Chapter 9 Population Distribution and Abundance

Standing on a headland in central California over looking the Pacific Ocean, a small group of students spots a group of gray whales, Eschrichtilus robustus, rising to the surface and spouting water as they swim northward (fig.9.la). The whales are rounding the point of land their way to feeding grounds off the coasts of Alaska and Siberia. This particular group is made up of females and calves. The calves were born during the previous winter along the coast of Baja California, the gray whale's wintering grounds. Over the course of the spring, the entire population of over 20,000 gray whales will round this same headland on their way to the Bering and Chukchi Seas.Gray whales travel from one end of their range to the other twice each year, a distance of about 18,000 km. Home to the gray whale encompasses a swath of seacoast extending from southern Baja California to the coast of northeast Asia.

the grove of pine trees on the headland where the students stand gazing at the whales is winter home to another long distance traveler：monarch butterflies，Danaus plexippus(fig.9.b)．The lazy flying of the bright orange and black monarch butterflies gives no hint of their capacity to migrate．Some of the butterflies flew to the grove of pines the previous autumn from as far away as the Rocky Mountains of southern Canada．As the students watch the whales．the male monarch butterflies pursue and mate with the female monarch butterflies．After mating．The males die, while the females begin a migration that leads inland and north．The females stop to lay eggs on any milkweeds they encounter along the way and eventually die; however their off spring continue the migration．the monarch caterpillars grow quickly on their diet of milkweed and then transform to pupae contained within cocoons．The monarch butterflies that emerge from the cocoons mate and，like the previous generation，fly northward and inland．By moving farther north and inland each generation, some of the monarch butterflies eventually reach the Rocky Mountains of southern Canada．far from where their ancestors fluttered around the group of students on the pine-covered coastal headland．

Figure 9.1 (a)During their annual migration，the entire population of gray whales migrates from subtropical waters Baja California to the Arctic and back again. (b)Some of the monarch butterflies roosting on these trees flew thousands if kilometers from the Rocky Mountains to reach their winter roost．In contrast, the entire natural population of the Monterey pine, Pinus radiata,is restricted to five small areas along the coast of California.

Then as the autumn days grow shorter．the monarch butterflies begin their long flight back to the coastal grove of pines．This autumn generation．which numbers in the millions．Flies southwest to their wintering grounds on the coast of central and southern California．Some of them might fly over 3.000 km．The monarch butterflies that survive the trip to the pine grove overwinter．hanging from particular roost trees in the thousands．They mate in the following spring and start the cycle all over again.

Gray whales and monarch butterflies, as diffluent as they may appear, lead parallel lives．The Monterey pines，Pinus radiata, covering the headland where the monarch butterflies overwinter and by which the gray whales pass twice each year are quite different．The Monterey pine population does not migrate each generation and has a highly restricted distribution.The current natural range of the Monterey pine is 1imited to a few sites on the coast of central and northern California and to two islands 0ff the coast of western Mexico．These scattered populations are the remnants of a large continuous population that extended for over 800 km along the California coast during the cooler climate of the last glacial period．

With these three examples．we begin to consider the ecology of populations．Ecologists usually define a population as a group of individuals of a single species inhabiting a specific area．A population of plants or animals might occupy a mountaintop．a river basin，a coastal marsh，or an island．All areas defined by natural boundaries．Just as often, the populations studied by biologists occupy artificially defined areas such as a particular country, country, or national park．The areas inhabited by populations range in size from the few cubic centimeters occupied by the bacteria in a rotting apple to the millions of square kilometers occupied by a population of migratory whales．A population studied by ecologists may consist of a highly localized group of individuals representing fraction of the total population of a species．or it may consist of all the individuals of a species across its entire range．

Ecologists study populations for many reasons. Population studies hold the key to saving endangered species, controlling pest populations, and managing fish and game populations. They also offer clues to understanding and controlling disease epidemics. Finally, the greatest environmental challenge to biological diversity and the integrity of the entire biosphere is at its heart a population problem—the growth of the human population.

All populations share several characteristics. The first is its distribution. The distribution of a population includes the size, shape, and location of the area it occupies. A population also has a characteristic pattern of spacing of the individuals within it. It is also characterized by the number of individuals within it and their density, which is the number of individuals per unit area. Additional characteristics of populations—their age distributions, birth and death rates, immigration and emigration rates, and rates of growth—are the subject of chapters 10 and 11. In chapter 9 we focus on two population characteristics: distribution and abundance.

CONCEPTS

l The physical environment limits the geographic distribution of species.

l On small scales, individuals within populations are distributed in patterns that may be random, regular, or clumped; on larger scales, individuals within a population are clumped.

l Population density declines with increasing organism size.

l Rarity is influenced by geographic range, habitat tolerance, and population size; rare species are vulnerable to extinction.

CASE HISTORIES: distribution limits

The physical environment limits the geographic distribution of species.

A major theme in chapters 4, 5, and 6 is that individual organisms have evolved physiological, anatomical, and behavioral characteristics that compensate for environmental variation. Organisms compensate for temporal and spatial variation in the environment by regulating body temperature and water content and by foraging in a way that maintains energy intake at relatively high levels. However, there are limits on how much organisms can compensate for environmental variation.

While there are few environments on earth without life, no single species can tolerate the full range of earth's environments. For each species some environments are too warm, too cold, too saline, or unsuitable in other ways. As we saw in chapter 6, organisms take in energy at a limited rate. It appears that at some point, the metabolic costs of compensating for environmental variation may take up too much of an organism's energy budget. Partly because of these energy constraints, the physical environment places limits on the distributions of populations. Let's now turn to some actual species and explore the factors that limit their distributions.

Kangaroo Distributions and Climate

The Macropodidea includes the kangaroos and wallabies, which are some of the best known of the Australian animals. However, this group of large-footed mammals includes many less familiar species, including rat kangaroos and tree kangaroos. While some species of macropods can be found in nearly every part of Australia, no single species ranges across the entire continent. All are confined to a limited number of climatic zones and biomes.

G. Caughley and his colleagues (1987) found a close relationship between climate and the distributions of the three largest kangaroos in Australia (fig. 9.2). The eastern grey kangaroo, Macropus giganteus, is confined to the eastern third of the continent. This portion of Anstralia includes several biomes (see chapter 2). Temperate forest grows in the southeast and tropical forests in the north. Mountains, with their varied climates, occupy the central part of the eastern grey kangaroo's range (see figs. 2.13, 2.28, and 2.37). The climatic factor that distinguishes these varied biomes is little seasonal variation in precipitation or dominance by summer precipitation. The western grey kangaroo, M. fuliginosus, lives mainly in the southern and western regions of Australia. Most of the western grey kangaroo's range coincides with the distribution of the temperate woodland and shrubland biome in Australia. The climatically distinctive feature of this biome is a predominance of winter rainfall (see fig. 2.22). Meanwhile, the red kangaroo, M. rufus, wanders the arid and semiarid interior of Australia. The biomes that cover most of the red kangaroo's range are savanna and desert (see figs. 2.16 and 2.19). Of the three species of large kangaroos, the red kangaroo occupies the hottest and driest areas.

FIGURE 9.2 Climate and the distributions of three kangaroo species (data from Caughley et al. 1987).

The distributions of these three large kangaroo species cover most of Australia. However, as you can see in figure 9.2, none of these species lives in the northernmost region of Australia. Caughley and his colleagues explain that these northern areas are probably too hot for the eastern grey kangaroo, too wet for the red kangaroo, and too hot in summer and too dry in winter for the western grey kangaroo. However, they are also careful to point out that these limited distributions may not be determined by climate directly. Instead, they suggest that climate often influences species distributions through factors such as food production, water supply, and habitat. Climate also affects the incidence of parasites, pathogens, and competitors.

Regardless of how the influences of climate are played out, the relationship between climate and the distributions of species can be stable over long periods of time. The distributions of the eastern grey, western grey, and red kangaroos have been stable for at least a century. In the next example, we discuss a species of beetle that appears to have maintained a stable association with climate for 10,000 to 100,00 years.

A Tiger Beetle of Cold Climates

Tiger beetles have entered our discussions several times. In chapter 4, we saw how one species regulates body temperatures on hot black beaches in New Zealand. In chapter 5, we compared the water loss rates of tiger beetles from desert grasslands and riparian habitats in Arizona. Here we consider the distribution of a tiger beetle that inhabits the cold end of the range of environments occupied by tiger beetles.

