gy and Ecology 342 (2007) 54–60www.elsevier.com/locate/jembe

Journal of Experimental Marine Biolo

Do artificial substrates favor nonindigenous foulingspecies over native species?

Megan C. Tyrrell a,⁎, James E. Byers b

a Wells National Estuarine Research Reserve, 342 Laudholm Farm Road, Wells, ME 04090, United Statesb Department of Zoology, University of New Hampshire, Durham, NH 03824, United States

Received 1 September 2006; received in revised form 1 October 2006; accepted 9 October 2006

Abstract

Exotic species are prominent constituents of fouling communities. If exotic fouling organisms colonize or compete better on awider range of substrate types than native species, this may partially account for their high abundance in estuaries and bays. Weused four artificial and four naturally occurring substrate types to compare initial settlement and percent cover of native and exoticfouling species through six months of community development. Both the identity of common taxa and the total number of speciescolonizing artificial versus natural substrate types were similar. Despite the similarities in species richness, relative abundancepatterns between natural and artificial substrate types varied, particularly as the communities developed. Native species wereinitially in equal abundance on natural and artificial substrate types. Initially, the two most common exotic species, the colonialtunicates, Botrylloides violaceus Ritter and Forsyth and Botryllus schlosseri (Pallas), were also in similar, but low, abundance onartificial and natural substrates. As the communities developed, there was little change in abundance of exotic or native species onnatural substrates. However, on artificial substrates the exotic tunicates increased dramatically and native species declined inabundance. Artificial surfaces may provide a novel context for competitive interactions giving exotic species a more “level playingfield” in an environment for which they otherwise might not be as well adapted compared to long-resident native species. Additionsof artificial substrates to nearshore environments may disproportionately favor exotic species by increasing local sources of exoticpropagules to colonize all types of substrates.© 2006 Elsevier B.V. All rights reserved.

Keywords: Anthropogenic disturbances; Community development; Invasion impact; Nonindigenous species; Selection regime modification;Settlement

1. Introduction

Competition is a highly context dependent interac-tion. Theoretically, one might assume that given thou-sands of years of adaptation to their local environment,resident species should have inherent advantages whencompeting with nonindigenous species because the

⁎ Corresponding author. Tel.: +1 207 646 1555; fax: +1 207 646 1290.E-mail address: mtyrrell@alumni.macalester.edu (M.C. Tyrrell).

0022-0981/$ - see front matter © 2006 Elsevier B.V. All rights reserved.doi:10.1016/j.jembe.2006.10.014

residents should be best adapted to local conditions(Byers, 2002). For an exotic species to becomeestablished in a novel, crowded community (i.e. withlittle “empty niche” space), let alone outcompete anative species, it would seemingly need to either enteran environment with conditions very similar to its homerange or be so competitively dominant that environmentaldifferences are inconsequential. The fact that most inva-sions fail (Williamson, 1996) suggests that these condi-tions are infrequently met. However, a third mechanism is

55M.C. Tyrrell, J.E. Byers / Journal of Experimental Marine Biology and Ecology 342 (2007) 54–60

also possible that may be partially responsible for theapparent increase in the rate of exotic species invasions(Cohen and Carlton, 1998). An invader may enter anenvironment that has been intensely altered byanthropogenic disturbance. These disturbances, if out-side the magnitude, duration, or frequency of naturaldisturbances that affect communities, can create amismatch between traits of the native species and theenvironmental conditions to which they have longadapted—a phenomenon termed selection regimemodification (SRM) (Byers, 2002). Not only is thisthird mechanism powerful, but it is likely to increase asanthropogenic impacts continue at unprecedented ratesin nearly all ecosystems on earth (e.g., Vitousek et al.,1997; Janzen, 1998). This mechanism may also help toexplain, at least in part, the observed strong correlationof invasions in disturbed environments (e.g., Hobbs andHuenneke, 1992).

