Understanding the drivers of Southeast Asian biodiversity loss · 2017. 7. 5. · cover between 1973 and 2009 (WWF Greater Mekong 2013); however, Lao PDR lost 5.29% of forest, Cambodia

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UnderstandingthedriversofSoutheastAsianbiodiversityloss

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SYNTHESIS amp INTEGRATION

Understanding the drivers of Southeast Asian biodiversity lossALICE C HUGHES

Xishuangbanna Tropical Botanical Garden Chinese Academy of Sciences Menglun Jinghong 666303 China

Citation Hughes A C 2017 Understanding the drivers of Southeast Asian biodiversity loss Ecosphere 8(1)e01624 101002ecs21624

Abstract Southeast Asia (SE Asia) is a known global hotspot of biodiversity and endemism yet theregion is also one of the most biotically threatened Ecosystems across the region are threatened by anarray of drivers each of which increases the probability of extinction of species in a variety of ecosystemsThese issues are symptomatic of the issues that face the global tropics however with around 4 billion peo-ple in the wider region and the associated pressures on biodiversity this region may be under some of thegreatest levels of biotic threat Deforestation rates in SE Asia are some of the highest globally additionallySoutheast Asia has the highest rate of mining in the tropics the around the greatest number of hydropowerdams under construction and a consumption of species for traditional medicines which is a threat to biodi-versity globally In this review the greatest threats to regional biodiversity in the SE Asian region are dis-cussed Tree-plantations and deforestation represents one of the most imminent threats and somecountries have already lost over half their original forest cover (ie the Philippines parts of Indonesia)with projections of as much as 98 loss for some regions in the coming decade Hunting and trade repre-sents a significant threat as demand stems not only for food but also for medicine for ornamentation andas a status symbol Mining represents a frequently overlooked threat as the Asian region is one of thegreatest exporters of limestone and various minerals globally and the cost of this to biodiversity is not onlythrough the direct loss of areas for mines but also through the development of roads that further fragmentthe landscape the leakage of heavy metals and the destruction of limestone karsts which represent globalendemicity hotspots Reservoir construction wetland drainage fires pollution invasive species diseaseand finally climate change are also considered Once each issue has been discussed the overall prognosisof regional biodiversity and priority actions to protect SE Asian biodiversity in the future is discussed

Key words climate change deforestation disease fire invasive species mining pollution reservoir constructiontrade wetland drainage

Received 25 July 2016 accepted 1 November 2016 Corresponding Editor Debra P C PetersCopyright copy 2017 Hughes This is an open access article under the terms of the Creative Commons Attribution Licensewhich permits use distribution and reproduction in any medium provided the original work is properly cited E-mail achughesxtbgaccn

INTRODUCTION

Southeast Asia (SE Asia) is a known hotspot ofbiodiversity and is of threat The region isuniquely biologically complex reflecting its com-plex biogeography and resulting in zonation ofregional biotic patterns and complex biogeo-graphic divides which require further research tofully understand (Sheldon et al 2015) Typically

when people consider SE Asian biodiversity theythink of the major biogeographic units it is madeof including Sundaland Wallacea Indochinaand the Philippines all of which are individuallyconsidered as some of the most diverse regions ofthe planet (Myers et al 2000)IUCN data (httpwwwiucnredlistorg) at a

country level show that if mammals birds andamphibians are analyzed at a family level SE

wwwesajournalsorg 1 January 2017 Volume 8(1) Article e01624

Asian countries have the highest global diversityfor a number of taxa However the level of taxo-nomic uncertainty associated with many taxamay be significantly higher than other parts of theworld with only a small proportion of many largetaxa described (ie 50 of bats Francis et al2010) and this lack of knowledge makes regionalprioritization challenging This taxonomic uncer-tainty and rapid rate of species descriptionextends across taxa with over 2216 describedbetween 1997 and 2014 (ie see WWF-GreaterMekong 2008 2009 2010 2011 2012 2013 2014)and consequently many species in the region maybe driven to extinction while still undescribed

The region is also said to be the most biologi-cally threatened globally (Schipper et al 2008)especially for certain taxonomic groups such asmammals (Duckworth et al 2012) These threatsare however complex and yet must be under-stood in order to develop coherent and effectiveconservation plans for the region In this reviewthese threats and their drivers are dissected anddiscussed to understand the real threats to biodi-versity on a regional and local level to nestle thiswithin the global context and to compare the dif-ferences and similarities of the threats faced bySE Asian diversity and those faced in tropicalregions in other parts of the planet

In the next section the greatest threats to SEAsian biodiversity are discussed in order of thoselikely to have the greatest impact in the widestselection of species on terrestrial (and in somecases freshwater) diversity Obviously many ofthese threats act in synergism and the outlook forany species or habitat reflects the complex inter-action of a number of these issues

ISSUES

Deforestation and tree plantationsOverview of regional changemdashSE Asia has some

of the highest deforestation rates in the worldwith estimates of around 145 of regional forestcover lost in the last 15 years and an average rateof 1 loss annually (Miettinen et al 2011) This isa conservative estimate as many of the estimateshave difficulty in disentangling forest from tree-plantations and even definitions of ldquoforestrdquo meanthat different measures are often not comparableNevertheless of the 73 of land covered by forestin 1973 only 51 existed by 2009 In countries

such as the Philippines deforestation has alreadyremoved 93 of the original forest cover a tra-gedy in one of the two regions considered both aglobal biodiversity hotspot and a megadiversitycountry (Myers et al 2000 Brooks et al 2006)Global analysis claimed that SE Asian protectedareas were performing comparatively well rela-tive to other parts of the world in terms of protect-ing forests (Heino et al 2015) However on closerscrutiny protected areas only perform 15 betterthan forest outside protected areas in terms ofpreventing deforestation and in a number ofcountries (ie the Philippines) protected areasactually have higher rates of deforestation thanunprotected areas (314 vs 286) and themajority of countries show under 1 differencebetween the two (Heino et al 2015)Most countries within Asia (Thailand Vietnam

Myanmar) lost between 2 and 4 of their forestcover between 1973 and 2009 (WWF GreaterMekong 2013) however Lao PDR lost 529 offorest Cambodia 697 Indonesia 843 andMalaysia 145 In recent years with increasinglyhigh prices for palm oil rubber and more recentlywood pulp these figures have increased ratherthan decreased and UNEP projects the loss of 98of forests in large parts of Indonesia by 2022(UNEP 2007) as by January of 2015 only 46 oforiginal forest cover in Indonesia remained with aloss of over 917000 ha annually between 2009 and2013 (Forest Watch Indonesia 2015 Butler 2015)Furthermore this loss of forest has included

not only encroachment but also in some cases thealmost entire denudation of protected areas suchas Riau National Park in Indonesia (Pearce 2007)of which only 26305 ha of the 1578274 ha offorest present in 1986 remained in 2006Drivers of deforestationmdashAcross the global trop-

ics the main drivers for deforestation differ signifi-cantly with clearance in the Neotropics oftenreflecting pressure for ranching in Africa for swid-den and in Asia for tree plantations (Boucheret al 2011) Several types of agroforestry exist atdifferent extents and scales across SE Asia includ-ing fruit orchards generally on a small-scale basisand large-scale oil-palm in Southern SE Asia(Malaysia and Indonesia) rubber throughout theregion andmore recently wood pulp and biofuelsThese new tree-plantation areas predominantlycome from formerly forested sites as SE Asiashows that forests are the primary source for a


SYNTHESIS amp INTEGRATION HUGHES

much higher percentage of new agricultural landthan any other region on earth (Gibbs et al 2010)

FAO statistics (httpfaostat3faoorghomeE)show that since 1985 the tonnage of fruitexported from Vietnam and Thailand has morethan doubled and in Indonesia it has tripledThis fruit export however is a relatively minordriver of deforestation compared to that of rub-ber and oil-palm Oil-palm was initially plantedin Asia in around 1970 yet by 2011 exports hadreached 30 million tonnes annually from Indone-sia and 20 million tonnes from Malaysia withIndonesia and Malaysia alone making up almost86 of global oil-palm exports (httpatlasmediamiteduprofilehs1511) In addition to havingsome of the worldrsquos highest palm-oil exportsIndonesia also has some of the highest exports ofrubber (as does Thailand) but countries acrossthe region have shown significant increases inthe growth of all tree crops in recent years

Eucalyptus and Acacia plantations for pulpand paper is also increasing rapidly in SE Asiaand as of 2008 83 million hectares of eucalyptusplantations had been planted within SE Asia outof a global total of 196 million ha (Rejmanek andRichardson 2011) Plantations for pulp are amajor issue across the Asian region as in addi-tion to being dominated by a small number oflarge corporations (ie APP Advance Agro andStora Enso Lang 2002 2008) have forced peopleoff their own land into increasingly marginalareas increasing the loss of forest in areas thathave poorer agricultural potential (Gerber 2011)The optimal size for a monoculture plantation is30000ndash50000 ha (Hall 2003) and therefore thedevelopment of these large monocultures hashomogenized the landscape and forced smallholders off the land in many cases (Gerber 2011)This loss of land is not a trivial issue and in the38 large monocultures examined in Gerber(2011) all 38 showed the loss of customary land4737 showed direct deforestation and 8showed water shortage as a result of plantations

SE Asia also exports 87 of the worlds naturalrubber but unlike oil-palm and pulp-paper rub-ber is still predominantly grown by small holders(85ndash93) probably due to the greater intensityrequired to harvest it relative to other tree-plantation products in the region (Fox and Castella2013) Yet this fact makes certification of sustain-ability challenging and though two reviews

have considered the eco-certification of naturalrubber (Gouyon 2003 Kennedy 2014) there hasbeen little uptake or enforcement despite theimplications (reduction in biodiversity increasederosion increased risk of landslides [Fox et al2014]) Rubber demand is also projected torequire a further 43ndash85 million hectares to meetdemands by 2024 (Warren-Thomas et al 2015)and given the low diversity of vertebrates mono-cultural rubber can sustain relative to the land-cover it most frequently replaces (ie swidden orforest) this has negative implications for diver-sity across much of the regionIn an analysis published in January 2015 that

scored and ranked 500 companies globally ontheir policies relating to deforestation SE Asiahad considerably lower scores than any otherregion and falls below the global average scoresfor all indices measured indicating less trans-parency fewer policies relating to commodities orforests and lower sustainability in its operations(Rautner et al 2015) Industries and banking cor-porations within Asia have the least sustainablepolicies of any globally and banks (particularlyin China httpblogbanktrackorgp=522) havebeen explicitly tied to large-scale deforestationin Indonesia with a single bank financing over$300 million toward deforestation and sevenChinese banks financing over $100 million eachFurther analysis brought out by a new ldquoforestsand financerdquo initiative (WWF 2006 httpforestsandfinanceorg) showed that the five coun-tries investing most in ldquodeforestation riskrdquo sectorcompanies (rubber oil palm or pulp and paper)in SE Asia are all Asian and have invested over$2508 billion and when the entire region is con-sidered this increases a further $16 billion Thishas caused shifts in the nature and the scale ofregional deforestation and causes plantations tobecoming larger and increases the overall pro-portion of ownership which is under large corpo-rations These corporations are also capable ofusing political influences to secure concessionsfor rubber and oil palm within areas classed asprotected areas (Global witness 2013 2004 Ilmanet al 2016 httpwwwglobalforestwatchorgcountryIDN) Furthermore despite originatingin South America rubber is officially consideredas a forest species in a number of SE Asiancountries and thus plantation coverage is usedtoward national forest coverage goals within the



UNFCC Kyoto protocol and GSF Frameworks(Bagri et al 1999 Dang 2012) and masks thealarming loss of forest across Asia with everincreasing expanses of monocultural plantation(Xu 2011) In fact across SE Asia the subsidiestied to the Convention on Biodiversity (CBD)have been systematically abused due to loosedefinitions lack of regulation and insufficientattention to detail resulting in some cases in thereplacement of natural forests with plantationsof non-native species (Totten et al 2003 Cien-ciala et al 2007 Meyer et al 2009 Zhai et al2014) Similar programs such as Chinarsquos ldquoGrainfor greenrdquo and sloping land conversion initia-tives have been stated to cause losses in nativebiodiversity due to the clearance of native vege-tation which are replaced by alien monoculturesoften stimulated by perverse incentives (Smajglet al 2015) These new plantations are oftendeveloped in areas unsuited to such species(Ahrends et al 2015) and thus not only removingnative habitat but also effecting the water-tablesoil composition erosion and increasing the riskof invasive species spread and thus negativelyaffecting a significantly larger region (Cao andYu 2009 Cao et al 2010 Wang et al 2013Giambelluca et al 2016 Hamilton et al 2016)This has potentially increased the loss and degra-dation of particularly vulnerable habitats suchas those on Hainan Island and has serious impli-cations for already critically endangered speciessuch as the Hainan gibbon (Zhang et al 2010bZhai et al 2014) In a number of countries thatare classed as showing net-afforestation it hasbeen demonstrated that they import unsustain-ably harvested native species from other parts ofAsia and that the plantations are not only non-native but cause changes in the water-table andthereby effect any remaining nearby forestedareas (Engel et al 2005 Zhai et al 2014) Reduc-ing emissions from deforestation and forestdegradation (REDD) is an example of a globalinitiative that has the potential to facilitate rain-forest preservation globally but criticisms that ithas failed to include sufficient metrics to ensurebiodiversity retention has in part resulted in thedevelopment of further programs (REDD+ andUN-REDD) (Schmidt 2009 Harvey et al 2010Rands et al 2010) REDD provides a mechanismto exchange ldquocarbon creditsrdquo for the protection ofldquotree-coveredrdquo areas but these have frequently

been low biodiversity monocultures of non-nativespecies (Kill et al 2010) Analysis in a number ofcountries in Southeast and Southern Asia high-lights not only the need for the tailoring of REDDto the local environment and situation but alsothe trade-offs between social and environmentalbenefits from REDD+ (Mohammed et al 2016)When well-orchestrated and monitored like pay-ment for ecosystem service (PES) schemes(Hughes 2012) and biodiversity offsetting (Maronet al 2012 Tregidga 2013) REDD+ has the poten-tial to provide useful mechanisms to finance theretention of forests but also face the risk of nothaving adequate mechanisms to ensure biodiver-sity retention and risk collapsing the value of bio-diversity to a single value (OrsquoNeill 1992) and thusat risk from market fluctuations It has beensuggested that REDD may be adapted and incor-porated into updates of the Kyoto as a mandatedcomponent of global-level agreements howeverbefore this can happen biodiversity must bebetter integrated into REDD programs possiblythrough the integration of pre-existing certifiedstandards such as the Biodiversity Alliance(As 2012)Many parts of SE Asia also face issues from

ldquoland-grabbingrdquo from large companies This prac-tice in which large corporations obtain land-own-ership through deals of questionable legality notonly force people off their traditional lands (caus-ing loss of livelihood) but furthermore both causedirect deforestation within the concession anddegradation of surrounding areas due to increasedpressure and usage from the former inhabitantsof the areas (Global Witness 2013) This hashelped shift the drivers of deforestation from thetraditional swidden and small-scale subsistencefarming for food to much larger scales of tree-plantation production (Michinaka et al 2013)Moreover several SE Asian countries have seen ashift in land tenure from communities to stateand this has several legacies including increasedintensification of agriculture and increased defor-estation in non-plantation areas and high pres-sure along road-sides especially in the event ofrelocated villages (Hett et al 2012) Relocationof villages for these large concessions may alsolead to a loss of traditional knowledge and con-nection to the land and local ecosystems andthus increase local pressure from hunting andother forms of natural resource use Issues with



governance and corruption have helped supportthe conversion of large tracts of formerly forestareas into tree-plantation production landscapes(Barr et al 2010 Phromlah 2014) These issueshave provided individuals and companies withaccess and political support which has increasedthe rate of deforestation for large parts of the1990s and beyond in countries including Cambo-dia Myanmar and Indonesia (McCarthy 2014)in some cases supported by funding designatedfor reforestation (Barr et al 2010)

