Download Pteropod time-series from the NE Pacific

ICES Journal of
Marine Science
ICES Journal of Marine Science (2012), 69(3), 448 –459. doi:10.1093/icesjms/fsr163
Pteropod time-series from the NE Pacific
David L. Mackas* and Moira D. Galbraith
Fisheries and Oceans Canada, Institute of Ocean Sciences, PO Box 6000, Sidney, BC, Canada V8L 4B2
*Corresponding Author: tel: +1 250 3636442; fax: +1 250 3636690; e-mail: [email protected]
Mackas, D. L., and Galbraith, M. D. 2012. Pteropod time-series from the NE Pacific. – ICES Journal of Marine Science, 69: 448 –459.
Received 1 April 2011; accepted 1 September 2011; advance access publication 11 October 2011.
Pteropods are marine planktonic molluscs that play important roles as broad-spectrum microplankton grazers, and as prey for fish,
squid, and other plankton. Most species (e.g. Limacina, Clio) form aragonite shells. Others (e.g. Clione) lack shells as adults but are
narrow-spectrum predators that rely on shelled pteropods as their primary or exclusive prey. The entire group is therefore potentially
threatened by increasing ocean acidification, which in some regions (including the NE Pacific) is now approaching the solubility
threshold for aragonite. Despite the grounds for ecological concern, there are few long-term time-series of pteropod populations.
Time-series of pteropod biomass anomalies off the Vancouver Island continental margin and in the eastern Alaska Gyre (Line P)
are analysed. Off both southern and northern Vancouver Island, Limacina (the dominant Subarctic thecate pteropod) has declined
notably. Continental margin trends for Clione (the dominant athecate) are mostly positive but not significant. Occurrence rate
and quantity of Clio (a subtropical species) have increased greatly. The shorter (13 – 14 year) Line P time-series as yet shows no
overall trends for any of the species, although there are positive annual anomalies of Clio in the same years in both continental
margin and oceanic regions.
Keywords: Northeast Pacific, ocean acidification, pteropod, zooplankton.
Introduction
Ocean acidification is an integral and important component of
anthropogenic global change (Feely et al., 2004; Doney, 2006;
IPCC, 2007). Atmospheric CO2 levels have increased substantially
during the past two centuries as a result of human activities such as
fossil fuel burning, the manufacturing of concrete, and land clearing for agriculture and settlement. The atmospheric increases
would have been larger, except that a large part of total anthropogenic CO2 emissions have subsequently entered the ocean, where
they are having effects on pH, and on the equilibrium balance
for carbonate and various metal ions.
Progressive ocean acidification and resulting changes in carbonate solubility could have important present and future consequences for organisms with carbonate skeletons. Many types of
calcifier live in the ocean and could be affected (see Table 1 in
Fabry et al., 2008). In the plankton, potentially sensitive organisms
include calcite-forming phytoplankton (coccolithophorids), protozoans (foraminifera), and a range of meroplanktonic larvae.
However, planktonic molluscs (pteropods, heteropods) are likely
to be especially sensitive because the mineral they use to form
their carbonate shells is aragonite rather than calcite. Aragonite
is considerably more soluble in seawater than calcite at most
ocean temperatures, pressures, and levels of pCO2 (Feely et al.,
2004). Aragonite solubility also varies considerably with location
and depth in the ocean; it is greater at lower pH and lower
concentrations of carbonate and bicarbonate ions, but is also
affected by hydrostatic pressure (more soluble at deeper depth),
temperature (more soluble at colder temperatures), and salinity
(less soluble at higher salinities). Recent evidence (Fabry et al.,
2008; Feely et al., 2008) suggests that the extent of upper ocean
habitat in which aragonite is soluble is increasing, largely
through the progressive shoaling of solubility isoclines. In some
parts of the ocean, notably the Subarctic North Pacific (Fabry
et al., 2008; see Figure 1), eastern-boundary-current upwelling
regions (Feely et al., 2008), the Arctic Ocean (Yamamoto-Kawai
et al., 2009), and the Southern Ocean (Orr et al., 2005), deep
ocean waters are strongly corrosive, and the solubility threshold
is persistently or intermittently at or very close to the sea surface.
