Download Insect herbivory in an experimental agroecosystem: the relative

Oikos 118: 14771486, 2009
doi: 10.1111/j.1600-0706.2009.17720.x,
# 2009 The Authors. Journal compilation # 2009 Oikos
Subject Editor: Daniel Gruner. Accepted 6 April 2009
Insect herbivory in an experimental agroecosystem: the relative
importance of habitat area, fragmentation, and the matrix
Kyle J. Haynes and Thomas O. Crist
K. J. Haynes ([email protected]), Dept of Biology, Univ. of Louisiana, PO Box 42451, Lafayette, LA 70504, USA. T. O. Crist, Dept of
Zoology, Miami Univ., Oxford, OH 45056, USA.
Habitat area, fragmentation, and the surrounding matrix influence levels of herbivory in various ecosystems, but the
relative importance of these effects has rarely been assessed. We compared levels of herbivory and densities of dominant
arthropod herbivores (the hemipteran insects Agallia constricta, Empoasca fabae, Therioaphis trifolii, Lygus lineolaris and
Halticus bractatus) among experimental plots that varied in the area and fragmentation of clover habitat and the
composition of the matrix (bare ground or grass) surrounding clover habitat. To assess levels of herbivory, we compared
clover biomass within herbivore exclosures to the biomass accessible to herbivores. The area and fragmentation of clover
habitat, as well as matrix composition, significantly influenced the collective densities of herbivores, although each species
exhibited unique responses to habitat structure. Herbivory was strongest in plots with large (64 m2) as compared to small
(16 m2) amounts of clover habitat. The difference in clover biomass between the inside and outside of exclosures
increased significantly with increasing density of Empoasca fabae but was unrelated to the densities of the other herbivores,
suggesting that Empoasca fabae was an exceptionally important herbivore in this system. This study supports the view that
herbivore densities and herbivory generally increase with increasing area of plant monocultures, but emphasizes that levels
of herbivory may be driven primarily by one or a few key herbivore species.
There is a large body of literature on the effects of the area
and fragmentation of a focal habitat type and composition
of the surrounding matrix on the distributions and
abundances of species (Moilanen and Hanski 1998,
Debinski and Holt 2000, Tscharntke et al. 2002, Cronin
2003). The effects of these factors on levels of herbivory
have received a smaller, but still considerable, amount of
attention (Thies et al. 2003, Östergård and Ehrlén 2005,
Valladares et al. 2006). However, few studies have evaluated
the relative importance of habitat area, fragmentation, and
matrix composition to levels of herbivory (but see Diekötter
et al. 2007).
If one or a few herbivore species are responsible for most
of the herbivory in a given community, the feeding
specialization of these key species may determine the
manner and strength with which habitat area, fragmentation and matrix composition affect levels of herbivory.
Positive, negative, and neutral density responses to habitat
area are frequently observed (Connor et al. 2000, Matter
2000, Zaviezo et al. 2006), but species with strong
preferences for a focal habitat type are more likely to
display positive densityarea relationships in the preferred
habitat type than are habitat-generalist species (Hambäck
et al. 2007). The fragmentation of a focal habitat type is
generally thought to adversely affect populations but, in
fact, positive effects of habitat fragmentation may be more
likely for species that use multiple habitat types (Law and
Dickman 1998). Fragmentation of a focal habitat type may
have positive effects on a habitat generalist by increasing the
extent to which complementary resources in the matrix
occur within the organism’s dispersal range (Law and
Dickman 1998, Fahrig 2003). Finally, whereas habitat
specialists may respond more strongly to the area and
fragmentation of a focal habitat type, habitat generalists
may be more sensitive to the composition of the matrix
(Brotons et al. 2003, Steffan-Dewenter 2003). For example,
Haynes et al. (2007) found that (adult) densities of the
polyphagous grasshopper Melanoplus femurrubrum in a
focal habitat type (clover) were more strongly influenced
by the availability of complementary resources in the matrix
than by the area and fragmentation of the focal habitat.
Assessing the relative importance of different attributes
of habitat structure and composition to herbivory presents
particular challenges. The habitat attributes of interest often
covary in natural landscapes, hindering a researcher’s ability
to isolate their independent effects. For example, Fahrig’s
(2003) review revealed that most studies examining the
effects of habitat area and fragmentation on population or
community dynamics confounded the effects of these two
factors. Furthermore, plant size or quality may covary with
landscape features (e.g. matrix composition; Haynes and
Cronin 2004), making it difficult to isolate the effects of
herbivory from the effects of other factors on measures of
plant growth (e.g. biomass, leaf area). One approach to
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evaluating the relative importance of different habitat
attributes to herbivory is to combine observational data
on herbivore densities and plant growth with experimental
manipulations of both the habitat attributes and herbivore
densities.
