Ecological Networks as Conceptual ... - Wiley Online Library

Ecological Networks as Conceptual Frameworks or Operational Tools in Conservation LUIGI BOITANI,∗ ‡ ALESSANDRA FALCUCCI,∗ † LUIGI MAIORANO,∗ † AND CARLO RONDININI∗ ∗

Department of Animal and Human Biology, Sapienza Università di Roma, Viale Università 32, 00185 Roma, Italy †Department of Fish and Wildlife Resources, University of Idaho, Moscow, ID 83844, U.S.A.

Abstract: The establishment of ecological networks (ENs) has been proposed as an ideal way to counteract the increasing fragmentation of natural ecosystems and as a necessary complement to the establishment of protected areas for biodiversity conservation. This conservation tool, which comprises core areas, corridors, and buffer areas, has attracted the attention of several national and European institutions. It is thought that ENs can connect habitat patches and thus enable species to move across unsuitable areas. In Europe, however, ENs are proposed as an oversimplification of complex ecological concepts, and we maintain that they are of limited use for biodiversity conservation for several reasons. The ENs are species specific and operate on species-dependent scales. In addition, the information needed for their implementation is only available for a handful of species. To overcome these limitations, ENs have been proposed on a landscape scale (and for selected “focal” species), but there is no indication that the structural composition of core areas, corridors, and buffer areas could ensure the functional connectivity and improve the viability of more than a few species. The theory behind ENs fails to provide sufficient practical information on how to build them (e.g., width, shape, structure, content). In fact, no EN so far has been validated in practice (ensuring connectivity and increasing overall biodiversity conservation), and there are no signs that validation will be possible in the near future. In view of these limitations, it is difficult to justify spending economic and political resources on building systems that are at best working hypotheses that cannot be evaluated on a practical level.

Keywords: connectivity, core areas, corridors, ecological networks, focal species Redes Ecol´ ogicas como Marcos Conceptuales o Herramientas Operacionales de la Conservaci´ on

Resumen: El establecimiento de redes ecológicas (RE) ha sido propuesto como una forma ideal para contrarrestar la creciente fragmentaci´ on de los ecosistemas naturales y como un complemento necesario del establecimiento de a on de biodiversidad. Esta herramienta de conservaci´ on, ´ reas protegidas para la conservaci´ que comprende a ucleo, corredores y a on de varias in´ reas n´ ´ reas de amortiguamiento, ha atra´ıdo la atenci´ stituciones nacionales y europeas. Se piensa que las redes ecol´ ogicas pueden conectar parches de h´ abitat y, por lo tanto, permitir que las especies se muevan a través de a ´ reas inadecuadas. Sin embargo, en Europa las RE son propuestas como una simplificaci´ on de conceptos ecol´ ogicos complejos, y mantenemos que su uso en la conservaci´ on de biodiversidad es limitado por varias razones. Las redes ecol´ ogicas son particulares para la especie y operan en escalas dependientes de la especie. Adicionalmente, la informaci´ on requerida para su implementaci´ on solo est´ a disponible para un pu˜ nado de especies. Para superar estas limitaciones, las RE han sido propuestas a escala de paisaje (y para especies “focales” selectas), pero no hay indicios de que la composici´ on estructural de las zonas n´ ucleo, los corredores y las zonas de amortiguamiento podr´ıa asegurar la conectividad funcional y mejorar la viabilidad de m´ as especies. La teor´ıa que sustenta a las RE no proporciona suficiente informaci´ on pr´ actica sobre c´ omo construirlas (e.g., anchura, forma, estructura, contenido). De hecho, hasta ahora ninguna RE ha sido validada en la pr´ actica (asegurar la conectividad e incrementar la conservaci´ on de la biodiversidad) y no hay se˜ nales de que la validaci´ on ser´ a posible en el futuro cercano. En

‡email [email protected] Paper submitted May 10, 2007; revised manuscript accepted July 16, 2007.

1414 Conservation Biology Volume 21, No. 6, 1414–1422 C 2007 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2007.00828.x

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vista de estas limitaciones, es dif´ıcil justificar el gasto de recursos econ´ omicos y pol´ıticos para la construcci´ on de sistemas que, en el mejor de los casos, son hip´ otesis de trabajo que no pueden ser evaluadas en un nivel pr´ actico.

Palabras Clave: áreas nucleo, conectividad, corredores, especies focales, redes ecológicas

Introduction Human impact on natural ecosystems is the most important driver of the current mass extinction of species (Millennium Ecosystem Assessment 2005) and one of the greatest concerns for biodiversity conservation. Landscapes modified by human civilizations across all continents have been transformed into vast agricultural expanses, where the original and natural ecosystems have often been reduced to small, isolated patches. The habitats of many species have been extensively reduced, degraded, and fragmented to the point that their survival and the functionality of these ecological systems are often seriously threatened (Sala et al. 2000). Maintenance and restoration of some sort of “connectivity” among ecosystem elements and processes is regarded as the most obvious answer to counteract the negative impacts of fragmentation and of the small sizes of remaining patches (Crooks & Sanjayan 2006). With these problems in mind, a series of concepts such as wildlife corridors, landscape links, and ecoducts has been developed within the theoretical framework of landscape ecology (Turner et al. 2001, Turner 2005). Nevertheless, the poor definition of many of these terms and, in particular, the range of the intended functions of these structures at the variety of scales needed for biodiversity conservation has not helped build a robust theoretical framework and are the source of much controversy in conservation biology (Hilty et al. 2006). A recent addition to the growing list of concepts related to that of ecological connectivity is the ecological network (EN), broadly defined as a network of areas that are connected to enhance biodiversity conservation. Since the 1980s the EN idea has received increasing attention, particularly in Europe ( Jongman & Kristiansen 2001), where landscape ecology was first explored as an ecological discipline. In 1993 the EN concept attained political significance with the launch of a major continental project in Europe sponsored by the Council of Europe (an international organization of 54 countries in Europe and adjacent areas, www.coe.int) (Bennett 1994). The Council of Europe also provides substantial technical information through a wealth of gray literature. The Pan-European Ecological Network (PEEN, www.coe. int/t/e/cultural co-operation/environment/nature and biological diversity/ecological networks/PEEN/) is a priority goal of the Pan European Biological and Landscape Diversity Strategy (PEBLDS), and, in 1995, it was

