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Effects of salinity gradients on larval growth and otolith asymmetry of austral hake Merluccius australis.

The austral hake Merluccius australis (Hutton, 1872) sustain an important fishery in New Zealand, Chile and around Falkland Islands (Horn, 2015). In South America, it inhabits from 40[degrees]S (Chiloe Island) in the Pacific Ocean, southward around the southern tip, to the continental shelf north of 49[degrees]S and the slope north to 38[degrees]S in the Atlantic Ocean (Brickle et al., 2016). The main spawning area is located along the shelf-break and canyons in the northern area of Chilean Patagonia, close to Guafo and Guamblin islands (43-45[degrees]S), and spawning occurs in austral winter from July to September (Balbontin & Bravo, 1993). However, the inner seas of southern Chile are also used as secondary areas of spawning (Medina et al., 2014) and larval nursery grounds (Bustos et al., 2007, 2015). This has been recently confirmed by Brickle et al. (2016) who found a large range in Sr/Ca ratios in the otolith cores, suggesting complex salinity structuring in the austral hake spawning and/or larval grounds.

The southern Patagonia is characterized by large inputs of freshwater through river discharge and runoff in coastal marine zones, besides marine precipitation, causing salinity and density anomalies that affect the dynamics of the coastal circulation (Davila et al., 2002). The Baker and Pascua rivers are the main rivers of Chilean Patagonia, with mean annual outflows of 1133 and 753 [m.sup.3] [s.sup.-1], respectively (Meerhoff et al., 2015). Additionally, particulate organic matter inputs from the rivers to the fjord ecosystem may partially sustain pelagic food webs during periods of food limitation (Vargas et al., 2011). The salinity field distribution along the Patagonian coast may affect the dispersion (Landaeta & Castro, 2006), feeding habits (Landaeta et al., 2011) and condition (Landaeta et al., 2012; Zenteno et al., 2014) of early life stages of marine fishes.

The analysis of microstructure pattern of sagittal otoliths has proven to be a useful tool in investigating different aspects of the early life history of hakes (Palomera et al., 2005; Grote et al., 2012; Betti et al., 2014; Bustos et al., 2015). It can be used to estimate back-calculated hatch dates, growth rates at population and individual levels and developmental instability (Campana, 1990; Diaz-Gil et al., 2015). Therefore, the main goal of this research was to test the effect of freshwater discharge from Baker and Pascua rivers on larval traits of marine fish using austral hake M. australis.

Between 10 and 22 October 2014, a biooceanographic sampling was carried out along Chilean Patagonia, Southeast Pacific Ocean (Fig. 1). Samples were collected in 40 stations, where environmental data of the water column (temperature, salinity, density) were collected from 1000 m depth or 10 m above the bottom with to the surface a Seabird SBE-19 CTD profiler. Turbidity was measured with a Hach[R] 2100q portable turbidimeter from water samples taken by Niskin bottles at 0, 10, 30, 50 and 100 m depth. Ichthyoplankton samples were collected from 100 m depth or 10 m above the bottom to the surface through oblique tows with a Bongo net (60 cm diameter, 300 [micro]m mesh size) with a TSK flowmeter mounted in the frame of the net to estimate the volume of the seawater filtered. Towing speed was ~2 knots. The volume filtered in each tow (range = 272.1-1158.2 [m.sup.3] [tow.sup.-1], mean [+ or -] SD = 612.8 [+ or -] 181.6 [m.sup.3] [tow.sup.-1]) was calculated from flowmeter counts. Once over the vessel, the nets were washed and all samples were fixed in 5% formalin buffered with sodium borate. Once in the laboratory, all plankton samples were washed and preserved in 96% ethanol.