Impacts on pteropods of low pH and aragonite solubility have
been demonstrated at the level of individual organisms (Orr et al.,
2005; Fabry et al., 2008). Clio pyramidata from the Subarctic
Pacific that were incubated for up to 48 h in aragonite-undersaturated water (artificially adjusted to levels forecast for Southern
Ocean surface water in 2100) showed microscopic evidence of
shell dissolution at their margins, and decreased uptake rate of
isotopically labelled calcium, i.e. a reduction in their deposition
of new shell material. Unfortunately, shell-forming pteropods
are notoriously difficult to maintain in laboratory containers for
more than a day or two, in part because of their unusual feeding
mechanism (a large external mucus feeding web; Gilmer and
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Pteropod time-series from the NE Pacific
449
Figure 1. Meridional sections of (a) aragonite solubility (Varag) and (b) partial pressure of carbon dioxide (pCO2) along 1528W in the North
Pacific Ocean (adapted with permission from Fabry et al., 2008). Aragonite is undersaturated at V , 1.0 (upper limit marked by dark shading).
Undersaturation covaries positively with pCO2 and depth, and negatively with dissolved oxygen (not shown). In the eastern North Pacific,
undersaturation is most extreme, and approaches closest to the sea surface, within the core of the Subarctic Alaska Gyre (538N).
Harbison, 1986). Therefore, very little is yet known about their
response to chronic exposure to levels of aragonite undersaturation already present in the contemporary ocean.
To evaluate ecological consequences, much more needs to be
known about long-term population-level changes in reproduction,
survival, and abundance, in addition to what is already being
learned about organism-level changes in physiology and details of
shell structure. To answer these questions, time-series of pteropod
abundance and species composition throughout the ocean
are needed. The need is most urgent in ocean areas in which acidification is most extreme. Palæo-stratigraphy of skeletal remains
buried in ocean sediments is one effective and traditional way to
estimate long-term histories of abundance and species composition. Unfortunately, over much of the globe, pteropod shells are
not preserved at seabed depths beneath many of the areas where
they now live in the upper ocean. In the ocean areas of greatest
concern (those where near-surface undersaturation is present
now or projected for the near future), their fossil shells will dissolve
quickly at depths of more than a few hundred metres (Figure 1).
In those areas, the best (probably the only) alternative is to estimate time-series of pteropod population density from systematic
and repeated zooplankton net tows collecting living animals from
the upper ocean. The resulting time-series are necessarily shorter
(the maximum length of ongoing zooplankton time-series is
about 60 years) than palæo-reconstructions, but because ocean
acidification is ongoing and cumulative, the existing time-series
do cover the years (present and recent past) in which the effects
of acidification are likely to have been largest. Despite this clear
rationale, there have as yet been few published studies of pteropod
time-series. In addition to this paper, we are aware of published anal
yses, all recent, from just two ocean regions: the California Current
(Lavaniegos and Ohman, 2007; Ohman et al., 2009) and the North
Atlantic (Head and Pepin, 2010). In this paper, we extend the base
of information with four time-series from the Subarctic NE Pacific.
NE Pacific time-series locations and their oceanographic
characteristics
Fisheries and Oceans Canada currently maintains zooplankton
time-series in four subregions of the NE Pacific. Figure 2 shows
their relative locations and the standard sampling stations within
each subregion (the number and locations of Line P stations
are fixed, but additional or different sites are sometimes sampled
in the continental margin regions). Sampling methods are
detailed later.
The longest time-series (1979–present) is from the continental
margin off the southwest coast of Vancouver Island. This region is
sampled four to six times per year. Sampling dates vary from year
to year, with best coverage during the March–October plankton
growing season. The southern Vancouver Island (SVI) region is
often considered to form the northern and upstream end of the
California Current system (CCS). There, the continental shelf
is wider than most places along the Pacific Coast of North
America. Oceanographic characteristics include strong seasonal
variability of the speed and direction of winds and surface currents
(for more details and comparison with other parts of the CCS, see
the review by Mackas, 2006). Winds and outer-continental-shelf/
450
D. L. Mackas and M. D. Galbraith
Figure 2. Map showing the range of locations included in the four DFO zooplankton time-series in the NE Pacific. Two of the regions are
temperate– boreal continental margin: SVI (standard sampling locations indicated by open triangles), and NVI (black inverted triangles).
