Active export of carbon and nitrogen at Station ALOHA by diel migrant zooplankton

Deep-Sea Research II 48 (2001) 2083}2103

Active export of carbon and nitrogen at Station ALOHA by diel migrant zooplankton Hussain Al-Mutairi, Michael R. Landry* Department of Oceanography, University of Hawaii at Manoa, 1000 Pope Road, Honolulu, HI 96822, USA

Abstract With a high proportion of diel migratory zooplankton and low particle #uxes, the oligotrophic subtropical Paci"c is a region where migrant-mediated export of materials across the base of the euphotic zone should be particularly important for elemental budgets. To assess the magnitude of this export #ux at Stn. ALOHA (22345N, 1583W), we determined size-structured migrant biomass on 26 cruises (1994}1996) and used allometric equations to compute metabolic losses of respiratory carbon (DIC) and excreted ammonium (DIN) at the migrant's daytime depth (temperature). Depth-integrated (155 m) migrant biomass varied interannually from 286 to 457 mg DW m\ and seasonally from 285 to 550 mg DW m\ (fall versus spring), with an overall average of 394 mg DW m\. The 2}5 mm size-fraction always dominated. Migrant #uxes varied from 0.22 to 0.37 mmol DIC m\ d\ and from 0.033 to 0.055 mmol DIN m\ d\ between years, with an overall average of 0.304 mmol C and 0.045 mmol N m\ d\ (15 and 20% of trap PC and PN #uxes). The #uxes were highest in the spring (0.405 mmol C and 0.060 mmol N m\ d\; 18 and 24% of trap PC and PN). Strong migratory taxa, de"ned as those that were virtually absent from the euphotic zone during the day, were dominated by Pleuromamma and Euphausia spp. and Aetideid copepods and accounted for 40% of the total biomass-derived estimates. Using mean cruise biomass structures and temperature information from Stn. ALOHA, migrant #ux estimates with di!erent literature-derived metabolic relationships and assumptions typically varied within 20% for carbon and 25% for nitrogen. When compared on the same basis, migrant #ux estimates as % trap #uxes were higher for oligotrophic regions compared to the high-nutrient, low-chlorophyll equatorial Paci"c. Long-term averages of migrant biomass were substantially (two- to three-fold) higher in the subtropical Paci"c compared to the Atlantic, but migrant #ux estimates were similar due to higher temperatures (18 versus 93C) at daytime depths in the Atlantic. Including the e!ects of undersampled micronekton, dissolved organic excretion, mortality losses at depth and inter-zonal fecal transport, mean #ux estimates were about doubled for carbon (30% of trap PC) and approximately

* Corresponding author. Fax: #1-808-956-9516. E-mail address: [email protected] (M.R. Landry).  Present address: Kuwait Institute for Scienti"c Research, Department of Fisheries and Aquaculture, P.O. Box 24885, 13109 Safat, Kuwait.

0967-0645/01/$ - see front matter  2001 Elsevier Science Ltd. All rights reserved. PII: S 0 9 6 7 - 0 6 4 5 ( 0 0 ) 0 0 1 7 4 - 0

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tripled for nitrogen (57% of trap PN) relative to those for DIC and DIN metabolic losses.  2001 Elsevier Science Ltd. All rights reserved.

1. Introduction Mesozooplankton are known to contribute to the export of organic material from the upper oceans by producing compact fast-sinking fecal pellets (Pa!enhoK fer and Knowles, 1979; Hofmann et al., 1981; Small et al., 1983, 1987). More recently, the regular crossings of the base of the euphotic zone by diel inter-zonal migrants have been recognized to provide other mechanisms for signi"cant export. Longhurst et al. (1988, 1989, 1990) and Dam et al. (1995) focused initially on losses of respiratory carbon and inorganic nitrogen excretion at the daytime depths of migrants. Le Borgne and Rodier (1997) and Steinberg et al. (2000) expanded this analysis with evidence of signi"cant excretory losses of DOC and DON. Zhang and Dam (1997) included additional consideration for mortality losses at depth. These studies give varying estimates of the magnitude of `activea migrant #ux and its relation to passive particle settling for the subtropical Atlantic and equatorial Paci"c. Direct comparison is di$cult, however, because the studies are based on di!erent sets of empirical metabolic relationships and assumptions, they vary from short-term cruise estimates to long-term system averages, and they include di!erent processes to varying degrees. The goal of the present study is to provide annual and seasonal averages for migrant-mediated export #uxes at Stn. ALOHA, a time-series sampling site in the oligotrophic central North Paci"c (Karl and Lukas, 1996). Hypothetically, the relative importance of migrant #uxes in elemental budgets should be maximal under severely oligotrophic conditions where the proportion of migrating zooplankton is typically high and where deep euphotic zones and rapid recycling allow only a small fraction of production to settle passively as particles. Given existing studies, active DIC and DIN #ux estimates from this area will give a relevant basis of comparison between subtropical regions of di!erent oceans and between equatorial and subtropical regions of the Paci"c. To facilitate these comparisons, our analysis includes the e!ects of di!ering metabolic relationships on migrant #ux calculations. In addition, we explore how other migrant-related mechanisms * organic excretion, deep mortality and fecal transport * in#uence our #ux estimates.

2. Materials and methods 2.1. Sample collection The present analyses are based on zooplankton samples collected at Stn. ALOHA ($10 km from 22345N,158300W; Karl and Lukas, 1996) on Hawaii Ocean Time-Series (HOT) cruises from 1994 to 1996. The samples were taken with a 1-m plankton net with 0.2-mm Nitex mesh equipped with a General Oceanics #owmeter (GO, Miami, FL) and a Brancker Model XL-200 temperature}pressure recorder (R. Brancker Research, Ottowa, Canada). For most cruises, three daytime (1000}1400) and three nighttime (2200}0200) tows of approximately 20-min duration were taken

