Drosophila (Diptera: Drosophilidae) Response to Changes in Ecological Parameters Across an Urban Gradient

September 22, 2017 | Autor: Mercedes Ebbert | Categoría: Zoology
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COMMUNITY AND ECOSYSTEM ECOLOGY

Drosophila (Diptera: Drosophilidae) Response to Changes in Ecological Parameters Across an Urban Gradient JENNIFER L. AVONDET, ROBERT B. BLAIR, DAVID J. BERG,

AND

MERCEDES A. EBBERT

Department of Zoology, Miami University, Oxford OH 45056

Environ. Entomol. 32(2): 347Ð358 (2003)

ABSTRACT Understanding the changes in biodiversity correlated with urbanization is essential for monitoring the complex effects of human activity on native ecosystems. We hypothesized that the Drosophila community native to temperate woodland forests would change along a gradient of urbanization, and could therefore serve as a model system in studies on urbanization. We used an urbanization gradient we had previously characterized in Southwest Ohio. Community composition gradually changed along the gradient, although community diversity did not. Abundance varied signiÞcantly among sites, with one species, Drosophila melanogaster, increasing in abundance from the least to the most urbanized sites. We used 28 parameters from three sets of environmental dataÑland cover, vegetation, and temperature and humidityÑto build a model with Canonical Correspondence Analysis and characterize the species-environment relationship. The most predictive variables explaining the distribution of the Drosophila community were maximum temperature, maximum saturation deÞcit, percent lawn cover, average diameter at breast height (dbh) of shrubs and trees, and number of tree species. We conclude that the presence of individual, easily identiÞable Drosophila species may serve as robust indicators of the habitat degradation brought about by urbanization, and as ideal models for exploring animal response to urbanization. KEY WORDS species diversity, species abundance, urbanization, Drosophila affinis, Drosophila melanogaster, Drosophila tripunctata

URBAN ENVIRONMENTS are complex, with land uses ranging from construction sites to golf courses in an integrated mosaic. This complexity generates equally complex effects on biodiversity (McDonnell et al. 1993, Pouyat et al. 1994, Clergeau et al. 1998). The long history of ecological and evolutionary research into the response of Drosophila (Diptera: Drosophilidae) to environmental gradients suggests the genus has considerable promise as a model for understanding the impact of urbanization on native biodiversity (Parsons 1991, Powell 1997). The population and community dynamics of Drosophila have already been used to monitor a variety of environmental disturbances. For example, they have been used as indicators to assess pest management strategies (Hodge 2000), climate change (Argemõ´ et al. 1999, Rodriguez-Trelles and Rodriguez 1998) and tropical deforestation (Davis and Jones 1994). The Drosophila community in temperate mixed hardwood forests is typically an aggregation of several species (Shorrocks 1982). Within this community, species differ in their preferred oviposition sites. Breeding substrates fall broadly into four categories of decaying vegetation: fruit, mushrooms, slime ßuxes (decaying wood), and herbaceous stems and leaves (Begon 1982, Shorrocks 1982). Seven of the ten Drosophila species common in wooded sites in and around

Oxford, OH are native to the mixed deciduous forests of the eastern United States, the remaining three are cosmopolitan (Table 1; Patterson and Wagner 1943; Patterson and Stone 1952; Miller 1958; Parsons and Stanley 1981; Wheeler 1981, 1986; Ebbert et al. 2001, M.A.E., unpublished data). Previous reports on Drosophila abundance across a range of habitats have revealed a consistent pattern: as habitats become more urbanized, cosmopolitan species become more common and endemic species less common. For example, cosmopolitan Drosophila are less common, and woodland species more common, from city markets to gardens near Leeds, UK (Shorrocks 1977), from a small town dump to “heavy forest” in Tippecanoe County, IN (McCoy 1962), and from a research station to birch forest in Northwest Canada (Toda 1985). Because Drosophila abundance and community composition changes with temperature, humidity, and vegetation along natural gradients (as in, for example, those associated with changes in latitude, Powell 1997), we hypothesized that the Drosophila community would also recognize the changing environment along an urban gradient. Valente and her colleagues provided the Þrst test of whether changes in the distribution of Drosophila might reßect a response to the ecological parameters along an urbanization gradient. In Porto Alegre, Brazil,

0046-225X/03/0347Ð0358$04.00/0 䉷 2003 Entomological Society of America

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Table 1. Taxonomic status, geographical distribution, preferences for oviposition substrate and relative abundance of woodland Drosophila trapped in and around Oxford, OH Speciesa

Subgenus/species group

Distribution

Substrateb

Abundancec (n)

D. affinis D. athabasca D. melanogaster D. busckii D. robusta D. tripunctata D. immigrans D. quinaria D. falleni D. putrida

Sophophora/obscura Sophophora/obscura Sophophora/melanogaster Dorsophilia Drosophila/robusta Drosophila/tripunctata Drosophila/immigrans Drosophila/quinaria Drosophila/quinaria Drosophila/testacea

Eastern U.S. Eastern U.S. Cosmopolitan Cosmopolitan Eastern U.S. Eastern U.S. Cosmopolitan Eastern U.S. Eastern U.S. Eastern U.S.

