Estuaries Vol. 27. No.6. p. ~14 Deoe~r 2004

Comparison of 1982-1983 and 1997. 1998 E Nino Effects on the

A. M. GARCIAl.., P. VIEIRAI, K. O. WINEMILLER2, and AM. GRIMM3

1 FundarM Universidade Federal de Rio Grande (FURG), Departamento de Oceanografia,

LaboratiJrio de Ictiologia, C. P. 474-Rio Grande, RS, Brasil2 Department of Wildlife and Fisheries Sciences, Texas A&M University, C..allege Station, Texas

77843-22583 Department of Physics, Federlll University of Parana, PR, Brazil

ABSTRACT: Meteorological impacts of E1 Nino events of 1982-1983 and 1997-1998 were observed in locationsdtroughout the world. In southern Brazil, E1 Nino events are associated with increased rainfall and higher freshwaterdischarge into Patos Lagoon, a large coastal lagoon that empties into the Atlantic Ocean. Based on interdecadal mete-orological and biological data sets encompassing the two strongest E1 Nino events of the la.~t 50 yr, we evaluated thehypothesis that E1 Nino-induced hydrological changes are a major driving force controlling the interannual variation inthe structure and dynamics of fishes in the Patos Lagoon estuary. High rainfall in the drainage basin of the lagooncoincided with low salinity in the estuarine area during both E1 Nino episodes. Total rainfall in the drainage basin washigher (767 versus 711 mm) and near-zero salinity conditions in the estuarine area lasted about 3 mo longer during the1997-1998 E1 Nino event compared with the 1982-1983 event. Hydrological changes triggered by both E1 Nino eventshad similar relationships to fish species composition and diversity patterns, but the 1997-1998 event appeared to havestronger effects on the species a.~emblage. Although shifts in species composition were qualitatively similar during thetwo E1 Nino events. distance between E1 Nino and non-EI Nino assemblage multivariate centroids was greater during the1996-2000 sampling period compared with the 1979-1983 period. We provide a conceptual model of the principalmechanisms and processes connecting the atmospheric-oceanographic interactions triggered by the E1 Nino phenomenaand their effect on the estuarine fish assemblage.

stood, Timmermann et al. (1999) showed that, un-der a scenario of increasing greenhouse-gas con-centrations, EI Nino-like conditions would becomemore frequent. The frequency and intensity of EINino events and their effects may also be influ-enced by the phases of interdecadal modes of seasurface temperature variation (Mestas-Nunez andEnfield 1999, 2001). If El Nino events increase inseverity and duration in response to global change,it will become critically important to understandhow meteorological and hydrological patterns as-sociated with EI Nino events affect ecosystems.

Patos Lagoon (3~, 490W) represents an appro-priate ecosystem to evaluate how disturbances in-duced by EI Nino can affect the dynamics andstructure of fish estuarine assemblages. EI Nino ep-isodes have affected the western coasts of theAmericas frequently over the last 5,000 yr (Rollinset al. 1986), which coincides with the geomorpho-logic age (5,000-6,000 yr) estimated for the PatosLagoon system on the Atlantic coast of southernBrazil (Knoppers and Kjerfve 1999). High rainfallin southern Brazil during EI Nino events (Grimmet al. 1998, 2000) increases freshwater discharged

IntroductionThe EI Nino phenomenon refers to a warming

of the tropical Pacific basin in association with aweakening of the trade winds that occur at inter-vals of 3-7 yr. El Nino events vary in intensity. The1982-1983 and 1997-1998 EI Nino episodes werecomparable in magnitude and represented thestrongest warming observed since 1950 (Glantz2001). Meteorological changes induced by EI Ninoevents are felt around the world, with importantimplications for the dynamics of aquatic ecosys-tems (Caviedes 2001; Enfield 2001) ranging fromcoral reefs (Glynn et aI. 2001) to upwelling regions(Brodeur et aI. 1985;Jimenez et aI. 2001; Roy andReason 2001).

