- Email: [email protected]
Bird community responses along urban–rural gradients: Does the size of the urbanized area matter?
Landscape and Urban Planning 90 (2009) 33–41
Contents lists available at ScienceDirect
Landscape and Urban Planning journal homepage: www.elsevier.com/locate/landurbplan
Bird community responses along urban–rural gradients: Does the size of the urbanized area matter? Pablo I. Garaffa a,∗ , Julieta Filloy a,b , M. Isabel Bellocq a,b a Dep. Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires–Ciudad Universitaria, Pab 2, Piso 4, C1428EHA C.A. Buenos Aires, Argentina b Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
a r t i c l e
i n f o
Article history: Received 9 November 2007 Received in revised form 11 September 2008 Accepted 2 October 2008 Available online 20 November 2008 Keywords: Urbanization Spatial patterns Community similarity Abundance Richness Argentina
a b s t r a c t Human settlements have a strong influence on bird communities. To explore the size effect of the urbanized area in avian community structure, we examined changes in species richness, composition and abundance along urban–rural gradients of different extensions. We measured land-cover variables and surveyed birds along nine urban–rural gradients in the Pampean region of Argentina. In towns over 7000 inh, increasing constructed area was negatively related to species richness. In towns over 13 000 inh, the abundance of native species decreased towards the urban core whereas total abundance increased, decreased or remained constant depending on town characteristics. In villages (<2000 inh), small (2000–14000 inh) and large towns (>60000 inh), there was a constant representation of the rural community composition along gradients. In towns of intermediate sizes (>14 000–60 000 inh), species composition was more similar to that from the rural zone as this zone was approached. Similarity between both urban-core and peripheral points and the rural zone decreased with increasing gradient extension. It appears to be a size threshold for community sensitivity to urbanization below which the impact on community attributes is insignificant; increasing urbanization above the threshold level had pronounced effects on bird assemblages. Research approaches separating responses of native and exotic species to urbanization enhance our understanding to favor native birds and quality of urban bird communities. The size of the urbanized area is a key factor in policies designed to improve ecosystem health and human interactions with nature. © 2008 Elsevier B.V. All rights reserved.
1. Introduction The conversion of natural habitats into managed systems and urbanization is a growing process (Alig and Healy, 1987). Urban areas are expanding in both size and quantity worldwide. As a result of urban development, native habitats are reduced and fragmented resulting in a landscape mosaic where impervious areas grow and natural vegetation remnants are progressively altered (Germaine et al., 1998; Marzluff et al., 1998). Human settlements have a strong influence on wildlife communities including birds (Chace and Walsh, 2004, and references therein). Typically, urban systems affect species diversity and composition of natural communities. Previous studies indicate that bird abundance increases and richness declines while approaching the urban core (Marzluff, 2001). It has been suggested that species composition of the avifauna in urban cores tend to be similar all over
∗ Corresponding author. E-mail address: [email protected] (P.I. Garaffa). 0169-2046/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.landurbplan.2008.10.004
the world, leading to biotic homogenization (Jokimäki et al., 1996; Blair, 2001; Clergeau et al., 2006a,b; McKinney, 2006). Thus, urban cores seem to hold a few, very abundant species, composing the “urban avifauna”. Bird species may respond differently to urban development and habitat fragmentation (Crooks et al., 2004). Earlier studies indicated that urbanization results in increasing numbers of exotic species and decreasing richness of native species (Marzluff, 2001; Turner et al., 2004). Thus, response patterns of the total avifauna may be influenced by the relative contribution of introduced and native species (Clergeau et al., 1998), hiding the actual mechanisms driving community attributes in urban environments. For that reason, the native-exotic species discrimination approach may be enlightening when studying spatial variation of urban bird communities. Factors influencing biodiversity may change with the spatial scale. The extension of a gradient or a geographic area may have a strong influence on patterns of species richness (Wiens et al., 1987; Rahbek, 2005). Although, there are some controversies about the effects of scale on richness response patters (Mittelbach et al., 2003; Whittaker and Heegaard, 2003), in non-urban gradients,
34
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
richness responses (less than 1000 m) are often monotonic along short environmental gradients whereas they are often unimodal in extensive gradients (Rahbek, 2005). The multi-scale approach to research along urban–rural gradients offers a promising opportunity to explore the factors underlying urban ecosystem patterns (McDonnell and Pickett, 1990; Clergeau et al., 2006b). For example, Jokimäki and Kaisanlahti-Jokimäki (2003) found that the composition of wintering bird communities changed above certain town size in Finland. However, the role that the size of urban systems plays in the biological consequences of urbanization remains unclear and little explored (Clergeau et al., 1998, and references therein; Clergeau et al., 2006a). Our aim is to explore the influence of the size of urbanized area on changes in the structure of breeding bird communities that occur along urban–rural gradients within a region. If size of the urbanized area affects community changes along the gradient, we expect a stronger effect on communities towards the urban core as gradient extension increases. To test this prediction, we examined changes in species richness, total bird abundance and species composition along urban–rural gradients of different length within the Pampean region in Argentina. We first measured habitat variables along each urban–rural gradient and identified the predictor variables that better explained changes in community attributes considering both native and exotic species. Then we performed further analyses to examine the intensity of the effect of the size of the urbanized area on bird community changes along gradients. Finally, we discussed the implications for future planning decisions that concern biodiversity conservation.
2. Methods 2.1. Study region and urbanized areas The research was conducted in villages (less than 2000 inh) and towns (small: 2000–14 000 inh; intermediate: >14 000–60 000 inh; large: over 60 000 inh) within the Pampean region, an extensive plain located in central-eastern Argentina (Fig. 1). The climate is warm-temperate averaging 7.5–9.5 ◦ C in July and 21.5–23 ◦ C in January. Precipitation ranges 800–1100 mm/year. The region was originally dominated by grasslands of the Poaceae (Cabrera, 1971). Since the Spanish colonization in the 16th century, the natural habitat has been gradually modified by agriculture, farming and human settlements (Facelli et al., 1989). Human population size and urban–rural gradient extent are commonly used to estimate town size (Clergeau et al., 2001; Jokimäki and Kaisanlahti-Jokimäki, 2003). We selected nine urbanized areas of different size (Table 1), and used either number of inhabitants or gradient extent (measured from the point at the urban core to the point reaching the rural zone) to indicate the size. Those urbanized areas were located at similar latitudes within the Pampean region to ensure the same regional context regarding the influence of climate, landscape matrix, and land uses (Fig. 1). 2.2. Bird surveys For each of the selected urbanized areas, a transect was established from the urban core to the rural zone. Transect length varied
Fig. 1. Location of the study urban–rural gradients. Ascending alphabetic order indicates increasing urbanized area size. (A) Rivas; (B) Castilla; (C) Rawson; (D) Suipacha; (E) SA Giles; (F) Chacabuco; (G) Mercedes; (H) Lujan; (I) La Plata.
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
35
Table 1 Information of the selected urbanized areas. Urbanized area name
Population (inhabitants)
Gradient extent (km)
Surveyed points
Rivas (A) Castilla (B) Rawson (C) Suipacha (D) SA de Giles (E) Chacabuco (F) Mercedes (G) Lujan (H) La Plata (I)
472 827 2184 7149 13 941 34 958 51 967 67 266 521 759
0.90 1.20 1.40 1.60 2.25 3.00 3.20 4.00 10.00
6 8 9 8 15 15 16 17 14
Land cover (mean % ± S.D.) OPEN 24.7 19.3 34.2 31.5 24.3 19.7 16.5 16.9 6.1
± ± ± ± ± ± ± ± ±
TREE 14.5 14.9 9.4 25.9 19.5 19.3 15.9 13.0 6.4
27.1 22.9 27.1 5.1 12.5 21.3 20.9 16.1 22.3
CONS ± ± ± ± ± ± ± ± ±
14.7 9.9 11.2 4.6 9.9 9.7 10.0 7.3 9.3
10.2 7.7 18.9 28.9 26.6 20.7 41.0 43.6 32.9
± ± ± ± ± ± ± ± ±
RURL 9.6 9.0 15.8 25.4 29.3 25.0 26.1 25.2 28.2
37.9 50.2 19.7 34.4 36.5 38.3 21.5 23.3 38.8
± ± ± ± ± ± ± ± ±
40.0 28.0 26.3 43.0 39.7 36.9 32.9 37.3 44.3
OPEN: non-paved open areas; TREE: canopy cover; CONS: constructed area; RURL: rural area with either cattle or agricultural activity.