Fruit/slime ßux Fruit/slime ßux Fruit Generalist Slime ßux Fungi Generalist Fungi Fungi Fungi

30.2% (733) 24.6% (598) 3.7% (90) None 19.3% (469) 8.5% (206) 2.4% (58) 4.1% (99) 5.6% (136) 1.7% (40)

a

Authorities and references in text. First/second preference. Generalist species oviposit in more than two categories of breeding substrates. Relative abundance (sample size) from collections at Þve woodland sites in Oxford, OH from 1996 to 1998 (Ebbert et al. 2001; Ebbert, unpublished data). D. busckii was not recorded from our previous collections. b c

they found that both relative abundance (between species) and chromosomal inversions (within species) varied across the urban gradient (Valente et al. 1989, Valente et al. 1993, Valiati and Valente 1997). These studies were based on collections in three urbanization “zones” deÞned by the percentage of land covered by vegetation and buildings. Here we test whether species diversity and abundance in the Drosophila community responds to a six-site gradient of urbanization deÞned using 28 environmental measures. This allowed us to use canonical correspondence analysis to test the following predictions: (1) that the Drosophila community and the abundance of individual Drosophila species would vary along the gradient, and (2) that this variation would be correlated with environmental variation in land cover, vegetation, temperature, and humidity measured along the same gradient. Materials and Methods Sites Along the Urban Gradient. We collected Drosophila along a gradient of urbanization ranging from a nature preserve to a business district (Fig. 1). Four of these sites are located within the municipal boundaries of Oxford, OH (14.7 km2; latitude 39.3025 N; longitude 84.4443 W; elevation 296 m; 2000 City Census of 21,943 individuals). The city consists of a university campus, business district, and apartment complexes surrounded by residential areas, agricultural Þelds, and natural areas used for recreation. The remaining two sites, a golf course and a natural area, are located seven km north of Oxford (latitude 39.3421 N; longitude 84.4429 W; elevation 284 m). The rank order of urbanization from natural area to business district was determined using the Delphi technique (Blair 1996, Gering and Blair 1999) and conÞrmed using a principal components analysis on land-cover variables (see below). The following is a brief description of the sites in order of least to greatest level of urbanization. Nature preserve (NP). We used two sites within the 1440-ha Hueston Woods State Park to represent the least disturbed habitat in our gradient: the old-growth nature preserve (67 ha) and a similar site outside the

preserve boundaries, but within the boundaries of the state park. The forest is comprised mainly of mixed deciduous and beech-maple forest with closed canopy, little or no shrub layer, and a sparse herbaceous understory (Gering and Blair 1999). Open space recreational area (OS). Peffer Memorial Park (80 ha) was purchased by Miami University as two separate parcels: one a pasture (in 1955) and the other a cultivated Þeld (in 1966). The vegetation is predominantly secondary growth of low stature with a dense herbaceous layer. The park includes a multiple-use trail system, and the surrounding landscape consists of a cemetery, woodlands, and agricultural Þelds. Golf course (GC). Hueston Woods golf course (established in 1980, 102 ha) is surrounded by state park woodlands and agricultural Þelds. The rough (where we placed our traps) consists of deciduous trees, grasses, and two small ponds. Residential district (RD). This ⬇10 city-block area consists of detached single-family houses built between 1960 and 1974. It is adjacent to a seasonal creek and a golf course. The landscape is primarily composed of lawns, gardens, and shade trees. Apartment complexes (AC). These multilevel apartment complexes were developed between 1960 and 1980. The area, ⬇20 ha, includes intervening parking lots, numerous refuse containers, isolated trees, and small-scale landscaping consisting of mostly lawn and hedges. Many other apartment complexes and single-family houses surround the apartments. Business district (BD). The district is 4 ⫻ 2 city blocks of primarily 2- and 3-story ofÞce buildings and parking lots. Construction of the district began in the middle 1800s. It is bordered on all sides by residential areas. Sampling of Drosophila. We used trapping methods that attract all the common ßies in our areas (Table 1), except those ßies specializing on mushrooms (Carson and Heed 1983, Oakeshott et al. 1989). We collected ßies using 250-ml glass bottles baited with banana, potato, or apple. Baits were washed and frozen before use, and seeded with commercial bakerÕs yeast. We Þtted the bottles with funnels and placed them in or

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Fig. 1. Aerial views of the (a) nature preserve, (b) open-space recreational area, (c) golf course, (d) residential area, (e) apartment complexes, and (d) business district in Oxford, OH, taken March 1994. All images are presented at the same scale.

around trees. We placed traps in the morning, on days during which no rain, moderate winds, and an overnight minimum temperature of at least 14⬚C were expected. For each collection, we set 72 traps in 23 locations. At each of the six sites, we placed groups of three bottles (one of each bait, about 3 m apart) in four different locations. Heavy construction in two blocks of the business district restricted us to four bottles at three locations. We chose locations that were as far apart as possible (up to 100 m) and in shade within 5 m of woody vegetation. We expected our traps would attract Drosophila from throughout the site (Powell 1997). We collected the traps in the afternoon, ⬇30 h after they were set, and identiÞed Drosophila to species and sex. We did not distinguish between Drosophila simulans Sturtevant 1919 and Drosophila melanogaster Meigen 1830. In Southwest Ohio, D. melanogaster is far

more common than its sibling species (Patterson and Wagner 1943, M.A.E. unpublished data). We collected six times from May to October 2000 and refer to these collections as follows: May (5, 6, 11 May), June (25Ð25 May, 1, 8 June), July (1, 6, 25 July), August (29 August), September (9, 13 September), and October (2, 4, 15 October). We tried to collect 100 ßies per site per collection. Except for the August collection, this required setting traps several times, and we pooled these repeat collections for our analysis. Environmental Parameters. We used three sets of environmental data to characterize our sites. Together, these provided 28 environmental parameters for the canonical correspondence analysis described below. Land cover. We used previous estimates (Gering and Blair 1999) of percent land cover within a 50-m radius of 16 sampling points within each site and principle component analysis (PCA) to derive a contin-

