ARTICLE IN PRESS

Deep-Sea Research I 53 (2006) 321–332 www.elsevier.com/locate/dsr

Effects of mesoscale phytoplankton variability on the flemingeri and N. plumchrus in the coastal Gulf of Alaska

M.J. Dagga,Ã, H. Liua,1, A.C. Thomasb

aLouisiana Universities Marine Consortium, 8124 Highway 56, Chauvin, LA 70344, USA bSchool of Marine Sciences, University of Maine, 5741 Libby Hall, Orono, ME 04469-5741, USA

Received 25 January 2005; received in revised form 16 June 2005; accepted 26 September 2005 Available online 28 November 2005

Abstract

The copepods Neocalanus flemingeri and N. plumchrus are major components of the mesozooplankton on the shelf of the Gulf of Alaska, where they feed, grow and develop during April–June, the period encompassing the spring phytoplankton bloom. Satellite imagery indicates high mesoscale variability in phytoplankton concentration during this time. Because ingestion is related to food concentration, we hypothesized that phytoplankton ingestion by N. flemingeri and N. plumchrus would vary in response to mesoscale variability of phytoplankton. We proposed that copepods on the inner shelf, where the phytoplankton bloom is most pronounced, would be larger and have more lipid stores than collected from the outer shelf, where phytoplankton concentrations are typically low. Shipboard feeding experiments with both copepods were done in spring of 2001 and 2003 using natural water as food medium. Chlorophyll concentration ranged widely, between 0.32 and 11.44 mgl1 and ingestion rates varied accordingly, between 6.0 and 627.0 ng chl cop1 d1. At chlorophyll concentrationso0.50 mgl1, ingestion is always low, o40 ng cop1 d1. Inter- mediate ingestion rates were observed at chlorophyll concentrations between 0.5 and 1.5 mgl1, and maximum rates at chlorophyll concentrations41.5 mgl1. Application of these feeding rates to the phytoplankton distribution on the shelf allowed locations and time periods of low, intermediate and high daily feeding to be calculated for 2001 and 2003. A detailed cross-shelf survey of body size and lipid store in these copepods, however, indicated they were indistinguishable regardless of collection site. Although the daily ingestion of phytoplankton by N. flemingeri and N. plumchrus varied widely because of mesoscale variability in phytoplankton, these daily differences did not result in differences in final body size or lipid storage of these copepods. These copepods efficiently dealt with small and mesoscale variations in their food environment such that mesoscale structure in phytoplankton did not affect their final body size. r 2005 Elsevier Ltd. All rights reserved.

Keywords: Neocalanus; Grazing; Mesoscale; Phytoplankton; Gulf of Alaska

ÃCorresponding author. Tel.: +1 985 851 2856; 1. Introduction fax: +1 985 851 2874. E-mail address: [email protected] (M.J. Dagg). 1 Three species of large calanoid copepods, Neoca- Current address: Department of Biology, Atmospheric, lanus flemingeri, N. plumchrus and N. cristatus, Marine and Coastal Environment, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, dominate mesozooplankton biomass throughout Hong Kong. the entire subarctic Pacific Ocean, including the

