Anomalous ichthyoplankton distributions and concentrations in the
northern California Current during the 2010 El Niño and La Niña events
Auth, T. D., Brodeur, R. D., Peterson, J. O. (2015). Anomalous Ichthyoplankton
Distributions and Concentrations in the Northern California Current during the
2010 El Niño and La Niña Events. Progress in Oceanography, 137(A), 103-120.
doi:10.1016/j.pocean.2015.05.025
10.1016/j.pocean.2015.05.025
Elsevier
Version of Record
http://cdss.library.oregonstate.edu/sa-termsofuse
Progress in Oceanography 137 (2015) 103–120
Contents lists available at ScienceDirect
Progress in Oceanography
journal homepage: www.elsevier.com/locate/pocean
Anomalous ichthyoplankton distributions and concentrations
in the northern California Current during the 2010 El Niño
and La Niña events
Toby D. Auth a,⇑, Richard D. Brodeur b, Jay O. Peterson c
a
b
c
Pacific States Marine Fisheries Commission, Hatfield Marine Science Center, 2030 Marine Science Drive, Newport, OR 97365, USA
Northwest Fisheries Science Center, National Oceanographic and Atmospheric Administration, Hatfield Marine Science Center, 2030 Marine Science Drive, Newport, OR 97365, USA
Cooperative Institute for Marine Resources Studies, Oregon State University, Hatfield Marine Science Center, 2030 Marine Science Drive, Newport, OR 97365, USA
a r t i c l e
i n f o
Article history:
Received 6 March 2013
Received in revised form 26 May 2015
Accepted 27 May 2015
Available online 3 June 2015
a b s t r a c t
In late spring of 2010, the northern California Current (NCC) experienced a transition from El Niño to La
Niña conditions resulting in anomalous distributions and concentrations within the ichthyoplankton
community. We analyzed larval fish data collected during the four months before and after this transition
and compared them to data from three previous studies conducted in the NCC. In one comparison, concentrations of larvae collected during winter from stations 2 to 46 km offshore along the central Oregon
coast were higher in 2010 than in any other year from 1998 to 2011. In a second comparison of nearshore
larvae collected during six periods (1971–1972, 1978, 1983, 1998, 1999–2002, and 2003–2005) previous
to 2010, concentrations of total larvae and most dominant larval taxa were higher during the winter/spring and lower during the summer/fall seasons in 2010 (corresponding to the shift from El Niño
to La Niña conditions) than during similar seasons in any other annual period. In a third comparison, larvae collected from stations 21 to 102 km offshore along the southern Washington to south-central
Oregon coast in May 2010, at the end of the El Niño event, were found in higher concentrations than during any May from 2004 to 2009 and 2011. The high concentration of larvae in the winter and spring of
2010 was likely the direct result of El Niño and warm-ocean conditions (high values of the MEI, NOI,
and PDO) along with strong downwelling and onshore transport that increased the abundance of offshore
taxa over the shelf. Continued monitoring of the NCC is warranted as El Niño effects on larval fish
observed in the past may not be indicative of future effects.
Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction
In late spring of 2010, the northern California Current (NCC)
experienced a sudden transition from the moderate El Niño of
2009 to 2010 to a strong La Niña characterized by cool ocean conditions followed by strong upwelling (Bjorkstedt et al., 2011).
Environmental fluctuations are common in the NCC (Schwing
et al., 2006; Checkley and Barth, 2009), and have the potential to
cause substantial changes to the community, composition, and
food-web dynamics of the ecosystem as a whole (King et al.,
2011; Francis et al., 2012), and in particular to trophic levels ranging from primary production (McGowan et al., 1998), through
zooplankton (Peterson et al., 2002; Menge et al., 2011), and on to
higher trophic levels (Ainley et al., 1995; Lluch-Belda et al., 2005;
Zamon and Welch, 2005; Brodeur et al., 2006). Ichthyoplankton
⇑ Corresponding author. Tel.: +1 541 867 0350.
E-mail address: tauth@psmfc.org (T.D. Auth).
http://dx.doi.org/10.1016/j.pocean.2015.05.025
0079-6611/Ó 2015 Elsevier Ltd. All rights reserved.
in particular have been shown to be a sensitive indicator of environmental conditions in the California Current (Smith and Moser,
2003; Brodeur et al., 2008; Hsieh et al., 2009; Auth et al., 2011),
including the often dramatic effects of El Niños (Brodeur et al.,
1985; Fiedler et al., 1986; Doyle, 1995; Franco-Gordo et al.,
2008). However, any resulting substantial and sudden changes in
ichthyoplankton community composition, distribution, and abundance, as well as the forcing factors driving them, are often masked
by the amalgamation of data across larger temporal scales. Only by
comparing larval data immediately before and after such dramatic
events to historical data collected at similar spatial and temporal
scales during other annual and decadal periods can the nature,
extent, cause, and effect of the anomalies be truly ascertained.
Moser et al. (1987) reported on broad changes in the ichthyoplankton community in the California Cooperative Oceanic
Fisheries Investigations (CalCOFI) region in the southern
California Current in 1954–1960, a period encompassing both El
Niño and La Niña conditions, and documented how changes
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T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
between the cold 1955–56 and warm 1958–59 periods altered the
boundary between two pelagic ichthyoplankton groups.
Funes-Rodríguez et al. (2011) conducted a more focused study on
the effects of the transition from the 1997–1998 El Niño to the
1998–2000 La Niña on the ichthyoplankton community off of the
Baja California Peninsula, and reported an increase in diversity,
richness, and abundance of tropical species expanding northward
during the El Niño, followed by a rapid recovery to normal assemblage structure during the following La Niña. Thompson et al.
(2012) conducted a similar study in the southern California
Current region for the 2002–2003 La Niña to El Niño transition,
and found that oceanic species moved into the near-shore
Cowcod Conservation Area between 2002 and 2003 in association
with the influx of warmer, offshore waters. Brodeur et al. (1985)
reported on the atypical ichthyoplankton community observed in
the near-shore region off the central Oregon coast in the NCC during the extreme 1983 El Niño, and concluded that changes in the
hydrographic conditions associated with onshore surface drift
and reduced summer upwelling during the El Niño period could
explain the changes in ichthyoplankton distributional patterns.
Doyle (1995) documented similar anomalous species occurrences
and distributions during the 1983 El Niño event and contrasted it
with normal years before and after this event. Although all of these
studies documented the response of ichthyoplankton assemblages
to either the initiation or cessation of El Niño-Southern Oscillation
(ENSO) events in different parts of the California Current, no study
to date has been conducted in the NCC region that has directly
assessed the effects of an ENSO change on the ichthyoplankton
community immediately before and after this transition in relation
to fluctuating environmental variables.
The purpose of this study is to compare the composition, concentration, distribution, and structure of the larval fish community
in the NCC immediately before and after the 2010 transition from
El Niño to La Niña conditions to similar seasonal periods described
in three previous studies conducted in the same region across comprehensive temporal (i.e., decadal, annual, seasonal, monthly, and
biweekly) and spatial (i.e., latitudinal and cross-shelf) scales, and
test for differences to determine the presence and extent of
anomalies in the ichthyoplankton community surrounding this
transitional period. Further, we identify the existence, magnitude,
and trends of environmental factors, both basin-scale and regional,
that may be driving any observed anomalies. Through this study
we assess how sudden changes in the environment may cause substantial anomalies in fish early-life stages that could affect future
recruitment of ecologically and commercially important fish
stocks.