Some authors suggest that recent EI Nino eventswere stronger and more frequent than those in thepast (Tudhope et aI. 2001). Although predictionscannot be conclusive because they may depend onatmospheric processes that are not well under-

. Corresponding author: tele: +5553/233-6752; fax: +5555/23~1; e-mail: amgarcia@mikrus.com.br

C> 2004 Estuarine ReseaIdI Federation 905

906 A. M. Garda et 81.

versity reveal similar trends during both EI Ninoevents? Did rainfall and salinity conditions prior tothe onset of the EI Nino events influence the mag-nitude of responses? Based on current findingsand those from previous studies, we developed aconceptual diagram showing the main mechanismsand processes linking atmospheric-oceanographicinteractions triggered by EI Nino phenomena tothe fish assemblage structure in Patos Lagoon es-

tuary.

Materials and Medtods

STUDY SITEThe southern 10% of Patos Lagoon (250 kIn

long and 60 km wide) has the geomorphologic fea-tures of a bar-built estuary. and its upper limnicarea (30 kIn wide) gradually narrows into a chan-nel (700 m wide) connected with the south Atlan-tic Ocean. Apart from a navigation channel, about80% of the estuarine zone is less than 2 m deep(Fig. 1). The estuarine ecosystem is a nurseryground for several abundant fish and shrimp spe-cies (Vieira and Castello 1996; Reis and D'incao2000).

Tidal influence in the estuary is minimal (meantidal amplitude is 0.47 m). Wind and seasonal puls-es of freshwater inflow influence patterns of watercirculation and salinity (longitudinally and verti-cally). The lagoon has a drainage basin formed byrivers characterized by a mid latitude flow regime:high discharge in late winter and early spring fol-lowed by low to moderate discharge through sum-mer and autumn (Moller et al. 2001). During ElNino events, rainfall in southern Brazil (Grimm etal. 2000) is above average, and the mesohalinezone can be displaced to the inner continentalshelf (Moller et al. 200 1).

FIELD SAMPUNG

Fishes were sampled using a 9 X 1.5 m beachseine (13 mm bar mesh in the wings and 5 mm inthe center 3-m section) that was pulled to cover anarea approximately 60 m2. Survey stations were lo-cated in shallow waters of the Patos Lagoon estuary(Fig. 1). The number of survey stations varied be-tween the two sampling periods, with four to sixsurvey stations during 1979-1983 and four during1996-2000. Each sample was composed of threebeach seine hauls. Seven samples (21 hauls) weremade during each season within two periods: win-ter 1979 to spring 1983 (the one exception wassummer 1983 with 15 hauls) and winter 1996 tospring 2000. Samples were grouped by seasons asfollows: summer (january-March), autumn(April-June), winter (july-September) , and spring(October-December). Salinity was measuredmonthly at each station, and precipitation was reo.

into Patos Lagoon several-fold (Garcia 1996). Thislagoon is one of the world's largest coastal aquaticecosystems (10,360 km2 with a drainage basin of201,626 km2), and its estuarine zone serves as anursery ground for coastal fishes (Vieira and Cas-tello 1996), including species that support impor-tant fisheries in the southwestern Atlantic Ocean(Haimovici et al. 1996; Reis and D'incao 2000).

Previous studies showed that EI Nino can affectthe primary productivity in the southern Braziliancoastal area and the fish assemblage of Patos La-goon estuary. The moderate 1987-1988 EI Ninoincreased freshwater discharge into the estuaryand coastal marine area, and affected phytoplank-ton production and biogeochemical cycles in thecoastal area (Ciotti et al. 1995; Lima et al. 1996).Garcia et al. (2001) demonstrated that the fish as-semblage had opposite trends in fish abundanceand diversity between cold (1995-1996 La Nina)and warm (1997-1998 EI Nino) ENSO episodes.Based on a larger data set, Garcia et al. (2003a)showed that the 1997-1998 EI Nino-inducedchanges were not highly persistent, with the fishassemblage returning to its pre-EI Nino state within18 mo following the EI Nino. Differences in sam-pling protocols, methods of data analysis, and lackof replication (i.e., more than one EI Nino eventanalyzed simultaneously) hinder efforts to con-struct predictive models of EI Nino effects on thefish assemblage of Patos Lagoon estuary.

