ASSISTED COLONISATION AS A CLIMATE CHANGE ADAPTATION TOOL
R.V. Gallagher1, N. Hancock1, R.O. Makinson2 & T. Hogbin3 1. Department of Biological Sciences, Macquarie University 2. Royal Botanic Gardens & Domain Trust, Sydney 3. Australian Network for Plant Conservation
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This document was compiled as part of a project funded by the NSW Biodiversity Research Hub in 2013-14. It is intended to act as an appendix to the NSW Draft Translocation Policy (2007).
Please cite this publication as: Gallagher, R.V., Hancock, N., Makinson, R.O. & Hogbin, T. (2014). Assisted colonisation as a climate change adaptation tool. Report to the Biodiversity Hub of the NSW Office of Environment & Heritage.
For further correspondence contact:
[email protected]
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TABLE OF CONTENTS
Summary
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Acknowledgments
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Abbreviations
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List of Tables
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LITERATURE REVIEW AND SYNTHESIS
Section 1
What is assisted colonisation? 1.1 Definition
1
1.2 Global changes in climate and implications for biological
2
systems 1.3 Climate change in Australia
Section 2
3
When is assisted colonisation most needed and how can we identify candidate species? 2.1 Introduction
4
2.2 Situations likely to exacerbate the impact of climate change
4
2.3 Identifying at-risk ecosystems
5
2.4 Traits associated with species most likely to be affected by rapid climate change and in need of assisted colonisation
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2.5 Existing approaches to assessing candidate species for assisted colonisation
Section 3
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Potential risks and benefits of assisted colonisation 3.1 Benefits of assisted colonisation
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3.2 Risks associated with assisted colonisation: lessons from invasion biology 3.3 Evidence of native species becoming invasive
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3.4 Operational hurdles and strategies for minimising risk when undertaking assisted colonisation
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3.5 Legislative, policy, social and ethical considerations when iii
pursuing assisted colonisation
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3.6 Is assisted colonisation the appropriate solution? Investigating lower risk strategies for climate change adaptation
Section 4
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When does assisted colonisation have the most likelihood of success? 4.1 Evaluating the success of past translocations
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4.2 Introducing six key themes for successful assisted colonisation
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4.3 Recipient site selection and preparation 4.4 Predictive models
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4.5 Genetic diversity
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4.6 Species information
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4.7 Learning from invasive species research
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4.8 Adaptive management
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References
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APPENDICES
Appendix 1
Compilation of established flora translocations in Australia
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Appendix 2
Global case studies of experimental assisted colonisations
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Case study 1: Wild orchids in southwest China Case study 2: European forest herbs Case study 3: Seed germination beyond range limits Case study 4: Butterflies in the United Kingdom The use of assisted colonisation in the forestry industry Case study 5: Hardiness and growth in trembling aspen
Appendix 3
Reviews of flora translocations
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Appendix 4
Reviews of fauna translocations
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Summary
This report synthesizes the current literature on assisted colonisation, a climate change adaptation strategy, in the context of terrestrial biodiversity conservation. Assisted colonisation introduces at-risk species to new habitats, beyond their current range, in anticipation of more suitable climates. The translocation of flora and fauna for conservation purposes has been increasingly practiced in Australia as the threats to our native biodiversity have become better understood. A body of literature now exists on theory, practice, and results of translocation for some groups of organisms and individual cases. For the most part, conservation translocations in Australia have to date been in response to threat processes other than climate change, such as habitat loss or fragmentation. Recently, the IUCN/SSC included climate change as a specific threatening process that might drive translocation actions using assisted colonisation techniques. Unlike other conservation translocations, the practice of assisted colonisations is limited and therefore there are few examples from which to guide practice. To assist in the preparation of biodiversity conservation actions under climate change, this report reviews the substantial and growing body of literature that concentrates on the theoretical aspects of assisted colonisation. In particular, the report discusses the risks and benefits of, traits that may render organisms candidates for, threats and situations under which a species may become at risk, and success factors for assisted colonisation.
Acknowledgments The authors would like to acknowledge the contributions of staff within the NSW Office of Environment and Heritage in helping to develop this document, specifically Linda Bell and James Brazil-Boast.
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ABBREVIATIONS
ANPC: Australian Network for Plant Conservation BOM: Bureau of Meteorology CSIRO: Commonwealth Scientific and Industrial Research Organisation IPCC: Intergovernmental Panel on Climate Change IUCN/SSC: International Union for Conservation of Nature Species Survival Commission OEH: New South Wales Office of Environment & Heritage
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LIST OF TABLES
Table 1. Ecosystems present in NSW identified as part of ten Australian major terrestrial and marine ecosystems with vulnerable tipping points to the impact of climate change (adapted from Laurance et al., 2011).
Table 2. The relative importance of biological and environmental traits, in order of influence on vulnerability to climate change in birds and amphibians (adapted from Foden et al., 2013).
Table 3. Existing frameworks for assessing candidate species and situations for assisted colonisation.
Table 4. Examples of policies and guidelines with reference to assisted colonisation as a response to climate change for biological conservation purposes.
Appendix 1. Compilation of established flora translocations in Australia
Appendix 3. Reviews of flora translocations
Appendix 4. Reviews of fauna translocations
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LITERATURE REVIEW AND SYNTHESIS
SECTION 1 - What is Assisted Colonisation? 1.1 Definition Assisted colonisation is a type of conservation translocation; a form of introduction, where organisms are intentionally moved outside their indigenous range to avoid extinction of populations of the focal species (IUCN/SSC, 2013). Assisted colonisation is most commonly identified as a conservation measure to counteract the projected effect of climate change on species survival. The movement of organisms beyond their indigenous range is also commonly referred to as ‘managed relocation’, ‘assisted migration’ and ‘benign introduction’ (Seddon, 2010; Maschinski & Haskin, 2012). Anthropogenically-induced climate change is predicted to engender changes in the distribution, phenology and abundance of species. Potential responses of atrisk species to rapid climate change are: (1) Remain within the current range and persist unchanged or adapt in-situ without migration 1 (via adaptive genetic variation or phenotypic plasticity) (2) Migrate to more suitable climes (3) Remain within the current range, without adaptation, leading to extinction if climate exceeds physiological tolerance
Species that cannot adapt in-situ or migrate are at risk and are candidates for assisted colonisation. Although the decision to implement assisted colonisation can be controversial and therefore may not be adopted, it is important to note that a failure to assist species may favour those species in categories (1) and (2) above, whilst disadvantaging those in (3) (Thomas, 2011). None of the three scenarios listed above can be treated in isolation and often the question of when or which species should be considered for assisted colonisation, or the various design and
1
‘migration’ and ‘migratory’ are predominantly used here, unless otherwise stated, to relate to
unidirectional movement in response to climate change, not to regular annual movement.
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implementation issues associated with the practice, have not been empirically tested. It is important to note that species that are adversely affected by climate change may undergo declines under any of these three scenarios, and that any increased risk of decline imposed by climatic factors may interact synergistically and unpredictably with other threatening processes. These singly or in combination may cause decline below recovery thresholds regardless of a species’ genetic or phenotypic potential to adapt or migrate successfully in response to climate-related factors. The suitability of candidate species for assisted colonisation needs to be assessed taking into account the full suite of actual or foreseeable threat factors. Carefully considered experimental translocations in the near future, whether with pre-critical threatened species or with non-threatened analogue species, could help to increase the level of empirical knowledge, refine techniques, improve suitability assessment, and obviate at least some of the risks for the future.
1.2 Global changes in climate and implications for biological systems This section gives a brief overview of the current science of climate change and implications for biological systems. •
The earth has warmed by ~0.85°C since the 1880s. Current greenhouse gas emissions are tracking the upper range of the IPCC projections, indicating that global mean temperatures are likely to increase by 2.6 – 4.8°C (compared to the 1986 – 2005 baseline) by the end of this century (IPCC, 2013).
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Changes in seasonal patterns of rainfall, an increase in the frequency and magnitude of extreme weather events and a rise in sea levels are predicted globally. The frequency and intensity of droughts, floods and wild fires are also expected to rise (IPCC, 2013).
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In some locations, current climate regimes may disappear altogether, creating novel or non-analogue environments (Williams, 2007; Dunlop et al., 2012). Novel climates have been projected to emerge primarily in the tropics and subtropics, whilst current regimes in poleward regions and tropical montane sites are projected to disappear (Williams, 2007). Estimates of the percentage of global land surface area which may experience novel combinations of climate variables by 2100 range from 12-39% (Williams et al., 2007). 2
Globally, on average, shifts to novel climates are projected to occur by 2047(±14 years) under a high emission scenario, with this change expected to be sooner (approximately 22.5 years), if calculations are based on preindustrial variability in climate alone (Mora et al., 2013). •
Isotherm migration will allow some species with the potential to disperse to track changes in climate regimes and stay within their optimal climate conditions. However, many species are predicted to be unable to keep pace with the velocity of climate change. Terrestrially, the pace at which the climate is changing has been calculated at 27.3 km/decade (Burrows et al., 2011). The pace of climate change is predicted to be slower in mountainous regions than in homogeneous topography, but this effect is dependent on latitude (Loarie et al., 2009).
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Broadly, species will face changes in four key areas as a consequence of climate change: (1) physiology, (2) distributional limits, (3) phenology, and (4) rates of microevolution and adaptation (Hughes, 2000).
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Species are already responding to the recent, relatively modest levels of climate warming (Parmesan & Yohe, 2003; Rosenzweig et al., 2008; Chen et al., 2011).
1.3 Climate change in Australia •
In Australia, by 2070, climate warming is projected to be in the range of 1 – 5°C above the climate of the baseline period of 1980 – 1999 (if global greenhouse gas emissions are within the IPCCs projected range) (CSIRO & Bureau of Meteorology, 2012). The number of hot days/warm nights and cool days/cold nights are predicted to increase and decrease respectively (CSIRO & BOM, 2012).
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Large natural variability in precipitation is expected, with a general drying trend in the southern areas during winter and over southern and eastern areas during spring. Droughts are expected to become more frequent in southern Australia, however intense rainfall events are still likely to occur (CSIRO & BOM, 2012).
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NSW encompasses wide latitudinal variation (29° - 37°S) and consists of heterogeneous landscapes. Future climate projections for eight regions of 3
NSW have been produced at a 50 x 50 km scale (Department of Environment Climate Change and Water NSW, 2010a). Regional future climate scenarios vary but are broadly in line with large scale predictions of higher maximum and minimum temperatures, change in rainfall patterns and a suite of corresponding ramifications (Department of Environment Climate Change and Water NSW, 2010a).
SECTION 2 - When is assisted colonisation most needed and how can candidate species be recognised?
2.1 Introduction Determining candidate species for assisted colonisation is multi-faceted and should be approached using diverse viewpoints across relevant disciplines. The capacity for an organism or population to adapt to climate change depends on biotic factors (such as adaptive genetic variation, capacity for phenotypic plasticity, inherent rates of evolution), abiotic factors (such as the availability and connectedness of suitable habitat, climate or soil conditions) and on the interaction between abiotic and biotic factors. Assisted colonisation is likely to be most needed for species which exhibit a combination of traits that limit their ability to disperse or to adapt to changing climate and the associated habitat change. It is important to recognise that individual species are likely to respond to changing climates at different rates, leading to changes in the composition of current communities or assemblages (Ackerly, 2003; Urban et al., 2012). The potential for reassembly of communities poses a set of distinct management challenges, which includes the need to identify and clearly define the role that multi-species translocations may play in attempts to retain current function into the future.
2.2 Situations likely to exacerbate the impact of climate change Whilst climate change is a global phenomenon and novel environments are predicted to be common (Dunlop et al., 2012), projected changes will vary spatially and seasonally, and influence vulnerability accordingly. Position in the landscape will influence exposure to environmental changes such as temperature extremes, 4
precipitation increases or decreases, changes in stream flow (floods and intermittent drying), changing fire regimes, frost exposure and reductions in snow cover and sea level rise (inundation and salinity). Homogeneous landscapes, particularly areas with low-relief topography, are projected to be particularly vulnerable to climate change impacts due to a reduced number of topographically determined microrefugia in which organisms can persist (Dobrowski, 2011). Vulnerability to climate change will also be exacerbated by interactions with preexisting stressors. These stressors may include (Lindenmayer et al., 2010): •
native vegetation clearance;
•
habitat fragmentation;
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altered land use practices;
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loss of habitat;
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altered natural disturbance regimes;
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competition and /or predation from introduced weeds, pests and pathogens;
In addition, stochastic events may also increase vulnerability to climate change by reducing the size of individual populations or the breakdown of meta-population dynamics (IUCN/SSC, 2013).
2.3 Identifying at-risk ecosystems Some ecosystems and their constituent species will be more vulnerable to the impacts of climate change than others. These ecosystems may require more active management solutions, including assisted colonisation of at-risk species, to maintain function. Six of the 10 major terrestrial and marine ecosystems in Australia identified as having vulnerable ‘tipping points’ (disproportionate large changes in ecosystems caused by modest environmental changes), are present in NSW (see Table 1 overleaf; adapted from Laurance et al., 2011).
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Table 1. Ecosystems present in NSW identified as part of 10 Australian major terrestrial and marine ecosystems with vulnerable tipping points.
Ecosystem Elevationally restricted mountains
Vulnerability factors Often narrow environmental envelopes; geographically restricted distribution; many are near climatic thresholds
Coastal floodplains and wetlands – particularly wetlands adjoining coastal areas with high tidal amplitudes (5–13 m)
Rising sea levels; extreme weather events (e.g. storm surges); plant invasions
Wetlands and floodplains of the MurrayDarling Basin
Clearing of vegetation; habitat loss; fragmentation; sedimentation & nutrient changes; rising temperatures and sea levels
Offshore islands
Restricted size, physical isolation; often narrow environmental envelops; endemic biodiversity; species invasions
Estuarine wetlands (salt marshes and mangroves)
Narrow environmental tolerances; geographically restricted; proximity to dense human populations in coastal regions; fragmentation; reliance on a few key (framework) species
Temperate eucalypt forests – only parts of the geographic range
Habitat loss; fragmentation; reliance on ‘framework’ species; close proximity to humans; loss of key fauna; synergisms between weed invasions and fire
The ecosystems listed in Table 1 are diverse and therefore ranking the factors that have rendered them vulnerable may not be informative. However, narrow environmental envelopes and restricted distributions are a recurring theme. The key drivers of vulnerability to tipping-points across all ecosystems studied were identified as (1) extreme weather events and, (2) changes in water balance and hydrology (Laurance et al., 2011). In addition to the broad ecosystems types identified in Table 1, specific environments are projected to be particularly exposed to the impacts of changing 6
climate regimes in NSW. For instance, the alpine area of NSW is considered to be highly vulnerable to climate change due to changes in summer temperatures and snow cover (Hughes, 2003; Whetton et al., 2003). Temperate subhumid areas in north-eastern NSW have also been identified as likely to undergo significant ecosystem-level change due to warming, especially in winter, and changes to fire regimes that may lead to changes in vegetation structure and composition (Hughes, 2011; Shoo et al., 2012). The south west of NSW has also been highlighted as particularly vulnerable to the impacts of climate change due to a predicted decrease in rainfall (Department of Environment Climate Change and Water NSW, 2010b). Marine and freshwater ecosystems have also been recognised as acutely susceptible to climate change (e.g. coral regions, coastal fringe habitats and wetlands and the Murray-Darling Basin (Steffen et al., 2009; Hughes, 2011)).