Though in recent years and especially in 2014many large companies have agreed to zero-defor-estation and other sustainability policies and amoratorium many of these are difficult to enforceand have had variable levels of success since theirinstigation (EIA 2014 Fishman 2014) Agree-ments such as those from Asia Pacific ResourcesInternational Ltd (APRIL) are now receiving criti-cism due to shifting targets and disputes over anumber of large land concessions SustainableForest Management Plan (SFMP) has receivedcriticism for not following through on commit-ments made and sceptics are becoming increas-ingly vocal on the lack of real behavioral changefollowing former agreements (Fishman 2014)

Roundtable on Sustainable Palm Oil (RSPO)has also attracted increasing attention and thenaming of companies and their sourcing policiesby WWF (2013 REPORT CARD httpwwfpandaorgpalmoilscorecard2013) highlights toconsumers the sustainability of choices theymake with regard to oil-palm sourcing

Charcoal production is another driver of defor-estation and degradation across the SE Asianregion with around 44 of global charcoal pro-duction occurring within Asia (with 1424 ofthis from Indonesia and 915 from China httpsatlasmediamiteduenprofilehs4402) yet thishas received very little attention even in pur-portedly global reviews (ie Chidumayo andGumbo 2013) In other parts of the world consid-erable research has examined the impacts ofcharcoal manufacture on biodiversity but nonehave so far been published within SE Asiathough it is likely to degrade and destroy foreststo release smoke and CO2 that contribute to glo-bal warming and to provide a fire risk especiallyin the peat-dominated soils of Indonesia

Impacts of deforestation and tree-plantationsmdashTheimpacts of increasing deforestation resound at

multiple levels from the increased erosion due tohigher surface run-off (Ma et al 2014) increasedrisks of landslides (Fox et al 2014) impactingfreshwater and terrestrial systems to the lossand degradation of important forest habitatsSE Asian forests include the majority of global

tropical peatland forest (56) in addition to 42of the worlds mangrove forests (Gopal 2013)However by 2010 only 45 of original tropicalpeat forests remainedThe effect of habitat loss on biodiversity across

Asia is a primary threat to regional biodiversitywith the progressive loss of species with habitatloss (Sodhi et al 2004 2010 Brook et al 2003Koh et al 2009) and regional endemics forest-dependent species and large ranging species inparticular are at high risk of regional extinctionfrom habitat loss (Turner et al 1994) With incre-asing fragmentation of remaining forest as aresult of conversion to tree-plantations comes thedegradation and increasingly high ratios of edgehabitat which is unsuitable for a proportion ofnative species Lower quality forest (due todegradation or selective logging) is known toretain less species at all tropic levels (Tawataoet al 2014) The majority of native species areunable to survive in tree-plantations meaning analmost total loss in native species diversity in theever expanding areas of tree-plantations acrossthe SE Asian region (Edwards et al 2010)Numerous studies have confirmed the value of

extensive areas of undisturbed primary forestwith disturbed forests retaining less species andthe loss of species from fragments over time(Sodhi et al 2012) Even taxa that may be exp-ected to be maintained in fragments such asants show low retention in small fragments(Lucey et al 2014) and the usage of chemical tre-atments within monocultures further decreasesbiodiversity in and around plantationsSelective loggingmdashSelective logging can take a

variety of forms from legal selective and ldquolowimpactrdquo logging to the illegal logging of oftenhigh-value timber from protected areas Illegallogging has highly variable impacts dependingif it is the extraction of a small number of high-value timber species covertly (which is likely to belocalized) or involves clear-cutting of larger areaswhich is obviously much more detrimental to bio-diversity Logging of some form is estimated tohave affected at least 20 of the global tropics in



just the period between 2000 and 2005 (Edwardset al 2014a b c d) thus understanding the impli-cations of logging for biodiversity is essential tofacilitate adaptive planning and conservation

In the case of selective logging and ldquoreducedimpact loggingrdquo minimal impacts on biodiversityhave purportedly been found for some taxa (Edw-ards et al 2012) However both species abundan-ces and diversity overall decreased markedly inselectively logged forest and higher diversity wasfound in areas that were made up of intact forestpatches and cleared areas than in those whereselective logging occurred (Edwards et al 2014aMartin et al 2015) Analyses also show progres-sive decreases in the volume of timber extractedon multiple iterations of selective logging anddecreases in carbon stock retention (of around25 per harvest) (Putz et al 2012) with variableretention of biomass and recovery speed depend-ing on the methods used to guide operations

In terms of ecosystem dynamics selective log-ging causes changes to species community com-position trophic organization and food-webcomplexity (Woodcock et al 2013 Edwards et al2014b Ewers et al 2015) though the impacts varysignificantly by guild and diet in some taxa(Burivalova et al 2015) Functioning of essentialecosystem services following logging has rarelybeen studied within Asia but studies within Bor-neo show considerable decreases in the rates ofkey processes including a 15 decrease in therate of litter decomposition (Ewers et al 2015)and differences in the dispersal and survival ofvarious tree seeds (Bagchi et al 2011) In additionselective logging may require more land for thesame profit margins and the necessary road net-work is likely to facilitate further logging in addi-tion to hunting and other forms of habitat usagewhich may have longer-term impact than logging(Brodie et al 2015) Roads built to facilitate log-ging have been correlated with numerous otherforms of disturbance from changing the densityof forest (and thus ecosystem structure and func-tion in the vicinity of the road (ie Hosaka et al2014 Yamada et al 2014) to facilitating numerousmore severe and long-lasting forms of unsustain-able ecosystem use and degradation (Clementset al 2014 Laurance et al 2014) in addition tofacilitating hunting (Brodie et al 2015)

Furthermore the standard definition andstandards of reduced impact logging at least

traditionally have allowed considerably moretree removal in SE Asia (9 trees per ha) than inother parts of the world (normally 1ndash2 trees perha [Sist 2000]) and at this intensity of logging itmay be that potential benefits to biodiversity arereduced considerably The frequency of loggingcycles has also not been well regulated across theregion resulting in marked decreases in diversityin countries where logging cycle length hasreduced in recent years (ie Myanmar Khaiet al 2016) Therefore though reduced impactlogging has the potential to mitigate the loss ofspecies (especially if well managed) when com-pared to clear-cutting the actual retention of spe-cies is higher and the change in ecosystemfunction lowers through land-sparing of largecontiguous forest patches (Edwards et al 2014a)even if this means that more land overall is moreintensively harvestedUrbanizationmdashOver the past several decades

the SE Asian region has seen the progressiveincrease in the size and populations of its citieswith the population approximately doublingfrom 760 million in 1985 to 16 billion by 2010equating to around 42 of the total population(Ismail 2014) Approximately 088 of the land-surface is covered by urban areas (Schneideret al 2010) and the peri-urban sprawl aroundmany of the regions larger cities has also dramat-ically increased the urban area (Murakami et al2005) Over half the worldrsquos expansion in urbanland over the next two decades is predicted tooccur in Asia (Schewenius et al 2014) with largeproportions of this occurring in relatively ruralcountries such as Vietnam and Myanmar Urban-ization has all the normal biotic consequences ofdeforestation in addition to increasing pollutionsurface run-off and providing a source of stablepopulations of potentially invasive species(Afroz et al 2014 Wells et al 2014) Further-more whereas urbanization may be theorized totake pressure off rural areas the opposite hasbeen found to be the case with increasing ratesof deforestation correlated with progressiveurbanization in 41 tropical countries studied(DeFries et al 2010)By 2000 over half of SE Asiarsquos urban areas

fell within biodiversity hotspots (Geurouneralp andSeto 2013) Furthermore in global analysis theexpansion of urban areas in East and SE Asia wasfound to potentially disproportionately impact on



protected areas with more protected areas pro-jected to become within 10 km of a city by 2030 inSE Asia than in any other region (McDonald et al2008) On a global scale this urban expansion alsoincreases the area of urban land within hotspots ofbiodiversity and endemism by around four times(Elmqvist et al 2016) driving a direct loss in bio-diversity in areas directly converted increases inaccessibility and potential disturbance to sur-rounding regions and increasing demands for con-version of surrounding regions to support theneeds of urban dwellers

Within urban areas parks can representrefuges for biodiversity in an otherwise hostileenvironment However within SE Asia largermore populated cities have fewer and smallerldquogreen spacesrdquo (Richards et al 2017) despite lar-ger parks unsurprisingly sustaining more species(Sing et al 2016 Yuan and Lu 2016) Howeverrelative to other regions relatively little researchon maximizing urban biodiversity retention hasbeen conducted within SE Asia and more workis required to better understand how urban con-figuration impacts on different species (Benindeet al 2015 Botzat et al 2016)

Within China the ldquoEcological redlinerdquo policybeing implemented in some cities aims to explorehow ecosystem service provision can be main-tained even within cities (Leurou et al 2013 Bai et al2016) If supported by empirical data suchapproaches have promise to moderate the impactsof further development on biodiversity howeverthe effectiveness such a system depends not onlyon solid and rigorous data during developmentbut also on clear implementation guidelines andstrict monitoring and reporting structures whichare still under development Such approaches areurgently needed in an urbanizing region withrapid population growth both to protect poten-tially vulnerable areas with high diversity and tomaintain biodiversity within urban environments

PrognosismdashDespite guarantees and promisesof no net-deforestation and increasing pressurefor sustainable palm-oil the prognosis for muchof the remaining forest in SE Asia remains poordue to enforcement corruption and governanceissues Even if only plantations and pulp millsthat have currently been planned (Verchot et al2010 Wakker 2014) are developed there willstill be considerable further forest loss acrossthe Asian region Though enforcement through

initiatives such as REDD+ could if used andenforced by external arbiters help protect pre-sent forests and their biodiversity and cease toclass and subsidize monocultures and as forestin reality enforcement is normally carried outthrough regional governing bodies Projectionsacross the region show considerable loss of for-ests into the future and with increasing fragmen-tation and decreasing overall extent the abilityof the ever shrinking forests to retain biodiversityis also progressively diminished Furthermorethe high levels of conflicts between local commu-nities and large corporations and decrease innearby land agricultural productivity increasethe unsustainable usage of remaining forestareas Without stricter international regulationand enforcement it is probable that large corpo-rations will continue with their current unsus-tainable practices leading to continued levels ofdeforestation and degradation across the regionFurthermore restoring areas following either

logging or plantations has proved difficult withstudies showing low soil nutrients even two dec-ades after logging (Amlin et al 2014) and poorregeneration in former plantations in additionaround them especially after the growth of Euca-lyptus (due to its allelopathy Chu et al 2014Thijs et al 2014) Recent studies have alsorevealed that not only does aboveground diver-sity decrease upon the establishment of monocul-tural plantations but furthermore there aresignificant reductions in species diversity in thesoil such as a 45 loss in invertebrates (Barneset al 2014) meaning that the restoration ofecosystem functioning even upon the removal ofthe plantation is likely to be slow at best Studieshave also shown that tree plantations cannot sus-tain high diversity of forest-dependent species(Wilcove et al 2013) and that ever expandingtree plantations therefore potentially have signifi-cant negative effects on native forest commu-nities through habitat loss and fragmentation

Hunting and tradeOverview of hunting and trademdashGlobally the

illegal wildlife trade is worth approximately $20billion annually (South and Wyatt 2011) and inSE Asia hunting and trade remain a major threatto biodiversity despite moves to tighten regula-tions regarding international trade in endangeredspecies Bushmeat markets across the region still



openly display various species some of which areyet to be scientifically described (as evidenced bythe Laotian rock rat and Biswamoyopterus laoensissquirrel [Jenkins et al 2004 Sanamxay et al2013]) Traffic seizure data detail an increasingnumber of seizures in addition to a growth in sei-zure size since monitoring began in 1975 (TRAF-FIC database httptradecitesorg)

Though much of the international trade inwildlife from Asia to other parts of the world isfor zoos and aquaria within Asia the driversare primarily for food traditional forms of medi-cine or ornamentation This broad swath of dri-vers means that no species is immune fromthreat (Corlett 2007) as many species have ldquopro-pertiesrdquo for traditional forms of medicine andalmost no species is too small to be exploited forbushmeat especially if that species can be har-vested in high quantities (ie entire roosts ofinsectivorous bats in caves may be hunted outA C Hughes and K Tanalgo personal observa-tion) Within SE Asia forests are increasinglybeing described as empty due to high huntingpressure even within reserves (Harrison 2011)As human populations have increased so has for-est accessibility additionally increases in demandhas driven the loss of the majority of mammalsover 2 kg in most forests across Tropical EastAsia (Corlett 2007) Furthermore bushmeat hasbecome the food of the rich within SE Asia andwith the expanding middle class prepared to paysignificantly more for wild meat than equivalentquantities of domestically sourced meat this isset to increase into the future (Drury 2011)

Between 2000 and 2006 the United Sates aloneimported over 500000 shipments of live wildlifemade up of over 1480000000 animals (Smithet al 2009) Shipments of wildlife to the UnitedSates were largely commercial (92) predomi-nantly the pet trade and over 69 of these liveanimal imports originated in SE Asia (Smithet al 2009) however the Middle East is alsobecoming a progressively important driver in thetrade of wild-caught species for pets (Bush et al2014) The sale of wild-caught SE Asian animalsfalsely classed as captive-bred to bypass existingtrade regulations has led to the illegal harvest ofincalculable numbers of animals (especially rep-tiles) to supply zoos aquariums and the pet-trade (Nijman and Shepherd 2009 Lyons andNatusch 2011 Natusch and Lyons 2012) in some

occasions cooperating with legitimate breedersto create false documentation (Herbig 2010) Thistrend is particularly interesting as recent analy-sis of the legal and illegal trade of terrestrialshowed with regard to legal trade in vertebratesglobally SE Asia had very little role yet the ille-gal trade within and from SE Asia for the pettrade is among the highest globally particularlyfor mammals and birds (Bush et al 2014) Fur-thermore until this point the scientific commu-nity has frequently failed to consider the role oftrade on the future survival of many reptile spe-cies and thus even basic ecology of these speciesis little known or studied and the control of exist-ing trade rare at best (Baker et al 2013)Across much of the region the enforcement of

existing laws is considered weak (TRAFFIC 2008Nowell 2012 Ngoc and Wyatt 2013 Brook et al2014) and the certified trade of pre-ban stock ofendangered species of a number of taxa creates aneasy loop-hole for trade The existence of anyform of legal trade in these species has consider-ably weakened the ability to enforce regulationson the sale of various endangered species includ-ing ivory and pangolin scales (Bennett 2015) oreven ascertain the legal status of various materialsacross much of the region An IFAW survey foundthat even in licensed facilities 591 violated cur-rent regulations (Gabriel et al 2012) A total banon trade may be needed to allow any opportunityfor the current illegal trade to be halted (Bennett2015) Furthermore the release of small controlledvolumes of some of these materials (ie ivory intoChina from the Hong Kong stock of confiscatedIvory) is shown to have driven up prices andstimulated further demand (by over 170) ratherthan the anticipated reductions in demand thatwere hoped to on the release of ivory stocks (Gab-riel et al 2012) Much of the current release ofivory has been tied to government officials (Wild-Aid 2014) and this together with the considerablenumber of people employed as ivory carvers arethought to be motivators for the continued tradein Ivory within China Ironically much of thisivory trade actually decreased prior to 2002 butwith government encouragement and supportthrough being defined as a part of ldquointangible cul-tural heritagerdquo (as are other species) the trade inivory has boomed in recent years particularlyafter 2009 (Gao and Clark 2014) with a fivefoldincrease in the number of legal carvers between



