Aranha et al., Primnoa pacifica growth and paleoceanography
1
Growth rate variation and potential paleoceanographic proxies in Primnoa pacifica:
insights from high-resolution trace element microanalysis.
Renita Aranhaa1,, Evan Edingera,b,c2, Graham Laynea, Glenn Pierceyd
a
Department of Earth Sciences, Memorial University of Newfoundland, St John’s,, NL
A1B 3X5, Canada, renitaaranha@gmail.com, eedinger@mun.ca, gdlayne@mun.ca,
b
Department of Geography, Memorial University of Newfoundland, St John’s, Canada,
NL A1B 3X9
c
Department of Biology, Memorial University of Newfoundland, St John’s NL A1B 3X9,
Canada
d
CREAIT, Memorial University of Newfoundland, , St John’s, NL A1B 3X9, Canada,
glennp@mun.ca
1Current Address: Divestco Inc 400, 520 – 3rd Avenue SW Calgary, Alberta, T2P 0R3
2: Corresponding author. +1-709-864-3233, fax +1-709-864-3019
Abstract:
Red tree coral, Primnoa pacifica, is one of the more common habitat-forming deep-sea
gorgonian corals in the Northeast Pacific Ocean, growing in colonies up to 2 m high and
living decades to hundreds of years. Growth characteristics of Primnoa pacifica were
studied in Dixon Entrance, northern British Columbia, and the Olympic Coast National
Marine Sanctuary, Washington State, USA, based on samples collected in July 2008. To
minimize the impact of scientific sampling on coral populations, only dead coral
skeletons and dislodged live corals were collected. Ages and growth rates were measured
using band counts, and checked against AMS-14C ages of gorgonin rings. Ba/Ca, Mg/Ca,
Aranha et al., Primnoa pacifica growth and paleoceanography
2
Na/Ca and Sr/Ca ratios in the calcite cortex were measured using radial Secondary Ion
Mass Spectrometer (SIMS) transects with a spot size of < 20 m and separation distance
of 25 m. Growth banding was consistent in width between the central mixed zone
consisting of calcite and gorgonin and the dominantly calcite cortex. Average annual
radial growth rate of the nine corals analysed ranged from 0.23 to 0.58 mm/yr, with an
average growth rate of 0.32 mm/yr in Dixon Entrance and 0.36 m/yr in OCNMS. These
growth rates are slightly higher than P. pacifica growth rates from the Gulf of Alaska, and
more than 4 times the growth rates of sister species P. resedaeformis in the Northwest
Atlantic. Primary productivity is likely a more important driver of geographic variation in
Primnoa growth rates than temperature or current strength. Both Dixon Entrance and
OCNMS are areas with high primary productivity and strong tidal currents.
Lack of
post-Atomic Bomb radiocarbon in all but one of the gorgonin samples, and long
radiocarbon reservoir ages in the Northeast Pacific, made radiocarbon-based verification
of coral ages and growth rates difficult due to wide errors in calibrated age estimates.
Mg/Ca and Sr/Ca ratios were inversely correlated in two of the three corals analyzed, and
showed evidence of interannual variation. Mg/Ca ratios ranged from 70-136 mmol/mol,
and Sr/Ca ratios from 2.041–3.14 mmol/mol. Previously published relationships between
gorgonian calcite Mg/Ca and seawater temperature yielded average temperatures
matching ambient measurements, but the intra- and inter-annual variation in apparent
temperature based on Mg/Ca ratios was more than double the observed variation in
modern seawater temperature ranges in the region. Annual variation in Mg/Ca and Sr/Ca
could be related to seasonal changes in precipitation efficiency, which is likely a function
Aranha et al., Primnoa pacifica growth and paleoceanography
3
of short-term fluctuations in coral growth rate, in turn related to variation in primary
productivity. Seasonal and interannual variations in food availability, driven by primary
productivity, may affect skeletal growth rate, hence in Mg/Ca and Sr/Ca ratios. Primnoid
coral skeletal microgeochemistry probably records temporal changes in both temperature
and primary productivity.
1 Introduction:
Primnoid gorgonians are important long-lived habitat forming corals in cold-water
coral provinces world-wide. Their size and longevity make them highly vulnerable to
damage from fisheries and other seafloor disturbances.
Primnoa are of interest
biologically for their role in structuring habitat (DuPreez and Tunnicliffe 2011), and
geologically for their calcite-protein skeletons, which may be useful as paleoceanographic
archives (Sherwood et al., 2005a; b; 2011). Further knowledge of their growth rates and
longevity, and of regional variation in their growth rates, can be important in
understanding recovery times from natural or anthropogenic disturbances, and designing
appropriate conservation strategies.
High-resolution studies of their skeletal
geochemistry can help to evaluate their utility as paleoceanographic archives. Here we
present growth and paleoceanographic records in the most common Primnoa of the
northeast Pacific Ocean, Primnoa pacifica.
Primnoa pacifica, like its Atlantic counterpart Primnoa resedaeformis, has a
skeleton composed of three distinct growth zones. It has an inner central rod, a middle
zone composed of both calcite and gorgonin, and an outer calcitic zone, the cortex, which
contains very little gorgonin (Sherwood et al., 2005b).
Aranha et al., Primnoa pacifica growth and paleoceanography
4
Smaller colonies only display two growth zones, the calcite cortex is absent. The
growth bands can be clearly seen as intercalations of calcite and gorgonin in the second
growth zone, and by changes in gorgonin colouration that remain visible after dissolution
of the calcite (Risk et al., 2002). More diffuse growth bands can also be recognized in the
calcite cortex. These growth bands are known to be annual in Primnoa pacifica (Andrews
et al., 2002) and in its Atlantic sister species Primnoa resedaeformis based on radiometric
dating (Sherwood, 2005c), and annual banding is also recorded in the calcitic cortex
(Sherwood, 2005c). Primnoids are known to have long life spans (up to 700 yrs;
Sherwood et al., 2006). Analysis of δ18O and Sr/Ca in the calcite skeletons of Primnoa
resedaeformis has suggested that growth related kinetic effects might have an impact on
these isotopic and elemental ratios (Heikoop et al., 2002). Preliminary studies on Primnoa
resedaeformis indicate that the variation in Mg/Ca in its skeleton may be controlled by
temperature (Sherwood et al, 2005a), and several authors have investigated potential
paleoceanographic records in primnoids, bamboo corals (Isididae), and other cold-water
gorgonian corals (e.g. Roark et al. 2005, Thresher et al., 2004, 2010, Hill et al., 2011,
2012). Mg/Ca and Sr/Ca in reef-forming tropical coral skeletons are very commonly used
as proxies for sea surface temperatures (e.g., Mitsuguchi et al., 1996; Cohen et al., 2006;
Azmy et al., 2010). Na/Ca and Ba/Ca also vary systematically in many types of marine
biomineralization (Boyle, 1981; Lea et al., 1989; Lea & Boyle, 1990; Amiel et al., 1973),
although their behaviour during skeletal growth, and their utility as proxies for seawater
temperature or chemical variations, has been examined in far less detail in the available
literature.
Aranha et al., Primnoa pacifica growth and paleoceanography
5
Primnoids’ longevity, annual skeletal banding and wide geographic distribution
make them potentially interesting from the standpoint of paleoceanography. The purpose
of this paper is to measure the growth rates and longevity of P. pacifica in two locations,
to investigate regional variation in the growth rate of P. pacifica and P. resedaeformis ,
and to assess the paleoceanographic significance of trace element (Mg/Ca, Sr/Ca Ba/Ca,
and Na/Ca,) variation in the calcitic portion of Primnoa pacifica skeletons. Since P.
pacifica is known to be a habitat forming deep sea coral (Andrews et al., 2002, DuPreez
and Tunnicliffe 2011); an accurate determination of its growth rate is extremely important
in order to gauge habitat recovery time after damage from deep sea trawling and similar
disturbances.
2 Materials and Methods:
2.1. Study areas.
Dixon Entrance is a large elongate strait between Haida Gwaii, northern British
Columbia, Canada, and Southeast Alaska, USA (Figure 1). Dixon Entrance experiences
strong tidal currents, and hosts a lush fauna of deep-sea corals including gorgonians,
stylasterids, soft corals, sea pens, and rare antipatharians (Edinger et al. 2008; DuPreez
and Tunnicliffe 2011, Neves et al, this issue). Dixon Entrance was scoured during
Pleistocene glaciations, and strong tidal currents limit post-glacial sedimentation, thus
leaving winnowed glacial deposits on the sea floor in much of Dixon Entrance, along
with large glacial erratic boulders and glacially scoured bedrock (Barrie and Conway
1999). Learmonth Bank is a large granite massif in the western end of Dixon Entrance,
Aranha et al., Primnoa pacifica growth and paleoceanography
6
which hosts abundant Primnoa pacifica, both on bedrock and on glacial erratic boulders
(Figure 2A-B) (Edinger et al., 2008, DuPreez and Tunnicliffe 2011).
The Olympic Coast National Marine Sanctuary (OCNMS) sits at the northwest corner of
Washington State, USA, facing Vancouver Island, British Columbia, Canada, across the
Strait of Juan de Fuca (Figure 1B).
