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AnenvironmentaloverviewofGuanabaraBay,RiodeJaneiro.RegionalStudiesinMarineScience.

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DOI:10.1016/j.rsma.2016.01.009

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Regional Studies in Marine Science

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An environmental overview of Guanabara Bay, Rio de JaneiroA. Soares-Gomes a,∗, B.A.P. da Gama a, J.A. Baptista Neto b, D.G. Freire c, R.C. Cordeiro d,W. Machado d, M.C. Bernardes d, R. Coutinho e, F.L. Thompson f, R.C. Pereira a

a Marine Biology Department, Universidade Federal Fluminense (UFF), P.O. Box 100.644, Niterói, RJ, 24001-970, Brazilb Marine Geology Department, Universidade Federal Fluminense (UFF), Av. General Milton Tavares de Souza, s/n, 4° andar, Campus da Praia Vermelha,24210-346, Niterói, RJ, Brazilc Geography Department, FFP/Universidade do Estado do Rio de Janeiro (UERJ), Rua Dr. Francisco Portela, 1470 – Patronato. CEP: 24435-005, São Gonçalo,RJ, Brazild Geochemistry Department, Universidade Federal Fluminense (UFF), Brazile Instituto de Estudos do Mar Almirante Paulo Moreira (IEAPM), Brazilf Laboratory of Microbiology, Institute of Biology and Center of Technology, CT-2, SAGE, COPPE, Universidade Federal do Rio de Janeiro (UFRJ), Brazil

h i g h l i g h t s

• We review environment impact on Guanabara Bay, and the Harbour of Rio de Janeiro.• We discuss geomorphology, climatology, hydrology, geography and biodiversity aspects.• We highlight action to reduce the environmental impact of the bay and the harbour.

a r t i c l e i n f o

Article history:Received 1 July 2015Received in revised form12 January 2016Accepted 30 January 2016Available online xxxx

Keywords:Guanabara BayEstuaryPollutionBioinvasionBiodiversity

a b s t r a c t

As most port areas throughout the world, Guanabara Bay (GB), which hosts the Harbour of Rio de Janeiro(HRJ), is under intense environmental stress. Located in one of the most iconic places of the world,GB environmental status has been the focus of worldwide attention with the imminent 2016 OlympicGames. The aim of this study was to discuss all past and current relevant aspects to characterize theenvironment of GB and its main harbour, including geomorphology, climatology, hydrology, geographyand biodiversity aspects. A historical view of the social and economic setting, as well as the majorthreats to the bay environment such as increased pollution, sedimentation, marine debris, culturaleutrophication, bioinvasions, resource utilization, climate change and habitat loss discussed. Aiming toidentify – and possibly manage – the threats to biodiversity in harbour areas, a case study comparingthe HRJ with the nearby Arraial do Cabo harbour was included. At last, conclusions were drawn so as tohighlight effective measures to reduce the environmental degradation of the bay and the harbour.

© 2016 Elsevier B.V. All rights reserved.

1. Introduction

Guanabara Bay is one of the most important embayments ofthe Brazilian coast, whose scenery displays some of the mostimportant icons of the country, such as ‘‘Pão de Açúcar’’ (SugarLoaf) and Corcovado, as well as many other natural beauties.Unfortunately, several forms of anthropogenic impacts threatenits environment since the beginning of the European colonizationin 1500 A.D. Nowadays, the edge and surroundings of GB are

∗ Corresponding author.E-mail address: abiliosg@id.uff.br (A. Soares-Gomes).

heavily urbanized and the bay receives inputs of both industrialand domestic sewage, as well as residuals of agricultural cropsfrom its green belt (Kjerfve et al., 1997; Xavier de Brito et al., 2002).In spite of the huge load of pollutants and their potential impacts,the bay supports important regional fisheries (Jablonski et al.,2006) and still retains 40% of original mangrove forestry (Pires,1992), half of which are relativelywell preserved in environmentalprotection areas—GuapimirimProtectedArea (Soares-Gomes et al.,2010).

The main port area in GB is the Harbour of Rio de Janeiro(HRJ), located in downtown of the homonymous city of Rio deJaneiro at 23°45′ S and 44°45′ W, at the edge of GB (Fig. 1). TheHRJ was established in 1910, and has been driven by Companhia

http://dx.doi.org/10.1016/j.rsma.2016.01.0092352-4855/© 2016 Elsevier B.V. All rights reserved.

2 A. Soares-Gomes et al. / Regional Studies in Marine Science ( ) –

Fig. 1. Location of Guanabara Bay in southeast Brazilian coastline. The arrow indicates the Harbour of Rio de Janeiro (HRJ).

Docas do Rio de Janeiro (formerly Companhia Docas da Guanabara)since 1973. The harbour handles shipping of automobiles, genericcontainers (electronics, petrochemicals, automotive parts, paperrolls, steel mill goods, and bulk cargos such as pig iron andwheat), and tourism. The harbour has 6740 m of continuouswharf and an 883 m pier, occupying 223 812 m2. It also has two

container terminals and an external warehouse, with, 324000and 76 394 m2, respectively. In 2013, the cargo movementtotalized 67544467 t and the transport of tourist was ca. 333.000passengers during the summer season (www.portosrio.gov.br).

The district where the harbour is settled is nowadays undera government refitting project that aims to promote the recov-

A. Soares-Gomes et al. / Regional Studies in Marine Science ( ) – 3

ery of the remaining city with the harbour region. The project,called ‘‘Porto Maravilha’’ (Marvel Harbour), is expected to re-store the nature, urban infrastructure, transport, history and cul-tural heritage, revitalizing an area of about 5 000 000 m2, repre-senting the most important legacy of the 2016 Olympic Games(www.portomaravilha.com.br).

Municipalities around GB harbour several universities andresearch centres, that have produced a huge amount of scientificknowledge concerning the bay. In this article, we review andpresent up-to-date information available, highlighting the mainaspects related to the environmental degradation of the bay.

2. Bio-Geo-Physical setting

2.1. Geomorphology

The GB connects to the Atlantic Ocean by a main channel thatextends from the entrance to the inner part of the bay. Apart fromthe region of the channel, where the width is about 1.6 km, the bayhas a semi-circular format, measuring 30 km and 28 km, in the N–Sand E–W axes, respectively. The area of the bay is ∼380 km2 andthe volume of about 1.87 × 109 m3 fills in its basin (Kjerfve et al.,1997). About 84% of the bay’s water are shallower than 10 m butin the region of the central channel, the bottom could reach morethan 40 m (Figueiredo et al., 2014).

