Effects of vegetation strata and human disturbance on bird diversity in green areas in a city in southern Chile

The area covered by urban settlements is increasing rapidly, since the world’s urban population is expected to increase by 72% between 2000 and 2030 (Pickett et al. 2011). Urbanisation is a dominant geographical trend and an important component of global change, with unprecedented implications for socio-economic, cultural and environmental characteristics. This accelerated urbanisation process is a threat to biodiversity conservation (Clergeau et al. 2001; Pickett et al. 2011), and may cause alterations of ecological systems and malfunctioning of urban systems as they are presently structured (McDonnell et al. 1997). McNeely et al. (1990) define biological diversity as a concept that encompasses the variety of nature, including the number and frequency of ecosystems, species and genes; Halffter and Ezcurra (1992) recall that it is the result of the evolutionary process and Solbrig (1994) clarifies that it is not an entity, a resource, but a property or characteristic of nature.

Due to the fragmentation or complete elimination of the natural habitats over which cities are built or expanded, an urban system contains only a small surface area with fragments of original vegetation or even artificial green areas (Rees 1997). The result is a drastic change in fauna, with a reduction in the original abundance and diversity, as documented by various authors: birds (e.g., Blair and Launer 1997; Faggi 1998; Blair 1999; Cam et al. 2000); marsupials (e.g., Almeida et al. 2008); rodents (e.g., Cavia et al. 2009); bats (e.g., Oprea et al. 2009); amphibians (e.g., MacGregor-Fors et al. 2013); reptiles (e.g., Cossíos and Icochea 2006); and fish (e.g., Cunico et al. 2011).

Biotic homogenization is considered to be one of the most prominent forms of biotic impoverishment induced by current global changes. It is described as the process by which species invasions and extinctions increase the genetic, taxonomic or functional similarity of two or more biotas over a specified time interval (Olden 2006; Devictor et al. 2008; Knop 2016). It has been demonstrated that the homogenization of bird communities is strongly positively correlated to landscape disturbance and fragmentation (Devictor et al. 2008). Considering that cities tend to homogenize the physical environment, consequently, as they expand, biological homogenization increases because the urban-adaptable species become increasingly widespread and locally abundant (McKinney 2006). By that, the urban conservation should therefore focus on promoting preservation and restoration of local indigenous species and their habitats (McKinney 2006).

The rural bird communities compared with urban bird communities have lower average evolutionary distinctiveness (Morelli et al. 2016) and by other hand in the urbanized environments, changes in phylogenetic richness and evolutionary distinctiveness are less substantial in moderately urbanized environments that still preserve much of the original diversity (Sol et al. 2017). The urban environments are a factor of concern for maintaining diversity across the tree of life of birds, and the urbanization planning could help buffer extreme loss of phylogenetic diversity caused by this process (Morelli et al. 2016).

However, green areas, including original fragments, can help to conserve native diversity (e.g., flora, birds), improving the functioning of these artificial systems in the long term (e.g., Chace and Walsh 2006). This has been shown in various green areas such as urban gardens in Hamilton, New Zealand (Day 1995); private gardens, semi-public spaces associated with apartment buildings, public parks and courtyards of industrial buildings in Zurich, Lucerne and Lugano in Switzerland (Fontana et al. 2011); urban parks in Hong Kong (Zhoua et al. 2012); urban parks in Beijing (Morelli et al. 2017) and Santiago of Chile (Urquiza and Mella 2002). For further research in Latin America see Ortega-Álvarez and MacGregor-Fors (2011a). All these studies address bird diversity in disturbed and/or artificial habitats with species surviving from the original habitats. Interest in the urban ecology of birds is growing (Grimm et al. 2000, 2008; Garaffa et al. 2009); however, most research in Latin America has focused on species lists, which, although they provide valuable information, need to be complemented by other aspects such as demographic patterns, physiological and behavioural ecology, interactions between exotic and native species and adaptation processes and functional diversity (Ortega-Álvarez and MacGregor-Fors 2011a, b; MacGregor-Fors and Ortega-Álvarez 2013).

During the 19th century, the coastal mountain range in southern Chile between the Biobío River and Puerto Montt (approx. 36°‒41°S) was thickly forested. In the north–south lying central depression, the forest was not so dense; the woods which covered the gullies and hills alternated with cleared areas in the plains where the indigenous people practiced various forms of agriculture (Góngora 1862; de Vivar 1979; Camus 2002; Solari et al. 2011).

After the Spanish occupation, fragmentation of the native vegetation was intensified due to the expansion of farmland, particularly from the second half of the 19th century. The new structure of the countryside was dominated by continuous anthropic matrices, enclosing isolated fragments of secondary native forest (Gantz and Rau 1999; Rau and Gantz 2001). This process was accompanied and accelerated by strong urban expansion of the main cities of southern Chile. The impact of this urban expansion on bird communities appears to have been high, but knowledge is still at a rudimentary stage (Chace and Walsh 2006).

The objective of the present study was to analyse the bird diversity in green areas of the city of Temuco and to characterise the environments which the birds occupy, in order to answer the following questions. Which structural elements of green areas (e.g., vegetation strata) affect bird diversity and species richness the most? Is this avian diversity affected by the diversity and origin (native/exotic) of the vegetation? Is it affected by human disturbance (e.g., proportion of bare soil area, vehicle traffic adjacent to green areas)?

In our study we found out that the three most important variables for bird diversity were the surface area, the cover of the shrub stratum and the presence of native species of shrub. So the structural elements of green areas affect bird diversity. This diversity is affected by some human disturbance like the bare soil areas, but not by vehicle flow, plant structure and tree and shrub cover.

