Environmental licensing on rhodolith beds: insights from a worm

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Natureza

&

Conservação

Brazilian

Journal

of

Nature

Conservation

SupportedbyBoticárioGroupFoundationforNatureProtection

Policy

Forums

Environmental

licensing

on

rhodolith

beds:

insights

from

a

worm

Cinthya

Simone

Gomes

Santos

_,

_Jaqueline

_Barreto

_Lino

_,

_Priscila

_de

_Cerqueira

_Veras

_,

Gilberto

Menezes

Amado-Filho

_,

_Ronaldo

_Bastos

_{Francini-Filho}

_,

_Fabio

_Santos

_Motta

_,

Rodrigo

Leão

de

Moura

_,

_Guilherme

_Henrique

_{Pereira-Filho}

a_{DepartmentofMarineBiology,InstituteofBiology,UniversidadeFederalFluminense,Niterói,RJ,Brazil}

b_{InstitutodoMar,LaboratoryofMarineEcologyandConservation,UniversidadeFederaldeSãoPaulo,Santos,SP,Brazil} c_{CenterforNaturalandHumanSciences,UniversidadeFederaldoABC,SãoBernardodoCampo,SP,Brazil}

d_{InstitutodePesquisasJardimBotânicodoRiodeJaneiro,RiodeJaneiro,RJ,Brazil}

e_{DepartmentofEngineeringandEnvironment,UniversidadeFederaldaParaíba,RioTinto,PB,Brazil}

f_{InstituteofBiology,LaboratóriodeSistemasAvanc¸adosdeGestãodaProduc¸ão(SAGE),InstitutoAlbertoLuizCoimbrade}

Pós-Graduac¸ãoePesquisadeEngenharia(COPPE),UniversidadeFederaldoRiodeJaneiro,RiodeJaneiro,RJ,Brazil

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Articlehistory:

Received12January2016

Accepted7June2016

Availableonline1July2016

Keywords:

Marinediversity

Maerl

Mesophoticreefs

Crustosecorallinealgae

a

b

s

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r

a

c

t

Rhodolithsarefree-livingnodulesformedbycrustosecorallinealgaethatpromote

multi-dimensionalmicrohabitatsforahighlydiversecommunity.BecausetheirCaCO3production,

rhodolithbedsconstituteareasofinterestforminingactivities.Ontheotherhand,other

goodsandservicesprovidedbytheseenvironmentssuchasnurserieshabitats,fishingand

climateregulationremainundersized.BesidesdirectlyCaCO3exploitation,thesediverse

ecosystemswithintheBrazilianeconomicexclusivezoneareoftencoveringpotentiallysites

foroilandgasextraction.TheIBAMA(EnvironmentalAgencyoftheBraziliangovernment)

havebeenapplyingtheprecautionaryprincipletodenyrequestsforoil/gasdrillingactivities

whererhodolithbedsoccur.Here,wediscussrecentdataaboutdiversityassociatedwith

rhodolithsandalsorecordthe“rare”wormNuchalosylliscf.maiteae.Morethanthe

distribu-tionofoneonlyspecies,ourfindingisanemblematicexampleofourinfancyknowledge

stateaboutdiversityassociatedwithrhodolithbedsinsouthwesternAtlantic.Wearguethat

theseknowledgeisstillinsufficienttosubsideanyattemptinclassifyprioritiesareasfor

oilwellsdrilling.Inaddition,weclaimthattheprecautionaryprincipleadoptedbyIBAMA

mustprevalenceuntilwehaverobustdataallowingpredictionsconcerninghigherorlower

biodiversityassociatedwithrhodolithbeds.

©2016Associac¸ ˜aoBrasileiradeCi ˆenciaEcol ´ogicaeConservac¸ ˜ao.PublishedbyElsevier

EditoraLtda.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http://

creativecommons.org/licenses/by-nc-nd/4.0/).

∗ _{Correspondingauthor.}

E-mailaddress:pereira.filho@unifesp.br(G.H.Pereira-Filho).

http://dx.doi.org/10.1016/j.ncon.2016.06.002

1679-0073/©2016Associac¸ ˜aoBrasileiradeCi ˆenciaEcol ´ogicaeConservac¸ ˜ao.PublishedbyElsevierEditoraLtda.Thisisanopenaccess

bycrustose corallinealgae.Theyoccurworldwideandmay

formlargebedsthatcoverhugeexpanseoftropical,

temper-ate,andevenpolarshelves,providingmulti-dimensionalhard

microhabitatsfordiversebiologicalcommunities(Fosteretal.,

2013).BecauseoftheirhugeCaCO3accumulation,rhodolith

bedsconstituteareasofgreatinterestforcarbonates’mining

thatsuppliesagriculturalandindustrialapplications

(Amado-Filhoetal.,2012a;Mouraetal.,2013).Whilerhodolithbeds

are largely and mistakenly seen as mineral resources, the

ecosystem services they provide, such as fishing and

cli-mate regulation, are grossly underrated in environmental

impact assessments(Amado-Filho and Pereira-Filho, 2012).