The bottom sediments of the GB are composed of sand, muddysand, sandy mud and mud (Amador, 1997; Quaresma et al.,2000), distributed in response to bottom topography, shorelineconfiguration, tidal currents and sediment sources. The sandsediments occur from the entrance of the bay and follow the mainchannel, which is the deepest part of the bay (Catanzaro et al.,2004). Detailed bathymetric information and spatial granulometrymaps are available (e.g., Kjerfve et al., 1997 and Baptista-Neto et al.,2006). That area is subject to intense hydrodynamic action fromwaves and tidal currents, indicated by the presence of sand waves.According to Quaresma et al. (2000) and Kjerfve et al. (1997), thosesand waves occur along the eastern margin of the central channelbetween the 10 and 6 m isobaths, indicating the importance ofmarine sands transport into the bay. Extensive mud and fine sanddeposits, resulting from the active transport of clastic material andflocculated clays, are found in the north area of the bay far frommarine influence. In the northwestern and western part of thebay, continental sediment inputs are substantial and the area ishighly influenced by anthropogenic activities (e.g. sewage inputs,channelling of rivers and deforestation for urban settlement andagriculture). On the other hand, in the muddy sediments of theNE part of the bay clays predominate. Such sedimentation can beexplained as a product of lower hydrodynamics in this area, and bythe presence of mangrove vegetation, which acts as a trap, whereonly the finest sediments bypass to the bay.

2.2. Climatology and hydrology

The local climate is tropical humid wet with strong oceaninfluence. Temporal variation in precipitation results in dry (fromJune to August) and wet (from December to April) periods, withmarked differences in the mean rainfall inputs (33 and 186 m3/s,respectively). South andNorth are themore frequentwind-types inthe bay,with amean speed of 5m/s. Southwinds aremore frequentalong the year, associated to cold atmospheric fronts (INMET, 1992;Filippo, 1997). The area of the GB basin has ca. 4000 km2, beingdrained by 45 rivers and countless streams that discharge a meanannual amount of ∼350 m3/s (Kjerfve et al., 2001). That dischargeshows a great timely variation, with minimum values observedduring austral winter and a maximum in summer (Amador, 1997).Rivers are unevenly distributed and drain diverse areas regarding

land use and relief, contributing in differentways to sediment load.Themain contribution of rivers is in the East and Northeast sectorsof the bay, where the bottom is shallow and high sedimentationrates occur.

The tide in the bay was classified as microtidal mixed mainlysemidiurnal. The mean tidal range is 0.7 m (extreme high waterspring goes up to 1.3 m), with no significant spatial variability(Kjerfve et al., 1997). Due to the influence of tidal currents andto the input of freshwater from rivers that occur mainly in theinner part of the bay, the salinity shows a spatial gradient fromthe outermost to the innermost sector of the bay. During the dryperiod, the salinity ranges from 34 to 29, while in the wet periodfrom 33 to 13. Temperature of bay’s water shows an opposite trendbecause of the influence of the ocean—the water temperature isusually lower in the outer sector and higher in the inner sector ofthe bay (Paranhos et al., 1993; Paranhos and Mayr, 1993). Duringaustral summer, the entrance of cold water into the bay is acommon phenomenon, associated to Cabo Frio Island upwelling(13–15 °C), situated ca. 110 km to the east of the bay, whose waterdrifts to the coast of Rio de Janeiro city.

Data on current circulation inside the GB are scarce. Studiesdone in a small section of the bay, situated in the outermost sector,provided data on transport of volume and structuring. During theflood tide, the volume transported was 17.620 m3/s, and duringebb tide 5.731 m3/s. Moreover, current velocity is more intensein the right side of the entrance of the bay (JICA, 1994; Bergamo,2006). The mean time to 50% bay volume renewal is 11.4 days,although in the inner part of the bay, mainly during neap tides anddry periods, this time could be much longer (Kjerfve et al., 1997).

2.3. Biodiversity

A diverse topography (mountains of different heights andplains) composes the hydrographic basin of the GB. In the Northlimit there is a great complex of mountains, the Serra do Mar,where summits could reach over 2000, but in the South themountains are lower, between 500 and 1000 m. The rivers thatdrain to GB run by the scarps of Serra do Mar and other coastalhighs, having a short track andhigh energy, showing a great erosivepower. In the river influx area internal estuaries are formed anddeltas are present, occupied bymangrove ecosystems in themouthof the main rivers, mainly in the northeastern bay area (Silva et al.,2015). Other common habitats are the remains of marginal coastalforests in non-urban areas (28 km2), mangroves (90 km2), marshes(75 km2), 47 sandy beaches, 65 islands, rocky coasts (3 km2), andthe extensive soft-bottom sublittoral (Pires, 1992; Amador, 2013).

A metagenomic comparison of 10 bays (Guanabara Bay, Brazil;Botany bay, Australia; Bay of British, Bay of Fundy, Canada; Mon-terey bay, DelawareBay, Chesapeake bay, USA; Cellulose Lpool bay;North James bay, Ecuador; Cooks bay, French Polynesia) showedthat GB is a heterotrophic system with reduced abundance ofmetagenomic sequences related to the photosynthesis sub-systemwhen compared to the other bays. On the other hand, there was asignificant increase in metagenomic sequence numbers related tothe phosphorus metabolism and respiration sub-systems in com-parison to the other bays (Gregoracci et al., 2012). Due to thestrong influence of the marine environment in the GB, the chan-nel and bridge areas have a dominance of alpha-proteobacterialgroups (SAR11 group, Flavobacteriales, and Rhodobacteriales),while in the anoxic inner portion of this bay, there is a clear pre-dominance of copiotrophic, facultative-anaerobic, or chemosyn-thetic Gammaproteobacteria (e.g., Alteromonadales, Pseudomon-adales, Enterobacteriales, Oceanospirrilales, Chromatiales, Vibri-onales, and Thiotrichales) (Silveira et al., 2013).

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Villac and Tenenbaum (2010) accounted for 308 phytoplank-tonic taxa in GB through direct microscopic identification, encom-passing diatoms as the more speciose taxon, followed by the di-noflagellates,with 199 and90 taxa, respectively. Themost conspic-uous species were the dinoflagellate Scrippsiella trochoidea and thediatom Skeletonema costatum complex, the former reaching a den-sity of 106 cell/L in the more protected area and the latter beingthe more spatially spread in the bay. The cell density could rangewidely, from 105 to 109/L, with higher abundance ones observedduring the rainy season in surface water, in sites closer to the mar-gins and in the inner sector of the bay. In the outer sector, mainly inthe central channelwhere the circulation is stronger, the cell abun-dance is lower and the diversity is higher, with the occurrence oflarger individuals diatom species.

Regarding the protozooplankton, there are 169 taxa foundin the GB (Gomes and Areas, 2012), the most speciose beenthe Ciliophora (148) and Sarcomastigophora (20). Among theCiliophora, the order Tintinnoidea is the more diverse one,contributing with 69 taxa. Greater body taxa predominatein the outer sector of the bay (such as Codonellopsis spp,Steentrupiella spp, Eutintinnus spp and Helicostomella spp), whilein the inner sector the dinoflagellates and loricated ciliates thathave heterotrophic feeding mode and are small-sized (such asGymnodinium/Gyrodinium complex, Protoperidinium spp, Halteriaspp and Euplotes spp) dominate.

According to Bonecker et al. (2012), about 150 taxa ofmesozooplankton occur in GB waters, including both mero-and holoplankton. The more speciose groups are Copepodaand Decapoda larvae. Like other plankton components, thespecies of mesozooplankton show a spatial distribution related tohydrodynamic conditions, although some species have a spreadoccurrence such as Temora turbinata and Paracalanus quasimodo.The fish larvae that occur in the bay, highlighting its role as anursery site, with amount ca. 64 taxa. The Engraulidae Cetengraulisedentulus and Anchoa lyolepis are the more abundant fish speciesand they occur throughout the year, alternating density accordingto their life cycles (Kurtz, 2012).

