Please cite this article in press as: Hughes et al., Double Jeopardy and Global Extinction Risk in Corals and Reef Fishes, CurrentBiology (2014), http://dx.doi.org/10.1016/j.cub.2014.10.037

Double Jeopardy and Global

Current Biology 24, 1–6, December 15, 2014 ª2014 Elsevier Ltd All rights reserved http://dx.doi.org/10.1016/j.cub.2014.10.037

ReportExtinction

Risk in Corals and Reef Fishes

Terry P. Hughes,1,* David R. Bellwood,1,2

Sean R. Connolly,1,2 Howard V. Cornell,3

and Ronald H. Karlson4,5

1Australian Research Council Centre of Excellence for CoralReef Studies, James Cook University, Townsville, QLD 4811,Australia2College of Marine and Environmental Sciences, James CookUniversity, Townsville, QLD 4811, Australia3Department of Environmental Science and Policy,University of California, Davis, Davis, CA 95616, USA4Department of Biological Sciences, University of Delaware,Newark, DE 19716, USA

Summary

Coral reefs are critically important ecosystems that support

the food security and livelihoods of hundreds of millionsof people inmaritime tropical countries, yet they are increas-

ingly threatened by overfishing, coastal pollution, climatechange, and other anthropogenic impacts, leading to con-

cerns that some species may be threatened with local oreven global extinction [1–7]. The concept of double jeopardy

proposes that the risk of species extinction is elevated ifspecies that are endemic (small range) are also scarce (low

local abundance) [8]. Traditionally, marine macroecologyhas been founded on patterns of species richness and pres-

ence-absence data [9–11], which provide no information onspecies abundances or on the prevalence of double jeop-

ardy. Here we quantify the abundances of >400 species ofcorals and fishes along one of the world’s major marine

biodiversity gradients, from the Coral Triangle hotspot toFrench Polynesia, a distance of approximately 10,000 km.

In contrast to classical terrestrial studies [12], we find thatthe abundance of these species bears no relationship to

the size of their geographic ranges. Consequently, doublejeopardy is uncommon because endemics are often locally

abundant, and conversely many pandemics are rare. TheCoral Triangle hotspot has more numerically rare species

(both endemic and pandemic) but also encompassesmore species with intermediate and higher abundances.

We conclude that conservation efforts in the sea shouldfocus less on extinction risk and more on maintaining

and rebuilding key ecological functions that are highlyvulnerable to human pressures, even if species can avoid

extinction.

Results and Discussion

Intuitively, a more expansive geographic range should reducethe likelihood of global extinction because the risk of extirpa-tion is spread across many locations. Similarly, greaterabundance and a larger population size should reduce thelikelihood of extinction due to chance or inbreeding [12]. Thedouble-jeopardy concept arose from empirical observations

5Present address: 266 Carters Mill Road, Elkton, MD 21921, USA

*Correspondence: terry.hughes@jcu.edu.au

that the macroecological relationship between geographicdistribution and local abundance is often strongly positiveamong suites of terrestrial species [12–14], and it has becomean important element in many qualitative Red List assess-ments of extinction risk [15, 16]. A comprehensive meta-anal-ysis of the relationship between distribution and abundance indifferent environments indicated that only 3 of 82 originalstudies were undertaken in the marine realm [17]. In contrastto classical studies [12–14], we find little evidence of doublejeopardy for either the principal structure-formers or majorconsumers on coral reefs: along the Pacific biodiversitygradient (Figure 1), the size of a species’ geographic rangebears no relationship to its local abundance among 321 spe-cies of reef-building corals or for 115 species of parrotfishand wrasses (Figure 2). Separate analyses for the speciespool of corals and fishes occurring on reef flats, crests, orreef slopes also show very weak or no relationships betweenthe size of each species range and their abundances in eachof these habitats (Figures S1–S3). Furthermore, the same flatrange-abundance relationship is exhibited for large- versussmall-bodied fish species, for brooding versus spawningcorals, and for corals that are reportedly more resilient to coralbleaching and disease (Figure S4).For both corals and a diverse suite of labrid reef fishes, the

