Urban ecology and biological studies in Brazilian cities: a systematic review

The number of papers focusing on ecological interactions in urban environments has increased in recent years. This review aimed to address the panorama of urban ecology and biological surveys in Brazil. A systematic search was carried out using the Web of Science and Scopus platforms for papers on urban ecology to understand which institutions, authors, themes, cities, biomes, states, and regions have addressed the theme in Brazil to date. A total of 932 articles were found, in 196 scientific journals. Most papers were published between 2010 and 2019. This involved 350 municipalities in the five Brazilian regions, with Curitiba, São Paulo, and Rio de Janeiro being the municipalities with the most papers. São Paulo was the state that presented the most papers, with 23.7% of the total, and the Southeast region was the most representative with 36.6%. The biome with the highest concentration of papers (61.2%) was the Atlantic Forest. A total of 2537 authors were registered, affiliated with a total of 413 institutions from 19 countries. The institutions with the most papers were the Federal University of Paraná and University of São Paulo. The most discussed topic was related to botany (69%), and the most used keyword was “urban afforestation”. The number of papers published was greater in municipalities with higher human development index, number of inhabitants and relative urbanized area. This review revealed the scarcity of studies in low-income areas, and the need for greater incorporation of the social aspect, landscape ecology and ecological interactions in urban ecology.


Introduction
The gradual increase in human population culminates in greater urbanization, in turn, leads to biotic and abiotic transformations on the planet (Pickett et al. 2001). Such transformations, as intensive land use, use of natural resources, formation of heat islands and vegetation fragmentation, modify the urban landscape unevenly (Grise et al. 2016), leading cities to a major political-sanitary crisis (Martinez-Alier 2018). Considering that there are both ecological and social aspects that compose the urban environment, in order to reduce such inequalities, the study of urban ecology is emerging (Cadenasso et al. 2006;Niemelä al. 2011).
As a multidisciplinary science, urban ecology seeks to integrate ecological and social knowledge with other fields of study (Grimm et al. 2000(Grimm et al. , 2008(Grimm et al. , 2013Boone and Fragkias 2012;Childers et al. 2015), such as urban planning, natural resource management, economics, among others (McPhearson 1 3 et al. 2016a, b) as presenting cities as complex, highly interactive social ecosystems (Alberti 2008). Through it, the ecological patterns and processes that act in urban ecosystems are identified (McDonnell 2011). In addition, urban ecology studies the interactions between organisms, the built structures that make up cities, and social attributes such as lifestyle, economic, and political processes, which interact and influence the physical environment (Cadenasso et al. 2006;Grimm et al. 2008;Collins et al. 2011;Forman 2014).
Urban ecology research has grown rapidly across the world over the past two decades, in both research and practice. Pioneering research has been conducted in Europe and Asia (Kowarik 2005;Sukkopp 2008;Wu et al. 2014;Collins et al. 2011), and in Brazil, there has been a clear trend of expansion (de Camargo Barbosa et al. 2021). In this sense, studies carried out in Brazilian cities can contribute to better planning of green areas by showing the wide use of exotic tree species (Moro and Castro 2015), their impact on native fauna (de Camargo Barbosa et al. 2021), the potential afforestation as ecological corridors (Freitas et al. 2020), and the uneven distribution of green areas across cities (Sartori et al. 2019;. Therefore, in view of the role of urban ecology for human well-being, reduction of socio-environmental inequalities (Porto and Martinez-Alier 2007) and conservation of biodiversity (Brun et al. 2007;Almeida et al. 2018) a diagnosis of how Urban Ecology has been approached is fundamental. To this end, carry out a survey of the most studied fields, where the research is being carried out and the main results obtained and, consequently, if there is a concentration of studies in specific regions. With this, contribute to a better distribution of public investments, seeking socio-environmental equality and biodiversity gain. To this end, this article proposes the first integrative review of urban ecology and related papers in Brazil and seeks to answer the following questions: i) What is the current panorama of urban ecology in Brazil? ii) Which are the most studied themes in this area? iii) Does the socio-economic aspect of regions directly affect the number of publications in the area of urban ecology? and iv) Which are the traits of municipalities linked to the highest number of publications?

