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Bomb radiocarbon dating of the endangered white
abalone (Haliotis sorenseni ): investigations
of age, growth and lifespan
Allen H. Andrews
A
,
G
,Robert T. Leaf
B
,Laura Rogers-Bennett
C
,
Melissa Neuman
D
,Heather Hawk
E
and Gregor M. Cailliet
F
A
NOAA Fisheries, Pacific Islands Fisheries Science Center, 99-193 Aiea Heights Drive,
#417, Aiea, HI 96701, USA.
B
Department of Coastal Sciences, The University of Southern Mississippi, 703 East Beach Drive,
Ocean Springs, MS 39564, USA.
C
Bodega Marine Laboratory 2California Department of Fish and Wildlife, 2099 Westside Road,
Bodega Bay, CA 94923, USA.
D
NOAA Fisheries, Southwest Region, Office of Protected Resources, 501 West Ocean Boulevard,
Suite 4200, Long Beach, CA 90802-4213, USA.
E
De
´partement de Biologie, Universite
´Laval, 1045 Avenue de la Me
´decine, Que
´bec,
QC G1V 0A6, Canada.
F
Moss Landing Marine Laboratories, California State University, 8272 Moss Landing Road,
Moss Landing, CA 95039, USA.
G
Corresponding author. Email: allen.andrews@noaa.gov
Abstract. Understanding basic life-history characteristics of white abalone (Haliotis sorenseni), such as estimated
lifespan, is critical to making informed decisions regarding the recovery of this endangered species. All predictive
modelling tools used to forecast the status and health of populations following restoration activities depend on a validated
estimate of adult lifespan. Of the seven Haliotis species in California, white abalone is considered to have the highest
extinction risk and was the first marine invertebrate listed as an endangered species under the Federal Endangered Species
Act (ESA). Lifespan was previously estimated from observations of early growth; however, no study has generated ages
for the largest white abalone. To address questions of age and growth, bomb radiocarbon (D
14
C) dating was used on shells
from large white abalone. Measured bomb D
14
C levels were compared to regional D
14
C reference records to provide
estimates of age, growth and lifespan. Bomb radiocarbon dating indicated that growth was variable among individuals,
with a maximum estimated age of 27 years. The findings presented here provide support for previous age and growth
estimates and an estimated lifespan near 30 years. These age data support the perception of a critical need for restoring the
remnant aging and potentially senescent population.
Additional keywords: age validation, carbon-14, Haliotidae, longevity, Mollusca, Southern California Bight.
Received 8 January 2013, accepted 27 April 2013, published online 19 July 2013
Introduction
Abalone (Haliotis spp.) of the north-eastern Pacific Ocean have
suffered severe population declines that have been primarily
attributed to commercial and recreational fishing (Karpov et al.
2000;Rogers-Bennett et al. 2002), and disease, poaching and
predation have exacerbated the decline (Daniels and Floren
1998;Watson 2000;Moore et al. 2002). Efforts to manage
abalone in California have relied on estimating current levels of
density in the wild, comparing current-day values to those
estimated before population collapse, and carrying out actions
that serve to restore densities to pre-exploitation levels. The
predictive value of models used to determine outcomes of
different restoration scenarios increases if validated estimates of
key demographic variables, such as lifespan and expected
survival rates, can be incorporated into the models (Tegner et al.
1989;Rogers-Bennett and Leaf 2006;Leaf et al. 2008b).
Obtaining this kind of information for endangered populations
is challenging because of their rarity and elusive nature,
research permitting requirements, and the pressure of destruc-
tive sampling. In this case, the use of archived museum materials
was invaluable (Suarez and Tsutsui 2004).
Of the seven Haliotis species in California, white abalone
(Haliotis sorenseni) is considered at highest risk of extinction,
with current estimates of population size less than 1% of historic
CSIRO PUBLISHING
Marine and Freshwater Research, 2013, 64, 1029–1039
http://dx.doi.org/10.1071/MF13007
Journal compilation ÓCSIRO 2013 www.publish.csiro.au/journals/mfr
estimates (Rogers-Bennett et al. 2002), and continue to decline
in the absence of fishing (Butler et al. 2006;Stierhoff et al.
2012). In 2001, the species became the first marine invertebrate
to be included on the endangered species list under the Federal
Endangered Species Act (ESA). As a result of this listing,
a recovery plan was drafted to guide efforts for rebuilding white
abalone populations (National Marine Fisheries Service 2008).
An understanding of white abalone life-history characteristics is
critical to restoring the species from its extirpated state and will
be necessary for post-recovery management. Although much of
the ecology of white abalone has been described (Tutschulte
1976), age and growth relationships and the maximum lifespan
are poorly understood. Given the large shell-size of extant
populations, and the uncertainty of reproductive potential from
large and potentially old individuals, it has been hypothesised
that remaining individuals are near the end of their lifespan and
may have little or no reproductive potential (Davis et al. 1996;
Hobday and Tegner 2000). This hypothesis is supported by 14%
per year declines documented in the remnant wild white abalone
populations (Stierhoff et al. 2012).
Estimates of age, growth and lifespan for white abalone are
limited to studies of early growth and growth in captivity.
Limited observations in the field and captive environments
indicate that early growth is initially rapid, slows with increas-
ing size, and is variable among individuals (Tutschulte and
Connell 1988). From those observations, an age near maximum
size (,210-mm maximum shell length, MSL) was extrapolated
to ,35 years; however, the estimates of age and growth remain
unconfirmed past an age of ,10 years and lifespan is not known.
