13.alcaraz. QXr+ - ICM

SCI. MAR., 61 (Supl. 1): 177-195
SCIENTIA MARINA
1997
LECTURES ON PLANKTON AND TURBULENCE, C. MARRASÉ, E. SAIZ and J.M. REDONDO (eds.)
Copepods under turbulence: grazing, behavior
and metabolic rates*
MIGUEL ALCARAZ
Institut de Ciències del Mar, CSIC, P. Joan de Borbó S/N, 08039 Barcelona, Spain
SUMMARY: This review focuses on the effects of small-scale turbulence on the rate processes of copepods, an important
group of planktonic animals, and on their consequences for the dynamics of pelagic ecosystems. Turbulent water motion
enhances the encounter rates between planktonic organisms and their food, changing the perception of the food environment
for copepods and other planktonic animals. As a consequence, their feeding behaviour is affected, and the grazing rates significantly increased. Direct effects of small-scale turbulence for planktonic copepods also include the enhancement of metabolic energy expenditure, excretion rates, growth, and development rates. Through complex cumulative processes of the
changes on individual rate-processes, the structural and functional properties of planktonic ecosystems are modified, with
important consequences for the ultimate fate of biogenic carbon in aquatic systems.
Key words: Turbulence, copepods, rate processes, plankton ecosystems.
INTRODUCTION
Water bodies of any size are basically turbulent
environments. In them, mechanical energy, driven
mainly by solar heat and wind (and in large water
bodies earth rotation), induces water movements
that resolve into swirls of decreasing size. The turbulent kinetic energy associated with the turbulent
eddies cascades from the larger eddies to the smaller, until dissipating into molecular viscosity (Ozmidov 1965).
Aquatic environments support a community of
organisms, the plankton, very diverse from the taxonomic and life-style points of view. Nevertheless,
they all share the common characteristic of living
suspended in a three-dimensional space, at the
*Received July 11, 1996. Accepted September 12, 1996.
mercy of water displacements, and without any relation to solid surfaces. Planktonic organisms cover a
broad size spectrum (Fig. 1), from the sub-micrometer range to hundreds of centimeters, and occupy
different trophic positions, from primary producers
to first- and second order carnivores, detritivores
and microheterotrophs.
The almost unique source of matter and energy
for the successive trophic levels in planktonic systems is provided by microscopic autotrophs. They
consist of protists and unicellular algae (phytoplankton) which inhabit the upper water layers, where
light conditions allow photosynthetic activity. The
concentration of primary producers is in general
very low (i.e., from 0.1 to 10 ppm by volume), and
their size-range covers about 3 orders of magnitude
(see Fig. 1).
Amongst the consumers, heterotrophic unicellular organisms and metazoans (zooplankton) are repCOPEPODS UNDER TURBULENCE 177
FIG. 1. – The categories in which plankton is divided according to size classes, and the corresponding functional groups, from viruses to large planktonic metazoan. The different functional
groups overlap into different plankton-size categories, which are somewhat artificial and in part
derived from the mesh-sizes used to sample them (redrawn from Sieburt et al., 1978).
resented by a taxonomically diverse community.
Their success depends on the probabilities of finding
food and mates and of escaping predation; these
probabilities are highly conditioned by the characteristics of the physical environment.
The effects of turbulent water motion on the
organisms which are free-living in the water column
differ according to the relationships between individual size and the scale length of turbulent eddies.
Mesoscale eddies represent mainly advection for
small (<10-2 m) organisms (Haury et al. 1978).
However, small-scale turbulence eddies, which are
in the size range of planktonic organisms and their
food, induce changes in the structural and functional properties of primary producers and consumers. It
seems that the complex nature of pelagic food webs,
and even the ultimate fate of biogenic carbon, would
be partially controlled by environmental turbulence
conditions (Kiørboe, 1993).
Taxonomically, the zooplankton is also very
complex. The majority of phyla are represented,
from protozoa to small fishes, although crustaceans
are most abundant. Amongst them, copepods are the
dominant group and play a fundamental role in herbivorous food webs.
The characteristics of planktonic primary producers (small size, generally low energetic value,
and extreme dilution) impose severe conditions for
its efficient exploitation by herbivorous copepods
(Conover, 1968).
In principle, the simplest solution to exploit the
small, dispersed food particles would consist of filtering large amounts of water through adequate
structures. Regarding crustacean zooplankton, and
in particular copepods, the morphology and quick
motion of their feeding appendages (Fig. 2 and 3)
suggested an automatic, mechanical filter-feeding
system. With the rows of bristles in the setae of their
LIFE IN THE PLANKTONIC DOMAIN
Problems of living in a nutritionally
dilute environment
Phytoplankton is assumed to be exploited mainly by the zooplankton, which constitute the first
level of consumers and is one of the most important
contributors to energy transfer in aquatic food webs.
From a trophic point of view, however, zooplankton
is far from uniform and includes, besides herbivores,
omnivores, detritivores (feeding on phyto and zooplankton remains) and carnivores of first- and second-order.
178 M. ALCARAZ
FIG. 2. – A marine planktonic copepod, Centropages violaceus,
with the maxilipedes extended. The rows of bristles in the setae are
visible. (Photograph by A. Calbet).
FIG. 3. – Scanning electron micrographs of planktonic marine copepods showing the appendages related with the feeding processes; a: Maxillipedes of a microphage, herbivorous Copepod, Temora stylifera; b: Maxilipedes of a herbivorous (omnivorous) copepod, Acartia grani;
c: Maxilipedes of an omnivorous copepod (Oithona sp); d: Maxilipedes of a carnivorous copepod (Candacia sp.). There is a transition in
the setal strength and bristle density and intersetule distance from microphagous herbivores (with thin setae provided with dense rows of
bristles), to carnivores, which have setae transformed into robust spines and almost no bristles.
mouthparts, copepods would sieve food particles.
The lower size of the particles would be determined
by the distance between the bristles (Nival and
Nival, 1976; Boyd, 1976). However, given the small
size of the moving appendages, and despite their relatively high velocity, the water flow regime results
in low Reynolds numbers (Lam and Frost, 1976;
Koehl and Strickler, 1981). Reynolds number (Re)
represents the dimensionless ratio between inertial
and viscosity forces. For low Re values (i.e., viscosity dominating over inertia forces, large boundary
layer, and laminar, reversible flow) water filtration
requires high amounts of energy, which cannot be
compensated for by the energy obtained from the
food particles (Alcaraz et al., 1980; Hansen and
Tiselius, 1992). Despite the problems of living in a
viscous world, where food is highly diluted and has
a relatively low nutritive value, copepods have
developed fairly sophisticated sensory systems and
rather complex behavioural patterns (Strickler,
1984) which have determined for their success in
aquatic systems.
How do copepods find food and mates, and
escape predation?