2004 and 2013 and dramatic increases in price(up to $1033 per gram in 2014) have causedincreased trade exponentially

Furthermore the exploitation and trade inendangered species has recently become moresophisticated and mechanized with much cur-rent trade under the control of internationallyrecognized criminal gangs (Van Uhm 2012)These gangs are part of organized crime syndi-cates with complex networks at all stages forprocurement transfer and distribution betweenall parts of the world (ie Europol 2011 Wylerand Sheikh 2013)

Regulation of hunting and trademdashRecent techno-logical advances have increased the tools avail-able for monitoring wildlife tracking acrossborders Broadly there are two main ways inwhich technological advances can help decreasethe illegal wildlife trade (1) reactively throughactual detection during trafficking and (2) proac-tively through online detection methods to haltthe sale and in some cases collection of CITES-listed species

Since the mid-2000s the molecular technolo-gies have been successfully used to detect andprevent the trade in particular endangered spe-cies (Coghlan 2014 Johnson et al 2014) Molecu-lar approaches can detect the species includedeven within complex traditional medicines (Luoet al 2013) These techniques are becoming fasterand more efficient (ie httpsnanoporetechcomproductsminion Hance 2015) and thus pro-vide true potential as a detection tool in manyborder situations These advances allow for thedetection of CITES-listed species in real time evenfrom samples of animal tissue making detectingtrade much simpler than was formerly the case

Other techniques such as the use of wildlifedetection (conservation) dogs to detect wildlifein the field or in illegal exports (Reed et al 2011TRAFFIC 2013) have started to be employed inairports across the region and if expanded havethe potential to significantly reduce wildlife traf-ficking The use of these new methods if appliedstrategically has the potential to curb wildlifetrade though it is unlikely to be able to copewith the huge volumes of material being tradedand further enforcement and monitoring isrequired within countries rather than only whencrossing borders to decrease the illegal traffick-ing of endangered species

The Internet and online auction sites have pre-viously hugely facilitated the trade in endangeredspecies and as a result TRAFFIC has workedwith 25 Chinese-based auction sites and used ahuge array of key words to detect and delist itemsoriginating from CITES-listed species (Stoner2014) Multiple similar websites to track the trad-ing of endangered species using key wordsearches combined with other forms of data nowexist (ie httpwildlifetradetrackerorg httpwwwhealthmaporgwildlifetrade) and are pro-viding new insights which may help reducefuture illegal trade Enforcement and monitoringnetworks are also evolving to detect and react toillegal trade (httpwwwasean-wenorg httpwwwlaga-enforcementorg httplusakaagreementorgpage_id=24) but much work is neededto strengthen such efforts across the Asian regionSophisticated methods of analysis such as the

use of scripts to break down and analyze pat-terns of trafficking (Hancock and Laycock 2010Moreto and Clarke 2013 Kretser et al 2014Lavorgna 2014) can even catch perpetratorsbefore they harvest or collect the threatened spe-cies The use of scripts can be as specific and tar-geted as needed and deal with all aspects oftrade (ie Lavorgna 2015) yet such analysis hasnot yet been concentrated on Asia despite themassive volume of trade and very low rates ofdetection (ie 3 in Vietnam DLA Piper 2014)For some rare large-bodied species (ie large

carnivores elephants rhinos) the use of real-time anti-poaching tags has been suggested(OrsquoDonoghue and Rutz 2015) Yet such meansare only viable for organisms that are alreadyvirtually on the brink of extinction and methodsthat do not require such high quantities of dataon the individual level need to be developedHowever what is most needed is enforcement

of existing rules as areas such as Vietnam haverigorous frameworks in place (DLA PIPER 2014)yet these regulations are not being enforced inmany cases and as a result CITES-listed speciesare often on open sale and easy to obtain (iePhelps and Webb 2015) Methods now exist toanalyze and anticipate sales and much morecould be done to reduce the threat of the wildlifetrade on regional and global biodiversityChanging human behaviormdashEducation on sus-

tainable practice is needed across SE Asia in addi-tion to the stigmatization of the consumption of



wildmeat as if the image of eating wildmeatbecomes branded a different way than it is likelyto lose its appeal to many current consumers Thisalso extends to traditional medicines where theincreasingly empirical approaches are of benefit toall in replacing unproven unsustainable medicineswith tested and sustainable alternatives but thereis still a long way to go before synthetic andor sus-tainable (ie FairWild harvested plants Bundalo2010) become mainstream in cultures which stillrely heavily on traditional medicines within healthcare (Xu and Yang 2009) Celebrities leaders andhealers can act as conservation ambassadors andhelp stigmatize the use or consumption of unsus-tainably harvested species (Blondeau and Buf-fetrille 2008 Lu et al 2013) Ultimately citizens arethe best emissaries monitors and enforcers and tomake this a reality requires education engage-ment and empowerment with communities acrossthe region For long-term change scientists need towork with society managers and politicians tocreate sustainable societies to protect both locallivelihoods and rights while guiding and support-ing sustainable use

MiningMining is a frequently overlooked driver of

extinctions and biodiversity loss across SE Asiayet both mining for underground minerals andof limestone outcrops for cement have majorimpacts on regional biodiversity Mining occursin two main forms in SE Asia the mining of lime-stone for the production of cement and the min-ing of underground minerals Both these formsof mining can have devastating consequences fordiversity but effect biodiversity in a number ofmarkedly different ways

KarstsmdashOverall there is approximately800000 km2 of karst in Tropical SE Asia andSouthern China (Day and Urich 2000) and theregion has eight of the 47 world-heritage pro-tected Karsts and a further eight of the 30 tenta-tive areas (Williams 2008)

However in recent years the increase incement exports has grown exponentially withthe global annual quarrying of 178 million metrictons and an annual increase of 57 (Kingston2010) Currently of the top five global exportersof limestone three are in SE Asia (India Vietnamand Malaysia) with these three countries aloneexporting 189 of global cement exports (http

atlasmediamiteduenprofilehs922521) Indo-nesian cement domestic sales increased by 17 in2011 representing a total of 479 million tonsannually in addition to a further 12 million tonsexport (Worldcement 2012a b) India also listedas the highest global importer at 27 of globallimestone imports Further increases in consump-tion and import of 5ndash18 annual growth are fore-cast for a number of countries in the region(Worldcement 2012b) The use of cement byChina has also increased exponentially and injust the period between 2011 and 2013 Chinaused more cement (66 gigatons) than the totaluse of cement by the United States through his-tory (45 gigatons) (Washington Post 24 March2015) and a current consumption equivalent to15 tonnes per person annually (Bell 2012) Thismining and export of limestone is from the exten-sive destruction of karsts often without in depthimpact assessmentsKarsts are recognized as hotspots of endemism

and are typically populated by highly specializedspecies with limited dispersal ability Karsts havealso been relatively understudied and as a resultevery study to karst regions describes new speciesof a wide variety of taxa A search on GoogleScholar using the search terms karst and ldquonewspeciesrdquo and specifying the period between 2010and 2016 yields 5680 results and adding the termAsia yields 2370 meaning that not only do karstshave a high rate of species discovery but around4173 come from the Asian region A furtherbreakdown yields 468 results from Reptiles (in-cluding 132 Gekkonidae and 171 Squamata) 446Amphibians 320 Rodent 155 Chiroptera 1680plant (including 114 Gesneriaceae 65 Begoniaand 59 Urticaceae) and 371 Molluscs (268 refer-ring to Gastropoda) these results are not thenumber of new species from the region (Asia is ahuge region and they are not all descriptive plusmany describe multiple species) but the resultsare indicative of huge levels of undescribed ende-mic species The level of isolation between karstsand the matrix characteristics contribute signifi-cantly to the level of endemism on any singlekarst (ie Schilthuizen et al 2005 Clements et al2008 Struebig et al 2009 Latinne et al 2011Chung et al 2014)In addition to highly specialized and endemic

species karsts also represent hotspots of biodiver-sity and in Vietnam karsts are stated to harbor



over 2000 plant species 541 chordates and 2000insect species when using relatively crude taxo-nomic metrics (Tuyet 2001) Caves and Karsts arealso essential for various life processes (ie Gloverand Altringham 2008) and intact forest in theregion surrounding the karst may be essential notonly to karst roosting species but also to maintainmicroclimatic conditions and thus karst habitatstructure (van Beynen and van Beynen 2011Nicolas et al 2012 Liu et al 2015)

Increasing exports of cement and limestoneacross Asia has significant implications for thelong-term survival of these species as each karstmay have a unique selection of species Eventhough some of the worldrsquos largest cement expor-ters (ie Lafarge Holcim) have biodiversitymanagement plans in place (ie Imboden et al2010 Frechette 2013 Lafarge 2014) many smal-ler companies do not and even the best manage-ment action plans cannot prevent the loss ofspecies with such high levels of endemismSustainability guidelines (httpwwwwbcsdcementorgindexphpenkey-issuesbiodiversityesia-guidelines) represent an important steptoward better management of karsts but withoutbaseline data or inventories from the majority ofSE Asian karsts making informed choices onquarry location and strategy to maximize biodi-versity retention is impossible When even com-panies such as Lafarge that promote best practiceguidelines are documented to risk species extinc-tions (Vermeulen and Marzuki 2014) the increas-ing extraction of limestone across SE Asiarepresents a huge driver of extinctions of some ofthe regions least known species

Mineral extractionmdashSE Asia is also globally oneof the greatest exporters of minerals with Indone-sia currently ranked as the 7th greatest exporterand Malaysia as the 15th (httpwwwindexmundicomtradeexportssection=5) Many countriesacross the region depend upon mineral exports asa significant proportion of their GDP for example50 of exports from Lao are copper ore (httpatlasmediamiteduprofilecountrylao) which indi-cates the huge dependence on mineral extractionfor many economies across the region Despitethis there has been very little empirical researchon the impacts of mining on regional biodiversitythough the indirect effects include opening areasup through road construction and direct impactsinclude seepage quarry collapse (Yang et al 2014)

On a global scale mining sites have a highcoincidence with protected areas (Duran et al2013) with 34 of mines for just four metals(copper bauxite zinc and iron) within 10 km ofmine boundaries and taking up 14 of the totalland area Furthermore a higher percentage ofprotected areas in Asia have mines within theirboundaries (771) than almost any other part ofthe world (with the exception of Europe) and at2462 of mines within the 10 km of PAs com-pared to 2263 predicted by the null modelIn addition to the direct impact of the clearance

associated with developing and utilizing a minethere are additional wider problems (the multi-plier effect) such as ground-water pollution fromseepage changing soil chemistry and fauna(Andres and Mateos 2006) and thereby all pro-cesses relating to biodiversity Few studies havebeen conducted in Asia but studies in other partsof the tropics show the loss of biodiversity andespecially aquatic diversity as a result of miningfor minerals (ie Brosse et al 2011 Wantzen andMol 2013 Edwards et al 2014c) Heavy metalaccumulation is noted to feed up through foodchain (Satta et al 2012) and may effect speciesreproductive viability and lifespan Coal miningis also a significant export from some parts of SEAsia with Indonesia as the worldrsquos second great-est exporter exporting 192 of global coalexports requiring the clearance of large areas offorest (httpatlasmediamiteduenprofilehs922701) Despite the fact that a framework to mini-mize the impacts of mining has been considered(Maryati et al 2012) it has clearly not been imple-mented in detail as coal mining is the fourthgreatest cause of deforestation for large parts (Kal-imantan Sumatra) of Indonesia (Abood et al2014) In addition to direct damage from clear-ance the extraction of coal also contaminates soils(Mizwar and Trihadiningrum 2015) and thereforeis likely to contaminate soil and freshwaterRestoration following mining also has a low

rate of success (Cristescu et al 2012 Majer 2014)and diversity in the region around former mine-sites loses species during mining and does notsubsequently regain them (Tropek et al 2012)Thus mining of all forms represents a significantthreat to biodiversity in a region considerablylarger than the mining site and this diversity isunlikely to recover even with restoration Thuscareful planning is needed to optimally locate



sites and ensure minimal disruption to biodiver-sity by preventing initial loss of sites with highbiodiversity or endemism

Reservoir constructionThe Asian region has long been the part of the

world with the greatest number of dams (ie30 in 1950 65 of all dams in 1982 Lehneret al 2011) Globally there are currently plans tomore than triple the number of dams and reser-voirs (Zarfl et al 2015) with a per basin pro-jected average of over 100 dams for most of theSE Asian region and even single rivers may havea have a significant proportion of global dams(ie the Yangtze river alone has 625 of damsglobally [50000800000]) Future plans for fur-ther construction of dams across the regioninclude the planning of over 116 new dams inLaos (Economist Asia 20 December 2014) andmore than this in single states of India and pro-vinces in China including plans for the worldrsquoslargest dam The results of the world commissionon dams study showed the negative impacts ofdams on the local economy and biodiversity andas a result the further development of dams inthe Southern and SE Asian the World Bank hasbeen less ready to fund the further constructionof dams (Economist 18 November 1999 13 June2007) However there is a significant risk thatother banking groups such as the Asian Develop-ment and Asian Infrastructure Investment Bankwill support further construction in the future(Economist Asia 3 November 2013a b) and inaddition hydropower developments are oftenconditions of aid packages and may not be in theinterests of the host country (ie CambodiaMarks et al 2015)

