Atractoscion Nobilis) in the Northeastern Paciﬁc Based on Otolith Isotopic Composition

Estuarine, Coastal and Shelf Science 170 (2016) 134e144

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Estuarine, Coastal and Shelf Science

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Rearing conditions and habitat use of white seabass (Atractoscion nobilis) in the northeastern Paciﬁc based on otolith isotopic composition

* Alfonsina E. Romo-Curiel a, Sharon Z. Herzka a, , Chugey A. Sepulveda b, Paula Perez-Brunius c, Scott A. Aalbers b a Departamento Oceanografía Biologica, Centro de Investigacion Científica y de Educacion Superior de Ensenada (CICESE), No 3918 Carretera Tijuana- Ensenada, Ensenada, Baja California, C.P. 22860, Mexico b Pfleger Institute of Environmental Research (PIER), 2110 South Coast Highway Suite F, Oceanside, CA, 92054, USA c Departamento Oceanografía Física, Centro de Investigacion Científica y de Educacion Superior de Ensenada (CICESE), No 3918 Carretera Tijuana- Ensenada, Ensenada, Baja California, C.P. 22860, Mexico article info abstract

Article history: White seabass, Atractoscion nobilis, is an important coastal resource throughout both California and Baja Received 14 May 2015 California, but whether this species comprises a single or multiple subpopulations in the northeastern Received in revised form Pacific is not known. The aim of this study was to infer larval rearing habitats and population structure of 17 November 2015 white seabass by sampling adults from three regions spanning a latitudinal temperature gradient and a Accepted 9 January 2016 distance of over 1000 km, and analyzing the isotopic composition (d18O and d13C) of otolith aragonite Available online 13 January 2016 corresponding to the larval, juvenile and adult stages. Otolith cores revealed high isotopic variability and no significant differences among regions, suggesting overlapping rearing conditions during the larval Keywords: stage, the potential for long distance dispersal or migration or selective mortality of larvae at higher White seabass d Atractoscion nobilis temperatures. Back-calculated temperatures of aragonite precipitation derived using regional salinity- w Otolith aragonite relationships and local salinity estimates also did not differ significantly. However, there were significant 18 Isotopic analysis differences between the d O values of the first seasonal growth ring of age 0 fish as well as back- Habitat use calculated aragonite precipitation temperatures, suggesting the presence of two potentially discrete subpopulations divided by Punta Eugenia (27N) along the central Baja California peninsula. These findings are consistent with regional oceanographic patterns and are critical for understanding white seabass population structure, and provide information needed for the implementation of appropriate management strategies. © 2016 Elsevier Ltd. All rights reserved.

1. Introduction distance is driven by a host of biological and physical processes (Largier, 2003; Cowen and Sponaugle, 2009). Juveniles can spend Assessing the role of dispersion, migration and the level of months to years in juvenile habitats (Griffiths and Hecht, 1995), and population connectivity is important for managing coastal fish adults have the potential to migrate tens to hundreds of kilometers populations and identifying ecologically important habitats to form spawning aggregations (Aalbers and Sepulveda, 2015). (Gillanders, 2005; Cowen and Sponaugle, 2009). Sciaenid fishes Hence, the population structure of sciaenids and other marine have early life stages that can be found in various coastal habitat species with similar life history strategies may reflect the processes types (Cowan and Birdsong, 1985; Gray and McDonall, 1993). The influencing dispersion as well as migration patterns. larval stage can last several weeks (Donohoe, 1997), and drift The white seabass, Atractoscion nobilis, is one the largest members of the family Sciaenidae, reaching 160 cm total length (TL) and more than 41 kg (Vojkovich and Reed, 1983). It is an * Corresponding author. important species for both the recreational and local commercial E-mail addresses: [email protected] (A.E. Romo-Curiel), sherzka@cicese. fisheries along the Pacific coast of California and Baja California mx (S.Z. Herzka), [email protected] (C.A. Sepulveda), [email protected] (P. Perez- (Allen and Franklin, 1992; Allen et al., 2007; Cartamil et al., 2011). Brunius), [email protected] (S.A. Aalbers). http://dx.doi.org/10.1016/j.ecss.2016.01.016 0272-7714/© 2016 Elsevier Ltd. All rights reserved. A.E. Romo-Curiel et al. / Estuarine, Coastal and Shelf Science 170 (2016) 134e144 135