0967-0637/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2005.09.013 ARTICLE IN PRESS 322 M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332 marginal seas. They have annual life cycles except less important to their diet in the Alaskan Gyre for a portion of the N. flemingeri population in the because the phytoplankton community consists western Pacific, which is biennial (Mackas and mostly of cells too small to be ingested, and because Tsuda, 1999; Miller and Terazaki, 1989; Tsuda et concentrations are routinely very low in these al., 1999). All three Neocalanus spp. mate and HNLC environments (Dagg, 1993a; Tsuda and spawn at depth (500–2000 m) in autumn to early Sugisaki, 1994). Microzooplankton, especially cili- winter. Their egg production is dependent on their ates and heterotrophic flagellates, are important diet lipid reserves and body tissues, and adults die after items for N. flemingeri and N. plumchrus in the gyres spawning in deep water. Development through the (Gifford and Dagg, 1991; Gifford, 1993). In naupliar (N1–N6) stages occurs while they ascend to contrast, in coastal regions during periods of high the surface. After ascending to the upper ocean, phytoplankton concentration, these copepods ap- Neocalanus spp. complete their annual feeding, pear to be predominantly herbivorous. For exam- growth and development above the permanent ple, ingestion rate of phytoplankton by Neocalanus pycnocline (0–150 m) in spring and summer. Diel spp. in the Bering Sea during the spring bloom vertical migration is weak or absent. N. flemingeri (Dagg et al., 1982; Dagg and Wyman, 1983) was and N. plumchrus partition the upper layer tempo- much higher than in the open subarctic Pacific rally. In the open Gulf of Alaska, N. plumchrus lags Ocean (Dagg, 1993a). N. flemingeri by about 1–2 developmental stages Phytoplankton concentration, however, is not (25–30 days) (Miller and Clemons, 1988). In the uniformly high during the spring bloom in the western gyre, seasonal segregation between N. coastal Gulf of Alaska but is spatially and flemingeri and N. plumchrus is also clear (Tsuda temporally variable, with significant mesoscale et al., 1999). On completion of their upper ocean variability superimposed on a general pattern of growing season and accumulation of large lipid high inshore and low offshore concentrations stores, Neocalanus spp. descend from the upper (Brickley and Thomas, 2004; Fig. 1). Consequently, layer to spend the late summer, autumn and early N. plumchrus and N. flemingeri in coastal regions winter at 500–2000 m. The life cycle of each species encounter a wide range of feeding conditions during then repeats. their major period of growth and development on Neocalanus spp. cannot overwinter on the con- the shelf. In this paper, we examine the effects of the tinental shelf, although there are small populations mesoscale structure of phytoplankton on the feed- in some of the deep coastal fjords of western North ing of these two copepods in the coastal Gulf of America (Fulton, 1973; Evanson et al., 2000; Alaska, and compare feeding variability with Cooney et al., 2001). Nevertheless, as a result of variability in body size and lipid storage across the onshore transport of oceanic surface water in the shelf. late winter and early spring, oceanic Neocalanus spp. typically dominate the biomass of mesozoo- 2. Methods and Materials plankton in shelf waters of the Gulf of Alaska during spring and early summer (Coyle and 2.1. Ingestion rates Pinchuk, 2005). The fate of these populations in the fall is unclear. Feeding experiments were conducted on ship- Neocalanus spp. are particle grazers, feeding on board during spring of 2001 and 2003 (Fig. 1). For suspended particulate materials in seawater. To a each experiment, copepods were collected by large degree, their diet reflects the composition of vertically hauling a plankton net with mesh size of the particulate materials surrounding them and 202 mm and a 20 l aquarium cod-end from 50 m to their nutritional state reflects the concentrations of the surface. Cod-end contents were gently poured available food. High nutrient, low chlorophyll into an insulated container. In the laboratory, (HNLC) conditions prevail in oceanic subarctic healthy individuals were sorted with ladles or regions but spring blooms of chain forming diatoms large-bore pipettes and transferred into small jars occur in the marginal seas and in the gyre margins containing surface seawater. These animals were (Miller et al., 1992; Banse and English, 1999). kept cool for about 30–90 min before being trans- Consequently, Neocalanus spp. occupy rather dif- ferred to experimental bottles. ferent ecological niches in marginal seas compared For food medium, seawater was collected to the oceanic gyres. Phytoplankton appears to be from the 50% light depth by Niskin bottles ARTICLE IN PRESS M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332 323

Fig. 1. Our study region including a sample image showing mesoscale structure of surface chlorophyll. For this image, chlorophyll concentration was derived from an 8 day average of SeaWiFS images between 5/1/2003 and 5/8/2003. All feeding experiments in this paper were done on the Seward line, indicated by the black line perpendicular to the coast, or in Prince William Sound. A region encompassing 30 km on each side of the Seward line is indicated by the white box. mounted to a CTD rosette. Seawater from to the formula of Frost (1972): several Niskin bottles was gently drained into a Vðk k Þ polycarbonate carboy and then screened through a F ¼ c t , Z 202 mm mesh during the filling of 2.3 l polycarbonate bottles. All carboys, bottles, tubing and other where V is the volume of the incubation bottle, Z is labware used in the experimental set-up the number of copepods in the incubation bottle, kc were acid cleaned and rinsed with milli-Q water and kt are the net or apparent prey growth rates in before use. the controls and treatments, respectively, which are N. flemingeri and N. plumchrus C5s were placed calculated by  into experimental bottles and incubated on deck for C0 24 h. In most experiments, three different concen- kðd1Þ¼ln C trations of copepods were incubated with 2–4 e replicate bottles for each treatment. Two or three for 24 h incubation, where C0 is the concentration of bottles with no copepods were incubated as phytoplankton at time 0, and Ce is the concentra- controls. All experimental bottles were tightly tion in the control and treatment bottles at the end capped after filling and one layer of neutral screen of the incubation. was applied to each bottle to reduce light by about Ingestion rate (I, ng chl cop1 d1) is calculated 50%. During incubation, temperature was con- by trolled by running surface seawater through the I ¼ CF, incubator. Except for ship motion, bottles were not mixed. Chlorophyll a concentration in three size where C is the mean concentration of prey classes (420, 5–20 ando5 mm) was determined at throughout the 24 h incubation period, which is the beginning and end of the incubation. For calculated by chlorophyll analysis, filters were placed in 90% C ðekt 1Þ acetone for 24 h at 20 1C and the extract was C ¼ 0 . measured with a Turner Designs fluorometer kt (Strickland and Parsons, 1972). To assess mesoscale structure of phytoplankton, Clearance rate, F (ml cop1 d1), on each size satellite-measured chlorophyll concentrations were category of phytoplankton was calculated according calculated from SeaWiFS imagery for 2001 and ARTICLE IN PRESS 324 M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332