No study has generated ages for large adult white abalone. For a
better understanding of ontogenetic growth, it is important to
evaluate as much of the lifespan as possible (Beamish and
McFarlane 1983). Because mollusk shell provides a conserved
carbonate record that covers the lifespan of any given individual
(Richardson 2000), there is promise for the use of bomb
radiocarbon dating as an independent measure of age for white
abalone beyond 10 years of age (e.g. Weidman and Jones 1993).
Bomb radiocarbon dating is a technique that has evolved as a
unique application for validating the age of fishes and inverte-
brates. The approach relies on a conserved record of the rapid
increase in radiocarbon (
14
C) that occurred in the oceans of the
world as a result of atmospheric testing of thermonuclear
devices in the 1950s and 1960s (Broecker and Peng 1982).
The marine signal is delayed relative to the atmospheric signal
by 7–10 years (Nydal 2000), but the uptake of bomb-produced
radiocarbon by the marine environment was virtually synchro-
nous in the mixed layer of mid-latitude oceans (Broecker and
Peng 1982). For marine carbonates, this signal was first recorded
as a time series in hermatypic corals (Druffel and Linick 1978).
This time-specific signal provides a reference point that can be
used to determine age. Application to fishes began with an
innovative comparison of D
14
C values recorded in otolith (fish
ear bone) carbonate relative to regional D
14
C records from
hermatypic corals (Kalish 1993). Measured D
14
C levels pro-
vided an independent determination of age for corroboration of
age estimates from growth-zone counting in otoliths (Campana
2001,Kalish 2001). Bomb radiocarbon dating has since been
applied successfully to numerous teleost fishes by using otoliths
(e.g. Andrews et al. 2007;Ewing et al. 2007;Neilson and
Campana 2008) and has been expanded to other marine organ-
isms (e.g. Ebert and Southon 2003;Frantz et al. 2005;Roark
et al. 2006;Stewart et al. 2006), including mollusks (e.g.
Weidman and Jones 1993;Kilada et al. 2009). In addition,
recent bomb radiocarbon work with red abalone (H. rufescens)
has shown that abalone shell can serve as a record of the D
14
C
signal in the north-eastern Pacific Ocean (Leaf et al. 2008a).
The aim of the present study was to use bomb radiocarbon
dating to provide estimates of age and growth for white abalone.
It was hypothesised that bomb radiocarbon dating can provide
age estimates for the largest shells because of the typically time-
specific nature of the rise of D
14
C. To test the applicability of the
technique relative to other regional D
14
C reference records,
D
14
C measurements were also made from shell material with
known collection dates. It was further hypothesised that the
compiled regional D
14
C reference information will provide
valid markers for age estimation of white abalone collected
during more recent years within the Southern California Bight
(SCB).
Materials and methods
Abalone shells
Five white abalone shells collected from the SCB were analysed
for D
14
C and estimates of age. Only shells with a known
collection date or year and known collection location were used.
Known location was important in order to avoid potential issues
associated with regional differences in patterns of D
14
C depo-
sition (e.g. shells from Baja California). The shells also had to be
in adequate condition, such that areas of the prismatic layer were
intact along the growth axis of maximum shell length (Fig. 1).
Selected sample locations in the shell were usually not free of
biotic and abiotic loss of material and microscopic examination
(Olympus dissecting microscope, Tokyo, Japan) was used to
select unaffected shell portions. The apex, or earliest shell
growth, has the thinnest prismatic layer and was often not intact;
however, the nacreous shell was considered acceptable for this
Fig. 1. Whole white abalone shell (1972-2), with sample locations denoted
with outlined black bars. Locations sampled were the apex (0-mm MSL) and
edge (193-mm MSL), with three intermediate samples at 50-mm, 100-mm
and 150-mm MSL (scale bar ¼,4 cm).
1030 Marine and Freshwater Research A. H. Andrews et al.
part of the shell when the apex included the earliest growth. As a
verification of proper extraction of the earliest shell growth in
the apex area, juvenile shell dimensions and shape were refer-
enced. Most samples were located in museum archives with the
best shells from the Santa Barbara Museum of Natural History
(n¼4) and one from a Proteus Farm aquaculture project
(Table 1). Collection years ranged from 1967 to 1996, with shell
sizes being from 151-mm to 200-mm MSL. All shells were
collected from within the SCB, ranging from Santa Catalina
Island to off Point Loma, San Diego, California.
Sampling design in this kind of study is usually focused on
validating estimates of age from some form of growth-zone
counting. White abalone has not been shown to have regular
banding patterns that can be quantified (e.g. Haliotis corrugata,
Shepherd and Avalos-Borja 1997); therefore, age was roughly
calculated on the basis of the age and growth data from
Tutschulte and Connell (1988). Sample locations across the
shell were selected to date back through the informative period
in bomb radiocarbon dating (between ,1955 and 1970). Edge
material was taken from each specimen, except the most
recently collected shell from Proteus Farm because its final
few years of life were in aquaria, which was used to determine
D
14
C levels near the time of collection. The sampling series for
each specimen proceeded from the edge sample through shell
material that was accreted at younger ages (Fig. 1).
