Deep-Sea Research II 49 (2002) 2695–2711
Latitudinal comparisons of equatorial Pacific zooplankton M.R. Romana,*, H.G. Damb, R. Le Borgnec, X. Zhanga a
Horn Point Laboratory, University of Maryland Center for Environmental Science P.O. Box 775, Cambridge, MD 21613, USA b Department of Marine Sciences, University of Connecticut, Groton, CT 06340, USA c Centre IRD de Noumea, B.P. A5, 98848 Noumea cedex, New Caledonia, France Received 15 May 2001; received in revised form 11 November 2001; accepted 22 November 2001
Abstract Zooplankton biomass and rates of ingestion, egestion and production in the equatorial Pacific Ocean along 1401W and 1801 exhibit maximum values in the High-Nutrient Low-Chlorophyll (HNLC) zone associated with equatorial upwelling (51S–51N) as compared to the more oligotrophic regions to the north and south. Zooplankton biomass and rates are not usually highest on the equator, but increase ‘‘downstream’’ of the upwelling center as the zooplankton populations exhibit a delayed response to enhanced phytoplankton production. The vertical distribution of zooplankton biomass in the equatorial HNLC area tends to be concentrated in surface waters and is more uniform with depth in oligotrophic regions to the north and south of the equatorial upwelling zone. In general, the amount of mesozooplankton (>200 mm) carbon biomass is approximately 25% of estimated phytoplankton biomass and 30% of bacterial biomass in the HNLC area of the equatorial Pacific Ocean. Zooplankton grazing on phytoplankton is low in the equatorial Pacific Ocean, generally o5% of the total chlorophyll-a standing stock grazed per day. Based on estimates of metabolic demand, it is apparent that zooplankton in the equatorial Pacific Ocean are omnivores, consuming primarily microzooplankton and detritus. Estimated zooplankton growth rates in the warm waters of the HNLC equatorial Pacific Ocean are high, ranging from 0.58 d1 for 64–200 mm zooplankton to 0.08 d1 for 1000–2000 mm zooplankton. Thus, the numerical and functional response of equatorial zooplankton to increases in phytoplankton production are more rapid than normally occurs in sub-tropical and temperate waters. Potential zooplankton fecal pellet production, estimated from metabolic demand, is approximately 1.6 times the estimated gravitational carbon flux at 150 m in the zone of equatorial upwelling (51S–51N) and 1.1 times the export flux in the more oligotrophic regions to the north and south. The active flux of carbon by diel migrant zooplankton in the HNLC zone is a minor fraction of the gravitational flux (2% at 1401W, 4% at 1801) but increases in the more oligotrophic regions to the north and south where there is a deeper mixed layer and a greater relative proportion of diel migrant zooplankton. r 2002 Elsevier Science Ltd. All rights reserved.
1. Introduction Upwelling in the equatorial Pacific Ocean may support a significant amount (0.8–1.8 Gt year1) of *Corresponding author. E-mail address:
[email protected] (M.R. Roman).
new production per year (Chavez and Barber, 1987) or approximately half of the estimated annual global new production (Eppley and Peterson, 1979). A paradox in understanding the ecology of this important oceanic region is the presence of relatively high concentrations of inorganic macronutrients accompanied with low
0967-0645/02/$ - see front matter r 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 0 2 ) 0 0 0 5 4 - 1
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M.R. Roman et al. / Deep-Sea Research II 49 (2002) 2695–2711
chlorophyll concentrations, a situation called ‘‘High-Nutrient Low-Chlorophyll (HNLC)’’ by Minas et al. (1986). Therefore, other factors such as micronutrients (i.e. iron, Martin et al., 1989), grazing (Walsh, 1976) or both (Landry et al., 1997) probably limit the amount of phytoplankton production. Copepods were once thought to be the major grazers of phytoplankton in the ocean. However, there now is increasing evidence that the majority of phytoplankton consumption is by small protozoa (Capriulo et al., 1991; Landry et al., 1993). Protozoa can efficiently ingest the small (o2 mm) phytoplankton that usually dominate oceanic waters and have growth rates similar to phytoplankton. In a review of the controls of phytoplankton production, Banse (1992) suggested that the most important limiting factor of phytoplankton production is grazing (mostly by protozoa), even in HNLC areas such as the equatorial Pacific Ocean (Dam et al., 1995b; Landry et al., 1997). Although copepods may not be the primary grazers that control phytoplankton production, they can be important in controlling the export flux. Through their production of rapidly sinking fecal pellets, copepods contribute substantially to the flux of biogenic material (e.g., Fowler and Knauer, 1986; Small et al., 1989; Altabet and Small, 1990). In addition to gravitational particle sinking and advection, diel and ontogenic zooplankton migrations have been proposed to be another important mechanism in transporting carbon from the euphotic zone to the deep water in some areas of the oceans (Longhurst and Harrison, 1988; Longhurst et al., 1990; Dam et al., 1995a, Le Borgne and Rodier, 1997; Zhang and Dam, 1997). This process has been termed the active flux. Diel migrant zooplankton are usually found below the euphotic zone by day and within the euphotic zone by night. A portion of the organic carbon acquired by diel migrant zooplankton through nocturnal feeding within the euphotic zone is released, as respiratory and excreted carbon, during the daytime below the euphotic zone by returning migrant mesozooplankton. Longhurst et al. (1990) and Dam et al. (1995a) showed that the amount of respiratory carbon transported from the euphotic zone by diel
migrant zooplankton can be, at times, of the same order of magnitude as that of the gravitational particle sinking in oligotrophic ocean regions. Upwelling at the equator is driven by a winddriven geostrophic divergence. Primary production and chlorophyll are usually centered near the equator and decrease north and south of the equator (Vinogradov, 1981; Barber et al., 1996). In contrast, equatorial Pacific Ocean mesozooplankton (>200 mm), presumably due to their slower growth rate as compared to phytoplankton, often exhibit peaks in abundance farther to the north and south than phytoplankton (Vinogradov, 1981; White et al., 1995; Le Borgne et al., 2002b). The spatial patterns of mesozooplankton are influenced by the temporal evolution of plankton communities in response to upwelling and meridional transport. This ‘‘downstream’’ succession of phytoplankton, herbivorous zooplankton, carnivorous zooplankton and fish has been observed in a number of equatorial and coastal upwelling systems (King and Hida, 1957; Vinogradov and Voronina, 1963; Blackburn et al., 1970; Vinogradov and Shushkina, 1978). The gradients in phytoplankton production and the numerical and functional response by the zooplankton community in the equatorial Pacific Ocean provide a range of conditions with which to compare the role of zooplankton in biogeochemical fluxes. Research conducted under the US Joint Global Ocean Flux Study (US JGOFS) and French ‘‘Etude du Broutage En zoNe Equatoriale’’ (EBENE) provide the framework for such a synthesis. The emphasis of this paper is how the size structure and rate processes of zooplankton vary in relation to the latitudinal patterns of primary production and the gravitational flux of particulate material in the HNLC and oligotrophic waters of the equatorial Pacific Ocean.
