ARTICLE

A California Current bomb radiocarbon reference chronology andpetrale sole (Eopsetta jordani) age validationMelissa A. Haltuch, Owen S. Hamel, Kevin R. Piner, Patrick McDonald, Craig R. Kastelle, and John C. Field

Abstract: As petrale sole (Eopsetta jordani) is a valuable groundfish harvested in the California Current, proper ageing isimportant for its assessment and management. This study presents the first bomb radiocarbon reference chronology for theCalifornia Current and petrale sole age validation. Break-and-burn and surface ages are negatively biased by approximately 1 yearand 2–3 years, respectively. The reference and validation curves are more variable and show a lag in the rate of radiocarbonincrease in comparison to most other time series of bomb radiocarbon in marine systems. Upwelling in the California Currentproduces a lagged rate of increase in radiocarbon levels owing to the introduction and mixing of radiocarbon-depleted deepwaters with surface waters that interact with the atmosphere. The variable and lagged rate of radiocarbon increase in the petralesole data may be due to their spending a substantial portion of their first year of life in areas subject to variable upwelling,illustrating the importance of using reference curves for age validation that are region and species specific when possible.

Résumé : La plie de Californie (Eopsetta jordani) étant un poisson de fond de valeur pêché dans le courant de Californie,l'évaluation et la gestion de cette ressource reposent sur la détermination adéquate de l'âge du poisson. L'étude présente lepremier cas de chronologie de référence au radiocarbone dérivé d'explosions pour le CC et de validation de l'âge de plies deCalifornie. Les âges de surface et obtenus par la méthode dite de �� cassé brûlé �� présentent des biais négatifs de l'ordre de 2a 3 ans et 1 an, respectivement. Les courbes de référence et de validation sont plus variables et montrent un retard du tauxd'augmentation du carbone radioactif comparativement a la plupart des autres séries chronologiques produites par analyse duradiocarbone post-bombe dans des systèmes marins. La remontée d'eau dans le CC entraîne un retard de l'augmentation desteneurs en radiocarbone résultant de l'apport d'eaux appauvries en carbone radioactif issues de zones profondes et de leurmélange avec des eaux de surface en contact avec l'atmosphère. Le retard de l'augmentation du radiocarbone et la variabilité dutaux de cette augmentation dont témoignent les données sur la plie de Californie pourraient découler du fait qu'une bonnepartie de la première année de vie est passée dans des zones caractérisées par des variations de la remontée d'eau. Ces résultatssoulignent l'importance d'utiliser, dans la mesure du possible, les courbes de référence propres a la région et a l'espèceconcernées pour valider l'âge des poissons. [Traduit par la Rédaction]

IntroductionPetrale sole (Eopsetta jordani) are right-eyed flounder in the fam-

ily Pleuronectidae that are widely distributed along the west coastof North America from the Bering Sea to Baja California (Charterand Moser 1996). As one of the highest-value groundfish speciesharvested on the USwest coast, petrale sole are almost exclusivelycaught by the bottom-trawl fishing fleet (Haltuch and Hicks 2009;Haltuch et al. 2011). Recent stock assessments (Haltuch and Hicks2009; Haltuch et al. 2011) suggest that petrale sole stock is at lowlevels off the US west coast, resulting in reduced catches. Thedemersal adults prefer soft substrate habitats at depths up to 550m,making them available to bottom-fishing gear. Along the westcoast of the continental US, spawning takes place in well-knownspawning aggregations fromwinter through early spring (Castilloet al. 1994). Both the egg and larvae stages are stenohaline, steno-thermal, and planktonic (Alderdice and Forrester 1971; Charterand Moser 1996) and are present up to 120 km offshore (Pearcyet al. 1977). Juveniles generally settle in the fall on the interconti-nental shelf at depths from 18 to 90 m (Ketchen and Forrester

1966; Pearcy et al. 1977; Castillo et al. 1994). The juvenile distribu-tion of petrale sole is relevant because the otolith core used inbomb radiocarbon analyses represents the environmental condi-tions during the first year of life.

Otolith-derived ages provide informative data in this fisher-ies stock assessment with regards to estimating recruitment,growth, and exploitation rates (Haltuch and Hicks 2009). His-torical petrale sole ages use the otolith surface ageing (SA) tech-nique, although more recently otoliths have been aged usingbreak-and-burn (BB) techniques or a combination of SA and BB.Despite the commercial importance of the species, a comprehen-sive validation study is lacking (Gregory and Jow 1976). Historicalotolith collections that include both juvenile and older fish takenfrom the 1960s through the 1980s are available owing to the longhistory of petrale sole exploitation. The presence of juvenile fishthat can be easily aged in archived commercial catch samples isunique, as such samples provide the first opportunity to constructa bomb radiocarbon reference chronology for the California Cur-rent (CC). These samples are nearly ideal for direct validationof age estimates using the bomb radiocarbon method (Kalish

Received 12 December 2011. Accepted 21 September 2012.