2.4 Traits associated with species most likely to be affected by rapid climate change and in need of assisted colonisation Individual species’ vulnerability to climate change will depend on its sensitivity (the potential to persist in-situ), exposure (the degree to which the physical environment will change) and adaptive capacity (persistence due to its ability to cope with microevolutionary change or dispersal) (Dawson et al., 2011; Foden et al., 2013). Species with the traits listed below have been identified as the most likely to be affected by rapid climate change (note that several of the traits listed are interconnected and should not be viewed in isolation): •
Species with small effective population sizes (less than a thousand breeding individuals) are likely to have reduced genetic diversity, a heightened risk of inbreeding depression and an increased vulnerability to demographic and environmental stochasticity, all factors that increase the risk of extinction (Hoffmann & Sgro, 2011). The effects of inbreeding depression are deleterious for reproduction and survival regardless of climate change (Frankham et al., 2010). However, the process of rapid climate change is thought to exacerbate the rate of reduction in genetic diversity and temperature stress has been demonstrated to heighten inbreeding depression in some species (Armbruster & Reed, 2005). Inbreeding depression also 7
reduces the capacity for species to evolve and therefore adapt to changing conditions (Frankham et al., 2010). The importance of recent demographic history to genetic variation (i.e. small populations having experienced gradual decline and/or subject to directional selection), should be treated differently to those experiencing rapid decline (e.g. bottleneck effects) (Frankham et al., 2010). •
Species with long generation times have slow replacement rates, fewer chances for genetic recombination and reduced opportunity to increase evolutionary responses to climate change than species which reproduce more frequently (Renton et al., 2012; Buckley & Kingsolver, 2012). In the case of the persistence of annual versus perennial plants under climate change, the outcome may be context dependant. For instance, annual plants have an increased likelihood of rapid adaptation to withstand in-situ climate change. However, annual plants have an increased vulnerability to unfavourable environmental extremes compared to perennials. Adult perennial plants may have an increased chance of persisting through climate extremes until conditions are favourable for seedling establishment (Peters & Darling, 1985).
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It is generally expected that adaptation to climate change may be more difficult for species with narrow distributions (narrow endemics) than those with broader habitat tolerances. Species with restricted ranges or limited distribution may not have sufficient genetic diversity to cope with changes affecting phenological events, thermal responses and/or resilience to stressful climatic conditions (Hoffmann & Sgro, 2011). Species with narrow ranges and small effective populations are more likely to have low genetic diversity and therefore reduced adaptive capacity (Pauls et al., 2013). Populations with narrow distributions that are also adapted to colder climates (either from high altitude or high latitudes) are at further risk (Pauls et al., 2013). Furthermore, narrow-range species with no environmental heterogeneity may no longer possess the phenotypic plasticity to cope in-situ with changing conditions (Hoffmann & Sgro, 2011). In contrast, widespread species, specifically plant and insect species, usually have sufficient genetic diversity to provide resistance to stressful climatic conditions (Hoffmann & Sgro, 2011). However, widespread species should not be overlooked as candidates for assisted 8
colonisation because (1) migration barriers (geological or anthropogenic) may prevent migration; (2) connectivity to new areas may not be feasible; (3) disruption to disturbance/obligate relationships may preclude persistence or colonisation in new areas; (4) differential rates of dispersal / migration and adaptation capacity may occur among the leading, central and lagging populations of widespread species (Zakharov & Hellmann, 2008; Mellick et al., 2012). •
The degree of vulnerability of narrowly-endemic species will be related to the extent of their distribution. For example, ‘organisms occupying a single lake, a single mountain top, an isolated mountain range or a single geological outcrop’ are at risk if they cannot be connected to suitable habitat (Thomas, 2011). High-elevation species may be adapted to cooler temperatures. For these species, such as the mountain pygmy possum (Burramys parvus), there may be limited options for translocation when suitable climate space is not projected to occur under future climate regimes (Brereton et al., 1995). Of particular concern are high-elevation endemic plants that are components of the relictual Gondwanan rainforest, rare species in lowland rainforests and cloud forest species at the level of the cloud base (800-900m) and other regionally endemic montane fauna constrained by physiological & ecological traits (Shoo et al., 2013).
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Specialist species (those with a narrow range of climatic conditions, habitat or diet) are predicted to be more sensitive to climate change than generalists (Thuiller et al., 2005; Buckley & Kingsolver, 2012). Specialists can include those species that are depended on or have a mutualistic relationship with another organism. Under climate change, the alteration to distribution, phenological events and / or abundance of one species may negatively affect the other and trophic interactions may be disrupted (Bernazzani et al., 2012). Specific mutualistic relationships between plants and mycorrhizae may also become decoupled.
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Higher trophic level species will be disproportionately affected if their host or prey species shifts distribution under climate change, particularly if the interaction represents a highly specialised relationship (Thackeray et al., 2010). 9
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Changing biotic interactions, other than those involving specialists and mutualisms, have been identified as an important proximate cause of population declines and local extinctions under climate change (Cahill et al., 2013). It has been argued that the preservation of biotic interactions is one of the most important factors in the ability of species to migrate and to successfully colonise under changing climates (Hellmann et al., 2012). Many examples of changes to biotic interactions as a result of current climate change have been identified including: increases in rates of insect herbivory (Blois et al., 2013), changes in the outcome of competitive interactions in European dragonflies (Suhling & Suhling, 2013), and the various case studies outlined in Hellmann et al. (2012). Disequilibrium in ecosystems will also be created by differential response rates to climate change from the introduction of non-native weeds, pests and pathogens. Non-native species may become more abundant or competitive than native species if they are advantaged due to changed climatic conditions, altered life cycles and/or rising atmospheric CO2 levels (Bernazzani et al., 2012).
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Increasing levels of atmospheric carbon dioxide (CO2) will affect vegetation community structure and function with flow-on effects at the ecosystem level. The ability of different plant species to take advantage of available CO2 differs according to their photosynthetic pathway. Generally, C3 plants (usually woody species) are able to take advantage of higher concentrations of atmospheric CO2 relative to C4 plants (often grasses). Incursions into grasslands and grassy woodlands by C3 plants are therefore expected (Hovenden & Williams, 2010). Increased growth rates vary considerably within taxa and depend on interactions with nutrients, temperature and rainfall. Increasing CO2 will also reduce leaf nitrogen content and increase secondary metabolites, altering plant herbivore relationships and nutrient recycling processes.
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Species close to their physiological limits are at risk from climate change. Currently, there is evidence that fauna is at risk from thermal stress affecting rates of locomotion and feeding, reducing food availability and changing biotic interactions (Buckley & Kingsolver, 2012; Cahill et al., 2013). The relative importance of physiological tolerance to high temperature stress may develop 10
over time as temperatures and extreme weather events increase in frequency and magnitude (Cahill et al., 2013). For example, death from over-heating (hyperthermia) in flying foxes in NSW was observed during an extreme temperature event in 2002 (Welbergen et al., 2008). Growth, survival, reproductive rates and generation time for fauna and flora are expected to alter in response to increasing temperatures, but with substantial variation amongst species (Buckley & Kingsolver, 2012; Cahill et al., 2013). The degree of species’ vulnerability is expected to be highest in the tropics (especially for insects and terrestrial ectotherms) due to limited seasonality offering a narrow thermal range (Deutsch et al., 2008). The risk to species of temperature stress lessens towards higher latitudes where species have broader thermal optima and are often living in conditions cooler than their optima (Deutsch et al., 2008). Hydric limits apply to species sensitive to intermittently dry conditions or restricted to moist conditions if precipitation patterns change (Hoffmann & Sgro, 2011; Buckley & Kingsolver, 2012). In addition, the interaction of thermal and hydric stress may prompt a unique suite of responses. For instance, birds are predicted to suffer high mortality rates from hyperthermia where extreme heat events combine with water stress (McKechnie & Wolf, 2010). Different organisms may be vulnerable to hydric and thermal limits at different life stages. Seedlings, for example, are more likely to be vulnerable to dry conditions than adult plants (McDowell et al., 2008) and some larval insects may be more immune to heat stress than the adults (Buckley & Kingsolver, 2012). Different seasonal rates of climate change may give early season developers a longer exposure to growing seasons (Buckley & Kingsolver, 2012). Where changes arise in the timing of life-cycle events there is potential for disruption of predator/prey relationships, mutualisms, pollination and competition. Mismatches between organisms that rely on photoperiod cues and thermal activity may also occur (Buckley & Kingsolver, 2012). •
Bergmann’s rule states that there is a trend for mean body size in endotherms to decrease with decreasing latitude (interpreted as body size decreases with increasing temperature). There are many lines of evidence to 11
support this rule. For instance, Gardner et al. (2009) found a latitudinal shift in size for 6 out of 8 species of Australian birds; wing length has reduced over the past 100 years. However, it has been demonstrated that the magnitude and direction of size response varies between endotherms and may depend on the nature of the change in temperatures, water stress and extreme events (Gardner et al., 2011). McCauley & Mabry (2011) argue that organisms with larger body size are more likely to be long-distance dispersers and successful colonisers. These traits may render large body mass species less vulnerable to climate change and smaller body mass species more likely to suffer adverse in-situ impacts. Furthermore, small-bodied desert birds are predicted to be most vulnerable to dehydration and mortality on extremely hot days (McKechnie & Wolf, 2010). There is no clear consensus as to whether body size changes are a plastic or evolutionary response to climate change (Teplitsky & Millien, 2014). It has been argued that changes in body size for all animals and plants may also be a function of altered diet and precipitation, rather than temperature alone (Bickford et al., 2011). •
Species lacking dispersal capability will have limited capacity for shifting their range in response to a rapidly changing climate. For sessile organisms like plants, species with seeds that lack adaptations for dispersal, such as aerodynamic appendages (pappus, coma, wings) for wind dispersal or fleshy fruits to attract dispersal mutualists such as birds or bats (Leishman et al., 2000) may be disadvantaged. Dispersal-limitation can arise in species that have been exposed to stable conditions over long periods. This can lead to: (1) a lack of genes to code for new functions, such as a change in thermal tolerance; (2) DNA decay in genes that are functionally important; and/or (3) low levels of genetic variation (Hoffmann & Sgro, 2011). Species incapable of achieving long-distance dispersal are particularly vulnerable to the potential effects of shifting climatic conditions. However, quantification of long distance dispersal events is typically subjective and varies substantially among taxa.
•
The ability of species to disperse or migrate may be constrained due to physical barriers in the landscape. Physical barriers can be created by geological factors (e.g. edaphic and/or topographic), as well as man-made pressures such as urban/agricultural land use. Species with poor dispersal 12
capacity will be at risk of extinction where habitat connectivity cannot aid their migration to more suitable climates or to micro-refugia. Candidate species for assisted colonisation may have a combination of the above described traits, be involved in several biotic interactions, suffer from multiple anthropogenic stressors and may respond using numerous modes. For example, large-bodied taxa that are ecological specialists at higher trophic levels with long generation times, poor dispersal ability, low or delayed reproductive output occupying small geographic ranges, may be particularly at risk (Dawson et al., 2011). Generalisations across taxa may not be feasible because different groups vary in the relative importance of their traits in determining exposure to climate change. For example, Table 2 compares the relative importance of a range of traits associated with vulnerability to climate change and highlights the limitations of taking a broad approach in assessing at-risk species. Table 2. The relative importance of biological and environmental traits, in order of influence on vulnerability to climate change in birds and amphibians (adapted from Foden et al., 2013) Biological & / or environmental trait Birds
Amphibians
Limited dispersal ability
Slow turnover of generations (poor ability to evolve)
Low reproductive output
Limited dispersal ability
Slow turnover of generations
Habitat specialist
Changes in mean precipitation
Changes in mean temperature
Changes in precipitation variability
Changes in temperature variability
Changes in mean temperature
Narrow temperature tolerance
Changes in temperature variability
Narrow precipitation tolerance
Intolerance of disturbance
Changes in precipitation variability
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Narrow temperature tolerance
Disease (Interspecific interaction)
Geographical barriers (poor dispersal ability)
Changes in mean precipitation
For birds and amphibians, low adaptive capacity (poor ability to evolve and disperse) and changes in environmental traits are relatively influential for assessing at risk species (Foden et al., 2013). Predicted responses to climate change within taxon have been modelled for some species, including plants and butterflies, and these findings can be used to make some generalisations. For example, a recent study showed that the best performing predictors of plant persistence under climate change include effective fecundity, years to maturity and dispersal distance (Renton et al., 2012). Functional trait approaches have also been used to predict the migratory potential of a range of butterfly species. An observational study comparing the distribution of 48 butterfly species in Finland over two time periods demonstrated that the following traits were correlated with successful migration: wide distribution; mobile; large body; overwinter as adults; feed on woody plants at the larval stage and use forest edges as their main breeding habit (Pöyry et al., 2009). In addition, changes in the timing of butterfly life-cycles have been linked to diet type, generation time, overwintering stage and dispersal ability (Buckley & Kingsolver, 2012).
2.5 Existing approaches to assessing candidate species for assisted colonisation Various frameworks exist for assessing the need for assisted colonisation in the literature. The complexity surrounding the question of when assisted migration is most needed and which species are at risk from rapid climate change suggests that a combination of decision-making tools may be necessary. Table 3 (overleaf) lists and describes appropriate frameworks that can be employed to assess candidate species.
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Table 3. Existing frameworks for assessing candidate species and situations for assisted colonisation Framework
Description
Reference
Planning & Questions to ask to implementing successful maximize the success of assisted colonisation assisted colonisation
Chauvenet et al.,
Vulnerability to climate change: exposure; sensitivity and adaptive capacity
Assess vulnerability of species or ecosystems to climate change with conservation responses
Dawson et al., 2011
Vulnerability to climate change: exposure; sensitivity and adaptive capacity
Assess vulnerability using biological traits of birds, amphibians and corals
Foden et al., 2013
Framework for recipient site selection Criteria for ranking good and bad managed relocation proposals
Supplementation of IUCN guidelines Uses rare plants as case studies
Harris et al., 2013
Potential actions to prevent extinction or ecosystem collapse
Assess feasibility of species movements under possible future climate scenarios
Hoegh-Guldberg et
Optimal timing for managed relocation
Focus on when to move a population where objective is to maximize population size
McDonald-Madden
Assessing the need to translocate dependent assemblages
Assemblage-level assessment
Moir et al., 2012
Evaluation of individual cases of managed relocation
Assess ecological and social criteria and acceptability and feasibility from different stakeholders perspectives
Richardson et al.,
Decision tree describing conservation introduction problems (under climate change)
Framework to assist decision making on whether or not to introduce, the choice of candidate species
Rout et al., 2013
2013
Haskins & Keel, 2012
al., 2008
et al., 2011
2009
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and locations and different strategies for the introduction Framework for socially & scientifically acceptable managed relocations
A series of ethical, policy, ecological & integrated questions to support proposed managed relocation proposals
Schwartz et al.,
Management actions
Identifies movement, evolutionary and ex-situ options
Shoo et al., 2013
Collection strategies for potential target species
Determines, prioritizes and develops collection strategies for plant species
Vitt et al., 2010
Vulnerability to climate change
Assess vulnerability including the effects of regional and local factors, potential for evolutionary and ecological responses, resilience, active management remediation and feedback effects
Williams et al., 2008
2012
In addition to the generalised frameworks presented in Table 3, there are several quantitative methods to assess individual species in most need of assisted colonisation and four methods are briefly discussed below. •
Predictive models (e.g. correlative or mechanistic species distribution models) combine various climate variables (e.g. both mean and extreme measures of temperature or rainfall) with species’ current known distributions to project their ranges under future climate change scenarios. A more thorough discussion on this topic is provided in Section 4.
•
Paleoecological records can provide insights into how abundant and widespread organisms responded to past climate change and are used to infer likely responses to the projected novel environments (Blois et al., 2013). However, even where the paleoecological records imply that species were able to persist through periods of hostile climate they may not be directly 16
comparable to the current situation where a higher rate of change and a different habitat-fragmentation regime apply, and where mass extinctions are predicted (Moritz & Agudo, 2013). •
Phylogenetic analyses allow the testing of the hypothesis that closely related species will respond similarly to climate change. Where phylogenetic clusters are found to be associated with a particular response to changing climatic conditions, predictions of which clades will be most vulnerable can be made (Angert et al., 2011; Buckley & Kingsolver, 2012).
