zooplankton vertical migration and the active transport of...

*Corresponding author. Fax: 001-441-297-8143.E-mail address: [email protected] (D.K. Steinberg)

Deep-Sea Research I 47 (2000) 137}158

Zooplankton vertical migration and the activetransport of dissolved organic and inorganic

carbon in the Sargasso Sea

Deborah K. Steinberg!,*, Craig A. Carlson!, Nicholas R. Bates!,Sarah A. Goldthwait!, Laurence P. Madin",

Anthony F. Michaels#!Bermuda Biological Station for Research, Inc., Ferry Reach, St. Georges GE 01, Bermuda

"Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA#USC Wrigley Institute of Environmental Studies, University of Southern California, Los Angeles,

CA 90089, USA

Received 23 July 1998; received in revised form 12 March 1999; accepted 12 March 1999

Abstract

The least known component of the `biological pumpa is the active transport of carbon andnutrients by diel vertical migration of zooplankton. We measured CO

2respiration and

dissolved organic carbon (DOC) excretion by individual species of common vertically migra-ting zooplankton at the US JGOFS Bermuda Atlantic Time-series Study (BATS) station. Theinclusion of DOC excretion in this study builds on published research on active transport byrespiration of inorganic carbon and allows a direct assessment of the role of zooplankton in theproduction of dissolved organic matter used in midwater microbial processes. On average,excretion of DOC makes up 24% (range"5}42%) of the total C metabolized (excreted#respired) and could represent a signi"cant augmentation to the vertical #ux that has alreadybeen documented for respiratory CO

2#ux by migrant zooplankton. Migratory #uxes were

compared to other transport processes at BATS. Estimates of combined active transport ofCO

2and DOC by migrators at BATS averaged 7.8% and reached 38.6% of mean sinking POC

#ux at 150 m, and reached 71.4% of mean sinking POC #ux at 300 m. DOC export by migratorexcretion averaged 1.9% and reached 13.3% of annual DOC export by physical mixing at thissite. During most of the year when deep mixing does not occur, diel migration by zooplanktoncould provide a supply of DOC to the deeper layers that is available for use by the microbialcommunity. A carbon budget comparing migrant zooplankton transport to the balance of

0967-0637/99/$ - see front matter ( 1999 Elsevier Science Ltd. All rights reserved.PII: S 0 9 6 7 - 0 6 3 7 ( 9 9 ) 0 0 0 5 2 - 7

#uxes in the 300}600 m depth strata at BATS shows on average that the total migrant #uxsupplies 37% of the organic carbon remineralized in this layer, and that migrant DOC #ux ismore than 3 times the DOC #ux gradient by diapycnal mixing. New estimates of activetransport of both organic and inorganic carbon by migrants may help resolve observedimbalances in the C budget at BATS, but the magnitude is highly dependent on the biomass ofthe migrating community. ( 1999 Elsevier Science Ltd. All rights reserved.

Keywords: Zooplankton; Vertical migration; Dissolved organic carbon (DOC); Carbon dioxide; SargassoSea; Bermuda Atlantic Time-series Study (BATS)

1. Introduction

The traditional concept of the biological pump is that phytoplankton convert CO2

into particulate organic carbon (POC) in the upper ocean, and some proportion ofthis is then transported as sinking particles to the deep sea. This passive sinking ofdetrital and living particles is commonly thought to be the dominant vertical trans-port process. More recently, two other processes have been proposed as important inthe net transport of organic material: vertical migration by zooplankton (e.g., Lon-ghurst and Harrison, 1988) and physical mixing of dissolved organic matter (Copin-MonteH gut and Avril, 1993; Carlson et al., 1994).

Zooplankton play a well-documented role in the biological pump by feeding insurface waters and producing sinking fecal pellets (Fowler and Knauer, 1986; Small etal., 1989; Altabet and Small, 1990). Diel vertically migrating zooplankton and nekton,which feed in surface waters at night and return to depth at dawn, may increase this#ux by releasing fecal pellets at depth during the day, although gut-clearance timesmay be too short for migration to signi"cantly increase this #ux (Longhurst andHarrison, 1989). Longhurst and Harrison (1988) suggested that migrating zooplan-kton play an important role in vertical #ux through a more subtle process, byconsuming organic particles at the surface at night and respiring the inorganicnutrients below the mixed layer during the day. This and recent studies show thatvertically migrating zooplankton can actively transport a signi"cant amount ofdissolved inorganic carbon (CO

2, as estimated by O

2consumption) and nitrogen

(NH4) to deep water, which can be signi"cant relative to the gravitational vertical

export of sinking particulate organic matter measured with sediment traps (Longhurstand Harrison, 1988; Longhurst et al., 1989,1990; Dam et al., 1995; Zhang and Dam,1997; Le Borgne and Rodier, 1997; Hays et al., 1997 } for total N #ux).

What has not been studied previously is how excretion of dissolved organic carbon(DOC) by migrating zooplankton might enhance carbon export. Zooplankton pro-duce dissolved organic matter by excretion, leaching from fecal pellets, and by loss ofcell contents from prey during handling (sloppy feeding) (Lampert, 1978). Physicallyforced DOC #uxes have proven important at the US JGOFS Bermuda AtlanticTime-series Study (BATS) site in the Sargasso Sea (Carlson et al., 1994). DOC that isnot remineralized in surface waters in spring and summer is exported during deep

138 D.K. Steinberg et al. / Deep-Sea Research I 47 (2000) 137}158

winter mixing; this annual export can equal or exceed the annual particulate verticalC #ux. In this study we used high precision measurements of DOC and total carbondioxide (TCO

2) to show that excretion by migrating zooplankton creates a migratory

DOC pump that enhances both respiratory C export and export of DOC by physicalmixing at BATS.

2. Materials and methods

2.1. Zooplankton collections

Physiological measurements were made on a variety of common migrant zooplank-ton. The zooplankton were collected monthly at the US JGOFS Bermuda AtlanticTime-series Station (BATS) in the Sargasso Sea (31350@N, 64310@W) from March 1996to May 1997. Migrators were collected within the surface 100 m at night in short,vertical tows. The mixed layer at BATS is at least this deep during much of the year,and during the most strati"ed summer period, temperature does not vary more than6}73C between the surface and 100 m (Michaels and Knap, 1996). Tows were per-formed with a 2 m diameter, 500 lm mesh plankton net equipped with a large-volume,`live cod-enda, designed so that water "lters out from the top of the cod end (Reeve,1980). This design retained the organisms in excellent condition, including some of thedelicate gelatinous forms, such as alciopid worms. Most previous studies of zooplan-kton migration have focused on mesozooplankton ((2 mm). In addition we usedsome of the larger migrators, such as sergestid shrimps, in our experiments.

