Does structural connectivity facilitate effective dispersal of native species in Australia’s fragmented terrestrial landscapes? (systematic review)
Habitat loss and fragmentation present increasingly serious problems in the context of global climate change, as smaller populations will be less resilient and isolated populations will have difficulty shifting their ranges to track changing environments. A potential solution is to provide structural connectivity—elements of the landscape (typically some form of native vegetation) that physically link isolated patches of habitat. According to metapopulation theory, these linkages will allow individuals and/or their genes to disperse between multiple small patches, allowing these subpopulations to collectively function as larger, more resilient metapopulations. Structural connectivity includes the concept of wildlife “corridors” (linear, continuous connections between patches), but also encompasses a wide variety of landscape elements in the form of corridors, disconnected linear elements that do not directly connect patches, and “stepping stones”— series of isolated features such as individual trees, shrubs, rocky outcrops or small clusters of these features. However, it is unclear whether structural connectivity really does facilitate the movement of native animals and plants between patches (and thus provide functional connectivity), or if particular characteristics of structural connectivity influence its effectiveness. Protection and restoration of structural connectivity is already being recommended across Australia, but given the lack of consensus on the relationships between structural and functional connectivity, specific guidelines for managers are lacking. The purpose of this review was to synthesise all available evidence on the relationship between structural connectivity and landscape-scale dispersal movements in Australian terrestrial landscapes in order to identify knowledge gaps and, if possible, to devise general principles for connectivity restoration.
Our primary question was:
- Do the various landscape elements that provide structural connectivity in Australian fragmented terrestrial landscapes facilitate dispersal of native species between habitat patches or populations? i.e., do they provide true functional connectivity?
Because we were particularly interested in knowing what form structural connectivity should take in order to be most effective, we also asked the secondary questions:
- Do the various landscape elements that provide structural connectivity differ in how well they facilitate dispersal of individuals between habitat patches or populations?
- What particular characteristics make structural connectivity most effective?
Finally, the effectiveness of structural connectivity may depend not just on its form but also on the species and ecosystem in question. Thus, we aimed to consider whether the effectiveness of different types of connectivity varies among taxonomic groups or other species categories (such as habitat specialists vs. generalists), and between temperate and tropical ecosystems.
Electronic searching using a pre-defined series of search terms was completed in May and June of 2008 using the following databases, catalogues and web-engines: ISI Web of Knowledge (including ISI Web of Science, ISI Proceedings, Current Contents, CAB Abstracts, Zoological Record, and Web Citation Index), Directory of Open Access Journals, Scopus, Australian Agriculture and Natural Resources Online (AANRO), CSPubList (via EnCompass; official CSIRO publications), CSIRO Library Catalogue (Voyager), Australasian Digital Theses Program, ProQuest Dissertations and Theses, Google Scholar, and AllTheWeb. A special protocol was developed to search for grey literature via university libraries, departments, and state and federal governmental organisations involved in environmental research. Bibliographies of articles viewed at full text, particularly narrative literature reviews, were searched for additional relevant sources. Experts were widely consulted in the development of the review protocol, resulting in the inclusion of two sources of unpublished data in the review.
Studies were included in the review if they:
- contained data on any terrestrial native Australian species;
- and had at least one study site that contained some type of structural connectivity (spatial heterogeneity) between otherwise isolated patches of native habitat;
- and contained data on movement of species through the connectivity or data that allowed inference of movement (e.g., presence in the connectivity, population genetic data, presence/absence in patches with different types or degrees of connectivity).
