Measurement of Herbivory

Effects of herbivory on ecosystem processes are determined by temporal and spatial variability in the magnitude of consumption. Clearly, evaluation of the effects of herbivory requires robust methods for measuring herbivory as well as primary productivity and other ecosystem processes. Measurement of herbivory can be difficult, especially for underground plant parts and forest canopies, and has not been standardized. Several methods commonly used to measure herbivory have been compared by Filip et al. (1995), Landsberg (1989), and Lowman (1984).

The simplest and most widely used technique is the measurement of feeding rate by individual herbivores and extrapolation to feeding rate by a population. This technique provides relatively accurate rates of consumption and can be used to estimate per capita feeding rate for sap-suckers as well as folivores (e.g., Gandar 1982, Schowalter et al. 1981c, B. Stadler and Müller 1996). Insect folivores usually consume 50-150% of their dry body mass per day (Blumer and

Diemer 1996, Reichle and Crossley 1967, Reichle et al. 1973, Schowalter et al. 1981c).

Rates of sap and root consumption are difficult to measure, but a few studies have provided limited information. For example, honeydew production by individual sap-sucking insects can be used as an estimate of their consumption rates. Stadler and Müller (1996) and Stadler et al. (1998) reported that individual spruce aphids, Cinara spp., produced from 0.1 mg honeydew day-1 for first instars to 1 mg day-1 for adults, depending on aphid species, season, and nutritional status of the host. Schowalter et al. (1981c) compiled consumption data from studies of eight herb- and tree-feeding aphids (Auclair 1958, 1959, 1965, Banks and Macaulay 1964, Banks and Nixon 1959, M. Day and Irzykiewicz 1953, Llewellyn 1972, Mittler 1958, 1970, Mittler and Sylvester 1961, Van Hook et al. 1980, M. Watson and Nixon 1953), a leafhopper (M. Day and McKinnon 1951), and a spit-tlebug (Wiegert 1964) that yielded an average consumption rate of 2.5 mg dry sap mg-1 dry insect day-1.

Several factors affect the rate of sap consumption. P. Andersen et al. (1992) found that leafhopper feeding rate was related to xylem chemistry and fluid tension. Feeding rates generally increased with amino-acid concentrations and decreased with xylem tension, ceasing above tensions of 2.1 Mpa when plants were water stressed. Stadler and Müller (1996) reported that aphids feeding on poor-quality hosts with yellowing needles produced twice the amount of honey-dew as did aphids feeding on high-quality hosts during shoot expansion, but this difference disappeared by the end of shoot expansion. Banks and Nixon (1958) reported that aphids tended by ants approximately doubled their rates of ingestion and egestion.

Measurement of individual consumption rate has limited utility for extrapolation to effects on plant growth because more plant material may be lost, or not produced, than actually consumed as a consequence of wasteful feeding or mortality to meristems (e.g., Blumer and Diemer 1996, Gandar 1982). For example, Schowalter (1989) reported that feeding on Douglas-fir, Pseudotsuga menziesii, buds by a bud moth, Zeiraphera hesperiana, caused an overall loss of <1% of foliage standing crop, but the resulting bud mortality caused a 13% reduction in production of shoots and new foliage.

Herbivory can be estimated as the amount of frass collected per unit time (Fig. 12.1), adjusted for assimilation efficiency (Chapter 4). This measure is sensitive to conditions that affect frass collection, such as precipitation. Hence, frass generally must be collected prior to rainfall events. Mizutani and Hijii (2001) measured the effect of precipitation on frass collection in conifer and deciduous broad-leaved forests in central Japan and calculated correction factors for loss of frass as a result of precipitation. Such methods enhance the use of frass collection for estimation of herbivory.

Percentage leaf area missing can be measured at discrete times throughout the growing season. This percentage can be estimated visually but is sensitive to observer bias (Landsberg 1989). Alternatively, leaf area of foliage samples is measured, then remeasured after holes and missing edges have been reconstructed (e.g., Filip et al. 1995, H. Odum and Ruiz-Reyes 1970, Reichle et al. 1973,

Swamp Tupelo Plant Georgia

Insect herbivore feces collected on understory vegetation in cypress-tupelo swamp in southern Louisiana, United States.

Insect herbivore feces collected on understory vegetation in cypress-tupelo swamp in southern Louisiana, United States.

Schowalter et al. 1981c). Reconstruction originally was accomplished using tape or paper cutouts. More recently, computer software has become available to reconstruct leaf outlines and fill in missing portions (Hargrove 1988). Neither method accounts for expansion of holes as leaves expand, for compensatory growth (to replace lost tissues), for completely consumed or prematurely abscissed foliage, for foliage loss as a result of high winds, nor for herbivory by sap-suckers (Faeth et al. 1981, Hargrove 1988, Lowman, 1984; Reichle et al. 1973, Risley and Crossley, 1993, Stiling et al. 1991).