2.2. Incubations

The experiments were designed to measure CO2

respiration and DOC excretion bymigrators simultaneously. In order to mimic the condition of animals just before theirdescent to depth after feeding in surface waters, experiments were initiated on boardthe ship at night after animal capture. Experimental animals were sorted withinminutes from tows and placed in beakers with natural surface seawater. Glass bottles(volume &600 ml) "tted with ground glass stoppers were used as experimental cham-bers.Experiments were carried out in 0.2 lm "ltered surface seawater (FSW) withhealthy, active organisms gently pipetted from beakers into bottles. A small headspacewas left in the bottles after "lling, and bottles were sealed with a small amount ofsilicon vacuum grease on top of stoppers. Analysis of DOC in water samples beforeand after adding animals in preliminary experiments indicated that dissolved materialadded with animals was undetectable, thus not a source of error. Numbers of eachspecies per bottle depended on their size and ranged from 1 (sergestid shrimps) to 25(copepods), but were usually between 1 and 10. Typically four replicate bottles of eachspecies and three controls (without animals) were incubated in the dark for 8 h at insitu sea-surface temperatures (range 19}263C). We determined this as a reasonabletime period: long enough to minimize the impact of initial high activity and obtain

D.K. Steinberg et al. / Deep-Sea Research I 47 (2000) 137}158 139

measurable changes in DOC and CO2, but not so long that starvation becomes a

factor (Regnault, 1987). Animals were healthy and active at the end of the incubations.At the end of the experiment, "nal samples were siphoned from incubation bottles

into precombusted 40 ml glass vials (sealed with Te#on-coated septa and open topscrew caps) for DOC analysis, and into 120 ml glass bottles with ground glassstoppers (sealed with Apiezont silicon vacuum grease) for CO

2analysis. (The siphon

was "tted with a 160 lm Nitex mesh at the collection end to exclude animals.) DOCsamples were immediately frozen, and 50 ll of saturated HgCl

2solution was added to

CO2

samples to prevent biological alteration. The average control value was subtrac-ted from experimentals to determine excretion and respiration rates (Quetin et al.,1980; Bidigare, 1983). Animals were then removed, dried at 603C for 24 h, and weighedon a Cahn electrobalance.

Additionally, time-course experiments of DOC excretion were run for three of themost common species to provide more detailed information on the organisms' meta-bolism, as changing excretion rates will in#uence the amount of dissolved materialexcreted at depth. The procedure for sampling and incubation was the same asdescribed above for the single-end point experiments with the following exceptions:Animals were incubated in 1 l polycarbonate bottles, two replicate experimentalbottles were run along with two control bottles, and DOC samples were takenapproximately every 4 h.

To ensure there was no loss of zooplankton-excreted DOC in experiments bybacterial metabolism, all experiments were monitored for bacterial growth by takingreplicate samples for bacterial abundance from the incubation water at the beginningof each experiment, and from both treatment and control bottles at the end of theexperiments. There was no signi"cant di!erence between bacterial abundance inexperimentals vs. controls at the end of the experiments, nor was there any signi"canttemporal variation in bacterial abundance over the course of the experiments (Stu-dent's t-test, P(0.05). To determine if leaching of DOC from fecal pellets defecatedduring the experiment was a potential additional source of DOC, 50 fecal pelletscollected from several of the same zooplankton species used in experiments wereplaced in 100 ml of 0.2 lm FSW in glass bottles (2}3 replicates) and incubated in thedark for 8 h at in situ sea-surface temperatures, along with 2}3 replicate controlbottles containing only FSW. By incubating 50 pellets in experiments we tested anextreme case, as typically far fewer pellets were defecated during animal excretionexperiments. Subsamples for DOC were taken at the end of the experiment in bothtreatments (with pellets) and controls (FSW).

2.3. CO2 and DOC analysis

TCO2

was measured using a gas extraction/coulometric detection system describedby Johnson et al. (1993) and recognized analytical protocols (DOE, 1994). A singleoperator multi-metabolic analyzer (SOMMA) was used to control the pipetting andextraction of the samples. The SOMMA was interfaced with a personal computer andcoupled to a CO

2coulometric detector (model 5011, UIC Coulometrics Inc.). This

method is highly precise and accurate (&0.025%, $0.5 lM) (Bates et al., 1996a,b)


and allowed us to detect 1 lM changes in TCO2. We measured CO

2respiration by

di!erence in TCO2, and as there is no expected change in carbon dioxide species other

than CO2, we refer to the measurement as CO

2throughout.

DOC samples were analyzed by the high-temperature combustion method (HTC)using a custom instrument described in Carlson et al. (1998). Samples were not "lteredafter collection, but as experiments were carried out in FSW, and preliminary trialsshowed no signi"cant di!erence between DOC and total organic carbon (TOC), werefer to the measurement as DOC. The method and system used is highly precise($1}2% error) and allows detection of small changes (1 lM) in DOC concentrations.The instrument's con"guration, operating parameters, and conditioning proceduresare described in Carlson et al. (1998). Low-carbon seawater and deep Sargasso Seawater ('2000 m) served as blank reference standards and were analyzed several timesa day to assess the instrument's stability. To ensure optimal stability of the DOCanalyzer, all samples were run in the shore lab back in Bermuda. In order to avoid thesmall error associated with instrumental day-to-day variability, all samples generatedfrom one experiment were run on the same day and systematically checked againstreference material.

2.4. Migrator biomass

Excretion data were incorporated into an ongoing time-series study of seasonalvariation in zooplankton biomass and diversity at BATS, which began in May 1994(L.P. Madin). Monthly, replicate day and night tows are routinely made in the upper200 m on all BATS cruises using a 202 lm, 1 m2 plankton net. Size-fractionatedbiomass (wet and dry weight) is determined from each tow by wet sieving and freezingeach fraction, which is subsequently thawed and weighed, and then dried at 603C for24 h and re-weighed. Migrator biomass was estimated by averaging replicate totaltow biomass (i.e., all size fractions), integrating to 150 m, and subtracting day fromnight values. We also determined the biomass contribution of two of the morecommon migrators from these tows that we used in our experiments, the euphausiidThysanopoda aequalis, and the copepod Pleuromamma xiphias, as well as other speciesin the genus Pleuromamma ("`other Pleuromammaa). These species (enumeratedaliquots) were counted from subsamples (12}50%) of each tow using a Wild dissectingmicroscope. Densities were then multiplied by the average dry weight of each speciesto determine their contribution to total migrator biomass. Zooplankton dry weightwas converted to carbon weight by assuming carbon weight"0.4]dry weight(Parsons et al., 1984; Madin, unpublished BATS data).

2.5. Determination of respiration and excretion at depth by migrant zooplankton

Downward #ux of CO2and DOC by migrant zooplankton was calculated using the

following equation from Dam et al. (1995):

F"BR12 h,


where F is the CO2

or DOC #ux by migrant zooplankton (mg C m~2 d~1), B thebiomass of migrant zooplankton (mg C m~2), and R the weight-speci"c respiration orexcretion rate at 183C (mg C (mg body C)~1 h~1). We assumed an average 12-h daylength throughout the year for the calculation; consequently migrants spend an equalamount of time above and below the mixed layer over a 24-h period (Longhurst et al.,1990; Dam et al., 1995). To determine R, a Q

10of 2.5 was applied to weight-speci"c

respiration and excretion rates from our experiments to calculate respiration andexcretion rates at 183C, the average temperature experienced by interzonal migrantzooplankton at depth during the day (Longhurst and Harrison, 1988; Dam et al.,1995). This broad 183C isothermal band (Talley, 1982) exists below 150 m at BATS,with the core lying between 250 and 400 m depth year-round (Michaels and Knap,1996). Downward #ux of CO

2and DOC by zooplankton vertical migration was then

compared to sinking of POC and physical mixing of DOC at BATS.