according to gradient extension. Birds were surveyed using a fixed 50-m radius point-count method (DeGraaf et al., 1991; Ralph et al., 1996; Melles et al., 2003). The spacing of point-count sites varied between 150 and 200 m (in villages and small towns), 250 m (in intermediate and large towns) and 600 m (in the largest town). The shortest distance between count points was 150-m as it is the minimum distance recommended to avoid double counting (Bibby et al., 1998). Bird surveys were conducted by the same observers on clear and calm weekdays, between 6:00 and 10:00. In each point count site, all birds seen and heard were recorded during five minutes. We ignored aquatic birds and those birds flying overhead. Each urban–rural gradient was surveyed once during November 2005 (spring) to maximize the number of urbanized areas that could be sampled on similar conditions (e.g. weather, bird activity – detection). Bird richness estimation using a single-visit is an accepted method in urban areas (Jokimäki and Suhonen, 1998; Jokimäki and Kaisanlahti-Jokimäki, 2003). 2.3. Land-cover quantification Latin-American cities often tend to be polycentric due to socioeconomic factors (Janoschka, 2002; Borsdorf, 2003). In such cases, the distance from the urban core to the rural area might be inadequate to quantify the urban–rural gradient. Although some urbanized areas are polycentric in Argentina, we selected those showing a marked monocentric structure. Thus, the distance from the urban core reflected a decline in the degree of urbanization towards the rural area. The quantification of land-cover types along urban–rural gradients can be useful to explore the association of particular urban variables to bird communities (Alberti et al., 2001). We measured urban-core-rural distance (DIST) and four local land-cover variables using IKONOS satellite images: constructed area (CONS), canopy cover (TREE), non-paved open areas (OPEN) and rural area with either cattle or agricultural activity (RURL). Roads were paved at the urban points and non-paved at the urban-peripheral and rural points. Because there was no transition from paved to non-paved roads, changes in road conditions were abrupt (rather than gradual) along the urban–rural gradients; consequently, we did not include roads as an explanatory land-cover variable. To quantify land cover along gradients, we established an area of 75-m radius centered at each bird survey point. 2.4. Data analysis To quantify the urban–rural gradient, we first performed Principal Component Analyses (PCA) using the land-cover data matrices. This technique allowed a synthetic quantification of the gradient from the rural zone to the urban core for each village or town. Thus, the first factors resulting from the PCA can be associated
to a land-cover gradient that represents the spatial expression of the urban–rural gradient. Following the Kaiser Criterion, only factors with associated eigenvalues greater than one were considered (Kaiser, 1960). By analyzing changes in bird community attributes along urban–rural gradients of different extensions, we assessed the effects of the size of the urbanized area. To study changes in species richness and abundance along the urban–rural gradients of different extents, we ran simple regressions analyses to test the isolated responses of species richness and abundance to the selected factor scores. The analyses were conducted including and excluding exotic species. Among the significant relationships, the analysis of factor loadings for each land-cover variable identifies those habitat variables determining changes in community attributes. Regression assumptions were tested for every analysis. To examine changes in species composition along gradients, we analyzed community similarity among urban–rural points as a function of the PCA factors that represented each urban–rural gradient. For the analyses we pooled all rural points from the urban–rural gradients, setting up a standardized “pooled rural point” to more accurately represent the regional species pool. This rural-point grouping was performed to avoid potential biases in rural species composition due to single-visit surveys. We used a qualitative similarity index to describe changes in species composition within the urban–rural gradients. We calculated the Sörensen index (Si) for each urban–rural gradient (Jongman et al., 1995) between the “pooled rural point” and the rest of the gradient points. We performed simple regressions including and excluding exotic species. Again, the factor loadings for each land-cover variable allowed inferring the primary land-cover variable associated with changes in community attributes along the urban–rural gradients. We further studied the size effect of the urbanized area on bird community composition from the rural zone to the urban core. For each urban–rural gradient, we established the urban-core point (Cp) as the surveyed point at the urban extreme and the most peripheral point (Pp) as the last suburban point just beside the first rural point. To represent the regional species pool we used the “pooled rural point” (Rp). Thus, for each urbanized area we calculated the similarity (Si ) between Cp–Rp and between Pp–Rp. We performed simple regressions between the obtained similarity values and urban–rural gradient length to find the best fitting model (the highest coefficient of determination) explaining the size effect of the urbanized area on species composition along urban–rural gradients. To avoid spurious results due to alpha inflation under multiple tests, we used the QVALUE software (available at http://faculty.washington.edu/∼jstorey/qvalue/) based on the positive false discovery rate (pFDR) (Storey, 2003). P-values were converted to q-values and hypotheses were rejected at q-values below 0.05 (Roback and Askins, 2005).
36
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
3. Results 3.1. Description of gradients The environmental changes caused by different land-cover types that occurred from the urban core to the rural zone were mostly explained by two land-cover variables. All first PCA factors were highly and positively associated with constructed areas and negatively with rural areas dominated by either cattle or agricultural activity (Table 2). Those first PCA factors were also highly and negatively correlated to the urban-core distance. These results indicated that all first PCA factors represented primarily a gradient of increasing rural coverage and decreasing construction density from the urban core to the rural zone. Open areas and canopy cover only seemed to be relevant in some villages and towns showing
well-vegetated urban cores (e.g. Rivas, SA Giles and Lujan). The percentage of variation along urban–rural gradients explained by first PCA factors decreased with the size of the urbanized area, likely revealing increasing spatial complexity of the urban–rural matrix in larger towns (Table 2). Arrangement of points along PCA factors indicates that villages and small or intermediate towns displayed a clear gradient in habitat composition whereas data progressively aggregated at the extremes of first PCA factors with increasing town size (see Figs. 2–4). 3.2. Responses of species richness and abundance to gradient extent A total of 2564 individual birds from 52 species were recorded (Appendix A). Passer domesticus (House Sparrow) and Columba livia
Table 2 Factor-variable correlations (factor loadings) of land-cover variables for the First Factor derived from Principal Component Analysis. Land-cover variables Open areas (OPEN) Tree canopy (TREE) Constructed area (CONS) Rural area (RURL) Distance to urban core (DIST) Percentage of variance explained
Rivas (A)
Castilla (B)
Rawson (C)
Suipacha (D)
SA Giles (E)
Chacabuco (F)
Mercedes (G)
Lujan (H)
La Plata (I)
0.973 0.876* 0.865* −0.993* −0.950*
0.935 0.530 0.839* −0.997* −0.973*
0.216 0.331 0.918* −0.921* −0.951*
0.274 0.189 0.879* −0.958* −0.956*
−0.158 0.750* 0.896* −0.884* −0.967*
0.220 −0.128 0.899* −0.887* −0.967*
−0.139 −0.799* 0.976* −0.825* −0.950*
0.325 0.737* 0.854* −0.972* −0.823*
0.286 0.343 0.950* −0.988* −0.922*
87.7
76.0
55.1
54.3
62.2
51.9
63.9
60.0
58.6
*
*
Analyzed land-cover matrices included the entire set of urban–rural gradient points, from urban core to last point of rural zone. * P < 0.05.
Fig. 2. Relationship between bird species richness and the First Factor obtained from Principal Components Analysis. Analyses were performed for native species (dashed lines, open circles) and for both native and exotic species (solid lines, filled circles). Coefficient of determination and significance (q, adjusted p-values by QVALUE method) are represented for native (bottom left) and exotic species (top right). Second Factors were not significantly correlated in any case. Ascending alphabetic order indicates increasing urbanized area size. (A) Rivas; (B) Castilla; (C) Rawson; (D) Suipacha; (E) SA Giles; (F) Chacabuco; (G) Mercedes; (H) Lujan; (I) La Plata.
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
37
Fig. 3. Number of individuals recorded per point count arranged across the First Factor resulted from Principal Components Analysis. Presentation is as in Fig. 2.
(Rock Dove) were the only exotic species registered during the surveys, representing 25% of the total number of individuals observed in all urbanized areas. Bird species richness was sensitive to the size of the urbanized area. Simple regression analyses showed that richness was significantly affected in towns larger than 7000 inhabitants, considering both native species and native plus exotic species (Fig. 2). In these towns, increasing proportion of constructed area was associated to a decline in species richness, whereas the rural environment appears to enhance the number of species (Fig. 2). Changes in bird abundance along the urban–rural gradients were also affected by gradient extension. In villages and most small towns the abundance of native species was constant along the gradients (Fig. 3A–D). In towns over 13 000 inhabitants, however, native species decreased their abundance from the rural zone to the urban core (Fig. 3E–G and I), with perhaps one exception (Fig. 3H). When exotic species were included, three different patterns were found. Total bird abundance increased (Fig. 3A and H), decreased (Fig. 3E and G), or remained constant (Fig. 3F and I) from the rural zone to the urban core. Villages and towns below 13 000 inh, showed similar abundance responses for both native and total birds along gradients (Fig. 3B–D). 3.3. Responses of community composition to gradient extent Changes in species composition from the rural zone to the urban core depended on gradient extent, and two different spatial patterns of response could be identified along gradients. First, there was a constant subset of the rural matrix community along the gradients in towns smaller than 14 000 inh (Fig. 4A–E). The same
pattern held for the largest town where the similarity between urban points and the rural zone remained constant and relatively low for both native and all species (Fig. 4I). Second, in towns between 34 000 and 68 000 inh, the composition of native species became more similar to that of the rural zone as the zone was approached (Fig. 4F–H); when considering all species, the pattern held for towns between 34 000 and 52 000 inh (Fig. 4F and G). In all urbanized areas, peripheral points showed higher similarity in species composition to the “pooled rural point” than the urban-core points (Fig. 5); in both cases similarity decreased with increasing size of the urban area. The peripheral similarity showed a constant decline with increasing size of the urbanized area (straight function). Urban-core similarity showed a sudden decline with little increments in the size of the urbanized area, until a plateau is reached and similarity remained constant (inverse function). Patterns were similar in both only-native and native plus exotic assemblages. 4. Discussion For birds, size does matter. Our work showed that spatial patterns of bird community composition, richness and abundance from the rural zone to the urban core changed with the size of the urbanized area. There seems to be a town-size threshold for bird community sensitivity to urbanization, as found by Jokimäki and Kaisanlahti-Jokimäki (2003) in Finnish cities. Our results suggested the existence of thresholds between 7000 and 35 000 inh depending on the community attribute considered. Above that threshold, there is a significant effect of urbanization on community structure; and below the threshold, the impact is insignificant.
