Journal of Plankton Research Vol.23 no.9 pp.963-975, 2001
© Oxford University Press 2001
Potential contribution that the copepod Neocalanus tonsus makes to downward carbon flux in the Southern Ocean
National Institute Of Water And Atmospheric Research, Po Box 14901, Kilbirnie, Wellington, 1 Department Of Marine Science, University Of Otago, Po Box 56, Dunedin And 2 Niwa Centre For Chemical And Physical Oceanography, C/o Chemistry Department, Department Of Marine Science, University Of Otago, Po Box 56, Dunedin, New Zealand
 |
Abstract |
|---|
 TOP Abstract INTRODUCTIONMETHOD AND RESULTSDISCUSSIONREFERENCES |
|---|
We estimate that Neocalanus tonsus makes a contribution to downwards carbon flux of 1.7–9.3 g C m–2 year–1, in subantarctic waters, the Subtropical Front and waters immediately to the north, based on its ontogenetic vertical migration minus the biomass of eggs, the products of which are returned to the surface the following season. This flux is an order of magnitude greater than that estimated (0.27 g C m–2 year–1) for vertical migration of large copepods in the North Atlantic. Over the total 55.6 x 106 km2 where N. tonsus is distributed, 0.17 Gt C year–1 are estimated to be lost annually to the ocean interior. In subantarctic water, this loss represents 1.4% of primary production and is 14% greater than the measured sedimented particulate organic carbon (POC) at 300 m. Similarly, in subtropical water, carbon loss to the ocean interior from N. tonsus seasonal migration is estimated to be 13% lower than measured POC flux. Nevertheless, N. tonsus was never found in time-incremental sediment trap samples. We hypothesize that the apparently proportionally different role of downwards seasonal migration of large copepods relative to sedimented POC in the North Atlantic compared with the subarctic North Pacific and Southern Ocean arises because of a combination of differences in the nutrient status of these oceans, differences in the rate of development of grazer populations in spring, and differences in life history characteristics of large copepods. The flux due to the behaviour of N. tonsus in different parts of its range, put into the context of the estimated global-mean net flux of 1.7–3.7 g C m–2 year–1 taken up by the ocean, may be a regionally significant amount. The summer downward migration of N. tonsus, however, does not entirely explain the observed seasonal variation in regional measurements of pCO2 off New Zealand.
|
INTRODUCTION |
|---|
|
TOPAbstractINTRODUCTIONMETHOD AND RESULTSDISCUSSIONREFERENCES |
|---|
The Southwest Pacific appears to be an important sink for atmospheric CO2 with some of the lowest recorded pCO2sea values (Murphy et al., 1991
; Takahashi et al., 1997; Currie and Hunter, 1998). In this region, air–sea CO2 flux is likely to be driven not only by physical mechanisms, but also by biological processes (Murphy et al., 1991; Watson, 1997; Currie and Hunter, 1998).
Particulate organic matter in the sea has autotrophic carbon-fixing phytoplankton as its primary source. Carbon leaves the photic zone either as sinking phytoplankton particles and aggregations, or faecal pellets produced by grazers (Fowler and Knauer, 1986), or through vertical migration of zooplankton [e.g. (Zhang and Dam, 1997)]. Longhurst and Williams estimated that carbon flux in the North Atlantic by seasonalvertical migrant copepods is insignificant relative to other oceanic fluxes (0.0018 Gt year–1) (Longhurst and Williams, 1992). However, unlike large North Atlantic calanoid copepods studied by Longhurst and Williams (Longhurst and Williams, 1992), the adults of Neocalanus tonsus (and their North Pacific congeners) appear not to return to surface waters after migrating downwards to overwinter and breed at depth (Jillett, 1968; Ohman et al., 1989). Additionally, N. tonsus can be found in swarm proportions in the Southern Ocean (Bradford-Grieve and Jillett, 1998), and in the Subtropical Frontal (STF) region N. tonsus can also be a significant fraction of zooplankton biomass (Voronina et al., 1988; Bradford-Grieve et al., 1999). This species is an important food source for higher trophic levels [e.g. basking sharks (Bradford, 1972); sei whales (Kawamura, 1974)]. Therefore, we re-evaluated the proposition that ontogenetic vertical migration transfers an insignificant amount of carbon in the case of the ontogenetically vertical migrant N. tonsus.
Neocalanus tonsus is distributed circumglobally in subantarctic waters, and in and north of the STF (Bradford-Grieve and Jillett, 1998). The majority of the spring/ summer surface-living population descends into deep water to mature and breed (Jillett, 1968; Bradford-Grieve and Jillett, 1998; Miller et al., 1999). The individuals that descend into deep water fuel their reproduction at depth on lipid reserves accumulated during spring and summer in Southern Ocean surface waters (Ohman et al., 1989). In winter, almost all surviving individuals are found well below 500 m in the water column, down to at least 1300 m (Voronina et al., 1988; Ohman et al., 1989). Neocalanus tonsus eggs are therefore laid below 500 m in winter. Developmental stages of N. tonsus probably migrate towards the surface without feeding (Saito and Tsuda, 2000), where juveniles arrive, at least as copepodite stage I (Ohman et al., 1989), possibly as earlier stages, in time for the spring growth season where they feed, grow and lay down reserves of wax esters (about November or slightly earlier). They begin their migration to deeper depths in mid to late January near the STF (Jillett, 1968; Bradford, 1972), but after mid-February further to the south (Voronina et al., 1988). A very small number of adult females are also observed at the surface in spring and their egg production depends on particulate food (Ohman, 1987). It is not known whether these females originate in deep water or develop at the surface (Miller et al., 1999).
