2| History and Biogeography

2| History and Biogeography

Self-Replicating Molecular Assemblages

Life began with the first self-replicating molecular assemblage; moreover, natural selection begins to operate as soon as any complex of molecules starts making replicates of itself. No copying device is perfect, and some variants of the molecular assemblage produced are bound to be better than others in their abilities to survive and replicate themselves under particular environmental conditions. As resources become depleted, competition can occur among various self-replicating units. Furthermore, given enough time, some inferior variants presumably become extinct. Thus, each molecular unit maximizes its own numbers at the expense of other such units. Even as the originally simple self-replicating units become more and more elaborate and eventually attain the complex form of present-day organisms, the same principles of natural selection must remain in effect throughout. Thus, we can make certain statements about life that are entirely independent of the precise mechanism of replication. For example, self-replicating molecular assemblages elsewhere in the cosmos doubtlessly will not obey the laws of Mendelian genetics, yet their basic attributes as living material will not be drastically altered. Natural selection and competition are inevitable outgrowths of heritable reproduction in a finite environment. Hence, natural selection exists independently of life on earth. Many of the principles developed here will persist as long as assemblages of molecules replicate themselves anywhere in the cosmos.

Once a self-replicating entity arises, qualitatively new phenomena exist that are not present in an inanimate world. To reproduce, living organisms (or replicating molecular assemblages) must actively gather other materials and energy; that is, they must have some sort of acquisition techniques. Direct and indirect disputes over resources place those units best able to acquire materials and energy (and most successful at transforming them into offspring) at a selective advantage over other such units that are inferior at these processes. Thus, natural selection has the same effect as an efficiency expert, optimizing the allocation of available resources among conflicting demands imposed by foraging, growth, maintenance, and reproduction.

Obviously, the ultimate end point of these processes would be for the one best organismic unit to take over all matter and energy and to exclude all others. This has not occurred for a variety of reasons, as discussed earlier, but especially because of the great variability of the earth's surface, both in time and space. (Humans are making a good stab at it, however!)

The Geological Past

Climatic changes over geological time, called paleoclimatology, are of considerable ecological interest because organisms have had to evolve along with such changes. A really thorough ecological study must include consideration of the past history of the area under study. The earth has changed in innumerable ways during the geological past: the planet's orbital motion undergoes several complex celestial cycles measured on time scales of many thousands of years (Milankovitch cycles), its poles have shifted and wandered, periods of orogeny (mountain building) by tectonic upheaval of the earth's crust have waxed and waned at different places and times, the continents have "drifted" and moved on its mantle, and the planet itself has alternately warmed and cooled, the latter resulting in periods of extensive glaciation. Sea levels dropped during glacial periods as water accumulated on land as snow and ice (such sea level changes controlled by glacier alterations are called "eustatic"; see Figure 2.1).

  1. Figure 2.1. Estimates of sea level changes over the past 35,000 years from three different sources.
    [After Williamson (1981) by permission of Oxford University Press.]

Although it is difficult to trace such distant history, a variety of techniques, some of them quite ingenious, have been developed that allow us to deduce many of the changes that earth has undergone. One way to look into the past is to examine the fossil record. Lake sediments are an ideal source of layered fossils and have often been used to follow the history of an area. Fossilized pollens in a lake's sediments are relatively easily identified; pollens of plants adapted to particular types of climates can be used as indicators of past climates, as well as the types and composition of forests that prevailed near the lake at different times (see Figure 2.2). Of course, such palynological analyses are fraught with difficulties due to both variations between taxa in rates of pollen production and differential transport and deposition. Moreover, many deposits may contain mixtures of pollens from several different communities.

  1. Figure 2.2. Fossil pollen profiles from dated layers of lake sediments in northeastern United States for the period following the last ice age. Upper plot shows number of pollen grains of each species group as a percentage of the total sample. Lower plot gives estimated rates of deposition of each type of pollen and, at the right, the type of vegetation that probably prevailed in the area. [Adapted from Odum (1971) after M. Davis.]

A technique known as carbon dating allows estimation of the age of fossil plant remains, including pollens and charcoal. Solar radiation converts some atmospheric nitrogen into a radioactive isotope of carbon called carbon 14 (14C). This 14C is oxidized to carbon dioxide and is taken up by plants in photosynthesis in proportion to its abundance in the air around the plant. All radioactive isotopes emit neutrons and electrons, eventually decaying into nonradioactive isotopes. Half of a quantity of 14C becomes nonradioactive carbon 12 (12C) each 5600 years (this is the half-life of 14C). When a plant dies, it contains a certain maximal amount of 14C. Comparison of the relative amounts of 14C and 12C in modern-day and fossil plants allows estimation of the age of a fossil. Thus, a fossil plant with half the 14C content of a modern plant is about 5600 years old, one with one-quarter as much 14C is 11,200 years old, and so on. The carbon dating method has been checked against ancient Egyptian relics of known age made from plant materials; it accurately estimates their ages, confirming that the rate of production of 14C and the proportion of 14C to 12C have not changed much over the last 5000 years. The technique allows assignment of fairly accurate ages to all sorts of recently fossilized plant materials. Other methods of radiometric dating, such as uranium-lead, uranium-thorium, and potassium-argon dating, allow older materials to be dated.

A similar dating technique makes use of the observation that the uptake of two oxygen isotopes, 16O and 18O, into carbonates is temperature dependent. Thus, the proportion of these two isotopes in a fossil seashell presumably reflects the temperature of an ancient ocean in which that particular mollusk lived.

The geological time scale is summarized in Table 2.1. Several major episodes of extinction stand out in the fossil record (Figure 2.3). These events are so striking that they are used to mark the boundaries between geological periods: (1) 70 percent of marine life went extinct at the Paleozoic-Mesozoic boundary, (2) the last dinosaurs went extinct at the Mesozoic-Tertiary transition, and (3) over many different parts of the planet, numerous species of large mammals1 died out rather suddenly and dramatically near the end of the Pleistocene ice ages.

Table 2.1 The Geological Time Scale


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Years in millions
since beginning of
Eras Periods Epochs period or epoch


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Quaternary Recent0.1
Pleistocene 1.6
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CenozoicPliocene5
Miocene 22
Tertiary Oligocene36
Eocene 55
Paleocene 65
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Cretaceous144
MesozoicJurassic192
Triassic245
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Permian290
Carboniferous360
Devonian408
PaleozoicSilurian435
Ordivician485
Cambrian570
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Precambrian4600
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Long geological periods without major extinctions, followed by abrupt periods of massive extinctions, are known as "punctuated equilibria." These widespread extinctions markedly altered almost all ecological communities. Moreover, their synchrony demands attention, since it strongly suggests general underlying causal explanations. Perhaps the most intriguing of those suggested for the extinction of the dinosaurs is the asteroid impact hypothesis (Alvarez et al. 1980), which asserts that extraterrestrial dust from a large comet drastically decreased incident solar radiation and hence primary productivity (this would also have made the planet colder). In support of this hypothesis, a thin fossil layer of iridium, a rare element on the earth but one that is more abundant in meteorites, has been found at widespread localities around the planet dating from this period.

Intriguing speculation has also been offered for the Pleistocene mammal extinctions (Martin and Wright 1967), including the possibility of "overkill" by prehistoric humans (Martin 1967), although climatological events must certainly have played a major role as well (Guilday 1967; Graham 1986). Pleistocene assemblages of small mammals seem to have been more diverse and fundamentally different than modern ones (Graham 1986).

  1. Figure 2.3. Marine extinctions in the fossil record. V = Precambrian, C = Cambrian,
    O = Ordivician, S = Silurian, D = Devonian, C = Carboniferous, P = Permian, TR = Triassic,
    J = Jurassic, K = Cretaceous, T = Tertiary (see Table 2.1) [After Erwin et al. (1987).]

South America was virtually completely isolated for most of the past 70 million years. In the absence of many major groups of placentals, a rich fauna of marsupials, including a saber-toothed catlike predator, evolved over this long time period. Edentates and proto-ungulates were present, and a rodent, a monkey, and a small raccoon-like carnivore did eventually reach the isolated continent. When the isthmus of Panama was formed about 3 million years ago, numerous different taxa of land and freshwater organisms were exchanged between North America and South America (this process has been termed the "great American biotic interchange"). Although Central America has since come to be dominated by South American elements, the impact of the North American fauna on South America was much more profound than the effect of the South American biota on that of North America. Many South American marsupial species went extinct, although a few ancient lineages persisted. South American mammals that have successfully invaded North America include the armadillo, opossum, and porcupine.

Reasons for many of the earth's past changes, such as polar movements and the alternate warming and cooling of the planet, are little known and may well involve solar changes. Piecing together all this diverse and sometimes conflicting evidence on the earth's past history is a most difficult and challenging task and one that occupies many fine minds.

Classical Biogeography

A major goal of ecology is to understand various factors influencing the present distribution and abundance of animals and plants (Andrewartha and Birch 1954; Krebs 1972; MacArthur 1972). Factors affecting abundances and microgeographic distributions (including habitat selection) will be considered later; here, we examine more gross geographic distributions -- the spatial distributions of plants and animals over large geographic areas such as major landmasses (continents and islands). The study of the geographical distributions of plants and animals, respectively, are termed phytogeography and zoogeography. Biogeography encompasses the geography of all organisms and involves a search for patterns in the distributions of plants and animals and an attempt to explain how such patterns arose during the geological past. In addition to classifying present distributions, biogeographers seek to interpret and to understand past movements of organisms. Ecology and biogeography are closely related and overlapping disciplines and have profoundly affected one another.

When early naturalists traveled to different parts of the world, they quickly discovered distinctly different assemblages of species. As data were gathered on these patterns, six major biogeographic "realms" or regions were recognized, three of which correspond roughly to the continents of Australia (Australian), North America north of the Mexican escarpment (Nearctic), and South America south of the Mexican escarpment (Neotropical). (The Neotropical region also includes the Antilles.) Africa south of the Sahara is known as the Ethiopian region. Eurasia is divided into two regions, the Palearctic north of the Himalayas (which includes Africa north of the Sahara desert) and the Oriental south of the Himalayas (India, southern China, Indochina, the Philippines, and Borneo, Java, Sumatra, and other islands of Indonesia east to, and including, the Celebes). Each of the six biogeographic regions (Figure 2.4) is separated from the others by a major barrier to the dispersal of plants and animals, such as a narrow isthmus, high mountains, a desert, an ocean, or an oceanic strait. There is generally a high degree of floral and faunal consistency within regions and a marked shift in higher taxa such as genera and families in going from one region to another. Although biogeographers familiar with different plant and animal groups often disagree on the exact boundaries between regions (Figure 2.5), there is broad agreement on the usefulness of recognizing these six major regions. High species diversities in the tropics, among other things, have led to the notion that speciation rates in these areas must be extremely high and that such regions often constitute "source areas" for production of new species, many of which then migrate into less hospitable areas, such as the temperate zones. Thus, Darlington (1957, 1959) proposed the "area-climate hypothesis," which states that most dominant animal species have arisen in geographically extensive and climatically

  1. Figure 2.4. The six major biogeographic regions of the world.
  2. Figure 2.5. Wallace's and Weber's "lines" in southeast Asia, which separate the Oriental from the Australian regions. The position of the volcanic island of Krakatau between Sumatra and Java is indicated at the lower left.

favorable areas; he considered the Old World Tropics, which include the tropical portions of the Ethiopian and Oriental regions, to be the major source area for most vertebrate groups and argued that such dominant forms have migrated centrifugally to other smaller and less favorable areas, including Europe, North and South America, and Australia.

Classical biogeography has produced several so-called biogeographic rules based on recurring patterns of adaptation of organisms. Thus, homeotherms living in cold climates are often larger than those from warmer regions. Such a trend or cline can even be demonstrated within some wide-ranging species. This tendency, termed Bergmann's rule after its discoverer, has a probable causal basis in that large animals have less surface per unit of body volume than small ones, resulting in more efficient retention of body heat. Many other biogeographic rules have also been proposed, all of which are basically descriptive. Allen's rule states that the appendages and/or extremities of homeotherms are either longer or have a larger area in warmer climates; a jackrabbit, for example, has much longer and larger ears than an arctic hare. The presumed functional significance is that large appendages, having a larger relative surface area, are better at heat dissipation than smaller ones. Another rule (Gloger's) asserts that animals from hot, dry areas tend to be paler than those from colder, wetter regions. Still another biogeographic rule is that fish from colder waters often have more vertebrae than those from warmer waters. The adaptive significance of many of these biogeographic trends remains obscure, although such geographically variable phenotypic traits are frequently developmentally flexible and respond more or less directly to temperature.

Continental Drift

Much of this classical biogeography assumed some permanence in the locations of continents. As a result, interpretations of faunal similarities between them often relied on hypothetical mechanisms of transport from one continent to another, such as "rafting" of organisms across water gaps. Such long-distance dispersal events are exceedingly improbable, although they must occur from time to time (cattle egrets, for example, apparently made a successful transatlantic crossing from Africa to South America without human assistance late in the 18th century).

Massive movements of the continents themselves were first suggested by Taylor (1910), but his bold hypothesis was not widely accepted.2 Wegener is usually credited with the idea of continental drift. Recent advances in geology indicate that the continents were once joined in a large southern landmass (Pangaea) and have "drifted" apart (Figure 2.6), with a gradual breakup that began in the early Mesozoic era (about 200 million years ago). Geological evidence that the continents have drifted (and are now drifting) is now extensive (Hallam 1973; Marvin 1973; J. T. Wilson 1973; Skinner 1986). Smaller fragments of land, known as "suspect terraines," also appear to have moved.


  1. Figure 2.6. Approximate positions of major landmasses at different times in the geological past, showing their probable movements. [Adapted from Dietz and Holden (1970). The Breakup of Pangaea. Copyright © 1970 by Scientific American, Inc. All rights reserved.]

Certain types of rocks, particularly basalts, retain a magnetic "memory" of the latitude in which they were solidified. Such paleomagnetic evidence allows mapping of the past position of the North Pole. (An intriguing but as yet still unexplained phenomenon has been discovered: reversals in magnetic polarity occur in geological time, the last of which has been dated at 700,000 years ago.) Recent rocks from different locations coincide in pinpointing the pole's position, but paleomagnetic records from older rocks from different localities are in discord. These discrepancies strongly suggest that the continents have moved with respect to one another. The continents are formed of light "plates" of siliceous, largely granitic, rocks about 30 km thick, which in turn float on denser mantlelike basaltic blocks. The ocean floors are composed of a relatively thin altered top of the earth's mantle. A mountain range of the seafloor in the mid-Atlantic represents a region of upwelling of the mantle. Under this interpretation, as the upwelling proceeds, seafloors spread and continents move apart (Figure 2.7). The positions of paleomagnetic anomalies (polarity reversals) in the seafloor allow geologists to calculate the velocity of lateral motion of the ocean floors, which correspond to comparable estimates for the landmasses. Thus, modern theory holds that, except for the Pacific (which is shrinking), the oceans are growing, with very young ocean floors in midocean and progressively older floors toward the continents. Other evidence, such as the apparent ages of islands and the depths of sediments, nicely corroborate this conclusion.

  1. Figure 2.7. Diagrammatic cross-sectional view of the probable movements of the earth's mantle and crust that led to seafloor spreading and continental drift. Upwelling of deep mantle materials in the mid-Atlantic is accompanied by a surface movement away from the mid-oceanic ridge. The continents, which float on top of these moving denser materials, are carried along. At the oceanic trench on the far left, these materials sink back down a subducting zone into the mantle, forming a closed system of circulating materials.

Much of classical biogeography is being reinterpreted in light of these new findings. For example, certain very ancient groups of plants, freshwater lungfishes, amphibians, and insects that had spread before the breakup of the continents now occur on several continents, whereas many other more recently evolved groups of plants and animals, such as mammals and birds, are restricted to particular biogeographic regions. These latter, more recent groups follow the regional divisions much more closely than the older groups (Kurtén 1969).

Imagine the effects of changing climates on plants and animals as continents drift through different latitudes! The Indian subcontinent changed from south temperate to tropical to north temperate and was virtually a "Noah's ark" carrying a flora and fauna. Australia became arid as it drifted into the mid latitudes; moreover, as this landmass continues to move toward the equator, its climate will gradually become wetter and more tropical.

Selected References

Self-Replicating Molecular Assemblages

Bernal (1967); Blum (1968); Calvin (1969); Ehrlich and Holm (1963); Fox and Dose (1972); Oparin (1957); Ponnamperuma (1972); Salthe (1972); Wald (1964).

The Geological Past

Alvarez et al. (1980); Birch and Ehrlich (1967); Brown (1982); Dansereau (1957); Darlington (1957, 1965); Dietz and Holden (1970); Erwin et al. (1987); Graham (1986); Guilday (1967); Hesse, Allee, and Schmidt (1951); Imbrie et al. (1984); Jelgersma (1966); Martin (1967); Martin and Klein (1984); Martin and Mehringer (1965); Martin and Wright (1967); Olsen (1983); Sawyer (1966); Skinner (1986); Stehli and Webb (1985); Tarling (1983); Udvardy (1969); Wilson (1971, 1973); Wiseman (1966); Wright and Frey (1965).

Classical Biogeography

Andrewartha and Birch (1954); Cain (1944); Dansereau (1957); Darlington (1957, 1959, 1965); Grinnell (1924); Hesse, Allee, and Schmidt (1951); Krebs (1972); MacArthur (1959, 1972); MacArthur and Wilson (1967); Nelson and Platnick (1981); Newbigin (1936); Schall and Pianka (1978); Terborgh (1971); Udvardy (1969); Wallace (1876); Watts (1971).

Continental Drift

Cracraft (1974); Dietz and Holden (1970); DuToit (1937); Kurtén (1969); Hallam (1973); Marvin (1973); Skinner (1986); Tarling and Runcorn (1975); Skinner (1986); Taylor (1910); Wegener (1924); J. T. Wilson (1971, 1973).


1. These megafauna include antelope, buffalo, camels, wild oxen, wild pigs, rhinoceros, tapirs, giant sloths, cave bears, as well as mammoths, mastodons, and saber-toothed cats.

2. Taylor speculated that our moon was captured by the earth, causing an increase in the speed of rotation, which in turn "pulled" the continents away from the poles and "threw" them toward the equator. He suggested, probably correctly, that the Himalayan mountains were formed by the collision of two tectonic plates.


3| Meteorology

3|Meteorology

Earth's Physical Environment

Earth supports an enormous variety of organisms. Plants range from microscopic short-lived aquatic phytoplankton to small annual flowering plants to larger perennials to gigantic ancient sequoia trees. Animals, although they never attain quite the massive size of a redwood tree, include forms as diverse as marine zooplankton, jellyfish, sea stars, barnacles, clams, snails, beetles, butterflies, worms, frogs, fish, lizards, sparrows, hawks, bats, elephants, whales, and lions. Different species have evolved and live under different environmental conditions. Some organisms are relatively specialized either in the variety of foods they eat or in the microhabitats they exploit, whereas others are more generalized; some are widespread, occurring in many different habitats, whereas still others have more restricted habitat requirements and geographic ranges. Temporal and spatial variation in the physical conditions for life often make possible or even actually necessitate variety among organisms, both directly and indirectly. Of course, interactions among organisms also contribute substantially to the maintenance of this great diversity of life.

Before considering such biological interactions, we first examine briefly the nonliving world, which sets the background for all life and often strongly influences the ecology of any particular organismic unit. A major factor in the physical environment is climate, which in turn is the ultimate determinant of water availability and the thermal environment; moreover, the latter two interact to determine the actual amount of solar energy that can be captured by plants (primary productivity) at any given time and place. Finally, because climate is a major determinant of both soils and vegetation, there is a close correspondence between particular climates and the types of natural biological communities that exist under those climatic conditions. Populations of many species are directly affected by climate. The interface between climate and vegetation is considered in Chapter 4.

Major global and local patterns of climate are described briefly in this chapter. Entire books have been devoted to some of these subjects, and the reader interested in greater detail is referred to the references at the end of the chapter.

Major Determinants of Climate

The elements of climate (sun, wind, and water) are complexly interrelated. Incident solar energy produces thermal patterns that, coupled with the earth's rotation and movements around its sun, generate the prevailing winds and ocean currents. These currents of air and water in turn strongly influence the distribution of precipitation, both in time and space.

The amount of solar energy intercepting a unit area of the earth's surface varies markedly with latitude for two reasons. First, at high latitudes, a beam of light hits the surface at an angle, and its energy is spread out over a large surface area. Second, a beam that intercepts the atmosphere at an angle must penetrate a deeper blanket of air, and hence more solar energy is reflected by particles in the atmosphere and radiated back into space. (Local cloud cover also limits the amount of the sun's energy that reaches the ground.) A familiar result of both these effects is that average annual temperatures tend to decrease with increasing latitude (Table 3.1). The poles are cold and the tropics are generally warm (seasons are discussed later).

Table 3.1 Average Annual Temperature (° C) at Different Latitudes

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Latitude Year January July Range

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90°N -22.7 -41.1-1.1 40.0
80°N -18.3 -32.2 2.0 34.2
70°N -10.7 -26.3 7.3 33.6
60°N -1.1 -16.114.1 30.2
50°N 5.8 -7.118.1 25.2
40°N 14.1 5.024.0 19.0
30°N 20.4 14.527.3 12.8
20°N 25.3 21.828.0 6.2
10°N 26.7 25.827.2 1.4
Equator 26.2 26.425.6 0.8
10°S 25.3 26.323.9 2.4
20°S 22.9 25.420.0 5.4
30°S 16.6 21.914.7 7.2
40°S 11.9 15.6 9.0 6.6
50°S 5.8 8.13.4 4.7
60°S -3.4 2.1-9.1 11.2
70°S -13.6 -3.5-23.0 19.5
80°S -27.0 -10.8-39.5 28.7
90°S -33.1 -13.5-47.8 34.3

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Water in the atmosphere is warmed by heat radiating from the earth's surface, and much of this heat is radiated back to the earth again. The result is the so-called greenhouse effect, which leads to the retention of heat, keeping the earth relatively warm even at night when there is temporarily no influx of solar energy. Without this effect, the earth's surface would cool to many degrees below zero -- like the dark side of the moon's surface. Thus, the atmosphere buffers day-night thermal change.

  1. Figure 3.1. Estimated amount of incoming solar radiation that would intercept the earth's surface in the absence of an atmosphere as a function of latitude. The six-month period from the spring equinox to the fall equinox (see Figure 3.7) is labeled "northern summer" and "southern winter," whereas the six months from the fall equinox to the spring equinox represent the "northern winter" and the "southern summer." [After Haurwitz and Austin (1944).]

Hot air rises. The ground and air masses above it receive more solar energy at low latitudes than at higher ones (Figure 3.1). Thus, tropical air masses, especially those near the equator, are warmed relatively more than temperate air masses, and an equatorial zone of rising air is created. These equatorial air masses cool as they rise and eventually move northward and southward high in the atmosphere above the earth's surface (Figure 3.2a). As this cold air moves toward higher latitudes, it sinks slowly at first and then descends rapidly to the surface at the so-called horse latitudes of about 30°N and 30°S. At ground level at these latitudes, some air moves toward the equator again and some of it moves toward the poles. (The amount of air in the atmosphere is finite, so air masses leaving one place must always be replaced by air coming from somewhere else; thus, a closed system of circulating air masses is set up.) An idealized diagram of the typical vertical and horizontal movements of atmospheric currents is shown in Figure 3.2.

At the surface, the equator is a zone of convergence of air masses, whereas they are diverging at the horse latitudes. Between latitudes 0° and 30°, surface air usually moves toward the equator; between latitudes 30° and 60°, it generally moves away from the equator. As air masses move along the surface, they are slowly warmed and eventually rise again.

