Chapeter 6  Energy and Nutrient Relations

A scorpion fish lies half buried in the sand near the edge of a coral reef; the only clues to its presence are the telltale movements of its gill covers. Its head looks so much like an algae-covered stone that several tiny shrimp gather over it and swim lazily in the current. A small fish on the nearby reef sees the shrimp and darts over to feed on them. The scorpion fish opens its mouth and swallows the small fish in a lightning quick movement. However, before the scorpion fish can settle back into the sand. a green moray eel, nearly 2 m long, darts from the reef, grabs the scorpion fish with its razor-sharp teeth, and swallows it (fig. 6.1).

FIGURE 6.1 The moray eel meets its energy and nutrient needs by being an effective predator.

An herbaceous plant with broad leaves and slender stems grows in the half light of the rain forest floor. It is difficult to understand how it can live in such dim light. However, as you watch, a small shaft of intense sunlight pierces an unseen hole in the rain forest canopy and shines on one of the plant’s leaves. The photosynthetic machinery of the plant takes advantage of the situation, and for a few minutes the plant uses the energy of the tiny sun fleck. Nearby is the buttressed trunk of a gigantic tree that has grown tall enough to emerge from the forest canopy and count itself among the rain forest giants, seemingly a mom secure position than that of the understory herb. However, a small vine has begun to grow up the side of the tree. It will grow quickly upward, winding its way toward the sun and exploiting the woody support of the tree. Soon the vine will overwhelm and kill the tree, which will be reduced to a trellis for the vine.

Whether on coral reef, rain forest, or abandoned urban lot, organisms engage in an active search for energy and nutrients. For must organisms, life boils down to converting energy and nutrients into descendants. The energy used by different organisms comes in the form of light, organic molecules, or inorganic molecules. Nutrients are the raw materials an organism must acquire from the environment to live. Because organisms acquire energy and nutrients in diverse ways, we need to organize our discussion under the umbrella of major concepts. In chapter 6, we focus on three.


l        Organisms use one of three main sources of energy: light, organic molecules, or inorganic molecules.

l        The rate at which organisms can take in energy is limited.

l        Optimal foraging theory attempts to model how organisms feed as an optimizing process.

CASE HISTORIES: energy sources

Organisms use one of three main sources of energy: light, organic molecules, or inorganic molecules.

     How do we group organisms? We generally group organisms on the basis of shared evolutionary histories, creating taxa such as vertebrate animals, insects, coniferous trees, and orchids. However, we can also classify organisms by how they obtain energy--that is, by their trophic (feeding) biology. Organisms that use inorganic sources of both carbon and energy are called autotrophs ("self-feeders") and are of two types, photosynthetic and chemosynthetic. Photosyntheic autotrophs use carbon dioxide (CO2) as a source of carbon and light as a source of energy. This group includes the plants, photosynthetic protists, and photosynthetic bacteria. Chemosynthetic autotrophs use inorganic molecules as a source of carbon and energy. These are made up of a highly diverse group of chemosynthetic bacteria. Heterotmphs ("other-feeders") are organisms that use organic molecules both as a source of carbon and as a source of energy. The heterotrophs include bacteria, fungi, protists, animals, and parasitic plants.

Bacteria show more trophic diversity than the other biological kingdoms (fig. 6.2). The protists are either photosynthetic or beterotrophic, most plants are photosynthetic, and all fungi and animals are heterotrophic. In contrast, the bacteria include photosynthetic, chemosynthetic, and heterotrophic species, making them, as a group, the most trophically diverse organisms in the biosphere.

FIGURE 6.2 Trophic diversity across the biological kingdoms.


Using Light and CO2

    Because photosynthetic organisms use light as a source of energy, we need to learn about light. We also need to understand how photosynthetic organisms use CO2. These are topics we investigate next.


The Solar-Powered Biosphere

    As we saw in chapters 2 and 3, solar energy powers the winds and ocean currents, and annual variation in sunlight intensity drives the seasons. In chapter 4, we also discussed how organisms use sunlight to regulate body temperature. Here, building on those discussions, we look at light as a source of energy for photosynthesis.

Light propagates through space as a wave, with all the properties of waves such as frequency and wavelength. When light interacts with matter, however, it acts not as a wave but as a particle. Particles of light, called photons, bear a finite quantity of energy. Longer wavelengths, such as infrared light, carry less energy than shorter wavelengths, such as visible and ultraviolet light.

Infrared light, as we saw in chapter 4 (see fig. 4.13), is very important for temperature regulation by organisms. This is because the main effect of infrared light on matter is to increase the motion of whole molecules, which we measure as increased temperature. However, infrared light does not carry enough energy to drive photosynthesis. At the other end of the solar spectrum, ultraviolet light carries so much energy that it breaks the covalent bonds of many organic molecules. Because it can break down organic molecules, ultraviolet light can destroy the complex biochemical machinery of photosynthesis. Between these extremes is the light we can see, so- called visible light, which is also called photosynthetically active radiation, or PAR. PAR, with wavelengths between about 400 and 700 nm, carries sufficient energy to drive the light-dependent reactions of photosynthesis but not so much as to destroy organic molecules. PAR makes up about 45% of the total energy content of the solar spectrum at sea level, while infrared light accounts for about 53% and ultraviolet light for the remainder.


Measuring PAR

    Ecologists quantify PAR as photon flux density. Photon tlux density is the number of photons striking a square meter surface each second. The number of photons is expressed as micromoles (μmol), where 1 mole is Avagadro's number of photons, 6.023×1023. To give you a point of reference, a photon flux density of about 4.6 μmol per square meter per second equals a light intensity of about 1 watt per square meter Measuring light as photosynthetic photon flux density makes sense ecologically because chlorophyll absorbs light as photons.

Light changes in quantity and quality with latitude, with the seasons, with the weather, and with the time of day. In addition, landscapes, water, and even organisms themselves change the amount and quality of light. For example, in aquatic environments (see chapter 3), only the superficial euphoric zone receives sufficient light to support photosynthetic organisms. In addition, light changes in quality, as well as quantity, within the euphotic zone, which ranges in depth from a few meters to about 100 m (see fig. 3.7).

As in the sea, sunlight changes as it shines through the canopy of a forest. A mature temperate or tropical forest can reduce the total quantity of light reaching the forest floor to about 1% to 2% of the amount shining on the forest canopy (fig. 6.3). However, forests also change the quality of sunlight. Within the range of photosynthetically active radiation, leaves absorb mainly blue and red light and transmit mostly green light with a wavelength of about 550 nm. As in the deep sea, the organisms on the forest floor live in a kind of twilight. Only here, the twilight is green (see fig. 2.9).

FIGURE 6.3 Photosynthetically active radiation (PAR) in a boreal forest (data from Larcher 1995. after Kairiukstis 1967).


Alternative Photosynthetic Pathways

    During photosynthesis, the photosynthetic pigments of plants, algae, or bacteria absorb light and transfer their energy to electrons. Subsequently, the energy carried by these electrons is used to synthesize ATP and NADPH. These molecules, in turn, serve as donors of electrons and energy for the synthesis of sugars. In this way, photosynthetic organisms convert the electromagnetic energy of sunlight into energy-rich organic molecules, the fuel that feeds most of the biosphere. Within photosynthetic organisms, specific biochemical pathways carry out this energy conversion; three different biochemical pathways are known: C3 photosynthesis, C4 photosynthesis, and CAM photosynthesis. These are found in ecologically different organisms.

Biologists often speak of photosynthesis as "carbon fixation,'' which refers to the reactions in which CO2 becomes incorporated into a carbon-containing acid. In the photosynthetic pathway used by most plants and all algae, the CO2 first combines with a five-carbon compound called ribulose bisphosphate, or RuBP. The product of this initial reaction, which is catalyzed by the enzyme RuBP carboxylase, is phosphoglyceric acid, or PGA, a three-carbon acid. Therefore, this photosynthetic pathway is usually called C3 photosynthesis and the plants that employ it are called C3 plants (fig. 6.4).

