Conservation of Reef Corals in the South China Sea Based on Species and Evolutionary Diversity

Home , Acanthastrea brevis, Acropora abrotanoides, Acropora aculeus, Acropora acuminata, Acropora anthocercis, Acropora aspera

Biodivers Conserv DOI 10.1007/s10531-016-1052-7

ORIGINAL PAPER

Conservation of reef corals in the South China Sea based on species and evolutionary diversity

1 2 3 Danwei Huang • Bert W. Hoeksema • Yang Amri Affendi • 4 5,6 7,8 Put O. Ang • Chaolun A. Chen • Hui Huang • 9 10 David J. W. Lane • Wilfredo Y. Licuanan • 11 12 13 Ouk Vibol • Si Tuan Vo • Thamasak Yeemin • Loke Ming Chou1

Received: 7 August 2015 / Revised: 18 January 2016 / Accepted: 21 January 2016 Ó Springer Science+Business Media Dordrecht 2016

Abstract The South China Sea in the Central Indo-Paciﬁc is a large semi-enclosed marine region that supports an extraordinary diversity of coral reef organisms (including stony corals), which varies spatially across the region. While one-third of the world’s reef corals are known to face heightened extinction risk from global climate and local impacts, prospects for the coral fauna in the South China Sea region amidst these threats remain poorly understood. In this study, we analyse coral species richness, rarity, and phylogenetic

Communicated by Dirk Sven Schmeller.

Electronic supplementary material The online version of this article (doi:10.1007/s10531-016-1052-7) contains supplementary material, which is available to authorized users.

& Danwei Huang [email protected]

1 Department of Biological Sciences and Tropical Marine Science Institute, National University of Singapore, Singapore 117543, Singapore 2 Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands 3 Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia 4 Marine Science Laboratory, Chinese University of Hong Kong, Shatin, NT, Hong Kong Sar, China 5 Biodiversity Research Center and Taiwan International Graduate Program, Academia Sinica, Nangang, Taipei 115, Taiwan 6 Institute of Oceanography, National Taiwan University, Taipei 106, Taiwan 7 Tropical Marine Biological Research Station in Hainan, Sanya 572000, China 8 Key Laboratory of Marine Bio-resources Sustainable Utilization, South China Sea Institute of Oceanology, CAS, Guangzhou 510301, China 9 Department of Biological Sciences, Universiti Brunei Darussalam, Jalan Tungku Link, Bandar Seri Begawan BE1410, Brunei Darussalam 10 Br. Alfred Shields FSC Ocean Research Center and Biology Department, De La Salle University, 1004 Manila, The Philippines 123 Biodivers Conserv diversity among 16 reef areas in the region to estimate changes in species and evolutionary diversity during projected anthropogenic extinctions. Our results show that richness, rarity, and phylogenetic diversity differ considerably among reef areas in the region, and that their outcomes following projected extinctions cannot be predicted by species diversity alone. Although relative rarity and threat levels are high in species-rich areas such as West Malaysia and the Philippines, areas with fewer species such as northern Vietnam and Paracel Islands stand to lose disproportionately large amounts of phylogenetic diversity. Our study quantiﬁes various biodiversity components of each reef area to inform conservation planners and better direct sparse resources to areas where they are needed most. It also provides a critical biological foundation for targeting reefs that should be included in a regional network of marine protected areas in the South China Sea.

Keywords IUCN Red List Á Marine biodiversity Á Phylogenetic diversity Á Rarity Á Scleractinia Á Species richness

Introduction

The South China Sea (SCS) is a large and species-rich marine region in the Central Indo- Paciﬁc (Fig. 1). Despite being situated adjacent to the Coral Triangle and hosting com- parable levels of biodiversity, including 571 species of scleractinian reef corals (Huang et al. 2015) and over 3000 species of ﬁsh (Randall and Lim 2000), this region has received much less research attention. The shortfall in biodiversity research on the SCS needs to be addressed as coral reefs are being destroyed at an alarming rate (Madin 2015). Besides exhibiting high species diversity, scleractinian corals in the SCS display a remarkable degree of spatial variability in species composition (Huang et al. 2015). The most coral-rich areas of the SCS include western Luzon and southern Vietnam, which contain more than 400 species (n = 433 and n = 406 respectively; Vo et al. 2014; Huang et al. 2015), but most other areas have less than 300 species. More specious areas stand to lose more species (Roberts et al. 2002), ultimately putting the entire ecosystem at risk by reducing functional redundancy and jeopardising key ecological functions (Jones et al. 2011; Hooper et al. 2012). However, species richness is not the sole determining factor of ecosystem functioning; other components of biodiversity such as relative abundance and functional diversity are also key determinants that should be considered for conservation (Hooper et al. 2005; Bellwood et al. 2006; D’agata et al. 2014). For complex ecosystems, despite a wealth of literature linking greater diversity to increased resilience to disturbance, work is emerging that demonstrates the contrary (Bellwood et al. 2006; Cadotte et al. 2011; Mouillot et al. 2014). Indeed, reefs with more coral species have lower resistance to crown-of-thorns seastar (Acanthaster planci) outbreaks, coral bleaching and storm impacts, and furthermore

11 Department of Fisheries Conservation, Fisheries Administration, Ministry of Agriculture, Forestry and Fisheries, Phnom Penh, Cambodia 12 Institute of Oceanography, Vietnam Academy of Science and Technology, 1 Cau Da, Nha Trang, Khanh Hoa, Vietnam 13 Marine Biodiversity Research Group, Department of Biology, Ramkhamhaeng University, Huamark, Bangkok 10240, Thailand 123 Biodivers Conserv

105ºE 120ºE

30ºN

CN2 TW (95) (316) VN4 (176) CN1 (102)

PA (201) 15ºN VN3 (252) LZ (433)

PL (398) TH (264) VN2 (406) SP VN1 (333) (251)

SA (248) MY (398) BN (391)

SG (255) 0ºN

Fig. 1 South China Sea reef areas examined in this study, indicating the respective species richness of stony corals do not recover faster (Zhang et al. 2014). Better understanding of the links between diversity, functional redundancy and resilience is therefore critical for predicting the future of reefs. For instance, important ecosystem contributions are made by species that are rare, both in terms of local abundance (Lyons et al. 2005) and geographic range (Mouillot et al. 2013; Jain et al. 2014), yet these species tend to have the highest extinction risk (Harnik et al. 2012). While over 10 % of coral species are considered to have restricted or highly fragmented ranges (Carpenter et al. 2008), aspects like their distribution in diverse areas, the overall extinction risk they face, and how their contributions to reef diversity will change in the future remain poorly known. Our study aims to fill this gap by characterising the degree of rarity contained within each SCS area. For more than two decades, evolutionary diversity has become a major component of conservation research (Vane-Wright et al. 1991; Nee and May 1997; Faith et al. 2010; Curnick et al. 2015). Preservation of the tree of life is now often set as a goal in itself (Posadas et al. 2001; Rodrigues and Gaston 2002; Forest et al. 2007), or as a proxy for the 123 Biodivers Conserv protection of ecosystem functioning (Maherali and Klironomos 2007; Cadotte et al. 2008; Flynn et al. 2011). Although biodiversity has been interpreted primarily in terms of species richness, it can also be quantified as evolutionary lineages (Altschul and Lipman 1990; May 1990; Faith 1992), which in turn can be used to examine phyloecological trends in distribution patterns (Hoeksema 2012) and other features relevant to species communities, such as coloniality and associated fauna in scleractinian corals (Barbeitos et al. 2010; Gittenberger et al. 2011; Hoeksema et al. 2012). In conserving biodiversity, a broader and more representative goal could be approached by prioritising species or areas that most likely protects the diversity of the tree of life (Witting and Loeschcke 1995; Isaac et al. 2007; Rosauer and Mooers 2013). Recent studies have shown that anthropogenic extinction threats against corals are not distributed randomly on a species phylogeny (Huang 2012). Rather, many risk factors such as mass bleaching, disease and crown-of-thorns seastar outbreaks have the potential to devastate evolutionary diversity of coral reefs on a global scale (Huang and Roy 2013). The future of evolutionary diversity at local and regional levels remains uncertain, but given the availability of species distributional data in the region (Huang et al. 2015), this now becomes possible to predict for the SCS. The primary objective of this study is to quantify and project changes in species and evolutionary diversity of 16 reef areas in the SCS region to better understand and prioritise conservation resources. We update coral distribution records compiled recently by Huang et al. (2015) and compare species richness, rarity and phylogenetic diversity among 16 reef areas in the SCS (Fig. 1; Table 1). Rarity is defined based on geographic range limitation (Gaston 1994), and the level of rarity in each area is determined by averaging species weights assigned based on their range restrictedness. We then integrate conservation status data from the IUCN Red List of Threatened Species (IUCN 2001; Carpenter et al. 2008) and perform extinction simulations to predict changes in phylogenetic diversity (Faith 1992) of reef areas caused by species loss. Our findings underscore the conservation value of particular SCS areas whose immense biodiversity is threatened by impending extinction.