In this study, we examine the relative importance of
habitat area, habitat fragmentation, and matrix composition
in determining levels of herbivory. We created a model
agroecosystem consisting of replicated plots containing
subplots of the forage-crop plant red clover Trifolium
pratense. We manipulated the area and fragmentation of
clover habitat and composition of the matrix (grass or bareground) according to a factorial design. Unlike many
previous experimental studies (Fahrig 2003), our design
manipulated habitat area independently of habitat fragmentation. In the experimental plots, we recorded the
densities of the five numerically dominant herbivores:
Agallia constricta, Empoasca fabae, Therioaphis trifolii, Lygus
lineolaris and Halticus bractatus. To quantify levels of
herbivory, we placed small herbivore exclosures in the
experimental plots. We also examined the impacts of each
herbivore species on clover biomass based on regressions of
paired exclosure-control differences in clover biomass and
herbivore abundance. Since clover represents the preferred
habitat for all of the dominant herbivore species (Methods),
we expected that densities and herbivory would increase
with the area of clover habitat. We also expected that
habitat-generalist species would have higher densities in
clover habitat bordered by the grass matrix because it may
provide complementary resources. Furthermore, we expected fragmentation to positively affect habitat generalists.
Effects of habitat fragmentation on specialist herbivores
may be positive or negative, because although dispersal
mortality and densities of habitat-generalist predators may
increase with fragmentation, parasitoids often are less
effective in fragmented landscapes (Kruess and Tscharntke
1994, Tscharntke and Brandl 2004).
Methods
Study system
The focal plant in this study was the herbaceous, perennial
red clover Trifolium pratense. Red clover is an important
forage crop worldwide, both in intensely managed cultivation and extensively managed pastures (Guretzky et al.
2005), and is commonly grown in clover/grass polycultures
(Heath et al. 1973). The dominant herbivores of clover
at our study site were all Hemiptera. They consisted of the
leafhoppers Agallia constricta and Empoasca fabae (Cicadellidae), the aphid Therioaphis trifolii (Aphididae), the plant
bug Lygus lineolaris (Mirididae), and the fleahopper Halticus
bractatus (Mirididae). Therioaphis trifolii is only known to
feed on legumes (e.g. alfalfa, clovers; Milne 1998, Nair et al.
2003). The remaining herbivore species are known to feed
on a wide variety of herbaceous plants (Osborn 1928,
Henry 1983, Young 1986, USDA 2002), but were found in
much higher densities on clover than grass in our system
(Haynes unpubl.).
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Experimental plots
We conducted the experiment in the summer of 2006 in a
2-ha field at Miami Univ. Ecology Research Center near
Oxford, OH. Two years earlier (in 2004), we created
replicated 14 14 m plots, each containing four patches
(or subplots) of red clover. The clover subplots varied in
fragmentation (continuous or isolated by 2 m), habitat area
(4 or 16 m2), and matrix type (grass or bare ground)
according to a fully factorial design (Fig. 1). Each
combination of fragmentation, area, and matrix was
originally replicated in four separate plots, and arranged
in a completely randomized design. However, we excluded
two plots from the experiment due to clover mortality in
the spring of 2006, leaving two treatment combinations
(large clover area/bare-ground matrix/fragmented and small
clover area/grass matrix/continuous) with three replicate
plots. We established the clover subplots and grass matrix
by sowing the plots with seeds of red clover Trifolium
pratense and orchard grass Dactylis glomerata. We maintained bare-ground matrix within experimental plots and in
the 8-m strips between plots by applying herbicide at
monthly intervals. We kept the grass matrix free of forbs by
applying 2,4-D herbicide annually in early summer (June).
We mowed the grass monthly to minimize variation in the
height of vegetation among plots because the structural
complexity of matrix habitats may influence rates of
movement into and out of focal patches (Kareiva 1985,
Lawrence and Bach 1989). Finally, we regularly weeded all
clover habitat.
