The expansion of urban areas is one of the greatest and most widespread threats to biodiversity worldwide (Lee and Rotenberry, 2015; Banville et al., 2017). The shift from original natural habitats to urban habitats triggers profound changes in many environmental factors (McDonnell and Hahs, 2008; Seress et al., 2014). The alteration of vegetation cover; an increase of chemical, light, and noise pollution; and higher environmental temperatures have been reported as the main effects of urbanization (Yow, 2007; Fox, 2013; Díaz et al., 2022). Those changes have strong cascading effects on species composition of plant and animal communities at both regional and global scales (Grimm et al., 2008; Arroyo-Rodríguez et al., 2013; Aronson et al., 2014) and usually involve a dramatic reduction of biodiversity (McDonnell and Hahs, 2008; Seress et al., 2014; Beninde et al., 2015; Sherry, 2021).

The effects of urbanization have been evaluated using different taxonomic groups, such as plants (Kowarik, 2008), insects (McIntyre, 2000; Blair, 2001; Gaona et al., 2021), aquatic macroinvertebrates (Zúñiga-Sarango et al., 2020), mammals (McIntyre, 2000), amphibians and reptiles (Hutto and Barrett, 2021), and birds (Pennington and Blair, 2011; McClure et al., 2015; Maure et al., 2018; Souza et al., 2019; Morelli et al., 2021; Valente-Neto et al., 2021). Birds tend to be especially affected by urbanization due to their high degree of specialization (Beaumont et al., 2011; Hermes et al., 2018). As a general rule, the effects of urbanization on bird communities are negative (Pennington and Blair, 2011; McClure et al., 2015; Ibáñez-Álamo et al., 2017; Maure et al., 2018; Morelli et al., 2021), evidencing decreases in species richness and abundance (Chiari et al., 2010; MacGregor-Fors et al., 2010), as well as decreases in phylogenetic and functional diversity (Carvajal-Castro et al., 2019; Morelli et al., 2021; Valente-Neto et al., 2021). Nevertheless, there is evidence for some positive effects of urbanization on specific bird species (Chiari et al., 2010; MacGregor-Fors et al., 2010; Møller and Díaz, 2018a). Therefore, the responses of birds to urbanization are difficult to predict (Rodewald and Yahner, 2001) because such responses are species-specific (Forsman et al., 2010; Montaño-Centellas and Garitano-Zavala, 2015).

Negative effects of urbanization on birds are especially significant for frugivores and nectarivores (de Oliveira Ramos and dos Anjos, 2014; Souza et al., 2019) because flower and fruit abundance drops in urban areas (Schütz and Schulze, 2015; Concepción et al., 2017). In contrast, generalist species such omnivores, granivores, or invasive species (Sol et al., 2017), and those foraging on the ground (MacGregor-Fors and Escobar-Ibáñez, 2017), usually take advantage of these urban habitats (Chiari et al., 2010; MacGregor-Fors et al., 2010). Increased abundance of generalist birds within cities (Møller and Díaz, 2018a) is likely the result of a dramatic reduction of predators, nest parasites, and competitors (de Oliveira Ramos and dos Anjos, 2014; Møller et al., 2016; Møller and Díaz, 2018b), an increase in refuges and/or nesting sites (Leveau, 2018), a higher supply of food associated with humans (McKinney, 2002; De León et al., 2019; Díaz et al., 2022), and a longer breeding season due to a warmer climate, especially in higher latitudes (Møller et al., 2015).

On the other hand, the trophic-guild organization of birds is directly related to the vegetation structure, which in turn is determined by the degree of anthropic modification (Laurance and Bierregaard, 1997). Several studies showed a positive association between structural complexity of vegetation and bird diversity (Fajardo et al., 2009; Carranza-Quiceno et al., 2018). Forested areas have greater plant diversity, occupying different strata and providing a complex canopy structure (de Toledo et al., 2012; Leveau et al., 2015). Conversely, vegetation within cities becomes simpler and sparser with few, scattered trees—mainly exotic species—and with the middle and lower vegetation strata disappearing (Chace and Walsh, 2006). Therefore, modified habitats allow the presence of an important number of bird species of different feeding guilds which take advantage of the available resources depending on the phenology and seasonality of the vegetation (Ramírez-Albores, 2004; Aycart and Díaz, 2021).