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obliquely from the surface to a mean depth of 155 m. This roughly coincides with the lower limit of the `euphotic zonea, as de"ned by the depth of penetration of 0.1% of incident photosynthetically available radiation (PAR). Contents of the net cod ends were subsampled on shipboard with a Folsom plankton splitter. Generally, half of the tow was preserved in a bu!ered 4% formalin-seawater solution for community analysis, and one-quarter was wet sieved through nested screens of 5-, 2-, 1-, 0.5- and 0.2-mm mesh for determination of size-fractioned biomass and abundance. The organisms in each of the size fractions (0.2}0.5, 0.5}1, 1}2, 2}5 and '5 mm) were concentrated onto preweighed 0.2}mm Nitex "lters, rinsed with isotonic ammonium formate to remove sea salt, placed in individual cryotubes, and #ash frozen in liquid N for later analysis.  2.2. Biomass and abundance In the laboratory, thawed "lters were blotted brie#y to remove excess water and analyzed (Mettler Model AE 160) for wet weight before and after duplicate random subsamples were taken for enumeration and for carbon-nitrogen determinations (Landry et al., 2001). The remaining sample was dried in a 603C oven for at least 24 h before weighing again for dry biomass. Zooplankton dry weight (DW) was computed for each size fraction from total wet weight (less "lter), the ratio of dry to wet weight, and the fraction of the net haul that was sized-sorted. Replicate subsamples for CHN analyses were placed into precombusted and preweighed aluminum boats, dried in a dessicator for at least 24 h, and weighed. Carbon and nitrogen contents and C : DW and N : DW ratios were then determined, relative to acetanilide standards, by combustion in a Perkin-Elmer Model 2400 CHN Elemental Analyzer. C : DW and N : DW ratios were not statistically di!erent between years or between day and night samples for individual size fractions ( p(0.05; t-test assuming unequal variances; Sokal and Rohlf, 1981). However, the ratios were di!erent among size fractions and between 1996 and other years for the 0.2}0.5 mm fraction. Therefore, carbon and nitrogen estimates for size classes '0.5 mm were pooled and averaged for subsequent calculations. For the 0.2}0.5 mm fraction, the 1994}95 estimates were averaged, and the 1996 estimates were used for that particular year. Total abundances of '5 mm animals were estimated by counting all of the identi"able organisms retained on the 5-mm screen in the wet size-fractions and/or in size-fractioned preserved samples (i.e., 50% of total sample). Zooplankton in the smaller size fractions were enumerated under a stereo-dissecting microscope from the replicate wet-fractioned subsamples. Mean abundance (number m\) and individual biomass (C, N or DW animal\) of zooplankton in each size fraction were determined from the mean numbers DW\ in the enumerated subsamples, the C : DW and N : DW ratios, and the estimated DW m\ of the size fraction in the net tow. To complement estimates of total zooplankton abundance from the frozen size-fractioned samples, formalin-preserved samples from one day and one night tow per cruise were analyzed microscopically for community composition. The samples were size-fractionated under a fume hood in the same manner as the subsamples were taken at sea. All of the '5 mm size class and 25}100% of the 2}5 mm fraction were counted. For the smaller size classes, several hundred to several thousand animals were enumerated per subsample analyzed. The subsamples were sorted to the lowest practical taxon, with particular attention to animals in the 0.5 to '5 mm size categories, which contained the bulk of the inter-zonal migrants. Copepods were taken to species

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where possible, and euphausiids were enumerated at the genus level. Other animals (chaetognaths, larvaceans, salps, etc.) were sorted to the group level, with a few to family or genus. A number of species exhibited strong migratory behavior, as evident by their presence in signi"cant numbers in nighttime net samples and their virtual absence in day samples. For each common taxon so identi"ed, individual biomass (DW) estimates were obtained by picking specimens from previously frozen (unpreserved) samples thawed in "ltered seawater. The animals were rinsed in isotonic ammonium formate, placed in like groups on preweighed Nitex screens, and dried in a 603C oven for several days before weighing. In the case of myctophid "sh, biomass estimates were based on Formalin-preserved individuals. For uncommon species or groups, we estimated individual dry weight from other organisms of comparable size. 2.3. Metabolic rate estimates Metabolic rate estimates for the size-fractioned zooplankton were calculated from the empirical allometric relationships of Ikeda (1985). These relationships were based on experiments with numerous (56}143) species, representing 7}8 phyla and habitat temperatures from !1.4 to 303C. Respiration rate estimates (RO:
l O organism\ h\) were determined from the average of  calculations based on three measures of individual body mass (DW, C and N; mg organism\) and environmental temperature T (3C) according to the following: ln RO"!0.251#0.789 ln DW#0.490 ¹, ln RO"0.525#0.835 ln C#0.0601 ¹, ln RO"1.741#0.850 ln N#0.0636 ¹. These rate estimates were converted to respiratory carbon equivalents (RC:
g C organism\ h\) as RC"RO;RQ;12/22.4, where RQ (respiratory quotient) is the molar ratio of carbon produced to oxygen utilized, 12 is the molecular weight of carbon, and 22.4 is the molar volume of an idealized gas at standard temperature and pressure. We assumed an RQ of 0.8, implying a largely protein-based diet for the migrating mesozooplankton of this region (Hayward, 1980). Ammonium excretion rates (E:
g N organism\ h\) were calculated similarly: ln E"!2.890#0.762 ln DW#0.051 ¹, ln E"!2.176#0.829 ln C#0.0648 ¹, ln E"!0.966#0.836 ln N#0.0656 ¹. Mean temperatures experienced by the zooplankton were determined from cruise-averaged CTD data from the surface to the maximum depth of each net tow and for the assumed daytime depth range of migrating zooplankton, 300}600 m (Longhurst and Harrison, 1988; Wiebe et al., 1992). Over the course of the study, temperatures varied from 21.8 to 24.93C (mean$standard deviation"23.2$0.953C) for the former and from 8.1 to 10.13C (9.0$0.453C) for the latter. Hourly estimates of C and N metabolism were converted to daily rates assuming migrants resided 12 h at depth during the day and 12 h in the euphotic zone at night. Carbon and nitrogen #uxes associated with the total migrating zooplankton assemblage were determined from the di!erences between size-fractioned nighttime and daytime mean biomass

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estimates for each cruise. These biomass di!erences were divided by nighttime cruise-averaged estimates of individual biomass to yield the number of migrating animals in each size fraction. Total metabolic losses at the daytime depths of migrating zooplankton were then calculated from the respiration and excretion rate equations above, given cruise-mean estimates of individual biomass, the relevant ambient temperature, and the number of migrants m\ in each size fraction. A more conservative estimate of active migrant #ux was similarly determined from the abundances and individual biomass estimates of strongly migrant taxa. 2.4. Statistical analyses For analysis of variability, values were "rst transformed to natural logarithms to normalize the data before performing statistical tests (t-tests, assuming unequal variances, or one-way ANOVA). Data distributions were considered to be normal if the p-value of the Kolomogorov}Smirnov test was '0.05, and they were generally '0.15 for most data. Variances were considered equal, for one-way ANOVA, if the p-value of Bartlett's test was *0.05 (Sokal and Rohlf, 1981). Test results are reported as signi"cant for p-values )0.05 (two-tailed).