Herbivory experiment
To quantify the effects of herbivores on clover biomass, we
placed small exclosures in one randomly selected subplot
per plot. Within each selected subplot, we placed the
exclosure at a stratified random location. An exclosure
consisted of fine-mesh (0.25 mm) polyester ‘no-see-um’
netting sewn to fit over a small (0.25w 0.4l 0.5h m)
frame constructed of PVC tubing. We pushed the legs of
the frame 5 cm into the soil. We prevented insects from
entering the exclosures by anchoring the base of the netting
firmly against the ground using iron rods. To kill any
insects that may have been inside the exclosures, we sprayed
0.15 l of an aqueous solution containing organic pyrethrin
Figure 1. Aerial view of the field containing 36 14 14 m
experimental plots. Photo credits: Beth Dickman.
pesticide through the netting onto the clover inside. Because
the pesticide was diluted in water (1:500 dilution), we
sprayed an equivalent amount of water onto an equivalent
area of clover within the same subplot, which was used as a
control. We assigned each control area to a stratified
random location. Experiments testing for potential effects
of the exclosures or pesticide on clover are described in the
following section.
The exclosures were in place for a 6-week period in 2006
while insects were at peak abundance (mid July to late
August). After six weeks, we compared clover biomass
inside the exclosures to clover biomass at control locations.
We clipped the clover biomass at these two locations using a
rectangular quadrat (0.2 0.35 m) to standardize the area
sampled. The plant material was dried at 608C for 48 h and
then weighed.
We evaluated effects of herbivore exclusion on clover
biomass using a profile ANOVA (Tabachnick and Fidell
2000). This procedure, which is comparable to repeated
measures ANOVA, allows for the two clover biomass
measurements (exclosure and control) taken from each
plot to be non-independent. Clover biomass measures taken
from the same plot could potentially be more similar than
measures taken in different plots due to differences in
abiotic conditions (e.g. soil quality). We also used the
profile ANOVA to test whether the effect of herbivore
exclusion on clover biomass was dependent on clover
habitat area, habitat fragmentation or matrix composition.
In addition, we tested whether clover biomass at control
locations was influenced by the plot treatments using a
three-way ANOVA. The clover biomass data were squareroot transformed prior to these analyses to homogenize
variances and improve normality of residuals. We also
removed a linear spatial trend in the control-location
biomass data that we found by performing a regression
against the x and y spatial positions of the plots (Crist et al.
2006). We did not use detrended data in the profile
ANOVA, however, because this would preclude direct
comparison of differences in biomass inside and outside
of exclosures within each plot.
We measured the densities of the herbivore species in the
clover habitat of each experimental plot in mid July and late
August. For each plot, we collected insects from the subplot
containing the herbivore exclosure using a D-vac insect
vacuum. Within each of these subplots, we placed the
0.08 m2 sampling head of the D-vac over the clover at four
stratified random locations. The suction samples were
transferred to plastic bags and placed in a freezer until all
insects were dead. We then counted the insects using a
stereoscopic dissecting microscope. To evaluate the relationships between the densities of individual herbivore species
and the level of herbivore damage to clover, we performed
multiple regression analysis using the densities of each
herbivore species as predictor variables and the difference in
clover biomass between the exclosure and control location
(exclosure biomass control biomass) as the response
variable. In addition, we examined the collective effects of
the herbivores on clover biomass by performing a linear
regression with total herbivore density as the predictor
variable. We also evaluated the effects of the area and
fragmentation of clover habitat and matrix composition on
the densities of the five herbivore species using MANOVA.
Following significant results from a MANOVA, we evaluated the effects of habitat area, fragmentation, and matrix
composition on the individual herbivore species using
univariate ANOVA (Quinn and Keough 2002). We
analyzed the July and August data separately because the
effects of herbivores on clover biomass could potentially shift
over time. To protect against inflated type I error due to
conducting two non-independent tests (on July and August
densities), we set the significance level for MANOVA and
multiple regression analyses to a 0.025 (0.05/2). To
minimize heterogeneity of variance and to normalize
residuals, the densities of each insect species were squareroot transformed prior to the analyses. As with the clover
biomass data, we removed linear spatial trends in the
densities of three herbivore species (Halticus bractatus in
July and August, Empoasca fabae in July, and Therioaphis
trifolii in July) prior to fitting the MANOVA and ANOVA
models.
Insect dispersal or spatially correlated environmental
conditions (e.g. soil quality) could potentially have lead to
non-independence of the insect density or clover biomass
measurements taken from neighboring plots. We tested for
spatial autocorrelation of the residuals from the ANOVA
and regression models (Ver Hoef and Cressie 1993) using
the nonparametric spatial correlation function (Bjørnstad
and Falck 2001), which revealed that none of the residuals
exhibited significant spatial autocorrelation at any lag distance between plots.