2.2 Field collection of specimens:
Several dead colonies of Primnoa pacifica were collected in July 2008 from Dixon
Entrance and the Olympic Coast National Marine Sanctuary (OCNMS) using the
Remotely Operated Vehicle (ROV) ROPOS deployed from the Canadian Coast Guard
ship John P. Tully (Table 1 Figures 1, 2). In Dixon Entrance, corals were collected from
Learmonth Bank and surrounding glacial deposits (Figure 1A, Table 1). In OCNMS,
corals were collected in 266-312 m water depth near the head of Juan de Fuca Canyon
(Figure 1B, Table 1). The specimens were collected using the ROV manipulator arms and
were measured, photographed, and frozen immediately after collection (Figure 2).
2.3 Growth rate estimation:
The radial growth banding in the mixed growth zone (consisting of alternating
gorgonin and calcite) of P. pacifica can be observed quite clearly in polished crosssections when photographed under UV light (Sherwood et al., 2005b; c). Since these
growth bands are known to be annual (Andrews et al., 2002, Sherwood et al., 2005c)
longevity estimates were made by counting the number of bands in the mixed growth
Aranha et al., Primnoa pacifica growth and paleoceanography
7
zone. Three independent readers counted rings in this zone for each colony. The average
number of bands for each colony was then divided by the length of the traversing radius
of this zone only to obtain the average annual radial growth rate. In order to determine
longevity, the average annual growth rate was extrapolated over the length of the whole
radius (including the calcite cortex region). Axial growth rates could not be determined
accurately as most colonies were broken and fragmented after death and before
collection.
To better enumerate the banding in the calcite cortex region, cross sections from
the base of the colonies were mounted on 25mm x 75mm or 50mm x75mm glass plates,
(depending on the size of the specimen) thin sectioned to 100 µm and petrographically
polished. These polished thin sections were then scanned with an HP Scanjet 3970
scanner using the greyscale ‘photograph’ setting at 2400 DPI resolution. This procedure
allowed growth banding to be observed and counted in the calcite cortexes of two of the
specimens used for detailed trace element profiling (R1162-0015, R1156-0016), using
essentially the same procedures as for the calcite-gorgonin middle zones. Growth rate in
the cortex appeared very similar to that in the calcite-gorgonin middle zone (Table 4),
validating the extrapolation of distance vs time in specimens where the cortex growth
banding is less clearly evident. Figure 3a shows an original raw photoscanned image of
specimen R1162-0015. Digital level pass and gradient filters were then applied to the
same image to emphasize the visibility of growth banding in the calcite cortex (Figure
3b).
Aranha et al., Primnoa pacifica growth and paleoceanography
8
2.4 Age validation by Radiocarbon dating:
Three colonies of P. pacifica were chosen for age validation by radiocarbon dating
(Figure 2C-H). These colonies were chosen for their relatively large calcite cortex region
and macroscopically non-degraded skeletons, features that would permit detailed SIMS
analysis of the calcite cortex along with corresponding
14
C dating of the gorgonin rings.
Calcite was not directed aged because carbon in the gorgonin layers is derived directly
from recently fixed organic carbon, hence tied to surface waters, while carbon in the
calcite layers records
14
colonies selected for
14
C of the ambient water mass (Sherwood et al. 2008b). All three
C dating were from the OCNMS. The colonies were dead when
collected, and had no soft tissue on their outer surface. It was initially assumed that the
colonies had died within the last 10 years; thus, it was expected that the colonies would
record the radiocarbon bomb spike that occurred between 1958 and the early 1970s. Basal
cross-sections of the three colonies were cut using a water-cooled diamond-blade rock
saw. Up to seven gorgonin rings were isolated from each cut sample using the method
described by Sherwood et al. (2005c).
separately and then
14
Each isolated gorgonin ring was packaged
C dated at the Center for Accelerator Mass Spectrometry at
Lawrence Livermore National Laboratory, California. 13C of the gorgonin samples could
not be measured concurrently, and the regional average 13C value of -15‰ was used for
all samples. The reported radiocarbon ages in Table 5 are in radiocarbon years using the
Libby half life (5568 years) and following the conventions of Stuiver and Polach (1977).
Aranha et al., Primnoa pacifica growth and paleoceanography
9
In order to convert the raw radiocarbon data into calendar years, a local
radiocarbon marine reservoir effect was calculated. The regional reservoir effect at the
OCNMS and southwestern Vancouver Island was calculated as 693±76 14C yrs, based on
the average reservoir effect documented for seven non-estuarine areas in the Northeast
Pacific close to the area of collection (Table 2) (McNeely et al., 2006). This reservoir age
was subtracted from the (δ13C -corrected) 14C age and this resultant age was converted to
calendar years using the Intcal09 calibration dataset (Reimer et al., 2009) via the CALIB
6.0 Radiocarbon Calibration Program (http://calib.qub.ac.uk/calib/calib.html). Ages are
reported in both 14C years and calibrated years relative to 1950.
2.5 Sample preparation for trace element analyses:
Cross sections between 3mm and 5mm in thickness were cut from the base of the
same three colonies selected for radiocarbon analyses, using a diamond-blade rock saw
cooled with water. These cross sections were then cut into transverse strips using a thin
kerf Buehler Isomet low speed diamond blade saw. The calcitic cortex portion was
subsequently isolated by simply breaking the gorgonin portion off by hand from the
transverse strips. A corresponding continuous strip of the calcitic cortex could then be
mounted into the 1” diameter SIMS sample ring - an aluminum ring with an outer
diameter of 1 inch (25.4 mm). The SIMS samples were embedded in the ring using
Buehler Epothin Epoxide (Resin:Hardener; 10:3.9). The casts were polished using silicon
carbide wet/dry sandpaper and then subsequently on a lapping wheel using 6µm diamond
polish, then manually polished 0.5 µm and 0.03 µm deagglomerated alumina.
10
Aranha et al., Primnoa pacifica growth and paleoceanography
2.6 Trace element analysis:
Trace element analysis followed the approach of Cohen et al. 2001. A Cameca
IMS 4f Secondary Ion Mass Spectrometer (SIMS) was used to perform high spatial
resolution (<25 µm) spot analyses of Na/Ca, Mg/Ca, Sr/Ca and Ba/Ca in detailed
traverses across the polished basal cross-sections from three specimens of P. pacifica. For
the Mg/Ca and Sr/Ca spot analyses reported here, typical internal precisions (1) were
better than 0.35% for Mg//Ca and 0.1% for Sr/Ca. SIMS also avoids the challenges
involving i) high analytical noise and ii) poor signal reproducibility associated with LAICP-MS and EPMA analyses documented by Sinclair et al (2005).
Individual SIMS transects began at the outermost edge of the calcite cortex region
and ended at the beginning of the gorgonin/calcite mixed zone. The traverses were 7 mm
to 11 mm long and individual SIMS spots were spaced 25 µm apart. Visible gorgonin
rings were avoided during analysis. Each coral consequently had between 303 and 367
SIMS analysis spots, depending on the length of the SIMS transect.
SIMS analyses utilized bombardment of the samples with primary
16
O- ions
accelerated through a nominal potential of 10 kV. A primary ion current of 3.0-6.0 nA
was critically focused on the sample over a spot diameter of 10-20 m.
Sputtered secondary ions were accelerated into the mass spectrometer through a
nominal potential of 4500 V. Secondary ions were energy filtered using a sample offset
voltage of -80 V and an energy window of 60eV to suppress isobaric interferences. Prior
to each analysis, the spot was pre-sputtered for 120 s. This was designed to eliminate
11
Aranha et al., Primnoa pacifica growth and paleoceanography
contamination from the 500Å gold coat and also to penetrate the damaged and
homogenized surface layer of the mechanically polished sample. Analytical craters were
thus typically < 20m diameter and <2 m deep at the completion of each analysis.
Each analysis involved repeated cycles of peak counting on
s),
42
Ca+ (2 s),
88
Sr+ (4 s),
138
23
Na+ (2s),
24
Mg+ (6
Ba+ (10 s), as well as counting on a background position
(22.67 Da; 1s) to monitor detection noise. A small wait time (0.2 – 0.5 s) was added
between each peak switch for magnet settling. For this study, 15 cycles of data were
collected over 546 s, for total analysis times of <10 minutes per spot, including presputtering. Typical signal on the 42Ca+ reference peak was 10,000-25,000 cps.
The Memorial IMS 4f is equipped with a High Speed Counting System (Pulse
Count Technology Inc.) that produces dark noise background of less than 0.03 cps (2
counts per minute) when used with an ETP133H discrete dynode electron multiplier.
Overall system dead time in pulse-counting mode is 14 ns. This system also produces
very low detection limits for the elements studied. The elemental detection limits based
only on the uncertainty in correcting for detector dark noise (0.03 cps) are typically 1 ng*
g-1 for Na, 2 ng*g-1 for Mg, 2 ng*g-1 for Sr and 2 ng*g-1 for Ba. The error of individual
spot analyses was estimated using the standard error of the mean of n cyclical
measurements of each ratio during an analysis (internal precision).
Detailed trace element profiles were plotted against a time axis (years before
death; year of death= 0). Time was calculated based on the average annual radial growth
rate. The smoothed data lines were produced using a second degree Savitzky-Golay type
Aranha et al., Primnoa pacifica growth and paleoceanography
12
generalized moving average with filter coefficients determined by an unweighted linear
least-squares regression and a second degree polynomial model.