Data collection and analysis
The selection criteria were met by 98 sources, representing 80 different studies. As the vast majority of studies did not directly test the primary question of the review, but contained data that could allow it to be evaluated, raw data rather than statistical results were extracted for each species included in each study. These included whether or not there was evidence for movement (or presence) of the species in the structural connectivity, whether or not there was evidence for movement (or presence) of the species in the matrix if that was also studied as a control, as well as the quality of the evidence (e.g., the degree to which movement was directly assessed versus inferred based various assumptions). A suite of other variables was extracted describing the species, the characteristics of the structural connectivity, and the general environment. Additional data on gap distances crossed, either between small elements of structural connectivity or between both structurally connected and isolated patches were also extracted where possible. Almost none of the studies provided data suitable for meta-analysis, so exploratory analyses using summary statistics and hierarchical modelling were undertaken instead.
The 80 studies included in the review varied enormously in their goals, methodologies, and theoretical frameworks and they measured responses to structural connectivity using more than two dozen different response variables. Too few studies were available on plants or invertebrates to include them in most of our analyses. Almost all studies were conducted in wooded habitat patches and/or in structural connectivity consisting of trees, so relatively little can be concluded about grassland or other non-treed ecosystems. Furthermore, the vast majority of studies only assessed the presence of species within structural connectivity without directly examining movement of species through the connectivity and thus probably tell us more about the value of connectivity as habitat rather than its effectiveness at facilitating movement. Despite these limitations, our exploratory analyses were able to reveal a few clear messages as well as some interesting patterns that suggest foci for future research.
Does structural connectivity help? Native species were more likely to be present in elements of structural connectivity than in the matrix, providing reasonable evidence that these landscape features provide habitat for these species, though only weak evidence that they facilitate dispersal movements. However, studies with specific evidence of movement between patches also generally found that the presence of structural connectivity increased the rates and/or likelihood of such movement. Both simple contingency analyses and HGLM (mixed) models confirmed that increased amounts of structural connectivity were correlated with increased movement between patches. Thus, we found considerable support for a positive answer to the review’s primary question (i.e., structural connectivity generally did facilitate greater functional connectivity).
Which types of structural connectivity (corridors, stepping stones, etc.) are better? All forms of structural connectivity for which there were sufficient data for analyses were effective to some degree in both providing habitat and in facilitating movement. In terms of providing habitat, our exploratory analyses suggest that while all forms were better habitat than matrix for most species, continuous corridors were better than discontinuous linear elements which were better than stepping stones. However, in terms of facilitating movement, our analyses suggest that stepping stones (generally, these were scattered paddock trees) were at least as effective if not more effective than continuous corridors.
Does the effectiveness of these different structures vary among ecosystems and species?
Effectiveness of structural connectivity at providing habitat varied somewhat according to the environment and the species. Species that disperse terrestrially were less likely to be found living between habitat patches, but where they were found between patches, they were significantly more restricted to elements of structural connectivity (as opposed to the matrix) than aerial dispersers. Similarly, habitat specialists were less likely to be present between patches, but when present were significantly more restricted to disconnected linear element and corridors than habitat generalists. Corridors were less likely to be used as habitat in tropical ecosystems than in temperate ones, and disconnected linear elements were more likely to be used as habitat when they were wider. Both types were less likely to contain reptile species (relative to other taxonomic groups), possibly because most studies focused specifically on wooded landscape elements, which may not constitute habitat for many of the reptiles studied. Interestingly, width had a significant effect on the likelihood of occupancy of disconnected linear elements but no effect on occupancy of continuous corridors.
In general, there were insufficient data and/or variability in the data to assess variation in the effectiveness of the different forms of structural connectivity at facilitating movement. However, similar to our analyses of connectivity as habitat, we did find evidence that wooded corridors were less likely to facilitate movement by reptiles relative to other taxonomic groups. Birds and mammals appeared to have similar responses to structural connectivity, and both groups appeared to be slightly more likely to move through stepping stones (scattered trees) than corridors.