The most accurate method for measuring loss to folivores is detailed life table analysis of marked leaves at different stages of plant growth (Aide 1993, Filip et al. 1995, Hargrove 1988, Lowman 1984). Continual monitoring permits accounting for consumption at different stages of plant development, with consequent differences in degree of hole expansion, compensatory growth, and complete consumption or loss of damaged leaves (Lowman 1984, Risley and Crossley 1993). Estimates of herbivory based on long-term monitoring often are 3-5 times the estimates based on discrete measurement of leaf area loss (Lowman 1984,1995). Filip et al. (1995) compared continual and discrete measurements of herbivory for 12 tree species in a tropical deciduous forest in Mexico. Continual measurement provided estimates 1-5 times higher than those based on discrete sampling. On average, measurements from the two techniques differed by a factor of 2. Broad-leaved plants are more amenable to this technique than are needle-leaved plants.

Several methods also have been used to measure effects of herbivory on plants or ecosystem processes. A vast literature is available on the effects of herbivory on growth of individual plants or plant populations (e.g., Crawley 1983, Huntly 1991). However, most studies have focused on effects of above-ground herbivores on above-ground plant parts. Few studies have addressed root-feeding insects or root responses to herbivory (M. Hunter 2001a, Morón-Ríos et al. 1997b, J. Smith and Schowalter 2001, D. Strong et al. 1995). J. Smith and Schowalter (2001) and D. Strong et al. (1995) found that roots can take at least a year to recover from herbivory, indicating that short-term experiments may be inadequate to estimate the herbivore effects on roots.

At the ecosystem level, a number of studies have compared ecosystem processes between sites naturally infested or not infested during population irruptions. Such comparison confounds herbivore effects with environmental gradients that may be responsible for the discontinuous pattern of herbivory (Chapter 7). Hurlbert (1984) discussed the importance of independent, geographically intermixed replicate plots for comparison of treatment effects. This requires manipulation of herbivore abundances in replicate plots to evaluate effects on ecosystem parameters.

A few studies have involved experimental manipulation of herbivore numbers, especially on short vegetation (e.g., Kimmins 1972, McNaughton 1979, Morón-Ríos et al. 1997a, Schowalter et al. 1991,Seastedt 1985,Seastedt et al. 1983, S. Williamson et al. 1989), but this technique clearly is difficult in mature forests. The most common method has been comparison of ecosystem processes in plots with nominal herbivory versus chemically suppressed herbivory (e.g.,V.K. Brown et al. 1987,1988, D. Gibson et al. 1990, Louda and Rodman 1996, Seastedt et al. 1983). However, insecticides can provide a source of limiting nutrients that may affect plant growth. Carbaryl, for example, contains nitrogen, which is frequently limiting and likely to stimulate plant growth. Manipulation of herbivore abundance is the best means for relating effects of herbivory over a range of intensity (e.g., Schowalter et al. 1991, S. Williamson et al. 1989), but such manipulation of herbivore abundance often is difficult (Baldwin 1990, Crawley 1983, Schowalter et al. 1991). Cages constructed of fencing or mesh screening are used to exclude or contain experimental densities of herbivores (e.g., McNaughton 1985, Palmisano and Fox 1997). Mesh screening should be installed in a manner that does not restrict air movement or precipitation and thereby alter growing conditions within the cage.

A third option has been to simulate herbivory by clipping or pruning plants or by punching holes in leaves (e.g., Honkanen et al. 1994). This method avoids the problems of manipulating herbivore abundance but may fail to represent important aspects of herbivory, other than physical damage, that influence its effects (e.g., Baldwin 1990, Crawley 1983, Frost and Hunter 2005, Lyytikainen-Saarenmaa 1999). For example, herbivore saliva may stimulate growth of some plant species (M. Dyer et al. 1995), and natural patterns of consumption and excretion affect litter condition, decomposition, and nutrient supply (Frost and Hunter 2005, Hik and Jefferies 1990, Lovett and Ruesink 1995, B. Stadler et al. 1998, Zlotin and Khodashova 1980). Lyytikainen-Saarenmaa (1999) reported that artificial defoliation of Scots pine, Pinus sylvestris, saplings caused greater growth reduction than did comparable herbivory by sawflies, Diprion pini and Neodiprion sertifer, in May and June, whereas the opposite trend was seen for trees subjected to treatments in July and August.

