Expanding fundamental ecological knowledge by studying urban ecosystems

Abstract

The expansion, densification and proliferation of urban areas around the world is currently occurring at a rate that is unprecedented in human history. It is predicted that global urban land cover will triple between 2000 and 2030, with some regions (including biodiversity hotspots) experiencing a ninefold increase in urban land cover over the same time period (Seto, Güneralp & Hutyra 2012). Accompanying the expansion of urban landscapes, it is anticipated that the human population living in cities and towns globally will increase from 3·5 to 5 billion people within the next 20 years (Fragkias et al. 2013). Thus, the demands of an expanding and urbanizing human population are one of the pressing ecological problems our world is facing (Sanderson et al. 2002), alongside, and in combination with, global climate change and changes to biodiversity at local and global scales (Pimm et al. 2014). Yet, urban environments also present a unique opportunity to expand our fundamental knowledge related to ecology and evolution due to the presence of intense and often novel selection pressures. In the inaugural issue of this journal, Calow (1987) defined functional ecology as the sum of three interactive processes: (i) those occurring between organisms and their environment, (ii) biotic interactions between organisms and (iii) adaptive processes driven by natural selection. The same three processes were highlighted 1 year earlier by Jared Diamond in Nature, when he called for biologists to pay more attention to the potential of using the unprecedented environmental conditions that exist within towns and cities to develop and test evolutionary and ecological theory (Diamond 1986). There is thus a natural synergy between functional ecology and urban ecology, as exemplified by some of the classic papers that have appeared in this journal, such as Rydell (1992) who demonstrated that the form of echolocation system determined the impact of light pollution on bat foraging behaviour. The potential of combining functional ecological research with urban ecology is, however, a long way from being fully realized. This is in part explained by the youth of urban ecology as a discipline. Scientific enquiry into the ecological consequences of urban environments has been underway for over half a century, although most of the momentum emerged after the mid 1990s (McDonnell 2011; Wu 2014). Thus, the focus of much urban research to date has involved describing patterns along environmental gradients (Gagné 2013; McDonnell & Hahs 2013) rather than investigating the mechanistic processes that lie at the heart of functional ecology. To be effective in addressing the global challenges of urbanization, a much better understanding of how the urban environment affects the ecology and evolution of organisms needs to be developed (Grimm et al. 2008; Marzluff 2012; Gil & Brumm 2014; McDonnell & Hahs 2015). The purpose of this special feature is to draw attention to the plethora of opportunities that await researchers investigating the ecology and evolution of organisms in urban environments. The combination of environmental stressors and conditions within urban areas provides a novel opportunity to test and expand our theories related to ecology and evolution of organisms, and some intriguing insights are already beginning to emerge. For example, the detailed understanding of the molecular, genetic and developmental mechanisms of beak evolution that has arisen from studying Galapagos finches has been significantly advanced by studying beak evolution in the house finch Carpodacus mexicanus in response to novel urban food sources and its consequences for acoustic communication (Badyaev 2010, 2014). Thus, urban ecology has the potential to extend our understanding of extremely well-studied ecological and evolutionary problems. The five papers presented in this special feature have been selected to highlight the three axes of functional ecology originally identified by Calow (1987) whilst avoiding overlap with other recent reviews and syntheses of urban ecology research published in the recent literature (Chamberlain et al. 2009; Evans et al. 2010; Bonier 2012; Foster & Sih 2013; Gil & Brumm 2014; Gaston, Visser & Hölker 2015). They were also selected to represent topics where the existing body of knowledge specifically related to urban environments is sufficient to enable a meaningful review and synthesis to be conducted at this point in time, although there are still occasions where the authors have been required to draw upon findings from research conducted in nonurban environments to reveal additional insights. Movement is one of the most fundamental ways in which an organism interacts with its environment determining crucial traits such as home range size (and thus population density), individual survival (and thus population demography), recolonization potential (and thus in a metapopulation structure, population survival rates) and gene flow (a core determinant of adaptive capacity). Urban landscapes are highly fragmented making understanding of movement patterns particularly important. LaPoint et al. (2015) explore ecological connectivity research in urban