Shading Impacts by Coastal Infrastructure On

This article isprotected Allrights bycopyright. reserved. doi: 10.1111/1365-2664.12811 thisversionandthe between lead todifferences been through the copyediting, typesetting, and proofreading which may pagination process, forpublicati accepted This articlehasbeen [email protected] Mendonça, 144, Santos (SP), Brazil, 11070-102. Phone +551338783899. University São Paulo of (IMar/UNIFESP), Santos/SP, Brazil. RuaDr Carvalho de Corresponding author: (CEBIMar/USP),São Sebastião/SP, [email protected] Áurea Maria Ciotti, Center of Marine Biology, University of São Paulo Anglesey, United Kingdom. [email protected] Stuart Rees Jenkins, School Oceanof Sciences, Bangor University, Menai Bridge, André/SP, ABC (CCNH/UFABC),Santo Gustavo Muniz Dias, Centre Naturalof and Human Sciences, Federal University of [email protected] Brazil. André/SP, ABC (CCNH/UFABC),Santo of University André Luiz Pardal-Souza, Centre of Natural and Human Sciences, Federal Piggott Editor :Jeremy Article type Date:21-Sep-2016 Accepted Revised Date :01-Jun-2016 Received Date

Accepted ArticleShading impacts by coastal infrastructure onbiological communities from : 02-Sep-2016 :02-Sep-2016 : Standard Paper Paper :Standard Ronaldo Adriano Christofoletti, Marine Institute, Federal subtropical rocky shores on and undergone full peer review buthasnot review undergone fullpeer on and Brazil. [email protected] [email protected] Brazil. Version of Record. PleaseVersion cite thisarticle as This article is protected by copyright. All rights reserved. copyright. This articleis protectedby barnacles recruiting more in shaded habitats. decreased in abundance. Larval recruitment was also affected, with oysters and mesolittoral, oysters became more abundant in shaded conditions, while barnacles infralittoral fringe and no community replacement over aperiod of 220days. Inthe 4. locations.but notatall In asimilar way, thecommunity from the mesolittoral was also affected by shading from macroalgae in unshaded habitats to invertebrate filter-feeders in shadedones. smaller in shaded habitat. In the infralittoral fringe, we recorded ashift in dominance biomass and cover of macroalgae and the size of most sedentary grazerswere 3. macrobenthic community, biofilm biomass and larval recruitment. manipulative fieldexperiment todeterminethe effects of shadingon the by human constructions with thosein unshaded areas. then implementedWe a 2. have been poorly explored from an environmental impact perspective. affecting both productivity andcommunity organisation. However, studies of shading 1. Summary Running title: Artificial shading has been highlighted as an important human disturbance, Accepted Experimental manipulation of shading led to atotal loss of macroalgae from the Shading consistently affected the biological community ofrocky shores. The Article shaded areas in shores rocky subtropical on structure community compared We Effectshading of on biological communities

This article is protected by copyright. All rights reserved. copyright. This articleis protectedby decreasing energetic resour (e.g., 1994; reducing heatstress)(Williams Kon,Kurokura &Tongnunui 2010), Sunlight limitation can influence animal communities by affecting physical conditions environments (Fitzprack &Kirkman 1995; Quinn terrestrial radiation, thus disturbing thegrowth andbiomass production by autotrophs in both communities in natural ecosystems, through areduction in the incidence solar of Introduction disturbances, intertidal, larval recruitment, luminosity, macroalgae, port expansion. Key-words: of the Araçá Bay andsurrounding areas. consequent shadingwill negatively affect proposed expansion by suspended structures of the port of São Sebastião, as the promote sustainable coastal development. As aresult, we do not recommend the emphasises the importance of careful evaluations of artificial structures in order to in our study site in south-eastern Brazil, are potentially under-estimated. Our work shading by artificial coastal structures, such as those proposed in the port expansion shores and thusconsequences man-made structures on patterns and proc 5.

Accepted Article Synthesisapplications and Sunlightshading the affectsstructure and functioning ofbiological

(Williams, Messier & Kneeshaw 1999; Pagès Pagès 1999; &Kneeshaw Messier (Williams,

Araçá Bay, biofilm, filter-feeder invertebrates, grazers, human ces of herbivores (Hill,Ryon & Schilling 1995;Harley . demonstrateWe a clear impact of shading by artificial for coastalecosystem for functioning. arguethat We the biodiversity andecosystem functioning esses regulating biodiversity onrocky et al.

1997; Ruiz& Romero 2001). et al . 2003) and aquatic This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Acceptedand associated infrastructure (VanGils& commercial trade has increased the demand construction for or expansion ports of (Small &Nicholls 2003; NOAA 2004; EEA 2006). Intensification of international consumers (Glasby 1999; Takada 1999 increasing theoverall abundances of some filter-feeding invertebrates and mobile & also by and Miller Etter 2008) 2007; Blockley 2006; &Chapman Blockley the diversity the of community, by reducing macroalgae cover (Glasby 1999; hard substrates, ar autotrophs and alterations in thestructure of biological communities. Specifically on 2007) consistently show negative effects shadingof by artificial structures on (Able, Manderson &Studholme 1998) andhard substrates (Glasby 1999;Blockley Struck Articleoverlooked. Results derived from salt marshes (Sanger, Holland &Gainey 2004; addressed (Bulleri &Chapman 2010), their role in artificial shading hasbeen additional substrate provided by suchstructures onaquatic biodiversity hasbeen such asbridges, piers, wharfs, docks & Foster 2004). However, sunlight canalso beblocked by man-made structures, due to riparian vegetation (Beschta 1997) or macroalgae coverage (Clark, Edwards Saunders & Connell 2001; Blockley &Chapman 2006). 2002) and influencing larval recruitment of marine organisms (Thorson 1964; The accelerating urbanisation of coastal areas worldwidewell is recognised In both freshwater and marine environments, sunlight shading occurs naturally et al. et 2004), seagrass beds (Burdick & Short 1999; Shafer 1999), estuaries tificial shading has been associatedwith sh ; Blockley 2007;Miller&Etter 2008). and ports.Although the influence the of Klijn 2007; Hricko2012).

