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Marine Pollution Bulletin 56 (2008) 1008–1014

Note

Diseases leading to accelerated decline of reef corals in the largestSouth Atlantic reef complex (Abrolhos Bank, eastern Brazil)

Ronaldo B. Francini-Filho a,b,*, Rodrigo L. Moura b, Fabiano L. Thompson c,Rodrigo M. Reis a, Les Kaufman d, Ruy K.P. Kikuchi a, Zelinda M.A.N. Leao a

a Grupo de Pesquisas em Recifes de Corais e Mudanc�as Globais, Universidade Federal da Bahia (UFBA), Rua Caetano Moura 123,

40210-340 Salvador, BA, Brazilb Conservation International Brazil, Marine Program, Rua das Palmeiras 451, 45900-000 Caravelas, BA, Brazil

c Instituto de Biologia, Universidade Federal do Rio de Janeiro (UFRJ), Ilha do Fundao, Caixa Postal 68011, CEP 21944-970 Rio de Janeiro, RJ, Brazild Boston University Marine Program, 5 Cummington Street Boston, MA 02215, USA

Abstract

Although reef corals worldwide have sustained epizootics in recent years, no coral diseases have been observed in the southwesternAtlantic Ocean until now. Here we present an overview of the main types of diseases and their incidence in the largest and richest coralreefs in the South Atlantic (Abrolhos Bank, eastern Brazil). Qualitative observations since the 1980s and regular monitoring since 2001indicate that coral diseases intensified only recently (2005–2007). Based on estimates of disease prevalence and progression rate, as well ason the growth rate of a major reef-building coral species (the Brazilian-endemic Mussismilia braziliensis), we predict that eastern Brazil-ian reefs will suffer a massive coral cover decline in the next 50 years, and that M. braziliensis will be nearly extinct in less than a century ifthe current rate of mortality due to disease is not reversed.� 2008 Elsevier Ltd. All rights reserved.

Keywords: Coral reefs; Infectious diseases; Prevalence; White plague; Mussismilia

1. Introduction

Coral diseases have flourished since the 1980s, and nowrepresent a major cause of the loss of coral biodiversity andcoral coverage worldwide (Harvell et al., 1999, 2002;Rosenberg and Loya, 2004). The Caribbean region is con-sidered a hotspot for diseases due to increased virulence,rapid spread of pathogens, increased numbers of affectedspecies and the emergence of new diseases (Green andBruckner, 2000; Bruckner, 2002). In recent years, infectiousdiseases have also appeared as a major cause of coral deg-radation in the Indo-Pacific Ocean (Raymundo et al., 2005;Kaczmarsky, 2006).

0025-326X/$ - see front matter � 2008 Elsevier Ltd. All rights reserved.

doi:10.1016/j.marpolbul.2008.02.013

* Corresponding author. Address: Grupo de Pesquisas em Recifes deCorais e Mudanc�as Globais, Universidade Federal da Bahia (UFBA),Rua Caetano Moura 123, 40210-340 Salvador, BA, Brazil. Tel./fax: +5573 32971499.

E-mail address: rofilho@yahoo.com (R.B. Francini-Filho).

Brazilian reefs are populated by an impoverished fauna(about 20 scleractinian coral species), but with a relativelyhigh proportion of endemic species concentrated in a smalland highly threatened area (Leao et al., 2003; Moura, 2003;Leao and Kikuchi, 2005; Dutra et al., 2006). Although coralbleaching (i.e., loss of symbiotic zooxanthellae or presence ofpathogenic Vibrio spp. (Rosenberg et al., 2007)) was alreadydocumented in Brazil (Garzon-Frreira et al., 2002), therehave been no records of coral diseases in Brazil until now.Here we present an overview of the main types of diseases,their gross signals, and their frequency in the Abrolhos Bank,eastern Brazil, where the largest and richest coral reefs in theSouth Atlantic Ocean are concentrated (Leao et al., 2003).