2. Data sources and processing Data used in our analysis are derived primarily from the US JGOFS equatorial Pacific study (EqPac) and the French study (EBENE). EqPac cruises (Table 1) consisted of transects along 1401W from 121S to 121N and two 20-day
M.R. Roman et al. / Deep-Sea Research II 49 (2002) 2695–2711 Table 1 JGOFS and EBENE stations JGOFS TT007 February–March 1992 TT008 March–April 1992 TT011 August–September 1992 TT012 October 1992
EBENE October–November 1996
Transect along 1401W from 121N to 121S 21 day time series on the equator at 1401W Transect along 1401W from 121N to 121S 21 day time series on the equator at 1401W
Transect along 1801 from 81S to 81N 48 h time series at 31S and at the equator
time-series stations on the equator (01, 1401W). The central equatorial Pacific Ocean experienced * conditions during the first US JGOFS El Nino field season (February–April) and ‘‘normal’’ upwelling conditions during the second US JGOFS field season (August–October) in 1992 (McPhaden, 1993). The EBENE cruise (Table 1) consisted of a transect along 1801 from 81S to 81N collected between October 21 and November 20, 1996, with 48-h diel studies at 31S and the equator. 2.1. Zooplankton biomass Zooplankton (>64 mm) on the EqPac cruises were collected from day/night pairs of tows in the surface 200 m with a 0.25 m2-mouth area MOCNESS equipped with nine nets with a 7:1 mouth:length ratio (Wiebe et al., 1985). Onboard ship, the contents of each net were split in half with a Folsom Plankton splitter. One-half of the sample was preserved in 4% buffered (sodium borate) Formalin. The remaining half of the sample was gently wet-sieved through a 2000-mm mesh to remove gelatinous zooplankton and micronekton (not caught quantitatively by the 0.25-m2 MOCNESS). The portion passing through this mesh was wet-sieved further through 1000, 500, 200 and 64 mm meshes. This procedure yielded four different size classes: 2000–1000; 1000–500; 500–200 and 200–64 mm. Organic carbon and nitrogen for each size fraction was measured with a Model 240 Control Equipment CHN analyzer. The average
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error associated with sub-sampling the zooplankton catch for carbon analysis was 16% (standard deviation/mean). Zooplankton biomass of the different size fractions as well as the amount of total (>64 mm) zooplankton is expressed as mmol C m3 or mmol C m2 (integrated). Details of the sampling procedures and the zooplankton biomass data can be found in Roman et al. (1995a), White et al. (1995) or on the US JGOFS database (http://usjgofs.whoi.edu). Zooplankton (>200 mm) on the EBENE cruises were collected with triple WP-2 nets (UNESCO, 1968) and the Hyrobios multiple plankton sampler, MPS II (Weikert and John, 1981). With the MPS II, five nets were opened and closed successively, using remote controls in the shipboard laboratory. The WP-2 nets sampled the 0– 100 and 0–400 m water columns and were fitted with two TSK flowmeters. Zooplankton collected with the MPS II net system were analyzed for dry weight (DW) and ash-free dry weight (AFDW). Samples from the triple WP-2 nets were wet-sieved through 2000 and 500 mm mesh, thus giving two size classes: 200–500 and 500–2000 mm. The C, N and P composition of zooplankton was determined on the catch from one of the WP-2 nets. Details of the sampling procedures and the zooplankton biomass and composition data can be found in Le Borgne et al. (2002b). 2.2. Zooplankton rates Direct estimates of mesozooplankton (>200 mm) grazing were made using the gut fluorescence technique (Dam et al., 1995b; Zhang et al., 1995; Champalbert et al., 2002) and by isotopic labeling of particulate material (Roman and Gauzens, 1997). In addition, we also performed indirect estimates of mesozooplankton growth, production, ingestion and egestion using the model of Hirst and Lampitt (1998), which predicts copepod growth rate from temperature and body size. Hirst and Lampitt (1998), combined published data (n ¼ 952) on copepod growth rates, body weights (0.075–3620 mg C), and habitat temperature (2.3–29.01C) in a multivariate regression equation that relates intrinsic growth rate (g ¼ d1) to temperature (T ¼ 1C) and copepod
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weight (BW=mg C individual1): log10 ðgÞ ¼ 0:0208T 0:0221 log 10 ðBWÞ 1:1408 ðr2 ¼ 0:435Þ: When Hirst and Lampitt compared the measured values of growth to the growth rates predicted by the equation, approximately 96% of the predicted values were between 5 and 0.2 times the measured values. Note that the 952 published growth rates used to generate the Hirst and Lampitt (1998) equation covered a range of food conditions. Thus, the predicted growth rates may be less than a maximum intrinsic growth rate if the growth rates included in the regression analysis were foodlimited. Conversely, if the in situ growth rates are severely food-limited, the Hirst and Lampitt (1998) predicted growth rates may represent an overestimate of the actual in situ rate. We have previously (Roman et al., 2000) compared three different empirical models (Huntley and Boyd, 1984; Huntley and Lopez, 1992; Hirst and Sheader, 1997) to estimate mesozooplankton growth rates in the Arabian Sea. The Hirst– Sheader (1997) model (which is similar to the Hirst and Lampitt (1998) model used here) provided the most reasonable estimates of growth rate for different mesozooplankton size-fractions when compared to published growth rates for similar-sized copepods at the ambient temperatures. Habitat temperature is used to estimate copepod growth. Temperature data were obtained by taking the average of all CTD casts from a particular station listed in the US JGOFS database (http://usjgofs.whoi.edu). We used the average of the 25-m bins for the MOCNESS zooplankton collections. In applying the Hirst–Lampitt (1998) equation to estimate zooplankton growth rate, we assumed that copepods comprised all of the measured zooplankton biomass. Based on previous studies of the mesozooplankton community in the EqPac study (Roman et al., 1995a), it appears that copepods usually comprised >80% of the mesozooplankton. We used estimated body weights for copepods in the various size-fractions that were determined during the EqPac study by Zhang et al.
