Hydrobiologia 375/376: 177–189,1998.S.Baden,L. Pihl, R. Rosenberg, J.-O. Strömberg, I. Svane& P. Tiselius(eds),Recruitment,Colonization andPhysical–ChemicalForcing in MarineBiological Systems.© 1998Kluwer AcademicPublishers. Printedin Belgium.

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Effectsof greenalgal matson infaunal colonization of a New Englandmud flat – long-lasting but highly localizedeffects

Martin Thiel∗ & Les WatlingDarling MarineCenter, University of Maine, Walpole, ME 04573,USA∗ Address for futurecorrespondence:Martin Thiel,SmithsonianMarineStation,5612Old Dixie Highway,Fort Pierce, FL 34946,USA; email: thiel@sms.hboi.edu

Key words: algalmats, soft-bottom infauna,community change,mudflats, reproduction

Abstract

Theresponseof benthic infaunato greenalgalmats iscommonly examinedin eithersmall-scaleshort-term exper-iments or large-scale long-term data sets that areaveragedover largeareas. In this study, we used a small-scaleapproachto study long-term effectscaused by therecurringappearanceof greenalgalmats in theearly 1990’sonaNew England mud flat. Algal matsfrequently coveredthe inner partsof themud flat, wherealgaepersistedfor 6monthsbetweenJulyandDecember, andwereincorporatedinto thesedimentafter thegrowth season.Theseinnerparts of the mud flat differedfrom the outer parts, wheregreenalgaenever occurred.Between1979and1996,infaunal numbers increasedten-fold at the 37 stations in the inner part, but not at the 19 stations in the outer partof the mud flat. Detritus-feeding annelids primarily contributed to thenumerical increase of infaunalcolonizers;grazing gastropodsandamphipods, and suspension- andfilter-feeding bivalves showed no change.Therecurringdevelopment and deposition of greenalgae in the inner part of the mud flat resulted in a localizedyet persistentchangein theinfaunalcommunity. Theresults suggest thatit is necessary to follow thefate of algalmatsafter thegrowth season. We propose that effectson infaunalcolonizersare most severe andlong-lasting wheredecayingalgalmatsfinally becomeincorporatedinto thesediment.Broodprotectingannelidsaremostlikely to benefitfromdetrital materialprovided by moderatelydensealgal mats.

Intr oduction

Growth of densegreenalgal matshasbeenreportedfrom intertidaland subtidal soft-bottomsfrom manypartsof theworld. Densealgal matscanhaveastrongimpact on macrofauna organisms (Nicholls et al.,1981; Soulsby et al., 1982; Breber, 1985; Butter-more,1977;Hull, 1987;Raffaelli et al., 1989,1991;Everett,1994;Petersonetal.,1994),resulting in deathof somespecieswhile othersmay thrive. In many ar-easwheremassdevelopmentof greenalgaehasbeenrecorded,simultaneouschangesof soft-bottom com-munitieshave beenobserved (Reise, 1982; Reise etal., 1989;Raffaelli et al., 1991).Most of these studiesarebased on qualitative samples(Reise et al., 1989)or selectedstationsthatweresampledin yearsbeforeand yearsafter the massoccurrenceof green algalmats (e.g.Nichollsetal., 1981;Raffaelli et al., 1991).

Several experimental studies have shown that algalmatsinitially have a detrimental effect on macrofau-nal numbers, but may at a later stage or after theremoval of thealgalcover result in increasednumbers(although reduceddiversity) due to rapid coloniza-tion by so-called opportunist species (e.g. Everett,1994; Norkko & Bonsdorff, 1996a, b). Althoughthese studiesshow that substantial changesoccurredin macrofaunanumbers, they usually do not allow fora detailedresolutionon a largerspatialscale.

