Herbivores can affect individual plants, plant populations, and plant communities in subtle, complex, and unexpected ways.
Distribution. Herbivores have the ability to limit the distribution of plants geographically or by habitat. Reef fishes limit the distribution of turtle grass Hhaiassia testudinum) to areas away from the protection provided to the fish by the reefs. Randall (1965) observed a conspicuous band of bare sand averaging 10 m in width that separated coral reefs from beds of sea grasses (Thalassia testudinum and Cymodocea manatorum). The klamath weed (Hypericum perforatum) introduced to California from Europe, became so widespread and common that it was considered a pest. The beetle Chrysolina quadrigemina, which feeds upon it in Europe, was introduced. This introduction, a successful case of biological control, limited the klamath weed so well that it is now found only in shady moist areas where the beetles do not reproduce (Holloway 1964).
Attack by other organisms. Although attack by herbivores may result in an increase in induced defenses, heavy attacks can leave the plant in such a weakened condition that it becomes subject to further attack. Rockwood (1974) described one variation on this theme. The calabash tree (Crescentia alata) was defoliated by hand in order to examine the effects of defoliation on reproduction (see below). At the time of defoliation it was noted that mature leaves had very little herbivore damage, but a beetle was consuming newly produced leaves at the top of the tree. After the hand defoliation the entire tree produced a crop of new leaves. Beetles flew in from a wide geographic area and began feasting on the new leaves. The tree was completely defoliated again, while neighboring control trees, full of mature leaves, were untouched by the beetles. The trees actually flushed a crop of leaves again and were once again defoliated by the beetles. This cycle of destruction ended when the beetles went dormant in the dry season.
Effects of herbivores on productivity and reproduction. One of the tenets of plant-herbivore theory is that herbivore activity has a negative effect on plant growth and reproduction. Such an obvious relationship is, however, more complex than it appears. Several authors have proposed that herbivory, up to a certain level, may be beneficial to plant growth and reproduction. Let us begin with the common recommendation that roses and fruit trees are kept productive by a constant pruning. Next we should note that grasslands are kept at high productivity by either allowing grazing by herbivores, or by a consistent mowing. Finally, Paige and Whitham (1987) and Whitham et al. (1991) found that when the scarlet gilia (Ipomopsis aggregata), an herbaceous plant from the southwestern United States, was browsed such that the apical meristem was destroyed, it responded by producing multiple inflorescences and up to three times as many flowers, fruits, and seeds. In all of these studies the plants appear to compensate for herbivore damage through re-growth. In some cases the re-growth appears to be great enough to surpass the growth in the un-browsed plants. This is known as overcompensation.
Is overcompensation possible, and is it real? In theory, low levels of herbivory can be beneficial to plants such as monocots, in which the meristems are near ground level, for the following reasons: (i) herbivores remove old, non-productive tissues while allowing light to penetrate to the ground where new leaves are found; (ii) herbivores speed up the cycling of mineral nutrients (old leaves are consumed and deposited on the ground as manure, which is quickly broken down by fungi and bacteria, releasing mineral nutrients); (iii) the saliva of herbivores contains growth-promoting substances or encourages an induced defense that protects the plant from further herbivore attacks. McNaughton (1986) endorsed overcompensation, asserting that plants have the capacity to compensate for herbivory and overcompensate for damage so as to increase fitness. Crawley (1997), however, stresses that there is actually no evidence that herbivory can increase Darwinian fitness. He believes that overcompensation has yet to be proven from a well-designed, controlled experiment. In grasses, for example, although above-ground production is maximized by frequent mowing or grazing, it is at the expense of energy storage in roots, or results in suppression of flowering and fruiting. In his critique of Paige and Whitham (1987), Crawley (1997) finds it likely that their result was due to large plants being allocated to the grazed group and small plants to the ungrazed controls.