In spite of the effort to understand the effects of urbanization on birds, the information for the Tropical regions such as the Andes is still scarce (see Escobar-Ibáñez and MacGregor-Fors, 2017). This is disconcerting because the tropical Andes are the richest hotspots of bird biodiversity globally (Mittermeier et al., 2011; Bax and Francesconi, 2019). However, the major concern is that the cities in these regions are experiencing rapid expansion, disturbing their adjacent natural habitats (Cincotta et al., 2000; Luck, 2007). The Tropical Andes host more than 25% of the world’s bird species in a territory that corresponds to approximately 3% of the planet’s surface (BirdLife International and Conservation International, 2005). Despite its importance for birds, this region is one of the most threatened, mainly due to a rapid land transformation (Jetz et al., 2007), urbanization being one of the most critical pressures on biodiversity (Ramirez-Villegas et al., 2014; Zúñiga-Sarango et al., 2020). Consequently, more than 10% of the bird species in the region are seriously threatened (IUCN, 2021).

Conscious of the dramatic loss of bird diversity and of the extreme habitat degradation due to the expansion of cities in the Tropical Andes, we have conducted a study of a bird community along an urbanization gradient. The study was carried out in one middle size Andean city of Ecuador in sites ranging from the best-preserved areas (peri-urban forests) to the most disturbed areas dominated by urban development. We specifically evaluated (1) to what extent the bird diversity is negatively affected by urbanization, (2) do these negative effects differ among trophic guilds and foraging strata of birds? We hypothesized that the diversity and abundance of birds would exhibit a drastic decrease along the urbanization gradient as a consequence of the simplification of the landscape. Also, we predicted that the effects would likely differ among trophic guilds and foraging strata. For instance, granivores or birds that forage on the ground would be positively impacted rather than negatively affected by urbanization due to food subsidies from human sources, whereas insectivores would be negatively affected within cities.

We recorded a total of 1,257 individuals of 74 bird species belonging to 30 families (Supplementary Material). We found changes in the total species richness along the urbanization gradient, with a total of 54 species in forest sites, 47 in forest-pasture sites, 36 in pasture sites, and 29 in urban sites. According to rarefaction, the differences between urbanization levels were significant (95% confidence intervals did not overlap) (Figure 2). The Chao2 estimate of species richness varies from 55 to 30 species along the urbanization gradient, showing a sampling coverage greater than 90%, being highest in forest (0.98) and lowest in forest-pasture (0.90), indicating an adequate sampling effort for all urbanization levels. Most bird species recorded use the understory (44%) followed by the terrestrial stratum (36%), with no difference in the proportion of species using the aerial, canopy, and midstory strata (c.a. 7% each).

Our models showed a strong negative effect of urbanization on bird species richness (Figure 3A). Species richness was significantly higher in forest sites, followed by the forest-pasture sites, and with lower numbers of species at pastures and urban sites, respectively. Bird abundance showed a similar pattern (Figure 3B) with the number of individuals decreasing from forest to urban sites. Significantly higher abundance was detected in forest and forest-pasture sites compared to pasture and urban sites. Species evenness only showed significant differences between the forest and the urban sites, with the bird community being more even toward the most disturbed sites (Figure 3C).

The proportion of the richness of the trophic guilds was significantly affected by urbanization only in granivorous birds (Figure 4A). We found a large amount of variation in sampling sites within the same level of urbanization. Proportion of abundance was affected in three of the four trophic guilds (Figures 4A–H). Granivorous birds increased in abundance in urban sites, while insectivorous birds decreased in abundance from forest to urban sites (Figures 4A,B,E,F). The omnivores showed a reduction in abundance in the first levels of urbanization, but the abundance of this guild was higher in the urban areas (Figures 4E,F,H).

Our models showed significant effects of urbanization in proportion of richness in two foraging guilds and proportion of abundance in all foraging guilds (Figures 5A–J). The proportion of richness in the understory and terrestrial foraging guilds changed significantly along the urbanization gradient. Understory species decreased and terrestrial species increased (Figures 5D,E). Abundance of all foraging guilds was significantly affected by urbanization, although the direction of the response depended on the guild. The midstory and terrestrial guilds increased in abundance along the gradient, while aerial, canopy, and understory guilds decreased in abundance (Figures 5F–J).

We included the year of sampling in all models to test interannual changes and quantify the possible effect of temporal collinearity between samples in the same study site. In general, the sampling year did not affect the richness and abundance of birds and guilds.