landscapes, reviewing methodological approaches and identify five important advances that will strengthen future research in this area. The focus then shifts to Calow's second axis of functional ecology, that is biotic interactions, and how these are moderated by urban selection pressures. Harrison & Winfree (2015) review the impacts of four major urban environmental stressors (landscape fragmentation, non-native species introductions, urban warming and environmental contaminants) on the function of plant–pollinator interactions. Epidemiology and disease risk are crucial fields for understanding individual performance and selection pressure, whilst zoonotic diseases have important implications for human health and thus human–wildlife conflict. Starting with a simple epidemiological model, LaDeau et al. (2015) demonstrate how urban landscapes can have opposing effects on five key parameters that determine the transmission potential of vector-borne diseases, thus helping to develop a mechanistic understanding of why generalizations regarding the impact of urbanization on wildlife disease are so elusive (Brearley et al. 2013). Our final two papers focus, albeit in nonclassical ways, on Calow's third axis of functional ecology, that is adaptive processes. In so doing they simultaneously draw attention to urban pollution gradients, that is heat pollution and oxidative stress, that have been somewhat left behind by the surge of interest in light (Gaston, Visser & Hölker 2015) and noise (e.g. Slabbekoorn 2013) pollution. Chown & Duffy (2015) use thermal tolerance as a mechanism to explore entry, exit and transformation rules for organisms exposed to urban heat islands. Isaksson (2015) explores mechanisms through which oxidative stress and inflammation determines the capacity of organisms to adapt, acclimatize or otherwise cope with urban environments. Although the papers in this special feature were each prepared independently, there are a number of instances where the content of one paper complements that presented in another. When read as a collection, a number of striking themes emerge, related to particular areas of research focus, current challenges and opportunities for progress. These themes will help shape the direction and scope of future urban ecology research, through both the insights articulated within the papers and the synergies that exist between papers which reveal additional areas for investigation. The remainder of this Editorial discusses and synthesises these major themes, challenges and opportunities for developing a broad and deep mechanistic, and thus functional, understanding of urban ecology. One of the key urban stressors that has received surprisingly little attention in the ecological literature is thermal pollution associated with the urban heat island effect (UHI). Chown & Duffy (2015) present an elegant case for why we need to redress this knowledge gap and identify a number of fruitful avenues for future research related to the role of thermal physiology in structuring urban assemblages, the underlying driving mechanisms, and investigations that specifically set out to collect direct evidence for physiological adaptations. This is further exemplified by consideration of how urban warming can modify phenology, behaviour and plant–pollinator (Harrison & Winfree 2015) and host–vector–pathogen interactions (LaDeau et al. 2015) in ways that will impact reproductive success and survival. Environmental contaminants provide another very different source of pollution in towns and cities that can alter all three of Calow's axes of functional ecology (Harrison & Winfree 2015; Isaksson 2015; LaDeau et al. 2015). Major knowledge gaps, however, remain. Isaksson (2015), for example, highlights that much of the limited research conducted on nanoparticles is based on the health impacts on humans at ground level. It is problematic to apply the findings to other species that exploit above-ground habitats, such as birds, as this exposes them to a very different suite of nanoparticles. This is just one further example of the importance of developing a more detailed understanding of how individuals move within and between urban environments (LaPoint et al. 2015), as there is often much fine-scale spatial variation in the distribution of environmental contaminants in urban landscapes (Charlesworth, De Miguel & Ordóñez 2011). Urban systems are characterized by tight coupling between human and natural systems, and urban ecology is thus unusually dependent on understanding how socio-economic factors influence the magnitude and form of this coupling. One powerful example of this is that lower socio-economic neighbourhoods typically provide more suitable breeding habitats (unmanaged water containers) for insect disease vectors such as the Asian tiger mosquito Aedes albopictus with important implications for disease risk to people, but also probably wildlife (LaDeau et al. 2015). Exposure to disease and the quality of the immune system are impacted by a diverse suite of environmental gradients that are altered by the nature and intensity of urbanization (Isaksson 2015; LaDeau et al. 2015) and provide excellent systems for developing an integrated framework of the mechanisms through which urbanization