Materials and methods

The SCS is a large marine region with a surface area of 3.4 million km2 (Fig. 1; Morton and Blackmore 2001), including about 12,000 km2 or 4.7 % of the world’s total coral reef area (Huang et al. 2015), and is surrounded by the coastlines of ten Asian nation states. Species distributional data of scleractinian reef corals in the SCS were previously consolidated by Huang et al. (2015). The dataset comprised occurrences for a total of 571 species (see Online Resource 1) recorded among 16 reef areas in the region (Table 1). Records for southern Vietnam (VN2) were updated (Vo et al. 2014). To determine the relationship between regional and global patterns of coral diversity, we supplemented the SCS distributional data with geographic range information from the Coral Geographic database (Veron et al. 2009, 2011, 2015). This database of 798 species divided the seas containing reef corals into 141 ecoregions. Data for SCS species not available in the Coral Geographic were obtained from the IUCN Red List of Threatened Species (IUCN 2001; Carpenter et al. 2008) and the Global Biodiversity Information Facility (GBIF; http://data.gbif.org). A total of 547 (out of 571) species were covered by these global databases. For each species, we computed ecoregion (global) and area (SCS) occupancies for each species by summing the number of the respective geographic units that contain it. The predictive capacity of the SCS data on global ecoregion occupancy was

123 idvr Conserv Biodivers

Table 1 South China Sea reef areas (according to Huang et al. 2015) examined in this study, showing species richness, the Index of Relative Rarity (IRR ) (Leroy et al. 2012, 2013), number (and percentage) of species in each IUCN Red List Category (EN endangered, VU vulnerable, NT near threatened, LC least concern, DD data deﬁcient) (Carpenter et al. 2008), and mean percent (and 95 % conﬁdence interval) excess loss of phylogenetic diversity (PD) (Parhar and Mooers 2011)

Area Richness IRR EN VU NT LC DD Excess PD loss (%)

Singapore (SG) 255 0.0063 1 (0.4) 39 (15.3) 83 (32.5) 130 (51.0) 2 (0.8) -1.05 (-1.10, -1.01) West Malaysia (MY) 398 0.0500 5 (1.3) 100 (25.1) 115 (28.9) 162 (40.7) 16 (4.0) 1.31 (1.24, 1.37) Thailand (TH) 264 0.0025 0 (0.0) 40 (15.2) 79 (29.9) 144 (54.5) 1 (0.4) -0.88 (-0.93, -0.84) Southwestern Vietnam (VN1) 251 0.0073 0 (0.0) 34 (13.5) 74 (29.5) 138 (55.0) 5 (2.0) 0.53 (0.48, 0.57) Southern Vietnam (VN2) 406 0.0228 3 (0.7) 93 (22.9) 117 (28.8) 179 (44.1) 14 (3.4) -1.38 (-1.42, -1.33) Central Vietnam (VN3) 252 0.0058 0 (0.0) 40 (15.9) 74 (29.4) 137 (54.4) 1 (0.4) -1.67 (-1.71, -1.62) Northern Vietnam (VN4) 176 0.0034 0 (0.0) 25 (14.2) 60 (34.1) 90 (51.1) 1 (0.6) 1.20 (1.15, 1.25) Paracel Islands (PA) 201 0.0249 2 (1.0) 34 (16.9) 57 (28.4) 101 (50.2) 7 (3.5) 1.31 (1.26, 1.37) Southern China (CN1) 102 0.0271 0 (0.0) 11 (10.8) 32 (31.4) 51 (50.0) 8 (7.8) -0.88 (-0.91, -0.85) Southeastern China (CN2) 95 0.0210 0 (0.0) 12 (12.6) 37 (38.9) 45 (47.4) 1 (1.1) 0.62 (0.58, 0.66) Brunei (BN) 391 0.0275 4 (1.0) 92 (23.5) 116 (29.7) 175 (44.8) 4 (1.0) -1.21 (-1.27, -1.16) Western Sabah (SA) 248 0.0212 1 (0.4) 42 (16.9) 69 (27.8) 131 (52.8) 5 (2.0) -0.87 (-0.92, -0.82) Spratly Islands (SP) 333 0.0108 0 (0.0) 59 (17.7) 97 (29.1) 168 (50.5) 9 (2.7) -1.24 (-1.29, -1.20) Northern Palawan (PL) 398 0.0333 4 (1.0) 95 (23.9) 110 (27.6) 180 (45.2) 9 (2.3) -0.50 (-0.55, -0.45) Western Luzon (LZ) 433 0.0296 3 (0.7) 112 (25.9) 122 (28.2) 188 (43.4) 8 (1.8) -1.01 (-1.06, -0.96) Taiwan (TW) 316 0.0253 1 (0.3) 54 (17.1) 97 (30.7) 157 (49.7) 7 (2.2) -0.82 (-0.86, -0.78) All areas 571 0.0848 11 (1.9) 160 (28.0) 145 (25.4) 210 (36.8) 45 (7.9) 0.17 (0.12, 0.23) 123 Biodivers Conserv estimated by fitting a linear model through the origin. We then used the global distributional data to assign species rarity weights for the characterisation of relative rarity among the 16 SCS assemblages. Gaston’s (1994) quartile definition was set as the rarity threshold, being the number of ecoregions at which 25 % of all species with the lowest global occurrence were considered rare (Leroy et al. 2012). These rare species were assigned weights that increased exponentially with the difference between their occurrences and the rarity cutoff. Finally, using the R (R Core Team 2013) package Rarity (Leroy et al. 2013), we computed the Index of Relative Rarity (IRR), given by the average weight of rarity for all species in each assemblage. The index was also calculated for the SCS as a whole. We derived coral conservation status data from the IUCN Red List of Threatened Species that included 827 reef-building scleractinian species assessed by many of the world’s leading coral experts in 2006 and 2007 (IUCN 2001; Carpenter et al. 2008). The assessment concluded that one-third of the 688 species not deemed data deficient (DD) faced heightened extinction risk (i.e., CR critically endangered, EN endangered, VU

Cyp

s i

r i i is amo

s s Echi Echi

Cyp

e e

hastr i a

Cyp i n d

S Cyph Ec i t a ens orm

h n pt Cy f is

y Cyphast s o ntast S a s u n i a S i c r Echin ha e nopora t m l s S i o i hi i a n l i opora Cy y s E r o y l t Ech i at a Ca p hastrea c a ea i y m Ech p a ra n i a no Symphyllia rect t p p r m s s sta a a a is H Ec c r t hastr n l s r m

astrea ocel h t m be e li a Hydnophor p tre a n eens o o hi u p tr i a t e e m ydnophora talap p y rowley ti s si pora hi ra l a ymb i hast micr e tu n s ns b i s h p i l p i n h a d r op nopora e s h a n l i hihir os ofl n i a o Hydno f a ph P a l o u ri n y a s h ma h