endorsed at the ministerial level by all countries of the Council of Europe (Council of Europe 1996). They called for the establishment, within 20 years, of “a physical network of core areas and other appropriate measures, linked by corridors and supported by buffer zones, thus facilitating the dispersal and migration of species.” Currently, there are at least 42 EN initiatives active across Europe, 7 of which are at the national level (Mackovcin 2000; Novicki et al. 1996; Jongman & Kristiansen 2001; Michal & Plesnik 2002; Remm et al. 2004; Van Maanen et al. 2006). Many others have been implemented at the local level with substantial economic support from European and national agencies (Cavalchi & Pungetti 2000). Therefore, ENs may be politically relevant across a large range of scales and central to conservation policies of several governments and conservation organizations. But what is the science behind this approach and, most important, the implementation of ENs? Will ENs help conserve biodiversity, or are they a misapplication of ecological theories? We reviewed the main goals, objectives, and methods of ENs, particularly as they are applied in Europe. We focused on the simplistic paradigm that fragmentation is increasing, connection is good, and more corridors are needed, and on how the concepts of core areas and corridors are implemented in the context of an EN. We maintain that ENs in Europe are planned and implemented as an oversimplification of complex and still-evolving ecological concepts and that the assumptions implied in EN theory suggest a more cautious approach to investing money and political energies in their development.

Definition of an Ecological Network The phrase ecological network is ill defined and has been used in a variety of contexts and scales to indicate several different concepts. These include the simple assemblage of protected areas (e.g., the Natura 2000 system in Europe), small-scale links to facilitate the crossing of barriers by animal species (e.g., “green bridges” for brown bears in Croatia; D. Huber, personal communication), and large-scale regional or continental “green backbones” that focus on the coarse-scale connectivity of biological communities and wildlands (e.g., Yellowstone-to-Yukon Conservation Initiative, Carroll et al. 2001). Nevertheless, the “typical” definition of an EN refers to a composition of

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structural elements at the landscape level, such as core areas and corridors, usually designed to favor overall biodiversity conservation but that in practice focus on the needs of species whose habitat is assumed to be on a landscape scale (e.g., PEEN, Jongman & Pungetti 2004; Hilty et al. 2006). More recently, the EN concept has been expanded to include webs of linkages for several different functions (e.g., ecological, social, political, cultural) to adopt a more holistic view of land-use planning and biodiversity conservation (Bennett 2004). Even though all the concepts mentioned earlier are in some way related to biodiversity conservation, the best definition of an EN that explicitly relates to conservation on a landscape scale states that ENs are “systems of nature reserves and their interconnections that make a fragmented natural system coherent, so as to support more biological diversity than in its non connected form” ( Jongman 2004). These systems are composed of “core areas, (usually protected by) buffer zones and (connected through) ecological corridors” (Bischoff & Jongman 1993; Jongman 2004). We focused on this type of EN, which is one of the potential applications of the structural perspective offered by landscape ecology (Noss & Harris 1986), but excluded consideration of large-scale continental “green backbones” and small-scale corridors. These three essential elements (core areas, buffers, and corridors) may sometimes be associated with “restoration areas” for the recovery of damaged elements of ecosystems, habitats, and landscapes (Cook & van Lier 1994) and with “sustainable-use areas where sufficient opportunities are provided within the landscape matrix for both exploitation of natural resources and the maintenance of ecosystem functions” (Bennett & Witt 2001; Bennett 2004). Although there are many variations in the definition of ENs, the most common goal (for 14 out of 17 ENs in Europe) of an EN is “to maintain the biological and landscape diversity of a region.”

Rationale for Ecological Networks An EN is meant to ensure biodiversity conservation by protecting areas of assumed or known high species richness (core areas) and connecting them through corridors that should enable species to move across unsuitable areas. The logical flow of justifications is as follows (Bennett 1998): (1) land-use patterns have increased landscape fragmentation; (2) connections among fragments and the resulting exchange of individuals, genes, nutrients, and ecosystem processes are important for species to survive and ecosystem processes to remain functional; and (3) landscape linkages are needed to restore connectivity and ensure long-term survival of species and functionality of the ecosystem processes.


