Butterfly diversity in a regional urbanization mosaic in two Mexican cities

Landscape and Urban Planning 115 (2013) 39–48

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Research paper

Butterfly diversity in a regional urbanization mosaic in two Mexican cities Lorena Ramírez Restrepo, Gonzalo Halffter ∗ Red Ecoetología, Instituto de Ecología A.C., Carretera Antigua a Coatepec 351, El Haya, Xalapa 91070, Veracruz, Mexico

h i g h l i g h t s • Within two urban areas butterfly species richness was higher than that of nearby forest ecosystems. • The highest number of species was found in areas of ecological protection in the two cities. • The butterflies in these areas reveal a dynamic process which involves many of the species from the nearby forests, along with others.

a r t i c l e

i n f o

Article history: Received 17 May 2012 Received in revised form 6 March 2013 Accepted 11 March 2013 Keywords: Abundance Richness Evenness Nymphalidae Landscape Latin America

a b s t r a c t Latin America is one of the most urbanized developing regions, however little is known about the biodiversity of its cities and the way this biodiversity is affected by landscape and local variables. We evaluated butterfly diversity in two Mexican cities by establishing four categories of urbanization: urban, suburban, areas of ecological protection (AEP) and forest. Butterflies were sampled at 300 m length and 10 m wide transects; rooted-fruit baited traps; and intentional sampling. Species accumulation curves indicate that sampling completeness was 91%; fifty species were recorded, with Satyrinae: Satyrini the richest group (15 species), and Heliconiinae the poorest subfamily (8 species). The AEP and forests had the highest (38 species) and lowest (21 species) richness respectively. Diversity and evenness were low in the most urbanized environments, indicating that urban butterfly ensembles are dominated by few abundant species. As expected, species turnover was greatest between forests and the urban area (Whittaker’s species turnover = 50.88). Local variables accounted for 74.9% of the variance in the abundance data, with mean environmental temperature, relative humidity, the number of pedestrians and plant cover the most important variables. At the level of the landscape, at small scale (50 and 100 m) arboreal vegetation cover (%VA) was the most important variable, meanwhile, as the scale increased the variables related to urbanization such as construction cover, number of pedestrian and distance to the center of the city became increasingly important. Connecting forest patches near cities with ecological protected areas would have a positive impact on butterfly diversity. © 2013 Elsevier B.V. All rights reserved.

1. Introduction Urbanization can be characterized as an increase in human habitation together with an increase in energy consumption and the extensive and intensive modification of the landscape, resulting in a system that does not depend on local natural resources (McDonnell & Pickett, 1990). Urbanization is a dominant demographic tendency and an important component of the global transformation of the Earth (Pickett et al., 2001), nowadays more than half of the human population is living in cities (Grimm et al., 2008), highlighting the importance of studying biodiversity in urban systems.

∗ Corresponding author. Tel.: +52 228 842 1842; fax: +52 228 8121897. E-mail addresses: [email protected] (L. Ramírez Restrepo), [email protected] (G. Halffter). 0169-2046/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.landurbplan.2013.03.005

Urban development is expected to increase dramatically in less developed regions of the world (e.g., Africa, Asia, Latin America) in the next decades (Ortega-Álvarez & MacGregor-Fors, 2011). According to the projections of the National Population Council (CONAPO, 2003), 90.2 million of 127.2 million inhabitants of Mexico will live in cities by 2030. Since Mexico is being urbanized at such a galloping rate (Garza & Schteingart, 2010), it is vitally important to carry out studies that allow us to understand the biodiversity dynamics associated with each urban landscape. Urban landscapes have a very high degree of heterogeneity in land use resulting from the broad range of human activities (Felson & Pickett, 2005), and the wide variety of small scale cultural practices (gardens, orchards, different types of buildings, green area management, waste management, etc.), this situation make cities very complex and interesting environments for scientific research. Fortunately, every day more researchers and institutions in Latin America are recognizing the importance of studying cities, their biodiversity and ecological processes.

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Fig. 1. Study area and location of sampling sites. Ma: Macuiltepetl Hill, Cu: Las Culebras Hill, Cl: Natural Protected Area Francisco Javier Clavijero, Br: Briones, Pi: La Pitaya, Ag: Agüitafria, Cr: Cruz Duela. (Satellite image from Google Earth 20013).

The aim of this study is to investigate the effects of urbanization on butterfly diversity of two Mexican cities: Xalapa and Coatepec.To this end, we used these butterflies groups of the Nymphalidae family (Biblidinae, Heliconiinae, Satyrini and Ithomiini) in a tropical mountain region in the center of the state of Veracruz. We studied species richness; abundance, evenness in guild composition of butterflies, and the influence that variables associated with urbanization and the local environment have on these measures of butterfly diversity. 2. Methods The study was performed in the cities of Xalapa and Coatepec in central Veracruz, located on the northern side of the Cofre de Perote Mountain Range facing the Gulf of Mexico (Fig. 1). Both urban areas together cover 41,300 ha and are inhabited by approximately

528,400 residents. The original vegetation cover was mainly tropical mountain cloud forest (Pineda, Moreno, Escobar, & Halffter, 2005), but the cover of cloud forest was calculated at only 7.6 percent (9.3 km2 ) and continues being threatened by the expansion of urban informal settlements (Benítez et al., 2012). The city of Xalapa is located at 19◦ 54 N, 96◦ 54 W and is the state capital. Its elevation ranges from 1350 m a.s.l. in the southeast, to 1550 m a.s.l. at the peak of Macuiltépetl Hill. The mean annual temperature ranges from 17 to 20 ◦ C and mean annual precipitation varies between 1600 and 1900 mm (Pineda et al., 2005). Xalapa is a fast growing city, according to Lemoine-Rodríguez (2012) the rate of growth of Xalapa’s urban area was for the decade of 2000–2010 of 11.24 km2 . Benítez, Pérez-Vázquez, Nava-Tablada, Equihua, & Álvarez-Palacios (2012) showed that by 2007, 90 percent of the land area in the municipality of Xalapa had already been altered by human activity.

