...(Thunnus albacares) mtDNA analysis. Ichthyoplankton data from bongo and Tucker trawl tows were used to examine the potential prey abundance in relation to the mean size-at-age and growth rates of the yellowfin tuna larvae and their otoliths. The most rapid growth rates occurred during June 1990 when plankton volumes were at their highest levels. The lowest plankton volumes coincided with the lowest growth rates and mean sizes-at-age during the August-September 1991 period. High densities of larval fish were prevalent in the ichthyoplankton tows during the 1991 period; therefore intra- and interspecific competition for limited food resources may have been the cause of slower growth (density-dependent growth) in yellowfin tuna larvae The highest mean sea-surface temperature and the lowest mean wind stress occurred during an El Nino-Southern Oscillation (ENSO) event during the 1997 period. There appeared to be no clear association between these environmental factors and larval growth rates, but the higher temperatures may have caused an increase in the short-term growth of otoliths in relation to larval fish size.

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Yellowfin tuna (Thunnus albacares) larvae inhabit the mixed layer of all tropical and subtropical oceans of the world (Ueyanagi, 1969; Nishikawa et al., 1985). When recruited to the commercial fishery, yellowfin tuna are one of the most important tuna species worldwide (Collette and Nauen, 1983; FAO, 2004). Near-daily spawning of yellowfin tuna, and the subsequent dispersal of fertilized eggs, appears to be largely dependent on the occurrence of surface water temperatures equal to or greater than 24[degrees]C (Schaefer, 1998). In the eastern Pacific Ocean (EPO), yellowfin tuna spawn continuously between 0[degrees] and 20[degrees]N (Schaefer, 2001). Despite widespread spawning of yellowfin tuna throughout the EPO, the larvae are patchy in distribution (Ahlstrom, 1971), and relatively large numbers have been collected only near islands (Graves et al., 1988; this study) and near shore (Gonzalez Armas, 2002).

The larvae of Thunnus are difficult to identify by meristic, morphological, or pigmentation characteristics (Matsumoto et al., 1972; Potthoff, 1974; Richards et al., 1990; Lang et al., 1994). In the EPO, the late-larval and early-juvenile stages of yellowfin and bigeye (T. obesus) tuna co-exist and cannot be differentiated by these conventional methods. However, allozyme (Graves, et al., 1988) and recent molecular (Takeyama et al., 2001; Chow et al., 2003) analyses have made it feasible to identify larvae of these two species that inhabit the EPO.

The growth dynamics of yellowfin tuna during early life stages may have a profound effect on cohort strength (Houde, 1987), but growth rates have not been described for the larvae in the Pacific Ocean. Larval and juvenile stage durations and corresponding growth rates (Houde, 1989), starvation rates (Margulies, 1993), and larval transport and predation (Grimes, 2001) may be strongly influenced by biological and physical processes that would affect pre-recruit survival in yellowfin tuna. Standing stocks of phytoplankton and zooplankton in the EPO, where yellowfin tuna larvae are found are seasonally variable (Blackburn et al., 1970; Owen and Zeitschel, 1970; Lauth and Olson, 1996; Gonzalez Armas, 2002) and influenced by interannual events such as El Nino-Southern Oscillation (ENSO) conditions (Dessier and Donguy, 1987; Fiedler, 1992; Chavez et al., 1999; Strutton and Chavez, 2000). In the northwestern Panama Bight of the EPO, nearshore ichthyoplankton surveys (from 1989 to 1993) (IATTC (1); IATTC (2); Lauth and Olson, 1996; Owen (3)) and experiments with captured scombrid larvae (from 1986 to 1997) at the Achotines Laboratory of the Inter-American Tropical Tuna Commission (IATTC) (Olson and Scholey, 1990; Margulies, 1993; Scholey, 1993; Wexler, 1993) have provided an opportunity to explore factors controlling prerecruit growth and survival of scombrids. These small- and fine-scale studies may provide some understanding of the recruitment variability of yellowfin tuna in the Panama Bight, considering that yellowfin tuna exhibit limited, small-scale movements within the EPO (Schaefer, 1991; Wild, 1994) and that processes important to recruitment probably occur at small scales (Fortier and Leggett, 1985).