The fish assemblage of the GB sums up to 245 species, but174 are true marine or estuarine species and the remainder71 occur more frequently in the rivers that drain to the bay,entering occasionally in the saline sector during periods of heavyrainfall. The more speciose group is the Scianidae, represented by18 species (Vianna et al., 2012). The more important groups asfishing resources are species of Clupeidae, Scianidae, Serranidae,Ariidae, Balistidae, Mugilidae and Centropomidae, among othertaxa. Atlantic anchoveta (Cetengraulis edentulous), whitemouthcroaker (Micropogonias furnieri), mullets (Mugil liza and Mugilcurema), and the Brazilian sardine (S. brasiliensis) are the mainspecies landed by local fishermen (Jablonski et al., 2006).

Another important component of the pelagic system of the GBare cetaceans and turtles. In the past, whales such as Eubalenaaustralis, Balaenoptera ederi, and Megaptera novaeangliae werecommon visitors, but nowadays only the dolphins Sotalia fluviatilisare regularly recorded inside the bay. Besides S. fluviatilis, theoceanic species of dolphins Tursiops truncatus, Steno bredanensis,Delphinus sp. and Lagenodelphis hosei were also recorded in thebay waters (Lailson-Brito et al., 2012). To our knowledge, thereis no reference recording the occurrence of turtles inside the GB.However, it is common to find reports on newspapers and otherpopular media about turtles accidentally captured by gill nets aswell as carcasses found adrift in the bay beaches. In the vicinitiesof the GB the occurrence of the turtles Chelonia midas and Carettacaretta are very common (Reis et al., 2009) and most likely thesespecies enter the bay to seek refuge and for foraging onmacroalgae.

In relation to the benthic system, molluscs, polychaetes andcrustaceans are the best-studied invertebrates of the sublittoral

soft-bottom fauna. Molluscs are the more speciose, summing upto 113 species, the more rich been the bivalves with 67 species(Mendes et al., 2006; Neves et al., 2013). The second most species-rich group are the crustaceans that, according to a review doneby Lavrado and Keunecke (2012), account for 91 taxa. In theirstudy, that do not considered the mangrove crustaceans, the morespeciosewere the Xantidae crabs (13 species) and swimming crabsof the Portunidae family (11 species). The third larger group isthe polychaetes, accounting for 77 species, with dominance of3 species—Poecilochaetus australis, Spiochaetopterus nonatoi andPrionospio heterobranquia (Santi et al., 2006; Santi and Tavares,2009). In a paper that reviewed the literature on sandy beaches,but that also included some studies that sampled the sublittoralzone, Omena et al. (2012) presented 139 taxa, the more diversebeen the polychaetes (58 taxa), crustaceans (25) andmolluscs (23).Concerning the benthic macroalgae, Yoneshigue-Valentin et al.(2012) listed about 172 taxa, the red (105 taxa) and green algae(43 taxa) being the more speciose.

According to Laut et al. (2011), 51 benthic diatoms occur insediments of GB. Regarding abundance, Plagiogramma pulchellumand Navicula sulcata are the dominant species, while Naviculayarrensis var. yarrensis is the most frequent species in the bay,occurring in 83% of sampling stations.

An increasing benthic biodiversity gradient is observed in GB,ranging from the azoic and species impoverished inner sector toa well-structured community in terms of species composition andabundance in the outer sector (Mendes et al., 2006; Van Der Venet al., 2006; Santi et al., 2006; Mendes et al., 2007; Santi andTavares, 2009; Laut et al., 2011; Soares-Gomes et al., 2012). Sincethere is a natural gradient coupled to the anthropogenic gradientin the entrance-interior axe of the bay, further confounded bythe occurrence of contamination hot spots, it is not possible toconclude what causes the observed patterns.

3. Social and economic setting

In 1500, the year of the discovery of Brazil by the Portuguese,indigenous peoples have inhabited the lands surrounding theGB for at least 12000 years (Amador, 2013). Shortly after thediscovery, the Portuguese governments sent an expedition alongthe Brazilian coast, to assess and name the geographical featuresof the coast. In 1502, they entered in the GB for the first time.However, the Western occupation began with the division of theBrazilian lands in hereditary captaincies, a private managementmode of the territory by the Portuguese government. The areain question was part of the Captaincy of São Vicente, with theadministrative centre located on the coast of the current state ofSão Paulo. The lack of enforcement allowed the installation of theFrench, who occupied the GB because of its physical attributessuch as the sheltered waters, an excellent harbour for ships androcky hills in its entrance (e.g., Pão de Açúcar), a perfect place fordefence. They settled for ten years and there founded a colony,France Antarctique. After several attempts to expel the French,the Portuguese finally succeeded and founded in 1565 a villageas a military unit of government management of the PortugueseCrown, the Royal City of São Sebastião do Rio de Janeiro. Theterritory to its surroundings was elevated to the captaincy of Realcategory of Rio de Janeiro, which centuries later changed legalstatus for State of Rio de Janeiro.

Established military occupation began donating land and theimplementation of the sugar activity with cane farms and millsin the vicinity of the GB. The water transport dominated thescene, because the rivers were the main route access to the landssurrounding the bay, so dozens of small harbours were created.Various shops and services were created in the city due to theharbour in question and on the farms, mills and villages the

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population showed great progress over the decades. At the end ofthe sixteenth century, the Portuguese established structures on thecoast for processing meat and oil from whales that were huntedin the bay. The coffee plantations marked the seventeenth centuryand togetherwith sugar canewas responsible for the deforestationof the bay surroundings, largely changing the natural landscape.The development of the city was also heavily influenced by thecountry’s mining cycle. Although the city was not a major mineralproducer, gold and other minerals extracted in the country’shinterlandwere transported to the Portuguese court by ships usingthe harbour facilities of the city.

After the European colonization period, urban areas expandedslowly, but in the mid-twentieth century an acceleration ofurbanization was observed as the city expanded to areas ill-suitedto urban uses such as wetlands, river banks, and steep slopes. Inthis period the most dramatic suppression of Atlantic rain forestthat surrounded the bay abundantly at the time of discoverywas observed (Brandão, 2006). Presently, the HRJ is inserted in aquite complex urban context in the heart of the metropolitan areaof Rio de Janeiro, the largest urban concentration in the coastalarea and the second economic and populational centre in Brazil.This territorial planning unit consists of 21 municipalities andit is marked by high population density and large numbers ofcompanies in comparison to the remaining state of Rio de Janeiro.According to the Brazilian Institute of Geography and Statistics—IBGE, in 2014 the metropolitan area housed 12229867 residents,corresponding to 74.3% of the state population and accountingfor 63.6% of the wealth produced by the state (IBGE, 2014). Theservices sector is one of the largest generators of wealth andjobs and the harbour activity plays a historically prominent role.The harbour sector of the Metropolitan region goes through anaccelerated process of change: the harbour of Rio is subject toexpansion and equipment installation for container operation inCaju pier, the pier of São Cristóvão was transformed into a supportbase for offshore oil and gas production activities and the pierof Gamboa, closer to the centre, remains as a passenger terminaland undergoes a profound metamorphosis for the development oftourist and cultural practises, as well as the port of Niterói, locatedin the opposite part of the bay, that has a new role to meet theneeds of offshore oil activities.

