Vertical Migration of
Zooplankton: a Bi-phasic Feeding Strategy that Enhances New Production?
Diel vertical migration in marine zooplankton may be a bi-phasic feeding
strategy involving the alternate exploitation of particulate and dissolved
organic material. Active uptake of dissolved material may be pressure sensitive
and occur to a significant extent at greater depths. In diving crustaceans this
function may be uniquely optimized as the descent of the rigid exoskeleton
induces a hydrostatic pressure gradient across the integument. It is generally
believed that crustaceans have no significant ability to absorb dissolved
organic material directly, but studies have not included normalization of
hydrostatic pressure. Anatomical and behavioral evidence support the hypothesis
that ammonia excretion by zooplankton occurs largely in surface waters, thereby
potentially providing a biological vector for the stimulation of new production.
An accurate model of the feeding ecology of zooplankton is critical to
understanding the marine nutrient cycle, but explanations for the extensive diel
vertical migration of zooplankton have failed to completely account for the
observed behavior (1, 2, 3, 4, 5). Descent through the water column as a
strategy to optimize dissolved organic material (DOM) uptake based on pressure
dynamics is an idea that has not been explored, and the hypothesis that
crustaceans have a significant capacity for direct DOM uptake appears to have
been rejected prematurely.
Zooplankton typically descend hundreds of meters at dawn and rise toward the
surface at dusk. Such a prominent behavior feature, involving a significant
energy expenditure (6), must confer an adaptive advantage to the organism. A
simple model of "hunger" has been suggested as the trigger for upward migration
(7), since feeding on particulate material, including phytoplankton, occurs near
the surface. "Satiation," however, seems less compelling as the trigger for the
active descent of animals to extreme depths. And the "hunger" hypothesis fails
to explain some observations, such as a downward migration in response to a
shortage of particulate food at the surface (7).
It is suggested here that "hunger" may also be the trigger for the downward
migration or ‘diving’ behavior in zooplankton, and that this hunger may be
satisfied by the direct uptake of DOM during descent and the time spent at
depth. If a feeding advantage for zooplankton exists in deeper water, it is more
likely related to dissolved, than to particulate organic material (POM), since
the availability of POM decreases with depth while the DOM concentration remains
relatively constant (8). DOM availability to organisms adapted to exploit a
gradient in hydrostatic pressure, however, might increase significantly with
increasing depth and pressure.
Effects of Hydrostatic Pressure on Crustaceans
The metabolic rate (oxygen uptake) of vertically migrating crustaceans has
been measured under elevated hydrostatic pressure, and no great pressure effect
has been detected (9). Therefore it has been considered that metabolic processes
measured at 1 atmosphere can reasonably be extrapolated to the depths normally
occupied by zooplankton (10). No evidence exists, however, that a similar
extrapolation can be made from studies of DOM uptake conducted at atmospheric
Along with temperature, salinity and pH (11), hydrostatic pressure is an
environmental variable with the potential to modify characteristics of living
membranes such as permeability and the function of active transport mechanisms
(11, 12). Behavioral responses to small changes in hydrostatic pressure have
been demonstrated in a variety of marine invertebrate species, including
crustaceans (12, 13), and it has been suggested that the physiological mechanism
mediating the behavioral responses might be pressure-induced alterations in
these functional properties of living membranes (12). Pressure-induced
physiological changes might reasonably be expected to alter membrane functions
involved in nutrient uptake as well. Since zooplankton may experience diel
pressure changes of 20 atm. or more, DOM uptake capabilities at depth may vary
significantly from those measured at atmospheric pressure.
Beyond the potential alteration in DOM uptake capacity that may occur with
depth, diving crustaceans may have the potential to develop a pressure gradient
across the integument as they descend. This dynamic may also affect the
efficiency of DOM uptake.