Shell-sample series
Each shell specimen was sampled in a manner that was suited for
the collection year and a projection of the potential age back
through the period of rising marine D
14
C. WA 1967 was
sampled on the edge and apex because of its proximity to the
peak D
14
C values anticipated for the year of collection. The
three specimens collected in 1972 were sampled the most
comprehensively because it was expected that the growth of
each individual would either span the D
14
C peak and rise, or
some portion of it. WA 1996 was the only sample available that
held promise of addressing the question of lifespan because it
was collected nearly 30 years after the D
14
C peak was reached
for the D
14
C rise (estimated as ,1967 to 1970 from other D
14
C
records). Therefore, two samples (each replicated) were taken at
and near the apex to evaluate the D
14
C values in the shell at the
earliest age of the specimen.
Sample extractions were made at points along the growth axis
(spiral) of the shell, following what would have been the MSL of
the specimen (Fig. 1). A DremelÒrotary tool (Robert Bosch Tool
Corporation,Mount Prospect, IL, USA) with a cutting wheel was
used to cut small sections fromthe shell locations. Each was cut to
a width of a few millimetres, with a length of up to 1 cm along the
arc of the shell increments. The extracted portions included both
prismatic and nacreous layers (Fig. 2), and the nacreous layer was
mostly removed by grinding with a lapidary wheel. Each
extracted portion provided variable amounts of prismatic materi-
al, the quality of which ranged from relatively pristine to highly
eroded (endoliths (H. Hawk unpubl. data) and other forms of
degradation). Each extracted portion of prismatic shell was
treated with a series of cleaning procedures that ranged from
sonication in ultra-pure water and weak acid (0.01 N HCl) to
remove adhering material and degraded carbonate, to extensive
Table 1. Five white abalone shells (Haliotis sorenseni) were sampled in a time series for bomb radiocarbon dating
Individual sizes are maximum shell length (MSL). Sample MSL is the shell length of the individual when the sampled shell materialwas accreted (edge to apex
to denote youngest to oldest). Radiocarbon values, reported as Fraction modern (Fm) and D
14
C, are adjusted for known or estimated formation year and
corrected for d
13
C fractionation. Collection numbers are for Santa Barbara Museum of Natural History, except WA 1996 (Proteus Farm)
Shell ID (collection #) Collection location and year Water depth (m) MSL (mm) Sample MSL (mm) Fraction modern D
14
C
A
(%)
WA 1967 (352560) Santa Catalina December 1966 Unknown 151 151 (edge) 1.0612 59.0 3.5
1.0542
D
42.0 3.4
0 (apex) 0.9672 42.0 4.0
WA 1972-3 (352558)
B
Point Loma, San Diego 1972 10–20 165 165 (edge) 1.0166 6.6 3.5
0 (apex) 0.9546 54.2 3.4
WA 1972-2 (352558)
B
Point Loma, San Diego 1972 10–20 193 193 (edge) 1.0384 27.3 3.7
150 0.9347 66.5 3.5
100 0.9242 75.8 3.5
0 (apex) 0.9347 85.5 3.2
WA 1972-1 (352558)
B
Uncertain
B
1961 (est.) Unknown 195 195 (edge) 0.9444 56.9 3.6
0.9456
D
61.0 3.9
169 0.9314 75.5 3.5
140 0.9164 90.9 3.5
109 0.9315 77.2 3.5
83 0.9135 95.0 3.5
0 (apex) 0.9259 83.5 3.5
WA 1996 (143) Los Angeles
C
1996 2 years
C
Unknown 200 61 1.0521 44.7 3.7
1.0406
D
38.1 5.2
0 (apex) 1.0792 76.6 3.5
1.0757
D
68.1 3.0
A
Adjusted for fractionation with an assumed q
13
C value of 1, or close to 1 where q
13
C was measured (range 0.1 to 2.1%).
B
All shells were in the same collection box at SBMNH.
C
Collection location generally known with a year of death between 1994 and 1998 (Tom McCormick, Proteus Farm).
D
Replicate sample.
Bomb radiocarbon dating of white abalone Marine and Freshwater Research 1031
microscopic examination with removal of endolithic material
with a fine-tipped probe, followed by repeated sonication and
weak acid treatments. Samples were considered finished when
only small grains of clean abalone shell were visible under a
dissecting microscope (ranging in weight from 5 to 27 mg).
These samples were submitted as carbonate to the Center for
Accelerator Mass Spectrometry at Lawrence Livermore National
Laboratories for radiocarbon measurement using standard
preparation procedures for analysis on an accelerator mass
spectrometer (AMS). Values for radiocarbon were reported as
Fraction modern (Fm), which were converted to D
14
Cin
reference to an established pre-nuclear-age radiocarbon record
(Stuiver and Polach 1977) and standardised for isotopic
fractionation. An assumed delta carbon-13 (d
13
C) value of
1 was used to correct for fractionation (based on the mean
measured value from other shells), except for samples where
d
13
C was measured (0.1 to 2.1%). In addition, dates
of collection and near year-of-formation dates wereused to adjust
D
14
C values for modern time (since 1950); pre-bomb required no
adjustment from 1950, but an assumed year of 1960 was used for
the rise D
14
C values and 1970 was used for the near-peak D
14
C
values. These adjustments minimisedpotential differences for the
comparison of these data with the reference D
14
Cdata.