•
Functional traits have been used to predict which species and communities are most vulnerable to climate change (Jiguet et al., 2007; Gallagher et al., 2012). The predictive power of traits for identifying at-risk species varies, depending on factors such as the position within the range where measurements were taken (core versus leading edge populations), position in the landscape (especially for elevationally restricted organisms), and projected exposure to climate change (Angert et al., 2011). However, no single trait-based approach is a consistently strong performer and results will vary based on both individualistic responses of species and the empirical limitations of each approach. Trait-based approaches perform better in predicting the likelihood of phenological changes in species as opposed to the extent and magnitude of potential range shifts (Buckley & Kingsolver, 2012).
SECTION 3 – Potential risks and benefits of assisted colonisation
3.1 Benefits of assisted colonisation The primary benefit of assisted colonisation is the potential to prevent extinction of species whose persistence is threatened either directly, or indirectly, by rapid climate change. Proponents of assisted colonisation argue that a decision not to assist species threatened by climate change by deliberately extending their current range dooms candidate species to extinction (McLachlan et al., 2007; Hoegh-Guldberg et al., 2008; Thomas, 2011). A recent review of 50 peer-reviewed articles on assisted colonisation found that 60% of studies supported the validity of assisted colonisation as a climate change adaptation strategy (Hewitt et al., 2011). However, despite this majority, 20% of studies indicated no clear position on the effectiveness of assisted 17
colonisation for climate change adaptation and the review’s authors note that debate around the practice of assisted colonisation is intensifying, rather than trending towards resolution (Hewitt et al., 2011). Scenarios under which individual species, species assemblages or entire communities may benefit from assisted colonisation to in response to climate change include:
(1) Loss of suitable climatic habitat within the current range. In some circumstances levels of change may fall outside the natural climatic variability experienced by some species under both current conditions and through evolutionary time. There is evidence that some organisms are already shifting their ranges to track optimal conditions for growth and reproduction under the relatively modest levels of climate warming already experienced globally (Parmesan & Yohe, 2003; Rosenzweig et al., 2008; Chen et al., 2011). The response of species is likely to be highly idiosyncratic, leading to the potential for substantial reassembly of the composition of communities, with flow-on effects to ecological interactions and ecosystem services (Gilman et al., 2010; Lavergne et al., 2010; Urban et al., 2012). Assisted colonisation may be the only option available for species that cannot keep pace with species with which they have coevolved and are dependent upon. (2) The emergence of novel or non-analogue climates. Projections for the emergence of novel climatic environments both globally and within Australia in a relatively short space of time (between 2050 and 2100) indicate that whole assemblages of species may be under threat and may need assistance (Williams, 2007; Dunlop et al., 2012; Mora et al., 2013). The large scale of these projections may make it difficult to prioritise species for assisted colonisation, however pre-emptive feasibility studies could aid in to identifying potential candidates or flag the need for multispecies translocations. (3) Multiple stressors. Many natural areas are now so anthropogenicallymodified (with no end in sight to the modifications) that managing for conservation to historically referenced conditions may no longer be 18
achievable (Thomas, 2011). Anthropogenically-modified habitats are typically characterised by the presence of invasive species, alterations to and disruption of disturbance regimes and changes to soil, hydrological and other conditions, altering both biotic and abiotic interactions (Fischer & Lindenmayer, 2007). In addition, modified habitats generally preclude effective species’ migration and gene flow by fragmenting populations into a matrix of land-uses (Cushman et al., 2006). As a result of extensive alterations to natural systems Shackelford et al. (2013) argue that restoration goals should no longer aim to reflect historic or reference sites. (4) Replacement of the loss of an ecological function/service. Assisted colonisation can allow for the replacement of species that have been lost from an ecosystem (and the corresponding loss of the role that species performs) and can thereby restore a similar ecological service and/or fill existing gaps in biological function (Hewitt et al., 2011).
3.2 Risks associated with assisted colonisation: lessons from invasion biology Opponents of the use of assisted colonisation as a climate change adaptation strategy typically draw examples from the lessons learnt from invasive species research, including biological control methods. Parallels have been drawn between species moved beyond their natural range for assisted colonisation purposes and the negative impacts of invasive species on recipient communities, such as: •
Reduced native plant recruitment through impacts on colonisation-extinction dynamics (Yurkonis & Meiners, 2004);
•
The disruption of key ecological interactions (i.e. plant-animal mutualisms) (Ricciardi & Simberloff, 2009);
•
The loss of fitness and/or local extinction of populations due to potential hybridization and introgression of the target species with close relatives at or nearby the recipient site (Hewitt et al., 2011 and references therein);
•
Unintentional introduction of novel pathogens or pests to ecosystems (Ricciardi & Simberloff, 2009 and references therein);
Therefore, the need to move species beyond their range to secure viable populations under climate change needs to be weighed against the potential non19
target effects on communities at recipient sites. However, whilst the risk of invasiveness and flow on effects from assisted colonisation are valid, it is important to note that candidate species often possess biological traits incompatible with the tendency to become invasive (e.g. poor dispersal, long generation times, low fecundity; this subject is further discussed in Section 2). The selection, refinement and application of appropriate Invasiveness Risk Assessment techniques needs to be an integral part of the identification and prioritisation of candidate species for assisted colonisation.
3.3 Evidence of native species becoming invasive There is potential for species considered native to become invasive within their country or region of origin if introduced beyond their historical, indigenous range (Gallagher & Leishman, in press; Mueller & Hellmann, 2008). In Australia, over 500 species of native plants have been introduced to areas outside their documented native range (Randall, 2007) with species in the genus Acacia (wattles) offering the most compelling example of the potential for native species to become invasive. Ecological studies of Acacia populations in their native and introduced ranges, and in common garden experiments, show that the introduced populations often have a competitive advantage over other species due to factors such as lower seed predation (M. Leishman, unpublished data) and different microbial associations (Birnbaum et al., 2012). Species such as Acacia saligna, introduced into NSW from WA, have been identified as significant threats to species listed under the TSC Act in NSW (Coutts-Smith & Downey, 2006). A study comparing within-country and between-country introductions in the United States as a proxy for the likely impact of assisted colonisation versus introduction of non-native organisms found that species moved as part of assisted colonisations were unlikely to become invasive. However, those that did become invasive could cause significant harm (Mueller & Hellmann, 2008). By comparing the proportions of invasive species of intra- and inter-continental origins, Mueller & Hellmann (2008) concluded that relatively small portion (15% of the 468 species studied) resembled assisted colonisations (i.e. were native species, introduced from within the United States). The lower risk for moving native species within the United States, as compared to introducing those from outside the country, was attributed to 20
the higher likelihood that close congeners of the species are already present and occupying established niches in the recipient habitat or ecosystem. Consequently, ecological control factors (e.g. predators, pathogens) are also more likely to be present at the site reducing the risk of invasion. In their study, plants were found to be least likely to become invasive, with fish and crustaceans most likely to become serious invaders (Mueller & Hellman, 2008). Species introduced as biological control agents also have the potential to cause harm to non-target species, often with serious ecological impacts on native species (e.g. Cane Toads (Rhinella marinus) introduced to Australia to control Cane Beetle; Burnett, 1997). However, the potential detrimental impact of biological control releases needs to weighed against the ecological benefits conferred by these species in limiting pest abundance. For instance, in the United States over the past 100 years only 0.76% of deliberate releases of biological agents to control weeds have been deemed harmful to non-target species, of which nearly all were minor (McFadyen, 1998; Mueller & Hellmann, 2008). Protocols for screening the harmful effects of biocontrol agents could be a useful source of information when designing assisted colonisation projects.
3.4
Operational hurdles and strategies for minimizing risk when undertaking assisted colonisation
Both advocates and critics of assisted colonisation recognise the significant operational obstacles to implementing this type of conservation action. These obstacles include, but are not limited to: •
Financial costs of design, implementation and on-going monitoring;
•
Coordination across political boundaries or jurisdictions;
•
Failure of species to colonise, despite a well-designed program;
•
Difficulty identifying suitable recipient sites. This may be due to habitat loss or a paucity of suitable land tenures, as well as the uncertainty inherent in identifying areas projected to contain suitable climatic habitat in coming decades.
Once the decision to undertake an assisted colonisation has been made, strategies are required to minimise the risk of failure and to protect the large financial 21
investment being made in this conservation action. Failures may occur due to biological factors such as inappropriate genetic mixing of populations leading to inbreeding depression, genetic swamping or hybridisation; introduction in recipient sites with unsuitable edaphic or climatic conditions in either the short or long term; or a lack of co-evolved mutualists, such as pollinators, leading to reproductive failure. In addition to these biological factors, a failure to implement long-term stewardship of and resources to assisted colonisations may result in a lack of monitoring, or the control of threats such as weed invasion or feral animals.
Strategies for minimising risks associated with assisted colonisation may include:
1) Completion of comprehensive pre-translocation assessments for each species targeted for assisted colonisation prior to the implementation of projects. This step would likely involve a desktop study to undertake activities such as: collating information on species biology and current range, bioclimatic modelling to locate areas of suitable habitat in coming decades as potential recipient sites, assessment of invasiveness risk, and seeking opinions from relevant experts in the taxon. For plant species, such a preliminary assessment should build on the protocols recommended in the Guidelines for the Translocation of Threatened Plants in Australia (Vallee et al., 2004) by including specific questions about the likelihood of climate change to adversely affect the species ability to survive in its current range. 2) The use of the principles of adaptive management to tailor the design, implementation and on-going monitoring of projects. In order to refine the practice, assisted colonisations should be designed and implemented on an experimental basis. This experimental approach allows for various methods to be tested and evaluated leading to an increase in the knowledge-base for future projects. Previous research into minimising specific risks should be used to inform the needs of individual assisted colonisation projects. For instance, various frameworks exist for assessing the risk of genetic mixing (e.g. determining the probability of outbreeding depression between two populations (see Frankham et al., 2011); evaluating the risk to native populations of adverse genetic change from revegetation (see Byrne et al., 22
2011a); considering the risk of genetic pollution in eucalypts from exotic pollen dispersal (see Potts et al., 2003). 3) The use of existing frameworks (see Table 3) and guidelines to inform specific aspects of assisted colonisation. Various international agencies and governments recognise the need to prepare for the potential use of assisted colonisation as a conservation tool in coming decades. Table 4 provides examples of the types of strategies and guidelines being implemented globally.
Table 4. Examples of policies and guidelines with reference to assisted colonisation as a response to climate change for biological conservation purposes.
Organisation Ontario Forest Research Institute
Publication Colombo, S., 2008, Ontario’s Forests and Forestry in a Changing Climate. Climate Change Research Report CCRR12,
Reference Page I: ‘Climate change will increasingly make species and local populations of tree species less well adapted to the climate where they occur’. ‘Increasingly, forest managers will consider planting non-local species and populations. Such potential adaptations, however, need to be carried out with consideration of potential negative consequences and if implemented should be well documented and monitored’.
(1) National Committee for Wild Flora and Fauna and (2) State Commission for Natural Heritage and Biodiversity, Spain
Comisión Estatal para el Patrimonio Natural y la Biodiversidad. 2013, unpublished report. Directrices técnicas para el desarrollo de programas de reintroducción y otras traslocaciones de conservación de especies silvestres en España. Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid, Spain Translated by http://translate.google.com:
Page 12: ‘Moreover, in general, the decision to initiate reintroduction programs or other translocation for conservation should be based on the situation in which he finds a taxon, recommending implementation:When the species / population is susceptible to negative effects of human activities, including anthropogenic climate change, or stochastic events,’…… Page 15: ‘The expected effects of climate change must be taken into account when planning all types of translocations, so that the results of 23
Technical guidelines for the development of programs and other reintroduction translocations conservation purposes wildlife in Spain. July 24, 2013
Council of Europe
Convention on the conservation of European wildlife and natural habitats, Standing Committee 32nd meeting Strasbourg, 27 - 30 November 2012
IUCN
IUCN/SSC, 2013, Guidelines for Reintroductions and Other Conservation Translocations. Version 1.0. Gland, Switzerland: IUCN Species Survival Commission, viiii + 57 pp.
Royal Society Internal policy on for the translocations Protection of Birds (UK) (RSPB)
these actions may be viable in the long term’. (Excerpts from the translated version of the Spanish document. No copy available in English. Translation provided by http://translate.google.com and Emilio Lacuna, Senior Officer Plant Conservation, in the Generalitat Valenciana section of Natural Resources Protection (pers. comm. 10 January, 2014). Recommendation No. 158 (2012), based on the IUCN Guidelines: Page 12 ‘To also consider ex situ measures, such as relocation, assisted migration and captive breeding, among others, that could contribute to maintaining the adaptive capacity and securing the survival of species at risk, taking into account the precautionary approach in order to avoid unintended ecological consequences including, for example, the spread of invasive alien species’ ‘Whilst assisted colonisation is controversial it is expected to be increasingly used in biodiversity conservation’. ‘The climate at the destination site should be suitable for the foreseeable future’.
Acknowledgement that ‘conservation introductions, including assisted colonisation in response to climate change, can have a valid role in conservation. It is recognised that conservation introductions pose far greater potential risks and uncertainties than reinforcements or reintroductions, and should therefore be only progressed when there is a high level of confidence over the organisms’ performance after release’ (pers. comm. Mary Davis, 24
Species Recovery Officer, RSPB, 12/10/2013).
Committee on Climate Change (Independent, evidencebased advice to the UK Government)
3.5
Managing the land in a changing climate – Adaptation Sub-Committee progress report, 2013
Page 51: ‘Other adaptation actions may be needed to accommodate inevitable changes. These are likely to include: translocating some species, and adapting conservation objectives and site management regimes to reflect changing climatic conditions and shifting species distributions’
Legislative, policy, social and ethical considerations when pursuing assisted colonisation
Assisted colonisation as a conservation strategy has ethical, social, cultural, economic and political implications. Programs and projects require a clear set of goals and objectives and procedures to anticipate and minimise the potential for conflict and maximise positive synergies. The implementation of assisted colonisations has the potential to create tension amongst stakeholders with competing interests. For instance, adherence to the obligations to save species/ecosystems from extinction at one site (by way of translocation) but to also guarantee that the action will not be detrimental to ecosystems or land-uses at the recipient site may not be possible. However, if assisted colonisation is not implemented, the focal species/ecosystem may suffer extinction, thereby causing a neglect of duty (Schwartz et al., 2012). Conservation strategy and operational actions, in all Australian jurisdictions, occur within general legislative and policy frameworks. These in turn represent a synthesis of prevailing social values and priorities, a prior history of conservation management practices, a scientifically informed legislative and policy development process, and an empirical determination of the necessary and acceptable scope of regulation and deployment of resources. Regulatory frameworks do not capture the full range of philosophical or ethical considerations that exist in society, nor do they provide resolution per se of potential differences over these, or of unresolved scientific questions, or of conflicts of perception and interest among stakeholders. 25
They do however provide a framework around which those issues can be identified and potentially resolved, and into which new subordinate policies and guidelines can be developed on an adaptive management basis. However, if there is one consistent theme over recent decades in all law and policy relating to biodiversity conservation, it is a recognition that we face an accelerating rate at which species are being driven towards or into extinction, as part of a general decline in natural systems, and a that conservation strategy should be directed to slowing and eventually reversing that process. In some overarching legislative and policy documents relevant to NSW, the commitment to prevention or minimisation of species extinction is explicit. The primary example is the NSW Threatened Species Conservation Act 1995: Section 3 (Objects of Act): (a) to conserve biological diversity and promote ecologically sustainable development, and (b) to prevent the extinction and promote the recovery of threatened species, populations and ecological communities, and (c) to protect the critical habitat of those threatened species, populations and ecological communities that are endangered, and (d) to eliminate or manage certain processes that threaten the survival or evolutionary development of threatened species, populations and ecological communities, and (e) to ensure that the impact of any action affecting threatened species, populations and ecological communities is properly assessed, and (f) to encourage the conservation of threatened species, populations and ecological communities by the adoption of measures involving co-operative management.