Few studies have provided information regarding spawning loca- movements and growth of this species, a clear understanding of its tions and migration patterns, and there is limited information on population structure remains lacking for this valuable bi-national larval and juvenile ecology. The white seabass spawning period is resource. To build upon recent population structure hypotheses during the spring and summer months (May to August), and and better understand white seabass population dynamics, this spawning aggregations may be found in the interface between the study used otolith isotopic composition to assess population sandy areas and shallow rocky reefs that support kelp forests connectivity. (Thomas, 1968; Aalbers and Sepulveda, 2012). Several studies focusing on different life stages have contributed 1.1. Isotopic analyses to the current understanding of white seabass population structure. Moser et al. (1983) found that while the spawning centers are The isotopic composition of otolith aragonite (d18O and d13C) has located off southern California and central Baja California, a higher been used as a natural tracer to evaluate habitat use, population abundance of white seabass larvae were caught in the inshore structure, migration, connectivity and mixing of fish populations, (<50 m from the surf zone) regions of San Sebastian Vizcaino Bay and for reconstructing their temperature and salinity history and the Gulf of Ulloa (Fig. 1). Allen and Franklin (1992) studied the (Patterson et al., 1993; Valle and Herzka, 2008). Isotopic ratios are distribution of newly settled juveniles in coastal waters and pro- permanently imprinted in the otolith carbonate, recording ambient posed that larvae transported from northern Baja California to conditions experienced by an individual fish at the time of arago- southern California were a major source juveniles. Previous genetic nite precipitation (Campana, 1999). The stable isotopes of oxygen studies have suggested a potentially continuous spawning popu- (18O/16O) in otolith aragonite are deposited near equilibrium with lation in the eastern Pacific(Bartley and Kent, 1990; Franklin, 1997; the isotopic composition of the ambient water (dw). However, there Coykendall, 2005), but the geographical range, sample size or is isotope discrimination against 18O as a function of temperature, number of genetic markers employed by these studies is limited. resulting in a negative relationship between d18O values and tem- Tagging studies suggest limited (ca. <200) seasonal migrations perature (Epstein et al., 1953; Iacumin et al., 1992; Patterson et al., along the California coastline (Hervas et al., 2010; Aalbers and 1993). It is possible to estimate the temperature of the water at the 18 Sepulveda, 2015). However, the absence of tagging studies in cen- time of aragonite deposition using d O values and estimates of dw tral and southern Baja California waters precludes the assessment (Campana, 1999; Darnuade et al., 2014), and to thereby discrimi- of connectivity between the northern and southern range of white nate between fish living under different environmental conditions seabass in the Pacific. More recently, regional differences in otolith (Iacumin et al., 1992; Godisken et al., 2012). Regional salinity-dw growth rates of age 1 fish have been found between southern relationships can be used to estimate the isotopic composition of California and southern Baja California, which are likely attributed seawater (Craig and Gordon, 1965; Paul et al., 1999), as predict d18O to differences in environmental conditions (Romo-Curiel et al., values for particular regions (Rowell et al., 2005; Valle and Herzka, 2015). These findings suggest limited mixing, at least during the 2008). first year of life. In summary, despite the recent work on In contrast, carbon isotope ratios reflect both dietary sources via metabolic processes as well as the dissolved inorganic carbon (DIC) pool (Thorrold et al., 1997; Hoie et al., 2003). The contribution of carbon deposited in the otoliths from metabolic sources varies and has been estimated at 20e30% of the total (Kalish, 1991; Weidman and Millner, 2000), and the remainder presumably reflects the isotopic composition of DIC (Campana, 1999). Nevertheless, geographic variations the carbon isotope ratios of the otolith aragonite have been successfully used as natural tags to differen- tiate between fish subpopulations (Newman et al., 2010; Steer et al., 2010; Correia et al., 2011). Data from the otolith core (the central portion of otoliths that is deposited during early life) can provide information regarding natal origin and spawning areas, while data corresponding to specific ages may indicate changes in fish habitat over time (Gao et al., 2004, 2013; Steer et al., 2010; Gao et al., 2013). The isotopic analysis of subsamples from specific sections of adult otoliths corresponding to specific time periods enables the reconstruction of each individual's environmental history as a function of age, date and other life history considerations (Gillanders, 2005, Weidman and Millner, 2000). Central to the robust interpretation of the isotopic composition of biogenic carbonates and the calculation of robust temperature estimates based on d18O values is the explicit consideration of the processes that underlie its variability (Thorrold et al., 1997; Campana, 1999; Elsdon and Gillanders, 2002). Thus, oceanographic data should incorporated into the analysis and interpretation of isotope ratios (Ashford and Jones, 2007). The isotopic composition of the otolith core of adult white seabass collected from three regions of the northeastern Pacific, encompassing a distance of over 1000 km, was measured to infer larval rearing habitats and population structure. We also analyzed Fig. 1. Sampling areas of white seabass, A. nobilis, off southern California and the Baja the isotopic composition of subsamples from seasonal translucent California peninsula (rectangles). Dots indicate the pixels considered to calculate the average monthly sea surface temperature (SST) using high-resolution estimates and opaque otolith growth rings corresponding to the juvenile (age generated by the Scripps Photobiology Group at Scripps Institution of Oceanography. 