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Zooplankton 1
Zooplankton
Two books were used mainly for this chapter and a majority of
figures are issued from
these books (extra figures were found on the Internet):
Robert Wetzel Limnology: lake and
river ecosystems
Academic Press
Elsevier 798-0-12-744760-5
BST 551.48 W 538 l
Jacob Kalff Limnology: inland
water ecosystems Prentice Hall 0-13-033775-7
BST 551.48 K 124 l
Definitions
Seston = all particulate matter in the water column, composed of
bioseston (= plankton +
nekton), abioseston (inorganic matter) and tripton (organic not
living matter)
Plankton = floating, weak-swimming organisms
Nekton = strong-swimming organisms, the limit between plankton
and nekton being
obviously arbitrary.
Microzooplankton: planktonic animals smaller than 200 m,
comprised principally of
protozoans, rotifers and the smallest larval instars of
copepods
Protozooplankton: planctonic protozoans, for several (mostly
technical) reasons they are
often considered separately from the other microzooplankton
members.
Macrozooplankton: animals, mainly Crustaceans that are larger
than 200 m
Picoplankton:
Filtration rate = filtering rate = filtration capacity = volume
of water containing food
particles that is filtered by an animal in a given time
Feeding rate = grazing rate = quantity of food ingested by an
animal in a given time
Diversity
Zooplankton is a characteristic of still waters, however, it can
develop in rivers if the
residence time is long enough; but then it will irreversibly be
carried to the sea Thus in
rivers regulated by dams zooplankton can develop better than in
natural rivers.
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Zooplankton 2
There are enormous variations from lake to lake in the
planktonic composition, density,
production, seasonal succession, etc. Therefore the information
that is mentioned
hereunder is of course correct (mainly for temperate lakes and
ponds) but many other
patterns can be encountered.
The zooplankton in fresh waters is much less diverse than in the
oceanic ecosystems, it is
made of (the dominant groups are underlined):
Holoplankton (planktonic their whole life) [Protozoans and
heterotrophic
flagellates, Rotifers, Crustacea (Cladocera, Cyclopoid and
Calanoid Copepoda,)]
Meroplankton (only a part of their life cycle is planktonic)
[Protozoans,
Ostracoda, Mysidaceaa, Branchiopoda (other as Cladocera), Insect
larvae (Chaoborus,
Chironomidae, Culicidae), Coelenterates (Jellyfish), Larval
trematode flatworms,
Gastrotrichs, Acarina (mites), Larval clams (Dreissena), Very
young larval fish]
Figure The protozooplankton freshwater diversity in one single
eutrophic pond with
water stratification (and a resultant gradient of oxygen
concentration). The heterotrophic
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Zooplankton 3
nanoflagellates (HNF) have not been drawn; mention that their
abundance scale is 105
times narrower than the scales for the ciliates (
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Zooplankton 4
Species richness
There are generally between 50 and 100 zooplanktonic (non
protozoan) species in
mesotrophic freshwater lakes at temperate latitudes.
PROTOZOA
This is not a clade but it is useful to keep this assemblage for
technical (sampling) and
ecological reasons. They are the most important bacterial
consumers, their biomass is low
(compared to Rotifers and crustacean) but their generation time
is short (between 3 and
13 hours at 20C).
Heterotrophic flagellates
Heterotrophic nanoflagellates are the smallest: 1 15 (or 20?) m,
the most abundant
(105 108 l-1 and even more) and the main consumers by
phagotrophy of free-living
bacteria, picophytoplankton and other (smaller) heterotrophic
nanoflagellates
Large heterotrophic flagellates measure 15 200 m
Main groups of heterotrophic flagellates:
Nonpigmented species of cryptomonads
Nonpigmented species of dinoflagellates (become numerous if pH
decreases)
Nonpigmented species of euglenoids
Nonpigmented species of chysophytes
Choanoflagellates
Kinetoplastids
Chrysomonads
Volvocids
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Zooplankton 5
Chilomonas paramecium
(Cryptomonadine flagellate)
Chilomonas sp
Food uptake
Flagellates mainly feed on bacteria and the smal
igure
lest phytoplankton
F Relationship between pelagic
everal kinds of food uptake can occur:
f small-sized
hy: feeding on larger living or
or sequestrated chloroplasts that continue to
photosynthezise
flagellate size and size range of food
particles (
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Zooplankton 6
A combination of the above mechanisms
Mixotrophy: many flagellates are mixotrophic: they can occur
with chlorophyll and be
n with chlorophyll but being deep into the autotrophic or
without chlorophyll (or eve
water and unable of photosynthetic production) and feed on
bacteria:
Ciliates
Ciliates are larger (8 300 m), less abundant (102 104 l-1); they
are more abundant in
water bodies eutrophic
Paramecium bursaria with
symbiotic zoochlorellae
Paramecium aurelia
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Zooplankton 7
Strombidium (Strombidiidae Oligotrichia
ciliate)
Titinnidae (Titinnidia ciliate)
Main groups of ciliates:
Oligotrichia
Tintinnidia
Haptoridia
Food uptake
Most are heterotrophic and feed on bacteria, picoplankton and
many other microscopic
organisms.
Some ciliates contain chloroplasts from the ingested algae or
symbiotic zoochlorellae,
they are mixotrophic.
A few are considered carnivorous, feeding on other ciliates and
small metazoans
Some ciliates attach themselves to other planktonic organisms,
they are not free-living
but epibionts
Amoeba
Amoeba are normally benthic organisms but are periodically swept
into the water column
Heliozoans
Testate amoeba (can float with lipid globules)
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Zooplankton 8
Amoeba as the ciliates, feed on bacteria and algal picoplankton
and many other
microscopic organisms. Some are considered as predators.
