Comment
1375
NHa/NH$
ATMOSPHERE
LONG-LIVED
DISSOLVED
ORGANIC
NITROGEN
( HORIZONTAL
EXUDATES
NH;,
ADVECTION
N2
)
EXUDATES
urea-N
T
REGENERATED
PRODUCTION
,NOi
T
T
+ HETEROTROPHS
4
+
NEW
T
PRODUCTION
Fig. 1. Export of dissolved and particulate organic matter from the euphotic zone and sourcesof allochthonous
inorganic nitrogen for primary production; in the euphotic zone, relationships between new and regenerated
production, pathways of nitrogen recycling, and advection of long-lived dissolved organic nitrogen. By contrast,
Eppley and Peterson’s (1979) scheme of new and regenerated production assumed that nitrogen fixation and
atmospheric transport of nitrate were much smaller than the other sources of allochthonous nitrogen (i.e. nitrate,
from vertical eddy diffusion and upwelling) and did not include atmospheric transport of ammonia or fluxes of
long-lived DON.
should be added to phytoplankton production since bacteria may often act more as a
sink than as a source of N (e.g. Caron et al.
1988).
New and regenerated production refers to
the origin of nutrients used by primary pro-
ducers, while export and recycled production concerns pathways in the food web. A
recent conceptual model of production export in oceans (Legendre and Le Fevre 1989;
Fig. 2) shows that there is no direct equivalence between the two sets of concepts. The
Comment
1376
A
1
LARGE
PHYTOPLANKTON
ULTRAPLANKTON
SINKING
( MICROPHAGY 1
/
RECYCLED/TOTAL
PRODUCTION
-w
Fig. 2. Model of export production (downward arrows) in oceans (after Legendre and Le Fevre 989).
each bifurcation, part of the primary production may be channeled into export pathways, which does not preclude
coexistence with recycling pathways. According to Legendre and Le FCvre (1989), hydrodynamic conditions
control the five bifurcations.
model explains why the ratio of recycled to
total production increases as one goes from
production of large phytoplankters (mainly
PN) with direct export of intact cells and
some recycling (exudation of dissolved organic matter; DOM), to grazing of large cells
by herbivores and associated excretion of
DOM, to grazing of detrital biogenic material by microphagous feeders (and excretion), to sinking of marine snow and associated recycling of POM, and finally to the
microbial food loop in which most of the
production (essentially PR) is recycled but
from which direct export is nevertheless
possible. Export and recycling thus occur
simultaneously in all compartments of the
pelagic food web, so that export or recycling
cannot specifically be associated with any
particular type of phytoplankton production (i.e. new or regenerated). The equivalence proposed by Eppley and Peterson
(1979) between new phytoplankton production and POM export results from mass
balance between upward and downward
fluxes. In order for masses to be balanced,
steady state must be assumed on appropriate spatial and temporal scales. It is generally recognized that relevant time scales
exceed those at which measurements are
often conducted at sea (a few hours), so that
new production would be equivalent to export production only if measurements are
time averaged over an appropriate period
(a year in areas where seasonal variations
are significant and shorter periods in central
oceanic gyres; e.g. Eppley 1989).
The approach of Eppley and Peterson
(1979) was based on the assumption that
organic matter exported to the deep ocean
is mainly particulate (i.e. intact phytoplankton cells, fecal pellets, marine snow), and it
implies that all the processes involved in
the production and export of biogenic material occur on roughly similar time scales.
When nitrogenous nutrients are used as
tracers, this approach also assumes negligible nitrogen fixation in the euphotic zone.
These assumptions were reasonable at the
Comment
time when Eppley and Peterson wrote their
paper, and they may well still be so. A number of recent oceanographic discoveries,
however, may lead us to question the validity of the present approach because they
suggest that uptake of 15N-labeled compounds may not account for the overall nitrogen budget of phytoplankton production
and that the spatio-temporal scalesat which
steady state would be achieved may significantly differ for particulate and dissolved
export. These discoveries concern nitrogen
fixation in open oceanic waters, the atmospheric transport of nitrate and ammonia,
and the concentrations of long-lived dissolved organic nitrogen in oceans.