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uous measure of urbanization. This allowed us to conduct statistical tests that require a continuous, rather than a categorical, designation for each site. Four types of land cover (surface area) were considered: trees and shrubs (woody plants greater than three cm diameter breast height, DBH), pavement, buildings, and a combination of lawn and un-mowed grass. Vegetation. We used four vegetation parameters previously measured within a 11.3 m radius of each sampling point to assess land cover (R.B.B., unpublished data): composition (number of species), DBH (cm) of trees and shrubs, density (number of species per ha), and total basal area (m2 per ha). Before each collection, we noted the presence or absence of six potential oviposition sites (dumpsters, compost heaps, fruiting trees, mushrooms, vegetable gardens, slime ßuxes) at each sampling point. Temperature and humidity. At one location at each site, we monitored temperature and humidity using Hobo data loggers (Onset Computer Corporation, Pocasset, MA). We mounted the data loggers on wood and placed each upside-down in a tree 1 m above the ground. The data logger recorded hourly readings of temperature (oC), relative humidity (%), absolute humidity (g per m3), and dew point (oC) during the Þrst trapping period of a collection. We used the relative and absolute humidity readings to calculate the saturation deÞcit (g per m3), a measure of desiccation stress relevant to small insects, including Drosophila (David et al. 1983). We then summarized information for the temperature, saturation deÞcit, and dew point as the maximum, minimum, average, and difference between maximum and minimum values for each collection. Data Analysis. Our collection data consisted of counts (number of individuals) and the relative abundance of each species (percentage of the total number of individuals) for each collection and site. From these data, we calculated three estimates of diversity: the Shannon index (Shannon and Weaver 1949), SimpsonÕs index (Simpson 1949), and evenness (Magurran 1988). To test whether abundance within a species varied along the gradient, we compared our actual counts with those expected given a uniform distribution. We calculated expected counts as the number of Drosophila collected at a site multiplied by the relative abundance of a given species over all sites. We used categorical analysis to document heterogeneity in count data across sites and regression analysis to characterize patterns in that heterogeneity. We assigned attributes to each Drosophila collected: species, month (May to October) and site of collection (NP, OS, GC, RD, AC, BD). We then tested for associations between these attributes and count data using logistic regression and likelihood-ratio chisquare tests (Sokal and Rohlf 1981, Collett 1991). We used the PCA variable we derived from the land-cover data for linear regression analysis. We took both the log and the square root of the count data and used the transformation that provided the best approximation of a normal distribution (Shapiro-Wilks test for normality, P ⬎ 0.05). We then tested whether the trans-

Vol. 32, no. 2

formed count data (y) Þt a linear (y ⫽ PCA) or quadratic (y ⫽ PCA ⫹ PCA2) model. We used canonical correspondence analysis (CCA) to assess potential relationships between Drosophila species distribution and the 28 environmental variables detailed above. CCA is a weighted averaging ordination technique that simultaneously orders sites and species based on the unimodal response of taxa to observed environmental variables (Palmer 1993). We Þrst identiÞed and removed redundant environmental variables (pairs of variables with correlation coefÞcients ⬎0.80) from the analysis. We then identiÞed uninformative variables by running the CCA and identifying which of the remaining (nonredundant) variables was least signiÞcant in ordering the species counts, i.e., had an eigenvalue close to one (ter Braak 1986). This variable was removed and the analysis repeated. We then selected the “best” model as the one that contained the fewest environmental variables while explaining the highest percentage of variance in the species data. We used Monte Carlo permutations to determine the signiÞcance of the main matrix (species) and the second matrix (environmental variables) by repeatedly shufßing the samples. Finally, we compared species composition and position along the gradient between all pairwise combination of sites. We calculated an “urban distance” matrix using the PCA-derived land-cover variables by subtracting one value from the other; for example, we assigned the pair “nature preserve” and “business district” a value of 4.47 U based on their axis scores of ⫺1.99 and 2.48. We then prepared “community distance” matrices using the squared Euclidean distance between all combinations of sites derived from a cluster analysis based on the number of individuals trapped per species at each site (Sneath and Sokal 1973, McCune and Mefford 1999). We tested if dissimilarity in species composition (i.e., community distance) at two sites correlated with the urban distance between these sites using a Mantel test (Mantel 1967). In this method, shorter community distances between two sites indicate more similar communities, with identical communities assigned a separation of zero. Both of these matrices were log-transformed (ln (x ⫹ 1)) for the Mantel test. We used PC-ORD version 4.0 (McCune and Mefford 1999) to calculate diversity estimates, for the CCA and PCA, and to derive the community distances for the Mantel Test. We used Tools for Population Genetics Analyses (TFPGA) for the Mantel test (Miller 1997). We conducted the remaining statistical analyses with JMP for Macintosh (version 3.2.6, SAS Institute 1999). We considered test statistics signiÞcant if they were unlikely (P ⬍ 0.05) to be obtained by chance. Results The relative percentage of each type of land varies over gradient (Fig. 2). The amount of cover assigned to trees and shrubs decreased with urbanization, while pavement and building cover increased. Grassland

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Fig. 2. Percent area (⫾SE) covered by trees and shrubs, lawn and grassland, pavement, and buildings in Ohio.

and lawn have a unimodal distribution with a peak at the golf course. Principal components analysis provided a continuous measure that summarized these patterns. The PCA explained 70.13% of variance in the Þrst axis and an additional 29.53% along the second axis. The loadings along the Þrst axis were ⫺1.99 (NP), ⫺1.70 (OS), ⫺0.84 (GC), 0.30 (RD), 1.75 (AC), and 2.48 (BD). We interpreted these values as estimates of the amount of urbanization at each site and use them below in evaluating Drosophila response to the gradient. We collected 2294 adult Drosophila representing 10 species. Trapping records for the eight most common species (D. affinis Sturtevant 1916, D. busckii Coquillett 1901, D. falleni Wheeler 1960, D. immigrans Sturtevant 1921, D. melanogaster, D. putrida Sturtevant 1916, D. robusta Sturtevant 1916, and D. tripunctata Loew 1862) are presented in Table 2. Drosophila quinaria Loew 1865 (n ⫽ 10) and D. athabasca Sturtevant and Dobzhansky 1936 (n ⫽ 3) were quite rare. In previous years, D. robusta and D. athabasca were among the most common Drosophila in our traps at OS, NP, and three similarly situated sites (Table 1). During our Þrst three collections at Hueston Woods we collected few ßies, and switched to a new site nearby. This moderately increased our sample size for the August, September, and October collections (Table 2). We used the entire data set to calculate abundance of all Drosophila collected. For the remaining analyses, we used a subset (n ⫽ 2179) of the total count. This subset excluded D. quinaria, D. athabasca and 102 ßies, either D. immigrans or D. putrida, incorrectly identiÞed in the May (n ⫽ 16) and June (n ⫽ 86) collections.

