Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
Jaime Andrés Garizábal Carmona
Universidad Nacional de Colombia Facultad de Minas, Departamento de Geociencias y Medio Ambiente Medellín, Colombia 2020
Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
Jaime Andrés Garizábal Carmona
Thesis presented as partial requirement for the degree of: Magister en Medio Ambiente y Desarrollo
Director: Ph.D. Biól. NÉSTOR JAVIER MANCERA RODRÍGUEZ Profesor Titular, Departamento de Ciencias Forestales Universidad Nacional de Colombia, Sede Medellín
Research Line Recursos Naturales y Desarrollo Sostenible Research group Ecología y Conservación de Fauna Silvestre (COL0068199 – Categoría A1 de Colciencias).
Universidad Nacional de Colombia Facultad de Minas, Departamento de Geociencias y Medio Ambiente Medellín, Colombia 2020
Cada cosa a su debido tiempo
Acknowledgements
This thesis would not have been possible without the immeasurable help of many people. My brother (Camilo Garizábal), my parents (Fermín and Mayo), and my wife (Juliana Ardila) were essential to support me emotionally. My friends and collegues Andrés Mercado, Paula Morales, Viviana Márquez, Rómulo Agudelo, Víctor Martínez, Deysi Carmona, Tomás Hinestroza, Samuel Monsalve, Jorjany Botero and Paubla Otálvaro, helped me unconditionally in different moments of this voyage, in the field, at the desk, or in contacting me with other people that contributed directly to the research. The last included the permission to visit some plots and the use of the Herbarium of University of Antioquia (HUA), including advisory and expert validation of plant species with no monetary budgets. Indeed, I thank especially Wilson Renfijo, and the botanists Ricardo Callejas, Felipe Cardona, Álvaro Roldán, Heriberto David, Wilson D. Rodríguez and Manuel Bernal.
I also thank co-authors of “in process” manuscripts derived from this thesis: Natalia Ruíz, Laura Franco, Jefry Betancur, Sergio Montoya and Néstor Mancera. Néstor was also my thesis director and so that I thank him especially for all the extra support and motivation. I also thank Luisa Arboleda who was my field assistant, and the marvelous “Numerical Ecology” professor Kenneth Roy, and other nice people who helped me during cartographical and statistical analysis, especially Luz María Morales and Carlos Justy. Additionally, I thank the non-profit organization Corporación Merceditas and the Departament of Geoscience and Environment of National University of Colombia for monetary support. Furthemore, I really appreciate to be given the chance of teaching in the undergraduate course “Evolutionary Biology”, a happy and well-intellectually worth responsibility that taught me more than any course I have been ever took as a student. I met exceptional undergraduate students, some of whom are now my friends. Last but not least, I thank Clara Villegas for advisory during the first stages of my research, and Dubán Canal Gallego and Rubén Ortega-Álvarez for accepting the invitation to evaluate this thesis.
Resumen y Abstract IX
Abstract
In the Northern region of Tropical Andes biodiversity hotspot, urban planning is formulated without background information on ecosystems dynamics, as urbanization is transforming natural ecosystems at accelerated rates. Structural and compositional traits of urban green spaces were used as proxies of local biodiversity patterns and species-specific tolerance to urbanization in urban and peri-urban areas of the Aburrá Valley-Colombia. Bird surveys were performed from 2014 to 2019 at 222 sampling points along with land cover description using Geographic Information System tools. Also, a vegetation assessment was made at 44 of those points where local responses of bird richness were evaluated using generalized linear models. 137 resident bird species were found, plus two exotics and 27 migrants, with 32 species categorized as urban exploiters, 65 as adapters, and 33 as avoiders, based on incidence and frequency data. We found 255 plant species, with only 20% shared between trees and regeneration vegetation levels, and most native species and individuals found in unmanaged sites. According to alpha and beta-biodiversity analysis, urbanization is causing biotic homogenization and decreasing local biodiversity, despite some urban neighborhoods having similar species richness than peri-urban areas, and some local policies prompt the increasing of plant richness and habitat heterogeneity. This study suggests that promoting retention of native understory vegetation and reducing urban compactation affecting green spaces size and perimeter/area ratio, along with conservation strategies that protect forest remnants in city periphery, could mitigate the local species loss caused by urbanization in the region.
Keywords: biodiversity conservation, Northern Andes, urban biodiversity, urban green spaces, urbanization.
X Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Resumen
En el norte de los Andes Tropicales la planificación urbana se formula sin información base sobre las dinámicas ecosistémicas, mientras la urbanización transforma los ecosistemas naturales aceleradamente. Se evaluaron efectos de composición y estructura de zonas verdes urbanas sobre patrones de diversidad local y tolerancia urbana de especies en el Valle de Aburrá-Colombia. Se hicieron muestreos de aves entre 2014-2019 en 222 puntos de conteo, describiendo las coberturas del uso del suelo de la tierra con Sistemas de Información Geográfica e inventariando la vegetación en 44 de los puntos, donde la riqueza de aves fue evaluada usando modelos lineales generalizados. Se encontraron 137 especies de aves residentes, dos exóticas y 27 migratorias: 32 categorizadas como especies que explotan la ciudad, 65 como especies adaptables a la ciudad y 33 como especies que repelen la ciudad, con datos de ocurrencia (presencia) y frecuencia. Se encontraron 255 especies de plantas, con solo el 20% compartidas entre regeneración y árboles, y la mayoría de especies e individuos nativos encontrados en sitios sin manejo silvicultural. Según análisis de diversidad alfa y beta, la urbanización esta causando homogenización biótica y disminuyendo la diversidad local de aves, aunque algunos barrios tienen riquezas similares a áreas peri-urbanas, existiendo políticas locales que promueven el aumento de la riqueza de plantas y la heterogeneidad de hábitat con manejo silvicultural. Este estudio sugiere que la retención de la vegetación nativa autóctona a nivel de sotobosque, además del incremento del tamaño y la reducción de la relación perímetro/área de zonas verdes, junto con estrategias de conservación que protejan los remanentes de bosque nativos en alrededores de las zonas más desarrolladas, podrían mitigar la pérdida local de especies de aves en ciudades andinas.
Palabras clave: Andes del norte, biodiversidad urbana, conservación de biodiversidad, urbanización, zonas verdes urbanas.
Contents XI
Contents
Page
Abstract...... IX
Resumen ...... X
Symbols and abbreviations list ...... XVII
Introduction ...... 1
Structure of this Master’s Thesis ...... 4
Objetives ...... 5
Chapter 1. Bird community assemblage of a Colombian Andean city: on categorizing urban exploiters, adapters, and avoiders ...... 7 Abstract ...... 7 Introduction ...... 8 Methods ...... 9 Study area ...... 9 Birds surveys ...... 11 Distribution, trophic guilds and foraging strata ...... 11 Categorization protocol and data analysis ...... 12 Results...... 14 Altitudinal range according to urban categorization ...... 15 Trophic guilds and foraging strata according to urban categorization ...... 16 Discussion ...... 17 References ...... 20 Supplementary material ...... 29
Chapter 2. Biotic homogenization along with high local richness in a Northern Andean city ...... 37 Abstract ...... 37 Introduction ...... 38 Methods ...... 40 Study area ...... 40 Sampling point selection...... 41 Bird surveys ...... 42 Data analysis ...... 42 Results...... 43 Alfa-diversity ...... 44 XII Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Beta-diversity ...... 45 Local diversity according to land cover composition and structure ...... 46 Discussion ...... 48 References ...... 51 Supplementary material ...... 59
Chapter 3. Native tree abundance and natural regeneration increase local bird richness in a Northern Andes city ...... 69 Abstract ...... 69 Introduction ...... 70 Methods ...... 72 Study area ...... 72 Urban Green Spaces structural and land use features ...... 73 Vegetation surveys and species origin categorization ...... 73 Bird surveys ...... 74 Data exploring ...... 74 Results ...... 75 Structural and land use features of green spaces ...... 75 Vegetation composition and structure ...... 75 Bird species composition and richness ...... 77 Local bird richness according to green spaces composition and structure ...... 77 Discussion ...... 80 References ...... 83 Supplementary material ...... 91
Chapter 4. Conclusions and recommendations ...... 109 Conclusions ...... 109 Recommendations...... 111
References cited on the main Introduction ...... 113
Contents XIII
List of figures
Page
Figure 1: Study area: Metropolitan Area of the Aburrá Valley in Northwestern South America. 10 Figure 2: Linear model plot of altitudinal range vs. bird species scores. Gray full-filled bar are 95% confidence intervals. Correlation coefficient (R) computed with “Pearson” method...... 15 Figure 3: Percentage of bird species by trophic guild (O: Omnivorous, FI: Frugivorous- Insectivorous, I: Insectivorous, F: Frugivorous; “Other” includes: Granivorous, Carnivorous, Scavengers, and Nectarivorous – as specialized or combined trophic guilds), and by foraging strata (Mu: Multiple, Gr: Ground, Gr-U: Ground-Understory, Mid-Can: Midstory- Canopy; “Other” includes: Understory, Midstory, Canopy – as specialized or combined foraging strata), according to urban categorization: urban avoiders (Avoi), suburban adapters (Adap) and urban exploiters (Expl)...... 17 Figure 4: Study area: neighborhoods and reference sites delimitated across the Aburrá Valley, Northern Colombia1 ...... 40 Figure 5: Estimated Shannon diversity (A) and bird species richness (B) in seven “neighborhoods” and “two reference sites” across the Metropolitan Area of the Aburrá Valley1, 2 ...... 45 Figure 6: Heat map showing plotted with Hellinger distances and clustering patterns of similarity between seven neighborhoods and two reference sites, based on bird abundance data1 ...... 46 Figure 7: Study area and location of the 44 sampling points in western center Medellín- Colombia, Northern South America ...... 72 Figure 8: Most abundant vascular plant species with individuals ≥10cm of perimeter at 130 cm from ground (pole stage plants), and their percentage on the 44 Urban Green Spaces (UGS) evaluated. Unfilled bars are Introduced species, black-line filled bars are Regional species and gray-filled bars are Local species. Black triangles are UGS percentage of presence (%) for each species shown...... 76
Contents XIV
List of tables
Page
Table 1: Categorization criteria and scores for bird species assemblage according to occurrence and frequencies...... 13 Table 2: Sites delimitated and number of points located for evaluating local bird diversity in the Metropolitan Area of the Aburrá Valley and surroundings, Northern Colombia...... 41 Table 3: Best supported models for explaining local bird species richness and Shannon diversity (Hill numbers) across seven urban neighborhoods in the city of Medellín-Colombia, Northern Andes (excluding interactions between explanatory variables). Significant variables1 are highlightingted (p <0.05) in each model with the symbol *. Models are compared using the Akaike Information Criterion corrected for small sample sizes (n = 7): AICc and ∆AICc. Only models with ∆AICc ≤ 3.0 and AICc ≤ AICc of “model Y ~ 1” are shown...... 48 Table 4: Some vegetation features across 44 urban green spaces of Medellín-Colombia, Northern South America: richness (species), abundance (individuals), basal area (m2) and crown coverage (m2), differentiating totals and by species origin (Native as Neotropical sensu lato; Local as native within Aburrá Valley above 1000 m.a.s.l.)...... 76 Table 5: Best supported models excluding interactions between variables for explaining observed bird richness (RBRiO) across urban green spaces in the city of Medellín- Colombia, Northern South America, highlighting significant variables (p <0.05) in each model with * (A: Area, PA: perimeter/area ratio, PerGr: percentage of grass-shrubs at 200m, PerBu: percentage of building at 200m, LRAb: local regeneration abundance, and LPAb: local plant abundance). Models are compared using the Akaike Information Criterion corrected for small sample sizes (n = 44): AICc and ∆AICc...... 78 Table 6: Best supported models including interactions between variables for explaining observed bird richness (RBRiO) across urban green spaces in the city of Medellín- Colombia, Northern South America, highlighting significant variables (p <0.05) in each model with * (A: Area, PA: perimeter/area ratio, PerGr: percentage of grass-shrubs at 200m, PerBu: percentage of building at 200m, LRAb: local regeneration abundance, NRAb: native regeneration abundance, and LPAb: local plant abundance). Models are compared using the Akaike Information Criterion corrected for small sample sizes (n = 44): AICc and ∆AICc...... 79
Contents XV
List of annexes (Supplementary material)
Page
Supplement 1: Bird species list and urban tolerance categorization based upon data collected in 222 point counts, between years 2014 and 2019. Points were located in urban (n = 197) and peri-urban areas (n = 25) of Aburrá Valley, Northern Colombia. Species are arranged in descendent order according to total point frequencies (Total Freq): all frequencies (Freq) are presented in percentage (%) and when all frequencies are zero the species were only recorded in points excluded for bird categorization procedures. Category was based upon data from 141 point counts (chosen from the former 222) that were at least 200m from each other: exploiter, adapter, avoider, and data deficient (DD). Ia to IVb are scores using the categorization criteria established in Table 1...... 29 Supplement 2: Tukey’s HSD test for bird species altitudinal ranges according to urban tolerance in Aburrá Valley, Northern Colombia...... 35 Supplement 3: Regression validation plots of altitudinal range vs. bird species scores in Aburrá Valley, Northern Colombia...... 35 Supplement 4: Boxplot comparison as exploratory method to evaluate the effect of different data transformation for bird abundances (the species Zenaida auriculata was used as model, due to high frequencies, abundances and tendency of gregarious behavior)1 59 Supplement 5: Shepard diagrams to evaluate goodness of fit for bird abundance data, using Hellinger distance in seven “neighborhoods” and two “reference sites”– Cophenetic correlation is also shown for each clustering method: Single linkage (“nearest neighbor”), Complete linkage (“furthest neighbor sorting”), UPGMA (“unweighted arithmetic average clustering”) and WPGMA (“weighted arithmetic average clustering”) ...... 60 Supplement 6: Fusion level and Silhouette plots using Hellinger distance and UPGMA clustering method for bird abundance data in seven “neighborhoods” and two “reference sites” ...... 61 Supplement 7: Sample completeness curves with 95% of confidence intervals (shaded areas) for bird species diversity in the Metropolitan Area of Aburrá Valley (Antioquia- Colombia) for local bird diversity analysis1 ...... 62 Supplement 8: Bird species recorded in 91 systematic point counts located on urban and peri-urban areas of the Aburrá Valley (data from 2014 to 2019). Species are arranged in descendent order according to the total relative abundance...... 63 Supplement 9: Residuals vs Fitted values, Normal Q-Q, Scale-Location, and Residuals vs Leverage plots for the best-supported models (∆AICc ≤ 0.0) on local bird richness across XVI Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes seven neighborhoods in the Metropolitan Area of the Aburrá Valley, Colombian Northern Andes. Explanatory variables included in the best models: mean size of Grass-shrubs patches (MGrassP), maximum size of Grass-shrubs patches (MaxGrassA), and total area of Grass-shrubs patches (Grass). AICc: Akaike’s Information Criterion corrected for small sample sizes ...... 66 Supplement 10: Residuals vs Fitted values, Normal Q-Q, Scale-Location, and Residuals vs Leverage plots for the best-supported models (∆AICc ≤ 3.0) on local Shannon diversity across seven neighborhoods in the Metropolitan Area of the Aburrá Valley, Colombian Northern Andes. The only explanatory variable included in the best model was total area of Grass-shrubs patches (Grass); models with AICc ≤ AICc of the model “Shannon ~ 1” were discarded. AICc: Akaike’s Information Criterion corrected for small sample sizes...... 68 Supplement 11: Potential explanatory variables to predict local bird richness in the city of Medellín-Colombia, Northern South America...... 91 Supplement 12: Local resident bird richness (RBRiO), and selected compositional and structural features in 44 urban green spaces of Medellín-Colombia, Northern South America: area in ha (A), perimeter/area ratio (PA), percentage of grass-shrubs at 200m (PerGr), percentage of buildings at 200m (PerBu), Native Regeneration abundance (NRAb), Local Tree abundance (LPAb), and Local regeneration abundance (LRAb)...... 93 Supplement 13: Trees (Trees) and Regeneration (Rege) relative abundance and occurrence of vascular plant species in 44 urban green spaces of Medellín-Colombia, Northern South America, arranged in descendent order according to relative abundance (%) of Trees (Trees Ab); relative abundance (%) of Renegeration (Rege Ab) is also shown. Species distribution origin (Dist) is shown as Reg (Regional), Loc (Local), and Int (Introduced), and species relative occurrence (%) as the percentage of sampling points with at least one individual per species per category (Trees Occ: Trees occurrence, Rege Occ: Regeneration Occurrence). “Species” marked with * were not counted in total plant richness...... 95 Supplement 14: Resident bird species recorded across 44 urban green spaces in Medellín-Colombia, Northern South America, arranged in descendent order according to relative abundance (%). Species occurrence (% of urban green spaces) is also shown...... 105
Contents XVII
Symbols and abbreviations list
Abbreviation Term e.g. Exempli gratia (for example) m.a.s.l Meters above sea level mm/year Millimeters per year (precipitation)
WGS World Geodetic System
GIS Geographic Information System m Meters n Sampling size
SD Standard deviation min Minimum max Maximum
POT Territorial Management Plan ha Hectares
DBH Diameter at breast height
NA Do not apply
AICc Akaike´s Information Criterion, corrected for small sample sizes
∆AICc Delta (difference) of AICc, compared to best model
VIF Variance Inflation Factor
Introduction
More than fifty years after modern ecology established its theoretical foundations at the early twentieth century (Smith and Smith 2006), the progressive evidence of human impacts on earth’s ecosystems addressed new perspectives of this science (Vitousek et al. 1997, McDonnell 2011). Therefore, cities became one of the main research focus as human population showed its growing tendency and preference to congregate in such artificial environments (Davis 1955, Cohen 2003). From the early 1970s, urban ecology arose with several studies that were rapidly improving the understanding of these novel ecosystems, where both natural and social sciences are needed to enhance this integrative science and adjust paradigms of modern ecology (Pickett et al. 1997, Zipperer et al. 2000, Pickett and Cadenasso 2006, McDonnell 2011).
According to McDonnell (2011), urban ecology has two main approaches: the ecology “in” and “of” cities, and the ecology of urbanization gradients. In that way, research problems of this discipline might focus on: 1) urban ecosystems themselves (e.g. Barbosa de Toledo et al. 2012, Busse Nielsen et al. 2013, Niemeï 2014, Cordero et al. 2015, Malkinson et al. 2017, Tryjanowski et al. 2017, Southon et al. 2018); 2) rural-urban comparisons (e.g. Blair 1996, Clergeau et al. 1998, Luck and Wu 2002, Melles et al. 2003, Hamer and Parris 2011), or natural-urban comparisons based on ecological gradients (Mcdonald et al. 2008, Seto et al. 2011, Jenkins et al. 2013); and, 3) multiscale approaches (e.g. Luppi et al. 2018, Fernández-Juricic 2000, Xie et al. 2016, Jokimäki & Kaisanlahti-Jokimäki 2003, Clergeau et al. 1998). Furthermore, at the beginning of the current century, Fernández-Juricic and Jokimäki (2001), proposed the “island biogeographic” perspective, which have been widely used since urban matrices could be seen as highly fragmented landscapes, either from local or regional perspectives (Mckinney 2008, Nielsen et al. 2013, Chang and Lee 2016, Malkinson et al. 2017), although this latter perspective has some conceptual limitations in urban ecology. 2 Introduction
The emerging paradigms of urban ecology, as well as the inherited debates from social and natural sciences (McIntyre et al. 2000, McDonnell 2011), have made imperative that every research question establishes an explicit statement on which theoretical framework is based upon. Besides, since implications of findings from studying urban ecosystems often involve political issues (McIntyre et al. 2000, Wolch et al. 2014, Southon et al. 2018), is also common that study cases make clear the scopes and limitations in such a scenario. Indeed, when research is related to biodiversity in urban ecosystems, the chosen theoretical framework has tended to be linked with empirical approaches that fit on the following issues: how adjacent ecosystems are affected by cities on a regional scale (and vice versa), how management of undesirable species within cities could be improved and how local biodiversity could be maximized within cities (Sandström et al. 2006).
Moreover, in recent years perception about biodiversity in cities have ranged from the basic idea of biotic homogenization, where cities are seen as one of the major causes of biodiversity extinction on earth (McKinney 2006) and the main driver of losing local identity (Clergeau et al. 2006, Ferenc et al. 2014), to more applied perspectives where urban ecosystems are used to test basic or novel theories on modern ecology (Savard et al. 2000, Sandström et al. 2006, Kowarik 2011, Barbosa de Toledo et al. 2012) and to exploit opportunities that enhance biodiversity conservation efforts in human-related ecosystems (Miller and Hobbs 2002, Reis et al. 2012, Escobar-Ibáñez and Macgregor-Fors 2016). These emerging perspectives focused on conservation biology could be particularly relevant in tropical regions, where there are major conflicts between biodiversity conservation (“hotspots” presence) and development of modern cities, which need to be solved in the years to come.
Additionally, some authors have recently argued that conservation biology needs to study different scenarios than native ecosystems and act beyond undisturbed locations management (Miller and Hobbs 2002, Kowarik 2011). Countries with high biodiversity often have higher rates of urbanization and house holding expansion than countries without these hotspots (Liu et al. 2003), and in the case of Northwestern South America, this is happening on territories without background information on local biodiversity patterns. Thus, biological conservation, emerging landscape planning strategies and urban environmental policies in Introduction 3 this region are mainly based on speculative patterns of local diversity and landscape dynamics that could be inaccurate in time and space, with no availability information of reliable bioindicators to be monitoring over time.
In the tropical Andes of Northwestern South America, one of the regions with higher biodiversity in the world (Myers et al. 2000), detailed studies in urban ecosystems are lacking (Alberico et al. 2005, Delgado-V and Correa-H 2013, Amador-Oyola 2015, Carvajal- Castro et al. 2019). So that, there is no current evidence that global patterns of urbanization and its effects on biodiversity, mainly described from temperate regions with less biogeographical variation, are working in the same fashion in Northwestern South America, where main cities and their associated landscape impacts are usually focused on areas of endemism with high local biodiversity, especially along the Andes (Cincotta et al. 2000, Etter et al. 2008). In this region, hereafter named “Northern Andes”, knowledge on urban biodiversity distribution is partitioned and mainly focus at municipality scale, especially in some places of interest for regional conservation like local protected areas or campus universities (Marín Gómez 2005, Peña-Nuñez & Claros-Morales 2016, Arteaga 2017, Ramírez-Cháves et al. 2010, Muñoz et al. 2007, Nolazco 2013, but see Carvajal-Castro et al. 2019 as an exception). This scenario represents knowledge gaps without systematic approaches that enable to understand how biodiversity patterns have been affected by recent landscape transformation, which is extensive and almost complete in urban-related ecosystems.
The Aburrá Valley is located in Colombian Central Andes and is the place of the second largest metropolitan area in Colombia, after Bogota D.C. that is located on Eastern Andes. In this thesis, the Metropolitan Area of Aburrá Valley was used as study case, which is composed by Medellín and conurbanized surrounding municipalities. Some recent studies have revealed the importance of native forest remnants for biological conservation in municipalities like Medellín, and the role of landscape heterogeneity for understanding bird communities composition and local patterns of biodiversity (Castaño-Villa and Patiño- Zabala 2007, Gutiérrez-Vásquez and Osorio-Vélez 2014). However, these studies were performed in rural areas where most of native forest remnants in Aburrá Valley still persist, usually isolated and clustered along the valley slopes. Native forests are at different altitudes and life-zones that those areas in the basin, where the effects of urbanization 4 Introduction compacted processes on local biodiversity have not been evaluated. Indeed, beyond some efforts to describe local patterns of bird diversity in isolated protected urban areas in the valley (Vásquez-Muñoz and Castaño-Villa 2008, SAO 2014), little is known about local patterns in urban ecosystems themselves, where high-density urbanization is taking place, along with the establishment of urban green spaces of different sizes, shapes and management.
Understanding the drivers that influence community assemblages and local diversity in Andean cities using birds as bioindicators, which is a recognized, diverse and easily monitored group (Bibby et al. 1998, Sutherland et al. 2004, Villarreal et al. 2004), could be useful to improve urban environmental policies and make their impacts measurable over time in Northern Andes, where not only biogeographical patterns, but urbanization and other historical processes, are different from those cities where similar studies have been performed around the world. Therefore, this Master’s Thesis will contribute to understand the local biodiversity patterns and improve the decisions making-processses on urban green spaces management and peri-urban conservation, by providing direct evidence that facilitates monitoring and application of local policies.
Structure of this Master’s Thesis
The document consists of four chapters, including the main research’s conclusions and recommendations that are considered a chapter itself (chapter 4). The first three chapters are written following a generic “research article” structure as they will be submitted independently to peer-review journals and they are addressing particular research questions, so that, each of the three has its own “Introduction, Methods, Results, Discussion, References and Supplementary material” sections. The same format is used for all to facilitate the reading of this document, even if they will be probably submitted to different journals with their own specific “Guide for authors” (format). Indeed, in this document certain information was repeated in some chapters when previous chapters Introduction 5 already had given it, especially in “Methods” and “References”. The compiled cited references are given at the end of the document, including those cited on the main introduction, conclusions and recommendations which were not cited on any of the first three chapters.
Chapters take into consideration different spatial and temporal scales under similar research focus, where the “patch-matrix” framework of urban ecology “in” the city was followed. The first chapter represent the widest local scale and is entitled: “Bird community assemblage of a Colombian Andean city: on categorizing urban exploiters, adapters and avoiders”. It is focused on analysis of bird composition and frequency using systematic bird surveys made in Medellín, Envigado, Bello and Itagüi, from 2014 to 2019, by five local ornithologists, under the lead of the author of this Thesis (who was an observer too). The second chapter represents the intermediate local scale and is entitled: “Biotic homogenization along with high local richness in a Northern Andean city”; it is focused mainly on the municipality of Medellín, along micro-watersheds with better data availability from the former systematic bird surveys that were mentioned. Data of bird abundance and presence, as well as data from remotely sensed imagery, was used for making comparisons between seven neighborhoods. Finally, the third chapter represents the finest local scale and is entitled: “Native tree abundance and natural regeneration increase local bird richness in a Northern Andean city”. In this case, data of bird richness collected from a systematic bird surveys from January to September 2018 (by only one observer), and data on vegetation composition and structure taken during the five following months, were used for evaluating the effects that composition and structure of urban green spaces have on local patterns of bird richness.
Objetives
The main question of this thesis was: “How do local bird diversity changes in relation with composition and structure of urban green spaces in a populated city located in Northern 6 Introduction
Tropical Andes?” Therefore, the general objective of this study when the thesis proposal was approved by the Academic Committee was “to evaluate the effects that composition and structure of urban green spaces have on local patterns of bird diversity (in western center Medellín)”. Now, despite of including a wider spatial scale after proposal approval, which derived into additional chapters (chapters 1 and 2, as chapter 3 was derived from the original proposal), the main objective did not change conceptually and the former chapters were thought-out under the main research question. Additional chapters, derived from specific questions and objetives when spatial scale and the availability of data were expanded from western center Medellín to other neighborhoods and some peri-urban areas of the Aburrá Valley. Hence, this thesis had a wider scope on the research problem under a multiscale approach, taking into consideration the multiscale fashion of “biodiversity” and “urbanization”. These specific research questions and derived specific objetives (within parenthesis) were:
• Chapter 1. ¿How urbanization patterns in a city of Northern Andes are affecting local bird community assemblages? (To evaluate the bird community assemblage in urban and peri-urban areas of Aburrá Valley according to species-specific responses to urbanization)
• Chapter 2. ¿What are the patterns of local bird diversity in peri-urban and urban areas across a Northern Andean city? (To evaluate local diversity of birds in a populated Metropolitan Area of Colombian Northern Andes, comparing with a peri- urban reference, using a microwatershed or “neighborhood” spatial scale)
• Chapter 3. ¿What features of urban green spaces related to composition and structure explain the local bird richness across a Northern Andes city? (To evaluate the effects of urban green spaces composition and structure on local bird richness in a high developed urban area of western center Medellín)
Chapter 1. Bird community assemblage of a Colombian Andean city: on categorizing urban exploiters, adapters, and avoiders
Garizábal-Carmona J. A.1, 2, Betancur J. S.3, Montoya-Arango S., Franco-Espinosa L., Ruiz-Giraldo N.1 and Mancera-Rodríguez N. J.1
1. Universidad Nacional de Colombia. Department of Forestry Sciences, Research group Wildlife Ecology and Conservation. Calle 59A No. 63-20, Bloque 20, oficina 211, Medellín, Colombia; Tel.: +57-4-4309129. Fax: +57-4-4309134, [email protected] (corresponding author) 2. Corporación Merceditas 3. Grupo de investigación de ecología y evolución de vertebrados, Facultad de Ciencias Exactas y Naturales, Universidad de Antioquia, Calle 67 # 53-108. Teléfono (+57-4) 219 83 32
This article will be submitted in July 2020 to the Journal “Biological Conservation”
Abstract
Due to species-specific responses to urbanization and its effects on local community assemblages, to evaluate urbanization tolerance at species level could be useful to focalize conservation efforts. We performed bird surveys at 222 point counts in urban and peri-urban areas of a Colombian Northern Andes valley between 2014 and 2019, and based upon bird occurrence and frequency data collected at 141 of these points (≥200m from each other), we evaluated the species-specific urbanization tolerance across a multiscale gradient: urban and peri-urban, and three decreasing buffers around each point (1000, 500 and 200m), which were assigned to high (67–100% of building surface), moderate (34-66%) or low urban developed areas (0-33%) following land cover reclassification procedures. We found 166 bird species and categorized 129: 37 as urban avoiders, 55 as adapters and 37 as exploiters. Urban avoiders had narrower altitudinal ranges (1991.67 ± 558.25m) than adapters (2200.00 ± 573.66m) and exploiters (2556.15 ± 633.23m) (F-value=6.834, p-value<0.05), and along with urban adapters, they had
8 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes lower proportion of omnivorous and more proportion of specialized diet species than urban exploiters. Multiple foraging stratum was the most common (35.51%), followed by Midstory-Canopy (10.28%) and Understory-Midstory (9.35%), with no clear differences between urban categories. Bird species with exclusive Trans-Andean distribution and narrow altitudinal ranges are the most threatened by urban sprawl in Andean cities, beyond their trophic guild or foraging strata.
Keywords: Andean city, biodiversity conservation, categorization, Tropical Andes, urban wildlife.
Introduction
More than half of world human population is now living in cities as urban sprawl has increased during the last decades (Seto et al. 2011), along with its negative effects on natural ecosystems and local biodiversity (Pauchard et al. 2006, Mckinney 2008, Melo et al. 2009, Aronson et al. 2014, Ciach and Fröhlich 2016). Conservation concerns increase in mountain biodiversity hotspots due to the high proportion of endemic or near-endemic taxa with narrow distributional ranges (Myers et al. 2000, Rahbek et al. 2019), which might be neglected by conservation efforts focused on the city surroundings (Mcdonald et al. 2008, Buchanan et al. 2011).
In biodiverse countries such as Colombia, research efforts prioritize the less human- perturbed ecosystems (Miller and Hobbs 2002, Martin et al. 2012, Arbeláez-Cortés 2013, Noreña-P et al. 2018), while conservation strategies focalize the endangered species at national scale (Renjifo et al. 2020). With more people living in cities, biodiversity conservation acquires more relevance in urban ecosystems worldwide (Pickett et al. 1997, Mcdonald et al. 2009, Puppim De Oliveira et al. 2011, Aronson et al. 2017, Lepczyk et al. 2017a). Nevertheless, knowledge gaps in Northern South America regarding the urbanization effects on local biodiversity represent a conservation limitation in the region (Ortega-Álvarez and Macgregor-Fors 2011).
Chapter 1. Bird community assemblage of a Colombian Andean city: on 9 categorizing urban exploiters, adapters and avoiders
Consequences of habitat loss and fragmentation could be difficult to identify when no species in the community assemblage is endangered at national levels, because less attention is given to “least concern” species (IUCN 2020). In this regard, Blair (1996) proposed an empirical framework to identify bird species tolerance to urbanization according to their density across urbanization gradients, differentiating “urban exploiters” (high tolerance), “suburban adaptable” or “urban adapters” (intermediate tolerance), and “urban avoiders” (low tolerance), as a widely used denomination after McKinney (2002) accomplished a theoretical framework on the matter and suggested its conservation implications (Chace and Walsh 2006, Shwartz et al. 2008, Matsuba et al. 2016, Dale 2018, Callaghan et al. 2019).