3. Results

3.1. Migrating community

Migrating zooplankton used in our experiments were taxa that were abundant orconsistently present in our net tows. Common vertical migrators o! Bermuda includecopepods such as Pleuromamma xiphias and P. abdominalis (Deevey, 1971; Deevey andBrooks, 1977). Longhurst et al. (1989) also report high abundances (relative to othercopepods) of adult P. xiphias, with some P. abdominalis and P. gracilis, in samplesabove 150 m at night and in deeper samples in the daytime in the northern SargassoSea. We chose P. xiphias for our experiments as it was abundant and easy to identify andpick from tows with the naked eye. The most common euphausiid was Thysanopodaaequalis, with Nematobrachion yexipes also occasionally abundant. Euphausiahemigibba was also occasionally present but not su$ciently abundant for use in ourexperiments.

Pleuromamma spp. copepods and the euphausiid Thysanopoda aequalis alone madeup a substantial proportion of the biomass of zooplankton present in surface waters atnight (mean"23%, range"4}70% for Pleuromamma and Thysanopoda combined)(Fig. 1). Other common migrators included the hyperiid amphipods Anchylomerablossevillei and Scina spp. The most common migrating sergestid shrimps present inthe night tows were Sergia splendens, Sergestes atlanticus, and Sergestes vigilax. Thegelatinous alciopid worm Naiades sp. was also a consistent member of the migratingcommunity.

3.2. Respiration and excretion rates

The mean respiration and DOC excretion rates for a variety of common verticalmigrators at BATS collected during March 1996}March 1997 are shown in Fig. 2a.Replicate experiments (e.g., N. yexipes and A. blossevillei) at similar temperaturesshow similar average respiration rates. As expected, species incubated at higher


Fig. 1. Proportion of total biomass contributed by common migrators. Time series of biomass of some ofthe important migrators at BATS. Data are averages of replicate night tows taken in the upper 200 m on allBATS cruises (202 lm mesh, 1 m2 plankton net). Numbered months denote '1 cruise in same month. Thebiomass of individual species was estimated by multiplying species counts in each tow by the mean dryweight determined for each species.

temperatures generally show higher respiration rates (e.g., T. aequalis, P. xiphias andA. blossevillei). The CO

2respiration rate determined for the euphausiid T. aequalis

(2.2 lg C mg dry wt~1 h~1 at 243C) is the same as published respiration rates for thesimilarly sized Euphausia pacixca at 253C (calculated from allometric equations andQ

10for respiration given in Ross, 1982). CO

2respiration of copepods (P. xiphias,

1.6 lg C mg dry wt~1 h~1 at 243C and 2.4 lg C mg dry wt~1 h~1 at 263C) is slightlylower than respiration rates of 3.86 and 5.51 lg C mg dry wt~1 h~1 reported formixed large copepods at a slightly higher temperature (273C) (Longhurst et al., 1990).The Sergestids Sergia splendens and Sergestes atlanticus have similar respiration rates(at 253C) of 1.5 and 1.7 lg C mg dry wt~1 h~1, respectively. Donnelly and Torres(1988) report mean respiration rates for Sergia splendens from which we computea mean rate of 0.9 lg C mg dry wt~1 h~1 (range 0.6}1.7) at 253C (calculated from theirTable 2, using their Q

10, and assuming a respiratory quotient of 1). Weight-speci"c

DOC excretion rates range from 0.01 to 1.64 lg C mg dry wt~1 h~1 (Fig. 2a) andcompare favorably with DOC excretion rates (0.18}2.63 lg C mg dry wt~1 h~1)reported for mixed, small ((300 lm) zooplankton (Small et al., 1983). As withrespiration, replicate experiments (e.g., N. yexipes and A. blossevellei) at similar


Fig. 2. (a) Mean CO2

respiration and DOC excretion rates of common vertical migrators at BATS.(b) Mean percent body C respired or excreted per day by common vertical migrators at BATS. n"4replicate bottles for each species except S. splendens, n"6; and P. xiphias experiment at 263C, n"3. Errorbars are 1 standard deviation. Incubation temperature is indicated above error bars. (Note: absence of DOCdata in some experiments indicates samples not taken; it does not indicate zero DOC excretion). N. yexipes} Nematobrachion yexipes; T. aequalis } Thysanopoda aequalis; P. xiphias } Pleuromamma xiphias, A.blossevillei } Anchylomera blossevillei; S. splendens } Sergia splendens; S. atlanticus } Sergestes atlanticus;Naiades sp.


Fig. 3. Time course of DOC excretion for three common vertical migrators at BATS. Incubation temper-ature"203C for all experiments. T-1 and T-2 indicate replicate time-course experiments.

temperatures show similar average DOC excretion rates, which increased at highertemperatures (e.g., T. aequalis and A. blossevillei) (Fig. 2a).

Leaching of DOC from fecal pellets was insigni"cant (often below the detec-tion limit of the method) compared to changes in DOC observed in the excretion


Fig. 4. Percent of total C excreted as DOC for common vertical migrators at BATS. Replication, tem-perature, and species names as in Fig. 2.

experiments, and thus likely not a signi"cant source of DOC over the course of theincubations. Average DOC changes of 0.12 lg C h~1 (T. aequalis pellets) and0.84 lg C h~1 (P. xiphias pellets) observed in the leaching experiments were orders ofmagnitude lower than in excretion experiments (mean"16.9 lg C h~1). If fecalpellets leach relatively more DOC when they are newly defecated (e.g., Jumars et al.,1989), then we could be underestimating this potential source of DOC, as we couldnot initiate experiments until enough pellets were collected (&1 h). However, this isunlikely to be a signi"cant error given the changes in DOC in the excretion experi-ments, and that in many experiments no or few pellets were even produced.

The fraction of body C respired or excreted per day is similar among the di!erentspecies, with a mean of 10% (range 3}22%) for CO

2and 4% (range 1}10%) for DOC

(Fig. 2b). These values (for respiration) are within the range reported for mixedzooplankton ('100 lm) at comparable temperatures (e.g., Schneider and Lenz, 1991)and for vertically migrating copepods (Metridia pacixca) in the subarctic Paci"c(Batchelder, 1986).

The rate of DOC excretion is linear throughout the time-course experiments (Fig.3), with the possible exception of the euphausiids (Fig. 3a). After 4 h, DOC excretionrates of euphausiids in T-1 appear to increase slightly, while in T-2 excretion levels o!(Fig. 3a). Possibly di!erences between animals in the type of food previously ingestedor di!erences in gut fullness caused the observed deviation. Excretion rates calculatedfrom regression of time-course data are similar to single-end point experiment data forthe same species at comparable temperatures.


Fig. 5. Time series of zooplankton biomass integrated to 150 m. (a) Day vs. night biomass. Values aremean of two replicate tows. (b) Migrator biomass. Day biomass subtracted from night biomass. (*)indicates that day biomass exceeded night biomass.

