13
1724 Ecological Applications, 14(6), 2004, pp. 1724–1736 q 2004 by the Ecological Society of America POSITIVE INTERACTIONS BETWEEN NONINDIGENOUS SPECIES FACILITATE TRANSPORT BY HUMAN VECTORS OLIVER FLOERL, 1,3 THOMAS K. POOL, 1,4 AND GRAEME J. INGLIS 2 1 School of Tropical Environment Studies and Geography, James Cook University, Townsville, Queensland 4811, Australia 2 National Center of Aquatic Biodiversity and Biosecurity, National Institute of Water and Atmospheric Research, P.O. Box 8602, Christchurch, New Zealand Abstract. Numerous studies have shown how interactions between nonindigenous spe- cies (NIS) can accelerate the rate at which they establish and spread in invaded habitats, leading to an ‘‘invasional meltdown.’’ We investigated facilitation at an earlier stage in the invasion process: during entrainment of propagules in a transport pathway. The introduced bryozoan Watersipora subtorquata is tolerant of several antifouling biocides and a common component of hull-fouling assemblages, a major transport pathway for aquatic NIS. We predicted that colonies of W. subtorquata act as nontoxic refugia for other, less tolerant species to settle on. We compared rates of recruitment of W. subtorquata and other fouling organisms to surfaces coated with three antifouling paints and a nontoxic primer in coastal marinas in Queensland, Australia. Diversity and abundance of fouling taxa were compared between bryozoan colonies and adjacent toxic or nontoxic paint surfaces. After 16 weeks immersion, W. subtorquata covered up to 64% of the tile surfaces coated in antifouling paint. Twenty-two taxa occurred exclusively on W. subtorquata and were not found on toxic surfaces. Other fouling taxa present on toxic surfaces were up to 248 times more abundant on W. subtorquata. Because biocides leach from the paint surface, we expected a positive relationship between the size of W. subtorquata colonies and the abundance and diversity of epibionts. To test this, we compared recruitment of fouling organisms to mimic W. subtorquata colonies of three different sizes that had the same total surface area. Sec- ondary recruitment to mimic colonies was greater when the surrounding paint surface contained biocides. Contrary to our predictions, epibionts were most abundant on small mimic colonies with a large total perimeter. This pattern was observed in encrusting and erect bryozoans, tubiculous amphipods, and serpulid and sabellid polychaetes, but only in the presence of toxic paint. Our results show that W. subtorquata acts as a foundation species for fouling assemblages on ship hulls and facilitates the transport of other species at greater abundance and frequency than would otherwise be possible. Invasion success may be increased by positive interactions between NIS that enhance the delivery of prop- agules by human transport vectors. Key words: antifouling paints; bryozoans; epibiosis; facilitation; hull fouling; nonindigenous species; perimeter; positive interactions; toxicity; Watersipora subtorquata. INTRODUCTION Positive or facilitative interactions between species are important structuring agents in ecological systems (Turner 1983, Jensen and Morse 1984, Thrush et al. 1992). Although mutualistic and commensal relation- ships are commonly the result of a coevolutionary his- tory (Stachowicz 2001, Bruno and Bertness 2003), pos- itive interactions can also occur between species that have coexisted for only short periods of time. For ex- ample, a surprisingly large number of nonindigenous Manuscript received 1 December 2003; revised 24 February 2004; accepted 15 March 2004. Corresponding Editor: P. K. Dayton. 3 Present address: National Center of Aquatic Biodiversity and Biosecurity, National Institute of Water and Atmospheric Research, P.O. Box 8602, Christchurch, New Zealand. E-mail: [email protected] 4 Present address: School of Aquatic and Fishery Sciences, University of Washington, 1122 NE Boat Street, Seattle, Washington 98195 USA. species (NIS) benefit from facilitative interactions with other introduced or native species (Simberloff and von Holle 1999, Richardson et al. 2000, Ricciardi 2001). Simberloff and von Holle (1999) coined the term ‘‘in- vasional meltdown’’ to describe the positive interac- tions between NIS that facilitate one another’s survival and accelerate the rate of successful invasion. These can take many forms. For example, introduced animals, such as insects, birds, rats, and mammalian herbivores act as pollinators or dispersal agents for exotic plants (Loope and Snowcroft 1985, Barthell et al. 2001). NIS can also have habitat-modifying effects by altering the physical or biological environment in their invaded range, making it more suitable for some species (fa- cilitation), and less so for others (inhibition) (Stachow- icz 2001, Bruno et al. 2003). For example, filtering by zebra mussels (Dreissena polymorpha) has improved water clarity in light-limited lakes, thereby accelerating the spread of a number of introduced macrophytes

POSITIVE INTERACTIONS BETWEEN NONINDIGENOUS SPECIES FACILITATE TRANSPORT BY HUMAN VECTORS

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Page 1: POSITIVE INTERACTIONS BETWEEN NONINDIGENOUS SPECIES FACILITATE TRANSPORT BY HUMAN VECTORS

1724

Ecological Applications, 14(6), 2004, pp. 1724–1736q 2004 by the Ecological Society of America

POSITIVE INTERACTIONS BETWEEN NONINDIGENOUS SPECIESFACILITATE TRANSPORT BY HUMAN VECTORS

OLIVER FLOERL,1,3 THOMAS K. POOL,1,4 AND GRAEME J. INGLIS2

1School of Tropical Environment Studies and Geography, James Cook University, Townsville, Queensland 4811, Australia2National Center of Aquatic Biodiversity and Biosecurity, National Institute of Water and Atmospheric Research,