The SRM mechanism predicts that highly disturbedenvironments will have a greater abundance of exoticspecies and that the impact of invading species on nativespecies will be greater in these environments. Marinefouling communities are excellent systems to test thishypothesis. Any hard surface in the marine environmentis potential habitat for fouling species. For foulingorganisms, artificial substrates represent an anthropo-genically altered environment that is equally foreign tothe evolutionary history of all species, both native andnonindigenous alike. Thus, artificial substrates have byour definition been in the marine environment for a briefperiod of time relative to the evolutionary history of theorganisms involved. Substrate recognition and prefer-ence is a characteristic described for many taxa withplanktonic life stages (e.g. McKinney and McKinney,2002; Harrington et al., 2004; Vermeij, 2005). Properrecognition followed by adhesion and growth, are traitsthat should be heavily selected for in fouling speciesand these processes are likely strongly influenced bysubstrate type. Because fouling species are usually spacelimited, they compete vigorously and it is easy to ma-nipulate the availability of their limiting resource byproviding habitat, both natural and artificial. Further-more, fouling communities represent a highly tractable,well studied system (e.g. Connell and Glasby, 1999;Connell, 2001; Stachowicz et al., 2002a) with a mode-rate number of exotic species to provide suitable reso-lution to test the predictions of the SRM hypothesis.

We predict that exotic species on average should bemore abundant on artificial substrates than on naturalsubstrates. There are two potential mechanisms thatwould lead to this pattern. First, if substrate recognitionand selection is important, then relative to natural

surfaces, native species will settle less on artificialsurfaces. Native species could actively avoid artificialsubstrates either because they don’t recognize them, orbecause they are suboptimal resources. For example,Anderson and Underwood (1994) reported higherrecruitment by oysters and barnacles on concrete andplywood than on two artificial substrate types. Similarly,Bulleri (2005) described different recruitment patternsof epibiotic organisms on sandstone seawalls versusrocky shores. Second, native species should competebest on natural surfaces, to which they are accustomed,compared to artificial substrates. That is, the loss of a“home court” competitive advantage for native specieson artificial substrates may lead to a higher abundanceof exotic species on artificial substrate types. If nativeand exotic species are equally non-discriminating intheir choices for settlement substrate, or if the environ-ment is saturated with larvae, there may be few initialdifferences in settlement pattern by native and exoticspecies on different substrate types as the first mechan-ism specified. Differences may accrue only later assettled individuals (and colonies) grow larger, intensify-ing competition for space. In such a case, post-settlement processes, such as relative adhesion strength,relative growth rates, and additional competitiveabilities, will have strong influence over final commu-nity structure on various substrate types.

Our hypotheses are more focused on native speciessettling or performing poorly on artificial surfaces ratherthan exotic species doing exceptionally well on thesetypes of substrates. After all, artificial substrates areforeign for exotic species too. However, because com-petition is a context-dependent interaction that operatesin relative, not absolute terms, we expect artificial sub-strates may erase much of native species’ prior residentadvantage. In contrast, native species are expected tocompete more successfully on natural substrates onwhich they evolved. Granted exotic species may haveevolved on these natural substrates as well, as thesesubstrates are often ubiquitous, but on natural substratesthe full environmental milieu to which the native isadapted should give it an advantage in contextdependent competition. It is only on foreign substratetypes that native species lose their relative competitiveadvantage.

Differences in the species composition of foulingcommunities on artificial substrates have long beenrecognized (Karlson, 1978; Anderson and Underwood,1994; Underwood and Anderson, 1994; Bulleri, 2005).However, a systematic bias in the trends of native andexotic species as a function of substrate type has yet tobe fully documented. A recently reported pattern of

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exotic species predominance on artificial substrates inElkhorn Slough, California USA strongly suggests sucha systematic bias may exist (Wasson et al., 2005). As inmany sedimentary estuarine environments, the onlyhard surfaces within Elkhorn Slough are provided byhuman-made structures. Wasson et al. (2005) found anapproximately equal number of species in soft and hardhabitats; however, exotic and cryptogenic speciescomprised 38% of species in soft sediment and 68%on hard substrates. Furthermore, exotic taxa covered thevast majority of space (84%) on the human introducedhard surfaces. The possibility of a high prevalence ofexotic species in highly modified estuarine embaymentshas influenced surveys of incipient exotic species totarget these types of environments (e.g., Pederson et al.,2005).

