teixeira thermal impact of a nuclear power plant in a coastal area in southeastern brazil

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PRIMARY RESEARCH PAPER

Thermal impact of a nuclear power plant in a coastal area

in Southeastern Brazil: effects of heating and physicalstructure on benthic cover and sh communities

Tatiana Pires Teixeira Leonardo Mitrano Neves

Francisco Gerson Arau jo

Received: 22 September 2010 / Revised: 27 August 2011 / Accepted: 23 December 2011 / Published online: 19 January 2012 Springer Science+Business Media B.V. 2012

Abstract The inuence of a nuclear power plantscooling water and physical structure on benthic coverand sh communities were assessed in a coastal area inSoutheastern Brazil. We hypothesised that thermaldischarges decrease benthic cover and consequently,change the associated rocky reef sh assemblagestructure and that physical structure is directly asso-ciated with sh richness and diversity. Twelve sites atdifferent distances (close, near and far) from thermaldischarge and types of physical structure (low andhigh) were sampled by visual census. The averagesurface temperature at the most impacted sites (close)ranged from 30.5 to 31 C, while at far sites it rangedfrom 25.5 to 28.5 C. Although thermal inuenceshave decreased benthic cover, and consequently,decreased sh richness and diversity, we found thatin near and far sites that had complex habitat structures(physical and benthic cover) sh communities wereunaffected. The greatest abundances of Eucinostomusargenteus , Mugil curema and Sphoeroides greeleyiwere associated with the highest temperatures at themost impacted sites. In contrast, Abudefduf saxatilis ,Chaetodon striatus , Stegastes fuscus , Diplodus

argenteus and Malacoctenus delalandii were moreabundant at high structured sites far from thermaldischarges. Our data support the hypothesis thatthermal discharge decreases benthic cover, sh rich-ness and diversity but physical structure, when cou-pled with high diversity and abundant benthic cover,minimised thermal effects on sh communities.

Keywords Thermal pollution Structuralcomplexity Habitat Rocky shore shes

Introduction

Temperature is a very important ecological parameterthat affects almost every aspect of aquatic life. Heatfrom the cooling water of nuclear power plantschanges the biological and ecological components of coastal area systems in an unpredictable manner.These effects depend on the quantity of heateddischarge, climate and the biological features of theenvironment (Schubel et al., 1978 ; Lardicci et al.,1999 ; Chou et al., 2004 ). Depending on the design andthe operating units of the power plants, water temper-ature in efuent sites can increase by as much as 8 C(Laws, 1993 ). Consequently in tropical oceans, sea-water temperatures can rise to 30 C or higher duringthe summer. Such high temperatures may approximateor even exceed what resident organisms can tolerate(Jokiel & Coles, 1974 ; Suresh et al., 1993 ; Wrightet al., 2000 ). Thus, condenser efuents have the

Handling editor: I. A. Nagelkerken

T. P. Teixeira L. M. Neves F. G. Arau jo (& )Laborato rio de Ecologia de Peixes, Universidade FederalRural do Rio de Janeiro, BR 465, Km 7, Serope dica,RJ 23.890-000, Brazile-mail: [email protected]

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potential to trigger thermal and chemical stress (e.g.dissolved oxygen depletion, water chlorination) andtherefore, may pose environmental problems to thereceiving water body (Krishnakumar et al., 1991 ;Chou et al., 2004 ). Tropical marine organisms areparticularly susceptible to thermal effects because the

water temperature in which they live in is generallyclose to their vital limits (Langford, 1990 ).

Several studies have assessed thermal inuence onsh, mainly in temperate areas. Some of these studiesrefer to the biological features of single species thathave been measured or observed in the eld, such asearly development and distribution (Shuter et al.,1985 ; Madenjian et al., 1986 ), reproduction (Luksiene& Sandstrom, 1994 ), and life history (Dembski et al.,2006 ). Others are restricted to laboratory experimentson thermal tolerance (Bennett & Judd, 1992 ; Mora &Osp na, 2001 ; Ospina & Mora, 2004 ). The effects of warmer temperatures on freshwater species can beboth direct and indirect, and furthermore, the magni-tude of these effects can range from minor to fullylethal (Verones et al., 2010 ). Direct effects includeincreased activity with faster digestion, which leads togreater food demand and disturbed reproduction(Sandstrom et al., 1997 ; Luksiene & Sandstro m,1994 ). Indirect effects are related to changes in foodavailability, community structure, pathogens, chemi-cal processes (modied oxygen content, increasedeffects of some pollutants) and competition with other,better adapted species (Mariazzi et al., 1992 ; Penazet al. 1999 ; Beitinger et al., 2000 ; Contador, 2005 ;Dembski et al., 2006 ; Encina et al., 2008 ; De Vrieset al., 2008 ). However, in tropical coastal systems, theinformation available on how thermal inuenceimpacts sh communities is limited (Teixeira et al.,2009 ).