(1995). The calculated individual copepod weights in the different size fractions for TT007 and TT011, respectively, were: 200–500 mm=2.0 and 3.6 mg C; 500–1000 mm=17.0 and 22.9 mg C; 1000– 2000 mm=45.8 and 61.4 mg C. We assumed that the average weight of zooplankton caught in the 64–200 mm fraction was 0.2 mg C, the value found by Rodriguez and Mullin (1986) for equatorial Pacific Ocean waters. Mesozooplankton production (mmol C m3 d1) is the product of the estimated growth rate (g) and the biomass (B). Thus, we multiplied our estimates of growth (g) for the different copepod sizefractions by the average of the day and night biomass estimates for each mesozooplankton sizefraction. Generally, the mesozooplankton biomass used was the average of two daytime and two nighttime tows at each station. We estimated mesozooplankton ingestion (mmol C m3 d1) by assuming a gross growth efficiency (growth/ingestion) of 30%. It has been suggested that copepod gross growth efficiency can vary with food quality and temperature, ranging from approximately 14% to 50% with a mean of approximately 30% (Omori and Ikeda, 1984). A similar mean gross growth efficiency was determined by Straile (1997) for both protozoa and crustacean zooplankton. Copepod fecal pellet production was estimated from the derived ingestion estimates and an assumed 70% assimilation efficiency for organic matter (n ¼ 104; SD=0.16; Conover, 1978). The actual efficiencies of copepod growth and assimilation likely varied over EqPac stations. However, these efficiencies have been shown to vary 20–50% over a range of temperatures, food qualities, and copepod sizes, whereas mesozooplankton biomass during our study varied by more than an order of magnitude. We make the following five assumptions to simplify the calculation of the downward export of carbon by diel migrant mesozooplankton. (1) The increase in biomass in the euphotic zone at night is caused exclusively by mesozooplankton diel vertical migration from below the euphotic zone. (2) Diel migrant mesozooplankton release a portion of their acquired food carbon within the euphotic zone as respiratory carbon below the euphotic
M.R. Roman et al. / Deep-Sea Research II 49 (2002) 2695–2711
zone during daytime at a rate determined by animal body weight and ambient temperature. (3) Diel migrant mesozooplankton are found during the daytime at depths ranging from 120 to 400 m, and experience the mean temperature in this layer. (4) The time mesozooplankton spend in upward and downward migration is ignored. (5) Diel migrant mesozooplankton acquire their daily carbon ration exclusively through nocturnal feeding in the euphotic zone. The downward flux of carbon by diel migrant mesozooplankton as respiratory carbon (mmol C m2 d1) was calculated from the relationship (Dam et al., 1995a) Fr ¼ B R T; where B is the biomass of diel migrant mesozooplankton (mmol C m2) estimated from the difference between night- and daytime biomass in the euphotic zone (120 m); R the hourly weightspecific rate of carbon respiration estimated from the body weight and the mean temperature (1C) between 120 and 400 m (h1); and T the number of hours per day that diel migrant mesozooplankton stay below the euphotic zone (12 h d1 in our case). The size-specific respiration rate was estimated from body weight (carbon) and temperature using Ikeda’s (1985) multivariate regression equation: lnðROÞ ¼ 0:5254 þ 0:835 lnðW Þ þ 0:0601 lnðTempÞ; where RO is the ml O2 animal1 h1; W the mg C animal1 (Zhang et al., 1995); Temp the mean temperature between 120 and 400 m (1C). The respiration rate (RO) expressed as ml O2 animal1 h1 was converted to carbon equivalent (RC: mg C animal1 h1) by the relationship: RC ¼ RO RQ 12=22:4; where RQ is the respiration quotient (the molar ratio of carbon dioxide produced to oxygen consumed as a result of respiration); 12 is the molecular weight of carbon; and 22.4 is the molar volume of an ideal gas at standard temperature and pressure. RQ was assumed to equal 1 (Omori and Ikeda, 1984). RC was converted to hourly weight-specific rate of carbon respiration (R: h1)
by dividing by (mg C animal1).
the
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animal
body
weight
3. Results and discussion 3.1. Meridional patterns in zooplankton biomass On both of the EqPac 1401W survey cruises, maximum integrated (surface 150 m) zooplankton (>64 mm) biomass values were found north of the equator, between 11N and 51N (Fig. 1; Table 2; White et al., 1995). Variations in the wind field can influence the position of the divergence within the South Equatorial Current (SEC; Cromwell, 1953) and the loci of convergences between the SEC and North and South Equatorial Counter Currents (Murray et al., 1995). Therefore, the meridional patterns of zooplankton biomass around the equator can vary on both seasonal and shorterterm time scales (King and Hida, 1957; White et al., 1995). In addition, as observed at a timeseries station on the equator (Fig. 1; Roman et al., 1995a; Le Borgne et al., 2002a), zooplankton biomass and species composition can vary with the passage of tropical instability waves. Note that there were lower zooplankton biomass values * conditions during Survey 1 (TT007) when El Nino were present as compared to Survey 2 (TT011) when ‘‘normal’’ conditions prevailed. Barber et al. (1996) found that primary productivity differences between the two survey cruises due to ENSO were more focused in the 51S–51N region of equatorial upwelling, with the primary productivity average for this region, 56 mmol C m2 d1 during Survey 1, and 91 mmol C m2 d1 during Survey 2. The average integrated (150 m) total (>64 mm) zooplankton biomass in the 51S–51N region was similar between the two survey cruises (41 mmol C m2 during Survey 1 and 47 mmol C m2 during Survey 2). However, the largest zooplankton fraction (1–2 mm) we sampled increased substantially (8 mmol C m2 during Survey 1 and 13 mmol C m2 during Survey 2). Presumably, this larger zooplankton size fraction responded to the greater biomass of chlorophyll during the second survey, when a greater fraction
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Fig. 1. Integrated (0–150 m) zooplankton (>64 mm) biomass (mmol C m2) along 1401W (transect; 121S–121N) and at the equator (time series; year day) during EqPac TT007 and TT011.
of the chlorophyll was contributed by diatoms (Bidigare and Ondrusek, 1996). The 64–200 mm zooplankton fraction is comprised primarily of copepod nauplii (Roman et al., 1995a), thus, the 64–200 mm/>200 mm zooplankton biomass ratio can be used as a crude indicator of zooplankton recruitment. The highest ratios generally occurred in the zone of equatorial upwelling and highest primary production (51S– 51N), suggesting that the increased phytoplankton production (and concomitant increased protozoan biomass) enhanced copepod reproduction. On the EBENE 1801 transect, maximum zooplankton biomass values were found between 61S and the equator (Fig. 2; Le Borgne et al., 2002b). This difference in the meridional distribution of zooplankton as compared to the 1401W transect may be due to the passage of a tropical instability wave that brought lower zooplankton biomass to
the north of the equator (Le Borgne et al., 2002b). The overall levels of zooplankton along the 1401W and 1801 transect were similar, with somewhat higher values near the equator on the 1801 transect. This may have been the result of increased production as a result of the tropical instability wave, or perhaps different methods of zooplankton sampling (Le Borgne et al., 2002b). In general, there are no significant zonal differences in mesozooplankton found along the equator at these longitudes (Le Borgne et al., 1999). Meridional differences in the vertical distribution of zooplankton biomass generally show that zooplankton are more concentrated in HNLC surface waters of the equatorial upwelling zone (51S–51N), but become more uniform with depth in oligotrophic regions north and south of the equator (White et al., 1995; Le Borgne et al., 2002b). The same differences in the vertical
Table 2 Zooplankton biomass, ingestion and production/egestion integrated to 150 m 0.2–0.5 mm biomass (mmol C m2)
0.5–1.0 mm biomass (mmol C m2)
1.0–2.0 mm biomass (mmol C m2)
Total biomass (mmol C m2)
Total ingestion (mmol C m2 d1)
Total production/ PP egestion (mmol C m2 d1)
3.28 1.67 4.27 6.73 10.10 6.64 8.39 4.81 5.18 7.19
8.96 4.95 8.60 14.89 15.17 12.31 16.53 8.38 8.00 12.62
12.45 2.53 7.11 16.54 14.45 13.92 18.62 12.70 13.40 9.11
3.60 0.96 3.20 6.50 9.60 10.44 8.63 7.14 9.30 4.87
28.29 10.11 23.18 44.66 49.32 43.31 52.17 33.03 35.88 33.79
9.78 5.42 15.03 29.07 34.05 27.32 33.52 20.41 20.99 25.06
2.93 1.63 4.51 8.72 10.22 8.20 10.06 6.12 6.30 7.52
27.47 25.39 37.94 47.36 62.96 62.39 50.83 62.77 82.65 48.86
6.14
12.36
11.77
5.33
35.6
24.75
7.42
60.14
5.45
8.02
6.73
2.01
22.21
17.00
5.10
33.57
Mean S.D.