0.5e2 yr) and adult (age 8e10 yr) stages to infer ontogenetic 136 A.E. Romo-Curiel et al. / Estuarine, Coastal and Shelf Science 170 (2016) 134e144 movement patterns and the level of mixing between different life core and four growth rings corresponding to the juvenile stage stages. Back-calculated aragonite precipitation temperatures were were sampled: the first and second summer growth seasons compared to regional coastal SST's and in situ measurement of (opaque rings corresponding to the first and second year of life, temperature and salinity to evaluate whether the d18O values of hereafter referred as 0.5 and 1.5 yrs) and the first and second otolith core and growth rings were consistent with regional winters (translucent rings, hereafter age 1 and 2 yrs). Likewise, five oceanographic conditions. Differences in the oxygen and carbon growth rings corresponding to the adult stage were sampled (8.5, isotopes values in otolith core and growth rings of adult white 9.5, and 10.5 yrs, corresponding to the summer opaque growth seabass from different locations would indicate that adult fish were rings and 9 and 10 yr, corresponding to the winter translucent reared under different environmental conditions, and would sug- rings). Each growth ring was sampled by drilling a single curve (650 gest limited connectivity between subpopulations. Further, given long 150 mm wide and 100 mm set depth). After the collection of that there is a sharp latitudinal gradient in SST throughout the each sample, the microdrill bit and work surface were cleaned with distribution of white seabass in Pacific waters, we hypothesized compressed air. that fish sampled in more southern waters would present d18O Between 30 and 60 mg of aragonite were weighed on a micro- values consistent with higher aragonite precipitation temperatures. balance. Analysis of otolith powder was performed in the Stable Isotope Laboratory of the University of California at Santa Cruz 2. Methods using a Kiel IV carbonate device coupled to a Thermo Scientific MAT253 Isotope Ratio Mass Spectrometer under certified standards 2.1. Sample collection (CM12, Atlantis II, NBS-18 and NBS-19). Precision measurements (SD) of d18O values were 0.03‰ for CM12, and 0.02‰ for Atlantis II, Otoliths were obtained opportunistically from commercial and NBS-18 and NBS-19. For d13C, the precision was 0.06‰ for CM12 recreational catches of white seabass from April through August of and Atlantis II, 0.02‰ for NBS-18 and 0.05‰ for NBS-19. All isotopic 2009e2011. Commercial fishing activities were conducted aboard analysis and measurements are reported in standard d notation (‰) small (5e7 m), outboard-powered fishing boats, within 5e20 km of using VPDB (Vienna Peedee Belemnite) as the international coastal fishing camps along Baja California. Samples were also ob- standard: tained from recreational fishing tournaments targeting white sea- . d ¼ bass within southern California, as well as from PIER research Rsample Rstandard 1 1000 (1) vessels (SCP ID NUMBER: 002471). A total of 117 samples were ¼ collected in three regions: southern California (SC; n 40), USA, where R is the abundance of the heavy to light isotope ratio of the ¼ San Sebastian Vizcaino Bay (VB; n 36) and the Gulf of Ulloa (GU; sample or standard. ¼ n 41) off the central and southern Baja California peninsula, The time period integrated by each core sample was estimated Mexico, respectively (Fig. 1). based on the analysis of young-of-the-year white seabass (4e12 cm TL; n ¼ 20) otolith samples collected during a trawl 2.2. Isotopic analysis survey along the coast off Camp Pendleton, California on July 19e21, 2010. Each sagittal otolith from young-of-the-year white fi One sagittal otolith from each sh was embedded in epoxy resin seabass was mounted sulcus-side up on a glass slide and polished and sectioned transversely using a low speed diamond saw using abrasive paper of decreasing grit and 0.05-micron alumina to ™ (Buehler, ISOMET ) to cut through the otolith core. The section enhance the visibility of daily growth increments. Polished otoliths containing the core was mounted on a microscope slide using were viewed with a microscope (Leica DMLS; 10e40 magnifica- epoxy resin and polished using abrasive paper of decreasing grit tion) and photographed with a digital camera (Leica DFC 450). Daily size. Age estimates of all otoliths sections were evaluated in a growth increments were counted twice for each individual by two previous study (Romo-Curiel et al., 2015), and the spawning year independent readers, starting from the focus of the core and core fi for each sh was back-calculated based on catch date. White sea- diameter was measured using the Image J software package (Na- e ¼ bass born between 1999 and 2006 (age range 4 12 yrs; n 32 for tional Institutes of Health, Bethesda, MD, USA). SC, n ¼ 36 for VB and n ¼ 32 for GU) were selected for isotopic analysis of the otolith core. This period excludes El Nino~ years, which has been shown to influence the isotopic composition of fish 2.3. Regional SST and salinity otoliths in the California Current region due to the abnormally high water temperatures (Dorval et al., 2011). To obtain temperature estimates representative of white sea- Carbonate was extracted from three different regions along the bass larval habitat, sea surface temperatures (SST) during the sectioned otolith surface with a high precision microdrill (ESI New spawning season (AprileSeptember) were obtained by down- Wave Micromill) at the Marine Science Institute, University of Texas loading oceanographic data from the Scripps Photobiology Group in Austin and at the Center for Scientific Research and Higher Ed- of Scripps Institute of Oceanography, University of California San ucation of Ensenada (CICESE). Each otolith core sample was ob- Diego (http://spg.ucsd.edu/Satellite_data/California_Current/ tained from a 300 300 mm square centered on the core using a viewed on October 2014). The SSTs represent an integration of raster pattern with parallel lines separated by 100 mm and with a data generated with the AquaMODIS, Terra and SeaWiFS satellites depth setting of 100 mm. The raster area was designed to coincide processed by Mati Kahru, and are available with high resolution with the dimensions of the otolith core (Fig. 2). The limited di- (approx. 1 km2). Monthly mean SST data were compiled for near- mensions of the area from which aragonite was extracted in the coastal waters from April 2000eSeptember 2006 (Fig. 1). Salin- otolith core was designed to reduce the potential for contamination ities at 10 m were obtained from reports and publications derived with aragonite precipitated during other life stages (e.g. Begg et al., from in situ measurements conducted during quarterly CalCOFI and 1999). Fishes of at least 10 years of age (mean age of 13 yrs) were Investigaciones Mexicanas de la Corriente de California (IMECO- selected for isotopic analysis of annual growth rings. Isotopic CAL) cruises off the coast of the Baja California peninsula (http:// analysis of annual growth rings was only conducted for white www.calcofi.org/ccpublications/ccreports.html). Salinities were seabass samples collected from the two distal regions (SC and GU) obtained for two periods: summer (April to September) and winter with the most contrasting environmental conditions. The otolith (October to March) for the same regions used to estimate SST A.E. Romo-Curiel et al. / Estuarine, Coastal and Shelf Science 170 (2016) 134e144 137

