Egg production rates of the copepod Calanus marshallae in relation to
seasonal and interannual variations in microplankton biomass and
species composition in the coastal upwelling zone off Oregon, USA
Peterson, W. T., & Du, X. (2015). Egg production rates of the copepod Calanus
marshallae in relation to seasonal and interannual variations in microplankton
biomass and species composition in the coastal upwelling zone off Oregon, USA.
Progress in Oceanography, 138, 32-44. doi:10.1016/j.pocean.2015.09.007
10.1016/j.pocean.2015.09.007
Elsevier
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Progress in Oceanography 138 (2015) 32–44
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Egg production rates of the copepod Calanus marshallae in relation
to seasonal and interannual variations in microplankton biomass
and species composition in the coastal upwelling zone off Oregon, USA
William T. Peterson a,⇑, Xiuning Du b
a
b
NOAA-Fisheries, Northwest Fisheries Science Center, Hatfield Marine Science Center, Newport, OR, United States
Cooperative Institute for Marine Resources Studies, Oregon State University, Hatfield Marine Science Center, Newport, OR, United States
a r t i c l e
i n f o
Article history:
Received 15 May 2015
Received in revised form 1 August 2015
Accepted 17 September 2015
Available online 5 October 2015
a b s t r a c t
In this study, we assessed trophic interactions between microplankton and copepods by studying
the functional response of egg production rates (EPR; eggs female 1 day 1) of the copepod Calanus
marshallae to variations in microplankton biomass, species composition and community structure.
Female C. marshallae and phytoplankton water samples were collected biweekly at an inner-shelf station
off Newport, Oregon USA for four years, 2011–2014, during which a total of 1213 female C. marshallae
were incubated in 63 experiments. On average, 80% of the females spawned with an overall mean EPR
of 30.4. EPRs in spring (Apr–May, average of 40.2) were significantly higher than summer (Jun–Oct;
26.4). EPRs were intermediate in winter (Jan–Feb; 32.5). Interannually, EPRs were significantly higher
in 2014 than 2011 and 2012. Total chlorophyll a (Chl a) concentration and diatom abundance both were
significantly higher in summer while no seasonal differences were found in abundance of dinoflagellates,
ciliates or Cryptophytes. Although total Chl a showed no interannual differences in bulk biomass of
phytoplankton, community structure analysis indicated differences among years. More diverse diatom
communities were observed in 2013 and 2014 compared to 2011 and 2012. Relationships between
EPR and potential food variables (phytoplankton and ciliates) were significant by season: a hyperbolic
functional response was found between EPR and total Chl a in winter–spring and summer, separately,
and between EPR and ciliate abundance in winter–spring; a linear model fit best the functional response
of EPR to diatom abundance in summer. The estimate of potential population recruitment rate (the
number of females EPR; eggs day 1 m 2) was highest in spring (Apr–May), and annually was highest
in 2013 (11,660), followed by 2011 (6209), 2012 (3172) and 2014 (1480). Our observations of in situ
EPR were far higher than published laboratory rates of 23.5, calling into question our past laboratory
studies that used mono-algae cultures as food for copepods. Moreover, an increasing number of studies
(including this study) are showing an apparent greater importance of ciliates as a nutritious food source
for Calanus species demonstrating the importance of the microbial loop to secondary production.
Ó 2015 Published by Elsevier Ltd.
1. Introduction
Calanus marshallae, a sibling species of Calanus finmarchicus,
Calanus sinicus and Calanus australis (Frost, 1974), occurs commonly
in continental shelf waters of the northern California Current from
January through August as well as in the coastal Gulf of Alaska and
Bering Sea. This species was thought to be restricted to the North
Pacific Ocean and Bering Sea (Frost, 1974) as well as the Chukchi
Sea (Hopcroft et al., 2010); however, there is evidence that it has
invaded the Arctic Ocean, in waters near Spitsbergen (Melle and
Skjoldal, 1998). In the northern California Current, adults usually
⇑ Corresponding author. Tel.: +1 5418670201.
E-mail address: bill.peterson@noaa.gov (W.T. Peterson).
http://dx.doi.org/10.1016/j.pocean.2015.09.007
0079-6611/Ó 2015 Published by Elsevier Ltd.
go through a brief period of diapause during autumn months after
which adults re-appear in January. The awakening in winter is presumably timed to take advantage of a winter bloom that occurs frequently in February (Feinberg et al., 2010). A cohort is born at this
time, which becomes mature within 7–8 weeks (Peterson, 1986);
during the course of annual growing season, at least five generations are produced (Peterson, 1980). This life history is in contrast
to that of C. marshallae populations in Dabob Bay, Washington
(Osgood and Frost, 1994) and the Bering Sea (Baier and Napp,
2003; Smith and Vidal, 1984) which produce only one or two generations per year. The reason that C. marshallae can produce multiple generations in the northern California Current is almost
certainly due to the availability of sufficient food resources
throughout much of the year which in turn supports egg production
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
and subsequent development and growth of nauplii and
copepodites.
The coastal waters off Oregon are characterized by high phytoplankton production nearly year-round due to four independent
‘‘primary production events” – a late winter bloom (in January/
February) in some years, a spring bloom (in April/May), multiple
summer blooms during the upwelling season (June–September),
and a fall bloom after the end of the upwelling season (October/
November). These blooms have vastly different magnitudes,
ranging from 1 to 2 lg Chl-a L 1 during the winter blooms to
15–30 lg Chl-a L 1 during summer blooms. The fall bloom, when
it occurs, is on the order of 10 lg Chl-a L 1 (Du and Peterson,
2014). The natural phytoplankton community contains a mixture
of taxa and sizes, from smaller nano- and micro-flagellates to larger long-chain diatoms that exceed 1 mm in length. Moreover,
the dominant species are highly variable and ephemeral during
bloom events (Du and Peterson, 2014). Thus we were curious as
to the ability of C. marshallae to take advantage of the different
prey types, bloom magnitude and sizes of the microplankton species as well as their functional response to phytoplankton biomass
and species composition.
Despite the broad distribution of C. marshallae around the margin of the temperate/subarctic waters of the eastern North Pacific,
Bering Sea and the Chukchi Sea, few studies ecological exist and
most are limited to the northern California Current. Past work on
egg production rates (EPR, eggs female 1 day 1) of C. marshallae
did not consider the potential effects from microplankton in terms
of species and community structure, except that significant relationships were found between chlorophyll-a (Chl a) and EPR.
Gómez-Gutiérrez and Peterson (1999) reported a mean EPR of
22.5 during Jul–Aug 1997. These rates were linearly correlated
with Chl a concentration. Similarly, Peterson et al. (2002) found a
significant linear relationship between EPR and Chl a in June
1996. The range in values of EPR across continental shelf waters
was 20–30 when Chl a >5–10 lg L 1. Shaw et al. (2009) reported
an average rate of 20.3 during three cruises in summers 2005 and
2006. There is a somewhat controversial report of EPR by ‘‘C. marshallae/glacialis” from the western Arctic Ocean by Plourde et al.
(2005) who found average EPRs of 14 and 20 in spring and summer
2002, respectively, but Lane et al. (2008) who sampled copepods
on the same cruise as Plourde et al. (op.cit) claimed that there were
no C. marshallae in samples.