2. Methods
2.1. Comparative studies
The three comparative studies used together with the new data
from the present study are: winter (Daly et al., 2013), near-shore
biweekly (Auth et al., 2011), and coast-wide (Auth, 2011). Daly
et al. (2013) conducted a study examining winter biomass of prey
fish larvae as a potential indicator of marine feeding conditions for
juvenile salmon using ichthyoplankton samples collected at five
stations located 9–46 km offshore along the Newport
Hydrographic (NH) line (44.65°N; Fig. 1) off the central Oregon
coast during January–March 1998–2010. Auth et al. (2011) characterized the influence of large-scale and local environmental factors
on the presence–absence, concentration, and community structure
of larval fish based on biweekly–monthly samples collected
throughout the year at two nearshore (9 and 18 km) stations along
the NH line as part of four previous studies: data from 1996 to
2005 (Brodeur et al., 2008) were compared with historical data
from the 1970s (Richardson and Pearcy, 1977; Laroche et al.,
1982) and 1980s (Brodeur et al., 1985) to evaluate decadal (5–
10 yr), annual, and seasonal variability in the larval community.
Lastly, Auth (2011) conducted a coast-wide analysis of the ichthyoplankton community off the Oregon and Washington coasts using
samples collected from five cross-shelf stations located 21–102 km
offshore along each of four latitudinal transects (i.e., Willapa Bay
[WB; 46.67°N], Columbia River [CR; 46.16°N], NH, and Heceta
Head [HH; 44.00°N]; Fig. 1) monthly from May to September in
2004–2009 that examined annual, monthly, latitudinal, and
cross-shelf variability.
2.2. Sampling procedures
A total of 236 ichthyoplankton samples were collected in 2010
and 2011 (Appendix) at the same station locations (Fig. 1) and
using similar sampling protocols as those collected in the three
comparative studies with which they were analyzed (Table 1).
For the samples collected for comparison with the near-shore
biweekly study, we used the sampling-depth protocol employed
in the collections in 1996–2005 (i.e., 0–20 m depth). The samples
collected prior to 1996 for the near-shore biweekly study were
obtained from within 5 m of the bottom to the surface (according
to the sampling protocols of the composite comparative studies
examined by Auth et al. [2011]) at the two stations sampled, which
were a relatively shallow 60 and 80 m in depth, respectively. We
have no way of assessing the effect that these two
slightly-varying sampling protocols would have on relative concentration estimation, but recognize that changes in vertical distribution may interact with sampling to generate bias that may blur
the effects of the environmental signals that we detected. Of the
new samples collected, 33 were used with the winter, 35 with
the near-shore biweekly, and 161 with the coast-wide analyses.
An additional 15 samples collected in 1998–2009 from a station
2 km offshore along the NH transect were processed and incorporated into the winter analyses. This does not bias the winter analyses since the same six stations (2, 9, 18, 28, 37, and 46 km from
shore) were sampled during the same period (winter) during all
sampling years (1998–2011). The six samples collected on June
3–4, 2010 were analyzed as part of the May samples, since they
were collected at the end of a cruise that began in late May, and
correspond to the season prior to the transition from El Niño to
La Niña conditions in mid-June 2010 (Appendix).
Collection methods consisted of a 60-cm diameter bongo frame
with 333-lm mesh nets and an attached General Oceanics
flowmeter fished obliquely from either 20- or 100-m depth (or
within 5 m of the bottom at stations shallower than 100 m) to
the surface, depending on the sampling protocols outlined in
Table 1. Ichthyoplankton samples were generally preserved in a
10% buffered-formalin seawater solution at sea. However, most
samples collected in accordance with the coast-wide protocol were
preserved at sea in 95% ethanol for 72 h, then filtered and
re-preserved in fresh 95% ethanol. Preserved samples were taken
to the laboratory where all fish larvae from each sample were
sorted, enumerated, and identified to the lowest taxonomic level
possible using a dissecting microscope. Most larval osmerids
(smelts), Sebastes spp. (rockfishes), and Citharichthys spp. (sanddabs) collected were not identifiable to species based on meristics
and pigmentation patterns, so these taxa were analyzed at the
family or generic level. However, the majority of individuals classified as Citharichthys spp. are either C. sordidus (Pacific sanddab) or
C. stigmaeus (speckled sanddab) based on the larger, identifiable
individuals collected and dominance of these paralichthyid species
in the NCC ichthyoplankton (Matarese et al., 1989).
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T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
Fig. 1. Locations and designations (in approximate km from shore) of stations sampled along four transects in the northern California Current region as part of the three
comparative studies presented in the current study. Contour lines representing the 100-, 200-, 500-, 1000-, and 2000-m isobaths are shown. All stations except NH 2, 9, 18,
and 37 were sampled as part of the coast-wide study. Internal box represents stations sampled as part of the winter study. Only stations NH 9 and 18 were sampled as part of
the near-shore biweekly study.
Table 1
Summary of sampling protocols for the three ichthyoplankton studies used in the current comparative study.
Study
Period
Frequency Latitudinal Longitudinal
range
range
Depth
range (m)
Transects Stations Samples Gear type (mouth
(no.)
(no.)
(no.)
diameter/area and
mesh size)
Auth (2011)
[Coast-wide]
2004–09
(May–September)
Monthly
44.00–
46.67°N
124.22–125.36°W
0–100
4
Auth et al. (2011)
[Near-shore
biweekly]
1971–1972, 1978,
1983, 1998–2005
(February–September)
Biweekly– 44.65°N
monthly
124.18–124.29°W
Daly et al. (2013)
[Winter]
1998–2010
(January–March)
Biweekly
124.18–124.65°W
44.65°N
Surface chlorophyll-a concentrations (mg/m3) were measured
from bucket samples collected at the 9- and 18-km station along
the NH transect as part of the near-shore biweekly sampling.
From each station, a 100-ml aliquot of whole seawater was filtered
through a 25-mm Whatman GF/F filter. The filter was placed in a
15-ml centrifuge tube and frozen for later analysis. In the laboratory, frozen filters were submerged in 10 ml of 90% HPLC grade
acetone for 24 h before analysis on a Turner Model 10-AU fluorometer. The mean chlorophyll-a concentrations were averaged from
the two stations for subsequent analyses. Because these samples
were not always collected at the same exact intervals (e.g.,
20
434
60- and 70-cm bongo
and 1-m2 Tucker trawl
(June 2004) (335-lm)
1
Entire water
column (0–20
in 1996–2005)
2
275
60- and 70-cm bongo
and 1-m ring
(200–571 lm)
0–20
5
161
60-cm bongo and 1-m
ring (200- and 333-lm)
1
biweekly–monthly) or at both stations on a given cruise, mean
chlorophyll-a concentration from both stations during each cruise
were averaged for all cruises within each month. All statistical
analyses were based on these monthly-averaged data.
2.3. Data analyses
Larval fish concentrations for each sample were expressed as
the number of individuals per 1000 m3. Sample data were averaged
by cruise then by month. Analysis of variance (ANOVA) and Tukey’s
multiple range tests were applied to the loge(N + 0.1)-transformed
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T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
larval concentrations, which normalized the data and homogenized residual variances, to test for significant differences
(P < 0.05) among winter annual means of the monthly-averaged
data (N = 14). Too few annually-averaged data points (N 6 8) were
available to conduct ANOVAs on the aggregated near-shore
biweekly and coast-wide data. All ANOVAs were performed using
the statistical software JMP Version 7.0 (SAS Institute Inc., 2007).
