Time for a change: dynamic urban ecology

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Time for a change: dynamic urban ecology Cristina E. Ramalho and Richard J. Hobbs School of Plant Biology (M090), The University of Western Australia, 35 Stirling Highway, Crawley, Perth, WA 6009, Australia

Contemporary cities are expanding rapidly in a spatially complex, non-linear manner. However, this form of expansion is rarely taken into account in the way that urbanization is classically assessed in ecological studies. An explicit consideration of the temporal dynamics, although frequently missing, is crucial in order to understand the effects of urbanization on biodiversity and ecosystem functioning in rapidly urbanizing landscapes. In particular, a temporal perspective highlights the importance of land-use legacies and transient dynamics in the response of biodiversity to environmental change. Here, we outline the essential elements of an emerging framework for urban ecology that incorporates the characteristics of contemporary urbanization and thus empowers ecologists to understand and intervene in the planning and management of cities. Challenges for urban ecology in a rapidly urbanizing world Not only is the world experiencing an unprecedented urban transition [1,2], but contemporary urbanization also differs markedly from historical patterns of urban growth [3] (Box 1), thus imprinting a unique signature on contemporary cities (Figure 1). Indeed, such cities are largely young urban landscapes that have expanded rapidly over the course of the major urban transition that started in 1950 and that has accelerated steeply over the past 10–20 years [3]. Importantly, contemporary cities are increasingly expansive and dispersed landscapes [3,4], which grow and age in a spatially complex, non-linear manner [5]. Consequently, they display multifaceted patterns of variable density across space and time, in which high density built-up areas can be finely interspersed with lower density, rural and natural areas [3,6]. By contrast, historically developed cities are contained areas that grew slowly, over several centuries or decades, in a relatively linear manner, through concentric and compact rings of development [3]. Contemporary urbanization has major implications for the ecology of cities, requiring ecologists to acknowledge the phenomenon actively in terms of the ways that they intervene in, and study, cities. As cities expand, protected areas that are currently outside city boundaries will soon become embedded in urban landscapes [4,7–9]. Furthermore, other natural areas and previously managed land with conservation value (e.g. old fields) will be largely reduced to small and scattered urban remnants. Whereas cities were previously relatively Corresponding author: Ramalho, C.E. ([email protected])

confined spaces and therefore conservation of remnant ecosystems within their boundaries was not a priority, this is no longer the reality. In fact, the conservation of urban remnant ecosystems will become increasingly important for several reasons. First, especially in areas with high beta-diversity, remnants provide the only remaining habitat for many species [10]. Second, they provide ecosystem services (e.g. water infiltration, microclimatic amelioration, sequestration of air pollutants, recreation and esthetics) that improve the urban environment and enhance the wellbeing and quality of life of urban dwellers [11–13]. Third, urban remnants are the primary connection that many humans have to the natural world [14]. Preventing the extinction of this experience [15] is important for conservation far beyond city boundaries [16]. Urban ecological research is largely framed by a conceptual approach that assumes that urbanization and its induced environmental changes decrease in a linear gradient from the core to the city fringes [17]. This assumption, as well as oversimplifying urban environments [6,18], does not fit with the non-linear and complex growth of contemporary cities. Equally important, a static approach neglecting the young and rapidly evolving nature of those landscapes (and consequent ecological implications) is predominant across current urban ecology frameworks. This might result from a slow recognition of the unprecedented spatial and temporal scale of contemporary urbanization [19]. Regardless of its cause, this mismatch has major consequences for the scope of urban ecological research and calls for an urgent revision of the way in which urbanization is assessed in ecological studies. Here, we review how urbanization is evaluated in ecological studies. We identify key drawbacks of current conceptual frameworks, emphasizing the misleading assumptions of linear variation in urbanization intensity and age, the simplification of the set of intervening drivers and the lack of a temporal approach. We then propose an emergent framework for urban ecology: the Dynamic Urban Framework. This incorporates an explicit temporal perspective that considers land-use legacies and timelagged ecological responses to ongoing environmental change. Furthermore, it includes a conceptual and analytical structure in which relationships between intervening drivers can be analyzed in a mechanistic manner. Here, it focuses on remnant ecosystems, but is extendable to other components of the urban environment. Finally, the framework can be incorporated or used in conjunction with other conceptual frameworks with a stronger multidisciplinary focus [20,21]. It is time for a change in the way in which

