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| Proc Natl Acad Sci U S A. 2000 December 19; 97(26): 14412–14417. Published online 2000 December 5. | PMCID: PMC18932 |
Copyright © 2000, The National Academy of Sciences Ecology Insect herbivory accelerates nutrient cycling and increases
plant production G. E. Belovsky * and J. B. Slade Ecology Center and Department of Fisheries and Wildlife, Utah State
University, Logan, UT 84322-5210 Received February 16, 2000; Accepted October 10, 2000. |
Abstract Ecologists hold two views about the role of herbivory in
ecosystem dynamics. First, from a food web perspective in
population/community ecology, consumption by herbivores reduces
plant abundance. Second, from a nutrient cycling perspective in
ecosystem ecology, herbivory sometimes slows down cycling, which
decreases plant abundance, but at other times speeds up cycling, which
possibly increases plant abundance. The nutrient cycling perspective on
herbivory has been experimentally addressed more thoroughly in aquatic
systems than in terrestrial systems. We experimentally examined how
grasshoppers influence nutrient cycling and, thereby, plant abundance
and plant species composition over a period of 5 years. We examined how
grasshoppers influence nutrient (nitrogen) cycling (i)
by their excrement, (ii) by changing the abundance of
and the decomposition rate of plant litter, and (iii) by
both. Grasshoppers may speed up nitrogen cycling by changing the
abundance and decomposition rate of plant litter, which increases total
plant abundance (up to 32.9 g/m2 or 18%),
especially, the abundance of plants that are better competitors when
nitrogen is more available. However, whether grasshoppers enhance plant
abundance depends on how much they consume. Consequently, ecosystems
and food web perspectives are not mutually exclusive. Finally, under
some conditions, grasshoppers may decrease nutrient cycling and plant
abundance. |
If other factors are not
limiting plant production (e.g., water availability, temperature, and
sunlight), plant abundance should decrease when nutrient cycling is
slowed down and increase when nutrient cycling is speeded up. It has
long been hypothesized that herbivory may affect the speed of nutrient
cycling ( 1). Herbivores change nutrient cycling by deposition of
excrement, by changing the quantity and quality (nutrient content and
decomposition rate) of plant litter, and by sequestering nutrients in
their bodies. However, because consumption reduces plant abundance,
herbivory can increase plant abundance only if the enhancement of
nutrient cycling exceeds the depressing effect of consumption. Herbivory's effects on nutrient cycling are summarized in Fig.
1. Nutrient release from excrement and
dead herbivores has been termed the fast cycle ( 2), because this
detritus rapidly decomposes and releases nutrients for plant uptake.
Release of nutrients from plant litter has been termed the slow cycle
( 2), because this detritus slowly decomposes and releases nutrients for
plant uptake. Herbivory affects the slow cycle by changing the quantity
of plant litter and its quality, if herbivores preferentially feed on
plants that differ in how rapidly their litter decomposes ( 3, 4).
Preferential feeding on plants that produce slower decomposing litter
reduces their relative abundance, speeding up the slow cycle, whereas
preferential feeding on plants that produce faster decomposing litter
slows down the slow cycle.
| Figure 1Conditions for herbivores to modify nutrient cycling and NPP are
presented as nutrient cycling slows down and NPP decreases
(A) and nutrient cycling speeds up and NPP increases
(B). Green lines, slow cycle; red lines, fast cycle;
blue lines, consumption. (more ...) |
Shifts in proportion of nutrients released by fast versus slow cycles
may change nutrient availability to plants, which may, in turn, modify
plant production and species composition. If preferential feeding on
slower decomposing plants overshadows deleterious effects of
consumption on plants, it may accelerate nutrient cycling and increase
plant production ( 3). However, preferential feeding on fast decomposing
plants may decelerate nutrient cycling and decrease plant production
( 3). Nutrient cycling changes are one of several factors that affect
plant species composition. For example, if slow decomposing plants are
better competitors when nutrients are less available, and fast
decomposing plants are better competitors when nutrients are more
available, herbivore-induced changes in nutrient cycling may affect
plant competition and, thereby, vegetation communities ( 3).
