On some cryptic sponges associated with Lessonia trabeculata holdfasts in the South-eastern Pacific

Marine Biology Research

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On some cryptic sponges associated with Lessonia trabeculata holdfasts in the South-eastern Pacific

Christian Polo, Bernabé Moreno, Yessenia Arroyo & Báslavi Cóndor-Luján

To cite this article: Christian Polo, Bernabé Moreno, Yessenia Arroyo & Báslavi Cóndor-Luján (2022): On some cryptic sponges associated with Lessonia trabeculata holdfasts in the Southeastern Pacific, Marine Biology Research, DOI: 10.1080/17451000.2022.2123521

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Onsomecrypticspongesassociatedwith Lessoniatrabeculata holdfastsinthe South-easternPacific ChristianPolo a,BernabéMoreno a,b,YesseniaArroyo a andBáslaviCóndor-Luján a aCarreradeBiologíaMarina,FacultaddeCienciasVeterinariasyBiológicas,UniversidadCientíficadelSur,Lima,Perú; bMarineEcology Department,InstituteofOceanology,PolishAcademyofSciences,Sopot,Poland

ABSTRACT

ThewarmtemperateSouth-eastPacificcoasthostsextensivekelpforeststhatprovide protectedhabitatstobenthicorganismssuchassponges.Tosoundlyunderstandthe interactionsbetweenkelpsandsponges,apriortaxonomicidentificationoftheassociated speciesisnecessary.Thisstudyaimedtoreportcrypticspongesfoundassociatedwiththe innerwallsoftheholdfastofthekelp Lessoniatrabeculata,opportunisticallycollectedinthe upwellingareaofSanJuandeMarcona(15°S,Peru).Threespongeswereidentified includingoneCalcarea, Clathrinaantofagastensis,andtwoDemospongiae, Johannesia reticulosa and Haliclona (Halichoclona) paracas.Noneofthemwaspreviouslyknownto occurassociatedwithkelps.These findingshighlighttheimportanceofexploringtheselessstudied(biogenic)substratestouncoverhiddenmarinebiodiversityandtheneedfor observationalorexperimentalstudiesaddressingtheinteractionsdevelopedbetweenkelps andtheirepiphytozoans.

Introduction

Kelpforestsconstituteoneofthemostconspicuous coastalmarineecosystemsthatdeveloponcoldwatershallowrockybottoms(Stenecketal. 2002).As autotrophs,theyareamongstthemostprolific primaryproducersglobally,formingbluecarbonhabitatsduetotheircapacityofcapturing(throughphotosynthesis)andstoringcarbonbyaccumulating biomassorgeneratingburialratesinsediments(Pessarrodonaetal. 2018),andultimatelyserveasa sourceforoutwellingprocesses(i.e.organicmatter exporttosurroundingareas,expandingprimaryproduction,seeSantosetal. 2021).Asecosystemengineers,theyprovidesuitablemicro-habitatsforthe colonizationofepifauna;inaddition,theyprovide abundantfoodsourceforprimaryconsumerssuchas herbivorous fishesandinvertebrates,thusincreasing secondaryproductivity(Smaleetal. 2013;Shelamoff etal. 2020).Moreover,theholdfastsofsomekelp speciesarecharacterizedbytheirlargesize,complexityandrobustness,providinganintricatesubstrate fordiverseorganismstothrive,includingsessile filter feederssuchassponges(phylumPorifera;Bell& Barnes 2000;Abdullah&Fredriksen 2004).

