Zooplankton

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

Academic Press

river ecosystems

Elsevier

Jacob Kalff

Limnology: inland
water ecosystems

Prentice Hall

798-0-12-744760-5
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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.

Zooplankton

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

Zooplankton

nanoflagellates (HNF) have not been drawn; mention that their abundance scale is 105
times narrower than the scales for the ciliates (<Kalff fig. 23-4).
For several reasons the unicellular protozoa will be considered apart and called
protozooplankton vs. zooplankton for the multicellular zooplanktonic organisms

Figure In
comparison with
the sea, the
freshwater holozooplankton
diversity is
characterized by
the abundance of
Rotifera (1:
Asplanchna, 2:
Keratella, 3:
Polyarthra, 4:
Filinia, 5:
Kellicottia, 6:
colony of
Conochilus) and
Cladocera (7:
Ceriodaphnia, 8:
Daphnia, 9: Bosmina, 10: Chydorus) and by the relative rarity of Copepoda (11 & 12:
Cyclopoid copepod Cyclops nauplius & female, 13: Calanoid copepod Diaptomus). The
mero-zooplankton is not very diverse (14: Harpacticoid copepod Canthocamptus, 15:
Ostracoda Cypridopsis, 16: Mysidaceae Mysis, 17: Branchiopoda Eubranchipus and
Insecta larvae: 18: Anopheles, 19: Culex, 20: Chaoborus) (< Kalff, fig 23-3, but items 1820 added from figures of the Internet).

Zooplankton

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

Zooplankton

Chilomonas paramecium

Chilomonas sp

(Cryptomonadine flagellate)
Food uptake
Flagellates mainly feed on bacteria and the smallest phytoplankton
Figure Relationship between pelagic
flagellate size and size range of food
particles (<Wetzel, part of fig.16-5)
Several kinds of food uptake can occur:
Osmotrophy: uptake of dissolved organic
compounds
Pinocytosis: uptake of small-sized
particles
Phagotrophy: feeding on larger living or
dead particles via a cytosome (mouth)
Metabolic exchanges with endosymbionts or sequestrated chloroplasts that continue to
photosynthezise

Zooplankton

A combination of the above mechanisms

Mixotrophy: many flagellates are mixotrophic: they can occur with chlorophyll and be
autotrophic or without chlorophyll (or even with chlorophyll but being deep into the
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
eutrophic water bodies

Paramecium aurelia

Paramecium bursaria with

symbiotic zoochlorellae

Zooplankton

Strombidium (Strombidiidae Oligotrichia

Titinnidae (Titinnidia ciliate)

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)

Zooplankton

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

Zooplankton

nanoflagellates, GRB = grazing-resistant bacteria (aggregates, filaments), C = ciliates

(<Wetzel fig. 16-6)

The microbial loop

A major portion of the pelagic metabolism occurs within a microbial food web. The socalled microbial loop is a model of C, N, P cycling through microbial components
(<5m).
DOM (dissolved organic matter) and POM (particulate organic matter) enter into the
freshwater bodies mainly from littoral and allochtonous sources. More than 50% of it is
metabolized by bacteria to gases, nutrients and bacterial biomass, which in turn is fed up
by flagellates and ciliates

Figure Model
of nutrient
cycling
emphasizing
the microbial
loop, only
organisms >5
m can be
consumed by
the higher organisms (Rotifera, Cladocera) (<Wetzel fig. 16-8, partim). The
surrounding ecosystem feeds the system with DOM and POM.