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The theoretical background for these justifications for ENs is in the theory of island biogeography (MacArthur & Wilson 1967), in metapopulation theory with its paradigm of source-sink dynamics (Hanski 1999), and in the broader perspective of landscape ecology (Turner 1989, 2005; Turner et al. 2001). It is also supported by the undisputable evidence that habitat fragmentation is among the primary threats to species survival (Wilcove et al. 1998; but see Fahrig 2003 for further research). Although each of the three contentions is supported by general ecological theories, they are flawed in several ways, or they are at the least too simplistic when applied in practice to real landscapes. We considered the most evident weaknesses of each contention. Increase of Landscape Fragmentation Whereas it is evident that landscape fragmentation is increasing in many areas of the world (e.g., where natural vegetation types are being converted to agricultural land), there are also regions where the trend appears to be in the opposite direction, although regenerated areas such as regrown forests may bear little ecological resemblance to the original landscape (Fuller et al. 1998). In Europe, in particular, forest cover has increased significantly in recent decades (Kauppi et al. 2006). In Italy agricultural land and pastures decreased, respectively, 13.2% and 50.7% from 1960 through 2000 and forests increased by 73%, which reduced landscape fragmentation (Falcucci et al. 2007). Moreover, because each species has its own habitat, which is defined on a specific speciesdependent scale (Corsi et al. 2000), fragmentation on a landscape scale implies a loss of connectivity only for species that have a landscape-scale habitat (Lindenmayer & Fisher 2006), such as those requiring vegetation types (e.g., forests) that are increasingly fragmented. The assumption that landscape fragmentation is increasing everywhere and has negative effects on all species should not be generalized without important caveats and exceptions. Connectivity and Species Movements There is growing evidence that a lack of connectivity between habitat patches can negatively affect the survival of species (Crooks & Sanjayan 2006), and the need to maintain and restore natural connectivity is accepted as a general principle of conservation biology (Noss 1991). Nevertheless, there is also substantial scientific evidence to support important caveats to the practical application of this principle. A long and lively academic debate has explored the positive and negative aspects of connectivity and especially of corridors (e.g., Hobbs 1992; Simberloff et al. 1992; Bennett 1999; Haddad 1999; Breininger & Carter 2003; Levey et al. 2005; Crooks & Sanjayan 2006). There is some evidence, although it is restricted to a few

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taxa, that corridors allow movement of individual animals (Bennett 1990; Beier & Noss 1998; Hilty et al. 2006; Noss & Daly 2006), but there is also evidence that some species, such as the Northern Spotted Owl (Strix occidentalis caurina) (Murphy & Noon 1992), Leadbeater’s possum (Gymonbelideus leadbeateri) (Lindenmayer & Nix 1993), and several bird species in Europe (Hindmarch & Kirby 2002) avoid landscape corridors. Moreover, there is little evidence that corridors have a positive impact on the connected populations and communities (Haddad & Tewksbury 2006; but see Damschen et al. 2006). Landscape connectivity may also provide connectivity for several ecological processes, although the evidence is weak particularly for species-specific effects (Bennett 1999; Noss & Beier 2000; Soulé et al. 2004). Connectivity per se is neither bad nor good, and, depending on species and context-specific conditions, it can be positively and negatively related to species conservation (Taylor et al. 2006). Landscape Linkages and Connectivity Connectivity can be divided into at least two main components: the structural component (connectedness) is a property of landscape features and their spatial arrangements and is generally measured at the scale of human perception; the functional component refers to the behavior of species and processes across the landscape and is, as is habitat, a species-specific property (Bennett 1999; Jongman 2004; Crooks & Sanjayan 2006; but see Lindenmayer & Fisher 2006 for a more articulated discussion of connectivity components). Although structural connectedness is the most easily measured and applied to conservation planning, it is only the physical background for the real function of connectivity, by which we mean the movement of organisms and processes. The assumption that structural connectedness ensures functional connectivity is unproven (Lindenmayer & Fisher 2006; Taylor et al. 2006), and matching the scale of spatial patterns and the process (animal movements and dispersal of plant propagules) does not ensure functional connectivity. Some EN proponents recognize the difference (e.g., Jongman 2004) but assert that “connectivity and connectedness come together in the concept of ecological corridors” ( Jongman 2004: 29). In this view the human perspective (landscape) is expected to match the ecological requirements of at least some species (Fischer et al. 2004). Functional connectivity is much more than structural connectedness. Because it is species-, population-, and context-specific (Beier & Noss 1998; Taylor et al. 2006), functional connectivity depends on species’ movement patterns and on individuals’ behavior (e.g., motivation to move, perception of the environment) (Belisle 2005). Although interesting contributions to an explicit thinking of functional connectivity have been proposed on the basis of graph theory (Bunn et al. 2000; Urban &

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Keitt 2001; Theobald 2006), movement models of individuals (Tracey 2006), and least-cost modeling (Beier et al. 2006), there is no satisfactory and comprehensive theoretical framework to support the concept of functional connectivity that complements that of landscape connectivity. Landscape, habitat types, and species’ habitat are very different concepts, but in the largely gray literature on ENs (and other aspects of conservation planning), they are often used interchangeably and at the same scale (i.e., landscape). The basis of connectivity in the European EN literature is fundamentally Forman’s (1995) classic patch-matrixcorridor model ( Jongman 2004), but Forman’s landscape model gives only a coarse view of the environment, with little explicit ecological support. The simplistic view of this model may be practical for broad landscape-scale analyses and applications, and this is the main reason why the model has been adopted so widely. Nevertheless, there are many other possible ways to interpret landscape patterns that may be better suited to model connectivity for species’ habitat and ecological processes (Lindenmayer & Fisher 2006). For example, models of individual species, such as the landscape contour models (Fischer et al. 2004), attempt to model the unique habitat requirements of one or several species across multiple spatial scales. This modeling approach offers a substantial improvement over pattern-based models, such as the island models (Haila 2002), which are based on the view that fragments of original vegetation are like islands with welldefined boundaries in an “ocean” of unsuitable habitat, and over the variegation model, which attempts to incorporate more gradual gradients and interspersion among vegetation patches (McIntyre & Barrett 1992).