Kelpholdfastsappeartobeappropriateforsponge larvalsettlementandearlydevelopment,asthey

©2022InformaUKLimited,tradingasTaylor&FrancisGroup

ARTICLEHISTORY

Received11May2022

Accepted6September2022

KEYWORDS

provideasubstratecharacterizedbylowlightintensityandlowsedimentationrates(Bell&Barnes 2000; Cárdenasetal. 2012, 2015).However,fromallthe reportedtaxaassociatedwith,andfoundwithinthe kelpholdfasts,Poriferaisunderrepresentedand poorlyidenti fied(Fernándezetal. 1999;González etal. 2002;Włodarska-Kowalczuketal. 2009).To helpreducethisknowledgegap,thisstudyaimsto reportthespongesopportunisticallyfoundinthe innerwallsoftheholdfastof Lessoniatrabeculata Villouta&Santelices, 1986,oneofmostcommercially exploitedkelpspeciesfromtheHumboldtCurrent LargeMarineEcosystem.

Materialsandmethods Sampling

Spongesampleswereobtainedfromapreviousstudy focusedontheassessmentofcarbonassimilationby kelps,conductedinSanJuandeMarcona,Ica,Peru, inMay2019(seeAller-Rojasetal. 2020). During that fieldwork,atotalof42kelpswerecollectedin threesitesbutattentiontothespongesassociated withtheholdfastswastakenonlyat ‘Playa Hermosa’ (15°21′ 10.80′′ S,75°10′ 4.80′′ W),at11m depth.Fromthethreekelpssampledin ‘Playa

Clathrina;Epiphytozoans; Haliclona; Johannesia;Peru; Porifera

Hermosa’,spongeswereobservedinallofthem,but onlyonekelp(holdfast)wasproperlycollectedand fixedforspongetaxonomystudies.

Kelpsporophyteswereidentified insitu following thedescriptionsofVillouta&Santelices(1986)and Arakakietal.(2018).Thepresenceofanirregular holdfastandslightly flattenedstipesinthespecimens,togetherwiththesubtidaldistribution matched Lessoniatrabeculata.Kelpsweredetached fromthesubstrateeithermanuallyorusinga modifiedaxe ‘barreta’ (fordetailsseeAller-Rojas etal. 2020;Morenoetal. 2021).Onceatthe surface,spongeswerecarefullyremovedfromthe innerwallsoftheholdfast, fixed,andpreservedin 96%ethanol.

Toregisterthe invivo characteristicsofthe sponges,underwaterphotographsweretakenwith acompactunderwatercamerarigconsistingofa GoProHERO6Blackeditionactioncamerawitha +15MacroMateminimacrolensandtwoSOLA 2000videolights.

Spongespeciesidentification

Externalmorphology(i.e.sizeandcolour,textureand consistency,sizeanddistributionofoscula)and internalanatomy(i.e.aquiferoussystemandskeleton organization)weredescribedfollowingBoury-Esnault &Rützler(1997)andKlautau&Valentine(2003).To characterizetheskeleton,sectionandspiculeslides werepreparedfollowingstandardproceduresfor Demospongiae(Rützler 1978;MothesdeMoraes 1985)andCalcarea(Klautau&Valentine 2003). Lengthandwidthofeachspiculecategory weremeasured,considering n =30spicules(when possible),fromwhichminimum,maximum,mean andstandarddeviationvalueswerecalculated,and presentedasfollows:min–mean±SD–max.Detailed observationsweremadeusingastereomicroscope CarlZeissStemiDV4andmicroscopeNikon Eclipsee100.Photographsofthepreservedspecimensandmicroscopeslidesweretakenwitha NikonCoolPixP310cameracoupledtotheoptic equipment.Speciesidentificationsfollowed SystemaPorifera (Hooper&vanSoest 2002)aswell asspecializedliterature(Gerasimovaetal. 2008; Azevedoetal. 2009, 2015;Bispoetal. 2022) andthemostrecentacceptedsystematic indices(Klautauetal. 2013;Morrow&Cárdenas 2015).Specimensweredepositedinthe ScientificCollectionofUniversidadCientíficadelSur (UCSUR).

Results

Taxonomy

ClassCalcarea Bowerbank,1862

SubclassCalcinea Bidder,1898

OrderClathrinida Hartman,1958

FamilyClathrinidae Minchin,1900

Genus Clathrina Gray,1867

Clathrina Gray,1867:(513).