Bathymetry contours are 200 m (thick dark grey line) and 1000 m (thin black line). The Line P section is oceanic and boreal– Subarctic, but
outer Line P (open circles, stations P, P20, and P16) and inner Line P (filled circles, stations P4, P8, and P12) locations differ in water properties,
plankton composition, and seasonality. Outer Line P is an iron-limited HNLC environment, whereas inner Line P usually shows summer
nitrogen-depletion (dashed line contours in the offshore region show typical locations of summer surface nitrate isopleths, based on Whitney
et al., 1998, 2005). The two oceanic subregions share similar zooplankton species-dominance hierarchies, but differ in seasonal timing (see text
for additional details).
slope surface currents are equatorward and upwelling-favourable in
summer, and poleward and onshore-convergent in winter. In
addition to summer upwelling, the region receives large and persistent nutrient inputs supplied by the estuarine circulation in Juan de
Fuca Strait and the poleward Vancouver Island Coastal Current.
Seasonal reversal of wind and currents contributes to seasonal
changes in zooplankton community composition by bringing
southern-origin species (both coastal and oceanic) into the region
in winter, and transporting boreal-origin species equatorward and
seaward in summer. One consequence is that the relative abundance
of lower-latitude “warm water” taxa in the northern California
Current is usually greatest in winter, whereas higher-latitude “cold
water” taxa become more dominant in summer. Interannual variability in the timing and intensity of the flow reversals appears to be
responsible for much of the interannual variability in community
composition (for examples and additional interpretation, see
Hooff and Peterson, 2006; Mackas et al., 2001).
The northern Vancouver Island (NVI) continental margin has
been sampled since 1990. The number of samples per year was
low (,10 year21) between 1992 and 1995, but since 1996, sampling
intensity and seasonal coverage has been similar to that in the SVI.
The NVI region is in the transition zone between the equatorward
California Current and the poleward Alaska Current. Although
wind and current patterns are seasonal, the duration and intensity
of summer upwelling is less than off SVI, and storms and windmixing are more frequent and more intense. The continental shelf
is very narrow off the west side of Vancouver Island, but broad
north of Vancouver Island. The zooplankton community
composition is similar to that in the SVI, except that the relative
importance of southern-origin taxa is usually lower.
Zooplankton were sampled frequently at Station P from 1956 to
1980 as part of the overall weathership programme (see Freeland,
2007, for a historical summary). However, most samples were processed only for total biomass (Fulton, 1983) or biomass within a
small number of higher level taxonomic categories (LeBrasseur,
1965). This time-series unfortunately ended in 1980 with the termination of the weathership programme. Zooplankton sampling
along Line P resumed, and the analysis of species-level community
composition was initiated in 1996. The Line P transect is now
sampled three times annually (February –early March, late May
or June, and between August and early September). Stations
along the line show a strong gradient in water properties and
also in nutrient and plankton dynamics, from relatively strong
coastal influence and seasonality of primary productivity at P4
(similar to the continental slope locations in the SVI and NVI
regions) to Subarctic high nutrient, low chlorophyll (HNLC)
waters at the west end of the line (Whitney et al., 1998, 2005;
Peña and Varela, 2007). For analysis, we separate Line P into
inner and outer segments based on the water property and plankton differences. Outer Line P locations (Stations P, P20, and usually
P16) are located within the HNLC environment: primary productivity, nitrate utilization, phytoplankton biomass accumulation, and average phytoplankton cell size are all limited by the
low supply of iron. At the inner Line P locations (P4, P8, and
usually P12), there is a spring phytoplankton bloom, post-bloom
availability of major nutrients is low, and the upper ocean is
warmer and slightly less saline. There are also along-line differences
in the composition and seasonal timing of the zooplankton community (see recent summary by Batten et al., 2010). The outer
Line P zooplankton community is dominated by Subarctic
oceanic species and the annual cycle of zooplankton biomass by
an early summer peak of large ontogenetically migrating copepods.
Although the large Subarctic and migratory copepods remain
dominant at inner Line P locations, their seasonal peak is earlier
by about a month, and the occurrence rate and contribution to
total biomass of smaller southern- and coastal-origin species are
greater (although remaining lower than in the SVI and NVI continental margin region).