Accordingly, we propose a semi-quantitative and multi-scale categorization protocol for evaluating species-specific responses to urbanization. Based on bird surveys performed across the second most populated city of Colombia, we categorized species as urban exploiters, adapters and avoiders from occurrence and frequency local patterns, and then contrasted with species-specific altitudinal ranges, trophic guilds and foraging strata. We considered a multi-scale scenario due to the multiple spatial scales influencing local biodiversity patterns and habitat use in urban ecosystems (Jokimäki and Kaisanlahti- Jokimäki 2003, Melles et al. 2003, Conole and Kirkpatrick 2011, Concepción et al. 2015, Xie et al. 2016). This categorization could be a useful tool to establish conservation priorities in Andean urban ecosystems, as new perspectives on biodiversity conservation are highlighted to identify and monitoring the most vulnerable species to urbanization.
Methods
Study area
The Metropolitan Area of the Aburrá Valley is located in the Northern central Andes of Colombia (Figure 1), between 1000 and 3000 m.a.s.l (Aristizábal and Yokota 2008), and It is shaped by ten municipalities with almost four million people (Figure 1) (6.26029 North, - 75.574139 West). We delimited the urban area (urban core) and created a 2000m buffer to 10 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes delimit peri-urban areas based on conurbanization patterns shown by Sentinel-2 satellite images taken on 20th December 2017 (USGS EROS Archive).
Urban core represented areas with more than 66% of surface occupied by buildings, roads and other human infrastructure, corresponding to “highly developed” urbanization intensity areas (MacGregor-Fors 2011). Otherwise, peri-urban areas had less than 66% of surface occupied by human infrastructure, with the other percentage occupied by lawns, exotic tree plantations, and native Andean forest remnants, corresponding to “sparsely developed” urbanization intensity areas (MacGregor-Fors 2011). We run all GIS analyses for delimitation and landscape descriptions in the QGIS free software, version 3.0.2. (Quantum-GIS-Development-Team 2018).
Figure 1: Study area: Metropolitan Area of the Aburrá Valley in Northwestern South America. Chapter 1. Bird community assemblage of a Colombian Andean city: on 11 categorizing urban exploiters, adapters and avoiders
Birds surveys
The data set we used resulted from a posteriori data compilation of independent sampling designs performed between January 2014 and June 2019, all bird point counts of 25m fixed radius that were visited during 10-min, four to ten times. To make a bird species check list, we used all data of 222 point counts that we located from 1486 to 2351 m.a.s.l. and sampled during urban connectivity assessments, local management plans, bird inventories, and personal research. All data was collected exclusively during favorable weather conditions (no rain, especially), mainly between 06:00 and 10:00 hours. Bird surveys included the twelve months across the five and a half year period, with sampling exercises at 33.50 ± 23.11 points per month (mean ± SD; min=4, max=67 points). We visited 68.46% of point counts during Nearctic-Neotropical migratory bird season (October to April), including 13 of the 25 points located in peri-urban areas.
To assess bird species categorization based on species occurrence and frequency, we only used data from 141 (64%) point counts located at least 200m from each other; points at less distance were excluded randomly to avoiding bird re-counting. We also excluded visits 6 to 10 of 44 points that were sampled within a 220-day range, so that only the first five visits within the first 90-day were taking into account in any point to avoiding temporal bias. Additionally, we excluded overflying and nocturnal species, as well as diurnal species with only one record. Total observation effort for making the check list was 11240 minutes (1124 total visits) and 6100 minutes (610 total visits) for assessing the bird species categorization.
Distribution, trophic guilds and foraging strata
We assigned altitudinal range according to Ayerbe-Quiñones (2018), endemism to Chaparro-Herrera et al. (2013), migratory status to Naranjo et al. (2012), and conservation status to Renfijo et al. (2014). We assigned diet and foraging strata categories based on Wilman et al. (2014): only one diet when some item had ≥80%, two simultaneous diets when there were two items with at least 30% each, and “Omnivorous” when there were three or more types of food and none of them had ≥80%. Similarly, we assigned a single foraging stratum when one stratum had ≥80%, two simultaneous stratum when there were two with at least 30% each, and “Multiple” when there were three or more strata present on Wilman’s database and none of them had ≥80%. 12 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
Categorization protocol and data analysis
To establish bird species categorization criteria we considered the “urban/peri-urban” spatial scale (urban vs. no urban) and three decreasing buffers around each point count: 1000m, 500m and 200m, respectively. For decreasing buffers, we calculated the percentage of building area to assign whether a point within the urban core corresponded to high (67–100%), moderate (34-66%) or low urban developed areas (0-33%), based on MacGregor-Fors (2011), and estimated the building area using Tasseled cap index and reclassification procedures (see Dymond et al. 2002, Samarawickrama et al. 2017 for example).
We considered “presence” when a species was found in at least one point of any given group and calculated species frequencies based on the proportion of points within each given group (e.g. species “X” frequency in the urban core = number of points within the urban core where species “X” was found / total number of points within the urban core). We assigned scores to bird species with the highest (10), middle (5) and lowest values (1) suggesting high, moderate and low tolerance to urbanization, respectively, according to each criteria given in Table 1. We assigned the lowest value in case of ties.
Minimum and maximum total scores possible were 8 and 80, respectively, and thus, we divided that range (72) by three to assign the final category as follows: avoider (8 to 31), adapter (32 to 56) and exploiter (57 to 80). We performed ANOVA tests (aov function) and Tukey Honest Significant Differences analysis (TukeyHSD function) for evaluating whether altitudinal ranges, trophic guilds and foraging strata explained differences in urbanization tolerance, after validating normal distribution with Shapiro tests (Shapiro.test function) using the “stats” package in R software (R Core Team 2019). Finally, we ran a simple regression linear model to test the effects of species altitudinal ranges on species tolerance to urbanization. We excluded migratory birds from altitudinal range, trophic guild and foraging strata analysis, as well as accidental species (only at one visit to point counts) and those with lower altitudinal distribution limits ≥1500 m.a.s.l.
Chapter 1. Bird community assemblage of a Colombian Andean city: on 13 categorizing urban exploiters, adapters and avoiders
Table 1: Categorization criteria and scores for bird species assemblage according to occurrence and frequencies.
Criteria Options Score Only urban core (based upon 126 point counts for residents 10 Ia. and 86 for migratory birds) I. Species Occurrence Both, urban core and peri-urban areas 5 (presence) Only peri-urban areas (based upon 15 point counts for presence 1 or residents and 9 for migratory birds) frequency UCF1 minus PUF1 fitted on the higher third of values range 10 according (min and max difference) to the Ib. UCF minus PEF fitted on the intermediate third of values urban Frequency 5 range (min and max difference) limits at points UCF minus PEF fitted on the lower third of values range 1 (min and max difference) Presence at points with ≥ 66% of building areas (based upon 13 point counts for residents and 12 for migratory 10 birds) II. Species IIa. Presence at points between 34 and 65%, and absence in presence Occurrence areas with ≥ 66% of building areas (based upon 88 point 5 or (presence) counts for residents and 62 for migratory birds) frequency Only at points with less than 33% of building areas (based according upon 40 point counts for residents and 21 for migratory 1 to building birds) percentage Highest frequencies at points with ≥ 66% of building areas 10 at 1000m IIb. Highest frequencies at points between 33 and 65% of buffer 5 Frequency building areas at points2 Highest frequencies at points with less than 33% of building 1 areas Presence at points with ≥ 66% of building areas (based upon 16 point counts for residents and 14 for migratory 10 birds) III. Species IIIa. Presence at points between 34 and 65%, and absence in presence Occurrence areas with ≥ 66% of building areas (based upon 83 point 5 or (presence) counts for residents and 54 for migratory birds) frequency Only at points with less than 33% of building areas (based according upon 42 point counts for residents and 27 for migratory 1 to building birds) percentage Highest frequencies at points with ≥ 66% of building areas 10 at 500m IIIb. Highest frequencies at points between 33 and 65% of buffer 5 Frequency building areas at points2 Highest frequencies at points with less than 33% of building 1 areas IV. IVa. Presence at points with ≥ 66% of building areas (based Species Occurrence upon 16 point counts for residents and 13 for migratory 10 presence (presence) birds) 14 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
Criteria Options Score or Presence at points between 34 and 65%, and absence in frequency areas with ≥ 66% of building areas (based upon 65 point 5 according counts for residents and 43 for migratory birds) to building Only at points with less than 33% of building areas (based percentage upon 60 point counts for residents and 39 for migratory 1 at 200m birds) buffer Highest frequencies at points with ≥ 66% of building areas 10 Highest frequencies at points between 33 and 65% of IVb. 5 Frequency building areas at points2 Highest frequencies at points with less than 33% of building 1 areas 1 UCF: urban core frequency. PUF: peri-urban frequency. 2 The lower score is suggested, in case any ties in frequencies are found.
Results
In the 222 total point counts, we made 23444 bird records of 166 species (Supplement 1): 6444 records (27.49%) in the 141 point counts used for bird species categorization (points located at least 200 m from each other and data from maximum a 90-day range). We categorized 129 bird species: 37 as urban exploiters (28.68%), 55 as urban adapters (42.64%) and 37 as urban avoiders (28.68%), with the other 37 species considered “Data Deficient” (22.29%). Final scores ranged between 8 and 80, with an average of 43.72 ± 20.70 (mean ± SD).
All except one species categorized as urban avoiders were resident (Cardellina canadensis was the only migratory species), with no endemic or near-endemic species categorized as urban exploiters. We categorized the two recorded Colombian endemic species as urban avoiders: Hypopyrrhus pyrohypogaster and Ortalis columbiana, as well as half of the eight categorized near-endemic species: Chlorostilbon melanorhynchus, Ramphocelus flammigerus, Sacurerottia saucerottei and Tangara labradorides, with the other half categorized as urban adapters and other three species considered Data Deficient. Most species categorized as urban avoiders (28 of 37: 75.68%) have an exclusive trans-Andean distribution, comparing with 14 of 55 species categorized as urban adapters (25.46%) and 2 of 37 species categorized as urban exploiters (5.40%). Chapter 1. Bird community assemblage of a Colombian Andean city: on 15 categorizing urban exploiters, adapters and avoiders
Altitudinal range according to urban categorization
Categorized resident bird species (n=107) had altitudinal ranges of 2214.02 ± 614.82 m (min=900, max= 4000 m) with significant differences between categories after sqrt- transformed altitudinal range (F-value = 6.834, p-value <0.05). The Tukey Honest Significant Differences test suggested not overlapping altitudinal ranges between urban avoiders and exploiters (adjusted p-value<0.05) that represented the tolerance extremes across the urbanization gradient (high and low tolerance, respectively), whereas we found no significant differences between urban avoiders and adapters (adjusted p-value=0.22), and between urban adapters and exploiters (Supplement 2). A simple regression linear model suggested a positive correlation between altitudinal ranges and the scores given to bird species on categorization, where lower values suggested lower urbanization tolerance (Figure 2, Supplement 3).
Figure 2: Linear model plot of altitudinal range vs. bird species scores. Correlation coefficient (R) computed with “Pearson” method.
On average, urban exploiters had altitudinal ranges of 2556.15 ± 633.23m, whereas adapters had altitudinal ranges of 2200.00 ± 573.66m and avoiders of 1991.67 ± 558.25m. Additionally, only one of the 26 urban exploiter species (3.85%) had a lower altitudinal range 16 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes different to zero, comparing to 8 of 45 adapters (17.78%) and 27 of 36 avoiders (75.00%). In other words, urban exploiters species had wider altitudinal ranges, including lowlands, with 200 m.a.s.l. being the maximum value of lower altitudinal range (on average 7.69 ± 39.23m), whereas urban adapter and avoider species had narrower altitudinal ranges and less proportion of species inhabiting lowlands (lower altitudinal ranges were on average
135.56 ± 340.56m and 694.44 ± 503.10m, respectively).
Trophic guilds and foraging strata according to urban categorization
We assigned more than half of categorized resident bird species to Insectivorous (32.71%) or Omnivorous (25.23%) trophic guilds, followed by Frugivorous-Insectivorous (14.95%); the rest of trophic guilds were represented by nine or fewer bird species (maximum 8.41% each). Proportionally, urban exploiters had more Omnivorous species, and fewer species assigned to Insectivorous or Frugivorous-Insectivorous, comparing with urban adapters and avoiders; no exploiter species was exclusively Frugivorous, whereas four species within both adapters and avoiders were assigned to this trophic guild (Figure 3).
Multiple foraging stratum was the most common (35.51%), followed by Midstory-Canopy (10.28%) and Understory-Midstory (9.35%), with the rest grouping nine or fewer species (maximum 8.41% each). Differences between categories on foraging strata percentages were less clear than trophic guilds, with urban avoiders including more species assigned to Multiple (Mu) stratum than urban adapters and exploiters, as well as more species assigned to Ground (Gr) (Figure 3). Otherwise, exploiters had less species assigned to Ground- Understory (Gr-U) than adapters and less species assigned to Midstory-Canopy (Mid-Can) than avoiders, with almost 40% of species assigned to Understory-Midstory, Understory, Midstory or Water surface trophic guilds.
Chapter 1. Bird community assemblage of a Colombian Andean city: on 17 categorizing urban exploiters, adapters and avoiders
O FI I F Other Mu Gr Gr-U Mid-Can Other
Avoi Avoi
Adap Adap
Expl Expl
0% 20% 40% 60% 80% 100% 0% 20% 40% 60% 80% 100% Percentage of species Percentage of species
Figure 3: Percentage of bird species by trophic guild (O: Omnivorous, FI: Frugivorous- Insectivorous, I: Insectivorous, F: Frugivorous; “Other” includes: Granivorous, Carnivorous, Scavengers, and Nectarivorous – as specialized or combined trophic guilds), and by foraging strata (Mu: Multiple, Gr: Ground, Gr-U: Ground-Understory, Mid-Can: Midstory- Canopy; “Other” includes: Understory, Midstory, Canopy – as specialized or combined foraging strata), according to urban categorization: urban avoiders (Avoi), suburban adapters (Adap) and urban exploiters (Expl).
Discussion
The 138 bird species that we found in the urban core of the Metropolitan Area of the Aburrá Valley (out of 166 total species recorded), is a relatively high richness compared to worldwide cities (usually under 110 species) (e.g. Mills et al. 1989, Tryjanowski et al. 2017, Callaghan et al. 2019), and most Latin American cities, including Belém-Brasil: 99 species (Lees and Moura 2017), Mexico City-Mexico: 96 species (Charre et al. 2013), Belo Horizonte-Brazil: 73 species (de Castro Pena et al. 2017), Armenia-Colombia: 75 species (Carvajal-Castro et al. 2019), among others (Leveau et al. 2017). In most Latin American studies, including ours, community assemblages have been described when urbanization had already changed the natural landscape, and then, less tolerant species to urbanization were already absent in the most developed areas. So that, Latin American cities have more bird species than other urban ecosystems worldwide, but data from a few historical studies suggest that local bird richness has decreased at higher rates across the region as urbanization sprawl (Stiles 1990, Biamonte et al. 2011, Escobar-Ibáñez and Macgregor- Fors 2016). 18 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
Regarding species composition, we found only two exotic bird species (1.20%), a low percentage similar to those reported across cities worldwide but with a lesser amount of records comparing to temperate and sub-temperate cities, where exotic species could represent more than 30% of total records (Ortega-Álvarez and MacGregor-Fors 2009, Aronson et al. 2014, de Castro Pena et al. 2017). In our study, the most common exotic species, Columba livia (Rock Dove), was only present in the 14.18% of evaluated points, especially on highly developed areas (>66% of buildings or impervious surfaces), as it had been reported across other Latin American cities (Ortega-Álvarez and Macgregor-Fors 2011, Sanz and Caula 2015, Bellocq et al. 2017). Thus, the bird community assemblage in our study area was still composed mainly by species that are Neotropical residents or Nearctic-Neotropical migrants.
However, most species we categorized as urban exploiters represent widely distributed Neotropical resident birds that without human-landscape transformation inhabits mainly below 1500 m.a.s.l. These species have been expanding geographical and altitudinal ranges and now are common in bird community assemblages of the most human-disturbed Andean landscapes, including cities as Armenia-Colombia, also located in Northern Andes (Carvajal-Castro et al. 2019), and Cali-Colombia, located in the inter-Andean Cauca river valley (Ruiz-Giraldo, Garizábal-Carmona, Vidal-Astudillo and Mancera-Rodríguez, in process). Some of these species, including Coereba flaveola, Thraupis palmarum, Pitangus sulphuratus, Tyrannus melancholicus, Columbina talpacoti and Melanerpes rubricapillus, are also common in community assemblages of Caribbean and cis-Andean (west from Andes) cities below 500 m.a.s.l. (Barbosa de Toledo et al. 2012, Avendaño et al. 2013, Elías Domínguez-López and Ortega-Álvarez 2014, Sanz and Caula 2015, de Castro Pena et al. 2017).
In contrast, most species we categorized as urban avoiders represent Neotropical birds only distributed across the Andes (trans-Andean species); they were rare during bird surveys and usually limited to peri-urban areas with less human disturbance (<33% of surface occupied by human infrastructure). Furthermore, some families such as Cotingidae, Chapter 1. Bird community assemblage of a Colombian Andean city: on 19 categorizing urban exploiters, adapters and avoiders
Furnariidae, Passerellidae, Grallaridae, Odontophoridae, and Rhynocryptidae were misrepresented in the urban and peri-urban areas we sampled, despite of being relatively common and rich families across Northern Andes (Hilty and Brown 1986, Ayerbe-Quiñones 2018), including rural landscapes of the Aburrá valley with Andean forest remnants (Castaño-Villa and Patiño-Zabala 2007, Garizábal et al. 2014). Indeed, bird community assemblages in Northern Andes cities are now dominated by widely distributed Neotropical species favored by agricultural and urban sprawl (Avendaño et al. 2013), whereas trans- Andean species are restricted to less developed areas.
Nearctic-Neotropical migratory birds are also suggested to be highly vulnerable to urban sprawl in Neotropical cities (MacGregor-Fors et al. 2010, Biamonte et al. 2011, Reis et al. 2012), but in our study, all except one Nearctic-Neotropical migratory bird species were categorized as adapters or exploiters (excluding Data Deficient species). Some Neotropical cities have also reported an unexpected high number of migratory species in urban sites (González-Oreja 2011), and even richness increments (Osorio-Olarte 2012). Nevertheless, similar to resident Neotropical species, migratory species that are now common in Andean cities could be the high or intermediate tolerant species to urbanization; thus, vulnerability of some Nearctic-Neotropical migratory species, as well as low tolerant resident Neotropical species to urbanization (categorized as Data Deficient or absent in our surveys), needs to be evaluated under experimental designs that reduce spatial and temporal bias (Biamonte et al. 2011), for example, by increasing sampling in unperturbed areas across the urbanization gradient and reducing the temporal window (ideally, collecting data during a single-year period, including migratory season).
Urban exploiters increase when rapid environmental changes occur and emerging novel resources and habitats arise (Clergeau et al. 1998, Conole and Kirkpatrick 2011, Kowarik 2011, Pape Møller et al. 2015, Ouyang et al. 2018). We found more Omnivorous species in proportion with other trophic guilds among urban exploiters as is expected for the most tolerant species to urbanization (Charre et al. 2013, Sanz and Caula 2015, Shih 2018); less flexible trophic guilds, including Insectivorous and Frugivorous, were more common in urban adapters and avoiders. Foraging strata patterns were ambiguous, probably because 20 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes body size was not used to control functional differences (Ortega-Álvarez and MacGregor- Fors 2009, Estevo et al. 2017), and we also lacked behavioral data on individual local responses. This could be a limitation because species commonly found in urban ecosystems are flexible in behavioral traits (Shochat et al. 2006) and their foraging strategies are related with other ecological traits like habitat use and human presence (McKinney 2006).
Despite some limitations in understanding proximate and ultimate drivers of bird tolerance to urbanization, our study highlights some conservation issues in Northern Andes beyond the species extinction paradigm based on IUCN criteria (IUCN 2020). Identifying and monitoring the most vulnerable species to urbanization under this novel approach could be an apprehensive strategy to mitigate the losing of beta-diversity and phylogenetic diversity that urbanization promotes (La Sorte et al. 2007, Blair and Johnson 2008, Ferenc et al. 2014, Morelli et al. 2016, Leveau et al. 2017), which is a challenging conservation issue across Northern Andes when urbanization sprawl coincides with biodiversity hotspots (Cincotta et al. 2000, Bax and Francesconi 2019). Additionally, creating conservation programs on species that could be found inside or nearby cities have the potential of involving citizens and make them more conscientious about biodiversity conservation concerns (Miller and Hobbs 2002, Soga et al. 2016): it is time to prioritize conservation in ecosystems where people and biodiversity coexist — rapidly expanding territories around the modern human world.
References
Arbeláez-Cortés, E., 2013. Knowledge of Colombian biodiversity: published and indexed. Biodivers Conserv 22, 2875–2906. https://doi.org/10.1007/s10531-013-0560-y
Aristizábal, E., Yokota, S., 2008. Evolución geomorfológica del Valle de Aburrá y sus implicaciones en la ocurrencia de movimientos en masa. Boletín Ciencias la Tierra 24, 5–18.
Aronson, M.F.J., La Sorte, F.A., Nilon, C.H., Katti, M., Goddard, M.A., Lepczyk, C.A., Warren, P.S., Williams, N.S.G., Cilliers, S., Clarkson, B., Dobbs, C., Dolan, R., Hedblom, M., Klotz, S., Kooijmans, J.L., Macgregor-fors, I., McDonnell, M.J., Mörtberg, U., Pyšek, P., Siebert, S., Sushinsky, J., Werner, P., Winter, M., 2014. A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc. R. Soc. 281, 1–8. Chapter 1. Bird community assemblage of a Colombian Andean city: on 21 categorizing urban exploiters, adapters and avoiders
https://doi.org/10.1098/rspb.2013.3330
Aronson, M.F.J., Lepczyk, C.A., Evans, K.L., Goddard, M.A., Lerman, S.B., MacIvor, J.S., Nilon, C.H., Vargo, T., 2017. Biodiversity in the city: key challenges for urban green space management. Front. Ecol. Environ. 15, 189–196. https://doi.org/10.1002/fee.1480
Avendaño, J.E., Cortés-Herrera, J.O., Briceño-Lara, E.R., Rincón-Guarín, D.A., 2013. Crossing or bypassing the Andes: a commentary on recent range extensions of cis- Andean birds to the West of the Andes of Colombia. Orinoquia 17, 207–214.
Ayerbe-Quiñones, F., 2018. Guía ilustrada de la avifauna colombiana (An illustrated field guide to the birds of Colombia). WSC, Cali, Colombia.
Barbosa de Toledo, M.C., Donatelli, R.J., Teixeira Batista, G., 2012. Relation between green spaces and bird community structure in an urban area in Southeast Brazil. Urban Ecosyst. 15, 111–131. https://doi.org/10.1007/s11252-011-0195-2
Bax, V., Francesconi, W., 2019. Conservation gaps and priorities in the Tropical Andes biodiversity hotspot: Implications for the expansion of protected areas. J. Environ. Manage. 232, 387–396. https://doi.org/10.1016/j.jenvman.2018.11.086
Bellocq, M.I., Leveau, L.M., Filloy, J., 2017. Urbanization and bird communities: spatial and temporal patterns emerging from Southern South America, in: Murgui, E., Hedblom, M. (Eds.), Ecology and Conservation of Birds in Urban Environments. Springer International Publishing, pp. 35–54. https://doi.org/10.1007/978-3-319- 43314-1
Biamonte, E., Sandoval, L., Chacón, E., Barrantes, G., 2011. Effect of urbanization on the avifauna in a tropical metropolitan area. Landsc. Ecol. 26, 183–194. https://doi.org/10.1007/s10980-010-9564-0
Blair, R.B., 1996. Land use and species diversity along an urban gradient. Ecol. Appl. 6, 506–519.
Blair, R.B., Johnson, E.M., 2008. Suburban habitats and their role for birds in the urban- rural habitat network: Points of local invasion and extinction? Landsc. Ecol. 23, 1157–1169. https://doi.org/10.1007/s10980-008-9267-y
Buchanan, G.M., Donald, P.F., Butchart, S.H.M., 2011. Identifying priority areas for conservation: A global assessment for forest-dependent birds. PLoS One 6, 1–10. https://doi.org/10.1371/journal.pone.0029080
Callaghan, C.T., Major, R.E., Cornwell, W.K., Poore, A.G.B., Wilshire, J.H., Lyons, M.B., 2019. A continental measure of urbanness predicts avian response to local urbanization. Ecography (Cop.). 42, 1–11. https://doi.org/10.1111/ecog.04863
Carvajal-Castro, J.D., María Ospina-L, A., Toro-Ló pez, Y., Pulido-G, A., Ximena Cabrera- Casas, L., Guerrero-Peláez, S., Hugo García-Merchá, V., Vargas-Salinas, F., 2019. Birds vs bricks: Patterns of species diversity in response to urbanization in a Neotropical Andean city. PLoS One 14, e0218775. 22 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
https://doi.org/10.1371/journal.pone.0218775
Castaño-Villa, G.J., Patiño-Zabala, J.C., 2007. The composition of avian communities in fragmented forest in Santa Elena region, Central Colombian Andes. Boletín Científico Mus. Hist. Nat. 11, 47–60.
Chace, J.F., Walsh, J.J., 2006. Urban effects on native avifauna: A review. Landsc. Urban Plan. 74, 46–69. https://doi.org/10.1016/j.landurbplan.2004.08.007
Chaparro-Herrera, S., Echeverry-Galvis, M.Á., Córdoba-Córdoba, S., Sua-Becerra, A., 2013. Listado actualizado de las aves endémicas y casi-endémicas de Colombia (Endemic and near-endemic birds of Colombia). Biota Colomb. 14, 235–272.
Charre, G.M., Zavala Hurtado, J.A., Néve, G., Ponce-Mendoza, A., Corcuera, P., 2013. Relationship Between Habitat Traits and Bird Diversity and Composition in Selected Urban Green Areas of Mexico City. Ornitol. Neotrop. 24, 275–293.
Ciach, M., Fröhlich, A., 2016. Habitat type, food resources, noise and light pollution explain the species composition, abundance and stability of a winter bird assemblage in an urban environment. https://doi.org/10.1007/s11252-016-0613-6
Cincotta, R.P., Wisnewski, J., Engelman, R., 2000. Human population in the biodiversity hotspots. Nature 404, 990–992. https://doi.org/10.1038/35010105
Clergeau, P., Savard, J.P.L., Mennechez, G., Falardeau, G., 1998. Bird abundance and diversity along an urban-rural gradient: a comparative study between two cities on different continents. Condor 100, 413–425.
Concepción, E.D., Moretti, M., Altermatt, F., Nobis, M.P., Obrist, M.K., 2015. Impacts of urbanisation on biodiversity: The role of species mobility, degree of specialisation and spatial scale. Oikos 124, 1571–1582. https://doi.org/10.1111/oik.02166
Conole, L.E., Kirkpatrick, J.B., 2011. Functional and spatial differentiation of urban bird assemblages at the landscape scale. Landsc. Urban Plan. 100, 11–23. https://doi.org/10.1016/j.landurbplan.2010.11.007
Dale, S., 2018. Urban bird community composition influenced by size of urban green spaces, presence of native forest, and urbanization. Urban Ecosyst. 21, 1–14. https://doi.org/10.1007/s11252-017-0706-x de Castro Pena, J.C., Martello, F., Ribeiro, M.C., Armitage, R.A., Young, R.J., Rodrigues, M., 2017. Street trees reduce the negative effects of urbanization on birds. PLoS One 12, 1–19. https://doi.org/10.1371/journal.pone.0174484
Dymond, C.C., Mladenoff, D.J., Radeloff, V.C., 2002. Phenological differences in Tasseled Cap indices improve deciduous forest classification. Remote Sens. Environ. 80, 460–472. https://doi.org/10.1016/S0034-4257(01)00324-8
Elías Domínguez-López, M., Ortega-Álvarez, R., 2014. The importance of riparian habitats for avian communities in a highly human-modified Neotropical landscape. Rev. Mex. Biodivers. 85, 1217–1227. https://doi.org/10.7550/rmb.43849 Chapter 1. Bird community assemblage of a Colombian Andean city: on 23 categorizing urban exploiters, adapters and avoiders
Escobar-Ibáñez, J.F., Macgregor-Fors, I., 2016. Peeking into the past to plan the future: Assessing bird species richness in a neotropical city. Urban Ecosyst. 19, 657–667. https://doi.org/10.1007/s11252-015-0517-x
Estevo, C.A., Nagy-Reis, M.B., Silva, W.R., 2017. Urban parks can maintain minimal resilience for Neotropical bird communities. Urban For. Urban Green. 27, 84–89. https://doi.org/10.1016/j.ufug.2017.06.013
Ferenc, M., Sedláček, O., Fuchs, R., Dinetti, M., Fraissinet, M., Storch, D., 2014. Are cities different? Patterns of species richness and beta diversity of urban bird communities and regional species assemblages in Europe. Glob. Ecol. Biogeogr. 23, 479–489. https://doi.org/10.1111/geb.12130
Garizábal, J.A., Gutiérrez-Vásquez, C.A., David, S., 2014. Diversidad de aves en cuatro localidades con bosques fragmentados en el municipio de Medellín (Bird diversity in four locations with fragmented forests in Medellín), in: Gutiérrez-Vásquez, C.A. (Ed.), Más Bosques Para Medellín: Sembrando Árboles Para La Vida. Alcaldía de Medellín, Fundación CIPAV, Medellín, pp. 164–199.
González-Oreja, J.A., 2011. Birds of different biogeographic origins respond in contrasting ways to urbanization. Biol. Conserv. 144, 234–242. https://doi.org/10.1016/j.biocon.2010.08.021
Hilty, S.L., Brown, W.L., 1986. A guide to the Birds of Colombia. Princeton University Press, Princeton, New Jersey, USA.
IUCN, 2020. IUCN Red List of Threatened Species. Versión 2020-1 [WWW Document]. URL http://www.iucnredlist.org/ (accessed 3.23.20).
Jokimäki, J., Kaisanlahti-Jokimäki, M.L., 2003. Spatial similarity of urban bird communities: a multiscale approach. J. Biogeogr. 30, 1183–1193.
Kowarik, I., 2011. Novel urban ecosystems, biodiversity, and conservation. Environ. Pollut. 159, 1974–1983. https://doi.org/10.1016/j.envpol.2011.02.022
La Sorte, F.A., McKinney, M.L., Pyšek, P., 2007. Compositional similarity among urban floras within and across continents: Biogeographical consequences of human- mediated biotic interchange. Glob. Chang. Biol. 13, 913–921. https://doi.org/10.1111/j.1365-2486.2007.01329.x
Lees, A.C., Moura, N.G., 2017. Taxonomic, phylogenetic and functional diversity of an urban Amazonian avifauna. Urban Ecosyst. 20, 1019–1025. https://doi.org/10.1007/s11252-017-0661-6
Lepczyk, C.A., Aronson, M.F.J., Evans, K.L., Goddard, M.A., Lerman, S.B., Macivor, J.S., 2017. Biodiversity in the City: Fundamental Questions for Understanding the Ecology of Urban Green Spaces for Biodiversity Conservation. Bioscience 67, 799–807. https://doi.org/10.1093/biosci/bix079
Leveau, L.M., Leveau, C.M., Villegas, M., Cursach, J.A., Suazo, C.G., 2017. Bird Communities Along Urbanization Gradients: a Comparative Analysis Among Three 24 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
Neotropical Cities. Ornitol. Neotrop. 28, 77–87.
MacGregor-Fors, I., 2011. Misconceptions or misunderstandings? On the standardization of basic terms and definitions in urban ecology. Landsc. Urban Plan. 100, 347–349. https://doi.org/10.1016/j.landurbplan.2011.01.013
MacGregor-Fors, I., Morales-Pérez, L., Schondube, J.E., 2010. Migrating to the City: Responses of Neotropical Migrant Bird Communities to Urbanization. Condor 112, 711–717. https://doi.org/10.1525/cond.2010.100062
Martin, L.J., Blossey, B., Ellis, E., 2012. Mapping where ecologists work: biases in the global distribution of terrestrial ecological observation. Front. Ecol. Environ. 10, 195– 201.
Matsuba, M., Nishijima, S., Katoh, K., 2016. Effectiveness of corridor vegetation depends on urbanization tolerance of forest birds in central Tokyo, Japan. Urban For. Urban Green. 18, 173–181. https://doi.org/10.1016/j.ufug.2016.05.011
Mcdonald, R.I., Forman, R.T.T., Kareiva, P., Neugarten, R., Salzer, D., Fisher, J., 2009. Urban effects, distance, and protected areas in an urbanizing world. Landsc. Urban Plan. 93, 63–75. https://doi.org/10.1016/j.landurbplan.2009.06.002
Mcdonald, R.I., Kareiva, P., Forman, R.T.T., 2008. The implications of current and future urbanization for global protected areas and biodiversity conservation. Biol. Conserv. 141, 1695–1703. https://doi.org/10.1016/j.biocon.2008.04.025
Mckinney, M.L., 2008. Effects of urbanization on species richness: A review of plants and animals. Urban Ecosyst. 11, 161–176. https://doi.org/10.1007/s11252-007-0045-4
McKinney, M.L., 2006. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260. https://doi.org/10.1016/j.biocon.2005.09.005
McKinney, M.L., 2002. Urbanization, biodiversity, and conservation. Bioscience 52, 883– 890.
