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Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. v.37 n.3 Valparaíso  2009

 

Lat. Am. J. Aquat. Res., 37(3): 409-428, 2009
DOI: 10.3856/vol37-issue3-fülltext-ll

Research Article

 

Biological patterns of the Argentine shortfin squid Illex argentinus in the slope trawl fishery off Brazil

Patrones biológicos del calamar argentino Illex argentinus en la pesquería de arrastre en el talud continental de Brasil

 

José Angel Alvarez Perez1, Tiago Nascimento Silva2, Rafael Schroeder1,3 Richard Schwarz1,3 & Rodrigo Silvestre Martins4,5

1 Grupo de Estudos Pesqueiros. Centro de Ciências Tecnológicas da Térra e do Mar. Universidade do Vale do Itajaí, Rúa Uruguai 458, Centro, Itajaí, SC, Brazil. Corresponding author: José Ángel Alvarez Pérez (angel.perez@univali.br)
2Biogás Energia Ambiental S.A., Rúa Mogeiro 1580. Bairro Perus, 05206-240 São Paulo, SP, Brazil
3
Curso de Pós-Graduação em Ciencia e Tecnología Ambiental, Centro de Ciências Tecnológicas da Térra e do Mar, Universidade do Vale do Itajaí, Rúa Uruguai 458, Centro, Itajaí, SC, Brazil
4Marine and Coastal Management (MCM), Private Bag X2, Rogge Bay 8012, Cape Town, South Africa
5Zoology Department and Marine Research Centre, University of Cape Town, Private Bag X3, Rondebosch 7701, Cape Town, South Africa


ABSTRACT. Commercial exploitation of the Argentine shortfin squid (Illex argentinus) was virtually non-existent in Brazilian waters until 2000 when foreign trawlers initiated their operations on slope grounds as part of a government-induced chartering program. Since then, the species has been included among the targets of a developing slope trawl fishing off southeastern and southern Brazil. Biological samples were collected from commercial catches of 25 national and seven foreign (chartered) trawlers between 23°-33°S and 170-740 m depth. These samples represent two periods of the commercial exploitation oí Illex argentinus in Brazil: 2001-2003, when both chartered and national trawlers operated simultaneously, and 2006-2007, when only national vessels continued to exploit I. argentinus along with other slope stocks. Catches contained immature and ma-turing squid throughout the year, as well as at least two distinct, fully mature, spawning groups: one composed of small-sized males and females present year-round on the shelf-break/ upper slope (< 400 m), and the other consisting of large squid present only in austral winter-spring in southern (26°-29°S ) and deep fishing grounds (400-700 m). The latter group has sustained the large winter catches reported since 2000 and the large sizes and concentrations of the specimens sparked the interest of the fishing industry as a potential target of the slope fishery. The reproductive attributes and temporal/ spatial distribution patterns of winter spawners support the hypothesis that relates this group to migrating concentrations of a north Patagonian shelf stock. If confirmed, the present data would underscore the need to consider multinational shared stock management strategies in the SW Atlantic.

Keywords: ommastrephid squid, Illex argentinus, slope trawl fishery, southern Brazil.


RESUMEN. La explotación comercial del calamar argentino (Illex argentinus) no existía en aguas brasilenas hasta el año 2000, cuando buques extranjeros iniciaron sus operaciones en el talud como parte de un programa gubernamental de arrendamiento. Desde entonces la especie forma parte de un conjunto de recursos que han motivado el desarrollo de una pesquería de arrastre en el talud del sur y sureste de Brasil. Se colectaron muestras biológicas de las capturas comerciales de 25 buques arrastreros nacionales y siete extranjeros entre los paralelos 23°-33°S y en profundidades de 170 a 740 m. Estas muestras representaron dos periodos de la explotación comercial de I. argentinus en Brasil: 2001-2003, cuando buques nacionales y extranjeros operaron simultáneamente, y 2006-2007 cuando sólo buques nacionales permanecieron explotando el calamar argentino en conjunto con otros recursos del talud. Las capturas estuvieron constituidas por calamares inmaduros y en-maduración a lo largo de todo el año, así como al menos dos grupos distintos de individuos maduros y desovantes: un grupo constituido por machos y hembras de pequeño tamaño que están presentes en todas las estaciones del año en el borde de la plataforma continental y talud superior (< 400 m), y otro grupo, constituido por calamares de gran tamaño, presente solamente durante el invierno-primavera australes en areas surenas (26°-29°S ) y profundidad (400-700 m). Este grupo ha sostenido las grandes capturas invernales reportadas desde 2000 y, dado su largo tamaño y concentración, ha justificado el interés de la industria pesquera como un potencial recurso para la pesca en el talud. Características reproductivas y patrones de distribución temporales/ espaciales de los desovantes de invierno corroboran la hipótesis que les relaciona a concentraciones migratorias de stock del norte de la plataforma Patagónica. Si se confirma esta hipótesis, estos datos resaltan la importancia de considerar estrategias de manejo dirigidas a stocks compartidos en el Atlántico SW.

Palabras clave: calamares omastréfidos, Illex argentinus, pesquería de arrastre de talud, sur de Brasil.