ifts inthe ifts Such projectsare struct ure and This article is protected by copyright. All rights reserved. copyright. This articleis protectedby (ii)reduces body size of sedentary grazers, owing tobottom-up controlAccepted from a hypotheses that shading (i) decreases abundance or biomass of primary producers; benthic community. Through adescriptive and manipulative approach, we tested the consequence we aimed to assess the effects shading of on the rocky intertidal disturbances, such plans would substantiallyrestrict sunlight tonatural habitats. As a other Bay. Among Araçá of 75% covering by pillars, suspended structure some debate,after it was proposedto avoid spot benthicfor biodiversity in theSouthwest Atlantic (Amaral hot bay isa small this However, S1). Bay (Fig. Araçá area, adjacent an of infilling through facilities port increase was to proposal initial The details). for Information Sebastião has been discussed for many decades (see Appendix S1in Supporting less attention than other sources of disturbance. shading, althoughArticle recognised, are potentially under-estimated and have received far However, in considering theimpacts of coastal development the effects of enhanced management (Bulleri &Airoldi 2005;Perkol over thepast decade, not only from an academic viewpoint, but as tools for coastal functioning biological of communities of natural ecosystems, has gained importance Quantifying thepotential effects of such urban structures on the organisation and 2005; Grech deterioration of air and waterquality (Darbra &Casal 2004;Gupta, Gupta &Patil biodiversity, contamination by toxic substa environment where they are installed and in nearby locations. Loss of habitat and usually great of magnitude and cause s On the north coast of São Paulo State, Brazil, theexpansion of the port of São et al. 2013) are some examples of potential impacts of ports. nces, introduction exoticof species and ‐ Finkel ubstantial disturbance tothenatural infilling of theinfilling bay of by a constructionof et al.

2012;Ferrario et al. 2010, 2015), and et al. 2016). This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepteddifferences in physical environment such as degree of wave exposure. Response shore were immediately adjacent to each other (separated by 20m) toavoid any approximately 50m horizontal distance was sampled in each habitat; these areas of under thestructure where no direct sunlight reached the substrate. An area of areas due to human-made structures. In the shaded habitat, we sampled the area three shores: (i) unshaded, naturally sunny Biological data were compared between two different habitats within each of the macroalgae (e.g., corticoid and turf forming algae) dominate the infralittoral fringe. invertebrates (e.g., barnacles, oysters and mussels) in the mesolittoral, while range for the sites is about 1.4 m. All shores are dominated by filter-feeding constructions (Fig. S1;Table S1), built atleast yearsfive before thestudy. Tidal rocky shoresSouthwest in the Atlantic that are partially shaded by man-made DESCRIPTIVE APPROACH ArticlemethodsMaterial and worldwide. development and policies for expansion of ports and man-made structures careful considerations shading of disturbance in discussions regarding sustainable biological communities the of rocky intertidal, supporting theimportance of the sunlightof shading on patterns and processes driving structure and functioning of consistent impacts, based on observational surveys andexperimental manipulation, communities through effects on autotrophs andonlarval recruitment. show We reduced and biofilm; th (iii)modifies In September 2014, a surveywas conducted in three subtropical sheltered e organisation of sessilemacrobenthice organisation of areas; and (ii) shaded,sunlight-restricted

specimens in each habitat on each shore. unshaded and shaded areas were performed onlywhen we obtained at least 50 longest length of the shell. Comparisons of body size consumers of between white background to facilitate counting an small body size, thelittorinids were collected and, photographed in the field on a per habitat) for mesolittoral was assessed through photography using quadrats of 100 cm² (n = 20 Echinolittorina lineolata subrugosa Sedentary grazers. ash free dry weight. weighed. The dry material was then burned at 500 This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted scraped clear and the macroalgae collected were dried at60 Articleareas of 100 cm² in the infralittoral fringe in both habitats on the three shores were shaded habitats. Macroalgal biomass was estimated by destructive sampling. Five haphazardly takenin the upper mesolittoral of each location in unshaded and supplementary materials for details). Ten images, each of 100 cm², were Underwood 2006; Murphy, method using digital photographs (adapted from Murphy Primary producers. sedentaryof grazers andsessile community organization. variables measured included the biomass of primary producers, population structure (d’Orbigny1846) in thelower mesolittoral and thelittorinid gastropods L. subrugosa Population structure of three benthic grazers - the limpet Biofilm biomass was estimated by afield-based remote sensing (d’Orbigny 1840) and and 25 cm² (n = 10 per habitat) for Underwood &Jackson2009; see Appendix S2in d measurement. Size was defined as the Littoraria flava

o C4h for and wecalculated the (King 1832) in the upper et al.

littorinids. Due to the 2005; Murphy 2005; & o C for 24h and and 24h C for Lottia This article is protected by copyright. All rights reserved. copyright. This articleis protectedby perimeter. Although partial shading (diffuse light) is anatural consequence of many Acceptedcentral 100 cm² for analyses, to avoid artefacts caused by diffuse light atthe all the40x 40cmarea is under the influence of the treatment we only usedthe penetration to the substratum ( mimicking the physical structure of the shaded treatment but allowing sunlight each corner; (ii) procedural control, sheets (40 x 40 cm) suspended 10 cm above the substrate by stainless steel bars in was performed with three treatments: (i) shaded, constructed with marine plywood lasted 221 days in two intertidal zones (infralittoral fringe and upper mesolittoral) and within Araçá Bay (São Sebastião, São Paulo State, Brazil; Fig. S1). The experiment and community organization were conducted on the shore of Pernambuco island, MANIPULATIVE APPROACH Articleshading. habitats to test the hypothesis of a dominance shift in the infralittoral fringe due to functional groups ‘macroalgae’ and‘filter-feeding invertebrates’ between different the lowest possible taxonomic group. alsoWe compared the abundance of the Littler &Arnold (1982) and Littler, Litter & Taylor (1983). Other taxa were identified to intersection grids. Macroalgae were classified into functional groups, according to habitat) and taxa abundance estimated as percentage cover using 100 regular Samples were taken haphazardly through photography (100 cm², n = 10or 20 per de mesolittoral, upper and mesolittoral between unshaded and shaded habitats in three tidal zones: infralittoral fringe, lower Community organization. Experimental manipulations to test the effect of shading onbiofilm biomass Sessile macrobenthic communities were compared ≈ 90%); and (iii) control, unmanipulated areas. While areas. While unmanipulated (iii) control, and 90%); limited according to Christofoletti Christofoletti to according limited provided by transparent acrylic sheets,