In the laboratory, larval hake Merluccius australis were identified based on descriptions of Balbontin et al. (2004) and Bustos & Landaeta (2005). Larval abundance was standardized to individuals (ind) 1000 [m.sup.-3] using the flowmeter counts for further analysis. All larvae were measured, from the tip of the premaxilla to the tip of the notochord (standard length, SL), to the nearest 0.01 mm under a stereomicroscope Olympus SZ-61 with a video camera Moticam 2500 (5.0 MPixel) connected to a PC with Moticam Image Plus 2.0 software. Later, extraction and measurement of left and right sagittal otoliths were carried out; a detailed description of the methods can be found elsewhere (Bustos et al., 2015). From the 138 larvae, undamaged otoliths of 100 individuals were available, and 88 were readable. The daily periodicity of the micro-increment deposition has not been validated for M. australis; nonetheless, it has been validated in postlarval and juvenile M. productus and M. merluccius (Bailey, 1982; Morales-Nin et al., 2005).

Estimations of the age of larval austral hake were compared among those collected over the shelf and those from channels and fjords, using a t-test, because data showed a normal distribution (Shapiro-Wilk test, W = 0.973, P = 0.063). A least-squares linear regression model was fitted to the relationship micro-increment counts (MC, days) and standard length (SL, mm), where the intercept corresponds to the larval size-at-hatch and the slope corresponds to the population larval growth rate. Residuals of the regression correspond to individual variability of the size-at-age (size-at-age residuals, SAR). Individual Growth Rates (IGR, mm [d.sup.-1]) were estimated as follows: individual size-at-hatch (SAH) was estimated using the relationship SL = 1.1183(OR)03813 (Fig. 2a), where OR is the otolith radius at hatch (i.e., hatch mark). Then, IGR was calculated as IGR = [SAC-SAH]/MC, where SAC is size-at-capture (mm, SL) and MC is micro-increment counts (days).

The sagittal otolith area was used as a trait to test fluctuating asymmetry (Diaz-Gil et al., 2015). Because the asymmetry of the trait (i.e., right, R, minus left, L, sagitta area) was positively correlated with the trait size ([R+L]/2). At the individual level (Spearman rs = 0.426; P = 5.72 x [10.sup.-5]), FA2 (R-L/([R+L]/2)) was used to test fluctuating asymmetry (normality, skewness and kurtosis), and FA6 ([absolute value of (R-L)]/([R+L]/2)) was used for further comparisons with the environmental conditions of the water column ([DELTA]temperature, [DELTA]salinity, maximum stability, maximum turbidity) derived from the CTD and turbidity data. Vertical stability was estimated using the Brunt-Vaisala frequency ([N.sup.2] = [g/[rho]]*[d[rho]/dz], where g = gravity, p = water density, and z = depth). Spearman correlation rank tests (rs) were run to test the independence of variables.

A total of 138 larval Merluccius australis, measuring between 2.77 and 6.07 mm SL (mean [+ or -] SD, 4.69 [+ or -] 0.90) were collected in larger abundance in open waters of Penas Gulf, but also along channels, fjords and zones influenced by the discharge of Baker and Pascua rivers (Chilean Patagonia), during austral spring 2014 (Fig. 1). Larval abundance ranged between 0.86 and 41.55 ind 1000 [m.sup.-3] (mean [+ or -] SD, median; 11.97 [+ or -] 14.33, 4.08 ind 1000 [m.sup.-3]).

Mean age of larvae collected in the shelf were slightly older (mean = 14.83 days) than those collected in channels and fjords (mean = 12.40 days) (t-test, t = 2.28, P = 0.024). This age difference suggests that: 1) spawning occurred in the shelf and later eggs/larvae were transported to channels and fjords, or 2) spawning occurred in both areas, but sequentially first in the shelf and then in channels. Population larval growth estimated by micro-increment counts of sagitta otoliths was 0.129 [+ or -] 0.010 mm [d.sup.-1], with age varying from 4 to 24 days old (Fig. 2b).