INTRODUCTION

Squids nave long represented important bycatch components of the multispecific trawl fishery off Brazil (Costa & Haimovici, 1990; Pérez & Pezzuto, 1998). On the continental shelf, loliginids nave further become seasonal targets of both hand jigging and trawl fisheries, as they are densely concentrated in space and time (Pérez, 2000; Martins & Pérez, 2007). In recent years, however, commercial landings of the ommastrephid Argentine shortfin squid Illex argentinus (Castellanos, 1960) nave been recorded in the southeastern and southern sectors of the Brazilian coast and nave placed this squid among the main cephalopod resources exploited in the country (Pérez et al., 2009a).

The species is distributed in the SW Atlantic from Rio de Janeiro (23°S ) to southern Argentina (54°S ) sustaining, on the Patagonian shelf and around the Falkland (Malvinas) Islands, one of the largest cephalopod fisheries in the world (Boyle & Rodhouse, 2005). Off Brazil, several fishing surveys conducted since the 1970s have revealed important concentrations of paralarvae, juveniles, and spawning individuals, particularly in the shelf break and slope waters of the southern coast (south of 25°S ) (Haimovici & Andriguetto Fo, 1986; Haimovici & Pérez, 1991; Haimovici et al., 1995, 2007, 2008). In this área, the species has also been often found in stomach contents of large predators, and it is regarded as one of the key components of both pelagic and demersal trophic chains (Santos & Haimovici, 2000; Gasalla et al., 2007).

Commercial exploitation of the Argentine shortfin squid was virtually non-existent in Brazilian waters until 2000, when foreign-chartered trawlers initiated their operations on the slope grounds south of 20°S (Pérez et al., 2003, 2009b). In that year, the Portu-guese trawler "Joana" landed approximately 48 ton of this species caught during one fishing trip between 26-29°S and 235-401 m isobaths (Pérez et al., 2003). In 2002, the South-Korean trawler "In Sung 207" exploited the same área in winter (June-September) catching, on average, 199 kg of I. argentinus per trawling hour. After four fishing trips, this vessel landed a total of 1,400 ton, the largest catch ever recorded in Brazilian waters (Pérez et al., 2009b). In total, landings of I. argentinus that year reached 2,601 ton, nearly twice the amount recorded for other squids (mostly loliginids). These catches, however, decreased to 100-400 ton in the following years, as chartered trawlers either abandoned Brazilian waters or moved to deeper areas (> 700 m). Since then, national trawlers have included I. argentinus among the targets of a developing "upper slope" (250-500 m) trawl fishery (Pérez & Pezzuto, 2006; Pérez et al., 2009a).

Preliminary assessments of this fishery have considered I. argentinus to be a seasonal resource with a fishing potential that has not been objectively defined but that is generally considered to be highly variable and unpredictable (Haimovici et al., 2006). The main questions regarding the biological aspects of I. argentinus commercial exploitation off Brazil, however, revolve around its complex population structure and potential connections with migrating stocks exploited off Uruguay and Argentina (Pérez et al., 2003; Haimovici et al., 2006). As most ommastrephid squids, I. argentinus is a short-lived species (~1 year) that matures late in Ufe and dies after a single and terminal spawning event (Haimovici et al., 1998). Because generations do not overlap in time, population resilience is highly dependent on recruitment and, consequently, annual abundances typically exhibit wide oscillations, as do commercial catches (Boyle & Rodhouse, 2005). Associated with this extreme life history pattern, ommastrephids tend to combine extended spawning seasons, long reproductive migrations, and the passive transport of offspring by surface geostrophic currents to produce both seasonal and geographic population units (stocks); this complex structure is regarded as an evolutionary strategy to minimize the risks of semelparity (O'Dor, 1998).

In the SW Atlantic, at least four stocks were distinguished from general size-at-maturity patterns: summer spawning stock (SSS), south Patagonian stock (SPS), Bonaerensis north Patagonian stock (BNS), and southern Brazil stock (SBS) (Brunetti, 1988; Haimovici et al., 1998). The latter group included the main concentrations of spawning squid found in winter months on the slope off southern Brazil (Haimovici & Pérez, 1990; Santos & Haimovici, 1997). Growing biological evidence (Le. maturation patterns, trophic relationships, the occurrence of certain parasites, statolith morphometrics), however, suggests that these squid are in fact BNS members that migrate north to spawn in Brazilian waters (Santos & Haimovici, 1997; Schwarz & Pérez, 2007). Although local spawning was also observed occuring off Brazil throughout the year, winter spawning was potentially linked to recruitment off the northern Patagonian shelf through paralarval transport by the Falkland (Malvinas) - Brazil Current system (Haimovici et al., 1995). In this context, this study analyzes biological attributes of commercial catches of the Argentine shortfin squid off southern Brazil as a descriptive approach to assess both the population structure subject to the seasonal exploitation regime and the hypothesis of a shared stock scenario.

MATERIAL AND METHODS

Biological samples of the Argentine shortfin squid were obtained from commercial catches of 25 national and seven foreign (chartered) trawlers all derived from operations in the southeastem and southern sectors of the Brazilian coast (Fig. 1) between 23°-33°S and 170-740 m depth. Samples represent two periods of the species' commercial exploitation in Brazil: 2001-2003, when both chartered and national slope trawlers operated simultaneously, and 2006-2007, when only national vessels continued to exploit I. argentinus along with other slope stocks (Table 1) (Pérez & Pezzuto, 2006; Pérez et al., 2009b).