The choice of technique for measuring herbivory and its effects depends on several considerations. The method of measurement must be accurate, efficient, and consistent with objectives. Measurement of percentage leaf area missing at a point in time is an appropriate measure of the effect of herbivory on canopy porosity, photosynthetic capacity, and canopy-soil or canopy-atmosphere interactions but does not represent the rate of consumption or removal of plant material. Access to some plant parts is difficult, precluding continuous monitoring. Hence, limited data are available for herbivory on roots or in forest canopies. Simulating herbivory by removing plant parts or punching holes in leaves fails to represent some important effects of herbivory, such as salivary toxins or stimulants or flux of canopy material to litter as feces, but it does overcome the difficulty of manipulating abundances of herbivore species.

Similarly, the choice of response variables depends on objectives. Most studies have examined only effects of herbivory on above-ground primary production, consistent with emphasis on foliage and fruit production. However, herbivores feeding above ground also affect root production and rhizosphere processes (Gehring and Whitham 1991, 1995, Holland et al. 1996, Rodgers et al. 1995, J. Smith and Schowalter 2001). Effects on some fluxes, such as dissolved organic carbon in honeydew, are difficult to measure (B. Stadler et al. 1998). Some effects, such as compensatory growth and altered community structure, may not become apparent for long time periods following herbivore outbreaks (Alfaro and Shepherd 1991, Wickman 1980).

C. Spatial and Temporal Patterns of Herbivory

All plant species support characteristic assemblages of insect herbivores, although some plants host a greater diversity of herbivores and exhibit higher levels of herbivory than do others (e.g., Coley and Aide 1991, de la Cruz and Dirzo 1987). Some plants tolerate continuous high levels of herbivory, whereas other species show negligible loss of plant material (Carpenter and Kitchell 1984, Lowman and Heatwole 1992, McNaughton 1979, Schowalter and Ganio 2003), and some plant species suffer mortality at lower levels of herbivory than do others. Herbivory usually is concentrated on the most nutritious or least defended plants and plant parts (Chapter 3; Aide and Zimmerman 1990).

The consequences of herbivory vary significantly, not just among plant-herbivore interactions but also as a result of different spatial and temporal factors (Huntly 1991, Maschinski and Whitham 1989). For example, water or nutrient limitation and ecosystem fragmentation can affect significantly the ability of the host plant to respond to herbivory (e.g., Chapin et al. 1987, Kolb et al. 1999, Maschinski and Whitham 1989, W. Webb 1978). The timing of herbivory with respect to plant development and the intervals between attacks also have important effects on ecosystem processes (Hik and Jefferies 1990).

Herbivory usually is expressed as daily or annual rates of consumption and ranges from negligible to several times the standing crop biomass of foliage (Table 12.1), depending on ecosystem type, environmental conditions, and regrowth capacity of the vegetation (Lowman 1995, Schowalter and Lowman 1999). Herbivory for particular plant species can be integrated at the ecosystem level by weighting rates for each plant species by its biomass or leaf area. When the preferred hosts are dominant plant species, loss of plant parts can be dramatic and conspicuous, especially if these species are slow to replace lost parts (B. Brown and Ewel 1987). For example, defoliation of evergreen forests may be visible for months, whereas deciduous forests and grasslands are adapted for periodic replacement of foliage and usually replace lost foliage quickly. Eucalypt forests are characterized by chronically high rates of herbivory (Fox and Morrow 1992). Some species lose more than 300% of their foliage standing crop annually, based on life table studies of marked leaves (Lowman and Heatwole 1992).

Comparison of herbivory among ecosystem types (see Table 12.1) indicates considerable variation. The studies in Table 12.1 reflect the range of measurement techniques described earlier in this chapter. Most are short-term snapshots of folivory, often for only a few plant species; do not provide information on herbivory by sap-suckers or root feeders; and do not address any deviation in environmental conditions, plant chemistry, or herbivore densities from long-term means during the period of study. Long-term studies using standardized techniques are necessary for meaningful comparison of herbivory rates.