2.7 Seawater temperature data:
Seawater bottom temperature data for the depths within the OCNMS region from
which the coral samples analyzed were collected were extracted from the World Ocean
Database 2009 (Boyer et al., 2009). All records within the bounding coordinates 48.0 –
48.5 N and 124.75- 125.5 W were collated, and analyzed within depth intervals of
260-280 m, 280-300 m, and 300-320 m. The mean, 95% confidence limits, minimum and
maximum observed temperatures, number of years of observation, and number of data
points for each depth class were calculated.
2.8 Paleotemperature estimation.
The temperature of the seawater in which the corals grew was estimated using the
empirically defined relationship between Mg/Ca and seawater temperature determined for
Primnoa resedaeformis in the NW Atlantic (Sherwood et al., 2005a).
(1) Mg/Ca (mmol.mol-1) = 5(±1.4) T (ºC) + 64(±10)
The paleotemperature estimate for all points was calculated using this equation, then the
curve was smoothed using a 5-point running average.
3 Results:
Aranha et al., Primnoa pacifica growth and paleoceanography
13
3.1 Growth rates:
All the growth rates listed in Table 3 and summarized in Figure 4 are calculated
from band counting results in the gorgonin/calcite mixed zone. The growth banding in the
calcite cortex was also clearly imaged in two of the six P. pacifica samples that were thin
sectioned and scanned (Figure 3). Therefore a separate growth rate estimate involving the
calcite cortex region was also possible for these samples. In both samples, the growth rate
in the calcite cortex was quantitatively identical to the growth rate in the gorgonin/calcite
zone in these samples (Table 4).
The average radial growth rate of Primnoa pacifica specimens from the Dixon
entrance is 0.323± 0.084 mm*yr-1 (1σ). The average growth rate of Primnoa pacifica
from OCNMS is 0.362±0.023mm*yr-1 (1σ). Published radial growth rates for the Gulf of
Alaska (Andrews 2002) and for P. resedaeformis in the Atlantic are plotted for
comparison (Figure 4)
3.2 Specimen age and radiocarbon validation of growth rates
Radiocarbon ages (Table 5) indicated that all of the rings analyzed, except sample
65-02 (A), were pre-bomb (i.e., formed prior to 1958). Almost all resultant reservoir
corrected radiocarbon ages were within error of each other. Sample 65-02 (A), the
outermost ring in specimen R1165-002, was of modern (post-bomb) age. The reservoir
corrected radiocarbon ages indicate that none of the samples died more recently than 30
years ago. Specimen # R1165-002 of P. pacifica has been dead for at least 30 years,
specimen # R1162-0015 has been dead for at least 45 years, and specimen R1162-0016
has been dead for at least 50 years (Figure 5).
Aranha et al., Primnoa pacifica growth and paleoceanography
14
In aggregate, the samples belonging to coral R1162-0015 showed a discernible
growth trend in radiocarbon age- with older radiocarbon ages for samples that were closer
to the center of the coral (Table 5, Figures 4, 5a). However, the slope of the growth
trajectories obtained through fitting the reservoir corrected radiocarbon ages for this
sample is steeper than that obtained from annual band counting (Figure 6a). Sample
R1165-0016 and Sample R1165-002 did not show any discernible trend in the
radiocarbon ages (Figure 6b,c).
3.3 Trace element analysis:
In the three specimens analyzed in detail by SIMS, the Sr/Ca varied between 2.04
and 3.14 mmol*mol-1, Mg/Ca varied between 70.6 and 136 mmol*mol-1, Ba/Ca varied
between 0.0036 and 0.0550 mmol*mol-1 and Na/Ca varied between 16.4 and 53.1
mmol*mol-1 (Table 6). Mean Mg/Ca and Na/Ca values are similar for Samples R11620015 and R1162-0016, but distinctly lower for Sample R1165-002. There was a weak, but
statistically valid, inverse correlation between Mg/Ca and Sr/Ca for samples R1165-0015
and R1165-0016, but a positive correlation for sample R1162-00 (Table 7).
All three samples analyzed showed some degree of cyclicity in the Mg/Ca and
Sr/Ca profiles (Figure 7). The Mg/Ca and Sr/Ca ratios in samples R1162-0015 and
R1162-0016 (Figure 7a,b) showed an obvious inverse correlation, both short-term and, in
R1162-0015, long term, as also reflected in Table 7. In Sample R1162-0015, a major
simultaneous spike in Mg/Ca and Sr/Ca occurred at the beginning of the profile (Figure
7a, between year 2 and 3). This spike corresponds to the SIMS analyses spots that passed
Aranha et al., Primnoa pacifica growth and paleoceanography
15
over a thin gorgonin ring. Because gorgonin has a higher concentration of many elements
than calcite, these analyses spots were excluded from the statistical analysis.
In both samples R1162-0015 and R1162-0016 (Figure 7a-b) a single large dip in
Sr/Ca values was observed, with a simultaneous spike in Mg/Ca. This excursion in trace
element values noted between year 6 and 7 in sample R1162-0015 and year 7 and 8 in
R11162-0016, was not associated with any specific contamination or growth feature in
the cross-section. It is very distinct from the profile obtained when the SIMS analyses
spot crossed the gorgonin ring; as there is a negative excursion in Sr/Ca values; not a
positive excursion as seen when the analyses crossed a gorgonin ring.
Ba/Ca and Na/Ca did not show any distinct cyclicity in the SIMS profiles of any
of the samples analyzed. This lack of cyclicity is probably due to the fact that Na/Ca and
Ba/Ca are not only dissolved in the skeletal material but are also present within the
skeleton as surface contaminants and/or particulate inclusions. Their patterns do not seem
as readily intepretable in P. pacifica as those observed for Mg/Ca and Sr/Ca.
3.4 Temperature records from the OCNMS region.
The World Ocean Database temperatrure records for the OCNMS region extend
from 1938 to 2006, and included 19 records between 260-279 m, 26 records between 280299 m, and 38 records between 300-320 m. The average temperatures ( 95% confidence
limits) observed in these three depth classes were 6.60.2, 6.40.2, and 6.40.1,
respectively (Figure 8). The complete temperature ranges recorded in each depth zone
were 5.6-7.6, 5.7-7.3, and 5.4-7.0, respectively. Intra-annual temperature variation in the
observed data from 280-320 m depth was less than 1C.
Aranha et al., Primnoa pacifica growth and paleoceanography
16
3.5 Paleotemperatre reconstructions.
Average calculated paleotemperatures in sample R162-0015 matched observed
bottom water temperatures in the 300-320 m depth range, but the range in calculated
paleotemperatures exceeded the observed range of temperatures by a factor of two
(Figure 9a). Calculated paleotemperatures matched observed temperatures in the first nine
years of the coral record in sample R1162-0016, but then dropped below observed
temperatures in the last five years (Figure 9b).
The calculated paleotemperatures in
sample R1165-0002 were appromiately 3C lower than the observed temperature at the
280-300 m depth range (Figure 9c).
Aranha et al., Primnoa pacifica growth and paleoceanography
17
4 Discussion
4.1 Growth rate variations:
The lowest radial growth rate recorded in this study was 0.22±0.09 mm.yr-1 for a
sample of P. pacifica from the Dixon entrance. This value closely matches the radial
growth rate (0.18± 0.03 mm,yr-1) for a colony of P. pacifica from Alaskan Dixon
Entrance studied by Andrews et al., 2002. The growth rates for P. pacifica reported here
thus support the conclusions of this previous study that these corals are slow to recover
from damage due to trawling and other disturbances.
Primnoa pacifica was formerly thought to be the same species as Primnoa
resedaeformis (Cairns & Bayer, 2009). The growth rates of Primnoa resedaeformis from
the Northwest Atlantic (Sherwood & Edinger, 2009) were more than 4 times lower than
the growth rate of Primnoa pacifica determined in this study. A log fit titled ‘model
maximum’ fitted through the four specimens of P.pacifica with the largest radius in
Figure 10; indicates the upper limit of growth rates in our study, along with log fit curves
for Dixon Entrance and OCNMS individually. Comparison of growth characteristics of
P. pacifica and P. resedaeformis from various locations, as compiled in Figure 10,
indicates that the samples from different locations follow similar logarithmic growth
trajectories, but with dramatically different radial growth rates.
Sherwood & Edinger (2009) attributed regional differences in growth rate of P.
resedaeformis in the North Atlantic to differences in the intensity of tidal currents,
suggesting that faster growth rates occur due to stronger tidal currents. Other possible
drivers of regional variation in gorgonian coral growth rates include temperature and
primary productivity.
Aranha et al., Primnoa pacifica growth and paleoceanography
18
The California undercurrent is active in the OCNMS region. The peak speed of
this current is 30 to 50 cm*s-1, similar to the currents in the Hudson Strait (~40 cm*s-1),
and considerably slower than the tidal currents in Dixon Entrance (90 cm*s-1, Crawford
and Thompson 1991) and the NE Channel (Sherwood & Edinger, 2009). Thus, current
velocity alone likely cannot explain the large difference in growth rate between the four
locations considered.
Similarly, temperature variation between the four locations does not appear to
explain the observed differences in growth rates. Average bottom temperatures (95%
confidence limit) at the depth zone from which corals were collected in the other three
areas were 5.60.1ºC (Dixon Entrance, 300 m), 4.00.1ºC (Hudson Strait, 400 m), and
6.10.4ºC (Northeast Channel, 400 m, Boyer 2009).
