Validation of age estimation in geoduck clams using the bomb radiocarbon signal.
KEY WORDS: bomb radiocarbon, geoduck, Panopea generosa, ageing
Accurate age estimates are imperative for effective management and sustainable yield of organisms targeted for harvest. In many marine species, annual growth increments are readily discernable in conserved carbonaceous structures. However, interpretation of annual growth increments requires some form of age validation to verify their annual periodicity before using them for age estimation (Kalish et al. 1995, Campana 2001). Although overestimation of age may be risk-averse for fisheries management, underestimating actual age and longevity of target species has frequently led to overexploitation.
Geoduck clams (Panopea generosa Gould 1850; referred to earlier as Panopea abrupta (see Vadopalas et al. 2010)) are the target of several valuable commercial fisheries conducted in the nearshore and inshore Pacific waters of Alaska, British Columbia, and Washington. Management agencies have estimated age frequencies from wild populations to develop models of population dynamics necessary for effective management of geoducks. Age estimation in geoducks is conducted using methods analogous to those used for otoliths in bony fishes--growth fines, assumed to be annuli, are visualized and counted via fight microscopy. Among bivalve molluscs, the putative longevity of the geoduck clam places them among the longest riving bivalve molluscs, with the oldest reportedly living to 168 y (Bureau et al. 2002). To date, verification that the growth bands quantified are actually annuli has been limited to (1) studies of young, known-age clams (Shaul & Goodwin 1982; Vadopalas unpubl, data), (2) correlation of age frequencies inside and outside a disturbance zone (Shaul & Goodwin 1982), and (3) correlation of bandwidth with sea surface temperature patterns (Strom et al. 2004, Black et al. 2008).
Although these verifications of annuli seem sufficient, three considerations suggest the utility of a different approach. First, growth bands may serve as a chronometer in early life, as demonstrated, but may then vary from an annual pattern as the individual ages (Rhoads & Lutz 1980). Second, spatial and temporal variation in geoduck recruitment may provide an alternate explanation for the correlation of maximum age with a localized substrate disturbance observed by Shaul and Goodwin (1982). The third consideration is the availability of an efficient and accurate means of achieving age verification.
Atmospheric testing of atomic bombs during the 1950s and 1960s produced a dramatic increase in atmospheric radiocarbon ([sup.14]C) that was reflected circumglobally in dissolved inorganic carbon (DIC) in marine waters (Broecker et al. 1985). As a result, organisms in the marine environment incorporated the signal as skeletal carbonate, such as the shells of bivalves. This increase in [sup.14]C provided a precise marker for age validation for species living during the bomb period (~1957 to ~1967). Thus, if previous geoduck age estimates are reasonable approximations for the population in Puget Sound, Washington, then bomb radiocarbon dating may provide the needed validation.
Whether this increase in [sup.14]C coincides with a concomitant change in shell [sup.14]C from the assumed annual periodicity of growth bands in geoducks is the subject of this investigation. We hypothesize that [sup.14]C values derived from the earliest growth bands in geoducks older than 50 years will be temporally correlated to prebomb levels in [sup.14]C chronologies derived from yelloweye rockfish (coastal Southeast Alaska (Kerr et al. 2004)) and Pacific halibut (Gulf of Alaska and British Columbia (Piner & Wischniowski 2004)), and that geoducks born during and after the bomb testing period (1953-1963) will exhibit elevated [sup.14]C levels in the earliest growth bands, again similar to those in the yelloweye rockfish and Pacific halibut reference chronologies.
In 2001, geoducks (n = 1,010) were collected from Dougall Point (the northeast side of Hartstine Island in Case Inlet) in the South Sound subbasin of Puget Sound, Washington (Fig. 1). Sampling date, estimated age, estimated birth year from growth zone counts, water depth, and GPS coordinates are shown in Table 1. To avoid possible [sup.14]C contamination, all work on shell samples occurred in laboratory areas where no [sup.14]C spiking work had ever occurred.
[FIGURE 1 OMITTED]
We modified the thin sectioning methods of Clark (1980) to estimate ages. Because the exterior portions of the valves are subject to erosion, potentially erasing the earliest growth bands, the interior chondrophore, or hinge plate, was excised from the right valves using a handheld abrasive cutoff wheel. The removed chondrophore was mounted in the mechanical chuck of a slow-speed diamond saw (Buehler, Lake Bluff, IL). A minimum of three 2-mm thin sections were made along the dorsal ventral axis of the chondrophore. Thin sections were slide mounted and polished to a final thickness of 1.5 mm using a series of 300-, 800-, and 2,400-grit paper. Individual growth bands, comprising both hyaline (translucent) and opaque sections, and assumed to form annually, were visualized using a compound microscope with transmitted light. Growth bands were tallied by three independent age readers over at least three sections to produce a final consensus age for each specimen.