impacts populations and resultant assemblages. One of the cited disadvantages of undertaking urban ecology research is the potential confounding effects of multiple interacting drivers (Catterall 2009). The novel combinations and magnitudes of stressors in urban environments certainly make it imperative that tests of theory developed in other settings are conducted in urban environments. A particular challenge for the future will be identifying the extent to which the stressors present in urban environments accelerate or alter the pathways through which organisms respond to the conditions in these landscapes. The occurrence of multiple urban stressors is, however, not necessarily a curse to urban ecology. There is increasing recognition that predicting the impacts of environmental change demands an understanding of the interactions between multiple environmental change drivers (Tylianakis et al. 2008). The spatial congruence of many different environmental change drivers in towns and cities thus provides crucial opportunities to understand such interactions and improve predictive ecology. In this context, Harrison & Winfree (2015) discuss the opportunities that urban environments provide to investigate how phenological shifts in plants and pollinators associated with warmer climates, and altered moisture and CO2 levels, generate selection pressures and the outcomes of resultant adjustments or adaptation. They propose cities provide natural experiments for testing the effects of climate change. Indeed, cities have notable advantages as current UHIs are often similar to projected conditions arising from climate change (Youngsteadt et al. 2015) whilst also varying within and between cities in relation to the physical properties of urban form (Stewart & Oke 2012) and they are widely distributed across multiple climatic zones (Chown & Duffy 2015). Urban ecology must indeed take advantage of the opportunity to conduct studies over multiple locations to address questions concerning generalizations of patterns and mechanisms across urban locations and the interconnectedness of urban adapted populations (Evans et al. 2009a,b, 2012). This type of research needs to be expanded over a range of continents, biomes, city shapes and sizes to investigate questions that cannot be addressed by research conducted in a single urban setting (McDonnell & Hahs 2009; Chown & Duffy 2015; Harrison & Winfree 2015; LaPoint et al. 2015). To date, urban ecology has largely focused on temperate cities in the Northern Hemisphere and Australasia with far fewer studies in other regions (e.g. LaSorte et al. 2014). Although cities share many similarities in terms of the built infrastructure, human population densities and associated environmental stressors (Rebele 1994), they are distributed across a wide range of biogeographic and climatic zones. Chown & Duffy (2015), for example, highlight that large cities span mean annual temperature gradients of 30 °C and total annual precipitation gradients of 4000 mm. Therefore, the likelihood of complete convergence in the environmental conditions or biotic homogenization across all cities is very low (Aronson et al. 2014). Expanding the representation of cities, and species, that shape urban ecological research is therefore the only way general principles concerning the mechanisms through which urban environments influence organisms, population and assemblages can be identified (McDonnell & Hahs 2013). One striking example of why this is important is that the largest ecological impacts of the urban heat island are predicted to occur at latitudes between 30 and 35° N or S (Chown & Duffy 2015), yet only a tiny fraction of urban ecological research is conducted in these regions. In many respects, the challenges identified in the previous section reflect the legacies of knowledge, technology and funding that have shaped the current body of urban ecology research. All of the papers in this special feature have identified new tools and methodologies that can be employed to progress beyond these historical barriers and deepen our understanding of the ecology of organisms in urban landscapes. Whilst research on a broader range of taxa is needed, it will never be possible to conduct autoecological studies on the complete range of species that occupy urban areas (McDonnell & Hahs 2009). Over the past 20 years, functional traits and other methods (such as phylogenetic approaches, behavioural guilds, etc.) have been developed which allow a generalized understanding based on species characteristics to emerge, including in response to urban selection pressures. Trait-based approaches will continue to be important in revealing relationships between organism traits and functional connectivity (LaPoint et al. 2015), trait-mediated interactions between organisms (Bonnington, Gaston & Evans 2013; Harrison & Winfree 2015) and refining biophysical models (Chown & Duffy 2015). The selection of informative and directly relevant traits will, however, be imperative if we are to identify the pathways through which urban environments impact on organisms and not simply document the outcomes from stochastic processes (Donihue & Lambert 2015). New genetic techniques open up exciting opportunities to collect new types