Melles, S., Glenn, S., Martin, K., 2003. Urban Bird Diversity and Landscape Complexity: Species– environment Associations Along a Multiscale Habitat Gradient. Conserv. Ecol. 7, 5–27.
Melo, A.S., Rangel, T.F.L.V.B., Diniz-Filho, J.A.F., 2009. Environmental drivers of beta- diversity patterns in New-World birds and mammals. Ecography (Cop.). 32, 226–236. https://doi.org/10.1111/j.1600-0587.2008.05502.x
Miller, J.R., Hobbs, R.J., 2002. Conservation Where People Live and Work. Conserv. Biol. 16, 330–337.
Mills, G.S., Dunning, J.B., Bates, J.M., 1989. Effects of Urbanization on Breeding Bird Community Structure in Southwestern Desert. Condor 91, 416–428. https://doi.org/10.2307/1368320
Morelli, F., Benedetti, Y., Ibáñez-Álamo, J.D., Jokimäki, J., Mänd, R., Tryjanowski, P., Møller, A.P., 2016. Evidence of evolutionary homogenization of bird communities in Chapter 1. Bird community assemblage of a Colombian Andean city: on 25 categorizing urban exploiters, adapters and avoiders
urban environments across Europe. Glob. Ecol. Biogeogr. 25, 1284–1293. https://doi.org/10.1111/geb.12486
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, G.A.B., Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Naranjo, L.G., Amaya, J.D., Eusse-González, D.E., Cifuentes-Sarmiento, Y., 2012. Guía de las Especies Migratorias de la Biodiversidad en Colombia. Aves (A guide to migratory species of Colombian biodiversity: birds), Vol 1. ed. Ministerio de Ambiente y Desarrollo Sostenible / WWF, Bogotá.
Noreña-P, A., González Muñoz, A., Mosquera-Rendón, J., Botero, K., Cristancho, M.A., 2018. Colombia, an unknown genetic diversity in the era of Big Data. BMC Genomics 19, 61–73.
Ortega-Álvarez, R., Macgregor-Fors, I., 2011. Dusting-off the file: A review of knowledge on urban ornithology in Latin America. Landsc. Urban Plan. 101, 1–10. https://doi.org/10.1016/j.landurbplan.2010.12.020
Ortega-Álvarez, R., MacGregor-Fors, I., 2009. Living in the big city: Effects of urban land- use on bird community structure, diversity, and composition. Landsc. Urban Plan. 90, 189–195. https://doi.org/10.1016/j.landurbplan.2008.11.003
Osorio-Olarte, J., 2012. Aves migratorias neotropicales en parques y jardines de Bogotá: 1945-2005 (migratory birds in parks and gardens of Bogotá). Nodo 6, 67–82.
Ouyang, J.Q., Isaksson, C., Schmidt, C., Hutton, P., Bonier, F., Dominoni, D., 2018. A New Framework for Urban Ecology: An Integration of Proximate and Ultimate Responses to Anthropogenic Change. Integr. Comp. Biol. 58, 915–928. https://doi.org/10.1093/icb/icy110
Pape Møller, A., Díaz, M., Flensted-Jensen, E., Grim, T., Diego Ibáñez-Álamo, J., Jokimäki, J., Mänd, R., Gábor, ·, · M., Tryjanowski, P., Møller, A.P., Díaz, M., Ibáñez- Álamo, J.D., Jokimäki, J., Mänd, R., Markó, G., Tryjanowski, P., Flensted-Jensen, E., Grim, T., Ibáñez-Álamo, J.D., Jokimäki, J., Mänd, R., Markó, G., Tryjanowski, P., 2015. Urbanized birds have superior establishment success in novel environments. Oecologia 178, 943–950. https://doi.org/10.1007/s00442-015-3268-8
Pauchard, A., Aguayo, M., Peña, E., Urrutia, R., 2006. Multiple effects of urbanization on the biodiversity of developing countries: The case of a fast-growing metropolitan area (Concepción, Chile). Biol. Conserv. 127, 272–281. https://doi.org/10.1016/j.biocon.2005.05.015
Pickett, S.T.A., Burch Jr., W.R., Dalton, S.E., Foresman, T.W., Grove, J.M., Rowntree, R., Burch, W.R., Dalton, S.E., Foresman, T.W., Grove, J.M., Rowntree, R., 1997. A conceptual framework for the study of human ecosystems in urban areas. Urban Ecosyst. 1, 185–199. https://doi.org/10.1023/A:1018531712889
Puppim De Oliveira, J.A., Balaban, O., Doll, C.N.H., Moreno-Peñaranda, R., Gasparatos, A., Iossifova, D., Suwa, A., 2011. Cities and biodiversity: Perspectives and governance challenges for implementing the convention on biological diversity (CBD) 26 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
at the city level. Biol. Conserv. 144, 1302–1313. https://doi.org/10.1016/j.biocon.2010.12.007
Quantum-GIS-Development-Team, 2018. Quantum GIS Geographic Information System.
R Core Team, 2019. The R Stats Package.
Rahbek, C., Borregaard, M.K., Colwell, R.K., Dalsgaard, B., Holt, B.G., Morueta-Holme, N., Nogues-Bravo, D., Whittaker, R.H., Fjeldsa, J., 2019. Humboldt’s enigma: What causes global patterns of mountain biodiversity? Science (80-. ). 365, 1108–1113. https://doi.org/10.1126/science.aax0149
Reis, E., López-Iborra, G.M., Pinheiro, R.T., 2012. Changes in bird species richness through different levels of urbanization: Implications for biodiversity conservation and garden design in Central Brazil. Landsc. Urban Plan. 107, 31–42. https://doi.org/10.1016/j.landurbplan.2012.04.009
Renfijo, L.M., Gómez, M.F., Velásquez-Tibatá, J., Amaya-Villarreal, Á.M., Kattan, G.H., Amaya-Espinel, J.D., Burbano-Girón, J., 2014. Libro rojo de aves de Colombia, Vol I: Bosques húmedos de los Andes y la costa pacífica (Red list of Colombian birds: humid forest and pacific coast), Primera ed. ed. Editorial Pontificia Universidad Javeriana, Bogotá, D.C.
Renjifo, L.M., Amaya-Villarreal, A.M., Butchart, S.H.M., 2020. Tracking extinction risk trends and patterns in a mega-diverse country: A Red List Index for birds in Colombia. PLoS One 15, 1–19. https://doi.org/10.1371/journal.pone.0227381
Samarawickrama, U., Piyaratne, D., Ranagalage, M., 2017. Relationship between NDVI with Tasseled cap Indices : A Remote Sensing based Analysis. Int. J. Innov. Res. Technol. 3, 13–19.
Sanz, V., Caula, S., 2015. Assessing bird assemblages along an urban gradient in a Caribbean island (Margarita, Venezuela). Urban Ecosyst. 18, 729–746. https://doi.org/10.1007/s11252-014-0426-4
Seto, K.C., Fragkias, M., Gü Neralp, B., Reilly, M.K., 2011. A Meta-Analysis of Global Urban Land Expansion. PLoS One 6. https://doi.org/10.1371/
Shih, W.Y., 2018. Bird diversity of greenspaces in the densely developed city centre of Taipei. Urban Ecosyst. 21, 379–393. https://doi.org/10.1007/s11252-017-0720-z
Shochat, E., Warren, P.S., Faeth, S.H., Mcintyre, N.E., Hope, D., 2006. From patterns to emerging processes in mechanistic urban ecology. Trends Ecol. Evol. 21, 186–191. https://doi.org/10.1016/j.tree.2005.11.019
Shwartz, A., Shirley, S., Kark, S., 2008. How do habitat variability and management regime shape the spatial heterogeneity of birds within a large Mediterranean urban park? Landsc. Urban Plan. 84, 219–229. https://doi.org/10.1016/j.landurbplan.2007.08.003
Soga, M., Gaston, K.J., Koyanagi, T.F., Kurisu, K., Hanaki, K., 2016. Urban residents’ perceptions of neighbourhood nature: Does the extinction of experience matter? Biol. Chapter 1. Bird community assemblage of a Colombian Andean city: on 27 categorizing urban exploiters, adapters and avoiders
Conserv. 203, 143–150. https://doi.org/10.1016/j.biocon.2016.09.020
Stiles, F.G., 1990. La avifauna de la Universidad de Costa Rica y sus alrededores a través de veinte años (1968-1989) (Birds to the University of Costa Rica and surroundings during 20 years, 1968-1989). Rev. Biol. Trop 38, 361–381.
Tryjanowski, P., Morelli, F., Mikula, P., Krištín, A., Indykiewicz, P., Grzywaczewski, G., Kronenberg, J., Jerzak, L., 2017. Bird diversity in urban green space: A large-scale analysis of differences between parks and cemeteries in Central Europe. Urban For. Urban Green. 27, 264–271. https://doi.org/10.1016/j.ufug.2017.08.014
Wilman, H., Belmaker, J., Simpson, J., de la Rosa, C., Rivadeneira, M.M., Jetz, W., 2014. Elton Traits 1.0: Species-level foraging attributes of the world’s birds and mammals. Ecology 95, 1–14.
Xie, S., Lu, F., Cao, L., Zhou, W., Ouyang, Z., 2016. Multi-scale factors influencing the characteristics of avian communities in urban parks across Beijing during the breeding season. Sci. Rep. 6, 1–9. https://doi.org/10.1038/srep29350
Supplementary material
Supplement 1: Bird species list and urban tolerance categorization based upon data collected in 222 point counts, between years 2014 and 2019. Points were located in urban (n = 197) and peri-urban areas (n = 25) of Aburrá Valley, Northern Colombia. Species are arranged in descendent order according to total point frequencies (Total Freq): all frequencies (Freq) are presented in percentage (%) and when all frequencies are zero the species were only recorded in points excluded for bird categorization procedures. Category was based upon data from 141 point counts (chosen from the former 222) that were at least 200m from each other: exploiter, adapter,
avoider, and data deficient (DD). Ia to IVb are scores using the categorization criteria established in Table 1.
1
3
2 Altitudinal Family Species Category
range Ia Ib IIa IIb IIIa IIIb IVa Ivb
urban Freq Freq urban
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stratum
Foraging Foraging
Total Freq Total Freq
Urban Freq Freq Urban Total score
Distribution
Trophic guild Trophic Peri Thraupidae Coereba flaveola 0-2000 IN U Nt 88,7 95,2 33,3 5 10 10 10 10 10 10 10 75 Exploiter Thraupidae Thraupis episcopus 0-2600 O Mi Nt 87,9 95,2 26,7 5 10 10 10 10 10 10 10 75 Exploiter Tyrannidae Pitangus sulphuratus 0-2600 O Mu Nt 83,0 89,7 26,7 5 10 10 10 10 10 10 10 75 Exploiter Turdidae Turdus ignobilis 0-2600 O Mu Nt 81,6 88,1 26,7 5 10 10 10 10 10 10 10 75 Exploiter Troglodytidae Troglodytes aedon 0-3300 I U Nt 80,9 85,7 40,0 5 10 10 10 10 5 10 5 65 Exploiter Columbidae Zenaida auriculata 0-3500 G Mu Nt 78,7 84,9 26,7 5 10 10 10 10 10 10 10 75 Exploiter Tyrannidae Tyrannus melancholicus 0-2800 I MiCa Nt 78,0 82,5 40,0 5 10 10 10 10 5 10 10 70 Exploiter Thraupidae Thraupis palmarum 0-2600 O Mu Nt 72,3 80,2 6,7 5 10 10 10 10 10 10 10 75 Exploiter Trochilidae Amazilia tzacatl 0-1900 N Mu Nt 70,2 75,4 26,7 5 10 10 10 10 10 10 10 75 Exploiter Parulidae Setophaga petechia 0-2700 I Mi Mg 69,5 76,7 0,0 10 10 10 10 10 10 10 10 80 Exploiter Columbidae Columbina talpacoti 0-2500 G Gr Nt 68,8 73,8 26,7 5 10 10 10 10 10 10 10 75 Exploiter Picidae Melanerpes rubricapillus 0-2000 FI UMi Nt 53,2 58,7 6,7 5 10 10 10 10 10 10 10 75 Exploiter Tyrannidae Pyrocephalus rubinus 0-2700 I UMi Nt 51,8 56,3 13,3 5 10 10 10 10 10 10 10 75 Exploiter Tyrannidae Contopus virens 0-3000 I Mu Mg 50,5 54,7 11,1 5 10 10 10 10 5 10 10 70 Exploiter Hirundinidae Pygochelidon cyanoleuca 0-3000 I Mi Nt 44,7 45,2 40,0 5 5 10 5 10 5 10 5 55 Adapter Trochilidae Anthracothorax nigricollis 0-2000 N Mu Nt 39,7 44,4 0,0 10 10 10 10 10 5 10 10 75 Exploiter Tyrannidae Elaenia flavogaster 0-2300 FI Mu Nt 39,0 39,7 33,3 5 5 10 5 10 5 10 1 51 Adapter Thraupidae Sicalis flaveola 0-2600 G GrU Nt 39,0 42,9 6,7 5 10 10 10 10 10 10 10 75 Exploiter Psittacidae Brotogeris jugularis 0-1500 O MiCa Nt 34,8 38,9 0,0 10 10 10 10 10 10 10 10 80 Exploiter
30 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
1
3
2 Altitudinal Family Species Ia Ib IIa IIb IIIa IIIb IVa Ivb Category
range
urban Freq Freq urban
-
stratum
Foraging Foraging
Total Freq Total Freq
Urban Freq Freq Urban Total score
Distribution
Trophic guild Trophic Peri Accipitridae Rupornis magnirostris 0-2700 IC Mu Nt 34,8 34,1 40,0 5 5 10 10 10 10 10 5 65 Exploiter Tyrannidae Todirostrum cinereum 0-2200 I Mu Nt 34,0 34,9 26,7 5 5 10 10 10 5 10 1 56 Adapter Thraupidae Saltator striatipectus 0-2500 I Mu Nt 32,6 34,1 20,0 5 5 10 1 10 1 10 1 43 Adapter Cathartidae Coragyps atratus 0-4000 S Gr Nt 31,9 32,5 26,7 5 5 10 5 10 10 10 10 65 Exploiter Fringillidae Euphonia laniirostris 0-2000 F MiCa Nt 31,9 34,1 13,3 5 5 10 1 10 1 10 1 43 Adapter Cardinalidae Piranga rubra 0-3200 I Mu Mg 31,6 32,6 22,2 5 5 10 10 10 10 10 10 70 Exploiter Tyrannidae Myiozetetes cayanensis 0-2200 FI Mu Nt 31,2 33,3 13,3 5 5 10 1 10 1 5 1 38 Adapter Thraupidae Stilpnia vitriolina 300-2500 FI Mu Ne* 29,1 27,8 40,0 5 1 10 5 10 5 10 1 47 Adapter Tyrannidae Empidonax virescens 0-2800 I Mu Mg 28,4 31,4 0,0 10 5 10 10 10 10 10 10 75 Exploiter Vireonidae Vireo olivaceus 0-3400 O Ca Mg 28,4 31,4 0,0 10 5 10 10 10 10 10 10 75 Exploiter Threskiornithidae Phimosus infuscatus 0-3000 I W Nt 28,4 31,7 0,0 10 5 10 5 10 10 10 5 65 Exploiter Psittacidae Forpus conspicillatus 0-2600 O GrU Ne 26,2 26,2 26,7 5 5 10 5 10 1 10 1 47 Adapter Thraupidae Saltator coerulescens 0-1300 I UMi Nt 25,5 26,2 20,0 5 5 10 5 10 5 10 5 55 Adapter Parulidae Setophaga castanea 0-1500 O Mi Mg 23,2 25,6 0,0 10 5 10 10 10 10 10 5 70 Exploiter Turdidae Catharus ustulatus 0-3000 FI GrU Mg 22,1 20,9 33,3 5 1 10 1 10 1 10 1 39 Adapter Parulidae Leiothlypis peregrina 0-2700 O Mu Mg 22,1 24,4 0,0 10 5 10 5 10 5 10 5 60 Exploiter Thraupidae Tiaris olivaceus 700-2400 G Gr Nt 22,0 16,7 66,7 5 1 5 1 5 1 5 1 24 Avoider Thamnophilidae Thamnophilus multistriatus 0-2000 I Mu Ne* 21,3 20,6 26,7 5 5 10 5 10 5 10 1 51 Adapter Tyrannidae Myiodynastes maculatus 0-1600 O Mi Nt 19,9 21,4 6,7 5 5 10 10 10 10 10 5 65 Exploiter Picidae Picumnus olivaceus 0-1800 I UMi Nt* 19,9 22,2 0,0 10 5 10 10 10 5 10 1 61 Exploiter Parulidae Parkesia noveboracensis 0-2000 I Gr Mg 18,9 20,9 0,0 10 5 10 1 10 5 5 1 47 Adapter Parulidae Geothlypis philadelphia 0-3000 I GrU Mg 17,9 18,6 11,1 5 5 10 5 10 1 10 1 47 Adapter Parulidae Setophaga fusca 600-3500 I Mu Mg 17,9 15,1 44,4 5 1 10 1 10 1 10 1 39 Adapter Fringillidae Spinus psaltria 500-3100 O Mu Nt* 16,3 15,1 26,7 5 1 5 1 10 1 10 1 34 Adapter Icteridae Molothrus bonariensis 0-2600 IG Gr Nt 15,6 16,7 6,7 5 5 5 5 10 10 10 1 51 Adapter Ardeidae Bubulcus ibis 0-3500 O GrW Ex 14,9 15,9 6,7 5 5 5 5 10 5 10 10 55 Adapter Falconidae Milvago chimachima 0-2700 O Gr Nt 14,9 15,9 6,7 5 5 10 10 10 5 10 5 60 Exploiter Tyrannidae Sayornis nigricans 200-2800 I U Nt* 14,9 15,9 0,0 10 5 10 10 10 5 10 5 65 Exploiter Thraupidae Sporophila nigricollis 0-2200 G GrU Nt 14,9 15,1 13,3 5 5 10 5 5 5 10 1 46 Adapter Cardinalidae Piranga olivacea 0-3200 I Mu Mg 14,7 16,3 0,0 10 5 10 10 10 10 10 10 75 Exploiter Columbidae Columba livia 0-3500 O Gr Ex 14,2 15,9 0,0 10 5 10 10 10 10 10 10 75 Exploiter Cracidae Ortalis columbiana 300-2000 F MiCa E* 14,2 10,3 46,7 5 1 10 1 5 1 5 1 29 Avoider Trochilidae Saucerottia saucerottei 0-2100 N Mu Ne* 14,2 15,1 6,7 5 5 5 1 5 1 5 1 28 Avoider Chapter 1. Bird community assemblage of a Colombian Andean city: on 31 categorizing urban exploiters, adapters and avoiders
1
3
2 Altitudinal Family Species Ia Ib IIa IIb IIIa IIIb IVa Ivb Category
range
urban Freq Freq urban
-
stratum
Foraging Foraging
Total Freq Total Freq
Urban Freq Freq Urban Total score
Distribution
Trophic guild Trophic Peri Tyrannidae Empidonax traillii 0-1300 I U Mg 13,7 15,1 0,0 10 5 10 10 5 5 10 5 60 Exploiter Thraupidae Stilpnia cyanicollis 700-2200 F Mi Nt* 13,5 13,5 13,3 5 5 5 1 10 1 10 1 38 Adapter Furnariidae Synallaxis albescens 0-2000 I GrU Nt 13,5 12,7 20,0 5 5 10 5 5 1 5 1 37 Adapter Momotidae Momotus aequatorialis 1300-3000 I Mu Nt* 12,1 8,7 40,0 5 1 5 1 5 1 5 1 24 Avoider Picidae Colaptes punctigula 0-1800 I UMi Nt 11,3 11,9 6,7 5 5 10 5 5 5 5 1 41 Adapter Psittacidae Amazona ochrocephala 0-1500 O Mu Nt 10,6 11,9 0,0 10 5 10 10 10 5 10 10 70 Exploiter Trochilidae Chlorostilbon melanorhynchus 600-2200 N Mu Ne* 10,6 9,5 20,0 5 1 5 1 5 1 5 1 24 Avoider Tyrannidae Zimmerius chrysops 500-2500 FI Ca Nt* 9,2 9,5 6,7 5 5 5 1 5 1 1 1 24 Avoider Parulidae Cardellina canadensis 0-3000 I Mi Mg 8,4 7,0 22,2 5 1 5 1 5 1 5 1 24 Avoider Parulidae Mniotilta varia 0-2700 I Mu Mg 8,4 5,8 33,3 5 1 5 1 10 1 10 1 34 Adapter Passerellidae Arremon brunneinucha 800-2600 O Mu Nt* 7,8 4,8 33,3 5 1 5 1 5 1 5 1 24 Avoider Thraupidae Stilpnia heinei 1400-2300 F Mu Nt* 7,8 4,8 33,3 5 1 5 1 5 1 5 1 24 Avoider Charadriidae Vanellus chilensis 0-3300 I Gr Nt 7,8 7,9 6,7 5 5 5 1 10 5 10 10 51 Adapter Parulidae Setophaga ruticilla 0-3000 I Mi Mg 7,4 8,1 0,0 10 5 5 1 5 1 5 1 33 Adapter Psittacidae Amazona amazonica 0-1500 F Mu Nt 7,1 7,9 0,0 10 5 5 5 5 5 10 10 55 Adapter Parulidae Basileuterus rufifrons 0-1800 I U Nt* 7,1 6,3 13,3 5 5 5 5 10 5 5 5 45 Adapter Cuculidae Crotophaga ani 0-3000 O Mu Nt 7,1 6,3 13,3 5 5 5 5 5 5 5 1 36 Adapter Psittacidae Eupsittula pertinax 0-2600 O UMi Nt 6,4 6,3 6,7 5 5 10 10 10 5 10 5 60 Exploiter Passerellidae Zonotrichia capensis 0-3600 O Gr Nt 6,4 2,4 40,0 5 1 5 1 5 1 1 1 20 Avoider Tyrannidae Camptostoma obsoletum 0-1900 FI Mi Nt 5,7 5,6 6,7 5 5 5 5 5 5 5 1 36 Adapter Picidae Melanerpes formicivorus 1400-2700 O MiCa Nt* 5,7 6,3 0,0 10 5 5 1 5 1 5 1 33 Adapter Parulidae Myioborus miniatus 600-2700 I Mi Nt* 5,7 2,4 33,3 5 1 1 1 1 1 1 1 12 Avoider Tyrannidae Myiophobus fasciatus 0-2000 I U Nt* 5,7 4,8 13,3 5 1 5 5 5 1 5 1 28 Avoider Thraupidae Sporophila minuta 0-2300 G GrU Nt 5,7 4,8 13,3 5 1 10 10 5 1 5 1 38 Adapter Troglodytidae Pheugopedius mystacalis 1300-2500 I Mu Ne* 5,0 14,3 6,7 5 5 5 5 5 1 5 1 32 Adapter Cracidae Chamaepetes goudotii 800-3300 F MiCa Nt* 4,3 2,4 20,0 5 1 1 1 5 1 5 1 20 Avoider Tyrannidae Myiarchus cephalotes 1500-2700 IG UMi Nt* 4,3 1,6 26,7 ------DD Accipitridae Buteo platypterus 0-3500 C Gr Mg 4,2 3,5 11,1 5 5 5 5 5 5 10 10 50 Adapter Icteridae Icterus galbula 0-2000 O Mu Mg 4,2 4,7 0,0 10 5 5 5 5 5 5 1 41 Adapter Tyrannidae Myiarchus crinitus 0-2700 FI Gr Mg 4,2 4,7 0,0 10 5 5 5 10 10 10 10 65 Exploiter Tyrannidae Tyrannus tyrannus 0-3200 I U Mg 4,2 4,7 0,0 10 5 10 10 5 5 10 10 65 Exploiter Passerellidae Atlapetes albinucha 1400-2500 O Gr Nt* 3,5 0,0 33,3 1 1 5 1 1 1 1 1 12 Avoider Troglodytidae Henicorhina leucophrys 1200-3000 I GrU Nt* 3,5 0,0 33,3 1 1 1 1 5 1 5 1 16 Avoider 32 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
1
3
2 Altitudinal Family Species Ia Ib IIa IIb IIIa IIIb IVa Ivb Category
range
urban Freq Freq urban
-
stratum
Foraging Foraging
Total Freq Total Freq
Urban Freq Freq Urban Total score
Distribution
Trophic guild Trophic Peri Tyrannidae Myiodynastes chrysocephalus 1000-3000 FI Mu Nt* 3,5 2,4 13,3 5 1 1 1 1 1 1 1 12 Avoider Furnariidae Synallaxis azarae 1300-3200 I UMi Nt* 3,5 1,6 20,0 5 1 5 1 5 5 5 1 28 Avoider Thraupidae Tangara labradorides 1400-2600 FI Mu Ne* 3,5 2,4 13,3 5 1 1 1 1 1 1 1 12 Avoider Turdidae Turdus fuscater 1700-4000 FI Gr Nt* 3,5 0,0 33,3 ------DD Scolopacidae Tringa solitaria 0-3500 I GrW Mg 3,2 3,5 0,0 ------DD Cathartidae Cathartes aura 0-2600 S Gr Nt 2,8 2,4 6,7 5 5 5 5 5 1 5 1 32 Adapter Turdidae Catharus aurantiirostris 600-2300 O Gr Nt* 2,8 3,2 0,0 10 5 5 1 5 1 1 1 29 Avoider Fringillidae Euphonia cyanocephala 600-3000 F Mu Nt* 2,8 3,2 0,0 10 5 10 10 5 1 5 1 47 Adapter Falconidae Falco sparverius 0-3000 IC Mu Nt 2,8 3,2 0,0 10 5 10 10 5 5 10 10 65 Exploiter Tyrannidae Leptopogon superciliaris 500-2000 I Mi Nt* 2,8 2,4 6,7 5 5 1 1 5 1 5 1 24 Avoider Tyrannidae Machetornis rixosa 0-3200 I Gr Nt 2,8 2,4 6,7 5 5 5 1 10 10 10 10 56 Adapter Tyrannidae Phaeomyias murina 0-1800 FI Mu Nt 2,8 2,4 6,7 5 5 10 10 5 5 5 1 46 Adapter Thraupidae Ramphocelus flammigerus 0-2200 FI Mu Ne* 2,8 2,4 6,7 5 5 5 1 1 1 1 1 20 Avoider Tyrannidae Serpophaga cinerea 1000-3300 I GrU Nt* 2,8 3,2 0,0 10 5 5 5 5 5 5 5 45 Adapter Hirundinidae Stelgidopteryx ruficollis 0-2600 I UMi Nt 2,8 0,8 20,0 5 1 5 1 5 1 1 1 20 Avoider Thraupidae Anisognathus somptuosus 1300-2800 O Mu Nt* 2,1 0,0 20,0 1 1 1 1 1 1 1 1 8 Avoider Passerellidae Chlorospingus flavopectus 1200-3100 I Mu Nt* 2,1 0,0 20,0 1 1 1 1 1 1 1 1 8 Avoider Picidae Dryocopus lineatus 0-2300 I Mu Nt 2,1 2,4 0,0 10 5 5 5 5 5 5 5 45 Adapter Icteridae Hypopyrrhus pyrohypogaster 1000-2800 O MiCa E* 2,1 0,0 20,0 1 1 1 1 5 1 1 1 12 Avoider Tyrannidae Legatus leucophaius 0-1800 FI Ca Nt 2,1 2,4 0,0 10 5 5 5 5 5 5 5 45 Adapter Columbidae Leptotila verreauxi 0-2800 O Gr Nt 2,1 1,6 6,7 5 5 5 1 5 1 1 1 24 Avoider Icteridae Molothrus oryzivorus 0-2600 O Mu Nt 2,1 1,6 6,7 5 5 10 10 5 5 5 1 46 Adapter Thraupidae Volatinia jacarina 0-2300 O Gr Nt 2,1 2,4 0,0 10 5 5 1 5 5 1 1 33 Adapter Cuculidae Coccyzus americanus 0-3500 O MiCa Mg 2,1 2,3 0,0 10 5 5 1 5 1 10 10 47 Adapter Tyrannidae Contopus cooperi 0-3200 I UMi Mg 2,1 2,3 0,0 10 5 5 5 5 5 1 1 37 Adapter Psittacidae Ara ararauna 0-1500 O MiCa Nt 1,4 1,6 0,0 10 5 5 1 10 10 5 1 47 Adapter Psittacidae Ara macao 0-1500 O MiCa Nt 1,4 1,6 0,0 10 5 1 1 1 1 1 1 21 Avoider Thraupidae Asemospiza obscura 0-1700 G GrU Nt* 1,4 1,6 0,0 10 5 5 1 5 1 5 1 33 Adapter Picidae Colaptes rubiginosus 900-3000 I Mu Nt 1,4 0,8 6,7 5 5 1 1 1 1 1 1 16 Avoider Trochilidae Colibri cyanotus 600-3200 N Mu Nt* 1,4 0,0 13,3 1 1 1 1 1 1 1 1 8 Avoider Tyrannidae Contopus cinereus 300-1500 I UMi Nt* 1,4 1,6 0,0 10 5 5 5 5 5 5 1 41 Adapter Ardeidae Egretta thula 0-3000 IC GrW Nt 1,4 1,6 0,0 ------DD Chapter 1. Bird community assemblage of a Colombian Andean city: on 33 categorizing urban exploiters, adapters and avoiders
1
3
2 Altitudinal Family Species Ia Ib IIa IIb IIIa IIIb IVa Ivb Category
range
urban Freq Freq urban
-
stratum
Foraging Foraging
Total Freq Total Freq
Urban Freq Freq Urban Total score
Distribution
Trophic guild Trophic Peri Tyrannidae Elaenia chiriquensis 0-2000 FI UMi Nt 1,4 1,6 0,0 10 5 5 5 5 1 1 1 33 Adapter Tyrannidae Elaenia frantzii 1000-3000 FI Mi Nt* 1,4 0,0 13,3 1 1 1 1 1 1 1 1 8 Avoider Rallidae Laterallus albigularis 0-2000 O Gr Nt* 1,4 0,8 6,7 5 5 5 5 5 5 5 1 36 Adapter Mimidae Mimus gilvus 0-2800 I GrU Nt 1,4 1,6 0,0 10 5 5 5 5 5 5 5 45 Adapter Turdidae Myadestes ralloides 600-3000 FI MiCa Nt* 1,4 0,0 13,3 1 1 1 1 1 1 1 1 8 Avoider Parulidae Myiothlypis coronata 1400-3200 I UMi Nt* 1,4 0,0 13,3 ------DD Thraupidae Sporophila schistacea 0-2200 G Gr Nt* 1,4 1,6 0,0 10 5 10 10 5 1 5 1 47 Adapter Cuculidae Tapera naevia 0-3000 I Mu Nt 1,4 0,0 13,3 1 1 5 5 5 5 5 5 32 Adapter Tyrannidae Tyrannulus elatus 0-1700 FI Ca Nt 1,4 0,0 13,3 1 1 5 5 5 5 5 5 32 Adapter Vireonidae Vireo leucophrys 1000-2800 I Mu Nt* 1,4 0,0 13,3 1 1 1 1 1 1 1 1 8 Avoider Falconidae Falco columbarius 0-3500 C Mu Mg 1,1 1,2 0,0 ------DD Cardinalidae Pheucticus ludovicianus 0-3400 O Mu Mg 1,1 1,2 0,0 ------DD Parulidae Protonotaria citrea 0-1800 O Mi Mg 1,1 1,2 0,0 ------DD Psittacidae Amazona autumnalis 0-1200 F Mu Nt 0,7 0,8 0,0 ------DD Psittacidae Ara severus 0-1100 O MiCa Nt 0,7 0,8 0,0 ------DD Parulidae Basileuterus tristriatus 500-2600 I U Nt* 0,7 0,0 6,7 1 5 1 1 1 1 1 1 12 Avoider Ardeidae Butorides striata 0-3000 PI W Nt 0,7 0,8 0,0 ------DD Trochilidae Chaetocercus mulsant 1500-3300 N Mu Nt* 0,7 0,8 0,0 ------DD Trochilidae Coeligena coeligena 1400-2600 N Mu Nt* 0,7 0,8 0,0 ------DD Cuculidae Crotophaga major 0-2600 O Mu Nt 0,7 0,8 0,0 ------DD Corvidae Cyanocorax affinis 0-2400 O Mu Ne 0,7 0,8 0,0 ------DD Vireonidae Cyclarhis nigrirostris 1500-2700 I MiCa Ne* 0,7 0,0 6,7 ------DD Accipitridae Elanus leucurus 0-3500 C Gr Nt 0,7 0,8 0,0 10 5 5 5 1 1 1 1 29 Avoider Thraupidae Emberizoides herbicola 0-1800 O GrU Nt 0,7 0,0 6,7 ------DD Trochilidae Haplophaedia aureliae 1500-2500 N Mu Nt* 0,7 0,0 6,7 ------DD Tyrannidae Myiozetetes similis 0-1300 O Mu Nt 0,7 0,8 0,0 ------DD Ardeidae Nycticorax nycticorax 0-3200 IC GrW Nt 0,7 0,8 0,0 ------DD Tyrannidae Phyllomyias griseiceps 0-1800 FI Mi Nt* 0,7 0,8 0,0 10 5 5 5 5 5 1 1 37 Adapter Cuculidae Piaya cayana 0-3000 I Ca Nt 0,7 0,8 0,0 10 5 5 5 5 5 1 1 37 Adapter Cotingidae Pipreola riefferii 1400-3200 F UMi Nt* 0,7 0,0 6,7 1 5 1 1 5 5 5 5 28 Avoider Tyrannidae Pyrrhomyias cinnamomeus 1500-3200 I U Nt* 0,7 0,0 6,7 ------DD Icteridae Quiscalus lugubris 0-3000 IG Gr Nt 0,7 0,8 0,0 ------DD Thraupidae Saltator atripennis 600-2300 O Ca Ne* 0,7 0,0 6,7 ------DD 34 Effects of urban green spaces composition and structure on local bird diversity: A study case in Colombian Northern Andes
1
3
2 Altitudinal Family Species Ia Ib IIa IIb IIIa IIIb IVa Ivb Category
range
urban Freq Freq urban
-
stratum
Foraging Foraging
Total Freq Total Freq
Urban Freq Freq Urban Total score
Distribution
Trophic guild Trophic Peri Fringillidae Spinus xanthogastrus 1200-3000 G MiCa Nt* 0,7 0,8 0,0 ------DD Thraupidae Sporophila intermedia 0-2300 G Gr Nt 0,7 0,8 0,0 10 5 1 1 1 1 1 1 21 Avoider Thraupidae Tangara arthus 1200-2500 FI Mu Nt* 0,7 0,0 6,7 ------DD Thraupidae Tangara gyrola 0-2200 FI Mu Nt 0,7 0,0 6,7 ------DD Thraupidae Tangara nigroviridis 1100-3000 I Mu Nt* 0,7 0,0 6,7 1 5 1 1 1 1 1 1 12 Avoider Tyrannidae Tolmomyias sulphurescens 0-1600 I UMi Nt 0,7 0,8 0,0 ------DD Rallidae Anurolimnas viridis 0-1200 IG Gr Nt 0,0 0,0 0,0 ------DD Accipitridae Buteo brachyurus 0-3000 C Ca Nt 0,0 0,0 0,0 ------DD Odontophoridae Colinus cristatus 0-2600 G Gr Nt 0,0 0,0 0,0 ------DD Grallariidae Grallaria ruficapilla 1200-3200 I Gr Nt* 0,0 0,0 0,0 ------DD Tyrannidae Myiarchus tuberculifer 0-1800 I Mu Nt 0,0 0,0 0,0 ------DD Cardinalidae Piranga flava 1400-2300 I Mu Nt* 0,0 0,0 0,0 ------DD Thraupidae Schistochlamys melanopis 0-1800 FI Mu Nt 0,0 0,0 0,0 ------DD Thraupidae Sporophila funerea 0-1700 G GrU Nt 0,0 0,0 0,0 ------DD Trochilidae Uranomitra franciae 1000-2100 N Mi Nt* 0,0 0,0 0,0 ------DD Vireonidae Vireo flavifrons 0-2800 FI Mu Mg 0,0 0,0 0,0 ------DD 1 Trophic level: C (Carnivore), F (Frugivore), G (Granivore), I (Insectivore), N (Nectarivore), O (Omnivore), P (Piscivorous), S (Scavenger). 2 Foraging strata: Ca (Canopy), Gr (Ground), Mi (Mid-high), Mu (Multiple), U (Understory), W (Water surface). 3 Distribution: E (Endemic), Ex (Exotic), Mg (Nearctic-Neotropical Migratory) Nt (Neotropical), Ne (Near endemic). *Trans- Andean distribution: only Andes (distribution west from Amazonas and Orinoco rivers basin, excluding Caribbean lowlands).
