Jessica Gurevitch, Samuel M. Scheiner, and Gordon A. Fox - The Ecology of Plants - 2002 / The Ecology of Plants Jessica Gurevitch, Samuel M. Scheiner, and Gordon A. Fox; 2002 / Ch 11

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vores can eat (or manipulate) only some of the parts of a plant, damaging, removing, or destroying those parts, but not necessarily immediately killing the plant. Deer, for example, frequently restrict their consumption to only the newest leaves or parts of shoots. Herbivores can also live on or within a plant and consume some of the plant’s resources. Insects called aphids, for example, extract dissolved sugars and other nutrients directly from the phloem; pathogenic microorganisms can parasitize a plant, depleting its resources over time. Some plants are parasites on other plants, tapping water, sugars, proteins, and other resources for their own use.

The effects of herbivory on the plant depend, among other things, on what parts of the plant are consumed. Removal of or damage to roots can reduce or prevent the plant’s uptake of water and mineral nutrients and can make the plant more vulnerable to being toppled by wind, flooding, or soil erosion. Consumption of leaves reduces the photosynthetic surface area, while removal of phloem sap may reduce the energy and materials available for growth and reproduction. Consumption of leaves, stems, and twigs may alter the competitive relationships among neighboring plants. Removal of meristems may alter the growth form of the plant. Consumption of flowers, fruits, and seeds may reduce the potential contribution of the plant to the next generation. Of course, to the new individual in each seed, consumption means death. Alternatively, fruits are often consumed without damage to the seeds, in which case the frugivore may disperse the seeds to potentially favorable locations.

Also important is the life history stage at which the plant is attacked or damaged. Seedlings are particularly vulnerable to herbivores. One mouthful for the herbivore can kill a seedling, but hardly affect a more mature plant. Grazing on grasses that have just begun to flower can critically affect their ability to produce seeds, whereas heavier grazing after seeds have been shed may have less of an effect on population dynamics.

How much do herbivores eat, on average? It has been estimated that about 10% of the leaves of forest trees are lost every year to herbivores (Coley and Barone 1996). Herbivory is greatest in dry tropical forests, somewhat less in tropical rainforests, and least in temperate forests. Young leaves tend to be eaten more readily than mature leaves in the Tropics. As you might expect, there is tremendous variation among species, locations, and years in the degree of damage caused by herbivores.

Can herbivory ever actually help plants to grow or reproduce? In the 1980s and early 1990s, a group of scientists postulated the existence of overcompensation, in which plants purportedly respond to herbivory by growing more (McNaughton 1983). (If a plant’s hypothesized extra growth in response to herbivory resulted in no net difference between grazed and ungrazed

individuals, it would be called compensation.) The researchers suggested that overcompensation was due to the coevolution of plants and herbivores, particularly grasses and mammalian herbivores. Buffalo saliva and urine, for example, were thought to contain growth stimulants for grasses (Detling et al. 1980). These ideas were highly controversial and received a great deal of attention; it seemed difficult for many ecologists to believe that being eaten could actually be a good thing for plants.

While there was some experimental evidence for these ideas, when taken as a whole, they were not well supported by the available data (Belsky 1986; Belsky et al. 1993). One of the possible explanations for reported overcompensation was that researchers had measured only aboveground plant parts, while underground reserves may have been depleted to stimulate the observed aboveground growth. Long-term herbivory might result in significant depletion of these underground reserves, ultimately harming the ability of the plant to recover from subsequent bouts of herbivory. Another explanation was that in dense plant stands, if herbivores eat only shaded, unproductive understory leaves, there may indeed be no reduction in the photosynthetic capacity of the plant, and thus no negative effects of herbivory. Joy Belsky and her associates (Belsky et al. 1993) argued that overcompensation seemed to occur mainly in the experimental treatments most favorable to plant growth, such as the combination of high nutrient availability and reduced competition.

