marine pollution bulletin - lecar lab · note decline in abundance and health state of an atlantic...

Marine Pollution Bulletin xxx (2016) xxx–xxx

MPB-07423; No of Pages 6

Contents lists available at ScienceDirect

Marine Pollution Bulletin

j ourna l homepage: www.e lsev ie r .com/ locate /marpo lbu l

Note

Decline in abundance and health state of an Atlantic subtropical gorgonian population

Gabriel Erni Cassola a,⁎, Matheus S.C. Pacheco b, Moysés C. Barbosa b, Dennis M. Hansen a, Carlos E.L. Ferreira b

a Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerlandb Departamento de Biologia Marinha, Universidade Federal Fluminense, Caixa Postal 100.644, CEP 24.001-970 Niterói, Rio de Janeiro, Brazil

⁎ Corresponding author at: School of Life Sciences, UniRoad, Coventry CV4 7AL, United Kingdom.

E-mail address: [email protected] (G. Ern

http://dx.doi.org/10.1016/j.marpolbul.2016.01.0220025-326X/© 2016 Elsevier Ltd. All rights reserved.

Please cite this article as: Erni Cassola, G., et aPollution Bulletin (2016), http://dx.doi.org

a b s t r a c t
a r t i c l e i n f o
Article history:Received 4 September 2015Received in revised form 12 January 2016Accepted 16 January 2016Available online xxxx

Losses in coral cover have been widely reported for the Caribbean. In contrast, much less is known about thehealth state of the Brazilian reef fauna, which was declared as a priority for Atlantic biodiversity conservationdue to its high degree of endemism. In the present study, we assessed the general health state of Phyllogorgiadilatata assemblages at the subtropical reefs of Arraial do Cabo (southeastern Brazil), where observations suggestthat the abundance of this endemic gorgonian species has declined.We found that about 49% of the sampled col-onies were dead, and 73% of the living colonies were affected by tissue loss. Tissue loss initially manifested asmultifocal holes in the planar colonial coenenchyme and peripheral tissue retraction leaving denuded skeletalaxes. In combination with other recent studies, our results raise the awareness for an increasingly threatenedSouthwestern Atlantic reef coral fauna.

© 2016 Elsevier Ltd. All rights reserved.

Keywords:GorgoniansDiseaseSubtropicalRocky reefBrazil

1. Introduction

About 75% of the world's coral cover is threatened (Burke et al.,2011). Declines in coral abundance have been attributed to various fac-tors, including climate change, overexploitation, increased water tur-bidity and nutrient input (Hughes et al., 2003; Reopanichkul et al.,2009). Overfishing, for instance, greatly changed faunal compositionsand as a consequence, increased the abundance of algae on coral reefs(Dulvy et al., 2004; Jackson et al., 2001). Synergistic effects betweenlowered predation pressure on macroalgae and increased productiondue to higher nutrient loads, cause macroalgae to release excessive dis-solved organic carbon (DOC), which indirectly affects corals (Smithet al., 2006). Indeed, DOC has been repeatedly linked to increasedcoral mortality by inducing uncontrolled bacterial growth and trigger-ing diseases in corals (Kline et al., 2006; Kuntz et al., 2005). Massive dis-ease outbreaks can lead to rapid reductions in live coral cover, resultingin further persisting changes of the community structure and ecosystemfunction, as has been frequently documented in the Caribbean region(Garzón-Ferreira and Zea, 1992; Gladfelter, 1982; Precht et al., 2010;Schutte et al., 2010).

In the Atlantic, other major coral reef communities can be foundalong the Brazilian coast. Althoughmuch less diverse, these reefs harborhigh percentages of endemic corals (50%, 9 species) and fish (15%, 65species) and must consequently be considered as a priority for Atlanticbiodiversity conservation (Moura, 2000). Many known threats to coralselsewhere, such as increasing sea surface temperature, overfishing,

versity of Warwick, Gibbet Hill

i Cassola).

l., Decline in abundance and/10.1016/j.marpolbul.2016.0

terrestrial run-off, as well as invasion by alien species, equally affectBrazilian reefs (Bender et al., 2014; Leão and Kikuchi, 2005; Leão et al.,2010; Sampaio et al., 2012). Even though, in comparisonwith Caribbeanreefs, major southwestern Atlantic coral species evolved to toleratesome stress, such as high sedimentation rates (Castro et al., 2012;Loiola et al., 2013), a clear deterioration of reef health has been notedduring recent assessments (Francini-Filho et al., 2008; Rogers et al.,2014). Still, very little is known about how severely individual specieshave suffered from extant impacts.