In this study we experimentally examine potentialsystematic trends in exotic and native species richnessand abundance in fouling communities as a function ofsettlement substrate. By standardizing for substrate areaand length of community development, we isolate theeffect of substrate per se. By examining replicates ofseveral types of artificial and natural substrates weintend to expose the generality of response of native andexotic species to the two substrate categories. Finally,comparison of the experimental results to our predic-tions will help to assess the potential of the SRMmechanism as an explanation for enhanced exoticspecies abundance and impact in disturbed environments.

2. Methods

To examine variation in exotic species success as afunction of substrate type, four natural and four artificialmaterials were chosen. Natural substrate types were:shell, marble, slate, and wood. Artificial substratesconsisted of aluminum sheet metal, styrofoam, PVC(polyvinylchloride), and rubber. The emphasis on ourchoice of artificial substrates was on materials that arewell outside of the historical exposure of the foulingorganisms, and thus not a part of their evolutionaryhistory. While rubber and metal are not human-madematerials, they are not substrates that would normally beencountered in a pristine estuarine environment. Thenatural substrates had relatively smooth surfaces due tobeing cut, but otherwise they were not modified in anyway (e.g., wood was not pressure treated, rocks wereunpolished). All substrates except the shell were flat10 cm×10 cm panels that were glued to Plexiglassbacking, secured with cable ties, and the Plexiglass wasattached to metal brackets. The shell substrates werescallops that were very slightly convex and ∼12.1 cm

wide and 11.7 cm long. In all cases, the center 68 cm2 ofthe substrate was analyzed to standardize area searchedand to minimize edge effects.

Five replicate brackets containing each of the eightsubstrate types were hung from floating docks so thatthe substrates faced down and were suspended ∼3 mbelow the water surface. The substrates were deployedon May 16, 2004 at the town landing in Wells, MaineUSA. The site is a busy commercial and recreationalmarina in an embayment with a naturally occurringmixture of soft and hard substrates. A water qualitymonitoring device is located at the pier. During the studyperiod, salinities ranged from 29–35 ppt and watertemperature ranged from 8.7 to 21.2 °C. In July,September, and October 2004, the substrates wereremoved from the brackets and brought to the laboratoryfor analysis. The major recruitment period for foulingspecies in New England is May to October (Stachowiczet al., 2002b), and previous investigations indicated thatmany fouling species begin to senesce in November(Tyrrell and Byers, unpub. data).

At the end of August, one of the brackets was lostwhen the piece of the dock that it was tied to wasdamaged; thus results are presented for four replicates ofeach substrate type. One metal substrate was lost beforethe July analysis and one slate and wood substrate werelost before the September analysis. Upon collection,each substrate was submerged in seawater and the center68 cm2 area was examined. To analyze the relativeattractiveness of different substrate types as settlementspace, a census was performed to quantify speciesrichness. To compare how the amount of space occupieddiffered between substrate types, relative abundance wasassessed by recording the identity of each species under50 random points on a Plexiglass plate. We focused onquantifying the occupation of primary space, i.e. thosespecies directly in contact with the supplied substrate. BySeptember, the arborescent hydroid Tubularia crocea(L. Agassiz) had become extremely abundant, but weassessed primary space occupation under the canopy ofTubularia. The substrates were returned to the fieldafter analysis to non-destructively follow the develop-ment of the communities through time.

For statistical analysis, species richness data weresquare root transformed and percent cover data were arcsine square root transformed. A repeated measuresANOVA was performed on species richness in July,September, and October as a function of substrate type(artificial versus natural). Cryptogenic species weregrouped with exotic species for comparisons of richnessof natives versus exotics (when cryptogenic specieswere excluded we got the same qualitative results across

Fig. 2. Percent cover of all native taxa (per 68 cm2±1 SE) on artificialand natural substrate types. Open bars indicate artificial substrate typesand shaded bars indicate natural substrate types.