451
Pteropod time-series from the NE Pacific
Figure 3. Time-series of three regional indices of ocean physical climate in the North Pacific. The solid black line is the upper ocean (10–
50 m) temperature anomaly averaged along Line P (updated from Crawford et al., 2007), and the solid grey line with filled circles the average
Pacific Decadal Oscillation (PDO) during the previous winter [the PDO is the leading Empirical Orthogonal Function (EOF) of sea surface
temperature variability, SST, in the North Pacific; positive values are associated with positive temperature anomalies in the NE Pacific]. The
dashed grey line and open triangles are sign-reversed annual averages of the North Pacific Gyre Oscillation (NPGO, estimated from sea surface
height anomalies, but it is strongly correlated with the second EOF of SST variability; negative values imply an additional warming component
in the NE Pacific).
Most parts of the NE Pacific experience strong interannualto-decadal variations in upper ocean temperature (Figure 3) that
are driven by between-year differences in wind intensity and direction, and resulting ocean current patterns. Many zooplankton taxa,
including pteropods, show strong interannual variations in abundance and biomass that are correlated with these variations in
ocean climate (Mackas et al., 2001).
Ecological characteristics of the dominant pteropods
in the NE Pacific
Except for the descriptions of relative abundance and seasonality
within the local time-series, the material here is summarized
from other sources. Information on taxonomic hierarchy, life histories, and diet is taken from the extensive material in Lalli and
Gilmer (1989). Additional information on zoogeographic distributions in the North Pacific is derived from McGowan (1967,
1971) and Bé and Gilmer (1977). Naming conventions for subspecies and morphotypes follow the ETIBioInformatics KeyToNature
Marine Species Identification Portal (http://species-identification.
org/index.php).
Taxonomically, the pteropods are broadly divided among taxa
that have a calcareous shell throughout their lifespan (Order
Thecosomata) and taxa that lack a shell after their larval stage
(Order Gymnosomata). Thecosomes feed on small particles (phytoplankton, microzooplankton, small mesozooplankton) captured
using a large external mucus feeding web. In contrast, gymnosomes
are voracious raptoral predators, with a diet consisting mostly of thecosomes. Both thecosomes and gymnosomes are hermaphroditic,
and produce floating egg masses that contain hundreds to thousands
of eggs. Only three pteropods have been regularly or occasionally
abundant in our time-series samples: two thecocomes (Limacina
and Clio) and one gymnosome (Clione), so most of the analysis
and discussion is limited to these three species.
Limacina helicina
The coiled thecosome Limacina helicina is usually the most abundant pteropod in all our study areas, and is present in most of the
samples throughout the year. Average seasonal cycles of abundance
and biomass in each region are presented below and in Figure 2. In
our sampling regions, its adult body size is smaller (typically
,2 mm, only rarely 3 –5 mm) than Clione or Clio, but high
average abundance usually also makes it the greatest contributor
to total pteropod biomass. At species level, the zoogeographic distribution of L. helicina is bipolar, but most taxonomists now consider it to be a species complex made up of two genetically distinct
subspecies (Hunt et al., 2010) and five morphotypes. Northern
hemisphere animals are the subspecies L. helicina helicina.
Morphotypes acuta and pacifica are present in the Pacific, with
acuta having an oceanic and Subarctic centre of distribution,
and pacifica extending farther south in the eastern North Pacific
(McGowan, 1971). Both forms (and possible intergrades) are
present in our samples. Peak reproduction in the study region is
in spring, when early growth stages (,1 mm) are sometimes
very abundant. Later stages show a highly variable vertical distribution that is weather-dependent (avoiding the surface under
stormy conditions; Mackas and Galbraith, 2002; Mackas et al.,
2005). Although most animals are above 100 m both day and
night in the study region, some healthy animals are often
present considerably deeper (to 500 m or more). This extensive
depth range may limit their ability to maintain nearshore populations; although Limacina is often present in the samples from
continental shelf locations, it is usually 2- to 5-fold more abundant
seaward of the shelf break.
Clione limacina
The gymnosome Clione limacina is also usually present in our
samples. Like L. helicina, it inhabits cool to cold water and has a
bipolar zoogeographic distribution, and is probably part of a
species complex (the subspecies and morphotype in our samples
is probably C. limacina subsp. limacina f. limacina, present in
both the North Atlantic and the North Pacific). Maximum body
size in the region is about 2 cm, but smaller animals (0.5 –1 cm)
are more common. In the NE Pacific, both seasonal (see below)
and spatial distributions are similar to those of L. helicina, which
452
is considered to be its primary food source. However, in recent
years, we have found Clione present, abundant, and apparently
healthy at dates and locations where the larger Clio was by far
the dominant thecosome.