Exclosure and pesticide effects on clover
Based on a previous field study (Cronin 2007) using insect
cages similar to ours, we did not expect the exclosures to
affect clover biomass. Nonetheless, we conducted a separate
but concurrent experiment to examine exclosure effects on
plant biomass. We built ‘leaky’ exclosures, which allowed
insects to access the clover inside. These ‘leaky’ exclosures
were identical to the exclosures used in the herbivory
experiment except that there were two large rectangular
holes in the netting on opposite sides of the exclosure. The
holes were 10 cm wide and extended from the soil to a
height of 20 cm. We placed ten ‘leaky exclosures’ in a small
secondary field (0.2 ha) of red clover 1 km from the
experimental plots. Exclosures and paired control locations
were arrayed along a linear transect. Exclosure-control pairs
were spaced 2 m apart. We placed each exclosure 1 m to
the left or right of the transect (at random) and located the
paired control on the opposite side (also 1 m from the
transect). After six weeks, we sampled clover biomass at
each location using methods described previously. We
tested whether clover biomass differed between the exclosures and controls using a paired t-test. Prior to this
analysis, the clover biomass data were ln-transformed.
We also experimentally tested whether clover sprayed
with the aqueous pesticide solution differed from clover
sprayed with water, as a check on the direct effects of
pyrethrins on clover growth. We established 20 herbivore
exclosures in the secondary clover field. We sprayed half of
the exclosures with the pesticide solution and other half
with an equivalent amount of water. The treatments were
assigned to the exclosures at random and clover biomass was
1479
Results
Herbivory experiment
We found a significant interactive effect of clover habitat
area and matrix composition on clover biomass at control
locations (Table 1). In plots with 64 m2 of clover habitat,
biomass was relatively constant across the combinations of
fragmentation and matrix composition (Fig. 2). On the
other hand, clover biomass in plots with 16 m2 of habitat
was substantially higher in plots with bare-ground matrix
than in plots with grass matrix.
Clover biomass was significantly higher inside the
experimental exclosures compared to control locations
with no exclosure (Table 2, Fig. 3). In addition, the effect
of the exclosures on clover biomass differed according to
clover habitat area. In plots with 16 m2 of clover habitat,
clover biomass did not differ strongly between exclosures
and controls. In plots with 64 m2 of clover habitat,
however, clover biomass was 1.4 times higher inside the
exclosures. Thus herbivores had strong effects on clover
biomass in larger patches of clover. Herbivory effects on
clover biomass were unrelated to matrix composition and
habitat fragmentation.
Based on a multiple regression analysis, the differences in
biomass between the exclosures and controls (exclosure
biomass control biomass) were not significantly related to
the July densities of any of the herbivore species (Table 3).
However, there was a positive relationship between the
difference in biomass and the density of Empoasca fabae in
August (Table 3, Fig. 4). The August densities of all other
insect species were unrelated to the difference in biomass
between exclosures and controls. For the August data, a
regression model including all of the herbivore species
explained 26.6% of the variation in the biomass differential
among plots (based on the r2 value). Despite the apparent
effects of Empoasca fabae on clover biomass, we found
no relationship between total herbivore density and the
biomass differential in July (biomass differential
1.121 (density)0.564.823, n 30, p 0.585, r2 0.011) or August (biomass differential10.102 (density)0.5 43.323, n 30, p0.287, r2 0.04).
Table 1. ANOVA results on the effects of habitat area, habitat
fragmentation and matrix composition on clover biomass in control
locations. Significant results at the a 0.05 level are shown in bold.
Source
DF
F
p
Area
Matrix
Fragmentation
AreaMatrix
AreaFragmentation
MatrixFragmentation
AreaMatrixFragmentation
Error
1
1
1
1
1
1
1
22
0.054
3.026
1.068
9.544
0.094
0.090
0.439
0.819
0.096
0.313
0.005
0.763
0.767
0.514
1480
20
Sq. root (clover biomass [g m-2])
measured after six weeks. We assessed whether clover
biomass differed between exclosures sprayed with pesticide
solution or water with ANOVA. Clover biomass was lntransformed prior to this analysis.
16
Bare, continuous
Bare, fragmented
Grass, continuous
Grass, fragmented
1
1, 2
12
1, 2
2
8
4
0
Large
Small
Habitat area
Figure 2. Effects of habitat area, habitat fragmentation, and
matrix composition on clover biomass in control locations
(means1 SE). Means labeled by different numbers respresent
significant differences at the a0.05 level (Tukey’s HSD tests
evaluated differences among all area and matrix combinations).
In July, the densities of herbivore species were collectively influenced by all three main effects, clover area, clover
fragmentation, and matrix composition (Appendix 1).