Industrial activity in the Metropolitan region is traditional andhad ca. 14.483 companies in 2012, representing 60.4% of thestate’s units, with a highly diversified profile in types and sizes,constituting strong potential polluter, 98 related to extractive oilindustry and gas, 50 companies in the industry manufacture ofcoke, petrochemicals and biofuels products and 518 chemicals(IBGE). The majority of these companies are installed in thewatersheds of Guanabara and Sepetiba bays and adjacent systems,as their water systems are often the local destination of industrialwaste.

Since 2006, the Metropolitan region of Rio de Janeiro expe-riences an intense spatial reconfiguration process with severalprojects under way. Oil activity is the driving force for most trans-formations, involving hundreds of companies, especially relatedto implementation of various projects for Petrobras. The mainprojects are the expansion ofmanagement and research structuresin the city of Rio de Janeiro, the gas terminal deployment in GB,increasing refining capacity in Duque de Caxias Refinery (REDUC)and the implementation of the Petrochemical Complex of Rio deJaneiro in Itaboraí-São Gonçalo (COMPERJ). The ship building in-dustry is currently reviving with the reopening of 20 shipyards onthe margins of the GB for the construction and repair of platformsand support vessels. It will also include the works for the 2016Olympic Games, the refitting of the surroundings of the HRJ to hostthe expansion of the downtown area, consisting in the largest ur-ban project in the country at the moment, development and re-structuring of tourist sectors and residential and commercial real

estate. Finally, the construction of the ring road, a peripheral high-way, facing the productive structure, which articulates importantindustrial and the harbour nuclei in the east, north and west areasof themetropolis and at the same time, can be considered as a newaxis of urban-industrial expansion of the metropolitan area.

It is important to highlight that this is an urban area of greatcontrasts, with many elite residential areas, the middle classesand, for the most part, popular. The lack of basic sanitation is anoteworthy reality in popular residential areas in the central andperipheral municipalities. About 13.9% of the population lives inshantytowns and 48.7% of the population lives without sewagesystem (CEPERJ Foundation, 2013), and the percentages are higherin municipalities that do not make up the Metropolitan Center,Rio de Janeiro and Niterói. To this fact is added the deficiencyin garbage disposal, which results in public health problemsas the huge discharge of untreated domestic sewage into thewatercourses in the metropolitan region inputting into GB andother coastal systems, causing serious social and environmentalimpacts.

4. Threats

4.1. Pollutants

Because of the historical background of occupation and theunassertive restoration actions, the GB is one of the most pollutedsites of the Brazilian coastline (Carreira et al., 2002). Pesticides andnutrients originated in the agricultural green belt located in itsdrainage basin join to other contaminants, such as heavy metals,hydrocarbons, and domestic sewage, that pollute the water andaccumulate in the sediments (Ventura et al., 2002; Xavier de Britoet al., 2002; Baptista Neto et al., 2005; Baptista-Neto et al., 2006;Silva et al., 2007; Soares-Gomes et al., 2010).

The texture of the sediment (particle size and organic carboncontent), hydrodynamic, and bathymetry play an important rolein the concentration of contaminants in the GB. The rivers andchannels that discharge into the bay cross greatly urbanized areas,receiving all kinds of effluents (Faria and Sanchez, 2001; Fonsecaet al., 2014; Borges et al., 2014).

Despite the development of plans for pollution control, thesituation of water quality and bottom sediments of the GB hasbeen critical during the last 20 years (JICA, 1994; Baptista Netoet al., 2005; Cordeiro et al., 2015). The emission of heavy metalsfrom anthropogenic origin into the bay and their accumulationin sediments has been evidenced by several studies. Such studiesallowed a characterization of heavy metals spatial variability,usually showing that the western portion of the bay and theharbour areas are the more eutrophic and exposed to trace metalscontamination, particularly due to the contributions of urbaneffluents from rivers, such as Iguaçu, Sarapuí, Irajá and São Joãode Meriti (Pfeiffer et al., 1982; de Souza et al., 1986; Rego et al.,1993). These have promoted the accumulation of metals in thebottom sediments under anaerobic conditions for the last fewdecades (Perin et al., 1997; Machado et al., 2004). A three-stepsequential extraction procedure, which was based on the BCRmethod, demonstrated different sources to GB metals. The urbanemission sources related to the discharges of the São João deMeritiriver exhibit significant levels of Ba, Cd, Ni, Zn, andHg. The São Joãode Meriti River and harbour areas also show a predominance of Pband Cu, while V and Cr mainly characterize the system formed bythe Iguaçu and Sarapuí rivers. Other metals, such as As and Mn,were found mainly in the central sector of the bay and they wereassociated to biogeochemical processes. Zn and Cd were found tobe themost labilemetals, in contrast to Cr, Cu, Ni, and Hg that werethe least labile metals, and 62%–84% of the concentrations of these

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metals were found in the organic residual fraction of the sedimentsamples (Cordeiro et al., 2015).

Based on studies carried out by distinct authors (e.g. Carreiraet al., 2002, 2004; Baptista Neto et al., 2005; Baptista-Neto et al.,2006; Melo et al., 2014 and Cordeiro et al., 2015) it is possible toidentify the main pollution hot spots in GB. According to thosestudies, five main areas of high degree of environmental pollutionwere identified: The northwestern area, which receives inputsfrom themost polluted rivers andwhere themain oil refinery of thecountry is located; TheHRJ area,where heavymetal concentrationsare associated with shipping activities and the outlet of one of themost polluted rivers of the catchment basin (Borges et al., 2014);The eastern area nearby São Gonçalo town and Niterói Harbour(Vilela et al., 2004; Baptista Neto et al., 2005), which is the secondbiggest urban concentration of the metropolitan area; The area ofJurujuba Sound, considered one of themost polluted sites (BaptistaNeto et al., 2000; Sabadini-Santos et al., 2014); and finally, thetransition zone between the former areas, which shows a widerange of values, from the highest to the lowest.

The high Pb concentration in themiddle of GBmay be related tothe presence of an oil terminal (Baptista-Neto et al., 2006). Large oilspills that occurred between 1998 and 2002 aggravated pollutionproblems by affecting, for example, the resident biota and itsenvironmental quality (Meniconi et al., 2002; Kfouri et al., 2005).On the other hand, there are two areas with better environmentalcondition, the northeastern, which is semi-enclosed, shows betterenvironmental conditions due to the preservation of themangroveswamps and possess lower heavy metal concentrations, andother located in the entrance of the GB, which is influenced bystrongwater exchange processes, with sandy sediments and lowerconcentrations of organic carbon as compared to the northwestern,semi-enclosed, area.