Many sh food sources and shelters (e.g. corals,sponges, macroalgae) are sessile, and will be adverselyaffected because benthic species are particularly sus-ceptible to thermal discharge effects (Bamber &Spencer, 1984 ; Bruno et al., 2007 ). Accordingly, shmay not be able to avoid the indirect effects of thermalpollution, such as decreased benthic cover or even thetotal lack of benthic cover, because it is used as afeeding resource or for protection. Fish are motile, andmost can emigrate to safe areas if temperatures riseabove tolerable levels, which would ultimately changetheir community structure. Moreover, apart fromsimply leaving an area, rock-dwelling shmay respond

more subtly by changing species distribution (Rong-Quen et al., 2001 ). Furthermore, a decrease in habitatcomplexity due to thermal pollution is also expected todecrease sh richness and benthic cover and increaseopportunistic and ephemeral species, thereby changingthe population dynamics (Devinny, 1980 ; Mahadevan,

1980 ; Verlaque et al., 1981 ; Bamber & Spencer, 1984 ;Sureshet al., 1993 ; Qian et al., 1993 ; Chou et al., 2004 ).Besides benthic cover, physical structure is known toinuence sh richness because it forms a complexframework that supports a variety of microhabitats,thus increasing richness when increasing complexity(Roberts & Ormond, 1987 ; Chabanet et al., 1997 ;Ohman& Rajasuriya, 1998 ). Attributes such as numberof holes and crevices, and rock size have been used asphysical descriptors (McCormick, 1994 ). Gladfelter &Gladfelter ( 1978 ), working with coral reef communi-ties in the western Atlantic, suggested that shabundance increases with physical structure. Thespatial distribution of topographical characteristics likerock size, holes and bottom types provide organismswith food, shelter and reproductive grounds (Aburto-Opereza & Balart, 2001 ). Therefore, it is widelyaccepted that sites with high physical structure anddiverse and abundant benthic cover have increased shrichness and diversity.

In the tropics, there are few nuclear power stations,scattered throughout Mexico, India, South Africa,Argentina and Brazil, and studies on thermal inuenceon sh communities are lacking. In Brazil, there aretwo nuclear power stations that pump approximately120 m 3 s

- 1 of cooling water to generate 1,900 MW of power. These power plants use seawater from IlhaGrande Bay, an embayment area in SoutheasternBrazil, for cooling. Given that its operation is likely tomodify some physical and chemical characteristics of the local rocky shore environment, and consequentlyits biological features, it provides an interestingopportunity to evaluate thermal effects on sh com-munities. We tested the hypothesis that speciesrichness, abundance and diversity in sh communitiesare inuenced by thermal discharges, and that thephysical structure of the habitat can minimise sucheffects because it increases diversity and richness. Ouraims were to interpret the overall variation in thestructure of a rocky reef sh assemblage across athermal gradient, and to study the relationship betweenphysical structure and sh richness and abundance.We also investigated the indirect effects of water

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warming on sh as a result of the benthic covermodications.

Materials and methods

Study area

This study was conducted along a rocky shore in IlhaGrande Bay, close to the water discharge of theBrazilian Nuclear Power Plant (BNPP), which iscomprised of two power plant units. Thermal dis-charge in this area is a local anomaly that can reachsome square kilometres from the outfall (Lucca et al.,2005 ). This thermal efuent is known to produce anincrease of up to 8 C in the area of dischargecompared to the adjacent area all year round (Bandeiraet al., 2003 ).

Twelve sites were selected and classied accordingto distance from the thermal discharge: four close(\ 200 m), four near (2001,500 m) and four far([ 1,500 m) from the impact source (Fig. 1). Theclose sites were directly affected by the thermaloutfall, the near sites were still affected by outfall

because they were located in a small (2 km 2 ) embay-ment, and the far sites were located outside of theinuenced area, * 3.8 km and 9.0 km from thedischarge outfall. We chose rocky shore sites in calmwaters that were not near sandy beaches or estuarineareas.

Physical structure

Sites also varied in physical structure. Each distancelevel had two low structured and two high structuredsites. The physical structure of sites was assigneda priori as either high or low based on previousobservations of topographical complexity and sub-stratum diversity (Teixeira personal observation). Thisqualitative assignment was subsequently conrmedwith a more detailed quantitative analysis based on aphysical structure index. A housed digital camera wasmounted onto a 1-m 2 polyvinyl chloride (PVC) photoquadrat framer. Thirty photographs taken in eachsampling plot of 90 m 2 were used to quantify thevariables describing physical structure followingChapman et al. ( 1995 ). Photographs were downloadedto a personal computer, renamed with a unique site

Fig. 1 Map of the studyarea with indication of thesampling sites coded by

distance from the outfall(close, near, far) andphysical structure (low,high): CL close low, CH close high, NL near low, NH nearhigh, FL far low, FH farhigh

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code, and then cropped and colour autocorrected withimage-editing software. The number of each descrip-tor was counted in each photograph (number persquare metre).