2. Material and methods

The Abrolhos Bank, south State of Bahia (16�400–19�400S, 39�100–37�200W), is a wide portion of the

R.B. Francini-Filho et al. / Marine Pollution Bulletin 56 (2008) 1008–1014 1009

continental shelf (42,000 km2), with depths rarely exceed-ing 30 m. Eight of the 18 reef coral species commonlyfound in the Abrolhos Bank occur only in the South Atlan-tic, and one species (Mussismilia braziliensis) is endemic tothe eastern Brazilian coast alone (Leao and Kikuchi, 2001).Surveys for coral diseases were carried out yearly from2001 to 2007, on 28 sites distributed along the AbrolhosBank (Fig. 1). Sampling was undertaken in the summer(January–April), when northeastern winds prevail, watervisibility is greater (�5–10 m) and sea surface water tem-peratures are relatively higher (�25–28 �C) (Leao andKikuchi, 2001). The disease progression rate was estimatedfor one site (Portinho Norte, within the Abrolhos Archipel-ago) between April 14 and July 04, 2006 and disease prev-alence was determined at two sites (Pedra de Leste, withinParcel das Paredes reef, and one site within Timbebas reef)between January and March 2007 (Fig. 1).

The presence of coral diseases was determined with apivoting line search pattern methodology (cf. Borger andSteiner, 2005). Basically, diseases were determined by closeinspection of each sampling site (�200 m2) for a total dura-tion of 20 h each year. Identification of diseased corals inthe field was based on the appearance of lesions, and thevariables recorded included the color of the affected tissueand/or the pattern of tissue loss (e.g., Borger and Steiner,2005; Voss and Richardson, 2006).

Total coral cover (all species) was assessed yearly at twosites (Timbebas and Pedra de Leste) from 2003 to 2007.

Fig. 1. Map of the Abrolhos Bank, eastern Brazil, showing study sites,marine protected areas and main municipalities along the coast. Presenceof coral diseases was determined in all sites from 2001 to 2007. (A)Itacolomis reef, (B) Timbebas reef (C) Parcel das Paredes reef, (D)Sebastiao Gomes reef, (E) Abrolhos Archipelago (five sites), and (F)Parcel dos Abrolhos reef (five sites). 1 (Timbebas) and 2 (Pedra de Leste) –sites where white plague (WP)-like disease prevalence was determined. 3(Portinho Norte) – site where WP disease progression rate wasdetermined.

From 2003 to 2005, coral cover was assessed using point-intercept lines (10 m length; 100 points). Four lines werehaphazardly laid per site per year. From 2006 to 2007,coral cover was assessed using benthic photo-quadrats(n = 10 per site per year). Each sample was constitutedby a mosaic of 15 high-resolution digital images totaling0.7 m2. Quadrats were permanently delimited by fixedmetal pins and set at random distances along 20–50 m axison the reef pinnacles’ tops. Relative coral cover was esti-mated through the identification of organisms below 200randomly distributed points per quadrat (i.e., 20 pointsper photograph) using the Coral Point Count with ExcelExtensions software (Kohler and Gill, 2006).

White plague (WP) disease prevalence on M. braziliensiswas investigated by using belt transects (10 m � 1 m). Fourreplicate transects were laid randomly in each site. All col-onies of M. braziliensis within each transect were counted,measured to their mean diameter (as calculated by averag-ing the smaller and larger diameters) and recorded ashealthy or diseased. Comparisons of M. braziliensis coverand disease prevalence between the two sites, as well as totalcoral cover between the two sampling periods (before andafter disease outbreak), were undertaken using a studentt-test for independent samples. Colony size distributionsof healthy and diseased coral populations were comparedusing a Kolmogorov–Smirnov two-sample test (Zar, 1999).

White plague disease progression rate on M. braziliensis

was evaluated by monitoring ten individually tagged colo-nies. Boundaries between healthy and diseased coral tissuewere delimited using metal nails and disease progressionwas measured by comparing photographs taken in thesame position over time. Information on prevalence andprogression rate was obtained for WP disease only, sinceit was the most common type of disease recorded duringthis study (see below).