The mass occurrence in near-surface waters in summer, growth and seasonal migration of N. tonsus to overwintering depths, deeper than 500 m, is a potentially significant mechanism contributing to the flux of carbon to the deep ocean in this region. The aim of this study is to review the existing literature and to assess the magnitude of the contribution that N. tonsus makes to the export of carbon; the contribution that diel vertical migration makes is not considered here. This analysis includes an estimation of the total carbon biomass of stage V copepodites (CV) ofN. tonsus, which migrate to deeper depths in summer, and of the carbon content of the eggs that are released at depth and which find their way to near-surface waters after hatching the following spring. Also, K. Currie (unpublished data) makes the observation that, between January and February, pCO2sea decreased at a rate of 2 µatm day–1 off the Otago Peninsula, near the Southland Front (a coastal analogue of the STF). This decrease was not related to temperature changes or to the flux of CO2 from the sea to the air. Because this period coincides with the period when N. tonsus leaves surface waters off the Otago Peninsula, we will also investigate the potential impact of the removal of N. tonsus respiration from surface waters at this time. The role that faecal pellets might have in carbon export is also evaluated.
|
METHOD AND RESULTS |
|---|
|
TOPAbstractINTRODUCTIONMETHOD AND RESULTSDISCUSSIONREFERENCES |
|---|
This paper is based almost entirely on data and information in the literature (Table I
). Calculations of the magnitude of the carbon flux, contributed by the onto-genetic vertical migration of N. tonsus, are based on a simplified model of their behaviour and role in the pelagic ecosystem (Figure 1). That is, we assume, in the first instance, that the entire net December–January (mid-summer) biomass migrates out of the surface 100 m to the ocean interior. The only biomass resulting from the previous year's population metabolism that returns to the surface the following spring is that contained in the eggs laid by deep-living females during the previous winter. All naupliar stages are non-feeding in Neocalanus plumchrus (Saito and Tsuda, 2000), and the earliest developmental stage of N. tonsus that has been recorded in surface water is CI (Ohman et al., 1989).
|
|
Area over which N. tonsus is distributed
The subantarctic area between the Antarctic Convergence (AC) and the STF was calculated from the mean position of these fronts (Bradford-Grieve and Jillett, 1998), using a graphical method that excluded land masses (Table II). Similarly, the areas of a 2° latitude strip at the STF and a 5° strip north of the STF were also estimated.
|
Summer biomass
A water column inventory of N. tonsus is used to assess summer biomass. Quantitative observations of the summer occurrence of N. tonsus have been made by only a few workers [see Bradford-Grieve and Jillett (Bradford-Grieve and Jillett, 1998), Figure 1
] (Table I). Where possible, these observations have been converted into integrated dry weight (DW) under a square metre of sea surface using the dry weight of CV given by Ohman et al. (Ohman et al., 1989) (i.e. 550 µg DW in late December). In addition, the total carbon biomass under a square metre of sea surface is calculated using a mean CV carbon content of N. tonsus of 353 µg carbon (C) (Ohman, 1987).
We assume that the integrated biomass in the upper 100 m encompasses the whole population before descent and that it is composed of CV alone. Data on the vertical distribution of N. tonsus in spring east of New Zealand were collected by the methods described by Bradford-Grieve et al. (Bradford-Grieve et al., 1998). These data show that the copepods were either concentrated entirely in the surface 25 m (6 out of 10 locations) or the surface 50 m (4 out of 10 locations) (J. M. Bradford-Grieve, unpublished data). There was very little biomass of this species at 50–100 m. Voronina et al. show a similar distribution in the upper water column at those stations (43–47°S) where N. tonsus was still in surface waters (Voronina et al., 1988).
Subantarctic water
Voronina et al. recorded an average of 5014 ± 2014 individuals (ind.) m–2 of N. tonsus in subantarctic waters in summer (Voronina et al., 1988). This mean value converts to 2758 mg m–2 DW. In the South Atlantic in summer, Voronina (Voronina, 1975) recorded a similar range of individuals per square metre (see her Figure 9). Therefore, we assume that 2758 mg m–2 DW (or 1770 mg C m–2) is the average summer biomass of N. tonsus for the region between the AC and the STF, since the data of Voronina (Voronina, 1988) are the most extensive. The subantarctic region covers 32.8 x 106 km2 (Table II).
Subtropical front
In summer, Voronina (Voronina, 1975) found narrow regions in the South Atlantic (covering at least 2° latitude on two transects), apparently just south of the STF, where the concentrations of N. tonsus were very high (100 000– 204 323 ind. m–2 or 55 000–112 378 mg m–2 DW). Jillett recorded swarms in November at 27 474 mg m–2 DW (Jillett, 1968). Kawamura reported surface concentrations up to 13 024 mg m–3 DW and more usually 3800–5700 mg m–3 DW (Kawamura, 1974). These surface swarm concentrations are not considered to be indicative of the general biomass of N. tonsus as they do not seem to cover extensive areas (Kawamura, 1974). A more average level of biomass in January in STF water appears to be 18 068 mg m–2 DW (Jillett, 1968). The biomass of N. tonsus in the STF region is assumed, therefore, to be 15 000 mg m–2 DW or 9600 mg C m–2, and the region where this level of biomass occurs is assumed to be 2° of latitude wide. The STF region covers 6.4 x 106 km2 (Table II).
Subtropical water
In summer, there is a region of variable width north of the STF where N. tonsus is also found (Bradford-Grieve and Jillett, 1998). Voronina's data suggest that the biomass of N. tonsus could be ~10 000 ind. m–2 or 5500 mg DW m–2 or 3530 mg C m–2 (Voronina, 1975). A similar biomass (6370 mg m–2 DW) is recorded here for north of the STF east of New Zealand (Table I). Therefore, we assume that biomass is 3500 mg C m–2 for the region north of the STF. In the SW Pacific and SW Indian Ocean, N. tonsus has been recorded as extending more than 15° north of the STF (Bradford-Grieve and Jillett, 1998), but over a much smaller distance in other parts of the circumglobal Southern Ocean. Because we do not know whether this northward extension is a regular occurrence, the conservative course is taken and the subtropical populations of N. tonsus are assumed to extend 5° of latitude north of the STF circumglobally. This region has a total area of 16.4 x 106 km2 (Table II).
