Historic checklist, core species and temporal composition turnover of birds in an urban protected natural area in central México over 50 years

Introduction

The Pedregal de San Ángel Ecological Reserve (REPSA) is a protected natural area located within the central campus of the National Autonomous University of Mexico (UNAM), in southwestern Mexico City. This area has a great richness of birds that has been documented in several research studies (Arizmendi, Espinosa & Ornelas, 1994; Chávez & Gurrola, 2007, 2009). Additionally, areas within the REPSA are frequently visited by birders participating in citizen science initiatives such as eBird and iNaturalist. However, historical information on bird richness has not been compiled or integrated, nor has it been assessed whether species composition within the reserve has changed over time. It is important to address this information gap due to the pressures on this habitat from the urbanization of Mexico City and the university campus. Urbanization processes are associated with human population growth and tend to reduce the number and quality of native vegetation patches, increase impervious surfaces and facilitate the introduction and establishment of exotic species (Hansen et al., 2005). During the last decade (2010–2020) the human population in Mexico City reached 9,209,944 inhabitants (INEGI, 2020). This population increase places greater pressure on the limits of natural areas due to the construction of urban infrastructure and demand for resources. Over time, within UNAM’s central campus, infrastructure construction has increased landscape fragmentation and reduced the number of native vegetation patches in the area (Peralta & Prado, 2009). These disturbances could impact the composition and ecological dynamics of the avifauna inhabiting the REPSA.

Species turnover is the change in the composition of a community as a result of species immigration and extinction processes (Russell et al., 1995). Migratory species have been reported to be an important component of the avifauna of Mexico City (Meléndez-Herrada, Gómez de Silva & Ortega-Álvarez, 2016). This pattern is evident in the REPSA; the latest avifauna checklist reported that 43% of the bird species present have some degree of migratory movement (Chávez & Gurrola, 2009). This flow of species during the fall and winter is generated by the convergence of Central and Eastern flyways that are interrelated in a larger migratory system (La Sorte et al., 2014). This migratory system crosses the Gulf and Central Mexico where REPSA is located. On the other hand, there are several factors associated with species extinction (e.g., habitat loss, establishment and spread of exotic species, predation). However, these factors could affect species differentially. Evaluating both processes over time is essential to understanding the dynamics and role of migratory and resident species in the richness of birds in the REPSA, it is essential to determine whether this flow of species is persistent over time—in other words, whether the same migratory and resident species have continued to be found in the REPSA year after year.

Evaluating species’ persistence over time will allow us to identify the area’s core species, i.e., species that persist over time and tend to be abundant, as opposed to transient species that occur intermittently and in low abundance (Magurran & Henderson, 2003; Coyle, Hurlbert & White, 2013). In general, the relationship between species and their permanence in an area is defined by the affinity of that species for the conditions and resources the area offers. A species that can obtain all the resources and conditions necessary for its survival in an area will tend to remain in that area over time (Magurran & Henderson, 2003).

Given the seasonal dynamics of the bird community in the REPSA and the increasing urbanization of the landscape matrix in which it is immersed, we expected the bird species composition to have changed over time. Russell et al. (1995) reported that the expected relationship between turnover and time (census interval) is non-linear and asymptotic. Species turnover at shorter time scales tend to increase, while at longer time scales turnover becomes asymptotic (Russell et al., 1995). In this study, we examine the trend of change in the dissimilarity (and its components) of the REPSA’s avifauna over 50 years. We expected that the turnover between species listings increases and reach an asymptotic trend with time (census interval). On the other hand, we expected the number of species recorded to be similar over time if there is a balance between the proportion of species that become extinct and those that reach the reserve. In addition, we estimate whether the proportion of species arriving and becoming extinct in the REPSA is influenced by time (census interval) and by the residency status of the species. Finally, we identified the core species of the REPSA based on their persistence. To explore these hypotheses, we set the following objectives: (1) generate a historical checklist of bird species recorded in the REPSA, (2) calculate Jaccard’s dissimilarity index and its components between the annual listings of species to determine if there is any trend of change over time, (3) determine the proportion of species arriving and becoming extinct from the REPSA between each pair of species listings and assess whether this is influenced by time (census interval) and the migratory status of the birds, and (4) identify core species in the reserve (persistent over time). In order to meet these objectives, we integrated the information on bird species richness reported in the REPSA over the time using three sources of information: (1) monthly monitoring of avifauna in six representative areas of the reserve, carried out from December 2013 to December 2023; (2) intensive search for species listings published in theses, scientific articles, or book chapters; and (3) information gathered through citizen science databases.