A simple model for estimating the loss of M. braziliensis

cover over time due to WP disease was built based on aradial growth rate of 8 mm per year (M.D.M. Oliveira,unpublished data) and our estimates of WP disease preva-lence and progression rate. Since most coral diseases(including WP) are seasonal and less active during periodsof colder sea water temperatures (Selig et al., 2006; authorsunpublished data), coral cover decline over time was con-servatively predicted under the assumption that WP isactive 100 days per year. Calculations were made consider-ing values of prevalence affecting different coral colony sizecategories. Four different scenarios were built, one assum-ing that WP disease prevalence and progression rate arestable over time (and similar to present day values), andthree other scenarios considering a 1%, 5% and 10%increase in both prevalence and progression rate each sub-sequent decade.

3. Results

Six types of coral diseases were recorded in the Abrol-hos Bank (Fig. 2; Table 1). They generally resemble

Fig. 2. Diseases affecting Brazilian corals and octocorals: (A) black-band like disease on Mussismilia braziliensis; (B) red-band like disease on Siderastrea

spp.; (C) dark spot like disease on Siderastrea spp.; (D) white plague-like disease on M. braziliensis; (E) tissue necrosis/mortality on Phyllogorgia dilatata;(F) tissue necrosis/mortality on Plexaurella grandiflora. All photographs by R.B. Francini-Filho except D (C.L.B. Francini).

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diseases already described for the Caribbean and Indo-Pacific regions, including WP, black-band (BB), red-band(RB), dark spot (DS), aspergillosis (ASP) and octocoraltissue necrosis (TN) (Alker et al., 2004; Sutherland et al.,2004).

Although we have been conducting underwater surveyson the Abrolhos Bank since the 1980s and searchingregularly for signs of disease since 2001, the first coral dis-ease was not detected until January of 2005. This initialrecord was comprised of only a few affected colonies of Sid-

erastrea spp. and M. braziliensis. The number of sitesshowing diseased corals increased sharply in the subse-quent years (Fig. 3), with records of hundreds of affectedcolonies across the region. In addition, diseases wereobserved in a widening range of species beginning in 2005(Table 1).

The coral cover of M. braziliensis was significantlyhigher at Timbebas than at Pedra de Leste (t = 2.98,P = 0.024). There was no significant difference in WP dis-ease prevalence between the two sites (t = 0.68, P = 0.51;Fig. 4). Although total coral cover tended to decrease afterthe disease outbreak, there was no difference between thetwo sampling periods (before and after the disease out-break) for both sites (Timbebas: t = 0.609, P = 0.546;Pedra de Leste: t = 0.840, P = 0.407; Fig. 5). Size distribu-tions of healthy coral populations revealed that colonies ofM. braziliensis were larger at Timbebas than at Pedra deLeste (Kolmogorov–Smirnov test: P < 0.001). Disease pre-dominantly affected colonies in the 10–15 cm size class atPedra de Leste (P < 0.001), while no differences in sizebetween healthy and diseased colonies were detected atTimbebas (P = 0.181) (Fig. 6). Linear progression rate of

Table 1Brazilian scleractinian corals and octocorals affected by diseases

Species affected Disease type

BB RB DS WP ASP TN

ScleractiniansFavia gravidaa XFavia leptophyllab XMussismilia braziliensisb X XMussismilia harttia XMussismilia hispidaa X XPorites astreoides XSiderastrea spp. X X X

OctocoralsPhyllogorgia dilatataa XPlexaurella grandiflora a XPlexaurella regia b X

(BB) black-band, (RB) red-band, (DS) dark spot, (WP) white plague,(ASP) aspergillosis and (TN) tissue necrosis.

a Endemic to Brazil.b Endemic to Eastern Brazil.

Fig. 3. Number of sites showing diseased corals from 2001 to 2007.

Fig. 4. Cover (mean ± SE) of M. braziliensis and white plague diseaseprevalence.

Fig. 5. Total coral cover (mean ± SE) before (2003–2004) and after(2005–2007) the disease outbreak.