Ecologists now generally believe that herbivory usually harms individual plants (Hawkes and Sullivan 2001). While there are cases of overcompensation, on average, herbivory reduces both growth and reproductive output, resource addition increases both, and there is no evidence of an interaction between the two effects (Figure 11.1). One interesting observation is that plant responses to herbivory depend to some degree on their growth forms and phylogenies: for example, monocots with basal meristems (such as grasses) have more regrowth after herbivory under high-resource conditions, while dicot herbs and woody plants regrow more after herbivory under lowresource conditions. Unfortunately, most studies have used only short-term measures of plant response to herbivory, not measures of lifetime fitness.

Herbivory and Plant Populations

The extent to which herbivores affect plant population dynamics is a highly controversial and unresolved question. Two different explanations have been put forward for why herbivores should not be important. The “top-down” school of thought argues that herbivores are maintained at such low densities by their own predators that they rarely exert negative effects on

Figure 11.1

The effect of herbivory on both growth and reproduction is generally negative. The graph shows the average effects on growth in 82 studies and reproduction in 24. The response ratio is the plant performance when subjected to herbivory or treated with resources divided by plant performance without additional resources or herbivory; error bars are 95% confidence intervals. A negative ratio means that the treatment decreased plant performance, while a positive value indicates increased performance. Resource addition improved plant performance, but there is no evidence of an interaction between resource addition and herbivory. (After Hawkes and Sullivan 2001.)

plant populations (e.g., Strong et al. 1984). The “bot- tom-up” school argues that plant populations are limited by abiotic factors such as water, light, and soil nutrients, not by herbivores (Hairston et al. 1960; Slobodkin et al. 1967; Hairston and Hairston 1993).

In contrast, others have argued that herbivores do play an important role in controlling plant populations. In all likelihood, herbivory regulates plant population dynamics in some cases, while “top-down” or “bottomup” processes dominate in others. More work is needed to determine not only under what circumstances each of these processes is important, but also what factors lead to the predominance of one kind of regulatory process over others, and when their interaction becomes important.

One of the most obvious situations in which plant populations are dramatically affected by herbivores is the killing of large stands of forest trees by insects. Outbreaks of lepidopteran larvae can cause massive defoliation, in some instances resulting in tree mortality. Repeated defoliation of oaks in the northeastern and midwestern United States by gypsy moths has caused die-offs of large numbers of trees (Davidson et al. 1999). Trees in more mesic areas appear to be more likely to die from a single episode of gypsy moth defoliation than those in more xeric sites.

Bark beetles (family Scolytidae) are an important cause of conifer mortality in western North America and

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the southeastern United States (Figure 11.2; Powers et al. 1999). While most bark beetles inhabit branches and trunks of trees already undergoing stress, such as those damaged by a lightning strike, some species attack and kill healthy trees. The beetles enter the tree by chewing a hole through the bark into the cambium, the actively growing layer under the bark, and lay their eggs there. After hatching, the larvae feed on the cambium, destroying it and the vascular tissue. Coniferous trees (particularly pines) usually respond to boring by oozing sap (also called pitch) into the wound, thus either suffocating the beetle or pushing it out of the hole. However, a massive attack by a large number of beetles appears to reduce the ability of the tree to “pitch out” the beetles. Stresses created by drought or injury may have the same effect in making trees more vulnerable.

Figure 11.2

A “ghost forest” of Pinus albicaulis (whitebark pine, Pinaceae) killed by Dendroctonus ponderosae (mountain pine beetle, Scolytidae) in an extensive outbreak during the late 1920s. The young trees growing on this site are mainly Abies lasiocarpa (subalpine fir, Pinaceae) and Picea engelmannii

(Engelmann spruce, Pinaceae). Scolytid beetles cause extensive damage to conifers in western and southeastern North America. (Photograph courtesy of K. Kipfmueller.)

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Bark beetles that are responsible for widespread tree mortality in North America include the Mexican bark beetle, the western pine beetle, the spruce beetle, the western balsam bark beetle, and the southern pine beetle. As their names suggest, bark beetles are fairly selective, generally specializing on one or a few species of conifers. The southern pine beetle, for example, primarily attacks Pinus echinata (shortleaf pine, Pinaceae), P. taeda (loblolly pine), P. palustris (longleaf pine), and P. elliottii (slash pine); the spruce beetle kills spruces. The beetles function with symbiotic fungal partners that also attack the trees, eliciting specific biochemical responses from their plant targets. We return to the effects of these fungal symbionts of bark beetles later in this chapter.