The first, direct observations of tethered copepods feeding on a suspension of phytoplankton,
were made possible by using high-speed filming
techniques (Alcaraz et al., 1980). The method
allowed the observation and quantification of the
exact movements performed by each feeding
appendage, as well as the path followed by the
food particles until captured and ingested or
rejected. Further laboratory experiments using the
same or similar methodology (Paffenhöfer et al.,
COPEPODS UNDER TURBULENCE 179
1982; Strickler, 1982; Cowles and Strickler,
1983) confirmed that copepods are not mere
mechanical filtering machines. They create feeding currents by moving their different feeding
appendages in a synchronous, although out of
phase, “fling and clap” motion. The temporal
sequence of movements ensures the creation and
maintenance of a laminar flow field of constant
structure, almost parallel to the body axis. This
current is necessary to direct food particles
towards the organism, and to detect them via
chemo- or mechanoreception (Strickler, 1982;
Buskey, 1984).
In the laminar feeding current created by a freeswimming calanoid copepod, Strickler (1985)
identified different areas or “cores” according to
the characteristics of water flow and the function
of the interacting appendages (Fig 4). The motion
core is the central kernel or volume and is defined
by the cross-section surface of the capture area.
The viscous core envelops the motion core and
originates in a surface larger than its cross-section.
In this viscous core, water velocity increases in the
proximity of the organisms so that all the water
goes through the capture area. Finally, the sensory
core includes the volume of water scanned by the
sensory structures in the antennae of the copepods.
The volume of water actually searched by the
organism is thus larger than the one defined by the
product of the cross-section of the sensory area of
the copepod times the water velocity relative to
FIG. 4. – Zones or “cores” in the feeding currents created by a
calanoid copepod. 1: Motion core. 2: Viscous core. 3: Sensitive
core. 4: Sensory field of the first antenna. 5: Capture area. (Redrawn
from Strickler, 1985).
180 M. ALCARAZ
the organism. The size and stability of the flow
fields generated by feeding copepods is speciesspecific (Strickler, 1985). In the laminar flow
field, where viscosity dominates over inertia (low
Reynolds numbers), the information necessary to
perceive food particles in advance (mostly chemical cues forming an active sphere around food
items) is adequately directed towards the receptory system of copepods. The precise location of the
incoming information allows the organism to
change the flow field in order to capture the food
particles (Strickler, 1985; Paffenhöfer et al.,
1982). Copepod feeding must be thus considered
as the consequence of a chain of successive steps,
starting with the encounter of a food item, followed by its recognition, capture, and eventual
ingestion or rejection.
It is still unknown the extent to which irregular water movements induced by small-scale turbulence modify the flow field of the feeding currents generated by copepods. In any case, hydrodynamic perturbations could represent changes in
the efficiency of food perception, capture and
ingestion.
After feeding, finding mates and escaping predation are essential for the maintenance of copepods and for zooplankton in general. The interactions between copepods, either of the same or different species, are also very dependent on the
physical properties of aquatic systems (Strickler,
1975 a, 1977). For a copepod, the encounter with
another individual can have either a beneficial
effect, when it finds a mate or a prey, or be disastrous, if the encounter is with a predator. For this
reason, the existence of mechanisms to detect and
identify the likely type of an encounter is essential (Strickler, 1977; Yen, 1988; Yen and Fields,
1992). Copepods use chemical cues (pheromones
for sexual attraction, other chemicals for prey or
predator detection) and mechanical cues (sex or
species-specific hydrodynamical tracks) to identify the nature of approaching encounters.
Although chemical or physical information
should be persistent enough to trigger adequate
behavioural responses (escape or attraction), their
durability must be limited, otherwise they will
accumulate as noise, thus limiting detection efficiency. Turbulent water dynamics, with its associated high diffusion rates, must significantly contribute to the disappearance of hydrodynamic and
chemical cues, so changing the perception scenario of zooplankters.
TURBULENCE, ENCOUNTER RATES AND
COPEPOD FEEDING
Turbulence and encounter rates
An encounter is the first, limiting step for feeding
and mating. In a theoretical model describing seasonal
variation in oceanic production, Cushing (1959) based
the grazing rates of copepods on this assumption. The
rate at which a predator (copepod) contacts food (phytoplankton, its presumably non-motile prey) was considered to be a function of the copepod velocity, the
“contact surface” (corresponding to the cross-section
of the organism including the sensing appendages),
and the concentration of phytoplankton. The contact
surface can be generalized to the encounter surface
defined by the predator’s reactive distance,
Cr = π R2 N v
π R2 N (u2 + 3 v2 )
3v
for v > u,
and
Cr =
π R2 N ( v2 + 3 u2 )
3u
v = (v2 + w2)0.5,
u = (u2 + w2)0.5
where w is root-mean square turbulent velocity.
The contact rate between predators and prey
when taking turbulence into account is then
Cr =
in which Cr is the encounter rate, R is the radius of
the perception area of the predator, N is the food
concentration, and v is the predator’s velocity.
This model of predator-prey contact rate, which
is valid for non-motile prey, was generalized by
Gerritsen and Strickler (1977) considering that both
predator and prey are motile. In their model, the
density component (π R2 N) is the same, but in the
velocity component (v), the velocities of predator
and prey are also taken into account.
Cr =
Taking into account the isotropic nature of smallscale turbulence in the ocean (Gargett et al., 1984;
Gargett, 1997), and the values of the root-mean
square turbulent velocity, (which are uncorrelated
with the swimming speed of planktonic organisms
and of the same order), Rothschild and Osborn
(1988) generalized the model of Gerritsen and
Strickler (1977) by including the effects of smallscale turbulence. The new velocity components of
predator and prey must thus be computed as:
for u > v,
where v and u are the respective velocities of predator and prey. The main consequences of the model
arise from the fact that contact rates are mainly
dependent on the higher of the two speeds. According to the model, and taking into account predation
efficiency (that is, the higher catches in relation to
the predator’s swimming energy expenditure), two
predation “strategies” arise: slow-swimming (or
even stationary), ambush predators, which will
exploit fast-swimming prey; and cruising predators,
preying on slow-swimming prey. The model also
allows the prediction of the trophic community
structure according to swimming speed and trophic
position (Gerritsen and Strickler, 1977).
π R2 N (u2 + 3 v2 + 4 w2 )
3( v2 + w2 )
0.5
for v > u,
which reverts to the equation of Gerritsen and
Strickler (1977) when root-mean square turbulent
velocity w = 0.
The first conclusion of the model is that the
kinetic nature of the environment affects the contact
rate between planktonic organisms. Under turbulence the contact rates are higher than predicted
when only densities and relative swimming velocities of predator and prey are considered. As a consequence, in laboratory experiments where turbulence has not been taken into account, the functional responses that are dependent on contact rates (i.e.,
feeding rates) may have been underestimated. The
extrapolation to natural systems of laboratory data
on copepod feeding rates obtained under calm (nonturbulent) experimental conditions could be biased
(Rothschild and Osborn, 1988; Kiørboe, 1993).