M.A. Haltuch and O.S. Hamel. Fishery Resource Analysis and Monitoring Division, Northwest Fisheries Science Center, National Marine Fisheries Service, NationalOceanic and Atmospheric Administration, 2725 Montlake Boulevard East, Seattle, WA 98112, USA.K.R. Piner. Pacific Islands Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2570 Dole Street, Honolulu, HI96822, USA.P. McDonald. Pacific States Marine Fisheries Commission, Cooperative Ageing Lab, Northwest Fisheries Science Center, 2032 SE OSU Drive, Newport, OR 97365, USA.C.R. Kastelle. Alaska Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 7600 Sand Point Way NE, Seattle,WA, USA.J.C. Field. Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 110 Shaffer Road, Santa Cruz, CA95060, USA.

Corresponding author: Melissa A. Haltuch (e-mail: melissa.haltuch@noaa.gov).

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Can. J. Fish. Aquat. Sci. 70: 22–31 (2013) dx.doi.org/10.1139/cjfas-2011-0504 Published at www.nrcresearchpress.com/cjfas on 16 January 2013.

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1995) for fish older than those used to construct the referencechronology.

The bomb radiocarbon method relies on the rapid increase inradiocarbon (14C) in the environment, due to atmospheric testingof thermonuclear devices, as a dated marker. The method is con-ditioned on obtaining otolith samples from fish spawned duringthe period of radiocarbon increase in the marine environment,typically the late 1950s to the late 1960s (Nydal 2000). Fish otolithsare carbonate structures that accumulate 14C, making it possibleto use the 14C as a timemarker for comparing otolith core samples(representing the birth year) to a reference chronology of theexpected levels of radiocarbon in the system (Kalish 1995;Campana and Jones 1998; Piner and Wischniowski 2004). Bombradiocarbon validation is considered one of the most effectiveways to validate fish ages (Campana 2001; Kastelle et al. 2008), butits assumptions include a biological and environmental referencechronology representative of the fish species being validated, i.e.,a single rearing region or location for a given fish species, and thatonce deposited, carbonate material is inert (Hamel et al. 2008;Kastelle et al. 2008). While often not available, ideally a referencechronology of dissolved inorganic carbon (Kalish et al. 2001) or aconspecific reference chronology for species that are not seden-tary (Campana 1997; Piner and Wischniowski 2004) is used.

Our objectives in this study were to complete three tasks usinghistorical petrale sole otolith samples: (i) to construct the firstbomb radiocarbon reference chronology for the CC using a set ofjuvenile petrale sole otoliths (generally aged ≤5 years) collectedbetween the late 1950s to the late 1980s; (ii) to compare the CCreference chronology against a test chronology made up of olderpetrale sole to provide age validation of both SA and BB ages; and(iii) to investigate the relationship between the increase in thebomb radiocarbon from reference chronology data and upwellingin the CC to provide insight into the characteristics of bomb ra-diocarbon data from upwelling systems.

Materials and methods

Sample selection and ageingA total of 346 petrale sole otolith pairs stored in dry paper

envelopes were retrieved from the Southwest Fisheries ScienceCenter (Santa Cruz, California) for potential inclusion in the bombradiocarbon analysis. Only samples that could be matched withtheir original data records and that had both eyed and blind-sideotoliths were selected from the limited number of archived sam-ples. The otoliths were collected from commercial fishery samplesfor which multiple vessels were sampled in each port between1959 and 1987. A majority of the samples were from female fish,although a few of the samples from the earliest years used for thereference curve were either males or of unknown sex. Most sam-ples were selected from the northern California ports of Eureka,Fort Bragg, San Francisco, and Monterey (ERK, BRG, OSF, MNT,respectively), while a few samples were sampled in unknown Cal-ifornia ports (Fig. 1). Prior to being aged the otoliths were hydratedby soaking in water for 24 h. The otoliths were then surface-agedby submersing them in a dish of water and counting the annuliunder a Leica MZ9.5 dissecting microscope. Observations for SAwere performed at a magnification of up to 16× (Fig. 2). A BB ageestimate was obtained by breaking the blind-side otolith throughthe nucleus and toasting the anterior portion over an ethanolflame. The annuli visible on the BB otoliths were then countedunder the same dissecting scope at magnifications of up to 25×(Fig. 2). The dorsal and ventral “wing-tips” were both examined todetermine a final age estimate. Two age readers produced both SAand BB ages for all otoliths, providing four age estimates for eachset of otoliths.