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Box 1. A rapidly urbanizing world

Box 2. Lost in translation

Since 2008, for the first time more than half of the human population of the world (3.3 billion) lives in urban areas and this number is expected to reach 5 billion by 2030 [1]. This figure reflects an unprecedented urban transition, with characteristics that are different from any other moment in history. In a thorough recent review [3], it was shown that contemporary urbanization differs markedly from historical patterns of urban growth in terms of scale, rate, location and form. First, the scale and rate of urban expansion, both in terms of population growth and land-cover change, are extraordinary. For instance, between 2000 and 2030 middle-sized cities with populations of 500 000 to 1 million are expected to triple their area [2]. Second, the location of urbanization is shifting. Indeed, whereas the first urban transition (1750–1950) took place in Europe and North America, increasing their urban population from 15 million to 423 million, the second urban transition (1950–2030) is happening largely in Africa and Asia and will increase their urban population from 309 million to 3.9 billion in only 80 years [2,91]. By 2030, these countries will contain 80% of the world urban population. Third, the shape of the cities has changed. Whereas historical cities were contained and well-defined areas that grew through concentric rings surrounding a dense urban core, contemporary cities are no longer sharply defined and are increasingly dispersed and expansive [3]. Furthermore, the patterns of urban sprawl differ between countries. Indeed, in places such as the USA and Australia, suburbanization is predominant and consists of single-family residential development. In developing countries and some European cities, sprawl occurs predominantly through periurbanization, a more disordered development that expands along urban corridors spreading out from metropolitan regions and incorporating small towns and rural areas [3].

Several terms and urbanization measures originating from social sciences, geography and urban planning are widespread in the ecological literature and have been adopted in core research aspects, such as study design. However, these are often used without a critical assessment of their ecological meaning [92] or of whether they reflect the actual range of disturbance to which ecosystems are exposed in the study context. Urban ecological research is hence wedded to broad, vague terms and measures of urbanization, which impedes ecologists from gaining a more mechanistic understanding of the ecology of cities. The problem above might result from two reasons. First, urban ecology has had its major methodological and conceptual development in social sciences, geography and urban planning, and has only recently emerged in mainstream ecological research [44,93]. Consequently, relevant bodies of knowledge from those fields might have been poorly transferred into ecological language and focus. This has the pernicious consequence that recent advances in the other fields are little recognized in urban ecological research. For instance, whereas the spatial and temporal complexity of cities is comprehensively acknowledged in urban planning (e.g. [94]), ecological studies still approach those characteristics in a rudimentary way. There is therefore a gap between fields, and important considerations get lost in translation. Second, the use of broad urbanization terms and measures has been promoted as a common platform for data collection and integration across different fields and in comparative studies [18,95]. However, it is almost impossible to determine the definition of single terms or a set of urbanization metrics that are universally applicable [96,97]. The quest for integration in such a multidisciplinary field is important, but must happen in parallel with the development of specific and ecologically driven vocabulary, concepts and theories.

ecologists view, study and intervene in cities, so that they can have a more active and positive role in the planning and management of the places in which most humans now live. Conceptual frameworks in urban ecology The urban-to-rural gradient framework The urban-to-rural gradient approach [17] has framed most ecological studies analyzing the effects of urbanization on biodiversity and ecosystem functioning [18,22,23]. For example, it aided in the understanding of how species richness varies across urban–rural gradients [22,24] and in response to important urbanization drivers, such as population density [25]. This framework views cities predominantly as monocentric or sometimes polycentric agglomerations that grow through concentric rings surrounding a dense urban core [26]. Most importantly, the framework assumes that urbanization and its induced environmental changes vary along linear gradients between the urban core and the peripheral rural matrix [6]. These include changes in land cover, species assemblages, the chemical and physical environment, and disturbance regimes [26]. Framed by the urban-to-rural gradient, urbanization is depicted and assessed in ecological studies in two main ways [18,26]. A first group of studies simply uses broad zoning categories that are defined subjectively based on the general landscape context [27] or along a geographical transect [28] (Box 2). Such studies compare responses between sites located in, for instance, urban, suburban and rural areas [29]; urban, rural and natural areas [27], or city centre, city edge and peri-urban areas [30]. Alternatively, linear distance to the city centre has been 180