et al. (2011). were replaced approximately every 30days.Inthelaboratory, we identified and treatments, avoiding central sampling area, and close toreplicates in control. Plates screwed in theupper mesolittoral, under theprocedural control andshaded This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Acceptedwith gray slip-resistant tape (3M covered x cm) (8 8 plates acrylic we utilized larval recruitment, on shading of effects Larval recruitment. space. macroalgae, oysters, the barnacle whole experiment, we tested how thetreatments affected the areas covered by tidal conditions. Because communities were dominated by a few species during the and, after 0,15,29, 75, 191 and 221 days intheinfralittoral fringe, asallowed by community composition was sampled on the same dates in the upper mesolittoral 0, 15, 29, 44, 73, 149, 191 and 220 days after the start of the experiment. Benthic remote sensing technique and protocols (Appendix S2). Samples were undertaken ArticleAppendix S3). reduced by shading, but did not differ between control treatments (more details in deployed on treatments atboth tide heights. Bothluminosity andtemperature were test the efficacy of manipulations, luminosity andtemperature sensors were regularly cleaned and damaged structures were replaced assoon aspossible. To treatments were randomly allocated within eachtidal zone. Acrylic plates were treatment in each intertidal zone. Replicates were separated by atleast 2 m and the shade expected following potential port expansion. deployedWe 5replicates of each artificial structures our manipulative approach intended to simulate the effect of full Biofilm biomass was evaluated in the upper mesolittoral using the same To test whether alterations in adult populations were linked to TM Chthamalus bisinuatus Safety-Walk, Minnesota, EUA). Plates were

(Pilsbry1916) and open This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Acceptedcommunities from different habitats within locations were performed by post-hoc PERMANOVA test (999 permutations) (Anderson2001). Comparisons of (fixed, 2levels: unshaded andshaded) and‘location’ (random, 3levels) using similarity matrix based on Bray-Curtis distance and compared between ‘habitat’ only in oneshore. homoscedasticity (Levene’s test), since we sampled this species in enough number cases. Body size of in these Ierrors type of probability increased for potential to the isdrawn attention and data, raw using was stillperformed procedure same the persisted, variances procedure and transformations were applied when needed. heterogeneousWhere specimens atone of the shores. Variance homogeneity was testedby Cochran’s lineolata Echinolittorina Article(random, 3levels). Specifically theanalysis for body of size of considering the factors ‘habitat’ (fixed, 2levels: unshaded and shaded) and ‘location’ macroalgae and filter-feeding invertebrates) were analyzed using factorial ANOVA, sedentary grazers andunivariate data from benthic community (combined ANALYSISDATA barnacles and oysters, the two most abundant taxa in the upper mesolittoral. treatment ontherecruitment rate (number recruits of per days in thefield) of quantified recruits under astereomicroscope. tested theeffectsWe time of and Data from the sessile macrobenthic communities were converted to a theIn descriptiveapproach, ecological parameters from primaryproducers, Littoraria flava , location had 2 levelswe as did not sample enough was compared through at-test after confirming

Lottia subrugosa and and This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted (mean ± SE: 1.01 ± 0.43 g) than in the unshaded habitat (8.33 ± 1.28 g) (Table 1). decreased the macroalgal biomass, which was about eight times lower in the shaded influence of man-made constructions (Table 1). On the other hand, shading Primary producers DESCRIPTIVE APPROACH Results approach were evaluated using a factorial ANOVA. ‘treatment’ and ‘time’ (random factor) on recruitment rate during the manipulative multiple comparisons of means for both statistical techniques. The effects of ArticleGeisser adjustment. Post-hoc Student-Newman-Keuls (SNK) test was used for assumption wasviolated, we corrected statistical significances with Greenhouse- Mauchly’s sphericity testwa covered by macroalgae, oysters, barnacle assess the differences between treatments through time on biofilm biomass, area contributed most to dissimilarity between habitats. visualization of data. SIMPER analysiswas applied to identity thetaxa which for was used (nMDS) scaling multidimensional Non-metric tests. pair-wise There was noinfluence of shading on biofilm biomass on shores under the In the experimental approach, repeated measures ANOVA was used to s appliedtoverifytime Chthamalus bisinuatus

autocorrelation. and open space. When this When invertebrates: F This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted(ANOVA, effect of ‘Habitat’, macroalgae: F invertebrate filter-feeders increased from 5% in unshaded to65% in shaded habitats 70% in unshaded habitat to 17% in shaded habitat. On the other hand, combined ‘Habitat x Location’ interaction: Table 2;Fig. 2). lower mesolittoral and oneshore in the upper mesolittoral (Post-hoc pair-wise test shading at all three shores, while the effect was significant on two shores in the community organization. Inthe infralittoral fringe, there was asignificant effect of Community organization interaction: Table 1; Fig. 1). Articleone rocky shore, was this effect shadeof significant (SNK ‘Habitat x Location’ abundance in unshaded areas (Fig. 1). However only for habitat (SNK ‘Habitat x Location’ interaction: Table 1). shaded habitat, although, 0.001) (Fig. 1). Grazers from of four the five sampled populations were smaller in the lineolata Echinolittorina Sedentary grazers In theinfralittoral fringe, cover combined of macroalgae decreased from about There was asignificant, although spatiallyvariable, effect of shading on There was ageneral trend across all three species at all shores for greater Shading affected body size ofthe limpet 1,54 1,54 = 491.84; (Table 1) and L. subrugosa P < 0.01). Macroalgae morphofunctional groups Littoraria flava in one the of localities was bigger in shaded Lottia subrugosa 1,54 1,54