5.82 2.16
10.90 3.42
11.61 4.33
5.97 3.01
34.30 11.66
21.87 2.57
6.56 0.77
50.19 16.31
TT011 121N 91N 71N 51N 31N 21N 11N 0 11S 21S 31S 51S 71S 91S 121S
3.72 2.98 8.60 8.63 6.56 15.18 17.48 6.74 9.35 8.16 11.17 6.98 4.37 4.24 3.06
5.98 5.43 6.39 12.24 8.58 17.67 17.66 7.29 12.42 13.49 12.02 9.10 6.91 5.51 4.85
7.55 5.84 5.13 15.14 11.22 13.57 11.29 7.70 9.72 12.92 8.41 14.58 10.32 7.09 4.93
3.40 3.05 2.44 19.77 19.84 12.68 13.84 12.23 11.37 10.89 6.83 12.75 11.76 4.20 4.89
20.65 17.3 22.56 55.78 46.2 59.1 60.27 33.96 42.86 45.46 38.43 43.41 33.36 21.04 17.73
10.56 8.98 18.71 29.98 21.17 34.57 36.40 16.65 24.14 23.23 24.37 21.59 15.97 12.66 9.65
3.17 2.69 5.61 9.00 6.35 10.37 10.92 4.99 7.24 6.97 7.31 6.48 4.79 3.80 2.90
29.83 23.28 22.36 46.49 57.26 149.36
Mean S.D.
7.81 4.11
9.70 4.16
9.69 3.26
10.00 5.49
37.21 14.44
20.58 2.21
6.17 0.66
70.27 40.10
TT007 121N 91N 71N 51N 31N 21N 11N 0 11S 21S 31S 51S 71S 91S 121S
M.R. Roman et al. / Deep-Sea Research II 49 (2002) 2695–2711
0.064–0.2 mm biomass (mmol C m2)
1401W
105.30 92.52 100.12 115.11 70.60
31.03 2701
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Fig. 2. Integrated (0–150 m) mesozooplankton (>200 mm) biomass (mmol C m2) along 121S–121N at 1401W (TT011) and at 1801.
distribution of zooplankton also appear on the equator, between the HNLC region and the warm pool in the western Pacific (Le Borgne and Rodier, 1997). The amount of depth-integrated (0–150 m) zooplankton (>64 mm) biomass at the 121N–121S stations along 1401W during both EqPac survey cruises was significantly (Po0:05) correlated to the integrated primary production but not to estimates of new production (Fig. 3). Zooplankton biomass (>200 mm) was also significantly correlated with estimates of primary production along the 1801 transect. As pointed out by previous workers (Dam et al., 1995b; Zhang et al., 1995; Roman and Gauzens, 1997; Gaudy et al., 2002), equatorial Pacific zooplankton are primarily omnivores. Thus, the correlation of zooplankton with primary
production is likely the result of an overall increase of other trophic groups consumed by zooplankton, coincident with increases in primary production. New production values along the EqPac 1401W transect were highest near the equator where the greatest amount of nitrate and iron are upwelled into the euphotic zone (McCarthy et al., 1996). However, because of their slower growth rates, maxima in zooplankton biomass are found downstream (Figs. 1 and 2) of the upwelling divergence and maxima of new production. Thus, the correlation between zooplankton biomass and new production was not significant (Fig. 3). In a broader spatial domain under steady state conditions, zooplankton biomass should increase with new production both as a result of increases in total productivity (Eppley and Peterson, 1979) and
M.R. Roman et al. / Deep-Sea Research II 49 (2002) 2695–2711
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Fig. 3. Integrated (0–150 m) zooplankton (>64 mm) biomass, primary production, new production, sinking phaeopigment, and carbon flux (at 150 m) along 1401W (121S–121N) during TT007 and TT011.
because new production often promotes the increase of larger phytoplankton (i.e. diatoms) that can be directly grazed by copepods (Roman and Gauzens, 1997). Zooplankton biomass along the US JGOFS meridional transects was significantly correlated with the sinking flux of phaeopigments (data available at http://usjgofs.whoi.edu) at the base of the euphotic zone (Po0:05; Fig. 3). The conversion of chlorophyll to phaeopigments can occur through the digestion process of copepods (Gaudy et al., 2002). Thus, the production of copepod fecal pellets is a primary mechanism for the gravitational flux of phaeopigments (Welsch-
meyer and Lorenzen, 1985). Note that the daily flux of phaeopigments in the HNLC region was generally o2% of the chlorophyll standing crop (Fig. 3; Barber et al., 1996). This flux percentage is similar to the daily consumption of phytoplankton biomass by mesozooplankton (>200 mm), which was generally o5% of the phytoplankton standing crop per day in the EqPac region (Dam et al., 1995b, Roman and Gauzens, 1997; Gaudy et al., 2002). The correlation between zooplankton biomass and the sinking carbon flux was not statistically significant. Intensive recycling of material in the water column may obscure any relationship between zooplankton and flux. In
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addition, the sinking of aggregates can be a major component of sinking particulate carbon in this oceanic region (Walsh et al., 1997). 3.2. Biomass comparisons of plankton groups We have compared the integrated (0–120 m) biomass of various plankton groups over the 1401W meridional transect (Fig. 4). The biomass values for bacteria, heterotrophic picoplankton/ nanoplankton (HPIC/HNAN) and heterotrophic microplankton (HMIC) were obtained from the US JGOFS database (http://usjgofs.whoi.edu). Phytoplankton carbon biomass was estimated from chlorophyll-a values using a C:chlorophylla ratio of 58 (Eppley et al., 1992). The amount of
integrated phytoplankton carbon was greater than any of the heterotrophic components in the 21S– 21N equatorial band, with the greatest autotrophic biomass found during the second survey when ‘‘normal’’ upwelling occurred (Fig. 4). The second largest carbon pool was found in bacteria, which was similar to, or exceeded, the amount of phytoplankton at latitudes greater than 51S and 51N (Fig. 4). The integrated bacterial biomass along the 1401W transect was fairly uniform with similar transect means for the two surveys (TT007=99 mmol C m2; TT011=113 mmol C m 2). There are limited data for HPIC/HNAN, especially for the second survey cruise. On survey one, the highest HPIC/HNAN biomass values were found north of the equator where the values
Fig. 4. Integrated (0–120 m) biomass of phytoplankton, bacteria, heterotrophic picoplankton and nanoplankton, heterotrophic microzooplankton, and mesozooplankton along 1401W (121S–121N).