Abundance within a species varied with the time of collection (Table 2). For example, of the 457 D. affinis we collected, 52% were trapped in June, whereas 41% of the 485 D. tripunctata were trapped in August. As a result, we could not analyze our data as a complete 8 (common species) ⫻ 6 (sites) ⫻ 6 (month) contingency table. A contrast between pooled counts from the earlier (May to July) and later (August to October) collections suggested both site and time (early versus late) of collection had a signiÞcant effect on species abundance. The full model (logistic model, count ⫽ site ⫹ time ⫹ site ⫻ time) provided a good Þt to the data (df ⫽ 77, G ⫽ 1988, P ⬍ 0.0001), and removing the interaction term resulted in a signiÞcant lack of Þt (df ⫽ 35, G ⫽ 206, P ⬍ 0.0001). We therefore considered the early and late collections separately in some of the analyses below. In the late season collections, the composition of the Drosophila community changed along the gradient, i.e., the community dissimilarity increased signiÞcantly with increasing urban distance (Fig. 3, Mantel test, r ⫽ 0. 58, P ⬍ 0.0340). Community composition did not change along the axis in the early season (r ⫽ 0. 10, P ⬍ 0.3360) or over the entire collection period (r ⫽ 0. 34, P ⬍ 0.1480). Other measures of the Drosophila community (species richness, evenness, Shannon diversity, and Simpson diversity) did not vary signiÞcantly across the urban gradient (Table 3, r2 ⬍ 0.5, and P ⬎ 0.05 for all linear and quadratic regressions). The number of Drosophila caught (pooled across species) did vary signiÞcantly when compared with a null hypothesis of even counts along the gradient (196.7 ßies per site in early months, 185.7 ßies per site in later months; Table 4; df ⫽ 4, P ⬍ 0.0001 for both

352 Table 2. Month May

June

July

Aug.

Sept.

Oct.

Grand total

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Common species of Drosophila trapped along an urban gradient in Oxford, OH Siteb NP OS GC RD AC BD Total NP OS GC RD AC BD Total NP OS GC RD AC BD Total NP OS GC RD AC BD Total NP OS GC RD AC BD Total NP OS GC RD AC BD Total

Speciesa DA

DB

DF

DI

DM

DP

DR

DT

1 1 6 32 0 6 46 22 58 98 28 9 23 238 9 17 32 13 4 15 90 0 10 12 4 1 1 28 4 16 5 4 2 0 31 13 2 2 4 3 0 24 457

0 0 0 2 0 0 2 0 0 67 3 0 4 74 0 1 9 8 17 3 38 0 0 0 0 5 4 9 0 0 9 5 7 2 23 0 0 5 9 9 6 29 175

0 0 0 0 0 0 0 7 5 1 4 1 0 18 0 0 0 0 0 0 0 8 1 0 6 0 0 15 5 7 0 2 0 1 15 7 11 1 2 0 0 21 69

0 0 1 1 0 0 2 0 0 0 39 0 1 40 5 4 0 74 29 11 123 0 3 2 0 0 4 9 0 1 0 2 1 2 6 1 0 1 1 0 0 3 183

0 0 0 0 0 4 4 0 0 2 1 2 15 20 1 1 12 27 30 81 152 0 1 38 16 49 35 139 0 0 10 13 37 17 77 1 3 26 29 27 9 95 487

0 0 0 0 0 0 0 0 17 0 3 1 1 22 5 16 8 29 3 13 74 40 14 4 11 0 4 73 2 18 7 0 1 10 38 9 9 2 5 0 1 26 233

0 0 0 0 0 0 0 0 10 0 4 0 0 14 0 5 14 2 0 4 25 3 0 8 0 0 1 12 0 0 0 0 0 1 1 7 1 5 0 0 0 13 65

0 1 2 0 0 0 3 2 11 4 8 1 1 27 8 29 4 7 8 4 60 39 53 10 37 32 28 199 16 9 8 26 3 18 80 37 54 1 28 13 8 141 485

Total 1 2 9 35 0 10 57 31 101 172 90 14 45 453 28 73 79 160 91 131 562 90 82 74 74 87 77 484 27 51 39 52 51 51 271 75 80 43 78 52 24 352 2179

a Species designated as follows: D. affinis, DA; D. busckii, DB; D. falleni, DF; D. immigrans, DI; D. melanogaster, DM; D. putrida, DP; D. robusta, DR; D. tripunctata, DT. b Sites designated as follows: nature preserve, NP; open space area, OP; golf course, GC; residential district, RD; apartment complex, AC; business district, BD.

tests, G (early) ⫽ 307, G (late) ⫽ 17.6). However, we detected no signiÞcant trend in this heterogeneity. The transformed counts did not Þt a linear (df ⫽ 1) or a quadratic (df ⫽ 2) model (P ⬎ 0.05 in all cases) using PCA values in place of site designations. Logistic analysis of species abundance showed signiÞcant variation with site in both the early and late collections (df ⫽ 35, P ⬍ 0.0001 for both tests, G (early) ⫽ 740, G (late) ⫽ 600). Collections for most species were conÞned to one or two sites. Fifty-one percent of the 175 D. busckii were trapped at GC and 117 (64%) of D. immigrans were collected from AC. In the remaining species, one half of the catch was spread over two contiguous sites. We trapped 63% of the 487 D. melanogaster at BD and AC, whereas most (66%) of the D. robusta and D. affinis (57%) were collected from GC and OS. Most of the D. falleni (74%), D.

putrida (56%), and D. tripunctata (51%) we collected were trapped from NP and OS. Four species accounted for 73% (1687 of 2294) of the total catch: D. tripunctata (22% of all Drosophila collected), D. melanogaster (21%), D. affinis (20%), and D. putrida (10%). Counts for these common species varied signiÞcantly among sites (when compared with a uniform distribution), but only D. melanogaster showed a monotonic trend across the gradient, increasing from less urbanized to more urbanized sites (Table 5). Note that in the D. melanogaster analysis, although both the linear and quadratic models were signiÞcant, within the quadratic model, the linear component (P ⫽ 0.008) but not the quadratic component (P ⫽ 0.1) was signiÞcant. We tested for correlation between species abundance and environmental variables by conducting