Primary productivity, and food supply, may best explain the differences in growth
rates among the areas compared. The California current system is one of the most
productive ecosystems in the world (Carr, 2002). Since growth of most deep sea corals is
dependent on POM flux, it is likely that the relative higher productivity in the NE Pacific
is the dominant driver of the higher growth rates of P. pacifica in comparison to P.
resedaeformis from the Hudson strait and NE channel (Jones & Anderson, 1994; Carr,
2002; Thomas et al., 2003b). Ongoing work quantitatively compares environmental
correlates of growth rate variation in several species of cold-water gorgonian corals
(Neves and Edinger 2012).
4.2 Radiocarbon dating:
Aranha et al., Primnoa pacifica growth and paleoceanography
19
Since the radiocarbon ages of most of the samples were pre-bomb, and within
error of each other, a precise age determination was not possible. It can be concluded,
however, that none of the samples died recently (within the past 30 years).
The
radiocarbon age ranges of R1162-0015 and R1162-0016 are mostly overlapping,
suggesting that the two corals may have lived at the same time (Figure 5), but the precise
times when the two corals lived are difficult to determine. The calcite layers of the two
corals likely overlapped the early part of the bottom temperature data reported in Figure
8. High precision dates of pre-bomb radiocarbon are unlikely to yield more precise age
estimates from the northeast Pacific, due to the large reservoir ages in that region.
4.3 Trace elements:
4.3.1 Primary controls on trace element variation in P.pacifica:
The skeletal morphology of Primnoa resedaeformis is indistinguishable from that
of Primnoa pacifica.. Sherwood et al. (2005a) analyzed the bulk skeletal composition of
several specimens of Primnoa resedaeformis from the North Atlantic and found that the
average bulk skeletal Mg/Ca varied between 86 and 118 mmol*mol-1. Comparison of
individual sample values to hydrographic temperature at their sites of collection yielded
the relationship Mg/Ca (mmol*mol-1) = 5(±1.4) T (ºC) + 64(±10).
Although the calculated average bottom temperature in one of the three samples
studied matched observed temperature, the range of variation in calculated bottom
temperatures within this coral far exceeded the observed temperature variation (Figure
9a).
The fact that calculated average bottom temperatures matched observed
temperatures in the beginning of sample R1162-0016 skeletal Mg/Ca record, but not at its
Aranha et al., Primnoa pacifica growth and paleoceanography
20
end, is confusing, as no similar large-scale change was recorded in the oceanographic
data. The skeletal Mg/Ca in samples of P. pacifica analyzed in this study varied between
70 and 136 mmol.mol-1, with averages of 103, 106 and 81 mmol.mol-1in the three samples
studied in detail. Applying the Sherwood et al. (2005b) temperature relationship to Mg/Ca
profiles obtained in this study implied temperature variation of ~3.5ºC to 12.4ºC in
sample R1162-0015, ~2.4ºC to 14.4ºC in sample R1162-0016 and ~1.2ºC to 5.6ºC in
sample R1165-0002. In OCNMS the highest ever temperature recorded at 300 m in the
past 70 years, by CTD casts, was 6.96ºC, and the lowest was 5.4ºC (Figure 8, Boyer et al.,
2009). Observed temperature variation alone cannot account for the range of observed
variation in Mg/Ca profiles of the samples studied herein. Thus subfossil Primnoa coral
skeletons may be more useful for indicating average temperatures at some time in the
past, and possibly for recording decadal-scale changes. High-amplitude-short wavelength
fluctuations in Mg/Ca and/or Sr/Ca ratios likely reflect growth rate variations responding
to changes in food availability, rather than highly-resolved annual or subannual
temperature variations (cf. Roark et al. 2005; Kuffner et al. 2012, see section 4.4, below).
The temperature dependence of Sr/Ca in most reef-forming tropical scleractinian
corals is between -0.08 and -0.10 mmol*mol-1/ºC (de Villiers et al., 1995; Gaetani &
Cohen, 2006). Cold water scleractinian corals like Lophelia pertusa have a more extreme
Sr/Ca sensitivity: approximately -0.18 mmol*mol-1 (Cohen et al., 2006). The temperature
dependence of Sr/Ca in abiogenic carbonate, however, is only -0.039 mmol*mol-1/º C
(Cohen et al., 2006).
If the variations of Sr/Ca record in the OCNMS Primnoa skeletons were attributed
solely to the observed temperature variation in the sampling areas, it would imply a
Aranha et al., Primnoa pacifica growth and paleoceanography
21
temperature dependence of approximately -0.74 mmol.mol-1/º C, seven times more
sensitive than observed in any tropical coral, and four times higher than that for the cold
water scleractinian L. pertusa. Factors other than temperature, most likely short-term
fluctuations in growth and calcification rate (cf. Kuffner et al. 2012) evidently exert a
major control on the variation in Mg/Ca and Sr/Ca ratios observed in P. pacifica.
4.3.2 Trace element ratio correlations and possible diagenetic effects
A significant inverse correlation between Mg/Ca and Sr/Ca was noted in the high
resolution trace element traverses of two of the three specimens of P. pacifica analyzed
(R1162-0015 and -0016; Figure 7a, b, Table 7).
In a third specimen (R1165-002; Figure 7c; Table 7) the Mg/Ca and Sr/Ca ratios
showed a significant positive correlation. R1165-002 shows several additional
differences, relative to R1162-0015 and -0016, in terms of its trace element profile. These
differences suggest diagenetic effects involving re-equilibration of the calcite skeleton
with seawater/shallow pore water before collection:
1) The mean Sr/Ca (2.39 mmolmol-1; Table 6) was discernibly lower. This agrees
with the empirical observation (e.g., Carpenter & Lohman, 1992) that Sr/Ca in abiotic
marine calcite is consistently lower than for biotic calcite.
2) The mean Mg/Ca for combined spot analyses of middle zone & calcite cortex
of R1162-0015 and -0016 were 103.5 and 106.4 mmolmol-1, respectively (Table 6).
These values are closely comparable to the 100 mmolmol-1 mean value for bulk skeletal
analysis of recent Primnoa by Sherwood et al (2005). The mean Mg/Ca (81.4 mmolmol1
; Table 6) is more than 20% lower for R1165-002; and more similar to the values
Aranha et al., Primnoa pacifica growth and paleoceanography
22
expected in abiotic calcite. This value also yields anomalously low calculated
temperatures relative to the observed range at the site of collection (Figure 9c).
Conversely, specimens R1162-0015 and -0016 yield calculated temperatures that closely
overlap those observed at their site of collection.
Sample 1165-002 did not yield discernibly older radiocarbon ages in its gorgonin
layers than the other two corals, nor was its macroscopic taphonomic condition noticeably
different. Despite the lack of any obvious “fossilization” or recrystallization textures
under the petrographic microscope, diagenesis seems the most likely explanation for the
observed trace element pattern in R1165-002. All three specimens were dead for at least
60 years before collection, with potential for the skeletal material of specimen R1165-002
to have experienced a period of shallow burial on the seafloor during that interval,
accelerating incipient diagenetic changes in the calcite composition through reaction with
shallow marine pore waters. It also implies a need for caution in the use of obviously
“sub-fossil” samples of Primnoa for paleoclimate proxies (e.g. Sinclair et al, 2005;
Heikoop et al, 2002). Use of SIMS microanalysis to assess the polarity of correlation
between Mg/Ca and Sr/Ca in this species appears to be a useful test to quickly assess if
individual samples have undergone partial or wholesale diagenetic alteration. If the
Mg/Ca and Sr/Ca ratios are positively correlated, then such samples should be avoided in
paleoceanographic studies.
Although the empirical expectation is that biotic marine calcite will also display a
positive correlation between Mg/Ca and Sr/Ca (e.g., Carpenter & Lohman, 1992), this is
largely based on compiled data on bulk skeletal analyses for shallow water marine
Aranha et al., Primnoa pacifica growth and paleoceanography
23
species. It is notable that the seemingly intact specimens of calcitic P. pacifica in this
study (R1162-0015 and -0016) show the opposite behaviour, mimicking the inverse
correlation between Mg/Ca and Sr/Ca observed in aragonitic zooxanthellate tropical reef
corals (e.g., Gaetani & Cohen, 2006).
4.4 Potential influence of primary productivity and growth rate on Mr/Ca and
Sr/Ca ratios.
Calculations performed by Gaetani & Cohen (2006) indicate that, at a constant
temperature, when ‘precipitation efficiency’ (i.e. the mass fraction of carbonate
precipitated from the calcifying fluid) increases then Mg/Ca values increase and Sr/Ca
and Ba/Ca values simultaneously decrease. In L. pertusa the oscillations in the Sr/Ca
ratios could be reproduced by two-fold variation of the assumed precipitation efficiency,
coupled with the observed temperature dependence of the partition coefficients
determined from the abiogenic aragonite (Cohen at al, 2006).
Since only about 50% of the variation observed in the Sr/Ca ratios in P. pacifica
can be attributed to temperature changes (Figure 9), the observed changes in Sr/Ca and
Mg/Ca ratios would call for substantial variations of precipitation efficiency through the
annual growth cycle.
