Bruce Webber, CSIRO Ecosystem Sciences, Private Bag 5, Wembley, WA 6913, Australia. E-mail: email@example.com
The ability to ascribe native or alien status to species in a rapidly changing world underpins diverse research fields that overlap with global change and biological invasions via biodiversity. Current definitions generally link alien status to anthropogenic dispersal events, but this can create conflicts for active management and global change adaptation strategies, such as managed relocation and restoration ecology. Here we propose a unifying approach that allows for the incorporation of rapid global change into biological invasion terminology. We introduce the concept of a projected dispersal envelope (PDE) to define the region where a species is or could be native, irrespective of human involvement. The PDE integrates biogeography and niche theory with existing invasion terminology to place a spatial and temporal context on species movements. We draw on a diverse suite of topical organism movements to illustrate these concepts. Our restructured definitions allow for native species to move into or with rapidly shifting climatic regions, as well as identifying the inappropriate introduction of alien species to new areas. Moreover, our definitions framework forms a timely and essential component of adaptation policies and responses for invasive species management and the enhancement of biodiversity in a rapidly changing world.
At the intersection of research on global change and on biological invasions it is becoming increasingly clear that there is a fundamental problem – how do you define whether a species is native or alien in a rapidly changing global environment (Preston, 2009; Walther et al., 2009)? Resolving this question is important not only for invasion biology, but also for biodiversity management strategies that involve the deliberate human-mediated movement of species to new areas. Reaching common consensus on a functionally relevant set of definitions may not be possible if: (1) all anthropogenic dispersal events are ascribed alien status (CBD, 2002; Davis, 2009); (2) the temporal divide separating native range shifts from alien introductions is not explicitly addressed (Valéry et al., 2008); or (3) the magnitude of natural species movements in a rapidly changing climate blurs the ecological distinction between disjunct and adjacent regions donating and receiving organisms (Lockwood et al., 2007; Sorte et al., 2010).
All extant species have the potential to expand their geographic range (Wilson et al., 2009); an important attribute given that the current global climate is changing at an unprecedented rate (Joos & Spahni, 2008). It is anticipated that entire biomes will shift, and for species to survive, populations will be required to track suitable climates, some at rates that most extant organisms will never have experienced before (Loarie et al., 2009). There are four recognized trajectories of species response to significant climate change. Species may migrate with the climate they currently experience, be resilient (tolerating novel climates), evolve (improving capacity for resilience or migration) or they may become extinct (Walther et al., 2002). Anthropogenic landscape modification adds a further layer of complexity to the likelihood of any one trajectory being realistic (Hobbs et al., 2006; Hoegh-Guldberg et al., 2008). In the ‘anthropocene’, rapid climate change and an inability to shift with suitable climates, combined with a lack of tolerance or ability to adapt to ecosystem change, may make extinction a more common outcome (Brook et al., 2008). Yet counter-measures of adaptation to global change to avoid extinction, such as managed relocation, are often in apparent conflict with the common approach to tie alien status to human-mediated species movements. Relocated populations may therefore be subject to regulatory control (Shirey & Lamberti, 2010).
Widely accepted definitions that implicitly allow for some level of anthropogenic dispersal without the ‘alien’ tag, couch their terminology in a framework of human versus ‘natural’ dispersal (IUCN, 2000; Richardson et al., 2000; Pyšek et al., 2004). Furthermore, such definitions have added an increasing number of global change caveats, such as anthropogenic climate change and landscape modification, which are now considered not to influence alien status (Pyšek et al., 2004). The end result is that these particular definitions are commonly interpreted to imply that all human-mediated movements are alien and the caveats are often overlooked (e.g. Davis, 2009; Preston, 2009; Walther et al., 2009). Moreover, such definitions do not allow for managed relocations of taxa with poor dispersal ability that require relatively large displacements to track climatically suitable regions under rapid climate change. The interaction of climate-driven range shifts with anthropogenic landscape modification further complicates the application of existing definitions (Manning et al., 2009). In this Ecological Sounding, we propose a definition of native (indigenous) and alien (exotic, introduced) species that can be applied independently of anthropogenic impacts on natural ecosystems, and the rate or magnitude of climate change and other rapidly changing drivers of species distributions.
