Effects of Local Habitat Characteristics and

Transcripción

Effects of Local Habitat Characteristics and Landscape
Context on Grassland Butterfly Diversity
SHARON K. COLLINGE,* KATHLEEN L. PRUDIC, AND JEFFREY C. OLIVER
Department of Environmental, Population, and Organismic Biology and Environmental Studies Program,
334 UCB, University of Colorado, Boulder, CO 80309–0334, U.S.A.
Abstract: Recent ecological studies suggest that the landscape context of native habitat remnants may significantly influence plant and animal abundance and distribution within those remnants. Other research has
revealed a weak link between landscape context and native community composition. To understand the relative importance of local and regional habitat characteristics for grassland butterflies, we assessed butterfly
community diversity in four types of grassland habitats surrounded by varying amounts of urban development near Boulder, Colorado (U.S.A.). We recorded butterfly species abundance and composition in 66 grassland study plots on five sampling dates in 1999 and 2000. Grasslands were of four types: native shortgrass,
native mixed grass, native tallgrass, and planted hayfields. Grasslands also varied in quality, determined by
the abundance of native versus exotic plant species. We observed highly significant effects of grassland type
on butterfly species richness and composition. For example, tallgrass plots supported significantly higher butterfly species richness than shortgrass plots (p 0.01). Habitat quality also affected butterfly species richness
and composition. Low-quality plots generally supported fewer species than moderate- or high-quality plots
( p 0.05). Landscape context—the percentage of urbanization in the surrounding landscape—did not significantly predict butterfly species richness or composition. Our observations suggest that for the grassland
butterfly communities in our study, (1) grassland type was the primary determinant of species richness and
composition, (2) habitat quality secondarily affected butterfly community diversity, and (3) landscape context did not significantly predict butterfly species composition. Our findings emphasize the importance of
maintaining high-quality grassland habitat to protect native butterfly diversity.
Efectos de las Características del Hábitat Local y el Contexto del Paisaje sobre la Diversidad de Mariposas de Pastizal
Resumen: Estudios ecológicos recientes sugieren que el contexto del paisaje de remanentes de hábitat nativo
puede afectar significativamente la abundancia de plantas y animales y su distribución en esos remanentes.
Otras investigaciones revelan un papel débil para el contexto de paisaje en la determinación de la composición de la comunidad nativa. Para entender la importancia relativa de las características del hábitat local y regional para mariposas de pastizal, evaluamos la diversidad de la comunidad de mariposas en cuatro
tipos de hábitats de pastizal, rodeados por diversas cantidades de desarrollo urbano cerca de Boulder, Colorado (E.U.A). Registramos la abundancia y composición de especies de mariposas en 66 parcelas de estudio
en cinco fechas de muestreo en 1999 y 2000. Los pastizales eran de cuatro tipos: pasto nativo corto, pasto nativo mixto, pasto alto nativo y campos cultivados de heno. Los pastizales también variaron en calidad, determinada por la abundancia de especies de plantas nativas versus exóticas. Observamos efectos altamente significativos del tipo de pasto sobre la riqueza y composición de mariposas. Por ejemplo, las parcelas de pasto
alto sostuvieron una riqueza de especies de mariposas significativamente mayor que las parcelas de pasto
corto ( p 0.01). La calidad del hábitat también afectó la riqueza y composición de especies. Parcelas de
baja calidad generalmente sostuvieron menos especies que las parcelas de calidad moderada o alta (p 0.05).
El contexto de paisaje y el porcentaje de urbanización en el paisaje circundante no predijeron la riqueza y
composición de especies de mariposas significativamente. Nuestras observaciones sugieren que para las co-
*email [email protected]
Paper submitted June 29, 2001; revised manuscript accepted March 6, 2002.
178
Conservation Biology, Pages 178–187
Volume 17, No. 1, February 2003
Collinge et al.
Grassland Butterfly Diversity
179
munidades de mariposas de pastizales en nuestro estudio (1) el tipo de pastizal fue el determinante primario
de la riqueza y composición de especies, (2) la calidad del hábitat afectó, de manera secundaria, a la diversidad de la comunidad de mariposas y (3) el contexto de paisaje no predijo significativamente la composición de especies de mariposas. Nuestros hallazgos enfatizan la importancia de mantener hábitat de pastizales de buena calidad para proteger la diversidad de mariposas nativas.
