Characteristics of climate change refugia forAustralian biodiversity

APRIL E. RESIDE,1* JUSTIN A. WELBERGEN,1,2 BEN L. PHILLIPS,1,3

GRANT W. WARDELL-JOHNSON,4 GUNNAR KEPPEL,5 SIMON FERRIER,6

STEPHEN E. WILLIAMS1 AND JEREMY VANDERWAL1

1Centre for Tropical Biodiversity and Climate Change, James Cook University, Townsville, Qld 4811,Australia (Email: april.reside@gmail.com), 2Hawkesbury Institute for the Environment, UWSHawkesbury Campus, Hawkesbury, New SouthWales, 3Department of Zoology, University ofMelbourne, Melbourne, Victoria, 4Curtin Institute for Biodiversity and Climate, Curtin University,Perth, Western Australia, 5School of Natural and Built Environments and Barbara Hardy Institute,University of South Australia, Adelaide, South Australia, and 6CSIRO Ecosystem Sciences, ClimateAdaptation Flagship, Canberra, Australian Capital Territory, Australia

Abstract Identifying refugia is a critical component of effective conservation of biodiversity under anthro-pogenic climate change. However, despite a surge in conceptual and practical interest, identifying refugiaremains a significant challenge across diverse continental landscapes. We provide an overview of the key prop-erties of refugia that promote species’ persistence under climate change, including their capacity to (i) bufferspecies from climate change; (ii) sustain long-term population viability and evolutionary processes; (iii) minimizethe potential for deleterious species interactions, provided that the refugia are (iv) available and accessible tospecies under threat. Further, we classify refugia in terms of the environmental and biotic stressors that theyprovide protection from (i.e. thermal, hydric, cyclonic, pyric and biotic refugia), but ideally refugia shouldprovide protection from a multitude of stressors. Our systematic characterization of refugia facilitates the iden-tification of refugia in the Australian landscape. Challenges remain, however, specifically with respect to how toassess the quality of refugia at the level of individual species and whole species assemblages. It is essential thatthese challenges are overcome before refugia can live up to their acclaim as useful targets for conservation andmanagement in the context of climate change.

Key words: climate change, conservation, refugia, synergies, terrestrial biodiversity.

INTRODUCTION

Climate change and associated changes to sea level,fire regimes and extreme weather are expected tochallenge terrestrial biodiversity at all system levels,including species-level reductions in range size andabundance, exposing many taxa to an increased riskof extinction (e.g. Thomas et al. 2004; Jetz et al. 2007;Wardell-Johnson et al. 2011). Refugia are habitatsthat components of biodiversity retreat to, persist in,and can potentially expand from under changingclimatic conditions (Keppel et al. 2012; Keppel &Wardell-Johnson 2012). Therefore, refugia provideuseful targets for conservation and managementstrategies that aim to reduce the worst impacts ofanthropogenic climate change.

Refugia have facilitated the survival of speciesduring past climatic changes (Tzedakis et al. 2002;Carnaval et al. 2009). Interest in refugia has expandeddue to their potential to be safe havens for biota underprojected anthropogenic climate change (Noss 2001).We follow the terminology that distinguishes be-tween the Latin form ‘refugium’ and the Englishform ‘refuge’; where ‘refugia’ are areas large enoughto support populations of species under changingclimatic conditions, while ‘refuges’ shelter indivi-duals from short-term disturbances (Ashcroft 2010;Keppel et al. 2012; Keppel & Wardell-Johnson 2012)(Table 1). Thus refuges are those that provide protec-tion to individuals during their lifetime, while refugiaprovide protection to populations or species over eco-logical or evolutionary time scales. While refuges playan important role in species persistence, their discus-sion is beyond the scope of this review. Instead, wefocus on the role of refugia, and specifically their

*Corresponding author.Accepted for publication April 2014.

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ability to provide protection to biodiversity underanthropogenic climate change.

Increasing recognition of the importance of refugiafrom climate change has led to a surge in conceptualand practical interest to define properties of refugia,and how best to find them in the landscape (Ashcroft2010; Keppel et al. 2012; Keppel & Wardell-Johnson2012). Here, we review the key properties that enableclimate change refugia to be effective in promotingspecies’ persistence in the Australian context. Fur-ther, we classify refugia in terms of the environmentaland biotic stressors that they provide protection from,and highlight the challenges that need to be over-come before protection of refugia can be an effectiveconservation strategy.