Each site was analysed based on photographs toquantify the following physical descriptors: rugosity,

refuge size categories (holes and crevices), substra-tum, height and hard substratum. The substratumprole across the 90 m 2 transect was examined toassign a rugosity score (in this study substratum refersto sand, boulders, bare rocks and any articialstructures). Flat sandy areas were given a score of 1regardless of whether any Sargassum , lamentousalgae or sessile invertebrates were present. If thesubstratum was generally at with few bumps its scorewas 3, while a very complex substratum prole scored5. A score of 3 was assigned to substrata of interme-diate complexity. Two refuge-type categories (holesand crevices) and three size ranges ( \ 30 cm; 30 cm1 m; [ 1 m) were used following the method proposedby Aburto-Opereza & Balart ( 2001 ). Holes in rockyshores were easily measured and counted, and crevices(gaps between structures that could provide a path fora sh to escape a predator) were estimated visually.Substratum complexity was also assessed by quanti-fying rock diversity in different size categories(\ 30 cm; 30 cm1 m; [ 1 m). Habitats that had rocksin a single size category scored 1 while substratumwith all size categories present scored 5. The aim of this score was to assess the diversity of structuralattributes across habitats, which have the potential to

provide settlement areas for benthic species andresources for different sh species. Habitat architec-ture height was a subjective visual estimate todistinguish between taller ( [ 100 cm) and shorter(\ 50 cm) rocks in relation to the lowest point in thesite. The height of the habitat architecture was used as

a surrogate for the surface available for benthiccolonisation. Hard substratum referred to the percent-age of substratum that was not sand, rubble or shellsand patches. Physical structure was assessed using anindex score adapted from Gratwicke & Speight ( 2005 )(Table 1). A total score was calculated by adding thescores of each of the ve physical descriptors to givean estimate of the overall degree of complexity of thesites physical structure (Table 1). Sites that had a highphysical structure had a total score equal or greaterthan 15, and sites with a low physical structure had atotal score below 15. The majority of physicalstructure classications made a priori were in agree-ment with the physical structure index results.

Sampling

Three samples were undertaken at each site duringeach sampling occasion, between 2006 and 2008. Sitesampling was accomplished on three sampling occa-sions in each season, totalling 90 samples in the dry/ winter season and 84 in the wet/summer season,yielding a total of 174 samples. High structured sitesclose (30 samples), near (30) and far (30) from theoutfall yielded 90 samples, and low structured sites

Table 1 Physical structure score to discriminate between high and low structured sites

Physical structure score

1 3 5

Rugosity (visual topographic estimate of the substratum in each site)

Flat areasregardless of any branched algae or softcorals growing on it

Generally at with fewbumps

Very complexsubstratum prole

Number of refuge size categories: refuge(2): holes and crevices; Size classes (3):\ 30 cm; 30 cm1 m; [ 1 m)

01 24 46

Substratum complexity (number of categories): rock size classes (3):\ 30 cm; 30 cm1 m; [ 1 m.

01 2 3

Height (visual estimate of height of physical structurecm)

050 51100 [ 100

Hard substratum (%) 020 2040 [ 40

High structured sites we those that have a total score C 15, while low structured sites have a total score \ 15

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close (36), near (18) and far (30) yielded 84 samples.Some replicates were not obtained as a result of inclement weather. The factors Season and Yearwere not included in the design, because according toour observations, rocky sh in this area did not changestructure seasonally (Linear mixed models with ran-

domised sites for the Number of individuals, F 1,173 =0.08, P = 0.77; Species richness, F 1,173 = 0.008,P = 0.93) and there were not enough samples toperform comparisons by year.

Underwater visual censuses were performed bySCUBA diving and snorkelling during a censusparallel to the coastline along transects 30 m longand 3 m wide (90 m 2 ). To obtain sh information,swimming along transects was performed twice. Therst time, the observer recorded the conspicuousspecies, and the second time the observer focused thesearch beneath rocks and in all crevices to observe themore cryptic species following the procedure of Aburto-Opereza & Balart ( 2001 ). The sampling unit,number of sh per 90 m 2 , was dened as the poolednumber of conspicuous and cryptic species. Sampleswere performed in good weather and stable oceano-graphic conditions, between 9:00 and 14:00 h, duringneap tide, near quarter moon. Additionally, wemeasured the percent of benthic cover from the 30photographs taken for each site. Each photo wasanalysed for percentage cover using Count Point Coral with Excel Extensions CPCe 3.4 (Kohler &Gill, 2006 ), a software programme capable of randompoint analysis on digital photography. Twenty randompoints were generated for the photographic analysis.

Benthic cover, similar to the physical structureanalysis, was assessed based on photographs toquantify the percentage of each benthic class. Benthiccover descriptors comprised three algae divisions(Chlorophyta, Phaeophyta and Rhodophyta) and ses-sile invertebrates, mainly represented by the phylaPorifera, Mollusca (genus Petaloconchus vermitid),Echinodermata (Crinoid) and the class Anthozoa. Theclass Ascidiacea from the phylum Urochordata wasalso present. Benthic organisms, expressed as per-centage of benthic cover, were grouped in thefollowing classes (adapted from Gratwicke & Speight,2005 ): (1) Growth forms applied very generally toliving organisms such as coral, algae and otherinvertebrates that contribute to habitat complexityand support a variety of organism forms, such asbranched, cylindrical, tube and pinnate among others.