Clio pyramidata f. lanceolata
Clio is a thecosome in the family Cavoliniidae. Shell shape is
conico-pyramidal rather than helical. In the study region, it
reaches an adult size that is considerably larger (shell and body
lengths up to 2 cm) than Limacina, and larger than most
co-occurring Clione. Diel vertical migration is more consistent
than Limacina, but does seem to show weather-dependence
(surface avoidance during stormy conditions). The form present
in our samples is C. pyramidata lanceolata. Its zoogeographic
distribution in the North Pacific is centred in the oceanic tropics
(Bé and Gilmer, 1977), but it extends regularly into the central
and southern parts of the CCS (32 –408N; McGowan, 1967;
Ohman et al., 2009), and in at least some years to 50 –538N in
the Subarctic Alaska Gyre (Mackas et al., 2005; Tsurumi et al.,
2005). The species is probably being carried into the region in
winter by poleward transport along the continental slope in the
Davidson Current (see Mackas et al., 2005, for further discussion),
but meridional exchange across the oceanic Subarctic front is also
possible. The presence of Clio in our study samples has historically
been rare and intermittent, but it has increased in recent years (see
below). In years when it is present, Clio can become very common
off Vancouver Island and in at least the SE portion of the Alaska
Gyre, accounting for 50% or more of the total zooplankton
biomass in the upper water column. It is also occasionally responsible for very large vertical flux into sediment traps moored at
depths of 1000 and 3800 m (Tsurumi et al., 2005).
Methods
Zooplankton sampling
Since 1983, nearly all sampling has been by vertically integrated
tows with flow-metered bongo nets (0.25 m2 mouth area) fitted
with 0.23 mm black nylon mesh (from 1979 to 1982, a slightly
smaller ringnet with white nylon netting was used). Tow depths
are near-bottom to surface at stations on the continental shelf,
and from 250 m to the surface at deeper locations. Tows are
made both day and night to maximize ship utilization. The
catch from one side of the bongo net is preserved immediately
in buffered seawater formalin, and is used for shore-based microscopic identification and enumeration of species and developmental stage. The catch from the other side is quick-frozen and usually
used for estimating the size-fractionated bulk dry-weight biomass.
In addition to this time-series sampling, several shorter term
studies have supported more-intensive sampling at Station P
(Mackas et al., 1993; Goldblatt et al., 1999), in the large anticyclonic eddies that propagate westwards from the continental margin
into the Alaska Gyre (Mackas and Galbraith, 2002; Mackas et al.,
2005), and along the Vancouver Island continental margin
(Mackas and Yelland, 1999; Lu et al., 2003). These studies provided
detailed information on zooplankton vertical distribution, zooplankton developmental timing, and the rates and mechanisms
of cross-shore and alongshore transport and dispersal.
Data analysis
Our analysis of interannual variability and trends in pteropod
abundance uses data-processing methods developed for our
studies of the SVI zooplankton time-series, and are described in
D. L. Mackas and M. D. Galbraith
detail in Mackas et al. (2001). A summary of the analysis sequence
is given below. As in our previous analyses, we use
biomass-within-species rather than numerical abundance as our
estimate of population size. This choice offers two advantages:
better cross-species comparison of standing stock, and greater
within-species weighting of individuals that have survived to
larger age and size, and are therefore more likely to reproduce
successfully.
(i) The first step is to develop monthly-resolution estimates of
average seasonal cycles of biomass B for each species and
spatial region. To do this, we use across-years, within-month,
within-region geometric means of estimated within-species
dry-weight biomass (in turn estimated as the sum across
size/stage of abundance multiplied by individual body
size). The baseline time-periods for these reference “zooplankton climatologies” run from the start of each timeseries through 2005.
(ii) For all months in which data are available in a given year, we
then compare the spatially averaged regional observations
B(t) with the corresponding climatology B to produce a
within-year set of log-scale anomalies b′ (t). These are
calculated as
B(t)
′
b (t) = log[B(t)] − log[B] = log
.
B
Although other anomaly formulations (e.g. linear-scale
difference B(t) − B) are possible, log-scale representation
provides a good description of proportional change, is symmetric about zero, is approximately normally distributed,
and largely eliminates sensitivity to capture-efficiency bias
(for further discussion, see Mackas et al., 2001; Mackas and
Beaugrand, 2010).