3. Results 3.1. Migrant biomass Cruise-averaged dry weights of mesozooplankton at Stn. ALOHA are presented by year in Table 1 and by season in Table 2. All di!erences between day and night total biomass estimates were highly signi"cant ( p)0.001), as were most di!erences for individual size fractions. In July 1994, however, day exceeded night estimates for the '1 mm fractions. Over the three years of study, nighttime biomass averaged 960 mg DW m\, of which 390 mg m\ was the nocturnal enhancement due to diel migrants (Table 1). N : D biomass ratios increased with animal size from 1.4 for the 0.2}0.5 mm size-fraction to 5.4 for the '5 mm fraction. However, since '5 mm biomass was low, the next larger size category (2}5 mm animals) contributed most to total migrant biomass for all years and seasons (Tables 1 and 2). Animals in the smallest fraction (0.2}0.5 mm) generally contributed least to migrant biomass, except during the fall season. Among years, total nighttime biomass and total migrant biomass were lowest in 1994 and highest in 1996 (Table 1). The 1996 values were principally due to signi"cantly elevated nocturnal biomass in the 0.5}1 and 1}2 mm fractions during summer and early spring (Landry et al., 2001). Among seasons, total night biomass and total migrant biomass were signi"cantly higher in spring (April}June) and summer (July}September) than in the winter (January}March) and fall (October}December) seasons (Table 2). The daytime standing stocks of smaller zooplankton ((2 mm) were signi"cantly higher in summer, resulting in little change in migrant biomass and lower N : D biomass ratios in these fractions relative to winter and fall seasons. Consequently, for summer and to a lesser extent spring, seasonal di!erences in migrant biomass were mainly due to increases in the standing stocks of zooplankton in the larger ('2 mm) size categories. Rodriguez and Mullin (1986) found that zooplankton at the central Paci"c CLIMAX (283N, 1553W) site had higher N : D biomass ratios in winter (2.8) and spring (3.4) than summer (2.1). That result is also evident in the

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Table 1 Interannual comparison of mean biomass estimates (mg DW m\) for night and day net tows, mean migrant biomass (night}day di!erence, mg DW m\), and mean night : day (N : D) biomass ratios for mesozooplankton size-fractions at Stn. ALOHA Year/size class

Night biomass

Day biomass

Migrant biomass

N : D ratio

Mean

S.D.

Mean

S.D.

0.5}1.0 mm 1.0}2.0 mm 2.0}5.0 mm '5.0 mm Total ('0.2 mm)

161 177 194 195 92 820

53 64 55 69 42 252

130 153 144 87 20 534

60 86 82 39 15 238

31 24 50 107 73 286

1.40 1.37 1.82 2.60 7.30 1.73

1995 0.2}0.5 mm 0.5}1.0 mm 1.0}2.0 mm 2.0}5.0 mm ' 5.0 mm Total ('0.2 mm)

147 185 209 255 94 890

52 44 52 100 47 205

109 121 135 77 40 482

57 40 65 41 49 159

38 64 74 178 54 408

1.49 1.63 1.75 3.75 5.34 1.93

1996 0.2}0.5 mm 0.5}1.0 mm 1.0}2.0 mm 2.0}5.0 mm '5.0 mm Total ('0.2 mm)

184 285 284 276 82 1111

80 139 127 156 72 405

148 188 183 111 24 654

59 93 56 65 16 182

37 97 101 165 58 457

1.27 1.57 1.55 2.60 4.18 1.71

Grand average 0.2}0.5 mm 0.5}1.0 mm 1.0}2.0 mm 2.0}5.0 mm '5.0 mm Total ('0.2 mm)

165 221 234 247 89 956

64 106 95 119 55 323

130 157 156 93 28 562

59 79 67 52 31 198

35 66 78 154 60 394

1.38 1.54 1.69 3.00 5.42 1.79

1994

present study, although the mean ratios are lower for all seasons (N : D"2.1 winter, 2.0 spring and 1.5 summer) than previously described. 3.2. Composition of the migratory community Copepods dominated the mesozooplankton at Stn. ALOHA, averaging 80% of all animals in daytime collections and 77% at night (Landry et al., 2001). Copepods were also the most abundant group among the zooplankton exhibiting strong migratory behavior (Table 3). Species of the genus Pleuromamma were particularly numerous in the 0.5}1 mm (P. piseki and gracilis) and the 1}2 mm

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Table 2 Seasonal comparison of mean biomass estimates (mg DW m\) for night and day net tows, mean migrant biomass (night}day di!erence, mg DW m\), and mean night : day (N : D) biomass ratios for mesozooplankton size-fractions at Stn. ALOHA Season/size class

Night biomass Mean

Winter (January}March) 0.2}0.5 mm 0.5}1.0 mm 1.0}2.0 mm 2.0}5.0 mm '5.0 mm Total ('0.2 mm)

130 179 186 182 58 736

Day biomass S.D.

54 42 54 56 41 144

Migrant biomass

N : D ratio

Mean

S.D.

95 103 100 70 18 385

47 49 65 32 15 184

35 76 86 111 40 350

1.51 1.91 2.30 2.93 5.63 2.11

Spring (April}June) 0.2}0.5 mm 0.5}1.0 mm 1.0}2.0 mm 2.0 } 5.0 mm '5.0 mm Total ('0.2 mm)

164 220 253 320 133 1090

70 81 78 180 61 343

119 126 143 121 32 540

34 36 36 90 14 145

44 94 110 200 102 550

1.37 1.74 1.79 3.19 4.80 2.02

Summer (July}September) 0.2}0.5 mm 0.5}1.0 mm 1.0}2.0 mm 2.0}5.0 mm '5.0 mm Total ('0.2 mm)

208 280 271 276 99 1132

72 151 135 87 52 374

181 230 208 89 31 740

68 89 51 29 48 150

27 49 63 187 67 392

1.28 1.22 1.34 3.52 6.97 1.54

Fall (October}December) 0.2}0.5 mm 0.5}1.0 mm 1.0}2.0 mm 2.0}5.0 mm '5.0 mm Total ('0.2 mm)