If overcompensation does occur, the following factors must be explored: (i) timing of herbivory: if a plant is browsed early in the growing season, there is ample evidence that many plants are able to recover; (ii) nutrient, water, and light availability: overcompensation can only occur if the plants are not stressed by a lack of resources needed for photosynthesis; (iii) competition: if there are few competitors in the area, then a plant can recover, again assuming adequate resources are available; under heavy competitive stress, however, a plant that is damaged by an herbivore will lose its position in the community to other plants that are not damaged; (iv) type of tissue lost: as seen in the paper by Ohnmeiss and Baldwin (2000), damage to certain tissues, such as new leaves, is of much greater importance to plant productivity than is damage to other tissues.
Certain plant species have little potential for compensatory responses. For example, species with a physiology that limits new growth, or that live in resource-limited environments, will be severely affected by herbivore attacks. On the other hand, species such as r-selected annuals and perennials, with rapid growth rates and a physiology that allows a rapid response to herbivore damage, are likely candidates for overcompensation. Long-lived, woody perennials, however, are unlikely to easily recover from severe herbivore damage.
High levels of herbivore damage severely limit reproduction in many species. Rockwood (1973) showed that heavy defoliation virtually eliminated reproduction in six species of tropical shrubs and small trees. Subsequently, Marquis (1984, 1992) and Rockwood and Lobstein (1994) have demonstrated a graduated response to differing levels of herbivory. At low levels of herbivory, reproduction is little reduced. However, the timing of the defoliation, its local intensity, and the amount of competition from other plants all modify the reproduction responses to defoliation. Less than 50% defoliation had little effect on herbaceous plants in northern Virginia (Rockwood and Lobstein 1994), and the effects of defoliation were often expressed a year later. Marquis (1992) discovered that a given branch of the tropical shrub Piper arieianum suffered an 80% reduction in seed production from a mere 10% leaf removal when it was concentrated on that one branch. Finally, when the plant Abutilon theophrasti was grown at low densities, up to 75% defoliation had no effect on reproductive fitness. At high densities, however, the same amount of defoliation reduced reproduction by 50% (Lee and Bazzaz 1980).
Community-level effects. Certain herbivores and predators have been described as keystone species. The mere presence or absence of such species is critical to community organization and ecosystem functioning. A simple example is the effect of elephants (Loxodonta africana) in East Africa. Because of their browsing activities and their ability to destroy even the largest trees, a large population of elephants can convert shrub land into a habitat dominated by grasses. Conversely, if elephants are removed from an area it may change back to heavy brush. Darwin discovered that the grazing of cattle on the English heath prevented forests from being established. Upon close examination, under the heath stems he found small fir trees, one of which was 26 years old according to its growth rings. When this common land was enclosed, ending a tradition dating to the Middle Ages, the heath quickly converted to forest (Kingsland 2004). The introduction of Nile perch (Lates niloticus) into Lake Victoria and a species of bass into Lake Gatun in Panama virtually eliminated many species of smaller plankton-feeding fish. This resulted in increases in zooplankton populations, higher consumption rates of phytoplankton, and a decline in overall productivity in the lakes. In some cases a group of ecologically related species, known as a guild, can be considered as keystones. Brown and Heske (1990) reported that eliminating three species of seed-eating kangaroo-rats in the Southwestern United States led to an increase in large-seeded winter annuals. Rescued from rodent predation, the large-seeded species eventually out-competed the small-seeded annuals.
Other rodents such as prairie dogs (Cynomys ludovicianus) can have complex effects on the plant community. In Texas, Weltzin (1991) found that the elimination of prairie dogs was usually followed by an increase in the shrub mesquite. He excluded cattle from an area containing a prairie dog colony. The rodents removed pods and seeds from mesquite and stripped bark from young plants. Such activities help reduce mesquite establishment from around their colonies. He concluded that elimination of prairie dogs in the past had allowed mesquite to spread throughout the cattle ranges.
On the other hand, at Wind Cave National Park in South Dakota, it was shown that prairie dogs favored the establishment of herbaceous dicots over grasses. With no prairie dogs present the herbaceous community consisted of 87% grasses and 13% herbaceous dicots. With prairie dogs present it shifted to 47% grasses and 53% herbs.