Furthermore, changes in nutrient cycling, with resulting changes in
plant species composition, may further accentuate changes in nutrient
cycling, plant species composition, and plant production, thereby
creating a self-enhancing or positive feedback. Herbivory's role in nutrient cycling has been investigated
experimentally in aquatic systems where both plants and herbivores are
small-bodied and short-lived. In those environments, herbivory tends to
accelerate nutrient cycling and increase plant production ( 5). In
terrestrial systems, the role of mammalian herbivores in nutrient
cycling has been studied most often, because mammals, with their large
body sizes, consume large quantities of plants. Mammals may either
decelerate nutrient cycling and diminish plant abundance ( 4– 6) or
accelerate cycling and increase plant abundance ( 2, 7, 8). These
findings tend to be observational because of the difficulty in
performing experiments on mammals with their large bodies and extensive
home ranges. However, insect herbivores, because of their abundance and
rapid turnover (short life span), may also strongly influence
terrestrial nutrient cycling and may generally accelerate it ( 9, 10).
Furthermore, because of their small size, short life span, and small
home ranges, insect herbivores and their role in nutrient cycling can
be studied experimentally. For 5 years (1994–1999), we experimentally examined the role that
grasshoppers play in nutrient cycling, plant production and plant
species composition in an ecosystem where large mammalian herbivores
are abundant, the Palouse prairie at the National Bison Range in
Montana. |
Methods Study System. Precipitation averages 350 mm/year, primarily falling as spring
rain (May–June). A 4-ha (1 ha = 10 4
m 2) flat site with homogeneous vegetation (plant
biomass and species composition) at an elevation of ≈750 m was
chosen. Three monocot species ( Elymus smithii, Poa
pratensis, and Poa compressa) composed more than 90%
of plant biomass, with a variety of herbaceous dicots being the
remainder. Net aboveground primary production (NPP) varied annually
from 108 to 237 g (dry weight)/m 2. NPP is
limited in part by nitrogen (N) availability, because plant growth
increased with addition of N fertilizer ( 11). The grasshopper ( Melanoplus sanguinipes) annually was
50–70% of all grasshoppers. Grasshopper hatchlings annually varied
from 11 to 91 hatchlings per m 2, and peak adult
densities were from 4 to 36 adults per m 2. Peak
grasshopper biomass annually varied from 2 to 8
g/m 2. During the 5-year study, grasshopper
density increased and then declined. High grasshopper densities are
typical for Palouse prairie ( 12, 13). At this site, mammalian
herbivores, ranging in size from Bison bison (636 kg) to
Microtus pennsylvanicus (3.5 ×
10 −2 kg), were abundant (≈2.5
g/m 2), densities similar to those reported by
early explorers of the Great Plains (5–9 g/m 2)
( 14, 15). Nevertheless, grasshoppers annually consume 1.25–2.25 times
more plant biomass than mammals at our study site, even if we ignore
cut but unconsumed vegetation, which can be considerable. Experiment. In May 1994, we established replicated mesocosms of the site's
ecosystem: 24 areas of 1 m 2 (1 m × 1
m) and 3 areas of 9 m 2 (3 m × 3 m)
that were delineated by burying plastic edging 15 cm in the soil. For
the first 4 years, we covered 18 of the 1-m 2
areas with an insect screen so that grasshopper densities could be
manipulated to assess how grasshopper density influences nutrient
cycling, annual aboveground plant production (aboveground NPP −
herbivore consumption), and plant species composition. We left 9 areas
uncaged (6 areas of 1 m 2 and 3 areas of 9
m 2) to serve as controls. For the fifth year (May
1998–April 1999), we did not cover any areas with screen, allowing
field grasshoppers to inhabit previously manipulated and control areas
to assess whether observed density effects persisted even though
density manipulations had ended. Finally, we examined aboveground plant
production and nutrient cycling without grasshoppers in 10 cages of
0.36 m 2 that were randomly placed over vegetation
from May 1994 to October 1995 and again from May 1996 to October 1997
(5 cages with no grasshoppers and 5 cages with each year's field
density; ref. 16). We manipulated each 1-m2 caged mesocosm in
one of three ways (six cages per way) from May 1994 to May 1998:
(i) Grasshopper density was manipulated (50% or 125% of
each year's field density: three replicates), with each mesocosm
having its litter removed and replaced with litter produced in a
1-m2 unenclosed area (field grasshopper density),
to examine fast cycle effects (variable consumption, but litter
produced by constant consumption levels). (ii) Grasshopper
density was kept constant (each year's field density), with each
mesocosm having its litter removed and replaced with litter produced in
mesocosms with different grasshopper densities (50% or 125% of each
year's field density–litter produced in cages from way i
above: three replicates) to examine slow cycle effects (constant
consumption, but litter produced by different consumption levels).
