Journal of Experimental Marine Biology and Ecology 412 (2012) 126–133

Contents lists available at SciVerse ScienceDirect

Journal of Experimental Marine Biology and Ecology

j ourna l homepage: www.e lsev ie r .com/ locate / jembe

How the timing of predation affects composition and diversity of species in a marinesessile community?

Edson Aparecido Vieira, Luiz Francisco Lembo Duarte, Gustavo M. Dias ⁎Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas (UNICAMP), CP 6109, CEP 13083-970 Campinas SP, Brazil

⁎ Corresponding author at: Departamento de CiAmbiente, Instituto Três Rios, Universidade Federal RuWalmir Peçanha, 54, Centro, Três Rios-RJ, CEP: 25.881431854.

E-mail address: gmunizdias@gmail.com (G.M. Dias).

0022-0981/$ – see front matter © 2011 Elsevier B.V. Aldoi:10.1016/j.jembe.2011.11.011

a b s t r a c t

a r t i c l e i n f o

Article history:Received 31 January 2011Received in revised form 26 May 2011Accepted 15 November 2011Available online 12 December 2011

Keywords:AscidianBryozoanCompetitionIndirect effectsPost-settlement

Predation during the early life history stages, when organisms are susceptible to both biotic and abiotic fac-tors, is likely to have pervasive effects on community development. However, few studies have examined therelative importance of predation during early life-history stages on long-term community composition. Usinga sessile marine community, we conducted a manipulative experiment to measure the effect of timing andextent of predator exposure. Every month over a 5 month period we assessed taxa composition, dominanceand taxa richness in each of the following five treatments: 1) never predated, 2) always predated, 3) earlypredated (during the first month of community development), 4) late predated and 5) uncaged panels. Pre-dation was very important in determining taxa identity and dominance, reducing spatial monopolization byascidians and increasing the area occupied by bryozoans, but overall predation did not result in a more di-verse community. The localized extinction of ascidians in predation treatments was compensated by an in-crease in the diversity of bryozoans and barnacles. Interestingly, predation during the early stages ofcommunity development had only short-term effects on the taxa richness and composition. After 5 months,predator exclusion during the early life-history stages had no effect on community composition and only cur-rent levels of predation determined differences in composition. Our results show that predation can causechanges in community composition, directly and indirectly, without necessary changing the total numberof co-occurring taxa. More important, we demonstrate to our study system that although predation duringthe early life-history stages can be strong and have important short-term effects, predation during theadult stages determines long-term community composition.

© 2011 Elsevier B.V. All rights reserved.

1. Introduction

Predation is one of the most important forces shaping the distribu-tion, abundance and composition of species in aquatic and terrestrialcommunities (Hulme, 1996; Huntly, 1991; Menge and Sutherland,1976, 1987; Menge et al., 1986; Pacala and Crawley, 1992; Paine,1966, 1969). Selective predation on dominant species may allowpoorer competitors, otherwise excluded from the community, to set-tle in open space and survive, thereby increasing species richness(Brown and Heske, 1990; Connell, 1972, 1978; Hulme, 1996;McGuinness, 1987; Menge and Sutherland, 1976; Olofsson et al.,2008; Wulff, 2005). In other cases, however, predators drive shiftsin community structure by removing more vulnerable prey, thus fa-cilitating colonization by more resistant species (Karlson, 1978;Nydam and Stachowicz, 2007; Peters, 2007; Stoner, 1990). Therefore,predation effects on the composition of communities may be direct

ências Administrativas e doral do Rio de Janeiro, Rua Dr.02-180, Brazil. Tel.: +55 24

l rights reserved.

and indirect (Connell, 2001; Huntly, 1991; Maron and Vilà, 2001;McClanahan, 1997; Pacala and Crawley, 1992; Russ, 1980).

In general, studies examining the effects of predation on commu-nity composition have focused on interactions during the adult life-history stage. How predation during the early life-history stages af-fects the composition of communities is much less understood.Some studies suggest that predation during the early post-settlement period, when individuals are generally small and still un-able to defend themselves, can control the recruitment process anddetermine the abundance and distribution of populations indepen-dently of predation on adults (Gosselin and Qian, 1997; Green et al.,1997; Hunt and Scheibling, 1997; Osman and Whitlatch, 1995,1996, 1998, 2004; Young and Chia, 1984). In plant communities, forexample, selective seedling predation by mammals can have dramaticeffects on community succession, diversity and dominance (Howe,2008; Pacala and Crawley, 1992). In a similar way, predation by fishesand gastropods during the post-settlement period can trigger long-term effects on the species composition of encrusting assemblagesin marine habitats (Osman and Whitlatch, 2004; Osman et al., 1992).