i i H h v ie Hydn opora taylorae ea salebrosa y n e n v m a pachyse a

c r l s a a o r l co c ch chi

y ea i k l a p ora l a or ch a a as e y o ry i l w a l i i a pi s Hydnophora pi po e a i a i ammifor r e a inat l a opht i i l l a dn h a e ty i ul a deca a p l i a a hyllia jardi l a i o e l l i s l l i a at A l ormi l i l s i h ag r i llia m l l pri a y l yllia se l l ora p hm a f P a l h j a l a y l gem y i a g y yllia d lac otund Platy r r llia s s n apon y y r y ust l y l Lepto o o h i h l y d Plat a g a li c t l phora lam s y hig h y h ia h ec h reg r h atygy h h pha nis ph phora rig s assizi h v P p o h yl abr subechinata uti h i a d p hy hal h hyllia s se r p v p yl d a r o a o e p p p r e a p a c p h ras l o i p latygy r i u o p alomus p hem r a gl a o h e o lina m i a a o r o rensis i o ophyl r s o o c s acera ea f P ygyr al a s o p a punct c b ai m o l

m e gyr b t o b dia ea a i ya b tr r ra bons r n el ma ic b a a r u b n a i si s o t r t la ci i P m y no ri r b i trea o c a e a inut o o a o op a o ra a o m i Gon Pl a s e r ace lia o a ae Pl id m obophy i narina in r a br t lo a o n l lat a p roc grand ma o h r tre r p or ty ey a cr fic S n mak a e L gyra L i L h ul l is L Favi a L i m Lob y hinophy e i L a L h p a a a L st s a o s Aus por i Goni Pla g r Pa i y xesa nei Ho pora c has st hi l tygyra a si u C tr m is ty a a Ec ch y po a s in i gyra ry y carnosa h onos i a Ec ch y a oba otus a Pla d Ec chinomor thas s e r l Fa g ra maensisossl n da ai s Ec nt h ha a l m rbid e r los E x anthas t s t s tes s t E xy ha e ti yr ae en z y E a t s ea e h u Favites mC t ygy i Ox n ussa v or a s vi rea aFavit g s O c an nt r tr a bo a t v e O t plex f s n i o ygy a a Ac a i F t st er a s ia A nthastre m es p l da ll ca ntha mul e et i e co Acanthast a mu ea t l i a ra pin ndi is i Ac can o as tre dia uo la rea u a tyli wey A a llia t n vit Ac c s tr sim h ls F e ra m lea c cr ra in y l n st us k nt A i a caul e av ara s y fe A cro nthas a h mer a e A o ias a i s s val r de t uen a orta M a l gy p lic we m ta i F it ea r russel l ra i Mi c a s a Fa agnist a cutali i Mont p r o z s ta s a es c fl n es ro ogyra ra a a n vitesF acutic a formisl A e ogyr z y n atus ea Dipsa F vite e ens s a Di l u d e Fav a xu Pl ogyr g uss ss n r avites v e sp is P ogy k obu ac ncieh er r o hin r e t ite l Pler l a s po ite s in e osu e is i Pler e mens om cia sinai a d a m P y t c ec tu F st Favites s ens llata ra Pl e omu a ru s a nn t ba a ith c os a r e s N as s b th us a O F vit a co bdita Ph a us ol li mo e av s li e a l ia il rup id u Favi ea p c is Bl d lo a a C lo e mp er ollis s Bl c i p ites rr au F it s ino i Podao opil a a o ia re s p es col m u P o d b ac u O h a r la vasta ra a sc h p osa is is last v te o a s m Z andan a it r ali u yll t S a ab gi ia in u s O lo it s u rs na a n utaru q ns C C ia es fl n S ia fung g c ru e e en a a r u p emani ha t Podod lom fu n s n aea l h b e d a P u a p p tae ck is C ula u o y e ha x a e f is a ina t i alis la ph lli n u t Ha a t ma m aulasstraes ech a c n lic o a Fung n ew o t yll s Dana ac ea a bo sversa or ra e o a tastrestretr n a f e ia r tt r Da p ta s re a b ni P traea in is a a Lob a a aequ ti e tum Pe ec a ca le p e Le p t tre e tra Ph t u e p a c ina la Pectiniati ter umidalatav a L e as lastre a l u a y ctin ni u is L ptast str a a d r P P s a fur r ta stre fr n ec e op c v Le p a u ab ifer My c h ia m cataa Lepte ngi n c in ti t rassa ta ptaasimpu gi o s c M P ni in ylli L e r n ll n pandainna ediuy e a i ax L a iof u c a ce c alca a P hy llo re n F Mycedi d ti la a i e el iof p llon nsp av m i nia y m s H el o hy o ites um roboi c le a H ll inataa elep p cor tu ni hop y llon coch s a c Lith ophyph y e s mi u eoniani a Lit ith s ra tentaculatina G Fa c m han s L ph p oni vi r As m k tho cti albial x ni t op t t a Li tho a ctis sc t ha Go a es en re ancot k Li en a ti a g G st a cu us i t n li limaau ilis Leptoron ni re pe ta aoi C te nachyl v s Sc ia astrea ntagogo C p itha is te ap s st n rta ly ol fragnu li tre ell u Cteo p erisis te lo o a a s P s er ta M phylliia minigern clo ris ensis ei e irr re a Hery os e s cycn tula ill Meruru a e tif a C cl os ri si s Gonia lina cy g ormut y cl se is o lis u a C y omervi na Go lin scablin la is C s o Gon strea a amp dri ris Cyclocloserseris c okaag Dipsas nia r ca y eris ex rta nsis Co ia st edw icu C yclo ris m o ne is strearea pe lia la C clos ris h ist s D Tra ela traea ar ta Cy ip c st fa dsi ycloselose ris d uccen sa hy re c vu C c se is taiwaol ulosa sis str phyla rot tin lu Cy clo ct D ae pal um atas y is mgran motenlata ipsastra v lia geoffa ana C is nu Dips ie ue Pleuraract t pla Dip ae tn nsi tis paux si astr ame r s Pleu ac s e lla Di sastr aeaa truncm oyi Pleuracur well ce p ar nsis loseriris avis i da sast ae itima Ple c gr jebb fun Dip ra a Cy lose is us raszi sastr ea rosariaat ell t Dip Dips m a Cyceuractr ra proers a sastraeaas ae ax Pl ntha a ni tat traea v ima Ca mmococor alis Dips a f ero mo ora digiaimianaici Dips as amicoa ni Psa oc a h as As traea ladvus m cor superf ta tra trea ru Psam ora ella a ea he an m Psammmo c igu Di l nul di Psa cora contst D psa iant igera sammo neilli ipsas stra hoi P mmo mc Dips e des Psa ea a traea a la sammocoraara a monilesa Dips stra danxa P scin as Dips astraeaea alp ai Co naraeea cr a Dips as alli osci ara a is as traea da C scin aea exesmn aens Di traea m bida Co inar a colu im tatus Heter psastra liz atth osc rae cos op ea ard aii C cina ea hahaz sam sp ensi Cos nara hus aequi T mia cocheci s ci yat pata urbinari osa Costeroc ris osa Turb a leata He strea c verruc is inari bifro IUCN Red List Category Turb n Oula lopora Tur inaria a cra s Pocil uxi Turb binari frondeter loporaa damicorneydo drina inaria mesea irregu ns Pocilillopor mean T laris Poc lopora oodjonesi urbina nte Pocil w i Turb ria paturina llopora her mis inaria pelt la Poci ora kelle Turb Pocillop a fungifors Turbinarinaria ata Vulnerable / Endangered illopor legan ia radica Poc pora e e Turb renifor lis Pocillo a dana Por inaria stellulatamis cillopor itipora pal Po opora ankeli Goniopora iform Pocill alb is tata Goniopora biconus Seriatoporapora hystrixgut a urgosi Seriato dentritic Goniopora riatopora Gon ciliatus Least Concern / Near Threatened / Data Deficient Se a stellata iopora columna Seriatopor a Goniopora opora aculeat Gon djiboutiensis Seriat iendrum iopora eclip Seriatopora cal Go sensis pistillata niopora fruticosa Stylophora Gon Stylophora danae iopora lobata subseriata Goniopora minor Stylophora Goniopora n Madracis kirbyi orfolkensis mosa Goniopora palmensis Palauastrea ra Goniopora Stylocoeniella guentheri pandoraensis Stylocoeniella armata Goniopora pendulus Stylocoeniella cocosensis Goniopora