Interannual variations in vital rates of copepods and euphausiids during the RISE study 2004–2006



[1] The River Influences on Shelf Ecosystems (RISE) program investigated the role of the Columbia River plume in enhancing productivity in the upwelling zone off Washington during four cruises from 2004 to 2006. Measurements of growth rates and brood sizes of euphausiids and egg production rates of copepods were used as indices of secondary production to determine whether these rates differed (1) among cruises as a function of differences in upwelling strength and (2) with latitude, both within the RISE study area and between the coastal waters of Washington and Oregon. Euphausia pacifica growth rates were significantly higher during June 2006 than during July 2004 and June 2005 but not significantly different between the RISE study area and Newport Hydrographic (NH) Line, Oregon. Euphausiid brood sizes were significantly higher during August 2005 than during any other cruise for both E. pacifica and Thysanoessa spinifera; our experiments did not indicate that brood sizes were higher in the northern part of the RISE study region. E. pacifica broods were larger for NH than RISE, but T. spinifera broods were not. Significant differences in egg production rates (EPRs) were found among cruises for both Calanus pacificus and C. marshallae, with higher EPRs during August 2005. EPRs on other cruises were less than half the maximum rates known for these species. EPRs of C. marshallae were similar between RISE and NH; C. pacificus EPRs were significantly higher (lower) in the RISE region in 2005 (2006). Interannual differences in ocean conditions affected zooplankton production more strongly than differences in latitude.

1. Introduction

[2] The River Influences on Shelf Ecosystems (RISE) program focused on the influence of the Columbia River plume on regional productivity of coastal waters off Washington and Oregon. One goal of the program was to explain observations that phytoplankton biomass is usually higher off Washington than off of Oregon [Landry and Hickey, 1989; Strub et al., 1990; Thomas and Strub, 1990; Thomas and Weatherbee, 2006; Ware and Thomson, 2005]. The greater phytoplankton biomass in shelf waters off Washington seems counterintuitive because upwelling winds are weaker there (∼48°N) compared to Oregon (∼45°N) by a factor of about 25%, on the basis of the Bakun upwelling index ( Moreover, the average upwelling season off Washington is shorter by about 1 month (May–September) than off Oregon (April–September) ( However, nutrient concentrations are similar in both areas during the upwelling season, suggesting that phytoplankton biomass should also be similar. Modeling studies suggest that higher summer phytoplankton biomass off Washington occurs because the continental shelf is wider there than it is off of Oregon; a wider shelf results in longer retention time of water on the shelf, and thus lower rates of cross-shelf transport and loss during the summer upwelling season [Banas et al., 2009]. Another factor that may contribute to higher phytoplankton biomass off Washington is that the Columbia River is a source of iron to the Washington coast during winter months when the river flows are high and the plume is directed toward the north [Chase et al., 2006]. During upwelling, as deep, nutrient-rich water moves shoreward, it entrains iron from the sediment-water interface and carries it to the surface, thus fueling large phytoplankton blooms [Lohan and Bruland, 2006].

[3] Ware and Thomson [2005] highlighted the need for a better understanding of productivity associated with the Columbia River plume region and Washington shelf. They studied latitudinal variations in phytoplankton biomass in relation to fish yields throughout the entire California Current and showed that phytoplankton biomass was highest off Washington and southern British Columbia, and also that fish biomass (particularly Pacific whiting, Merluccius productus) was highest in this same region, suggesting strong trophic coupling and bottom-up control of fish production. Along the same lines, juvenile coho and Chinook salmon (Oncorhyncus kisutch and O. tshawytsha) are more abundant off Washington than Oregon [Bi et al., 2006], suggesting that there are differences in the ecosystem dynamics of the Washington shelf which result in prime fish habitat off Washington.

[4] Our zooplankton research during the RISE program focused on two goals. One was to determine the fine- and broad-scale distribution and abundance of zooplankton in relation to fronts associated with the Columbia River plume using data from a Laser Optical Plankton Counter [Peterson and Peterson, 2008, 2009]. The other goal was to determine if there were regional differences in euphausiid and copepod production in shelf waters off Washington and Oregon. Toward this end, we measured vital rates of several zooplankters as indices of secondary production. Two species of euphausiids dominate shelf and slope waters of the northern California Current, Euphausia pacifica and Thysanoessa spinifera. E. pacifica is a more oceanic species and T. spinifera tends to be found on the shelf [Gómez-Gutiérrez et al., 2005]. Two species of Calanus commonly occur in shelf and slope waters, with their relative abundance depending on environmental conditions. Calanus marshallae is the dominant species during cold summers. C. pacificus is more common during winters, but is the dominant form during warm summers [Peterson and Keister, 2003]. In this paper we describe results of our experiments conducted on the four RISE cruises and test whether there were any latitudinal differences in these vital rates within the RISE study region and between the coastal waters off Washington and Oregon, and whether there were differences among cruises as a function of differences in upwelling strength.

2. Materials and Methods

2.1. Environmental Variables

[5] Interannual variability in environmental conditions during the RISE cruises was described from (1) sea surface temperature data from NOAA weather buoys (buoys 46050 moored off Newport, Oregon, latitude 44°38′N and 46041 moored off Aberdeen, Washington, 47°20′N); (2) monthly values of the Pacific Decadal Oscillation (PDO) ( and the multivariate El Niño–Southern Oscillation (ENSO) index (MEI) (; (3) the date of spring transition (; and (4) the cumulative sums of the daily values of upwelling at 48°N, in units of m3 of water upwelled s−1 100 m−1 of coastline, calculated using a climatology over 1990–2007 (

[6] As an index of phytoplankton biomass, we include surface chlorophyll data averaged over each cruise for stations from the continental shelf (to offshore depths of 150 m). Water samples were filtered onto GF/F filters and extracted in 90% acetone for 24 h at −20°C [Kudela et al., 2006]. Samples were run at sea on a Turner 10-AU fluorometer using the nonacidification method [Welschmeyer, 1994].

2.2. Collection of Zooplankton for Experiments

[7] All RISE cruises reported here were conducted aboard the R/V Wecoma. Euphausiids and copepods were collected during all RISE cruises for use in growth and egg production experiments (Table 1). Euphausiids were only collected at night (when they are typically found near the surface) using either a 75 cm diameter ring net or 70 cm diameter Bongo nets. All frames were fitted with black 333 μm mesh nets with nonfiltering cod ends. Tow depths were to ∼20 m. The catches were diluted into coolers filled with surface seawater from the station being sampled and incubations were set up within a few minutes of collection. Copepods were collected from the same tows as euphausiids, and also occasionally from daylight tows. Sampling locations for zooplankton experiments were similar for all four RISE cruises (Figure 1).