A total of 37 samples were selected from the original data set of346 surface- and break-and-burn-aged otoliths for the CC referencechronology bomb radiocarbon analysis (Fig. 3). These samples

encompassed years expected to show bomb radiocarbon increase,as well as the years immediately preceding (early to mid-1950s)and following (generally from the 1970s onward) the period ofincrease. Known-age fish were used for reference chronologieswhen available. However, petrale sole samples from the CC con-sist of young otoliths that are as close to known age as possible,suggesting that ageing inaccuracies are likely to be of small mag-nitude. Thirty-four petrale sole otoliths aged between 3 and 5years with clear annuli and complete age agreement betweenboth ageing method and age reader were selected for inclusion inthe reference chronology (Fig. 3). Stratified random samplingwithin each year was used to select the final samples for radiocar-bon analysis. Given the age agreement between two ageing meth-ods and two independent age readers, these samples were treatedas known-age fish for the reference chronology. Three of the sam-ples collected during 1959 (ages 6, 8, and 9 years) were used toestimate the prebomb radiocarbon levels between 1950 and 1953.

A final test set of 39 otoliths collected during 1961–1987 with BBage estimates of at least 6 years were selected from the original346 aged otoliths for the petrale sole age validation. Otoliths wereselected based on a stratified random sample, within birth year,based on BB age.

Bomb radiocarbon analysisA 1-year core from the first year of life could be reliably ex-

tracted from either the eyed or blind-side otolith, as the firstannulus and cores of both were easily identifiable. Surface exam-

Fig. 1. Map of ports where petrale sole were landed and otolithswere sampled in California, USA. The abbreviations ERK, BRG, SF,and MNT are the ports of Eureka, Fort Bragg, San Francisco, andMonterey, respectively.

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ination of the otoliths suggested that core length and width weresimilar between the eyed and blind sides, allowing a minimum of2 mg of carbonate material to be obtained from either otolith. Atransverse section of each otolith that approximated the core wasremoved using a Buehler low-speed isomet saw. Additional mate-rial beyond the first annulus, not removed by sectioning, wasremoved using a variable speed Dremel drill and a variable-speedlapping wheel with 220-grit sandpaper. Both the sandpaper andDremel tip were changed for each otolith to prevent cross-contamination. An iterative process of otolith material removaland subsequent verification of the coring progress under micro-scopic examination was used to produce the final core.

Final otolith cores were cleaned in an ultrasonic bath, dried,and packaged in glass vials before being transported to the Na-tional Ocean Sciences Accelerator (NOAA) Mass Spectrometry fa-cility located at the Woods Hole Oceanographic Institute (WoodsHole, Mass., USA) for analysis. Bomb radiocarbon dating includeshydrolysis of the otolith in phosphoric acid to produce CO2, whichis turned into graphite using heat in a vacuum and then pressedinto a target for �14C and �C13 assays. The reported values werecalculated following the conventions of Stuiver and Polach (1977).

California Current reference chronology and age validationA quantitative analytical method recently published as an im-

proved way of estimating the level of ageing error using bombradiocarbon data as the model is capable of fitting both the in-crease and decrease in radiocarbon observed in many time series(Hamel et al. 2008). This method was applied to the US west coastpetrale sole radiocarbon data. The deterministic coupled-functions model developed by Hamel et al. (2008) was used todescribe the increase in radiocarbon levels due to the atmospherictesting of thermonuclear devices in petrale sole otoliths from theCC. The Hamel et al. (2008) method models the pulse of radiocar-bon from nuclear testing as a Gaussian curve over time coupledwith a continuous exponential decay process that represents thediffusion and dispersal of the radiocarbon to different layers ofthe ocean, not radioactive decay (at least not to a significant de-gree), and is given by

(1) y(t) � ymin � k er(��t) ��2r2

2 �(� � �2r,�, t)

where y is the estimated �14C, t is time in years, ymin is the initial�14C that accounts for naturally occurring background 14C, k is ascalar for the total input magnitude of radiocarbon due to atmo-

Fig. 2. Images of a whole otolith that was surface read at 16×magnification (a) and broken-and-burned otolith at 25×magnification (b) with growth increments marked as points.

Fig. 3. The petrale sole California Current bomb radiocarbon, �14C,reference chronology data collected in San Francisco (filled points),Eureka (open circles), Fort Bragg (open squares), and unknown ports(open upward facing triangles) with the model fitted referencechronology (bold black line) (a). A comparison of the petrale solereference chronology (San Francisco (filled points), Eureka (opencircles), Fort Bragg (open squares), and unknown ports (openupward facing triangles)), and Pacific halibut bomb radiocarbondata (open downward facing triangles), fitted reference chronologies(petrale sole, all data: bold black line; halibut: dashed line), and thepetrale sole reference chronology fitted without the data from FortBragg (thin black line) (b). The normalized reference chronologiesfor straight forward comparison for Pacific halibut samples (opentriangles) and model fit (dashed line) and the petrale sole samples(solid circles) and model fit (bold black line) (c).