This study considers several new topics related to EPR of C. marshallae and the in situ food environment in the shelf waters off Newport, Oregon. The first topic considers reasons why a wide range of
EPRs were observed during incubation experiments over a four-year
period and how that was affected by the potential microplankton
food resources. For example, in our experiments, individual female
C. marshallae were found to be capable of producing up to 97 eggs
per spawn with a maximum population average EPR of 68.5. These
rates are far higher than any of our previous studies (Peterson, 1988;
Gómez-Gutiérrez and Peterson, 1999; Peterson et al., 2002; Shaw
et al., 2009). Meanwhile, the present study also observed very low
EPRs of <10. Thus we wanted to determine if such a wide range of
EPR values were simply a matter of seasonal variations in
microplankton biomass as opposed to variations in abundance of
specific functional groups (diatoms, dinoflagellates, Cryptophytes
and ciliates), community structure and/or species diversity. Second,
on a few occasions, EPRs were depressed during certain diatom
blooms, noteworthy because past studies have indicated that some
diatom blooms may be detrimental to copepod egg production and
egg hatching success (Paffenhofer, 2002; Paffenhofer et al., 2005).
Thus we tried to determine if the reduced EPRs could be attributed
to specific diatom taxa. Third, we compared results of EPR based on
incubation of freshly-caught females (this study) with EPR
measured under controlled laboratory conditions (Peterson, 1988)
33
during which females were fed a single diatom species Thalassiosira
weissflogii. We discuss reasons why the rates measured in the lab
were less than half of the rates from in situ incubation. Finally, we
discuss the potential reproduction rates (as the product of EPR on
a given day abundance of females in situ on the same day) to
determine if there were seasonal and interannual differences in
potential ‘recruitment’.
2. Methods
Female C. marshallae for egg production experiments and
phytoplankton were collected biweekly from a station located 5
nautical miles (9 km) from shore, in 62 m of water along the Newport Hydrographic line (station NH05, 124.2°W, 44.6°N) off central
Oregon, USA over a four-year period of 2011–2014. C. marshallae
were collected mostly at night from the upper 20 m of the water
column using a 60 cm diameter Bongo net (333 lm mesh). Live
samples were placed in a 20 L cooler filled with surface seawater
and were transported to a temperature-controlled room in our
shore-based laboratory within 2–3 h of collection. To collect sample
for analysis of abundance of female C. marshallae, we used a ½ m
202 lm mesh net hauled vertically from a few meters above the
sea floor to the sea surface. The contents of the cod-end were preserved in formalin (final concentration of 5–10%).
2.1. Copepod egg production experiments
Individual female C. marshallae were sorted with the aid of a
stereomicroscope and a wide-bore pipette. Healthy-appearing
individuals were placed into 60 ml jars prefilled with sieved
(200 lm mesh) surface seawater. The goal was to pick 20–25
females for each experiment but this depended on the availability
of female C. marshallae. Individual jars were incubated for 24 h in
the dark at a constant temperature 10 ± 0.5 °C, chosen because it
is the average year-around value observed for the upper 20 m of
the water column over the inner and middle shelf off Oregon (winter is 10.3 °C; summer 10.1 °C, Peterson, unpublished data). Eggs
were first counted in the late morning, about 6–8 h after setting
up each experiment. Individuals that had not spawned by that time
were reexamined every 4–5 h until the end of the experiment.
Most females spawn eggs between 0400 and 1100 h (Peterson,
pers. obs. for C. marshallae), thus enumerating the eggs shortly
after they were spawned reduces the potential for egg cannibalism
following recommendations of Runge and Roff (2000). Also
Peterson (1988) discussed why cannibalism is not likely to be a
problem in these types of experiments. Egg production rate (EPR;
eggs female 1 day 1) is calculated from the total eggs in an experiment divided by the number of females in that experiment, thus it
is an estimate of the ‘‘population” egg production rate, not an average of only those females that spawned during each experiment.
2.2. Phytoplankton sample analysis
On each cruise, surface water samples were collected for the
analyses of phytoplankton species and chlorophyll-a (Chl a). Total
Chl a and >5 lm size fraction subsamples (each of 100 ml) were filtered through GF/F filters and >5 lm polycarbonate filters, respectively, extracted in 90% acetone for 24 h in the dark, and then
fluorescence was measured using a Turner 10-AU fluorometer.
The concentration of Chl a was calculated following equations in
Strickland and Parsons (1972). The <5 lm Chl a concentration
was the difference between total Chl a and the >5 lm fraction.
Phytoplankton samples were fixed with acid Lugol’s solution in
125 ml bottles (2% final concentration) immediately after collection.
To identify and enumerate species, a subsample of 50 ml was taken
34
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
from the full sample and then settled in a 50 ml tissue culture flask
(Falcon) for at least 24 h prior to counting. The wide flat side of the
flask was placed on the stage of an inverted light microscope (Leica
DM IRB); species identification and enumeration were carried out at
the magnifications of 200 or 400. The portion of the 50 ml subsample that was examined varied with species density. To meet a
minimum total count of 500 cells, between 2 and 20 transects across
the wide side of the flask were counted. For diatoms and dinoflagellates, species identification was made primarily following Horner
(2002). A group of smaller dinoflagellates (length <20–30 lm) were
relatively consistent and abundant in our samples but difficult to be
identified to species, thus we use ‘‘small dinoflagellates” to name
this group. Ciliates, a common group of microzooplankton in our
phytoplankton water samples, were included for this study and
are important because during the non-diatom bloom season they
comprised a significant fraction of total microplankton biomass.
For ciliates, identification to species level was not made, instead,
the major subgroup of naked ciliates were recorded as size categories, small ciliates (length <30 lm) and large ciliates (>30 lm).
Loricate ciliates were named as ‘‘tintinnids”. Cryptophytes were
enumerated because they are morphologically easier to be recognized, whereas other nanoflagellates were not included for quantitative analysis due to the identification limitation of light microscopy.
Cell abundance is expressed as cells per liter (cells L 1).
2.3. Statistical analysis
To compare interannual and seasonal variations in EPR and
microplankton biomass, Analysis of Variance (ANOVA) was implemented on EPR, abundance of four functional groups (diatom,
dinoflagellate, ciliate and Cryptophyte) and Chl a concentration
data series, respectively. Tukey HSD pairwise comparisons were
used to test for the differences in pairs. Phytoplankton abundance
and Chl a concentration were log10(x + 1) transformed before analyses so as to achieve normality and equal variance. The functional
response of EPR (dependent variable) to the various measures of
microplankton biomass (taxa and chlorophyll) was characterized
by ordinary linear regression and by hyperbolic (Michaelis–Menton) models. The equation for the hyperbolic model is y = ax/(b
+ x), where a is the maximum EPR and b, the half-saturation constant value of the independent variable where one-half of the maximum value of the dependent variable (EPR) is reached.
Differences in phytoplankton community structure were examined using hierarchical cluster analysis (with SIMPROF significance
test at 0.05) and nonmetric multidimensional scaling (NMDS).
Two-way crossed ANOSIM (Analysis of Similarity) was used to test
for differences in phytoplankton community structure by year and
season. The statistic R (scaled to a range of values from 0 to 1) in
ANOSIM is a measure of community separation between groups
with 0 indicating no separation and 1 indicating complete separation. Similarity of percentage (SIMPER) analysis provides a list of
species in rank order of high to low species percent contribution
to the overall similarity of a specific group. The length of the species list presented in Results was determined when cumulative
individual species percent contribution added up to 80% of total.
The above multivariate analyses were conducted in PRIMER-E software (Clarke and Gorley, 2006). Other statistical comparisons and
correlation analysis were performed in JMP 11 (SAS).