Cebrian and Duarte (1994) compiled data from a number of aquatic and terrestrial ecosystems and found a significant relationship between percentage plant material consumed by herbivores and the rate of primary production. Herbivory ranged from negligible to >50% of photosynthetic biomass removed daily. Rates were greatest in some phytoplankton communities where herbivores consumed all production daily and least in some forests where herbivores removed <1% of production. Insects are the primary herbivores in forest ecosystems (Janzen 1981, Wiegert and Evans 1967) and account for 11-73% of total herbivory in grasslands, where native vertebrate herbivores remove an additional 15-33% of production (Detling 1987, Gandar 1982, Sinclair 1975). Temperate deciduous forests and tropical evergreen forests show similar annual losses of 3-20%, based on discrete sampling of leaf area loss (Coley and Aide 1991, Landsberg and Ohmart 1989, H. Odum and Ruiz-Reyes 1970, Schowalter and Ganio 1999, Schowalter et al. 1986, Van Bael et al. 2004). Aquatic ecosystems, evergreen forests, and grasslands, which replace lost photosynthetic tissue continuously, often lose several times their standing crop biomass to herbivores annually, based on loss of marked foliage or on herbivore exclusion (Carpenter and Kitchell 1984, Cebrian and Duarte 1994, Crawley 1983, Landsberg 1989, Lowman and Heatwole 1992, McNaughton 1979).

In addition to the conspicuous loss of photosynthetic tissues, terrestrial plants lose additional material to sap-suckers and root feeders. Schowalter et al. (1981c) compiled data on rates of sap consumption to estimate turnover of 5-23% of foliage standing crop biomass through sap-sucking herbivores, in addition to 1-2% turnover through folivores in a temperate deciduous forest. J. Smith and

Herbivory measured in temperate and tropical ecosystems (including understory). Expanded from Lowman (1995).

Location Ecosystem type Level of grazing Techniquea Source

Tropical

Costa Rica

Tropical forest

7.5% (new leaves)

1

N. Stanton (1975)

Tropical evergreen forest

30% (old)

1

N. Stanton (1975)

Panama

Tropical evergreen forest

13%

1

Wint (1983)

Panama (BCI)

Tropical evergreen forest

8% (6% insect; 1-2% vertebrates)

1,2

Leigh and Smythe (1978)

15%

1,2

Leigh and Windsor (1982)

Understory only

21% (but up to 190%)

S

Coley (1983)

Puerto Rico

Tropical evergreen forest

7.8%

1

H. Odum and Ruiz-Reyes (1970)

5.5-16.1%

1

Benedict (1976)

2-6%

1

Schowalter (1994a)

2-13%

1

Schowalter and Ganio (1999)

Mexico

Tropical deciduous forest

7-9%

1

Filip et al. (1995)

Tropical deciduous forest

17%

S

Filip et al. (1995)

Venezuela

Understory only

0.1-2.2%

1

Golley (1977)

New Guinea

Tropical evergreen forest

9-12%

1

Wint (1983)

Australia

Montane or cloud forest

26%

S

Lowman (1984)

Warm temperate forest

22%

S

Lowman (1984)

Subtropical forest

14.6%

S

Lowman (1984)

Cameroon

Tropical evergreen forest

8-12%

S

Lowman et al. (1993)

"0

Tanzania South Africa

Temperate

North America

Australia

Europe

Tropical grassland Tropical savanna

Deciduous forest

Herbaceous sere Coniferous forest

Grassland Evergreen forest Dry forest

Deciduous forest Alpine grassland

14-38% (4-8% insect; 8-34% vertebrates) 38% (14% insect; 24% vertebrates)

Sinclair (1975) Gandar (1982)

Reichle et al. (1973) Schowalter et al. (1981c) Crossley and Howden (1966) Schowalter (1989) Schowalter (1995) Detling (1987)

Lowman and Heatwole (1992) Fox and Morrow (1983) Ohmart et al. (1983) Nielsen (1978) Blumer and Diemer (1996)

al, Leaf area missing; 2, litter or frass collection; 3, turnover of marked foliage; 4, individual consumption rates. Please see extended permission list pg 572.

W Ul Ul

Schowalter (2001) found that shoot-feeding aphids, Cinara pseudotsugae, significantly reduced Douglas-fir root tissue density and growth and that at least 1 year was required for recovery after feeding ceased. V.K. Brown and Gange (1991) and Morón-Ríos et al. (1997a) reported that root-feeding insects can reduce primary production of grasses by 30-50%.

Factors that promote herbivore population growth (e.g., abundant and susceptible hosts) also increase herbivory (see Chapters 6 and 8). Proportional losses of foliage to folivores generally are higher in less diverse ecosystems, compared to more diverse ecosystems (Kareiva 1983), but the intensity of herbivory also depends on the particular species composition of the vegetation (R. Moore and Francis 1991, R. Moore et al. 1991). B. Brown and Ewel (1987) demonstrated that ecosystem-level foliage losses per unit ground area were similar among four tropical ecosystems that varied in vegetation diversity, but the proportional loss of foliage standing crop was highest in the less diverse ecosystems. Nevertheless, rare plant species in diverse ecosystems can suffer intense herbivory, especially under conditions that increase their apparency or acceptability (Brown and Ewel 1987, Schowalter and Ganio 1999). C. Fonseca (1994) reported that an Amazonian myrmecophytic canopy tree showed 10-fold greater foliage losses when ants were experimentally removed than when ants were present.