The tiger beetle Cicindela longilabris lives at higher latitudes and higher elevations than just about any other species of tiger beetle in North America. In the north, C. longilabris is distributed from the Yukon Territory in northwestern Canada to

the maritime provinces of eastern Canada (fig. 9.3). This northern band of beetle populations coincides with the distribution of northern temperate forest and boreal forest in North America (see figs. 2.28 and 2.30). C. longilabris also lives as far south as Arizona and New Mexico. However, these southern populations are confined to high mountains, where C. longilabris is associated with montane coniferous forests. As we saw in chapter 2, these high mountains have a climate similar to that of boreal forest (.see fig. 2.38).

FIGURE 9.3 A tiger beetle, Cicindela Iongilabris, confined to cool environments

(data from Schultz Quinlan, and Hadley 1992).

Ecologists suggest that during the last glacial period C. longilabris lived far south of its present range limits. Then with climatic warming and the retreat of the glaciers, the tiger beetles followed their preferred climate northward and up in elevation into the mountains of western North America (fig. 9.3). As a consequence, the beetles in the southern part of this species range live in isolated mountaintop populations. This hypothesis is supported by the fossil records of many beetle species.

Intrigued by the distribution and history of C. longilabris, Thomas Schultz, Michael Quinlan, and Neil Hadley (1992) set out to study the environmental physiology of widely separated populations of the species. Populations separated for many thousands of years may have been exposed to significantly different environmental regimes. If so, natural selection could have produced significant physiological differences among populations. The researchers compared the

physiological characteristics of beetles from populations of C. longilabris from Maine, Wisconsin, Colorado, and northern Arizona. Their measurements included water loss rates, metabolic rates, and body temperature preferences.

Schultz and his colleagues found that the metabolic rates of C. longilabris are higher and its preferred temperatures lower than those of most other tiger beetle species that have been studied. These differences support the hypothesis that C. longilabris is adapted to the cool climates of boreal and montane forests. In addition, the researchers found that none of their measurements differed significantly among populations of C. longilabris. Figure 9.4 illustrates the remarkable similarity in preferred body temperature shown by foraging C. longilabris from populations separated by as much as 3,000 km and, perhaps, by 10,000 years of history. These results support the generalization that the physical environment limits the distributions of species. It also suggests that those limits may be stable for long periods of time.

FIGURE 9.4 Uniform temperature preference across an extensive geographic range (data from Schuttz, Quinlan, and Hadley 1992).

Now, let's consider how the physical environment may limit the distribution of plants. Our example is drawn from the arid and semiarid regions of the American Southwest.

Distributions of Plants along a Moisture-Temperature Gradient

In chapter 4, we discussed the influence of pubescence on leaf temperature in plants of the genus Encelia. Variation in leaf pubescence among Encelia species appears to correspond directly to the distributions of these species along a moisture-temperature gradient from the California coast eastward (Ehleringer and Clark 1988). Encelia californica, the species with the least pubescent leaves, occupies a narrow coastal zone that extends from southern California to northern Baja California (fig. 9.5). Inland, E. californica is replaced by E. actoni, which has leaves that are slightly more pubescent. Still farther to the east, E. actoni is in turn replaced by E. frutescens and E. farinosa.

FIGURE 9.5 The distributions of four Encelia species in southwestern North America (data from Ehleringer and Clark 1988).

These geographic limits to these species' distributions correspond to variations in temperature and precipitation. The coastal environments where E. californica lives are all relatively cool. However, average annual precipitation differs a great deal across the distribution of this species. Annual precipitation ranges from about 100 mm in the southern part of its distribution to well over 400 mm in the northern part. By comparison, E. actoni occupies environments that are only slightly warmer but considerably drier. The rainfall in areas occupied by E. frutescens and E. farinosa is similar to the amount that falls falls in the areas occupied by E. actoni and E. californica. However, the environments of E. frutescens and E. farinosa are much hotter.

Variation in leaf pubescence does not correspond entirely to the macroclimates inhabited by Encelia species, The leaves of E. frutescens are nearly as free of pubescence as the coastal species E. californica. However, E. frutescens grows side by side with E. farinosa in some of the hottest deserts in the world. Because they are sparsely pubescent, the leaves of E. frutescens absorb a great deal more radiant energy than the leaves of E. farinosa (fig. 9.6). Under similar conditions, however, leaf temperatures of the two species nearly identical. How does E. frutescens avoid overheating? The leaves do not overheat because they transpire at a high rate and are evaporatively cooled as a consequence.

FIGURE 9.6 Light absorption by leaves of Encelia frutescens and E. farinosa (data from Ehleringer and Clark 1988).

Evaporative cooling solves one ecological puzzle appears to create another. Remember that these two shrubs live: in some of the hottest and driest deserts in the world. Where does E. frutescens get enough water to evaporatively cool its Leaves? Though the distributions of E. frutescens and E. farinosa overlap a great deal on a geographic scale, these two species occupy distinctive microenvironments. As shown in figure 9.7, E. farinosa grows mainly on upland slopes, while E. frutescens is largely confined to ephemeral stream channels, or desert washes. Along washes, runoff combined with deep soils increases the availability of soil moisture. This example reminds us of a principle that we first considered in chapter 4: organisms living in the same macroclimate may, because of slight differences in local distribution, experience substantially different microclimates. This is certainly true of the two barnacle species we consider in the following example.

FIGURE 9.7 Temperature regulation and distributions of Encelia farinosa and E. frutescens across microenvironments.

Distributions of Barnacles along an Intertidal Exposure Gradient

The marine intertidal zone presents a steep gradient of physical conditions from the shore seaward. As we saw in chapter 3, the organisms high in the intertidal zone are exposed by virtually every tide while the organisms that live at lower levels in the intertidal zone are exposed by the lowest tides only. Exposure to air differs at different levels within the intertidal zone. Organisms that live in the intertidal zone have evolved different degrees of resistance to drying, a major factor contributing to zonation among intertidal organisms (see fig. 3.17).

Barnacles, one of the most common intertidal organisms, show distinctive patterns of zonation within the intertidal zone. For example, Joseph Connell (1961) described how along the coast of Scotland, adult Chthamalus stellatus are restricted to the upper levels of the intertidal zone, while adult Balanus balanoides are limited to the middle and lower levels (fig. 9.8). What role does resistance to drying play in the intertidal zonation of these two species? Unusually calm and warm weather combined with very low tides gave Connell some insights into this question. In the spring of 1955, warm weather coincided with calm seas and very low tides. As a consequence, no water reached the upper intertidal zone occupied by both species of barnacles. During this period, Balanus in the upper intertidal zone suffered much higher mortality than Chthamalus (fig. 9.9). Meanwhile, Balanus in the lower intertidal zone showed normal rates of mortality. Of the two species, Balanus appears to be more vulnerable to desiccation. Higher rates of desiccation may exclude this species of barnacle from the upper intertidal zone.

FIGURE 9.8 Distributions of two barnacle species within the intertidal tone (data from Connell 1961).

FIGURE 9.9 Barnacle mortality in the upper intertidal zone (data from ConneU 1961).

Vulnerability to dessication, however, does not completely explain the pattern of intertidal zonation shown by Balanus and Chthamalus. What excludes Chthamalus from the lower intertidal zone? Though the larvae of this barnacle settle in the lower intertidal zone, the adults rarely survive there. Connell explored this question by transplanting adult Chthamalus to the lower intertidal zone and found that transplanted adults survive in the lower intertidal zone very well. If the physical environment does not exclude Chthamalus from the lower intertidal zone, what does? It turns out that this species is excluded from the lower intertidal zone by competitive interactions with Balanus. We discuss the mechanisms by which this competitive exclusion is accomplished in chapter 13, which covers interspecific competition.

These barnacles remind us that the environment consists of more than just physical and chemical factors. An organism's environment also includes biological factors, in many situations, biological factors may be as important or even more important than physical factors in determining the distribution and abundance of species. Often the influences of biological factors remain hidden, however, because of the difficulty of demonstrating them. In ecology, we must usually probe deeper to see beyond outward appearances, as Connell did when he transplanted Chthamalus from the upper to the lower intertidal zone. The influence of biological factors, such as competition, predation, and disease, on the distribution and abundance of organisms is a theme that enters our discussions frequently in the remainder of this book, especially in chapters13.14, and15.