Are gap distances and distances between patches important? Data on critical gap-crossing and interpatch-crossing distance thresholds could be estimated for only a subset of studies and most of these estimates were based on relatively small sample sizes. Based on these limited data we calculated a mean gap-crossing threshold of 106m, indicating that many species are unable to cross open areas (i.e., matrix) that exceed this distance. We also calculated an interpatch-crossing threshold of 1100m, indicating that many species are unable to disperse between patches of habitat separated by >1100m, even where structural connectivity exists between the patches. While it must be reiterated that these threshold values are based on limited data that come primarily from bird and mammal species inhabiting wooded habitats, they should provide a useful starting point for future connectivity research, modelling and planning.
Research implications: Structural connectivity can serve multiple functions in a landscape, providing additional habitat but also facilitating dispersal movements and gene flow between larger patches of habitat. The distinction between these two functions of connectivity is critical because the vast majority of data on the use of structural connectivity by Australian native species have focused on presence in connectivity and thus tested whether the connectivity was providing habitat (94% of the data in this review fall into this category). Yet conclusions are often drawn and management actions undertaken as though the movement function was tested, despite the fact that such tests have rarely been performed. To redress this imbalance more research is urgently needed that examines movements of a wide range of native species (including invertebrates and plant seeds and pollen) through a wide range of heterogeneous, “real” landscapes (including grassland and shrubland systems). Studies should be designed to consider multiple forms of structural connectivity in a comparative framework, to gather data on a large sample of individuals (even where this means limiting the number of species examined in any single study) and to aim for meaningful replication with entire landscapes acting as replicates. Data collection should be particularly focused on recording the details of precise movement paths, accurately characterising all elements of structural connectivity (and the matrix itself) through which movements do and do not occur, and assessing effective dispersal (i.e., post-dispersal contribution to the gene pool). Such data will be critical for developing a meaningful understanding of how different types of structural connectivity contribute to true functional connectivity, and ultimately allow managers to accurately weigh the costs and benefits of different options for preserving or restoring such connectivity.
Management implications: Until the research gaps described above are filled, many aspects of functional connectivity will remain poorly understood. However, management efforts must continue armed with the best available knowledge. Thus, we have attempted to provide guidelines for managing and restoring structural connectivity with the caveat that more research is still needed, so all of our recommendations are intended to be applied in an adaptive management framework. It is particularly important to reiterate that most of the data on which our recommendations are based come from studies of Australian mammals and birds living in woodland and forest ecosystems. Our guidelines (see attached “Summary of Guidelines for Connectivity Management and Restoration” and the full review for more detail) should thus be most applicable in similar systems and applied more broadly only with caution.
This systematic review of available empirical evidence suggests that structural connectivity is currently providing some benefit for native species in Australian landscapes, but that with better information resulting from new research, these benefits and their cost-effectiveness could be significantly improved. Although limited, currently available data indicate that the effectiveness of connectivity initiatives could be enhanced for many species by considering diverse types of structural connectivity (particularly scattered trees separated by no more than ~100m) and by targeting patches less than 1.1km apart for connectivity protection and restoration.
The modification, loss and fragmentation of natural ecosystems are among the most serious threats to global biodiversity because the resulting altered landscapes invariably support smaller, more isolated populations of native species and increasingly degraded habitats, all of which are likely to reduce population viability and increase risk of extinction. Habitat fragmentation is thought to impact populations through three main effects: edge, area and isolation effects. Edge effects can include increased rates of predation and altered microclimates which may reduce survivorship and reproductive success. Due to the smaller habitat patches and thus smaller populations created by fragmentation, area effects may include increased levels of inbreeding, reduced genetic variability, and increased sensitivity to stochastic events. These area effects will be further intensified when combined with isolation effects, whereby the possibility of demographic or genetic rescue is reduced or eliminated because individuals cannot disperse between fragments through the matrix of unsuitable habitat. Extensive research has demonstrated these impacts of fragmentation, and numerous syntheses have been produced, so the basic problem is relatively well understood (e.g., Wilcove 1985; Wilcox & Murphy 1985; Rolstad 1991; Harrison & Bruna 1999, Debinski & Holt 2000; Villard 2002; McGarigal & Cushman 2002; Lindenmayer & Fischer 2006; Fischer & Lindenmayer 2007).