Internal Pressure Equalization: Potential Relevance to DOM Uptake
Although the compressibility of seawater is very low, the rigidity of the
exoskeleton is such that crustaceans are significantly less compressible than
seawater (12). Rising external hydrostatic pressure on descent, if unaccompanied
by compression of the exoskeleton, will induce a relatively lower internal
pressure, which the animal will most easily be able to equalize by the ingestion
of water. Although the volulme of water ingested for this purpose will be very
small, crustaceans appear to have the ability to actively control the degree of
internal pressure equalization by regulating the movement of water into the
digestive tract. (Small crustaceans have been observed to take water in through
both mouth and anus (14).) An optimal pressure gradient could therefore
conceivably be maintained across the crustacean integument during diving. Such a
pressure gradient, occurring on even a very small scale, may have a significant
effect on membrane transport functions of the softer regions of the exterior
(the dermal glands, and possibly also the membranes involved in gas exchange).
Chapman (1981) demonstrated direct DOM uptake at atmospheric pressure through
the dermal glands in a marine copepod, and concluded that "the presence of an
exoskeleton, although it may restrict uptake to specific sites, does not
necessarily restrict DOM uptake" (15). A rigid exoskeleton may prove to be
advantageous if its rigidity allows the enhancement of DOM uptake by the
induction of a slight pressure gradient across the integument during descent. An
ability to exploit the pressure gradient in the water column in this manner may
be an unrecognized adaptive feature of the hard exoskeleton of crustaceans.
The compressibility of water increases as temperature is lowered, therefore
exploitation of the compressibility differential between water and crustacean
may be enhanced at the lower temperatures associated with deeper water.
Zooplankton may also find an advantageous decline in viscosity of water at
depth, if conditions are encountered where the viscosity increase induced by
lowered temperature is outweighed by the viscosity decrease associated with
increasing pressure. (This is an anomalous property of water at ocean
temperatures (16).) Subtle physical properties of water may therefore be used to
greater advantage in DOM uptake in deeper water. These factors may come into
play and help explain the extreme depths to which these tiny organisms descend,
or membrane transport capacity may simply continue to increase with ambient
Pressure Equalization during Feeding: Potential implications for N-cycling
During ascent, the compressibility differential will induce a reverse
pressure gradient across the integument. Although it appears unlikely due to the
very small volume involved, if the animal becomes stressed by rising internal
pressure from this source, equalization will easily be accomplished by the
expulsion of space-occupying organ contents. Besides water and solids ingested
and retained in the gut, crustaceans can release controlled amounts of liquid
metabolic waste to equalize internal pressure. The internal anatomy of
crustaceans includes paired bladders into which nitrogenous metabolic waste is
channelled and significant volumes can be retained (14). The existence of these
bladders implies that excretion of the waste product to the environment is
controlled and intermittent in nature, rather than occurring continuously as it
is produced by metabolic processes, and experimental observations confirm this
(14). It is hypothesized that the discharge of bladder contents is delayed
during ascent, in part due to positive buoyancy offered by the major nitrogenous
waste product, ammonia. Ammonium has been observed to be used for flotation by
other marine organisms (17). Retaining ammonia in the bladders during ascent
would therefore be energetically advantageous, as would be discharging this
waste prior to descent.
In a study reported by Norfolk (1978), internal hydrostatic pressure in the
crab, Carcinus maenas, increased in response to the osmotic effect of a
transfer from 100% to 50% seawater. Several times, as the pressure increased,
sharp decreases in internal hydrostatic pressure were noted to occur, which were
associated with the release of urine from the bladders (14). The pattern of
urine release in response to steadily rising internal pressure was intermittent,
and a degree of internal pressure elevation was tolerated before the release was
triggered. Release of bladder contents by ascending zooplankton is therefore
likely to be triggered primarily by rising internal pressure associated with the
oral ingestion of POM.
In contrast, the pressure dynamics during descent after cessation of oral
feeding appear most likely to inhibit discharge of bladder contents. And if, as
argued above, urine release is also delayed during the initial phase of ascent,
the excretion of ammonia will be concentrated in areas relatively closer to the
surface, where upward migrating zooplankton resume oral feeding. The suggested
spatial pattern of waste elimination offers the ecological benefit of
stimulating phytoplankton productivity by the net delivery of nitrogen to the
Research on DOM Uptake by Crustaceans
In recent decades very little scientific research has focused on the
question of direct DOM uptake by marine crustaceans. Early in the twentieth
century, however, this was a topic of great interest (19). Most notably, the
hypothesis was described by August Pütter who, in 1909, concluded that DOM must
be the major energy source for marine organisms, since the ocean did not appear
to contain enough particulate food to meet their needs (19, 20). The quantity of
organic material in the DOM pool has been consistently estimated to be
approximately an order of magnitude greater than that contained in POM (8).