Although the focus of the present study was on the larval community as a whole (i.e., total larvae), taxa examined individually in
the analyses were consistent with those examined in each of the
comparative studies and corresponded to the dominant taxa found
in each study. For the winter study, the following taxa were examined: Ammodytes hexapterus (Pacific sand lance), Citharichthys spp.,
Isopsetta isolepis (butter sole), Osmeridae, Parophrys vetulus
(English sole), Psettichthys melanostictus (sand sole), Sebastes spp.,
and Stenobrachius leucopsarus (northern lampfish). For the
near-shore biweekly study, these same taxa were examined in
addition to Engraulis mordax (northern anchovy). For the
coast-wide study, the following taxa were examined: E. mordax,
Lyopsetta exilis (slender sole), Sebastes spp., S. leucopsarus, and
Tarletonbeania crenularis (blue lanternfish).
We used principal coordinates analysis (PCO), an ordination
technique similar to principal components analysis, but more flexible in that it allows the use of resemblance measures other than
Euclidean distance to examine structure of sample units (years)
in taxon space (Legendre and Legendre, 1998). In order to reduce
the distorting effects on the analyses of very large catches of any
taxon, mean concentrations of the most abundant taxa for each
sampling program were fourth-root transformed. Distances among
years in taxon space were measured using the Sørensen (Bray–
Curtis) distance measure (McCune et al., 2002). A single ordination
was performed on the years (based on annual averages of the
monthly means) by taxon matrix for the winter larvae from
January to March. For the coast-wide larvae, the years were further
divided into spring (May) and summer (based on seasonal averages
of the monthly means from June to September) to examine seasonal changes in community composition. Based on the decrease
in variation accounted for with the addition of each ordination
axis, a two-dimensional solution was most effective for explaining
variation in the original multidimensional taxon space. The software PERMANOVA + for PRIMER (Anderson et al., 2008) was used
for all ordination analyses.
In order to describe the environmental gradients associated
with the PCO ordination axes, three monthly-averaged
basin-scale variables (i.e., MEI, NOI, and PDO), four
monthly-averaged regional variables (i.e., UPW, EET, NET, COL),
and the chlorophyll-a concentration measurements (CHL) made
with the different near-shore biweekly hauls were correlated with
the ordination scores along each axis (Table 2). These variables
were chosen based on their accessibility and relevance as outlined
in previous ichthyoplankton studies in the region (e.g., Auth, 2011;
Auth et al., 2011). For the winter larval analysis, we used
seasonally-averaged values of the monthly means of each variable
lagged to the three months prior to collection (October–December
of previous year). For the coast-wide analysis, we used these same
months for the spring larvae but used the following three months
(January–March) for the summer larvae. These lags correspond to
the mean period influencing spawning conditions and early larval
development for the taxa of concern (Auth, 2011; Auth et al., 2011;
Daly et al., 2013). Since the environmental variables have substantially different units, we used Z-score standardized values for
the analysis, which relativized them to a mean of zero and a
variance of one and is recommended for environmental variables
(McCune et al., 2002). However, correlation analyses among these
variables revealed that MEI was highly correlated (Pearson
R > ±0.75) with NOI and PDO and was subsequently dropped from
Table 2
Abbreviations, descriptions, and sources of the environmental variables used in this
study. All websites were last accessed in December 2012.
Abbreviation Description and source
MEI
NOI
PDO
UPW
EET
NET
COL
CHL
Multivariate El Niño-Southern Oscillation Index. From the
National Oceanic and Atmospheric Administration (NOAA)
Earth System Research Laboratory website: http://www.cdc.
noaa.gov/ENSO/enso.mei_index.html
Northern Oscillation Index. From the NOAA Environmental
Research Division website: http://www.pfeg.noaa.gov/
products/PFEL/modeled/indices/NOIx/noix.html
Pacific Decadal Oscillation. From the University of Washington
(Nathan Mantua administrator) website: http://jisao.
washington.edu/pdo
Upwelling Index for 45°N, 125°W. From the NOAA Southwest
Fisheries Science Center Environmental Research Division live
access server website: http://www.pfeg.noaa.gov/products/las.
html
Eastward Ekman transport (kg/m) from a 1° 1° square area
centered at 44.5°N, 124.5°W. From the NOAA Southwest
Fisheries Science Center Environmental Research Division live
access server website: http://www.pfeg.noaa.gov/products/las.
html
North–south Ekman transport (kg/m) from a 1° 1° square area
centered at 44.5°N, 124.5°W. From the NOAA Southwest
Fisheries Science Center Environmental Research Division live
access server website: http://www.pfeg.noaa.gov/products/las.
html
Columbia River outflow (1000 ft3/s) measured at Bonneville
Dam located 235 km upriver from the mouth of the Columbia
River. From the U.S. Army Corps of Engineers, NWD, Grant
County PUD, and Oregon Department of Fish and Wildlife
website: http://www.cbr.washington.edu/dart/river.html
Mean surface chlorophyll-a concentration (mg/m3) measured
biweekly–monthly from two stations located 9 and 18 km west
of Newport, Oregon
this analysis. Relationships between the environmental variables
and ordination scores (R > ±0.30) were shown as vectors overlaid
on the ordination plots. The coefficient of determination (R2)
among distances in the ordination space and distances in the
original space was used to determine the proportion of variation
represented by each axis. We classified the winter larvae into
two groups, warm and cool years, based on PDO variations from
the preceding 3 months (October–December), where positive
PDO = warm, negative PDO = cool (see Brodeur et al., 2008; Auth
et al., 2011; Daly et al., 2013). The groupings were used to test
for differences in community structure using an analysis of similarities procedure (ANOSIM), which tests the null hypothesis of no
difference between groups. This analysis gauges within- and
between-group differences using a Global R statistic that ranges
between 0 and 1, with 0 being no agreement within a group and
1 being complete agreement, based on 1000 random permutations
(Clarke and Warwick, 2001). Taxa that contributed the most to the
between-group differences were identified using post hoc similarity percentages (SIMPER) analyses (Clarke and Gorley, 2006).
We used multivariate regression trees (MRTs), a multivariate
analog to classification and regression trees (De’Ath, 2002;
Ruppert et al., 2010) to explore the relative importance of the
large-scale and local environmental variables (i.e., all of the same
variables that were used in the previously-outlined analyses) that
contributed to the community structure of the dominant larval
species for the winter and near-shore biweekly data. This method
relies on very few statistical assumptions and allows for collinearity of the explanatory independent variables (De’Ath, 2002). The
MRT analysis first classifies the taxa hierarchically into different
clusters (leaves) corresponding to the assemblages observed at
the nodes of each tree. The tree is then ‘pruned’ based on the overall fit expressed as the relative error (RE). The optimum size of the
tree is arrived at by minimizing the cross-validated relative error
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T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
(CVRE), which in effect maximizes the variability between leaves.
As suggested by Breiman et al. (1984), the selection of the final tree
was made using the one standard error (1 SE) rule. The MRT analyses were run using the mvpart package in R (De’Ath, 2007).
3. Results
3.2. Larval concentrations and assemblages
3.1. Environmental factors
A total of 9,189 fish larvae were collected in 2010–2011 that
were included in the analyses with the comparative studies: winter
(N = 1879), near-shore biweekly (N = 799), and coast-wide
(N = 7185). The difference between the total larval count and the
sum of the individual study counts (N = 674) is due to several samples (N = 7) that were used in multiple comparative study analyses.
The dominant taxa were the same as those found in each of the
three comparative studies. An additional 2088 larvae were included
in the winter analyses from the additional 15 samples collected in
1998–2009 at the station 2 km offshore along the NH transect.
