Temporal Development of Biofouling Assemblages

Prepared for the Department of Agriculture, Fisheries and Forestry

June 2010

Authors/Contributors:

Oliver Floerl
Serena Wilkens
Chris Woods

For any information regarding this report please contact:

Graeme Inglis

Programme Leader

Marine Biosecurity

+64-3-3488987

National Institute of Water & Atmospheric Research Ltd
10 Kyle Street
Riccarton
Christchurch 8011
PO Box 8602, Riccarton
Christchurch 8440
New Zealand
Phone +64-3-348 8987
Fax +64-3-348 5548

NIWA Client Report No:CHC2012-103

Report date:June 2010

NIWA Project:NAU10105

Cover image: The Mediterranean fanworm, Sabella spallanzanii, in a biofouling assemblage [Serena Wilkens, NIWA]

Contents

Executive summary......

1Introduction......

2Methods......

2.1Biofouling accumulation on submerged surfaces over time......

2.2Survivalofbiofoulingorganisms......

2.3Ability to identify biofouling organisms during the first 4 weeks following settlement

3Review: Biofouling accumulation on submerged surfaces over time......

3.1Interpretation of literature summaries presented......

3.2Biofoulingaccumulation in temperateenvironments......

3.3Biofouling accumulation in tropical environments......

4Review: Survival of biofouling organisms......

4.1Mortality duringstationary periods......

4.2Mortality induced by vessel voyages......

5Summary and conclusions: Biofouling accumulation on vessel hulls......

5.1Seasonalvariationin biofoulingrisk......

5.2Influence ofphysicalenvironmenton biofouling risk......

5.3Biofoulingaccumulationon vesselsfollowingin-wateror shore-basedcleaning..

6Identification of biofouling organisms during the first 4 weeks following settlement

6.1Abilityto identify biofouling recruitsatages1 – 4weeks......

6.2Notes on the identification of biofouling taxa......

7Acknowledgements......

8References......

Appendix A

Tables

Table 31:Short-term (<4 weeks) examples of settlement and recruitment density (number of colonies or individuals per cm2) of various biofouling taxa to non-taxa surfaces in temperate marine environments on a per-week basis.

Table 41: Mortality rates of marine invertebrate taxa during the first 4 weeks following settlement.

Table 61: The likely ability of (1) a trained field officer (FO) and (2) a recognised taxonomid specialist (TS) toidentifynewlysettledrecruitsofarangeofbiofoulingtaxa between1-4weekspostsettlement..

Figures

Figure 31: Summary of short-term (< 4 weeks) biofouling accumulation to non-toxic surfaces in temperate marine environments on a weekly basis..

Figure 32:Summary of short-term (≤ 4 weeks) biofouling accumulation to non-toxic surfaces in tropical marine environments on a weekly basis.

Reviewed byApproved for release by

Graeme InglisDon Robertson

Temporal development of biofouling assemblages1

Executive summary

A literaturereviewwas conductedtoevaluatethedevelopmentofbiofouling assemblagesonnon-toxic substrates following immersionperiodsof1 –4weeks,in both temperate and tropicalclimates. The Australian DepartmentofAgriculture, FisheriesandForestry (DAFF)requiresthis informationtodeterminewhethervessels undergoing hullcleaning inforeignportsmay becomerecolonisedby localbiota following cleaning ifthey reside intheseportsfora further1–4weeksfollowing cleaningpriorto departingforAustralia.

Ourreviewsuggestedthatbiofouling organismsareable torecruittosusceptible surfaceswithin 1week ofimmersion.Thesesurfacesincludehullareasnotcoatedin antifouling paintaswellasareas coated in ineffectualantifouling paint. However, reports areinconsistentandbiofouling does notalwaysaccumulatewithin 1 week. Especially intemperatelatitudes,theintensity ofrecruitmentby biofouling organisms tends tobeseasonalandmay belimitedduring colderperiodsoftheyear.Incontrast, recruitmentofbiofoulingorganisms in the tropicsisnotas seasonal and occurs throughout theyear.

Depending ongeographicallocationand season,moderate toextensivebiofouling assemblages featuring dozenstohundreds of individuals and coloniesper10 x10 cm maydevelop on cleaned hullsovera3 –4 weektimeframe.

Aproportionoftheseorganismswillmostlikelyperishfrom eithernatural(stochastic mortality,predation,rainfall)oranthropogenicinfluences (pollution)beforeavessel leaves forAustralia.Furthermortality is likely tooccuren route, depending on travel speedand duration.