planulata Acro iopora savignyi pora humilis Gon Acropora globiceps Goniopora somaliensis si Acropora gemmifera Goniopora stoke Acropora s a stutchburyi amoensis Goniopor Acropora digitife iopora tenuidens Acr ra Gon nctata opora retusa Stylaraea pu Acropora mu s aranetai Acr ltiacuta Porite ta opora monticulosa ites attenua Acropor Por ensis Ac a fastigata orites australi s ropora lut P ocosensi Acrop keni Porites c atus Ac ora secale tes cumul s 123 4 5 67891011 12 13 14 15 16 ropora Pori deformi Acropora valida Porites ensa Ac pruinos rites d a ropora a Po hinulat Acro nasuta rites ec ni Ac pora ki Po es erida ropor mbee Porit talata Acr a cerealis nsis orizon a opora tes h istellat i Acro micr Pori ites lat ayer Acr pora i oclado Por rites m opora ndon s Po iculosa Acropor pan esia mont nsis Number of areas recorded Acr a icul rites rraye a opor cyther ata Po s mu Acrop a hyac ea orite napoporsis A o int P ites sen s crop ra an hus Por negro cen Acro ora s thoce rites igres a A pora qua rcis Po n ornat s crop lor rrosa orites su Acro ora ipes P Poritesrugo na A po simpl ites ia i cropora ro e Por iman son Acr r sar x sill hen s A opo a lo ia es step losu cro ra kan Porit tes rcu ani Acro por lovel i ori be ugh A p a g li P s tu va nnae cr ora lau rite rites a nni Acroporaopo bu ca Po Po tes rma ta A ra g shy Pori ve ba cr ran ens s e s lo rus Ac opo carduusulo is orite rite tes n Acrrop ra sa P Po ori che or so P s li ica Acrooporaa c lita te ndr a Acro lathr ry ri yli id por hoeksata ens Po s c sol ea Ac pora di is ite es lut s A ro v Por orit es i c po a aric em P rit ensna A rop ra rus at ai Po aw a cr or te sel a in nya Acr op a pi ne li ok avig ai Ac o ora ch lla es s am a ro po el o rit rea ay Acro po ra eg ni Po t rea formosanat s Acro ra lon tu ans eras trea t pl an a A po raki id ex ust er i cro porra gicy S iderastas is cr lif er A awi ider er in bu in A cr po a ath eudos os s tu rd ea c op ra bat s i is ga rac sa A rop ora p u us P seudosLeptser er is y s A cr rox n P to tos er p lio c o ora deraim ai ep p s pa oide Ac rop por a L Le to s ris for s Acropor a ki li ep eri se se yabei op ora st rs wa s L os to to s ra Acr o s ri ty n p ce ri iiensi a A ra elagoat a ens Lept Le e a id c o r m a e my os l ta Acr ropporaa to ill is ris pt hawris scabso ia a A ep se Le ris str at i cr op o rtuo o to e se s ul r Acroporao o ara spe ra p os pto oseris ye s Ac p ra c sa Le e t lan a Ac ora deyo a ci L ep serip m rian rop roli o Lept L pto s is a a A r ng sa e ri er v avustit A croporaoporora val e ni L se s cl r ai cr n i a ro lo na a Acr a te cumid na e o na ip anata Ac o ru o b d s o po e m C Pav a A r po ra sarmentr nci nata ardine Pavona us deni Ac c o es G o c latais ro por r fl en v von s ta A ro pora a o n a de n u A c wi rid e Pa P ve n a ro p a s na planui s Ac c p o d ll a osa i o ex ld mi o us A ro o ra esalwisae v a a cror porr s a m a en er A opor a m pi P Pavona duern v sa a A crop s icro ci a cactdif o cr p a u n vo na li e Acr or l ka fe ii avonao a o on a a Ac op o a i p r P v P v fr fo s opora ro a p s n h a is volut A r ra pulc o te o th Pa a r a A c o or ho ri i a P avona emm iosar Ac c ro p lys l P onase g ugo o or a r m y is in r a Ac ro p aspe ri tom a av r is s s A ro o a h d P r i pec is r p ra a ach e r ancncoraivi A cr opop or ra ab busta P yses e s s a d ta Ac c o o a s i ia a A ra a p r r y r l a enst ro p ot a chy li a sa A c r o r e v lum h cens A c r o po r a a an Pacha c ysehyl yl ris vi o p a v xq ugha P a parah ens ris A c ro p o oi ch di A c r o r sp u P a c c la s op p o r a e s de a Eupllia li bres s elian A cr ro o r a p r isi a P Eup aeyam a ra e ta A c a pa ath w s y yl h e p A o p or ra t n gl r c ro po o m p e a i pa br cicu sc a Ac c r in a u y ph a a s sa A r o po r a u lm i la i llia li a a ise eata A o ra a ll li f re g r a c r p he sig r a ta Euphy l gl r Acr ro op p r g ic e Eu o n ept a A cr ora a a r y ra ea ac amos at t a o a ra n r e phyl x h l Ac c op po or r nanappre m ta a uphy r a Ac o a n is e E pa a asto s a i A ro a s a di p Eu uph t o Ac ro p r l r auci i ic Isop c ro o o a a cu E a xea excelsa dale gi p s i li Gala p a g ai I r p r ra t ssa ch l Galaxeala r a ocel I s ropoo por ora a e ubu is laxea lo in I s o lse leus a minu izardl s o por s t ii a o or r on t tal I o r ab e dae gas ata An s o po Ga G Galaxe xea o p al i a An p o a t a e u l l japona r A o yi ata la op ca g p o r ra a bg ro nsisana Anacro p r a d chin xea cryp op st i at Mon na a o r enu Euphy ala a e ata is a Mon ac o a a inte o l a ve ra s r l M c r l l e ll M c a a h l G n s a M r a cr n o el tans M cr r p u us b osen AlveopA lv po pora ri o rop o a t e ene M o a is at ra pora io m lli Mo ont n t b ate n r Ga A eoporao veoporo f l e s M ont opor pora m i op r a Mo nt t i l t e us Mon o ti p ogi r ife e era e a racilis M ipor a a verri cucull e M onti u a v Al v da Mo n i po o o e ve g ha gesta r M por l r cr list i Mo nti i po ri s Alv l ra oc t is Mo o e ra ta di lveopora a a expans n M ipor por r g ta r M o n t r Al Ana a i A n Mo ip an g fo A a a Mo ont a a i Monti n r s A i e M a u M n ca ulata M t a M nsis M s M o tipora r M a po ra r M n pora c p s ge Alveo retonen liensi l ns o a ra ata e a t ip a c t a c n n t o p ret rmis s i w s a u a nt s o tu pi en ont tip i ora por por ffusa i p o n y o a o ver o ioph o i o t p ol sis n n ti ipor ra g mat s r eopo ra suta e o ma r n cula s c ris ata o ca lo a n ip danae ue tte t tip ge n ipo n n n pora m ra s ali s n p o no opor rina n i ti t unda a i o ro ra s t eo n eo pora r r tip o c st ormi r i o t t t r t ugini t i e a a e gson n i p o streo por o a p r tle p p i hir i i v a mo i por c e a e ip r i u s r u m p a tr o ra p Alv p reopo be p s n l u p o r s e o a t p f i t A reopo ne r ra his t opora a mp o or onfus a t fove n c cen t ra g inf o a co lat r ng p u o h o s or o a p a oga a n A r o r o o o ns a cebuensis ra a and r d i s a ap or r s e eo o a a a p r a s r r ai i As re p ta l mard t ipor asteri a r e A a l t pora f a a a ra Ast a r ae a Alveo a a ituber a i p sa ora my c i a al f a a A p s a cocose r c w o u ra a ti c r t l a f elic d streopora st i is s m t

r m e lores i p h n f r a i s d l v o t t l me viet t eopor o a nt fo a pongodes l l ac fo i e ora nodosa q A A ss a a u a l ma pora ni v pora of cra ase a Astr ig a co r o r e l a p o p on ipo a uit a r tipor i tipora friabilis s ta b i e r r ip

t o n w r ae Mont ma ll a ita f b i n t p tu t mi ontipor Mo e M r nt m id is a

p rni n o a Monti ss t ipora hod a e u ora i r c onti Ast o on r r p u o n a t s M Montipo o s tipor u ta c e n a s be s onti ntipora mill ens r Astreo a cra ta la o a

n a M ora ip a M n Monti u s M c i i M e o ipora o M t st m M Mon o p p t t l u r n