(a)

  • Figure 3.2. Idealized atmospheric circulation patterns. (a) Vertical profile against latitude. Dashed ellipses represent positions of jet streams. (b) Prevailing wind currents on the earth's surface. Belts of moving air move north and south with the seasons. [After MacArthur (1972).]
  • Movements of air masses are not strictly north-south as suggested by Figure 3.2a; instead, they acquire an east-west component due to the rotation of the earth about its axis (Figure 3.2b). The earth rotates from west to east. A person standing on either pole would rotate slowly around and do a full "about face" each 12 hours. (Near the North Pole the ground moves counterclockwise under one's feet, whereas near the South Pole it moves clockwise; other related important differences between the hemispheres are considered in the following paragraphs.) However, someone located near the equator travels much farther during a 24-hour period; indeed, such a person would traverse a distance equal to the earth's circumference, or about 40,000 km, during each rotation of the globe. Hence, the velocity of a body near the equator is approximately 1600 kilometers/hour (relative to the earth's axis), whereas a body at either pole is, relatively speaking, at a standstill.

    Previous considerations, plus the physical law of conservation of momentum, dictate that objects moving north in the Northern Hemisphere must speed up, relative to the earth's surface, and thus veer toward the right. Similarly, objects moving south in the Northern Hemisphere slow down relative to the earth's surface, which means that they also veer to the right. In contrast, moving objects in the Southern Hemisphere always veer to the left; northward-moving objects slow down and southward-moving ones speed up. These forces, known collectively as the Coriolis force, act on north-south wind and water currents to give them an east-west component. The Coriolis force is maximal at the poles, where a slight latitudinal displacement is accompanied by a large change in velocity, and minimal at the equator, where a slight latitudinal change has little effect upon the velocity of an object.

    Equator-bound surface air between latitudes 0° and 30° slows relative to the surface and veers toward the west in both hemispheres, producing winds from the east ("easterlies"); these constitute the familiar trade winds, known as the northeast trades between 0° and 30°N and the southeast trades between 0° and 30°S. Between latitudes 30° and 60°, surface air moving toward the poles speeds up (again, relative to the earth's surface) and veers toward the east, producing the familiar prevailing "westerly" winds at these latitudes in both hemispheres (Figure 3.2b).

    These wind patterns, coupled with the action of the Coriolis force on water masses moving north to south, drive the world's ocean currents; in the Northern Hemisphere, ocean waters rotate generally clockwise, whereas they rotate counterclockwise in the Southern Hemisphere (Figure 3.3).

    1. Figure 3.3. Major surface currents of the world's oceans.

    During their movement westward along the equator, oceanic waters are warmed by solar irradiation. (These waters also "pile up" on the western sides of the oceanic basins; in Central America, the sea level of the Atlantic is about a meter higher than that of the Pacific.) As this warm equatorial water approaches the eastern side of landmasses, it is diverted northward and/or southward to higher latitudes, carrying equatorial heat toward the poles along the eastern coasts of continents. Cold polar waters flow toward the equator on west coasts (this is the main reason the Pacific Ocean off southern California is cold but at the same latitude the Atlantic Ocean off Georgia is quite warm).

    Heat is molecular movement. Compressing a volume of air results in more collisions between molecules and increased molecular movement; hence, compression causes an air mass to heat up. Exactly analogous considerations apply in the reverse case. Allowing compressed air to expand decreases the number of molecular collisions and the air mass cools off. As warm air rises, atmospheric pressure decreases, and the air expands and is cooled "adiabatically," or without change in total heat content. Some of the air's own heat is used in its expansion. As descending cold air is compressed, it is adiabatically warmed in a similar manner.

    1. Figure 3.4. Histogram of average annual precipitation versus latitudinal zones. Note the effect of the earth's major deserts in the horse latitudes. [From Haurwitz and Austin (1944).]

    Warm air can carry more water vapor than cold air. As warm, water-laden equatorial air rises and cools adiabatically, it first becomes saturated with water at its dew point, and then its water vapors condense to form precipitation. As a result, regions of heavy rainfall tend to occur near the equator (Figure 3.4). In contrast, at the horse latitudes, as cold dry air masses descend and warm adiabatically, they take up water; such desiccating effects help to produce the earth's major deserts at these latitudes (see Figures 3.4 and 3.5). Deserts occur mainly on the western sides of continents, where cold offshore waters are associated with a blanket of cold, and therefore dry, air; westerly winds coming in off these oceans do not contain much water to give up to the descending dry air, and precipitation must therefore be scanty. The global pattern of annual precipitation shown in Figure 3.5 conforms in general outline to the expected, but there are many local anomalies and exceptions.

    1. Figure 3.5. Geographic distribution of average annual precipitation.
      [After MacArthur and Connell (1966) after Koeppen.]

    Local Perturbations

    Major climatic trends are modified locally by a variety of factors, most notably by the size(s) and position(s) of nearby water bodies and landmasses and by topography (especially mountains). Ascending a mountain is, in many ways, comparable to moving toward a higher latitude. Mountains are usually cooler and windier than adjacent valleys and generally support communities of plants and animals characteristic of lower elevations at higher latitudes (100 meters of elevation corresponds roughly to 50 kilometers of latitude). In addition to this thermal effect, mountains markedly modify water availability and precipitation patterns. Water rapidly runs off a slope but sits around longer on a flatter place and soaks into the ground. For this reason, precipitation falling on a mountainside is generally less effective than an equivalent amount falling on a relatively flat valley floor. Precipitation patterns themselves are also directly affected by the presence of mountains. Consider a north-south mountain range receiving westerly winds, such as the Sierra Nevada of the western United States. Air is forced upward as it approaches the mountains, and as it ascends, it cools adiabatically, becomes saturated with water, and releases some of its water content as precipitation on the windward side of the Sierra. After going over the ridge, this same air, now cold and dry, descends, and, as it warms adiabatically, it sucks up much of the moisture available on the leeward (downwind) side of the mountains. The so-called rainshadow effect (Figure 3.6) is produced, with windward slopes being relatively wet and leeward slopes being much drier. Desiccating effects of these warm dry air masses extend for many miles beyond the Sierra and help to produce the Mojave Desert in southern California and Nevada.

    1. Figure 3.6. Illustration of the "rainshadow" effect of the Sierra Nevada in central California.

    Water has a high specific heat; that is, a considerable amount of heat energy is needed to change its temperature. Conversely, a body of water can give up a relatively large amount of heat without cooling very much. A result of these heat "sink" attributes is that large bodies of water, particularly oceans, effectively reduce temperature changes of nearby landmasses. Thus, coastal "maritime" climates are distinguished from inland "continental" climates, with the former being much milder and less variable. Large lakes, such as the Great Lakes, also decrease thermal changes on adjacent landmasses and produce a more constant local temperature.

    Variations in Time and Space

    The seasons are produced by the annual elliptical orbit of the earth around its sun and by the inclination of the planet's axis relative to this orbital plane (Figure 3.7). These orbital movements do not repeat themselves exactly but follow a complex celestial periodicity measured on a time scale of many thousands of years (Milankovitch cycles). For historical reasons, these movements and patterns have been described from the point of view of the Northern Hemisphere, although by symmetry the same events occur some six months out of phase in the Southern Hemisphere. Twice each year, at the vernal equinox (March 21) and the autumnal equinox (September 22), solar light beams intercept the earth's surface perpendicularly on the equator (i.e., the sun is "directly overhead" at its zenith and equatorial shadows point exactly east to west).

    1. Figure 3.7. Diagram of the earth's annual elliptical orbit around the sun, which produces the seasons.
      [After MacArthur and Connell (1966).]

    At two other times of year, the summer solstice (June 22) and the winter solstice (December 22), the earth's axis is tilted maximally with respect to the sun's rays. Viewed from the Northern Hemisphere, the axis at present inclines approximately 23.5° toward the sun during the summer solstice and 23.5° away from it during the winter solstice (this angle of inclination itself varies cyclically between 22° and 24.5°, with a periodicity of about 41,000 years). At each of the solstices, rays of light hit the surface perpendicularly (the sun is at its zenith) near the Tropic of Cancer (23°N) and the Tropic of Capricorn (23°S), respectively. At summer solstice, the North Pole is in the middle of its six-month period of sunlight (the "polar summer"). The excess of daylight in summer is exactly balanced by the winter deficit, so the total annual period of daylight is precisely six months at every latitude; the equator has invariate days of exactly 12 hours duration, whereas the poles receive their sunshine all at once over a six-month interval and then face six months of twilight and total darkness. Day length is one of the most dependable indicators of seasonality and many temperate zone plants and animals rely on photoperiod as an environmental cue (Figure 3.8).

    1. Figure 3.8. Seasonal changes in photoperiod at different latitudes. [After Sadleir (1973).]

    Of course, prevailing winds and ocean currents are not static, as suggested by Figures 3.2 and 3.3; in fact, they vary seasonally with the earth's movement about its sun (Figure 3.9). The latitudinal belt receiving the most solar radiation (the thermal equator) gradually shifts northward and southward between latitudes 23°S and 23°N; moreover, latitudinal belts of easterlies and westerlies also move northward and southward with the seasons, producing seasonal weather changes at higher latitudes. Because of the earth's spherical shape, seasonal changes in insolation increase markedly with increasing latitude.

    Although temperatures are modified by prevailing winds, topography, altitude, proximity to bodies of water, cloud cover (Figure 3.10), and other factors, annual marches of average daily temperatures at any given place nevertheless closely reflect earth's movement around the sun. Thus, average daily temperatures on the equator change very little seasonally, whereas those at higher latitudes usually fluctuate considerably more; moreover, the annual range in temperature is also much greater in the temperate zones (Table 3.1).

    Annual patterns of precipitation also reflect earth's orbital movements (Figure 3.11), although precipitation patterns are perhaps modified locally more easily than thermal patterns. At very low latitudes, say, l0°S to l0°N, there are often two rainfall maxima each year (Figure 3.12a), one following each equinox as the region of rising air (the thermal equator) passes over the area. Thus, the sun's passing over these equatorial areas twice each year produces a bimodal annual pattern of precipitation. Bimodal annual precipitation patterns also occur in other regions at higher latitudes, such as the Sonoran Desert in Arizona (Figure 3.12b), but for different reasons. However, not all equatorial areas have such a rainfall pattern, and some have only one rainy season each year (Figure 3.12c).

    1. Figure 3.9. Precipitation zones vary latitudinally in a more-or-less regular fashion, as indicated. [After Haurwitz and Austin (1944).]

    During summer, air masses in the central parts of continents at high latitudes tend to warm faster than those around the periphery, which are cooled somewhat by nearby oceans. As hot air rises from the center of continents, a "low" pressure area is formed and cooler, but still warm and water-laden, coastal air can be drawn in off the oceans and coastlines. When this moist air is warmed over the land, it rises, cools adiabatically, and releases much of its water content on the interiors of continents. Thus, continental, in contrast to coastal, climates are often characterized by summer thunderstorms (Figure 3.12d). In winter, as the central regions of continents cool relative to their water-warmed edges, a "high" pressure area develops and winds reverse, with cold dry air pouring outward toward the coasts. Stationary high pressure areas arise during hot summers in the interior of continents forming a dome of hot air that compresses air at the surface and holds in heat. These domes are held in place by dry heavier colder air and jet streams to the north, and by hot, humid air from the Gulf of Mexico on the south. These air masses circulate clockwise around the dome, holding the dome in place.

    1. Figure 3.10. Cloud cover reduces both the amplitude and the extremes of the daily march of temperature. [After Haurwitz and Austin (1944).]
    1. Figure 3.11. Annual marches of average daily temperature at an equatorial locality (Batavia) and two temperate areas, one coastal (Scilly) and one continental (Chicago). [After Haurwitz and Austin (1944).]

    A weather "front" is produced when a cold (usually polar) air mass and a warm air mass collide. The warmer lighter air is displaced upward by the heavy cold air; as this warm air rises, it is cooled adiabatically, and provided it contains enough water vapor, reaches its dewpoint, forming clouds and eventually producing precipitation. Such fronts typify the boundaries between the polar easterlies and the midlatitude westerlies, which move north to south with the seasons as shown in Figure 3.9.

    1. Figure 3.12. Annual marches of average yearly precipitation from eight selected localities (see text). (a) Bimodal equatorial rainfall. (b) Bimodal annual precipitation pattern of the Sonoran Desert. (c) Unimodal annual rainfall pattern of an equatorial area. (d) Typical continental summer rainfall regime. (e) Coastal area with winter precipitation. (f) Typical maritime rainfall regime with more winter precipitation than summer rain. (g) The annual march of precipitation in eastern North America is distributed fairly evenly over the year. (h) An area with a pronounced summer drought that would support a chaparral vegetation. [After Haurwitz and Austin (1944).]

    The seasonality of coastal rainfall is affected by the differential heating of land and water in another, almost opposite, way. At high latitudes, say, 40° to 60°, land-masses cool in winter and become much colder than offshore oceans; along the west coasts of continents, water-rich westerly winds coming in off such a relatively warm ocean are rapidly cooled when they meet a cold landmass and hence deposit much of their moisture as cold winter rain and/or snow along the coast (Figure 3.12e). Maritime climates typically have precipitation through the entire year, with somewhat more during the winter months (Figure 3.12f). As a result of prevailing westerly winds at latitudes 30° to 60°, east coasts at these latitudes have continental climates, whereas west coasts have maritime climates. In eastern North America, precipitation is spread fairly evenly over the year (Figure 3.12g). Areas with a long summer drought and winter rains (Figure 3.12h) typically support a vegetation of chaparral.

    A convenient means of graphically depicting seasonal climates is the "climograph," a plot of average monthly temperature against average monthly precipitation (Figure 3.13). Although such graphs do not reflect year-to-year variability in climate, they do show at a glance the changes in both temperature and precipitation within an average year, as well as the season(s) during which the precipitation usually falls. (Without actually identifying points by months, however, spring cannot be distinguished from fall since both are seasons of moderate temperatures -- hence the arrows in Figure 3.13.) Exactly analogous plots are often made for any two physical variables, such as temperature versus humidity, or temperature versus salinity in aquatic systems (Figure 3.14). Many other variables of biological importance, such as acidity (pH) and dissolved phosphorus or nitrogen, can be treated similarly. When coupled with information on the tolerance limits of organisms, climographs and their analogues can be useful in predicting responses of organisms to changes in their physical environments (Figure 3.15).

    Very cold climates are usually dry, whereas warmer regions show a wide range of average annual precipitation (Figure 3.16). Although an infinite number of different types of climates exist, attempts have been made to classify them. One scheme (Köppen's) recognizes five major climatic types (as well as many minor ones): tropical rainy, dry, warm temperate rainy, cool snow forest, and polar. Another classification is shown in Figure 3.17.

    1. Figure 3.13. Climographs for eight different areas with different vegetation types. [After Smith (1940).]
    1. Figure 3.14. Graphs of average monthly temperature versus salinity of some estuarine and marine waters; seasonal variation is great in the brackish waters, whereas salinity varies little in true oceanic waters. [After Odum (1971) after Hedgepeth.]
      1. Figure 3.15. Two plots of temperature against moisture. (a) Climographs for an area in Montana where the Hungarian partridge was introduced successfully and a Missouri locality where its introduction failed, compared to the average climatic conditions of its European geographic range. Apparently Missouri summers are too hot and/or too wet for these birds. (b) Plots of temperature versus relative humidity in 1927 and 1932 in Israel superimposed on optimal (inner rectangle) and favorable (outer rectangle) conditions for the Mediterranean fruit fly. [Note that as drawn these rectangles assume no interaction between temperature and humidity; in actuality the edges would presumably be rounded due to the principle of allocation (see also Chapter 5).] Damage to fruit crops by these flies was much greater in 1927 than in 1932. [After Odum (1959).]
      1. Figure 3.16. Average annual temperature and annual precipitation for many localities scattered more or less evenly over the land area of the earth. [Adapted from Ricklefs (1973) based on data of Clayton. By permission of the Smithsonian Institution Press, from Smithsonian Misc. Col. 79, World Weather Records. H. H. Clayton, Smithsonian Institution, Washington, D.C., 1927.]
      1. Figure 3.17. Geographic distribution of the principal climates, according to the Thornthwaite classification. [After Blumenstock and Thornthwaite (1941).]

      Global Weather Modification

      Earth's atmosphere is unusual in that it has a relatively high oxygen content (about 21 percent). Most other planets have a reducing atmosphere. The free oxygen in today's atmosphere was probably produced largely by the activities of primary producers. The most plausible hypothesis to explain our planet's rather unusual atmosphere is that activities of living organisms, particularly green plants and certain bacteria, play vital roles in the building and maintenance of air. Photosynthetic activities of plants utilize carbon dioxide and water to produce oxygen as a by-product, along with energy-rich reduced carbon compounds, such as glucose.

      Free oxygen is released into the atmosphere by an inanimate process, too. High in the atmosphere above the ozone shield, ionizing solar radiation dissociates water vapor into molecular hydrogen and oxygen. Free oxygen is left behind as the light hydrogen atoms escape into outer space. In a reduced atmosphere, oxidation quickly uses up such free oxygen. Both of these oxygen-generating mechanisms have been important; dissociation was probably much more significant billions of years ago before the ozone layer was formed than it is at present (it will become more important as the ozone layer is further thinned by the release of chlorofluorocarbon gases). Ozone depletion has also increased ultraviolet radiation at the surface, which has almost certainly increased the frequency of skin cancers (though these may not be easily detectable for another decade).

      Our atmosphere is in a complex quasi equilibrium, but CO2 concentration has risen steadily for the last quarter of a century and continues to rise due to deforestation and burning of fossil fuels. Over the past 30 years, consumption of fossil fuels has more than doubled carbon emissions. This increase in atmospheric carbon dioxide has enhanced atmospheric heat retention and would have produced global warming sooner except for a fortuitous spin-off of atmospheric pollution -- particulate matter increased earth's albedo (reflectance of solar irradiation), so that less solar energy penetrates to the surface (volcanic ash in the atmosphere has the same effect). Until recently these two opposing phenomena more or less balanced one another, but now the balance has clearly shifted and the "greenhouse effect" is leading to rapid global warming. Long-held meteorological records the world over are being broken: the decades from 1990-2010 included the hottest years ever recorded, including the lowest low pressure zone ever recorded in late summer followed in the next winter by the highest high pressure area ever measured.

      A very dangerous new greenhouse gas molecule has begun to appear in earth's atmosphere during the past few decades: trifluoromethyl sulfer pentafluoride (CF3SF5). Each molecule of this gas traps as much heat as 18,000 CO2 molecules (Sturges et al. (2000). This new molecule is increasing at 6% per year and it is exceedingly stable (half life = 1,000 years). This molecule was not present in air before about 1960, so it is man-made. However, its exact source remains unknown --it could be an unintentional byproduct of some manufacturing process.

      Desertification has been greatly accelerated during the past century due to above-mentioned processes. Arid areas are in a more precarious and perilous position than wetter areas. As the population burgeons, the last remaining natural habitats are rapidly being destroyed. Earth's atmosphere is being altered at an ever-increasing rate, leading to rapid weather modification. There is some concern that agents of infectious disease, such as malaria and cholera, will spread as a result of climatic change. Lyme disease spreads with mouse epidemics, and these could be more extreme now than they were when millions of passenger pigeons competed with mice for acorns. Moreover, new types of infectious diseases such as ebola, fungi, and hantavirus appear to be emerging, possibly as a result of habitat destruction and climate change. Global warming is having its impact on virtually all Earthlings, both plants and animals, including humans, and its effects will continue to intensify into the foreseeable future. Crop failures would seem to be inevitable.

      Empty shelves in supermarkets will eventually awaken people to the dire danger of tampering with earth's atmosphere, but by then it will be much too late to rectify the situation. People will be appalled that scientists cannot restore the atmosphere to its former condition. But there can be no quick "technological fix" for Earth's maligned atmosphere. The continuing existence of all the denizens of this poor beleaguered planet, including ourselves, will ultimately depend more on our ecological understanding and wisdom than it will on future technological "advances."

      Unlimited, cheap, clean energy, such as that much hoped for in the concept of cold fusion, would actually be one of the worst things that could possibly befall humans. Such energy would enable well-meaning but uninformed massive energy consumption (i.e., mountains could be leveled, massive water canals dug, ocean water distilled, water pumped to deserts and turned into green fields of crops). Heat dissipation would of course set limits, for when more heat is produced than can be dissipated, the resulting thermal pollution would quickly warm the atmosphere to the point that all life is threatened, perhaps the ultimate ecocatastrophe. (Die-hard technologists will no doubt argue that we will invent ways to shoot our excess heat out into space.)

      Industrial pollutants cause acid rain, which can kill trees and fish. Recently, toxic levels of pesticides have been found in rain which has been linked to one of the most rapidly increasing cancers in the western world, non-Hodgkin's lymphoma. This type of cancer has increased by 73 percent in the last 25 years, probably directly due to several commonly used aerial crop sprays. Researchers suggest that the chemicals suppress immune systems, allowing viruses to trigger cancers (Pearce and Mackenzie 1999).

      Selected References

      Blair and Fite (1965); Blumenstock and Thornthwaithe (1941); Byers (1954); Chorley and Kennedy (1971); Collier et al. (1973); Finch and Trewartha (1949); Flohn (1969); Gates (1962); Haurwitz and Austin (1944); Lowry (1969); MacArthur (1972); MacArthur and Connell (1966); Taylor (1920); Thornthwaithe (1948); Trewartha (1943); U.S. Department of Agriculture (1941); Vitousek et al. (1986, 1997).


      4|Climate and Vegetation

      4| Climate and Vegetation

      Climate is the major determinant of vegetation. Plants in turn exert some degree of influence on climate. Both climate and vegetation profoundly affect soil development and the animals that live in an area. Here we examine some ways in which climate and vegetation interact. More emphasis is given to terrestrial ecosystems than to aquatic ones, although some aquatic analogues are briefly noted. Topics presented rather succinctly here are treated in greater detail elsewhere (see references at end of chapter).

      Plant Life Forms and Biomes

      Terrestrial plants adapted to a particular climatic regime often have similar morphologies, or plant growth forms. Thus, climbing vines, epiphytes, and broad-leafed species characterize tropical rain forests. Evergreen conifers dominate very cold areas at high latitudes and/or altitudes, whereas small frost-resistant tundra species occupy still higher latitudes and altitudes. Seasonal temperate zone areas with moderate precipitation usually support broad-leafed, deciduous trees, whereas tough-leafed (sclerophyllous) evergreen shrubs, or so-called chaparral-type vegetation, occur in regions with winter rains and a pronounced long water deficit during spring, summer, and fall. Chaparral vegetation is found wherever this type of climate prevails, including southern California, Chile, Spain, Italy, southwestern Australia, and the northern and southern tips of Africa (see Figure 4.1), although the actual plant species comprising the flora usually differ. Areas with very predictable and stable climates tend to support fewer different plant life forms than regions with more erratic climates. In general, there is a close correspondence between climate and vegetation (compare Figures 3.5 and 3.17 with Figure 4.1); indeed, climatologists have sometimes used vegetation as the best indicator of climate! Thus, rain forests occur in rainy tropical and rainy warm-temperature climates, forests exist under more moderate mesic climates, savannas and grasslands prevail in semiarid climates, and deserts characterize still drier climates. Of course, topography and soils also play a part in the determination of vegetation types, which are sometimes termed "plant formations." Such major communities of characteristic plants and animals are also known as biomes. Classification of natural communities is discussed later in this chapter.

      1. Figure 4.1. Geographic distribution of major vegetation types.
        [After MacArthur and Connell (1966) after Odum.]