Figure 1.

Chart showing locations of stations where zooplankton were sampled during each of the four RISE cruises.

Table 1. Summary of Cruise Dates and Euphausiid Live Experiment Work for All RISE Cruises
CruiseZooplankton Start DateZooplankton End DateDays at Sea for Zooplankton TeamAdult E. pacifica Incubated for Instantaneous Growth Rate ExperimentsE. pacifica Incubated for Brood Size MeasurementT. spinifera Incubated for Brood Size MeasurementC. marshallae Incubated for Egg ProductionC. pacificus Incubated for Egg Production
RISE 18 Jul 200428 Jul 20042090133529218
RISE 26 Jun 200520 Jun 2005146051935318
RISE 34 Aug 200513 Aug 200590793618364
RISE 41 Jun 200613 Jun 200612903300483

[8] We conducted more incubation experiments on copepods than on euphausiids (Table 1) because of differences in their distribution patterns. The copepod species of interest, Calanus marshallae and C. pacificus, are broadly distributed in shelf and slope waters so we sampled at a wide variety of station depths, from the nearshore zone out to beyond the shelf break, allowing us to test for differences in egg production as a function of station depth and latitude. Euphausiids in general have a patchier distribution than copepods. Of the two species we studied, Euphausia pacifica is the more abundant and is usually found only at or near the shelf break, whereas Thysanoessa spinifera are less common and are generally restricted to shelf waters. As a consequence of these distribution patterns it was not feasible to test for differences in euphausiid vital rates in relation to station depth.

2.3. Euphausiid Growth Rates

[9] Euphausiid growth rate experiments were conducted during RISE 1, RISE 2, and RISE 4. No growth experiments were conducted during RISE 3 because we encountered so many gravid females during this cruise that we devoted all of our euphausiid experimental effort and incubator space to measuring their egg production. All euphausiid growth data are for Euphausia pacifica because Thysanoessa spinifera were not collected in sufficient numbers for these experiments.

[10] Growth rate experiments were conducted using the instantaneous growth rate method [Nicol et al., 1992; Quetin and Ross, 1991]. For each experiment, healthy, actively swimming animals with no visible damage were gently removed from the diluted catch and placed in a container of 200 μm filtered seawater. From this container, 30 individuals were randomly selected and each was placed in a separate 500 mL jar filled with 200 μm filtered seawater. The animals were incubated in the dark at 10.5°C. Experiments lasted 48 h and were checked at 12 h intervals for molts. When an animal molted, it was preserved along with its molt in 5% formalin. At the end of each experiment all nonmolters were preserved together in 5% formalin. Animals that died during the experiment were not included in any calculations.

[11] All measurements were conducted by the same person (C.T.S.) to minimize bias. Telson lengths of the preserved molt and animal were measured to determine the premolt and postmolt lengths of the euphausiid. The telson lengths of the animal and molt were converted to total length using the following equation derived from measurements in our laboratory:

equation image

The premolt total length was subtracted from the postmolt total length to determine the growth increment (change in total length in mm).

[12] Molting rate is defined as the percentage of animals molting d−1. The inverse of the molting rate (percentage d−1) is the intermolt period (IMP) in days. IMP was calculated as in the work by Tarling et al. [2006]:

equation image

where N is the number of E. pacifica incubated (less those that died during the experiment), including the number of E. pacifica that molted, m is the number of E. pacifica that molted and d is the length of the incubation in days (2 days for our experiments). We did not calculate an IMP from experiments with <15 surviving E. pacifica or <3 molts because the number of individuals and/or molts was too small to yield robust results.

[13] Growth rate (G) (mm d−1) of each individual Euphausia pacifica that molted was calculated by dividing the growth increment (mm) by the intermolt period (days):

equation image

2.4. Euphausiid Egg Production

[14] Gravid females that were ready to spawn were easily recognized by the distinct coloration of their ovaries, (purple for Euphausia pacifica and blue for Thysanoessa spinifera) just under the pericardial area of the cephalothorax [Gómez-Gutiérrez, 2002, 2003; Ross et al., 1982; Summers, 1993]. Previous work in our laboratory showed that females with colored ovaries generally spawned completely within the first 12 h of an incubation [Gómez-Gutiérrez et al., 2007]. To set up an incubation experiment, we gently removed gravid female euphausiids from the diluted plankton sample and placed each individual in a plastic incubation bottle filled with 200 μm filtered surface seawater. E. pacifica females were incubated in 1 L bottles while T. spinifera females were incubated in 500 mL bottles. T. spinifera eggs tend to adhere to incubation bottles [Gómez-Gutiérrez et al., 2007]; therefore, we used 500 mL jars that fit between the stage and the ocular of the dissecting microscope, allowing us to count the eggs without removing them from the bottles. This minimized errors caused by trying to remove sticky eggs from jars or sieves in order to count them. Bottles were incubated in the dark at a constant temperature of 10.5°C. All incubations lasted 48 h and bottles were monitored every 12 h. At each 12 h check point all bottles were examined and any eggs were counted with the aid of a dissecting microscope. At the end of an experiment, the females were measured from the posterior part of the eye to the tip of the telson (total length, mm) and any eggs remaining in the incubation bottle were counted. Brood size was defined as the number of eggs produced female−1 (eggs brood−1 female−1) during the 48 h of incubation. Gravid females that did not spawn during an experiment were not included in our analyses.

2.5. Copepod Egg Production

[15] Adult female copepods were picked from the live tows and sorted individually into 50 mL Nalgene jars filled with 64 μm filtered seawater. Jars were incubated in the dark at 10.5°C. The jars were examined after 24 h and eggs were counted with the aid of a binocular microscope, at 25X. No provision was made to guard against cannibalism because it is believed to be low in Calanus marshallae and Calanus pacificus [Peterson, 1988]. We intended to compare egg production by the two Calanus species from each of the four cruises, but females of both species were not present on all cruises. Ordinarily, C. marshallae, a “cold water” neritic species is common in shelf waters and C. pacificus, a “warm water” oceanic species is common in outer shelf and slope waters off Oregon and Washington. However, because of unusual ocean conditions (described later) we incubated only 18 female C. pacificus (but 283 C. marshallae) on RISE 1, and 481 C. pacificus (but zero C. marshallae) on RISE 4. Table 1 shows the total number of individuals incubated per cruise.