In other overarching legislation and policy the commitment to minimisation or prevention of species extinction is implicit within generalised conservation objectives, e.g.: •
Commonwealth Environment Protection and Biodiversity Conservation Act 1999 (section 3, Objects of the Act);
26
http://www.environment.gov.au/topics/about-us/legislation/environmentprotection-and-biodiversity-conservation-act-1999 •
Australia’s Biodiversity Conservation Strategy 2010–2030 (e.g. ‘Our Vision’, ‘Principles underpinning the Strategy’, and ‘Call to action’ sections); http://www.environment.gov.au/node/14488
•
Draft New South Wales Biodiversity Strategy 2010–2015 (Objective 4) http://www.environment.nsw.gov.au/biodiversity/nswbiostrategy.htm
There is thus a clear legislative and policy mandate for conservation actions aimed at reducing extinction risk. Insofar as such governmental documents also embody a social ethical consensus, this overarching goal can also be assumed to have broad social acceptability, at least to the extent the actions proposed are compatible with other social objectives. Generalised acceptability however does not mandate all potential actions nor ensure best practice. A large literature, too large to survey in this report, documents inadvertent adverse effects on biodiversity from inappropriate actions in natural resource management in general and sometimes directly in conservation programs. As a result, conservation agencies and responsible practitioners place heavy stress on nesting conservation actions within broadly agreed science-based and (preferably) critically evaluated programs, which are often government-led. Actions involving vertebrate animals, whether for research or direct conservation management, are now also usually subject to one or more specific institutional ethics approval processes. Agencies and most practitioners are properly cautious where highly interventionist techniques are proposed for the conservation of wild species. Translocation in general, and assisted colonisation in particular, are techniques of this sort. There is an ultimate dilemma, to be assessed and resolved on a case by case basis, between acting to reduce extinction risk versus the risk of failure and/or inadvertently making the situation worse for the subject species or others. One of the main precepts of medical bioethics (“first, do no harm”) is an appropriate guideline. The decision for or against a strongly interventionary action is the core conservation question (along with associated issues of shortfalls in knowledge-base and technical capabilities). It needs to be addressed, to the extent possible, before or at least 27
distinct from the evaluation of other considerations not driven by the conservation goal (e.g. cost/benefit, competing socio-economic interests, conflicts with other policy), although any of the latter may in practice be sufficient to negate the purely conservation considerations in any one case. While assisted colonisation projects remain at a relatively low level of frequency, tensions and conflicting goals may be, and usually are, resolvable on a case by case basis. However it will be better in the long run, and particularly if assisted colonisation becomes a more frequent technique, for the necessarily unique factors in each case to be situated within a policy and guidelines framework that applies to all conservation translocations (including climate-related assisted colonisation), and provides planners and managers with general guidance on consultation, stakeholder identification, proposal development, and socio-ethical case analysis. A requirement for a formal translocation proposal for each project, coupled with a pro-forma for such proposals that requires that scientific, socio-ethical and consultation factors all be addressed, would help to ensure consistency to the degree possible and anticipate, prevent or minimise conflicts. The uncertainties and risks associated with assisted colonisations for legislators can also be lessened by the use of structured and transparent decision making processes. It will be imperative that policy makers coordinate at the national through to local government level to provide consistent legislation and policy. The fate of alpine species that are elevationally restricted in one state but not another is a prime example of where State co-operation will be required. Co-ordination at the international level may also be required for migrant species protected under treaties such as the Ramsar Convention on Wetlands. The input of researchers and groups with practical conservation experience such as Birdlife Australia, Australian Network for Plant Conservation, Greening Australia, and other various ecological experts and conservation stakeholders should also be incorporated. At the societal level, Schwartz et al. (2012) argue that legislators must be vigilant that any new laws encompassing assisted colonisation do not weaken society’s commitment to biodiversity protection. Public consultation and education on the merits and possible downsides of assisted colonisation will be critical in maintaining legislative strength and agency leadership, and acquiring acceptance of new species in new locations. The acceptance and involvement of local groups in 28
the colonisation of new species as care takers and protectors of the focal species at the new site may also be helpful in translocation success. The financial cost of assisted colonisations is likely to require additional government funding and the amount will be context specific, as are all types of translocations. As a guide, the cost of flora translocations in Australia varies enormously between projects: ~ $5,000 for basic projects with sub-optimal monitoring; $30,000 for large projects with >1000 individuals with limited monitoring; at least $100,000 over 15 years; $10,000 to $1,000,000 (Hancock et al., 2014). In comparison, the reported cost of a Chinese translocation project that moved orchid species beyond its current range was 1.5 million USD in 2012 (Liu et al., 2012). As with all innovative conservation techniques, both the chances of success and greater efficiencies are likely to increase ‘with practice’. Encouragement of experimental actions to test procedures and identify problems will pay dividends in the future.
3.6 Is assisted colonisation the appropriate solution? Investigating lower risk strategies for climate change adaptation Translocations, whether specifically designed for climate change adaptation (assisted colonisation) or for managing more proximal threats to species, are expensive, difficult to implement, and require a long-term commitment of resources. Even after considerable effort, success may not be guaranteed. Therefore, all alternative management actions that may help to ensure the survival of a species or community should be considered prior to making the decision to create new populations. Whilst predictions of the adverse effects of climate change on species have rapidly accumulated over the last three decades, evidence for the efficacy of assisted colonisation as a tool for adaptation has been slower to emerge. The lack of empirical information on which to base assisted colonisation guidelines increases the uncertainty surrounding the planning, implementation and monitoring of this type of conservation action. Implementing lower-risk strategies that can be undertaken now may help to increase the capacity for at-risk species to adapt to a changing climate, and ultimately may negate the need for assisted colonisation in some circumstances. Actions for facilitating climate change adaptation in species may include:
29
•
Increasing and/or restoring landscape connectivity; (Heller & Zavaleta, 2009; Shoo et al., 2013);
•
Identifying and protecting potential micro-climate refugia (Corlett & Westcott, 2013; Shoo et al., 2013);
•
Reducing multiple stressors to increase resilience (Lindenmayer et al., 2010);
•
Expanding ex-situ conservation (Vitt et al., 2010);
•
Revising protocols on provenance to take account of climate change (Broadhurst, 2008; Breed et al., 2013; Sgro et al., 2011; Whalley et al., 2013);
•
Updating conservation translocation guidelines to include translocations outside of their indigenous range due to threats from climate change (assisted colonisation) (Byrne et al., 2011b).
It is generally recognised that assisted colonisation will not be effective as a climate change adaptation measure if implemented in isolation (Lindenmayer et al., 2010). In-situ measures to mitigate other threatening processes that are likely to be exacerbated by climate change should be tackled first, with assisted colonisation only recommended if these strategies fail or are deemed inappropriate.
SECTION 4 - When does assisted colonisation have the most likelihood of success?
4.1 Evaluating the success of past translocations Evaluating the success of past translocation projects provides insight into how to improve the likelihood of an assisted colonisation being successful. Unfortunately, there are relatively few well-documented examples of successful translocation projects where self-sustaining populations have been formed. The value, efficiency & effectiveness of translocation in general (and hence also assisted colonisation) remains largely unknown given that the success of most past translocation projects is uncertain or unevaluated & there has been a general lack of monitoring, evaluation & comparative studies. Improved monitoring and evaluation of translocation activities will increase the effectiveness of decision making regarding the role of translocation and specifically assisted colonisation. Appendices 1-4 of this report catalogue known flora translocations undertaken in Australia, published reviews of flora and 30
fauna translocations and a series of case-studies on experimental assisted colonisations.
4.2 Introducing six key themes for successful assisted colonisation The IUCN states that ‘the pivotal criteria for justifying any conservation translocation will be situation-and species-specific’ (IUCN/SSC, 2013). However, six key and interrelated themes repeatedly appear in the literature with general suggestions or recommendations for successful assisted colonisations. The themes: site selection and preparation, predictive tools, genetic diversity, lessons from invasive species research, species information and adaptive management are discussed below.
4.3 Recipient site selection and preparation The characteristics of the sites that receive assisted colonised species (recipient sites) will have a major influence on the success or otherwise of assisted colonisations. The purpose of assisted colonisation is to move species to areas with suitable future climate and hence reduce the extinction threat present at the donor site. Species distribution models are helpful in selecting suitable sites (see Predictive Models section below), provided long term reliable climate projections are available for the site. In general, translocations and ecological restorations are more likely to fail where there is a large difference in the biogeographic regions between the source and the recipient populations (Dalrymple & Broom, 2010; Thomas, 2011). Potential recipient sites for plants, for example, should be representative of predicted future climate and edaphically match the source site. The introduction of organisms into sites free from predators, pests and / or pathogens may increase the chance of translocation success. In a review of Australian vertebrate translocations, predation was cited as the key reason for the project failure for mammals and birds and a significant issue for reptiles and amphibians (Short, 2009). Furthermore, sites free of key threatening processes yielded greater translocation success than sites that were less secure. For plant translocations, in some cases, the exclusion of grazing herbivores is desirable (Vallee et al., 2004). However, the financial and potential ecological costs of fencing need to be considered and managed in any conservation translocation (Hayward & Kerley, 2009). 31
Site selection should also consider the availability of co-dependent organisms, and the adequacy of site size and tenure. The decision where to introduce populations to ensure continued stewardship and protection will also have a bearing on success (Bennett et al., 2013). Preferably, sites will be located inside the protected area network, such as national parks and reserves. It should be noted, however, that the most suitable habitat may lie outside the protected area network. For instance, land owned by non-government organizations such as Bush Heritage, Birdlife Australia, or Arid Recovery as well private land-holders may become increasingly important for recipient site selection for assisted colonisation projects. Potential sites may include those where there are existing gaps in biological function that can be filled by candidate species or fall within migration corridors in order to aid meta-population establishment (Harris et al., 2013). A range of alternative strategies for locating suitable recipient sites and/or expanding existing populations into suitable habitats have been identified, including: •
the rehabilitation of unproductive or marginal agricultural land and degraded mining leases with ‘climate ready’ plants (Lindenmayer et al., 2010);
•
active promotion of the benefits of pollination services to agricultural sectors to promote the introduction of bee species (Lunt et al., 2013);
•
use of golf courses, public spaces and private gardens as stepping stones or corridors to, or as recipient sites (Harris et al., 2013).
However, the use of recipient sites on non-government land will also need to take account of socioeconomic factors important to the stakeholders to provide secure tenure.
4.4 Predictive Models The use of predictive tools to assist in facilitating successful assisted colonisations is a vital part of planning and implementation. Here we describe three predictive tools: climate models, species distribution models and population viability analysis.
Climate models (e.g. Global Circulation Models or Global Climate Models (GCMs)) are used to predict the future climate of both source and recipient sites. The current generation of climate models reproduce observed continental-scale surface temperature patterns and trends over many decades with a high-level of confidence 32
(IPCC, 2013). Similarly, model simulation of extreme weather events and other climate phenomena such as ENSO has improved substantially, increasing the level of confidence assigned to predictions of future climate conditions under higher greenhouse gas concentrations (IPCC, 2013). Whilst there is high confidence in models of climate at the global scale, predictions from regional climate models are essential for finer-scale identification of at-risk species or communities and recipient sites for assisted colonisation projects (e.g. NARCLIM – NSW/ACT Regional Climate Modelling project producing an ensemble of regional climate projections for southeast Australia.
Species distribution models (SDMs), are used to predict the distribution of suitable habitats for species, under both current and future climate scenarios. Also termed ecological niche, environmental niche, habitat suitability and bioclimatic envelope models (Pearson, 2007), SDMs employ either a correlative or mechanistic approach. Correlative models combine species occurrence records with gridded environmental data (e.g. climate, soils) to project the location of suitable habitat for individual species, or suites of species (Guisan & Thuiller, 2005). By contrast, mechanistic SDMs project species’ ranges by incorporating information on physiologically-limiting mechanisms which govern tolerance to conditions with environmental data (Pearson, 2007). Correlative models are more commonly employed due to the availability of occurrence records, climate data and freesoftware, whereas detailed biological data needed for mechanistic models is often unavailable (Pearson, 2007).There is some evidence that mechanistic models may be more informative for selecting suitable recipient sites than are correlative approaches. For instance, Mitchell et al. (2013) showed that mechanistic models performed better than correlative models at identifying recipient sites for rangerestricted species, such as the Critically Endangered Western Swamp Tortoise (Pseudemydura umbrina) in Western Australia. It is important to note that the utility of models for identifying candidate species or recipient sites is substantially improved when a combination of tools and parameters are used (Pearson & Dawson, 2003; Angert et al., 2011). For instance, extending the type of parameters used to calibrate SDMs beyond climate variables to include such factors as topography, soil conditions, dispersal distances, 33
evolutionary change, biological traits and biological interactions will fine-tune predictions. Where dispersal distances are combined with SDM output, estimates can be made as to whether the rate of dispersal will match the rate of climate change (Engler et al., 2009). A recent example of this approach used genetic information to project the future distribution of a widely distributed Australian gecko, Gehyra variegata (Duckett et al., 2013). Genetic analysis showed that dispersal rates for the gecko varied across the landscape (from a mean of 1.69 - 6.26 km year -1) and that the current range of the gecko is predicted to decline by 0.87 (±0.25) million km-2 by 2030 and further by 0.62 (±0.24) million km-2 by 2070 (Duckett et al., 2013). The authors inferred from the results that 17 – 41% of the species’ current distribution will not keep pace with the predicted velocity of climate change. The study also identified populations that may become isolated and suffer the consequences of environmental stochastic events and population viability problems (Duckett et al., 2013). Other examples of more complex modelling approaches include: (1) Assessing the vulnerability to climate change of 16,857 species of birds, amphibians and corals species using biological traits alongside of habitat suitability projections under climate change (Foden et al., 2013). (2) Dispersal kernel models that simulate migration rates, allowing for rare, long distance dispersal events in order to predict the probability of colonisation beyond the current range over long time periods (Iverson et al., 2004).
However, predictive models have limitations which include: (1) Species distributions used as baseline observations may not be in equilibrium with the current climate; (2) Realized niches used in models may not represent absolute ranges, effecting predictions for future distributions; (3) Impact of dispersal barriers are not always identified; (4) Modelling done at the global scale does not always allow for widespread application at the regional scale or for specific species. These limitations need to be taken into account when interpreting the outputs.
Population Viability Analyses (PVAs) model the effects of different life history, environmental and threat factors (deterministic and stochastic) on the population size 34
and extinction risk of populations or species (Frankham et al., 2010). Historically, PVAs have been used to predict reproductive and survival parameters for threatened species. PVAs would arguably be of benefit in assessing potential assisted colonisation projects, for both the source and recipient populations. Information on reproduction, mortality rates, population size, carrying capacity, frequency and effects of threats and genetic information (susceptibility to inbreeding depression and gene flow) are required for analysis (Frankham et al., 2010). In reality, there are low prospects of being able to meet PVA data requirements for more than a small set of species. Hence, the initial choice of species for investment in PVA needs to screen for the likely generalisability of some / all outcomes, and all actual outcomes need to be carefully evaluated.