Seasonal and annual changes in herbivore abundance affect patterns and rates of herbivory, but the relationship may not be linear, depending on variation in per capita rates of consumption or wasteful feeding with increasing population density (Crawley 1983, B. Stadler et al. 1998). Herbivory in temperate forests usually is concentrated in the spring during leaf expansion (Feeny 1970, M. Hunter 1987). M. Hunter (1992) reported that more than 95% of total defoliation on Quercus robur in Europe occurs between budburst in April and the beginning of June. Although some herbivorous insects prefer mature foliage (Cates 1980, Sandlin and Willig 1993, Volney et al. 1983), most defoliation events are associated with young foliage (Coley 1980, M. Hunter 1992, R. Jackson et al. 1999, Lowman 1985). Herbivory also is highly seasonal in tropical ecosystems. Tropical plants produce new foliage over a more protracted period than do temperate plants, but many produce new foliage in response to seasonal variation in precipitation (Aide 1992, Coley and Aide 1991, Lowman 1992, Ribeiro et al. 1994). Young foliage may be grazed more extensively than older foliage in tropical rainforests (Coley and Aide 1991, Lowman 1984, 1992). Schowalter and Ganio (1999) reported significantly greater rates of leaf area loss during the "wet" season than during the "dry" season in a tropical rainforest in Puerto Rico (Fig. 12.2). However, seasonal peaks of leaf expansion and herbivory are broader in tropical ecosystems than in temperate ecosystems.

Few studies have addressed long-term changes in herbivore abundances or herbivory as a result of environmental changes (see Chapter 6). However, disturbances often induce elevated rates of herbivory at a site. Periods of elevated herbivory frequently are associated with drought (Mattson and Haack 1987; Chapter 6). Although herbivore outbreaks are usually associated with temperate forests, Van Bael et al. (2004) documented a general outbreak by several lepi-dopteran species on multiple tree and liana species during an El Niño-induced

dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet
dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet

Sloanea berteriana

H-1-1-1-1-1-h wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet dry wet

1989-1999

Effects of tree species, hurricane disturbance, and seasonal cycles on leaf area missing in a tropical rainforest in Puerto Rico, as affected by two hurricanes (1989 and 1998) and a drought (1994-1995). Cecropia is an early successional tree; Manilkara and Sloanea are late successional trees. Green lines represent intact forest (lightly disturbed); red lines represent treefall gaps.

drought in Panama. Torres (1992) reported outbreaks of several lepidopteran species on understory forbs and vines following Hurricane Hugo in Puerto Rico. These studies suggest that outbreaks may be common but less conspicuous in tropical forests. Other disturbances that injure plants also may increase herbivory, especially by root feeders and stem borers (e.g., T. Paine and Baker 1993, Witcosky et al. 1986).

Changes in vegetation associated with disturbance or recovery affect temporal patterns of herbivory. Bach (1990) reported that intensity of herbivory declined during succession in dune vegetation in Michigan (Fig. 12.3). Coley (1980,1982,1983), Coley and Aide (1991), and Lowman and Box (1983) found that rapidly growing early successional tree species showed higher rates of her-bivory than did slow-growing late successional trees. Schowalter (1995), Schowalter and Ganio (1999, 2003), and Schowalter and Crossley (1988) compared canopy herbivore abundances and folivory in replicated disturbed (harvest or hurricane) and undisturbed patches of temperate deciduous, temperate coniferous, and tropical evergreen forests. In all three forest types, disturbance resulted in greatly increased abundances of sap-suckers and somewhat increased abundances of folivores on abundant, rapidly growing early successional plant species. The resulting shift in biomass dominance from folivores to sap-suckers following disturbance resulted in an elevated flux of primary production as soluble photo-synthates, relative to fragmented foliage and feces. Schowalter et al. (1981c) calculated that loss of photosynthate to sap-suckers increased from 5% of foliage standing crop in undisturbed forest to 20-23% of foliage standing crop during the first 2 years following clearcutting, compared to relatively consistent losses of 1-2% to folivores. Torres (1992) reported a sequence of defoliator outbreaks on early successional herbs and shrubs during several months following Hurricane Hugo in Puerto Rico. As each plant species became dominant at a site, severe defoliation facilitated its replacement by other plant species. Continued measurement of herbivory over long time periods will be necessary to relate changes in the intensity of herbivory to environmental changes and to effects on ecosystem processes.

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