CASE HISTORIES:distribution patterns

On small scales, individuals within populations are distributed in patterns that may be random, regular, or clumped; on larger scales, individuals within a population are clumped.

We have just considered how the environment limits the distributions of species. When you map the distribution of a species such as the red kangaroo in Australia (see fig. 9.2), or the zoned distribution of Chthamalus and Balanus in the intertidal zone (see fig. 9.8), the boundaries on your map indicate the range of the species. In other words, your map shows where at least some individuals of the species live and where they axe absent. Knowing a species' range, as defined by presence and absence, is useful, but it says nothing about how the individuals that make up the population are distributed in the areas where they are presenL Are individuals randomly distributed across the range? Are they regularly distributed? As we shall see, the distribution pattern observed by an ecologist is strongly influenced by the scale at which a population is studied.

Ecologists refer frequently to large-scale and small-scale phenomena. What is "large" or "small" depends on the size of organism or other ecological phenomenon under study. For this discussion, small scale refers to distances of no more than a few hundred meters, over which there is little environmental change significant to the organism under study. Large scale refers to areas over which there is substantial environmental change. In this sense, large scale may refer to patterns over an entire continent or patterns along a mountain slope, where environmental gradients are steep. Let's begin our discussion with patterns of distribution observed at small scales.

Distributions of Individuals on Small Scales

Three basic patterns of distribution are observed on small scales: random, regular, or clumped. A random distribution is one in which individuals within a population have an equal chance of living anywhere within an area. A regular distribution is one in which individuals are uniformly spaced. In a clumped distribution, individuals have a much higher probability of being found in some areas than in others (fig. 9.10).

FIGURE 9.10 Random, regular, and clumped distributions.

These three basic patterns of distribution are produced by the kinds of interactions that take place between individuals within a population, by the structure of the physical environment, or by a combination of interaction and environment each other, repel each other, or ignore each other. Mutual attraction creates clumped, or aggregated, patterns of distribution. Regular patterns of distribution are produced when individuals avoid each other or claim exclusive use of a patch of landscape. Neutral responses contribute to random distributions.

The patterns created by social interactions may be reinforced or damped by the structure of the environment. An environment with patchy distributions of nutrients, nesting site, water, and so forth fosters clumped distribution patterns. An environment with a fairly uniform distribution of resources and frequent, random patterns of disturbance (or mixing) tends to reinforce random or regular distributions. Let's now consider factors that influence the distributions of some species in nature.

Distributions of Tropical Bee Colonies

Stephen Hubbell and Leslie Johnson (1977) recorded a dramatic example of how social interactions can produce and enforce regular spacing in a population. They studied competition and nest spacing in populations of stingless bees in the family Trigonidae. The bees they studied live in tropical dry forest in Costa Rica, Though these bees do not sting, rival colonies of some species fight fiercely over potential nesting sites.

Stingless bees are abundant in tropical and subtropical environments, where they gather nectar and pollen from a wide variety of flowers. They generally nest in trees and live in colonies made up of hundreds to thousands of workers, Hubbell and Johnson observed that some species of stingless bees are highly aggressive to other members of their species from other colonies, while others are not. Aggressive species usually forage in groups and feed mainly on flowers that occur in high-density clumps. The nonaggressive species feed singly or in small groups and on more widely distributed flowers.

Hubbell and Johnson studied several species of stingless bees to determine whether there is a relationship between aggressiveness and patterns of colony distribution. They predicted that the colonies of aggressive species would show regular distributions while those of nonaggressive species would show random or clumped distributions, They concentrated their studies on a 13 ha tract of tropical dry forest that con-rained numerous nests of nine species of stingless bees.

Though Hubbell and Johnson were interested in how bee behavior might affect colony distributions, they recognized that the availability of potential nest sites for colonies could also affect distributions. So, in one of the first steps in their study, they mapped the distributions of trees suitable for nesting. They found that potential nest trees were distributed randomly through the study area and that the number of potential nest sites was much greater than the number of bee colonies. What did these measurements tell the researchers? They indicated that the number of colonies in the study area was not limited by availability of suitable trees and that clumped and regular distribution of colonies would not be due to an underlying clumped or regular distribution of potential nest sites,

Hubbell and Johnson were able to map the nests of five of the nine species of stingless bees accurately, The nests of four of these species were distributed regularly. As they had predicted, all four species with regular nest distributions were highly aggressive to bees from other colonies of their own species, The fifth species, Trigona dorsalis, was not aggressive and its nests were randomly distributed over the study area. Figure 9.11 contrasts the random distribution of T. dorsalis with the regular distribution of one of the aggressive species, T. fulviventris.

FIGURE 9.11 Regular and random distributions of stingless bee colonies in the tropical dry forest (data from Hubbell and Johnson 1977).

The researchers also studied the process by which the aggressive species establish new colonies. In the process, they made observations that provide insights into the mechanisms that establish and maintain the regular nest distributions of species such as T. fulviventris. This species and the other aggressive species apparently mark prospective nest sites with a pheromone. Pheromones are chemical substances secreted by some animals for communication with other members of their species, The pheromone secreted by these stingless bees attracts and aggregates members of their colony to the prospective nest site; however, it also attracts workers from other nests.

If workers from two different colonies arrive at the prospective nest, they may fight for possession. Fights may be escalated into protracted battles. Hubbell and Johnson observed battles over a nest tree that lasted for 2 weeks. Each dawn, 15 to 30 workers from two rival colonies arrived at the contested nest site. The workers from the two rival colonies faced off in two swarms and displayed and fought with each other. In the displays, pairs of bees faced each other, slowly flew vertically to a height of about 3 m, and then grappled each other to the ground. When the two bees Mt the ground, they separated, faced off, and performed another aerial display. Bees did not appear to be injured in these fights, which were apparently ritualized. The two swarms abandoned the battle at about 8 or 9 A.M. each morning, only to re-form and begin again the next day just after dawn. While this contest over an unoccupied nest site produced no obvious mortality, fights over occupied nests sometimes killed over 1,000 bees in a single battle. These tropical bees space their colonies by engaging in pitched battles, but as we see next, plants space themselves by more subtle means.

Distributions of Desert Shrubs

Half a century ago desert ecologists suggested that desert shrubs tend to be regularly spaced due to competition between the shrubs. You can see the patterns that inspired these early ecologists by traveling across the seemingly endless expanses of the Mojave Desert in western North America. One of the most common plants that you will see is the creosote bush, Larrea tridentata, which dominates thousands of square kilometers of this area. As you look out across landscapes dominated by creosote bushes it may appear that the spacing of these shrubs is regular (fig. 9.12). in places, their spacing is so uniform that they appear to have been planted by some very careful gardener. As we shall see, however, visual impressions can be deceiving.

FIGURE 9.12 Are local populations of the creosote bush. Larrea tridentata, distributed reguarly?

Quantitative sampling and statistical analysis of the distributions of creosote bushes and other desert shrubs led to a controversy that took the better part of two decades to settle. In short, when different teams of researchers quantified the distributions of desert shrubs, some found the regular distributions reported by earlier ecologists. Others found random or clumped distributions. Still others reported all three types of distributions.

Though we are generally accustomed to having one answer to our questions, the answers to ecological questions are often more complex. Research by Donald Phillips and James MacMahon (1981) showed that the distribution of creosote bushes changes as they grow. They mapped and analyzed the distributions of creosote bushes and several other shrubs at nine sites in the Sonoran and Mojave Deserts. Because earlier researchers had suggested that creosote bush spacing changed with available moisture, they chose sites with different average precipitations. Precipitation at the study sites ranged from 80 to 220 mm, and average July temperature varied from 27°to 35℃. Phillips and MacMahon took care to pick sites with similar soils and with similar topography. They studied populations growing on sandy to sandy loam soils with less than 2% slope with no obvious surface runoff channels.

The results of this study indicate that the distribution of desert shrubs changes from clumped to random to regular distribution patterns as they grow. The young shrubs tend to be clumped for three reasons: because seeds germinate at a limited number of "safe sites," because seeds are not dispersed far from the parent plant, or because asexually produced offspring are necessarily close to the parent plant. Phillips and MacMahon proposed that as the plants grow, some individuals in the clumps die, which reduces the degree of clumping. Gradually, the distribution of shrubs becomes more and more random. However, competition among the remaining plants produces higher mortality among plants with nearby neighbors, which thins the stand of shrubs still further and eventually creates a regular distribution of shrubs. This hypothetical process is summarized in figure 9.13.