In Brazil, the country with the world’s largest rhodolith

beds,extractionofup to18t/companyyear−1 may be

regu-larlylicensedbyIBAMA,theFederalEnvironmentalLicensing

Agency (Instruc¸ão Normativa 89, Feb. 02, 2006). Although

sub-surfacerhodolithsare oftenaliveanddefinitelyharbor

high marine biodiversity, the Brazilian law refers to them

asnon-livingmarineresources,withexploratoryregulations

established by the National Mining Department

(Departa-mento Nacionalde Produc¸ão Mineral– DNPDM).Moreover,

rhodolithbedsoverlapwithseveraloilandgasfieldswithin

the Brazilian Economic Exclusive Zone (EEZ). The

build-ing of new infrastructurein such areas has been recently

restrictedbyIBAMA,basedonthePrecautionaryPrinciple–

afundamentaltoolforcounteringthechronicoverlookof

sci-entificuncertaintiesinanunscientificmanner(Cooney,2004).

A

N

Brazil

B

C

Fig.1–SamplinglocalitiesforallknownspecimensofNuchalosyllis.(A)FernandodeNoronhaArchipelago(detail).Light brownpatchesindicateareaswhererhodolithbedshavebeenmapped(Gherardi,2004;Pascellietal.,2013;Amado-Filho etal.,2007;Amado-Filhoetal.,2010;Villas-Boasetal.,2013;Pereira-Filhoetal.,2012;Amado-Filhoetal.,2012a;Bahia etal.,2010;Riuletal.,2009;TestaandBosence,1999;Amado-Filhoetal.,2012b,respectivelyfromsouthtonorth).Blue arrowsindicatelocalitiesofthetwoknownNuchalosyllisspecies,(FukudaandNogueira,2012;RullierandAmoureux,1979). DarkgreenarrowindicatesthesitewherewesampledNuchalosyllisat40mdepth.(BandC)Detailofrhodolithbed(Photos: ZairaMatheus).

etal.,2010;Bahiaetal.,2010;Brasileiroetal.,2015),

knowl-edgeaboutthedistributionandbiodiversityassociatedwith

rhodolithbeds inBrazil isstillfragmentedand incomplete,

impedingthoroughenvironmentalimpactassessmentsofthe

steadilygrowingindustrialactivities.Paradoxically,

uncertain-tiesinpredictingenvironmentalimpactshavebeenevoqued

byeconomicgroupsasareasonfortheapprovalofmining

licenses(Cooney,2004).Oncerhodolithbedscoverextensive

areas ofthe BrazilianEEZ (Fig.1A),large-scale mining and

hydrocarbon’s exploitation are indeed an imminent threat

withyetunpredictableconsequences.Here,whilerecording

theoccurrenceofthe“raregenus”Nuchalosyllis(Polychaeta)in

theFernandodeNoronhaArchipelago(FNA),weemphasize

themajorknowledgegapsaboutthebiodiversityassociated

toBrazilianrhodolithbeds,andtheconsequencesfor

envi-ronmentallicensing.

Beforeourfind(Fig.1)(specimendepositedinMNRJP785),

Nuchalosyllismaiteaewasonlyknownfortheholotype(MZUSP

01016)collected at75mdepthoffshoreRiodeJaneiroState

(Fukuda and Nogueira, 2012). Suchas other known specie

of the same genus, N. maiteae was initially obtained by

ship-based dredgingand grabbing. Despite being the tools

used to provide most of the currently available biological

data about rhodolith-associated biodiversity (Foster et al.,

2013),dredgingandgrabbingarelimitedforsamplingsmall

invertebrates within rhodoliths’ microhabitats, especially

Fig.2–Nuchalosylliscf.maiteae.(A)Anteriorend,dorsalview.(B)Parapodia15,posteriorview;(C)detailofdorsalcirriwith darkredinclusions;(D)Chaetaeheterogomphfalcigerfromparapodia15;(E)Chaetaeheterogomphfalcigerfromparapodia 41;(F)parapodia41,posteriorview,dorsalcirrilost;(G)dorsalcirrophorewithpapillae.Papillae.Legends:ac.,Acicula;cp., Cirrophore;pa.,Papillae;pc.,Peristomialcirri;vc.,Ventralcirri.Scale:A.0.8mm;B.0.13mm;C.0.25mm;D.0.03mm;E. 0.03mm;F.0.1mm;G.0.08mm.

significantrolesinfoodweb(Fosteretal.,2013;Kenchington

and Hutchings, 2012).Only recentlythe use ofSCUBA has

been recognized and established as a complimentary tool

forsamplingsuchsoft-bodiedinfaunalspecies(Fosteretal.,

2013).Forexample,SCUBA-basedassessmentsinCalifornia,

USA, revealed eight species of cryptofaunal chitons, four

ofwhich were previouslyundescribed (Clark, 2000).Santos

etal.(2011)alsousedSCUBAtosamplehoneycombworms

(Polychaeta:Sabellariidae),findingthatsixofthetenSabellaria

rodoliths.