Figure 1. Spatial distribution of Argentine shortfin squid Illex argentinus catches off southeastem and southern Brazil. a) chartered trawlers (2001-2003), b) national trawlers (2006-2007). Latitude and longitude were decimal transformed.

Figura 1. Distribución espacial de las capturas del calamar argentino Illex argentinus en el sureste y sur de Brasil, a) arrastreros arrendados (2001-2003), b) arrastreros nacionales (2006-2007). Latitudes y longitudes fueron transformadas en valores decimales.



Table 1. Summary of data for the Argentine shortfin squid Illex argentinus obtained from chartered and national trawlers operating off Brazil between 2001 and 2007. N: number of individuals; Min-Max: smallest and largest mantle length (ML) and total wet body weight (BW).

Tabla 1. Resumen de datos de calamar argentino Illex argentinus obtenidos en las operaciones de pesca de arrastreros arrendados y nacionales en Brasil entre 2001 y 2007. N: número de individuos, Min-Max: valores máximos y mínimos de la longitud del manto (ML) y peso total húmedo (BW).

Onboard observers collected samples from chartered trawlers for all fishing trips conducted principally between September 2001 and April 2003. After each positive trawl, a sample was taken from the catch and deep-frozen for posterior analysis in the laboratory ashore. Each sample had detailed information on trawl position (lat-long), date, time, and fishing effort (trawling hours). Samples from national trawlers were collected from landings at the harbors of Santa Catarina state (southern Brazil) as part of a daily fishery sampling program (Pérez et al., 1998). From each landed catch, approximately 20 kg of squid were measured for their dorsal mantle length (ML) to the nearest centimeter, and a length stratified subsample was taken to the laboratory. These subsamples could not be related to individual trawls conducted during each fishing trip, but represented the entire fishing área covered by it. Information on the fishing área, effort (mean trawl duration, number of trawls per day, trip duration in days), and total catch were obtained during interviews with skippers at the time of the landings.

In the laboratory, the ML and the total body weight (BW) were recorded to the nearest millimeter and gram, respectively. After dissecting the mantle, males and females were differentiated and maturity stages were assigned according to the macroscopic scale proposed by Brunetti (1990). This scale defined seven and eight maturity stages for males and females, respectively, including: immature (stages I and II), in maturation (stage III), early maturity (stage IV), advanced maturity (stage V), spawning (stage VI for males and stages VI and VII for females), and spent (stage VII for males and stage VIII for females).

In females, the ovary and accessory organs (ovi-duct + nidamental glands + oviducal gland) were weighed (OW and AOW, respectively), the nidamental gland length was measured (NGL), and the gills were checked for the presence of spermatophores as signs of mating. In males, the testis and accessory organs (spermatophoric complex + Needhan's sac + penis) were weighed (TW and AOW, respectively), the testis length was measured (TL), and the Needhans's sac was examined for the presence of spermatophores. All weights were taken to the nearest 0.1 g and measurements to 0.1 mm.

Maturation in males and females was expressed numerically by three indices:

a) the Gonadosomatic index defined for males (GSIM) and females (GSIF) as:

b) the Hayashi index (HI) defined for males (HIM) and females (HIF) as

c) the Testis (TI) - Nidamental Gland (NGI) indices defined as

A data bank was produced in which each squid was described by its origin (sample, landing date), sex, size (ML, BW), and reproductive characteristics (maturity stage, OW, TW, AOW, GSI, HI, TI/ NGI).

Size-at-maturity was assessed from the cumulative ML frequency distribution of mature and spawning males and females (stages > IV). This distribution was linearized by the probit transformation of cumulative ML frequencies and a straight line was then fitted to the transformed frequency vs. ML class relationship using the least-squares method. Precise ML at different percentiles were then estimated by substituting the probit values in the estimated linear equation (Le. probit 5 corresponds to 50% percentile):

where pf is the probit transformed ML cumulative frequency and c and d are the intercept and the slope of the fitted line, respectively.

Population differentiation among squid caught by commercial trawlers was explored through a multivariate Principal Component Analysis (PCA) applied separately for males and females. Variables included in this analysis involved size and reproductive attributes (BW, GSI, HI, TI/ NGI), day-of-the-year (DYR), decimal latitude (LAT), decimal longitude (LONG), and depth (DEPTH). A correlation matrix was calculated for the variables (previously standardized as a proportion of their mean) and new axes (factors) were extracted in the direction of greatest variance. These factors were linear combinations of the original variables and used to interpret the potential existence of biologically similar groups of squids and their occurrence in space and time.

RESULTS

Size structure of catches

Males and females caught during slope trawl fishing exhibited a bi-modal ML frequency distribution (Fig. 2). Males ranged from 78 to 340 mm ML, exhibiting one pronounced mode centered around 160 mm ML and a secondary mode between 220 and 240 mm ML. Females were generally larger, ranging from 91 to 395 mm ML. A main modal group was formed around 180 mm ML and a less pronounced one between 280-320 mm ML (Fig. 2, Table 1). The overall size structures remained practically unchanged as the catches by the chartered and national trawlers in 2001-2007 were examined separately, although larger females were found in the former (Fig. 2).