FIGUIRE 9.13 Hypothetical change in shrub distributions with increasing shrub size.

Phillips and MacMahon and other ecologists proposed that desert shrubs compete for water and nutrients, a competition that takes place belowground. How can we study these belowground interactions? Work by Jacques Brisson and James Reynolds (1994) provides a quantitative picture of the belowground side of creosote bush distributions. These researchers carefully excavated and mapped the distributions of 32 creosote bushes in the Chihuahuan Desert. They proposed that if creosote bushes compete, their roots should grow in a way that reduces overlap with the roots of nearby individuals.

The 32 excavated creosote bushes occupied a 4 by 5 m area on the Jomada Long Term Ecological Research site near Las Cruces, New Mexico. The creosote bush was the only shrub within the study plot. Their roots penetrated to only 30 to 50 cm, the depth of a hardpan calcium carbonate deposition layer. Because they did not have to excavate to great depths, Brisson and Reynolds were able to map more root systems than previous researchers. Still, their excavation and mapping of roots required 2 months of intense labor.

The complex pattern of root distributions uncovered confirmed the researchers proposal: Creosote bush roots grow in a pattern that reduces overlap between the roots of adjacent plants (fig. 9.14a). We can make the root distributions of individual plants clearer by plotting their perimeters only. Figure 9.14b shows the hypothetical distributions of creosote bushes with circular root systems, while figure 9.14c shows their actual root distributions. Notice that the root systems of creosote bushes overlap much less than they would if they had circular distributions. Brisson and Reynolds conclude that competitive interactions with neighboring shrubs influence the distribution of creosote bush roots. Their work suggests that creosote bushes compete for belowground resources.

FIGURE 9.14 Creosote bush root distributions: hypothetical versus actual root overlap (data from Brisson and Reynolds 1994).

After more than two decades of work on this single species of plant, desert ecologists have a much clearer understanding of the factors that influence the distribution of individuals on a small scale. On small scales, the creosote bush may have clumped, random, or regular distributions. Hubbell and Johnson (1977) showed that stingless bee colonies may also show different patterns of distribution, depending on the level of aggression between colonies. As we shall see in the following section, however, on larger scales, individuals have clumped distributions.

Distributions of Individuals on Large Scale

We have considered how individuals within a population are distributed on a small scale: how bee colonies are distributed within a few acres of forest and how shrubs are distributed within a small stand. Now let's step hack and ask how individuals within a population are distributed on a larger scale over which there is significant environmental variation. For instance, how does the density of individuals vary across the entire range of a species? Is population density fairly regularly distributed across the entire area occupied by a species, or are there a few centers of high density surrounded by areas in which the species is present but only in low densities?

Bird Populations Across North America

Terry Root (1988) mapped patterns of bird abundance across North America using the "Christmas Bird Counts." These bird counts provide one of the few data sets extensive enough to study distribution patterns across an entire continent. Christmas Bird Counts, which began in 1900, involve annual counts of birds during the Christmas season. The first Christmas Bird Count was attended by 27 observers, who counted birds in 26 localities--2 in Canada and the remainder in 13 states of the United States. In the 1985-86 season, 38,346 people participated in the Christmas Bird Count. The observers counted birds in 1,504 localities throughout the United States and most of Canada. The Christmas Bird Count marks its centennial anniversary in the year 2000. It continues to produce a unique record of the distribution and population densities of wintering birds across most of a continent.

Root's analysis centers around a series of maps that show patterns of distribution and population density for 346 species of birds that winter in the United States and Canada. Although species as different as swans and sparrows are included, the maps show a consistent pattern. At the continental scale, bird populations show clumped distributions. Clumped patterns occur in species with widespread distribution, such as the American crow, Corvus brachyrhynchos, as well as in species with restricted distributions, such as the fish crow, C. ossifragus. Though the winter distribution of the American crow includes most of the continent, the bulk of individuals in this population are concentrated in a few areas. These areas of high density, or "hot spots," appear as red dots in figure 9.15a. For the American crow population, hot spots are concentrated along river valleys, especially the Cumberland, Mississippi. Arkansas, Snake, and Rio Grande. Away from these hot spots the winter abundance of American crows diminishes rapidly.

The fish crow population, though much more restricted than that of the American crow, is also concentrated in a few areas (fig. 9.15b). Fish crows are restricted to areas of open water near the coast of the Gulf of Mexico and along the southern half of the Atlantic coast of the United States. Within this restricted range, however, most fish crows are concentrated in a few hot spots--one on the Mississippi Delta, another on Lake Seminole west of Tallahassee, Florida, and a third in the everglades in southern Florida. Like the more widely distributed American crow, the abundance of fish crows diminishes rapidly away from these centers of high density.

FIGURE 9.15 (a) Winter distribution of the American crow, Corvus brachyrynchos (b) winter distribution of the fish crow. C. ossifragus (data from Root 1988).

Might bird populations have clumped distributions only on the wintering grounds? James H. Brown, David Mehlman, and George Stevens (1995) analyzed large-scale patterns of abundance among birds across North America during the breeding season, the opposite season from that studied by Root. In their study these researchers used data from the Breeding Bird Survey, which consists of standardized counts by amateur ornithologists conducted each June at approximately 2,000 sites across the United States and Canada under the supervision of the Fish and Wildlife Services of the United States and Canada. For their analyses, they chose species of birds whose geographic ranges fall mainly or completely within the eastern and central regions of the United States, which are well covered by study sites of the Breeding Bird Survey.

Like Root, Brown and his colleagues found that a relatively small proportion of study sites yielded most of the records of each bird species. That is, most individuals were concentrated in a fairly small number of hot spots. For instance, the densities of red-eyed vireos are Iow in most places (fig. 9,16). Clumped distributions were documented repeatedly. When the numbers of birds across their ranges were totaled, generally about 25% of the locations sampled supported over half of each population. By combining the results of Root and Brown and his colleagues we can say confidently that at larger scales, bird populations in North America show clumped patterns of distribution. In other words, most individuals within a bird species live in a few hot spots, areas of unusually high population density.

FIGURE 9.16 Red-eyed vireos, Vireo olivaceus, counted along census routes of the Breeding Bird Survey (data from Brown. Mehlman, and Stevens 1995)

Brown and his colleagues propose that these distributions are clumped because the environment varies and individuals aggregate in areas where the environment is favorable. What might be the patterns of distribution for populations distributed along a known environmental gradient? Studies of plant populations provide interesting insights.

Plant Abundance Along Moisture Gradients

Several decades ago, Robert Whittaker gathered information on the distributions of woody plants along moisture gradients in several mountain ranges across North America. As we saw in chapter 2 (see fig, 2.38) environmental conditions on mountainsides change substantially with elevation. These steep environmental gradients provide a compressed analog of the continental-scale gradients to which the birds studied by Root and Brown and his colleagues were presumably responding.

Let's look at the distributions of some tree species along moisture gradients in two of the mountain ranges studied by Whittaker. Robert Whittaker and William Niering (1965) studied the distribution of plants along moisture and elevation gradients in the Santa Catalina Mountains of southern Arizona. These mountains rise out of the Sonoran Desert near Tucson, Arizona, like a green island in a tan desert sea. Vegetation typical of the Sonoran Desert, including the saguaro cactus and creosote bush, grow in the surrounding desert and on the lower slopes of the mountains. However, the summit of the mountains is topped by a mixed conifer forest. Forests also extend down the flanks of the Santa Catalinas in moist, shady canyons.

There is a moisture gradient from the moist canyon bottoms up the dry southwest-facing slopes. Whittaker and Niering found that along this gradient the Mexican pinyon pine, Pinus cembroides, is at its peak abundance on the uppermost and driest part of the southwest-facing slope (fig. 9.17). Along the same slope, Arizona madrone, Arbutus arizonica, reaches its peak abundance at middle elevations. Finally. Douglas firs, Psuedotsuga menziesii, are restricted to the moist canyon bottom. Mexican pinyon pines, Arizona madrone, and Douglas fir are all clumped along this moisture gradient, but each reaches peak abundance at different positions on the slope. These positions appear to reflect the different environmental requirements of each species.

