DISTRIBUTION OF PARACALANIDAE SPECIES ( COPEPODA , CRUSTACEA ) IN THE CONTINENTAL SHELF OFF SERGIPE AND ALAGOAS STATES , NORTHEAST BRAZIL *

The spatial and seasonal distribution of the Paracalanidae species were studied in eighteen stations in the continental shelf off Sergipe and Alagoas States, northeast Brazil, in December, 2001 and 2003, and in June, 2002 and 2003. The Paracalanidae family was constituted by coastal and shelf species such as Parvocalanus crassirostris, Paracalanus quasimodo, P. indicus and P. aculeatus and oceanic species, Calocalanus pavo and Acrocalanus longicornis. Density values were higher in stations located at 10 m isobath with respect to those located at 20 and 30 m depths. Paracalanidae abundance presented differences between seasons with values higher in June (2002, 2003) than in December (2001, 2002). All species were more abundant in the rainy season except Parvocalanus crassirostris. Paracalanus quasimodo was the dominant species with average densities of 949, 740 and 41 ind.m in December months and 4231, 2389 and 1185 ind.m in June months, at stations with local depths of 10, 20 and 30 m, respectively. Canonical correspondence analysis showed that salinity and temperature were the environmental variables that presented significant correlation with the distribution of Paracalanidae species, probably because these variables are influenced by the estuarine waters and by the dynamic of oceanic water masses in the continental shelf.


INTRODUCTION
The continental shelf off Sergipe and Alagoas is narrow varying from 18 km at the extreme south of this area to 42 km in front of the city of Maceió.It has an average width of 30 km.Most part __________ (*) Paper presented at the 2 nd Brazilian Congress of Oceanography, on [9][10][11][12]Vitória,Brazil. of this shelf has depths of less than 50 m and presents an abrupt slope interrupted by two large submarine canyons of the São Francisco and Japaratuba Rivers that reach up to 10 km from the shore line.These canyon heads are steep-walled, V-shaped in crosssection, and narrow with wall heights locally reaching about 800 m (França et al., 1976;Summerhayes et al., 1976).This shelf has a predominance of carbonatic biogenic sediments and the only exception is the area under the influence of the São Francisco River (Coutinho, 1981).
The shelf and oceanic areas of the northeast Brazil are affected by the Tropical (TW) and South Atlantic Central Waters (SACW).The SACW (temperature < 20 ºC and salinity < 36.4 psu) cover the upper ocean of the subtropical South Atlantic and spreads northward underneath the Tropical Water (temperature > 20ºC and salinity > 36,4 psu) (Stramma et al., 1990;Castro & Miranda, 1998).
Copepods are numerous and abundant and they may sometimes form up to 90-97% of the biomass of marine zooplankton.Therefore, copepods are an important link in marine food webs and marine economy (Bradford-Grieve et al., 1999).The Paracalanidae family is compounded by the genera Acrocalanus, Bestiolina, Calocalanus, Delius, Paracalanus and Parvocalanus and from these only Bestiolina has not been registered in the South Atlantic (op.cit.).Paracalanus is one of the most important genus in the neritic region of the Brazilian coast and according to Lopes et al. (1999) its distribution pattern mirrored that of total copepods.
The present study was part of a large monitoring program on the continental shelf off Sergipe and Alagoas, where the company Petróleo Brasileiro S.A. develops its activities of gas and oil production.This paper describes the spatial and seasonal distribution of the Paracalanidae species collected in eighteen stations in December 2001, 2002and June 2002, 2003.

