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.

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

Zooplankton 3

nanoflagellates (HNF) have not been drawn; mention that their abundance scale is 105

times narrower than the scales for the ciliates (

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

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 (

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

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)

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

Zooplankton 9

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

(

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

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

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.

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)

(

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

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.

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.

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.

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

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).

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)

(

Zooplankton 21

Figure Relationship between

Daphnia hyalina density and its

grazing rate. This is a typical mutual

interference response (

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.

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.

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)

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

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.

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.

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)

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 (

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.

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

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