-------------
All Protozoa
Size and shape of prey:
Prey geometry is the first-order determinant of ingestion
through passive mechanical
selection. Large (vs. small) bacteria are preferred (as measured
for example by an
electivity index) and consumed in larger numbers than expected
by chance. See the
chapter Food web interactions
Feeding rates
Orders of magnitude:
10 50 bacteria per individual per hour for the flagellates
30 3000 bacteria per individual per hour for the ciliates
The rate of bacterivory by flagellates is smaller than that of
ciliates but flagellates are so
much more numerous that their grazing effect is much larger
Order of magnitude: in a eutrophic lake ca. 50-70% of the
bacterial production is
consumed by flagellates and 20 % by ciliates; in mesotrophic
lakes the difference is even
higher [other causes of bacterial death: bacteriophage viruses
(and sedimentation?)]
N.B.: Cladocera, Copepoda (even their nauplius larvae) and
Rotifera normally only
feed marginally (or do not feed at all) on bacteria
Therefore the median cell volume of bacteria decreases during
the summer period but
still larger (colonial or filamentous bacteria) can develop (by
size-selective grazing)
Figure Model of microbial
succession B = easy edible
bacteria, HNF =
heterotrophic
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Zooplankton 9
nanoflagellates, GRB = grazing-resistant bacteria (aggregates,
filaments), C = ciliates
(
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Zooplankton 10
in spring and early summer, when the phytoplankton is the most
productive; a secondary
maximum can occur in the autumn.
Example in Lake Constance (German side), a mesotrophic lake.
Figure Seasonal cycle of
heterotrophic nanoflagellates in
Lake Constance, Germany (1990):
for comments, see text hereunder (<
Wetzel fig. 16-4)
The Nanoflagellate numbers are the
lowest in winter and the highest in
late spring, after the phytoplankton
and bacteria peaks (bottom-up
effect: abundance of edible
bacteria). The flagellate biomass
equals five times that of the
bacteria.
The Nanoflagellates are grazed all year round by Ciliates
(Oligotrichia ciliates are the
most efficient grazers). During the spring clearwater phase they
are also grazed heavily
by Rotifera and Cladocera (top-down regulation by predators)
when their mean size is
maximal (up to 20 m); by selective grazing, their mean size
becomes minimal ( 5 m)
towards the end of the clear water phase (the larger ones have
been grazed by Cladocera
and Rotifera)
Speed of swimming:
Ciliates 200 1000 m/s
Flagellates 15 300 m/s
Amoeba 0.5 - 3 m/s
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Zooplankton 11
Life in low oxygen concentrations
Most protozoa are aerobic but some are microaerophilic: they can
live in organically
polluted waters with very low oxygen concentrations [< 1
mg/l] and build up high
densities (because there are also many bacteria). They therefore
have been used as
indicators in saprobic organism indices
- specialized anaerobic ciliates have methanogen symbionts (ex.:
Saprodinium)
- microaerophilic ciliates without symbionts can use NO3 as a
source of oxygen (ex.
Loxodes)
- microaerophilic ciliates with zoochlorellae symbionts can use
CO2 and NH4+ (ex.:
Frontonia)
- microaerophilic ciliates with periodic symbiotic chloroplasts
from ingested algae (ex.:
Strombidium)
In a summer-stratified eutrophic pond, (see figure 23-4 from
Kalff at the beginning of
this chapter) one can find in the epilimnion:
- aerobic obligate planktonic (epilimnetic) protozoans
And deeper
- temporary planktonic (hypolimnetic) protozoans that are
migrants from the sediments
when these are devoid of oxygen: microaerophilic species migrate
to the level where they
meet the best oxygen concentration, which is often linked wit
bacterial abundance
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Zooplankton 12
ROTIFERA
Rotifera are the smallest multicellular planktonic organisms (40
m 2 mm)
Rotifera are pseudocoelomates originating in fresh water [only
two genera and a few
species are marine].
Several hundreds of species are sessile and fixed on sediments
or vegetation and about
100 ubiquitous species are completely planktonic.
Schematic benthic rotifer with a flexible
cuticle
Schematic planktonic rotifer with a lorica, the
foot can be withdrawn within the lorica
There are great morphological variations.
Most have an elongated body covered with a thin and flexible
cuticle, sometimes
thickened and more rigid and then termed lorica. At the anterior
end they wear a corona,
a kind of wheel of cilia allowing locomotion and movement of
food particles toward
the mouth.
The digestive track contains a muscular pharynx, termed the
mastax, with two or more
jaws that crush the ingested food particles.
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Zooplankton 13
The body ends in a foot (in sessile species). The planktonic
species tend to have
suspension devices (spines, setae) and reduce or lose their
foot.
Figure Planktonic rotifers (a: Keratella, b:
Kellicottia, c: the predacious Asplanchna
(not at the right scale), d: Conochilus)
(
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Zooplankton 14
Polyarthra: a planktonic rotifer with
characteristic adjustable spines
Asplanchna a planktonic predacious
rotifer of varying size, with another
rotifer, Keratella, in its stomach
Food and feeding.
Seston particles (picoplankton, flagellates and small ciliates,
generally less than 12 m)
are directed by the corona toward the mouth. Some selection of
food can occur through
rejection mechanisms (even after having been ingested). Transit
time of food in the gut =
3 20 minutes.
Some Rotifera (as Polyarthra) only feeds on algae while others
feed on bacteria, yeast
and algae
There is a reasonable separation of rotifer species along a
food-particle-size gradient
The genus Asplanchna is a predator feeding on algae, rotifers
and small crustaceans
Very fast development and short life-time (~ one month) under
optimal conditions (25C)
Reproduction
Adult parthenogenic amictic females produce up to two dozen of
young and development
from egg to adult is short (one to a few days under favourable
conditions). There is no
distinct larval stage: the young that hatch from an egg already
looks like an adult. Thus
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Zooplankton 15
most rotifers are multivoltine (sometimes more than 20
generations per year and can
become very abundant: often 200 300 (up to 5000 individuals) per
litre.
