Spatial patterns of distribution and the influence of seasonal and abiotic factors on demersal

26 Pages·2016·1.9 MB·English

JournalofFishBiology(2016)89,821–846
doi:10.1111/jfb.13033,availableonlineatwileyonlinelibrary.com
Spatial patterns of distribution and the influence of seasonal
and abiotic factors on demersal ichthyofauna in an estuarine
tropical bay
D. R. da Silva Jr.*†, R. Paranhos‡ and M. Vianna*
*Federal University of Rio de Janeiro, Institute of Biology, Department of Marine Biology,
Laboratory of Fisheries Biology and Technology, CCS, Bl. A, 21949-900, Cidade
Universitária, Ilha do Fundão, Rio de Janeiro, Brazil and ‡Federal University of Rio de
Janeiro, Institute of Biology, Department of Marine Biology, Laboratory of Hydrobiology,
CCS, Bl. A, 21949-900, Cidade Universitária, Ilha do Fundão, Rio de Janeiro, Brazil
This study focused on the influence of local-scale environmental factors on key metrics of fish
communitystructureandfunctionatGuanabaraBay,anestuarinesystemthatdiffersfromallother
south-western Atlantic estuaries due to the influence of an annual low-intensity upwelling event
duringlatespringandsummer,betweenNovemberandMarch,whenawarmrainyclimateprevails.
Thespatialpatternsofthebottomtemperatureandsalinityweremoreheterogeneousduringtherainy
seasonthanthedryseason,beinglinkedtototalprecipitationandseasonaloceanographicevents.The
studyidentified130speciesand45families,placingGuanabaraBayasoneofthemostspecies-rich
tropicalestuarineecosystems,farexceeding22otherBrazilianestuaries.Theseresults,inadditionto
characteristicssuchasarelativelywell-preservedmangroveforest,highproductivityandfavourable
conditionsforthegrowthandreproductionofestuarinespecies,indicatethatGuanabaraBayplaysa
centralroleinsupportinglargepopulationsoffishes,includingcommerciallyimportantspecies.
©2016TheFisheriesSocietyoftheBritishIsles
Keywords:environmentaldrivers;estuarinefunctionalgroups;estuary;fishfaunalrichness.
INTRODUCTION
Estuariescomprisealmost13%ofallmarinecoastalenvironmentsandgiventheirpar-
ticular attributes, including high primary and secondary productivity, warm shallow
waters and key ecological resources including shelter and protection and food avail-
ability,thesehighlydynamicecosystemssustainlargenumbersoffishspecies,(Thiel
etal.,2003;McLusky&Elliott,2004;Elliottetal.,2007).Thesecharacteristicsgive
estuariesafundamentalroleinregionalichthyofaunadynamics,functioningasgrowth
sitesformanymarinespeciesandreproductionareasforestuarinespecies.
Sinceestuariesexperiencemajorshiftsinenvironmentalconditionsovershortperi-
ods, one of the classical hypotheses is that water variables are the principal drivers
that shape the patterns of species distribution and composition (Maes etal., 2004).
Therefore, determining how the ichthyofauna responds to these factors is among the
†Author to whom correspondence should be addressed. Tel.: [phone]; email: demarques-
[email protected]
821
©2016TheFisheriesSocietyoftheBritishIsles
822 D. R. DA SILVA ET AL.
centralgoalsofestuarinefishecology.Studiesonmanyofthesesystemshaveidenti-
fiedtemperature,freshwaterinput,salinity,dissolvedoxygenandtransparencyasthe
main environmental drivers (Thiel etal., 2003; Maes etal., 2004; Akin etal., 2005).
Asestuariesarehighlydynamicecosystems,however,therelativeweightofthesefac-
torsdifferstosomedegree,evenamongneighbouringestuaries,whichcreatestheneed
forlocalcase-by-casestudiesoftherolesofabioticfactors(Blaber,2013).