P.O. Box 8602, Christchurch, New Zealand

Abstract. Numerous studies have shown how interactions between nonindigenous spe-cies (NIS) can accelerate the rate at which they establish and spread in invaded habitats,leading to an ‘‘invasional meltdown.’’ We investigated facilitation at an earlier stage in theinvasion process: during entrainment of propagules in a transport pathway. The introducedbryozoan Watersipora subtorquata is tolerant of several antifouling biocides and a commoncomponent of hull-fouling assemblages, a major transport pathway for aquatic NIS. Wepredicted that colonies of W. subtorquata act as nontoxic refugia for other, less tolerantspecies to settle on. We compared rates of recruitment of W. subtorquata and other foulingorganisms to surfaces coated with three antifouling paints and a nontoxic primer in coastalmarinas in Queensland, Australia. Diversity and abundance of fouling taxa were comparedbetween bryozoan colonies and adjacent toxic or nontoxic paint surfaces. After 16 weeksimmersion, W. subtorquata covered up to 64% of the tile surfaces coated in antifoulingpaint. Twenty-two taxa occurred exclusively on W. subtorquata and were not found ontoxic surfaces. Other fouling taxa present on toxic surfaces were up to 248 times moreabundant on W. subtorquata. Because biocides leach from the paint surface, we expecteda positive relationship between the size of W. subtorquata colonies and the abundance anddiversity of epibionts. To test this, we compared recruitment of fouling organisms to mimicW. subtorquata colonies of three different sizes that had the same total surface area. Sec-ondary recruitment to mimic colonies was greater when the surrounding paint surfacecontained biocides. Contrary to our predictions, epibionts were most abundant on smallmimic colonies with a large total perimeter. This pattern was observed in encrusting anderect bryozoans, tubiculous amphipods, and serpulid and sabellid polychaetes, but only inthe presence of toxic paint. Our results show that W. subtorquata acts as a foundationspecies for fouling assemblages on ship hulls and facilitates the transport of other speciesat greater abundance and frequency than would otherwise be possible. Invasion successmay be increased by positive interactions between NIS that enhance the delivery of prop-agules by human transport vectors.

Key words: antifouling paints; bryozoans; epibiosis; facilitation; hull fouling; nonindigenousspecies; perimeter; positive interactions; toxicity; Watersipora subtorquata.

INTRODUCTION

Positive or facilitative interactions between speciesare important structuring agents in ecological systems(Turner 1983, Jensen and Morse 1984, Thrush et al.1992). Although mutualistic and commensal relation-ships are commonly the result of a coevolutionary his-tory (Stachowicz 2001, Bruno and Bertness 2003), pos-itive interactions can also occur between species thathave coexisted for only short periods of time. For ex-ample, a surprisingly large number of nonindigenous

Manuscript received 1 December 2003; revised 24 February2004; accepted 15 March 2004. Corresponding Editor: P. K.Dayton.

3 Present address: National Center of Aquatic Biodiversityand Biosecurity, National Institute of Water and AtmosphericResearch, P.O. Box 8602, Christchurch, New Zealand.E-mail: [email protected]

4 Present address: School of Aquatic and Fishery Sciences,University of Washington, 1122 NE Boat Street, Seattle,Washington 98195 USA.

species (NIS) benefit from facilitative interactions withother introduced or native species (Simberloff and vonHolle 1999, Richardson et al. 2000, Ricciardi 2001).Simberloff and von Holle (1999) coined the term ‘‘in-vasional meltdown’’ to describe the positive interac-tions between NIS that facilitate one another’s survivaland accelerate the rate of successful invasion. Thesecan take many forms. For example, introduced animals,such as insects, birds, rats, and mammalian herbivoresact as pollinators or dispersal agents for exotic plants(Loope and Snowcroft 1985, Barthell et al. 2001). NIScan also have habitat-modifying effects by altering thephysical or biological environment in their invadedrange, making it more suitable for some species (fa-cilitation), and less so for others (inhibition) (Stachow-icz 2001, Bruno et al. 2003). For example, filtering byzebra mussels (Dreissena polymorpha) has improvedwater clarity in light-limited lakes, thereby acceleratingthe spread of a number of introduced macrophytes

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December 2004 1725FACILITATION OF NONINDIGENOUS SPECIES

(MacIsaac et al. 1992, MacIsaac 1996). Seventy-threepercent of the 254 studies examined by Simberloff andvon Holle (1999), and 89% of the 101 studies examinedby Ricciardi (2001), describe interactions betweenpairs of NIS from which either one (commensalism orexploitation) or both (mutualism) of the species benefit.

Human-mediated biotic invasions are a process thatconsists of several successive stages: (1) engagementof propagules with a transport vector in a source lo-cation, (2) transport from source to recipient location,(3) establishment of a self-sustaining population, and(4) spread through the new habitat (Mack et al. 2000,Sakai et al. 2001). A large number of studies of inter-actions between invaders have attempted to identifyfactors that facilitate or impede the spread of NIS oncethey have established beachhead populations (Richard-son et al. 2000, Barthell et al. 2001, Lohrer and Whit-latch 2002, Morales and Aizen 2002). In this study, weinvestigated facilitation at an earlier stage in the in-vasion process: during entrainment in a human trans-port pathway (e.g., Sakai et al. 2001). The rate of de-livery of NIS (‘‘propagule pressure’’) to novel envi-ronments is an important correlate of establishmentsuccess (Kolar and Lodge 2001). Processes that in-crease the frequency at which species are transportedand introduced by humans, therefore, are likely to in-crease the overall probability that they will establishoutside their natural range. Understanding these pro-cesses is a research priority in invasion biology to re-duce the risk of accidental introductions of NIS viaactivities such as the movement of cargo containers,ballast water-release, and hull fouling (Williamson1999, Wonham et al. 2000). Here, we examined howan encrusting bryozoan, Watersipora subtorquata, fa-cilitates the development of hull-fouling assemblages,a major transport pathway for aquatic NIS (Minchinand Gollasch 2003).