Introduction
In the process of land conversion for human use, native
ecosystems are transformed from old-growth forest to
clear cut, from coastal scrub to agricultural field, and
from native grassland to residential development. In addition to the loss and fragmentation of native habitats,
the resulting shift from continuous habitat to disjoined
remnants drastically changes the landscape context in
which these fragments are embedded (Forman 1995;
Collinge 1996; Mazerolle & Villard 1999).
Most studies of the ecological consequences of landscape change have focused on how the size and isolation of remnant habitats affect population persistence
and community structure (Collinge 2000; Steffan-Dewenter
& Tscharntke 2000; Thomas et al. 2001). Relatively few
researchers have examined how the landscape context
of habitat remnants affects these same population and
community dynamics. Several published studies reveal
striking ecological patterns among remnants that differ
in their surroundings (e.g., Åberg et al. 1995; Sisk et al.
1997; Ricketts et al. 2001). Other researchers have documented that local habitat characteristics determine ecological patterns and that landscape context plays a relatively weak role (Edenius & Sjoberg 1997; Lindenmayer
et al. 1999). As an example of a strong effect of landscape context, Sisk et al. (1997) found that bird species
richness and abundance in woodland patches significantly differed in patches surrounded by chaparral compared to those surrounded by grassland.
An increasingly common landscape configuration is
that of native habitat surrounded by urban and suburban
development (Theobald et al. 1997). With human population growth as high as 13% per year in some parts of
the western United States (Riebsame 1997), the juxtaposition of native habitat and urban development in this region continues to increase. Yet little is known about the
effects of urban land uses on ecological communities.
Two main approaches characterize ecological studies
of urbanization. Some urban ecological studies have focused on native habitats embedded within urban areas
and have quantified the diversity of plant or animal
groups in these fragments (Soulé et al. 1988; Panzer et
al. 1995; Bolger et al. 1997; McGeoch & Chown 1997;
Bolger et al. 2000). For example, Panzer et al. ( 1995)
surveyed invertebrates of prairie remnants in the region
of Chicago, Illinois, revealing that 40% of the butterfly
species observed depended on native habitat remnants
and were not observed in habitats modified by humans.
Other studies have focused on patterns of community
composition along urban gradients (e.g., Blair & Launer
1997; Clergeau et al. 1998; Blair 1999). This approach
samples flora and fauna in novel habitats, such as business districts and golf courses, and in more remote, native habitats. In a study of butterfly species composition
in relation to an urban gradient in northern California,
Blair (1999) found the highest butterfly richness and diversity at an intermediate level of urban development
and the highest abundance at the least-developed plot.
These results are consistent with expectations that urban land uses will have negative effects on native species abundance, and they suggest a more complex, nonlinear response of butterfly richness and diversity to
urbanization (Blair 1999).
Researchers in native grasslands near Boulder, Colorado (Bock et al. 1995; Berry et al. 1998; Bock et al. 1998;
Craig et al. 1999; Haire et al. 2000) adopted the former
approach, investigating patterns of native plant and animal diversity in grassland habitats surrounded by varying
levels of urbanization. We extended previous research
to investigate the relative importance of local habitat
quality and landscape context on butterfly species composition in grasslands surrounded by urbanization. Because of the relatively contiguous spatial configuration
of these grasslands (Fig. 1), characterizing them in terms
of their surrounding context was more appropriate than
quantifying patch size and isolation. Our research goals
were to (1) examine relationships among grassland habitat type and quality and butterfly species composition,
(2) assess how the landscape context of grassland plots,
particularly the percentage of the surrounding landscape that is urbanized, affects butterfly species abundance and distribution, and (3) compare the results of
these butterfly surveys to prior results for flowering
plants, small mammals, raptors, songbirds, and grasshoppers (Bennett 1997; Berry et al. 1998; Bock et al. 1998;
Craig et al. 1999; Haire et al. 2000).
We predicted a significant negative effect of landscape
context on butterfly species richness and abundance,
but we expected that the magnitude and extent of the
effect would depend on the habitat type and condition
of the grassland. A grassland site must contain both nectar and host-plant resources for successful larval and
adult butterfly survival and reproduction. If survey plots
Conservation Biology
180
Figure 1. Open-space grasslands surrounding Boulder,
Colorado. Shaded areas represent grasslands owned
or managed by city and county agencies; open areas
represent developed, incorporated, or other non-grassland properties.
near urban development lack abundant nectar resources
and appropriate larval host plants, then we would expect to find low densities of native butterflies in them. If
plots contain abundant nectar resources and mostly native plant species, then we would expect to find native
butterflies in them, but their abundance may be limited
by the amount of urbanization.