The available information on the ecology and dynamics of ichthyofaunal assem-
blagesinSouthAmericanestuariesandmarineecosystemsisconcentratedinrelatively
few coastal areas [e.g. Caeté, Goiana and Sepetiba Bay, tropical estuaries from the
northern, north-east and south-east coasts of Brazil; Patos Lagoon, Guaratuba and
Paranaguá, subtropical estuaries from the southern coast of Brazil; La Plata, a sub-
tropicalestuaryfromthesouth-westAtlanticcoastofArgentina;Barlettaetal.(2010)],
andafewstudieshavebeenconductedrecentlyinGuanabaraBay.Together,theycover
thefollowingtopics:ichthyoplanktoncompositionandvariability(Kraus&Bonecker,
1994; Castro etal., 2005), fisheries (Jablonski etal., 2006) and ichthyofauna spatial
andtemporaldynamics(Rodriguesetal.,2007;Silvaetal.,2007;Vasconcellosetal.,
2007,2010,2011;Andrade-Tubinoetal.,2009;Silvaetal.,2013).Thereis,however,
considerablelackofinformationaboutthefishfauna,includingbasicinformationsuch
asspeciesoccurrence,patternsofoccupancy,andestuarineuse.
Guanabara Bay is of immense ecological, social and economical importance for
the south-eastern region of Brazil, strategically located adjacent to one of the most
industrializedregionsofthecountryandundertheinfluenceofnumerousfishingand
commercial port facilities, in addition to ship yards and oil refineries. Regardless of
its history of environmental depletion as a result of diverse anthropogenic activities,
thebaystillexhibitscharacteristicsofatypicaltropicalestuary,includingarelatively
well-preserved mangrove forest, high productivity and favourable conditions for
growth and reproduction of estuarine species (Blaber, 2000). Therefore, it continues
tosustainimportantfisheriesandalargenumberoffishers(Jablonskietal.,2006).
To improve the knowledge of the ichthyofaunal dynamics in Guanabara Bay, the
present study adopted a narrow approach, focusing on the influence of local-scale
environmental factors on key metrics of community structure and function, such as
estuarineuse.Theobjectiveswereto(1)describethespatialdistributionoflocalfishes
inthebay,particularlythedemersalichthyofauna,basedonimportantcommunitymet-
ricsandecologicalfeaturessuchasfeeding-mode,habitatandestuarine-usefunctional
group and (2) elucidate the influence of seasonal factors on the fish community of
GuanabaraBay.
MATERIALSANDMETHODS
STUDY AREA
GuanabaraBayisasemi-enclosedtropicalbaylocatedonthesouth-easterncoastofBrazil,
inthecentreofadenselyurbanizedandindustrializedareaofthemetropolitanregionofRio
deJaneiro(Baptista-Netoetal.,2006)(22∘41′–22∘03′S;043∘16′–043∘01′W)(Fig.1).Itis
oneofthelargestestuarinesystemsontheBraziliancoast(381km2),surroundedby16cities,
andthedrainagebasin(4081km2)containsatotalof91riversandcanals.Regionalclimateis
humidtropical,with twomainseasons:warm rainy(DecembertoMarch)andcolddry(July
toAugust) (Paranhos& Mayr,1993).Thesemi-diurnal tide fluctuates0·7m onaverage.The
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846
ICHTHYOFAUNA OF ESTUARINE TROPICAL BAY 823
(a) (b)
680 000 685 000 690 000 695 000 700 000 0 680 000 685 000 690 000 695 000 700 000 0
0 0
0 0
Duque de Caxias Magé BG-24 490 Duque de Caxias Magé 490
7 7
BG-20 BG-22
Paquetá Island
BG-31 BG-26 Paquetá Island 00 00
0 0
3 3
BG-29BG-28 Upper bay BG-17 7 48 Duque de Caxias 7 48
BG-16
GBoGv-e34rnador IBslGa-n1d0 BG-13BG-12BG-11 BG-15São Gonçalo 7 476 000 Governador Island Central CGharandnieml São Gonçalo 7 476 000
BG-09
Governador Island
BG-07 00 00
0 0
9 9
C.PL.o Rwieor dbea yJaneiro - Praça Mauá 7 46 C.P. Rio de Janeiro - Praça Mauá 7 46
BG-04 BG-03 Niterói Niterói
Rio de Janeiro BG-02 BG-01 00 Rio de Janeiro Entrance 00
0 0
2 2
Seaward end 7 46 Seaward end 7 46
N N
0 2·5 5 10 SAD 1969 UTM Zone 23S 0 2·5 5 10 SAD 1969 UTM Zone 23S
km km
Fig. 1. (a)Environmentalsamplingpointsand(b)ichthyofaunasamplingsitesinGuanabaraBay,RiodeJaneiro.