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Table 3. Diversity measures for Drosophila along an urban gradient in Oxford, OH Collectiona Early

Late

Siteb

Richness

Evenness

Shannon

Simpson

NP OS GC RD AC BD NP OS GC RD AC BD

7 9 9 8 7 7 8 8 9 8 6 8

0.76 0.70 0.64 0.75 0.84 0.69 0.68 0.64 0.74 0.73 0.59 0.68

1.49 1.53 1.41 1.55 1.64 1.35 1.42 1.33 1.63 1.52 1.06 1.41

0.70 0.73 0.67 0.72 0.78 0.64 0.69 0.64 0.73 0.71 0.57 0.70

a Early season: collections in May through July. Late season: collections in Aug. through Oct. b Sites designated as in Table 2.

separate CCA for the early and late collections. In both analyses, we considered the same 17 variables to be redundant, and used the remaining 11 variables in the CCA. Five variables were constant throughout the sampling period. These included percent lawn cover (zero for NP and OS, 48.9% for GC, 31.5% for RD, 28.1% for AC, and 9.7% for BD), compost piles (present only at RD), garbage dumpsters (present at AC and BD), fruiting trees (OS, GC, and BD) and fruiting mushrooms (BD and NP). The variables that differed between the early and late collections are listed in Table 6. Biplots of the species and site scores along the Þrst two axes of the ordination are presented in Fig. 4 (early season) and Fig. 5 (late season) with the relative importance of environmental variables indicated by the length and direction of vectors. For the early collection, the Þrst two axes explained 37.3% (eigenvalue ⫽ 0.297, P ⫽ 0.010, Monte Carlo permutation test) and 33.0% (eigenvalue ⫽ 0.263, P ⫽ 0.040) of the variance in species counts. In the late collections, the Þrst two axes explained 79.6% (eigenvalue ⫽ 0.351, P ⫽ 0.010) and 14.5% (eigenvalue ⫽ 0.064, P ⫽ 0.020) of the variance. In both analyses, the most predictive environmental variables in explaining distribution of Drosophila were the maximum temperature, maximum saturation deÞcit, percent lawn Table 4.

May June July Total (early) % total (early) Aug. Sept. Oct. Total (late) % total (late)

Discussion This is the Þrst study to describe the relationship between changes in environmental variables and the

Siteb NP

OS

GC

RD

AC

BD

6 32 29 67 5.7 90 27 78 195 17.5

3 101 76 180 15.3 82 51 81 214 19.2

19 180 79 278 23.6 75 39 43 157 14.1

37 165 160 362 30.7 74 52 80 206 18.5

0 16 91 107 9.1 87 51 52 190 17.1

10 45 131 186 15.8 77 51 24 152 13.6

Binomial errors on all percentages ⬍ 2%. Collections designated as in Table 3. Sites designated as in Table 2.

b

cover, average DBH, and number of tree species. The score on axis I (horizontal) separated the most urban sites (BD, AC, RD) from the less urban sites (GC, OS, NP). Drosophila affinis, the most common species in the early collections, was most abundant at cool and dry sites (Fig. 4). Among species common in the later collections, D. melanogaster was abundant at sites characterized by high saturation deÞcits and warm temperatures, while D. putrida and D. tripunctata were more common in moist and cool environments (Fig. 5).

Drosophila abundance along an urban gradient in Oxford, OH

Collectiona

a

Fig. 3. Community dissimilarity of Drosophila (as measured by community distance) increases with urban distance between points along the urban gradient in the late season but not in the early season. (Mantel test for late season: r ⫽ 0. 58, P ⬍ 0.0340; for early season r ⫽ 0. 10, P ⬍ 0.3360). Filled circles, late season. Open squares, early season. Urban distance is the difference between two sites along the Þrst axis of a PCA which used the measures of percentage land cover.

Total 75 539 566 1180 485 271 358 1114

354 Table 5.

a b c

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Correlations between site characteristics and Drosophila abundance along an urban gradient in Oxford, OH Species

Heterogeneitya

Linearb

Quadraticc

D. affinis D. melanogaster D. putrida D. tripunctata

P ⬍ 0.0001 (106) P ⬍ 0.0001 (404) P ⬍ 0.0001 (105) P ⬍ 0.0001 (147)

P ⫽ 0.2 (33.4%) P ⫽ 0.011 (83.6%) P ⫽ 0.1 (44.3%) P ⫽ 0.4 (13.7%)

P ⫽ 0.4 (45.7%) P ⫽ 0.019 (92.9%) P ⫽ 0.4 (49.6%) P ⫽ 0.7 (19.4%)

SigniÞcance (P) of likelihood-ratio chi-square (G, df ⫽ 4) comparing actual and expected counts across sites. SigniÞcance (P) of regression coefÞcient (r2, df ⫽ 1) for the model transformed (log or square root) counts ⫽ PCA. SigniÞcance (P) of regression coefÞcient (r2, df ⫽ 2) for the model log transformed (log or square root) counts ⫽ PCA ⫹ PCA2.

Drosophila community across a well-deÞned gradient of urbanization. We found that (1) Drosophila abundance varies with urbanization, (2) individual species differ in their preferred habitat along the gradient, in particular, D. melanogaster becomes more abundant with increasing urbanization, and (3) these patterns in the distribution were correlated with Þve environmental variables. Although broad community measuresÑsuch as diversity or overall abundanceÑ did not correlate well with urbanization, our results show that the distributions of individual species could serve as reliable indicators of the habitat degradation associated with urbanization. Individual species responded differently to the gradient, and these patterns were related to changes in land cover, vegetation, temperature, and humidity. The cosmopolitan species were rare in our earlier collections at wooded sites (Table 1), but a major component of the catch along the gradient (Table 2). This difference is likely because of the addition of urbanized sites to our current study: our earlier collections were conÞned to Hueston Woods, another site in the open recreational area at Peffer Park, and similar sites (Ebbert et al. 2001, M.A.E. unpublished data). Parsons and Stanley (1981) point out that although the eight cosmopolitan Drosophila have successfully colonized every continent, their relative abundance varies considerably. Our results provide an interesting illustration of this observation on a very Table 6.