Fig. 2. Image of a transverse section of an adult white seabass (A. nobilis) otolith. The core is at the center with the raster sampling pattern of the automated micro-milling (dotted lines). White lines represent the single curve for each sampled growth ring of the juvenile and adult stage.

18 values. To evaluate the degree of similarity between monthly Predicted d Ooto values for aragonite for temperatures and sa- average SSTs and salinity very near the coast (not covered by Cal- linities of each region were calculated based on dw estimates COFI or IMECOCAL cruises), the SST and salinity records were derived using the Craig and Gordon (1965) equation for north Pa- compared with in situ measurements made at the Scripps Institu- cific surface waters and Campana (1999) aragonite equation. 18 18 tion of Oceanography Pier in southern California (http://www. Measured d Ooto values were compared to predicted d Ooto values sccoos.org/data/piers). For the waters off the Baja California to evaluate whether there was overlap in the environmental con- peninsula regions, the comparisons were made with the seasonal ditions typical of each sampling region and the stage-specificox- climatology provided by Durazo et al. (2010). ygen isotopic composition of fish otoliths.

2.5. Statistical analysis 2.4. Isotopic composition of seawater (dw) and back-calculated temperature Using the Quartile Method based on median distribution values (Zar, 1999), all outliers were identified and excluded from statistical The isotopic composition of seawater (dw) was calculated from regional salinity estimates using the Craig and Gordon (1965) analysis. One-way analysis of variance (ANOVA) was used to test 13 18 equation for north Pacific surface waters: whether d C and d O values of otolith cores differed between sampling regions. The non-parametric KolmogoroveSmirnov test dw ¼18:5 þ 0:54 Salinity (2) (KeS) was used to compare the distribution of isotopic values among regions. Back-calculated temperatures were compared be- There is an absence of detailed regional data on the isotopic tween regions using a one-way ANOVA. The post-hoc multiple composition of seawater, particularly for the waters off central and comparisons between isotopic values among regions were per- southern Baja California. The processes that contribute to changes formed using Scheffe's test. Age-specific d13C and d18O values from in the salinity and d of surface waters are rainfall, freshwater w juvenile and adult growth rings were compared between regions inflow, melting ice, evaporation and freezing, as well as vertical with a two-way repeated measures analysis of variance (RM mixing and horizontal advection (Schmidt, 1998; Sharp, 2007). ANOVA); the data corresponding to juvenile and adult growth rings However, the waters off southern California and Baja California are were treated separately. Holm-Sidak post-hoc tests for pairwise not subject to freezing and are limited in freshwater inflow due to comparisons were used to identify whether there were differences the region's arid nature (Wilkinson et al., 2009). The primary fac- in isotopic values between ages and regions. All data complied with tors driving variations in salinity in the coastal waters inhabited by parametric assumptions of normality (ShapiroeWilks test) and white seabass are therefore upwelling events, evaporation and the homoscedasticity (Levene's test). Data were analyzed using the mixing of different water masses. The slope of Craig and Gordon Systat 13 and plotted using Sigma Plot 12.5 software packages. (1965) equation is similar to the one reported by Paul et al. (1999) for mid-latitudes and the one derived from GEOSECS data (dw ¼17.95 þ 0.50 Salinity; see also Valle and Herzka, 2008), 3. Results supporting the use of relationship for deriving estimates of dw. The isotopic composition of the water was corrected (0.22‰) to ac- 3.1. Isotopic analysis of otolith cores count for the difference in the standards used to report oxygen isotope ratios of water and biogenic carbonates (Sharp, 2007). Stable isotope values were obtained for 100 white seabass Back-calculated temperatures were estimated from oxygen otolith cores (Fig. 3). Two outliers were identified in two different 18 ‰ d13 ‰ d18 isotope ratios (d Ooto) at the otolith core from SC, VB and GU and GU samples with values of 5.37 for C and 1.88 for O; 13 along juvenile growth rings of fish caught in SC and GU by applying both fish were excluded from further analysis. The average d C the aragonite equation proposed by Campana (1999) in an exten- value was 2.66 ± 0.60 for SC (mean ± SD; range 3.73 to 1.54‰), sive review of the literature: 3.75 ± 0.78‰ for VB (4.74 to 1.92‰) and 2.81 ± 0.64 for the GU (range 4.17 to 1.28‰). The d18O values were also variable, 18 ‰ ± ¼ ± d Ooto ¼ dw þ 3:71 0:206 T C (3) ranging from 1.52 to 0.02 for SC (mean SD 0.61 0.31‰),1.57 to 0.01‰ for VB (0.75 ± 0.35‰) and 1.49‰ 18 where d Ooto is the isotopic composition measured from otolith to 0.09 (0.71 ± 0.34) for GU. subsamples. The isotopic composition of the water was estimated There was a significant difference in d13C values between re- based on mean salinity estimates of the region where the corre- gions (ANOVA F(2,95) ¼ 27.47, P < 0.001); the mean carbon isotope sponding adult was caught (see results). composition of VB differed from SC and GU (Scheffe's test, 138 A.E. Romo-Curiel et al. / Estuarine, Coastal and Shelf Science 170 (2016) 134e144

showed a high level of dispersal, even when the number of individuals analyzed for a particular year was limited (Fig. 4).