Bottomwatervariablesweresampledevery15daysfor24months(July2005toJune2007).
seaward end (lower bay, euryhaline) is narrow (1·6km) and has the strongest tidal currents,
reaching1·6ms−1(SEMADS,2001).Inthissectionofthebay,theinfluenceofcoastalwaters
ismaximumandtheeffects(highersalinityandlowertemperatures)extendthroughthelong
centralchannel(18km;maximumdepthof50m)towardstheupperbay.Inthemiddleandupper
bays(exceptthecentralchannel),areasdepthsare<10mandextensiveshallowmudbanksexist.
Inthesesections,specificallythoseclosetoGovernadorIslandandthecitiesofDuquedeCaxias,
MagéandSãoGonçalo,theinfluenceofcontinentaldrainageisgreater,imposingmesohaline
topolyhalinecharacteristicsduringtherainyseasonandeuryhalineonesinthedryseason.
Inadditiontothenaturalgradientfromoceanictocontinentalwaters,GuanabaraBayexhibits
a water quality gradient, as pollution loads undergo different degrees of dilution (Paranhos
etal.,1998).Thisconditionisessentiallyattributedtohighsedimentationratesassociatedwith
landfills,whichhaveledtosevererestrictionofwatercirculationandincreasingwaterturnover
time (Amador, 1980) in the middle and upper bays (except central channel). On the other
hand, bathymetric profiles of the central channel show it contributes to a high water renewal
promotedbytidalcycles.Theinnerpartsofthebayexhibitthepoorestwaterquality,especially
thenorth-westernside,giventhehighlyurbanizedandindustrializeddrainagebasincomposed
oftheSãoJoãodeMeritiRiverandtheSarapuíRiver(Baptista-Netoetal.,2006;Kalasetal.,
2009). On the opposite shore, the north-eastern portion is better preserved because of the
integrity of the drainage basin of the Guapimirim Environmental Protection Area (Ribeiro &
Kjerfve,2002).
Intherainyseason,GuanabaraBayisinfluencedbyanannuallow-intensityupwellingevent
duringlatespringandsummer(NovembertoMarch).Thisperiodischaracterizedbyanincrease
ofnorth-eastwindsthatbringSouthAtlanticCentralWater(SACW)tothesurface100kmnorth
ofthebayentrance,establishingsubtropicalandtemperatecharacteristicsfortheRiodeJaneiro
∘ ∘
coast,withtemperaturesbetween10 and20 C(Matsuura,1986;Barlettaetal.,2010).Oceano-
graphiccharacteristicsthatopposethetypicalinfluenceoftropicalwaters(temperature>20∘C
andsalinity>36;Matsuura,1986)aredrivenbytheBrazilcurrentduringtherestoftheyear
(Brandini,1990).
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846
824 D. R. DA SILVA ET AL.
ENVIRONMENTAL DRIVERS
Precipitationandwatervariableswereassessedinordertoinvestigatethespatialandtemporal
patternsofthedemersalichthyofauna.Precipitationwasevaluatedforeachmonth,basedontwo
categories defined by Walter & Lieth (1967) indicating dry and rainy months based on mean
temperatureandtotalprecipitation.DataforbothfactorswereobtainedfromtheC.P.Riode
Janeiro,PraçaMauáweatherstation.Bottomwatervariablesweresampledevery15daysduring
a24monthperiod,fromJuly2005toJune2007,at21pointsacrossGuanabaraBay[Fig.1(a)]
andanalysedbystandardoceanographicmethods(Grasshoffetal.,1999).Watertemperature
wasmeasuredwithagraduatedthermometer(∘C).Salinityanddissolvedoxygen(DO;mgl−1)
wereevaluated,respectively,bythechlorinityandWinkler-azidemethods.Inorganicnutrients
were also analysed: ammonium nitrogen by indophenol (𝜇M), and total phosphorus by acid
digestiontophosphate(𝜇M).
FISH SAMPLING
Fish surveys were conducted under the authorisation of SISBio (Sistema de Autorização e
InformaçãoemBiodiversidade,‘AuthorizationandInformationSystemonBiodiversity’)No.