Willson and Armesto (2003) stated that the consequences of fragmentation for bird species depend on their habitat requirements and their home range, and that larger areas, such as parks, are more likely to be colonised by rare or randomly distributed species. The surface area would therefore explain the greater diversity (species richness) in the parks as compared to squares and median strips of main streets; however, the diversity was also correlated with the number of tree species in the squares, the presence of shrub species of native origin and the absence of bare soil areas. It seems that native shrubs present in the study area offer more food (e.g., Ugni molinae, Berberis buxifolia, Berberis darwini, Fuchsia magellanica).

In squares and median strips of main streets, the majority of bird species were exotic (60%), which was rather less than the percentage documented in some European cities (80%) (e.g., Blair and Launer 1997; Chace and Walsh 2006). This is explained by the lack of natural habitat (high proportion of bare soil areas) and intolerance to human disturbance (Vejrup 2004), for this reason the exotic species Passer domesticus is a bird associated with anthropized environments around the world (De Laet and Summers-Smith 2007). In this study a significant linear relation was demonstrated between bird diversity (species richness) on the one hand, and the surface area of the units, the shrub cover and the presence of native species on the other. The lower diversity of birds in squares and median strips of main streets compared to their diversity in parks may be explained by the smaller surface area and isolation in a hostile matrix (Fahrig 2003). In this type of green area the surface areas are small (< 4 ha) and structurally simple, with geometric architecture, rectangular in the squares and linear in the median strips of main streets. In addition, their location in the city centre results in the predominance of tall buildings all around, narrow streets with high vehicle flows, low or poor plant cover and large bare soil areas, similar to the situation described in other Southern Hemisphere cities with low diversity (e.g., Garitano-Zavala and Gismondi 2003; Leveau and Leveau 2004, 2006; Faggi and Perepelizin 2006; Pauchard et al. 2006). Clergeau et al. (2001) and Jokimäki and Kaisanlahti-Jokimäki (2003) reported that cities offer a habitat for birds independent of the phyto-geographical origin of the plants (native/exotic) because plants are a scarce resource. In this study this was true for the origin of tree species, but the native origin of shrub species was positively correlated with bird diversity.

With respect to disturbance caused by vehicle traffic, Chace and Walsh (2006) reported that it causes isolation of populations, alteration of acoustic communication patterns, and direct mortalities due to collisions with vehicles, reducing the recreation value of green areas as well as their value as fauna corridors (Nilsson and Randrup 1997). In this study, however, we found no significant correlation between vehicle flow and bird species richness. Although the bare soil area variable presented a significant negative correlation with bird species richness in town squares and median strips of main streets, it was not considered in the model as it does not occur in the three parks.

This is a very interesting case of urban ecosystem, because of the environmental characteristics of the city (e.g., high air pollution, low surface of green areas, vegetation ecotone between sclerophyll and temperate rainforest), and the proximity to protected areas (Ñielol, Rucamanque) (Romero et al. 2001). The landscaping of the green areas in Temuco is European in style, characterised by exotic tree and shrub species and little native flora. These mosaics of small-scale habitats contain a high diversity of vegetation but are very small in area, with the character of plant collections. Anguita (2003) proposed that many of these exotic plant species (shrubs and trees) have little value for native bird species especially because they have a low food supply. The preference of town planners and urban landscapers for exotic species does not favour the creation of habitats suitable for birds, which is why many birds only visit these green areas but do not reside or nest there. Furthermore the vegetation in green areas is subjected to regular intervention (e.g., pruning, fumigation and removal of dead plants), displacing bird species which require intact plant cover, dead stumps, plant litter, or a quiet habitat (Lim and Sodhi 2004). Finally, urbanisation tends to select omnivorous or grain-eating species, and those which nest in cavities, and drives the progressive loss of insectivorous and nectarivorous species dependent on structurally diverse and/or native vegetation for both shelter and food resources, so this type of habitat increases avian biomass but reduces diversity (White et al. 2005).

Greater connectivity increases the area of habitat that birds can occupy, resulting in greater species richness, while a larger surface area of green areas would allow greater abundance due to an increase in the habitat available to the species already present in a fragment (Shanahan et al. 2012). A combined focus on improving the connectivity and the habitat in terms of life forms, diversity and connectivity (e.g., higher number of tree species, greater proportion of native shrub species, soil with plant cover, plants which provide food) would lead to an increase in the richness of bird species in green areas. For future research, it would be interesting to study their relationships with nearby protected areas, and the habitat requirements for the different bird species and their relationships with different vegetation strata and plant functional groups.

Ecological research has moved into the cities, and the challenge is to put knowledge into practice, with regulatory policies based on incentives which influence the design of green infrastructure to really conserve and increase biodiversity (Hostetler et al. 2011; Steiner 2011). For all this it is recommended in the planning and management of the green areas of cities in the south of Chile, to include native vegetation, especially increasing its cover (in park, square and median strips of main streets) and, as much as possible, increasing its surfaces. To increase the avian diversity we propose, for park and square, increasing the coverage of shrubs and trees of different heights and as far as possible to decrease the bare soil. For median strips it is proposed to increase the coverage of shrubs and medium height trees.

The bird diversity varied significantly according to the type of urban green area. Greater diversity, expressed as species richness and evenness, was observed in parks than in town squares and median strips of main streets. The environmental variables presenting significant correlations with bird diversity were: surface area, native species of shrub stratum, shrub cover, and bare soil area. The BEST multiple regression model showed that the three most important variables for bird diversity are the surface area of the green area, the cover of the shrub stratum and the presence of native shrub species. All these variables should be considered by urban planners in the construction or modification of urban green areas, in order to avoid biotic homogenization.