Fragmentation is an even more serious concern now that we know the planet’s climate is changing, as global climate change is predicted to force species to locally adapt or move elsewhere in order to survive (Davis & Shaw 2001; Gitay et al. 2002; Parmesan 2006). Yet smaller populations will be less resilient to altered local conditions and therefore less able to adapt, and isolated populations will have difficulty shifting their ranges to track changing environments. This may be of particular concern in Australia, where extensive land clearing was conducted following European settlement, leaving fragments of remnant native vegetation within a matrix dominated by agricultural production systems (Saunders 1989; Bennett & Ford 1997). The long-term consequences of this fragmentation are expected to be serious with at least some researchers predicting that Australia will lose half of its bird species within the next century (Recher 1990).
Action is therefore urgently needed to reverse some of the effects of fragmentation—to reconnect small, isolated populations and restore their ability to function as larger, more resilient populations. Such actions need to occur at local, regional, and even continental scales to ensure benefits accrue at the population level but also that species can move to new areas as necessary under climate change. Fortunately, this need has captured the attention of government and the public. Connectivity restoration is frequently a goal of private revegetation efforts, local landcare groups, and incentive schemes administered by regional natural resource management bodies. Almost two decades ago, authors first proposed large networks of connected habitats in North America (Harris & Gallagher 1989) and Australia (Hobbs & Hopkins 1991), and the Australian Government and non-governmental organisations have recently initiated a number of major projects involving continental scale connectivity restoration such as Gondwana Link and the Great Eastern Ranges Initiative (formerly known as Alps to Atherton), including its component projects such as Kosciusko- to-Coast and Slopes-to-Summit.
The difficulty is that it is unclear exactly what actions should be taken to restore connectivity to our landscapes, aside from trying to recreate vast swaths of native ecosystems (which would not be practicable given the need for other land uses). By definition, a connected landscape is one in which individuals of all species (or their propagules or genes) can move or disperse from one resource patch to another (see Appendix B for definitions of terms used in this protocol). So how much habitat, what kind of habitat, and in what spatial configuration might be required to facilitate such dispersal? Unfortunately, the many syntheses of the problems of habitat fragmentation tell us relatively little about dispersal, and thus about the appropriate solutions to the problem, and new research and syntheses specifically focused on connectivity, as opposed to fragmentation, are required.
The most commonly proposed solution is to retain or restore habitat corridors. While the interpretation of this term varies (see Simberloff et al. 1992 for six different definitions), we define a corridor as a relatively unbroken (contiguous) linear strip of habitat that connects two or more patches of habitat that are otherwise surrounded by unsuitable areas for the species or community in question (Saunders & de Rebeira 1991; Hobbs 1992; Beier & Noss 1998). We believe this matches the operational definition used by most Australian land managers and by members of the public. The theory behind corridors is that individuals will be exchanged and/or genes will flow between connected patches or populations either because the corridor is occupied by the species or community and thus the corridor creates a continuous population between the two patches, or because dispersing individuals (or seed dispersers or pollinators) will use the corridor to move from one patch to the other. However, the ability of corridors to achieve this goal, and provide for dispersal just as much as continuous habitat would, may depend very much on the dispersal behaviour of the species involved as well as many other characteristics of the corridors themselves, the habitat patches, and the surrounding matrix (Tischendorf & Wissel 1997; Lindenmayer 1998; St Clair et al. 1998; Heinz et al. 2007). As a result, the effectiveness of corridors has been the subject of considerable debate (Noss 1987; Simberloff & Cox 1987; Simberloff et al. 1992; Beier & Noss 1998; Haddad et al. 2000; Hannon & Schmiegelow 2002; Damschen et al. 2006), and there is an imperative to determine which characteristics might make them most effective across different species and even different ecosystems, and whether there are alternatives.