Three of the five herbivore species displayed a trend
towards higher density in the plots with greater clover
area (Halticus bractatus, Lygus lineolaris, Empoasca fabae ;
Fig. 5), though this trend was significant only for Halticus
bractatus (Appendix 2). Densities of this species were 3.2
times greater in plots with 64 compared to 16 m2 of clover
habitat. Conversely, Therioaphis trifolii density was 3.5
times higher in the latter plots. Matrix composition
significantly affected the densities of both Therioaphis
trifolii and Agallia constricta (Appendix 2). Therioaphis
trifolii densities were 5.8 times higher in clover habitat
embedded within the bare-ground matrix. Agallia constricta
exhibited the opposite response; densities were twice as high
in clover habitat within the grass matrix. Finally, fragmentation did not significantly affect the July densities of any
single herbivore species. In August, herbivore densities were
not collectively influenced by any of the experimental
factors (Appendix 1). With regard to the effect of clover
habitat area, however, all of the herbivore species individually exhibited the same trends that were observed in July.
Table 2. Results from a profile ANOVA on effects of herbivore
exclosure, habitat area, matrix composition, and habitat fragmentation on clover biomass. Significant results at the a 0.05 level are
shown in bold.
Source
DF
F
p
Exclosure
ExclosureArea
ExclosureMatrix
ExclosureFragmentation
ExclosureAreaMatrix
ExclosureAreaFragmentation
ExclosureMatrixFragmentation
ExclosureAreaMatrixFragmentation
Error
1
1
1
1
1
1
1
1
22
7.178
5.256
1.036
0.028
1.862
0.512
0.828
0.168
0.014
0.032
0.320
0.868
0.186
0.482
0.373
0.686
210
300
Biomass differential (residuals)
Bare, continuous
Biomass differential (g m-2)
Bare, fragmented
Grass, continuous
140
Grass, fragmented
70
0
200
100
0
-100
-200
-300
-400
0
-70
1
2
3
4
5
6
7
Square root (no. m-2)
Large
Small
Habitat area
Figure 3. Differences in clover biomass between herbivore
exclosures and control locations (biomass inside exclosures control biomass, means1 SE). Results from a profile ANOVA
(Table 2) showed that the effect of herbivore exclusion on biomass
was greater in plots with 64 m2 of clover habitat than in plots with
16 m2 of clover habitat.
Exclosure and pesticide effects on clover
Our experimental test for enclosure effects on clover
biomass revealed no difference between controls and the
‘leaky’ exclosures (0.00890.427 g m 2, mean difference
of ln(g m 2) 995% CI, t9 0.466, p 0.652), which
allowed insects to move freely in or out of the exclosures. In
addition, clover biomass did not differ between exclosures
sprayed with pesticide solution (82.498.4 g m 2, mean9
1 SE) and exclosures sprayed with water (79.696.1 g m2;
F1,18 0.003, p0.955).
Figure 4. Relationship between the density of Empoasca fabae and
the effect of herbivores on clover biomass. The effect of herbivores
on clover biomass was measured as the difference in clover biomass
between herbivore exclosures and control locations (biomass inside
exclosure control biomass). To indicate the effect of Empoasca
fabae alone on clover biomass, the residuals from a model
including all of the herbivores except Empoasca fabae were
regressed against the density of Empoasca fabae (biomass differential [residuals] 38.26(Empoasca fabae density)0.5 114.21,
n30, r2 0.219).
exclosures and controls to differences in the intensity of
herbivory. Thus, herbivory was much stronger in plots with
greater clover area. Similar findings of insect herbivory
increasing with increasing patch area have been reported in
other systems (e.g. understory herbs, forest fragments;
Östergård and Ehrlén 2005, Valladares et al. 2006). Unlike
clover area, the fragmentation of clover habitat and
composition of the matrix had no effects on herbivory.
Habitat-structure effects on herbivore densities and
herbivory
Discussion
Our study shows that herbivore damage to red clover was
influenced by the area of clover habitat. We found a
substantial difference in clover biomass between exclosures
and open controls in plots with 64 m2 of clover habitat, but
no such difference in biomass in plots with 16 m2 of clover
habitat. Because we found no exclosure effects on clover
biomass, we attribute differences in clover biomass between
The strong effect of habitat area on herbivory may be partly
explained by the collective effects of habitat area on
herbivore densities. Densities of three of the five herbivore
species (Halticus bractatus, Lygus lineolaris and Empoasca
fabae) increased with increasing clover area, whereas two
herbivore species (Therioaphis trifolii and Agallia constricta)
exhibited negative responses to increasing clover area (these
responses were statistically significant only for Halticus
Table 3. Results from multiple regression analyses examining the relationships between the densities of each herbivore species in July and
August and the clover biomass differential (biomass inside exclosure biomass outside exclosure). Densities were square-root transformed.