The Panama Bight is characterized by distinct seasonal and interannual variations in atmospheric and oceanic conditions (Wooster, 1959; Smayda, 1963, 1966; Forsbergh, 1963, 1969). The climatological and physical oceanographic properties that occur within the Panama Bight are determined by the north-south seasonal movement of the northeast trade winds of the Atlantic Ocean, the equatorial calm belt (i.e., the doldrums), the southeast trade winds of the Pacific Ocean, and the convergence of these trade wind systems within the doldrums (i.e., the intertropical convergence zone, ITCZ) (Smayda, 1966). From January through April, the ITCZ is displaced to the south and strong northerly trade winds create a dry season and produce local upwelling. From about May through December, the ITCZ is displaced to the north and the Panama Bight is dominated by southeast trade winds and a rainy season characterized by reduced upwelling, higher sea-surface temperatures (SSTs), lower ocean salinities, and a deeper thermocline and mixed layer (Lauth and Olson, 1996). The growth and subsequent survival of yellowfin tuna larvae that occur during the reduced upwelling season may be regulated more by the spatial patchiness of prey organisms coincident with lower plankton volumes (Owen, 1989). ENSO events could further affect the seasonal availability of nutrients and food organisms during this period (Barber and Chavez, 1986; Dessier and Donguy, 1987; Fiedler, 1992; Chavez et al., 1999). A mild ENSO event occurred during our sampling periods in 1991-92 (Barber et al., 1996) and a strong event occurred in late 1997 (Chavez et al., 1999; Strutton and Chavez, 2000; Glynn et al., 2001).

The objectives of this study were 1) to identify the species of Thunnus sampled in the northwestern Panama Bight by molecular analysis, 2) to determine ages and compare the size-at-age data of yellowfin tuna larvae collected during the periods of reduced upwelling of 1990, 1991, 1992, and 1997, and 3) to explore relationships between the temporal variation in growth rates and measured levels of plankton and physical processes in the Panama Bight.

Materials and methods

Larval fish collections

Fish larvae were collected in the northwestern Panama Bight (Fig. 1) during the seasons of reduced upwelling in June 1990, July and September 1991, June and July 1992, and August 1997 (Table 1). Most of the larvae were collected with a dipnet just below the ocean surface after they were attracted with an underwater light at night (night-lighting, NL) (Olson and Scholey, 1990) near Frailes del Sur in the vicinity of the 100- and 200-meter isobaths. Larvae were also collected in this area in July 1991 by a light trap (LT) (design described in Thorrold, 1993) deployed near the surface. All larvae were fixed in 95% ethyl alcohol shortly after capture, except for some that were caught alive and used in laboratory experiments. Fish used in laboratory experiments were not used for the age and growth analyses. SSTs were recorded with a bucket thermometer, and the salinity of a sample of water taken just below the surface was measured with a handheld salinometer. Visual observations of environmental conditions (e.g., wind, currents, and weather) were recorded at the time of sampling.

[FIGURE 1 OMITTED]

Laboratory procedures and analyses

Larvae of the genus Thunnus were sorted from other scombrid larvae by the morphological features and meristics described in Nishikawa and Rimmer (1987) and Ambrose (1996). The standard length (SL) of each larva was measured in distilled water before the sagittal otoliths were removed for aging and before the remaining tissue of each individual was placed in 95% ethyl alcohol for species identification. The sagittae were removed, cleaned of tissue with chlorine bleach, rinsed in distilled water, dried, and embedded distal side up with Eukitt (O. Kindler, Freiberg, Germany) mounting medium on a glass slide. The diameter along the longest axis of each sagitta was measured with an ocular micrometer and light microscope. The sagittae were polished at the surface until the increments were clearly visible with transmitted light at a magnification of 480 or 720x. Daily increments (previously validated in Wexler et al., 2001) of the left and right sagittae were counted "blindly" (i.e., repeated counts were made without prior knowledge of the previous counts) by the first author until the same number of increments were counted at least three times in one of the sagittae. The number of increments in the sagitta that was more clearly read (which usually resulted in a higher count) was used as a direct estimate of age for that fish.

The temporal variation in growth was examined by comparing the size-at-age data of the larvae and their otoliths among collection periods through analysis of covariance (ANCOVA) and a multiple range comparison test (Tukey HSD) (XLSTAT vers. 7.5.2, Addinsoft USA, New York, NY) (a=0.05).

DNA analysis and species identification

The flanking region between ATPase 6 and cytochrome oxidase subunit I (COI) genes of mtDNA was amplified by using the polymerase chain reaction (PCR), and restriction fragment length polymorphism (RFLP) patterns were used to identify the species of Thunnus larvae according to protocols of Takeyama et al. (2001) and Chow et al. (2003). Albacore (T. alalunga), yellowfin, and bigeye tunas in the Pacific Ocean can be identified by the diagnostic restriction profile of Mse I digestion (Chow and Inoue, 1993), and this enzyme assay was used to identify the species of larvae collected in 1990-92. Chow et al. (2000) found, however, that many specimens of bigeye tuna in the Atlantic Ocean shared the same restriction profile with yellowfin tuna; this also occurred in the Pacific Ocean, but at a much lower frequency (1 out of 144 individuals examined). Takeyama et al. (2001) found another restriction enzyme (Tsp 5091) that was diagnostic for bigeye tuna regardless of where the specimens came from. Therefore, in addition to using Mse I digestion, Tsp 5091 was also used for all individuals collected in 1997.

Back-calculated dates

Spawning dates were back-calculated for each larva by subtracting the number of otolith increments counted from the...

NOTE: All illustrations and photos have been removed from this article.



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