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Fig. 2. Example of a buffer for the sampling points: a.) Site location and capacity of the buffer, and b.) Outcome of the digitization of different land uses.

Coatepec is bordered by Xalapa to the northwest and is located at 19◦ 21 N, 96◦ 47 W. The elevation of this city is 1252 m a.s.l. (INEGI, 1995). At 1355 m a.s.l. the Las Culebras Hill (Snake Hill) Ecological Reserve, mainly covered by secondary forest and coffee plantations, is the highest point in the urban area. The mean annual temperature ranges from 18 to 20 ◦ C and mean annual precipitation varies between 2000 and 2500 mm (Gómez & Soto, 1990). There’s no published information about the growth of Coatepec’s urban area, but urbanization is rapidly replacing shaded coffee plantations.

Buffer areas 50, 100, 250 and 500 m in radius were generated around each sampling point to evaluate the effect of the landscape variables on butterfly diversity at different spatial scales (Fig. 2). For each buffer these spatial cover types were calculated: (1) Arboreal vegetation (AV), (2) Low vegetation (LV), (3) Buildings (B), and (4) Lakes and ponds (L&P). Data for the sites and the number of inhabitants (Pn) were obtained from the national population and housing census (INEGI, 2005). Additionally, the distance to the center of the nearest city was calculated using the main cathedrals of Xalapa and Coatepec as reference points.

2.1. Sampling sites

2.2. Data analysis

Sampling was carried out at nine localities, taking into account their location with respect to the two cities, as well as their type of land use. The nine sites were assigned to four categories: (1) Urban: Xalapa and Coatepec; (2) Suburban: Briones and La Pitaya; (3) Areas of ecological protection (AEP): Macuiltepetl Hill, Las Culebras Hill and the Protected Natural Area Francisco Javier Clavijero. (PNAFJC); (4) Forest: Agüita Fría and Cruz Duela (Fig. 1). Butterfly sampling. Between May and November 2008 each site was visited every two months, between 0830 and 1830 h. Butterflies were sighted and collected using three methods. (1) Baited traps: Five Van Someren-Rydon traps with attractants, baited with rotting banana, located along a 200-m-long sampling transect at 1–3 m above the ground and with 50 m between traps. (2) Fixed-length transects: Three transects 300 m long and 10 m wide, separated for at least 200 m, and were surveyed at a slow, constant pace with an aerial insect net. (3) Intentional sampling: Thirty minute collections by aerial net and direct observation in areas where butterflies were likely to be found, Butterflies were identified in the field with the help of specialized guides (Glassberg, 2007). In case that their identification was difficult, specimens were captured and identified at the laboratory and by consulting experts. Local variables. The following variables were measured every 100 m along the transects: (1) Canopy cover using a spherical densitometer, (2) elevation above sea level using a Garmin GPS 12XL, (3) air temperature, (4) relative humidity, (5) thermal sensation, (6) wind speed with the help of a pocket weather station (Kestrel® 3000), and (7) number of pedestrians found during the surveys. Landscape variables. We used an IKONOS satellite image provided by the BIOCAFE-INECOL project, and the program GoogleEarth Pro to obtain missing images for the study area.

Butterfly diversity. For each site and urbanization category, richness (number of species) and total abundance (number of individuals) were obtained. Local alpha diversity was obtained with each species count for the four sampling transects (using nets and traps) for each site. Mean alpha diversity was calculated for each sampling site by averaging the four local alpha values obtained during a day of sampling. In order to determine sampling effort, species accumulation curves were generated based on observed and estimated species for all of the records obtained in the urbanization categories using the program EstimateS 8.0 (Colwell, 2006) with 200 randomizations to avoid the effect of sampling order. The estimators of species diversity Chao 1 and Chao 2 were calculated as they take into account both species presence and their abundance. The Shannon–Wiener diversity index and Pielou’s evenness index were calculated using the program PAST, version 1.86b (Hammer, Harper, & Ryan, 2001) for each site and for each urbanization category. Additionally, Whittaker’s beta diversity indices were calculated as proposed by Halffter et al. (2001). Local and landscape variables. All variables were tested for normality (Shapiro–Wilk). The only non-normally distributed variable, the number of pedestrians, was square root transformed prior to any data analysis. In order to establish whether there are differences between local environmental variables and those of the environment for the four categories of urbanization studied (urban, suburban, areas of ecological protection and forests), one-way ANOVAs were applied using the program PAST version 1.86b (Hammer et al., 2001) at ˛ = 0.05, followed by Tukey’s multiple comparisons. Canonical correspondence analysis (CCA) was used to determine how much of the variation in butterfly species abundance could be explained by the local and landscape environmental variables using the program PC-ORD version 5.0 (McCune & Mefford,

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2006). Fifty species and nine sites were used in the analyses. Seven local environmental variables and six landscape variables were analyzed. The local and landscape variables were analyzed independently to avoid using different spatial scales in the same analysis (Morrison, Marcot, & Mannan, 1998; Wiens, 1989).