Materials and Methods

Bird monitoring

We selected eight of the 16 areas that make up the reserve and established six routes. Route 1 included the Botanical Garden, Zona Núcleo Poniente (ZNP) and zone A11; Route 2, the Espacio Escultórico (A12); Route 3, zone A13; Route 4, the Paseo de las Esculturas (A5); Route 5, the Zona Núcleo Suroriente (ZNSO), and Route 6, the Cantera Oriente (A3) (Fig. 1). We conducted 96 bird samplings from December 2013 to December 2023 in these six areas of the REPSA. These zones were selected because together they encompass the variety of resources and conditions that the reserve provides. The length of each route was determined based on the total surface and the existing trails in each zone (1 = 4.1 km; 2 = 0.82 km; 3 = 0.79 km; 4 = 0.86 km; 5 = 1 km and 6 = 2 km). We performed monthly monitoring from December 2013 to February 2020 and from August 2021 to December 2023. We alternated the zone in which each monitoring was carried out, visiting each study zone twice per year—once during the rainy season (June–October) and once during the dry season (November–May). Due to the health contingency caused by the Sars-CoV-2 virus, we suspended this monitoring between March 2020 and July 2021. All monitoring started between 7:00 and 8:00 h and finished between 11:00 and 12:00 h depending on the time of sunrise. This period was selected because it includes the hours of peak bird activity (Bibby et al., 2000). During monitoring we determined to the species level the birds we sighted or heard and recorded the number of individuals observed per species. Observations were made using 8 × 42 and 10 × 50 binoculars and the species were determined using specialized field guides (Howell & Webb, 1995; Van Perlo, 2006).

Results

As result of bird monitoring we recorded the presence of 157 bird species. As a result of the bibliographic review, we found 14 published studies, of which seven were undergraduate theses in biology, five were book chapters and two were research articles (Table 1). The time range covered by these studies was from 1973 (Ramos, 1974) to 2019 (Rodríguez, 2020). Together, these publications contributed 52 species that were not recorded by any other source of information (Table 1). In the citizen science platforms, the oldest record of avifauna in the study area was from 2005 in iNaturalist and 1967 in eBird. Together, the two databases provided 49 species that were not recorded by any other source of information (Table 1). Integrating the results obtained through our monitoring, bibliographic review and data from citizen science initiatives from 1967 to 2023 within the REPSA resulted in records of a total of 258 bird species belonging to 18 Orders and 50 families (following the taxonomy of Chesser et al., 2023, Table 2).

The best represented families were Parulidae and Tyrannidae, with 29 and 26 species respectively. Based on our data of residency within the reserve, we determined that 55 species are residents, 66 are winter migrants, six are summer migrants, 16 species are considered escapes and 115 species did not have sufficient information to determine its residency pattern within the reserve. However, the categories of residence of these species for Mexico are as follows: 68 residents, 38 winter migrants, two are summer migrants and seven are transient migrants (Berlanga et al., 2015). Considering the total number of bird records (10,882 records) obtained through our avifauna monitoring between December 2013 and December 2023, we classified 15 species as very abundant, 22 as abundant, 40 as common, 42 as rare and 139 as very rare (Table 2, Supplemental Information). The resident species with the highest number of records was the House Finch (Haemorhous mexicanus), while the migratory species with the highest number of records was the Yellow-rumped Warbler (Setophaga coronata).

The lowest Jaccard’s dissimilarity values occurred at low census intervals (1 to 5 years), while the highest dissimilarity values were reached at census intervals greater than 30 years (Fig. 2, blue dots and blue line). The species turnover shows a pattern similar to Jaccard’s dissimilarity, with the lowest turnover values occurring between low census intervals (1 to 5 years) and the highest turnover occurring at census intervals greater than 20 years (Fig. 2, pink squares and pink line). The nestedness showed similar values throughout all census intervals (Fig. 2, orange triangles and orange line).

The GLMs indicated that time and species residency status did not have significant effect on the proportion of species that become extinct in the reserve (Table 3, Fig. 3A). The proportion of species arriving in the reserve followed a similar trend and was not influenced by time or residency status of the species (Table 3, Fig. 3B).

Based on the percentage of persistence of each species in the REPSA, we detected 58 core species (i.e., species recorded in more than 66% of the lists evaluated; Fig. 4, green boxes). Among the core species, 35 were resident, 22 have some migratory movement and one exotic species (Fig. 4, Table 2). Additionally, we detected that 20 of the core species had 100% persistence in the REPSA (Table 2); that is, their presence has been recorded in every listing from the reserve from 1973 to 2023. Of these, 15 species were residents and five had some migratory movement (Table 2). We detected that 33 species had intermediate persistence (33–66% persistence over time, Fig. 4, purple boxes). Of these species, 13 are residents, 19 have some migratory movement and one exotic species. While 167 species were classified as transient since their persistence in the REPSA was less than 33%.