Garcia et al. (2001, 2003a) proposed that thehigh rainfall associated with EI Nino events signif-icantly increases runoff and freshwater dischargein the drainage basin of Patos Lagoon, which, intum, changes salinity patterns within the estuary.This hypothesis was based on rainfall data obtainedfrom a single meteorological station located in theestuarine area (Rio Grande City). Due to the spa-tial variability of EI Nino effects in southem SouthAmerica (Grimm et al. 2000), there is uncertaintyas to whether the rainfall pattern observed at agiven station would be an accurate predictor of EINino-induced changes in rainfall over the entirePatos Lagoon drainage basin.

Based on an interdecadal biological data set en-compassing the two strongest EI Nino events of thelast 50 yr, and an regional rainfall data set that in-cludes 81 sample stations scattered around thedrainage basin, we evaluated the hypothesis that EINino-induced hydrological change is a major driv-ing force controlling interannual variation in thedistribution and abundance of fish species in PatosLagoon estuary. We addressed the following que~tions in the present study. Did EI Nino-inducedchanges in rainfall and salinity occur with the samemagnitude during both El Nmo events? Did spe-cies composition, abundance pattems, and fish di-

)~ ...

r',

( EI Nino Effects on Palos Lagoon Fish 907

"

'"-'

2705

I I

I!

Atlantic35 Ocean

~OW", '-

'.

~ Fig. 1. Drainage basin of the Patos Lagoon (bold line) with the spatial distribution of the 81 meteorological stations (filled squares),

and the estuarine area showing beach survey stations (dots).

, !corded daily at 81 meteorological stations located tained with different amounts of effort. Evennessalong the lagoon drainage basin. was analyzed by the Evar index proposed by Smith

" and Wilson (1996), which has equal sensitivity toDATA ANALYSIS rare and abundant species. This index converges

Environmental Parameters to one when species abundances are equal. SpeciesMeteorological effects of the two EI Nino peri- ?iversity w.as .esti~at~d u~ing .the Shannon-Wiener

ods on the Patos Lagoon estuary were determined mdex. VarIatIon m dIversIty, rlchnes.s, and eve?nessby comparing individual seasonal rainfall and salin- were analyzed by one-way analysIs of varIance.ity values (winter 1979 to spring 1983 and winter1996 to spring 2000) with a long-term database ofseasonal averages. Seasonal values (x) from theshort-term data were contrasted with seasonal av- ~ ~erages (IJ.) using x - IJ.. Rainfall data were com- i 100 0 ~pared with a database of22 yr (1979-2000) of pre- :cipitation in the Patos Lagoon drainage basin. Amean rainfall series for the basin was calculated for E 1

Ethis period from the data of 81 stations (Fig. 1). iSalinity data were compared with a 10-yr database I(1978-1983 and 1996-2000) of monthly values ob- ~tained from 10 sample stations located at the Patos !-50

Lagoon estuary. Based on the rainfall and salinity 1

distributions and anomalies in Patos Lagoon, we ~used the following seasons to set the temporallim- Iits of EI Nino events: spring 1982 to winter 1983 t(1982-1983 EI Nino) and spring 1997 to winter ;Z-11998 (1997-1998 EI Nino).

1979 I 1- I 1~ I 1- I 1~ 19$ I 1997 I 1- I 1999 I 2000

Diversity Indices . I f) .. h 1., dFIg. 2. Seasona uctuatton m t e two samp mg peno s

Species richness was calculated by the rarefac- (1979-1983 and 1996-2000) of average rainfall in the drainagetion method (Sanders 1968; Hurlbert 1971). This basin of Patos Lagoon and average salinity in its estuarine area,approach provides a standardized measure of spe- rainfall anomalies, and salinity anomalies. Anomalies represent

. . . . . difference between each seasonal value from 1979-1983 andCles d!V~rsIty adJust~d for the effect of sample sI~e, 1996-2000 and each seasonal long-term average (rainfall: 22 yrpermIttIng companson between assemblages WIth from 1979 to 2000 and salinity: 10 yr from 1978 to 1983 anddifferent densities of organisms or samples ob- 1996 to 2000). The shaded area represents El Nino periods.

"""'~ I,~",

908 A. M. Garcia et al.

TABLE 1. Relative importance (based on percent nume-rical abundance and frequency of occurrence) of the most representativefishes captured during the tWo sampling periods (1979-1983 and 1996-2000). ~nter. s-spring. s-summer. a-autumn. Seelegend below and details in the material and methods.