Hull fouling is a nuisance to owners and operatorsof commercial and private craft as it reduces speed andmaneuverability of the vessels (Christie and Dalley1987). Toxic ‘‘antifouling’’ paints are commonly usedto prevent the development of fouling assemblages onthe underside of ocean-going vessels and other sub-merged structures. The paints typically incorporate bio-cides based on copper, zinc, or tin compounds that deteror kill the larvae and spores of aquatic organisms(Comber et al. 2002, Thomas et al. 2002). Over thepast few decades, paints have been developed that aresuccessful in preventing hull fouling for periods of upto five years (Christie and Dalley 1987, Hunter andAnderson 2001, available online).5 Some species, no-tably the bryozoan genus Watersipora and the ma-croalgae Enteromorpha and Ectocarpus, however, ex-hibit a physiological tolerance to popular antifoulingbiocides including copper (Wisely 1962, Callow 1986,AMOG Consulting 2002, Ng and Keough 2003). Wa-

5 ^http://www.international-marine.com/&

tersipora subtorquata (d’Orbigny) and W. arcuataBanta are common fouling organisms in shipping portsaround Australia, New Zealand, and California (USA),and appear to have been introduced to many of theselocations by trans-oceanic movements of vessels (Allen1953, Banta 1969, Gordon and Matawari 1992, Hewittet al. 1999).

We tested the hypothesis that the sheet-like coloniesof W. subtorquata provide a nontoxic refuge on vesselhulls for the settlement and transport of epibiotic foul-ing taxa that would otherwise not be present on thesesurfaces. Like many other marine sessile taxa, the bry-ozoa possess a variety of chemical or mechanical de-fense mechanisms to prevent epibiotic growth (Dyryn-da 1983, 1986, Davis et al. 1989), but our observationsof W. subtorquata colonies on boat hulls suggest thatthese can be overcome by a range of organisms (Floerl2002). Because many vessels travel extensively, anyepibionts on W. subtorquata may be dispersed far fromparent populations, possibly to locations outside theirnative or existing range (Carlton 1987, 1992). Anti-foulant biocides act by leaching from the paint surface,deterring the larvae of some marine species from set-tlement and killing other taxa prior to, or followingsettlement (Crisp and Austin 1960, Wisely 1963a,1964). Because antifoulant biocides diffuse within sea-water, we expected greater abundance and diversity ofsecondary colonists on large W. subtorquata coloniesthat had a relatively small perimeter : area ratio andwhere the diffusion of biocides would be minimized.By manipulating the size and number of mimic W. sub-torquata colonies, we tested the effect of refuge sizeon the abundance and composition of fouling assem-blages on vessel hulls. This question is of particularimportance for the transport of NIS, as both the sizeof individual inocula and the frequency of transpor-tation are key components of propagule pressure foraccidental introductions of marine species (Carlton1996, Ruiz et al. 2000, Forsyth and Duncan 2001).

METHODS

Study sites

Experiments were carried out in small boat marinasin the cities of Townsville and Cairns, located on theeast coast of Queensland, Australia (Fig. 1). Both ma-rinas were partially enclosed by breakwalls and pro-vided berths for .200 recreational vessels of up to 30m length. At the time of the study, the marinas had hadbeen in operation for at least seven years. Water tem-perature during the study ranged from 268C to 298C.For more detail on the study sites refer to Floerl andInglis (2003).

Effects of antifouling-paint type on colonization byWaterpipora subtorquata and facilitation

of other fouling taxa

Three broad types of antifouling paint are availablefor use on small vessels such as private sailing and

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1726 OLIVER FLOERL ET AL. Ecological ApplicationsVol. 14, No. 6

FIG. 1. The study sites on the Great Barrier Reef coastline,eastern Australia.

TABLE 1. Antifouling paint types used in this study.

Paint type Specifications Application

1 high strength, self-polishing, cuprous oxide based,soft paint, high toxin release rate

cruising vessels in regular use

2 medium strength, ablative, no cuprous oxide, softpaint, high toxin release rate

cruising vessels in irregular use

3 medium strength, non-ablative hard paint, no cuprousoxide, low toxin release rate

fast-moving vessels in very frequent use

motor yachts. Each type is designed for boats withdifferent patterns of activity (Table 1). We assessed thesusceptibility of an example of each type of antifoulingpaint to colonization by W. subtorquata within marinaenvironments, where private vessels typically spendextended periods at anchor. Because most (;62%) rec-reational vessels that reside in Queensland marinashave fiberglass hulls (Floerl 2002), we compared ratesof recruitment of fouling organisms to tiles made of 2-mm thick fiberglass sheets (17 3 17 cm). The sheetshad a smooth gel coat finish on the upper surface, andwere thus identical to the outer surface of boat hulls.Paints were applied to the tiles according to manufac-turer’s specifications. Each tile was painted with twocoats of protective primer, and then variously paintedwith two coats of the antifouling coatings (treatments)or not further manipulated (controls). The tiles werethen left for five days before being deployed.

Between 17 and 20 July 2000, 12 tiles from each ofthe four treatments were mounted horizontally (facedown) on each of four polyvinyl chloride (PVC) frames(4.8 3 0.8 m). Two frames were suspended in eachmarina in randomly chosen sites at a depth of 80 cmbelow the water surface. Four randomly selected tilesfrom each treatment were recovered from each frameafter 4, 8, and 16 weeks of incubation within the ma-rinas. These periods were chosen to represent typical

residency periods for visiting vessels in Queenslandmarinas (Floerl 2002).

Sample analyses

Once recovered, the tiles were placed in racks withinlarge plastic tubs that were designed to prevent abra-sion of the fouled surfaces. The tubs were filled witha 5% formaldehyde–seawater solution and transportedto the laboratory, where the percent cover of organisms(both primary and secondary cover) that had recruitedto the tiles was recorded by superimposing 64 randomdots onto each tile. Direct counts were also made ofindividuals and colonies. Tiles with particularly largenumbers of small or very abundant organisms (e.g.,serpulid and spirorbid polychaetes, barnacles, and hy-droids ,5 mm in dimension) were subsampled usingsix randomly placed 5.2-cm2 quadrats. Estimated den-sities in the quadrats were converted to total numbersper tile prior to analysis. Absolute counts were madefor larger and less numerous individuals and colonies.Organisms were identified to the lowest possible tax-onomic level, which ranged from species to families.Organisms that could not be specifically identified weregrouped according to morphotype and coded appro-priately (e.g., Hydroid D).

Differences in the diversity and density of foulingorganisms on W. subtorquata colonies and bare tilespace (‘‘Substratum’’) were tested for using ANOVA.The linear model consisted of a mixed design with threefixed orthogonal factors (marina, a 5 2; paint treat-ment, b 5 4; and substratum, c 5 2) and one nestedrandom factor (site, d 5 2).