At GB the organic matter flow to the sediments over the last100 years reaches a maximum of 41.7 mol C/m2/yr. High res-piration rates occur in the water column and fast sedimentationrates result in the transfer of a significant carbon fraction to anoxicsediments. Elemental and isotopic (C/N and d13C) time–space dis-tribution indicate that the organic matter results from a mix-ture of marine, terrestrial and estuarine sources, with a grow-ing predominance of autochthonous inputs in recent years. A di-noflagellate lipid, dinosterol, is by far the most abundant sterolfound in the GB highlighting the presence of high concentrationsof the faecal sterol, coprostanol (>40 mg/g). Its spatial distribu-tion generally coincided with the presence of untreated domesticsewage sources (Carreira et al., 2002, 2004). Santos et al. (2008)also associated coprostanol inputwith recent eutrophic conditions,which are one of the causes of the rise of autochthonous sterols(e.g. cholesterol, dinosterol, brassicasterol and partially stigmas-terol and beta-sitosterol). Trends in degradation of organic mat-ter were evidenced by sterol/stanol ratios. Dinosterol behaviourindicated that the bay has been dominated by the accumula-tion of phytoplankton-derived organic matter since earlier times.In the northwestern sector, the faecal sterols coprostanone, epi-cholestanol and coprostanol from suspended particles and sed-iments occurred in high concentration (up to 12.3 µg/L and70.6 µg/g, respectively) and were associated with increasing dis-tance from the diffuse sewage sources (Cordeiro et al., 2008).

Among the principal classes of organic pollutants found inthe GB are the persistent organic pollutants (POP). Christensenet al. (2010) characterized the complex polycyclic aromatichydrocarbons (PAH) pollution patterns in sediments from GB andrevealed five distinct sources of 3- to 6-ring PAH. The HRJ is themost contaminated site in the bay, with the pollutant spreadingto southwestern and northeastern regions. Concentrations of totalPAH in about 100 sediment samples from GB were in the range of96–135 000µg/kg, similar to other coastal urbanized embayments

(Wagener et al., 2012). PAH in suspended particulate matter of sixof the major rivers and two channels of the GB basin ranged from28 ng/L to 11.514 ng/L. Using the concentration information fromthose rivers,Mauad et al. (2015) estimated a total flow rate of 3 t/yr,which corresponds to 30% of the total PAH annual input into thenorthern area of the bay.

After an oil spill of 60 000 L of diesel oil in January, 2000 inGB, the total PAH concentrations ranged from 77 to 7.751 µg/kgdry weight in surface sediment samples and from undetectedto 1.592 ng/L in water samples. The majority of the sedimentsamples were classified as highly contaminated (total PAH >500 µg/kg), while in water samples the PAH concentrations werenot sufficiently high to induce acute toxicity to aquatic organisms(Silva et al., 2007). After the accident, samples from animalswith different biological requirements were analysed. Barnaclespresented the highest PAH concentrations in the first month afterthe oil spill, decreasing to background levels after a few months.A background level of <50 kg/L was suggested based on thereference site and on values observed in the followingmonths afterthe accident (Soares-Gomes et al., 2010).

Transfer of methylmercury in GB food webs was observed be-tween trophic levels from prey (microplankton, mesoplankton andfishwith different feeding habits) to top predators (pelagic and de-mersal fish). Top predator fish presented the highest methylmer-cury concentrations (320.3 ± 150.7 µg/kg dry wt), whereas mi-croplankton presented the lowest (8.9 ± 3.3 µg/kg dry wt.). Thesuccessive amplification of methylmercury concentrations and itsbioconcentration factor with increasing of the trophic levels, frombase to top, indicated that biomagnification may indeed occur.These results highlight the importance of the feeding habits andtrophic level in the bioaccumulation of methylmercury by aquaticbiota (Kehrig et al., 2011).

Black carbon (BC) embodies a group of recalcitrant carbona-ceous materials produced by incomplete combustion of biomassand fossil fuels (Goldberg, 1985). BC has been found in mangrovesediments of the GB in concentrations ranging from 0.03% to 0.47%(sediment dry wt), and reaching a maximum of 9% of the total or-ganic carbon (Luz et al., 2010). BCmass accumulation increase overthe last 118 years with a concentration that varied between 0.23%and 0.51%, whereas a decrease in the values of the ratio BC/organiccarbon was observed in the upper sediment layers, probably re-flecting the enhancement of the GB eutrophication process in thelast 30 years (Mauad et al., 2013). Higher concentrations of py-rolytic PAH were observed between 1925 and 1976, being consis-tentwith the subsequent deforestation, urbanization, and industri-alization that occurred in the GB basin in that period (Mauad et al.,2013; Ribeiro et al., 2008).

Polychlorinated biphenyls (PCB) and polybrominated diphenylethers (PBDE) were investigated in mussels (Perna perna) andtwo commercially important fish species, croaker (M. furnieri)and mullet (M. liza) from GB. The results show that all sampleshad higher PCB contamination than other ecosystems around theworld. On the other hand, PBDE presented lower concentrations in41% of the samples. Croakers presented the highest PCB and PBDElevels, with mullets showing intermediary values andmussels, thelowest (Gonçalves da Silva et al., 2013).

Eight chlorinated pesticides were detected in the tissues of themussel P. perna from GB. All monitored pesticides were detectedwith higher concentrations during the dry season, likely due tothe higher dilution of inflowing pesticide residues in the rainysummer season. In general, the concentrations of the DDT groupof pesticides were higher than those of the other organochlorines.Amongst those, DDE predominated in most samples, although theproportion of unmetabolised DDT was significant in almost allsamples. It is clear that DDT continues to be washed into theestuary from sources within the catchment. The concentrations of

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ofaldrin, dieldrin and lindane were all similar in general terms.The spatial differences between the sites were not particularlymarked, however there was a trend towards lower pesticide levelsinmussels nearest to the bay entrance (Xavier de Brito et al., 2002).

4.2. Sedimentation

The sedimentation rate in the last 6000 years, integrating14C and 210Pb chronologies, showed three distinct non-anthropicphases of sedimentation. In the first phase, between 6000 and4.300 yr, sediment accumulation rates were high, related to themarine Holocene transgression, reaching 0.87 cm/yr. In the secondphase, between 4300 and 2000 yr, the sediment accumulationrate decreased, reaching the lowest value around 0.03/0.04 cm/yr.Between 2000 and 500 years, the sediment accumulation ratewas higher than the previous phase. After human occupation,the sedimentation rate is constantly increasing since 1922(0.14 cm/yr), doubling in the last 5 years, from 0.60 to 1.25 cm/yr.Although interventions in the GB have occurred since colonialtimes, the major ones have happened in the twentieth centurywith the industrial development of the regions surrounding thebay that brought up the current sedimentation rate to ca. 1 cm/yr(Godoy et al., 2012). The more recent increment was attributed tothe increase in urbanization issues, such as deforestation, farming,paving roadways, and dredging of silted channels (Figueiredo et al.,2014). The organicmatter flux to the sediment in the last 100 yearschanged from4.2mol C/m2/y to 41.7mol C/m2/yr, causing anoxicsediments and creating a 2–3 cm nepheloid layer (Wagener, 1995;Carreira et al., 2002).