Þne scale. The three cosmopolitan species we collected differed in their preferred sites: D. busckii was most common at the golf course, D. immigrans at the apartment complexes, and most of the D. melanogaster were trapped at the business district and apartments. We collected D. affinis and D. robusta at similar sites, with sites of intermediate urbanization (the golf course and open space recreational area) accounting for more than half the total catch of each species. Shorrocks (1977) suggests that European members of the obscura group (of which D. affinis and D. athabasca are North American representatives) use intermediate habitats (gardens and orchards) as well as woodlands. Use of slime ßuxes as oviposition sites may explain a preference for intermediate habitats: D. robusta is a specialist on this resource, and the obscura group ßies breed in both ßuxes and rotting fruits (Shorrocks 1982). Fluxes result from the colonization of sap ßows by yeasts, bacteria, and molds: if sap ßows are more common on damaged trees, then ßuxes may be more common in disturbed areas (e.g., wooded areas under recreational use, Pedersen 1999). Our data were not sufÞcient to test for this correlation: we noted only a single slime ßux within 50 m of our traps (Table 6). Future work on the potential relationships between slime ßuxes, intermediate habitat and Drosophila abundance will require monitoring sites with a wider range of slime ßux density in years when D. affinis, D. athabasca, or D. robusta are abundant.

Environmental variables at sites along an urban gradient in Oxford, OH

Collectiona

Siteb

MaxTc

MaxSDd

DBHe

Treesf

Gardensg

Fluxesh

Early

NP OS GC RD AC BD NP OS GC RD AC BD

17.32 23.04 20.04 26.04 26.73 21.23 22.35 23.26 22.49 29.02 27.53 27.24

8.15 6.58 11.29 12.47 14.06 14.22 2.91 5.11 11.08 13.50 14.17 12.99

28.08 6.87 25.97 14.91 13.22 28.52 13.84 6.87 25.97 14.91 13.22 28.52

18 27 13 24 14 10 17 27 13 24 14 10

None None None None None None None None None Present None None

Present None None None None None None None None None None None

Late

a

Collections designated as in Table 3. Sites designated as in Table 2. Max temp (⬚C), averaged across months within collections. d Max saturation deÞcit (g per m3), averaged across months within collections. e Avg diam woody shrubs and trees (⬎3 cm) at breast ht. f No. tree species at site. g Presence or absence of vegetable gardens. h Presence or absence of slime ßuxes on trees. b c

April 2003

AVONDET ET AL.: Drosophila RESPONSE TO URBANIZATION

355

Fig. 4. CCA analysis of early season Drosophila distribution along an urban gradient. Diamonds, study sites, designated as in Table 2. Circles, Drosophila species, designated as in Table 2. Vectors, environmental variables, designated as Table 6. Note that D. athabasca (Dat) is located outside the graph at 2.314, 0.059.

During the late season, communities closer to one another on the urban axis were more similar to one another in species composition. This indicates that the late-season Drosophila community changes gradually from natural to urban areas, as does the relative percentage of land cover assigned to trees and shrubs, grass and lawn, buildings, and pavement. We found no evidence of this pattern early in the season, and suggest that the early data swamps out the later data when seasons were pooled. The variation between seasons

in community composition is consistent with previous reports of temperate woodland Drosophila (Patterson 1943, Williams and Miller 1952, Miller 1958, McCoy 1962, Shorrocks 1975). The consistency we observed in measures of community diversity is an intriguing contrast to collections of other taxa along this same gradient, which show a peak in diversity at intermediate sites. Bird and butterßy species diversity peaked at intermediate levels of urbanization on this gradient of sites in both Ohio

Fig. 5. CCA analysis of late season Drosophila distribution along an urban gradient. Diamonds, study sites, designated as in Table 2. Circles, Drosophila species, designated as in Table 2. Vectors, environmental variables, designated as Table 6. Note that D. robusta (DR) is located outside the graph at ⫺0.092, 5.047.

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(Blair 2001a, 2001b) and along a similar gradient in Palo Alto, CA (Blair 1996, Blair and Launer 1997). Measures of spider diversity at the level of family and genus peaked at intermediate levels of urbanization along the Ohio gradient (Tierce 2000). Birds, butterßies, and spiders operate at different scales within the landscape, and the mechanisms generating greater diversity at intermediate levels of urbanization probably vary with taxonomic group. However, the response of all three taxa could be related to changes in habitat heterogeneity with urbanization: birds respond to patches of woody vegetation (Hostetler 1999), butterßies respond to patches of their larval host plant and adult nectaring source (Ricketts 2001), and spiders respond to physical structure (Wise 1993). This does not explain why Drosophila, as a community, do not show a similar response to urbanization. Our earlier studies included many more species and a broader range of habitat preferences than did our current work. In particular, we did not use baits that would attract the mycophagous ßies (Courtney et al. 1990). This bias may account for the lack of variation in the diversity measures, and future work on a more diverse assemblage could alter our conclusion that community diversity in Drosophila does not respond to this gradient. Application of our results to monitoring animal response to urbanization is necessarily tentative pending validation studies at other sites and across time along the Oxford gradient. In addition, our data highlight two potential limitations of any taxa, including Drosophila, as indicators of the habitat degradation associated with urbanization. First, population density can be low in natural areas. All four of the taxa we have sampled along our gradient, birds, and butterßies (Blair 2001a, 2001b), spiders (Tierce 2000), and Drosophila (Ebbert et al. 2001; M.A.E. unpublished data, this study), are less abundant in Hueston Woods compared with the rest of the gradient. In this study, we were able to switch sites within Hueston Woods and collect more ßies, but this may not be possible in other sampling protocols. Lower abundance at any site compromises the statistical power of the gradient analysis, and chance errors in a smaller data set from the site representing the least disturbed habitat could skew interpretation of changes along the gradient. Second, seasonal variation in animal communities can be considerable. For some taxa, such as Drosophila, variation in the community over the season is well documented and can be accounted for; in our study, we planned multiple collections over a six-month period to accurately characterize the community. However, the normal ßuctuations in temperature and humidity from year to year and between regions are likely to induce subtle changes in even a well documented pattern, and underscores the need for repeated sampling within and between seasons. With these limitations in mind, and based on the available data, we suggest that Drosophila has strong potential as indicators of the changes in habitat and ecological function that occur with urbanization. The