ESSENTIAL PROPERTIES OF REFUGIA

Refugia will be important for species persistenceif they provide protection from climate change; safe-guard long-term population viability and evolutionaryprocesses; and minimize the potential for deleteriousspecies interactions. However, refugia can only providethese protections if they are available and accessible tospecies under threat.We discuss these essential refugialproperties in turn below.

Protecting species from the impactof climate change

Protecting species from the direct impacts of cli-mate change is arguably the most important attri-bute of contemporary refugia. These impacts includeincreased average temperature; changes in timingand quantity of precipitation (Whetton et al. 2005);increases in the frequency of extreme events including

heat waves, droughts and floods (BoM-CSIRO 2006;IPCC 2007); and changes in fire regimes (Bradstock2010). The Australia-wide climate change predictionssuggest there will be an increase in annual mean tem-perature of 0.5–5.1°C by 2080 (Reside et al. 2012).Precipitation predictions vary from severe decreasesto substantial increases depending on the general cir-culation model used; however, mean predictions showincreased precipitation in the central tropical northand south-east coast and decreased precipitation overmost of the rest of the continent (Whetton et al. 2005).Therefore, refugia for Australian species need toprotect from varying combinations of heat, changes toprecipitation, and the flow on effects such as droughtand floods.

Climate change will also affect fire regimes, but dueto the complex interactions between fire, rainfall, tem-perature, wind, vegetation, carbon dioxide enrichmentand land management, predicting future fire has manyuncertainties. Overall though, there is a predictedincrease in fire frequency across Australia (Williamset al. 2001; Cary 2002; Krawchuk et al. 2009), butwith decreases in fire frequency in some areas as aresult of predicted dryness of woodland communities(Bradstock 2010). Species differ in their requirementswith regards to fire; therefore, refugia for some speciesmight be an absence of fire, or maintenance of thepreferred fire regime (Roques et al. 2001; Andersenet al. 2005). Refugia may play a role in protectingspecies from climate change by being buffered bybiotic or physically properties, therefore maintainingclimates that are more similar to present than thefuture regional climate. In some cases the bufferingfrom regional climate may occur in a uniform way,for example refugia may always be 3oC cooler thanthe regional temperature. Importantly, refugia mightbuffer the regional climate in a non-uniform way, sothat extreme climatic events are mitigated within the

Table 1. Definitions of refugia gleaned from the literature

Term Definition Reference

Refuge Shelter individuals from disturbances, e.g. predationor competition

Berryman and Hawkins (2006)Ashcroft (2010)Keppel et al. (2012)

Refugia Areas large enough to support populations of species,over ecological and evolutionary time scales of millennia

Ashcroft (2010)Keppel et al. (2012)

Micro refugia Small areas with local favourable environmental featureswhere small populations can survive outside their maindistributional area

Rull (2009)

Macro refugia Refugia where the general climate of the region is suitablefor the species

Mosblech et al. (2011)

In situ refugia Within the species current range Ashcroft (2010), Keppel et al. (2012)Ex situ refugia Outside the species current range Ashcroft (2010), Keppel et al. (2012)Cryptic refugia Refugia at different latitudes or longitudes than normally

expectedRull (2010), Stewart et al. (2010)

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refugia. Non-uniform buffering is likely to be crucialfor many species, as extreme climatic events can havelarge consequences for populations (Welbergen et al.2008; Saunders et al. 2011; Scheffers et al. 2014).If species are buffered non-uniformly from extremeevents, they may have a greater chance of adapting tolong term changes in average climatic conditions.

Safeguarding long-term population viabilityand evolutionary processes

The properties required by refugia to safeguard evo-lutionary processes are akin to the principles of reservesystem design: refugia need to be large enough tosustain populations without erosion of genetic diver-sity (Ovaskainen 2002), and networks should capturea sufficient range of habitats and areas that enableswithin species genetic diversity to be maintained.This would enable the maintenance of longer-termevolutionary processes, such as speciation and lineagesorting.