      Microclimate

      Even in the complete absence of vegetation, major climatic forces, or macroclimates, are expressed differently at a very local spatial level, which has resulted in the recognition of so-called microclimates. Thus, the surface of the ground undergoes the greatest daily variation in temperature, and daily thermal flux is progressively reduced with both increasing distance above and below ground level (Figure 4.2). During daylight hours the surface intercepts most of the incident solar energy and rapidly heats up, whereas at night this same surface cools more than its surroundings. Such plots of temperature versus height above and below ground are called thermal profiles. An analogous type of graph, called a bathythermograph, is often made for aquatic ecosystems by plotting temperature against depth (see Figure 4.17).

      1. Figure 4.2. Idealized thermal profile showing temperatures at various distances above and below ground at four different times of day. [After Gates (1962).]

      Daily temperature patterns are also modified by topography even in the absence of vegetation. A slope facing the sun intercepts light beams more perpendicularly than does a slope facing away from the sun; as a result, a south-facing slope in the Northern Hemisphere receives more solar energy than a north-facing slope, and the former heats up faster and gets warmer during the day (Figure 4.3). Moreover, such a south-facing slope is typically drier than a north-facing one because it receives more solar energy and therefore more water is evaporated.

      1. Figure 4.3. Daily marches of temperature on an exposed south-facing slope (solid line) and on a north-facing slope (dashed line) during late summer in the Northern Hemisphere. [After Smith (1966) after van Eck.]

      By orienting themselves either parallel to or at right angles to the sun's rays, organisms (and parts of organisms such as leaves) may decrease or increase the total amount of solar energy they actually intercept. Leaves in the brightly illuminated canopy often droop during midday, whereas those in the shaded understory typically present their full surface to incoming beams of solar radiation. Similarly, many desert lizards position themselves on the ground perpendicular to the sun's rays in the early morning when environmental temperatures are low, but during the high temperatures of midday these same animals reduce their heat load by climbing up off the ground into cooler air temperatures and orienting themselves parallel to the sun's rays by facing into the sun.

      1. Figure 4.4. Temperature profiles in a growing cornfield at midday, showing the effect of vegetation on thermal microclimate. [After Smith (1966).]

      The major effect of a blanket of vegetation is to moderate most daily climatic changes, such as changes in temperature, humidity, and wind. (However, plants generate daily variations in concentrations of oxygen and carbon dioxide through their photosynthetic and respiratory activities.) Thermal profiles at midday in corn fields at various stages of growth are shown in Figure 4.4, demonstrating the marked reduction in ground temperature due especially to shading. In the mature field, air is warmest at about a meter above ground. Similar vegetational effects on microclimates occur in natural communities. A patch of open sand in a desert might have a daily thermal profile somewhat like that shown in Figure 4.2, whereas temperatures in the litter underneath a nearby dense shrub would vary much less with the daily march of temperature.

      Humidities are similarly modified by vegetation, with relative humidities within a dense plant being somewhat greater than those of the air in the open adjacent to the plant. An aphid may spend its entire lifetime in the very thin zone (only about a millimeter thick) of high humidity that surrounds the surface of a leaf. Moisture content is more stable, and therefore more dependable, deeper in the soil than it is at the surface, where high temperatures periodically evaporate water to produce a desiccating effect.

      1. Figure 4.5. Wind velocities within a forest vary relatively little with changes in the wind velocity above the canopy. [After Smith (1966) after Fons (1940).]

      Wind velocities are also reduced sharply by vegetation and are usually lowest near the ground (Figures 4.5 and 4.6). Moving currents of air promote rapid exchange of heat and water; hence an organism cools or warms more rapidly in a wind than it does in a stationary air mass at the same temperature. Likewise, winds often carry away moist air and replace it with drier air, thereby promoting evaporation and water loss. The desiccating effects of such dry winds can be extremely important to an organism's water balance.

      1. Figure 4.6. Daily march of average wind velocities during June at various heights inside a coniferous forest in Idaho. [After Smith (1966) after Gisborne.]

      In aquatic systems, water turbulence parallels wind in many ways, and rooted vegetation around the edges of a pond or stream reduces water turbulence. At a more microscopic level, algae and other organisms that attach themselves to underwater surfaces (so-called periphyton) create a thin film of distinctly modified microenvironment in which water turbulence, among other things, is reduced. Localized spatial patches with particular concentrations of hydrogen ions (pH), salts, dissolved nitrogen and phosphorus, and the like, form similar aquatic microhabitats.

      By actively or passively selecting such microhabitats, organisms can effectively reduce the overall environmental variation they encounter and enjoy more optimal conditions than they could without microhabitat selection.

      Innumerable other microclimatic effects could be cited, but these should serve to illustrate their existence and their significance to plants and animals.

      Primary Production and Evapotranspiration

      In terrestrial ecosystems, climate is by far the most important determinant of the amount of solar energy plants are able to capture as chemical energy, or the gross primary productivity (Table 4.1). In warm arid regions, water is a master limiting factor, and in the absence of runoff, primary production is strongly positively correlated with rainfall in a linear fashion (see Figure 5.1). Above about 80 centimeters of precipitation per year, primary production slowly decreases with increasing precipitation and then levels off (asymptotes) (Figure 4.7). Notice that some points fall below the curve in this figure, presumably because there is some water loss by runoff and seepage into groundwater supplies.

      1. Figure 4.7. Net primary productivity (above ground) plotted against average annual precipitation. [From Whittaker (1970). Reprinted with permission of Macmillan Publishing Co., Inc., from Communities and Ecosystems by Robert H. Whittaker. Copyright © 1970 by Robert H. Whittaker.]

      Table 4.1 Net Primary Productivity and World Net Primary Production for Major Ecosystems

      _________________________________________________________________________________

      Net Primary Productivity
      per Unit Area (dry g/m2/yr) World Net
      _______________________Primary
      AreaNormal Production
      (106 km2)RangeMean(109 dry tons/yr)

      _________________________________________________________________________________

      Lake and stream 2 100-1500 500 1.0

      Swamp and marsh 2 800-4000 2000 4.0

      Tropical forest 20 1000-5000 2000 40.0

      Temperate forest 18 600-2500 1300 23.4

      Boreal forest 12 400-2000 800 9.6

      Woodland and shrubland7 200-1200 600 4.2

      Savanna45 200-2000 700 10.5

      Temperate grassland9 150-1500 500 4.5

      Tundra and alpine8 10-400 140 1.1

      Desert scrub18 10-250 70 1.3

      Extreme desert, rock, ice240-10 3 0.07

      Agricultural land14 100-4000 650 9.1

      Total land149 730 109.0

      Open ocean332 2-400 125 41.5

      Continental shelf27 200-600 350 9.5

      Attached algae, estuaries2 500-4000 2000 4.0

      Total ocean361 155 55.0

      Total for earth510 320 164.0

      ________________________________________________________________________________

      Source: Adapted from Whittaker (1970).

       

      Evapotranspiration refers to the release of water into the atmosphere as water vapor, both by the physical process of evaporation and by the biological processes of transpiration and respiration. The amount of water vapor thus returned to the atmosphere depends strongly on temperature, with greater evapotranspiration at higher temperatures. The theoretical temperature-dependent amount of water that could be "cooked out" of an ecological system, given its input of solar energy and provided that much water fell on the area, is called its potential evapotranspiration (PET). In many ecosystems, water is frequently in short supply, so actual evapotranspiration (AET) is somewhat less than potential (clearly, AET can never exceed PET and is equal to PET only in water-saturated habitats). Actual evapotranspiration can be thought of as the reverse of rain, for it is the amount of water that actually goes back into the atmosphere at a given spot.

      The potential evapotranspiration for any spot on earth is determined by the same factors that regulate temperature, most notably latitude, altitude, cloud cover, and slope (topography). There is a nearly one-to-one correspondence between PET and temperature, and an annual march of PET can be plotted in centimeters of water. By superimposing the annual march of precipitation on these plots (Figure 4.8), seasonal changes in water availability can be depicted graphically. A water deficit occurs when PET exceeds precipitation; a water surplus exists when the situation is reversed.

      1. Figure 4.8. Plots of annual march of potential evapotranspiration superimposed on the annual march of precipitation for three ecologically distinct regions showing the water relations of each. (a) Temperate deciduous forest, (b) chaparral with winter rain, (c) desert. [From Odum (1959) after Thornthwaite.]

      During a period of water surplus, some water may be stored by plants and some may accumulate in the soil as soil moisture, depending on runoff and the capacity of soils to hold water; during a later water deficit, such stored water can be used by plants and released back into the atmosphere. Winter rain is generally much less effective than summer rain because of the reduced activity (or complete inactivity) of plants in winter; indeed, two areas with the same annual march of temperature and total annual precipitation may differ greatly in the types of plants they support and in their productivity as a result of their seasonal patterns of precipitation. An area receiving about 50 cm of precipitation annually supports either a grassland vegetation or chaparral, depending on whether the precipitation falls in summer or winter, respectively.

      Net annual primary production above ground is strongly correlated with actual evapotranspiration, or AET (Figure 4.9). This correlation is remarkable in that AET was crudely estimated using only monthly macroclimatic statistics with no allowance for either runoff and water-holding capacities of soils or for groundwater usage.


      1. Figure 4.9. Log-log plot of net primary productivity above ground against estimated actual evapotranspiration for 24 areas, ranging from barren desert to luxurious tropical rain forest. [After Rosenzweig (1968).]


      Rosenzweig (1968) suggested that the reason for the observed correlation is that AET measures simultaneously two of the most important factors limiting primary production on land: water and solar energy. Photosynthesis, that fundamental process on which nearly all life depends for energy, is represented by the chemical equation

      6CO2 + 12H2O ----> C6H12O6 + 6O2 + 6H2O

      where C6H12O6 is the energy-rich glucose molecule. Carbon dioxide concentration in the atmosphere is fairly constant at about 0.03 to 0.04 percent and does not strongly influence the rate of photosynthesis, except under unusual conditions of high water availability and full or nearly full sunlight, when CO2 is limiting (Meyer, Anderson, and Bohning 1960). (Effects of increased CO2 levels on plants and various ecosystems as a result of anthropogenic global change will be most interesting to observe!) Rosenzweig notes that, on a geographical scale, each of the other two requisites for photosynthesis, water and solar energy, are much more variable in their availabilities and more often limiting; moreover, AET measures the availability of both. Temperature is often a rate-limiting factor and markedly affects photosynthesis; it, too, is presumably incorporated into an estimated AET value. Primary production may be influenced by nutrient availability as well, but in many terrestrial ecosystems these effects are often relatively minor. Two major kinds of photosynthesis are known as the C3 and C4 pathways (plants with each differ in their response to elevated CO2 levels, among other things).

      In aquatic ecosystems, nutrient availability is often a major determinant of the rate of photosynthesis. Primary production in aquatic systems of fairly constant temperature (such as the oceans) is often strongly affected by light. Because light intensity diminishes rapidly with depth in lakes and oceans, most primary productivity is concentrated near the surface (Figure 4.10a). However, short wavelengths (blue light) penetrate deeper into water than longer ones, and some benthic (bottom-dwelling) marine "red" algae have evolved unique photosynthetic adaptations to utilize these wavelengths.

      1. Figure 4.10. Vertical profiles of (a) the amount of photosynthesis versus depth in a lake and (b) light intensity versus height above ground in a forest.

      Similarly, within forests, light intensity varies markedly with height above ground (Figure 4.10b). Tall trees in the canopy receive the full incident solar radiation, whereas shorter trees and shrubs receive progressively less light. In really dense forests, less than 1 percent of the incident solar energy impinging on the canopy actually penetrates to the forest floor. Although a tree in the canopy has more solar energy available to it than a fern on the forest floor, the canopy tree must also expend much more energy on vegetative supporting tissues (wood) than the fern. (Understory plants are usually very shade tolerant and able to photosynthesize at very low light intensities. Also, herbs of the forest floor often grow and flower early in the spring before deciduous trees leaf out.) Hence, each plant life form and each growth strategy has its own associated costs and profits.

      Soil Formation and Primary Succession

      Soils are a key part of the terrestrial ecosystem because many processes critical to the functioning of ecosystems occur in the soil. This is where dead organisms are decomposed and where their nutrients are retained until used by plants and, indirectly, returned to the remainder of the community. Soils are essentially a meeting ground of the inorganic and organic worlds. Many organisms live in the soil; perhaps the most important are the decomposers, which include a rich biota of bacteria and fungi. Also, the vast majority of insects spend at least a part of their life cycle in the soil. Certain soil-dwelling organisms, such as earthworms, often play a major role in breaking down organic particles into smaller pieces, which present a larger surface area for microbial action, thereby facilitating decomposition. Indeed, activities of such soil organisms sometimes constitute a "bottleneck" for the rate of nutrient cycling, and as such they can regulate nutrient availability and turnover rates in the entire community. In aquatic ecosystems, bottom sediments like mud and ooze are closely analogous to the soils of terrestrial systems.

      1. Figure 4.11. Diagram of typical soil changes along the transitition from prairie (deep black topsoil)
        to forest (shallow topsoil) at the edge of the North American Great Plains. [After Crocker (1952).]

      Much of modern soil science, or pedology, was anticipated in the late l800s by the prominent Russian pedologist V. V. Dokuchaev. He devised a theory of soil formation, or pedogenesis, based largely on climate, although he also recognized the importance of time, topography, organisms (especially vegetation), and parent materials (the underlying rocks from which the soil is derived). The relative importance of each of these five major soil-forming factors varies from situation to situation. Figure 4.11 shows how markedly the soil changes along the transition from prairie to forest in the midwestern United States, where the only other conspicuous major variable is vegetation type. Grasses and trees differ substantially both in mineral requirements and in the extent to which the products of their own primary production contribute organic materials to the soil. Typically, natural soils underneath grasslands are considerably deeper and richer in both organic and inorganic nutrients than are the natural soils of forested regions. Jenny (1941) gives many examples of how each of the five major soil-forming factors influence particular soils.

      The marked effects some soil types can have on plants are well illustrated by so-called serpentine soils (Whittaker, Walker, and Kruckeberg 1954), which are formed over a parent material of serpentine rock. These soils often occur in localized patches surrounded by other soil types; typically the vegetation changes abruptly from nonserpentine to serpentine soils. Serpentine soils are rich in magnesium, chromium, and nickel, but they contain very little calcium, molybdenum, nitrogen, and phosphorus. They usually support a stunted vegetation and are relatively less productive than adjacent areas with different, richer soils. Indeed, entire floras of specialized plant species have evolved that are tolerant of the conditions of serpentine soils (particularly their low calcium levels). Introduced Mediterranean "weeds" have replaced native Californian coastal grasses and forbs almost everywhere except on serpentine soils, where the native flora still persists.

      Soil development from bare rock, or primary succession, is a very slow process that often requires centuries (soil losses due to erosion caused by human activities are serious and long-term). Rock is fragmented by temperature changes, by the action of windblown particles, and in colder regions by the alternate expansion and contraction of water as it freezes and thaws. Chemical reactions, such as the formation of carbonic acid (H2CO3) from water and carbon dioxide, may also help to dissolve and break down certain rock types like limestones. Such weathering of rocks releases inorganic nutrients that can be used by plants. Eventually, lichens establish themselves, and as other plants root and grow, root expansion further breaks up the rock into still smaller fragments. As these plants photosynthesize, they convert inorganic materials into organic matter. Such organic material, mixed with inorganic rock fragments, accumulates, and soil is slowly formed. Early in primary succession, production of new organic material exceeds its consumption and organic matter accumulates; as soil "maturity" is approached, soil eventually ceases to accumulate. Whereas most organic material is contributed to soils from above as leaf and litter fall, mineral inorganic components tend to be added from the underlying rocks below. These polarized processes thus generate fairly distinct layers, termed soil "horizons."

      Even though litter fall is high in tropical forests, it does not accumulate to nearly as great an extent as it does in the temperate zones, presumably because decomposition rates are very high in the warm tropics. As a result, tropical soils tend to be poor in nutrients (high rainfall in many tropical areas further depletes these soils by leaching out water-soluble nutrients). For both reasons, tropical areas simply cannot support sustained agriculture nearly as well as can temperate regions (in addition, diverse tropical communities are probably much more fragile than simpler temperate-zone systems).

      There are fairly close parallels between concepts of soil development and those for the development of ecological communities; pedologists speak of “maturesoils at the steady state, whereas ecologists recognize the “climaxcommunities that grow on and live in these same soils. These two components of the ecosystem (soils and vegetation) are intricately interrelated and interdependent; each strongly influences the other. Except in forests and rain forests, there is usually a one-to-one correspondence between them (Figure 4.12). (Compare also the geographic distribution of soil types shown in Figure 4.13 with the distribution of vegetation types shown in Figure 4.1.)

      Once a mature soil has been formed, a disturbance such as the removal of vegetation by fire or human activities often results in gradual sequential changes in the organisms comprising the community. Such a temporal sequence of communities is termed a secondary succession.

      1. Figure 4.12. Relationships between temperature and precipitation and (a) climatic types, (b) vegetation formations, and (c) major zonal soil groups. Numbered scales in (a) and (c) indicate centimeters of precipitation per year. [From Blumenstock and Thornthwaite (1941).]

      Ecotones and Vegetational Continua

      Communities are seldom discrete entities; in fact they usually grade into one another in both space and time. A localized "edge community" between two other reasonably distinct communities is termed an ecotone. Typically, such ecotonal communities are rich in species because they contain representatives from both parent communities and may also contain species distinctive of the ecotone itself.

      1. Figure 4.13. Geographic distribution of the primary soil types. Compare with vegetation map
        shown in Figure 4.1. [After Blumenstock and Thornthwaite (1941).]

      Often a series of communities grade into one another almost continuously (Figure 4.14); such a gradient community is called an ecocline. Ecoclines may occur either in space or in time.

      Spatial ecoclines on a more local scale have led to so-called gradient analysis (Whittaker 1967). The abundance and actual distribution of organisms along many environmental gradients have shown that the importances of various species along any given gradient typically form bell-shaped curves reminiscent of tolerance curves (considered in the next chapter). These curves tend to vary independently of one another and often overlap broadly (Figure 4.15), indicating that each species' population has its own particular habitat requirements and width of habitat tolerance -- and hence its own zone of maximal importance. Such a continuous replacement of plant species by one another along a habitat gradient is termed a vegetational continuum (Figure 4.15).

      A temporal ecocline, or a change in community composition in time, both by changes in the relative importance of component populations and by extinction of old species and invasion of new ones, is termed a succession. Primary succession, as we have just seen,

      1. Figure 4.14. Vegetation profiles along three ecoclines. (a) A gradient of increasing aridity from seasonal rainforest to desert. (b) An elevation gradient up a tropical mountainside from tropical rainforest to alpine meadow (paramo). (c) A humidity gradient from swamp forest to savanna. [From Beard (1955).]

      is the development of communities from bare rock; secondary successions are changes that take place after destruction of the natural vegetation of an area with soil. Secondary succession is often a more-or-less orderly sequential replacement of early succession species, typically rapidly growing colonizing species, by other more competitive species that succeed in later stages, usually slow-growing and shade-tolerant species. The final stage in succession is termed the climax. Secondary succession is discussed in more detail in Chapter 17.

      1. Figure 4.15. Actual distributions of some populations of plant species along moisture gradients from relatively wet ravines to dry southwest-facing slopes in the Siskiyou mountains of northern California (above) and the Santa Catalina mountains of Arizona (below). [After Whittaker (1967).]

      Classification of Natural Communities

      Biotic communities have been classified in various ways. An early attempt to classify communities was that of Merriam (1890), who recognized a number of different "life zones" defined solely in terms of temperature (ignoring precipitation). His somewhat simplistic scheme is no longer used, but his approach did link climate with vegetation in a more or less predictive manner.

      Shelford (1913a, 1963) and his students have taken a somewhat different approach to the classification of natural communities that does not attempt to correlate climate with the plants and animals occurring in an area. Rather, they classify different natural communities into a large number of so-called biomes and associations, relying largely upon the characteristic plant and animal species that compose a particular community. As such, this scheme is descriptive rather than predictive. Such massive descriptions of different communities (see, for example, Dice 1952 and Shelford 1963) can often be quite useful in that they allow one to become familiar with a particular community with relative ease.

      Workers involved in such attempts at classification typically envision communities as discrete entities with relatively little or no intergradation between them; thus, the Shelford school considers biomes to be distinct and real entities in nature rather than artificial and arbitrary human constructs. Another school of ecologists, represented by McIntosh (1967) and Whittaker (1970), takes an opposing view, emphasizing that communities grade gradually into one another and form so-called continua or ecoclines (Figures 4.14 and 4.15).

      Vegetational formations typically occurring under various climatic regimes are superimposed on a plot of average annual precipitation versus average annual temperature in Figure 4.16. Macroclimate determines the vegetation of an area -- these correlations are not hard and fast but local vegetation type depends on other factors such as soil types, seasonality of rainfall regime, and frequency of disturbance by fires and floods.

      1. Figure 4.16. Diagrammatic representation of the correlation between climate, as reflected by average annual temperature and precipitation, and vegetational formation types. Boundaries between types are approximate and are influenced locally by soil type, seasonality of rainfall, and disturbances such as fires. The dashed line encloses a range of climates in which either grasslands or woody plants may constitute the prevailing vegetation of an area, depending on the seasonality of precipitation. Compare this figure with Figure 3.16. [After Whittaker (1970). Reprinted with permission of Macmillan Publishing Co., Inc., from Communities and Ecosystems by Robert H. Whittaker. Copyright © 1970 by Robert H. Whittaker.]

      Aquatic Ecosystems

      Although the same ecological principles presumably operate in both aquatic and terrestrial ecosystems, there are striking and interesting fundamental differences between these two ecological systems. For example, primary producers on land are sessile and many tend to be large and relatively long-lived (air does not provide much support and woody tissues are needed), whereas, except for kelp, producers in aquatic communities are typically free-floating, microscopic, and very short-lived (the buoyancy of water may make supportive plant tissues unnecessary; a large planktonic plant might be easily broken by water turbulence). Most ecologists study either aquatic or terrestrial systems, but seldom both. Various aquatic subdisciplines of ecology are recognized, such as aquatic ecology and marine ecology.

      Limnology is the study of freshwater ecosystems (ponds, lakes, and streams); oceanography is concerned with bodies of salt water. Because the preceding part of this chapter and most of the remainder of the book emphasize terrestrial ecosystems, certain salient properties of aquatic ecosystems, especially lakes, are briefly considered in this section. Lakes are particularly appealing subjects for ecological study in that they are self-contained ecosystems, discrete and largely isolated from other ecosystems. Nutrient flow into and out of a lake can often be estimated with relative ease. The study of lakes is fascinating; the interested reader is referred to Ruttner (1953), Hutchinson (1957b, 1967), Cole (1975), Wetzel (1983), and/or Bronmark and Hansson (1998).

      Water has peculiar physical and chemical properties that strongly influence the organisms that live in it. As indicated earlier, water has a high specific heat; moreover, in the solid (frozen) state, its density is less than it is in the liquid state (that is, ice floats). Water is most dense at 4°C and water at this temperature "sinks." Furthermore, water is nearly a "universal solvent" in that many important substances dissolve into aqueous solution.

      A typical, relatively deep lake in the temperate zones undergoes marked and very predictable seasonal changes in temperature. During the warm summer months, its surface waters are heated up, and because warm water is less dense than colder water, a distinct upper layer of warm water, termed the epilimnion, is formed (Figure 4.17a). (Movement of heat within a lake is due to water currents produced primarily by wind.) Deeper waters, termed the hypolimnion, remain relatively cold during summer, often at about 4°C; an intermediate layer of rapid temperature change, termed the thermocline, separates the epilimnion from the hypolimnion (Figure 4.17a). (A swimmer sometimes experiences these layers of different temperatures when diving into deep water or when in treading water his or her feet drop down into the cold hypolimnion.) A lake with a thermal profile, or bathythermograph, like that shown in Figure 4.17a is said to be "stratified" because of its layer of warm water over cold water. Typically there is little mixing of the warm upper layer with the heavier deeper water. With the decrease in incident solar energy in autumn, surface waters cool and give up their heat to adjacent landmasses and the atmosphere (Figure 4.17b). Eventually, the epilimnion cools to the same temperature as the hypolimnion and the lake becomes isothermal (Figure 4.17c). This is the time of the "fall turnover." With winter's freezing temperatures, the lake's surface turns to ice and its temperature versus depth profile looks something like that in Figure 4.17d. Finally, in spring the ice melts and the lake is briefly isothermal once again (it may have a spring turnover) until its surface waters are rapidly warmed, when it again becomes stratified and the annual cycle repeats itself.