With this class we assessed the diversity of structuralattributes in habitats that could potentially provideresources for different sh species; (2) Encrustingcover referred to individuals that were encrusted inthe substratum but did not form a complex habitat;(3) Sargassum spp., common and abundant phe-

aophyta in tropical rocky shores. (4) Palythoa carib-aeorum encrusting coral; (5) Jania sp. rhodophytaalgae; and (6) Petaloconchus sp. vermitid mollusc.

During each sampling occasion, sub-surface(30 cm) and bottom (near to the bottom) watertemperature were measured in triplicate.

Data analyses

Two-way analysis of variance was used to comparewater temperature among the factor distances from theoutfall and surface versus bottom, followed by aTukey post hoc test. A principal component analysis(PCA) was performed on habitat structure descriptors(physical structure ? benthic cover) to detect siteenvironmental patterns and to assess thermal inuenceon benthic cover. Habitat structure descriptorsincluded in the PCA were the scores obtained fromphysical structure index (rugosity, refuge size catego-ries, substratum complexity, height and hard substra-tum) and benthic cover classes (growth forms,encrusting cover, Sargassum spp., Palythoa caribae-rum , Jania sp. and Petaloconchus sp.). Benthic coverdescriptors expressed as percentages were arcsine-square-root transformed, and then a log 10 ( x ? 1)transformation was applied to the whole dataset.Component loads greater than 0.5 were used toidentify latent patterns.

Two factors were tested using linear mixed models:Distance from the thermal discharge (close vs. nearvs. far), 3 levels, and Physical structure (high vs.low), 2 levels. We compared sh species richness,number of individuals, Shannon diversity index(Magurran, 1988 ), densities of the 10 most abundantspecies and benthic cover classes among the distancesfrom the outfall and physical structure (xed factors),with the sites included as a random factor. Linearmixed models take into account the nested structure of data, considering physical structure nested within thedistance from the outfall, which are nested into sites.In addition, a Tukey post hoc test was performed when H o was rejected. Prior to analysis, the data weretransformed to stabilise variances and to minimise the

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effect of abundant species (Underwood, 1997 ). Fishdata were log 10 ( x ? 1) transformed (Sokal & Rohlf,1998 ). To explore the relationship between benthiccover (independent variables) and sh abundance(dependent variables), a stepwise multiple regressionanalysis was performed.

Two-way analysis of similarity (ANOSIM) wasused to test for signicant differences in sh commu-nity structure among distance from the discharges andphysical structure. ANOSIM provides an R statisticthat reects the amount of dissimilarity associatedwith each factor. An R value close to one indicatesvery different composition, whereas values near zeroshow little difference (Clarke & Warwick, 1994 ). Toreveal the percentage contribution of each taxon toaverage similarity within each factor, we ran thesimilarity percentages (SIMPER). Analyses werebased on the Bray-Curtis measure and performed withthe computer programme PRIMER, version 5 (Clarke& Warwick, 1994 ).

Results

Temperature decreased signicantly from the close tothe far sites ( F = 32.7, P \ 0.001), and surfacetemperature was signicantly different from bottomtemperature ( F = 24.3, P \ 0.001) at the close andnear sites but not at the far sites (Fig. 2). Signicantdistance versus water column interactions ( F = 3.2,

P = 0.04) were found although these were compara-tively lower than the main effects of distance fromoutfall and depth (bottom versus surface). The highesttemperature was 36.2 C, recorded at the surface of theclose sites, and the lowest temperature was 23.9 C,recorded at the bottom of near and far sites.

All benthic cover classes changed signicantly withdistance to the thermal discharge. Branched calcareousalgae from the Jania genus ( F = 21.8, P \ 0.01) andPetaloconchus sp. vermitid ( F = 175.4, P \ 0.01)were found almost exclusively at the sites close to theoutfall. Jania species were most abundant at lowstructured sites ( F = 20.6, P \ 0.01) and the Petalo-conchus sp. vermitid was most abundant at highstructured sites ( F = 73.7, P \ 0.01). Growth formswere most abundant at sites near the outfall ( F = 29.6,P \ 0.01), with decreasing abundance at further sites.Sargassum spp. were more abundant at the far sitescompared to near and close sites ( F = 81.5,P \ 0.01). Growth forms were signicantly moreabundant at high structured sites ( F = 6.1, P \ 0.05),while Sargassum spp. did not differ in abundancebetween high and low structured sites. Encrustingcover was widely distributed at all sites irrespective of distance from the outfall but was more abundant at lowstructured sites ( F = 27.9, P \ 0.01) close and near tothe outfall ( F = 23.4, P \ 0.01), while Palythoacaribaeorum was found exclusively at the highstructured sites near and far from the outfall (Fig. 3).