38
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
Fig. 4. The similarity (Si) in the composition of native species (dashed lines, open circles) and both native and exotic species (solid lines, filled circles) between each point and the “pooled rural point” vs. urbanization gradient (summarized by the First Factor resulted of Principal Component Analysis). Presentation is as in Fig. 2.
4.1. Responses of species richness and abundance to gradient extent We found that bird richness decreased towards the urban core in towns over 7000 inh. Previous studies comparing bird communities along a complete urban gradient, as we did, found that bird richness reached a peak at moderate levels of urbanization (Jokimäki and Suhonen, 1993; Blair, 1996, 2001; Crooks et al., 2004). In relatively arid environments of developed countries, suburban areas are usually well vegetated having higher primary productivity than either the core area or the surrounding environment (Imhoff et al., 2000). In villages and towns of the Pampean region in Argentina,
our results showed decreasing species richness as impervious area (i.e. land covered by concrete) increased towards the core area, and the pattern held for all urbanized areas beyond the size threshold. In rural areas of the Pampean region, primary productivity is higher than either urban or suburban areas which could explain the observed pattern in species richness (Guerschman et al., 2003). Below the urbanized area size threshold, it is possible that habitat changes along the gradient occurred at such a small spatial scale that bird species typical of rural areas also use urban areas. The patterns of abundance along urban–rural gradients reported in the literature are variable. While most studies reported that total bird biomass increases towards the urban core (Marzluff,
Fig. 5. Regression analysis between the urban core and the “pooled rural point” similarity (Cp–Rp) (filled circles), the peripheral point and the “pooled rural point” similarity (Pp–Rp) (open circles) vs. the urban–rural gradient extent. The analysis was performed for native (A) and for both native and exotic species (B).
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
2001), others suggested that bird abundance decrease towards more urbanized areas (Leveau and Leveau, 2004). In our study, abundance of native species decreased towards the urban core in most intermediate and large size towns; however, different patterns emerged when including exotic species. Our findings suggest that the abundance patterns along the gradients depend on both habitat structure (e.g. well-vegetated urban core) and the contribution of exotic species. Exotic bird species often tend to be aggregated in the most urbanized centric points due to high efficiency in exploiting urban resources (see review by Chace and Walsh, 2004). We found three patterns of abundance along the gradient. First, the smallest village (i.e. Rivas) had only one fully urbanized point along the gradient where the exotic individuals aggregate, increasing the total bird abundance and producing the observed pattern. A similar pattern of constant abundance of native species and increasing total abundance towards the urban core was also found for a large town (i.e. Lujan). In that case, the increasing tree coverage towards the urban core could promote the increasing total bird abundance and the maintenance of constant abundance of native birds trough the gradient. Well-vegetated urbanized areas are likely providing refuge, nesting sites, and food source for both native and exotic species. Second, for some towns above the 13 000 inh threshold (i.e. S.A. Giles and Mercedes) bird abundance declined towards the urban core either including or excluding exotic species. However, the negative effect of urbanization on the avifauna appeared to be less severe when including exotic species, as total bird abundance showed an apparent slighter response. That slighter effect caused by adding exotic species is better observed in a third pattern (i.e. Chacabuco and La Plata) where their inclusion leads to the absence of response. Thus, an increase in exotic species in town centers compensated the negative response by native species such that total bird abundance remained constant along the gradient. As patterns of response often differ considering or excluding exotic species, using the total bird abundance patterns may be insufficient to understand the mechanisms underlying community changes along urban–rural gradients. 4.2. Responses of community composition to the size of the urbanized area Every point of every urbanized area holds a subset of the regional pool of species. Towns and villages in the Pampean region are embedded in a rural matrix. The analysis of similarity in species composition between points along gradients and the rural zone showed that similarity was either constant or decreased from the rural zone to the urban core. When levels of urbanization are low (villages and small towns), there is a constant subset representation of the rural pool of species along the gradient; thus, similarity remains relatively constant and high. Increasing levels of urbanization may enhance the difference between both extremes of a gradient by decreasing the similarity between urban points and the rural zone. However, the largest town showed a similar pattern to that of villages and small towns, with similarity remaining constant along the gradient but at a lower level. Apparently, as the size of the urbanized area increases, bird assemblages along the gradients become more influenced by the urban-core environment; in contrast, the rural influence becomes more relevant as the size decreases. Both the decreasing pattern of similarity along urban gradients (Clergeau et al., 2006a) and the town size effect (Jokimäki and Kaisanlahti-Jokimäki, 2003) have been previously reported. In fact, Jokimäki and Kaisanlahti-Jokimäki (2003) found that bird community similarity among urban sectors within a town decreased over a threshold of 35 000–105 000 inh in Finland. Our results also showed a threshold for towns between 34 000
39
and 52 000 inh, but revealed another threshold point where the decreasing trend ends and similarity remains constant and low along the gradient. Not surprisingly, peripheral points were more similar to the rural zone than the urban cores in all study towns and villages. Nevertheless, our results revealed that increasing size of the urbanized area had a negative effect on similarity between urban points (i.e. peripheral and core points) and the rural zone, showing a stronger negative effect on urban-core bird assemblages than on peripheral assemblages. For villages and small towns, slight changes in size may lead to a more sudden reduction in similarity values in the urban cores than in the periphery. Bird assemblages from the urban cores seemed more sensitive to increasing urbanization than the peripheral assemblages. Clergeau et al. (2006a) found no town size effects in bird community and argued that detailed knowledge of habitat structure is required. Our analysis showed that, regardless of the knowledge of local habitat characteristics, the use of several urbanized areas determining an urban-size gradient (from a small village to a large town) allowed to detect the size effect of the urbanized area. 4.3. Final remarks Increasing urbanization had pronounced effects on bird communities. Most studies on animal or plant responses to urbanization were based on the comparison between few sites with different levels of development (Crooks et al., 2004). Our study, incorporating complete and well described urban–rural gradients into a gradient of sizes of urbanized areas, allowed to reveal urbanization thresholds at which bird community attributes started to respond; and a saturation point where urbanization reached the maximum effect. The clarification of patterns and the examination of potential environmental forces driving diversity along urban gradients is a further step to the understanding of mechanisms causing the observed patterns (Shochat et al., 2006). Town core areas seem to be holding the same few and very abundant “urban exploiters” worldwide, by providing resources that enhance exotic species colonization and restrict native species settlement. In other regions of the New World, most communities in highly urbanized areas are dominated by three exotic birds, introduced from Europe and adapted to high levels of land covered by concrete and low tree density: House Sparrows, Rock Doves and European Starlings (Sturnus vulgaris) (Melles et al., 2003; Crooks et al., 2004). House Sparrows and Rock Doves were also very common in urban cores of the Pampean region, and were often found aggregated in squares and recreation areas. Although we recorded no European Starlings in our surveys, this recently introduced species is increasingly expanding into the Pampean region (Peris et al., 2005). The patterns we detected here might be best reflected by alternative biological models including taxa with higher number of exotic species in urban areas. Urbanization was defined as the primary force promoting biotic homogenization worldwide, where a few widespread and locally abundant “urban-adaptable” species would occur in urban environments around the world (McKinney, 2006; Sorace and Gustin, 2008). In that scenario, most of the urban world human population is meant to live in global biological poverty (Turner et al., 2004). Research approaches separating responses of native and exotic species to urbanization will enhance our understanding to favor native birds and quality of urban bird communities. The size of the urbanized area has a strong effect on urban bird communities and it is a key factor to be considered in urbanization policies to improve ecosystem health and human interactions with nature. It would be interesting to evaluate whether the described patterns hold in other biogeographic regions.