FIGURE 6.4 C3 photosynthesis.

To fix carbon, plants must open their stomata to let CO2 into their leaves, but as CO2 enters, water exits. Water vapor flows out faster than CO2 flows in. The movement of water is more rapid because the gradient in water concentration from the leaf to the atmosphere is much steeper than the gradient in CO2 concentration from the atmosphere to the leaf. In CO3 plants, there is another factor that contributes to a low rate of CO2 uptake: RuBP carboxylase has a low affinity for CO2. Relatively high rates of water loss are not a problem for plants that live in cool, moist conditions but in hot, dry climates, high rates of water loss can close the stomata and shut down photosynthesis.

In add environments, two alternative photosynthetic pathways have evolved. Both pathways fix and store CO2 in acids containing four carbon atoms. Light plays no part in carbon fixation, but the reactions that follow depend on light. Both alternative pathways separate the initial fixation of carbon from the light-dependent reactions.

One of these alternative pathways, C4 photosynthesis, separates carbon fixation and the light-dependent reactions of photosynthesis into separate cells (fig. 6.5). C4 plants fix CO2 in mesophyll cells by combining it with phosphoenol pyruvate, or PEP. to produce an acid. This initial reaction, which is catalyzed by PEP carboxylase, concentrates CO2. Because PEP carboxylase has a high affinity for CO2, C4 plants can reduce their internal CO2 concentrations to very low levels. Low internal concentration of CO2 increases the gradient of CO2 from atmosphere to leaf, which in turn increases the rate of diffusion of CO2 inward. Consequently, compared to C3 plants, C4 plants need to open fewer stomata to deliver sufficient CO2 to photosynthesizing cells. By having fewer stomata open, C4 plants conserve water.

FIGURE 6.5 C4 photosynthesis.

In C4 plants, the acids produced during carbon fixation diffuse to specialized cells surrounding a structure called the bundle sheath. There, deeper in the leaf, the four-carbon acids are broken clown to a three-carbon acid and CO2. In this way, C4 plants can build up the CO2 concentration in bundle sheath cells to high levels, increasing the efficiency with which RuBP carboxylase combines CO2 with RuBP to produce PGA. C4 plants do better than C3 plants under conditions of high temperature, high light intensity, and limited water. Review C3 and C4 photosynthesis (figs. 6.4 and 6.5) before considering the third major photosynthetic pathway.

CAM (crassulacean acid metabolism) photosynthesis is largely limited to succulent plants in arid and semiarid environments. In this pathway, carbon fixation takes place at night, when lower temperatures reduce the rate of water loss during CO2 uptake. CAM plants fix carbon by combining CO2 with PEP to form four-carbon acids. These acids are stored until daylight, when they are broken down into pyruvate and CO2, which then enters the C3 photosynthetic pathway (fig. 6.6). In CAM plants, all these reactions take place in the same cells. While CAM plants do not normally show very high rates of photosynthesis, their water use efficiency, as estimated by the mass of CO2 fixed per kilogram of water used, is higher than that of either C3 or C4 plants.

FIGURE 6.6 Crassulacean acid metabolism, or CAM, photosynthesis.

Separating initial carbon fixation from the other reactions reduces water losses during photosynthesis: C3 plants lose from about 380 to 900 g of water for every gram (dry weight) of tissue produced. C4 plants lose from about 250 to 350 g of water per gram of tissue produced, while CAM plants lose approximately 50 g of water per gram of new tissue. The differences in these numbers give us one of the masons C4 and CAM plants do well in hot, dry environments.

Whether the pathway of carbon fixation is CAM, C3, or C4, plants and photosynthetic algae and bacteria capture energy from sunlight and carbon from CO2. These photosynthesizers package this energy and carbon in organic molecules. The photosyntbesizers and other autotrophs opened the way for the evolution of organisms that could get their energy and carbon from organic molecules. And this new trophic level did indeed evolve.


Using Organic Molecules

    Heterotrophic organisms use organic molecules both as a source of carbon and as an energy source. They depend, ultimately, on the carbon and energy fixed by autotrophs. Heterotrophs have evolved numerous ways of feeding. This trophic variety has stimulated ecologists to invent numerous terms to describe the ways heterotrophs feed; a few of these terms have already crept into our discussions. In chapter 2, we referred to the "browsers" of temperate woodlands and shrub-lands and in chapter 3, when discussing James Karr's Index of Biological Integrity, we defined "omnivores," "insectivores," and "piscivores." A full list of the trophic categories proposed by ecologists would be impossibly long and not especially useful to this discussion. So, we will concentrate on three major categories: herbivores, organisms that eat plants; carnivores, organisms that mainly eat animals; and detritivores, organisms that feed on nonliving organic matter, usually the remains of plants. While these categories do not capture all the trophic diversity in nature, they are not arbitrary. Herbivores, carnivores, and detritivores must solve fundamentally different problems in order to obtain adequate supplies of energy and nutrients.


Chemical Composition and Nutrient Requirements

    We can get some idea of the nutrient requirements of organisms by examining their chemical composition. Biologists have found that the chemical composition of organisms is very similar. Just five elements (carbon [C], oxygen [O], hydrogen [H], nitrogen [N], and phosphorus [P]) make up 93% to 97% of the biomass of plants, animals, fungi, and bacteria. Of these four groups, plants are the most distinctive chemically. Plant tissues generally contain lower concentrations of phosphorus and nitrogen. The nitrogen content of plant tissues averages about 2%, while in fungi, animals, and bacteria it averages about 5% to 10%. Ecologists often express the relative nitrogen content of whole organisms or tissues as the ratio of carbon to nitrogen (C:N ratios). A high C:N ratio indicates low nitrogen content. The C:N ratio of plants averages about 25:1, which is substantially higher than the C:N ratios of animals, fungi, and bacteria, which average approximately 5:1 to 10:1 (fig. 6.7). Differences in C:N ratios among tissues or among organisms significantly influence what organisms eat, how rapidly consumers reproduce, and how rapidly organisms decompose.

FIGURE 6.7 Ratio of carbon to nitrogen (C:N) actress biological kingdoms (data from Spector 1956).

If carbon, oxygen, hydrogen, nitrogen, and phosphorus make up 93% to 97% living biomass, then what accounts for the remainder? Dozens of other elements occur in the tissues of organisms. Essential plant nutrients include potassium (K), calcium (Ca), magnesium (Mg), sulfur (S), chlorine (Cl), iron (Fe), manganese (Mn), boron (B), zinc (Zn), copper (Cu), and molybdenum (Mo). Most of these nutrients are also essential for other organisms. Some organisms require additional nutrients. For instance, animals also require sodium (Na) and iodine (I).

Plants obtain carbon from the air through their stomata. They obtain other essential nutrients from the soil through their roots. For the most part, animals obtain both the energy they require and essential nutrients with their food. Let's now turn to the energy and nutrient relations of herbivorous, detritivorous, and carnivorous animals.



    While a band of zebra grazing on the plains of Africa or a sea turtle munching on sea grass in a tropical lagoon may suggest a life of ease, this image does not accurately represent the life of an herbivore. Herbivores face substantial problems that begin at the level of nutritional chemistry. Most plant tissues contain a great deal of carbon but low concentrations of nitrogen (fig. 6.7).

Herbivores must also overcome the  physical and chemical defenses of plants. Some physical defenses are obvious, such as thorns that deter some herbivores entirely and slow the rate of feeding of others (fig. 6.8). However, plants also often deploy a variety of mote subtle physical defenses. Grasses incorporate large amounts of abrasive silica into their tissues, which makes feeding on them difficult and which has apparently selected for specialized dentition among grazing mammals. Many plants toughen their tissues with large quantities of cellulose and lignin, producing leaves that are fibrous and difficult to chew.

FIGURE 6.8 Herbivores must overcome the wide variety of physical arm chemical defenses evolved by plants.