4.3. Marine debris

According BaptistaNeto and Fonseca (2011), the abundance anddistribution of debris in the GB, floating and on the beaches, arerelated to local land-based or nearshore sources, where the riversrepresent the main source of debris, due to the use of the riversby the municipality inhabitants for garbage disposal. The authorsmonitored debris on 12 beaches of GB over 10 years and verifiedthat the waste amount in the wet season (summer) was nearly3 times higher than the amount in the dry season. These authorssuggested that this greater waste amount during the wet seasonattests that river systems are the major suppliers of debris to GB,as many rivers were supplied by rainwater. Their results indicatethat the relationship to the amount and composition of the debrisdeposited on beaches also reflect the cleanness practise by themunicipality (mechanical and manual cleaning).

Besides litter gathered on beaches, floating litter from riversof the GB catchment basin is collecting using artificial retainingbarriers (Ecobarreiras 2016 Project) in order to prevent the input oflitter to the bay’swaters. According to Franz (2011), plastic (66.4%),paper (9.8%), and carton packs (6.6%) are the main items retainedby those ‘‘ecobarriers’’. Other items include metal, styrofoam,rubber, wood, diapers, sanitary napkins, and pottery.

4.4. Eutrophication

The primary productivity of the GB is huge, probably due toanthropogenic nutrient input that causes phytoplankton blooms.Maximum chl-a concentrations can reach 90 × 10−3 mg chl-a/L(Braga et al., 1993). Carbon assimilation ranges from 800 to3.600mg/day,with ameannet production of about 0.17mol C/m/d(Rebello et al., 1988). Those figures are supported by a great inputof nutrients from gross domestic sewage (3.2 × 109 mol P/yr and6.2 × 1010 mol N/yr), and elevated temperatures and solar radia-tion year round (Wagener, 1995).

Pelagic dissolved oxygen shows a strong spatial and temporalvariation in the bay. The surfacewater could get 300% of saturationdue to phytoplankton blooms and concentration of bottom watercould drop below 1 mL O2/L (Rebello et al., 1988, 1990). In theinner sector of the bay, where circulation is poor, concentrationranges from anoxia to 7.26 mL/L (Paranhos et al., 2001; Pereiraet al., 2006).

Clear evidences of eutrophication also come from vibrio countsand total microbial counts in different locations of the GB(Gregoracci et al., 2012). Total microbial and vibrio counts reach>10 million cells/ml and >40000 cells/ml, respectively, in theinner bay, nearby Fundão and Governador Island, while countsdrop to around 100 vibrio cells/ml, beneath the middle (Rio-Niterói bridge) and in the main channel. Despite the extremelyhigh P concentration levels observed in the GB (2–20 µM totalphosphorus), shotgun metagenomic analysis clearly showed thatVibrio populations and complete communities have their growthand diversity controlled by phosphorus as the N:P ratio in theGB is always higher than 26:1 (Gregoracci et al., 2012). Theimportance of top down controls, e.g. phages and protozoa, areunder investigation. Potentially pathogenic bacteria are foundin higher abundance in the inner bay. The identified bacterialtaxa (e.g. burkholderias, vibrios, pseudomonas, klebsiellas) mayrepresent a serious threat to human and animal health. Multidrugresistant bacteria have been isolated from GB areas, indicating afurther threat to human health (Coutinho et al., 2014). The spreadof organic matter rich and anoxic regions around the Fundão andGovernador islandsmay further contribute to the dissemination ofimportant pathogenic microbes in the GB.

4.5. Habitat modification

Sandy beaches, estuaries, marshes, mangroves, lagoons androcky coasts characterized the pristine environment of Rio deJaneiro coastline. The coastal mountains were covered by theAtlantic rain forest that overtakes to the sandbanks of the littoralzone.

The suppression of vegetation (Atlantic rainforest) to makeroom for human settlements occurred early after the Europeansettlement in the XVI century. The Tijuca rain forest was almostcompletely denuded for coffee crops by the Portuguese and onlyreplanted years after. The loss of the Atlantic rainforest from 1500to 1997 was ca. 40%, with only 2100 km2 remaining nowadays(Amador, 2013). Therefore, the nude granite and gneiss bedrocksuffered weathering and the resulting material filled in manycoastal habitats.

Mangroves originally occupied 257 km2 of the bay margins(Amador, 2013). Mangrove trees were historically used as a sourceof timber for coal, house construction, and fishing traps. Extensivemangrove areas were suppressed by landfills for sanitary purposesand urban pressure. Today, only ca. 40% of the original amountremain (ca. 90 km2), located mainly in the northwestern portionof the bay (Pires, 2010; Lardosa et al., 2013; Fundação SOSMata Atlântica, 2015). Although the rate of suppression is lowernowadays, in the period of 2000–2011, 3.18 km2 of mangroveswere suppressed due to urban pressure caused by the growingpopulation density (Pereira and Kampel, 2014).

Marshes and other humid areas occupy about 75 km2 of themargins of the GB, which represent only 30% of the originaloccurrence in the beginning of the European colonization. Themain reason for this loss was sanitary, use of lands for agriculture,and urban pressure (Amador, 2013).

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4.6. Invasive species

The benthic ecosystem is the best known example, wherethe larger number of exotic and cryptogenic species wereregistered in the bay. In hard bottom habitats, the barnaclesMegabalanus cocopoma, Amphibalanus reticulatus, Amphibalanuseburneus, Amphibalanus amphitrite and Balanus trigonus (Lacombeand Monteiro, 1974; Young, 1994; Carlton et al., 2011), theascidians Styella plicata and Ciona intestinalis (Rocha and Kremer,2005), the ectoprocta Schizoporella errata, the sponge Paraleucillamagna (Klautau et al., 2004), the bivalve mollusc Isognomonbicolour (Breves-Ramos, 2004), and the polychaete Branchiomaluctuosum (Costa-Paiva, 2006) were found. In soft bottoms, thepolychaetes Polydora cornuta and Pseudopolydora paucibrachiatawere reported (Radashevsky, 2004). The exotic swimming-crabCharybdis helleri occurs in great abundance in some sites, althoughno ecological consequences have been recorded (Tavares andMendonça, 1996).

In the pelagic system, there is only one exotic species ofplankton reported in the literature, the copepod T. turbinata(Bonecker et al., 2012). Regarding fishes, the freshwater speciesClarias gariepinus (African sharptooth catfish) and Oreochromisniloticus (Nile tilapia) now occur in rivers that discharge into thebay (Soares-Gomes et al., 2010).

4.7. Resource utilization

There is currently no regular fisheries monitoring program inGB, although it represents an important regional economic activity.Jablonski et al. (2006) did the best evaluation of fishing in the baybased in monthly data obtained from 2001 to 2002. According tothem, there were 32 landing points and among 517–690 fishingboats (62% employing gillnet gear) regularly operating within baywaters. The number of fishermen involved oscillated between1400 and 2100, excluding crab, swimming crab and musselcatchers. The total landing in that period was ca. 19 000000 t,pricing about US$ 4.8 million. Atlantic anchoveta (Cetengraulisedentulus) corresponded to 69% of the total. Other importantfishes were the Brazilian menhaden (Brevoortia spp.), whitemouthcroaker (M. furnieri), mullet (M. liza), Brazilian sardine (Sardinellabrasiliensis), and the lagehead hairtail (Trichiurus lepturus). Amongshellfishes, shrimps (Farfantepeneus brasiliensis, F. paulensis, andLitopeneus schmittii), swimming crabs (Callinectes danae and otherspecies), mangrove crabs (Ucides cordatus), and brown mussels(P. perna) are also important items harvested. Farmed seafoodsare restricted to mussels, reared in longline systems in a sitenear the mouth of the bay by the Mariculture Association ofJurujuba. Besides mariculture, mussels are harvested by a numberof independent collectors that operate mainly in the region nearthe mouth of the bay and in nearby rocky coasts (Lage andJablonski, 2008).

