in which she was born, thus effecting pollination. After laying eggs in many gall flowers, where her young will develop, her life will be complete. Once the wasp larvae have fed, matured, and pupated inside the gall flowers, blind and wingless males are the first to emerge. These raunchy fellows proceed to mate with the females, still trapped within their gall flowers. The males then get together and chew a passageway through the thick wall of the fig. Fresh air from this new opening activates the females, who emerge from their galls, gather pollen into special “pockets” alongside their abdomen, then leave by the exit the males have fashioned. The females must then fly to a fig tree that is both the correct species and whose figs are ready for pollination. This elaborate symbiosis includes three different types of flowers inside the fig. The female flowers come in two forms: the gall flowers in which the wasp larvae will develop and fertile female flowers, which will produce seeds. The third group are male flowers, producing pollen for transport by the female wasps. Soon after the female wasps leave, the fig becomes sweet and succulent, with seeds ready for dispersal by birds, bats, monkeys, and others.
Fig-wasps cannot develop or mate outside of the fig, and fig trees cannot produce seeds without the pollination services of the wasps. This is an obligate mutualism, a tightly constrained relationship essential to both members of the association. One might expect such a completely dependent mutualism to be risky business. If either partner goes extinct, so does the other. Indeed, the fig-tree/fig-wasp mutualism is one of only a very few such tightly integrated relationships, among tens of thousands of flowering plant genera. Nevertheless, the fig genus (Ficus in the mulberry family) is one of the most successful tree genera on the planet, numbering around seven hundred species. Fig trees have an advantage: they do not have to compete with other plants for pollinators. They've got their very own!19 And there's more: To keep themselves and their wasps going, fig trees fruit throughout the year in evergreen tropical forests. This means that fruiting figs are usually available as food throughout the year, even during the dry season when other fruits are scarce. Consequently, figs are a major source of nourishment for monkeys during the dry season in Peru's Manu Park.20 In this same forest, a single fig tree bearing an estimated 200,000 mature figs was monitored for twenty days. During this time, forty-eight species of birds and monkeys were recorded feeding at the tree during daylight hours. Considering how many bats and other creatures might come to feed at night, you can understand why fig trees often serve as keystone species, critical to the welfare of many other members of the forest community.
OTHER SYMBIOTIC ASSOCIATIONS
Ants, in particular, have developed many cooperative arrangements with plants. Small ants inhabit stems and leaf stalks in a few Central American species of Piper and small trees of the laurel family. These plants afford enclosed spaces that house the little ants. In return, the ants bring organic matter into the plant, supplementing the plant's nutrition.21 Much more impressive are those plants that host a police force of larger, nasty, biting or stinging ants. Mess with these plants and you are met with a phalanx of little warriors ready to do battle. That's the good news; the bad news is that armies are expensive. Ant-plants must provide both housing and food for their defenders. The tree genus Acacia (in a wide sense) contains a few species, both in Africa and the American tropics that display this unusual mutualism. Cecropia trees, common in lowland wet forests of the Americas, support an army of stinging ants in distal hollow stems; only slow-moving sloths feed on these distinctive plants. After cutting down a slender Cecropia tree in Costa Rica to collect foliage and inflorescences, I stepped back and waited. I expected the ants to run over my boots and bite my legs, where I would pick them off. Unfortunately, these little beasts ran up my legs with such speed and determination that they didn't slow down to bite until they had reached a very tender region. I've never made that mistake again.
Another important symbiotic system resembles what we call agriculture. Both termites and some ant species fashion special chambers where they cultivate fungi upon which they feed. The leaf-cutting ants of the Americas bring leaf fragments down from high trees to provision their underground fungal colonies.22 Tropical savanna termites keep their underground chambers cool by building hollow spires of dried mud high above the ground, allowing air to circulate within the colony. Because they concentrate nutrients and rework the soil, both termite mounds and leaf-cutter nests play an important role in many ecosystems.