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substrate types). For percent cover analyses, a repeatedmeasures ANOVA was used to compare the abundanceof all native species on natural and artificial substrates inSeptember and October. A second repeated measuresANOVA was used to compare the abundance of thenonindigenous tunicates, Botrylloides violaceus andBotryllus schlosseri, on natural and artificial substratesin the same two months. We focused on analyzing theabundance of these two nonindigenous tunicate speciesbecause these two species were conspicuous compo-nents of the community and the other nonindigenousand cryptogenic species occurred in only trace abun-dance in comparison. The substantial bare space on thepanels in July (>50%) indicated that after only twomonths of community development, competition forspace and species interactions in general were likelyminimal, so we did not use the July data for abundancecomparisons.

3. Results

A total of thirty-five species were encountered on thesubstrates, of these, three are nonindigenous (B. violaceus,B. schlosseri and Membranipora membranacea [Lin-naeus]) and four are cryptogenic (Bowerbankia gracilisLeidy, Cryptosula pallasiana Levinson, Electra pilosa[Linnaeus], and Campanularia sp.) (Carlton, 2003). Thefour most abundant species in order were: T. crocea(native), B. violaceus (exotic), B. schlosseri (exotic), andthe spongeHalichondria panicea [Pallas] (native). Thesefour species occurred on every substrate type, indicatingthat these common species were able to colonize allsubstrate types. For the less common species, there weresmall variations in settlement between substrate types. Forexample, Campanularia sp. only appeared on shell whileM. membranacea never colonized shell or marble

Fig. 1. Total number of species (±1 SE, solid bars) and number ofnonindigenous and cryptogenic species (NIS) (±1 SE, stippled bars)on artificial (light colored bars) and natural substrate types (darkcolored bars).

substrates. Generally, species lists were very similarbetween all of the substrate types.

Average species richness was similar on each of thesubstrate types (e.g. in October mean=7.10, SE±0.38).The total number of species did not differ between sub-strate categories (Fig. 1, F1,27=0.014, p=0.91), indicat-ing that the relative attractiveness of natural versusartificial substrate types was very similar. The number ofspecies on the substrates increased with time(F2,26=26.75, p<0.001), but the time by substrate typeinteraction was not statistically significant (F2,26=0.67,p=0.52).

Despite similarities between natural and artificialsubstrates in the species richness patterns, there werestrong differences in the amount of space occupied bynative and exotic taxa between these two substratecategories. The percent cover of native species onnatural substrates increased only slightly from 47% inSeptember to 51% in October (Fig. 2). However, onartificial substrates, natives declined from 42% inSeptember to 28% in October. This differential declinein native percent cover on artificial substrates relative tonatural substrates was significant (time by substrate typeinteraction: Fig. 2, F1,27=4.96, p=0.035). The effect oftime alone on the amount of space occupied by nativespecies was not significant (F1,27=2.34, p=0.14), andthe effect of substrate type alone was also notsignificantly different (F1,27=1.77, p=0.19). The sta-tistical results were qualitatively similar when T. crocea(the most abundant native species) was examinedindividually.

The second and third most abundant species acrosssubstrate types were the nonindigenous tunicates,B. violaceus and B. schlosseri, whose abundance

Fig. 4. Percent cover (±1 SE) of fouling organisms on all substratetypes in October 2004. Open bars indicate artificial substrate types andshaded bars indicate natural substrate types. A) Botrylloides violaceus,B) Botryllus schlosseri and C) all species combined.