(iii) Grasshopper density was manipulated (50% or 125% of
each year's field density: three replicates) with litter annually
produced in situ clipped and placed back in the mesocosm
(see below) to examine combined slow and fast cycles. We defined litter as the aboveground portions of plants in October that
become dormant over the winter and grow from stem bases in the
following spring. We manipulated litter by clipping the aboveground
portions at a height of 1.5 cm, removing them, weighing them, and then
spreading them on the appropriate area. To keep clipped litter in each
area from October to May when cages were removed, we staked netting
(2.54-cm mesh) over areas. We manipulated litter in the six control
mesocosms of 1 m2 as above, but we placed it back
on each respective area. We did not manipulate litter in the three
uncaged mesocosms of 9 m2. We measured field densities of grasshoppers weekly in the
9-m 2 control areas by counting grasshoppers in
0.1-m 2 rings (eight rings per control area) at
times of about 1100 and 1600 ( 17). We stocked the
1-m 2 caged mesocosms with M.
sanguinipes nymphs (≤3rd instar) in mid-June to 50%, 100%, or
125% of current field density. We counted grasshoppers in each caged
mesocosm weekly in three 0.05-m 2 rings at about
1100 and 1600. We added or removed M. sanguinipes
individuals weekly from cages to maintain experimental densities
relative to the field. We added individuals of the current most common
developmental stage and removed individuals by killing and leaving them
in each cage, which had no significant impact on N availability ( 16). We made the following measurements each year in each of the 27
mesocosms, and we made measurements 1 and 7 in the 10
0.36-m 2 mesocosms ( 16). Measurement 1. An index of N availability (NH 4,
NO 2, and NO 3) to plants was
provided by ion-exchange resin (Rexyn, Fisher Scientific) bags ( 18,
19). A bag was buried (15-cm depth) in May and removed in October to
reflect N availability during the plant-growing season, and another bag
was buried in October and removed in May for N availability at
initiation of spring plant growth. N absorbed in resin bags was
correlated with N mineralization (NH 4,
NO 2, and NO 3) measured by
soil cores and in situ incubation tubes (ref. 20;
r2 = 0.47, df = 10,
P < 0.01). Samples were kept frozen until analyzed. Measurement 2. Soil percent water content [(1 − dry weight in g/wet weight in
g) × 100%] was measured with soil cores (3 cm in diameter
× 15 cm deep) taken in May and October. This measure does not reflect
absolute water availability to plants but does reflect whether soil
moisture was greater in mesocosms receiving one type of treatment
compared with mesocosms receiving other treatments. Measurement 3. Plant N content for the most common plant species (E.
smithii, P. pratensis, and P. compressa) was
measured in early June (time of peak biomass) from a 5-g dry sample
(<2% of plant biomass). Measurement 4. Litter N content was measured in October (time of onset of dormancy and
litter manipulation) from a 5-g dry sample (<2% of litter biomass). Measurement 5. Decomposition rates (percent change in dry matter and total N per
period) were measured for common sources (field) of the two most
abundant grasses (P. pratensis and E. smithii).