2003. Daily 1 km resolution LAC data for each year Chlorophyll concentration ranged widely, between from the study region were acquired from the 0.32 and 11.44 mgl1, and ingestion rates varied NASA Distributed Active Archive Center, re- accordingly, between 6.0 and 627.0 ng chl cop1 d1 mapped to a standard projection, cloud masked, (Table 1). and processed to chlorophyll by the current global An example of the feeding behavior observed at SeaWiFS chlorophyll algorithm, OC4v4 (O’Reilly et high phytoplankton concentration is shown in al., 2000). Daily scenes were formed into 8-day Fig. 2. In this experiment with N. flemingeri C5 composites, beginning January 1 of each year, to (Experiment 2, Table 1), total chlorophyll concen- reduce data volume and reduce data gaps caused by tration at the beginning of the experiment was clouds. Cross-shelf chlorophyll profiles along the 3.75 mgl1 and the community was dominated by Seward line were subsampled from the 8-day large cells, with 82% of the total in the420 mm composite time series by extracting chlorophyll fraction, 10% in the 5–20 mm fraction and only 8% concentration at each 1 km location along the line, in theo5 mm fraction (Table 1). The apparent and forming a spatial mean of all valid returns growth rate of cells in the420 mm size fraction within a 30 km direction perpendicular to each side declined as the concentration of grazing copepods of the Seward line. This extracted a 60 km wide increased (Fig. 2a), indicating direct consumption of mean chlorophyll transect, centered on the Seward these cells. In contrast, the apparent growth rate of line, with 1 km cross-shelf resolution (e.g. Fig. 1), as cells in the two smaller size categories increased with an 8-day time series in each study year. increasing copepod concentration (Fig. 2a). We Between May 3 and 8, 2004, samples of C5 N. attribute this to a cascade effect whereby the flemingeri and N. plumchrus were collected by protozoan grazers of these smaller cells are con- MOCNESS net at locations along the Seward line sumed by the copepods, reducing the mortality rate from the inner shelf to outer shelf. A subsample of of small cells (Liu et al., 2005). The ingestion rate copepods collected at each station was taken and measured in this experiment was high (mean- immediately frozen in seawater for later determina- 292 ng chl cop1 d1, n ¼ 6, stdev ¼ 71), and in- tion of dry weight and lipid content. In the gested phytoplankton consisted almost entirely of laboratory, frozen samples were thawed under a cells in the420 mm size fraction (Fig. 2b, Table 1). dissecting microscope. C5 N. flemingeri and N. An example of feeding behavior observed at low plumchrus were identified (Miller, 1988) and sorted. phytoplankton concentration is shown in Fig. 3.In Prosome length of each was recorded. At this experiment with N. flemingeri C5 (Experiment stations with plentiful animals, 15 replicates of each 5, Table 1), total chlorophyll concentration was species were analyzed for dry weight and lipid 0.77 mgl1 and the community was dominated by content. Fewer replicates were used at some small cells, with 75% of the total in theo5 mm size stations. Once sorted and measured, copepods were fraction and only 6% in the420 mm category rinsed in distilled water and placed in pre-weighed (Table 1). In common with the experiment at high aluminum pans. Samples were dried for424 h at food concentration (Fig. 2), there was a strong 55 1C and weighed on a Cahn microbalance to decrease in the net growth of phytoplankton in determine dry weight. After weighing, samples were the420 mm size fraction with increasing copepod immersed in 2 ml of methylene chloride in capped concentration, indicative of increased grazing with vials to extract body lipids (Miller, 1993). The increased number of grazers (Fig. 3a). In this solvent was changed after 6 and 24 h with dis- experiment however, there was also some measur- posable glass pipettes. After 30 h, the final volume able grazing in the 5–20 mm size category. No was removed and the samples were dried again measurable grazing was seen in theo5 mm size for424 h and weighed to determine lipid-free dry fraction and, as was typically observed, there was an weight. Lipid content was determined as the apparent cascade effect in this size category (Fig. 3a). difference between total dry weight and lipid-free Total ingestion rate of phytoplankton was low dry weight. (mean ¼ 24.2 ng chl cop1 d1, n ¼ 6, stdev ¼ 5.3), less than 10% of the ingestion observed at high 3. Results chlorophyll concentration in Fig. 2. In spite of their scarcity, large cells dominated the diet with 50% of Seventeen feeding experiments were done with N. the ingested phytoplankton derived from this size flemingeri C5 and 13 with N. plumchrus C5. category. Most of the remainder (47%) came from ARTICLE IN PRESS M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332 325

Table 1 The average ingestion rate of phytoplankton, by size category, in each shipboard experiment with Neocalanus flemingeri and N. plumchrus during 2001 and 2003