3.2. Regional SST and salinity

Comparison of mean monthly SSTs between regions indicated a marked latitudinal gradient (Supplementary Fig. 1), and there was a similar pattern in SSTs during the spawning period (AprileSep- tember) from 1999 to 2006. Monthly average temperatures from April to September were similar between SC and VB (ranging from 15.8 to 21.0 C and 16.3e21.8 C, respectively). Higher temperatures were observed for GU (17.3e26.6 C). During the summer, SSTs at GU were 3 to 6 C higher than at SC and 4 to 5 C greater than VB. In SC the highest monthly SST was observed during August (21.0 Con average). In both VB and the southern region the highest SST occurred during September (21.8 C and 26.6 C, respectively, on average). Regional salinity at 10 m depth during the spawning season (AprileSeptember) and winter (OctobereMarch) months of 1999e2006 also showed a latitudinal gradient (Table 1). Given the linear relationship between salinity and dw, estimates of the isotopic composition of seawater in GU exhibited lighter values than that from SC and VB (Supplementary Fig. 2). Within a region, average dw values showed limited temporal variability, varying by <0.02‰ between seasons in SC and VB, and by 0.25‰ in GU.

3.3. Back-calculated temperature of otolith cores

18 The back-calculated temperatures derived from d Ooto values of the otolith cores of white seabass ranged from 14 Cto23C(Fig. 5). The back-calculated temperatures for fish captured in each region Fig. 3. Carbon and oxygen isotope ratios measured in the otolith cores of White 18 were highly variable, reflecting the variability in d Ooto values. For Seabass (A. nobilis) sampled off Southern California (SC), Vizcaino Bay (VB) and in the SC, the average back-calculated temperature was 17.8 C (range Gulf of Ulloa (GU). White circles indicate outliers that were excluded from statistical e e analyses. 15.3 21.9 C), 18.6 C for VB (range 14.9 22.5 C) and 18.9 C for GU (range 16.0e22.2 C). Despite the overlapping back-calculated temperatures between regions, there were significant differences 13 18 MS ¼ 0.506, P < 0.001). The frequency distributions of d C values in d Ooto values (F (2, 95) ¼ 3.979, P ¼ 0.026); the mean back- between localities differed significantly between VB and the calculated temperature in GU was significantly higher than SC northern and southern regions (KeS, P < 0.001). In contrast, (Scheffe's test, MS ¼ 2.572, P ¼ 0.032). There were no significant average d18O values were not significantly different between re- differences between the mean back-calculated temperature for SC gions (ANOVA F(2,95) ¼ 1.41, P ¼ 0.249), nor were there differences vs VB and between VB vs GU (Scheffe's test, P > 0.05). in the frequency distributions of isotopic values (KeS, P > 0.05). The range of d13C and d18O values as a function of spawning year 3.4. Comparison of predicted vs. measured d18O values

The range of predicted aragonite d18O values obtained by considering regional summer SSTs and salinities had a broader range for the GU than SC and VB, and showed overlap between regions (Table 1; Fig. 6). For SC the predicted d18O values ranged from 0.10‰ and 1.40‰; the range for VB was similar (from 0.15‰ to 1.50‰). In contrast, the range of predicted d18O values was greatest for GU (0.17‰ to 2.30‰). Comparison of the 18 18 range of predicted d O values with d Ooto measurements indi- 18 cated that almost all d Ooto measures were within the range of the predicted isotopic values for a given region. For SC and VB, the range of predicted d18O values (rectangles) is almost the same as 18 18 the measured d Ooto. For GU, the range of predicted d O values 18 was greater than the measured d Ooto values; none of the otolith cores had isotope ratios <1.6‰.

3.5. Isotopic analysis of juvenile and adult growth rings

The d13C values of individual juvenile and adult white seabass Fig. 4. d13C (a) and d18O (b) values of otoliths cores of White Seabass plotted as a otolith growth rings collected in SC and GU exhibited an increasing function of their spawning year and by sampling region: Southern California (SC), Vizcaino Bay (VB) and Gulf of Ulloa (GU). The numbers above the boxplot represent the level of variability as a function of age; the range of values increased sample size for each year. from 2 to 3‰ during the juvenile stage to ca 4.5‰ for the adult A.E. Romo-Curiel et al. / Estuarine, Coastal and Shelf Science 170 (2016) 134e144 139

Table 1 Regional salinities (minimum, maximum and average), estimated oxygen isotopic composition of the water (dw), and summer SSTs obtained from satellite images for Southern California (SC), Vizcaino Bay (VB) and Gulf of Ulloa (GU).

Region Salinity dw(‰) SST (C)

Summer Winter Summer Winter Summer

Min Max Mean Min Max Mean Min Max Min Max Min Max

SC 33.2 33.6 33.4 33.2 33.9 33.6 0.79 0.58 0.79 0.41 15.76 21.06 VB 33.3 33.7 33.6 33.3 33.6 33.5 0.74 0.52 0.74 0.58 16.32 21.81 GU 33.6 34.1 33.9 33.7 34.5 34.1 0.58 0.31 0.52 0.09 17.28 26.58

stage (Supplementary Fig. 3a and c). In contrast, the d18O values of juvenile growth rings showed a consistent pattern between opaque (summer growth, more depleted isotope ratios) and translucent (winter growth, more enriched isotope ratios) rings and a much narrower range than d13C values. However, the seasonal pattern was no longer observed during the adult stage (Supplementary Fig. 3b and d). The mean carbon and oxygen isotope ratios for white seabass otolith growth rings showed distinct patterns when comparing the juvenile and adult life stages (Fig. 7). While mean isotope ratios showed distinct seasonal shifts during the juvenile stage, these were not evident during the adult stage. Two-way repeated measures ANOVA indicated that there were no significant differences in mean d13C and d18O values between regions during either the juvenile or adult stage (Supplementary Table 1). However, for the juvenile stage, mean d13C and d18O values differed significantly between ages for fishes sampled in both regions (Supplementary 18 Fig. 5. Frequency distribution of back-calculated temperatures obtained from d Ooto values of otolith cores of White Seabass, A. nobilis, adults collected in Southern Cali- fornia (SC), Vizcaino Bay (VB) and Gulf of Ulloa (GU).