Four nylon mesh (1-mm mesh) bags of each plant species (10 g collected
in May) were placed on soil in May and collected in October and May
over the next 2 years. Measurement 6. Plant species composition and proportion of bare ground were measured
in July by point-sampling ( 21) 100 points along four transects. Measurement 7. Living-plant aboveground (green) biomass was measured by radiometer
every 2 weeks from May to October. Radiometers measure the ratio of
far-red/infrared reflected radiation, which is used to estimate
living-plant biomass ( 22, 23) by regressions, which are based on
clipped living-plant biomass and radiometer readings for 10 areas of
0.10 m 2 in early May and 4 areas of 0.1
m 2 every 2 weeks until October. Annual
aboveground NPP, less herbivore consumption, equals May plant biomass
plus all positive differences between consecutive biweekly measures
from May to October. Radiometer measures (0.1 m 2)
were made at three permanent locations in each
1-m 2 and 0.36-m 2 area and
at four permanent locations in each 9-m 2 area. Measurement 8. Grasshopper feeding on each of the most common grasses (P.
pratensis, P. compressa, and E. smithii) was
measured as the percentage of 25 blades exhibiting damage. Plant matter was dried at 60°C for 48 h, and soil was dried at
100°C for 48 h. Plant and litter N measurements were made by
extracting N by using micro-Kjeldahl methods ( 28). Inorganic N in the
soil and resin bags was extracted with 2 M KCl ( 24, 25) after samples
were thawed. The extractant N [g/g (dry weight) of soil, plant, or
litter] was assessed colorimetrically with an autoanalyzer ( 24,
26– 28). We expressed measurements from manipulated mesocosms as percent change
relative to control areas since the start of the experiment (May 1994):
where Si is the measure in year
i from mesocosms, So is the
measure from those mesocosms in 1994 (start of experiment),
Ci is the average measure in year
i for 1-m 2 control areas, and
Co is the average measure in 1994 for
1-m 2 control areas. Percent change was normalized
by logit transformation for statistical tests [analysis of variance
(ANOVA), analysis of covariance (ANCOVA), and t tests]. We compared measurements from 1-m2 control
mesocosms with those from 9-m2 areas to determine
whether litter manipulation or mesocosm area created differences. We
compared measurements from 1-m2 control mesocosms
with those from 0.36-m2 mesocosms containing each
year's field density to examine for cage effects. |
Results Control mesocosms (1 m2), where litter was
clipped, did not differ from 9 m2 control areas
for N availability (ANOVA: F = 0.03; df = 1, 28;
P < 0.86), annual aboveground NPP less herbivory
(ANOVA: F = 0.21; df = 1, 39; P <
0.64), and plant species composition (χ2 =
0.14, df = 1, P < 0.85). This indicated that
mesocosm size and litter manipulation methods did not account for
differences between mesocosms where grasshopper density and litter were
manipulated. Control mesocosms (1 m2) did not
differ from 0.36-m2 caged areas that
contained each year's grasshopper density (1994, 1996) for N
availability (ANOVA: F = 0.25; df = 1, 15;
P < 0.63) and annual aboveground NPP less
herbivory (ANOVA: F = 0.59; df = 1, 18;
P < 0.45). This indicated that there were no cage
effects on ecosystem processes. Therefore, we conclude that mesocosms
reflect processes in the larger ecosystem. Next year's aboveground NPP less consumption increases at a decreasing
rate because the previous year's grasshopper density increases from
0% to 125% of field density (Fig.
2A). N availability increases
in a similar manner ( r2 = 0.68,
df = 4, P < 0.04) and changes in N correlate with
changes in aboveground NPP less consumption (Fig.
2B). Because N additions increase NPP at this site
( 11), grasshopper herbivory appears to increase aboveground NPP after
consumption by increasing available N for plant growth. Over the 5
years of the study, herbivory increased aboveground NPP by 19.9–32.9 g
(dry weight) per m 2 per year.
| Figure 2 Impacts in 1995 (red) and 1996 (green) of grasshopper density (0%,
50%, and 125% of year's field density) on percent change in
aboveground NPP less herbivory (A) and its relationship
to percent change in N availability (B). |
We examined how grasshoppers increase NPP by using the
1-m2 mesocosm experiments as follows: Experiment 1: Fast Cycle Experiment (Varied Grasshopper
Density/ Control Litter). Aboveground NPP less consumption was 4–12% greater when grasshoppers
were at 125% versus 50% of field density (Fig.