79 1980 1981 1982 1983 96 1997 1998 1999 2000_w:_-~ ~ a w s saw s saw s saw s w s saw s saw s saw s saw sSpecies

-I. !j;~~~;. .

..

Mugil platanusAtherinella brasiliensis

Odontesthes argentinensis

Micropogonias fumieri

Jenynsia multidentata

Mugil curema

Brevoortia pectinata

L ycengraulis grossidens

Platanichthys platana

Mugil gaimardianusRamnogaster arcusta

Parapimelodus nigribarbisGobione/lus shufeldti

Ulaema lefroyi

Astyanas eigenmanniorum

OIigosarcus jenynsiiTrachinotus marginatus

Anchoa marinii

Genidens genidens

Harengula c/upeola

Syngnathus fofletti

I fj;;,'. ... .. -Legend: - frequent

These data met the assumptions of normality (Kol-mogorov-Smirnov test) and homogeneity of vari-ances (Cochran test). We used the following peri-ods to achieve a balanced design without con-founding seasonal samples: spring 1979 to winter1980, spring 1980 to winter 1981, spring 1981 towinter 1982, spring 1982 to winter 1983, spring1996 to winter 1997, spring 1997 to winter 1998,spring 1998 to winter 1999, and spring 1999 to win-ter 2000. El Nino years were represented by spring1982 to winter 1983 and spring 1997 to winter1998.

divided by the total abundance (N) of all speciescaptured (X 100). Fishes showing FO% > 50 byseason were considered frequent species, whereasfishes showing PN% > the ratio (100/number ofspecies) were considered abundant. These criteriaselected 21 fish species (out of 63) as the mostrepresentative for use as predictor variables inDFA

We performed stepwise DFA to select variables(F values of 1 for entry and 0 for removal) thatyielded the most significant linear combination fordiscrimination between groups. Four groups weredetermined a priori as follows: EI Nino and non-EI Nino during the 1979-1983 period, and EI Ninoand non-EI Nino during the 1996-2000 period. Atolerance value of 0.01 was used as the criterionfor assuming that variables were not redundant (atolerance value of 0.01 means that the variable is99% redundant with other variables already includ-ed in the model). Data (log relative abundance +1) were checked for normality (normal probabilityplots) and homogeneity of variances (Cochran testand standard deviation&-means plots) prior to use

Discriminant Function Analysis (Df:4)Species classified as infrequent and less abun-

dant were omitted to avoid a disproportionate ef-fect of rare species on the DFA. We used the fol-lowing procedure to sort out rare species. The fre-quency of occurrence (FO%) for each species wascalculated as the ratio of the number of occur-rences of a species divided by the total (X 100).The percent numerical abundance (PN%) was cal-culated as the total abundance (n) of a species,

EI Nino Effects on Patos Lagoon Fish 909

TABLE 2. Indices of diversity (Shannon-Wiener,.H'), equita- 8 '"bility (Evar), and richness (Rarefaction, E[Sn]; adjusted sample 117S-1- .:-EN

equals 155 individuals) calculated for each season during thetwo sampling periods (1979-1983 and 1996-2000). The bold 4

represents El Nino periods.

Year Season H' £var £(So) 2 ..1979 winter 0.30 0.10 4.42 . .. .. 6

. .. 8spnng 0.73 0.49 7.92 0 . ~~ ~~~

1980 summer 0.46 0.09 5.63 :.:. ~~#"";~6. -*~ 6autumn 0.43 0.13 7.41 . . ~.: -11.: ~winter 0.36 0.10 4.93 -2 - . ~ 6spring 0.69 0.13 8.25 ~ .. 6 A

1981 summer 0.61 0.08 6.02 Aautumn 0.81 0.18 11.61 N -4

winter 0.32 0.09 4.80 ~ -4 -2 0 2 4 8

spring 0.64 0.11 7.48 8 1_2000 0 EN

1982 summer 0.93 0.14 13.16 ._-EN.autumn 0.76 0.11 8.82winter 0.57 0.08 5.79 4 . -spring 0.67 0.20 11.54 .. CJ

