COMMENT
Limnol.
Oceanogr., 38(6), 1993, 1328-1331
0 1993, by the American
Society of Limnology
and Oceanography,
Inc.
Flux feeding as a mechanism for zooplankton
implications for vertical particulate flux l
Food concentrations
within the euphotic
zone are frequently too low to support growth
of the filter-feeding organisms that consume
phytoplankton
and other forms of particulate
matter (e.g. Checkley 1980; Dagg 199 1; Durbin et al. 1983). How, then, are particle-consuming zooplankton living in subeuphotic zone
waters able to exist in their more impoverished
milieu? I suggest that it is not by filtering water
to strain the few particles available but rather
by intercepting settling particles.
The necessity to consider a feeding mode
different from filter feeding can be clearly seen
in the pteropods-zooplankton
known to consume detrital particles and small animals without filtering the water. Many pteropods feed
by building fragile mucous webs that are spherical or cone shaped, can be as large as 20 cm
across, and hang in the water above the animal
(Gilmer and Harbison 1986; Lalli and Gilmer
1989). A web collects small zooplankton, diatoms, and detritus. Eventually, a pteropod
eats its mucous web, consuming the organisms
and other materials that have collected on it.
Webs are able to collect food particles from
the surrounding water without having the rigidity to filter for the particles. How do they
do so?
Gilmer and Harbison (1986) noted that a
web collects copepods that swim into it. This
mechanism does not explain how such a large,
fragile structure as a relatively immobile mucous web collects algal cells. I suggest that the
webs collect particles falling on top of them
and that this is an important part of their func-
grazing and its
tion. The rate at which particles collect should
depend on their concentrations and fall velocities, i.e. their fluxes. In this sense, pteropods
should be thought of as flux feeders rather than
as filter feeders. Because large particles tend to
fall faster than small ones, a flux feeder should
feed preferentially on such larger particles as
fecal pellets and marine snow. (Note that this
is a simplification
of the analysis by Shimeta
and Jumars 199 1, which suggested that turbulent shear and diffusion would also cause
particles to impact the web.)
The impact of flux feeding by pteropods can
be estimated with a standard cross-sectional
formulation.
If F is the particle flux, P the
number concentration of pteropods at a given
depth z, and (T the projected area on a horizontal plane of an individual
pteropod web,
then the rate of change of the flux with depth
is given by
dF
- -aPF
zor
1 dF
-=
Fdz
-k
I Accepted: 2 March
1992.
M. Dagg, P. Jumars, and L. Madin provided useful suggestions.
This work was supported by ONR Contract NO00 14
87-K0005 and U.S. DOE Grant DE-FG05-85-ER6034
1.
(2)
where k = (TPis the vertical decrease rate. This
expression leads to
F = F, exp(-2)
(3)
where
z
k dz’
lx=
s
Acknowledgments
(1)
ZO
is the ratio of total cross section of mucous
web per unit area and z, is the initial depth.
For constant k, this reduces to
1328
F = F, exp [ - k(z - zo)].
(4)
Comment
1329
Table 1. Representative concentrations of pteropods of the genus Limacina. Values of k
diameter of the mucous web is 20 mm and the resulting value of u is 3 x 1O-4 m2. Note that
reported concentrations of L. retroversa as high as 13,600 mP3 in the upper 25 m of the water
dominantly juveniles ~0.5 mm. Several investigators also reported other pteropod species
increase the value of k.
Location
Judkins et al. 1980
Bathmann et al. 199 1
Snider 1975
Wells 1976
Wormuth 198 1
L.
L.
L.
L.
L.
retroversa
retroversa
injlata
infrata
infrata
New York Bight
Norwegian Sea
Gulf of Mexico
Barbados
North Atlantic
What are typical values for A, C, and k?
Measured pteropod abundances are extremely
variable with respect to time, space, sampling
gear, and investigator. For five cases where the
distribution of members of the common genus
Limacina has been measured, k ranged from
0.15 to 3 x lop5 m-l, with a median of 3 x
lop3 m-l (Table 1). Particle fluxes at the bottom of a 100-m layer with the above values
of k would range from 3 x 10m7 to 1.0, with
a median of 0.74, of those at the top.