Chronic herbivory—herbivory that occurs over long time periods—can have large effects on plant demography. Pinus edulis (pinyon pine) trees subjected to chronic herbivory have reduced rates of growth, an altered shape, and produce male cones almost exclusively (Whitham and Mopper 1985). In a study of Eucalyptus in subalpine habitats in the Snowy Mountains of Australia, Patrice Morrow and Valmore LaMarche (1978) found that trees treated with insecticide experienced large increases in growth. Given the growth history of trees on that site, they concluded that growth was suppressed by chronic herbivory. These results imply that chronic herbivory can greatly reduce lifetime fitness. By spraying insecticides on experimental plants several times a year, Waloff and Richards (1977) showed that chronic herbivory reduced the seed yield of the British shrub Sarothamnus scoparius (broom, Fabaceae) by about 75% over 10 years. Similarly, in a study of the semelparous plant Cirsium canescens (Platte thistle, Asteraceae; see Figure 9.5), Svata Louda and Martha Potvin (1995) excluded inflorescence-feeding herbivores from exper-

imental plants, which led to increases in the total number of seeds set, seedling density, and the number of flowering adults.

Herbivory and Spatial Distribution of Plants

The spatial distribution of plants can also be affected, or even determined, by herbivores. The role of granivorous rodents in the distribution of a range grass with large, nutritious seeds, Achnatherum hymenoides (Indian ricegrass, Poaceae), was studied in the desert of western Nevada. Indian ricegrass is common in sandy soils, but rare in adjacent rocky habitats (Breck and Jenkins 1997). The grass was able to survive and grow in both soil types when planted experimentally, although the plants grew taller on the sandy soils. However, rodents cached seeds only in the sandy areas, and this seed dispersal behavior appears to be an important factor in determining the distribution of this plant.

The distribution of the shrub Haplopappus squarrosus (yellow squirrel cover, Asteraceae) in California is strongly affected by granivory. Louda (1982) showed that H. squarrosus was most abundant in an inland transitional zone between coastal and interior climates, but produced more seeds closer to the ocean (Figure 11.3). This pattern appears to be mainly a result of increased insect granivory on the plants growing closest to the ocean.

Donald Strong and his colleagues have unraveled a complex set of interactions that apparently underlie the population dynamics of a shrub, Lupinus arboreus (lupine, Fabaceae), along the central coast of California (Strong et al. 1995, 1996). Large patches of this woody perennial periodically die off and are eventually regenerated from seed, so that the population fluctuates over time. The plants are killed primarily by subterranean caterpillars of the ghost moth, Hepialus californicus, which

Figure 11.3

(A) Observed (bars) versus expected (dashed line) relative frequency of Haplopappus squarrosus (yellow squirrel cover, Asteraceae) over a climatic gradient in San Diego County, California. The observed distribution is based on the presence or absence of plants along 15,250 roadside segments,

each 167 meters in length. The expected frequency is derived by assuming that relative population size should be proportional to relative seed production. (B) Percentage of flower heads destroyed by insect granivores in each climate zone; error bars are 95% confidence intervals. (After Louda 1982.)

bore into the roots. However, an insect-killing nematode, Heterorhabditis hepialus, with its symbiotic bacterium, Photorhabdus luminescens, is a highly effective predator on the ghost moth caterpillars. Consequently, lupinedominated areas that are heavily colonized by the nematode are protected from attack by the caterpillar, while those areas without the nematode experience massive periodic die-offs. Few other studies have reported control of plant populations by underground herbivores, not to mention such trophic complexity, but then, few studies have looked for either.