Montipo i i p o a n

M i c t t er l s t M en por s Mo Mont i o u

n a

ontipora mon s i lat s

Mo o o sis Mon a

M a Mon M M

Mont

Fig. 2 Strict consensus phylogenetic tree of reef corals in the South China Sea. The number of reef areas recorded for each species is shown using a coloured circle, with IUCN Red List threat status denoted as red (threatened) or blue (non-threatened) tip label 123 Biodivers Conserv vulnerable). Of the 571 coral species recorded in the SCS, 543 were characterised based on the IUCN Red List categories. The remaining 28 species not assessed previously were categorised as DD. We note that the lack of information for DD species may be related to inadequate taxonomic study, or to their possible rarity and restricted distribution range, in which case the number of threatened species may be underestimated (see below). Based on the threat levels for species, we carried out a simulation study to predict regional changes in evolutionary diversity arising from projected extinctions. To quantify the pre- and post-extinction diversity of each SCS area and the region as a whole, we employed the phylogenetic diversity (PD) measure (Faith 1992), computed in R (R Core Team 2013) packages caper (Orme et al. 2013) and Picante (Kembel et al. 2010) as the total branch length in the phylogeny of species present in an area (Davies et al. 2008; Fritz and Purvis 2010). For this computation, we pruned the 1000 time-calibrated posterior supertrees of reef scleractinian corals reconstructed recently (Huang 2012; Huang and Roy 2013) to a taxon subset corresponding to the species complement of each area (Fig. 2). Species loss was simulated by assuming that all threatened (CR, EN or VU) corals in an area would go extinct, with the results compared to a null model of random extinction repeated 1000 times with the same extinction rate (Purvis et al. 2000; Sechrest et al. 2002; Fritz and Purvis 2010). We then calculated the excess loss of PD as the extra loss of actual PD over the null result, expressed as a proportion of the latter (Parhar and Mooers 2011), and assessed for statistical signiﬁcance using the Student’s t test. The analysis was carried out for each of the 1000 posterior trees, with results summarised as means and 95 % conﬁdence intervals.

Results and discussion

Our study brings together species and phylogenetic diversity data at the regional scale with global distribution and extinction risk information of the 571 reef coral species in the SCS (see Online Resource 1). Species occurring in the SCS include geographically-restricted species such as Physophyllia ayleni in the Macclesfield Bank (Paracel Islands reef area) and Pseudosiderastrea formosa in Taiwan, as well as widespread species such as Pocil- lopora damicornis that inhabits every SCS area and are present in nearly all (118) of the reef ecoregions in the Indo-Pacific marine realm (Veron et al. 2009). There is a statistically significant positive linear relationship between SCS area occupancy and global ecoregional distribution (slope = 6.39, p \ 10-15, R2 = 0.942; Online Resource 2). As expected, species that are rare in the SCS region tend to be less widespread at the global level. Therefore, focusing on reef conservation efforts at the regional level, like an implementation of a regional network of marine protected areas, or MPAs (Clifton 2009; Walton et al. 2014; White et al. 2014), will help preserve a good representation of global species diversity. Despite the strong positive relationship between global and regional occupancies, there are considerable variations in the global distribution of species (Online Resource 2). For example, Cycloseris distorta is recorded in 89 reef ecoregions according to the Coral Geographic (Veron et al. 2009, 2011), yet it is only present in two SCS areas (Fig. 2)— Thailand and southern Vietnam—which could also be related to differences in species identifications among studies as seen in the Great Barrier Reef (Hoeksema 2015). There are also regionally widespread species such as Montipora florida, Pleuractis gravis and Turbinaria bifrons that are present in as many as half of the SCS reef areas (Hoeksema

123 Biodivers Conserv

1993; Veron et al. 2009), but are in fewer of the world’s ecoregions (15–20) than expected (*50). These variations in global occupancy are useful in helping to determine the relative rarity of species hosted by each SCS area. The globally widespread Cycloseris distorta (for locality records, see Hoeksema 1989), for instance, receives a weight of zero and is not in the quartile of species with the lowest global occurrence to be considered rare (Leroy et al. 2012). By contrast, Montipora florida, Pleuractis gravis and Turbinaria bifrons meet the threshold of rarity and have weights of 0.163, 0.285 and 0.205, respectively. The index of relative rarity (IRR), calculated by averaging these weights for all species in an area, gives an indication of the relative proportion of globally geographically-restricted corals present in the area (Leroy et al. 2013). The SCS reef areas with the highest IRR are the east coast of West Malaysia and northern Palawan (Table 1), which contain globally and regionally rare species such as Euphyllia paradivisa and E. paraglabrescens. In particular, West Malaysia’s east coast harbours 70 species, or 17.6 % of its total species richness, that meet the rarity threshold of B29 ecoregion occupancy. Northern Palawan has far fewer rare species (50), but these include extremely rare corals such as Plerogyra cauliformis and P. multilobata. Each of these species is present in only one ecoregion, although both of them have been recorded in nearby eastern Sabah (Waheed and Hoek- sema 2013). Other noteworthy areas in terms of relative rarity are western Luzon and Brunei, which have slightly lower IRR but contain more rare species overall (66 and 51 respectively) than northern Palawan. While the richness component cannot be completely isolated from our rarity statistics, this set of reef areas does not include southern Vietnam, the second most species-rich area in the SCS, with greater richness than even West Malaysia. Consequently, the choice to focus on either component of biodiversity—richness or rarity—can affect regional priorities of conservation considerably (Prendergast et al. 2002; Lennon et al. 2004; Orme et al. 2005). Note that this set of results is robust to variations in rarity thresholds; the use of 15 and 35 % rather than Gaston’s (1994) quartile definition gives rank contrasts of only 1.75 and 1.00 respectively, with IRR values that are ranked identically among many reef areas. Almost one-third of the SCS species (29.9 %) are threatened according to the IUCN Red List of Threatened Species (Carpenter et al. 2008), including 11 and 160 in EN and VU categories respectively (Table 1). While there are no CR species in the SCS, the proportion of non-DD species facing elevated extinction risk is nearly identical regionally and globally (*33 %). Interestingly, areas with the largest proportions of threatened species—West Malaysia (26.4 %), northern Palawan (24.9 %) and western Luzon (26.6 %)—are also those with the highest relative rarity. This should hardly be surprising given that at the global scale, a greater proportion of range-restricted species (44.7 %) are threatened as compared to those that are more widespread (31.0 %) (Carpenter et al. 2008). That is, the greater the number of threatened species in an area, the more likely it will contain geographically-restricted species. Although the east coast of West Malaysia has the highest number of DD species (16), there is no clear pattern of how IUCN Red List data deficiency relates to the rarity of species within an area. Southern Vietnam, for instance, contains numerous DD species (14) as well, but it ranks eighth in terms of relative rarity. However, when species in the SCS are pooled, DD species occupy only an average of 21 reef ecoregions globally, compared to 36 ecoregions for threatened and 66 for non-threatened species. Indeed, our results suggest that species deemed DD during the IUCN assessment are lacking in data mainly because their global range restriction hinders understanding which is necessary for conservation evaluation (see Robbirt et al. 2006).