4.5 Genetic diversity The presence of genetic diversity is an important factor in the success of any conservation translocation. Genetic considerations in successful translocations include the avoidance of inbreeding and outbreeding depression, a loss of genetic diversity due to founder effects or genetic drift and the ability to maintain appropriate breeding systems (Menges, 2008). Genetic diversity can be divided into two categories: neutral and adaptive. Neutral genetic diversity reflects population dynamics and evolutionary forces such as genetic drift, mutation and migration and is not under natural selection (Sgro et al., 2011). Adaptive genetic diversity is under natural selection and gives rise to the ability to adapt to new environments (Sgro et al., 2011). It is therefore important that translocations that introduce populations outside of its known historical range (assisted colonisations) have adequate levels of both types of genetic diversity to enable adaptive capacity. Estimates of both types of genetic diversity may be difficult to attain. Commonly-proposed strategies to retain maximum genetic diversity are to source the transplant genetic material from multiple sources (Frankham et al., 2010) and from provenances that match likely future climate at the recipient site to increase adaptability (Sgro et al., 2011). The minimum number of reproductive individuals required to keep pace with environmental change by maintaining adaptive potential is estimated to be in the low thousands (Willi et al., 2006; Frankham et al., 2014). A review of plant reintroductions found that mixing material from diverse populations 35
resulted in higher survival rates of restored individuals than where sourced from a single population (Godefroid et al., 2011). Information that attributes translocation success or failure because of levels of genetic diversity is, however, not always available. Consideration should also be given to potential detrimental effects on the genetic diversity of source populations where extensive harvesting of seed material is carried out to help establish new populations. Population viability analysis that model genetic factors will be helpful in determining the degree of detrimental effect on the source population and the numbers needed for new populations to persist. In the context of assisted colonisation, it is important to identify the financial and ecological trade-offs between moving unthreatened extant populations, currently with substantial adaptive capacity, and prioritizing threatened species with reduced genetic diversity, but with a high need for translocation due to other stressors. A review of Australian vertebrate translocations found that translocation success rates were higher for non-threatened bird and mammal species, than for threatened species (Short, 2009). If the assumption is made that threatened species have low levels of genetic diversity (due to small population numbers), the results of this study implies that it is better to translocated before genetic diversity is further reduced. Frameworks of genetic considerations for translocations under climate change are provided by Weeks et al., (2011).
4.6 Species information There is a long list of biological information that is lacking for many species to enable confident predictions of successful assisted colonisations. All translocations are undoubtedly more successful where there is knowledge of: •
Climatic breadth and niche;
•
Expected successional trajectories;
•
Disturbance regimes required for reproduction;
•
Breeding system;
•
Genetic diversity;
•
Ideal growing conditions (e.g. moisture, light, nutrients) for plants;
•
Mutualisms;
36
•
Critical life stage requirements (e.g. early progeny needs, reproductive triggers);
•
Habitat preferences;
•
Diet breadth (for animals);
•
Physiological constraints on growth and survival.
However, the time taken to acquire knowledge before acting needs to be balanced against the potential consequences of failing to act soon enough. The risk of acting without knowledge also needs to be evaluated. Species and situations that present low-risk opportunities for assisted colonisation should be prioritised. For instance, the IUCN/SSC (2013) have identified a situation where a species has gone locally extinct, creating a gap in ecological function, as a potentially low-risk translocation project. In this situation, a functionally similar species that is threatened by climate change elsewhere could perform a replacement ecosystem function. Species known to have high levels of phenotypic plasticity may be better adapted to withstand extreme events and to therefore successfully colonise recipient sites (Bernazzani et al., 2012) and make ideal candidates to serve as ecological replacements (on the basis that high levels of plasticity may mean that they are less likely to be threatened in-situ).
4.7 Learning from invasive species research To mitigate against the potential for species which are subject to assisted colonisation becoming invasive, rigorous monitoring of recipient sites and dispersal corridors needs to be conducted. However, conflicts may arise when trying to define ‘success’ in an assisted colonisation project where large numbers of new individuals are being recruited, leading to a reduction in the abundance and diversity of extant vegetation at the recipient sites. A clear, working definition of optimal success should therefore be outlined prior to the commencement of an assisted colonisation to avoid ambiguity between appropriate population growth and invasive behaviour (Vallee et al., 2004). Practitioners of assisted colonisations need to balance both how to prevent invasive behaviour in translocated species, and how to increase the potential for success. Research shows that the following factors are crucial in successful
37
invasions and should be taken into account when designing assisted colonisation projects:
(1) Propagule pressure and introduction effort. The number of times and the number of individuals that have been introduced to a new range is a critical predictor of the ability for species to naturalise and become invasive (Lockwood et al., 2005; Simberloff, 2009). (2) Minimum residence time. The amount of time since the species was introduced to the new range. Invasions typically progress through a lag phase for several years immediately following introduction where population numbers build as species adapt to novel conditions. Once a critical threshold of individuals has been reached, population growth is exponential and introduced species can spread rapidly (Pyšek et al., 2005). Total eradication is only considered feasible during the lag-phase, when population numbers are low and locally contained. (3) Climate matching. Species are more likely to become invasive if the recipient site where they are introduced has similar abiotic conditions to their native range (Gordon et al., 2008; Bomford et al., 2009). Whilst species do have the capacity to shift their niche upon introduction (Gallagher et al., 2010), similarity in climate and abiotic conditions between the native and exotic range is repeatedly identified as crucial in invasions.
4.8 Adaptive management Due to the nascent nature of assisted colonisation, it follows that management will need to be structured and adaptive. Actions should be based on the best available knowledge and any uncertainties should be acknowledged (Chauvenet et al., 2013). Theoretical guidelines, risk management tools and decision frameworks have previously been developed to assist all aspects of decision making surrounding assisted colonisation (Table 3). The use of more than one framework may be necessary and should incorporate risk management tools that are not specifically designed for assisted colonisations but are nonetheless applicable. A comprehensive synthesis of some of these tools appears in Chauvenet et al. (2013)
38
which also provide a comprehensive list of pre- translocation questions to ask and details of where to find the answers.
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50
Zakharov, E.V. & Hellmann, J.J. (2008) Genetic differentiation across a latitudinal gradient in two co‐occurring butterfly species: revealing population differences in a context of climate change. Molecular Ecology, 17, 189-208.
51
Appendix 1 Compilation of established flora translocations in Australia The transfer of knowledge of prior translocations is important to the success of future projects. Respondents from the Flora translocation survey (2013) were asked how the availability of data can be ensured for future workers. No single preferred repository was identified but a common theme was that it is preferable to publish data in as many locations as possible, although the ‘grey’ literature was preferred to more formal journals. For some respondents, this preference arises from the inaccessibility of formal journals and the potential for misplacement of data/reports by Government Agencies that change through time. The most often mentioned non-formal venue for publication was the ANPC's bulletin Australasian Plant Conservation. Respondents were also asked to provide details of where they have lodged reports of their projects. Table 1 lists by species, details of published, “grey” or unpublished reports, websites or locations of reports that contain information regarding the translocation project. This information was provided by respondents of the Flora Translocation Survey (2013) and therefore contains various referencing styles. Table 2 lists vegetation communities and groups of species for which information on translocations was identified in the course of this survey and review. In addition, general publications nominated by the survey respondents, or opportunistically found by the author, are included at the end of the paper. This report has not systematically searched for translocation knowledge in the large body of forestry literature. While experimental forestry plantings often deal with strongly selected or cross-bred genotypes, this is not always the case – and even for those the techniques used are highly relevant for trait selection for future assisted colonisation projects. In addition, the projects cited below are heavily skewed towards threatened species, whereas a large body of information on revegetation and restoration exists from which important principles can be drawn.
52
Details of information sources and translocation details from the Flora Translocation Survey, 2013. Notes pertaining to the table: Species: Name of the species translocated. State: Distribution by State/Territory as per the Atlas of Living Australia website: http://ala.org.au. Conservation status: Survey respondents provided the conservation status or indicated (yes or no) if the species was legislatively listed at the time of translocation as ‘threatened’ (State, Commonwealth &/or IUCN) or on the non-legislative ROTAP list. Habit: Woody plant - short-lived < 10 years; Woody plant - long-lived ≥ 10 years; Non-woody plant – perennial; Non-woody plant – biennial; Non-woody plant – annual Breeding System: Sexual; Asexual; Can be sexual &/or asexual; Other Translocation type: Respondents were provided with a glossary containing descriptions of the following translocation types (IUCN/SSC (2013): Assisted colonisation (Benign introduction; Assisted migration; Managed relocation): the intentional movement and release of an organism outside its indigenous range to avoid extinction of populations of the focal species. For the purposes of this survey, it is used as a conservation strategy for species facing extreme threat from climate change. Ecological replacement (Taxon substitution; Ecological substitutes / proxies / surrogates; Subspecific substitution, Analogue species): the intentional movement and release of an organism outside its indigenous range to perform a specific ecological function. Introduction: the intentional movement and release of an organism outside its indigenous range. Reinforcement (Augmentation; Supplementation; Re-stocking; Enhancement): the intentional movement and release of an organism into an existing population of conspecifics. Reintroduction: the intentional movement and release of an organism inside its indigenous range from which it has disappeared. Method: Transplant method – method of planting: seedling transplant; adult transplant; direct seeding. For the purposes of this survey, the definition of seedling transplant was assumed to cover those plants grown by seed in a nursery or propagated by cuttings. However, this definition was not included in the glossary and some respondents distinguished between the two. Completion: Has the project finished (has formal monitoring ceased)? Group: If the project is finished, is there an informal interest group maintaining some involvement? N.B. Where the species’ translocation details are listed more than once, it is possible that they represent the same projects but note that not all details are the same.
53
Species
State
Report/citation details
Acacia aprica
WA
Monks L and Coates D (2002) The translocation of two critically endangered Acacia species Conservation Science Western Australia Vol 4(3) 54-61
Acacia pubescens
NSW
Acacia volubilis
WA
Conservation status Critically endangered: State level, Critically Endangered or Endangered: Federal level
Breeding System Sexual and other (possible selfing)
Habit
Translocation type Introduction
Method
Complete
Seedling transplant & direct seeding
No
1. Moore R. J. and Clements A. (June 1998) Acacia pubescens (Vent.) R. Br. (Downy Wattle) – a threatened species of western Sydney, Australia Conference documentation - Planta Europa – Second European conference on the conservation of Wild Plants, 9-14 June 1998, Uppsala, Sweden 2. Moore, R., Peakall, R. & Clements, A. (1999). Analysis of the genetic diversity of Acacia pubescens: an assessment of clonality and its conservation implications. Prepared for NSW NPWS Central Directorate, Hurstville
Endangered and Vulnerable
Sexual
Woody plant longlived ≥ 10 years
Reinforcement
Adult transplant
Yes
Yes
3. Unpublished ecological reports to the client, various government departments (inc. OEH) from ecological consultant. Consultants have given talks to various bodies (workshops, seminars, conferences)
Yes
Can be sexual &/or asexual
As above
Ecological replacement
As above
As above
No
Limited information available from Dept. Parks and Wildlife (WA)
Critically endangered: State level, Critically
Sexual and other (possible selfing)
Nonwoody plant -
Reinforcement
Seedling transplant & plants grown
No
Woody plant longlived ≥ 10 years
54
Group
Species
State
Report/citation details
Conservation status Endangered or Endangered: Federal level
Breeding System
Habit
Translocation type
perenni al
Method
Complete
Group
from cuttings as well as seed
Acacia whibleyana
SA
1. Jusaitis M (2010) Augmentation of a Whibley Wattle population in South Australia by translocation IUCN "Global ReIntroduction Perspectives. 2010 Additional case-studies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 297-300. 2. Jusaitis M and B Sorensen (1998). Conservation Biology of Acacia whibleyana. Black Hill Flora Centre, Botanic Gardens of Adelaide. 3. Jusaitis M and B Sorensen (2007). Successful augmentation of an Acacia whibleyana (Whibley Wattle) population by translocation. Australasian Plant Conservation 16(1): 23-24 4. Jusaitis M and L Polomka (2008). Weeds and propagule type influence translocation success in the endangered Whibley Wattle, Acacia whibleyana (Leguminosae: Mimosoideae). Ecological Management & Restoration 9: 72-75
CE (IUCN)
Sexual
Woody plant longlived ≥ 10 years
Reinforcement
Seedling transplant & direct seeding
Yes
Acanthocladium dockeri
NSW SA
1. Jusaitis M and M Adams (2005). Conservation implications of clonality and limited sexual reproduction in the endangered shrub Acanthocladium dockeri
Yes
Other
Nonwoody plant – perenni al
Reintroduction
Seedling transplant
No
Yes
55
Species
State
Report/citation details
Conservation status
Breeding System
Habit
Translocation type
Method
Complete
Group
Asexual
As above
Introduction
As above
Yes
As above
Yes
Sexual
Reinforcement
Direct seeding
Yes
Yes
Yes
Sexual
Reinforcement
Seedling transplant
Yes
Yes
State (E) and Commonwealth (CE)
Sexual
Woody plant longlived ≥ 10 years Woody plant longlived ≥ 10 years Woody plant longlived ≥ 10 years
Introduction
No
n/a
Nonwoody plant -
Introduction
Seedling transplant but not actually planted yet Direct seeding
No
n/a
(Asteraceae). Australian Journal of Botany 53: 535-544. CE (IUCN) 2. Sharp A, A Clarke, M Jusaitis, A Pieck, P Slattery and D Potter (2010). Translocations of the critically endangered spiny daisy in the Mid-north of South Australia. In PS Soorae (ed), Global Reintroduction Perspectives: 2010. Additional case-studies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 340-344 Allocasuarina glareicola
NSW
Allocasuarina portuensis
NSW
Arachnorchis actensis now: Caladenia actensis
ACT
Artanema fimbriatum
NSW QLD
NPWS reports and recovery plans
http://www.rms.nsw.gov.au/roadprojects/pro jects/pac_hwy/coffs_harbour_ballina/devils _pulpit/public_information.html (construction documentation)
Sexual
56
Species
State
Report/citation details
Conservation status
Breeding System
Habit perenni al Nonwoody plant perenni al Nonwoody plant perenni al Nonwoody plant perenni al Woody plant longlived ≥ 10 years
Translocation type
Method
Complete
Group
Reinforcement
Seedling transplant
No
Yes
Reinforcement
Seedling transplant
No
Yes
Ecological replacement
Adult transplant
No
Yes
Introduction
Seedling transplant
No
n/a
Astelia alpina
NSW TAS VIC
No
Can be sexual &/or asexual
Astelia psychrocharis
NSW VIC
No
Can be sexual &/or asexual
Baloskion australe
ACT NSW TAS VIC
No
Can be sexual &/or asexual
Banksia anatona
WA
Critically Endangered EPBC
Sexual
Banksia brownii
WA
Cochrane, J. A.; Barrett, S.; Monks, L.; et al., 2010, Partnering conservation actions. Inter situ solutions to recover threatened species in South West Western Australia, Kew Bulletin, Volume: 65 Issue: 4 Pages: 655-662 1. Cochrane, J. A.; Barrett, S.; Monks, L.; et al., 2010, Partnering conservation actions. Inter situ solutions to recover threatened species in South West Western Australia, Kew Bulletin, Volume: 65 Issue: 4 Pages: 655-662
Endangered EPBC
Sexual
Woody plant longlived ≥ 10 years
Introduction
Seedling transplant
No
n/a
2. Internal reports for translocation approvals and monitoring reports. Overall reports to be published
Threatened State &
As above
As above
As above
As above
As above
As above
57
Species
State
Report/citation details
Conservation status Endangered EPBC
Breeding System
Habit
Translocation type
Method
Complete
Group
Banksia montana
WA
1. Sarah Barrett, Rebecca Dillon, Anne Cochrane & Leonie Monks 2011 Conservation introduction of a threatened narrow range endemic species, Banksia montana, from the Stirling Range National Park, southern Western Australia In PS Soorae (ed), Global Re-introduction Perspectives: 2011.IUCN Additional casestudies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 220- 223. 2. Cochrane, J. A.; Barrett, S.; Monks, L.; et al., 2010, Partnering conservation actions. Inter situ solutions to recover threatened species in South West Western Australia, Kew Bulletin, Volume: 65 Issue: 4 Pages: 655-662 3. Internal reports for translocation approvals and monitoring reports. Overall reports to be published (see Dryandra nivea ssp uliginosa)
Threatened State & Endangered EPBC
Sexual
Woody plant longlived ≥ 10 years
Introduction
Seedling transplant
No
n/a
Critically endangered
As above
As above
As above
As above
As above
As above
Accepted for publication in the upcoming IUCN "Global Re-Introduction Perspectives" due to come out later this year (2013)
E (SA)
Sexual
Nonwoody plant perenni al
Introduction
Seedling transplant
No
No
Banksia nivea ssp. uliginosa Brachyscome diversifolia
ACT NSW QLD SA TAS VIC
58
Species
State
Report/citation details
Brachyscome muelleri
SA
1. Paper accepted for publication in the upcoming IUCN "Global Re-Introduction Perspectives" due to come out later this year (2013). 2. Jusaitis M, L Polomka and B Sorensen (2004). Habitat specificity, seed germination and experimental translocation of the endangered herb Brachycome muelleri (Asteraceae). Biological Conservation 116: 251-266. 3. Jusaitis M, B Sorensen and L Polomka (1998). Conservation Biology of Brachycome muelleri. Black Hill Flora Centre, Botanic Gardens of Adelaide.