055,5December2005.Thesameperiodicityofevery15dayswasadoptedforfishsampling
during a 24month period (July 2005 to June 2007) in six areas [Fig. 1(b)]. Each sampling
area was evaluated by means of two to four hauls made during the day, at a constant speed
[2·8–3·7kmh−1 (1·5–2·0 knots)], for 30min, using a typical boat of the local artisanal fleet,
andtheGPSco-ordinatesofthebeginningandtheendofsamplingwererecorded.Thetrawl
netwas7mlong,witha14mgroundropeanda18mmmeshcodend.Allfisheswerecounted,
identified, measured to the nearest 0·1cm (total length, L ) and weighed to the nearest 0·1g.
T
No sub-sampling method was employed. The catch per unit effort (CPUE) was used to esti-
mate abundance (number of individuals=0·5h−1) for all analyses, given the consistency of
thesamplinggearandfieldmethods.Threeotherunivariatemeasurementsregardingcommu-
nitystructureweredetermined:speciesrichness(totalnumberofspecies,S);Shannondiversity
index(H′)andPielouequitability(J)(Margalef,1974).Complementarybiologicalfeaturesof
thefeeding-modefunctionalgroup,habitatandestuarine-usefunctionalgroupwereassessedfor
eachspeciesthroughspecializedreferences(Cervigón&Fischer,1979;Menezes&Figueiredo,
1980; Randall, 1983; Marceniuk, 2005). The classification followed the definitions of Elliott
etal.(2007).
DATA ANALYSIS
Environmentaldatawereanalysedasmeans±s.d.,minimumandmaximumvaluesforeach
site.At-testwasusedtoverifythedifferenceofmeanprecipitationbetweenseasons.Fishmea-
surements(eachhaulwastreatedasasample)weretestedfornormality(Kolmogorov–Smirnov
test)andhomoscedasticity(Levene’stest)andthenevaluatedbytwo-wayANOVAwithoutdata
transformation.ATukeyposthoctestwasusedtoassessthevariabilityofthesemeasurements
(Zar, 1999), considering the spatial (areas: six levels, fixed) and seasonal patterns (precipita-
tion: two levels, random). Next, fish patterns were explored using a correspondence analysis
(CA),followedbyacanonicalcorrespondenceanalysis(CCA)inordertoscreenfortheenvi-
ronmental variables that best explained the ichthyofauna distribution and seasonality. Not all
speciescapturedwereemployedintheanalyses.Becauseofthetypeofsamplinggearusedin
thisstudy,thosespeciesthatwereconsideredasbeingpelagicorstrictlyassociatedwithhard
bottoms were removed from the analysis, focusing the investigation on the soft-bottom fish
community.AnothercriterionspecificallyemployedintheCAandCCAwasthetotalindexof
relative importance (I ) (Selleslagh & Amara, 2008). This analysis was carried out only for
RI
thedominantspeciesduringthestudyperiod,i.e.thosethatindividuallycontributed>0·1%of
theI .Thisapproachremovesrarespeciesthatincreasenoise,andaffectsonlythetotalvari-
RI
ationexpressedbytheeigenvalueswithoutalteringtheinterpretationofresults.Analyseswere
performed using the programmes Statistica 7.1 (StatSoft; www.statsoft.com) and PC-ORD 4
(McCune&Mefford,1999).Asignificancelevelof0·05wasusedinalltests.
Additionally, Kriging and Co-Kriging geostatistical techniques (Matheron, 1971) were
employedtoexplorethespatialorganizationoffishmetrics(abundance,richnessanddiversity)
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846
ICHTHYOFAUNA OF ESTUARINE TROPICAL BAY 825
40 80
30 60 m)
Temperature (° C) 20 No data available 40 al precipitation (m
10 20 Tot
0 0
July August September October November December January February March April May June July August September October November December January February March April May June
2005 2006 2007
Fig. 2. Climatediagram[temperature( )andtotalprecipitation( )]basedonthemethodologyofWalter
&Lieth(1967).DataobtainedfromtheC.P.RiodeJaneiro–PraçaMauáweatherstationduringthestudy
period(July2005toJune2007).Duetotechnicalproblems,itwasnotpossibletoobtainrainfalldatafor
December2006andJanuary2007.
acrossGuanabaraBay.Eachareawasevaluatedbyasetof28–64datapointsforeachfishmet-
riccalculatedforalocationx,wherexisdefinedbylatitudeandlongitudeinatwo-dimensional
space. All interpolation models were submitted to validation by the method of leave-one-out
(Isaaks & Srivastava, 1989). Models were generated by the programme ArcMap 10.0 (ESRI,
2010).