4.8. Climate change

A recent study on the present and future climate of Rio deJaneiro city reported a trend for air temperature increase, withlonger dry seasons and shorter wet seasons for the end of 21stCentury (Dereczynski et al., 2013). Possible impacts of sea-levelrise associated to climate change are alterations in themorphologyand dynamics of sandy beaches and other sedimentary intertidalsites, shifts in water quality, and flooding of mangrove and otherlow coastal vegetation habitats. The potential of mangroves andother coastal habitats to retreat inland in response to invasion ofwater is hampered by urban occupation, such as roadways andbuildings (Schiller et al., 2001). Young (2011) analysed the risk ofsea level rise caused by global warming in association with intense

rainfall events. Although the focus was on human aspects, thestudy warned about negative effects of shoreline erosion relatedto increasing wave energy, as well as a groundwater level rise andincreased frequency of flooding events in lowareas associatedwithheavy rainfalls, spring tides and meteorological tides.

5. A comparison between two nearby harbour areas within Riode Janeiro state: A case study

The worldwide decline of marine biodiversity – due tooverfishing, pollution, habitat destruction, biological invasion orglobal climate change – calls for an urgent reassessment of currentmanagement practises. Confronting large-scale crises requires amajor scaling-up of management efforts based on an improvedunderstanding of the complex ecological processes that underlieecosystem resilience. Managing for improved resilience andincorporating the role of human activity in shaping ecosystems,will provide a basis for copingwith uncertainty, future changes andecological surprises.

Arraial do Cabo (AC), a town in Rio de Janeiro state of ca. 20 000residents, is located on a cape (formerly called Cabo Frio, i.e., ‘‘coldcape’’, 23° S, 42°W) that extends 40 km into the ocean. Fishermenhave been drawn to the cape for centuries due to the rich marineenvironment, nourished by upwelling of the South Atlantic CentralWater. The region also constitutes a biogeographical transitionzone between the northern warm tropical region and the southerncolder water areas. In 1997, AC became Brazil’s first open-waterMarine Extractive Reserve (MER), or ‘‘Artisanal Fisheries Reserve’’.MERs are a new type of collaboratively managed marine protectedareas, established in coastal areas of Brazil in order to protectmarine resources while sustaining the livelihoods of traditionalresource user communities. However, as GB in past and presenttimes, AC population is increasing, as well as the importance ofits harbour, which has recently been approved for support tooil and gas activities. Anthropic influence in the local marineecosystem is therefore growing in a similar manner to that of GBin past times, which provides a unique opportunity to understandthe modifications underwent by GB communities, as well as tounderstand and even prevent those modifications from happeningor progressing in AC.

Hard bottom communities in this place do not form atypical coral reef, but some corals do thrive in its waters,such as the dominant zoanthid Palythoa caribaeorum, the firecoral Millepora spp. (a hydrocoral), six scleractinian coral species(Siderastrea stellata, Mussismilia hispida, Porites branneri, Madracisdecactis, Phyllangia americana), andAstrangia rathbuni, the endemicgorgonian Phyllogorgia dilatata and a diverse assemblage ofseaweeds and other benthic invertebrates such as sponges, aswell as over 150 associated fish species (Ferreira, 2003). Floeteret al. (2006) classified the region as a partially protected (PP)area, where the surroundings are open to all types of fishingwhile at the area of the reserve only hook and line fishing ofmid-water fishes is allowed. A crucial weakness of the reserveas it currently operates rests in its ineffective monitoring system(Pinto da Silva, 2004), and the Arraial do Cabo MER has notbeen continuously enforced since its creation. As a result, thereis evidence that some fish species may be overfished (Silva,2004), while some reef fish species are clearly benefiting fromthe protection conferred (Floeter et al., 2006). Therefore, althoughthe region is still considered to be relatively pristine comparedto nearby coastal areas such as GB, at least two non-indigenoustropical coral species have been detected. They include the softcoral Chromonephthea braziliensis, and a scleractinian, the sun coralTubastraea coccinea (Ferreira, 2003). A third invasive species is theintertidal purse oyster, Isognomon bicolour (López et al., 2014).These specieswere probably introduced via fouling in oil platforms

A. Soares-Gomes et al. / Regional Studies in Marine Science ( ) – 9

Fig. 2. Relationships among hard-bottom community diversity (species composi-tion and richness), productivity (the rate of production of organicmatter) and stabil-ity (temporal constancy) within a local scale (triangle). The effects of regional scaleprocesses (square) such as disturbance rate, resource supply and propagule sup-ply, as well as anthropogenic activities such as pollution, human-mediated speciestransport and fisheries are also shown. The circle is presumed to be a spinningwheel, powered by larger scale processes, which then shift positions to influencelocal scale processes. Dotted arrows indicate hypothetical relationships.Source:Modified fromWorm and Duffy (2003).

or ships, and appeared in natural hard substrata within the last20 years or less. In the small local port area, a number of otherexotic species can be found, but so far they have not dispersedbeyond the port surroundings.

Experimental evidence suggests that local benthic diversity ismaintained by a number of factors (Fig. 2), including the localproductivity (usually low), the natural disturbance regime andthe resilience conferred by the local species pool, i.e., its ownhigh diversity tends to prevent ecological dominance. Just as someexotic species aremore successful invaders than others, dependingon their intrinsic traits, some communities are more susceptibleto invasion than others (i.e., they have more invasibility). Morediverse communities are thought to be more invasion resistant,although this assumption has rarely been experimentally testedin hard bottom communities (but see Stachowicz et al., 2002).Similarly, communities with hypothetically identical diversity, butcomposed by different species can differ in their invasibility.

Among the numerous theories that have been developed tounderstand the role of disturbance on species diversity, the mostprominent is perhaps the ‘intermediate disturbance hypothesis’(IDH), but supportive experimental evidence, although abundant,remains contradictory, leading scientists to suggest the existenceof an interaction between disturbance and productivity (Kondoh,2001). Jara et al. (2006) assessed experimentally the interactiveeffects of disturbance frequency (i.e., biomass removal, with 7levels) and nutrient enrichment (as a proxy for productivity, with 3levels) at AC, relatively oligotrophic, and GB, an eutrophic site. Theresults indicated site-specific diversity-driving processes in theabsence of disturbance. Diversity and species richness peaked atboth sites at some intermediate level of disturbance, corroboratingthe IDH. Nutrient enrichment increased total species richness andalgal species richness in particular, but only at AC. Only here,did nutrient enrichment eliminate the unimodal species richnesspattern observed along the disturbance gradient under ambientnutrient concentrations. Such interactive effects of disturbanceand productivity on diversity confirm the general predictions of

advanced IDH models. Another study (Ilarri, 2005) in the samesite assessed the effects of different levels of productivity inhard bottom communities protected from fish predation. Modularorganisms tended to monopolize space, thus reducing diversity,and nutrient enrichment favoured the encrusting bryozoan S.errata, a species commonly found in port areas and consideredto be invasive elsewhere. Thus, predation alleviation and/ornutrient enrichment could both lead to space monopolization,with differing composition outcomes depending on whether thesefactors where combined or not.