Denitrification and nitrogen fixation are
two complementary processesby which oxidized forms of combined nitrogen (nitrate,
nitrite, and nitrous oxide) are reduced to
free nitrogen gas (denitrification) and combined nitrogen is produced from free nitrogen gas (nitrogen fixation). It is generally
considered that denitrification occurs only
under anoxic or low-oxygen conditions (see
Codispoti 1989), which would also be the
casefor nitrogen fixation (e.g. Paerl and Prufert 1987). In the open ocean, sites favorable
for denitrification would be the oxygen-deficient portions of the water column below
the euphotic zone (e.g. Ward and Zafiriou
1988) while those favorable for nitrogen
fixation would be reducing microzones
within the well-oxygenated euphotic zone
(Codispoti 1989). Denitrification and nitrogen fixation may be approximately balanced
on a time scale of about 10’ yr, but imbalances in which denitrification may exceed
nitrogen fixation could reduce export production by 20-30% for periods of several
thousand years (Codispoti 1989).
Since denitrification occurs at depth, the
reduced upwards flux of nitrate is reflected
by decreased new production. Thus, measurements of new production in the euphotic zone would adequately account for
denitrification. This balance does not hold,
however, for nitrogen fixation since uptake
of 15N03- does not reflect new production
derived from free nitrogen gas. If nitrogen
fixation in the open ocean were important,
usual measurements would underestimate
1377
new production (Fig. 1). According to Lewis
et al. (1986), the rate of nitrogen fixation is
currently thought to be several orders of
magnitude less than the rate of supply of
nitrate by upward turbulent transport, but
nitrogen fixation by cyanobacteria and the
difficulties of making the necessary measurements at sea leave open the possibility
that this rate may be higher than presently
thought. Higher rates of nitrogen fixation in
open oceanic waters would require larger
numbers of reducing microzones in surface
waters, and examples of such microzones
have recently been described in the literature. They include oxygen-depleted microzones associated with surfaces of organic or
inorganic aggregates(e.g. Paerl and Carlton
1988), internal microzones within aggregates (bundles) of the filamentous nitrogenfixing cyanobacterium Oscillatoria spp.
(Paerl and Bebout 1988), and perhaps food
vacuoles of phagotrophic phototrophs (photosynthetic protista) in which bacteria may
be found (e.g. Boraas et al. 1988). The importance of reducing microzones for nitrogen fixation is stressed by differences measured in blooms of Oscillatoria off North
Carolina (Paerl and Bebout 1988), where
nitrogen fixation rates vary from about 0.1
nmol (mg Chl a)-’ h-l for bundles of ~30
filaments to 0.7 for bundles of > 75 filaments (acetylene reduction assay, assuming
a ratio of 3 mol of acetylene reduced to 1
mol of dinitrogen fixed).
If reducing microzones in surface waters
were really more prevalent than previously
thought, or if nitrogen fixation could occur
under high oxygen concentrations (as recently shown by Ohki and Fujita 1988), new
production by nitrogen-fixing organisms
might have been underestimated in some
environments. An additional aspect is that
nitrogen fixation may occur preferentially
at night (e.g. Mitsui et al. 1986, for Ajvzechococcus), whereas most field incubations
are conducted during the day. Magnitudes
of these phenomena have not been quantified, but recent evidence suggests that nitrogen fixation may be significant, especially
in nitrogen-depleted tropical and subtropical waters as previously pointed out by
Dugdale and Goering ( 1967). If so, biolog-
1378
Comment
ical oceanographers would be confronted
with the task of including in their routine
field measurements new production derived
from nitrogen fixation.
Several papers dealing with new production have mentioned the atmosphere (Fig.
1) as a potential source of nutrients (e.g.