When conditions become less favourable (return of either the
winter period or the dry
season or overcrowded population), mictic female appear that
produce haploid eggs
developing into males, sexual reproduction occurs with the
mictic females and thick-
walled resting diapausing eggs are produced that can survive
anaeroby, frost and
desiccation. After weeks or months, when the conditions restore,
resting eggs develop
into parthenogenetic females.
Because their fast growth rate and short generation time the
relative production by
Rotifera is always higher than their relative biomass
The most important niche resources are food size, food nature,
time (seasonality), life
histories and depth (tolerance to temperature and oxygen).
Population dynamics
Most Rotifera have wide temperature tolerance and many have
maximal populations in
summer. However, some species are cold stenotherms and are most
abundant in winter
and early spring.
The rotifer community of Lake Constance has been sampled over a
period of more than
50 years (marked by a progressive change from oligotrophic to
mesotrofic conditions).
Rotifera populations gradually increased. Then Daphnia hyalina
became abundant and
the predatory Cyclops vicinus developed. The latter controlled
Daphnia and the rotifers,
including the predatory rotifer Asplanchna. In May Cyclops
enters into diapause and all
rotifers rapidly recover.
Smaller rotifers require less food to reach maximal growth rate
and thus are better
adapted to live in food-poor environments
Competition and predation
Copepoda and large Cladocera prevent the rotifers to become
abundant
Rotifera often dominate early in the annual succession, they
decrease when Cladocera
develop and recover when the Cladocera decrease (eaten by
planktivorous fish).
Larval Chaoborus can feed on rotifers but their impact is
generally not high.
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Zooplankton 16
The predatory rotifer Asplanchna feeds on other rotifers but it
releases a soluble chemical
inducing the development of longer spines in other rotifers
which reduces predation.
In reservoirs with a high load of silt or clay, rotifers can
develop because they are
selective to mineral vs. organic particles (and they will be
favored over crustaceans).
In ancient tropical lakes Rotifers (and protozoans) are favored
by the low density of
crustacean zooplankton and by the fact they are not preyed upon
by fish.
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Zooplankton 17
CRUSTACEA
BRANCHYOPODA (order)
Notostraca, Anostraca and Conchostraca are characteristic
inhabitants of temporary
shallow water bodies. Generally bisexual reproduction and
resistant eggs (resistant to
drought).
Phyllopoda [Cladocera] live as planktonic members of permanent
water bodies
CLADOCERA (sub
order)
Figure Freshwater
Cladocera: a: Daphnia
pulicaria with an
ephippium in her brood
chamber, b: Daphnia
retrocurva, c: Alona bicolor
(littoral species), d:
Bosmina coregoni, e:
Bythotrephes cederstroemii
(predacious species) (<
Wetzel fig. 16-11)
Cladocera have a distinct
head and their body is
covered by a hard chitinous
bivalve carapace
Size between 0.2 and 3 mm.
A large Daphnia = 35 g
The second antennae are used for locomotion and produce a
typical hopping style of
swimming responsible for their common name of water fleas.
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Zooplankton 18
They bear one compound eye
Mouthparts :
- 2 large chitinized mandibles (that grind food particles)
- 2 small maxillules (that push food between the mandibles)
- 1 labrum covering the other mouth parts
Figure Schematic feeding mechanism of Daphnia : for
explanations, see the text
hereunder (< Kalff fig. 23-6)
Most Cladocera are filter-feeders. The five pairs of thoracic
limbs bear setae themselves
covered with setules spaced a few m, these flattened limbs flip
back and forth several
times per second.
The limbs # 1 and # 2 eject large and undesirable particles
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Zooplankton 19
The limbs # 3 and # 4 collect food particles, they comb one
another, food particles and
mucous are shaped into a bolus at the base of the legs, moved
toward the mouth, and
there it is chewed by the mandibles and swallowed (it can also
be rejected). The
postabdominal claw is also used for ejecting undesirable
particles.
The distance between setules varies with species and instar, the
filtering selectivity varies
therefore with species and instar but also with taste and
nutritional quality.
Because the small intersetular spaces and the resulting low
Reynolds number (10-3) a
difference of pressure is needed to make pass water through the
mesh. This occurs in a
closed filtering chamber. Electrostatic forces (e.g. hydrogen
bonds, Van der Waals
forces) are also evoked for explaining that bacteria and algal
cells stick to the long setae
of the legs 3 and 4.
igureF Picture
gs 3
iltering rates
ody
thus
of the le
and 4 of a
Daphnia.
F
are influenced
by b
length and
temperature.
They
vary with
season, sometimes exceeding 100% (of the volume of water
filtered per day); filtering
rates decrease if the dissolved oxygen is below 3 mg/l and no
filtering occurs if the
dissolved oxygen falls below 1 mg/l (think at the problem of
dial vertical migrations).
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Zooplankton 20
Figure Filtering rate increases regularly with body length
(constant food supply at 20C)
and varies in a more complex way with temperature (body length
of 1.75 0.1 mm)
(
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Zooplankton 21
Figure Relationship between
Daphnia hyalina density and its
grazing rate. This is a typical mutual
interference response (
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Zooplankton 22
Toxic algae (mainly cyanobacteria) are sometimes selected
against but some Cladocerans
do not avoid them resulting in a reduction of thoracic beat rate
and thus filtering rate
Figure Some genera are
carnivorous (Polyphemus,
Leptodora) or omnivorous
(Bythotrepes).
Development is fast and the life-
time is short (~ two to three
months) under optimal conditions
(20 25C and plentifull of algae). Longevity in Daphnia magna
varies from 26 days at
28C to 108 days at 8C.