(t-test, df = 121, t= 5.36, = 23,470.89; filter-feeding Echinolittorina lineolata and the littorinids littorinids the and , on P < This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Acceptedmonths, completely disappearing atday 221(SNK ‘Treatment xTime’ interaction: the experiment and quickly decreased in the shading treatment during the first 2 Community organization which might indicate divergence of the treatments over time (Table 3). experiment (Fig. 3). There was nosignificant interaction between treatment and time a consequence of the control being placed in time (Fig. 3). Although there was asignificant effect of treatment (Table 3), this was Biofilm biomass MANIPULATIVE APPROACH mesolittoral. Articlethe sessile communities from shaded and unshaded habitats in the upper an opposite pattern. These two species contributed 91% of the dissimilarity between abundant in shaded than in unshaded habitats, while barnacle the mesolittoral, communities shadedfrom and unshaded habitats atthis shore height. Intheupper pattern. These two species contributed 55% the of dissimilarity between the sessile in shaded than in unshaded areas, while shading (SIMPER: Table S2). In the lower mesolittoral, oysters were more abundant shaded and unshaded habitats, the relative abundance of organisms was affected by (SIMPER: Table S2). For both other zones, while thesame species occurred in combined were responsible morefor than 45% of dissimilarity between habitats In the infralittoral fringe, macroalgae covered almost 100% at the beginning of Biofilm biomass showed a high degree of variation among replicates and over Microeuraphia rizophorae Brachidontes plots of higherplots of NDVI atthestart the of

(De Oliveira 1940) was more Chthamalus sp. showed anopposite

bisinuatus showed This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Acceptedchanged, and the results were consistent both for descriptive andmanipulative body size of primary consumers, community structure and larval recruitment consequence of shading. Under shading disturbance, biomass of primary producers, with suchstructures and demonstrated through experiments that the changes were a showedWe important ecological changes on natural rocky substrates associated ecosystems by the addition of substrate (see Bulleri &Chapman 2010 review).for Discussion differone from another (SNK‘Time’: Table 4). bisinuatus Also, there was variation among sampling dates,with larger numbers of control than in shaded and procedural control (SNK ‘Treatment’: Table 4; Fig. 5). 5). For the barnacle Articlethe shaded treatment than in the control treatments (SNK ‘Treatment’: Table 4; Fig. Larval recruitment of the experiment (SNK ‘Treatment x Time’ interaction: Table 3; Fig. 4). decreased in abundance dueto shading, reaching acover about of 10%by theend was nochange in other treatments. Conversely, thebarnacle from 1.2% at the beginning of the experiment to 37.8% after 220 days, while there in theupper mesolittoral. Inthe shaded treatment, oysters increased in abundance Table 3, Fig. 4). Shading also affected the structure of the macrobenthic community Many studies have shown how artificial structures caninfluence local Larval recruitment rate was affected by shade. Oyster larvae recruited more in larvae recruiting in April/2015 than in all 5 months before, which did not Chthamalus bisinuatus , larval recruitment was smaller in the

Chthamalus bisinuatus C.

This article is protected by copyright. All rights reserved. copyright. This articleis protectedby throughout AraçáBay dep is common Acceptedsedimentation was an artefact theof shade structures, since sedimentation on rock in experimental plots (Airoldi 2003). It was notclear the extent towhich such potentially owing tohigh mortality of early settlers caused by sedimentation observed consequence of limited recruitment over the 220day experimental period, but also invertebrates was not observed following shade manipulation, possibly asa made structures, dominance shifted toward filter-feeding invertebrates. This shift to post-settlement mortality spores of and low growth (Goldberg &Foster 2002). limited areas (Clark, Edwards &Foster 2004; Blockey &Chapman 2006) dueto high habitats canalso be linked torecruitment, as macroalgae tend torecruit less in light- months. Differences in abundance of macroalgae between unshaded andshaded shade caused progressive loss of existing macroalgae, with total loss in about 6 macroalgae coverage andbiomass were low,while experimental manipulation of 2008). Surveys showed thatin areas shadedby human-made structures, Articleautotrophs survival Glasby (e.g., 1999;S macroalgae, expected since light restriction limits photosynthesis and may prevent vulnerable toshading. There was astrong negative influence of shading on communities found at the lower levels in the shore, suggesting that this zone is more under pressure from urbanization (Bulleri &Chapman 2010; Dugan results contribute quantitatively totheextensive debateon coastal management status of the organisms, asdiscussed below. Our observational andexperimental and biological processes such as competition, recruitment rates and physiological approaches. The changes in communities are likely explained by physical factors With the reduction in macroalgae in theinfralittoral zone affected by man- The results highlighted more pronounced changes in the intertidal hafer 1999; Blockley 2007; Miller&Etter ending on prevailingweather andsea

et al. 2011). This article is protected by copyright. All rights reserved. copyright. This articleis protectedby habitats is that grazer size is related to increased heat stress in sunny habitats, most locations. Another, non-exclusive hypothesis to explain bigger animals in sunny was notseen,our prediction ofnegative shade effects ongrazerswas confirmed at biofilm on shading of influence the Although 2011). Ciotti & Almeida (Christofoletti, whilegrazing pressures of bothtogether maskenvironmental influences shown that fast-moving grazers mask the effect sedentaryof grazers onbiofilm, manipulation did not exclude biofilm grazers. Previous work in thestudy region has & Cruz 2008;Coelho, Vieira &Serôdio 2009). Also, it is important tonote that our exposed to excess sunlight, due to photoinhibition or thermal stress (Serôdio, Vieira al. Biofilm biomass can increase due to shading or reduced sunlight regimes (Jenkins complex and system the influence light of still controversial. onitsdynamics is biofilm, but we found nosupport for this hypothesis. The intertidal biofilm is a Harley 2002),thatshading w 2008; Dafforn, Johnston &Glasby 2009). spread of exotic species (Bulleri& Airold bywhich urbaninfrastructure in port fa (Arenas establishment opening bare upof spaceandan enhanc Fredriksen 2009). An additional consequence of loss of turf macroalgae cover is the loss of macroalgae species and their associated fauna (Christie, Norderhaug & open bare space, there was aclear reduction in local biodiversity, considering the conditions. Whether shading leads todominance by filter feeding invertebrates, or to

