Plant Productivity Survival and Growth Form

Traditionally, herbivory has been viewed solely as a process that reduces primary production. As described in the preceding text, herbivory can remove several times the standing crop of foliage, alter plant growth form, or kill all plants of selected species over large areas during severe outbreaks. However, several studies indicate more complex effects of herbivory. The degree to which her-bivory affects plant survival, productivity, and growth form depends on the plant parts affected; plant condition, including the stage of plant development; and the intensity of herbivory.

Different herbivore species and functional groups (e.g., folivores, sap-suckers, shoot borers, and root feeders) determine which plant parts are affected. Foli-vores and leaf miners reduce foliage surface area and photosynthetic capacity, thereby limiting plant ability to produce and accumulate photosynthates for growth and maintenance. In addition to direct consumption of foliage, much unconsumed foliage is lost as a result of wasteful feeding by folivores (Risley and Crossley 1993) and induction of leaf abscission by leaf miners (Faeth et al. 1981, Stiling et al. 1991). Sap-suckers and gall-formers siphon fluids from the plant's vascular system and reduce plant ability to accumulate nutrients or photosyn-thates for growth and maintenance. Shoot borers and bud feeders damage meristems and growing shoots, altering plant growth rate and form. Root feeders reduce plant ability to acquire water and nutrients. Reduced accumulation of energy often reduces flowering or seed production, often completely precluding reproduction (V.K. Brown et al. 1987, Crawley 1989). For example, M. Parker (1985) and Wisdom et al. (1989) reported that flower production by composite shrubs, Gutierrezia microcephala, was reduced as much as 80% as a consequence of grazing by the grasshopper, Hesperotettix viridis. Many sap-suckers and shoot-and root-feeders also transmit or facilitate growth of plant pathogens, including viruses, bacteria, fungi, and nematodes (e.g., C. Jones 1984).Alternatively, folivory may induce resistance to subsequent infection by plant pathogens (Hatcher et al. 1995).

Plant condition is affected by developmental stage and environmental conditions and determines herbivore population dynamics (see Chapters 3 and 6) and plant capacity to compensate for herbivory. Low or moderate levels of herbivory often increase photosynthesis and stimulate plant productivity (e.g., Belovsky and Slade 2000, Carpenter and Kitchell 1984, Carpenter et al. 1985, C. Carroll and Hoffman 1980, Detling 1987, 1988, M. Dyer et al. 1993, Kolb et al. 1999, Lowman 1982, McNaughton 1979,1993a, Pedigo et al. 1986, Trumble et al. 1993, S. Williamson et al. 1989), whereas severe herbivory usually results in mortality or decreased fitness (Detling 1987,1988, Marquis 1984, S.Williamson et al. 1989). Healthy plants can replace lost foliage, resulting in higher annual primary production, although standing crop biomass of plants usually is reduced.

Kolb et al. (1999) experimentally evaluated a number of factors that potentially influence the effect of western spruce budworm, Choristoneura occidentalis, defoliation on potted Douglas-fir seedling physiology and growth. They demonstrated that seedling biomass decreased, but photosynthetic rate; stomatal conductance; foliar concentrations of N, Ca, and Mg; and soil water potential increased with increasing intensity of herbivory. Increased photosynthesis and reduced water stress may improve tree survival in environments where water stress has a more serious negative effect on survival than does defoliation. Pearson et al. (2003) evaluated factors that influenced growth and mortality of 6 pioneer tree species in forest gaps of different sizes in Panama. They found that herbivory varied from 2% to 10% overall, with Croton bilbergianus showing levels of 5-30%. Most species showed a trend of increasing leaf area loss with increasing gap size, but the fastest-growing species did not have the highest levels of herbivory. Variation in growth rate and mortality of these plant species could not be explained by foliage losses to herbivores but was strongly influenced by a tradeoff between maximum growth in the wet season and ability to survive seasonal drought, particularly in small gaps.