About the same amount is allocated to growth and to
reproduction. However, when food
becomes scarce the relative allocation to reproduction
decreases. Cladocera not only feed
on algae, they are able to feed on bacteria (but they are less
efficient bacteria filters than
the flagellates). Moreover bacterioplankton seems inadequate to
support growth and
reproduction (some bacteria are not digested and remain viable)
but enable them to
survive during algal shortage.
Adult parthenogenic females produce many young (between 1 and 40
per clutch). The
eggs are laid in a dorsal brood chamber and hatch as small forms
of the adults (there are
no free-living larvae). The young are released when the female
molts (this can occur 20
times in its life and they grow a little at each molt.). There
are 2 to 8 predult stages.
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Zooplankton 23
Dapnia pulex with parthenogenetic eggs Dapnia pulex with a
fertilized egg
protected in an ephippium
Thus most Cladocera are multivoltine and can become very
abundant.
When conditions become less favourable (decreasing temperature,
drying of the pond,
short day-length photoperiod, crowding, reduction of food
supply, abundance of
predators), haploid males are produced, sexual reproduction
occur and thick-walled
resting eggs (saddle-shaped ephippia) are produced (only one or
two per female) that can
survive frost and desiccation.
When favourable conditions come back, ephippia hatch into
parthogenetic females, etc.
Population dynamics
Some species are perennial and overwinter as parthenogenetic
females, they can
dominate during the cold period of late winter and early spring
or in the cool
hypolimnetic layers of the lakes.
Most species overwinter as resting eggs (ephippia), they develop
their maximal
population in spring summer and often a second peak in
autumn.
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Zooplankton 24
The spring peak induces such a filtering rate that the Cladocera
can reduce the density of
algae to a low level creating the Clear water phase. They then
decline (food-limited)
and are preyed upon by fish.
In summer, the Cladocera are smaller which is a predator-escape
response (or the result
of selective predation on the largest individuals)
In reservoirs with a high load of silt or clay, most Cladocera
develop slowly or not at all
because of mechanical interference and of reduced algal growth
(shading). Under tropical
climate, this explains the decline of Cladocera during high
water in the rivers
(consequence of rainy season) inundating the nearby lakes.
In ancient tropical lakes crustacean zooplankton is always at a
low density as a
consequence of permanent fish predation (even the herbivorous
Cichlidae, when they are
young, feed on zooplankton), even more than by food limitation
(low nutrient levels).
Riverine vegetation offers shelter where zooplankton can
maintain
Predation
Fish feed preferably on the largest Cladocera
Mysid malacostraceae can also play a role in predation on
Cladocera
Chaoborus is more important as predator in warm countries
The predator Cladocera Leptodora (when they have reached the
size of 6 12 mm)
ingests the fluid of their prey (other Cladocera, nauplius
larvae of Copepoda)
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Zooplankton 25
COPEPODA (order)
Free-living copepoda: Calanoidea (planktonic, female antennae of
23-25 articles),
Cyclopoidea (most benthic, some planktonic, female antennae of 6
- 17 articles) and
Harpacticoidea (littoral benthic, female antennae of 5 9
articles)
Copoepods are covered by a chitinous carapace
The head bears five pairs of appendages
The anterior antennae are used for locomotion and produce a
typical rowing or jerky style
of swimming.
Figure Free-living Copepoda: A: Cyclopoid, B: Calanoid, C:
Harpacticoid. The females
are shown in full, with the antennae of the males and early and
late nauplius stages. (<
Wetzel fig; 16-12
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Zooplankton 26
Cyclops (Cyclopoid copepode) Diaptomus (Calanoid copepode)
The thorax bears six pairs of swimming legs that produce a
regular slow style of
swimming.
Food and feeding.
Harpacticoidea have mouthparts that seize and scrape the biofilm
developing on
sediments and hydrophytes (periphyton).
Cyclopoidea are considered omnivorous and raptorial, they have
mouthparts that seize
the food particles: the maxillules hold and pierce the prey and
force it between the
mandibles. The large genera (Macrocyclops, Acanthocyclops,
Cyclops and Mesocyclops)
are carnivores feeding on small crustaceans, dipteran larvae and
oligochetes. Smaller
genera (Eucyclops, Acanthocyclops, Microcyclops) feed on algae,
including filamentous
species.
Calanoidea exhibit a continuous swimming: actually they propel a
column of water (by
flapping four pair of appendages) from which the second maxillae
capture parcels of
that water, containing food particles that are pushed into the
mouth by the first maxillae.
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Zooplankton 27
Filtering rates (order of magnitude, much lower than in
Cladocera): for Diaptomus spp:
0.3 2.8 ml per animal per day (but up to 12.9 ml per animal per
day from another
source)
This figure, probably wrong, can
be found in several books. The
vortex-like currents were
observed on an individual
maintained in a drop of water,
but it should be different in open
water (< Pinet fig. 9-19a)
This grazing h
been shown to
be rather
selective; the
appendages
function more
like paddles
than filters and
tend to
concentrate the
particles
as
Figure
Diaptomus
development a:
six nauplius
stages, c and d:
five copepodite
stages.
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Zooplankton 28
Reproduction
Copepods always reproduce sexually, after copulation the females
can be recognized
from the egg sack(s) they bear on the first abdominal segment:
two egg sacks in
Cyclopoidea and Harpacticoidea, one egg sack in Calanoidea. They
produce between 1
and 30 eggs per egg sack. The eggs hatch into small
free-swimming nauplii bearing three
pairs of appendages (first and second antennae and mandibles).
There are five or six
nauplius instars followed with five instars known as copepodites
before the last, adult
stage. Therefore their life-time is much longer than those of
the Cladocera. The different
stages can be recognized on basis of the number of appendages
that are present.