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spheric testing of thermonuclear devices (in units of �14C), r is anexponential decay rate per year, � represents the point at which50% of the radiocarbon input occurred, and � represents the cu-mulative normal function with a mean year, � + �2r, and a stan-dard deviation in years, �. Equation 1 was fitted to a data set vianumerical optimization by assuming a normal error structure forthe �14C value around the curve using ADModel Builder to obtainmaximum likelihood estimates for the parameters k, �, �, and r(Hamel et al. 2008). Themodel assumes that all (random) error andvariation was in the �14C values, not in the otolith ages (while biasin ageing for the test series affects the values of the parameters,particularly �). The model estimated the timing and pattern ofincrease in �14C given both the reference and test data series,allowing the estimation of bias and variability in ageing (Hamelet al. 2008).

Themodel consistently fits bomb radiocarbon chronologies rea-sonably well as evidenced in Hamel et al. (2008), Cook et al. (2009),and Friess and Sedberry (2011). Tests analogous to two-samplet tests were used to compare values of � (with all other parametersfixed) between the reference and test chronologies. The t tests andage bias plots comparingmethods and reader differences using allthe age data are provided (Campana 1995). Model sensitivity toport of landing and age groups are presented for the referencechronology and the test samples, respectively. Z scores, with amean of zero and a standard deviation of 1, for the petrale refer-ence chronology and the Pacific halibut reference chronologyfrom the Gulf of Alaska are calculated to make these data setscomparable.

Upwelling analysesThe relationship between upwelling in the CC and the in-

crease in bomb radiocarbon in the reference data were com-pared with the mean May to October coastal upwelling indexacross 3° of latitude centered at 39°N and 125°W (downloadedfrom the Pacific Fisheries Environmental Laboratory Live Ac-cess Server; Fig. 4), the approximate region where the otolithswere collected. The coastal upwelling index is an index of thestrength of the wind forcing on the ocean across large spatialscales. Differences in upwelling dynamics provided a hypothesisthat could explain differences between the petrale sole and Pacifichalibut reference chronologies. The petrale reference chronologydata were from the CC, a wind-driven upwelling system, while thePacific halibut data were from the Gulf of Alaska, a shelf ecosys-tem that has less upwelling (Fig. 1). Linear models were used toinvestigate the ability of the coastal upwelling index to explaindifferences between the petrale sole reference chronology dataand Pacific halibut reference chronology model fit across threetime periods: 1950–1959, 1961–1969, and 1970–1985. The first pe-riod encompasses years inwhich radiocarbonwas considered gen-erally well mixed between the surface waters and upwellingwaters in the CC, while the second period encompasses yearswhen radiocarbon was increasing in both the CC and the Gulf of

Alaska. The third period includes the years when radiocarbonlevels in the Gulf of Alaska plateaued and the rate of radiocarbonincrease in the petrale sole data slowed.

Results

California Current reference chronologyThe 37 CC reference chronology samples were approximately

equally distributed between the ports of Eureka (n = 11), Fort Bragg(n = 11), and San Francisco (n = 11), with a few early samples fromunknown ports (n = 4) (Fig. 3). Exploring the distribution of sam-ples across ports and 5-year time periods indicated that moresamples were available from the northern ports of Eureka andFort Bragg after 1974, while no samples were available from SanFrancisco after 1980. All the samples were from female fish, ex-cept for two male samples and one unsexed sample. Total lengthof fish ranged from 204 to 444 cm, with a mean length of 333 cm.The mean length of fish sampled in San Francisco was greatestover the entire time period (358 mm), followed by the ports ofEureka (336 mm) and Fort Bragg (300 mm). The mean size of fishdeclined over time from 402 mm in 1955–1964 to 289 mm after1985, consistent with a similar pattern of decreasing mean age.Three samples were older than 5 years, while 5, 12, and 17 sampleswere 3, 4, and 5 years old, respectively.