Dugdale and Goering 1967; Eppley and Peterson 1979; Lewis et al. 1986). For nearneutral and acidic rainfall, respectively, Paerl
( 198 5) has reported concentrations off North
Carolina of 16 and 33 mmol (NOz- + N03-)
rnp3 and 18 and 17 mmol NH4+ mp3. Off
the southern Norwegian coast, values for
total inorganic-N nutrients (NO,- + N03+ NH,+) in precipitation are -70 mmol
me3 (Dahl et al. 1987). For ammonia, these
values are one order of magnitude higher
than those reported by Quinn et al. (1988)
for the northeast Pacific Ocean (about 1
mmol mm3).If we assume 2 cm of rainfall
every second day and use the values of Paerl
( 1985), atmospheric fluxes of inorganic-N
nutrients into the North Atlantic Ocean
would be 0.3-0.4 mmol rnT2 d-l, similar to
the average measured flux of 0.3 mmol me2
d-l (- 1.5 g N m-2 yr-l; Dahl et al. 1987)
from precipitation off the Norwegian coast.
Such values are 2-3 times higher than new
production calculated from the upward diffusion of nitrate in the oligotrophic eastern
Atlantic (0.14 mmol N rnp2d-l; Lewis et al.
1986), which means that calculations based
on the upward transport of nitrate (e.g. Lewis et al. 1986) could underestimate new production by a factor of three or more, especially in areas subject to industrially
contaminated or acidic rainfall (e.g. the
North Atlantic Ocean).
A peculiar problem with ammonia is that
atmospheric inputs would contribute to increase production exported to deep water
while decreasing the f-ratio as measured
from the uptake of 15N-labeled compounds
(uptake of 15NHq+is ascribed entirely to regenerated production). This effect may become important if fluxes of ammonia between atmosphere and ocean are large
relative to other allochthonous nitrogen
fluxes. In oligotrophic subtropical waters for
example (Eppley and Peterson 1979), P,may
be as low as 0.9 mmol N me2 d-l (with a
C : N molar ratio of 6.4 : l), with an f-ratio
of 6% (as measured from the uptake of 15Nlabeled nitrate and ammonia). It follows that
PN M 0.05 and PR x 0.85 mmol N rnp2 d-l;
assuming that 0.15 mmol N m-2 d-l of PR
is due to NH,+ in rainfall and should therefore rightly be assigned to PN, the true&ratio
corresponding to actual production export
would be three times higher than that measured from 15N uptake.
Sugimura and Suzuki ( 1988) have reported concentrations of dissolved organic
carbon (DOC) and dissolved organic nitrogen (DON) about four times higher in surface waters and two times higher in deep
waters than previously thought and have
also shown large vertical gradients of DOC
and DON into deep waters. In the North
Pacific Ocean, they found 180-490 mmol
mm3DOC and 30-45 mmol m-3 DON in
the upper 300 m and 35-85 mmol m-3 DOC
and 4-l 5 mmol m-3 DON from 400 to 4,100
m. If these new measurements prove correct, it may be inferred from the vertical
DON gradient that the downward flux of
DON balances much of the upward flux of
nitrate (Toggweiler 1989) -contrary to the
assumption that organic matter exported to
the deep ocean is mainly particulate (e.g.
Eppley and Peterson 1979). Toggweiler
( 1989) concluded from modeling studies that
solely balancing the upward flux of nutrients
by a sinking flux of organic particles, mineralized according to the vertical scaling
demonstrated by sediment traps, would radically alter nutrient distributions in the ocean
and particle production would be many
times higher than is currently measured, that
downward fluxes of DOM on a global scale
may be of equal importance to those of
POM, and that about half the new production may find its way into a long-lived DOM
pool (breakdown rate of l/200 yr-l) advected with the water. He hypothesized that
the long-lived organic compounds may be
formed by condensation reactions between
carbon-rich phytoplankton exudates and
nitrogen-rich bacterial enzymes. Because
concentrations of DOM are highest in low
and midlatitude surface waters, Toggweiler
suggested that these waters are the sources
of most of the long-lived DOM and that the
Comment
actual pathway by which it reaches the interior of the ocean is likely to include a detour through higher latitudes.