Accepted 2001; Thompson, Norton &Hawkins2004) or showrestricted growthwhen Article We predicted, based on pr predicted,based on We et al. 2006). This shading may beanadditional mechanism ould have anegative effecton the intertidal epilithic evious observations ( i 2005; Vaselli, Bulleri& Benedetti-Cecchi cilities can facilitate the introduction and ed probability invasive of species

Hill, Ryon & Schilling 1995;Hill, Ryon &Schilling et This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted & (Bulleri to facilities port defences sea artificial from ranging constructions through biota of intertidal rocky shores. Coastlines worldwide are being increasingly modified settlement mortality and the development of adult populations. indicate the need to differentiate between effects of shade on settlement/ early post under shading. Such patterns, both in the natural environment and experiments shaded habitats. However, interestingly, theabundance of adult barnacles reduced upper mesolittoral in theshaded treatment and barnacle recruitment increased in shading may belinked tolarval recruitment. Oysters became more abundant in the changes in community organisation in the infralittoral fringe and mesolittoral following established shaded communities in the present study, supporting theconclusion that on seawalls. Such results are consistent with theabundance theseof taxa in recruitment some of filter-feeding invertebrates butreduced macroalgae recruitment ArticleConnell 2001). Blockley &Chapman (2006) showed that shading increased thus settling in light-limited habitats (Thorson 1964; Young &Chia 1984;Saunders & with many larvae of marine organisms exhibiting negative phototactic behaviour, choice atsettlement (Keough &Downes 1982); available lightan important is cue recruitment regime (Chapman &Blockley 2006). Many late-stage larvae show active & Gray 1999). (Chelazzi, metabolism higher Williams a due rate growth (Vermeij 1973; Tanaka, Duque-Estrada & Magalhães 2002) and also increasing whichwould select specimens with larger shells due to optimized water storage Our study shows the consequences shading of from artificial structures onthe Shading canalso promote differences between communities by changing the

potential impacts) across much of the bay, we do not recommend it. expansion plan, and, basedon the likelyshade effects (as well asmany other functioning. As aresult, we recommend that stakeholders carefully evaluate the ecosystem and biodiversity on effects negative major will have structure suspended of the port of São Sebastião, our results suggest that covering the bay with a this and other regions around the world. Specifically regarding theexpansion plans development and hence informs discussions regarding sustainable development, in impact of shading contributes to a wider view the of consequences of such et al. coastal sites threatened by development is a hot spot in marine biodiversity (Amaral influencing the dynamics of the pelagic environment. The Araçá Bay, like many other Shading is also predicted to increase filter-feeding invertebrate cover strongly reduction in primary production, carbon exchange andhabitat for associated fauna. cause substantial decreases in macroalgae cover onhard substrate leading to a sediment habitats and mangroves. Results indicate such a development would This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted Articleshaded area of approximately 1km by theproposal for expansion of the port of São Sebastião which would result in a support the same communities (Bulleri & Chapman 2004). Our studywas prompted Underwood 2007), and modify biodiversity, sinceartificial and natural habitats do not loss, addition or fragmentation of habitat (Chapman 2006; Goodsell, Chapman & Chapman 2010; Dugan 2010, 2015) supporting awide range of ecosystem services. Understanding the

et al. 2011). Such urban infrastructures alter landscape via 2 of theAraçá Bay, of impacting rocky shores, soft

This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Acceptedbiodiversidade, impactos e ameaças. A.C.Z.,Amaral, Migotto, A.E., A. Turra, Oceanography and Marine Biology: an Annual Review Airoldi, L.(2003) The sedimentation of effects on rocky coastassemblages. lower Hudson river. water juvenile in fishes anurban estuary: theeffects manmadeof structures in the Able, K.W., Manderson, J.P.&Studholme, A.L. (1998) Thedistribution shallow of References (Pardal-Souza Figshare- Dataarchived https://dx. in - Study sites locations: uploaded as online supporting information (Table S1). ArticleData accessibility their valuable comments on the manuscript. figures, and to M.O. Tanaka, G.H.Pereir work. Finally,we grateful are to Isabella and A.C.Z Amaral for help with some Deborah, Jaqueline, Gabriella, Neemias, Ivan, Elso and Joseilto for support with field R.A.C. (#2013/11594-9) andto Biota Araçá Project (#2011/50317-5). thank We This workwas supported by research funds granted by SãoPaulo Research Foundation (FAPESP) toA.L.P.S (#2013/19122-9), to A.M.C (#2013/50199-8), to Acknowledgments et al. Estuaries 2016). , 21 , 731–744. Biota Neotropica & Schaeffer-Novelli, & a-Filho andthe anonymous referees for doi.org/10.6084/m9.figshare.3205285.v2

, , 41 10 , 161–236. , 219–264. Y. (2010) Araçá: This article is protected by copyright. All rights reserved. copyright. This articleis protectedby driver change of in marine environments. AcceptedBulleri, F. & Chapman, M.G. (2010) The introduction of coastal infrastructure as a habitats in marinas on the north-west coast of Italy. Bulleri, F.& Chapman, M.G. (2004) Intertidal assemblages on artificial and natural Sea. non-indigenous green alga, Bulleri, F.&Airoldi,L.(2005) Sydney Harbour, Australia. Blockley, D.J. (2007) wharves of Effect onintertidal assemblages onseawalls in Series between assemblages onshaded or unshaded seawalls. Blockley, D.J.&Chapman, M.G. (2006) perspective. Beschta, R.L. (1997) Riparian shadeand stream temperature: analternative ArticleMarine Biological Association of the United Kingdom rapid assessment survey marinas of onthe southcoast of England. J.S., S. Ward, & C.A.Wood, (2006) Alien species and other notable records from a D.J., Jacobs, Lambert, M.W., C.,Lambert, G. Arenas, F., Bishop, J.D.D., Carlton, J.T., Dyrynda, P.J.,Farnham, Gonzalez,W.F., variance. Anderson, M.J. (2001) Anew method for non-parametric multivariate analysis of São Paulo. Novelli, Y. (2015) Amaral, A.C.Z., A.,Ciotti,A.M., Turra,