Excretion of DOC by zooplankton made up a signi"cant proportion of the totalcarbon released through respiration and excretion combined (Fig. 4). On average,excretion of DOC made up 24% of the total C metabolized (excreted#respired)(range"5}42%) or 31% of the C respired (Fig. 4). No particular taxa excretedsubstantially di!erent fractions carbon as DOC than others, with the possible excep-tions of the amphipods (mean"15%), and one polychaete trial (5%), which appearedto be comparatively low.

3.3. Active transport of CO2 and DOC by zooplankton vertical migration compared tosinking of POC and physical mixing of DOC

Zooplankton biomass in surface waters was highest in the spring, and was greaterat night on all but three cruises (Fig. 5a and b), with a mean night/day ratio of 1.7($SE"0.1, range 0.6}3.1). Migrant zooplankton biomass averaged 49.1 mg C m~2

($SE"8.2) and ranged from less than zero (indicating higher day vs. night biomass)to 122.9 mg C m~2 (Fig. 5b).


Table 1Active transport of CO

2and DOC by zooplankton vertical migration compared to sinking of POC and

physical mixing of DOC at the BATS. Migrator CO2

respiration and DOC excretion rates, and all #uxes,are all calculated at 183C. Migrant zooplankton biomass is given as night}day values in the top 150 m. Allmigratory #uxes are calculated across 150 m. BATS sediment trap #uxes are mean of monthly trap #uxes at150, 200, and 300 m for the period 1989}1997. DOC export is the mean of 1992 and 1993 DOC #ux to the150}250 m layer at BATS (recalculated from Carlson et al., 1994; see text)

Mean Max

Migrator CO2

respiration rate(mg C (mg body C)~1 d~1 0.03 0.05

Migrator DOC excretion rate(mg C (mg body C)~1 d~1) 0.01 0.03

Migrant zooplankton biomass(mg C m~2) 49.1 122.9

Migratory CO2#ux

(mg C m~2 d~1) 1.5 6.4Migratory DOC #ux

(mg C m~2d~1) 0.5 3.5Migratory CO

2#DOC #ux

(mg C m~2 d~1) 2.0 9.9Migratory CO

2#DOC #ux/mean BATS POC #ux at

150 m ("25.6 mg C m~2 d~1) (n"105) (%) 7.8 38.6200 m ("19.8 mg C m~2 d~1) (n"104) (%) 10.1 49.9300 m ("13.9 mg C m~2 d~1) (n"104) (%) 14.4 71.4

Migratory DOC #ux/BATS DOC export due to physical mixing("9.6 g C m~2 yr~1) (%)

1.9 13.3

Weight-speci"c CO2

respiration and DOC excretion rates of migrators weremultiplied by the migrant zooplankton biomass to obtain estimates of the #ux of bothrespiratory and excretory carbon by zooplankton migration (Table 1). Flux of DOCby migrants increases total carbon #ux due to migrators by about another third toa half over respiratory C #ux alone, with combined CO

2and DOC #ux due to

migrators equal to a mean of 2 and a maximum of 9.9 mg C m~2 d~1 (Table 1).Comparing this to POC #ux at 150 m at BATS reveals that combined active transportof CO

2and DOC by migrators can equal up to 38.6% of the mean BATS #ux,

although mean #ux of C due to migrators is (10% of the BATS POC #ux (Table 1).As the main scattering layer o! Bermuda lies below 400 m (see discussion), mostmigrators routinely travel deeper than 150 m. Therefore, we also compared migrant#ux to sinking POC #ux at deeper depths. As POC #ux decreases with depth, migrant#ux becomes a signi"cant proportion of the sinking POC #ux } up to 71% at 300 m(Table 1). Carlson et al. (1994) calculated annual mean DOC #uxes across 100 m byphysical mixing at BATS of 1.21 and 0.99 mol C m~2 yr~1 (for 1992 and 1993, res-pectively). Recalculating this #ux across 150 m, gives 0.91 (1992) and 0.69 mol C m~2

yr~1 (1993), or a mean of &0.8 mol C m~2 yr~1 ("9.6 lg C m~2 yr~1). DOC #ux


due to migrators is equal to a mean of 1.9% and maximum of 13.3% of the DOC #uxdue to physical mixing across 150 m (Table 1).

4. Discussion

Approximately 15}50% of the zooplankton biomass above 500 m vertically mi-grates into the surface waters at night (Longhurst and Harrison, 1988). The mainscattering layer near Bermuda lies at 400}600 m in the daytime (Menzel and Ryther,1961; Moore, 1950), and zooplankton biomass in the upper 160 m can nearly doubleat night due to vertically migrating zooplankton (Roman et al., 1993; this study). Thedownward migration of zooplankton that have been feeding in the surface watersreleases not only particulate organic matter, via fecal pellet production, but alsodissolved inorganic and organic material, via respiration and excretion below themixed layer during the day. Rates of zooplankton vertical transport across thepycnocline reported in previous studies (Longhurst and Harrison, 1988; Longhurst etal., 1989,1990; Dam et al., 1995; Zhang and Dam, 1997; Le Borgne and Rodier, 1997)are necessarily conservative, because dissolved organic carbon (and nitrogen) excre-tion were not measured.

4.1. Zooplankton excretion of dissolved organic matter

Vertical migrators can increase dissolved C export (over respiratory C #ux alone)below the mixed layer by excretion of DOC. Excretion of DOC by migrating zoo-plankton at BATS made up a signi"cant proportion (mean"24%, range"5}42%)of total carbon released through respiration and excretion combined, or 31% ofcarbon respired. While there are few measurements of organic excretion by zooplank-ton, other studies also show that excretion of DOC by zooplankton can make upa large proportion of total carbon released through respiration and excretion com-bined, as well as a large fraction of the carbon ingested. The amphipod Calliopiuslaeviusculus excretes DOC at approximately 30% of its respiration rate (Dagg, 1976).Small et al. (1983) report mean (although extremely variable) rates of DOC excretionof 1.28 lg C mg dry wt~1 h~1 (range 0.18}2.63) for small ((300 lm) zooplankton.Using the Small et al. respiration rates of 2.11 lg C mg dry wt~1 h~1, calculated at253C for small zooplankton, we calculate DOC excretion as an average of 61% ofrespiration (range 9}124%) or 38% (range 5}77%) of total carbon released (CO

2respired#DOC excreted) (Small et al., 1983). Similarly, DOC made up on average38% of total carbon released for the ctenophore Mnemiopsis leidyi (Kremer, 1977).A reasonably large fraction, 17}19%, of ingested C is released as DOC by the copepodCalanus pacixcus (Copping and Lorenzen, 1980). Similar rates of 16}21% of ingestedC released as DOC have been found for euphausiids (Lasker, 1966). Daphnia pulexfeeding on 14C-labeled algae lost 4% of the algal C ingested as DOC (Lampert, 1978).Gelatinous zooplankton may also release DOC through mucus production; themedusa Aurelia aurita is estimated to release 2.5}7.1% of its assimilated C as DOC(Hansson and Norrman, 1995).