Methods
Study Area
We conducted our study near the city of Boulder, Colorado, which is located at the intersection of the western
Great Plains and the eastern edge of the Rocky Mountain
foothills (lat. 400054″N, long. 1051612″W). Boulder
lies within the Colorado Front Range, a region with one
of the highest levels of butterfly species richness in the
western United States (Opler 1995). Boulder’s human
population has increased nearly five-fold since 1950,
from 20,000 residents to a current population of 96,000.
The Boulder Open Space Department owns or manages
over 10,000 ha of grassland habitat, which forms a
nearly continuous green belt around the city ( Fig. 1).
Collinge et al.
These protected grasslands include tallgrass remnants
and hayfields in lowland floodplains, and mixed-grass
and shortgrass prairies on upland slopes and mesas bordered by Ponderosa pine (Pinus ponderosa) foothill
woodlands (Bock et al. 1995).
We used established plots from previous studies of
plant and animal diversity in these grasslands (Bock &
Bock 1994) so that butterfly data could be compared
readily with data gathered for other taxonomic groups.
Because butterfly species composition is closely related
to host-plant and nectar resources, we used vegetation
data previously collected from these plots (Bennett
1997) as a guide to interpreting patterns of butterfly species composition in relation to local habitat characteristics.
As described by Bock and Bock ( 1994), all 66 study
plots were located in one of four grassland types. Shortgrass prairie plots (n 13) were on upland areas that
had a recent or current history of grazing by horses, cattle, or black-tailed prairie dogs (Cynomys ludovicianus).
These plots were dominated by Agropyron smithii
(western wheatgrass), Bouteloua gracilis (blue grama),
Buchloe dactyloides ( buffalo grass), Artemisia frigida
( pasture sagebrush), and Plantago patagonica (woolly
plantain).
Mixed-grass prairie plots (n 21) were on slopes and
upland areas that at the time were lightly grazed or ungrazed. Depending on topography and soil type, they
were dominated by a variety of short to medium-height
grasses, sedges, and herbaceous plants, including Bouteloua gracilis (blue grama), Bouteloua curtipendula
(side-oats grama), Liatris punctata (blazing star), Carex
heliophylla (sedge), Artemisia ludoviciana (prairie
sage), and Aster falcatus (aster).
Tallgrass prairie plots (n 11 ) occurred in the lowland floodplains or on low benches. Some were wintergrazed, but all were ungrazed during the summer sampling period. Dominant vegetation was medium-height
and tall grasses characteristic of tallgrass prairies in the
eastern Great Plains, including Andropogon gerardii
(big bluestem), Panicum virgatum (switchgrass),
Sorghastrum nutans (indian-grass), Aster falcatus, and
Sporobolus asper (dropseed).
Hayfield plots (n 21) also occurred in the lowland
floodplains, but were irrigated during the summer season. Most were mowed at least once between sampling
periods, and many of these plots were grazed by cattle
during the winter months. Along the irrigation ditches
and field edges, there were remnants of the tallgrass vegetation that the planted hayfields replaced. Dominant
species included either alfalfa (Medicago sativa) or coolseason pasture grasses such as Bromus inermis (smooth
brome), Festuca pratensis (meadow fescue ), Dactylis
glomerata (orchard grass), and Phleum pratense
(timothy). Thirty of the 66 plots were adjacent to some
form of human activity, such as residential or commer-
Collinge et al.
cial development, and 36 plots were surrounded by native habitat (Bock & Bock 1994).