Urban areas across the planet contain substantially lower species densities as compared to non-urban surroundings (Chace and Walsh, 2006; Aronson et al., 2014; Lee and Rotenberry, 2015). Species loss can exceed 75% relative to species pools in the original habitats that cities have replaced (Newbold et al., 2015). Our work also demonstrates a drastic loss of bird diversity along the urbanization gradient in a megadiverse tropical region. However, these effects are not the same for all species and can change depending on the guild they belong to. The urbanization was “good” for some guilds, such as granivorous and terrestrial species; the areas most urbanized show higher richness and/or abundance for these guilds. The urbanization was “bad” for the others guilds, with a reduction in the species richness and/or abundance. Finally, the urbanization was “ugly” for whole bird community, the richness and abundance decreasing drastically with the increase of urbanization.

According to our expectations, tropical areas should show a greater loss of diversity as a consequence of the levels of specialization that birds present in tropical ecosystems. Although comparison with other ecosystems and studies with different methods and sampling efforts have limitations, we found some indications that the magnitude of loss is greater in our ecosystem. In the studies by Mikami and Mikami (2014) in Fukuoka, Japan and by Blair (1996) in Palo Alto, California, they found a decrease in 10 of the 22 and 21 species found in forested areas, respectively. In the case of cities of similar size to Loja such as Örebro in Sweden (155,989 inhabitants), the bird community showed similar losses reaching values as high as 66% (Sandström et al., 2006). The reported changes are similar to those found in our study where 25 of the 54 species found in the forest sites are lost. Although the loss ratios of these three studies are similar, the disturbance gradient that is used in each is very different. While the studies in Fukuoka, Örebro, and Palo Alto cover fully urbanized areas, in our study the areas with the highest urbanization are not fully urbanized, thus we would expect this loss to be even stronger. On the other hand, the history of intervention and the size of the cities is very different, while Loja is a relatively new small city, Palo Alto and Fukuoka are older and larger than Loja. Other studies have found high losses of bird diversity in temperate cities. In Chile (Silva et al., 2016), where three cities were studied (Temuco, Osorno, and Valdivia) with populations between 100,000 and 300,000 inhabitants, results showed bird species loss of 40, 17, and 15%, respectively. In Argentina, bird species losses of at least 40% of the total species richness were recorded for the cities of Mar del Plata (500,000 inhabitants), Balcarce (35,000 inhabitants), and Miramar (24,000 inhabitants), when comparing natural and the urban sites (Leveau et al., 2017). Although the data presented here show some dissimilarities in the percentages of species loss between less undisturbed areas and urban areas, all the studies reviewed here are consistent in their findings. Urban environments always tend to harbor a smaller number of species than forested areas or areas with greater vegetation cover surrounding the cities.

While bird community response has been consistent across different regions, these effects are expected to be species dependent, with certain species being favored by new habitats and resources, and others being harmed by habitat-level alterations (Chace and Walsh, 2006; Walker and Shochat, 2010; Valente-Neto et al., 2021). Our results showed trophic guild-dependent responses. Granivorous bird diversity and abundance increased toward the most urbanized sites. This response is consistent with what was found in other urbanized areas (Chace and Walsh, 2006; Fox and Hockey, 2007; Blair and Johnson, 2008). The group of granivorous terrestrial-feeding birds within the city of Loja is composed mainly of generalist species (e.g., Rock Dove Columba livia, Eared Dove Zenaida auriculata, Rufous-collared Sparrow Zonotrichia capensis), which have adapted quite well to coexistence with humans. These conditions have favored an increase in the population densities of these species in the last decade, similar to what has been reported for other generalist species, like Passer domesticus and Sturnus vulgaris in cities in the United Kingdom (Evans et al., 2009), C. livia, and P. domesticus in Chile (Silva et al., 2016) or in Mexico (Escobar-Ibáñez et al., 2020).