 

Figure 2. Mantle length frequency distributions (in mm) of males and females of the Argentine shortfin squid Illex argentinus caught by commercial trawlers off Brazilian coast between 2001 and 2007. a) total catches, b) male catches obtained by chartered vs. national trawlers, c) female catches obtained by chartered vs. national trawlers.

Figura 2. Distribución de tallas (largo de manto ML en mm) de machos y hembras del calamar argentino Illex argentinus capturados por arrastreros comerciales en la costa de Brasil entre 2001 y 2007. a) capturas totales, b) capturas de machos obtenidas por arrastreros arrendados y nacionales, c) capturas de hembras obtenidas por arrastreros arrendados y nacionales.

During the early exploitation period (2001-2003), the size structure of the chartered fleet catches varied with the season, latitude, and depth of commercial operations (Figs. 3 and 4). Large males (ML > 200 mm) dominated catches obtained in winter (July-September) south of 28°S , between 350-540 m depth (Fig. 3). During the rest of the year, catches were generally unimodal, concentrating on individuals between 100-250 mm ML that originated north of 28°S and on the upper slope (< 400 m depth). In females, the patterns observed were virtually the same (Fig. 4), with an uniform group of individuals (100-250 mm ML long) dominating the catches throughout the year, except for winter months when a distinct group of large females was caught in southern (south of 28°S ) and deeper (> 350 m) areas.


Figure 3. Size structure of male Illex argentinus caught by chartered trawlers off Brazil between 2001 and 2003. Mantle length frequency distributions (in mm) are presented by latitudinal (left column) and depth (right column) strata. Colors differentiate maturity stages according to the Brunetti (1990) macroscopic scale.

Figura 3. Estructura de tallas de machos del calamar argentino Illex argentinus capturados por arrastreros arrendados en Brasil entre 2001 y 2003. Las distribuciones de frecuencia de tallas (largo de manto ML en mm) están presentadas por estratos latitudinales (columna de la izquierda) y estratos batimétncos (columna de la derecha). Los colores diferencian los estadios de maduración sexual según la escala macroscópica de Brunetti (1990).


Figure 4. Size structure of female Illex argentinus caught by chartered trawlers off Brazil between 2001 and 2003. Mantle length frequency distributions (in mm) are presented by latitudinal (left column) and depth (right column) strata. Colors differentiate maturity stages according to the Brunetti (1990) macroscopic scale.

Figura 4. Estructura de tallas de hembras del calamar argentino Illex argentinus capturadas por arrastreros arrendados en Brasil entre 2001 y 2003. Las distribuciones de frecuencia de tallas (largo de manto ML en mm) están presentadas por estratos latitudinales (columna de la izquierda) y estratos batimétncos (columna de la derecha). Los colores diferencian los estadios de maduración sexual según la escala macroscópica de Brunetti (1990).

Slope trawling between 2006-2007, as conducted by the national fleet, concentrated on the larger fractions of both males and females (Fig. 5). These fractions were generally obtained in areas south of 29° S (Fig. 1), inshore of the 400 m isobath, and in autumn (April-June) and winter (July-September) months.


Figure 5. Size structure of lllex argentinus caught by national trawlers off Brazil between 2006 and 2007. Mantle length frequency distributions (in mm) are presented for males and females by latitudinal (left column) and depth (right column) strata. Colors differentiate maturity stages according to the Brunetti (1990) macroscopic scale.

Figura 5. Estructura de tallas del calamar argentino lllex argentinus capturados por arrastreros nacionales en Brasil entre 2006 y 2007. Las distribuciones de frecuencia de tallas (largo de manto ML en mm) de machos y hembras están presentadas por estratos latitudinales (columna de la izquierda) y estratos batimétricos (columna de la derecha). Los colores diferencian los estadios de maduración sexual según la escala macroscópica de Brunetti (1990).

Maturation and maturity stages

Males and females in all maturity stages were present in the slope trawling catches off southeastern and southern Brazil (Table 2). The spawning stage (stage VI) was the most frequently identified maturity condition in both sexes and nearly 50% off all individuals caught were at least in an early maturity stage (stage IV and higher). This overall maturity stage composi-tion was observed in 2001-2003 but shifted towards a complete dominance of spawning (and spent) squid after 2003, as the national trawlers that continued to exploit the Argentine shortfin squid tended to catch and land larger males and females (Fig. 6).


Table 2. Summary of the maturity conditions of the Argentine shortfin squid Illex argentinus in commercial trawl catches off Brazil between 2001 and 2007. Examined males and females were pooled by maturity stages (after Brunetti, 1990) and the relative and cumulative frequencies of each stage were calculated and expressed in percentages (% and Cum.% respectively). The largest (Max) and smallest (Min) mantle length of squid in each maturity stage are indicated. Males with no, few, and many spermatophores (spermat.) in the Needhan's sac and females with and without spermatophores at the base of the gills were also quantified for each maturity stage.