1983 summer 0.76 0.13 10.33 ".' ." .. .- CJ

2 CJautumn 0.47 0.15 7.45 - . -. '.' CJ CJ-'. 0 CJwinter 0.93 0.16 11.00 - - "."30 .-.spring 0.76 0.11 9.21 0 ~: :...gd'."D4.cPCJ CJ

1996 winter 0.66 0.13 6.99 - .'. . -~~~. D.spring 0.58 0.14 8.12 .". .1::1='.0

1997 summer 0.44 0.11 7.80 -2 0 CJ

autumn 0.58 0.11 8.19winter 0.72 0.10 7.20spring 0.76 0.21 12.60 -4

1998 summer 0.87 0.25 13.29 -4 -2 0 2 4 6Root 1autumn 0.63 0.18 9.05

winter 0.79 0.31 10.39 Fig. 3. Scatter plot of the individual scores for the two firstspring 0.76 0.13 11.04 discriminant functions (Root 1 and 2) for the two sampling pe-

1999 summer 0.74 0.10 9.62 riods 1979-1983 and 1996-2000. Centroid groups are repre-.. autumn 0.71 0.10 8.66 sented as (1) Non-El Nino, (2) El Nino during the 1979-1983

winter 0.75 0.12 7.19 period, (3) Non-El Nino, and (4) El Nino in 1996-2000.spring 0.75 0.11 8.85

2000 summer 0.65 0.10 7.61a~tumn 0.71 0.10 8.98 linity conditions in the estuarine area lasted aboutWln.ter 0.30 0.16 6.35 3 mo longer during the 1997-1998 El Nino com-spnng 0.70 0.25 9.04 pared with the 1982-1983 El Nino (Fig. 2). Rainfall

was above its historic average across all seasons in

.. . . both EI Nino periods, being particularly strongm the analysI~. Only a few spe~Ies dId no~ meet during spring and summer of the 1997-1998 Elthese .assumptIons, bu.t w~ retaIned them m ~e Nino. High rainfall anomalies during both El Ninoan~lysis beca~se DFA IS fairly r~bu~t to these Vlo- events were preceded by extended periods of be-latI?ns,.especiallywhen sample SIze IS large and the low-average rainfall (Fig. 2). In contrast with rain-desIgn IS balanced (Underwood 1997). fall trends, salinity was below its historic average

R ults across all seasons during both EI Nino events, es-es pecially during summer and autumn of 1982-1983

ENVIRONMENTAL PARAMETERS and autumn of 1997-1998 (Fig. 2).Comparison of seasonal rainfall and salinity with

long-term seasonal averages revealed similar trends SPECIES COMPOSITION AND DIVERSITYwithin both sampling periods (1979-1983 and A total of 87,901 fishes, representing 63 species,1996-2000). High rainfall in the drainage basin of was captured in 750 beach seine hauls made overPatos Lagoon coincided with low salinity in the es- the study period. Most species, especially marinetuarine area, which can be attributed to the strong and freshwater vagrants, had low abundance andEI Nino events of 1982-1983 and 1997-1998. The frequency in samples. Based on percent numericalmagnitudes of meteorological (rainfall) and hydro- abundance and frequency of occurrence, 21 spe-logical (salinity) effects differed between the two cies were identified as the most important assem-EI Nino events. Total rainfall in the drainage basin blage elements (Table 1).was higher (767 versus 711 mm) and near-zero sa- Dominance by a few species was reflected in low

.

~".= ,,;L4~'"

910 A. M. Garda et al.

TABLE 3. Summary of the discriminant function analysis (DFA) and canonical coefficient of the predictor variables selected by thestepwise forward method. * p < 0.01. Data were log,o transformed.

tAxes

O.100.'

0.:42.16

0.82160.0o.~

257.054.