Supplement 2: Tukey’s HSD test for bird species altitudinal ranges according to urban tolerance in Aburrá Valley, Northern Colombia.
Supplement 3: Regression validation plots of altitudinal range vs. bird species scores in Aburrá Valley, Northern Colombia.
Chapter 2. Biotic homogenization along with high local richness in a Northern Andean city
Garizábal-Carmona J. A.1, 2, Betancur J. S.3, Montoya-Arango S., Franco-Espinosa L., Ruiz-Giraldo N.1 and Mancera-Rodríguez N. J.1
1. Universidad Nacional de Colombia. Department of Forestry Sciences, Research group Wildlife Ecology and Conservation. Calle 59A No. 63-20, Bloque 20, oficina 211, Medellín, Colombia; Tel.: +57-4-4309129. Fax: +57-4-4309134, [email protected] (corresponding author) 2. Corporación Merceditas 3. Grupo de investigación de ecología y evolución de vertebrados, Facultad de Ciencias Exactas y Naturales, Universidad de Antioquia, Calle 67 # 53-108. Teléfono (+57-4) 219 83 32
This article will be submitted in May-June 2020 to the Journal “Perspectives in Ecology and Conservation”, and its main findings were already presented in the XXIII Mesoamerican Conservation Biology Congress as an oral presentation (October 2019, Antigua, Guatemala)
Abstract
Biodiversity is a concept intending to describe the multidimensional nature of biological entities. Evaluating the scale effect on local biodiversity could elucidate conservation issues in urban ecosystems, where multiscale habitat transformation occurs. We compared seven urban neighborhoods against two reference sites in a Colombian Northern Andes city: a peri-urban native forest remnant and an urban protected park. Based on bird surveys data collected in 91 fixed radio sampling points from September 2014 to June 2019, we found 114 diurnal resident bird species: 92 species were confirmed in urban neighborhoods or the urban protected park, whereas 21 species were only found at the peri-urban reference. The peri-urban site had the highest local diversity according to Shannon diversity (Hill numbers), whereas its species richness was similar to a couple of urban sites. Cluster analysis showed a separation of the peri-urban reference from all the urban sites (including the urban protected park), as local biodiversity patterns across the urban sites were not
38 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes well-explained by land cover composition at micro-watershed scale. Our findings suggest that several scales of biodiversity descriptors and area delimitation are needed for a better understanding of biodiversity in Andean cities and to design urban planning strategies that prevent the loss of native biodiversity.
Keywords: urbanization, biotic homogenization, Tropical Andes, urban biodiversity, Neotropical birds.
Introduction
Biodiversity represents a multidimensional concept where scales are interdependent on each other (Bennie et al. 2011), following the hierarchical nature of biological entities, from genes and species to ecosystems (Barbault 1995, Savard et al. 2000). The concept biodiversity is usually simplified to “species loss” (Kowarik 2011, Aronson et al. 2014, Sol et al. 2014, Mcgill et al. 2015), which under public media and political popularization results in the misunderstanding of the original concept, obnubilating its functional relevance (Walker 1992), and its direct application on sustainability strategies in human-dominated ecosystems (Vitousek et al. 1997, Larondelle and Haase 2013).
Conceptual complexity and methodological bias complicate the measurability and monitoring of biodiversity (Diefenbach et al. 2003, Chace and Walsh 2006, Ouyang et al. 2018), so simple measurements such as species richness are the most common in urban ecosystems (Nielsen et al. 2013, Matthies et al. 2017, Gutiérrez-Tapia et al. 2018), as they could be easier to understand by policymakers (Palliwoda et al. 2017, Southon et al. 2018). However, focusing exclusively on species richness is not always operational (Barbault 1995, Botzat et al. 2016), and the deficiency of other biodiversity measurements could eclipse other conservation issues and weaken environmental policies.
In some biodiversity hotspots such as the Tropical Andes, urban sprawl is occurring at higher rates than the global average (Cincotta et al. 2000, Cohen 2003) without detailed background information on local biodiversity patterns (MacGregor-Fors and Ortega-Álvarez Effects of urban green space size, structure and vegetation on local bird 39 richness: a study case in Colombian Northern Andes
2013, Mejía 2016). Thus, the high endemism and species turnover in Northern Andes (Myers et al. 2000), along with high density urbanization processes (CAF 2017), implies a high risk of biotic homogenization driven by landscape transformation (McKinney 2006, Olden and Rooney 2006) as natural habitats across cities and surroundings are rapidly lost and fragmented (Pauchard et al. 2006, Andrade et al. 2013, Quintero et al. 2017).
Biodiversity monitoring could be an overwhelming task that can be mitigated by focusing on certain groups. Birds are highly conspicuous and well-known bioindicators in a wide range of environmental conditions (Becker 2003), and it is possible to gather bird data with observational methods that are simple to implement and replicate (Bibby et al. 1998, Sutherland et al. 2004). Unsurprisingly, birds have been one of the most studied groups in urban ecosystems (Marzluff et al. 2001, Chace and Walsh 2006, Nielsen et al. 2013, Lepczyk et al. 2017b), but this advantage has been overlooked in some regions such as Northern Andes (Ortega-Álvarez and Macgregor-Fors 2011, Delgado-V and Correa-H 2013, MacGregor-Fors and Ortega-Álvarez 2013), constraining biological conservation strategies in this biodiversity hotspot.
Hence, we aimed to evaluate local bird diversity patterns across a Metropolitan Area of Colombian Northern Andes by estimating two alpha-diversity descriptors —species richness and Shannon diversity (Hill numbers)— and assessing cluster analysis of beta- diversity. We tested whether the micro-watershed scale manifested local diversity patterns regarding land cover composition and structure (percentage of trees, grass-shrubs, and buildings), under the hypothesis that sites within most developed areas would have lower diversity than sites within less developed areas. We also expected that sites within most developed areas, despite the percentage of urban green areas they had, would be more resembling to each other in biodiversity than any of them with peri-urban areas, which would be suggesting biotic homogenization across Northern Andes due to urbanization densification and sprawl. 40 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Methods
Study area
The Metropolitan Area of the Aburrá Valley is located in the Northern central Andes of Colombia (Figure 4) (6.26029 North, -75.574139 West), between 1000 and 3000 m.a.s.l (Aristizábal and Yokota 2008), and it is shaped by ten municipalities with almost four million inhabitants. The basin of the Aburrá Valley has been completely transformed by urbanization and silvicultural management (Molina-Franco 2015), so that natural vegetation only remains along the Valley’s slopes above 1800 m.a.s.l.
Figure 4: Study area: neighborhoods and reference sites delimitated across the Aburrá Valley, Northern Colombia1
1PER: peri-urban reference site, WCI: western center “Iguaná”, FSW: far south west, FSE: far south east, URB: urban reference site, MSE: middle south east, CSE: close south east, MSW: middle south west, WCH: western center “Hueso” Effects of urban green space size, structure and vegetation on local bird 41 richness: a study case in Colombian Northern Andes
We subdivided the Metropolitan Area according to micro-watershed delimitation by the Management and Ordering Plan of the Aburrá Valley Watershed (Universidad Nacional de Colombia 2005), which is the environmental planning tool at the Metropolitan level. We excluded the peripheral section of each micro-watershed with sparcely developed areas (0- 33% built cover) (MacGregor-Fors 2011), and the resulting polygons were considered urban neighborhoods (Figure 4), joining adjacent micro-watersheds when they both had less than 200ha.
Sampling point selection
A shapefile with 222 bird point counts that we sampled between 2014 and 2019 was intercepted with the urban neighborhoods, using the QGIS software (Quantum-GIS- Development-Team 2018). We used a total of seven neighborhoods with 11-point counts each as comparative units (Figure 4, Table 2), with point counts at least 200m apart from each other. We also included two reference sites, each one with seven-point counts: a peri- urban area with native forests remnants in Southeastern Medellín, and a regional urban protected park under human-managed green spaces in downtown Bello (Piamonte Protected Urban Area). All point counts were located between 1486 and 2351 m.a.s.l.
Table 2: Sites delimitated and number of points located for evaluating local bird diversity in the Metropolitan Area of the Aburrá Valley and surroundings, Northern Colombia. Micro- Count Area Municipality Site Abbreviation watershed points (ha) Middle south Medellín Altavista MSW 11 793,76 west Medellín-Envigado La Ayurá Far south east FSE 11 822,06 Western center Medellín La Hueso WCH 11 1082,24 (Hueso) Western center Medellín La Iguaná WCI 11 537,24 (Iguana) Medellín-Itagüí La Jabalcona Far south west FSW 11 651,12 Close south Medellín La Presidenta CSE 11 525,07 east La Volcana + Middle south Medellín MSE 11 299,32 La Aguacatala east Medellín NA Urban Reserve URB1 7 NA 42 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Micro- Count Area Municipality Site Abbreviation watershed points (ha) Peri-urban Bello NA PER1 7 NA forest 1 Reference sites: only for cluster analysis and local diversity comparisons, not for associations with landscape features
Bird surveys
We followed bird surveys protocols proposed by Bibby et al. (1998) and Sutherland et al. (2004). From September 2014 to June 2019, we recorded every bird seen or heard during 10-minute periods at 25m-fixed radius point counts, between 06:00 and 10:00 hours, excluding nocturnal, overflying birds and migratory Nearctic-Neotropical birds. A single observer visited each point four times within three month periods (n = 87), reaching a total effort of 3640 minutes (60.67 hours). Bird surveys included the twelve months along with the five-and-a-half-year period and data was compiled for overall analysis.
Data analysis
We considered each point a sampling replicate and the maximum of individuals per species the independent record for statistical analysis, with 50 individuals being the maximum value for mono-specific bird flocks. We plotted sample completeness curves based on the number of individuals detected (abundance), with 95% confidence intervals, and calculated two Hill numbers for each site: species richness and Shannon diversity, using the package “iNEXT” in the program R (Hsieh et al. 2016, R Core Team 2019), avoiding sampling and abundance problems (Chao et al. 2014), as well as other conceptual and interpretation issues of alfa- diversity indexes (Barrantes and Sandoval 2009).
We calculated the asymmetrical Hellinger distance using the decostand and vegdist functions of the Community Ecology Package vegan in R version 2.5-5 (Oksanen et al. 2019, R Core Team 2019). Hellinger distance avoids double zero issues, and therefore, it is a highly recommended distance for analysis based on abundance data (Legendre and Legendre 2012) (Supplement 4). Then, we plotted hierarchical clusters with the hclust function of the R Package stats (R Core Team 2019), using complete linkage, single linkage, UPGMA, WPGMA, and Ward methods. We evaluated clusters based on Effects of urban green space size, structure and vegetation on local bird 43 richness: a study case in Colombian Northern Andes cophenetic correlation, Shepard-like diagrams, Silhouette width, and Fusion levels (Borcard et al. 2011) (Supplement 5, Supplement 6), and we selected the most supported cluster for drawing a heat map using the pheatmap function of the Pheatmap package version 1.0.12 (Kolde 2019).
To evaluate local bird diversity patterns in the study area, we considered species richness and Shannon diversity index as independent response variables. As explanatory variables, we considered some land use characteristics based on the Tasseled cap vegetation Index (Samarawickrama et al. 2017), using Sentinel-2 satellite images taken on 20 December 2017 (USGS Archive). We delimited grass-shrubs, trees, and built areas with 10m of accuracy across the seven neighborhoods using the Build Virtual Raster tool in QGIS (version 2.18.25) and the SCP tool for atmospheric correction, following a semi-automatic land cover classification. We estimated patch mean size, patch maximum size and total area for each land cover type (nine explanatory variables overall).
We ran the glmulti function of the “Model Selection and Multimodel Inference Made Easy” package (Calcagno and de Mazancourt 2010), based on generalized linear models (GLM) (version 1.0.7.1.) to find the best models using the Akaike’s Information Criterion corrected for small sample sizes (AICc), taking into account models with ∆AICc ≤ 3.0 against the best model and including only marginal models (with k ≤ 9). We fitted all variables under the formulas “Richness ~.” and “Shannon ~.”, independently, following the Poisson distribution and restricted the model selection to main effects (without variable interactions), due to high autocorrelation between explanatory variables, which was tested running the function chart.Correlation of the package “PerformanceAnalytics” (Peterson et al. 2019).
Results
Total sample coverage was above 0.95, with all the urban sites getting values above 0.96 and the peri-urban reference site (PER) getting a lower value but still representative: 0.91, (Supplement 7). We found 114 diurnal resident bird species, with only two non-Neotropical native species (Supplement 8): Columba livia and Bubulcus ibis. We confirmed 92 species 44 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes within urban neighborhoods (80.70%), with one species only recorded at the urban reference (URB): Contopus cinereus, and 21 species only recorded at the peri-urban reference (PER) (18.42%), four of which have lower altitudinal ranges above 1500 m.a.s.l: Cyclarhis nigrirostris, Haplophaedia aureliae, Pyrrhomyias cinnamomeus and Turdus fuscater.
About 70% of the 5723 bird records corresponded to only 20 species, with greater number of records in the urban neighborhoods and the protected urban parked used as an urban reference site. The most common species were the exotic C. livia (7.83% of records), and some Neotropical birds with wide distributional ranges: Pygochelidon cyanoleuca (6.88%), Thraupis episcopus (6.37%), Zenaida auriculata (5.88%), and Columbina talpacoti (4.71%). By contrast, most of the bird species had less than 1% of total records, with 17 species with lower altitudinal ranges below 1500m only found at the peri-urban reference site.
Alfa-diversity
Total bird richness was estimated at 122.03 ± 5.46 resident species (mean ± SD) (116.40 min, 140.90 max, 95% of confidence). Estimated values of local diversity suggested that the peri-urban reference site had bird assemblages with more common species (Shannon diversity: 57.77 ± 3.30 species), comparing with any urban site (max = 43.35 ± 1.72 species, WCI), including the seven neighborhoods evaluated and the urban protected park used as a reference site (Figure 5, A); indeed, after counting species in proportion to their abundances, the peri-urban reference site showed the highest local bird diversity. In contrast, richness values suggested that the peri-urban site had similar diversity (71.99 ± 5.46) to one of the closest neighborhoods to downtown Medellín, WCI: 72.06 ± 7.99, and lower values than a neighborhood located in southeastern Medellín at the city periphery, MSE: 81.57 ± 14.34 (Figure 5, B).
Effects of urban green space size, structure and vegetation on local bird 45 richness: a study case in Colombian Northern Andes
70 140 60 120
50 100
40 80
30 60 20
Shannon diversity diversity Shannon 40 Species richness Species 10 20
0
PER WCI FSW FSE URB MSE CSE MSW WCH
Total 0
Total PER WCI FSW FSE URB MSE CSE MSW WCH
A B Figure 5: Estimated Shannon diversity (A) and bird species richness (B) in seven “neighborhoods” and “two reference sites” across the Metropolitan Area of the Aburrá Valley1, 2
1Sites arranged in descending order of Shannon diversity values, also for species richness. Bars are ± SD 2 PER: peri-urban reference site, WCI: western center “Iguaná”, FSW: far south west, FSE: far south east, URB: urban reference site, MSE: middle south east, CSE: close south east, MSW: middle south west, WCH: western center “Hueso”
Beta-diversity
The Hellinger distance matrix showed that the seven neighborhoods and the urban protected park shared more bird species composition and abundance patterns than any of these sites with the peri-urban reference (Figure 6). The heat map and cluster analysis of beta-diversity suggested that all urban sites were indistinguishable to one each other, especially sites located on highly developed areas (67–100% of built cover). Hellinger distances were above 0.95 between any urban site (the seven neighborhoods and the urban protected park) and the peri-urban reference (PER), with CSE being the closest (0.9661) and WCH the farthest (1.1819), and the latter representing the highest distance (√2, c.a. 1.4142, is the upper limit of Hellinger distances). On the other hand, urban sites had 0.5871 ± 0.1033 of distance between them (max = 0.7886), with WCI-FSW and FSW- MSW having the lowest values: 0.4317 and 0.4449, respectively.
46 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Figure 6: Heat map showing plotted with Hellinger distances and clustering patterns of similarity between seven neighborhoods and two reference sites, based on bird abundance data1
1 PER: peri-urban reference site, WCI: western center “Iguaná”, FSW: far south west, FSE: far south east, URB: urban reference site, MSE: middle south east, CSE: close south east, MSW: middle south west, WCH: western center “Hueso”
Local diversity according to land cover composition and structure
Species richness and Shannon diversity local patterns across the seven neighborhoods were unclear regarding land cover variation at the micro-watershed spatial scale. The two best supported models for species richness had relatively high beta R2 and included statistically significant variables associated with grass-shrubs cover features: mean size of patches (MGrassP), max size of patches (MaxGrassA), and total area (Grass) (Table 3). Nevertheless, besides a small sample size (n = 7), the low parameter coefficients (≤ 4.44 x 10-2), uneven residuals distribution, and statistically significant leverage effects suggest they are ambiguous and weak models for predicting local bird diversity (Supplement 9). Similarly, the two best models for Shannon diversity included the model “Shannon ~ 1” that implies no significant effects of any explanatory variable (Table 3); the other best model: Shannon ~ 1 + Grass, had relatively low beta R2, with no significant effects of the only Effects of urban green space size, structure and vegetation on local bird 47 richness: a study case in Colombian Northern Andes explanatory variable (Grass: p > 0.05), besides relatively low parameter coefficients (≤ 0.22), uneven residuals distribution, and also, statistically significant leverage effects (
48 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Supplement 10).
Table 3: Best supported models for explaining local bird species richness and Shannon diversity (Hill numbers) across seven urban neighborhoods in the city of Medellín-Colombia, Northern Andes (excluding interactions between explanatory variables). Significant variables1 are highlightingted (p <0.05) in each model with the symbol *. Models are compared using the Akaike Information Criterion corrected for small sample sizes (n = 7): AICc and ∆AICc. Only models with ∆AICc ≤ 3.0 and AICc ≤ AICc of “model Y ~ 1” are shown. Species richness Residual Model Formula AICc ∆AICc R2 Deviance Richness ~ 1 + MGrassP* + MaxGrassA* 4.13 51.18 0 0.80 Richness ~ 1 + Grass* + MaxGrassA* 5.36 52.41 1.23 0.75 Shannon diversity Shannon ~ 1 + Grass 5.66 46.48 0.00 0.45 Shannon ~ 1 9.32 48.14 1.66 - 1 Explanatory variables included in the best models: MGrassP (Mean size of grass-shrub cover patches), MaxGrassA (Maximum size of grass-shrub cover patches), Grass (Total area of grass-shrub cover).
Discussion
We found evidence of biotic homogenization in the Aburrá Valley of Colombian Northern Andes, as bird community assemblages highly resembled each other across urban sites yet all differentiated from the peri-urban reference. Urban sites had a fewer number of common species within community assemblages while most records corresponded to expanding range species favored by agricultural and urban sprawl (Avendaño et al. 2013). Cluster analysis and Shannon diversity (Hill numbers) showed decreasing of local bird diversity across urban sites, whereas species richness blurred the biotic homogenization in some neighborhoods, which is challenging because species richness is usually the main indicator of urban conservation efforts and monitoring (Pickett et al. 2011, Aronson et al. 2017). Additionally, territorial planning in urbanized landscapes such as the Aburrá Valley focuses on watershed management, acting on landscape rather than local scales Effects of urban green space size, structure and vegetation on local bird 49 richness: a study case in Colombian Northern Andes
(Universidad Nacional de Colombia 2005), which could be reducing the capacity of detecting conservation issues.
Regarding species richness, which adjusted as Hill numbers (order q = 0) considers species independently to their abundances (Hsieh et al. 2016), an urban neighborhood had the highest value, overcoming the periurban reference site. We found the highest species richness in a residential area by some of the busiest streets of the city (“The Golden Mile”), where no public urban parks or private green areas >50 ha were present. In contrast, we found the second highest bird richness in a micro-watershed where the National University of Colombia has one of its city campuses, by the >100 ha “Cerro El Volador” hill, both sites considered important bird areas for urban conservation (Vásquez-Muñoz and Castaño-Villa 2008). In these cases, local bird richness were high as a consequence of having a high proportion of intermediate tolerant bird species to urbanization, as other studies have shown (Blair 1996, Marzluff 2005). These “urban adapters”, “suburban adapters”, or “utilizers” (McKinney 2002, Fischer et al. 2015), are the richest and most abundant bird group across urban ecosystems (McKinney 2006, Shwartz et al. 2008, Kowarik 2011, Andersson and Colding 2014); therefore, species richness without differenciating bird species composition or relative abundances could be ambiguous to evaluating local patterns in and around cities.
Regarding Shannon diversity, the peri-urban reference site had the highest value; Shannon diversity adjusted as Hill numbers (order q = 1) counts species in proportion to their abundances (Hsieh et al. 2016); this measurement might reflect local diversity patterns that are masked by species richness (Stiles 1990, Clergeau et al. 1998, 2006; Biamonte et al. 2011). In fact, although species richness suggested that two urban neighborhoods had higher local diversities, Shannon diversity showed that any urban neighborhood had lower local diversitiy than the peri-urban reference site. The differences shown by alpha-diversity measurements and the inclusion of beta-diversity analysis acquire relevance in high biodiverse Andean ranges (Myers et al. 2000, Rahbek et al. 2019), especially when biotic homogenization is reported across several Neotropical cities (Leveau et al. 2015). 50 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Most abundant species are usually ecologically generalist birds commonly reported in urban bird assemblages (La Sorte et al. 2018), whose presence in cities could be a nuisance for more specialized birds (Sax and Gaines 2003, Faeth et al. 2005, Conole and Kirkpatrick 2011). A study in fragmented forests of Andean Ecuador between 1400-2600 m.a.s.l. demonstrated that certain species are forest-obligated (Becker et al. 2008), and similarly, studies in fragmented landscapes in the Aburrá Valley have suggested it (Castaño-Villa and Patiño-Zabala 2007, Garizábal et al. 2014). Hence, the topographical complexity within Andean valleys needs to be considered in more detail, because there could be unknown proxies of urbanization tolerance and city colonization regarding the species altitudinal ranges, species interaction, and species-specific habitat use. For example, we only found Turdus fuscater in the peri-urban reference site of the Aburrá Valley, whereas T. ignobilis was one of the most abundant species in the urban sites; in other Andean cities such as Bogota-Colombia (approx. 2600m) and Quito-Ecuador (approx. 2800m), T. fuscater it is a common bird species in highly developed areas, whereas T. ignobilis is rare or absent (Asociación Bogotana de Ornitología 2000, Travez and Yánez 2017).
When bird richness is the main alpha-diversity measurement and only landscape scales are evaluated, several studies have failed to find differences in bird community assemblages across urbanized landscapes (Andersson and Colding 2014, Ferenc et al. 2014, Morelli et al. 2016, Malkinson et al. 2017). It has been suggested that urban species richness is a matter of scale (Niemelä 1999), as more local approaches have shown significant differences in species richness (White et al. 2005, Evans et al. 2009, Shwartz et al. 2013, Strohbach et al. 2013, Chong et al. 2014, Beninde et al. 2015). Hence, it could be helpful that urban planning includes multiscale approaches (Savard et al. 2000, Jokimäki and Kaisanlahti-Jokimäki 2003, Melles et al. 2003), as evaluating only local or landscape scales might difficult the understanding of urbanization effects on biodiversity, besides the statistical limitation of small sample sizes and spatial bias represented by only taking into account the landscape scale.
Effects of urban green space size, structure and vegetation on local bird 51 richness: a study case in Colombian Northern Andes
In conclusion, combining spatial scales along with beta-diversity analysis and alpha- diversity measurements that not only consider species richness could help to detect urbanization effects, especially when losing local identity by local extinction of small range fauna is one of the main conservation issues in human-transformed landscapes (Melo et al. 2009, Ferenc et al. 2014, La Sorte et al. 2018, Müller et al. 2018). Accordingly, although species richness could be an indicator of better urban green spaces management (Threlfall et al. 2017), biotic homogenization is still a conservation issue that needs to be considered, because some bird populations are isolated and fragmented without being noticed. In other words, recognition of urbanization as “the most homogenizing of all major human activities” (McKinney 2006) is critical: We need to develop policies to protect endemic, less abundant and most vulnerable species, rather than only enhancing local richness across cities.
References
Andersson, E., Colding, J., 2014. Understanding how built urban form influences biodiversity. Urban For. Urban Green. 13, 221–226. https://doi.org/10.1016/j.ufug.2013.11.002
Andrade, G.I., Remolina, F., Wiesner, D., 2013. Assembling the pieces: a framework for the integration of multi-functional ecological main structure in the emerging urban region of Bogotá, Colombia. Urban Ecosyst. 16, 723–739. https://doi.org/10.1007/s11252-013-0292-5
Aristizábal, E., Yokota, S., 2008. Evolución geomorfológica del Valle de Aburrá y sus implicaciones en la ocurrencia de movimientos en masa. Boletín Ciencias la Tierra 24, 5–18.
Aronson, M.F.J., La Sorte, F.A., Nilon, C.H., Katti, M., Goddard, M.A., Lepczyk, C.A., Warren, P.S., Williams, N.S.G., Cilliers, S., Clarkson, B., Dobbs, C., Dolan, R., Hedblom, M., Klotz, S., Kooijmans, J.L., Macgregor-fors, I., McDonnell, M.J., Mörtberg, U., Pyšek, P., Siebert, S., Sushinsky, J., Werner, P., Winter, M., 2014. A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc. R. Soc. 281, 1–8. https://doi.org/10.1098/rspb.2013.3330
Aronson, M.F.J., Lepczyk, C.A., Evans, K.L., Goddard, M.A., Lerman, S.B., MacIvor, J.S., Nilon, C.H., Vargo, T., 2017. Biodiversity in the city: key challenges for urban green space management. Front. Ecol. Environ. 15, 189–196. https://doi.org/10.1002/fee.1480
Asociación Bogotana de Ornitología, 2000. Aves de la Sabana de Bogotá, guía de campo (Birds of Bogotá, a field guide). Asociación Bogotána de Ornitología y Corporación Autonóma Regional de Cundinamarca, Bogotá, D.C., Colombia. 52 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Avendaño, J.E., Cortés-Herrera, J.O., Briceño-Lara, E.R., Rincón-Guarín, D.A., 2013. Crossing or bypassing the Andes: a commentary on recent range extensions of cis- Andean birds to the West of the Andes of Colombia. Orinoquia 17, 207–214.
Barbault, R., 1995. Biodiversity dynamics: from population and community ecology approaches to a landscape ecology point of view. Landsc. Urban Plan. 31, 89–98.
Barrantes, G., Sandoval, L., 2009. Conceptual and statistical problems associated with the use of diversity indices in ecology. Rev. Biol. Trop. 57, 451–460. https://doi.org/10.15517/rbt.v57i3.5467
Becker, C.D., Loughin, T.M., Santander, T., 2008. Identifying forest-obligate birds in tropical moist cloud forest of Andean Ecuador. J. F. Ornithol. 79, 229–244. https://doi.org/10.1111/j.1557-9263.2008.00184.x
Becker, P.H., 2003. Biomonitoring with birds, in: Rooks, M.K., Aramco, S., Snyder, K., Wilson, L., Fleming, J., Wisnewski, M. (Eds.), Bioindicators and Biomonitors. Elsevier Science Ltd, pp. 677–736. https://doi.org/10.1016/S0927-5215(03)80149-2
Beninde, J., Veith, M., Hochkirch, A., 2015. Biodiversity in cities needs space: A meta- analysis of factors determining intra-urban biodiversity variation. Ecol. Lett. 18, 581– 592. https://doi.org/10.1111/ele.12427
Bennie, J., Anderson, K., Wetherelt, A., 2011. Measuring biodiversity across spatial scales in a raised bog using a novel paired-sample diversity index. Source J. Ecol. 99, 482–490. https://doi.org/10.1111/j.l365-2745.2010.01762.x
Biamonte, E., Sandoval, L., Chacón, E., Barrantes, G., 2011. Effect of urbanization on the avifauna in a tropical metropolitan area. Landsc. Ecol. 26, 183–194. https://doi.org/10.1007/s10980-010-9564-0
Bibby, C., Jones, M., Marsden, S., 1998. Expedition Field Techniques: Bird Surveys. Expedition Advisory Centre, Royal Geographical Society, London.
Blair, R.B., 1996. Land use and species diversity along an urban gradient. Ecol. Appl. 6, 506–519.