Another important issue is the possibility of linking the physical-biological interaction for different
temporal and spatial scales of variability. Further
improvements of the model include the substitution
of average, constant speeds of predator and prey by
more realistic Gaussian 3-D variable velocity distributions (Evans, 1989) or different motility patterns
and behaviours of predator and prey (Kiørboe and
Saiz, 1995; Saiz and Kiørboe, 1995).
Small-scale turbulence and copepod feeding
The main issue of the models describing the
effects of turbulent water motion on plankton contact
COPEPODS UNDER TURBULENCE 181
FIG. 5. – Time series of the frequency of encounter rates with food particles, fast swimming (escape) events, and
percent time allocated to slow swimming (feeding) of a tethered calanoid copepod (Centropages hamatus) under
turbulent and calm conditions and low (70 cells/ml) and high (350 cells/ml) food concentrations (the dinoflagellate
Gymnodinium sp.). C: Calm. T: Turbulence. (Redrawn from Costello et al., 1990).
rates, is an increase in the “perceived” food abundance from the predator’s point of view, which
could, as a consequence, induce higher feeding rates.
Calanoid copepods create laminar flow fields
(feeding currents) which entrain food particles as well
as the cues to perceive them in advance. It is still
unknown whether the irregular water movements
induced by small-scale turbulence modify the flow
field of the feeding currents generated by copepods,
or can negatively interfere with their perception systems. Theoretical models, however, suggest that
small-scale turbulence has positive effects when
predators (copepods) feed on a “swept clear” mode as
considered in the Rothschild and Osborn (1988)
model which depends on direct contact rates. According the Osborn (1996) model, the feeding currents
182 M. ALCARAZ
created by a copepod would be at scales appropriate
to act in concert with the turbulent motion and diffusion of prey. Feeding currents represent a significant
expansion of the capture radius of copepods, which
will take advantage of the increase in the flux of food
directed by turbulent diffusion (Osborn, 1996).
The effects of turbulence on encounter rates
between copepods and their food, as predicted by
theoretical models, have been confirmed by laboratory experiments. The rate at which food particles
reached the capture area of calanoid copepods was
quantitatively estimated through visual observation
(Marrasé et al., 1990; Costello et al., 1990; Saiz,
1991). In tethered individuals submitted to alternating calm and experimentally induced turbulence
conditions (dissipation rates ranging from ε=0.05
and ε=0.15 cm2 s-3), the encounter rates were dependent on food concentration and local turbulence conditions (Fig. 5).
However, higher encounter rates do not necessarily translate into higher feeding rates. Small-scale
turbulence tends to reduce the “feeding efficacy
index” (Marrasé et al., 1990). This was estimated as
the ratio between the encounter rates of food particles with the copepod’s capture area during slow
swimming (assimilated to feeding activity), versus
the encounter rates in a “control” area far from the
feeding activity of the copepod (Fig. 6). The “effective encounter rate”, equivalent to the frequency of
encounters while the copepod was slow-swimming
(feeding), was significantly higher under turbulence
but only for low food concentrations (Fig. 6).
On the other hand, the balance between energetic
gains (as deduced from the feeding efficacy index),
and losses (i.e., swimming energy expenditure) are
modified by turbulence, but are also dependent on
food concentration (Marrasé et al., 1990). While for
low (undersaturating) food concentrations turbu-
TABLE 1. – The energetic costs of different behavioural activities in
a planktonic copepod, Centropages hamatus, in relative units, and
ratios of the energy spent for the same behaviour under high and
low food concentration . “Low” and “high” values correspond to the
minimum and maximum energetic costs for the different activities.
LFT: Low food concentration, turbulence. LF: Low food concentration, calm. HFT: High food concentration, turbulence. HF: High
food concentration, calm. (From Marrasé et al., 1990).
Energetic costs in relative units
Low value
High value
Slow swimming and
resting stage
1
1.25
Fast swimming
40
400
Ratio of energetic costs
LFT/LF
HFT/HF
HF/LFT
1.04
1.82
1.04
1.42
6.78
1.27
lence increases the potential energy gains of copepods, at high (saturating) food conditions, the
enhancement of energetic costs is much higher than
the gains derived from the higher encounter rates
(Table 1). The above results, however, were
FIG. 6. – The effects of turbulence on A: The encounter rates between copepods and their food. B: Feeding (foraging) efficacy index. C: Effective encounter rates (see text). Experimental food concentrations
as for Fig. 5. (Redrawn from Marrasé et al., 1990).
COPEPODS UNDER TURBULENCE 183
obtained in tethered animals, which perceive a different velocity spectrum than in the case of freeswimming organisms.
These cases provide indirect evidence of higher
feeding rates under turbulence deduced from the
observed higher contact rates with food particles on
tethered copepods (Costello et al., 1990; Marrasé et
al., 1990). Experimental confirmation of the effects
of small-scale turbulence on grazing rates for freeswimming copepods were experimentally confirmed by Saiz et al. (1992 b). The functional
response of grazing and clearance rates to different
turbulent conditions (low turbulence, ε=0.06 cm2 s-3,
high turbulence ε=0.12 cm2 s-3) were highly dependent on food concentration. The higher feeding and
clearance rates of copepods at food concentrations
below saturation (Table 2), confirm the hypothesis
of Rothschild and Osborn (1988), regarding the
increase in food concentration as perceived by
organisms under turbulence. It is also in agreement
with the observed dependence of the “feeding efficiency index” on food concentration (Marrasé et al.,
1990). The degree at which feeding rates are
enhanced by turbulence is species-specific (Table
II), even for closely-related species of the same
genus (Saiz et al., 1992), and probably also depends
on the average turbulence conditions experienced by
the copepods in their natural habitat.
Those direct effects of turbulence, mainly attributable to changes in the food environment as perceived by copepods, are indirectly modulated by the
TABLE 2. – Average clearance and ingestion rates under turbulent and
calm conditions in relation to food concentration for two Acartia
species. FC: Food concentration range, in ppm. by volume. F: Clearance
rates, volume of water swept clear, in ml/ind/day. I: Food ingestion
rates in algal volume, µm3/ind./day. 106. (From Saiz, 1991).
modifications induced on phytoplankton by turbulent water motion. Phytoplankton cell size and
chemical composition are affected by small-scale
turbulence through changes in nutrient uptake kinetics and light environment (Kiørboe, 1993). Similarly, turbulence and other co-variant factors such as
nutrients and light, are selective forces that can
determine the dominance, in natural ecosystems, of
the different phytoplankton life forms (non-motile
forms like diatoms in turbulent, high-nutrient environments, and motile forms like dinoflagellates in
low turbulent, poor nutrient conditions: Margalef,
1978).