Seven specimens with presumed birth years before, during, and after the bomb testing period were chosen for [sup.14]C analysis (Table 1). This sample size is within the range prescribed by Kerr et al. (2005) as sufficient for validating age estimates given the large amplitude of the bomb signal in reference chronologies. Thin sections of these specimens were sampled from the first 3 to 5 years of growth, closest to the umbo. Approximately 12-mg valve material (CaC[O.sub.3]) was removed via a semi-automated microsampler guided by a digital image. Carbon dioxide generated from milled CaC[O.sub.3] material removed from thin-sectioned valves was reacted with a catalyst to form graphite for accelerator analysis along with standard blanks. The samples were assayed for [sup.14]C using accelerator mass spectrometry at the National Ocean Sciences Accelerator Mass Spectrometry Facility at Woods Hole Oceanographic Institute. The radiocarbon values reported represent deviations of the [sup.14]C-to-C ratio of the samples from the internationally accepted "modern" (Olsson 1970) value (Karlen et al. 1968) and presented as [DELTA][sup.14]C (Stuiver & Polach 1977).
To calibrate our measurements, we reference two [DELTA][sup.14]C chronologies for the northeast Pacific (Kerr et al. 2004, Piner & Wischniowski 2004). The [DELTA][sup.14]C values from each of our specimens were compared with those in the reference chronologies at estimated birth years to gauge temporal correlation. The [sup.14]C levels were compared with estimates derived from growth band counts to validate current age determination methodology.
Growth band counts were consistent among readers across sections, with the exception of the single cut possible through the umbo. The umbo thin sections were the only sections to show a ventral growth band for the first year of growth; thin sections that were anterior or posterior to the umbo routinely missed this first annulus. Growth bands for the first 4-10 y appeared as opaque regions separated by more translucent areas, and were very wide relative to growth bands more than 20 bands dorsal to the umbo. A distinctive and obvious shift in the appearance and width of the growth bands occurred between the 4th and 10th growth band. The postshift growth bands were much narrower than those preceding them ventrally. Growth bands closer to the dorsal margin of the hinge plate were generally quite narrow, especially in older clams; with more than 50-60 growth bands present, the dorsal margin of the hinge plate became so densely packed with growth lines an increase from 400-600x magnification was necessary.
As expected, radiocarbon values derived from chondrophore samples exhibited an expected increase. The sample from the specimen with the putative birth year of 1949, prior to initiation of thermonuclear bomb testing in 1953, and detection of elevated [sup.14]C in DIC showed a radiocarbon value of -107.1 [per thousand]. This value is based on putative annuli that span the years 1949 to 1952 (Table 1) and is within the range of prebomb [sup.14]C values exhibited by yelloweye rockfish (-102.2 [+ or -] 9.3[per thousand] (Kerr et al. 2004)) and Pacific halibut (-107.0 [+ or -] 6.9 [per thousand] (Piner & Wischniowski 2004); Fig. 2). The sample taken from specimen B comprised the years 1957 to 1960 based on annuli counts. The [DELTA][sup.14]C value of -96.7 [per thousand], although greater than that for specimen A, fell above the halibut prebomb range but was within the reported prebomb range for yelloweye rockfish. Yelloweye rockfish reference chronology [DELTA][sup.14]C values increased from -94.7-68.9[per thousand], and Pacific halibut reference chronology [DELTA][sup.14]C values increased from -99.1-84.0[per thousand] during the period of dramatic increase in atmospheric [sup.14]C. Putative birth years for specimens B, C, and D occur during this period, and [DELTA][sup.14]C values increased from 46.7[per thousand] (sample B) to -30.3[per thousand] (sample D). Levels of [sup.14]C for samples E, F, and G were relatively similar.
We analyzed [sup.14]C levels in a time series of samples from geoduck clam valves from Puget Sound, Washington, and found levels that correspond to the documented increase in atmospheric [sup.14]C resulting from the nuclear bomb testing that occurred from 1953 to 1963. The year of probable first increase and the year of maximum [sup.14]C show good concordance with the yelloweye rockfish and Pacific halibut reference chronologies. This correspondence provides strong evidence that growth rings in geoduck clams are deposited annually throughout their life history, and validates age estimates based on growth ring counts. This concordance provides the first [sup.14]C chronology specific to Puget Sound, Washington.