Table 2Comparison of studies measuring the ratio of downward transport of carbon by migrating zooplankton togravitational POC #uxes measured by sediment traps. Migratory and sediment trap #uxes are calculatedacross 150 m or the depth of the euphotic zone. Mean and range (given in parentheses). (Data not listed herewere not provided in reference)

Location of studyand time of year

Migratingbiomass(mg C m~2)

Migratory#ux(mg C m~2 d~1)

% of meanPOC #ux

Reference

BATS 50 (0}123) 2.0 (0}9.9)! 8 (0}39) (this study)(year-round)

Subtropical andtropical Atlantic }several stations

} 5.5 (2.8}8.8)" 6 (4}14) Longhurst et al.(1990)

(September)

BATS 191 (82}536) 14.5 (6.2}40.6) 34 (18}70) Dam et al. (1995)(March/April)

Equatorial Paci"c(March/April) 96 4.2# 18

Zhang and Dam(1997)

(October) 155 7.3# 25

Equatorial Paci"cOligotrophic 47$ 3.8",% 8%

Le Borgne andRodier (1997),

HNLC area(September/October)

53$ 7.9",% 4% and Rodier andLe Borgne (1997)

!Migratory #ux includes DOC#CO2

(values in other studies are respiratory #ux only)."Includes migrating micronekton or nekton in addition to zooplankton.#Does not include #ux due to mortality.$Calculated from Table 10, Le Borgne and Rodier (1997), assuming C"0.4]dry weight.%Calculated from Table 8, Rodier and Le Borgne (1997).

4.2. Active yux due to migrators } comparison to other export processes (sinking of POC,mixing DOC )

Our results indicate that the metabolic activities of diel migrant zooplanktonshould be included in calculations of export of C out of the mixed layer. Ratios ofdownward transport of CO

2and DOC by migrators to gravitational #uxes in our

study are similar to (or slightly higher than) ratios of respiratory CO2#ux to sediment

trap #uxes reported for a range of stations in the subtropical and tropical Atlantic(Longhurst et al., 1990; for copepods and nekton) and in the equatorial Paci"c (LeBorgne and Rodier, 1997; Rodier and Le Borgne, 1997; for mesozooplankton andmicronekton) (Table 2). However, they are considerably smaller (by a factor of 4) than


those reported for mesozooplankton by Dam et al. (1995) at BATS, and Zhang andDam (1997) in the equatorial Paci"c (by a factor of 2}3) (Table 2). This di!erencemay be attributed to a greater biomass of migrating zooplankton in the latter twostudies (Table 2). It is perplexing that the zooplankton biomass at BATS reported inDam et al. (1995) is signi"cantly higher than we have found in the BATS zooplan-kton time series (Table 2); although this may be a result of plankton patchiness,higher frequency sampling during the peak zooplankton biomass season, or use ofdi!erent sampling gear (MOCNESS) in Dam et al. (1995). Summer biomass ofmigrating mesozooplankton was lower (mean 42.4 mg C m~2 in top 160 m; H. Dampers. comm.) and within the range seen in the BATS zooplankton time series. Thus,active transport of carbon and the relative importance of migration vs. other #uxesis highly dependent on the biomass of the migrating community. Active transport ofcarbon by vertical migration is likely to be important in other systems witha higher migrating biomass, such as the Azores front region in the North Atlantic,where the daily biomass #ux of migrating zooplankton and micronekton is200}700 mg C m~2 d~1 (Angel, 1989).

At the BATS site, biological activity in surface waters can produce a surfacemaximum in DOC. DOC that is not remineralized in surface waters in spring andsummer is exported during deep winter mixing, resulting in a net transport of thisDOC into the mesopelagic (100}250 m) that can equal or exceed the annual partic-ulate vertical C #ux (Carlson et al., 1994). DOC #ux due to vertical migrators is equalto a mean of 1.9% and maximum of 13.3% of the DOC #ux due to physical mixing(Table 1). This zooplankton-mediated DOC is available for use by the microbialcommunity, which can increase their biomass and production in the presence ofzooplankton-excreted DOC (Hansson and Norrman, 1995; Hygum et al., 1997). DOCalso disappears at depths of 100}250 m during the rest of the year, when deep mixingdoes not occur (Carlson et al., 1994). During this time migrating zooplankton couldsupply DOC to the deeper layers. There is no net increase in DOC at depth afterstrati"cation (Carlson et al., 1994), which suggests that the excreted material isrelatively labile and susceptible to microbial mineralization. Thus, for most of the yearwhen the water is strati"ed and deep mixing does not occur, active #ux of DOC byvertical migration will be a more important #ux below the 150 m depth stratum thanphysical mixing of DOC. In addition, as vertically migrating zooplankton andmicronekton can routinely travel deeper than most winter-mixing events (mixingbelow 300 m is rare, e.g., Michaels and Knap, 1996), DOC exported by migratorscould remain at depth (ultimately as CO

2) for the longer term.

To illustrate the importance of zooplankton active #uxes in the deeper layers wecompare migrant zooplankton transport to the balance of biogeochemical #uxes inthe 300}600 m depth strata (Fig. 6). This depth range is below deep winter-mixingevents and convective overturn; thus the vertical physical #uxes are by diapycnal andisopycnal mixing. This depth range also contains most of the deep scattering layer (i.e.,most migrators travel below 300 m but stay above 600 m during the day), and thusmost of the respiratory migrant #uxes end up in this layer.

Diapycnal DOC and CO2#uxes were determined using concentration gradients for

DOC and CO2

at the 300 and 600 m depths at BATS and applying a diapycnal


Fig. 6. Carbon #ux gradients between 300 and 600 m at BATS. Units are mg C m~2 d~1 (see Table 1 forindividual components, i.e., DOC and CO

2, of the migrator #ux).

mixing rate of 1.5]10~5 m~2 s~1 (Gregg, 1987; Ledwell et al., 1993). POC #ux at300 m is the mean BATS #ux for the period 1989}1997 (n"104). POC #ux at 600 mwas calculated from "tting a power function (Martin et al., 1987) to mean BATS traporganic carbon #uxes (at 150, 200, 300, and 400 m) and the mean 3200 m trap organiccarbon #ux from Deuser et al. (1990). (log}log slope `ba"!0.781, r2"0.99; seeMartin et al., 1987 for equation).

On average, the total migrant #ux (2 mg C m~2 d~1) supplies 37% of the TotalOrganic Carbon (#ux gradient of DOC#POC; 0.15#5.2 mg C m~2 d~1) re-mineralized in this layer (Fig. 6). On a short-term basis, when zooplankton biomass ishigh (spring), migrant #ux becomes the main supply of carbon for remineralization inthis layer. The DOC #ux by migrant zooplankton (0.5 mg C m~2 d~1, Table 1) ismore than 3 times the DOC #ux gradient by diapycnal mixing (0.15 mg C m~2 d~1).Isopycnal mixing rates are unknown, but preliminary data show that the horizontalgradients of DOC on density surfaces at these depths are small ((1 lmol kg~1),indicating that the horizontal #ux is minimal. These data suggest that the migratory#ux may be the primary source of DOC for bacteria in this mesopelagic layer.