FIGURE. 9.17 Abundances of three tree species on a moisture gradient in the Santa Catalina Mountains, Arizona (data from Whittaker and Niering 1965).

Whittaker (1956) recorded analogous tree distributions along moisture gradients in the Great Smoky Mountains of eastern North America, Again, the gradient was from a moist valley bottom to a drier southwest-facing slope, Along this moisture gradient, hemlock, Tsnga canadensis, was concentrated in the moist valley bottom and its density decreased rapidly upslope (fig. 9.18). Meanwhile red maple, Acer rubrum. grew at highest densities in the middle section of the slope, while table mountain pine, Pinus pungens, was concentrated on the driest upper sections. As in the Santa Catalina Mountains of Arizona, these tree distributions in the Great Smoky Mountains reflect the moisture requirements of each tree species.

FIGURE 9. 18 Abundance of three tree species on a moisture gradient in the Great Smoky Mountains, Tennessee (data from Whittaker 1956).

The distribution of trees along moisture gradients seems to resemble the clumped distributional patterns of birds across the North American continent but on a smaller scale. All species of trees discussed here showed a highly clumped distribution along moisture gradients, and their densities decreased substantially toward the edges of their distributions. In other words, like birds, tree populations are concentrated in hot spots.

In this section, we have reviewed patterns of distribution within populations. We have seen that those patterns vary from one population to another and may depend upon the scale at which ecologists make their observations. Now we turn from patterns of spatial variation within populations to compare the average densities of different populations. Is there any way to predict the average population density of populations? While it is not possible to make precise predictions, the following examples show that population densities are very much influenced by organism size.

CASE HISTORIES: organism size and population density

Population density declines with increasing organism size.

If you estimate the densities of organisms in their natural environments, you will find great ranges. While bacterial populations in soils or water can exceed l0⁹ per cubic centimeter and phytoplankton densities often exceed 10⁶ per cubic meter, populations of large mammals and birds can average considerably less than one individual per square kilometer. What factors produce this variation in population density? The densities of a wide variety of organisms are highly correlated with body size. In general, densities of animal and plant populations decrease with increasing size.

FIGURE 9.19 Body size and population density of herbivorous mammals (data from Damuth 1981).

While it makes common sense that small animals and plants generally live at higher population densities than larger ones, quantifying the relationship between body size and population density provides valuable information. First, quantification translates a general qualitative notion into a more precise quantitative relationship. For example, you might want to know how much population density declines with increased body size. Second, measuring the relationship between body size and population density for a wide variety of species reveals different relationships for different groups of organisms. Differences in the relationship between size and population density can be seen, among major groups of animals.

Animal Size and Population Density

John Damuth (1981) produced one of the first clear demonstrations of the relationship between body size and population density. He focused his analysis on herbivorous mammals. The size of herbivorous mammals included in the analysis ranged from small rodents, with a mass of about 10 g, to large herbivores such as rhinoceros, with a mass well over 10⁶ g. Meanwhile, average population density ranged from about 1 individual (10^-1) per 10 km² to about 10,000 (10⁴) per 1 km², which spans approximately five "orders of magnitude," or powers of 10, in population density. As figure 9.19 shows, Damuth found that the population density of 307 species of herbivorous mammals decreases, from species to species, with increased body size. The line in the graph, which is called the regression line, shows the average decrease in population density with increased body size.

Building on Damuth's analysis, Robert Peters and Karen Wassenberg (1983) explored the relationship between body size and average population density for a wider variety of animals. Their analysis included terrestrial invertebrates, aquatic invertebrates, mammals, birds, and poikilothermic vertebrates. They included animals representing a great range in size and population density. Animal mass ranged from 10^-11 to about 10^2.3 kg, while population density ranged from less than 1 per square kilometer to nearly 10¹² per square kilometer. When Peters and Wassenberg plotted animal mass against average density, they, like Damuth, found that population density decreased with increased body size.

If you look closely at the data in figure 9.20, however, it is clear that there are differences among the animal groups. First, aquatic invertebrates of a given body size tend to have higher population densities, usually one or two orders of magnitude higher, than terrestrial invertebrates of similar size. Second, mammals tend to have higher population densities than birds of similar size. Peters and Wassenberg suggest that it may be appropriate to analyze aquatic invertebrates and birds separately from the other groups of animals.

FIGURE 9.20 Animal size and population density (data from Peters and Wassenberg 1983).

The general relationship between animal size and population density has held up under careful scrutiny and reanalysis. Plant ecologists have found a qualitatively similar relationship in plant populations, as we see next. Plant Size and Population Density James White (1985) pointed out that plant ecologists have been studying the relationship between plant size and population density since early in the twentieth century. He suggests that the relationship between size and density is one of the most fundamental aspects of population biology. White summarized the relationship between size and density for a large number of plant species spanning a wide range of plant growth forms (fig. 9.21).

FIGURE 9.21 Plant size and population density (data from White 1985).

The pattern in figure 9.21 illustrates that as in animals, plant population density decreases with increasing plant size. However, the biological details underlying the size-density relationship shown by plants are quite different from those underlying the size-density patterns shown by animals. The different points in figures 9.19 and 9.20 represent different species of animals, A single species of tree, however, can span a very large range of sizes and densities during its life cycle. Even the largest trees, such as the giant sequoia, Sequoia gigantea, start life as small seedlings. These tiny seedlings can live at very high densities. As the trees grow, density declines progressively until the mature trees live at low densities. We discuss this process, which is called self-thinning, in chapter 13. Thus, the size-density relationship changes dynamically within plant populations and also differs significantly between populations of plants that reach different sizes at maturity. Despite differences in the underlying processes, the data summarized in figure 9.21 indicate a predictable relationship between plant size and population density.

The value of such an empirical relationship, whether for plants or animals, is that it provides a standard against which we can compare measured densities and gives an idea of expected population densities in nature. For example, suppose you go out into the field and measure the population density of some species of animal. How would you know if the densities you encounter are unusually high, low, or about average for an animal of the particular size and taxon? Without an empirical relationship such as that shown in figures 9.20 and 9.21 or a list of species densities, it would be impossible to make such an assessment. One question that we might attempt to answer with a population study is whether a species is rare. As we shall see in the next section, "Rarity and Extinction," rarity is a more complex consideration than it might seem at face value.

CASE HISTORIES: rarity and extinction

Rarity is influenced by geographic range, habitat tolerance, and population size; rare species are vulnerable to extinction.

Viewed on a long-term, geological timescale, populations come and go and extinction seems to be the inevitable punctuation mark at the end of a species' history. However, some populations seem to be more vulnerable to extinction than others. What makes some populations likely to disappear, while others persist through geological ages? At the heart of the matter are patterns of distribution and abundance. Species that are rare seem to be more vulnerable to extinction. In order to understand and, perhaps, prevent extinction, we need to understand the several forms of rarity.

Seven Forms Of Rarity and One of Abundance.

Deborah Rabinowitz (1981) devised a classification of commonness and rarity, based on combinations of three factors: (1) the geographic range of a species (extensive versus restricted), (2) habitat tolerance (broad versus narrow), and (3) local population size (large versus small). Habitat tolerance is related to the range of conditions in which a species can live. For instance, some plant species can tolerate a broad range of soil texture, pH, and organic matter content, while other plant species are confined to a single soil type. As we shall see, tigers have broad habitat tolerance; however, within the tiger's historical range in Asia lives the snow leopard, which is confined to a narrow range of conditions in the high mountains of the Tibetan Plateau. Small geographic range, narrow habitat tolerance, and low population density are attributes of rarity.

As shown in figure 9.22, there are eight possible combinations of these factors, seven of which include at least one attribute of rarity. The most abundant species and those least threatened by extinction have extensive geographic ranges, broad habitat tolerances, and large local populations at least somewhere within their range. Some of these species, such as starlings, Norway rats, and house sparrows, are associated with humans and are considered pests. However. Many species of small mammals, birds, and invertebrates not associated with humans, such as the deer mouse, Peromyscus maniculatus, or the marine zooplankton, Calanus finmarchicus, also fall into this least threatened category. The seven other combinations of range, tolerance, and population size each create a kind of rarity. As a consequence, Rabinowitz referred to "seven forms of rarity."