Dams and reservoirs impact on biodiversity ina number of ways through the loss and transfor-mationsignificant altering of systems and indi-rectly putting additional livestock pressure ontoremaining unflooded areas due to reductions infish-stocks Furthermore the production ofmethane from the decomposition of inundatedplants as a result of dam construction is calcu-lated to have released enough greenhouse gasesto account for around 4 of global warming(Lima et al 2008 Barros et al 2011 Bastvikenet al 2011) Additional impacts of reservoirsinclude increased landslides along the rivercourse and increased seismicity which can both

impact on regional biodiversity (Li et al 2013)Additionally changes in regional climate havealso been noted in reservoirs monitored overextensive time periods (MEP 2009) which ulti-mately will effect regional species distributionsand survival probabilityAquatic impacts of damsmdashContrary to the belief

that large reservoirs will favor a significant num-ber of native freshwater species the constructionof dams is known to not only disrupt freshwatercommunities (Dudgeon et al 2006 2011) butcurrently planned dams on the Mekong are pro-jected to decrease fish freshwater biomass by20 and if all planned dams are completedmigratory fish biomass may decrease by up to70 (Ziv et al 2012 Welcomme et al 2016) Tur-bulent water in the vicinity of a dam and otheraltered regions causes significant volumes ofwater to become anoxic and this phenomenonalone is estimated to cause barotrauma andanoxia to over 1200 fish species in the Mekongregion (Brown et al 2014) Some of the speciesnotably at risk include the Asian Freshwater cat-fish and the Irrawaddy dolphin (Economist Asia2013a b 7 September 2013 Li et al 2013)Changes in water chemistry salination sedimen-tation siltation enhanced algal bloom probabil-ity and the loss of breeding grounds due to damconstruction slowing water flow-speed on tribu-taries and changing water-table levels also effectlong-term survival probability of numerousgroups and change aquatic community struc-tures from lotic to lentic in some parts of rivers(Xie 2003 Li et al 2013)Terrestrial impacts of damsmdashThe terrestrial

impacts of dams and reservoirs on biodiversity areeasy to forget yet highly significant The directloss due to flooding of large regions of intact forest(and in the case of karst regions high levels ofendemism) is often enormous for example theconstruction of the three Gorges dam is known tohave directly impacted upon over 3418 insect spe-cies 6388 plants 552 terrestrial vertebrates 350fish and over 1085 other aquatic taxa (MEP 20002001 Huang 2001) Negative social and environ-mental impacts resulting from dam constructionhave been found repeatedly particularly forindigenous groups and the rural poor (Aiken andLeigh 2015 Kirchherr et al 2016 Siciliano andUrban 2016) There is the additional loss of habitatfrom relocating settlements plus if fish biomass



has decreased due to changing river conditionsthen there are the additional needs for protein tho-ugh raising livestock which requires significantlymore land as the fisheries along the Mekong arecurrently estimated to feed over 65 million people(Economist 26 July 2012 Xu et al 2013)

In addition islands (former hilltops) in reser-voirs have been demonstrated to lose almost allmammal species including small rodents overrelatively short time periods (Gibson et al 2013)Studies in other parts of the world describe simi-lar effects on numerous other taxa includingamphibians (Lima et al 2015) and plants onboth islands and the new riparian zone (Li et al2013) This simplification and fracturing of meta-communities upon the formation of islands hasbeen modeled to affect the majority of communi-ties and implies that complex communities can-not survive on islands unless they adapted insuch conditions (Fisher and Mehta 2014)

In addition some of the regions currently atrisk of being flooded include the Nu valley (onlyrecorded locality of the critically endangeredMyanmar Snub-nosed monkey and endemicityhotspot [Geissmann et al 2012 South ChinaMorning Post 30 March 2014]) and the ecologi-cal impact of dams in some of the regions diverseand fragile ecosystems has not received sufficientattention With high regional endemism espe-cially on karsts (which are frequently dammed)reservoir construction is likely to represent a sig-nificant threat to a large number of little knownspecies across the Asian region

Furthermore and potentially most signifi-cantly the impact of upstream dams in China isnow having a profound effect across the regionby driving regional droughts and river depletion(China US focus 2016) In 2016 alone large areasof the greater Mekong Subregion faced the worstdroughts in recorded history due to upstreamdams driving 400000 ha of saltwater intrusionin Vietnam and affecting 67 of provinces in theCuu Long delta in addition to a multitude ofother negative social and environmental conse-quences (South China Morning Post 2 April2016) Not only do these droughts effect naturalsystems and riparian areas along the Mekongbut declining salinity and saltwater intrusionmay drive further deforestation and the exploita-tion of other natural resources by those losingtheir livelihoods as a result of the drought

Wetland drainageGlobally around 54ndash57 of wetlands that

existed in 1700 (and up to 87) have been lost(Davidson 2014) and a considerable portion ofthis has been in the Asian region Across SE Asiathere has been the progressive degradation andloss of wetland ecosystems The drivers of this areeither conversion to other land uses includingagriculture (ie oil palm) or degradation in extra-cting various resources (minerals oil peat) over-fishing siltation and pollution This degradationand destruction of wetlands has global implica-tions as among other issues SE Asia has a 56 ofglobal tropical peatland but 45 of the originalarea has been converted to oil-palm (Gopal 2013)Across the SE Asian region similarly high

levels of threat exist with 80 of SE Asian wet-lands threatened and up to 45 of inter-tidalwetland already lost in parts of the region Theloss of these coastal and inter-tidal wetlands notonly effects resident coastal and mangrove spe-cies but also impacts upon the over 50 millionmigratory waterbirds which use the East AsiaAustralasia Flyway (Conklin et al 2014) SE Asiahas the highest proportion globally in additionto absolute number of its migratory specieswhich are classed as threatened with 11 ofmigratory land-birds (52477) 23 of migratorywaterbirds (46201) and 33 of migratory soar-ing birds (2423) classed as threatened (Kirbyet al 2008) As a direct result of wetland degra-dation 62 of SE Asian waterbird populationshave recorded reductions and wader popula-tions of species utilizing the flyway havedecreased by 79 in just 24 years (Delany andScott 2006 Conklin et al 2014)SE Asia also has 42 of global mangroves

(Indonesia alone has 226) and the highestglobal mangrove tree diversity (Polidoro et al2010 Giri et al 2011) but a high proportion ofthese wetlands have already been cleared (ieover 80 of original coastal wetlands in thePhilippines Gopal 2013) Mangroves are beingcleared at three to five times the rate at whichother forests are stated to being lost and globally20ndash35 of former mangroves were lost since 1980(Valiela et al 2001 FAO 2003 2007) Mangroveloss in Asia is largely caused by six major driversconversion to sea-salt farms to shrimp (or otheraquaculture) to other types of agriculture or fromhydrological disturbance or development (Biswas



et al 2009) and of all these conversion to agricul-ture is the most common (Giri et al 2011)Though further conversions of mangrove siteshave been restricted by governmental regulations(due to the recognized role of mangroves inbuffering coastal erosion and reducing the risk offlood and tsunamis Polidoro et al 2010) this hashad limited success in some parts of the regionOn a more localized scale the use of ldquoAgentOrangerdquo is likely to have caused significant reduc-tions in the mangroves of Vietnam which mayhave been prevented from regenerating in someareas (Hong 2003) Sadly for many SE Asian man-groves the majority of clearance has already hap-pened (ie 55 of Thai mangroves were clearedprior to 1961 [Charuppat and Charuppat 1997]and 22ndash35 further from 1973 to 2000 [Wilkieand Fortuna 2003]) and analysis indicates the lossof up to 90 of Thai mangroves altogether (Wells2007) Analysis shows that though restoration isoccurring in some areas overall the rate of man-grove loss is actually accelerating and with anannual global loss of between 1 and 8(Miththapala 2008) and if present rates continueall mangroves are projected to be lost within thecoming century (Duke et al 2007)

The loss of mangrove habitats has serious impli-cations for biodiversity as many species (includ-ing fish reptiles birds and mammals) areendemic to mangrove systems and at least 40 ofmangrove dwelling animals have elevated red-liststatuses according to the IUCN (Polidoro et al2010) For both amphibians and reptiles Indochi-nese mangroves have similar or high levels ofdiversity and endemism to many of the forestecoregions within Asia (Das and van Dijk 2013)yet are rarely the subject of global discussions onpreserving biodiversity across the region On aglobal basis about 90 of marine organismsspend part of their lifecycle in mangrove systemsand 80 of global fish captures are mangrovedependant (Silyan and Kathiresan 2012) There-fore losses of mangroves have global conse-quences for biodiversity especially as any declinesin fish-stocks needs to be replaced by othersources of protein typically from the expansionand intensification of other forms of agriculturewith ensuing implications for terrestrial systems

Mangroves also act as a pollution filter fortruly marine systems though this can lead todangerously high levels of heavy metals (Silyan

and Kathiresan 2014) which not only potentiallydamage resident species but may damage mar-ine systems if mangroves are destroyed (throughthe release of accumulated toxins)Thus the loss and degradation of wetlands and

mangroves is a serious regional issue with globalimplications especially given that at present only69 is protected (Giri et al 2011) Mangroves arealso the worldrsquos incubators for many marine spe-cies and essential stop-overs for migratory birdsthus continued declines in these habitats havepotentially devastating consequences for the mil-lions of organisms dependent upon themFreshwater and peat wetlands are also impor-

tant for a wide selection of species with 200-300fish species recorded from Peninsula Malaysiaand over 83 taxa of aquatic invertebrates reco-rded from a single wetland (North SelangorPeat-Swamp) (Yule 2010) Changes in wetlandsnot only threaten aquatic species with extinctiondue to habitat loss and degradation but addi-tionally change nutrient cycling pH andincreases the probability of peat-dome collapse(Dommain et al 2010) These species are entirelydependent on intact wetland habitats thusmanaging wetlands is essential for the long-termsurvival of many species (but especially amphib-ians aquatic invertebrates and fish)

FireFire is another threat to biodiversity across SE

Asia which has been understudied despitelarge-scale issues in parts of the region such asMalaysia and Indonesia Trends in fires between1997 and 2011 show that SE Asia has the highestregional increase in fire frequency and intensityglobally at 02 (Giglio and Schroeder 2014) andfires are projected to further increase into thefuture (Kim et al 2015) Furthermore though inSE Asia these fires are largely in forest or savan-nah (about 80) in insular SE Asia over 60 offires occur in forests (Giglio et al 2013) Theimpact of these fires varies considerably acrossthe region but they are increasingly moving intonatural systems especially in the peat-swampforests of Southern SE Asia (ie 21 of land areain Borneo affected by fire between 1997 and2006 and of this 1997ndash2006 with 61 burnedrepeatedly [Langner and Siegert 2009]) Peaks infire activity have been linked to natural fluctua-tions in the ENSO cycle (Page et al 2002) for over



100 years (as the majority of droughts over thelast century are ENSO related and have beenlinked with an increased fire activity) but recentchanges in land cover have exacerbated thespread frequency and severity of fires (Pageet al 2013)

The majority of uncontrolled fires start fromhuman initiated and frequently ldquomanagedrdquo fireevents (Langner and Siegert 2009) thus strictercontrols on fire are needed to prevent futurespread of fires especially during times of drought

Changes in landcover and management havesignificantly exacerbated fire activities with thedrainage of peat-swamps in much of the South-ern SE Asia the worst culprit though conver-sions of former peat-swamp forest to tree-plantations have also led to drying of the soiland increased incidence of fire activity (Hosciloet al 2008 Spessa et al 2009) Drainage canalsbuilt to support tree-plantations activity in 1995ndash1996 have been explicitly linked to an increasefrom 24 of the land area affected by firesbetween 1973 and 1996 to 34 of the areaeffected in just 1997 an increase of almost anadditional half of the area burnt over a 23-yearperiod in a single year and almost exclusivelydue to changes in drainage (Page et al 2013)

In addition to removing areas of forest whichare frequently not adapted to surviving frequentfires (poor survival and slow regeneration[Goldammer and Seibert 1989]) fires change thestructure diversity soil and hydrology of natu-ral systems Even low-intensity fires in lowlandforests are associated with high rates of tree mor-tality especially in understory trees (Slik et al2002 Baker et al 2008) After fire occurrenceforest stands may show impaired regenerativepotential even after prolonged time periodswith a high incidence of the growth of low-diversity fire-adapted pioneer and alien speciesor ferns rather than the former diverse or ende-mic species assemblages (Woods 1989 VanNieuwstadt 2002 Cleary and Priadjati 2005Toma et al 2005 Slik et al 2008) If fires areinfrequent then forest diversity may recover intime but studies show that biomass in theseregenerated stands remains low (under 10 offormer biomass even 9 years after a fire [Hosciloet al 2008 Slik et al 2008])

Ecosystem function is also impaired signifi-cantly in post-fire forests with low levels of

recruitment and growth and often the domina-tion of non-woody plant species excluding thegrowth of trees in these areas Burning has alsobeen shown to reduce the litter seed-bank to 15and the soil seed-bank to 40 of pre-fire levels(Van Nieuwstadt 2002) and to reduce soilmicroorganism diversity and soil bacterial com-position (Syaufina and Ainuddin 2011) Ecosys-tem functions such as flooding probability andregime are also altered by fire activity (Van Eijkand Leenman 2004 Weuroosten et al 2006)Changes in forest structure and function will

have undeniable effects on animal communitiesand in addition to high mortality during the fireitself (and the low dispersal capability of manyspecies in a fragmented landscape) speciesdiversity is likely to decrease in these altered for-est patches and have a reduced chance at recolo-nization due to the fragmentation of remainingforests These further impairments of forest func-tion due to the probable loss of seed dispersersand pollinators as a direct result of fire have yetto be explored in depth but may have seriousrepercussions for a high proportion of alreadyfragmented SE Asian forestsEvidence suggests that protected areas can play

a role in protecting forests from burning as firedensity of protected areas in Myanmar was halfthat of unprotected areas (Biswas et al 2015)

PollutionWhile SE Asia is known for air-pollution

resulting from increasing industrialization andfires (ie Lin et al 2014) little research has beenconducted on the direct linkages of this hazepar-ticulate matter on terrestrial ecosystems otherthan through the deposition (to a limited extent)of heavy metals and chemicals into soil and riv-ers (Forsyth 2014) However analysis of theeffect of various forms of atmospheric pollutionon SE Asian agricultural areas reveals a high riskto many current crop types and therefore nativetypes of vegetation may be similarly at risk (Per-madi et al 2012)Studies have detected the deposition of pollu-

tant chemicals such as perfluorooctane sulfonatesin a huge taxonomic range of species but insuffi-cient evidence currently exists to explore theeffects of high concentrations of such chemicalsin animal tissues and organs (Zhao et al 2012)on long-term survival and reproduction



Rivers and waterwaysmdashAnalysis on the effectsof atmospheric pollution on marine systems hasbeen extensively discussed (ie Jaafar and Loh2014) and many of these processes are likely tobe similar for freshwater and brackish systems

Aquatic systems are more vulnerable to theeffect of pollution in many ways than terrestrialsystems especially given that many chemicalsare soluble they may easily diffuse into the tis-sues of aquatic organisms (ie Wu et al 2013)Increased levels of organic compounds (carbonnitrogen and phosphorous) in riverine systemsfrom industry and agriculture have been associ-ated with increased prevalence of algal blooms(Glibert 2014) causing high mortality to fish andother organisms and other physiological effectsincluding spontaneous abortions in aquaticmammals At present records of high mortalityof aquatic species resulting from algal bloomsare largely limited to large waterbodies in North-ern SE Asia (Glibert 2014) but with changingagricultural practices in other parts of the regionthis may become an increasing risk for otherparts of SE Asia into the future