The present study aimed at providing a baseline of abundance andgeneral health of the octocoral Phyllogorgia dilatata in a subtropicalrocky reef of the southwestern Brazilian coast. This species is endemicto Brazil and occurs frequently along the Brazilian coast from ParcelManoel Luiz (north) to Arraial do Cabo (south–east), including nearbyoceanic islands (Castro et al., 2010). Aggregations of P. dilatata canoften constitute the main biotic structures providing habitat heteroge-neity, particularly in subtropical reefs, where branching corals werehighly impacted by the aquarium trade and SCUBA diving (Gaspariniet al., 2005; Rogers et al., 2014). At our study site, we found the popula-tion in a depleted state of health in which the most pervasive factor af-fecting P. dilatata colonial health was tissue loss. For the latter, wefurther provide morphological descriptions.

2. Materials and methods

2.1. General health assessment

This studywas conducted on the subtropical rocky reefs of Arraial doCabo (22°58′35″S, 42°00′W), southeastern Brazilian coast. Colonies ofP. dilatata were examined via SCUBA at three sites of high abundance

health state of an Atlantic subtropical gorgonian population, Marine1.022

mailto:[email protected]

Journal logo

http://dx.doi.org/10.1016/j.marpolbul.2016.01.022

www.elsevier.com/locate/marpolbul


2 G. Erni Cassola et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

(Anequim, Prainha and Porcos; for amap of the study area see Appendix1) to determine the general state of health of its populations. P. dilatatacolonies at Anequim are found at about 11 m depth, while at Prainhaand Porcos they are situated at approximately 6 m depth. We madetwo surveys per site, recording different measures of coral health. Thefirst, conducted in April 2013, categorized every colony according topreviously defined potential proximate causes for partial colonymortal-ity (Table 1); the total sample size was 650 colonies (223 at Anequim,77 at Porcos and 350 at Prainha). The second survey, in August 2013, in-cluded 280 colonies (114 at Anequim, 48 at Porcos and 118 at Prainha)and assigned tissue loss categories to each living colony affected by tis-sue loss: area loss ≤5%, 5–25%, 25–50%, 50–75% and 75–99%. During thesecond survey we also scored the presence of juvenile colonies(height ≤ 10 cm). Per site, each survey consisted of four parallelinterrupted belt transects (each 42 m long) laid out parallel to thecoast in 2 m intervals. Sampling plots covered an area of 2 m2 andwere deployed every 6 m. Transects for the second survey were laidout independently from the first survey, at a different location withineach study site.

To measure tissue retraction rates in situ, 10 colonies of P. dilatatawith naturally occurring tissue loss syndrome were identified atAnequim between 12 and 13 July 2014. The colonies were within simi-lar depth ranges (8–11 m), had lost at least 5% of host coral tissue andbore no other visual anomalies apart from tissue loss. On each colony,two reference cable binder rings were attached to two denuded skeletalaxes at the beginning of the experiment, in 1 cmdistance to living tissue.At monthly intervals tissue loss rates were recorded to the nearest mmusing calipers. The cable binder ringsweremarked, to ensure that tissueloss was measured at the same point. Systematic descriptions of lesionsfound on colonies with tissue loss were characterized in accordancewith Work and Aeby (2006).

2.2. Statistical analysis

Interrupted belt transect datawere analyzed for differences betweensites using generalized linear models. For comparisons of density differ-ences in living colonies, a quasi-Poisson regressionwas fitted to accountfor over dispersion, using the number of colonies per plot as responseand site as explanatory variable. Differences in general health state be-tween sites were assessed by fitting a logistic regression to the com-bined data of all colonies that were observed to have some form oflesion. Differences in the different health categories were modeledwith logistic regressions. Quasi-binomial link functions were employedwhere over dispersion was present. The effect of site was tested viaanalysis of deviance using a X2-test. If site was significant, the analyses

Table 1Brief description of the categories of colony health that were assigned to Phyllogorgiadilatata colonies during the survey in April.

Category Description

Healthy colony Colony with no visible signs of stress and no colonizedholdfast (Fig. 4a)

Tissue loss Colony with denuded skeletal axes colonized by algae,macroalgae, hydrozoans, sponges and bryozoans (Fig. 4b)

Dead colony Remains of the skeletal structure still attached to thesubstrate (Fig. 4c)

Holes in colonialtissue

Holes may result as local adaptation to stronger watercurrents and not necessarily indicate disease

Colonized by Bivalvia Colonies with attached Bivalvia do not seem to sufferfrom tissue loss

Colonized byMilleporaalcicornis

Millepora alcicornis is known to actively kill gorgoniansand colonize their skeletal structures (Wahle, 1980)

Entanglement withfishing line

Colonies entangled with monofilament fishing line

Detached colony Living colony that is not attached to the substratePurpled tissue Purpling without showing signs of other damages

Please cite this article as: Erni Cassola, G., et al., Decline in abundance andPollution Bulletin (2016), http://dx.doi.org/10.1016/j.marpolbul.2016.0

were followed by post-hoc Tukey's HSD tests to discern significant dif-ferences between.

