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Introduction
Urbanization is a process in which humans establish and develop cities (Vlahov and Galea, 2002; Berkowitz et al., 2003; United Nations, 2014). This process implies the transformation of preexisting non-urban systems into urban novel ones with unique physical, biological, and social traits (Alberti et al., 2003; Grimm et al., 2008; Pickett et al., 2011). In general, urban areas are established to fulfill human modern housing needs, which have varied along regions and through time (Berry, 2008). Thus, as the urbanization process tends to replace original vegetation, as well as many other important local changes, it represents a threat for biodiversity in larger scales (Czech and Krausman, 1997; Czech et al., 2000; McKinney, 2006; Kowarik, 2011; Aronson et al., 2014).
As a crucial ecological component of urban areas, its vegetation provides important social and environmental benefits to urban dwellers (Dwyer et al., 1992; Tyrväinen et al., 2005; Manning, 2008), as well as a wide array of resources for wildlife species that dwell within cities (Ortega-Álvarez and MacGregor-Fors, 2011; Antonini et al., 2013; Ramírez-Restrepo and Halffter, 2013; Lintott et al., 2014). Moreover, it is noteworthy that tree and shrub diversity, composition, cover, and spatial distribution within a city are basically driven by the interaction between physical (e.g., topography), ecological (e.g., preexistent vegetation type) and human factors (e.g., planting, pruning, preference for some species, socioeconomics; Zipperer et al., 1997; Dwyer et al., 2000; Ramage et al., 2013), often representing part of the identity of cities (Konijnendijk, 2008; Li et al., 2011). In general, urban trees and shrubs are located on sidewalks, median strips, and urban greenspaces (e.g., woodlands, parks, cemeteries, gardens; Konijnendijk et al., 2005; Ardila et al., 2012), commonly aggregated and distributed unevenly throughout cities (Escobedo and Nowak, 2009; McConnachie and Shackleton, 2010; Cohen et al., 2012).
Although urban vegetation has received important attention by urban ecologists in the past (Rowntree, 1984; Jim, 1988; Zipperer et al., 1997; Luck et al., 2009; Ortega-Álvarez et al., 2011), little is known about their ecological patterns and processes in highly biodiverse regions; woefully, Latin America is not an exception (MacGregor-Fors and Ortega-Álvarez, 2013; Pauchard and Barbosa, 2013). Although many studies on trees and shrubs in Mexican urban areas have been concentrated in Mexico City (e.g., Díaz-Betancourt et al., 1987; Cruz, 1989; López-Moreno and Díaz-Betancourt, 1989; López-Moreno, 1991; Chacalo and Corona, 2009; Ortega-Álvarez et al., 2011), there is a growing number of studies focusing on different aspects of urban trees and shrubs (e.g., diversity, origin, spatial distribution, environmental function, landscape architecture, management, social perception) in other cities, such as: Monterrey, Nuevo León (Alanís, 2005); Mérida, Yucatán (Sosa and Flores, 1993; Orellana et al., 2003; López-Falfán, 2008); Campeche, Campeche (Niembro-Rocas, 1992); Chihuahua, Chihuahua (Alcalá et al., 2008); Morelia, Michoacán (Conejo, 2011; Sánchez and Peralta, 2013; Camacho-Cervantes et al., 2014); and Xalapa, Veracruz (Arias, 1983; García-Campos, 1993; Ruiz-Montiel et al., 2014).
Particularly, the city of Xalapa-Enriquez (referred to as Xalapa hereafter) has recently received special attention as it represents an excellent urban laboratory due to its location and orography that promote highly biodiverse wildlife communities (Capitanachi et al., 2001; Williams-Linera et al., 2002; MacGregor-Fors et al., 2015). Previous studies have assessed the woody vegetation of Xalapa in specific areas of the city, most of which include greenspaces (e.g., Arias, 1983; García-Campos, 1993; Díaz-Betancourt and López-Moreno, 1993; Capitanachi and Amante, 1995; SCDEPEV, 2010; Lemoine, 2012; Ruiz-Montiel et al., 2014); however, there is an important dearth of knowledge regarding the woody vegetation along its streetscapes, including its spatial distribution.
In this study, we focused on the streetscape of Xalapa using a city-wide survey approach. City-wide surveys take into account the spatial heterogeneity of the ecological, infrastructure, and social conditions of the city, allowing studies to have a representative sample of its most frequent scenarios (Turner, 2003; Davies et al., 2011; McCaffrey and Mannan, 2012). Based on previous studies, we expected that the surveyed trees and shrubs would show: (1) low species richness (López-Moreno and Díaz-Betancourt, 1991; Li et al., 2011; Yang et al., 2012), (2) high representation of exotic species (Castillo-Campos, 1991; López-Moreno and Díaz-Betancourt, 1991; Kuruneri-Chitepo and Shackleton, 2011; Wang et al., 2012), and (3) an uneven distribution of richness across the city (Landry and Chakraborty, 2009; Kuruneri-Chitepo and Shackleton, 2011; Kendal et al., 2012).