Recent DNA surveys have given us a better understanding of a symbiosis critical to the lives of many animals. These are microbes within the alimentary canal that help digest food and form feces. Among larger animals, it is the ruminant ungulates (cows, buffalo, antelope, deer, goats, sheep, etc.) that have the most elaborate digestive systems. These animals have a four-part stomach in which chewed plant food is digested, regurgitated, re-chewed, and further processed along the alimentary canal before it is expelled. Bacteria, amoeba, and fungi are part of this digestive system, allowing these animals to make cellulose a part of their diet!
Even the little laboratory fruit fly (Drosophila melanogaster) has a number of bacterial species helping digest its food. These commensal bacteria are especially important to the fly's survival during times of food scarcity. We ourselves have a huge entourage of digestive assistants. Genomic screenings estimate that several hundred kinds of bacteria, numbering in the trillions, inhabit our alimentary canal, help digest our food, provide a few essential vitamins, and even defend us against diseases. This “symbiotic human microbiome” is critical to our own good health.23
Unfortunately, cooperation can also produce trouble. A nasty fungal disease of rice includes a bacterium living within the fungus. This bacterium produces a toxin (rhizoxin), killing the rice plant upon which the fungus then feeds. Thanks to its bacterial partner, this fungus can devastate one of our most important food crops. Another recent discovery involves a three-way partnership in a tropical panic grass. But this relationship is beneficial to the grass. Here a fungus, infested with a virus and living within the grass, confers greater heat-tolerance to the grass.24
On a larger scale, the most important symbiosis in terrestrial ecosystems is that of specific soil fungi joining with the roots of plants, called Mycorrhizae (fungus-roots; singular: mycorrhiza). In these symbioses, specific soil fungi attach their tissues to the outer cells of plant roots (Ectomycorrhizae), while other smaller fungi actually enter into the root tissue itself (Endomycorrhizae). Connected in this way, plant and fungus can exchange soil nutrients, water, and sugars. Fungi are especially good at absorbing available nitrogen and phosphorus from the soil, and they can transmit these elements to the root. Thanks to photosynthesis, the plant produces sugars in abundance, and these are available to the fungus through the mycorrhizal connection. Providing essential nutrients to the plant and energy-rich sugars to the fungus; this relationship is thought to benefit 80 percent to 90 percent of land plants. In fact, this symbiosis may have begun over four hundred million years ago, when plants were first establishing themselves on land.
Though not symbiotic, many fungi are critical in breaking down woody tissues and returning vital nutrients to the soil. Whether detritovores, pathogens, or symbionts, fungi are essential in sustaining healthy ecosystems. In addition, a few fungi have developed a very distinctive symbiosis, allowing them to live in even the Earth's most severe polar environments.
LICHENS: GLOBALLY SUCCESSFUL MUTUALISTS
Actually, we're not supposed to call them lichens any more. The appropriate nomenclature today is lichenized fungi. There are two reasons for insisting on a new label. The first is simple: most of the lichen is, actually, a fungus. The microscopic photosynthesizing algae within the lichen's tissue are minute and difficult to see. But the second reason is more fundamental: the lichens are not a single (monophyletic) lineage. Different fungi have formed lichen associations with different algae, and even with blue-green bacteria. DNA studies make clear that different fungi have formed lichen associations independently and at different times in the past.
Most remarkable, lichens are often the only visible non-transient forms of life in the world's most severe habitats. Lichens outnumber plants and animals by a wide margin in Antarctica. Mosses are found in a few sites, with higher plants represented by less than ten species in Antarctica. Only a few species of birds and mammals survive there, feeding on the riches of the southern sea. At the other end of the Earth, lichens are a prominent part of the northern tundra, helping nourish herds of caribou. Lichens also flourish on high mountains and rocky outcrops exposed to wind and weather. We often see them on tree trunks and rock surfaces. North America boasts about 3,600 species, ranging in color from brilliant orange and bright yellow to quiet gray and dull brown.25 Some tropical lichens look like dabs of paint on smooth tree trunks. Though not that conspicuous amidst all the greenery, six hundred species of lichens have been found within one square kilometer (0.38 sq. mi.) of lowland rain forest in Costa Rica's La Selva preserve.26
What makes lichens so adaptable? Surely their most important quality is that they are autotrophic; they can feed themselves thanks to their photosynthesizing partners (called photobionts). Safely tucked away within their fungal host, the photobionts are nurtured and protected. Though the fungal element remains constant in a species of lichen, the algal element may vary. That is, the same lichen species may have different photobionts in different parts of its range. The algae provide carbohydrates to the fungus through “leaky walls.” In turn, the fungal body of the lichen has the job of remaining firmly attached to an appropriate substrate, while resisting the wear and tear of wind and weather. In addition, the fungus provides the alga with water and minerals. Simply put: “Lichens are fungi that discovered agriculture” (as lichenologist Trevor Goward once said). Numbering more than 17,000 species, lichens are a splendid example of biological cooperation.