123 Biodivers Conserv

Five reef areas stand to lose significantly more PD than expected by the extinction risk of their coral assemblages, including the most species-poor area of southeastern China (Table 1). Excess losses in the latter area and southwestern Vietnam are projected to be 0.62 and 0.53 % respectively, whereas Paracel Islands, West Malaysia’s east coast and northern Vietnam could lose at least an extra 1.20 % of phylogenetic diversity compared to a random extinction event. Threatened species in these areas are thus likely to be clustered on the area phylogeny and/or consist of highly distinctive species (Purvis et al. 2000; Vamosi and Wilson 2008; Huang and Roy 2013). In the Paracel Islands, for example, the excess PD loss is caused mainly by the projected extinction of evolutionarily distinct Vulnerable species Acropora echinata (sister to 42 other Acropora spp. in the area), Isopora brueggemanni (sister to the rest of Isopora), Alveopora excelsa and Heliofungia actiniformis (the only representatives of their genera in the area). The loss of the Vul- nerable, monotypic Physogyra also leads to the depletion of a long phylogenetic branch. By contrast, because West Malaysia’s east coast contains a much larger tree with nearly twice the species richness, it is more likely to have taxa that are closely related to these distinct species. Unfortunately, the clustering of threatened species in particular parts of the tree, such as Isopora, Alveopora and Turbinaria results in imperilment of entire clades. Southeastern China and southwestern Vietnam could also lose significantly more PD than random species extinction, but are less likely than the Paracel Islands, east coast of West Malaysia and northern Vietnam to lose deep lineages. Across the entire SCS, excess PD loss is positive, indicating that the threatened unique lineages in these five reef areas are not buffered from extinction by the rest of the region’s coral fauna. The remaining 11 reef areas stand to lose less PD than if extinction were by chance, suggesting that these areas either contain proportionally fewer threatened long-branch species, or have more instances of persistent species that are closely related to threatened species. Species in an assemblage contribute differently to ecological functioning, but the actual variation is difficult to establish (Cadotte 2013). Nevertheless, phylogenetic diversity has been shown to correlate strongly with ecosystem productivity and stability (Maherali and Klironomos 2007; Cadotte et al. 2008; Flynn et al. 2011). This relationship generally results from the increase in trait diversity as more phylogenetically-diverse species are included in an assemblage. The projected excess decline of PD in the five SCS reef areas mentioned above could therefore spell the inordinate loss of coral traits that are important for local ecosystem functioning. While the link between phylogenetic and functional diversity needs to be tested, trait information for a majority of corals remains scant (Dıáz and Madin 2011; Darling et al. 2012, 2013). Moreover, high diversity systems like coral reefs have historically been expected to possess a certain level of functional redundancy (McCann 2000; Bellwood et al. 2004; Nystro¨m 2006), but more recent research on reef fishes shows that only a limited number of functional groups are actually buffered against species loss (Bellwood et al. 2003, 2006; Mouillot et al. 2014). This dire pattern and lack of coral data suggest that conservation of PD specifically by minimising excess loss over random extinction is a prudent strategy for preserving ecosystem functioning. Furthermore, an enhanced conservation focus on the tree of life is ultimately key to protecting evolutionary heritage, a critical biodiversity component (Purvis and Hector 2000; Mace et al. 2003; Rosauer and Mooers 2013). Overall, our results highlight the need to go beyond the conventional emphasis on species richness when planning for conservation in the SCS (see Devictor et al. 2010). Coral richness, rarity, and phylogenetic diversity differ considerably among reef areas in the region, and their outcomes from projected extinctions due to anthropogenic disturbances are not predicted simply by species numbers. On the one hand, rare species in terms 123 Biodivers Conserv of global ecoregion occupancy are more likely to be threatened with extinction and should be prioritised for conservation (Arponen 2012). West Malaysia’s east coast and the Philippine reef areas harbour the greatest levels of rarity and threat, so clearly, they are of potential conservation interest, yet species-poor areas such as southern China and the Paracel Islands also contain many rare species. On the other hand, areas that stand to lose more-than-expected levels of PD, such as the Paracel Islands, east coast of West Malaysia and southeastern China, are also critical for biodiversity conservation. Taken together, while a few areas with moderate to high species richness (e.g., West Malaysia and the Paracel Islands) feature prominently on the basis of various measures used here, areas containing the fewest species (e.g., China and northern Vietnam) also need to be protected for their contributions to rarity and evolutionary diversity. Given that rare species are known to contribute disproportionately more to the functioning of coral reef ecosystems (Mouillot et al. 2013), it may be more cost effective to target these areas. Ultimately, priorities to be developed must take into account conservation financing and potential returns on investment (Murdoch et al. 2007), as well as diverging socioeconomic costs associated with the protection of large marine regions (Klein et al. 2010). This may require a multilateral framework that prioritises investment at the national level based on com- plementary sets of objectives for achieving regional conservation goals (Beger et al. 2015). Anthropogenic threats to the coral reefs of the SCS include overfishing, destructive fishing, coral mining, the aquarium trade, coastal development, sedimentation and pollu- tion (McManus 1997; Kimura et al. 2008; Tun et al. 2008), all of which have led to an estimated 16 % regional loss of live coral cover between 1994 and 2004 (UNEP 2007). Many reef areas bordering the SCS are under some form of management but conservation effectiveness remains weak for much of the region (UNEP 2007; Vo et al. 2013). Apart from the need to improve management effectiveness, recommendations have been proposed for the development of a network of MPAs as a regional strategy to conserve coral reefs globally (MOE Japan 2010; see also McManus 1994; McManus and Men˜ez 1997; McManus et al. 2010). Our results show that such a network can help preserve a considerable portion and representation of global coral diversity, as well as enhance spatial links for maintaining ecosystem connectivity and resilience (Walton et al. 2014; White et al. 2014). The findings here will also aid conservation planners in efficiently directing different resources to the most suitable reef areas, depending on the goal of individual MPAs (see Bennett et al. 2014), and will provide a foundation for identifying reefs that should be included in an MPA network. For example, an MPA designed to give equal consideration to species richness, rare species and evolutionary diversity ought to include the east coast of West Malaysia as it has the highest IRR (0.0500) and is one of the top two reef areas in projected rate of extinction (26.4 %) and excess PD loss (1.31 %) from a diverse assemblage (398 species). More broadly, the practical tools used here can be applied to areas and taxa in the SCS not covered by our study to attain a more comprehensive understanding of various reef diversity components and extinction risk. Corals are hosts to a large array of associated fauna and the loss of any particular coral could lead to the demise of other species, especially if these are host-specific (Hoeksema et al. 2012). In the SCS, extinctions of large proportions of threatened corals (Table 1) could compromise the complex three-dimensional architecture of coral reefs, putting at risk the existence of reef inhabitants such as fish (Graham et al. 2006; Wilson et al. 2006; Chong-Seng et al. 2012) and invertebrates (Idjadi and Edmunds 2006; Pratchett et al. 2009; Fabricius et al. 2014). Therefore, comprehensive protection of coral species and evolutionary diversity via the formation of an MPA network in the SCS will go a long way towards securing the future of reef faunal assemblages in the region. 123 Biodivers Conserv

Acknowledgments We thank Zarinah Waheed for helping to verify the data, and Kaustuv Roy for ideas and advice. This work was supported by NUS Start-up Grant R-154-000-671-133.