The use of cellulose and lignin to strengthen tissues may also provide plants with a kind o chemical defense. Increasing the cellulose and lignin content of tissue mcreases their C:N ratios. An increased C:N ratio decreases the nutritional value of plant tissues. Some plant tissues have C:N ratios that are far higher than the average values we saw in figure 6.7. For instance, the tree trunks that make up most of the plant biomass in a pine forest have a C:N ratio of over 300:1 (fig. 6.9). This ratio is much higher than that of either branches or needles. The living needles of pine trees have C:N ratios very similar to those of understory herbs living on the forest floor.

FIGURE 6.9 Variation in C:N ratios in a pine forest (data from Klemmedson 1975).

In addition, most animals cannot digest either cellulose or lignin. Those that can generally do so with the help of bacteria, fungi, or protists that live in their digestive tracts. This suggests that the cellulose and lignin in plants may be a first line of chemical defense against herbivores, a defense that most herbivores overcome with the help of other organisms.

When ecologists talk about plant chemical defenses, however, they are generally referring to two other classes of chemical, toxins and digestion-reducing substances. Toxins are chemical that kill, impair, or repel most would-be consumers. Digestion-reducing substances are generally phenolic compounds such as tannins that bind to plant proteins, inhibiting their breakdown by enzymes and further reducing the already low availability of nitrogen in plant tissues.

Chemists have isolated thousands of toxins from plant tissues, and the list continues to grow. The great variety of plant toxins defies easy description and generalization. However, one interesting pattern is that more tropical plants contain toxic alkaloids than do temperate species (fig. 6.10). In addition, on average, the alkaloids produced by tropical plants are more toxic than their temperate counterparts. Despite these higher levels of chemical defense, herbivores appear to remove approximately 11% to 48% of leaf biomass in tropical forests, while in temperate forests they remove about 7%. These higher levels of herbivore attack on tropical plants suggest that natural selection for chemical defense is more intense in tropical plant populations.

FIGURE 6.10 Proportion of temperate and tropical plants bearing toxic alkaloids (data from Coley and Aide 1991).

The generalization about higher levels of' chemical defense also appears to apply to marine algae. Robin Bolser and Mark Hay (1996) tested the hypothesis that tropical sea- weeds have more chemical defenses than temperate sea- weeds. They gathered several species of seaweeds from the coast of temperate North Carolina and from the tropical Bahama Islands. Bolser and Hay were careful to pick the same species of seaweed in the two study sites or at least to pick species that belonged to the same genus. They tested the relative palatability of temperate and tropical seaweeds using temperate and tropical sea urchins.

The researchers were very careful to preserve any chemical defenses their study algae might contain. They cleaned and then froze the seaweeds in a freezer (-20) on the research ship. On shore, the seaweeds were transferred to a colder freezer (-70) to minimize chemical changes.

To remove the potential confounding effect of various physical factors, Bolser and Hay created artificial algae to test their hypothesis. They did this by freeze-drying samples of each seaweed and grinding them up in a coffee mill. The powdered algae was then mixed with agar at a concentration of 0.1 g alga per milliliter of agar. The warm alga and agar mixture was poured into a mold set on screening. As the mixture gelled it attached to the screening. The result was strips of artificial seaweed that could be cut up into equal-sized squares and presented to sea urchins in equal numbers. This method of presentation also provided an easy means of quantifying the actual amount of seaweed eaten.

The results of this study showed a clear preference for temperate species of seaweed (fig. 6.11). When given a choice the urchins removed approximately twice as much of the available temperate seaweed. In addition, both temperate and tropical urchins showed a similar preference for temperate seaweeds. What caused the lower palatability of the tropical seaweeds? In additional tests, Bolser and Hay showed that the tropical seaweeds have more potent chemical defenses. So we see that this study produced a pattern in the sea that parallels the better-studied pattern known for tropical and temperate forests. Tropical plants and algae appear to possess stronger chemical defenses.

FIGURE 6.11 Sea urchin preference for temperate versus tropical seaweeds (data from Bolser and Hay 1996).

 No defense is perfect; the defenses of most plants work against some herbivores, but not all. The tobacco plant uses nicotine, a toxic alkaloid, to repel herbivorous insects, most of which die suddenly after ingesting nicotine. However, several insects specialize in eating tobacco plants and manage to avoid the toxic effects of nicotine. Some simply excrete nicotine, while others convert it to nontoxic molecules. Similarly, toxins and repellents produced by plants in the cucumber family repel most herbivorous insects but attract the spotted cucumber beetle. This beetle is a specialist that feeds mainly on members of the cucumber family. Some specialized herbivores go even further by using plant toxins as a source of nutrition!

The effectiveness of phenolic compounds as digestion-reducing substances is also uneven. For example, while the tannins in oak leaves deter feeding by some insects, they only reduce the growth and development of the winter moth, Operophtera brumata, which specializes on oak leaves. Meanwhile, other insects appear to be unaffected by moderate concentrations of tannins or may even be stimulated to feed by the presence of tannins.

The world may appear green to us, but to herbivores only some shades of green are edible. Plant defenses and the adaptations of herbivores that overcome those defenses are complex.



    The problems faced By herbivores in their search for energy and nutrients are related to those faced by detritivores, which feed on dead plant material. These organisms consume food that is rich in carbon and energy but very poor in nitrogen. In fact, plant tissues, already relatively low in nitrogen when living (see figs. 6.7 and 6.9), are even lower in nitrogen content when cast off by plants as detritus. Keith Killingbeck and Walt Whitford (1996) averaged the nitrogen contents of living and dead leaves of many plant species of environments from tropical rain forests through deserts and temperate forests. Their results show that in all these environments, living leaves contain about twice the nitrogen as dead leaves (fig. 6.12).

FIGURE 6.12 Nitrogen content of live and dead leaves (data frorn Killingbeck and Whirford 1996).

In addition, fresh detritus may retain levels of chemical defenses high enough to reduce its use by detritivores. I. Middleton (1984) suggested that plant chemical defenses may evolve because reducing the rate of decomposition increases a plant's fitness. Why? Middleton proposed that toxic chemicals may delay the rate of decomposition just enough to give the plant more control over limited nutrients. Delayed decomposition may also promote the buildup of organic matter in soils. Like herbivores, detritivores may have important influences on the evolution of plant chemical defenses.



    Carnivores consume prey that are nutritionally rich. However, carnivores cannot go out into their environment and choose prey at will. Most prey species are masters of defense. One of the most basic prey defenses is camouflage. Predators cannot eat prey they cannot find. Other prey defenses include anatomical defenses such as spines, shells, repellents, and poisons and behavioral defenses such as flight, taking refuge in burrows, banding together in groups, playing dead, fighting, flashing bright colors, spitting, hissing, and screaming at predators. It's enough to spoil your appetite!

Prey that carry a threat to predators often advertise that fact, usually by being brightly colored or conspicuous in some other way. The conspicuous, or aposematic, colors of many distasteful or toxic butterflies, snakes, and nudibranchs warn predators that "feeding on me may be hazardous to your health." Many noxious organisms, such as stinging bees and wasps, poisonous snakes, and butterflies, seem to mimic each other. This form of comimicry among several species of noxious organisms is called Mullerian mimicry (fig. 6.13a). In addition, many harmless species appear to mimic noxious ones. For instance, king snakes mimic coral snakes, and syrphid flies mimic bees. This form of mimicry is called Batesian mimicry. In Batesian mimicry, the noxious species serves as the model and the harmless species is the mimic (fig. 6.13b).

FIGURE 6.13 POISONOUS Mullerian (a) and nonpoisonous Batesian (b) mimics.

How have prey populations evolved their defenses? The predators themselves are usually the agents of selection for refined prey defense. In one of the most thoroughly studied cases of natural selection for prey defense, H. Kettlewell (1959) found that predation by birds favors camouflage among peppered moths, Biston betularia. Birds eliminate the more conspicuous members of the peppered moth population, leaving the better camouflaged (fig. 6.14). In general, predators eliminate poorly defended individuals and leave the well defended. Consequently, the average level of defense in the prey population increases with time.

FIGURE 6.14 Birds and other predators act as agents of natural selection for improved prey defense.