Literature search
We consider that the term "urban ecology" includes not only articles developed purely in the scope of ecology, but also everything that surrounds it, such as wildlife ecology, as well as economic and social research linked to green areas and landscape analysis. We performed a systematic search for articles as suggested by Page et al. (2021) (i.e., PRISMA statement) (Fig. 1). The searches were carried out in the Web of Science, SciELO, and Google Scholar databases. The bibliographic survey was carried out in March 2020 and did not limit publications by year.
From the initial survey of articles, we created a list of the journals with the greatest coverage of the topic and the most cited authors. Therefore, further searches were carried out for papers in the journals with most articles, considering articles accepted until 2019. Articles were also searched in the Curriculum Vitae of the most cited authors, to ensure that no article had been excluded.
After the removal of duplicate records, the remaining records were analyzed, and the following inclusion criteria were applied: (i) articles focused on urban ecology, (ii) studies were carried out in Brazil, and (iii) studies were located in urban and peri-urban areas.

Data collection
From the articles obtained in the bibliographic survey, the following data were collected: A) Study Location; B) Central theme and subthemes; C) Paper information. Regional data (D) were obtained a posteriori from the list of cities using IBGE data (IBGE 2021). The data collected is described in detail in Table 1. To be accepted in the present review, the only guideline was that the paper had to be conducted within cities and in relation to living beings.
Most data included in the biome category included urban field sites such as urban green areas. Urban green areas are defined as forest fragments, urban trees, and squares. Biome classification used here was according to Coutinho (2006), who define biome as a "set of life (vegetable and animal) constituted by the grouping of contiguous and identifiable vegetation types on a regional scale, with similar geoclimatic conditions and history shared change, resulting in a biological diversity of its own." With this, six biomes were described for Brazil: Atlantic Forest, Cerrado, Amazon, Caatinga, Pampas, and Pantanal.

Data analysis
Data was compiled and analyzed using Microsoft Excel software. The R program (R Core Team 2021) was used through the base package for the construction of graphs and the ggplot2 and ggspatial packages for the construction of the map. For the analysis between the social data of the municipalities and the publications, a spearman correlation was performed using the R base package.

Results
A total of 1209 scientific articles were collected from the search engines. In the first selection, articles that did not fit were removed, and a selection was made by the authors, leaving 932 articles belonging to 181 scientific journals ( Fig. 1; Complementary Table S1). The journals with the most published articles were Revista Brasileira de Arborização Urbana with 311 articles (33.4%), followed by Biotemas with (5.7%), Revista Árvore (4.3), Revista Brasileira de Geografia Física (3.6%), Ciência Florestal (3%), Biota Neotropica (2.6%) and Urban Ecosystems (2.6%). Of the scientific journals, 15 presented more than 10 scientific articles, representing 68.2% of the total.
Most of the articles (75.2%) were published between 2010 and 2019. Between 2000 and 2009, 23.6% were published, and finally, from 1990 to 1999, 1.1% were published ( Fig. 2A). Only one article was found in digital format between 1980 and 1989. Between the years 2017 and 2019, the highest number of articles was published, representing 9.44% and 9.12% of the total, respectively. These years were followed by 2018, 2010, and 2016 (Fig. 2B).
The reviewed papers were carried out in 350 municipalities, representing 6.3% of Brazilian municipalities (Instituto Brasileiro De Geografia E Estatística 2021) (Complementary Table S2). Most of the publications (88%) were carried out in only one location. Papers in more than one location accounted for 5.2%, ranging from two to 50 municipalities. Theoretical papers (not related, therefore, to any specific location) corresponded to 6.8% of the total.