2.6. Statistical Analyses

[16] We used ANOVA (PROC GLM SAS 9.1) to test the hypothesis that euphausiid growth rates, euphausiid brood sizes, and copepod egg production rates were the same among the RISE cruises. This method was also used to test the hypothesis that euphausiid growth rates and brood sizes were the same in both the RISE (near the Columbia River) and Newport Hydrographic (NH) Line (Oregon) study areas.

[17] To test the hypothesis that euphausiid brood sizes did not vary with latitude within the RISE study area, both overall and for each cruise, we used PROC GLM with the following model: Brood size = Latitude + Latitude × Cruise. If the coefficient is significant, that indicates that there is a difference with latitude. If the interaction term between latitude and cruise is significant, it suggests that there is a difference among cruises. The hypothesis that copepod egg production is a function of depth and latitude was tested using a similar model: Egg production = Depth + Latitude + Depth × Cruise + Latitude × Cruise. To test whether the length of spawning euphausiid females had an effect on their brood sizes, we calculated a brood size to total length ratio (BS:TL) for each cruise and used a t test to compare among cruises. Each RISE cruise was also compared to data from the NH Line, using a climatology of summer (June–August) brood size data (E. pacifica broods n = 176, T. spinifera broods n = 102) from 2001 to 2007 as a baseline. Differences in copepod egg production rates among the four cruises were compared using t tests. We also tested for potential differences in egg production between the RISE study area and the NH line, using as a baseline all incubations made between June and August of 2004–2006 from the NH line, a total of 1264 female C. pacificus and 346 female C. marshallae. We compared egg production rates on each RISE cruise to the NH 2004–2006 summer climatology.

3. Results

3.1. Summary and Comparison of RISE Cruises

3.1.1. Environmental Conditions

[18] The climatological date for the start of the upwelling season at 48°N is 26 April. The climatological average rate of upwelling is about 16 units (units are m3 of water upwelled s−1 100 m−1 of coastline d−1) in May and June, increases to 38 units in July, and then declines to about 12 units d−1 in August–September (Figure 2). During the RISE study (2004–2006), upwelling was relatively weak during the summer of 2004, averaging 18.4 units d−1 from 19 May through 23 July (during RISE 1) and 18.0 units d−1 from 24 July to 2 September. In 2005, upwelling was again weak, 14.5 units d−1 through mid-July (during RISE 2), then the winds became strong and produced 49 units d−1 of upwelling from 13 July to 9 August (during RISE 3). Upwelling was also strong in 2006 (45.2 units d−1) from 17 June to 31 August, however before RISE 4 (1–13 June) there was either weak upwelling or downwelling prevailed (Figure 2).

Figure 2.

Cumulative upwelling averaged for 1990–2007 (climatology) and for years in which RISE cruises took place: 2004, 2005, and 2006. Units are m3 of water upwelled s−1 100 m−1 d−1 of coastline. Short thick vertical black bars show the time span of each RISE cruise. Here cumsum indicates cumulative sum.

[19] Differences in the relative strength of the upwelling among years are evident in the SST anomalies from both NOAA buoys (Table 2a). Monthly averaged SSTs were more than 1°C above average during RISE 1 and 2, 0.7°C below average during RISE 3 (at Newport) and about 0.4°C above average for RISE 4. (Table 2a).

Table 2a. Values of Sea Surface Temperature Anomalies at NOAAa
YearBuoy 46050Buoy 46041PDOMEI
  • a

    Buoy 46050 is off Newport, Oregon; buoy 46041 is off Aberdeen, Washington. Values of the Pacific Decadal Oscillation (PDO) and multivariate ENSO index (MEI) are averaged for the three summer months in each year 2004–2006. ND, no data.

Table 2b. Dates of Sustained Upwelling and Mean Upwelling Rate for Each Year of the RISE Studya
YearUpwelling Bout 1Upwelling Bout 1 UnitsUpwelling Bout 2Upwelling Bout 2 UnitsUpwelling Bout 3Upwelling Bout 3 Units
  • a

    Mean upwelling rate was estimated from the slope of the line on the basis of the value of the upwelling index at the indicated time points and total number of days per upwelling bout. Units of upwelling are m3 of water upwelled s−1 100 m−1 d−1 of coastline.

200419 May to 23 Jul18.424 Jul to 2 Sep18.0  
200523 May to 2 Jul14.513 Jul to 9 Aug49.29 Aug to 5 Oct19.8
200617 Jun to 31 Aug45.2    

[20] Large-scale indices of climate conditions such as the Pacific Decadal Oscillation and the multivariate ENSO index had been in positive (warm) phase since autumn 2002 and remained so until 2007 (Figure 3 and Thus, all four RISE cruises took place during a 5 year period of warm ocean conditions. There was relatively weak upwelling during RISE 1 and 2, strong upwelling during RISE 3, and no upwelling during RISE 4, giving contrasting environmental conditions during the study period (Table 2b).

Figure 3.

Pacific Decadal Oscillation (PDO) and sea surface temperature time series from NOAA buoy 46050 located 20 miles off Newport, Oregon.

[21] Mean chlorophyll a concentrations (Table 3a) were relatively high on RISE 1 and RISE 3 (∼8 μg L−1) but low on RISE 2 and 4 (2.9 and 1.9 μg L−1, respectively). Similar species of diatoms and nondiatoms were present in the phytoplankton assemblages during all RISE cruises, but abundances varied among cruises [Frame and Lessard, 2009, Tables 2 and 3 and Figure 2].

Table 3a. Mean Surface Chlorophyll a Concentrations and Average Copepod Egg Production Rates With 95% Confidence Intervals and Average Copepod Egg Production Rates Measured off Newport in June–August of 2004–2007 Compared to the Grand Mean for All RISE Cruises Combineda
 ChlorophyllCalanus pacificusCalanus marshallae
Mean95% CIMeann95% CIMeann95% CI
  • a

    CI, confidence interval.