Greenalgalmatsclearly have aneffect on macro-fauna communities, but it is not known how far-reachingtheseeffectsare,i.e.,whetherthey alsoaffectmacrofaunain neighboringsedimentsnotusually cov-ered by the algae. Experiments by Thrush (1986)haveshown thatmacrofaunain the immediatevicinity(0.5m) canbeaffectedby densemacroalgalmats,yetit is not known whether areasfurther away from the

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Figure 1. StudyareaLowesCove in theDamariscottaEstuary, Maine; macrofaunasamplesweretaken at 56 stationsin June1979andJune1996; biomass of greenalgaewasdetermined every month at stations8, 24 and55 in 1996; additionalmacrofaunadatawereevaluatedforstation32.

algal mats are also affected.Since greenalgal matsusually redevelop eachyear in the same areasof amud flat, but never or rarely cover other partsof amud flat (e.g. Reise, 1983; Reise & Siebert, 1994)two scenariosarepossible.In thefirstscenario,macro-faunachangesundergreenalgalmats may have somelarger scale effect on neighboring areasnot usuallycoveredby algae.In thesecondscenario,macrofaunachangesonly occuron mud flat areasimmediatelyaf-fectedby greenalgal mats, but macrofaunain areasadjacentto the matsarenot influenced.In this studywe used a small scalesampling approachthat allowsfor a detailed spatial resolution to examine which ofthe two scenariosis more likely to occur. Availableinformation on the life-history characteristicsof the

most commonmacrofaunaspeciesis usedto exam-inethereasonsfor theobserved pattern in macrofaunachanges.

Material and methods

Studysite

LowesCove is a shelteredcove in the DamariscottaEstuary, Maine, USA. Themud flat is surroundedonthreesidesby woodedareas(seeFigure1). Freshwaterdischargeinto theDamariscottaEstuaryison theorderof 1–3m3 s−1 (McAlice,1977;cited in Mayeret al.,1996), resulting in salinities of 30 at the study site.Maximumnitrate levels in theestuarinewatersrange

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Figure2. Extension andestimateddensity of greenalgalmatsin LowesCove betweenNovember 1995andDecember1996.

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between6 and12µm NO3-N (McAlice,1993;Mayeretal., 1996).

Sediments on the mud flat areclayey silt (McAl-ice 1993).Dense greenalgal mats did not develop inLowes Cove during the 1970sandearly 1980s(per-sonal observations). It is not known when the firstmassdevelopmentof greenalgaeoccurredin LowesCove, but at least since 1993 greenalgal mats de-veloped eachsummer and persisted throughoutthefall (pers. obs.). The first scientific observations ofdense greenalgal mats on mud flats in Maine are re-ported by Vadas& Beal (1987) for the mid 1980s.However, clam harvesterswere concerned with theeffectsof greenalgalmatson somemud flats in east-ern Maine throughoutthe 1970s(Arbuckle, 1982).In Lowes Cove the mats are composed primarily ofEnteromorpha species(E. prolifera usually being themost abundantspecies).

Sampling

The coverageof the mud flats by greenalgae wasqualitatively monitoredbetweenNovember1995andDecember1996 accordingto a scale (1–10% arealcoverage;11–30%coverage;31–70%coverage;71–100%coverage)providedby Schories(1995).At threestations (Nrs. 8, 24, and55 – Figure1) greenalgaewere collectedmonthly betweenNovember1995andDecember1996andtheir biomass (dry weight)deter-mined.A ring (176cm2 surfaceareaand1 cm high)wasplacedontothesediment.A knife wasusedto cutthe algaealong the inneredgeof the ring, the algallayer was carefully removed and placedin a plasticbag.Theupper1 cmof thesedimentwasthenscoopedinto a secondplastic bag. In the laboratory, the con-tentsof eachbagweresieved over a 1 mm-sieve. Allmacrofauna intertwined betweenthe algal layer wasremoved. All algaethat were found in the sedimentlayer weresorted out, combined with the algaefromthe algal layer and dried at 70 ◦C for 24 h. At eachstation(Nrs. 8, 24 and55) six replicatesamplesweretaken.