Paine (1966) carried out the classic study on keystone predators. In the rocky intertidal zone off the coast of Washington state there were 15 species of coexisting invertebrates. The dominant predator was the starfish Pisaster. The community consisted of species of chitons, limpets, bivalves, barnacles, and a marine snail. Paine experimentally removed starfish from half of the experimental areas. In those areas where the starfish was removed, the bivalve Mytilus and the barnacles became the dominant competitors. They crowded out several other species and the community declined to eight coexisting species. The starfish, when present, preyed consistently on the dominant competitors, preventing them from crowding out the other species.
Paine's work lead to the general hypothesis that predators restrict populations of competitively dominant species and allow coexistence of a greater number of species than would occur in the absence of the predators. This is known as the "top-down" control of communities. As has been recently shown by Robles and Desharnais (2002), this view was too simplistic. A variety of factors, including the interplay of the physical environment with prey refuges, prey dispersal, and prey production determine prey populations and community structure. Nevertheless, Paine's classic work was an important milestone in the history of ecology.
The relationship between herbivores and plant diversity is muddled. Though some studies have shown an increase in plant diversity with her-bivory (Belsky 1992), some have shown a decrease (Milton 1940), and still others no effect whatsoever (Crawley 1989). Again, we must stress that herbivore populations are themselves affected by their own predators and parasites (Hartley and Jones 1997). Thus, the control herbivores might have on plant communities can be neutralized by top-down forces. Herbivores themselves, of course, are most likely controlled by a combination of bottom-up and top-down forces.
Multiple-trophic-level effects. As mentioned in Chapter 10, tritrophic interactions involving plants, herbivores, and predators can produce "trophic cascades" by which predators affect prey populations to the extent that the herbivore-plant interactions are fundamentally altered. Predators can thereby influence plant productivity and community composition (Marquis and Whelan 1994). Evidence for trophic cascades includes the reintroduction of wolves (Canis lupus) to Yellowstone National Park described in Chapter 10. In other cases, the effect of predators on herbivore-plant interactions has been demonstrated by experimentally removing predators. In one such experiment, Marquis and Whelan (1994) caged white oak (Quercus alba) saplings to eliminate bird predation on insect herbivores over a two-year period. Birds were allowed free access to control plants and to a third treatment in which they used insecticides to estimate plant growth with minimal insect damage. In the first year, caged plants suffered 25% leaf area loss, as compared to 13% in plants where birds preyed upon insect herbivores. Sprayed plants suffered only 6% leaf damage. Figures in the second year were 34%, 24%, and 9%, respectively. Prior to this study, most examples of trophic cascades (the effect of predators and parasites on plant productivity and composition) had come from aquatic ecosystems. For terrestrial forests, these results mirror those of Turchin (2003) (larch budworms and their parasitoids) described above. In this case, however, we are dealing with the entire insect herbivore community and its interaction with the insect-consuming bird community.
In conclusion, herbivores have had significant effects on the evolution of plants and continue to exert considerable selective pressure on plants today. Yet herbivores themselves have been under "the gun" from their own predators, so to speak, in both contemporary and evolutionary time. Several lines of evidence tell us that the most effective way to investigate herbivores is to evaluate both their food resources and their predators. Of course the roles of herbivores in an ecosystem are also undoubtedly affected by the physical environment, including the soil and the local climate.
In this book we began with simple growth models for single populations. These models became increasingly complex as we added time lags and stochastic effects. In the second half of the book we began with relatively simple competitive interactions involving only two species. We then moved on to consider interactions between different trophic levels, again starting with simple two-species models (one predator, one prey). But you should now realize that all interspecific interactions must be analyzed in the context of the entire community of organisms, not simply in terms of one competing or one predatory species. Plants are attacked by a multitude of herbivores; herbivores exist in a community of both competitors and predators; and predators themselves are bedeviled with parasites while they compete with other predators of their own species, as well as with individuals of other species. All of this takes place on a complex physical landscape and in an ever-changing climate. Attempting to understand, much less model, these complexities should keep population ecology (indeed all types of ecology) fresh and challenging for a long time to come.
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