Trained field officerswillbeunable to identify in thefield themajority of species currently consideredtoposeamedium,highorextremebiosecurity risk toAustralia if specimenshavean ageof1– 4 weeks. Some speciesmaybe identified to familylevel. Taxonomicspecialistswillbeabletoidentifymost3-4weekoldspecimenscollected intemperate environments tofamily orgenuslevel.Becauseof the fastergrowth rates ofmanysessilespeciesintropicallatitudes,identificationtofamilyorgenuslevel maybeachieved 1 weeksoonerifrecruitmentoccurred inthetropics.

Temporal development of biofouling assemblages1

1Introduction

In April 2010, the Australian Department of Agriculture, Fisheries and Forestry (DAFF)contractedNIWA toconductaliterature reviewoftheratesofbiofouling accumulationon submergedsurfaces intemperateandtropicallocations. DAFF requires this information to support the development of policy for managing biofouling threats toAustralia.Ofparticular interesttothe Department is information onthe relationship betweenthe timeavessel spends inaforeignport following hull cleaning (in-waterorshore-based)andthelikelihoodthatitshullwillbecome recolonisedbybiofoulingorganismspriortodepartingfor,orduringcallstoother portsen-routetoAustralia. Depending ontheageofthesebiofouling assemblages, it maynotbeeasyorpossibleto identify them tospecieslevelduring routinehull surveys.

Theaimofthisprojectwastocollectandsummariseinformationonthedevelopment ofbiofoulingassemblagesonsusceptiblevesselhullsovera1-monthperiod,andon thelikelihoodthatcollectedspecimenscould beidentifiedto specieslevel.

Thespecificobjectivesofthisliteraturereview wereto summariseinformation on:

1. Therateofaccumulationofbiofoulingorganismsonsubmergedsurfacesin weekly incrementsover4 weeksforboth tropicaland temperateclimates (worldwide);

2. Thesurvivalofbiofoulingorganismsfrom thepointofsettlementovertime(4 weeks);and

3. The ability to identify biofouling organisms from tropical and temperate climatesatarangeofageclasses (1–4 weeks).

2Methods

2.1Biofouling accumulation on submerged surfaces over time

Biofouling assemblages develop on surfaces submerged throughout the world’s oceans,but thecompositionandintensity ofbiofoulingvarieswidely inspace (e.g. between climate regions, different physical environments, depth, etc.) and time (season, immersion period, etc.) (Dürr2010 and references therein).Weundertook a literaturereview tocollate informationonthetypesofbiofoulingorganismsthatare likely to colonisenon-toxicsurfaceswithin 1month of immersion in temperateand tropicalcoastalwaters,wherepossibleatweeklyintervals.

Wegaveparticularattentiontostudiesconductedwithin,or inthevicinity of,portand harbourenvironments.Forsimplicity,broadclimatezonesofTemperate(between23.5and66.5degreesoflatitude)andTropical(0– 23.5degrees)wereused. Within thesetwo broadcategories are included subtropical(20–40degrees)and subarctic/subantarcticclimatezones (50– 70 degrees).

Usingthelimitedinformationavailable,wealsodiscusshowcolonisationpatterns may differbetweenentirely non-toxicsurfacesand surfacescoated in antifouling paint that has no or limited biocide remaining (“ineffectual” coatings), particularly followingin-watercleaningofvesselhulls.

The reviewwasconducted by accessing peer-reviewedscientificpublications(journal articles,booksandbook chapters),technicalreportsandunpublisheddatasets.We identifiedtheseresources byqueryingliteraturedatabases(e.g.ISIWebofScience; GoogleScholar),directcontactwithrelevantspecialistsandfromourowncollection ofrelevantpublicationsin thisfield.Asoutlinedintheprojectproposalandcontract, theproject’sbudgetand timeline limited theamountof relevant information thatcould bereviewedonbiofouling accumulation.However,wetookcaretoensurethatour review targetedthemost relevant sourcesofinformation.

2.2Survivalofbiofoulingorganisms

Biofoulingorganismsthathavecolonisedthehullofvesselsintendingtotravelfrom aninternationallocationtoAustralia may notarrivein aviable state.Sourcesof mortalityincludenaturalmortality(e.g.predation,competition)andmortalitycaused bythevoyagetoAustralia(e.g.damageincurredfrom hydrodynamicdrag;starvation, etc.).Weconductedaliteraturereview todeterminethelikely ratesofsurvivalof differentbiofoulingtaxatravellingtoanAustralianportfrom overseas. Themethods usedtoidentify relevantsourcesof informationare thesameasthosedescribedin Section 3.1.

