Ecological research can augment restoration practice in urban areas degraded by invasive species—examples from Chicago Wilderness
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- Heneghan, L., Umek, L., Bernau, B. et al. Urban Ecosyst (2009) 12: 63. doi:10.1007/s11252-008-0057-8
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Urban biodiversity conservation needs a firm scientific foundation, one that draws upon active and regionally calibrated research programs. Until recently this foundation has not existed. In this paper we examine the way in which the emerging discipline of restoration ecology in an urban context can learn from the experiences of ongoing restoration projects and in turn how novel insights from research of urban soils can help these projects define and reach their goals. Limitations on collaboration between academic researchers and practitioners continues be problematic. We discuss a model whereby this impediment may be removed. A case study of Rhamnus cathartica, an invader of Midwestern woodlands which modifies some important soil ecosystem properties will be used to illustrate the potential for engagement between research and practice.
KeywordsUrban ecologyRestorationEcology and managementInterdisciplinary researchSoil restorationBuckthornRhamnus catharticaInvasive species
Biodiversity conservation in urban environments can contribute in significant ways to the conservation of global biodiversity (Crane and Kinzig 2005). However, because urban environments suffer from considerable anthropogenic stresses, most sites set aside in metropolitan settings are severely degraded, and therefore are in need of active management (Miller and Hobbs 2002). Despite the recognition of a need for intensive conservation management in urban settings, systematic ecological research of a sort likely to be useful in directing is a relatively poorly developed. In this paper we present a case study on the significant challenges surrounding woodland conservation in the Midwestern USA and the ways in which developing relationships between researchers and practitioners are useful in achieving conservation goals. In particular, we show that investigations of the ways in which an invasive shrub impact soil processes may necessitate modified management approaches. Developing similar models of linking ongoing research and practice will be important.
Urban ecology: An emerging priority
Much of conceptual underpinning of ecological thought was formulated by thinkers living close to town but drawing upon vicariously collected data or ruminations initiated elsewhere. This includes the work of Darwin and Thoreau, identified by Worster (1994) as founders of the discipline. The development of key theoretical insights providing a framework for much of modern ecology deriving from a range of late nineteenth and early twentieth century scientists (e.g. Forbes 1887; Cowles 1899; Clements 1936; Gleason 1926; Lindeman 1942) follows an analogous pattern. Of these Frederic Clements, like Thoreau and Darwin, drew much of his inspiration from wilder places, (in Clements’ case, the relatively undisturbed grasslands of the American West). The data upon which many of the other foundational papers were based was collected at sites closer to large metropolitan areas, but despite the proximity of these authors to the city and town, the city was generally not reflected in the work.
Despite the unprecedented urbanization that occurred during the twentieth century, resulting in approximately 50% of the world population living in urban areas (UNPF 2007), the development of a systematic ecology of urban spaces began relatively recently (McDonnell and Pickett 1990; Zipperer et al. 2000). Although there are numerous scattered references to urban sites in ecological literature throughout the last century, the city remained largely absent from mainstream ecological literature until late in the twentieth century. The deployment of ecological concepts to urban settings was largely left to researchers from other disciplinary fields (e.g. Park 1936; Quinn 1940; Wirth 1945). According to Pickett et al. (2001) it was however largely deterministic, equilibrium versions of classical ecology used in these early sociological formulations. Another consequence of the neglect of urban systems by ecological researchers was that the application of ecology to environmental resource management was not informed by systematic programs of research and evaluation. Although many metropolitan areas had set aside land for reasons that included biological conservation, and these were managed in a variety of ways, there was little systematic attempts to evaluate the outcome of management.
A variety of well funded projects now underway are designed to provide a firm theoretical and empirical basis for urban ecology (Pickett et al. 2001; Grimm and Redman 2004). This emergence of urban ecology into the mainstream of the discipline is important not just because it complements and challenges the discipline of ecology as a whole, but because it provides an opportunity to calibrate theory developed in areas of lower human impact for its application in areas of high human density where land use is more highly variegated. Concepts that emerged early in ecology’s development remain influential and “popular” (i.e. the most commonly used ecological concepts according to the British Ecological Society: ecosystem, succession, energy flow, conservation of resources, competition, niche, materials cycling, the community and life-history strategies (Cherret 1989)) and many of these have been applied recently to analyzing ecological issues in cities (for instance, (Matlack 1997; Pickett et al. 2001; Tarvainen et al. 2003; Kaye et al. 2006). In addition to these more traditional ecological concepts, urban ecology has benefited from the development of a variety of newer conceptual approaches, including those that examine spatially fragmented ecosystems, such as, metapopulations, patch dynamics, source-sink dynamics, the use of habitat corridors, and a soil-oriented ecosystem focus (Collinge 1996; Pickett et al. 2001; Cadenasso et al. 2006). This may be an especially fruitful area of continued research because urban areas are characterized by intensified landscape configurations (e.g. fragmentation), distinct biological communities patterns (e.g. great susceptibility to invasion), and greatly modified ecosystem properties (e.g. modified hydrology and degraded or novel soils). An examination of these characteristic urban issues may therefore serve as a model for insights that can be subsequently applied elsewhere.