The cumulative records of species with 100% persistence (20 species, 6,406 records) represented 58% of the total bird records. On the other hand, the sum of the records of all core species (58 species, 9,885 records) represented 90% of the total records of avifauna in the REPSA (Supplemental Information).

Discussion

The historical checklist of avifauna reported in the REPSA comprised 258 species, reported from 1967 to 2023. In Mexico, the presence of between 1,123–1,150 bird species is reported (Navarro-Sigüenza et al., 2014), while 355 species occur in Mexico City (Meléndez-Herrada, Gómez de Silva & Ortega-Álvarez, 2016). Thus, 22% of the country’s bird species richness and 72% of the bird species reported for Mexico City have been recorded in the REPSA. The high richness of bird species that have been recorded in the REPSA can be explained by the unique environmental heterogeneity (conditions and resources) that the area presents. It has been reported that vegetation composition and structure are the main factors that determine bird species richness at macrogeographic, regional, and local scales (Cueto & López de Casenave, 1999). Areas with a complex vegetation structure and great variety of environmental conditions, as well high plant richness generates a high availability of resources, refuges and nesting sites which promotes high bird richness (Tu, Fan & Ko, 2020). Because of its volcanic origin, seven microenvironments have been described within the reserve, each of which presents different conditions in terms of humidity, soil depth, and solar incidence, which in turn have allowed the establishment of 377 plant species (Castillo-Argüero et al., 2009).

The dissimilarity between the listings of avifauna showed a tendency to increase with increasing census interval (Fig. 2). The greatest source of dissimilarity between annual listings was attributed to species turnover (Fig. 2). As expected, turnover increase with time. This increase was non-linear and asymptotic. Russell et al. (1995) postulated that the asymptotic trend in turnover will occur at census intervals between 10 and 50 years. Time range in which asymptotic turnover is reached will depend on intrinsic factors such as the probability of extinction or species arrival in the community and extrinsic factors such as habitat succession (Russell et al., 1995). Our results showed that the asymptotic trend in species turnover begins at the 20-year census interval reaching values of 0.50 (Fig. 2, pink line). Long-term research has reported bird species turnover rates similar to what we found in our study. Diamond (1969) reported that in the Channel Islands of Southern California the number of bird species remained stable over time (51 years), however species turnover varied among each island from 10 to 62 per cent. Higher species turnover was inversely correlated with total bird richness as well as with plant richness and complexity on each island (Diamond, 1969). Highly variable turnover values have been reported in different bird communities, for example in an altitudinal gradient in the Sierra Nevada of southern Spain a species turnover rate of 0.27 evaluated over a 30-year period was reported (Zamora & Barea-Azcón, 2015). However, the turnover rate was different in each vegetation type along this altitudinal gradient: high mountain pasture (0.16), Juniperus forest (0.25) and Oak forest (0.35; Zamora & Barea-Azcón, 2015). Similarly, in a Mediterranean shrubland in southwestern Spain the average annual bird species turnover rate was 0.24 over a 40-year time scale (Campo-Celada et al., 2022). It has been reported that habitats with a more stable vegetation structure over time, such as mature forests, will have a more predictable and stable bird community (Bengtsson, Baillie & Lawton, 1997). Due to succession processes, shrublands could present changes in their vegetation structure over time, increasing the variability in the composition of their bird species. However, specific long-term research is needed to evaluate changes in vegetation structure within the reserve and their effect on bird community composition.

Nestedness was the component that contributed least to the dissimilarity between bird listings. As we expected the number of species recorded was similar over time (Fig. 2, orange line). MacArthur & Wilson (1963) reported the positive relationship of number of birds and island area. Larger islands may have greater diversity of habitats that provide a greater gradient of conditions and resources for species (Lack, 1969). The reserve was decreed in 1983 with an initial extension of 124.5 hectares, over time more polygons were included until reaching the current extension of 237.3 hectares in 2005 (Peralta & Prado, 2009). However, the matrix surrounding the reserve (Ciudad Universitaria, Fig. 1, yellow line) has suffered fragmentation and habitat loss due to the development of university infrastructure over time. Despite the urbanization process, the reserve has managed to conserve the ecological heterogeneity and general conditions necessary to maintain a relatively similar number of bird species over time.

The proportion of species arriving and becoming extinct in the reserve was not influenced by time or by the species’ residency status (Table 3). This implies that the proportion of birds arriving and becoming extinct to the reserve is similar for resident and migratory species (Fig. 3). This pattern makes sense since the effect of both ecological processes would cancel out, generating little variation in the number of species reported in the reserve over time. This pattern is consistent with the nestedness values reported in this study (Fig. 2, orange line). The arrival of resident and migratory birds to the reserve can be explained by the fact that in urban environments, birds will look for habitat patches that allow them to obtain resources and have optimal conditions (Pacheco-Muñoz, Aguilar-Gómez & Schondube, 2022). Because of this, urban green areas will concentrate a greater richness of bird species than completely urbanized areas. On the other hand, complex habitats are more vulnerable to disturbances and are prone to local extinctions (Pimm, Jones & Diamond, 1988). In the reserve, different disturbances could promote the loss of the heterogeneity of the microenvironments such as habitat loss and fragmentation, the introduction and establishment of exotic species that modify the structure and composition of the vegetation, and the presence of exotic predators such as dogs and cats.