References

Altschul SF, Lipman DL (1990) Equal Anim. Nature 348:493–494. doi:10.1038/348493c0 Arponen A (2012) Prioritizing species for conservation planning. Biodivers Conserv 21:875–893. doi:10. 1007/s10531-012-0242-1 Barbeitos MS, Romano SL, Lasker HR (2010) Repeated loss of coloniality and symbiosis in scleractinian corals. Proc Natl Acad Sci USA 107:11877–11882. doi:10.1073/pnas.0914380107 Beger M, McGowan J, Treml EA et al (2015) Integrating regional conservation priorities for multiple objectives into national policy. Nat Commun 6:8208. doi:10.1038/ncomms9208 Bellwood DR, Hoey AS, Choat JH (2003) Limited functional redundancy in high diversity systems: resilience and ecosystem function on coral reefs. Ecol Lett 6:281–285. doi:10.1046/j.1461-0248.2003.00432.x Bellwood DR, Hughes TP, Folke C, Nystro¨m M (2004) Confronting the coral reef crisis. Nature 429:827–833. doi:10.1038/nature02691 Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Curr Biol 16:2434–2439. doi:10.1016/j.cub.2006.10.030 Bennett JR, Elliott G, Mellish B et al (2014) Balancing phylogenetic diversity and species numbers in conservation prioritization, using a case study of threatened species in New Zealand. Biol Conserv 174:47–54. doi:10.1016/j.biocon.2014.03.013 Cadotte MW (2013) Experimental evidence that evolutionarily diverse assemblages result in higher productivity. Proc Natl Acad Sci USA 110:8996–9000. doi:10.1073/pnas.1301685110 Cadotte MW, Cardinale BJ, Oakley TH (2008) Evolutionary history and the effect of biodiversity on plant productivity. Proc Natl Acad Sci USA 105:17012–17017. doi:10.1073/pnas.0805962105 Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the mainte- nance of ecological processes and services. J Appl Ecol 48:1079–1087. doi:10.1111/j.1365-2664.2011. 02048.x Carpenter KE, Abrar M, Aeby GS et al (2008) One-third of reef-building corals face elevated extinction risk from climate change and local impacts. Science 321:560–563. doi:10.1126/science.1159196 Chong-Seng KM, Mannering TD, Pratchett MS et al (2012) The influence of coral reef benthic condition on associated fish assemblages. PLoS One 7:e42167. doi:10.1371/journal.pone.0042167 Clifton J (2009) Science, funding and participation: key issues for marine protected area networks and the Coral Triangle Initiative. Environ Conserv 36:91–96. doi:10.1017/S0376892909990075 Curnick DJ, Head CEI, Huang D et al (2015) Setting evolutionary-based conservation priorities for a phylogenetically data-poor taxonomic group (Scleractinia). Anim Conserv 18:303–312. doi:10.1111/ acv.12185 D’agata S, Mouillot D, Kulbicki M et al (2014) Human-mediated loss of phylogenetic and functional diversity in coral reef fishes. Curr Biol 24:555–560. doi:10.1016/j.cub.2014.01.049 Darling ES, Alvarez-Filip L, Oliver TA et al (2012) Evaluating life-history strategies of reef corals from species traits. Ecol Lett 15:1378–1386. doi:10.1111/j.1461-0248.2012.01861.x Darling ES, McClanahan TR, Coˆte´ IM (2013) Life histories predict coral community disassembly under multiple stressors. Glob Chang Biol 19:1930–1940. doi:10.1111/gcb.12191 Davies TJ, Fritz SA, Grenyer R et al (2008) Phylogenetic trees and the future of mammalian biodiversity. Proc Natl Acad Sci USA 105:11556–11563. doi:10.1073/pnas.0801917105 Devictor V, Mouillot D, Meynard C et al (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 3:1030–1040. doi:10.1111/j.1461-0248.2010.01493.x Dıáz M, Madin JS (2011) Macroecological relationships between coral species’ traits and disease potential. Coral Reefs 30:73–84. doi:10.1007/s00338-010-0668-4 Fabricius KE, De’ath G, Noonan S, Uthicke S (2014) Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc Roy Soc B-Biol Sci 281:20132479. doi:10.1098/rspb.2013.2479 Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. doi:10.1016/ 0006-3207(92)91201-3 Faith DP, Magalloń S, Hendry AP et al (2010) Evosystem services: an evolutionary perspective on the links between biodiversity and human well-being. Curr Opin Environ Sustain 2:66–74. doi:10.1016/j.cosust. 2010.04.002

123 Biodivers Conserv

Flynn DFB, Mirotchnick N, Jain M et al (2011) Functional and phylogenetic diversity as predictors of biodiversity–ecosystem-function relationships. Ecology 92:1573–1581. doi:10.1890/10-1245.1 Forest F, Grenyer R, Rouget M et al (2007) Preserving the evolutionary potential of ﬂoras in biodiversity hotspots. Nature 445:757–760. doi:10.1038/nature05587 Fritz SA, Purvis A (2010) Phylogenetic diversity does not capture body size variation at risk in the world’s mammals. Proc Roy Soc B 277:2435–2441. doi:10.1098/rspb.2010.0030 Gaston KJ (1994) Rarity. Chapman & Hall, London Gittenberger A, Reijnen BT, Hoeksema BW (2011) A molecularly based phylogeny reconstruction of mushroom corals (Scleractinia: Fungiidae) with taxonomic consequences and evolutionary implications for life history traits. Contrib Zool 80:107–132 Graham NAJ, Wilson SK, Jennings S et al (2006) Dynamic fragility of oceanic coral reef ecosystems. Proc Natl Acad Sci USA 103:8425–8429. doi:10.1073/pnas.0600693103 Harnik PG, Simpson C, Payne JL (2012) Long-term differences in extinction risk among the seven forms of rarity. Proc Roy Soc B 279:4969–4976. doi:10.1098/rspb.2012.1902 Hoeksema BW (1989) Taxonomy, phylogeny and biogeography of mushroom corals (Scleractinia: Fungi- idae). Zool Verh Leiden 254:1–295 Hoeksema BW (1993) Historical biogeography of Fungia (Pleuractis) spp. (Scleractinia: Fungiidae), including a new species from the Seychelles. Zool Meded Leiden 67:639–654 Hoeksema BW (2012) Evolutionary trends in onshore-offshore distribution patterns of mushroom coral species (Scleractinia: Fungiidae). Contrib Zool 81:199–221 Hoeksema BW (2015) Latitudinal species diversity gradient of mushroom corals off eastern Australia: a baseline from the 1970s. Estuar Coast Shelf Sci 165:190–198. doi:10.1016/j.ecss.2015.05.015 Hoeksema BW, van der Meij SET, Fransen CHJM (2012) The mushroom coral as a habitat. J Mar Biol Assoc UK 92:647–663. doi:10.1017/S0025315411001445 Hooper DU, Chapin FS III, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35. doi:10.1890/04-0922 Hooper DU, Adair EC, Cardinale BJ et al (2012) A global synthesis reveals biodiversity loss as a major driver of ecosystem change. Nature 486:105–108. doi:10.1038/nature11118 Huang D (2012) Threatened reef corals of the world. PLoS One 7:e34459. doi:10.1371/journal.pone. 0034459 Huang D, Roy K (2013) Anthropogenic extinction threats and future loss of evolutionary history in reef corals. Ecol Evol 3:1184–1193. doi:10.1002/ece3.527 Huang D, Licuanan WY, Hoeksema BW et al (2015) Extraordinary diversity of reef corals in the South China Sea. Mar Biodivers 45:157–168. doi:10.1007/s12526-014-0236-1 Idjadi JA, Edmunds PJ (2006) Scleractinian corals as facilitators for other invertebrates on a Caribbean reef. Mar Ecol Prog Ser 319:117–127. doi:10.3354/meps319117 Isaac NJB, Turvey ST, Collen B et al (2007) Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLoS One 2:e296. doi:10.1371/journal.pone.0000296 IUCN (2001) IUCN Red List Categories and Criteria: Version 3.1. IUCN, Gland, Switzerland and Cambridge Jain M, Flynn DFB, Prager CM et al (2014) The importance of rare species: a trait-based assessment of rare species contributions to functional diversity and possible ecosystem function in tall-grass prairies. Ecol Evol 4:104–112. doi:10.1002/ece3.915 Jones AM, Berkelmans R, Houston W (2011) Species richness and community structure on a high latitude reef: implications for conservation and management. Diversity 3:329–355. doi:10.3390/d3030329 Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. doi:10.1093/bioinformatics/btq166 Kimura T, Dai C-F, Park H-S et al (2008) Status of coral reefs in East and North Asia (China, Hong Kong, Taiwan, South Korea and Japan). In: Wilkinson C (ed) Status of Coral Reefs of the World: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, pp 145–158 Klein CJ, Ban NC, Halpern BS et al (2010) Prioritizing land and sea conservation investments to protect coral reefs. PLoS One 5:e12431. doi:10.1371/journal.pone.0012431 Lennon JJ, Koleff P, Greenwood JJD, Gaston KJ (2004) Contribution of rarity and commonness to patterns of species richness. Ecol Lett 7:81–87. doi:10.1046/j.1461-0248.2004.00548.x Leroy B, Petillon J, Gallon R et al (2012) Improving occurrence-based rarity metrics in conservation studies by including multiple rarity cut-off points. Insect Conserv Divers 5:159–168. doi:10.1111/j.1752-4598. 2011.00148.x Leroy B, Canard A, Ysnel F (2013) Integrating multiple scales in rarity assessments of invertebrate taxa. Divers Distrib 19:794–803. doi:10.1111/ddi.12040