In an opposite way, predation during the post-settlement stage,although intense, may not affect species richness and compositionwhen other processes, such as recruitment or competition, dominate

127E.A. Vieira et al. / Journal of Experimental Marine Biology and Ecology 412 (2012) 126–133

community dynamics or when predators are non-selective (Chesson,2000; Connell, 2001; Rey and Alcantara, 2000). For example,Andersen (1989) observed that in four long-lived perennial trees,mortality during the early life history stage was high, but not neces-sary important for recruitment because safe sites for adults wererare. Sams and Keough (2007) found no effects of predation overthe initial post-settlement period for a marine encrusting communityin Australia. The authors suggest that the high abundance of larvaemay swamp predation and account for the observed pattern. There-fore, the relative importance of predation during early and latesuccessional stages on the establishment of long-term patterns ofspecies diversity and composition may vary among communities.

In rocky subtidal habitats, space is a major factor regulating spe-cies abundance. The capacity for rapid asexual growth of many colo-nial ascidians, allows these organisms to overgrow competitors (e.g.barnacles, mussels, bryozoans and sponges) and dominate commu-nity assemblages by monopolizing space (Dias et al., 2008; Kayand Keough, 1981; Keough, 1984; Lambert, 2007). Interestingly,however, these organisms are more abundant in protected areas,where the risk of predation is low (Jackson, 1977; Kay andKeough, 1981), and studies suggest that predation during the post-settlement period may be an important factor limiting their distri-bution and abundance (Osman and Whitlatch, 2004). It is thereforepossible that predation during early life-history stages of ascidianswill have cascading indirect effects on the composition of subtidalcommunity assemblages by reducing spatial monopolization(Connell, 2001).In southeastern Brazil, Dias (2008) found thatchemical extracts of some ascidians can elicit a predation responseby fishes, suggesting that this process has an important influenceon the abundance and distribution of these clonal invertebrates,and may consequently have important implications for communitydynamics in this region. To test this hypothesis, we manipulatedpredation at different periods of community development andquantified the short and long-term effects of predation on taxa di-versity and composition of a subtidal encrusting community. Ashighlighted before, while some studies suggest that predationduring the post-settlement period may be especially important forcommunity organization, regardless of the intensity of predationon adult stages, other studies found weak or inexistent long-termeffects of predation during this period. Our data from communitiesexposed to predators at different stages of communitydevelopment allowed us to understand the relative importance ofpast and current predation on community diversity andcomposition.

2. Material and methods

2.1. Study location

We conducted this study at Praia do Segredo (23° 49′ 44″ S, 45°25′ 24″ W), within a few tens of meters from the facilities of the Cen-tre for Marine Biology of the University of São Paulo (CEBIMar-USP),São Sebastião, SP, southeastern Brazil. The beach is located in asmall bay, surrounded by boulders of different sizes that protect thearea against waves and wind. During the study, the rocky substratawere dominated by the zoanthid Palythoa caribaeorum (Duchassaing& Michelotti 1860) and several species of ascidians and sponges.Benthic-feeding fishes and invertebrate predators were frequentlyseen feeding over the boulders.

2.2. Experimental design and sampling protocols

We assessed the effects of predation on taxa assemblages develop-ing in 30 roughened PVC panels (22×22×0.3 cm). These panels weresuspended horizontally 2 m below the MLW and 2 m above the seabottom, spaced 30 cm from each other and fixed by cables to an

artificial mooring structure that was covered by several species of as-cidians, bryozoans and sponges. We performed all analyses using thedownward facing surface of each panel to avoid problems of sedi-mentation and algal growth. Since the manipulation of the panel dur-ing the sampling periods could affect the organisms growing in theborder of the panels, we just sampled the 10×10 central area ofeach panel. The absence of predators was simulated by placing stain-less steel mesh cages (0.5 cm mesh) over panels. Cage dimensionswere 22×22×6 cm allowing an unobstructed vertical growth of theorganisms while successfully excluding most of the potential preda-tors. Partially caged treatments were used as caging controls (Russ,1980). In this case, cages had the same dimensions of the completecages, but with two holes of 16×8 cm each on the roof of the cage.Snorkeling observations showed that open cages provided access ofcrabs, gastropods and fishes to the panels. The partially caged treat-ments allowed predators to access the organisms developing on thepanels but modified the water flow and light levels in a similar wayto complete cages for almost all organisms (Sams and Keough, 2007).

We initiated the experiment in October 2007, when the panelswere randomly assigned to one of the following treatments:1) “Uncaged panels” (UP): panels without any cage, allowing accessof predators during the whole experiment; 2)“Always predatedpanels” (AP): panels partially caged, allowing access of predators dur-ing the whole experiment and acting as a control of possible cage ef-fects; 3) “Never predated panels” (NP): panels completely caged andprotected from predators during the whole experiment; 4) “Latepredated panels” (LP): panels completely caged only during the firstmonth and partially caged during the rest of the experiment; and 5)“Early predated panels” (EP): panels partially caged during the firstmonth and then completely caged until the end of the experiment.Each treatment consisted of 6 replicates. Because the cage from onereplicate of the treatment NP was broken in the fifth sampling period,we removed this replicate from the analyses.