Sampling and Sample Processing
The studied area is located in the northeastern coast of Brazil (Lat. 10º30' and 11º27'S;Long. 36º20' and 37º16'W).
Sampling was carried out in eighteen stations during the dry season (December 2001(December , 2002) ) and the rainy season (June 2002(June , 2003) ) on the continental shelf off Sergipe and Alagoas States.The stations were positioned at 10, 20 and 30 m isobaths along six transects, perpendicular to the shore line (Fig. 1).Water samples were taken with a Van Dorn bottle at two levels in the water column (surface and near the bottom) to analyze the environmental variables including salinity (refratometer), pH (digital pH meter), dissolved oxygen and chlorophyll-a (Strickland & Parsons, 1965) and nutrients (ammonia, nitrite, nitrate, phosphate and silicate -according to APHA,1995).In each station, water temperature ( o C) and water transparency (Secchi disc) were also determined before each plankton haul.
Oblique plankton tows were done during the day, using a plankton net with a 200 µm mesh size and 0.60 m diameter.A General Oceanic flowmeter was adjusted to the net mouth for measuring the water volume sampled during each haul.Samples were preserved in a buffered 4% formaldehyde solution.
Taxonomic composition and abundance were determined in subsamples obtained with a 5 ml Stempel pipette.The species abundance was expressed as number of individuals per cubic meter (ind.m -3 ).

Data Analysis
The cluster analysis was applied to the density matrix, after being normalized by log (x+1) transformation.The Bray Curtis dissimilarity coefficient and the Ward cluster method were used.The species were codified by four letters, the first two corresponding to genus name and the other two to species name.
Association among the copepod community and environmental variables were analyzed using canonical correspondence analysis -CCA with the Canoco program (ter Braak, 1987;1989).The relation between the inertia associated with CCA and the inertia of CA (correspondence analysis) indicated the extent to which the measured variables explained the variability in the species community.The robustness of this analysis was determined using the Monte Carlo's permutation test (ter Braak, 1986).