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Marine Biology

, 86 , 1329–1337. Marine Ecology Progress , 63 , in the north Adriatic , 409–427. , 145 , , 1stedn. Lume, 47

Journal ofthe , 381–391. , 26–35. This article is protected by copyright. All rights reserved. copyright. This articleis protectedby promote marine invader dominance. AcceptedDafforn, K.A., Johnston, E.L. &Glasby, T.M. (2009) Shallow moving structures methods. photosynthetic activity of intertidal microphytobenthos biofilms as studied by optical Coelho, H., Vieira, S. &Serôdio, J.(2009) Effects desiccation of onthe 107–119. canopies on an understory algal assemblage. Clark, R.P., Edwards, M.S. &Foster, M.S. (2004) Effects shade of from multiple kelp Association of the United Kingdom a subtropical area of thesouth-west Atlantic. and temporal variation sedentary of consumers andsessile organisms onshores of Christofoletti, R.A., Takahashi, C.K., Oliveira, D.N. & Flores, A.A.V. (2011) Spatial Ecology Progress Series influence on spatial variability interti of ArticleChristofoletti, R.A., Almeida, T.V.V. &Ciotti, A.M. (2011) Environmental and grazing fauna. Christie, H., Norderhaug, K.M. &Fredriksen, S. (2009) Macrophytes as habitat for Association of the United Kingdom limpet, atropical in rate heart of Chelazzi, G., G.A. &Gray, D.G.Williams, Molluscan Studies Chapman, M.G. (2006) Intertidal s coastal waters of Massachusetts. Burdick, D.M.& Short, F.T. (1999) The effects of boat docks on eelgrass beds in Marine Ecology Progress Series Journal of Experimental Marine Biology and Ecology , 72 , 247–257. , 424 , 15–23. Environmental Management , , 79 Cellana grata 91 Biofouling eawallsas habitats formolluscs. dal biofilm on subtropical rocky shores. , 749–751. , 961–967. , 396 (1999) Field and labor , 221–233. Marine Ecology Progress Series , 25 . Journal ofthe Marine Biological , 277–287. Journalof theMarineBiological

, , 23 381 atory measurement , 231–240. , 98–104. Journal of Marine Marine , 267 , This article is protected by copyright. All rights reserved. copyright. This articleis protectedby H., Neil, K.,Pressey, R.L., Rasheed, M.A., Sheaves, M. &Smith, A. (2013) Guiding AcceptedGrech, A.,Bos, M.,Brodie,J.,Coles, R Ecology Progress Series in anthropogenically fragmented habitats and in naturally patchyhabitats. Goodsell, P.J.,Chapman, M.G. &Underwood, A.J.(2007) Differences between biota of Experimental Marine Biology and Ecology alga coralline geniculate the of abundance the Goldberg, N.A. & Foster, M.S. (2002) Settlement and postsettlement processes limit Experimental Marine Biology and Ecology Glasby, T.M. (1999) Effects shading of onsubtidal epibiotic assemblages Australia. and survival seagrass of Fitzpatrick, J.& Kirkman, H. (1995) Effects prolongedof shading stress on growth habitats. Article marine ofartificial performance ecological the in controlling factors biotic of role Ferrario, F., Iveša, L., Jaklin, A., Perkol-Finkel, S. & Airoldi, L. (2016) The overlooked OPOEC, Luxembourg. EEA (2006) D.S. McLusky), pp. 17-41. Academic Press, Waltham. nearshore structures. Estuarine andcoastal structures: environmental effects, a focus onshore and Dugan, J.E.,Airoldi,L.,Chapman, M Science Darbra, R.M. &Casal, J.(2004) Historical analysis accidents of in seaports. ,

Journal of Applied Ecology 42 Marine Ecology Progress Series Progress Ecology Marine , 85–98. The changing faces of Europe’s coastal areas Treatise onEstuarineCoastal andScience , 351 Posidonia australis , 15–23. , 53 , 16–24. 16–24. , ., Dale, A.,Gilbert,R.,Hamann, M.,Marsh, .G., Walker, S.J.&Schlacher,.G., Walker, (2011) T. , , 234 127 , 278 , 275–290. Calliarthron , 279–289. in Jervis Bay, New South Jervis in South Bay, New Wales, , 31–45.

onsubtidal walls. . EEA Report 6/2006. (eds E. & Wolanski . Journal of Journal Marine Marine Safety Safety This article is protected by copyright. All rights reserved. copyright. This articleis protectedby AcceptedBiologyEcology and mangrove vegetation on abenthic faunal community. Kon, K., Kurokura, H. &Tongnunui, P. (2010) Effects of the physical structure of active larval choices and early mortality. Keough, M.J. &Downes, B.J.(1982) Recruitment of marine invertebrates: the role of Progress Series variability grazing inlimpet ac Thompson, R.C. & Hartnoll, R.G. (2001) European-scale analysis seasonal of Hawkins, S.J.,Kay, S.,Martínez, B., Oliveros, J.,Roberts, M.F., Sousa, S., Jenkins, S.R., Arenas, F., Arrontes, J., expansion. Hricko, A.(2012) Progress &Pollution: Port cities prepare for the Panama Canal 1309. Articleecosystem: responses by primary producers andconsumers. Ryon, M.G.&Schilling, E.M. Hill, W.R., Oceanography abundance in ahigh rocky intertidal community during thewinter. Harley, C.D.(2002) Light availability i 141. port and harbour projects. Gupta, A.K., Gupta, S.K. &Patil, R.S. (2005) Environmental management plan for Reef. Barrier principles theimprovedfor governance of port andshipping impacts in theGreat

Environmental Health Perspectives Marine Pollution Bulletin Pollution Marine , , 47 211 , 1217–1222. , , 193–203. 383 , 171–180. Clean Technologies and Environmental Policy tivity andmicroalgal abundance. , 75 Oecologia , 8–20. ndirectly herbivore limits growth and Bussel, J.,R.A., J., Castro, Bussel, Coleman, (1995) Light limitation inastream , 120 , , 470–473.

