Seasonal and Spatial Changes of Cephalopods Caught in the Cabo Frio (Brazil) Upwelling Ecosystem

BULLETIN OF MARINE SCIENCE, 52(2): 751-759, 1993

SEASONAL AND SPATIAL CHANGES OF CEPHALOPODS CAUGHT IN THE CABO FRIO (BRAZIL) UPWELLING ECOSYSTEM

Paulo Alberto S Costa and Flavio da Costa Fernandes

ABSTRACT Variations in the distribution and abundance of coastal cephalopods in the Cabo Frio (Brazil) region were studied from 71 trawl samples obtained between November 1986 and October 1988. Species abundance was compared over the depths sampled and their relationship with hydrological features investigated. Best catches were markedly associated with upwelling of nutrient-rich water (South Atlantic Central Water) during the spring-summer period, at depths from 45 to 60 m. Two species, Lo/igo sanpaulensis and Eledone massyae, account for most of this increase. Variations in abundance of these species are related to recruitment and periods of high productivity on the feeding grounds. Benthic octopods such as Octopus tehuelchus, O. vulgaris and Eledone gaucha occurred in small numbers at 60 m. Species broadly distributed in the western Atlantic, such as Semirossia tenera and Lo/igo plei, were also present.

Along the Rio de Janeiro coast (central-southern Brazilian littoral), peak squid catches in demersal fisheries occur from November to April (mid spring to early autumn), when northeastern and eastern winds create coastal upwelling off the Cabo Frio region (Costa and Haimovici, 1990). During this period, prevailing E-NE winds drive the Brazil Current surface waters offshore by Ekman transport, allowing the deeper and cooler South Atlantic Central Water to surface along the coast (Ikeda et aL, 1971; Mascarenhas et aL, 1971; Magliocca et aL, 1979). In summer, however, local phytoplankton blooms of less than 1 day, and low intensity (max. 6 /lg·liter-I of chlorophyll a) occur (Valentin, 1984; Valentin et aL, 1985). Although not comparable to the great upwelling regions (west Pacific and Atlantic coasts), the Cabo Frio upwelling area constitutes a peculiar ecosystem of the tropical Brazilian coast. The water masses of tropical oceans are the basic environmental matrix within which fisheries ecosystems must be studied (Longhurst and Pauly, 1987). The characteristics of a coastal upwelling system that determine its biological and fisheries impacts are rather complex. Here one frequently encounters concentra- tions of seabirds, pelagic fishes and other evidence of enhanced biological production. Voss (1983) and Rathjen and Voss (1987) discussed the aspects of cephalopod migrations and cited temperature as the prime factor. They suggested a probable relationship between seasonal temperatures, prevailing winds, and the inshore arrival of long-finned squid in southern New England in spring. A strong El Nino condition in the equatorial Pacific during 1983 elevated the sea water temperature along the California coast resulting in a reduction in squid production of 60 to 80% compared with the average catch. The purpose of this study is to examine the relationship between the presence of cephalopods in a tropical upwelling ecosystem and the environmental data to understand the fishery variations.

MATERIAL AND METHODS

Cephalopods were sampled monthly at depths of 30, 45 and 60 m with 20-min day-time hauls in the Cabo Frio region, central southern Brazilian littoral (23"S; 42°W), between November 1986 and

751 752 BULLETINOFMARINESCIENCE.VOL.52. NO.2. 1993

~ ,,11'" -~. ~ ,, ,, ,I

I .RW DE JANEIRO ,I I ,, , <'" \

.i'" .•••------'/ ,, ' ------"" '--100- ./

ATLANTIC OCEAN

Figure I. Map of the Cabo Frio region showing where the trawls were taken. Oceanographic stations 1-6 were at depths of 30, 45 and 60 m.