[FIGURE 2 OMITTED]
The current study provides valuable verification of the annular nature of growth bands in a wide age range of geoduck clams over 5 decades. In specimen A, the presence of carbonaceous material with a [DELTA][sup.14]C value that corresponds with [DELTA][sup.14]C values in yelloweye rockfish and Pacific halibut with similar estimated birth years provides strong evidence that material sampled must have been formed prior to 1957, when elevated [sup.14]C first becomes detectable in DIC, suggesting that specimen A was born prior to 1957. The [DELTA][sup.14]C value for specimen B is slightly elevated, again in accord with the two northeast Pacific chronologies (Kerr et al. 2004, Piner & Wischniowski 2004). The steep increase in [DELTA][sup.14]C values for specimens C, D, and E with putative birth years during the 1960s is in accord with almost all ocean surface [DELTA][sup.14]C chronologies (including Kerr et al. (2004), Piner and Wischniowski (2004), and Kastelle et al. (2008) from the northeast Pacific). The correspondence with growth line count chronologies strongly supports and verifies growth line annularity in geoduck clams.
The three most recent samples (E, F, and G) exhibited [sup.14]C levels well below those of both the yelloweye rockfish and the Pacific halibut chronologies. These samples included growth band count estimates corresponding to the periods 1968 to 1971, 1974 to 1977, and 1978 to 1982, respectively. Bomb [DELTA][sup.14]C signal maxima and the corresponding potential rates of decline are strongly dependent on regional oceanographic water mass circulation patterns, such as exchange volume, residence times, upwelling, and mixing (Weidman & Jones 1993). Values from the two [sup.14]C chronologies we reference are from the Gulf of Alaska and the southeast coast, both receiving more surface waters via the Alaskan Gyre and less influenced by coastal upwelling (Whitney et al. 2005). In contrast, Puget Sound is strongly influenced by upwelled, nutrient-rich water entering the Juan de Fuca submarine canyon via remote southern forcing (Hickey & Banas 2003) during summer months when bivalve feeding is most active and shell growth occurs.
There are sources of potential error in [DELTA][sup.14]C dating. First, the shell material used may have included more recent shell deposits, which would elevate [sup.14]C levels in samples with birth years during the rise of atmospheric [sup.14]C and decrease [sup.14]C levels in samples with birth years after the peak. However, the correspondence between prebomb values in all 3 data sets may falsify such systematic sampling bias. Thus, the most parsimonious explanation for the lower maxima observed here versus the yelloweye rockfish and Pacific halibut data sets is that [sup.14]C depauperate upwelled waters entering the Strait of Juan de Fuca buffer the bomb signal relative to the Gulf of Alaska and southeast Alaskan waters.
Although pelagic fish integrate [sup.14]C information from broadened spatial scales, depending on foraging and migration patterns, obligate sedentary organisms (e.g., clams) can provide precise indications of historical bomb radiocarbon levels for specific locales. For example, although the data from yelloweye rockfish (Kerr et al. 2004) and Pacific halibut (Piner & Wischniowski 2004) may be affected by the general water mass circulation patterns in southeast Alaska and the Gulf of Alaska, respectively, the data reported herein are specific to Case Inlet (47-16'34" N, 122-50'53" W), an inland subbasin of Puget Sound. The flow into Puget Sound of older, upwelled waters (Feely et al. 2008) during the summer period of growth may dampen the [sup.14]C maxima and hasten the decline of the bomb signal relative to the observations from the Gulf of Alaska.
The importance of accurate aging methods cannot be overemphasized. Age frequency distributions and management models developed from erroneously low age estimates may allow unsustainable harvest levels as a result of premature truncation of stock reproductive output. Underestimations of age were partially responsible for the overharvest of the Pacific ocean perch (Sebastes alutus) (e.g., Beamish 1979) orange roughy (Hoplostethus atlanticus) (e.g., Smith et al. 1995), and red sea urchins (Strongylocentrotus franciscanus) (Ebert & Southon 2003). Although geoduck clams show a linear relationship between age and shell length during the first 8-10 y, the correlation rapidly disappears with increased age (Vadopalas, unpubl, data), notwithstanding genetic and phenotypic variability in growth. Counts of growth rings gained importance as the wild geoduck fishery developed, increasing the need for sound resource management. Shaul and Goodwin (1982) validated annuli in geoduck valves by counting growth rings in geoducks taken in 1978 and 1979 from within and directly adjacent to an area subjected to removal of clams via dredging in 1952. Within the dredged area, 89% of specimens were less than 26 y old based on growth ring counts, compared with only ~50% outside the dredged area. Another method to verify age estimation was needed because of an assumption of the dredged area experiment conducted by Shaul and Goodwin (1982). Although it may seem intuitively obvious that the age structure should be similar in a given area, significant spatial and temporal recruitment variability (patchiness) has been observed in geoduck (Vadopalas 2003, Valero et al. 2004). Thus, the results observed by Shaul and Goodwin (1982) might be explained by highly variable annual settlement on small spatial scales.
