Black rockfish (Sebastes melanops) range from California to Alaska and are found in both nearshore and shallow continental shelf waters (Love et al., 2002). Juveniles and subadults inhabit shallow water, moving deeper as they grow. Generally, adults are found at depths shallower than 55 meters and reportedly live up to 50 years. The species is currently managed by using information from an age-structured stock assessment model (Ralston and Dick, 2003).
In many studies, ages are assumed to be accurate and there is no effort to validate the accuracy of the ages (Beamish and McFarlane, 1983). Recent methods of age validation rely upon environmental events that serve as time markers (Campana, 2001). Bomb radiocarbon released during nuclear bomb testing has been used to validate fish ages (Kalish et al., 1996; Campana, 1997; Kalish et al., 1997). Unfortunately, bomb radiocarbon can be used only for fish that lived during the informative period (~1960-70); thus the technique has been used primarily on older ages. For many stock assessments, the validation of younger ages is more critical because of their importance in estimating vital rates, such as growth and maturity schedules.
In this note we apply the well-studied relationship between water temperature and the ratio of oxygen stable isotopes in otoliths to assess the accuracy of young black rockfish ages. Oxygen isotope ratios serve as a record of past water temperatures because the isotope ratio is incorporated into the otolith in near equilibrium with the ratio found in the environment (Patterson et al., 1993; Thorrold et al., 1997) and ambient water temperatures are inversely correlated with [sup.18]O/[sup.16]O ratios (Gao et al., 2001). Calcified structures have a strong history of being used in environmental reconstructions based on incorporated trace elements and isotopes (Chivas et al., 1985; Holmden et al., 1997). Otolith microchemistry has been used to successfully reconstruct the environmental history of fish and to answer questions about natal homing (Thorrold et al., 2001) and population mixing (Campana et al., 1999). Variation in oxygen isotopes has been used to confirm visually observed growth increments (Campana, 2001). Recently, stable oxygen isotopes from Pacific halibut (Hippoglossus stenolepis) otoliths were used to examine regime shifts in the Northeast Pacific for the identification of changes in bottom water temperatures (Gao and Beamish, 2003). In addition, otolith chemistry may be used to identify environmental events that serve as natural tags for such studies (Campana and Thortold, 2001). We used a strong regional environmental event, the 1983 El Nino, as a time marker to judge the accuracy of age assignment for black rockfish <15 years of age. The 1983 El Nino produced anomalously warm oceanic conditions along the coastlines in the eastern Pacific; therefore the stable oxygen isotope ratio from 1983 should reflect this change in oceanic conditions.
Materials and methods
We obtained nine pre-aged black rockfish otoliths collected during 1987-91 from recreationally caught fish off Cape Lookout, Oregon (~45.25[degrees]N, 145[degrees]W), from approximately 15-30 m water depth. One otolith was aged by Oregon Department of Fish and Wildlife scientists by using the traditional break-and-burn method; the matching otolith was used in the stable isotope analysis. Fish from a range of years and ages (Table 1) were selected to include the 1983 El Nino year. A time series of annual summer bottom water temperatures from the same region and depth where the black rockfish otolith samples were obtained, were provided by the Pacific Hindcast from the Columbia University International Research Institute for Climate Prediction, Palisades, New York.
To estimate the year containing the warmest oceanic conditions, we examined otolith material from all opaque growth zones within each otolith for oxygen isotopes ([sup.18]O/[sup.16]O) and assigned to a year of formation based on estimated age and capture year. Chemical assay and otolith processing were completed at the Stable Isotope Laboratory of the University of Michigan. Each otolith was embedded in epoxy resin and cut transversally with a low-speed diamond-bladed saw. Three or four thin sections ~150 [micro]m thick were removed from the center of each otolith. The thin sections were then glued with cyanoacrilate glue to petrographic glass slides. Samples from multiple thin sections were combined for a single assay. Each opaque growth zone was sampled by using a Merchantek Micromilling system and assays were completed with a Finnigan 251 MAT mass spectrometer. All measurements were reported in standard Vienna Pee Dee Belemnite (VPDB) and notation as [differential][per thousand] (per mil), where
[[differential].sup.18]O=((([sup.18]O/[sup.16]O).sub.sample]/ [([sup.18]O/[sup.16]O).sub.standard]) - 1 x 1000).