Tabla 2. Resumen de las condiciones de madurez sexual de calamar argentino Illex argentinus en capturas comerciales de la pesca de arrastre en Brasil entre 2001 y 2007. Los machos y hembras examinados fueron agrupados por estadios de madurez (según Brunetti, 1990). Para cada estadio se calcularon las frecuencias relativas y acumuladas expresadas en valores porcentuales (% y Cum.% respectivamente). Para cada estadio de madurez sexual se indica la longitud máxima (Max) y mínima (Min) del manto. También se contaron para cada estadio de madurez los machos con ninguno, pocos o muchos espermatóforos (spermat.) en la bolsa de Needhan y las hembras con y sin espermatóforos en las bases de las branquias.


Figure 6. Annual distribution of mantle length (ML in mm) (right column) and maturity stages (left column) of the Argentine squid Illex argentinus in commercial catches off Brazil. a and b, males; c and d, females. Size distributions are represented by cumulative frequencies.

Figura 6. Distribución anual de tallas (largo de manto ML en mm) (columna de la derecha) y estadios de maduración sexual (columna de la izquierda) del calamar argentino Illex argentinus en capturas comerciales en Brasil, a y b, machos; c y d, hembras. Las distribuciones de tallas están representadas por las frecuencias cumulativas.

Catches included immature males and females as small as 78 and 91 mm ML, respectively. Spawning males (stage VI) and females (stage VII) attained the largest sizes (Table 2). Squids of both sexes enlarged homogenously as maturation progressed. At an advanced maturity-spawning condition (stages V, VI, and VII), however, two distinct size groups were found (Fig. 7). The first group was dominant in the samples and was composed of males and females ranging from 140-180 mm ML and 160-240 mm ML, respectively. The second group was less abundant but included larger individuals (males > 200 mm ML; females > 260 mm ML). Male size-at-maturity was estimated to be 163.3 mm ML and 211.8 mm ML for the smaller and larger modal groups, respectively (Fig. 8). In females, size-at-maturity was estimated to be 201.3 mm ML for the smaller modal group and 292.3 mm ML for the larger one.


 

Figure 7. Size distribution (mantle length in mm) of the Argentine squid Illex argentinus caught by commercial trawlers off Brazil between 2001-2007 according to sexual maturity stages (defined following Brunnetti, 1990). a) males, b) females.

Figura 7. Distribución de tallas (largo de manto ML en mm) del calamar argentino Illex argentinus capturado por arrastreros comerciales en Brasil entre 2001-2007 según estadio de maduración sexual (definidos según Brunetti, 1990). a) machos, b) hembras.


 

Figure 8. Mantle length (ML) cumulative frequeney distribution of mature males (a) and females (b) Argentine squid Illex argentinus caught by commercial trawlers off Brazil between 2001 and 2007 (dark blue symbols). ML-at-maturity of two modal classes are indicated for both sexes as calculated after the probit transformation of frequencies (light blue symbols).

Figura 8. Distribución acumulada de tallas (largo de manto ML en mm) de machos (a) y hembras (b) sexual-mente maduras del calamar argentino Illex argentinus capturado por arrastreros comerciales en Brasil entre 2001 y 2007 (puntos azules oscuros). ML del inicio de la maduración sexual de las dos clases modales están indicados para los dos sexos según estimados por la transformación probit de frecuencias (puntos azules claros).

The overall maturity condition of the squid in the catches oscillated in space and time (Fig. 9). The GSI variability in males and females indicated that gonads and accessory organs tended to be relatively larger in the second half of the year in both central and northern latitudinal strata. In the southern areas, however, they enlarged earlier, reaching a máximum in autumn. A similar pattern was also revealed by the Hayashiindex, which expresses the advanced maturity condition when values are low (Table 2, Fig. 9).


Figure 9. Seasonal and latitudinal variability of maturity indices of the Argentine shortfin squid Illex argentinus caught by commercial trawlers off Brazil between 2001 and 2003. Symbols represent median values and vertical bars represent standard errors. a and c, males; b and d, females.

Figura 9. Variabilidad temporal y latitudinal dos los índices de madurez sexual del calamar argentino Illex argentinus capturado por arrastreros comerciales en Brasil entre 2001 y 2003. Símbolos representan valores medianos y líneas verticales representan error estándar, a y c, machos; b y d, hembras.

Sex ratio and mating activity

Overall catches during the 2001-2003 period were slightly but significantly biased towards males (male/female ratio = 1.1; p = 0.001) (Table 3). Season, latitudinal, and depth strata, however, significantly affected this general pattern, particularly as females tended to outnumber males in winter months, both in shallow areas (< 250 m) and along the central latitudinal stratum (Table 3). A contrasting scenario characterized the 2006-2007 samples: females dominated all spatial and temporal situations except in the northern areas (Table 3).


Table 3. Sex ratio of the Argentine shortfin squid Illex argentinus in commercial trawl catches off Brazil in two periods: 2001-2003 and 2006-2007. M/F: male/ female ratio, p: probability (Π2). Values in bold correspond to probabilities obtained by contingency table analysis to compare the effects of trimesters, depth, and latitudinal strata on the sex-ratio.