Various workers have expressed the downward particulate flux estimated by sediment
traps as functions of depth (e.g. Betzer et al.
1984; Martin et al. 1987). Although these estimates suffer from various procedural problems (e.g. Silver and Gowing 199 l), they do
offer a way of comparing the decrease of particulate flux with the above estimates of the
pteropod effect. Martin et al. (1987) developed
a formula for the vertical flux at a depth z
relative to that at 100-m depth, Floe, where z
> 100 m:
Its derivative
dF
- = -8.58
dz
is
x 10-3F100
(6)
Hence,
k = ;$-
= -8.58
x 10-l
z-‘.
(7)
For z = 200 m, k = 4.3 x 10e3 m-l. This
value of k estimated from sediment trap data
is near the median of k values estimated from
Limacina abundances (Table 1).
P
(No. m-‘)
480
50
10
3
0.1
calculated assuming the
Bathmann et al. (199 1)
column, but these were
whose inclusion would
(m”- I)
1.51 x
1.57 x
3.14X
9.42 x
3.14x
10-I
10-2
10-J
1O-4
10-S
The development of this argument has emphasized pteropods feeding with mucous webs
because they are particularly dramatic examples of flux feeding. The problem of feeding in
an environment
with low concentrations
of
food exists, however, for any particle-consuming animal living below the euphotic zone. Dagg
(pers. comm.) has suggested that there are copepods living below the euphotic zone that
also flux feed. Silver et al. (1978) suggested that
marine snow particles could have a significant
role in slowing the descent of fecal pellets. Silver and Gowing (199 1) suggested a similar role
for the large larvacean houses found off Monterey Bay. They further suggested that settling
matter, which collected on marine snow or on
larvacean houses, would be available for microbial degradation or feeding by other zooplankton. Such interactions
should also be
considered flux feeding because their rates
would depend on particle fluxes rather than
concentrations even though both capturing and
consuming falling particles might involve two
or more groups of organisms.
A major distinction between flux and filter
feeding is that flux feeding is proportional to
particle fall velocity as well as concentration.
Because large particles tend to fall faster than
small ones, flux feeding would allow organisms
to subsist on the rare larger particles rather
than the more common small ones. As such,
it increases the importance of large aggregates
or fecal pellets as food sources.
Because the particle source is localized near
the surface, flux feeders could adopt different
strategies for capturing the flux. If Z is large,
the fraction of particles reaching the ocean bottom is small. For example, if Z = 4, then only
0.02 of the surface flux reaches the bottom. A
food-limited flux feeder would need to be near
1330
Comment
the surface to maximize its food intake. If it
feeds on fecal pellets of a vertically migrating
zooplankton, the flux feeder might migrate to
just underneath its food sources. If Z: is 1, then
0.37 of the flux reaches the bottom. In this
case, food capture by a flux feeder would be
fairly constant throughout the water column.
Uniform dispersion might help flux feeders
minimize losses to predation. To the extent
that the inverse relationship between k and z
shown in Eq. 7 is true, it could be caused by
a decrease in the abundance of animals with
depth.
The fact that animals whose numbers vary
could control the vertical particle flux implies
that the rate at which the vertical flux decreases
with depth should also vary spatially and seasonally. To the extent that flux feeders are important consumers of falling particles, there
should not be a standard relationship between
depth and decrease in particulate flux. In particular, there should be more activity in regions
where fluxes are high, possibly leading to greater remineralization
of falling particles near the
surface than in oligotrophic regions. Low concentrations of flux feeders early in the season
could explain how large fluxes of algal floes
reach the bottom of the North Atlantic after
the spring bloom (Billett et al. 1983; Thiel et
al. 1989; Turley and Lochte 1990).
Models incorporating global circulation and
biological processing of carbon have had problems demonstrating high enough carbon consumption in shallow regions to reproduce the
observed nutrient distributions found in shallow regions below the euphotic zone (Bacastow
and Maier-Reimer
1990, 199 1; Toggweiler
1988). As a result, production of dissolved organic matter, particularly in areas of high productivity, has been deemed essential to stop
particles from carrying nutrients too deep before they are recycled. These models have relied on the simple, unvarying curve fits derived
from sediment-trap
data (e.g. Martin et al.