(iii) Finally, we calculate within-year averages of the available
monthly anomalies to produce time-series of annual
anomalies. Results for SVI and NVI are based on the offshore
subset of samples (locations deeper than 200 m); adjoining
shelf populations closely tracked the offshore time-series,
but on-shelf abundances were usually lower and more erratic.
Average annual cycles and anomaly time-series are reported here
using plots of geometric mean abundance and biomass, and
log-scale annual biomass anomalies for each region and species.
Individual point estimates for the monthly climatologies and
annual anomalies can be noisy if averaged from a small number
of samples, because of contamination by unresolved spatial and
temporal patchiness. Therefore, only the months (climatologies)
and years (anomaly time-series) for which we had a reasonably
large (.10) total number of samples that were also broadly distributed across years and locations-within-region are shown.
The main question posed is whether all or most species and
regions share significant downward trends that (if present)
would be evidence for a shared adverse response to increasing
pCO2 and aragonite solubility. To address this, trendlines were
fitted to each time-series, and the fluctuations and trends in the
time-series are compared with the three regional-scale indices of
regional ocean warming and circulation shown in Figure 3. Line
P upper ocean temperature anomalies were updated from
Crawford et al. (2007); Pacific Decadal Oscillation time-series
Pteropod time-series from the NE Pacific
453
Figure 4. Average seasonal cycles of the three regionally dominant pteropod species in each of the four time-series regions. Monthly
geometric mean abundances are indicated by line graphs, monthly geometric mean biomass by column graphs (vertical axes are on a log scale
in all panels). In all regions, Limacina has the highest average biomass and abundance, followed by Clione. The annual maxima of the cool water
species Limacina and Clione are in spring (April or May) in all regions; the continental margin regions have a secondary maximum in October
or November (after the autumn transition to poleward alongshore flow). The annual maximum of the temperate –subtropical species Clio is in
September/October.
were downloaded and averaged from http://jisao.washington.
edu/pdo/PDO.latest); and North Pacific Gyre Oscillation data
were downloaded from http://www.o3d.org/npgo/.
Results and discussion
Average seasonal cycles of abundance and biomass
Figure 4 depicts estimates of average monthly abundance and
biomass for the three dominant pteropod species in each timeseries region. As noted above, estimates for months in which
sampling was limited in a given region were excluded as unreliable,
but estimates from those months are consistent with the descriptions that follow.
In all regions and months of the year, Limacina is on average
the most abundant pteropod, and also has the highest biomass.
Annual ranges of Limacina biomass and abundance overlap
among regions, but are on average higher at more oceanic and/
or colder locations (outer Line P inner Line P . NVI . SVI).
The seasonal maximum of abundance and biomass is in spring
in all regions (April along the continental margin, May or June
454
D. L. Mackas and M. D. Galbraith
Figure 5. Interannual fluctuations and trends of L. helicina populations in four NE Pacific regions [top panel, NVI; centre panels, outer Line P
(left) and inner Line P (right); bottom panel, SVI]. Column graphs are annual log-scale biomass anomalies. Grey circles indicate years with little
or no data. Lines are linear trend vs. year (significant trends indicated by solid lines and non-significant by dashed lines). Limacina has declined
significantly in both continental margin regions. It has also declined on the nearshore end of Line P, but the time-series is not yet long enough
for this decline to be statistically significant. The seaward half of Line P shows great interannual variability, but no significant trend.
in the Alaska Gyre). Minimum abundance/biomass is in
September along the continental margin, and in winter in the
Alaska Gyre. Continental margin regions show a secondary
autumn maximum (October or November). Timing of this peak
follows the autumn transition back to poleward, downwelling-
favourable winds and poleward alongshore currents. This increase
is probably attributable to advection/immigration rather than
local growth and reproduction, and the probable source is adjoining offshore waters, although alongshore transport from southerly
source regions cannot be eliminated as a contributor.
455
Pteropod time-series from the NE Pacific
Table 1. Statistical associations among NE Pacific time-series of pteropod biomass anomalies and regional indices of ocean physical
climate.