Borcard, D., Gillet, F., Legendre, P., 2011. Numerical Ecology with R. Springer Science+Business Media, New York.
Botzat, A., Fischer, L.K., Kowarik, I., 2016. Unexploited opportunities in understanding liveable and biodiverse cities. A review on urban biodiversity perception and valuation. Glob. Environ. Chang. 39, 220–233. https://doi.org/10.1016/j.gloenvcha.2016.04.008
CAF, 2017. Crecimiento urbano y acceso a oportunidades: un desafío para América Latina (Urban sprawl and oportunities access: a Latin American challenge). Corporación Andina de Fomento, Bogotá, D.C., Colombia.
Calcagno, V., de Mazancourt, C., 2010. glmulti: An R package for easy automated model selection with (generalized) linear models. J. Stat. Softw. 34, 1–29. https://doi.org/10.18637/jss.v034.i12 Effects of urban green space size, structure and vegetation on local bird 53 richness: a study case in Colombian Northern Andes
Castaño-Villa, G.J., Patiño-Zabala, J.C., 2007. The composition of avian communities in fragmented forest in Santa Elena region, Central Colombian Andes. Boletín Científico Mus. Hist. Nat. 11, 47–60.
Chace, J.F., Walsh, J.J., 2006. Urban effects on native avifauna: A review. Landsc. Urban Plan. 74, 46–69. https://doi.org/10.1016/j.landurbplan.2004.08.007
Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, R.K., Ellison, A.M., 2014. Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67. https://doi.org/10.1890/13-0133.1
Chong, K.Y., Teo, S., Kurukulasuriya, B., Chung, Y.F., Rajathurai, S., Tiang, H., Tan, W., 2014. Not all green is as good: Different effects of the natural and cultivated components of urban vegetation on bird and butterfly diversity. Biol. Conserv. 171, 299–309. https://doi.org/10.1016/j.biocon.2014.01.037
Cincotta, R.P., Wisnewski, J., Engelman, R., 2000. Human population in the biodiversity hotspots. Nature 404, 990–992. https://doi.org/10.1038/35010105
Clergeau, P., Croci, S., Jokimäki, J., Kaisanlahti-Jokimäki, M.L., Dinetti, M., 2006. Avifauna homogenisation by urbanisation: Analysis at different European latitudes. Biol. Conserv. 127, 336–344. https://doi.org/10.1016/j.biocon.2005.06.035
Clergeau, P., Savard, J.P.L., Mennechez, G., Falardeau, G., 1998. Bird abundance and diversity along an urban-rural gradient: a comparative study between two cities on different continents. Condor 100, 413–425.
Cohen, J.E., 2003. Human population: the next half century. Science (80-. ). 302, 1172– 1175. https://doi.org/10.1126/science.1088665
Conole, L.E., Kirkpatrick, J.B., 2011. Functional and spatial differentiation of urban bird assemblages at the landscape scale. Landsc. Urban Plan. 100, 11–23. https://doi.org/10.1016/j.landurbplan.2010.11.007
Delgado-V, C.A., Correa-H, J.C., 2013. Estudios ornitológicos urbanos en Colombia: revisión de literatura (Urban ornithological studies in Colombia: a literature review). Ing. y Cienc. 9, 215–236. https://doi.org/10.17230/ingciecia.9.18.12
Diefenbach, D.R., Brauning, D.W., Mattice, J.A., 2003. Variability in grassland bird counts related to observer differences and species detection rates. Auk 120, 1168–1179.
Evans, K.L., Newson, S.E., Gaston, K.J., 2009. Habitat influences on urban avian assemblages. Ibis (Lond. 1859). 151, 19–39. https://doi.org/10.1111/j.1474- 919X.2008.00898.x
Faeth, S.H., Warren, P.S., Shochat, E., Marussich, W.A., 2005. Trophic Dynamics in Urban Communities. Bioscience 55, 399–407.
Ferenc, M., Sedláček, O., Fuchs, R., Dinetti, M., Fraissinet, M., Storch, D., 2014. Are cities different? Patterns of species richness and beta diversity of urban bird 54 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
communities and regional species assemblages in Europe. Glob. Ecol. Biogeogr. 23, 479–489. https://doi.org/10.1111/geb.12130
Fischer, J.D., Schneider, S.C., Ahlers, A.A., Miller, J.R., 2015. Categorizing wildlife responses to urbanization and conservation implications of terminology. Conserv. Biol. 29, 1246–1248. https://doi.org/10.1111/cobi.12451
Garizábal, J.A., Gutiérrez-Vásquez, C.A., David, S., 2014. Diversidad de aves en cuatro localidades con bosques fragmentados en el municipio de Medellín (Bird diversity in four locations with fragmented forests in Medellín), in: Gutiérrez-Vásquez, C.A. (Ed.), Más Bosques Para Medellín: Sembrando Árboles Para La Vida. Alcaldía de Medellín, Fundación CIPAV, Medellín, pp. 164–199.
Gutiérrez-Tapia, P., Azócar, M.I., Castro, S.A., 2018. A citizen-based platform reveals the distribution of functional groups inside a large city from Southern Hemisphere: e-Bird and the urban birds of Santiago (Central Chile). Rev. Chil. Hist. Nat. 91, 1–16. https://doi.org/10.1186/s40693-018-0073-x
Hsieh, T.C., Ma, K.H., Chao, A., 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456. https://doi.org/10.1111/2041-210X.12613
Jokimäki, J., Kaisanlahti-Jokimäki, M.L., 2003. Spatial similarity of urban bird communities: a multiscale approach. J. Biogeogr. 30, 1183–1193.
Kolde, R., 2019. Package “pheatmap.”
Kowarik, I., 2011. Novel urban ecosystems, biodiversity, and conservation. Environ. Pollut. 159, 1974–1983. https://doi.org/10.1016/j.envpol.2011.02.022
La Sorte, F.A., Lepczyk, C.A., Aronson, M.F.J., Goddard, M.A., Hedblom, M., Katti, M., MacGregor-Fors, I., Mörtberg, U., Nilon, C.H., Warren, P.S., Williams, N.S.G., Yang, J., 2018. The phylogenetic and functional diversity of regional breeding bird assemblages is reduced and constricted through urbanization. Divers. Distrib. 928– 938. https://doi.org/10.1111/ddi.12738
Larondelle, N., Haase, D., 2013. Urban ecosystem services assessment along a rural- urban gradient: A cross-analysis of European cities. Ecol. Indic. 29, 179–190. https://doi.org/10.1016/j.ecolind.2012.12.022
Legendre, P., Legendre, L., 2012. Numerical Ecology, Third Ed. ed. Elsevier B. V., Amsterdam.
Lepczyk, C.A., La Sorte, F.A., Aronson, M.F.J., MacGregor-Fors, I., Nilon, C.H., Warren, P.S., 2017. Global patterns and drivers of urban bird diversity, in: Murgui, E., Hedblom, M. (Eds.), Ecology and Conservation of Birds in Urban Environments. Springer International Publishing, pp. 13–33. https://doi.org/10.1007/978-3-319- 43314-1
Leveau, L.M., Isla, F.I., Bellocq, M.I., 2015. Urbanization and the temporal homogenization of bird communities: a case study in central Argentina. Urban Ecosyst. 18, 1461–1476. https://doi.org/10.1007/s11252-015-0469-1 Effects of urban green space size, structure and vegetation on local bird 55 richness: a study case in Colombian Northern Andes
MacGregor-Fors, I., 2011. Misconceptions or misunderstandings? On the standardization of basic terms and definitions in urban ecology. Landsc. Urban Plan. 100, 347–349. https://doi.org/10.1016/j.landurbplan.2011.01.013
MacGregor-Fors, I., Ortega-Álvarez, R., 2013. Ecología urbana: Experiencias en América Latina (Urban ecology: experiences in Latin America), Primera ed. ed. D.R., Ciudad de México.
Malkinson, D., Kopel, D., Wittenberg, L., 2017. From rural-urban gradients to patch – matrix frameworks: Plant diversity patterns in urban landscapes. Landsc. Urban Plan. 169, 260–268. https://doi.org/10.1016/j.landurbplan.2017.09.021
Marzluff, J.M., 2005. Island biogeography for an urbanizing world: how extinction and colonization may determine biological diversity in human-dominated landscapes. Urban Ecosyst. 8, 157–177. https://doi.org/10.1007/978-0-387-73412-5
Marzluff, J.M., Bowman, R., Donnelly, R., 2001. A historical perspective on urban bird research: trends, terms, and approaches, in: Avian Ecology and Conservation in an Urbanizing World. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 1– 15.
Matthies, S.A., Rüter, S., Schaarschmidt, F., Prasse, R., 2017. Determinants of species richness within and across taxonomic groups in urban green spaces. Urban Ecosyst. 20, 897–909. https://doi.org/10.1007/s11252-017-0642-9
Mcgill, B.J., Dornelas, M., Gotelli, N.J., Magurran, A.E., 2015. Fifteen forms of biodiversity trend in the Anthropocene. Trends Ecol. Evol. 30, 104–113. https://doi.org/10.1016/j.tree.2014.11.006
McKinney, M.L., 2006. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260. https://doi.org/10.1016/j.biocon.2005.09.005
McKinney, M.L., 2002. Urbanization, biodiversity, and conservation. Bioscience 52, 883– 890.
Mejía, M.A., 2016. Naturaleza urbana: Plataforma de experiencias (Urban nature: an experience platform). Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, D.C., Colombia.
Melles, S., Glenn, S., Martin, K., 2003. Urban Bird Diversity and Landscape Complexity: Species– environment Associations Along a Multiscale Habitat Gradient. Conserv. Ecol. 7, 5–27.
Melo, A.S., Rangel, T.F.L.V.B., Diniz-Filho, J.A.F., 2009. Environmental drivers of beta- diversity patterns in New-World birds and mammals. Ecography (Cop.). 32, 226–236. https://doi.org/10.1111/j.1600-0587.2008.05502.x
Molina-Franco, D.A., 2015. Los árboles se toman la ciudad: el proceso de modernización y la transformación del paisaje en Medellín, 1890-1950 (The trees are taking the city: the process of modernization and landscape transformation in Medellín, 1890-1950). Universidad de Antioquia, Medellín, Colombia. 56 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Morelli, F., Benedetti, Y., Ibáñez-Álamo, J.D., Jokimäki, J., Mänd, R., Tryjanowski, P., Møller, A.P., 2016. Evidence of evolutionary homogenization of bird communities in urban environments across Europe. Glob. Ecol. Biogeogr. 25, 1284–1293. https://doi.org/10.1111/geb.12486
Müller, A., Bøcher, P.K., Fischer, C., Svenning, J.C., 2018. ‘Wild’ in the city context: Do relative wild areas offer opportunities for urban biodiversity? Landsc. Urban Plan. 170, 256–265. https://doi.org/10.1016/j.landurbplan.2017.09.027
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, G.A.B., Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Nielsen, A.B., van den Bosch, M., Maruthaveeran, S., van den Bosch, C.K., 2013. Species richness in urban parks and its drivers: A review of empirical evidence. Urban Ecosyst. https://doi.org/10.1007/s11252-013-0316-1
Niemelä, J., 1999. Ecology and urban planning. Biodivers. Conserv. 8, 119–131.
Oksanen, J., Guillaume, F., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P.R., O’Hara, R.B., Simpson, G.L., Solymos, P., Stevens, M.H., Szoecs, E., Wagner, H., 2019. Vegan: Community Ecology Package.
Olden, J.D., Rooney, T.P., 2006. On Defining and Quantifying Biotic Homogenization. Glob. Ecol. Biogeogr. 15, 113–120.
Ortega-Álvarez, R., Macgregor-Fors, I., 2011. Dusting-off the file: A review of knowledge on urban ornithology in Latin America. Landsc. Urban Plan. 101, 1–10. https://doi.org/10.1016/j.landurbplan.2010.12.020
Ouyang, J.Q., Isaksson, C., Schmidt, C., Hutton, P., Bonier, F., Dominoni, D., 2018. A New Framework for Urban Ecology: An Integration of Proximate and Ultimate Responses to Anthropogenic Change. Integr. Comp. Biol. 58, 915–928. https://doi.org/10.1093/icb/icy110
Palliwoda, J., Kowarik, I., Von Der Lippe, M., 2017. Human-biodiversity interactions in urban parks: The species level matters activities of visitors on park grass lands in Berlin. Landsc. Urban Plan. 157, 394–406. https://doi.org/10.1016/j.landurbplan.2016.09.003
Pauchard, A., Aguayo, M., Peña, E., Urrutia, R., 2006. Multiple effects of urbanization on the biodiversity of developing countries: The case of a fast-growing metropolitan area (Concepción, Chile). Biol. Conserv. 127, 272–281. https://doi.org/10.1016/j.biocon.2005.05.015
Peterson, B.G., Carl, P., Boudt, K., Bennet, R., Ulrich, J., Zivot, E., Cornilly, D., Hung, E., Lestel, M., Balkissoon, K., Wertz, D., Alexander, A., Martin, R.D., Zhou, Z., Shea, J.M., 2019. Package “PerformanceAnalytics.”
Pickett, S.T.A., Cadenasso, M.L., Grove, J.M., Boone, C.G., Groffman, P.M., Irwin, E., Kaushal, S.S., Marshall, V., McGrath, B.P., Nilon, C.H., Pouyat, R. V, Szlavecz, K., Troy, A., Warren, P.S., 2011. Urban ecological systems: Scientific foundations and a decade of progress. J. Environ. Manage. 92, 331–362. Effects of urban green space size, structure and vegetation on local bird 57 richness: a study case in Colombian Northern Andes
https://doi.org/10.1016/j.jenvman.2010.08.022
Quantum-GIS-Development-Team, 2018. Quantum GIS Geographic Information System.
Quintero, E., Benavides, A.M., Moreno, N., Gonzalez-Caro, S., 2017. Bosques Andinos: Estado actual y retos para su conservación en Antioquia (Andean forests: conservation status and challenges in Antioquia), 1ra ed. Fundación Jardín Botánico de Medellín Joaquín Antonio Uribe- Programa Bosques Andinos (COSUDE), Medellín.
R Core Team, 2019. The R Stats Package.
Rahbek, C., Borregaard, M.K., Colwell, R.K., Dalsgaard, B., Holt, B.G., Morueta-Holme, N., Nogues-Bravo, D., Whittaker, R.H., Fjeldsa, J., 2019. Humboldt’s enigma: What causes global patterns of mountain biodiversity? Science (80-. ). 365, 1108–1113. https://doi.org/10.1126/science.aax0149
Samarawickrama, U., Piyaratne, D., Ranagalage, M., 2017. Relationship between NDVI with Tasseled cap Indices : A Remote Sensing based Analysis. Int. J. Innov. Res. Technol. 3, 13–19.
Savard, J.P.L., Clergeau, P., Mennechez, G., 2000. Biodiversity concepts and urban ecosystems. Landsc. Urban Plan. 48, 131–142. https://doi.org/10.1016/S0169- 2046(00)00037-2
Sax, D.F., Gaines, S.D., 2003. Species diversity: From global decreases to local increases. Trends Ecol. Evol. 18, 561–566. https://doi.org/10.1016/S0169- 5347(03)00224-6
Shwartz, A., Muratet, A., Simon, L., Julliard, R., 2013. Local and management variables outweigh landscape effects in enhancing the diversity of different taxa in a big metropolis. Biol. Conserv. 157, 285–292. https://doi.org/10.1016/j.biocon.2012.09.009
Shwartz, A., Shirley, S., Kark, S., 2008. How do habitat variability and management regime shape the spatial heterogeneity of birds within a large Mediterranean urban park? Landsc. Urban Plan. 84, 219–229. https://doi.org/10.1016/j.landurbplan.2007.08.003
Sol, D., González-Lagos, C., Moreira, D., Maspons, J., Lapiedra, O., 2014. Urbanisation tolerance and the loss of avian diversity. Ecol. Lett. 17, 942–950. https://doi.org/10.1111/ele.12297
Southon, G.E., Jorgensen, A., Dunnett, N., Hoyle, H., Evans, K.L., 2018. Perceived species-richness in urban green spaces: Cues, accuracy and well- being impacts. Landsc. Urban Plan. 172, 1–10. https://doi.org/10.1016/j.landurbplan.2017.12.002
Stiles, F.G., 1990. La avifauna de la Universidad de Costa Rica y sus alrededores a través de veinte años (1968-1989) (Birds to the University of Costa Rica and surroundings during 20 years, 1968-1989). Rev. Biol. Trop 38, 361–381. 58 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Strohbach, M.W., Lerman, S.B., Warren, P.S., 2013. Are small greening areas enhancing bird diversity? Insights from community-driven greening projects in Boston. Landsc. Urban Plan. 114, 69–79. https://doi.org/10.1016/j.landurbplan.2013.02.007
Sutherland, W.J., Newton, I., Green, R.E., 2004. Bird Ecology and Conservation: A Handbook of Techniques. Oxford University Press / USA, New York.
Threlfall, C.G., Mata, L., Mackie, J.A., Hahs, A.K., Stork, N.E., Williams, N.S.G., Livesley, S.J., 2017. Increasing biodiversity in urban green spaces through simple vegetation interventions. J. Appl. Ecol. 54, 1874–1883. https://doi.org/10.1111/1365- 2664.12876
Travez, J.J., Yánez, P., 2017. Diversidad y abundancia de avifauna en el campus de la UIDE y el Parque Metropolitano Guanguiltagua, Distrito Metropolitano de Quito, recomendaciones para su conservación (Bird diversity and abundance in UIDE campus and Guanguiltagua Metropolitan park). Boletín Técnico , Ser. Zoológica 12– 13, 53–69.
Universidad Nacional de Colombia, 2005. Plan de ordenación y manejo de la cuenca del Río Aburrá (POMCA) (Territorial planning and management of the Aburrá River watershed). Medellin.
Vásquez-Muñoz, J., Castaño-Villa, G., 2008. Identificación de áreas prioritarias para la conservación de la avifauna en la zona urbana del municipio de Medellín, Colombia. Boletín Científico Mus. Hist. Nat. 12, 51–61.
Vitousek, P.M., Mooney, H.A., Lubchenco, J., Melillo, J.M., 1997. Human Domination of Earth’s Ecosystems. Science (80-. ). 277, 494–499.
Walker, B.H., 1992. Biodiversity and Ecological Redundancy. Conserv. Biol. 6, 18–23. https://doi.org/10.1046/j.1523-1739.1992.610018.x
White, J.G., Antos, M.J., Fitzsimons, J.A., Palmer, G.C., 2005. Non-uniform bird assemblages in urban environments: The influence of streetscape vegetation. Landsc. Urban Plan. 71, 123–135. https://doi.org/10.1016/j.landurbplan.2004.02.006
Effects of urban green space size, structure and vegetation on local bird 59 richness: a study case in Colombian Northern Andes
Supplementary material
Supplement 4: Boxplot comparison as exploratory method to evaluate the effect of different data transformation for bird abundances (the species Zenaida auriculata was used as model, due to high frequencies, abundances and tendency of gregarious behavior)1
1 Others species such as Thraupis episcopus (high frequencies and some points with high abundances) and Amazilia tzacatl (high frequencies, low abundances), were also explored, given similar graphical patterns
60 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Supplement 5: Shepard diagrams to evaluate goodness of fit for bird abundance data, using Hellinger distance in seven “neighborhoods” and two “reference sites”– Cophenetic correlation is also shown for each clustering method: Single linkage (“nearest neighbor”), Complete linkage (“furthest neighbor sorting”), UPGMA (“unweighted arithmetic average clustering”) and WPGMA (“weighted arithmetic average clustering”)
Effects of urban green space size, structure and vegetation on local bird 61 richness: a study case in Colombian Northern Andes
Supplement 6: Fusion level and Silhouette plots using Hellinger distance and UPGMA clustering method for bird abundance data in seven “neighborhoods” and two “reference sites”
62 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Supplement 7: Sample completeness curves with 95% of confidence intervals (shaded areas) for bird species diversity in the Metropolitan Area of Aburrá Valley (Antioquia- Colombia) for local bird diversity analysis1
1PER: peri-urban reference site, WCI: western center “Iguaná”, FSW: far south west, FSE: far south east, URB: urban reference site, MSE: middle south east, CSE: close south east, MSW: middle south west, WCH: western center “Hueso”
Effects of urban green space size, structure and vegetation on local bird 63 richness: a study case in Colombian Northern Andes
Supplement 8: Bird species recorded in 91 systematic point counts located on urban and peri-urban areas of the Aburrá Valley (data from 2014 to 2019). Species are arranged in descendent order according to the total relative abundance.
Relative abundance (%)
Order Family Species
urban
-
Total
Urban
reference
Peri
Neighborhoods Urban reference Passeriformes Hirundinidae Pygochelidon cyanoleuca 8,3380 9,5436 2,3148 8,0895 Passeriformes Thraupidae Thraupis episcopus 6,8421 7,0539 1,3889 6,5650 Columbiformes Columbidae Zenaida auriculata 6,8144 3,3195 1,8519 6,3437 Columbiformes Columbidae Columbina talpacoti 5,3463 6,2241 0,0000 5,1143 Passeriformes Thraupidae Thraupis palmarum 5,3186 2,0747 2,7778 4,9914 Passeriformes Thraupidae Coereba flaveola 4,9030 7,8838 0,0000 4,8193 Columbiformes Columbidae Columba livia1 5,1524 0,0000 0,0000 4,5734 Passeriformes Turdidae Turdus ignobilis 4,3213 3,7344 3,2407 4,2292 Passeriformes Tyrannidae Pitangus sulphuratus 3,8781 3,3195 0,4630 3,6636 Psittaciformes Psittacidae Brotogeris jugularis 3,9889 1,2448 0,0000 3,6145 Passeriformes Troglodytidae Troglodytes aedon 3,2133 3,3195 2,3148 3,1719 Passeriformes Tyrannidae Tyrannus melancholicus 3,2964 1,2448 1,8519 3,0981 Cathartiformes Cathartidae Coragyps atratus 1,8006 7,0539 0,0000 2,0162 Apodiformes Trochilidae Amazilia tzacatl 2,0776 1,6598 0,9259 1,9916 Passeriformes Tyrannidae Pyrocephalus rubinus 1,9391 1,6598 0,0000 1,8195 Passeriformes Thraupidae Sicalis flaveola 1,6898 4,9793 0,0000 1,7949 Psittaciformes Psittacidae Forpus conspicillatus 1,7729 0,8299 2,3148 1,7458 Passeriformes Tyrannidae Myiozetetes cayanensis 1,7452 1,2448 0,0000 1,6228 Piciformes Picidae Melanerpes rubricapillus 1,5235 2,9046 0,0000 1,5245 Pelecaniformes Threskiornithidae Phimosus infuscatus 1,5512 2,0747 0,0000 1,4999 Passeriformes Tyrannidae Elaenia flavogaster 1,2465 2,4896 0,4630 1,2786 Passeriformes Thraupidae Tiaris olivaceus 0,8310 4,5643 5,0926 1,2786 Pelecaniformes Ardeidae Bubulcus ibis1 1,1080 1,6598 1,3889 1,1556 Passeriformes Fringillidae Euphonia laniirostris 1,1911 0,0000 0,0000 1,0573 Passeriformes Thraupidae Saltator striatipectus 1,0249 2,4896 0,0000 1,0573 Passeriformes Thraupidae Saltator coerulescens 1,1080 0,8299 0,0000 1,0327 Accipitriformes Accipitridae Rupornis magnirostris 1,0249 0,4149 0,9259 0,9835 Passeriformes Thraupidae Stilpnia cyanicollis 0,9418 0,0000 0,9259 0,8852 Apodiformes Trochilidae Anthracothorax nigricollis 0,9418 0,4149 0,0000 0,8606 Passeriformes Icteridae Molothrus bonariensis 0,7756 0,4149 1,8519 0,8114 Galliformes Cracidae Ortalis columbiana 0,5540 0,0000 5,5556 0,7868 Passeriformes Thamnophilidae Thamnophilus multistriatus 0,8033 1,2448 0,0000 0,7868 Passeriformes Thraupidae Stilpnia vitriolina 0,7202 1,6598 0,4630 0,7622 Passeriformes Tyrannidae Todirostrum cinereum 0,7756 0,4149 0,4630 0,7376 Passeriformes Fringillidae Spinus psaltria 0,6094 1,6598 0,9259 0,6885 Piciformes Picidae Picumnus olivaceus 0,5263 1,6598 0,0000 0,5655 64 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Relative abundance (%)
Order Family Species
urban
-
Total
Urban
reference
Peri
Neighborhoods Urban reference Passeriformes Tyrannidae Sayornis nigricans 0,5540 1,2448 0,0000 0,5655 Piciformes Picidae Melanerpes formicivorus 0,6094 0,0000 0,0000 0,5409 Falconiformes Falconidae Milvago chimachima 0,6094 0,0000 0,0000 0,5409 Charadriiformes Charadriidae Vanellus chilensis 0,5540 0,0000 0,9259 0,5409 Passeriformes Thraupidae Stilpnia heinei 0,3601 0,0000 3,7037 0,5164 Psittaciformes Psittacidae Amazona amazonica 0,5540 0,0000 0,0000 0,4918 Passeriformes Tyrannidae Myiodynastes maculatus 0,4986 0,8299 0,0000 0,4918 Passeriformes Thraupidae Sporophila nigricollis 0,4986 0,4149 0,0000 0,4672 Cuculiformes Cuculidae Crotophaga ani 0,4155 0,0000 1,3889 0,4426 Passeriformes Furnariidae Synallaxis albescens 0,4432 0,8299 0,0000 0,4426 Coraciiformes Momotidae Momotus aequatorialis 0,3324 0,0000 2,3148 0,4180 Apodiformes Trochilidae Saucerottia saucerottei 0,4432 0,4149 0,0000 0,4180 Passeriformes Tyrannidae Zimmerius chrysops 0,3878 0,0000 1,3889 0,4180 Passeriformes Paserellidae Arremon brunneinucha 0,1939 0,0000 4,1667 0,3934 Psittaciformes Psittacidae Amazona ochrocephala 0,4155 0,0000 0,0000 0,3688 Galliformes Cracidae Chamaepetes goudotii 0,1939 0,0000 3,7037 0,3688 Passeriformes Tyrannidae Myioborus miniatus 0,1385 0,0000 3,2407 0,2951 Passeriformes Icteridae Molothrus oryzivorus 0,0000 0,0000 4,6296 0,2459 Piciformes Picidae Colaptes punctigula 0,1662 0,8299 0,4630 0,2213 Passeriformes Tyrannidae Myiarchus cephalotes 0,0554 0,0000 3,2407 0,2213 Passeriformes Thraupidae Tangara labradorides 0,1662 0,0000 1,3889 0,2213 Apodiformes Trochilidae Chlorostilbon melanorhynchus 0,1385 0,8299 0,4630 0,1967 Psittaciformes Psittacidae Eupsittula pertinax 0,1939 0,0000 0,0000 0,1721 Passeriformes Troglodytidae Henicorhina leucophrys 0,0000 0,0000 3,2407 0,1721 Passeriformes Tyrannidae Leptopogon superciliaris 0,1385 0,0000 0,9259 0,1721 Passeriformes Tyrannidae Myiodynastes chrysocephalus 0,0831 0,0000 1,8519 0,1721 Passeriformes Thraupidae Sporophila minuta 0,1939 0,0000 0,0000 0,1721 Passeriformes Paserellidae Atlapetes albinucha 0,0277 0,0000 2,3148 0,1475 Passeriformes Tyrannidae Camptostoma obsoletum 0,0831 1,2448 0,0000 0,1475 Passeriformes Icteridae Hypopyrrhus pyrohypogaster 0,0000 0,0000 2,7778 0,1475 Passeriformes Troglodytidae Pheugopedius mystacalis 0,1385 0,0000 0,4630 0,1475 Passeriformes Thraupidae Ramphocelus flammigerus 0,1662 0,0000 0,0000 0,1475 Passeriformes Fringillidae Euphonia cyanocephala 0,1385 0,0000 0,0000 0,1229 Passeriformes Tyrannidae Machetornis rixosa 0,1108 0,0000 0,4630 0,1229 Passeriformes Tyrannidae Serpophaga cinerea 0,1385 0,0000 0,0000 0,1229 Passeriformes Hirundinidae Stelgidopteryx ruficollis 0,0554 0,4149 0,9259 0,1229 Passeriformes Turdidae Catharus aurantiirostris 0,1108 0,0000 0,0000 0,0984 Passeriformes Thraupidae Chlorospingus flavopectus 0,0000 0,0000 1,8519 0,0984 Passeriformes Thraupidae Anisognathus somptuosus 0,0000 0,0000 1,3889 0,0738 Passeriformes Parulidae Basileuterus rufifrons 0,0277 0,8299 0,0000 0,0738 Passeriformes Corvidae Cyanocorax affinis 0,0831 0,0000 0,0000 0,0738 Effects of urban green space size, structure and vegetation on local bird 65 richness: a study case in Colombian Northern Andes
Relative abundance (%)
Order Family Species
urban
-
Total
Urban
reference
Peri
Neighborhoods Urban reference Piciformes Picidae Dryocopus lineatus 0,0831 0,0000 0,0000 0,0738 Pelecaniformes Ardeidae Egretta thula 0,0831 0,0000 0,0000 0,0738 Columbiformes Columbidae Leptotila verreauxi 0,0554 0,0000 0,4630 0,0738 Passeriformes Parulidae Myiothlypis coronata 0,0000 0,0000 1,3889 0,0738 Passeriformes Thraupidae Sporophila intermedia 0,0831 0,0000 0,0000 0,0738 Passeriformes Vireonidae Vireo leucophrys 0,0000 0,0000 1,3889 0,0738 Passeriformes Thraupidae Volatinia jacarina 0,0831 0,0000 0,0000 0,0738 Passeriformes Paserellidae Zonotrichia capensis 0,0277 0,0000 0,9259 0,0738 Psittaciformes Psittacidae Ara ararauna 0,0554 0,0000 0,0000 0,0492 Passeriformes Parulidae Basileuterus tristriatus 0,0000 0,0000 0,9259 0,0492 Cathartiformes Cathartidae Cathartes aura 0,0277 0,4149 0,0000 0,0492 Piciformes Picidae Colaptes rubiginosus 0,0277 0,0000 0,4630 0,0492 Passeriformes Tyrannidae Elaenia frantzii 0,0000 0,0000 0,9259 0,0492 Falconiformes Falconidae Falco sparverius 0,0277 0,0000 0,4630 0,0492 Passeriformes Tyrannidae Legatus leucophaius 0,0554 0,0000 0,0000 0,0492 Passeriformes Turdidae Myadestes ralloides 0,0000 0,0000 0,9259 0,0492 Passeriformes Tyrannidae Myiophobus fasciatus 0,0554 0,0000 0,0000 0,0492 Passeriformes Thraupidae Saltator atripennis 0,0000 0,0000 0,9259 0,0492 Passeriformes Furnariidae Synallaxis azarae 0,0000 0,0000 0,9259 0,0492 Passeriformes Thraupidae Tangara arthus 0,0000 0,0000 0,9259 0,0492 Passeriformes Thraupidae Tangara nigroviridis 0,0000 0,0000 0,9259 0,0492 Passeriformes Turdidae Turdus fuscater 0,0000 0,0000 0,9259 0,0492 Psittaciformes Psittacidae Ara macao 0,0277 0,0000 0,0000 0,0246 Pelecaniformes Ardeidae Butorides striata 0,0277 0,0000 0,0000 0,0246 Passeriformes Tyrannidae Contopus cinereus 0,0000 0,4149 0,0000 0,0246 Passeriformes Vireonidae Cyclarhis nigrirostris 0,0000 0,0000 0,4630 0,0246 Passeriformes Grallaridae Grallaria ruficapilla 0,0000 0,0000 0,4630 0,0246 Apodiformes Trochilidae Haplophaedia aureliae 0,0000 0,0000 0,4630 0,0246 Gruiformes Rallidae Laterallus albigularis 0,0277 0,0000 0,0000 0,0246 Passeriformes Mimidae Mimus gilvus 0,0277 0,0000 0,0000 0,0246 Pelecaniformes Ardeidae Nycticorax nycticorax 0,0277 0,0000 0,0000 0,0246 Passeriformes Tyrannidae Phaeomyias murina 0,0277 0,0000 0,0000 0,0246 Passeriformes Cotingidae Pipreola riefferii 0,0000 0,0000 0,4630 0,0246 Passeriformes Tyrannidae Pyrrhomyias cinnamomeus 0,0000 0,0000 0,4630 0,0246 Passeriformes Thraupidae Sporophila schistacea 0,0277 0,0000 0,0000 0,0246 Passeriformes Thraupidae Tangara gyrola 0,0000 0,0000 0,4630 0,0246 Passeriformes Tyrannidae Tolmomyias sulphurescens 0,0277 0,0000 0,0000 0,0246 1 Exotic (Non-Neotropical) bird species 66 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Supplement 9: Residuals vs Fitted values, Normal Q-Q, Scale-Location, and Residuals vs Leverage plots for the best-supported models (∆AICc ≤ 0.0) on local bird richness across seven neighborhoods in the Metropolitan Area of the Aburrá Valley, Colombian Northern Andes. Explanatory variables included in the best models: mean size of Grass-shrubs patches (MGrassP), maximum size of Grass-shrubs patches (MaxGrassA), and total area of Grass-shrubs patches (Grass). AICc: Akaike’s Information Criterion corrected for small sample sizes
Model Formula: Richness ~ 1 + MGrassP + MaxGrassA
Effects of urban green space size, structure and vegetation on local bird 67 richness: a study case in Colombian Northern Andes
Model Formula: Shannon ~ 1 + Grass
68 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Supplement 10: Residuals vs Fitted values, Normal Q-Q, Scale-Location, and Residuals vs Leverage plots for the best-supported models (∆AICc ≤ 3.0) on local Shannon diversity across seven neighborhoods in the Metropolitan Area of the Aburrá Valley, Colombian Northern Andes. The only explanatory variable included in the best model was total area of Grass-shrubs patches (Grass); models with AICc ≤ AICc of the model “Shannon ~ 1” were discarded. AICc: Akaike’s Information Criterion corrected for small sample sizes.