3. Results
3.1. Egg production rate (EPR)
A total of 1213 females were incubated in 63 experiments, an
average of 19 females per experiment. EPRs (eggs female 1 day 1)
were highly variable (Fig. 1A). The three lowest values were 3.9 (27
Jul 2011), 4.0 (7 Mar 2012) and 7.7 (20 July 2012) and the three
highest 68.5 (1 Apr 2014), 62.0 (29 Jul 2013) and 55.1 (16 Jan
2014). The overall mean EPR was 30.4 ± 15 (standard error). It
was unusual for all females to spawn in an experiment (only 12
out of 63 experiments). The average percentage of females which
spawned during the 24 h incubation was 80%, and by season, 84%
in winter–spring (Jan–May) and 75% in summer (Jun–Oct). The
average percentage of females that spawned was related to Chl a
concentration: 81% when Chl a concentrations were high
(5–30 lg L 1), 77% when less than 5 lg/L and 74% when below
1 lg L 1. Because not all females spawned during a 24 h incubation, per capita rates (egg production rate calculated using only
those females that spawned) were higher than the population rates
(mean 39.7 vs. 30.4, t = 5.77, p < 0.001). However, the two ‘rates’
were significantly correlated (R2 = 0.87, not illustrated) suggesting
results of comparing EPR rates in response to various food environments are not dependent upon which method is used to calculate
EPR. We chose the ‘population’ rates as this method is most often
used by copepodologists.
3.2. Monthly EPR and Chl a concentration
The correspondence between monthly average EPR and Chl a
was poor. Monthly average EPRs (Fig. 2) were higher in Jan–Feb
and Apr–May than Aug-Oct, and lower in Mar, Jun–Jul and
Nov–Dec. Total Chl a concentration ranged from 0.5 to 28.8 lg L 1
(Fig. 1B) and was much higher from July to September and lower in
the other months (Fig. 2). The >5 lm Chl a size fraction followed
the same seasonal patterns as total Chl a, whereas monthly
averaged percentage of Chl a <5 lm size fraction was relatively
constant, ranging from 50.3% to 70.8%.
3.3. Seasonal and interannual variations in EPR, phytoplankton
biomass and functional groups
Fewer experiments were carried out in November (1 experiment) and December (2 experiments) due to low numbers and/or
lack of females in the Bongo net samples. Although there was a
high number of females (average of 19) per experiment in March,
the dramatically decreased monthly average EPR compared to
February and April (Fig. 2) was likely related to a small sample size
(2 experiments). We were concerned that the low sample size in
March, November and December might bias quantitative evaluation of EPR. Therefore, the three months with small sample sizes
were not included in the seasonal/interannual quantitative
analyses.
Interannual differences in EPR were significant (p = 0.023).
There were higher EPRs in 2014 than 2011 and 2012 (p = 0.05),
respectively (Table 1). Seasonal changes were also significant
(p = 0.018) and showed higher EPRs in Apr–May (spring) than
Jun–Oct (summer) but similar rates between winter (Jan–Feb)
and spring.
In contrast, no significant interannual changes were shown in
either total Chl a or size-fractionated Chl a concentrations
(p = 0.9), but seasonal variations were significant (p < 0.01) and
the overall difference was the result of higher Chl a concentrations
in summer than winter.
Interannual variations were not consistent for the four functional groups (two-way ANOVA, year and season): diatoms were
significantly more abundant in 2013 than 2012, and Cryptophytes
were more abundant in 2013 than in 2011, but interannual differences were insignificant for dinoflagellates and ciliates. There were
seasonal differences for diatoms only (p < 0.05): higher abundance
in summer than in spring and winter, and spring higher than winter. The abundances of dinoflagellates, ciliates and Cryptophytes
35
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
Fig. 1. Upper panel (A): Egg production rates (EPRs) during 2011 to 2014. The dotted line is the average EPR over all experiments. Lower panel (B): total Chl a concentration
(lg L 1) on the same dates as EPR. Note the lack of correspondence between EPR and Chl a concentration.
in 2014 than 2011 and Cryptophytes were more abundant in
2013 than 2011 (p < 0.05).
3.4. Phytoplankton community structure and EPR
Fig. 2. Monthly average egg production rates (EPR, eggs female 1 day 1) and Chl a
size-fraction concentrations (lg L 1). The array of numbers on the top is the average
number of female copepod Calanus marshallae used in all experiments in each
month for 2011–2014.
were similar among seasons. One-way ANOVA for testing interannual differences in each of the phytoplankton functional groups
was also run for the winter and spring seasons, separately. In winter, significantly higher abundances were found for ciliates in 2014
than 2011 and 2012 (p = 0.02), and for dinoflagellates in 2014 than
2011 (p = 0.04), but no significant differences in diatoms and Cryptophytes among years. As for spring, diatoms and ciliates were
similar among years; dinoflagellates were again more abundant
Cluster analysis identified five different communities (Fig. 3,
upper panel), among which cluster ‘‘a” represents a community
type characterized by the lowest average diatom abundance
(174,040 cells L 1) and lowest species richness (13 diatom species).
Most of the samples were from January, February and April with
some from September and October. Cluster ‘‘c” represents a summer community type with the highest average diatom abundance
(1,740,800 cells L 1) and species richness (31 diatom species) and
includes samples mostly from May to October. Notice that nearly
all samples in ‘‘c” were from 2013 and 2014. Clusters ‘‘d” and ‘‘e”
include spring and fall samplings, respectively, with moderately
Table 1
Interannual variation in egg production rate (EPR ± SE, eggs female 1 day 1) of the
female copepod Calanus marshallae. March, November and December are not included
for the comparisons since fewer experiments over the four years were done. Numbers
in the brackets indicate sample size.
Year
Annual
Jan–Feb
2011
2012
2013
2014
26.1 ± 3.3(18)
26.3 ± 3.8(13)
35.3 ± 3.8(14)
40.9 ± 4.1(12)
29.7 ± 6.3(4)
23.3 ± 9.4(2)
26.5 ± 9.0(2)
53.4 ± 10.3(2)
Apr–May
28.6 ± 7.3(3)
38.0 ± 6.0(5)
44.7 ± 5.7(5)
44.9 ± 6.5(5)
24.2 ± 3.8(11)
18.7 ± 5.0(6)
31.1 ± 4.8(7)
31.9 ± 6.5(5)
Jun–Oct
Mean
31.8 ± 2.0(57)
32.5 ± 4.7(10)
40.2 ± 3.0(18)
26.4 ± 2.6(29)
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W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
20
clusters
a
b
c
d
e
Bray-Curtis similarity
40
60
80
9/1/2011
9/13/2011
8/4/2011
4/27/2013
10/25/2012
4/8/2014
7/27/2011
7/22/2011
4/1/2014
1/10/2011
1/25/2011
2/24/2012
2/4/2014
1/16/2014
2/23/2014
1/8/2012
2/11/2012
4/7/2012
5/30/2013
9/29/2011
4/1/2013
4/16/2013
4/8/2011
4/14/2012
10/26/2011
10/4/2013
10/15/2011
7/6/2011
1/14/2013
2/10/2011
2/26/2011
8/17/2011
8/7/2012
7/23/2013
7/29/2013
7/20/2012
7/6/2014
7/22/2014
7/9/2013
10/22/2013
8/25/2013
5/8/2013
6/7/2013
6/19/2013
4/25/2014
5/19/2014
2/14/2013
5/6/2014
6/11/2014
9/11/2013
9/26/2013
6/8/2011
5/9/2011
5/18/2011
4/17/2011
5/19/2012
10/7/2012
100
Samples
a
a
d
d
c
a
a
a
a
a
a
c
c
c
c
c c
c
c
c
c
c
c
c
aa
e
a
e
a
e
a
a
a
e
e
a
a
a
a
aa
a
3
2
2
2
a
a a
a
a
c
b
b
a
d
2D Stress: 0.2
2D Stress: 0.2
1
4
3
2
2
4
a
4
4
3
2
1
2
4
3
1
a
1
4
3
4
3
2
44
3
3
a
4
4
3
3
1
1
1
4
3
2
3
1
2
1
2
2
1
e
3
Fig. 3. Phytoplankton community clusters (a–e, p = 0.05) were identified through hierarchical cluster analysis (upper panel) and were also shown in a nonmetric
multidimensional scaling plot (NMDS, left lower panel). Quartile EPR (right lower panel) was overlaid on the phytoplankton community pattern in NMDS. Numbers 1–4 stand
for levels of EPR (eggs female 1 day 1). 1: 3.9–17.6; 2: 17.6–29.4; 3: 29.4–40.2; 4: 40.2–68.5. Note that cluster ‘‘a” is a winter community, ‘‘c” a summer community, ‘‘d” and
‘‘e” seasonal transition communities and ‘‘b” abnormal summer community.