      Because prevailing winds produce surface water currents, a lake's waters circulate. In stratified lakes, the epilimnion constitutes a more or less closed cell of circulating warm water, whereas the deep cold water scarcely moves or mixes with the warmer water above it. During this period, as dead organisms and particulate organic matter sinks

      1. Figure 4.17. Hypothetical bathythermographs showing seasonal changes typical of a deep temperate zone lake. (a) A stratified lake during summer. (b) In early autumn, upper waters cool. (c) In late autumn or early winter, the lake's waters are all at exactly the same temperature, here 4°C. (The lake is "isothermal.") (d) During the freezing winter months, a layer of surface ice chills the uppermost water.

      into the noncirculating hypolimnion, the lake undergoes what is known as summer stagnation. When a lake becomes isothermal, its entire water mass can be circulated and nutrient-rich bottom waters brought to the surface during the spring and/or fall "turnover." Meteorological conditions, particularly wind velocity and duration, strongly influence such turnovers; indeed, if there is little wind during the period a lake is isothermal, its waters might not be thoroughly mixed and many nutrients may remain locked in its depths. After a thorough turnover, the entire water mass of a lake is equalized and concentrations of various substances, such as oxygen and carbon dioxide, are similar throughout the lake.

      Lakes differ in their nutrient content and degree of productivity and they can be arranged along a continuum ranging from those with low nutrient levels and low productivity (oligotrophic lakes) to those with high nutrient content and high productivity (eutrophic lakes). Clear, cold, and deep lakes high in the mountains are usually relatively oligotrophic, whereas shallower, warmer, and more turbid lakes such as those in low-lying areas are generally more eutrophic. Oligotrophic lakes typically support game fish such as trout, whereas eutrophic lakes contain "trash" fish such as carp. As they age and fill with sediments, many lakes gradually undergo a natural process of eutrophication, steadily becoming more and more productive. People accelerate this process by enriching lakes with wastes, and many oligotrophic lakes have rapidly become eutrophic under our influence. A good indicator of the degree of eutrophication is the oxygen content of deep water during summer. In a relatively unproductive lake, oxygen content varies little with depth and there is ample oxygen at the bottom of the lake. In contrast, oxygen content diminishes rapidly with depth in productive lakes, and anaerobic processes sometimes characterize their depths during the summer months (an example of succession). With the autumn turnover, oxygen-rich waters again reach the bottom sediments and aerobic processes become possible. However, once such a lake becomes stratified, the oxygen in its deep water is quickly used up by benthic organisms (in the dark depths there is little or no photosynthesis to replenish the oxygen).

      These seasonal physical changes profoundly influence the community of organisms living in a lake. During the early spring and after the fall turnover, surface waters are rich in dissolved nutrients such as nitrates and phosphates and temperate lakes are very productive, whereas during mid-summer, many nutrients are unavailable to phytoplankton in the upper waters and primary production is greatly reduced.

      Organisms within a lake community are usually distributed quite predictably in time and space. Thus, there is typically a regular seasonal progression of planktonic algae, with diatoms most abundant in the winter, changing to desmids and green algae in the spring, and gradually giving way to blue-green algae during summer months. The composition of the zooplankton also varies seasonally. Such temporal heterogeneity may well promote a diverse plankton community by periodically altering competitive abilities of component species, hence facilitating coexistence of many species of plants and animals in the relatively homogeneous planktonic environment (Hutchinson 1961). Although plankton are moved about by water currents, many are strong enough swimmers to select a particular depth. Such species often actually "migrate" vertically during the day and/or with the seasons, being found at characteristic depths at any given time (Figure 4.18). Some zooplankters sink into the dark depths during the daylight hours (probably an adaptation to avoid visually hunting predators such as fish), but ascend to the surface waters at night to feed on phytoplankton.

      More than half of all accessible surface freshwater is used by humans. Ships releasing ballast water have dispersed exotic species of invertebrates worldwide -- many of these have wreaked havoc on aquatic systems. Freshwater aquatic systems everywhere are polluted and threatened -- one third of the world's freshwater fish are threatened or endangered and many freshwater amphibians (especially frogs) are considered threatened. Human wastes, particularly plastics, release large amounts of estrogen mimics that are concentrated in natural food webs and are increasingly becoming a very serious threat to the continuing health and viability of humans and many other animals (Colburn et al. 1996). Reduced sperm counts and infertility, as well as higher incidences of prostate and breast cancers, could well be caused by these hormone mimics.

      1. Figure 4.18. Many small freshwater planktonic animals move vertically during the daily cycle of illumination somewhat as shown here (widths of bands represent the density of animals at a given depth at a particular time). [After Cowles and Brambel 1936].

      Selected References

      Allee et al. (1949); Andrewartha and Birch (1954); Clapham (1973); Clarke (1954); Colinvaux (1973); Collier et al. (1913); Daubenmire (1947, 1956, 1968); Gates (1972); Kendeigh (1961); Knight (1965); Krebs (1972); Lowry (1969); Odum (1959, 1971); Oosting (1958); Ricklefs (1973); Smith (1966); Watt (1973); Weaver and Clements (1938); Whittaker (1970).

      Plant Life Forms and Biomes

      Cain (1950); Clapham (1973); Givnish and Vermeij (1976); Horn (1971); Raunkaier (1934); Whittaker (1970).

      Microclimate

      Collier et al. (1973); Fons (1940); Gates (1962); Geiger (1966); Gisborne (1941); Lowry (1969); Schmidt-Nielsen (1964); Smith (1966).

      Primary Production and Evapotranspiration

      Collier et al. (1973); Gates (1965); Horn (1971); Meyer, Anderson, and Bohning (1960); Odum (1959, 1971); Rosenzweig (1968); Whittaker (1970); Woodwell and Whittaker (1968).

      Soil Formation and Primary Succession

      Black (1968); Burges and Raw (1967); Crocker (1952); Crocker and Major (1955); Doeksen and van der Drift (1963); Eyre (1963); Fried and Broeshart (1967); Jenny (1941); Joffe (1949); Oosting (1958); Richards (1974); Schaller (1968); Waksman (1952); Whittaker, Walker, and Kruckeberg (1954).

      Ecotones and Vegetational Continua

      Clements (1920, 1949); Horn (1971, 1975a, b, 1976); Kershaw (1964); Loucks (1970); Margalef (1958b); McIntosh (1967); Pickett (1976); Shimwell (1971); Terborgh (1971); Whittaker (1953, 1965, 1967, 1969, 1970, 1972).

      Classification of Natural Communities

      Beard (1955); Braun-Blanquet (1932); Clapham (1973); Dice (1952); Gleason and Cronquist (1964); Holdridge (1947, 1959, 1967); McIntosh (1967); Merriam (1890). Shelford (1913a, 1963); Tosi (1964); Whittaker (1962, 1967, 1970).

      Aquatic Ecosystems

      Bronmark and Hansson (1998); Clapham (1973); Colburn et al. (1996); Cole (1975); Cowles and Brambel (1936); Ford and Hazen (1972); Frank (1968); Frey (1963); Grice and Hart (1962); Henderson (1913); Hochachka and Somero (1973); Hutchinson (1951, 1957b, 1961, 1967); Mann (1969); National Academy of Science (1969); Perkins (1974); Russell-Hunter (1970); Ruttner (1953); Sverdrup et al. (1942); Watt (1973); Welch (1952); Wetzel (1983); Weyl (1970).


      5 Resource Acquisition and Allocation

      5| Resource Acquisition and Allocation

      Limiting Factors and Tolerance Curves

      Ecological events and their outcomes, such as growth, reproduction, photosynthesis, primary production, and population size, are often regulated by the availability of one or a few factors or requisites in short supply, whereas other resources and raw materials present in excess may go partially unused. This principle has become known as the "law of the minimum" (Liebig 1840). For instance, in arid climates, primary production (the amount of solar energy trapped by green plants) is strongly correlated with precipitation (Figure 5.1); here water is a "master limiting factor." Of many different factors that can be limiting, frequently among the most important are various nutrients, water, and temperature.

      1. Figure 5.1. An example of the strong correlation between annual rainfall and primary production along a precipitation gradient in a desert region of Namibia. [Adapted from Odum (1959) after Walter (1939).]

      When considering populations, we often speak of those that are food-limited, predator-limited, or climate-limited. Populations may be limited by other factors as well; for example, density of breeding pairs of blue tits (Parus caeruleus) in an English woods was doubled by the addition of many new nesting boxes (Lack 1954, 1966), providing an indication that nest sites were limiting. However, limiting factors are not always so clear-cut but may usually interact so that a process is limited simultaneously by several factors, with a change in any one of them resulting in a new equilibrium. For instance, both increased food availability and decreased predation pressures might result in a larger population size.

      A related concept, developed by Shelford (1913b), is now known as the "law of tolerance." Too much or too little of anything can be detrimental to an organism. In the early morning, a desert lizard finds itself in an environment that is largely too cold, whereas later in the day its environment is too hot. The lizard compensates somewhat for this by spending most of its time during the early morning in sunny places, whereas later on most of its activities take place in the shade. Each lizard has a definite optimal range of temperature, with both upper and lower limits of tolerance. More precisely, when measures of performance (such as fitness, survivorship, or foraging efficiency) are plotted against important environmental variables, bell-shaped curves usually result (for examples, see Figures 5.2 and 5.8).

      1. Figure 5.2. Distance jumped by a frog as a function of its body temperature. Notice that performance diminishes at both low and high temperatures. [From Huey and Stevenson (1979).]

      Organisms can be viewed as simple input-output systems, with foraging or photosynthesis providing an input of materials and energy that are in turn "mapped" into an output consisting of progeny. Fairly extensive bodies of theory now exist both on optimal foraging and reproductive tactics (see next chapter). In optimal foraging theory, the "goal" usually assumed to be maximized is energy uptake per unit time (successful offspring produced during an organism's lifetime would be a more realistic measure of its foraging ability, but fitness is exceedingly difficult to measure). Similarly, among organisms without parental care, reproductive effort has sometimes been estimated by the ratio of calories devoted to eggs or offspring over total female calories at any instant (rates of uptake versus expenditure of calories have unfortunately not yet infiltrated empirical studies of reproductive tactics). To date, empirical studies of resource partitioning have been concerned largely with "input" phenomena such as overlap in and efficiency of resource utilization and have neglected to relate these to "output" aspects. In contrast, empirical studies of reproductive tactics have done the reverse and almost entirely omitted any consideration of foraging. Interactions and constraints between foraging and reproduction have barely begun to be considered. A promising area for future work will be to merge aspects of optimal foraging with optimal reproductive tactics to specify rules by which input is translated into output; optimal reproductive tactics ("output" phenomena) surely must often impose substantial constraints upon "input" possibilities and vice versa.

      Resource Budgets and the Principle of Allocation

      Any organism has a limited amount of resources available to devote to foraging, growth, maintenance, and reproduction. The way in which an organism allocates its time and energy and other resources among various conflicting demands is of fundamental interest because such apportionments provide insight into how the organism copes with and conforms to its environment. Moreover, because any individual has finite resource and energy budgets, its capacity for regulation is necessarily limited. Organisms stressed along any one environmental variable are thus able to tolerate a lesser range of conditions along other environmental variables. Various tolerance and performance curves (Figure 5.2) are presumably subject to certain constraints. For example, their breadth (variance) usually cannot be increased without a simultaneous reduction in their height and vice versa (Levins 1968). This useful notion of trade-offs, known as the principle of allocation, has proven to be quite helpful in interpreting and understanding numerous ecological phenomena.

      As an example of allocation, imagine an animal of a given size and mouth-part anatomy. A certain size of prey item is optimal, whereas other prey are suboptimal because they are either too large or too small for efficient capture and swallowing. Any given animal has its own "utilization curve" that indicates the actual numbers of prey of different sizes taken per unit time under particular environmental conditions. In an idealized, perfectly stable, and infinitely productive environment, a utilization curve might become a spike with no variance, with the organism using only its most optimal prey resource type. In actuality, limited and changing availabilities of resources, in both time and space, result in utilization curves with breadth as well as height. In terms of the principle of allocation, an individual with a generalized diet adapted to eat prey of a wide range of available sizes presumably is not so effective at exploiting prey of intermediate size as another, more specialized, feeder. In other words, a jack-of-many-trades is a master of none. We will consider this subject in more detail later.

      Time, Matter, and Energy Budgets

      Time, matter, and energy budgets vary widely among organisms. For example, some creatures allot more time and energy to reproduction at any instant than do others. Varying time and energy budgeting is a potent means of coping with a changing environment while retaining some degree of adaptation to it. Thus, many male songbirds expend a great deal of energy on territorial defense during the breeding season but little or none at other times of the year. Similarly, in animals with parental care, an increasing amount of energy is spent on growing offspring until some point when progeny begin to become independent of their parents, whereupon the amount of time and energy devoted to them decreases. Indeed, adult female red squirrels, Tamiascurus, at the height of lactation consume an average of 323 kilocalories of food per day compared with an average daily energy consumption of a similar-sized adult male of only about 117 kilocalories (C. Smith 1968). The time budgets of these squirrels also vary markedly with the seasons.

      In a bad dry year, many annual plants "go to seed" while still very small, whereas in a good wet year, these plants grow to a much larger size before becoming reproductive; presumably more seeds are produced in good years, but perhaps none (or very few) would be produced in a bad year if individuals attempted to grow to the sizes they reach in good years.

      An animal's time and energy budget provides a convenient starting point for clarifying some ways in which foraging influences reproduction and vice versa. Any animal has only a certain finite period of time available in which to perform all its activities, including foraging and reproduction. This total time budget, which can be considered either on a daily basis or over the animal's lifetime, will be determined both by the diurnal rhythm of activity and by the animal's ability to "make time" by performing more than one activity at the same time (such as a male lizard sitting on a perch, simultaneously watching for potential prey and predators while monitoring mates and competing males). Provided that a time period is profitable for foraging (expected gains in matter and energy exceed inevitable losses from energetic costs of foraging), any increase in time devoted to foraging clearly will increase an animal's supply of matter and energy. However, necessarily accompanying this increase in matter and energy is a concomitant decrease in time available for nonforaging activities such as mating and reproduction. Thus, profits of time spent foraging are measured in matter and energy while costs take on units of time lost. Conversely, increased time spent on nonforaging activities confers profits in time while costs take the form of decreased energy availability. Hence, gains in energy correspond to losses in time, while dividends in time require reductions in energy availability. (Of course, risks of foraging and reproduction also need to be considered.)

      The preceding arguments suggest that optimal allocation of time and energy ultimately depends on how costs in each currency vary with profits in the opposite. However, because units of costs and profits in time and energy differ, one would like to be able to convert them into a common currency. Costs and profits in time might be measured empirically in energetic units by estimating the net gain in energy per unit of foraging time. If all potential foraging time is equivalent, profits would vary linearly with costs; under such circumstances, the loss in energy associated with nonforaging activities would be directly proportional to the amount of time devoted to such activity. Optimal budgeting of time and energy into foraging versus nonforaging activities is usually profoundly influenced by various circadian and seasonal rhythms of physical conditions, as well as those of predators and potential prey. Clearly, certain time periods favorable for foraging return greater gains in energy gathered per unit time than other periods. Risks of exposure to both harsh physical conditions and predators must often figure into the optimal amount of time to devote to various activities. Ideally, one would ultimately like to measure both an animal's foraging efficiency and its success at budgeting time and energy by its lifetime reproductive success, which would reflect all such environmental "risks."

      Foraging and reproductive activities interact in another important way. Many organisms gather and store materials and energy during time periods that are unfavorable for successful reproduction but then expend these same resources on reproduction at a later, more suitable, time. Lipid storage and utilization systems obviously facilitate such temporal integration of uptake and expenditure of matter and energy. This temporal component greatly complicates the empirical measurement of reproductive effort.

      Prey density can strongly affect an animal's time and energy budget. Gibb (1956) watched rock pipits, Anthus spinoletta, feeding in the intertidal along the English seacoast during two consecutive winters. The first winter was relatively mild; the birds spent an average of 6-1/2 hours feeding, 1-3/4 hours resting, and 3/4 hour fighting in defense of their territory (total daylight slightly exceeded 9 hours). The next winter was much harsher and food was considerably scarcer; the birds spent 8-1/4 hours feeding, 39 minutes resting, and only 7 minutes on territorial defense! Apparently the combination of low food density and extreme cold (endotherms require more energy in colder weather) demanded that over 90 percent of the bird's waking hours be spent feeding and no time remained for frivolities. This example also illustrates that food is less defendable at lower densities, as indicated by reduced time spent on territorial defense. Obviously, food density in the second year was near the lower limit that would allow survival of rock pipits. When prey items are too sparse, encounters may be so infrequent that an individual cannot survive. Gibb (1960) calculated that to balance their energy budget during the winter in some places, English tits must find an insect on the average once every 2-1/2 seconds during daylight hours.

      Time and energy budgets are influenced by a multitude of other ecological factors, including body size, mode of foraging, mode of locomotion, vagility, trophic level, prey size, resource density, environmental heterogeneity, rarefaction, competition, risks of predation, and reproductive tactics.

      Leaf Tactics

      Leaves take on an almost bewildering array of sizes and shapes: some leaves are deciduous, others evergreen; some are simple, others compound; and their actual spatial arrangement on a given plant differs considerably both within and between species (Figure 5.3).

      1. Figure 5.3. Leaves have evolved a spectacular variety of shapes and sizes, yet repeatable patterns do occur.

      Some leaves are much more costly to produce and maintain than others (elementary economic considerations dictate that any given leaf must pay for itself plus generate a net energetic profit). Presumably, this great diversity of leaf tactics is a result of natural selection maximizing the lifetime reproductive success of individual plants under diverse environmental conditions. Leaf tactics are influenced by many factors that include light, water availability, prevailing winds, and herbivores. When grown in the shade, individuals of many species grow larger, less dissected leaves than when grown in the sun. Similarly, shade-tolerant plants of the understory usually have larger and less lobed leaves than canopy species. Similar types of leaves often evolve independently in different plant lineages subjected to comparable climatic conditions at different geographic localities, especially among trees (Bailey and Sinnot 1916; Ryder 1954; Stowe and Brown 1981). Compound leaves, thought to conserve woody tissue, with small leaflets are found in hot dry regions, whereas those with larger leaflets occur under warm moist conditions. Lowland wet tropical rain forest trees have large evergreen leaves with nonlobed or continuous margins, chaparral plants tend to have small sclerophyllous evergreen leaves, arid regions tend to support leafless stem succulents such as cacti or plants with entire leaf margins (especially among evergreens), plants from cold wet climates often have notched or lobed leaf margins, and so on. Such repeated patterns of leaf size and shape suggest that a general theory of leaf tactics is possible.

      Several models for optimal leaf size under differing environmental conditions have been developed. Efficiency of water use (grams of carbon dioxide assimilated per gram of water lost) was the measure of plant performance maximized by Parkhurst and Loucks (1971). A similar model for size and shape of vine leaves was developed by Givnish and Vermeij (1976). Even these relatively simple models predict several observed patterns in leaf size, such as large leaves in warm, shady, wet places and small leaves in colder areas or warmer and sunnier locales (Figure 5.4).

      1. Figure 5.4. Patterns of leaf sizes predicted under differing environmental conditions from wet to dry (mesic to xeric) and shady to sunny. The shaded region represents conditions likely to prevail in nature. [From Givnish and Vermeij (1976). Copyright © 1976 by The University of Chicago Press.]

      The evergreen versus deciduous dichotomy can be approached similarly using cost-benefit arguments (Orians and Solbrig 1977; Miller 1979). In considering leaf tactics of desert plants, Orians and Solbrig contrast leaf types along a continuum ranging from the relatively inexpensive deciduous "mesophytic" leaf to the more costly evergreen "xerophytic" leaf. Mesophytic leaves photosynthesize and transpire at a rapid rate and hence require high water availability (low "soil water potential"). In deserts, such plants grow primarily along washes. In contrast, xerophytic leaves cannot photosynthesize as rapidly when abundant water is available, but they can extract water from relatively dry soil. Each plant leaf tactic has an advantage either at different times or in different places, thereby promoting plant life form diversity. During wet periods, plants with mesophytic leaves photosynthesize rapidly, but under drought conditions, they must drop their leaves and become dormant. During such dry periods, however, the slower photosynthesizers with xerophytic leaves are still able to function by virtue of their ability to extract water from dry soils. Of course, all degrees of intermediate leaf tactics exist, each of which may enjoy a competitive advantage under particular conditions of water availability (Figure 5.5). In a predictable environment, net annual profit per unit of leaf surface area determines the winning phenotype. Even a relatively brief wet season could suffice to give mesophytic leaves a higher annual profit (which accounts for the occurrence of these plant life forms in deserts).

    2. Figure 5.5. Probable relationship between efficiency of photosynthesis and water availability among different types of leaves. The most xerophytic leaf performs best under conditions of low water availability (zone a), whereas the most mesophytic leaf does best when soils are wet (zone d). Intermediate types are superior under intermediate conditions of water availability. Shaded areas indicate superiority of various leaf types under different conditions of soil moisture availability. [Adapted from Orians and Solbrig (1977). Copyright © 1977 by The University of Chicago Press.]
    3. In an interesting discussion of leaf arrangement and forest structure, Horn (1971, 1975a, 1976) distinguished "monolayers" from "multilayers." Each plant in the multilayer of a forest (usually sunnier places such as the canopy) has leaves scattered throughout its volume at several different levels, whereas monolayer plants have essentially a single blanket or shell of leaves. Plants in the multilayer gain from a geometry that allows some light to pass through to their own leaves at lower levels. Horn points out that lobing facilitates passage of light and that such plants do well in the sun (in the shade, inner leaves may respire more than they photosynthesize). In contrast, the optimal tree design in the shade is a monolayer in which each leaf typically intercepts as much light as possible (leaves are large and seldom lobed). Moreover, slow-growing monolayered plants eventually outcompete fast-growing multilayered plants that persist by regular colonization of newly vacated areas created by continual disturbance (Horn 1976).

      Foraging Tactics and Feeding Efficiency

      Foraging tactics involve the ways in which animals gather matter and energy. As explained above, matter and energy constitute the profits gained from foraging, in that they are used in growth, maintenance, and reproduction. But foraging has its costs as well; a foraging animal may often expose itself to potential predators, and much of the time spent in foraging is rendered unavailable for other activities, including reproduction. An optimal foraging tactic maximizes the difference between foraging profits and their costs. Presumably, natural selection, acting as an efficiency expert, has often favored such optimal foraging behavior. Consider, for example, prey of different sizes and what might be termed "catchability." How great an effort should a foraging animal make to obtain a prey item with a given catchability and of a particular size (and therefore matter and energy content)? Clearly, an optimal consumer should be willing to expend more energy to find and capture food items that return the most energy per unit of expenditure upon them. Moreover, an optimal forager should take advantage of natural feeding routes and should not waste time and energy looking for prey either in inappropriate places or at inappropriate times. What is optimal in one environment is seldom optimal in another, and an animal's particular anatomy strongly constrains its optimal foraging tactic. Evidence is considerable that animals actually do attempt to maximize their foraging efficiencies, and a substantial body of theory on optimal foraging tactics exists.