FIGURE 9.22 Commonness, rarity, and vulnerability to extinction.

Let's look at species that represent the two extremes of Rabinowitz's seven forms of rarity. The first two discussions concern species that are rare according to only one attribute. These are species that, before they become extinct, may seem fairly secure. The final discussion concerns the very rarest species, which show all three attributes of rarity. Though these rarest species are the most vulnerable to extinction, rarity in any form appears to increase vulnerability to extinction.

Rarity I: Extensive Range, Broad Habitat Tolerance, Small Local Populations

It is easy to understand how people were drawn to the original practice of falconry. The sight and sound of a peregrine falcon, Falco peregrinus, in full dive at over 200 km per hour must have been one of the great experiences of a lifetime (fig. 9.23). To have held such a bird on your arm and launched it at its avian prey must have seemed liked controlling the wind. The peregrine, which has a geographic range that circles the Northern Hemisphere and broad habitat tolerance, is uncommon throughout its range. Apparently, this one attribute of rarity was enough to make the peregrine vulnerable to extinction. The falcon's feeding on prey containing high concentrations of

DDT, which produced thin eggshells and nesting failure, was enough to drive the peregrine to the brink of extinction. Peregrine falcons were saved from extinction by control of the use of DDT, strict regulation of the capture of the birds, capfive breeding, and reintroduction of the birds to areas where local populations had become extinct.

FIGURE 9.23 The peregrine falcon, Falco peregrinus, is found throughout the Northern Hemisphere but lives at low population densities throughout its range.

The range of the tiger, Panthera tigris, once extended from Turkey to eastern Siberia, Java, and Bali and included environments ranging from boreal forest to tropical rain forest. The tigers in this far-flung population varied enough from place to place in size and coloration that many local populations were described as separate subspecies, including the Siberian, Bengal, and Javanese tigers. Like peregrine falcons, tigers had an extensive geographic range and broad habitat tolerance but low population density. Over the centuries, relentless pursuit by hunters reduced the tiger's range from nearly half of the largest continent on earth to a series of tiny fragmented populations. Many local populations have become extinct and others, such as the magnificent Siberian tiger, teeter on the verge of extinction in the wild. These populations may survive only through captive breeding programs in zoos. The next example shows that narrow habitat tolerance can also lead to extinction.

Rarity II: Extensive Range, Large Populations, Narrow Habitat Tolerance

When Europeans arrived in North America, they encountered one of the most numerous birds on earth, the passenger pigeon. The range of the passenger pigeon extended from the eastern shores of the present-day United States to the Midwest, and its population size numbered in the billions. However, the bird had one attribute of rarity: it had a narrow requirement for its nesting sites. The passenger pigeon nested in huge aggregations in virgin forests. As virgin forests were cut, its range

diminished and market hunters easily located and exploited its remaining nesting sites, finishing off the remainder of the population. By 1914, when the last passenger pigeon died in captivity, one of the formerly most numerous bird species on earth was extinct. Extensive range and high population density alone do not guarantee immunity from extinction.

The rivers in the same region inhabited by the passenger pigeon harbored an abundant, widely distributed but narrowly tolerant fish, the harelip sucker, Lagochila lacera. This fish was found in streams across most of the east-central United States and was abundant enough that early ichthyologists cited it as one of the commonest and most valuable food fishes in the region. However, the harelip sucker, like the passenger pigeon, had narrow habitat requirements. It was restricted to large pools with rocky bottoms in clear, medium-sized streams about 15 to 30 m wide. This habitat was eliminated by the silting of rivers that followed deforestation and by the erosion of poorly managed agricultural lands. The last individuals of this species collected by ichthyologists came from the Maumee River in northwestern Ohio in 1893.

Extreme Rarity: Restricted Range, Narrow Habitat Tolerance, and Small Populations

Species that combine small geographic ranges with narrow habitat tolerances and low population densities are the rarest of the rare. This group includes species such as the mountain gorilla, the giant panda, and the California condor. Species showing this extreme form of rarity are clearly the most vulnerable to extinction. Many island species have these attributes, so it is not surprising that island species are especially vulnerable. Of the 171 bird species and subspecies known to have become extinct since 1600, 155 species have been restricted to islands. Of the 70 species and subspecies of birds known to have lived on the Hawaiian Islands, 24 are now extinct and 30 are considered in danger of extinction.

Organisms on continents that are restricted to small areas, have narrow habitat tolerance, and small population size are also vulnerable to extinction. Examples of populations in such circumstances are common. More than 20 species of plants and animals are confined to about 200 km² of mixed wetlands and upland desert in California called Ash Meadows. The Ash Meadows stick-leaf, Mentzelia leucophylla, inhabits an area of about 2.5 km² and has a total population size of fewer than 100 individuals. Another plant, the Ash Meadows milk vetch, Astragalus phoenix, has a total population of fewer than 600 individuals. Human alteration of Ash Meadows appears to have caused the extinction of at least one native species, the Ash Meadows killifish, Empetrichthys merriami.

Amazingly, there are species with ranges even more restricted than those of Ash Meadows, California. In 1980. the total population of the Virginia round-leaf birch, Betula uber. was limited to 20 individuals in Smyth County, Virginia. Until recently the total habitat of the Socorro isopod, Thermosphaeroma thermophilum, of Socorro, New Mexico. was bruited to a spring pool and outflow with a surface area of a few square meters. Meanwhile, a palm species, Pritchardia monroi, which is found only on the island of Maui in the Hawaiian Islands, has a total population in nature of exactly one individual!

Examples such as these fill books listing endangered species. In nearly all cases, the key to a species' survival is increased distribution and abundance. One of the most fundamental needs for managing species, endangered or not, is making accurate estimates of population size. Some of the conceptual and practical issues that population ecologists must consider when censusing a population are the subject of the Applications and Tools section.

APPLICATIONS AND TOOLS: estimating abundance --- from whales to sponges

The abundance of organisms and how abundance changes in time and space are among the most fundamental concerns of ecology. These factors are so basic that some authors define ecology as the study of distribution and abundance of organisms. Because abundance is so important, ecologists should understand how to estimate it for a wide variety of organisms. Keep in mind, however, that ecologists do not measure abundance as an end in itself but as a tool to understand the ecology of populations. Knowing how abundant an organism is can tell us whether its population is growing, declining, or stable. As we saw in the previous section, population size is one of the characteristics that helps ecologists assess a species' vulnerability to extinction. However, to estimate the abundance of species the ecologist must contend with a variety of practical challenges and conceptual subtleties. Some of these are discussed here..

Estimating Whale Population Size

In 1989, the journal Oceanus published a table that listed the estimated sizes of whale populations. The table included the following note: "All estimates . . . are highly speculative." Why is it difficult to provide firm estimates of whale population size.'? Briefly, whales live at low population densities and may be distributed across vast expanses of ocean. They also spend much 6me submerged and move around a great deal. As large as they are, you cannot count all the whales in the ocean. instead, marine ecologists rely on population estimation. Each method of estimation has its own limitations and uncertainties.

One method used to estimate population sizes of elusive animals involves marking or tagging some known number of individuals in the population, releasing the marked individuals so they will mix with the remainder of the population, and then sampling the population at some later time. The ratio of marked to unmarked individuals in the sample gives an estimate of population size. The simplest formula expressing this relationship is the Lincoln-Peterson index:

M/N = m/n

where:

M = the number of individuals marked and released

N = the actual size of the study population

m = the number of marked individuals in a sample of the population

n = the total number of individuals in the sample

The major assumption of the Lincoln-Peterson index is that the ratio of marked to unmarked individuals in the population as a whole equals the ratio of marked to unmarked individuals in a sample of the population, ff this is approximately so, then the population size is estimated as:

N = Mn/m

However. on average, the Lincoln-Peterson index overestimates population size. To reduce this tendency to overestimate, N. Bailey (1951, 1952) proposed a corrected formula:

N=M(n+ I)/m+ 1

Some of the assumptions of mark and recapture studies are:

l All individuals in the population have an equal probability of being captured.

l The population is not increased by births or immigration between marking and recapture.

l Marked and unmarked individuals die and emigrate at the same rates.

l No marks are lost.

Although real populations rarely meet ail these assumptions, mark and recapture estimates of population size are often the best estimates available.