Pollution in Asian waterways has long beendocumented to drive declines in all taxonomiclevels (ie Dudgeon 1992 Flores and Zafaralla2012 Chanpiwat and Sthiannopkao 2013) fromlarge aquatic mammals such as river dolphins toinsects and microbenthos Yet aquatic diversityand the effects of pollution have receivedremarkably little attention in recent years InNorthern SE Asia pollution has driven the lossof almost all aquatic vertebrates in at least 5 oftotal stream length with major reductions inaquatic diversity in other parts of waterways(Dudgeon 2005) and impairments of reproduc-tive ability have been noted for some species (Huet al 2009) Furthermore the concentrations oforganic and inorganic compounds from agricul-tural run-off and other forms of pollution havebeen shown to drive a shift from sensitive andspecialist species to more generalist and commonspecies within riverine systems (Choi et al 2015)

Therefore pollution and agricultural organicrun-off is likely to drive significant declines indiversity especially as additional parts of the SEAsian region industrialize but more attention isneeded to regulate industries to limit pollutionfrom agriculture industry and untreated sewageflowing into waterways The majority of SE

Asian rivers have had relatively little researchbut are likely to be increasingly at risk of pollu-tion in the future unless safeguards are imple-mented and enforced

Invasive alien speciesThe majority of aliens have entered the region

either as ornamental or agricultural crops orweeds (Peh 2010) but there is still relatively littleevidence of demonstrable impacts of invasivespecies on undisturbed terrestrial systems acrossSE AsiaAquatic systems have suffered significant

losses resulting from invasive plants causingclogging of waterways and various alien fishesthat have out-competed native species and trans-formed aquatic ecosystems (Yan et al 2001 Yonget al 2014) Snails (ie Pomacea canaliculata) havealso been found to alter regime and functioningof aquatic systems (Carlsson et al 2004)Invasive insects especially ant species (ie

Anoplolepis gracilipes and Paratrechina longicornis)are known in both natural and developed sys-tems but have rarely been found far fromhuman-modified systems Forests on margins ofagricultural and urban areas are the only knownnatural systems affected (Bos et al 2008 Wet-terer 2008) However these species are thoughtto further diminish already low diversity withintree-plantation regions (Breurouhl and Eltz 2010)Several invasive termite species (Cryptotermescynocephalus and C domesticus) are also knownwithin SE Asia but relatively few associateddeclines in biodiversity are known (Evans et al2013)Many more invasive plant species than animals

have been recorded though as with insects therehave been relatively few records in intact naturalterrestrial habitats With a small number of nota-ble exceptions (ie Lantana camara Mikaniamicrantha Mimosa pigra) few plant species havebeen found in forest habitats except in forest gapsand in the immediate vicinity of paths Howeversome non-native species (ie Acacias) show evi-dence of outcompeting native pioneer species dueto their ability to fix nitrogen (Vanna and Nang2003 Osunkoya et al 2005 Peh 2010) Howeverthese trends may be set to change as factors thatnaturally reduce the establishment of alien species(ie low light intensity and thick leaf litter) maychange upon habitat disturbance and thereby



facilitate the growth of alien species following dis-turbance in natural forests (Yeo et al 2014Nghiem et al 2013 2015) or from reduced com-petition following the extirpation of many formerspecies (Castelletta and Subaraj 2000 Brook et al2003) However examples do exist of ecosystemtransformation following the naturalization ofinvasive plant species by changing importantecosystem processes such as regeneration (ie Cli-demia hirta in forests in West Malaysia Peters2001 Peh 2010 Cronk and Fuller 2014) in addi-tion to the impact of alien species upon vulnerableisland ecosystems across the Asia-Pacific region(Corlett 2010 Meyer 2014) Furthermore initia-tives such as ldquoflower stripsrdquo being implementedin some parts of Asia (A C Hughes personal obs-ervation) to stabilize land and provide pollinationservices (Westphal et al 2015) also have thepotential to facilitate the spread of invasive spe-cies into neighboring natural systems if plants arechosen on the basis of attractiveness rather thanservice provision Vertebrate invaders have notbeen tied to the decline or extinction of manynative species though the potential for competi-tion and hybridization have both been docu-mented (Peh 2010) However the repeated andpoorly regulated release of non-native species aspart of Buddhist prayer ceremonies has the poten-tial to spread invasive species and the risk of dis-ease across SE Asia (Severinghaus and Chi 1999Liu et al 2012)

Invasives have the potential to become anincreasing threat to biodiversity in an increas-ingly fragmented landscape and through everincreasing propagule pressure reduced redun-dancy in ecosystems and novel climates Thoughat present with a few exceptions invasive alienspecies have not been linked to reductions innative biodiversity they require monitoring andregulation to prevent the development of issuesin the future

DiseaseDiseases are not a well-known threat to SE

Asian biodiversity despite the number of pan-demics that have originated in Asia in recent years(Coker et al 2011) Chytrid virus (Batrachochytriumdestructans) has however been confirmed in mar-ket populations and wild populations at lowlevels in countries across SE Asia (wwwbd-mapsnet) though data suggest that chytrid has been

present in at least parts of Asia for over 100 years(Bai et al 2012 Fong et al 2015) and has not beenassociated with large-scale declines and evidenceof adaptations to reduce the impact of the virushas also been detected in wild Asian amphibianpopulations (Harris et al 2009) Spread of bothchytrid virus and ranavirus has been associatedwith markets and farmed animals and the waterthey are kept and transported in (Bai et al 2012Gilbert et al 2012 Kolby et al 2014) and morestringent regulations may be necessary to preventthe possibility of future emergent diseases (Schloe-gel et al 2012 Liu et al 2013) A similar virus hasbeen detected in Caudata (B salamandrivorans)but has also not been associated with high deathrates in Asia at this point in time and is alsothought to have originated in Asia (Martel et al2014)Ranavirus however has been associated with

higher rates of mortality in wild populations(Kanchanakhan 2011) but further research isneeded to assess the level of threat posed to wildamphibian populations Ranavirus has alsocaused high rates of death in some farmedamphibians (Meng et al 2014) which could posea huge threat to native species in the wild with-out strict control Species currently at threatinclude the giant salamander (Dong et al 2011Zhou et al 2013) which showed a 95 mortalityrate in mesocosms designed to breed populationsof this already endangered speciesSeveral diseases of freshwater fishes are

already associated with variable mortality levelsacross SE Asia (Tompkins et al 2015) largely asa result of trade Other taxa are not currentlyknown to suffer high mortality levels as a resultof disease but other species (especially planttaxa) may be susceptible to diseases especiallythose transported into Asia for commercial rea-sons from elsewhere

Climate changeClimate change is frequently cited by scientists

from outside the SE Asian region as the greatestthreat to terrestrial biodiversity Yet here climatechange is listed last because it can only affectspecies that are able to survive the effects of habi-tat loss and degradation hunting other forms ofhabitat modification and the other factors listedabove This is not to say that it is not of concernand that people should not act to prevent the loss



of species resulting from former habitats becom-ing unsuitable from climate change but it shouldnot be the most immediate concern and shouldbe dealt with using methods that also deal withmore immediate concerns (ie connecting thelandscape) The effects of greenhouse gas emis-sions alone may also alter ecosystems for exam-ple CO2 fertilization in some native ecosystemsthereby causing changes to productivity bio-mass and community assemblage and structure(Hickler et al 2015) though this depends onother conditions and nutrient availability (Oishiet al 2014)

Projections show increases in mean tempera-ture variability and the potential for extreme cli-matic events (Hijioka et al 2014) yet relativelylittle long-term data exists to document bioticresponses to climate change across tropical SEAsia Predictive analyses show the potential for asignificant loss of species and shrinking range-sizes (ie Menon et al 2009 Li et al 2010Klorvuttimontara et al 2011 Hughes et al 2012Ko et al 2012) and these losses may be exacer-bated by changes in the timings of various bioticpatterns causing asynchronies that may impacton any species reliant on seasonal events (Kris-tensen et al 2015) The ability to disperse is likelyto be key to ensure the retention of species underclimatic change and especially on elevationalgradients (Chen et al 2011 Harris et al 2014)where species are more likely to be able to ldquotrackclimate changerdquo due to the rapid spatial gradientof temperature change over short distances (Cor-lett and Westcott 2013) Biome shifts as a result ofchanging climate and changes in various impor-tant ecosystem functions are also likely to havesignificant effects on remaining regions of intactnatural vegetation (Choi et al 2011) and meansthat protecting natural ldquoclimate refugiardquo whichmay remain more thermally stable as a result oftopographic buffering may be essential to pre-serve current species assemblages in someregions (Suggitt et al 2011)

Some ecosystems such as karsts may be espe-cially vulnerable to climatic change and poten-tially desertification (Anderson and Ferree 2010Zhang et al 2010a b) which may alter the spe-cies assemblage able to survive on the karst andchange the proportion of tree species with differ-ent degrees of drought tolerance (Fu et al 2012)Ecosystems that are fragmented (either naturally

or as a result of habitat destruction) are likely tobe most at risk at climate change-induced specieslosses as species unable to survive changes in cli-mate may become regionally extinct if unable todisperse and other species may not be able totravel through the matrix to reach such frag-ments Though reduced competitive pressurefrom incomers may occur in fragmented land-scapes the interaction of competition and rela-tive fitness compared to absolute tolerance indetermining species range boundaries is poorlyknown and thus the impact of climate changeon isolated fragments is difficult to ascertain atpresentThe most important components of climatic

change are likely to be changes in seasonalityand potentially drought as the region is alreadywater-limited and water-stressed (Zhang et al2016) The impact of drought on forest ecosys-tems is still poorly understood but is known toalter leaf chemistry and mortality rates in treesand is therefore likely to alter community com-position (Allen et al 2015 Schlesinger et al2015) Recovery following droughts may take upto several years (Anderegg et al 2015) thus inwater-limited regions across SE Asia increasingdrought frequency may permanently alterecosystems (Bennett et al 2015) Water-stressedforests across the region in addition to higheraltitude regions may be most vulnerable (Zomeret al 2016) Climatic change is also likely to alterfire regimes especially if biomes have becomedryerThus though climate change represents a les-

ser threat to the short-term survival of species itsimpacts are also the least easy to understand asthe interaction between the availability of mois-ture and varying temperature may have very dif-ferent effects at the ecosystem and species leveland vary dramatically between different speciesand systems

CONCLUSIONS

1 SE Asia has frequently been overlooked inglobal discourse on threats to biodiversity andonly in recent years have the most pertinentissues such as trade and deforestation garneredthe global attention they deserve Other issuesare rarely mentioned and even on a regionalbasis are regularly ignored in the wake of the



most significant drivers of biodiversity lossNone of these issues are simple and thus as glo-bal citizens and societies we must act to reducetheir effects through sensible and stratified con-servation measures across different timescalesto address the multifaceted problems that facethe region However none of the above ten majorissues is insoluble and though there are no pana-ceas even climate change can be mitigated to adegree by sensible conservation planning andthe preservation of connectivity and regional cli-mate refugia

2 There are no ecosystems or species that areimmune from the ever increasing threats tobiodiversity across the SE Asian region Manyhabitats such as forests mangroves karsts andstreams are likely to be considerably reducedin size and conditions due to the insatiableglobal demand for timber cement palm oil andrubber and the regional need for electricity (viadam construction) Protected areas may sufferencroachment and are not immune from climatechange or from fire which threatens to trans-form landscapes alter processes of regeneration(and regional climate) and provide a conduit forinvasive species Even in those protected andremaining habitat patches hunting and trade arestill issues that are difficult to tackle especiallyfor high-value animals which may be targetedby increasingly sophisticated international crimi-nal-networks

3 For many species there are no availablebaseline data to examine trends yet by combiningthe available data with the latest tools providesthe means that exist to prioritize regions forprotection and identify gaps of endemism andhighest biodiversity These regions need to beidentified and protected as a matter of urgencyespecially in regions such as Cambodia Indone-sia and Myanmar which are currently sufferingthe highest rates of deforestation (Cambodia220 Indonesia 203 Myanmar 190 FAO2011) Once priority areas are identified then fur-ther developments have a basis which to plan andmitigate for

4 Enforcement remains the major issue andeven countries with existing ldquolawsrdquo against issuessuch as poaching (ie Vietnam Ngoc and Wyatt2013) require enforcement Overarching agree-ments and possibly international sanctions suchas stopping subsidies or freezing international

loans may be required to externally enforce theimportance of maintaining and protecting criticalareas for biodiversity Mechanisms such asREDD+ and programs such as ldquoGrain for Greenrdquowithin China could also work harder to includebetter metrics for ensuring the retention of biodi-versity which is frequently either lacking or insuf-ficiently incorporated at present meaning thatthese strategies may damage rather than protectbiodiversity5 Technologies and platforms now exist to

detect and report environmental crimes of alltypes but this information needs to be dissemi-nated in effectively and acted upon within coun-tries to make committing environmental crimesharder and punishments more severe Interna-tional pressure using sanctions and rewardsthrough international treaties protocols andagreements may be what is required to ensurethat enforcement really is on the agenda of coun-tries through the region but that assistance inbuilding the networks and infrastructure todetect illegal actions are also in place and avail-able to these countries6 The prognosis for much of SE Asian biodi-

versity is poor and international interventionsmay be needed to lend credence and strength tosustainability mandates to share relevant datatechnologies and good practice Monitoring ofall animal and plant trade needs better licensingand management to protect endangered speciesand prevent the future spread of disease (ie Bdestructans)7 Without dramatic and immediate changes in

focus to change policy and practice then thelosses of many species (except those generalistenough to co-habit with humans or tolerate atransformed landscape) and dominated by earlysuccessional and alien species are likely Singa-pore represents an area in which almostnowhere has not been modified by human activ-ity and Java is almost facing the same situationand as a result both have lost a significant num-ber of native species These microcosms may rep-resent a SE Asian future and one that becomesincreasingly probable without better environ-mental safeguards and standards and enforce-ment to ensure that SE Asian species andsystems that exist today can persist and adaptinto the future without exponential losses ofcurrent species



ACKNOWLEDGMENTS

I would like to thank Richard Corlett and StuartPimm for interesting discussions and support on ear-lier versions of this manuscript I also thank thereviewers for their comments on an earlier draft of thismanuscript

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Afroz R M M Masud R Akhtar and J B Duasa2014 Water pollution challenges and future direc-tion for water resource management policies inMalaysia Environment and Urbanization Asia563ndash81

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Allen C D D D Breshears and N G McDowell2015 On underestimation of global vulnerability totree mortality and forest die-off from hotterdrought in the Anthropocene Ecosphere 61ndash55

Amlin G M N Suratman and N N M Isa 2014Soil chemical analysis of secondary forest 30 yearsafter logging activities at Krau Wildlife ReservePahang Malaysia APCBEE Procedia 975ndash81

Anderegg W R C Schwalm F Biondi J J CamareroG Koch M Litvak and A Wolf 2015 Pervasivedrought legacies in forest ecosystems and theirimplications for carbon cycle models Science349528ndash532

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Andres P and E Mateos 2006 Soil mesofaunal res-ponses to post-mining restoration treatments App-lied Soil Ecology 3367ndash78