Granivory

Granivory can also have important consequences for plant populations. In some populations, granivores consume a large fraction of the seeds. Tachigali versicolor (alazan, Fabaceae) is a monocarpic tree from Central America with unusually large (500–600 mg) seeds. In a detailed study of the seeds and seedlings produced by two large adult trees, Kaoru Kitajima and Carol Augspurger (1989) found that 51% to 83% of seeds died prior to germination, depending on the tree and the distance of the seed from the tree. The important granivores were bruchid beetles (eating 13% to 38% of seeds) and vertebrates (eating 0% to 59% of seeds). Seedlings had somewhat lower mortality rates in their first two months (24% to 47%, again depending on the tree and distance from the tree). Seedling mortality was primarily due to herbivory (6% to 17% of seedlings) and disease (3% to 25% of seedlings).

The chemical properties of seeds can deter or enhance granivory. Some seeds contain compounds that strongly deter granivores (we discuss such defensive compounds in more detail below). Seeds of Erythrina (coral bean trees, Fabaceae), for example, contain compounds that are strongly neurotoxic in vertebrates; as a result, they are rarely eaten. On the other hand, a study of squirrel granivory on oaks provided some surprises. Quercus rubra (red oak, Fagaceae) has high tannin concentrations in its acorns, while Q. alba (white oak) does not. One might expect that gray squirrels (Sciurus carolinensis) would prefer the acorns of white oaks. However, Peter Smallwood and Michael Steele (Smallwood et al. 2001; Steele et al. 2001) showed that the interaction is more complicated. Squirrels prefer to eat white oak acorns, but prefer to cache red oak acorns because the tannins protect them from fungi and bacteria, making them less perishable. Moreover, the squirrels often remove the embryos of the white oak acorns before caching them. Thus, more red oak than white oak seedlings emerge from squirrel caches, and the squirrels are more effective as dispersers of red oaks—not because the squirrels avoid the tannin-laden red oak acorns, but because they actively prefer them!

Many plants—especially woody plants—show large

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and erratic variation among years in the size of the seed crop produced, and this variation is generally synchronized among most of the plants in a population. This phenomenon, called masting, has been widely explained as an adaptation to granivory. Various ecologists have hypothesized that during masting years, the large numbers of seeds overwhelm the capacity of granivores to eat them all, allowing at least some seeds to survive. This explanation has been questioned recently by other ecologists, who argue that other factors may be more important in selection for masting. They argue that masting can more easily be explained as an adaptation to wind pollination, which is increasingly efficient at high pollen densities (Smith et al. 1990; Kelly et al. 2001).

In a large survey of studies on variation in seed production, Carlos Herrera and associates (Herrera et al. 1998) argued that the distinction between masting species and non-masting species is false because there is a continuum of variability. Most iteroparous woody plants have variable seed production. Even when phylogenetic relationships are controlled for, there is slightly more variability in wind-pollinated species than in animal-pollinated species. However, these researchers also found more year-to-year variation in species dispersed by granivores or abiotic mechanisms (such as wind or water) than in those dispersed by frugivores. It seems clear that more studies are needed to assess the importance of pollination and granivore satiation in among-year variability in seed production.

Biological Control

Biological control is the deliberate use by humans of herbivores or pathogens to control populations of undesirable plant (or other) species. Many such biological control agents are introduced from other continents, and successful instances of biological control of plant pests offer examples of herbivores controlling plant populations. One well-known example is the introduction of the moth Cactoblastis cactorum to Australia to control the introduced and invasive prickly pear cacti Opuntia inermis and O. stricta (Cactaceae). The cacti had spread to cover vast areas in Australia, rendering them useless for sheep grazing (Figure 11.4). The moth was introduced in 1925 from Argentina, where its caterpillars were found to be specialist herbivores on prickly pears. By 1935, the prickly pear populations had been decimated, and they have remained at low levels since that time.

Unfortunately, the success of Cactoblastis in Australia is colored by recent problems with this species in North America. C. cactorum was introduced to the Caribbean in 1957 to control Opuntia species that had spread due to overgrazing. Subsequently, the moths invaded Florida and are now spreading rapidly in the southeastern United States, where they are affecting several endangered Opuntia species (Johnson and Stiling 1998). There

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(A)

Figure 11.4

(A) A dense stand of Opuntia in Queensland, Australia, prior to the release of Cactoblastis. (B) The same stand three years later. (Photographs by A. P. Dodd and the Commonwealth Prickly Pear Board.)

is much concern that this invasion will spread to the southwestern United States and Mexico. Opuntia species are ecologically important in both countries, and are also economically important in Mexico.