Macrofaunal samples were taken at 56 stationscovering the wholemud flat area(Figure1). At eachstation,onecore(78cm2 surfacearea)hasbeentakento a depth of 12 cm. Eachsample was sieved over a500-µm mesh,preserved in 4%-formalin,thenstoredin 70%-ethanol, and later sorted undera dissectingmicroscope.Macrofaunaspecieswereidentifiedto thelowest feasible taxonomic level andcounted.Sampleswere taken in June1979 and June1996. Additional

datafromoneselectedstation (Nr. 32,datafromThiel,1997; unpubl. data) were used to reveal whether theobserved infaunalchangesunderthe mat are a per-sistent phenomenonor only reflect a singular event.The trophic levels of macrofaunawere determinedfollowing theexampleprovidedby Ambrose(1993).

Themacrofaunadistribution pattern betweenJune1979 and June 1996 were comparedusing a fuzzycluster analysis. The relationshipsamongthe 56 sta-tions in eachyear were examinedby meansof thedivisive fuzzy c-meansclustering techniqueusing theprogramFCM (Podani, 1994)after applying a cube-root transformation to thedata (Findlay et al., 1995).Thismethodhastheadvantageof notconstraininganysample to anindividual cluster, but ratherdeterminingthedegreeof membership basedonthedistanceof thesample from the clustercenter. Herein, we present theresults of the fuzzycluster analysis in a geographicalmanner, rather thana list of membership functionsashasbeenusedin thepast (Findlayetal., 1995).On themaps, any sample having a membership affinity of atleast 0.1 (maximumaffinity to onecluster canbe1.0)to a second or third clusteris indicatedassharing itsmembership among two or moreclusters.

Results

Extension andbiomassof greenalgal mats in LowesCove

Greenalgalmatsonly developedin theeastern,mostsheltered, parts of LowesCove (Figure2). In 1995,dense algal mats that haddevelopedduring the sum-mer of 1995persisted until Novemberbut graduallydisappearedbetween November 1995 and January1996(Figure2). Greenalgaestarted to redevelop onthemudflats in June1996andreachedmaximumcov-eragein August 1996(Figures2 and 3). Coveragebygreenalgaewascomparatively low in 1996(compareNovember1995andNovember1996)but somealgalpatchespersisteduntil latefall (Figure4). Theaveragebiomass of greenalgaein August 1996rangedfrom< 1 g dry weight m−2 to more than 200 g dw m−2

(Figure3 andFigure4).

Abundanceanddistribution of macrofaunain 1979and1996

Macrofauna densities ranged between 6700 and74000 individuals m−2 in 1979andbetween10100and 237000 individuals m−2 in 1996. The densities

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Figure3. Biomass of greenalgaeat all 56stationsin August 1996;onesample was takenat eachstation.

increased about11-fold at the stations1–37between1979and1996while no such increase wasobservedat the stations38–56(Figure5). The largest numer-ical increaseswere observed for oligochaetes,spi-onid polychaetes, Capitella sp. and Leitoscoloplossp., while few changes occurred in bivalves, Hy-drobia sp., Corophium volutator andthe polychaetesNereis sp., Heteromastus filiformis and Mediomas-tus ambiseta (Figure 6a, b). At station 32 which isfrequently covered by greenalgae(see Figure2 andFigure3), apersistentnearly3-fold increasein macro-faunanumbersbetweenthe late 1970sandthe early1990soccurred(Figure 7). This increase in abun-danceof macrofaunacan primarily be attributed tosubsurface-living deposit-feeders(Figure7).