average local abundance of species varied by three to four or-ders of magnitude from the most common to the rarest (Fig-ure 3), whereas geographic range size varied by 200-fold incorals and 1,300-fold among species of fish (Figure 2). Con-trary to the double-jeopardy concept, the spectrum of abun-dances of pandemic and endemic species is equally broad(Figure 2). There is no trend for the numerically rarest speciesto have smaller ranges than co-occurring species thatare >100 times more abundant. Although large-scale abun-dance data for other taxonomic groups are very sparse, ourocean-scale results are supported by earlier smaller-scalestudies of butterflyfishes (family Chaetodontidae), surgeon-fishes (family Acanthuridae), and an array of other fishes thatare restricted to oceanic islands or small archipelagos. Theseendemics are often numerically dominant compared to mostco-occurring pandemics [19, 20], further suggesting that thelack of a positive abundance-range size relationship is a gen-eral phenomenon on coral reefs. Similarly, on land, someendemic species can be locally abundant [21], contributingin some cases to significant negative interspecific relation-ships between abundance and distribution [17].Our findings refute the common assumption that the Coral

Triangle hotspot is generated by the co-occurrence of adisproportionately large number of numerically rare, endemicspecies. The spectrum of species abundances does indeedvary strikingly among biogeographic regions, with the globalcenter of reef biodiversity in the Coral Triangle having morerare corals and fish species (Figure 3). However, manyof the numerically rare species we measured in the CoralTriangle hotspot and elsewhere are pandemics rather thanendemics (Figure 2). Unexpectedly, the Coral Triangle alsohas more coral species with intermediate and high abun-dances compared to more depauperate regions to the east(Figure 3A), and many of these more abundant species areendemics.

501-600401-500301-400201-300101-2000-100

FrenchPolynesiaSamoa

SolomonIslands

Micronesia

Papua NewGuineaIndonesiadddddddddddddddddddddddddddddddddddddd eeeeeeeee

Figure 1. Planet Earth, Showing Locations of

Islands that Were Sampled across the Western

and Central Pacific Ocean

Local abundances of coral (circles) and fishes (tri-

angles) were measured at multiple sites and hab-

itats (reef flat, crest, and slope) on each island.

Also shown are contours of species richness

for corals [18], indicating the steep latitudinal

gradient in biodiversity across the Pacific Ocean.

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Almost all of the west-east decline in species richnessalong the Pacific diversity gradient represents the stepwiseloss of smaller-range Coral Triangle species that reach theirgeographical limits at faunal breaks between the regions weexamined [9–11]. Consequently, the paucity of endemic spe-cies that are also rare in our samples (species with doublejeopardy, in the bottom left of Figure 2) is consistent with thesharp drop in endemism in regions eastward of the CoralTriangle and with the negatively skewed distribution of rangesizes of corals and reef fishes in the tropical Indo-Pacific [9].The gradient in species richness in the habitats that wesampled is steeper for corals (274 species in Indonesia,declining 4-fold to 67 in French Polynesia) compared to labridreef fishes (85 species in Indonesia, decreasing 2-fold to 46species in French Polynesia). The number of abundant coralspecies decreases along with the number of rare species ateach successive region across the biodiversity gradient,whereas the number of abundant species of fishes is main-tained across a huge swath of the Pacific (Figure 3).