Objectives
To generate an updated species list of trees and shrubs of the streetscape of Xalapa based on a city-wide approach, describing their native/exotic ratio.
Materials and methods
Study area
We performed this study in the city of Xalapa (19°32'37" N, 96°54'37" W), including its conurbation with Banderilla (Municipality of Banderilla), Guadalupe Victoria (Municipality of Tlalnehuayocan), and Bugambilias (Municipality of Emiliano Zapata). The urban continuum of Xalapa has a territory of ~60 km2 and is an updated version of that proposed by Lemoine (2012), based on MacGregor-Fors (2010), and current ongoing research (Muñoz-Robles et al., unpublished data) (Fig. 1). Following its 600 m elevation gradient (1120 m 1720 m asl; Inegi, 2009), Xalapa has a semicalid climate on its southeast side, while a temperate climate dominates its northwestern section (Soto and Gómez, 1993). The original vegetation of the region was diverse, comprised mainly of pine forests, oak forests, cloud forests, and tropical dry forests (Castillo-Campos, 1991). Currently, ~20% of the city's area is covered by woody vegetation (Lemoine, 2012) and, as in many other cities in the world, it is comprised of a mixture of native and exotic species, basically confined to greenspaces (e.g., parks, streets, gardens; Castillo-Campos, 1991; García-Campos, 1993; Ruiz-Montiel et al., 2014).
Field surveys and plant identification
To establish sampling sites across Xalapa, we used a polygon of the city from ongoing research (Muñoz-Robles et al., unpublished data). Briefly, we delimited the polygon of Xalapa following spatial aggregation and communication criteria on an up-to-date high-quality satellite image. We then set a 750 m × 750 m grid on the polygon of the city and considered the centroid of cells as sampling sites. Finally, we adjusted the position of sampling sites in situ to the nearest accessible public area where sampling was feasible. The resulting number of sampling sites was 110, which for security reasons at some peri-urban areas of the city was reduced to 106 (Fig. 1).
We surveyed trees and shrubs in 106 sites, identifying all species present in an area of 150 m2 per site. Due to the complexity of urban areas and their streetscapes, we used three procedures depending on the nature of the sampling site, considering the same survey area: (1) two 75 m transects on both sidewalks of streets without median-strips, (2) three 50 m transects on both sidewalks and the median-strip, when the latter were present, and (3) two 50 m transects on both sides of pathways of greenspaces and a parallel one 5 m away from the pathway.
All trees (including palms) and shrubs (including hedges) inside the surveyed area were recorded and identified to species level, whenever possible. When we were not able to identify an individual in the field, we collected a sample for further identification in the herbarium (Herbario XAL, Inecol). We identified the recorded trees and shrubs using available identification keys and specialized literature (Arias, 1983; Benítez et al., 2004; Calderón and Rzedowski, 2005; Pennington and Sarukhán, 2005; Vázquez, 2007; Chacalo and Corona, 2009; the "Flora de Veracruz" series; and those in www.tropicos.org). Some species that could not be determined in the herbarium were identified by an expert botanist (G. Castillo-Campos, pers.com.). Nevertheless, three tree individuals could not be identified as we could not get a field sample during the fieldwork due to their height and/or location. We will deposit all collected samples with herbarium minimum requirements in the Herbarium XAL (Inecol).
Data analysis
Although we could not identify all recorded trees and shrubs to species level, we considered all identified taxa as species because we are certain that they belong to different species. After identifying all recorded tree and shrub species, we determined their origin and categorized them in native and exotic. We based the native/exotic categorization in relation to the region of study (central Veracruz), considering species as exotic if they do not occur naturally in central Veracruz (Richardson et al., 2000; Lodge and Shrader-Frechette, 2003; Jørgensen and Fath, 2008). We also contrasted our results with those reported in previous studies considering taxonomical changes in a world-wide database (Tropicos: www.tropicos.org). In order to set our species list into context, we compared it with previous local and regional studies (Arias, 1983; García-Campos, 1993; Díaz-Betancourt and López-Moreno, 1993; Capitanachi and Amante, 1995; SCDEPEV, 2010; Lemoine, 2012; Ruiz-Montiel et al., 2014).
We used basic statistics to describe average, standard deviation, and data distribution of tree and shrub richness species recorded per sampling site. We carried out a two-sample Kolmogorov-Smirnov test to compare the distributions of the proportions of both native and exotic species. Due to the non-normality of our data (i.e., native and exotic tree and shrub species richness assessed with one sample Kolmogorov-Smirnov test: D = 0.60, P < 0.001; D = 074, P < 0.001, respectively), we carried out a Wilcoxon rank-sum test for paired data to compare the values of native and exotic richness. We performed all statistical procedures in R (R Development Core Team, 2012).