19 8 7). Changes in animal concentrations would
change the depths of nutrient recycling and
could diminish the need to invoke high production rates of dissolved organic C, N, and P.
Taylor and Karl (199 1) have argued that
simple remineralization
by microbes attached
to falling particles is insufficient to explain observed vertical flux patterns and that something like consumption by organisms in the
water column is needed. This deduction is consistent with the ideas proposed here.
The role of flux feeders in controlling carbon
recycling below the euphotic zone emphasizes
the importance of groups of organisms, such
as larvaceans and pteropods, that are not usually included in quantitative studies of organic
carbon cycling. The calculations performed
here emphasized only two species. The effects
of all the organisms feeding in a similar way
surely are greater.
(Note: Although the work had been extensively discussed, the details reported by Najjar
et al. 1992 had not been published when this
manuscript was prepared. The invocation of
flux feeders may not explain problems with
that model, but flux feeding has a different
impact on material cycling that should be included in studies of the fate of organic matter
in the ocean.)
George A. Jackson
Department of Oceanography
Texas A&M University
College Station 77843
References
BACASTOW, R., AND E. MAIER-REIMER. 1990. Ocean-circulation and the carbon cycle. Clim. Dyn. 4: 95-125.
-,
AND p.
199 1. Dissolved organic carbon in
modeling oceanic new production.
Global Biogeothem. Cycles 5: 7 l-85.
BATHMANN, U. U., T. T. NOJI, AND B. VON BODIJNGEN.
199 1. Sedimentation of pteropods in the Norwegian
Sea in autumn. Deep-Sea Res. 38: 1341-1360.
BETZER, P. R., AND OTHERS. 1984. Primary productivity
and particle fluxes on a transect of the equator at
153”W in the Pacific Ocean. Deep-Sea Res. 31: l-l 1.
BILLET-T, D. S. M., R. S. LAMPIIT, A. L. RICE, AND R. F.
C. MANTOURA. 1983. Seasonal sedimentation
of
phytoplankton
in the deep sea. Nature 333: 67-69.
CHECKLEY, D. M. 1980. Food limitation of egg production by a marine, planktonic copepod in the sea off
southern California. Limnol. Oceanogr. 25: 99 l-998.
DACG, M. J. 199 1. Neocalanus plumchrus (Marukawa):
Life in the nutritionally-dilute
subarctic Pacific Ocean
and the phytoplankton-rich
Bering Sea, p. 2 17-225.
Bull Plankton Sot. Jpn. Spec. Vol.
DURBIN, E. G., A. G. DURBIN, T. J. SMAYDA, AND P. G.
VERITY.
1983. Food limitation of production by adult
Acartia tonsa in Narragansett Bay, Rhode Island.
Limnol. Oceanogr. 28: 1199-l 2 13.
GILMER, R. W., AND G. R. HARJSISON. 1986. Morphology
and field behavior of pteropod molluscs: Feeding
methods in the families Cavoliniidae,
Limacinidae,
and Peraclididae (Gastropoda: Thecosomata). Mar.
Biol. 91: 47-57.
JUDIUNS, D. C., C. D. WIRICK, AND W. E. ESALU. 1980.
1331
Comment
Composition,
abundance, and distribution
of zooplankton in the New York Bight, September 1974September 1975. Fish. Bull. 77: 669-683.
LALLI, C. W., AND R. W. GILMER. 1989. Pelagic snails:
The biology of holoplanktonic
gastropod molluscs.
Stanford.
MARTIN, J. H., G. A. KNAUER, D. M. KARL,, AND W. W.
BROENKOW. 1987. VERTEX: Carbon cycling in the
northeast Pacific. Deep-Sea Res. 34: 267-285.
NAJJAR, R. G., J. L. SARMIENTO, AND J. R. TOGGWEILER.