Influence of colony size on epibiosison Watersipora subtorquata

Hypotheses regarding epibiotic growth on W. sub-torquata were tested using mimic bryozoan coloniesconstructed from a 1:1 ratio mix of marine filler putty(International Epiglass Epifill all purpose epoxy filler,International Coatings, Felling, UK) and a glass fiberfiller (Fibre Tough filler, Septone Products, Hemmant,Australia). Mimics have been used for a range of othermarine sessile organisms (e.g., barnacles, ascidians,and tubiculous polychaetes) in previous studies andwere found adequate surrogates for their biologicalcounterparts (Eckman 1985, Edgar 1991, Walters andWethey 1996, Wright and Boxshall 1999, Holloway andKeough 2002).

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December 2004 1727FACILITATION OF NONINDIGENOUS SPECIES

TABLE 2. The treatments used in this experiment.

Treatment Total perimeter (cm)

1) Primer2) Primer 1 1 large colony3) Primer 1 2 medium colonies4) Primer 1 18 small colonies

09.33

13.1939.58

5) Primer 1 antifouling paint6) Primer 1 antifouling paint 1 1 large colony7) Primer 1 antifouling paint 1 2 medium colonies8) Primer 1 antifouling paint 1 18 small colonies

09.33

13.1939.58

Note: On all tiles an equal area (6.92 cm2) of Watersipora subtorquata mimics or tile surface(controls) was sampled.

Approximately 3–4 mL of a nontoxic generic amberpaint were added to each 200-g batch of putty mixtureto give the mixture the amber color observed in naturalcolonies of W. subtorquata. Pilot experiments had in-dicated that this composition did not degenerate whenimmersed in the sea and attracted a range of epibioticrecruits similar to that on natural colonies (Pool 2002).All mimic colonies were made circular in shape be-cause most natural recruits in the earlier experimentwere approximately circular.

Eighty fiberglass tiles were coated with marine prim-er (n 5 40) or marine primer and a commercial anti-fouling paint (n 5 40; paint type 1, see Table 1) in themanner described for the previous experiment. Thesetiles were then separated into eight treatment groups(n 5 10 per treatment) that variously contained toxicantifouling paint and 18 small, two medium, or onelarge mimic W. subtorquata colonies (Table 2). Thethree sizes reflected the numerically most abundant nat-ural colonies observed in the earlier experiment: small(7 mm diameter), medium (21 mm diameter), and large(29.7 mm diameter). All colonies had an approximateheight of 1.5 mm.

Mimic colonies were fixed in random locations tothe tiles before the putty–paint mixture had hardened,and no glue was required for permanent fixation. In alltreatments, mimic colonies covered a total area of 6.92cm2 (3.08% of the total tile area), but the total perim-eter : area ratio of the colonies differed between treat-ments and was 5.72, 1.91, and 1.34 for small, medium,and large colony sizes (Table 2).

Five replicate tiles of each treatment were attachedin randomly selected positions to each of two PVCframes (20 mm diameter piping, 4.8 3 0.8 3 0.3 moverall dimension). Distances between individual tileswere at least 17 cm. In June 2001, the frames weresuspended at 1 m depth from two randomly chosenpontoons (separated by a distance of ;100 m) withinthe Townsville marina (Fig. 1). Five replicate tiles ofeach treatment group were recovered from each frameafter an immersion period of six weeks. Retrieval andtransport of the tiles was done as described for Ex-periment 1.

Sample analyses

On tiles containing mimic W. subtorquata colonies,the number and identity of recruits that had settleddirectly on top of each colony were recorded. On tileswithout mimic patches (N 5 20; this included tilescoated in toxic antifouling paint or nontoxic primer),a total area of 6.92 cm2 of the tile surface was sampled.This was done by sampling randomly located patcheson each tile that were identical in size to the mimiccolonies of other treatments. On each control tile, thesize of successively sampled patches was randomly de-termined; that is, in some cases on a single tile bothsmall- and medium-sized patches were sampled. Or-ganisms were identified using the same methods asdescribed for the earlier experiment.

ANOVA was used to test for differences in the totalnumber of recruits and taxa, and in the numerical abun-dance of broad taxonomic groups on tiles of the varioustreatments. The linear model was a mixed design withtwo fixed effects (antifouling paint, a 5 2; perimeter,b 5 4) and one random effect (site, c 5 2). Student-Newman-Keuls post hoc comparisons (Winer et al.1991) were used when main or interaction effects weresignificant. Analysis of similarities (ANOSIM, PRIM-ER 5 Statistical package, Primer-E 2001) was carriedout to test for differences between assemblages of re-cruits on antifoulant-coated tiles of the various perim-eter treatments (N 5 40). Bonferroni’s procedure wasused to control for Type-II error inflation from multiplepairwise comparisons (Winer et al. 1991). Similaritypercentages (SIMPER, PRIMER 5 Statistical package,Primer-E 2001) were calculated for the treatments. Thistechnique calculates average dissimilarities within andbetween groups of samples. For both ANOSIM andSIMPER, data were log(x 1 1)-transformed to preservetrends in numerical abundance, and the Bray-Curtissemi-metric was used as the dissimilarity measure(Bray and Curtis 1957).

RESULTS

Effects of antifouling paint type on colonizationby Watersipora subtorquata and facilitation

of other fouling taxa

A total of 35 fouling taxa recruited to tiles of thevarious treatments. In each marina, the antifouling

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1728 OLIVER FLOERL ET AL. Ecological ApplicationsVol. 14, No. 6

FIG. 2. Percent cover (mean 6 1 SE) of Wa-tersipora subtorquata (filled symbols, closedline) and other sessile organisms (open symbols,dashed line) on tiles submerged in marinas inTownsville (circles) and Cairns (squares). Tileswere coated in (a–c) antifouling paints 1–3 and(d) nontoxic marine primer.