Assuming a steady state and no net accumulation of carbon in this stratum, theTOC #ux gradient in the 300}600 m layer is 5.85 mg Cm~2 d~1 (DOC vertical #uxes,POC #uxes, and DOC excretion by migrants). We estimated bacterial carbon demand(BCD) in this layer to determine if requirements of microbial metabolism were beingmet by the supply (i.e., to maintain steady-state conditions). Bacteria production wasmeasured by the thymidine incorporation method (Carlson et al., 1996) on watersamples collected between 300 and 500 m at BATS (n"12). Thymidine incorporationwas converted to carbon demand using a thymidine conversion factor of 1.18]1018cells mol~1 (Cho and Azam, 1988), applying a carbon conversion factor of 10 fg cell~1

(within the range of commonly employed open ocean conversion factors; Ducklow


and Carlson, 1992), and assuming the fraction of thymidine incorporated into bacter-ial DNA in deep water to be 29% (after Cho and Azam, 1988). Using a bacterialgrowth e$ciency (BGE) of 10% for deep-water bacteria, we calculate BCD in the300}600 m depth stratum to be 24.4 mg C m~2 d~1. At BGE of 50% (e.g., Cho andAzam, 1988) the estimate of BCD is 4.9 mg C m~2 d~1. The #ux gradient in the300}600 m layer (5.85 mg C m~2 d~1) is at the low end of these BCD estimates, andthe two rates might be balanced only if bacterial BGE is at the high end of thepublished range (also, BCD estimates are highly dependent on carbon and thymidineconversion factors, of which there is little information for deep-sea bacteria) of ifisopycnal transport is high (as noted above, we cannot accurately assess isopycnalmixing at this time).

4.3. Consequences for carbon imbalance at BATS

Excretion of DOC by migrants in addition to respiratory C #ux may partially helpresolve the carbon imbalance at BATS, where there is a documented spring}falldecrease in the 0}150 m carbon stock that is 3 times larger than the sum of the bioticand abiotic vertical #uxes of carbon (Michaels et al., 1994). Michaels et al. (1994)estimated the #ux of respiratory C by vertically migrating zooplankton from a studynorth of Bermuda (Longhurst et al., 1990). Based on that cruise, the average migratory#ux was signi"cant (6 mg C m~2 d~1, Table 2) but not large compared to the other#uxes. We can re-evaluate the role of vertical migration of zooplankton in the exportprocess of carbon with data from more recent studies and by adding export of DOCcalculated from our experiments. Results from our study show a migratory #uxsimilar to that found by Longhurst et al. (1990), even though DOC excretion wasincluded in our study (Table 2). Recent data from another study at BATS (Dam et al.,1995) indicate a higher average migrant #ux of respiratory C due to zooplankton(14.5 mg C m~2 d~1, Table 2). If we apply DOC excretion rates from our results(DOC excretion"31% respiration) to the Dam et al. (1995) migrant respiratory #uxto estimate total dissolved C transport, the migrator #ux increases signi"cantly to19 mg C m~2 d~1. Thus, when migrating biomass is high, and DOC excretion isincluded, transport by migrators is signi"cant and partly reduces the discrepancy inthe carbon balance at BATS (from 94 to 81 mg C m~2 d~1, calculated from Table 1 inMichaels et al. (1994) by substituting a migrant #ux of 19 mg C m~2 d~1).

4.4. Other zooplankton-mediated yuxes

Our estimates of active transport of dissolved C are necessarily conservative esti-mates of total C transport by zooplankton, as several other processes exist by whichvertical migration actively transports organic material into the interior of the oceanthat we did not attempt to quantify. These processes include loss due to mortality(predation or senescence) in deep water (Longhurst and Williams, 1992; Zhang andDam, 1997), molting, and defecation at depth. Zhang and Dam (1997) estimatedone-third of the downward #ux of carbon by diel vertical migration of mesozooplankton


in the central equatorial Paci"c was due to mortality of migrators at depth (the othertwo-thirds was due to respiratory carbon #ux). Estimates of winter mortality ofseasonal vertical migrant copepods in the North Atlantic were approximately 75% ofthe overwintering population, although this loss was small compared with the respir-atory #ux by diel migrants or sinking particle #ux (Longhurst and Williams, 1992).The seasonal ontogenetic migrator Calanus hyperboreus lost more than half its fallpopulation biomass at over wintering depths (below 500 m) to metabolic processesand predation (Hirche, 1997). This active #ux of migrators in the Greenland Sea wassimilar to the passive particle #ux measured in deep sediment traps there (Hirche,1997).

The rate of loss of body carbon in crustacean zooplankton due to molting appearsto be small in relation to other metabolic processes and is generally less than a fewpercent of body carbon per day (Vidal, 1980). However, molts have been reported toconstitute a signi"cant part of the total production of some zooplankton (Ritz andHosie, 1982). For example, molt (exuviae) production by the euphausiid Nyctiphanesaustralis made up 34% of its total annual production ("biomass#exuviae) (cal-culated from production of exuviae/total production given in Ritz and Hosie, 1982).Currently, there are no estimates of loss of carbon due to molt production at depth bydiel migration, but the rate would be highly dependent on food availability andtemperature (Soussi et al., 1997).

Meso- and macrozooplankton contribute substantially to #ux (loss) of particulateorganic matter from the euphotic zone via production of fecal pellets (Fowler andKnauer, 1986; Small et al., 1989; Altabet and Small, 1990). Diel vertical migrators mayincrease this #ux by feeding in the surface at night and releasing fecal pellets at depthduring the day } providing that migration speeds are fast enough and gut clearancetimes are slow enough to allow them to return to depth before defecating. Reportedmigration speeds of zooplankton range from about 40 to over 200 m h~1 (Roe, 1984;Wiebe et al., 1992; Heywood, 1996). A number of studies show that clearance times aregenerally shorter (e.g., 25}100 min for copepods in the North Paci"c; Dagg andWyman, 1983) than the time required for migration, or that animals have littlematerial left in the gut (e.g., 10% of initial amount for copepods in Dabob Bay; Dagget al., 1989) when they reach their daytime depths. However, there is evidence that dielmigrating copepods have longer gut clearance times and slower defecation rates thantheir surface-living counterparts and may actively transport POM to depth (Moraleset al., 1993; Atkinson et al., 1996). For example, Atkinson et al. (1996) show thatMetridia spp. copepods were capable of rapidly descending to depths below the mixedlayer in less than 1 h, and by this time guts would still have contained more than halfof the ingested material. Migration swimming speeds reported for species used in ourexperiments appear to be relatively fast (e.g., 130 and 145 m h~1 for Pleuromammaxiphias copepod females and males, respectively, and 191 m h~1 for Thysanopodaaequalis euphausiids; Wiebe et al., 1992) and may allow transport of fecal material outof the mixed layer if gut passage times are su$ciently long. Thus, it appearsthat an individual species approach is necessary for determining if migrators canactively transport fecal material out of the mixed layer. This remains an area forfurther study.


5. Conclusion

The #ux of particulate organic matter is an integral component of the ocean carboncycle and crucial to our understanding of long-term changes in atmospheric CO

2.

This link between surface primary production and deeper waters has importantimplications for deep-sea food webs, sequestration of atmospheric CO

2, and for

regeneration and cycling of other elements as well. If migrating zooplankton doexport signi"cant amounts of dissolved organic material, we may be underestimatingtheir contribution to the ocean carbon cycle. In this study we found that verticalmigrators can increase dissolved C export (over respiratory C #ux alone) below themixed layer by excretion of DOC. Some of the dissolved organic matter excreted byzooplankton could be readily usable by microbes and feed the microbial loop; thisbecomes particularly important for bacteria below the deep winter-mixing depths,where migrators could seasonally be the major source of DOC. The relative import-ance of migration vs. other #uxes is highly dependent on the biomass of the migratingcommunity, and will di!er with location and season. As vertical migration of zooplank-ton is a ubiquitous phenomenon throughout the world's oceans, active transportshould always be included in calculations of export to deep waters.