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Bagchi R C D Philipson E M Slade A HectorS Phillips J F Villanueva and M C Press 2011Impacts of logging on density-dependent predation

of dipterocarp seeds in a South East Asian rain-forest Philosophical Transactions of the Royal Soci-ety B 3663246ndash3255

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Bai Y B Jiang M Wang H Li J M Alatalo andS Huang 2016 New ecological redline policy(ERP) to secure ecosystem services in China LandUse Policy 55348ndash351

Bai C X Liu M C Fisher T W Garner and Y Li2012 Global and endemic Asian lineages of theemerging pathogenic fungus Batrachochytrium den-drobatidis widely infect amphibians in ChinaDiversity and Distributions 18307ndash318

Baker P J S Bunyavejchewin and A R Robinson2008 The impacts of large-scale low-intensity fireson the forests of continental South-east Asia Inter-national Journal of Wildland Fire 17782ndash792

Baker S E R Cain F Van Kesteren Z A ZommersN Drsquocruze and D W Macdonald 2013 Roughtrade animal welfare in the global wildlife tradeBioScience 63928ndash938

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Barros N J J Cole L J Tranvik Y T Prairie D Bastvi-ken V L Huszar and F Rol 2011 Carbon emissionfrom hydroelectric reservoirs linked to reservoirage and latitude Nature Geoscience 4593ndash596

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Bennett E L 2015 Legal ivory trade in a corruptworld and its impact on African elephant popula-tions Conservation Biology 2954ndash60



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Botzat A L K Fischer and I Kowarik 2016 Unex-ploited opportunities in understanding liveableand biodiverse cities a review on urban biodiver-sity perception and valuation Global Environmen-tal Change 39220ndash233

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Brown R S A H Colotelo B D Pflugrath C ABoys L J Baumgartner Z D Deng and D Sing-hanouvong 2014 Understanding barotrauma infish passing hydro structures a global strategy forsustainable development of water resources Fish-eries 39108ndash122

Breurouhl C A and T Eltz 2010 Fuelling the biodiversitycrisis species loss of ground-dwelling forest ants inoil palm plantations in Sabah Malaysia (Borneo)Biodiversity and Conservation 19519ndash529

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Burivalova Z T M Lee X Giam C H SekerciogluD S Wilcove and L P Koh 2015 Avian responsesto selective logging shaped by species traits andlogging practices Proceedings of the Royal Societyof Biology 28220150164

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Cao S and L Yu 2009 Impact of Chinarsquos Grain forGreen Project on the landscape of vulnerable aridand semi-arid agricultural regions a case study innorthern Shaanxi Province Journal of AppliedEcology 46536ndash543

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climate warming Global Ecology and Biogeogra-phy 2034ndash45

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Choi J W J H Han C S Park D G Ko H I KangJ Y Kim and K G An 2015 Nutrients and ses-tonic chlorophyll dynamics in Asian lotic ecosys-tems and ecological stream health in relation toland-use patterns and water chemistry EcologicalEngineering 7915ndash31

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Cleary D F R and A Priadjati 2005 Vegetationresponses to burning in a rain forest in BorneoPlant Ecology 177145ndash163

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Clements R P K Ng X X Lu S Ambu M Schilthui-zen and C J Bradshaw 2008 Using biogeographi-cal patterns of endemic land snails to improveconservation planning for limestone karsts Biolog-ical Conservation 1412751ndash2764

Coghlan M L 2014 Development of new moleculartechniques for wildlife forensic applications Dis-sertation Murdoch University httpresearchrepositorymurdocheduau23045

Coker R J B M Hunter J W Rudge M Liveraniand P Hanvoravongchai 2011 Emerging infec-tious diseases in Southeast Asia regional chal-lenges to control Lancet 377599ndash609

Conklin J R Y I Verkuil and B Smith 2014 Priori-tizing migratory shorebirds for conservation actionon the East Asian-Australasian Flyway WWF-Hong Kong Hong Kong

Corlett R T 2007 The impact of hunting on the mam-malian fauna of tropical Asian forests Biotropica39292ndash303

Corlett R T 2010 Invasive aliens on tropical EastAsian islands Biodiversity and Conservation19411ndash423

Corlett R T and D Westcott 2013 Will plant move-ments keep up with climate change Trends inEcology and Evolution 28482ndash488

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Dang K T 2012 Reducing emissions from deforesta-tion and forest degradation (redd1) implementa-tion issues for lower Mekong subregion Trends inEcology and Evolution 25396ndash402

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Davidson N C 2014 How much wetland has theworld lost Long-term and recent trends in globalwetland area Marine and Freshwater Research65934ndash941

Day M J and P B Urich 2000 An assessment of pro-tected karst landscapes in Southeast Asia Caveand Karst Science 2761ndash70

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Delany S and D Scott 2006 Waterbird populationestimates Fourth edition Wetlands InternationalWageningen The Netherlands

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Dommain R J Couwenberg and H Joosten 2010Hydrological self-regulation of domed peatlands insouth-east Asia and consequences for conservationand restoration Mires and Peat 61ndash17

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Drury R 2011 Hungry for success urban consumerdemand for wild animal products in VietnamConservation and Society 9247

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Dudgeon D 2011 Asian river fishes in the Anthro-pocene threats and conservation challenges in anera of rapid environmental change Journal of FishBiology 791487ndash1524

Dudgeon D et al 2006 Freshwater biodiversityimportance threats status and conservation chal-lenges Biological Reviews 81163ndash182

Duke N C J O Meynecke S Dittmann A M EllisonK Anger U Berger and F Dahdouh-Guebas 2007Aworld without mangroves Science 31741ndash42

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Economist 2012 httpwwweconomistcomblogsbanyan201207mekong-river

Economist Asia 2013a httpwwweconomistcomnewsasia21565676-laos-admits-work-going-ahead-controversial-dam-river-elegy

Economist Asia 2013b httpwwweconomistcomnewsasia21585000-dam-takes-shape-fierce-opposition-continues-fish-friendly

Economist Asia 2014 httpwwweconomistcomnewsasia21636978-laoss-neighbours-may-not-its-plans-dam-mekong-they-can-do-little-about-it-unquiet-grows

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Wilcove 2010 Wildlife-friendly oil palm planta-tions fail to protect biodiversity effectively Conser-vation Letters 3236ndash242

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Elmqvist T W Zipperer and B Geurouneralp 2016 Urb-anization habitat loss biodiversity decline solu-tion pathways to break the cycle Pages 139ndash151 inK Seta W D Solecki and C A Griffith editorsRoutledge handbook of urbanization and globalenvironmental change Routledge London UK

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Fisher C and P Mehta 2014 httpmeetingsapsorglinkBAPS2014MARF107



Fishman A 2014 Understanding lsquodeforestation-freersquothe state of play and issues to consider duringTFDrsquos October 2014 dialogue The Forests Dia-logue New Haven Connecticut USA httptheforestsdialogueorgsitesdefaultfilesfilesUnderstaning20Deforestation-Free_background_Finalpdf

Flores M J L and M T Zafaralla 2012 Macroinver-tebrate composition diversity and richness in rela-tion to the water quality status of Mananga RiverCebu Philippines Philippine Science Letters 5103ndash113

Fong J J T L Cheng A Bataille A P PessierB Waldman and V T Vredenburg 2015 Early1900s detection of Batrachochytrium dendrobatidis inKorean amphibians PLoS One 10e0115656

Forsyth T 2014 Sustainable land use and rural devel-opment in Southeast Asia innovations and policiesfor mountainous areas Mountain Research andDevelopment 3476ndash77

Fox J and J C Castella 2013 Expansion of rubber(Hevea brasiliensis) in Mainland Southeast AsiaWhat are the prospects for smallholders Journal ofPeasant Studies 40155ndash170

Fox J J C Castella A D Ziegler and S B Westley2014 Rubber plantations expand in mountainousSoutheast Asia What are the consequences for theenvironment AsiaPacific Issues 1141ndash8

Francis C M A V Borisenko and N V Ivanova2010 The role of DNA barcodes in understandingand conservation of mammal diversity in South-east Asia PLoS One 5e12575

Frechette A 2013 External review of Phase II of theIUCN-Holcim agreement final report IUCNhttpcmsdataiucnorgdownloadsreview_of_phase_ii_iucn_holcim_agreement___final_report__1__1pdf

Fu P L Y J Jiang A Y Wang T J Brodribb J LZhang S D Zhu and K F Cao 2012 Stemhydraulic traits and leaf water-stress tolerance areco-ordinated with the leaf phenology of angios-perm trees in an Asian tropical dry karst forestAnnals of Botany 110189ndash199

Gabriel G N Hua and J Wang 2012 Making a kill-ing a 2011 survey of ivory markets in China Inter-national Fund for Animal Welfare China

Gao Y and S G Clark 2014 Elephant ivory trade inChina trends and drivers Biological Conservation18023ndash30

Geissmann T F Momberg and T Whitten 2012Rhinopithecus strykeri The IUCN Red List ofThreatened Species Version 2014 3 wwwiucnredlistorg

Gerber J F 2011 Conflicts over industrial tree planta-tions in the South Who how and why GlobalEnvironmental Change 21165ndash176

Giambelluca T W R G Mudd W Liu A D ZieglerN Kobayashi T O Kumagai and S Yin 2016Evapotranspiration of rubber (Hevea brasiliensis)cultivated at two plantation sites in Southeast AsiaWater Resources Research 2660ndash679

Gibbs H K A S Ruesch F Achard M K ClaytonP Holmgren N Ramankutty and J A Foley 2010Tropical forests were the primary sources of newagricultural land in the 1980s and 1990s Proceed-ings of the National Academy of Sciences USA 10716732ndash16737

Gibson L A J Lynam C J Bradshaw F He D PBickford D S Woodruff and W F Laurance 2013Near-complete extinction of native small mammalfauna 25 years after forest fragmentation Science3411508ndash1510

Giglio L J T Randerson and G R Werf 2013Analysis of daily monthly and annual burned areausing the fourth-generation global fire emissionsdatabase (GFED4) Journal of Geophysical ResearchBiogeosciences 118317ndash328

Giglio L and W Schroeder 2014 A global feasibilityassessment of the bi-spectral fire temperature andarea retrieval using MODIS data Remote Sensingof Environment 152166ndash173

Gilbert M D Bickford L Clark A Johnson P HJoyner L O Keatts and T A Seimon 2012Amphibian pathogens in Southeast Asian frogtrade EcoHealth 9386ndash398

Giri C E Ochieng L L Tieszen Z Zhu A SinghT Loveland J Masek and N Duke 2011 Statusand distribution of mangrove forests of the worldusing earth observation satellite data Global Ecol-ogy and Biogeography 20154ndash159

Giri C Z Zhu L L Tieszen A Singh S Gillette andJ A Kelmelis 2008 Mangrove forest distributionsand dynamics (1975ndash2005) of the tsunami-affectedregion of Asia Journal of Biogeography 35519ndash528

Glibert P M 2014 Harmful algal blooms in Asia aninsidious and escalating water pollution phe-nomenon with effects on ecological and humanhealth ASIANetwork Exchange A Journal forAsian Studies in the Liberal Arts 2152ndash68

Global Witness 2004 Cambodian government autho-rises clear-cutting in National Park 6 July

Global Witness 2013 Sarawakrsquos forests myths ampreality httpswwwglobalwitnessorgsitesdefaultfileslibrarySarawak20myths20and20realitydocpdf

Glover A M and J D Altringham 2008 Cave selec-tion and use by swarming bat species BiologicalConservation 1411493ndash1504

Goldammer J G and B Seibert 1989 Natural rain-forest fires in Eastern Borneo during the Pleistoceneand Holocene Naturwissenschaften 76518ndash520



Gopal B 2013 Future of wetlands in tropical and sub-tropical Asia especially in the face of climatechange Aquatic Sciences 7539ndash61

Gouyon A 2003 Eco-certification as an incentive toconserve biodiversity in rubber smallholder agro-forestry systems a preliminary study World Agro-forestry Centre - ICRAF SEA Regional OfficeBogor Indonesia p 58

Geurouneralp B and K C Seto 2013 Futures of globalurban expansion uncertainties and implications forbiodiversity conservation Environmental ResearchLetters 8014025

Hall D 2003 The international political ecology ofindustrial shrimp aquaculture and industrial plan-tation forestry in Southeast Asia Journal of South-east Asian Studies 34251ndash264

Hamilton R L M Trimmer C Bradley and G Pinay2016 Deforestation for oil palm alters the funda-mental balance of the soil N cycle Soil Biology andBiochemistry 95223ndash232

Hance J 2015 Scientists identify frog through DNAwithout leaving forest httpnewsmongabaycom20150505-hance-expedition-genomics-labhtml

Hancock G and G Laycock 2010 Organised crimeand crime scripts prospects for disruption Pages172ndash193 in K Bullock R V Clarke and N Tilleyeditors Situational prevention of organised crimesWillan Publishing London England UK

Harris R N R M Brucker J B Walke M H BeckerC R Schwantes D C Flaherty and K P Minbiole2009 Skin microbes on frogs prevent morbidityand mortality caused by a lethal skin fungus ISMEJournal 3818ndash824

Harris J B C D DwiPutra S D Gregory B WBrook D M Prawiradilaga N S Sodhi and D AFordham 2014 Rapid deforestation threatens mid-elevational endemic birds but climate change ismost important at higher elevations Diversity andDistributions 20773ndash785

Harrison R D 2011 Emptying the forest hunting andthe extirpation of wildlife from tropical naturereserves BioScience 61919ndash924

Harvey C A B Dickson and C Kormos 2010Opportunities for achieving biodiversity conserva-tion through REDD Conservation Letters 353ndash61

Heino M M Kummu M Makkonen M MulliganP H Verburg M Jalava and T A Reuroaseuroanen 2015Forest loss in protected areas and intact forest land-scapes a global analysis PLoS One 10e0138918

Herbig J 2010 The illegal reptile trade as a form ofconservation crime a South African criminologicalinvestigation Pages 110ndash131 in R White editorGlobal Environmental Harm Criminological Per-spectives Willan Publishing Portland OregonUSA

Hett C J C Castella A Heinimann P Messerli andJ L Pfund 2012 A landscape mosaics approachfor characterizing swidden systems from a REDD+perspective Applied Geography 32608ndash618

Hickler T A Rammig and C Werner 2015 Model-ling CO2 impacts on forest productivity CurrentForestry Reports 169ndash80

Hijioka Y E Lin J J Pereira R T Corlett X CuiG E Insarov R D Lasco E Lindgren andA Surjan 2014 Asia In Climate change 2014impacts adaptation and vulnerability Part Bregional aspects Contribution of Working Group IIto the Fifth Assessment Report of the Intergovern-mental Panel on Climate Change Cambridge Uni-versity Press Cambridge United Kingdom andNew York New York USA pp 1ndash32

Hong P N 2003 Mangrove forests in Vietnammdashpresent status and challenges InternationalSymposium on Conservation and Wise Use ofMangroves in Southeast Asia Brunei Darussalam6ndash8 October 2003 Forestry Department of BruneiDarussalam University Brunei Darussalam Bru-nei and the Ramsar Center Japan Tokyo Japan