The analysis of variance to compare the richness and abundance of each group of butterflies in the different urbanization categories only detected significant differences in the richness of Biblidinae between forests and urban areas (F = 4.44, P = 0.0282, d.f. = 10.99), with species richness lower in the forests. Although there were no significant differences in the abundance of this subfamily, values were very high in the urban areas, mainly owing to the presence of flocks of Diaethria anna anna (Guérin-Méneville, [1844]), which was very common in muddy areas, on rotting fruit and even in garbage dumps. The AEP had the highest richness for Satyrini, though they had a lower abundance. Subfamily Heliconiinae showed no significant difference in richness and abundance at all the urbanization categories. Forests had the lowest number of Heliconiinae species and the most urbanized areas had the greatest number of individuals and species.

3. Results There were fifty species of butterflies, with Satyrini the richest tribe (15 species), followed by Biblidinae (14), Ithomiini (13) and Heliconiinae (8) (Table 1). With 38 species, the areas of ecological protection (AEP) had the highest richness, followed by the urban areas (36 species) and the suburban sites (27). Richness was lowest in the forests, which had 21 species (Table 2).

Table 1 Presence/absence list of butterfly species in four categories of urbanization in Xalapa and Coatepec, Veracruz, Mexico.

Urban Suburban EPA Biblidinae Biblis hyperia aganisa Boisduval, 1836 Catonephele numilia esite (R. Felder, 1869) Diaethria anna anna (Guérin-Méneville, [1844]) Diaethria astala astala (Guérin-Méneville, [1844]) Diaethria bacchis (Doubleday, 1849) Diaethria pandama (Doubleday, [1848]) Dynamine postverta mexicana Dálmeida, 1952 Epiphile adrasta adrasta Hewitson, 1861 Eunica monima (Stoll, 1782) Eunica tala tala (Herrich-Schäffer, [1855]) Hamadryas februa ferenna (Godart, [1824]) Hamadryas feronia farinulenta (Fruhstorfer, 1916) Hamadryas fornax fornacalia (Fruhstorfer, 1907) Hamadryas sp1 Heliconiinae Dione juno huascuma (Reakirt, 1866) Dione moneta poeyii Butler, 1873 Dryas iulia moderata (Riley, 1926) Eueides aliphera gracilis Stichel, 1903 Eueides Isabella eva (Fabricius, 1793) Heliconius charitonia vazquezae W.P. Comstock y F.M. Brown, 1950 Heliconius hortense Guérin-Méneville, [1844] Heliconius ismenius telchinia Doubleday, 1847

x x x

x x x x

x x x x

x

x x x x x x x x x

x

x x x

x x

x x x x x

x x x x x x

x x

x x

x x

x x x

Danainae: Ithomiini

Dircenna klugii klugii (Geyer, 1837) Episcada salvinia salvinia (H.W. Bates, 1864) Greta andromica lyra (Salvin, 1869) Greta annee annee (Guérin-Méneville, [1844]) Greta morgane oto (Hewitson, [1855]) Ithomia leila Hewitson, 1852 Mechanis menapis doryssus H.W. Bates, 1864 Mechanis polymnia lycidice H.W. Bates, 1864 Melinaea lilis imitate H.W. Bates, 1864 Oleria paula (Weymer, 1883) Pteronymia artena artena (Hewitson, [1855]) Pteronymia cotyo cotyo (Guérin-Méneville, [1844]) Satyrinae: Satyrini Manataria hercyna maculata (Hopffer, 1874) Oxeoschistus tauropolis tauropolis (Westwood, [1850]) Pareuptychia ocirrhoe (Fabricius, 1793) Pedaliodes circumducta Thieme, 1905 Tayges thamyra (Cramer, 1779) Satyrinae sp1 Satyrinae sp2 Satyrinae sp3

Forest

x x x x x x x x x

x x x x x x x x

x x x

x x

x x

x x

x x

x x

x x

x x

x x

x

x x x

x x x

x x x x

x

x x x x

x

x x x

x x

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Table 2 Butterfly diversity and evenness indices for the four urbanization categories. Species richness (S), cumulative number of individuals, Shannon–Wiener index (H ), Pielou’s Evenness index (J ), and Dominance Index (D).

Forest AEP Suburban Urban

S

# individuals

H

J

D

21 38 27 36

179 692 419 562

2.503 2.739 2.304 2.309

0.8223 0.7531 0.6991 0.6444

0.1078 0.09913 0.1584 0.1809

On comparing diversity (H ) using the method of Solow (1993), Shannon diversity of butterflies did not differ statistically between urban and suburban areas (D = 0.0825651; P = 0.1569; ˛ = 0.05), and both forests and AEP were more diverse than urban areas (D = 0.186685; P = 0.2005; ˛ = 0.05 and D = 0.397585; P = 0; ˛ = 0.05). Additionally, forests were not significantly different from AEP or suburban areas (D = 0.2109; P = 0.3678; ˛ = 0.05 and D = 0.2109; P = 0.0948; ˛ = 0.05). Beta diversity values were intermediate, with the highest – as expected – between the least similar categories: forest and urban areas; and the lowest between urban areas and AEP (Table 3), which are immersed in the city (with the exception of the PNAFJC, which is located approximately 3 km from the urban area of Xalapa). Species accumulation curves. Our sampling effort reached 90.9% of Chao 1’s estimated species richness (Fig. 3). For the different environments studied, the species accumulation curves revealed that the degrees of completeness, according to Chao 1, ranged from 77% for the urban area to 91% for the forests. It is possible that the urban areas are much more permeable to tourist species, with the continual arrival of new species preventing the species accumulation curves from reaching the asymptote (Fig. 4). Local and environmental variables. There were significant differences in the number of pedestrians between forests, the AEP and urban areas, between the urban and suburban areas,

Fig. 3. Species accumulation curve includes data from all three sampling methods.