Model Formula: Shannon ~ 1 + Grass
Effects of urban green space size, structure and vegetation on local bird 69 richness: a study case in Colombian Northern Andes
Chapter 3. Native tree abundance and natural regeneration increase local bird richness in a Northern Andes city
Garizábal-Carmona J. A.1, 2 and Mancera-Rodríguez N. J.1
1. Universidad Nacional de Colombia. Department of Forestry Sciences, Research group Wildlife Ecology and Conservation. Calle 59A No. 63-20, Bloque 20, oficina 211, Medellín, Colombia; Tel.: +57-4-4309129. Fax: +57-4-4309134, [email protected] (corresponding author) 2. Corporación Merceditas
This article was submitted to “Landscape and Urban Planning” in April 2020 and it was rejected in May. It was submitted to Urban Forestry & Urban Greening in June 2020, after improving some issues commented by Christopher Lepczyk - associated editor of Landscape and Urban Planning. To date, no reply from Urban Forestry & Urban Greening have been received
Abstract
Cities are human-dominated ecosystems where landscape transformation decreases biodiversity, a conservation concern when cities are located in biodiversity hotspots. We aimed to evaluate the effects of site-specific land use and vegetation features on bird richness and to note variables that could increase local biodiversity in an Andean city of Northern South America. From February 2018 to February 2019, we conducted vegetation assessments and bird surveys, and described size, shape, and land cover features in 44 urban green spaces. We found 255 plant species, with only 20% shared between trees and regeneration vegetation levels, and most native species and individuals found in unmanaged sites. According to generalized linear mixed models, local bird richness (25.80 ±8.05 species per point) increased with the percentage of grass-shrubs cover, and the 70 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes abundance of natural regeneration and tree native species, whereas tree features on introduced plant species had no significant effects. Area and perimeter/area ratio were also significant explanatory variables, but only meant a partial limitation for urban planning as relatively small urban green spaces (<5ha) had high local bird richness when they were dominated by natural regeneration and tree native species. Our study suggests that promoting retention of native vegetation, especially at the understory level, could mitigate species loss across high developed Andean cities.
Keywords: bird diversity, natural regeneration, sustainable cities, Tropical Andes, urbanization
Introduction
Cities reflect modern human life and its impacts on the planet. Sociocultural issues influence the composition and structure of cities, where humans transform natural landscapes into novel ecosystems with structurally simple green spaces (Paz Silva et al., 2015; Shih, 2018). These urban green spaces are dominated by a high percentage of non- native introduced vegetation (Nielsen et al., 2013), and they are mainly managed to improve public health, social interaction, and public recreation (Dooling et al., 2006; McDonnell, 2011; Wolch et al., 2014).
Recent thinking in urban planning now includes biodiversity conservation as a key factor to make sustainable cities (Botzat et al., 2016; Puppim De Oliveira et al., 2011; Threlfall and Kendal, 2018), but decision-makers might fail to implement better practices if local ecological studies are lacking (Aronson et al., 2014; Kowarik, 2011), and this is challenging when cities are located in biodiversity hotspots such as the Tropical Andes (Cincotta et al., 2000), where urban bird studies are mostly species lists that have limited use in urban planning and biodiversity conservation (Ortega-Álvarez and Macgregor-Fors, 2011).
Bioindicator groups help to understand how organismal composition of green spaces influences biodiversity, and how local governments could improve urban planning by specific vegetation management (Puppim De Oliveira et al., 2011; Threlfall et al., 2016). Effects of urban green space size, structure and vegetation on local bird 71 richness: a study case in Colombian Northern Andes
Birds are well-known bioindicators (Becker, 2003), and species richness values, which are easy to measure and interpret, reveal reliable patterns across urban ecosystems in response to features of green spaces (Marzluff et al., 2001; Mckinney, 2008; Tryjanowski et al., 2017). The area (size) of green spaces could be a key factor for explaining local bird richness (Beninde et al., 2015; Fernández-Juricic and Jokimäki, 2001; Matthies et al., 2017; Nielsen et al., 2013), but increasing the area is limited in cities with high development. In this case, promoting the dominance of native vegetation could improve green space management towards conserving local biodiversity (Chace and Walsh, 2006; Fontana et al., 2011; Threlfall et al., 2017; Yang et al., 2015).
Landscape and site-specific spatial scales influence biodiversity patterns in cities (Dale, 2018; Jokimäki and Kaisanlahti-Jokimäki, 2003; Nielsen et al., 2013; Xie et al., 2016), but site-specific scales are easier to manage as habitat characteristics explain differences on urban local biodiversity (Ferenc et al., 2014; Shwartz et al., 2013; Threlfall et al., 2017). Site-specific features affect local patterns of several taxonomic groups in Neotropical cities (Macgregor-Fors et al., 2015), but urban ecosystems in this region are understudied and generalizations might not apply to areas like Northern Andes, where high endemic rates and species turnover occur (Rahbek et al., 2019).
In this study, we aimed to evaluate the effects of site-specific land use and vegetation composition and structure features on bird richness, and to note variables that could increase local biodiversity in an Andean city of Northern South America. We hypothesized that urban green spaces with native vegetation and natural regeneration would enhance local bird diversity, and to test it, we focused on individual attributes that could be more accessible to urban planners, and thus, prone to be included in green space management. 72 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Methods
Study area
Medellín is located in Northern central Andes of Colombia, along the Aburrá Valley (6º 15´ N; 75º 34´ W, ¡Error! No se encuentra el origen de la referencia.). It is part of a ten-m unicipality metropolitan area with almost four million inhabitants living between 1450 and 1700 m.a.s.l (Schnitter et al., 2006). We delimited a sampling area of 1383h using a Digital Elevation Model (DEM) corrected by the GRASS GIS r.fill.dir tool (GRASS-Development- Team, 2017), interpolating with Delaunay triangulation method, and processing outputs with r.watershed and half-basin tools in the software QGIS (Quantum-GIS-Development- Team, 2018) (Figure 7).
Figure 7: Study area and location of the 44 sampling points in western center Medellín- Colombia, Northern South America
Effects of urban green space size, structure and vegetation on local bird 73 richness: a study case in Colombian Northern Andes
We selected green spaces >0.1ha systematically across a landscape dominated by infrastructure, locating 44 sampling points with 395.02m between each other on average (min 200m) (Figure 7): two at an urban regional protected park and four at non-urbanized plots with ≥10ha and ≤10% of impervious cover; two at university campuses with ≥10ha and >10% of impervious cover; the rest were located at 38 green spaces ≤10ha, including small parks, street green spaces, and riverside green spaces.
Urban Green Spaces structural and land use features
We delimited green spaces based on satellite imagery taken on 22 February 2019 by Sentinel-2 (USGS EROS Archive), using streets and other impervious surfaces to define limits. We estimated total area, perimeter/area ratio, and land cover type occupied area for each green space. Land cover type was defined as grass-shrubs, trees, or buildings, at 200m radius from sampling point centroids, using Tasseled cap index (Samarawickrama et al., 2017) and reclassification land cover procedures (Quantum-GIS-Development-Team, 2018).
Vegetation surveys and species origin categorization
We accounted and identified all individual vascular plants with circumference ≥10cm at 130cm high, hereafter ‘Trees”, at 25m radius circular plots (n = 44). We also accounted and identified all individuals with <10cm at 130cm high, hereafter “Regeneration”, at five 2.5m radius sub-plots per sampling point (n = 220). On Trees, we estimated basal area and diameter at breast height (accuracy: ±0.01m), and tree crown coverage (longitude from each individual canopy at 90º angle; accuracy: ±1.0m). For unidentified plants, we collected a specimen to be identified at the University of Antioquia Herbarium (HUA) (taxonomy was determined by curators).
To assign species geographic distribution, we used local plant checklist (Ortiz and Idárraga Piedrahita, 2019), and when information was ambiguous, we asked up to six local experienced botanists for validation. We assigned “Native” when natural distribution of species included the Neotropical region and “Introduced” for non-Neotropical plants. Within Native category, we differentiated two subcategories: “Regional”, when the species was 74 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes locally introduced by silvicultural practices from other Neotropical regions (Molina-Franco, 2015), and “Local”, if it naturally occurs within the Aburrá Valley above 1000 m.a.s.l.
Bird surveys
We sampled birds within 25m fixed-radius points (n = 44) during two seasons in 2018: February-April and June-September (half of total sampling each), in the same plots we conducted the vegetation surveys. We made bird surveys only during favorable weather conditions (no rain, especially), adapting protocols from Bibby et al. (1998), between 06:00 and 10:00 hours, always with the same observer recording every individual seen or heard in ten 10-minute visits. We excluded migratory species and overflying birds for analysis.
Data exploring
We evaluated completeness of bird census with sample-size-based and coverage-based rarefaction curves (95% confidence intervals), using the package “iNEXT” in R (Hsieh et al., 2016). For explanatory variables (Supplement 11), we performed Principal Components Analysis (PCA) to identify the most explicative features, exclude ecological redundancy, and reduce the number of variables (see Borcard, Gillet, & Legendre, 2011), and using the function chart.Correlation of the package “PerformanceAnalytics” to identify individual responses against bird richness (Peterson et al., 2019), we selected the following explanatory variables with correlation coefficient R2 ≥ 0.5 and p-value < 0.001: Log green space area (A), perimeter/area ratio (PA), percentage of grass-shrubs at 200m (PerGr), percentage of buildings at 200m (PerBu), Log Native Regeneration abundance (NRAb), Log Local Tree abundance (LTAb) and Log Local Regeneration abundance (LRAb).
We selected the best 10 models using the glmulti function of “Model Selection and Multimodel Inference Made Easy” package (version 1.0.7.1.) in R (Calcagno and de Mazancourt, 2010), fitted under Poisson distribution, seven terms maximum (including the intercept), and only non-redundant formulas: first, we restricted to main effects, and then, included variable interactions. We ranked candidate generalized mixed models using the Akaike’s Information Criterion corrected for small sample sizes (AICc), taking into account only marginal models (due to the high correlation found between explanatory variables). Effects of urban green space size, structure and vegetation on local bird 75 richness: a study case in Colombian Northern Andes
Results
Structural and land use features of green spaces
Green spaces areas ranged between 0.11 and 103.73ha (9.44 ±24.17 on average), and perimeter/area ratios between 0.005 and 0.124m-1 (0.059 ± 0.029). Despite they showed high autocorrelation (R2 = -0.80 and p < 0.001), both structural features contributed highly to the variability of the system, describing different structural features of green spaces. Site- specific land use at the 200m also showed high contribution to the system’s variability: grass-shrub percentage area was 29.83% (±18.38) on average, tree percentage 25.85% (±14.69) and building percentage 44.31% (±23.83).
Vegetation composition and structure
We found 2136 individuals of Trees and 1196 individuals of Regeneration, with 255 species overall and only 50 (20%) shared between categories: 158 were exclusive of Trees (62%, 207 species), and 47 of Regeneration (18%, 106 species) (Supplement 13). On Trees, 65% of species and 53% of individuals were Native (Neotropical sensu lato), but only 23% of species and 23% of individuals were Local (Aburrá Valley above 1000 m.a.s.l.). On Regeneration, less species and individuals were introduced globally or regionally: 67% of species and 68% of individuals were Native, and 48% of species and the 64% of individuals were Local.
Non-native Introduced species were more frequent and abundant in most of the urban green spaces, whereas Native and Local plants were more frequent and abundant in specific green spaces: those with less silvicultural intervention and unmanaged vegetation (Figure 8). In average, species richness decreased between 44 and 50% per plot when we excluded globally introduced species (Introduced), and between 70 and 81% when we excluded regionally introduced species (Regional); we found similar decreasing in abundance and structural vegetation features when differentiated species origin (Table 4).
76 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Figure 8: Most abundant vascular plant species with individuals ≥10cm of perimeter at 130 cm from ground (pole stage plants), and their percentage on the 44 Urban Green Spaces (UGS) evaluated. Unfilled bars are Introduced species, black-line filled bars are Regional species and gray-filled bars are Local species. Black triangles are UGS percentage of presence (%) for each species shown.
Table 4: Some vegetation features across 44 urban green spaces of Medellín-Colombia, Northern South America: richness (species), abundance (individuals), basal area (m2) and crown coverage (m2), differentiating totals and by species origin (Native as Neotropical sensu lato; Local as native within Aburrá Valley above 1000 m.a.s.l.).
Feature Mean Range Feature Mean Range
Total Richness Total basal area
Trees 17.8 (±7.4) 5 - 37 394.3 (±207.7) 19.1 - 931.7
Regeneration 5.4 (±5.8) 1 - 21
Native Richness Native basal area
Trees 9.9 (±5.5) 1 - 26 152.8 (±111.0) 3.2 - 444.2
Effects of urban green space size, structure and vegetation on local bird 77 richness: a study case in Colombian Northern Andes
Feature Mean Range Feature Mean Range
Regeneration 2.7 (±4.1) 0 - 17
Local Richness Local basal area
Trees 3.4 (±3.2) 0 - 16 63.3 (±73.4) 0 - 308.5
Regeneration 1.6 (±3.6) 0 - 14
Total Abundance Total crown coverage
3154.3 419.2 - Trees 48.3 (±28.9) 16 - 173 (±1174.8) 11112.0
Regeneration 27.2 (±45.7) 0 - 202
Native Abundance Native crown coverage
1462.3 33.2 - Trees 25.6 (±28.3) 1 - 139 (±1281.7) 7905.2
Regeneration 18.2 (±37.6) 0 - 154
Local Abundance Local crown coverage
Trees 11.3 (±22.5) 0 - 126 494.0 (±534.8) 0 - 2250.2
Regeneration 14.0 (±34.9) 0 - 146
Bird species composition and richness
We made 9803 records of 81 native (88% of records) and two exotic bird species (12% of records) (Supplement 14). Sampling coverage was above 0.99 overall with 79.84% (±9.91) of estimated bird richness confirmed by direct observation. We observed 25.80 (±8.05) resident bird species per point, with 10.57 (±3.72) species recorded per visit; there was a statistically significant correlation between cumulative bird richness and observed species richness per visit per point (Adjusted R2 >0.7, p-value <0.001).
Local bird richness according to green spaces composition and structure
The percentage of grass-shrubs at 200m and the perimeter/area ratio of green spaces composed the best candidate model from the “only main effects” procedure; both variables were statistically significant (p < 0.05, R2 beta = 0.57). This model was returned after 78 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes comparing 150 candidate models with the seven selected explanatory variables (all with R2 ≥ 0.5 and p < 0.001). All the ten best models with main effects included either the percentage of grass-shrubs at 200m, the percentage of buildings at 200m, or both land use features, whereas the perimeter/area ratio or the area were included in six of these models, but the area never appeared without the perimeter/area ratio and was present only in two of them (Table 5).
Table 5: Best supported models excluding interactions between variables for explaining observed bird richness (RBRiO) across urban green spaces in the city of Medellín- Colombia, Northern South America, highlighting significant variables (p <0.05) in each model with * (A: Area, PA: perimeter/area ratio, PerGr: percentage of grass-shrubs at 200m, PerBu: percentage of building at 200m, LRAb: local regeneration abundance, and LPAb: local plant abundance). Models are compared using the Akaike Information Criterion corrected for small sample sizes (n = 44): AICc and ∆AICc. Model Formula AICc ∆AICc Beta R2
RBRiO ~ 1 + PA* + PerGr* 270.86 0 0.57
RBRiO ~ 1 + PA + PerBu* + LRAb* 271.68 1.38 0.62
RBRiO ~ 1 + PA + PerGr* + PerBu 271.68 1.38 0.59
RBRiO ~ 1 + A* + PA + PerBu + LRAb* 271.87 1.57 0.62
RBRiO ~ 1 + PerGr200 + PerBu 271.93 1.63 0.56
RBRiO ~ 1 + A+ PA* + PerGr* 272.15 1.85 0.57
RBRiO ~ 1 + PerGr* 272.45 2.15 0.52
RBRiO ~ 1 + PerBu* + LRAb* 272.51 2.21 0.58
RBRiO ~ 1 + PA + PerGr + LRAb 272.73 2.43 0.59
RBRiO ~ 1 + PerGr + PerBu* + LRAb* 272.79 2.49 0.59
When we considered variable interactions, after comparing 3200 candidate models, the best model was composed by four elements besides the intercept: the percentage of grass- shrubs at 200m, the area of green spaces (A), Log Local regeneration plants abundance Effects of urban green space size, structure and vegetation on local bird 79 richness: a study case in Colombian Northern Andes
(LRAb), and the interaction of these last two variables (LRAb:A); all included variables were statistically significant (p < 0.05). The latter model, as well as the other nine best models with variable interaction allowed, had a higher R squared beta (0.72) than any best model found with only main effects (max = 0.62) (Table 5). The percentage of grass-shrubs at 200m was present in all of these models (Table 6).
Table 6: Best supported models including interactions between variables for explaining observed bird richness (RBRiO) across urban green spaces in the city of Medellín- Colombia, Northern South America, highlighting significant variables (p <0.05) in each model with * (A: Area, PA: perimeter/area ratio, PerGr: percentage of grass-shrubs at 200m, PerBu: percentage of building at 200m, LRAb: local regeneration abundance, NRAb: native regeneration abundance, and LPAb: local plant abundance). Models are compared using the Akaike Information Criterion corrected for small sample sizes (n = 44): AICc and ∆AICc.
Model Formula AICc ∆AICc Beta R2
RBRiO ~ 1 + A* + PerGr* + LRAb* + LRAb:A* 259.30 0.00 0.72
RBRiO ~ 1 + A* + PerGr* + NRAb* + LRAb* + NRAb:A* 260.17 0.87 0.74
RBRiO ~ 1 + A + PA + PerGr* + LoRAb* + LRAb:A* 260.93 1.63 0.73
RBRiO ~ 1 + A* + PerGr* + PerBu + LRAb* + PerBu:A + LRAb:A* 261.19 1.89 0.76
RBRiO ~ 1 + A + PerGr* + PerBu + LRAb* + LRAb:A* 261.48 2.18 0.72
RBRiO ~ 1 + A* + PerGr* + LRAb* + LRAb:A* + LRAb:PerGr 261.62 2.32 0.72
RBRiO ~ 1 + A + PerGr + LRAb* + PerGr:A + LRAb:A* 261.67 2.37 0.72
RBRiO ~ 1 + A* + PerGr* + LPAb + LRAb* + LRAb:A* 261.72 2.42 0.72
RBRiO ~ 1 + PA* + PerGr* + LRAb* + LRAb:PA* 261.81 2.51 0.70
RBRiO ~ 1 + A* + PerGr* + NRAb + LRAb* + LRAb:A* 261.84 2.54 0.72
Log Native Regeneration abundance and Log Local Trees abundance were absent in the best models from the “only main effects” procedure, but Log Local Regeneration abundance was present in five of them (Table 5). When we considered variable interactions, Log Local 80 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Regeneration abundance was present in all the top-ten models, Log Native Regeneration plant abundance in two, and Log Local plant abundance in one (Table 6). Variables associated with vegetation composition were included as independent elements, and they were also frequently present in the interaction elements within each best model, linked with the area of green spaces, the perimeter/area ratio or a land use feature (Table 6).
Discussion
Area (size) of green spaces is one of the most important features for explaining local bird richness in urban ecosystems (Beninde et al., 2015; Callaghan et al., 2018; Chang and Lee, 2016; Dale, 2018; Nielsen et al., 2013); other features associated with green space shape, such as the perimeter/area ratio, sometimes could be more relevant than the area for explaining it (Helzer and Jelinski, 1999; Horák, 2016; Shih, 2018). In our study, the area as an explanatory variable was absent in the top-ten best models considering only main effects, whereas perimeter/area ratio was present in six of these models; however, both area and perimeter-area ratio were included frequently in the top-ten best models when variable interactions were allowed, so both seemed to be relevant for explaining local bird richness.
The problem in cities like Latin American capitals is that green spaces are enclosed by highly developed territories, making it difficult to manage area and shape features (Leveau et al., 2017; Ortega-Álvarez and MacGregor-Fors, 2009; Paz Silva et al., 2015). As other world regions do, Latin American cities focus urban planning on ecological connectivity frameworks (Andrade et al., 2013; Beninde et al., 2015; Ives et al., 2011; Matsuba et al., 2016; Schütz et al., 2017), but in some cities such as Medellín-Colombia ― due to that “area and shape” problem ― local government is promoting the addition of tree plant species and individuals in existing green spaces to enhance tree richness and abundance, and to enhance vegetation complexity structure, which are supposed to promote habitat heterogeneity; indeed, increasing local biodiversity (Collas et al., 2017; Roy et al., 2012).
Effects of urban green space size, structure and vegetation on local bird 81 richness: a study case in Colombian Northern Andes
Besides area and area-perimeter ratio, our study shows that site-specific land use and vegetation characteristics increase local bird richness. The highest percentage of grass- shrubs at 200m coincided with the highest abundance of native regeneration, local regeneration richness, and local tree abundance, all explanatory variables that were included in most of the best models. Otherwise, no explanatory variables regarding tree richness or tree structural features had a high influence on local bird richness, and this could explain why some studies in Neotropical cities that were mainly focused on tree composition and structure have found no relation between vegetation features and local bird richness (González-Oreja et al., 2012; Paz Silva et al., 2015).
Retention of native vegetation enhances urban biodiversity as economic costs of green space management might be reduced (Aronson et al., 2017; Chong et al., 2014; Threlfall et al., 2017, 2016); that is, local conditions could be effectively enhanced by merely discouraging human disturbance (Kang et al., 2015). Nevertheless, in most urban ecosystems, native understory plant species are more likely to be extirpated than native woody species (Nielsen et al., 2013), resulting in understory dominated by non-native herbaceous and shrubby vegetation that are addressed by silvicultural practices, as is the case in some Neotropical cities (de Castro Pena et al., 2017; Paz Silva et al., 2015). As a consequence, habitat heterogeneity under public management is mainly the result of silvicultural practices of human-selected species while natural regeneration is repressed.
Our data suggest that understory plants in human-managed green spaces had little effect on increasing local bird richness, as they were mainly ornamental introduced herbs or shrubs species (global or regional). This might address nonequivalent habitat structure compared with natural regeneration and reduce the recruitment of woody native plants (Doroski et al., 2018), as midstory and canopy establishment would still depend upon future silvicultural interventions (Quinton et al., 2020). Thus, despite the need of some management to control introduced invasive species in urban green spaces (Nowak, 2012), an effective way to increase local biodiversity is to avoid repressing natural regeneration and promote the abundance of local plants: according to our data, unmanaged green 82 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes spaces embedded within the urban matrix could increase the local bird richness up to 46% compared with managed green spaces of similar size.
The “area and shape” problem could be mitigated by better local management practices, as there is an area threshold around 20ha for increasing bird richness in cities (Fernández- Juricic and Jokimäki, 2001). In our study, a green space with 16.13ha had the highest resident bird richness (44), and one out of two sampling points located in a green space with 103.71ha had less resident bird species (29) than seven points in sites smaller than 5ha, which have more percentage of grass/shrubs cover, and more richness and abundance of native plant species. Hence, relatively small green spaces in Andean cities will be able to increase bird richness by improving site-specific habitat characteristics, especially for suburban adapters species (Shwartz et al., 2008) that are found mainly in green spaces with less human disturbance at ground or understory vegetation level (Rousseau et al., 2015; Yang et al., 2015). However, these would represent other challenges for citizen security and social aesthetic perception (Carrus et al., 2015; Ignatieva et al., 2011; Soga et al., 2016).
Trees still might be important to enhance local biodiversity in urban Neotropical ecosystems in small green spaces (Barbosa de Toledo et al., 2012; de Castro Pena et al., 2017), besides improving the connectivity of isolated patches (Beninde et al., 2015; Strohbach et al., 2013). In our data, it was difficult to find any response on local bird richness related with tree features, and this was probably a result of having a high percentage of non-Neotropical or regional introduced plants (González-Oreja et al., 2012; Paz Silva et al., 2015). Thus, local rather than regional native vegetation need to be established in urban green spaces in a biodiverse and biogeographically complex region such as the Tropical Andes (Bax and Francesconi, 2019; Melo et al., 2009; Rahbek et al., 2019), as a way to alleviate urbanization-biodiversity conflicts across the highly developed Andean cities.
Our results supported the prediction that variables associated with native vegetation features had the highest effects on local bird richness, especially the land use type that Effects of urban green space size, structure and vegetation on local bird 83 richness: a study case in Colombian Northern Andes represented non-human managed green spaces, as well as site-specific habitat characteristics related to higher natural regeneration abundance and tree abundance. Therefore, it seems that vegetation could have limited effects on local bird richness unless its composition and structure are shaped by native species.
Area and perimeter/area ratio of green spaces also influenced local bird richness, but their effects only meant a partial limitation for urban planning strategies on biodiversity conservation, as we found that relatively small urban green spaces (<5ha) would be able to increase local bird richness by local vegetation management, particularly when Native Local species are differentiated from Native Regional and Introduced (non-Neotropical) species. So that, in the matter of urban planning of vegetation, the more species are not necessarily the better: it depends on how urban planning is aligned with the surrounding natural ecosystems and their biodiversity.