      Numerous aspects of optimal foraging theory are concisely summarized in an excellent chapter, "The Economics of Consumer Choice," by MacArthur (1972). He makes several preliminary assumptions: (a) Environmental structure is repeatable, with some statistical expectation of finding a particular resource (such as a habitat, microhabitat, and/or prey item). (b) Food items can be arranged in a continuous and unimodal spectrum, such as size distributions of insects (Schoener and Janzen 1968; Hespenhide 1971). (This assumption is clearly violated by foods of some animals, such as monophagous insects or herbivores generally, because plant chemical defenses are typically discrete; see Chapter 15) (c) Similar animal phenotypes are usually closely equivalent in their harvesting abilities; an intermediate phenotype is thus best able to exploit foods intermediate between those that are optimal for two neighboring phenotypes (see Chapter 13). Conversely, similar foods are gathered with similar efficiencies; a lizard with a jaw length that adapts it to exploit 5-mm-long insects best is only slightly less efficient at eating 4- and 6-mm insects. (d) The principle of allocation applies, and no one phenotype can be maximally efficient on all prey types; improving harvesting efficiency on one food type necessitates reducing the efficiency of exploiting other kinds of items. (e) Finally, an individual's economic "goal" is to maximize its total intake of food resources. (Assumptions b, c, and d are not vital to the argument.)

      MacArthur (1972) then breaks foraging down into four phases: (1) deciding where to search; (2) searching for palatable food items; (3) upon locating a potential food item, deciding whether or not to pursue it; and (4) pursuit itself, with possible capture and eating. Search and pursuit efficiencies for each food type in each habitat are entirely determined by the preceding assumptions about morphology (assumption c) and environmental repeatability (assumption a); moreover, these efficiencies dictate the probabilities associated with the searching and pursuing phases of foraging (2 and 4, respectively). Thus, MacArthur considers only the two decisions: where to forage and what prey items to pursue (phases 1 and 3 of foraging).

      Clearly, an optimal consumer should forage where its expectation of yield is greatest -- an easy decision to make, given knowledge of the previous efficiencies and the structure of its environment (in reality, of course, animals are far from omniscient and must make decisions based on incomplete information). The decision as to which prey items to pursue is also simple. Upon finding a potential prey item, a consumer has only two options: either pursue it or go on searching for a better item and pursue that one instead. Both decisions end in the forager beginning a new search, so the best choice is clearly the one that returns the greatest yield per unit time. Thus, an optimal consumer should opt to pursue an item only when it cannot expect to locate, catch, and eat a better item (i.e., one that returns more energy per unit of time) during the time required to capture and ingest the first prey item.

      Many animals, such as foliage-gleaning insectivorous birds, spend much of their foraging time searching for prey but expend relatively little time and energy pursuing, capturing, and eating small sedentary insects that are usually easy to catch and quickly swallowed. In such "searchers," mean search time per item eaten is large compared to average pursuit time per item; hence, the optimal strategy is to eat essentially all palatable insects encountered. Other animals ("pursuers") that expend little energy in finding their prey but a great deal of effort in capturing it (such as, perhaps, a falcon or a lion) should select prey with small average pursuit times (and energetic costs). Hence, pursuers should generally be more selective and more specialized than searchers. Moreover, because a food-dense environment offers a lower average search time per item than does a food-sparse area, an optimal consumer should restrict its diet to only the better types of food items in the former habitat. To date, optimal foraging theory has been developed primarily in terms of the rate at which energy is gathered per unit of time. Limiting materials such as nutrients in short supply and the risks of predation have so far been largely neglected.

      Carnivorous animals forage in extremely different ways. In the "sit-and-wait" mode, a predator waits in one place until a moving prey item comes by and then "ambushes" the prey; in the "widely foraging" mode, the predator actively searches out its prey (Pianka 1966b; Schoener 1969a, 1969b). The second strategy normally requires a greater energy expenditure than the first. The success of the sit-and-wait tactic usually depends on one or more of three conditions: a fairly high prey density, high prey mobility, and low predator energy requirements. The widely foraging tactic also depends on prey density and mobility and on the predator's energy needs, but here the distribution of prey in space and the predator's searching abilities assume paramount importance. Although these two tactics are endpoints of a continuum of possible foraging strategies (and hence somewhat artificial), foraging techniques actually employed by many organisms are rather strongly polarized. The dichotomy of sit-and-wait versus widely foraging therefore has substantial practical value. Among snakes, for example, racers and cobras forage widely when compared with boas, pythons, and vipers, which are relatively sit-and-wait foragers. Among hawks, accipiters such as Cooper's hawks and goshawks often hunt by ambush using a sit-and-wait strategy, whereas most buteos and many falcons are relatively more widely foraging. Web-building spiders and sessile filter feeders such as barnacles typically forage by sitting and waiting. Many spiders expend considerable amounts of energy and time building their webs rather than moving about in search of prey; those that do not build webs forage much more widely. Some general correlates of these two modes of foraging are listed in Table 5.1.

      Table 5.1 Some General Correlates of Foraging Mode

      _______________________________________________________________________

      Sit-and-Wait Widely Foraging

      _______________________________________________________________________

      Prey type Eat active prey Eat sedentary and unpre- dictable (but clumped or
      large) prey

      Volume prey captured/dayLow Generally high, but low
      in certain species

      Daily metabolic expense Low High

      Types of predators Vulnerable primarily Vulnerable to both sit-and-
      to widely foraging wait and to widely
      predators foraging predators

      Rate of encountersProbably lowProbably high
      with predators

      MorphologyStocky (short tails)Streamlined (generally
      long tails)

      Probable physiologicalLimited enduranceHigh endurance capacity
      correlates(anaerobic)(aerobic)

      Relative clutch mass High Low

      Sensory modeVisual primarily Visual or olfactory

      Learning abilityLimitedEnhanced learning and
      memory, larger brains

      Niche breadthWideNarrow

      _______________________________________________________________________

      Source: Adapted from Huey and Pianka (1981).

      Similar considerations can be applied in comparing herbivores with carnivores. Because the density of plant food almost always greatly exceeds the density of animal food, herbivores often expend little energy, relative to carnivores, in finding their prey (to the extent that secondary chemical compounds of plants, such as tannins, and other antiherbivore defenses reduce palatability of plants or parts of plants, the effective supply of plant foods may be greatly reduced). Because cellulose in plants is difficult to digest, however, herbivores must expend considerable energy in extracting nutrients from their plant food. (Most herbivores have a large ratio of gut volume to body volume, harbor intestinal microorganisms that digest cellulose, and spend much of their time eating or ruminating -- envision a cow chewing its cud.) Animal food, composed of readily available proteins, lipids, and carbohydrates, is more readily digested; carnivores can afford to expend considerable effort in searching for their prey because of the large dividends obtained once they find it. As would be expected, the efficiency of conversion of food into an animal's own tissues (assimilation) is considerably lower in herbivores than it is in carnivores.

      1. Figure 5.6. Diagram showing how Holling used geometry to calculate an estimated optimal size of a prey item from the anatomy of a mantid's foreleg. Optimal prey diameter, D, is simply T sin (β - α), where T is the distance A to C. [From Holling (1964).]
      1. Figure 5.7. The percentage of prey items actually attacked
        by hungry mantids versus prey size. [From Holling (1964).]

      Many carnivores have extremely efficient prey-capturing devices (see Chapter 15); often the size of a prey object markedly influences this efficiency. Using simple geometry (Figure 5.6), Holling (1964) estimated the diameter of a prey item that should be optimal for a praying mantid of a particular size. He then offered hungry mantids prey objects of various sizes and recorded percentages attacked (Figure 5.7). Mantids were noticeably reluctant to attack prey that were either much larger or much smaller than the estimated optimum. Hence, natural selection has resulted in efficient predators both by producing efficient prey-capturing devices and by programming animals so that they are unlikely to attempt to capture decidedly suboptimal items. Larger predators tend to take larger prey than smaller ones (see Figure 12.12). It may in fact be better strategy for a large predator to overlook prey below some minimal size threshold and to spend the time that would have been spent in capturing and eating such small items in searching out larger prey (see also above). Similarly, the effort a predator will expend on any given prey item is proportional to the expected return from that item (which usually increases with prey size). Thus, a lizard waiting on a perch will not usually go far for a very small prey item but will often move much greater distances in attempts to obtain larger prey.

      Because small prey are generally much more abundant than large prey, most animals encounter and eat many more small prey items than large ones. Small animals that eat small prey items encounter prey of suitable size much more frequently than do larger animals that rely on larger prey items; as a result, larger animals tend to eat a wider range of prey sizes. Because of such increased food niche breadths of larger animals, size differences between predators increase markedly with increasing predator size (MacArthur 1972).

      Physiological Ecology

      The concern of environmental physiology, or ecophysiology, is how organisms function within, adapt and respond to, and exploit their physical environments. Physiological ecologists are interested primarily in the immediate functional and behavioral mechanisms by which organisms cope with their abiotic environments. Physiological mechanisms clearly must reflect ecological conditions; moreover, mutual constraints between physiology and ecology dictate that both must evolve together in a synergistic fashion.

      A fundamental principle of physiology is the notion of homeostasis, the maintenance of a relatively stable internal state under a much wider range of external environmental conditions. Homeostasis is achieved not only by physiological means but also by appropriate behavioral responses. An example is temperature regulation in which an organism maintains a fairly constant body temperature over a considerably greater range of ambient thermal conditions (homeostasis is never perfect). Homeostatic mechanisms have also evolved that buffer environmental variation in humidity, light intensity, and concentrations of various substances such as hydrogen ions (pH), salts, and so on. By effectively moderating spatial and temporal variation in the physical environment, homeostasis allows organisms to persist and be active within a broad range of environmental conditions, thereby enhancing their fitness. The subject of environmental physiology is vast; some references are given at the end of this chapter.

      Physiological Optima and Tolerance Curves

      Physiological processes proceed at different rates under different conditions. Most, such as rate of movement and photosynthesis, are temperature dependent (Figure 5.8). Other processes vary with availability of various materials such as water, carbon dioxide, nitrogen, and hydrogen ions (pH). Curves of performance, known as tolerance curves (Shelford 1913b), are typically bell shaped and unimodal, with their peaks representing optimal conditions for a particular physiological process and their tails reflecting the limits of tolerance. Some individuals and species have very narrow peaked tolerance curves; in others these curves are considerably broader. Broad tolerance curves are described with the prefix eury- (e.g., eurythermic, euryhaline), whereas steno- is used for narrow ones (e.g., stenophagous). An organism's use of environmental resources such as foods and microhabitats can profitably be viewed similarly, and performance can be measured in a wide variety of units such as survivorship, reproductive success, foraging efficiency, and fitness.

      1. Figure 5.8. Two plots of performance against temperature. (a) Goldfish swimming speed versus temperature for fish acclimated to different thermal conditions; in most cases, performance peaks near the temperature to which fish are accustomed. [From Ricklefs (1973) after Fry and Hart (1948).] (b) Photosynthetic rate versus leaf temperature in the plant Atriplex lentiformis at two different localities. [From Mooney, Bjorkman, and Berry (1975).]

      Performance curves can sometimes be altered during the lifetime of an individual as it becomes exposed to different ambient external conditions. Such short-term alteration of physiological optima is known as acclimation (Figure 5.8). Within certain design constraints, tolerance curves clearly must change over evolutionary time as natural selection molds them to reflect changing environmental conditions. However, very little is known about the evolution of tolerance; most researchers have merely described the range(s) of conditions tolerated or exploited by particular organisms. Tolerance curves are often taken almost as given and immutable, with little or no consideration of the ecological and evolutionary forces that shape them.

      Performance or tolerance is often sensitive to two or more environmental variables. For example, the fitness of a hypothetical organism in various microhabitats might be a function of relative humidity (or vapor pressure deficit), somewhat as shown in Figure 5.9a. Assume that fitness varies similarly along a temperature gradient (Figure 5.9b). Figure 5.9c combines humidity and temperature conditions to show variation in fitness with respect to both variables simultaneously (a third axis, fitness, is implicit in this figure). The range of thermal conditions tolerated is narrower at very low and very high humidities than it is at intermediate and more optimal humidities. Similarly, an organism's tolerance range for relative humidity is narrower at extreme temperatures than it is at more optimal ones. The organism's thermal optimum depends on humidity conditions (and vice versa). Fitness reaches its maximum at intermediate temperatures and humidities. Hence, temperature tolerance and tolerance of relative humidities interact in this example. The concept of a single fixed optimum is in some ways an artifact of considering only one environmental dimension at a time.

      1. Figure 5.9. Hypothetical responses curves showing how two variables can interact to determine an organism's fitness. Fitness is reduced at extremes of either temperature or humidity, and the range of humidities tolerated is less at extreme temperatures than it is at intermediate ones.

      Energetics of Metabolism and Movement

      Some of the food ingested by any animal passes through its gut unused. Such egested material can be as high as 80 to 90 percent of the total intake in some caterpillars (Whittaker 1975). Food actually digested is termed assimilation: A fraction of this must be used in respiration to support maintenance metabolism and activity. The remainder is incorporated into the animal concerned as secondary productivity and ultimately can be used either in growth or in reproduction. These relationships are summarized below:

      Ingestion = Assimilation + Egestion

      Assimilation = Productivity + Respiration

      Productivity = Growth + Reproduction

      The total amount of energy needed per unit time for maintenance increases with increasing body mass (Figure 5.10). However, because small animals have relatively high ratios of body surface to body volume, they generally have much higher metabolic rates and hence have greater energy requirements per unit of body weight than larger animals (Figure 5.11). Animals that maintain relatively constant internal body temperatures are known as homeotherms; those whose temperatures vary widely from time to time, usually approximating the temperature of their immediate environment, are called poikilotherms. These two terms are sometimes confused with a related pair of useful terms. An organism that obtains its heat from its external environment is an ectotherm; one that produces most of its own heat internally by means of oxidative metabolism is known as an endotherm. All plants and the vast majority of animals are ectothermic; the only continuously endothermic animals are found among birds and mammals (but even some of these become ectothermic at times). Some poikilotherms (large reptiles and certain large fast-swimming fish such as tuna) are at times at least partially endothermic. Certain ectotherms (many lizards and temperate-zone flying insects) actually regulate their body temperatures fairly precisely during periods of activity by appropriate behavioral means. Thus, ectotherms at times can be homeotherms! An active bumblebee or desert lizard may have a body temperature as high as that of a bird or mammal (the layman's terms "warm-blooded" and "cold-blooded" can thus be quite misleading and should be abandoned). Because energy is required to maintain a constant internal body temperature, endotherms have considerably higher metabolic rates, as well as higher energy needs (and budgets), than ectotherms of

      1. Figure 5.10. Metabolic rates of a variety of organisms of different sizes (log-log plot). Total oxygen consumption increases with increasing body size. [From Schmidt-Nielsen (1975).]
      1. Figure 5.11. Semilogarithmic plot of rates of oxygen consumption per unit of body mass for a wide variety of mammals plotted against body mass. [From Schmidt-Nielsen (1975).]

      the same body mass. There is a distinct lower limit on body size for endotherms -- about the size of a small hummingbird or shrew (2 or 3 grams). Indeed, both hummingbirds and shrews have very high metabolic rates and hence rather precarious energetic relationships; they depend on continual supplies of energy-rich foods. Small hummingbirds would starve to death during cold nights if they did not allow their body temperatures to drop and go into a state of torpor.

      Body size, diet, and movements are complexly intertwined with the energetics of metabolism. Energy requirements do not scale linearly with body mass, but instead as a fractional exponent: E = k m0.67 where k is a taxon-specific constant and m is body mass. Large animals require more matter and energy for their maintenance than small ones, and in order to obtain it they usually must range over larger geographical areas than smaller animals with otherwise similar food requirements. Food habits also influence movements and home range size. Because the foods of herbivorous animals that eat the green parts of plants (such as grazers, which eat grasses and ground-level vegetation, and browsers, which eat tree leaves) are usually quite dense, these animals usually do not have very large home ranges. In contrast, carnivores and those herbivores that must search for their foods (such as granivores and frugivores, which eat seeds and fruits, respectively) frequently spend much of their foraging time and energy in search, ranging over considerably larger areas. McNab (1963) termed the first group "croppers" and the latter "hunters." Croppers generally exploit foods that occur in relatively dense supply, whereas hunters typically utilize less dense foods. Hunters are often territorial, but croppers seldom defend territories. Croppers and hunters are not discrete but in fact grade into each other (Figure 5.12). A browser that eats only the leaves of a rare tree might be more of a hunter than a granivore that eats the seeds of a very common plant. However, such intermediates are uncommon enough that separation into two categories is useful for many purposes. Figure 5.13 shows the correlation between home range size and body weight for a variety of mammalian species, here separated into croppers and hunters. Analogous correlations, but with different slopes and/or intercepts, have been obtained for birds and lizards (Schoener 1968b; Turner et al. 1969). Very mobile animals, like birds, frequently range over larger areas than less mobile animals such as terrestrial mammals and lizards. In areas of low productivity (for example, deserts), most animals may be forced to range over a greater area to find adequate food than they would in more productive regions. Large home ranges or territories usually result in low densities, which in turn markedly limit possibilities for the evolution of sociality. Thus, McNab (1963) points out that complex social behavior has usually evolved only in croppers and/or among exceptionally mobile hunters.

      1. Figure 5.12. Biomass, in kilograms/hectare, of various mammals, arranged according to their food habits. Although mammals as a class vary over five orders of magnitude, the range among those that eat any given type of food is considerably smaller. Meat eaters and omnivores are much less dense than herbivores. [From Odum (1959) after Mohr (1940).]

       

      1. Figure 5.13. Log-log plot of average home range area against mean body mass for a variety of mammals, separated into "croppers" (open symbols and lower regression line) and "hunters" (closed symbols and upper line). [After McNab (1963).]

      The metabolic cost of movement varies with both an animal's body size and its mode of locomotion. The cost of moving a unit of body mass some standard distance is actually less in larger animals than in smaller ones (Figure 5.14). Terrestrial locomotion is the most expensive mode of transportation, flight is intermediate in cost, and swimming is the most economical means of moving about -- provided body shape is fusiform and buoyancy is neutral (Figure 5.14).

      1. Figure 5.14. Comparison of the energetic cost of moving a unit of body mass one kilometer for several different modes of locomotion. [From Schmidt-Nielsen (1975).]

      Physiologists have documented numerous consistent size-related trends in organs and metabolic properties. For example, among mammals, heart mass is always about 0.6 percent of total body mass, whereas blood volume is almost universally about 5.5 percent of body mass over a great range of body sizes (these organ systems are thus directly proportional to size). Other physiological attributes, such as lung surface in mammals, vary directly with metabolic rate rather than with size. However, some organ systems, such as the kidney and liver, do not scale directly with either size or metabolic rate (Schmidt-Nielsen 1975). Such "physiological rules" apparently dictate available avenues for physiological change, thereby constraining possible ecological adaptations.

      Adaptation and Deterioration of Environment

      Organisms are adapted to their environments in that, to survive and reproduce, they must meet their environment's conditions for existence. Evolutionary adaptation can be defined as conformity between an organism and its environment. Plants and animals have adapted to their environments both genetically and by means of physiological, behavioral, and/or developmental flexibility. The former includes instinctive behavior and the latter learning. Adaptation has many dimensions in that most organisms must conform simultaneously to numerous different aspects of their environments. Thus, for an organism to adapt, it must cope not only with various aspects of its physical environment, such as temperature and humidity conditions, but also with competitors, predators, and escape tactics of its prey. Conflicting demands of these various environmental components often require that an organism compromise in its adaptations to each. Conformity to any given component takes a certain amount of energy that is then no longer available for other adaptations. The presence of predators, for example, may require that an animal be wary, which in turn is likely to reduce its foraging efficiency and hence its competitive ability.

      Organisms can conform to and cope with highly predictable environments relatively easily, even when they change in a regular way, as long as they are not too extreme. Adaptation to an unpredictable environment is usually more difficult; adapting to extremely erratic environments may even prove impossible. Many organisms have evolved dormant stages that allow them to survive unfavorable periods, both predictable and unpredictable. Annual plants everywhere and brine shrimp in deserts are good examples. Brine shrimp eggs survive for years in the salty crust of dry desert lakes; when a rare desert rain fills one of these lakes, the eggs hatch, the shrimp grow rapidly to adults, and they produce many eggs. Some seeds known to be many centuries old are still viable and have been germinated. Changes in the environment that reduce overall adaptation are collectively termed the "deterioration of environment"; such changes cause directional selection resulting in accommodation to the new environment.

      A simple but elegant model of adaptation and undirected environmental deterioration was developed by Fisher (1930). He reasoned that no organism is "perfectly adapted" -- all must fail to conform to their environments in some ways and to differing degrees. However, a hypothetical, perfectly adapted organism can always be imagined (actually this reflects the environment) against which existing organisms may be compared. Fisher's mathematical argument is phrased in terms of an infinite number of "dimensions" for adaptation (only three are used here for ease of illustration).

      Imagine an adaptational space of three coordinates representing, respectively, the competitive, predatory, and physical environments (Figure 5.15). An ideal "perfectly adapted" organism lies at a particular point (say A) in this space, but any given real organism is at another point (say B), some distance, d, away from the point of perfect adaptation. Changes in the position of A correspond to environmental changes making the optimally adapted organism different; changes in B represent changes in the organisms concerned, such as mutations. The distance between the two points, d, represents the degree of conformity between the organism and environment, or the level of adaptation. Fisher noted that very small undirected changes in either organism or environment have a 50:50 chance of being to the organism's advantage (i.e., reducing the distance between A and B). The probability of such improvement is inversely related to the magnitude of the change (Figure 5.16).

      1. Figure 5.15. Fisher's model of adaptation and deterioration of environment. Point A represents a hypothetical "perfectly adapted" organism; an actual organism (point B) is never perfectly adapted and thus lies at some distance, d, from point A. The surface of the sphere represents all possible points with a level of adaptation equal to the organism under consideration. Very small undirected changes in either organism (point B) or environment (point A) are equally likely to increase or to decrease the level of adaptation, d. Notice the duality of the model (make A --> B and B --> A).
      1. Figure 5.16. The probability of improvement of the level of adaptation (i.e., of reducing d) is plotted against the magnitude of an undirected change when the number of dimensions is large. Two hypothetical organisms are shown, one highly adapted such as a specialist with narrow tolerance limits and one less highly adapted such as a generalist with broader tolerance limits and/or a greater number of niche dimensions. A random change of a given magnitude is more likely to improve the level of adaptation of the generalist than the specialist. [Partially adapted from Fisher (1958a).]

      Very great changes in either organism or environment are always maladaptive because even if they are in the correct direction, they "overshoot" points of closer adaptation. (Of course, it is remotely possible that such major environmental changes or "macromutations" could put an organism into a completely new adaptive realm and thereby improve its overall level of adaptation.) Fisher makes an analogy with focusing a microscope. Very fine changes are as likely as not to improve the focus, but gross changes will almost invariably throw the machine further out of focus. Organisms may be thought of as "tracking" their environments in both ecological and evolutionary time, changing as their environments change; thus, as point A shifts because of daily, seasonal, and long-term environmental fluctuations, point B follows it. Such environmental tracking may be physiological (as in acclimation), behavioral (including learning), and/or genetic (evolutionary), depending on the time scale of environmental change. Reciprocal counterevolutionary responses to other species (prey, competitors, parasites, and predators) constitute examples of such evolutionary tracking,1 and have been termed coevolution (see Chapter 15). Individual organisms with narrow tolerance limits, such as highly adapted specialists, generally suffer greater losses in fitness due to a unit of environmental deterioration than generalized organisms with more versatile requirements, all else being equal. Thus, more specialized organisms and/or those with restricted homeostatic abilities cannot tolerate as much environmental change as generalists or organisms with better developed homeostasis (Figure 5.16). Fisher's (1930) model applies only to nondirected changes in either party of the adaptational complex -- such as mutations and perhaps certain climatic fluctuations, or other random events. However, many environmental changes are probably nonrandom. Changes in other associated organisms, especially predators and prey, are invariably directed so as to reduce an organism's degree of conformity to its environment; thus, they constitute a deterioration of that organism's environment. Directed changes in competitors can either increase or decrease an organism's level of adaptation, depending on whether they involve avoidance of competition or improvements in competitive ability per se. Directed changes in mutualistic systems would usually tend to improve the overall level of adaptation of both parties.