The size of an effective refugium will be species-specific. Small body size, capacity for asexual re-production (clonal growth or parthenogenesis) andlow genetic loads favour survival in small refugia(Mosblech et al. 2011). Thus, if an area acts as arefugium for larger, sexual species (such as verte-brates), then it will also likely be of sufficient size forthe more numerous smaller species that use the samehabitat (Simberloff 1998).Therefore, a focus on iden-tifying refugia for vertebrates is likely to capture areasthat will act as refugia for invertebrates and manyplants (subject to proximity constraints, see below).Minimum refugium size will also depend on site-basedfactors such as latitude, productivity and environ-mental heterogeneity. However, overall larger refugia,and networks of refugia, have a higher likelihoodof maintaining viable populations of many species(Ovaskainen 2002).

Minimizing deleterious species interactions

Invasive species are a significant threat to biodiversity(Lodge 1993), and it is likely that this threat willincrease under climate change (Brook 2008). Invasivespecies impact on biodiversity in a variety of ways:preying on native mammals (Johnson et al. 2007),competing with native herbivores for scarce resources(Morton 1990), changing fire regimes (Setterfieldet al. 2010) or altering microclimatic properties(Valentine 2006). Novel species assemblages and eco-systems are likely to result from changing climates(Williams & Jackson 2007). Land managers will facesignificant challenges when balancing the need to

facilitate the required range shifts of native specieswhile minimizing adverse interactions from shiftinginvasive species.

Availability and accessibility of refugia

A critical attribute of a refugium is its availability. Is itclose enough for a given species to make use of? Is therefugium in situ (within a species’ range) or ex situ(outside the species’ range)? In situ refugia providebetter prospects for species persistence because fewerrange shifts are required.The ability of species to reachex situ refugia, on the other hand, will depend on thedistance from the current species range, the dispersalability of the species, the conditions in the interveninghabitat (i.e. can individuals survive and reproduce),and whether there are any physical barriers to dispersal(e.g. rivers, mountain ranges).

Landscape position and structure influence refugialavailability. High topographic variability can reducethe distance a species is required to move to track itsclimatic envelope, and therefore provide effectiverefugia (Tzedakis et al. 2002). However, the reverse istrue for species already confined to mountain tops; inwhich case the nearest refugia may be at higher lati-tudes with intervening lowlands creating a dispersalbarrier (Laurance et al. 2011). In some cases, themuted topography of old or ancient landscapes maymask profound barriers to dispersal over short dis-tances (Mucina & Wardell-Johnson 2011). Addition-ally, there is a latitudinal gradient in dispersal abilityfor some taxa, with tropical species physiologically andbehaviourally less suited to dispersal than their tem-perate counterparts (Salisbury et al. 2012).

Connectivity of habitats throughout the landscapewill facilitate species’ movement to ex situ refugia,especially as the spatial locations of refugia themselvesmay shift. Connectivity will also allow species to tracktheir climatic niche more generally. Where landscapecontexts prevent species from reaching ex situ refugia,such as for mountain top endemics or other isolatedhabitats, active conservation measures such as assistedcolonization may be required (Hoegh-Guldberg et al.2008).

So, what is the ideal climate change refugium?

Identifying refugia requires defining what it is we aretrying to find. Ideally, climate change refugia are areaswhere the current climatic conditions will be best con-served into the future. Evidence for this can be foundfrom phylogeographic studies: climatic stability hasbeen an important component of long-term refugia(Tzedakis et al. 2002; Carnaval et al. 2009), particu-larly for species with low dispersal abilities (Graham

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et al. 2006). Where the current conditions cannotbe retained in situ, ideal refugia may be where spe-cies need to move the least geographical distance inorder to maintain suitable conditions; for examplesteep elevational gradients can have steep temperaturegradients. Functionally, however, the refugia needingto be identified are the areas likely to harbour the mostbiodiversity, or the areas that facilitate the persi-stence of the most vulnerable taxa. Factors likely tomeet these ends include environmentally stable, largeenough to allow population persistence and maintainevolutionary process, and accessible from the species’current range.

TYPES OF REFUGIA

Climate change refugia differ in terms of the environ-mental and biotic stressors that they provide protec-tion from: i.e. refugia from thermal, hydric, cyclonic,

pyric and biotic stressors. This classification is impor-tant as it facilitates the identification of refugia in thelandscape.