Regional D
14
C reference
To provide a temporal calibration for the measured D
14
Cin
white abalone shell samples, a series of records were compiled
to describe the temporal nature of the regional D
14
C signal
(Fig. 3). The nearest complete D
14
C records were from otoliths
of yelloweye rockfish (Sebastes ruberrimus;Kerr et al. 2004;
A. H. Andrews, unpubl. data) and Pacific halibut (Hippoglossus
stenolepis;Piner and Wischniowski 2004). To provide a
regional abalone context to the comparisons, a series of known-
age abalone shell samples from within the SCB were analysed
for D
14
C(Table 2). The additional samples covered the periods
of pre-bomb to post-bomb decline. In addition, measurements of
dissolved inorganic carbon (DIC) from various locations and
points in time were considered (Linick 1978;Robinson 1981;
Druffel and Williams 1991;Williams et al. 1992). A local
regression (Loess curve) was fit to the revised yelloweye
rockfish D
14
C data to provide a general indication of the central
distribution of the time series, which was reinforced with the
known-age abalone samples and concurrent D
14
C rise docu-
mented with Pacific halibut D
14
C record. The measured
D
14
C values from some white abalone samples could be
assigned to the period of rising D
14
C (diagnostic values) and
were given a year-of-formation based on this median Loess
curve estimate. A range of possible years for the sample for-
mation was estimated based on the 95% CI of the yelloweye
rockfish D
14
C data, a range taken into consideration when
estimating age and growth.
Growth function
The information associated with each sample point consisted
of the estimated year-of-formation, the D
14
C value, and the MSL
of the specimen where the sample was extracted. The distance of
each sample location to the edge of the shell was used to
determine the potential age range of the formation period.
We used a two-parameter von Bertalanffy growth function
(Fabens 1965),
Lt¼L1ð1ektÞ;
to evaluate the range in ages when the sample was formed. To do
this, we used an iterative procedure where the value of the mean
asymptotic shell length was fixed L
N
¼210-mm MSL,
Tutschulte and Connell 1988). Iterations were performed by
changing the value of the von Bertalanffy growth function
parameter kto match the estimated year-of-formation and
associated 95% CI determined from D
14
C analysis. Addi-
tionally, we explored how the estimated age of the sample and
k-values changed at 5.0 mm from the sample. Results from
iterative fits of the von Bertalanffy growth function were
reported as a value with a range that covered the potential
variation in the year-of-formation, leading to a range in the
k-values. Extrapolation of the fitted functions provided
estimates of lifespan for some shells that extended into the
pre-bomb period.
Results
Bomb radiocarbon values and dates
Measurements of D
14
C from the white abalone shell-sample
series ranged, as expected, from pre-bomb to post-bomb
(Table 1). Determination of dates associated with the values was
Fig. 2. Cross-section of an abalone shell showing how the shell material is structured (modified from
Bevelander 1987). The outer prismatic layer was targeted for sampling because of its greater time-
specificity, relative to the more splayed growth pattern of the nacreous layer. A small block was cut from the
prismatic layer for sample processing (scale bar ¼,1 mm).
1032 Marine and Freshwater Research A. H. Andrews et al.
a combination of known-age edge material and alignment to the
reference series (Fig. 4). Lowest values were from two shells
that were living during the pre-bomb period (WA 1972-1 and
WA 1972-2), with values that were similar to the pre-bomb
reference abalone D
14
C data (mean s.d. ¼83.7 5.0%;
n¼6). The greatest D
14
C values were from the most recently
collected shell (WA 1996), with a mean of 72.3%, being
equivalent to the peak values recorded for yelloweye rockfish,
but less than the other references. Temporal correlation was
somewhat arbitrary for this shell because of the regional
variability in the D
14
C signal and is considered an age estimate.
The known-age D
14
C values from the edge of shells provided
reference points that supported projection of D
14
C values to the
period of the first rise in D
14
C(Table 2). The D
14
C values from
two shells provided a good fit to the reference chronology
(WA 1967, WA 1972-2), one being slightly lower than expected
(WA 1972-3), and one indicating that the collection date was not
accurate (WA 1972-1; Fig. 4). Edge material from shells
WA 1967 and WA 1972-2 provided D
14
C values similar to the
reference chronology, with the highest confidence in terms of
providing age and growth characteristics. The D
14
C value from
the edge of specimen WA 1972-1 could not be assigned a year of
formation of 1972 because the D
14
C value was too low
(61.0 3.9%) relative to the reference curve and was assigned
a year-of-formation of 1961 (based on the Loess curve). Further
adjustment to the uncertainty of selecting 1961 (95% CI) was
not considered because the value of the sample series became
useful only as pre-bomb reference material. Apex material from
the 1996 shell provided D
14
C values that could be attributed to
a year-of-formation associated with near-peak D
14
C values, but
could have been younger based on the regional D
14
C reference
variation. In addition, greater uncertainty in the collection year
(2 years) was revealed for WA 1996 after analyses had been
performed. Each of the D
14
C values fitted to the reference
chronology using the Loess curve and each was given a range
for the potential period of formation based on the 95% Loess
CI, with the exception of WA 1972-1, as stated previously
(Fig. 4).
Regional D
14
C reference
Compilation of the regional D
14
C reference from otoliths, DIC
and known-age abalone shell material led to a pattern of rapid
rise in D
14
C, with highly variable post-bomb amplitude (Fig. 3).