Monthly, from November 2007 to March 2008, we removed thepanels from the field and took them to the laboratory (a 2 min trip),where they were kept in running sea-water aquaria until processing.We scanned each panel under a dissecting microscope and identifiedall the encrusting organisms found, to the lowest possible taxonomiclevel. We then photographed the panels for later quantification of thearea covered by each taxonomic group, and returned the panels totheir original position at the field. After the last sampling, we pre-served the encrusting organisms in 70% alcohol for posterior confir-mation of the identified taxa.

Because colonial organisms, such as ascidians and bryozoanscould monopolize the settlement panels through clonal reproduc-tion, we used the area covered by each taxonomic group, insteadof the number of individuals, to estimate the relative abundance oftaxa. We quantified the area covered by the most abundant taxa(ascidians, bryozoans, oysters and barnacles) as percentage, on the100 cm2 central area of the panels, using a grid of 361 evenly spacedpoints, generated by the software Adobe Photoshop 7.0. Sponges(mean covered area=1.05%; SE=0.16) and sessile polychaetes(mean covered area=1.80%; SE=0.29) were grouped in the cate-gory “others” because they covered a small area during the wholeexperiment. In contrast, the area occupied by the cryptogenic ascid-ian Clavelina oblonga Herdman, 1880 (Rocha and Kremer, 2005)(mean covered area=42.93%; SE=2.08) was analyzed separatelyfrom the other ascidian species as it was the most abundant organ-ism on all the panels.

2.3. Statistical analyses

We examined differences in the area covered by each taxon of themain taxonomic groups in the five treatments, using a non-metricmultidimensional scaling (n-MDS) analysis (Clarke, 1993). We per-formed the test from a matrix (treatment replicates×percent cover

128 E.A. Vieira et al. / Journal of Experimental Marine Biology and Ecology 412 (2012) 126–133

of each taxon) using Euclidean distance among treatments and thesoftware PAST (Hammer et al., 2001). Each month was analyzed sep-arately. The n-MDS analysis provided a general overview of the dataand can be used for clarifying relationships among the treatments.To detect the differences among groups (treatments), established apriori in n-MDS, we used the ANOSIM test (analysis of similarity)(Clarke, 1993). The ANOSIM is a permutation test analogous to thestandard ANOVA (analysis of variance) that calculates the probabilityof random occurrence of the observed groups. The ANOSIM was per-formed using Euclidean distances after 200,000 permutations andBonferroni correction for multiple a posteriori comparisons. Weused the SIMPER test to detect which taxa were the most importantin establishing the separated groups (Clarke, 1993).

As an additional test to confirm the effects of predation on the taxarichness of encrusting organisms among treatments we used a two-way repeated measures ANOVA (Potvin et al., 1990) with time as awithin-subjects factor (repeated), and richness as the between sub-jects factors. Homogeneity of variance among cells was evaluatedusing Greenhouse–Geisser's and Huynh–Feldt's epsilon indices(Quinn and Keough, 2002). No departure of variance was observed.We performed the analyses using the software Systat 12.

Because ascidians are strong competitors but susceptible to preda-tion, we were interested in how predation could affect the relation-ship between the richness of ascidians and the richness of otherencrusting organisms. Thus, for each predation treatment we also ex-amined the relationship between the number of ascidian species andthe number of non-ascidian species in the community. We then test-ed for differences in the proportional abundance of ascidians amongtreatments using repeated measures ANOVA, after arcsin–squareroot transformation.

We did pairwise comparisons, with Scheffé post-hoc test forrichness and the proportion between ascidians/total richness. Be-cause we were interested in the short and long term effects ofpredation on the community organization, we used the data fromthe first and last sampling period of the experiment (30 and150 days). For richness pairwise comparisons we also used thedata from 90 days (when the largest difference among treatmentswas observed). Not to increase type I error, we performed theBonferroni adjustment of p critical value, considering as criticalvalue, p=0.025 for the proportion between ascidians/total richnessand p=0.017 for taxa richness.

3. Results

Ascidians were the most abundant and occupied the largest areain all treatments during most of the experiment. Colonial species,mainly C. oblonga, Didemnum perlucidumMonniot F., 1983, Didemnumpsammatodes (Sluiter, 1895), Trididemnum orbiculatum (Van Name,1902), Botrylloides nigrum Herdman, 1886 and Symplegma spp., cov-ered a larger area than solitary species, mainly Phallusia nigra Savigny,1816, Herdmania pallida (Heller, 1878),Microcosmus exasperatus Hell-er, 1878, Ascidia curvata (Traustedt, 1882), Ascidia interrupta Heller,1878 and Ciona intestinalis (Linnaeus, 1767). Barnacles, as Megabala-nus coccopoma (Darwin, 1854), Chthamalus sp. and Tetraclita stalacti-fera (Lamarck, 1818) and oysters (family Ostreidae) were present inthe beginning of the experiment while bryozoans, as Zoobotrium sp.,Bugula neritina (Linnaeus 1758), Catenicella uberrima (Harmer,1957), Savignyella lafontii (Audouin, 1826), Schizoporella sp. andworms (families Serpulidae and Sabellidae) were present during thewhole experiment. Hydrozoans and sponges were rarely observed.Fishes were the predators most frequently observed, mainlyAbudefduf saxatilis (Linnaeus, 1758), Stephanolepis hispidus (Linnaeus,1766) and Diplodus argenteus (Valenciennes, 1830). However, crabs,Microphrys sp., and gastropods, Cymatium parthenopeum (Von Salis,1793), were eventually seen feeding on the experimental exposedpanels. We rarely found small gastropods (mostly juveniles of C.