In the CC reference chronology, prebomb levels of radiocarbon(� – � from Table 1a) had a minimum value of –110.2‰ (ymin fromTable 1a, Fig. 3a). Radiocarbon levels begin increasing during thelate 1950s through the end of the time series during the late 1980s,and the rate of increase slows from the late 1970s forward (Fig. 3a).The estimated mean year of radiocarbon increase, �, was 1966.6,and the standard deviation, �, of the cumulative normal functionwas 8.2 years, indicating a prolonged period of radiocarbon in-crease (Table 1a, Fig. 3a). The rate of radiocarbon increase declinedafter themid-1970s with the postbomb high value of 53.8‰ occur-ring in 1983 (Fig. 3a). The within-year variability in radiocarbonvalues was high, particularly for samples spawned in 1971 and1973 and collected at Fort Bragg in 1976 (Table 1b, Figs. 3a and 3b).Removing the Fort Bragg samples from the reference chronologyreduces the standard deviation, �, of the cumulative normal func-tion from 8.2 to 6.0 years when using all the data (Table 1b, Fig. 3b).Removing the data from the ports of Eureka and San Franciscoproduced smaller changes in �, suggesting that the data from FortBragg were the primary contributor to the high estimate of �. The� and � from the normalized petrale sole reference chronologywere later and larger, respectively, in comparison to those fromthe Pacific halibut (Fig. 3c).

Age validationA majority of the 39 test samples were collected at Fort Bragg

(n = 23), an approximately equal number of samples were from Eu-reka (n = 7) and Monterey (n = 6), a few samples were from SanFrancisco (n = 2), and 1 sample was from an unknown port. Totallength ranged from 360 to 578 cm, with a mean fish length of506 cm. All estimated ages were at least 4 years using SA and 6 yearsusing BB, while only five samples were estimated to be less than 8years of age. The median ages were 11–12 years old, and the maxi-mum ages were 20–31 years old, depending on the ageing method.Test samples with birth years prior to 1956 and after 1979 were lack-ing (Figs. 5 and 6), so the k, ymin, and � parameters were fixed at thereference data estimates (Table 1a) to anchor the base, peak, andrate of increase of the test curves. This allowed for a direct com-parison of the � parameters between the CC reference chronologyand the petrale sole test data. This was similar to the validationpresented in Piner et al. (2006) using a simple logistic fit to theradiocarbon data. Radiocarbon levels increased rapidly from 1961to 1979 and from 1961 to 1978 for the SA and BB samples, respec-tively (Fig. 5). The estimatedmean year of radiocarbon increase, �,in the SA and BB test samples was 1969 and 1968, respectively

Fig. 4. The average May to October coastal upwelling index across 3degrees of latitude centered at 39 degrees north and 125 degreeswest.

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Table 1. Parameters (standard errors in parentheses) andderived quantities from the coupled functionmodel fits for the petrale sole reference and testdata sets as well as the Pacific halibut reference data (a) and model sensitivity runs (b).

(a) Reference and test data sets.

k (‰) � (year) � � – � (year) ymin (‰) yasym (‰)

Reference chronology 149.2 (7.4) 1966.6 (0.80) 8.2 (1.0) 1958.4 (1.65) −110.2 38.98Pacific halibut 247.5 (16.9) 1962.4 (0.31) 3.1 (0.3) 1959.3 (0.55) −129.6 117.87Test dataS (All) 149.2 1968.5 (0.35) 8.2 1960.3 (0.69) −110.2 38.98S (#1) 149.2 1968.3 (0.49) 8.2 1960.1 (0.55) −110.2 38.98S (#2) 149.2 1968.8 (0.50) 8.2 1960.6 (0.54) −110.2 38.98BB (All) 149.2 1967.5 (0.22) 8.2 1959.3 (0.82) −110.2 38.98BB (#1) 149.2 1966.8 (0.28) 8.2 1958.6 (0.76) −110.2 38.98BB (#2) 149.2 1968.1 (0.31) 8.2 1959.9 (0.73) −110.2 38.98

(b) Model sensitivity runs and comparison between the petrale sole and Pacific halibut.

k (‰) � (year) � � – � (year) ymin(‰) yasym(‰)

Reference chronology 149.2 (7.4) 1966.6 (0.80) 8.2 (1.04) 1958.4 (1.65) −110.2 38.98Reference sensitivitiesNo Eureka 161.7 (12.3) 1968.4 (1.30) 9.4 (1.32) 1959.0 (2.45) −110.2 51.54No Fort Bragg 135.6 (4.9) 1965.3 (0.43) 6.0 (0.81) 1959.3 (1.04) −110.2 25.43No OSF 141.9 (8.4) 1966.9 (1.02) 7.8 (1.31) 1959.1 (2.01) −104.0 37.88

Test data sensitivitiesBB #1 test age < 12 149.2 1967.3 (0.18) 8.2 1959.1 (0.86) −110.2 38.98BB #1 test age ≥ 12 149.2 1967.7 (0.40) 8.2 1959.5 (0.64) −110.2 38.98

Note:When all other parameters are fixed at their estimated values, the standard error on � is reduced to 0.44, this value is used in the statistical tests. Parametersare the total radiocarbon input (k), mean year of increase (�), the standard deviation of the cumulative normal (�), the estimated timing of initial radiocarbon increase(� – �), the minimum observed radiocarbon level (ymin), the maximum radiocarbon level (estimated by the cumulative normal) that would have occurred in theabsence of r (yasym). The value ymin is an observation and does not have an error estimate from the coupled functions model. The parameters k and yasym (defined asymin + k) necessarily have the same standard deviation. The exponential decay rate (r) was 0 for all model runs. All parameters are estimated for the reference data. Thetest data k and � are fixed at the same values as those estimated for the reference data.