Tissue retraction rate data were tested for tissue loss over time usinga mixed-effects model to account for temporal pseudo-replication. Percolony, the log-transformed mean distances of tissue to the referencewere fitted as response and time as the explanatory variable (fixed ef-fect). All statistical analyses were performed using R: Statistical Com-puting Software version 3.0.2 (R Core Team, 2014).

3. Results

Our study revealed that about 48% of the surveyed P. dilatata colo-nies at Arraial do Cabo were dead, and that 80% of the remaining colo-nies suffered from some form of injury. Mean colony density at Porcoswas 0.85 colonies m−2, which was about three times lower than atAnequim (Fig. 1a, 2.7 colonies m−2, t = −3.405, p b 0.01) and fourtimes lower than at Prainha (Fig. 1a, 3.38 colonies m−2, t = 1.374,p b 0.001). Juvenile colonies were only encountered twice. The percent-ages of dead colonies were similar between Porcos (50%) and Prainha(52%), while Anequim (41%) only differed significantly from Prainha(Fig. 1b, z = 2.9, p b 0.01). Tissue loss accounted for 75% of the diseasedcolonies (Fig. 2) and affected all sites similarly (X2= 4.038, df= 2, p=0.269). Colonies affected singly by tissue purplingwere rare at Anequim(3%), about four timesmore frequent at Porcos (11%, z= 2.14, p b 0.03)and absent from Prainha. Roughly 4% of the assessed colonies only pre-sented holes in their colonial tissue and the incidence was similaramong sites (X2 = 3.036, df = 2, p = 0.219). However, it is importantto state, that the real prevalence of tissue purpling aswell as holes in co-lonial tissue were considerably higher than these results suggest, be-cause both categories mostly co-occurred with tissue loss. Hence,according to our sampling protocol, colonies affected by tissue purplingand partial mortality were only scored once in the category ‘tissue loss’.Entanglement with monofilament fishing was lowest at Anequim (6%),twice as high at Porcos (13%, t = 1.566, p = 0.123) and highest atPrainha (37%) differing from Anequim (t = 4.218, p b 0.01) and fromPorcos (z = 2.304, p = 0.05).

Colonization by Bivalvia was rarely found (3%) and equally scarce atall sites (X2= 2.602, df= 2, p= 0.272). Similarly limitedwas the prev-alence of detached colonies (2%), which was evenly distributed amongsites (X2 = 3.387, df = 2, p = 0.183).

In situ measurements of colonial tissue retraction over time indicat-ed ongoing tissue loss (Figs. 3 and 5d–g, t = 8.6, df = 11, p b 0.001).After 161 days, tissue loss on colonial axes ranged between 2 and35 mm with a mean of 10.9 mm (SD ± 13.7), resulting in a tissue lossrate of about 0.07 mm d−1. Scoring of tissue loss classes revealed thatroughly half of the colonies at each site presented tissue losses of atleast 5% of their colonial area (Fig. 4). Affected colonies exhibitedsmall to large numbers of areas with tissue loss (Fig. 5b and d–f).These areas were sometimes focal, but more commonly multifocal tocoalescing, and observed centrally and at colony peripheries (Fig. 5b).Central holes were circular when small, and oblong with increasingsize, predominantly situated between skeletal axes. Peripheral areas oftissue loss presented serpiginous margins of tissue and denuded skele-tal axes. Except purpling, tissue bordering the affected areas did nothave any particular coloration.

4. Discussion

Our survey showed that about half of the sampled P. dilatata coloniesof Arraial do Cabo were dead, while colonial tissue loss accounted forthe most widespread impact, affecting 75% of the living colonies. Thispattern persisted across all study sites, suggesting a recent regional de-cline in abundance. Long-term population dynamic data are lacking, butif high mortality rates naturally occurred in this species, we would ex-pect to findhigher densities of juvenile colonies than the two specimensdetected in this study. In Espírito Santo (southeastern Brazil) Krohling



Fig. 1.Density and proportion of dead Phyllogorgia dilatata colonies at each site. (a) colonies m−2, mean± SE, nAnequim= 131, nPorcos= 41, nPrainha= 162. (b) mean± SE, nAnequim= 92,nPorcos = 36, nPrainha = 188.