used as a precise measure of the gradient [31]. A second group of studies combines gradient analysis with landscape metrics [32,33] and/or land-use types [34]. In the first case, census, cartography and remote-sensing data are used to quantify socio-economic, land cover, land use and built infrastructure variables in or around the study sites. These variables are used individually or aggregated as proxies to characterize the degree of urbanization. Commonly used metrics measure population density [32], income [35,36], percentage of impervious surface [37], housing [38] and road density [31]. This approach has recently featured in studies aiming to define standardized measures of urbanization to be used in comparative studies [26,39]. Other frameworks Other conceptual frameworks have been proposed in urban ecology, whose use has been restricted to a few specific case studies [20,21,40]. These frameworks are strongly based on the integration of social and environmental sciences. Importantly, they have an ecosystem focus, exploring the links between human and biophysical drivers, patterns and processes, to understand the relationships between urbanization and ecosystem functioning. The Human Ecosystem Model [40,41] is strongly rooted in social sciences and, together with the hierarchical patch dynamics framework [42] and watershed models [43], provides the conceptual and analytical core for the urban Long-term Ecosystem Research (LTER) projects in Baltimore and Central Arizona-Phoenix [44,45]. Other frameworks include the Human Modification Framework [18], the

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Figure 1. Contemporary cities. Aerial perspectives of Chicago (a,b) and Houston, USA (c,d) illustrating how contemporary urbanization imprints a unique signature on cities. Contemporary cities are largely young and rapidly evolving urban landscapes that have expanded dramatically over the past few decades, during the second major world urban transition. These cities no longer have a compact development, but instead are highly expansive and dispersed, sprawling in fractal or spider-like configurations [5], and embedding functioning or decaying fragments of other land uses (e.g. agriculture, forestry or remnant vegetation) in the rapidly changing matrix. The complex spatial patterns of urban growth reflect not only past landscape configurations, but also current socioeconomic and political processes, such as planning, transportation costs, agglomeration economies and market prices [3]. Reproduced with permission from R. Hobbs (a,b) and C.E. Ramalho (c,d).

Multidimensional Biocomplexity Framework [46] and the emerging framework based on the LTER Baltimore Ecosystem Study [47]. Limits to current approaches Linear gradients do not fit with the characteristics of contemporary cities Urban-to-rural gradient studies oversimplify cities [6,18]. Initially, this simplification was important in developing an understanding of these highly complex human-modified ecosystems. However, the underlying assumption of a linear gradient in the urbanization-induced environmental changes does not fit with the spatial-temporal characteristics of contemporary urbanization. Indeed, the fact that contemporary cities grow in a rapid, complex, non-linear, dispersed and expansive manner, means that urbanization intensifies and ages in patchy and complex spatial patterns across the landscape, rather than in a linear gradient (Figure 1). Consequently, the environmental or ecological conditions in one focal remnant patch depend not on its position along the linear gradient, but on the characteristics of the neighboring patches. In a similar way, remnants closer to the city have not necessarily been isolated for longer than remnants in rural areas, and remnants

close to each other might have been isolated for different lengths of time (Figure 2). This means that the use of categorical or quantitative measures of geographical linear distance in urban ecological studies can be ambiguous and misleading. Simplification of the set of intervening drivers Urban-to-rural gradient studies using landscape metrics and/or urban land-use types can partially capture some of the non-linear heterogeneity and complexity of cities. Nevertheless, these studies still oversimplify urban environments, as they often ‘flatten’ several human and environmental drivers into a reduced number of aggregated variables used in study design and data analysis [6,18,21], although there are a few exceptions [35,36,48]. The aggregated representation of drivers does not fully encapsulate the complex dynamics in urban ecosystems, because it neglects the role of a broader set of drivers and their interactions affecting remnant biodiversity and ecosystem functioning. These drivers include, for instance, landscape fragmentation, disturbance regimes, local environmental conditions and the features of the local environment that are not affected by urbanization. Biotic responses to environmental changes associated with 181