Implementing EN All EN projects in Europe, from continental (e.g., PEEN) to national (e.g., Mackovcin 2000) and local scales, follow the guidelines proposed by Bennett (1998), van Opstal (1999), and Jongman (1995, 2004). These ENs are designed to contain at least core areas and corridors. A few projects also add buffer and other types of areas. The translation of these theoretical designs into practical application, however, takes place through the application of scientifically tenuous assumptions and hypotheses about core areas and corridors. Core Areas Existing protected areas (Natura 2000 sites, national and local reserves) are usually taken as the core areas of ENs. These areas are expected to represent the best areas available to ensure biodiversity conservation, but there is little evidence that existing protected areas actually represent ideal core areas for biodiversity. Few existing systems


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of protected areas have ever been tested with a systematic conservation-planning approach (Margules & Pressey 2000; Maiorano et al. 2007 [this issue]), and all systems have been assembled through a variety of criteria, among which biodiversity conservation was often not included. In Italy, for example, the existing protected areas cover 11% of the national land area, but their imbalanced distribution regarding habitat type leaves 63.2% of all vertebrate species insufficiently represented within the system (Maiorano et al. 2006). The assumption that the existing protected areas should be considered the best or the only possible selection of core areas for biodiversity and that they should have this role in an EN has yet to be proven. Corridors Early attempts to ensure connectivity in ENs through ecological corridors were based only on the structural features of the landscape, namely, the major types of natural vegetation, most commonly forests (e.g., Plesnik 1996; Pungetti & Romano 2004). More recently, recognizing that corridors are species specific, ENs are being designed to account for the ecology of one or more species, and all biodiversity is assumed to benefit (Bonnin et al. 2006). Different species use landscapes differently and on different scales. Even if the data existed, it would be impossible to reconcile landscape connectivity with habitat connectivity of more than a few species (Haddad et al. 2003). When sufficient data are available, it might be possible to design a species-specific EN (e.g., cougar [Felis concolor] in California, Beier 1993; red deer [Cervus elaphus] in central Europe, Bruinderink et al. 2003; Florida panther [F. concolor coryi] and black bear [Ursus americanus] in Florida, Smith 2004). In an attempt to account for several species with the same approach, ENs are increasingly being designed around focal (Lambeck 1997) or indicator (Landres et al. 1988) species. This approach has been widely debated in conservation planning, and it is important to recall that it is far from being satisfactorily developed. The focal and indicator concepts are weak when attempts are made to render them operational because they must rely on several assumptions about species co-occurrence and the power of surrogacy of individual species (Niemi et al. 1997; Lindenmayer et al. 2000; Rolstad et al. 2002) and the response of any species to changes in landscape attributes is poorly known and often assumed. Moreover, optimal management for one species may be the opposite for other species (Landres et al. 1988). Large carnivores, particularly wolves (Canis lupus), are often used as indicator species to identify corridors for many wildlife species and reduce landscape fragmentation (Noss et al. 1996; Bolck et al. 2004; Carroll 2006; van Maanen et al. 2006), but wolves, as habitat generalists, would adapt to any kind of habitat (Mech & Boitani 2003). Wolf mortality is caused mostly by direct human


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actions, and the assumption that the structural features of the landscape could act as a surrogate of human behavior has, for the moment, yet to be demonstrated. Even in the case of ENs for selected species, however, there are serious unresolved issues hindering their practical implementation. Key ecological and behavioral data (e.g., dispersal patterns, optimal habitat types) that are context-specific and measure variation are seldom available (Harris & Scheck 1991): use of gross averages over large areas will cause unknown and potentially farreaching errors (Bouwma et al. 2004). Wolves, for example, are known to disperse from only a few to more than 1000 km, and any gross average value would be of limited use. In addition, the often-articulated values given to the “permeability” or “optimality” of habitat types appears affected by the same basic weaknesses (Verboom & Pouwels 2004). As in most projects of conservation planning, the majority of data on species, habitat types, maps, and models are plagued by various degrees of uncertainty and are potential sources of error that will seriously affect analyses and output (Burgman et al. 2005). To date there is no consistent framework to account for data uncertainty. This is particularly problematic for ENs that are untested models whose outputs are used for practical applications. Nevertheless, sensitivity analysis could be applied to examine the uncertainty (Burgman et al. 2005). In general, the theory behind corridors does not extend to a body of practical indications on how to implement them (e.g., width, shape, content) to ensure their functionality. Bennett (1999) describes eight main issues relevant to the design of species-specific linkages and Noss and Daly (2006) describe methods to identify broad-scale corridors. These are useful guidelines, but a set of objective and prescriptive methods to identify corridors on a landscape scale and on the scale of species’ habitats is still lacking.

Evaluating ENs Bennett (2004) reports that more than 150 landscapescale or regional ENs are at various stages of development around the world and that no single EN has ever been assessed to measure levels of success (in ensuring connectivity and increasing biodiversity conservation). He believes that this is due to the fact that the effects of ENs are only measurable over large temporal scales, unlike corridor effects that can be measured at local scales and over short time periods (e.g., Biek et al. 2006; Chetkiewicz et al. 2006). Nevertheless, there are other reasons for this lack of evaluation. First, there are no explicit quantitative objectives that ENs can be tested against. Second, ENs are almost impossible to evaluate. In fact, although individual corridors may be evaluated (Nicholls & Margules 1991;

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Inglis & Underwood 1992), it would be necessary to provide evidence that demonstrates that an EN (i.e., the whole EN structure of several core areas, corridors, and buffer areas) has had an effect on some biodiversity value (e.g., richness, densities) in the presence of many confounding variables and in a continuously changing matrix. Nevertheless, if an EN were given a precise and quantified objective, it should be possible to gather evidence when the objective has been reached and this would allow at least some inference regarding the potential role played by the EN. The earliest ENs are more than 20–30 years old such as those Latvia, Lithuania, Estonia, and The Netherlands ( Jongman & Kristiansen 2001), and some evidence of their impact could already be obtained and could provide guidance on improving their design elsewhere. Modeling approaches without adequate validation (e.g., Bolck et al. 2004) provide insights but are a poor substitute for hard data when confirming the evidence of the effect. Although the contribution of ENs to biodiversity conservation is difficult to measure, several categories of metrics can be used to quantify connectivity, depending on the quantity and quality of data (Carroll 2006; Fagan & Calabrese 2006; Tracey 2006). Each category can be taken as an indication of the strength and reliability of the results of the connectivity project.