Significant results at the a0.05 level are shown in bold.
Herbivore species
Agallia constricta
Empoasca fabae
Therioaphis trifolii
Lygus lineolaris
Halticus bractatus
July
August
Coefficient
t
p
Coefficient
t
p
3.990
2.434
0.843
10.841
14.733
0.400
0.303
0.119
0.507
1.124
0.693
0.764
0.906
0.617
0.272
5.490
39.112
10.791
8.444
5.545
1.153
2.634
1.148
0.468
0.679
0.735
0.015
0.260
0.644
0.504
July: r2 0.101.
August: r2 0.266.
1481
Bare, continuous
Bare, fragmented
Grass, continuous
Grass, fragmented
Agallia constricta
120
Grass > Bare
(p < 0.001)
50
40
30
20
10
0
80
40
0
Empoasca fabae
30
30
20
20
10
10
Density (no. m-2)
0
2500
2000
1500
1000
500
0
0
Therioaphis trifolii
Small > Large
(p = 0.005)
Bare > Grass
(p= 0.002)
50
40
30
20
10
0
Lygus lineolaris
25
20
15
10
5
0
10
8
6
4
2
0
Halticus bractatus
50
40
30
20
10
0
Large > Small
(p = 0.001)
Large
Small
100
80
60
40
20
0
Large
Small
Habitat area
Habitat area
July
August
Figure 5. Effects of habitat area, habitat fragmentation, and matrix composition on the densities of Agallia constricta, Empoasca fabae,
Therioaphis trifolii, Lygus lineolaris and Halticus bractatus (means1 SE). After finding that the densities of the herbivore species were
collectively influenced by the experimental factors in July, but not August (based on MANOVAs), the July data was further analyzed by
performing separate ANOVAs for each herbivore species (Quinn and Keough 2002). Significant results at the a0.05 level are listed in
the figure.
bractatus and Therioaphis trifolii). Positive densityarea
relationships in herbivorous insects are traditionally thought
to result from increased rates of immigration into and (or)
decreased rates of emigration out of large host-plant patches
in order to maximize feeding efficiency (the resource
concentration hypothesis; Root 1973). Given that all of
the herbivore species appeared to strongly prefer the clover
habitat over the grass matrix (all exhibited much higher
densities in clover; Haynes unpubl.), this hypothesis may
explain the positive responses of Halticus bractatus, Lygus
lineolaris and Empoasca fabae to increasing clover area. Even
among habitat-specialist species, however, negative density
area relationships, like we report for Therioaphis trifolii and
Agallia constricta, are not atypical. In a meta-analysis,
Hambäck and Englund (2005) found that various aphid,
leafhopper and planthopper species exhibited densityarea
relationships ranging from slightly negative to slightly
positive. Negative densityarea relationships, they showed,
1482
are likely for species exhibiting area-dependent immigration
and perimeter-dependent emigration (Hambäck and Englund 2005). An alternative explanation for the negative
responses of Therioaphis trifolii and Agallia constricta to
increasing clover area is that predation pressure on these
species was higher in plots with large clover subplots.
Reductions in habitat area are often expected to have
stronger adverse effects on predators than on their prey
(Holt et al. 1999, Tscharntke and Brandl 2004). One major
consequence of this effect is that reducing the area of habitat
could potentially lead to outbreaks of herbivores and plant
destruction (With et al. 2002). If predation was responsible
for the negative densityarea relationships of Therioaphis
trifolii and Agallia constricta, this effect was not sufficient to
have a cascading influence on clover biomass.
For herbivores that forage in multiple habitat types,
densities may often be elevated in patches of the focal
habitat type that border matrix habitat types that provide
supplementary or complementary resources (Dunning et al.
1992, Haynes et al. 2007). Consistent with this hypothesis,
we found that Agallia constricta, a polyphagous leafhopper
which feeds on both forbs and grasses, exhibited higher
densities in clover habitat embedded within grass matrix
compared to bare-ground matrix. The more-specialized,
legume-feeding aphid, Therioaphis trifolii, showed the
opposite response to matrix composition; densities were
higher in clover within bare-ground matrix. The higher
densities of aphids in clover habitat embedded within bareground matrix may be the result of a reluctance to move
over bare ground. The planthopper Prokelisia crocea, a
monophagous herbivore of the grass Spartina pectinata,
displays a similar distributional pattern. The planthopper
reaches higher densities in host-plant patches bordered by
mudflats than in patches bordered by non-host grasses
because the rate of emigration from patches in mudflats is
much lower (Haynes and Cronin 2003, Cronin 2007,
Reeve et al. 2008). Despite the effects of matrix composition on herbivore densities in our system, matrix composition did not influence levels of herbivory. The lack of effects
of matrix composition on herbivory may be explained by
the fact that neither Agallia constricta nor Therioaphis trifolii
appeared to strongly affect clover biomass.