Figure Undetermined copepode early
nauplius stage (with three pairs of
appendages: A1, A2 and Md)
Population dynamics
Figure Development of Cyclops
strenuus in a small lake,
Bergstjern, near Oslo, Norway:
there is a midsummer diapause
of a copepodite stage in the
sediment (< Wetzel fig. 16-28)
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Zooplankton 29
Under temperate climates Cyclopoidea exhibit various periods of
diapause (often at egg
and copepodite stages, sometimes also as adult or nauplius). A
resting stage is common in
summer. Diapausing eggs can remain viable for several tens of
years in the sediments.
Therefore it is not always possible to see clear annual cycles
because of generation
overlap. These diapauses are less common in cold climates and
they are not known from
tropical regions.
Development of the univoltine Cyclops
scutifer in Lake vre Heimdalsvatn,
Norway (< Kalff fig. 23-8)
Development of four generations of
Diaptomus reighardi in a beaver pond in
Ontario, Canada (
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Zooplankton 30
There are several generations per year under tropical or
temperate eutrophic conditions
but only one generation per year or even per two or three years
in the arctic oligotrophic
lakes.
Coexistence of several Cyclopoidea in the same lake is explained
by differences in
seasonality, vertical distribution, size and quality of food
particles and selective predation
by fish. Nauplii and young copepodites are more susceptible to
predation, the adults
being able to escape predation by their quick move. This is made
possible by a sudden
flap of the antennae. The acceleration makes shift the Reynolds
number from 0.1
(predominance of viscous forces when the copepod is grazing) to
100 and even more
(predominance of inertia forces) and the copepod jumps over
several mm, enough for
escaping many predators.
The cycles of Calanoidea are closer to those of Cladocera:
resting Diaptomus eggs hatch
in spring Some generations will follow one another until the
production of the next
resting eggs in autumn.
Calanoidea populations may be controlled by Cyclopoidea
predation (rather selectively)
either on their nauplii or on their young copepodites.
Calanoidea often feed also on their
own naplii (cannibalism).
A parasitic fungus can induce a high mortality of the eggs and
female adults.
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Zooplankton 31
MYSIDACEAE (sub-order, order Peracarida)
The opossum shrimps are slender fast-swimming organisms. Without
gills, they are
sensitive to poor oxygen conditions and thus develop mainly in
cold oligotrophic lakes.
The day is spent near the bottom (escaping visually hunting fish
predators) and the night
near the surface filter-feeding on phyto- and zooplankton.
They have been introduced in some lakes for increasing large
particle food availability
for fish. Instead, they sometimes became competitors for young
fish and even predators
for newly hatched fish!
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Zooplankton 32
INSECTA
Chaoborus the phantom midge
The larvae of the non biting midge Chaoborus (Chaoboridae) are
typically planktonic.
Because of the transparency of their larvae, they are called
phantom midges.
The larva has two expansible gas bladders allowing the animal to
move up and down
(they can be targeted by echolocators and allow following their
daily vertical migrations:
up to 200 m).
The first and second instars feed on
nanoplankton, large protozoans and
small crustaceans in the lower depths of
the epilimnion
The third and fourth instars are benthic
during the day and hide in hypoxic
sediments from fish predators (actually
they do not exhibit any diurnal
migrations when planktivorous fish are
absent). At night they feed in the
epilimnion on large rotifers,
intermediate size Daphnids, etc.
-
Zooplankton 33
Figure Chaoborus larva, note raptorial antennae, the gas
bladders (a thoracic one and an
nal segment.
abdominal one) and the swimming paddle under the last abdomi
Figure Chaoborus l
having ing
arva
ested a
ladocera (located under
ke, large Daphnids
cing
d
osquitoes
mosquitoes are not taken into account in the books written by
Kalff and by
c
the thoracic gas bladder)
In an experimental
enclosure of a fishless
la
were removed, redu
competition for food an
allowing the rotifers and small Cladocera to develop.
Consequently Chaoborus could
develop much better than previously (Neil, 1984)
M
The larvae of
Wetzel, probably because they live in the littoral zone (and
never in open water): they are
thus not considered as planktonic organisms.
-
Zooplankton 34
ZOOPLANKTON SYNTHETIC DATA
Sampling of zooplankton
Nets
Nets made of silk bolting cloth (for
sieving flour) [Fr: soie bluter (la
farine); nl: zijde zeef?] were
historically used in the 19th 20th
centuries with the finest mesh
openings available at that time of
60 70 m. This mesh opening is
still used if adult crustaceans are
the target of sampling.
However, small crustacean larvae and most rotifers are smaller
and escape those nets,
therefore smaller mesh openings (35 m and even 10 m) are used
nowadays. The
trouble with such nets is that during horizontal towing or
vertical hauling a backpressure
is produced that allows the best swimmers (copepods) to escape
capture and that prevents
to know the exact volume filtered
Traps
To avoid the previously mentioned flaws, traps have
been developed
The Schindler-Patalas trap (figured) is a transparent
plastic box with two open sides (bottom and
ceiling), it is sunk at a given depth; then a shock
closes all the sides and the trap is hauled up. The
known volume of water collected (10 to 30 litres) is
either filtered through a net or fixed for the analysis
of the protozooplankton
-
Zooplankton 35
Pumps
Water is pumped at a given depth and either filtered through a
net or fixed for the
analysis of the protozooplankton
Echolocators
Echolocation can be used for mapping the zooplankton
distribution but this requires
calibration with one of the previous methods
Patchiness and representativeness of the zooplankton
sampling.
A one-point zooplankton sampling cannot be quantitatively
representative of a body of
water because
- technical problems (mainly appropriate sampling method)
- patchy horizontal and vertical distributions of the
zooplankton
Figure
distribu
Bosmin
obtusir
ladocera) in Lake
23-2)
Spatial
tion of
a
ostris
(C
Latnjajaure, in
September 1968 (< Kalff fig.
Figure Lake Latnjajaure,
Lapland, Sweden: an
oligotrophic alpine arctic
lake (area = 0.73 km,
maximal depth = 17 m).