The regions with the highest number of municipalities with published papers were the Southeast, with 36.6% of the total, followed by the South (26.3%), Northeast (16.6%), Central-West (11.4%) and North (9.1%). Proportional to the total number of municipalities in the region, the Central-West had 8.6% of the municipalities represented, followed by the Southeast and South with 7.7% each, the North with 7.1% and the Northeast with 3.2%. As for the Brazilian regions, the Southeast represents 42.3% of the papers, followed by the South (25.8%), Northeast (14.5%), North (8.9%) and Central-West (8.5%) ( Table 2). Considering that Brazil is a country of extreme inequality, and most of its population, GDB and academic institutions are in the Southeast, a higher concentration of papers in this region was expected. Regions with less economic productivity are also the least researched when it comes to urban ecology.
Among the biomes, 61.2% of the reviewed papers were carried out in municipalities located in the Atlantic Forest, 20.8% were carried out in the Cerrado, 8.3% in the Amazon, 1 3 5.3% in the Caatinga, 4.3% in the Pampas, and only 0.2% in the Pantanal. Papers carried out in only one biome added up to 82.4% of the total, while papers carried out in more than one biome, meaning those also carried out in more than one municipality, added up to 17.6%. Of these, 17% were developed in two biomes, 0.34% in three biomes, and only one paper presented four biomes. Most of those focused on two biomes included the Atlantic Forest (Fig. 4a, b).
We found 2537 authors from 932 reviewed papers (Complementary Table S3). The number of authors in each of the reviewed papers varies from one to 32, and the values decreased as the number of authors increased. The most common number of authors per paper was three (24.5% of articles), followed by two (21.5%), and four authors (18.3%). Papers with 10 authors or more represented 3.6% of the total (Fig. 5a, b).
The authors are affiliated with 413 institutions, located in 19 countries. Brazil's largest research partners were the United States, Germany, England, and Spain. Brazilian institutions were responsible for 95% of registered institutions. The institutions with the highest number of published articles were the UFPR, University of São Paulo (USP), Federal University of Uberlândia (UFU) and ESALQ. Institutions with only one record accounted for 62.3% of the total, while institutions with two papers accounted for 12.8%. Only 7.7% of institutions had more than 10 records (Complementary Table S4). Among the universities that stood out, only one is not public, this As for the topics covered in the articles, those with the highest incidence were Botany (68.6%) and Zoology (34.9%), followed by Social (33%), Ecology (13%), Landscape (12.4%), Theoretical (10.8%), and Environment (7.3%). Botany, the subject that has the largest number of papers published, was divided into six sub-themes, with floristic surveys being the main sub-theme with 32% of the total. As for social issues, the most discussed sub-themes were related to society (21.5%), the economy (5.5%) and public management (2.2%). As for zoology, the reviewed papers were classified into 15 sub-themes, and papers on invertebrates (10.6%), birds (6.9%), and mammals (6.7%) were the most abundant (Table 3; Fig. 6).
We found 1915 keywords used in the reviewed articles. Words used only once accounted for 76% of the total. The words that appeared more often were: "Urban afforestation," "Urban planning," "Green areas," "Urban ecology," "Urban ecology," "Afforestation," "Urban trees," "Exotic species," "Inventory," and "Urban forestry". Table 4 shows the 20 most-used keywords.
Regarding the attributes of municipalities acquired through the IBGE data platform, when only municipalities with five or more reviewed papers were observed, the variables that showed a significant correlation with the number Fig. 4 Most representative biomes in terms of the percentage of published articles on urban ecology and the percentage of area that the biome occupies in the country of publications were HDI, number of inhabitants, and percentage of urbanized area (Table 5). The total area of the municipality and percentage of afforestation of public roads did not correlate with the number of published articles.