LEGUMES: ANOTHER MAJOR SYMBIOTIC SYSTEM
Another grand symbiosis, helping support biodiversity in many ecosystems, is that of legumes and rhizobial bacteria. The legume family (Fabaceae) includes many impressive tropical trees, from flat-topped acacias of African savannas to giant rosewood trees in rain forests. The family also includes many twining plants, like garden peas, wisteria, and kudzu. Legumes provide us with nutritious foods: chickpeas, lentils, kidney beans, peas, soybeans, peanuts, and many others. Complementing our grain crops (such as wheat, barley, rice, and maize), the legumes, or pulses, are an important source of amino acids, essential for building proteins. Not only are the legumes more nutritious, they add available nitrogen to the soil when they die and decompose, contributing to sustainable agriculture in this way. By supporting nitrogen-fixing bacteria, legumes enrich themselves and the soil in which they grow. But why is this symbiosis so special?
Molecular nitrogen is unavailable to plants and animals, despite being a major component of our atmosphere. The reason is simple: molecular nitrogen has two nitrogen atoms in tight embrace, locked together by three strong covalent bonds. Only a few bacteria have the chemical machinery that can rip those two nitrogen atoms apart, transforming the relatively inert nitrogen of air into available nitrogen for other living things. Since amino acids, proteins, DNA, and RNA all contain nitrogen, available nitrogen is essential for all living things. But there's a problem: these nitrogen-fixing bacteria abhor oxygen! And this is why legumes produce pink-colored nodules on their roots, in which these bacteria live and work. The nodules are pinkish because they contain a special hemoglobin, which can bind oxygen, maintaining an oxygen-poor zone where the rhizobial bacteria can rip apart molecular nitrogen!
The legume symbiosis is a great story, but there's a problem: benefits have costs. Building nodules and nurturing nitrogen-fixing bacteria require a significant expenditure of energy. This means that a field of legumes is less productive of seeds than is a field of grains. Likewise, wild legumes living in natural habitats need to expend energy on maintaining their symbionts. Nevertheless, the sacrifice has been grandly successful. Numbering around 19,500 species in over six hundred genera, the legume family contributes significantly to the world's biodiversity.
A few other plants and animals harbor nitrogen-fixing bacteria. A remarkable example is found in termites, where the bacteria that help termites digest cellulose can also fix atmospheric nitrogen in a three-tiered system.27 These bacteria live only inside protozans that live in the termite's gut! With bacteria on board that can both digest cellulose and fix nitrogen—and with water from their own respiration—termites are able to prosper in dry dead wood.
The big message here is that, just as endosymbiosis created eukaryotic cells, and intercellular cooperation made multicellular organisms possible, positive interactions have also fostered greater complexity within modern ecosystems.28 A striking aspect of these many important biological mutualisms is that they are members of different kingdoms: algae within fungi forming lichens, legumes with bacteria to fix nitrogen, flowers and the animals that pollinate them, microbes helping us digest our food.29 Such examples make clear how “getting along well with others” can be a sound survival strategy in a difficult world. But having reviewed cooperation, disruption, disease, and niche division in maintaining local biodiversity, we need to examine another fundamental driver of biodiversity.
AVOIDING EXTINCTION: REPRODUCTION AND DISPERSAL
Cruising down the Amazon during an ecotour, it was my job to give lectures in the evening. I had just finished talking about biodiversity and it was time for questions, when a tour member seized the moment. An author of business management texts, this gentleman was sharp, as was his question.