Seasonal dynamics
In oligotrophic lakes, there are few and unpredictable seasonal variations, especially for
the flagellates, regulated by the abundance of available bacteria.
In more productive lakes, abundance of bacteria allows the development of protozoa
populations and regulation mostly occurs through predation. Ciliates are more abundant

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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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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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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 Schematic planktonic rotifer with a lorica, the
cuticle

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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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)
(<Wetzel fig. 16-9, partim)

Kellicottia: a planktonic rotifer with its lorica

Keratella: a planktonic rotifer with a

characteristically extended in long spines

characteristic lorica)

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14

Polyarthra: a planktonic rotifer with

Asplanchna a planktonic predacious

characteristic adjustable spines

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

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 thickwalled 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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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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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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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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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.
Figure Picture
of the legs 3
and 4 of a
Daphnia.
Filtering rates
are influenced
by body
length and
temperature.
They thus
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).

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)
(<Wetzel fig. 16-13)

Figure Filtering rate decreases (but ingestion rate increases) with increasing particle
concentration. For Daphnia pulex the ingestion rate of Stichococcus (small cells of 5 m
long) is drawn X 0.1 (<Wetzel fig. 16-16).

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21

Figure Relationship between

Daphnia hyalina density and its
grazing rate. This is a typical mutual
interference response (<Kalff fig. 2321).

Filtering rates (order of magnitude):

Daphnia spp 0.7 1.7 mm: 3;6 6.4 ml per animal per day
Bosmina spp 0.4 0.6 mm : 0.4 0.6 ml per animal per day

Figure Bosmina longirostris: a

small (0.5 mm long) filter feeder,
its gut is filled with green algae
Selective feeding can modify the
equilibrium within the algal
community.
If algae with thick walls (as
Scenedesmus and Stichococcus) are ingested without being crushed (by the mandibles)
they pass through the gut intact without being assimilated and they remain viable.
Feeding on algae of course decreases the algal population but simultaneously (through
the release of nutrients) it increases algal productivity.

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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 lifetime 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.

Zooplankton

Dapnia pulex with parthenogenetic eggs

23

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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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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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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Cyclops (Cyclopoid copepode)

26

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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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 has
been shown to
be rather
selective; the
appendages
function more
like paddles
than filters and
tend to
concentrate the
particles
Figure
Diaptomus
development a:
six nauplius
stages, c and d:
five copepodite
stages.

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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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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

Development of four generations of

scutifer in Lake vre Heimdalsvatn,

Diaptomus reighardi in a beaver pond in

Norway (< Kalff fig. 23-8)

Ontario, Canada (<Wetzel fig. 16-31)

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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.

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!

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
abdominal one) and the swimming paddle under the last abdominal segment.
Figure Chaoborus larva
having ingested a
cladocera (located under
the thoracic gas bladder)
In an experimental
enclosure of a fishless
lake, large Daphnids
were removed, reducing
competition for food and
allowing the rotifers and small Cladocera to develop. Consequently Chaoborus could
develop much better than previously (Neil, 1984)

Mosquitoes
The larvae of mosquitoes are not taken into account in the books written by Kalff and by
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 Spatial
distribution of
Bosmina
obtusirostris
(Cladocera) in Lake
Latnjajaure, in
September 1968 (< Kalff fig.
23-2)

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 England
and Africa (open circles) (< Kalff
fig. 23-9)
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 aestivalis
(a planktivorous
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)

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 AprilSeptember 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. 2317).

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 (<Tait fig. 4-8).
These diel migrations of the zooplancton occur as well in lakes as in the sea.
Anesthetized Daphnia galeata sinks passively at a speed of 3.6 (small individuals) to
14.4 (large individuals) m/h
The stimulus that triggers these migrations seems clearly be light intensity. The plankton
wheel of Hardy and Bainbridge decisively demonstrated the role of light. In a horizontal
position, the wheel is filled with water and some cladocerans are introduced into the
wheel, then it is put in a vertical position where it can slowly rotate: with a source of light
(or without any source of light) it is possible to make migrate the plankton for hours in a
kind of infinite column of water, downwards (or upwards).