The rapid replacement of primary production lost to herbivores in many aquatic systems is well-known (Carpenter and Kitchell 1984, 1987, 1988, Carpenter et al. 1985, J.Wallace and O'Hop 1985). J.Wallace and O'Hop (1985) reported that new leaves of water lilies, Nuphar luteum, disappeared within 3 weeks as a result of grazing by the leaf beetle, Pyrrhalta nymphaeae. A high rate of leaf production was necessary to maintain macrophyte biomass. Trumble et al. (1993) reviewed literature demonstrating that compensatory growth (replacement of consumed tissues) following low to moderate levels of herbivory is a widespread response by terrestrial plants as well. Increased productivity of grazed grasses, compared to ungrazed grasses, has been demonstrated experimentally in a variety of grassland ecosystems (Belovsky and Slade 2000, Detling 1987, 1988, McNaughton 1979, 1986, 1993a, Seastedt 1985, S. Williamson et al.

1989), but growth enhancement may depend on the presence of herbivore feces (Baldwin 1990, Hik and Jefferies 1990) or other herbivore products (Baldwin

1990). M. Dyer et al. (1995) demonstrated that crop and midgut extracts present in grasshopper regurgitants during feeding stimulate coleoptile growth in grasses, but saliva may not stimulate growth of all plant species (Detling et al. 1980). Wickman (1980) and Alfaro and Shepherd (1991) reported that short-term growth losses by defoliated conifers were followed by several years, or even decades, of growth rates that exceeded predefoliation rates (Fig. 12.4). Romme et al. (1986) found that annual wood production in pine forests in western North America reached or exceeded preoutbreak levels within 10-15 years following mountain pine beetle, Dendroctonus ponderosae, outbreaks.

Detling (1987, 1988), M. Dyer et al. (1993, 1995), McNaughton (1979, 1986, 1993a), and Paige and Whitham (1987) have argued that herbivory may benefit some plants to the extent that species adapted to replace consumed tissues often disappear in the absence of grazing. NPP of some grasslands declines when grazing is precluded, as a result of smothering of shoots as standing dead material accumulates (Kinyamario and Imbamba 1992, Knapp and Seastedt 1986, x

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Changes in ring width indices for Douglas-fir defoliated at different intensities by the Douglas-fir tussock moth, Orgyia pseudotsugata, in 1981 (arrow) .The horizontal line at 0% represents ring width index for nondefoliated trees. From Alfaro and Shepherd (1991) with permission from the Society of American Foresters. Please see extended permission list pg 572.

McNaughton 1979). D. Inouye (1982) reported that herbivory by several insect and mammalian herbivores had a variety of positive and negative effects on fitness of a thistle, Jurinea mollis.

These observations generated the herbivore optimization hypothesis (Fig. 12.5), or overcompensation hypothesis, that primary production is maximized at low to moderate levels of herbivory (Carpenter and Kitchell 1984, Mattson and Addy 1975, McNaughton 1979, Pedigo et al. 1986). This hypothesis is widely recognized among aquatic ecologists as the basis for inverted biomass pyramids (Carpenter and Kitchell 1984,1987,1988, Carpenter et al. 1985). Its application to terrestrial systems has been challenged (e.g., Belsky 1986, Painter and Belsky 1993, D. Patten 1993) but has been supported by experimental tests for both insect and vertebrate herbivores in grassland (Belovsky and Slade 2000, Detling 1987, M. Dyer et al. 1993, McNaughton 1979, 1993b, Seastedt 1985), salt marsh (Hik and Jefferies 1990), forest (Lovett and Tobiessen 1993, Schowalter et al. 1991), and even agricultural (Pedigo et al. 1986) ecosystems.

Compensatory growth likely depends on environmental conditions, availability and balances of limiting nutrients, timing of herbivory, and plant adaptation to herbivory (de Mazancourt et al. 1998, Loreau 1995, Trlica and Rittenhouse 1993, S. Williamson et al. 1989). C. Lovelock et al. (1999) demonstrated that CO2 enrichment did not enhance compensation by a tropical legume, Copaifera aromatica, compared to compensation under ambient atmospheric CO2, following artificial defoliation in Panama. Rastetter et al. (1997) used a multi-element model to demonstrate that plant response to CO2 enrichment could be constrained by nitrogen limitation. De Mazancourt et al. (1998) and Loreau (1995) used a theoretical model to study conditions under which grazing optimization could occur. They found that grazing optimization required that moderate her-

Primary Production Limiting Factor
I Relationship between intensity of phytophagy and net primary production. Net primary production often peaks at low to moderate intensities of phytophagy, supporting the grazing optimization hypothesis. From S. Williamson et al. (1989) with permission from the Society for Range Management.

bivory decreased nutrient losses from the system. They concluded that grazing optimization is most likely to occur in ecosystems with large losses of limiting nutrients during decomposition or where herbivores import nutrients from outside the ecosystem.