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genus Drosophila is diverse (at last count, 1595 species, Wheeler 1986), and the depth of the literature on every aspect of its biology is extraordinary. Easily identiÞable Drosophila species may therefore ideal organisms with which to characterize animal response to urbanization. As an example, we note that D. melanogaster increases monotonically in abundance with increasing urbanization (this study) and day-ßying lepidoptera decrease monotonically with increasing urbanization (Blair and Launer 1997; Blair 2001b) over this same gradient. Abundance of these two taxa could therefore be components of an indicator metric that is easy to assess and would require only minimal training in taxonomy (Karr and Chu 1998).

Acknowledgments We are indebted to T. Gregg for advice in all aspects of Drosophila ecology, collection, and identiÞcation. We are grateful to the state of Ohio for permission to collect at the Hueston Woods State Park and to residents and business owners of Oxford for permission to collect on their property. Salaries and support were provided by State of Ohio funds and an Ohio Board of Regents Research Challenge Grant to R. B. Blair, D. J. Berg, and M. A. Ebbert. We thank two anonymous reviewers and the editor for their thoughtful comments on this manuscript.

References Cited Argemı´, M., M. Monclus, F. Mestres, and L. Serra. 1999. Comparative analysis of a community of Drosophilids (Drosophilidae; Diptera) sampled in two periods widely separated in time. J. Zool. Syst. Evol. Res. 37: 203Ð210. Begon, M. 1982. Yeasts and Drosophila, pp. 345Ð381. In M. Ashburner, H. L. Carson, and J. N. Thompson, Jr. [eds.], The genetics and biology of Drosophila, vol. 3b. Academic Press, New York. Blair, R. B. 1996. Land use and avian species diversity along an urban gradient. Ecol. Appl. 6: 506 Ð519. Blair, R. B. 2001a. Creating a homogeneous avifauna: Local extinction and invasion along urban gradients in California and Ohio, pp. 459 Ð 486. In J. Marzluff, K. McGowan, R. Bowman [eds.], Avian ecology in an urbanizing world. Kluwer/Academic, Norwell, MA. Blair, R. B. 2001b. Birds and butterßies along urban gradients in two ecoregions of the United States: is urbanization creating a homogeneous fauna?, pp. 33Ð56. In J. L. Lockwood and M. L. McKinney [eds.], Biotic homogenization: the loss of diversity through invasion and extinction. Kluwer/Academic, Norwell, MA. Blair, R. B., and A. E. Launer. 1997. Butterßy diversity and human land use: species assemblages along an urban gradient. Biol. Conservation. 80: 113Ð125. Carson, H. L., and W. B. Heed. 1983. Methods of collecting Drosophila, pp. 1Ð28. In M. Ashburner and H. L. Carson [eds.], The genetics and biology of Drosophila, vol. 3e. Academic Press, New York. Clergeau, P., J. L. Savard, G. Mennechez, and G. Falardeau. 1998. Bird abundance and diversity along an urban-rural gradient: A comparative study between two cities on different continents. Condor. 100: 413Ð 425. Collett, D. 1991. Modeling binary data. Chapman & Hall, London, UK.

April 2003

AVONDET ET AL.: Drosophila RESPONSE TO URBANIZATION

Courtney, S. P., T. T. Kibota, and T. A. Singleton. 1990. Ecology of mushroom-feeding Drosophilidae. Adv. Ecol. Res. 20: 225Ð274. David, J. R., R. Allemand, J. Van Herrewege, and Y. Cohet. 1983. Ecophysiology: abiotic factors, pp. 105Ð170. In M. Ashburner, H. L. Carson, and J. N. Thompson, Jr. [eds.], The genetics and biology of Drosophila, vol. 3d. Academic Press, New York. Davis, A. J., and K. E. Jones. 1994. Drosophila as indicators of habitat type and habitat disturbance in tropical forest, central Borneo. Drosophila Information Service. 75: 150 Ð 151. Ebbert, M. A., J. J. Burkholder, and J. L. Marlowe. 2001. Pathogen prevalence and host habitat choice in woodland Drosophila. J. Invertebrate Pathol. 77: 27Ð32. Gering, J. C., and R. B. Blair. 1999. Predation on artiÞcial bird nests along an urban gradient: predatory risk or relaxation in urban environments? Ecography. 22: 532Ð 541. Hodge, S. 2000. A comparison of Drosophila assemblages in conventional, integrated, and organic apple production. Drosophila Information Service. 83: 1Ð 4. Hostetler, M. 1999. Scale, birds, and human decisions: a potential for integrative research in urban ecosystems. Landscape and Urban Planning 45: 15Ð19. Karr, J. R., and E. W. Chu. 1998. Restoring life in running waters: using multimetric indexes effectively. Island Press, Covelo, CA. Magurran, A. E. 1988. Ecological diversity and its measurements. Princeton University Press, NJ. Mantel, N. 1967. The detection of clustering and a generalized regression approach. Cancer Res. 27: 209 Ð220. McCoy, C. E. 1962. Population ecology of the common species of Drosophila in Indiana. J. Economic Entomol. 55: 978 Ð985. McCune, B., and M. J. Mefford. 1999. PCORD Multivariate Analysis of Ecological Data. Version 4.0. MjM Software Design, Gleneden Beach, OR. McDonnell, M. J., S.T.A. Pickett, and R. V. Pouyat. 1993. The application of the ecological gradient paradigm to the study of urban effects, pp. 175Ð189. In M. J. McDonnell and S.T.A. Pickett [eds.], Humans as components of ecosystems. Springer, New York Miller, D. D. 1958. Geographical distributions of the American Drosophila affinis subgroup species. Am. Midland Naturalist. 60: 52Ð70. Miller, M. P. 1997. Tools for population genetics analyses (TFPGA) 1.3: a Windows program for the analysis of allozyme and molecular population genetic data. Computer software distributed by author. Arizona State Univ., Dep. Biol., Tempe, AZ. Oakeshott, J. G., D. C. Vacek, and P. R. Anderson. 1989. Effects of microbial ßoras on the distributions of Þve domestic Drosophila species across fruit resources. Oecologia (Berl.). 78: 533Ð541. Palmer, M. W. 1993. Putting things in even better order: the advantages of canonical correspondence analysis. Ecology. 74: 2215Ð2230. Parsons, P. A. 1991. Biodiversity conservation under global climatic change: the insect Drosophila as a biological indicator? Global Ecol. Biogeography Lett. 1: 77Ð 83. Parsons, P. A., and S. M. Stanley. 1981. Domesticated and widespread species, pp. 349 Ð393. In M. Ashburner, H. L. Carson, and J. N. Thompson, Jr. [eds.], The genetics and biology of Drosophila, vol. 3a. Academic Press, New York.