Estimated individual growth rates (IGR) varied from 0.111 to 0.345 mm [d.sup.-1] (0.181 [+ or -] 0.049 mm [d.sup.-1]). IGR was slightly significantly faster for those individuals collected in fjords and channels (median = 0.128 mm [d.sup.-1]) compared to those collected in shelf waters (median = 0.126 mm [d.sup.-1], Mann-Whitney test, U = 1737, P = 0.012). The fluctuating asymmetry (FA2) showed normal distribution (Kolmogorov-Smirnov test, KS = 0.091, P = 0.20, Fig. 2c), scarce positive skewness (0.337 [+ or -] 0.264) and platykurtic (kurtosis = 1.697 [+ or -] 0.522). FA2 of otolith area from larval hake collected in fjords and channels showed larger variance (i.e., more asymmetry) than those otoliths from larvae collected in shelf waters (F test, F = 2.03, P = 0.024). IGR and FA6 were not correlated (Spearman rs = 0.222; P = 0.119).

When all three indicators derived from otolith analysis (SAR, IGR, and FA6) were compared with environmental conditions of the water column (Table 1), all showed positive and significant correlations with vertical salinity gradients (Fig. 3, Table 2). IGR and FA6 were also positively correlated with the vertical stability (B-V frequency, Fig. 3, Table 2). Finally, FA6 was also positively correlated with turbidity (Table 2).

Therefore, in areas with large freshwater input from the Baker and Pascua rivers (Fig. 1), larval hakes were less abundant, but larger-at-age showed faster growth rates and were more asymmetrical than those individuals collected in the open sea and along channels of Chilean Patagonia. This bio-physical interaction seems to be species-specific; freshwater runoff in fjords may reduce recent growth rates in larval stages of rockfish Sebastes oculatus and lightfish Maurolicus parvipinnis, but it has no effect in clupeid larvae Sprattus fuegensis (Landaeta & Castro, 2006; Landaeta et al., 2012).

Why does freshwater input appear to benefit larval growth rate in austral hake from this region? Large water stability in fjords ecosystems caused by freshwater discharges could have a potential benefit for larval hake in terms of predator-prey encounter rates and a subsequent increase of feeding success (large ingested prey volume, Landaeta et al., 2011). Additionally, hake larvae have a wide visual acuity from its early stages (Morote et al., 2011), aiming them to successfully capture prey at low light intensities in fjords and channels. Near the Baker River mouth, net flux estimates showed that small meroplankton, such as barnacle nauplii are advected landward (Meerhoff et al., 2015), indicating that suitable prey for small hake larvae is more abundant inside fjords and channels than over the shelf.

Channels and fjords had sea water colder than shelf waters (Table 1). The lack of significance of the relationship between IGR of austral hake and sea temperature has been previously described for larval hake elsewhere (Cass-Calay, 1997; Brown et al., 2004; Alvarez & Cotano, 2005). Timescale changes for growth rate in fish larvae and temperature in the water column are different. For larval hake during spring 2014, growth seemed to respond more to food availability than temperature variations.

Recently, the use of otolith fluctuating asymmetry (OFA) to assess fitness has been questioned (Diaz-Gil et al., 2015). Similarly, OFA was unsuccessful to find any significant difference between fast-growing and slow-growing larval Atlantic menhaden Brevoortia tyranus (Fey & Hare, 2008), or in larval M. parvipinnis inhabiting fjords and channels of southern Chile (Zenteno et al., 2014). Nonetheless, the level of the stress factors, in the present case, low salinity (as fresh as 1.15) and high turbidity (from 0 to 15 NTU) must be significant to affect OFA, and these stressors may affect differentially to early life stages of epipelagic or benthic species (Grenkjoer & Sand, 2003; Fey & Hare, 2008). Austral hake larvae can be found in the first 100 m depth of the water column, with largest abundances from the surface to 25 m depth (Castro et al., 2011), and therefore it is plausible that larvae experienced fresher and turbid waters.

Present results confirm recently published evidence based on trace element signatures of otolith cores of austral hake collected in Chilean and Falkland Islands' waters (Brickle et al., 2016). These authors suggest that there is only one spawning stock of austral hake with spawning situated in and around the Chilean fjords, and the variation in Sr/Ca ratios likely suggest that survivors were moving across salinity gradients during early ontogeny, i.e., they used nursery areas with different salinities (open areas, channels, fjords) prior to the migration to their feeding grounds in southern South Atlantic (Arkhipkin et al., 2003).