RESULTS
During the studied period the water temperature values ranged from 23.0 at station 9 (bottom layer) to 29.5ºC at station 17 (surface and bottom layers).Maximum differences between surface and bottom temperatures values were registered in December, 2001 at station 2 (3.0ºC), station 3 (2.5ºC),stations 9 and 12 (2.0ºC) and in December, 2002 at stations 2 and 3 (2.0ºC)(Table 1).
Salinity varied from 25.8 psu at station 3 (surface layer) to 39.3 psu at station 20 (bottom layer), both values registered in the rainy months (Table 1).In most stations salinity values of the bottom layer were slightly higher than those of the surface.However a higher salinity gradient was observed at stations 1, 2 and 3, located in the São Francisco plume, especially in June, 2002 (station 2 -12.3 psu and station 3 -13.3psu).
Dissolved oxygen ranged from 5.8 mg.L -1 at the 10 m isobath (bottom) to 8.9 mg.L -1 at the 10 m isobath (both layers).Higher values were measured in the rainy months in the surface layer of the water column.The pH values were above 8.0 in all water samples.Chlorophyll-a concentrations were low in general and its highest value was 2.8 µg.L -1 measured at the 10 m isobath in the dry season (Table 2).
The Paracalanidae family was represented by six species: Paracalanus quasimodo Bowman, 1971 Paracalanidae species densities in the continental shelf off Sergipe and Alagoas presented spatial and seasonal variations with higher values at the stations located at 10 m isobath and in the rainy season.
Paracalanus quasimodo was the dominant species, recorded in 95.8% of all analyzed samples and its relative abundance considering all studied period was 76.7%.Mean density values considering the dry months were 949, 740 and 41 ind.m -3 and the rainy months were 4231, 2389 and 1185 ind.m -3 in the 10, 20 and 30 m isobaths, respectively (Table 3).In fact, 81.9% of individuals of this species were registered in the June months.Density values were higher in the rainy months when the greatest abundance (9909 ind.m 3 ) was recorded at 10 m isobath.In the dry months the maximum of 6359 ind.m -3 was recorded at 20 m isobath.It was registered in salinity values between 25.8 and 39.3 psu and temperature values between 23.0 and 29.5ºC.
Paracalanus indicus occurred in 75% of the samples but the relative abundance was low (6.30%).Total means of the density values were 40, 53 and 19 ind.m -3 in the dry months and 164, 175 and 362 ind.m -3 in the rainy months at 10, 20 and 30 m isobaths, respectively.P. indicus was more abundant in the rainy months and even reached the maximum value of 2433 ind.m -3 at 30 m isobath (Table 3).In the present study this species was recorded in salinity values from 25.8 to 39.3 psu, and temperature values from 24.0 to 29.5ºC.Paracalanus aculeatus was registered in 75% of the total samples but it was less abundant.This population compounded 3.9 % of the Paracalanidae assemblage during the studied period.Overall means of the density values were 24, 22 and 4 ind.m -3 in the dry months and 230, 146 and 57 ind.m -3 in the rainy months, at 10, 20 e 30 m isobaths, respectively.Densities were higher in the rainy months when the maximum abundance (1682 ind.m -3 ) was registered at 10 m isobath (Table 3).In the shelf off Sergipe and Alagoas P. aculeatus occurred in salinity values between 25.8 and 39.3 psu, and temperature values between 23.5 and 29.5ºC.
Parvocalanus crassirostris occurred in 34.7% of the samples and its density values were low.This species was more frequent and abundant in stations located in the inner shelf during the dry season in contrast with the other species which presented higher densities in the rainy months.The maximum value was 329 ind.m -3 , recorded at 10 m isobath (Table 3).The distribution of P. crassirostris occurred in salinity values between 29.9 and 38.3 psu and temperature values between 24.0 and 29.0°C.Calocalanus pavo and Acrocalanus longicornis were mainly recorded at the 30 m isobath and presented low abundances.C. pavo presented a density peak (270 ind.m -3 ) in the rainy season.It was identified in 56% of all analyzed samples, in the salinity range from 25.8 to 39.3 psu, and in temperatures ranging from 23.5 to 29.5°C.Acrocalanus longicornis presented maximum density (123 ind.m -3 ) in the rainy season.This species occurred in salinities ranging from 25.8 to 39.3 psu and temperatures from 24.0 to 29.0ºC.
Cluster analysis revealed two groups of species.Group 1 compounded by oceanic species Calocalanus pavo and Acrocalanus longicornis and group 2 by coastal and shelf species such as Parvocalanus crassirostris, Paracalanus quasimodo, Paracalanus aculeatus, Paracalanus indicus and Paracalanus spp.(Fig. 2).Among the species of group 2 P. crassirostris was far apart from the other ones because it is a coastal species whose abundance was high in the dry season and basically remains restrict to 10 m isobaths.
The correlation analyses between the abiotic and biotic variables performed by the canonical correspondence analysis (CCA) revealed that samples of December 2001 and 2002 were correlated directly to nitrite and phosphate and inversely correlated to temperature.Conversely the samples of June 2002 and 2003 were directly correlated to nitrate, ammonia and temperature.The spatial gradient was associated with depth and salinity.The measured variables explained 35% of biotic data variance.(Fig. 3).
The Monte Carlo permutation test revealed that the Paracalanidae species distribution presented significant correlation to salinity, temperature and depth (p<0.05).