Fig. 5. The bomb radiocarbon, �14C, chronologies used to validate the assumption that there was no aging bias for petrale sole. The coupledfunction model fit from the reference curve (bold black line) is compared with the surface read (open squares, dashed grey line) and breakand burn (solid circle, thin black line) aging methods. Data for both age readers is plotted.

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Fig. 6. The bomb radiocarbon, �14C, chronologies used to validate the assumption that there is no aging bias for petrale sole. The coupledfunction model fit from the reference curve (bold black line) is compared with the ages from reader 1 (black line, solid circles) and reader 2(grey line, open squares) for each aging method, break and burn (a) and surface read (b). Note that the reader 1 line is obscured by thereference curve line in panel a.

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(Table 1a; Fig. 5). The standard deviation of the cumulative normalfunction for both the SA and BB samples was fixed at 8.2 years, theestimate from the reference data (Table 1a, Fig. 5), indicating aprolonged period of radiocarbon increase. The postbomb high

value of 23.5‰ occurred in 1980 (Fig. 5), and the within-year vari-ability in radiocarbon during the period of increase was high,similar to the CC reference chronology observations (Fig. 5). Incomparison to the reference chronology, the SA data from reader1 was negatively biased by 1.6 years (p < 0.01, two-sample t test),reader 2 was negatively biased by 2.2 years (p < 0.001), and thecombined reader ages were negatively biased by 1.9 years(p < 0.001) (Table 1a; Figs. 5 and 6). In comparison to the referencechronology, the BB data from reader 1 was unbiased (0.1 yearnegative bias, p = 0.4), reader 2 was negatively biased by 1.5 years(p < 0.01), and the combined reader ages were negatively biased by0.8 years (p < 0.05) (Table 1; Figs. 5 and 6). Matched pair compari-sons and age bias plots (Fig. 7) using all aged otolith samplesyielded similar results to the above for BB versus SA (p < 7.38 ×10–9, one way t test) and the between-reader differences for SA(p < 0.001, two-way t test) and BB (p < 8.73 × 10–11, two-way t test)data. However, the age bias plots show that the SA and BB ageingmethods differ across age, whereby BB ages are 1–2 years greaterthan the SA ages until approximately age 10, after which thenegative bias in SA increases rapidly and SA is unable to produceaccurate ages beyond approximately age 14 (Fig. 7a). Nearly iden-tical results were achieved for analyses done using the referencecurve without data from Fort Bragg. Test sensitivity model runs toinvestigate possible differences in ageing bias between younger(<12 years) and older (≥12 years) fish found a small and non-significant difference in bias between the two groups (0.4 years,p = 0.2; Table 1b).

Upwelling analysesDuring the period in which radiocarbon was well mixed in

the CC (1950–1958) and the period when the difference betweenthe Pacific halibut and petrale sole was smaller (1970–1985), thecoastal upwelling index did not explain the difference betweenthe petrale sole reference chronology and the Pacific halibutreference chronology (1950–1959: F[1,8] = 0.1995, p = 0.667, ad-justed R2 = −0.098; 1970–1985: F[1,15] = 0.0017, p = 0.968, adjustedR2 = −0.067) (Figs. 8a and 8c). In contrast, the coastal upwellingindex did explainmuch of the difference between the petrale solereference chronology and the Pacific halibut reference chronol-ogy during the 1960s, when the rate of radiocarbon increase isgreatest (F[1,8] = 17.67, p = 0.003, adjusted R2 = 0.649), suggestingthat upwelled radiocarbon-poor waters dilute radiocarbon levelsin the CC (Fig. 8b).

Discussion

Age validationThis study has successfully evaluated otolith ageing methods

routinely applied to petrale sole for fisheries research and stockassessment. There is a small negative ageing bias that occurs atapproximately age 5, the age at 50%maturity, or older for both theSA and BB methods. Given that the model-based analyses are notdesigned to evaluate ageing bias across ages, the age bias plots actas a complementary tool to the overall accuracy test provided bythe models. The strong negative bias for SA reads older than ap-proximately age 14 suggest that SA data need to either be cor-rected for this ageing error during the stock assessment process or(preferably) SA samples need to be re-aged using the BB method.The negative biases from the BB method and for younger SA sam-ples are not significant impediments to the use of petrale sole agedata. The larger SA bias is expected based on the otolith morpho-logical changes that occur around age 10, when otoliths appear togrow more in the proximal–distal axis, potentially masking an-nuli when using SA. The demonstrated ageing bias is applicable tohistorical petrale sole ages, as the ageing methods applied in thisstudy are the standardmethods used to produce age estimates forthe petrale sole stock assessment. It is not necessary to assumethat the reference chronology is measured without ageing error

Fig. 7. Age bias plots with 95% confidence intervals showing thebias between the BB and SR ages (a), the between reader SR ages (b),and the between reader BB ages (c).