3G. Erni Cassola et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

et al. (2010) also found extremely low frequencies of small colonies.Further, tropical and temperate gorgonian taxa appear to have a narrowrange of growth rates averaging 3 cm colony−1 year−1 (Coma et al.,1998). Thus, one can infer that P. dilatata possesses a similar life historyto other gorgonian species, which are long-lived and suffer little adultcolony mortality (Roark et al., 2006; Yoshioka and Yoshioka, 1991).For instance, in healthy Paramuricea clavata populations, less than 2%of the colonies were dead, and fewer than 10% were affected by partialmortality (Coma et al., 2006). Diseased gorgonian populations reflectedour findings, such as Eunicella singularis (59% partially dead and 46%dead, Coma et al., 2006) and Gorgonia ventalina (50% partially dead,Nagelkerken et al., 1997). We therefore conclude that the abundanceof P. dilatata at Arraial do Cabo has clearly declined.

The natural history of disease in gorgonians in other regions sharessimilarities, but also some differences to what we observed in Arraialdo Cabo. Reported massive die-offs manifested themselves through tis-sue loss and have been attributed to a fungus (Aspergillus sydowii) in theCaribbean and a bacterium (Vibrio coralliilyticus) in the Mediterranean(Bally and Garrabou, 2007; Smith et al., 1996). Vibrio bacteria havebeen identified as the causative agents of diseases in numerous coralspecies and were found on P. dilatata (Alves et al., 2009; Ben-Haimand Rosenberg, 2002; Cervino et al., 2004). However, Alves et al.(2009) detected no differences in Vibriomicrobiota between apparentlyhealthy and diseased P. dilatata colonies, a possible pathogen remainingelusive. Also, the rate of colonial tissue loss recorded in our study(0.07 mm d−1) appears very low in comparison with rates found forother widely reported bacterial diseases, such as white plague type I(0.18 mm d−1, Francini-Filho et al., 2008) or black band disease(0.6 mm d−1, Voss and Richardson, 2006). At Arraial do Cabo, Coelho-Souza et al. (2013) showed that bacterial production was highly vari-able in the embayments and strongly influenced by occasional sewagedischarges. They further noticed that high water circulation reduced

Fig. 2. Percent of living Phyllogorgia dilatata colonies affected by different syndromes ateach site (mean ± SE). TL = tissue loss; CB = colonized by Bivalvia; L = entanglementwith monofilament fishing line; D = detached colonies; H = holes in colony area; P =purpled tissue.


punctual discharge impacts but dispersed pollutants to adjacent areas.Our results could therefore reflect a stationary phase in tissue loss pro-gression as environmental factors, such aswater temperature and nutri-ent enrichment, which are tightly linked to disease severity in corals,may have been absent during our assessment (Bruno et al., 2003,2007; Kuta and Richardson, 2002). Alternatively, the low tissue lossrates could indicate that the severity peak has passed and the remainingcolonies are more tolerant of the syndrome.

In contrast to the Mediterranean, P. dilatata colonies with purpledcolonial tissue reflect Caribbean gorgonians infected with A. sydowii,which typically displayed purpling around infected areas (Smith et al.,1998). Based on visual comparison, Francini-Filho et al. (2008) sug-gested that aspergillosis could equally account for the decline ofP. dilatata in Brazil. However, research has shown, that tissue purplingin sea fans, i.e., melanization, represents an unspecific immune reactionto several different stressors, such as fungi, abrasion or contact withmacroalgae (Alker et al., 2004; Reed et al., 2010). It is therefore difficult,withoutmolecularmethods, to suggest a causative agent responsible forthe observed tissue loss in P. dilatata at Arraial do Cabo.

The high incidence of tissue loss encountered at Arraial do Cabo to-gether with reports from Abrolhos (Northeastern Brazil, Francini-Filhoet al., 2008) and Fernando de Noronha (tropical oceanic island, pers.comm. Zaira Matheus), suggest that this syndrome might constituteoneof themain threats to P. dilatata populations along a large geograph-ic scale. Although devastated areasmay recover fasterwith larval supplyfrom unaffected reefs, self-seeding appears to be more effective for the

Fig. 3. Tissue loss on axes of Phyllogorgia dilatata colonies over a period of 161 days(mean ± SD, n = 10).