145 187 213 202 62 809

30 82 72 96 37 174

107 138 155 94 31 524

29 52 72 38 33 143

38 50 59 108 31 285

1.40 1.38 1.46 2.17 3.75 1.59

(P. abdominalis and xiphias) fractions. Overall, they comprised 76% of the animals captured in the euphotic zone at night but rarely during the day (Table 3). Copepods of the family Aetideidae, including the genera Euchirella, Undeuchaeta, Aetideus, Gaetanus and Chiridius, were also well represented among the small migrating taxa, accounting for 4.5% of the strong migrants. Euphausiids were most abundant in absolute terms in the 1}2 mm fraction, but they were relatively more important among the strong migrant taxa in the 2}5 mm size category, the fraction contributing most to total migrant biomass. Myctophid "sh and large shrimp and euphausiids were approximately equally represented in the largest ('5 mm) fraction. Gelatinous zooplankton,

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Table 3 Mean nighttime abundances (number m\) and size distributions of strong migratory taxa at Stn. ALOHA. Table includes only those animals that were virtually absent from the euphotic zone in daytime net tows. Within groups, species are listed in order of numerical abundance Taxon

Copepods Pleuromamma immature Pleuromamma piseki female Phaena spinifera Pleuromamma piseki & gracilis male Pleuromamma abdominalis Pleuromamma gracilis female Pleuromamma xiphias Heterorhabdus papilliger Undeuchaeta plumosa Gaetanus minor Candacia longimana Paraeuchaeta media Lophothrix latipes Euchirella curticauda Euchirella immature Euchirella spp. Chiridius poppei Euchirella indica Scottocalanus securifrons Aetideus acutus Euchirella amoena Heterorhabdus spinifrons Chirundina streetsi Pleuromamma quadrungulata Heterostylites sp. Paraeuchaeta spinosa Undeuchaeta major Arietellus armatus Ostracods Euphausiids Euphausia spp. Thysanopoda spp. Nematoscelis spp. Nematobrachion yexipes Penaeid shrimp Sergestid shrimp Caridean shrimp Fish Myctophid Melanostomiatid

Size fraction (mm) 0.5!1

1!2

399 154 190 149

28.9 59.4 0.5 7.8 140.0 7.0 59.4 5.4 28.0 7.6 12.7 11.1 5.0 5.8 6.1 2.6

132 50.7 10.3

1.8

2!5

'5

1.0 3.9 1.0 0.5 0.3 0.5 0.3

2.7 1.7 1.9 1.3 0.8

1.0 0.3 1.0 0.1 0.6

0.4 0.4

15.2 96.7

0.4 0.2 0.1 0.7 20.2 2.20 0.51 0.15 0.42

0.19 0.34 0.06 0.10 0.37 0.14 0.06

0.57 0.03

0.45

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including salps and siphonophores, were also present in the '5 mm size fraction in both day and night tows. However, because they were relatively rare and not identi"ed to species or genus, their diel migratory behaviors could not be unambiguously determined. 3.3. Active migratory yuxes Export #uxes of carbon and nitrogen computed from total migrant biomass at Stn. ALOHA are presented as individual cruise estimates in Figs. 1 and 2 and as mean annual and seasonal rates in Table 4. Overall, migratory export averaged 0.304 mmol C and 0.045 mmol N m\ d\, corresponding, respectively, to 15 and 20% of measured particulate carbon (PC) and nitrogen (PN) #uxes in sediment traps (150 m). The highest cruise estimates were obtained for July 1996 (0.77 mmol C and 0.115 mmol N m\ d\, representing 25 and 35% of PC and PN #uxes), and the lowest were calculated for September 1994 (0.084 mmol C and 0.012 mmol N m\ d\"5.6% of PC and 6.6% of PN trap #uxes). Interannual and seasonal di!erences in #ux estimates roughly followed the pattern for total migrant biomass. The lowest mean annual rates estimates were determined for 1994 (0.22 mmol C and 0.033 mmol N m\ d\) and the highest for 1996 (0.37 mmol

Fig. 1. Seasonal and interannual variations in migratory #ux (mmol C m\ d\ and % of particulate carbon collected in sediment traps) for respiratory carbon at daytime depth. Data are mean cruise estimates for 1994}1996.

Fig. 2. Seasonal and interannual variations in migratory #ux (mmol N m\ d\ and % of particulate nitrogen collected in sediment traps) for excreted ammonium at daytime depth. Data are mean cruise estimates for 1994}1996.

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Table 4 Estimates of carbon and nitrogen export #uxes (mmol m\ d\) associated with daytime metabolic losses of migratory zooplankton at Stn. ALOHA. Flux estimates based on allometric relationships and total size-fractioned migrant biomass. N"number of cruises averaged in period grouping. % trap #ux"mean percentage of active migratory #ux estimate divided by passive trap #ux measured at 150}m depth on the same cruises Period

N

Carbon #ux

Nitrogen #ux

Mean

Std. Dev.

% Trap C Flux

Mean

Std. Dev.

% Trap N Flux

7 9 10

0.220 0.295 0.371

0.120 0.016 0.235

11.3 15.8 17.8

0.033 0.043 0.055

0.018 0.004 0.035

14.8 21.5 23.5

Winter Spring Summer Fall

6 6 8 6

0.270 0.405 0.317 0.220

0.084 0.190 0.317 0.115

16.2 18.3 13.8 12.4

0.040 0.060 0.047 0.032

0.013 0.028 0.034 0.017

23.1 24.4 18.8 16.1

Overall

26

0.304

0.173

15.3

0.045

0.026

19.9

1994 1995 1996

C and 0.055 mmol N m\ d\). The greatest rate discrepancies between 1994 and 1996 were observed for spring and early summer cruises (Figs. 1 and 2). Rate estimates were highly variable during other times of the years, however, and interannual di!erences were not statistically signi"cant (t-test, p'0.1). Seasonally, migrant #uxes were highest in the spring and summer months, largely due to high rate estimates from 1996. Migratory #uxes calculated from the biomass and size composition of strong migratory animals in taxonomically sorted night samples averaged 39% of the carbon estimates and 40% of the nitrogen estimates from cruise-averaged night and day biomass di!erences (Table 5). The dominant migratory taxa, Euphausia spp. and copepods of the genus Pleuromamma and family Aetideidae, accounted for 85% of the #uxes of DIC and DIN calculated from sorted night samples. Occasionally, and with no coherent pattern among years or seasons, the #ux associated with readily identi"ed migrants exceeded that of the total size-fractioned biomass (Fig. 3). More typically, strong migrators accounted for (40% of the total migrant #ux, implying that most of the nocturnal enhancement in mesozooplankton biomass at Stn. ALOHA comes from organisms whose vertical distributions at least partially overlap the euphotic zone during the day. 3.4. Sensitivity of rate calculations The migratory #ux estimates presented above were calculated for a given set of empirically based metabolic equations and assumptions (Ikeda, 1985). In order to evaluate the sensitivity of the computed values, we applied several di!erent sets of empirical relationships and assumptions to the size-structured zooplankton data from Stn. ALOHA. The common features in these comparisons were environmental temperatures and cruise estimates of zooplankton migrant biomass in the