Extinction Risk on Coral Reefs

Despite extensive research on the degradation of the world’scoral reefs over the past half-century, there is only a singledocumented instance of extinction of a reef fish and of a spe-cies of reef-building coral [22, 23]. In these two cases, doublejeopardy did apply: both of these recently extinct reef specieshad very small populations and were endemic to sparse andmarginal habitats in the remote Eastern Pacific [24, 25]. How-ever, the overwhelming majority of reef fishes and especially

corals have very large geographicranges and much larger populationscompared to these two extinct species(Figure 2). For example, many endemiccorals in the Coral Triangle hotspotspan a region of 5.5 million km2 (anarea equivalent to two-thirds of the con-tinental US) that encompasses 30% ofthe world’s coral reef habitat. Whenrange size is calculated on the basis ofreef area, 8% of the corals and 10%of the fish species that we examinedfrom Indonesia to French Polynesia fallinto the bottom quartile for both rangesize and local abundance (Figures 2Band 2D). Clearly, this estimate of doublejeopardy depends entirely on an arbi-trary definition of how many millionsof square kilometers of ocean, or tensof thousands of square kilometers ofreef area, constitute a small range (Fig-ure 2). Endemic corals and fishes (i.e.,species that fall within the bottom quar-tile of ranges in the Indo-Pacific [9])

nonetheless typically have substantially larger geographic dis-tributions than most cosmopolitan North American mammals,birds, or plants. Moreover, our results show that the localabundances of species of corals and fishes with relativelysmaller ranges are often as high as or higher than pandemics(Figure 2), indicating that double jeopardy is a comparativelyrare phenomenon on coral reefs, especially in the biogeo-graphic hotspot where the bulk of the world’s coral reefs lie(Figure 1) and where peak numbers of species with intermedi-ate and higher abundances co-occur (Figure 3).Studies of life histories and population biology are inevitably

biased toward a small subset of species that are abundant andwidespread. Common and relatively well-studied corals showa very broad diversity of demographic and life-history traitssuch as brooding or spawning, fast or slow growth, or shortversus long life [26, 27]. Similarly, abundant and broadlydistributed reef fishes occupy all trophic levels and exhibit ahuge spectrum of body sizes and life histories [28]. The spe-cies that we identified as both numerically rare and endemic(Figure 2) also do not conform to a specific subset of lifehistories ormorphologies. For example, the corals with doublejeopardy (in the bottom quartile for abundance and range size)are aclonal or clonal and are free-living, encrusting, hemi-spherical, bushy, or tree like. Although their natural history ispoorly understood, only two of these uncommon and endemiccoral species (Acropora suharsonoi and Anacropora puerto-galerae) are restricted to one of the three habitats that we sur-veyed, the reef slope at 6–7 m, although they also extend todepths of >20 m [29]. Similarly, only one numerically rare and

0.01

0.1

1

Mea

n co

ral p

erce

ntag

e co

ver

A Corals R2 = 0.017 B Corals R2 < 0.01

Range extent ( x 106, km2)

0 20 40 60 80 100

1010

010

00

Mea

n fis

h ab

unda

nce

( ha

-1)

C Fishes R2 < 0.01

Reef area ( x 104, km2)

0 5 10 15 20 25

D Fishes R2 < 0.01

Figure 2. Relationship between Geographic Range and Mean Local Abundance for Species of Corals and Reef Fishes

Local abundance is measured as percentage coral cover (A and B) and density of reef fishes (C and D). Range is calculated as the total area within a species

geographic boundary, excluding land (A and C), and as the summed area of reefs encompassed by each range boundary (B and D). Data points represent

individual species (n = 323 species of corals and n = 115 species of labrid fishes). The spread of ranges along the x axes indicates the arbitrary distinction

between endemics (to the left) and pandemics (to the right). See also Figures S1–S4 and Tables S1 and S2.

Double Jeopardy and Extinction Risk on Coral Reefs3

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endemic fish species,Halichoeres pallidus, is absent from reefflats and crests, and its depth range on reef slopes extends to>70 m [30], suggesting that species with double jeopardy donot routinely face the further risk of being habitat specialists.Furthermore, we found the same abundance-range relation-ship for species of corals and fishes that are considered tobe more versus less sensitive to environmental stressors(Figure S4).