THE PROJECTED DISPERSAL ENVELOPE
Central to our approach for defining native and alien status is the concept of a ‘projected dispersal envelope’ (PDE; Fig. 1). The PDE describes the area in which a dispersal unit (i.e. propagules or individuals) or population of a species could be found, based on natural dispersal or migratory traits (Nathan et al., 2008) in a given time frame. Thus, populations of a species have ‘native’ status within an area defined by the cumulative PDEs of progeny that are spatially or temporally contiguous with the species’ original distribution. Conversely, populations of a species have ‘alien’ status when found outside the PDEs of populations with native status. The PDE concept considers population range shifts and size changes as well as movement potential over time, defines the area of the potential dispersal unit shadow for a species population at a given time for a nominated period, and has two primary components.
First, a PDE is constructed around dispersal traits and natural dispersal vectors, both extant and extinct, for all native individuals and populations. PDE margins are defined by natural mechanisms that could move the dispersal unit the furthest distance in its native range, and PDEs for populations could be combined in an additive way to produce an overall PDE for a species. Our definition assumes that novel species interactions and landscape modifications (natural or anthropogenic), can only increase the PDE, as all previous movement in the native range is still considered theoretically possible even if it is not under current circumstances (e.g. if agriculture has introduced physical barriers, or if a seed-dispersal vector is now extinct). When deciding whether a dispersal unit or population is native or alien, our definition recognizes that identifying the mechanism of actual movement of a dispersal unit is problematic and largely unrealistic (Wilson et al., 2009). Therefore, it is the position of the dispersal unit relative to the PDE, not the mechanism of movement, which is important for assessment decisions.
Second, PDEs have a temporal component and can therefore be used not only for interpreting present-day biological invasions, but also for projecting possible species range shift scenarios (forecasting, hindcasting), such as previous expansion from glacial refugia (Davis & Shaw, 2001; Nogués-Bravo, 2009). Establishing the current PDE (i.e. a point-in-time assessment) for an existing population draws on the native home range or migratory potential for a mobile species, or the distance of a single propagule dispersal event for species with mostly immobile life stages. A temporally projected PDE is defined by the sum of all possible dispersal or migratory events in the period under consideration (Fig. 1). For example, a point-in-time assessment would only involve a PDE for the current generation (PDE0, Fig. 1), whereas a temporal projection for a population would involve a cumulative PDE (PDE0–x, Fig. 1) for as many generations that are possible in the time frame under consideration. It may be that a projected PDE is not a linear extrapolation of a single movement multiplied by the number of movements possible in the period considered, as dispersal or migratory ability can change spatially and temporally.
It is not possible to be generally prescriptive as to what is a feasible distance for natural dispersal because it is context related. That is, the context relates to the distance within a given time period for a set of case-specific parameters – thus requiring human judgement and depending on a case built with available knowledge (e.g. Gubili et al., 2011). In practice, for certain species it may prove challenging to provide concrete parameters for defining PDEs, due to the difficulty of factoring in events such as jump-dispersal and changes to dispersal barriers over time. Critically, any PDE construction process should be evidence based, transparent, grounded in theory and open to revision when new information becomes available, so as to resolve the inevitable differences of opinion over alien or native status for controversial or problematic species (e.g. the dingo; Savolainen et al., 2004). As for existing definitions, there will be a gradual transition from populations clearly defined as alien to those that are indisputably native. Outliers in population dispersal curves corresponding to human-mediated movements beyond ‘a potential range as defined by their natural dispersal mechanisms and biogeographic barriers’ (Richardson & Pyšek, 2006) should remain classified as alien introductions (Table 1). The ability to identify such inter-PDE (i.e. alien) movement events should improve with increasing synergy between the fields of invasion biology, movement ecology (Nathan et al., 2008) and palaeoecology (Froyd & Willis, 2008), among others.
Table 1. Example scenarios for native and alien species movements.
Implicit in our definition is the decoupling of alien status from all human-mediated dispersal events; an association that is over-simplified at best and confusing in extant ecosystems. We consider it unrealistic to draw a global line between early humans as natural dispersal vectors and their gradual transition into an ‘external problem’ driving global biological invasions (Mack, 2001; Bean, 2007) and even influencing natural range shifts through landscape modification by the removal or addition of dispersal barriers (Vermeij, 1991; Opdam & Wascher, 2004).