3; ANOVA: F = 6.8;
df = 1, 26; P < 0.01). This is expected if the
fast cycle's magnitude is increased when more grass is produced at
higher densities, which makes more N available to plants.
| Figure 3Percent increase (mean ± SEM) in aboveground NPP with increased
(125%) compared with decreased (50%) grasshopper density for fast
(red), slow (green), and combined fast and slow cycle (blue) effects.
Cross-hatching denotes the (more ...) |
Experiment 2: Slow Cycle Experiment (Control Grasshopper
Density/ Varied Litter). Aboveground NPP less consumption was 9–20% greater with litter from
mesocosms with 125% versus 50% field density (Fig. 3; ANOVA:
F = 21.71; df = 1, 26; P <
0.0001). This is expected if grasshoppers speed up the slow cycle,
releasing more N by decomposition of litter. Experiment 3: Combined Fast and Slow Cycle Experiment (Varied
Grasshopper Density/in Situ Litter). Aboveground NPP less consumption was 4–18% greater when grasshoppers
were at 125% versus 50% of field density (Fig. 3; ANOVA:
F = 4.39; df = 1, 26; P < 0.04).
This is expected given that both fast and slow cycles increase NPP.
However, when combined effects were correlated with associated fast
(experiment 1) and slow cycle (experiment 2) effects, the fast cycle
was found to diminish the slow cycle, and the slow cycle was twice as
important as the fast cycle ( r2 =
0.99, df = 3, P < 0.003). Antagonism between fast
and slow cycles is expected, because greater consumption (increased
fast cycle effects) reduces litter abundance, which diminishes the
magnitude of the slow cycle. Our result that NPP enhancement is
greatest when grasshopper density is neither too great nor too small
(Fig. 4) supports this “tradeoff”
between fast and slow cycle effects.
| Figure 4 A regression relating changes in aboveground NPP with grasshopper
density is presented. |
As expected, N availability to plants is greater when grasshoppers were
at 125% versus 50% of field density (Fig.
5: t = 3.10, df = 6,
P < 0.02), and we suggest that this increases NPP
because N additions increase NPP at this site ( 11). Grasshoppers
influence the more important slow cycle by changing the amount of
litter and its N content. As consumption increases (125% versus 50%
field density), litter abundance decreases (Fig. 5: t =
2.9, df = 6, P < 0.04), which reduces the amount
of N contained in the slow cycle. However, as consumption increases,
litter N content increases (Fig. 5: t = 4.69, df =
6, P < 0.009), which increases the amount of N
contained in the slow cycle and its rate of cycling. Slow
cycle speed increases because decomposition is more rapid as
litter N content increases ( r2 = 0.91,
df = 4, P < 0.04). For example, E.
smithii decomposed 11% slower than P. pratensis
( t = 5.10, df = 2, P < 0.03), and
E. smithii contained 28% less N than P.
pratensis ( t = 13.76, df = 8,
P < 0.0001). Increased litter N content, in part, is
due to increases in relative abundance of grasses with greater N
content ( P. pratensis and P. compressa versus
E. smithii; Fig. 5: t = 48.18, df = 6,
P < 0.0005), which is partially due to preferential
feeding on E. smithii (χ 2 = 9.45,
df = 1, P < 0.002).
| Figure 5 Average percent changes (±SEM) in ecosystem characteristics with
decreased (red) and increased (green) grasshopper densities. |
Increased grasshopper density can counter the slow cycle in two ways.