RESULTS
CHARACTERIZATION OF ENVIRONMENTAL PATTERNS
BasedontheclimatediagramofWalter&Lieth(1967),onlysevenofthe24months
were considered as dry periods: August 2005, March 2006, July 2006, August 2006,
March2007,April2007andJune2007(Fig.2).Itwasnotpossibletoobtainrainfall
dataforDecember2006andJanuary2007duetotechnicalproblems,butthosemonths
wereconsideredasrainyperiods(Paranhos&Mayr,1993;Kjerfveetal.,1997).During
thesemonths,themeanprecipitationwas30·1±19·1mm,avaluestatisticallydifferent
(P<0·05)fromtherainyperiod,whichhadameanprecipitationof112·4±44·1mm.
Below,therainyanddryperiodsaretogethertermed‘seasons’,althoughtheydidnot
correspondexactlytothenormalannualcycle.
The environmental characterization of sampling sites is shown in Table I and indi-
cates the spatial and seasonal heterogeneity of bottom water variables in Guanabara
Bay.Thespatialpatternsoftemperatureandsalinityweremoreheterogeneousduring
rainy months, periods when s.d. was consistently higher. The same period revealed
∘
greater amplitudes of minimum and maximum temperature (16–29 C) than in dry
∘
months(18–28 C;TableIandAppendixI).Lowesttemperatureswereobserveddur-
∘ ∘
ingrainyperiodsatEntrance(16 C),CentralChannel(17 C)andGovernadorIsland
∘
(17 C). On the other hand, the highest temperature was measured at Gradim during
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846
826 D. R. DA SILVA ET AL.
y,
GuanabaraBa ance Rainy(17) 21·1±2·516·0–26·0±0·634·933·4–36·11·4±0·70·5–4·64·2±5·30·1–29·24·3±0·62·4–5·2 Island Rainy(17) 24·1±1·721·0–28·0±2·430·422·6–33·53·7±1·02·1–6·221·7±12·30·6–45·72·4±1·30·2–6·7
r á
n nt et
entheses)iJune2007 E Dry(7) 21·6±1·818·0–24·035·1±0·534·2–35·81·4±0·50·6–2·53·8±4·40·3–16·94·4±0·63·2–5·4 Paqu Dry(7) 23·9±2·320·0–28·032·8±0·931·1–34·13·3±0·82·0–4·716·9±14·00·4–51·53·2±1·31·3–5·1
parto
5
(numberofmonthsgiveninsolvedoxygen,fromJuly200 DuquedeCaxias Dry(7)Rainy(17) 23·8±2·523·5±1·520·0–28·021·0–27·032·8±0·931·1±1·630·8–33·927·5–33·43·9±1·44·6±1·32·0–7·62·7–9·542·1±50·231·3±16·47·4–198·12·2–82·43·0±2·82·0±1·51·3–12·30·0–6·2 Gradim Dry(7)Rainy(17) 23·6±2·224·2±2·220·0–27·020·0–29·032·1±1·329·3±3·129·7–33·718·8–33·63·2±0·83·8±2·41·5–4·61·1–16·27·8±8·09·1±9·00·2–21·40·2–33·03·1±2·22·7±1·40·2–8·00·5–5·6
ss
inthedryandrainyperiodosphorus,ammoniumanddi CentralChannel Dry(7)Rainy(17) 21·9±2·021·5±2·318·0–25·017·0–25·034·8±0·634·6±0·533·8–35·733·4–35·82·1±0·62·2±1·71·3–3·60·9–11·29·9±6·28·1±7·40·3–20·20·2–41·53·4±0·83·3±0·62·1–4·91·1–4·3 GovernadorIsland Dry(7)Rainy(17) 23·4±1·723·0±2·220·0–27·017·0–28·033·6±0·932·4±1·432·2–35·629·1–34·43·9±0·63·7±1·23·0–4·91·3–6·89±12·729·3±19·924·5·2–51·41·7–102·62·1±1·22·5±1·40·7–3·90·7–7·0
dh
ep
samply,total mum mum mum mum mum mum mum mum mum mum
achareae,salinit s.d.m–maxis.d.m–maxis.d.m–maxis.d.m–maxis.d.m–maxi s.d.m–maxis.d.m–maxis.d.m–maxis.d.m–maxis.d.m–maxi
esofeperatur Mean±MinimuMean±MinimuMean±MinimuMean±MinimuMean±Minimu Mean±MinimuMean±MinimuMean±MinimuMean±MinimuMean±Minimu
blm
ae
rit
ag
vn ) )
Environmentalincludi ∘re(C) 𝜇phorus(M) 𝜇m(M) −1oxygen(mgl ∘re(C) 𝜇phorus(M) 𝜇m(M) −1oxygen(mgl
TableI. Area Season Temperatu Salinity Totalphos Ammoniu Dissolved Area Season Temperatu Salinity Totalphos Ammoniu Dissolved
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846
ICHTHYOFAUNA OF ESTUARINE TROPICAL BAY 827
∘
therainyperiod(29 C),followedbyPaquetáIsland(bothperiods),GovernadorIsland
∘
(rainyperiod)andDuquedeCaxias(dryperiod),allexhibitedthemaximumof28 C
(TableIandAppendixI).