Typespecies: Clathrinaclathrus (Schmidt,1864):(24).

Clathrinaantofagastensis Azevedo,Hajdu,Willenz& Klautau, 2009

(Figures1Aand 2, TableI)

Clathrinaantofagastensis:Azevedoetal. 2009:4, figure2;Azevedoetal. 2015:796, figure4.

Materialexamined

UCSUR07-000062,07–000083and07–000084(ethanol); PlayaHermosa,SanJuandeMarcona,Ica,Peru,15° 21′ 10.80′′ S,75°10′ 4.80′′ W,11mdepth,17May2019,collectorB.Moreno.

Description

Whiteinlifeandbeigeinethanol(Figures1Aand 2A). Finelyencrustingtoslightlymassivesponge.Smooth surface.Softandfragileconsistency.Thelargestspecimen(07-000083)measures12.0×4.0×1.5mm. Cormusformedbyirregularandmostlylooselyanastomosedtubeswithwater-collectingtubes(Figures1A and 2A).Asconoidaquiferoussystem.

Skeleton

Withoutanyspecialorganizationandexclusivelycomposedoftriactines(Figures2B–C).

Spicules

TriactinesI.Regular(equiangularandequiradiate). Actinesareslightlyconicaltoconical,slightlyundulated atthedistalpart,andwithsharporblunttips,50

82.3± 9.5–102.5×6.3–8±0.9–10µm(Figure2D, TableI).

TriactinesII.Regular(equiangularandequiradiate). Actinesareconical,straight,andwithsharptips,27.5–42.3±5.4–52.5×5–5.3±0.4–6.3µm(Figure2E, TableI).

Ecology

Clathrinaantofagastensis waspreviouslycollectedin intertidalandsubtidalrockysubstrates,inhabiting

areasprotectedfromsunlight(underneathboulders) andwithmoderatetohighconcentrationof sediments.Ithasbeenfoundattachedtoredmacroalgae(Rhodymenia sp.)andgastropodshellsandcloseto ascidians,brachiopods,bryozoans,hydroids,polychaetesandothersponges,downto24mdepth

(Azevedoetal. 2009, 2015).Itis firstlyreportedinhabitingtheinnerwallsofakelpholdfast(L. trabeculata), at11mdepth.Withintheholdfast,thedistance amongtheindividualsvariedfrom5–188mm(rough estimationobtainedfromtheunderwaterimages, Figure1).

Figure1. Spongesassociatedwith Lessoniatrabeculata holdfast.(A) Clathrinaantofagastensis (water-collectingtubeindicatedby circle);(B) Johannesiareticulosa;(C) Haliclona (Halichoclona) paracas

Figure2. Clathrinaantofagastensis Azevedoetal.(2009)(UCSUR07-000062):(A)specimenafter fixation;(B)cormusanastomosis; (C)skeleton(tangentialsection);(D)triactineI;(E)triactineII.

TableI. Spicule(triactines)measurementsof Clathrinaantofagastensis.Min,minimum;Max,maximum;SD,standarddeviation;N, numberofspiculesmeasured;H,holotype.

1Azevedoetal.(2009); 2Azevedoetal.(2015):specimensMNRJ11282,MNRJ13125andMNRJ13148.