The results of the fuzzy cluster analysis showthat the station grouping pattern betweenJune 1979andJune1996hasdistinctly changed.In June1979,the results for the clustering partition in two, three

and four clustersshow a division along the east-westaxesthroughLowesCove(Figure8). Themacrofaunaassemblagein Lowes Cove was relatively heteroge-neous, indicatedby the fact that some stationsin theeastern-most parts hadsubstantial membership in thesameclustersassomeof thewestern-most stations. InJune1996,theclusterssplit alonganorth-southaxisataboutthe middle of LowesCove (Figure8). Theeast-erncluster(s)closelyoverlap with the areasthat werefrequentlycoveredby greenalgae(compareFigure2and Figure 3). The partition to threeclustersrevealsacluster that closelyoverlapswith the distribution cen-ter of greenalgae in LowesCove, while partitioninginto 4 clusterssplits off a ‘Corophium’ clusteron thenorthern edgeof Lowes Cove from the remainderofthewesterncluster (Figure8).

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Figure4. Averagebiomass (± 1 s.e.) of greenalgaeat station8 (opendots) andstation24 (filled dots) betweenNovember 1995andDecember1996;nogreenalgaewerefoundat station55.

Figure5. Total macrofaunaabundance(individualsm−2) at all 56stationsin LowesCove in 1979and1996.

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Figure6a. Abundanceand distribution of major macrofaunaorganisms (individualscore−1) in 1979and1996.

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Figure6b. For legendseep. 183.

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Figure 7. Total macrofaunaabundance(individuals [× 1000]m−2) at station 32 in LowesCove in June1979,August 1979,May 1994,June1996,August 1996andJune1997;at eachstationn= 1–3samplesweretaken;small boxesshow numbersfor minor functionalgroups.

Discussion

During the early 1990sgreenalgal mats frequentlycovered the eastern, sheltered, parts of Lowes Covewhich may be considereda relatively typical NewEngland mud flat. Between the late 1970sand theearly 1990sa strong increase in macrofaunaabun-danceoccurredin partsof themudflat thatareusuallycovered by greenalgaebut not in other parts. Thisincreaseis particularly due to subsurface-dwelling,deposit-feeding,annelids.

Extension,biomassandpersistenceof greenalgalmats in LowesCove

LowesCove is a relatively shelteredmud flat, greenalgaedevelopautochthonously,andremainonthemudflats until well after the growth season. Greenalgalmats persist throughoutthe fall and during the win-ter they are finally incorporated into the sedimentsby macrofaunal activities (seeFigure 4). Similarly,

for Chesapeake Bay Kemp et al. (1994)reported thatmacrophytespersist longerat the site of origin in ashelteredcove thanin anopenembayment.This pro-longedpersistenceof algalmats in onelocation is nottypical for mud flats in the EuropeanWaddenSeaorsubtidal watersin the Irish Seaand the Baltic Sea.Inthese areas, strong currents or storms may dislodgealgal matswithin days or weeks after first deposition(e.g.Thrush, 1986;Reise & Siebert, 1994;Norkko &Bonsdorff, 1996b).Thedislodgedalgaethenaccumu-late andare redeposited at other locations(Bonsdorff,1992).

Algal biomasses found in Lowes Cove are rel-atively moderate comparedto those found in otherstudyareasor usedin experimental studies. For exam-ple, Bonsdorff (1992)foundalgal biomasses of 150–830 g dw m−2, Everett (1994)foundanaveragealgalbiomass of ≈ 300 g dw m−2, Hull (1987)applied inthe most dense experimental treatmentapproximately300g dw m−2 (conversion factor fw to dw: 10), and

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Figure 8. Results of fuzzy cluster analysis for n= 56 samplesfrom June1979andn= 56 samplesfrom June1996;presentedare partitionsintwo, three,andfour cluster; cluster are indicatedby differentcoloursandshading;samplesthathaveaffinitiesof ≥ 0.1 to morethanoneclusterareindicatedby overlappingcoloursand shading;only onesample (station52 in June1979,3 cluster partition)hadaffinities to threeclusters.

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Table 1. Abundancechangesand reproductive traits of major macrofaunaspeciesin LowesCove,Maine.