    As a consequence of prey defenses, the rate of prey capture by predators is often low. For instance, wolves on Isle Royale in Lake Superior capture moose only about 8% of the_ times they try. Bernd Heinrich (l984) found that predatory bald-faced hornets have an even lower success rate. The hornets hunt other insects by flying rapidly among the plants in their environment and pouncing on objects that may be prey. Because their prey are well camouflaged, the hornets often pounce on inanimate objects. Heinrich was able to observe 260 pounces by hornets. About 72% of these pounces were directed at inanimate objects, such as bird droppings and brown spots on leaves. Another 21% of the pounces were directed at insects, such as bumblebees and other wasps, that are too well defended to be prey. Only 7% of the pounces were on potential insect prey. The hornets managed to capture two of these, a moth and a fly. Heinrich's observations indicate bald-faced hornets have a prey capture rate of less than 1%.

Though elusive, the prey of carnivores are generally similar in nutrient content. Consequently, carnivores, which are often widely distributed geographically, can vary their diets from one region to another. The Eurasian otter, Lutra lutra, which is distributed from Europe and North Africa through northern and central Asia, changes its diet based on the local availability of prey. Manuel Graca and E X. Ferrand de Almeida (1983) compared otter diets along a gradient from northern to southern Europe (fig. 6.15). On the Shetland Islands, otter diets are over 91% fish, with the remainder consisting almost entirely of crabs. To this staple diet of fish the otters of England add frogs, mammals, and birds. Meanwhile, the diets of otters in central Portugal are less than one-third fish, with the remainder consisting of frogs, water snakes, birds, and aquatic insects. While some of the items that Graca and Ferrand de Almeida found on the otters' menus may be esthetically unacceptable to us, they are all fairly similar in terms of their carbon, nitrogen, and phosphorus content; they are just packaged differently.

FIGURE 6.15 Geographic variation in river otter diets (data from Graca and Ferrand de Almeida 1983).

Because predators must catch and subdue their prey, they often select prey by size, a behavior that ecologists call size-selective predation. Because of this behavior, prey size is often significantly correlated with predator size, especially among solitary predators. One such solitary predator, the puma, or mountain lion, Fells concolor, ranges from the Canadian Yukon to the tip of South America. Puma size changes substantially along this latitudinal gradient. Mammals make up over 90% of the puma's diet and large mammals, especially deer, are its main prey in the northern part of its range in North America. However, Augustin Iriarte and his colleagues (1990) found that as pumas decrease in size southward, the average size of their prey also decreases (fig. 6.16). In the tropics, the puma feeds mainly on medium and small prey, especially rodents. Then, as pumas again increase in size south of the equator, large mammals form an increasing portion of their diet. Why should different-sized pumas feed on different-sized prey? One reason is that large prey may be difficult to subdue and may even injure the predator, while small prey may be difficult to find or catch. As we shall see later in chapter 6, size selective predation may also have an energetic basis.

FIGURE 6.16 The size of pumas and their prey (data from Iriate et al. 1990).

In summary, predators consume nutritionally rich but elusive and often well-defended prey. As a consequence, predators and their prey appear engaged in a coevolutionary race. In this race, predators eliminate poorly defended individuals in the population and average prey defenses improve. As average prey defenses improve, the poorer hunters go bungry and leave fewer offspring. Consequently, improved hunting skills evolve in the predator population, which exerts further selection on the prey population.

Now let's turn from typical heterotrophs such as the puma to organisms that obtain their energy from inorganic molecules. These are the chemosynthetic autotrophs. Though less familiar to most of us, chemosynthesis may be the oldest way of making a living.


Using Inorganic Molecules

    In 1977, a routine dive by a small submersible carried scientists exploring the Galapagos rift to a grand discovery. Their discovery changed our view of how a biosphere can be structured. Ecologists had long assumed that photosynthesis provides the energy for nearly all life in the sea. However, these unsuspecting scientists came across a world based upon an entirely different energy  source, energy captured by chemosynthesis. The world they discovered was inhabited by giant worms up to 4 m long with no digestive tracts, by filter-feeding clams, and by carnivorous crabs tumbling over each other in tangled abundance (see fig. 3.8). These organisms lived on nutrients discharged by deep-sea volcanic activity through an oceanic rift, a crack in the seafloor. Interconnected systems of rifts extend tens of thousands of kilometers along the seafloor, Subsequent explorations have confirmed that chemosynthetic communities exist at many points of volcanic discharge along the seafloor.

The autotrophs upon which these submarine oases depend are chemosynthetic bacteria. Some of the most common are sulfur oxidizers, bacteria that use CO2 as a source of carbon and get their energy by oxidizing elemental sulfur, hydrogen sulfide, or thiosulfite. The submarine volcanic vents with which these organisms are associated discharge large quantities of sulfide-rich warm water The sulfur-oxidizing bacteria that exploit this resource around the vents are of two types: free-living forms and those that live within the tissues of a variety of invertebrate animals, including the giant tube worms (fig. 6.17). Other communities dependent upon sulfur-oxidizing bacteria have been discovered in thermal vents in deep freshwater lakes, in surface hot springs, and in caves.

FIGURE 6.17 Hydrogen sulfide as an energy source for chemoautotrophic bacteria in the deep sea.

Other chemosynthetic bacteria oxidize ammonium (NH4+), nitrite (NO2-), iron (Fe2+), hydrogen (H2), or carbon monoxide (CO). Of these, the nitrifying bacteria, which oxidize ammonium to nitrite and nitrite to nitrate, are undoubtedly among the most ecologically important organisms in the biosphere. Figure 6.18 summarizes one of the energy-yielding reactions exploited by nitrifying bacteria. The importance of these bacteria is due to their role in cycling nitrogen. As we saw earlier in the chapter, nitrogen is a key element in the chemical makeup of individual organisms. It also plays a central role in the economy of the entire biosphere. Nitrogen will frequently enter our discussions in later chapters. In the Applications and Tools section of this chapter, we will see how nitrifying bacteria have contributed to a pollution problem associated with an old gold mine.

FIGURE 6.18 Ammonium as an energy source for chemoautotrophic bacteria in soil.

As you can see, the trophic diversity among organisms is great. However, at least one ecological characteristic is shared by all organisms, regardless of the trophic group to which they belong--all organisms take in energy at a limited rate.


CASE HISTORIES: energy limitation

The rate at which organisms can take in energy is limited.

    As children, many of us imagined that if we had free access to a candy or ice cream shop we would consume an infinite quantity of goodies. But even if we were given a chance to do this, our rate of intake would be limited, not by supply but by the rate at which we could process what we ate. In reality, the rate of intake of candy or ice cream for most children is limited, at least in the short term, by how much is available. The same is true in nature. If organisms are not limited by the availability of energy in the environment, their energy intake is limited by internal constraints. Limits on the potential rate of energy intake by animals have been demonstrated by studying how feeding rate increases as the availability of food increases. Limits on rates of energy intake by plants have been demonstrated by studying how photosynthetic rate responds to photon flux density.


Photon Flux and Photosynthetic Response Curves

    Plant physiologists generally test the photosynthetic potential of plants in environments that are ideal for the particular species being studied. These environments have abundant nutrients and water, normal concentrations of oxygen and carbon dioxide, ideal temperatures, and high humidity. If you gradually increase the intensity of light shining on plants growing under these conditions, that is, if you increase the photon flux density, the plants' rates of photosynthesis gradually increase and then level off. At low light intensities, photosynthesis increases linearly with photon flux density. At intermediate light intensities, photosynthetic rate rises more slowly. Finally, at high light intensity, but well below that of full sunlight, photosynthesis levels off. Data that show this type of photosynthetic response curve have been collected in studies of terrestrial plants, lichens, planktonic algae, and benthic algae.

 Let's examine the structure of a theoretical photosynthetic response curve before comparing the photosynthetic responses of representative plant species. The response curves for different plant species generally level off at different maximum rates of photosynthesis. This rate in figure 6.19 is indicated as Pmax. A second difference among photosynthetic response curves is the photon flux density, or irradiance, required to produce the maximum rate of photosynthesis. The irradiance required to saturate photosynthesis is shown in figure 6.19 as Isat

FIGURE 6.19 A theoretical photosynthetic response curve.