54 Journal ofExperimental Marine , 348–352. Ecology Marine Ecology Limnology and , 76 , , 1297– 7 , 133– This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted2741–2750. indirect effects shadeof on four forest tree seedlings in the French Alps. Pagès, J.P., Pache, G., Joud, D.,Magnan, Office Special Projects. Trends Report Series. NOAA’s National Ocean Service Management and Budget NOAA (2004 Journal of Experimental Marine Biology and Ecology rocky shores. on microalgae epilithic investigate to new methods spectrometry: Murphy, R.J., Underwood, A.J.,Pinkerton, M.H. &Range, P.(2005) Field cameras. Journal intertidalof epilithicchlorophyll: techniq Murphy, R.J.,Underwood, A.J. & Jackson, A. Experimental Marine Biology and Ecology Articleto test hypotheses about grazing by intertidal herbivorous gastropods. Murphy, R.J. &Underwood, A.J.(2006) Novel use of digital colour-infrared imagery the rocky subtidal Gulf Maine.of in sessile invertebrate R.J.&Etter,dominance R.J.Miller, Shading (2008) facilitates Phycology barrier reef system: functional-form groups of marine macroalgae. Littler, M.M., Littler, D.S. & Taylor, P.R. (1983) Evolutionary strategies in atropical 307–311. functional-form groups from Southwestern North America. Littler, M.M. & Arnold, K.E. (1982) Primary productivity of marine macroalgal , 19 ) Population trends along the coastal United States: 1980-2008 , 229–237. of Experimental Marine Biology and Ecology Ecology ues using specialized and conventional digital , , 89 330 , 452–462. N.&Michalet, R. (2003) Directand C. (2009) Field-bas , 437–447.

, 325 , 111–124. JournalPhycology of , 380 ed remotesensing , 68–76. Ecology Journal of Journal of . Coastal , ,

18 84 , , This article is protected by copyright. All rights reserved. copyright. This articleis protectedby AcceptedPerdido Bay, Alabama. Shafer, D.J. (1999) The effects dockshadingof ontheseagrass chlorophyll fluorescence. photoinhibition in intertidal microphytobenthos asstudied Serôdio, J., Vieira, S. & Cruz, S.(2008) Photosynthetic activity, photoprotection and 115. orientation on the recruitment of spirorbid polychaetes. Saunders, R.J. &Connell, S.D. (2001) Interactive effects shadeof and surface Management shading on Sanger, D.M., Holland, A.F. & Gainey, C. (2004) Cumulative impacts dockof 107–120. Mediterranean seagrass ArticleRuiz,Romero, J.M. & J.(2001) Effects of Zealand Journal of Marine and Freshwater Research stream periphyton and invertebrates: An experiment in streamside channels. Quinn, J.M., Cooper, A.B., Stroud, M.J. & Burrell, G.P.(1997) Shade effects on coastal infrastructures. challenges in urban seascapes: promoting thegrowth of threatened species on Perkol https://dx.doi.org/10.6084/m9.figshare.3205285.v2 communities subtropicalfrom rockyfigshare. shores. Pardal-Souza, A.L.(2016) Shading impacts by coastal infrastructure onbiological ‐ Finkel, S.,Ferrario, F.,Nicotera, V.&Airoldi, L.(2012) Conservation , Spartina alterniflora 33 , 741–748. Journal ofAppliedEcology Estuaries Posidonia oceanica Continental Shelf Research , 22 in South Carolina estuaries. , 936–943. . Marine Ecology Progress Series in situ in , 49

, , experimental shading onthe , 1457–1466. 31 28 , 665–683. , 1363–1375. Austral Ecology in situ Halodule wrightii using variable Environmental , 26 , 109– , New 215 in , This article is protected by copyright. All rights reserved. copyright. This articleis protectedby strategies and their limitations. AcceptedVermeij, G.J. (1973) Morphological patterns in high-intertidal gastropods: adaptive Research as habitats for native and exotic rocky-bottom species. Vaselli, S.,Bulleri, F.&Ben decision making. Rotterdam harbour expansion. Connecting decisions, arenas and actors in spatial case the making: Gils, M. of The Van Complexity& Klijn, decision in E.H. (2007) larvae ofmarine bottom invertebrates. Thorson, G. (1964) Light as an ecological factor in the dispersal and settlement of 1372–1382. control regulate the producer-consumer balance in intertidal biofilms. Thompson, R.C., Norton, T.A. & Hawkins, S.J.(2004) Physical stress andbiological along awave exposure gradient. Articleacmaeid limpet Tanaka, M.O., Duque-Estrada, T.E. &Magalhães, C.A.(2002) Dynamics the of 189 organisms onawarm temperate boulder shore. Takada, Y. (1999) Influence of shade and number of boulder layers onmobile structure and function. Effects of bridge shading on estuarine marsh benthic invertebrate community Struck, S.D., Craft, C.B., Broome, S.W., Sanclements, M.D. &Sacco, J.N. (2004) zones. Small, C. & Nicholls, R.J. (2003) Aglobal analysis of human settlement in coastal , 171–179. Journal of Coastal Research , 66 , 395–403. Collisella subrugosa Collisella Planning Theory & Practice Environmental Management edetti-Cecchi, L. (2008)Hard Marine Biology Journal of Molluscan Studies , and vertical distribution of size and abundance 19 Ophelia , 584–599. , , 8 , 20 , 139–159. 1 , 167–208. , 319–346. Marine Ecology Progress Series ,