RISE 1 (Jul)7.60.7212.7186.4713.72831.78
RISE 2 (Jun)2.90.2521.83321.9914.2403.97
RISE 3 (Aug)8.01.0831.93632.9332.9236.60
RISE 4 (Jun)1.90.388.44811.33---
NH grand mean  16.01763.0521.13161.94
RISE grand mean  19.512601.2915.03461.65
Different?  Not = 1.86p < 0.06Yest = 4.74p < 0.0001

3.1.2. Euphausiid Growth Rates

[22] Growth rates of individual adult Euphausia pacifica were measured on RISE 1, RISE 2, and RISE 4. The number of euphausiids incubated varied between cruises (Table 1), depending on the number of euphausiids collected and the availability of incubator space. The size range of euphausiids in experiments was similar for RISE 1 (12–20 mm) and RISE 4 (12–21 mm) with euphausiids incubated during RISE 2 being slightly smaller (10–18 mm) (Figure 4a). Intermolt period (IMP) for experiments with at least three molters and 15 survivors ranged from 6 to 15 days, with an average of 9.6 days for all cruises.

Figure 4.

Euphausiid total length versus (a) Euphausia pacifica growth, (b) E. pacifica brood sizes, and (c) Thysanoessa spinifera brood sizes on RISE cruises. Growth rates were not measured during RISE 3 because of limited incubator space (Figure 4a). No gravid T. spinifera were found during RISE 4 (Figure 4c).

[23] Individual growth rates were variable within and among cruises (Figure 4a). Growth rates ranged from −0.07 to +0.06 mm d−1 during RISE 1, −0.03 to +0.06 mm d−1 during RISE 2, and −0.06 to +0.14 mm d−1 during RISE 4 (Figure 4a). RISE 1 had the highest frequency of negative or zero growth (6 out of 12 animals), while RISE 4 had only one animal with negative growth and seven with growth rates >0.05 mm d−1. RISE 2 growth rates were the least variable, with only one negative rate; most rates were between 0 and 0.05 mm d−1. Growth rates were significantly higher on RISE 4 than on RISE 1 (F = 10.77, p < 0.01) and RISE 4 than on RISE 2 (F = 3.90, p = 0.05). Growth rates were not significantly different between RISE 1 and RISE 2 (F = 1.07, p = 0.31).

3.1.3. Euphausiid Egg Production

[24] During RISE 1, 133 Euphausia pacifica females were incubated for egg production from 11 stations. The overall mean brood size was 103 eggs with brood sizes ranging from 3 to 455 eggs. The average TL of E. pacifica females was 19.6 mm with a range of 13.6–23.8 mm (Figure 4b). Gravid Thysanoessa spinifera females were rarely encountered on RISE 1, with only five females incubated from three different <100 m depth stations. Of these five females, only three spawned with a mean brood size of 36 eggs. The average TL of these females was 22.5 mm with a range of 18–25 mm (Figure 4c).

[25] During RISE 2, 51 Euphausia pacifica females were incubated for egg production from five stations and nine Thysanoessa spinifera females were incubated from four different stations. We never found gravid females of both species at the same station on this cruise. The mean E. pacifica brood size was 107 eggs with a range of 4–413 eggs. The average TL (mm) of E. pacifica females was 19.8 mm with a range of 16–22.6 mm (Figure 4b). The mean T. spinifera brood size was 166 eggs with a range of 28–240 eggs. The average TL (mm) of T. spinifera females was 22.6 with a range of 20.6–24.5 mm (Figure 4c).

[26] Gravid Thysanoessa spinifera females were far more common on RISE 3, with 36 females incubated from 10 stations, including some from stations as deep as 300 m. The overall mean brood size was 269 eggs with a range of 25–820. The average TL (mm) of T. spinifera females was 23.82 with a range of 21.5–26.5 mm (Figure 4c). Euphausia pacifica females were also relatively common on this cruise and 79 were incubated for egg production from nine stations. The mean E. pacifica brood size was 194 eggs with a range of 4–697. The average TL (mm) of E. pacifica females was 18.7 mm with a range of 13–23 mm (Figure 4b).

[27] No gravid Thysanoessa spinifera females were found on RISE 4. Incubations of 33 Euphausia pacifica females were set up at 10 stations. Mean brood size was 131 eggs and the range was from 11 to 345 eggs. Average TL (mm) was 19.9 mm with a range of 17.5–22.3 mm (Figure 4b).

[28] More small Euphausia pacifica females (<16 mm) were incubated on RISE 1 and 3 than on RISE 2 and 4 (Figure 4b). There were more small females with larger broods during RISE 3 than during RISE 1 (Figure 4b), although this difference was not statistically significant (F = 1.39, p < 0.25). Average TL (mm) of E. pacifica females from RISE 3 was significantly smaller than during the other three RISE cruises (F = 8.15, p < 0.005) because of the number of small females (<16 mm) encountered in the southern part of the RISE study area. Although there were more small females during RISE 3, the size range of larger spawning females (>16 mm) was comparable to other cruises (Figure 4b).

[29] Observation of euphausiid brood size data (Figures 4b and 4c) suggests that broods might have been larger during RISE 3. For Euphausia pacifica, there was a significant difference between cruises (overall F = 9.42, p < 0.01). Pairwise comparisons showed that brood sizes on RISE 3 were significantly higher than on RISE 1 and 2 (F = 25.35 and 15.76, respectively, p < 0.01 for both) and higher than brood sizes on RISE 4 (F = 4.07, p < 0.05). None of the other cruises were significantly different from each other at the p < 0.05 level. Differences between cruises for Thysanoessa spinifera brood sizes followed the same trend (overall F = 4.06, p < 0.05), but there were not enough samples for as rigorous a comparison between individual cruises. Brood sizes for T. spinifera on RISE 3 were higher than on RISE 1 and 2 (F = 5.59 and 3.93, p = 0.024 and 0.055, respectively).

[30] TL of Euphausia pacifica females was positively related to brood size for all cruises (p < 0.0001) but the relationship was not as strong for Thysanoessa spinifera females (p < 0.0491). There is a lot of variability associated with this relationship: although larger females (E. pacifica > 18 mm, T. spinifera > 22 mm) are capable of producing larger broods than smaller females, they do so only on occasion (Figures 4b and 4c). It was more common for larger females to have broods similar in size to those of smaller females. In fact, the smallest and largest E. pacifica females often had brood sizes ≤100 eggs (Figure 4b).

3.1.4. Copepod Egg Production

[31] During RISE 1, Calanus marshallae females were common, and 283 females were incubated from 28 stations, with a mean egg production rate (EPR) of 13.7 eggs female−1 d−1. Calanus pacificus were seldom encountered (at only five stations), and the average egg production by a total of only 18 females was similar to that of C. marshallae, 12.7 eggs female−1 d−1 (Table 3a). These few C. pacificus are not included in the graph of RISE 1 egg production data (Figure 5).

Figure 5.