Field Surveys
We used a modified line-transect method (Pollard 1977)
to sample butterflies in the 66 circular, 200-m-diameter
study plots ( Bock & Bock 1994; Craig et al. 1999 ). We
sampled twice in 1999 ( July, August) and three times in
2000 ( June, July, and August ). We timed the five sampling dates to span peak flight periods for all breeding
butterfly species. We conducted all surveys on sunny
days between 1000 and 1600 hours. Each plot was divided into four quadrants of equal area. Beginning 20
paces from the center of the circle, a trained observer
walked back and forth through the quadrant for 10 minutes, identifying and recording all individual butterflies
observed. We used butterfly nets to capture the first
three to five individuals of all butterfly species observed
for deposition in a voucher collection. Subsequently,
species that could not be identified visually were captured, placed in glassine envelopes, and taken to the laboratory for identification. We deposited voucher specimens in the Entomology Collection at the University of
Colorado Museum. Field data were used to calculate butterfly species richness (number of species), evenness (relative abundance of species; Vandermeer 1981), and abundance (number of individuals) for each study plot. To
prevent temporal bias in our measures of richness, evenness, and abundance, we pooled data from the five sampling dates for statistical analyses.
Characterization of Habitat Quality and Landscape Context
Our study plots varied in grassland type and in the degree to which they had been previously grazed, disturbed, plowed, and planted with or invaded by exotic
species. Bennett (1997) conducted a detailed vegetation
study of these 66 sampling plots in 1995–1996. He recorded both frequency and percent cover of all plant
species observed along transects established at 100 m
due east and west from the center of each study plot.
These data were incorporated into a principal components analysis (PCA) to describe the vegetation communities in all 66 grassland study plots. Using the results of
the PCA, Bennett (1997 ) categorized each plot as of
low, moderate, or high quality, based on the relative
cover and richness of native versus exotic plant species
in the plots. Low-quality plots were dominated by exotic
forbs and C3 grasses, whereas high-quality plots were
rich in native forbs and C4 grasses. In Bennett’s (1997 )
designations, all hayfields were considered of low quality, primarily due to their dominance by exotic species.
Thus, we excluded hayfields from our investigation of
the effect of habitat quality on butterfly species composition. Bennett’s (1997 ) vegetation data were particu-
181
larly useful because native plant diversity and abundance
are typically positively correlated with butterfly species
diversity (Wettstein & Smith 1999; Thomas et al. 2001).
To examine butterfly diversity in relation to landscape
context, we used a geographic information system (GIS)
land-cover database for the Boulder Valley ( Berry et al.
1998; Haire et al. 2000). Database construction is described elsewhere ( Berry et al. 1998; Haire et al. 2000).
This database used a Landsat thematic mapper image
from August 1995, additional data from existing GIS coverage, and data gathered from field visits. Image classification was completed with ERDAS IMAGINE software,
version 8.2, on a Sun Sparc Workstation, and image
pixel size was 27.4 27.4 m. The centers of the 66 sampling plots we used were located with global positioning systems (GPS). For each sampling plot, the surrounding landscape was described in terms of percentages of
various types of land cover and was computed at five
spatial scales: 6, 40, 103, 244, and 423 ha. We used four
continuous variables as predictors of urbanization: (1)
distance from the center of the study plot to the nearest
urban cell, (2) percentage of urban vegetation in the surrounding landscape, (3) percentage of buildings and
pavement in the surrounding landscape, and (4 ) percentage of non-native hayfield in the surrounding landscape.
Statistical Analyses
We used analysis of variance (ANOVA ) to quantify the
effects of grassland type and habitat quality on butterfly
species richness, evenness, and abundance, averaged
over the five sampling dates. We used a priori linear contrasts to compare our dependent variables in specific
grassland types. To determine the effects of landscape
context on each of our dependent variables, we used a
mixed-model approach, consisting of grassland type (a
coded categorical variable) and the continuous predictors of urbanization. Abundance and species richness
were not normally distributed, so we log-transformed
these values before completing the analyses. We performed all analyses with the Statistical Analysis System,
version 6.12 (SAS Institute 1996 ) or JMP Version 3.2.2
(SAS Institute 1997).
To compare butterfly communities across the 66 sampling plots, we used detrended correspondence analysis
(DCA), a multivariate technique that orders plots based
on the number of individuals of each species. Our ordination used the total number of each butterfly species
recorded at each study plot. Plots closer to one another
in ordination space are more similar in species composition than plots that are further apart. A DCA is most appropriate when data sets consist of many species occurrences but few explanatory environmental variables (ter
Braak 1995). We used the software PC-ORD, version 4
( McCune & Mefford 1999) to perform the DCA.
182
Table 1.
Collinge et al.