Exp. no. Species Date Location Initial chlorophyll (mgl1) Ingestion (ng chlor cop1 d1)

o5 mm 5–20 mm 420 mm Total o5 mm 5–20 mm 420 mm Total

1 flemingeri 4/20/2001 MS 0.300 0.060 0.030 0.393 0.00 2.00 3.99 5.99 2 flemingeri 4/25/2001 IS 0.302 0.362 3.087 3.751 0.00 6.06 286.21 292.27 3 flemingeri 4/27/2001 PWS 0.112 0.112 0.538 0.762 1.67 8.39 112.14 122.19 4 flemingeri 4/28/2001 PWS 0.071 0.175 1.202 1.448 0.00 0.42 127.14 127.56 5 flemingeri 5/18/2001 OS 0.577 0.143 0.051 0.772 0.85 11.31 12.06 24.23 6 plumchrus 5/18/2001 OS 0.577 0.143 0.051 0.772 0.00 1.85 9.57 11.41 7 flemingeri 5/24/2001 MS 0.272 0.048 0.054 0.374 0.00 0.04 7.06 7.10 8 plumchrus 5/24/2001 MS 0.272 0.048 0.054 0.374 0.00 6.20 10.42 16.62 9 flemingeri 5/27/2001 MS 0.184 0.131 3.413 3.728 1.33 1.46 158.70 161.49 10 plumchrus 5/27/2001 MS 0.184 0.131 3.413 3.728 0.81 2.04 239.88 242.73 11 plumchrus 5/29/2001 IS 0.228 0.199 4.766 5.192 5.29 0.57 84.36 90.22 12 flemingeri 5/29/2001 IS 0.228 0.199 4.766 5.192 0.00 1.11 205.35 206.45 13 plumchrus 5/22/2001 PWS 0.231 0.315 0.741 1.287 0.00 2.42 101.83 104.25 14 plumchrus 5/23/2001 PWS 0.170 0.102 0.183 0.455 0.00 0.00 23.28 23.28 15 plumchrus 7/12/2001 IS 0.174 0.234 0.914 1.323 25.38 0.00 141.24 166.62 16 plumchrus 7/15/2001 MS 0.773 0.176 0.060 1.008 67.37 31.30 10.92 109.59 17 plumchrus 7/17/2001 MS 0.716 0.151 0.075 0.942 21.71 14.66 3.77 40.14 18 plumchrus 7/18/2001 OS 0.790 0.245 0.068 1.103 10.81 40.16 7.16 58.13 19 plumchrus 7/20/2001 OS 0.905 0.215 0.108 1.227 33.69 27.65 10.81 72.16 20 plumchrus 4/27/2003 OS 0.320 0.096 0.065 0.481 12.40 2.50 6.60 21.50 21 flemingeri 4/28/2003 OS 0.199 0.075 0.050 0.324 0.00 1.60 8.30 9.90 22 flemingeri 4/30/2003 PWS 0.165 0.201 1.317 1.684 0.00 0.00 187.20 187.20 23 flemingeri 5/2/2003 PWS 0.291 0.147 0.610 1.048 0.00 0.00 89.60 89.60 24 flemingeri 5/3/2003 PWS 0.041 0.081 1.151 1.273 0.00 0.00 192.20 192.20 25 flemingeri 5/6/2003 IS 0.281 0.458 2.050 2.789 0.00 0.00 127.80 127.80 26 flemingeri 5/7/2003 IS 0.248 0.599 2.476 3.333 0.00 0.00 328.10 328.10 27 flemingeri 5/11/2003 PWS 0.552 0.829 9.103 10.484 0.00 0.00 109.10 109.10 28 flemingeri 5/12/2003 PWS 0.456 0.457 10.526 11.438 0.00 0.00 627.00 627.00 29 flemingeri 5/13/2003 MS 0.999 0.244 0.058 1.301 0.00 0.00 136.60 136.60 30 plumchrus 5/13/2003 MS 0.999 0.244 0.058 1.301 0.00 0.00 144.20 144.20

IS ¼ inner shelf, MS ¼ mid-shelf, OS ¼ outer shelf, PWS ¼ Prince William Sound.

the intermediate size class and only a few consumed significant amounts of phytoplankton percent came from the smallest size category in theo5 mm size fraction (experiments 15–20, (Fig. 3b, Table 1). Table 1). As an example, results from experiment With only a few exceptions (see below) large cells 20 (Table 1) are shown in Fig. 4. Total chlorophyll dominated the diet of both copepods under all concentration at the beginning of this experiment conditions. Generally, when large cells were abun- was 0.48 mgl1 and the community was dominated dant, chlorophyll concentration was high and high by small cells, with 66% in theo5 mm category and ingestion rates resulted. When large cells were rare only 14% in the 420 mm category. Total ingestion and chlorophyll concentration was low, ingestion was low, averaging only 21.5 ng chl cop1 d1 rate was low but large cells still dominated the diet. (n ¼ 4, stdev ¼ 11.8) but cells in theo5 mm category Simultaneous experiments with N. flemingeri and comprised 58% of this (Fig. 4). As observed in N. plumchrus during periods when their populations almost all experiments, large cells were ingested in overlapped did not show any consistent differences greater proportion than their abundance (30% vs. in their feeding behavior (paired experiments 5 and 14%) but only in these experiments with N. 6, 7 and 8, 9 and 10, 11 and 12, 29 and 30 in Table 1) plumchrus was there a significant contribution by but in all 30 experiments, only N. plumchrus small cells to the diet, between 15 and 61% of the ARTICLE IN PRESS 326 M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332