In conclusion, turbulent water movements induce
changes in the velocity components affecting copepods and their food and increasing their rate of
encounter. As a consequence of the higher concentrated food environment as perceived by copepods,
feeding rates increase accordingly. However, given
the functional relationships between food abundance and grazing, small-scale turbulence has an
enhancing effect on feeding rates mainly for undersaturating food concentrations. The possible interaction between turbulent water motion and laminar
flow field generated by feeding currents remain
unknown, although theoretical models predict a
more efficient use of turbulent water motion by
copepods creating feeding currents.
To those general, direct issues of small-scale turbulence on copepod feeding, indirect effects derived
from turbulence-induced changes in food quality
should be added. In any case, the consequences of
turbulence from a trophodynamic point of view can
be very complex, and dependent not only on food
concentration, but also on the size and motility of
food and the copepod, its feeding behaviour, and
turbulence intensity.
Acartia tonsa
Calm
FC
0.18-0.23
0.24-0.29
0.4-0.5
0.57-0.87
1.08-1.23
Turbulence
F
I
F
I
139.4
156.9
62.0
59.0
50.5
28.1
41.9
29.6
44.4
57.1
165.4
181.4
79.3
134.73
41.5
32.2
46.6
32.9
92.1
45.3
Acartia grani
Calm
FC
0.15-0.18
0.20-0.29
0.24-0.38
1.14-1.37
1.69-1.90
Turbulence
F
I
F
I
50.5
69.6
41.4
19.9
24.0
8.5
18.9
13.4
25.8
44.1
128.7
131.4
49.0
45.8
30.2
14.5
27.8
12.7
53.3
52.1
184 M. ALCARAZ
TURBULENCE, COPEPOD BEHAVIOUR AND
METABOLISM
Swimming in copepods: behavioural pattern
and energetic costs
The most important fraction of the energetic budget of copepods corresponds to active metabolism.
This includes the basal or maintenance metabolism,
plus a variable amount of energy derived from the
costs of swimming (Prosser, 1973). By definition,
copepod swimming capacity appears as almost negligible if compared with large scale advective water
movements. However, copepods, and in general
planktonic animals, exhibit an almost constant activity in searching for food and mates, or escaping predation. The vertical migrations performed by the
majority of zooplankters involve displacements of
hundreds of meters and, when scaled to the relative
size of organisms, the daily traveled distances are
considerable (tens of thousands of body lengths per
hour). Locomotion includes a diversity of swimming movements and propulsion mechanisms in
planktonic copepods, with different consequences
from the point of view of the energy consumed
(Strickler, 1977). Normal cruising is characterized
by almost constant or oscillating swimming speeds.
In this swimming mode, displacement usually takes
place in smooth gliding (slow swimming). This generally results from the creation of feeding currents,
as in the majority of calanoid copepods. Oscillating
swimming speeds are typical of cyclopoid copepods, which swim in a hop-and-sink pattern, a consequence of a series of powerful strokes of the
swimming legs (Strickler, 1977).
Apart from this undisturbed swimming model,
some stimuli can trigger escape reactions (Singarajah, 1975), involving velocities about 500 body
lengths per second, and accelerations as high as
1200 cm s-2 (Strickler, 1975 a). Escape reactions are
generally the consequence of avoidance responses
to an undesirable encounter. They occur after the
detection of the flow disturbance created by another
swimming zooplankter, a possible predator.
The detection of changes in flow velocity is
made possible by the existence of a sensory system
able to measure very small disturbances of flow
velocity (Strickler, 1975 a). In copepods, the sensory system is represented by chemoreceptors (aesthetascs) and mechanoreceptive sensilla (Bundy and
Paffenhöfer, 1993) displayed in arrays mainly in the
first antennae. Mechanoreceptors consist of modified ciliary structures able to detect the changes in
inertial forces (Barrientos, 1980). Their arrangement, size and orientation (Fig. 7) are probably
determined by the flow characteristics and intensity
of the stimulus to detect (Haury and Kenyon, 1980;
Yen and Nicoll, 1990). The neural activity recorded
when antennal receptors are mechanically stimulated evidences a very high sensitivity. Neural responses have been obtained for frequencies ranging from
40 to 1000 Hz, and setal displacements as small as
10 nm (Yen et al., 1992). The main behavioural consequences of the stimulation of antennal mechanoreceptors are changes in the swimming pattern, with
FIG. 7. – Scanning electron micrograph of the first antenna of a male
calanoid copepod, Acartia clausi, showing the distribution of
mechano- and chemoreceptors.
an increase in the frequency of escape responses
(Gill and Crisp, 1985).
The evaluation of the proportion of the active
metabolism that corresponds to swimming costs in
copepods entrains serious difficulties. The available
data are scarce and contradictory, and differ by
orders of magnitude, depending on the methodological approach. The higher values correspond to indirect estimates based on the decrease on lipid contents of organisms after long, sustained vertical
migrations (95% of total metabolism: Petipa, 1966).
Other high values were obtained from the comparison of oxygen consumption rates on free-swimming
and inactive (narcotized) copepods (30-40% of total
metabolism: Klyastorin and Yarzombek, 1973;
Paulova and Minkina, 1983). Values deduced from
the evaluation of parameters of Newton’s quadratic
resistance law, using data on velocity and acceleration obtained through high-speed filming, give
much lower values (around 0.1% of total metabolism: Vlymen, 1970; Strickler, 1975 b). These low
energetic costs coincide with direct measurements
COPEPODS UNDER TURBULENCE 185
of the work done (deformation of a calibrated
spring) by a restrained copepod in each swimming
leap (Alcaraz and Strickler, 1988).
Part of the disagreement between the estimations
of the energetic costs of swimming arises from
methodological problems and considerations about
the efficiency of the work done by swimming organisms (Alcaraz and Strickler, 1988). However, part of
the variability is probably due to differences in the
swimming behavioural pattern displayed by the
organisms. The various behavioural components of
swimming activity (i.e., resting, non-disturbed
swimming, and escape reactions) require different
energetic costs, so their relative frequency and duration can significantly modify metabolic expenditure.
While for non-disturbed swimming the energetic
consumption corresponds to the lower values here
reported, a single escape reaction requires about 400
times more energy per unit time than normal cruising speed (Strickler, 1977).
The most conspicuous direct effects of smallscale turbulence on copepod activity refer to
changes in the pattern of swimming behaviour
(Costello et al., 1990; Marrasé et al., 1990). Visual
observations of tethered copepods indicate an
increase in the proportion of time allocated to the
“slow swimming”. This behaviour, which is assimilated to feeding, or at least to the creation of feeding
currents, appears to be triggered by the higher rate
of encounter of the copepod with food particles, and
is more conspicuous for low food concentration (see
Fig. 6). Simultaneously, the frequency of fast-swimming events (or escape reactions) also increases.