In biogenic carbonate growth, a change in precipitation efficiency (i.e. mass of
carbonate precipitated/growth rate of biogenic carbonate) occurs due to changes in the
saturation state of the calcifying fluids. In tropical corals this change in saturation state is
linked to zooxanthellate photosynthesis which is, in turn, linked to changes in temperature
and sunlight (Cohen & McConnaughey, 2003; Cohen et al., 2006). Since any change in
Aranha et al., Primnoa pacifica growth and paleoceanography
24
precipitation efficiency would be primarily reflected as a change in the observed growth
rate of the coral, factors controlling growth rate are reflected in the trace element changes
observed in P. pacifica and similar deep sea corals (cf. Kuffner et al. 2012). Observations
of Sr/Ca ratios in the cold-water gorgonian Corallium rubrum indicate that Sr/Ca ratios
vary with skeletal density; i.e., they are indirectly coupled to growth rate (Weinbauer et
al., 2000). Cyclicity of Sr/Ca in deep sea bamboo corals can be used as an indicator of
growth rate, rather than being coupled directly to temperature (Roark et al., 2005).
Since no changes in light occur at depths of ~300m (from where P. Pacifica was
collected), and short-term variations in temperature in the area of collection are negligible
,, the primary factor driving changes in the growth rate is most likely a change in food
availability (Miller 1995; Ferrier-Pages, 2003; Houlbreque et al., 2003; Houlbreque et al.,
2005).
Several corals, including zooxanthellate species, can meet part of their energy
requirements by preying on zooplankton, phytoplankton, pico-nanplankton, dissolved
organic matter and particulate organic matter (Tsounis et al., 2010; Ribes et al., 2003;
Miller, 1995; Ferrier-Pages, 2003; Houlbrèque et al., 2003; Houlbrèque et al., 2004,
Orejas et al., 2011). Stable isotope analysis of two commonly occurring cold water corals,
Lophelia pertusa and Madrepora oculata, indicated that they might be omnivores and
may primarily feed on mesozooplankton (Duineveld et al., 2004; Kiriakoulakis et al.,
2005). Stable isotope (δ13C and δ15N) analysis indicated that P. resedaeformis likely feeds
on phytodetritus supplemented by mesozooplankton (Sherwood et al., 2008). A previous
study on P. pacifica suggested that it likely feeds on the same trophic level as P.
resedaeformis (Sherwood et al., 2005b).
Aranha et al., Primnoa pacifica growth and paleoceanography
25
In controlled laboratory experiments on Stylophora pistillata (a zooxanthellate
scleractinian coral) it was noted that an increase in plankton feeding under constant water
temperature increased the rate of both skeletal and tissue growth of the coral. This
occurred under both light and dark conditions, indicating that feeding has a direct effect
on the mass fraction of skeletal material precipitated in the absence of light or
temperature changes. (Miller,1995; Ferrier-Pages, 2003; Houlbrèque et al., 2003;
Houlbrèque et al., 2005). It was also noted that in Stylophora pistillata the amount of food
ingested was proportional to food density and that the coral never reached a saturation of
feeding capacity in the experiments (Ferrier-Pages, 2003). Growth rates almost equivalent
to tropical corals were noted in Lophelia pertusa and Madrepora oculata specimens
stored in dark conditions in aquaria and fed exclusively with zooplankton - with
temperature variation during the experiments controlled to ~±0.5°C (Orejas et al., 2008,
2011).
In aragonitic scleractinian reef corals, Sr/Ca ratio is inversely correlated with
calcification rate, and with temperature, thus short-term variation in calcification rate
causes high-amplitude fluctuations in Sr/Ca that mimic wide SST variations (Kuffner et
al. 2012). Thus, accurate short-term fluctuations in Sr/Ca-derived paleotemperatures
from tropical reef scleractinians should incorporate growth rate into the Sr/Ca-SST
calibration (Gaetani, et al. 2011).
For Primnoa calcite, in the absence of light, zooxanthellae, or substantial
temperature variations, short-term changes in the feeding of the coral should be the major
factor modulating the skeletal precipitation efficiency and, consequently, the trace
element values. If the mass fraction of carbonate precipitated increases at a fixed
Aranha et al., Primnoa pacifica growth and paleoceanography
26
temperature then we would expect to observe a decrease in the Sr/Ca ratios and an
increase in the Mg/Ca ratios of the carbonate (Gaetani & Cohen, 2006). By analogy with
the tropical scleractinians, our results suggest that measured Mg/Ca and Sr/Ca ratios in
cold-water gorgonian calcites may indicate changes in food supply, hence
paleoproductivity, if seawater temperature variation is known (cf. Hill et al. 2012).
Similarly, Ba/Ca in cold-water gorgonian coral skeletons may serve as a measure of
paleoproductivity (Hill et al. 2011), although in our data, Ba/Ca ratios did not yield a
readily interpreted signal.
4.4.1 Oceanography of the Olympic Coast National Marine Sanctuary:
The waters of OCNMS, are subject to changes in physical, chemical and
biological properties due to the California Current system (CCS) (Hickey et al., 2006).
The CCS mainly includes the southward California Current, the wintertime northward
Davidson Current, and the northward California Undercurrent (Hickey & Banas, 2003).
The California Undercurrent (CUC) is of special interest with respect to our samples
because it is very active in the area of collection. It is continuous at depths of about 100400 m and likely carries larval fish, invertebrates and even phytoplankton seed stock
(Hickey & Banas, 2003). The intensity of the CUC is known to attain its maximum values
in late spring and early autumn (Collins et al., 2003), and is the source of much of the
nutrient-rich water supplied to the shelf during coastal upwelling (Hickey & Banas,
2003).
Aranha et al., Primnoa pacifica growth and paleoceanography
27
The seasonal upwelling (Huyer, 1983) in this area favours a large spring plankton
bloom, followed by a smaller autumn plankton pulse (Anderson, 1964; Landry et al.,
1989; Thomas & Strub, 2001). Landry et al. (1989) have reported an increased
concentration in chlorophyll twice a year offshore of Washington State (between 50 to 90
km); one of these episodes occurs between February and April and the other in October.
Thomas & Strub (2001) observed that, in the Pacific Northwest, chlorophyll
concentrations greater than 2.0 mg m-3 extend further offshore in late spring-summer
(May- June) and that a second offshore extension occurs in late summer (September).
4.4.2 Expected and observed trace element variations in P. pacifca based on
the oceanography of the region:
Although the average paleotemperature estimate for one of the corals analyzed
matched observed temperatures (Figure 9a), observed temperature variation cannot
account for the measured variation in Mg/Ca and Sr/Ca ratios in the Primnoa skeletons
analyzed (figure 9 and section 4.3.1). Given that P. pacifica likely feeds on the downward
flux of particulate organic matter, plankton and similar sources; the measured Sr/Ca and
Mg/Ca ratios could respond to changes in the skeletal growth rate brought about by
changes in food availability (Roark et al., 2005, Kuffner et al., 2012, and section 4.3.1,
above). In reviews of the primary production, new production and vertical flux of organic
carbon in the eastern Pacific it has been argued that production and vertical flux were
directly related (Pace et al., 1987; Loubere & Fariduddin, 1999).
Aranha et al., Primnoa pacifica growth and paleoceanography
28
The biannual increase in food availability (due to the two plankton blooms per
year) should theoretically be observed as two cycles per year in Mg/Ca and Sr/Ca
profiles. While an inverse correlation is apparent in Sr/Ca and Mg/Ca profiles in Figure 7,
a biannual cyclicity is not obviously resolved.
There are suggestions in our data that P. pacifica may also record more abrupt
events. A particularly drastic decrease in Sr/Ca values is noted along the SIMS profile in
R1162-0016 (between year 6 and 7) and R1162-0015 (between year 7 and 8). This
decrease in Sr/Ca is accompanied by a simultaneous increase in the Mg/Ca ratios. This
excursion is distinct from spikes caused by gorgonin-rich calcite samples because of the
inverse relationship between Mg/Ca and Sr/Ca, as opposed to parallel Mg/Ca and Sr/Ca
changes in gorgonin-rich spots. This inverse Mg/Ca-Sr/Ca event could be attributed to a
single period of increased growth due to substantial increase in the availability of food.
This single period of increased growth occurs ~7 years before death in sample R11620015 and ~8 years before death in sample R1162-0016. The corals were collected during
the same ROPOS dive from adjacent areas. Thus the trace element profiles may provide a
unique method of correlating growth patterns in corals from proximal colonies. While it is
possible that both P. pacifica samples have recorded the same event, the age uncertainty
of the radiocarbon ages from the two corals is high enough that it is impossible to
demonstrate that the two Mg/Ca records precipitated at the same time.
A substantial, unusual increase in phytoplankton biomass was recorded in the
waters off Washington, Oregon and British Columbia in the spring of 2002 (Wheeler et
al., 2003; Thomas et al., 2003) due to the invasion of cool, saline subarctic waters
(Freeland et al., 2003; Bograd & Lynn, 2003). Similar events could have occurred during
Aranha et al., Primnoa pacifica growth and paleoceanography
29
the lifetime of R1162-0016 and -0015, leading to the spikes in the Mg/Ca and decreases
in the Sr/Ca. Thus, elemental ratios in the calcite skeletons of Primnoa spp. may be useful
in recording short term changes in productivity in the ocean, which reflect basin-scale
changes in circulation, similar to the records of oceanographic change preserved in the
gorgonin layers (Sherwood et al., 2011). This attribute would be most useful in samples
harvested live, where exact year of death is easily established.