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Figure 2. Urban growth is a dynamic process in space and time. Traditional approaches measuring the degree of urbanization in study sites often neglect the temporal dynamics of landscape change, with only the most recent spatial configuration and surrounding land uses taken into account. This approach provides only a snapshot in which all the dynamics that led to that captured spatial moment are neglected, severely limiting understanding into the past and future. In this figure, the landscape context and spatial configuration of four different remnants (a–d) are represented along a period of 30 years. A ‘snapshot’ approach taken at the current time would classify these remnants in the same category. However, their trajectories of landscape change show that the intensity of exposure through edge effects to the disturbance processes originating in the surrounding urbanized areas is different in the four cases. While remnant (a) has been isolated for 30 years, with the same spatial configuration, remnant (b) has only recently had its area reduced to the same size and, in the near past, was part of a much larger and continuous remnant. This means that, in remnant (a), the sampling site has been highly exposed through edge effects to the urban disturbance processes from the immediate vicinity, and is probably highly degraded, unless it has been targeted by management and restoration efforts. In remnant (b), the exposure to an edge is relatively recent, and communities in the sampling site might or might not already exhibit an altered composition and structure owing to the current spatial configuration. Whereas in (a) and (b) the major driver of landscape fragmentation was urbanization, in remnants (c) and (d), the major driver was agriculture. This means, first, that the isolation history of the remnant could be much older and, second, that both (c) and (d) have been exposed for a long time to an agriculture matrix and its disturbance processes, only recently being exposed to urbanization. Solely considering the current landscape context means that land-use legacies from the surrounding agricultural matrix prior to the onset of urbanization are missed.

urbanization might be masked if such factors are ignored [49]. In fact, the action and interaction of multiple drivers, including those that are unique to cities, is responsible for different processes and dynamics of disturbance [19,50] that can even decouple fundamental ecological mechanisms [51]. Predator–prey relationships can break down because synanthropic predators become strongly subsidized by anthropogenic resources [52]. Urban species assemblages can also be determined mainly by stochastic processes rather than by mechanisms such as interspecific competition [53,54]. For these reasons, single or simple combinations of aggregated urbanization measures must be used with caution, and an explicit quantification of the 182

intervening drivers and their interactions is required. The absence of such an approach limits the capacity to understand and forecast the effects of urbanization on remnant biodiversity and ecosystem functioning, as well as their combined effects with other global change drivers, such as climate change [55,56]. Moreover, it diminishes the ability to provide ecologically derived guidelines for management and restoration [10,57]. Other frameworks [20,21,40] are generally based on a comprehensive set of human and biophysical drivers. However, the focus on social sciences, and ecosystem processes and functions rather than on biodiversity dynamics has reduced the ecological utility of those frameworks and

Review might explain their lack of application in urban ecological studies. This simplification is not problematic in the study of human-created and highly managed habitats (e.g. parks, lawns, or green roofs). However, it becomes relevant if applied to remnant ecosystems, as aspects such as fragmentation and associated direct and indirect effects on biodiversity are not properly accounted for. Lack of a temporal perspective Another major limitation of current conceptual frameworks is the absence of an explicit temporal perspective. Although the importance of temporal dynamics is well recognized in ecology [58–61], this has been incorporated less well into the study of cities. However, urbanization age [35,36,62,63], time-lagged social factors [47,64], the development history of the cities [65] and their agrarian legacies [66] have all been shown to be important factors in determining current urban biodiversity and ecosystem patterns. The importance of a temporal perspective An explicit temporal perspective in the study of contemporary cities is crucial for several reasons. First, cities are highly dynamic landscapes and, therefore, a dynamic approach is required to study them. Indeed, the configuration, composition and function of patches in the urban mosaic are dynamic. For example, as urban growth occurs through infilling, scattered remnant vegetation is cleared in stages, sometimes over several decades, as different suburbs are developed. Moreover, vegetation condition in parks and reserves changes as a consequence of natural and human-driven disturbance regimes and restoration efforts, which vary across time, influenced by climatic and socio-economic drivers [67]. Backyard species composition and structure also change, influenced by gardening practices and fashions, and local socio-economic drivers [64,67,68]. Furthermore, as urban populations and demand for land increase, block subdivision and demolition for higher density construction also increase. Finally, cities can ‘shrink’ because of population loss, employment decline and/or economic downturns, which can result in the passive or forced abandonment of entire neighborhoods, and commercial and industrial areas, a phenomenon called ‘deurbanization’ [69]. Second, contemporary cities are young and rapidly evolving landscapes [70] that have been through recent large-scale habitat destruction and land-use changes. In such emergent landscapes, remnant ecosystems are likely to be strongly shaped by past land uses [71], and time-lags might mask remnant biodiversity response to ongoing fragmentation and environmental change [60,65,72,73]. Considering these two aspects is of major importance to the understanding of biodiversity patterns and processes (e.g., invasion and extinction) in rapidly urbanizing landscapes. Land-use legacies Past land use can affect ecological systems with lasting legacies that persist over time, sometimes for hundreds to thousands of years [74,75]. These effects can remain even after land-use change and after other more recent disturbance processes begin operating [66,71,76]. Depending on