Climatic refugia

Thermal refugia

Thermal refugia are areas that are thermally stableover time. Specifically, they are areas in which regionaltemperatures are moderated by local topographic,vegetative and orographic factors (Fig. 1). This localthermal buffering can dampen daily fluctuations,lessen the impacts of extreme temperatures such asregional heat waves and cold snaps, and moderate thegeneral long-term increases in temperatures fromclimate change, resulting in overall greater thermalstability. However, in some cases, areas with thecoolest temperatures are different from the areas with

Fig. 1. Rugged areas can offer multiple refugial properties. An example of the thermal gradient of a daily maximumtemperature in a mountainous region, the AustralianWetTropics (AWT) in north-east Queensland (high temperatures indicatedby warmer colours on the continental and regional maps).This rugged area provides thermal, hydric and pyric refugial propertiesat both local and continental scales. The upland areas are cooler than their surrounds, and generate substantial orographicrainfall; this in turn promotes the growth of rainforest communities and the suppression of fire. Additional refugial properties aregenerated by steep gullies (which may protect against cyclonic events and strengthen the hydric refugial properties of the region).Data shown are at a 250-m resolution, adapted from Storlie et al. (2013).

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greatest stability, because the cold air drainage thatleads to cooler temperatures also causes more climatevariability (Ashcroft et al. 2012).

A range of factors influence the temperature thatorganisms experience. Elevation is a major factor inspatial heterogeneity of temperature through theprocess of adiabatic cooling, and therefore manycurrent and predicted future thermal refugia are asso-ciated with heterogeneous terrain and, in particular,mountains. Mountain tops currently provide refugiafor cool-adapted species in tropical areas, such asmicrohylid frogs (Shoo & Williams 2004), and rainfor-est endemic birds and mammals (Shoo et al. 2011).Slope and aspect also have substantial effects on tem-perature, reflected by varying plant communities ondifferent aspects at similar elevations.Terrain positionsthat promote cold-air pooling, convergent environ-ments such as valleys, local depressions and basins, areimportant refugia for temperature-sensitive species(Dobrowski 2011).

High temperatures can also be mediated by struc-tures that minimize direct radiation on large scalessuch as shading by mountains and gorges, and onsmall scales with individual rocks (Shoo et al. 2010)(Table 2). High shading can occur in valleys, depend-ing on the depth, width, and orientation of the valley;which influence the amount and timing of insola-tion and the amount of boundary layer mixing due

to wind (Colette et al. 2003; Whiteman et al. 2004).Other factors such as foliage cover, clouds, proximityto streams and sea breezes can also act to reducemaximum temperatures (Shoo et al. 2011). Exposureto wind can have a varied impact on temperaturesexperienced by species: offshore and polar windsmoderate high temperatures (van der Molen et al.2006), while wind coming from lower latitudes or frominland areas can have a warming effect (Ashcroft et al.2009).

Where species have insufficient mobility to tracklong-distance shifts in their climatic niche, environ-ments with pronounced thermal heterogeneity makecool refugia more accessible. Mountain tops mayprovide refugia for species currently at mid-elevations.Other species may retreat to gorges and other conver-gent environments. Recent shifts to higher elevationsby some species correlate with changing climate inrecent decades (Parmesan & Yohe 2003).

Hydric refugia

Hydric refugia occur where water availability isgreater, or is more consistent, than in the surroundinglandscape (Wardell-Johnson & Horwitz 2000). Hydricrefugia are particularly important in the Australiancontext, as water is the major limiting factor in many

Table 2. Synergies of multiple refugia properties afforded by key landscape features

Feature Type of refugial properties Process

Mountains Thermal Adiabatic coolingAspect shading reducing radiationKatabatic cooling (cold air pooling)

Hydric Orographic precipitationAspect shading reducing evaporationProtection from flood

Cyclonic refugia Physical barrier from windPyric refugia Physical barrier from firePrevent invasives Dispersal barrierPrevent pathogens Cooler temperatures

Rocks and gorges Thermal Shading reducing radiationBuffering

Hydric Shading reducing evaporationWater accumulation from runoff

Cyclonic refugia Physical barrier from windPyric refugia Physical barrier from fire

Reduced or breaks in fuel loadPrevent invasives Dispersal barrier

Riparian zones Thermal Shading by riparian vegetationHydric Greater surface and subterranean water availability

Islands Prevent invasives Water body as a physical barrier to dispersalThermal Ocean stabilizes temperatureHydric Orographic rainfall on high islands