Table 2
Summary of two-way crossed ANOSIM comparisons of phytoplankton community structure. R value (range of 0–1) in the global and pairwise tests (shown as ‘‘R” and ‘‘p” values)
indicates the relative degree of difference by year and season. W: winter, Sp: spring; Su: summer.
Source of variation (Global test)
Year
11 vs 12
0.4, 0.007
Season
R = 0.408
p < 0.001
R = 0.352
p < 0.001
11 vs 13
0.521, <0.001
Pairwise test – between year
11 vs 14
0.513, <0.001
12 vs 13
0.43, 0.007
12 vs 14
0.364, 0.009
W vs Sp
0.423, 0.005
Pairwise test – between season
W vs Su
Sp vs Su
0.23, 0.042
0.417, <0.001
high diatom abundance (721,380 and 583,970 cells L 1, respectively) and species richness (27 and 17 diatom species, respectively). The three sampling dates in ‘‘d” were from 2013 to 2014
and the six sampling dates in ‘‘e” were from 2011 to 2012. The
cluster ‘‘b” included two sampling dates and was distinguished
from ‘‘c” by some unusually abundant species (a silicoflagellate
13 vs 14
0.11, 0.2
Dictyocha speculum and a dinoflagellate Protoperidinium depressum)
in addition to the common ones in ‘‘c”. The ordination analysis
(Fig. 3, left lower panel) also showed a clear separation of
phytoplankton community types. Cluster ‘‘a” and ‘‘c” had no overlap, ‘‘b” was associated with ‘‘c” whereas ‘‘d” and ‘‘e” appeared as
transitional communities.
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W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
Changes of phytoplankton community structure were significant
across years (ANOSIM, R = 0.408, p < 0.001, Table 2) and seasons
(R = 0.352, p < 0.001). Pair-wise year comparisons were significant
except 2013 vs 2014 (p = 0.2) and all the pair-wise seasonal comparisons were significant as well (e.g. winter vs spring, p = 0.005).
Although there were significantly different phytoplankton
community clusters, the corresponding EPRs were similar
(p = 0.6, one-way ANOVA). For example, the sampling dates of
two most contrasting clusters ‘‘a” (winter) and ‘‘c” (summer) had
very similar EPRs on average, 32.9 ± 3.1 and 32.6 ± 4.4, respectively. Furthermore, patterns of the five clusters shown in the ordination plot were not mirrored by the values of EPR represented as
quartile levels (Fig. 3, right lower panel). Thus phytoplankton
community structure alone cannot account for variations in EPR.
Table 3
Egg production experiments conducted in winter (Jan–Feb). Chl a concentration
indicates if a small winter bloom (>1 lg L 1) was present or not. Abundances
(cells L 1) of s-dino (small dinoflagellates), ciliates and Cryptophytes are also shown
along with egg production rates (EPR) eggs female 1 day 1.
Date
Chl a
s-dino
Ciliates
Cryptophytes
EPR
10-Jan–11
22-Jan–11
10-Feb-11
26-Feb-11
8-Jan–12
11-Feb-12
24-Feb-12
14-Jan–13
24-Feb-13
16-Jan–14
4-Feb-14
0.6
0.8
0.5
1.7
0.7
0.9
0.7
0.7
0.8
0.8
1.5
3430
3773
3087
8233
3773
6861
4460
1201
8576
14,408
42,880
343
5489
686
1029
5832
na
686
1887
4803
13,379
9148
30,188
66,207
5832
52,828
113,890
na
14,751
6518
36,019
145,449
101,197
19.9
26.6
35.6
36.7
na
37.7
8.9
15.6
37.4
55.1
51.8
Average
0.9
9153
4771
60,299
33.9
3.5. Relationships between EPR and Chl a, phytoplankton functional
groups
When EPRs were plotted against total Chl a concentrations in
winter–spring (Jan–May) and summer (Jun–Oct), respectively,
hyperbolic models (Michaelis–Menton) best represented their correlations at p < 0.01 (Fig. 4). The estimated maximum EPR was 50.4
in winter–spring with a 0.4 lg L 1 Chl a half-saturation constant,
higher than the summer maximum EPR of 39.7 with a 2.6 lg L 1
Chl a half-saturation constant.
In the 10 experiments in Jan–Feb (Table 3), we collected female
C. marshallae either before or during the small winter bloom (Chl
a = 1–2 lg L 1). An average EPR for winter was 33.9 (maximum
of 55.1). Thus it is clear that significant numbers of eggs are produced annually during winter months regardless of the presence
of significant phytoplankton blooms.
To further explore this idea, EPRs were regressed against ciliate
and diatom abundance by season, respectively (Fig. 5). A significant
correlation was found between EPR and ciliate abundance in
winter–spring (hyperbolic model, p = 0.008) with an estimated
maximum EPR of 44.6, while in summer EPR and diatom abundance
was significantly correlated (linear model, p = 0.01, Fig. 5). A
hyperbolic model was also applied for EPR versus diatom
abundance in summer but the result was less significant (p = 0.07)
with a maximum EPR of 40.6.
Non-significant relationships were found between ciliates and
EPR in summer (hyperbola, p = 0.64), and between diatoms and
EPR in winter–spring (hyperbola, p = 0.19). Neither dinoflagellates
nor Cryptophytes were correlated significantly with EPR in either
season (not illustrated). An exception for dinoflagellates is that
the subgroup – small dinoflagellates, was found significantly
correlated with EPRs in winter–spring (R2 = 0.24, p = 0.02) and this
correlation was strengthened when only winter data were
considered (R2 = 0.65, p = 0.005).
3.6. Diatom community composition and species richness
While the abundance of dinoflagellates, ciliates and Cryptophytes were similar among years and seasons, large fluctuations
were seen within diatom functional group in terms of species richness and composition (Table 4). Species composition was generally
similar between 2013 and 2014, and in both years species richness
was far higher (17 and 18 species, respectively) than 2011 and
2012 (7 and 9 species, respectively).The three most abundant taxa
contributing to the interannual differences in the diatom community in 2011 were Nitzschia, Dactyliosolen fragilissimus and Pseudonitzschia deli/p-deli; in 2012, Chaetoceros debilis, D. fragilissimus and
Nitzschia; in 2013, three Chaetoceros species (debilis, socialis and
contortus); in 2014, Leptocylindricus minimus, D. fragilissimus and
Ch. debilis. The full list is shown in Table 3.
By season, species richness increased gradually from winter (4
species) to summer (15 species) with only three species common
in all seasons Cylindrotheca closterium, Thalassionema nitzschioides
and Asterionellopsis glacialis (Table 3). There were 9 common
diatom species between spring (Apr–May) and summer and the
ones more likely to be present in both seasons are the genera
Chaetoceros, Pseudo-nitzschia and Thalassiosira.