Table 3. Proporción de sexos del calamar argentino Illex argentinus en capturas de la pesca comercial de arrastre en Brasil en dos periodos: 2001-2003 y 2006-2007. M/F: fracción número de machos / número de hembras; p: probabilidad (Π2). Valores en negrita corresponden a probabilidades resultantes del análisis de la tabla de contingencia para comparar los efectos de trimestres, estratos batimétricos y estratos latitudinales sobre la proporción sexual.

Spermatophore production and storage increased in stage IV males and peaked in fully mature males (stage V) (Table 2). Mating activity was evidenced in the subsequent maturity stages by a sharp decrease in the presence of spermatophores in the Needhan's sac. Similarly, mated females (evidenced by the presence of spermatophores inside the mantle) were generally scarce in the catches obtained between 2001-2003 period (not mated/ mated female ratio = 1.8) (Table 4) except in winter months and > 400 m depths between 25°-29°S , where the opposite pattern was observed. On the other hand, mated females largely dominated landings in 2006-2007 (Table 4).


Table 4. Evidence of mating in female Argentine shortfin squid Illex argentinus caught in commercial trawl catches off Brazil in two periods: 2001-2003 and 2006-2007. N/M: not mated/mated female fraction, p-values correspond to prob-abilities obtained by contingency table Π2 analysis to compare the effects of trimesters, depth, and latitudinal strata on the mated condition of females.

Tabla 4. Evidencias de cópula en hembras de calamar argentino Illex argentinus capturado por la pesca comercial de arrastre en Brasil en dos periodos: 2001-2003 y 2006-2007. N/M: fracción no-copuladas/copuladas. P: probabilidades resultantes del análisis Π2 para comparar los efectos de trimestres, estratos batimétncos y estratos latitudinales sobre la actividad de cópula de las hembras.

Stock differentiation

The association among squids caught by trawlers between 2001-2003 was analyzed from the scores produced by the first three PCA extracted factors (axes) that, together, explained 63% and 72% of the total variance in males and females (Table 5). In males, factor 1 was defined mainly by geographical variables (lat, long) and squid size (BW) (higher positive and negative weights, respectively). Consequently, in the graphic representation (Fig. 10), large mature males caught at southwesterly sites should be plotted on the left hemiplane, whereas small mature squid caught at northeasterly sites should appear in the right hemiplane. Depth and maturity condition, as expressed by the Hayashi índex (HI), were particularly important in factor 2 (Table 5); males caught in deep areas with enlarged accessory reproductive organs (i.e. Needham's sac loaded with spermatophores) should be plotted on the left hemiplane and small mature males caught in shallower areas on the right one (Fig. 10). Factor 3 was highly influenced by seasonality, being mostly defined by the day-of-the-year (DYR) (Table 5); squid caught in spring and summer should be plotted in the extremes of the upper and lower hemiplanes, respectively, whereas autumn-winter squids should appear near the center of the axis (Fig. 10). A similar spatial scenario resulted from the three factors obtained with female variables except that factor 2 was also highly influenced by maturity indices (GSI and NGI) and high loads for the depth (DEPTH) variable were placed in factor 3 (Table 5).


Table 5. Principal Component Analysis employed to differentiate Argentine shortfin squid Illex argentinus stocks within the catches obtained by commercial trawlers off Brazil between 2001 and 2003. Variables included were: day-of-the-year (DYR), decimal latitude (LAT), decimal longitude (LONG), depth (DEPTH), body wet weight (BW), gonadosomatic index (GSI), Hayashi índex (HI), Nidamental gland/ Testis índex. The linear coefficients of the variables (loadings) in the first three factors rotated by the PCA are indicated for males and females. The eigenvalues and the variance explained by each factor are indicated in the last three rows.

Tabla 5. Análisis de Componentes Principales aplicada en la diferenciación de los stocks de calamar argentino Illex argentinus en las capturas de arrastreros comerciales en Brasil entre 2001 y 2003. Las variables incluidas fueron: día-del-año (DYR), latitud decimal (LAT), longitud decimal (LONG), profundidad (DEPTH), peso húmedo del cuerpo (BW), índice gonadosomático (GSI), índice de Hayashi (HI), índice de la glándula nidamental/ testículo. Los coeficientes lineales de las variables (pesos) en los tres primeros factores rotacionados por el PCA se indican para machos y hembras. Los valores propios y la varianza explicada por cada factor se indican en las últimas tres líneas.


 

Figure 10. Spatial representation of males (a) and females (b) of the Argentine shortfin squid Illex argentinus caught by commercial trawlers off Brazil between 2001 and 2003 according to the values generated by the first three factors obtained with Principal Component Analysis. The green line indicates small-sized mature squid caught all year round on the upper slope. The red line indicates large-sized mature squid caught in winter at depths over 400 m.

Figura 10. Representación espacial de machos (a) y hembras (b) de calamar argentino Illex argentinus capturado por arrastreros comerciales en Brasil entre 2001 y 2003 según los valores generados por los tres primeros factores obtenidos con el Análisis de Componentes Principales. La línea verde indica el grupo de calamares sexualmente maduros de pequeño tamaño capturado a lo largo del año en el talud superior. La línea roja indica el grupo de calamares sexualmente maduros de mayor tamaño capturado en los meses de invierno a profundidades mayores de 400 m.