Table 3 Whittaker’s beta diversity index.

Urban Suburban AEP

Suburban

AEP

Forest

33.33

21.62 32.31

50.88 41.67 32.2

Fig. 4. Species accumulation curves for each type of environment studied: a). Urban (77%), b). Suburban area (87%), c). Ecological Protection Areas (81%), and d). Forests (91%).

16.5 74.9 1

16.4 71.5 0.995 18 55.1 0.956

20.5 58.4 1

0.124

500 m

38 38 1

0.153

37.2 37.2 0.993

0.284

Axis 3 0.135

Eigenvalue Variance in species data: % of variance explained % of cumulative variance explained Correlation between species and environmental variables

Axis 2

0.279

Axis 1

Axis 2

Number of canonical axes: 3 Total variance of species data: 0.7494

Axis 3

Table 4 Summary of the canonical correspondence analysis for butterfly abundance and local environmental variables.

0.123

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Axis 1

44

16.4 74.7 0.999 20.4 58.3 0.999 37.8 37.8 0.999 12 68.6 0.871 19.1 56.6 0.982 37.5 37.5 0.996 20.2 53.1 0.998 32.9 32.9 0.947

9.5 62.6 0.86

0.123 0.153 0.284 0.09 0.143 0.281 0.071 0.151 0.247

Eigenvalue Variance in species data % Variance explained % Cumulative variance explained Correlation between species and environmental variables

Axis 2 Axis 1 Axis 3 Axis 2 Axis 2

Axis 3

Axis 1

Butterfly diversity. The city of Xalapa and Las Culebras Hill, an AEP, had higher species richness than the cloud forests. Similar results have been found for dung beetles by Rös, Escobar, & Halffter (2012) at Sierra Norte de Puebla, were species richness was higher in secondary forest than at the cloud forest. In a similar way, studying dung beetles, Pineda et al. (2005) found that richness was higher at shaded coffee agroecosystems than at cloud forest fragments at central Veracruz, México. For a wide variety of taxonomic groups (plants, vertebrates and invertebrates) richness can be greater in urban areas than in the surroundings, this higher richness in urban areas, usually results from the accelerated addition of nonnative species that replace some of the more sensitive native species before they completely disappear from urban areas (McKinney, 2002, 2008), creating an assemblage with greater species richness and with different origins: those that

Axis 1

4. Discussion

Total variance (inertia) in the species data: 0.7494

and between suburban areas and the AEP (F = 21.19, d.f. = 38.96; P = 2.649 × 10−8 ). The environmental variables were different between all sites with the exception of thermal sensation, which was the same on all study sites. The canonical correspondence analysis was performed including all 50 butterfly species, nine localities, 50 species, 7 local environmental variables and a variable indicating the urbanization category of each site (Urban, suburban, AEP, forest). The environmental variables explain 74.9% of the variance in the butterfly abundance data (Table 4), with mean air temperature, relative humidity, the number of passersby and plant cover, in that order, accounting for most of the variability (Table 5). For the landscape variables, the CCA indicated that three canonical axes explain from 62.9% of the variance in the species data for buffers with a 50 m radius to 74.7% for buffers with a 250 m radius (Table 6). At each spatial scale, different environmental variables were important. At smaller scales (50 and 100 m) the percent arboreal vegetation (%AV) had the greatest explanatory power. Unexpectedly, the relationship between the species and this variable was negative (Table 7). At larger scales the variables related with urbanization became more important: the percentage of buildings was most important and had a negative relationship with butterfly diversity (Table 7).

250 m

−0.706 −3.143 −0.061 2.309 0.629 −1.051 −0.261 0.176

100 m

Axis 3

2.023 5.163 −1.31 −4.76 −0.802 2.734 0.628 −0.683

50 m

Axis 2

0.416 1.166 0.689 −0.351 −0.393 0.456 0.331 0.312

Number of canonical axes: 3

Axis 1

Plant cover Temperature Relative humidity Thermal sensation Wind speed Passers by Elevation above sea level (m) Urbanization category

Table 6 Summary of the canonical correspondence analysis for butterfly abundance and the environmental variables of the landscape on different spatial scales.

Variable

Axis 3

Table 5 Canonical coefficients, resulting from the multiple regressions for all butterfly records and local environmental variables.

Table 7 Canonical coefficients, resulting from the multiple regressions for all butterfly records and the environmental variables of the landscape on different spatial scales. (AV: % arboreal vegetation; LV: % low vegetation; B: % with buildings; Pn: number of inhabitants; DC: distance to the city center; UC: urbanization category; L&P: % lakes and ponds). Variable

Standardized units

original units

S.D.