Variable
Limacina
Clione
Clio
Line P Tanom
Winter PDO
Annual NPGO
Limacina
–
20.23 to +0.36
20.45 to +0.01
+0.14 to +0.37
20.01 to +0.44
20.33 to 20.04
Clione
0.11
–
+0.04 to +0.58
20.41 to 20.05
20.39 to 20.20
20.19 to +0.30
Clio
20.28
+0.26
–
20.32 to 20.13
20.20 to 0.00
+0.09 to +0.60
Line P Tanom
+0.30
20.24
20.23
–
n/a
n/a
Winter PDO
+0.21
20.31
20.14
+0.43
–
n/a
Annual NPGO
20.19
+0.01
+0.31
20.63
20.14
–
Table entries are mean (above diagonal) and range (below diagonal) of within-region product-moment correlations.
Monthly Clione abundances and biomass levels are considerably less than those of Limacina (1 and 20%, respectively),
but the two species have similar seasonal cycles within each
region. This is not surprising, given the known dependence of
Clione on Limacina as its main food.
For the warm-water species Clio, occurrence rates and abundance/biomass are extremely variable among years (discussed
below along with its anomaly time-series). However, there are clear
differences from the seasonal patterns of Limacina and Clione. Clio
is not common in most years (Figure 4; monthly average abundance
,0.01 m22; often absent in individual samples) and shows no clear
seasonal cycle, but monthly average biomass has a strong autumn
maximum driven by the combination of large adult body size and
moderate-to-high abundance in some years. This pattern of interannual variability is consistent with occasional winter or spring
advective delivery of eggs or early juveniles from the south, followed
by strong individual somatic growth and relatively good survival
through summer and early autumn, and eventual late autumn mortality of the adults. Sediment-trap records from Station P also indicate occasional large autumn mortality and sinking of Clio in the
Alaska Gyre (Tsurumi et al., 2005). Between-region comparisons of
average biomass suggest higher population density along Line P
than along the continental margin, but this comparison may be misleading because of differences in the years covered by the Line P and
continental margin baselines. The occurrence rate of Clio was very
low in all regions in years before 2001, but subsequent years with elevated abundance in all regions make up nearly half the Line P climatology baseline and a much smaller fraction of the SVI and NVI
climatologies (18 and 33%, respectively).
Interannual variability in the Subarctic NE Pacific
Limacina helicina
Annual anomalies of Limacina biomass in each subregion are shown
in Figure 5. The time-series include large short-term fluctuations but
also significant or near-significant sustained and approximately
linear downward temporal trends in three of the four subregions.
If consistent across species, these temporal trends provide plausible
evidence for the effects of the corresponding gradual trends of pCO2
and aragonite solubility. Associations with additional potential
drivers of changes in Limacina populations are quantified in
Table 1. These include changes in the abundance of competitors
and predators (correlations among the anomaly time-series of the
three pteropod species) and changes in the physical rather than
the chemical “climate” of the ocean (temperature and circulation
indexed by the time-series in Figure 3).
Clione limacine
The corresponding annual anomalies of Clione are shown in
Figure 6. Again, the time-series include large interannual
variability together with persistent trends, but for this species,
the temporal trends are consistently upward (significant in the
SVI region, and near-significant in the short-time outer Line P
time-series). Correlation with the preferred prey (Limacina) is
weakly negative in three of the four regions (Table 1), possibly
indicating top-down control of Limacina by the abundance of
an obligate predator. However, Limacina has many additional predators, e.g. fish and baleen whales, and bottom-up correlations of
Clione with its physical environment usually have opposite sign to
those of Limacina.
Clio pyramidata
Figure 7 shows the annual anomalies of C. pyramidata in each
region. The Clio time-series are dominated by large-to-very-large
positive anomalies in a small subset of years (i.e. 2001, 2007,
and 2009) that are essentially the same in all four regions, although
the strength of the 2007 spike was quite variable. As all these highbiomass years are relatively recent, the linear fit to the longer SVI
time-series shows a significant upward trend. However, the main
within-time-series contrast is before vs. after 2000.
Between-pteropod-species comparisons within
the Subarctic NE Pacific
One of our three pteropod species (Limacina) showed fairly strong
declining temporal trends (downwards in three of four regions)
that could be indicative of population responses by Limacina to
increasing ocean acidity. However, two lines of evidence suggest
that acidification has not yet become the primary driver of pteropod population changes in the NE Pacific. First, present-day and
year-round acidification stress is probably most severe in the offshore core of the Alaska Gyre (the outer Line P region). There,
the recent Limacina and Clione temporal trends are both weakly
positive, and Clio has shown little or no trend. Second, Clione
and Clio have had weak-to-significant upward trends in the
more nearshore regions where Limacina has been declining.