3.2.1. Winter study
Total mean larvae concentration was higher in 2010 than in any
other year in the study (Fig. 4). Total larval concentration in the
warm year 2010 was significantly higher than in any other warm
year (ANOVA P < 0.05) but not significantly different than in any
150
2
4
100
1
2
0
-1
-2
-2
-4
-3
-6
3
150
2
100
1
0
-1
-2
-900
1970
NET anomaly
6
-50
2
0
-100
-2
-150
-4
1970
600
-600
-150
0
600
-300
-50
4
900
0
0
-100
50
900
300
50
CHL anomaly
0
COL anomaly
6
NOI
3
UPW anomaly
PDO
MEI
Basin-scale and regional environmental indices and variables
varied seasonally, annually, and decadally in 1970–2011 throughout the study area (Fig. 2). During this period, the NCC experienced
fluctuating cool and warm periods, marked by warm, strong El
Niño events in 1972–1973, 1983, 1987, 1992, and 1997–1998.
Weak El Niño conditions were prevalent during 2004, while 2005
was marked by highly anomalous late upwelling (mid-July) unrelated to the ENSO (Schwing et al., 2006) followed by a sudden negative shift in the MEI that persisted through mid-2006. La Niña
conditions were prevalent during most of 2007 and 2008, followed
by a switch to El Niño conditions in mid-2009 that persisted until
the sudden switch to La Niña conditions in mid-June 2010 that is
the focus of this study. This transition can also be seen in the
monthly variability of many of the basin-scale and regional environmental factors plotted from October 2009 through September
EET anomaly
2010 (Fig. 3). For the sampling periods in this study, 1971–1972
were relatively cool years, 1977–1978 warm, 1983 warm, 1996–
1998 warm, 1999–2002 cool, 2003–2005 warm, 2006 cool, 2007
warm, 2008–2009 cool, late 2009-mid 2010 warm, and late
2010–2011 cool.
1980
1990
2000
2010
Year
300
0
-300
-600
1980
1990
2000
-900
1970
2010
1980
1990
2000
2010
Year
Fig. 2. Time-series of 13 4-month (February–May, June–September, October–January) averaged environmental indices/variables used in this study from 1970 to 2011:
Multivariate El Niño-Southern Oscillation Index (MEI), Northern Oscillation Index (NOI), Pacific Decadal Oscillation (PDO), and Upwelling Index (UPW) anomaly, eastward
Ekman transport (EET, kg/m) anomaly and north–south Ekman transport (NET, kg/m) anomaly each for 45°N, 125°W, Columbia River outflow (COL, 1000 ft3/s) anomaly
measured at Bonneville Dam located 235 km upriver from the mouth of the Columbia River, and mean surface chlorophyll-a concentration (CHL, mg/m3) anomaly measured
from two stations located 9 and 18 km west of Newport, Oregon. Anomalies for CHL are based on monthly averages in 1997–2011, while anomalies for all other variables are
based on monthly averages in 1970–2011. Dotted lines depict 5-year intervals.
T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
6
1
3
0
0
NOI
2
-1
-3
-2
-6
-3
1
-9
0
PDO
MEI
108
-1
-2
200
100
UPW anomaly
UPW
100
0
-100
-200
-300
3000
-100
-200
-300
1400
EET anomaly
2000
EET
0
1000
0
700
0
-700
600
0
400
NET anomaly
-1000
200
NET
-200
-400
-600
200
0
-200
-400
-600
60
COL anomaly
-800
-1000
400
COL
300
200
100
0
10 11 12 1
2
3
4
5
6
7
8
30
0
-30
-60
-90
9
10 11 12 1
2
Month
12
CHL
4
5
6
7
8
9
5
6
7
8
9
12
CHL anomaly
16
8
4
0
3
Month
10 11 12 1
2
3
4
Month
5
6
7
8
9
8
4
0
-4
10 11 12 1
2
3
4
Month
Fig. 3. Monthly averaged (October 2009 through September 2010) time series of Multivariate El Niño-Southern Oscillation Index (MEI), Northern Oscillation Index (NOI),
Pacific Decadal Oscillation (PDO), and Upwelling Index (UPW), UPW anomaly, eastward Ekman transport (EET, kg/m), EET anomaly, north–south Ekman transport (NET, kg/
m), and NET anomaly each for 45°N, 125°W, Columbia River outflow (COL, 1000 ft3/s) and COL anomaly each measured at Bonneville Dam located 235 km upriver from the
mouth of the Columbia River, and mean surface chlorophyll-a concentration (CHL, mg/m3) and CHL anomaly measured from two stations located 9 and 18 km west of
Newport, Oregon. Anomalies for CHL are based on monthly averages in 1997–2011, while anomalies for all other variables are based on monthly averages in 1970–2011.
Dotted line depicts the delineation between El Niño (left) and La Niña (right) periods.
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T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
1800
Other
Psettichthys melanostictus
Citharichthys spp.
Stenobrachius leucopsarus
Isopsetta isolepis
Osmeridae
Sebastes spp.
Ammodytes hexapterus
Parophrys vetulus
1600
Mean concentration (no./1000 m3)
1400
1200
a
ab
1000
ab
ab
b
800
ab
600
ab
ab
b
400
b
ab
b
ab
200
b
0
1998W
1999C
2000C
2001C
2002C
2003W 2004W 2005W
2006C
2007W
2008C
2009C
2010W
2011C
Year
Fig. 4. Annual mean concentrations of the dominant larval fish taxa and all others collected from stations 2 to 46 km offshore along the Newport Hydrographic (NH) line
during winter (January–March) in 1998–2011. Annual regimes (C: cool; W: warm) are indicated along the x-axis. For annual comparisons of total larval concentration among
years, different letters above the bars indicate significant differences (ANOVA P < 0.05).
of the cool years (ANOVA P > 0.05; Fig. 4). Of the dominant taxa
examined, five out of eight (i.e., Citharichthys spp., I. isolepis,
Osmeridae, P. melanostictus, and S. leucopsarus) were found in
higher concentrations in 2010 than in any other year. Several other
larval taxa that are normally found in the offshore (46–84 km) or
far-offshore (>100 km) regions were collected as close as 18 km
from shore in 2010 and in higher concentrations than in any other
year in the study: Anoplopoma fimbria (sablefish), Glyptocephalus
zachirus (rex sole), Lestidiops ringens (slender barracudina),
Microstomus pacificus (Dover sole), Sebastolobus spp. (thornyhead),
and T. crenularis. In fact, T. crenularis larvae were only collected
once before in the study, at the station 9 km from shore in 1998:
a strong El Niño year. The larval community did not differ between
warm and cool years as a whole (ANOSIM Global R = 0.04; P = 0.47),
although the larval community in the winter of 2010 was significantly different from the other warm and cool years (ANOSIM;
P = 0.03 and P = 0.03, respectively). SIMPER analyses suggested that
these differences were due to higher concentrations of I. isolepis
and Osmeridae in 2010 compared to the other years.
3.2.2. Near-shore biweekly study
Total mean larval concentrations in 2010 were higher in the
winter/spring (February–May) and as low as or lower in the summer/fall (June–September) than those found in the same seasons in
any other sampling period in the study (Fig. 5). Of the dominant
taxa examined, six out of nine (i.e., Citharichthys spp., I. isolepis,
Osmeridae, P. vetulus, P. melanostictus, and Sebastes spp.) were
found in higher concentrations in the winter/spring in 2010 than
in the same season in any of the other sampling periods.