This view has several consequences concerning the export of organic matter to the
deep ocean (Fig. 1). First, the equation “new
production = POM export” (Eppley and Peterson 1979) should be modified for “new
production = POM export + DOM export,” where dissolved export may be of the
same order of magnitude as particulate export. There is no conceptual problem with
changing the equation, especially when the
aim is to quantify global fluxes of organic
matter (i.e. both POM and DOM). It would
be extremely difficult to test this new definition against field data, however, since only
POM export can be measured directly at sea
(sediment traps). On the other hand, a major problem concerning the new definition
would arise from the different temporal and
spatial scales of POM and DOM export.
Sinking of POM (as intact cells, fecal pellets,
or marine snow) or export through vertically migrating organisms (Longhurst and
Harrison 1988) occurs locally and on time
scales of days to months after primary production has taken place (scales of about 10
km and 1Om2-10-l yr). By contrast, transport
of DOM from surface to deep waters would
involve basin-scale circulation (1O4 km;
Toggweiler 1989), which extends over decades and centuries. The two components
of organic matter export may therefore occur on scalesfour orders of magnitude apart;
in other words, the downward fluxes of POM
and DOM would be separated in space by
thousands of kilometers and in time by decades or centuries. This disparity of scale
means that the equation “new production
= POM export + DOM export” would be
true only at the basin scale over long periods, which in turn requires long-term
steady state. One wonders whether such an
assumption is reasonable for the past and if
it is tenable in the present context of global
change. A possible approach allowing the
original definition of Eppley and Peterson
(1979) might be to quantify the proportion
of new production that finds its way into
the long-lived DOM pool and to subtract it
from PNto get a “POM-exportable new pro-
1379
duction”; whether this method is practical
remains to be explored.
If the new measurements of DOM are
correct and their implications for export of
organic matter have been properly assessed,
data on new production may overestimate
POM export by a factor of about two. Such
an error is well within the confidence limits
of present-day measurements (e.g. Lewis et
al. 1986) so that it would easily remain undetected with a direct approach (e.g. comparing 15N03- uptake to sediment trap data).
A factor of two, however, could prove important when estimating global fluxes in a
rapidly changing environment.
In the current literature, there are serious
discrepancies between measurements of PN
using the above approaches and those derived from changes in concentrations of
chemical tracers observed in water masses
isolated from the sea surface. In the oligotrophic eastern Atlantic, for example, Lewis
et al. (1986) reported PN= 0.81 (20.2, 95%
C.I.) mmol N m-2 d-l as measured by incorporation of 15N-labeled nitrate and PN =
0.14 (0.0 l-0.89) mmol N m-2 d-l as estimated from the upward diffusion of nitrate.
Corresponding rates calculated from changes
of oxygen concentrations in the euphotic
zone (Jenkins and Goldman 1985) are 2.5
mmol N me2 d-l (Lewis et al. 1986). Even
without invoking higher rates of nitrate diffusion (e.g. Jenkins 1988; 1.5 mmol N rnp2
d-l), these discrepancies would be resolved
if the various additional sources of nitrogen
discussed here were truly significant to new
plankton production (i.e. PNhigher by a factor of about two or three).
Finally, even if new production could be
measured adequately in the euphotic zone,
the relationship between new and export
production in the deep ocean would remain
very problematical since vertical distributions of DOM suggest that exports of POM
and DOM might be taking place on time
and space scales that are respectively
hundreds of years and thousands of kilometers apart. Further, there is no evidence
that over comparable scales steady state is
achieved for the various fluxes of inorganic
nitrogen in the euphotic zone (upward diffusion of nitrate, nitrogen fixation, atmo-
1380
Comment
spheric transport of nitrate and ammonia).
On the contrary, the concept of global change
(Joint Global Ocean Flux Study; Brewer et
al. 1986) denies steadiness on these scales.
Louis Legendre
Michel Gosselin
Departement de biologie
Universite Lava1
Quebec, Quebec Gl K 7P4
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Erratum
The large narcomedusan discussed in the paper by J. J. Childress et al. in the July issue
(Vol. 34, No. 5, p. 913-930) is not a Solmaris species as indicated. Based on its size,
depth distribution, number of marginal tentacles, and presence of perradial stomach
pouches, it is a species of Solmissus.