0.35185.6

0.618114.434

*

-o.~0.154

-0.1170.0250.216

-0.3440.2000.320

-0.495-0.148-0.148

0.324-0.033

0.2600.2730.4030.1530.167

-0.088

-0.105

0.0820.4gg

-0.4110.4-'40.289

-0.1600.15g0.075O.20g0.272

-O.~-0.090

0.2200.0150.2460.267

-0.525-0.502

-0.161

-'0.148

-0.094

-0.069

-0.016

-0.008

0.3880.3120.2800.2630.2530.1960.0570.0-'90.0-'60.004

Summary statistics for ordination axes

EigenvaluesCumulative percentage varianceWilks' Lambda

Chi~uaredf

Significance

Standardized canonical coefficient

Jmynsia multidenlalaOdonIesthes ~nensis

Mugil platanusMugilcu~Mugil gaimanlianusBmIOOrlia pectinataUlaema lefroyiRamnogaster arcuala

Astyanax eiglmmanniorumOligosarcus jmynsiiParapimelodus nigribarbisAtherinella brasiliensisL ,cengraulis grossidens

GenidensgmidensPtatanidlthys platanaMiQoopog1mias furnieriHafmgula dupeoiaGobionellus shufeJdti

values of assemblage evenness (Evar index usuallyless than 0.15) among survey periods. Evennesstended to increase during EI Nino events, with sta-tistically significant higher values observed duringthe 1997-1998 event (n = 14, F = 10.598, P <0.01). There was also an increase in the numberof species (obtained by the rarefaction method)captured during both EI Nino events, with the1997-1998 episode yielding significantly highervalues (n = 14, F = 4.302, P < 0.05; Table 2).

FISH COMPOSmON DURING EL NINo VERSUS NoN-EL NINO PERIODS

Stepwise DFA derived linear combinations of 18variables (species) to discriminate among the fourperiods (EI Nino and non-EI Nino during 1979-1983, and EI Nino and non-El Nino during 1996-2000). Three species (Trachinotus mafR'inatus, An-choa marinii, and Syngnathus Jolleth) were redun-dant (tolerance> 0.01) and eliminated from thedata set of 21 dominant species. The two first ca-nonical functions explained 85.6% of the variance,but the first root alone account for 60% and hadhigher discrimination power (Wilks' lambda =0.34; Table 3). The distance between EI Nino andnon-El Nino group centroids along the first axeswas greater during 1996-2000 (2.13 to -0.20) than1979-1983 (1.00 to -0.675). The second rootmodeled a weak trend of interdecadal differences

between 1979-1983 (centroids: -0.43 and -1.00)

and 1996-2000 (0.17 and 0.65; Fig. 3).The three species most associated with non-EI

Nino conditions (positive canonical coefficientsgiven in Table 3) were jenynsia multidentata, Odon-testhes a~tinensis (both estuarine residents), andMugil platanus (estuarine dependent; Fig. 4). Thethree species most associated with EI Nino condi-tions (negative canonical coefficients) were thefreshwater vagrants Astyanax eigenmanniorum, Oli-gosarcus jenynsii, and Parapimelodus nigribarbis thatoccurred in the estuarine area almost exclusivelyduring EI Nino events (Fig. 5).

DiscussionCOMPARING THE STRENGTH OF EL NiNo EVENTS

Meteorological and hydrological pattems ass0-ciated with the 1982-1983 and 1997-1998 EI Ninoevents had similar relationships to fish species com-position and diversity pattems, but the 1997-1998event appeared to have stronger effects on the fishassemblage. Evenness values tended to increaseduring both episodes; this was caused by decreasesin number of dominant species and increases invagrant fishes. Species richness also increased dur-ing both EI Nino events when several freshwaterspecies expanded their ranges into the estuary, butthis difference was only statistically significant dur-ing the 1990s. The present interdecadal study, with

19708-'68

911EI NRio Effects 00 Palos Lagooo FIsh

~

--I

;1 ~I..~108 .!c -,.--

0..

1--.- . j, A\1 ". I

-. \ i1..-' ~ ..I j .-.' I 1 - 1 -. '82 ,- ,- ,., ,- ,.. .-

Fig. 5. Seasonal fluctuation in relative abundance of Astya-nax eigmmanniorum, Oligosarcus jenynsii, and Parapimelodus nigri-barlJis in the tWo sampling periods (1979-1983 and 1996-2000).These species had higher positive standardized coefficients inthe first discriminant function (Root I, see Table 3), showinggreater association with EI Nmo periods. The shaded area rep-resents EI Nino periods.

conditions associated with the 1982-1983 event.Such differences in the magnitude of effects ass0-ciated with the 1982-1983 and 1997-1998 EI Ninoevents have also been reported from studies of Pa-cific coastal systems of South America. Sanchez etal. (2000) demonstrated that both events had com-parable effects on the coastal marine ecosystem offPeru, although the 1997-1998 produced more ex-treme conditions. Arcos et al. (2001) showed thatthe 1982-1983 and 1997-1998 EI Ninos led tochanges in diet and habitat use by jack mackerel(Trachurus symmetricus mu1fJhyi) off the coast ofChile. These pattems were only evident duringmoderate to strong EI Nino events and littlechange occurred during weak events.