Measured D
14
C values from known-age shell material (collec-
tion years 1948–1979) ranged as suspected from fairly well
constrained pre-bomb levels (mean s.d. ¼83.7 5.0%)to
elevated and variable post-bomb decline values (Table 2). Rise
values were in close agreement with the otolith records in the
early 1960s and provided support for the alignment of samples
from other shells of unknown age. Peak and post-peak values
were variable and differed on the order of 100%for similar
dates. This difference was similar to what was documented by
⫺140
⫺120
⫺100
⫺80
⫺60
⫺40
⫺20
0
20
40
60
80
100
120
140
1935 1940 1945 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995
Δ
14
C (‰)
Year of formation
Yelloweye rockfish (NE Pacific)
Pacific halibut (NE Pacific)
Half Moon Bay – Seasonal DIC
SCB – Regional DIC
SCB – Abalone (reference)
Fig. 3. Measured D
14
C values from known-age white abalone shell material, plotted with a compilation of regional
D
14
C reference records from various sources along the coastal margin of the north-eastern Pacific Ocean. Results from
abalone shell were similar in the timing of the rise and amplitude of D
14
C when compared to the closest comprehensive
D
14
C records (derived from otoliths of two fishes in the Gulf of Alaska). In addition, a high degree of post-peak D
14
C
variability was documented from the shell material. Other D
14
C records of interest were from within or near the Southern
California Bight (SCB) as individual measurements of dissolved inorganic carbon (DIC) from seawater. The yelloweye
rockfish data have been fitted with a Loess curve (spline interpolation smoothing parameter ¼0.5, two-parameter
polynomial; SigmaPlot 11.2), to provide a central distribution reference for the D
14
C data series with a 95% CI.
Bomb radiocarbon dating of white abalone Marine and Freshwater Research 1033
⫺140
⫺120
⫺100
⫺80
⫺60
⫺40
⫺20
0
20
40
60
80
100
120
140
1935 1940 1945 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995
Year of formation
Yelloweye rockfish (NE Pacific)
Pacific halibut (NE Pacific)
Half Moon Bay – Seasonal DIC
SCB – Regional DIC
SCB – Abalone (reference)
WA-1967
WA-1972-3
WA-1972-2
WA-1972-1
WA-1996
Δ
14
C (‰)
Fig. 4. Bomb radiocarbon plot of results from large white abalone shells, with compiled D
14
C reference data from
various sources (see Fig. 3). White abalone D
14
C data were plotted based on collection-year data and diagnostic D
14
C
values were fitted to the rise in D
14
C. Beyond these values (pre-1958), the measured D
14
C values from other parts of the
shell were plotted in time using the calculated von Bertalanffy growth functions (VBGF) for each shell (Table 2).
Table 2. Southern California Bight D
14
C reference series from abalone shells
Collection numbers are for Santa Barbara Museum of Natural History. Shell size is maximum shell length (MSL) and radiocarbon results are from edge
material (prismatic layer) taken near MSL. Radiocarbon values, reported as Fraction modern (Fm) and D
14
C, are adjusted to collection date or year and
corrected for d
13
C fractionation. Three shells in this set were sampled further for a D
14
C time series used in bomb radiocarbon dating (Series). WA ¼white
abalone (Haliotis sorenseni) and RA ¼red abalone (H. rufescens). n.m. ¼Not measured
Shell ID (collection #) Collection location and date or year Water depth MSL (mm) Fraction modern D
14
C(%)
WA 1948 Santa Barbara Island 5 fathoms 184 0.9148 85.0 3.8
(116192) August 1948 (9 m)
WA 1952 San Clemente Island 70 feet 102 0.9188 88.4 3.5
(122917) September 1952 (21 m)
WA 1955 San Clemente Island Unknown 170 0.9130 87.6 2.9
(129843) May 1955 0.9205
D
80.1 3.1
RA 1958
A
Santa Cruz Island Unknown 211 0.9255 75.4 3.2
(130608) 2 December 1958 0.9150
D
85.9 3.1
WA 1964 Channel Islands Unknown 148 0.9880 3.7 3.4
(349096) 1964 0.9917
D
10.0 3.2
WA 1965 Santa Rosa Island Unknown 154 1.0000 1.8 3.7
(352559) 1965 0.9980
D
3.8 3.2
WA 1966 (Series) Santa Catalina Island Unknown 151 1.0612 59.0 3.5
(352560) December 1966 1.0542
D
42.0 3.4
WA 1972-2 (Series) Point Loma, San Diego 10–20 m 193 1.0384 27.3 3.7
(352558)
B
1972
WA 1972-3 (Series) Point Loma, San Diego 10–20 m 165 1.0166 6.6 3.5
(352558)
B
1972
WA 1972-4 Point Loma, San Diego 10–20 m 135 1.1163 113.0 3.4
C
(352558)
B
1972 1.1164
D
113.0 3.8
C
RA 1976 Point Conception Unknown n.m. 1.0072 4.0 3.4
(352503) 31 December 1976
RA 1979 Oil Platform off Gaviota 55 feet n.m. 1.0957 91.8 4.3
(2397) 3 October 1979 (17 m)
A
Noted as ‘presumed hybrid.’
B
All shells under the same museum accession number.
C
Plotted as 112.0%and 114.0%to provide visible separation of the two measurements in figures.
D
Replicate sample.
1034 Marine and Freshwater Research A. H. Andrews et al.
Robinson (1981), which is the only continuous DIC record that
provides a measure of annual variation as a result of seasonal
changes (Fig. 3).
Growth estimates
Von Bertalanffy growth functions fitted to the period of shell
formation and the change in shell length provided a range of
growth scenarios for each shell (Table 3). Because there was a
potential range in the year-of-formation for what was considered
the diagnostic D
14
C values, the result was a predicted k-value
or growth-constant range for each shell. Growth constants
provided an indication that she ll growth was highly variable, with a
range of 0.105–0.305 year
1
(uncertainty of 0.074–0.368 year
1
).