SumJune SumJune Change > 5-fold Larval Duration

1979 1996 79–96 increase stage

Mya arenaria 144 133 n p l

Macoma balthica 251 101 – p l

Gemmagemma 0 159 + p l

Hydrobiasp. 3413 1262 – b

Corophiumvolutator 1578 753 – b

Oligochaetes 2853 24827 + + b

Heteromastusfiliformis 42 24827 + p m

Mediomastusambiseta 534 124 – p? ?

Capitellacapitata 67 4705 + + b/p m

Streblospio benedicti 268 5246 + + b/p m

Pygospio elegans 63 1831 + + b/p

Polydoraligni 42 630 + + b/p

Leitoscoloplossp. 376 1194 + b/p m

Tharyxsp. 109 51 – p m

Eteonesp. 50 262 + + b/p m

Exogonehebes 11 231 + + b?

Nereissp. 121 57 – p l

Nemertean (white) 0 136 + b

Changes: n= no change;–=decrease; + = increase.Larval stage:p= planktonic;b= benthic;b/p= bothreported.Durationof pelagicphase: l = long;m=moderate.

Norkko & Bonsdorff (1996a,b) applied artificial algalmatsof ≈ 440 g dw m−2, amounts that were rarelyreachedin LowesCove(seeFigures3 and4). Despitetheir relatively large areal extension and prolongedpersistence,algalmatsin LowesCove appearto havemoderatebiomass.They do not reachbiomassesforwhich strong detrimental effectson macrofauna havebeenreported (Hull, 1987;Bonsdorff, 1992;Everett,1994;Norkko & Bonsdorff, 1996a,b).

Macrofaunachangesin LowesCove between1979and1996

Few species decreased in abundancesbetweenJune1979 and June 1996 (e.g. Mediomastus ambiseta,Nereis spp.,Hydrobia sp.),but thesedecreasesdo notshow a distinct pattern.Somespeciesdecreasedrel-atively evenly throughoutthe mud flat (M. ambiseta)while othersdisappearedonly from the eastern parts(Nereis spp.)or from thewesternparts(Hydrobia sp.).The data obtained for snails Hydrobia sp. need tobeinterpretedwith cautionbecausethesesnailscom-pletely vanishedfrom LowesCove during the 1980sfor unknown reasons (own observations). While noconsistent spatial pattern was recognizablefor species

that decreased in abundance,a distinct pattern couldberecognizedfor speciesthat increasedin abundance.Several macrofaunaspecies increased in abundancebut theseincreasesare largely limited to the 37 sta-tions that wereat leasttemporarilycoveredby greenalgal mats in 1996(Table 1). The distinct pattern asrevealed by the fuzzy cluster analysis for June1996strongly indicates that the observed macrofaunare-sponse isan immediate result of theoccurrenceof thegreenalgal mats. While in June1979several diverseinfaunalassociationswere irregularly distributed overthe mud flats, the situation had drastically changedin June1996when a clearseparation is recognizablebetweenthestationsaffectedby greenalgalmatsandthose stations that were unaffected. It thus appearsthat green algae have a strong impact on infaunalcolonization, and those effects may overshadow ef-fects of e.g. predation, adult-larval interactions andsediment-disturbance.

Theincreasein macrofaunaabundanceisprimarilydueto subsurface-dwelling,deposit-feeding,annelidsthat aretolerantto, or even benefitfrom, enrichmentof sediments with organic matter (oligochaetes,spi-onid polychaetes, Capitella sp.). Thisdominanceshift

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towards burrowing detritivoresunderalgal mats wasalso observed by Norkko & Bonsdorff (1996b).Thespeciesresponsible for this shift arethose most likelyto benefitfrom organic detritusin form of decayinggreenalgal parts becausethey are able to toleratehypoxiacommonlyassociatedwith these algal mats.They are also relatively mobile within the sedimentandmay move higherup in thesedimentin responseto decreasing oxygenlevels.

Is life history responsible for highly localizedeffects?