Hosaka T M Niino M Kon T Ochi T YamadaC Fletcher and T Okuda 2014 Effects of loggingroad networks on the ecological functions of dungbeetles in Peninsular Malaysia Forest Ecology andManagement 32618ndash24

Hoscilo A S E Page and K J Tansey 2008 Develop-ment of post-fire vegetation in the tropical ecosys-tem of Central Kalimantan Indonesia Pages 202ndash205 in J H M Weuroosten J O Rieley and S E Pageeditors Restoration of tropical peatlands Alterra -Wageningen University and Research Centre andthe EU INCO ndash RESTORPEAT Partnership Wagen-ingen The Netherlands

Hu J Z Zhang Q Wei H Zhen Y Zhao H Pengand B Zhang 2009 Malformations of the endan-gered Chinese sturgeon Acipenser sinensis and itscausal agent Proceedings of the National Acad-emy of Sciences USA 1069339ndash9344

Huang Z L 2001 Biodiversity conservation forthe Three Gorges Project Biodiversity Science 9472ndash481

Hughes A C 2012 Mapping a future for SoutheastAsian biodiversity httpwwwintechopencombookszoologymapping-a-future-for-southeast-asian-biodiversity

Hughes A C C Satasook P J J Bates S Bum-rungsri and G Jones 2012 The projected effects ofclimatic and vegetation changes on the distributionand diversity of Southeast Asian bats GlobalChange Biology 181854ndash1865

Ilman M P Dargusch and P Dart 2016 A historicalanalysis of the drivers of loss and degradation



of Indonesiarsquos mangroves Land Use Policy 54448ndash459

Imboden C D Gross P J Meynell D Richards andM Stalmans 2010 Biodiversity management sys-tem proposal for the integrated management ofbiodiversity at Holcim Sites IUCN GenevaSwitzerland

Ismail R 2014 Southeast Asian urbanisation and thechallenge to sustainability implications for theenvironment and health Environmental Policy andLaw 4455

Jaafar Z and T-L Loh 2014 Linking land air andsea potential impacts of biomass burning and theresultant haze on marine ecosystems of SoutheastAsia Global Change Biology 202701ndash2707

Jenkins P D C W Kilpatrick M F Robinson andR J Timmins 2004 Morphological and molecularinvestigations of a new family genus and species ofrodent (Mammalia Rodentia Hystricognatha) fromLao PDR Systematics and Biodiversity 2419ndash454

Johnson R N L Wilson-Wilde and A Linacre 2014Current and future directions of DNA in wildlifeforensic science Forensic Science InternationalGenetics 101ndash11

Kanchanakhan 2011 Ranaviruses in frogs and fish inSoutheast Asia 2011 Joint Meeting (JMIH) Min-neapolis Minnesota USA

Kennedy S 2014 Eco-certification of natural rubberdemand supply and potential implications of pri-vate global environmental governance CriticalPlanning 2183ndash96

Khai T C N Mizoue T Kajisa T Ota andS Yoshida 2016 Stand structure composition andillegal logging in selectively logged production for-ests of Myanmar comparison of two compart-ments subject to different cutting frequency GlobalEcology and Conservation 7132ndash140

Kill J S Ozinga S Pavett and R Wainwright 2010Trading carbon How it works and why it is con-troversial Fern The Netherlands

Kim P S D J Jacob L J Mickley S N Koplitz M EMarlier R S DeFries and Y H Mao 2015Sensitivity of population smoke exposure to firelocations in Equatorial Asia Atmospheric Environ-ment 10211ndash17

Kingston T 2010 Research priorities for bat conserva-tion in Southeast Asia a consensus approach Bio-diversity and Conservation 19471ndash484

Kirby J S A J Stattersfield S H Butchart M IEvans R F Grimmett V R Jones and I Newton2008 Key conservation issues for migratory land-and waterbird species on the worldrsquos majorflyways Bird Conservation International 18S49

Kirchherr J K J Charles and M J Walton 2016Multi-causal pathways of public opposition to dam

projects in Asia a fuzzy set qualitative comparativeanalysis (fsQCA) Global Environmental Change4133ndash45

Klorvuttimontara S C J McClean and J K Hill2011 Evaluating the effectiveness of protectedareas for conserving tropical forest butterflies ofThailand Biological Conservation 1442534ndash2540

Ko C Y T L Root S H Lin S H Schneider andP F Lee 2012 Global change projections for Tai-wan island birds linking current and future distri-butions Nature Conservation 221ndash40

Koh L P P Levang and J Ghazoul 2009 Designerlandscapes for sustainable biofuels Trends in Ecol-ogy and Evolution 24431ndash438

Kolby J E K M Smith L Berger W B KareshA Preston A P Pessier and L F Skerratt 2014First evidence of amphibian chytrid fungus (Batra-chochytrium dendrobatidis) and ranavirus in HongKong amphibian trade PLoS One 9e90750

Kretser H E R Wong S Roberton C PershynJ Huang F Sun and P Zahler 2014 Mobile deci-sion-tree tool technology as a means to detect wild-life crimes and build enforcement networksBiological Conservation httpsdoiorg101016jbiocon08018

Kristensen N P J Johansson J Ripa and N Jonzen2015 Phenology of two interdependent traits inmigratory birds in response to climate change Pro-ceedings of the Royal Society B 28220150288

Lafarge 2014 httpwwwlafargecom22052014_Lafarge_Biodivesrity_Strategy-ukpdf

Lang C 2002 The pulp invasion the international pulpand paper industry in the Mekong region WorldRainforest Movement Montevideo Uruguay

Lang C 2008 Plantations poverty and power Eur-opersquos role in the expansion of the pulp industry inthe South World Rainforest Movement Montev-ideo Uruguay

Langner A and F Siegert 2009 Spatiotemporal fireoccurrence in Borneo over a period of 10 yearsGlobal Change Biology 1548ndash62

Latinne A S Waengsothorn V Herbreteau and J RMichaux 2011 Evidence of complex phylogeo-graphic structure for the threatened rodent Leopol-damys neilli in Southeast Asia ConservationGenetics 121495ndash1511

Laurance W F G R Clements S Sloan C S OrsquoCon-nell N D Mueller M Goosem and I B Arrea2014 A global strategy for road building Nature513229ndash232

Lavorgna A 2014 Wildlife trafficking in the internetage Crime Science 31ndash12

Lavorgna A 2015 The social organization of pet traf-ficking in cyberspace European Journal on Crimi-nal Policy and Research 211ndash18



Lehner B et al 2011 High-resolution mapping of theworldrsquos reservoirs and dams for sustainable river-flow management Frontiers in Ecology and theEnvironment 9494ndash502

Li R H Tian and X Li 2010 Climate changeinduced range shifts of Galliformes in China Inte-grative Zoology 5154ndash163

Li K C Zhu L Wu and L Huang 2013 Problemscaused by the Three Gorges Dam construction inthe Yangtze River basin a review EnvironmentalReviews 21127ndash135

Lima J R U Galatti C J Lima S B Faveri H LVasconcelos and S Neckel-Oliveira 2015 Amphi-bians on Amazonian land-bridge islands areaffected more by area than isolation Biotropica47369ndash376

Lima I B F M Ramos L A Bambace and R RRosa 2008 Methane emissions from large dams asrenewable energy resources a developing nationperspective Mitigation and Adaptation Strategiesfor Global Change 13193ndash206

Lin J D Pan S J Davis Q Zhang K He C Wangand D Guan 2014 Chinarsquos international tradeand air pollution in the United States Proceedingsof the National Academy of Sciences USA 1111736ndash1741

Liu B C Chen Y Lian J Chen and X Chen 2015Long-term change of wet and dry climatic condi-tions in the southwest karst area of China Globaland Planetary Change 1271ndash11

Liu X M E McGarrity and Y Li 2012 The influenceof traditional Buddhist wildlife release on biologi-cal invasions Conservation Letters 5107ndash114

Liu X J R Rohr and Y Li 2013 Climate vegetationintroduced hosts and trade shape a global wildlifepandemic Proceedings of the Royal Society B28020122506

Lu J K Bayne and J Wang 2013 Current status ofanimal welfare and animal rights in China Alter-natives to Laboratory Animals ATLA 41351ndash357

Leurou Y Z Ma L Zhang B Fu and G Gao 2013 Redli-nes for the greening of China EnvironmentalScience and Policy 33346ndash353

Lucey J M N Tawatao M J Senior V K CheyS Benedick K C Hamer and J K Hill 2014 Trop-ical forest fragments contribute to species richnessin adjacent oil palm plantations Biological Conser-vation 169268ndash276

Luo J Y D Yan J Y Song D Zhang X Y XingY M Han and X H Xiao 2013 A strategy fortrade monitoring and substitution of the organs ofthreatened animals Scientific Reports 33108

Lyons J A and D J D Natusch 2011 Wildlife laun-dering through breeding farms illegal harvestpopulation declines and a means of regulating the

trade of green pythons (Morelia viridis) fromIndonesia Biological Conservation 1443073ndash3081

Ma X X Lu M van Noordwijk J T Li and J C Xu2014 Attribution of climate change vegetationrestoration and engineering measures to thereduction of suspended sediment in the Kejiecatchment southwest China Hydrological EarthSystem Science 181979ndash1994

Majer J D 2014 Mining and biodiversity Are theycompatible Pages 195ndash205 in M BruecknerA Durey R Mayes and C Pforr editors Resourcecurse or cure Springer Berlin Germany

Marks D A Sirithet A Rakyuttitham S WulariS Chomchan and P Samranjit 2015 Land grabbingand impacts to small scale farmers in Southeast Asiasub-region Paper series of the Conference Pro-gramme of the International Institute of Social Stud-ies in The Hague wwwlandactionthaiorg

Maron M R J Hobbs A Moilanen J W MatthewsK Christie T A Gardner and C A McAlpine2012 Faustian bargains Restoration realities in thecontext of biodiversity offset policies BiologicalConservation 155141ndash148

Martel A M Blooi C Adriaensen P Van RooijW Beukema M C Fisher and F Pasmans 2014Recent introduction of a chytrid fungus endangersWestern Palearctic salamanders Science 346630ndash631

Martin P A A Newton M Pfeifer M Khoo andJ Bullock 2015 The effects of reduced impact log-ging and logging intensity on stand damage bio-mass loss and tree species richness in tropical forestsa meta-analysis PeerJ PrePrints 3e1046

Maryati S H Shimada T Sasaoka A HamanakaK Matsui and H Nagawa 2012 GIS databasetemplate for environmental management of miningin Indonesia Journal of Geographic InformationSystem 417071

McCarthy S 2014 Norm diffusion and the limits toforestry governance reform in Southeast Asiarsquosnew democracies Pacific Review 27755ndash778

McDonald R I P Kareiva and R T Forman 2008 Theimplications of current and future urbanization forglobal protected areas and biodiversity conserva-tion Biological Conservation 1411695ndash1703

Meng Y J Ma N Jiang L B Zeng and H B Xiao2014 Pathological and microbiological findingsfrom mortality of the Chinese giant salamander(Andrias davidianus) Archives of Virology 1591403ndash1412

Menon S M Z Islam and A T Peterson 2009 Pro-jected climate change effects on nuthatch distribu-tion and diversity across Asia Raffles Bulletin ofZoology 57569ndash575

MEP 2000 Bulletin on the ecological and environmen-tal monitoring results of the Three Gorges Project



1999 httpjcsmepgovcnhjzlsxgb1999200211t20021117_83203htm

MEP 2001 Bulletin on the ecological and environmen-tal monitoring results of the Three Gorges Project2000 httpjcsmepgovcnhjzl

MEP 2009 Bulletin on the ecological and environmen-tal monitoring results of the Three Gorges Project2009 httpenglishmepgovcndown_loadDocuments201002P020100225376514651439pdf

Meyer J Y 2014 Critical issues and new challengesfor the research and management of invasiveplants in the Pacific Islands Pacific ConservationBiology 20146ndash164

Meyer C S Schmidt B Meyer K Schlegelmilch andM Schlereth 2009 Environmentally harmful subsi-dies How perverse financial incentives threatenbiodiversity Green Budget Germany MunichGermany

Michinaka T M Miyamoto Y Yokota H SokhS Lao and V Ma 2013 Factors affecting forestarea changes in Cambodia an econometricapproach Journal of Sustainable Development612

Miettinen J C Shi and S C Liew 2011 Deforestationrates in insular Southeast Asia between 2000 and2010 Global Change Biology 172261ndash2270

Miththapala S 2008 Mangroves coastal ecosystemsseries Ecosystems and Livelihoods Group AsiaIUCN Colombo Sri Lanka

Mizwar A and Y Trihadiningrum 2015 PAH con-tamination in soils adjacent to a coal-transportingfacility in Tapin District South KalimantanIndonesia Archives of Environmental Contamina-tion and Toxicology 6962ndash68

Mohammed A J M Inoue G P Shivakoti T KNath M Jashimuddin M De Zoysa and R JPeras 2016 Analysis of national forest programsfor REDD+ implementation in six South andSoutheast Asia countries Forest Systems 25061

Moreto W D and R V Clarke 2013 Script analysisof the transnational illegal market in endangeredspecies dream and reality Pages 209ndash220 inB Lecrec and R Wortley editors Cognition andcrime offender decision-making and script analy-sis Routledge London UK

Murakami A A M Zain K Takeuchi A Tsunekawaand S Yokota 2005 Trends in urbanization andpatterns of land use in the Asian mega citiesJakarta Bangkok and Metro Manila Landscapeand Urban Planning 70251ndash259

Myers N R A Mittermeier C G Mittermeier G ADaFonseca and J Kent 2000 Biodiversity hotspotsfor conservation priorities Nature 4032853ndash858

Natusch D J and J A Lyons 2012 Exploited forpets the harvest and trade of amphibians and

reptiles from Indonesian New Guinea Biodiversityand Conservation 212899ndash2911

Nghiem L T T Soliman D C Yeo H T Tan T AEvans J D Mumford and L R Carrasco 2013Economic and environmental impacts of harmfulnon-indigenous species in Southeast Asia PLoSOne 8e71255

Nghiem L T H T Tan and R T Corlett 2015 Inva-sive trees in Singapore Are they a threat to nativeforests Tropical Conservation Science 8201ndash214

Ngoc A C and T Wyatt 2013 A green criminologi-cal exploration of illegal wildlife trade in VietnamAsian Journal of Criminology 8129ndash142

Nicolas V V Herbreteau A Couloux K KeovichitB Douangboupha and J P Hugot 2012 Aremarkable case of micro-endemism in Laonastesaenigmamus (Diatomyidae Rodentia) revealed bynuclear and mitochondrial DNA sequence dataPLoS One 7e48145

Nijman V and C R Shepherd 2009 Wildlife tradefrom ASEAN to the EU issues with the trade incaptive-bred reptiles from Indonesia TRAFFICEurope Report for the European CommissionBrussels Belgium

Nowell K 2012 Wildlife crime scorecard WorldWildlife Fund Gland Switzerland httpawsassetspandaorgdownloadswwf_wildlife_crime_scorecard_reportpdf