A recent example of a similar phenomenon has been the introduction of several specialist insects to control purple loosestrife (Lythrum salicaria), an introduced, highly invasive species that now dominates vast areas of wetlands in eastern and central North America (see Figure 14.3). Bernd Blossey and his colleagues found that purple loosestrife was attacked by many different insects in central Europe, where it is native. These researchers imported populations of a root-mining weevil (Hylobius transversovittatus) and two leaf-feeding chrysomelid beetles (Galerucella calmariensis and G. pusilla) and released them in the United States and Canada in 1992 and 1993 (Blossey et al. 2001). These and other host-specific insects released later appear to be successfully eliminating the dense populations of purple loosestrife without attacking other species, allowing the recolonization of native wetland plants in areas where purple loosestrife had maintained monospecific stands. Purple loosestrife may be limited by herbivores in its native habitat. In Europe, it never reaches more than 5% cover and remains a minor component of wetland vegetation, in dramatic contrast to its spread in North America when it was introduced without specialist herbivores.

An important question, however, is the extent to which these and other biological control agents may affect nontarget species. The control agents released for purple loosestrife were characterized as “specialists” because

(B)

they prefer L. salicaria to related native North American species. However, these insects feed on native species when there is little purple loosestrife available, creating a potential for negative effects on the native species.

An agent introduced to control the severely invasive exotic plant Carduus nutans (musk thistle, Asteraceae) and its relatives in the midwestern United States has proved to have serious negative effects on rare native thistles. Rhinocyllus conicus (flowerhead weevil) was introduced to control Carduus species after studies indicated that this weevil prefers Carduus to native thistles of the genera Cirsium, Silybum, and Onopordum.

However, despite this preference for the invasive musk thistle, studies by Louda and her associates (Louda et al. 1997) showed that the weevil is also consuming, and is negatively affecting, three native thistle species—Cir- sium canescens, C. centaureae, and C. undulatum. Observed levels of R. conicus infestation were as great or greater on the native thistles than on the exotic thistles, and were also greater than the levels of native insect infestation on the native thistles. As a result, infested plants set many fewer seeds. In the case of C. canescens, which is already uncommon and restricted in habitat, this new herbivore may present a danger to population persistence, as reduction in seed production is expected to reduce the population growth rate of this species (Louda et al. 1997). The best protection for the native C. canescens may be the maintenance of the invasive Carduus populations in the same habitat to attract the weevils away from the native thistle—thus the original target species may act as sort of a biological control agent for the weevils!

These studies, together with other recent empirical studies (Henneman and Memmott 2001), have caused many biologists to begin reconsidering the safety of biological control in general (Simberloff and Stiling 1996).

While biological control has proved strikingly successful in cases such as that of Opuntia in Australia, its strong point—the fact that the control agents disperse and reproduce on their own—is also what makes it potentially risky.

Effects of Herbivory

at the Community Level

Consequences of Herbivore Behavior

Herbivores show preferences and exhibit behavior with respect to what they eat and how and when they eat it. Their behavior can have profound consequences for species richness and abundance. One important way in which herbivore behavior can affect plant community composition is the extent to which animals behave as generalists versus specialists with regard to what they eat. At one extreme, a pure generalist herbivore eats plants in the same proportions at which they are present in the community. At the other extreme, a pure specialist herbivore eats only plants (or even only specific plant parts) belonging to a single species or to a small group of closely related species. Extreme specialists are the most desirable choices for biological control agents to minimize effects on nontarget species.