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the land use within and surrounding remnant ecosystems prior to urbanization (e.g. agriculture, livestock grazing, or industrial activities), there might be legacies that influence current biotic and/or abiotic ecosystem components. For instance, in expanding European cities, the biodiversity in newly formed urban remnants might have been reduced long before urbanization owing to historical agricultural land uses [65]. Agrarian legacies can also affect urban remnants soils. In Arizona, for example, residential yards converted from farms had double the organic matter, nitrogen and phosphorus than yards converted from native desert [66]. Time-lagged responses to fragmentation Biodiversity responses to urbanization-induced fragmentation might show a temporal delay [72]. This depends on several factors, including the species turnover rate, remnant area, landscape connectivity and disturbance intensity. Temporal delays are shorter for species with higher turnover rates (e.g. annual vs perennial plants), for smaller and more isolated remnants, and following small perturbations [72]. In old cities, remnant biodiversity might be largely shaped by the disturbance processes originating from the surrounding urban matrix. However, in young and rapidly urbanizing landscapes, communities are likely to be gradually adjusting to the novel environment. During this transient period, biological communities might be better explained by previous rather than current remnant and landscape spatial configurations [72,77,78]. Furthermore, these communities contain a transient species pool that might include species that will go extinct once the transient period is over (i.e. extinction debt) [72]. In a similar way, they might not yet be affected by the invasion of exotic species, which is more likely to occur once remnants re-equilibrate (i.e. invasion credit) [60,73,79]. Failure to consider land-use legacies effects and transient dynamics in the response of biodiversity to fragmentation can have major consequences for the scope of urban ecological research. Indeed, it might lead ecologists to classify remnants with different fragmentation trajectories and legacies in the same class of urbanization. Essentially, communities at different stages along the course of adjustment to the surrounding environment are mixed more or less indiscriminately and independently of their past. This can lead to incorrect and misleading study design (Figure 2) and, ultimately, to contradictory and unexpected results. Research on the species richness–area relationship is an example in which misleading interpretations are likely to arise if time is not considered, because if data were collected in remnants with different ages, any area effect might be masked by the differences resulting from different trajectories of fragmentation [80]. Towards an emerging framework in urban ecology A new approach to studying the ecology of cities is needed that incorporates: (i) awareness that urbanization intensity and age needs to be assessed based on the analysis of the focal remnant patch and neighboring landscape, rather then on its position along a linear geographic transect; (ii) a mechanistic perspective, considering the role of multiple drivers and their direct and indirect effects on remnant 183

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ecosystems; and (iii) an explicit temporal perspective, acknowledging land-use legacies and time-lagged responses to environmental change. A more effective emerging framework would incorporate three essential elements (Figure 3). A first element is a comprehensive set of intervening factors selected using an ecologically oriented perspective. These factors can quantify drivers, patterns, or processes, and include: (i) human factors (e.g. socio-economic, demographic and built infrastructure); (ii) environmental factors affected by urbanization, including landscape-scale (e.g. fragmentation and land use) and local-scale factors (e.g. disturbance regimes and local environmental conditions); and (iv) environmental factors unaffected by urbanization (e.g. geological or geographical). An ecologically

oriented approach is important to guide in the identification of the factors relevant to the ecological question addressed. On the one hand, this requires focus on the species or community of study, because the response to the environment is species and/or trait specific [81,82]. Therefore, environmental attributes and scales meaningful to one species or community might not be relevant to another. On the other hand, it demands a careful analysis of the study area. For instance, if a study is undertaken in a suburban-type landscape, then income or education level might be more appropriate drivers of ecological variation in the area than is human population density. A second element is an explicit temporal perspective. Given that urban and landscape ecology have focused