EPRs were significantly correlated with species richness of
those species which dominate in a given sample (those species
which had an abundance >104 cells L 1 in summer from June to
August). Species richness accounted for 32% of the variance
(Fig. 6); however, this relationship became insignificant (p = 0.26)
when the test period was expanded from June to October (plot
not shown).
3.7. EPR and summer diatom blooms
Fig. 4. Egg production rates (EPR; eggs female 1 day 1) of female Calanus marshallae as a function of total Chl a concentrations (lg L 1). Two hyperbolic curves are
the regressions of EPR versus total Chl a in Jan to May (green and grey symbols) and
Jun to Oct (red symbols), respectively. Coefficients (a and b) are 50.4 and 0.4 for Jan
to May, 39.7 and 2.6 for Jun to Oct, respectively. (For interpretation of the references
to color in this figure legend, the reader is referred to the web version of this
article.)
In 5 of 21 experiments in summer (Jun–Oct), EPRs were lower
than expected, determined by the data points falling outside of
the lower 95% confidence interval (CI) band in the linear regression
plot (Fig. 5C). These observations raise the question as to what
might have been different in the phytoplankton community when
Chl a concentrations are high and/or when large diatom blooms
38
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
Fig. 5. Egg production rates of female Calanus marshallae as a function of total diatom (left panel A and C) and ciliate abundance (right panel B and D) by season (winter–
spring, summer). In plot C, the blue lines indicate the 95% confidence intervals (CI). Below the lower 95% CI, empty circles indicate dates with very low EPRs and above the
upper 95% CI, filled red circles indicate dates with very high EPRs. Note that the hyperbola model for diatom abundance versus EPR in summer was less significant (r = 0.41,
p = 0.07, not illustrated here) than linear model. Coefficients (a and b) in each of the hyperbola models are: 43.7 and 61046.2 in (A); 44.6 and 544.2 in (B); 24.5 and 297.9 in
(D). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
were observed in this season. Thus we inspected closely relationships between EPRs and diatoms on those few dates (Table 5).
22 July 2011 (EPR = 3.8). Chl a concentrations were moderately
high (3.6 lg L 1) but the small <5 lm size fraction was 81% of
total. Total diatom abundance was very low (31,903 cells L 1)
while the small dinoflagellates group was the highest observed
during our study (99,767 cells L 1, 99% of total dinoflagellate
abundance on this date). Since both diatoms and Chl a >5 lm
size fraction had low concentrations, this suggests that on this
date small dinoflagellates alone, though abundant, might not
be a suitable food resource to induce high EPRs.
27 July 2011 (EPR = 10.1). Chl a concentration was higher
(6.3 lg L 1) than on 22 July but with 84% in the <5 lm size fraction. A mono-species bloom of the diatom D. fragilissimus
occurred (691,827 cells L 1, 98% of total diatom abundance)
which might explain the low EPR.
20 July 2012 (EPR = 7.7). Chl a concentration was 3.0 lg L 1
with 48% in the <5 lm size fraction. EPR should have been
higher because a typical summer diatom bloom was observed
on this date, with total diatom abundance of 960,511 cells L 1
and a diverse set of dominants: D. fragilissimus, Skeletonema
costatum, Guinardia delicatula, Chaetoceros (Ch. contortus, Ch.
debilis, Ch. socialis, Ch. radicans, Ch. affinis, Ch. lorenzianus and
similis) and Thalassiosira nordenskioeldii, The most abundant
species was again D. fragilissimus (564,302 cells L 1, 51% of total
diatom abundance), the same species associated with the low
EPR on 27 July 2011. However, for all experiments, the relationship between EPR and D. fragilissimus was not statistically
significant (Hyperbolic model, n = 25, r = 0.2, p = 0.4).
7 Aug 2012 (EPR = 5.7). Chl a concentration was 3.8 lg L 1 with
66% in the <5 lm size fraction. The low EPR was similar to the
earlier observation on 20 July 2012. Diatoms developed another
typical bloom (324,688 cells L 1) with co-existed dominants
such as Coscinodiscus, Pseudo-nitzschia, G. delicatula and Ch.
debilis. However, the large dinoflagellate Protoperidinium compressum and silicoflagellate D. speculum both were unusually
abundant at the same time (31,388 and 162,944 cells L 1,
respectively) compared to their long term average amount in
our study area (510 and 3808 cells L 1, respectively). The low
EPR might be related to these two unusually abundant species.
7 June 2013 (EPR = 13.7). Chl a concentration was again at a
moderate level, 4.2 lg L 1, with 39% in the <5 lm size fraction.
Diatom blooms were characterized by both high species
richness and abundance in June and July 2013. The diatom
bloom on 7 June 2013 (1,205,789 cells L 1) was in a similar
magnitude to the other June and July observations and
characterized by a common set of genera/species including
Chaetoceros (e.g. Ch. contortus and debilis), Asterionellopsis,
S. costatum, Pseudo-nitzschia and C. closterium. This gives an
example of the apparent mismatch between a seemingly ideal
food supply and a low EPR.
39
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
Table 4
Comparisons of diatom community composition by year (shown as abundance) and season (as rank). The species list was determined by similarity of percentage (SIMPER)
analysis (more details in Methods). Genus: A (Asterionellopsis); As (Asteromphalus); C (Cerataulina); Ch (Chaetoceros); Cylin (Cylindrotheca); D (Dactyliosolen); L (Leptocylindrus); P-n
(Pseudo-nitzschia); S (Skeletonema); T (Thalassiosira).
Taxa
Abundance (104 cells L
2011
A. glaciali
A. socialis
As. sarcophagus
C. pelagica
Ch. affinis
Ch. contortus
Ch. debilis
Ch. decipiens
Ch. didymus
Ch. laciniosus
Ch. lorenzianus
Ch. radicans
Ch. socialis
Ch. vanheurckii
Coscinodiscus
Cylin. closterium
D. fragilissimus
L. danicus
L. minimus
Navicula
Nitzschia
P-n deli/p-deli
P-n fraud/aust
P-n multi/pung
S. costatum
T. nitzschioides
T. nordenskioeldii
T. rotula
Thalassiosira
1
)
2012
0.8
Rank
2013
2014
8.7
0.9
Jan–Feb
Apr–May
Jun–Oct
4
6
4
15
7
11
13
5
0.2
0.1
0.4
14.6
13.1
17
0.2
0.5
16.8
0.1
5.1
0.1
5.2
0.9
0.6
6.5
3.4
0.5
0.1
0.7
0.3
0.2
0.2
2.5
3.8
0.6
4.1
0.9
4.9
1.8
3.3
0.5
0.5
0.4
0.6
0.4
2.5
0.4
2.1
28.1
0.2
29.7
0.3
0.8
2.1
10
10
3
2
1
4
12
9
3
5
3
6
12
11
1
2
14
7
2.4
1
2
9
8
8
0.1
1.3
26 Oct 2011 (EPR = 24.9). The Chl a value was very low, only
1.3 lg L 1 (62% for <5 lm fraction) and EPR was close to the
average. Diatom abundance was similarly low, 14,065 cells L 1,
whereas small dinoflagellates were more abundant
(23,670 cells L 1).
23 and 29 July 2013 (EPR = 35.6 and 61.7, respectively). A bloom
developed during these two sampling dates, with Chl a ranging
from 7.5 lg L 1 to 15.9 lg L 1 and <5 lm size fraction comprising 11% and 77%, respectively. Diatom abundances were exceptionally high (1.1 and 1.6 106 cells L 1). Dominance within the
diatom community was shared between Chaetoceros (61% and
44%, respectively) and Thalassiosira (24% and 44%, respectively).