Copepod egg production versus station depth: (a) Calanus marshallae on RISE 1 and (b) Calanus pacificus on RISE 2, 3, and 4. Regression lines are labeled with the number of the cruise (1 is RISE 1 and so on). C. pacificus from RISE 1 and C. marshallae from RISE 2 and 3 are not shown because there were so few.

[32] During RISE 2, only 40 female C. marshallae were collected (only five stations had ≥5 females), with an average EPR of 14.2 eggs female−1 d−1. Calanus pacificus were commonly collected and a total of 332 female C. pacificus were incubated from 33 stations, with an average EPR of 21.8 eggs female−1 d−1.

[33] During RISE 3, Calanus pacificus continued to dominate the copepod assemblage with 363 females incubated from 26 stations, and an average EPR of 31.9 eggs female−1 d−1. The mean EPR for C. marshallae was 32.9 eggs female−1 d−1, on the basis of 23 females from 8 stations.

[34] During RISE 4, egg production rates by female C. pacificus were the lowest of any RISE cruise, 8.3 eggs female−1 d−1 (481 females from 24 stations). There were no Calanus marshallae found at any station during this cruise.

[35] The EPRs of female Calanus pacificus were significantly higher on RISE 3 than the other three RISE cruises (RISE 3 versus 1 (t = 5.68), RISE 3 versus 2, (t = 5.78), and RISE 3 versus 4 (t = 15.5)). Rates on RISE 1 were slightly but significantly lower than rates on RISE 2 (t = 1.95) but the same as rates on RISE 4 (t = 0.69) (Table 3a). For C. marshallae, EPRs on RISE 1 and 2 were also the same, but EPRs on RISE 3 were significantly higher than EPRs on RISE 1 or 2 (RISE 1 versus 3, t = 5.83; RISE 2 versus 3, t = 5.3).

[36] There was a significant negative relationship between Calanus pacificus egg production and water depth for RISE 1 (F = 10.76, p < 0.0001) and for RISE 3 when the two deep water stations (water depths of ∼500 m) were excluded (F = 8.2, p = 0.0083) (Table 3b and Figures 5a and 5b), but not for RISE 2 and 4 (Table 3b and Figure 5b). Similarly, C. marshallae egg production rates were only correlated with water depth for RISE 1, with EPRs higher in shallower waters (F = 7.22, p = 0.0076) (Table 3b and Figure 5a).

Table 3b. Results of Statistical Tests for Differences in Egg Production Rates of Calanus pacificus and Calanus marshallae Among Cruises by Water Depth, Latitude, and Cruisea
 Calanus pacificusCalanus marshallae
  • a

    Two deepwater stations (water depths of ∼500 m in Figure 5a) were excluded from the RISE 3 statistical tests in “depth-latitude” results. Had we included them in the analysis, there would have been no difference in egg production with water depth. Here ns indicates not significant. An * indicates a significant relationship at the p < 0.05 level, ** indicates a significant relationship at the p < 0.001 level.

RISE 110.760.0051*0.800.397.720.0076*0.040.85
RISE 20.250.6244.070.0001*0.660.421.270.27
RISE 38.20.0083*5.460.02*2.380.144.450.048*
RISE 41.780.180.150.70----
RISE 1-   -   
RISE 2−1.95 *-  −0.21 ns-  
RISE 3−5.78 **−5.68 **- −5.83 **−5.3 **- 
RISE 41.25 ns11.32 **15.5 **---- 
NH−0.69 ns3.15 **6.61 **−5.23 **−5.53 **−2.42 **3.13 ** 

3.2. RISE Hypothesis: Does Zooplankton Productivity Increase With Latitude in the RISE Study Area?

[37] The relationship between euphausiid brood sizes and latitude within the RISE study area is shown in Figure 6. Euphausia pacifica brood sizes (Figure 6a) showed an overall significant relationship with latitude (higher at the southern end of the RISE study area) (F = 9.46, p < 0.01), however this relationship was driven entirely by results from RISE 1 (F = 14.4, p < 0.01). This indicates that there was no significant relationship between brood size and latitude for RISE 2, 3 and 4, and that on RISE 1 brood sizes were actually higher to the south, rather than to the north as was postulated by the RISE hypothesis. There were not enough Thysanoessa spinifera incubations to rigorously test this hypothesis, but on RISE 3 when we incubated the largest number of females (Table 1), there was a clear trend toward higher brood sizes to the south (Figure 6b). This result once again suggests that we can reject the hypothesis that euphausiid brood size is higher to the north of the RISE study area.

Figure 6.

Latitude versus mean brood size per incubation for (a) Euphausia pacifica and (b) Thysanoessa spinifera and latitude versus mean egg production rate per incubation for (c) Calanus marshallae on RISE 1 and (d) Calanus pacificus on RISE cruises 2, 3, and 4. Regression lines are labeled with the number of the cruise (1 is RISE 1 and so on). C. pacificus from RISE 1 and C. marshallae from RISE 2 and 3 are not shown because there were so few.

[38] The relationships between euphausiid length, brood size, and latitude, were examined for Euphausia pacifica. There was a strong correlation between length and brood size (F = 36.84, p < 0.0001) as previously discussed (Figure 4b). The relationship between length and brood size is further examined later in this paper. There was a strong relationship between latitude and length (F = 14.12, p = 0.0002) suggesting that females were larger in the northern part of the RISE study area, but this relationship was actually due to the small size of the spawning females (13–16 mm) on the southernmost sampling line during RISE 3 rather than to females being larger to the north. As a result, the significant relationship between latitude and brood size (F = 8.11, p = 0.0049) may be an artifact of the relationship between latitude and length, since the small females spawning in the southern part of the RISE study area would produce only smaller broods while the females of more typical adult size, which were found everywhere except the southernmost sampling line, were producing the full range of brood sizes (Figure 4b). Thus, although the statistical tests suggest a relationship between latitude and brood size, this relationship appears to be a consequence of the size distribution of females during RISE 3 rather than a direct effect of latitude.

[39] Relationships between copepod EPR and latitude were mixed (Table 3b and Figures 6c and 6d), with Calanus pacificus showing a significant increase in EPR with latitude on RISE 2 but a significant decrease on RISE 3 (Figure 6d), and C. marshallae a significant decrease on RISE 3 (Table 3b). On all other cruises, the slopes of the relationships between EPR and latitude were not significantly different from zero (Figures 6c and 6d) thus we have little evidence to support the hypothesis that egg production rates should be higher toward the northern part of the RISE study area.