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WP disease on M. braziliensis was estimated at 0.18 ± 0.06(SE) mm day�1, while area progression rate was estimatedat 0.21 ± 0.07 (SE) cm2 day�1.

The model estimating the loss of M. braziliensis coverover time showed that if the current rate of mortality dueto WP disease is maintained, about 40% of M. braziliensiscover will be lost in the next 50 years, and more than 60%will by lost by the year 2100. If a 1% increase on WP dis-ease prevalence and progression rate occurs each subse-quent decade, about 60% of M. braziliensis cover will belost in the next 50 years, and almost 90% by the year2100. If a 5% and 10% increase in disease severity occurseach successive decade, a 15% and 20% cover decline willoccur in the next 10 years, respectively, and M. braziliensiswill be nearly extinct (remaining cover < 1%) by the years2077 and 2057, respectively (Fig. 7).

4. Discussion

The main postulated stress linked to the recent prolifer-ation of coral diseases on a global scale is elevated seawatertemperature, while major local drivers include pollutionand eutrophication of coastal waters, sedimentation andintroduction of terrestrial microbes in the marine environ-ment (Harvell et al., 1999, 2002; Selig et al., 2006). Resultsfrom the present study indicate that coral diseases blos-somed into significance only recently in Brazil, perhapsdue to the synergistic effect of multiple stressors.

Elevated seawater temperature is associated with the eti-ologies of at least nine coral diseases (Harvell et al., 1999,2002; Selig et al., 2006). In addition, global warming hasbeen predicted to expand the geographic distribution ofmarine diseases, either by increasing the virulence ofalready existing pathogens or by creating appropriate con-ditions for the invasion of new ones (Harvell et al., 2002;Selig et al., 2006). Warm sea surface temperature (SST)anomalies have been recorded in Brazil, particularly duringthe strongest El Nino-southern oscillation (ENSO) eventsof 1987, 1992, 1998 and 2003 (Soppa et al., 2007). Accord-ingly, coral bleaching events have been documented duringyears with warm SST anomalies, but most of the bleachedcorals recovered a few months latter (Garzon-Frreira et al.,2002). Future research and continued monitoring may elu-

Fig. 6. Size distributions of healthy and diseases colonies of M. braziliensis.

Fig. 7. Predicted loss of M. braziliensis cover over time due to whiteplague disease.

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cidate the relative contribution of SST anomalies to theproliferation of coral diseases in the South Atlantic (e.g.,Selig et al., 2006).

Sedimentation, pollution and nutrient enrichment areassociated with elevated severity of coral diseases (Brunoet al., 2003; Frias-Lopez et al., 2002; Patterson et al.,2002). For example, both BB and WP diseases may beassociated with fecal contamination of human origin(Frias-Lopez et al., 2002; Patterson et al., 2002). In addi-tion, the causative agent of the fungal infection on theCaribbean sea fans Gorgonia ventalina and Gorgonia flabel-lum is a terrestrial fungus (Aspergillus sydowii), possiblydelivered to the marine environment by local sediment run-

off and/or long distance transport (Smith et al., 1996; Shinnet al., 2000). In the last 20 years, the coast of the State ofBahia has experienced an acceleration of urbanizationand large-scale agriculture, with the indiscriminate dis-charge of untreated wastes leading to the contaminationof coastal reefs (e.g., Costa et al., 2000). Recent findingsshow that sulfide producing bacteria, pathogenic Vibrio

spp., and human enteric bacteria are common on coralreefs of the Abrolhos Bank (F.L. Thompson, unpublisheddata). These types of microbes are among the main coralpathogens (Rosenberg et al., 2007). Finally, the Abrolhosregion is subjected to a high influx of terrigenous sedi-ments, with up to 70% of siliciclastic constituents, partiallyas a consequence of increased coastal erosion caused by thedestruction of the Atlantic rain forest (Leao et al., 1997).