M.R. Roman et al. / Deep-Sea Research II 49 (2002) 2695–2711
were similar to the carbon estimated for phytoplankton and bacteria (Fig. 4). The smallest biomass component was HMIC (ciliates, forams, heterotrophic dinoflagellates, and copepod nauplii). As observed for mesozooplankton (>200 mm), maximum values of microzooplankton were found north of the equator. Mesozooplankton carbon biomass as compared to phytoplankton carbon showed minimum ratios near the equator during the second transect (0.17) when ‘‘normal’’ upwelling occurred, and maximum values (0.38) on both transects at 51N, the approximate location of a convergence associated with the transition between the South Equatorial Current and North Equatorial Counter Current. In general, integrated mesozooplankton carbon biomass in the euphotic zone was approximately 25% of estimated phytoplankton carbon biomass and 30% of bacterial biomass. Roman et al. (1995b) found similar values for plankton at the US JGOFS time-series station off Bermuda. The meridional differences in the ratio of mesozooplankton C/bacterial C were opposite to those of mesozooplankton C/phytoplankton C, with higher mesozooplankton C/bacterial C near the equator. The average amount of integrated mesozooplankton biomass compared to all measured heterotrophic plankton (bacteria+HPIC)/ (HNAN+MICRO+MESO) was 0.14, which was similar to an analogous calculation (0.12) made for the biomass contribution by mesozooplankton to total heterotrophic plankton off Bermuda (Roman et al., 1995b). We did not find any meridional differences in this ratio during the first survey (there were only HPIC/HNAN measurements on the equator during the second survey). 3.3. Meridional patterns in zooplankton rate processes Meridional measurements made during EqPac (Zhang et al., 1995) showed that zooplankton grazing (daily removal of phytoplankton by >200 mm mesozooplankton) was highest in the equatorial zone (21S–21N) and decreased at higher latitudes. Overall grazing rates were low, however, with generally o5% of the total chlorophyll
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standing stock grazed per day. These rates were similar to values found by Champalbert et al. (2002) for equatorial stations at 1801W and generally agree with estimates of grazing by open-ocean zooplankton (Roman and Gauzens, 1997). Based on estimates of metabolic demand, Zhang et al. (1995) concluded that ingestion of phytoplankton would meet, on average, 46% (200–500 mm), 34% (500–1000 mm), and 22% (1000–2000 mm) of estimated maintenance-carbon demand of zooplankton. These estimates agree with the general findings of Dam et al. (1995a), Roman and Gauzens (1997), and Gaudy et al. (2002), and suggest that equatorial Pacific zooplankton are primarily omnivores. Using the equation of Hirst and Lampitt (1998), ambient temperature, and the body weights of copepods determined for the four size fractions (Zhang et al., 1995), we have calculated the growth rates (d1) of zooplankton in the euphotic zone (100 m) at the various US JGOFS transect stations (Table 3) by assuming that copepods comprised all of the measured zooplankton biomass. The lower estimated growth rates during TT011 was the result of colder temperatures and larger average size of the copepods (Zhang et al., 1995). The highest average growth rates were for the 64– 200 mm fraction at the equator and 51S (0.58 d1), and the lowest growth rates were estimated for 1000–2000 mm zooplankton at 121N (0.06 d1) during TT007. Overall zooplankton growth rate means, weighted by the relative contribution by the various size fractions, were 0.27 d1 in TT007 and 0.21 d1 in TT012 (Table 3). Note that zooplankton production is the product of growth rate biomass. Zooplankton ingestion is derived using a 0.3 gross growth efficiency (production/ingestion), and zooplankton egestion (fecal pellet production) assumes a 0.7 assimilation efficiency of organic matter, or that egestion is 0.3 ingestion. Thus, the estimates of zooplankton production are the same as zooplankton egestion. The meridional patterns of zooplankton ingestion and production (Fig. 5; Table 2) are similar, but not identical to the patterns of zooplankton biomass because of differences in water temperature and changes in the relative distribution of
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Table 3 Equatorial Pacific zooplankton growth rates (d1) in the surface 120 m along 1401W 64–200 mm 200–500 mm 500–1000 mm 1000–2000 mm Total TT007 121N 0.26 91N 0.35 71N 0.42 51N 0.46 31N 0.46 21N 0.46 11N 0.45 0 0.47 11S 0.45 21S 0.46 31S 51S 0.47 71S 91S 121S 0.45
0.13 0.16 0.20 0.22 0.22 0.22 0.22 0.22 0.22 0.22
0.06 0.07 0.10 0.11 0.11 0.11 0.11 0.11 0.11 0.11
0.05 0.06 0.07 0.08 0.08 0.08 0.08 0.08 0.08 0.08
0.10 0.15 0.19 0.20 0.21 0.19 0.19 0.19 0.18 0.22
0.23
0.11
0.08
0.21
0.22
0.11
0.08
0.23
Mean 0.43 S.D. 0.06
0.21 0.03
0.10 0.02
0.08 0.01
0.19 0.03
TT011 121N 0.39 91N 0.39 71N 0.45 51N 0.45 31N 0.41 21N 0.38 11N 0.38 0 0.38 11S 0.40 21S 0.38 31S 0.39 51S 0.41 71S 0.43 91S 0.44 121S 0.43
0.16 0.16 0.17 0.18 0.16 0.15 0.15 0.15 0.16 0.15 0.15 0.16 0.17 0.17 0.17
0.08 0.08 0.09 0.10 0.09 0.08 0.08 0.08 0.09 0.09 0.08 0.09 0.09 0.09 0.09
0.06 0.06 0.07 0.07 0.06 0.06 0.06 0.06 0.06 0.06 0.06 0.06 0.07 0.07 0.07
0.15 0.16 0.25 0.16 0.14 0.18 0.18 0.15 0.17 0.15 0.19 0.15 0.14 0.18 0.16
Mean 0.41 S.D. 0.03
0.16 0.01
0.09 0.01
0.06 0.00
0.17 0.03
zooplankton size fractions. Thus, even though there was more zooplankton biomass during the second survey cruise (TT011), higher water temperatures and a greater percentage of smaller zooplankton (higher weight-specific ingestion rates) during the first cruise (TT007) resulted in similar estimates ingestion and production values for the two survey cruises (Fig. 5). As shown for
the meridional patterns in zooplankton biomass, our estimates of zooplankton ingestion and production were highest 1–51N. When we compare the estimated zooplankton ingestion and production to primary production, higher ratios were found during the TT007 when primary production was lower (Fig. 5). Thus, the average grazing ratio (zooplankton ingestion/ primary production) for the entire transect was 0.56 on TT007 and 0.46 on TT011. Zooplankton ingestion rates are estimated from growth rates and published growth efficiencies and thus represent total carbon ingested. We know that a major portion of the carbon ingested by zooplankton is from protozoa and detritus; thus, we do not mean to imply that our estimates of zooplankton carbon ingestion equate to phytoplankton ingestion. The grazing ratio (zooplankton ingestion/primary production) is used in a comparative sense, but serves to illustrate relative carbon flows from autotrophic production through zooplankton. The meridional patterns from our two survey cruises suggest that relative to primary production, there is more carbon flux through zooplankton at the stations north of the equator, where greater zooplankton production and biomass would be available to higher trophic levels. Minimum ratios of zooplankton ingestion/primary production occur near the equator, where, due to upwelled nutrients, primary production is high (Barber et al., 1996), but where zooplankton populations have not had sufficient time to increase in the newly upwelled waters. The average production ratio (zooplankton production/primary production) calculated for the stations along the 1401W transect was 0.17 on TT007 and 0.11 on TT011. These average production ratios also were estimated in the Arabian Sea (0.12; Roman et al., 2000), Hawaiian Ocean Time Series station (0.05; Roman et al., 2002) and Bermuda Atlantic Time Series station (0.03; Roman et al., 2002) and are consistent with our past notions of the transfer efficiency of aquatic food webs (Slobodkin, 1961; Ryther, 1969). We found the lowest ratio (0.06) at the equator during the second cruise when ‘‘normal’’ upwelling occurred, and the highest ratios (0.25 and 0.32) near areas of convergence at 51N and
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Fig. 5. Zooplankton ingestion and production/egestion (mmol C m2 d1) and the ratio of zooplankton ingestion/primary production and zooplankton production/primary production along 1401W (121S–121N).