3.3. Comparison of RISE Results With Results From Long-Term Study of the NH Line

3.3.1. Euphausiid Growth Rates

[40] We compared individual Euphausia pacifica growth rates from RISE cruises with those from long-term sampling (2001–2007) of NH Line off Newport, Oregon. We used NH line growth rates from June/July in order to match the timing of the RISE cruises. There were 78 June/July growth rates from the NH line and 34 from the RISE cruises (Figure 7a). The size ranges of the animals were similar, with euphausiids from the NH line ranging in total length from 12 to 22 mm, while those from the RISE study ranged from 10 to 21 mm. The percentage of individuals with negative growth was the same for both data sets (11%). The percentage of animals with zero growth was higher for NH (45%) than for RISE (15%). The percentage of animals with positive growth was lower for NH (40%) than for RISE (70%). Growth rates of Euphausia pacifica were not significantly different between the NH and RISE study areas (F = 1.74, p = 0.19). Average overall growth rates were 0.02 mm d−1 for the NH line and 0.03 mm d−1 for the RISE area. Average positive growth rates were also not statistically significant (F = 0.8, p = 0.37) with an average of 0.07 mm d−1 for the NH line and 0.06 mm d−1 for the RISE study.

Figure 7.

Euphausiid total length versus (a) Euphausia pacifica growth, (b) E. pacifica brood sizes, and (c) Thysanoessa spinifera brood sizes for the Newport Hydrographic Line (June–August 2001–2007) and the combined RISE cruises.

3.3.2. Euphausiid Brood Sizes

[41] Euphausiid brood sizes from RISE cruises were compared to a long-term data set for June–August 2001–2007 from off Newport, Oregon. Average Euphausia pacifica brood size for all the RISE cruises combined was 132 eggs, while the mean for summertime Newport line incubations was 170 eggs. Analysis of variance showed that there was a significant difference between the two groups, with the Newport brood sizes being significantly larger (F = 7.37, p < 0.01). Observation of the data also suggests that gravid E. pacifica females smaller than 16 mm were more common in the RISE study area (Figure 7b). Mean Thysanoessa spinifera brood size was 217 eggs for all RISE cruises combined, and 178 eggs for summertime Newport line incubations. Analysis of variance showed no significant difference between these two groups (F = 0.88, p = 0.35). The data suggest that the distribution of brood sizes was similar for both groups and that Newport line females had a slightly larger size range than RISE females (Figure 7c).

[42] To determine whether female length had an effect on brood size, we calculated a mean BS:TL ratio for each RISE cruise and for the data from the NH line. After determining that the variances among data sets were similar, these means were compared using a t test. We tested among individual RISE cruises to explore whether length had an influence on brood size during some cruises but not others. Each RISE cruise was also compared to the NH data. Euphausia pacifica from RISE 3 were significantly different from all other cruises and from the NH line (p < 0.05 for all). As previously shown, there were more small females spawning on RISE 3 than on any other cruise (Figures 4b and 7b). RISE 1, RISE 2, and RISE 4 were not significantly different from each other (p > 0.13). Like RISE 3, RISE 1 and RISE 2 were significantly different from the NH line (p < 0.05 for all). RISE 4 was not significantly different from NH (p = 0.24), but the number of E. pacifica brood sizes measured during RISE 4 was also relatively small compared to other RISE cruises (Table 1). There was only enough Thysanoessa spinifera data to make this comparison between RISE 3 and the NH line, and the difference was not significant (p = 0.24).

3.3.3. Copepod Egg Production

[43] Egg production rates averaged over all RISE cruises for Calanus marshallae were significantly lower than the June–August average for Newport (mean of 21.1 eggs female−1 d−1 (NH) versus 15.0 eggs female−1 d−1 (RISE) t = 4.74, p < 0.001) (Table 3a). However, when compared on a cruise-by-cruise basis, NH was significantly higher than RISE 1 and 2 (t = 5.53 and 2.42, respectively) and significantly lower than RISE 3 (t = 3.13) (Table 3a).

[44] For Calanus pacificus, a comparison of the grand means (RISE compared to NH) showed that the two rates were not different (mean of 19.5 versus 16.0; t = 1.86, p = 0.06) (Table 3a). However, on a cruise-by-cruise basis, RISE 1 was equal to NH (t = 0.69), RISE 2 and 3 were higher than NH (t = 3.15 and 6.61, respectively), and RISE 4 was lower than NH (t = 5.23).

4. Discussion

[45] No consistent correlations were found between egg production rates and latitude over the spatial domain from 45.5 to 48°N for euphausiids or copepods. Thus, apart from one cruise and species (RISE 2, Calanus pacificus) where egg production was higher off Washington than Oregon, we did not find support for the hypothesis that higher zooplankton egg production rates should be expected off Washington than off Oregon.

[46] The most consistent results from this study were the differences in vital rates observed among cruises. For the euphausiids, brood sizes were significantly higher during RISE 3; the same was true for both copepod species. Moreover, for the euphausiids and Calanus marshallae, average rates measured during the RISE study were usually lower than averages from long-term measurements off Newport, Oregon. For Euphausia pacifica, apart from RISE 3 when brood sizes were the same as the long-term Newport measurements, brood sizes were about 60% of the average rates. Thysanoessa spinifera were found during the first three RISE cruises, but females were abundant and brood sizes high only during RISE 3. Similarly, Calanus marshallae were also found only during the first three RISE cruises and egg production rates for Calanus marshallae never averaged more than 14 eggs d−1 on RISE 1 and 2, about 60% of the maximum average rates known from laboratory measurements (23.9 eggs female−1 d−1 [Peterson, 1988; W. T. P. Peterson, unpublished data, 2008]). However, egg production rates during RISE 3 were high, similar to the long-term mean and the laboratory-measured maximum rates. These observations suggest that C. marshallae was food limited on RISE 1 and 2. Calanus pacificus rates averaged for RISE 1, 2, and 4 ranged from 8 to 22 eggs female−1 d−1, or about 12–48% of the maximum rate of ∼50 eggs female−1 d−1 [Mullin, 1991; Runge, 1984]. Higher rates were observed during RISE 3, 32 eggs female−1 d−1. These observations again point to food limitation of egg production rates on RISE 1, 2 and 4, suggesting that oceanographic conditions were suboptimal for all taxa except during RISE 3.