The smallest and youngest animal (WA 1967) shell grew
most rapidly and the slowest-growing were the two largest
shells (WA 1972-2 and 1996). An investigation of the effect of
changing L
N
from 200-mm MSL by 5mm onk-values for each
shell revealed only minor differences in k-values. These minor
differences are not reported because of greater uncertainty asso-
ciated with the year-of-formation chosen from the Loess 95% CI.
Age estimates
From the D
14
C data and the estimated growth parameters, age
was estimated for all of the shells with post-bomb collection
years (Table 4). Age was extrapolated for the other two shells
(WA 1972-1 and 1972-2) based on information from other shells
or the range in fitted k-values. For specimen WA 1972-1, the
collection year was not in agreement with the year applicable for
the measured D
14
C at the shell edge (assigned a birth year of
1961); hence, an assumption was made that the shell had a
growth trajectory similar to that of WA 1972-2 (shell size and
structure were similar and the shells were collected from the
same location), resulting in a calculated age of ,25 years.
The utility of this projection is strictly for establishing a
pre-bomb record for white abalone from the region, and the
age estimate is not considered critical for this reason. For WA
1972-2, a projection from the known period of formation (outer
43 mm of shell in ,12 years) to the MSL led to an estimated age
at collection of 24 years. Each of these age determinations has
a relatively high margin of uncertainty; however, this is likely to
be a conservative margin. More precise ages were determined
Table 3. Diagnostic portions of shell growth providing measures of age and growth
Formation time was calculated based on the difference between the known collection date and a temporal reference point in the D
14
C reference series that
corresponded to the measured D
14
C level (centred on the Loess curve). The first value for each is the collection year and second was determined from the fit to
the Loess curve. The uncertainty of the D
14
C reference dates is reflected in the calculated formation time as a range in parentheses. For k,L
N
was chosen as
210-mm MSL from Tutschulte and Connell (1988)
Shell ID D
14
C(%) Year of formation
A
Formation time (years) Length change (mm) k(year
1
) (range)
B
WA 1967 59.0 3.5 1966.9 4.1 151 0.305
42.0 3.4 (3.4–5.4) (0–151) (0.230–0.368)
42.0 4.0 1962.8
(þ0.8/1.3 years)
WA 1972-2 27.3 3.7 1972.5 12.0 43 0.105
66.5 3.5 1960.5 (11.9–23.9) (150–193) (0.074–0.120)
(þ1.5/5.0 years)
WA 1972-3 6.6 3.5 1972.5 10.7 165 0.144
54.2 3.4 1961.8 (9.5–12.5) (0–165) (0.123–0.162)
(þ1.2/1.8 years)
WA 1996 n.m. 1996 2 years 27.0 200 0.113
76.6 3.5 1969.0 (22.0–30.5) (0–200) (0.100–0.139)
44.7 3.7 (þ3.0/1.7)
A
Year of formation determined from either year of collection or based on a diagnostic fit of a given rise or peak D
14
C value to the Loess reference curve.
B
L
N
was chosen as 210 mm MSL from Tutschulte and Connell (1988).
Table 4. Summary of estimated age data for the white abalone shells used in the study
Because collection year and shell size varied considerably, each shell had unique circumstances in making the age estimations. Specifically, 1972-1 was
extrapolated, after reclassifying with a collection year of 1961, to provide a pre-bomb D
14
C reference series that was in agreement with other shell material of
known age
Shell ID Year of collection Birth year MSL (mm) Shell age
WA 1967 1966.9 1962.8 (1961.5–1963.6) 151 4.1 (3.4–5.4)
WA 1972-1 1961
A
1935.9 (1925.3–1939.0)
A
195 25.1 (22.0–35.7)
A
WA 1972-2 1972.5 1948.6 (1938.5–1951.6)
B
193 23.9 (20.9–34.0)
B
WA 1972-3 1972.5 1961.8 (1960.0–1963.0) 165 10.7 (9.5–12.5)
WA 1996 1996 1969.0 (1967.4–1972.0) 200 27.0 (22.0–30.5)
A
Selected median year from Loess curve fit and extrapolated age assuming growth characteristics similar to those of 1972-2.
B
Extrapolated age and growth, based on diagnostic fit to the rise of D
14
C value at 150 mm.
Bomb radiocarbon dating of white abalone Marine and Freshwater Research 1035
for shells with D
14
C values in the diagnostic portion of the
reference curve and measured from the apex of the shell,
encompassing the full lifespan. The estimated age of these shells
was 4, 11 and 27 years old for shell lengths of 151-mm, 165-mm
and 200-mm MSL (WA 1967, 1972-3 and 1996), respectively.
Given these estimates, lifespan of white abalone can approach
30 years.
Discussion
Age and growth estimates
Bomb radiocarbon dating has provided estimates of age for a
collection of white abalone shells and the results are con-
sistent with those of earlier studies. Previous studies have
indicated that early growth is well documented up to 10
years of age and an extrapolation of those data to the max-
imum size (210-mm MSL) provided a lifespan estimate of
,35 years (Tutschulte and Connell 1988). The largest shell
in the present study was 10 mm smaller than the estimated
maximum size for white abalone. This implies that lifespan
could be greater than 30 years, as was predicted from the
present work, and that a maximum lifespan of 35 years is
reasonable.