Fig. 6. Isotopic map of predicted d18O values for aragonite as a function of salinity and temperature. Rectangles represent the range of predicted d18O values for three regions of the California current system in which white seabass were sampled, based on Fig. 7. Mean d13C and d18O values (±standard error) measured in seasonal otolith regional sea surface temperature and salinities during their summer spawning season. growth rings of juvenile and adult of white seabass, A. nobilis. Samples were collected Diagonal lines indicate the full range of isotopic values measured in the otolith cores in Southern California (SC; white circles dots) and Gulf of Ulloa (GU; black circles). for each region: Southern California (line with dots), Vizcaino Bay (dashed line) and N ¼ otolith core; S ¼ summer growth ring; W ¼ winter growth ring; subscripts Gulf of Ulloa (dots). correspond to the estimated age of each growth ring. 140 A.E. Romo-Curiel et al. / Estuarine, Coastal and Shelf Science 170 (2016) 134e144

Table 1). The Holm-Sidak post-hoc pairwise comparison test indi- 4. Discussion cated significant differences in d18O values between summer (S) and winter (W) growth rings of juveniles (Fig. 7; Supplementary Findings of this study provide evidence to support the presence Table 2). The only significant differences in d18O values between of two potentially discrete subpopulations of white seabass divided ages was for S0.5, which corresponds to summer growth during the by Punta Eugenia in the Baja California peninsula. The isotopic first year of life (the difference between mean isotope ratios was analysis of the first otolith growth ring indicated that white seabass 0.65‰), with significant differences at that age among regions (RM collected in southern California must consistently experience ANOVA, t ¼ 2.663, P ¼ 0.010). different environmental conditions than individuals reared within the Gulf of Ulloa. These results agree with the differences in growth rates reported by Romo-Curiel et al. (2015) for the first year of life in fi 3.6. Back-calculated temperature for core and seasonal growth adult white seabass from the same regions, and have signi cant rings of juveniles management implications.