Our findings call into question the growing practice of as-sessing extinction risk of coral reef species from fragmentaryinformation on trends in overall community abundance (suchas total coral cover or fish biomass for all species combined).For example, one recent study posited that one-third of theworld’s reef-building corals (i.e., 231 species) are vulnerableto extinction, endangered, or critically endangered [31],despite a lack of regional-scale data on the abundance of indi-vidual species. In a second risk assessment, only 16% ofcorals (i.e., seven species) in the depauperate and extremelyisolated tropical Eastern Pacific were considered to fall intothe same extinction risk categories, despite their isolation,proportionately high levels of endemism, small population

sizes, and vulnerability to volatile El Nino events [25]. In a thirdassessment, only 1.7% of parrotfishes and surgeonfishes(three species) were assessed as having an elevated risk ofglobal extinction using IUCN criteria [32], even though manyspecies in these two taxonomic groups are subject to heavyfishing pressure over much of their geographic range [33], re-sulting in reductions in population size that are likely to becomparable to the decline in many vulnerable coral species.Thus, the accuracy of global and regional threat assessmentsof coral reef species, and their consistency across regions andmajor reef taxa, is currently unclear. Indeed, a petition to list 83species of corals as endangered or threatened under the USEndangered Species Act (ESA) was only partially acceptedby the US National Oceanographic and Atmospheric Adminis-tration (NOAA) in August 2014, despite their preexisting IUCNrisk classification [31]: 63 of the Red Listed coral specieswere not considered to be under threat of extinction byNOAA [34].Five of the 15 species of Indo-Pacific corals that are now

listed as threatened under the ESA [34] have geographicdistributions that overlap with the regions and habitats that

A B

Figure 3. Rank Abundance Curves for Species in Multiple Regions across the Pacific Biodiversity Gradient

Note the large span of abundances of individual species of corals (A) and fishes (B) and biogeographic shifts in the spectrum of abundances along the Pacific

biodiversity gradient. See also Tables S3 and S4.

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we sampled (Figure 1): Acropora globiceps, A. retusa,A. speciosa, Isopora crateriformis, and Montipora australien-sis. However, none of these species fall in the bottom quartileof the spectrum of range sizes of Indo-Pacific corals [9] or inthe bottom quartile of species abundances in the biogeo-graphic regions that we sampled (Table S1). Consequently,we consider their risk of global extinction to be very low andlikely to be far lower than that for >250 other species of Indo-Pacific and Atlantic corals that are less abundant and/orhave more restricted ranges.

In contrast to terrestrial mammals or birds, whose biologyhas substantially informed the development of IUCN RedList criteria, the vast majority of marine plants and animals(including corals and most fishes) are comparatively resistantto global extinction because of their high fecundities, ability todisperse widely and recolonize, relatively large populationsizes, and geographic ranges that typically span tens of mil-lions of square kilometers or more in extent (Figure 2). IUCNthreatened species categories may be reasonable first-orderapproaches for assessing extinction risk for large terrestrialmammals or birds with small effective population sizes thatnumber in the hundreds or less [15, 16]. However, for marineinvertebrates and fishes, application of these same methodol-ogies and assumptions produces assessments that, in mostcases, are unlikely to reflect actual extinction risks in the sea.

In conclusion, although our results offer positive news forthe vulnerability of coral reef species to imminent globalextinction, we emphasize that a low extinction risk affords nogrounds for complacency about the future of coral reef eco-systems. In this respect, a renewed focus on local actionto avert or recoup the loss of ecosystem function causedby habitat destruction and severe depletion of key species(ecological extinction) is likely to be a more productiveapproach to conservation and management than makinglong lists of species thatmay ormay not be globally threatenedwith extinction. The contemporary loss of habitat and localdepletion of functional groups directly impacts ecosystemsand the important goods and services that they provide,

even when the future global extirpation of the last individualin a species remains a comparatively remote possibility.