      Heat Budgets and Thermal Ecology

      When averaged over a long enough period of time, heat gained by an organism must be exactly balanced by heat lost to its environment; otherwise the plant or animal would either warm up or cool off. Many different pathways of heat gains and heat losses exist (Figure 5.17). The notion of a heat budget is closely related to the concept of an energy budget; balancing a heat budget requires very different adaptations under varying environmental conditions. At different times of day, ambient thermal conditions may change from being too cold to being too warm for a particular organism's optimal performance. Organisms living in hot deserts must avoid overheating by being able to minimize heat loads and to dissipate heat efficiently; in contrast, those that live in colder places such as at high altitudes or in polar regions must avoid overcooling -- hence they have evolved efficient means of heat retention, such as insulation by blubber, feathers, or fur, that reduce the rate of heat exchange with the external environment.

      1. Figure 5.17. Diagrammatic representation of various pathways of heat gains and losses between an animal and its environment under moderately warm conditions. Heat exchange between an animal and its environment is roughly proportional to its body surface: Because small animals have a larger surface area relative to their weight than larger ones, the former gain or lose relatively more heat than the latter. [From Bartholomew (1972). Reprinted with permission of Macmillan Publishing Co., Inc., from Animal Physiology: Principles and Adaptations, M. S. Gordon (ed.). Copyright © 1972 by Malcolm S. Gordon.]

      As seen in previous chapters, environmental temperatures fluctuate in characteristic ways at different places over the earth's surface, both daily and seasonally. In the absence of a long-term warming or cooling trend, environmental temperatures at any given spot remain roughly constant when averaged over an entire annual cycle. Recall that the range in temperature within a year is much greater at high latitudes than it is nearer the equator. An organism could balance its annual heat budget by being entirely passive and simply allowing its temperature to mirror that of its environment. Such a passive thermoregulator is known as a thermoconformer (Figures 5.18 and 5.19). Of course, it is also an ectotherm. Another extreme would be to maintain an absolutely constant body temperature by physiological and/or behavioral means, dissipating (or avoiding) excess bodily heat during warm periods but retaining (or gaining) heat during cooler periods (in endotherms, energy intake is often increased during cold periods and more metabolic heat is produced to offset the increased heat losses).

      1. Figure 5.18. Average temperatures of leaves of Larrea divaricata and Ambrosia deltoidea during three sunny days in June with slight breezes prevailing. [From Patten and Smith (1975).]
      1. Figure 5.19. Body temperatures of 86 active Australian nocturnal gekkonid lizards (Nephrurus laevissimus) plotted against ambient air temperature. The line represents body temperatures equal to air temperatures. Like most nocturnal lizards, these animals are nearly perfect thermoconformers.

      Organisms that carefully regulate their internal temperatures are called thermoregulators, or homeotherms. (Recall that both endotherms and ectotherms may regulate their body temperatures.) There is, of course, a continuum between the two extremes of perfect conformity and perfect regulation (see Figure 5.22). Homeostasis, remember, is never perfect. Because regulation clearly has costs and risks as well as profits, an emerging conceptual framework envisions an optimal level of regulation that depends on the precise form of the constraints and interactions among the costs and benefits arising from a particular ecological situation (Huey and Slatkin 1976). Thermoregulation often involves both physiological and behavioral adjustments; as an example of the latter, consider a typical terrestrial diurnal desert lizard. During the early morning, when ambient temperatures are low, such a lizard locates itself in warmer microclimates of the environmental thermal mosaic (e.g., small depressions in the open or on tree trunks), basking in the sun with its body as perpendicular as possible to the sun's rays and thereby maximizing heat gained. With the daily march of temperature, ambient thermal conditions quickly rise and the lizard seeks cooler shady microhabitats. Individuals of some species retreat into burrows as temperatures rise; others climb up off the ground into cooler air and orient themselves facing into the sun's rays, thereby reducing heat load. Many lizards change colors and their heat reflectance properties, being dark and heat absorbent at colder times of day but light and heat reflectant at hotter times. Such adjustments allow individual lizards to be active over a longer period of time than they could be if they conformed passively to ambient thermal conditions; presumably, they are also more effective competitors and better able to elude predators as a result of such thermoregulatory behaviors.

      Hot, arid regions typically support rich lizard faunas, whereas cooler forested areas have considerably fewer lizard species and individuals. Lizards can enjoy the benefits of a high metabolic rate during relatively brief periods when conditions are appropriate for activity and yet can still become inactive during adverse conditions. By facilitating metabolic inactivity on both a daily and a seasonal basis, poikilothermy thus allows lizards to capitalize on unpredictable food supplies. Ectotherms are low-energy animals; one day's food supply for a small bird will last a lizard of the same body mass for a full month! Most endothermic diurnal birds and mammals must wait out the hot midday period at considerable metabolic cost, whereas lizards can effectively reduce temporal heterogeneity by retreating underground, becoming inactive, and lowering their metabolic rate during harsh periods (some desert rodents estivate when food and/or water is in short supply). Poikilothermy may well contribute to the apparent relative success of lizards over birds and mammals in arid regions. Forests and grasslands are probably simply too shady and too cold for ectothermic lizards to be very successful because these animals depend on basking to reach body temperatures high enough for activity; in contrast, birds and mammals do quite well in such areas partly because of their endothermy.

      Water Economy in Desert Organisms

      Because water conservation is a major problem for desert organisms, their physiological and behavioral adaptations for acquisition of water and for economy of its use have been well studied. These interesting adaptations are quite varied. Like energy and heat budgets, water budgets must balance; losses must be replaced by gains. For examples of water acquisition mechanisms, consider rooting strategies. Desert plants may usually invest considerably more in root systems than plants from wetter areas; one study showed that perennial shrubs in the Great Basin desert allocate nearly 90 percent of their biomass to underground tissues (Caldwell and Fernandez 1975), whereas roots apparently represent a much smaller fraction (only about 10 percent) of the standing crop biomass of a mesic hardwood forest.

      The creosote bush Larrea divaricata has both a surface root system and an extremely deep tap root that often reaches all the way down to the water table. This long tap root provides Larrea with water even during long dry spells when surface soils contain little moisture. Cacti, in contrast, have an extensive but relatively shallow root system and rely on water storage to survive drought. Many such desert plants have tough sclerophyllous xerophytic leaves that do not allow much water to escape (they also photosynthesize at a low rate as a consequence). Mesophytic plants occur in deserts too, but they photosynthesize rapidly and grow only during periods when moisture is relatively available; they drop their leaves and become inactive during droughts. Plants also reduce water losses during the heat of midday by closing their stomata and drooping their leaves (wilting). Many desert plants and animals absorb and use atmospheric and/or substrate moisture; most can also tolerate extreme desiccation.

      Camels do not rely on water storage to survive water deprivation, as is commonly thought, but can lose as much as a quarter of their body mass, primarily as water loss (Schmidt-Nielsen 1964). Like many desert organisms, camels also conserve water by allowing their temperature to rise during midday. Moreover, camels tolerate greater changes in plasma electrolyte concentrations than less drought-adapted animals. In deserts, small mammals like kangaroo rats survive without drinking by relying on metabolic water derived from the oxidation of their food (here, then, is an interface between energy budgets and water budgets). Most desert rodents are nocturnal and avoid using valuable water for heat regulation by spending hot daytime hours underground in cool burrows with high relative humidity, thereby minimizing losses to evaporation (most desert organisms resort to evaporative cooling mechanisms such as panting only in emergencies). The urine of kangaroo rats is extremely concentrated and their feces contain little water (Schmidt-Nielsen 1964). Most other desert animals minimize water losses in excretion, too. Birds and lizards produce solid uric acid wastes rather than urea, thereby requiring little water for excretion. Desert lizards also conserve water by retreating to burrows and lowering their metabolic rate during the heat of the day.

      Other Limiting Materials

      Numerous other materials, including calcium, chloride, magnesium, nitrogen, potassium, and sodium, may be in short supply for particular organisms and must therefore be budgeted. Neural mechanisms of animals depend on sodium, potassium, and chloride ions, which are sometimes available in limited quantities. Because many herbivorous mammals obtain little sodium from their plant foods (plants lack nerves and sodium is not essential to their physiology), these animals must conserve sodium and/or find supplemental sources at salt licks -- indeed, Feeny (1975) suggests that plants may actually withhold sodium as an antiherbivore tactic. Similarly, amino acids are in short supply for many insects, such as in Heliconius butterflies, which supplement their diets with protein-rich pollen (Gilbert 1972).

      An organism's nutrient and vitamin requirements are strongly influenced by the evolution of its metabolic pathways; likewise, these same pathways may themselves determine certain of the organism's nutritional needs. To illustrate: Almost all species of vertebrates synthesize their own ascorbic acid, but humans and several other primate species that have been tested cannot; they require a dietary supplement of ascorbic acid, known as vitamin C. Of thousands of other species of mammals, only two -- the guinea pig and an Indian fruit-eating bat -- are known to have lost the ability to synthesize their own ascorbic acid. A few species of birds must supplement their diets with ascorbic acid, too. Thus, a frog, a lizard, a sparrow, or a rat can make its own ascorbic acid, but we cannot. Why should natural selection favor the loss of the ability to produce a vital material? Pauling (1970) suggests that species of animals that have lost this capacity evolved in environments with ample supplies of ascorbic acid in available foods. It might actually be advantageous to dismantle a biochemical pathway in favor of another once it becomes redundant. Conversely, natural selection should favor evolution of the ability to synthesize any necessary materials that cannot be predictably obtained from available foods where this is possible (clearly organisms cannot synthesize elements -- herbivores cannot make sodium).

      Sensory Capacities and Environmental Cues

      Animals vary tremendously in their perceptive abilities. Most (except some cave dwellers and deep-sea forms) use light to perceive their environments. But visual spectra and acuity vary greatly. Some, such as insects, fish, lizards, and birds, have color vision, whereas others (most mammals, except squirrels and primates) do not. Ants, bees, and some birds can detect polarized light and exploit this ability to navigate by the sun's position; pigeons have poorly understood backup systems that enable them to return home remarkably well even when their vision is severely impaired with opaque contact lenses. Many temperate zone species of plants and animals rely on changes in day length to anticipate seasonal changes in climatic conditions. This, in turn, requires an accurate "biological clock." (Some organisms may also use barometric pressure to anticipate climatic changes.)

      Certain snakes, such as pit vipers and boas, have evolved infrared receptors that allow them to locate and capture endothermic prey in total darkness. Most animals can hear, of course, although response to different frequencies varies considerably (some actually perceive ultrasonic sounds). Bats and porpoises emit and exploit sonar signals to navigate by echolocation. Similarly, nocturnal electric fish perceive their immediate environments by means of self-generated electrical fields. Certain bioluminescent organisms, such as "fireflies" (actually beetles), produce their own light for a variety of purposes, including attraction of mates and prey as well as (possibly) predator evasion (in some cases a mutualistic relationship is formed with a bioluminescent bacteria). Certain deep-sea fish probably use their "headlights" to find prey in the dark depths of the ocean. Pigeons can detect magnetic fields. Although a few animals have only a relatively feeble sense of smell (birds and humans, for example), most have keen chemoreceptors and/or olfactory abilities. Certain male moths can detect exceedingly dilute pheromones released by a female a full kilometer upwind, allowing these males to find females at considerable distances. Similarly, dung beetles use a zigzag flight to "home in" on upwind fecal material with remarkable precision.

      Various environmental cues clearly provide particular animals with qualitatively and quantitatively different kinds and amounts of information. Certain environmental cues are useful in the context of capturing prey and escaping predators; others may facilitate timing of reproduction to coincide with good conditions for raising young. Some environmental signals are noisier and less reliable than others. Moreover, the ability to process information received from the environment is limited by a finite neural capacity. The principle of allocation and the notion of trade-offs dictate that an individual cannot perceive all environmental cues with high efficiency. If ability to perceive a broad range of environmental stimuli actually requires lowered levels of performance along each perceptual dimension, natural selection should improve perceptual abilities along certain critical dimensions at the expense of other less useful ones. Clearly, echolocation has tremendous utility for a nocturnal bat, whereas vision is relatively much less useful. In contrast, the values of these two senses are reversed for a diurnal arboreal squirrel. Within phylogenetic constraints imposed by its evolutionary history, an animal's sensory capacities can be viewed as a bioassay of the importance of particular perceptual dimensions and environmental cues in that animal's ecology.

      Adaptive Suites

      A basic point of this chapter is that any given organism possesses a unique coadapted complex of physiological, behavioral, and ecological traits whose functions complement one another and enhance that organism's reproductive success. Such a constellation of adaptations has been called an optimal design (Rosen 1967) or an adaptive suite (Bartholomew 1972).

      Consider the desert horned lizard Phrynosoma platyrhinos (Figure 5.20). Various features of its anatomy, behavior, diet, temporal pattern of activity, thermoregulation, and reproductive tactics can be profitably interrelated and interpreted to provide an integrated view of the ecology of this interesting animal (Pianka and Parker 1975a). Horned lizards are ant specialists and usually eat essentially nothing else. Ants are small and contain much undigestible chitin, so that large numbers of them must be consumed. Hence, an ant specialist must possess a large stomach for its body size. When expressed as a proportion of total body mass, the stomach of this horned lizard occupies a considerably larger fraction of the animal's overall body mass (about 13 percent) than do the stomachs of all other sympatric desert lizard species, including the herbivorous desert iguana Dipsosaurus dorsalis (herbivores typically have lower assimilation rates and larger stomachs than carnivores). Possession of such a large gut necessitates a tanklike body form, reducing speed; selection has favored a spiny body form and cryptic behavior rather than a sleek body and rapid movement to cover (as in most other species of lizards), decreasing the lizard's ability to escape from predators by flight. As a result, natural selection has favored a spiny body form and cryptic behavior rather than a sleek body and rapid movement to cover (as in most other species of lizards).

      Risks of predation are likely to be increased during long periods of exposure while foraging in the open. A reluctance to move, even when actually threatened by a potential predator, could well be

      1. Figure 5.20. Diagrammatic portrayal of factors influencing the ecology and body form of the North American desert horned lizard, Phrynosoma platyrhinos.

      advantageous; movement might attract attention of predatorsand negate the advantage of concealing coloration and contour. Such decreased movement doubtless contributes to the observed high variance in body temperature of Phrynosoma platyrhinos, which is significantly greater than that of all other species of sympatric lizards.

      Phrynosoma platyrhinos are also active over a longer time interval than any sympatric lizard species. Wide fluctuations in horned lizard body temperatures under natural conditions presumably reflect both the long activity period and perhaps their reduced movements into or out of the sun and shade (most of these lizards are in the open sun when first sighted). More time is thus made available for activities such as feeding. A foraging anteater must spend considerable time feeding. Food specialization on ants is economically feasible only because these insects usually occur in a clumped spatial distribution and hence constitute a concentrated food supply. To make use of this patchy and spatially concentrated, but at the same time not overly nutritious, food supply, P. platyrhinos has evolved a unique constellation of adaptations that include a large stomach, spiny body form, an expanded period of activity, and "relaxed" thermoregulation (eurythermy). The high reproductive investment of adult horned lizards is probably also a simple and direct consequence of their robust body form. Lizards that must be able to move rapidly to escape predators, such as racerunners (Aspidoscelis formerly Cnemidophorus), would hardly be expected to weight themselves down with eggs to the same extent as animals like horned lizards that rely almost entirely upon spines and camouflage to avoid their enemies.

      Energetics of metabolism of weasels provide another, somewhat more physiological, example of a suite of adaptations (Brown and Lasiewski 1972). Due to their long, thin body shape, weasels have a higher surface-to-volume ratio than mammals with a more standard shape, and as a consequence, they have an increased energy requirement. Presumably, benefits of the elongate body form more than outweigh associated costs; otherwise natural selection would not have favored evolution of the weasel body shape. Brown and Lasiewski (1972) speculate that a major advantage of the elongate form is the ability to enter burrows of small mammals (weasel prey), which results in increased hunting success and thus allows weasels to balance their energy budgets (Figure 5.21). A further spin-off of the elongate shape is

      1. Figure 5.21. A schematic representation of factors involved in the evolution of elongate body shape in weasels. Circles indicate primary consequences of evolving a long, thin body configuration; ellipses show secondary consequences; rectangles indicate phenotypic characteristics of weasels affected by evolution of this body shape. Unbroken arrows indicate selective pressures and dashed arrows show causal sequences. Changes proceed in the direction of the arrows as long as selection favors a more elongate shape. [From Brown and Lasiewski (1972). Copyright © 1972 by the Ecological Society of America.]

      the evolution of a pronounced sexual dimorphism in body size, which allows male and female weasels to exploit prey of different sizes and hence reduces competition between the sexes (related mustelids such as skunks and badgers do not have the marked sexual size dimorphism characteristic of weasels).

      Design Constraints

      Most biologists are acutely aware that possible evolutionary pathways are somehow constrained by basic body plans. Although natural selection has "invented," developed, and refined a truly amazing variety of adaptations,2 selection is clearly far from omnipotent. Wheels might be a desirable solution to certain environmental contingencies and yet they have not been evolved. Such "design constraints" are usually elusive and not easily demonstrable. Students of thermoregulation have often noted an apparent upper thermal limit of about 40°C for most of the earth's eukaryotic creatures (most plants, invertebrates, and vertebrates). This thermal "lid" has frequently been used as evidence for some extremely archaic and inflexible fundamental physiological process (perhaps an enzyme basic to life processes, such as a dehydrogenase, denatures). The major exceptions are certain heat-tolerant bacteria and blue-green algae, inhabitants of hot springs and oceanic volcanic vents. These prokaryotic organisms may well have arisen before the origin of the heat-sensitive metabolic pathway that seems to limit the eukaryotes.

      An example of such a physiological design constraint involves the thermal relationships of vertebrates, spanning classes from reptiles to mammals (Pianka 1985, 1986a). Detailed consideration of behavioral thermoregulation in lizards enables a fairly accurate prediction of the active body temperatures of mammalian homeotherms. A provocative biological "constant" can thus be identified that suggests a substantial degree of physiological inertia.

      An intriguing hypothesis for the evolution of homeothermy was offered by Hamilton (1973), who suggested that homeothermy is a by-product of advantages gained from maintaining maximum body temperatures in the face of such an innate physiological ceiling. Ecologically optimal temperatures need not coincide with physiological optima.

      Remember that not all homeotherms are endotherms; many ectotherms have attained a substantial degree of homeothermy by means of behavioral thermoregulation. Typically, such organisms actively select thermally suitable microhabitats, orient their bodies (or parts thereof) to control heat exchange, and/or shuttle between sun and shade as necessary to maintain a more-or-less constant internal body temperature.

      Thermoregulation in lizards is not nearly as simple as it might appear to be at first glance, but rather encompasses a wide diversity of very different thermoregulatory tactics among species ranging from ectothermic poikilothermy to and including ectothermic homeothermy. Even a casual observer quickly notices that various species of desert lizards differ markedly in their times and places of activity. Some are active early in the morning, but other species do not emerge until late morning or midday. Most geckos and pygopodids and some Australian skinks are nocturnal. Certain species are climbers, others subterranean, while still others are strictly surface dwellers. Among the latter, some tend to be found in open areas whereas others frequent the edges of vegetation. Thermal relations of active lizards vary widely among species and are profoundly influenced by their spatial and temporal patterns of activity. Body temperatures of some diurnal heliothermic species average 38°C or higher, whereas those of nocturnal thigmothermic species are typically in the mid-twenties, closely paralleling ambient air temperatures.

      Interesting interspecific differences also occur in the variance in body temperature as well as in the relationship between body temperatures and air temperatures. For example, among North American lizards, two arboreal species (Urosaurus graciosus and Sceloporus magister) display narrower variances in body temperature than do terrestrial species. Presumably, arboreal habits often facilitate efficient, economic, and rather precise thermoregulation. Climbing lizards have only to shift position slightly to be in the sun or shade or on a warmer or cooler substrate, and normally do not move through a diverse thermal environment. Moreover, arboreal lizards need not expend energy making long runs as do most ground dwellers, and thus climbing species do not raise their body temperatures metabolically to as great an extent as do terrestrial lizards.

      Such differences in temporal patterns of activity, the use of space, and body temperature relationships are hardly independent. Rather, they complexly constrain one another, sometimes in intricate and obscure ways. For example, thermal conditions associated with particular microhabitats change in characteristic ways in time; a choice basking site at one time of day becomes an inhospitable hot spot at another time. Perches of arboreal lizards receive full sun early and late in the day when ambient air temperatures tend to be low and basking is therefore desirable, but these same tree trunks are shady and cool during the heat of midday when heat-avoidance behavior becomes necessary. In contrast, the fraction of the ground's surface in the sun is low when shadows are long early and late, but reaches a maximum at midday.

      Terrestrial heliothermic lizards may thus experience a shortage of suitable basking sites early and late in the day; moreover, during the heat of the day, their movements through relatively extensive patches of open sun can be severely curtailed. Hence, ground-dwelling lizards encounter fundamentally different and more difficult thermal challenges than do climbing species.

      Radiation and conduction are the most important means of heat exchange for the majority of diurnal lizards, although the thermal background in which these processes occur is strongly influenced by prevailing air temperatures. Ambient air temperatures are critical to nocturnal lizards as well as to certain very cryptic diurnal species.

      In an analysis of the costs and benefits of lizard thermoregulatory strategies, Huey and Slatkin (1976) identified the slope of the regression of body temperature against ambient environmental temperature as a useful indicator (in this case, an inverse measure) of the degree of passiveness in regulation of body temperature. On such a plot of active body temperature versus ambient temperature, a slope of one indicates true poikilothermy or totally passive thermoconformity (a perfect correlation between air temperature and body temperature results), whereas a slope of zero reflects the other extreme of perfect thermoregulation. Lizards span this entire thermoregulation spectrum. Among active diurnal heliothermic species, regressions of body temperature on air temperature are fairly flat (for several species, including some quite small ones, slopes do not differ significantly from zero); among nocturnal species, slopes of similar plots are typically closer to unity. Various other species (nocturnal, diurnal, and crepuscular), particularly Australian ones, are intermediate, filling in this continuum of thermoregulatory tactics.

      A straight line can be represented as a single point in the coordinates of slope versus intercept; these two parameters are plotted for linear regressions of body temperatures on air temperatures among some 82 species of lizards in Figure 5.22.

      Each data point represents the least-squares linear regression of body temperature against air temperature for a given species of desert lizard. Interestingly enough, these data points fall on yet another, transcendent, straight line. The position of any particular species along this spectrum reflects a great deal about its complex activities in space and time. The line plotted in Figure 5.22 thus offers a potent linear dimension on which various species can be placed in attempts to formulate general schemes of lizard ecology (Pianka 1985, 1986a, 1993). Various other ecological parameters, including reproductive tactics, can be mapped on to this emergent spatial temporal axis.