[47] Food limitation may explain why we did not see differences between the Washington and Oregon shelf ecosystems for any of the taxa studied, especially for RISE 2 and 4 when chlorophyll averaged only ∼2 μg L−1. However, chlorophyll values during RISE 1 should have been high enough to elicit maximum or near-maximum egg production rates by the copepods, yet very low rates were observed. This suggests the influence of an unmeasured variable, possibly related to food quality. Chlorophyll only serves as a proxy for food if the zooplankton are eating predominantly phytoplankton.

[48] All oceanographic process studies are conducted within the context of a set of ocean conditions that have prevailed before and during the study period. For the RISE study, all cruises took place during a multiyear period of weak coastal upwelling and generally warm ocean conditions. Both the PDO and the MEI were in positive phase (Table 2a), indicating that weak but persistent El Niño–like conditions were present during all 3 years of the RISE study. This was clearly illustrated in local sea surface temperature data sets: SSTs during June 2005 and 2006 (RISE 2 and 4) were the warmest in the previous 10 years, warmer even than in June during the most recent strong El Niño (1998); July 2004 (RISE 1) was also the warmest since 1998. Only RISE 3 had a negative temperature anomaly.

[49] Warm ocean conditions have a clear impact on the copepod community composition [Hooff and Peterson, 2006]. The first RISE cruise (July 2004) was perhaps closest to typical conditions because the zooplankton community was composed of the boreal neritic coastal copepod species such as Calanus marshallae, Pseudocalanus mimus, and Acartia longiremis, which are typical of the upwelling system of the northern California Current [Hooff and Peterson, 2006; Mackas, 1992; Peterson and Keister, 2003; Peterson and Miller, 1975]. Warm water species such as Calanus pacificus and Paracalanus parvus were present but not abundant. However, the other cruises were typical of what can be expected during persistent warm phases of the PDO and ENSO, with warm water oceanic copepod species such as Calanus pacificus being relatively abundant and largely replacing the cool water C. marshallae. On RISE 4, no C. marshallae were collected and C. pacificus dominated the copepod community. Abundances of other boreal neritic species were low as well, whereas subtropical neritic species such as Paracalanus parvus, Ctenocalanus vanus, and Acartia tonsa were highly abundant.

[50] The RISE 2 cruise (June 2005) was particularly anomalous as it took place during a period of weak upwelling. In 2005, upwelling did not become established until mid-July, 2 months later than usual (Figure 2) (the climatological start of upwelling is 26 April at 48°N and 31 March at 45°N). The impact of the anomalously late start to the 2005 upwelling season on regional physical and biological oceanography has been described by Hickey et al. [2006], Mackas et al. [2006], Schwing et al. [2006], and Sydeman et al. [2006]. Even after upwelling became firmly established in July 2005, the copepod community was still dominated by warm water species and, during RISE 3, Calanus pacificus continued to dominate. Warm ocean conditions continued into spring and summer 2006, to the point that C. pacificus was again the dominant Calanus species. No Calanus marshallae were collected during the final RISE cruise (June 2006).

[51] In contrast with copepods, the species composition and biomass of euphausiids are not strongly associated with changes in ocean conditions. Euphausia pacifica always dominates and although its abundance fluctuates with season and year, we have not found a clear pattern in biomass fluctuations that is related to either the PDO or MEI, an observation based on more than 10 years of sampling off Newport. This species is oceanic, and off Oregon it lives in slope waters at depths of 250–350 m by day, thus is probably not as influenced by variations in SST as copepods. The only clear pattern is that E. pacifica are found in greater numbers in shelf waters during warm years [Feinberg and Peterson, 2003] but this will not necessarily translate into differences in vital rates. Thysanoessa spinifera, like Calanus mashallae, is a cold water coastal neritic species. The fact that very few were found on RISE 1 and 2 and none were found on RISE 4 is consistent with the observation that warm water conditions and a warm water zooplankton community prevailed during those three cruises.

[52] RISE 2 (2005) and RISE 4 (2006) both took place during June. Even though these cruises occurred during the same month in different years, euphausiid growth rates measured during these cruises were statistically different from each other (p = 0.05). It is likely that differences in environmental conditions in the RISE study area between these 2 years had an effect on euphausiid growth (Tables 2a and 2b). The spring transition (heralding the onset of the upwelling season) occurred extremely late in 2005 (25 May) but at a more typical time in 2006 (22 April) ( The late onset of upwelling in 2005 should have delayed the formation of phytoplankton blooms and therefore delayed the availability of the primary food supply for euphausiids. In contrast, winds were upwelling favorable for much of May 2006 [Bruland et al., 2008, Figure 2], prior to the start of zooplankton sampling during RISE 4 (June 2006). This should have provided a sufficient time interval for phytoplankton blooms to become established and for euphausiids to feed and assimilate energy to allocate to somatic growth. However, comparison of environmental indices between these two time periods does not yield the expected differences (Table 2a). In spite of the upwelling-favorable winds in May 2006, there was no measurable upwelling until 17 June, after RISE 4 had ended. Average chlorophyll (chl) concentrations were also similar, with 3.71 μg L−1 in June 2005 and 2.02 μg L−1 in June 2006. In spite of the fact that there were no clear differences in environmental conditions between these two cruises, all of the highest growth rates (>0.10 mm d−1) measured during RISE cruises were from RISE 4. This may be a result of the quality of food available to the euphausiids. Alternatively, the euphausiids may have been exploiting another food source, such as copepods or ciliates, either in addition to or instead of phytoplankton. In this case, chl would not serve as a proxy for food availability. We have no data on growth rates during RISE 3, the cruise with the highest rates of upwelling, because lack of incubator space limited us to measuring brood sizes only during this cruise.

[53] Why was RISE 3 so different for euphausiid egg production? The mean Euphausia pacifica brood size was 194 eggs with a range of 4–697. A brood size of 697 eggs is an all-time high for an E. pacifica brood size from all of our field incubations in the northern California Current. We have measured brood sizes of more than 1000 females and the previous high was 599 eggs [Gómez-Gutiérrez et al., 2007]. During RISE 3, winds were upwelling favorable for a 3 week period prior to the start of zooplankton sampling and remained so during the zooplankton sampling period (Figure 2) [Bruland et al., 2008, Figure 2]. As a result, phytoplankton blooms should have been well established, and euphausiids would have had sufficient time to assimilate energy for egg production. Finally, RISE 3 had notably more spawning E. pacifica in the smaller size range (12–15 mm) than any other cruise. Despite the favorable conditions during RISE 3, we were not surprised to see small females given that it takes several months for euphausiids to mature [Feinberg et al., 2006; Harvey et al., 2009] and the first half of 2005 was characterized by poor conditions for growth.