A Way Forward Some EN promoters in Europe acknowledge the problems of translating some concepts (e.g., corridors, connectivity, buffer, role of the matrix) into practical applications, but they state that “the current rate of decline of Europe’s biodiversity is such that it would be irresponsible to wait for detailed and incontrovertible evidence before taking action . . . and ENs are the necessary answer” (Council of Europe 2000). But in light of the limitations discussed earlier, it seems difficult to justify spending economic and political resources in building structures that cannot be evaluated after implementation. The fact that ENs certainly do no harm is insufficient because their planning and implementation take away funds from other conservation initiatives. To justify investing in their use, net benefits should be demonstrated. In spite of all the scientific weaknesses, ENs on a landscape scale have attracted much interest and resources in Europe for the following reasons. (1) The basic idea is good and intuitive. (2) They operate on a landscape scale and can be easily adopted by landscape planners who generally know little of ecology. Examples across scales have been widely and often wrongly used. (3) They offer an opportunity for politicians and governmental bodies to intervene, even if only at the planning stage. Regrettably, some land managers lack the ecological background (van Helsdingen 2000) to understand well the limitations and

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complexities of connectivity. (4) They offer an opportunity for transboundary cooperation, a politically sensitive concept in Europe. (5) They offer an alibi for not caring for nature in the matrix. Although difficult to prove, there is widespread anecdotal evidence that landscape planners and politicians prefer to focus on easily identifiable new structures instead of applying codes of conduct for the use of the matrix. (6) They have been strongly advocated by some EU governments. Nevertheless, poor definitions and the lack of a body of practical indications have prompted a variety of projects whose effectiveness for species conservation on a landscape level appears to be dubious. Moreover, focusing political energies and economic resources on ENs draws attention away from considering possible and more effective alternatives. Maintenance and restoration of connectivity is generally agreed to be an essential element in any conservation strategy and a complement to protected areas (Bennett et al. 2006; Noss & Daly 2006). In Europe this goal may best be achieved through a suite of environmental measures, such as the following, that are particularly relevant for European landscapes, even though they may suffer from some of the same weaknesses of ENs (e.g., lack of data and practical indication for implementation, poor evaluation). (1) Manage the environmental matrix through agrienvironmental measures funded by the European Commission (Kleijn & Sutherland 2003; Vickery et al. 2004) and through an expanded role for off-reserve conservation with innovative economic frameworks. (2) Maintain land mosaics through active maintenance and restoration of the landscape heterogeneity formed by centuries of farming and forestry and responsible for much of the current European biodiversity (Benton et al. 2003). (3) Expand and increase the efficiency of protected areas with a more systematic approach to ensure representation and, as far as possible, persistence of all species. (4) Apply and enforce a specific code of conduct (e.g., hunting, road access, responsible tourism) to obtain more effective public participation in conservation programs. Landscapes, especially when they are heavily influenced by humans, are constantly changing (e.g., Italy’s rate of land-use change in the last 30 years; Falcucci et al. 2007), and an adaptive approach to land management appears better suited to an evolving landscape than permanent structures such as ENs. This is particularly the case in Europe. Global changes will deeply affect European landscapes and biodiversity, and a flexible approach to land-use planning offers more opportunity to adapt human impacts to the changing and largely unpredictable scenarios. ENs should be maintained in the political agenda of the European countries as useful conceptual frameworks to reinforce a coherent perspective on biodiversity conservation, but we suggest that their study, design, and implementation follow a more rigorous logical approach, similar to what has been proposed by Margules and


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Pressey (2000) for systematic conservation planning. ENs can contribute substantially to nature conservation if their limitations are addressed explicitly and their hypotheses tested through evaluation. Nevertheless, more recently, a broader view of EN has been developed to produce a more multiobjective vision of the concept. The new general definition is as follows: “a coherent system of natural and/or semi/natural landscape elements that is configured and managed with the objective of maintaining or restoring ecological functions as a means to conserve biodiversity while also providing appropriate opportunities for the sustainable use of natural resources” (Bennett 2004). This new approach shifts the emphasis from an EN made of core areas and corridors to a multifunction multiobjective tool that is open to a more widely accepted vision of biodiversity conservation. This definition opens the door to a variety of modern techniques, such as those offered by systematic conservation planning that can help overcome at least some of the shortfalls of the current Pan European Conservation Strategy. Conservation is urgent in Europe and elsewhere, and there is no excuse for not using the most advanced tools available to make these conservation strategies as effective as possible.

Acknowledgments The Italian Ministry of the Environment (Directorate for Nature Protection) provided financial support. Literature Cited Beier, P. 1993. Determining minimum habitat areas and habitat corridors for cougars. Conservation Biology 7:94–108. Beier, P., and R. F. Noss. 1998. Do habitat corridors provide connectivity? Conservation Biology 12:1241–1252. Beier, P., K. L. Penrod, C. Luke, W. D. Spencer, and C. Cabanero. 2006. South Coast missing linkages: restoring connectivity to wildlands in the largest metropolitan area in the USA. Pages 555–586 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Belisle, M. 2005. Measuring landscape connectivity: the challenge of behavioural landscape ecology. Ecology 86:1988–1995. Bennett, A. F. 1990. Habitat corridors: their role in wildlife management and conservation. Department of Conservation and Environment, Melbourne, Australia. Bennett, A. F. 1999. Linkages in the landscape: the role of corridors and connectivity in wildlife conservation. World Conservation Union, Gland, Switzerland. Bennett, A. F., K. R. Crooks, and M. Sanjayan. 2006. The future of connectivity conservation. Pages 676–694 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Bennett, G., editor. 1994. Conserving Europe’s natural heritage: towards a European ecological network. Graham and Trottman/Martinus Nijhoff, London. Bennett, G. 1998. Guidelines for the development of the Pan-European Ecological Network. Council of Europe, Committee of Experts for the European Ecological Network. STRA-REP (98).6. Council of Europe, Strasbourg, France. Bennett, G. 2004. Integrating biodiversity conservation and sustainable use. Lessons learned from ecological networks. World Conservation Union (IUCN), Gland, Switzerland. Conservation Biology Volume 21, No. 6, 2007

Boitani et al.