Biomass of eggs
We assume that the biomass of N. tonsus is reduced to a quarter of the surface biomass by winter [cf. (Longhurst and Williams, 1992)] as a result of deaths or of predation by other zooplankton (e.g. chaetognaths) and larger organisms such as fish. The biomass of eggs, which is all that is returned to the surface after winter breeding of N. tonsus at depth, is calculated based on one-quarter of the summer surface biomass and assuming that the female:male ratio is 1:1 [see (Jillett, 1968)] (Table III). We are assuming that eggs laid by overwintering females are not extensively preyed upon, although this undoubtedly occurs.
|
Egg production per female N. tonsus is estimated to be 285 [(Ohman, 1987
); his Table 5]. The density of an N. tonsus egg is assumed to be 1.027 g cm–3 (Ohman, 1987). Since the diameter of an N. tonsus egg is 139 µm (Ohman, 1987), the volume of an N. tonsus egg is, therefore, 1.4 x 106 µm3 = 1.4 x 10–6 cm3. The calculated wet weight of an egg of N. tonsus is 1.445 µg. If we assume that the dry weight of an egg is 34% of wet weight, and carbon content is 66% of dry weight (Omori, 1969), then an N. tonsus egg is estimated to be 0.491 µg DW or 0.324 µg C.
|
Carbon potentially exported through faecal pellets
We do not know whether faecal pellets of large copepods sediment out of the surface layers in the Southern Ocean, although this mechanism is considered to be an important mode of organic carbon transfer out of the euphotic zone (Fowler and Knauer, 1986). Here, we calculate the theoretical biomass of faecal pellets and compare this biomass with recent measurements of the quantity of organic matter sedimenting to 300 m east of New Zealand (Nodder and Northcote, 2001) (Table IV).
|
The carbon content of N. tonsus faecal pellets (Table IV
) is calculated using several assumptions. Neocalanus tonsus is in the upper water layers for at least 3 months and has been recorded in surface waters during the period October–January (Jillett, 1968; Bradford, 1972; Ohman et al., 1989). For the purposes of this calculation, we assume, conservatively, that faecal pellets sediment out of the upper water column only from the CV and that this occurs only in December and January.
Faecal pellet volume is calculated from the relationship between body mass and pellet volume (Legendre and Michaud, 1998):
 |
), the upper limit of which is close to the volume calculated above for N. tonsus.
There are no direct measurements of the mass and carbon content of N. tonsus faecal pellets in the literature. We therefore use data from other species of large copepods in the same family. Honjo and Roman show that the dry weight of Calanus finmarchicus faecal pellets is 10–26 µg (mean 19 µg), with a combustible organic fraction of 25–45% (Honjo and Roman, 1978). Assuming that the weight of a female C. finmarchicus is 150 µg C (Carlotti and Hirche, 1997), then the volume of its faecal pellet would be 2.17 x 106 µm3. The dry weight of an N. tonsus faecal pellet is estimated proportionally to be ~13 µg C using the data on pellet carbon for C. finmarchicus (Honjo and Roman, 1978) and the faecal pellet volumes estimated from body carbon for both species (see the previous paragraph).
The gut passage time for N. tonsus is estimated from the work of Ohman, who showed that CV fed continuously had an average of 30 min between pellets (Ohman, 1987). This rate compares well with a gut passage time in N. plumchrus of 23.4 min at food concentrations >4 µg chlorophyll l–1 and 85 min at a food concentration of 0.33 µg chlorophyll l–1 (Dagg and Walser, 1987). Therefore, the number of faecal pellets produced per day by N. tonsus is assumed to be 48 and it is assumed that there is no difference between night and day pellet production.
The calculated carbon flux (mg C m–2 day–1) from CV faecal pellets is two orders of magnitude greater than the measured particulate organic carbon (POC) flux at 300 m in summer (Nodder and Northcote, 2001) (Table IV, column 5).
Impact on pCO2 of removal of respiration of N. tonsus from surface waters in summer
The act of downward migration by N. tonsus not only removes their carbon from surface waters, but also the CO2 they produce through respiration. The daily respiration of CO2 just before N. tonsus descends is calculated here (Table V) and compared with seasonal information on pCO2 of sea water (K. Currie, unpublished data) to determine whether the downward migration of N. tonsus in January can be detected. We expect that the descent of N. tonsus will perceptively impact pCO2 initially, but that the role that N. tonsus plays in total community respiration at the surface would be, to some extent, taken over by that of the microzooplankton on which N. tonsus prey (Atkinson, 1996). That is, the removal of N. tonsus predation pressure would allow the microzooplanton population to grow.
In order to calculate the amount of carbon respired by N. tonsus, we assume that the respiratory quotient (RQ) (or ratio of CO2 produced to O2 consumed) is 1. For aquatic animals that excrete ammonia, RQ is 0.949 (or even higher) [(Downing and Rigler, 1984), p. 443]. James and Wilkinson estimated the relationship between oxygen consumption and body size at 14–16°C (James and Wilkinson, 1988). For planktonic crustacea, log M = log a + b log W, where M is oxygen uptake (µl O2 ind.–1 h–1) and W is body dry weight (µg). For Calanus australis, a = 0.0196 (log a = –1.707) and b = 0.632. Therefore, M = 1.059 µl O2 ind.–1 h–1 (25.41 µl O2 ind.–1 day–1). Given that 12.011 g C as CO2 occupy 22.4 l at STP, then 13.63 µg C ind.–1 day–1 is respired. Alternatively, Vidal and Whitledge give a relationship between rates of oxygen consumption and DW for spring N. plumchrus + Neocalanus cristatus at 4°C so that M = 14.91 µl O2 ind.–1 day–1 or 7.99 µg C ind.–1 day–1 are respired (Vidal and Whitledge, 1982).
Since summer water temperatures in the Southern Ocean are nearer the experimental temperatures used by James and Wilkinson, we use their equation, which predicts that N. tonsus respires 13.63 µg C ind.–1 day–1 (James and Wilkinson, 1988). Therefore, in summer, immediately before N. tonsus descends to deep water, we might expect them to be respiring 68.3, 371.7 and 136.3 mg C m–2 day–1 in subantarctic water, STF waters and north of the STF, respectively (or 5.7, 30.9 and 11.3 mmol C m–2 day–1).
Between 20 January 1998 and 16 February 1998, a decrease in pCO2 of surface sea water was observed in the Southland Current off Otago Peninsula, New Zealand (K. Currie, unpublished data). Preliminary models suggest that this is due to biological factors rather than thermodynamic or air–sea exchange effects (K. Currie, unpublished data).