Fig. 6. Relationships between egg production rate (EPR) and diatom species
richness during Jun to Aug (hyperbolic model, R2 = 0.32). Species richness used
here is the number of species with cell abundance (N) >104 cells L 1. Coefficient
a = 46.9 and b = 6.9.
In comparison, five dates in summer had extraordinarily high
EPRs and fell above of the upper 95% CI. These dates were in
2011 (17 Aug, 29 Sep and 26 Oct) and 2013 (23 and 29 July).
17 Aug 2011 (EPR = 30.9). Chl a value was very high, 17.3 lg L 1
(76% in the <5 lm fraction). Total diatom abundance was moderately high (571,849 cells L 1) with a 41% contribution from
Thalassiosira.
29 Sep 2011 (EPR = 48.6). Chl a value was low as 2.6 lg L 1 (65%
for <5 lm fraction) but EPR was high. Diatoms were dominant
(487,118 cells L 1) and Ch. debilis alone made up 83% of total
abundance.
Note that (Table 5) EPRs were high on days when Thalassiosira
were abundant during summer. Regression analysis (Fig. 7)
between EPR and Thalassiosira abundance showed a significant
hyperbolic relationship (n = 17, r = 0.64, p = 0.0057).
4. Discussion
4.1. Spawning of Calanus copepods
Multiple years of egg production experiment demonstrate that
the C. marshallae population off Oregon produces eggs from winter
through late summer. Eggs are produced in winter months soon
after the termination of diapause and mostly before the first phytoplankton bloom supporting the idea that there must be triggers
other than the bloom that act to awaken them from diapause
(Miller et al., 1991).
Spawning before the first bloom of the year, either in winter or
spring, is not an exclusive trait for C. marshallae. Many studies of
other Calanus species also found that eggs were produced before
40
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
Table 5
EPR (eggs female 1 day 1), diatom species richness (S), diatom total cell abundance (N, cells L 1) and the general amount (<104 or >104 cells L 1) of those diatom taxa that form
blooms during the summer upwelling season (Jun–Oct) in 2011–2014. S (N > 104): the number of species with abundance >104 cells L 1. Aster: Asterionellopsis; Chae: Chaetoceros;
Rhiz: Rhizosolenia + Dactyliosolen + Guinardia + Proboscia; Lept: Leptocylindrus; Pennate: Navicula + Nitzschia + Pleurosigma + Thalassionema; P-n: Pseudo-nitzschia; Thal: Thalassiosira. ‘‘ + ” means N < 104; ‘‘++” means N > 104.
Samples
S
S(N > 104)
N
EPR
Aster
Chae
Rhiz
Lept
Pennate
P-n
Thal
6/8/2011
7/6/2011
7/22/2011
7/27/2011
8/4/2011
8/17/2011
9/1/2011
9/13/11
9/29/11
10/26/11
7/20/2012
8/7/2012
6/7/2013
6/19/2013
7/9/2013
7/23/2013
7/29/2013
9/26/13
10/22/13
6/11/2014
7/22/2014
9
11
6
4
8
20
8
3
7
10
24
19
25
27
21
24
20
17
28
21
26
3
1
2
1
6
10
5
3
3
0
12
6
14
13
7
16
11
6
20
7
23
100,854
35,676
31,903
702,376
4,077,042
571,849
1,034,268
512,846
487,118
14,065
960,515
324,688
1,205,789
2,181,740
874,183
1,129,462
1,602,001
1,154,561
1,306,986
373,572
8,694,373
14
10
4
10
40
31
25
20
43
25
8
6
14
31
24
36
62
24
28
18
41
0
+
0
+
++
++
+
0
++
+
+
0
++
++
++
++
++
0
++
0
++
++
+
0
0
0
++
0
0
++
+
++
++
++
++
++
++
++
++
++
++
++
+
0
++
++
++
++
++
0
0
+
++
++
++
+
++
+
0
++
+
++
++
+
+
0
0
0
0
0
0
0
0
+
+
+
++
+
+
0
+
++
0
++
++
++
+
+
++
++
++
++
+
+
++
+
++
+
++
++
++
+
++
++
++
+
+
0
0
++
++
++
++
++
+
+
++
++
++
++
++
++
++
++
++
++
0
+
+
+
++
++
++
0
0
+
++
++
0
++
++
++
++
+
++
++
++
Fig. 7. Relationship (hyperbolic model, coefficients a = 40.6, b = 24794.9) between
egg production rate (EPR) and diatom genus Thalassiosira abundance (cells L 1).
the first bloom of the year, although the numbers of eggs were substantially lower than those observed during or post-blooms. As
examples, Plourde and Runge (1993) working on C. finmarchicus
in the Gulf of St. Lawrence reported EPR <10 pre-bloom, 22–82
during the bloom and 30–50 post-bloom. Niehoff et al. (1999) for
C. finmarchicus in the Norwegian Sea reported EPR of 8
pre-bloom and 44 during the spring bloom. Gislason and
Astthorsson (2000) reported a maximum EPR for C. finmarchicus
of 7 pre-bloom and 46 during the bloom in waters off Iceland. A
similar result for C. glacialis (Melle and Skjoldal, 1998; Niehoff
and Hirche, 2005) was found in a Norwegian fjord (see Table 2 in
Niehoff and Hirche, 2005). Stenevik et al. (2007) reported for
C. finmarchicus in the Norwegian Sea EPR of 10, 22 and 18 with
pre-, during and post-bloom conditions, respectively. Madsen
et al. (2008) found both C. finmarchicus and C. glacialis spawned
before the spring bloom in Disco Bay Greenland, as did Runge
et al. (2006) for C. finmarchicus on Georges Bank, U.S. Conversely,
Head et al. (2013) found that EPRs of C. finmarchicus in the central
Labrador Sea were not different under pre-, during, and
post-bloom conditions. Most of these observations cited for other
Calanus species are in stark contrast to our work off Oregon where
EPRs were often higher in winter before any blooms and lower during summer when large diatom blooms were frequent.
As for Calanus species in the Pacific Ocean, Baier and Napp
(2003) reported that C. marshallae in the Bering Sea also spawned
well before the spring bloom, as early as February based on
back-calculated temperature-dependent development rates of the
age-structure observed in April and May. The same is true for C.
pacificus in Dabob Bay, WA (Leising et al., 2005; Pierson et al.,
2005), and for C. pacificus in the coastal waters off Oregon (Peterson, unpublished data). Spawning by C. chilensis in the southern/
central Chile (Hidalgo and Escribano, 2007) is seasonal whereas
C. chilensis spawn year round in waters off northern Chile
(Hidalgo and Escribano, 2008). C. sinicus can spawn year around
in the Yellow Sea, P.R. China, although most females do not
produce eggs during summer months but go through
‘over-summering’ at depth because temperature of the upper
mixed layer is very high, exceeding 18 °C (Huo et al., 2008; Kang
et al., 2011; Wang et al., 2009; Zhang et al., 2005). Uye and
Murase (1997) reported maximum EPRs of 22–24 for C. sinicus
from coastal waters off Japan (Seto Inland Sea) in spring, similar
to the rates reported by the above cited studies in the Yellow Sea.
4.2. EPR and phytoplankton concentrations
Significant functional relationships were found between EPR
and total Chl a concentration in our study. Our past work in June
1996 and July–September 1997 also found strong correlations
between EPR and Chl a (Gómez-Gutiérrez and Peterson, 1999;
Peterson et al., 2002). This result is common to studies of other
species in the genus of Calanus. However, the uniqueness of our
findings is that we noted differences in season-specific functional
response of C. marshallae EPR to phytoplankton availability. Hyperbolic models provided the best fit for both winter–spring and summer and the parameters from the models inform clearly different
biological behaviors and are consistent with in situ observations.
