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Edad y crecimiento del pez espada (Xiphias gladius Linnaeus, 1758) en el Pacifico suroriental frente a Chile (2001).

Age and growth of the swordfish (Xiphias gladius Linnaeus, 1758) in the southeastern Pacific off Chile (2001).

INTRODUCTION

The swordfish (Xiphias gladius) is a cosmopolitan species that is found from tropical to temperate waters (between 5 and 27[degrees]C). Commercial catch data indicate a latitudinal distribution that extends from 50[degrees]N to 45[degrees]S in the western Pacific and from 50[degrees]N to 35[degrees]S in the eastern Pacific (Nakamura, 1985). In Chile, swordfish are caught with small-scale drift gill nets and large-scale commercial longlines. Catches have been recorded since 1938, but fisheries did not experience significant growth until 1986. Total landings peaked in 1991, reaching 5,959 tons (Barbieri et al., 1998), and then stabilized in recent years with catches of 1,397 and 1,586 tons in 2001 and 2002, respectively (Donoso et al., 2002, 2003a).

Swordfish age and growth studies have been based mainly on two different methods: modal decomposition analysis of length frequency data and the analysis of hard parts such as otoliths, dorsal and anal fin rays, and vertebrae. These studies have been carried out in different geographic areas, including the Atlantic, the Mediterranean Sea, and the North Pacific (Yabe et al., 1959; Berkeley & Houde, 1983; Wilson & Dean, 1983; Tserpes & Tsimenides, 1995; Ehrhardt et al., 1996; Sun et al., 2002). Conversely, only one attempt has been made to estimate age and growth in the southeastern Pacific region (Donoso & Chong, 1992); this study was based on a few samples obtained at the onset of longline activities.

Assessing the growth of a species is a fundamental part of fisheries population dynamics, particularly for highly migratory species, as growth comparisons could also facilitate understanding of their life history traits. Therefore, the objective of the current study was to estimate sex-specific age and growth of swordfish by counting growth rings in cross sections of anal fin rays from the southeastern Pacific off Chile.

MATERIALS AND METHODS

Swordfish lower jaw fork length (cm), total weight (kg), and anal fin rays were sampled by sex and monthly on board longline vessels in the fishing areas of the Chilean longline fleet in 2001 (Fig. 1). A total 1,143 anal fin rays were collected and processed (511 males, 632 females). In the laboratory, anal fins ray were boiled for 5 min; the second rays were cleaned and dried at room temperature. Second anal fin rays were cross sectioned at a location equivalent to 3/4 the maximum width of the condyle base (Fig. 2). Sections approximately 1.5 mm thick were obtained using an "ISOMET" saw with diamond wafering blades. These sections were immersed in 96% alcohol for 20 min and then stored dry.

Sections were analyzed under a stereomicroscope with reflected light at a magnification of 10x or higher when needed to observe details of the type of edge. Measurements from the focus to the distal edge of the section (ray radius) and from the focus to the distal edge of each annulus were measured for each specimen using an eyepiece equipped with a graduated reticule. The criteria of Berkeley & Houde (1983) and Ehrhardt (1999) were used to identify annuli. The cross section readings were conducted deliberately without prior information of the sampled fish (i.e., length, weight, date of capture). Ageing bias and band count precision between readers were assessed using age-bias plots and the coefficient of variation (Campana, 2001) and average percent error (IAPE, Beamish & Fournier, 1981).

Two methods were used to evaluate the annual periodicity in the formation of ray growth bands in swordfish. The first method considered the monthly proportion in the type of band (opaque, translucent) present on the edge of each cross section. 2) For the second method, the marginal increment ratio (MIR) was also estimated for each specimen using the following formula (Sun et al., 2002):

MIR = (S - [S.sub.n])/([S.sub.n] - [S.sub.n-1])

where S: distance from the section ray focus to the edge,

[S.sub.n] and [S.sub.n-1]: distance from ray focus to bands n and n-1, respectively.

Due to a lack of small-sized swordfish (age 0-1+ year old), a back-calculation procedure was used. The relationship between the ray radius and the length of the fish (LJFL) was nonlinear; therefore, the proportional method described by Bagenal & Tesch (1978 fide Francis, 1990) was used as follows:

[L.sub.n] = [([S.sub.n]/S).sup.b]L

where L: LJFL at the time of capture

[L.sub.n]: LJFL when band n was formed

b: exponent of the nonlinear regression of fish length on ray radius at capture.