SA VIC
Caladenia concolor
Caladenia hastata
Caladenia actensis See Arachnorchis actensis Caladenia calcicola
Conservation status CE (IUCN)
Breeding System Sexual
Habit
Provided (initially) to research institute
Endangered EPBC, listed Vic.
Sexual
NSW SA VIC
ANPC plant conservation journal Regional Reports- personal comments.
Threatened in State and vulnerable in Federal
Sexual
VIC
Data unpublished and held with DEPI
Endangered EPBC, listed Vic.
Sexual
Nonwoody plant perenni al Nonwoody plant perenni al Nonwoody plant -
Nonwoody plant perenni al
Translocation type Introduction
Method
Complete
Group
Seedling transplant & Direct seeding
No
No
Reintroduction
Seedling transplant
No
Reinforcement
Reintroduction
Seedling transplant
No
Yes
Yes
No
59
Species
State
Cassinia rugata
TAS VIC
Celmisia pulchella
ACT NSW
Chorizema humile
WA
Cupaniopsis newmanii
Darwinia carnea
Report/citation details
Data unpublished and held with DEPI
Conservation status
Breeding System
Habit perenni al Woody plant longlived ≥ 10 years Nonwoody plant perenni al Nonwoody plant perenni al
Translocation type
Method
Complete
Group
Reintroduction
Seedling transplant
Yes
No
Reinforcement
Seedling transplant
No
Yes
Introduction
Seedling transplant & Plants grown from cuttings as well as seed Seedling transplant from cuttings / some direct seed Seedling transplant
No
Vulnerable EPBC, listed Vic.
Sexual
No
Sexual
Limited information available from Dept. Parks and Wildlife (WA)
Critically endangered: State, Critically Endangered or Endangered: Federal
Sexual and other (possible selfing)
NSW QLD
http://www.tmr.qld.gov.au/~/media/Projects/ B/Beechmont%20Road%20Upgrade%20Lo wer%20Beechmont/beechmontroadupgrad ecompliancereport.pdf.
Near threatened (NCA)
Sexual
Woody plant longlived ≥ 10 years
Reinforcement
WA
Internal reports for translocation approvals and monitoring reports. Overall reports to be published
Critically endangered
Sexual
Woody plant shortlived < 10 years
Reinforcement
No
Yes
Yes
60
Species
State
Report/citation details
Darwinia ferricola
WA
Daviesia bursarioides
WA
Dixon B 2010 Translocation of four rare ironstone endemic species onto a premined area at Beenup in SW Australia In PS Soorae (ed), Global Re-introduction Perspectives: 2010.IUCN Additional casestudies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 301- 305. http://www.bgpa.wa.gov.au/science/biodiver sity-and-extensions/beenup-translocation Limited information available from Dept. Parks and Wildlife (WA)
Daviesia cunderdin
WA
Dillwynia tenuifolia
NSW
Diuris chryseopsis
ACT NSW SA TAS
Limited information available from Dept. Parks and Wildlife (WA)
ANPC plant conservation journal Regional Reports- personal comments
Conservation status State, IRP176 as Priority? Endangered under Commonwealth EPBC Act
Breeding System Sexual
Habit
Translocation type Reintroduction
Method
Complete
Group
Seedling transplant of cuttings only
Yes
No
Critically endangered: State, Critically Endangered or Endangered: Federal Critically endangered: State, Critically Endangered or Endangered: Federal
Sexual and other (possible selfing)
Woody plant longlived ≥ 10 years
Reinforcement
Seedling transplant
No
Sexual and other (possible selfing)
Woody plant longlived ≥ 10 years
Introduction
No
Yes
Sexual
Reinforcement
Yes
Yes
No
Sexual
Woody plant longlived ≥ 10 years Nonwoody plant -
Seedling transplant & Plants grown from cuttings as well as seed Direct seeding
Adult transplant
No
Yes
Woody plant longlived ≥ 10 years
Reinforcement
61
Species
State
Report/citation details
Conservation status
Breeding System
VIC
Habit perenni al Nonwoody plant perenni al Woody plant longlived ≥ 10 years Woody plant longlived ≥ 10 years
Translocation type
Method
Complete
Group
Ecological replacement
Adult transplant
no
n/a
Introduction
Seedling transplant & Direct seeding
Yes
Yes
Yes
No
Diuris tricolor
NSW QLD
Annual monitoring reports & a paper for publication to a mining company
Yes
Sexual
Dodonaea subglandulifera
SA
Paper accepted for publication in the upcoming IUCN "Global Re-Introduction Perspectives" due to come out later this year (2013)
V (IUCN)
Sexual
Dryandra nivea ssp uliginosa (now Banksia nivea ssp. uliginosa)
WA
WA State, IRP 255 as Priority? Endangered under Commonwealth EPBC Act
Sexual
Elaeocarpus williamsianus
NSW
Dixon B 2010 Translocation of four rare ironstone endemic species onto a premined area at Beenup in SW Australia In PS Soorae (ed), Global Re-introduction Perspectives: 2010.IUCN Additional casestudies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 301- 305; http://www.bgpa.wa.gov.au/science/biodiver sity-and-extensions/beenup-translocation 1. NSW NPWS
Yes
Can be sexual &/or asexual
Woody plant longlived ≥ 10 years
Reintroduction
Seedling transplant
No
n/a
2.
Endangered
Sexual
As above
Reinforcement /recombination
Seedling transplant / cuttings
As above
As above
Reintroduction
62
Species
State
Empodisma minor
QLD
Epacris purpurascens var purpurascens
NSW
Eremophila resinosa
WA
Fontainea oraria
NSW QLD
Gentianella meulleriana
ACT NSW
Report/citation details
Conservation status No
Breeding System Sexual
Unpublished ecological reports to the client, various government departments (inc. OEH) from ecological consultant. Consultants have given talks to various bodies (workshops, seminars, conferences)
Yes
Can be sexual &/or asexual
Dixon B Translocation of the resinous Eremophila, from test tube, to a degraded bushland site in the wheatbelt of Western Australia In PS Soorae (ed), Global Reintroduction Perspectives: 2010. IUCN Additional case-studies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 311- 315. http://www.bgpa.wa.gov.au/science/biodiver sity-and-extensions/eremophilatranslocation 1. NSW NPWS
State as Priority 3
Sexual
Endangered
2.
Habit
Translocation type Reinforcement
Method
Complete
Group
Adult transplant
No
Yes
Ecological replacement
Adult transplant
Yes
No
Woody plant longlived ≥ 10 years
Reintroduction
Tissue culture & some direct seeding
No
No
Sexual
Woody plant longlived ≥ 10 years
Reinforcement / recombination
Seedling transplant / cuttings
No
n/a
Yes
As above
As above
Reinforcement
Seedling transplant
As above
As above
No
Sexual
Nonwoody
Reinforcement
Seedling transplant
No
Yes
Nonwoody plant perenni al Woody plant longlived ≥ 10 years
63
Species
State
Report/citation details
Conservation status
Breeding System
VIC
Grevillea batrachioides
WA
Limited information available from Dept. Parks and Wildlife (WA)
Grevillea brachystylis ssp australis
WA
Grevillea caleyi
NSW
Dixon B 2010 Translocation of four rare ironstone endemic species onto a premined area at Beenup in SW Australia In PS Soorae (ed), Global Re-introduction Perspectives: 2010.IUCN Additional casestudies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 301- 305. http://www.bgpa.wa.gov.au/science/biodiver sity-and-extensions/beenup-translocation Unlublished data on experimental translocation with OEH
Grevillea humifusa
WA
Limited information available from Dept. Parks and Wildlife (WA)
Habit plant perenni al Woody plant longlived ≥ 10 years
Translocation type
Method
Complete
Introduction
Seedling transplant
No
Critically endangered: State level, Critically Endangered or Endangered: Federal level WA State as Priority? Endangered under Commonwealth EPBC Act
Sexual and other (possible selfing)
Sexual
Woody plant shortlived < 10 years
Reintroduction
Endangered State & Commonwealth
Sexual
Reinforcement
Seedling transplant & seed
No
Critically endangered: State level, Critically Endangered or Endangered: Federal level
Sexual and other (possible selfing)
Woody plant longlived ≥ 10 years Nonwoody plant perenni al
Introduction
Seedling transplant
No
Yes
Group
No
64
Species
State
Report/citation details
Conservation status TSC Act & EPBC Endangered
Breeding System Sexual
Habit
Grevillea iaspicula
ACT NSW
published articles by John Briggs (NSW OEH) in Australian Plant Conservation
Grevillea parviflora ssp. parviflora
NSW
Wyong Shire Council, Donaldson Coal, Centennial Coal
Vulnerable NSW & Commonwealth
Can be sexual &/or asexual
Woody plant longlived ≥ 10 years
Grevillea scapigera
WA
1. Dixon, B. and Krauss, S. (2004).The Grevillea scapigera case study. Chapter 9. In Vallee, L., Hogbin, T., Monks, L., Makinson, B., Matthes, M. and Rossetto, M (2004). Guidelines for the translocation of threatened plants in Australia (2nd. Edn) pp. 65-69. Australian Network for Plant Conservation, Canberra. 2. Krauss, S.L., Dixon, B., and Dixon, K.W. (2002). Rapid genetic decline in a translocated population of the rare and endangered Grevillea scapigera (Proteaceae). Conservation Biology 16: 986-994. 3. Dixon,B. and Krauss, S. (2008). Translocation of the Corrigin grevillea in south Western Australia. Page 229-234 in Ed. Soorae,P.S. (October 2008) Global reintroduction perspectives: Re-introduction case studies from around the
WA State and Commonwealth as Critically Endangered
Sexual
Woody plant shortlived < 10 years
Woody plant longlived ≥ 10 years
Translocation type Reinforcement
Method
Complete
Group
Seedling transplant
no
n/a
Other experimental translocation from a development site Reintroduction
Adult transplant
No
Seedling transplant & includes tissue culture
Yes
Yes
65
Species
Grevillea wilkinsonii
Haloragis eyreana
State
Report/citation details
NSW
globe.ICUN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE. 4. Dixon, B. and Krauss, S. (2006). The Corrigin Grevillea: 12 years of recovery. Western Wildlife vol.10:2, p.1, 4&5. 5. http://www.bgpa.wa.gov.au/science/biodiver sity-and-extensions/grevillea-translocation 1. ANPC.
SA
Conservation status
Breeding System
Habit
Translocation type
Method
Complete
Group
TSC Act & EPBC – Endangered
Sexual
Woody plant longlived ≥ 10 years
Reinforcement & Reintroduction
Seedling transplant
No
n/a
2. Partial (and only partially quantitative) results and appraisals have been presented in several conference/forum situations separately and together by John Briggs (OEH NSW) and Bob Makinson (RBG Sydney), and in one of two non-peer reviewed articles, in the (non-public) process of expert interviews for the PAS2 process (2012), and in occasional partiallyminuted meetings of the recovery team for the species
ROTAP
As above
Woody plant shortlived ≥ 10 years
Reinforcement
Seedling transplant / cuttings
As above
Yes
1. Jusaitis M and A Freebairn (2010). Habitat manipulation stimulates natural regeneration of Prickly Raspwort (Haloragis eyreana) on Eyre Peninsula (South Australia). Ecological Management & Restoration 11: 81-82.
CE (IUCN)
Can be sexual &/or asexual
Nonwoody plant perenni al
Reinforcement
Seedling transplant & Direct seeding
Yes
66
Species
State
Hemigenia ramosissima
WA
Lachnagrostis limitanea
SA
Lambertia fairallii
Lambertia orbifolia ssp Scott River Plains
WA
WA
Report/citation details 2. Jusaitis M and A Freebairn (2011). Trial translocations into edaphically modified habitats enhanced the regeneration of prickly raspwort on Eyre Peninsula, South Australia. In PS Soorae (ed), Global Reintroduction Perspectives: 2011. More case studies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 205-209. Limited information available from Dept. Parks and Wildlife (WA)
Cochrane, J. A.; Barrett, S.; Monks, L.; et al., 2010, Partnering conservation actions. Inter situ solutions to recover threatened species in South West Western Australia, Kew Bulletin, Volume: 65 Issue: 4 Pages: 655-662 Dixon B 2010 Translocation of four rare ironstone endemic species onto a premined area at Beenup in SW Australia In PS Soorae (ed), Global Re-introduction Perspectives: 2010.IUCN Additional case-
Conservation status
Breeding System
Habit
Translocation type
Method
Complete
Critically endangered: State level, Critically Endangered or Endangered: Federal level
Sexual and other (possible selfing)
Nonwoody plant perenni al
Introduction & Reinforcement
No
Yes
Sexual
Reintroduction
Yes
Yes
Endangered EPBC
Sexual
Nonwoody plant perenni al Woody plant longlived ≥ 10 years
Seedling transplant & Plants grown from cuttings as well as seed Seedling transplant
Seedling transplant
No
n/a
WA State, IRP 178 as Priority ? Endangered under
Sexual
Woody plant longlived ≥ 10 years
Reintroduction
Yes
No
Introduction
67
Group
Species
State
Leionema equestre
SA
Lepidium ginninderrense
ACT
Report/citation details studies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 301- 305. http://www.bgpa.wa.gov.au/science/biodiver sity-and-extensions/beenup-translocation Jusaitis M (2011). Trial translocations of Leionema equestre on Kangaroo Island, South Australia. In PS Soorae (ed), Global Re-introduction Perspectives: 2011.IUCN More case-studies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 210-214 1. ACT Conservation Planning and Research as unpublished reports.
2.
3
Conservation status Commonwealth EPBC Act
Breeding System
Habit
Translocation type
Method
Complete
Group
E (IUCN)
Sexual
Nonwoody plant perenni al
Introduction
Seedling transplant & Direct seeding
Yes
No
ACT and Commonwealth
Sexual
Nonwoody plant – perenni al
Reintroduction - but no populations there
Seedling transplant
No
As above
As above
Introduction
As above
As above
n/a
As above
As above
As above
As above
No
n/a
Woody plant longlived ≥ 10 years Woody plant long-
Reinforcement
Seedling transplant
No
Reinforcement
Adult transplant , Direct
No
State (E) and Commonwealth (V) Nationally threatened
Macadamia integrifolia
NSW QLD
http://www.tmr.qld.gov.au/~/media/Projects/ B/Beechmont%20Road%20Upgrade%20Lo wer%20Beechmont/beechmontroadupgrad ecompliancereport.pdf.
Vulnerable (EPBC, NCA)
Sexual
Macrozamia pauli-guilielmi
QLD
Translocation Performance Report for Macrozamia pauli-guilielmi and Acacia attenuata (Vegetation Matters 2013).