The very high EPRs in winter and spring were not simply a function
of autotrophic phytoplankton as a food source; rather, they were
likely the result of multiple feeding strategies that female C. marshallae use for producing eggs. In summer, the half-saturation constant (Chl a = 2.6 lg L 1) for reaching the maximum EPR was much
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
lower than the magnitude of summer blooms (10–20 lg L 1)
suggesting the amount of phytoplankton (mostly diatoms) was
not limiting egg production and instead other factors (prey types
or environment) caused the high variability in EPR. The significant
correlation between EPR and Chl a were obscured when the data
from all seasons were combined for the test (r = 0.17, p = 0.2),
which again highlights the different functional response in egg
production at different times of the year.
The significance of EPRs for C. marshallae responding to the
abundance of different microplankton functional groups also differed by season: EPRs in winter/spring were best correlated with
ciliate abundance, whereas in summer were best correlated with
diatom abundance. Similar findings were reported by Vargas
et al. (2006) for the copepods Acartia tonsa and Centropages
brachiatus from the coastal upwelling zone off Dichato, Chile where
copepods fed on dinoflagellates and ciliates in winter but diatoms
in summer.
Some of our winter EPRs were the highest in a given year and
occurred before the winter bloom. We thus hypothesize that in winter energetic requirements for egg production and embryo development may come from a combination of lipid reserves and from
feeding omnivorously on both phytoplankton and microzooplankton. At this time of the year, EPR ranged from 4 to 68.5 over a range
of diatom abundance of 0–180,000 cells L 1 (mean 28,650; median
3002 cells L 1) and ciliate abundance of 343–13,379 cells L 1 (mean
3345; median 4328 cells L 1). We attribute the extraordinary EPR in
winter 2014 (that were nearly double that in the other winters
and summers) to the abundance of ciliates (naked ciliates,
11,263 cells L 1, Table 3) and dinoflagellates (mostly small dinoflagellates, 28,644 cells L 1). Jonasdottir et al. (2002) also reported
unusually high clutch size of C. finmarchicus (75–110 eggs per
female) in April when Chl a concentrations were below 1 lg L 1;
however, they did not report ciliate/dinoflagellate information.
There are only a few studies about relationships between Calanus egg production rate and concentration of taxa/species of
microplankton, but most of them, such as Ohman and Runge
(1994) for C. finmarchicus in the Gulf of St. Lawrence, reported similarly that EPRs were high when feeding on ciliates and/or dinoflagellates under post-spring bloom conditions. Another study by
Irigoien et al. (2000a) in a 7-year study of egg production by
C. helgolandicus in the English Channel at Station L4 off Plymouth
showed that flagellates and ciliates were the most important
factors explaining variations in egg production. Further evidence
that ciliates are important prey comes from feeding studies – the
Nejstgaard et al. (2001) mesocosm experiments showed that
C. helgolandicus generally preferred non-diatom foods such as ciliates and metazoans. Jonasdottir et al. (2011), in another mesocosm
study, reported significant correlations between egg production of
C. finmarchicus and ciliate biomass. Moreover, Jonasdottir
and Koski (2011) showed that EPR of C. finmarchicus and
C. helgolandicus from the North Sea in July and August were best
explained by the abundance of dinoflagellates, flagellates and
ciliates. Finally, Fessenden and Cowles (1994) who conducted feeding experiments on copepods collected from the same station off
Newport, Oregon and as our work, showed that during summer
diatom blooms (when Chl a reached 45 lg L 1), C. pacificus fed on
diatoms but switched to ciliates in winter.
Our results support the importance of diatom diets to
C. marshallae egg production during summer upwelling months.
This has been acknowledged by many studies for different species.
For example, Irigoien et al. (2000b) measured both EPRs and ingestion rates of C. helgolandicus on various phytoplankton taxa and his
results showed little selective feeding but a slight preference for
diatoms. Jonasdottir et al. (2002) compared egg production of C.
finmarchicus to quality of phytoplankton (indexed through fatty
acid analysis) in shelf waters off Iceland and found that diatom
41
fatty acid markers were correlated with EPRs. Vargas et al.
(2010) reached the same conclusion for copepods from the upwelling zone off Dichato, Chile. Ceballos and Alvarez-Marques (2006)
also found significant correlations between diatom concentration
and egg production of both C. helgolandicus and Calanoides carinatus, in the coastal upwelling zone off northern Spain (Cantabrian
Sea). EPR of C. pacificus in Dabob Bay, WA was significantly correlated with diatom concentration in winter and spring (Pierson
et al., 2005; Leising et al., 2005). The study by Ianora et al.
(2015) observed higher in situ EPRs of Acartia clausi and
C. helgolandicus in the years when diatoms were more productive
in Adriatic Sea.
4.3. EPR and phytoplankton community structure
We had hypothesized that the patterns of phytoplankton community structure from traditional cluster and ordination analysis
would explain the variation in EPR due to the combined information on species composition and abundance, functional groups
and species richness. However, our results did not show any
covariance between the five significantly different community
types and EPR values (as compared in Fig. 3). On the other hand,
species richness alone seemed to inform better variation in EPR
which supports the hypothesis presented by others (e.g., Irigoien
et al., 2000b; Leising et al., 2005; Paffenhofer et al., 2005 and reference therein) that mono-specific blooms (lower species diversity)
may result in a decline in EPR. In contrast, a mixture of microplankton species may provide a more balanced diet for copepods (Poulet
et al., 2006; Uye, 1996; Vehmaa et al., 2011).
4.4. Why were there some cases of exceptionally low EPR in summer?
Average EPRs were lower in summer as compared to spring or
winter. Our analyses of individual cases in summer (see Section 3.7)
provide the following empirical understanding. First, in the trivial
case, when both Chl a and diatom concentration were low, EPRs
were low; second, mono-species blooms of certain diatoms and
dinoflagellates were associated with low EPR; third, high abundance of Thalassiosira along with a diverse set of other abundant
diatoms were associated with high EPRs. The second and third
points are consistent with positive association of higher species
richness with higher EPR (Fig. 6). Limited evidence was shown
about the possibility of detrimental effects caused by monospecies blooms of certain phytoplankton species (as in 2 of 21
experiments). Recall cases on both 27 July 2011 and 20 July 2012,
the dominant diatom was D. fragilissimus whereas EPRs were exceptionally low. The same observation was made by Ceballos and
Álvarez-Marqués (2006) that EPRs were decreased during a bloom
of D. fragilissimus for both C. helgolandicus and Calanoides carinatus
in July 2002. Further, the bloom observed by us on 7 Aug 2012
showed that an unusually high concentration of the silicoflagellate
D. speculum was associated with very low EPR, and this too has been
found previously by Nejstgaard et al. (2001) in their mesocosm
experiments with C. helgolandicus. The dinoflagellate Gyrodinium
aureleum was shown to have a negative influence on egg production
of C. helgolandicus (Irigoien et al., 2000a) as was the haptophyte
Phaeocystis sp. (Bautista et al., 1994) on egg production of the same
species. Others have shown reduced EPRs during dense diatom
blooms but either species were not enumerated or there were no
dominant species that could be associated with reduced EPR
(Nejstgaard et al., 2001; Paffenhofer, 2002; Poulet et al., 2007,
2006). Pierson et al. (2005) noted that EPRs of C. pacificus in Dabob
Bay, WA were reduced during a bloom of Thalassiosira; however, we
did not detect such negative effects (Fig. 7) by this species. Some
studies did not report negative effects from mono-species blooms
on egg production: these include blooms of Phaeocystis (Irigoien
42
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
et al., 2000b; Jonasdottir et al., 2011) and Skeletonema (Irigoien
et al., 2005).