[FIGURE 1 OMITTED]

The back-calculated length-at-age data were then fitted to the Von Bertalanffy equation in its standard (Ehrhardt et al., 1996; Sun et al., 2002) and generalized (Richards, 1959) forms, according to the following equations:

Standard:

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]

Generalized:

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]

where: [L.sub.t] : mean lower jaw fork length at age t

[L.sub.[infinity]] : asymptotic length or the mean maximum length of the fish

[t.sub.0] : hypothetical age at length zero

K : growth coefficient VB standard equation

k : growth coefficient VB generalized equation

m : fitted fourth growth-function parameter.

[FIGURE 2 OMITTED]

The standard and generalized Von Bertalanffy growth parameters for males, females, and combined sexes were estimated using a nonlinear least square procedure, through a Gauss-Newton algorithm (SYSTAT 7.0, Systat Software Inc., SSI). To test for significant differences in growth between males and females, Hotelling's [T.sup.2] multivariate statistical procedure was used (Bernard, 1981; Cerrato, 1990).

In order to assess the growth model that best fits the swordfish data, goodness-of-fit (coefficients of determination, ([r.sup.2]), sum of residual squares (SSR), and standard error (SE) were considered. Akaike Information Criterion statistics (AIC, Akaike, 1973) were examined. The AIC is described by the following equation:

AIC = -2 log (L)+2 p

where, L : residual sum of squares at the maximum goodness-of-fit and p = the number of free parameters in the model.

RESULTS

The length frequency distributions of sampled fish ranged from 100 to 265 cm for males and from 116 to 289 cm for females (Fig. 3). The relationships between LJFL and total weight for males, females, and combined sexes were described by these equations: males, TW = 4.5 x [10.sup.-6] [LJFL.sup.3.21] ([r.sup.2] = 0.97, n = 541); females, TW = 3.7 x [10.sup.-6] [LJFL.sup.3.26] ([r.sup.2] = 0.96, n = 452), and both sexes combined, TW = 4.1x[10.sup.-6] [LJFL.sup.3.24] ([r.sup.2] = 0.97, n = 993) (Fig. 4). The ANCOVA of log-transformed LJFL and weight did not show significant differences in either slope (P value = 0.55) or intercepts (P value = 0.59) between males and females. However, the females become heavier than males when larger than 200 cm LJFL. Another ANCOVA indicated no significant differences in the relationship between males and females for lengths larger than or equal to 200 cm LJFL (slope; P > 0.36).

[FIGURE 3 OMITTED]

From the 1,235 ray samples, 511 males and 632 females were successfully aged; 92 (7%) fin rays were unreadable. The comparison of counts between two readers indicated no appreciable bias (Fig. 5). The IAPE and CV were 7.0 and 9.9, respectively. An analysis of same reader performance at different times showed even more precision (IAPE and CV equal at 5.17 and 7.31, respectively).

Monthly rates of translucent edge formation showed a distinctive seasonal pattern with higher values in summer months for both sexes (Fig. 6a). This pattern indicated the formation of one growth ring per year during the December-March period (Fig. 6a). The MIR also showed a trend, with higher relative values in winter. This trend is indicative of the formation of one translucent growth ring (annulus) from October to March, although it is not completely conclusive due to the absence of significant differences over months (Fig. 6b).

The relationship between LJFL and ray radius was fitted using a non-linear procedure, producing the following parameter estimates: for males, a = 87.26, b = 0.457, [r.sup.2] = 0.80, and n = 503 and, for females, a = 79.44, b = 0.522, [r.sup.2] = 0.84, and n = 630. Logtransformed LJFL and ray radius showed significant differences in the relationship between males and females in slope and intercept (ANCOVA; P value < 0.00012).

[FIGURE 4 OMITTED]

Growth parameter estimates for the standard and generalized Von Bertalanffy models are provided in Table 1. The findings between sexes for both standard and generalized models differed significantly (Fig. 7); the standard VB model shows greater sexual dimorphism in growth (Table 2). The curves of the size-atage von Bertalanffy model fits are shown for different regions in Figure 8.