Differences in photosynthetic response curves have been used to divide plants into "sun" and "shade" species. The response curves of plants from shady habitats suggest selection for efficiency at low light intensities. The photosynthetic rate of shade plants levels off at lower light intensities, and they are often damaged by intense light. However, at very low light intensities, shade plants usually have higher photosynthetic rates than sun plants. Park Nobel (1977) determined the photosynthetic response curve for the maiden hair fern, Adiantum decorum. This plant generally grows at low light intensities in forests. In one of Park's trials, the maximum rate of photosynthesis by A. decorum, Pmax, was approximately 9 μmol of CO2 per square meter per second. The amount of light required to achieve this maximum rate of photosynthesis, Isat, was a photon flux density of about 300 μmol per square meter per second (fig. 6.20). The values of Pmax and Isat shown by A. decorum are much lower than those observed in plants that have evolved in sunny environments.

FIGURE 6.20 Contrasting photosynthetic response curves (data from Ehleringer: Bj6rkman, and Mooney 1976. after Nobel 1977).

Herbs and short-lived perennial shrubs that have evolved in sunny environments show high maximum rates of photosynthesis, Pmax, at relatively high light intensities, Isat. One such plant, Encelia farinosa, grows in the hot deserts of North America. James Ehleringer and his colleagues (1976) found that E. farinosa has a high Pmax, more than four times that of A. decorum. In addition, E. farinosa reaches these maximum rates of photosynthesis at a photon flux density of about 2,000 μmol per square meter per second (fig. 6.20). This combination of high Pmax and Isat allows E. farinosa to fix energy at a high rate during the infrequent times when water is plentiful in its desert environment.

Whether of shade or sun plant, photosynthetic response curves eventually level off. In other words, the rate at which photosynthetic organisms can take in energy is limited. As we shall now see, animals also take in energy at a limited rate.


Food Density and Animal Functional Response.

    If you gradually increase the amount of food available to a hungry animal, its rate of feeding increases and then levels off. This relationship is called the functional response.

Ecologists use graphs to describe functional responses. C. S. Holling (1959) described three types of functional responses, all of which level off at a maximum feeding rate (fig. 6.21).

FIGURE 6.21 Three theoretical functional response curves.

Type l functional responses are those in which feeding rate increases linearly (as a straight line) as food density increases and then levels off abruptly at some maximum feeding rate. The only animals that have type 1 functional responses are consumers that require little or no time to process their food; for example, some filter-feeding aquatic animals that feed on small prey.

 In a type 2 functional response, feeding rate at first rises linearly at low food density, rises more slowly at intermediate food density, and then levels off at high densities. At low food densities, feeding rate appears limited by how long it takes the animal to find food. At intermediate food densities, the animal's feeding rate is partly limited by the time spent searching for food and partly by the time spent handling food. "Handling" refers to such activities as cracking the shells of nuts or snails, removing distasteful scent glands from prey, and chasing down elusive prey. At high food density an animal does not have to search for food at all and feeding rate is determined almost entirely by how fast the animal can handle its food. At these very high densities, the animal, in effect, has "all the food it can handle."

The type 3 functional response is S-shaped. What mechanisms may be responsible for the more complicated shape of the type 3 functional response? Why does feeding rate increase slowly at low densities? At low density, food organisms may be better protected from predators because they occupy relatively protected habitats, or "safe sites." In addition, animals often ignore uncommon foods. Many animals seem to focus most of their attention on more abundant foods, switching to less common food only when it exceeds some threshold density. Animals may also require some learning to exploit food at a maximum rate. At low food densities they do not have sufficient exposure to a particular food item to fully develop their searching and handling skills. Holling's research provided a theoretical basis for later empirical studies of animal functional response.

Of the hundreds, perhaps thousands, of functional response curves described by ecologists, the most common is the type 2 functional response. Here are some examples. John Gross and several colleagues (1993) conducted a well-controlled study of the functional responses of 13 mammalian herbivore species. The researchers manipulated food density by offering each herbivore various densities of fresh alfalfa, Medicago sativa. The rate of food intake was measured as the difference between the amount of alfalfa offered to an animal at the beginning of a trial and how much was left over at the end. Gross and his colleagues ran 36 to 125 feeding thais for each herbivore species for a total of over 900 trials. Every species of herbivore examined, from moose to lemmings to prairie dogs, showed a type 2 functional response. Figure 6.22 shows the type 2 functional response shown by moose, Alces alces.

FIGURE 6.22 A functional response by moose (data from Gross etal. 1993).

Gross and his colleagues worked in a controlled experimental environment. Do consumers in natural environments also show a type 2 functional response? To answer this question, let's examine the functional response of wolves, Canis lupus, feeding on moose. Francois Messier (1994) examined the interactions between moose and wolves in North America. He focused on areas where moose are the dominant large prey species eaten by wolves. When moose density in various regions was plotted against the rate at which they are killed by wolves, the result was a clear type 2 functional response (fig. 6.23).

FIGURE 6.23 Wolf functional response (data from Messier 1994).

Type 2 functional responses are remarkably similar to the photosynthetic response curves shown by plants (see fig. 6.20) and have the same implications. Even if you provide an animal with unlimited food, its energy intake eventually levels off at some maximum rate. This is the rate at which energy intake is limited by internal rather than external constraints. What conclusions can we draw from this parallel between plants and animals? We can conclude that even under ideal conditions, organisms as different as wolves, moose, and the plants eaten by moose take in energy at a limited rate. As we shall now see, limited energy intake is a fundamental assumption of optimal foraging theory.


CASE HISTORIES: optimal foraging theory

Optimal foraging theory attempts to model how organisms feed as an optimizing process.

    Evolutionary ecologists predict that if organisms have limited access to energy, then natural selection is likely to favor individuals within a population that are more effective at acquiring energy. This prediction spawned an area of ecological inquiry called optimal foraging theory. Optimal foraging theory assumes that if energy supplies are limited, organisms cannot simultaneously maximize all of life's functions; for example, allocation of energy to one function, such as growth or reproduction, reduces the amount of energy available to other functions, such as defense. As a consequence, there must be compromises between competing demands. This seemingly inevitable conflict between energy allocations has been called the principle of allocation.

Optimal foraging theory attempts to model how organisms feed as an optimizing process, a process that maximizes or minimizes some quantity. In some situations, the environment may favor individuals that assimilate energy or nutrients at a high rate (e.g., some filter-feeding zooplankton and short-lived weedy annual plants growing in disturbed habitats). In other situations, selection for minimum water loss appears much stronger (e.g., cactus and scorpions in the desert). Optimal foraging theory attempts to predict what consumers will eat, and when and where they will feed. Early work in this area concentrated on animal behavior More recently the acquisition of energy and nutrients by plants has been modeled, using ideas borrowed from economic theory.


Testing Optimal Foraging Theory

    How can you test optimal foraging theory? Unfortunately, you cannot test this theory, or any other complex theory, directly in one grand experiment. Consequently, researchers chip away at the problem by testing specific predictions of the theory. One of the most productive avenues of research has been to use optimal foraging theory to predict the composition of animal diets.

When ecologists consider potential prey for a consumer, they try to identify the prey attributes that may affect the rate of energy intake by the predator One of the most important factors is the abundance of a potential food item. All things being equal, a more abundant prey item yields a larger energy return than an uncommon prey. In optimal foraging studies, prey abundance is generally expressed as the number of the prey encountered by the predator per unit of time, Ne. Another prey attribute is the amount of energy, or costs, expended by the predator while searching for prey, Cs. A third characteristic of potential prey that could affect the energy return to the predator is the time spent processing prey in activities such as cracking shells, fighting, removing noxious scent glands, and so forth. Time spent in activities such as these are summarized as handling time, H. Ecologists ask, given the searching and handling capabilities of an animal and a certain array of available prey, Do animals select their diet in a way that yields the maximum rate of energy intake? We can rephrase this question mathematically by incorporating the terms for prey encounter rate, Ne, searching costs, Cs, and handling time, H, into a model.