A time series of [[differential].sup.18]O was constructed for each fish by using the assay from each year-specific sample of the otolith material. Assay results from the collection year were not included because of differences in the season of capture. Years with missing results were due to micromilling or assay errors that resulted in no results reported by the stable isotope laboratory.
To gauge the accuracy of age assignments, we fitted a linear model to each time series and analyzed the residuals from the linear model fit. The [[differential].sup.18]O value corresponding to the negative residual of greatest magnitude from that linear model would be associated with the anomalously warmest oceanic conditions (El Nino). If the age assignments were correct, that portion of the otolith corresponding to 1983 would have the negative residual of greatest magnitude because the observed [[differential].sup.18]O value was much lower than the linear model predicted. Temporal shifts of the most anomalous negative residual with respect to 1983 were interpreted as either an under- or over-estimation of age.
A randomization procedure (20,000 iterations) was used to determine if the magnitude of the average residual in any year was more negative than expected, thus identifying the signal associated with the 1983 El Nino. The residuals from the linear models within each of the fish were randomized with respect to year. Randomized residuals from all iterations were averaged across all fish to produce a distribution of averages. The original year-specific residual averages were compared to the randomization distribution to estimate statistical significance. We rejected the hypothesis of any year with an average residual [greater than or equal to] 0 if less than 5% of the randomizations produced a negative average residual of equal or greater magnitude than the observed year-specific average residual, thus identifying anomalously warm years.
An iterative sensitivity analysis was performed by retrospectively removing sequential blocks of years of data and by estimating the statistical significance of the originally determined anomalous years with the reduced data sets. All data taken from years more recent that the cutoff year were removed, and the linear model fitting and randomization procedures were recalculated. The cutoff year was sequentially changed beginning with 1989 to 1986.
Results
The period 1980-90 was characterized by an isolated and historically strong 1983 El Nino event (Fig. 1), that resulted in a 1-2[degrees]C increase in water temperatures along the Oregon coast. Average summer water temperatures declined slightly over this period. The [[differential].sup.18]O values measured in each fish resulting from this period (Table 1) showed strong patterns that indicated temperature differences both within fish (between years) and between fish (same year). In addition, many fish contained trends in [[differential].sup.18]O across time (Fig. 2). Precision of the reported [[differential].sup.18]O measurements ranged from 0.01 to 0.07[per thousand] (SD).
[FIGURES 1-2 OMITTED]
The residual patterns (Fig. 3A) showed that anomalously warm conditions existed in otolith material corresponding to those of 1983 (n=9, P=0.0338) and 1985 (n=7, P=0.0409). Both old (ages 11-12) and young (ages 6-8) fish appeared to have similar temporal patterns of residuals; however in older fish this pattern shifted by 1-2 years toward more recent years (Fig. 3B). The year-specific averaged residuals of the age 6-8 fish depicted a single anomalously warm year corresponding to 1983. The anomalously warm year in the age 11-12 fish was 1984-85, thus explaining the significance result in 1985. The results of the randomization test were not sensitive to the exclusion of data from the four most recent years (Table 2).
[FIGURE 3 OMITTED]
Discussion
The location of the anomalously warm signal in 1983, in the youngest and likely the more accurately aged fish, supports the hypothesis that the 1983 El Nino can be detected by using oxygen stable isotopes. From this analysis, we concluded that the break-and-burn aging method is accurate on average but has a potential tendency toward underaging fish >10 years.
Confirmation of the annual banding pattern in the ololiths of other Sebastes species has been accomplished by using a variety of methods. Woodbury (1999) confirmed the accuracy of age assignment in widow (Sebastes entomelas) and yellowtail (S. flavidus) rockfish, using the change in growth increment width associated with El Nino. Piner et al. (in press) has used bomb radiocarbon to confirm the annual pattern of otolith banding in canary rockfish (S. pinniger) and has reported a possible underaging bias for older fish. Andrews et al. (1999) used radiometric age determination to confirm the longevity of long-lived species. However, a larger study on black rockfish with stable isotopes is necessary to conclusively determine age estimates accurately and potential underaging bias.