References
Andrade, G.I., Remolina, F., Wiesner, D., 2013. Assembling the pieces: a framework for the integration of multi-functional ecological main structure in the emerging urban region of Bogotá, Colombia. Urban Ecosyst. 16, 723–739. https://doi.org/10.1007/s11252-013-0292-5 Aronson, M.F.J., La Sorte, F.A., Nilon, C.H., Katti, M., Goddard, M.A., Lepczyk, C.A., Warren, P.S., Williams, N.S.G., Cilliers, S., Clarkson, B., Dobbs, C., Dolan, R., Hedblom, M., Klotz, S., Kooijmans, J.L., Macgregor-fors, I., McDonnell, M.J., Mörtberg, U., Pyšek, P., Siebert, S., Sushinsky, J., Werner, P., Winter, M., 2014. A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc. R. Soc. 281, 1–8. https://doi.org/10.1098/rspb.2013.3330 Aronson, M.F.J., Lepczyk, C.A., Evans, K.L., Goddard, M.A., Lerman, S.B., MacIvor, J.S., Nilon, C.H., Vargo, T., 2017. Biodiversity in the city: key challenges for urban green space management. Front. Ecol. Environ. 15, 189–196. https://doi.org/10.1002/fee.1480 Barbosa de Toledo, M.C., Donatelli, R.J., Teixeira Batista, G., 2012. Relation between 84 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
green spaces and bird community structure in an urban area in Southeast Brazil. Urban Ecosyst. 15, 111–131. https://doi.org/10.1007/s11252-011-0195-2 Bax, V., Francesconi, W., 2019. Conservation gaps and priorities in the Tropical Andes biodiversity hotspot: Implications for the expansion of protected areas. J. Environ. Manage. 232, 387–396. https://doi.org/10.1016/j.jenvman.2018.11.086 Becker, P.H., 2003. Biomonitoring with birds, in: Rooks, M.K., Aramco, S., Snyder, K., Wilson, L., Fleming, J., Wisnewski, M. (Eds.), Bioindicators and Biomonitors. Elsevier Science Ltd, pp. 677–736. https://doi.org/10.1016/S0927-5215(03)80149-2 Beninde, J., Veith, M., Hochkirch, A., 2015. Biodiversity in cities needs space: A meta- analysis of factors determining intra-urban biodiversity variation. Ecol. Lett. 18, 581– 592. https://doi.org/10.1111/ele.12427 Bibby, C., Jones, M., Marsden, S., 1998. Expedition Field Techniques: Bird Surveys. Expedition Advisory Centre, Royal Geographical Society, London. Borcard, D., Gillet, F., Legendre, P., 2011. Numerical Ecology with R. Springer Science+Business Media, New York. Botzat, A., Fischer, L.K., Kowarik, I., 2016. Unexploited opportunities in understanding liveable and biodiverse cities. A review on urban biodiversity perception and valuation. Glob. Environ. Chang. 39, 220–233. https://doi.org/10.1016/j.gloenvcha.2016.04.008 Calcagno, V., de Mazancourt, C., 2010. glmulti: An R package for easy automated model selection with (generalized) linear models. J. Stat. Softw. 34, 1–29. https://doi.org/10.18637/jss.v034.i12 Callaghan, C.T., Major, R.E., Lyons, M.B., Martin, J.M., Kingsford, R.T., 2018. The effects of local and landscape habitat attributes on bird diversity in urban greenspaces. Ecosphere 9, e02347. https://doi.org/10.1002/ecs2.2347 Carrus, G., Scopelliti, M., Lafortezza, R., Colangelo, G., Ferrini, F., Salbitano, F., Agrimi, M., Portoghesi, L., Semenzato, P., Sanesi, G., 2015. Go greener, feel better? The positive effects of biodiversity on the well-being of individuals visiting urban and peri- urban green areas. Landsc. Urban Plan. 134, 221–228. https://doi.org/10.1016/j.landurbplan.2014.10.022 Chace, J.F., Walsh, J.J., 2006. Urban effects on native avifauna: A review. Landsc. Urban Plan. 74, 46–69. https://doi.org/10.1016/j.landurbplan.2004.08.007 Chang, H.-Y., Lee, Y.-F., 2016. Effects of area size, heterogeneity, isolation, and Effects of urban green space size, structure and vegetation on local bird 85 richness: a study case in Colombian Northern Andes
disturbances on urban park avifauna in a highly populated tropical city. Urban Ecosyst. 19, 257–274. https://doi.org/10.1007/s11252-015-0481-5 Chong, K.Y., Teo, S., Kurukulasuriya, B., Chung, Y.F., Rajathurai, S., Tiang, H., Tan, W., 2014. Not all green is as good: Different effects of the natural and cultivated components of urban vegetation on bird and butterfly diversity. Biol. Conserv. 171, 299–309. https://doi.org/10.1016/j.biocon.2014.01.037 Cincotta, R.P., Wisnewski, J., Engelman, R., 2000. Human population in the biodiversity hotspots. Nature 404, 990–992. https://doi.org/10.1038/35010105 Collas, L., Green, R.E., Ross, A., Wastell, J.H., Balmford, A., 2017. Urban development , land sharing and land sparing : the importance of considering restoration. J. Appl. Ecol. 54, 1865–1873. https://doi.org/10.1111/1365-2664.12908 Dale, S., 2018. Urban bird community composition influenced by size of urban green spaces, presence of native forest, and urbanization. Urban Ecosyst. 21, 1–14. https://doi.org/10.1007/s11252-017-0706-x de Castro Pena, J.C., Martello, F., Ribeiro, M.C., Armitage, R.A., Young, R.J., Rodrigues, M., 2017. Street trees reduce the negative effects of urbanization on birds. PLoS One 12, 1–19. https://doi.org/10.1371/journal.pone.0174484 Dooling, S., Simon, G., Yocom, K., 2006. Place-based urban ecology: A century of park planning in Seattle. Urban Ecosyst. 9, 299–321. https://doi.org/10.1007/s11252-006- 0008-1 Doroski, D.A., Felson, A.J., Bradford, M.A., Ashton, M.P., Oldfield, E.E., Hallett, R.A., Kuebbing, S.E., 2018. Factors driving natural regeneration beneath a planted urban forest. Urban For. Urban Green. 29, 238–247. https://doi.org/10.1016/j.ufug.2017.11.019 Ferenc, M., Sedláček, O., Fuchs, R., 2014. How to improve urban greenspace for woodland birds: site and local-scale determinants of bird species richness. Urban Ecosyst. 17, 625–640. https://doi.org/10.1007/s11252-013-0328-x Fernández-Juricic, E., Jokimäki, J., 2001. A habitat island approach to conserving birds in urban landscapes: case studies from southern and northern Europe. Biodivers. Conserv. 10, 2023–2043. Fontana, S., Sattler, T., Bontadina, F., Moretti, M., 2011. How to manage the urban green to improve bird diversity and community structure. Landsc. Urban Plan. 101, 278– 285. https://doi.org/10.1016/j.landurbplan.2011.02.033 86 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
González-Oreja, J.A., Barillas-Gómez, A.L., Bonache-Regidor, C., Buzo-Franco, D., García-Guzmán, J., Hernández-Santín, L., 2012. Does habitat heterogeneity affect bird community structure in urban parks?, in: Lepczyk, C.A., Warren, P.S. (Eds.), Urban Bird Ecology and Conservation. Studies in Avian Biology. University of California Press, Berkeley, pp. 1–15. GRASS-Development-Team, 2017. Geographic Resources Analysis Support System (GRASS) Software. Helzer, C.J., Jelinski, D.E., 1999. The relative importance of patch area and perimeter- area ratio to grassland breeding birds. Ecol. Appl. 9, 1448–1458. https://doi.org/10.1890/1051-0761(1999)009[1448:TRIOPA]2.0.CO;2 Horák, J., 2016. Suitability of biodiversity-area and biodiversity-perimeter relationships in ecology: a case study of urban ecosystems. Urban Ecosyst. 19, 131–142. https://doi.org/10.1007/s11252-015-0492-2 Hsieh, T.C., Ma, K.H., Chao, A., 2016. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456. https://doi.org/10.1111/2041-210X.12613 Ignatieva, M., Stewart, G.H., Ignatieva, M., Stewart, G.H., Meurk, C., 2011. Planning and Design of Ecological Networks in Urban Areas. Landsc. Ecol. Eng. 7, 17–25. https://doi.org/10.1007/s11355-010-0143-y Ives, C.D., Hose, G.C., Nipperess, D.A., Taylor, M.P., 2011. Environmental and landscape factors influencing ant and plant diversity in suburban riparian corridors. Landsc. Urban Plan. 103, 372–382. https://doi.org/10.1016/j.landurbplan.2011.08.009 Jokimäki, J., Kaisanlahti-Jokimäki, M.L., 2003. Spatial similarity of urban bird communities: a multiscale approach. J. Biogeogr. 30, 1183–1193. Kang, W., Minor, E.S., Park, C.-R., Lee, D., 2015. Effects of habitat structure, human disturbance, and habitat connectivity on urban forest bird communities. Urban Ecosyst. 18, 857–870. https://doi.org/10.1007/s11252-014-0433-5 Kowarik, I., 2011. Novel urban ecosystems, biodiversity, and conservation. Environ. Pollut. 159, 1974–1983. https://doi.org/10.1016/j.envpol.2011.02.022 Leveau, L.M., Leveau, C.M., Villegas, M., Cursach, J.A., Suazo, C.G., 2017. Bird Communities Along Urbanization Gradients: a Comparative Analysis Among Three Neotropical Cities. Ornitol. Neotrop. 28, 77–87. Effects of urban green space size, structure and vegetation on local bird 87 richness: a study case in Colombian Northern Andes
Macgregor-Fors, I., Avendaño-Reyes, S., Bandala, V.M., Chacón-Zapata, S., Díaz- Toribio, M.H., González-García, F., Lorea-Hernández, F., Martínez-Gómez, J., Montes De Oca, E., Montoya, L., Pineda, Eduardo, Ramírez-Restrepo, Lorena, Rivera-García, Eduardo, Utrera-Barrillas, Elsa, Escobar, Federico, Ecosyst, U., Pineda, E, Ramírez-Restrepo, L, Rivera-García, E, Utrera-Barrillas, E, Escobar, F, 2015. Multi-taxonomic diversity patterns in a neotropical green city: a rapid biological assessment. Urban Ecosyst. 18, 633–647. https://doi.org/10.1007/s11252-014-0410- z Marzluff, J.M., Bowman, R., Donnelly, R., 2001. A historical perspective on urban bird research: trends, terms, and approaches, in: Avian Ecology and Conservation in an Urbanizing World. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp. 1– 15. Matsuba, M., Nishijima, S., Katoh, K., 2016. Effectiveness of corridor vegetation depends on urbanization tolerance of forest birds in central Tokyo, Japan. Urban For. Urban Green. 18, 173–181. https://doi.org/10.1016/j.ufug.2016.05.011 Matthies, S.A., Rüter, S., Schaarschmidt, F., Prasse, R., 2017. Determinants of species richness within and across taxonomic groups in urban green spaces. Urban Ecosyst. 20, 897–909. https://doi.org/10.1007/s11252-017-0642-9 McDonnell, M.J., 2011. The History of Urban Ecology: An Ecologist’s Perspective, in: Niemelä, J., Breuste, J.H., Elmqvist, T., Guntenspergen, G., James, P., Mcintyre, N.E., Mcdonnell, M.J. (Eds.), Urban Ecology. Oxford University Press, Oxford, pp. 5– 13. Mckinney, M.L., 2008. Effects of urbanization on species richness: A review of plants and animals. Urban Ecosyst. 11, 161–176. https://doi.org/10.1007/s11252-007-0045-4 Melo, A.S., Rangel, T.F.L.V.B., Diniz-Filho, J.A.F., 2009. Environmental drivers of beta- diversity patterns in New-World birds and mammals. Ecography (Cop.). 32, 226–236. https://doi.org/10.1111/j.1600-0587.2008.05502.x Molina-Franco, D.A., 2015. Los árboles se toman la ciudad: el proceso de modernización y la transformación del paisaje en Medellín, 1890-1950 (The trees are taking the city: the process of modernization and landscape transformation in Medellín, 1890-1950). Universidad de Antioquia, Medellín, Colombia. Nielsen, A.B., van den Bosch, M., Maruthaveeran, S., van den Bosch, C.K., 2013. Species richness in urban parks and its drivers: A review of empirical evidence. 88 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Urban Ecosyst. https://doi.org/10.1007/s11252-013-0316-1 Nowak, D.J., 2012. Contrasting natural regeneration and tree planting in fourteen North American cities. Urban For. Urban Green. 11, 374–382. https://doi.org/10.1016/j.ufug.2012.02.005 Ortega-Álvarez, R., Macgregor-Fors, I., 2011. Dusting-off the file: A review of knowledge on urban ornithology in Latin America. Landsc. Urban Plan. 101, 1–10. https://doi.org/10.1016/j.landurbplan.2010.12.020 Ortega-Álvarez, R., MacGregor-Fors, I., 2009. Living in the big city: Effects of urban land- use on bird community structure, diversity, and composition. Landsc. Urban Plan. 90, 189–195. https://doi.org/10.1016/j.landurbplan.2008.11.003 Ortiz, R. del C., Idárraga Piedrahita, A., 2019. Catálogo de las Plantas Vasculares del Departamento de Antioquia (The Catalogue of the Vascular Plants of the Department of Antioquia, Colombia) [WWW Document]. Trop. Bot. Inf. Syst. Missouri Bot. Gard. St. Louis, USA. URL http://tropicos.org/projectwebportal.aspx?pagename=Home&projectid=11&langid=66 (accessed 6.9.19). Paz Silva, C., García, C.E., Estay, S.A., Barbosa, O., 2015. Bird Richness and Abundance in Response to Urban Form in a Latin American City: Valdivia, Chile as a Case Study. PLoS One 10, 1–16. https://doi.org/10.1371/journal.pone.0138120 Peterson, B.G., Carl, P., Boudt, K., Bennet, R., Ulrich, J., Zivot, E., Cornilly, D., Hung, E., Lestel, M., Balkissoon, K., Wertz, D., Alexander, A., Martin, R.D., Zhou, Z., Shea, J.M., 2019. Package “PerformanceAnalytics.” Puppim De Oliveira, J.A., Balaban, O., Doll, C.N.H., Moreno-Peñaranda, R., Gasparatos, A., Iossifova, D., Suwa, A., 2011. Cities and biodiversity: Perspectives and governance challenges for implementing the convention on biological diversity (CBD) at the city level. Biol. Conserv. 144, 1302–1313. https://doi.org/10.1016/j.biocon.2010.12.007 Quantum-GIS-Development-Team, 2018. Quantum GIS Geographic Information System. Quinton, J.M., Duinker, P.N., Steenberg, J.W.N., Charles, J.D., 2020. The living among the dead: Cemeteries as urban forests, now and in the future. Urban For. Urban Green. 48, 126564. https://doi.org/10.1016/j.ufug.2019.126564 Rahbek, C., Borregaard, M.K., Colwell, R.K., Dalsgaard, B., Holt, B.G., Morueta-Holme, N., Nogues-Bravo, D., Whittaker, R.H., Fjeldsa, J., 2019. Humboldt’s enigma: What Effects of urban green space size, structure and vegetation on local bird 89 richness: a study case in Colombian Northern Andes
causes global patterns of mountain biodiversity? Science (80-. ). 365, 1108–1113. https://doi.org/10.1126/science.aax0149 Rousseau, J.S., Savard, J.-P.L., Titman, R., 2015. Shrub-nesting birds in urban habitats: their abundance and association with vegetation. Urban Ecosyst. 18, 871–884. https://doi.org/10.1007/s11252-014-0434-4 Roy, S., Byrne, J., Pickering, C., 2012. A systematic quantitative review of urban tree benefits, costs, and assessment methods across cities in different climatic zones. Urban For. Urban Green. 11, 351–363. https://doi.org/10.1016/j.ufug.2012.06.006 Samarawickrama, U., Piyaratne, D., Ranagalage, M., 2017. Relationship between NDVI with Tasseled cap Indices : A Remote Sensing based Analysis. Int. J. Innov. Res. Technol. 3, 13–19. Schnitter, P., Giraldo, M.L., Patiño, J.M., 2006. La ocupación del territorio en el proceso de urbanización del área metropolitana del valle de Aburrá, Colombia (Urbanization process in the Metropolitan Area of Aburrá Valley, Colombia). Rev. electrónica Geogr. y ciencias Soc. 10, 83–90. Schütz, C., Reckendorfer, W., Schulze, C.H., 2017. Local quality versus regional connectivity—habitat requirements of wintering woodpeckers in urban green spaces. J. Urban Ecol. 3, 1–11. https://doi.org/10.1093/jue/jux019 Shih, W.Y., 2018. Bird diversity of greenspaces in the densely developed city centre of Taipei. Urban Ecosyst. 21, 379–393. https://doi.org/10.1007/s11252-017-0720-z Shwartz, A., Muratet, A., Simon, L., Julliard, R., 2013. Local and management variables outweigh landscape effects in enhancing the diversity of different taxa in a big metropolis. Biol. Conserv. 157, 285–292. https://doi.org/10.1016/j.biocon.2012.09.009 Shwartz, A., Shirley, S., Kark, S., 2008. How do habitat variability and management regime shape the spatial heterogeneity of birds within a large Mediterranean urban park? Landsc. Urban Plan. 84, 219–229. https://doi.org/10.1016/j.landurbplan.2007.08.003 Soga, M., Gaston, K.J., Koyanagi, T.F., Kurisu, K., Hanaki, K., 2016. Urban residents’ perceptions of neighbourhood nature: Does the extinction of experience matter? Biol. Conserv. 203, 143–150. https://doi.org/10.1016/j.biocon.2016.09.020 Strohbach, M.W., Lerman, S.B., Warren, P.S., 2013. Are small greening areas enhancing bird diversity? Insights from community-driven greening projects in Boston. Landsc. 90 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Urban Plan. 114, 69–79. https://doi.org/10.1016/j.landurbplan.2013.02.007 Threlfall, C.G., Kendal, D., 2018. The distinct ecological and social roles that wild spaces play in urban ecosystems. Urban For. Urban Green. 29, 348–356. https://doi.org/10.1016/j.ufug.2017.05.012 Threlfall, C.G., Mata, L., Mackie, J.A., Hahs, A.K., Stork, N.E., Williams, N.S.G., Livesley, S.J., 2017. Increasing biodiversity in urban green spaces through simple vegetation interventions. J. Appl. Ecol. 54, 1874–1883. https://doi.org/10.1111/1365- 2664.12876 Threlfall, C.G., Williams, N.S.G., Hahs, A.K., Livesley, S.J., 2016. Approaches to urban vegetation management and the impacts on urban bird and bat assemblages. Landsc. Urban Plan. 153, 28–39. https://doi.org/10.1016/j.landurbplan.2016.04.011 Tryjanowski, P., Morelli, F., Mikula, P., Krištín, A., Indykiewicz, P., Grzywaczewski, G., Kronenberg, J., Jerzak, L., 2017. Bird diversity in urban green space: A large-scale analysis of differences between parks and cemeteries in Central Europe. Urban For. Urban Green. 27, 264–271. https://doi.org/10.1016/j.ufug.2017.08.014 Wolch, J.R., Byrne, J., Newell, J.P., 2014. Urban green space, public health, and environmental justice: The challenge of making cities “just green enough.” Landsc. Urban Plan. 125, 234–244. https://doi.org/10.1016/j.landurbplan.2014.01.017 Xie, S., Lu, F., Cao, L., Zhou, W., Ouyang, Z., 2016. Multi-scale factors influencing the characteristics of avian communities in urban parks across Beijing during the breeding season. Sci. Rep. 6, 1–9. https://doi.org/10.1038/srep29350 Yang, G., Xu, J., Wang, Y., Wang, X., Pei, E., Yuan, X., Li, H., Ding, Y., Wang, Z., 2015. Evaluation of microhabitats for wild birds in a Shanghai urban area park. Urban For. Urban Green. 14, 246–254. https://doi.org/10.1016/j.ufug.2015.02.005
Effects of urban green space size, structure and vegetation on local bird 91 richness: a study case in Colombian Northern Andes
Supplementary material
Supplement 11: Potential explanatory variables to predict local bird richness in the city of Medellín-Colombia, Northern South America. Variable Abbrev Description Units
2 Urban green space area A Area based on delimited green spaces m
Urban green space 푃 PA 푃퐴 = 1/m perimeter/area ratio 퐴 Percentage of trees at 푇푟푒푒푠 푎푟푒푎 푎푡 200푚 PerTr 푃푒푟푇푟 = ∗ 100% % 200m 푇표푡푎푙 푎푟푒푎 푎푡 200푚 Percentage of grass- 퐺푟푎푠푠/푠ℎ푟푢푏푠 푎푟푒푎 푎푡 200푚 PerGr 푃푒푟퐺푟 = ∗ 100% % shrubs at 200m 푇표푡푎푙 푎푟푒푎 푎푡 200푚 Percentage of buildings 퐵푢𝑖푙푑𝑖푛𝑔 푎푟푒푎 푎푡 200푚 PerBu 푃푒푟퐵푢 = ∗ 100% % at 200m 푇표푡푎푙 푎푟푒푎 푎푡 200푚 Total Trees richness TTRi 100% field inventory at 25m circular plots Spp
Total Trees abundance TTAb 100% field inventory at 25m circular plots Ind
Total Regeneration Field inventory at five 2.5m circular sub-plots TRRi Spp richness (within the 25m plot)
Total Regeneration Field inventory at five 2.5m circular sub-plots TRAb Ind abundance (within the 25m plot)
Total Trees crown Estimated longitude from each individual TTCo m2 coverage canopy at 90º angle (accuracy: ±1.0m)
Estimated from perimeters at 130cm from Total Trees basal area TBA m2 ground
Total Trees average TTH 100% field inventory at 25m circular plots m height
Native Trees richness NPRi 100% field inventory at 25m circular plots Spp
Native Trees abundance NPAb 100% field inventory at 25m circular plots Ind
Native Regeneration Field inventory at five 2.5m circular sub-plots NRRi Spp richness (within the 25m plot)
Native Regeneration Field inventory at five 2.5m circular sub-plots NRAb Ind abundance (within the 25m plot)
Native Trees crown Estimated longitude from each individual NTCo m2 coverage canopy at 90º angle (accuracy: ±1.0m) 92 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Variable Abbrev Description Units
Estimated from perimeters at 130cm from Native Trees basal area NBA m2 ground
Native Trees average NTH 100% field inventory at 25m circular plots m height
Local Trees richness LPRi 100% field inventory at 25m circular plots Spp
Local Trees abundance LPAb 100% field inventory at 25m circular plots Ind
Local Regeneration LRRi 100% field inventory at 25m circular plots Spp richness
Local Regeneration LRAb 100% field inventory at 25m circular plots Ind abundance
Local Trees crown Estimated longitude from each individual LTCo m2 coverage canopy at 90º angle (accuracy: ±1.0m)
Estimated from perimeters at 130cm from Local Trees basal area LBA m2 ground
Local Trees average LTH 100% field inventory at 25m circular plots m height
Effects of urban green space size, structure and vegetation on local bird 93 richness: a study case in Colombian Northern Andes
Supplement 12: Local resident bird richness (RBRiO), and selected compositional and structural features in 44 urban green spaces of Medellín-Colombia, Northern South America: area in ha (A), perimeter/area ratio (PA), percentage of grass-shrubs at 200m (PerGr), percentage of buildings at 200m (PerBu), Native Regeneration abundance (NRAb), Local Tree abundance (LPAb), and Local regeneration abundance (LRAb). Point RBRiO A PA PerGr PerBu NRAb LPAb LRAb
80-1 19 A 0.087 6.51 83.29 0 2 0
80-2 16 0.2 0.063 22.14 46.28 0 1 0
80-3 17 1.0 0.076 17.22 65.06 0 0 0
80-4 17 0.2 0.102 24.11 60.87 1 1 0 Al1 44 0.5 0.012 67.31 9.82 133 126 112 Al2 30 16.1 0.059 32.01 44.55 32 16 15 Al3 24 1.9 0.072 22.75 61.30 4 7 0 Am1 18 1.4 0.067 19.63 71.61 0 5 0 Am2 14 0.8 0.055 13.27 76.75 0 2 0 Am3 24 0.8 0.071 23.70 44.85 2 9 0 Am4 20 2.1 0.111 11.00 80.48 0 1 0 Cal1 43 0.2 0.009 74.64 21.49 42 35 37 Cal2 44 48.9 0.009 77.64 18.68 124 38 116 Cal3 26 48.9 0.009 53.03 30.82 59 14 56 CE 21 48.9 0.104 24.30 12.65 17 4 1 Con 17 0.5 0.070 21.00 36.58 37 5 0 Es1 26 1.5 0.059 23.42 58.15 0 8 0 Es2 28 0.8 0.036 32.02 38.47 1 3 0 Flo1 19 1.7 0.049 13.78 48.96 0 5 0 Flo2 23 1.1 0.072 17.87 68.94 10 2 1 FN 17 0.3 0.124 14.06 81.95 0 3 0 I1 33 0.1 0.037 23.20 41.95 2 2 0 I2 35 3.6 0.037 23.26 19.88 1 6 0 I3 40 3.6 0.049 31.66 35.60 23 3 9 I4 26 1.6 0.076 38.88 28.47 3 4 0 Lau2 19 1.2 0.048 21.15 54.58 1 2 0 Lau3 21 0.7 0.060 21.12 45.05 1 8 0 Mac1 18 0.3 0.091 15.01 51.17 0 2 0 Mac2 31 0.3 0.029 25.93 21.55 0 15 0 SJ 19 1.8 0.085 19.62 69.96 0 1 0 SL1 34 0.4 0.058 30.13 40.95 15 28 12 SL2 24 1.6 0.063 17.71 66.46 4 5 0 94 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Point RBRiO A PA PerGr PerBu NRAb LPAb LRAb
SL3 28 1.5 0.076 19.11 58.92 1 0 0 SL4 23 0.5 0.089 18.84 62.34 1 2 0 SM1 39 0.7 0.024 53.74 32.99 30 3 18 SM2 27 4.3 0.041 42.14 36.50 0 1 0 Sur1 27 0.9 0.087 17.77 42.53 1 0 1 Sur2 21 0.5 0.069 29.32 21.88 0 3 0 UNAL 27 0.9 0.049 34.03 15.79 0 4 0 UPB 31 1.0 0.060 44.20 23.47 4 5 0 Vel1 18 1.2 0.071 19.19 57.36 3 9 0 Vel2 22 2.1 0.069 18.07 55.33 0 3 0 Vo1 29 1.1 0.005 53.66 5.15 94 29 92 Vo2 36 103.7 0.005 83.75 0.33 154 77 146 Prom 25.8 103.7 0.060 29.84 44.31 18.18 11.34 14 SD 8.1 9.4 0.030 18.38 21.84 37.61 22.49 34.92 Max 44.0 24.2 0.120 83.75 83.29 154 126 146 Min 14.0 103.7 0.010 6.51 0.33 0 0 0
Effects of urban green space size, structure and vegetation on local bird 95 richness: a study case in Colombian Northern Andes
Supplement 13: Trees (Trees) and Regeneration (Rege) relative abundance and occurrence of vascular plant species in 44 urban green spaces of Medellín-Colombia, Northern South America, arranged in descendent order according to relative abundance (%) of Trees (Trees Ab); relative abundance (%) of Renegeration (Rege Ab) is also shown. Species distribution origin (Dist) is shown as Reg (Regional), Loc (Local), and Int (Introduced), and species relative occurrence (%) as the percentage of sampling points with at least one individual per species per category (Trees Occ: Trees occurrence, Rege Occ: Regeneration Occurrence). “Species” marked with * were not counted in total plant richness.
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Fraxinus uhdei Int 8.38 63.64 0.25 6.82
Leucaena leucocephala Int 6.04 45.45 4.10 18.2
Guazuma ulmifolia Reg 4.78 6.82 0.00 -
Myrsine coriacea Loc 4.31 9.09 0.17 4.55
Mangifera indica Int 3.42 65.91 2.93 6.82
Spathodea campanulata Int 2.81 45.45 0.00 -
Erythrina fusca Loc 2.25 40.91 0.00 -
Eucalyptus sp. Int 2.25 13.64 0.00 -
Dypsis lutescens Int 2.15 29.55 0.33 2.27
Pithecellobium dulce Reg 2.15 43.18 0.84 4.55
Citrus sp. Int 2.11 36.36 0.59 2.27
Psidium guajava Loc 1.92 40.91 1.17 4.55
Ficus benjamina Int 1.83 38.64 0.00 -
Tabebuia chrysantha Reg 1.78 43.18 0.08 2.27
Eugenia uniflora Int 1.69 18.18 0.00 -
Zygia longifolia Reg 1.50 15.91 0.08 2.27
Bauhinia picta Reg 1.45 27.27 0.59 4.55
Caesalpinia cf. peltophoroides Reg 1.45 29.55 0.08 2.27
Senna spectabilis Reg 1.36 27.27 0.25 4.55
Solanum sp. Loc 1.31 9.09 1.42 6.82 96 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Erythrina poeppigiana Loc 1.26 25 0.00 -
Terminalia catappa Int 1.26 27.27 0.17 2.27
Cascabela thevetia Reg 1.17 20.45 0.08 2.27
Dead Trees* - 1.17 22.73 0.00 -
Acnistus arborescens Loc 1.12 18.18 1.09 6.82
Jacaranda mimosifolia Int 1.12 25 0.00 -
Persea caerulea Loc 1.12 18.18 0.42 6.82
Persea americana Reg 1.08 25 0.25 4.55
Miconia resima Loc 1.03 2.27 0.00 -
Schinus terebinthifolia Int 1.03 22.73 0.00 -
Miconia caudata Loc 0.98 4.55 0.25 2.27
Inga cf. edulis Loc 0.89 11.36 0.00 -
Adonidia merrillii Int 0.84 13.64 0.00 -
Zanthoxylum fagara Loc 0.80 4.55 0.08 2.27
Calliandra haematocephala Reg 0.75 13.64 0.00 -
Cojoba arborea Reg 0.75 20.45 0.00 -
Lafoensia acuminata Reg 0.75 18.18 0.00 -
Schefflera actinophylla Int 0.75 25 0.00 -
Yucca gigantea Int 0.75 18.18 0.00 -
Brunfelsia pauciflora Int 0.70 13.64 0.08 2.27
Dracaena sp. Int 0.70 18.18 1.25 9.09
Hibiscus elatus Int 0.70 6.82 0.08 2.27
Tabebuia rosea Loc 0.70 11.36 0.00 -
Byrsonima crassifolia Loc 0.61 6.82 0.84 4.55
Cassia fistula Reg 0.61 6.82 0.00 -
Piper aduncum Loc 0.61 9.09 0.42 2.27
Malpighia glabra Reg 0.51 13.64 0.00 -
Syzygium jambos Int 0.51 18.18 0.33 6.82
Bunchosia armeniaca Reg 0.47 6.82 0.00 - Effects of urban green space size, structure and vegetation on local bird 97 richness: a study case in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Ceiba pentandra Reg 0.47 13.64 0.00 -
Hura crepitans Reg 0.47 13.64 0.00 -
Caesalpinia ebano Reg 0.42 11.36 0.00 -
Caryota urens Int 0.42 11.36 0.00 -
Cestrum nocturnum Reg 0.42 6.82 0.00 -
Codiaeum variegatum Int 0.42 13.64 0.42 2.27
Trichanthera gigantea Loc 0.42 9.09 0.17 2.27
Anacardium excelsum Reg 0.37 9.09 0.00 -
Delonix regia Int 0.37 18.18 0.00 -
Piper crassinervium Loc 0.37 4.55 0.25 2.27
Sapindus saponaria Loc 0.37 15.91 0.00 -
Tabernaemontana litoralis Reg 0.37 13.64 0.00 -
Acrocomia aculeata Reg 0.33 4.55 0.00 -
Flacourtia indica Int 0.33 9.09 0.00 -
Brassiophoenix schumanii Int 0.28 2.27 0.00 -
Carica papaya Reg 0.28 9.09 0.08 2.27
Eriobotrya japonica Int 0.28 13.64 0.08 2.27
Hymenaea courbaril Reg 0.28 9.09 0.00 -
Lagerstroemia speciosa Int 0.28 6.82 0.00 -
Uknown* - 0.28 11.36 2.84 -
Albizia saman Reg 0.23 6.82 0.00 -
Araucaria excelsa Int 0.23 9.09 0.00 -
Cecropia sp. Loc 0.23 11.36 0.00 -
Myrcia sp. Loc 0.23 2.27 0.08 2.27
Pseudobombax septenatum Reg 0.23 6.82 0.00 -
Roystonea regia Int 0.23 9.09 0.00 -
Zanthoxylum rhoifolium Loc 0.23 2.27 0.00 -
Calophyllum sp. Loc 0.19 2.27 0.00 -
Caryodendron orinocense Reg 0.19 6.82 0.00 - 98 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Cedrela odorata Loc 0.19 9.09 0.00 -
Cocos nucifera Reg 0.19 6.82 0.00 -
Cupania americana Reg 0.19 2.27 0.00 -
Dypsis decaryi Int 0.19 4.55 0.00 -
Hamelia patens Loc 0.19 6.82 0.00 -
Machaerium biovulatum Reg 0.19 2.27 0.00 -
Miconia aeruginosa Loc 0.19 2.27 0.08 2.27
Pachira sp. Loc 0.19 4.55 0.00 -
Pseudosamanea guachapele Reg 0.19 4.55 0.00 -
Syzygium malaccense Int 0.19 6.82 0.00 -
Tithonia diversifolia Int 0.19 2.27 1.09 4.55
Adenaria floribunda Loc 0.14 4.55 0.00 -
Albizia carbonaria Loc 0.14 4.55 0.00 -
Archontophoenix cunninghamiana Int 0.14 4.55 1.76 2.27
Averrhoa carambola Int 0.14 6.82 0.00 -
Azadirachta indica Int 0.14 4.55 0.00 -
Blighia sapida Int 0.14 4.55 0.00 -
Bomarea sp. Loc 0.14 2.27 0.00 -
Brownea grandiceps Reg 0.14 4.55 0.00 -
Bucida buceras Reg 0.14 6.82 0.00 -
Calliandra medellinensis Loc 0.14 4.55 0.00 -
Cariniana pyriformis Reg 0.14 6.82 0.00 -
Coffea arabica Int 0.14 4.55 1.25 4.55
Cupressus lusitanica Int 0.14 2.27 0.00 -
Enterolobium cyclocarpum Reg 0.14 6.82 0.00 -
Erythrina crista-galli Int 0.14 4.55 0.00 -
Hibiscus rosa-sinensis Int 0.14 6.82 2.84 6.82
Jatropha multifida Int 0.14 4.55 0.00 -
Murraya paniculata Int 0.14 4.55 0.00 - Effects of urban green space size, structure and vegetation on local bird 99 richness: a study case in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Musa acuminata Int 0.14 2.27 0.00 -
Phoenix canariensis Int 0.14 2.27 0.00 -
Quararibea cordata Reg 0.14 6.82 0.00 -
Ricinus communis Int 0.14 2.27 0.08 2.27
Swietenia macrophylla Reg 0.14 4.55 0.00 -
Annona muricata Reg 0.09 2.27 0.00 -
Bastardia viscosa Reg 0.09 2.27 0.92 2.27
Caesalpinia pulcherrima Reg 0.09 2.27 0.00 -
Callistemon speciosus Int 0.09 4.55 0.00 -
Crescentia cujete Reg 0.09 4.55 0.00 -
Dilodendron costaricense Reg 0.09 4.55 0.00 -
Dipteryx oleifera Reg 0.09 4.55 0.00 -
Garcinia madruno Reg 0.09 4.55 0.00 -
Genipa americana Reg 0.09 4.55 0.00 -
Livistonia chinensis Int 0.09 2.27 0.00 -
Luehea seemannii Reg 0.09 4.55 0.00 -
Miconia albicans Loc 0.09 2.27 1.59 4.55
Myroxylon balsamum Reg 0.09 4.55 0.00 -
Palicourea garciae Loc 0.09 2.27 0.08 2.27
Petrea rugosa Reg 0.09 2.27 0.00 -
Pterocarpus acapulcencis Reg 0.09 2.27 0.00 -
Sambucus nigra Reg 0.09 4.55 0.00 -
Spondias mombin Reg 0.09 2.27 0.00 -
Syagrus romanzoffiana Int 0.09 2.27 0.00 -
Syzygium paniculatum Int 0.09 4.55 0.00 -
Tabebuia serratifolia Reg 0.09 4.55 0.00 -
Tecoma stans Reg 0.09 2.27 0.00 -
Terminalia ivorensis Int 0.09 4.55 0.00 -
Triplaris americana Reg 0.09 2.27 0.00 - 100 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Vernonanthura patens Loc 0.09 4.55 0.67 4.55
Weinmannia pubescens Loc 0.09 2.27 0.00 -
Anacardiaceae 1* Int 0.05 2.27 0.00 -
Andira inermis Reg 0.05 2.27 0.00 -
Artocarpus altilis Int 0.05 2.27 0.00 -
Astronium graveolens Reg 0.05 2.27 0.00 -
Bactris pilosa Reg 0.05 2.27 0.00 -
Billia rosea Loc 0.05 2.27 0.00 -
Bischofia javanica Int 0.05 2.27 0.00 -
Boehmeria caudata Loc 0.05 2.27 0.00 -
Brownea ariza Reg 0.05 2.27 0.00 -
Brugmansia candida Loc 0.05 2.27 0.00 -
Bursera simaruba Reg 0.05 2.27 0.00 -
Cespedesia spathulata Reg 0.05 2.27 0.00 -
Cestrum racemosum Loc 0.05 2.27 0.00 -
Cf. Retrophyllum rospigliosii Loc 0.05 2.27 0.00 -
Coccoloba uvifera Reg 0.05 2.27 0.00 -
Cochlospermum orinocense Reg 0.05 2.27 0.00 -
Copernicia tectorum Reg 0.05 2.27 0.00 -
Cordia alliodora Loc 0.05 2.27 0.17 2.27
Croton sp. Int 0.05 2.27 0.00 -
Cryosophila kalbreyeri Reg 0.05 2.27 0.00 -
Dovyalis hebecarpa Int 0.05 2.27 0.00 -
Duranta sp. Loc 0.05 2.27 0.00 -
Elaeis guineensis Int 0.05 2.27 0.00 -
Erythroxylon coca Reg 0.05 2.27 0.00 -
Euphorbia pulcherrima Int 0.05 2.27 0.00 -
Ficus aff. citrifolia Reg 0.05 2.27 0.00 -
Ficus cf. maxima Reg 0.05 2.27 0.00 - Effects of urban green space size, structure and vegetation on local bird 101 richness: a study case in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Ficus lyrata Int 0.05 2.27 0.00 -
Flacourtiaceae sp. Int 0.05 2.27 0.00 -
Geoffroea spinosa Reg 0.05 2.27 0.00 -
Guarea guidonia Loc 0.05 2.27 0.00 -
Guarea kunthiana Loc 0.05 2.27 0.00 -
Hasseltia floribunda Reg 0.05 2.27 0.00 -
Hymenaea oblongifolia Reg 0.05 2.27 0.00 -
Inga cf. columbiana Reg 0.05 2.27 0.00 -
Lantana camara Reg 0.05 2.27 2.09 6.82
Lecythis tuyrana Reg 0.05 2.27 0.00 -
Lonchocarpus sp. Reg 0.05 2.27 0.00 -
Megaskepasma erythrochlamys Int 0.05 2.27 0.00 -
Melia azedarach Int 0.05 2.27 0.00 -
Melicoccus bijugatus Reg 0.05 2.27 0.00 -
Morus alba Int 0.05 2.27 0.00 -
Muntingia calabura Reg 0.05 2.27 0.00 -
Musa paradisiaca Int 0.05 2.27 0.00 -
Ochroma pyramidale Loc 0.05 2.27 0.00 -
Ormosia cf. colombiana Loc 0.05 2.27 0.00 -
Pachira speciosa Loc 0.05 2.27 0.00 -
Palicouorea sp. Loc 0.05 2.27 0.08 2.27
Patinoa almirajo Reg 0.05 2.27 0.00 -
Petitia domingensis Int 0.05 2.27 0.00 -
Phoenix cf. reclinata Int 0.05 2.27 0.00 -
Phyllanthus acidus Int 0.05 2.27 0.00 -
Phytelephas macrocarpa Reg 0.05 2.27 0.00 -
Pinus patula Int 0.05 2.27 0.00 -
Plinia cauliflora Reg 0.05 2.27 0.00 -
Plumeria sp. Int 0.05 2.27 0.67 2.27 102 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Polyscias scutellaria Int 0.05 2.27 0.00 -
Pourouma cecropiifolia Reg 0.05 2.27 0.00 -
Psidium cf. guineense Loc 0.05 2.27 1.09 2.27
Quercus humboldti Loc 0.05 2.27 0.00 -
Rollinia mucosa Reg 0.05 2.27 0.00 -
Schizolobium parahyba Reg 0.05 2.27 0.00 -
Senna sp.* Reg 0.05 2.27 0.67 6.82
Stemmadenia grandiflora Reg 0.05 2.27 0.00 -
Syagrus sancona Reg 0.05 2.27 0.00 -
Syzygium tamnoisno Int 0.05 2.27 0.00 -
Terminalia sp. Int 0.05 2.27 0.00 -
Trattinnickia aspera Reg 0.05 2.27 0.00 -
Vitex cf. parviflora Int 0.05 2.27 0.00 -
Washingtonia robusta Int 0.05 2.27 0.00 -
Xylopia aromatica Reg 0.05 2.27 0.00 -
Acalypha macrostachya Loc 0.00 0.00 1.51 2.27
Acanthus spinosus Int 0.00 0.00 0.59 2.27
Ageratina sp. - 0.00 0.00 0.92 2.27
Annonacea sp.* - 0.00 0.00 0.08 2.27
Argyranthemum frutescens - 0.00 0.00 1.59 2.27
Aristolochia cf. ringens Loc 0.00 0.00 0.08 2.27
Asteraceae sp1. - 0.00 0.00 0.00 2.27
Asteraceae sp2. - 0.00 0.00 0.00 2.27
Asteraceae sp3. - 0.00 0.00 0.00 2.27
Baccharis nitida Loc 0.00 0.00 0.08 2.27
Bixa orellana Reg 0.00 0.00 0.08 2.27
Calathea sp. - 0.00 0.00 3.34 2.27
Calea angosturana Loc 0.00 0.00 0.08 2.27
Calliandra sp. - 0.00 0.00 0.67 6.82 Effects of urban green space size, structure and vegetation on local bird 103 richness: a study case in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Cf. Petiveria alliacea Reg 0.00 0.00 1.00 2.27
Chromolaena tacotana Loc 0.00 0.00 1.42 6.82
Citharexylum kunthianum Reg 0.00 0.00 0.08 2.27
Clibadium surinamense Loc 0.00 0.00 0.17 4.55
Clidemia capitellata Loc 0.00 0.00 2.68 2.27
Clidemia ciliata Loc 0.00 0.00 1.00 4.55
Clidemia hirta Loc 0.00 0.00 0.33 4.55
Clidemia sericea Loc 0.00 0.00 2.59 4.55
Cryosophila kanbrexen Reg 0.00 0.00 0.08 2.27
Cupania sp. - 0.00 2.27 0.33 -
Erechtites hieraciifolius Loc 0.00 0.00 0.17 2.27
Euphorbiaceae sp.* - 0.00 0.00 0.33 2.27
Fabacea sp.* - 0.00 0.00 0.25 4.55
Guaiacum officinale Reg 0.00 0.00 0.08 2.27
Hyptis capitata Loc 0.00 0.00 0.67 2.27
Impatiens walleriana Int 0.00 0.00 0.08 2.27
Inga sp.* - 0.00 0.00 0.67 2.27
Miconia cf. prasina Loc 0.00 0.00 0.08 2.27
Miconia ibaguensis Loc 0.00 0.00 1.17 2.27
Miconia rubiginosa Loc 0.00 0.00 1.25 2.27
Miconia sp.* - 0.00 0.00 0.59 2.27
Mimosa albida Loc 0.00 0.00 0.92 6.82
Mimosaceae sp.* - 0.00 0.00 0.25 4.55
Monnina phytolaccifolia Loc 0.00 0.00 0.33 2.27
Monstera deliciosa Reg 0.00 0.00 1.00 25
Monstera sp2. Reg 0.00 0.00 1.92
Nictaginacea sp. - 0.00 0.00 0.50 2.27
Peltaea sessiliflora Reg 0.00 2.27 0.33 -
Piper eriopodon Loc 0.00 0.00 0.17 2.27 104 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Species Dist Trees Ab Trees Occ Rege Ab Rege Occ
Piper hispidum Reg 0.00 0.00 0.17 4.55
Piper holtonii Loc 0.00 0.00 2.68 2.27
Piper jericoense Loc 0.00 0.00 18.48 9.09
Piper sp.* - 0.00 0.00 0.17 2.27
Rhynchosia schomburgkii Loc 0.00 0.00 3.85 9.09
Rubus urticifolius Loc 0.00 0.00 1.51 6.82
Sambucus peruviana Reg 0.00 0.00 0.08 2.27
Schefflera cf. arboricola Int 0.00 0.00 0.67 2.27
Solanum umbellatum Loc 0.00 0.00 0.08 2.27
Strelitzia reginae Reg 0.00 0.00 0.25 2.27
Swinglea sp. Reg 0.00 0.00 0.25 2.27
Theobroma cacao Reg 0.00 0.00 0.17 2.27
Tibouchina cf. ciliaris Loc 0.00 0.00 0.08 2.27
Verbena sp. - 0.00 0.00 4.35 4.55
Verbenaceae sp* - 0.00 0.00 0.42 6.82
Effects of urban green space size, structure and vegetation on local bird 105 richness: a study case in Colombian Northern Andes
Supplement 14: Resident bird species recorded across 44 urban green spaces in Medellín-Colombia, Northern South America, arranged in descendent order according to relative abundance (%). Species occurrence (% of urban green spaces) is also shown.