Most herbivores are somewhere between these two extremes, preferring certain foods to others, but able to eat a variety of plants. Thus, it is misleading to strictly contrast specialists and generalists. However, it is often believed that generalist herbivores tend to promote or maintain species diversity because they keep faster-growing, dominant species from outcompeting

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others. The effects of specialists, on the other hand, depend on the roles that their preferred food species play in the community. It is likely that a specialist on a potentially dominant species will have a very different effect on the community than a specialist on a less common species. Thus, herbivory can either increase or decrease the diversity of the plant community. The outcome depends not only on patterns of consumption, but also on interactions between herbivory, plant competition, and abiotic factors such as soil moisture, nutrients, and light levels. The effects of herbivory can vary over spatial scales and over the course of time.

Nancy Huntly (1987) studied the foraging behavior of pikas and the consequences of their foraging for the plant community. The pika, a small, territorial relative of rabbits and a strong contender for the world’s cutest mammal, lives on high-altitude, rocky talus slopes in western North America. Pikas forage outward from their dens. They are generalists, but prefer certain plant foods to others. Pikas do not hibernate; instead, they collect large haypiles during the summer for winter use (Figure 11.5). Huntly experimentally excluded pikas from vegetation plots at different distances from their dens into the surrounding meadows. She found that the foraging animals had large effects on plant community composition close to their dens, where they spent the most time, with decreasing effects farther away.

Introduced and Domesticated Herbivores

One of the classic stories in the ecology of herbivory is that of rabbits, chalk grassland vegetation, and a rabbit disease, myxomatosis. Chalk grasslands are highly

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diverse plant communities found on limestone-derived soils in southern England. These grasslands alternate with woodlands, and they have been used for centuries to graze sheep and, beginning in the twentieth century, cattle. Rabbits were brought to England in medieval times as a source of food and for sport hunting, where they, well, bred like rabbits. They became widespread, attaining very high numbers after about 1850, undoubtedly due to direct and indirect human influences, including predator reduction. Rabbit densities varied greatly from one spot to another.

What effects have the rabbits had on the vegetation of the chalk grasslands? The father of modern experimental plant ecology, Arthur Tansley, observed that where rabbit populations were high, the turf was typically chewed down to a height of 1 to 2 centimeters, while that of sheep-grazed grasslands was typically 5 to 10 centimeters in height. He hypothesized that if sheep grazing and rabbit feeding were prevented, the grasslands would revert to forest. Tansley experimentally fenced plots of vegetation to

exclude rabbits and sheep (Tansley and Adamson 1925). At first, there was a great increase in the growth of plants inside the exclosures, and many plants flowered abundantly inside the exclosures that never succeeded in reproducing outside the fences. After some time, however, perennial grasses, the preferred food of the rabbits, grew up and shaded shorter dicot species. Total biomass and average vegetation height increased substantially. The palatable grasses became more dominant, while less

competitive plant species declined in abundance, but did not disappear altogether. In addition, plants not characteristically found in the chalk grasslands invaded some of the ungrazed areas. However, the predicted largescale colonization by woody species did not occur, perhaps because the exclosures were too small or too far away from sources of tree seeds.

This experiment was repeated unintentionally on a larger scale some 30 years later, when a viral rabbit disease, myxomatosis, was accidentally introduced into Great Britain and nearly wiped out rabbit populations in the chalk grasslands and elsewhere. Immediately following the decimation of the rabbit population in 1954, many rare plant species were found in the chalk grasslands that had not been seen in years (Thomas 1960, 1963). These species had been selectively grazed by rabbits, never becoming large enough to flower and be noticed, or had been grazed as soon as they grew past the seedling stage. Various rare orchids and other showy species, such as Helianthemum chamaecistus (frostweed, Cistaceae) and Primula veris (primrose, Primulaceae), appeared and flowered in abundance. Some of these species had been common a hundred years before, prior to the great increase in rabbits. Other species decreased as the rabbits disappeared, either because they were outcompeted or because they had been favored by the nitrogen from the rabbits’ urine. Tall grasses began to become more prominent, and woody species began to invade. When the rabbit populations recovered from the epidemic of myxomatosis in the early 1960s, the vegetation largely reverted to its previous state.