2.3Ability to identify biofouling organisms during the first 4 weeks following settlement

Theeasewithwhichbiofouling organismscanbe identifiedtospecies levelisoften highly dependenton their stageofdevelopment.Morphologicalcharacteristicsthat distinguishonespeciesfrom anotherareoftennotpresentinjuvenileorganisms.The reliable identification ofevenhigh-profilemarinepestspeciescanbechallenging if availablespecimensareonlydaysorweeksold.Ouraimwastodeterminewhether, andhoweasily,biofoulingorganismsofanageof1–4 weeks(followingsettlement) canbeidentifiedtospecies level. ThisinformationwillenableDAFF toconsiderthe feasibilityand design offield-based quarantinechecks forbiofoulingtarget species.

Thefollowinginformationwascollatedfor thisreport:

Thelikelysizeandappearanceof1–4weekoldrecruitsofmajorbiofouling taxaintemperateand tropicalenvironments;and

The ability of (i)a field officer with a general understanding of marine biofoulingtaxaandsometrainingintheidentificationoftargetspecies,and (ii)arecognisedtaxonomicexpert,toidentifyarangeofmarinebiofouling taxa(and species)atagesof1–4 weeks followingsettlement.

In consultation withtheDAFF ProjectManager, wedecided thatourassessmentof the easeof identification ofbiofouling speciesatan early stagewouldfocuson a subsetof the listofmarine non-indigenousspecies thatwere identified in a recentDAFFrisk analysisasposing amoderate, highorextremeoverallrisk toAustralia. Because this list did not contain species belonging to all major biofouling taxa (e.g. it lacks bryozoa,hydroids,solitaryascidiansandsabellidpolychaetes)wesupplementedit with examplespecies belonging tothesemissing groups.Someof these speciesare already established inAustraliabutareused inthisreportto illustratetheability to identify themor similarspeciesatdifferentearly ages.Acompletelistofthese species ispresented intheResultssection of thisreport.

Informationontheappearanceandeaseofidentificationofbiofouling taxaand target species was obtained from two sources: (1) from managers of NIWA’s Marine Invasive TaxonomicService(MITS)whoprocessand identify awiderangeofmarine species onadaily basis andmanageandmaintain NIWA’sextensivebiological specimen collections, and (2)from NIWA’s in-house taxonomic experts who are recognised expertsin their field and who providespecialistidentificationservicesfora rangeofbiosecurityand biodiversityprojectson an on-goingbasis.

3Review: Biofouling accumulation on submerged surfaces over time

3.1Interpretation of literature summaries presented

The levelofdetailinwhichcolonisationpatternsarereportedin theliteraturevaries betweenstudies.Forexample, studiesfocusedonparticularspecies or taxamaynot recordthepresenceofothertypesofrecruitsonexperimentalsurfaces(e.g.Hurlbut, 1991). Likewise, studiesspecifically targeted at sessilespeciesdonotoften recordthe presenceofmobileorganismsassociatedwithbiofouling assemblages,andalsodonot employmethodsdesignedtopreventthelossofmobileorganismsduring retrievalof settlementsubstrates(e.g.enclosing thesurfacesbeforetheyareretrieved).Forthese reasons thetaxonomic listsprovided insomestudiesarelikely tobeincomplete.In addition, factors such as substrate material, substrate orientation and deployment depth, and sampling effort (numberofexperimental surfaces)vary widely between studies, yetcan significantly affectbiofouling recruitment,diversity/richnessand community composition(RichmondandSeed1991;Glasby 2001).Theseissues complicateattempts togeneralisebiofouling recruitmentpatterns,and they maynot accuratelyreflectbiofoulingrecruitmentto vessels.

Wehaveattempted to presentoursummariesofbiofouling patternsinaclearand intuitivemannerthatconsiderspotentialconfounding factors.Wehavealsoexcluded microbialfilms(‘biofilms’)inourdescriptionofbiofouling accumulation.Biofilms developonanysurface submergedintheseaandare aprerequisiteofmacro-fouling assemblages(Dobretsovetal.2010).Theycanthusbeassumedtohavebeenpresent on any of the substrates examined by the studies we reviewed - yet they are infrequently included in taxonomicsummaries,which aremostly restricted tomacro- biota.Recruitment isoftendefined heuristically,i.e.according to thepurposesof specificstudiesorexperiments.Forthepurposes ofthisreview,wedefined “recruitment”asthedetectionofanorganism onasurfacebyanobserver.Formost studies, this involved thepresenceofindividualsorcolonies thatcould beobserved with thenakedeye.A largenumberofwell-designed studieshave investigated biofouling accumulation to non-toxicsubstrates over longer timeframes(monthsto years)(e.g.Greeneetal.1983;Glasby2001;LinandShao2002;Daffornetal. 2008; Pierrietal. 2010).Suchstudieswereexcluded fromourreviewas they did notpossess relevant short-term(≤4 weeks)data.