Family Species Abundance Occurrence Columbidae Zenaida auriculata 8.90 97.73 Columbidae Columba livia 8.74 29.55 Thraupidae Thraupis episcopus 6.64 97.73 Columbidae Columbina talpacoti 5.92 95.45 Psittacidae Brotogeris jugularis 4.89 72.73 Hirundinidae Pygochelidon cyanoleuca 4.61 70.45 Thraupidae Thraupis palmarum 4.07 90.91 Thraupidae Coereba flaveola 3.70 97.73 Thraupidae Sicalis flaveola 3.51 93.18 Turdidae Turdus ignobilis 3.51 97.73 Tyrannidae Pitangus sulphuratus 2.88 100.00 Tyrannidae Tyrannus melancholicus 2.88 97.73 Troglodytidae Troglodytes aedon 2.73 95.45 Cathartidae Coragyps atratus 2.41 56.82 Trochilidae Amazilia tzacatl 2.29 100.00 Picidae Melanerpes rubricapillus 1.97 86.36 Threskiornithidae Phimosus infuscatus 1.97 40.91 Tyrannidae Pyrocephalus rubinus 1.75 77.27 Psittacidae Forpus conspicillatus 1.57 40.91 Fringillidae Euphonia laniirostris 1.54 59.09 Thraupidae Stilpnia vitriolina 1.25 43.18 Trochilidae Anthracothorax nigricollis 1.16 72.73 Psittacidae Amazona ochrocephala 1.10 22.73 Psittacidae Amazona amazonica 1.07 20.45 Accipitridae Rupornis magnirostris 1.03 56.82 Tyrannidae Myiozetetes cayanensis 0.97 43.18 Tyrannidae Elaenia flavogaster 0.94 29.55 Tyrannidae Todirostrum cinereum 0.94 43.18 Icteridae Molothrus bonariensis 0.91 25.00 Thraupidae Saltator coerulescens 0.88 38.64 Psittacidae Eupsittula pertinax 0.85 13.64 Cuculidae Crotophaga ani 0.78 9.09 Falconidae Milvago chimachima 0.78 36.36 Tyrannidae Myiodynastes maculatus 0.75 43.18 Tyrannidae Sayornis nigricans 0.72 38.64 Picidae Picumnus olivaceus 0.66 38.64 106 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Family Species Abundance Occurrence Thamnophilidae Thamnophilus multistriatus 0.60 25.00 Thraupidae Saltator striatipectus 0.56 22.73 Thraupidae Sporophila nigricollis 0.56 25.00 Furnariidae Synallaxis albescens 0.47 18.18 Trochilidae Saucerottia saucerottei 0.44 27.27 Thraupidae Tiaris olivaceus 0.44 13.64 Picidae Colaptes punctigula 0.41 27.27 Fringillidae Spinus psaltria 0.35 15.91 Charadriidae Vanellus chilensis 0.35 13.64 Psittacidae Ara severus 0.28 6.82 Thraupidae Sporophila minuta 0.28 13.64 Parulidae Basileuterus rufifrons 0.25 9.09 Turdidae Catharus aurantiirostris 0.25 11.36 Trochilidae Chlorostilbon melanorhynchus 0.25 15.91 Fringillidae Euphonia cyanocephala 0.25 6.82 Falconidae Falco sparverius 0.25 18.18 Tyrannidae Camptostoma obsoletum 0.22 11.36 Tyrannidae Elaenia chiriquensis 0.22 6.82 Tyrannidae Myiophobus fasciatus 0.22 11.36 Cracidae Ortalis columbiana 0.22 9.09 Icteridae Molothrus oryziborus 0.19 4.55 Troglodytidae Pheugopedius mystacalis 0.19 6.82 Thraupidae Sporophila schistacea 0.13 9.09 Ardeidae Bubulcus ibis 0.09 4.55 Corvidae Cyanocorax affinis 0.09 2.27 Picidae Dryocopus lineatus 0.09 4.55 Ardeidae Egretta thula 0.09 4.55 Tyrannidae Phaeomyias murina 0.09 6.82 Tyrannidae Serpophaga cinerea 0.09 4.55 Thraupidae Stilpnia cyanicollis 0.09 4.55 Passerellidae Zonotrichia capensis 0.09 6.82 Accipitridae Elanus leucurus 0.06 2.27 Columbidae Leptotila verreauxi 0.06 2.27 Momotidae Momotus aequatorialis 0.06 4.55 Cuculidae Piaya cayana 0.06 2.27 Psittacidae Amazona autumnalis 0.03 2.27 Rallidae Anurolimnas viridis 0.03 2.27 Ardeidae Butorides striata 0.03 2.27 Cathartidae Cathartes aura 0.03 2.27 Trochilidae Coeligena coeligena 0.03 2.27 Effects of urban green space size, structure and vegetation on local bird 107 richness: a study case in Colombian Northern Andes
Family Species Abundance Occurrence Cuculidae Crotophaga major 0.03 2.27 Rallidae Laterallus albigularis 0.03 2.27 Tyrannidae Machetornis rixosa 0.03 2.27 Ardeidae Nycticorax nycticorax 0.03 2.27 Tyrannidae Phyllomyias griseiceps 0.03 2.27 Furnariidae Synallaxis azarae 0.03 2.27 Tyrannidae Zimmerius chrysops 0.03 2.27
Chapter 4. Conclusions and recommendations
Conclusions
This Master’s thesis represents the first multiscale approach to evaluate the effects of urban green spaces on local biodiversity in a city of Northern Andes of South America. Using birds as bioindicators, we found that urbanization in this region is a scale-dependent and a species-specific environmental human-pressure, which effects relies upon some biogeographical and ecological traits of each species, including habitat use, distributional patterns, altitudinal range, and trophic guilds, along with green space area, shape, and local composition and structure, which are now highly influenced by urban planning and silvicultural management.
The level of urbanization at different spatial scales (urban core, 1000m, 500m, and 200m) explained the composition of bird community assemblages, as well as the occurrence and frequency patterns of most species detected during our sampling exercises: 129 of 166 bird species (77.71%) were categorized as urban avoiders (37), adapters (55), and exploiters (77), with the other 37 species considered data deficient. The latter were mainly low density bird species that were rare in highly or moderately developed areas, where most sampling points used for bird categorization were located (126 out of 141 points used). Urban avoider species responded negatively to the percentage of building cover across the multiscale urban gradient, and their occurrence and frequency were higher in peri-urban areas with Andean forest remnants; these species represent mainly taxa with narrow altitudinal ranges, including endemic, near-endemics and other species with an exclusively trans- Andean distribution.
Bird community assemblages across most developed areas of the Aburrá Valley are now composed by widely distributed and generalist species that are favored by agricultural and urban sprawl, deriving in a process of biotic homogenization as common species in most
110 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes developed areas, including urban parks and metropolitan regional protected areas, are actually part of a larger scale Neotropical biota. In other words, urbanization is causing the loss of native biota of Northern Andes, probably decreasing local phylogenetic and evolutionarily diversity in a region that is considered a global biodiversity hotspot, precisely by its high endemism rates and species turnover. Futhermore, the lack of historical data on bird community assemblages and the severe landscape transformation in the region probably underestimates the negative effects that urbanization has driven across Andean cities and surroundings, as less tolerant bird species are already absent of the most developed areas.
Additionally, biodiversity descriptors beyond species richness are needed to understand the urbanization effects on local biodiversity, and also, multiscale approaches, in both biodiversity measurements and spatial scales, are critical to describe ecological patterns and detect biodiversity conservation issues. In the some urban neighborhoods of the Aburrá Valley species richness could be as high as those found in less-perturbed contiguous ecosystems, but species composition and other biodiversity descriptors differ, and thus, evaluating biodiversity beyond the number of species will be essential to get a wider scope of the conservation status across Northern Andes cities.
Furthermore, urban green spaces management in Andean cities must take into account the relativeness of being “native” in this biogeographically complex region, especially when silvicultural processes have been developed under a different scale, evaluating the species origin at national/regional rather than at local levels. Indeed, certain species that are considered native on inaccurate distributional data are now a significant part of vegetation composition and abundance in the city, which is a biodiversity conservation concern as native Andean biota with narrower distributional ranges, including both plants and birds, are disappearing from the community assemblages, as well as the ecological and evolutionary dynamics that rely upon them. This study demonstrates the importance of natural regeneration and understory development under more natural than human-managed influences to enhance local bird richness across the most developed areas, although it would be compelling to test whether this pattern is also supported by other biodiversity analysis on alfa, beta and gamma scales.
Effects of urban green spaces composition and structure on local bird 111 diversity: a study case from a populated city in Colombian Northern Andes
This thesis is a contribution to the knowledge of biodiversity patterns across the Northern Andes biodiverse region, with potential applications in both conservation biology and urban planning. Our findings are critical to developing more effective conservation strategies in Andean urban ecosystems, as not only bird biodiversity but vegetation and other biological groups are similarly affected by urbanization pressures.
Recommendations
Landscape approaches such as ecological connectivity studies could improve the interpretation of local biodiversity patterns. Due to the relevance in addressing multiscale scenarios along with the highly complex and heterogeneous topography of Northern Andes, it would be useful to study a wider rural-urban gradient in the Metropolitan Area of the Aburrá Valley, including areas under 2000 m.a.s.l. with forest remnants and human- dominated land covers (recreational farms and cattle-agricultural areas). This sort of mixed- landscape is present between 1000 and 1500 m.a.s.l. in Northern Aburrá Valley (municipalities of Barbosa and Don Matias), and between 1700 and 2000 m.a.s.l. in the southern Aburrá Valley (municipality of Caldas).
Additionally, it would be informative to include areas above 2300 m.a.s.l., where the cloud Andean forest had been less perturbed, but in the last decade (2010-2020) new suburban areas have been developed, especially in the southeastern slope of the Valley in the municipalities of Medellín, Envigado, and Sabaneta. These areas would add to the picture other environmental conditions, both in terms of natural and human determinants, which are possibly influencing biodiversity patterns in the region and will be increasing the conservation concerns at the regional scale in the near future.
Otherwise, at the local scale, it would be useful to replicate similar sampling designs in other micro-watersheds of the Metropolitan Area of the Aburrá Valley, mixing bird studies (or similar fauna bioindicators) and vegetation inventories (both trees and grass-shrubs strata), as this study suggest that there are urbanization patterns and urban green spaces management at a micro-watershed scale that could be driving differential responses of biodiversity within the most developed urban areas. Additionally, it is necessary to reduce several barriers existing between university academic circles and decision-makers in developing countries, including local governments, citizens, environmental entities and the 112 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes building industry, to encourage multidisciplinary approaches and to enhance the impact of these sort of research on urban planning, environmental education, and citizen’s perceptions. In addition, citizen science could be an excellent tool for improving, both data availability in the long term and social involvement in biodiversity conservation, although educational programs are needed to make citizen data more accurate and useful for scientific research.
The Aburrá Valley with its altitudinal range (1000 to 3000 m.a.s.l.) and its heterogeneous landscape is a good model for evaluating urbanization effects on Northern Andes biodiversity. Nevertheless, taking into account the huge amount of biodiversity and the high rates of endemism and species turnover in this region, it is also necessary to address multiscale studies in other cities, where urban ecology studies are lacking or absent. Also, it is essential to develop theoretical and methodological integrative frameworks applying to the particular biogeographic and socio-political circumstances in the region, which could facilitate the synthesis, interpretation, and application of knowledge in urban ecosystems, and make local policies more effective in the goal of having most sustainable cities.
Finally, in the light of our findings, we would recommend adjusting some urban planning strategies and silvicultural practices in the Metropolitan Area of the Aburrá Valley. Beyond the connectivity framework, the municipalities are already enhancing, identification and evaluation of connectivity networks must include the “urban gradient” paradigm because the “patch-matrix” paradigm tends to exclude the regional context, which in the case of the Aburrá Valley implies to overlook most vulnerable species to urbanization sprawl. Connectivity networks in cities could represent ecological traps for more specialized species without including the urban gradient contexts and the biodiversity patterns of surrounding natural ecosystems. Also, the reforestation programs to implement under connectivity frameworks need to prioritize local native plants and natural regeneration, not only in urban protected parks but also in small urban green spaces (<10ha). The understanding of the city within the local biogeography context is the only way to mitigate the growing conflict between urbanization and biodiversity and to develop a truly sustainable city into the near future.
References cited on the main Introduction
Alberico, M., Saavedra-R, C., García-Paredes, H., 2005. House bats of Cali, Colombia. Caldasia 27, 117–126.
Amador-Oyola, L.A., 2015. Fauna urbana de Guayaquil: el caso de los anfibios y reptiles, nuestros vecinos menospreciados. Yachana Rev. Científica 4, 181–188.
Arteaga, W., 2017. Diversidad de aves del campus universitario de la Universidad Central del Ecuador, Quito. Siembra 4, 172–182.
Barbosa de Toledo, M.C., Donatelli, R.J., Teixeira Batista, G., 2012. Relation between green spaces and bird community structure in an urban area in Southeast Brazil. Urban Ecosyst. 15, 111–131. https://doi.org/10.1007/s11252-011-0195-2
Bibby, C., Jones, M., Marsden, S., 1998. Expedition Field Techniques: Bird Surveys. Expedition Advisory Centre, Royal Geographical Society, London.
Carvajal-Castro, J.D., María Ospina-L, A., Toro-Ló pez, Y., Pulido-G, A., Ximena Cabrera- Casas, L., Guerrero-Peláez, S., Hugo García-Merchá, V., Vargas-Salinas, F., 2019. Birds vs bricks: Patterns of species diversity in response to urbanization in a Neotropical Andean city. PLoS One 14, e0218775. https://doi.org/10.1371/journal.pone.0218775
Castaño-Villa, G.J., Patiño-Zabala, J.C., 2007. The composition of avian communities in fragmented forest in Santa Elena region, Central Colombian Andes. Boletín Científico Mus. Hist. Nat. 11, 47–60.
Chang, H.-Y., Lee, Y.-F., 2016. Effects of area size, heterogeneity, isolation, and disturbances on urban park avifauna in a highly populated tropical city. Urban Ecosyst. 19, 257–274. https://doi.org/10.1007/s11252-015-0481-5
Cincotta, R.P., Wisnewski, J., Engelman, R., 2000. Human population in the biodiversity
114 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
hotspots. Nature 404, 990–992. https://doi.org/10.1038/35010105
Clergeau, P., Croci, S., Jokimäki, J., Kaisanlahti-Jokimäki, M.L., Dinetti, M., 2006. Avifauna homogenisation by urbanisation: Analysis at different European latitudes. Biol. Conserv. 127, 336–344. https://doi.org/10.1016/j.biocon.2005.06.035
Clergeau, P., Savard, J.P.L., Mennechez, G., Falardeau, G., 1998. Bird abundance and diversity along an urban-rural gradient: a comparative study between two cities on different continents. Condor 100, 413–425.
Cohen, J.E., 2003. Human population: the next half century. Science (80-. ). 302, 1172– 1175. https://doi.org/10.1126/science.1088665
Cordero, P., Vanegas, S., Hermida, M.A., 2015. La biodiversidad urbana como síntoma de una ciudad sostenible. Estudio de la zona del Yanuncay en Cuenca, Ecuador. MASKANA 6, 107–130.
Davis, K., 1955. The Origin and Growth of Urbanization in the World. Am. J. Sociol. 60, 429–437.
Delgado-V, C.A., Correa-H, J.C., 2013. Estudios ornitológicos urbanos en Colombia: revisión de literatura (Urban ornithological studies in Colombia: a literature review). Ing. y Cienc. 9, 215–236. https://doi.org/10.17230/ingciecia.9.18.12
Escobar-Ibáñez, J.F., Macgregor-Fors, I., 2016. Peeking into the past to plan the future: Assessing bird species richness in a neotropical city. Urban Ecosyst. 19, 657–667. https://doi.org/10.1007/s11252-015-0517-x
Etter, A., Mcalpine, C., Possingham, H., 2008. Historical Patterns and Drivers of Landscape Change in Colombia since 1500: A Regionalized Spatial Approach. Ann. Assoc. Am. Geogr. 98, 2–23.
Ferenc, M., Sedláček, O., Fuchs, R., Dinetti, M., Fraissinet, M., Storch, D., 2014. Are cities different? Patterns of species richness and beta diversity of urban bird communities and regional species assemblages in Europe. Glob. Ecol. Biogeogr. 23, 479–489. https://doi.org/10.1111/geb.12130
Fernández-Juricic, E., 2000. Local and regional effects of pedestrians of forest birds in a References 115
fragmented landscape. Condor 102, 247–255.
Fernández-Juricic, E., Jokimäki, J., 2001. A habitat island approach to conserving birds in urban landscapes: case studies from southern and northern Europe. Biodivers. Conserv. 10, 2023–2043.
Gutiérrez-Vásquez, C.A., Osorio-Vélez, L.F., 2014. Más bosques para Medellín: sembrando árboles para Medellín. Alcaldía de Medellín, Fundación CIPAV, Medellín.
Jenkins, C.N., Pimm, S.L., Joppa, L.N., 2013. Global patterns of terrestrial vertebrate diversity and conservation. PNAS 2602–2610. https://doi.org/10.1073/pnas.1302251110
Jokimäki, J., Kaisanlahti-Jokimäki, M.L., 2003. Spatial similarity of urban bird communities: a multiscale approach. J. Biogeogr. 30, 1183–1193.
Kowarik, I., 2011. Novel urban ecosystems, biodiversity, and conservation. Environ. Pollut. 159, 1974–1983. https://doi.org/10.1016/j.envpol.2011.02.022
Liu, J., Daily, G.C., Ehrlich, P.R., Luck, G.W., 2003. Effects of household dynamics on resource consumption and biodiversity. Nature 421, 530–533.
Luppi, M., Dondina, O., Orioli, V., Bani, L., 2018. Local and landscape drivers of butterfly richness and abundance in a human-dominated area. Agric. Ecosyst. Environ. 254, 138–148. https://doi.org/10.1016/j.agee.2017.11.020
Malkinson, D., Kopel, D., Wittenberg, L., 2017. From rural-urban gradients to patch – matrix frameworks: Plant diversity patterns in urban landscapes. Landsc. Urban Plan. 169, 260–268. https://doi.org/10.1016/j.landurbplan.2017.09.021
Marín Gómez, O.H., 2005. Avifauna del campus de la Universidad del Quindio (Birds of Quindio University Campus). Boletín SAO 15, 42–60.
Mcdonald, R.I., Kareiva, P., Forman, R.T.T., 2008. The implications of current and future urbanization for global protected areas and biodiversity conservation. Biol. Conserv. 141, 1695–1703. https://doi.org/10.1016/j.biocon.2008.04.025
McDonnell, M.J., 2011. The History of Urban Ecology: An Ecologist’s Perspective, in: Niemelä, J., Breuste, J.H., Elmqvist, T., Guntenspergen, G., James, P., Mcintyre, 116 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
N.E., Mcdonnell, M.J. (Eds.), Urban Ecology. Oxford University Press, Oxford, pp. 5– 13.
McIntyre, N.E., Knowles-Y, K., Hope, D., Knowles-Yánez, K., Hope, D., 2000. Urban ecology as an interdisciplinary field: differences in the use of “urban” between the social and natural sciences. Urban Ecosyst. 4, 5–24.
Mckinney, M.L., 2008. Effects of urbanization on species richness: A review of plants and animals. Urban Ecosyst. 11, 161–176. https://doi.org/10.1007/s11252-007-0045-4
McKinney, M.L., 2006. Urbanization as a major cause of biotic homogenization. Biol. Conserv. 127, 247–260. https://doi.org/10.1016/j.biocon.2005.09.005
Miller, J.R., Hobbs, R.J., 2002. Conservation Where People Live and Work. Conserv. Biol. 16, 330–337.
Muñoz, M.C., Fierro-Calderón, K., Rivera-Gutierrez, H., 2007. Las aves del campus de la universidad del Valle, una isla verde urbana en Cali, Colombia (The birds of the Universidad del Valle campus, a green island in the city of Cali, Colombia). Ornitol. Colomb. 5, 5–20.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Da Fonseca, G.A.B., Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Nielsen, A.B., van den Bosch, M., Maruthaveeran, S., van den Bosch, C.K., 2013. Species richness in urban parks and its drivers: A review of empirical evidence. Urban Ecosyst. https://doi.org/10.1007/s11252-013-0316-1
Niemeï, J., 2014. Ecology of urban green spaces: The way forward in answering major research questions. Landsc. Urban Plan. 125, 298–303. https://doi.org/10.1016/j.landurbplan.2013.07.014
Nolazco, S., 2013. Diversidad de aves silvestres y correlaciones con la cobertura vegetal en parques y jardines de la ciudad de Lima. Editoras, Guzlop, Lima.
Peña-Nuñez, J.L., Claros-Morales, A.F., 2016. Estudio preliminar de la avifauna en el campus de la Universidad de la Amazonia, en Florencia, Caquetá, Colombia. Rev. Biodivers. Neotrop. 6, 85–92. https://doi.org/10.18636/bioneotropical.v6i1.352 References 117
Pickett, S.T.A., Burch Jr., W.R., Dalton, S.E., Foresman, T.W., Grove, J.M., Rowntree, R., Burch, W.R., Dalton, S.E., Foresman, T.W., Grove, J.M., Rowntree, R., 1997. A conceptual framework for the study of human ecosystems in urban areas. Urban Ecosyst. 1, 185–199. https://doi.org/10.1023/A:1018531712889
Pickett, S.T.A., Cadenasso, M.L., 2006. Advancing urban ecological studies: Frameworks, concepts, and results from the Baltimore Ecosystem Study. Austral Ecol. 31, 114– 125. https://doi.org/10.1111/j.1442-9993.2006.01586.x
Ramírez-Cháves, H.E., Pérez, W.A., Mejía-Egas, O., Tobar-Tosse, H.F., Muñoz, A., Trujillo-Lozada, A., 2010. Biodiversidad en el campus de la Universidad del Cauca, Popayán, Colombia. Fac. Ciencias Agropecu. 8, 104–117.
Reis, E., López-Iborra, G.M., Pinheiro, R.T., 2012. Changes in bird species richness through different levels of urbanization: Implications for biodiversity conservation and garden design in Central Brazil. Landsc. Urban Plan. 107, 31–42. https://doi.org/10.1016/j.landurbplan.2012.04.009
Sandström, U.G., Angelstam, P., Mikusiński, G., 2006. Ecological diversity of birds in relation to the structure of urban green space. Landsc. Urban Plan. 77, 39–53. https://doi.org/10.1016/j.landurbplan.2005.01.004
SAO, 2014. Inventario de la diversidad de aves en dos áreas protegidas urbanas del Valle de Aburrá: APU Piamonte - Bello, APU Cerro La Asomadera - Medellín. Medellín.
Savard, J.P.L., Clergeau, P., Mennechez, G., 2000. Biodiversity concepts and urban ecosystems. Landsc. Urban Plan. 48, 131–142. https://doi.org/10.1016/S0169- 2046(00)00037-2
Seto, K.C., Fragkias, M., Gü Neralp, B., Reilly, M.K., 2011. A Meta-Analysis of Global Urban Land Expansion. PLoS One 6. https://doi.org/10.1371/
Smith, T.M., Smith, R.L., 2006. Elements of Ecology, 6th ed. Pearson Education, Inc., San Francisco.
Southon, G.E., Jorgensen, A., Dunnett, N., Hoyle, H., Evans, K.L., 2018. Perceived species-richness in urban green spaces: Cues, accuracy and well- being impacts. 118 Effects of urban green spaces composition and structure on local bird diversity: a study case from a populated city in Colombian Northern Andes
Landsc. Urban Plan. 172, 1–10. https://doi.org/10.1016/j.landurbplan.2017.12.002
Sutherland, W.J., Newton, I., Green, R.E., 2004. Bird Ecology and Conservation: A Handbook of Techniques. Oxford University Press / USA, New York.
Tryjanowski, P., Morelli, F., Mikula, P., Krištín, A., Indykiewicz, P., Grzywaczewski, G., Kronenberg, J., Jerzak, L., 2017. Bird diversity in urban green space: A large-scale analysis of differences between parks and cemeteries in Central Europe. Urban For. Urban Green. 27, 264–271. https://doi.org/10.1016/j.ufug.2017.08.014
Vásquez-Muñoz, J., Castaño-Villa, G., 2008. Identificación de áreas prioritarias para la conservación de la avifauna en la zona urbana del municipio de Medellín, Colombia. Boletín Científico Mus. Hist. Nat. 12, 51–61.
Villarreal, H., Álvarez, M., Córdoba, S., Escobar, F., Fagua, G., Gast, F., Mendoza, H., Ospina, M., Umaña, A., 2004. Manual de métodos para el desarrollo de inventarios de biodiversidad. Programa de inventarios de biodiversidad (Biodiversity inventory methods). Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá, D.C., Colombia.
Vitousek, P.M., Mooney, H.A., Lubchenco, J., Melillo, J.M., 1997. Human Domination of Earth’s Ecosystems. Science (80-. ). 277, 494–499.
Wolch, J.R., Byrne, J., Newell, J.P., 2014. Urban green space, public health, and environmental justice: The challenge of making cities “just green enough.” Landsc. Urban Plan. 125, 234–244. https://doi.org/10.1016/j.landurbplan.2014.01.017
Xie, S., Lu, F., Cao, L., Zhou, W., Ouyang, Z., 2016. Multi-scale factors influencing the characteristics of avian communities in urban parks across Beijing during the breeding season. Sci. Rep. 6, 1–9. https://doi.org/10.1038/srep29350
Zipperer, W.C., Wu, J., Pouyat, R. V, Pickett, S.T.A., 2000. The Application of Ecological Principles to Urban and Urbanizing Landscapes. Ecol. Appl. 10, 685–688.