Experimental Procedures

Coral abundances and numbers of species were recorded on fringing

reefs in five regions spanning the western and central Pacific: Indonesia,

Papua New Guinea, Solomon Islands, American Samoa, and French Poly-

nesia (the Society Islands; Figure 1). We used a hierarchical sampling

design to ensure that all regions were sampled with the same intensity,

to allow comparisons of rarity and commonness. In each region, four

matched sites on each of three islands were sampled. To maximize the

number of species encountered, we measured abundances separately in

three habitats (the reef flat at 0.5–1 m depth, crest at 1–2 m, and reef slope

at 6–7 m) at each of the 60 sites (five regions 3 three islands 3 four sites),

using ten 10-m-long line-intercept transects per habitat. Transects were

laid parallel to depth contours and were draped over the substratum

in each habitat, and all coral colonies >1 cm in size intercepted by the

tape were identified to species and measured in situ to record species-

level abundances. Following normal convention for clonal organisms,

abundance was measured as cover of each species rather than counts

of colonies. Abundances were calculated as the number of centimeters

of tape overlying each species converted to percentage cover along a

10 m transect, separately for each habitat and also pooled for the three

habitats at each site (30 transects per site). For local abundance (Figure 2),

an average was calculated for all sites (up to 60) where each species was

present. For regional abundance distributions (Figure 3), coral cover and

fish counts were averaged for all sites in each region including zero values.

Over all regions and habitats, we identified and measured a total of 41,710

coral colonies along the 1,800 transects, comprising 323 scleractinian

species.

A similar sampling design was used to measure species richness and

abundances of all fishes from the family Labridae (i.e., parrotfishes and

wrasses) in Indonesia, Papua New Guinea, Micronesia, Samoa, and French

Polynesia. We chose this diverse family because of its ecological impor-

tance throughout the Indo-Pacific and because it encompasses a broad

spectrum body sizes, trophic levels, and life histories. In each region, spe-

cies-level abundances were measured on fringing reefs at four sites on

two islands. At each of the eight sites per region, fish were counted along

a 20 min transect in each of the same three habitats as for corals (reef flat,

crest, and reefs slope). Fish larger than 10 cm in length were counted on

5-m-wide belt transects, whereas those smaller than 10 cm were counted

on 1-m-wide belt transects. For standardization of the sampling effort,

Double Jeopardy and Extinction Risk on Coral Reefs5

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20% of the individuals counted on the wider transects were chosen at

random from each site and were used in the abundance plots shown in

the Results and Discussion. The resulting subsampled data set encom-

passed 20,978 individuals and 115 species. All field work was conducted

by a small taxonomically trained team led by T.P.H. (corals) and D.R.B.

(fishes) to ensure consistency in data collection and sampling effort at all

locations. For both taxa, we recorded abundances only in the three most

prevalent habitats (reef flat, crest, and slope) that occur ubiquitously across

the Pacific biodiversity gradient.

We used a spatial database of geographic range boundaries of corals

[35] to map the ranges of the species whose abundances were recorded

in the field. Fish ranges were based on IUCN distribution records (IUCN

Red List of Threatened Species, Version 2012.1, http://www.iucnredlist.

org; downloaded on October 22, 2012). Ranges were measured in two

ways: the total area within each species’ boundary (minus any land areas)

and the area of reef habitat within each range based on the global distribu-

tion of coral reefs [10]. Abundance data reported in the paper are presented

in Tables S1 and S2. Species with double jeopardy were identified by

plotting local abundance versus range size. We also examined abun-

dance-range relationships in species with traits that may affect the risk

of extinction: small versus large body size in fishes [30], reproductive

mode in corals [36], and the capacity of corals to recover quickly from

disease or thermal bleaching [31].

Supplemental Information

Supplemental Information includes four figures and four tables and can be

found with this article online at http://dx.doi.org/10.1016/j.cub.2014.10.037.

Acknowledgments

This work was supported by grants and fellowships from the Australian

Research Council, the US National Science Foundation, the National

Geographic Society, and James Cook University. We thank A.H. Baird,

M.J Boyle, E.A. Dinsdale, C.H.R. Goatley, M. Hisano, A. Hoey, P. Osmond,

J. Wolstenholme, and M.A.L. Young for technical assistance.

Received: June 5, 2014

Revised: July 24, 2014

Accepted: October 13, 2014

Published: November 13, 2014

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