[FIGURE 5 OMITTED]

Comparisons between the standard and generalized growth models showed equal [R.sup.2] and similar SSR. Nevertheless, the standard Von Bertalanffy model showed a lower AIC (2 points) for males and females than did the generalized Von Bertalanffy model. According to significant criteria for comparing AIC values (Sakamoto et al., 1986), this result is enough to conclude that the standard model is more appropriate for representing swordfish growth in the southeastern Pacific off Chile (Table 3).

Table 4 shows mean size-at-age estimated by back-calculating and the standard and generalized von Bertalanffy models.

DISCUSSION

As Berkeley & Houde (1983) mentioned in an early study, the main problems with ageing swordfish are the missing first band in large specimens and the presence of multiple bands or false rings. Other authors have confirmed those observations (Tsimenides & Tserpes, 1989; Tserpes & Tsimenides, 1995; Ehrhardt et al., 1996). However, the problem of multiple bands can be overcome by experienced readers, and the problem of the missing band in some large fish can be solved by estimating its position at a distance that is comparable to its position in small specimens (Ehrhardt, 1999).

[FIGURE 6 OMITTED]

Precision in age estimation was evaluated for different readers, and both IAPE and bias statistics indicated acceptable indices of precision. Furthermore, the precision indices obtained here (IAPE 7.0 and CV 9.9) agree with the information provided by the European Fish Ageing Network (EFAN). In addition, in a recent initiative, no significant differences were reported in age estimations of swordfish between the NMFS Honolulu Laboratory, CICESE laboratory (Mexico), NRIFSF laboratory (Japan), and IFOP (Chile) (De Martini, unpublished). All this evidence suggests that the age estimates in the current study were reliable.

The analysis of the distribution of the monthly proportion of edge types indicated the formation of an annual translucent ring between December and March with a maximum in January and February. The translucent ring deposition coincides with the spawning season of the swordfish in the southeastern Pacific (Donoso et al., 2003b). This could be because, when spawning, fish use more energy to produce gametes than for growth, resulting in a less calcified ring. Alternatively, deposition of the translucent zone over summer could also be related to swordfish migration to reproductive areas as suggested by Berkeley & Houde (1983), Tserpe & Tsimenides (1995), and Sun et al. (2002). The current study provides the first evidence that an annual growth ring formation occurs in the swordfish of the southeastern Pacific. Further studies using techniques such as tag-recapture and oxytetracycline tagging (Campana, 2001; Sun et al., 2002) are needed to validate this evidence.

Swordfish growth did not differ between the estimates made by the standard and generalized Von Bertalanffy equations for males and females. Such results show both equations provide similar explanations for the age-size relationship of fish between the ages of zero and seven years. However, estimates from the generalized equation showed a higher [L.sub.[infinity]] in males than in females, which differs from previous studies with higher growth in females (Berkeley & Houde, 1983; Ehrhardt, 1992; Tserpes & Tsimenides, 1995; Ehrhardt et al., 1996; Sun et al., 2002). If both equations are compared using AIC, the standard equation is the most appropriate according to Sakamoto et al. (1986), because two points of difference in the AIC are enough to conclude that the model is correct. In addition, the incorporation of a fourth parameter in the generalized Von Bertalanffy equation did not provide a better fit to the age-size relationship, which, biologically, is meaningless (Ehrhardt, 1992). The generalized VBGF would be appropriate for describing swordfish size-at-age only if there was a compelling reason to fit the growth curve through zero length at zero age (De Martini et al., 2007). Consequently, the standard Von Bertalanffy growth equation seems to be more appropriate, statistically and biologically, to represent the growth of the swordfish in the southeastern Pacific off Chile.

A comparison of the growth in males and females revealed significant differences that were more marked in the standard growth equation. In general, females grew more quickly than males during their second year, reaching larger sizes than males. This response has also been observed in other regions (Tserpes & Tsimenides, 1995; Ehrhardt et al., 1996; Sun et al., 2002, De Martini et al., 2007). When comparing overall growth curves of swordfish, we found lower growth rates and lower [L.sub.[infinity]] in the current study than those recorded for the North Atlantic (Berkeley & Houde, 1983; Ehrhardt, 1992; Ehrhardt et al., 1996), the Mediterranean (Tsimenides & Tserpes, 1989; Tserpes & Tsimenides, 1995), and the northwestern Pacific (Sun et al., 2002). In general, the Chilean fisheries were aged as younger at given body lengths than in other studies.