Visual observations of video-recorded free-swimming calanoid copepods (Acartia clausi) confirmed
the general character of behavioural changes, and
allowed quantitative estimates of the effects of turbulence on swimming patterns. Turbulence levels
similar to those observed in highly dynamic shelf and
coastal ecosystems (low turbulence, ε= 1 mm2 s3, high
turbulence, ε= 5 mm2 s-3) significantly increased the
proportion of time allocated to slow swimming, even
in the absence of food, when compared to calm conditions (about 2.5 times higher: Saiz and Alcaraz,
1992 a). Simultaneously, the frequency of escape
reactions was about three times that observed under
calm conditions, as was the velocity displayed, while
the time allocated to rest proportionally decreased.
The energy consumed under turbulence as compared
with calm conditions due to the change in the frequency of the different swimming patterns represented a 83-115% increase.
186 M. ALCARAZ
Effects of turbulence on zooplankton
metabolism
The turbulence-induced changes in the swimming behavioural pattern of planktonic copepods
result in an enhancement of the frequency and intensity of high-energy consuming activities (Marrasé et
al., 1990; Costello et al., 1990; Saiz and Alcaraz,
1992 a; Hwang et al., 1993), which must translate
into higher respiration and excretion rates.
The effects of small-scale turbulence on respiration rates of crustacean zooplankton have been
experimentally confirmed through the study of the
changes on heart-beat rates (Alcaraz et al., 1994a).
The rate of heart-beating is an efficient descriptor of
the respiration rates of crustaceans (Ingle et al.,
1937; Pavlova and Minkina, 1983), and its almost
immediate response is very adequate for the study of
short-time metabolic responses to microscale perturbations. Small-scale turbulence (ε ranging from
0.002 to 0.32 cm2 s-3) increases heart-beat (respiratory) rates in a variety of planktonic crustaceans
with a differentiated heart, from cladocerans to
decapod crustacean larvae (Table 3). Although the
experiments were performed on tethered organisms,
and thus the experienced flow field must be different from that of free-swimming individuals (Tiselius
and Jonsson, 1990), tethered copepods seem to display the same activity pattern as free-swimming
ones (Hwang et al., 1993).
The intensity at which heart-beat rate is
enhanced by turbulence appears to be species-specific, and seems to be related to differences in sensitivity to hydrodynamic disturbances, probably due
TABLE 3. – Effects of turbulence on heart-beat rates for different
planktonic crustaceans. The heart beating was video-recorded on
tethered individuals, and corresponds to average values of two alternate 15 min. periods of calm and turbulence for each individual.
Experimental temperature in º C. Average increase of heart-beat
rates under turbulence in %. Probability values for the two-tailed
Wilcoxon ranked sign test. N is the number of individuals tested.
(Modified from Alcaraz et al., 1994a).
Organism
Temp ºC
Decapod larvae
Porcellana longicornis 19.3
Brachinotus sexdentatus 25.0
HBR increase
(%)
N Probability
9.2
9.4
2
5
<0.005
<0.005
Cladocerans
Daphina pulex
Penilia avirrostris
18.0
15.6
14.6
5.9
12
4
<0.001
<0.001
Copepoda
Calanus gracilis
22.0
93.7
1
<0.001
those observed in respiration (heart-beat rates) estimated for other copepod species (Table 3).
To these direct effects of turbulent water movement, the enhancement of the nutritious value and
cell size of phytoplankton, and changes in their pattern of spatial distribution and patchiness field
(Kiørboe, 1993), indirectly modify zooplankton
activity pattern under turbulence, with consequent
changes in energy expenditure.
TURBULENCE, GROWTH EFFICIENCY AND
DEMOGRAPHIC STRUCTURE OF COPEPODS
Turbulence and gross-growth efficiency
FIG. 8. – Percent increase in the rate of heart beating under turbulence relative to calm conditions, for a planktonic crustacean Daphnia pulex, in relation to temperature. The shaded area corresponds
to the average increase. The effect of turbulence is temperaturedependent, being maximum at 18 ºC, corresponding to the temperature at which Daphnia cultures were maintained in the
laboratory. (Modified from Alcaraz et al., 1994).
to differences in the mechanoreception system. The
effects of small-scale turbulence appear to be modulated by temperature, with the higher percent
increase in heart-beat rates around the environmental “in situ” temperature experienced by the organisms (Fig. 8).
Laboratory measurements of excretion rates in
copepods also confirm the higher metabolic activity
induced by turbulence (unquantified turbulence levels: Saiz and Alcaraz, 1992 b). Under turbulence,
ammonia and phosphate excretion rates increased
about 60% with respect to calm conditions, equivalent to a temperature rise of about 7º C assuming a
Q10 of 2 (Table 4). The percent increases in excretion
rates are lower, although of the same order, than
TABLE 4. – Increase of NH4-N and PO4-P weight-specific excretion
rates under turbulence as compared to calm conditions for several
planktonic copepods (Acartia). Average percent increase and standard deviation (STD). N= number of replicates. (Modified from
Saiz and Alcaraz, 1992b).
Species
Ammonia excretion (ng NH4-N.µg bodyN-1.day-1)
Average % increase
STD
A. margalefi
A. clausi
A grani
55.6
26.0
65.8
34.7
23.6
N
33
3
29
Phosphorus excretion (ng PO4-P.µg bodyN-1.day-1)
A. margalefi
63.8
16.3
7
The energy obtained through the ingestion of
food by planktonic copepods must supply, apart
from the requirements for active metabolism (basal
metabolism plus swimming), the costs for growth
and reproduction. In the balanced equation, a term
that remains almost constant, or at least that cannot
suffer a drastic reduction, is basal metabolism. As
swimming activity must also be maintained above a
minimum level, any reduction in energy intake will
affect mainly the production term.
There are no satisfactory methods to estimate the
amount of energy invested in zooplankton production. For planktonic copepods, however, it is commonly accepted that the rate of egg production by
females is directly related to the amount of food
ingested (Kiørboe et al., 1985; Berggreen et al.,
1988), and can be considered as a robust estimator
of secondary production (Poulet et al., 1995). The
gross-growth efficiency (production/ingestion) is a
crucial parameter in plankton production models.
For copepods, it can be adequately estimated
through the ratio egg produced/food ingested, either
in units of carbon or energy (Kiørboe et al., 1985).
As discussed above, turbulence has a direct
enhancement effect on grazing (food intake) rates,
and on metabolic energy consumption. The balance
between the energy gains derived from the enhancement of grazing rates, and the corresponding losses
resulting from increased metabolic rates, will thus
determine the amount of energy allocated to zooplankton production.