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Figure 3. Dynamic Urban Framework: an emerging framework for the study of cities. The urban-to-rural gradient approach classifies the degree of urbanization of remnant ecosystems using either categorical classes or quantitative measures of linear distance between the city centre and the rural matrix (a) (remnant vegetation in black); or a combination of those with socio-economic, land cover, land use, or built infrastructure metrics (b) (road density depicted here). Data analysis usually focuses on the comparison between ecological responses across different urban classes or on the single effects of a simplified set of explanatory variables (c). A more comprehensive Dynamic Urban Framework uses a temporal perspective that places the focal urban remnants in their trajectory of change, analyzing the length of time they have been in the urban landscape and their past spatial configurations and land uses (d). It also uses an ecological perspective that identifies the variables that best describe the range of variation in the community or ecological process of interest (d). A hierarchical perspective is used to understand the causal and interacting relationships between multiscale drivers and their direct and indirect effects on the ecological community or ecological process of interest (e).

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Box 3. Measuring the temporal dynamics of landscape change Landscapes are complex systems with two main vectors of dynamism and change: space and time [83]. Landscape and urban ecology have developed their main body of knowledge from research on spatial patterns. However, temporal dynamics have often been ignored and there are very few consistent examples of case studies, nomenclature, or conceptual frameworks supporting research along the temporal axis of ecological variation. Nonetheless, historical geographic data, such as aerial photographs and cartographic maps, are available and can be used to assess how urban landscapes changed through time. Here, we suggest three types of variable that can be used to quantify temporal dynamics of landscape change in urban ecological research. Urbanization or remnant age Urbanization or remnant age reflects the time since the urban patch was developed or the remnant patch was isolated and surrounded by urbanization, respectively [36,62,63]. This variable can be used to

mostly on the analysis of spatial patterns, a deliberate shift is needed from that purely spatially oriented approach towards a perspective that recognizes landscapes with two main vectors of change: space and time [83]. From a theoretical perspective, this involves the incorporation of important conceptual constructs, such as extinction debts [72,77], invasion credits [60,73] and land-use legacies [71]. From a methodological perspective, it demands consideration of the intervening factors mentioned above from a spatial and temporal perspective. Here, we underline the importance of characterizing the temporal dynamics of landscape change, including urbanization or remnant age, past remnant and landscape attributes, and fragmentation drivers (Box 3). Temporal dynamics of landscape change are likely to be particularly important when: (i) urbanization is relatively recent; (ii) there is a range of time since remnant isolation and/or urbanization; and (iii) there is a range of previous land uses. A third element is a conceptual and analytical structure where the relationships between and among driving and response factors are analyzed in a mechanistic manner.

quantify the length of exposure to the urban environment and the time lag in ecological responses to urbanization-induced fragmentation; Past remnant and landscape attributes Past remnant and landscape attributes refer to patch and landscape spatial configurations (e.g. remnant area and landscape connectivity) [77,98], land cover (e.g. urban cover) and socio-economic attributes (e.g. population density and build-up density) [64] that can be quantified in a time series. Future studies could develop timeweighted variables, measuring the age of attributes of interest; Landscape fragmentation drivers Landscape fragmentation drivers are variables identifying the main drivers of landscape fragmentation and isolation of the focal remnant patch (often agriculture, urban or industrial development). Such variables can be used to track the presence of land-use legacies.

This can be achieved using a hierarchical approach. Urban ecosystems are more likely to be described as heterarchical rather than hierarchical systems, in the sense that different factors might or might not be related by causal relationships, depending on the conditions and scale of analysis [84,85]. Nevertheless, a hierarchical approach provides a middle ground where the complexity of these coupled human–nature systems can be accommodated, and their multidimensional nature partitioned into smaller, more manageable subsystems [42,86,87]. The hierarchical patch-dynamic framework [42] provides an integrative approach to spatial analysis, whereby the nested structure of spatial and temporal patterns and processes in urban landscapes can be depicted [88]. This framework provides core structure to urban LTER projects in the USA [20,44,47] and its use should be further encouraged. Furthermore, structural equation [89] and Bayesian hierarchical modelling [87,90] are promising statistical tools to investigate the complex networks of causal and interacting relationships between multiple factors, and their direct and indirect effects on remnant biodiversity and ecosystem