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Australian landscapes. Just as topographic heterogene-ity is important for providing thermal refugia, topo-graphy is also a major factor in providing hydricrefugia across many scales. Mountains themselves areoften sources of hydric refugia due to orographic pre-cipitation (Tzedakis et al. 2002). Convergent environ-ments (e.g. valley bottoms, local depressions, coves,sinks, basins) also accumulate water and soil, and theaccumulated soil helps retain water (Dobrowski2011). Even on very small scales (0.2–3 m), topo-graphic and topo-edaphic heterogeneity facilitate sur-vival and population recovery (Godfree et al. 2011).Additionally, slope and aspect have a pronouncedeffect on water balance, as differences in insolation andwind exposure as a result of slope and aspect influenceevapotranspiration (McVicar et al. 2007; Dobrowski2011). The importance of shelter often depends onwind direction: in particular, winds coming frominland or the north can have a desiccating effect(Ashcroft et al. 2009).

Greater water availability can be provided by drain-age areas such as riparian areas and basins. Riparianareas across Australia support ecological and evolu-tionary processes that maintain a large variety andabundance of wildlife in an otherwise largely water-limited environment (Soderquist & Mac Nally 2000;Woinarski et al. 2000). Connected waterways andassociated riparian areas facilitate processes such asthe redistribution of nutrients, evolution, and move-ment of wildlife (Klein et al. 2009). The higher mois-ture and nutrient levels of riparian areas result inmore diverse plant communities and increased struc-tural complexity (Croonquist & Brooks 1991). Thesefactors all contribute to higher abundances and diver-sity of vertebrates in riparian areas (Monadjem &Reside 2008).

Rocky outcrops are known refugia for many speciesin Australia due to higher water availability around therocky area when compared with the surrounding land-scape (Couper & Hoskin 2008). Runoff from rockyescarpments, water absorption by large rock forma-tions, and the presence of aquifers in rock all resultin greater water availability close to rock escarpments(Freeland et al. 1988). Many species rely on themicroenvironment provided by rocky areas (Woinarskiet al. 2006). In particular, rocky habitats providerefuges for mammals occurring in the savanna duringlow groundwater periods (Braithwaite & Muller1997).

Hydric refugia also include areas protected fromextreme precipitation. Projections for future precipita-tion in some areas include a greater concentration intoa shorter, more intense wet season followed by anextensive, severe dry season (Hughes 2003). Extremeprecipitation can lead to decreased long-term wateravailability through greater run off; which in turn canresult in erosion. Extreme precipitation can also result

in extensive flooding. Such refugia include areas ofstable precipitation, with lower extremes of seasonalprecipitation, and elevated areas.

Cyclonic refugia

The mean and maximum intensities of tropical cy-clones are projected to increase as a result of climatechange (Walsh & Ryan 2000). Tropical cyclones canhave substantial impacts on biodiversity, even whereother threats are controlled, by damaging large tractsof vegetation, opening up a forest to heat, light, fire andinvasive species (Laurance & Curran 2008). Ecosys-tems respond differently depending on species com-position and forest structure (Cook & Goyens 2008;Turton 2012), as tree species vary in their susceptibil-ity to cyclones (Curran et al. 2008; Keppel et al.2010). Additionally, tropical cyclones bring extremeprecipitation. Greater landscape resilience can bufferareas from cyclones, as fragmented and small remnantforests are more susceptible to cyclone impact due totheir high forest edge to area ratios (Laurance &Curran 2008; Turton 2012). Cyclone impact varieswith site exposure and local topography such as wind-ward exposure and topographic shading (Boose et al.1994; Metcalfe et al. 2008). However, the shelteringbenefits may be outweighed by extremely strongcyclonic winds and down-draughts (Catterall et al.2008). Generally, the highest elevation montane rain-forests are more resistant than lowland rainforests tocyclones due to their lower vegetation stature andaerodynamically smooth canopies (Boose et al. 1994;Turton 2012). However, at a local scale elevated areasare more exposed and thus more vulnerable (Laurance& Curran 2008). Overall, intact high elevation foreston mountains sheltered from direct wind are the mostlikely to provide refugia from cyclones; however, morework is required to identify cyclone refugia.