The PCA showed that the high structured sites nearand far from the outfall have more complex habitatscompared to the low structured sites, and to a lesserextent, to the close high structured sites. The rst twoPCA axes accounted for 43.8% (Axis 1, 26.9%; Axis2, 16.8%) of the variance among sites. Axis 1 waspositively correlated with rugosity and height andnegatively correlated with encrusting cover and Janiasp. (Fig. 4). Axis 2 was positively correlated withPetalochonchus sp. and negatively correlated withgrowth forms and hard substratum. Sites highlystructured close to the thermal outfall correspondedto high percentages of Petaloconchus sp., while lowstructured sites close to the thermal outfall corre-sponded to high percentage of Jania sp. (Fig. 4). Onthe other hand, high structured sites near and far fromthe thermal outfall corresponded to high rugosity, hardsubstrate and height. The low structured sites near andfar from the thermal efuent had high percentages of encrusting cover and Sargassum spp.

FarNearClose24

27

30

33

T e m p e r a

t u r e

( o C )

a

d

d

bcd

bc

Fig. 2 Box and whisker plot of variation in surface ( whiteboxes ) and bottom ( black boxes ) water temperatures amongdistance from the outfall categories. Letters indicate signicantdifference levels from ANOVA at P \ 0.05

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A total of 57 sh species comprising 32 familieswas observed. A member of the Haemulidae family( Haemulon steindachneri ), a common group of coastal

sh, was the most abundant species ( [ 9 individu-als 9 90 m

- 2 ) and was widely distributed across allsites. The 20 most abundant species accounted for97% of the total number of individuals and had anoccurrence higher than 1% throughout all sites.

Theve most abundant speciesat closeand near sites

accounted for 89% of the total number of individuals(each with a frequency of occurrence [ 4%) and were, indecreasing order: the gerreid Eucinostomus argenteus ,the haemulid H. steindachneri , the pomacentrid A. saxatilis , the haemulid Haemulon aurolineatum ,and the mugilid M. curema . Conversely, the ve mostabundant species at sites far from the outfall, whichcontributed to 81% of thetotalnumber of sh (each witha frequency of occurrence [ 4%) were, in decreasingorder: A. saxatilis , H. steindachneri , H. aurolineatum ,the sparid Diplodus argenteus and the territorialistpomacentrid Stegastes fuscus .

Species richness increased signicantly with dis-tance from the outfall ( F = 15.8, P \ 0.01) withhigher values at near and far sites compared with theclose sites. Moreover, the high structured sites hadhigher species richness ( F = 9.8, P \ 0.01) comparedwith the low structured sites (Fig. 5a). The meannumber of individuals (density) did not differ accord-ing to both the distance from the outfall and physicalstructure (Fig. 5b). Similarly to species richness, theShannon diversity index differed among distance(F = 9.1, P \ 0.01) and physical structure ( F = 5.1,P \ 0.01) (Fig. 5c).

0204060 Growth forms

0204060

B e n

t h i c c o v e r

( % )

Encrusting cover

020

4060

Palythoa caribaeorum

Sargassum spp.

Close Near Far0

20

40

0102030

Jania sp.

0

204060

Petaloconchus sp.

Fig. 3 Mean percent of benthic cover ( SE) among thethermal gradient (close, near, far) and physical structure ( whiteboxes low, black boxes high)

Sargassum spp.

Petaloconchus sp.

Substratumcomplexity

Refuge size categories

Palythoa caribaeorum

Jania sp .

Encrusting cover

Growth formsHard substratum

RugosityHeight

-2

-1,5

-1

-0,5

0

0,5

1

1,5

2

2,5

3

-2 -1 0 1 2 3 4

CLCHNLNHFLFH

Fig. 4 Distribution of sampling points on the rsttwo axes of the PCA basedon habitat structuredescriptors(physical ? benthic cover)according to distance fromoutfall ( open circle close,open triangle near, opensquare far) and physicalstructure ( white low, black high)

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Nine ( E. argenteus , M. curema , S. greeleyi , A. saxatilis , D. argenteus , S. fuscus , H. aurolineatum ,C. striatus and Malacoctenus delalandii ) of the mostabundant species differed signicantly among thedistances from the outfall and six ( M. curema , A. saxatilis , S. fuscus , H. aurolineatum , C. striatusand M. delalandii ) differed between physical structure.E. argenteus (F = 5.1, P \ 0.01) and M. curema(F = 7.1; P \ 0.05) had higher abundances at theclose sites compared with near and far sites. Thepuffersh Sphoeroides greeleyi had higher abundanceat the sites close to and near the outfall ( F = 17.7,P \ 0.01) compared with the far sites. In contrast, A. saxatilis (F = 33.3, P \ 0.01), D. argenteus , (F =9.8, P \ 0.01), S. fuscus (F = 66.0, P \ 0.01), thebutterysh Chaetodon striatus (F = 36.4, P \ 0.01)and the cryptic scaled blenny Malacoctenus delalandii(F = 29.1, P \ 0.01) were signicantly more abun-dant at sites far from the outfall. H. aurolineatum wasthe only species to have signicantly higher abun-dance at the near sites ( F = 6.2, P = 0.01).