parthenopeum) and benthic fishes, Malacoctenus delalandii(Valenciennes, 1836) inside the complete caged treatments and theimportance of these small predators will be discussed.

In all tests performed, uncaged panels (UP) always provided sim-ilar results to the partially caged treatment (AP), indicating that cag-ing had no effects on the area covered by the major encrustinggroups. Thirty days after the start of the experiment, panels belongingto the five treatments formed two distinct groups regarding the areacovered by different taxonomic groups (ANOSIM: global R=0.54,pb0.001): panels exposed to predation were covered mainly by bar-nacles, while protected panels were dominated by ascidians, mainlyC. oblonga. The effects of predation during the post-settlement periodpersisted for 2 months in the field: after 60 days, panels exposed topredators during the first 30 days (UP, EP and AP) had similar com-munities, regardless of being protected (EP) or not protected (UPand AP) against predators between 30 and 60 days. The sameoccurred in panels protected from predators during the post-settlement period (LP and NP) (ANOSIM: global R=0.32, pb0.001)(Figs. 1 and 2).

After 60 days, there was a reduction in free space and in the spaceoccupied by barnacles on the settlement panels and a concurrent in-crease in the area covered by C. oblonga. At this moment, C. oblongadominated almost 70% of the substrate in panels protected from pred-ators during the first 30 days (NP and LP), but only 40% of the sub-strate on panels exposed to predators during the first 30 days (UP,AP and EP). Bryozoans showed an opposite pattern, covering a largerarea in panels exposed (25%) than in panels protected against preda-tors (10%). After 90 days, different groups were apparent (ANOSIM:global R=0.11, p=0.039), and divergences persisted after 120 days(ANOSIM: global R=0.43, pb0.001) and remained until the end ofthe experiment (ANOSIM: global R=0.46, pb0.001). At this momentpanels exposed to predators and panels protected from predators dif-fered in the taxa composition that made up communities, regardlessof exposure to predators during the first 30 days of experimentation.While predation reduced the area occupied by C. oblonga at the begin-ning of the experiment, it worked in an opposite way after 120 days.Predation after 120 days reduced the area occupied by others ascid-ians and bryozoans (Fig. 2) and consequently increased the areaoccupied by C. oblonga. The importance of C. oblonga for the organiza-tion of these species assemblages through the experimental time wasconfirmed by the SIMPER test (Table 1).

Panels protected and exposed to predation had a similar taxa rich-ness after 30 days in the field (Scheffé post-hoc test, p>0.05). The ex-posure of panels protected against predators only during the first30 days (LP) reduced the richness in the following 2 months to valuessmaller than that on panels that were always predated (AP). The op-posite pattern was observed when panels exposed to predators onlyduring the first 30 days (EP) were protected: richness increased inthe following 2 months to values higher than that on panels thatwere never predated (NP) (Scheffé post-hoc test, pb0.05 for90 days). However, these changes in the number of taxa did not per-sist and communities in all four treatments had the same taxa rich-ness after 150 days (Scheffé post-hoc test, p>0.05) (Fig. 3A). Whilepredation had only short-term effects on taxa richness, it determinedthe composition of taxa in the community. After 30 days, panelsexposed to predators had proportionally less species of ascidiansand more non-ascidian species such as, bryozoans, barnacles and oys-ters, than protected communities (Scheffé post-hoc test, pb0.05). Theonly exception was after 60 days, when panels from treatments LPand EP presented proportionally less species of ascidians than panelsnever predated (NP) but more species of ascidians than panels alwayspredated (AP). While the general pattern of more ascidian species inprotected panels seems to be maintained until the end of the experi-ment, after the 150 days the five treatments had similar ascidians/total community richness ratio (Scheffé post-hoc test, p>0.05)(Table 2) (Fig. 3B).

Fig. 1. Two-dimensional plot of area covered by each species of the main taxonomic groups analyzed by non-metric multidimensional scaling (n-MDS). Treatments: always pre-dated (diamond); never predated (square); late predated (circle); early predated (triangle) and uncaged panels (cross).