Plants often are able to compensate for herbivory in the spring when conditions favor plant productivity but become less able to compensate later in the season (Akiyama et al. 1984, Hik and Jefferies 1990, Thompson and Gardner 1996). Grasshopper, Aulocara elliotti, did not significantly reduce standing crop of blue grama grass, Bouteloua gracilis, when feeding occurred early in the growing season but significantly reduced standing crop when feeding occurred later in southwestern New Mexico, United States (Thompson and Gardner 1996).

M. Dyer et al. (1991) reported that grazing-adapted and nongrazing-adapted clones of an African C4 grass, Panicum coloratum, differed significantly in their responses to herbivory by grasshoppers. After 12 weeks of grazing, the grazing-adapted plants showed a 39% greater photosynthetic rate and 26% greater biomass, compared to the nongrazing-adapted plants. Lovett and Tobiessen (1993) found that experimental defoliation resulted in elevated photosynthetic rates of red oak, Quercus rubra, seedlings grown under conditions of low and high nitrogen availability but that high nitrogen seedlings were able to maintain high photosynthetic rates for a longer time (Fig. 12.6). Vanni and Layne (1997)


Mean net photosynthetic rate in old leaves from Quercus rubra seedlings subjected to four combinations of nitrogen fertilization and defoliation intensity. Defoliation and fertilization treatments began July 26. From Lovett and Tobiessen (1993) with permission from Heron Publishing.


Mean net photosynthetic rate in old leaves from Quercus rubra seedlings subjected to four combinations of nitrogen fertilization and defoliation intensity. Defoliation and fertilization treatments began July 26. From Lovett and Tobiessen (1993) with permission from Heron Publishing.

reported that consumer-mediated nutrient cycling strongly affected phytoplank-ton production and community dynamics in lakes.

Honkanen et al. (1994) artificially damaged needles or buds of Scots pine. Damage to buds increased shoot growth. Damage to needles stimulated or suppressed shoot growth, depending on the degree and timing of damage and the position of the shoot relative to damaged shoots. Growth was significantly reduced by loss of 100%, but not 50%, of needles and was significantly reduced on shoots located above damaged shoots, especially late in the season. Shoots located below damaged shoots showed increased growth. Honkanen et al. (1994) suggested that these different effects of injury indicated an important effect of physiological status of the damaged part (i.e., whether it was a sink [bud] or source [needle] for resources).

Morón-Ríos et al. (1997a) reported that below-ground herbivory by root-feeding scarab beetle larvae, Phyllophaga sp., prevented compensatory growth in response to above-ground grazing. Furthermore, salivary toxins or plant pathogens injected into plants by some sap-sucking species can cause necrosis of plant tissues (C. Jones 1984, Miles 1972, Raven 1983, Skarmoutsos and Millar 1982), honeydew accumulation on foliage can promote growth of pathogenic fungi and limit photosynthesis (Dik and van Pelt 1993), and some leaf miners induce premature abscission (Chabot and Hicks 1982, Faeth et al. 1981, Pritchard and James 1984a, b, Stiling et al. 1991), thereby exacerbating the direct effects of herbivory. However, foliage injury can induce resistance to subsequent herbivory or infection by plant pathogens (Hatcher et al. 1995, M. Hunter 1987, Karban and Baldwin 1997; see Chapters 3 and 8). Although primary productivity may be increased by low to moderate intensities of grazing, some plant tissues may be sacrificed by plant allocation of resources to replace lost foliage. Morrow and LaMarche (1978) and Fox and Morrow (1992) reported that incremental growth of Eucalyptus stems treated with insecticide was 2-3 times greater than that of unsprayed stems. Root growth and starch reserves are affected significantly by above-ground, as well as below-ground, herbivory. Morón-Ríos et al. (1997a) noted that root-feeders reduced root-to-shoot ratios by 40% and live-to-dead above-ground biomass ratio by 45% through tiller mortality, apparently reducing plant capacity to acquire sufficient nutrients for shoot production. Rodgers et al. (1995) observed that starch concentrations in roots were related inversely to the level of mechanical damage to shoots of a tropical tree, Cedrela odorata (Fig. 12.7). Gehring and Whitham (1991,1995) reported that folivory on pinyon pine adversely affected mycorrhizal fungi, perhaps through reduced carbohydrate supply to roots. However, Holland et al. (1996) reported that grasshopper