A framework of possible movement scenarios can thus be inferred from this set of guidelines and represented spatially using Hutchinsonian realized and Grinnelian fundamental niches (sensuSoberón, 2007) with a temporal context (Fig. 2; examples in Table 1). To maintain a native status, dispersal units from a native source under consideration (A1) can only be dispersed within the PDE of that source (Fig. 2). This definition includes dispersal of propagules from the current population into nearby existing populations (A1 to A2), examples of which require detection of gene flow (maternal for immobile organisms) since populations are usually morphologically indistinguishable between locations. It could also include dispersal into existing suitable areas that are currently uncolonized (A1 to A3), such as after the removal of a geographical barrier through landscape modification or through opportunistic long-distance dispersal events. The A1 to A3 scenario is critical in the context of adaptation to global change, as it incorporates assisted migration. Taking into account temporal projections, a current population may be displaced, due to shifting niche suitability, to a contiguous area in a projected timeframe (A1 to A4). Species range expansions over time are in this category. If temporal projections suggest that a population is currently situated (A5), or either an artificially maintained population (A6) or dispersed propagules (A1 to A7) will be situated, within the projected fundamental niche, then these individuals should be considered native. In the A5 scenario, a species maintains its realized niche despite the fundamental niche changing radically. This could be interpreted as resilience to change; however, the species has effectively migrated with respect to the fundamental niche. If a propagule is dispersed outside both its existing and projected fundamental niches, but within the PDE for the temporal projection (A1 to A8), then the propagule should still be considered native, even if it is unlikely to survive and establish.
Conversely, propagules from a source population dispersed to a location outside the PDE for a given scenario are always considered alien (i.e. movements from PDEA1 to PDEB1; Fig. 2). The alien label not only applies to the dispersed propagules, but any progeny they subsequently produce, including novel species and hybrids. Propagules deemed to be alien include those dispersed outside their PDE to either other current populations (A1 to B1), to uncolonized areas within the fundamental niche found elsewhere (A1 to B2), or to a projected fundamental niche (A1 to B3). The A1 to B1 movement scenario would again require detection of gene flow and may be difficult to detect, while the A1 to B2 scenario represents the most common example of alien species introductions.
A BROADER TERMINOLOGICAL CONTEXT
Our proposed niche-dispersal classification framework complements existing definitions and concepts used in invasion ecology and conservation biology. For invasion ecology, it formalizes key components of the ecological–phytogeographical–historical (EPH) approach to plant origins (Webb, 1985; Bean, 2007) and operates at the first ‘introduction’ step of the ‘invasion pathway’ (Richardson et al., 2000) or prior to ‘Stage 0’ of the ‘neutral invasional framework’ (Colautti & MacIsaac, 2004). The concepts outlined here are therefore complementary to the subsequent possible steps of naturalization and invasion for alien species, as well as being applicable to range shifts in native species. Our definitions framework also allows conservation biology terminology (e.g. Shirey & Lamberti, 2010) to give ecologically relevant meaning to discrimination between human-assisted translocation and various levels of managed relocation. Relative to commonly applied existing terminology for native and alien status (IUCN, 2000; Richardson et al., 2000; CBD, 2002; Pyšek et al., 2004), our framework is in broad agreement with existing alien definitions, but provides more pragmatic insight into movements that should be viewed as native range shifts, rather than alien introductions, in an era of rapid global change (Table 1).
SPECIES MOVEMENT AND GLOBAL CHANGE
Our approach to defining native and alien species can be applied independently to the rate or magnitude of global change. It takes into account the two significant anthropogenic influences on species distributions (climate change and landscape modification) and is equally applicable to assessing population range shifts where impacts of anthropogenic global change are minimal – for example, where humans have removed previous geographical barriers spatially separating fundamental niches (Vermeij, 1991), allowing for rapid range expansion in a way that mirrors previous natural events (Garcia-Castellanos et al., 2009). In contrast, the addition by humans of considerable geographic barriers in the landscape (Chase & Griffin, 2009) has had a significant impact on the ability of species to shift with suitable climates (Hoegh-Guldberg et al., 2008).
Active management strategies, such as the facilitated movement of populations from areas projected to be unsuitable under future climates (Harris et al., 2006), are a logical answer to restore fluidity (sensuManning et al., 2009) in fragmented landscapes, yet managed relocation strategies have an alien status according to many definitions currently used. This conflict of interests has considerable implications when existing legislation requires the control of alien species. Our proposed definition set allows for carefully considered managed relocations to be viewed as a range extension rather than as an alien introduction. In reality, managed relocation (albeit within a PDE) can be seen as speeding up a range shift that may have occurred naturally if current climate change had been operating at rates experienced for the majority of the Holocene. Regardless of the underlying dispersal mechanism, range shifts within a PDE for native species can now be excluded from the possibility of being classified as an alien incursion.