129E.A. Vieira et al. / Journal of Experimental Marine Biology and Ecology 412 (2012) 126–133

4. Discussion

Overall, our data suggest that predation had no long-term effectson the number of taxa, but was very important in determining taxacomposition in these assemblages: ascidians dominated panels pro-tected against predators but were less abundant in panels exposedto predation, as also shown by Osman and Whitlatch (2004). Preda-tion is considered an important mechanism that maintains high bio-logical diversity by limiting population abundance below levels atwhich individuals compete for resources, and may thereby promotecoexistence (Chesson, 2000; Lubchenco, 1978; Paine, 1966), especial-ly in physically stable environments, such as subtidal environments(Menge, 1992; Menge and Sutherland, 1976). Because ascidians arestrong spatial competitors (Bullard et al., 2007; Dias et al., 2008;Nandakumar et al., 1993; Russ, 1982) but are susceptible to predation(Osman and Whitlatch, 2004; Sams and Keough, 2007), we expectedthat partial removal of those organisms by predators would result inan indirect increase in the number species of other taxa, and

consequently an increase of overall richness. In agreement with thishypothesis, our results show that predation directly reduced thedominance of some species of ascidians, such as C. oblonga, increasingthe richness of bryozoans and others groups of encrusting organisms,however, predation seems to be strong enough to completely excludesome species of ascidians, resulting in no net increase of the total spe-cies richness. In this way, our data suggest that while predatedcommunities had overall diversity similar to protected panels, thecommunities in each habitat were fundamentally different. Consider-ing that sessile communities are exposed to different levels of preda-tion due to environmental heterogeneity, predation can result in alarge scale increase in ecosystem biodiversity.

Mortality during the early life stages is usually high in fishes(Searcy and Sponaugle, 2001), plants (Howe, 2008) and sessile or-ganisms (Stoner, 1990) because juveniles are more susceptible toboth abiotic and biotic disturbances than adults. Reviews byGosselin and Qian (1997) and Hunt and Scheibling (1997) listed themain causes of mortality during the early post-settlement stages for

Fig. 2. Mean cover percentage of the different encrusting groups (Ascidian Clavelina oblonga; others ascidians except C. oblonga; bryozoans; oysters; barnacles; sponges and hydro-zoans grouped as ‘other groups’) and free space, in the five different treatments and during the 5 months of experimentation. Treatment legends: NP = “never predated”, EP =“early predated”, LP = “Late predated”, AP = “always predated”, UP = “uncaged panels”.

130 E.A. Vieira et al. / Journal of Experimental Marine Biology and Ecology 412 (2012) 126–133

sessile marine organisms and concluded that predation is one of themain causes of juvenile mortality in the subtidal zone. Our resultssuggest that predation on juveniles of colonial organisms, duringthe first 30 days, reduced the monopolization of space by ascidiansand bryozoans, minimizing smothering and death of barnacles andoysters. In experiments carried out at the same site, Dias et al.(2008) demonstrated that D. perlucidum, one of the most frequent

ascidians in our study, overgrew barnacles and mussels in morethan 70% of border encounters, suggesting that competitive over-growth by ascidians is one of the major sources of mortality for soli-tary organisms in sessile communities in the area in early stages ofthe community development. We also observed small gastropodsand fishes on both protected and exposed communities. Predationof settlers by micropredators could account for part of the juvenile

Table 1Summary of the three taxa primarily providing the discrimination among treatmentsalong the sampled period (SIMPER analysis).

30 60 90 120 150

Clavelina oblonga 1st 1st 1st 1st 1stCatenicella uberrima 2nd 2nd 2nd 2ndSchizoporella sp. 2ndDidemnum perlucidum 3 rdBugula sp. 3 rdZoobotrium sp. 3 rdOysters 3 rd 3 rd

Table 2Repeated measures ANOVA examining the effect of exposure to predators on the rich-ness of encrusting organisms and on the proportion between richness of ascidians andtotal richness of the community.

Source Df MS F p

RichnessBetween subjects

Treatments 4 63.71 6,77 0.001Error 24 9.41

Within subjectsTime 4 29.44 6.22 b0.001Treatments×time 16 14.56 3.10 b0.001Error 96 4.73

Richness of ascidians/total richnessBetween subjects

Treatments 4 0.15 7.69 b0.001Error 24 0.02

Within subjectsTime 4 0.46 78.51 b0.001Treatments×time 16 0.02 3.30 b0.001Error 96 0.01

131E.A. Vieira et al. / Journal of Experimental Marine Biology and Ecology 412 (2012) 126–133

mortality, of both colonial and solitary organisms, as demonstratedfor the gastropod Strombus gigas in the Bahamas (Ray-Culp et al.,1999) and for encrusting communities at docks and marinas inNorth America (Nydam and Stachowicz, 2007; Osman et al., 1992),but is insufficient to explain the observed differences of species com-position between protected and predated communities in our study.