Remarks

Theanalysedspecimensresemble C.antofagastensis in bothexternalmorphologyandskeletoncomposition butpresentsubtledifferences.Intheoriginaldescription,basedontheexaminationoftwospecimens fromChile,Azevedoetal.(2009)describedthis speciesasalightbeigespongeformedbytightlyanastomosedtubeswithnowater-collectingtubes.Later, consideringtheanalysisof10specimensfromPeru, Azevedoetal.(2015)specifiedthatthecolourinlife of C.antofagastensis couldalsobewhiteandthat water-collectingtubeswereobserved.Differentfrom theholotypeandthespecimensofAzevedoetal. (2015),theanastomoseofthecormusofourspecimensismostlyloose(asifthetubeswereexpanding onanewsubstrate),butinsomeotherregions,it canalsobecometight.Thiscormusvariationhas beenpreviouslyreportedinotherclathrinas(e.g. Klautauetal. 2020),anditmaycorrespondtothe species’ morphologicalvariability.Therefore,weidentifyourspecimensas C. antofagastensis.Thisspeciesis distributedfromthenorthcoastofChile(23°S,Antofagasta)tothenorthofthePeruviancoastline(5°S,Piura; Azevedoetal. 2009, 2015).Herein,weaddanew localityrecord:PlayaHermosa(15°S,Marcona). MEOWecoregion:CentralPeruandHumboldtian (Spaldingetal. 2007).

ClassDemospongiae Sollas,1885

SubclassHeteroscleromorpha Cárdenas,Pérez& Boury-Esnault,2012

OrderSuberitida Chombard&Boury-Esnault,1999

FamilyHalichondriidae Gray,1867

Genus Johannesia Gerasimova,Erpenbeck&Plotkin, 2008

Johannesia Gerasimova,Erpenbeck&Plotkin, 2008: (19).

Typespecies: Johannesiareticulosa (Thiele, 1905):(423).

Johannesiareticulosa (Thiele, 1905)

(Figures1Band 3, TableII)

Vosmaeriareticulosa Thiele, 1905;423, figures45a–c; Erpenbeck&VanSoest,2002;815.

Johannesiareticulosa Gerasimovaetal. 2008;19; figures10–12.

Materialexamined

UCSUR07–000061(ethanol);PlayaHermosa,SanJuan deMarcona,Ica,Peru,15°21′ 10.80′′ S,75°10′ 4.80′′ W, 11mdepth,17May2019,collectorB.Moreno.

Description

Orangeinlifeandbeigeinethanol(Figures1Band 3A). Massivesponge(fragment:31×25×70mm, Figure3A). Surfaceslightlyroughandridged.Compressibleconsistency.Osculaarecircular(1.2mm,diameter)andrandomly disposedonthesurface.Leuconoidaquiferoussystem.

Skeleton

Specializedanddetachableectosome.Ectosomalskeleton reticulated,withmeshescomposedoftylostylesandoxeas (Figure3B).Choanosomalskeleton,composedofmultispicularascendingtractsoftylostyles.Someoxeaslocated obliquelyalongthetractswerealsoobserved.Oxeasand fewtylostylesarescatteredbetweenthetracts,arranged perpendicularly,interconnectingtheascendingtracts (Figure3C)orliningthesubectosomalcavities.

Spicules

Oxeas.Straightandslightlycurved,330–508.9±70.5–670×5–12.3±2.8–17.5µm(Figure3D, TableII).

Tylostyles.Mostlyslightlycurvedbutalso straight,withsharptips,160–290.3±54.4–400×

5–7.9±1.3–10.3µm(Figures3E–G, TableII).Somesubtylostyleswerealsofound(Figure3H).

Ecology

Johannesiareticulosa waspreviouslyfoundassociated withthesponge Plicatellopsisexpansa at30mdepthin Chile(Thiele 1905).Nomoredetailsregardingthetype ofsubstratewereprovided.Herein,wefounditcovering theholdfastof Lessoniatrabeculata,at11mdepth.

Remarks

Themorphologicalcharactersobservedintheanalysed specimenmatchtheoriginaldescriptionof J.reticulosa aswellasitsre-description(Thiele 1905;Gerasimova etal. 2008).Onlyaslightdifferencewasnoticed;incontrasttoGerasimovaetal.(2008),someoxeasalsocomposedthemaintractsofthechoanosomalskeletonof thespecimenfromSanJuandeMarcona.Thisspecies isknownfromnorthernChile(20°S,Iquique)to southernPeru(14°S,Paracas,Thiele, 1905;Gerasimova etal. 2008),andnow,weincludeanintermediate locality(15°S,SanJuandeMarcona).MEOWecoregion: Humboldtian(Spaldingetal. 2007).