Box 4. A temporal perspective in the planning and management of urban remnants Urban planning Identification of remnant sizes Extinction debt research aids in the understanding of how biodiversity varies in time in response to remnant size and connectivity, variables that are often the scope of urban planning decisions. Therefore, it can provide guidance on the selection of remnant sizes and landscape configurations that will allow reasonable conservation outcomes in the future. Identification and prioritization of remnants to set aside for conservation A temporal perspective considering the remnant age and past land uses can provide insight into the biodiversity value of particular remnants and, therefore, can be used in prioritization for conservation. Priorities could be, for instance, those remnants without significant land-use legacies and those that were recently fragmented. Management and restoration Managing and restoring remnants that have land-use legacies A temporal perspective considering land-use legacies adds realism to the formulation of goals and understanding of outcomes in restoration. The presence of land-use legacies might mean that ecosystems

have passed biotic and/or abiotic thresholds that might impede restoration [71]. Furthermore, if thresholds were crossed, ecosystems are likely to require specific interventions that are not required in remnants not subject to those legacies. For example, whereas prescribed burning and mechanical overstorey thinning were important drivers of the plant community in post-agricultural Pinus palustris woodlands in the south-eastern USA, these actions had barely any effect on historically forested sites [99]. Improving the habitat quality of remnants in transient periods of adaptation In rapidly urbanizing landscapes where natural areas were cleared for urban development, the transient period in which remnant biodiversity gradually adjusts to the novel urban scenario provides a unique opportunity for action [65]. Interventions should improve the habitat quality of these remnants and target: (i) the core patch with restoration efforts and the design of margins and tracks that minimize influence from humans and external processes; and (ii) the buffer areas [100], by improving connectivity and enhancing the urban matrix at various scales, from the individual garden to the neighborhood or suburb [68]. These interventions should target priority remnants and also those where keystone species are present and whose extinction are predicted to have cascade effects on the survival of other species [77]. 185

Review functioning [87,90]. Finally, keeping in mind the heterarchical nature of urban ecosystems is essential because the importance of different ecological–social drivers and their temporal and spatial boundaries is fluid [85]. This flexibility is fundamental to a dynamic approach. Application to planning, management and restoration in contemporary cities A critical approach to the assessment of urbanization in ecological studies will expand the ability and scope of urban ecological research to better intervene in the planning, management and restoration of remnant ecosystems in contemporary cities. First, a proper identification of the drivers controlling remnant ecosystems elucidates where management and restoration efforts should focus, helping to formulate meaningful management guidelines and tailor strategies of action. This is important not only to maximize conservation outcomes, but also to minimize costs. Second, a temporal perspective considering landuse legacies and time-lagged ecological responses to fragmentation places current condition of an ecosystem in the context of its trajectory of change [71], enhancing the understanding not only of observed patterns, but also the processes and dynamics that generate and maintain them (Box 4). Concluding remarks In the context of a rapidly urbanizing world, it is important to consider the complex growth, relative youth and dynamic nature of contemporary cities if ecologists want to move forward in the study and conservation of the places where most humans live and work [10]. Failure to consider these characteristics compromises the scope of urban ecological research, potentially leading to ill-designed studies and partial or misleading research outcomes. Furthermore, it limits the ability of urban ecology to provide meaningful guidance to planning, conservation and restoration in cities. Here, we have suggested the essential elements of an emerging Dynamic Urban Framework. From a conceptual perspective, this framework is based on ecological theory that urgently needs to be incorporated into mainstream urban ecological research. In particular, the transient dynamics in biodiversity response to environmental change, including extinction debts [72,77] and invasion credits [60,73], implications of land-use legacies for conservation [71], hierarchical patch dynamics [42,87] and hierarchical modelling [87,90], all need to be incorporated. From a practical perspective, the Dynamic Urban Framework: (i) is grounded in the area and community of study; (ii) places the process of urbanization and its effects on biodiversity and ecosystem functioning in a temporal context; and (iii) depicts the observed ecological responses as the result of multiple measurable factors that relate and interact at different spatial and temporal scales. As a whole, the conceptual and practical elements of the framework can be a first step towards the foundation of a new approach to the study of cities. Acknowledgements C.E.R. was funded by a Portuguese National Science Foundation (Fundac¸a˜o para a Cieˆncia e a Tecnologia) doctoral scholarship. The 186

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authors thank Lauren M. Hallett for her encouragement and input, and Michael Perring, Kris Hulvey and two anonymous reviewers for useful comments on earlier versions of the manuscript.

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