The 1983 El Nino was chosen for the present study because it was one of the strongest recorded in the century (Sharp and McClain, 1993). Warm water conditions associated with the 1983 El Nino were sufficient to slow growth (MacLellan and Saunders, 1995; Woodbury, 1999) and alter reproductive patterns (VenTresca et al., 1995) in species occupying similar geographic ranges. In contrast, this study attempted to indirectly measure the environment experienced by black rockfish without the need to infer changes to biological processes. Nevertheless, our results appear to support the conclusions of MacLellan and Saunders (1995) and Woodbury (1999) that the anomalous oceanic conditions in 1983 are identifiable.
The analysis of model residuals rather than raw isotope ratios is more appropriate because of the obvious [[differential].sup.18]O temporal trend in some samples. Otolith processing difficulties also may have contributed to the trend. The opaque region of the otolith decreases in size with increasing age. The narrowing of the otolith region associated with older ages made precise sampling more difficult and may have resulted in accidental sampling from otolith material outside the opaque region. The sampling of otolith material from outside the opaque region may have contributed otolith material formed in cooler waters in contrast to the sampling of areas of the otolith associated with younger ages. The increasing trend in [[differential].sup.18]O was not explained solely by the decreasing temporal trend of summer water temperatures. However, an additional component of that trend may be the result of age-dependent fish movement to cooler waters that are deeper or more northerly. Furthermore, the isotope variability between fish may be due to fish inhabiting different areas in the early periods of life or to temporal differences in growth. Finally, changes in calibration of the spectrometer between assays may be a source of uncertainty.
A critical assumption behind the present study was that the lowest [[differential].sup.18]O corresponds to the warmest water temperature, and consequently the 1983 El Nino that serves as the time marker. The [[differential].sup.18]O values may be impacted by salinity in addition to water temperature (Dorval, 2004), and we assumed that salinity was constant and that the changes in [[differential].sup.18]O values were largely influenced by changes in temperature. A further confounding element to this kind of study is the ability of fish to move and potentially select microhabitats with different temperatures than that of the average local environment. Natural date-specific markers also must be monitored over a number of years to ensure that they remain identifiable within the otolith (Campana, 2001). We addressed this concern by selecting fish of various ages and from various collection dates and by performing the same analysis on each fish. Lastly, this method of age validation can be difficult to implement for fish with small otoliths or for long-lived fish because of the difficulties in obtaining sufficient otolith material from small growth increments.
The detection of El Nino events using [[differential].sup.18]O may allow the use of this reoccurring climatic event as a natural tag for age validation. Because previous studies that used El Nino events as time markers were forced to measure biological reactions to environmental changes, the use of [[differential].sup.18]O may be an improvement because it avoids assuming the intermediate step, namely that environment affects a biological process. The results from this study, however, were based on a small sample size and are, therefore, only preliminary. Further work in this area is warranted.
Acknowledgments
We are grateful to Maria Marcano of the University of Michigan geochemical laboratory for her help in setting up the assays. Bill Miller of the Oregon Department of Fish and Wildlife provided aging expertise. We thank the Sea Grant Fellowship in Population Dynamics and the National Marine Fisheries Service Northwest Fisheries Science Center for financial support. Finally, the anonymous reviewers and Christian Reiss greatly helped our efforts.
Manuscript submitted 13 February 2004 to the Scientific Editor's Office.
Manuscript approved for publication 8 February 2005 by the Scientific Editor.
Literature cited
Andrews, A. H., K.H. Coale, J. L. Nowicki, C., Lundstrom, Z. Palacz, J. E. Burton, and G. M. Cailliet. 1999. Application of an ion-exchange separation technique and thermal ionization mass spectrometry to [sup.226]Ra determination in otoliths for radiometric age determination of long-lived fishes. Can. J. Fish. Aquat. Sci. 56:1329-1338.