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comprised 90% of total nonindigenous abundance. Theamount of space occupied by these two exotic speciessignificantly increased through time (Fig. 3, F1,27=41.56, p<0.0001) and their percent cover increasedsignificantly more on artificial than natural substratesthrough time (time by substrate type interaction:F1,27=7.18, p=0.012); substrate type alone was notsignificant (F1,27=1.60, p=0.22). Specifically, the twoexotic tunicates occupied similar amounts of space onartificial and natural substrates in September (8% and9%), and by October had increased to 16.5% on naturalsubstrates and to 36% on artificial ones (Fig. 3). Bo-trylloides occupied 45% of primary substrate on the PVCsubstrate in October (Fig. 4A), which was notably higherthan its abundance on any of the natural substrate types(maximum was 17% on slate) and Botryllus was muchmore abundant on metal (21%, Fig. 4B) than on the othersubstrate types. Despite the strong increases in exotictunicate abundance on artificial substrates, the totalabundance of fouling organisms was similar betweennatural and artificial substrate types in October (Fig. 4C),because the increase in exotics on artificial substrateswas compensated by a decrease in native abundance(Fig 2).

4. Discussion

Our study focused specifically on substrate type as adeterminant of fouling community structure. We foundthat average species richness patterns did not differ as afunction of substrate type. Thus, in this system it appearsthat natives and exotics alike appear physiologicallycapable of settling on a variety of substrates. However, alarge difference was observed in the relative abundance

Fig. 3. Percent cover (±1 SE) of the nonindigenous tunicates Botryl-loides violaceus and Botryllus schlosseri on artificial and naturalsubstrate types. Open bars indicate artificial substrate types and shadedbars indicate natural substrate types.

of exotic and native species between the two substratecategories due to post-settlement processes (e.g. relativeadhesion strength, growth rates, and competition). Theexotic tunicates, Botrylloides and Botryllus, increaseddramatically on artificial substrates through time at theexpense of native species abundance, which declined. Incontrast, Botrylloides and Botryllus increased onlyslightly on natural substrates; native species on thesesame substrates did not change, indicating that the slightincrease in exotics was primarily due to their occupationof bare space. Exotic species were thus disproportio-nately enhanced on artificial surfaces, as predicted bythe SRM hypothesis. Our results are consistent withpost-settlement processes driving the observed patternand suggest that a lack of shared evolutionary history ofany species with artificial substrate types weakens po-tential competitive advantages of native species on suchsurfaces.

The abundance of native species was stronglydominated by T. crocea, which has an upright growth

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form in comparison with the prostrate form of the twononindigenous tunicates, Botrylloides and Botryllus.Obviously these growth form differences may affectrelevant, substrate-influenced properties such as adhe-sion and growth. While it might have been insightful tocompare natives and exotics with similar growth forms,we were primarily interested in species invasive statusas a contributor to their relative abundance on varioussubstrate types, and none of the native colonial (i.e.prostrate) tunicates of this region are common in foulingcommunities.

Certainly microtopographic differences existedbetween our substrate treatments. In part, we embracedthese differences because such properties are what makeeach substrate distinct. However we also standardizedfor these differences somewhat by using naturalsubstrates in slightly processed forms. For example,the wood, slate, and marble substrates were cut andsmoothed to expose a flat surface, thus their surfaceswere less rugose than they would be in nature, andtherefore more similar to (the typically smooth) artificialsubstrates. This reduction in microtopography of naturalsubstrates resulted in substrate surface characteristicsbeing more uniform between natural and artificialsubstrate treatments, which helped to isolate substratecomposition, per se as a major factor driving our results.

Coastal infrastructure such as pilings, buoys and floatsare often constructed of the artificial materials that weused in this experiment. We included PVC as an artificialsubstrate type because it is commonly utilized for foulingcommunity studies. Our study, like others (e.g., Ander-son and Underwood, 1994; Glasby, 2000), suggestscareful consideration of substrates used for experimentalpurposes. For example, Connell and Glasby (1999)reported differences in community structure betweenartificial substrates and natural rocky reefs in Sydney,Australia. They suggested that these artificial substratesare not surrogates for natural rock substrates, but ratherthey present a novel habitat type for fouling taxa. Smithand Rule (2002) similarly showed that assemblages ofmotile fauna recruiting to artificial surfaces were notrepresentative of adjacent natural communities. Particu-larly in the case of exotic species studies, it may behelpful to recognize that, relative to natural substrates,artificial substrates may result in unnaturally depressedabundance of native species and enhanced abundance ofinvasive tunicates and other exotic species. Not only doessubstrate type affect the performance of some types ofspecies, ubiquitous exotic species such as tunicates maydifferentially thrive on certain types of artificial sub-strates that are commonly used for ecological studies.Thus, in general, our results suggest that communities do