Whale populations have been studied using mark and recapture techniques for some time. In the early days of whale population studies, population biologists marked whales by shooting a numbered metal dart into their blubber with a modified shotgun. The idea was that the dart would be recovered when marked whales were caught and processed during whaling operations. However, the accuracy of this method was limited by several factors. First, it is difficult to mark a free-swimming whale from a moving boat on the open sea, and so biologists never knew exactly how many whales shot at were actually marked. Second, the recovery of darts during processing was poor. It is easy to overlook a relatively small dart on a huge whale. Experiments showed that Japanese whalers recovered 60% to 70% of marks from whales known to be marked, while other whaling fleets recovered an even lower proportion. Still, the greatest limitation of this early mark and recapture technique is that it requires killing whales during the recapture phase, which is unacceptable when studying protected or endangered species,

Refined mark and recapture methods do not require artificially marking or capturing whales. In the "marking" phase of newer procedures, a whale is photographed and its distinguishing marks are identified. These photographs, along with information such as where the photograph was taken and whether the whale was accompanied by an offspring, are catalogued for future reference. In the "recapture" phase the whale is photographed at a later date and identified from previous photos. This method is called photoidentification.

For more than two decades, Steven Katona (1989) has used photoidentification to study die humpback whales, Megaptera novaeangliae, of the North Atlantic (fig. 9.24). Humpback whales are particularly rich in individual marks, especially on the tail or flukes, This is convenient for photographic studies because humpback whales generally raise their flukes above the water before they dive. This behavior, called "fluking," exposes the flukes to the photographer and reveals potentially unique markings (fig. 9.25).

FIGURE 9.24 A humpback whale, Megaptera novaeangliac.

FIGURE 9.25 Unique markings identify individual humpback whales. A humpback whale called "Siphon." #700, photographed in Frenchman Bay, Maine' (a) in 1995 and (b) in 1993.

Katona points out that the unique markings on a humpback whale's flukes result from a combination of genetics and accidents. In humpback whales, fluke pigmentation ranges from completely black to white. This variation in pigmentation probably reflects genetic differences between individuals. Injuries often produce sears that superimpose other marks on the basic pigmentation of the flukes. Injuries may be the result of fighting between humpback whales, attacks by sharks, or attachment by parasites. The sears produced when these injuries heal create black marks on white flukes and white marks on black flukes. Using photographs of these marks, Katona and his colleagues have produced the North Atlantic Humpback Catalog, which includes photographs of more than 4,000 individual whales. The photographs included in the catalog, along with information on where each photograph was taken, whether the whale was accompanied by an

offspring, and other available observations, are curated for future reference. This photographic record is an invaluable source of information for determining the migration mutes, feeding grounds, breeding grounds, and size of the North Atlantic humpback whale population (fig. 9.26).

FIGURE 9.26 Photo identification and the North Atlantic humpback whale population.

From 1979 to 1986, Scott Baker, Janice Straley, and Anjanette Perry (1992) photographed and identified 257 humpback whales along the coast of southeastern Alaska. In one part of their study the researchers used photoidentification to estimate the number of humpback whales in Frederick Sound, Alaska. In their first sampling period, from July 31 to August 3, 1986, the team photographed and identified 72 humpback whales. In a second sampling period, from August 29 to September 1. 1986, they photographed and identified 78 humpback whales. Of the 78 whales photographed in the second sampling period, 56 were photographed for the first time, while 22 had also been photographed during the first sampling period. These 22 whales were the "recaptures." We can use these data and the corrected Lincoln-Peterson index to estimate the total number of whales in Frederick Sound from August 29 to September 1, 1986:

N=M(n+l)/m+l=72(78+l)/22+l=247

In other words, Baker and his colleagues estimated that there were 247 humpback whales in Fredrick Sound during the time of their study. Population estimates such as this are very important for monitoring the state of populations. In addition, photographic studies provide information on movements, calving intervals, and survival because photoidentified whales can go on yielding information throughout their lives.

Population ecologists have now applied the photoidentification techniques to several whale species including gray, right, blue, fin, sei, and killer whales. For instance, by 1986, scientists had photographed about 200 of the 300 to 400 North Atlantic right whales remaining in the Atlantic. From the growing photographic record of the North Atlantic right whale population, ecologists have estimated a 4- to 7-year calving interval for the population. This long period between offspring alone gives a clue to why this population is so vulnerable to extinction in the face of whaling pressure. In another study, population ecologists photographed and identified the entire population of 325 killer whales in Puget Sound and around Vancouver Island. revealing information about births, deaths, and the size of the population. An advance in this research approach is the use of computerized image analysis to help identify and match photos of whales. While not providing all the information necessary for conserving and managing whale populations, photographic studies are clearly making an important contribution.

Though it may be more challenging physically, the process of counting whales is much like counting many other kinds of animals such as humans, lynxes, trout, or ladybird beetles. However, ecologists must use different methods to estimate the abundance of organisms that have a more variable growth form or differ greatly in size. As we shall see in the next example, this is particularly true when the relative abundances of very different organisms are compared.

The Relative Abundance of Corals, Algae, and Sponges

The reefs along the north coast of Jamaica were once dominated by corals. Thickets of staghorn coral rose from the seafloor like marine bramble bushes, and elkhorn coral grew in abundance in the surging waves. Then dramatic change came in 1980 with Hurricane Allen, which generated waves large enough to flatten the staghorn coral thickets and dislodge elkhorn corals. Most of the branching corals in shallow water were reduced to rubble. However, Hurricane Allen and its devastation was not the only problem. The reefs seemed to he changing even at depths below 25 m, where there was little hurricane damage. Assessing the extent and nature of

changes on the reef would require detailed population studies.

Fortunately, Terence Hughes (1996) had started long-term studies of coral populations near Discovery Bay, Jamaica, in 1977, 3 years before Hurricane Allen. One of his goals was to document and understand apparent shifts in dominance from corals to algae. He was also concerned with documenting possible changes in sponge populations. But how can the relative abundance of organisms so different in size and growth form he estimated? A coral colony may cover several square meters or just a few square centimeters. Sponges also differ greatly in size. Algae of several species may grow together in a tangled mat covering several square meters or as a few isolated individuals. Ecologists studying terrestrial plants encounter similar size differences among plants of different ages and species, in the face of this variation, ecologists resort to measures of abundance that take into account differences in size. For instance, ecologists studying shrubs, herbaceous vegetation, or marine organisms such as corals, algae, and sponges often measure coverage, the area of landscape or reef covered by a species.

Hughes estimated percent cover by corals, algae, and sponges on his study reef nearly every year from 1977 to 1993. He made his estimates from photographs of 12 study plots I m² in size taken from a standard distance using slide film. He then mapped the positions and sizes of all coral and sponge colonies within the quadrats. He used a computer pro- gram to measure the areas on his maps that were covered by corals and sponges and then converted these measurements of absolute area to percent cover. Hughes estimated percent cover of algae by projecting the slide images of his study plots on a screen and superimposing a uniform grid of points on the image. The grid contained 100 points per square meter. The percentage of these points contacting algae in the image gave him an estimate of percent algal cover.

Hughes' 16-year study shows clear changes in the abundances of corals and algae (fig. 9.27). During the study, algal cover increased 10-fold from 7% to 76%. At the same time, coral cover decreased from about 48% to 13%, while sponge populations remained fairly constant. Verifying the status of populations such as these is one of the most basic aspects of ecological research. Such measurements are the first step toward identifying the factors that determine the distribution and abundance of organisms. With his photographs Hughes was able to show that this shift from a coral-dominated reef to one dominated by algae was due to increased mortality of coral colonies and reduced recruitment of new corals to the population. These are aspects of population dynamics that we cover in chapter 10.

FIGURE 9.27 Estimating abundance as percent cover: corals, sponges. and algae (data from Hughes 1996).

SUMMARY CONCEPTS

Ecologists define a population as a group of individuals of a single species inhabiting an area delimited by natural or human-imposed boundaries. Population studies hold the key to solving practical problems such as saving endangered species, controlling pest populations, or managing fish and game populations. All populations share a number of characteristics. Chapter 9 focused on two population characteristics: distribution and abundance.