OrderHaplosclerida Topsent,1928

FamilyChalinidae Gray,1867

Genus Haliclona Grant,1841

Subgenus(Halichoclona) deLaubenfels,1932

Haliclona (Halichoclona)deLaubenfels,1932(113).

Typespecies: Haliclona (Halichoclona) gellindra (de Laubenfels,1932)(114).

Haliclona (Halichoclona) paracas Bispo,Willenz& Hajdu, 2022 (Figures1Cand 4, TableIII)

Materialexamined

UCSUR07–000063(ethanol);PlayaHermosa,SanJuan deMarcona,Ica(15°21′ 10.80′′ S,75°10′ 4.80′′ W),11m depth,17May2019,collectorB.Moreno.

Description

Beigeinlifeandslightlytransparentinethanol(Figures 1Cand 4A).Encrustingtomassivesponge(18×13× 3mm).Surfacesmoothandporous.Compressible andsoftconsistency.Osculaaresmallcircles(1

2mm,diameter)randomlydisposedonthesurface (Figure4A).Leuconoidaquiferoussystem.

Skeleton

Ectosomalskeleton,atangentiallayerwithunispicular isotropicreticulation(Figure4B).Choanosomalskeleton dense,forminganisotropicnetworkmostlyunispicular, occasionallywith2–3oxeasbyside(Figure4C).

Figure3. Johannesiareticulosa (Thiele 1905)(UCSUR07-000061):(A)specimenafter fixation;(B)ectosomalskeleton(tangential section);(C)choanosomalskeleton(crosssection);(D)oxeas;(E–G)tylostyles;(H)subtylostyle.

TableII.

Spiculemeasurementsof Johannesiareticulosa.Min,minimum;Max,maximum;SD,standarddeviation;N,numberof spiculesmeasured;H,holotype.

Spicules

Oxeas.Slightlycurved,small,acerate,125–143.8±9.2–155×6.3–7.9±0.9–10µm(Figure4D, TableIII).Verythin oxeaswerealsoobservedintheectosome(Figure4D’).

Ecology

Haliclona (Halichoclona) paracas waspreviouslyfound growingonrockysubstrate,attachedtoothersponges andseaanemones,at8mdepth(Bispoetal. 2022). Herein,we firstlyreportitassociatedwiththeholdfast of Lessoniatrabeculata,at11mdepth.

Remarks

Amongthe10 Haliclona speciesreportedfromPeru (deVoogdetal. 2022),ourspecimenissimilarto

1Thiele(1905), 2Gerasimovaetal.(2008), 3Gerasimovaetal.(2008):specimensHL2352,HL2354andHL2425.

6 C.POLOETAL.

TableIII.

(14°S,Paracas,Bispoetal. 2022)andnow,weextendits distributiontoPlayaHermosa(15°S,Marcona).MEOW ecoregion:Humboldtian(Spaldingetal. 2007).

Discussion

Severalspeciesofspongeshavebeenreportedasepiphytozoans(sensu Taylor&Wilson, 2002)onholdfast kelpsdistributedworldwide.Acompilationofthese speciesisshowninTableSI,includinglocalitiesin theNorthAtlantic(Christieetal. 2003;Blight&Thompson 2008;Wallsetal. 2016;Teagleetal. 2018),Western Pacific(Flukes,Johnson&Wright 2014;Cárdenasetal. 2015)andEasternPacific(Ávilaetal. 2010;Cárdenas etal. 2016;Vega 2017;Carbajaletal. 2022).Regarding theSouth-easternPacific,intheMagellanStrait, Amphimedon cf. maresi, Clathrina sp.and Haliclona cf. porcelana werefoundassociatedwiththegiantkelp Macrocystispyrifera,whereas H. cf. porcelana, Halisarca sp.and Scopalina sp.havebeenreportedinassociation with Lessonia spp.,including L.vadosa and L. flavicans (Vasquez&Santelices 1984;Cárdenasetal. 2016;Vega, 2017;Newcombe&Cárdenas 2011;seeTableSI,for moredetails).InPeru,spongesassociatedwiththe holdfastof L.trabeculata and M.pyrifera havebeen recentlyreported,howevertheiridentificationhas remainedasundetermined(Carbajaletal. 2022).