“What purpose do mosquitoes have?” he demanded to know.
“Making more mosquitoes!” was my response.
Every organism on this planet has the same intrinsic drive: not just survival, but reproduction. Whether it is a solitary mushroom sending millions of spores into the wind, or a primate mother carefully nurturing her single offspring, the bottom line is the same for everybody. Just as death ends the life of a multicellular individual, extinction of a species means the game of life has ended for that particular lineage. In the real world, natural enemies, natural disasters, and plain old bad luck are part of the landscape. Fail to produce viable offspring and—in a biological sense—your life has been for naught. Here again, natural selection is the driving force. Healthy individuals with a strong reproductive drive will produce many offspring. Unhealthy individuals, or those who aren't interested in sex, will produce few. With these traits governed by multiple gene interactions, a strong reproductive drive will be maintained in every species, automatically, and for all time!
Every proper plant and animal has the same set of inherited instructions: reproduce! Those that fail this dictate compromise the future of their species. Reproductive protocols are central to the behavior of every living thing. Nutrition and survival may be the primary parameters, but they only serve the urge to procreate. This urge, in turn, powers both local and global biodiversity. For many lineages, the best strategy for long-term species survival is producing lots and lots of offspring. Year after year, elm trees cover our lawns with tens of thousands of little winged seeds. Cottonwood trees waft away countless cottony seeds on the winds of early summer. Spawning fish release millions of eggs and sperm into lakes and streams. Producing huge numbers of fertilized eggs or seeds is one way to keep the threat of extinction at bay.
In botany we often call seeds and fruits disseminules; their job is moving on out. Mobility is a central feature of survival. For animals, mobility allows escaping or avoiding predators, or finding better forage in a distant landscape. For plants and fungi, it is the ability to send seeds and spores far and wide across the landscape. With a bit of luck, a few of these disseminules will find the right niche in which to grow and flourish. In times of climatic change or local calamity, mobility may determine which species survives and which cannot. In the marine world, many animals have minute larval stages that allow the tiny offspring to disperse far and wide. More significantly, these huge numbers, whether animal larvae or fruits and seeds, are a primary food source for others in the community, helping sustain local biodiversity.
Today, both deliberately and accidentally, humans are dispersing many species around the globe. Consider Ascension Island, far from other landfalls in the mid-Atlantic ocean. When Darwin visited this island, the vegetation was treeless, and he promoted the introduction of woody plants. Now, over 150 years later, the island is richly covered in vegetation, with “cloud forests” contributing to stream flow. Here, deliberate dispersal has assembled a new self-sustaining ecosystem.30
Large numbers is one way a species can play nature's lottery of life, but there are other, equally effective, strategies as well. Having fewer offspring but generously tending and carefully protecting them can also foster reproductive success. Elaborate behaviors such as burying, hiding, or encapsulating the little eggs increases survivorship. Birds prepare a safe nesting site, then diligently rear a new brood each and every spring. Likewise, mammals invest virtually all of their adult lives in protecting and nurturing their young, generation after generation. Many land animals, and even a few fish, have abandoned egg-laying altogether. They may produce eggs, but the eggs remain within the mother's body to develop before the young are released into a hostile world. Some cichlid fishes are “mouth brooders,” holding the little ones within their mouths, providing the little fry protection until they become larger and better able to fend for themselves. Overall, two very different reproductive strategies are obvious: (1) make lots of eggs/spores/seeds and disperse them into the environment, versus (2) give birth to fewer offspring and take good care of them. For this latter group “species do not just happen, but must be achieved in each new generation, held in the world through the labor, skill and determination of individual organisms in real relationships of procreation, nourishment and care.”31
Many species exhibit additional “insurance policies” with which they improve their survival over time. Bacteria can transform into spore-like states to survive difficult conditions. Many species of plants and insects cannot survive dry weather or long winters; rather, their little offspring must endure these difficult episodes in the form of seeds, eggs, and pupae. A further strategy in the business of survival is to have seeds or eggs of the same season vary in their dormancy periods. Even under the best conditions, some seeds or eggs will remain dormant the following year, “waiting” several seasons before they sprout or begin developing. If next summer brings severe drought after all your seeds have sprouted, they will likely perish, and you have failed to reproduce your kind. Delayed dormancy, on the part of a percentage of your offspring, can avoid such a disaster. Many animals do the same. In fact, some soybean pests now remain dormant in the soil, as farmers grow two years of corn over a three-year crop rotation in the same field. You guessed it: these soybean pests have “learned” to cycle with the farmer's crop-rotation pattern. Actually, the pests hadn't learned anything. But, with variable and genetically determined dormancy times, it didn't take too many generations to have selection get most of the pests cycling in synchrony with the rotation of their soybean hosts. By staying dormant over two years, these pests emerge for the third year in the rotation: soybean time! Thanks to environmental selection, Mother Nature has solved a lot of problems in the business of survival. Best of all, staggered germination times give the plant community a seed bank sitting in the ground over many years, ready to emerge after stressful times. However, while surviving minor calamities is one challenge, being fed upon by nasty neighbors is yet another.