The midsummer removal of the respiration potential of N. tonsus potentially reduces the pCO2 in the surface waters, thus affecting the air–sea flux of CO2. In subantarctic waters, N. tonsus respires ~5.7 mmol C m–2 day–1. This is equivalent to 6 x 10–2 µmol C kg–1 being respired per day, assuming that the upper 100 m of the water column is fully mixed. The effect on pCO2 of removal of this carbon from the surface waters can be estimated by using the Revelle factor (R):
 |
), and a value of 10 for the Revelle factor is typical for open-water situations (Liss, 1983). 
pCO2 thus calculated is 0.1 µatm day–1. Similar calculations for frontal and subtropical waters indicate that pCO2 changes of ~1 µatm day–1 would result when the N. tonsus respiration is removed. |
DISCUSSION |
|---|
|
TOPAbstractINTRODUCTIONMETHOD AND RESULTSDISCUSSIONREFERENCES |
|---|
Role of faecal pellets in downwards carbon flux
To estimate the contribution that N. tonsus makes to downwards carbon flux, we have considered the possibility that their faecal pellets make a major contribution. Nevertheless, calculations of the quantity of carbon in the faecal pellets produced daily by late stage N. tonsus are two orders of magnitude greater than the total daily measured flux of POC in subtropical and subantarctic waters east of New Zealand (Nodder and Northcote, 2001) (Table IV, columns 4 and 5). This implies that either we have overestimated the carbon in a faecal pellet and the number of pellets produced in a day, and/or faecal pellets do not sediment out of these waters, but are mostly reprocessed in the upper water column. In the case of subantarctic water, the latter result is likely, as our analysis of the subantarctic ecosystem (Bradford-Grieve et al., 1999) shows that it behaves like an oligotrophic system even though there is plenty of dissolved inorganic nitrate nitrogen (N). Small cells dominate the autotrophs and the food web approaches the ‘microbial’ web or even ‘microbial loop’ system (Legendre and Rassoulzadegan, 1995), which is characterized by low sedimentation of phaeopigment (Nodder and Gall, 1998). Therefore, we have not included faecal pellet production in our estimate of the contribution the N. tonsus makes to carbon flux to the deep ocean even though there will be a minor loss. Faecal pellet fluxes are generally <5% of total particle flux at deep ocean sites (Pilskaln and Honjo, 1987; Ayukai and Hattori, 1992).
pCO2 and N. tonsus respiration
The respiration of N. tonsus returns the greatest amount of CO2 to STF surface waters where their biomass is greatest (
1 µatm day–1). Therefore, removal of this potential, assuming that there is no compensatory increase in respiration from heterotrophic prey of N. tonsus, would be of the order of ~30 µatm in a month. This is about half of the maximum observed change in pCO2 between January and February 1998 off Otago Peninsula (K. Currie, unpublished results). Nevertheless, it is likely that there will be a compensatory increase in the respiration of, for example, microzooplankton on which N. tonsus apparently preys and, therefore, the descent of N. tonsus will contribute only partially to the observed pCO2 decrease in late summer.
Carbon flux due to ontogenetic vertical migration of N. tonsus
Annual downwards carbon flux contributed by N. tonsus is estimated from the downwards migration of surface biomass in summer minus the carbon contained in the eggs, produced by surviving females. These eggs form the basis of the following year's surface population. We estimate that the carbon that is lost between summer and the following spring is 3.4, 9.3 and 1.7 g C m–2 year–1 in subtropical, STF and subantarctic waters, respectively. We note that the carbon that is returned to the surface in spring is an insignificant proportion (3%) of the biomass that descends in summer.
In the North Atlantic Ocean, there is considerableseasonal information on the vertical and seasonal distribution of large copepods. From these data, Longhurst and Williams suggest that 0.3 g C m–2 year–1 of overwintering biomass is lost before next spring (Longhurst and Williams, 1992). If our calculations are correct (1.7–9.3 g C m–2 year–1), annual carbon lost through the seasonal vertical migration of N. tonsus in the Southern Ocean is an order of magnitude greater, on a square metre basis, than observed in the North Atlantic. Are these differences real?
Impact of assumptions
Our estimate depends on the assumption that all the CV N. tonsus population descends in midsummer and that the predation that occurs during descent does so at depths deeper than the mixed layer and that the predators do not return to the mixed layer. Also, our estimate of surface summer biomass of N. tonsus is derived from limited data based on counts of individuals and their carbon content from Ohman (Ohman, 1987).
The assumption that none of the carbon that predators obtained from feeding on descending N. tonsus is respired in the mixed layer may not be reasonable. Currently, we do not have any information on the behaviour of predators. Among potential predators, Pseudosagitta gazellae, a large antarctic/subantarctic chaetognath species, is found in maximum abundance between 50 and 100 m. It does not undergo diel migration, but migrates to deep water in winter (David, 1955). The summer mixed-layer depth is <40 m in the north of the range of N. tonsus, but is 60 to >100 m over a large proportion of subantarctic water [M. Hadfield, National Institute of Water and Atmospheric Research (NIWA), personal communication, calculated from Levitus (Levitus and Boyer, 1994; Levitus et al., 1994). Therefore, an unknown proportion of predation on N. tonsus is likely to occur in the mixed layer during descent. The proportion of the N. tonsus population that is preyed upon early during descent in subantarctic water needs to be estimated to firm up our estimates of downwards carbon flux.
Our assumption that the midsummer population of CV N. tonsus represents the total population that descends underestimates the downward flux due to vertical migration. Not included in our assumption is the fact that the descent of CV takes place as early as early November, at least at 45°S off southeastern New Zealand (Ohman et al., 1989). By early November, at least 40% of the population is found deeper than 500 m.
It is possible that we have overestimated the average biomass of N. tonsus globally. The biomass data used for the present calculations come from the very few sources where data on N. tonsus densities and weights have been collected in December and January (Table I), and these concentrations have been extrapolated over large areas. Evaluation of the representativeness of the numbers that we have used, and the impact of interannual variability, will have to await further quantitative sampling in the Southern Ocean, especially in December and January.
Comparison with total zooplankton biomass data
The recent collation of zooplankton biomass information on a global scale [e.g. (Tseitlin et al., 1997)] presents data in a manner that allows a summer maximum to be calculated. For example, an average wet weight biomass of 200 mg m–3 or 2350 mg m–2 DW (0–100 m) is the upper limit of total biomass for 45°S. This translates to a summer maximum of 272 mg m–3 or 3397 mg m–2 DW. There are a number of instances in Table I where the summer biomass of N. tonsus, alone, is much greater. Were the concentrations of N. tonsus available for this study, by chance, greater than average because of interannual variability or because they were collected in relatively biologically rich locations? Or were the available zooplankton biomass data for the Southern Ocean (Tseitlin et al., 1997) not collected at the time of the summer surface maximum of N. tonsus, therefore underestimating total midsummer maximum zooplankton biomass? Unfortunately, we do not have the information necessary to answer these questions.