October 1988. The hauls were taken aboard the Research Vessel SUBOFICIALOLIVEIRA(Brazilian Navy). using an otter-trawl with 12 m footrope and cod-end mesh size of 25 mm, towed at approx- imately 3.0 knots. All the hauls were taken from the same area (Fig. I). Samples of near-bottom water were taken with Nansen bottles equipped with reversing thermometers at six stations, at the beginning and at the end of the hauls. Dissolved oxygen was analyzed according to Winkler's method (Strickland and Parsons, 1972) and salinity measured with a Beckman induction salinometer. The dorsal mantle length (ML) of all specimens was measured to the nearest 0.5 mm. The specimens were weighed, their sex determined, and the stage of maturity determined according to the five-step scale outlined by Juanico (J 983) for the squids and a three-step scale outlined by Sanchez (J 976) for the octopuses. All fwld collections were fixed in 10% formalin solution for a 48-h period and preserved in 70% ethanol. Abundance was calculated for each depth; frequencies of each species in the catches are given as the number of tows in which each species was found. The seasonal pattern of abundance was expressed as total biomass (kg·h-I) and its distribution according to the depth was calculated monthly. The mantle length distribution and the species density relationship with temperature range and water masses are also presented. COSTA AND FERNANDES: CEPHALOPODS FROM BRAZIL 753

NW w z o SW f0- e,.) S UJ II:: o SE

o E Z ~ NE

NDJ FMAMJ A SON 0 M J A S 0 1986 , 1987 1988

MONTHS Figure 2. Contour plot of the monthly averaged values of surface wind at Cabo Frio region between November 1986 and October 1988. No records from January to April 1988. Contour intervals are 1.5 m·sec·'.

RESULTS Hydrography. - The oceanography of Cabo Frio region has been studied since 1968. Available data include local wind stress and hydrographic observations. These records vary in length and completeness, and only temperature and wind intensity were used, and are the most useful for the purpose of this study. Variation in wind direction and intensity (m· secl) causes hydrographic changes through upwelling and changes in the Brazil Current position. Upwelling is favored during the spring-summer period (September to March) when prevailing E-NE winds can attain 9.5 m· sec· I (Fig. 2). The upwelling cycle is interrupted during fall-winter (April to August), when S-SW winds become progressively stronger increasing from 2.5 m 'sec! in Novemberto 7.5 m ·sec·l in June. Monthly variation of temperature, salinity and dissolved oxygen at the three different depths throughout the study period are shown in Figure 3. Bottom temperatures ranged from 13.3° to 24.2°C. The upwelling periods are characterized by the dominance of South Atlantic Central Water (rC < 18°; So/oo < 36.0), mainly during the austral summer, from September to April. Temper- atures were rarely higher than 18°C, and frequently lower than 16°C. Nevertheless, sporadically upwelled waters can also occur throughout the year, according to changes in wind direction and intensity. Colder waters « 14°C)recorded in March and August were caused by atypical E-NE wind and warmer waters (> 21°C) were observed mainly in June, indicating the presence of oceanic water of the Brazil Current (TOC > 18°; So/oo> 36.0), sometimes mixed with coastal water. Bottom salinities ranged from 34.7 to 36.50/00indicating the little variability in the area. Oxygen values varied from 3.54 to 6.62 mi, liter-I. Neither parameter showed a well-defined seasonal pattern. Species Composition and Size Structure. - A total of 2,147 cephalopods, belonging to eight species and four families was recorded, Table 1 lists the total number of individuals caught, their frequencies and the catch rates at each depth. Neritic squids, Loligo sanpaulensis and Loligo plei, amounted respectively to 74.2% and 13.2% of the total catch. Benthic species, Semirossia tenera (6.9%) and Eledone massyae (5.3%), were well represented, while Octopus vulgaris, O. tehuelchus and E. gaucha occurred in small numbers. Two immature specimens of the epipelagic octopod Argonauta nodosa were recorded at 60 m. The mean mantle length increased with depth for most of the species, except 24 ,.'I' .. (.) ' , 0 1\ ' , 22 : '\ ,I '. I i:\ : \ I ! \, I&l , I \ , I a:: ,,. . , i I, 20 , I :J , I , : I, ... (/\\ I ,: : / \ ~ , j ~. , \, a:: 18 , , \'d f \ I&l : ; \~i '. C1. \, , /!\ ~ , )/I \/ 16 .I' ." I&l I I ,/ .' ... , ,; ~_•.....~ 14

36.5 • " 0 ; \'. ~ i"""'0' 0 36 ...>- Z -I ~ rn 35

34.5

F M A M J J A SON 0 J FMAMJJASO 1987 I 1988 1 months ___ 30m _60m Figure 3. Monthly variation of temperature, salinity and dissolved oxygen. COSTA AND FERNANDES: CEPHALOPODS FROM BRAZIL 755

Table I. Total number of cephalopods caught by depth. Brackets indicate the frequency of capture in the trawls

Depths (m)