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for this comparison, as a bias is demonstrated between the pri-marily juvenile fish used for the reference chronology and theprimarily adult fish used for the test data. However, the relativeease of age assignment at young ages (<7 years) and good agree-ment between ageing methods and readers argues that the refer-ence chronology is a reasonable depiction of the change inradiocarbon levels for this area of the CC.

California Current reference chronologyThis is the first bomb radiocarbon reference chronology for

both the CC and for an eastern boundary current ecosystem usingwhat can be reasonably assumed to be known-age samples. Theonset of the radiocarbon increase is consistent with those of othernorthern hemisphere chronologies (e.g., Hamel et al. 2008; Cooket al. 2009) as well as those from other upwelling ecosystems(Druffel 1981; Druffel 1987; Druffel 1991). In comparison to manyprevious studies (Campana 1997; Piner and Wischniowski 2004;Hamel et al. 2008), the CC reference chronology derived frompetrale sole otoliths is more variable and has a notable lag in therate of radiocarbon increase during what is generally consideredto be the period of bomb radiocarbon increase, and may not havereached an asymptote. However, a previous bomb reference curvefrom the Eastern Arctic – Northwest Atlantic Greenland halibuthas a similar lag in the rate of radiocarbon increase, a depletedmaximum, and variability at given year classes (Treble et al. 2008).The same patterns are also apparent in the bomb radiocarbontime series from the Galapagos Islands, also an upwelling system(Druffel 1981; Druffel 1987; Druffel 1991). The midpoint of thepetrale sole increase is delayed by 4–5 years, and the length of theperiod of increase is about twice as long as chronologies publishedby Hamel et al. (2008). The Pacific halibut reference chronologyfrom the northeast Pacific has a � near 1962 and � between 3 and4 years (Hamel et al. 2008); these differences with the petrale solereference chronology are more easily identified by plotting nor-malized data andmodel fits. Themaximum observed radiocarbonlevel is lower and variability for a given birth year is greater thanthat seen in any of the species considered by Hamel et al. (2008).Upwelling is a local event that can vary in different locationsalong the CC; fishing in different locations (i.e., ports) may lead tosampling fish that experienced different upwelling conditionsduring the first year of life, thus explaining the high variability inthe petrale sole radiocarbon data. Furthermore, the expectation isthatmost of this variability is due to the upwelling of radiocarbon-poor waters (Druffel 1991), so that most of the outliers could beexpected to fall below the fitted curve, such as the petrale solereference data points from Fort Bragg during the early 1970s.Bomb radiocarbon results from other studies conducted in the CC— canary rockfish off of Oregon (Piner et al. 2005), juvenile rock-fish off of California (Rau et al. 2001), and biological samples off ofBaja California (Druffel 1991) — report maximum observed radio-carbon values similar to those from the petrale sole off of Califor-nia. Rau et al. (2001) used data collected during the mid-1990s,approximately 10 years later than the petrale sole data, and re-ported �14C values ranging from approximately 22 to 60. By com-parison, petrale sole �14C values from the 1980s samples rangefrom 21 to 54, suggesting that levels of bomb radiocarbon in theCC may have stabilized at an upper limit during the 1980s and1990s. Similar maximum observed radiocarbon values for boththe petrale sole and canary rockfish data sets suggest that theseCC data sets come from a much different coastal upwelling envi-ronment than reference chronologies developed from other eco-systems along the west coast of the United States and Canada. TheOregon canary rockfish age validation uses the northeast Pacifichalibut reference chronology (Piner et al. 2005). However, thisstudy suggests that it may be necessary to revisit the canary rock-fish age validation using the CC reference chronology developedfrom petrale sole, as this reference chronology is likely more en-vironmentally representative of the canary rockfish distribution.

Fig. 8. Data and linear model fits showing the relationship betweenthe annual and spatial (3 degree) average May to October upwellingcentered at 39 degrees north and the difference between the petralesole reference chronology data and the fitted halibut referencechronology. The lack of significant relationships during the 1950–1959 period (a) and 1970–1985 period (c) in which radiocarbon wasgenerally well mixed in the CC and the rate of radiocarbon increaseslowed, respectively, are contrasted with the significant relationshipduring 1961–1969, the period of rapid radiocarbon increase (b).