None Moderate Severe

Damage level

| Effect of intensity of artificial herbivory (to simulate terminal shoot damage by a lepidopteran, Hypsipyla grandella) on mean relative change (+ standard error) in starch concentrations (percent of initial level) in roots and lower boles of a neotropical hardwood, Cedrela odorata, in Costa Rica. In the moderate treatment, 0.2-0.3 cm of terminal shoot was excised; in the severe treatment, 0.5-0.6 cm of terminal was excised. Data represent 5 sampling dates over a 12-day period beginning 18 days after treatment. From Rodgers et al. (1995) with permission from the Association of Tropical Biologists.

grazing on maize increased carbon allocation to roots. Soil microbial biomass peaked at intermediate levels of herbivory in no-tillage agricultural systems (Holland 1995), perhaps because moderate intensities of herbivory increased root exudates that fuel microbial production (Holland et al. 1996). McNaughton (1979,1993a) and van der Maarel and Titlyanova (1989) concluded that sufficient shoot biomass to maintain root function is critical to plant ability to compensate for losses to herbivores.

Levels of herbivory that exceed plant ability to compensate lead to growth reduction, stress, and mortality. Seedlings are particularly vulnerable to herbivores because of their limited resource storage capacity and may be unable to replace tissues lost to herbivores (P. Hulme 1994, Wisdom et al. 1989). D. Clark and Clark (1985) reported that survival of tropical tree seedlings was highly correlated with the percentage of original leaf area present 1 month after germination and with the number of leaves present at 7 months of age. Continued grazing during periods of reduced plant productivity generally exacerbates stress. Resource-limited plants are more likely to succumb to herbivores than are plants with optimal resources (Belovsky and Slade 2000, Lovett and Tobiessen 1993). Plant species most stressed by adverse conditions suffer severe mortality to herbivores (e.g., Crawley 1983, Painter and Belsky 1993, Schowalter and Lowman 1999). Wright et al. (1986) found that Douglas-fir beetle, Dendroc-tonus pseudotsugae, and fir engraver beetle, Scolytus ventralis, preferentially colonized Douglas-fir trees that had lost >90% of foliage to Douglas-fir tussock moth although larval survival was greater in nondefoliated than in defoliated trees. However, Kolb et al. (1999) demonstrated that intense defoliation could reduce moisture stress during dry periods (see earlier in this chapter).

Herbivory by exotic species may cause more severe or more frequent reduction in productivity and survival, in part because plant defenses may be less effective against newly associated herbivores. The most serious effects of herbivory, however, result from artificially high intensities of grazing by livestock or game animals (Oesterheld et al. 1992, D. Patten 1993). Whereas grazing by native herbivores usually is seasonal and grasses have sufficient time to replace lost tissues before grazing resumes, grazing by livestock is continuous, allowing insufficient time for recovery (McNaughton 1993a, Oesterheld and McNaughton 1988, 1991, Oesterheld et al. 1992).

Herbivory also can alter plant architecture, potentially influencing future growth and susceptibility to herbivores. Gall-formers deform expanding foliage and shoots. Repeated piercing during feeding-site selection by sap-sucking species also can cause deformation of foliage and shoots (Miles 1972, Raven 1983). Shoot-borers and bud-feeders kill developing shoots and induce growth of lateral shoots (D. Clark and Clark 1985, Nielsen 1978, Reichle et al. 1973, Zlotin and Khodashova 1980). Severe or repeated herbivory of this type often slows or truncates vertical growth and promotes bushiness. Gange and Brown (1989) reported that herbivory increased variation in plant size. Morón-Ríos et al. (1997a) found that both above-ground and below-ground herbivory alter shoot-to-root ratios. Suppression of height or root growth restricts plant ability to acquire resources and often leads to plant death. However, pruning also can stimulate growth and seed production (e.g., D. Inouye 1982) or improve water and nutrient balance (e.g., W. Webb 1978).

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