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Table 5 Estimates of carbon and nitrogen #uxes (mmol m\ d\) associated with daytime metabolic losses of strong migratory zooplankton at Stn. ALOHA. Strong migrators were those taxa determined from microscopical analysis of preserved samples to be virtually absent from the euphotic zone during daylight hours (Table 3). `% Strong Migranta is the mean percentage of the total #ux estimate (Table 4) attributed to strongly migrant taxa. `% Major Taxaa is the percentage of #ux estimate for strong migrators attributed to dominant taxa (Euphausia spp. and copepods of the genus Pleuromamma and family Aetideidae). N"number of cruises averaged Period

N

Carbon #ux

Nitrogen #ux

Mean

Std. Dev.

% Strong migrant

% Major taxa

Mean

Std. Dev.

% Strong migrant

% Major taxa

7 9 10

0.101 0.105 0.140

0.031 0.050 0.087

45.9 35.6 37.7

82.7 84.4 86.8

0.015 0.016 0.021

0.005 0.008 0.013

45.4 37.2 32.7

83.2 85.1 87.0

Winter Spring Summer Fall

6 6 8 6

0.110 0.134 0.134 0.083

0.028 0.071 0.089 0.038

40.8 33.1 42.5 38.1

88.8 86.1 82.0 83.5

0.017 0.020 0.020 0.013

0.004 0.011 0.013 0.006

42.1 34.1 43.6 39.6

89.2 86.8 82.2 84.2

Overall

26

0.117

0.064

38.4

84.9

0.018

0.010

40.0

85.3

1994 1995 1996

Fig. 3. Seasonal and interannual variations in migratory #ux (mmol N m\ d\ and % of total migratory N #ux) attributable to strong migratory taxa at Stn. ALOHA. Data are mean cruise estimates for 1994}1996.

0.2}2 mm size fractions, the applicable range for metabolic rate estimates in the various studies. Variables included the di!erent metabolic rate versus weight relationships, the Q temperature  e!ects on metabolic rates and the respiratory quotients (RQ), as provided by or determined from the original studies. According to these comparisons, relatively good agreement exists among the various approaches for estimating respiratory carbon loss (Table 6). Calculations based on the Vidal and Whitledge (1982) rate relationships conformed the most closely to those from the Ikeda (1985) equations, showing no signi"cant di!erence on average. Of the studies showing higher rate ratios relative to Ikeda (1985), con"dence limits for the Le Borgne and Rodier (1997) HNLC relationship would

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Table 6 Sensitivity of migratory #ux estimates at Stn. ALOHA to di!erent empirical relationships for metabolic rates (carbon respiration and inorganic nitrogen excretion) as a function of mesozooplankton biomass. Each example applies the empirical relationships for the cited study to the 0.2}2 mm size fractions of the mesozooplankton community and the environmental temperature at Stn. ALOHA (this study). RQ"respiratory quotient (CO generated : O consumed)   ("0.8). Q "rate multiplying factor for temperature increase of 103C. `Ratea gives the means and standard deviations  (std. dev.) for #ux rate estimates (N"26 cruises). `Ratioa gives the mean rate ratios and con"dence intervals (95% C.I.) for rate estimates based on the cited study divided by those computed from Ikeda (1985) equations (N"25 cruises where night/day biomass '1.0) Study

Carbon #ux (DIC) Ikeda (1985) Vidal and Whitledge (1982) Longhurst et al. (1990) LeBorgne and Rodier (1997) Oligotrophic Paci"c HNLC Equatorial Paci"c Steinberg et al. (2000) Nitrogen #ux (DIN) Ikeda (1985) Mullin et al. (1975) Vidal and Whitledge (1982) Longhurst et al. (1989) LeBorgne and Rodier (1997) Oligotrophic Paci"c HNLC Equatorial Paci"c

RQ

Q 

Rate (mmol m\ d\)

Rate ratio

Mean

Std. Dev.

Mean

95% C.I.

0.8 0.8 1.0

1.78 2.00 2.54

0.212 0.213 0.233

0.156 0.156 0.170

* 1.01 1.12

* 0.98}1.04 1.03}1.21

0.8 1.0 1.0

3.83 3.31 2.50

0.242 0.296 0.086

0.178 0.216 0.065

1.17 1.34 0.41

1.06}1.27 1.19}1.49 0.37}0.45

1.84 2.00 2.00 2.60

0.034 0.025 0.025 0.028

0.025 0.018 0.019 0.021

* 0.73 0.75 0.86

* 0.69}0.77 0.71}0.79 0.79}0.93

2.63 2.85

0.055 0.037

0.040 0.027

1.67 1.11

1.53}1.81 1.01}1.21

Indicates Q "2.0 if not given in the original study. 

overlap 1.0, and those for Longhurst et al. (1990) would be slightly under, if all rates were calculated with an equivalent RQ ("0.8). With this modest adjustment, only the Le Borgne and Rodier (1997) relationship for the oligotrophic, western equatorial Paci"c yields consistently higher estimates than Ikeda (1985), 17% on average for conditions at Stn. ALOHA. On the other extreme, rate estimates based on Steinberg et al. (2000) are markedly lower than other relationships because the approach applies measured rates for relatively large animals to the whole migrating community without correction for the higher weight-speci"c rates of small migrants. Rate estimates for nitrogen excretion exhibited greater variability than carbon metabolism, ranging about a factor of two for the di!erent empirical relationships. For the present data set, calculations based on the Ikeda (1985) relationships agreed most closely ($15%) with rates computed according to Longhurst et al. (1990, 1989) and the HNLC equatorial relationship from Le Borgne and Rodier (1997). Rate estimates based on Mullin et al. (1975) and Vidal and Whitledge (1982) were about 25% lower than those based on the Ikeda (1985), and Le Borgne and Rodier (1997) relationship for the oligotrophic western Paci"c gave results 50}80% higher.