Pyric refugia

Climate change is likely to result in changes in thefrequency and intensity of fire (Williams et al. 2001;Cary 2002; Krawchuk et al. 2009). Refugia from firecan include areas where fire occurs at the requiredinterval, season and extent; or an area where fire isexcluded altogether. Many Australian species havetraits strongly linked to particular fire regimes, andrequire particular fire regimes in order to persist(Bond et al. 2005). Changing fire regimes have beendetrimental to many species; this has been shown inAustralian tropical savannas where fire regimes haveshifted from small-scale early dry-season burns toextensive late dry-season fires (Williams et al. 2002).The late dry-season fires burn at a greater intensity

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and have a homogenizing effect on the landscape byremoving the unburnt patches (Bradstock et al. 2005).Refugia in this case are areas where fire regimes thatoptimize biodiversity are maintained.

In contrast, some species can only persist in theabsence of any fire.Topographic complexity, and infla-mmable substrates such as rock and wet vegetation,can provide barriers to fire.These barriers break up thefire landscape and can lead to a greater range of firehistories per unit area (Wood et al. 2011).Topographyinteracts with fire weather and the direction andspread of fire movement to influence the fire regime(Lee et al. 2009).The effect of aspect on the likelihoodof fire can depend on the direction of the prevailingwinds (Wood et al. 2011). Slope angle can alter theprobability of fire, with steeper slopes reducing thelikelihood that fire will reach the vegetation canopy(Bradstock et al. 2010).Therefore, refugia from all fireare mostly found in rocky areas and gorges, such as thedeep gorges that have protected the recently discov-ered Wollemi Pine (Wollemia nobilis) (Offord et al.1999). Many fire-sensitive plants and communitiescurrently persist in areas that are protected from fireby physical barriers and topography (Lindenmayeret al. 2000), or where the vegetation remains insuffi-ciently dry to burn (Wood et al. 2011).

Biotic refugia

Climate change will drive distributional shifts for manyspecies (Taberlet & Cheddadi 2002), therefore chang-ing species interactions, as already observed (Visser &Holleman 2001; Winder & Schindler 2004). In somecases, effective refugia will be areas where speciesturnover is low, such that deleterious interactions frominvasive or new competitor species are minimized(Iwamura et al. 2010). However, evidence from thepast demonstrates that dynamic species compositionsare common; therefore, the relative importance ofselecting refugia based on minimizing species turnoveris dependent on the species targeted for protection(Moritz & Agudo 2013).

Refugia from invasive species will be crucial forpersistence of some species under climate change. Iso-lated areas such as islands can act as refugia frominvasive species where access is restricted, such hasbeen shown for native mammals (Short & Turner1993). When invasive species do threaten nativespecies on islands, control and eradication of theinvasives is often more feasible than on larger landmasses (Szabo et al. 2012).

Areas removed from water also serve as refugia fromnegative biotic interactions for many arid-adaptedspecies. Artificial water sources have been establishedacross Australia for stock grazing, which lead to zonesof extreme degradation and decreases in palatable

native perennial grasses (James et al. 1999). Thesechanges are implicated in the decline and extinction ofmedium-sized native mammals and ground-dwellingbirds. Artificial and natural water bodies also facilitatethe spread and persistence of cane toads (Floranceet al. 2011), and decommissioning artificial waterbodies may be the best defence against cane toadsdispersing down the west coast of Australia (Tingleyet al. 2013).

Climate change is also likely to alter the pathogenprevalence, particularly where pathogens are limitedby climate. The geographic spread of vector-bornediseases is predicted to expand under rising globaltemperatures (Patz & Reisen 2001). High eleva-tion bird populations may be faced with greaterlevels of blood parasites, as high temperatures facili-tate the development and transmission of haematozoa(Zamora-Vilchis et al. 2012). Hotter temperaturesoccurring during periods of high soil moisture willintensify the effects of soil borne pathogens suchas Phytophthora cinnamomi (Shearer et al. 2004).In contrast, hotter temperatures are likely to limitthe prevalence of the amphibian chytrid fungus Batra-chochytrium dendrobatidis, which is responsible foramphibian declines across the globe (Puschendorfet al. 2009). However, for many species vulnerable topathogens it will be important to protect cool uplandareas as refugia from pathogens.