Osman andWhitlatch (1995, 1996, 1998, 2004), showed that preda-tor–prey interactions during the post-settlement period can have long-term effects on the subtidal encrusting community composition in thenortheastern coast of North America. Sams and Keough (2007) in a sim-ilar study conducted in southeastern Australian, found contrary results:predation during post-settlement period was not important for the or-ganization of the community. Differences in the relative importance of

Fig. 3. A) Total richness of species in the community and B) proportion between rich-ness of ascidians and total richness of species in panels of the five different treatmentsalong the 5 months of experimentation. Data are mean±standard error. For codes seelegend of Fig. 2.

predation between North American and Australian communities wereattributed to lower abundance of predators and/or higher recruitmentin the study by Sams and Keough (2007).We observed that, as predictedby Osman andWhitlatch (1995, 1996, 1998, 2004), predation during thepost-settlement stage affected the development of the communities, re-ducing the diversity and dominance of ascidians at this Brazilian site.However, in contrast to previous studies, we found no long-term effectsof predation on species richness. Significant effects of predation wereonly observed during the first 2 months of the experiment, after whichtaxa richness in predator exclusion and predator access treatments coa-lesced and taxa composition was determined by current levels of preda-tion in the community, independently of being or not exposed topredators during the initial colonization stage. During the first month,the amount of free space is still large (~20%) and recruitment is an im-portant process, being deeply affected by predation, reflecting ourshort time result. After 30 days, the colonial organisms begin to growfast and rapidly monopolize almost the total space (available freespace is less than 10%), so recruitment, while still occurring, becomeless important and the current predation on adults is responsible forthe long time results. The high density of encrusting organisms andlow amounts of free space observed during the first 30 days of the ex-periment (ranging from 30 to 80 animals per cm2; unpublished data)suggests that recruitment in our study area was high, and, as proposedby Sams and Keough (2007), could swamp predation effects in a shortperiod of time. High recruitment could lead to predator satiation andmay explain why early predation in this study did not affect speciescomposition, dominance and richness on later successional stages.

The ability to outcompete native species andhigh resistance to preda-tion are fundamental traits that allow invasive species to colonize newareas. Because invasive species are often free of co-evolved predators,predation is usually considered weaker on invasive than native species.However, if we consider the effects of generalist predators, such as themain species of fish observed in our study (Ferreira et al., 2004), whetherpredationwill facilitate or inhibit invasion depends on the relative palat-ability of introduced and native species (Maron and Vilà, 2001). At theend of our experiment, five individuals of the ascidian C. intestinaliswere observed in protected panels. This species has not been registeredon the Brazilian Coast since 1998, but is one of the most common inva-sive ascidians around theworld, often observed inmussel farms,marinasand harbors. The presence of this invasive species only on protectedpanels supports the hypothesis that predation can limit the success of in-vasive species. However, as discussed above, predation can also have in-direct effects on communities and promotes the successful invasion ofsome species. For example, Osman and Whitlatch (2007) observed thatpredation on native ascidians increased the occurrence of the invasive

132 E.A. Vieira et al. / Journal of Experimental Marine Biology and Ecology 412 (2012) 126–133

ascidian Didemnum sp. by providing free space and reducing competi-tion. In our study, predation affected the abundance of the cryptogenicspecies C. oblonga differently, depending on the period in which preda-tion occurred (i.e. during early or late development stages). Predationin the first months of our study directly reduced the occurrence of C.oblonga increasing the area occupied by bryozoans. But after 5 months,predation indirectly increased the occurrence of C. oblonga by reducingthe area occupied by others ascidians, similar to results obtained byOsman andWhitlatch (2007). Didemnid ascidians constituted themajor-ity of the “other ascidians” group in this study; these species are domi-nant competitors, capable to overgrow other organisms andmonopolize large amounts of space on rocky shores (Dias et al., 2008;Russ, 1982). Therefore, while predation can be an important factor limit-ing the recruitment of invasive species, it can also play an opposite roleenhancing the abundance of invasive species by acting against strong na-tive competitors.

Overall, our results show that predation is an important processdetermining, directly and indirectly, the identity of species, but notdiversity, in a marine encrusting community. The interaction be-tween strong predation and high settlement resulted in a situationwhere predation during the post-settlement stage produced nolong-term effects on community composition and species domi-nance. We suggest that the relative importance of predation overdifferent stages of ecological succession depends on the relation-ship between predation strength and the magnitude of recruitmentrate. Additionally, our results suggest that predation can both facil-itate and inhibit species invasions, depending on the period that itoccurs and on the competitive hierarchy of native and invasivespecies.

Acknowledgments

The authors thank the staff at the CEBIMar-USP for field support, L.M. Vieira for the identification of bryozoans, F. D. Passos for the iden-tification of gastropods and oysters, F. Z. Gibran for the identificationof fishes and A. Flores, S. Hart, D. Aguirre-Davies and two anonymousreviewers for helpful suggestions on this manuscript. EAV thanksCNPq (Conselho Nacional de Pesquisa) for providing an undergradu-ate scholarship (PIBIC-UNICAMP) and GMD thanks CAPES for provid-ing a PhD scholarship. [RH]

References

Andersen, A.N., 1989. How important is seed predation to recruitment in stable-populations of long-lived perennials? Oecologia 81, 310–315.