Discussion
Ecology is a branch of science that was initially dedicated to rural areas with little human influence (Grimm et al. 2008). However, with the increase in urban populations and the increasing alteration of natural landscapes, new studies have also begun to be conducted in urban environments (Ramalho and Robbs 2012). Urban ecology was established in Brazil during the 1970s (Noyes and Progulske 1974;Sukopp 1998;Grimm et al. 2008), with an emphasis on purely biological research, ignoring the social aspect (Wu et al. 2014). In recent years, there has been interest in researching the relationship between ecological, socioeconomic, and cultural attributes of urban centers (Ramalho and Hobbs 2012;Shackleton et al. 2021).
This increase may be related to the growing concern of societies about the environment, which is a global trend in countries such as China (Yao et  Most of the articles found in this review focus on urban Botany. The attention given to urban afforestation can be explained by the "luxury effect" (Hope et al. 2003), that is, the tendency of neighborhoods and cities with high socioeconomic standards to be "greener" and to present a more biodiverse flora. Another important aspect is the immediate and measurable benefits of afforestation (Sartori et. al 2021), which could promote greater interest in this area of study. It is also relatively easier to study plants as a proxy for urban ecology benefits in biodiversity, socioeconomic wellbeing and ecosystem services provision, when compared to other study focuses. Davis et al. (2011), for example, demonstrated the possibility of reducing carbon emissions by 80% with afforestation of streets and backyards in the city of Leicester, England. Jones (2021) reported an increasing improvement in the quality of life of New York residents with each tree planted. In addition, health improvements in the population due to the increase in air quality (Jones and McDermott 2018) and climate mitigation (Martini et al. 1 3 2017) result from investment in biodiverse and abundant urban afforestation. The studies analyzed a combination of socioeconomic aspects, human well-being, and biodiversity. More such efforts are needed to achieve transdisciplinary research in urban ecology. Brazilian journals focusing on botany have the highest number of records, as indicated by the Revista da Sociedade Brasileira de Arborização Urbana (REVSBAU), with onethird of the articles published. In addition, there are a significant number of records published in botanical journals such as Rodriguésia, Cerne, Árvore, and Revista da Sociedade Brasileira de Botânica, in addition to REVSBAU. Once again, this is due to the fact that papers focused on plant biology have a greater tradition, especially those focused on urban afforestation. Studies involving fauna and human health in the context of urban ecology are more recent and sporadic; therefore, journals that publish these themes were less frequent in the present review. Furthermore, we can see that 92% of journals published less than ten times on urban ecology.
Despite growth, areas such as landscape ecology, environment, and ecology are rarely addressed in urban ecology, and this is emphasized by the use of the keyword "urban ecology" in recent years. The importance of landscape ecology, for example, is expressed by the potential of the afforestation of streets and avenues to connect urban forest fragments (Brun et al. 2007). Understanding the relationship between the isolation of urban green areas, the behavioral characteristics of the fauna in these fragments, and the role of street afforestation as ecological corridors is essential to make cities a shelter for biodiversity (Soares and Lentini 2019). Landscape ecology allows an integrated look at spatial heterogeneity on the ecological scale: ecosystem, community, and population (Metzger 2001).
The context of the word "ecology" is broad and needs to be understood within the scope of species and the relationships between them. Thus, we consider that surveys, economic, and social studies are equally important for the understanding of this subject. The papers incorporated in the theme of "environment" ("climate," "soil," "acoustics," and "water") and "ecology" ("ecosystem services," "restoration," "ecological interactions," and "conservation") proved to be little-addressed in the urban ecology theme. As being transdisciplinary is one of the objectives of urban ecology (Young and Wolf 2006), it is essential to further study these themes, which directly affect the human population. The urgency of this inclusion is highlighted when we observe the key role played by afforestation of urban roads in noise attenuation (Oliveira et al. 2018), the role of green areas in greater thermal comfort (Tejas et al. 2011), water regulation in cities, and carbon sequestration (Almeida et al. 2018).