-
Zooplankton 36
Patchiness of the zooplankton can make vary the density of
zooplankton more than
tenfold from one place to another or at the same point at some
days apart.
This patchiness is determined by the lake depth and shape, by
inflows (and outflows), by
winds and currents (including possible upwellings and Langmuir
circulation), by
competition for food and predation and by vertical and
horizontal migrations.
Prediction of species richness
The first best predictor of species richness is the area of the
lake, explained by the habitat
diversity hypothesis (related to MacArthurs island theory).
Figure Relationship between lake
area and plankton species richness:
either Crustacea from 66 North
American lakes (filled circles) or
Rotifera from 12 lakes from E
and Africa (open circles) (< Kalff
fig. 23-9)
ngland
A second good predictor is
phytoplankton production but the
relation is not linear: zooplankton species richness is low in
highly oligotrophic lakes,
peaks at relatively low primary production and declines at
higher rates (> 180 mg C m-2
yr-1)
The depth of the lake, its pH and the number of fish species
(predators) can also act as
predictors of zooplankton species richness.
Seasonal cycles and clear-water phase
Let us examine what happens in meso- to eutrophic temperate
dimictic lakes (see figure
hereunder).
In the winter phytoplankton is inhibited (by light and
temperature), and zooplankton is
inhibited (by food and temperature). In early spring
phytoplankton develops and
-
Zooplankton 37
consequently small zooplanktonts (Rotifers, bosminids) increase
first (thanks to their
short development time) followed with larger zoplanktonts
(daphnids); the latter
outcompete the former and exhaust the phytoplankton in late
spring (a clear water phase
can be observed); at the same time young-of-the-year fish have
hatched and prey upon
the larger zooplanktonts; these subsequently decline. The second
phytoplankton peak is
due to grazing-resistant algae and cyanobacteria. The second
peak of zooplankton is
made mainly of small species (the larger are still under control
by young fish). In the
autumn the young fish are progressively controlled by
piscivorous fish, decreasing
temperature induces the production of resting eggs.
Figure Model of seasonal variations of zooplankton in eutrophic
and oligotrophic
temperate dimictic lakes: (a) phytoplankton (dashed line), (b)
small zooplankton species
(black) and (c) large zooplankton species (grey). Lower bars
indicate the factors acting on
zooplankton (< Wetzel fig. 16-27).
Large filter-feeding Cladocera, as Daphnia, can bring about or
contribute to a clear-water
phase (transparent water) in the springtime (or early summer).
This is not the only cause,
the other ones are the loss of diatoms by sedimentation when a
thermocline has
established and exhaustion of nutrients in the euphotic
zone.
The clear water phase is clearly related to the density of
Daphnids: for example a
threefold increase in Daphnia biomass is correlated with a 3 m
increase in transparency
in the Saidenbach reservoir.
-
Zooplankton 38
Figure Relationship between
the water transparency and the
Daphnid density in Saidenbach Reservoir near Dresden, Germany;
each point is a
different year (< Kalff fig. 23-18).
Top-down control of zooplankton by fish
If large or medium-sized zooplankton crustaceans are present,
planktivorous fish will
feed on them: for reasons of energy efficiency the predators
consume the largest prey
possible. Vision is therefore essential in detecting prey.
Manipulations of planktivorous fish (removal or addition) have
dramatic direct effects on
zooplankton abundance and indirect effects on phytoplankton and
macrophytes. When
planktivorous fishes are removed, large zooplanktonts develops,
phytoplankton is
reduced, a clear phase establishes and submerged macrophytes can
develop.
The effect of manipulations of planktivorous fish was first
demonstrated experimentally
by Hrbacek (1958, etc.) in Czechoslovakia and has been confirmed
many times by
introduction or removal of the fish or by enclosure experiments.
The planktivorous fish
do not control all the zooplankton but only the large
individuals / species (thus mainly
Daphnids and invertebrate predators) and produce a change in the
zooplankton
community composition. Therefore the size distribution of
macrozooplankton is
sometimes used as a surrogate of the fish community structure
(zooplanktivorous versus
piscivorous species). If zooplanktivorous fish are removed,
predacious crustaceans and
-
Zooplankton 39
Chaoborus develop and feed on smaller zooplankton thus large
zooplankton species can
dominate the zooplankton community.
Figure Impact of
the introduction
of Alosa a
(a planktivoro
fish all its life
long) in Lake
Crystal,
Connecticut:
reduction in size
of the grazers and
invertebrate
predators and
change of their
species
composition (<
Kalff fig. 23-15)
estivalis
us
Figure: Relationship between the
YOY (young of the year) roach
(Rutilus rutilus) density and
Daphnia abundance in a small
English lake (< Kalff fig. 23-13).
-
Zooplankton 40
Figure Mean biomass of the April-
September period for PHY:
phytoplankton, PIC: picoalgae,
BAC: bacteria, HNF: heterotroph
nanoflagellates, MIC:
microzooplankton, MAZ:
macrozooplankton in duplicate
enclosures with and without
planktivorous fish (< Kalff fig. 23-
17).
Invertebrate predators and competitors (for the Daphnids)
Predacious Cladocerans (Leptodora, Bythotrephes), shrimps (Mysis
relicta), Cyclopoid
Copepods and / or insect larvae (Chaoborus) tend to reduce the
number of Daphnids.
Filter-feeding molluscs (Dreissena) also increase the water
clarity and reduce the food
available for the filter-feeding macrozooplankton: the
introduction of the zebra mussel
(Dreissena) reduced the phytoplankton by by 85% in an American
lake.
-
Zooplankton 41
Diel vertical migrations
There is a conspicuous synchronized periodical migration,
downward at sunrise and
upward at sunset. This concerns mainly crustacean plankton and a
depth between 1 and
50 m
Figure Model of diel vertical migration of the zooplankton (
-
Zooplankton 42
Figure Hardy and Bainbridge Perspex plankton wheel in horizontal
position: the
organisms can be introduced through three little doors (<
Tait )
The ultimate (adaptive) explanation seems to be linked with (a)
predator avoidance
and/or (b) energy saving.