DOI: 10.3856/vol46-issue1-fulltext-20


We are in debt with the field support of all the crew of RV Cabo de Hornos during the cruise, and particular thanks to Viviana Rios (Universidad de Valparaiso, Chile). We appreciate the comments and suggestions made by two anonymous reviewers to an early version of the manuscript. This research was funded by Comite Oceanografico Nacional (CONA, Chile) [grant number CIMAR C20F 14-09] adjudicated to MFL and CAB.


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Received: 4 November 2016; Accepted: 27 March 2017

Mauricio F. Landaeta (1,2), Gissella Castillo-Hidalgo (1) & Claudia A. Bustos (1)

(1) Laboratorio de Ictioplancton (LABITI), Escuela de Biologia Marina Facultad de Ciencias del Mar y de Recursos Naturales, Universidad de Valparaiso Vina del Mar, Chile

(2) Centro de Observacion Marino para Estudios de Riesgos del Ambiente Costero (COSTA-R)

Corresponding author: Mauricio F. Landaeta (

Corresponding editor: Guido Plaza

Caption: Figure 1. Location of the study site, Chilean Patagonia, abundance and distribution of larval austral hake Merluccius australis during October 2014.

Caption: Figure 2. a) Potential relationship between sagitta otolith radius (OR, [micro]m) and larval size (standard length, SL, mm), SL = 1.1183[(OR).sup.0.3813], n = 100, b) Linear relationship between age (microincrement counts, A, days) and larval size (SL, mm), SL = 3.031 + 0.1297(A), n = 88. Dotted lines correspond to 95% confidence interval; c) frequency of signed asymmetry of left and right sagitta area from larval Merluccius australis from south Patagonia.

Caption: Figure 3. Relationships between size-at-age residuals (from the linear growth model), individual growth rates and otolith fluctuating asymmetry with vertical gradients of salinity ([DELTA]salinity) and stability (Brunt-Vaisala frequency).
Table 1. Summary of water column (first 100 m depth) environmental
conditions, during austral spring 2014 in the study area (south
Chilean Patagonia). SD: one standard deviation. P values correspond to
results of Mann-Whitney U tests.


                                    Mean                    SD

Temperature ([degrees]C)           9.405                  0.508
Salinity                           32.953                 0.825
Stability (cycles            1.44 x [10.sup.-4]     2.45 x [10.sup.-4]
Turbidity (NTU)                    0.777                  0.754

                                       Channels and fjords

                                    Mean                    SD

Temperature ([degrees]C)           9.068                  0.673
Salinity                           31.538                 2.927
Stability (cycles            6.62 x [10.sup.-4]     3.49 x [10.sup.-3]
Turbidity (NTU)                    0.967                  2.117

                            Channels and fjords


Temperature ([degrees]C)        5.54 x 10-35
Salinity                        5.31 x 10-59
Stability (cycles               7.86 x 10-31
Turbidity (NTU)                    0.238

Table 2. Spearman correlation rank tests (rs) between
size-at-age residuals (SAR), individual growth rates
(IGR), and fluctuating asymmetry (FA6) and environmental
conditions of the water column. Bold numbers
indicate significant correlations (P < 0.05)

                                 SAR        IGR        FA6

Delta temperature                0.139      0.187      0.103
Delta salinity                   0.287#     0.373#     0.283#
Maximum stability                0.181      0.294#     0.280#
Maximum turbidity                0.032      0.072      0.222#

Note: Significant correlations (P < 0.05) were indicated with #.
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Title Annotation:Short Communication
Author:Landaeta, Mauricio F.; Castillo-Hidalgo, Gissella; Bustos, Claudia A.
Publication:Latin American Journal of Aquatic Research
Date:Mar 1, 2018
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