OrsquoDonoghue P and C Rutz 2015 Real-time anti-poaching tags could help prevent imminent speciesextinctions Journal of Applied Ecology 535ndash10

Oishi A C S Palmroth K H Johnsen and H ROren 2014 Sustained effects of atmospheric [CO2]and nitrogen availability on forest soil CO2 effluxGlobal Change Biology 201146ndash1160

OrsquoNeill J 1992 The varieties of intrinsic value Monist75119ndash137

Osunkoya O O F E Othman and R S Kahar 2005Growth and competition between seedlings of aninvasive plantation tree Acacia mangium andthose of a native Borneo heath-forest species Melas-toma beccarianum Ecological Research 20205ndash214

Page S J Rieley A Hoscilo and A Weber 2013 Cur-rent fire regimes impacts and the likely changesIV tropical Southeast Asia Pages 89ndash99 in J GGoldberg editor Vegetation fires and globalchange challenges for concerted internationalaction United Nations and International Organiza-tions Kessel The Netherlands

Page S E F Siegert J O Rieley V Hans-DieterW Boehm J Adi and S Limin 2002 The amountof carbon released from peat and forest fires inIndonesia during 1997 Nature 42061ndash65

Pearce F 2007 Bog barons Indonesiarsquos carbon catas-trophe New Scientist 19650ndash53



Peh K S H 2010 Invasive species in Southeast Asiathe knowledge so far Biodiversity and Conserva-tion 191083ndash1099

Permadi D A F Murray and N T K Oanh 2012Regional scale modeling for projection of ozone airquality and potential effects on agricultural cropsin Southeast Asia Pages 199ndash219 in N T K Oanheditor Integrated Air Quality Management AsianCase Studies CRC Press Boca Raton FloridaUSA

Peters H A 2001 Clidemia hirta invasion at the PasohForest Reserve an unexpected plant invasion in anundisturbed tropical forest Biotropica 3360ndash68

Phelps J and E L Webb 2015 ldquoInvisiblerdquo wildlifetrades Southeast Asiarsquos undocumented illegaltrade in wild ornamental plants Biological Conser-vation 186296ndash305

Phromlah W 2014 A systems perspective on forestgovernance failure in Thailand Journal of Law andSocial Sciences 37ndash14

Polidoro B A K E Carpenter L Collins N C DukeA M Ellison J C Ellison and J W H Yong 2010The loss of species mangrove extinction risk andgeographic areas of global concern PLoS One 5e10095

Putz F E P A Zuidema and T Synnott 2012 Sus-taining conservation values in selectively loggedtropical forests the attained and the attainableConservation Letters 5296ndash303

Rands M R W M Adams L Bennun S H ButchartA Clements D Coomes and B Vira 2010 Biodi-versity conservation challenges beyond 2010Science 3291298ndash1303

Rautner M L Lawrence T Bregman and M Leggett2015 The forest 500 Global Canopy Programmehttpforest500orgsitesdefaultfilescompanies_analysis_january_2015pdf

Reed S E A L Bidlack A Hurt and W M Getz2011 Detection distance and environmental factorsin conservation detection dog surveys Journal ofWildlife Management 75243ndash251

Rejmanek M and D M Richardson 2011 EucalyptsPages 203ndash209 in D Simberloff and M Rejmanekeditors Encyclopedia of invasive introduced spe-cies Vol 3 University of California Press BerkeleyCalifornia USA

Richards D R P Passy and R R Y Oh 2017 Impactsof population density and wealth on the quantityand structure of urban green space in tropicalSoutheast Asia Landscape and Urban Planning157553ndash560

Sanamxay D B Douangboubpha S BumrungsriS Xayavong V Xayaphet C Satasook and P J Bates2013 Rediscovery of Biswamoyopterus (Mammalia

Rodentia Sciuridae Pteromyini) in Asia with thedescription of a new species from Lao PDR Zootaxa3686471ndash481

Satta A M Verdinelli L Ruiu F Buffa S SalisA Sassu and I Floris 2012 Combination of bee-hive matrices analysis and ant biodiversity to studyheavy metal pollution impact in a post-mining area(Sardinia Italy) Environmental Science and Pollu-tion Research 193977ndash3988

Schewenius M T McPhearson and T Elmqvist 2014Opportunities for increasing resilience and sustain-ability of urban social-ecological systems insightsfrom the URBES and the cities and biodiversityoutlook projects Ambio 43434ndash444

Schilthuizen M T-S Liew B B Elahan and I Lack-man-Ancrenaz 2005 Effects of karst forest degra-dation on Pulmonate and Prosobranch land snailcommunities in Sabah Malaysian Borneo Conser-vation Biology 19949ndash954

Schipper J et al 2008 The status of the worldrsquos landand marine mammals diversity threat and knowl-edge Science 322225ndash230

Schlesinger W H M C Dietze R B Jackson R PPhillips C C Rhoades L E Rustad and J MVose 2015 Forest biogeochemistry in response todrought Global Change Biology 222318ndash2328

Schloegel L M L F Toledo J E Longcore S EGreenspan C A Vieira M Lee and T Y James2012 Novel panzootic and hybrid genotypes ofamphibian chytridiomycosis associated with thebullfrog trade Molecular Ecology 215162ndash5177

Schmidt L 2009 REDD from an integrated perspec-tive considering overall climate change mitigationbiodiversity conservation and equity issues httpedocvifapoldeopusvolltexte20113307

Schneider A M A Friedl and D Potere 2010Mapping global urban areas using MODIS 500-mdata new methods and datasets based on lsquourbanecoregionsrsquo Remote Sensing of Environment 1141733ndash1746

Severinghaus L L and L Chi 1999 Prayer animalrelease in Taiwan Biological Conservation 89301ndash304

Sheldon F H H C Lim and R G Moyle 2015Return to the Malay Archipelago the biogeogra-phy of Sundaic rainforest birds Journal ofOrnithology 15691ndash113

Siciliano G and F Urban 2016 Hydropower devel-opment and natural resource allocation betweencompeting users and uses evidence from South-east Asia and Africa Colloquium Paper No 49Global governancepolitics climate justice amp agrar-iansocial justice linkages and challenges an inter-national colloquium 4ndash5 February 2016



Silyan S and K Kathiresan 2012 Mangrove conser-vation a global perspective Biodiversity and Con-servation 213523ndash3542

Silyan S and K Kathiresan 2014 Decline of man-groves a threat of heavy metal poisoning in AsiaOcean and Coastal Management 102161ndash168

Sing K W W F Jusoh N R Hashim and J JWilson 2016 Urban parks Refuges for tropical but-terflies in Southeast Asia Urban Ecosystems 31ndash17

Sist P 2000 Reduced-impact logging in the tropicsobjectives principles and impacts InternationalForestry Review 23ndash10

Slik J C Bernard M Beek F Breman and K Eich-horn 2008 Tree diversity composition foreststructure and aboveground biomass dynamicsafter single and repeated fire in a Bornean rain for-est Oecologia 158579ndash588

Slik J W F R W Verburg and P J A Kessler 2002Effects of fire and selective logging on the tree spe-cies composition of lowland dipterocarp forest inEast Kalimantan Indonesia Biodiversity and Con-servation 1185ndash98

Smajgl A J Xu S Egan Z F Yi J Ward and Y Su2015 Assessing the effectiveness of payments forecosystem services for diversifying rubber in Yun-nan China Environmental Modelling and Soft-ware 69187ndash195

Smith K F M Behrens L M Schloegel N MaranoS Burgiel and P Daszak 2009 Reducing the risksof the wildlife trade Science 324594

Sodhi N S L P Koh B W Brook and P K Ng 2004Southeast Asian biodiversity an impending disas-ter Trends in Ecology and Evolution 19654ndash660

Sodhi N S L P Koh R Clements T C Wanger J KHill K C Hamer and T M Lee 2010 ConservingSoutheast Asian forest biodiversity in human-mod-ified landscapes Biological Conservation 1432375ndash2384

Sodhi N S M R C Posa K S H Peh L P KohM C Soh T M Lee and B W Brook 2012 Landuse changes imperil south-east Asian biodiversityland use intensification effects on agriculture bio-diversity and ecological processes CRC Press BocaRaton Florida USA

South China Morning Post 2014 httpwwwscmpcommagazinespost-magazinearticle1457035myanmar-snub-nosed-monkey-faces-extinction

South China Morning Post 2016 Chinese damsblamed for exacerbating Southeast Asian droughthttpwwwscmpcomnewsasiasoutheast-asiaarticle1932944chinese-dams-blamed-exacerbating-southeast-asian-drought

South N and T Wyatt 2011 Comparing illicit tradesin wildlife and drugs an exploratory study Devi-ant Behavior 32538ndash561

Spessa A U Weber A Langner and F Heil 2009Fire in the vegetation and peatlands of Borneo1997ndash2007 patterns drivers and emissions Posterpresented at the European Geophysical UnionConference Vienna Austria

Stoner S 2014 Tigers exploring the threat from illegalonline trade Seizures and Prosecutions 2626

Struebig M J T Kingston A Zubaid S C LeCom-ber A Mohd-Adnan A Turner and S J Rossiter2009 Conservation importance of limestone karstoutcrops for Palaeotropical bats in a fragmentedlandscape Biological Conservation 1422089ndash2096

Suggitt A J P K Gillingham J K Hill B HuntleyW E Kunin D B Roy and C D Thomas 2011Habitat microclimates drive fine-scale variation inextreme temperatures Oikos 1201ndash8

Syaufina L and N A Ainuddin 2011 Impacts of fireon SouthEast Asia tropical forests biodiversitya review Asian Journal of Plant Sciences 10238ndash244

Tawatao N J M Lucey M Senior S Benedick C VKhen J K Hill and K C Hamer 2014 Biodiver-sity of leaf-litter ants in fragmented tropical rain-forests of Borneo the value of publically andprivately managed forest fragments Biodiversityand Conservation 233113ndash3126

Thijs K W R Aerts P Van de Moortele W Musilaand H Muys 2014 Contrasting cloud forestrestoration potential between plantations of differ-ent exotic tree species Restoration Ecology 22472ndash479

Toma T A Ishida and P Matius 2005 Long-termmonitoring of post-fire aboveground biomassrecovery in a lowland dipterocarp forest in EastKalimantan Indonesia Nutrient Cycling in Agroe-cosystems 7163ndash72

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Yang Y Y Y S Xu S L Shen Y Yuan and Z Y Yin2014 Mining-induced geo-hazards with environ-mental protection measures in Yunnan China anoverview Bulletin of Engineering Geology and theEnvironment 741ndash10

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Yule C M 2010 Loss of biodiversity and ecosystemfunctioning in Indo-Malayan peat swamp forestsBiodiversity and Conservation 19393ndash409

Zarfl C A E Lumsdon J Berlekamp L Tydecksand K Tockner 2015 A global boom in hydro-power dam construction Aquatic Sciences 77161ndash170

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Zhang M J R Fellowes X Jiang W Wang B P ChanG Ren and J Zhu 2010b Degradation of tropicalforest in Hainan China 1991ndash2008 conservationimplications forHainanGibbon (Nomascus hainanus)Biological Conservation 1431397ndash1404

Zhang P Y Hu D Xiao X Li J Yin and H S He2010a Rocky desertification risk zone delineationin Karst plateau area a case study in PudingCounty Guizhou Province Chinese GeographicalScience 2084ndash90

Zhang Y Z Zhu Z Liu Z Zeng P Ciais M Huangand S Piao 2016 Seasonal and interannualchanges in vegetation activity of tropical forests inSoutheast Asia Agricultural and Forest Meteorol-ogy 2241ndash10

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(PFOS) focusing on Asian countries Chemosphere89355ndash368

Zhou Z Y Y Geng X X Liu S Y Ren Y Zhou K YWang and W M Lai 2013 Characterization of aranavirus isolated from the Chinese giant salaman-der (Andrias davidianus Blanchard 1871) in ChinaAquaculture 38466ndash73

Ziv G E Baran S Nam I Rodrıguez-Iturbe andS A Levin 2012 Trading-off fish biodiversity foodsecurity and hydropower in the Mekong RiverBasin Proceedings of the National Academy ofSciences USA 1095609ndash5614

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SYNTHESIS amp INTEGRATION

Understanding the drivers of Southeast Asian biodiversity lossALICE C HUGHES

Xishuangbanna Tropical Botanical Garden Chinese Academy of Sciences Menglun Jinghong 666303 China

Citation Hughes A C 2017 Understanding the drivers of Southeast Asian biodiversity loss Ecosphere 8(1)e01624 101002ecs21624

Abstract Southeast Asia (SE Asia) is a known global hotspot of biodiversity and endemism yet theregion is also one of the most biotically threatened Ecosystems across the region are threatened by anarray of drivers each of which increases the probability of extinction of species in a variety of ecosystemsThese issues are symptomatic of the issues that face the global tropics however with around 4 billion peo-ple in the wider region and the associated pressures on biodiversity this region may be under some of thegreatest levels of biotic threat Deforestation rates in SE Asia are some of the highest globally additionallySoutheast Asia has the highest rate of mining in the tropics the around the greatest number of hydropowerdams under construction and a consumption of species for traditional medicines which is a threat to biodi-versity globally In this review the greatest threats to regional biodiversity in the SE Asian region are dis-cussed Tree-plantations and deforestation represents one of the most imminent threats and somecountries have already lost over half their original forest cover (ie the Philippines parts of Indonesia)with projections of as much as 98 loss for some regions in the coming decade Hunting and trade repre-sents a significant threat as demand stems not only for food but also for medicine for ornamentation andas a status symbol Mining represents a frequently overlooked threat as the Asian region is one of thegreatest exporters of limestone and various minerals globally and the cost of this to biodiversity is not onlythrough the direct loss of areas for mines but also through the development of roads that further fragmentthe landscape the leakage of heavy metals and the destruction of limestone karsts which represent globalendemicity hotspots Reservoir construction wetland drainage fires pollution invasive species diseaseand finally climate change are also considered Once each issue has been discussed the overall prognosisof regional biodiversity and priority actions to protect SE Asian biodiversity in the future is discussed

Key words climate change deforestation disease fire invasive species mining pollution reservoir constructiontrade wetland drainage

Received 25 July 2016 accepted 1 November 2016 Corresponding Editor Debra P C PetersCopyright copy 2017 Hughes This is an open access article under the terms of the Creative Commons Attribution Licensewhich permits use distribution and reproduction in any medium provided the original work is properly cited E-mail achughesxtbgaccn

INTRODUCTION

Southeast Asia (SE Asia) is a known hotspot ofbiodiversity and is of threat The region isuniquely biologically complex reflecting its com-plex biogeography and resulting in zonation ofregional biotic patterns and complex biogeo-graphic divides which require further research tofully understand (Sheldon et al 2015) Typically

when people consider SE Asian biodiversity theythink of the major biogeographic units it is madeof including Sundaland Wallacea Indochinaand the Philippines all of which are individuallyconsidered as some of the most diverse regions ofthe planet (Myers et al 2000)IUCN data (httpwwwiucnredlistorg) at a

country level show that if mammals birds andamphibians are analyzed at a family level SE





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