Axis 1

Axis 2

Axis 3

Axis 1

Axis 2

Axis 3

50 m

AV LV B Pn DC UC

−0.469 0.01 −0.225 0.375 0.056 −0.22

0.309 0.107 0.065 0.361 −0.117 0.049

−0.074 0.198 −0.606 0.471 −0.145 −0.067

−0.143 0.012 −0.108 0 0 0.043

0.094 0.124 0.031 0 0 −0.059

−0.022 0.228 −0.291 0 0 −0.059

3.28E+00 8.68E−01 2.08E+00 1.40E+05 1.83E+03 1.13E+00

100 m

AV LV B Pn DC UC

−1.09 −0.355 −0.258 −0.11 0.264 −0.499

0.519 0.299 −0.183 0.846 −0.175 0.142

−0.084 0.504 −0.91 1.066 0.097 −0.204

−0.388 −0.475 −0.133 0 0 −0.44

0.185 0.399 −0.094 0 0 0.125

−0.03 0.673 −0.469 0 0 −0.179

2.81E+00 7.49E−01 1.94E+00 1.40E+05 1.83E+03 1.13E+00

250 m

AV LV B L&P Pn DC UC

−1.343 −0.736 5.215 −0.244 −4.456 3.429 0.346

0.259 0.265 −3.671 0.257 3.196 −2.061 −0.531

0.358 0.326 0.067 −0.418 0.622 −0.117 0.097

−0.48 −0.921 2.959 −1.348 0 0.002 0.305

0.093 0.332 −2.083 1.419 0 −0.001 −0.468

0.128 0.409 0.038 −2.309 0 0 0.085

2.80E+00 7.99E−01 1.76E+00 1.81E−01 1.40E+05 1.83E+03 1.13E+00

500 m

AV LV B L&P Pn DC UC

0.707 −1.376 −3.932 −0.912 3.251 −1.49 0.029

−0.976 0.953 1.873 0.833 −1.56 0.627 −0.465

1.909 −0.757 −1.912 −1.166 2.658 −1.25 0.681

0.267 −1.751 −1.716 −5.805 0 −0.001 0.026

−0.369 1.213 0.817 5.303 0 0 −0.41

0.721 −0.963 −0.834 −7.427 0 −0.001 0.6

2.65E+00 7.86E−01 2.29E+00 1.57E−01 1.40E+05 1.83E+03 1.13E+00

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Spatial scale

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were originally in the area (and effectively belong there or are in the process of disappearance), those that arrive at these new environments but are just passing through (i.e. tourist species), or those that take advantage of the new resources offered by the cities and establish occasionally dominant populations (Jokimaki, 1999; Ruszczyk & Nascimento, 1999). Although species richness and abundance was high in the urban areas, butterfly assemblages in this category were less even, that is, they were dominated by a few very abundant species. Luniak (2008) states that abundance in communities of invertebrates in urban areas may be relatively high, and in many instances may exceed that of rural habitats, due to the presence of very frequent species that occasionally appear en masse (super dominant). One example is Diaethria anna anna with more than two hundred recorded individuals in the urban area of Coatepec, usually around a specific resource such as rotting fruit. This species occurred in very low numbers in forested areas. A similar example is Pterourus scamander scamander (Boisduval, 1836), considered the most abundant species of Papilionidae in the city of Porto Alegre in Brazil, but with small populations in natural environments (Ruszczyk, 1986). Sampling of urban areas was the least complete (77%), likely because of its high degree of spatial heterogeneity (Fermon, Waltert, Van-Wright, & Mühlenberg, 2005) that was not completely sampled at this study, and its permeability to tourist species from the cities. Tourist species are found in the urban community for brief periods of time, but neither reproduces nor maintains stable populations there. They may arrive as a result of physical phenomena such as geographic proximity to their area of origin, air currents or orographic conditions (Halffter & Moreno, 2005). Additionally, the areas of ecological protection (AEP) may be home to butterfly populations that move between urban areas and their green perimeters. It would be interesting to examine the dynamics of these butterfly assemblages with respect to functional connectivity, and to determine the role of urban reserves such as Macuiltepetl Hill and Las Culebras Hill in maintaining the biological diversity of Xalapa and Coatepec. Pin Koh and Sodhi (2004) stated that the increasing isolation of urban green areas negatively impacts on species richness in these environments. In Xalapa and Coatepec, the presence of urban reserves allows for the possibility of green areas to be connected to other urban green areas and at to adjacent green patches. As described by Brown and Freitas (2002), Heliconiinae and Ithomiini have showed a high tolerance to environmental conditions in urban areas. These groups of butterflies mainly feed on pollen and nectar, resources that are easily found in the urban mosaic studied. Regarding species distribution, 30% occurred from the forests to the urban areas, mainly representatives of Ithomiini such as Dircenna klugii klugii (Geyer, 1837), Episcada salvinia salvinia (Bates, 1864), Greta annette annette (Guérin-Méneville, 1844), G. morgana oto (Hewitson, 1855), Mechanitis menapis doryssus H.W. Bates, 1864, M. polymnia lycidice H.W. Bates (1864) and Pteronymia simplex fenochioi Lamas (1978). Ithomiini larvae feed almost exclusively on plants in the Solanaceae family (Brown & Freitas, 1994; Willmott & Mallet, 2004), which are economically important and very widespread, with more than 2500 species worldwide (Knapp, 2002). Eighty-nine percent of Ithomiini feed on Solanum which makes up 70% of the Neotropical Solanaceae (Willmott & Freitas, 2006). This plant family is one of the most diverse in the municipality of Coatepec (Luna, 1997), mostly represented by shrubs (Castillo-Campos & Luna, 2009), and outstanding for its endemic richness in the state of Veracruz (Tovar, 2003), which might account for the high richness of Ithomiini in the study region. Fourteen percent of the species were recorded in only one category of urbanization. For example, Pedaliodes circumducta Thieme (1905) was only recorded in forest, even though it was reported by