Striking pictures of the effects of grazing are offered by fence lines where one side is heavily grazed and the other ungrazed or lightly grazed (Figure 11.6). Like pikas, cattle are selective generalists, eating many

species, preferring some, and avoiding others. They usually avoid woody and spiny species, as well as those with toxic or noxious defensive chemicals. Cattle can poison themselves, for example, by grazing on species such as Digitalis (foxglove, Scrophulariaceae; see Figure 9.1) and Astragalus (locoweed, Fabaceae). Cattle can have dramatic effects on community composition as a result of grazing, particularly when their densities are high or when grazing occurs at particularly sensitive times of the year for plant recovery and regeneration (e.g., when grass seeds are ripening). Over time, particularly with heavy grazing, preferred plants such as palatable and nutritious grasses decline in abundance and are replaced by less edible species, drastically changing the composition and appearance of the plant community. Heavy overgrazing leads to bare patches of ground, weed invasion, and severe erosion, especially on slopes. The very landscape can be changed, with deep ravines and gullies replacing rolling, grass-covered slopes, as a result of long-term damage to the plants that once held the soil in place. These problems tend to be more severe in arid environments, but can occur even in mesic habitats. Other grazing animals, including sheep and goats, can cause similar effects. Problems caused by overgrazing are widespread in western North America, but also occur in Africa, the Mediterranean region, and Australia, among other places. Overgrazing by domestic animals has contributed to turning vast areas of grassland into shrublands or deserts.

Effects of Native Herbivores

Seed-eating and vegetation-eating small mammals have been shown to affect plant community structure in a number of arid environments. In the semiarid shrubland of northern Chile, Javier Gutiérrez and his colleagues used fences and netting to selectively exclude small mammals (principally the herbivorous degu, Octodon degus; Figure 11.7) and predatory birds (particularly owls) from large plots (Gutiérrez et al. 1997). The exclusion of degus resulted in an increase in the cover of shrubs and perennial grasses, an increase in the diversity of perennial species, and a decrease in annual plant cover. The researchers found some indirect effects of predator exclusion on the vegetation (presumably by allowing increases in herbivores), and they also documented strong effects of weather as well as interactions between weather and herbivore effects.

Interestingly, while the arid and semiarid vegetation of Chile and Argentina is primarily home to herbivorous and insectivorous species, with few granivores, seed-eat- ing rodents dominate North American deserts. James Brown and his colleagues have conducted a series of very long-term experiments to exclude different small mammals (particularly heteromyid rodents) and ants from plots in the Chihuahuan Desert of eastern Arizona

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Figure 11.7

The degu (Octodon degus) is a small rodent that is a principal herbivore in Chilean deserts. (Photograph courtesy of B. Lang.)

(Brown and Munger 1985; Brown et al. 1997). Over time, removing either rodents or ants caused substantial changes in plant species composition. Where rodents were removed, large-seeded species increased and small-seeded species decreased. Where ants were removed, the opposite results were found (Guo and Brown 1996).

Valerie Brown and her colleagues have carried out many innovative field experiments to investigate the effects of herbivores on plant communities. In one large study, they used insecticides to kill either aboveground or belowground insects in an early successional field in Great Britain (Brown and Gange 1992). The purpose of the experiment was to see how the effects of root-feed- ing insects on the plant community might differ from the effects of foliage feeders. They found that both aboveground and belowground herbivory by insects had major (but different) effects on the timing and direction of succession. In this field, the aboveground insects were largely sap-feeding Hemiptera, which preferred perennial grasses. Their herbivory suppressed perennial grass colonization, slowing succession. The removal of the insects led to a luxuriant growth of the grasses, which then shaded and replaced the lower-growing herbaceous dicots, leading to a steep decline in species richness. Underground, chewing insects in the Coleoptera and Diptera fed primarily on the roots of the dicots. Reducing belowground insect numbers led to the persistence of annual dicots and a great increase in colonization by perennial dicots, and consequently a great increase in species richness. The ordinary presence of these root-feeding insects thus speeds up succession by reducing the dicots and increasing the colonization of the field by grasses.