Like matrix composition, habitat fragmentation did not
affect levels of herbivory. The collective densities of
herbivore species were influenced by habitat fragmentation,
but no single species was strongly affected by this factor.
The lack of clear fragmentation effects may be partially
explained by the fact that the scale of fragmentation in this
study was likely small relative to the dispersal abilities of
three of the five herbivore species. The leafhoppers Agallia
constricta and Empoasca fabae and the plant bug Lygus
lineolaris are sufficiently mobile that the fragmentation of
clover habitat probably did little to improve access to
resources in the matrix (Fleischer et al. 1988, Hoffman and
Hogg 1992, B. Schroeder pers. comm.). For Halticus
bractatus, however, it is conceivable that fragmentation
increased the ability to forage both in clover and the matrix
since a large percentage of adult females are wingless (Day
1991). Similarly, most Theroaphis trifolii adults were
wingless in July and August (92% and 100% of captured
adults). Thus, rates of movement of this habitat-specialist
herbivore among clover subplots were likely substantially
reduced by the fragmentation of clover habitat.
Competition between clover and matrix vegetation
Our results also showed that clover biomass was influenced
by an interactive effect of clover habitat area and composition of the matrix. Clover biomass was highest in plots with
less clover area and bare-ground matrix. Given that we
did not see interactive effects of area and matrix on
herbivore densities, this effect was probably not a result of
herbivory. It is more likely that the observed differences in
clover biomass resulted because of competition between
clover plants and grass in the matrix, particularly along
clover-matrix edges. In plots with bare-ground matrix,
clover plants near the edges of subplots may have exhibited
increased growth due to reduced competition for water or
nutrients. Because clover plants in small (4 m2) clover
subplots were closer to clover-matrix edges, on average, than
in large clover subplots (16 m2), the lack of competitors at
the cloverbare-ground boundary would likely be more
beneficial to clover in small clover subplots. A review by
Haynes and Cronin (2004) found that matrix composition
often influences the quality (e.g. plant size, tissue nitrogen
content) of focal patches of vegetation by altering competition between plants in the patch and the matrix or by
altering nutrient subsidies across the patch edge.
Species-specific impacts of herbivores
The density of only one herbivore species, Empoasca fabae,
was significantly related to the difference in clover biomass
between exclosures and controls. The biomass differential
(exclosure biomass control biomass) increased with
increasing density of Empoasca fabae in August, explaining
approximately one fifth of the variation in the biomass
differential among plots (Fig. 3). This greater importance of
Empoasca fabae is likely due to the feeding habits of this
species. Unlike many other hemipterans which are sheath
feeders (stylet tips are sealed into a plant’s vascular cell using
a sheath composed of hardened saliva), Empoasca spp. feed
by rupturing plant cells with a unique form of stylet
movement, secreting saliva, and then sipping the contents
of damaged cells (reviewed by Backus et al. 2005).
Consequently, Empoasca fabae and its congeners are
especially likely to cause hopperburn, a type of damage
that results in tip-wilting, leaf yellowing, and plant stunting
(reduced growth). Stunting caused by Empoasca fabae is a
major cause of reduced yield in legume forage crops in
North America (Backus et al. 2005).
Empoasca fabae was likely the most damaging herbivore
in our clover agroecosystem, but spatial variation in levels of
herbivory can not be understood solely on the basis of the
spatial distribution of this species. Although our experiment
revealed that the effects of herbivores on clover biomass
were much stronger in plots with more clover area, densities
of Empoasca fabae were only slightly higher in these plots.
One possible explanation for the disproportionately high
reduction in clover biomass in plots with large clover
subplots is that increased clover habitat area had positive
effects on the densities of three of the five dominant
herbivores (Empoasca fabae, Lygus lineolaris and Halticus
bractatus) in both July and August. Densities of Halticus
bractatus, for example, were 1.9 and 3.2 times higher in
large than in small clover subplots in July and August,
respectively. Furthermore, although the multivariate response of all five herbivore species in August to habitat area
was not significant, the consistently positive effects of clover
habitat area on the densities of Empoasca fabae, Lygus
lineolaris and Halticus bractatus likely explains the importance of habitat area in influencing levels of herbivory.