Bennett, G., and P. Witt. 2001. The development and application of ecological networks: a review of proposals, plans and programmes. Report B1142. World Conservation Union (IUCN), Gland, Switzerland. Benton, T. G., J. A. Vickery, and J. D. Wilson. 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends in Ecology & Evolution 18:182–188. Biek, R., A. J. Drummond, and M. Poss. 2006. A virus reveals population structure and recent demographic history of its carnivore host. Science 311:538–541. Bischoff, N. T., and R. H. G. Jongman. 1993. Development of rural areas in Europe: the claim for Nature. Preliminary and background studies no. V79. Netherlands Scientific Council for Government Policy, SDU Publishers, The Hague. Bolck, M., G. De Togni, T. van der Sluis, and R. H. G. Jongman. 2004. From models to reality: design and implementation process. Pages 128–150 in R. H. G. Jongman and G. Pungetti, editors. Ecological networks and greenways: concept, design, implementation. Cambridge University Press, Cambridge, United Kingdom. Bonnin, M., D. Richard, H. Lethier, S. Rientjes, A. Bruszik, B. Delbaere, G. van Uden, and A. Terry. 2006. Draft report on the assessment of the setting up of the Pan-European Ecological Network. Council of Europe, Strasbourg, France. Available from http://www.coe.int/t/e/ cultural co-operation/environment/nature and biological diversity/ ecological networks/peen/3BelgradePeenReport EN.pdf (accessed February 2007). Bouwma, I. M., R. P. B. Foppen, and A. J. F. M. van Opstal. 2004. Ecological corridors on a European scale: a typology and identification of target species. Pages 94–106 in R. H. G. Jongman and G. Pungetti, editors. Ecological networks and greenways: concept, design, implementation. Cambridge University Press, Cambridge, United Kingdom. Breininger, D. R., and G. M. Carter. 2003. Territory quality transitions and source-sink dynamics in a Florida Scrub-Jay population. Ecological Applications 13:516–529. Bruinderink, G. G., T. van der Sluis, D. Lammertsma, P. Opdam, and R. Pouwels. 2003. Designing a coherent ecological network for large mammals in northwestern Europe. Conservation Biology 17:549– 557. Bunn, A. G., D. L. Urban, and T. H. Keitt. 2000. Landscape connectivity: a conservation application of graph theory. Journal of Environmental Management 59:239–255. Burgman, M. A., D. B. Lindenmayer, and J. Elith. 2005. Managing landscapes for conservation under uncertainty. Ecology 86:2007–2017. Carroll, C. 2006. Linking connectivity to viability: insights from spatially explicit population models of large carnivores. Pages 369–389 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Carroll, C., R. F. Noss, and P. C. Paquet. 2001. Carnivores as focal species for conservation planning in the Rocky Mountain region. Ecological Applications 11:961–980. Cavalchi, B., and G. Pungetti, editors. 2000. Verso la realizzazione di reti ecologiche in aree rurali. Agenzia Regionale Protezione Ambiente, Bologna, Italy. Chetkiewicz, C.-L. B., C. C. St. Clair, and M. S. Boyce. 2006. Corridors for conservation: integrating pattern and process. Annual Review of Ecology, Evolution, and Systematics 37:317–342. Cook, E. A., and H. N. van Lier. 1994. Landscape planning and ecological networks. Elsevier, Amsterdam, The Netherlands. Corsi, F., J. de Leeuw, and A. K. Skidmore. 2000. Modeling species distribution with GIS. Pages 389–434 in L. Boitani and T. K. Fuller, editors. Research techniques in animal ecology: controversies and consequences. Columbia University Press, New York. Council of Europe. 1996. The Pan-European biological and landscape diversity strategy, a vision for Europe’s natural heritage. Council of Europe, Strasbourg, France. Council of Europe. 2000. General guidelines for the development of the Pan-European Ecological Network. Nature and environment no. 107. Council of Europe Publishing, Strasbourg, France.

Boitani et al.