When discussing the colonization pattern of marinesoft-bottoms, consideration of the life history of po-tential colonizersis important (Thrush & Townsend,1986;Shull, 1997).In defaunated sediments, thefirstcolonizersusually arespecieswith planktonic larvalstages. These initial colonizers are generally poorcompetitorsand usually disappearat a later succes-sional stage when larger organisms that are compet-itively superior reachadult size (e.g. Watling, 1975;Pearson & Rosenberg, 1978). Temperate intertidalmud flats are inhabited by macrofauna specieswithhighly diversereproductivestrategies. Larvaeof somespecies have long-lasting (months to weeks) plank-tonic larval stages (e.g. large bivalves, large poly-chaetesand other worms) while othersspendveryshort time periodsin the water column (daysto hours– e.g. some polychaetes and enteropneusts) or donot enter the water columnat all (e.g.small bivalvesandgastropods, small polychaetes, oligochaetes). Thelatter specieswith brood protection are particularlycommonin intertidalhabitatscomparedto otherhabi-tats(Clutton-Brook,1991).They maybemost tolerantto moderatechangesin an intertidalenvironmentsincethey protect their offspring during the most sensitiveearlylarval stages.While many planktoniclarvaemaynotbecapable,or are toosubstrate-selective(seeBut-man,1987),to colonizedisturbedareas, benthic larvaethatenjoy parentalprotectionmay bemoreproneandcompetentto colonizemoderately disturbedareas. In-deed,most of thespeciesthat increasedin abundancein Lowes Cove between1979and1996providesomeform of broodprotection (see Table 1). Small crawl-away larvae that do not undergo a planktonic phaseemergefrom oligochaeteegg-cocoons, from maternalburrows (Capitella sp. – see e.g. Rasmussen, 1973;Pearson & Pearson, 1991; Baoling et al., 1991) orfrom maternaltubes(Pygospio elegans– Rasmussen,1973;Streblospio benedicti – Dean,1965;Grassle &Grassle, 1974).Broodprotecting speciesmaybe able

to convert algal detritus immediatelyinto offspringandwould thusbenefit most from moderatealgalcov-erage (for a detailed discussion seealso Grassle&Grassle, 1974). Pearson & Pearson (1991)note thatbroodprotectingCapitella speciesarefavoredin envi-ronmentswith rich local food resources(such asalgaldetritus). Thesuggestion thatbroodprotecting speciesare favored in moderatelyenrichedenvironmentsissupported by the findings of Norkko & Bonsdorff(1996b)who recordedhighabundancesof oligochaeteegg cocoonswithin 10 d after experimentalestablish-ment of algal mats.Theability of crawl-awaylarvaetorecruit immediately into theparental habitat withoutacostly detour throughthewatercolumnmayprimarilybe responsible for the strong abundanceincrease ofthe subsurface-dwelling,deposit-feeding,annelidsinLowes Cove. This ‘neighbourhoodrecruitment’ mayalso be responsible for the highly localized macro-faunachangesobserved in LowesCove. Macrofaunaspecieswith planktonic larvae (e.g. bivalvesMacomabalthica and Mya arenaria, and nereid polychaetes)maynotbeable to benefit from moderatealgal cover-agebecauserecruitsaretoo sensitive to potentialhy-poxiaor successful settlementis adversely affectedbygreenalgalmats (Ólafsson,1988;Bonsdorff, 1992).

Acknowledgements

Our very special thanksgo to Heidi Ryder for her in-exhaustiblepatiencein sorting samplesthat containedmoreoligochaetesthanwe ever wishedfor. Thecom-mentsfrom two anonymousreviewershelpedimprovetheoriginalmanuscripts. Thisstudywassupported bytheUniversity of Maine/Universityof New HampshireSeaGrantOfficein the1970sandby theGulf of MaineFoundation in 1996.Furtherfinancial supportwasre-ceived from the Graduate School and the School ofMarineSciencesboth at theUniversity of Maine.

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