A Model for Prey Choice

    We can represent the rate of energy intake of a predator as E/T, where E is energy and T is time. Earl Werner and Gary Mittelbach (1981) modeled the rate of energy intake for a

predator feeding on a single prey species as follows:

    In this equation, Nel is the number of prey I encountered per unit of time. El is the energy gained by feeding on an individual of prey 1 minus the costs of handling. Cs, is the cost of searching for the prey. Hi is the time required for "handling" an individual of prey 1. Once again, this equation expresses the net rate at which a predator takes in energy when it feeds on a particular prey species.

What would be the rate of energy intake if the predator fed on two types of prey? The rate is calculated as follows:

    This is an extension of the first equation. Here, we've added encounter rates for prey 2, Ne2, the energetic return from feeding on prey 2, E2, and the handling time for prey 2, H2. The searching costs, Cs, are assumed to be the same for prey I and prey 2.

The rate of energy intake by a predator feeding on several prey can be represented as:

Here, means "the sum of' and I equals 1, 2, 3, etc., to n, where n is the total number of prey. Remember that this equation gives an estimate of the rate of energy intake. The question that optimal foraging theory asks is whether organisms feed in a way that maximizes the rate of energy intake, E/T.

Optimal foraging theory predicts that a predator will feed

exclusively on prey I, ignoring other available prey, when:

This expression says that the rate of energy intake is greater if the predator feeds only on prey 1. If the predator feeds on both prey species, the rate will be lower.

Optimal foraging theory predicts that predators will include a second prey species in their diet when:

In this case, feeding on two prey species gives the predator a higher rate of energy intake than if it feeds on one. The general prediction is that predators will continue to add different types of prey to their diet until the rate of energy intake reaches a maximum. This is called optimization.

Now let's get back to our basic question: Do animals select food in a way that maximizes their rate of energy intake? Testing such a prediction requires a great deal of information. Fortunately, mathematical models such as this one help focus experiments and observations on a few key variables.


Foraging by Bluegill Sunfish

    Some of the most thorough tests of optimal foraging theory have been conducted on the bluegill sunfish, Lepomis macrochirus. The bluegill is a medium-sized fish native to eastern and central North America, where it inhabits a wide range of freshwater habitats, from small streams to the shorn-lines of small and large lakes. Bluegills feed mainly on benthic and planktonic crustaceans and aquatic insects, prey that differ in size and habitat and in ease of capture and handling. Bluegills often choose prey by size, feeding on organisms of certain sizes and ignoring others. This behavior is convenient because it gives the ecologist a relatively simple measure to describe the composition of the available prey and the composition of the theoretically optimal diet.

Werner and Mittelbach used published studies to estimate the amount of energy expended by bluegills while they search for (Cs) and handle prey. They used laboratory experiments to estimate handling times (H) and encounter rates (Ne) for various prey. For these laboratory experiments, they constructed approximations of the places where bluegills forage in nature---open water, sediments, and vegetation. These model habitats were constructed in large aquaria and stocked with some of the important prey of bluegills: damselfly larvae, midge larvae, and Daphnia. These experiments showed that encounter rates increase as fish size, prey size, and prey density increase and that handling time depends on the relative sizes of predator and prey. Small bluegills require a relatively long time to handle large prey, while large bluegills expend little time handling small prey.

The energy content of prey was calculated by measuring the lengths of prey available in lakes and ponds; prey length was converted to mass, and then mass was converted to energy content using published values. With this information, Werner and Mittelbach characterized the prey available in Lawrence Lake, Michigan, and then estimated the diet that would maximize the rate of energy intake. They then sampled the bluegills of Lawrence Lake and examined their stomach contents to see how closely their diet approximated the diet predicted by optimal foraging theory.

The upper graph in figure 6.24 shows the size distribution of potential prey in vegetation in Lawrence Lake. The middle graph shows the composition of the optimal diet as predicted by the optimal foraging model just presented. Finally, the bottom graph shows the actual composition of the diets of bluegills from Lawrence Lake. Bluegills feeding in vegetation selected prey that were uncommon and larger than average. The match between the optimal diet and the prey that bluegills in Lawrence Lake actually ate seems uncanny. A similar match was obtained for bluegills feeding on zooplankton in open Water.

FIGURE 6.24 Optimal foraging theory predicts composition of bluegill sunfish diets (data from Werner and Mittelbach 1981).

Werner and Mittelbach found that optimal foraging theory provides reasonable predictions of prey selection by natural populations of bluegills. Ecologists studying plants have developed an analogous predictive framework for foraging by plants.


Optimal Foraging by Plants

    How do plants "forage"? What animals do with behavior, plants do with growth. Plants forage by growing and orienting structures that capture either energy or nutrients. They grow leaves or other green surfaces to capture light and roots to capture nutrients. Terrestrial plants harvest energy from sunlight aboveground and nutrients and water from soil. Because of the structure of their environment and the distribution of their resources, plants forage in two directions at once. Like animals, however, plants face limited supplies of energy and nutrients and so face the prospect of compromises between competing demands for energy. Allocation of energy to leaves and stems reduces the amount of energy available for root growth. Increased allocation to root growth means less energy available for leaves and stems.

In some environments, such as the desert, plants have access to an abundance of light but face shortages of water In other environments, such as in the understory of temperate forests, there is little light but the soil may be rich in moisture and nutrients. In the face of such environmental heterogeneity, how do plants invest their energy? Using economic theory, Arnold Bloom and his colleagues (1985) suggested that plants adjust their allocation of energy to growth in such a way that all resources are equally limited. They predicted that plants in environments with abundant nutrients but little light would invest more energy in the growth of stems and leaves and less in roots to match their supply of energy to the supply of nutrients. They predicted that in environments rich in light but poor in nutrients, plants would invest more in roots.

The predictions of this economically based model have been supported by numerous studies showing that plants in light-poor environments invest more aboveground, while plants from nutrient-poor environments invest more below- ground. So, it appears that plants allocate energy for growth to those structures that gather the resources that most limit growth in a particular environment. Some of the most revealing tests of these predictions come from studies of plants growing along gradients of nutrient availability.

Experimental studies show that the same plant species grown in nutrient-poor soils often develop a higher ratio of root biomass to shoot biomass, the so-called root:shoot ratio, than when grown on nutrient-rich soils. For example, when H. Setala and V. Huhta (1991) grew birch tree seedlings in boreal forest soils of low and high nitrogen content, those in the nitrogen- poor soils developed higher root: shoot ratios (fig. 6.25).

FIGURE 6.25 Soil fertility and ratio of root biomass to shoot biomass (data from Setala and Huhta 1991).

David Tilman and M. Cowan (1989) obtained similar results when they grew four species of grass and four species of forbs on soils of different nitrogen content. They created a nitrogen gradient by mixing three different soils in different proportions. The soils were a subsoil (B horizon, see fig. 2.3) containing approximately 25 mg of nitrogen per kilogram of soil, a topsoil (A horizon) with 350 mg of nitrogen per kilogram of soil, and a black loam topsoil (A horizon) from a nearby site containing 5,000 mg of nitrogen per kilogram of soil. These soils were mixed to produce seven levels of soil nitrogen ranging from about 125 to 1,800 mg N per kilogram of soil. Several other nutrients were added to the experimental soils so that other nutrients would not limit growth of the experimental plants.

Tilman and Cowan conducted their growth experiments in 504 flowerpots that were 30 cm wide by 30 cm deep. They filled several pots with each of their seven soil mixtures and grew each of the eight study species from seed at high densities, 100 plants per pot, and low densities, 7 plants per pot. In each of the soil types, six pots of each species were planted at low density and three pots of each species at high density. Why did Tilman and Cowan plant several pots of each species in each of their growing conditions? Replicating their experimental conditions allowed them to test the statistical significance of their results.