( i) Less litter might increase soil evaporation so that
plants become water-limited, but soil moisture was not diminished in
our experiments (Fig. 5: t = 0.55, df = 14,
P < 0.70). ( ii) Less litter and higher
litter and soil N might make the soil microbes that are responsible for
decomposition carbon-limited rather than N-limited, and thereby,
decrease decomposition rates ( 29, 30). However, decomposition rates for
common litter sources did not change with grasshopper density in our
experiments (Fig. 5: t = 0.59, df = 4,
P < 0.62). Therefore, countermechanisms to
herbivory-enhancing slow-cycle effects and aboveground NPP were not
observed. All of the above fast, slow, and combined cycle effects were maintained
in the last year (e.g., NPP in 1999; Fig. 3) when mesocosms were not
caged, so that all areas were open to field grasshopper densities (for
fast cycle, ANOVA: F = 0.2; df = 1, 26;
P < 0.66; for slow cycle, ANOVA: F =
0.57; df = 1, 26; P < 0.46; for combined cycles,
ANOVA: F = 3.15; df = 1, 26; P <
0.09). This suggests long-lasting influences of grasshoppers on
nutrient cycling and NPP. |
Discussion Grasshopper herbivory appears to affect the Palouse prairie in the
manner depicted in Fig. 1B, because N availability for
plants and plant abundance increased with grasshopper density. Plant
abundance probably increased because of greater N availability, because
N additions are known to increase NPP at this site ( 11). In this
scenario (Fig. 1B), N availability is primarily enhanced
when the herbivore speeds up the slow cycle, which requires the
herbivore to feed preferentially on plants of lower N content that
decompose more slowly, as observed for E. smithii and
P. pratensis. The above ecosystem changes (Fig. 1B) may be self-enhancing
(positive feedback) and no longer dependent on herbivory, if plants
with higher N content and decomposition rates are competitively
superior to other plants once N is more available. P.
pratensis is competitively superior to E. smithii at
higher N availability ( 31, 32), and Poa increased relative
to E. smithii (Fig. 5). Poa's increase is not
solely caused by preferential feeding by grasshoppers on E.
smithii, because Poa increased when grasshopper
consumption was held constant and litter was manipulated (slow cycle
experiment 1; t = 5.42, df = 4, P
< 0.005). Self-enhancement was further supported in 1999 when
mesocosms were not caged and grasshoppers had equal access to all
areas, because increased plant abundance and N availability were
maintained in areas previously experiencing higher grasshopper
densities (Fig. 2). The observed increase in plant abundance is not due to herbivores
benefiting consumed plants in a mutualistic fashion ( 33, 34), because
consumed plants do not grow or survive as well as unconsumed plants
( 16). Rather, consumed and unconsumed plants grow better when herbivory
makes more nitrogen available, an ecosystem function. Thus, herbivory
can increase plant abundance if neither too little nor too much is
consumed (Fig. 3). If too little is consumed, herbivory will have too
little influence on nutrient cycling to increase plant production. If
too much is consumed, herbivory will depress plant growth and survival
more than can be compensated for by greater growth as nutrient cycling
increases. In conclusion, our results indicate that ecosystem processes (nutrient
cycling), functions (NPP) and structure (plant composition) are
interrelated and strongly influenced by biotic interactions ( 35– 37).
We cannot assess how typical our observations are for terrestrial
systems. Other grasslands have lower grasshopper densities ( 38, 39) and
nutrient cycling that depends more on fire ( 40). Mammalian herbivory is
not equivalent to grasshopper herbivory, because mammals, especially
ungulates, uproot and trample plants and compact soil, which can
decrease nutrient cycling and NPP ( 41). However, generalizing about
herbivory's ecosystem effects depends on whether herbivores
preferentially feed on slower decomposing plants. Grasshoppers within 4
km of our study site fed preferentially on P. pratensis over