There are a number of ecological reasons which suggest that alternatives to corridors need to be seriously considered. First, if corridors are to provide for gene flow by providing occupied habitat, then there may be costs to the populations involved, so a thorough weighing of the balance between benefits and costs is required. In particular, edge effects in narrow habitat strips may mean that population sinks may be created when corridors are occupied (Lynch et al. 1995; Cale 1999; Hess & Fischer 2001). Such sinks could potentially decrease both the likelihood of dispersal between patches and the overall viability of the population, even though the corridor might appear to be a success because it is occupied. Second, the corridor concept is based on a binary patch/matrix model of the landscape—that there are distinct, suitable parts of a landscape (patches) and unsuitable parts (matrix), but nothing in between. However, ecologists now recognise that there are other valid landscape models, including the variegated model (McIntyre & Barrett 1992; McIntyre & Hobbs 1999) and continuum models (Manning et al. 2004; Fischer & Lindemayer 2006), in which different parts of the landscape may vary in their suitability for any given species, resulting in different densities or patterns of use. These models are particularly important in Australia, as many of Australia’s ecosystems naturally form a patchy mosaic (e.g., Bentley & Catterall 1997), so native species may have evolved to take advantage of that heterogeneity during dispersal. This means that individuals may not require continuous strips of habitat for dispersal, and also that suitable habitat for dispersal might actually have a very different composition and structure than habitat suitable for long-term survival and reproduction.
The increased appreciation of these ecological concepts has led scientists to broaden their thinking about connectivity restoration beyond corridors and into the paradigm of structural vs. functional connectivity (With et al. 1999; Uezu et al. 2005; Crooks & Sanjayan 2006; Hilty et al. 2006). Under this new paradigm, structural connectivity is anything that physically links separate populations, and it may consist of just about any kind of landscape heterogeneity in between occupied patches of habitat. Examples of structural connectivity include corridors and partially vegetated drainage lines or fence lines, but it may also consist of more subtle habitat elements such as scattered trees or shrubs, or even scattered clumps of tussock grass or coarse woody debris. In contrast, functional connectivity refers to the outcome we desire from these structural features—the degree to which movement and dispersal actually occur. Research is now focused on trying to understand the relationships between structural and functional connectivity, which includes work on corridors but is more broadly focused on movement and gene flow in heterogeneous landscapes. In other words, we need to know exactly which types of structural connectivity really do provide functional connectivity (dispersal in the landscape) for the majority of species in an ecosystem.
These general principles for connectivity restoration—recommendations for what is likely to work for most species in most systems—can only come from syntheses of many empirical studies. A synthesis that incorporates a variety of types of structural connectivity, not just corridors, has yet to be performed. While the utility of corridors has been tested using theoretical modelling (e.g., Hanson et al. 1990; Tilman et al. 1997), and empirical evidence for use of corridors has been accumulating for a number of years (Saunders & Hobbs 1991; Beier & Noss 1998; Bennett 1998; Haddad et al. 2003; Davies & Pullin 2007), research on other types of structural connectivity is relatively recent. Furthermore, recent evidence comes from a variety of different types of studies (survey, mark-recapture, genetic, radiotracking, etc.), which can make the resulting conclusions difficult to interpret across studies. Thus, the time is ripe to attempt a synthesis of the relationships between structural and functional connectivity, particularly in Australia where there may be considerable variation in structural connectivity and how it is used by native species. The systematic review approach may be especially useful, as it provides a rigorous framework in which to attempt a formal comparison of the different types of evidence produced by different types of studies. These are our goals in this review, with the ultimate aim of providing clearer, science-based information to natural resource planners and managers about how best to invest in connectivity, and to identify critical knowledge gaps that will guide future research to ensure that Australia’s significant on-ground expenditures achieve their goals of restoring functional connectivity in Australian landscapes.