In simultaneous estimates of ingestion rates and
egg production by female copepods, Saiz et al.
(1992) observed a decline in the number of eggs laid
by females under turbulence as compared with calm
conditions. The importance of the reduction in the
COPEPODS UNDER TURBULENCE 187
TABLE 5. – Effect of turbulence on the gross-growth efficiency of
planktonic copepods (Acartia) as estimated through the quotient
“carbon egg produced/carbon food ingested”. C: Calm. T: Turbulence. Average values ± standard deviation. Data pooled for all the
experimental food concentrations. Test: one way ANOVA, or when
its assumptions are not accomplished, Mann-Whitney two tailed
test, (*). (Modified from Saiz et al., 1992).
Species
A. tonsa
A. grani
A. clausi
Experimental conditions
Calm
Turbulence
0.37 ± 0.029
0.36 ± 0.035
0.70 ± 0.052
Significance
0.33 ± 0.024
Non-significant
0.26 ± 0.018 Significant, p<0.007*
0.49 ± 0.037 Significant, p<0.002
gross-growth efficiency under turbulence (Table 5)
differed even for closely-related (congeneric)
species, probably in relation to the turbulence conditions of their habitat. These results are in accordance with the stronger influence of turbulence on
metabolic rates as compared with grazing (energy
intake), and reflect a global reduction in the energy
allocated to egg production, once the metabolic
demands have been satisfied.
Other effects of small-scale turbulence on zooplankton: Development rates, individual size,
and sex ratio under turbulence
The cumulative effects of turbulence on the
copepod rate processes discussed above (grazing,
swimming behaviour, metabolic expenses, excretion, gross-growth efficiency) result into changes in
the extensive properties of their populations. The
positive or negative effects of small-scale turbulence
on secondary production (or, at least on the fraction
of energy allocable for production) are highly
dependent of the balance between energetic gains
and losses. Energetic gains can be either induced
directly by turbulence (higher feeding rates: Saiz et
al., 1992) or indirectly, through the higher nutritious
value, higher size or changes in the field patchiness
of algal food (Kiørboe, 1993); losses are mainly the
consequence of direct increases in metabolic
expenses due to changes in swimming behaviour
(Marrasé et al., 1990; Saiz and Alcaraz, 1992 a).
Thus, the turbulence characteristics of the environment are a significant factor in the modulation of the
dynamics of copepod populations.
Other effects of small-scale turbulence on the
dynamics and structure of copepod communities
concern the development times for the different
instars of copepods, and the final body size of
adults. Alcaraz et al. (1988) and Saiz and Alcaraz
188 M. ALCARAZ
FIG. 9. – Development times of two cohorts of Acartia grani (copepod) under calm and turbulent conditions, relative to the maximum
time needed to reach the adult stage. The development of the two
cohorts was made under similar food conditions. Under turbulence,
there is an acceleration of the rate of development, more important
for the younger stages. (Redrawn from Saiz and Alcaraz, 1992).
(1991) observed a significant reduction in the development time for the different instars of Acartia
grani in laboratory-reared cohorts submitted to turbulence (ε around 0.05 cm2 s-3) as compared to calm
conditions (Fig. 9). Development under turbulent
and calm conditions started simultaneously, from
eggs laid by females belonging to the same population and in cultures with saturating food concentrations. The effects of turbulence appear to be agedependent, as the maximum reduction in the duration of successive instars occurs for naupliae and
early copepodites.
The acceleration in the development of copepods
under turbulence can be a phenomenon comparable
with the ageing effect and reduction in the life span
observed by Shaw and Bercaw (1962) for other
crustaceans, and related to temperature-induced
higher metabolic expenses. The same explanation
can be valid for the reduction of individual size
observed when the cohort develops under turbulence (Saiz and Alcaraz, 1991). Although the size
differences between equivalent instars for cohorts
grown under calm and turbulent conditions are only
significant for adult stages, the effects were also
observed from the stage copepodite II onwards
(Table 6).
TABLE 6. – Effects of turbulence on individual size (µm) and biomass (µg dry weight) of a planktonic copepod, Acartia grani, in laboratory
microcosms at equivalent food conditions. Only data for Copepodite II and onwards have been represented. Mean values and standard deviations for calm and turbulent conditions. *: Significant at the 0.01 level. (Modified from Saiz and Alcaraz, 1991).
Instar
Size
Biomass
Calm
CII
CIII
CIV
CV-VI (male)
CV-VIf (female)
Male
Female
Turbul.
Calm
Turbul.
450.9 ± 23.2
555.3 ± 19.3
677.0 ± 32.4
787.2 ± 16.2
863.5 ± 32.1
441.4 ± 20.0
555.9 ± 23.7
672.5 ± 28.2
788.2 ± 21.6
855.3 ± 26.3
0.938
1.776
3.259
5.176
6.873
0.879
1.782
3.194
5.197
6.675
883.7 ± 25.8
1013.7 ± 32.5
873.6 ± 23.2*
1006.6 ± 37.2
7.378
11.235
7.123
10.997
Other effects of small-scale turbulence on copepod demographic structure concern the determination of adult sex ratios (Alcaraz et al., 1988). In the
same laboratory populations of copepods used as in
the study of development rates, a lower proportion
of males was observed under turbulence as compared with calm conditions (Table 7). Simultaneously, female fecundity was highly depressed, not only
due to the already discussed reduction on grossgrowth efficiency (Saiz et al., 1992), but also due to
the reduction of the male proportion. As observed
by Wilson and Parrish (1971), Alcaraz (1977) and
Alcaraz and Wagensberg (1978), the fecundity of
Acartia species is very sensitive to changes in the
sexual ratio. Nevertheless, these negative effects of
turbulence on copepod communities were observed
at saturating food concentrations, in which ingestion
rates cannot benefit from the higher encounter rates
between copepods and their food, and the higher
energetic losses due to turbulence clearly reduce the
energy allocated to reproduction.
The final consequence of the above mentioned
effects of turbulence on copepod communities is the
increase in the turnover rate of their populations due
TABLE 7. – Effects of turbulence on the mean adult sex ratios
(male/male+female) and instantaneous values of the quotient
eggs/female of Acartia grani in laboratory microcosms under similar food conditions. Day: number of days after starting the experiment. C: Calm. T: Turbulence. In parentheses, standard error of the
mean. (Modified from Alcaraz et al., 1988).
Day
0
4
8
12
16
Mean
Sex ratio (/+)
Calm
Turbul
Eggs/female
Calm
Turbul
0.23
0.29
0.26
0.40
0.48
0.23
0.36
0.17
0.07
0.19
61.6
111.0
84.8
119.7
89.86
72.6
50.3
41.4
0.33
(0.04)
0.20
(0.04)
94.2
(11.4)
63.5
(10.9)
to the shorter cohort development time. Simultaneously, there is a tendency toward a reduction in
copepod biomass as a result of the decrease in individual size and the decline in female fecundity.