In the case of omnivorous birds, we found an “U” shape response with a decrease in abundance in the first levels of urbanization, but another increase of abundance in more urbanized areas. These results differ from some studies that reported that abundance and species richness were lower in the least urbanized areas (Walker and Shochat, 2010; Huang et al., 2015). The shift in this pattern could be a consequence of the appearance of exotic generalist bird species, associated with the consumption of food provided directly or indirectly by humans. The omnivorous birds found in the forest sites are native species (e.g., Aulacorhynchus prasinus, Cyclarhis gujanensis), while the bird community in the urban sites is dominated by exotic species associated with humans and the resources that they provide (e.g., C. livia). This change in the trophic organization, again, is influenced by the difference in the presence of food resources and perching or nesting sites. Previous studies have already reported that urbanization favors terrestrial-feeding omnivorous and granivorous birds (Beissinger and Osborne, 1982; Lim and Sodhi, 2004). Omnivorous birds in forested areas use different strata to forage, while omnivorous birds in the city efficiently use the resources available in the urban areas, feeding in trees in the parks or on the ground.

As for insectivorous birds, our hypothesis was corroborated. In the Tropical Andes, the richness and abundance of this trophic guild decreased toward sites with higher degrees of urbanization, as reported by Amaya-Espinel et al. (2019) in Chile or by Máthé and Batáry (2015) in Romania. Many resident insectivorous birds are dependent on insect populations, both for their own food (Tallamy, 2004) and for feeding their nestlings (Dickinson, 1999). Hence the scarcity of vegetation, and particularly the scarcity of native species in urban green spaces, directly causes a decrease in insect diversity, which in turn negatively influences the diversity of birds, particularly insectivorous birds (Burghardt et al., 2009; Sherry, 2021). In our study area, Gaona et al. (2021) found a severe decrease in the diversity, abundance and species richness of moth species, which could reflect a reduction of insects because of urbanization in the city of Loja. Despite the decreases in insectivorous birds, some studies have showed an increased diversity of insectivorous birds in the most-urbanized areas (Hayes et al., 2020), for example, in Guyana (Escobar-Ibáñez and MacGregor-Fors, 2016) and various locations in Mexico (Escobar-Ibáñez et al., 2020). Leveau (2013) attributed the presence and distribution of remnants of native vegetation within or near urban areas as the main factor causing this phenomenon. Cities with the presence of native vegetation in their parks have the possibility of providing a greater amount of food resources to bird species. Many of the changes that were observed in trophic guilds can be partially explained by changes in the supply of food resources. However, further research is needed to quantify the changes in the supply of resources along the urbanization gradient and how these affect the trophic guilds.

Our results showed very clear responses to urbanization of birds using the lower strata (understory and terrestrial). As urbanization increases, the species richness and abundance of these groups changes abruptly, but in opposite directions. While urbanization favors terrestrial bird species, understory bird species show a reduction in diversity and abundance. We believe that the lack of trees within the city has a direct effect on birds that occupy the upper strata. Although we did not find significant differences in the richness of birds using the canopy and aerial strata between urbanization levels, the trend of reduction in their abundance at the most urbanized sites suggests that canopy birds and those that feed during flight are negatively affected by the urbanization process. This could be also explained by the lack of trees and food resources (e.g., insects) that have been drastically reduced in these urban sites (Gaona et al., 2021). Although the changes in resource availability in response to the structural changes of vegetation and other resources along the urbanization gradient is a plausible explanation, other authors have proposed that the restriction of nesting sites in urban areas could explain the changes in the diversity and abundance of the birds. It is necessary to carry out further studies to assess the extent to which nesting habits could be a taxonomic diversity filtering factor.

Our work shows the “ugly” side of the urbanization: a severe reduction in the diversity of birds along the urbanization gradient, which is consistent in cities with different demographic characteristics and environmental features. On the other hand, the effect of urbanization showed that the responses of the birds are species-dependent. The “bad” side of the urbanization is the reduction of richness and abundance of most guilds. Finally, for granivorous and terrestrial trophic guilds, the urbanization shows its “good” side as there is an increase of species richness and abundance. Although the answers found here are consistent with other studies, it has been observed that in certain cities the favored or affected groups may vary. It is necessary to develop a more in-depth study that allows us to understand what the factors within the urbanization process are that are causing this variation in the responses of the bird community.

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author.

Ethical review and approval was not required for the animal study because the study did not contemplate the direct manipulation of the animals, only their visual and/or auditory recording.

CI-A and LW provided the funding acquisition. CI-A, CE, and LO-D contributed to the conception and design of the study and wrote the first draft of the manuscript. LO-D and EG performed the fieldwork. CE and LO-D organized the database. CE and CI-A performed the statistical analysis. MD, AE, LW, and EG revised and edited the new versions of the manuscript. All authors contributed to manuscript revision, read, and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.