Differences in mean size-at-age observed in the Atlantic, Pacific, and Mediterranean regions could be due to variations in growth patterns, given that these regions have been identified as different population units based on genetic studies. Chow et al. (1997) proposed that at least four large stocks exist: North Atlantic, South Atlantic, Mediterranean, and Indo Pacific. In the Pacific, although the differences seem to be less marked, the population is not homogeneous (Rosel & Block, 1996; Chow, 1998; Ward et al., 2001). According to Reeb et al. (2000), the north and south populations of the western Pacific appear to diverge although, in the eastern Pacific, the populations seem to be interconnected by a corridor along the equator. Galleguillos et al. (2001) also proposes two population groups: one formed by genetically similar fish corresponding to Chile, Ecuador, and Mexico, which is assumed to include fish from Peru and Colombia as well, and another in the area of Hawaii and Australia, which differs significantly from the first group.

Growth rate differences were observed among the northwestern Pacific (Taiwan) (Sun et al., 2002), southwestern Pacific (Australia) (Young et al., 2004), and southeastern Pacific (Chile). The swordfish caught in the southeastern Pacific (Chile) grow in length faster than those caught in the northwestern Pacific (Taiwan) and southwestern Pacific (Australia). On the other hand, the growth rate of Chilean swordfish is similar to the swordfish caught in the central North Pacific (Hawaii). For example, the mean length at age 1 of swordfish in the Hawaii fishery is about 99 cm eye-fork length (EFL), which is equivalent to 114 cm LJFL (De Martini et al., 2007), whereas the mean length at age 1 of swordfish in the Chilean fishery is 118 for females and 119 for males cm LJFL. This was confirmed by readers from other laboratories during the inter-laboratory exercise (De Martini et al., 2007).

This faster growth in the southeastern Pacific (Chile) and North Pacific (Hawaii) suggests similar environmental conditions reflected in the high productivity of Humboldt Current ecosystem and Subtropical Convergence Zone. Although the genetic evidence shows that different populations could exist in the northwestern (Japan, Taiwan), southwestern (Australia), and southeastern Pacific (Chile, Peru, Mexico) (Reed et al., 2000), no genetic similarity has been established between the southeastern and central North Pacific. Chow et al. (1997) stated that the degree of differentiation between the swordfish population units in the Pacific is very low due to the short divergence time. In this context, the life history information for different regions, e.g. the variations in growth rates (Sun et al., 2002; Young et al., 2004; De Martini et al., 2007, this study), spawning season and area (De Martini, et al., 2000; Donoso et al., 2003b), and stock structure with an environmental mark (Humphreys et al., 2005) are important for stock assessment and identification because these differences in life history may result from different adaptive responses, such as those observed among the Atlantic, Mediterranean, and Pacific populations.

[FIGURE 7 OMITTED]

CONCLUSIONS

The standard Von Bertalanffy growth equation seems to be more appropriate for modeling swordfish growth in the southeastern Pacific off Chile. This fit of growth revealed the existence of significant differences between males and females.

The southeastern Pacific swordfish stock off Chile has different growth rates than those of the Atlantic Ocean, Mediterranean Sea, northwestern Pacific (Taiwan), and southwestern Pacific (Australia). These regions show lower rates than those estimated for Chile, coinciding with the grade of differentiation between the population units of different oceans. On the other hand, the rate of growth in the central North-Pacific should be more similar to Chile's estimate (De Martini et al., 2007).

ACKNOWLEDGMENTS

The author expresses his gratitude to Patricio Barria and Miguel Donoso of the Instituto de Fomento Pesquero of Chile (IFOP), Robert Humphreys and Dr. Edward de Martini of the Honolulu Laboratory National Marine Fisheries Service (NMFS) NOAA, and Roberto Licandeo for their useful comments on earlier drafts of this paper, and two anonymous reviewers for constructive criticisms of the manuscript draft. The present research was supported by the project "Seguimiento de las Pesqueria Nacionales. Investigacion Situacion Pesqueria Recursos Altamente Migratorios" Instituto de Fomento Pesquero (IFOP) and Subsecretaria de Pesca (SUBPESCA), of the Chilean Government.