3.2.3. Coast-wide study
Total mean larval concentration was more than twice as high in
May 2010 than in the same month in any other year in the study
(Fig. 6). Of the dominant taxa examined, four out of five (i.e., E.
mordax, L. exilis, Sebastes spp., and T. crenularis) were found in
higher concentrations in May 2010 than in the same month in
any other year. Several species were collected in May 2010 that
were not found in May of the other sampling years: A. fimbria,
Pleuronichthys decurrens (curlfin sole), Protomyctophum crockeri
(California flashlightfish), P. thompsoni (bigeye lanternfish),
Sardinops sagax (Pacific sardine), and Scorpaenichthys marmoratus
(cabezon). In addition, several other common taxa were found in
higher concentrations in May 2010 than in May of any of the other
years in the study: Citharichthys spp., Icichthys lockingtoni (medusafish), Liparis fucensis (slipskin snailfish), Nannobrachium regale (pinpoint lampfish), P. melanostictus, Radulinus asprellus (slim sculpin),
and Sebastolobus spp. By contrast, total mean larval concentration
in June–September 2010 was as low as or lower than that found
in the same months in any other year in the study except for in
2006, which experienced abnormally low larval production due
to the disruptively late upwelling in 2005 (Auth, 2008).
Significant differences in community composition were found
between the spring (May) and summer (June–September) seasons
(ANOSIM Global R = 0.80; P = 0.02), with the 2010 spring samples
being significantly different from the other spring (P = 0.01) and
all summer samples (P = 0.01). The offshore taxa G. zachirus, L. exilis, and S. leucopsarus were significant indicator species for spring
and E. mordax was an indicator species for summer (SIMPER).
Sebastes spp. was the taxon that distinguished spring 2010 from
all other spring and summer collections.
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1500
A
Mean concentration (no./1000 m3)
1250
1000
Other
Engraulis mordax
Psettichthys melanostictus
Citharichthys spp.
Stenobrachius leucopsarus
Isopsetta isolepis
Osmeridae
Sebastes spp.
Ammodytes hexapterus
Parophrys vetulus
750
500
250
0
1971-1972
1978
1983
1998
1999-2002
2003-2005
2010
Year
250
B
Mean concentration (no./1000 m3)
200
150
100
50
0
1971-1972
1978
1983
1998
1999-2002
2003-2005
2010
Year
Fig. 5. Seasonal mean concentrations of the dominant larval fish taxa and all others collected from stations 9 and 18 km offshore along the Newport Hydrographic line as part
of the near-shore biweekly study during (A) winter/spring (February–May) and (B) summer/fall (June–September) in 1971–72 (Richardson and Pearcy, 1977), 1978 (9 km
station only) (Laroche et al., 1982), 1983 (Brodeur et al., 1985), and 1998, 1999–2002, 2003–2005 (Brodeur et al., 2008), and 2010 (current study). Note that the y-axis for
winter/spring is greater than that for summer/fall by a factor of six.
3.3. Environmental-taxa relationships
The first two principal coordinate axes of the winter larval data
accounted for 63.7% of the variation and showed that 2010 was an
anomalous year compared to the others included in the analysis, as
evidenced by the 2010 data point being separated from all of the
other years in ordination space (most negative loading on PCO axis
1; Fig. 7). There were no clear patterns associated with the warm
vs. cool years as determined by the PDO (Fig. 7). A similar analysis
performed on the coast-wide data revealed the presence of spring
(May) and summer (June–September) clusters which separated
mainly along PCO axis 1 (58.4% of the variation explained), with
the spring 2010 larvae again standing out as an anomaly due to
its extreme negative loading with PCO axes 2 (21.2% of the
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T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
800
A
Other
Tarletonbeania crenularis
Stenobrachius leucopsarus
700
Sebastes spp.
Mean concentration (no./1000 m3)
Lyopsetta exilis
600
Engraulis mordax
500
400
300
200
100
*
0
2004
*
2005
2006
2007
2008
2009
2010
2011
Year
450
B
400
Mean concentration (no./1000 m3)
350
300
250
200
150
100
50
0
2004
2005
2006
2007
2008
2009
2010
2011
Year
Fig. 6. Mean concentrations of the dominant larval fish taxa and all others collected as part of the coast-wide study in 2004–2011 during (A) May from stations 28 to 84 km
offshore along the Newport Hydrographic (NH) line and 21–69 km offshore along the Heceta Head (HH) line, and during (B) June–September from stations 18–102 km
offshore along the Willapa Bay, Columbia River, NH, and HH lines. Note that the y-axis for May is greater than that for June–September by a factor of two. ⁄ = no samples
collected.
variation; Fig. 8). It is interesting that the summer larval fish community in 2010 was rather typical and did not stand out from several of the other years, although 2006 did. Several lagged
environmental variables appear to be related to the 2010 anomalies. For the winter data, CHL was negatively related and
3-month lagged NET and COL were positively related to PCO axis
1, but no variables exceeded the correlation threshold with PCO
axis 2 (Fig. 7 and Table 3). For the coast-wide data,
seasonally-lagged NET and COL were negatively related to PCO axis
1, whereas EET, NET and PDO were positively related and CHL was
negatively related to PCO axis 2 (Fig. 8 and Table 3).
The species scores for the winter data showed that Osmeridae
and Citharichthys spp. were positively related to PCO axis 1, and
P. melanostictus, I. isolepis, and S. leucopsarus were negatively
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T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
Fig. 7. Ordination plots resulting from the principal coordinate (PCO) analysis of winter (January–March) fish larvae collected off the central Oregon coast in 1998–2011.
Inverted triangles represent cool years; standard triangles represent warm years. Relationships between environmental variables and ordination scores (R > 0.30) are shown
as vectors. CHL = mean surface chlorophyll-a concentration (mg/m3); COL = Columbia River outflow (1000 ft3/s); NET = north–south Ekman transport (kg/m). Abbreviated
names of important larval taxa are also shown.
Fig. 8. Ordination plot resulting from the principal coordinate (PCO) analysis of fish larvae collected off the Oregon and Washington coasts in 2004–2011 as part of the coastwide study. Triangles represent spring (May); Circles represent summer (June–September) samples. No spring samples were collected in 2004 and 2005. Relationships
between environmental variables and ordination scores (R > 0.30) are shown as vectors. CHL = mean surface chlorophyll-a concentration (mg/m3); COL = Columbia River
outflow (1000 ft3/s); NET = north–south Ekman transport (kg/m); EET = eastward Ekman transport (kg/m); PDO = Pacific Decadal Oscillation. Abbreviated names of important
larval taxa are also shown.
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Table 3
Pearson correlation coefficients of the first two principal coordinate axes (PCO1 and PCO2) with the environmental indices (above dotted line) and taxa data (below dotted line)
for the winter and coast-wide studies. Correlations exceeding ± 0.3 for environmental variables and ± 0.6 for taxa are in bold.
*
Taxon not analyzed for that study.
PDO ≥ - 1.24
UPW ≥ - 59
EET ≥ 784.7
PDO < - 1.24
UPW < - 59
EET < 784.7
Paro_vetu
Ammo_hexa
Sebastes
Osmerid
Isop_isol
Sten_leuc
Citharicht
Pset_mela
CV Error = 1.64 SE = 0.33
Fig. 9. Pruned multivariate regression tree for the winter (January–March) fish larvae collected off the central Oregon coast in 1998–2011. The data at the nodes of the trees
represent the lagged environmental factors most contributing to the separation of the branches (PDO = Pacific Decadal Oscillation; UPW = Upwelling Index; EET = eastward
Ekman transport [kg/m]). The histograms below each branch constitute the community composition of the dominant larval fish taxa resulting after each split. CV = coefficient
of variation; SE = one standard error.
associated with this axis (Table 3). For the coast-wide analysis, L.
exilis and S. leucopsarus had nearly identical negative loadings on
PCO axis 1, and Sebastes spp. had a negative relationship to PCO
axis 2 (Table 3).