Endangered (Qld NCA, EPBC)
Sexual
n/a
68
Species
Marsdenia longiloba
State
NSW QLD
Report/citation details Qld Department of Transport and Main Roads; Opus; DSEWPAC; Qld Parks and Wildlife Service, Department of Environment and Heritage Protection 1.http://www.rms.nsw.gov.au/roadprojects/p rojects/pac_hwy/port_macquarie_coffs_har bour/nambucca_hds_to_urunga/project_do cuments/index.html (construction documentation)
Conservation status
NSW
Montia australasica
ACT NSW SA TAS VIC WA ACT
Muehlenbeckia tuggeranona
Unpublished ecological reports to the client, various government departments (inc. OEH) from ecological consultant. Consultants have given talks to various bodies (workshops, seminars, conferences)
1. ACT Conservation Planning and Research as unpublished reports
Habit
Translocation type
lived ≥ 10 years
NSW Endangered, Federal Vulnerable
Sexual
Endangered
Can be sexual &/or asexual
Yes
Can be sexual &/or asexual
No
Can be sexual &/or asexual
ACT and Commonwealth
Sexual also possibly asexual but not confirmed
2. Nambucca Shire Council
Melaleuca deanei
Breeding System
Method
Complete
Group
seeding, Seedling transplant
Nonwoody plant – perenni al As above
Introduction
Direct seeding
No
n/a
Other
Adult transplant
Yes
No
Woody plant longlived ≥ 10 years Nonwoody plant perenni al
Ecological replacement
Adult transplant
Yes
No
Reinforcement
Seedling transplant
No
Yes
Woody plant longlived ≥ 10 years
Reinforcement /Reintroductio n - but no populations there
Adult transplant
No
Introduction
As above
69
n/a
Species
State
Report/citation details
Conservation status State (E) and Commonwealth (E)
Breeding System Can be sexual &/or asexual
Habit
No
Sexual
Reinforcement
1. Internal reports for translocation approvals and monitoring reports. Overall reports to be published
critically endangered
Sexual
Nonwoody plant perenni al Woody plant longlived ≥ 10 years
2.
Endangered EPBC
As above
Criticlly endangered
Sexual
E (SA)
Sexual
2. Preliminary results unpublished, ACT Govt
Oreobolus pumilio
NSW TAS VIC
Persoonia micranthera
WA
Persoonia pauciflora
NSW
Phebalium glandulosum
NSW QLD SA VIC
1. Jusaitis M (1991). Endangered Phebalium (Rutaceae) species return to South Australia. Re-introduction News No. 3: 4. 2. Jusaitis M (1991). Micropropagation of endangered Phebalium (Rutaceae) species in South Australia. Botanic Gardens Micropropagation News 1: 43-45.
Translocation type
Complete
Group
Seedling transplant
No
Yes
Introduction
Seedling transplant
No
As above
As above
As above
No
n/a
Woody plant longlived ≥ 10 years Nonwoody plant perenni al
Not yet
Seedling transplant & Direct seeding
Yes
Yes
As above
Method Seedling transplant
Introduction
70
Species
State
Report/citation details
Conservation status
Breeding System
Habit
Translocation type
Method
Complete
Group
Yes
Sexual
Reinforcement
Seedling transplant
Yes
Yes
Critically endangered: EPBC Act and endangered: Victoria Yes
Sexual
Reinforcement
Adult transplant
Yes
No
Ecological replacement
Adult transplant
no
n/a
CE (IUCN)
Sexual
Nonwoody plant perenni al Woody plant longlived ≥ 10 years Nonwoody plant perenni al Woody plant long-
Reinforcement
Seedling transplant
Yes
Yes
3. Jusaitis M (1996). Experimental translocations of endangered Phebalium spp. (Rutaceae) in South Australia: An update. Re-introduction News No. 12: 7-8. 4. Jusaitis M (2000). The Ecology, Biology and Conservation of Threatened Phebalium Species in South Australia. Plant Biodiversity Centre, South Australia. 5. Jusaitis M (2011). Translocation of the desert Phebalium to Yookamurra Sanctuary, South Australia. In PS Soorae (ed), Global Re-introduction Perspectives: 2011. More case studies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 215-219 Pimelea spicata
ACT NSW
Pimelea spinescens ssp spinescens
VIC
Mueck, S. 2000. Translocation of Plains Rice-flower (Pimelea spinescens ssp. spinescens), Laverton, Victoria. Ecol. Man & Restor. 1(2): 111- 116.
Prasophyllum sp Wybong
NSW (not show n in ALA) SA
Annual monitoring reports & a paper for publication held by a mining company
Prostanthera eurybioides
Jusaitis M (2010). Enhancement of Monarto Mintbush populations in South Australia by translocations. In PS Soorae (ed), IUCN
Sexual
71
Species
State
Report/citation details
Conservation status
Breeding System
Psychrophyla introloba
NSW VIC
No
Can be sexual &/or asexual
Pterostylis arenicola
NSW SA VIC
E (SA)
Can be sexual &/or asexual
Pterostylis basaltica
VIC
Endangered EPBC, listed Vic.
Sexual
No
Sexual
Ranunculus gunnianus
Translocation type
Method
Complete
Group
Reinforcement
Seedling transplant
No
Yes
Introduction
Seedling transplant
No
Yes
Reintroduction
Seedling transplant
Yes
No
Reinforcement
Seedling transplant
No
Yes
Reinforcement
Seedling transplant
No
Yes
Reinforcement
Seedling transplant
No
Yes
lived ≥ 10 years
"Global Re-Introduction Perspectives: 2010. Additional case-studies from around the globe. IUCN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE, pp 306-310
Data unpublished and held with DEPI
Habit
Ranunculus millanii
ACT NSW VIC
No
Sexual
Ranunculus pimpinellifolius
ACT NSW TAS VIC
No
Sexual
Nonwoody plant perenni al Nonwoody plant perenni al Nonwoody plant perenni al Nonwoody plant perenni al Nonwoody plant perenni al Nonwoody plant -
72
Species
Rutidosis leptorrhynchoid es
State
ACT NSW VIC
Report/citation details
Conservation status
1. ACT Conservation Planning and Research as unpublished reports.
ACT and Commonwealth
2.
Nationally threatened
Breeding System
Sexual
Habit perenni al Woody plant longlived ≥ 10 years
Translocation type
Method
Complete
Group
Reintroduction - but no populations there
Direct seeding & Seedling transplant
Yes
Yes
n/a
As above
Nonwoody plant perenni al
Introduction
As above
No
Senna acclinis
NSW QLD
Stanwell Corporation Limited; Qld Parks and Wildlife Service, Department of Environment and Heritage Protection; Vegetation Matters
Rare (Qld Nature Conservation Act)
Sexual
Woody plant longlived ≥ 10 years
Reinforcement
Adult transplant , Direct seeding, Seedling transplant
Yes
Swainsona recta
ACT NSW VIC
1 .ACT Conservation Planning and Research as unpublished reports
ACT and Commonwealth
Sexual
Woody plant longlived ≥ 10 years
Reintroduction - but no populations there
Adult transplant
No
2. ANPC ?
TSC Act & EPBC – Endangered
As above
Nonwoody plant – perenni al
Reintroduction
Seedling transplant & Direct seeding
Yes
No
73
Species
State
Report/citation details
Conservation status
Breeding System
Habit
Translocation type
Method
Complete
Group
3 Preliminary results unpublished, ACTEW
Endangered (or threatened) under Commonwealth, NSW, ACT and Vic legislation
As above
As above
As above
Adult transplant
No
Will be
As above
As above
Introduction
Seedling transplant
No
n/a
WA State and Commonwealth as Critically Endangered
Sexual
Woody plant longlived ≥ 10 years
Reintroduction
Tissue culture
Yes
Yes
Endangered: State level, Critically
Can be sexual
Nonwoody plant -
Introduction
Tissue culture
No
4.
Symonanthus bancroftii
WA
Synaphea quarztitica
WA (not show
1. Bunn, E. and Dixon,B. (2008). Reintroduction of the endangered Bancroft’s Symonanthus in Western Australia. Page 224-228 in- Ed. Soorae,P.S. (October 2008) Global re-introduction perspectives: Re-introduction case studies from around the globe.ICUN/SSC Re-introduction Specialist Group, Abu Dhabi, UAE. 2. Qigang Ye, Eric Bunn, Siegfried L. Krauss, Kingsley W. Dixon 2007 Reproductive success in a reintroduced population of a critically endangered shrub, (Solanaceae) Australian Journal of Botany 55(4) 425–432. 3.http://www.bgpa.wa.gov.au/science/biodiv ersity-and-extensions/symonanthustranslocation Limited information available from Dept. Parks and Wildlife (WA)
State (E) and Commonwealth (E)
74
Species
State
Report/citation details
Conservation status Endangered or Endangered: Federal level Vulnerable NSW & Commonwealth
Breeding System &/or asexual
Habit
Can be sexual &/or asexual
2. Assessment reports submitted by EFS to Wyong Shire Council and the developer involved. Documents can be supplied if required
Yes
3. Great lakes Council
n in ALA) Tetratheca juncea
NSW
1. Wyong Shire Council, Donaldson Coal, Centennial Coal
Translocation type
Method
Complete
Nonwoody plant perenni al
Other experimental translocation from a development site
Adult transplant
No
As above
As above
Ecological replacement
As above
Yes
Vulnerable
As above
As above
Other
Bulk topsoil
No
Seedling transplant & Plants grown from cuttings as well as seed
No
Group
perenni al
Verticordia albida
WA
Limited information available from Dept. Parks and Wildlife (WA)
Critically endangered: State level, Critically Endangered or Endangered: Federal level
Sexual and other (possible selfing)
Woody plant longlived ≥ 10 years
Introduction
Verticordia lindleyi ssp lindley
WA
http://www.bgpa.wa.gov.au/science/biodiver sity-and-extensions/verticordiatranslocation
WA State as Priority 3.
Sexual
Reintroduction
Wilsonia backhousei
NSW SA
Sullivan M et al. Present to Ecological Soc in NZ
Yes
Sexual
Woody plant shortlived < 10 years Woody plant -
Reinforcement
Seedling transplant
No
Yes
Yes
Yes
Yes
75
Species
Xanthorrhoea glauca
Zieria prostrata
State TAS VIC WA ACT NSW QLD VIC NSW
Report/citation details
Conservation status
Breeding System
Abigroup (Lend Lease); North Burnett Regional Council; Qld Parks and Wildlife Service, Department of Environment and Heritage Protection; Vegetation Matters
Type ! restricted (Qld NCA)
Sexual
http://www.environment.nsw.gov.au/resourc es/nature/recoveryplanFinalZieriaProstrata. pdf
Endangered
Sexual
Habit longlived ≥ 10 years Woody plant longlived ≥ 10 years Woody plant longlived ≥ 10 years
Translocation type
Method
Complete
Group
Other Conservation translocation
Adult transplant
No
n/a
Reintroduction
Seedling transplant
Yes
No
,
76
Table 2. Details of published, “grey” or unpublished reports, websites or locations of reports that contain information on flora translocations, listed by groups Taxon Cooks River Castlereagh Ironbark Forest community
Cumberland Plain Woodland community
Orchids - various
Sydney Sandstone Ridgetop Woodland Various non-threatened Western Sydney species
Report/citation details Unpublished ecological reports to the client, various government departments (inc. OEH) from ecological consultant. Consultants have given talks to various bodies (workshops, seminars, conferences). Unpublished ecological reports to the client, various government departments (inc. OEH) from ecological consultant. Consultants have given talks to various bodies (workshops, seminars, conferences). Unpublished ecological reports to the client, various government departments (inc. OEH) from ecological consultant. Consultants have given talks to various bodies (workshops, seminars, conferences). http://www.dixonsand.com.au/environment_frame.htm (Annual Environmental Monitoring Reports) Unpublished ecological reports to the client, various government departments (inc. OEH) from ecological consultant. Consultants have given talks to various bodies (workshops, seminars, conferences).
General/other publications Cochrane, Anne; Monks, Leonie 2006 : Seedbanks and the conservation of threatened species In Eds: Sweedman, L; Merritt, AUSTRALIAN SEEDS: A GUIDE TO THEIR COLLECTION, IDENTIFICATION AND BIOLOGY Pages: 61-66 Dixon, B. (2005). Managing Phytophthora cinnamomi on a rare ironstone multitranslocation site in Western Australia. Australasian Plant Conservation vol. 13:4, 1819. Dixon B (2010) Controlling weeds on translocation sites, strategies, solutions and probable short term costs to the environment. Abstracts< Australian Network for Plant Conservation, 8th National Conference, Perth. Jusaitis M (2012). Serendipity during long-term monitoring of translocation trials. Australasian Plant Conservation 20(3): 8-10. Jusaitis M (1993). Conservation studies on four endangered plants from Kangaroo Island, South Australia. Final report. Black Hill Flora Centre, Botanic Gardens of Adelaide. Jusaitis M and B Sorensen (1994). Conservation studies on endangered plant species from South Australia's Agricultural regions. Black Hill Flora Centre, Botanic Gardens of Adelaide. Jusaitis M (1997). Experimental translocations: Implications for the recovery of endangered plants. In DH Touchell, KW Dixon, AS George and AT Wills (eds), Conservation into the 21st Century. Proceedings of the 4th International Botanic Gardens Conservation Congress, Perth, Western Australia. Kings Park and Botanic Garden, Western Australia, pp 181-196.
77
Jusaitis M and J Val (1997). Herbivore grazing: an important consideration in plant translocations. Re-introduction News No. 13: 11-12. Jusaitis M and J Val (1997). Success of plant translocations can be improved by optimising choice of propagule. Re-introduction News No. 13: 10-11. Jusaitis M (2005). Translocation trials confirm specific factors affecting the establishment of three endangered plant species. Ecological Management & Restoration 6: 61-67.
78
Appendix 2 Global case studies of experimental assisted colonisations
Case study 1: Wild Orchids in southwest China Liu H., Feng C.-L., Chen B.-S., Wang Z.-S., Xie X.-Q., Deng Z.-H., Wei X.-L., Liu S.Y., Zhang Z.-B. & Luo Y.-B. (2012) Overcoming extreme weather challenges: Successful but variable assisted colonization of wild orchids in southwestern China. Biological Conservation 150, 68-75.’
In southwestern China in 2006, 1000 endangered wild orchid plants were translocated to higher elevations to avoid inundation from human development. All of the species translocated were growing at 350 – 400 m above sea level and were translocated to ~ 1000 m above sea level. The largest elevation difference was approximately 3.6 °C cooler. Some of the species were translocated beyond their natural elevational range (i.e. only known to occur below 900m above sea level) whilst others are known to exist beyond 900 m above sea level. The study compared the impacts of multiple stressors (extreme cold spell, extreme drought, herbivory and initial translocation stress) of the out-of-range plants to the within range-species of 20 orchid species (462 individuals) for 5 years. Results from individual stressors: •
An extreme cold spell accounted for < 10% of total plant mortality. All of the mortalities were from the out-of-range species but due to large variances, this was not significantly different to the within-range species. The majority of the species that recorded mortalities are not found above 700 m, with one species (350 – 500 m) suffering 90% mortality due to cold stress.
•
No translocated plants died due to extreme drought conditions.
•
Less than 10% of total plants died due to translocation stress. Interestingly, more within-range species failed to acclimatize than out-of-range species but variation was high and the result was not statistically significant.
•
Herbivory from insects and mammals accounted for 21.6% of total plant mortality, causing higher mortality rates than the climate extremes (or transplantation stress). Mortality occurred in only three species, of which two were out-of-range species but difference between total individuals was not statistically significant between the two groups. 79
Overall, 60.4% of individual plants survived after five years. There was no survival difference between the within and out-of range species and the experiment was therefore considered an example of a successful assisted colonisation. All species flowered at least once one year after the translocation. No seedlings were observed within 0.5 m around the transplanted plants during the 2011 survey. The cost of project was 10 million RMB ($1.5m USD at the time of publication).