not just develop differently on artificial substrates, butthat the artificial substrates may be systematically biasedin their reflection of natural communities.

The ability of exotic tunicates to occupy and maintainsubstantial amounts of space on artificial substrateslikely contributes to their success in highly modifiedestuarine embayments. Human structures may attractand even promote nonindigenous species by differen-tially benefiting them. For example, in a thoroughsystem-wide assessment of Elkhorn Slough, CA, exoticspecies were heavily dominant on novel, hard substrates(Wasson et al., 2005). Similarly, the spread of theproblematic, newly identified tunicate Didemnumvexillum in New Zealand may have been facilitated byartificial substrates in the marine environment. Thistunicate attaches to a wide variety of substrate types andforms lobes than hang down from docks, wharves andboat bottoms. These lobes are easily dislodged by waveactivity allowing the tunicate to spread to the seafloorand other surfaces (A. Coutts, pers. comm.).

The patterns we documented focused on the twohighly abundant exotic tunicates, Botrylloides and Bo-tryllus. Many of the exotic and cryptogenic species inthis system were too sparse to provide necessaryresolution to determine if they exhibited the samerelative abundance patterns as these two nonindigenousascidians. However the power of the SRM prediction isin the aggregate prediction it makes for exotic species asa whole. We believe that species identity will always beimportant in establishing dominance; however, onartificial substrates, or in disturbed environments ingeneral, the SRM mechanism predicts that on averagethe identity of those species is increasingly likely to benonindigenous.

The communities we studied are annual and amajority of the species senesce every winter. If allowedto persist year-round, we believe the dominance byexotic tunicates on artificial substrates would have beengreater because of their high rate of increase right upthrough peak abundance and into senescence. Thus,highly modified embayments in milder climates thathave perennial fouling communities may have evenstronger skew to nonindigenous species. If true, theextension of this idea also has implications for globalclimate change. Specifically, warmer water temperaturesthat promote perennial community persistence may alsoenhance exotic species relative abundance (Stachowiczet al., 2002b). Rising ocean temperatures, in concertwith steadily increasing coastal and offshore infrastruc-ture, which often provides artificial and altered settlinghabitats, could lead to substantial increases in exoticfouling species.

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Fouling communities are an attractive choice formanipulation and testing of ecological hypotheses. Thedependence of these communities on substrate as habitatallows disturbances or habitat alterations to be easilyimposed. We chose a particular habitat alteration, na-mely the substitution of artificial settling surfaces fornatural ones, to ascertain how developing foulingcommunities are affected. We have demonstrated thatsystematic variation in community development pat-terns is based on the interaction of substrate type andnative and exotic status. However, further investigationinto the specific mechanisms behind the apparent loss ofadvantage for native species on artificial substrate typesis warranted. Nevertheless, to avoid contributing to thespread and proliferation of exotic species, coastalmanagers should consider limiting the amount ofsubmerged artificial substrates and avoiding destructionof naturally occurring hard substrates in coastal andestuarine habitats.

Acknowledgments

Support was provided by the Ford PostdoctoralFellowship at the Wells National Estuarine ResearchReserve to M.C. Tyrrell and from the Hubbard MarineEndowment to J. Byers. We especially thank A. Couttsfor the superlative support and observations aboutinvasive tunicates and their interactions with artificialsubstrates. This manuscript was greatly improved bycomments from B. Pister, C. terHorst, J. Dijkstra andtwo anonymous reviewers. [SS]

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