Synergies

Many locations can provide refugia from more thanone climate change-related threat (Table 2). In par-ticular, the synergies between thermal, hydric and fireprocesses mean that refugia will often protect speciesfrom changes in these processes simultaneously. Areasof hydric refugia (e.g. streams, riparian zones) areoften cooler (Dobrowski 2011) and less fire-pronethan the surrounds as a result of riparian vegetationsupported by the available water (Woinarski et al.2000). Areas protected from direct radiation have lessevaporation and often less flammable material, provid-ing thermal, hydric and fire refugia (Couper & Hoskin2008). Mountains and rocky gorges provide thermal,mesic and fire refugia through physical barriers toradiation and fire; also water accumulation and subse-quently less-flammable vegetation (Fig. 1). Mountainsalso provide refugia from cyclones through protectionfrom wind.

Identifying refugia that can protect against mul-tiple threats will be essential for the persistence ofbiodiversity. It is increasingly recognized that species’extinction risk is driven by a suite of processes, includ-ing climate change, overharvesting, land modificationand invasive species, and the synergistic interactionsbetween these processes can substantially increase

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this risk (Brook et al. 2008). Effective refugia pro-vide buffers against climate change in addition toother threatening processes, particularly habitat modi-fication. Increasing the resilience of the landscape islikely to enhance the potential for that landscape toact as a refugium from multiple threats. For example,intact forest vegetation is likely to provide thermal,biotic and cyclone refugia. The size of intact areas iscrucial to the ability of the area to maintain theirrefugial properties. Additionally, large refugial areasare required to support long-term viable populations;large population sizes reduce the probability of extinc-tion of species from climate change and all otherthreats (Brook et al. 2008).

CHALLENGES

Identifying refugia

The challenge that remains is how to identify refugiaacross the landscape effectively. Species have differingclimatic and biotic requirements, and thus what is anideal climate change refugia will depend on the speciesin question. A first step to identifying refugia for bio-diversity across Australia is to locate the areas whichshow the most environmental stability along axes oftemperature, water, extreme events, and negativebiotic interactions (Mackey et al. 2012). Where tem-perature and rainfall stability is high, stability of fireregime and biotic interactions are also likely to behigh. Challenges also remain in identifying the beststability metric, and in particular the most importanttime frame over which to measure stability (Ashcroftet al. 2012). A combination of climate stabilitymetrics, and biotically scaled metrics is likely to be thebest approach for identifying crucial refugia areas.Studies have used species distribution modelling toidentify future locations of climatic suitability to iden-tify areas of high future species richness (James et al.2013; Reside et al. 2013; Warren et al. 2013). Impor-tantly, some work has been done to identify the impor-tant areas for species current and future distributions,and the minimum-dispersal corridors between the two(Williams et al. 2005).

Assessing the effectiveness andquality of refugia

A final challenge is to rank refugia in terms of theirquality and effectiveness in protecting biodiversityunder climate change (Keppel & Wardell-Johnson2012). Measures of effectiveness can be drawn fromthe conservation planning literature, for example,representation and persistence (Margules & Pressey

2000). Representation refers to how well each speciesis represented within identified refugia, and persis-tence is the likelihood of an area maintaining refugialvalues in the long term.The quality or effectiveness ofa refugium can be further ranked by its irreplaceabil-ity: how crucial an area is to protect species threatenedby climate change (Margules & Pressey 2000). Suchranking would enable conservation and managementagencies to prioritize their investments and so protectbiodiversity from the worst impacts of climate changemore efficiently.

CONCLUSIONS

Natural systems are under threat from unprece-dented planetary engineering by human activities(Brook et al. 2008), resulting in decreased resilienceto rapid climate change (Millennium EcosystemAssessment 2005). Identifying and protecting refugiain the landscape to shield species from all aspects ofclimate change are crucial steps to conservation. Ourreview has identified the properties of refugia that aremost important for species’ persistence, and has clas-sified refugia in terms of the stressors that they provideprotection from. Effective refugia will be those thatprotect biodiversity from multiple climate change-related stressors, in addition to non-climatic threaten-ing processes. More research is required into specificaspects of identifying individual refugia in the land-scape, linking refugia to species, and prioritizing theserefugia for protection.

ACKNOWLEDGEMENTS

This work was funded by the National ClimateChange Adaptation Research Facility (NCCARF).J.A.W. was supported, in part, by ARC DiscoveryGrant DP110104186.

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