Abalone are known to exhibit individual variation in growth
(Sainsbury 1980), which can affect both k(some individuals
growing slower or faster) and L
N
(allowing for differences in
the mean final size for the population). A greater estimate of
lifespan is supported when alternative growth scenarios are
considered. For example, the largest specimen we examined
had an estimated k¼0.100–0.139 year
1
and could be 27–32
years old at 97% of the maximum asymptotic length (L
N
5
210-mm MSL). If L
N
is increased by 5 mm in MSL, the time
required to reach 97% of maximum size could be up to 37 years.
Given that the von Bertalanffy growth function and other
measures of growth tend to overestimate early growth rates
(Yamaguchi 1975,Rogers-Bennett et al. 2007), it is suggested
that lifespan is close to 30 years. Another consideration is that
shell loss has been documented in tag–recapture studies of other
species of abalone, with the inclusion of negative growth data
resulting in an increase in the von Bertalanffy k-value (Button
and Rogers-Bennett 2011). However, this would affect only
estimates of projected age and would lead to an underestimate of
the maximum age; shell loss would not change age estimates
from measured D
14
C values.
The age determinations from the smaller shells in the present
study can be further evaluated based on observations of growth,
flexibility in the iterative fit of the von Bertalanffy growth
functions, and potential variations in regional D
14
C records. The
WA 1967 shell was perhaps the most informative in terms of
indicating a maximum growth-rate potential for white abalone.
The lower limit for growth is well defined by the rise in D
14
Cat
k¼0.230 year
1
. On the other extreme, it is likely that the
youngest age estimate for this shell (3.4 years) is not possible
because growth would have had to occur much faster than what
has been observed in other empirical studies (Tutschulte and
Connell 1988); hence, the growth trajectory for this 151-mm-
MSL shell can be more realistically described as k¼0.230–
0.305 year
1
and age of ,4–5 years. Similar scenarios can be
applied to the other shells where iterative fits of von Bertalanffy
growth functions are applied to a conservative year-of-formation
uncertainty (95% CI). However, this kind of speculation high-
lights the need for a better regional D
14
C record. At this
time, the D
14
C time series from yelloweye rockfish and Pacific
halibut from the Gulf of Alaska provides the closest references
to use for calibration purposes. Although it is desirable to define
the characteristics of the D
14
C changes in the SCB, it is likely
that the rise period is similar for coastal areas of the north-
eastern Pacific Ocean. In support of this argument is the
magnitude and timing of the measured D
14
C values from edge
material from the WA 1967 specimen, as well as the other
reference abalone D
14
C data. Although it is clear that post-bomb
D
14
C variation is great for the region, it is likely that the
D
14
C rise in the early to mid-1960s was well constrained.
Bomb radiocarbon values and regional references
Pre-bomb values can be used to establish a D
14
C threshold to
understand what D
14
C values represent the initial D
14
C rise in
the SCB. The shell that was determined to have a 1961 birth year
provided a long time series of pre-bomb values for the region.
Given the calculated growth trajectory for this shell, the record
of pre-bomb D
14
C values was estimated to extend back 22–36
years from 1961. Despite the shell-age uncertainty and the year
of formation of the extracted material, it is certain that this series
of samples is representative of D
14
C levels before significant
atmospheric testing. The mean pre-bomb D
14
C value for this
series (84.4 8.5%, s.d.) was consistent with the regional pre-
bomb shell reference values (83.7 5.0%), and greater than
pre-bomb D
14
C levels in the Gulf of Alaska (Kerr et al. 2005).
The elevated trend in pre-bomb D
14
C for the SCB is interme-
diate to subtropical pre-bomb levels of the northern Pacific
(Druffel 1987), and most similar to regions affected by strong
upwelling (i.e. Galapagos, Druffel 1981). Given a combined
record of all pre-bomb abalone shell data (mean ¼83.5%,
n¼13), the year-of-formation for shell material with a
D
14
C value slightly exceeding 2 s.d. of this mean (.70.9%)
can be classified as the first rise of D
14
C(Kerr et al. 2005). This
observation and the temporal alignment are further supported
by the known-age shell samples that are consistent with the
D
14
C rise in the mid- to late 1960s.
This analysis of radiocarbon in white abalone shell material
is subject to multiple sources of imprecision. The first is the
highly variable nature of D
14
C measured in the post-bomb
abalone shell material, consistent with the dynamic marine
environment of the SCB. The coastal regions of the north-
eastern Pacific Ocean are prone to strong and variable upwell-
ing, leading to complex seasonal and annual cycles that ebb and
flow with deep-water sources depleted in
14
C(Robinson 1981;
Rau et al. 2001;Haltuch et al. 2013). Despite the seasonal
variability, the temporal specificity of the D
14
C rise is evident
among records, and was supported by known-age shell material.
The first rise D
14
C values, once defined relative to regional pre-
bomb levels, remain diagnostic and are most informative for
assigning a year-of-formation with some level of quantitative
uncertainty (95% CI), as was the case in the present study.