Predator avoidance hypothesis: if the planktonts spend the
daytime in deep, dark water,
they will be less accessible to visual predators and will
experience less predation.
Energy saving hypothesis: if the planktonts spend a part of the
day in deep, cool water,
their respiration intensity will decrease and they will spend
less energy that can be
allowed to more reproduction [consequently their growth speed
can strongly be reduced,
by 50-60%]
Figure The midday and midnight
vertical distribution (in %) of Cyclops abyssorum in Lake
Porskie (with fish) and Lake
Czarny nad Morskim (without fish), both in the Tatra mountains,
Poland (
-
Zooplankton 43
A quality-of-food argument has also been proposed: during
daytime the algae synthesize
mainly carbohydrates and during nighttime proteins; therefore
acquiring food at night
might be more interesting, at least at low food density
Experimental evidence (at the Max-Planck Institute): in an
aquarium of 11 m height and
1 m diameter, with natural profiles of light and temperature
(thermocline at 4 m depth).
(1) Three Daphnia species were introduced and their movements
were recorded: they
migrated daily on a height of 1 to 3 m (within the epilimnion).
(2) Water with fish
kairomones was injected in the aquarium: the amplitude of the
migrations increased and
two out of the three species daily crossed the thermocline and
spent the daytime in the
cold hypolimnion, the third Daphnia species is a macrotherm
species. (3) Some young
fish were introduced, there was no change in the diel migrations
but after 30 days the
macrotherm Daphnia species was eliminated totally.
In open water (without littoral vegetation), most plankton
crustacean migrate away from
the shore. The cue of this avoidance of shore is the elevation
of the horizon and the
position of the sun. Young fish (most of them feeding on
zooplankton) tend to stay close
to the shore, avoiding predation by larger fish
Horizontal migrations also occur in shallow water bodies with
fish: aggregation in plant
beds during daytime and migration towards the open water during
nighttime.
Rotifers exhibit some migratory movement but it is not as clear
as for the crustaceans.
Ciliary locomotion and the small size of the rotifers (low
Reynolds number) would make
these migrations very costly in energy. Moreover their small
size makes them
inconspicuous for fish
N.b.: some motile flagellate algae also migrate, but downward
during darkness (escaping
high predation pressure) and upward during day (necessary for
photosynthesis)
-
Zooplankton 44
Cyclomorphosis
Cyclomorphosis is the seasonal change in the morphology of
successive generations
(Lauterborn, 1904). It is mentioned for Cladocera, Rotifera,
Protozoa and Dinoflagellates.
Changes in head shape, length of spines, etc. are linked with
temperature, food, light,
turbulence and soluble organic matter (kairomones).
These changes (increased or decreased surface) can affect the
sinking rate and oxygen
uptake, but the best explanation seems to be that longer spines
or an elongate body make
the prey more difficult to be handled by predators.
Rotifera. The large spines developed by the rotifer Brachionus
definitely decrease
predation by the rotifer Asplanchna spp but are inefficient
against copepods.
Figure Change in spine morphology of the rotifer
Brachionus calyciflorus, induced by the
kairomones released by its predator (the rotifer
Asplanchna) (< Wetzel fig 16-37)
Cladocera. From spring to summer, the successive generations
exhibit a gradual
extension of the head forming a crest.
-
Zooplankton 45
Figure Cyclomorphosis of Daphnia cucullata from Esrom S, Denmark
(Hutchison,
1967), and Daphnia retrocurva from Lake Bantam, Connecticut
(Brooks, 1946) (<
Wetzel fig. 16-38).
Temperature has been demonstrated experimentally to be the main
primary stimulus of
these changes (this anticipates the hatching of young fish).
Accordingly there is no cyclomorphosis in Cladocera under
tropical conditions.
Copepoda. No or few cyclomorphosis: summer individuals tend to
be smaller than the
individuals from colder seasons
Biomanipulation and lake management
Knowing the filter-feeding efficiency of the Daphnids and the
top-down control of fish
on those Daphnids the elimination of planktivorous fish has been
proposed as a useful
management tool for increasing water transparency in ponds where
the reduction of
nutrient concentration is difficult to control.
Actually biomanipulation can be efficient in small shallow
ponds. However, it must be
sustained and therefore it can be expensive. The result can,
however, be uncertain
-
Zooplankton 46
because of the variability of fish reproduction and mainly the
young-of-the-year fish (the
most planktivorous). Biomanipulation can also fail by the
replacement of the edible algae
by large inedible algae and cyanobacteria.
Biomanipulation will become efficient if it is coupled with a
substantial nutrient
reduction (< 50-100 g total P l-1)
Other biomanipulation tend to increase the amount of large food
items available to young
Salmonids, but sometimes with unexpected and unwanted results.
Mysis relicta has been
introduced in several lakes: this species are omnivorous, can
feed either on algae or on
Cladocera and they obviously prefer the latter when available
and thus reduce the
populations of Daphnids. Therefore, their introduction sometimes
creates one step more
in the food chain thus leaving finally less food for the top
predators. So the result was in
some cases a reduction in fish production!
Long-term variation in zooplankton abundance
An extensive study of Lake Windermere (UK) (biweekly planktonic
crustacean sampling
from 1940 to 1980) shows (a) a biomass increase in the 1970s,
attributed to
eutrophication (b) a 10-year cycle linked with the North
Atlantic Oscillation and (c) low
summer macrozooplankton biomass after a warm June (associated
with an early
stratification and a more rapid exhaustion of nutrients in the
epilimnion). However,
eutrophication and climate explained only 35% of the
year-to-year variation; an extra
6.5% were explained by the year-class strength of the perch
(Perca fluviatils), the
dominant planktivorous fish (when young). Thus more than 50% of
the variation
remained unexplained.