In conclusion, the current study provides strong evidence that growth lines present in geoduck clam shells are annular, and thus extends and supports the indirect evidence presented by Shaul and Goodwin (1982), Strom et al. (2004), and Black et al. (2008). This evidence verifies age frequency data sets used in the management of wild geoduck clam fisheries of significant economic importance to British Columbia, Canada, and Alaska and Washington states. Future studies using the long-lived geoduck clam to establish annual [sup.14]C chronologies from specific locations could help elucidate the annual upwelling history for the northeast Pacific coast, a potentially useful tool to increase our understanding of Pacific decadal oscillations and El Nino events.
We are indebted to and thank Don Rothaus, Bob Sizemore, Michael Ulrich, and Alex Bradbury (aka. The Fab Four) of the Washington Department of Fish and Wildlife for sample collections, and Heather Honeycutt and Jessica Raaum for additional age estimates. Lab space for age estimation at the University of Washington School of Aquatic and Fishery Sciences was generously provided by David Beauchamp. We are also indebted to L. A. Kerr, A. H. Andrews, B. R. Frantz, K. H. Coale, T. A. Brown, and G. M. Cailliet for providing comparison data prior to publication of their reference chronology; Craig Kastelle and Allen Andrews for important suggestions that greatly improved the manuscript; Steve Campana for advice on the design of our study; and John Hayes for valuable discussions that stimulated the investigation. This work was funded in part by a grant from the Washington Sea Grant Program, University of Washington, pursuant to National Oceanic and Atmospheric Administration (NOAA) award no. NA76RG0119. The views expressed herein are those of the authors and do not necessarily reflect the views of NOAA or any of its subagencies. Additional support for B. V. was received from the Jensen Fellowship, and for E. C. and B. V. from the Egtvedt Endowment, both via the University of Washington School of Aquatic and Fishery Sciences. Support for C. W. was through NSF Cooperative Agreement no. OCE-9807266.
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BRENT VADOPALAS, (1) * CHRIS WEIDMAN (2) AND ELYSE K. CRONIN (3) ([dagger]).
(1) University of Washington School of Aquatic and Fishery Sciences, Box 355020, 1122 NE Boat Street, Seattle, WA 98105; (2) Waquoit Bay National Estuarine Research Reserve, PO Box 3092149, Waquoit Highway, Waquoit, MA 02536; (3) University of Washington School of Dentistry, 1959 NE Pacific Street, D323 HSC, Seattle, WA 98195-6365
* Corresponding author. E-mail: firstname.lastname@example.org
([dagger]) Current address: Vista Ridge Dental, 4300 N. Quinlan Park Road, #230, Austin, TX 78732
TABLE 1. Summary age estimation data for geoduck clams Panopea generosa from Case Inlet, Puget Sound, Washington. Final No. of Consensus Growth Estimated Weight Sample Age Bands Years Sampled Sample ID Estimate (y) Sampled Sampled (mg) A 464-b 52 1-5 1949-1952 12.9 B 94-a 44 1-4 1957-1960 11.4 C 188-a 38 1-3 1963-1965 8.9 D 213-a 36 1-4 1965-1968 6.7 E 189-a 33 1-4 1968-1971 17.4 F 485-a 27 1-4 1974-1977 11.1 G 241-a 23 1-5 1978-1982 16.9 Sample [D.sup.14]C [+ or -] SD A -107.1 3.90 B -96.7 3.30 C -46.9 3.49 D -30.3 3.29 E -3.5 3.69 F -9.7 4.19 G -1.7 4.19
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|Author:||Vadopalas, Brent; Weidman, Chris; Cronin, Elyse K.|
|Publication:||Journal of Shellfish Research|
|Date:||Aug 1, 2011|
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