Species 30 45 60 Total %

Semirossia tenera 5 (3) 74 (8) 70 (13) 149 (24) 6.9 Loligo sanpalilensis 386 (15) 929 (21) 279 (21) 1,594 (57) 74.2 Loligo plei 57 (8) 177 (11) 46 (7) 280 (26) 13.2 Eledone massyae 8 (3) 106 (14) 114 (17) 5.3 Eledone gaucha 3 (3) 3 (3) 0.13 Octopus vulgaris 4 (4) 4 (4) 0.18 Octopus tehue/chus I (I) I (1) 0.05 Argonauta nodosa 2 (2) 2 (2) 0.09 Number of trawls 24 24 23 71 Total of specimens 448 1,188 511 2,147 Specimens' haul-I 18.7 49.5 22.2 30.3 Diversity (H') 0.64 0.98 1.80

for L. plei, in which it varied without a clear pattern (Fig. 4). The sex ratio was nearly 1:1 for L. sanpaulensis and L. plei. A larger proportion of females was observed for E. massyae and S. tenera. The total number of species increased with depth: three species were found at 30 m, four at 45 m and eight species at 60 m depth. Specific diversity (Shannon's index) also increased with depth; 0.6, 0.9 and 1.8 respectively (Table 1). Distribution oj Catches. - Mean faunal density, measured as catch per haul, was 30.3 specimens' haul-I. Higher catches were obtained in spring and summer, with maxima of 52.3 and 79.3 specimens' haul-I respectively. Most catches were of two squids; L. sanpaulensis and L. plei. The first species constitutes the most abundant cephalopod in this study; an average of 22.4 individuals' haul-1 was recorded for the whole period, attaining 256 individuals' haul-I during spring and

~ pl.i ~ aonpalll.nsi. $.mlrOllid !.!l!.!..!:!! ,EI.dDnt mu,a.

n = 57 n = 366 n = 5 30m ML = 45.7 ML= 42.1 eM= 16.2

o~ n = 929 n = 74 n = 6 45 m ML= 43.9 ML= 17.7 ML=58.7

60m

010 MANTLE LENGTH Imml Figure 4. Length frequency distribution of the species by depth of capture. 756 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.2, 1993

_30m ~ 45m ~ 60m

OJ FMA M J J AS 0 NO J FM AM J J A 5 Q I 1987 I 1988 I months Figure 5. Monthly variation of cephalopod catch per unit of effort (CPU E) by depth. summer. Recruitment accounts for most of this increase. The abundance of L. plei varies without a seasonal pattern, although both species were more abundant at 45 m (Table 1). Cephalopod abundance (kg' h·l) varied markedly with depth and sampling period. Best catches were obtained from September to March with higher yields at 45 and 60 m depths (Fig. 5), when low temperature « 18°C) upwelling waters (SACW) were more frequent. These maxima were largely determined by the largest catches of L. sanpaulensis at 45 m and E. massyae at 60 m. The species abundance in the T-S diagram (Fig. 6) allowed a global view of the influence of hydrological conditions in relation to the species densities, enabling the characterization, individualization or grouping of samples collected on the crUIses. The physicochemical gradient between 12°C and 18°C of temperature and salinity from 35.00/00to 35.90/00depicts cold and rich upwelling water (SACW), from the poor and more saline warm water (BC, CW). The concentration of points recorded below 18°C correspond to 74.6% of the samples and 84% of the total number of cephalopods caught (N = 2,147), eVIdencing the strong influence of upwelling water in the distribution of catches. Otherwise, the points allocated at temperatures higher than 18°C conform to the influence of tropical waters (BC, CW), representing only 25% of samples and 16.4% of cephalopods.

DISCUSSION The results enable us to distinguish seasonal changes in species abundance in terms of their distribution according to different water types. Higher faunal density and biomass coincided with upwelling events mainly observed during spring and summer months under the influence of South Atlantic Central Water in the region. This pattern follows the seasonal catch trends landed by shrimp trawlers along the Rio de Janeiro littoral (Costa and Haimovici, 1990). COSTA AND FERNANDES: CEPHALOPODS FROM BRAZIL 757

35 35,5 36 SALINITY %. I I SACW 12

/4 ®

16 I U I . •I I l(J ,J a:: ;j . t- 16 « a:: w Q. ::IE w 20 l- e «:) e • 22 ~ 0 ® ~O '24

~>IOO Ind.