E. smithii. P. pratensis decomposed faster and had higher N
content, providing conditions for herbivory to diminish nutrient
cycling and NPP (Fig. 1A). Consequently, ecosystem
processes may vary because of biotic influences at smaller spatial
scales than typically considered. |
Acknowledgments D. Branson and J. Chase aided in establishing the long-term
experiments. We thank The Utah State Agricultural Experiment Station
and The National Science Foundation (DEB-9317984, DEB-9707654) for
financial support. |
Abbreviation NPP | net primary production |
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References 1. Hutchinson, G E; Deevey, E S. Biol Prog. 1949;1:325–359. 2. McNaughton, S J; Ruess, R W; Seagle, S W. BioScience. 1988;38:794–800. 3. Pastor, J; Naiman, R J. Am Nat. 1992;139:690–705. 4. Pastor, J; Naiman, R J; Dewey, B; McInnes, P. BioScience. 1988;38:770–777. 5. DeAngelis, D L. Dynamics of Nutrient Cycling and Food Webs. London: Chapman & Hall; 1992. 6. Pastor, J; Dewey, B; Naiman, R J; McInnes, P F; Cohen, Y. Ecology. 1993;74:467–480. 7. Frank, D A; McNaughton, S J. Oecologia. 1993;96:157–161. 8. Holland, E A; Parton, W J; Detling, J K; Coppock, D L. Am Nat. 1992;140:685–706. 9. Seastedt, T R; Crossley, D A. BioScience. 1984;34:157–161. 10. Lovett, G M; Ruesink, A E. Oecologia. 1996;104:133–138. 11. Schmitz, O J. Oecologia. 1993;93:327–335. 12. Shelford, V E. The Ecology of North America. Urbana: Univ. Illinois Press; 1963. 13. Sheldon, J K; Rogers, L E. Oecologia. 1978;32:85–92. 14. Watts, L R; Stewart, G; Connaughton, C; Palmer, L J; Talbot, M W. US Senate Doc. 1936;199:501–522. 15. French, N R; Steinhorst, R K; Swift, D M. Perspectives in Grassland Ecology. French N. , editor. New York: Springer; 1979. pp. 59–87. 16. Belovsky, G E. Grasshoppers and Grassland Health. Lockwood J A, Latchininsky A V, Sergeev M G. , editors. Dordrecht, The Netherlands: Kluwer; 2000. pp. 7–29. 17. Onsager, J A; Henry, J E. Acridida. 1977;6:231–237. 18. Binkley, D; Matson, P. Soil Sci Soc Am J. 1983;47:1050–1052. 19. Binkley, D. Soil Sci Soc Am J. 1984;48:1181–1184. 20. Binkley, D; Hart, S C. Adv Soil Sci. 1989;10:57–112. 21. Daubenmire, R F. Plants and Environment. New York: Wiley; 1947. 22. Pearson, R L; Miller, L D; Tucker, C J. Applied Optics. 1976;15:416–418. 23. Milton, E J. Int J Remote Sensing. 1987;8:1807–1827. 24. Page, A L; Miller, R H; Keeney, D R. Methods of Soil Analysis. Madison, WI: Am. Soc. Agron. Soil Sci. Soc. Am.; 1982. , Part 2. 25. Adamsen, F J; Bigelow, D S; Scott, G R. Com Soil Sci Plant Anal. 1985;16:883–898. 26. Adamski, J M. Anal Chem. 1976;48:1194–1197. [PubMed]27. Nelson, D W; Sommers, L E. J Assoc Off Agric Chem. 1980;63:770–778. 28. Association of Official Agricultural Chemists. Official Methods of Analysis. Washington, DC: Assoc. Off. Agric. Chem.; 1984. 29. Seastadt, T R. The Changing Prairie: North American Grasslands. Joern A, Keeler K H. , editors. New York: Oxford Univ. Press; 1995. pp. 157–174. 30. Zheng, D W; Ågren, G I; Bengtsson, J. Oikos. 1999;86:430–442. 31. Smika, D E; Hass, H J; Power, J F. Agron J. 1965;57:483–486. 32. Tilman, D. Plant Strategies and the Dynamics and Structure of Plant Communities. Princeton: Princeton Univ. Press; 1988. 33. Dyer, M; Bokhari, U G. Ecology. 1976;57:762–772. 34. Owen, D F; Wiegert, R G. Oikos. 1982;38:258–259. 35. Tilman, D. Nature's Services: Societal Dependence on Natural Ecosystems. Daly G C. , editor. Washington, DC: Island; 1997. pp. 685–700. 36. Chapin, F S; Walker, B H; Hobbs, R J; Hooper, D U; Lawton, J H; Sala, O E; Tilman, D. Science. 1997;277:500–504. 37. Hooper, D U; Vitousek, P M. Science. 1997;277:1302–1305. 38. Evans, E W. Ecology. 1989;70:435–444. 39. Mitchell, J E; Pfadt, R E. Environ Entomol. 1974;3:358–360. 40. Bragg, T B. The Changing Prairie: North American Grasslands. Joern A, Keeler K H. , editors. New York: Oxford Univ. Press; 1995. pp. 49–81. 41. Wallace, L L; Dyer, M I. The Changing Prairie: North American Grasslands. Joern A, Keeler K H. , editors. New York: Oxford Univ. Press; 1995. pp. 177–198. |
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