-
Zooplankton 47
Figure Long-term
fluctuation of zooplankton
in the north basin of Lake
Windermere. In 1976 the
perch population was
dramatically depleted by a
fungal disease (
-
Zooplankton 48
N = number of filtering individuals (individuals)
The filtering rate increases with temperature to an optimum and
then decreases sharply
(Horn, 1981, this has been illustrated for the Clacocera). The
mass-specific filtering rate
(= F per unit biomass) declines with the size of the
organism.
Many filtering rates are measured in the lab under artificial
conditions which may result
in unknown errors. Better measurements are made with the
Haney-in-situ-grazing-
chamber, a kind of Schindler-Patalas trap enclosing the
macrozooplankton individuals
and their food. Then some radio-labelled cells are injected into
the chamber, after some
minutes of feeding (before the ingested marked cells could be
defecated), the chamber is
hauled, the water filtered and the radioactivity in the water
and in the macrozooplankton
individuals is measured. This allows calculation of the
filtering rate; however, providing
highly palatable particles of the optimal size can also
overestimate the filtering rate! Thus
the same chamber can be used and studied by the changing
abundance over time of algae.
The grazing rate or ingestion rate is calculated as
2
0 tCCFG+=
It is generally expressed in terms of energy content, carbon
content and wet or dry mass
Most studies have shown that the grazing rates range between 2
and 25% day-1 (100% =
the total amount of chlorophyll in the algal community)
Figure Distribution frequency of
grazing rates by
macrozooplankton, provided by
369 publications from various
geographical origins (and o
by different methods). Over 50%
of the papers quote a grazing rate
< 25% per day (
-
Zooplankton 49
The gross growth efficiency (= 100 x G / growth) of
macrozooplankton generally varies
s have higher relative metabolic rates (per unit
r
Filtering rate (ml h-1) Preferred particle size (m)
between 15 and 30% (Winberg, 1972)
It is a general rule that smaller organism
biomass). Thus according to their biomass the effect on nutrient
recycling follows this
order: protozoa > rotifers and small crustaceans > large
crustaceans > young-of-the-yea
fish > zooplanktivorous adult fish
Table from Brnmark
Filterer
Rotifera 0.02 0.11 0.5 18
Calanoidea 2.4 21.6 5 15
Small Daphnia 1.0 7.6 1 24
Large Daphnia 31 1 47
Zooplankton production
ade during the 1960s and 1970s in the IBP (International
here PR = Production
e end of time interval
l
e interval
l
l
lculated by life instar or by
of continuous reproduction the most used method uses the
turn-over time Tt
Most measurements were m
Biological Program). In case there is neither recruitment nor
mortality
000 NMNMBBP tttR == W
Bt = biomass at th
B0 = biomass at the begin of time interva
Mt = mass of an individual at the end of tim
M0 = mass of an individual at the begin of time interva
Nt = individual number at the end of time interval
N0 = individual number at the begin of time interva
If cohorts can be recognized (as in copepods) this must be
ca
cohort
In case
required for a population biomass to replace itself (P/B)
BTP tR =
-
Zooplankton 50
Production methodologies and measurements are not very reliable:
using the same data
roduction can be deduced from a multiple regression model based
on a metastudy on
Figure
gathered on a single Daphnia population, the computed production
can range from 13 to
51 g DM m-2 yr-1 (Andrew, 1983)
P
137 populations (zooplankton, benthic insects, annelids and
molluscs) (Plante &
Downing, 1989):
Relationship
te
us
f
by
if
5
here
DM m-2)
g DM)
between
invertebra
biomass and
production
(plankton pl
benthos): 63% o
the variation in
production is
accounted for
the biomass, 79%
).
Log(P) = 0.06 + 0.79 log(B) 0.16 log (M
temperature is added in a multifactorial regression (< Kalff
fig. 23-2
M) + 0.05 T
R2 = 0.79, F = 165, p
-
Zooplankton 51
Figure Duration of embryonic
fera
t
ooplankton lipids
mulate lipids (up to 60% of their dry mass!) originated from
their
:
utrient cycling - stoechiometry
a top-down control on their food but also a bottom-
n the
se
development in planktonic Roti
and Crustacea: the smallest the fastes
(< Kalff fig. 23-7) $
Z
Zooplankton can accu
diet. These lipids are mainly energy reserves [and help the
animals float?]. However, the
essential fatty acid (polyunsaturated fatty acids or PUFA)
contents of the phytoplankton
can limit (or stimulate) the zooplankton growth (and this is
true for fish also). The lipid
content decreases from spring to summer and increases again in
late summer and autumn
this mirrors the availability of those fatty acids in
phytoplankton
N
Predators of algae not only produce
up effect through the recycling of nutrients which stimulates
the algal growth.
Herbivore predators have lower and less variable C/N/P
protoplasmic ratios tha
phytoplanktonic organisms. These predators thus will retain the
phosphorus and relea
some nitrogen and a large part of the carbon (respiration) and
they will produce still
higher C/N/P ratios in their faeces and urine.
-
Zooplankton 52
Among the Cladocera Daphnia has a high phosphorus demand and can
be limited (in
p
her
n the other hand zooplankton predators have C/N/P ratios very
close to those of their
oligotrophic lakes) not by the food quantity and energy but by
phosphorus. Daphnia sp
thus have low N/P ratios (~ 14/1 by atoms): they dominate in
eutrophic water bodies with
low seston ratio N/P. In contrast N/P is higher in Calanoid
copepods (30 50/1 by
atoms): they are proportionally more common in oligotrophic
water bodies with hig
seston ratio N/P.
O
prey thus predators of zooplankton recycle the nutrients with
better C/N/P ratios