Fig. 2. Results from feeding experiment 2, with N. flemingeri C5 Fig. 3. Results from feeding experiment 5, with N. flemingeri C5 on April 25, 2001, using water collected from the inner shelf on May 18, 2001, using water collected from the outer shelf containing a high concentration of phytoplankton. (a) The containing a low concentration of phytoplankton. (a) The apparent growth rate of each size category of phytoplankton. apparent growth rate of each size category of phytoplankton. Slopes are significantly different from each other (ANCOVA, Slopes are significantly different from each other (ANCOVA, p 0:001) and significantly different from 0 for the420 mm po0:005) and significantly different from 0 for the420 mm o (p 0:001) and 5–20 mm(p 0:001) lines. (b) Phytoplankton (po0:001) ando5 mm(po0:05) lines. (b) Phytoplankton ingested o o in each size category. ingested in each size category. total ingested phytoplankton. Collectively, these 6 experiments suggest that N. plumchrus C5 may be more capable of feeding on small cells than N. flemingeri C5. Although feeding behavior of these two copepods is yet not fully understood, there is sufficient information to allow an initial estimate of the effect of mesoscale or small-scale variation in phytoplank- ton on their feeding in the Gulf of Alaska shelf region. Data from all feeding experiments combined (n ¼ 132) show there is a general tendency for higher ingestion rates at higher phytoplankton concentrations (Fig. 5). There is a lot of variability Fig. 4. Results from feeding experiment 20, with N. plumchrus C5 but we can use this relationship to characterize on April 27, 2003, using water collected from outer shelf shelf waters as supportive of low, intermediate containing a low concentration of phytoplankton. ARTICLE IN PRESS M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332 327

Fig. 5. The relationship between ingestion rate and total chlorophyll concentration derived by combining all feeding Fig. 6. Chlorophyll concentration within the area 30 km each experiments: (a) all data for both N. flemingeri C5 and N. side of the Seward line (the white line in Fig. 1). Blue indicates plumchrus C5; (b) expanded scale showing ingestion rates at concentrationso0.5 mgl1 which support low feeding rates, chlorophyll concentrationso1.5 mg chl l1. The curvilinear rela- yellow indicates concentrations between 0.5 and 1.5 mgl1 which tionship plotted in both panels is the same. support intermediate feeding rates, and orange indicates con- centrations41.5 mgl1 which support high feeding rates. (top panel) 2001, (bottom panel) 2003. or high ingestion rate. At chlorophyll con- centrationso0.50 mgl1, ingestion is always low, phytoplankton on the shelf from the perspective of o40 ng cop1 d1 (Fig. 5). Ingestion rate calculated C5 N. flemgeri and N. plumchrus feeding. Condi- from the derived equation for a chlorophyll tions that identify periods and locations of low concentration of 0.50 mgl1 is 44.7 ng chl cop1 d1. feeding rate are represented by the portions of Fig. 6 At chlorophyll concentrations between 0.5 and in blue, intermediate feeding rate is represented by 1.5 mgl1, ingestion increases rapidly and can yellow, and high feeding rate by orange. The spring be4300 ng cop1 d1 (Fig. 5). Ingestion rate calcu- bloom is readily apparent in both years between lated from the derived equation for a chlorophyll approximately day 120 and 180. During this time, concentration of 1.00 mgl1 is 85.2 ng chl cop1 d1, there is a tendency for higher concentrations of and at 1.50 mgl1 is 121.8 ng chl cop1 d1.At phytoplankton to occur in the inner shelf compared chlorophyll concentrations41.5 mgl1, ingestion to the outer shelf but mesoscale structure is evident can be even higher,4500 ng cop1 d1 (Fig. 5). in both years and there is some interannual Ingestion rate calculated from the derived equation variability apparent. At all times some portion of for a chlorophyll concentration of 5.00 mgl1 is the study region is supportive of at least two levels 297.4 ng chl cop1 d1. of feeding. The fractions of our imaged region that The spatial and temporal distribution of chlor- support low, intermediate and high ingestion rates ophyll in these three concentration ranges is shown of phytoplankton directly reflect this phytoplankton in Fig. 6. This represents the mesoscale structure of distribution (Fig. 7). A seasonal integration of these ARTICLE IN PRESS 328 M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332