The distinction between different types of WP-like dis-eases is generally based upon rates of disease progressionand species affected. Progression rates of WP disease TypesI and II vary from 1.3–3.1 mm day�1 to 14–20 mm day�1,respectively (Dustan, 1977; Richardson et al., 1998a,b;Nugues, 2002). White plague disease Type III affects onlylarge colonies (3–4 m diameter) of Colpophyllia natansand Montastrea annularis, with rates of tissue mortalityfar exceeding that of WP diseases Types I and II (Richard-son et al., 2001). The progression rate observed in thisstudy (i.e., 0.18 mm day�1 ± 0.06) is compatible with WPdisease Type I.

White plague-like disease prevalence values for M. bra-

ziliensis in Brazil (8.9–12.5%) were similar to those reportedby Nugues (2002) for M. faveolata and C. natans in theCaribbean island of St. Lucia (13–19%). In contrast, theywere much greater than the values reported by Voss and

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Richardson (2006) for several species in the Bahamas (0.2–2.7%) and lower than the values reported by Bruckner andBruckner (1997) during a major WP disease outbreakaffecting Diploria labyrinthiformes in Puerto Rico (47%).

Coral susceptibility to disease may vary according tocolony size. Although larger hosts are generally more sus-ceptible to infection than smaller ones (Nugues, 2002; Bor-ger and Steiner, 2005), results from the present studyshowed that WP-like disease selectively struck medium-sized (10–15 cm size class) colonies of M. braziliensis atone site only (Pedra de Leste).

Disease prevalence on the Abrolhos Bank has escalatedfrom negligible to alarmingly high levels in recent years.Our simple model indicates that a sharp decline on M. bra-ziliensis cover may occur in the next 50 years and that thismajor reef-building endemic species may be nearly extinctin less than a century if the current rate of mortality isnot reversed. If moderate increases in disease prevalenceand progression rate are considered, the forecasted decaybecomes even more severe. Such increases are expectedgiven the worldwide intensification on warm SST anoma-lies (Hoegh-Guldberg, 1999), and the linked positive rela-tionship between SST and disease incidence (Selig et al.,2006; Bruno et al., 2007). Coral disease incidence may beadditionally intensified by the rapid deterioration ofcoastal environments in the Abrolhos region in recent years(Leao and Kikuchi, 2005; Dutra et al., 2006). The conse-quences of such coral decline to the maintenance of reefintegrity in a region with high endemism levels (Moura,2003) are not yet totally predictable, but in the specific caseof the relatively low diversity Brazilian reef ecosystem, thereduction in coral cover and diversity may be more cata-strophic than previously anticipated. It is important to notethat disease incidence may be positively correlated withcoral cover (Bruno et al., 2007) and thus the loss of coverdue to disease over time may lower after reaching a givencritical level. Thus, more sophisticated models incorporat-ing additional information, such as coral recruitment ratesand factors influencing disease incidence, as well as contin-ued monitoring, are greatly needed in order to betterunderstand and defy coral disease impacts.

Acknowledgements

We thank G.F. Dutra for valuable comments and sup-port; G. Fiuza-Lima, A. Diocleciano do Carmo, I. Cruz,P. Meirelles, C.M. Ferreira and E. Coni for field assistance;C.L.B. Francini for providing the photograph of WP dis-ease affecting Mussismilia braziliensis (Fig. 2D); M.D.M.Oliveira for providing unpublished data on M. braziliensis

growth rate; Parque Nacional Marinho de Abrolhos/IBA-MA (through M. Lourenc�o), and Reserva ExtrativistaMarinha do Corumbau/IBAMA (through R.F. Oliveiraand A.Z. Cordeiro) for logistical support and research per-mits. This is contribution number five of the Marine Man-agement Areas Science Program, Brazil Node. F.L.T.,R.L.M., R.K.P.K. and Z.M.A.N.L. acknowledge grants

from the Pro-Abrolhos Project (Brazilian Council ofDevelopment of Science and Technology – CNPq).F.L.T. benefited with grants from IFS and Z.M.A.N.L.and R.K.P.K. benefited with grants from CNPq.

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