71N during the second cruise (Fig. 5) where there were high stocks of zooplankton (Fig. 1). 3.4. Migrant zooplankton biomass We calculated diel migrant mesozooplankton biomass from the difference between night- and daytime biomass in the euphotic zone and found that diel vertical migration was greatest for animals in the 1000–2000 mm size fraction and small or negative for the medium zooplankton size fraction (500–1000 mm) and the small zooplankton size fraction (200–500 mm; Fig. 6). Thus, we focus on only the large zooplankton size fraction (1000– 2000 mm) for estimates of active flux. Diel migrant mesozooplankton (1000–2000 mm) biomass was 1.82 and 0.23 mmol C m2 within the equatorial * divergence region (51S–51N) during the El Nino and ‘‘normal’’ conditions of cruises TT007 and TT011, respectively. At higher-latitude oligotrophic regions (9–121S, 9–121N), migrant biomass was similar between the two cruises (2.82 mmol C m2 during TT007 and 2.52 mmol
C m2 during TT011; Fig. 6). The 8-fold higher values within the equatorial divergence during the * conditions were likely a reflection of the El Nino warmer surface waters and deeper mixed layer. The average mixed-layer depth was 51 and 27 m within the equatorial divergence region (51S–51N) during TT007 and TT011, respectively (Murray et al., 1996). Therefore, the higher diel migrant mesozooplankton biomass during TT007 as compared to TT011 within the equatorial divergence region was probably due to a deeper mixed layer during TT007. These results agree with Longhurst’s (1976) observations that diel mesozooplankton vertical migration is more intense in waters with a deeper mixed layer. 3.5. Downward transport of carbon by diel migrant mesozooplankton The mean downward flux of carbon by diel migrant 1000–2000 mm zooplankton in EqPac was 0.08 and 0.01 mmol C m2 d1 within the equatorial divergence region (51S–51N) during
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Fig. 6. Migrant zooplankton biomass (mmol C m2); active migrator flux (mmol C m2 d1) along 1401W near the equator (51S–51N) and oligotrophic stations (9–121S, 9–121N); and, active flux expressed as a % of the gravitational flux.
* and ‘‘normal’’ conditions of cruises the El Nino TT007 and TT011, respectively. Higher, and more similar values of the downward flux of carbon by diel migrant zooplankton were found in higherlatitude (9–121S, 9–121N) oligotrophic regions (0.14 mmol C m2 d1 during TT007 and 0.11 mmol C m2 d1 during TT011). Carbon flux due to diel migrant zooplankton was equivalent to
2% and o1% of the gravitational flux estimated from 234Th measurements by Murray et al. (1996) within the equatorial divergence region (51S–51N) during TT007 and TT011, respectively (Fig. 6). Carbon flux due to diel migrant zooplankton was equivalent to 4% of that from gravitational particle sinking estimated from 234Th measurements by Murray et al. (1996) at higher-latitude oligotrophic regions (9–121S, 9–121N) both during TT007 and TT011. The diel migrant biomass was 6.30 and 12.61 mmol C m2 at 01 and 31S, respectively, during the EBENE study, a value of diel migrant biomass that was higher that that of the EqPac study. The large difference in diel migrant biomass between these studies may be ascribed to the decrease in the intensity of divergence at 1801 (EBENE) as compared to 1401W (EqPac). Because the temperatures varied by only a couple of degrees between the EBENE and JGOFS studies, the zooplankton metabolic rates should be similar between the two areas. We therefore conclude that the amount of carbon transported to deep water by migrant diel migration was higher at 1801W during EBENE as compared to the equatorial stations at 1401W during JGOFS. At a station at 1501W, Le Borgne and Rodier (1997) found that active flux of carbon by migrating zooplankton in relation to the passive flux measured by sediment traps was 4.2%. Zooplankton in the equatorial Pacific Ocean likely contribute more to the gravitational flux of carbon through sinking fecal material. Comparing our estimates of carbon egestion by zooplankton to carbon flux measured by free-drifting sediment traps at the 51S–51N stations along 1401W, we found an average ratio of egestion/sinking flux of 1.5. Clearly, much of the zooplankton fecal material is recycled within the euphotic zone. High temperatures in the surface mixed layer (>251C) are sufficient to decompose fecal pellets in the upper water column (Honjo and Roman, 1978). The consumption of fecal pellets by zooplankton . (e.g., Paffenhoffer and Knowles, 1979) also serves to recycle fecal pellets within the euphotic zone. Our observation that zooplankton biomass is significantly correlated with the sinking flux of phaeopigments (Fig. 3) and the results from
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Rodier and Le Borgne (1997), which suggest that zooplankton fecal pellets contribute approximately 35% of the sinking carbon flux at 01, 1501W, both support the notion that zooplankton can be important contributors to the export flux of carbon in equatorial HNLC areas.
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9725976. Suggestions by Sharon Smith improved an earlier version of this manuscript. Denis Mackey provided helpful editorial suggestions. Hallie Adolf and Adam Spear helped with data analysis. Contribution No. 3556 from the University of Maryland Center for Environmental Science and US JGOFS Contribution No. 796.