34 , 99–111. coastal-defence structures Marine Environmental , 68 , 55–64. Ecology , 85 , , This article is protected by copyright. All rights reserved. copyright. This articleis protectedby habitats. AcceptedTable S2. Table S1. expansion. Figure S1. Appendix S3. Appendix S2. expansion of port of São Sebastião. Appendix S1. Additional Supporting Information may be found in the online version of this article: ArticleSupporting Information Biology growth subtidal of solitary ascidians during the first 21 days after settlement. Young,F.S. ( C.M.&Chia, Experimental Marine Biology and Ecology structuring communities onamoderately-exposed tropical rockyshore. G.A.(1994)Williams, relationship between The shadeand molluscan grazing in lodgepole pine sapling size onthegrowth andcrown morphology understory of Douglas-fir and H., Messier, Williams C. &Kneeshaw D.D. (1999) Effects of light availability and , 81 Details study of sites. SIMPER analysis biological of communities in shaded and unshaded , 61-68. , 61-68. Map of study sites and representation of port of São Sebastião Details on measuring physical data. . Canadian Journal of Forest Research History of alterations in the Araçá Bay andjudiciary the statusof Methodological details for estimating biofilm biomass. 1984) Microhabitat-asso , 178 , 79–95.

ciated variabilityin survival and , 29 , 222–231. Journal of Marine Marine oain=L 1.2 00708 1 81 .1 0.30 38.18 3.61 1 Grazers Cochran’s 0.027 0.89 abundance 34.66 Error 3.28 0.32 1 H*L 11.52 test 1066 0.001 Location 0.03 0.25 0.78 1 0.97= 1 L 416.12 Habitat 2 0.529.77 C = 1 H 2.92 0.06 606 42.56 Grazers 0.024 = 0.88 Cochran’s 0.49 16.92 2 *** 0.05 body 4.02 137.25 Error 2 1 **0.51 10.55 1 H*L test 3.84 0.20 54 Location size 0.16 0.72 0.008 11.95 0.094 = (***) Habitat 0.004 L C = 2 Biofilm 24 1 H *** C Primary 0.11 = biomass Macroalgae = producers 0.47 biomass 0.39 (***) (***) C = 0.45 (ns) * 1 2.0 33 .7 2 0.90 9.79 *** 2 3.37 0.07 423.20 Cochran’s 2.99 3.30 0.23 1 1.97 2.17 0.28 Error 2 1 H*L test 0.14 0.76 76 Location 5.26 0.26 125.46 61.25 = Habitat 2,226.05 L C = 1 1 H 54 0.09 = 0.47 (***) C = 0.28 (ns) This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted ArticleEffect df MS F 0.001; ns = not significant. §Data transformed toln (x +1) producers and sedentarygrazers onsubtropical rocky shores. ** Table 1. TABLES Effect of habitats (unshaded and shaded) (2-way ANOVA) onprimary L. L. subrugosa E. lineolata L. subrugosa E. lineolata P df df MS F

§ P

< 0.01; ***

P < 0.40 0.80 5.31 *** 1.44 0.16 t oain=L 160 .6 * 2 ,2.0 147.30 1,521.10 t (c) 2 (a) Location *** Upper Pair-wise Infralittoral 54 mesolittoral tests 7.36 17.91 Error fringe *** ‘unshaded’ 54 156.02 2 H*L (b) 240.12 21.17 *** 2 2 177.87 2 =Location L Lower 376.64 114 13.41 0.60 1,102.40 8.40 Habitat 1 mesolittoral *** 21.03 150.98 (c) *** (a) = 2 *** 252.02 0.63 Upper Infralittoral H 0.57 26.06 mesolittoral 1 315.96 fringe (b) 1.77 0.24 Lower 1 138.69 mesolittoral 0.55

This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted Article Effect df MS Pseudo-F All data was transformed to arcsine ( macrobenthic communities ondifferent zonation ranges in subtropical rocky shores. Table 2. RS3 3.30 RS2 *** 3.43 4.69 RS1 *** *** 3.06 4.84 *** *** 1.02 0.36 P df MS Pseudo-F Effects habitats of (unshaded and shaded) (PERMANOVA) onsessile P P

t ) +1.*** P P P

df MS Pseudo-F < 0.001 <0.001

vs. ‘shaded’inside P

Error Error Tr*Ti 60 Time 0.03 10 Error 0.34 0.03 Treatment = 12 10.64 Macroalgae0.09 Infralittoral = Ti *** 0.08 5 0.01 0.98 0.32 0.05 4.10 ** fringe Error Tr 2 5.75 30.87 10.03 84 Tr*Ti 64.22 0.0015 *** *** 0.70 0.94 14 *** Time 50.40 0.0021 0.01 5.16 29.09 0.15 0.62 4.13 * Error = 61.05 *** 1.36 *** 12 Treatment *** 0.19 Ti 0.0028 7 0.0058 0.10 = 0.05 6.45 3.79 Tr 2 ** 0.0240 ** 0.02 8.87 1.48 ** 0.25 0.60 12.31 Open*** space Biofilm Upper MS F mesolittoral Oysters§

This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Accepted ArticleEffect df MS F biofilm were transformed to arcsine ( values corrected by Greenhouse-Geisser adjustment. All response variables except the uppermesolittoral infralittoral and fringe. * primary producers, sessile invertebrates and open space on shading manipulation in Table 3. C. bisinuatus C.

Effects oftreatments (repeated measures ANOVA) on abundance of § P

) P P < 0.05; ** <0.05; MS MS F

P <0.01; *** P < 0.001; P

§ P - oha’ et C=02 ** C=0.83 (***) 0.09 1.79 0.07 C=0.25 (***) 0.09 0.84 0.58 10 0.10 1.07 0.42 testCochran’s Error 0.48 5.32 * 1.34 15.01 *** Tr*Ti 5 72 Time 0.98 10.97 0.10 ** = Treatment 2 Ti = 0.05 Tr This article is protected by copyright. All rights reserved. copyright. This articleis protectedby Effect df MS F * barnacle Table 4. P

Accepted Article < 0.05; ** Effects of treatments (2-way ANOVA) onrecruitment rate of oysters andthe Chthamalus bisinuatus P < 0.01; *** Chthamalus bisinuatus Chthamalus P < 0.001 <0.001 onshading manipulation in theupper mesolittoral. P Oysters MS MS F