Characteristics of grassland study plots and butterfly community measures in Boulder, Colorado.a
Grassland type
Shortgrass
Mixed-grass
Tallgrass
Hayfields
Number
of plots
Distance to
urban
development
(m)b
13
21
11
21
1,083.6 (162.2)
371.4 (86.8)
299.7 (46.3)
689.1 (235.2)
Richness c
3.12 (0.25)
4.99 (0.35)
5.67 (0.25)
4.95 (0.19)
Evenness d
0.72 (0.02)
0.83 (0.02)
0.78 (0.03)
0.72 (0.02)
Abundance e
7.65 (1.11)
18.02 (2.07)
25.95 (2.72)
40.63 (4.82)
a
Means and standard errors are presented for each study site over the five sampling dates.
Distance to urban development was measured from the center of the sampling plot to the nearest urban cell and was averaged for the sites in
each of the four grassland types.
c
Number of butterfly species per plot.
d
Shannon-Wiener diversity index divided by the natural logarithm of species richness (Vandermeer 1981) for each plot.
e
Mean number of individuals per plot.
b
Results
Butterfly Species Richness
We counted 7246 individuals of 58 species over the 2year sampling period (a full species list is available from
the first author). Grassland type—shortgrass, mixed
grass, tallgrass, and hayfield—significantly predicted
species richness and explained a large proportion of the
variance in species richness among plots (F3,62 15.23,
r 2 0.42, p 0.001) (Table 1; Fig. 2a). In particular,
tallgrass plots had significantly higher richness than
shortgrass plots, with mixed-grass plots in between ( linear contrast, F1,62 43.03, r 2 0.41, p 0.001). However, butterfly species richness in the three grassland
types depended significantly on habitat quality (interaction between grassland type and habitat quality: F4,46 2.99, r 2 0.57, p 0.05, Fig. 2a). We excluded hayfields from the analysis of habitat quality because all hayfields were categorized as low in quality (Bennett 1997).
When we controlled for grassland type in our model,
butterfly species richness was not significantly predicted
by distance to the center of the nearest urban cell (F1,61 0.19, r 2 0.003, p 0.66). Distance was correlated
with grassland type, however, and could be predicted
by grassland type (r 2 0.61, p 0.001). Specifically,
tallgrass plots tended to be relatively close to urban development (Table 1), mixed-grass plots and hayfields
were farther away, and shortgrass plots were farthest
from urban development. Further, the effect of grassland type on butterfly species richness was not dependent on distance to urban development (interaction between grassland and distance: F3,58 0.81, r 2 0.04,
p 0.05).
We detected no significant relationships between butterfly species richness and percentage of hayfield in the
surrounding landscape at any spatial scale (6, 40, 103,
244, and 423 ha) when we controlled for grassland type
(five separate single-degree-of-freedom tests, all p 0.05). Similarly, there were no significant relationships
between richness and percentage of urbanization at any
spatial scale (five separate two-degree-of-freedom tests,
all p 0.05) when we controlled for grassland type. Because percentage of urban vegetation and percentage of
buildings and pavement in surrounding areas were highly
correlated, the model to test the influence of percentage
of urbanization on butterfly species richness included
both of these parameters.
Butterfly Species Evenness
Grassland type significantly influenced species evenness
(F3,62 3.87, r 2 0.16, p 0.01) (Table 1). Butterflies
in mixed-grass plots were more evenly distributed among
species than the average of the tallgrass and shortgrass
plots (F1,62 7.13, r 2 0.10, p 0.01). When grassland
type was controlled for, distance to the center of the
nearest urban cell did not predict evenness (F1,61 0.10,
r 2 0.001, p 0.75). Furthermore, there was no significant grassland-by-distance interaction effect on evenness
(F3,58 1.17, r 2 0.06, p 0.05). Percentage of surrounding hayfield did not predict evenness at any spatial
scale (five separate one-degree-of-freedom tests, all p 0.05). When grassland type was controlled for, there
were no significant relationships between evenness and
percentage of urbanization at any spatial scale (five separate two-degree-of-freedom tests, all p 0.05).
Butterfly Species Abundance
Grassland type significantly predicted butterfly abundance (F3,62 24.60, r 2 0.54, p 0.001) ( Table 1;
Fig. 2b). We observed more butterflies in hayfields than
in other grassland types (F1,62 33.18, r 2 0.35, p 0.0001), and tallgrass plots had more butterflies than
shortgrass plots (F1,62 44.36, r 2 0.42, p 0.0001).