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 (<Kalff fig. 2326).
The facts (a) that migrations also occur in the tropics [few temperature change with
depth] (b) that the migration amplitude increases when predators are present [fish or
Chaoborus, release of kairomones], (c) that the migration amplitude is larger in lakes
with long-established fish populations than in lakes with recently introduced
planktivorous fish and (d) that the migration amplitude is larger in more transparent
lakes, all this gives more strength to the predator avoidance hypothesis (but the energy
saving hypothesis is not abandoned).

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

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

45

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 (<Kalff fig.
23-14).

Zooplankton feeding
The filtering rate or clearance rate is calculated from the volume of water cleansed by an
individual:
F=

ln(C 0 ) ln(C t ) W
t
N

Where F = filtering rate (ml individual-1 h-1)

C0 = initial concentration of planktonic cells (# ml-1)
Ct = final concentration of planktonic cells (# ml-1)
T = duration of experiment (h)
W = water volume (ml)

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-grazingchamber, 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
G=F

C0 + Ct
2

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 obtained
by different methods). Over 50%
of the papers quote a grazing rate
< 25% per day (<Kalff fig. 23-22).

Zooplankton

49

The gross growth efficiency (= 100 x G / growth) of macrozooplankton generally varies

between 15 and 30% (Winberg, 1972)
It is a general rule that smaller organisms have higher relative metabolic rates (per unit
biomass). Thus according to their biomass the effect on nutrient recycling follows this
order: protozoa > rotifers and small crustaceans > large crustaceans > young-of-the-year
fish > zooplanktivorous adult fish
Table from Brnmark
Filtering rate (ml h-1)

Filterer

Preferred particle size (m)

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
Most measurements were made during the 1960s and 1970s in the IBP (International
Biological Program). In case there is neither recruitment nor mortality
PR = Bt B0 = M t N t M 0 N 0
Where PR = Production
Bt = biomass at the end of time interval
B0 = biomass at the begin of time interval
Mt = mass of an individual at the end of time interval
M0 = mass of an individual at the begin of time interval
Nt = individual number at the end of time interval
N0 = individual number at the begin of time interval
If cohorts can be recognized (as in copepods) this must be calculated by life instar or by
cohort
In case of continuous reproduction the most used method uses the turn-over time Tt
required for a population biomass to replace itself (P/B)
PR = Tt B

Zooplankton

50

Production methodologies and measurements are not very reliable: using the same data
gathered on a single Daphnia population, the computed production can range from 13 to
51 g DM m-2 yr-1 (Andrew, 1983)
Production can be deduced from a multiple regression model based on a metastudy on
137 populations (zooplankton, benthic insects, annelids and molluscs) (Plante &
Downing, 1989):
Figure Relationship
between
invertebrate
biomass and
production
(plankton plus
benthos): 63% of
the variation in
production is
accounted for by
the biomass, 79% if
temperature is added in a multifactorial regression (< Kalff fig. 23-25).
Log(P) = 0.06 + 0.79 log(B) 0.16 log (MM) + 0.05 T
R2 = 0.79, F = 165, p<0.001, n = 137
Where P = annual production (g DM m-2 yr-1)
B = mean annual population biomass (g DM m-2)
MM = maximal individual mass of the organism (mg DM)
T = water annual mean temperature

Zooplankton

51

Figure Duration of embryonic

development in planktonic Rotifera
and Crustacea: the smallest the fastest
(< Kalff fig. 23-7) $

Zooplankton lipids
Zooplankton can accumulate lipids (up to 60% of their dry mass!) originated from their
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

Nutrient cycling - stoechiometry

Predators of algae not only produce a top-down control on their food but also a bottomup effect through the recycling of nutrients which stimulates the algal growth.
Herbivore predators have lower and less variable C/N/P protoplasmic ratios than the
phytoplanktonic organisms. These predators thus will retain the phosphorus and release
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
oligotrophic lakes) not by the food quantity and energy but by phosphorus. Daphnia spp
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 higher
seston ratio N/P.
On the other hand zooplankton predators have C/N/P ratios very close to those of their
prey thus predators of zooplankton recycle the nutrients with better C/N/P ratios