40
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
Acknowledgements We appreciate comments made by G.A. Zurita, J. Jokimäki and two anonymous reviewers to the manuscript. The work was financially supported by the Universidad de Buenos Aires and the Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina). Appendix A. List of bird species found in the gradients Family
Scientific name
Common name
Tinamidae Ardeidae
Nothura maculosa Syrigma sibilatrix Casmerodius albus Elanus leucurus Ictinia plumbea Rostrhamus sociabilis Buteo magnirostris Polyborus plancus Milvago chimango Vanellus chilensis Larus maculipennis Columba picazuro Columba maculosa Columba livia Zenaida auriculata Columbina picui Myiopsitta monachus Guira guira Athene cunicularia Chlorostilbon aureoventris Colaptes campestris Colaptes melanolaimus Furnarius rufus Anumbius annumbi Schoeniophylax phryganophila Synallaxis frontalis Machetornis rixosus Pitangus sulphuratus Tyrannus melancholicus Tyrannus savana Serpophaga nigricans Serpophaga subcristata Progne chalybea Phaeoprogne tapera Tachycineta leucorrhoa Troglodytes aedon Mimus satrurninus Turdus rufiventris Geothlypis aequinoctialis Sporophila caerulescens Sicalis luteola Sicales flaveola Zonotrichia capensis Ammodramus humeralis Poospiza nigrorufa Poospiza melanoleuca Carduelis magellanica Molothrus rufoaxillaris Molothrus bonariensis Molothrus badius Leistes superciliaris Passer domesticus
Spoted Nothura Whistiling Heron Great Egret White-tailed Kite Plumbeous Kite Snail Kite Roadside Hawk Southern Crested Caracara Chimango Caracara Southern Lapwing Brown-hooded Gull Picazuro Pigeon Spot-winged Pigeon Rock Dove Eared Dove Picui Ground-Dove Monk Parakeet Guira Cockoo Burrowing Owl Glittering-bellied Emerald Field Flicker Golden-Breasted Woodpecker Rufous Hornero Firewood-Gatherer Chotoy Spinetail Sooty-fronted Spinetail Cattle Tyrant Great Kiskadee Tropical Kingbird Fork-tailed Flycatcher Sooty Tyrannulet White-crested Tyrannulet Gray-breasted Martin Brown-chested Martin White-rumped Swallow House Wren Chalk-browed Mockingbird Rufous-bellied Thrush Masked Yellowthroat Double-collared Seedeater Grassland Yellow-Finch Saffron Yellow-Finch Rufous-collared Sparrow Grassland Sparrow Black-and-Rufous Warbling-Finch Black-capped Warbling-Finch Hooded Siskin Screaming Cowbird Shiny Cowbird Bay-winged Cowbird White-browed Blackbird House Sparrow
Accipitridae
Falconidae Charadriidae Laridae Columbidae
Psittacidae Cuculidae Strigidae Trochilidae Picidae Furnariidae
Tyrannidae
Hirundinidae
Troglodytidae Mimidae Turdidae Parulidae Emberizidae
Fringilidae Icteridae
Ploceidae
References Alberti, M., Coe, A., Botsford, E., 2001. Quantifying the urban gradient: linking urban planning and ecology. In: Marzluff, J.M., Bowman, R., Donnelly, R. (Eds.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell, MA, USA, pp. 89–105. Alig, R.J., Healy, R.G., 1987. Urban and built-up land area changes in the United States: an empirical investigation of determinants. Land Econ. 63, 215–226. Bibby, C., Jones, M., Mardsen, S., 1998. Expedition Field Techniques. In: Bird Surveys. Expedition Advisory Centre, London. Blair, R.B., 1996. Land use and avian species diversity along an urban gradient. Ecol. Appl. 6 (2), 506–519.
Blair, R.B., 2001. Creating a homogeneous avifauna. In: Marzluff, J.M., Bowman, R., Donnelly, R. (Eds.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell, Massachusetts, USA, pp. 459–486. Borsdorf, A., 2003. Hacia la ciudad fragmentada. Tempranas estructuras segregadas en la ciudad latinoamericana. Scripta Nova 7 (146) (available at: http://www. ub.es/geocrit/sn/sn-146(122).htm). Cabrera, A., 1971. Fitogeografía de la Argentina. Boletín de la Sociedad Argentina de Botánica 14 (1–2), 1–43. Chace, J.F., Walsh, J.J., 2004. Urban effects on native avifauna: a review. Landscape Urban Plan. 74, 46–69. Clergeau, P., Croci, S., Jokimäki, J., Kaisanlahti-Jokimäki, M.L., Dinetti, M., 2006a. Avifauna homogenisation by urbanisation: analysis at different European latitudes. Biol. Conserv. 127, 336–344. Clergeau, P., Jokimäki, J., Savard, J.P.L., 2001. Are urban bird communities influenced by the bird diversity of adjacent landscapes? J. Appl. Ecol. 38, 1122–1135. Clergeau, P., Jokimäki, J., Snep, R., 2006b. Using hierarchical levels for urban ecology. Trends Ecol. Evol. 21 (12), 660–661. Clergeau, P., Savard, J.P.L., Mennechez, G., Falardeau, G., 1998. Bird abundance and diversity along an urban–rural gradient: a comparative study between two cities on different continents. Condor 100, 413–425. Crooks, K.R., Suarez, A.V., Bolger, D.T., 2004. Avian assemblages along a gradient of urbanization in a highly fragmented landscape. Biol. Conserv. 115, 451– 462. DeGraaf, R.M., Geis, A.D., Healy, P.A., 1991. Bird population and habitat surveys in urban areas. Landscape Urban Plan. 21, 184–188. Facelli, J.M., Leon, R.J.C., Deregibus, V.A., 1989. Community Structure in grazed and ungrazed grassland sites in the flooding Pampa, Argentina. Am. Midl. Nat. 121, 125–133. Germaine, S.S., Rosenstock, S.S., Schweinsburg, R.E., Richarsdson, W.S., 1998. Relationships among breeding birds, habitat, and residential development in Greater Tucson, Arizona. Ecol. Appl. 8, 680–691. Guerschman, J.P., Paruelo, J.M., Di Bella, C., 2003. Land cover classification in the Argentine Pampas using multi-temporal Landsat TM data. Int. J. Remote Sens. 24, 3381–3402. Imhoff, M.L., Tucker, C.J., Lawrence, W.T., Stutzer, D.C., 2000. The use of multisource satellite and geospatial data to study the effect of urbanization on primary productivity in the United States. IEEE Trans. Geosci. Remote Sens. 38, 2549– 2556. Janoschka, M., 2002. El nuevo modelo de la ciudad latinoamericana: fragmentación y privatización. Eure 28, 11–20. Available at: http://www.scielo.cl/scielo.php? script=sci arttext&pid=S0250-71612002008500002&lng=en&nrm=iso. Jokimäki, J., Kaisanlahti-Jokimäki, M.L., 2003. Spatial similarity of urban bird communities: a multiscale approach. J. Biogeogr. 30, 1183–1193. Jokimäki, J., Suhonen, J., 1993. Effects of urbanization on the breeding bird species richness in Finland: a biogeographical comparison. Ornis Fennica 70, 71–77. Jokimäki, J., Suhonen, J., 1998. Distribution and habitat selection of wintering birds in urban environments. Landscape Urban Plan. 39, 253–263. Jokimäki, J., Suhonen, J., Inki, K., Jokinen, S., 1996. Biogeographical comparison of winter bird assemblages in urban environments in Finland. J. Biogeogr. 23, 379–386. Jongman, R.H.G., ter Braak, C.J.F., Van Tongeren, O.F.R., 1995. Data Analysis in Community and Landscape Ecology. Cambridge University Press. Kaiser, H.F., 1960. The application of electronic computers to factor analysis. Educ. Psychol. Meas. 20, 141–151. Leveau, L.M., Leveau, C.M., 2004. Comunidades de aves en un gradiente urbano de la ciudad de Mar del Plata, Argentina. Hornero 19, 13–21. Marzluff, J.M., 2001. Worldwide urbanization and its effects on birds. In: Marzluff, J.M., Bowman, R., Donnelly, R. (Eds.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell, MA, USA, pp. 19–47. Marzluff, J.M., Gehlbach, F.R., Manuwal, D.A., 1998. Urban environments: influences on avifauna and challenges for the avian conservationist. In: Marzluff, J.M., Bowman, R., Donnelly, R. (Eds.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell, MA, USA, pp. 283–296. McDonnell, M.J., Pickett, T.A., 1990. Ecosystem structure and function along urban–rural gradients: Aan unexploited opportunity for ecology. Ecology 71, 1232–1237. McKinney, M.L., 2006. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260. Melles, S., Glenn, S., Martin, K., 2003. Urban bird diversity and landscape complexity: species-environment associations along a multiscale habitat gradient. Conserv. Ecol. 7, 5 (available at: http://www.consecol.org/vol7/iss1/art5/main.html). Mittelbach, G.G., Scheiner, S.M., Steiner, C.F., 2003. What is the observed relationship between species richness and productivity? Reply. Ecology 84 (12), 3390–3395. Peris, S., Soave, G., Camperi, A., Darrieu, C., Aramburu, R., 2005. Range expansion of the European Starling Sturnus vulgaris in Argentina. Ardeola 52 (2), 359–364. Rahbek, C., 2005. Review: The role of spatial scale and the perception of large-scale species-richness patterns. Ecol. Lett. 8, 224–239. Ralph, C.J., Geupel, G.R., Pyle, P., Martin, T.E., DeSante, D.F., Milá, B., 1996. Manual de métodos de campo para el monitoreo de aves terrestres. Gen. Tech. Rep. PSWGTR-159. Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture, Albany, CA. Roback, P., Askins, R.A., 2005. Judicious use of multiple hypothesis tests. Conserv. Biol. 19, 261–267. Shochat, E., Warren, P.S., Faeth, S.H., McIntyre, N.E., Hope, D., 2006. From patterns to emerging processes in mechanistic urban ecology. Trends Ecol. Evol. 21, 186–191.
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41 Sorace, A., Gustin, M., 2008. Homogenisation processes and local effects on avifaunal composition in Italian towns. Acta Oecol. 33, 15–26. Storey, J.D., 2003. The positive false discovery rate: a Bayesian interpretation and the q-value. Ann. Stat. 31, 2013–2035. Turner, W.R., Nakamura, T., Dinetti, M., 2004. Global urbanization and the separation of humans from nature. Bioscience 54, 585–590.
41
Whittaker, R.J., Heegaard, E., 2003. What is the observed relationship between species richness and productivity? Comment. Ecology 84, 3384– 3390. Wiens, J.A., Rotenberry, J.T., Van Horne, B., 1987. Habitat occupancy patterns of North American shrubsteppe birds: the effects of spatial scale. Oikos 48, 132–147.