Fig. 8. The dry weight (a) and lipid store (b) of individual N. flemingeri C5 and N. plumchrus C5 collected May 3–10, 2004. Fig. 7. The fraction (%) of the 60 km wide cross-shelf swath Samples from three stations are pooled from the inner shelf (IS), supporting low, medium and high feeding rates of N. flemingeri from four stations for the middle shelf (MS) and from six stations and N. plumchrus C5 during 2001 (top) and 2003 (bottom). for the outer shelf (OS). The number of samples used for each plot are: N. flemingeri IS 24, MS 22, OS 35; N. plumchrus IS 27, patterns over the April, May and June period when MS 30, OS 36. Bars indicate 95% C.I. N. flemingeri and N. plumchrus do most of their feeding and growing on the shelf indicates, in 2001, % body weight consisting of lipid (Fig. 8b) were a copepod would have encountered low feeding identical over all parts of the shelf in C5s of both conditions 18% of the time, intermediate feeding species. Day to day variation in the ingestion of conditions 41% of the time and high feeding phytoplankton did not affect the total amount of conditions 41% of the time. In 2003, the fractions growth and food storage that occurred over the are 29%, 42%, and 29% for low, intermediate and 60–90 day period these copepods spent feeding and high feeding rates, respectively, for the AMJ time growing in surface water. period. Throughout the growing season for N. flemingeri and N. plumchrus, there is always some 4. Discussion mesoscale phytoplankton structure on the shelf and this structure affects the daily ingestion rate of C5s Our feeding experiments indicated that total of both copepods. However, variability in the daily chlorophyll was a reasonable indicator of daily ingestion rate of phytoplankton, induced as a phytoplankton ingestion, although there is a lot of response to mesoscale structure in the phytoplank- variability in the data used to derive this relation- ton, was not reflected in the body size or lipid ship. Ingestion was always low at low phytoplank- content of individual copepods (Fig. 8). In May ton concentrations and higher but variable at 2004, the individual body weight (Fig. 8a) and the high concentrations. This pattern has also been ARTICLE IN PRESS M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332 329 observed in other studies with these copepods optical depth. However, based on vertical profiles of (e.g. Dagg et al., 1982; Dagg and Walser, 1987). chlorophyll made at stations used for collecting In all feeding experiments at chlorophyll con- water for feeding experiments, subsurface chloro- centrations41.50 mgchll1 ingestion of phyto- phyll maxima were typically not present and plankton was heavily dominated by cells420 mm. community composition was similar at all depths. In some of these experiments, ingestion of inter- The exceptions were late in the season during the mediate sized cells was measurable but made only a post-bloom period on the mid- and outer-shelf, minor contribution to the total diet. Ingestion of when a subsurface chlorophyll maximum sometimes cells from the small size category,o5 mm, was developed. Neocalanus spp. do not undergo diel typically not measurable. At low chlorophyll con- migrations in this region (Napp unpublished) and centrations, ingestion rates were much lower and are most heavily concentrated in the surface layer. small and intermediate sized cells often made up a We believe that surface chlorophyll represents the greater proportion of the diet than large cells. Even phytoplankton environment encountered by N. under low chlorophyll conditions however, large flemingeri and N. plumchrus. cells were always a greater fraction of the diet than An accurate assessment of the validity of the they were in the phytoplankton community. Small NASA global chlorophyll algorithm for these cells were a significant portion of the total ingestion waters requires optical sampling protocols, instru- only for N. plumchrus, perhaps indicating that N. ments and effort beyond the scope of our study. The plumchrus is more capable of feeding on smaller in situ surface chlorophyll data we do have available food sizes than N. flemingeri. This needs to be is formed into cross-shelf transects representative of further examined in detailed, direct comparative two time periods, and compared to satellite-derived experiments. In the five direct comparisons made in transects subsampled from monthly composite this study, there were no consistent differences in imagery approximately concurrent with the field the feeding behavior of N. flemingeri and N. operations. Comparisons of these transects (Fig. 9) plumchrus, but size fractionated chlorophyll is a further suggests that, within the strong temporal coarse index of feeding behavior. and spatial variability present on the shelf, the The satellite data clearly indicate strong mesos- satellite data provide a reasonable assessment of cale structure of chlorophyll on the shelf during our chlorophyll structure. study years (2001 and 2003), even during the spring Another potential difficulty with the satellite bloom, consistent with earlier analyses for the derived chlorophyll calculations is that the size 1997–2001 time period (Brickley and Thomas, composition of the phytoplankton community 2004). The imagery measures surface chlorophyll cannot be resolved. Because both N. flemingeri as a weighted integral of radiance over the first and N. plumchrus fed more efficiently on large