Abudefduf saxatilis (F = 10.3, P \ 0.05), S. fuscus (F = 82.1, P \ 0.01), C. striatus (F = 10.9,P \ 0.01) and M. delalandii (F = 23.2, P \ 0.01)were signicantly more abundant at the high struc-tured sites, while H. aurolineatum (F = 13.6, P \0.01) was more abundant at the low structured sites

(Fig. 6).When exploring the relationship between habitat

structure (physical structure and benthic cover),species richness, number of individuals, Shannonindex and abundance of the 10 most numerous species(Table 2), we found that with the exception of numberof individuals and abundance of H. steindachneri , allsh variables showed signicant dependency onhabitat structure, save for one species ( H. aurolinea-tum ) in which the proportion of variance explainedwas below 10%. The multiple regression analysis of species richness and diversity index, H 0, accounted for26 and 19% of the variation of their estimated values,respectively. Twenty-six percent of total variation inspecies richness was explained by the variation inPetaloconchus sp., Jania sp. (negative relationship)and Palythoa caribaeorum and growth forms (positiverelationship) (Table 2). Species abundance was gen-erally higher in those sites with more P. caribaeorumand Sargassum spp. cover (e.g. A. saxatilis , C. striatus , M. delalandii and S. fuscus ). In the case of E. argenteus and M. curema (positive relationship)and A. saxatilis (negative relationship), Petaloconchussp. explained most of the variance.

Signicant differences in the sh communityamong the distances from the thermal outfall weredetected by ANOSIM ( R global = 0.427; P \ 0.01),indicating shifts in the structure of the commu-nity. As expected, the largest difference was foundbetween the close and far sites ( R = 0.648), butsignicant differences, although of smaller magni-tude, were also found between the close and near( R = 0.366; P \ 0.01) and between the near and far( R = 0.209; P \ 0.01) sites. Furthermore, a lowsignicant difference ( R global = 0.101; P \ 0.01)was also found between the high and low structuredsites. An increased number of typical species wasdetected at the far sites from the thermal outfall (8species), whereas the sites close to the outfall werecharacterised by four species only (Table 3). Thelow structured sites had a lower number of speciesthat contributed to mean within-group similaritythan the high structured sites.

0

2

4

6

8

10

12

R i c h n e s s

0

25

50

75

100

125

150

I n d i v i d u a

l s x

9 0 m

2

Close Near Far0.0

0.5

1.0

1.5

S h a n n o n

( H ' )

a

b

c

Fig. 5 Mean ( SE) of sh species richness, number of individuals and Shannon diversity index among the thermalgradient (close, near, far) and physical structure ( white low,black high)

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Discussion

Thermal discharges from the Brazilian cooling waternuclear power plants alter sh composition and habitatstructure, and this factor was more inuential on shassemblages than the physical structure of surrounding

habitats. Three species were directly associated withthe most thermally impacted sites (close to and nearthe outfall) namely, E. argenteus , M. curema andS. greeleyi , but only the latter is a true rocky shorespecies. E. argenteus was the species that tolerates themost thermal stress, because it was highly abundant at

sites that were close to the outfall. Our nding thatspecies were less abundant at sites under ther-mal pollution coincides with the pattern reported byRong-Quen et al. ( 2001 ), who conducted a 21-yearstudy (19791999) on reef sh communities near anuclear power station in southern Taiwan. Mora &Osp na (2001 ) determined the critical thermal maxi-mum of reef sh from the tropical eastern Pacic andfound that some species are able to colonise hightemperature habitats, such as Haemulon steindachneri(36 C), Mugil curema (40.8 C) and Eucinostomusgracilis (38 C). In this study, a similar tolerancepattern was found for Haemulon steindachneri , M. curema and a Eucinostomus species (not E.gracilis ). These species had a high occurrence atimpacted sites and were abundant mainly at thosesites, suggesting a preference for areas with hightemperatures. The abundant E. argenteus and M. cur-ema have been reported mostly in sandy banks andmuddy at areas, respectively (Benetti & Neto, 1991 ;Alvarez-Lajonchere et al., 1992 ; Chaves & Otto, 1999 ;Gaelzer & Zalmon, 2003 ). These species are probablyalready adapted to living in high temperature areas andas a consequence, they can use the resources availablein these areas, whereas other species cannot subsist inhigh temperatures at all.

As a result of living in areas impacted by thermalinuence, sh can alter their behaviour. For instance,some studies on thermal inuence have focused onaspects of reproductive biology. Increased tempera-ture can have positive or negative effects on repro-ductive capacity depending on whether the species isnear its optimal thermal point (Munday et al., 2008 ).Ruttenberg et al. ( 2005 ) found that egg production inStegastes beebei is optimal at 25 C and decreases to avery low production rate at either 20 or 27 C. Thissuggests that with only a few degrees of temperaturedifference the reproductive success of a given speciescan signicantly decrease. One possible strategy forcircumventing this problem is to change the timing of reproduction.