A distinctive aspect of urban ecology is that it retains an interdisciplinary flavor as the biophysical aspects of the discipline intersect with a sociologically oriented human ecology (Pickett et al. 2001; Alberti et al. 2003; Grimm and Redman 2004). The necessity of combining the biophysical with the social may serve as a strength, as relationships between the researchers and other disciplinary experts and practitioners developed in urban settings may serve as models for relationships in non-urban areas. At present, management strategies for the ecological resources of cities have largely developed, as we previously noted, in the absence of systematic programs of ecological research. As such the development of best practices for evaluating the effectiveness of ongoing management has proceeded without a firm research base. These management strategies were often based and still rely upon principles drawn from plant-oriented community ecology and ignore ecosystem-oriented and soil-based ecology (Choi 2004; Wardle et al. 2004). The collaborative ties between heterogeneous professional communities—for instance, scientists, managers, planners and conservation volunteers—that should emerge as urban conservation research develops will be crucial for improving conservation outcomes.
Conservation practice in urban areas
Ecological researchers in cities have stimulated fresh perspectives on management practices within the city. These include contributions to urban design (Van der Ryn and Cowan 1995; Todd et al. 2003), architecture (Edwards 1998; Ong 2003), resource sustainability (Wackernagel and Yount 1998) and urban biodiversity conservation (Goode 1989; Niemela 1999). The potential contribution of soil ecological research to urban biodiversity conservation efforts is the primary focus of the remainder of this study.
Problems and opportunities associated with urban conservation have assumed a growing importance in the consciousness of conservation advocates (Harrison and Davies 2002; Rudd et al. 2002; Crane and Kinzig 2005). In some instances conservation in highly fragmented urban areas contributes in quantitatively significant ways to conservation goals. In the case of the larger Chicago metropolitan region, for example, a vigorous ecological restoration movement contributes in meaningful ways to conservation in Illinois (Stevens 1996; Wang and Moskovits 2001). This is because many of the higher quality residual fragments of presettlement habitat are preserved in the hinterland of the city, whereas, by virtue of the fertility of its prairie soils the extensive rural landscapes of the state are dominated by intensive agriculture with consequent depletion of biodiversity (Cronon 1992; Warner 1994). Even where the cumulative impact of urban conservation is modest in both its success and its extent compared to conservation in more traditional preserves, the efforts of urban conservations may contribute in an underappreciated way to conservation outcomes. Urban ecological conservation, even when limited in scale, gives urban dwellers an opportunity to see and to value native communities, and these citizens may subsequently be more inclined to promote support for conservation policy directed at locations distant from the seat of power.
Habitats of conservation value in cities are part of an interstitial ecology; biodiversity is often where you least expect it: in pavement cracks and crevices (Chronopoulos and Christodoulakis 2000), along transportation rights of way (Bowles et al. 2003), in disused or abandoned patches (Goode 1989), all invariably representing fragments of formerly contiguous pre-urbanized communities that are now arrayed along a gradient of historical land use and human impact (Kent et al. 1999). Because of the landscape context, urban habitat fragments are confronted with a suite of problems that make their long-term sustainability improbable without management (Palmer et al. 2004). An analysis of threats to terrestrial habitats in Chicago, for instance, identify hydrological changes, fragmentation, altered fire regimes, loss of structural diversity, nutrient loading, increased salinity, erosion and increase sedimentation, invasive species, overgrazing by deer, as well a variety of other human impacts (Council 1999). In the face of such problems, conservation strategies that merely set aside land of conservation interest are not destined to succeed, and require, therefore, intervention in the form of restoration management (Miller and Hobbs 2002).