A SIMPUFlED CoNCEPTUAL MODEL OF EL NINOEFFEcrs ON THE FIsH AssEMBLAGE

A conceptual model summarizes mechanismsand processes associated with EI Nino phenomenaand their effects on the ichthyofauna of Patos La-goon estuary (Fig. 6), and synthesizes informationscattered within regional literature (Ciotti et al.1995; Lima et aI. 1996; Grimm et al. 1998; Garciaet al. 2003a; Costa et al. 2003).

The warming of the sea surface temperatures inthe eastern equatorial Pacific Ocean (shaded areain Fig. 6 no. 1) during EI Nino episodes enhancesthe convection and rainfall in this area, producinganomalous heating in the troposphere. This gen-erates perturbations in the atmospheric divergentHadley and Walker circulations, as well as anoma-lous Rossby waves that propagate poleward and

EI Nino replication and regional rainfall data set,seemed to corroborate the hypothesis that positiverainfall anomalies triggered by EI Nino events playa major role on the interannual variability of thefish assemblage of Patos Lagoon estuary.

Differences in assemblage structure associatedwith EI Nino events were even more apparent inresults from DFA. The distance between EI Ninoand non-EI Nino DFA centroids was greater duringthe 1996-2000 sampling period compared with the1979-1983 period. Although shifts in species com-position had similar patterns during both EI Ninoevents, the temporal changes in species relativeabundances were greater during the 1997-1998 ep-isode. Some freshwater fishes (e.g., the freshwatercatfish P. nigribarbis and the characins A. eigl':nman-nionlm and o. jenynsiz) were more common duringEI Nino periods. Freshwater vagrants were onlycaught in the estuarine area during higher fresh-water outflow trigged by the elevated rainfall of EINino episodes. These species achieved greater rel-ative abundance during the 1997-1998 El Ninothan the 1982-1983 El Nino.

Differences in the magnitudes of 1982-1983 and1997-1998 El Nmo effects on the fish assemblageof Patos Lagoon estuary probably result from dif-ferences in the intensity of associated salinityanomalies. During both EI Nino periods, high rain-fall within the drainage basin resulted in unusuallylow salinity in the estuarine zone, but the 1997-1998 EI Nino had a greater effect. The 1997-1998event was associated with near-zero salinity for aperiod that lasted 3 mo longer than the low-salinity

~

912 A. M. Garcia et al.

~~::~~j~,.,,--- .-

I~Atlantic

@ Ocean-~

Fig. 6. A simplified conceptual diagram showing the linkages between El Nino events in the Equatorial Pacific Ocean and theestuarine fish assemblage of Patos Lagoon in southern Brazil (see detailed explanation in the Discussion).

eastward. These atmospheric perturbations affect conditions can last for several months (Costa et al.rainfall in southern Brazil especially in austral 2003; Garcia et al. 2003b). Freshwater from thespring and the next winter. They produce a cyclon- middle to upper lagoon expands towards the es-ic circulation anomaly over southern South Amer- tuarine zone carrying with them several freshwaterica, with an anticyclonic one northeast of this re- fishes (e.g., P. nigribarbis, A. eigenmanniorum, and O.gion. These anomalies strengthen the subtropical jenynsiz) that spread throughout the estuary, andjet (a belt of strong upper-level westerly winds) and in some cases, are even caught in the adjacent ma-produce a cyclonic vorticity advection over south- rine coastal area. This increase in the number ofern Brazil. These aspects favor the intensification freshwater fishes is the main factor leading to highof mesoscale systems and cyclogenesis over this re- fish diversity usually associated with EI Nino eventsgion (Grimm el al. 1998,2000). (Garcia et al. 2003a). High freshwater discharge