Results
We recorded a total of 1116 trees and shrubs in our citywide survey. Of them, we identified 140 species (Table 1), 126 to the species level, eight to genus, and three to family, while three specimens could not be identified at all, reason why they were not considered in further analyses. From the 49 recorded families, the one with highest representation was Arecaceae (12 species), followed by Fabaceae (10 species), Fagaceae (9 species), and Malvaceae (8 species). It is noteworthy that almost half (47%) of the recorded families were represented by a single species. In relation to their distribution in the city, the six most frequent species were: Weeping Fig (Ficus benjamina; 32% of the sampling sites), Chinese Hibiscus (Hibiscus rosa-sinensis; 19% of the sampling sites), Paper Flower (Bougainvillea glabra; 15% of the sampling sites), Rhododendron (Rhododendron sp.; 15% of the sampling sites), Mexican Cypress (Cupressus lusitanica; 15% of the sampling sites), and Little-leaf Boxwood (Buxus microphylla; 15% of the sampling sites; Fig. 2, Table 1).
Table 1 List of recorded tree and shrub species in the streestscape of Xalapa, Veracruz, ordered alphabetically by family.
1 Origin: native/exotic in relation to central Veracruz.
2 Frequency: number of sampling sites where the species was recorded (n = 106). a Arias (1983), b García-Campos (1993), c Díaz-Betancourt & López-Moreno (1993), d Capitanachi & Amante (1995), e SCDEPEV (2010), f Lemoine (2012), g Ruiz-Montiel et al. (2014).
* Not previously reported to the urban area of Xalapa.
** These two shrubs may comprise several taxonomic entities, nevertheless, for practical matters, we report them here as one unknown species.
From the trees and shrubs we could identify and relate to their geographical origin (n = 131 species), 55.7% are exotic and 44.3% are original of central Veracruz. When considering the six most frequent species (found in > 15 sampling sites), only one is native to central Veracruz (Mexican Cypress-Cupressus lusitanica). An important difference found between the surveyed sites from greenspaces (i.e., Cerro de la Galaxia, Cerro Macuiltepetl, Ecologic Reserve Tejar-Garnica, Seminario Mayor, Parque Natura) and the rest of highly developed urban areas was a higher presence of native tree and shrub species (68% in five greenspaces; 36% in 101 highly developed urban sites).
Regarding all tree and shrub species richness across Xalapa, we recorded values ranging from 0-20 species per sampling site, with an average of 4.8 (± SD 4.9) species. After excluding the 19 sites where we did not record any tree or shrub (located basically in the downtown and peripheral areas of the city; Fig. 1), native tree and shrub richness per sampling site ranged from 0-10 species, with an average of 1.8 (± SD 2.1) species. Contrastingly different to native species, exotic species richness was higher, with up to 15 species per sampling site (average: 3.9 ± SD 3.7 species). According to the Wilcoxon rank-sum test for paired data, significant differences exist between the amount of native and exotic species per sampling site, with the later showing higher numbers (V = 661.5, P < 0.001).
As predicted, the spatial distribution of tree and shrub species richness showed to be unequally distributed across the city, with the richest sites (with > 15 tree and shrub species) located in the northern part of the city (Fig.1). Interestingly, sampling sites with the highest values of exotic species were also located in the northern-central portion of the city (Fig. 3). We found no clear spatial distribution patterns for neither native nor exotic species richness across the city (Fig. 3). Still, the few sampling sites at which we recorded 100% native trees and shrubs are mainly located on peripheral areas of Xalapa, while those where we recorded 100% exotic trees and shrubs are dispersed throughout the city (Fig. 4). Although the proportion of recorded native and exotic tree and shrub species ranged from 0%-100% per site, the average percentage of exotics was of 65.7% (± SD 31.7% species), and was of 33.0% (± SD 31.4%) for natives, with the frequency distribution of native/exotic ratios showing significant differences (two-sample Kolmogorov-Smirnov test: D = 0.44, P < 0.001; Fig. 4).
Figure 3 Spatial distribution of native and exotic trees and shrubs recorded in the streetscape of Xalapa.
Figure 4 Distribution of the origin (native/exotic) of trees and shrubs recorded in the streetscape of Xalapa.