FIG. 3. Epibiosis on Watersipora. (Left) Colonies of W. subtorquata on a fiberglass surface coated in antifouling paintafter four months of submersion in the Townsville marina. No other taxa have recruited directly to antifouling paint surfaces,but erect bryozoans, tubiculous polychaetes, and tubiculous amphipods occupy the upper surface of W. subtorquata colonies.Photo credit: O. Floerl (2000). (Right) An individual of the nonindigenous kelp Undaria pinnatifida (UN) has been transportedthrough New Zealand’s South Island on the hull of a fishing vessel as an epibiont on Watersipora sp. (WS). Photo credit:T. Dodgshun, Cawthron Institute (1999). Color versions of the photos in this figure are available in the Appendix.

paints prevented recruitment of all taxa for a period offour weeks. Over the same period, recruits covered anaverage of 87.89 6 1.49% (Townsville; mean 6 1 SE)and 27.15 6 1.77% (Cairns) of the surface of tilescontaining just the nontoxic primer (Fig. 2). After animmersion time of eight weeks, colonies of W. sub-torquata were present on 66% (Townsville) and 29%(Cairns) of tiles coated with antifoulant. After 16weeks, it occurred on all antifoulant-coated tiles from

Townsville and on 88% of those from Cairns. The areait covered on these tiles varied between marinas andtreatments and was generally highest for tiles coatedin paint type 3 (Townsville, 64.5 6 4.8%; Cairns, 22.36 4.2%; ANOVA, marina 3 paint type, F3,8 5 24.85,P , 0.001, SNK test, P , 0.05; Fig. 2).

After 16 weeks of immersion, 34 fouling taxa hadsettled directly onto painted tile surfaces and on theupper surfaces of W. subtorquata colonies (Fig. 3, Ap-

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December 2004 1729FACILITATION OF NONINDIGENOUS SPECIES

TABLE 3. Summary of ANOVA on percent cover and density of recruits on tile surfaces andnatural Watersipora subtorquata colonies after 16 weeks of tile immersion.

Treatment df

Percent cover†

F P

Density of recruits(no./cm2)

F P

Marina (M)Paint treatment (PT)Substratum (S)M 3 PTM 3 S

13131

4.549.47

13.387.321.85

0.0490.0010.0020.0030.192

0.441.57

19.205.65

12.77

0.5170.235

,0.0010.0080.003

PT 3 SM 3 PT 3 SSite (M 3 PT 3 S)Residual

32

1586

29.493.462.20

(0.85)‡

,0.0010.0410.010

15.441.063.71

(2.57)‡

,0.0010.392

,0.001

Note: Abbreviations are: M, marina (Townsville, Cairns); PT, paint treatment (antifoulingpaints 1–3, nontoxic primer); S, substratum (W. subtorquata colonies vs. tile surface).

† Log(x 1 1)-transformed (following Cochran’s C test, P , 0.05).‡ MSResidual.

FIG. 4. Recruitment of sessile organisms toWatersipora subtorquata and tile surfaces coat-ed in antifouling paints 1–3 (P1, P2, and P3)and control (C) after 16 weeks immersion in thesea. Shown are: (a) density of recruits (no. re-cruits/cm2 of substratum) and (b) percent cover.Values for cover on W. subtorquata coloniesindicate the percentage of the colony surfacearea that was colonized by epibiotic organisms.Data are means 1 1 SE. No data on the percentcover of epibionts on W. subtorquata exist forcontrol tiles from Townsville.

pendix). The zooids within those portions of W. sub-torquata colonies that were colonized by epibiontswere usually found dead and unoccupied. On tiles coat-ed in antifoulant, both the proportion of space the newrecruits occupied as well as their density (number persquare centimeter) were greater on W. subtorquata col-onies than on surrounding paint surfaces (Table 3, Fig.4a). Between 13.7% and 95.8% of the upper surfacearea of W. subtorquata colonies were occupied by sec-ondary recruits, at densities of 2.4–7.9 recruits/cm2. Incontrast, only 0.6–8.8% of the tile area coated in an-tifouling paint was occupied, at densities of 0.1–2.79recruits/cm2. The density of recruits on W. subtorquatacolonies was always greater than on surrounding toxicsurfaces. On 53% of tiles coated with antifoulant (allthree paint types; N 5 48), densities of recruits on W.subtorquata colonies were 11–40 times higher thanthose observed directly on the paint surface. Maximumdensities reached 20.5 recruits/cm2 on W. subtorquata,which was up to 200 times higher than directly onpainted surfaces. Generally, only a small subset of theavailable species (principally the introduced bryozoan

Bugula neritina) settled directly to antifouling paintsurfaces. In contrast, up to 13 different taxa were foundon W. subtorquata colonies on a single tile. On tilesthat did not contain the antifoulant biocide, the percentcover and density of recruits on the tile surface weresimilar to, or larger than on the percent cover and den-sity of recruits on W. subtorquata colonies on the sametile (Fig. 4b). The abundance of recruits varied in space(Table 3). There were no differences in the averagepercent cover and density of recruits between differentantifouling paints; differences among treatments oc-curred only between toxic and nontoxic surfaces.

Influence of colony size on epibiosison Watersipora subtorquata

A total of 23 different taxa recruited to the tiles inthis experiment. Epibionts were encountered through-out the entire upper surface of mimic colonies of allsizes. Generally, recruitment (all taxa pooled) wasgreater to mimic W. subtorquata colonies on the tilesthat were coated in the toxic antifouling paint (108–185 recruits per tile depending on perimeter : area ra-

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1730 OLIVER FLOERL ET AL. Ecological ApplicationsVol. 14, No. 6

FIG. 5. Abundance of recruits on mimic Watersipora subtorquata colonies with small (1.34), medium (1.91), and large(5.72) perimeter : area ratios and control surfaces (no perimeter) after six weeks of tile immersion. All treatments werereplicated on toxic (antifouling paint) and nontoxic (marine primer) tiles (N 5 80). Data are means 1 1 SE. Results of SNKtests are depicted by letters above each mean. Treatment means with the same letter are not significantly different at P 50.05.