3.2Biofoulingaccumulation in temperateenvironments

Wereviewed19studiesthatexaminedtheaccumulationofbiofouling onnon-toxic surfacesforperiodsofupto4weeksfrom immersionofthesurfaces. Thepresenceof biofouling taxaover time,andthe frequency atwhichbiofouling wasrecordedat differenttimeperiods(1,2,3or4weeks)inthe19studiesaresummarizedinFigure 3-1. Detailson the designoftheindividualstudies (e.g.substratetypeused,author details)arepresentedin Appendix1.

Overaperiodof4weeks,diverseassemblagesofbiofoulingorganismscandevelop onnon-toxicsurfaces intemperatemarine environments.A totalof18 taxonomic groupingsbelonging toninemarinephylawererecordedfrom experimentalsurfaces usedin the19studies.Seventaxonomicgroups(hydroids,encrusting bryozoans, barnacles,calcareous tubeworms,gastropods, spongesandsolitary ascidians), were encountered inatleastone

Temporal development of biofouling assemblages1

100

1 week (n =5)

2 weeks(n =7)

3 weeks(n =2)

4 weeks(n =17)

Temporal development of biofouling assemblages1

Figure 31:Summary of short-term (< 4 weeks) biofouling accumulation to non-toxic surfaces in temperate marine environments on a weekly basis.

Bars represent the percentage of the total number of studies examined in which recruitment of different biofouling taxa had been noted after 1, 2, 3 and 4 weeks. Study-specific details on biofouling accumulation are provided in Appendix 1.

Temporal development of biofouling assemblages1

study afteranimmersionperiodofonly 1week.However, eachof thesetaxawasrecordedin only oneoutof the fivestudies thatmeasured recruitmentafter1week. Additional taxawere reported following 2weeksof immersion(macroalgae, scyphozoans,arborescentbryozoans,polychaetes inhabiting softtubesandcolonialascidians).Therewasalsolittleconsistencyamongthestudies inthecompositionofthe assemblagesafter2weeks(Figure 3-1).However,sometaxa, notably bryozoans,barnaclesand calcareous tubeworms,occurredreasonably consistentlyandwererecordedinupto43%ofstudies.Fewdatawereavailableto evaluate biofoulingaccumulationduringa3-weekimmersion period as onlytwo studiesexaminedthistimeframe,ofwhichonerecordedexclusivelymacroalgae.All 18ofthetaxonomicgroupspresentedinFigure 3-1werereportedfrom surfaces immersed foraperiod of4weeks. Thebiofoulers thatweremostconsistentlyrecorded after 4 weeks were barnacles (94% of studies), bryozoans (82%), calcareous tubeworms (65 %), hydroids (71%), ascidians (53 %), macroalgae (71%) and bivalves(41%).Sponges,anemonesandmobileorganismswereencounteredless frequently (Figure 3-1). Wehavenotpresentedthetaxonomicrecordsovertimeas cumulativepresenceinwhichcaseataxoncouldbeconsideredasbeingabletooccur atany timefrom the shortestimmersionperiod itwasfirstreported.However,we suggestthatthis interpretationmay notbeunreasonable,aswesuspectthat thesparse presenceof taxaonsurfacesimmersedfora3-week period(Figure 3-1) isanartefactof therestricted numberofstudieswe reviewed andthefocusof thesestudies.

Thedensity atwhichbiofouling organismsrecruitedtosubstratesimmersedfor1–4 weeksvaried considerably between studiesand wasnotconsistentlyavailable formost taxa. However, it is evidentthatevenafter shortperiodsofimmersion (1– 2weeks) notoriousbiofouling groupscanattainlargeabundanceonsubmergedsubstrates. For example, after2 weeks, upto 27 encrustingbryozoans,5 arborescentbryozoans, 1,600 barnaclesand220tubewormscouldrecruitper10x10 cmareaofsubstratum(Table 3-1).Afteranimmersionperiodof4weeks,densitiesofbiofoulinggroupsreportedin theliteratureweregenerallyconsiderablyhigherthanafter2 weeks immersion.