The decreased Mg/Ca ratios, and apparently cooler water temperatures recorded in
sample R1162-0016 indicate variation on the same temporal scale as the Pacific Decadal
Oscillation (PDO), although with only one shift, a correlation with PDO is impossible to
demonstrate. The seasonal upwelling in this region is also influenced greatly by ENSO
events, and a reduction in the nutrients and chlorophyll standing stock is known to occur
in association with ENSO events (Carr, 2002; Corwith & Wheeler, 2002). A strong
ENSO event should be recorded as a dramatic dip in the Mg/Ca ratios with a
simultaneous spike in the Sr/Ca ratios in response to decreased productivity. Thus if a
coral could survive through a strong ENSO event it might also record changes occurring
in surface productivity due to the changes in upwelling.
5 Conclusions:
The annual radial growth rate of Primnoa pacifica calculated in this study was
0.23 to 0.58 mm*yr-1. The lowest reported growth rate closely coincides with the
previously reported growth rate for P. pacifica from the Dixon entrance (Andrews el al,
2002). This lends further support to studies indicating that recovery time from damage
Aranha et al., Primnoa pacifica growth and paleoceanography
30
due to trawling and similar disturbances are very long for this species (Andrews et al.,
2002) and other deep-sea gorgonians in Canadian waters (Sherwood and Edinger 2009).
Primnoa pacifica and P. resedaeformis showed dramatic regional differences in
radial growth rate, with growth rates in P. pacifica more than 4 times greater than in its
northwest Atlantic sister species. Primary productivity is likely the variable best able to
explain these regional differences in growth rate.
Growth rates in the calcite cortex and gorgonin/calcite mixed zone are virtually
identical, thus indicating that the growth rate of the coral remains constant in spite of a
change in the skeletal growth mode.
The previously established paleotemperature equation of Mg/Ca ratios in Primnoa
resedaeformis, applied to P. pacfica, yielded average bottom water temperatures
matching observed temperatures, but the range of variation in Mg/Ca ratios and
calcualted paleotemperatures exceeded the range of variation in observed bottom
temperatures.
The Mg/Ca and Sr/Ca ratios in Primnoa pacifica calcite are likely controlled by
surface water productivity changes rather than bottom water temperature alone. The
changes in Mg/Ca and Sr/Ca thus have potential to record major changes in productivity,
which in turn can provide evidence of other large scale annual and decadal changes in
hydrographic conditions.
The polarity of the correlation between Mg/Ca and Sr/Ca ratios indicated
diagenetic change in gorgonian coral skeletons that was otherwise not readily apparent.
Original biogenic calcites retained a negative correlation, while diagenetically altered
gorgonian calcite exhibited a positive Mg/Ca – Sr/Ca correlation.
Aranha et al., Primnoa pacifica growth and paleoceanography
31
6. Acknowledgements.
We thank the crew of the ROV ROPOS and CCGS John P. Tully for making field
work possible. Canadian Hydrographic Service, Geological Survey of Canada, and
Olympic Coast National Marine Sanctuary provided access to bathymetric datasets. O.
Sherwood provided invaluable guidance in sample processing and analysis. V. Lecours
and B. Neves helped with cartography. Joel Finnis assisted with analysis of archival
oceanographc data. M. Wisshak and D. Scott provided helpful comments on the thesis
from which this paper is derived, and O. Sherwood, C. Dullo, and an anonymous
reviewer provided helpful comments on the manuscript. This research was sponsored by
the NSERC-funded Canadian Healthy Oceans Network - a university-government
partnership dedicated to biodiversity science for the sustainability of Canada's three
oceans. Additional funding was provided by NSERC Discovery grants to EE and GL.
Aranha et al., Primnoa pacifica growth and paleoceanography
32
7 References cited:
Amiel, A. J., Friedman, G. M., and Miller, D. S. (1973) Distribution and nature of
incorporation of trace elements in modern aragonitic corals. Sedimentology 20, 1: 47-64.
Anderson, G. C. (1964) The seasonal and geographic distribution of primary productivity
off the Washington and Oregon coasts. Limnol Oceanogr, 9, 284-302.
Andrews, A.H., Cordes, E., Heifetz, J., Cailliet,G.M., Coale, K.H., Somerton, D., Munk,
K. and Mahoney, B. M.(2002) Age and growth of a deep sea, habitat-forming
octocorallian (Primnoa sp.) from the Gulf of Alaska, with radiometric age validation.
Hydrobiologia 471: 101-111
Azmy, K., Edinger, E., Lundbergm J., and Diegor, W. (2010) Sea level and
paleotemperature records from a mid-Holocene reef on the north coast of Java, Indonesia.
Int. J. Earth Sci. 99, 231-244.
Barrie, J.V., and Conway, K.W. (1999) Late Quaternary glaciation and post-glacial
stratigraphy of the Northern Pacific margin of Canada. Quater. Res. 51, 113-123.
Boyer, T.P., J. I. Antonov, O. K. Baranova, H. E. Garcia, D. R. Johnson, R. A. Locarnini,
A. V. Mishonov, D. Seidov, I. V. Smolyar, and M. M. Zweng, 2009: World Ocean
Aranha et al., Primnoa pacifica growth and paleoceanography
33
Database 2009, Chapter 1: Introduction, NOAA Atlas NESDIS 66, Ed. S. Levitus, U.S.
Gov. Printing Office, Wash., D.C. , 216 pp., DVD
Boyle, E. A., (1981) Cadmium, zinc, copper, and barium in foraminifera tests,” Earth.
Planet. Sci. Lett. 53, 1: 11-35.
Bograd, S. J., and R. J. Lynn. (2003). Anomalous Subarctic influence in the southern
California Current during 2002. Geophys. Res. Lett. 30 (15):8020.
Cairns S.D. and Bayer F.M. (2009). A generic revision and phylogenetic analysis of the
Primnoidae (Cnidaria: Octocorallia). Smithson Contrib Zool 629:1–79.
Carpenter, J. and Lohman, K.C. (1992). Sr/Mg ratios of modern marine calcite: Empirical
indicators of ocean chemistry and precipitation rate. Geochim. Cosmochim. Acta
56: 1837-1849
Carr, M.-E. (2002), Estimation of potential productivity in Eastern Boundary Currents
using remote sensing, Deep Sea Res., Part II, 49, 59– 80.
Cohen, A.L., Layne, G.D., Hart, S.R., and Lobel, P.S. (2001) Kinetic control of skeletal
Sr/Ca in a symbiotic coral; implications for the paleotemperature proxy.
Paleoceanography 16, 20-26.
Aranha et al., Primnoa pacifica growth and paleoceanography
34
Cohen, A., McConnaughey, T. (2003) Geochemical perspectives on coral mineralization.
Rev Mineral Geochem 54:151-187
Cohen, A.L., Gaetani, G.A., Lundalv, T., Corliss, B.H., George, R.Y.,( 2006).
Compositional variability in a cold-water scleractinian, Lophelia pertusa: new insights
into “vital effects”. Geochem. Geophys. Geosyst. 7, Q12004
Collins, C. A., Ivanov, L.M. and Melnichenko, O.V. (2003), Seasonal Variability of the
California Undercurrent: Statistical Analysis based on the Trajectories of Floats with
Neutral Buoyancy, Phys. Oceanogr., 13 (3), 135–147
Corwith, H., and Wheeler, P.A. (2002), El Niño related variations in nutrient and
chlorophyll distributions off Oregon, Progr. Oceanogr., 54, 361–380.
Crawford, H., and Thompson, R.E. (1991) Physical oceanography of the western
Canadian continental shelf. Continent. Shelf Res. 11, 669-683.
Duineveld, G.C.A., Lavaleye, M.S.S., Berghuis E.M. (2004) Particle flux and food supply
to a seamount cold-water coral community (Galicia Bank, NW Spain). Mar Ecol Prog
Ser 277:13–23
Aranha et al., Primnoa pacifica growth and paleoceanography
35
DuPreez, C.,Tunnicliffe, V., 2011. Shortspine thornyhead and rockfish (Scorpaenidaea)
distirubtion in response to substratum, biogenic structures and trawling. Mar. Ecol. Progr.
Ser. 425, 217-231.
Edinger. E., Boutillier. J., Workman, G. Coral Distributions around Learmonth Bank,
Northern British Columbia, Canada: Influence of Surficial Geology and Tidal Currents
Deep Sea Coral Symposium. 4th International Symposium on Deep Sea Corals, 2008
Wellington, New Zealand p.98 Abstract nr 6.04
Edinger, E.N., Sherwood, O.A. (2012). Applied taphonomy of gorgonian and
antipatharian corals in Atlantic Canada: experimental decay rates, field observations, and
implications for assessing fisheries damage to deep-se coral habitats. N. Jb. Geol.
Palaont. Abh. 265, 199-218.
Ferrier-Pagès C, Witting J, Tambutté E, Sebens KP (2003) Effects of natural zooplankton
feeding on the tissue and skeletal growth of the scleractinian coral Stylophora pistillata.
Coral Reefs 22:229–240
Freeland, H. J., G. Gatien, A. Huyer, and R. L. Smith (2003), Cold halocline in the
northern California Current: An invasion of subarctic water, Geophys. Res. Lett., 30(3),
1141.
Aranha et al., Primnoa pacifica growth and paleoceanography
36
Gaetani, G. A., and A. L. Cohen (2006), Element partitioning during precipitation of
aragonite from seawater: A framework for understanding paleoproxies, Geochim.
Cosmochim. Acta, 70, 4617–463
Gaetani, G.A., Cohen, A.L., Wang, Z., and Crusius, J. (2011) Rayleigh-based, multielement coral thermometry: a biomineralization approach to developing climate proxies.