Brown, J.H., Heske, E.J., 1990. Control of a desert-grassland transition by a keystone ro-dent guild. Science 250, 1705–1707.

Bullard, S.G., Shumway, S.E., Whitlatch, R.B., 2007. Effects of the colonial ascidianDidemnum sp a on cultured scallops with a comparison to other bivalves. J. Shell-fish Res. 26, 1296–1297.

Chesson, P., 2000. Mechanisms of maintenance of species diversity. Annu. Rev. Ecol.Syst. 31, 343–366.

Clarke, K.R., 1993. Non-parametric multivariate analyses of changes in communitystructure. Aust. J. Ecol. 18, 117–143.

Connell, J.H., 1972. Community interactions on marine rocky intertidal shores. Annu.Rev. Ecol. Syst. 3, 169–192.

Connell, J.H., 1978. Diversity in tropical rain-forest and coral reefs. Science 199,1302–1310.

Connell, S.D., 2001. Predatory fish do not always affect the early development of epi-biotic assemblages. J. Exp. Mar. Biol. Ecol. 260, 1–12.

Dias, G.M., 2008. Influência de interações bióticas na aptidão, abundância e defesa deascídias coloniais. PhD thesis. Universidade Estadual de Campinas, Campinas.

Dias, G.M., Delboni, C.G.M., Duarte, L.F.L., 2008. Effects of competition on sexual andclonal reproduction of a tunicate: the importance of competitor identity. Mar.Ecol. Prog. Ser. 362, 149–156.

Ferreira, C.E.L., Floeter, S.R., Gasparini, J.L., 2004. Trophic structure patterns of Brazilianreef fishes: a latitudinal comparison. J. Biogeogr. 31, 1093–1106.

Gosselin, L.A., Qian, P.Y., 1997. Juvenile mortality in benthic marine invertebrates. Mar.Ecol. Prog. Ser. 146, 265–282.

Green, P.T., O'Dowd, D.J., Lake, P.S., 1997. Control of seedling recruitment by land crabsin rain forest on a remote oceanic island. Ecology 78, 2474–2486.

Hammer, Ø., Harper, D.A.T., Ryan, P.D., 2001. Palaeontological statistics software pack-age for education and data analysis. Paleontologia Electronica 4 9 pp.

Howe, H.F., 2008. Reversal of fortune: plant suppression and recovery after vole her-bivory. Oecologia 157, 279–286.

Hulme, P.E., 1996. Herbivory, plant regeneration, and species coexistence. J. Ecol. 84,609–615.

Hunt, H.L., Scheibling, R.E., 1997. Role of early post-settlement mortality in recruitmentof benthic marine invertebrates. Mar. Ecol. Prog. Ser. 155, 269–301.

Huntly, N., 1991. Herbivores and the dynamics of communities and ecosystems. Annu.Rev. Ecol. Syst. 22, 477–503.

Jackson, J.B.C., 1977. Competition on marine hard substrata: the adaptative significanceof solitary and colonial strategies. Am. Nat. 111, 743–767.

Karlson, R., 1978. Predation and space utilization patterns in a marine epifaunal com-munity. J. Exp. Mar. Biol. Ecol. 31, 225–239.

Kay, A.M., Keough, M.J., 1981. Occupation of patches in the epifauna communities onpier pilings and the bivalve Pinna bicolor at Edithburgh, South Australia. Oecologia48, 123–130.

Keough, M.J., 1984. Dynamics of the epifauna of the bivalve Pinna bicolor: interactionsamong recruitment, predation, and competition. Ecology 65, 677–688.

Lambert, G., 2007. Invasive sea squirts: a growing global problem. J. Exp. Mar. Biol. Ecol.42, 3–4.

Lubchenco, J., 1978. Plant species-diversity in a marine inter-tidal community —

importance of herbivore food preference and algal competitive abilities. Am.Nat. 112, 23–39.

Maron, J.L., Vilà, M., 2001. When do herbivores affect plant invasion? Evidence for thenatural enemies and biotic resistance hypotheses. Oikos 95, 361–373.

McClanahan, T.R., 1997. Primary succession of coral-reef algae: differing patterns onfished versus unfished reefs. J. Exp. Mar. Biol. Ecol. 218, 77–102.

McGuinness, K.A., 1987. Disturbance and organisms on boulders: causes of patterns indiversity and abundance. Oecologia 71, 420–430.

Menge, B.A., 1992. Community regulation — under what conditions are bottom-up fac-tors important on rocky shores. Ecology 73, 755–765.

Menge, B.A., Sutherland, J.P., 1976. Species diversity gradients: synthesis of the roles ofpredation, competition and temporal heterogeneity. Am. Nat. 110, 351–369.