However, the mixed-grass plots did not differ significantly in abundance from the average of the tallgrass
and shortgrass plots. Butterfly abundance in the three
grassland types ( hayfields excluded) depended significantly on habitat quality (interaction between grassland
Collinge et al.
183
Figure 3. Butterfly abundance (number of individuals per plot, averaged over the five sampling dates)
and percent surrounding urban vegetation at the 103ha scale. There was no significant correlation between
butterfly species abundance and percentage of surrounding urban vegetation at any spatial scale (6, 40,
103, 244, and 423 ha).
Figure 2. Butterfly species richness and abundance in
relation to grassland type and habitat quality. Butterfly
(a) richness is the number of species per plot and (b)
abundance is the mean number of individuals per plot.
Means and standard errors are presented for study sites
over the five sampling dates. Quality categories are
based on those of Bennett (1997) and indicate the relative proportion of exotic plants (low quality, many exotics; high quality, few exotics).
type and habitat quality: F4,46 3.86, r2 0.57, p 0.01) ( Fig. 2b). As above, we excluded hayfields from
the analysis of habitat quality because all hayfields were
categorized as low in quality (Bennett 1997).
When grassland type was controlled for, distance to
the nearest urban cell did not affect abundance (F1,61 0.76, r2 0.01, p 0.23). When grassland type was
controlled for, neither percentage of surrounding hayfield nor percentage of surrounding building or pavement affected abundance at any spatial scale (6, 40, 103,
244, or 423 ha) (10 separate two-degree-of-freedom
tests, all p 0.05) (Fig. 3).
We defined common species as the seven most numerous species observed in our surveys, including Cercyonis pegala, Colias eurytheme, Colias philodice, Euptoieta claudia, Pieris rapae, Pontia protodice, and
Speyeria aphrodite ethne. Grassland type significantly
predicted the abundance of common butterfly species
(F3,62 24.13, r 2 0.54, p 0.0001) (Fig. 4). Hayfields
were higher in abundance of common species than the
other plots (F1,62 35.40, r2 0.36, p 0.0001), and
tallgrass plots had more common butterflies than shortgrass plots (F1,62 21.07, r 2 0.40, p 0.0001). However, the mixed-grass plots did not differ significantly in
abundance from the average of the tall- and shortgrass
plots. When grassland type was controlled for, distance
to the nearest urban cell did not affect the abundance of
common species (F1,61 0.01, r 2 0.0002, p 0.92).
When grassland type was controlled for, percentage of
surrounding hayfield did not affect abundance at any spatial scale (6, 40, 103, 244, or 423 ha). When grassland type
was controlled for, there was no relationship between
abundance and percent urbanization at any spatial scale
(five separate two-degree-of-freedom tests, all p 0.05).
Uncommon butterfly species included all species minus the seven most abundant species listed above (n 51 species). Grassland type significantly influenced the
abundance of uncommon butterfly species (F3,62 5.56,
r 2 0.21, p 0.0019) (Fig. 4). We observed fewer uncommon butterflies, on average, in hayfields than in
other grassland types (F1,62 4.75, r 2 0.07, p 0.03).
Tallgrass plots had higher values of abundance, on aver-
184
Collinge et al.
Figure 4. Abundance (means and standard errors) of
common and uncommon butterfly species in four
grassland types. Butterfly abundance is the mean
number of individuals per plot averaged over the five
sampling dates.
age, than shortgrass plots (F1,62 8.12, r 2 0.12, p 0.006). The mixed-grass plots were significantly higher
in abundance than the tall- and shortgrass plots as a
group (F1,62 4.00, r 2 0.12, p 0.049). In sum, the order from greatest to least abundance in the uncommon
species was tallgrass, mixed grass, shortgrass, and hayfields. When habitat type was controlled for, distance to
the nearest urban cell did not affect uncommon species
abundance (F1,61 3.24, r 2 0.05, p 0.08). When
grassland type was controlled for, percentage of surrounding hayfield did not affect abundance at any spatial
scale (6, 40, 103, 244, or 423 ha) (five separate onedegree-of-freedom tests, all p 0.05). When grassland
type was controlled for, there were no significant relationships between abundance of uncommon species and
percentage of urbanization at any spatial scale (five separate two-degree-of-freedom tests, all p 0.05).
Community Composition
Our 66 sampling plots clustered into four groups differentiated by grassland type (Fig. 5). Hayfield and tallgrass
plots were more similar to each other in species composition than were shortgrass and mixed-grass plots.