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The extended period of the radiocarbon increase, the lowermaximum radiocarbon level, the higher variability, and the po-tential continuing rise of bomb radiocarbon beyond the 1980s areall likely related to the dynamics of the CC, an eastern boundarycurrent system exhibiting wind-driven upwelling (Druffel 1987,1991; Masiello et al. 1998). The strongest upwelling typically occursduring the spring and summer months, coinciding with the pe-lagic period of petrale sole larvae and juveniles. The petrale solepelagic larval stage spans about 6 months, from approximatelyDecember to June, after which larvae settle to the benthos. Whilelarvae can be found far (up to 150 km) offshore (Casillas et al. 1998),in the upper 50 m of the water column (Starr and Fargo 2004),pelagic petrale sole juveniles move inshore and settle to the ben-thos on the intercontinental shelf (Ketchen and Forrester 1966;Pearcy et al. 1977; Castillo et al. 1994). Cold, deep upwelling watersmix with surface layers during upwelling events. Therefore, theradiocarbon created by atmospheric nuclear testing in surfacewaters would take longer to reach deep upwelling waters duringand after the period of radiocarbon increase in the atmosphereand surface waters, producing a radiocarbon signature in the CCthat is diluted by the mixing of surface radiocarbon-rich waterswith deeper radiocarbon-poor waters (Druffel 1987, 1991; Masielloet al. 1998). Radiocarbon in surface and deep upwelled waterscould be assumed to be relatively well mixed during the prebombperiod and after the rate of fastest increase, during the 1960s and1970s. Rau et al. (2001) found that �14C levels in surface-dwellingjuvenile rockfish changed with variable upwelling conditionsalong the coast of California, suggesting that the more variableand slower rate of radiocarbon increase in the petrale sole refer-ence chronology may be due to petrale sole being subject to vari-able strong upwelling events. As expected, the coastal upwellingindex has considerable explanatory power that can account fordifferences between the petrale sole and Pacific halibut referencechronologies during the period of fastest radiocarbon increase.This conclusion is supported by the lack of a significant relation-ship outside this period of radiocarbon increase.

Alternative hypotheses to upwelling dynamics that could ex-plain the lagged increase of bomb radiocarbon in the petrale solereference chronology are that trends in the data over time orspace may have influenced the shape of the fitted curve. First,changes in environmental conditions from south to north mayhave impacted the reference data. The ports of Fort Bragg and SanFrancisco are both in the same commonly recognized biogeo-graphic region, south of Cape Mendocino and north of Point Con-ception (Cope and Haltuch 2012), while the port of Eureka is nearCape Mendocino. A priori one would expect that if samples fromone port were going to be different than the others, Eureka wouldbe the one to stand out. However, in these environmentally dif-ferent areas, Eureka and Fort Bragg port samples are similar, sug-gesting that environmental differences from north to south didnot impact the �14C values from the reference data. Second, age-ing differences between fish from the northern and southernports can be discounted, as all of the samples were aged at thesame time by the same lab. Third, spatial trends in growth orfishing pressure may explain the larger fish from San Francisco.Previous investigations of spatially divergent and time-varyinggrowth have not found strong patterns (Haltuch and Hicks 2009).However, fishing pressure increased during the 1950s to 1980s, at thesame time that the fishing fleet moved from south to north, provid-ing an explanation for the larger, older fish from San Francisco inearlier years. While small sample sizes and the lack of spatially ex-plicit catch data prevent the investigation of changes in size-at-ageover time for each port with these data, larger mean fish size andolder ages in all ports from 1955 to 1974, when the size and ageselective impacts of fishing would have been less, suggest thatchanges in size over time are due to fishing pressure.

The importance of using region-specific reference curves ishighlighted given that the petrale sole reference chronology var-ies from reference curves in other ecosystems, such as the Pacifichalibut chronology from the north Pacific (Piner and Wischniowski2004), and is similar to data collected in other upwelling systems(Druffel 1981, 1987, 1991). Furthermore, reference chronologiesused in age validation studies should ideally be from the samespecies or at a minimum should be from a species with a similarearly life history with regards to location of rearing, as noted byCampana et al. (2008). In this case the reference and test data areregion and species specific, alleviating the need to assume thatthe functional form of the 14C chronologies are the same. Giventhe high level of variable upwelling and radiocarbon levels indifferent regions of the CC (Druffel 1991; Masiello et al. 1998), theCC petrale sole reference chronology could be used for age valida-tion of additional CC species with samples from the same regionand similar early life histories to petrale sole.

AcknowledgmentsThanks to Alec MacCall and Don Pearson for help with access-

ing the samples. Reviews from Ian Taylor, Curt Whitmire, IngridSpies, Vlada Gertseva, Jim Hastie, and two anonymous reviewersgreatly improved this manuscript.

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