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3.5. Nitrogen excretion in the euphotic zone To assess the contribution of mesozooplankton to phytoplankton nitrogen demand in the euphotic zone, we calculated nitrogen excretion from the Ikeda (1985) relationships using mean euphotic zone temperatures (range 21.8}24.93C), day and night estimates of mesozooplankton and summing their respective rates for 12 h each per day. Phytoplankton nitrogen demand was determined from depth-integrated C production and a C : N ratio of 6.8 for euphotic zone particulate matter (D.M. Karl, pers. comm.). Mean estimates of zooplankton excretion were lowest in 1995 and highest in 1996, accounting for 7.2 and 10.9% of the nitrogen required for primary production (Table 7). Seasonally, excretion rates were highest during summer and spring months, when mesozooplankton biomass was elevated. However, fall replaced spring as the second highest season in terms of the percentage of primary production supported because phytoplankton N demand was substantially reduced in fall compared to spring. Overall, mesozooplankton excretion in the upper waters averaged 0.46 mmol N m\ d\, supplying 9.1% of the nitrogen required for primary production. 4. Discussion 4.1. Assumptions and sampling errors As discussed in detail by Zhang and Dam (1997), assessing the contributions of migrating zooplankton to export #uxes from the upper oceans involves many assumptions about capture e$ciencies, depth distributions and feeding habits of the migrant populations. In the present study,

Table 7 Mesozooplankton contribution to nitrogen excretion and phytoplankton nitrogen demand (mg N m\ d\) in the euphotic zone at Stn. ALOHA. N"number of cruises averaged in period grouping. Excretion estimates based on nighttime and daytime standing stocks and size distributions and mean euphotic zone temperature per Ikeda (1985). Phytoplankton nitrogen demand"C primary production times 0.15 (N : C ratio). % PP supported"mean percentage of primary production supported by computed excretion rates for all cruises in the time period identi"ed Period

N

Zooplankton excretion

Phytoplankton Nitrogen demand

% PP supported

Mean

Std. Dev.

7 9 10

0.435 0.397 0.544

0.138 0.101 0.215

4.74 5.49 4.97

9.2 7.2 10.9

Winter Spring Summer Fall

6 6 8 6

0.310 0.477 0.596 0.426

0.062 0.135 0.192 0.107

4.28 6.02 5.60 4.28

7.4 8.5 10.9 10.4

Overall

26

0.463

0.170

5.49

9.1

1994 1995 1996

2096

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we implicitly assumed that day}night biomass di!erences in the euphotic zone re#ected true migrant biomass, rather than daytime net avoidance, and that the animals fed only in the euphotic zone at night and resided well below (300}600 m) the euphotic zone during the day. These assumptions are generally consistent with the known behaviors of strongly migrating taxa in the subtropical North Paci"c and elsewhere. For instance, our nighttime abundances of Pleuromamma spp., Aetideidae and Euphausia spp. in the euphotic zone are comparable to estimates for the 400}550 m depth range in daytime collections (Clarke, 1982). In addition, many of the same species undergo well-documented diel migrations to similar depths in the subtropical Atlantic (Wiebe et al., 1992). Regarding feeding patterns, Hayward (1980) observed pronounced nocturnal feeding for all Pleuromamma species in the central Paci"c, with little or no food in the guts of animals caught in deep daytime samples. Similar diel feeding rhythms have been noted for deep migratory copepods and euphausiids in other tropical as well as temperate systems (Roger, 1975; Hu, 1978; Longhurst et al., 1989; Stuart and Pillar, 1990). Zhang and Dam (1997) reported no statistically signi"cant di!erence between day and night estimates of depth-integrated zooplankton biomass to 1000 m in the equatorial Paci"c, implying little daytime net avoidance. Since their collections were made with a 0.25-m net, we assumed that our 1-m net, "shed at comparable speeds, would also quantitatively sample most of the zooplankton size fractions. Nonetheless, undersampling of larger animals, such as shrimp and "sh, is suggested by the drop-o! in biomass for the '5-mm size fraction. Previous studies on the vertical migrations of mesopelagic micronekton o! Hawaii place some constraints on the magnitude of this potential error. Based on quantitative catches with large mid-water trawls, for example, Maynard et al. (1975) showed a nocturnal increase of about 2.3 g wet weight m\ for mesopelagic "shes (60%) and crustaceans (40%) in the upper 400 m. Assuming that dry weight is 10% and that all migrant biomass is concentrated in the euphotic zone at night, the maximum error in our estimate of the '5-mm size fraction is about a factor of 4. In its extreme, this error (170 mg DW m\) represents a 40% increase in the total migrant biomass for all size fractions. Assuming a lower mean daytime temperature (53C) and lower weight-speci"c rates for these larger migrating organisms (mean"60 mg DW indiv\; Maynard et al., 1975), their metabolism increases migrant #ux by about 12%. Since strong migrating taxa comprised only 40% of the average day}night biomass di!erence in the present study, the remaining 60% may have had characteristics that conformed less well to the assumptions of the #ux calculations. These smaller and weaker migrants resided partially within the euphotic zone during the day; consequently, their contributions to export #ux may have been understated by asynchronous vertical excursions throughout the day and night (Pearre, 1979) and by temperature-enhanced metabolic rates at shallower depths (e.g., 150}300 m versus 300}600 m). However, if these organisms also derived signi"cant nutrition by daytime feeding below the euphotic zone, the calculated release of metabolic by-products at depth would be an overestimate of materials exported from the euphotic zone (Zhang and Dam, 1997). The net e!ects of these opposing complications are unknown, but they are assumed to cancel one another in the present analysis. 4.2. Migratory yuxes in tropical and subtropical oceans During the period of the present study, 1994}1996, annual primary production at Stn. ALOHA averaged 14.7 mol C m\, and mean export #uxes of 0.72 mol C and 0.08 mol N m\ yr\ were