Beamish, R. J., and G. A. McFarlane. 1983. The forgotten requirement for age validation in fisheries biology. Trans. Am. Fish. Soc. 112(6):735-743.
Campana, S. E. 1997. Use of radiocarbon from nuclear fallout as a dated marker in the otoliths of haddock (Melanogrammus aeglefinus). Mar. Ecol. Prog. Ser. 150(1-3):49-56.
2001. Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J. Fish. Biol. 59(2):197-242.
Campana, S. E., G. A. Chouinard, J. M. Hanson, and A. Frechet. 1999. Mixing and migration of overwintering Atlantic cod (Gadus morhua) stocks near the mouth of the Gulf of St. Lawrence. Can. J. Fish. Aquat. Sci. 56(10):1873-1881.
Campana, S. E., and S. R. Thorrold. 2001. Otoliths, increments, and elements: keys to a comprehensive understanding offish populations? Can. J. Fish. Aquat. Sci. 58(1):30-38.
Chivas, A. R., P. DeDeckker, and J. M. G. Shelley. 1985. Strontium content of ostracods indicates lacustrine paleosalinity. Nature 316(6025):251-253.
Dorval, E. 2004. Relating water and otolith chemistry in Chesapeake Bay, and their potential to identify essential seagrass habitats for juveniles of an estuarine-dependent fish, spotted seatrout (Cynoscion nebulosus). Ph.D. diss., 134 p. Old Dominion Univ., Norfolk, VA.
Gao, Y. W., and R. J. Beamish. 2003. Stable isotope variations in otoliths of Pacific halibut (Hippoglossus stenolepis) and indications of the possible 1990 regime shift. Fish. Res. 60(2-):393-404.
Gao, Y., H. P. Schwarcz, U. Brand, and E. Moksness. 2001. Seasonal stable isotope records of otoliths from ocean-pen reared and wild cod, Gadus morhua. Environ. Biol. Fish. 61(4):445-453.
Holmden, C., R. A. Creaser, and K. Muehlebachs. 1997. Paleosalinities in ancient brackish water systems determined by Sr-87/Sr-86 ratios in carbonate fossils: a case study from the Western Canada Sedimentary Basin. Geoch. Cosmochim. Acta. 61(10):2105-2118.
Kalish, J. M., J. M. Johnston, J. S. Gunn, and N. P. Clear. 1996. Use of the bomb radiocarbon chronometer to determine age of southern bluefin tuna (Thunnus maccoyii). Mar. Ecol. Prog. Ser. 143(1-3):1-8.
Kalish, J. M., J. M. Johnston, D. C. Smith, A. K. Morison, and S. G. Robertson. 1997. Use of the bomb radiocarbon chronometer for age validation in the blue grenadier (Macruronus novaezelandiae). Mar. Biol. 128(4):557-563.
Love, M. S., M., Yoklavich, and L. Thorsteinson. 2002. The rockfishes of the Northeast Pacific, 404 p. Univ. California Press, Los Angeles, CA.
MacLellan, S. E., and M. W. Saunders. 1995. A natural tag on the otoliths of Pacific hake (Merluccius productus) with implications for age validation and migration. In Recent developments in fish otolith research (D. H. Secor, J. M. Dean, and S. E. Campana, eds.), p. 567-580. Univ. South Carolina Press, Columbia, SC.
Patterson, W. P., G. R. Smith, and K.C. Lohmann. 1993. Continental paleothermometry and seasonality using isotopic composition of aragonitic otoliths in freshwater fishes. Geophys. Monogr. 78:191-202.
Piner, K. R, O. S. Hamel, J. L. Menkel, J. R. Wallace, and C. E. Hutchinson. In press. Age validation of canary rockfish (Sebastes pinniger) from off the Oregon coast (USA) using the bomb radiocarbon method. Can. J. Fish. Aquat. Sci.