Some information on the inuence of thermaldischarge on freshwater sh from temperate areas is

Close Near Far0,1

110

100 A. saxatilis

0,11

10100 D. argenteus

0,11

10100 S. fuscus

0,11

10100 C. striatus

0,11

10100

I n d i v i d u a

l s x

9 0 m 2

M. delalandii 0,1

110

100 H. aurolineatum

0,11

10100 H. steidacneri

0,11

10100 S. greeleyi

0,11

10100 M. curema

0,11

10100 E. argenteus

Low High

Fig. 6 Mean abundance for the ten most numerous species( SE) along the thermal gradient (close, near, far) and physicalstructure ( white low, black high)

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available. Luksiene & Sandstro m (1994 ) found that Rutilus rutilus fail to recruit in areas that are exposedto thermal discharge from a nuclear power station inSweden. Madenjian et al. ( 1986 ) found a decreasedabundance of Alosa pseudoharengus and Perca avescens at a nuclear power plant on Lake Michiganwhen compared to a reference condition. Negativeeffects of thermal inuence on the growth and thespawning period of Micropterus dolomieu were foundfor the Dore Bay in Lake Huron (Shuter et al. 1985 ).

We also found that physical structure plays animportant role in sh species composition and distri-bution along the thermal gradient that seems to havemore relevance at sites far from the thermal outfall.For example, higher occurrences and abundances of S. fuscus , A. saxatilis , C. striatus and M. delalandii werefound only at high structured sites far from the outfall.This can be attributed to the high physical structureand benthic cover found in these areas. These speciesare cryptic or territorial and habitat complexity is an

Table 2 Summary of the results of multiple linear regression analyses for sh assemblage structure and abundance of the 10 mostnumerous species, indicating the benthic cover independent variables included in each model and the sign of their relationship

Variable Adj. R2 P Variables included in the model

Species richness 0.26 *** - Petaloconchus sp.**- Jania sp.*

? Palythoa caribaeorum**? Growth forms**

Number of individuals 0.03 * - Jania sp.*

Shannon diversity index 0.19 *** ? Palythoa caribaeorum**? Growth forms*

Eucinostomus argenteus 0.37 *** ? Petaloconchus sp.**? Encrusting cover*

Mugil curema 0.18 ** ? Petaloconchus sp.**

Sphoeroides greeleyi 0.19 ** - Sargassum spp.**- Palythoa caribaeorum**

Abudefduf saxatilis 0.30 *** - Petaloconchus sp.*

? Palythoa caribaeorum**? Sargassum spp.**? Growth forms**

Haemulon steindachneri 0.04 * ? Palythoa caribaeorum**? Growth forms**

Diplodus argenteus 0.20 ** ? Sargassum spp.**- Petaloconchus sp.**

Stegastes fuscus 0.38 ** ? Palythoa caribaeorum**? Sargassum spp.**? Growth forms**? Encrusting cover**

Haemulon aurolineatum 0.07 ** - Petaloconchus sp.*? Sargassum spp.*

Chaetodon striatus 0.17 *** ? Sargassum spp.**? Palythoa caribaeorum**? Growth forms*? Encrusting cover*

Malacoctenus delalandii 0.18 ** ? Palythoa caribaeorum**? Sargassum spp.**

ns not signicant; * P \ 0.05, ** P \ 0.01, *** P \ 0.001

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important factor providing shelters, feeding andreproductive grounds (Ferreira et al., 2001 ). In con-trast, warm-water species such as E. argenteus , M. curema and S. greeleyi , and species that occurredmainly at far sites, such as D. argenteus , seemed to notbe inuenced by physical structure.

Physical structure is closely related to sh species

richness (Letourneur, 1996 ; Friedlander & Parrish,1998 ; Grober-Dunsmore et al., 2008 ) because itprovides shelter opportunities and places for sh toreproduce. Several studies (O hman & Rajasuriya,1998 ; Aburto-Opereza & Balart, 2001 ; Garc a-Charton et al., 2004 ; Tittensor et al., 2007 ) havereported the effects of habitat structure on shcommunities, but most of them fail to discriminatethe particular inuence of either physical structure orbenthic cover. In this study, sites classied as highlystructured had more structural complexity and showed

greater rugosity and height than the other sites. Theywere comprised of more physical structures, such asrocks of different sizes, holes and crevices. Thesefeatures were closely related to higher sh richnessand abundance as compared to the low structured sites.

Structural complexity per se, aside from the ben-ets that structure can provide such as shelter orincreased surface area for accumulation of food, maynot be greatly attractive to juvenile sh (Laegdsgaard& Johnson, 2001 ). However, these benets can be

important for habitat selection for certain species.Cabaitan et al. ( 2008 ) found that adding live corals toconsolidated dead corals increased juvenile sh col-onisation, with these patches acting as true articialreefs to concentrate organisms. Friedlander & Parrish(1998 ) reported that physical structure and speciesabundance are weakly correlated, while Gladfelter

et al. ( 1980 ) suggested that the abundance of coral shincreases with structural complexity. Therefore, phys-ical structure, when coupled with diverse benthiccover, provided the best conguration for supporting arich and diverse sh community, as it was observed atthe high structured sites far from the outfall.