The second source of imprecision in our analysis is the use of
the two-parameter von Bertalanffy growth function to model
growth of the white abalone. A variety of alternative growth
1036 Marine and Freshwater Research A. H. Andrews et al.
models have been devised and evaluated to model individual
growth, and these models vary in the number of parameters
that are estimated and their assumptions about individual
growth dynamics. Rogers-Bennett et al. (2007) analysed the
relative quality of a suite of growth models to describe mean
length-at-age and found that the three-parameter logistic and
Richards’ functions provided a comparable and superior fit to
the von Bertalanffy growth function to describe red abalone
length-at-age. Because of our desire to perform the iterative
fitting procedure by altering a single model parameter, and
fixing the value of L
N
, and its computational simplicity, we
performed the analysis using the two-parameter variant of the
von Bertalanffy growth function. The use of such a parsimoni-
ous model is justified, given the limited data available for the
endangered white abalone.
The present work represents an expansion of radiocarbon
ageing methods to the SCB and it is therefore desirable to
understand how bomb radiocarbon has entered this environ-
ment. Records from Baja California and the north-eastern
Pacific aid in our understanding of the potential variability,
but also the temporal specificity of the D
14
C rise and decline
over time (e.g. Frantz et al. 2000;Ebert and Southon 2003;Piner
et al. 2005;Andrews et al. 2007;Haltuch et al. 2013). The
determination of age for the 1996 white abalone shell was based
on a fit to peak D
14
C values from the yelloweye rockfish record,
with a notable drop in D
14
C levels for the more recent shell
growth. Within 61-mm MSL, or .3 years according to
Tutschulte and Connell (1988), the change in D
14
C was a
decrease of 20–30%. Other records from the northeastern
Pacific are not as well defined in terms of peak D
14
C values
and timing. Some provide records that do not decline substan-
tially post-bomb, making age determinations for near-peak
D
14
C values dubious, imprecise or impossible (e.g. see post-
bomb records in Frantz et al. (2000) and Piner et al. (2005)). The
D
14
C signal in the SCB appears to follow a rapid rise that is
similar in timing to other records, but is followed by a compli-
cated post-bomb decline that is punctuated with strong inter-
annual and seasonal oscillations.
Implications of white abalone age
Bomb radiocarbon dating of white abalone shells has provided
estimates of age, growth and lifespan from large adult shells and
can be related to previous work. The use of empirical evidence
provided sound age estimates, with a marginal level of uncer-
tainty where no age was previously determined. Growth was
variable among shells, with potential k-values ranging from
,0.105 to 0.305. The lifespan of animals 151-mm to 200-mm
MSL was ,4–27 years old. Lifespan estimates of nearly 30
years made in previous studies are consistent with the findings of
the present study. These independent estimates of age provide a
basis for greater confidence in the execution of proposed mea-
sures in the ESA white abalone recovery plan (National Marine
Fisheries Service 2008).
The goal of the ESA recovery plan is to increase the
abundance of white abalone to viable and self-sustaining
levels. The results of the present study will help in achieving
the goal of increasing the abundance of white abalone by
providing information for the following two recovery actions:
(1) developing and refining population data and demographic
population-viability models that will be used to evaluate threats,
population trends and make predictions about future trends
following restoration activities; and (2) guiding the protocols
for brood-stock collection as a part of a captive propagation and
enhancement program. In the first instance, the age, growth and
lifespan estimates generated in the present study can be incor-
porated into predictive models that will help identify factors that
have the greatest effect on population growth following restora-
tion activities, such as aggregation or enhancement using
captive-reared animals. Trustworthy estimates of lifespan, com-
bined with an understanding of the reproductive potential of
individuals over the lifespan, are needed to choose an enhance-
ment strategy that will maximise population growth until self-
sustaining densities are attained. Future studies should focus on
understanding what factors control the reproductive potential of
white abalone. In the second instance, the estimated maximum
shell length, corresponding age estimation and lifespan estimate
may guide the process for selecting which individuals are the
best candidates for brood-stock collection. Animals that are
large (.190-mm MSL) and solitary are likely to be approaching
their maximum age and may have very low reproductive
potential; thus, these individuals could be good candidates.
Given that recent surveys have suggested that the wild white
abalone population is composed primarily of large (.100-mm)
individuals (Butler et al. 2006;Stierhoff et al. 2012), the age
data presented here provide an indication that natural mortality
is likely to occur for these animals in less than 20 years. This
highlights the critical and timely need for restoration and
implementation of the white abalone recovery plan.
Acknowledgements
Dan Geiger and Paul Valentich-Scott (Santa Barbara Museum of Natural
History) and Tom McCormick (Proteus SeaFarms) provided important
shells. Radiocarbon measurements were made at Lawrence Livermore
National Laboratory and Woods Hole Oceanographic Institution. Thanks go
to Dan Richards and David Kushner (National Parks Service, Channel
Islands National Park), Ian Tanaguchi (California Department of Fish and
Wildlife), Lindsey Groves (Los Angeles County Museum), Terry Gosliner
and Robert Van Syoc (California Academy of Sciences), and others involved
in locating shells with known collection dates. We thank the California
Department of Fish and Wildlife for supporting Laura Rogers-Bennett. This
is a publication of the Bodega Marine Laboratory, University of California,
Davis. Moss Landing Marine Laboratories provided part of the laboratory
support. We thank Robert Humphreys, Edward DeMartini (NOAA Fisher-
ies), and anonymous reviewers for editorial comments. This publication was
prepared under NOAA Grant Numbers NA04OAR4170038 and OCA09010,
California Sea Grant Project Numbers R/F-202 and R/FISH-214PD, through
NOAA’s National Sea Grant College Program, USA Department of
Commerce, and was supported in part by the California Natural Resources
Agency.
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Bomb radiocarbon dating of white abalone Marine and Freshwater Research 1039