Fig. 4. Percent of colonies with different extent of tissue loss by site, stacked by increasingextent of tissue loss (mean− SE). nAnequim = 114, nPorcos = 48, nPrainha = 118.


maintenance of reef communities (Ayre and Hughes, 2000; Nishikawaet al., 2003;West and Salm, 2003). As a comprehensive study on the im-pacts of aspergillosis on G. ventalina demography revealed, the restora-tion of lost tissue in established colonies was crucial for populationrecovery, as only colonies above a certain size threshold were sexually

Fig. 5. Phyllogorgia dilatata at different health states. (a) Healthy: note intact laminae. (b) DiseasTissue purpling and formation of holes on different colonies. Arrowheads indicate exposed, uncomonofilament fishing line.


active (Bruno et al., 2011). Future studies should therefore focus on elu-cidating possible causal mechanisms that drive the observed tissue lossdisease in P. dilatata in order to exploremitigationmeasures that ensurethe survival of large established colonies.

Gorgonians are frequently found entangledwithmonofilament fish-ing line, which could impair survival rates of established colonies(Bavestrello et al., 1997; Chiappone et al., 2005). Entanglement ofPocillopora meandrina colonies with fishing line was also associatedwith higher rates of partially and completely dead colonies(Yoshikawa and Asoh, 2004). Although we found high percentages ofentangled P. dilatata colonies (37% Prainha and 13% Porcos), no correla-tion with a generally lowered health state at those sites was obvious,when compared to Anequim (6%). Experimental entanglement ofhealthy P. dilatata colonies with monofilament fishing line duringseven months also failed to induce significant abrasion lesions and tis-sue necrosis (the authors, unpublished data). Our results further indi-cate that colony detachment was not more frequent at sites withhigher hook and line fishing intensity (using incidence of colony entan-glement as proxy).

As indicated for tropical reefs of the Brazilian coast (Francini-Filhoet al., 2008) and in combination with a study from the subtropicalreefs of Arraial do Cabo (Rogers et al., 2014), our survey demonstratesthat impacts from diseases have now as well increased in the south-western Atlantic reef communities and have become capable of shapingfuture reef community compositions. For instance, changes of the ben-thic fauna may have repercussions for reef fish species, as habitat het-erogeneity is commonly associated with fish biodiversity (Ferreiraet al., 2001; Gratwicke and Speight, 2005). Brazilian reefs are devoidof branching scleractinian corals, such as Acropora spp., which are ofcritical importance to Caribbean and Indo-Pacific reefs (Bellwoodet al., 2004). In turn Brazilian reefs depend on two species of branching

ed: note holes and colonized skeletal axes (arrow). (c) Dead: note colonized skeleton. (d–f)lonized skeletal axes. (g–j) Disease progressionwithin 30weeks on the same colony; note



5G. Erni Cassola et al. / Marine Pollution Bulletin xxx (2016) xxx–xxx

fire corals, which fulfill similar ecological roles, providing shelter for adiverse range of small-bodied and juvenile fish (Coni et al., 2013). How-ever, SCUBA diving and the aquarium trade industry have heavily dam-aged Millepora alcicornis colonies and reduced their abundance atArraial do Cabo, leaving P. dilatata as an important species still providinghabitat heterogeneity (Gasparini et al., 2005; Rogers et al., 2014). P.dilatatamay therefore be important for the maintenance of fish speciesthat are generalists in terms of microhabitat use (Coni et al., 2013).

Acknowledgements

Special thanks go to Cesar A. M. M. Cordeiro for his assistance in thefield and comments on the manuscript. Funding was provided by theUniversity of Zurich and FAPERJ (grant #111.711/2012). Carlos E. L.Ferreira is further supported by a CNPQ productivity research grant.The authors would also like to thank ECOHUB for providing continuousfinancial support to the LECAR lab. Research permit (#38879) wasgranted by ICMBio.

Appendix 1

Map of the Arraial do Cabo region (Rio de Janeiro, Brazil) indicatingsampled sites. Sampling depth is given in parentheses after the sitename: 1—Prainha (6m), 2—Porcos (6m), 3—Anequim (11m). (Courte-sy by Cesar Cordeiro).

References

Alker, A.P., Kim, K., Dube, D.H., Harvell, C.D., 2004. Localized induction of a generalized re-sponse against multiple biotic agents in Caribbean sea fans. Coral Reefs 23, 397–405.

Alves Jr., N., Neto, O.S.M., Silva, B.S.O., DeMoura, R.L., Francini-Filho, R.B., Barreira e Castro,C., Paranhos, R., Bitner-Mathé, B.C., Kruger, R.H., Vicente, A.C.P., Thompson, C.C.,Thompson, F.L., 2009. Diversity and pathogenic potential of vibrios isolated fromAbrolhos Bank corals. Environ. Microbiol. Rep. 2, 90–95.