Only three and two of the eight environmental variables were
useful indicators of branch separation for the MRT analysis of the
winter ichthyoplankton and summer coast-wide larval community
composition, respectively (Figs. 9 and 10). For the winter
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EET ≥ 597.2
MEI ≥ - 0.77
EET < 597.2
MEI < - 0.77
CV Error = 2.94 SE = 0.59
Engr_mord
Sebastes
Sten_leuc
Tarl_cren
Lyop_exil
Nano_rega
Citharicht
Lipa_fuce
Fig. 10. Pruned multivariate regression tree for the fish larvae collected off the Oregon and Washington coasts in 2004–2011 as part of the coast-wide study. The data at the
nodes of the trees represent the lagged environmental factors most contributing to the separation of the branches (EET = eastward Ekman transport [kg/m],
MEI = Multivariate El Niño-Southern Oscillation Index). The histograms below each branch constitute the community composition of the dominant larval fish taxa resulting
after each split. CV = coefficient of variation; SE = one standard error.
ichthyoplankton, the PDO split off the first branch with a community composition dominated by A. hexapterus (Fig. 9). Additional
splits occurred due to UPW (dominated by P. vetulus and
Osmeridae) and finally EET (P. vetulus and Sebastes spp.). For the
summer coast-wide larvae, the MRT analysis determined that EET
contributed to
the first split and MEI was related to the second split, although the
community composition did not differ substantially among the different branches (Fig. 10). Finally, no environmental variables were
found to be significant for the spring coast-wide larvae, perhaps
due to the low sample size (N = 6) used in the analysis.
4. Discussion
The evidence presented in this study strongly suggests that
2010 was a year marked by anomalously high larval fish concentrations in the NCC during the winter and spring followed by a
sudden transition to relatively, if not abnormally, low concentrations during the summer and fall corresponding to the transition
from El Niño to La Niña conditions in June 2010. As noted by
Jacox et al. (2015), the Oceanic Niño Index (ONI) was tied for
the third highest in 2009–2010 compared to ten other El Niño
periods since 1982, and was the second lowest compared to the
same ten periods for the later La Niña component. The high concentration of larvae in the winter of 2010 was likely the direct
result of El Niño and warm-ocean conditions (i.e., high values of
the MEI, NOI, and PDO) along with strong downwelling (i.e., negative UPW anomaly) and onshore transport that allowed more
normally-offshore taxa to be present on the shelf along with
the shelf species, resulting in higher overall abundance. This
annual anomaly in seasonal (i.e., winter/spring vs. summer/fall)
concentrations was consistently demonstrated through three
comparative studies, each with different latitudinal and/or
cross-shelf coverage. In addition, Roegner et al. (2013) conducted
a study that sampled the surface ichthyoplankton in the
near-shore region of the Columbia River plume in June 9–15,
2010 (a period encompassing the El Niño to La Niña transition)
and also found that larval fish and decapod concentrations
decreased during the period immediately after the transition to
upwelling conditions, likely due to offshore advection beyond
the sampling grid.
The findings in the present study that seasonal larval concentrations and distributions in 2011 were similar to those
found in the years prior to 2010, even though negative ENSO
conditions persisted from June 2010 through 2011, suggests
that the observations in the ichthyoplankton community associated with the transition from El Niño to La Niña conditions in
2010 were a temporary event, rather than marking the onset
of a regime shift, and possibly a result of environmental conditions occurring in or immediately before 2010. Doyle (1995)
argued that the assemblage of larval fishes in the NCC showed
a high degree of stability in that it returned to a typical community structure just one year after the anomalously strong
1983 El Niño event.
Auth (2009) conducted a study of the cross-shelf distribution
and concentration of ichthyoplankton from stations extending
2–364 km offshore at 7–53 km intervals along two latitudinal transects (NH and Crescent City, California [41.90°N]) during March,
April, and October 2007, and March, June, and July 2008 that examined variability between the coastal-shelf (<2000-m depth) and
far-offshore (>2000-m depth) regions. In a preliminary analysis
of unpublished data from samples collected at similar cross-shelf
T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
stations in March, May, and August 2010, we found that during the
El Niño, E. mordax and Sebastes spp. larvae were distributed closer
to shore than had previously been observed during any month in
the Auth (2009) study, but shifted offshore following the transition
to La Niña conditions in 2010. In contrast, larval distributions of
the myctophids S. leucopsarus and T. crenularis did not change with
the environmental shift. This is not surprising, as E. mordax and
Sebastes spp. larvae are found primarily near the surface while
myctophid larvae are found deeper in the water column (Auth
et al., 2007) where they are less susceptible to wind-driven
cross-shelf advection. A similar phenomenon was described for
the same taxa in previous studies conducted in the NCC (Auth,
2008, 2011). Brodeur et al. (1985) and Yoklavich et al. (1996) also
found similar onshore movements of E. mordax and Sebastes spp.,
respectively, during strong El Niño events in the California
Current. In addition, two species that are normally found in the
far-offshore region, Embassichthys bathybius (deepsea sole) and I.
lockingtoni, were recorded in the highest concentrations in the
Auth (2009) and unpublished data at coastal-shelf stations in
spring 2010, while two normally southern species, Merluccius productus (Pacific hake) and S. sagax, were recorded in the highest concentrations in the same two data sets as far north as the NH
transect. Latitudinal changes in species distributions can also be
affected by whether the species remains in the mesopelagic zone
or if it undertakes vertical migration into the surface zone (Hsieh
et al., 2009).
Previous studies conducted in the California Current region
comparing ichthyoplankton communities between ENSO periods
reported latitudinal and cross-shelf changes in assemblage structure. Funes-Rodríguez et al. (2011) found that the abundance and
diversity of tropical species increased during the 1997–1998 El
Niño off the coast of the Baja California Peninsula (25–31°N), while
the number and abundance of temperate species increased during
the 1998–2000 La Niña. Thompson et al. (2012) reported that the
ichthyoplankton community in the Cowcod Conservation Area
(CCA) off the southern coast of California (32.4–33.8°N, 119.9–
118.8°W) was dominated by coastal-oceanic species during the
2002 La Niña period, but that more oceanic species dominated
the community during the following 2004 El Niño. Similarly,
Brodeur et al. (1985) documented a northward and coastal shift
in the larval fish assemblage during the 1983 El Niño along the
near-shore (2–18 km offshore) region of the NH transect off the
coast of Oregon compared to the larval assemblage observed in
the same region and season during more normal conditions.
Doyle (1995) also described a shoreward displacement of the oceanic community off Oregon and Washington and more near-shore
retention of the coastal and slope-transitional assemblages compared to the years bracketing the 1983 El Niño. However, the present study is the first to document not only the northward changes
in the ichthyoplankton community associated with an El Niño
event, but also the dramatic increase in resident larval concentrations during the El Niño followed by a subsequent, though less dramatic, decrease immediately following the transition to La Niña
conditions, compared to similar seasons in previous annual
periods.