Geochim. Cosmochim. Acta 75, 1920-1933
Heikoop, J.M., Hickmott, D.D., Risk MJ, Shearer CK, Atudorei V (2002) Potential
climate signals from the deep-sea gorgonian coral Primnoa resedaeformis. Hydrobiologia
471: 117-124
Hickey, B.M., Banas, N.S., (2003). Oceanography of the Pacific Northwest coastal ocean
and estuaries with application to coastal ecosystems. Estuaries 26 (48), 1010–1031.
Hickey, B., A. MacFadyen,W. Cochlan, R. Kudela, K. Bruland, and C. Trick (2006),
Evolution of chemical, biological, and physical water properties in the northern California
Current in 2005: Remote or local wind forcing?, Geophys. Res. Lett., 33, L22S02.
Hill, T.M., Spero, H.J., Guilderson, T., LaVigne, M., Clague, D., Macalello, S., and Jang,
N. (2011). Temperature and vital effect controls on bamboo coral (Isididae) isotope
geochemistry: a test of the "lines method". Geochemistry, Geophysics, Geosystems
Q04008, doi:10.1029/2010GC003443.
Aranha et al., Primnoa pacifica growth and paleoceanography
37
Hill, T.M., LaVigne, M., Spero, H.J., Guilderson, T., Gaylord, B., and Clague, D., (2012).
Variations in seawater Sr/Ca recorded in deep-sea bamboo corals. Paleoceanography 27,
PA3202, doi:10.1029/2011PA002260.
Houlbrèque, F., Tambutté, E. and Ferrier-Pagès, C. (2003). Effect of zooplankton
availability on the rates of photosynthesis, tissue and skeletal growth of the scleractinian
coral Stylophora pistillata J. Exp. Mar. Biol. Ecol. 296, 145-166.
Houlbrèque, F., Tambutté E, Allemand D, Ferrier-Pagès C (2005) Interactions between
zooplankton feeding, photosynthesis and skeletal growth in the scleractinian coral
Stylophora pistillata. J Exp Biol 207:1461–1469
Huyer, A. (1983) Coastal Upwelling in the California Current System. Prog. Oceanogr.
12:3 259-284
Jones, E. P. & Anderson, L. G. (1994). Northern Hudson Bay and Foxe Basin water
masses, circulation and productivity. Atmos.Ocean 32: 361-374
Khripounoff, A., Vangriesheim, A. and Crassous, P. (1998) Vertical and temporal
variations of particle fluxes in the deep tropical Atlantic. Deep-Sea Res. I, 45, 193–216.
Aranha et al., Primnoa pacifica growth and paleoceanography
38
Kiriakoulakis, K., Fisher, E., WolV, G.A., Freiwald, A., Grehan, A. and Roberts, J.M
(2005) Lipids and nitrogen isotopes of two deep-water corals from the North-East
Atlantic: initial results and implications for their nutrition. In: Freiwald A, Roberts JM
(eds) Cold-water corals and ecosystems. Springer, Berlin, pp 715–729
Kuffner, I.B.,, Jokiel, P.L., Rodgers, K.S., Andersson, A.J., and MacKenzie, F.T. (2012)
An apparent "vital effect" of calcification rate on the Sr/Ca temperature proxy in the reef
coral Montipora capitata. Geochemistry, Geophysics, Geosystems 13, doi:
10.1029/2012GC004128
Layne, G.D. and Cohen, A.L.,( 2002), Advantages of Secondary Ion Mass Spectrometry
for trace element studies of marine biomineralization, Geochim. Cosmochim. Acta, 66,
A436 (abstr.)
Lea D.W., Shen G.T., Boyle E.A., (1989) “Coralline barium records temporal variability
in equatorial Pacific upwelling,” Nature 340, 6232: 373-376.
Lea, D.W. and Boyle, E.A. (1990), Foraminiferal reconstruction of barium distributions
in water masses of the glacial oceans, Paleoceanography 5: 719–742.
Loubere,P., Fariduddin, M.,(1999). Quantitative estimation of global patterns of surface
ocean biological productivity and its seasonal variation on timescales from centuries to
millennia. Global Biogeochem. Cycles 13,115-133.
Aranha et al., Primnoa pacifica growth and paleoceanography
39
Landry, M.R., Postel, J.R., Peterson, W.K., Newman, J., (1989). Broad-scale distribution
patterns of hydrographic variables on the Washington Oregon shelf. In: Landry, M.R.,
Hickey, B.M. (Eds.), Coastal Oceanography of Washington and Oregon. Elsevier,
Amsterdam (Chapter 1).
McNeely, R., Dyke, A. S., and Southon, J. R. (2006) Canadian marine reservoir ages,
preliminary data assessment, Open File 5049, pp. 3. Geological Survey Canada.
Miller, M. W. (1995). Growth of a temperate coral: effects of temperature, light, depth,
and heterotrophy. Mar. Ecol. Prog. Ser. 122:217-225.
Mitsuguchi, T., Matsumoto, E., Abe, O., Uchida, T., Isdale, P.J., (1996) Mg/Ca
thermometry in coral skeletons. Science 274, 961-963
Neves, B.M., Du Preez, C., Edinger, E., submitted. Mapping coral and sponge habitats on
a shelf-depth environment using multibeam sonar and ROV video observations:
Learmonth Bank, Northern British Columbia, Canada. Deep-Sea Research II (this issue)
Neves, B. de M., Edinger, E.N. (2012) Geographic and environmental variation in
gorgonian coral skeletal growth rates. Geological Association of Canada annual meeting,
St. Johns, Canada, Abstracts with program, p. 98.
Aranha et al., Primnoa pacifica growth and paleoceanography
40
Orejas, C., Gori, A., and Gili, J. M.(2008) Growth rates of live Lophelia pertusa and
Madrepora oculata from the Mediterranean Sea maintained in aquaria, Coral Reefs, 27,
p. 255.
Orejas, C.,Ferrier-Pages, C., Reynaud, S., Tsounis, G., Allemand, D., Gili, J.M. (2011).
Experimental comparison of skeletal growth rates in the cold-water coral Madrepora
oculata Linnaeus, 1758, and three tropical scleractinian corals. J. Exp. Mar. Biol. Ecol.,
405, 1-5.
Pace, M. L., Knauer, G. A., Karl, D. M., and Martin, J. H. (1987) Primary production,
new production, and vertical flux in the eastern Pacific Ocean. Nature, 325, 803-804.
Reimer, P.J., Baillie, M.G.L., Bard, E., Bayliss, A., Beck, J.W., Blackwell, P.G., Bronk
Ramsey , C., Buck, C.E., Burr, G.S., Edwards, R.L., Friedrich, M., Grootes, P.M.,
Guilderson, T.P., Hajdas, I., Heaton, T.J., Hogg, A.G., Hughen, K.A., Kaiser,K.F.,
Kromer, B., McCormac, F.G., Manning, S.W., Reimer, R.W., Richards, D.A., Southon,
J.R.,Talamo, S., Turney, C.S.M., van der Plicht, J. and Weyhenmeyer,
C.E. (2009) INTCAL 09 and MARINE09 Raadiocarbon age calibration curves, 0-50,000
years Cal BP .Radiocarbon, 51 (4). 1111-115
Aranha et al., Primnoa pacifica growth and paleoceanography
41
Ribes, M., Coma,R.,and Gili,J.M. (1999)Heterogenus feeding n benthic suspension
feeders : The natural diet and feeding rate of the temperate gorgonian Paramuricea
clavata (Cnidaria:Octocorallia) over a year cycle . Mar Ecol Prog Ser,183,125-137.
Ribes, M., Coma,R., and Rossi,S. (2003) Natural feeding of the temperate asymbiotic
octocoral gorgonian Leptogorgia sarmentosa (Cnidaria:Octocorallia). Mar Ecol Prog Ser
254,141-15
Risk. M.J., Heikoop, J.M., Snow, M.G., and Beukens, R. (2002) Lifespans and growth
patterns of two deep-sea corals: Primnoa resedaeformis and Desmophyllum cristagalli.
Hydrobiologia 471, 125-131.
Roark, E.B., Guilderson, T.P., Flood-Page, S.R., Dunbar, R.B., Ingram, B.L., Fallon, S.J.
and McCulloch, M.T. (2005) Radiocarbon-based ages and growth rates for bamboo
corals from the Gulf of Alaska. Geophys Res Lett 32:L04606
Sherwood, O.A., Heikoop, J.M., Sinclair, D.J., Scott, D.B., Risk, M.J., Shearer, C. and
Azetsu-Scott, K. (2005a) Skeletal Mg/Ca in Primnoa resedaeformis: relationship to
temperature. In: Freiwald A, Murray JM (eds) Cold-water corals and ecosystems.