Contents lists available at ScienceDirect
Landscape and Urban Planning journal homepage: www.elsevier.com/locate/landurbplan
Bird community responses along urban–rural gradients: Does the size of the urbanized area matter? Pablo I. Garaffa a,∗ , Julieta Filloy a,b , M. Isabel Bellocq a,b a Dep. Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires–Ciudad Universitaria, Pab 2, Piso 4, C1428EHA C.A. Buenos Aires, Argentina b Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
a r t i c l e
i n f o
Article history: Received 9 November 2007 Received in revised form 11 September 2008 Accepted 2 October 2008 Available online 20 November 2008 Keywords: Urbanization Spatial patterns Community similarity Abundance Richness Argentina
a b s t r a c t Human settlements have a strong influence on bird communities. To explore the size effect of the urbanized area in avian community structure, we examined changes in species richness, composition and abundance along urban–rural gradients of different extensions. We measured land-cover variables and surveyed birds along nine urban–rural gradients in the Pampean region of Argentina. In towns over 7000 inh, increasing constructed area was negatively related to species richness. In towns over 13 000 inh, the abundance of native species decreased towards the urban core whereas total abundance increased, decreased or remained constant depending on town characteristics. In villages (<2000 inh), small (2000–14000 inh) and large towns (>60000 inh), there was a constant representation of the rural community composition along gradients. In towns of intermediate sizes (>14 000–60 000 inh), species composition was more similar to that from the rural zone as this zone was approached. Similarity between both urban-core and peripheral points and the rural zone decreased with increasing gradient extension. It appears to be a size threshold for community sensitivity to urbanization below which the impact on community attributes is insignificant; increasing urbanization above the threshold level had pronounced effects on bird assemblages. Research approaches separating responses of native and exotic species to urbanization enhance our understanding to favor native birds and quality of urban bird communities. The size of the urbanized area is a key factor in policies designed to improve ecosystem health and human interactions with nature. © 2008 Elsevier B.V. All rights reserved.
1. Introduction The conversion of natural habitats into managed systems and urbanization is a growing process (Alig and Healy, 1987). Urban areas are expanding in both size and quantity worldwide. As a result of urban development, native habitats are reduced and fragmented resulting in a landscape mosaic where impervious areas grow and natural vegetation remnants are progressively altered (Germaine et al., 1998; Marzluff et al., 1998). Human settlements have a strong influence on wildlife communities including birds (Chace and Walsh, 2004, and references therein). Typically, urban systems affect species diversity and composition of natural communities. Previous studies indicate that bird abundance increases and richness declines while approaching the urban core (Marzluff, 2001). It has been suggested that species composition of the avifauna in urban cores tend to be similar all over
∗ Corresponding author. E-mail address: [email protected] (P.I. Garaffa). 0169-2046/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.landurbplan.2008.10.004
the world, leading to biotic homogenization (Jokimäki et al., 1996; Blair, 2001; Clergeau et al., 2006a,b; McKinney, 2006). Thus, urban cores seem to hold a few, very abundant species, composing the “urban avifauna”. Bird species may respond differently to urban development and habitat fragmentation (Crooks et al., 2004). Earlier studies indicated that urbanization results in increasing numbers of exotic species and decreasing richness of native species (Marzluff, 2001; Turner et al., 2004). Thus, response patterns of the total avifauna may be influenced by the relative contribution of introduced and native species (Clergeau et al., 1998), hiding the actual mechanisms driving community attributes in urban environments. For that reason, the native-exotic species discrimination approach may be enlightening when studying spatial variation of urban bird communities. Factors influencing biodiversity may change with the spatial scale. The extension of a gradient or a geographic area may have a strong influence on patterns of species richness (Wiens et al., 1987; Rahbek, 2005). Although, there are some controversies about the effects of scale on richness response patters (Mittelbach et al., 2003; Whittaker and Heegaard, 2003), in non-urban gradients,
34
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
richness responses (less than 1000 m) are often monotonic along short environmental gradients whereas they are often unimodal in extensive gradients (Rahbek, 2005). The multi-scale approach to research along urban–rural gradients offers a promising opportunity to explore the factors underlying urban ecosystem patterns (McDonnell and Pickett, 1990; Clergeau et al., 2006b). For example, Jokimäki and Kaisanlahti-Jokimäki (2003) found that the composition of wintering bird communities changed above certain town size in Finland. However, the role that the size of urban systems plays in the biological consequences of urbanization remains unclear and little explored (Clergeau et al., 1998, and references therein; Clergeau et al., 2006a). Our aim is to explore the influence of the size of urbanized area on changes in the structure of breeding bird communities that occur along urban–rural gradients within a region. If size of the urbanized area affects community changes along the gradient, we expect a stronger effect on communities towards the urban core as gradient extension increases. To test this prediction, we examined changes in species richness, total bird abundance and species composition along urban–rural gradients of different length within the Pampean region in Argentina. We first measured habitat variables along each urban–rural gradient and identified the predictor variables that better explained changes in community attributes considering both native and exotic species. Then we performed further analyses to examine the intensity of the effect of the size of the urbanized area on bird community changes along gradients. Finally, we discussed the implications for future planning decisions that concern biodiversity conservation.
2. Methods 2.1. Study region and urbanized areas The research was conducted in villages (less than 2000 inh) and towns (small: 2000–14 000 inh; intermediate: >14 000–60 000 inh; large: over 60 000 inh) within the Pampean region, an extensive plain located in central-eastern Argentina (Fig. 1). The climate is warm-temperate averaging 7.5–9.5 ◦ C in July and 21.5–23 ◦ C in January. Precipitation ranges 800–1100 mm/year. The region was originally dominated by grasslands of the Poaceae (Cabrera, 1971). Since the Spanish colonization in the 16th century, the natural habitat has been gradually modified by agriculture, farming and human settlements (Facelli et al., 1989). Human population size and urban–rural gradient extent are commonly used to estimate town size (Clergeau et al., 2001; Jokimäki and Kaisanlahti-Jokimäki, 2003). We selected nine urbanized areas of different size (Table 1), and used either number of inhabitants or gradient extent (measured from the point at the urban core to the point reaching the rural zone) to indicate the size. Those urbanized areas were located at similar latitudes within the Pampean region to ensure the same regional context regarding the influence of climate, landscape matrix, and land uses (Fig. 1). 2.2. Bird surveys For each of the selected urbanized areas, a transect was established from the urban core to the rural zone. Transect length varied
Fig. 1. Location of the study urban–rural gradients. Ascending alphabetic order indicates increasing urbanized area size. (A) Rivas; (B) Castilla; (C) Rawson; (D) Suipacha; (E) SA Giles; (F) Chacabuco; (G) Mercedes; (H) Lujan; (I) La Plata.
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
35
Table 1 Information of the selected urbanized areas. Urbanized area name
Population (inhabitants)
Gradient extent (km)
Surveyed points
Rivas (A) Castilla (B) Rawson (C) Suipacha (D) SA de Giles (E) Chacabuco (F) Mercedes (G) Lujan (H) La Plata (I)
472 827 2184 7149 13 941 34 958 51 967 67 266 521 759
0.90 1.20 1.40 1.60 2.25 3.00 3.20 4.00 10.00
6 8 9 8 15 15 16 17 14
Land cover (mean % ± S.D.) OPEN 24.7 19.3 34.2 31.5 24.3 19.7 16.5 16.9 6.1
± ± ± ± ± ± ± ± ±
TREE 14.5 14.9 9.4 25.9 19.5 19.3 15.9 13.0 6.4
27.1 22.9 27.1 5.1 12.5 21.3 20.9 16.1 22.3
CONS ± ± ± ± ± ± ± ± ±
14.7 9.9 11.2 4.6 9.9 9.7 10.0 7.3 9.3
10.2 7.7 18.9 28.9 26.6 20.7 41.0 43.6 32.9
± ± ± ± ± ± ± ± ±
RURL 9.6 9.0 15.8 25.4 29.3 25.0 26.1 25.2 28.2
37.9 50.2 19.7 34.4 36.5 38.3 21.5 23.3 38.8
± ± ± ± ± ± ± ± ±
40.0 28.0 26.3 43.0 39.7 36.9 32.9 37.3 44.3
OPEN: non-paved open areas; TREE: canopy cover; CONS: constructed area; RURL: rural area with either cattle or agricultural activity.