Although the causes of habitat decline in their urban interstitial locations have been well characterized, and the stresses enumerated above may serve as a point of analytic departure elsewhere, it is clear that these factors are interrelated in complex ways. For instance, habitats that are highly fragmented, nutrient loaded, unburned (where burning is the historical maintenance pulse (sensu Odum (1969), suppressing fire-intolerant species and increasing plant-available nutrients) become vulnerable to exotic species invasion (Rejmanek 1996; Davis et al. 2000). Invaded sites loose structural diversity, become further invaded, and in some case are more susceptible to soil erosion (Crooks 2002). Although the tasks that face the ecological restorationist are many (Packard and Mutel 1997) the removal of invaders consumes a significant share of the work in most parts of the world where restoration is undertaken (D’Antonio and Meyerson 2002). However, it is not always clear that this removal is effective or without unforeseen complications (Gordon 1998; Zavaleta et al. 2001). In particular, many invasive species may impose changes to ecosystem process and the invaded systems remain in resilient altered states even after the structural removal of the invaders (Suding et al. 2004). Ecological restoration has not, arguably, developed a reflexive practice that rapidly accommodates such challenges—where there are no clear goals set for restoration there is little incentive to evaluate outcomes and modify practice in the face of new challenges (Choi 2004). It is not at all apparent, on the other hand, that there has been a willingness by ecologists to draw extensively upon the experiences of managers, an attentiveness to which would undoubtedly enhance development of theory. Tensions between researchers and practitioners are such that there the relevance of restoration theory for the practice of management has been questioned (Cabin 2007; Giardina et al. 2007).
Despite the shared interest in urban conservation by resource managers and the growing number of urban ecological researchers, there are fundamental obstacles to success—gaps in knowledge about species and processes in urban habitats, inadequate monitoring of the results of management, and limited public understanding of the aims of urban conservation. This list, not intended to be exhaustive, underscores the obvious phenomenon that developing a productive relationship between the emerging science undergirding ecosystem management (and evaluating its success) and the management practice will be important for successful conservation outcomes. Because of differences in the way these professions evaluate problems, and gauge their successes and failures, developing this relationship has proved difficult (Huenneke 1995; Underwood 1995). The challenge that awaits urban ecology and restoration ecology is to develop an optimal and useful relationship with land managers, landowners, policy makers, and conservation volunteers. It should be pointed out that such difficulties are not confined to resource management. Problems of a similar nature have been highlighted in fields as diverse as consciousness research (Midgely 2001), and urban sociology (Lefebvre 2003). Developing strategies of effective engagement between researchers and practitioners may, in fact, be a substantial contribution of urban ecology to applied studies in general.
In the remainder of this paper we will develop a case study, that of the impact of the exotic invader European Buckthorn (Rhamnus cathartica) on ecosystem properties in relictual woodlands in metropolitan Chicago. The example demonstrates the degree to which restoration practice associated with the management of this prevalent invasive species has provided stimulating questions for ecological research and how the results of this work may both complicate, and enhance, restoration practice. When results relevant to practice emerge from restoration ecology, it is inherently difficult to implement them into practice. We will conclude with suggestions for developing a reciprocal model for moving theory and practice forward, in a manner that may be useful for both sides of the debate. The region in which this research is being conducted is referred to as Chicago Wilderness. The region embraces over 225,000 acres of protected openlands throughout Southeastern Wisconsin, Northeastern Illinois, and Northwestern Indiana, an area, perhaps surprisingly, with a rich natural history (Greenberg 2002). Chicago Wilderness also refers to the coalition of over 200 organizations (land agencies, museums, universities, arboreta, planning agencies, municipalities, etc.) that work towards preservation in this region (www.chicagowilderness.org).
Rhamnus cathartica in the Chicago Wilderness region
The shrub has been an object of management concern in the Chicago Wilderness region since the 1970s, although at the time when managers attempted to develop remediation strategies the primary literature on the ecology of this species was sparse (e.g. (Godwin 1936, 1943). Management was developed largely on the basis of attentive trial-and-error in the field (Stevens 1996). The history of successes and failure of management in the Chicago Wilderness region is not chronicled in detail in the primary literature (though see Gourley and Howell 1984; Boudreau and Willson 1992 which records management strategies in other regions). Observations over the past quarter of a century of management (recorded in communications to management-oriented journals e.g. Packard 1988, 1993 and proceedings volumes e.g. Stearns and Holland 1993; Fralish et al. 1994, Umek and Heneghan 2007) illustrate at least two important things. On the ground management of invasive species in the context of biodiversity conservation generates a number of interesting questions providing fertile areas for ecological research. Management in the absence of strong links to an active ecological research program may miss several opportunities for augmenting the efficiency and effectiveness of restorative management.