In the spatial representation of both males and fe-males, a large group of squid corresponded to small mature animals caught throughout the year in shallower areas of the northeastern slope. In contrast, a smaller group of both sexes, detached from the former group, was composed of large mature animals caught in deep southwestern areas during a restricted period in the middle of the year (winter) (Fig. 10).

DISCUSSION

Interpreting the biological patterns of I. argentinus from commercial catches off Brazil requires the initial consideration that these patterns may combine the mixed effeets of three critical sources: (a) existing biologically distinct population units that may exhibit particular spatial/ temporal distribution patterns, (b) non-random spatial/ temporal fishing strategies that may or may not include squid as a principal target, and (c) on board discards (at least for the national trawl fleet). The two latter sources of bias limit our capacity to comprehensively address the entire population diversity of the species in Brazilian waters. On the other hand, it is possible to conclude, by confronting biological patterns of the catches with synoptic descriptions of the Illex population structure as produced by preceding trawl surveys (Haimovici & Pérez, 1990, 1991; Santos & Haimovici, 1997), that different spawning groups can be identified in the commercial catches and, more importantly, that the availability/vulnerability of these groups and their specific biological features may have influenced the trawl fishing patterns on the slope off southern Brazil (Pérez & Pezzuto, 2006; Pérez et al., 2009b).

Samples of commercial catches obtained between 2001-2003 contained immature and maturing squid throughout the year, as well as at least two distinguishable fully mature-spawning groups. The first group, composed of small-sized males and females, was present during all seasons on the shelf-break/ upper slope (< 400 m). In winter-spring, however, a distinctive group of large squid dominated the catches in southern (south of 28°S ) and deep fishing grounds (400-700 m). Both groups had been previously identified in trawl surveys off southern Brazil, the latter being specifically referred to as the southern Brazil stock (SBS) (Haimovici et al., 1998). In the present study, this group was shown to sustain the exceptionally large catches obtained by the chartered trawler "In Sung 270" in September 2001 and also the winter catches produced by national trawlers, mostly from 2003 onwards (Pérez & Pezzuto, 2006; Pérez et al., 2009b). Unlike the upper slope concentrations of small squid, it seems evident that these large individuals, seasonally available in dense concentrations on the lower slope, attracted the attention of the fishing industry and became valued targets of the developing multispecies deep-water trawl fishery off southern Brazil (Pérez & Pezzuto, 2006; Pérez et al., 2009b). A relevant issue regarding this pattern, however, has been the fact that SBS squid could actually be connected to the Patagonian shelf stocks through spawning migrations and paralarval transport, as described for other ommastrephid species elsewhere (Hatanaka et al., 1985). If confirmed, this hypothesis would directly characterize a shared stock scenario with important implications for management in Argentina, Uruguay, and Brazil (Haimovici et al., 2007).

Population connections between I. argentinus oc-curring in the SW Atlantic were formerly addressed by Brunetti (1988), who defined three major stocks occurring off the coast of Argentina and Uruguay (SSS, SPS, and BNS) and concluded that squid distributed along southern Brazil were an extensión of the northernmost stock (BNS). Because partly spawned or spent squid were never observed in BNS catches, the spawning location remained uncertain but was speculated to occur between July and September somewhere offshore, north of 38°S , under the Falkland (Malvinas) or Brazil Currents. Santos & Haimovici (1997) analyzed reproductive patterns of the previously considered SBS members and also concluded that these squid were, in fact, members of BNS, but proposed alternatively that southern Brazil was their major winter-spring spawning ground. Tak-ing into consideration records of elevated concentr-tions of I. argentinus paralarvae under the core of the Brazil Current (Haimovici et al., 1995) and other evidence derived from trophic relations, parasites, and body proportions (Santos, 1992), Santos & Haimovici (1997) further postulated that maturing BNS squid would migrate in early winter from northern Argentina to southern Brazil slope waters, where spawning would take place under the warm Brazil Current. During spring-summer, as the Subtropical Convergence retracted, egg masses and paralarvae would be trans-ported southwards, allowing recruitment to occur on the southern feeding grounds off northern Argentina (Haimovici et al., 1998). Whereas this hypothesis still requires corroboration through high-resolution methods such as tagging experiments or genetic markers, the biological data from commercial catches off southern Brazil may provide further indirect evidence in its support.

Initially, the sizes of mature squid present in winter catches off Brazil resembled those reported for members of both BNS and SBS, although precise comparisons were not possible because the different studies included different maturity stages for estimating size-at-maturity. Nonetheless, mantle lengths of males and females of these groups were noticeably larger than those estimated for a presumably "local" upper -slope stock, suggesting that these squid were, in fact, biologically distinct (Table 6). Schwarz & Pérez (2007) analyzed the morphology and morphometry of stato-liths extracted from squid caught by commercial trawlers off Brazil and reached similar conclusions.


Table 6. Summary of characteristics of two stocks of the Argentine shortfin squid Illex argentinus in waters of the northern Patagonian shelf (BNS) and southern Brazil (SBS) in comparison with spawning groups differentiated in the commercial trawl catches off southern Brazil between 2001 and 2007. Sizes at maturity refer to modal mantle lengths of males and females in different maturity stages (between parentheses) as defined by Brunetti (1990).