Hernández Baz (1993) for the municipality of Xalapa. This genus of butterflies belongs to the tribe Satyrini which often occurs in areas with low to intermediate levels of disturbance. P. zíngara, described by Heredia and Viloria (2004), was found in an area of cloud forest fragments surrounded by suburban and recreational properties in the Western Cordillera of the Colombian Andes. Three species of Biblidinae (Dynamine postverta mexicana Dálmeida, 1952; Eunica monima (Stoll, 1782) and E. tatila tatila (Herrich-Schäffer, 1855)) were only recorded in urban areas, mainly in the baited traps at Xalapa. Diaethria bacchis (Doubleday, 1849) was only caught in suburban areas on muddy roads, while the satyrini Taygetis thamrya (Cramer, 1779) was attracted to traps exclusively in the AEP. Butterfly species that are restricted to a certain environment may be responding to local factors – such as the availability of host plants for immature stages and adults – but that according to Ruszczyk (1986) have a notable effect on the distribution of butterflies in urban environments. The most contrasting categories of urbanization had the least similar butterfly fauna, urban areas and forests had high complementarity indices (>50). A similar result was reported by Blair and Launer (1997) and by Blair (1999) who found that no species were shared between the financial district (a highly urbanized area) in the city of Palo Alto, California and remnants of original forest in the region. The most similar urbanization categories, i.e. the AEP and urban areas, had the lowest complementarity. This could indicate that some species are actually moving between these environments, resulting in the most similar faunas within the regional mosaic of urbanization studied. Local and landscape variables. Climatic factors such as temperature are important in determining the richness and structure of butterfly communities, both at the local (Brown & Freitas, 2002; Checa, Barragán, Rodríguez, & Christman, 2009) and regional scales. In our study, temperature had the greatest explanatory power according to the CCA scores (Table 7). Factors such as plant cover and light intensity may also affect butterfly diversity and composition in tropical forests (Hamer et al., 2003; Hill, Hamer, Lace, & Banham, 1995; Laurance et al., 2002). The close dependence of butterflies on certain host plants may be an element that should have been explored to see whether butterfly distribution is related not only to habitat quality but also to the presence of this resource. In our study, at each spatial scale, different variables explained butterfly distribution to a large extent. At the smallest scale (50 m), human population, the percentage of arboreal vegetation and of buildings were the most important variables, while at a scale of 100 m, arboreal and low (pastures) vegetation along with the distance to the urban center had the most notable effect. Surprisingly, the relationship between butterfly diversity and the variables related to vegetation (percent arboreal and percent low vegetation) were negative, and were opposite to results for metropolitan Boston, USA (Clark, Reed, & Chew, 2007). The latter authors found that butterfly richness per visit was greater in areas with more plant cover at scales of 50 and 150 m. Our results, however, were similar to those reported for bees and butterflies in the city of New York (Matteson & Langellotto, 2010). Also, in a fragmented landscape in Brazil was found that the best predictor for the abundance of Satyrini and Biblidinae was the percent of pasture cover and for Satyrini the best nule model that explains the abundance of these butterflies was proportion of pasture present in 100 m of radius (Ribeiro, Batista, Prado, Brown, & Freitas, 2012). At greater spatial scales (250 and 500 m) the variables related to urbanization, such as the percentage of buildings, the human population and the distance to the city center became more important and were negatively related to butterfly diversity. Clark et al. (2007) reported similar results at a scale of 500 m with one variable related to urbanization (total road length) negatively related to butterfly diversity in the city of Boston.

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5. Conclusion The four groups of Nymphalidae were represented in all of the environments studied, but responded differently to urbanization, making it necessary to study in detail the biology and ecology of each group in the most highly urbanized environments. Butterfly diversity was significantly different between the least similar categories of urbanization (urban and forest), and although species richness and abundance was higher in the most urbanized areas, butterfly communities were dominated by fewer species than in the less urbanized areas. Temperature was the most important environmental variable to explain butterfly distribution in the study region. At the landscape level at smaller scales (50 and 100 m) there was strong but negative relation with vegetation variables meanwhile at the larger scales (250 and 500 m) there was a negative relationship between butterfly diversity and urbanization. Research based on landscape ecological theories can provide guidelines for urban planning, and management (Breuste, Niemelä, & Snep, 2008). For Xalapa and Coatepec, the AEP showed a very high species richness, their importance for the biodiversity at these two cities must be stated, Macuiltepetl Hill and Las Culebras Hill are located at the center of Xalapa and Coatepec respectively, these AEP’s need to be effectively managed and connected to peripheral green areas, and to the remnants of cloud forest near this urbanization mosaic. Acknowledgments We are grateful to the Consejo Nacional de Ciencia y Tecnología (CONACYT) for graduate studies scholarship number 244461/213179. Funding was provided for the project “Agroecosistemas y conservación de la biodiversidad en el centro de Veracruz” # 34103 by the Fondo Mixto, Gobierno del Estado de VeracruzCONACYT. Roberto Monroy provided guidance for the GIS analysis. Dr. Victor Rico-Gray kindly donated material and equipment. We are grateful to Dr. Klaus V. Mehltreter and three anonymous reviewers for helpful comments and discussion. We extend our thanks to Biol. Sergio H. Aguilar, Biol. Orlik García Gómez, Dra. Guadalupe ˜ Williams Linera, M. Sc.Claudia Gallardo, Dr. Inigo Verdalet Guzmán, M.Sc. Eva Piedra Malagon, Dr. Armando Aguirre and Dr.Hugo Fernando Lopez-Arevalo. Bianca Delfosse translated the manuscript from the original in Spanish References Benítez, G., Pérez-Vázquez, A., Nava-Tablada, M., Equihua, M., & Álvarez-Palacios, J. L. (2012). Urban expansion and the environmental effects of informal settlements on the outskirts of Xalapa city, Veracruz, Mexico. Environment and Urbanization, 24(1), 149–166. Blair, R. B. (1999). Birds and butterflies along an urban gradient: Surrogate taxa for assessing biodiversity? Ecological Applications, 9(1), 164–170. Blair, R. B., & Launer, A. E. (1997). Butterfly diversity and human land use: Species assemblages along an urban gradient. Biological Conservation, 80(1), 113–125. Breuste, J., Niemelä, J., & Snep, R. P. H. (2008). Applying landscape ecological principles in urban environments. Landscape Ecology, 23(10), 1139–1142. Brown, K. S., & Freitas, A. V. L. (1994). Juvenile stages of Ithomiini: Overview and systematics (Lepidoptera: Nymphalidae). Tropical Lepidoptera, 5(1), 9–20. Brown, K. S., Jr., & Freitas, A. V. L. (2002). Butterfly communities of urban forest fragments in Campinas, Sao Paulo, Brazil: Structure, instability, environmental correlates, and conservation. Journal of Insect Conservation, 6(4), 217–231. Castillo-Campos, G., & Luna, V. E., 2009. Flora y vegetación del municipio de Coatepec, Veracruz. (The flora and vegetation of the municipality of Coatepec, Veracruz) Flora de Veracruz. Fascículo complementario I. 280 pp. [In Spanish]. Checa, M. F., Barragán, A., Rodríguez, J., & Christman, M. (2009). Temporal abundance patterns of butterfly communities (Lepidoptera: Nymphalidae) in the Ecuadorian Amazonia and their relationship with climate. Annales de la Société Entomologique de France: Revue d‘Entomologie Générale et Appliquée (n.s.), 45(4), 470–486. Clark, P. J., Reed, J. M., & Chew, F. S. (2007). Effects of urbanization on butterfly species richness, guild structure, and rarity. Urban Ecosystems, 10(3), 321–337. Colwell, R., 2006. EstimateS: Statistical estimation of species richness and shared species from samples. Version 8. Persistent http://purl.oclc.org/estimates