While there are few environments on earth without life, no single species can tolerate the full range of earth's environments. Because all species find some environments too warm, too cold, too saline, and so forth, the physical environment limits the geographic distribution of species. For instance, there is a close relationship between climate and the distributions of the three largest kangaroos in Australia. The tiger beetle Cicindela longilabris is limited to cool boreal and mountain environments. Large- and small-scale variation in temperature and moisture limits the distributions of certain desert plants, such as shrubs in the genus Encelia. However, differences in the physical environment only partially explain the distributions of barnacles within the marine intertidal zone, a reminder that biological factors constitute an important part of an organism's environment.

On small scales, individuals within populations are distributed in patterns that may be random, regular, or clumped. Patterns of distribution can be produced by the social interactions within populations, by the structure of the physical environment, or by a combination of the two. Social organisms tend to be clumped; territorial organisms tend to be regularly spaced. An environment in which resources are patchy also fosters clumped distributions. Aggressive species of stingless bees live in regularly distributed colonies, while the colonies of nonaggressive species are randomly distributed. The distribution of creosote bushes changes as they grow. On larger scales, individuals within a population are dumped. In North America, populations of both wintering and breeding birds are concentrated m a few hot spots of high population density. Clumped distributions are also shown by plant populations living along steep environmental gradients on mountainsides.

Population density declines with increasing organism size. In general, animal population density declines with increasing body size. This negative relationship holds for animals as varied as terrestrial invertebrates, aquatic invertebrates, birds, poikilothermic vertebrates, and herbivorous mammals. Plant population density also decreases with increasing plant size. However, the biological details underlying the size--density relationship shown by plants are quite different from those underlying the size--density patterns shown by animals. A single species of tree can span a very large range of sizes and densities during its life cycle. The largest trees start life as small seedlings that can live at very high population densities. As trees grow, their population density declines progressively until the mature trees live at low densities.

Rarity is influenced by geographic range, habitat tolerance, and population size. Rarity of species can be expressed as a combination of extensive versus restricted geographic range, broad versus narrow habitat tolerance, and large versus small population size. The most abundant species and those least threatened by extinction combine large geographic ranges, wide habitat tolerance, and high local population density. All other combinations of geographic range, habitat tolerance, and population size include one or more attributes of rarity. Rare species are vulnerable to extinction. Populations that combine restricted geographic range with narrow habitat tolerance and small population size are the rarest of the rare and are usually the organisms most vulnerable to extinction.

The abundance of organisms and how abundance changes in time and space are among the most fundamental concerns of ecology. To estimate the abundance of species the ecologist must contend with a variety of practical challenges and conceptual subtleties. Mark and recapture methods are useful in the study of populations of active, elusive, or secretive animals. Mark and recapture techniques, which use natural distinguishing marks, are making an important contribution to the study of populations of endangered whales. Ecologists studying organisms, such as corals, algae, and sponges or many types of terrestrial plants, that differ a great deal in size and form often estimate abundance as coverage, the area covered by a species. Patterns of distribution and abundance are ultimately determined by underlying population dynamics.

REVIEW QUESTIONS

1. What confines Encelia farinosa to upland slopes in the Mojave Desert? Why is it uncommon along desert washes, where it would have access to much more water? What may allow E. frutescens to persist along desert washes while E. farinosa cannot?

2. Spruce trees, members of the genus Picea. occur throughout the boreal forest and on mountains farther south, For example, spruce grow in the Rocky Mountains south from the heart of boreal forest all the way to the deserts of the southern United States and Mexico. How do you think they would be distributed in the mountains that rise from the southern deserts? In particular, bow do altitude and aspect (see chapter 4) affect their distributions in the southern part of their range? Would spruce populations he broken up into small local populations in the southern or the northern part of the range? Why?

3. What kinds of interactions within an animal population lead to clumped distributions? What kinds of interactions foster a regular distribution? What kinds of interactions would you expect to find within an animal population distributed in a random pattern?

4. How might the structure of the environment, for example, the distributions of different soil types and soil moisture, affect the patterns of distribution in plant populations? How should interactions among plants affect their distributions?

5. Suppose one plant reproduces almost entirely from seeds, and that its seeds are dispersed by wind. and a second plant reproduces asexually, mainly by budding from runners. How should these two different reproductive modes affect local patterns of distribution seen in populations of the two species?

6. Suppose that in the near future, the fish crow population in North America declines because of habitat destruction. Now that you have reviewed the large-scale distribution and abundance of the fish crow (see fig. 9.15b), devise a conservation plan for the species that includes establishing protected refuges for the species. Where would you locate the refuges? How many refuges would you recommend?

7. Use the empirical relationship between size and population density observed in the studies by Damuth (1981) (see fig. 9.19) and Peters and Wassenberg (1983) (see fig. 9.20) to answer the following: For a given body size, which generally has the higher population density, birds or mammals? On average. which lives at lower population densities, terrestrial or aquatic invertebrates? Does an herbivorous mammal twice the size of another have on average one-half the population density of the smaller species? Less than half? More than half?

8. Outline Rahinowitz's classification (1981) of rarity, which she based on size of geographic range, breadth of habitat tolerance, and population size. In her scheme, which combination of attributes makes a species least vulnerable to extinction? Which combination makes a species the most vulnerable?

9. Can the analyses by Damuth (1981) and by Peters and Wassenberg (1983) be combined with that of Rabinowitz (1981) to make predictions about the relationship of animal size to its relative rarity? What two attributes of rarity, as defined by Rabinowitz, are not included in the analyses by Damuth and by Peters and Wassenberg?

10. Suppose you have photoidantified 30 humpback whales around the island of Oahu in one cruise around the island. Two weeks later you return to the same area and photograph all the whales you encounter. On the second trip yon photograph a total of 50 whales, of which 10 were photographed previously. Use the Lincoln-Peterson index with the Bailey correction to estimate the number of humpback whales around Oahu during your study.

SUGGESTED READINGS

Caughley, G., J. Short, G. C. Gfigg, and H. Nix. 1987. Kangaroos and climate: an analysis of distribution. Journal of Animal Ecology 56:751-61.

Ehleringer, J. R. and C. Clark. 1988. Evolution and adaptation in Encelia (Asteraceae). In L. D. Gottlieb and S. K. Jain., eds. Plant Evolutionary Biology. London: Chapman and Hall. These two papers provide good introductions to climate and the distributions of species within an animal genus and within a plant genus.

Bfissou, J. and J. F. Reynolds. 1994. The effects of neighbors on root distribution in a creosote bush (Larrea tridentota) population. Ecology 75:1693-702.

The paper by Brisson and Reynolds demonstrates extended studies of creosote bush distributions belowground.

Phillips, D. L. and J. A. MacMahon. 1981. Competition and spacing patterns in desert shrubs. Journal of Ecology 69:97-115.

The paper by Phillips and MacMahon gives an excellent summary of the history and apparent resolution of a controversy surrounding distributions of creosote bush.

Brown, J. H., D. W. Mehlman, and G. C. Stevens. 1995. Spatial variation in abundance. Ecology 76:2028-43.

Root, T. 1988. Atlas of Wintering North American Birds. Chicago: University of Chicago Press. These two references provide excellent entries into the area of large-scale distribution patterns in bird populations. These are pioneering efforts.

Damuth, J. 1981. Population density and body size in mammals. Nature 290:699-700.

Peters, R. H. and K. Wassenberg. 1983. The effect of body size on animal abundance. Oecologia 60:89-96.

These are benchmark papers on the relationship between animal size and population density.

Rabinowitz, D., S. Cairns. and T. Dillon. 1986. Seven forms of rarity and their frequency in the flora of the British Isles. In M. E. Sonic. ed. Conservation Biology: The Science of Scarcity and Diversity. Sunderland, Mass.: Sinauer Associates.

This paper provides an introduction and application of the concept of rarity developed by Deborah Rabinowitz.

Baker. C. S., J. M. Straley, and A. Perry. 1992. Population characteristics of individually identified humpback whales in southeastern Alaska: summer and fall 1986. Fishery Bulletin 90:429--37.

Katona, S.K. 1989. Getting to know you. Oceanus 32:37-44.

These papers provide detailed accounts of using photoidentification to study humpback whale populations.

ON THE NET

Visit our website at http://www, mhhe.com/ecology for links to the following topics:

Animal Population Ecology

Population Density of Animals

Biodiversity

Endangered Species

Legislation Regarding Endangered Species