In the present study P. quasimodo was the dominant and most frequent species in all sampled months.The mean density values of this species were higher in the 10 m isobath, decreasing towards 20 and 30 m isobaths.It has been registered in other regions of the continental shelf off Northeast Brazil but not as one of the most abundant species (Neumann-Leitão et al., 1998;1999).Björnberg (1963;1980) characterized this species as abundant in coastal waters with salinity above 30 psu and in shelf waters of tropical regions.The dominance of P. quasimodo in the Brazilian shelf waters has been cited by Campaner (1985), Araujo et al. (1991), Vega-Pérez & Hernandez (1997) and Lopes et al. (1999).It was also registered in the mouth of estuarine areas where tidal currents have a great influence (Montú & Cordeiro, 1988;Lopes, 1994;Eskinazi-Sant'Anna & Tundisi, 1996).Paracalanus indicus seems to be a typically shelf species, more abundant in the 20 and 30 m isobaths.It was the second species in abundance as also recorded by Vega-Pérez & Hernandez (1997) and Lopes et al. (1999) in the Brazillian southeast shelf.P. indicus is a coastal and shelf species and jointly with P. quasimodo and P. aculeatus dominate most part of the Paracalanidae assemblages of the Brazilian coast (Björnberg, 1981;Bradford-Grieve et al., 1999).
P. aculeatus is an offshore and shelf species (González & Bowman, 1965;Bowman, 1971) and it has been recorded in the Brazilian coastal and shelf waters (Björnberg, 1963).It occurred in the dry and rainy months in all extension of the continental shelf off Sergipe and Alagoas as well.
P. crassirostris was more abundant on the inshore shelf, confirming its characteristics as an indicator species of coastal waters and reflecting the influence of estuarine outflow on the shelf.In Brazilian waters it was observed only in coastal or mixed coastal and shelf waters (Björnberg, 1963) and belongs to the central complex of species that appear in all estuaries along the East coast of Brazil (Almeida Prado-Por & Lansac-Tôha, 1984).
Calocalanus pavo and Acrocalanus longicornis were more abundant in the outer-shelf stations and in the rainy season.They are thermophile species, common in temperatures above 25°C (Björnberg, 1963).In the Northeastern Brazilian coast (Lat. 2 to 9 o ) C. pavo was the most abundant Paracalanidae species (Neumann-Leitão et al., 1999).In the dry months P. indicus and C. pavo presented higher abundance at stations located in the 20 m isobath while in the rainy months these populations were more abundant in the 30 m stations, probably avoiding low salinity waters of the inner shelf.
According to Bowman (1971) and Bradford-Grieve et al. (1999) A. longicornis is limited to oceanic waters of tropical and sub-tropical regions but in the present study it was recorded at 10, 20 and 30 m isobaths.Although this species had limited influence on community dynamics, its distribution may indicate the influence of oceanic water masses on the Sergipe and Alagoas shelf.Lopes et al. (1999) verified that copepod assemblages were strongly related to distinct water masses in the continental shelf off Rio de Janeiro.
The tropical zones of the oceans are usually considered to have low organic production and within this oligotrophic environment, trophic enrichments occur in response to wind-induced coastal upwelling along the continental shore (Dessier & Donguy, 1985).Besides the coastal upwelling contribution, the estuarine mangrove ecosystems play an important role as sources of food for marine food webs (Schwamborn et al., 1999) and replenishes inorganic components, mainly phosphorates, nitrogenates and silicates (Eskinazi-Leça et al., 2004).
Although the identified species have been registered in all isobaths, in the dry and rainy months, abundance values of the Paracalanidae assemblage presented very clear spatial and temporal patterns.The spatial pattern included maximum densities at the inner shelf in both seasons and the seasonal pattern was characterized by high abundances in the rainy season, when the water flux from estuarine areas increased.
The CCA analysis showed that samples collected in December (2001,2002) were associated directly to high nitrite and phosphate values and low temperatures.A slight vertical gradient of temperature was observed at stations located in the 20 and 30 m isobaths.Paes (2004) verified that in the December months the northeast winds transported surface waters (Ekman transport) and allowed the entrance of deep cold waters from SACW into the Sergipe shelf.The lowest temperatures were registered near the canyons of the São Francisco and Japaratuba rivers suggesting that coastal upwelling was occurring in these areas.In these months species densities were low.
In June (2002June ( , 2003) ) samples were associated to high temperature, nitrate and ammonia values.A salinity vertical gradient was only observed at the stations near the São Francisco river mouth.In the rainy season, runoff increases the water flux coming from estuaries and the surface salinity values decrease.All species presented density peaks during these months except Parvocalanus crassirostris.
In the studied area the Paracalanidae species distribution seems to be influenced by the estuarine waters and oceanic water masses as indicated by the significant correlations between salinity and temperature values and species densities in the Monte Carlo's permutation test.
Further studies about the dynamic of water masses at the Sergipe coast are essential to understand the distribution patterns of the zooplanktonic populations.

Fig. 1 .
Fig. 1.Continental shelf off Sergipe and Alagoas with the sampling stations.

Fig. 3 .
Fig. 3. Projection of stations, months and environmental variables on the first two axis of canonical correspondence analysis.D = depth; S = salinity; T = temperature; Si = silicate; s = surface; b = bottom.

Table 2 .
Continental shelf off Sergipe and Alagoas.Value ranges of the environmental variables in the dry months (December 2001/2002) and in the rainy months (June 2002/2003) at 10, 20 and 30 m depths.Surface (s); bottom (b).