Herbivory is not the only way in which plant-eating animals affect plant communities. Other kinds of herbivore behavior can also change the environment and

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have strong effects on plant communities. Mammalian herbivores, in particular, create gaps and patches when making burrows and trails, and trample vegetation around available water sources. Domesticated cattle herds can cause severe damage to vegetation along streams and watercourses by repeated trampling. Elephants consume and trample enormous amounts of plant material. Tree canopy cover in Serengeti National Park in Kenya, for example, was reduced by about 50% by elephants (Pellew 1983).

Not all such effects of herbivores are negative. In tallgrass prairies in the midwestern United States, native bison (see Figure 1.2C) create depressions where they roll in the dust. In the spring these areas contain small temporary pools of water, and in the summer they are inhabited by annual species that otherwise would be excluded by perennial grasses (Collins and Uno 1983).

Large herbivores can also affect plant distributions and species richness through strong effects on soil nutrients caused by their urination and defecation. In a study at Yellowstone National Park, David Augustine and Douglas Frank (2001) compared soil characteristics and community characteristics between ungrazed grasslands and grasslands grazed by large herbivores—elk, bison, and pronghorn. Species richness and diversity were greater in the grazed grasslands, particularly at very small scales (Figure 11.8).

Even smaller animals can have dramatic effects, particularly when they reach very high numbers. Lesser snow geese breed on the coastal marshes of the tundra of Hudson Bay and James Bay in Canada during the summer, migrating in autumn to the Gulf Coast of Louisiana and Texas. Over the past 30 years their population has grown tremendously, with midwinter counts climbing from about 0.8 million in 1969 to about 3 million in 1994. Their winter and summer habitat use has expanded greatly, both in area and in the variety of habitats they occupy (Abraham and Jefferies 1997). Much of this population growth appears to be caused by the response of the geese to changes in land use by humans. Expansion of farmland and the use of crops as food sources by the geese, both during migration and on their wintering grounds, have decreased overwinter adult mortality. Changes in predation rates may also be a factor. In summer, ever larger flocks of geese return each year to the tundra in excellent nutritional condition, capable of rearing large numbers of young. Snow geese are grazers; however, they are also capable of killing plants by pulling them up by their roots or rhizomes. Large flocks of the birds can have dramatic effects on the tundra landscape, not only changing plant species composition but also leaving entire areas bare of plants. It has been estimated that over a third of the tundra coastal marsh ecosystem has been severely overgrazed, threatening some 200 other species of water birds that summer

Figure 11.8

Plant species richness and plant species diversity, as measured by the Shannon-Weiner index (see Chapter 12), are greater in grazed than in ungrazed grasslands in Yellowstone National Park. The effect was greater for comparisons of 20 × 20-centimeter quadrats than for 4 × 4-meter quadrats, implying that the effects were occurring at a very small spatial scale. This scale effect was contrary to expectations because urination and defecation by large mammals is thought to lead to a very patchy distribution of soil nitrogen and nitrogen-mineralization rates. Species richness is the mean number of species per plot on the 20-centimeter scale, and the mean number of species per plot divided by 10 on the 4-meter scale. Error bars are ± 1 standard error. (After Augustine and Frank 2001.)

there (Abraham and Jefferies 1997). The greater snow geese that summer in the eastern Canadian Arctic and migrate to the southeastern United States are poised for a similar population explosion, with similar effects predicted for the vegetation in their breeding habitat.

Generality

How general and important are the effects of herbivores on plant communities? This question has been a controversial one. In a classic and much-cited conceptual paper, Hairston et al. (1960) suggested that herbivores are kept at low densities by their own predators, limiting their effects on plants. Widely referred to as the HSS hypotheses (after the authors’ initials), this point of view has been controversial ever since it was proposed. William Murdoch (1966) argued that the logic of HSS is circular. Pointing to its argument that because they do not eat all the available plant material, herbivores must not be food-limited, Murdoch observed that one could apply the same logic to the next trophic level: because they do not eat all the available herbivores, carnivores must not be food-limited—exactly the opposite of what Hairston et al. argued was the case. Murdoch also argued that the HSS hypotheses were poorly defined