according to gradient extension. Birds were surveyed using a fixed 50-m radius point-count method (DeGraaf et al., 1991; Ralph et al., 1996; Melles et al., 2003). The spacing of point-count sites varied between 150 and 200 m (in villages and small towns), 250 m (in intermediate and large towns) and 600 m (in the largest town). The shortest distance between count points was 150-m as it is the minimum distance recommended to avoid double counting (Bibby et al., 1998). Bird surveys were conducted by the same observers on clear and calm weekdays, between 6:00 and 10:00. In each point count site, all birds seen and heard were recorded during five minutes. We ignored aquatic birds and those birds flying overhead. Each urban–rural gradient was surveyed once during November 2005 (spring) to maximize the number of urbanized areas that could be sampled on similar conditions (e.g. weather, bird activity – detection). Bird richness estimation using a single-visit is an accepted method in urban areas (Jokimäki and Suhonen, 1998; Jokimäki and Kaisanlahti-Jokimäki, 2003). 2.3. Land-cover quantification Latin-American cities often tend to be polycentric due to socioeconomic factors (Janoschka, 2002; Borsdorf, 2003). In such cases, the distance from the urban core to the rural area might be inadequate to quantify the urban–rural gradient. Although some urbanized areas are polycentric in Argentina, we selected those showing a marked monocentric structure. Thus, the distance from the urban core reflected a decline in the degree of urbanization towards the rural area. The quantification of land-cover types along urban–rural gradients can be useful to explore the association of particular urban variables to bird communities (Alberti et al., 2001). We measured urban-core-rural distance (DIST) and four local land-cover variables using IKONOS satellite images: constructed area (CONS), canopy cover (TREE), non-paved open areas (OPEN) and rural area with either cattle or agricultural activity (RURL). Roads were paved at the urban points and non-paved at the urban-peripheral and rural points. Because there was no transition from paved to non-paved roads, changes in road conditions were abrupt (rather than gradual) along the urban–rural gradients; consequently, we did not include roads as an explanatory land-cover variable. To quantify land cover along gradients, we established an area of 75-m radius centered at each bird survey point. 2.4. Data analysis To quantify the urban–rural gradient, we first performed Principal Component Analyses (PCA) using the land-cover data matrices. This technique allowed a synthetic quantification of the gradient from the rural zone to the urban core for each village or town. Thus, the first factors resulting from the PCA can be associated
to a land-cover gradient that represents the spatial expression of the urban–rural gradient. Following the Kaiser Criterion, only factors with associated eigenvalues greater than one were considered (Kaiser, 1960). By analyzing changes in bird community attributes along urban–rural gradients of different extensions, we assessed the effects of the size of the urbanized area. To study changes in species richness and abundance along the urban–rural gradients of different extents, we ran simple regressions analyses to test the isolated responses of species richness and abundance to the selected factor scores. The analyses were conducted including and excluding exotic species. Among the significant relationships, the analysis of factor loadings for each land-cover variable identifies those habitat variables determining changes in community attributes. Regression assumptions were tested for every analysis. To examine changes in species composition along gradients, we analyzed community similarity among urban–rural points as a function of the PCA factors that represented each urban–rural gradient. For the analyses we pooled all rural points from the urban–rural gradients, setting up a standardized “pooled rural point” to more accurately represent the regional species pool. This rural-point grouping was performed to avoid potential biases in rural species composition due to single-visit surveys. We used a qualitative similarity index to describe changes in species composition within the urban–rural gradients. We calculated the Sörensen index (Si) for each urban–rural gradient (Jongman et al., 1995) between the “pooled rural point” and the rest of the gradient points. We performed simple regressions including and excluding exotic species. Again, the factor loadings for each land-cover variable allowed inferring the primary land-cover variable associated with changes in community attributes along the urban–rural gradients. We further studied the size effect of the urbanized area on bird community composition from the rural zone to the urban core. For each urban–rural gradient, we established the urban-core point (Cp) as the surveyed point at the urban extreme and the most peripheral point (Pp) as the last suburban point just beside the first rural point. To represent the regional species pool we used the “pooled rural point” (Rp). Thus, for each urbanized area we calculated the similarity (Si ) between Cp–Rp and between Pp–Rp. We performed simple regressions between the obtained similarity values and urban–rural gradient length to find the best fitting model (the highest coefficient of determination) explaining the size effect of the urbanized area on species composition along urban–rural gradients. To avoid spurious results due to alpha inflation under multiple tests, we used the QVALUE software (available at http://faculty.washington.edu/∼jstorey/qvalue/) based on the positive false discovery rate (pFDR) (Storey, 2003). P-values were converted to q-values and hypotheses were rejected at q-values below 0.05 (Roback and Askins, 2005).
36
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
3. Results 3.1. Description of gradients The environmental changes caused by different land-cover types that occurred from the urban core to the rural zone were mostly explained by two land-cover variables. All first PCA factors were highly and positively associated with constructed areas and negatively with rural areas dominated by either cattle or agricultural activity (Table 2). Those first PCA factors were also highly and negatively correlated to the urban-core distance. These results indicated that all first PCA factors represented primarily a gradient of increasing rural coverage and decreasing construction density from the urban core to the rural zone. Open areas and canopy cover only seemed to be relevant in some villages and towns showing
well-vegetated urban cores (e.g. Rivas, SA Giles and Lujan). The percentage of variation along urban–rural gradients explained by first PCA factors decreased with the size of the urbanized area, likely revealing increasing spatial complexity of the urban–rural matrix in larger towns (Table 2). Arrangement of points along PCA factors indicates that villages and small or intermediate towns displayed a clear gradient in habitat composition whereas data progressively aggregated at the extremes of first PCA factors with increasing town size (see Figs. 2–4). 3.2. Responses of species richness and abundance to gradient extent A total of 2564 individual birds from 52 species were recorded (Appendix A). Passer domesticus (House Sparrow) and Columba livia
Table 2 Factor-variable correlations (factor loadings) of land-cover variables for the First Factor derived from Principal Component Analysis. Land-cover variables Open areas (OPEN) Tree canopy (TREE) Constructed area (CONS) Rural area (RURL) Distance to urban core (DIST) Percentage of variance explained
Rivas (A)
Castilla (B)
Rawson (C)
Suipacha (D)
SA Giles (E)
Chacabuco (F)
Mercedes (G)
Lujan (H)
La Plata (I)
0.973 0.876* 0.865* −0.993* −0.950*
0.935 0.530 0.839* −0.997* −0.973*
0.216 0.331 0.918* −0.921* −0.951*
0.274 0.189 0.879* −0.958* −0.956*
−0.158 0.750* 0.896* −0.884* −0.967*
0.220 −0.128 0.899* −0.887* −0.967*
−0.139 −0.799* 0.976* −0.825* −0.950*
0.325 0.737* 0.854* −0.972* −0.823*
0.286 0.343 0.950* −0.988* −0.922*
87.7
76.0
55.1
54.3
62.2
51.9
63.9
60.0
58.6
*
*
Analyzed land-cover matrices included the entire set of urban–rural gradient points, from urban core to last point of rural zone. * P < 0.05.
Fig. 2. Relationship between bird species richness and the First Factor obtained from Principal Components Analysis. Analyses were performed for native species (dashed lines, open circles) and for both native and exotic species (solid lines, filled circles). Coefficient of determination and significance (q, adjusted p-values by QVALUE method) are represented for native (bottom left) and exotic species (top right). Second Factors were not significantly correlated in any case. Ascending alphabetic order indicates increasing urbanized area size. (A) Rivas; (B) Castilla; (C) Rawson; (D) Suipacha; (E) SA Giles; (F) Chacabuco; (G) Mercedes; (H) Lujan; (I) La Plata.
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
37
Fig. 3. Number of individuals recorded per point count arranged across the First Factor resulted from Principal Components Analysis. Presentation is as in Fig. 2.
(Rock Dove) were the only exotic species registered during the surveys, representing 25% of the total number of individuals observed in all urbanized areas. Bird species richness was sensitive to the size of the urbanized area. Simple regression analyses showed that richness was significantly affected in towns larger than 7000 inhabitants, considering both native species and native plus exotic species (Fig. 2). In these towns, increasing proportion of constructed area was associated to a decline in species richness, whereas the rural environment appears to enhance the number of species (Fig. 2). Changes in bird abundance along the urban–rural gradients were also affected by gradient extension. In villages and most small towns the abundance of native species was constant along the gradients (Fig. 3A–D). In towns over 13 000 inhabitants, however, native species decreased their abundance from the rural zone to the urban core (Fig. 3E–G and I), with perhaps one exception (Fig. 3H). When exotic species were included, three different patterns were found. Total bird abundance increased (Fig. 3A and H), decreased (Fig. 3E and G), or remained constant (Fig. 3F and I) from the rural zone to the urban core. Villages and towns below 13 000 inh, showed similar abundance responses for both native and total birds along gradients (Fig. 3B–D). 3.3. Responses of community composition to gradient extent Changes in species composition from the rural zone to the urban core depended on gradient extent, and two different spatial patterns of response could be identified along gradients. First, there was a constant subset of the rural matrix community along the gradients in towns smaller than 14 000 inh (Fig. 4A–E). The same
pattern held for the largest town where the similarity between urban points and the rural zone remained constant and relatively low for both native and all species (Fig. 4I). Second, in towns between 34 000 and 68 000 inh, the composition of native species became more similar to that of the rural zone as the zone was approached (Fig. 4F–H); when considering all species, the pattern held for towns between 34 000 and 52 000 inh (Fig. 4F and G). In all urbanized areas, peripheral points showed higher similarity in species composition to the “pooled rural point” than the urban-core points (Fig. 5); in both cases similarity decreased with increasing size of the urban area. The peripheral similarity showed a constant decline with increasing size of the urbanized area (straight function). Urban-core similarity showed a sudden decline with little increments in the size of the urbanized area, until a plateau is reached and similarity remained constant (inverse function). Patterns were similar in both only-native and native plus exotic assemblages. 4. Discussion For birds, size does matter. Our work showed that spatial patterns of bird community composition, richness and abundance from the rural zone to the urban core changed with the size of the urbanized area. There seems to be a town-size threshold for bird community sensitivity to urbanization, as found by Jokimäki and Kaisanlahti-Jokimäki (2003) in Finnish cities. Our results suggested the existence of thresholds between 7000 and 35 000 inh depending on the community attribute considered. Above that threshold, there is a significant effect of urbanization on community structure; and below the threshold, the impact is insignificant.