Crooks, K. R., and M. Sanjayan. 2006. Connectivity conservation: maintaining connections for nature. Pages 1–20 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Damschen, E. I., N. M. Haddad, J. L. Orrock, J. J. Tewksbury, and D. J. Levey. 2006. Corridors increase plant species richness at large scales. Science 313:1284–1286. Fagan, W. F., and J. M. Calabrese. 2006. Quantifying connectivity: balancing metric performance with data requirements. Pages 297–317 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. Annual Review of Ecology, Evolution and Systematics 34:487–515. Falcucci, A., L. Maiorano, and L. Boitani. 2007. Changes in land-use/landcover patterns in Italy and their implications for biodiversity conservation. Landscape Ecology 22:617–631. Fischer, J., D. B. Lindenmayer, and A. Cowling. 2004. The challenge of managing multiple species at multiple scales: reptiles in an Australian grazing landscape. Journal of Applied Ecology 41:32–44. Forman, R. T. 1995. Land mosaics: the ecology of landscapes and regions. Cambridge University Press, New York. Fuller, T. L., D. R. Foster, T. S. McLachlan, and N. Drake. 1998. Impact of human activity on regional forest composition and dynamics in central New England. Ecosystems 1:76–95. Haddad, N. M. 1999. Corridor and distance effects on interpatch movements: a landscape experiment with butterflies. Ecological Applications 9:612–622. Haddad, N. M., and J. Tewksbury. 2006. Impacts of corridors on populations and communities. Pages 390–415 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Haddad, N. M., D. R. Bowne, A. Cunningham, B. J. Danielson, D. J. Levey, S. Sargent, and T. Spira. 2003. Corridor use by diverse taxa. Ecology 84:609–615. Haila, Y. 2002. A conceptual genealogy of fragmentation research from island biogeography to landscape ecology. Ecological Applications 12:321–334. Hanski, I. 1999. Metapopulation ecology. Oxford University Press, Oxford, United Kingdom. Harris, L. D., and J. Scheck. 1991. From implications to applications: the dispersal corridor principle applied to conservation of biological diversity. Pages 189–220 in D. A. Saunders and R. J. Hobbs, editors. Nature conservation 2: the role of corridors. Surrey Beatty and Sons, Chipping Norton, New South Wales. Hilty, J. A., W. Z. Lidicker Jr., and A. M. Merenlender. 2006. Corridor ecology: the science and practice of linking landscapes for biodiversity conservation. Island Press, Covelo, California. Hindmarch, C., and J. Kirby. 2002. Corridors for birds within a PanEuropean Ecological Network. Nature and environment no. 123. Council of Europe Publishing, Strasbourg, France. Hobbs, R. J. 1992. The role of corridors in conservation: solution or bandwagon? Trends in Ecology & Evolution 7:389–391. Inglis, G., and A. J. Underwood. 1992. Comments on some designs proposed for experiments on the biological importance of corridors. Conservation Biology 6:581–586. Jongman, R. H. G. 1995. Nature conservation planning in Europe: developing ecological networks. Landscape and Urban Planning 32:170– 183. Jongman, R. H. G. 2004. The context and concept of ecological networks. Pages 7–33 in R. H. G. Jongman and G. Pungetti, editors. Ecological networks and greenways: concept, design, implementation. Cambridge University Press, Cambridge, United Kingdom. Jongman, R. H. G., and I. Kristiansen. 2001. National and regional approaches for ecological networks in Europe. Nature and environment no. 110. Council of Europe Publishing, Strasbourg, France. Jongman, R. H. G., and G. Pungetti, editors. 2004. Ecological networks

Ecological Networks

1421

and greenways: concept, design, implementation. Cambridge University Press, Cambridge, United Kingdom. Kauppi, P. E., J. H. Ausubel, J. Fang, A. S. Mather, R. A. Sedjo, and P. E. Waggoner. 2006. Returning forests analyzed with the forest identity. Proceedings of the National Academy of Sciences of the United States of America 103:17574–17579. Kleijn, D., and W. J. Sutherland. 2003. How effective are European agrienvironment schemes in conserving and promoting biodiversity? Journal of Applied Ecology 40:947–969. Lambeck, R. J. 1997. Focal species: a multi-species umbrella for nature conservation. Conservation Biology 11:849–856. Landres, P. B., J. Verner, and J. W. Thomas. 1988. Ecological uses of vertebrate indicator species: a critique. Conservation Biology 2:316– 328. Levey, D. J., B. M. Bolker, J. J. Tewksbury, S. Sargeant, and N. M. Haddad. 2005. Effects of landscape corridors on seed dispersal by birds. Science 309:146–148. Lindenmayer, D. B., and H. A. Nix. 1993. Ecological principles for the design of wildlife corridors. Conservation Biology 7:627–630. Lindenmayer, D. B., and J. Fisher. 2006. Habitat fragmentation and landscape change: an ecological and conservation synthesis. Island Press, Covelo, California. Lindenmayer, D. B., C. R. Margules, and D. Botkin. 2000. Indicators of forest sustainability biodiversity: the selection of forest indicator species. Conservation Biology 14:941–950. MacArthur, R. H., and E. O. Wilson. 1967. The theory of island biogeography. Princeton University Press, Princeton, New Jersey. McIntyre, S., and G. W. Barrett. 1992. Habitat variegation, an alternative to fragmentation. Conservation Biology 6:146–147. Mackovcin, P. 2000. A multi-level ecological network in the Czech Republic: implementating the Territorial System of Ecological Stability. GeoJournal 51:211–220. Maiorano, L., A. Falcucci, and L. Boitani. 2006. Gap analysis of terrestrial vertebrates in Italy: priorities for conservation planning in human dominated landscape. Biological Conservation 133:455–473. Maiorano, L., A. Falcucci, E. O. Garton and L. Boitani. 2007. Contribution of the Natura 2000 network to biodiversity conservation in Italy. Conservation Biology: in press. Margules, C. R., and R. L. Pressey. 2000. Systematic conservation planning. Nature 405: 243–253. Mech, L. D., and L. Boitani. 2003. Wolves: behavior, ecology and conservation. The University of Chicago Press, Chicago. Michal, I., and J. Plesnik, editors. 2002. National ecological network in the Czech Republic. A contribution to National Biodiversity Strategy and Action Plan. Agency for Nature Conservation and Landscape Protection of the Czech Republic, Prague, and IUCN, Gland, Switzerland. Millennium Ecosystem Assessment. 2005. Ecosystems and human wellbeing: biodiversity synthesis. World Resources Institute, Washington, D.C. Murphy, D. D., and B. R. Noon. 1992. Integrating scientific methods with habitat conservation planning: reserve design for northern spotted owls. Ecological Applications 2:3–17. Nicholls, A. O., and C. R. Margules. 1991. The design of studies to demonstrate the biological importance of corridors. Pages 49–61 in D. A. Saunders and R. J. Hobbs, editors. Nature conservation 2: the role of corridors. Surrey Beatty & Sons, Sydney. Niemi, G. J., J. M. Hanowski, A. R. Lima, T. Nicholls, and N. Weiland. 1997. A critical analysis on the use of indicator species in management. Journal of Wildlife Management 61:1240–1252. Noss, R. F. 1991. Landscape connectivity: different functions at different scales. Pages 27–39 in W. E. Hudson, editor. Landscape linkages and biodiversity. Island Press, Covelo, California. Noss, R. F., and L. D. Harris. 1986. Nodes, networks, and MUMS: preserving diversity at all scales. Environmental Management 10:299–309. Noss, R. F., and P. Beier. 2000. Arguing over little things: response to Haddad et al. Conservation Biology 15:1546–1548.