Discussion and Conclusion
Urban vegetation is dynamic due to the human forces behind its presence and abundance (McPherson et al., 1997; Zipperer et al., 1997; Hope et al., 2006; Ortega-Álvarez et al., 2011; Ramage et al., 2013). Our results show that tree and shrub species richness of the streetscape of Xalapa is high, with an important exotic component, and unevenly distributed across the city. Due to the human forces driving its streetscape, the unique location of the city of Xalapa in a highly biodiverse region did not prevent the replacement of its vegetation in the urbanization process, completely shifting its species composition (Castillo-Campos, 1991; Williams-Linera et al., 2002).
Throughout the globe, street tree species richness varies among urban areas, with some medium-sized cities, as Toledo (Ohio, USA; ~ 225 km2) showing high values (170 species; Subburayalu and Sydnor, 2012), while others, also larger than Xalapa (e.g., Bangalore, India: ~740 km2; Curitiba, Brazil: ~430 km2; Bangkok, Thailand: ~1570 km2) have fewer species (108, 122, 127, respectively; Thaiutsa et al., 2008; Nagendra and Gopal, 2010; Bobrowski and Biondi, 2012) than those we report for Xalapa. Although comparing street tree richness of different cities is complex due to the nature of the surveys, as well as the location of the cities, it is clear that Xalapa has a considerably high number of tree and shrub species richness along its streetscape. When we compared our results with previous studies focused on the urban vegetation of Xalapa, we noted 32 species that had not been previously reported for the city, of which half are native and half are exotic. It is notable that we recorded a higher number of species when compared to a study of vegetation in public spaces of Xalapa (102 tree species; Arias, 1983); nonetheless, the number of species reported in greenspaces of Xalapa is higher (187 tree and shrub species; Capitanachi and Amante, 1995; ~185 woody species; García-Campos, 1993). These comparisons show the kind of results that city-wide surveys can provide, often underestimating species from urban greenspaces, which are often unevenly distributed throughout cities (also recorded for other wildlife groups; Nilon et al., 2011).
Previous studies have suggested that urban tree and shrub species composition changes with time (LópezMoreno and Díaz-Betancourt, 1991; Dwyer et al., 2000; Alanís, 2005). In Xalapa, this is the case of the exotic Weeping Fig (F. benjamina), by far the most frequent species of the streetscape of Xalapa (Fig. 2). This exotic species is not reported by Arias (1983), but is reported in the subsequent published literature of urban vegetation for the city. Regardless that this species has caused urban-related problems (e.g., urban sidewalks cracks) and has even been considered as inadequate for planting in urban areas (Conejo, 2011; Moro and Westerkamp, 2011; Vargas-Garzón and Molina-Prieto, 2012), the Weeping Fig has been extensively planted throughout the country since the mid-1990s (Vargas-Garzón and Molina-Prieto, 2012), becoming a dominant urban tree in many cities.
As expected, we recorded a high proportion exotic species. This is consistent with previous studies that have found important number of exotic species dominating urban streetscapes (e.g., 62.8%: López-Moreno and DíazBetancourt, 1991; 56%: Kuruneri-Chitepo and Shackleton, 2011; 61.8%: Ortega-Álvarez et al., 2011; ≥ 50%: Sjöman et al., 2012; 48.3%: Wang et al., 2012). The high proportion of exotics in Xalapa is due to the import of plant species from other parts of Mexico and the rest of the world for several reasons (e.g., ornamental, edibility, erosion control; Castillo-Campos, 1991; Eldredge, 2002; Verhoef and Morin, 2010). High tree and shrub species richness recorded in the streetscape of Xalapa is heavily biased by the introduction of exotic species, pattern that has been recorded in cities from around the globe (McKinney, 2008).
Regarding the spatial distribution of the studied tree and shrub species, it was not surprising to find an unequal distribution of species richness values across the city; such pattern has been reported for other urban areas from around the world (Landry and Chakraborty, 2009; Kuruneri-Chitepo and Shackleton, 2011; Kendal et al., 2012). The unequal distribution of greenspaces and woody vegetation across Xalapa has been reported previously by García-Campos (1993) and Lemoine (2012), but to our knowledge, there are no previous studies that report the unequal spatial distribution of woody plant species richness along its streetscapes. Nevertheless, further studies are needed to identify the processes behind this pattern, exploring which variables could be associated with this particular spatial configuration of species richness in Xalapa.
Our results, mainly the unequal distribution of tree and shrub species richness across the streetscape of Xalapa, as well as the high proportion of recorded exotics should be considered carefully, as they have been associated to the irregular distribution of the benefits that vegetation can provide to citizens (Garzón et al., 2004; Escobedo and Nowak, 2009; McConnachie and Shackleton, 2010; Cohen et al., 2012; Kendal et al., 2012). Also, the high proportion of exotic species needs to be considered due to the potential negative effects of such species, including a vast array of detrimental effects that have been documented on local, and even regional, ecological processes (Vitousek et al., 1997; Schmidt and Whelan, 1999; Richardson et al., 2000; McKinney, 2004).