Mixed-grass and shortgrass plots were variable in butterfly species composition, with plots scattered throughout
the ordination space. In particular, two highly disturbed
mixed-grass plots and three shortgrass plots were quite
separate in ordination space from the majority of mixedgrass and shortgrass plots (Fig. 5).
Discussion
Grassland type strongly influenced butterfly species
richness, evenness, abundance, and composition in our
Figure 5. Detrended correspondence analysis (DCA)
of butterfly species composition at 66 grassland study
plots near Boulder, Colorado. Each symbol represents
the total number of individuals and species observed
per plot over the 2-year sampling period. Letters refer
to the mean ordination scores for shortgrass plots (S),
mixed-grass plots (M), tallgrass plots (T), and hayfields (H).
study area, but the influence of grassland type depended
on habitat quality. The extent to which grassland plots
were surrounded by urban development did not affect
butterfly species composition. We conclude that for
these butterfly species in the Boulder Valley, maintaining high-quality grassland habitat will be the most effective conservation strategy.
Tallgrass plots harbored the most butterfly species,
and several species were observed only in tallgrass prairies. Tallgrass prairie in the Boulder Valley is relictual of
the last glacial period, when climatic conditions were
cooler and wetter in the region (Livingston 1952).
Tallgrass remnants persist in mesic lowland areas (Bennett 1997). These plots are similar in plant-species composition to the historically more extensive eastern
tallgrass prairies (Bennett 1997), and the butterfly fauna
in these plots reflects that observed in eastern prairies
(Swengel 1996). For example, we observed 11 of 58 butterfly species only in tallgrass plots, including Hesperia
ottoe (prairie skipper), Hesperia leonardus pawnee
( blazing-star skipper), Euphyes bimacula ( two-spot
sedge skipper), and Speyeria idalia (regal fritillary).
These four species are found in tallgrass remnants in the
midwestern states ( Panzer et al. 1995; Swengel 1996),
Collinge et al.
and all four are of conservation concern (Association for
Biodiversity Information 2001). Despite the relatively
small size of the tallgrass remnants in the Boulder Valley
(approximately 27–280 ha), they clearly make a critical
contribution to the overall diversity of the butterfly communities in this region.
Our results suggest that the influence of grassland
type on butterfly species composition depends significantly on habitat quality. We observed the highest species
richness in tallgrass plots, but high-quality, mixed-grass
plots also supported high butterfly species richness.
Mixed-grass plots harbored a more even distribution of
species. Most diversity measures combine species richness and evenness, and in our study high-quality, mixedgrass plots would likely be considered the most diverse.
Low-quality plots of all three grassland types generally
supported fewer butterfly species, except for mixedgrass plots, where low- and moderate-quality plots were
similar. Bennett (1997) recorded more exotic plant species but also more species overall in two of the low-quality,
mixed-grass sites. Two of the moderate-quality sites
were comprised mostly of native plant species but had
fewer species overall ( Bennett 1997 ). Although these
four sites sustained similar numbers of butterfly species,
the plots dominated by exotic plant species were also
dominated by common butterfly species. The plots with
more native plant species supported more uncommon
butterfly species. Similarly, Nelson and Epstein (1998)
recorded primarily common butterfly species in overgrazed grasslands at Roxborough State Park, approximately 80 km southeast of Boulder, noting that species
indicative of undisturbed grassland were “noticeably absent”. Exotic plant species may provide nectar sources
but likely provide few host-plant resources for native
butterflies (Kocher & Williams 2000; Ries et al. 2001).
Butterfly abundance varied widely in relation to grassland type and quality. Tallgrass plots generally supported
more individuals than short- and mixed-grass plots, and
low-quality plots generally supported fewer individuals
than moderate- and high-quality plots. For mixed-grass
plots, however, low- and moderate-quality sites were
similar in butterfly abundance, perhaps for the same reason noted above for species richness. In tallgrass prairie,
we observed the fewest individuals in high-quality plots.
This may be a case in which high butterfly densities indicate low-quality rather than high-quality habitat (e.g.,
Van Horne 1983).