The back-calculated temperatures for the seasonal growth rings 4.1. Isotopic composition of otolith cores and back-calculated larval sampled during the juvenile stage showed a broad range and rearing temperatures overlapped between ages and seasons (Fig. 8). The limited variability in salinity (and hence d estimates) led to temperature The estimated time interval represented by otolith core sub- w e e differences of <2 C for individual growth rings. Higher tempera- samples was 18 25 days, consistent with the 2 3 week duration of tures coincided with the summer aragonite precipitation and lower the white seabass larval period reported by Donohoe (1997). The d13 d18 temperatures corresponded to the winter rings. Back-calculated C and O values of the otolith cores of adult white seabass fi captured within each sampling region were highly variable across temperatures were higher in sh captured in GU than those from ‰ SC, with a difference around 1 C for the same age among regions. spawning years and age classes (up to 2 ; Fig. 3). The variability in isotopic ratios were persistent through time and thus representa- However, the temperature of the first summer opaque ring (S0.5) was higher in the GU than SC by about 4.5 C on average. tive of the white seabass population, allowing for robust inferences into its population structure. The d13C values of the carbon precipitated in fish otoliths is a function of the dissolved inorganic carbon (DIC) as well as the byproducts of an individual's metabolism (Kalish, 1991; Weidman and Millner, 2000; McMahon et al., 2013). The d13C value of the DIC in surface waters of the Pacific off North America is approxi- mately 0.8e0.9‰ as a result of upwelling events along the coast, and those values do not change substantially at spatial scales dominated by isolated physical processes (Kroopnick, 1985; McMahon et al., 2013). In contrast, the relative contribution of metabolically derived carbon to the d13C values of otolith carbonate varies between species and even among individuals of the same species (Iacumin et al., 1992; Weidman and Millner, 2000; Nelson et al., 2011). Estimating the percent contribution of each source of carbon to the d13C values of white seabass otoliths was beyond the scope of this study. However, the d13C values measured in otolith core of white seabass from each sampled region were highly variable and lighter (ca 1.5 to 5‰) than regional DIC values (ca. 1‰; Fig. 3a), suggesting that the contribution of metabolic carbon is likely important, albeit variable. The difference in average d13Cin VB relative to those from SC and GU suggests that larval white seabass from VB probably relied on a different food source, or that the relative contribution of food-based carbon varied between regions. The isotopic composition of seawater (dw) varied seasonally between regions, mirroring regional shifts in surface salinities. Craig and Gordon (1965) reported dw values between 0.5 and 0.4‰ for the northeastern Pacific surface waters based on samples taken between 20N, 130W and 32N, 120W. For the summer season during which white seabass spawn, the range of dw values reported by Craig and Gordon (1965) is only 0.12 and 0.19‰ more enriched in 18O than the mean values applied to back- calculated temperature estimates of fish caught in SC and VB, respectively, and similar to the estimates for the GU (0.58 to 0.31‰). Limited variability in regional salinity (<1, equivalent to 0.5‰ in dw) indicates regional temperature is the most important factor Fig. 8. Back-calculated temperatures for the core and seasonal growth rings of white influencing d18O values observed in white seabass otoliths. The high seabass sampled off southern California (a) and the Gulf of Ulloa (b). Minimum (black variability in d18O values measured in otolith core (range 2‰)was circles) and maximum temperatures (white circles) were calculated using minimum fl and maximum regional salinity estimates. In X axis: N ¼ otolith core, W ¼ winter, re ected in a wide range of back-calculated temperatures for each S ¼ summer, subscript ¼ age of fishes in years. sampling region, which overlapped. Aalbers (2008) reported an A.E. Romo-Curiel et al. / Estuarine, Coastal and Shelf Science 170 (2016) 134e144 141 ambient water temperature of 11.3e21.7 C in coastal waters off offshore, and some exposed coastlines or points are prone to local southern California during spawning events of wild white seabass. intense upwelling (Graham and Largier, 1997; Marin et al., 2003; The highest frequency of spawning activity was recorded between Tapia et al., 2009). Given that the local temperature regime near 15 and 18 C, similar to the back-calculated temperatures estimated the coast is highly dynamic and variable, it could generate high for otolith cores of adults caught in SC waters. The broad range of variability in the oxygen isotope composition of larval otoliths. back-calculated temperatures might reflect seasonal changes in the White seabass larvae are also epipelagic during the late larval environmental conditions prevalent during the long spawning phase, which may be related with seeking preferential tempera- period of white seabass (Thomas, 1968; Aalbers, 2008). The differ- tures or their predator-avoidance capabilities (Margulies, 1989). In ences in average back-calculated temperature between SC and GU addition, off southern California white seabass larvae change from a likely reflects the well-documented latitudinal temperature pelagic distribution to a demersal environment following the gradient found along the southern California and Baja California 12e21 d larval period (Margulies, 1989; Donohoe, 1997). Selective peninsula during summer months (e.g. Lynn and Simpson, 1987; mortality of larvae at the higher temperatures found in southern Durazo et al., 2010; Supplementary Fig. 1). Alternatively, the dif- waters late in the spawning season, may explain the lack of adults ferences in the estimates of average temperature could be biased with otolith cores with relatively negative isotope ratios in the Gulf due to variations in the region-specific salinity estimates. The of Ulloa. Unfortunately, there are no ecological studies of white higher temperature found in the GU compared to SC could in fact be seabass larvae or juveniles off the Baja California peninsula. offset by the higher salinity found in more southern waters. How- In summary, the results of this study do not clearly identify the 18 ever, the salinity differed by a maximum of 0.55, which would lead processes that produce the high variability in d Ooto from otolith to a limited impact in back-calculated temperature estimates. cores of adult white seabass. However, the high degree of overlap in 18 18 The predicted range of d O values for each region was calcu- predicted and measured d Ooto values between regions coupled lated based on the full range of local salinity and SST estimates for with the potential for long-distance adult migration indicate that the larval rearing period. A broader range of potential aragonite connectivity among potential subpopulations could occur during precipitation temperatures (including lighter d18O values corre- the adult stage. sponding to warmer temperatures) was predicted for GU than SC and VB; however, there was a high degree of overlap between re- 4.3. Isotopic composition of juvenile otolith growth rings gions. Even though the predicted d18O values for GU included lighter isotope ratios, the isotopic values measured in fish caught in The variation in d13C values of juvenile otolith aragonite be- GU covered roughly the same range as those of SC and VB. This may tween translucent and opaque growth rings may be due to differ- suggest that (1) white seabass have a behavioral preference for ences in the isotopic composition of food sources and changes in more temperate waters and avoid the warmer nearshore temper- metabolic rate; the latter is considered the most important factor atures found in GU late in the summer season, (2) larvae spawned and varies with temperature (Kalish, 1991; Gauldie et al., 1994). toward the end of the