Acknowledgements

Special thanks to the captain, crew, and marine technicians of the R.V. WeatherbirdII for help with sample collection. We are grateful to Dennis Hansell for helpfuldiscussions and for assistance with sample analyses, and to Richard Harbison, NancyCopley, and Kathy Coates for help with species identi"cation. We appreciate tech-nical assistance given by Bermuda Atlantic Time-series Study (BATS) technicians andby Erich Horgan. Hans Dam, David Malmquist, and an anonymous reviewer madehelpful suggestions and comments on the manuscript. This work was funded in partby NSF grants OCE-9301950, and OCE-9202336. This paper is BBSR contributionnumber 1524 and JGOFS contribution number 502.

References

Altabet, M.A., Small, L.F., 1990. Nitrogen isotopic ratios in fecal pellets produced by marine zooplankton.Geochimica et Cosmochimica Acta 54, 155}163.

Angel, M.V., 1989. Does Mesopelagic biology a!ect verical #ux? In: Berger, W.H., Smetacek, V.S., Wefer, G.(Eds.), Productivity of the Oceans: Present and Past. Dahlem Conference. pp. 155}173.

Atkinson, A., Ward, P., Murphy, E.J., 1996. Diel periodicity of Subantarctic copepods: relationshipsbetween vertical migration, gut fullness, and evacuation rate. Journal of Plankton Research 18 (8),1387}1405.

Batchelder, H.P., 1986. Phytoplankton balance in the oceanic subarctic Paci"c: grazing impact of Metridiapacixca. Marine Ecology Progress Series 34 (3), 213}225.

Bates, N.R., Michaels, A.F., Knap, A.H., 1996a. Seasonal and interannual variability of oceanic carbondioxide species at the U.S. IGOFS Bermuda Atlantic Time-series Study (BATS) site. Deep-Sea ResearchII 43 (2}3), 347}383.


Bates, N.R., Michaels, A.F., Knap, A.H., 1996b. Alkalinity changes in the Sargasso Sea: geochemicalevidence of calci"cation?. Marine Chemistry 51, 347}358.

Bidigare, R.R., 1983. Nitrogen excretion by marine zooplankton. In: Carpenter, E.J., Capone, D.G. (Eds.),Nitrogen in the Marine Environment. Academic Press, New York, pp. 385}409.

Carlson, C.A., Ducklow, H.W., Hansell, D.A., Smith, W.O., 1998. Organic carbon partitioning duringspring phytoplankton blooms in the Ross Sea polynya and the Sargasso Sea. Limnology and Oceanog-raphy 43 (3), 375}386.

Carlson, C.A., Ducklow, H.W., Michaels, A.F., 1994. Annual #ux of dissolved organic carbon from theeuphotic zone in the northwest Sargasso Sea. Nature 371, 405}408.

Carlson, C.A., Ducklow, H.W., Sleeter, T.D., 1996. Stocks and dynamics of bacterioplankton in thenorthwestern Sargasso Sea. Deep-Sea Research II 43, 491}515.

Cho, B.C., Azam, F., 1988. Major role of bacteria in biogeochemical #uxes in the ocean's interior. Nature332, 441}443.

Copin-MonteH gut, G., Avril, B., 1993. Vertical distribution and temporal variation of dissolved organiccarbon in the north-western Mediterranean Sea. Deep-Sea Research I 40 (10), 1963}1972.

Copping, A.E., Lorenzen, C.J., 1980. Carbon budget of a marine phytoplankton}herbivore system withcarbon-14 as a tracer. Limnology and Oceanography 25 (5), 873}882.

Dagg, M.J., 1976. Complete carbon and nitrogen budgets for the carnivorous amphipod, Calliopiuslaeviusculus (Kroyer). International Revue der gesamten Hydrobiologie 61, 297}357.

Dagg, M.J., Frost, B.W., Walser Jr., W.E., 1989. Copepod diel migration, feeding, and the vertical #ux ofpheopigments. Limnology and Oceanography 34 (6), 1062}1071.

Dagg, M.J., Wyman, K.D., 1983. Natural ingestion rates of the copepods Neocalanus plumchrus and N.cristatus calculated from gut contents. Marine Ecology Progress Series 13, 37}46.

Dam, H.G., Roman, M.R., Youngbluth, M.J., 1995. Downward export of respiratory carbon and dissolvedinorganic nitrogen by diel-migrant mesozooplankton at the JGOFS Bermuda time-series station.Deep-Sea Research I 42 (7), 1187}1197.

Deevey, G.B., 1971. The annual cycle in quantity and composition of the zooplankton of the Sargasso Seao! Bermuda I. The upper 500 m. Limnology and Oceanography 16, 219}240.

Deevey, G.B., Brooks, A.L., 1977. Copepods of the Sargasso Sea o! Bermuda: species composition,and vertical and seasonal distribution between surface and 2000 m. Bulletin of Marine Science 27,256}291.

Deuser, W.G., Muller-Karger, F.E., Evans, R.H., Brown, O.B., Esaias, W.E., Feldman, G.C., 1990. Surface-ocean color and deep-ocean carbon #ux: how close a connection?. Deep-Sea Research 37, 1331}1343.

DOE, 1994. In: Dickson, A.G., Goyet, C. (Eds.), Handbook of methods for the analysis of the variousparameters of the carbon dioxide system in seawater; version 2.0. US Department of Energy CO

2Science Team Report.

Donnelly, J., Torres, J.J., 1988. Oxygen consumption of midwater "shes and crustaceans from the easternGulf of Mexico. Marine Biology 97, 483}494.

Ducklow, H.W., Carlson, C.A., 1992. Oceanic bacterial production. In: Marshall, K.C. (Ed.), Advances inMicrobial Ecology, Vol. 12. Plenum Press, New York.

Fowler, S.W., Knauer, G.A., 1986. Role of large particles in the transport of elements and organiccompounds through the oceanic water column. Progress in Oceanography 16, 147}194.

Gregg, M.C., 1987. Diapycnal mixing in the thermocline: a review. Journal of Geophysical Research 92,5249}5286.

Hansson, L.J., Norrman, B., 1995. Release of dissolved organic carbon (DOC) by the scyphozoan jelly"shAurelia aurita and its potential in#uence on the production of planktic bacteria. Marine Biology 121,527}532.

Hays, G.C., Harris, R.P., Head, R.N., 1997. The vertical nitrogen #ux caused by zooplankton diel verticalmigration. Marine Ecology Progress Series 160, 57}62.

Heywood, K.J., 1996. Diel vertical migration of zooplankton in the Northeast Atlantic. Journal of PlanktonResearch 18 (2), 163}184.

Hirche, H.J., 1997. Life cycle of the copepod Calanus hyperboreus in the Greenland Sea. Marine Biology128, 607}618.