While the issue stimulated considerable debate initially, the technology did not
exist to directly test Pütter’s hypothesis until later in the century. In 1961,
Stephens and Schinske demonstrated the general ability of marine invertebrates
to remove glycine from solution in seawater (21). The single notable exception
in their study were the Arthropods; six species were tested and all failed to
remove measurable amounts of glycine from solution. In 1966, however, McWhinnie
and Johannek briefly reported apparently contradictory evidence, that Antarctic
euphausiids were capable of direct uptake of acetate and glucose from seawater
(22). Subsequently, Anderson and Stephens demonstrated in 1969 that an apparent
ability to accumulate labelled glycine from seawater by four small crustacean
species, was an artifact only of direct uptake of DOM by microorganisms
colonizing their exoskeletons (22). Anderson and Stephens (1969) acknowledged
that the limitations of their study included the testing of only a single
dissolved organic compound, and also the lack of testing on any arthropod
belonging to the deepwater zooplankton (22). Nevertheless, it appears that,
based on these few studies, it subsequently became widely accepted and reported
as "a general rule" that crustaceans lack the ability to uptake DOM directly
from seawater (1, 3, 10, 11, 15, 19, 23, 24). It was assumed that the rigid and
relatively impermeable exoskeleton was the primary reason that crustaceans
lacked this capacity (3, 11, 22).
It is a further important limitation of the studies of Stephens and Schinske,
and Anderson and Stephens, that their experiments were conducted in very small
volumes of water (50-1000ml) (21, 22). The crustaceans tested were consequently
unable to migrate along any significant pressure gradient, as most zooplankton
do in their natural environment. This factor, which may potentially affect their
ability to uptake DOM, was not considered in these early studies.
A very few studies conducted since the late 1960s have suggested that direct DOM
uptake does play a role in the nutrition of marine crustaceans (25). However,
although the topic has been considered a "controversial" one (25), research
interest has apparently waned. In the last 2 decades there seems to have been no
significant published additions to this limited body of knowledge. Recent
comprehensive reviews on calanoid copepods and general zooplankton biology have
discussed POM ingestion at length while dismissing the potential for DOM uptake
by these marine crustaceans as trivial (1, 10). Citations indicate that
justification for this position still appears to be largely based on the work of
Anderson and Stephens (1969).
In the most recent experimental study that I am aware of (also conducted at
atmospheric pressure, in 500 ml of water), Chapman (1981) used autoradiographic
studies to demonstrate the direct uptake of low concentrations of dissolved
glucose from seawater by the marine copepod, Neocalanus plumchrus (15).
The anatomical regions of uptake were shown to be the midgut gland and the
dermal glands. Transport of glucose through the circulatory system and
incorporation into somatic tissue were also demonstrated. Dermal glands are
common to all crustaceans, but their function remains poorly understood (1, 15).
They are, however, small areas where soft tissue extends through pores which
penetrate the rigid exoskeleton. Mauchline (1998) discounted the potential
significance of Chapman’s finding based on the observation that the anatomical
regions involved in DOM uptake were areas "with thin or no cuticle, forming a
small region of the body surface, (therefore) little nutritional advantage would
be expected" (1). This may be inadequate grounds to draw this conclusion,
however, if those small areas are specially adapted for DOM uptake under the
fluctuating hydrostatic pressure conditions encountered in nature.
Recent investigations into the direct DOM uptake capabilities of marine
invertebrates have focused exclusively on the "soft-bodied" species, and highly
efficient uptake abilities have been demonstrated (11, 23, 26, 27). In contrast
to crustaceans, some soft bodied invertebrate species seem able to absorb DOM
directly through virtually the entire integument (11, 23). In bivalves, the gill
is an important site of DOM uptake as well as gas exchange (26).