DYNAMIC INTERACTIONS!
Predators, parasites, pathogens, and herbivores have given rise to a cruel and dangerous world—though one with millions of species. There have been “arms races” between every species and its enemies over time, making the local environment a very harrowing and dynamic arena. Predators are being selected to become more effective; pathogens are evolving to counter the defenses of their hosts. Large numbers of herbivores play an important role in maintaining vegetation with many co-occurring species.32 A host of ongoing ecological interactions, both negative and positive, explains how local communities can support so many plants and animals. Having a specific niche in all this turmoil is one way to survive. But this is also a playing field in which good luck plays a significant role. And, because good luck is largely a random statistical operation, many lucky species can stay in business within diverse and complex ecosystems. All the while, rampant reproduction and effective dispersal keep the system going.
In his book The Diversity of Life, Edward O. Wilson referred to the ESA theory of biodiversity.33 ESA stands for Energy, Stability, and Area. Energy for life, of course, comes mostly from the Sun, and this factor explains why life is more abundant in the Sun-drenched tropics. Stability contrasts with major cataclysms, such as expanding ice sheets, extensive drought, or sudden climate change. Finally, a larger Area will support many species and this can be critical after a local region suffers annihilation. Migrants and propagules from the larger region can recolonize the locally devastated area and rebuild the local biota. As species go extinct in one place, they can be replaced by migrants from elsewhere. A steady flow of new immigrants requires similar communities over a larger area, and this is why area is so important in Wilson's formulation.
Today, natural communities are becoming smaller in the face of human expansion; sources of new native immigrants are diminished, and replacement becomes less likely. At the very same time, and thanks to global commerce, species from distant regions, arriving without their pests and pathogens, may become explosively invasive. Whether a fungal disease exterminating the American chestnut, zebra mussels devouring phytoplankton in the Great Lakes, or West Nile virus threatening birds and ourselves, we live in a world of increasing extinction (a topic we'll revisit in the final chapters).
Coevolution is a crucial process in the organization of biodiversity specifically because it is simultaneously flexible yet conservative in how it shares interspecific interactions in a constantly changing world.
—John N. Thompson34
Nature is dynamic, both globally and locally. Unreliable weather, nasty parasites, harrowing diseases, fearsome predators, and a few helpful mutualists, all interacting in complex environments, help sustain diversity in the same area over time. From a local perspective, all evolution is coevolution. Darwin used the example of an “entangled bank” to remind us of species interacting at a local scale. Often encountered along stream-sides, light from above the open water illuminates a tangle of shrubs and clambering vines along the bank. Maintaining local biodiversity is an operation of many entangled and interacting factors. All this is contemporary ecology, helping us understand today's biodiversity. But how did such elaborate biomes arise? Pursuing that theme, let's move on to paleontology, examining the escalation of biodiversity on planet Earth across deep time.
Figure 1. The last 560 million years of Earth's history. The Phanerozoic eon. Epochs are listed for the last 65 million years. Periods are listed for the time between 65 and 560 million years ago. Note that the time-scale for 0 to 65 million years ago is not the same as the time-scale for 65 to 560 million years ago.