tio) than to mimics on tiles that lacked the toxic biocide(50–68 recruits per tile). In the latter case, the meannumber of recruits did not vary with colony size, buton the tiles coated with antifoulant recruitment was, onaverage, 150–170% greater to colonies with a largeoverall perimeter : area ratio (5.72) than on colonieswith small- (1.34) or intermediate-sized (1.91) coloniesthat had smaller perimeter : area ratios (Fig. 5a; SNK-

test, P , 0.05). The number of taxa that recruited tomimic W. subtorquata colonies was similar for all col-ony size and antifouling paint treatment configurationsand ranged from 8.8–11.6 taxa per tile. The mean num-ber of taxa was smallest on antifoulant-coated tileslacking mimic colonies (2.1 6 0.23) and largest onnontoxic tiles with mimic colonies that had a largeperimeter : area ratio (11.6 6 0.65; Fig. 5b, Table 5;

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TABLE 4. Results of calculation of similarity percentages (SIMPER) on assemblages of recruitson antifoulant-coated tiles with mimic colonies of small, medium, and large total perimeters.

Colonyperimeter Small Medium

Medium 1) Sabellids (160%)2) Corophium (231.5%)3) Hydroids (234.3%)4) Spirorbids (137.5%)5) Sol. ascidians (123%)

Large 1) Bugula sp. A (275.8%)2) Corophium (258.9%)3) Hydroids (176%)4) B. neritina (262.1%)5) Spirorbids (237.5%)

1) Sabellids (249.2%)2) Hydroids (116.8%)3) Corophium (240%)4) B. neritina (260.1%)5) Bugula sp. A (260.7%)

Notes: For each comparison the taxa are ranked according to their relative contribution tothe multivariate dissimilarities between perimeter treatments. The cutoff point was at 50%dissimilarity. Values in parentheses indicate the difference in abundance of the respective taxa(column minus row abundance) expressed as the percentage of the column abundance. Forexample, Sabellids were 60% more abundant on small-perimeter colonies, and Corophium was31.5% less abundant.

SNK-test, P , 0.05). The composition of epibiotic as-semblages on colonies with small and medium perim-eter : area ratios significantly differed from those witha large ratio, but not from one another (ANOSIM, GlobalR 5 0.594, P , 0.001; pairwise comparisonsmall/medium,R 5 0.037, P 5 0.240). The colonies with a largeperimeter : area ratio were characterized by: (1) a high-er abundance of bugulid bryozoans (60–76% more B.neritina and Bugula sp. A than in other treatments),(2) a higher abundance of Corophium sp. (40–59%more), (3) a higher abundance of tubiculous poly-chaetes (38–49% more spirorbids and sabellids), and(4) a lower abundance of hydroids (17–76% less) (SIM-PER, Table 4). Furthermore, the bryozoans Savignyellalafontii, Celleporaria sp., and Bugula sp. A recruitedto large-perimeter colonies, but not to those with amedium or small perimeter.

Patterns of recruitment to mimic W. subtorquata col-onies varied strongly between taxonomic groups andtreatments (Table 5, Fig. 5c–m). On tiles coated withtoxic paint, recruitment of encrusting and erect bryo-zoans, Corophium sp. and serpulid and sabellid poly-chaetes was higher to mimic colonies with a large pe-rimeter : area ratio than to those with small or mediumratios (Fig. 5; ANOVA, significant perimeter or anti-fouling paint 3 perimeter effects, SNK-tests; Table 5).On surfaces without the toxic antifoulant, the only sig-nificant difference in recruitment to mimic coloniesoccurred for colonial ascidians, which were found ingreatest numbers (2.9 6 0.52 tile21) on colonies withlarge perimeter : area ratios (Table 5, Fig. 5e). Erectbryozoans were strongly associated with small mimiccolonies on surfaces painted with antifoulant. Meandensities of erect bryozoans were 2.5 and 3.1 timesgreater on colonies with large perimeter : area ratios(42 6 2.3 recruits/tile), than on colonies with smalland intermediate perimeter : area ratios, respectively(Fig. 5h). The size of the mimic colonies on tiles coated

in antifoulant had no influence on the number of bar-nacles, bivalves, colonial and solitary ascidians, andhydroids that recruited them (Fig. 5c–f, j, Table 5).

The presence of toxic paint adjacent to mimic col-onies influenced recruitment of encrusting and erectbryozoans, hydroids, serpulids, sabellids, and spirorbidpolychaetes to upper W. subtorquata colony surfaces(Table 5, Fig. 5). Generally, greater numbers of thesetaxa occurred on mimic colonies surrounded by toxicantifouling paint compared to when antifouling paintwas absent (ANOVA, significant toxic or toxic 3 pe-rimeter effects; SNK-tests; Table 5). Amongst the spe-cies exhibiting this pattern, the numerically most abun-dant ones were the introduced species Hydroides ele-gans, Ficopomatus uschakovi (tubiculous polychaetes),Balanus amphitrite (a barnacle), and Bugula neritina(an erect bryozoan). H. elegans, F. uschakovi, and B.amphitrite occurred only on toxic tiles that containedW. subtorquata colonies, and B. neritina was ;250times more abundant on such tiles than on those lackingW. subtorquata colonies. All four species are nonin-digenous to Australia, but today are widely distributedaround its coastline (Ryland and Hayward 1977, Hewittet al. 1999).

DISCUSSION

Our study shows that habitat modification by theintroduced bryozoan W. subtorquata facilitates the col-onization of toxic ship hull surfaces by marine foulingorganisms. The presence of W. subtorquata on simu-lated vessel hulls coated in toxic antifouling paints fa-cilitated the recruitment of a total of 22 sessile marinetaxa that were not able to colonize adjacent toxic sur-faces, and greatly enhanced the abundance of four spe-cies that did recruit to toxic surfaces in small abundance(Fig. 3). The interaction observed between W. subtor-quata and its epibionts is best described as a form ofexploitation (Ricciardi 2001). Organisms growing on

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1732 OLIVER FLOERL ET AL. Ecological ApplicationsVol. 14, No. 6

TABLE 5. Summary of ANOVA on the numerical abundance of recruits on mimic Watersipora subtorquata colonies andcontrol surfaces after 16 weeks of tile immersion.