Areasclosetotheseawardend(Entrance)andthoseunderthedirectinfluenceoftidal
currents(CentralChannel)showedthehighestsalinityvalues,attainingamaximumof
36·1 at Entrance and 35·8 at Central Channel, both during rainy periods (Table I and
AppendixII).GradimandPaquetáIslandshowedthelowestsalinityvalues(18·8and
22·6)duringrainymonths.
Thepatternobservedfortotalphosphorouswassimilartosalinityandtemperature,
with values more homogeneous along the bay during dry periods (range=0·6–7·6).
LowestmeanvalueswereobtainedatEntranceandCentralChannelwithnocleardis-
tinctionbetweenseasons(TableIandAppendixIII).
Dissolved oxygen and ammonium revealed an inverse pattern and had more het-
erogeneous values during the dry months. The lowest concentrations of dissolved
oxygen were observed at Duque de Caxias and Gradim during the dry period (0·0
and0·2mgl−1)andatPaquetáIslandduringrainyperiod(0·2mgl−1).Coincidentally,
DuquedeCaxiasandGradimhadhigherconcentrations,attaining12·3and8·0mgl−1
(Table I and Appendix IV). Lastly, the highest concentrations of ammonium were
associated with the western portion of the Bay, including Duque de Caxias during
thedryperiod(198·1𝜇M)andGovernadorIslandduringtherainyperiod(102·6𝜇M;
TableIandAppendixV).
COMMUNITY DESCRIPTORS
A total of 74186 specimens were caught during the 2years of sampling, compris-
ing 130 species and 45 families. The three most numerous species [Chilomycterus
spinosus spinosus (L. 1758), Genidens genidens (Cuvier 1829) and Micropogonias
furnieri(Desmarest1823)]accountedfor57·8%oftheabsoluteabundance.Sciaenidae
wasthemostnumerousfamily,contributing27·5%ofthetotalcatch(AppendixVI).
ANOVA indicated no interaction between environmental drivers (areas v. season)
for any fish metric (Table II). Therefore, the influence of each of these drivers was
examinedindividually.Changesinabundance,diversityandequitabilitywerestatisti-
callyexplainedbythetwodriversindependently,andtheshiftsinrichnessvalueswere
associatedonlywithspatialvariability(P<0·05).
Abundancechangedmarkedlyduringthestudyperiod,asevidencedbythelarges.d.
SamplingwasmosteffectiveintheDuquedeCaxiasarea,withc.250individualsper
haul (0·5h) during dry months. Regardless of the season, the mean catch at Duque
de Caxias was statistically dissimilar from those at the Entrance and Paquetá Island
sites.Generally,largermeancatcheswereobtainedduringdrymonthsforallsampling
locationsexceptDuquedeCaxias.OnlythecatchesfromGradimdivergedstatistically
betweenseasons[TableIIandFig.3(a)].
Higher richness values were obtained at areas close to the seaward end. At the
Entrance, a total of 87 species were collected, while 69 species were recorded from
the Central Channel. The catches at Entrance showed the highest mean richness, in
contrast to Paquetá Island, which showed the lowest values. Richness in both areas
was statistically different from the others [Table II and Fig. 3(b)]. Rainy months
usually showed higher levels, with the exception of Paquetá Island and Central
Channel.