Ralston, S., and E. J. Dick. 2003. The status of black rockfish (Sebastes melanops) off Oregon and northern California in 2003. In Status of the Pacific coast groundfish fishery through 2003 and stock assessment and rishery evaluation, 75 p. Pacific Fishery Management Council, Portland, OR.
Sharp, G. D., and D. R. McClain. 1993. Fisheries, El Nino-Southern oscillation and upper ocean temperature records: an eastern Pacific example. Oceanography 6:13-22.
Thorrold, S. R., S. E. Campana, C. M. Jones, and P. K. Swart. 1997. Factors determining delta super(13)C and delta super(18)O fractionation in aragonitic otoliths of marine fish. Geochim. Cosmochim. Acta 61(14):2909-2919.
Thorrold, S. R., C. Latkoczy, P. K. Swart, and C. M. Jones. 2001. Natal homing in a marine fish metapopulation. Science 291(5502):297-299.
VenTresca, D. A., R. H. Parrish, J. L. Houk, M. L. Gingas, S. D. Short, and N. L. Crane. 1995. El Nino effects on the somatic and reproductive condition of blue rockfish, Sebastes mystinus. Calif. Coop. Oceanic Fish. Invest. Report 36:167-174.
Woodbury, D. 1999. Reduction of growth in otoliths of widow and yellowtail rockfish (Sebastes entomelas and S. flavidus) during the 1983 El Nino. Fish. Bull. 97:680-89.
Kevin R. Piner
Southwest Fisheries Science Center
National Marine Fisheries Service, NOAA
8604 La Jolla Shores Drive
La Jolla, California 92037
E-mail address: Kevin.Piner@noaa.gov
Melissa A. Haltuch
School of Aquatic and Fishery Sciences
University of Washington,
1122 NE Boat Street
Seattle, Washington 98105
John R. Wallace
Northwest Fisheries Science Center
National Marine Fisheries Service,
2725 Montlake Blvd East
Seattle, Washington 98112
Table 1
Age-specific 5180 values for each black rockfish (Sebastes
melanops), along with annulus age and collection year.
Values replaced by "N/A" indicates samples that were not
reported by the stable isotope laboratory.
Sample number
Age 1987-33 1987-86 1987-98
0+ -0.96 N/A -0.633
1+ -1.17 0.914 -0.981
2+ -0.42 0.654 -0.644
3+ -0.04 0.461 -0.518
4+ 0.42 1.006 -0.202
5+ 0.28 0.946 -0.037
6+ 0.957 0.630
7+
8+
9+
10+
11+
Annulus age (yr) 6 7 7
Collection year 1987 1987 1987
Sample number
Age 1988-7 1988-100 1991-27
0+ -0.357 1.209 N/A
1+ -0.513 0.725 -0.53
2+ -0.504 -0.544 -0.42
3+ -0.579 1.037 -0.39
4+ -0.320 N/A -0.09
5+ -0.257 N/A -0.22
6+ 0.137 N/A -0.05
7+ 0.962 1.00
8+ N/A
9+ N/A
10+ N/A
11+ N/A
Annulus age (yr) 8 7 12
Collection year 1988 1988 1991
Sample number
Age 1991-86 1991-168 1991-178
0+ -0.128 -2.06 0.756
1+ -0.114 -1.77 0.948
2+ -0.358 -1.09 0.869
3+ -0.409 -0.64 0.741
4+ -0.082 -0.85 0.338
5+ -0.218 -0.73 N/A
6+ 0.1067 0.35 0.785
7+ 0.512 1.08 1.054
8+ 0.805 1.07 1.113
9+ 1.053 N/A 1.404
10+ 1.164 N/A 1.510
11+ 1.881
Annulus age (yr) 12 11 11
Collection year 1991 1991 1991
Table 2
Results of the retrospective analysis that estimated the
statistical significance of the magnitude of the average
negative residual from the years 1983 and 1985. Assay
results from otolith material formed after the cutoff year
were removed from the randomization analysis.
Cutoff year 1983 1985
1989 *0.03 *0.05
1988 *0.03 *0.05
1987 *0.04 *0.06
1986 *0.05 *0.26