Menge, B.A., Sutherland, J.P., 1987. Community regulation — variation in disturbance,competition, and predation in relation to environmental-stress and recruitment.Am. Nat. 130, 730–757.

Menge, B.A., Lubchenco, J., Gaines, S.D., 1986. A test of the Menge–Sutherland model ofcommunity organization in a tropical rocky intertidal food web. Oecologia 71,75–89.

Nandakumar, K., Tanaka, M., Kikuchi, T., 1993. Interespecific competition among foul-ing organisms in Tomioka Bay, Japan. Mar. Ecol. Prog. Ser. 94, 43–50.

Nydam, M., Stachowicz, J.J., 2007. Predator effects on fouling community development.Mar. Ecol. Prog. Ser. 337, 93–101.

Olofsson, J., Mazancourt, C., Crawley, M.J., 2008. Spatial heterogeneity and plantspecies richness at dfferent spatial scales under rabbit grazing. Oecologia 156,825–834.

Osman, R.W., Whitlatch, R.B., 1995. Predation on early ontogenetic life stages and its ef-fect on recruitment into a marine epifaunal community. Mar. Ecol. Prog. Ser. 117,111–126.

Osman, R.W., Whitlatch, R.B., 1996. Processes affecting newly-settled juveniles and theconsequences to subsequent community development. Invertebr. Reprod. Dev. 30,217–225.

Osman, R.W., Whitlatch, R.B., 1998. Local control of recruitment in an epifaunal com-munity and the consequences to colonization process. Hydrobiologia 375 (376),113–123.

Osman, R.W., Whitlatch, R.B., 2004. The control of the development of a marine benthiccommunity by predation on recruits. J. Exp. Mar. Biol. Ecol. 311, 117–145.

Osman, R.W., Whitlatch, R.B., 2007. Variation in the ability of Didemnum sp. to invadeestablished communities. J. Exp. Mar. Biol. Ecol. 342, 40–53.

Osman, R.W., Whitlatch, R.B., Malatesta, R.J., 1992. Potential role of micro-predatorsin determining recruitment into a marine community. Mar. Ecol. Prog. Ser. 83,35–43.

Pacala, S.W., Crawley, M.J., 1992. Herbivores and plant diversity. Am. Nat. 140,243–260.

Paine, R.T., 1966. Food web complexity and species diversity. Am. Nat. 100, 65–75.Paine, R.T., 1969. A note on trophic complexity and community stability. Am. Nat. 103,

91–93.Peters, H.A., 2007. The significance of small herbivores in structuring annual grassland.

J. Veg. Sci. 18, 175–182.Potvin, C., Lechowicz, M.J., Tardif, S., 1990. The statistical analysis of ecophysiological

response curves obtained from experiments involving repeated measures. Ecology71, 1389–1400.

Quinn, G., Keough, M., 2002. Experimental Design and Data Analysis for Biologists.Cambridge University Press, New York.

Ray-Culp, M., Davis, M., Stoner, A.W., 1999. Predation by xanthid crabs on early post-settlement gastropods: the role of prey size, preys density, and habitat complexity.J. Exp. Mar. Biol. Ecol. 240, 303–321.

Rey, P.J., Alcantara, J.M., 2000. Recruitment dynamics of a fleshy-fruites plant (Oleaeuropaea): connecting patterns of seed dispersal to seedling establishment. J. Ecol.88, 622–633.

Rocha, R.M., Kremer, L.P., 2005. Introduced ascidians in Paranaguá Bay, Paraná, south-ern Brazil. Rev. Bras. Zool. 22, 1170–1184.

Russ, G.R., 1980. Effects of predation by fishes, competition, and structural complexityof the substratum on the establishment of a marine epifaunal community. J. Exp.Mar. Biol. Ecol. 42, 55–69.

133E.A. Vieira et al. / Journal of Experimental Marine Biology and Ecology 412 (2012) 126–133

Russ, G.R., 1982. Overgrowth in a marine epifaunal community — competitivfe hierar-chies and competitive networks. Oecologia 53, 12–19.

Sams, M.A., Keough, M.J., 2007. Predation during early post-settlement varies in impor-tance for shaping marine sessile communities. Mar. Ecol. Prog. Ser. 348, 85–101.

Searcy, S.P., Sponaugle, S., 2001. Selective mortality during the larval-juvenile transi-tion in two coral reef fishes. Ecology 82, 2452–2470.

Stoner, D.S., 1990. Recruitment of a tropical colonial ascidian: relative importance ofpre-settlement vs. post-settlement processes. Ecology 71, 1682–1690.

Wulff, J.L., 2005. Trade-offs in resistance to competitors and predators, and their effectson the diversity of tropical marine sponges. J. Anim. Ecol. 74, 313–321.

Young, C.M., Chia, F.S., 1984. Microhabitat-associated variability in survival and growthof subtidal solitary ascidians during the first 21 days after settlement. Mar. Biol. 81,61–68.