The plants were grown outdoors in full sun and watered twice a week throughout the growing season except when there was adequate rain. The pots used for determining how nitrogen availability affects root: shoot ratios were maintained through two growing seasons. At the end of the second growing season, the researchers harvested the plants in these 280 pots, separating aboveground shoots from roots and carefully washing the soil from roots. They then dried roots and shoots for I week in an oven at 50. Finally, they weighed their dried samples and calculated root: shoot ratios of each study species grown at each nitrogen level.

Virtually all the species at both high and low densities had lower root: shoot ratios when grown with more nitrogen. Figure 6.26 shows the pattern for the grass Sorghastrumnutans when grown at high density. Like the other species, S. nutans reduced its root biomass and increased its shoot biomass in the presence of higher nitrogen availability. These results indicate that many plants modify their anatomy to match environmental circumstance in the direction predicted by economic theory.

FIGURE 6.26 Root: shoot ratios along a gradient of nitrogen availability (data from Tilman and Cowan 1989).

In summary, ecologists, using simple models of feeding behavior, have successfully predicted the feeding behavior of organisms as different as predatory animals and plants. Many animals forage in a way that tends to maximize their rate of energy intake. Meanwhile, plants, from birch trees to temperate grasses and forbs, appear to allocate energy to growth in a way that increases the rate at which they acquire those resources in shortest supply. While the optimal foraging approach to trophic ecology is far from complete, it is a substantial improvement over a body of knowledge consisting of a long list of species-specific descriptions of diet and feeding habits.

In the following example in the Applications and Tools section, we see how biologists are using some of the patterns and concepts we have discussed in chapter 6 to address important environmental problems.


APPLICATIONS AND TOOLS: bioremediation--using the trophic diversity of bacteria to solve environmental problems

    Imagine yourself in the center of a densely populated region with a mountain of sewage to dispose of or with thousands of leaky gasoline tanks contaminating the groundwater. How would you solve these environmental problems? Where would you turn for help? Increasingly, we are turning to nature's own cleanup crew, the bacteria. Environmental managers are taking advantage of the exceptional trophic diversity of bacteria to perform a host of environmental chores.


Removing a Mountain of Sewage

    Human populations produce prodigious amounts of sewage. Europe alone produces approximately 6 million tons per year. This sewage presents a tremendous disposal problem. Historically, much of this sewage was dumped into the sea, but European countries have agreed to stop this practice. Consequently, alternative disposal strategies must be developed, some of which are spreading sewage sludge on agricultural lands or burning it. Both these alternatives are expensive and both pose some environmental hazards because sewage is generally contaminated by heavy metals. One of the most promising disposal techniques involves bacteria.

John Pirt of Kings College London discovered bacteria living in horse manure that can break down sewage at temperatures of 80 (Coghlan 1993). He used these bacteria to develop a system for sewage disposal that alternates these high-temperature bacteria with bacteria that grow at 37.Pitt's system nearly eliminates the organic material in sewage sludge, leaving water and some mineral waste. The mineral waste contains heavy metal contaminants that can be isolated and either disposed of or recycled.

 In the first stage of the process, the high-temperature bacteria consume about 55% of the organic material in sewage sludge (fig. 6.27). Some of this organic matter is used as an energy source and converted into CO2 during respiration. The remainder is used as a source of carbon to construct more bacteria and is converted into bacterial biomass. The mixture of high-temperature bacteria and residual sludge from stage 1 is cooled to 37 and moved to another chamber. In stage 2, bacteria consume the biomass created by high-temperature bacteria in the previous stage and reduce the organic content of the material by another 5%. In the third stage high-temperature bacteria remove another 25% of the original organic matter. The remaining 15% of the organic matter is removed in the fourth stage of the process, which is carried out at 37.

FIGURE 6.27 Sewage digestion using bacteria with different temperature requirements (data from Coghlan 1993).

This process takes advantage of the biology of heterotrophic bacteria that use organic molecules as a source of energy and structural carbon. Some of the organic molecules are broken down into CO2 and H2O during respiration. Some are incorporated into the organic molecules that make up the bacteria. By using two different groups of bacteria in alternating high- and medium-temperature environments the system eventually converts almost all of the organic matter in sewage to carbon dioxide and water.

The process is projected to cost much less than burning sludge or spreading it on agricultural lands. It also prevents contamination with heavy metals. Pirt points out that he did not have to go to the far-off hot springs of Yellowstone National Park to find his thermophilic bacteria but just to the nearest pile of horse dung. As we shall see in the next two examples, other ecologists are using local bacteria to meet daunting environmental challenges.


Leaking Underground Storage Tanks

    Gasoline and other petroleum derivatives are stored in underground storage tanks all over the planet. Those that leak are a serious source of pollution. Madbeth Watwood and Cliff Dahm (1992) have been exploring the possibility of using bacteria to clean up soils and aquifers contaminated by leaking storage tanks. The first step in their work was to determine if there are naturally occurring populations of bacteria that can break down complex petroleum derivatives such as benzene.

Watwood and Dahm collected sediments from a shallow aquifer that contained approximately 8.5 x l08 bacterial cells per gram of wet sediment. Of these, 6.55 x 104 bacterial cells per milliliter were capable of living on benzene as their only source of carbon and energy. By exposing sediments from the aquifer to benzene for 6 months, the researchers increased the populations of benzene-degrading bacteria approximately 100 times.

How rapidly can these bacteria break down benzene? Watwood and Dahm found that with no prior exposure, becterial populations could break down 90% of the benzene in their test flasks within 40 days (fig. 6.28). Exposing sediments to benzene prior to their tests increased the rate of breakdown.

FIGURE 6.28 Benzene breakdown by soil bacteria (data from Watwood and Dahm 1992).

Briefly, this study demonstrated that naturally occurring populations of bacteria can rapidly break down benzene leaking from underground storage tanks. This study suggests that these bacteria will eventually clean up the organic contaminants from leaking gasoline storage tanks without manipulation of the environment. However, in the next example, environmental managers found that they had to manipulate the environment to stimulate the desired bacterial cleanup of a contaminant.


Cyanide and Nitrates in Mine Spoils

    Many gold mines were abandoned when they could not be mined profitably with the mining technology of the nineteenth and early twentieth centuries. Then, in the 1970s, techniques were developed to economically extract gold from low-grade ores. One of the main extraction techniques was to leach ore with cyanide (CN). Dissolved CN forms chemical complexes

with gold and other metals. The solution containing gold-bearing CN can be collected and the gold and CN removed by filtering the solution with activated charcoal.

This new method of mining solved a technical problem but contaminated soils and groundwater. When the leaching process is finished, the leached ore is stored in piles; however, much CN remains. Several kinds of bacteria can break down CN and produce NH3. This NH3 can, in turn, be used by nitrifying bacteria as an energy source, producing NO3. Thus, leaching gold-bearing ores and subsequent microbial activity can contaminate soil and groundwater with CN, a deadly poison, and with nitrate, another contaminant.

Carleton White and James Markwiese (1994) studied a gold mine that had been worked with the CN leaching process. The leached ores from the mine were gradually releasing CN and NO3 into the environment. The researchers looked to bacteria to solve this environmental problem. They first documented the presence of CN degraders by looking for bacterial growth in a diagnostic medium. This medium contained CN as the only source of carbon and nitrogen. Using, this growth medium, White and Markwiese estimated that each gram of ore contained approximately 103 to 105 cells of organisms capable of growing on CN.

The leached ores presented bacteria with a rich source of nitrogen in the form of CN and NO3 but the ores contained little organic carbon. White and Markwiese predicted that adding a source of carbon to the residual ores would increase the rate at which bacteria break down CN and reduce the concentration of NO3 in the environment. Why should adding organic molecules rich in carbon increase bacterial use of nitrogen in the environment? Look back at figure 6.7, which shows that bacteria have a carbon: nitrogen ratio of about 5:1. In other words, growth and reproduction by bacteria require about five carbon atoms for each nitrogen atom.