Ayre, D.J., Hughes, T.P., 2000. Genotypic diversity and gene flow in brooding andspawning corals along the Great Barrier Reef, Australia. Evolution (N. Y) 54,1590–1605.

Bally, M., Garrabou, J., 2007. Thermodependent bacterial pathogens and mass mortalitiesin temperate benthic communities: a new case of emerging disease linked to climatechange. Glob. Chang. Biol. 13, 2078–2088.

Bavestrello, G., Cerrano, C., Zanzi, D., Cattaneo-Vietti, R., 1997. Damage by fishing activitiesto the Gorgonian coral Paramuricea clavata in the Ligurian Sea. Aquat. Conserv. Mar.Freshwat. Ecosyst. 7, 253–262.

Bellwood, D.R., Hughes, T.P., Folke, C., Nyström, M., 2004. Confronting the coral reef crisis.Nature 429, 827–833.

Bender, M.G., Machado, G.R., de Silva, P.J.A., Floeter, S.R., Monteiro-Netto, C., Luiz, O.J.,Ferreira, C.E.L., 2014. Local ecological knowledge and scientific data reveal overex-ploitation by multigear artisanal fisheries in the southwestern Atlantic. PLoS One 9,e110332.

Ben-Haim, Y., Rosenberg, E., 2002. A novel Vibrio sp. pathogen of the coral Pocilloporadamicornis. Mar. Biol. 141, 47–55.

Bruno, J.F., Petes, L.E., Drew Harvell, C., Hettinger, A., 2003. Nutrient enrichment can in-crease the severity of coral diseases. Ecol. Lett. 6, 1056–1061.

Bruno, J.F., Selig, E.R., Casey, K.S., Page, C.A., Willis, B.L., Harvell, C.D., Sweatman, H.,Melendy, A.M., 2007. Thermal stress and coral cover as drivers of coral disease out-breaks. PLoS Biol. 5, e124.

Bruno, J.F., Ellner, S.P., Vu, I., Kim, K., Harvell, C.D., 2011. Impacts of aspergillosis on sea fancoral demography: modeling a moving target. Ecol. Monogr. 81, 123–139.

Burke, L., Reytar, K., Spalding, M., Perry, A., 2011. Reefs at Risk Revisited. World ResourcesInstitute, Washington DC.

Castro, C.B., Medeiros, M.S., Loiola, L.L., 2010. Octocorallia (Cnidaria: Anthozoa) fromBrazilian reefs. J. Nat. Hist. 44, 763–827.

Castro, C.B., Segal, B., Negrão, F., Calderon, E.N., 2012. Four-year monthly sediment depo-sition on turbid southwestern Atlantic coral reefs, with a comparison of benthic as-semblages. Braz. J. Oceanogr. 60, 49–63.

Cervino, J.M., Hayes, R.L., Polson, S.W., Polson, S.C., Goreau, T.J., Martinez, R.J., Smith, G.W.,2004. Relationship of Vibrio species infection and elevated temperatures to yellowblotch/band disease in Caribbean corals. Appl. Environ. Microbiol. 70, 6855–6864.

Chiappone, M., Dienes, H., Swanson, D.W., Miller, S.L., 2005. Impacts of lost fishing gear oncoral reef sessile invertebrates in the Florida Keys National Marine Sanctuary. Biol.Conserv. 121, 221–230.

Coelho-Souza, S.A., Pereira, G.C., Coutinho, R., Guimarães, J.R.D., 2013. Yearly variation ofbacterial production in the Arraial do Cabo protection area (Cabo Frio upwelling re-gion): an evidence of anthropogenic pressure. Braz. J. Microbiol. 44, 1349–1357.

Coma, R., Ribes, M., Zabala, M., Gili, J., 1998. Growth in a modular colonial marine inver-tebrate. Estuar. Coast. Shelf Sci. 47, 459–470.


Coma, R., Linares, C., Ribes, M., Diaz, D., Garrabou, J., Ballesteros, E., 2006. Consequences ofa mass mortality in populations of Eunicella singularis (Cnidaria: Octocorallia) in Me-norca (NW Mediterranean). Mar. Ecol. Prog. Ser. 327, 51–60.

Coni, E.O.C., Ferreira, C.M., de Moura, R.L., Meirelles, P.M., Kaufman, L., Francini-Filho, R.B.,2013. An evaluation of the use of branching fire-corals (Millepora spp.) as refuge byreef fish in the Abrolhos Bank, eastern Brazil. Environ. Biol. Fish 96, 45–55.