Toourknowledge,thisstudyrepresentsthe first descriptionofthespongespeciesoccupyingtheholdfastinnerwallsofthesubtidalkelp L.trabeculata inthe South-easternPacific. Thesespongescorrespondedto threepreviouslyreportedspecies,whichwerefound attachedtorockysubstrates(Azevedoetal. 2009, 2015; Bispoetal. 2022)ortoothersponges(Thiele 1905),indicatingthattheyarenotexclusivelyassociatedwithholdfastkelps.

Lessoniatrabeculata isthesecondmostcommerciallyexploitedkelpspeciesintheSEPacific,andis byfarthemostabundantoftheseinthesublittoral fringeenvironment(Vásquez 2016).InPeru,kelp researchhasbeenfocusedonkelppopulationstructureanddynamics(Zavalaetal. 2015;Tejadaetal. 2019)astheyproviderelevantinformationtohelp regulatetheextractionofthisbioresource.However, studiesonthemacrofaunaassociatedwithkelpsas

.Min,minimum;Max,maximum;SD,standard

wellastheinteractionsamongthemhavereceived limitedattention(butseeRomeroetal. 1988;Carbajal etal. 2022).Assessingthoseinteractionswouldhelpin understandingtheinfluenceofotherorganisms(such assponges)onkelpforestfunctioning,andwould eventuallyprovidenewinsightsforthemanagement ofkelpresources.

Theopportunisticsamplingdescribedinthisstudy yieldednewunderstandingonthespongesaskey usersofthekelpinnerwalls,highlightingthe urgencyofspecialistsforcompletingthetotal specieslistatthelowestpossibletaxonomiclevel. Thethreespongesidentifiedhereindonotreflect thespongerichnessassociatedwiththeholdfastof L.trabeculata.Itispossiblethatifalargernumberof holdfastsofthisspeciesareanalysed,moresponge specieswouldbefoundasthissubstratefacilitates larvalsettlementandjuvenilegrowth(Bell&Barnes 2000;Cárdenasetal. 2012, 2015).

Our findingshighlighttheimportanceofexploring theseless-studied(biogenic)substrates(kelps)to uncoverthecrypticmarinebiodiversity,andthe needforobservationalorexperimentalstudiesaddressingkelp–spongeinteractions.

Acknowledgements

WearethankfultoEdgarLopezandFernandoCaldasfor aidinginthelaboratoryprocedures.Thanksaredueto D.K.A.BarnesandR.Downeyfortheircommentsonthe firstdraftofthemanuscript,aswellastothetwoanonymous refereesforprovidingtheirvaluablefeedback.

Disclosurestatement

Nopotentialconflictofinterestwasreportedbythe author(s).

Funding

ThisworkwassupportedbyUniversidadCientíficadeSur underGrant ‘EvaluacióndeladiversidaddeDemospongiae (PhylumPorifera)delascostascentralysurdelPerú (FondoSemilla2019,N°015-2019-PRO99)’ and ‘Inmovilizacióndecarbonoazulporbosquesdemacroalgasenel litoralcentro-surdelPerú(FondoSemilla2018)’

Spicule(oxeas)measurementsof Haliclona (Halichoclona) paracas

deviation;N,numberofspiculesmeasured;H,holotype.

ORCID

ChristianPolo http://orcid.org/0000-0001-6775-8156

BernabéMoreno http://orcid.org/0000-0002-9751-6307

YesseniaArroyo http://orcid.org/0000-0003-2477-7079

BáslaviCóndor-Luján http://orcid.org/0000-0001-78327319

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