      1. Figure 5.22. Each data point represents the least-squares linear regression of body temperature against air temperature for a given species of desert lizard (data given in Pianka 1986a). Sample sizes are usually substantial (average is 145). The horizontal axis represents the spectrum of thermoregulatory tactics ranging from active thermoregulators (slope of zero) to entirely passive thermoconformity (slope of one). Squares represent Australian skinks in the genus Ctenotus, which span much of the range of thermoregulatory tactics. The intriguing "intercept" of the intercepts (38.8°C) approximates the point of intersection of all 82 regression lines and presumably represents an innate design constraint imposed by lizard physiology and metabolism.

      The intriguing "intercept" of the intercepts (38.8°C) approximates the point of intersection of all 82 regression lines and presumably represents an innate design constraint imposed by lizard physiology and metabolism. It is presumably not an accident that this value also corresponds more or less to the body temperature of homeotherms, particularly mammals!

      Birds, which maintain slightly higher body temperatures than mammals (Hamilton 1973), descended from another reptilian stock, the archosaurs, represented today by the crocodilians. Would a comparable study of crocodilian thermoregulation yield a higher intercept of the intercepts? (This prediction could be doomed to failure by the mere fact that crocodilians are aquatic and very large -- yet they obviously thermoregulate when out of the water.) Although most insects are so small that convective heat exchange prevents them from attaining body temperatures much higher than that of ambient air, some, such as bumblebees and butterflies, do exhibit behavioral thermoregulation; would a plot for insects show more scatter and a different intercept?

      Selected References

      Limiting Factors and Tolerance Curves

      Ehrlich and Birch (1967); Errington (1956); Hairston, Smith, and Slobodkin (1960); Lack (1954, 1966); Liebig (1840); Murdoch (1966a); Odum (1959, 1963, 1971); Shelford (1913b); Terborgh (1971); Walter (1939).

      Resource Budgets and the Principle of Allocation

      Fitzpatrick (1973); Levins (1968); Randolph, Randolph, and Barlow (1975); Townsend and Calow (1981).

      Time, Matter, and Energy Budgets

      Emlen (1966); Gadgil and Bossert (1970); Gibb (1956, 1960); Grodzinski and Gorecki (1967); Hickman (1975); Pianka (1976b, 1981); C. Smith (1968); Townsend and Calow (1981); Willson (1972a); Wooten (1979); Zeuthen (1953); Whittaker (1975).

      Leaf Tactics

      Bailey and Sinnott (1916); Esser (1946a, b); Gentry (1969); Givnish (1979); Givnish and Vermeij (1976); Horn (1971, 1975a, b, 1976); Howland (1962); Janzen (1976); Miller (1979); Mooney et al. (1975); Orians and Solbrig (1977); Parkhurst and Loucks (1971); Ryder (1954); Stowe and Brown (1981); Vogel (1970); Wolf and Hainsworth (1971); Wolf et al. (1972).

      Foraging Tactics and Feeding Efficiency

      Bell (1991); Charnov (1973, 1976a, b); Charnov et al. (1976); Cody (1968); Emlen (1966, 1968a); Hespenhide (1971); Holling (1964); Huey and Pianka (1981); Kamil and Sargent (1982); MacArthur (1959, 1972); MacArthur and Pianka (1966); Morse (1971); Orians and Pearson (1977); Perry (1999); Perry and Pianka (1997); Pianka (1966b); Pulliam (1974); Rapport (1971); Royama (1970); Schoener (1969a, b, 1971); Schoener and Janzen (1968); Tullock (1970a); Uetz (1992); Werner and Hall (1974); Wolf et al. (1972).

      Physiological Ecology

      Bligh (1973); Cloudsley-Thompson (1971); Florey (1966); Folk (1974); Gates and Schmerl (1975); Gordon (1972); Guyton and Horrobin (1974); Hadley (1975); Hochachka and Somero (1973); Levitt (1972); Patten and Smith (1975); Prosser (1973); Schmidt-Nielsen (1964, 1975); Townsend and Calow (1981); Vernberg (1975); Vernberg and Vernberg (1974); Wieser (1973); Yousef, Horvath, and Bullard (1972).

      Physiological Optima and Tolerance Curves

      Brown and Feldmeth (1971); Huey and Stevenson (1979); Ruibal and Philibosian (1970); Schmidt-Nielsen (1975); Shelford (1913b).

      Energetics of Metabolism and Movement

      Bennett and Nagy (1977); Denny (1980); McNab (1963); Mohr (1940); Nagy (1987); Pearson (1948); Schmidt-Nielsen (1972, 1975); Schoener (1968b); Tucker (1975); Turner, Jennrich, and Weintraub (1969); Zeuthen (1953).

      Adaptation and Deterioration of Environment

      Fisher (1930, 1958a, b); Henderson (1913); Maynard Smith (1976); Odum (1965); Van Valen (1973).

      Heat Budgets and Thermal Ecology

      Bartholomew (1972); Bartlett and Gates (1967); Brown and Feldmeth (1971); Brown and Lasiewski (1972); Cowles and Bogert (1944); Dawson (1975); Gates (1962); Hamilton (1973); Huey and Slatkin (1976); Huey and Stevenson (1979); Patten and Smith (1975); Porter and Gates (1969); Porter et al. (1973); Ruibal (1961); Ruibal and Philibosian (1970); Schmidt-Nielsen (1964); Schmidt-Nielsen and Dawson (1964); Wittow (1970); Wieser (1973).

      Water Economy in Desert Organisms

      Caldwell (1979); Caldwell and Fernandez (1975); Cloudsley-Thompson (1971); Folk (1974); Gindell (1973); Hadley (1975); Main (1976); Schmidt-Nielsen (1964, 1975).

      Other Limiting Materials

      Feeny (1975); Gilbert (1972); Pauling (1970).

      Sensory Capacities and Environmental Cues

      Griffin (1958); Lloyd (1965, 1971, 1975); Machin and Lissmann (1960); Schmidt-Nielsen (1975).

      Adaptive Suites

      Bartholomew (1972); Brown and Lasiewski (1972); Frazzetta (1975); Pianka and Parker (1975b); Rosen (1967); Wilbur (1977).

      Design Constraints

      Brown and Feldmeth (1971); Duellman and Trueb (1986); Hamilton (1973); Huey and Pianka (1977); Huey and Slatkin (1976); LaBarbera (1983); Liem and Wake (1985); Pianka (1985, 1986a).


      1. The phenomenon of evolving as fast as possible just to maintain a given current level of adaptation in the face of a continually deteriorating environment has been called the "Red Queen" hypothesis by Van Valen (1973), after the famous character in Alice in Wonderland who ran as fast as she could just to stay where she was.

      2. Consider, for example, photosynthesis, the immune response, vision, flight, echolocation, and celestial navigation to name only a few of the more magnificent biotechnological innovations. Feathers remain one of the very best insulators (down-filled sleeping bags).


      6 Rules of Inheritance

      6| Rules of Inheritance

      Basic Mendelian Genetics

      Although a background in genetics is certainly not essential for appreciation of many populational and ecological phenomena, it is a useful aid for application to some such phenomena and is required for a full understanding of others. Precise rules of inheritance were actually unknown when Darwin (1859) developed the theory of natural selection, but they were formulated a short time afterward (Mendel 1865). Darwin accepted the hypothesis of inheritance in vogue at the time: blending inheritance. Under the blending inheritance hypothesis, genetic makeups of both parents are imagined to be blended in their progeny, and all offspring produced by sexual reproduction should be genetically intermediate between their parents; genetic variability is thus lost rapidly unless new variation is continually being produced. (Under blending inheritance and random mating, genetic variability is halved each generation.) Darwin was forced to postulate extremely high mutation rates to maintain the genetic variability observed in most organisms, and he was painfully aware of the inadequacy of knowledge on inheritance. Mendel's discovery of particulate inheritance represents one of the major empirical breakthroughs in biology.

      Mendel performed breeding experiments with different varieties of peas, paying close attention to a single trait at a time. He had two types that bred "true" for yellow and green peas, respectively. When a purebred green pea plant was crossed with a purebred yellow pea plant, all progeny, or individuals of the first filial generation (F1), had yellow peas. However, when these F1 plants were crossed with each other or self-fertilized, about one out of every four offspring in the second filial generation (F2) had green peas. Furthermore, only about one-third of the yellow F2 pea plants bred true; the other two-thirds, when self-fertilized, produced some offspring with green peas. All green pea plants bred true. Mendel proposed a very simple quantitative hypothesis to explain his results and performed many other breeding experiments on a variety of other traits that corroborated and confirmed his interpretations. Subsequent work has strengthened Mendel's hypothesis, although it has also led to certain modifications and improvements.

      Modern terminology for various aspects of Mendelian inheritance is as follows: (1) the “character” or “dose” controlling a particular trait is termed an allele; (2) its position on a chromosome (defined later) is termed its locus; (3) a single dose is the haploid condition, designated by n, whereas the double-dosed condition, designated by 2n, is diploid (polyploids, such as triploids and tetraploids, are designated with still higher numbers); (4) the set of alternative alleles that may occur at a given locus (there can be only two alleles in an individual, but there may be more than two in any given population) is termed a gene; (5) purebred diploid individuals with identical alleles are homozygotes, homozygous for the trait concerned; (6) individuals with two different alleles, such as the preceding F2 plants, are heterozygotes, heterozygous at that locus; (7) an allele that masks the expression of another allele is said to be dominant, whereas the one that is masked is recessive; (8) unlinked alleles separate, or segregate, from each other in the formation of gametes; (9) whenever heterozygotes or two individuals that are homozygous for different alleles mate, new combinations of alleles arise in the following generation by reassortment of the genetic material; (10) observable traits of an individual (e.g., yellow or green in the previous example) are aspects of its phenotype, which includes all observable characteristics of an organism; and (11) whether or not an organism breeds true is determined by its genotype, which is the sum total of all its genes.

      Occasionally, some organisms have pairs of alleles with incomplete dominance. In such cases, the phenotype of the heterozygote is intermediate between that of the two homozygotes; that is, phenotype accurately reflects genotype and vice versa. Presumably, alleles conferring advantages upon their bearers usually evolve dominance over time because such dominance ensures that a maximal number of the organism's progeny and descendants will benefit from possession of that allele. The apparent rarity of incomplete dominance is further evidence that dominance has evolved. So-called wild-type alleles, that is, those most prevalent in natural wild populations, are nearly always dominant over other alleles occurring at the same locus. Geneticists have developed numerous theories of the evolution of dominance, but the exact details of the process have not yet been completely resolved.

      Mendel postulated that each pea plant had a double dose of the "character" controlling pea color but that only a single dose was transmitted into each of its sexual cells, or gametes (pollen and ovules or sperm and eggs). Purebred plants, with identical doses, produced genetically identical single-dosed gametes; the above-mentioned F1 plants, on the other hand, with two different doses, produced equal numbers of the two kinds of gametes, half bearing the character for green and half that for yellow. In addition, Mendel proposed that yellow masked green whenever the two occurred together in double dose; hence all F1 plants had yellow peas, but when self-fertilized, produced some F2 progeny with green peas. All green pea plants, which had a double dose of green, always bred true.

      Cytological observations of appropriately prepared cell nuclei confirm Mendel's hypothesis beautifully (Figure 6.1). Microscopic examination of such cells reveals elongated dense bodies in cell nuclei; these are chromosomes, which contain actual genetic material, DNA. Nuclei of diploid cells, including the zygote (the fertilized ovule or egg) and the somatic (body) cells of most organisms, always contain an even number of chromosomes. (The exact number varies widely from species to species, with as few as two in certain arthropods to hundreds in some plants.) Pairs of distinctly similar homologous chromosomes are always present and often easily detected visually. However, gametes contain only half the number of chromosomes found in diploid cells, and, except in polyploids, none of them are homologous. Thus, haploid cells contain only one full set of different chromosomes and alleles, or one genome, whereas all diploid cells contain two. During the reduction division (meiosis) in which diploid gonadal cells give rise to haploid gametes, homologous chromosomes separate (Figure 6.1). Later, when male and female gametes fuse to form a diploid zygote that will develop into a new diploid organism, homologous chromosomes come together again. Hence, one genome in every diploid organism is of paternal origin while the other is of maternal ancestry. Because each member of a pair of homologous chromosomes separates from its homologue independently of other chromosome pairs, the previous generation's chromosomes are reassorted with each reduction division. Thus, the genetic material is regularly rearranged and mixed up by the dual processes of meiosis and the actual fusion of gametes (this has been termed the "Mendelian lottery").

      • Figure 6.1. Diagrammatic representation of the cytological events in cell nuclei showing how the two parental genomes are sorted and recombined in the next generation, or the F2. For simplicity, only one pair of chromosomes is shown and the complex events of the reduction division (meiosis) are omitted.

      Numerous different loci and allelic systems occur on each chromosome. Two different traits controlled by different alleles located on the same chromosome do not segregate truly independently but are statistically associated with or dissociated from one another. This is the phenomenon of linkage. During meiosis, homologous chromosomes can effectively exchange portions by means of crossovers; this process is referred to as recombination. Because the frequency of occurrence of crossovers between two loci increases with the distance between them on the chromosome, geneticists use crossover frequencies to map the effective distance between loci, as well as their positions relative to one another on chromosomes. By means of close linkage, whole blocks of statistically associated alleles can be passed on to progeny as a functionally integrated unit of coadapted alleles.

      Certain kinds of chromosomal rearrangements, such as inversions, may suppress crossovers. Indeed, a major advantage of chromosomes is that they enhance the degree to which clusters of genes can occur together. In many organisms a single pair of chromosomes, termed sex chromosomes, determine the sex of their bearer (the remaining chromosomes, which are not involved in sex determination, are autosomes). Typically one homologue of the sex chromosome pair is smaller. In the diploid state, an individual heterozygous for the sex chromosomes is heterogametic. In mammals, males are the heterogametic sex with an XY pair of sex chromosomes, whereas females are the homogametic sex with an XX pair. Because male-male matings are impossible, the homozygous genotype YY can never occur. In birds and some other organisms, the female is the heterogametic sex. In many reptiles, sex chromosomes do not exist and sex is determined by the environmental temperature at which eggs are incubated.

      Although natural selection actually operates on phenotypes of individuals (i.e., an organism's immediate fitness is determined by its total phenotype), the effectiveness of selection in changing the composition of a population depends on the heritability of phenotypic characteristics or the percentage of phenotypic variability attributable to genotype.

      Traits that are under strong selection usually display low heritability because the genetic component of phenotypic variability has been reduced by selection. Because nongenetic traits are not inherited, differential reproduction by different phenotypes stemming from such nontransmittable traits obviously cannot alter a population's gene pool. Different genotypes may often have fairly similar phenotypes and thus similar fitnesses. Selection may even favor alleles that are "good mixers" and work well with a wide variety of other genes to increase their bearer's fitness in various genetic backgrounds (Mayr 1959). Conversely, of course, identical genotypes can develop into rather different phenotypes under different environmental conditions.

      Genes that act to control the expression of other genes at different loci are called modifier or regulatory genes, whereas those that code for specific cell products are termed structural genes (some genes do not fit this dichotomy but may serve in both capacities). Although relatively little is known, geneticists imagine that an intricate hierarchy must exist leading from regulator genes to structural genes to proteins to other non-proteinaceous metabolic products to specific phenotypes. Moreover, complex interactions must occur among regulators as they do among proteins and other metabolites such as neurotransmitters and hormones.

      Humans and the great apes share many genes, including the familiar ABO blood groups. A detailed molecular comparison of human proteins with those of chimpanzees by three different techniques (sequencing, immunological distance, and electrophoresis) revealed nearly identical amino acid sequences in the vast majority of proteins (99 percent similarity, with concordant results at 44 loci), presumably the products of structural genes (King and Wilson 1975). Apparently, a relatively few genetic changes in major regulatory genes can have profound phenotypic effects without much difference at the level of proteins. Thus, relatively trivial genetic differences can lead to major phenotypic differences. The genetic similarity between humans and chimps is comparable to that of sibling species in insects and other mammals. Recent DNA hybridization studies have demonstrated 98.4 percent similarity between humans and chimpanzees (Sibley et al. 1990). Whereas humans are placed in the family Hominidae, chimps are placed with the great apes in the family Pongidae. However, phylogenies based on molecular similarities show that humans are embedded within the apes (Figure 6.2). Clearly, it is time to consider reclassification!

      • Figure 6.2. Phylogeny of primates based on DNA hybridization. [Adapted from Diamond (1991) after Sibley and Ahlquist.]

      Nature versus Nurture

      A widespread misconception is that any phenotypic trait can always be assigned to either one of two mutually exclusive categories: genetic or environmental. However, this dichotomy is not only oversimplified but can be rather misleading. Because natural selection acts only on heritable phenotypic traits, even environmentally flexible traits must usually have an underlying genetic basis. For example, when grown on dry plant foods, the Texas grasshoppers Syrbula and Chortophaga become brown, but when fed on moist grasses, these same insects develop green phenotypes -- this classic "environmentally induced" polymorphism is presumably highly adaptive since it produces background color-matching cryptic green grasshoppers when environments are green but brown ones in brown environments (Otte and Williams 1972). The capacity for developmental plasticity itself has almost surely evolved in response to the unpredictable environment these grasshoppers must face. If enough were known, much environmentally determined phenotypic variation would presumably have a somewhat comparable basis in natural selection. Thus, truly nongenetic traits are unimportant and uninteresting simply because they cannot evolve and do not affect fitness. Indeed, for purposes of evolutionary ecology, virtually all traits can be considered as being subject to natural selection (those that are not cannot easily persist and have little or no evolutionary significance). The complete set of different phenotypes that can be produced by a given genotype across a range of environments is called its reaction norm.

      Selfish Genes

      Certain alleles do not obey the Mendelian lottery of meiosis and recombination: instead these "outlaw genes" obtain disproportionate representation in a carrier's gametes at the expense of alternate alleles on homologous chromosomes. An example of such a selfish gene is the "segregation distortion" allele in the fruit fly Drosophila. Males heterozygous for this sex-linked trait produce sperm of which some 95 percent carry the allele (rather than the expected 50 percent). This process is known as meiotic drive. Why don't more genes behave in this manner? Very probably the intense contest for representation in the gametes has itself ended in a stalemate, yielding the traditional Mendelian ratios (viewed in this way, segregation itself is clearly a product of natural selection).

      Advocates of the "selfish gene" hypothesis (Dawkins 1982, 1989) argue somewhat as follows. Barring mutations, genes are perfect replicators, always making exact copies of themselves. However, phenotypes of individual organisms are transmitted to their offspring only imperfectly, at least in sexually reproducing species. Individuals can thus be viewed as mere "vehicles" for the genes that they carry.

      Except for viruses, genes usually do not exist in isolation but must occur together in large clusters. A sort of "packaging problem" arises, with the number of copies left by any given allele depending upon the particular combination of other genes, or "genetic background," in which the allele concerned actually occurs. (Actually, of course, selection "sees" the phenotypic expression resulting from interactions among all alleles in a particular genetic constellation in a given environment.) Also, genes clearly cannot replicate themselves except by means of successful reproduction of the entire organism. Hence selection must usually favor genes that work together to enhance an individual's ability to perpetuate them, thus increasing its fitness. A "parliment of genes" acts to govern the phenotype. A mutant gene that prevented its bearer from reproducing would be short-lived indeed! Likewise, mutations that reduce the reproductive success of individuals will normally1 be disfavored by natural selection. Viruses are indeed selfish genes, as their interests need not coincide with those of their hosts.

      Population Genetics

      Each generation, sexually reproducing organisms mix their genetic materials. Such shared genetic material is called a gene pool, and all the organisms contributing to a gene pool are collectively termed a Mendelian population. Gene pools have continuity through time, even as individuals are added and removed by births and deaths. One of the most fundamental concepts of population genetics is the notion of gene frequency. An allele's frequency in the haploid gene pool, or its proportional representation, is traditionally represented by the symbol p or q. Changes in allele frequencies in a gene pool in time constitute evolution. An individual's ability to contribute its own genes to the gene pool represents that individual's fitness.

      Equilibrium frequencies of various diploid genotypes that emerge in a given gene pool, given random mating and no evolution, can be calculated from the haploidgene frequencies using the binomial2 expansion (also known as the Hardy-Weinberg equilibrium):

      1 = (p + q)(p + q) = p2 + 2pq + q2

      If p is the frequency of allele A1 and q the frequency of allele A2, the expected equilibrium frequencies of the three diploid genotypes A1/A1, A1/A2, and A2/A2 are given by the three terms at the right: p2 , 2pq, and q2, respectively.

      With random mating and no evolution, allele frequencies remain unchanged from generation to generation. The equilibrium frequency of heterozygotes reaches its maximum of 50 percent when the two alleles are equally represented (p = q = 0.5;
      Figure 6.3).

      • Figure 6.3.Frequencies of the three diploid genotypes for various gene frequencies in a two-allele system in Hardy-Weinberg equilibrium.

      Population geneticists have relaxed these limiting assumptions and elaborated and extended these equations to model various phenomena such as random genetic drift, gene flow, nonrandom mating, and frequency-dependent selection. Genotypes can also be assigned fixed relative fitnesses; when the heterozygote is fitter than either homozygote, both alleles are maintained indefinitely, even if one or both of the homozygotes is actually lethal! This widespread and important phenomenon is known as heterozygote advantage or heterosis. Such a reduction in fitness due to genetic segregation is termed genetic load. If one homozygote enjoys the highest fitness, it is favored by natural selection until that locus becomes "fixed" with an allele frequency of 1.0. Ultimately, maintenance of genetic variation depends on the precise rules coupling allele frequencies to genotype frequencies.

      Maintenance of Variability

      The fundamental source of variation between individuals is sexual reproduction; reassortment and recombination of genes in each generation ensures that new genotypes will arise regularly in any population with genetic variability. In most higher organisms, no two individuals are genetically identical (except identical twins and progeny produced asexually). Population biologists are interested in understanding factors that create and maintain genetic variability in natural populations. When a population is reduced to a very small size, it must go through a genetic bottleneck which can greatly reduce genetic variability. Numerous genetic mechanisms, including linkage and heterosis, produce genetic variability both within and between populations.

      At the outset, we must distinguish phenotypic from genotypic variation. The phenotypic component of variability is the total observable variability; the genotypic component is that with a genetic basis. It is usually difficult to distinguish genetically induced variation from environmentally induced variation. However, by growing clones of genetically identical individuals (i.e., with the same genotype) under differing environmental conditions, biologists have been able to determine how much interindividual variation is due to the developmental plasticity of a particular genotype in different environments. Pedigree studies show that approximately half the phenotypic variation in height observed in human populations has a genetic basis and the remaining variation is environmentally induced. The proportion of phenotypic variation that has a genetic basis is known as heritability. Because natural selection can act only on heritable traits, many phenotypic variants may have little direct selective value. The degree of developmental flexibility of a given phenotypic trait strongly influences an organism's fitness; such a trait is said to be canalized when the same phenotypic character is produced in a wide range of genetic and environmental backgrounds. Presumably, some genes are rather strongly canalized, such as those that produce "wild-type" individuals, whereas others are less determinant, allowing individuals to adapt and regulate via developmental plasticity. Such environmentally induced phenotypic varieties are common in plants, but they are less common among animals, probably because mobile organisms can easily select an appropriate environment. Presumably, it is selectively advantageous for certain genetically induced traits to be under tight control, whereas others increase individual fitness by allowing some flexibility of response to differing environmental influences.

      Genotypic and phenotypic variation between individuals, in itself, is probably seldom selected for directly. But it may often arise and be maintained in a number of more or less indirect ways. Especially important are changing environments; in a temporally varying environment, selective pressures vary from time to time and the phenotype of highest fitness is always changing. There is inevitably some lag in response to selection, and organisms adapted to tolerate a wide range of conditions are frequently at an advantage. (Heterozygotes may often be better able to perform under a wider range of conditions than homozygotes.) Indeed, in unpredictably changing environments, reproductive success may usually be maximized by the production of offspring with a broad spectrum of phenotypes (which may well be the major advantage of sexual reproduction).