In considering the impact of ontogenetic vertical migration of large copepods on carbon flux in the Southern Ocean, it is necessary to take into account the date on which total zooplankton biomass estimates were made. That is, surface zooplankton biomass measurements need to be evaluated in relation to what is known about the timing of vertical migration. Neocalanus tonsus spends a relatively small proportion of its time in surface water layers (from September/October to January) (Ohman et al., 1989). Even then, they are nearly all in the surface 150 m only in early October. During the remainder of the period, when they may be found near the surface, 50% of the population is found deeper than 500 m.
Impact of life history attributes of N. tonsus
The ability of N. tonsus to make an apparently remarkable contribution to carbon flux may be partly due to a unique characteristic of its life history. The reproductive capacity of deep-living females of N. tonsus is not the only source of increase in this species. Jillett (Jillett, 1968) notes that even though surface hauls are dominated by CV in spring and summer, a few females are found at the surface in August and September and through to January (Bradford, 1972). These females appear to be genetically indistinguishable from their deep-living relatives (Miller et al., 1999). It is not known how they arrive at the surface, as they appear to be completely absent from surface waters in winter (Jillett, 1968). These females actively feed and are capable of laying eggs, based on particulate ambient food (Ohman, 1987). Not only does the reproductive capacity of this species support extensive predation [(Bradford-Grieve and Jillett, 1998) and references therein], but it is uniquely able to respond to variability in primary production of surface waters. This aspect of its life history serves to augment the concentrations of developmental stages in surface waters such that the density of individuals is apparently not only dependent on the density of deep-living females that survived the previous winter at depth. The North Pacific Neocalanus do not have a similar capacity to breed at the surface (Miller et al., 1984; Miller and Clemons, 1988).
It is interesting to note that examination of time-incremental moored sediment trap samples [see (Nodder and Northcote, 2001)] for ‘swimmers’ revealed no identifiable N. tonsus. Samples examined were collected from late November to late February in traps suspended at 300 and 1000 m in subtropical and subantarctic waters, and from August to October from a trap suspended at 1000 m in subantarctic waters. Other copepods were found in some of the samples (Metridia, Pleuromamma, Clausocalanus, Scaphocalanus, other scolectrichids and Oncaea), so the impression gained is that this large copepod, N. tonsus, actively avoids going into the traps on their downward migration. At the end of their life, they are either not recognizable or are not dense enough to be caught in the 1000 m trap when they sink out of the water column, or the traps were not deep enough to catch them.
Comparison with other fluxes
The total annual loss of carbon over the whole area of distribution of N. tonsus is 0.171 Gt C year–1. This number is calculated from the total summer CV biomass (Table I) minus the biomass of eggs produced by surviving females (Table III) over an area of 55.6 x 106 km2 (Table II). In subantarctic waters alone, this loss is 0.056 Gt C year–1 or 1.7 g C m–2 year–1. Average primary production in subantartic water is 80 g C m–2 year–1 (Moore and Abbott, 2000) or 2.624 Gt C year–1 (area of subantarctic from Table II). The sedimentation of POC from subantarctic surface waters to 1000 m immediately east of New Zealand is calculated to be 0.5 g C m–2 year–1 [(Nodder and Northcote, 2001); Table VI). The POC flux is possibly overestimated for subantarctic waters circumglobally as these measurements were made close to the STF and may reflect processes occurring in this productive region immediately east of New Zealand (Bradford-Grieve et al., 1999). Nevertheless, from these data, migration of N. tonsus is associated with a loss of carbon that is ~2% of the measured primary production and is about three times greater than calculated sedimented POC flux. Similarly, in waters north of the STF, 3.4 g C m–2 year–1 are exported by the descent of N. tonsus, which is about three times greater than the calculated total POC flux at 1000 m of 1.3 g C m–2 year–1 and is ~3% of calculated primary production of 106 g C m–2 year–1.
|
Annual POC flux at 1000 m at 48°N in the North Atlantic (Table VI
) was 1.5 g C m–2 year–1. If we replace the estimated particle flux of 0.033–0.093 g C m–2 year–1, based on primary production (Longhurst and Williams, 1992), then the flux due to seasonal vertical migrant copepods is ~17% of POC flux to 1000 m.
In the Northeast Pacific at 50°N, the annual average POC flux between 1983 and 1993 was 2.7 g C m–2 year–1 (Table VI). The late summer biomass of N. plumchrus in the Subarctic Pacific was on average 87 g wet weight (WW) m–2 (0–150 m) (range <25–150 g WW m–2) between 1956 and 1981 (Mackas et al., 1998) [or 5.0 g C m–2 using the equation of Wiebe (Wiebe, 1988)]. If we make the same assumptions about the export of carbon due to seasonal vertical migration being approximately equivalent to the late summer biomass of N. plumchrus (here we are ignoring the contribution that Neocalanus flemingeri and N. cristatus make), then the annual loss of carbon is ~5.0 g C m–2 year–1, which is, on average, greater than the mean annual POC flux at 1000 m (Table VI).
Neocalanus tonsus and N. plumchrus carbon flux in the Southern Hemisphere and subarctic North Pacific, respectively, through ontogenetic vertical migration, seems be of a similar size or larger than the sedimentary flux at 1000 m, whereas in the North Atlantic the downward flux of large copepods is much smaller than the sedimentary flux to 1000 m (Table VI). Why might this be so?