Many factors are suspected for the depressed EPR during diatom blooms, such as growth rate and phase of the bloom/taxa during a bloom, fatty acid composition and content of diatoms, ratios
of protein: carbohydrate, toxin effects associated with the presence
of certain aldehydes, etc. and each of these factors have been
reviewed succinctly in Paffenhofer et al. (2005) thus need not be
restated here. Beyond the potential effects of the factors related
to food quality, there are also response differences by the copepods
themselves, for example, their susceptibility to toxins and detoxification capability (Wichard et al., 2008).
Another potential reason for the reduced EPR is that during the
summer upwelling season in the northern California Current the
blooms are often caused by long-chain diatom species easily
extending beyond 1 mm in length, and those species are from
the genera Chatoceros, Thalassiosira, Leptocylindrus, Pseudonitzschia, Skeletonema, Guinardia, etc. We speculate that these species may be too large to be handled easily and thus would be less
actively selected by copepods and is based on our observations
that when blooms of large-cell diatoms were present, EPR were
low (e.g. 7 June 2013). Studies by Peterson et al. (2002) and
Vargas et al. (2007) both argued for low efficiency of primary
production transfer through the classical diatom food chain in
the productive coastal upwelling system and this may be partially
related to inedible diatom species.
4.5. Potential recruitment rates (eggs day
1
m 2)
Ceballos and Alvarez-Marques (2006) may have been the first to
coin the term ‘‘potential reproduction rate” (PRR) for the calculation of in situ female abundance egg production rate. In our
study, the highest PRR was found in 2013 whereas PRRs were very
low throughout 2014 and as well in 2012 (Fig. 8). When shown as
climatology, rates were highest in spring and lower during the
summer
upwelling
season.
Maximum
rates
were
174,977 eggs day 1 m 2 (the same units are used hereafter) with
an average of 30,433. No recruitment was apparent after August
of any year, because there were no females in the quantitative vertical towed net since most of them had entered diapause by that
time (although in 2011 and 2013, there were enough females in
the Bongo net tow in fall and winter to be used for the EPR
incubations).
Niehoff et al. (1999) reported nearly the same result of PRR for
C. finmarchicus from the North Atlantic at Weathership M – up to
200,000 but with an average of 34,187 pre-spring bloom and
34,855 during the bloom. Stenevik et al. (2007) working on the
same species in the Norwegian Sea as part of the ESSAS study
reported an average PRR of 146,926 before the spring bloom period
and 220,742 during the spring bloom. Gislason and Astthorsson
(2000) reported much lower PRRs, noting a maximum of 16,000
for C. finmarchicus in oceanic waters but only 1000 in shelf
waters. Harris et al. (2000) reported a maximum of 180,000 for
C. finmarchicus in the Norwegian Sea and an average of about
10,000 for C. helgolandicus from the English Channel (a coastal station at a similar water depth as Newport Line). Bonnet et al. (2005)
compared data on C. helgolandicus from Stonehaven (North Sea,
50 m depth), English Channel (Plymouth, 55 m depth) and the Cantabrian Sea (N. Spain). Maximum values were 256,000 (Cantabrian
Sea), 35,146 (English Channel) and 11,764 (Stonehaven). Ceballos
and Alvarez-Marques (2006) reported maximum PRR of 56,140
for C. helgolandicus and 57,444 for Calanoides carinatus in coastal
waters off Spain. Jonasdottir and Koski (2011) reported similar
maxima for Calanus helgolandicus in the North Sea (Dogger Bank)
during summer with a range of 443–49,355 and for C. finmarchicus,
162–49,954.
Fig. 8. Interannual and seasonal changes of potential recruitment rate of Calanus
marshallae during 2011–2014.
The PRR calculation may be considered as estimate of potential
‘‘recruitment rate”, but obviously do not account for egg mortality
(Ohman et al., 2002; Peterson and Kimmerer, 1994) nor for variable
egg hatching or naupliar survival rates. However, the PRR calculation does illustrate the total number of egg produced by all females
on a given day thus is an estimate of secondary production by the
‘population’, which is especially relevant because even if the
females in an incubation produce high numbers of eggs, if there
are few-to-no females in the ocean, then the data from incubations
must be valued differently. In this regard, we have clearly shown
that there was no recruitment after August in any of the four years
of data reported here, a fact that adds value to the calculation of PRR.
4.6. Laboratory estimates of EPR compared to in situ results
In an extensive set of laboratory experiments, Peterson (1988)
estimated the functional response of feeding rates, fecal pellet production rates and egg production rates by female C. marshallae fed
a wide range of concentrations of T. weissflogii. The maximum EPR
estimated from an Ivlev model was only 23.5. This is similar to (for
some cases) but mostly lower than values observed in this study
during summer, and far less than rates observed in winter (e.g.,
an EPR of 53.4 in 2014 and four-year mean of 32.5) and spring
(EPR of 44.7 in 2013 and four-year mean of 40.2). The reason for
these large differences cannot be known but we are concerned that
T. weissflogii, being an easily-grown ‘laboratory weed’, was not
nutritionally adequate during those experiments despite every
attempt to maintain cells in log-growth phase, as described in
Peterson (1988). We suggest that some zooplanktologists may
need to re-think past lab work which used easily cultured diatoms
(‘weeds’) and re-do important rate measurements, especially if
reported rates are less than rates known from in situ incubations.
This is especially true for C. marshallae development time for individual life stages from N3 to adult – in the experiments reported by
Peterson (1986), the C5 stage required several weeks to mature;
moreover, only females were produced in those experiments.
W.T. Peterson, X. Du / Progress in Oceanography 138 (2015) 32–44
43
4.7. Limitation of our approach
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5. Conclusions
We have shown that EPRs were highest in spring and winter
and lowest during the summer upwelling season. Significant functional relationships were shown between EPR and Chl a, but only
when the dates were parsed into winter–spring and summer. High
egg production in winter and spring were attributed to a greater
abundance of ciliates and likely dinoflagellates at that time. Variations in EPR during summer remain enigmatic in that on some
occasions, extremely low rates were measured whereas at other
times, extremely high rates were measured; based on Chl a concentrations, EPR should not have been food limited. We suggested
that during certain mono-specific diatom blooms, EPRs were
depressed whereas when diatom species richness was high during
some blooms in summer, EPRs were high. Since we did not conduct
copepod feeding experiments on natural particle assemblages, we
do not know if ciliates continue to contribute as an important component of copepod diets in summer, but clearly, diatom blooms are
important to sustain high EPRs although they do not always result
in high EPRs. Finally, Vargas et al. (2006) remarked ‘‘that the classical marine food web model does not apply to some coastal
upwelling systems”. Further, Calbet (2008) reminds us that the
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Acknowledgements
We thank C. Tracy Shaw, Jay Peterson (JP), Jennifer Fisher (JF) and
the captains of the R/V ELAKHA for collecting all the samples for this
study along the Newport Hydrographic Line. Jay and Jennifer
conducted many of the egg production incubation experiments as
well. JP and JF provided comments on various earlier drafts of this
manuscript. Post-doctoral support for X. Du was provided by a grant
from the NOAA-MERHAB program (NA07NOS4780195). Funding for
collection of zooplankton samples from 2011 onwards was provided
by the NOAA Stock Assessment Improvement Program, NOAA Fisheries and the Environment Program, as well as residual funds from
the U.S. GLOBEC/Synthesis program.
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