Despitetheaforementionedvalueforcomprehensive

bio-diversityassessments,SCUBA recreational standards limits

sampling to <30m depths. Recently, we used mixed-gas

(TRIMIX)andtechnicaldivingtechniquestosamplerhodolith

bedsinscatteredcontinentalandoceaniclocalitiesalongthe

Brazilian coast (e.g. Pereira-Filho et al., 2012; Moura et al.,

2013;Amado-Filho etal., 2016).Althoughwesampled only

onespecimenofN.cf.maiteaeintheFernandodeNoronha

Archipelago (i.e.; >2000km from the type and onlyknown

locality)(Figs. 1 and 2), it ispossible to hypothesizedthat

thedistributionofthistaxonismuchwiderthanpreviously

known,andthatsamplingeffortisinsufficienttoany

com-prehensiveunderstandingaboutthebiodiversityharboredby

thishabitat.Morethananadditionalrangeextensionrecord

foroneofhundredsofthousands“worm”species,N.maiteae

isanemblematicexampleoftheincipientknowledgeabout

the biodiversity of Southwestern Atlantic rhodolith beds.

Conversely,researchanddiscoveryofhydrocarbon

exploita-tion fields rapidly increased in the last decade, especially

inthemesophotichabitatsofthis region(e.g.,Mouraetal.,

2013), many of those in rhodolith beds such as Peregrino

oilfield,CamposBasin(Tâmegaetal.,2013,2014),thearea

whereN.maiteaewasdiscovered.Offshoredrillingincreases

theconcentrationofsuspendedparticles(Patin,1999),with

well-establishednegativeeffectsoverthehealthofcrustose

coralline algae (e.g., Reynier et al., 2015) and

community-widechangesfromsedimentationandcontamination(Patin,

1999).

Theterm“rarespecies”isassociatedtolowfrequencyand

smallpopulationsizes(Caoetal.,1998).Evenonlytwo

speci-mensofN.maiteaehavebeenfounduptodate;thesampling

effortistoolimitedtoclassifyitoranyotherassociatedspecies

asrareorabundant.Basicinformationaboutpredictor

vari-ablesofassociatedbiodiversityisstilllacking(e.g.;rhodolith

size,volume,form,complexityanddensity).Rhodolithbeds

are extensive and heterogeneous habitats, and the small

spatial scales within the nodules representand additional

challenge fordesigning comprehensivesampling programs

to assess biodiversity patterns. However, considering the

increased rates of anthropogenic disturbances (Broderick,

2015),itisclearthatthetimingneededforextensivesampling

isnotcompatiblewiththespeedatwhichimportant

manage-mentdecisionsneedtobetaken(KenchingtonandHutchings,

2012).

Whilerobustdataon species’occurrencesand

distribu-tion patterns accumulate, and surrogates for biodiversity

patterns are developed(Kenchingtonand Hutchings, 2012),

the precautionary principle adopted by IBAMA must be

consistently appliedin order tosafeguard biodiversityand

ecosystemservicesprovidedbyrhodolithbeds,asevidenced

fromrecentdataaboutmacroalgae(Amado-Filhoand

Pereira-Filho, 2012), fishes (Simon et al., 2016)and the polychaete

worm,N.maiteaerecordedherein.InsteadofpressingIBAMA

for rapid licensing, the industries that affect rhodoliths

andothermegadiversityBrazilianmarineecosystemsmust,

truly, engage in research and conservation initiatives that

go beyondthe immediate needs ofindividual exploitation

projects.

Conflicts

of

interest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

We thankthe Fernando de Noronha Marine National Park

staffforlogisticsupportandresearchpermits

(SISBIO/34245-3).FinancialsupportwasprovidedbytheBrazilianResearch

Council (CNPq; grant 484875/2011-6 to GHPF). GMAF, RBFF

andRLMacknowledgegrantsfromCNPq,CAPES,FAPERJand

Brasoil. PCV and JBL acknowledge their scholarships from

Fundac¸ão de Amparo à Pesquisa do Estado de São Paulo

(FAPESP, processes 2013/26594-4 and 2015/15212-9,

respec-tively).

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