123 Biodivers Conserv

Lyons KG, Brigham CA, Traut BH, Schwartz MW (2005) Rare species and ecosystem functioning. Conserv Biol 19:1019–1024. doi:10.1111/j.1523-1739.2005.00106.x Mace GM, Gittleman JL, Purvis A (2003) Preserving the tree of life. Science 300:1707–1709. doi:10.1126/ science.1085510 Madin EMP (2015) Halt reef destruction in South China Sea. Nature 524:291. doi:10.1038/524291a Maherali H, Klironomos JN (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science 316:1746–1748. doi:10.1126/science.1143082 May RM (1990) Taxonomy as destiny. Nature 347:129–130. doi:10.1038/347129a0 McCann KS (2000) The diversity–stability debate. Nature 405:228–233. doi:10.1038/35012234 McManus JW (1994) The Spratly Islands: a marine park? Ambio 23:181–186 McManus JW (1997) Tropical marine fisheries and the future of coral reefs: a brief review with emphasis on Southeast Asia. Coral Reefs 16:S121–S127. doi:10.1007/s003380050248 McManus JW, Men˜ez LAB (1997) The proposed international Spratly Island marine park: ecological considerations. In: Proceedings of the 8th international coral reef symposium, vol 2, pp 1943–1948 McManus JW, Shao K-T, Lin S-Y (2010) Toward establishing a Spratly Islands international Marine Peace Park: ecological importance and supportive collaborative activities with an emphasis on the role of Taiwan. Ocean Dev Int Law 41:270–280. doi:10.1080/00908320.2010.499303 MOE Japan (2010) ICRI East Asia regional strategy on MPA Networks 2010. Ministry of the Environment, Tokyo Morton B, Blackmore G (2001) South China Sea. Mar Pollut Bull 42:1236–1263 Mouillot D, Bellwood DR, Baraloto C et al (2013) Rare species support vulnerable functions in high- diversity ecosystems. PLoS Biol 11:e1001569. doi:10.1371/journal.pbio.1001569 Mouillot D, Ville´ger S, Parravicini V et al (2014) Functional over-redundancy and high functional vul- nerability in global fish faunas on tropical reefs. Proc Natl Acad Sci USA 111:13757–13762. doi:10. 1073/pnas.1317625111 Murdoch W, Polasky S, Wilson KA et al (2007) Maximizing return on investment in conservation. Biol Conserv 139:375–388. doi:10.1016/j.biocon.2007.07.011 Nee S, May RM (1997) Extinction and the loss of evolutionary history. Science 278:692–694. doi:10.1126/ science.278.5338.692 Nystro¨m M (2006) Redundancy and response diversity of functional groups: implications for the resilience of coral reefs. Ambio 35:30–35. doi:10.1579/0044-7447-35.1.30 Orme CDL, Davies RG, Burgess M et al (2005) Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–1019. doi:10.1038/nature03850 Orme CDL, Freckleton RP, Thomas GH, et al. (2013) caper: Comparative Analyses of Phylogenetics and Evolution in R. R Package Version 0.5.2. http://caper.r-forge.r-project.org. Accessed 19 Feb 2014 Parhar RK, Mooers AØ (2011) Phylogenetically clustered extinction risks do not substantially prune the Tree of Life. PLoS One 6:e23528. doi:10.1371/journal.pone.0023528 Posadas P, Esquivel DRM, Crisci JV (2001) Using phylogenetic diversity measures to set priorities in conservation: an example from southern South America. Conserv Biol 15:1325–1334 Pratchett MS, Wilson SK, Graham NAJ, Munday PL (2009) Coral bleaching and consequences for motile reef organisms: past, present and uncertain future effects. In: van Oppen MJH, Lough JM (eds) Ecological studies: coral bleaching. Springer, Berlin, pp 139–158 Prendergast PR, Quinn RM, Lawton JH et al (2002) Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365:335–337. doi:10.1038/365335a0 Purvis A, Hector A (2000) Getting the measure of biodiversity. Nature 405:212–219. doi:10.1038/35012221 Purvis A, Agapow P-M, Gittleman JL, Mace GM (2000) Nonrandom extinction and the loss of evolutionary history. Science 288:328–330. doi:10.1126/science.288.5464.328 R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 19 Feb 2014 Randall JE, Lim KKP (2000) A checklist of the fishes of the South China Sea. Raffles Bull Zool Suppl 8:569–667 Robbirt KM, Roberts DL, Hawkins JA (2006) Comparing IUCN and probabilistic assessments of threat: do IUCN red list criteria conflate rarity and threat? Biodivers Conserv 15:1903–1912. doi:10.1007/ s10531-005-4307-2 Roberts CM, McClean CJ, Veron JEN et al (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295:1280–1284. doi:10.1126/science.1067728 Rodrigues ASL, Gaston KJ (2002) Maximising phylogenetic diversity in the selection of networks of conservation areas. Biol Conserv 105:103–111. doi:10.1016/S0006-3207(01)00208-7 Rosauer DF, Mooers AØ (2013) Nurturing the use of evolutionary diversity in nature conservation. Trends Ecol Evol 28:322–323. doi:10.1016/j.tree.2013.01.014

123 Biodivers Conserv

Sechrest W, Brooks TM, da Fonseca GAB et al (2002) Hotspots and the conservation of evolutionary history. Proc Natl Acad Sci USA 99:2067–2071. doi:10.1073/pnas.251680798 Tun K, Chou LM, Yeemin T et al (2008) Status of coral reefs in Southeast Asia. In: Wilkinson C (ed) Status of coral reefs of the world: 2008. Global Coral Reef Monitoring Network and Reef and Rainforest Research Centre, Townsville, pp 131–144 UNEP (2007) Reversing environmental degradation trends in the South China Sea and Gulf of Thailand. Report of the Eighth Meeting of the Regional Working Group on Coral Reefs. UNEP/GEF/SCS/RWG- CR.8/3, Bangkok Vamosi JC, Wilson JRU (2008) Nonrandom extinction leads to elevated loss of angiosperm evolutionary history. Ecol Lett 11:1047–1053. doi:10.1111/j.1461-0248.2008.01215.x Vane-Wright RI, Humphries CJ, Williams PH (1991) What to protect?—systematics and the agony of choice. Biol Conserv 55:235–254. doi:10.1016/0006-3207(91)90030-D Veron JEN, DeVantier LM, Turak E et al (2009) Delineating the Coral Triangle. Galaxea 11:91–100. doi:10. 3755/galaxea.11.91 Veron JEN, DeVantier LM, Turak E et al (2011) The Coral Triangle. In: Dubinsky Z, Stambler N (eds) Coral Reefs: an ecosystem in transition. Springer, Dordrecht, pp 47–55 Veron J, Stafford-Smith M, DeVantier L, Turak E (2015) Overview of distribution patterns of zooxan- thellate Scleractinia. Front Mar Sci 1:81. doi:10.3389/fmars.2014.00081 Vo ST, Pernetta JC, Paterson CJ (2013) Status and trends in coastal habitats of the South China Sea. Ocean Coast Manag 85:153–163. doi:10.1016/j.ocecoaman.2013.02.018 Vo ST, DeVantier LM, Tuyen HT, Hoa`ng PK (2014) Ninh Hai waters (south Vietnam): a hotspot of reef corals in the western South China Sea. Raffles Bull Zool 62:513–520 Waheed Z, Hoeksema BW (2013) A tale of two winds: species richness patterns of reef corals around the Semporna peninsula, Malaysia. Mar Biodivers 43:37–51. doi:10.1007/s12526-012-0130-7 Walton A, White AT, Tighe S et al (2014) Establishing a functional region-wide Coral Triangle Marine Protected Area System. Coast Manag 42:107–127. doi:10.1080/08920753.2014.877765 White AT, Alinõ PM, Cros A et al (2014) Marine protected areas in the Coral Triangle: progress, issues, and options. Coast Manag 42:87–106. doi:10.1080/08920753.2014.878177 Wilson SK, Graham NAJ, Pratchett MS et al (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Glob Chang Biol 12:2220–2234. doi:10.1111/j.1365- 2486.2006.01252.x Witting L, Loeschcke V (1995) The optimization of biodiversity conservation. Biol Conserv 71:205–207. doi:10.1016/0006-3207(94)00041-N Zhang SY, Speare KE, Long ZT et al (2014) Is coral richness related to community resistance to and recovery from disturbance? PeerJ 2:e308. doi:10.7717/peerj.308

123