The main universities are in the cities of Curitiba and São Paulo, both with a significant population and a high HDI (IBGE 2021). This relationship between socioeconomic factors and publications shows a pattern: municipalities with a higher HDI present more research in urban ecology. At the same time, this shows that the scarcity of studies, access to green areas, and ecosystem services mainly affect marginalized populations (Porto and Martinez-Alier 2007). These populations are often exposed to greater risks of flooding (Pontes et al. 2017) and live in precarious housing in "sacrifice zones" (Bullard 1994;Santos 2019). In addition, low-income populations, which are already in environmentally unstable areas, will be the most affected by climate change, according to the Intergovernmental Panel on Climate Change (IPCC) climate report (2021).
This review shows the spatial heterogeneity in urban ecology research in Brazil. It is clear that the municipalities with highest HDI and urban population density are the most researched, while the others are overlooked. This is likely linked to the concentration of research institutes and universities in these municipalities. However, this result evidences the environmental injustice still predominant in the country (Costa 2018). Rich states and municipalities present numerous urban green areas and tree-lined streets, while poor communities are denied these spaces (Schwarz et al. 2015;Gould and Lewis 2016;Rigolon et al. 2018). Similarly, urban ecology research in Brazil focuses on already developed and biodiverse sites, disregarding marginalized communities, Schell et al (2020) defined this process like a "environmental racism". Even though research in urban ecology is becoming increasingly popular, future research must focus on these underprivileged areas. Poor municipalities are also more vulnerable to environmental degradation, pollution, deforestation, and natural disasters, including landslides and flooding (de Loyola Hummell et al. 2016;Rasch 2017;Debortoli et al. 2017;). Research on urban ecology is essential to assess the present state of degradation in these areas, and propose better city planning (Pickett et al. 2014;Childers et al. 2015;McPhearson et al. 2016a, b). Only through detailed research can we uncover the ongoing issues in urban areas and create solutions for a better quality of life, for the people and for the biodiversity that coexist in the cities.
In addition to municipalities, the results showed a great disparity between states and regions in terms of the number of articles published. The South and Southeast regions were responsible for 63% of published papers, despite having an area of less than 20% of the national territory. These are also the most developed states with a longer tradition of urban research universities.
The Atlantic Forest, despite occupying only 15% of the national territory, is where 70% of the population and 60% of Brazilian municipalities are concentrated (IBGE 2021). This region houses the main universities and researchers, thus being the most studied region in the country in terms of urban ecology. At the same time, in the Cerrado and in the Amazon, the number of reviewed papers is related to the population that occupies these areas, and not to the territorial area. For example, the Amazon occupies about 50% of the national territory, and is responsible for only 8% of the papers, proportional to the population of the biome.
The studies reflect the reality in Brazil. Municipalities with more universities and researchers have more research in the area, even more whith the consolidated line and a group of researchers in urban ecology. We were also able to present the need for research in biomes such as the Caatinga, the Amazon and the Pantanal. We believe that with the results presented we can show bottlenecks for future research.

Final considerations
With this review, we present a panorama of publications focused on urban ecology in Brazil. Our study revealed the growing interest and importance of ecology in Brazil, as demonstrated by the increase in publications on the topic over the last few decades. However, these papers are still concentrated in the major areas of biological sciences (i.e., botany and zoology), with an emphasis on research on urban afforestation and surveys of urban fauna, especially birds and insects. Thus, we emphasize the knowledge gap in studies that intrinsically relate ecology and society, approach the ecology of landscape in the urban environment, or focus on ecology as research into the interaction between fauna and flora in the urban environment, as well as essential knowledge for the conservation of these species.
We found that the universities that publish the most on this subject are in Curitiba and São Paulo, which represent the relationship between cities with a dense population, higher HDI, and a greater representation of publications related to urban ecology. Our results highlight the scarcity of studies on the subject in regions other than the southern and southeastern regions of the country. It is expected that the number of papers will increase over time, with a greater concentration of frequent authors currently starting their studies in this line of research.