White and Markwiese tested their ideas in the laboratory. In one experiment, they added enough sucrose to pmduce a C:N ratio of 10:1 within leached ores. This experiment included two controls, both of which contained leached ores without sucrose. One of the controls was sterilized to kill any bacteria. The other control was left unsterilized.

Bacteria in the treatments containing sucrose broke down all the CN within the leached ore in l 3 days. Meanwhile, only a small amount of CN was broken down in the unsterilized control and no CN was broken down in the sterilized control (fig. 6.29). Why did the researchers include a sterilized control? The sterilized control demonstrated that nonbiological processes were not responsible for the observed break- down of CN.

FIGURE 6.29 Manipulating C:N ratios to stimulate breakdown of cyanide (CN) (data from White and Markwiese 1994).

Figure 6.29 shows that adding sucrose to the residual ore stimulates the breakdown of CN. However, remember that this process ultimately leads to the production of NO3. Does adding sucrose to eliminate CN lead to the buildup of NO3, trading one pollution problem for another? No, it does not. In another experiment White and Markwiese showed that adding sucrose also stimulates uptake of NO3 by heterotrophic bacteria and fungi. These organisms use organic molecules, in this case sucrose, as a source of energy and carbon and NO3 as a source of nitrogen. The nitrogen taken up by bacteria and fungi becomes incorporated in biomass as complex organic molecules. Nitrogen in this form is recycled within the microbial community and is not a source of environmental pollution.

White and Markwiese recommended that sucrose be added to leached gold-mining ores to stimulate breakdown of CN and uptake of NO3 by bacteria. This environmental cleanup project was successful because the researchers were thoroughly familiar with the energy and nutrient relations of bacteria and fungi. Another key to the project's success was the great trophic diversity of bacteria. Bacteria will likely continue to play a great role as we address some of our most vexing environmental problems.



    Organisms use one of three main sources of energy: light, inorganic molecules, or organic molecules. Photosynthetic plants and algae CO2 as a source of carbon and light, of wavelengths between 400 and 700 nm, as a source of energy. Light within this band, which is called photosynthetically active radiation, or PAR, accounts for about 45% of the total energy content of the solar spectrum at sea level. PAR can be quantified as photosynthetic photon flux density, generally reported as μmol per square meter per second. Among plants, there are three major alternative photosynthetic pathways, C3, C4, and CAM. C4 and CAM plants are more efficient in their use of water than are C3 plants. Heterotrophs use organic molecules both as a source of carbon and as a source of energy. Herbivores, caunivores, and detritivores face fundamentally different trophic problems. Herbivores feed on plant tissues. which often contain a great deal of carbon but little nitrogen. Herbivores must also overcome the physical and chemical defenses of plants. Detritivores feed on dead plant material, which is even lower in nitrogen than living plant tissues. Carnivores consume prey that are nutritionally rich but very well defended. Chemosynthetic autotrophs, which consist of a highly diverse group of chemosynthetic bacteria, use inorganic molecules as a source of energy. Bacteria are the most trophically diverse organisms in the biosphere.

The rate at which organisms can take in energy is limited, either by external or internal constraints. The relationship between photon flux density and plant photosynthetic rate is called photosynthetic response. Herbs and short-lived perennial shrubs from sunny habitats have high maximum photosynthetic rates that level on at high light intensities. The lowest maximum rates of photosynthesis occur among plants from shady environments. The relationship between food density and animal feeding rate is called the functional response. The shape of the functional response is generally one of three types. The forms of photosynthetic response curves and type 2 animal functional responses are remarkably similar. Energy limitation is a fundamental assumption of optimal foraging theory.

Optimal foraging theory attempts to model how organisms feed as an optimizing process. Evolutionary ecologists predict that if organisms have limited access to energy, natural selection is likely to favor individuals that are more effective at acquiring energy and nutrients. Many animals select food in a way that appears to maximize the rate at which they capture energy. Plants appear to allocate energy to roots versus shoots in a way that increases their rate of intake of the resources that limit their growth. Plants in environments with abundant nutrients but little light tend to invest more energy in the growth of stems and leaves and less in roots. In environments rich in light but poor in nutrients, plants tend to invest more energy in the growth of roots.

The trophic diversity of bacteria, which is critical to the health of the biosphere, can also be used as a tool to address some of our most challenging waste disposal problems. Bacteria can be used to eliminate the huge quantities of sewage produced by human populations, clean up soils and aquifers polluted by petroleum products such as benzene, and eliminate the pollution caused by some kinds of mine waste. The success of these projects requires that ecologists under- stand the energy and nutrient relations of bacteria. Bacteria will likely continue to play a great role as we address some of our most vexing environmental problems.



1. Why don't plants use highly energetic ultraviolet light for photosynthesis? Would it be impossible to evolve a photosynthetic system that uses ultraviolet light? Does the fact that many insects see ultraviolet light change your mind? Would it be possible to use infrared light for photosynthesis? (Photosynthetic bacteria tap into the near infrared range.)

2. In what kinds of environments would you expect to find the greatest predominance of C3, C4, or CAM plants? How can you explain the co-occurrence of two, or even all three, of these types of plants in one area? (Think about the variations in microclimate that we considered in chapters 4 and 5.)

3. In this chapter, we emphasized how the (24 photosynthetic pathway saves water, but some researchers suggest that the greatest advantage of C4 over C3 plants occurs when CO2 concentrations are low. What is the advantage of the C4 pathway when CO2 concentrations are low? As we shall see in chapter23, the atmospheric concentration of CO2 has been increasing for the last century or so. If this trend continues, and if the interactions between C4 and C3 plants are influenced by atmospheric CO2 concentrations, how might the geographic distributions of C3 and C4 plants change?

4. What are the relative advantages and disadvantages of being an herbivore, detritivore, or carnivore? What kinds of organisms were left out of our discussions of herbivores, detritivotes, and carnivores? Where do parasites fit? Where does Homo sapiens fit?

5. What advantage does advertising give to noxious prey? How would convergence in aposematic coloration among several species of Mullerian mimics contribute to the fitness of individuals in each species? In the case of Batesian mimicry, what are the costs and benefits of mimicry to the model and to the mimic?

6. Design a planetary ecosystem based entirely on chemosynthesis. You might choose an undiscovered planet of some distant star or one of the planets in our own solar system, either today or at some distant time in the past or future.

7. What kinds of animals would you expect to have type 1, 2, or 3 functional responses? How should natural selection for better prey defense affect the height of functional response curves? How should natural selection for more effective predators affect the height of the curves? What net effect should natural selection on predator and prey populations have on the height of the curves?

8. The rivers of central Portugal have been invaded, and densely populated, by the Louisiana crayfish, Procambarus clarki, which looks like a freshwater lobster about 12 to 14 cm long. The otters of these rivers, which were studied by Graca and Ferrand de Almeida (1983), can easily catch and subdue these crayfish. Using the model for prey choice:

explain why the diets of the otters of central Portugal would shift from the highly diverse menu shown in figure 6.15, which included fish, frogs, water snakes, birds, and insects, to a diet dominated by crayfish. For the ctayfish, assume low handling time, very high encounter rates, and high energy content.

9. The data of Iriarte and colleagues (1990) suggest that prey size may favor a particular body size among pumas (see fig. 6.16). However, this variation in body size also correlates well with latitude; the larger pumas live at high latitudes. Consequently, this variation in body size has been interpreted as the result of selection for efficient temperature regulation. Homeothermic animals are often larger at high latitudes, a pattern called Bergmann's rule. Larger animals, with lower surface area relative to their mass, would be theoretically better at conserving heat. Smaller animals, with higher surface area relative to their mass, would be theoretically better at keeping cool. So what determines predator size? Is predator size determined by climate, predator-prey interactions, or both? Design a study of the influence of the environment on the size of homeothermic predators.

10. How is plant allocation to roots versus shoots similar to plant regulation of temperature and water? (We discussed these topics in chapters 4 and 5.) Consider discussing these processes under the more general heading of homeostasis. (Homeostasis is the maintenance of a relatively constant internal environment in the face of variation in the external environment.)