High sh richness was found at high structured sitesnear to the outfall. This suggests that the thermalplume was restricted to the more supercial layers. Asmall difference (about 2 C) between surface andbottom water temperatures seemed not to affect

benthic cover, and consequently, sh species richness,which was favoured by high habitat complexity.Thermal discharge affected habitat structure moreintensely at the sites close to the outfall, which had lowbenthic cover. In these sites, a few organisms werefound, such as vermetid molluscs of the Petalocon-chus genus and calcareous algae of the Jania genus.Therefore, low richness at the most impacted sites wasassociated with thermal inuence, and consequently,low benthic cover, which limited feeding resource

Table 3 Contribution made by each species to the overall measure of similarity within the factor (distance from the outfall andphysical structure)

Distance from the outfall Physical structure

Similarity average (%) Close Near Far Low High37.49 40.10 34.31 27.39 30.93

Eucinostomus argenteus 56.94 11.64 29.45 12.49Sphoeroides greeleyi 17.82 9.25 10.14 8.31

Haemulon steindachneri 10.15 32.96 18.03 22.65 24.02

Mugil curema 6.85 3.27

Abudefduf saxatilis 25.53 40.98 18.41 31.35

Diplodus argenteus 5.50 8.92 3.00

Haemulon aurolineatum 4.74 6.20 9.64

Serranus aviventris 2.83

Stegastes fuscus 7.76 7.84

Chaetodon striatus 4.17

Malacoctenus delalandii 3.56

Halichoeres poeyi 2.11

Only species contributing to more than 2% similarity according to SIMPER are shown

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availability. Furthermore, sh abundance was high atthe sites close to the outfall, indicating that tolerantspecies can take advantage of such unoccupied nichesand increase in number. Overall, to support high shrichness and abundance, high benthic cover and largerocky areas are required; a notion corroborated at the

high structured sites near and far from the outfall.Lardicci et al. ( 1999 ), studying thermal discharges

on the spatial distribution of meiobenthic and macro-benthic communities in Follonica Gulf (WesternMediterranean), found that thermal efuent did notinuence benthic community distribution. On theother hand, Vilanova et al. ( 2004 ), working in thesame area as this study, found differences in richnessand abundance of sponge communities between anarea under thermal inuence from the BNPP and acontrol area. Overall, sessile benthic organisms havebeen recorded as being susceptible to thermal efuent,and an increase by a few degrees can jeopardise theirsurvival (Laws, 1993 ; Logue et al., 1995 ), as wasobserved at the sites close to the outfall. This suggeststhat thermal pollution is the main limiting factor forthe composition and abundance of benthic communi-ties. In this study, most of the algae species wereincrustant and lamentous with limited capacity toform banks and complex patches. Even the growthforms species had a small size (height aver-age = 15 cm, T. P. Teixeira personal observation)with low contribution to structural complexity. Veg-etated areas are attractive for sh because they areused as feeding resources and refuge against predators.Conversely, unvegetated areas usually have low shabundance and diversity (Robertson, 1984 ; Bell et al.,1987 ; Ornellas & Coutinho, 1998 ). Several plants areassociated with high diversity of invertebrates, andthey are an important part of the diet of juvenile sh(Lubbers et al., 1990 ; Schneider & Mann, 1991 ).Zalmon et al. ( 2002 ), working with articial reefs,detected that increased species richness of the reef shcommunity may be related to the gradual developmentof a fouling community on the rocky structure.

In this study, we conrmed the inuence of thermalpollution on the biota. However, little information isavailable on the effects of the damage caused by hightemperatures on the distribution of sh in tropicalareas, and the present ndings can provide relevantinformation for mitigating the potential impactscaused by this kind of anthropogenic inuence thatis becoming very common in developing countries.

Other natural environmental stressors not accountedfor in this study (e.g. predation, limitation in foodavailability) and human disturbance (e.g. sheries,pollution, increased ow near to the outfall, waterchlorine discharges), may also play an important rolein structuring sh communities. For instance, chlorine

is added to the power station cooling water forantibiotic purposes (Jenner et al., 1997 ), and chlori-nation by-products (CBPs) may act as biocides oncethe water is introduced into the ocean.

Overall, the sites close to the thermal dischargewere more heavily impacted by thermal pollution,reected by low benthic cover, and consequently, lowsh richness, where opportunist and tolerant speciesdominated. On the other hand, areas that were lessimpacted were colonised by typical rocky shorespecies. The more structured sites minimised thethermal inuence, as was observed at some sites nearthe thermal discharge that had benthic cover and a shcommunity that was relatively unaffected.

We have provided basic information for environ-mental managers to minimise the inuence of thermalpollution and to contribute to the knowledge of changes in habitat structure and sh communities inthermally impacted coastal tropical areas. Environ-mental policies should consider that the effects of cooling water from nuclear power plants can beminimised by increasing the complexity of physicalstructures at some hundreds of metres away from thedischarges, where, as we report in the study, benthiccover can develop. In such cases, the thermal plumemay be restricted to the surface layers making thethermal effects less harmful for sh communities.

Acknowledgments We thank Hamilton Hissa Pereira andRafael Jardim Albieri for their help in the eld work, and totechnical staff of the Laboratory of Fish Ecology, UniversityFederal Rural of Rio de Janeiro for useful help in the laboratory.This study was partially nanced by CNPqBrazilian NationalCouncil for Research Development (Proc. 302555/2008-0).

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