Case study 2: European forest herbs Van der Veken S., De Frenne P., Baeten L., Van Beek E., Verheyen K. & Hermy M. (2012) Experimental assessment of the survival and performance of forest herbs transplanted beyond their range limit. Basic and Applied Ecology 13, 10-9.
Four European herb species were transplanted in a northerly direction, beyond their known range to two transplant sites in Belgium. The minimum distance from the northern range edge of each species to the transplant site was different for each species: 50, 100, 200 and 500 km. After seven years, the species planted 50 and 200 km from their most northerly range edge had a high and intermediate success rate respectively. The success rate of species transplanted at 100 km was poor and no plants transplanted 500 km from their native range edge survived. The authors note that the poor results for two of the species are inconsistent with anecdotal evidence from European nurseries that sell many native species approximately 1000 km north of their current range edges. The inconsistency may be due to unqualified factors that could affect survivorship. For example, inappropriate seed origin and seed quality may contribute to low recruitment of the underperforming species. This experiment demonstrates that three of four species investigated can tolerate climate conditions outside of their native range and could be considered as candidates for assisted colonisation.
Case study 3: Seed germination beyond range limits in orchids Keel B. G., Zettler L. W. & Kaplin B. A. (2011) Seed germination of Habenaria repens (Orchidaceae) in situ beyond its range, and its potential for assisted migration imposed by climate change. Castanea 76, 43-54.
80
A 5.8°C increase in mean temperatures is expected over the next 50 – 100 years in the south east of the USA. Organisms with a requirement to stay within their current climatic envelope will need to shift 580 km north. Orchids are wind dispersed and considered to have good potential to range shift to stay within their climate envelope. However, orchids are thought to be particularly vulnerable to climate change because they are reliant on fungal associations. The aim of this study was to assess the ability of seeds from a southern provenance of a generalist orchid, Habenaria repens, to germinate in situ when buried at five sites at its northern limit and up to 850 km beyond its natural range. Seeds were buried without fungal inoculation and after five months the hyphal growth on the protocorms (leafless seedlings) was assessed. Only two of the five sites produced protocorms with active mycoflora (fungi). The authors conclude that it is possible for southern populations of H. repens to germinate up to 850 km beyond their natural range, provided active mycoflora is present.
Case study 4: Butterflies in the United Kingdom Willis S. G., Hill J. K., Thomas C. D., Roy D. B., Fox R., Blakeley D. S. & Huntley B. (2009) Assisted colonization in a changing climate: a test-study using two U.K. butterflies. Conservation Letters 2, 46-52. Two butterfly species that are naturally expanding northward in the UK, but whose migration will possibly be interrupted by barriers, were used as test cases of assisted colonisation. Species distribution models calibrated with three climate variables were used to predict the potential habitats of Melanargia galathea and Thymelicus sylvestris. As a result of the modeling, the two species were introduced 65 and 35km respectively north, beyond their known range. This experiment was deemed to be successful, both from the modeling approach and from species’ perspectives. After 6+ years, populations had established and expanded at a rate similar to other naturally-colonised sites of migrating butterflies. Furthermore, the pace at which the assisted migrants expanded their range was consistent with other naturally expanding butterfly species, < 1 km / year. However, the pace of their expansion is less than the current ~4.5 km / year northwards shift of the northern British isotherms. Therefore, the assisted migrants are not keeping pace with climate change and their introductions may need to be extended north to match or pre-empt changes in the suitable climate niche. 81
The use of assisted colonisation in the forestry industry The forest industry has a long history of moving tree species and genotypes within and beyond their natural range to increase productivity. More recently, many high latitude foresters, particularly in Canada, have planted tree species beyond their current range as a climate change adaptation strategy to offset the expected decrease in productivity (see Table 1 in main document).
Case study 5: Hardiness and growth in trembling aspen Schreiber S. G., Ding C., Hamann A., Hacke U. G., Thomas B. R. & Brouard J. S. (2013) Frost hardiness vs. growth performance in trembling aspen: an experimental test of assisted migration. Journal of Applied Ecology 50, 939-49.
In a ten-year reciprocal transplant experiment in western Canada, seeds of Populus tremuloides were collected from and planted at five sites within its natural range. In addition, seeds were collected from Minnesota and planted at the five sites. The maximum distance between seed sources was 2300 km from Minnesota (north-east USA) to north-east British Columbia (western Canada); a difference of 11° latitude and ~5°C cooler in mean annual temperature (based on the 1961-1990 period). There were pronounced increases in height and biomass of non-local provenance plants compared to local provenance plants when moved in the direction of cooler climates. Whilst there were clear regional differences in phenological traits associated with frost tolerance, after ten years, this did not translate into inferior survival or growth by the plants sourced from warmer locations. The reciprocal transplant also demonstrated that where the northern provenances were planted into southern regions, their performance was inferior to the local provenance. These results suggest that genotypes of Populus tremuloides from warmer, southern locations should be planted at sites in a north-westerly direction to cooler climates. The authors conclude that failure to move genotypes of Populus tremuloides to cooler climates will have negative consequences for the forestry industry. Forestry translocations have not always been successful. Translocations of Pinus pinasta from Spain/Portugal to France in the mid-1950s failed because the southern populations were maladjusted to the infrequent extreme frost events (Benito-Garzón et al. 2013). Consideration should be given to extreme weather 82
events, not only averages, and adherence to an adaptive management strategy is recommended (Benito-Garzón et al. 2013).
REFERENCES Benito-Garzón M., Ha-Duong M., Frascaria-Lacoste N. & Fernández-Manjarrés J. (2013) Habitat Restoration and Climate Change: Dealing with Climate Variability, Incomplete Data, and Management Decisions with Tree Translocations. Restoration Ecology, 21, 530-6.
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Appendix 3
Reviews of flora translocations Date(s) Up to 3/2009
Author Sheean et al., 2012
1985 - 2010
1Guerrant
8/2006 – 10/2009
2Dalrymple
1989 - 2009
Godefroid et al., 2011
Earlier than 2008
Menges, 2008
Jr, 2012
et al., 2012
Type(s) Reintroductions Supplementations Introductions (conservation) Reintroductions (20%) Augmentations (30%) Introductions: within range (32%) outside of range (8%) Reintroductions within and outside of historic range
Species 13 species
Location Australia and offshore islands
Method Peer-reviewed literature
107 taxa
Mostly USA and Australia
Projects entered into the web-based CPC International Reintroduction Registry (CPCIRR; Centre for Plant Conservation 2009; peer-reviewed and grey literature
Rare plants
Global: Europe USA Australia
Reintroductions Reinforcements Translocations Reintroductions Introductions Augmentations
94 plants
Global. Survey responses mostly European Global
UK botanical libraries; peer-reviewed and grey literature; direct contact with practitioners using IUCN Peer-reviewed literature and survey for unpublished work Review of the evaluation of translocations using peer-reviewed literature
General plant examples
84
1996 - 2005
Guerrant Jr & Kaye, 2007
Reintroductions
1985 - 1997
Morgan, 1999
Reintroduction
~1980 -1990s Hodder & Bullock, 1997
Translocations
10 rare or endangered plants 48 threatened and nonthreatened species Various plant species
Oregon USA
Projects the authors were involved in
Australia – western Victoria
Field assessment of 3 planting sites
United Kingdom
Examples of studies and proposed translocations in the UK 1Guerrant Jr The central message is that the empirical evidence we have about reintroductions, though substantial and growing, is limited and not necessarily representative of species, life forms, life histories, or geographic locations. 2 See
also: http://www.environmentalevidence.org/SR32.html
REFERENCES Dalrymple S. E., Banks E., Stewart G. B. & Pullin A. S. (2012) A Meta-Analysis of Threatened Plant Reintroductions from across the Globe. In: Plant reintroduction in a changing climate. Promises and perils (eds J. Maschinski and K. E. Haskins) pp. 31-50, Island Press, USA.
Godefroid S., Piazza C., Rossi G., Buord S., Stevens A. D., Aguraiuja R., Cowell C., Weekley C. W., Vogg G., Iriondo J. M., Johnson I., Dixon B., Gordon D., Magnanon S., Valentin B., Bjureke K., Koopman R., Vicens M., Virevaire M. & Vanderborght T. (2011) How successful are plant species reintroductions? Biological Conservation 144, 672-82.
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Guerrant Jr. E. O. (2012) Characterizing two decades of rare plant reintroductions. In: Plant reintroduction in a changing climate. Promises and perils (eds J. Maschinski and K. E. Haskins) pp. 9-29. Island Press, USA.
Guerrant Jr E. O. & Kaye T. N. (2007) Reintroduction of rare and endangered plants: common factors, questions and approaches. Australian Journal of Botany 55, 362-70.
Hodder K. H. & Bullock J. M. (1997) Translocations of Native Species in the UK: Implications for Biodiversity. Journal of Applied Ecology 34, 547-65.
Menges E. S. (2008) Restoration demography and genetics of plants: when is a translocation successful? Australian Journal of Botany 56, 187-96.
Morgan J. W. (1999) Have tubestock plantings successfully established populations of rare grassland species into reintroduction sites in western Victoria? Biological Conservation 89, 235-43.
Sheean V. A., Manning A. D. & Lindenmayer D. B. (2012) An assessment of scientific approaches towards species relocations in Australia. Austral Ecology 37, 204-15
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Appendix 4 Reviews of fauna translocations Date(s) Not specified
Author 1Williams et al., 2013
Type(s) Translocations
Species Birds
Location Global
Up to 3/2009
Sheean et al., 2012
Reintroductions Supplementations Introductions (conservation)
Australia and offshore islands
1991 2006 Up to 2008
Germano & Bishop, 2009 Short, 2009
1990 2005 1996 ~2003
Seddon et al., 2007 Possingham et al., 2004
Translocations (within natural range) Reintroductions (65%) Introductions (22%) Restocking (13%) Reintroductions
25 mammals; 9 birds; 3 amphibians; 1 fish; 1 invertebrate Amphibians and reptiles 102 Vertebrates
1979 1998
Fisher & Lindenmayer, 2000
Translocations
Relocations
Method www.conservationevidence.com. Conservation Evidence; database and systematic reviews collated by the Collaboration for Environmental Evidence; peer-reviewed literature Peer-reviewed literature
Global
Peer-reviewed literature
Australia
Emphasis on threatened sp. (EPBC Act) published & grey literature; pers. comms.
Animals
Global
15 mammal species, 3 bird species, and a few reptile species Animals
Western Australia
Report on general trends from peer-reviewed papers, Review of the Western Shield project:
Global
12 peer-reviewed journals
87
Not specified ~1980 1990s
Cade, 2000
Translocations
Raptors
Hodder & Bullock, 1997
Translocations
Vertebrates and invertebrates
1993
Wolfe et al., 1996
Translocations – intentional release
93 birds and mammals
Up to 1993 ~1970 1980 Pre 1960 to 1995
Cade & Temple, Not specified in 1995 abstract Meads, 1995 Translocations
1907 1993
Copley, 1995
1972 1980
Short et al., 1992
Not specified
Stanley Price, 1991
~1962 1990
Dodd & Seigel, 1991
Saunders, 1995
Endangered birds 4 threatened invertebrates Vertebrates
Not specified in abstract United Kingdom
USA & Canada (and possibly Aust & NZ) Not specified in abstract New Zealand
Translocations (establish, reestablish or augment) Translocations Native vertebrates (both within and outside of native range) Reintroductions 6 threatened wallabies (& a summary of other wallaby translocations) Reintroductions Mammals
New Zealand
Repatriation (within natural range)
Global
25 species of amphibians and reptiles
Report not sighted - cited in Godefroid et al 2011 Examples of studies and proposed translocations in the UK Survey of wildlife professionals
Review of 30 presentations at a Symposium Overview of 4 specific case studies Historical overview
South Australia
All documented attempts (presumably Government and some peer-reviewed journals)
Australia – WA & NSW
Reporting of case studies
Global
Report presented at Symposia of the Zoological Soc. London. Report not sighted – cited in Fischer et al 2000 Peer-reviewed and grey literature
88
1973 1986
Griffith et al., 1989
Translocations (outside natural range) Relocation (move from threat) Translocations – intentional release
93 birds and USA & Canada mammals of which (and possibly 90% were game Aust & NZ) species 1 Bird Synopsis: http://www.conservationevidence.com/collected-evidence/567
Survey of wildlife professionals
REFERENCES Cade T. J. & Temple S. A. (1995) Management of threatened bird species: evaluation of the hands-on approach. Ibis 137, 161-72. Cade, T. J. (2000). Progress in translocation of diurnal raptors. Raptors at Risk. WWGBP and Hancock House, Surrey, 343-372. Copely P. B. (1995) Translocations of native vertebrates in South Australia: a review. In: Reintroduction biology of Australian and New Zealand fauna (ed M. Serena). Surrey Beatty & Sons Pty Ltd, Chipping Norton, New South Wales. Dodd C. K., Jr. & Seigel R. A. (1991) Relocation, Repatriation, and Translocation of Amphibians and Reptiles: Are They Conservation Strategies That Work? Herpetologica 47, 336-50. Fischer J. & Lindenmayer D. B. (2000) An assessment of the published results of animal relocations. Biological Conservation 96, 111. Germano J. M. & Bishop P. J. (2009) Suitability of Amphibians and Reptiles for Translocation Aptitud de Anfibios y Reptiles para la Translocación. Conservation Biology 23, 7-15. Griffith B., Scott J. M., Carpenter J. W. & Reed C. (1989) Translocation as a Species Conservation Tool: Status and Strategy. Science 245, 477-80. 89
Hodder, K. H., & Bullock, J. M. (1997). Translocations of native species in the UK: implications for biodiversity. Journal of Applied Ecology, 547-565. Meads M. J. (1995) Translocation of New Zealand's endangered insects as a tool for conservation. In: Reintroduction biology of Australian and New Zealand fauna (ed M. Serena). Surrey Beatty & Sons Pty Ltd, Chipping Norton, New South Wales. Possingham H., Jarman P. & Kearns A. (2004) Independent review of Western Shield - February 2003. Conservation Science Western Australia 5, 2-11. Saunders A. (1995) Translocations in New Zealand: an overview. In: Reintroduction biology of Australian and New Zealand fauna (ed M. Serena). Surrey Beatty & Sons Pty Ltd, Chipping Norton, New South Wales. Seddon P. J., Armstrong D. P. & Maloney R. F. (2007) Developing the Science of Reintroduction Biology Desarrollando la Ciencia de Biología de la Reintroducción. Conservation Biology 21, 303-12. Sheean V. A., Manning A. D. & Lindenmayer D. B. (2012) An assessment of scientific approaches towards species relocations in Australia. Austral Ecology, 37, 204-15. Short J., Bradshaw S. D., Giles J., Prince R. I. T. & Wilson G. R. (1992) Reintroduction of macropods (Marsupialia: Macropodoidea) in Australia - A review. Biological Conservation 62, 189-204. Stanley Price, M. R. (1991). A review of mammal re-introductions, and the role of the Re-introduction Specialist Group of IUCN/SSC. In Beyond Captive Breeding: Re-introducing Endangered Mammals to the Wild. Symposium of the Zoological Society of London (Vol. 62, pp. 9-25). Williams D. R., Pople R. G., Showler D. A., Dicks L. V., Child M. F., zu Ermgassen E. K. H. J. & Sutherland W. J. (2012) Bird conservation: Global evidence for the effects of interventions, Exeter, Pelagic Publishing. Wolfe C. M., Griffith B., Reed C. & Temple S. A. (1996) Avian and Mammalian Translocations: Update and Reanalysis of 1987 Survey Data. Conservation Biology 10, 1142-54. 90
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