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measured by passive particle accumulation in sediment traps (HOT database * http://hahana.soest.hawaii.edu). According to our calculations, mesozooplankton nutrient cycling in the euphotic zone accounted for 9% of the nitrogen required for primary production, and active migrants exported 0.110 mol C and 0.016 mol N m\ yr\, or about 15 and 20%, respectively, of the passive trap #uxes. Somewhat surprisingly, given the complications inherent to metabolic rate measurements (e.g., variable e!ects due to capture stress, crowding, feeding histories, experimental duration and phylogenetic di!erences), our migrant #ux estimates proved relatively insensitive to the varying metabolic relationships and assumptions from other studies. Assuming an RQ of 0.8, for instance, migrant #uxes of 0.099}0.141 mol C m\ yr\ (14}19% of PC trap #uxes) include 95% con"dence limits for all calculations based on respiration relationships from Vidal and Whitledge (1982), Longhurst et al. (1990) and Le Borgne and Rodier (1997). The full range in con"dence limits for metabolic losses of inorganic nitrogen is a little broader (0.011}0.030 mol N m\ yr\; 14}36% of trap PN), but reasonably well constrained by all possible assumptions. Among the various estimates of migrant-mediated export #uxes in tropical and subtropical oceans, migrant biomass estimates vary by about a factor of 4 and calculated #uxes have a 10-fold range (Table 8). At "rst glance, carbon-based estimates from Stn. ALOHA are most similar to those for the central equatorial Paci"c during El Nin o conditions (i.e., March}April 1992; Zhang and Dam, 1997), which are based on similar calculations from Ikeda (1985) relationships. We believe, however, that the rate estimates of Zhang and Dam (1997) require modi"cation. First, the migrant biomass estimates for March}April 1992 are exaggerated by the arbitrary rejection of data from 4 of 10 sampling dates for which the N-D biomass di!erence was negative. As a simple correction for these missing data, we multiply the reported mean biomass times 0.6, essentially assuming `zeroa migrant biomass for these four sampling dates. Second, Zhang and Dam (1997) compared their migrant #uxes to Th estimates of PC #uxes from Bacon et al. (1996), 1.9 and 2.4 mmol C m\ d\ for March}April and October, respectively. Because all other comparisons in Table 8 use PC estimates from sediment traps, we recalculated % trap PC using 150-m trap #uxes reported by Murray et al. (1996). These measured rates (4.6 and 8.3 mmol C m\ d\, respectively) are considerably higher than those in Bacon et al. (1996), but they are consistent with independent Th-based estimates (Murray et al., 1996) and closer to seasonally averaged, carbon mass balances (Quay, 1997). The combined e!ects of these modi"cations is to reduce the migrant biomass for March}April 1992 to 144 mg DW m\, and the #ux estimates to 0.168 mmol C m\ d\ and 3.7% of trap PC. Migrant biomass and daytime respiratory losses remain unchanged for October 1992, but the #ux estimate accounts for 5.9% of trap PC. In e!ect, as a percentage of trap-based particulate carbon export in the HNLC equatorial Paci"c, the modi"ed migrant #ux estimates of Zhang and Dam (1997) are comparable to those of Le Borgne and Rodier (1997), and both are substantially lower than the estimates for Stn. ALOHA. Among studies conducted in the subtropical Atlantic, the sampling program of Dam et al. (1995) was designed to occur during the early spring period of maximum system productivity and zooplankton abundance. Although the migrant biomass and #ux estimates for this period do not re#ect mean conditions at the BATS site, they clearly show that migrant contributions to export #ux can be occasionally quite high. Similarly, in the 3 years and 26 cruises of the present study, we encounter three occasions (April, June and July 1996) when migrant #ux estimates exceeded 25% of

Sept. 1988

Oligotrophic Equator BATS 31350N, 64310W ALOHA 22345N, 1583W

72 (0.2}2 mm) 402 (2}20 mm) 479 240 387 132 (0.2}2 mm)

Migrant biomass (mg DW m\ d\)

Sept.}Oct. 1994 118 (0.2}2 mm) 1994}97 37 cruises 123 1994}96 26 cruises 394

Indicates #ux estimates include authors' correction for migrants '2 mm.

Steinberg et al. (2000) This study

Le Borgne and Rodier (1997)

NFLUX 383N, 653W

Longhurst et al. (1989, 1990) Dam et al. (1995) Zhang and Dam (1997)

Period

BATS 31350N, 64310W Mar}Apr. 1990 HNLC Equator 03, 1403W Mar}Apr. 1992 Oct. 1992 HNLC Equator 03, 1503W Sept.}Oct. 1994

Location

Study

14 18 9

18 13 13 14

18

Temp (3C)

0.257 0.100 0.304

0.967 0.280 0.488 0.529

0.186

5.5 4.7 15.3

29.7 14.7 20.3 3.5

3.1

0.045

0.106

0.139

0.136

0.051

mmol N m\ d\

mmol C m\ d\

% PC

Nitrogen Flux

Carbon Flux

19.9

19.8

4.9

37.3

7.6

% PC

Table 8 Comparison of migrant #ux estimates for carbon and nitrogen in tropical and subtropical open-ocean ecosystems. Flux estimates, mmol C or N m\ d\ and % trap particulate carbon (PC) or nitrogen (PN) at 150 m, are only for dissolved inorganic by-products of metabolism. All C #ux estimates are computed assuming RQ"0.8. Temp"mean temp at daytime depth of diel migrants

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2099

trap PC, and three cruises (March 1994, September 1995 and April 1996) when the estimates were 35% or more of trap PN (Figs. 1 and 2). More typically, migrant biomass appears to be substantially lower at the BATS site than Stn. ALOHA, as judged by the mean estimates of Steinberg et al. (2000) using similar sampling gear. As previously noted (Table 6), however, migrant #ux estimates computed according to Steinberg et al. (2000) are much lower than other approaches because they are based on low weight-speci"c rates from large animals. For the purpose of the present comparison, we multiply the Steinberg et al. (2000) estimates by 3.1 to correct for the di!erences in rate estimates and RQs in Table 6. The e!ect of this correction is to make the BATS estimates of migrant #uxes (0.31 mmol C m\ d\ and 15% trap PC) virtually identical to those for Stn. ALOHA. Overall, several studies have arrived at somewhat di!erent conclusions about the magnitude and relative importance of migrant-mediated export #uxes in the tropical open oceans. Patterns only emerge when results are evaluated on a comparable basis. First, migrants play a more important export role in more oligotrophic areas (ALOHA, BATS, western equatorial warm pool) where a high proportion of the zooplankton migrate and where particulate #uxes are relatively low. This pattern is consistent with the predictions of Longhurst et al. (1989, 1990). Second, in comparing subtropical regions of the Atlantic and Paci"c Oceans, the two- to three-fold greater migrant biomass in the Paci"c is compensated by higher daytime temperatures in the Atlantic, resulting in similar estimates of migrant metabolism. From this result, one might speculate that diel migration is less feasible as an adaptive strategy in the subtropical Atlantic given higher energetic costs associated with temperature-enhanced daytime metabolism. This could be one explanation for the disparity in zooplankton biomass between systems.