Despite the success of management in restoring the light gradients in degraded woodlands, it is obvious that a chronic problem with reinvasion by R. cathartica which impedes restoration (Heneghan, personal observation). Based upon these observations concerning reinvasion, it is important to consider the possibility that R. cathartica invasion imposes a persistent impact on ecosystem properties in a manner observed for a variety of other invasive shrubs (Ehrenfeld 1997; Ehrenfeld et al. 2001; Kourtev et al. 2002; Ehrenfeld 2003; Rice et al. 2004). If this is the case for R. cathartica, managed woodlands may retain modified ecosystem properties that constrain the success of subsequent restoration. That is, an invasion may shift the ecosystem into a relative persistent modified state that is not easily repaired in the absence of specialized intervention (Suding et al. 2004).
Rhamnus cathartica and the modification of soil ecosystems properties
We review the results of a number of recent replicated observations and experimental studies that demonstrate that R. cathartica is indeed associated with significant modifications to a variety of ecosystem properties in an urban woodland. We discuss several of these impacts, and conclude with a summary of the implications for future management.
Success of R. cathartica and its impact of some ecosystem properties
The success of buckthorn in ecosystems of the Midwest may be accounted for, among other factors, by virtue of its escape from herbivory, by alterations of soil processes including decomposition in the woodland floor where they grow, and by its synergy with other invaders.
We discuss each of these factors in turn.
European buckthorn escape from herbivory
Rapid decomposition of buckthorn litter and elevated decomposition rates within invaded areas
The rapid decomposition of forest floor material associated with buckthorn has at least two significant consequences
There is a collapse of the soil arthropod community in woodland areas associated with R. cathartica. We sampled these communities in quadrats measuring 255 cm2 in invaded areas and compared them from the litter in uninvaded areas in June and December of 2002, and April 2003. There was consistently a lower abundance of microarthropods in R. cathartica plots. For instance, in June 2002 there was an average of 83 individuals per quadrat in uninvaded areas, and six individuals per quadrat in invaded plots. To a large extent this was a function of the amount of DOM in the plots. However, even when abundance was expressed per unit mass of DOM there were differences found between plots in the April samples (Heneghan and Bernau, unpublished data).
Interactions between R. cathartica and invasive earthworms
There is a strong relationship between the presence of R. cathartica and the abundance of earthworms of Eurasian origins in Mary Mix McDonald woods. We exploited this gradient of invasive earthworm density to examine the effect of earthworms on litter dynamics on woodland floors. Using R. cathartica, Q. rubrum, Q alba, and A. saccharum litter, we demonstrated that in buckthorn thickets where earthworm populations attain the highest abundance and mass, litter loss were high where earthworms had unrestricted access to the litter. In contrast, litter of low substrate quality (Quercus spp.) were little affected by earthworm presence (Heneghan et al. 2006).
The results of our studies on R. cathartica in urban woodlands in the Chicago area indicate that this invader has impacts both above and below ground. Management that aims at rehabilitating woodland light regimes can be successful as revealed by analysis of canopy openness in invaded versus managed plots. The success of R. cathartica as an invader may be attributed to its escape from herbivory, but also to its impacts upon the soil. There has been no attention paid to ‘legacy’ effects of the invasion on the soil properties. We have demonstrated that invasion by R. cathartica has dramatic effects on the critical ecosystem process of decomposition. Not only is the litter of R. cathartica rapidly decomposed, but the overall rate of decomposition in invaded plots is elevated. As a result, many associated soil characteristics, including extent of the O horizon, pH, nitrogen cycling, and moisture levels, are different in invaded plots compared with adjacent uninvaded areas. Soil biological characteristics are also modified, including microbial community functioning and the abundance and diversity of litter dwelling arthropods (communities collapse in areas with high R. cathartica density). No systematic evaluation of the persistence of these effects has been undertaken. However, it seems likely that the legacy effects of R. cathartica invasion persist after the plant has been physically removed. Since many of the impacts are associated with conditions and resources important in determining plant community structure and function, it is possible that failure of restoration subsequent to aboveground removal of buckthorn is associated with these modified soil properties (discussed in more detail in the next section). The soil subsequent to invasion may be primed for the successful reinvasion of these woodlands by the same problematic species which were removed by management.