Tabla 6. Resumen de las características de dos stocks de calamar argentino Illex argentinus en el norte de la plataforma patagónica (BNS) y el sur de Brasil (SBS) en comparación con los grupos desovantes diferenciados en las capturas comerciales de pesca de arrastre en el sur de Brasil entre 2001 y 2007. La talla de madurez sexual corresponde a la longitud modal del manto de machos y hembras en diferentes estadios de madurez (entre paréntesis) definidos por Brunetti (1990).

Secondly, the majority of the squid present in the winter catches off Brazil were mated females in a spawning-spent condition, indicating that fishing was concentrated on a spawning event that could be related to a) the spawning seasons proposed for BNS and SBS and b) the spawning grounds proposed for the latter, namely the slope área between 27°S and 34°S (Bru-netti, 1988; Santos & Haimovici, 1997) (Table 6). Within these grounds, commercial catches further revealed that large spawning squid concentrated in high densities during the day on the deep slope (400-700 m). This pattern was also observed by both fishing and acoustic surveys conducted between 2001 and 2002, which further associated spawning squid con-centrations with temperature ranges between T and 13°C (Madureira et al., 2005; Haimovici et al., 2008). The deep, cold environment off southern Brazil is generally associated with the influence of South Atlantic Central Water (SACW), which flows south-wards over the slope as a deep layer of the Brazil Current (Castro et al., 2006). Temperature and salinity within this water mass range from 6-20°C and 34.6-36.0, respectively, characterizing a considerably colder, less saline environment than that of the over-laying Tropical Water, which is also transported, although superficially, by the Brazil Current. Considering that (a) spawning squid from the Patagonian shelf may require an optimal thermal environment ranging from 4o to 13°C (Brunetti et al., 1998) and (b) that pre-reproductive BNS members at the Argentine-Uruguayan Common Fishing Zone (34°00'- 39°30'S) were shown to concéntrate in subantarctic waters between 4-10°C (Bazzino et al., 2005), it seems reasonable that a spawning migration towards Brazilian waters (Santos & Haimovici, 1997) would take place in association with deep water masses such as SACW. A final element in support of a connection between Brazilian and Patagonian squid stocks can be drawn from the combination of the commercial valué of "big squid", the opportunistic behavior of the trawl fishery, and the general evolutionary population strategies of ommastrephid squids (O'Dor, 1992). These squids normally exhibit complex population structures in association with geostrophic currents, protracted spawning, and latitudinal migrations as a strategy to spread - over space and time - the risks of their short, semelparous life cycle (O'Dor, 1998). Because cold, nutrient-enriched températe waters tend to delay maturity and enhance survivorship of juvenile squid, stocks whose offspring drift, carried by geostrophic currents, to these waters attain larger sizes, are more abundant, and sustain larger fisheries (e.g. I. illecen-brosus, O'Dor & Coelho, 1993; Pérez & O'Dor, 1998). Although these squid need to perform long migrations, their large body size favors swimming long distances (O'Dor, 1988). In contrast, those stocks that remain in food-poorer, warmer, tropical and sub-tropical waters tend to grow fast but also to mature early at smaller sizes (O'Dor & Coelho, 1993). In a less productive environment, these squids are also less abundant and sustain significantly lower annual landings.

By experiencing their early life in a highly productive and cold environment such as the Patagonian Shelf, BNS squid would tend to be abundant (actually sustaining large catches in the northern Patagonian Shelf) and to mature late in life at large sizes, fit for a ~2,000-km-long winter spawning migration towards Brazilian waters. Because these are cold-water squid, they would tend to reach the deep layers of the slope as they approach southern Brazil, concentrating within the 300-400-m-high SACW layer (Madureira et al., 2005; Castro et al., 2006) and, henee, becoming vulnerable to the slope trawling in winter and early-spring. Off southern Brazil during this period of the year, winter spawners should be markedly distinct from the "local" spawners, both by their larger body size and their deeper bathymetric distribution, attracting the attention first of the highly efficient and ex-ploratory foreign chartered trawlers (Pérez et al., 2009b) and later the more conservative but overcapitalized national trawl fleet (Pérez & Pezzuto, 2006). In 2002, trawler skippers persistently tried to convince fishing biologists involved with this study that their large catches off Brazil were, in fact, a different squid species due to their obviously different body proportions and suggested that it be given a new ñame as a marketing strategy (Pérez pers. observ.). Albeit anecdotal, this fact highlights the effect of the diversity of this species population (and particular biological attributes) on the observed exploitation patterns in the SW Atlantic, reinforcing the need to consider multinational, shared stock management strategies in the region. Other shellfish and finfish resources exploited in the deep waters off southern Brazil (e.g. deep-water crabs, hake, and others) seem to justify the same strategies (Pérez et al., 2009a).

ACKNOWLEDGEMENTS

The authors are indebted to all observers, captains, and crews that allowed this large body of data to be collected during their commercial operations off southern Brazil. We also thank Rodrigo Sant'Ana for invaluable help with figures. Funding for this study was provided by the Special Secretariat for Aquaculture and Fisheries (SEAP/PR/027/2007) and the National Council for Scientific and Technological Development (CNPq) research grant (Process 306184/2007-9).

 

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Received: 23 March 2009; Accepted: 31 August 2009