GAK Line Chlorophyll April-May, 2003 GAK Line Chlorophyll July-August, 2003 12 12 SeaWiFS Chl with 1/2 Standard Error SeaWiFS Chl with 1/2 Standard Error In situ Chl and range 10 10 In situ Chl -3 -3 8 8

6 6

4 4 Chlorophyll mg m Chlorophyll Chlorophyll mg m Chlorophyll 2 2

0 0 0 50 100 150 200 250 0 50 100 150 200 250 Distance along GAK line (km) Distance along GAK line (km)

Fig. 9. Comparisons of cross-shelf chlorophyll structure in the vicinity of the Seward line using satellite-derived chlorophyll and available surface in situ data from two periods in 2003. Although strong time and space differences coupled with strong variability do not allow direct comparison of the two data sets, overall structure and magnitudes are similar. ARTICLE IN PRESS 330 M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332 particles, the ingestion per unit of chlorophyll was of N. flemingeri and N. plumchrus development and higher when the phytoplankton community was growth on the shelf. Relationships between phyto- dominated by large cells. The same amount of plankton concentration and ingestion rate are not chlorophyll detected by imagery might support known for younger copepodid stages of N. flemin- different amounts of ingestion if the size composi- geri and N. plumchrus but, in general, smaller tion of that chlorophyll was different. This would copepods reach feeding saturation at lower food introduce an error in our use of imagery to map the concentrations than larger copepods. It is reason- feeding environment. However, with few exceptions, able to assume that effects of mesoscale phytoplank- the size composition of the phytoplankton commu- ton variability on the daily ingestion by younger nity changed in a systematic manner (Fig. 10), being (smaller) copepodid stages are less than we indicate dominated by large cells (420 mm) whenever total for the C5s. Ingestion of phytoplankton by the chlorophyll concentration was higher than about earliest (smallest) copepodid stages may even be 0.5 mg chl l1 and by small cells otherwise. This might maximum over all conditions observed on the shelf. introduce a small systematic error but would not be As development and growth proceed, however, the significant given the broad variability around our food concentration required for maximum ingestion shipboard derived relationship between ingestion increases and variation in available phytoplankton and chlorophyll concentration. We concluded that, will induce wider variations in daily ingestion. In for the purposes of this paper, surface chlorophyll spite of this, variations in daily ingestion did not measured by satellite imagery is a reasonable result in differences in final body size or food storage representation of the phytoplankton food environ- (% lipid), which were statistically similar for all ment for C5 N. flemingeri and N. plumchrus. individuals collected on the shelf. Copepodid stage Imagery indicated that mesoscale variability in C5s collected from anywhere on the shelf during phytoplankton concentration existed on the Gulf of early May 2004 were indistinguishable in terms of Alaska shelf at all times that N. flemingeri and N. body weight and food lipid store. N. flemingeri and plumchrus were present during 2001 and 2003. Our N. plumchrus were able to average out mesoscale- shipboard experiments indicated this variability induced fluctuations in daily feeding during their affected the daily feeding of C5 N. flemingeri and 60–90 day period of growth and development. There N. plumchrus on phytoplankton although it did not are several possible mechanisms for this, including explain all the variability in phytoplankton ingestion alternative food sources, physiological adaptations, that we observed. This mesoscale effect will not be and environmental displacement. equally important over the entire 60–90 day period Additional food sources such as microzooplank- ton and other particulate matter may smooth out variability in the phytoplankton environment if they are not distibutionally or temporally correlated with phytoplankton. These foods could provide nutrition in areas or times of scarce phytoplankton food, resulting in approximately similar daily ingestion rates in terms of carbon. Microzooplankton, how- ever, are not sufficiently abundant to support high carbon ingestion rates during the months of the spring bloom (Liu et al., 2005). Microzooplankton concentrations increase dramatically during the post-bloom period (Lessard et al., 2003), but N. flemingeri and N. plumchrus have completed their growth and development by this time. The role of detrital aggregates as food for N. flemingeri and N. plumchrus is not well understood but aggregates Fig. 10. The relationship between the large cell component of the appear to be an important source of nutrition for N. phytoplankton community and the total chlorophyll concentra- cristatus (Dagg, 1993b). tion, indicating the phytoplankton community is always domi- nated by large cells when chlorophyll concentration is high, and Most copepods are able to smooth out some of typically dominated by small cells when the chlorophyll the variability in their food environment as long as concentration is low. they encounter conditions supporting a high feeding ARTICLE IN PRESS M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332 331 rate at a physiologically