4.1. Comparisons Between NH and RISE

[54] Our regional comparisons of vital rates are imperfect because of differences in the temporal scales of the data sets used to compare the study areas off Newport, Oregon and the region surrounding the Columbia River plume. Sampling off Oregon (the NH line) occurs once every 2 weeks, compared to the RISE cruises where there were intensive sampling efforts over periods of 9–20 days (Table 1). This means that RISE data are from concentrated sampling efforts in summer 2004–2006 while the NH data come from one to two cruises month−1 from 2001 to 2007 for euphausiids and 2004 to 2006 for copepods. Thus, there is a higher potential for interannual variability to influence the NH data set, especially for euphausiids. In spite of this consideration, we feel that these two data sets yield a useful comparison of the two regions.

[55] Previous work in our laboratory has shown that euphausiid brood sizes are strongly correlated with female length [Gómez-Gutiérrez et al., 2006]. However, during the RISE 3 cruise, mean brood sizes were the highest measured during this study (194 eggs female−1) yet mean total lengths were the smallest (18.7 mm). To investigate the effect of total length on brood size we used the mean ratio of BS:TL per cruise. Our results showed that the mean BS:TL ratio for Euphausia pacifica from the NH line was significantly different from the first three RISE cruises (but not for RISE 4). The mean BS:TL ratios for RISE 1 (5.08) and RISE 2 (5.45) were lower than the mean ratio for NH (7.58); the mean ratio for RISE 3 (9.95) was higher. The mean TL of females in the NH climatology (20.7 mm) was higher than for the first three RISE cruises: RISE 1 (19.6 mm), RISE 2 (19.8 mm), and RISE 3 (18.7 mm) as reported in section 3 of this paper. Care should be taken in the interpretation of the BS:TL ratios because the results from RISE 3 suggest that smaller females found on that cruise were producing larger broods. However, we know from examination of the data on brood size versus length (Figures 4b and Figure 7b) that small females did not produce higher broods on RISE 3 than they did on the other cruises. The high BS:TL ratio was obtained because there were more small females spawning during RISE 3 in comparison with the other cruises.

[56] There were statistically significant differences between the NH climatology and most of the RISE cruises for both C. pacificus and C. marshallae. Egg production rates by both C. pacificus and C. marshallae were higher during RISE 3 than the Newport climatology, but no other pattern was apparent (i.e., for C. pacificus, NH rates were equal to RISE 1, lower than RISE 2 and 3 but greater than RISE 4; for C. marshallae, NH rates were greater than RISE 1 and 2 but less than RISE 3 (no females were collected on RISE 4). Our conclusion is that although some significant differences were found, we do not regard this finding as strong evidence that egg production rates are higher off Washington than Oregon largely because of the imperfect comparison of a summer climatology to rates measured over a ∼14 day period.

4.2. Rejection of RISE Hypothesis for Zooplankton Production

[57] Growth rates of euphausiids were not significantly different between the two study areas. We believe that this is a robust result because other research has shown that growth rates of Euphausia pacifica were quite similar from northern California to Washington [Shaw et al., 2009]. However, concerning euphausiid brood sizes, although our data show that brood sizes were not statistically different between the two study areas, this information alone is not sufficient to reject the hypothesis that euphausiid production is higher off of Washington, because there are other factors to consider when determining production. For example, differences in fecundity between the two regions could result in higher production in one region than in another. Our egg production experiments yielded brood sizes for individual euphausiids, but this is not the same as knowing the total fecundity of a female or a population. Given that brood sizes were similar between the two regions, if euphausiids in the RISE study area had shorter interbrood periods (i.e., fewer days between releasing broods of eggs), higher survivorship, or if there were higher densities of euphausiids overall, euphausiid production as a whole could be higher off Washington than it is off of Oregon. We need a better understanding of these aspects of euphausiid population dynamics in order to conclusively determine whether or not production is higher off of Washington.

[58] It is clear now that the RISE cruises occurred during anomalous conditions, so our experiments were conducted under environmental conditions that were not typical of this region. However, it is also possible that we may never be able to evaluate this hypothesis because when chlorophyll concentrations are high off Washington, they can easily exceed 10–20 μg chl a L−1. Assuming a minimal C:chl a of 40, this translates to 400–800 μg C L−1, a sufficient concentration to elicit maximum ingestion rates by both Calanus spp. [Frost, 1972; Peterson, 1988] and Euphausia pacifica (A. Sremba and W. T. Peterson, Feeding and ingestion rates of adult Euphausia pacifica under laboratory conditions, submitted to Journal of Plankton Research, 2008). As a result, the high phytoplankton biomass would not necessarily lead to a corresponding increase in euphausiid or copepod growth or reproductive output because their growth rates or egg production would have already reached their maximum rates at a lower phytoplankton biomass. That is, during the peak of the upwelling season in July and August, phytoplankton biomass could be high enough off both Washington and Oregon to result in maximum growth rates of copepods and euphausiids. Thus, the key to understanding why Washington seems to harbor a greater biomass of phytoplankton, zooplankton, and pelagic fish, (the Ware and Thomson hypothesis) may be related to differences in rates of offshore transport between the two regions. It might be that vital rates are always the same off Oregon and Washington but that more of the new production which results from these rates is retained on the shelf off Washington simply because the shelf is wider and upwelling weaker there than off Oregon.

5. Conclusions

[59] The RISE hypothesis proposed that high phytoplankton biomass on the Washington shelf should result in an increase in zooplankton production there as well. The experiments reported here did not find evidence to support this hypothesis. However, the timing of the RISE cruises provided an imperfect opportunity for testing this idea since all of the cruises took place during a period of anomalously warm ocean conditions. Thus, the fact that we did not find increased zooplankton productivity off the Washington coast versus the Oregon coast does not allow us to conclusively reject the hypothesis. Overall, the differences in oceanographic conditions (especially upwelling strength) at the time of these incubations seemed to affect zooplankton production more strongly than the hypothesized differences with latitude.


[60] We thank the captain and crew of the R/V Wecoma for willingly accommodating our nocturnal working schedule during the RISE cruises. We are greatly in debt to R. Kudela for making the chlorophyll data available for our use. Thanks go to J. Menkel for conducting the copepod experiments during RISE 4 and to REU students N. Román and K. Ruck for their participation in these cruises. We also thank H. Bi for his assistance and advice regarding the statistical procedures.