Recruits

Source of variation

Antifouling paint (AP)[d.f. 5 1]

F P

Perimeter (P)[d.f. 5 3]

F P

AP 3 P[d.f. 5 8]

F P

Site(AP 3 P)[d.f. 5 8]

F PMSerror

[d.f. 5 64]

Total recruitsNo. taxaBarnaclesBivalves

30.103769

4.160.71

0.001,0.001

0.0760.424

20.4163.10

2.220.63

,0.001,0.001

0.1630.614

14.8143.66

2.391.25

,0.001,0.001

0.1440.354

4.880.580.530.88

,0.0010.7870.8270.539

329.732.780.560.98

Colonial ascidians†Solitary ascidiansEncrusting

bryozoans†Erect bryozoans

0.320.42

3.9248.58

0.5900.533

0.083,0.001

6.103.81

4.3059.61

0.0180.058

0.044,0.001

4.389.37

1.4452.28

0.0420.005

0.303,0.001

0.970.79

7.251.02

0.4670.616

,0.0010.434

0.223.75

0.1527.11

Corophium†HydroidsSerpulidsSabellidsSpirorbids

0.0010.18

179.8033.97

2.26

0.9810.013

,0.001,0.001

0.171

4.592.41

85.6211.39

1.72

0.0380.1420.0010.0030.239

0.353.46

73.459.062.35

0.7890.071

,0.0010.0060.149

3.041.580.481.318.89

0.0060.1490.8660.257

,0.001

0.729.41

50.3760.4661.03

† Log(x 1 1)-transformed data.

W. subtorquata colonies caused the death of the basalzooids they covered, presumably by inhibiting the feed-ing movements of their lophophores. After 16 weeksof immersion, the entire upper surface of W. subtor-quata colonies was often overgrown, resulting in com-plete mortality of the zooids.

Virtually all existing accounts of facilitation amongstNIS describe interactions in the latter stages of theinvasion process that enhance establishment or the rateof spread in the invaded habitat (see references in Ric-ciardi [2001] and Simberloff and von Holle [1999]).On the basis of the patterns observed for Hydroideselegans, Ficopomatus uschakovi, Balanus amphitrite,and Bugula neritina, our study shows that facilitationamong NIS can also occur in the transportation stage.F. uschakovi and B. neritina were the numerically mostabundant epibionts on W. subtorquata colonies duringthis experiment, and would have been transported byinfested vessels in large numbers. Watersipora sp. hasalso facilitated transport of the invasive kelp Undariapinnatifida on vessel hulls in New Zealand (Fig. 3).Facilitation of locally native taxa by Watersipora couldalso lead to their transport to habitats to which theymay be nonindigenous. Propagule supply is an impor-tant correlate of invasion success in both aquatic andterrestrial systems (Lonsdale 1999, Ruiz et al. 2000).Interactions between NIS that enhance transport ofpropagules by human vectors (such as ship hulls) tonew locations or habitats, therefore, have the potentialto increase the probability of a successful invasion(Wonham et al. 2000).

Influence of toxic paint and colony sizeon epibiotic recruitment

Studies in both aquatic and terrestrial ecosystemshave documented that the number of species and in-dividuals that live in a patch of habitat can be influ-

enced by the size and shape of the patch and by itssurroundings. In dense aggregations of gregarious ma-rine species, such as those of the barnacle Chamaesiphotasmanica and the serpulid worm Galeolaria caespi-tosa, the presence of conspecific individuals surround-ing vacant patches provides a positive cue for com-petent larvae to settle (Minchinton 1997, Jeffery 2000).Patches with a large perimeter : area ratio, therefore,receive more settlement than patches with smaller ra-tios but the same area (see also Crisp and Meadows1962, Burke 1986, Pawlik 1992). Studies concernedwith the design of nature reserves have generally foundthat several small patches of habitat contain more spe-cies of arboreal arthropods, marine crustaceans, birds,plants, mammals, and lizards than a single patch of thesame area, possibly due to a greater diversity of habitatswithin several smaller patches (Simberloff and Abele1982, Simberloff 1988 and references therein). In thisstudy, we anticipated toxic paint surfaces to act as neg-ative cues for recruitment to W. subtorquata. Becauseantifouling toxins could leach across adjacent colonysurfaces, we predicted that (1) less recruitment shouldoccur on W. subtorquata colonies that are surroundedby toxic paint than on those that are not surrounded bysuch paint and, therefore, (2) in the presence of toxicpaint, less recruitment should occur on several smallW. subtorquata colonies with a large perimeter : arearatio than on a single large colony with a small ratio.

Contrary to our predictions, recruitment of epibiotawas generally two to three times greater on mimic col-onies surrounded by toxic antifouling paint. Further-more, the density of recruits on mimic colonies wasnegatively correlated with colony size. For five out of11 taxa (encrusting and erect bryozoans, Corophium sp.and serpulid and sabellid polychaetes), maximum num-bers of recruits on antifoulant-coated surfaces were en-countered on small colonies with large perimeter : area

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December 2004 1733FACILITATION OF NONINDIGENOUS SPECIES

ratios. Several species of bryozoans (Savignyella la-fontii, Celleporaria sp., and Bugula sp. A) recruitedexclusively to these small colonies. Our results suggestthat the presence of antifouling compounds generallyenhanced epibiotic recruitment to W. subtorquata col-onies, and this pattern was driven primarily by highrecruitment of the nonindigenous species F. uschakovi,H. elegans, and B. neritina.

The absence or very low abundance of recruitmentdirectly onto toxic surfaces indicates that the biocideswithin the paints inhibited settlement of competent lar-vae. Recruitment of epibionts occurred throughout theupper surface of mimic W. subtorquata colonies, in-cluding peripheral areas, suggesting that diffusion ofbiocides across colonies either did not occur or wastoo weak to influence settlement and recruitment. Likenatural W. subtorquata colonies, our mimic colonieswere ;1.5 mm thick. Depending on the flow of wateracross antifouling paint surfaces, the boundary layerinto which toxins leach from the paint concentrate hasa thickness of only 10–500 mm (Marine Science andEcology 2002). In contrast to other approaches aimedat exposing marine sessile invertebrate larvae to copperpollutants (Johnston and Webb 2000, Johnston andKeough 2002, Ng and Keough 2003), larvae settlingto upper surfaces of the colonies in this experimentmay not have come into contact with sufficiently highconcentrations of biocide to inhibit recruitment.