A further consequence of the intersection of rapid global change and landscape modification is that complex interactions between native and alien species will be more prevalent. For example, novel ecosystems will become an increasingly common part of the landscape (Hobbs et al., 2006). Many existing definitions don't allow for organisms in novel ecosystems to be native. Although both native and alien species may be present in these novel environments and both groups could be invasive, our new definitions allow range-shifting species (including those that have moved through appropriate managed relocation) to be native in novel ecosystems. Similarly, our definition avoids the paradox of splitting dispersal due to interactions with other alien species (an indirect unintentional form of human-mediated transport) from native distribution vectors.
FUTURE MANAGEMENT OF NATIVES AND ALIENS
Current policies for managing native and invasive species are unlikely to be adequate in an era of rapid global change (Shirey & Lamberti, 2010). The implications of concepts covered by our proposed definitions may require a re-thinking of policy, which will not happen unless there is prior recognition of how global change influences our view of ‘nativeness’. Defining native and alien status has different implications for many fields that rely on differentiation between native and alien populations. For example, pest or weed risk assessments used to determine the location and level of quarantine required for trade and biodiversity protection may need modification to take into account species PDEs. Obviously, there are currently more implications for these definitions than those considered here and further implications will emerge as species continue to move, naturally and via adaptation strategies, with rapid global change. This paper opens the dialogue on such issues.
It is important to clarify that alien or native status should not automatically imply a single management outcome, although existing legislation may need to be revised to accommodate this viewpoint. While management and the legislation that drives it has, up to now, largely focused on the control of aliens and the conservation of natives, we suggest that it will be increasingly important in the future to consider both management options for certain species regardless of status. Indeed, this approach is happening already in the control of native elephant and kangaroo populations (Barnes, 1983; Cowan & Tyndale-Biscoe, 1997), as well as the conservation of native butterfly populations relocated well outside their native range (Willis et al., 2009).
Despite many advantages, we are aware of three consequences that need to be considered for a niche-dispersal classification approach to defining natives and aliens. First, unnatural (i.e. anthropogenic) but still spatiotemporally feasible (i.e. within a PDE) dispersal events may be more common and more likely to be found in the tail of the dispersal unit curve. This situation increases the chance that the realized distribution of a dispersal-limited species will more closely approximate its fundamental niche. For a species where a rapid range shift is required to track the projected fundamental niche, this situation may actually be a positive outcome. Furthermore, this ‘enhanced’ dispersal may be seen as a counter-measure to offsetting reduced dispersal ability that follows anthropogenic landscape modification (Fischer & Lindenmayer, 2007; Manning et al., 2009). Second, enhanced dispersal may have unintended consequences for genotypic mixing between populations. Rapid climate change, independent of anthropogenic dispersal, will result in an increase in genotypic mixing for certain mobile species due to long-distance range shifts. Climate change will also introduce constrictions and disjunctions in the realized niche of many species (e.g. retreat to refugia), thereby increasing the chance of allopatric speciation. Lastly, for many species PDEs will be challenging to define due to a lack of basic knowledge on interactions with other organisms (Higgins & Richardson, 1999) or the landscape (Opdam & Wascher, 2004) that affect dispersal ability, particularly at the extremes of the dispersal curve. Even so, this does not preclude an adaptive management approach using information from the current distribution, proxy data or trait generalizations until specific information can be obtained.
Removing the alien tag from all anthropogenic dispersal events by placing a spatiotemporal context on the definition of native and alien species brings clarity to an inconsistency that has been frequently highlighted as an issue but has never been adequately addressed. Our framework provides a solution for existing terminological conflicts that are becoming increasingly problematic as the fields of invasion ecology, ecosystem restoration and movement ecology integrate through global change adaptation. When combined with invasion pathway theory and managed relocation, our revised definitions create a framework for managing both the ability of native species to track shifting regions of climatic suitability, and provide relevant identification of natives and aliens for appropriate control or preservation. Both outcomes will have significant impacts on enhancing global biodiversity in a rapidly changing world.
We thank the CSIRO Climate Adaptation Flagship for funding this work. We thank Raphael Didham, David Le Maitre, David Richardson, Andy Sheppard and three anonymous referees for comments on early drafts of the manuscript.
Bruce Webber is a plant ecophysiologist with research interests in plant resource allocation and plant–animal interactions. He applies these interests to understanding the dynamics of species movements and interactions within the context of a rapidly changing climate.
John Scott is a plant ecologist with interests in invasive weed ecology, climate change, biological control of weeds and policy development for weed management. His research mainly focuses on invasive plants in Australia, especially those from regions of Mediterranean climate.