47

CONAPO – Consejo Nacional de Población, 2003. Informe de ejecución. Programa Nacional de Población 2001–2006. (National Population Council. Performance report. National Population Program 2001–2006) México. Primera edición: julio de 2004. ISBN: 970-628-687-X. 22 pp. [In Spanish]. Felson, A. J., & Pickett, S. T. A. (2005). Designed experiments: New approaches to studying urban ecosystems. Frontiers in Ecology and the Environment, 3(10), 549–556. Fermon, H., Waltert, M., Van-Wright, R. I., & Mühlenberg, M. (2005). Forest use and vertical stratification in fruit-feeding butterflies in Sulawesi, Indonesia: Impacts for conservation. Biodiversity and Conservation, 14(2), 333–350. Garza, G., & Schteingart, M. (2010). ((1st ed.)). Desarrollo urbano y regional: Los grandes problemas de México (Urban and regional development: Major problems in Mexico) México, D.F: El Colegio de México. [In Spanish] Glassberg, J. (2007). A swift guide to the butterflies of Mexico and Central America. Morristown, NJ: Sunstreak. Gómez, M., & Soto, M. (1990). Atlas climático del municipio de Coatepec. (Climate atlas for the municipality of Coatepec) ((1st ed.)). Xalapa, México: Instituto de Ecología A.C. [in Spanish]. Grimm, N. B., Faeth, S. H., Golubiewski, N. E., Redman, C. L., Wu, J., Bai, X., et al. (2008). Global change and the ecology of cities. Science, 319, 756–760. Halffter, G., & Moreno, C. E., 2005. Significado biológico de las diversidades Alfa, Beta y Gamma. (The biological meaning of Alpha, Beta and Gamma diversity) Sobre Diversidad Biológica: El significado de las diversidades Alfa, Beta y Gamma. Monografías Tercer Milenio. Vol. 4 (5–18). [in Spanish]. Halffter, G., Moreno, C.E., Pineda, E.O., 2001. Manual para la evaluación de la biodiversidad en Reservas de la Biosfera. (Manual for the evaluation of biodiversity in Biosphere Reserves) M&T-Manuales y Tesis SEA, Vol. 2. Zaragoza. [in Spanish]. Hamer, K. C., Hill, J. K., Benedick, S., Mustaffa, N., Sherratt, T. N., Maryati, M., et al. (2003). Ecology of butterflies in natural and selective logged forests of northern Borneo: The importance of habitat heterogeneity. Journal of Applied Ecology, 40(1), 150–162. Hammer, Ø., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological statistics software package for education and data analysis. Paleontología Electrónica, 4(1), 9pp. http://palaeo-electronica.org/2001 1/past/issue1 01.htm Heredia, M. D., & Viloria, A. (2004). Description and life history of Pedaliodes zingara, a new satyrinae species from Colombia (Nymphalidae). Journal of the Lepidopterists’ Society, 58(2), 80–87. Hernández Baz, F., 1993. La fauna de Mariposas (Lepidoptera: Rhopalocera) de Xalapa, Veracruz, México. (The butterfly fauna of Xalapa) La Ciencia y el Hombre. 14: 55–88. [in Spanish]. Hill, J. K., Hamer, K. C., Lace, L. A., & Banham, W. M. T. (1995). Effects of selective logging on tropical forest butterflies on Buru, Indonesia. Journal of Applied Ecology, 32(4), 754–760. INEGI-Instituto Nacional de Estadística, Geografía e Informática, 1995. Estadísticas del Medio Ambiente. (Environmental Statistics) México. [in Spanish]. Jokimaki, J. (1999). Occurrence of breeding bird species in urban parks: Effects of park structure and broad-scale variables. Urban Ecosystems, 3(1), 21–34. Knapp, S. (2002). Floral diversity and evolution in the Solanaceae. In Q. C. B. Cronk, R. M. Bateman, & J. A. Hawkins (Eds.), Developmental genetics and plant evolution (pp. 267–297). London: Taylor and Francis. Laurance, W. F., Lovejoy, T. E., Vasconcelos, H. L., Bruna, E. M., Didham, R. K., Stouffer, P. C., et al. (2002). Ecosystem decay of Amazonian fragments: A 22-year investigation. Conservation Biology, 16(3), 605–618. Lemoine-Rodríguez, R., 2012. Cambios en la cobertura vegetal de la ciudad de Xalapa-Enríquez, Veracruz y zonas circundantes entre 1950 y 2010. (Changes in vegetation cover in the city of Xalapa-Enriquez, Veracruz and surrounding areas between 1950 and 2010.) Thesis. Facultad de Biología, Universidad Veracruzana. México. 44 p. [in Spanish]. Luna, V. E., 1997. Estudio de vegetación y flora del municipio de Coatepec, Veracruz. (A study of the vegetation and flora of the municipality of Coatepec) B.Sc. Thesis. Facultad de Biología. Universidad Veracruzana. Xalapa, Veracruz, México. [in Spanish]. Luniak, M., 2008. Fauna of the Big City – Estimating species richness and abundance in Warsaw, Poland. Urban Ecology. Marzluff et al., eds. pp: 349–354. Matteson, K. C., & Langellotto, G. A. (2010). Determinates of inner city butterfly and bee species richness. Urban Ecosystems, 13, 333–347. McCune, B., & Mefford, M. J., 2006. PC-ORD. Multivariate analysis of ecological data. Version 5.10. MjM Software, Gleneden Beach, Oregon, U.S.A. McDonnell, M. J., & Pickett, S. T. A. (1990). Ecosystem structure and function along urban–rural gradients: An unexploited opportunity for ecology. Ecology, 71(4), 1232–1237. McKinney, M. L. (2002). Urbanization, biodiversity, and conservation. BioScience, 52(10), 883–890. McKinney, M. L. (2008). Effects of urbanization on species richness: A review of plants and animals. Urban Ecosystems, 11(2), 161–176. Morrison, M. L., Marcot, B. G., & Mannan, R. W. (1998). Wildlife-habitat relationships: Concepts and applications ((2nd ed.)). USA: The University of Wisconsin. Ortega-Álvarez, R., & MacGregor-Fors, I. (2011). Dusting-off the file: A review of knowledge on urban ornithology in Latin America. Landscape and Urban Planning, 101(1), 1–10. Pickett, S. T. A., Cadenasso, M. L., Grove, J. M., Nilon, C. H., Pouyat, R. V., Zipperer, W. C., et al. (2001). Urban ecological systems: Linking terrestrial, ecological, physical, and socioeconomic components of metropolitan areas. Annual Review of Ecology and Systematics, 32(1), 127–157.