Although we do not yet know the relative sensitivity of the three
species to ocean acidification, it seems unlikely that the consequences would be negative for one thecosome, but positive for a
gymnosome and a different thecosome.
If past and current acidification stress is excluded as a primary
driver of changes to date (consistent with the time-series from
other regions described below), we are still left with an interpretative puzzle. Taken alone, the pteropod time-series (Figures 5 –7)
are consistent with a hypothesis of poleward zoogeographic displacement in response to progressive global warming: a moderate
decline of the (primarily) Subarctic Limacina, a strong increase
of the subtropical Clio, and a moderate increase of the
(prey-limited?) thecosome predator Clione. Strong poleward displacement has been observed both locally and elsewhere for
456
D. L. Mackas and M. D. Galbraith
Figure 6. Interannual fluctuations and trends of C. limacina populations in four NE Pacific regions (panel configuration and symbols as in
Figure 4). Clione trends are opposite to those of Limacina in three of the four regions (significantly positive in SVI, and non-significantly
positive in NVI and inner Line P), but close to being significantly positive on outer Line P.
other zooplankton taxa (Lavaniegos and Ohman, 2007; Mackas
and Beaugrand, 2010). The problem with this explanation for
the NE Pacific pteropod changes is that the local 10– 20 year
temperature trend in the Subarctic NE Pacific has been downward
rather than upward. We are left with the somewhat paradoxical
observation that anomalies of a zoogeographically cool-water,
boreal –Subarctic thecosome (Limacina) are positively correlated
with warm anomalies, whereas the anomalies of a zoogeographically warm-water, temperate–subtropical thecosome (Clio) are
correlated with cool anomalies. The remaining, but not yet satisfactory, explanation is that trophic interactions, or climate influences other than temperature, e.g. zonal circulation, must be
involved. Something has clearly allowed Clio to colonize the
Subarctic NE Pacific more often than it used to, and something
is driving a coincident decline in continental margin abundance
of Limacina. The thecosome predator Clione does not seem to
be bothered by the change, suggesting that it can and does eat
Clio if Limacina is less available.
Pteropod time-series from the NE Pacific
457
Figure 7. Interannual fluctuations and trends of C. pyramidata populations in four NE Pacific regions (panel configurations and symbols as in
Figures 4 and 5). The Clio time-series are dominated by large-to-very-large positive anomalies in a small subset of years (2001, 2007, and 2009).
As all these high-biomass years are relatively recent, the linear fit to the longer SVI time-series shows a significant upward trend.
Comparison with pteropod time-series elsewhere,
and recommendations for the future
We earlier cited recent published analyses of 60-year pteropod
time-series from two other ocean regions: the California Current
(a group-level analysis by Lavaniegos and Ohman, 2007, and a
species-level analysis by Ohman et al., 2009), and the
Subarctic NW Atlantic (“Limacina spp.” in CPR samples; Head
and Pepin, 2010).
Both these analyses agree with our observation/interpretation
that there have been (as yet) no sustained and strong downward
trends in total pteropod abundance/biomass. The California
Current time-series contain substantial interannual variability,
but almost no long-term trend. The NW Atlantic (where aragonite
solubility is much less than in either the California Current or the
Alaska Gyre) shows an erratic upward trend (maximum pteropod
abundance during the 1990s and minimum abundance during
458
the 1970s and 1980s, and the most-recent decade intermediate
between these extremes).
An important caveat in this discussion is that the main concerns about ocean acidification are for what will happen to
ocean biota post 2050 or 2100. The conclusion that we have not
yet passed a tipping point does not mean that we will not pass a
tipping point in the near (or moderately distant) future. One of
the best candidates for “canary” indicators will be the continued
maintenance of pteropod time-series in regions where we now
know past and recent population histories and baselines.
Acknowledgements
We thank all our seagoing DFO colleagues who helped to collect
the samples in all seasons and weathers. We also enjoyed and
learned from our frequent conversations with retired pteropod
expert Carol M. Lalli, and the manuscript was improved by the
constructive comments of Lou Hobson, guest editor Sanae
Chiba, and two anonymous, but very helpful, referees.
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