Received: 18 January 2007; Accepted: 26 May 2008

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Jose F. Cerna

Division de Investigacion Pesquera, Instituto de Fomento Pesquero (IFOP) Blanco 839, Valparaiso, Chile

Corresponding author: Jose F. Cerna (fcerna@ifop.cl)
Tabla 1. Parametros de crecimiento del pez espada en el Pacifico
suroriental estimados con la ecuacion de crecimiento de Von
Bertalanffy estandar y generalizada. Error estandar entre
parentesis. Von Bertalanffy growth model

Table 1. Parameter estimates of standard and generalized Von
Bertalanffy growth models for swordfish in the southeastern Pacific
off Chile. Standard errors in parenthesis.

                                  Standard

                                                Combined
Parameter             Male         Female         sexes

[L.sub.[infinity]]     279           321           327
                     (9.11)        (8.30)        (6.75)
K                     0.158         0.133         0.126
                    (0.0127)      (0.0075)      (0.0056)
k

[t.sub.0]             -2.65         -2.46         -2.59
                    (0.1529)      (0.0987)      (0.0790)
m

[r.sup.2]             0.85          0.89          0.89

                                 Generalized

                                                Combined
Parameter             Male         Female         sexes

[L.sub.[infinity]]     365           344           396
                    (158.47)       (39.69)       (80.94)
K

k                     0.027         0.077         0.033
                    (0.0512)      (0.0546)      (0.0292)
[t.sub.0]             -1.14         -1.81         -1.4
                    (0.7544)      (0.6815)      (0.4506)
m                    -1.023        -0.307        -0.706
                    (0.8068)      (0.3880)      (0.3606)
[r.sup.2]             0.85          0.89          0.87

Tabla 2. Resultados del test multivariado (Hotelling's
[T.sup.2]) que determina las diferencias entre sexos para los
parametros de Von Bertalanffy.

Table 2. Results of the multivariate test (Hotelling's [T.sup.2])
to determine sex specific differences between the estimated
Von Bertalanffy growth parameters.

                            Von Bertalanffy model

                           Standard   Generalizaded

[T.sup.2]                   222.48        24.95
df                           6.66         6.66
[T.sup.2.sub.(0.01, df)]    19.99         19.99

Tabla 3. Resultados del Akaike information criteria (AIC) que
determina cual es el mejor ajuste de los datas talla-edad para el
pez espada del Pacifico suroriental frente a Chile. Akaike
information criteria (AIC)

Table 3. Results of the Akaike information criteria (AIC) to
determine which model best fits the length-at-age data for
swordfish in the southeastern Pacific off Chile.

                             Male

                 Standard V-B   Generalized V-B

RSS                186,124          185,928
No. parameters           3                4
No. samples          1,421            1,421
AIC                  -4.45            -2.45

                            Female

                 Standard V-B   Generalized V-B

RSS                313,636          313,555
No. parameters           3                4
No. samples          2,171            2,171
AIC                     -6               -4

Tabla 4. Promedio de la longitud mandibula inferior horquilla por
edad (LMIH-cm) estimada por retrocalculo y a traves de la ecuacion
de Von Bertalanffy estandar y generalizada para el pez espada en el
Pacifico suroriental frente a Chile. Lower jaw fork length
estimates (cm)

Table 4. Average lower jaw fork length-at-age
(LJFL-cm) estimated by back calculation and standard and
generalized Von Bertalanffy equations for swordfish in the
southeastern Pacific off Chile.

                            Standard Von    Generalized Von
          Back-calculated   Bertalanffy     Bertalanffy
  Age
(years)   Male   Female     Male   Female   Male   Female

   1      122     117       119     118     122     118
   2      146     145       142     144     146     144
   3      164     164       161     166     165     166
   4      182     183       178     185     182     185
   5      197     202       192     202     196     202
   6      206     218       205     217     208     216
   7      217     230       215     230     220     230
   8      228     244       224     241     230     241
   9      244     252       232     251     239     252
  10              251       239     260     247     261
  11              255       244     267     255     269
  12              259       249     274     262     277
  13                        254     280     268     283
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Title Annotation:Research Article
Author:Cerna, Jose F.
Publication:Latin American Journal of Aquatic Research
Article Type:Report
Date:Mar 1, 2009
Words:4485
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