Conclusions
Our findings support the view that the area of a focal
habitat (e.g. crop) is an important factor influencing
herbivore densities and herbivore damage (Root 1973)
as well as the concept that the practice of planting in large
monocultures may ensure continued high losses of crop
1483
productivity to herbivores (Russell 1989, Daily 1997,
Altieri 1999, Landis et al. 2000, Tscharntke et al. 2005).
Given the small size of our experimental plots, however,
how well our conclusions apply to agricultural landscapes is
an important question. Monotonically increasing or decreasing density-area relationships have frequently been reported
for herbivorous insects (MacGarvin 1982, Nowicki et al.
2007, but see Hambäck and Englund 2005), suggesting
that herbivore densityarea relationships and levels of
herbivory may remain more or less constant across a wide
range of spatial scales. In contrast, matrix composition may
often be more important in influencing herbivory within
small experimental fields than in larger agricultural fields.
Cross-edge foraging of matrix-dwelling or habitat-generalist
herbivores and natural enemies into agricultural fields
results in greater impacts on community structure near
the field margin than in the field interior (Clough et al.
2005, Rand et al. 2006). Therefore, herbivore impacts in
large fields, with their low edge-to-area ratios, may be less
dependent on composition of the surrounding matrix.
Finally, given that colonization rates typically decrease
with increasing distance between source and recipient
habitats (Hanski 1999), habitat fragmentation may be
more important to community structure and herbivory at
larger scales.
By documenting considerable asymmetry in the impacts
of different herbivore species on plant biomass, this study
suggests that the effects of landscape features on herbivory
may differ among systems supporting different suites of
herbivores. The relative importance of habitat area, fragmentation, and matrix composition to herbivory in a given
system could depend on how the distributions of a few key
herbivore species, rather than overall herbivore densities, are
influenced by these factors. This notion suggests that the
relative importance of different landscape attributes to
herbivory may be difficult to predict without a detailed
understanding of the ecological impacts of the species in a
given system (Rosenlew and Roslin 2008).
Acknowledgements Special thanks to Candace Crist for sewing the
herbivore exclosures and to Tim Diekötter for assisting with pilot
studies. Laura Douglas, Sam Evans, Rodney Kolb, Brad Schroeder
and Dave Stasek provided valuable help in the field. Daniel
Gruner provided useful comments on earlier drafts of this
manuscript. Funding for this project was provided by Miami
Univ. and a Miami Univ. Postdoctoral Research Scholarship.
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Appendix 1
Results from MANOVAs on the effects of habitat area, matrix composition, and habitat fragmentation on the collective densities of the five herbivore species. Densities were square-root transformed.
Significant results at the a0.025 level are shown in boldface.
Source
July
Wilk’s l
Area
Matrix
Fragmentation
AreaMatrix
AreaFragmentation
Matrix Fragmentation
AreaMatrixFragmentation
0.351
0.318
0.500
0.787
0.799
0.815
0.642
August
DF
5,
5,
5,
5,
5,
5,
5,
18
18
18
18
18
18
18
F
p
Wilk’s l
6.657
7.724
3.593
0.974
0.903
0.818
2.004
0.001
B0.001
0.020
0.460
0.501
0.553
0.127
0.539
0.696
0.649
0.693
0.874
0.744
0.801
DF
5,
5,
5,
5,
5,
5,
5,
18
18
18
18
18
18
18
F
p
3.084
1.571
1.946
1.598
0.519
1.238
0.896
0.035
0.218
0.136
0.211
0.759
0.332
0.505
Appendix 2
Results from univariate ANOVAs examining effects of habitat area (A), matrix composition (M), and habitat fragmentation (F) on the densities of each herbivore species in July. Densities were square-root
transformed. Significant results at the a 0.025 level are shown in boldface.
Source
A
M
F
A M
A F
MF
A MF
DF
1,
1,
1,
1,
1,
1,
1,
22
22
22
22
22
22
22
Agallia constricta
Empoasca fabae
Therioaphis trifolii
Lygus lineolaris
Halticus bractatus
F
p
F
p
F
p
F
p
F
p
0.424
24.393
3.457
0.057
2.232
2.145
0.015
0.522
B0.001
0.076
0.813
0.149
0.157
0.903
0.362
0.864
0.274
1.391
3.171
1.504
0.010
0.643
0.363
0.606
0.251
0.089
0.233
0.922
9.486
12.941
0.847
2.651
0.435
0.026
0.642
0.005
0.002
0.367
0.118
0.516
0.873
0.432
2.736
0.035
2.490
0.377
0.914
0.824
4.287
0.112
0.854
0.129
0.546
0.350
0.374
0.050
13.143
0.021
0.224
0.734
0.615
0.045
3.726
0.001
0.886
0.641
0.401
0.441
0.835
0.067