As shown in these previous studies, not all species are
expected to show similar responses to ENSO events due in part
to their divergent life-history strategies (e.g., timing of spawning,
ovipary vs. vivipary, pelagic vs. demersal eggs) and choice of
spawning areas (e.g., near-shore retention zones or the relatively
stable Columbia River plume vs. upwelling cells, near-surface vs.
deep-water). Some taxa (such as Sebastes spp.) appear to be
favored by the conditions occurring during the El Niño of 2010
115
leading to high larval and juvenile abundance that year
(Brodeur et al., 2011; Roegner et al., 2013), although it is uncertain whether these abundant early-life stages will ultimately lead
to higher recruitment and adult abundances. Further complicating
the situation, not all El Niño events are similar in terms of their
timing, duration, or strength so their effects on fish can be equally
variable. The El Niño events appear to have evolved over the last
few decades into at least two modes: a canonical Eastern Pacific
(EP) and a Central Pacific (CP or Modaki) type, with different
physical manifestations (Ashok and Yamagata, 2009; Weng
et al., 2009; Di Lorenzo et al., 2013). Indeed, whereas many of
the stronger events up to 1999 were classified as the EP mode,
the more recent events, including the relatively strong 2010
event, were classified as CP events (McPhaden et al., 2011).
Based on model projections of ocean warming, the frequency of
both CP and EP mode El Niños (Yeh et al., 2009) and extreme
events (Cai et al., 2014) are likely to increase due to increased
build-up of greenhouse gases. Thus, the effects of events that
have occurred in the past may not be indicative of future effects
as climate change intensifies.
Although the MEI index was not included as a variable in the
PCO analysis (due to high correlations with some other variables
– see methods), the more seasonally-driven upwelling, Ekman
transport, chlorophyll-a, and Columbia River dynamics were
important. However, the MEI did appear as a significant variable
in the MRT results for the coast-wide larvae, albeit of less importance than EET. Our limited ability to find effects of lagged environmental
variables/indices
on
spawning
and
larval
concentrations/distributions in our study may be due to the differences in the frequency of our observations (weekly to monthly)
and the temporal scales of the relevant processes. Although PDO
shifts and ENSO processes can extend over several months and
even years, upwelling and production cycles can occur on finer
scales that we have not captured in our basin-wide environmental indices. In examining the effects of environmental variability
on ichthyoplankton assemblages in the southern California
Current region during a transition from La Niña to El Niño conditions in 2002–2004, Thompson et al. (2012) found that environmental variables explained relatively little of the variation in
the ichthyoplankton community in the smaller sampling area
(11,138 km2) of the Cowcod Conservation Area (CCA), but better
explained the variability in ichthyoplankton distributions in the
larger CalCOFI sampling area (238,000 km2; 30–35°N, 117–
124°W) encompassing the CCA. Thompson et al. (2014), however,
found local environmental variables such as upwelling and
Columbia River flow may have a greater effect on ichthyoplankton assemblages off Oregon compared to Southern California,
but these can be strongly modulated by ENSO conditions. In addition, smaller-scale distribution patterns such as those related to
frontal regions (Bjorkstedt et al., 2002) may not have been
detected due to the station spacing along the transects we
sampled.
Environmental factors may influence spawning and larval survival in different ways. Auth (2011) found that correlations between
in situ environmental variables and larval concentrations differed
from environmental variables that were compared with 2–4 month
lagged larval concentrations and diversity. For example, he found
that larval concentrations were generally positively correlated with
in situ sea-surface temperature (SST), while negatively correlated
when lagged 2–4 months behind SST. The same study also suggested that 0–2 month lagged larval concentrations were positively
correlated with Columbia River outflow (COL), while those lagged
3–5 months were negatively correlated with COL. In the present
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T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
study, COL anomaly was highly negative during the winter-spring
when larval concentrations were high and only slightly negative
during the summer when concentrations were low.
In addition to changes in larval concentrations and distributions
in space, anomalous conditions associated with strong perturbations like El Niños can affect the timing of fish spawning, thereby
changing the phenology of larval occurrence. Increases in temperature can lead to earlier spawning (Greve et al., 2005; Asch, 2013),
which will influence community composition in surveys that are
fixed in time from year-to-year. For example, in the NCC Brodeur
et al. (1985) found that E. mordax spawned several months earlier
than previously documented in normal years (e.g., Richardson and
Pearcy, 1977) due to the warm and relatively stable conditions
experienced during the strong 1983 El Niño. Also, Kruse and
Tyler (1989) suggested that timing of spawning for P. vetulus in
the NCC is generally adaptive, and is at least in part initiated by
an increase in temperature along the shelf that coincides with periods of favorable onshore transport of larvae and possibly their
major prey, Oikopleura spp. This, coupled with potential increased
growth rates in warmer conditions, may allow the larvae to grow
sufficiently to evade normal plankton samplers by late summer.
However, the delayed upwelling and overall lower food availability
occurring during anomalous years may lead to a mismatch of
first-feeding larvae and the production cycle (Cushing, 1990;
Platt et al., 2003) and also depress the overall larval growth rate
despite the earlier hatching (Takahashi et al., 2012).
Changes in the sign and magnitude of environmental variables
such as MEI and PDO occurred at the transition from El Niño to La
Niña conditions in June 2010. Hooff and Peterson (2006) found that
copepod biomass and diversity in the NCC are strongly correlated
with both the MEI and PDO. Although the present study did not
focus on predator–prey or competitive interactions, availability
and timing of suitable prey and proper environmental conditions
are known to be critical factors influencing larval survival (Hjort,
1914; Cushing, 1972, 1990; Lasker, 1978; Houde, 1996). During
the 2010 summer (La Niña) period of this study, an anomalously
large number of salps and ctenophores were caught in the plankton
and accompanying midwater trawl samples (Brodeur, unpublished
data). The prevalence of these organisms may have contributed to
the reduction in larval fish concentrations after the transition due
to predation and/or competition for prey resources, or may have
been symptomatic of unfavorable environmental conditions that
were not adequately measured in our study. Auth and Brodeur
(2006) had found digested fish larvae in the gastric cavity of both
these gelatinous predators along the NH line. In a recent modeling
study, Francis et al. (2012) showed that changing ocean conditions,
including ENSO conditions, can modify the food web interactions in
the NCC, and found that gelatinous zooplankton play a pivotal role
in the food webs in some years.
From the perspective of the prey field for larval fish, the copepod community had an anomalously high number (richness) of
species throughout 2010 (Peterson et al., 2014). The high
species-richness reflects the presence of more southern,
sub-tropical waters and their associated plankton persisting in
the study area and is indicative of more transport of water from
the south and west (Keister et al., 2011), as was indexed by eastward Ekman transport (EET) and north–south Ekman transport
(NET; Fig. 3). In fact, the negative upwelling (UPW) anomaly in late
2009 through early 2010 was the largest ever recorded in the
region in at least the last 40 years, resulting in a positive EET
anomaly during the same period, and a highly negative NET in
November 2009 (Figs. 2 and 3). Bograd et al. (2009) showed that
the onset of upwelling is often delayed and the duration of the
upwelling season is anomalously short during El Niños. Auth
(2011) found that 2–4 month lagged larval concentrations were
positively correlated with EET and negatively correlated with
UPW and NET. The increased transport of zooplankton prey from
the south and west associated with these currents could explain
both the anomalously high concentrations of fish larvae found in
the NCC during winter–spring 2010 and also offer a mechanism
for the correlations reported in Auth (2011). Fisher et al.
(submitted for publication) found that warm water copepod biomass was relatively high after the 2010 event, but lagged the initiation of the MEI signature by 6 months. The dramatic shift in the
PDO during this event from negative to positive resulted in a concurrent high biomass of cold water copepods which was unique in
the time series (Fisher et al., submitted for publication).