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846
828 D. R. DA SILVA ET AL.
TableII. Results of two-way ANOVA on fish metrics using area and season as orthogonal
factors
Sumof Mean
Sourcesofvariation squares d.f. square F P
CPUE Area 310672 5 62134 4·0388 <0·01
Season 61764 1 61764 4·0147 <0·05
Areav.season 58497 5 11699 0·7605 >0·05
Error 2030757 132 15385 – –
Richness Area 1355·64 5 271·13 14·837 <0·001
Season 0·01 1 0·01 0·001 >0·05
Areav.season 163·75 5 32·75 1·792 >0·05
Error 2412·07 132 18·27 – –
Diversity Area 9·1130 5 1·8226 9·899 <0·001
Season 1·5998 1 1·5998 8·689 <0·01
Areav.season 1·2460 5 0·2492 1·354 >0·05
Error 24·3028 132 0·1841 – –
Equitability Area 0·60160 5 0·12032 6·492 <0·001
Season 0·23562 1 0·23562 12·713 <0·001
Areav.season 0·09526 5 0·01905 1·028 >0·05
Error 2·44643 132 0·01853 – –
Boldvaluesindicatealpha=0.05.
Diversity was higher during rainy months at all locations, with the exception of
Duque de Caxias, where it was almost equal between seasons. Similar to richness,
diversityshowedhighervaluesatEntrance[TableIIandFig.3(c)].Inaddition,equi-
tabilitysuggestedthatdrymonthsshowedhigherdominancesofoneormorespecies
[TableIIandFig.3(d)].ThelowestvalueswereobservedatDuquedeCaxias,Gradim
andGovernadorIslandduringdrymonths.
Geostatistical results visually demonstrated the same patterns as the ichthyofauna
metrics,butgavemoreemphasistothedifferencesbetweenseasons.Thehigherspatial
heterogeneityoftheCPUEatGuanabaraBayduringrainymonths,withanamplitude
of c. 800 individuals 0·5h−1 while during dry periods, the CPUE was less spatially
concentrated(amplitudeofc.200individuals0·5h−1)(Fig.3).Latitudinaldifferences
in capture can also be observed in the model (Fig. 4). Richness (Fig. 5) and diver-
sity (Fig. 6) models agree with the higher spatial heterogeneity associated with rainy
months.Bothgradientsdisplayedhighervaluesinareasclosetotheseawardend,cor-
roboratingtheresultsfromANOVA.
The CA and CCA revealed that the longitudinal spatial gradient within Guanabara
Bay is stronger than the seasonal gradient with respect to the patterns of occupancy
of the demersal ichthyofauna (Figs 7 and 8). The results demonstrated that marine
estuarine-opportunists [e.g. Orthopristis ruber (Cuvier 1830), Diplectrum formosum
(L.1766),Cynoscionjamaicensis(Vaillant&Bocourt1883)andCtenosciaenagracili-
cirrhus(Metzelaar1919)]wereassociatedwithlower-baylocations,wherethehigher
dissolvedoxygencontentandsalinitymayberesponsibleforthesimilarityofthefish
assemblagebetweentheEntranceandCentralChannelduringbothseasons.Incontrast,
marine estuarine-dependent species, such as the catfishes G. genidens and Genidens
barbus(Lacépède1803),wereassociatedwiththeupperbay.TheassemblageatDuque
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846
ICHTHYOFAUNA OF ESTUARINE TROPICAL BAY 829
(a)450 (b)
30
400
–1Abundance (individuals 0.5h)112233050505000000 Richness 112205055
50
0 a; b a b 0 * *
(c) 3·0 (d)0·80
0·75
2·5
H'Diversity (shannon index ) 0112····5050 J'Equitability (pielou index ) 000000······455667505050
0·40
a a * a; b a; c; d c; e; f e b; f d
0 0·35
Central Channel Entrance Gradim Central Channel Entrance Gradim
Duque de Caxias Governador Island Paquetá Island Duque de CaxiasGovernador Island Paquetá Island
Fig. 3. Spatialmean±s.e.variationinbothseasons( ,dry; ,rainy)of(a)abundance,(b)richness,(c)diversity
and(d)equitability(d)ofsoft-bottomdemersalichthyofaunainGuanabaraBay,RiodeJaneiro,sampled
fromJuly2005toJune2007.Lettersfrom‘a’to‘f’indicatethepairsofareaswhicharestatisticallydifferent
basedonTukeypost-test(P<0·01); ,theareadiffersstatisticallyfromallotherareas(P<0·05); ,the
pairsofseasonswhicharestatisticallydifferentbasedonTukeypost-test(P<0·01).
deCaxiaswasassociatedwithhigherlevelsofammoniumandtotalphosphorus,aswell
ashighertemperatures.