We know that the three regions have different nutrient status and physical characteristics of the upper water column, with consequent implications for ecosystem structure and function [e.g. (Parsons and Lalli, 1988)]. In the Southern Ocean, iron and silica limitation in subantarctic waters (Boyd et al., 1999) and low summer inorganic nutrients in subtropical water (Bradford-Grieve et al., 1999) result in small cells dominating autotrophs that contribute very little directly to downward carbon flux (Nodder and Gall, 1998; Boyd and Newton, 1999). Thus, subantarctic and subtropical ecosystems are skewed towards microbial processes (Bradford-Grieve et al., 1999), although there is evidence that a silica- and organic-rich sedimentation event occurs in subtropical water just north of the STF in October (Nodder and Northcote, 2001). In this context, N. tonsus appears to prefer protozoan food (Atkinson, 1996; Bradford-Grieve et al., 1998). Similarly, the subarctic North Pacific phytoplankton populations are skewed towards microbial processes and are iron limited (Martin et al., 1991), whereas in the North Atlantic a relatively good supply of silica and other nutrients leads to a conspicuous spring bloom of diatoms [e.g. (Lochte et al., 1993)] which sediment out of the upper water layers during the bloom period (Honjo and Manganini, 1993).
Combined with the above differences, there are conspicuous differences in total planktonic community partitioning between the three regions. In the North Atlantic, in spring (Harrison et al., 1993), phytoplankton and bacteria make up the majority of the total community biomass (~85%) (Figure 2). In the Southwest Pacific (Bradford-Grieve et al., 1999) and Northeast Pacific (Boyd et al., 1999), these two compartments were 45–69 and 48%, respectively, of the total community biomass (Figure 2). In the North Atlantic, mesozooplankton were only 3–4% of the total community biomass, whereas in the Southwest Pacific and Northeast Pacific this compartment was 12–40 and 14%, respectively, of the total community biomass. It appears that, in the North Atlantic, grazers are far behind in development of their populations, compared with the Southwest Pacific and Northeast Pacific (Figure 2). This has implications for the recycling of organic and inorganic material in the upper water column through the processing of phytoplankton and bacterial biomass by their consumers. Is it possible that more biological material can be produced annually in surface layers and sedimented or migrated out of the water column in the Southwest Pacific because of the efficiency with which limiting nutrients are used? We note that in spring in the North Atlantic, where a rapid and direct sedimentation of phytoplankton occurs, the C:N ratio of sedimented material at 1000 m is close to the Redfield ratio of 6.6 (Redfield et al., 1963). In comparison, in the SW and NE Pacific spring trap C:N ratios at 1000 m are well above 6.6, implying that the original nitrogen contained in the sedimented autotropic particles has been remineralized in the water column [between 100 and 200 m in the NE Pacific; (Wong et al., 1999; Boyd et al., 1999), their Figure 6]. These observations, based on recent data, are parallel to the notion of Parson and Lalli (Parson and Lalli, 1988), who introduced the idea that the ecological efficiency of the North Pacific might be greater than that of the North Atlantic. That is, ‘relatively little energy and material fixed by the nanoplankton [in the North Pacific] may be lost to the larger consumers by the insertion of a ciliate "extra link" into the food chain’.
|
It is instructive to place this assessment of carbon export to depth in a context of global carbon dynamics. Prior to the industrial revolution, the global carbon cycle was close to steady state. Gross carbon exchanges in this steady state are quite uncertain. Those exchanges between the atmosphere and ocean (as CO2) are believed to have been 50–100 Gt C year–1, corresponding to fluxes in the range 140–280 g C m–2 year–1. Most of this uncertainty is in the dependence of the ‘gas exchange co-efficient’ on atmospheric conditions such as wind speed, but values near the upper end of the range are required for consistency with ‘bomb 14C’ (Wanninkhof, 1992
). The carbon cycle has been perturbed by human activities over the past 200 years, due principally to atmospheric release of CO2 from fossil fuel combustion and land use change, averaging ~6 Gt C year–1 during the 1980s (Schimel et al., 1995). Such perturbation has resulted in net carbon uptake into the ocean and terrestrial biosphere, reducing the atmospheric accumulation to only 3.2 ± 0.2 Gt C year–1. The partitioning of net carbon flows between these reservoirs is uncertain. Most carbon cycle models calibrated to ‘bomb 14C’ data favour an ‘ocean uptake’ of ~2 Gt C year–1 during the 1980s (Schimel et al., 1995), which corresponds to a global-mean net flux of 5.6 g C m–2 year–1 to the ocean. However, estimates based on global mapping of direct pCO2 measurements andgas exchange coefficient favour uptakes in the range 0.60–1.34 Gt C year–1 (Takahashi et al., 1997),corresponding to global-mean net flux of 1.7–3.7 g C m–2 year–1. Thus, the estimate of 1.7–9.2 g C m–2 year–1 exported by N. tonsus in the Southern Ocean may be a regionally significant amount relative to the global-mean net flux.
|
Acknowledgments |
|---|
We are grateful to Alan Longhurst (Cajarc, France) and Philip Boyd (NIWA, Dunedin, New Zealand) for discussing aspects of this paper with us. This work was funded by the New Zealand Foundation for Research Science and Technology, Contract CO1214.
|
REFERENCES |
|---|
|
TOPAbstractINTRODUCTIONMETHOD AND RESULTSDISCUSSIONREFERENCES |
|---|
Atkinson, A. (1996) Subantarctic copepods in an oceanic, low chlorophyll environment: ciliate predation, food selectivity and impact on prey populations. Mar. Ecol. Prog. Ser., 130, 85–96.
Ayukai, T. and Hattori, H. (1992) Production and downward flux of zooplankton fecal pellets in the anticyclonic gyre off Shikoku, Japan. Oceanol. Acta, 15, 163–172.
Boyd, P. W. and Newton, P. P. (1999) Does planktonic community structure determine downward particulate organic carbon flux in different oceanic provinces? Deep-Sea Res. I, 46, 63–91.
Boyd, P., LaRoche, J., Gall, M., Frew, R. and McKay, R. M. L. (1999) The role of iron, light and silicate in controlling algal biomass in sub-Antarctic water SE of New Zealand. J. Geophys. Res., 104, 13,395–13,408.
Bradford, J. M. (1972) Systematics and ecology of New Zealand central east coast plankton samples at Kaikoura. N. Z. Oceanogr. Inst. Mem., 54, 1–87.
Bradford-Grieve, J. M. and Jillett, J. B. (1998) Ecological constraints on horizontal patterns—with special reference to the copepod Neocalanus tonsus (Brady, 1883). In Pierrot-Bults, A. C. and van der Spoel, S. (eds), Pelagic Biogeography, ICoPB II. Proceedings of the 2nd International Conference. Final Report of SCOR/IOC Working Group 93. IOC Workshop Rep., 142, 65–77.