3.3Biofouling accumulation in tropical environments

Twelvestudieswere reviewedthatexamined thedevelopmentofbiofouling assemblagesovera4-week period in tropicalenvironments.Biofouling organisms belonging to18taxonomicgroupswerereported.Oneoutofthreestudiesrecorded biofouling organismson experimental surfaces after1-week’simmersion. These comprisedhydroidsandnematodeworms(Figure3-2).After2weeks’immersion,a totalof16 taxawererecorded, someofwhich occurred consistently acrossmost studies: barnacles (100% of studies), amphipods and bivalves (67%), hydroids, tubeworms, ascidians (60%) and bryozoans (33%) (Figure 3-2). As in temperate environments,most taxonomicgroupswereencountered following 4weeksof immersion.Hydroids, bryozoans,barnacles, calcareoustubeworms,amphipods, bivalvesandcolonialandsolitaryascidianswererecordedin45– 89%ofthestudies reviewed.

Thedensity atwhich biofouling organismscanrecruit tosubmergedsubstratesin the tropicsovera short timeframeisconsiderable.Following a2-week immersionperiod, dozensofbryozoans, ascidians, and nematodes, hundredsofhydroids, polychaetesand bivalves,andthousandsofbarnaclesandtube-dwellingamphipods,werereported fromartificialsubstratesusedinthestudieswereviewed(Table 3-2).Forsometaxa, suchas hydroids,bryozoans,nematodes, calcareous tubewormsandsolitary ascidians, thesedensitiesincreased with anincreasein immersionperiod.

Where multiple estimates were available in the literature, they are presented as ranges. Literature sources are provided in table footnote.

Taxon / Week 1 / Week 2 / Week 3 / Week 4
Macroalgae / 9
Hydroids / 1 – 273
Anenomes / 9
Scyophozoans / 150
Bryozones – encrusting / 26 / 270 / 1 – 88
Bryozones – arborescent / 5 / 1-75
Barnacles / 1600 / 5 – 1870
Calcareous tube-forming polychaetes / 12 / 5 – 220 / 2- 5280
Seimentary tube-forming polychaetes / 18
Errant polychaetes / 23
Isopods / 37
Amphipods / 1100
Bivalves / 0.03 – 5910
Gastropods / 1
Sponges / 62
Colonial ascidians / 4 / 1-17

Literature soures: Scheer (1945); Skerman (1958); Skerman (1959); Chalmer (1982; El-Komi (1991); Henrikson and Pawlik (1995); Fairfull and Harriott (1999); Johnston and Keough (2000); Berntsson and Jonsson (2003); Bullard et a. (2004); Darbyson et al. (2009)

Table 32:Short-term (<4 weeks) examples of settlement and recruitment density (number of colonies or individuals per cm2) of various biofouling taxa to non-taxa surfaces in tropical marine environments on a per-week basis.

Where multiple estimates were available in the literature, they are presented as ranges. Literature sources are provided in table footnote.

Taxon / Week 1 / Week 2 / Week 3 / Week 4
Hydroids / 14 – 70 / 80 / 140
Bryozones – encrusting / 0..1 / 1 / 2
Bryozones – arborescent / 3 / 9 / 7 - 800
Nematodes / 2 / 40 / 50 / 140
Calcareous tube-forming polychaetes / 17 -19 / 17 / 29 -300
Seimentary tube-forming polychaetes / 440
Errant polychaetes / 28
Amphipods / 1 -1250 / 5 – 23 / 1 – 300
Bivalves / 0.2 – 1.5 / 0.3 / 0.3 – 4
Sponges / 0.1
Colonial ascidians / 0.3 =- 30 / 1 / 1
Solitary ascidians / 0.1 / 14 / 17

Literature sources: Lee and Trott (1973); Floerl (2002); Johnston et al. (2002); da Fonsêca-Genevois et al. (2006); Satheesh and Wesley(2008a, b)

Temporal development of biofouling assemblages1

100

901 week (n=3)

802 weeks(n =6)

3 weeks(n =3)

704 weeks(n =9)

Figure 32:Summary of short-term (≤4weeks)biofoulingaccumulationtonon-toxicsurfacesintropicalmarineenvironmentsonaweeklybasis.