Productivity is considered to be another key factor affecting andregulating diversity (e.g.Worm and Duffy, 2003), and has attractedincreasing attention due to worldwide human-mediated increasesin coastal eutrophication (Nixon, 1995). Productivity and diversityare often unimodally related, such that peak diversity is observedat intermediate productivity levels (e.g., Kassen et al. 2000). Theseobservations have been further mathematically elaborated usinga spatial competition model. Non-selective types of disturbances,e.g. randomly located clearings in benthic assemblages, shouldbenefit superior colonizers (i.e. inferior competitors) while theydisfavour superior competitors by reducing competitive exclusion.In contrast, higher productivity, which increases colonizationrate, encourages inferior colonizers (superior competitors) whilediscouraging inferior competitors by increasing the risk ofcompetitive exclusion. Furthermore, the model predicts thatthe separate effects of disturbance on the competitive outcomeof multi-species dynamics will mostly result in hump-shapeddisturbance–diversity relationships, while the interactive effectsof diversity and productivity will shift the diversity peak towardshigher disturbance regimes with increasing productivity levels.

Another experimental study between these two sites consistedof reciprocally transplanting hard bottom communities to assesscommunity invasibility (Antunes, 2007; Wahl et al., 2011). Forthat purpose, young (2 mo.) and old (4 mo.) communitiespreviously developed in panels at each site were transplantedat two different moments in time and assembled in a pairwisefashion with native (non-transplanted) communities and followedafterward. Similarity between native and transplanted pairs ofcommunities was estimated to assess the invasibility of eachcommunity. The results were surprising, with completely newcommunities sometimes emerging at the new site, as a resultof increased propagule survival at the new site. In AC, somepanels transplanted from GB developed into a community withalmost complete dominance (>90% cover) of the green seaweedCodium decorticatum, a species not found in native communitiesand rarely occurring in panels at the origin (GB). What preventedthe development – and possibly further expansion – of Codiumwas selective and complete removal by fish grazers in AC. Anotherspecies that persisted and even recruited at the newAChabitatwasthe invasive ascidian Styela plicata. Abundantly found throughoutGB (and in the AC harbour, but not elsewhere), it exhibited anexcellent growth at the new habitat, but again, what prevented‘‘long-term’’ (experiments lasted 6 mo.) establishment at AC wasfish consumption. In fact, some individuals persisted attached tothe backside of the panels, where they remained protected fromfish predators up to the end of the experiment, when they werecarefully removed by experimenters.

The integration of existing theoreticalmodels (WormandDuffy,2003) with the results of these experiments applied for both sites(Fig. 2) allowed us to draw some interesting conclusions: (1)disturbance, either physical (as modulated in Jara et al., 2006) orbiological (as predation in Antunes, 2007) has a unimodal influenceon diversity, and biological disturbance prevents bioinvasion orfurther expansion of newcomer species; (2) productivity (asnutrient increase or eutrophication) interacts with disturbance toinfluence diversity, and can cause a phase shift from invertebrate-dominated to seaweed-dominated communities (Jara et al.,

10 A. Soares-Gomes et al. / Regional Studies in Marine Science ( ) –

2006); this can occur in both places as a result of increasedpollution following augmented population at coastal areas;(3) the community at AC is currently clearly nutrient-limiteddespite the occasional upwelling occurrence, since total diversitydid not decrease even at the highest productivity level; (4)human-mediated transport of hard bottom invaders occurs (asshown by the species already established, by the presence ofa number of others at the AC harbour, and by transplantationexperiments) and can influence the local species pools, butcurrent levels of consumption by fish predators appear to preventbioinvasion success at AC. However, if continuous monitoring offisheries at this MER does not prevent further fishing pressure,the alleviation of predator pressure over benthic communitiescould allow the establishment of invaders with a concurrentdecrease in local diversity, endangering endemic species; (5)these pervasive processes interact with each other in a complexmanner; e.g., pollution can provide nutrients for algae to thriveover invertebrates, decreasing their relative importance, thusaffecting diversity; on its turn, decreased diversity can increaseinvasibility, thus changing the local species pool; increasedstability (i.e., decreased disturbance) can also boost invasibility.On the other hand, pollution at GB is known to increasesedimentation rates, decreasing light availability to macroalgaeand also preventing visual predators from consuming potentialinvaders arriving at this site through ship hull fouling.

This study case indicates that interactive effects of ‘bottom-up’ and ‘top-down’ processes may explain more of the variationin community diversity than the separate models. Similarly, thegeneral model can help explain and predict the future outcome ofthe benthic community in AC (and possibly in any new, recentlysettled harbours), its invasibility and how it depends on present-day conditions. These findings can have profound implicationsfor restoration of degraded reefs, management of fisheries, andthe focus on marine protected areas and biodiversity hotspotsas priorities for conservation. On the other hand, these data canprovide valuable information to prevent diversity loss in new portareas.

6. Conclusions

Guanabara Bay has a great environmental and socio-economicimportance to its catching basin municipalities. Its current state ofenvironmental degradation jeopardizes its biodiversity and posesrisks to the human populations of its surroundings, who use itswaters for leisure, transportation, or for their livelihood. Thus, therestoration of the bay ecosystem is of great importance for socio-economic, ecological, aesthetic, and public health reasons. Over thepast 20 years several bay recovery programmes were started, butthe available data hereby presented indicates that these effortsdid not achieve their goals. Remediation programmes focusedprimarily onwater quality, neglecting social and economic aspects.A clean-up programme must also improve sanitation, wastewatertreatment, collection and disposal of garbage, aswell as restorationof the original vegetation of the bay margins and rivers.

Moreover, for plans and actions to be effective, they shouldbe based on the ecological knowledge gathered during the last20 years, yielded by local universities and research institutes,filling existing knowledge gaps in an integrated manner withcurrent GB recovery actions.

It is important to implement a continuous monitoring pro-gramme in order to produce a consistent database that could thenbe used for the development of realistic remediation programmes.To build this programme, theminimumrequirementswould be thecreation of a reference group to re-evaluate periodically the pro-gramme, disseminating the results to the scientific and local com-munities, and the establishment of biological and chemical moni-toring programmes to assess the effectiveness of the bay recoverymeasures.

The programme strategy would be guided since the beginningby the participation of the scientific community from universitiesand research institutes based in Rio de Janeiro state, to assessexisting actions, expansion, and monitoring of new actions, withrepresentatives of governmental and local non-governmentalorganizations.

Appendix A. Supplementary data

Supplementary material related to this article can be foundonline at http://dx.doi.org/10.1016/j.rsma.2016.01.009.

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