      Similar considerations apply to spatially varying environments because phenotypes best able to exploit various "patches" usually differ. On a broader geographic level, differences from one habitat to the next presumably often result in different selective milieus and therefore in different gene pools adapted to local conditions. Gene flow between and among such divergent populations can result in substantial amounts of genetic variability, even at a single spot.

      Competition among members of a population for preferred resources may often confer a relative advantage on variant individuals that are better able to exploit marginal resources; thus, competition within a population can directly favor an increase in its variability. By virtue of such variation between individuals, the population exploits a broader spectrum of resources more effectively and has a larger populational "niche breadth"; the "between phenotype" component of niche breadth is great (Roughgarden 1972).

      Because such increased phenotypic variability between individuals promotes a broader populational niche, this has been termed the "niche-variation hypothesis" (Soulé and Stewart 1970). Similarly, environments with low availability of resources usually require that individuals exploiting them make use of a wide variety of available resources; in this case, however, because each individual must possess a broad niche, variation between individuals is not great (i.e., the "between-phenotype" component of niche breadth is slight, whereas the "within-phenotype" component is great).

      One further way in which variability can be advantageous involves coevolutionary interactions between individuals belonging to different species, especially interspecific competition and predation. Fisher (l958b) likened such interspecific interactions and coevolution to a giant evolutionary game in which moves alternate with countermoves. It may well be more difficult to evolve against an unpredictable and variable polymorphic species than against a better standardized and more predictable monomorphic species. A possible example may be foraging birds developing a "search image" for prey items commonly encountered, often bypassing other less abundant kinds of suitable prey.

      Units of Selection

      Classical Darwinian natural selection acts only on heritable phenotypic traits of individuals. As discussed earlier, selfish genes are also known to exist. Can selection operate on entire groups of individuals such as families, colonies, populations, species, communities, and ecosystems? To what extent is the individual a natural "unit" of selection? How are conflicts between suborganismal, organismal, and superorganismal levels of selection resolved? These questions are often discussed both by geneticists and by ecologists, but there is no clear consensus as to correct answers.

      Many behavioral and ecological attributes can be interpreted as having evolved for the benefit of the group rather than the individual. As an example of such group selection, consider the assertion that "mockingbirds lay fewer eggs during a drought year because competition for limited food supplies would be detrimental to the species." Such statements have a fatal flaw: "Cheaters" that laid as many eggs as possible would reap a higher reproductive success than individuals that voluntarily decreased their clutch size for the "benefit of the species." The same phenomenon can be interpreted more plausibly in terms of classical Darwinian selection at the level of the individual. During droughts, parental birds cannot bring as many insects to their nest and therefore cannot feed and fledge as many chicks as they can when food supplies are more ample. Birds can actually leave more surviving offspring to breed in the next generation by laying fewer eggs. Most evolutionary biologists now dismiss the preceding sort of "naive" group selection as untenable.

      In the last two decades, thinking about group selection has achieved considerably greater sophistication, although it remains speculative. Two distinct types of selection at the level of groups emerge from these mathematical arguments. For "extinction" group selection to oppose natural selection at the level of the individual, isolated selfish subgroups must go extinct faster than selfishness arises within altruistic subgroups and most newly founded isolates must be altruistic. "Graded" group selection requires that distinct subpopulations contribute differentially to reproduction in a bigger population at large. In essence, entire groups must possess differential rates of survivorship or reproduction (i.e., differential fitness).

      A major consideration is the extent to which an individual's own best interests are in conflict with those of the group to which it belongs. Ultimately, the frequency of occurrence of socially advantageous behaviors depends largely on the precise form of the trade-offs between group benefit(s) versus individual cost(s). Any individual sacrificing its own reproductive success for the benefit of a group is obviously at a selective disadvantage (within that group) to any other individual not making such a sacrifice. Classical Darwinian selection will always favor individuals that maximize their own reproductive success. Clearly, the course of selection acting within groups cannot be altered by selection operating between groups. Group selection requires very restricted conditions.

      Williams (1966a) reemphasized, restated, and expanded the argument against naive group selection, pointing out that classical Darwinian selection at the level of the individual is adequate to explain most putatively "group-selected" attributes of populations and species, such as those suggested by Wynne-Edwards (1962) and Dunbar (1960, 1968, 1972). Williams reminds us that group selection has more conditions and is therefore a more onerous process than classical natural selection; furthermore, he urges that it be invoked only after the simpler explanation has clearly failed. Although group selection is certainly possible, it probably would not actually oppose natural selection at the individual level except under most unusual circumstances. A special form of selection at the level of the individual, kin selection, may frequently be the mechanism behind many phenomena interpreted as evidence for group selection. We will return to this issue from time to time in later chapters.

      Genetic Engineering

      Modern molecular biotechnological tools,3 such as restriction enzymes and gene splicing, now enable geneticists to transfer particular genes from one organism to another. For example, the firefly gene for luciferase has been successfully transferred to tobacco, resulting in transgenic bioluminescent plants. Human insulin and growth hormones are now routinely produced in chemostats of E. coli bacteria that have had human genes spliced into their genomes. Some researchers have even proposed using such transgenic bacteria as live vaccines (the genetically altered bacteria would live within humans and would confer resistance to particular diseases such as hepatitis). Such recombinant DNA technology has also enabled us to produce useful new life forms such as pollutant-eating bacteria that can help us to clean up what's left of our environment. Research is in progress to transfer nitrogen-fixing genes into crop plants.

      There are legitimate concerns, however, about the safety of research on such man-made transgenic organisms, particularly the possibility of accidental release of virulent strains that might attack humans. Such concerns have been addressed by implementation of strict containment procedures for recombinant DNA products, as well as by selecting and creating host organisms for foreign DNA that are incapable of surviving outside the laboratory.

      Obviously, genetically engineered organisms must eventually be designed for release into nature (indeed, genetically engineered tomatoes are now being grown commercially). Another concern is that genetically engineered organisms could have adverse effects on other species in natural ecosystems. We already have enough natural pests and certainly don't want to make any new ones!

      Unfortunately, we still know far too little to engineer ecological systems intelligently (obviously genetic engineers should work hand in hand with ecological engineers). Still another problem is the human tendency to allow short-term financial returns to override long-term prospects.

      Selected References

      Basic Mendelian Genetics

      Darlington and Mather (1949); Darwin (1859); Ehrlich and Holm (1963); Fisher (1930); Ford (1931, 1964); King and Wilson (1975); Maynard Smith (1958); Mayr (1959); Mendel (1865); Mettler and Gregg (1969); Sheppard (1959).

      Nature versus Nurture

      Bradshaw (1965); Clausen, Keck, and Hiesey (1948); Greene (1989); Otte and Williams (1972); Quinn (1987); Via et al. (1995)

      Selfish Genes

      Alexander and Borgia (1978); Dawkins (1982, 1989); Hamilton (1967); Leigh (1977); Orgel and Crick (1980).

      Population Genetics

      Crow (1986); Crow and Kimura (1970); Falconer (1981); Fisher (1930, 1958a); Ginzburg and Golenberg (1985); Haldane (1932, 1941, 1964); Hedrick (1983); Mayr (1959); Mettler and Gregg (1969); Wright (1931, 1968, 1969, 1977, 1978).

      Maintenance of Variability

      Ehrlich and Raven (1969); Fisher (l958b); Mettler and Gregg (1969); Roughgarden (1972); Somero (1969); Soulé and Stewart (1970); Van Valen (1965); Wilson and Bossert (1971).

      Units of Selection

      Alexander and Borgia (1978); Boorman and Levitt (1972, 1973); Brown (1966); Cole (1954b); Darlington (1971); Darnell (1970); Dawkins (1976, 1982); Dunbar (1960, 1968, 1972); Emerson (1960); Emlen (1973); Eshel (1972); Fisher (l958a); Gilpin (1975a); Leigh (1977); Levins (1970, 1975); Lewontin (1970); Maynard Smith (1964); Sober and Wilson (1998); Uyenoyama (1979); Van Valen (1971); Wade (1976, 1977, 1978); Wiens (1966); Williams (1966a, 1971); D. S. Wilson (1975, 1980, 1983); E. O. Wilson (1973, 1976); Wright (1931); Wynne-Edwards (1962, 1964, 1965a, b).

      Genetic Engineering

      Baba et al. (1992); Cockburn (1991); Tiedje et al (1989); Simonsen and Levin (1988).


      1. The qualifiers "usually" and "normally" in the above sentences are necessary because other copies of the genes concerned, identical by descent, occur in the bodies of related individuals (the important phenomenon of kin selection is considered later).

      2. With only two alleles, q = 1 - p. For three alleles, the appropriate equation is a trinomial, with p + q + r = 1, and so on.

      3. Other techniques, such as polymerase chain reaction (PCR) amplification of DNA segments, DNA sequencing, and DNA fingerprinting hold great promise as tools that will allow informative evolutionary studies.

       


      7 Evolution and Natural Selection

      7| Evolution and Natural Selection

      Agents of Evolution

      Evolution occurs whenever gene frequencies in a population change in time. Individuals do not evolve, but populations do. In addition to natural selection, there are several other agents of evolution, including genetic drift, gene flow, meiotic drive, and mutation. Genetic drift operates by random sampling bias and is confined to relatively small populations. Gene flow occurs by migration movements of plants and animals among and between populations with different gene frequencies. Meiotic drive, or segregation distortion, was briefly considered in Chapter 6. Forward and backward rates of mutation are seldom the same, and the resulting mutation pressure can cause gene frequencies to change. Of these five different agents of evolution, only natural selection is directed in that it results in conformity between organisms and their environments.

      Types of Natural Selection

      Under stable conditions, intermediates in a population typically leave more descendants, on the average, than do the extremes. We say that they are more "fit." An individual's "fitness" is measured by the proportion of its genes left in the population gene pool. Selection of this sort, which continually crops the extremes and tends to hold constant the intermediate or average phenotype, is termed stabilizing selection (Figure 7.1a). In a stable environment, genetic recombination increases the population's variance each generation, whereas stabilizing selection reduces it to approximately what it was in the previous generation. However, in a changing environment, average individuals (modal phenotypes) may not be the most fit members of the population. Under such a situation, directional selection occurs and the population mean shifts toward a new phenotype (Figure 7.1b) that is better adapted to the altered environment. Eventually, of course, unless the environment continues to change, an equilibrium is reached in which the population is readjusted to the new environment, whereupon stabilizing selection resumes.

      A third type of selection, disruptive selection, takes place when two or more phenotypes with high fitnesses are separated by intermediate phenotypes of lower fitness (Figure 7.1c). This usually occurs in distinctly heterogeneous environments with a discrete number of different "patches." Disruptive selection is one mechanism that produces and maintains polymorphisms, such as the green-brown color polymorphisms of many insects. For instance, some butterflies (commonly called "leaf butterflies") mimic leaves; one population may contain both green and brown animals, with the former matching living leaves and the latter dead ones. Through appropriate behavior and selection of matching resting sites, each color morph enjoys a relatively high fitness; in contrast, a butterfly intermediate between green and brown would presumably match its surroundings less well and thus have a considerably lower fitness.

      1. Figure 7.1. Graphic portrayal of the three types of selection. (a) Stabilizing selection, which occurs in constant environments, holds the modal phenotype constant. (b) Directional selection takes place in a changed environment and causes a shift in the modal phenotype. (c) Disruptive selection, with two or more modal phenotypes, occurs in patchy environments with more than one discrete phase.

      Another important type of selection is known as frequency-dependent selection -- this occurs when the fitness of a particular phenotypic trait varies with its frequency in the population. Negative frequency-dependent selection promotes genetic variability. An example would be a bird forming a search image for an abundant prey type, but switching to an alternate prey type when the abundance of the first type is reduced. Such predator switching behaviors favor the rarer prey type which can then increase in abundance until a flip-flop occurs and the predator resumes eating the first prey type again.

      Both disruptive selection and frequency-dependent selection can act to help maintain genetic polymorphisms. Other types of selection to be considered in subsequent chapters include age-specific selection, density-dependent selection, density-independent selection, kin selection, and sexual selection.

      Ecological Genetics

      The European land snail, Cepaea nemoralis, is polymorphic for shell color, with three phases: brown, pink, and yellow. This polymorphism is genetic, based on a three-allele system, with each of the six diploid genotypes varying in color between the endpoints of brown and yellow. In England, a major predator of these snails is the song thrush Turdus ericetorum. These birds break open snail shells on stones ("thrush anvils"). Proportions of shells accumulated at these anvils usually differ from those in the population at large, thereby reflecting the relative intensity of thrush predation on the various snail morphs (Figure 7.2).

      1. Figure 7.2. Percentages of yellow snails taken by thrushes versus those in the population at large, showing differential predation in time. [From Shepard (1951).]

      During April, available backgrounds in the woods are largely brown; conditions become progressively greener during May. The percentage of yellow shells (with the animal inside, yellow shells take on a greenish hue) found at thrush anvils is higher than in the population at large in April, but lower than in the population in late May (Figure 7.2), indicating differential predation by thrushes. Thrushes form search images for common Cepaea morphs, resulting in negative frequency-dependent selection (Harvey et al. 1975) favoring rare morphs. Thrush predation may well help to maintain the polymorphism in shell color since the brown and pink morphs have a fitness advantage early in the season while yellow snails are at an advantage later.

      Allopatric and Sympatric Speciation

      How do new species arise? How can one set of interbreeding populations break into two? There are two distinct modes of speciation, the process by which new species arise. Allopatric speciation or geographic speciation occurs in different areas slowly over thousands of years. When the geographic range of a species is broken into two, sets of populations are isolated and gene exchange is prevented, thus allowing such populations to diverge if they are subjected to different selection pressures (this may usually occur when different local conditions require divergent adaptations).

      Barriers that can cause such events to occur include glaciers, mountain ranges, oceanic straits and isthmuses, as well as habitat changes caused by long-term shifts in climate. For example, during the pluvial glacial periods in the recent past (about 10,000 years ago), Australia was considerably wetter and an uninterrupted belt of lush mesic forested habitat extended from east to west across the southern third of the continent. Species of birds, frogs, lizards, and other animals had geographic ranges coincident with this contiguous belt of habitat. With the retreat of glaciers and the advent of interglacial conditions (also called interpluvials), an extensive arid area developed in the center of the continent and spread to the south coast. Wetter habitats survive today in the southeast and southwest, but these areas are now separated by a vast arid zone that includes the Nullarbor plain. Closely related species pairs of birds, frogs, and lizards now occur in these southeastern and southwestern refugia.

      Due to the lack of gene flow, geographically isolated populations of a species are free to adapt to local conditions. Following an extensive period of experiencing different selective pressures in isolation, the two subsets of what was formerly a single species may have diverged greatly from one another. Whether or not speciation has actually occurred may be put to the test at some later point in time if the two subsets come back together again in sympatry (this might happen, for example, with the advent of another ice age). If the two incipient "species" interbreed and hybridize extensively, the two subsets merge together into one species again in a process known as introgression. However, if the two incipient species are different enough that hybrid individuals suffer reduced fitness, natural selection can favor the evolution of reproductive isolating mechanisms (next section) that prevent introgression from occurring and reinforces the differences between the two new species.

      Speciation can also occur more or less instantly, without geographic isolation, and in several different ways. Many species of plants appear to have arisen by the hybridization of two parental species and subsequent chromosome doubling. This process, known as allotetraploidy, occurs as follows: let the two parent species' diploid genomes be represented as AA BB CC and XX YY ZZ, respectively (A, B, C, X, Y, and Z could represent chromosomes). Because the hybrid's genotype is ABCXYZ, chromosomes have no homologues to pair with in meiosis and the hybrid is sterile. However, since the hybrid has attributes of both parental species, it might well be superior to both of them in intermediate habitats (for example, if one parent species is cold-adapted and the other is hot-adapted, the hybrid could outperform both under warm conditions). Such hybrids can survive and even increase in numbers by clonal or vegetative reproduction. Eventually endoduplication or a non-disjunction event during meiosis converts the hybrid's genome from ABCXYZ to AA BB CC XX YY ZZ, restoring fertility (chromosomes can now pair and the hybrid can therefore produce viable gametes). Species that arose via such biparental origin and consequent chromosome doubling are often phenotypically intermediate between their parental species and are often found under intermediate environmental conditions.

      Another example of sympatric speciation occurs in tephritid fruit flies (Tephritidae). In most tephritids, males and females are attracted to the same host, which serves as a rendezvous for courtship and mating. Genetic variation in host choice can therefore affect mate choice. Such is the case in Rhagoletis pomonella, which originally oviposited on the fruits of hawthorn. This fly established new host races sypatrically on other members of the plant family Rosaceae, including apples, cherries and roses introduced to North America from Europe. Genetic studies of the apple and Haw populations indicate that they now maintain genetically distinct populations in sympatry (Feder et al. 1988). The sympatric shift from haws to apple involved genetic divergence in genes responsible for host recognition, the timing of adult emergence and differential host related survival (Feder 1998). Adults of the apple and haw populations are now adapted to and mate on different hosts. Thus, the apple population actually represents a newly evolved species (Bush and Smith 1998).

      Reproductive Isolating Mechanisms

      Many closely related species that do not interbreed in nature have been hybridized in captivity. For example, all pairs of species of falcons (Falco) can produce viable progeny. Mechanisms that prevent interbreeding between species, known as reproductive isolating mechanisms, have frequently evolved.

      Isolating mechanisms can be prezygotic or postzygotic, depending upon whether or not fertilization actually occurs. Hybrid sterility is an example of a postzygotic isolating mechanism. Prezygotic behavioral isolating mechanisms can involve courtship behavior, pheromones, vocalizations, and/or color patterns that promote species recognition and prevent mismatings from occurring between species. As an example, female fireflies (actually beetles) respond only to the flashing pattern and flight paths of males belonging to their own species (Lloyd 1986).

      Galápagos Finches

      The Galápagos Islands, an archipelago of relatively small and remote, deep water, volcanic islands located about a thousand kilometers west of the Ecuadorian coast (Figure 7.3), support a remarkable group of finches that nicely illustrate a number of evolutionary and ecological principles. These birds dominate the avifauna of the Galápagos. Only 26 species of land birds occurred in the archipelago naturally (i.e., before human introductions), and 13 of these are finches (the islands also support four species of mockingbirds, two flycatchers, two owls, a hawk, a dove, a cuckoo, a warbler, a martin, and a rail).

      1. Figure 7.3. Two maps of the main islands in the Galápagos Archipelago. [Inset from Lack (1947). Larger map from Bowman (1961), originally published by the University of California Press. Reprinted by permission of the Regents of the University of California.]

      This archipelago (16 major islands and a sprinkling of tiny islets) was formed from volcanic eruptions of the ocean floor about 3 to 5 million years ago; thus originally, there were no organisms on the islands, and their entire biota has been derived from mainland species. Because of their remoteness, relatively few different plant and animal stocks have been able to colonize the Galápagos. (However, the position of these islands on the equator presumably makes them particularly vulnerable to invasions from rafts and floating islands carried out to sea in the equatorial current.)

      The 13 species of finches are thought to have evolved from a single mainland finch ancestor that reached the islands long ago. (The birds are similar enough to each other that they are classified as a distinct subfamily of finches, endemic to the Galápagos and Cocos islands.) Archipelagos are ideal for geographic isolation and speciation, especially in land birds such as finches that do not readily fly across wide stretches of water. In such effectively isolated populations, different selective pressures on different islands lead to divergent evolution and adaptations; moreover, occasional interchanges between islands result in heightened interspecific competition, which promotes niche diversification. Drepanid honey creepers underwent a similar adaptive radiation in the Hawaiian islands.

      The necessity of geographic isolation and subsequent inter-island colonization for the occurrence of speciation and adaptive radiation is nicely demonstrated by the Cocos Island finch, Pinaroloxias inornata. Cocos Island is a remote and solitary island several hundred kilometers north of the Galápagos and about the same distance from the mainland (Figure 7.3, inset). Cocos Island supports only one species of finch. There has been no opportunity for geographic isolation or reduced gene flow, and the Pinaroloxias gene pool has never split. As might be expected, this finch is a generalist (Smith and Sweatman 1976), probably with a high degree of phenotypic variability between individuals.

      Adaptive radiation of these finches in the Galápagos has produced five different genera that differ in where they forage, how they forage, and what they eat (Figure 7.4). So-called ground finches (Geospiza) include six ground-foraging species with broad beaks that eat seeds of different sizes and types as well as flowers of Opuntia cactus. The genus Camarhynchus, termed tree finches because they forage in trees, contains three insectivorous species with generally somewhat narrower beaks; another species (Platyspiza crassirostris) is a vegetarian. Another species, the "woodpecker finch," Cactospiza pallida, uses sticks and cactus spines to probe cracks and crevices for insects, much like a woodpecker uses its long pointed tongue. One very distinctive and monotypic genus, the so-called warbler finch, Certhidea olivacea, is insectivorous and occurs on almost all the islets and islands in the archipelago and breeds throughout most habitats.

      1. Figure 7.4. Phylogeny of the Galápagos finches. [Phylogenetic tree after Lack (1947); head sketches from Grant (1986) after Swarth and Bowman.]
      2. From three to ten species of finches occur on any given island in various combinations, although some species have now gone extinct on some islands. Beak lengths and depths are highly variable from island to island (Figure 7.5), presumably reflecting different environmental conditions among islands, including interspecific competitive pressures. Figure 7.5 illustrates character displacement in beak depths; the tiny islets of Daphne and Los Hermanos support only one member of a pair of very similar species, either Geospiza fuliginosa or G. fortis, respectively. On these two small islands, beaks of both species are more similar in beak size than they are on a larger island where the two species occur together in sympatry (Santa Cruz -- upper part of Figure 7.5), where beak depths are completely non-overlapping, with G. fuliginosa having a small beak (about 6 to 8 mm deep) and G. fortis a larger beak (about 9 to 15 mm deep). Of course, beak dimensions determine in large part the size of the food items the birds eat, but beaks are also used in species recognition. Beak depths in contemporary finch populations have evolved over the past two decades with changes in seed availability arising from varying climatic conditions: during drought years, large hard seeds become relatively more available favoring finch individuals with deeper beaks (these have more power and can handle and crush large hard seeds more efficiently).

        1. Figure 7.5. Histograms of the beak depths of several species of finches, genus Geospiza, on different islands. In allopatry on the islets of Daphne and Los Hermanos, G. fortis and G. fuliginosa are more similar in beak size than they are in sympatry on Santa Cruz, where their beak depths are entirely non-overlapping. [Adapted from Schluter et al. (1985).]

        Larger islands in the Galápagos Archipelago contain a greater variety of habitat types and, as a result, support more species of finches than do smaller islands. Moreover, the total number of finch species decreases with "average isolation," or the mean distance from other islands, whereas the number of endemic species increases with isolation.

      Selected References

      Agents of Evolution

      Fisher (1930, 1958a, b); Ford (1964); Haldane (1932); Maynard Smith (1958); Wilson and Bossert (1971); Wright (1931).

      Types of Natural Selection

      Kettlewell (1956, 1958); Mettler and Gregg (1969); Wilson and Bossert (1971).

      Ecological Genetics

      Cockburn (1991); Dobzhansky (1970); Ford (1964); Harvey et al. (1975); Kettlewell (1956, 1958).

      Allopatric and Sympatric Speciation

      Bush (1975, 1976); Bush and Smith (1998); Feder et al. (1988, 1998); Futuyma (1987); Mayr (1963); Otte and Endler (1989); Patterson (1982); Prokopy et al. (1982).

      Galápagos Finches

      Abbott et al. (1977); Bowman (1961); Cox (1995); Grant (1981, 1986); Hamilton and Rubinoff (1963, 1967); Lack (1947); Petren et al. (1999); Schluter (1988); Schluter et al. (1985); Weiner (1994).