Temporal development of biofouling assemblages1

4Review: Survival of biofouling organisms

Not all ofthebiofouling organismsthatsettleon asubmergedsurfacewillsurviveto becomereproductively activeadults.A rangeofnaturalandanthropogenic factors causemortality of juvenile andadultmarinebenthic biota.Inthecontextofvessel biofouling, sources of mortality can be separated into two categories. The first category includes thoseacting uponbiofouling assemblageswhen they are stationary (e.g.whenavesselismooredinaportoratanchorin shallowwaters).Here,mortality canbecaused by naturalfactors, such as senescence, predation, competition,disease, variation in water temperature, salinity or oxygen levels, or by anthropogenic influences (e.g. environmental pollutants) (Day and Osman 1981; Hurlbut 1991; OsmanandWhitlatch1995;GosselinandQian1997;HuntandScheibling1997;Holloway andConnell2002;Johnstonetal.2003;Boyleetal.2007). Thesecond category of mortality acts upon biofouling organisms when a vessel is moving betweendestinations.Here,damageormortalitycanbecausedbyhydrodynamic forces(drag),starvation(e.g.inability tofilter-feed)orexposuretounsuitable environmentalconditions(e.g.transportofcold-water speciestotropical latitudes,or passage through low-salinity or freshwater environments) (Minchin and Gollasch2003;Couttsetal. 2009).

4.1Mortality duringstationary periods

GosselinandQian(1997)andHuntandScheibling (1997)reviewednaturalmortality andsurvivalofmarineinvertebratespecies thatincludedbivalves,gastropods, barnacles,ascidians,andbryozoans.Bothstudies foundmortality ishighestin the first few monthsfollowingsettlementsuchthat,bytheage of4 months,cohorts are generally reduced to< 20%of theirinitialnumbers. Theresultsofboth studies(and others) pertaining to mortality during the first month following settlement are presented in Table 4-1. Natural mortality rates of marine invertebrates are highly variable(asevidencedby thewideranges)andsuggestthatasignificantproportionof recruitsareremovedfromacohortonaweeklybasis.Forexample,upto78%of juvenilebarnaclesand43to 90%ofsolitaryandcolonialascidians,respectively, may perishduring thefirstweek following settlement.Ofthespeciesexaminedby thesetwo studies,bryozoansandbivalvesgenerally displayedthesmallest ratesof mortality.Itisnotknownwhethertheseratesofnaturalmortality (mostly observedin benthicenvironments)directly apply tobiofouling assemblagesonvesselhulls,which mightbelessaccessible tomobilebenthicpredators than regularbenthicsubstrates.

Survivalofbiofouling assemblagesinportandharbourenvironmentscanalsobe affectedby suddendisturbances such aschemicaloroilspills,orsudden changesin salinity.Forexample, apeakmonsoonal rainfall in2001inCairns,Australia,lowered salinitiesinthe region’slargestmarinato aslowas11psu,resulting inthesudden mortalityof95%ofallbiofoulingassemblageswithinthemarina(Floerl2002;also see Rajagopal et al. 1997). Experimental exposure of biofouling assemblages to higher-than-normalconcentrationsofcopperhavebeenshown to resultin significant levels of mortality in particular biofouling taxa and changes in community composition(Johnstonand Keough2000;Johnstonetal.2002; Johnstonetal.2003). Biofouling assemblageson vesselhullsresiding inportorothercoastalenvironments maybe subjectto similartypesofdisturbance,resultingin elevated mortalityrates.

Table 41:Mortality rates of marine invertebrate taxa during the first 4 weeks following settlement.

Estimates were derived via the weekly standardised survival rates calculated by Hunt and Scheibling (1997) and from estimates of cumulative morality presented in Gosselin and Qian (1997). other data were obtained from Stoner (1990), Hurlbut (1991) and Petersen and Svane (1995).

Time / Taxon / Cumulative mortality
Week 1 / Barnacles / 0 – 78%
Bryozoa / 1 – 6%
Bivalves / 15 – 20%
Gastropods / 23%
Colonial ascidians / 0 – 90%
Solitary ascidians / 13 – 43%
Week 2 / Barnacles / 0 – 75%
Bryozoa / 2 – 12%
Bivalves / 28 – 36%
Gastropods / 41%
Colonial ascidians / 0 -100%
Solitary ascidians / 24 – 68%
Week 3 / Barnacles / 0 – 88%
Bryozoa / 3 – 17%
Bivalves / 39 – 49%
Gastropods / 54%
Colonial ascidians / 0 – 100%
Solitary ascidians / 34 – 81%
Week 4 / Barnacles / 0 – 94%
Bryozoa / 4 – 22%
Bivalves / 48 – 59%
Gastropods / 24 – 99%
Colonial ascidians / 22 – 99%
Solitary ascidians / 43 – 89%