4. Summary Estimates of mesozooplankton biomass, grazing, egestion and production in the HNLC area of the equatorial Pacific Ocean are intermediate between the oligotrophic ocean gyre JGOFS time-series stations off Bermuda and Hawaii (Roman et al., 2002), and the JGOFS process studies of the spring bloom in the North Atlantic (Dam et al., 1993), and upwelling area of the Arabian Sea (Roman et al., 2000). Ratios of both mesozooplankton grazing and mesozooplankton production in relation to primary production are lowest near the zone of equatorial upwelling and increase north and south of the equator as zooplankton populations increase in response to the enhanced primary production. Most of phytoplankton production in the HNLC region is consumed by microzooplankton (Landry et al., 1997), with mesozooplankton grazing generally o5% of the phytoplankton standing stock per day (Zhang et al., 1995; Champalbert et al., 2002). Food requirements based on estimated metabolic demands of mesozooplankton, combined with these low phytoplankton ingestion estimates, suggest that most of the diet of equatorial Pacific Ocean mesozooplankton is microzooplankton. Estimates of potential fecal pellet production by mesozooplankton in the HNLC region of the equatorial Pacific Ocean suggest that much of the measured gravitational flux of carbon could be the result of mesozooplankton fecal pellet production.
Acknowledgements This work was part of the US JGOFS and French EBENE studies and was support by National Science Foundation grant OCE
References Altabet, M.A., Small, L.F., 1990. Nitrogen isotopic ratios in fecal pellets produced by marine zooplankton. Geochimica Cosmochimica Acta 54, 155–163. Banse, K., 1992. Grazing, temporal changes of phytoplankton concentration, and the microbial loop in the open ocean. In: Falkowski, P.G., Woodhead, A.D. (Eds.), Primary Productivity and Biogeochemical Cycles in the Sea. Plenum, New York, pp. 409–440. Barber, R.T., Sanderson, M.P., Lindley, S.T., Chai, F., Newton, J., Trees, C.C., Foley, D.G., Chavez, F.P., 1996. Primary production and its regulation in the equatorial Pacific during and following the 1991–92 El Nino. Deep-Sea Research II 43, 970–993. Bidigare, R.R., Ondrusek, M.E., 1996. Spatial and temporal variability of phytoplankton pigment distributions in the central equatorial Pacific Ocean. Deep-Sea Research II 43, 809–834. Blackburn, M., Laurus, R.M., Zeitzschel, B., 1970. Seasonal and areal changes in standing stocks of phytoplankton, zooplankton and micronekton in the eastern tropical Pacific. Marine Biology 7 (1), 14–31. Capriulo, G.M., Sherr, E.M., Sherr, B.F., 1991. Trophic behavior and related community feeding activities of heterotrophic marine protists. In: Reid, P.C., Turley, C.M., Burkhill, P.H. (Eds.), Protozoa and their Role in Marine Processes. Springer, Berlin, pp. 219–265. Champalbert, G., Neveux, J., Gaudy, R., Le Borgne, R., 2002. Diel variations of in situ grazing rates of copepods in the HNLC zone of the equatorial Pacific Ocean (01, 31S, 1801). Journal of Geophysical Research, in review. Chavez, F.P., Barber, R.T., 1987. An estimate of new production in the equatorial Pacific. Deep-Sea Research 34, 1229–1243. Conover, R., 1978. Transformations of organic matter. In: Kinne, O. (Ed.), Marine Ecology, Vol. 4. Dynamics. Wiley, Chichester, pp. 221–499. Cromwell, T., 1953. Circulation in a meridional plane in the central equatorial Pacific. Journal of Marine Research 12, 196–213. Dam, H.G., Miller, C.A., Jonasdottir, S.H., 1993. The trophic role of mesozooplankton at 471N, 201W during the North Atlantic Bloom Experiment. Deep-Sea Research II 40, 197–212.
2710
M.R. Roman et al. / Deep-Sea Research II 49 (2002) 2695–2711
Dam, H.G., Roman, M.R., Youngbluth, M.J., 1995a. Downward export of respiratory carbon and dissolved inorganic nitrogen by diel-migrant mesozooplankton at the JGOFS Bermuda time series station. Deep-Sea Research I 42, 1187–1197. Dam, H.G., Zhang, X., Butler, M., Roman, M.R., 1995b. Mesozooplankton grazing and metabolism at the equator in the central Pacific: implications for carbon and nitrogen fluxes. Deep-Sea Research II 42, 735–756. Eppley, R.W., Peterson, B.J., 1979. Particulate organic flux and planktonic new production in the deep ocean. Nature 282, 677–680. Eppley, R.W., Chavez, F.P., Barber, R.T., 1992. Standing stocks of particulate carbon and nitrogen in the equatorial Pacific at 150 W. Journal of Geophysical Research 97, 655–661. Fowler, S.W., Knauer, G.A., 1986. Role of large particles in the transport of elements and organic compounds through oceanic water column. Progress in Oceanography 16, 147–194. Gaudy, R., Champalbert, G., Le Borgne, R., 2002. Feeding and metabolic features of the mesozooplankton in the Equatorial Pacific HNLC zone. Consequences on particulate biomass. Journal Geophysical Research, in review. Hirst, A.G., Lampitt, R.S., 1998. Towards a global model of in situ weight-specific growth ratesin marine planktonic copepods. Marine Biology 132, 247–257. Hirst, A.G., Sheader, M., 1997. Are in situ weight-specific growth rates body-size independent in marine planktonic copepods? A re-analysis of the global synthesis and a new empirical model. Marine Ecology Progress Series 154, 155–165. Honjo, S., Roman, M.R., 1978. Marine copepod fecal pellets: production, preservation and sedimentation. Journal of Marine Research 36, 45–57. Huntley, M., Boyd, C., 1984. Food limited growth of marine zooplankton. The American Naturalist 124, 455–478. Huntley, M., Lopez, M.D.G., 1992. Temperature-dependent production of marine copepods: a global synthesis. The American Naturalist 140, 201–242. Ikeda, T., 1985. Metabolic rates of epipelagic marine zooplankton as a function of body mass and temperature. Marine Biology 85, 1–11. King, J., Hida, T.S., 1957. Zooplankton abundance in the central Pacific, Part II. Fisheries Bulletin of the US Fish and Wildlife Service 57, 365–395. Landry, M.L., Monger, B.C., Selph, K.E., 1993. Timedependency of microzooplankton grazing and phytoplankton growth in the subarctic Pacific. Progress in Oceanography 32, 205–222. Landry, M.L., Barber, R.T., Bidigare, R.R., Chai, F., Coale, K.H., Dam, H.G., Lewis, M.R., Lindley, S.T., McCarthy, J.J., Roman, M.R., Stoecker, D., Verity, P.G., White, J.R., 1997. Iron and grazing constraints on primary production in the central equatorial Pacific: an EqPac synthesis. Limnology and Oceanography 42, 405–418.