Dulvy, N.K., Freckleton, R.P., Polunin, N.V.C., 2004. Coral reef cascades and the indirect ef-fects of predator removal by exploitation. Ecol. Lett. 7, 410–416.

Ferreira, C.E.L., Gonçalves, J.E.A., Coutinho, R., 2001. Community structure of fishes andhabitat complexity on a tropical rocky shore. Environ. Biol. Fish 61, 353–369.

Francini-Filho, R.B., Moura, R.L., Thompson, F.L., Reis, R.M., Kaufman, L., Kikuchi, R.K.P.,Leão, Z.M.A.N., 2008. Diseases leading to accelerated decline of reef corals in the larg-est South Atlantic reef complex (Abrolhos Bank, eastern Brazil). Mar. Pollut. Bull. 56,1008–1014.

Garzón-Ferreira, J., Zea, S., 1992. A mass mortality of Gorgonia ventalina (Cnidaria:Gorgoniidae) in the Santa Marta area, Caribbean coast of Colombia. Bull. Mar. Sci.50, 522–526.

Gasparini, J.L., Floeter, S.R., Ferreira, C.E.L., Sazima, I., 2005. Marine ornamental trade inBrazil. Biodivers. Conserv. 14, 2883–2899.

Gladfelter, W., 1982. White-band disease in Acropora palmata: implications for the struc-ture and growth of shallow reefs. Bull. Mar. Sci. 32, 639–643.

Gratwicke, B., Speight, M.R., 2005. The relationship between fish species richness, abun-dance and habitat complexity in a range of shallow tropical marine habitats. J. FishBiol. 66, 650–667.

Hughes, T.P., Baird, A.H., Bellwood, D.R., Card, M., Connolly, S.R., Folke, C., Grosberg, R.,Hoegh-Guldberg, O., Jackson, J.B.C., Kleypas, J., Lough, J.M., Marshall, P., Nyström, M.,Palumbi, S.R., Pandolfi, J.M., Rosen, B., Roughgarden, J., 2003. Climate change,human impacts, and the resilience of coral reefs. Science 301, 929–933.

Jackson, J.B., Kirby, M.X., Berger, W.H., Bjorndal, K.A., Botsford, L.W., Bourque, B.J.,Bradbury, R.H., Cooke, R., Erlandson, J., Estes, J.A., Hughes, T.P., Kidwell, S., Lange,C.B., Lenihan, H.S., Pandolfi, J.M., Peterson, C.H., Steneck, R.S., Tegner, M.J., Warner,R.R., 2001. Historical overfishing and the recent collapse of coastal ecosystems. Sci-ence 293, 629–637.

Kline, D.I., Kuntz, N.M., Breitbart, M., Knowlton, N., Rohwer, F., 2006. Role of elevated or-ganic carbon levels and microbial activity in coral mortality. Mar. Ecol. Prog. Ser. 314,119–125.

Krohling, W., Freitas Netto, R., Mercier, A.L.F., 2010. Estudo populacional das colônias dePhyllogorgia dilatata (Esper, 1806) em dois ambientes costeiros no Estado do EspíritoSanto. Nat. Line 8, 123–126.

Kuntz, N.M., Kline, D.I., Sandin, S.A., Rohwer, F., 2005. Pathologies and mortality ratescaused by organic carbon and nutrient stressors in three Caribbean coral species.Mar. Ecol. Prog. Ser. 294, 173–180.

Kuta, K., Richardson, L., 2002. Ecological aspects of black band disease of corals:relationships between disease incidence and environmental factors. Coral Reefs 21,393–398.

Leão, Z.M.A.N., Kikuchi, R.K.P., 2005. A relic coral fauna threatened by global changes andhuman activities, Eastern Brazil. Mar. Pollut. Bull. 51, 599–611.

Leão, Z.M.A.N., Kikuchi, R.K.P., Oliveira, M.D.M., Vasconcellos, V., 2010. Status of EasternBrazilian coral reefs in time of climate changes. Panam. J. Aquat. Sci. 5, 224–235.

Loiola, M., Oliveira, M.D.M., Kikuchi, R.K.P., 2013. Tolerance of Brazilian brain coralMussismilia braziliensis to sediment and organic matter inputs. Mar. Pollut. Bull. 77,55–62.

Moura, R.L., 2000. Brazilian reefs as priority areas for biodiversity conservation in the At-lantic Ocean. Proc. 9th Int. Coral Reef Symp. Bali, Indones. 23–27 Oct. 2.