4.2Mortality induced by vessel voyages

During vesselvoyages,biofouling organismsare exposedtohydrodynamicdrag that canhaveasignificanteffecton survivalviadislodgementor inhibitionoffeeding. Typically,fast-movingvessels (> 15knots)inregularusehave relatively lowlevelsof biofoulingthataremostlyconfinedtonicheareasprotectedfromvoyage-induced drag.Slow-moving (5knots)vessels,suchasbargesandmany sailing yachts,are morelikely tosupportbiofouling assemblagesthataremorewidespreadacross the submergedhullarea(Fosterand Willan1979; JamesandHayden2000;Couttsand Taylor2004;Davidsonet al.2008;Inglisetal.2010).Couttsetal. (2009)tested the effectofvesselspeedonbiofouling assemblagesup to 7daysfollowing voyagesof20 minutesduration. They foundthat: (1)vesselspeedsof5and10knotshad littleeffect onbiofouling species richness, but speciesrichnessdecreasedby 50%following voyagesof18knots,(2)percentagebiofouling coverdecreasedwith increasing speed, withdecreasesmostpronouncedat10and18knots(percentcoverreducedby24% and85%,respectively),and(3)survivalwasgreatestforbiofoulingorganismswith colonial,encrusting,hardand/or flexiblemorphologicalcharacteristics,and thiseffect increasedwith speed.For example,solitaryascidiansand sabellidwormshadlower rates of survival than encrusting bryozoans, hydroids and arborescent bryozoans. MeanreductioninpercentagecoverofthesolitaryascidianCorellaeumyotawas 100% at 18 knots, compared to 18% for the colonial ascidian Botryllus leachi. However,whilsthighervesselspeedsmay reduceoverallbiofouling biomass and removesomeorganism types,theydonoteliminatebiofouling translocation risk, especiallynotforprotectednicheareasthatarenotexposedto drag.

A further sourceofmortality associatedwithvesselvoyagesisthepassagethroughor into environments that are not within the physiological tolerance range of the biofouling organisms(Visscher1928; MoranandGrant1991).Forexample,transition into environments withdifferentorhighercontaminantlevelscanaffect survivalof biofouling organisms.Turneretal. (1997)reported substantialmortality and achange inassemblagecomposition whenexisting biofouling assemblageswere translocatedto differentmarinaenvironmentsalong putativegradientsofcontaminantand sedimentation levels. Similar resultsare reportedby Moran andGrant(1991)and Mayer-Pintoand Junqueira(2003).Passagesofvessels from marinetobrackishor freshwaterenvironmentsorfrom tropicaltotemperateseawatertemperatures(and vice-versa) typically resultinconsiderablebiofoulingmortality (Visscher1928; Davidsonetal.2006).Whilefastervesselspeedsmaysignificantly affectthesurvival andgrowthofsomebiofouling organisms,there isalso aconverserisk thatfaster passagethroughunfavourableenvironmentsmay reducemortality ofsomebiofouling organismsasthey spendlesstimeinconditionsthataredetrimentalto them (Minchin and Gollasch 2003).

5Summary and conclusions: Biofouling accumulation on vessel hulls

Ourreviewofbiofouling accumulationintemperateandtropicalenvironments indicates thatbiofouling organismscanrecruitto susceptiblesubstrates following an immersionperiodofasingleweek.Whilenoneof the studieswereviewedexamined recruitmenttovesselhullsspecifically,weexpectthatsuchshort-termaccumulation ofbiofouling ispossibleonhullsurfaceslacking functionalantifouling paint. These willmostcertainly includenicheareasdevoid ofantifouling paint, such aspropeller shafts,ruddershafts,bowthrustersandsimilarstructures.Darbysonetal.(2009) foundthatcolonizationofuntreatedvesselhullmaterialsbythesolitaryascidian Styelaclavawasgreateronbarealuminium substratesthanonanyothersubstrate examined,illustrating the susceptibility ofcommon,unprotectedhullmaterialsto marinebiofouling.Biofouling accumulationisalso likely inlocationswherethe antifouling paintiseithertoooldorhasbeenwornoffby drag orabrasive/mechanical damage(Davidsonetal.2006;ASA2007;PiolaandJohnston2008).However,itis importantto emphasise that, inthestudieswe reviewed,recruitmentdidnotoccur consistentlyoververy short(1-week)timeframes–atleastnottoorganism sizesthat weredetectedby the samplingmethodsused in thevarious studies.Biofouling accumulation became more consistentand, generally, attained higherdensities, followingimmersion periodsexceeding1 week.