season didn't survive, and (3) that the White seabass exhibit significant phenotypic plasticity in terms of spawning period is shorter in GU, and that it occurs prior to the growth rates and size-at-age (Romo-Curiel et al., 2015), suggesting warming of nearshore waters. In addition, the warmer and more that individuals of the same age may have different food sources saline waters found in the southern sampling region yielded a due to size-related feeding preferences, as has been documented similar range of predicted d18O values than the more northern for other sciaenid species (Stickney et al., 1975; Peters and waters that are colder and less saline (Fig. 6). Whatever the cause, McMichael, 1987). The most depleted d13C values were measured the high degree of overlap in the d18O values of otolith cores did not in the growth rings laid down during the summer, when growth allow for discrimination between regions. rates, water temperature, and respiration rates are higher, while the most enriched values corresponded to the winter growth rings, 4.2. Causes driving variability in d13C and d18O of otolith core of when growth and metabolic rates are reduced (Gauldie, 1996; Hoie adults et al., 2003; Portner et al., 2008). This suggests that the relative contribution of metabolically derived carbon to the carbon isotope The predicted regional d18O values calculated from regional ratios of the otoliths may be higher during the summer, a period of temperature and salinity measurements did not yield sufficient increased growth. 18 differences to ensure the conclusive discrimination of larval rearing The linear relationship between carbonate d Ooto values and habitats (i.e., there was a high degree of overlap in predicted oxygen temperature has been used to validate the seasonality of ring 18 isotope ratios). In addition, there was a high variability in d Ooto deposition in otoliths (e.g. Weidman and Millner, 2000). Samples values measured in the cores of adult white seabass collected in SC, taken from the translucent rings (summer growth season) of ju- VB and GU which could be attributed to different causes. Off venile white seabass had the lightest d18O values. Opaque growth southern California, white seabass have a long spawning season rings had more enriched d18O values, consistent with the lower that extends from March to August (Thomas, 1968; Aalbers, 2008); temperatures of the winter season. Similar to other sciaenids, SST increases by around 5 C in SC waters, 6 C in VB and 10 Cin previous age and growth studies of white seabass suggest that this the GU throughout the season. Hence, the mixing of larvae reared at species has an annual ring deposition rate (Romo-Curiel et al., different times during the spawning season could drive the large 2015); however, a rigorous validation of the deposition of annuli 18 13 18 variation in core d Ooto and d C values. Adult white seabass can remained lacking. The clearly seasonal pattern in d O values found migrate relatively long distances to feeding or spawning grounds, in juveniles implies that one opaque and one translucent growth in which case adults may spawn in different regions than those ring is deposited every year, further validating the yearly deposition where they were born (Overstreet, 1983). When otolith samples are assumed by Romo-Curiel et al. (2015). collected opportunistically from adults captured by local fishing There was a significant difference in the isotopic composition of vessels, as was done in this study, it is possible that fish had the first summer growth ring (S0.5) between SC and GU. The ab- migrated from different rearing grounds, contributing to the vari- solute difference in mean d18O values of 0.65‰ is equivalent to a ability in the isotopic composition of otolith cores. In addition, 4 C back-calculated temperature difference. Southern California along protected coastal areas of southern California and Baja Cali- and the Gulf of Ulloa are located toward the northernmost and fornia, temperatures are typically higher in shallower waters than southernmost extent of the distribution of white seabass in Pacific 142 A.E. Romo-Curiel et al. / Estuarine, Coastal and Shelf Science 170 (2016) 134e144 waters, and along a well-documented latitudinal temperature 5. Conclusions gradient (e.g. Lynn and Simpson, 1987; Durazo et al., 2010). Given that in this study the otoliths came from fish collected in SC and GU In conclusion, the isotopic composition of the otolith core of over the course of several years and belonged to different age adult white seabass vary substantially but did not differ sufficiently groups, the significant difference in the d18O values of the first to discriminate between potential subpopulations of larvae reared summer growth ring indicates that there is likely limited mixing in three different potential spawning regions. However, there were between the northernmost and southernmost sampled differences between the oxygen isotopic composition and back- populations. calculated temperature of the first seasonal growth ring of fish captured in SC and GU, suggesting the presence of two potentially discrete subpopulations divided by Punta Eugenia along the central 4.4. Isotopic composition of adult growth rings Baja California peninsula (27N). While seasonal variations in the carbon and oxygen isotopic Acknowledgments composition were evident during the juvenile stage, this was less evident for the growth rings corresponding to the adult stage. We thank the many students and local fishermen involved in Aalbers and Sepulveda (2015) reported that adults tagged in field sampling. Dr. Benjamin Walther (University of Texas, Marine southern California were found at a mean depth of 30 m during the Science Institute) loaned his facilities during processing of the winter, at average temperatures between 13 and 14 C. During the otolith samples on the microdrill. Dr. Dyke Andreasen (University of spring and summer months, these same fish were primarily found California in Santa Cruz, Stable Isotope Laboratory) provided tech- in surface waters at depths of less than 10.5 m, and at mean tem- nical assistance with isotopic analysis. Dr. Reginaldo Durazo (Uni- peratures between 16 and 18 C. Hence, white seabass, like many versidad Autonoma de Baja California, Facultad de Ciencias other pelagic species, may actively select their thermal distribution Marinas) and Drs. Oscar Sosa and Juan Carlos Herguera (CICESE) throughout the year (Morita et al., 2010; Aalbers and Sepulveda, provided helpful comments and suggestions. Mexico's Consejo 2015), which is consistent with the more limited range of isotopic Nacional de Ciencia y Tecnología (CONACyT) provided a graduate values that were measured during the adult stage. In addition, the fellowship to A.E.R.C. Financial support was provided by the George smaller ring widths in adult otoliths may lead to a less recognizable T. Pfleger Foundation and Offield Family Foundation (Project No. seasonal cycle in isotope ratios of carbonate subsamples (Rowell 1.47), and CICESE (Project No. 625116). et al., 2005). Specifically, the absence of a more marked seasonal pattern in the carbon and oxygen isotope ratios of growth rings sampled during the adult stage could also be due to a limitation in Appendix A. Supplementary data the spatial resolution of the milling procedure. The narrowing of the growth rings with age increased the possibility of sampling Supplementary data related to this article can be found at http:// more than one growth season. Lastly, some studies have shown an dx.doi.org/10.1016/j.ecss.2016.01.016. uncoupling between seasonal patterns of ring deposition and growth in adult fishes which could also dampen the seasonal signal References recorded in the isotope ratios of adult stage growth rings (Hoie and Aalbers, S.A., 2008. Seasonal, diel, and lunar spawning periodicities and associated Folkvord, 2006; Sturrock et al., 2015). sound production of white seabass (Atractoscion nobilis). Fish. Bull. 106 (2), 143e151. Aalbers, S.A., Sepulveda, C.A., 2012. 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