1992. Downward transport and fate of organic matter in the ocean: Simulations with a general circulation
model. Global Biogeochem. Cycles 6: 45-76.
SHIMETA, J., AND P. A. JUMARS. 1991. Physical mechanisms and rates of particle capture by suspensionfeeders. Oceanogr. Mar. Biol. Annu. Rev. 29: 19 l-
257.
SILVER, M. W., AND M. W. GOWING. 1991. The “particle” flux: Origins and biological components. Proc.
Oceanogr. 26: 75-l 13.
p,
A. L. SHANKS, AND J. D. TRENT. 1978. Marine
snow: Microplankton
habitat and source of smallscale patchiness in pelagic populations. Science 201:
371-373.
SNIDER, J. E. 1975. Quantitative
distribution of shelled
Lunnol.
Oceanogr.,
38(6),
1993, 1331-1332
of Limnology
0 1993,bythe AmericanSociety
and Oceanography,
pteropods in the Gulf of Mexico including related
sampling studies. Ph.D. thesis, Texas A&M Univ.
TAYLOR, G. T., AND D. M. KAFU. 199 1. Vertical fluxes
of biogenic particles and associated biota in the eastem North Pacific. Implications
for biogeochemical
cycling and productivity.
Global Biogeochem. Cycles
5: 289-303.
THIEL, H., AND OTHERS. 1989. Phytodetritus on the deepsea floor in a central oceanic region of the northeast
Atlantic. Biol. Oceanogr. 6: 203-239.
TOGGWEILER, J. R. 1988. Is the downward dissolved
organic matter flux important in carbon transport?,
p. 65-83. Zn W. H. Berger et al. [eds.], Productivity
of the ocean: Present and past. Wiley.
TURLEY, C. M., AND K. L~CHTE. 1990. Microbial
response to the input of fresh detritus to the deep-sea
bed. Palaeogeogr. Palaeoclimatol.
Palaeoecol. 89: 3-
23.
WELLS, F. E. 1976. Seasonal patterns of abundance
reproduction of euthecosomatous pteropods off
bados, West Indies. Veliger 18: 241-248.
WORMUTH, J. H. 198 1. Vertical distributions
and
migrations of Euthecosomata in the northwest
gasso Sea. Deep-Sea Res. 28: 1493-l 5 15.
and
Bardiel
Sar-
Inc.
Reply to the comment by Jackson
Recent simulations of the cycle of organic
matter in the ocean with general circulation
models suggest that most of the downward
transport is in a dissolved form (Najjar 1990;
Bacastow and Maier-Reimer
199 1; Najjar et
al. 1992). Particle remineralization
below the
euphotic zone in these models is treated in a
highly simplified form. Both the fraction of the
export production that is sinking particulate
matter and the remineralization
length scale
of this particulate matter are spatially invariant. In his comment concerning zooplankton
and their relationship to the particle flux below
the euphotic zone, Jackson (1993) suggests that
the assumption of a constant remineralization
length scale is important with regard to the
conclusions of these modeling studies. In particular, he suggests that a shorter remineralization length scale in regions of higher productivity (where animal populations are greater)
would improve simulation of the nutrient distribution.
We disagree. In one of our simulations where
all export production is in the form of sinking
particulate matter that is remineralized below
the euphotic zone with a length scale consistent
with sediment trap observations (Martin et al.
1987), we found that nutrients
become
“trapped” below the euphotic zone in regions
of shallow upwelling, such as the eastern equatorial regions of the Pacific and Atlantic Oceans.
This trapping is a positive feedback between
new production, remineralization,
and the upward flux of nutrients; it is discussed in detail
by Najjar et al. (1992). Nutrient trapping becomes more pronounced with a shorter length
scale for remineralization.
We see no evidence
for nutrient trapping in the real ocean, at least
to the degree found in this simulation, and
conclude that the new production of the equatorial upwelling zones cannot be leaving the
euphotic zone primarily as sinking particles
which are regenerated in the upper few hundred meters. Including dissolved organic matter in our model improves the simulation of
the nutrient distribution because it eliminates
nutrient trapping.
The remineralization
length scale used in