DISCUSSION
Estuariesexhibitbothhorizontalandverticalgradientsintheirwatervariables.Since
thisstudyfocusedondemersalsoft-bottomspecies,interestwasinthehorizontalgradi-
entofGuanabaraBay,whichistypicallystructuredbythebalancebetweencontinental
drainage,influencedbyrainyanddryperiods,andcoastalcurrents(Mayretal.,1989;
Valentin,1993,1999;Ribeiro&Kjerfve,2002).Continentaldrainageisanimportant
factor,withmoreinfluenceontheinnerbayareasandduringtherainyseason,apattern
thatinGuanabaraBayisespeciallypronouncedduetoitsextensivedrainagebasin.The
proximityoftheSerradoMarmountainrange(c.20km)contributestoamuchlarger
freshwaterinput,predominantlyfromDecembertoMarch,comparedtootherimpor-
tantBrazilianestuarineecosystemssuchasthePatosLagoon(Garciaetal.,2012).At
theoppositeendofthebay,theinfluenceofcoastalwaterswasanotherdriverforthe
horizontal gradient, as the Central Channel as well as the bay mouth (Entrance) are
stronglyinfluencedbytidalcurrents(Mayretal.,1989).
Corresponding with the continental drainage, the influence of coastal waters on
the spatial organization and composition of the ichthyofauna is seasonally structured
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846
830 D. R. DA SILVA ET AL.
(a) (b)
0 0
0 0
0 0
0 Magé Magé 0
49 Duque de Caxias Duque de Caxias 49
7 7
Paquetá Island Paquetá Island
0 0
0 0
0 0
3 3
8 8
4 4
7 7
0 0
00 Governador Island Governador Island 00
6 6
47 São Gonçalo São Gonçalo 47
7 7
0 0
0 0
0 0
9 9
6 6
4 4
7 Rio de Janeiro Rio de Janeiro 7
Niterói Niterói
0 0
0 0
0 0
2 2
6 6
4 4
7 N N 7
680 000 687 000 694 000 701 000 680 000 687 000 694 000 701 000
SAD 1969 UTM Zone 23S
0 2·5 5 10
km
85 – 152 218 – 285 352 – 418 485 – 552 618 – 685 752 – 818
152 – 218 285 – 352 418 – 485 552 – 618 685 – 752 818 – 885
Fig.4. Spatialpatternofcatchperunitofeffort(CPUE;numberofindividuals0·5h−1)ofthesoft-bottomdem-
ersalichthyofaunasampledfromJuly2005toJune2007inGuanabaraBay,RiodeJaneiro,inthe(a)rainy
and(b)drymonths.
in Guanabara Bay. One of the principal oceanographic features of the south-eastern
Brazilian coast is the prevalence of tropical waters carried by the Brazil Current
during most of the year (Brandini, 1990). During late spring and summer, how-
ever, the South Atlantic Central Water (SACW) surfaces 100km north of the bay
entrance,establishingsubtropicalandtemperatecharacteristicsfortheRiodeJaneiro
∘
coast, with temperatures between 10 and 20 C (Matsuura, 1986; Barletta etal.,
2010). This oceanographic phenomenon distinguishes Guanabara Bay from all other
south-western Atlantic estuaries, as the only one under the influence of an annual
low-intensity upwelling event. Due to the correspondence between rainy periods and
theproximity oftheSACW totheshore, theeffectsof bothenvironmental processes
were clearly observed in the geostatistical models. The results for rainy months
showed higher heterogeneity than those for dry months, due to the concomitantly
higher freshwater input of Duque de Caxias, Paquetá Island, Governador Island and
Gradim and the effects of cold and saline intrusion of SACW along the bottom,
creatingadensity-dependentverticalgradient,andimposingmesohalinetopolyhaline
characteristicstoupper-bayareasduringtherainymonths(Valentin,1993).
Considering all the limitations of an estuarine environmental quality assessment,
combinedwiththeintrinsicallyhighvariabilityandtheadaptationoftheichthyofauna
to these conditions, known as the ‘estuarine quality paradox’ (Elliott & Quintino,
2007), the results presented here support some inferences about the influence of
©2016TheFisheriesSocietyoftheBritishIsles,JournalofFishBiology2016,89,821–846