of information from organisms, including associations between functional connectivity and population genetic structure (LaPoint et al. 2015), the link between genotypic and phenotypic adaptations (Chown & Duffy 2015), the use of transcriptional profiles to estimate ages of individuals (LaDeau et al. 2015) and investigations into the roles of epigenetic mechanisms in regulating responses to urban environments (Isaksson 2015). As noted by Donihue & Lambert (2015), the link between physical or behavioural adaptations and genetic signatures is critical for confirming evolutionary mechanisms of adaptation. Advances in modelling techniques are also poised to make a substantial contribution to knowledge of urban ecology. Chown & Duffy (2015) present examples of how trait-based biophysical models can provide information on the individual and interactive roles of plasticity and evolutionary change on the likelihood of species entering, exiting or transforming in urban landscapes. LaPoint et al. (2015) also highlight the role of computer modelling techniques to inform studies of functional connectivity through the concept of landscape resistance. Conceptual models and frameworks are also improving, with implications for the quantitative models used to represent study systems. LaDeau et al. (2015), for example, highlight how more nuanced understanding of disease dynamics in urban landscapes can be developed by including human behaviour and fine-scale environmental conditions into spatio-temporal models. The tools and methodologies discussed above allow ecologists to develop insights into temporal dynamics from relatively static snapshots of data. New technologies also exist which allow us to improve the empirical data which can be collected in the future. Investment in the collection of empirical data in urban environments is critical, both to confirm predictions that arise through other methodological approaches and to capture new data that can be used to feed into future models and trait-based analyses. Examples of improved field technology include miniaturized GPS tracking devices that capture real-time biotelemetry data in urban landscapes (LaPoint et al. 2015), and whilst not necessarily new, improvements in fluorescent dye techniques can contribute to improved understandings of plant–pollinator interactions (Harrison & Winfree 2015). Examples of important opportunities for experiments include the use of cities as natural experiments for understanding the impacts of climate change (Chown & Duffy 2015; Harrison & Winfree 2015), testing laboratory-based knowledge on the impacts of environmental pollutants on organisms in actual urban landscapes (Harrison & Winfree 2015; Isaksson 2015), common garden experiments and long-term studies of multiple populations or study organisms with pedigree data to test evolutionary responses (Isaksson 2015) and Before After Control Impact Reference studies on the efficacy of efforts to restore connectivity in urban landscapes (LaPoint et al. 2015). As these tools and methods become increasingly incorporated into urban ecology research both now and in the future, a more sophisticated understanding of the mechanistic and functional ecology of organisms in urban environments will begin to emerge. Faced with the global environmental challenges that now confront us, it is imperative that we develop a strong ecological evidence base that can be drawn upon to inform important decisions related to future courses of action. Urban ecosystems offer a valuable microcosm in which we can test our existing ecological knowledge and address some of the key knowledge gaps that will be required for humanity to successfully navigate through the anthropocene (Sanderson et al. 2002). The research topics presented in this special feature are firmly grounded in existing ecological frameworks. The main knowledge gap lies in understanding how these systems perform under the novel stressors that are present in urban environments. By undertaking basic research on the ecology of organisms in urban landscapes, we will not only enhance our scientific understanding, but we also enlarge our opportunities to use this knowledge to inform decisions that will impact on the ability of organisms to persist and adapt to cities in the future. We hope this special feature will inspire readers of Functional Ecology to consider extending their research into urban environments. To existing urban ecology researchers, we hope this special feature will provide additional impetus for undertaking mechanistic research that helps to redress critical knowledge gaps related to population, community and evolutionary ecology in urban environments. By bringing these various disciplines together, an exciting new frontier of research and understanding begins to unfold. We look forward to learning what lies beyond these emerging horizons. We would like to thank Charles Fox for the invitation to prepare this special feature for Functional Ecology, Jennifer Meyer for her assistance in the editorial process and Mark McDonnell for constructive advice and feedback. AKH was supported by funds from the Baker Foundation. Our deepest thanks go to the invited authors for the time and effort they have expended in producing this special feature.