§ 10 to 100 Ind. 0 \0 to 100 Ind. ~ 10 to 100 Ind .• 10 to 100 Ind. e I to 100 Ind. 0 I to 100 Ind. ~ I to 100 Ind. • 1 to 100 Ind. L. sanpau/ens/s L.p/ei E massyae $.tenera Figure 6. Distribution of cephalopod species according to the water masses present at the study area. SACW: South Atlantic Central Water; BC: Brazil Current; CW: Coastal Water; ind·h-I = number of individuals per 2Q-min haul.

The Cabo Frio hydrological system is characterized mostly by its sensitivity to winds. Onset of upwelling coincides with the more frequently cool water temperatures between September and March. During this period, under the influence of prevailing E-NE winds and Coriolis deviation, the surface water of the Brazil Current flows toward the open sea and is replaced by South Atlantic Central Water, which moves northward below the Brazil Current, as a result of the mixture between tropical and subantarctic water (Thomsen, 1962). This upwelling of cold, nutrient-rich water results in areas of high productivity which provide feeding grounds for squid (Voss and Brakoniecki, 1985). The squids, L. sanpaulensis and L. plei, showed great fluctuations in their abundance, apparently influenced by temperature changes and water mixing. Al- though both species were caught in most of the hauls, numerical dominance of L. sanpaulensis was always observed. These observations support those of Juanico (1979) and Haimovici and Perez (1991). However, we do not dismiss the pos- sibility that the distributional patterns reported here reflect problems of interpre- tation due to the relatively small area sampled. Global distribution of these two 758 BULLETINOFMARINESCIENCE,VOL.52,NO.2. 1993 species of Loligo in the Atlantic indicates that they are associated with different water types: L. plei is a widespread species in tropical and subtropical waters of the western Atlantic, extending from 35°N to northern Argentina (35°S) and L. sanpaulensis in the Subtropical Convergence Zone, occurs from 200S to 42°S (Roper et a1., 1984). The benthic genera, Semirossia and Eledone. were found mainly at depths deeper than 45 m, and their variability in abundance seems to be closely related to seasonal, shoreward reproductive migrations. Mature individuals of E. massyae were predominant in the samples (91.7%). Spermatangia and free sperm were found within the ovaries of females in many specimens suggesting reproductive activity in the area. According to Coelho (1985), benthic species, or at least those species lacking a pelagic phase during early development, take advantage of areas with high productivity (upwelling zones), These animals, due to their limited mobility, need to select areas with optimal conditions to spawn and grow. It is worth noting, however, that no egg masses of either species were found by us. Our results suggest that E. massyae migrate towards the shore to feed and mate during spring and early summer, leaving the shelf in late summer, probably to spawn in slope (deeper) waters. Comparing our data with those in Haimovici and Andriguetto (1986), we found that the number of species and the species abundance were similar in both areas. All the species found off Cabo Frio (Lat 22°S) also occur in Rio Grande do SuI shelf (Lat 34°S). This region, as stated by Palacio (1982) is typically transitional between a tropical or Caribbean Province (Milne-Edwards, 1838) and a warm- temperate or Patagonian Province (d'Orbigny, 1835-48). The cephalopod fauna along this part of the coast and shelf are dominated by subtropical and warm- temperate species, including a small percentage of species from both adjacent provinces, as well as species broadly distributed in the western Atlantic.

ACKNOWLEDGMENTS

We gratefully acknowledge M. Haimovici and J. H. Leal for their helpful suggestions and critical reviews of the manuscript. We wish to extend our thanks to our colleagues at the Instituto de Estudos do Mar Alte Paulo Moreira, and crews of the Research Vessels SUBOFICIALOLIVEIRAand MIGUELDOS SANTOSwho provided assistance during the course of this study.