38
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
Fig. 4. The similarity (Si) in the composition of native species (dashed lines, open circles) and both native and exotic species (solid lines, filled circles) between each point and the “pooled rural point” vs. urbanization gradient (summarized by the First Factor resulted of Principal Component Analysis). Presentation is as in Fig. 2.
4.1. Responses of species richness and abundance to gradient extent We found that bird richness decreased towards the urban core in towns over 7000 inh. Previous studies comparing bird communities along a complete urban gradient, as we did, found that bird richness reached a peak at moderate levels of urbanization (Jokimäki and Suhonen, 1993; Blair, 1996, 2001; Crooks et al., 2004). In relatively arid environments of developed countries, suburban areas are usually well vegetated having higher primary productivity than either the core area or the surrounding environment (Imhoff et al., 2000). In villages and towns of the Pampean region in Argentina,
our results showed decreasing species richness as impervious area (i.e. land covered by concrete) increased towards the core area, and the pattern held for all urbanized areas beyond the size threshold. In rural areas of the Pampean region, primary productivity is higher than either urban or suburban areas which could explain the observed pattern in species richness (Guerschman et al., 2003). Below the urbanized area size threshold, it is possible that habitat changes along the gradient occurred at such a small spatial scale that bird species typical of rural areas also use urban areas. The patterns of abundance along urban–rural gradients reported in the literature are variable. While most studies reported that total bird biomass increases towards the urban core (Marzluff,
Fig. 5. Regression analysis between the urban core and the “pooled rural point” similarity (Cp–Rp) (filled circles), the peripheral point and the “pooled rural point” similarity (Pp–Rp) (open circles) vs. the urban–rural gradient extent. The analysis was performed for native (A) and for both native and exotic species (B).
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
2001), others suggested that bird abundance decrease towards more urbanized areas (Leveau and Leveau, 2004). In our study, abundance of native species decreased towards the urban core in most intermediate and large size towns; however, different patterns emerged when including exotic species. Our findings suggest that the abundance patterns along the gradients depend on both habitat structure (e.g. well-vegetated urban core) and the contribution of exotic species. Exotic bird species often tend to be aggregated in the most urbanized centric points due to high efficiency in exploiting urban resources (see review by Chace and Walsh, 2004). We found three patterns of abundance along the gradient. First, the smallest village (i.e. Rivas) had only one fully urbanized point along the gradient where the exotic individuals aggregate, increasing the total bird abundance and producing the observed pattern. A similar pattern of constant abundance of native species and increasing total abundance towards the urban core was also found for a large town (i.e. Lujan). In that case, the increasing tree coverage towards the urban core could promote the increasing total bird abundance and the maintenance of constant abundance of native birds trough the gradient. Well-vegetated urbanized areas are likely providing refuge, nesting sites, and food source for both native and exotic species. Second, for some towns above the 13 000 inh threshold (i.e. S.A. Giles and Mercedes) bird abundance declined towards the urban core either including or excluding exotic species. However, the negative effect of urbanization on the avifauna appeared to be less severe when including exotic species, as total bird abundance showed an apparent slighter response. That slighter effect caused by adding exotic species is better observed in a third pattern (i.e. Chacabuco and La Plata) where their inclusion leads to the absence of response. Thus, an increase in exotic species in town centers compensated the negative response by native species such that total bird abundance remained constant along the gradient. As patterns of response often differ considering or excluding exotic species, using the total bird abundance patterns may be insufficient to understand the mechanisms underlying community changes along urban–rural gradients. 4.2. Responses of community composition to the size of the urbanized area Every point of every urbanized area holds a subset of the regional pool of species. Towns and villages in the Pampean region are embedded in a rural matrix. The analysis of similarity in species composition between points along gradients and the rural zone showed that similarity was either constant or decreased from the rural zone to the urban core. When levels of urbanization are low (villages and small towns), there is a constant subset representation of the rural pool of species along the gradient; thus, similarity remains relatively constant and high. Increasing levels of urbanization may enhance the difference between both extremes of a gradient by decreasing the similarity between urban points and the rural zone. However, the largest town showed a similar pattern to that of villages and small towns, with similarity remaining constant along the gradient but at a lower level. Apparently, as the size of the urbanized area increases, bird assemblages along the gradients become more influenced by the urban-core environment; in contrast, the rural influence becomes more relevant as the size decreases. Both the decreasing pattern of similarity along urban gradients (Clergeau et al., 2006a) and the town size effect (Jokimäki and Kaisanlahti-Jokimäki, 2003) have been previously reported. In fact, Jokimäki and Kaisanlahti-Jokimäki (2003) found that bird community similarity among urban sectors within a town decreased over a threshold of 35 000–105 000 inh in Finland. Our results also showed a threshold for towns between 34 000
39
and 52 000 inh, but revealed another threshold point where the decreasing trend ends and similarity remains constant and low along the gradient. Not surprisingly, peripheral points were more similar to the rural zone than the urban cores in all study towns and villages. Nevertheless, our results revealed that increasing size of the urbanized area had a negative effect on similarity between urban points (i.e. peripheral and core points) and the rural zone, showing a stronger negative effect on urban-core bird assemblages than on peripheral assemblages. For villages and small towns, slight changes in size may lead to a more sudden reduction in similarity values in the urban cores than in the periphery. Bird assemblages from the urban cores seemed more sensitive to increasing urbanization than the peripheral assemblages. Clergeau et al. (2006a) found no town size effects in bird community and argued that detailed knowledge of habitat structure is required. Our analysis showed that, regardless of the knowledge of local habitat characteristics, the use of several urbanized areas determining an urban-size gradient (from a small village to a large town) allowed to detect the size effect of the urbanized area. 4.3. Final remarks Increasing urbanization had pronounced effects on bird communities. Most studies on animal or plant responses to urbanization were based on the comparison between few sites with different levels of development (Crooks et al., 2004). Our study, incorporating complete and well described urban–rural gradients into a gradient of sizes of urbanized areas, allowed to reveal urbanization thresholds at which bird community attributes started to respond; and a saturation point where urbanization reached the maximum effect. The clarification of patterns and the examination of potential environmental forces driving diversity along urban gradients is a further step to the understanding of mechanisms causing the observed patterns (Shochat et al., 2006). Town core areas seem to be holding the same few and very abundant “urban exploiters” worldwide, by providing resources that enhance exotic species colonization and restrict native species settlement. In other regions of the New World, most communities in highly urbanized areas are dominated by three exotic birds, introduced from Europe and adapted to high levels of land covered by concrete and low tree density: House Sparrows, Rock Doves and European Starlings (Sturnus vulgaris) (Melles et al., 2003; Crooks et al., 2004). House Sparrows and Rock Doves were also very common in urban cores of the Pampean region, and were often found aggregated in squares and recreation areas. Although we recorded no European Starlings in our surveys, this recently introduced species is increasingly expanding into the Pampean region (Peris et al., 2005). The patterns we detected here might be best reflected by alternative biological models including taxa with higher number of exotic species in urban areas. Urbanization was defined as the primary force promoting biotic homogenization worldwide, where a few widespread and locally abundant “urban-adaptable” species would occur in urban environments around the world (McKinney, 2006; Sorace and Gustin, 2008). In that scenario, most of the urban world human population is meant to live in global biological poverty (Turner et al., 2004). Research approaches separating responses of native and exotic species to urbanization will enhance our understanding to favor native birds and quality of urban bird communities. The size of the urbanized area has a strong effect on urban bird communities and it is a key factor to be considered in urbanization policies to improve ecosystem health and human interactions with nature. It would be interesting to evaluate whether the described patterns hold in other biogeographic regions.