appropriate frequency Bochdansky, A.B., Bollens, S.M., 2004. Relevant scales in (Dagg, 1977; Bochdansky and Bollens, 2004). Such zooplankton ecology: distribution, feeding, and reproduction behavior, sometimes called a ‘hunger response’ of the copepod Acartia hudsonica in response to thin layers of the diatom Skeletonema costatum. Limnology and Oceano- (Runge, 1980), involves bursts or short periods of graphy 49, 625–636. very high feeding activity when a patch or region of Brickley, P.J., Thomas, A.C., 2004. Satellite-measured seasonal high food concentration is encountered. This might and interannual chlorophyll variability in the Northeast explain how N. flemingeri and N. plumchrus in our Pacific and coastal Gulf of Alaska. Deep-Sea Research II study are able to accommodate mesoscale varia- 51, 229–245. Cooney, R.T., Coyle, K.O., Stockmar, E., Stark, C., 2001. bility in their food environment without affecting Seasonality in surface-layer net zooplankton communities in their final body size. This behavior might also Prince William Sound, Alaska. Fisheries Oceanography 10 explain some of the variability observed in our (Supplement 1), 97–109. shipboard experiments, assuming individuals in Coyle, K.O., Pinchuk, A.I., 2005. Seasonal cross-shelf distribu- different bottles had different feeding histories. tion of major zooplankton taxa on the northern Gulf For individual copepods to encounter a range of of Alaska shelf relative to water mass properties, species depth preferences and vertical migration behavior. Deep-Sea phytoplankton concentrations over periods of days, Research II 52, 217–245. either the phytoplankton within the water contain- Dagg, M.J., 1977. Some effects of patchy food environments on ing both phytoplankton and copepods must change copepods. Limnology and Oceanography 22, 99–107. or the copepods must somehow be displaced or Dagg, M.J., 1993a. Grazing by the copepod community does not moved to a different parcel of water containing a control phytoplankton production in the subarctic Pacific Ocean. Progress in Oceanography 32, 163–183. different concentration of phytoplankton. Both are Dagg, M.J., 1993b. Sinking particles as a possible source of probable for large copepods like N. flemingeri and nutrition for the calanoid copepod in the N. plumchrus. subarctic Pacific Ocean. Deep-Sea Research I 40, 1431–1445. In conclusion, the daily ingestion of phytoplank- Dagg, M.J., Walser Jr., W.E., 1987. Ingestion, gut passage, and ton by N. flemingeri and N. plumchrus varies with egestion by the copepod , in the laboratory and in the subarctic Pacific Ocean. Limnology phytoplankton concentration, but mesoscale varia- and Oceanography 32, 178–188. bility in phytoplankton on the shelf of the Gulf of Dagg, M.J., Wyman, K.D., 1983. Natural ingestion rates Alaska does not result in differences in final body of the copepods Neocalanus plumchrus and N. cristatus, size or lipid storage of these copepods. These calculated from gut contents. Marine Ecology Progress Series copepods efficiently deal with small and mesoscale 13, 37–46. Dagg, M.J., Vidal, J., Whitledge, T.E., Iverson, R.L., Goering, variations in their food environment such that J.J., 1982. The feeding respiration, and excretion of zoo- mesoscale structure in phytoplankton does not plankton in the Bering Sea during the spring bloom. Deep-Sea affect their final body size. Research 29, 45–63. Evanson, M., Bornhold, E.A., Goldblatt, R.H., Harrison, P.J., Lewis, A.G., 2000. Temporal variation in body composition Acknowledgements and lipid storage of the overwintering, subarctic copepod Neocalanus plumchrus in the Strait of Georgia, British This field work would not have been possible Columbia (Canada). Marine Ecology Progress Series 192, without close collaborations with S. Strom and 239–247. J. Napp and their assistants. We thank the Captain Frost, B.W., 1972. Effects of size and concentration of food and crew of the R.V. Alpha Helix for shipboard particles on the feeding behavior of the marine planktonic copepod pacificus. Limnology and Oceanography 17, assistance. This research was supported by the 805–815. Biological Oceanography program of the National Fulton, J.D., 1973. Some aspects of the life history of Calanus Science Foundation under grant number OCE- plumchrus in the Strait of Georgia. Journal of the Fisheries 0102381 to MJD/HL and OCE-0000899 to ACT Research Board of Canada 30, 811–815. as part of the US GLOBEC program, and by Gifford, D.J., 1993. Protozoa in the diets of Neocalanus spp. in the subarctic Pacific Ocean. Progress in Oceanography 32, NASA grant number NAG5-6604 to ACT. 223–237. Gifford, D.J., Dagg, M.J., 1991. The microzooplankton-meso- zooplankton link: consumption of planktonic Protozoa by the References calanoid copepods Acartia tonsa Dana and Neocalanus plumchrus Marukawa. Marine Microbial Food Webs 5, Banse, K., English, D.C., 1999. Comparing phytoplankton 161–177. seasonality in the eastern and western subarctic Pacific and Lessard, E.J., Foy, M.S., Bernhardt, M., Opatkiewicz, A., 2003. the western Bering Sea. Progress in Oceanography 43, Seasonal, interannual and spatial patterns in phytoplankton 235–288. and microzooplankton community composition and size ARTICLE IN PRESS 332 M.J. Dagg et al. / Deep-Sea Research I 53 (2006) 321–332

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