TURBULENCE, COPEPOD-PHYTOPLANKTON
INTERACTIONS AND THE TROPHIC STRUCTURE OF PLANKTONIC COMMUNITIES
The structure and dynamics of planktonic systems are the consequence of a complex web of positive and negative feed-back mechanisms between
the elements conforming the different trophic
groups. Copepods, as the most important component
of the first level of consumers, exert a double control of qualitative and quantitative properties of phytoplankton. Apart from reducing phytoplankton biomass by grazing pressure, through selective feeding
copepods can modify the size-spectrum and even the
structure of phytoplankton communities. In turn, the
nitrogen (mainly ammonia) and phosphorus (as soluble reactive phosphate) excreted by zooplankton
can represent a significant contribution to the phytoplankton requirements of nutrients, thus allowing
the increase of the regenerated production (Sterner,
1986).
From rate processes to extensive properties:
interaction between copepods and phytoplankton under turbulence
Through the enhancing effects of turbulence on
copepod activity (higher feeding and excretion
rates, higher foraging activity by enhanced swimming pattern), the turnover rate of primary producers should increase. On the contrary, the turbulenceinduced lower gross-growth efficiency tends to
depress the production rate of copepods. As a conCOPEPODS UNDER TURBULENCE 189
FIG. 10. – Effects of the interaction between turbulence and zooplankton on the evolution of natural phytoplankton communities. Time
changes of phytoplankton biomass (chlorophyll) on natural marine communities developed in laboratory microcosms. Q: Calm conditions
without zooplankton. QZ: Calm conditions with zooplankton added. A: Turbulent conditions without zooplankton. AZ: Turbulent conditions with zooplankton. Continous and dashed lines correspond to the two duplicates for each experimental condition. Abscissae: Time in
days. Ordinate: µg Chla/l. While no significant differences were observed amongst microcosms under calm (Q), turbulent (A), or calm conditions with zooplankton (AZ), the pressence of zooplankton in turbulent microcosms significantly modified the temporal evolution of
phytoplankton biomass. (Modified from Alcaraz et al., 1989).
sequence of the reduction on the growth of copepod
populations, the overall grazing pressure on primary producers is significantly reduced. To these
direct effects of turbulence on copepod activity,
other indirect effects must be added. The increase
of phytoplankton production caused by turbulence
(Margalef, 1974; Legendre, 1981), and the changes
on qualitative properties of phytoplankton like cell
size, life-forms selection, and chemical composition (Margalef, 1978; Marrasé, 1986; Kiørboe et
al., 1990; Estrada et al., 1987 a; Estrada and
Berdalet, 1997), would affect the feeding activity of
herbivorous copepods. At the smaller length-scales,
turbulence will have effects only at the individual
level. However, its consequences accumulate and
translate into changes in the planktonic community,
modifying the structure and function for the whole
ecosystem.
The study of the effects directly induced by turbulence on natural systems is complicated, amongst
other reasons, by the impossibility of controlling
turbulence, or of separating its effects from other co190 M. ALCARAZ
variant factors (i.e., nutrients and light: Estrada et
al., 1987 a, b; Alcaraz et al., 1989; Marrasé, 1986).
These inconveniences are partly prevented by the
use of laboratory microcosms. The existence of
well-defined boundaries, their replicability, and the
possibility of controlling environmental factors,
allow the study of the direct effects of turbulence on
the evolution of the structure and dynamics of
planktonic systems (Perez et al., 1977; Nixon et al.,
1979; Oviatt, 1981; Alcaraz et al., 1989). Nevertheless, due to scale constraints and altered spatial and
temporal variability patterns, microcosms must not
be considered as laboratory replicates of natural
ecosystems (Harte et al., 1980).
In studies addressed to experimentally verify the
Margalef (1978) model about the selection of phytoplankton life-forms in relation to the environmental
turbulence and nutrient conditions (Estrada et al.,
1987 a, 1988), the effects of trophic interactions
with planktonic herbivores was also studied
(Alcaraz et al., 1989).
In all the microcosm experiments, and regard-
less of the nutrient or turbulence conditions, the
time-course of phytoplankton biomass followed a
similar pattern. After few days of enclosing the
experimental communities, there was the development of a phytoplankton burst composed by centric diatoms, similar to the spring phytoplankton
bloom. This was followed by a decline in phytoplankton biomass to values similar to the initial
conditions (Marrasé, 1986; Estrada et al., 1987 a,
b; Alcaraz et al., 1988, 1989). No significant differences were observable when comparing calm
microcosms (with and without copepods), or turbulent microcosms in which copepods had been
removed. On the contrary, when the trophic structure of plankton was not changed (herbivorous
copepods not excluded), turbulence induced significant changes in the time-course of phytoplankton biomass development (Alcaraz et al., 1988,
1989). There was a delay in the development of the
phytoplankton bloom with respect to calm microcosms (Fig. 10), or secondary blooms occurred.
The values of integrated phytoplankton biomass
were also higher, and there was a tendency towards
the selection of larger sized phytoplankton cells,
independently of the possible formation of large
aggregates of plankton and detritus due to the
coagulative effects of turbulence (Oviatt, 1981;
Alcaraz et al., 1989; Kiørboe, 1997). The evolution of the taxonomic composition of phytoplankton assemblages, although modulated by turbulence conditions, appeared more dependent on the
successional stage of the natural communities
(Estrada et al., 1987a).
The trends observed in the evolution of the state
variables of primary producers in microcosms confirm the cumulative effects of enhanced rateprocesses of copepods at an individual level under
TABLE 8. – Effects of turbulence on the trophic efficiency (ratio
consumers biomass/producers biomass) of copepod communities
(Acartia grani) in laboratory microcosms at equivalent initial food
conditions, copepod abundance and sex ratios. Day: days after starting the experiment. C: calm. T: turbulence. In parentheses: standard
error of the mean. (Modified from Saiz et al., 1992).
Day
Trophic efficiency
Calm
Turbulence
0
4
8
12
16
0.031
0.012
0.132
0.280
3.210
0.029
0.010
0.095
0.600
1.070
0.731
(0.619)
0.361
(0.208)
Mean
turbulence. The higher values of integrated phytoplankton biomass are consistent with the reduction
of consumers biomass, a general tendency
observed in microcosms under turbulence (Oviatt,
1981; Alcaraz et al., 1988, 1989). The consequences from a functional point of view are the
final reduction of the grazing pressure, and the
lower trophic efficiency of the system (Table 8),
which result in a reduction of the biomass of consumers (copepods) supported per unit of producers
biomass (phytoplankton).