Bradford-Grieve, J. M., Murdoch, R., James, M., Oliver, M. and McLeod, J. (1998) Mesozooplankton biomass, composition, and potential grazing pressure on phytoplankton during austral winter and spring 1993 in the Subtropical Convergence region near New Zealand. Deep-Sea Res., 45, 1709–1737.
Bradford-Grieve, J. M., Boyd, P. W., Chang, F. H., Chiswell, S., Hadfield, M., Hall, J. A., James, M. R., Nodder, S. D. and Shushkina, E. A. (1999) Pelagic ecosystem structure and functioning in the Subtropical Front region east of New Zealand in austral winter and spring 1993. J. Plankton Res., 21, 405–428.
Carlotti, F. and Hirche, H.-J. (1997) Growth and egg production of female Calanus finmarchicus: An individual-based physiological model and experimental validation. Mar. Ecol. Prog. Ser., 149, 91–104.
Currie, K. I. and Hunter, K. A. (1998) Surface water carbon dioxide in the waters associated with the Subtropical Convergence, east of New Zealand. Deep-Sea Res., 45, 1765–1777.
Currie, K. I. and Hunter, K. A. (1999) Seasonal variation of surface water CO2 partial pressure in the subtropical convergence zone east of New Zealand. Mar. Freshwater Res., 50, 375–382.
Dagg, M. J. and Walser, W. E. (1986) The effect of food concentration on fecal pellet size in marine copepods. Limnol. Oceanogr., 31, 1006–1071.
Dagg, M. J. and Walser, W. E. (1987) Ingestion, gut passage, and egestion by the copepod Neocalanus plumchrus in the laboratory and in subarctic Pacific Ocean. Limnol. Oceanogr., 32, 178–188.
David, P. M. (1955) The distribution of Sagitta gazellae Ritter-Zahony. Discovery Rep. 27, 235–278.
Downing, J. A. and Rigler, F. H. (eds) (1984) A Manual on Methods for the Assessment of Secondary Productivity in Freshwaters. Blackwell Scientific, Oxford, 501 pp.
Flint, M. V. and Yakushev, Ye. U. (1988) Spatial structure of mesoplankton and distribution of dissolved ammonia in the vicinity of Pulkovskaya seamount. Oceanology, 28, 655–660.
Fowler, S. W. and Knauer, G. A. (1986) Role of large particles in the transport of elements and organic compounds through the oceanic water column. Prog. Oceanogr., 16, 147–194.
Harrison, W. G., Head, E. J. H., Horne, E. P. W., Irwin, B., Li, W. K. W., Longhurst, A. R., Paranjape, M. A. and Platt, T. (1993) The western North Atlantic Bloom Experiment. Deep-Sea Res. II, 40, 279–395.
Honjo, S. and Manganini, S. J., (1993) Annual biogenic particle fluxes to the interior of the North Atlantic Ocean, studied at 34°N 21°W and 48°N 21°W. Deep-Sea Res., 40, 587–607.
Honjo, S. and Roman, M. R. (1978) Marine copepod fecal pellets: production, preservation and sedimentation. J. Mar. Res., 36, 45–57.
James, M. R. and Wilkinson, V. H. (1988) Biomass, carbon ingestion, and ammonia excretion by zooplankton associated with an upwelling plume in western Cook Strait, New Zealand. N. Z. J. Mar. Freshwater Res., 22, 249–257.
Jillett, J. B. (1968) Calanus tonsus (Copepoda, Calanoida) in southern New Zealand waters with notes on the male. Aust. J. Mar. Freshwater Res., 19, 19–30.
Kawamura, A. (1974) Food and feeding ecology in the Southern Sei whale. Sci. Rep. Whales Res. Inst. Tokyo, 26, 25–144, 3 pls.
Legendre, L. and Michaud, J. (1998) Flux of biogenic carbon in oceans: size-dependent regulation by pelagic food webs. Mar. Ecol. Prog. Ser., 164, 1–11.
Legendre, L. and Rassoulzadegan, F. (1995) Plankton and nutrient dynamics in marine waters. Ophelia, 41, 153–172.
Levitus, S. and Boyer, T. B. (1994) World Atlas 1994. Vol. 4. Temperature. U. S. NOAA, NESDIS, Washington, D.C. 4.
Levitus, S., Burgett, R. and Boyer, T. B. (1994) World Atlas 1994. Vol. 3. Salinity. U. S. NOAA, NESDIS, Washington, D.C. 3.
Longhurst, A. and Williams, R. (1992) Carbon flux by seasonal vertical migrant copepods is a small number. J. Plankton Res., 14, 1495–1509.
Liss, P. S. (1983) Gas transfer: experiments and geochemical implications. In Liss, P. S. and Slinn, W. G. N. (eds), Air–Sea Exchange of Gases and Particles. D. Riedel, Dordrecht, pp. 241–298.
Lochte, K., Ducklow, H. W., Fasham, M. J. R. and Stienen, C. (1993) Plankton succession and carbon cycling at 47°N 20°W during the JGOFS North Atlantic Bloom Experiment. Deep-Sea Res. II, 40, 91–114.
Mackas, D. L., Goldbaltt, R. and Lewis, A. G. (1998) Interdecadal variation in developmental timing and Neocalanus plumchrus populations at Ocean Station P in the subarctic North Pacific. Can. J. Fish. Aquat. Sci., 55, 1878–1893.
Marin, V. and Antezana, T. (1985) Species composition and relative abundance of copepods in Chilean fjords. J. Plankton Res., 7, 961–966.
Martin, J. H., Knauer, G. A., Karl, D. M. and Broenkow, W. W. (1987) VERTEX: carbon cycling in the northeast Pacific. Deep-Sea Res., 34, 267–285.
Miller, C. B. and Clemons, M. J. (1988) Revised life history analysis for large grazing copepods in the subarctic Pacific Ocean. Prog. Oceanogr., 20, 293–313.
Miller, C. B., Frost, B. W., Batchelder, M. J., Clemons, M. J. and Conway, R. E. (1984) Life histories of large, grazing copepods in a subarctic ocean gyre: Neocalanus plumchrus, Neocalanus cristatus and Eucalanus bungii in the Northeast Pacific. Prog. Oceanogr., 13, 210–243.