4.3. Migrant-mediated organic yuxes The preceding discussion focused on the inorganic by-products of zooplankton metabolism (NH> and CO ), with Table 8 speci"cally excluding all estimates for organic   constituents provided by the original authors. As noted by them, however, various forms of organics may contribute signi"cantly to total migrant #ux estimates, as well as provide important nutritional links between the euphotic zone and the communities of microbes and animals in deeper waters. In the discussion below, we consider three components of migrant-mediated organic #uxes * excretion of dissolved organics (DOC and DON), zooplankton mortality at depth, and fecal material released at depth * which could reasonably enhance the present migrant #ux estimates. Eppley et al. (1973) reported that roughly half of the nitrogen excreted by zooplankton in the central North Paci"c was in organic form as urea. Similarly, Le Borgne and Rodier (1997) determined that DON comprised an average of 53% of total nitrogen excreted by mesozooplankton at two stations in the equatorial Paci"c (60% DON at the oligotrophic site, and 46% in the HNLC area). More recently, Steinberg et al. (2000) measured signi"cant rates of DOC excretion, averaging 24% of the total carbon (DIC#DOC) metabolism, in the Sargasso Sea. Based on these results, migrant #ux estimates at Stn. ALOHA should increase by an additional third for carbon (0.405 mmol C m\ d\; 20% of trap PC) and double

2100

H. Al-Mutairi, M.R. Landry / Deep-Sea Research II 48 (2001) 2083}2103

for nitrogen (0.090 mmol N m\ d\; 39% of trap PN) to account for the e!ects of dissolved organic excretion. If we also include an additional 12% for the metabolic contributions of undersampled micronekton (see above), total metabolic losses increase to 23 and 45% of PC and PN, respectively. To the extent that they represent the permanent transfer of material derived from near-surface waters to the deep sea, losses of diel migrants to predators at their daytime depths clearly should be included in total migrant #ux estimates. Given the paucity of information on the organisms and rates involved, however, this is a di$cult problem. Zhang and Dam (1997) derived a "rst-order approximation of the migrant mortality e!ect using the Peterson and Wroblewski (1984) relationship for speci"c mortality as a function of organism size. Their estimates, averaging 70% of computed migrant DIC #uxes, were considered conservative according to McGurk (1986). An alternative approach is to consider the problem from the point of view of the predators at depth. According to Maynard et al. (1975), 57% of the mesopelagic micronekton in Hawaiian waters do not undergo a nocturnal feeding migration to shallower waters. That is, about 260 mg DW m\ resides permanently below 400 m, indirectly linked to production in the euphotic zone via the daily migrations of their prey. Given mean estimates of 5.1 animals m\ and 51 mg DW animal\ from Maynard et al. (1975), the non-migrating community must consume about 0.098 mmol C to satisfy its daily metabolic carbon requirement, with organic and inorganic components as described above. Simplifying assumptions of this calculation, no intra-zonal predation and zero net growth, tend to o!set one another. The computed mortality estimate is 32% of the migrant DIC #ux, about half that suggested by Zhang and Dam (1997). Adding these modest mortality losses to the previous subtotals and accounting for the C : N ratios of the consumed migrants (4.2; Landry et al., 2001) brings migrant #ux estimates to 0.552 mmol C and 0.124 mmol N m\ d\ (28 and 55% of trap PC and PN). Lastly, we want to consider the extent to which migrant zooplankton can actively transport fecal material past the base of the euphotic zone. In principle, weakly migrating organisms with daytime distributions that broadly overlap the euphotic could shuttle feces and metabolic by-products into water deeper than 150 m by alternating feeding in the euphotic zone and resting in the lower end of their range. As above, however, we account for no complications associated with asynchronous migratory cycles. Among stronger migrants, smaller taxa (copepods) likely vacate their gut contents many times over in warm surface waters during nocturnal feeding (Dam and Peterson, 1988; Landry et al., 1994). While they also might export some residual fecal matter during their morning descent, we assume that this #ux is small relative to the uncertainties in fecal transport by larger migrants. For the sake of argument, we calculate an upper limit to the latter, assuming that migrating micronekton (230 mg DW m\) derive all of their nutrition from the euphotic zone, leaving in the morning with stomach contents equivalent to 2% of body weight and returning with none (Clarke, 1978). After accounting for C and N assimilation e$ciencies of 70 and 80%, respectively, the estimates of fecal egesta at depth are relatively low, 0.041 mmol C and 0.006 mmol N m\ d\. Accordingly, total migrant #ux estimates are 0.593 mmol C and 0.13 mmol N m\ d\ ("30% of trap PC and 57% of trap PN #ux). In summary, migrant-mediated elemental #uxes at Stn. ALOHA are substantially enhanced by reasonable estimates of dissolved organic excretion, mortality at depth, and migrant fecal transport. These organic components comprise 43% of the computed total estimate

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2101

for active carbon export and 61% of migrant N #ux. As previously reported (Emerson et al., 1996), active carbon #ux of the magnitude of the present calculations (i.e., 0.2 mol C m\ yr\) contributes signi"cantly to new production mass balance in the subtropical North Paci"c. Given the depleted N : C ratio of passively sinking particulate material as well as the relative richness of nitrogen in the migrant biomass pool, the ratio of active-to-passive #uxes is markedly higher (about double) for nitrogen, as compared to carbon. Export #uxes associated with migrating zooplankton therefore should play an even more prominent role in closing nutrient budgets in the central Paci"c. Thus, we need continued e!orts to address the uncertainties in these rate estimates.

Acknowledgements We are extremely grateful to the captain and the crew of the R/V Moana Wave and to the many students, techs and colleagues who helped with sample collection and analyses (K. Selph, S. Christensen, D. Gravitt, L. Pozzi, B. Miller, J. Rooney, J. Constantinou, and C. Allen). In addition, we thank D. Karl and J. Hirota for their many comments and contributions to data analysis and interpretation. This work was funded by National Science Foundation Grant OCE-9218152 to MRL, and HA-M was supported in part by a scholarship from the Kuwait Institute for Scienti"c Research, Department of Mariculture and Fisheries. Contributions 5299 from the School of Ocean and Earth Science and Technology and 626 from the US JGOFS Program.

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