5.1Seasonalvariationin biofoulingrisk

Thebiofouling risk ofvesselsundergoing short residency periodsislikely to vary geographically and seasonally,particularly in higherlatitudes,where reproduction and settlementofbiofoulingorganismsishighlyseasonal(Coe1932;Skerman1958,1959;RichmondandSeed1991;WatsonandBarnes2004;Holm etal.2008).In contrast,biofouling risk is likely tobe moreconsistent inmany tropicalenvironments, where recruitmentofsessilespeciesoccursmoreorlessthroughout theyear,withthe exceptionofperiodsofextrememonsoonalevents(RichmondandSeed1991;Floerl2002; Swami and Udhayakumar 2010). Tropical marine environments may also possess greater biofouling diversity, and faster growth rates resulting in earlier maturityofbiofoulingspecies(Paul1942;RichmondandSeed1991;Holmetal.2008).Forexample,Rajagopaletal.(1997)foundamaximum biofoulingbiomass accumulation of64kgm-2within30 daysata locationinIndia, and Paul(1942),also workinginIndia,observedsexualmaturityintheserpulidHydroidesnorvegicaand thebarnacleBalanus amphiriteat9and16daysafter recruitment,respectively. Biofouling assemblages thatcolonized and developedon hull surfaces in tropical environmentsmaythuspose a particularly highrisk to potential recipient environments,insofarasthesedisplaysimilarenvironmentalcharacteristics.

5.2Influence ofphysicalenvironmenton biofouling risk

Ratesofrecruitmentofbiofouling organismsarelikely tobehighestin port environments,wherethereareextensiveresidentpopulationsofbiofoulingspecies and where protective breakwalls often restrictexchange ofwaterwith surrounding coastalareas (FloerlandInglis2003;Daffornetal. 2008).Somestudieshavealso recordedgreaterratesofrecruitmentinpollutedportenvironmentscompared toless pollutednaturallocations(e.g.Kocaketal.1999),althoughexperimentsmayhave beenconfoundedby the absence ofsampling inunpollutedportenvironments. Many shipping environments possess a characteristic suite of biofouling organisms that recruitwithvarying intensitydependingonthetimeofyear(Holm etal.2008). Generally,asvesselsresidefor increasing periods in portandmarinaenvironments, they accumulateagreaterproportionoftheresidentbiofouling assemblageontheir submerged hullsurfaces(Floerland Inglis2005).

5.3Biofoulingaccumulationon vesselsfollowingin-wateror shore-basedcleaning

There is someuncertainty regarding theperformance ofantifouling paints following manualremovalofbiofouling.Representativesof theantifouling paint industry frequently suggestthathullcleaning (e.g.using mechanicalbrushes) removes biofouling andtheupper, hydrolysedlayersofantifouling coatingsand‘restores’the effectivenessofantifouling paints. Thiswasnotconfirmedinexperimentsundertaken byFloerletal.(2005) intropicalAustralia,wheresurfacescoatedinthree contemporaryantifoulingpaintswereimmersedinstaticconditionsfor7monthsuntil extensivebiofoulingassemblageshaddeveloped.Thesewerethenremovedusinga stiffbrush.Recolonisation ofcleanedsurfacesoccurred rapidly:after2weeks,an averageof3,000recruitswerepresenton manuallycleaned surfaces (17 x 17 cm). The recruits included barnacles, bivalves, ascidians, bryozoans, hydroids, amphipods, tubewormsandsponges (Floerletal.2005). Lowerbiofouling rates on cleaned and sterilizedsurfacessuggestedthattheelevatedrecruitmentoccurredinresponseto tracesoforganicmaterial remaining onsurfacesthathadbeensubjectedto brush cleaning.A relevant real-world exampleisprovidedby afloating dry-dock towedto PearlHarbor,Hawaii,by theU.S.Navy approximately 20yearsago.Thedock had beencleanedby diversinSubicBay,Philippines,but remainedmooredinSubic Bay forapproximately 3-4weekspriortobeing towedtoHawaii. Translocationofthe floating dock to Hawaiiwasfollowed by the localizedappearanceandsubsequent expansion of twonon-indigenous species(onesponge andone oyster) thatare thought tohaveoriginated from thePhilippines.Itisprobable thatthese speciesmayhave originatedfromthe floatingdock(M. Hadfield,pers. comm. 2010).