Supportive Findings in Zooplankton Research
Difficulties commonly encountered in working with zooplankton may be rooted
in a nutritional deprivation imposed when diving animals are held in the
relatively shallow, low pressure tanks used in laboratory experiments. Even with
the addition of concentrations of particulate food far greater than those
occurring in nature, zooplankton have been unusually difficult animals to
maintain in laboratories. Similar difficulties are encountered in rearing the
young of benthic crustaceans (which also migrate vertically during the
planktonic stages), in the laboratory (3). A common observation is that the
metabolic rates of zooplankton are initially relatively high immediately after
capture, but that rates decrease markedly in the following hours and days. This
pattern was initially believed to be due to physical trauma, or "capture
stress," but Ikeda and Skjoldal (1980) demonstrated that the pattern of
declining metabolism post-capture is an effect of the onset of starvation (18).
In incubations in natural seawater, it has been noted that one common "bottle
effect" is a decline in the growth rate of phytoplankton, and the procedure used
to counteract this problem is the addition of ammonia to the incubation (10).
These observations suggest that a nutrient impoverishment exists in the usual
experimental set-ups in which small vertically migrating crustaceans are fed
exclusively on POM at low hydrostatic pressure. Also suggested is that the
stimulation of phytoplankton growth in nature involves the frequent injection of
a nitrogenous fertilizer (possibly ammonia) into the surface water.
Low natural availability of POM in the ocean, and the difficulty in providing
adequate nutrition to zooplankton via POM alone in the laboratory, seem
inconsistent with the common finding of empty guts in a high proportion of
apparently healthy, freshly captured organisms (20, 28). Observations of deep
living copepod species have at times included seemingly unlikely
generalizations, such as "adult males do not feed" (28). Mature zooplankton at
higher latitudes descend to deeper water for months during the winter season.
While, as is generally believed, they may maintain themselves largely on energy
stores accumulated during the months of extensive migration and active oral
feeding, these organisms may also continue to absorb DOM directly during this
time. They may continue to undergo lesser degrees of vertical migration,
confining themselves to the deeper water layers during the months of low
phytoplankton productivity, and rely more heavily on DOM-acquired nutrients
during these times. In 1916, Esterly reported his observations of one abundant
pelagic copepod, Eucalanus elongatus, in which "most specimens (were)
devoid of any intestinal contents," and the small bit of fecal material
occasionally seen "never (contained) the recognizable remains of any ingested
organism" (20). Might some species be more heavily oriented toward the
exploitation of DOM, and might the more important function of the digestive
tract in crustaceans sometimes be its utility in regulating the hydrostatic
pressure gradient across the integument as the organism migrates vertically? As
noted by Chapman (1981), the fact that any capacity for direct DOM uptake has
been demonstrated in a copepod that "does not appear to feed during the last 7
months of its life cycle" (15), strongly suggests that further research into
this question is warranted.
Bi-phasic feeding strategies may be a common trait of many aquatic
invertebrates. Research into the nutritional requirements of marine invertebrate
larvae has led to the conclusion that the optimum balance of nutrients for these
organisms is provided by a "bi-phasic diet (algae and DOM)" (3). A diel bi-phasic
feeding strategy (benthic and pelagic) has recently been described by Wilhelm et
al (1999) in a vertically migrating freshwater copepod (29). Interestingly,
these authors concluded that the behavior pattern of this copepod causes a net
regeneration of "new" phosphorus, the limiting nutrient in the lake system, into
the pelagic zone from the sediment, thus enhancing primary production. This
echoes the ecological role suggested here for vertically migrating marine
zooplankton, that of augmenting marine primary production by the physical
transport of "new" nitrogen from deeper water to the photic zone.
Current understanding of the marine nutrient cycle holds that DOM uptake plays
an important role in zooplankton nutrition, but only via the microbial loop or
other physical or chemical processes that convert DOM into POM (e.g. 24, 30).
Studies of planktonic marine crustacean nutrition today are focused exclusively
on the ingestion of POM (1, 10). The enhancement of phytoplankton growth by
ammonia excretion by zooplankton has long been considered to be significant,
although it has been viewed only as the "regeneration" of nutrients that were
originally obtained by grazing in the euphotic zone (e.g. 8). The acquisition of
organic material and energy from lower parts of the water column and the active
upward transport of nitrogen by zooplankton has not been considered. If this
dynamic occurs, then part of the ammonia excreted by zooplankton in surface
waters results in the stimulation of "new" rather than "regenerated" production.
Therefore, this question has major implications for our understanding of the
global carbon cycle as well as the marine nutrient cycle, and should become a
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