Miller, K. M., Bradford-Grieve, J. M. and Jillett, J. B. (1999) The genetic relationship between spring surface-living and winter deep-living females of Neocalanus in the Southern Ocean. Mar. Biol., 134, 99–106.
Moore, J. K. and Abbott, M. R. (2000) Phytoplankton chlorophyll distribution and primary production in the Southern Ocean. J. Geophys. Res., 105, 28709–28722.
Murphy, P. P., Feely, R. A., Gammon, R. H., Harrison, D. E., Kimberly, C. K. and Waterman, L. S. (1991) Assessment of air–sea exchange of CO2 in the South Pacific during austral autumn. J. Geophys. Res., 96, 20455–20465.
Nodder, S. and Gall, M. (1998) Pigment fluxes from the Subtropical Convergence Region, east of New Zealand: relationships to planktonic community structure. N. Z. J. Mar. Freshwater Res., 32, 441–465.
Nodder, S. D. and Northcote, L. C. (2001) Episodic particulate fluxes at southern temperate mid-latitudes (41–45°S) in the Subtropical Front region, east of New Zealand. Deep-Sea Res. I, 48, 833–864.
Ohman, M. D. (1987) Energy sources for recruitment of the subantarctic copepod Neocalanus tonsus. Limnol. Oceanogr., 32, 1317–1330.
Ohman, M. D., Bradford, J. M. and Jillett, J. B. (1989) Seasonal growth and lipid storage of the circumglobal, subantarctic copepod, Neocalanus tonsus (Brady). Deep-Sea Res., 36, 1309–1326.
Omori, M. (1969) Weight and chemical composition of some important oceanic zooplankton in the North Pacific Ocean. Mar. Biol., 3, 4–10.
Parsons, T. R. and Lalli, C. M. (1988) Comparative oceanic ecology of the plankton communities of the subarctic Atlantic and Pacific Oceans. Oceanogr. Mar. Biol. Annu. Rev., 26, 317–359.
Pilskaln, C. H. and Honjo, S. (1987) The fecal pellet fraction of biogeochemical particle fluxes to the deep sea. Global Biogeochem. Cycles, 1, 31–48.
Redfield, A. C., Ketchum, B. H. and Richards, F. A. (1963) The influence of organisms on the composition of sea-water. In Hill, M. (ed.), The Sea, Vol. 2. Interscience, John Wiley & Sons, New York, pp. 26–77.
Saito, H. and Tsuda, A. (2000) Egg production and early development of the subarctic copepods Neocalanus cristatus, N. plumchrus, and N. flemingeri. Deep-Sea Res. I, 47, 2141–2158.
Schimel, D., Enting, I. G., Heimann, M., Wigley, T. M. L., Raynaud, D., Alves, D. and Siegenthaler, U. (1995) CO2 and the carbon cycle. In Houghton, J. T., Meira Filho, L. G., Bruce, J., Lee, H., Callander, B. A., Haites, E., Harris, N. and Maskell, K. (eds), Climate Change 1994: Radiative Forcing of Climate Change. Cambridge University Press, Cambridge, pp. 37–71.
Takahaski, T., Feely, R. A., Weiss, R. F., Wanninkhog, R. H., Shipman, D. W., Sutherland, S. C. and Takahashi, T. T. (1997) Global air–sea flux of CO2: An estimate based on measurements of sea–air pCO2 difference. Proc. Natl Acad. Sci. USA, 94, 8292–8299.
Taw, N. and Ritz, D. A. (1979) Influence of subantarctic and subtropical oceanic water on the zooplankton and hydrology of waters adjacent to the Derwent River Estuary, south-eastern Tasmania. Aust. J. Mar. Freshwater Res., 30, 179–202.
Tseitlin, V. B., Rudyakov, Yu. A. and Kitain, V. Ya. (1997) Zooplankton biomass distribution in the surface layer of the Pacific Ocean. Oceanology, 37, 75–82.
Vidal, J. and Whitledge, T. E. (1982) Rates of metabolism of planktonic crustaceans as related to body weight and temperature of habitat. J. Plankton Res., 4, 77–84.
Vinogradov, M. E., Musaeva, E. I., Michaailovsky, G. E. and Nikolaeva, G. G. (1988) Bathymetric distribution of mesoplankton biomass. In Vinogradov, M. E. and Flint, M. V. (eds), Pacific Subantarctic Ecosystems. Nauka, Moscow, pp. 178–187 (English translation available from NIWA, Box 14901, Wellington, New Zealand).
Voronina, N. M. (1975) [On the ecology and biogeography of plankton of the Southern Ocean.] Tr. Inst. Okeanogr., 103, 60–87.
Voronina, N. M., Kolosova, E. G. and Flint, M. V. (1988) Distribution and biology of mass species of mesoplankton. In Vinogradov, M. E. and Flint, M. V. (eds), Pacific Subantarctic Ecosystems. Nauka, Moscow, pp. 197–210 (English translation available from NIWA, Box 14901, Wellington, New Zealand).
Weibe, P. H. (1988) Functional regression equations for zooplankton displacement volume, wet weight, dry weight, and carbon: a correction. Fish. Bull., 86, 833–835.
Wanninkhof, R. (1992) Relationship between wind speed and gas exchange over the ocean. J. Geophys. Res., 97, 7373–7382.
Watson, A. J. (1997) Volcanic iron, CO2, ocean productivity and climate. Nature, 385, 587–588.[Medline]
Wong, C. S., Whitney, F. A., Crawford, D. W., Iseki, K., Matear, R. J., Johnson, W. K., Page, J. S. and Timothy, D. (1999) Seasonal and interannual variability in particle fluxes of carbon, nitrogen and silicon from time series of sediment traps at Ocean Station P, 1982–1993: relationship to changes in subarctic primary productivity. Deep-Sea Res. II, 46, 2735–2760.
Zhang, X. and Dam, H. G. (1997) Downward export of carbon by diel migrant mesozooplankton in the central equatorial Pacific. Deep-Sea Res. II, 44, 2191–2202.
Received on October 6, 2000
; accepted on April 10, 2001
CiteULike 
Connotea 
Del.icio.us What's this?
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||