Nagelkerken, I., Buchan, K., Smith, G.W., Bonair, K., Bush, P., Garzón-Ferreira, J., Botero, L.,Gayle, P., Harvell, C.D., Heberer, C., Kim, K., Petrovic, C., Pors, L., Yoshioka, P., 1997.Widespread disease in Caribbean sea fans: II. Patterns of infection and tissue loss.Mar. Ecol. Prog. Ser. 160, 255–263.

Nishikawa, A., Katoh, M., Sakai, K., 2003. Larval settlement rates and gene flow ofbroadcast-spawning (Acropora tenuis) and planula-brooding (Stylophora pistillata)corals. Mar. Ecol. Prog. Ser. 256, 87–97.

Precht, W.F., Aronson, R.B., Moody, R.M., Kaufman, L., 2010. Changing patterns of micro-habitat utilization by the threespot damselfish, Stegastes planifrons, on Caribbeanreefs. PLoS One 5, e10835.

R Core Team, 2014. R: A language and environment for statistical computing. R Founda-tion for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.

Reed, K., Muller, E., vanWoesik, R., 2010. Coral immunology and resistance to disease. Dis.Aquat. Org. 90, 85–92.

Reopanichkul, P., Schlacher, T.A., Carter, R.W., Worachananant, S., 2009. Sewage impactscoral reefs at multiple levels of ecological organization. Mar. Pollut. Bull. 58,1356–1362.

Roark, E.B., Guilderson, T.P., Dunbar, R.B., Ingram, B.L., 2006. Radiocarbon-based ages andgrowth rates of Hawaiian deep-sea corals. Mar. Ecol. Prog. Ser. 327, 1–14.

Rogers, R., de Oliveira Correal, G., de Oliveira, T.C., de Carvalho, L.L., Mazurek, P., Barbosa,J.E.F., Chequer, L., Domingos, T.F.S., de Andrade Jandre, K., Leão, L.S.D., de AndradeMoura, L., Occhioni, G.E., de Oliveira, V.M., Silva, E.S., Cardoso, A.M., de Castro eCosta, A., Ferreira, C.E.L., 2014. Coral health rapid assessment in marginal reef sites.Mar. Biol. Res. 10, 612–624.

Sampaio, C.L.S., Miranda, R.J., Maia-Nogueira, R., José de Anchieta, C.C.N., 2012. New oc-currences of the nonindigenous orange cup corals Tubastraea coccinea andT. tagusensis (Scleractinia: Dendrophylliidae) in southwestern Atlantic. Check List 8,528–530.

Schutte, V., Selig, E., Bruno, J., 2010. Regional spatio-temporal trends in Caribbean coralreef benthic communities. Mar. Ecol. Prog. Ser. 402, 115–122.

Smith, G.W., Ives, L.D., Nagelkerken, I.A., Ritchie, K.B., 1996. Caribbean sea-fan mortalities.Nature 383, 487.


http://refhub.elsevier.com/S0025-326X(16)30026-1/rf0005


































































































https://www.R-roject.org/




















Smith, G.W., Harvel, C.D., Kim, K., 1998. Response of sea fans to infection with Aspergillussp. (fungi). Rev. Biol. Trop. 46, 205–208.

Smith, J.E., Shaw, M., Edwards, R.A., Obura, D., Pantos, O., Sala, E., Sandin, S.A., Smriga, S.,Hatay, M., Rohwer, F.L., 2006. Indirect effects of algae on coral: algae-mediated,microbe-induced coral mortality. Ecol. Lett. 9, 835–845.

Voss, J.D., Richardson, L.L., 2006. Nutrient enrichment enhances black band disease pro-gression in corals. Coral Reefs 25, 569–576.

Wahle, C.M., 1980. Detection, pursuit, and overgrowth of tropical gorgonians bymilleporid hydrocorals: Perseus and Medusa revisited. Science 209, 689–691.


West, J.M., Salm, R.V., 2003. Resistance and resilience to coral bleaching: implications forcoral reef conservation and management. Conserv. Biol. 17, 956–967.

Work, T.M., Aeby, G.S., 2006. Systematically describing gross lesions in corals. Dis. Aquat.Org. 70, 155–160.

Yoshikawa, T., Asoh, K., 2004. Entanglement of monofilament fishing lines and coraldeath. Biol. Conserv. 117, 557–560.

Yoshioka, P.M., Yoshioka, B.B., 1991. A comparison of the survivorship and growth ofshallow-water gorgonian species of Puerto Rico. Mar. Ecol. Prog. Ser. 69, 253–260.



















marine pollution bulletin - lecar lab · note decline in abundance and health state of an atlantic...

Documents