1422

Ecological Networks

Noss, R. F., and K. M. Daly. 2006. Incorporating connectivity into broadscale conservation planning. Pages 587–619 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Noss, R. F., H. B. Quigley, M. G. Hornocker, T. Merrill, and P. C. Paquet. 1996. Conservation biology and carnivore conservation in the Rocky Mountains. Conservation Biology 10:949–963. Novicki, P., G. Bennett, D. Middleton, S. Rientjes, and S. Wolters, editors. 1996. Perspectives on ecological networks. European Center for Nature Conservation, Tilburg, The Netherlands. Plesnik, I., editor. 1996. National and European ecological network in the Czech Republic. A methodological approach. Czech IUCN Project Coordination Unit, Prague. Pungetti, G., and B. Romano. 2004. Planning the future landscape between nature and culture. Pages 107–127 in R. H. G. Jongman and G. Pungetti, editors. Ecological networks and greenways: concept, design, implementation. Cambridge University Press, Cambridge, United Kingdom. ¨ Mander, and K. Sepp. 2004. Design of the Remm, K., M. K¨ ulvik, U. Pan-European Ecological Network: a national level attempt. Pages 151–170 in R. H. G. Jongman and G. Pungetti, editors. Ecological networks and greenways: concept, design, implementation. Cambridge University Press, Cambridge, United Kingdom. Rolstad, J., I. Gjerdde, V. S. Gundersen, and M. Saetersal. 2002. Use of indicator species to assess forest continuity: a critique. Conservation Biology 16:253–257. Sala, O. E., et al. 2000. Global biodiversity scenarios for the year 2100. Science 287:1770–1774. Simberloff, D., J. A. Farr, J. Cox, and D. W. Mehlman. 1992. Movement corridors: conservation bargains or poor investments. Conservation Biology 6:493–504. Smith, D. J. 2004. Impacts of roads on ecological networks and integration of conservation and transportation planning: Florida as a case study. Pages 73–93 in R. H. G. Jongman and G. Pungetti, editors. Ecological networks and greenways: concept, design, implementation. Cambridge University Press, Cambridge, United Kingdom. Soulé, M. E., B. G. Mackey, H. F. Recher, J. E. Williams, J. C. Z. Woinarski, D. Driscoll, W. C. Dennison, and M. E. Jones. 2004. The role of connectivity in Australian conservation. Pacific Conservation Biology 10:266–279. Taylor, P. D., L. Fahrig, and K. A. With. 2006. Landscape connectivity: a return to the basics. Pages 29–43 in K. R. Crooks and M. Sanjayan, ed-


Boitani et al.

itors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Theobald, D. M. 2006. Exploring the functional connectivity of landscapes using landscape networks. Pages 416–444 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Tracey, J. A. 2006. Individual based modeling as a tool for conserving connectivity. Pages 343–368 in K. R. Crooks and M. Sanjayan, editors. Connectivity conservation. Cambridge University Press, Cambridge, United Kingdom. Turner, M. G. 1989. Landscape ecology: the effect of pattern on process. Annual Review of Ecology and Systematics 20:171–197. Turner, M. G. 2005. Landscape ecology: what is the state of the science? Annual Review of Ecology and Systematics 36:319–344. Turner, M. G., R. H. Gardner, and R. V. O’Neill. 2001. Landscape ecology in theory and practice: pattern and processes. Springer, New York. Urban, D. L., and T. H. Keitt. 2001. Landscape connectedness: a graph theoretic perspective. Ecology 82:1205–1218. van Helsdingen, P. J. 2000. What can spiders expect from artificial manmade ecological corridors? Nature and environment no. 45. Council of Europe Publishing, Strasbourg, France. van Maanen, E., G. Predoiu, R. Klaver, M. Soulè, M. Popa, O. Ionescu, R. Jurj, S. Negus, G. Ionescu, and W. Altenburg. 2006. Safeguarding the Romanian Carpathian ecological network. A vision for large carnivores and biodiversity in eastern Europe. A&W Ecological Consultants, Veenwouden, The Netherlands, and Icas Wildlife Unit, Brasov, Romania. van Opstal, A. 1999. The architecture of the Pan-European ecological network. Report 37. National Reference Centre for Nature Conservation, Wageningen, The Netherlands. Verboom, J., and R. Pouwels. 2004. Ecological functioning of ecological networks: a species perspective. Pages 56–72 in R. H. G. Jongman and G. Pungetti, editors. Ecological networks and greenways: concept, design, implementation. Cambridge University Press, Cambridge, United Kingdom. Vickery, J. A., R. B. Bradbury, I. G. Henderson, M. A. Heaton, and P. V. Grice. 2004. The role of agri-environment schemes and farm management practices in reversing the decline of farmland birds in England. Biological Conservation 119:19–39. Wilcove, D. S., D. Rothstein, J. Dubow, A. Phillips, and E. Losos. 1998. Quantifying threats to imperilled species in the United States. BioScience 48:607–615.