357

Patterson, J. T. 1943. The Drosophilidae of the Southwest. University of Texas Publications. 4313: 7Ð216. Patterson, J. T., and W. S. Stone. 1952. Evolution in the genus Drosophila. Macmillan, New York. Patterson, J. T., and R. P. Wagner. 1943. Geographic distribution of species of the genus Drosophila in the United States and Mexico. University of Texas Publications. 4313: 217Ð281. Pedersen, B. S. 1999. The mortality of Midwestern overstory oaks as a bioindicator of environmental stress. Ecol. Appl. 9: 1017Ð1027. Pouyat, R. V., R. W. Parmalee, and M. M. Carreiro. 1994. Environmental effects of forest soil-invertebrate and fungal densities in oak stands along an urban-rural gradient. Pedobiologia. 38: 385Ð399. Powell, J. R. 1997. Progress and prospects in evolutionary biology: The Drosophila model. Oxford University Press, Oxford, UK. Ricketts, T. H. 2001. The matrix matters: effective isolation in fragmented landscapes. Am. Naturalist. 158: 87Ð99. Rodriguez-Trelles, F., and M. A. Rodriguez. 1998. Rapid micro-evolution and loss of chromosomal diversity in Drosophila in response to climate warming. Evol. Ecol. 12: 829 Ð 838. SAS Institute. 1999. JMP for Macintosh, version 3.2.6. SAS Institute, Cary, NC. Shannon, C. E., and W. Weaver. 1949. The mathematical theory of communication. University of Illinois Press, Urbana, IL. Shorrocks, B. 1975. The distribution and abundance of woodland species of British Drosophila (Diptera: Drosophilidae). J. Animal Ecol. 44: 851Ð 864. Shorrocks, B. 1977. An ecological classiÞcation of European Drosophila species. Oecologia (Berl.). 26: 335Ð345. Shorrocks, B. 1982. The breeding sites of temperate woodland Drosophila, pp. 385Ð 428. In M. Ashburner, H. C. Carson, and J. N. Thompson, Jr. [eds.], The genetics and biology of Drosophila, vol. 3b. Academic Press, New York. Simpson, E. H. 1949. Measurement of diversity. Nature (Lond.). 163: 688. Sokal, R. R., and F. J. Rohlf. 1981. Biometry, 2nd ed. W. H. Freeman and Company, New York. Sneath, P.H.A. and R. R. Sokal. 1973. Numerical taxonomy. W. H. Freeman and Company, San Francisco, CA. ter Braak, C.J.F. 1986. Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology. 67: 1167Ð1179. Tierce, V. 2000. The effects of urbanization on the diversity of ground-dwelling spiders (Araneae): implications for assessment and monitoring. M.S. Thesis. Miami University, Oxford, OH. Toda, M. J. 1985. Habitat structure of a drosophilid community at Inuvik, NWT, Canada (Diptera: Drosophilidae). Canadian Entomologist. 117: 135Ð137. Valente, V.L.S., A. Ruszczyk, R. A. Santos, C.B.C. Bonorino, B.E.P. Brum, L. Regner, and N. B. Morales. 1989. Genetic and ecological studies on urban and marginal populations of Drosophila in the south of Brazil. Evolucion Biologica. 3: 19 Ð35. Valente, V.L.S., A. Ruszczyk, and R. A. Dossantos. 1993. Chromosomal polymorphism in urban Drosophila willistoni. Rev. Bras. Genet. 16: 307Ð319. Valiati, V. H., and V.L.S. Valente. 1997. Chromosomal polymorphism in urban populations of Drosophila paulistorum. Braz. J. Genet. 20: 567Ð581.

358

ENVIRONMENTAL ENTOMOLOGY

Wheeler, M. R. 1981. The Drosophilidae: a taxonomic overview, pp. 1Ð97. In M. Ashburner, H. C. Carson, and J. N. Thompson, Jr. [eds.], The genetics and biology of Drosophila, vol. 3a. Academic Press, New York. Wheeler, M. R. 1986. Additions to the catalog of the worldÕs Drosophilidae, pp. 395Ð 409. In M. Ashburner, H. C. Carson and J. N. Thompson, Jr. [eds.], The genetics and biology of Drosophila, vol. 3e. Academic Press, New York.

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Williams, D., and D. D. Miller. 1952. A report on Drosophila collections in Nebraska. Bulletin University Nebraska State Museum 3: 1Ð19. Wise, D. H. 1993. Spiders in ecological webs. Cambridge University Press, Cambridge, UK. Received for publication 24 April 2002; accepted 3 September 2002.

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