40
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41
Acknowledgements We appreciate comments made by G.A. Zurita, J. Jokimäki and two anonymous reviewers to the manuscript. The work was financially supported by the Universidad de Buenos Aires and the Consejo Nacional de Investigaciones Científicas y Técnicas (Argentina). Appendix A. List of bird species found in the gradients Family
Scientific name
Common name
Tinamidae Ardeidae
Nothura maculosa Syrigma sibilatrix Casmerodius albus Elanus leucurus Ictinia plumbea Rostrhamus sociabilis Buteo magnirostris Polyborus plancus Milvago chimango Vanellus chilensis Larus maculipennis Columba picazuro Columba maculosa Columba livia Zenaida auriculata Columbina picui Myiopsitta monachus Guira guira Athene cunicularia Chlorostilbon aureoventris Colaptes campestris Colaptes melanolaimus Furnarius rufus Anumbius annumbi Schoeniophylax phryganophila Synallaxis frontalis Machetornis rixosus Pitangus sulphuratus Tyrannus melancholicus Tyrannus savana Serpophaga nigricans Serpophaga subcristata Progne chalybea Phaeoprogne tapera Tachycineta leucorrhoa Troglodytes aedon Mimus satrurninus Turdus rufiventris Geothlypis aequinoctialis Sporophila caerulescens Sicalis luteola Sicales flaveola Zonotrichia capensis Ammodramus humeralis Poospiza nigrorufa Poospiza melanoleuca Carduelis magellanica Molothrus rufoaxillaris Molothrus bonariensis Molothrus badius Leistes superciliaris Passer domesticus
Spoted Nothura Whistiling Heron Great Egret White-tailed Kite Plumbeous Kite Snail Kite Roadside Hawk Southern Crested Caracara Chimango Caracara Southern Lapwing Brown-hooded Gull Picazuro Pigeon Spot-winged Pigeon Rock Dove Eared Dove Picui Ground-Dove Monk Parakeet Guira Cockoo Burrowing Owl Glittering-bellied Emerald Field Flicker Golden-Breasted Woodpecker Rufous Hornero Firewood-Gatherer Chotoy Spinetail Sooty-fronted Spinetail Cattle Tyrant Great Kiskadee Tropical Kingbird Fork-tailed Flycatcher Sooty Tyrannulet White-crested Tyrannulet Gray-breasted Martin Brown-chested Martin White-rumped Swallow House Wren Chalk-browed Mockingbird Rufous-bellied Thrush Masked Yellowthroat Double-collared Seedeater Grassland Yellow-Finch Saffron Yellow-Finch Rufous-collared Sparrow Grassland Sparrow Black-and-Rufous Warbling-Finch Black-capped Warbling-Finch Hooded Siskin Screaming Cowbird Shiny Cowbird Bay-winged Cowbird White-browed Blackbird House Sparrow
Accipitridae
Falconidae Charadriidae Laridae Columbidae
Psittacidae Cuculidae Strigidae Trochilidae Picidae Furnariidae
Tyrannidae
Hirundinidae
Troglodytidae Mimidae Turdidae Parulidae Emberizidae
Fringilidae Icteridae
Ploceidae
References Alberti, M., Coe, A., Botsford, E., 2001. Quantifying the urban gradient: linking urban planning and ecology. In: Marzluff, J.M., Bowman, R., Donnelly, R. (Eds.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell, MA, USA, pp. 89–105. Alig, R.J., Healy, R.G., 1987. Urban and built-up land area changes in the United States: an empirical investigation of determinants. Land Econ. 63, 215–226. Bibby, C., Jones, M., Mardsen, S., 1998. Expedition Field Techniques. In: Bird Surveys. Expedition Advisory Centre, London. Blair, R.B., 1996. Land use and avian species diversity along an urban gradient. Ecol. Appl. 6 (2), 506–519.
Blair, R.B., 2001. Creating a homogeneous avifauna. In: Marzluff, J.M., Bowman, R., Donnelly, R. (Eds.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell, Massachusetts, USA, pp. 459–486. Borsdorf, A., 2003. Hacia la ciudad fragmentada. Tempranas estructuras segregadas en la ciudad latinoamericana. Scripta Nova 7 (146) (available at: http://www. ub.es/geocrit/sn/sn-146(122).htm). Cabrera, A., 1971. Fitogeografía de la Argentina. Boletín de la Sociedad Argentina de Botánica 14 (1–2), 1–43. Chace, J.F., Walsh, J.J., 2004. Urban effects on native avifauna: a review. Landscape Urban Plan. 74, 46–69. Clergeau, P., Croci, S., Jokimäki, J., Kaisanlahti-Jokimäki, M.L., Dinetti, M., 2006a. Avifauna homogenisation by urbanisation: analysis at different European latitudes. Biol. Conserv. 127, 336–344. Clergeau, P., Jokimäki, J., Savard, J.P.L., 2001. Are urban bird communities influenced by the bird diversity of adjacent landscapes? J. Appl. Ecol. 38, 1122–1135. Clergeau, P., Jokimäki, J., Snep, R., 2006b. Using hierarchical levels for urban ecology. Trends Ecol. Evol. 21 (12), 660–661. Clergeau, P., Savard, J.P.L., Mennechez, G., Falardeau, G., 1998. Bird abundance and diversity along an urban–rural gradient: a comparative study between two cities on different continents. Condor 100, 413–425. Crooks, K.R., Suarez, A.V., Bolger, D.T., 2004. Avian assemblages along a gradient of urbanization in a highly fragmented landscape. Biol. Conserv. 115, 451– 462. DeGraaf, R.M., Geis, A.D., Healy, P.A., 1991. Bird population and habitat surveys in urban areas. Landscape Urban Plan. 21, 184–188. Facelli, J.M., Leon, R.J.C., Deregibus, V.A., 1989. Community Structure in grazed and ungrazed grassland sites in the flooding Pampa, Argentina. Am. Midl. Nat. 121, 125–133. Germaine, S.S., Rosenstock, S.S., Schweinsburg, R.E., Richarsdson, W.S., 1998. Relationships among breeding birds, habitat, and residential development in Greater Tucson, Arizona. Ecol. Appl. 8, 680–691. Guerschman, J.P., Paruelo, J.M., Di Bella, C., 2003. Land cover classification in the Argentine Pampas using multi-temporal Landsat TM data. Int. J. Remote Sens. 24, 3381–3402. Imhoff, M.L., Tucker, C.J., Lawrence, W.T., Stutzer, D.C., 2000. The use of multisource satellite and geospatial data to study the effect of urbanization on primary productivity in the United States. IEEE Trans. Geosci. Remote Sens. 38, 2549– 2556. Janoschka, M., 2002. El nuevo modelo de la ciudad latinoamericana: fragmentación y privatización. Eure 28, 11–20. Available at: http://www.scielo.cl/scielo.php? script=sci arttext&pid=S0250-71612002008500002&lng=en&nrm=iso. Jokimäki, J., Kaisanlahti-Jokimäki, M.L., 2003. Spatial similarity of urban bird communities: a multiscale approach. J. Biogeogr. 30, 1183–1193. Jokimäki, J., Suhonen, J., 1993. Effects of urbanization on the breeding bird species richness in Finland: a biogeographical comparison. Ornis Fennica 70, 71–77. Jokimäki, J., Suhonen, J., 1998. Distribution and habitat selection of wintering birds in urban environments. Landscape Urban Plan. 39, 253–263. Jokimäki, J., Suhonen, J., Inki, K., Jokinen, S., 1996. Biogeographical comparison of winter bird assemblages in urban environments in Finland. J. Biogeogr. 23, 379–386. Jongman, R.H.G., ter Braak, C.J.F., Van Tongeren, O.F.R., 1995. Data Analysis in Community and Landscape Ecology. Cambridge University Press. Kaiser, H.F., 1960. The application of electronic computers to factor analysis. Educ. Psychol. Meas. 20, 141–151. Leveau, L.M., Leveau, C.M., 2004. Comunidades de aves en un gradiente urbano de la ciudad de Mar del Plata, Argentina. Hornero 19, 13–21. Marzluff, J.M., 2001. Worldwide urbanization and its effects on birds. In: Marzluff, J.M., Bowman, R., Donnelly, R. (Eds.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell, MA, USA, pp. 19–47. Marzluff, J.M., Gehlbach, F.R., Manuwal, D.A., 1998. Urban environments: influences on avifauna and challenges for the avian conservationist. In: Marzluff, J.M., Bowman, R., Donnelly, R. (Eds.), Avian Ecology in an Urbanizing World. Kluwer Academic, Norwell, MA, USA, pp. 283–296. McDonnell, M.J., Pickett, T.A., 1990. Ecosystem structure and function along urban–rural gradients: Aan unexploited opportunity for ecology. Ecology 71, 1232–1237. McKinney, M.L., 2006. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260. Melles, S., Glenn, S., Martin, K., 2003. Urban bird diversity and landscape complexity: species-environment associations along a multiscale habitat gradient. Conserv. Ecol. 7, 5 (available at: http://www.consecol.org/vol7/iss1/art5/main.html). Mittelbach, G.G., Scheiner, S.M., Steiner, C.F., 2003. What is the observed relationship between species richness and productivity? Reply. Ecology 84 (12), 3390–3395. Peris, S., Soave, G., Camperi, A., Darrieu, C., Aramburu, R., 2005. Range expansion of the European Starling Sturnus vulgaris in Argentina. Ardeola 52 (2), 359–364. Rahbek, C., 2005. Review: The role of spatial scale and the perception of large-scale species-richness patterns. Ecol. Lett. 8, 224–239. Ralph, C.J., Geupel, G.R., Pyle, P., Martin, T.E., DeSante, D.F., Milá, B., 1996. Manual de métodos de campo para el monitoreo de aves terrestres. Gen. Tech. Rep. PSWGTR-159. Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture, Albany, CA. Roback, P., Askins, R.A., 2005. Judicious use of multiple hypothesis tests. Conserv. Biol. 19, 261–267. Shochat, E., Warren, P.S., Faeth, S.H., McIntyre, N.E., Hope, D., 2006. From patterns to emerging processes in mechanistic urban ecology. Trends Ecol. Evol. 21, 186–191.
P.I. Garaffa et al. / Landscape and Urban Planning 90 (2009) 33–41 Sorace, A., Gustin, M., 2008. Homogenisation processes and local effects on avifaunal composition in Italian towns. Acta Oecol. 33, 15–26. Storey, J.D., 2003. The positive false discovery rate: a Bayesian interpretation and the q-value. Ann. Stat. 31, 2013–2035. Turner, W.R., Nakamura, T., Dinetti, M., 2004. Global urbanization and the separation of humans from nature. Bioscience 54, 585–590.
41
Whittaker, R.J., Heegaard, E., 2003. What is the observed relationship between species richness and productivity? Comment. Ecology 84, 3384– 3390. Wiens, J.A., Rotenberry, J.T., Van Horne, B., 1987. Habitat occupancy patterns of North American shrubsteppe birds: the effects of spatial scale. Oikos 48, 132–147.