Contrary to our prediction, we found no effect of surrounding urbanization on butterfly species richness and
composition. Our 200-m diameter (3-ha) sampling plots
were embedded in grassland parcels ranging from approximately 5 to 390 ha. Parcel sizes, however, were
based on land-ownership boundaries, yet the protected
grasslands near Boulder form a relatively contiguous
band of habitat bordering the city ( Fig. 1). For butterflies these grassland habitats may actually be quite exten-
185
sive. If we had sampled in isolated grasslands of smaller
size surrounded by urbanization 5–30% (Fig. 3), we
may have observed significant effects of surrounding urbanization on butterfly communities. For example, McGeoch and Chown (1997) studied gall-forming Lepidoptera in habitat fragments in Pretoria, South Africa,
and noted lower species richness and larval densities in
reserves surrounded by urbanization than in more remote
plots. In their study, urban fragments ranged from 0.6 to
6.5 ha, which suggests that as patch size declines urbanization may have stronger effects than we observed.
The response of butterflies to the urbanization of the
Boulder Valley appears to be similar to that of grasshoppers (Craig et al. 1999) but different from that of raptors,
small mammals, and songbirds (Berry et al. 1998; Bock
et al. 1998; Haire et al. 2000). The abundance and species composition of small mammals shifted significantly
when only 5–10% of the surrounding landscape was urbanized (Bock et al. 1998), suggesting strong effects of
urban development on native grassland species. Grasshoppers showed no relationship between species composition or abundance and urbanization (Craig et al.
1999). Grasshopper abundance and distribution, however, were strongly affected by local habitat characteristics. The centers of all circular, 200-m-diameter grassland plots surveyed in these studies were at least 100 m
from the nearest urban edge. One explanation for the
lack of a significant effect of landscape context for grasshoppers and butterflies is that they may respond to urbanization on a much finer spatial scale than raptors,
small mammals, and songbirds. Alternatively, the 5–30%
surrounding urbanization that we observed may not be
sufficient to influence grasshopper and butterfly abundance and distribution.
These combined results suggest that the response of
grassland animals to urbanization in our region is scaledependent, with larger animals responding to landscape
structure at broader spatial scales or at lower levels of
urbanization. Because herbivorous insects such as grasshoppers and butterflies tend to be relatively host-plant
specific, their occurrence at a site may depend largely
on local habitat characteristics, such as the presence of
their food resources. For example, we observed the rare
Speyeria idalia only at two adjacent tallgrass plots, one
of which contained its native host plant, Viola nuttallii
(Violaceae) (Bennett 1997).
Our results corroborate those in a recent review of
other studies on landscape context. Mazerolle and Villard (1999) examined published research on species
abundance and richness in different landscapes, as influenced by patch ( local) characteristics and landscape
characteristics, such as the configuration or total cover
of surrounding habitat. They reported that for most
invertebrate studies, patch characteristics explain a
greater proportion of the variation in abundance and
richness than do landscape characteristics, which is con-
186
sistent with our findings. For vertebrate species, landscape characteristics explain a greater proportion of
variation in abundance and species richness (Mazerolle
& Villard 1999), consistent with previous studies of vertebrate taxa in Boulder’s grasslands ( Berry et al. 1998;
Bock et al. 1998; Haire et al. 2000).
Our research contributes to the growing body of
knowledge of the effects of local habitat characteristics
and landscape context, particularly urbanization, on native species composition. For native butterfly species in
the Boulder Valley, we conclude that grassland habitat
type and quality, but not surrounding urbanization, are
the key determinants of species diversity and composition. Although the direct effects of urbanization were not
apparent from our study, indirect effects—such as increased nutrient deposition, concomitant shifts in distributions of exotic plant species (Lejeune & Seastedt 2001),
and increased butterfly mortality from traffic (Ries et al.
2001)—may ultimately contribute to the long-term persistence of butterfly populations in urban landscapes.
Acknowledgments
We greatly appreciate our enthusiastic field assistants W.
Johnson, A. Pattison, H. Kippenhan, S. McKinney, and T.
Levy. We thank V. Scott and D. Bowers for lending their
expertise on local butterfly collections, A. Warren for assisting us with skipper identification, and L. Riedel and
C. Richardson for facilitating our research on City of
Boulder property. Earlier research by C. and J. Bock inspired us to conduct this study, and they provided expert guidance on study-area access and descriptions. We
thank F. Gerhardt and C. Bock for providing helpful
comments on an earlier draft of the paper. This research
was supported by the University of Colorado at Boulder.
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