We recorded the presence of 115 species to which we could not assign a residency category in the REPSA due to their low number of records. However, 68 of these species are considered residents in Mexico while 47 have some migratory movement within the country (Berlanga et al., 2015). These species contribute to the high turnover in community composition as they perform altitudinal or latitudinal migratory movements, but do not seem to use the reserve as a stopover or non-breeding area repeatedly or persistently over time. This pattern could reflect changes in the migration flyways that bird species follow to reach their non-breeding areas. Land-use change and infrastructure development promotes habitat loss and fragmentation along flyways and could limit the quantity and quality of stopover or non-breeding areas (Kirby et al., 2008). Additionally, climate change could affect the timing of migratory movements, as well as flight duration due to changes in wind current speeds (La Sorte et al., 2014; Barton & Sandercock, 2018; Howard et al., 2018). The loss of suitable habitat could extend the duration of migratory journeys and increase the number of stopover areas that birds would need to complete their annual journey (Howard et al., 2018). The intensity of these adverse effects is associated with the distance each species migrates and the size of their non-breeding areas (Barton & Sandercock, 2018; Patchett, Finch & Cresswell, 2018). The high number of migratory species passing through the REPSA without their presence being reiterative over time could be a reflection of habitat degradation at a regional scale that forces species to modify their flyways in search of suitable areas to resupply and continue their migratory journey. However, species’ migratory dynamics in their stopover and non-breeding areas in Mexico is understudied. This highlights the need to investigate these phenomena in order to contribute to the development of conservation strategies for North American birds.

Based on their persistence over time, we categorized 58 bird species as core, 33 as intermediate, and 167 as transient (Fig. 4, Table 2). The richness of core species will be related to local-scale environmental factors such as the resources and conditions of the studied area, while the richness of transient species will be influenced by factors at larger scales such as regional spatial heterogeneity or the potential number of species that may migrate through the studied area (Magurran, 2007; Coyle, Hurlbert & White, 2013). This implies that the persistence of core species could be an indicator that the conditions and resources that enable their persistence have been successfully conserved from 1973 to the present. Being immersed within Mexico City and being part of the central campus of the UNAM, the REPSA is subject to several disturbances such as habitat loss and fragmentation due to the development of university infrastructure (buildings and parking lots), inadequate management of solid and construction waste, the establishment of exotic plant species (e.g., Leonotis nepetifolia) and the presence of exotic predators such as dogs and cats. However, we have implemented constant and permanent conservation actions to mitigate these pressures. For example, since 2015 we have carried out L. nepetifolia removal days to prevent its spread, and since 2011 we have maintained a constant monitoring program to prevent the establishment of feral dog and cat populations within the REPSA. In addition, we seek to conserve the patches of native habitat (“pedregales remanentes”) that do not belong to the reserve but are essential for the functioning and connectivity of the habitat by promoting awareness activities for the university community. The REPSA also collaborates with Mexico City government institutions to improve the management of the system of natural protected areas and areas of environmental value and thus favor connectivity and conditions for urban wildlife in Mexico City.

On the other hand, the richness of transient species with intermediate persistence (Fig. 4, blue boxes) could represent a reservoir of potential colonizing species that could facilitate the maintenance of biodiversity and ecological functions in the future in the event that local environmental changes affect the persistence of core species (Magurran & Henderson, 2003). It is essential to maintain constant and permanent biological monitoring that allows us to evaluate whether the rate of species turnover changes and if the persistence of the core species is maintained over time.

Conclusions

In summary, our research provides the most complete historical checklist of bird species reported in the REPSA by covering a temporal period of more than 50 years and integrating data generated during this period from three sources: scientific literature, citizen science, and systematic biological monitoring. Turnover increased over time to values of 0.50 and showed an asymptotic trend over the 20-year census interval. Nestedness showed similar values over time. Additionally, we determine that the birds that arrive and become extinct in the reserve have similar proportions; this cancels out its effect and promotes maintaining similar species richness values over time. Finally, based on their persistence we were able to identify core, intermediate and transient species. Our results highlight the importance of the REPSA as a fundamental area for the avifauna of Mexico City and for a great variety of migratory bird species. This research is the baseline to continue and design new conservation strategies for the birds of REPSA and the environment on which they depend for example assessing population trends of the core species or determine their habitat use within the reserve.

Supplemental Information