Le Borgne, R., Rodier, M., 1997. Net zooplankton and the biological pump: a comparison between the oligotrophic and mesotrophic equatorial Pacific. Deep-Sea Research 44, 2003–2023. Le Borgne, R., Rodier, M., Murray, J.W., 1999. Zonal variability of plankton and particle export flux in the equatorial Pacific between 1651W and 1501W. Oceanologica Acta 22, 57–66. Le Borgne, R., Barber, R.T., Delcroix, T., Inoue, H.Y., Mackey, D.J., Rodier, M., 2002a. Pacific warm pool and divergence: temporal and spatial variations on the equator and their effects on the biological pump. Deep-Sea Research II 49, 2471–2512. Le Borgne, R., Champalbert, G., Gaudy, R., 2002b. Mesozooplankton biomass and composition in the equatorial Pacific along 180 degrees. Journal of Geophysical Research, in review. Longhurst, A.R., 1976. Vertical migration. In: Cushing, D.H., Walsh, J.J. (Eds.), The Ecology of Seas. Blackwell Scientific Publications, Oxford, pp. 116–137. Longhurst, A.R., Harrison, W.G., 1988. Vertical nitrogen flux from the ocean photic zone by diel migrant zooplankton and nekton. Deep-Sea Research 35, 881–889. Longhurst, A.R., Bedo, A., Harrison, W.G., Head, E.J.H., Sameoto, D.D., 1990. Vertical flux of respiratory carbon by oceanic diel migrant biota. Deep-Sea Research 37, 684–694. Martin, J.H., Gordon, R.M., Fitzwater, S.E., Broenkow, W.W., 1989. VERTEX: phytoplankton/iron studies in the Gulf of Alaska. Deep-Sea Research 36, 649–680. Minas, H.J., Minas, M., Packard, T.T., 1986. Productivity in upwelling areas deduced from hydrographic and chemical fields. Limnology and Oceanography 31, 1182–1206. McCarthy, J.J., Garside, C., Nevins, J.L., Barber, R.T., 1996. New production along 1401W in the equatorial Pacific * event. Deep-Sea during and following the 1992 El Nino Research II 43, 1065–1094. McPhaden, M.J., 1993. TOGA-TAO and the 1992–93 El NinoSouthern Oscillation Event. Oceanography 6, 36–44. Murray, J.W., Johnson, E., Garside, C., 1995. A U.S. JGOFS Process Study in the equatorial Pacific (EqPac). Deep-Sea Research II 42, 275–295. Murray, J.W., Young, J., Newton, J., Dunne, J., Chapin, T., Paul, B., McCarthy, J.J., 1996. Export flux of particulate organic carbon from the central equatorial Pacific determined using a combined drifting trap-Th approach. DeepSea Research II 43, 1095–1132. Omori, M., Ikeda, T., 1984. Methods in Marine Zooplankton Ecology. Wiley, New York, 332pp. . Pafenhoffer, G.A., Knowles, S.S., 1979. Ecological implications of fecal pellet size, production and consumption by copepods. Journal of Marine Research 37, 35–49. Rodier, M., Le Borgne, R., 1997. Export flux of particles in the western and central upper equatorial Pacific, October, 1994. Deep-Sea Research 44, 2085–2113. Rodriguez, J., Mullin, M.M., 1986. Diel and interannual variations in the size distribution of oceanic zooplankton biomass. Ecology 67, 215–222.
M.R. Roman et al. / Deep-Sea Research II 49 (2002) 2695–2711 Roman, M.R., Gauzens, A.L., 1997. Copepod grazing in the equatorial Pacific. Limnology and Oceanography 42, 623–634. Roman, M.R., Dam, H.G., Gauzens, A.L., Urban-Rich, J., Foley, D.G., Dickey, T.D., 1995a. Zooplankton variability on the equator at 140 degrees W during the JGOFS EqPac study. Deep-Sea Research II 42, 673–693. Roman, M.R., Caron, D.A., Kremer, P., Lessard, E.J., Madin, L.P., Malone, T.C., Napp, J.M., Peele, E.R., Youngbluth, M.J., 1995b. Spatial and temporal changes in the partitioning of organic carbon in the plankton community of the Sargasso Sea off Bermuda. Deep-Sea Research 42, 973–992. Roman, M.R., Smith, S., Wishner, K., Zhang, X., Gowing, M., 2000. Mesozooplankton production and grazing in the Arabian Sea. Deep-Sea Research II 47, 1423–1450. Roman, M.R., Adolf, H.A., Landry, M.R., Madin, L.P., Steinberg, D.K., Zhang, X., 2002. Estimates of oceanic mesozooplankton production: a comparison using the bermuda and hawaii time-series data. Deep-Sea Research II 49, 175–192. Ryther, J.H., 1969. Photosynthesis and fish production in the sea. Science 166, 72–76. Slobodkin, L.B., 1961. Growth and Regulation of Animal Populations. Holt, Rhinehart & Winston, New York. Small, L.F., Landry, M.R., Eppley, R.W., Azam, F., Carlucci, A.F., 1989. Role of plankton in the carbon and nitrogen budgets of Santa Monica Basin, California. Marine Ecology Progress Series 56, 57–73. Straile, D., 1997. Gross growth efficiencies of protozoan and metazoan zooplankton and their dependence of food concentration, predator–prey weight ratio, and taxonomic group. Limnology and Oceanography 42, 1375–1385. UNESCO, 1968. Zooplankton Sampling. Monographs on Oceanographic Methodology, Vol. 2. Paris, 174pp. Vinogradov, M.E., 1981. Ecosystems of equatorial upwellings. In: Longhurst, A.R. (Ed.), Analysis of Marine Ecosystems. Academic Press, New York, pp. 69–90.
2711
Vinogradov, M.E., Shushkina, E.A., 1978. Some development patterns of plankton communities in the upwelling areas of the Pacific Ocean. Marine Biology 48 (4), 357–366. Vinogradov, M.E., Voronina, N.M., 1963. Quantitative distribution of plankton in the upper layers of the Pacific equatorial currents. 1. Transactions of the Institute of Oceanology 71, 22–59. Walsh, J.J., 1976. Herbivory as a factor in patterns of nutrient utilization in the sea. Limnology and Oceanography 21, 1–13. Walsh, I.D., Gardner, W.D., Richardson, M.J., Chung, S.P., Plattner, C.A., Asper, V.L., 1997. Particle dynamics as controlled by the flow field of the eastern equatorial Pacific. Deep-Sea Research 44, 2025–2048. Weikert, H., John, H., 1981. Experiences with a modified B!e multiple opening–closing plankton net. Journal of Plankton Research 3, 167–176. Welschmeyer, N.A., Lorenzen, C.J., 1985. Chlorophyll budgets: zooplankton grazing and phytoplankton growth in a temperate fjord and the Central Pacific Gyres. Limnology and Oceanography 30, 1–21. White, J.R., Zhang, X., Welling, L.A., Roman, Dam, H.G., 1995. Latitudinal gradients in zooplankton biomass in the tropical equatorial Pacific at 140 W during the JGOFS EqPac study: effects of El Nino. Deep-Sea Research II 42, 715–733. Wiebe, P.H., Morton, A., Bradley, A., Backas, A., Craddock, J., Barber, V., Cowles, T., Flierl, G., 1985. New developments in the MOCNESS, an apparatus for sampling zooplankton and micronekton. Marine Biology 87, 313–323. Zhang, X., Dam, H.G., 1997. Downward export of carbon by diel migrant mesozooplankton in the central equatorial Pacific. Deep-Sea Research II 44, 2191–2202. Zhang, X., Dam, H.G., White, J.R., Roman, M.R., 1995. Latitudinal variations in mesozooplankton grazing and metabolism in the central tropical Pacific during the US JGOFS EqPac study. Deep-Sea Research II 42, 695–715.