Global effects of turbulence on pelagic systems
The control exerted by mechanical (exosomatic) energy on plankton distribution (Mackas et al.,
1985; Tett and Edwards, 1984), production (Margalef, 1974; Legendre, 1981) and selection of phytoplankton life forms (Margalef, 1978), is particularly evident in relation to hydrographic singularities that occur across a wide range of space and
time. In the majority of examples in which the
structure, spatial distribution, and relative proportion of the trophic components in pelagic systems
appear related with the forcing induced by exosomatic energy, the characteristics of small-scale turbulence play an important role (Cushing, 1989;
Kiørboe, 1993). The matter and energy originated
from phytoplankton production circulates in pelagic systems across two main trophic webs. By the
classical, herbivorous food webs, the production of
relatively large phytoplankton is transferred to
higher trophic levels mainly through herbivorous
copepod grazing; by microbial food webs, phytoplankton production goes to microheterotrophs
(bacteria), and enters the microbial loop (Azam et
al., 1983; Le Fèvre and Frontier, 1988).
The relative importance of either of the two
transfer pathways has significant consequences for
the ultimate fate of the biogenic carbon. The carbon circulating through the microbial loop returns
to the atmosphere in about < 10-2 years, and constitutes the short-lived carbon pool. When biogenic carbon circulates via classical herbivorous
food webs (mainly copepods), its turnover time
ranges from > 10-2 to 102 years, which correspond
to the long-lived or sequestered pools (Legendre et
al., 1993).
The selection of either of two transfer pathways
is in part controlled by the coupling between the
temporal scales of energy inputs (responsible for
the phtyoplankton outbursts), and those correCOPEPODS UNDER TURBULENCE 191
sponding to the different trophic compartments
(i.e., the response time of bacteria, bacterivores,
phytoplankton and herbivorous copepods). In
marine areas where the energy inputs are periodic,
the cycles of stabilization-destabilization can
induce phytoplankton pulses, either tuned or not
with the time-response of the different groups of
heterotrophs. This is the case observed by Holligan et al. (1984a, b) and Le Fèvre and Frontier
(1988) in the vicinity of the English Channel,
where the heterogeneity in the spatial distribution
of the different trophic groups of plankton is highly persistent and related to the different frequencies at which mechanical energy inputs occur. At a
thermally stratified zone on the shelf and a tidal
front, the dominant periodicity of energy inputs
corresponds to the alternation between neap and
spring tides that allows short phytoplankton pulses every two weeks. Due to the lack of tuning
between the frequency of phytoplankton pulses
and the time-response of herbivorous zooplankton,
these areas are cumulative biotopes. The biomass
of primary producers is not grazed and a microhetrotrophic food web develops, although eventually, microheterotrophs can be grazed upon by
large macrozooplankton. In the Shelf-Break zone,
the periodicity corresponds to the M2 tide. The frequency of phytoplankton bursts is coupled with
the response time of herbivorous copepods. The
result is a quasi-permanent regime that leads to a
classical food web dominated by herbivorous
copepods (Le Fèvre and Frontier, 1988; Legendre
et al., 1993).
When the inputs of external energy are not periodic (i.e., weather induced), the spatial heterogeneity in the planktonic trophic groups is less persistent, and the changes in the trophic pathway are
hardly reflected by the taxonomic structure of the
planktonic communities. This is the case observed
in the vicinity of the Catalan density front in the
Western Mediterranean (Estrada and Margalef,
1988; Font et al., 1988), where the spatial heterogeneity of the different trophic groups is weak. In
such circumstances, the time changes in the relative importance of both transfer pathways are better indicated by the relationships between rate
processes of the different trophic groups, which
respond almost immediately to biological (trophic)
or physical (turbulence) stimulation (Alcaraz et al.,
1994 a, b; Calbet et al., 1996), and are in agreement with the intermittent and fluctuating nature of
turbulence.
192 M. ALCARAZ
CONCLUSIONS
Apart from the changes in the velocity components of planktonic organisms (and consequently on
their rate of encounter) due to hydrodynamism,
small scale turbulence enhances copepod rate
processes similar to an increase in temperature (i.e.,
higher feeding, respiration, excretion, swimming
behaviour, and development rates), and modifies
organism size and even sex determination.
The changes on copepod rate processes at the
individual level translate, through cumulative
processes, to changes in the extensive properties of
whole plankton communities. Our knowledge about
the functional response of copepod rate processes to
changes in physical, chemical or biological conditions, and the corresponding interaction with other
trophic components of the pelagic system, derives
from laboratory experiments. Until recent years, the
importance of turbulence had not been considered
and, as a consequence, the underestimated activity
rates used to produce plankton production models
have been biased.
The forcing induced by small-scale turbulence
on the feed-back mechanisms that control the interaction between phytoplankton and herbivorous
copepods is schematized in Fig. 11 (Saiz, 1991).
However, the functional response of planktonic
copepods to small-scale turbulence has been only
partially studied. Uncertainities derive not only from
the observed species-specific differences in the
organismal reponse to turbulence. An important
unresolved problem refers to the “quality” of the turbulent flow generated in laboratory experiments,
which need to be compared with the characteristics
of “true” field turbulence (Strickler et al., 1997). A
second source of undetermination arises from the
turbulence intensity used in laboratory studies. The
energy dissipation rates of experimentally generated
turbulence (ε) usually correspond to the highest values recorded in highly dynamic marine environments, which represent a reduced proportion of the
overall marine turbulence (Peters and Redondo,
1997). Nevertheless, average values of ε do not adequately represent singular, extreme values as expected taking into account the intermittent nature of
small-scale turbulence.
Planktonic copepods occupy a key position in
planktonic systems. Their size, swimming velocity
and feeding behaviour could explain their evolutive
success and the important role played in the matter
and energy flow in aquatic systems. Copepods feed
FIG. 11. – Diagram of the effects of turbulence on rate processes of zooplankton and qualitative and quantitative properties of phytoplankton at the individual level, and their consequences for plankton communities and ecosystem
function. (Modified from Saiz, 1991).
in a “viscous” world, at low Reynolds numbers (Re ≈
1), but are preyed upon and develop escape responses in the “inertial” realm, under high Reynolds numbers (Re up to 1000: Naganuma, 1996), linking primary producers with carnivores (mainly fishes). For
this reason, a better understanding of the changes
induced by small-scale turbulence on the processes
taking place in this border line between viscous and
inertial forces would represent a significant step in
the knowledge of pelagic systems.
ACKNOWLEDGEMENTS
This work was made possible by the organizers
of the MAST-II Advanced Course “Ocean turbulence: A basic environmental property for plankton”, and financially supported by the CICYT
grants AMB94-0853 and AMB94-0746. The author
wishes to express his gratitude to C. Marrasé and
unknown referees for their critical reading of the
manuscript.
COPEPODS UNDER TURBULENCE 193
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