The above average rainfall triggered by EI Nino also decreases the relative abundance of those fish-events over the large drainage basin (201,626 km2) es occurring year-round and breeding in the es-of Patos Lagoon greatly increases freshwater out- tuary. Two phenomena seem to explain theseflow into the lagoon (10,360 km2; no. 2 in Fig. 6). trends. Vegetation-affiliated fishes (e.g.,]. multiden-Freshwater outflow in the northern region of Pat os tata) have greater access to flooded vegetated hab-Lagoon estuary normally ranges from 700 to 3,000 itats in low and mid marshes during periods ofm3 S-I. But during EI Nino events, discharges> high freshwater discharge, and may be less abun-3,000 m3 S-1 frequently occur and the estuarine dant at shoreline sample stations used for seineplume can extend several kilometers into the ad- surveys (dilution hypothesis; Garcia et al. 2004).jacent coastal marine area (Garcia 1996; Moller For other species (e.g., Atherinella brasiliensis), pe-personal communication). lagic juveniles are transported in large numbers

This elevated freshwater outflow affects hydrol- out of the estuary into adjacent marine coastal wa-ogy, water quality, and the fish assemblage in the ters (flushing hypothesis; Garcia et al. 2001). Inestuarine area (971 km2; no. 3 in Fig. 6). Water contrast to estuarine resident fishes, marine spe-levels along the estuarine margin increase, water cies that predictably use estuarine areas asjuvenilestransparency tends to fall, and near-zero salinity (e.g., M. platanus) or occasional marine visitors

: i

913EI Nino Effects on Pam L8gOUI ~

(e.g., A. marinii, Ulaema leJroyz) enter the estuary inlower numbers during periods of high freshwaterdischarge. Apparently the high freshwater outflowthrough the narrow mouth of the estuary (only700 m wide) impairs physical mechanisms that al-low passive movement of these fishes into the es-tuary (i.e., net upstream movement of high-salinitybottom waters).

Recruitment of marine organisms into nurseryareas of Patos Lagoon estuary may be severely cur-tailed during high freshwater outflow indirectlytriggered by El Nino events. Mullet (M. platanus)and pink shrimp (Farfantepenaeus paulensis) , whichtogether sustain the increasingly impoverished ar-tisanal estuarine fishery in this region (Reis andD'incao 2000), are among those estuarine-depen-dent species that could be negatively affected bysustained, high freshwater discharge (see discus-sion in Garcia et al. 2003a). The degree of associ-ation between fishery catches of adult stocks andjuvenile recruitment into the estuary is currentlyunknown, particularly for the mullet. According toTyler (1992), management of commercially ex-ploited fish stocks is severely hampered withoutsome understanding of the processes that drive re-cruitment variability on a long-term basis.

As emphasized by Jaksic (2001), EI Nino phe-nomena provide natural experiments that revealconnections between atmospheric-<>ceanographicprocesses and marine biota that may occur on verybroad geographic scales. The causal linkages be-tween EI Nino phenomena in the South Pacificand the ichthyofauna of Patos Lagoon estuary arean example of complex, large-scale biophysical in-teractions. Additional ecosystem components (e.g.,nutrient dynamics, productivity) need to be addedto the model.

ACKNOWLEDGMENTS

We thank researchers and staff from the FURG IchthyologyLaboratory that collected historical data (1979-1983), LisianeA. Ramos for collecting data between August 1996 and August1997, and numerous colleagues who assisted in the field. Thisstudy received financial support from the Coordenadoria deAperfei~oamento de Pessoal de Nivel Superior-CAPES (Bra-zil), the Conselho Nacional de Desenvolvimento Cientifico eTecnolOgico-CNPq (Brazil), Brazilian Long Term EcologicalResearch (LTER), and the Inter American Institute for GlobalChange Research (1Al) through a fellowship granted by theSACC/Consortium (CRN-O19). Alice Grimm acknowledges thesupport of Inter-American Institute for Global Change Research(IAl-CRNO55) and of the Conselho Nacional de Desenvolvimen-to Cientifico e TecnolOgico (CNPq, Brazil).

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