Integrating basic research into new management strategies
Although there are some reports of success in restoring sites subsequent to the removal of R. cathartica, many restorationists report having to revisit managed areas repeatedly since these areas become rapidly reinvaded (Thomas Murphy, personal communication) Arguably, if fire was reintroduced into these areas with some frequency reinvasion could be efficiently controlled (James Steffen, personal communication). Although anecdotal evidence exists to substantiate these claims there is no published confirmation of this in the peer-reviewed literature. There is a clear need for such a study, and a positive relationship between fire and resistance to reinvasion is a plausible hypothesis. The reinvasion of cleared areas with R. cathartica is also consistent with a general theory of invasibility, which posits that systems where the gross resource supply exceeds the capacity of the resource uptake of the vegetated community are more susceptible to invasion (Davis et al. 2000). The results above indicate that soils with a history of invasion have a legacy of accumulated total nitrogen, altered nutrient cycling, and modified soil biota—all factors in determining subsequent secondary succession (Tilman 1987; Brown and Gange 1992; Brussaard et al. 1997). Successional sequences that start with an inappropriate mix of species, and this can often be the case in sites recently cleared that retain altered soil conditions and foodwebs, can produce unanticipated results—that is, the plant community may have neither the planned composition and structure (Van-der-Putten et al. 2000). Therefore a useful management intervention might be to modify soil properties as part of the restoration of a degraded site prior to revegetation with native species.
One approach to reducing N content is to ultilize plants that high N requirement followed by an end-season removal (Maron and Jeffries 2001). Many of the techniques to de-fertilize soil have been developed in the context of restoring grasslands with a history of agricultural use. Typically, this has been achieved by growing a cover crop, followed by mowing and removal of the crop (Clark and Wilson 2001). The use of corn might be desirable for these purposes because of its high requirement for N, it is easily harvested and it can be removed entirely from the site after the treatments (several restorations employ this strategy, although there are not published accounts of it success (Sara Baer, personal communication)). There are several studies which indicate a benefit from adding sawdust or mulch (cellulose) or sugar to alter C/N ratios and to slow down modified N cycles (Reever-Morghan and Seastedt 1999; Averett et al. 2004). We are currently conducting an experiment which attempts to modify soil properties in a heavily invaded are prior to the application of more habitual restoration.
A fresh approach in the Chicago Wilderness region: The development of an integrative research program
Over the past 18 months Chicago Wilderness (CW) has been developing a research agenda based upon inputs by member organizations (Heneghan, Umek, and Mulvaney, unpublished data). The objective is to produce a document, the Natural Science Research Agenda, intended for use by research scientists and managers who are investigating major research questions regarding biodiversity conservation and land management in the region. Though it does not aspire to being all encompassing it should enable researchers to reflect upon the topics of most pressing concern to the CW coalition (http://www.depaul.edu/~lumek/CWRA). The research agenda is designed to lead to the development of a research program investigating the highest priority research questions for conservation in the region. Although the writing of the agenda is by one author (and the project managed by three investigators), the input of dozens of scientists, managers, and volunteers was solicited. The process was deliberately designed to be ‘bottom-up’, where the input of participants at workshops was captured in transcripts and then separated into research questions and assigned to their appropriate levels of organization (population, community, ecosystem, and landscape—a traditional ecological hierarchy recognizable to all participants). The research questions, and associated project suggestions, are placed within their relevant literature context. Despite the extensiveness of the input the number of questions has stabilized into priority areas. Among priorities identified so far, concerns about invasive species and about degraded soil processes have emerged strongly, and these questions will be the first questions addressed by the Chicago Wilderness Research Program.
We have provided a case study illustrating the manner in which research on the effects of an invasive shrub on soil ecosystem processes highlights a need for novel restoration management approaches. This specific case study is nested within a broader effort to develop a research agenda for ecological restoration in a major urban setting. Though not perhaps unique the case study provides an example of the dialogue between researchers and practitioners that surely must develop in several metropolitan areas in order to produce robust and transferable lessons useful to urban conservation elsewhere.
This work was funded in part by grant from USDA Forest Service to DePaul University. We thank them for this support. The project would not have been possible without the cooperation and support of James Steffen, Chicago Botanic Garden, Glencoe, Illinois, Wayne Vanderploeg, Department of Resource Management District of Cook County Forest Preserve, Dr Christopher Dunn, formerly of the Morton Arboretum, and Steve Bartram, of Lake Forest Openlands Association. Colleagues in the Environmental Science Program, especially Drs Thomas Murphy and James Montgomery are thanked for their lively interest and collegial support of this work. Help in the field and laboratory from, Evan Barker, Melissa Barnhart, Frank Cristelli, Kristen Fagen, Phoi Hua, Michelle Hargreaves, Mitchell Melton, Jamie Sandifer, and Daniel Strain was appreciated. We thank Dr Christ Iatropulos (Kieh company) for assistance with measuring cotton strip tensile strength. The figure of the sites was provided by John Foster, DePaul University. Undergraduate student grants from the Liberal Arts and Sciences program, and support from the Gutgsell Foundation were critical to completion of this project. Support from the National Park Service to review links between soils and restoration is gratefully acknowledged. Comments on an earlier version of this paper by two anonymous reviewers and by Mitchell Pavao-Zuckerman on a later version were very useful.