The level of surface chlorophyll-a (CHL) was quite high in late
2009 and summer 2010 (Figs. 2 and 3), relative to the 15-yr data
set, but in general is only weakly correlated with the abundance of
ichthyoplankton over the time series. Phytoplankton are an important component of the ichthyoplankton food chain, but they are
highly patchy in both time and space, and are only a portion of the
microplankton community, especially in winter months when sunlight is limited. The CHL values are likely a further indication of
water-mass transport, but without species information or availability of broad-scale distribution data (remote sensing data are lacking
due to wintertime cloud cover) this remains only speculative.
The anomalous ichthyoplankton concentrations, distributions,
and community structure observed in this study may have
occurred far more times in the past than have been documented
in previous studies, and are likely to become more prevalent as
ocean conditions change in the California Current (Hsieh et al.,
2009; King et al., 2011; McClatchie, 2013). Because environmental
shifts such as those which occurred during the 2010 El Niño to La
Niña transition are commonplace in the NCC region and can lead to
highly variable within-year larval production and survival
(McClatchie, 2013), more attention needs to be given to maintaining consistent sampling regimes across a comprehensive range of
temporal and spatial scales if fisheries scientists and managers
are to truly understand the connectivity among the environment,
larval community, and recruitment of ecologically and commercially important fish stocks in upwelling systems such as the
California Current.
Acknowledgements
We thank the captains, crews, and participating scientists of the
many ships employed to collect the data used in this study. We
also appreciate the assistance of A. Stephens with R programming.
We thank M. Litz, W. Pearcy, and three anonymous reviewers for
critical reviews of the manuscript. Funding was provided by
NOAA’s Stock Assessment Improvement Program (SAIP), Fisheries
and the Environment Initiative (FATE), and Northeast Pacific
GLOBEC Program.
Appendix A
Ichthyoplankton samples collected in 2010 and 2011, and 15
additional samples collected in 1998–2009 which were incorporated into the winter analyses. Transect and station (km from
shore) locations are shown in Fig. 1. ’Study’ refers to the comparative study with which the samples were analyzed: CW = coast wide
(Auth, 2011); NSB = near-shore biweekly (Auth et al., 2011);
W = winter (Daly et al., 2013).
117
T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
Year
Month
Day
Transect
1998
1998
1999
2000
2000
2001
2001
2001
2002
2004
2009
2009
2009
2009
2009
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
3
3
3
2
3
1
2
2
3
1
1
1
2
2
3
2
2
2
2
2
2
2
2
2
2
2
2
3
3
3
3
3
3
4
4
5
5
5
5
5
5
5
5
5
5
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
5
18
11
16
7
16
14
28
20
15
14
23
4
17
24
9
9
9
9
9
9
22
22
22
22
22
22
19
19
19
19
19
19
11
11
5
5
15
15
29
29
29
29
30
30
3
3
3
4
4
4
16
16
17
17
17
17
17
17
18
18
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
HH
HH
HH
HH
NH
NH
NH
NH
NH
NH
NH
NH
CR
CR
CR
CR
CR
HH
HH
HH
HH
NH
Station
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
9
18
28
37
46
2
9
18
28
37
46
2
9
18
28
37
46
9
18
9
18
9
18
21
37
53
69
9
18
46
65
84
9
18
28
22
39
57
75
95
21
37
53
85
9
Study
Year
Month
Day
Transect
Station
Study
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
NSB/W
NSB/W
W
W
W
W
NSB/W
NSB/W
W
W
W
W
NSB/W
NSB/W
W
W
W
NSB
NSB
NSB
NSB
NSB
NSB
CW
CW
CW
CW
NSB
NSB
CW
CW
CW
NSB/CW
NSB
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
NSB
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
6
6
6
6
6
6
6
6
6
6
6
6
6
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
7
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
18
18
18
18
19
19
19
19
19
20
20
26
26
8
12
12
13
13
13
13
14
14
14
14
14
15
15
15
15
15
15
16
16
16
20
20
29
29
7
7
18
18
24
25
25
25
25
25
26
26
26
26
26
26
27
27
27
27
28
28
28
NH
NH
NH
NH
NH
NH
WB
WB
WB
WB
WB
NH
NH
NH
HH
HH
HH
HH
HH
NH
CR
NH
NH
NH
NH
CR
CR
CR
NH
WB
WB
WB
WB
WB
NH
NH
NH
NH
NH
NH
NH
NH
HH
HH
HH
HH
NH
NH
CR
CR
CR
NH
NH
NH
CR
CR
WB
WB
WB
WB
WB
18
28
46
65
84
102
22
39
56
71
87
9
18
9
21
37
53
69
85
102
75
28
46
65
84
22
39
57
9
22
39
56
71
87
9
18
9
18
9
18
9
18
37
53
69
85
84
102
22
39
57
28
46
65
75
95
71
87
22
39
56
NSB
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
NSB
NSB
NSB
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
NSB
CW
CW
CW
CW
CW
NSB
NSB
NSB
NSB
NSB
NSB
NSB
NSB
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
(continued on next page)
118
T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
Appendix A (continued)
Year
Month
Day
Transect
Station
Study
Year
Month
Day
Transect
Station
Study
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2010
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
9
9
9
9
9
9
9
9
9
9
9
9
9
9
1
1
1
1
1
1
1
1
2
2
2
2
2
2
3
5
5
5
5
5
5
5
5
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
7
7
7
7
7
7
7
9
9
20
20
21
21
21
22
22
22
22
23
23
23
10
10
10
10
10
10
25
25
10
26
26
26
26
26
23
12
12
12
13
13
14
14
14
12
12
13
13
13
13
13
14
14
14
14
14
14
15
15
15
15
16
16
16
13
13
13
14
14
14
14
NH
NH
NH
NH
HH
HH
HH
HH
HH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
NH
HH
HH
HH
HH
NH
NH
NH
NH
HH
HH
HH
HH
HH
NH
NH
CR
CR
CR
NH
NH
NH
CR
CR
WB
WB
WB
WB
WB
HH
HH
HH
HH
HH
NH
NH
9
18
9
18
21
37
53
69
85
84
102
28
46
65
2
9
18
28
37
46
2
9
9
9
18
28
37
46
9
21
37
53
69
84
28
46
65
21
37
53
69
85
84
102
22
39
57
28
46
65
75
95
71
87
22
39
56
21
37
53
69
85
84
102
NSB
NSB
NSB
NSB
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
W
W
W
W
W
W
W
W
W
W
W
W
W
W
W
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
2011
7
7
7
7
7
7
7
7
7
7
7
7
7
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
8
9
9
9
9
9
9
9
9
9
9
9
9
9
9
9
9
9
9
9
9
15
15
15
15
15
15
16
16
16
16
17
17
17
13
13
14
14
14
14
14
15
15
15
15
15
16
16
17
17
17
15
15
15
16
16
16
16
17
17
17
18
18
18
19
19
19
19
19
20
20
CR
CR
CR
NH
NH
NH
CR
CR
WB
WB
WB
WB
WB
HH
HH
HH
HH
HH
NH
NH
CR
CR
NH
NH
NH
WB
WB
WB
WB
WB
HH
HH
HH
HH
HH
NH
NH
NH
NH
NH
CR
CR
CR
CR
CR
WB
WB
WB
WB
WB
22
39
57
28
46
65
75
95
71
87
22
39
56
21
37
53
69
85
84
102
22
39
28
46
65
22
39
56
71
87
21
37
53
69
85
84
102
28
46
65
22
39
57
75
95
56
71
87
22
39
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
CW
T.D. Auth et al. / Progress in Oceanography 137 (2015) 103–120
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