48

L. Ramírez Restrepo, G. Halffter / Landscape and Urban Planning 115 (2013) 39–48

Pin Koh, L., & Sodhi, N. S. (2004). Importance of reserves, fragments, and parks for butterfly conservation in a tropical urban landscape. Ecological Applications, 14(6), 1695–1708. Pineda, E., Moreno, C., Escobar, F., & Halffter, G. (2005). Frog, bat, and dung beetle diversity in the cloud forest and coffee agroecosystems of Veracruz, Mexico. Conservation Biology, 19, 400–410. Ribeiro, D. B., Batista, R., Prado, P. I., Jr., Brown, K. S., & Freitas, A. V. L. (2012). The importance of small scales to the fruit-feeding butterfly assemblages in a fragmented landscape. Biodiversity and Conservation, 21(3), 811– 827. Rös, M., Escobar, F., & Halffter, G. (2012). How dung beetles respond to a human modified variegated landscape in Mexican cloud forest: A study of biodiversity integrating ecological and biogeographical perspectives. Diversity and Distributions, 18, 377–389. Ruszczyk, A. (1986). Ecologia urbana da borboletas, I. O gradient de urbanizacao e a fauna de Porto Alegre, RS. (Urban ecology of butterflies. I. The gradient of urbanization and the fauna of Porto Alegre, RS). Revista Brasileira de Biología, 46(4), 675–688 [in Portuguese].

Ruszczyk, A., & Nascimento, E. S. (1999). Biologia dos adultos de Methona themisto (Hübner, 1818) (Lepidoptera, Nymphalidae, Ithomiini) em prac¸as públicas de Uberlândia, Minas Gerais, Brasil. (The biology of adult Methona themisto (Hübner, 1818) (Lepidoptera, Nymphalidae, Ithomiini) in the public places of Uberlândia, Minas Gerais, Brazil.). Revista Brasileira de Biología, 59(4), 577–583 [In Portuguese]. Solow, A. (1993). A simple test for change in community structure. Journal of Animal Ecology, 62(1), 191–193. Tovar, G. L., 2003. Endemismos de la flora vascular en Veracruz, México. (Endemisms in the vascular flora of Veracruz, Mexico) B.Sc. Thesis. Universidad Veracruzana. Facultad de Biología. Xalapa. México. [in Spanish]. Wiens, J. A. (1989). The ecology of bird communities. UK: Cambridge University. Willmott, K. R., & Freitas, A. V. L. (2006). Higher-level phylogeny of the Ithomiini (Lepidoptera: Nymphalidae): Classification, patterns of larval hostplant colonization and diversification. Cladistics, 22, 297–368. Willmott, K. R., & Mallet, J. (2004). Correlations between adult mimicry and larval hostplants in ithomiine butterflies. Proceedings of the Royal Society of London. (Biological Letters.), 271(Suppl.), 266–326.