Hygum, B.H., Petersen, J.W., Sondergaard, M., 1997. Dissolved organic carbon released by zooplanktongrazing activity } a high quality substrate pool for bacteria. Journal of Plankton Research 19 (1),97}111.

Johnson, K.M., Wills, K.D., Butler, D.B., Johnson, W.K., Wong, C.S., 1993. Coulometric total carbondioxide analysis for marine studies: maximizing the performance of an automated gas excretion systemand coulometric detector. Marine Chemistry 44, 167}188.

Jumars, P.A., Penry, D.L., Baross, J.A., Perry, M.J., Frost, B.W., 1989. Closing the microbial loop: dissolvedcarbon pathway to heterotrophic bacteria form incomplete ingestion, digestion, and absorption inanimals. Deep-Sea Research 36, 483}495.

Kremer, P., 1977. Respiration and excretion by the ctenophore Mnemiopsis leidyi. Marine Biology 44,43}50.

Lampert, W., 1978. Release of dissolved organic carbon by grazing zooplankton. Limnology and Oceanog-raphy 23 (4), 831}834.

Lasker, R., 1966. Feeding, growth, respiration and carbon utilization of a euphausiid crustacean. Journal ofthe Fisheries Research Board of Canada 23, 1291}1317.

Le Borgne, R., Rodier, M., 1997. Net zooplankton and the biological pump: a comparison between theoligotrophic and mesotrophic equatorial Paci"c. Deep-Sea Research II 44, 2003}2023.

Ledwell, J.R., Watson, A.J., Law, C.S., 1993. Evidence for slow mixing across the pycnocline from an openocean tracer-release experiment. Nature 364, 701}703.

Longhurst, A.R., Bedo, A., Harrison, W.G., Head, E.J.H., Horne, E.P., Irwin, B., Morales, C., 1989.NFLUX: a test of vertical nitrogen #ux by diel migrant biota. Deep-Sea Research 36, 1705}1719.

Longhurst, A.R., Bedo, A.W., Harrison, W.G., Head, E.J.H., Sameoto, D.D., 1990. Vertical #ux ofrespiratory carbon by oceanic diel migrant biota. Deep-Sea Research 37 (4), 685}694.

Longhurst, A.R., Harrison, W.G., 1988. Vertical nitrogen #ux from the oceanic photic zone by diel migrantzooplankton and nekton. Deep-Sea Research 35, 881}889.

Longhurst, A.R., Harrison, W.G., 1989. The biological pump: pro"les of plankton production andconsumption in the upper ocean. Progress in Oceanography 22, 47}123.

Longhurst, A., Williams, R., 1992. Carbon #ux by seasonal vertical migrant copepods is a small number.Journal of Plankton Research 14 (11), 1495}1509.

Martin, J.H., Knauer, G.A., Broenkow, W.W., 1987. VERTEX: carbon cycling in the northeast Paci"c.Deep-Sea Research 34, 329}352.

Menzel, D.W., Ryther, J.H., 1961. Zooplankton in the Sargasso Sea o! Bermuda and its relation to organicproduction. Journal du Conseil/Conseil Permanent International pour l'Exploration de la Mer 26,250}258.

Michaels, A.F., Bates, N.R., Buesseler, K.O., Carlson, C.A., Knap, A.H., 1994. Carbon system imbalances inthe Sargasso Sea. Nature 372, 537}540.

Michaels, A.F., Knap, A.H., 1996. Overview of the U.S. JGOFS BATS and hydrostation S program.Deep-Sea Research II 43 (2}3), 157}198.

Morales, C.E., Harris, R.P., Head, R.N., Tranter, P.R.G., 1993. Copepod grazing in the oceanic northeastAtlantic during a 6 week drifting station: the contribution of size classes and vertical migrants. Journalof Plankton Research 15 (2), 185}211.

Moore, H.B., 1950. The relation between the scattering layer and the Euphausiacea. Biological Bulletin(Woods Hole) 99, 181}212.

Parsons, T.R., Takahashi, M., Hargrave, B., 1984. Biological Oceanographic Processes. Pergamon Press,New York, pp. 50.

Quetin, L.B., Ross, R.M., Uchio, K., 1980. Metabolic characteristics of midwater zooplankton: ammoniaexcretion, O : N ratios, and the e!ect of starvation. Marine Biology 59, 201}209.

Reeve, M.R., 1980. Large cod-end reservoirs as an aid to the live collection of delicate zooplankton.Limnology and Oceanography 26 (3), 577}580.

Regnault, M., 1987. Nitrogen excretion in marine and fresh-water crustacea. Biological Reviews of theCambridge Philosophical Society 62, 1}24.

Ritz, D.A., Hosie, G.W., 1982. Production of the euphausiid Nyctiphanes australis in Storm Bay, south-eastern Tasmania. Marine Biology 68 (1), 103}108.


Rodier, M., Le Borgne, R., 1997. Export Flux of particles in the western and central upper equatorialPaci"c, October 1994. Deep-Sea Research II 44, 2085}2113.

Roe, H.S.J., 1984. The diel migrations and distributions within a mesopelagic community in the North EastAtlantic. 4. The copepods. Progress in Oceanography 13, 353}388.

Roman, M.R., Dam, H.G., Gauzens, A.L., Napp, J.M., 1993. Zooplankton biomass and grazing at theJGOFS Sargasso Sea time series station. Deep-Sea Research I 40, 883}901.

Ross, R.M., 1982. Energetics of Euphausia pacixca. I. E!ects of body carbon and nitrogen and temperatureon measured and predicted production. Marine Biology 68, 1}13.

Schneider, G., Lenz, J., 1991. Zooplankton community metabolism in the upper 200 m of the central RedSea and the Gulf of Aden. Marine Ecology Progress Series 77 (2}3), 301}306.

Small, L.F., Fowler, S.W., Moore, S.A., La Rosa, J., 1983. Dissolved and fecal pellet carbon and nitrogenrelease by zooplankton in tropical waters. Deep-Sea Research 30, 1199}1220.

Small, L.F., Landry, M.R., Eppley, R.W., Azam, F., Carlucci, A.F., 1989. Role of plankton in the carbon andnitrogen budgets of Santa Monica Basin, California. Marine Ecology Progress Series 56, 57}74.

Soussi, S., Carlotti, F., Nival, P., 1997. Food and temperature dependent function of moulting rate incopepods * an example of parameterization of population dynamics models. Journal of PlanktonResearch 19 (9), 1331}1346.

Talley, L.D., 1982. Eighteen degree water variability. Journal of Marine Research 40, 757}775.Vidal, J., 1980. Physioecology of zooplankton. II. E!ects of phytoplankton concentration, temperature, and

body size on the development and molting rates of Calanus pacixcus and Pseudocalanus sp. MarineBiology 56, 135}146.

Wiebe, P.H., Copley, N.J., Boyd, S.H., 1992. Coarse-scale horizontal patchiness and vertical migration ofzooplankton in Gulf Stream warm-core ring 82-H. Deep Sea Research 39 (Suppl. 1), S247}S278.

Zhang, X., Dam, H.G., 1997. Downward export of carbon by diel migrant mesozooplankton in the centralequatorial Paci"c. Deep-Sea Research II 44, 2191}2202.


zooplankton vertical migration and the active transport of...

Documents