It is unclear why densities of fouling organisms onmimic colonies were greater when they were surround-ed by toxic paint surfaces rather than by nontoxic prim-er. Active avoidance and searching behavior by com-petent larvae has been documented for many marinesessile species (Meadows and Campbell 1972, Crisp1984, Abelson 1997), and competent larvae may havecongregated on mimic colonies following avoidance oftoxic surfaces. Laboratory-based studies suggest thatthe release of biocides from antifouling paint surfacesinduces pre- or post-settlement mortality in marine in-vertebrates (Crisp and Austin 1960, Wisely 1962,1963b, 1964), which could be used to argue againstactive avoidance. However, in situ concentrations ofantifouling biocides may be lower than those in lab-oratory assays, and the patterns observed here may becaused by hormesis, the induction of settlement,growth, or other physiological responses in marine in-vertebrates and plants under low concentrations of tox-icants (McCann et al. 2000, Migliore et al. 2000).

Influences of facilitation on vector selectivityand transport of NIS by human vectors

The types of species and propagules that are trans-ported by humans are determined by the selectivity ofthe transport mechanisms (vectors) involved. For ex-ample, only small organisms are able to pass throughthe filtration systems on a ship’s ballast water intake,and only insects buried in the pot soil might survivethe treatment with insecticides, herbicides, or irradia-

tion that many flowers undergo prior to export or uponimport. Species such as W. subtorquata are able toovercome the selective exclusion mechanisms of avail-able transport vectors and make them available to spe-cies that would otherwise be excluded from transport.

Watersipora subtorquata is now widely distributedacross the globe, occurring in Brazil, the West Indies,Bermuda, Cape Verde Islands, New Zealand, TorresStrait, and northeastern and southern Australia (Ryland1974, Gordon and Matawari 1992, Hayward and Ry-land 1995, Hewitt et al. 1999, Floerl 2002). Watersi-porid bryozoans are able to thrive in waters pollutedby heavy metal contaminants (Allen 1953, Wisely andBlick 1967, Moran and Grant 1993). In many urbanand industrial marine environments, there is an abun-dance of surfaces coated with antifouling paint, in-cluding the hulls of boats and ships of all kinds andsizes, harbor buoys and markers, and other permanentstructures associated with shipping ports. On suchstructures, W. subtorquata can act as a ‘‘foundationspecies’’ (sensu Dayton 1975) for diverse secondaryassemblages such as mytilid bivalves do in many rockyintertidal communities (Lohse 1993). The ongoingmaintenance of fouled manmade structures such as shiphulls, piers, bridges, offshore oil and gas structures, orcooling water intakes of power plants can involve sub-stantial costs (Costlow 1984, Nalepa and Schloesser1993, Marshall 1994). Facilitation by W. subtorquatais of particular importance for fouling assemblages onship hulls for two reasons. First, hull fouling has largeeconomic impacts on the shipping industry because thecolonization of submerged hull surfaces leads to lossesin cruising speed and increases in fuel consumption(AMOG Consulting 2002, Marine Science and Ecology2002). Second, commercial ports and recreational ma-rinas throughout the world are connected by a densenetwork of shipping routes, and are often ‘‘hotspots’’for populations of NIS (Carlton 1987, Hewitt 2002,Hutchings et al. 2002). The occurrence of W. subtor-quata in international shipping hubs may facilitate thetransport of locally occurring species that may other-wise have been prevented from attaching to ships’ hullsby antifouling paints. Exposure of W. subtorquata lar-vae to antifouling toxins (copper) has delayed effectsand reduces growth of adult colonies (Ng and Keough2003). However, even when growth is impeded andcolonies reach sizes of only 7 mm diameter, W. sub-torquata is able to facilitate the transport of large num-bers of fouling organisms, including some NIS, if col-onies are present at sufficient densities. Our studyshowed that as many as 102 colonies of W. subtorquatarecruited to an area of 225 cm2 over a four-week period.Vessels that are moored in environments where W. sub-torquata is present may risk transporting fouling spe-cies on their hulls despite having treated them withtoxic antifouling paints only recently.

With ever increasing global markets and the contin-ual development of networks for transport and trade,

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1734 OLIVER FLOERL ET AL. Ecological ApplicationsVol. 14, No. 6

the number of transportation pathways for NIS is likelyto rise (Jenkins 1999, Carlton 2000). An ‘‘invasionalmeltdown’’ may be caused by positive interactions be-tween NIS that arrive and establish in new habitatsindependently from one another. Our study suggeststhat ‘‘meltdowns’’ could also be fostered by facilitativeinteractions during earlier stages of the invasion pro-cess by species that modify human transport vectorsand increase the supply of nonindigenous propagulesto uninvaded habitats.

ACKNOWLEDGMENTS

We thank the operators of the Townsville Breakwater Ma-rina and the Cairns Halfmoon Bay Marina for access to thesesites and help with our research. Thanks are also due to GillCarr, Matthias Floerl, Amanda Hodgson, Helene Marsh, JohnMillett, Kirsti Sampson, and Susan Tallarico for technicaladvice and invaluable assistance with fieldwork and prepa-ration of the various experiments. An earlier manuscript ben-efited greatly from helpful comments by Nick Gust (NIWA),Emma Johnston (University of New South Wales), Ivan Law-ler and Scott Smithers (James Cook University), and twoanonymous reviewers. This study was supported by researchgrants from the School of Tropical Environment Studies andGeography (James Cook University), the CRC Reef ResearchCenter (Task B1.10) and Akzo Nobel Coatings.

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APPENDIX

Color photos corresponding to Fig. 3 are available in ESA’s Electronic Data Archive: Ecological Archives A014-034-A1.