LITERATURE CITED

Coelho, M. L. 1985. Review of influence of oceanographic factors on cephalopod distribution and life cycles. NAFO Sci. Council Studies 9: 47-57. Costa, P. A. S. and M. Haimovici. 1990. A pesca de polvos e lulas no litoral do Rio de Janeiro. Ciencia e Cultura 42(12): 1124-1130. Haimovici, M. and 1. M. Andriguetto-Filho. 1986. Cefalopodes costeiros capturados na pesca de arrasto do litoral suI do Brasil. Arq. BioI. Tecnol. 29(3): 473-495. -- and J. A. A. Perez. 1991. Abundancia e distribui~ao de cefalopodes em cruzeiros de prospec~ao pesqueira demersal na plataforma extema e talude continental do suI do Brasil. Atlantica, Rio Grande 13(I): 189-200. Ikeda, Y., L. B. Miranda and N. J. Rock. 1971. Observations on stages of upwelling in the region of Cabo Frio (Brazil) as conducted by continuous surface temperature and salinity measurements. Pages 74-97 in Proceedings of the United Nations Panel Meeting on the Establishment and Implementation of Research Programmes in Remote Sensing. Report 14, United Nations, New York. Juanico, M. 1979. Contribui~ao ao estudo da biologia dos cefal6poda Loliginidae do atlantico suI Ocidental entre Rio de Janeiro e Mar del Plata. Ph.D. Dissertation, IOUSP, Sao Paulo. 103 pp. --. 1983. Squid maturity scales for population analysis. Pages 341-378 in J. F. Caddy, ed. Advances in assessment of world cephalopod resources. FAO Fish. Tech. Paper, 231. Longhurst, A. R. and D. Pauly. 1987. Circulation of tropical seas and oceans. Pages 27-55 in A. R. Longhurst and D. Pauly, eds. Ecology of tropical oceans. Acad. Press Inc., London. 407 pp. COSTAANDFERNANDES:CEPHALOPODSFROMBRAZIL 759

Magliocca, A., L. B. Miranda and S. S. Signorini. 1979. Physical and chemical aspects of the upwelling at southwest of Cabo Frio (Lat. 23"S-Long. 42°W). Bol. Inst. Oceanogr., Sao Paulo 261: 11-30. Mascarenhas, A. S., L. B. Miranda and N. J. Rock. 1971. A study of the oceanographic conditions in the region of Cabo Frio. Pages 285-308 in J. D. Costlow Jr. ed. Fertility of the sea, Vol. 1. Gordon and Breach, New York. Pp. 238-308. Milne-Edwards, H. 1838. Memoir sur la distribution geographique des crustacees. Annis. Sci. nat., Zool. 129-174. d'Orbigny, A. D. 1835-1848. Voyage dans I'Amerique Meridionale execute pendant les annees 1826, 1827, 1828, 1829, 1830, 1831 1832 et 1833. Tome V. Partie 3. Mollusques. Paris et Strasbourg. Pp. 1845-55. Palacio, J. F. 1982. Revision zoogeografica marina del sur del Brazil. Bol. Inst. Oceanogr. Sao Paulo, 31(1): 69-92. Rathjen, W. F. and Voss, G. 1987. The cephalopod fisheries: a review. Pages 253-267 in P. R. Boyle, cd. Cephalopod life cycles, Vol. II. Acad. Press Inc. London. Roper, C. F. E., M. J. Sweeney and C. E. Nauen. 1984. FAO species catalogue, Vol. 3. Cephalopods of the world. An annotated and illustrated catalogue of species of interest to fisheries. FAO Fish. Synop. 125(3): 277 pp. Sanchez, P. 1976. Contribueion al estudio de la maturaeion sexual de Eledone cirrhosa (Lamarck). Barcelona, Tesis de Licenciatura. Universidade de Barcelona, Barcelona 39 pp. Strickland, 1. D. H. and T. R. Parsons. 1972. A practical handbook of seawater analysis. Fish Res. Board. Can. 167: 310 pp. Thomsen, H. 1962. Massas de agua caracteristicas del Atlantico (parte sudoeste). Servo Hidrografia Naval, Secret. Mar., Buenos Aires Public. H 632: 1-27. Valentin, J. L. 1984. Analyse des parametres hydrobiologiques dans la remontee de Cabo Frio (Bresil). Mar. BioI. 82: 259-276. ---, N. M. Lins da Silva and C. T. B. N. Bastos. 1985. Les diatomees dans I'upwelling de Cabo Frio (Bresil): list d'especes et etude eeologique. J. Plankton Res. 7: 313-337. Voss, G. L. 1983. A review of cephalopods fisheries biology. Mem. Nat. Mus. Viet. 44: 229-241. --- and T. F. Brakonieeki. 1985. Squid resources of the Gulf of Mexico and Southeast Atlantic coasts of the United States. NAFO Sci. Council Studies 9: 27-37.

DATEACCEPTED:February 26, 1992.

ADDRESS: Instillllo de ESludos do Mar AIle Paulo Moreira. Arraial do Cabo. 28910 Rio de Janeiro. Brazil.