Springer, Berlin, p 1061–1079
Aranha et al., Primnoa pacifica growth and paleoceanography
42
Sherwood, O.A., Heikoop, J.M., Scott, D.B., Risk, M.J., Guilderson, T.P. and McKinney,
R.A. (2005b) Stable istopic composition of deep sea gorgonian corals Primnoa spp.: a
new archive of surface processes. Mar Ecol Prog Ser 301:135–148
Sherwood, O.A., Scott, D.B., Risk, M.J., and Guilderson, T.P.. (2005c) Radiocarbon
evidence for annual growth rings in the deep-sea octocoral Primnoa resedaeformis. Mar
Ecol Prog Ser 301:129–134
Sherwood, O.A., Scott, D.B. and Risk, M.J. (2006) Late Holocene radiocarbon and
aspartic acid racemization dating of deep-sea octocorals. Geochim Cosmochim Acta
70:2806–2814
Sherwood O.A., Jamieson, R.E., Edinger, E.N. and Wareham, V.E. (2008a) Stable C and
N isotopic composition of cold-water corals from the Newfoundland and Labrador
continental slope: examination of trophic, depth and spatial effects. Deep-Sea Res I
55:1392–1402
Sherwood, O.A., Edinger, E.N., Guilderson, T.P., Ghaleb, B., Risk, M.J., Scott, D.B., (2008b)
Late Holocene radiocarbon variability in Northwest Atlantic slope waters. Earth Planet. Sci. Lett.
275: 146-153
Aranha et al., Primnoa pacifica growth and paleoceanography
43
Sherwood, O.A. and Edinger E. (2009) Ages and growth rates of some deep-sea
gorgonian and anthipatharian corals of Newfoundland and Labrador. Can J Fish Aquat
Sci 66: 142–152
Sherwood, O.A., Lehmann, M.F., Schubert, C.J., Scott, D.B., McCarthy, M.D., 2011.
Nutrient regime shift ni the western North Atlantic indicated by compound-specific d15N
of deep-sea gorgonians. Proc. Natl. Acad. Sci. USA 108, 1011-1015
Sinclair, D.J., Sherwood, O.A., Risk, M.J., Hillaire-Marcel, C., Tubrett, M., Sylvester, P.,
McCulloch, M., Kinley, L. (2005). Testing the reproducitility of Mg/Ca profiles in the
deep-water coral Primnoa resedaeformis: putting the proxy through its paces. In: Freiwald
A, Murray JM (eds) Cold-water corals and ecosystems. Springer, Berlin, p 1039–1060.
Sinclair, D.J., Williams, B., Allard, G., Ghaleb, B., Fallon, S., Ross, S.W., and Risk, M.,
(2011) Reproducibility of trace element profiles in a specimen of the deep-water bamboo
coral Keratoisis sp.. Geochim. Cosmochim. Acta 75, 5101-5121.
Smith, S.V., Buddemeier, R.W., Redalje, R.C., Houck, J.E., (1979). Strontium-calcium
thermometry in coral skeletons. Science 204 (4391), 404–407
Stuiver, M., Polach, H.A., (1977). Discussion: reporting 14 C data. Radiocarbon 19, 355–
363
Aranha et al., Primnoa pacifica growth and paleoceanography
44
Tsounis, G., Orejas, C., Reynaud, S., Gili, J.M., Allemand, D., Ferrier-Pagès, C. (2010)
Prey-capture rates in four Mediterranean cold water corals. Mar Ecol Prog Ser 398:149155
Thomas, A. C., and P. T. Strub, (2001) Cross-shelf phytoplankton pigment variability in
the California Current, Cont. Shelf Res., 21, 1157–1190
Thomas, A. C., Strub, P. T. and Brickley, P. (2003a), Anomalous satellite measured
chlorophyll concentrations in the northern California Current in 2001 – 2002, Geophys.
Res. Lett., 30(15), 8022
Thomas, A.C., Townsend, D.W., Weatherbee, R., (2003b). Satellite measured
phytoplankton variability in the Gulf of Maine. Cont. Shelf. Res . 23, 971–989
Thresher, R., Rintoul, S.R., Koslow, J.A., Weidman, C., Adkins, J., and Proctor, C.,
(2004). Oceanic evidence of climate change in southern Australia over the lsst three
centuries. Paleoceangraphy 31, L07212, doi:10.1029/2003GL018869.
Thresher, R.E., Wilson, N.C., MacRae, C.M., Neil, H., (2010) Temperature effects on the
calcite skeletal composition of deep-water gorgonians (Isididae). Geochim. Cosmochim.
Acta 74, 4655-4670.
Aranha et al., Primnoa pacifica growth and paleoceanography
45
Weber, J. N. & Woodhead, P. M. J. (1972) Stable isotope ratio variations in
nonscleractinian coelenterate carbonates as a function of temperature. Mar. Biol., 15, 293297
Weinbauer, M. G., Brandstatter, F., and Velimirov, B. (2000), On the potential use of
magnesium and strontium concentrations as ecological indicators in the calcite skeleton
of the red coral (Corallium rubrum), Mar. Biol., 137, 801–809.
Wheeler, P. A., Huyer, A. and Fleischbein J. (2003), Cold halocline, increased nutrients,
and higher chlorophyll off Oregon in 2002, Geophys. Res. Lett., 30(15), 8021
Aranha et al., Primnoa pacifica growth and paleoceanography
46
Figure Captions.
Figure 1: Location map. A. Learmonth Bank, Dixon Entrance, northern British Columbia,
Canada. B. Olympic Coast National Marine Sanctuary, Washington state USA. Dots
indicate locations of coral collections from both study areas. Inset map shows regional
geography.
Figure 2: A. Live Primnoa pacifica as observed in Dixon Entrance, ~350 m water depth,
July 2008. Note standing dead branches, also rockfish resting among branches of coral.
B. Dead Primnoa pacifica skeleton as observed on the sea floor, Dixon Entrance, ~300 m
water depth, July 2008. This sample broke during collection. C-H: The three colonies of
Primnoa pacifica chosen for radiocarbon dating and SIMS analyses and their
corresponding basal cross-sections (photographed under UV light). C-D: Sample R11620015 (top), E-F: sample R1162-0016 (middle) and G-H: sample R1165-0002 (bottom).
Red and yellow markers in cross-section photos (D,F, H) indicate the position of the
gorgonin rings which were isolated for 14C dating.
Figure 3: A. Original grayscale photoscanned image of thin section of specimen R11620015 showing alternating calcite and gorgonin layers in the mixed growth zone. White
scale bar = 1 cm. B. The same image with digital level and gradient filters applied to
emphasize banding in the outer calcite cortex.
Figure 4. Growth rate (mm.yr-1) vs Age of the coral for P. pacifica. The error bars are 1σ.
Dixon entrance samples are represented by grey markers and OCNMS samples are
Aranha et al., Primnoa pacifica growth and paleoceanography
47
represented by black markers. The dotted line represents the average growth rate of all
samples. Average growth rate estimates for P. pacifica in the Gulf of Alaska (Andrews et
al., 2002) and P. resedaeformis from two sites in the northwest Atlantic plotted for
comparison.
Figure 5. Radiocarbon ages of P. pacifica gorgonin subsamples analyzed, reservoircorrected 14C years 1 error.
Figure 6. Radiocarbon validation of growth rates and ages based on ring counts. (A)
Sample R1162-0015 (B) Sample R1162-0016. (C) Sample R1165-002 Distance (From
the center of the coral. Center is at 0 mm) vs reservoir corrected radiocarbon years. The
radiocarbon age of the outermost ring was considered valid in plotting the age based on
band counting. The error bars (1σ) for the age based on band counts are smaller than the
size of the symbol in the graph.
Figure 7: Mg/Ca and Sr/Ca ratios vs. time (years) in the calcite cortex of P. pacifica.
Time was calculated by extrapolating average annual radial growth rate over the calcite
cortex. Error bars are ±1σ. The profiles start from the time of death of the organism (i.e.
the outer edge), hence younger ages are to the left, and older to the right. The data
presented has been smoothed using a second degree Savitzky-Golay filter. A. Sample
R1162-0015. B. Sample R1162-0016. C. Sample R1165-0002. In B, data are missing in
the areas where visible gorgonin rings cut across the calcite cortex.
Aranha et al., Primnoa pacifica growth and paleoceanography
48
Figure 8. Observed bottom temperatures in the Olympic Coast National Marine Sanctuary
(OCNMS) region. All data derived from the World Ocean Database 2009, within the
bounding coordinates 48-48.5 N and 124.75-125.5 W. Mean temperatures  95%
confidence limits, along with minimum and maximum observed temperatures and the
duration of observations, in the depth intervals from which corals were collected: 260-280
m, 280-300 m, and 300-320 m.
Figure 9. Calculated paleotemperatures from P. pacifica in OCNMS region, using the
published equation of Sherwood et al. 2005, Mg/Ca (mmol.mol-1) = 5(±1.4) T (ºC) +
64(±10). A: R1162-0015. B: R1162-0016. C: R1165-0002. In A and B, shaded band
indicates maximum temperature range observed in World Ocean Database data for
OCNMS region at 300-320 m depth, 1938-1983. In C, shaded band indicates maximum
observed temperature range at 280-300 m depth, 1953-2006.
Figure 10: Comparison of radial growth rates of Primnoa resedaeformis from the Hudson
strait ([1]: Sherwood & Edinger, 2009) and the Northeast Channel ([2]: Mortensen &
Buhl-Mortensen, 2005) with those of P. pacifica from Dixon Entrance (this study, and
[3]: Andrews et al, 2002), and P. pacifica from Olympic Coast National Marine
Sanctuary (OCNMS; this study). All logarthimic best-fit curves were passed through the
youngest and largest coral data points in the Mortensen & Buhl-Mortensen (2005) data
set. Andrews et al (2002) provided radial growth data only for one colony of P. pacifica
(Gulf of Alaska), thus only one data point for [3] exists in the graph. The fitted line
labelled ‘Model Maximum’, is the logarithmic fit for the four coral specimens from this
study with the largest radii.