on the different nature of top-down and bottom-up … 2002.pdfon the different nature of top-down...

On the different nature of top-down and bottom-upeffects in pelagic food webs

Z. MACIEJ GLIWICZ

Department of Hydrobiology, University of Warsaw, Warsaw, Poland

SUMMARY

1. Each individual planktonic plant or animal is exposed to the hazards of starvation and

risk of predation, and each planktonic population is under the control of resource

limitation from the bottom up (growth and reproduction) and by predation from the top

down (mortality). While the bottom-up and top-down impacts are traditionally conceived

as compatible with each other, field population-density data on two coexisting Daphnia

species suggest that the nature of the two impacts is different. Rates of change, such as the

rate of individual body growth, rate of reproduction, and each species’ population growth

rate, are controlled from the bottom up. State variables, such as biomass, individual body

size and population density, are controlled from the top down and are fixed at a specific

level regardless of the rate at which they are produced.

2. According to the theory of functional responses, carnivorous and herbivorous predators

react to prey density rather than to the rate at which prey are produced or reproduced. The

predator’s feeding rate (and thus the magnitude of its effect on prey density) should hence

be regarded as a functional response to increasing resource concentration.

3. The disparity between the bottom-up and top-down effects is also apparent in

individual decision making, where a choice must be made between accepting the hazards

of hunger and the risks of predation (lost calories versus loss of life).

4. As long as top-down forces are effective, the disparity with bottom-up effects seems

evident. In the absence of predation, however, all efforts of an individual become

subordinate to the competition for resources. Biomass becomes limited from the bottom up

as soon as the density of a superior competitor has increased to the carrying capacity of a

given habitat. Such a shift in the importance of bottom-up control can be seen in

zooplankton in habitats from which fish have been excluded.

Keywords: biomanipulation, bottom-up, Daphnia, fish feeding, food web

Introduction

One of the most fundamental questions in the early

days of zooplankton studies, centred on the relative

importance of competition and predation. The two

factors used to be looked on as mutually exclusive, so

the question was often asked in a conclusive way as to

whether zooplankton abundance would be controlled

by the limitation of growth and reproduction as a

result of short food supply or by enhanced mortality

through predation. These contrasting views were

most apparent between those plankton ecologists

involved in the International Biological Program

focussing on productivity, and those taking a more

evolutionary approach, mostly ‘Hutchinson’s stu-

dents’ who had been inspired by Ivlev’s (1955, 1961)

book on the ‘Experimental ecology of the feeding of fishes’

and Hrbacek’s (1962) paper on ‘zooplankton in relation

to the fish stock’.

However, the opposing views soon started to be

reconciled. An important impetus came from

Hrbacek’s (1962) fishpond observations, which were

Correspondence: Z. Maciej Gliwicz, Department of Hydrobiol-

ogy, University of Warsaw, Warsaw, 02-097 Warsaw, Poland.

E-mail: [email protected]

Freshwater Biology (2002) 47, 2296–2312

2296 � 2002 Blackwell Science Ltd

expanded to lake zooplankton by Brooks & Dodson

(1965) and formalised as the ‘size-efficiency hypothesis’.

Although the spirit of the confrontation was still much

alive at the Dartmouth College workshop on the

‘Evolution and ecology of zooplankton communities’ in

1979 (Kerfoot, 1980), the gap between the food and

predation explanations was being closed. Eventually,

the two approaches were combined successfully, as

reflected by publications such as the ‘Effects of food

availability and fish predation’ (Vanni, 1987) and the

‘Relative importance of food limitation and predation’

(Lampert, 1988).

Two decades after the pioneering papers by Hrbacek

(1962) and Brooks & Dodson (1965), the importance of

both food limitation and predation had been widely

accepted by zooplankton ecologists working at both

the community (Fig. 1a) and population level (Fig. 1b).

Thus, the abundance and specific structure of

zooplankton communities has been perceived as being

controlled from both the top down and the bottom up:

by predation, because of species-specific vulnerability

to predators such as planktivorous fish, and by food

levels, because of species-specific efficiency in food

utilisation (Fig. 1a). The density and age structure of

the population would be controlled by predation

because of different age-specific mortality, and by

food levels because of different body-size-dependent

abilities to utilise food (Fig. 1b).

The notion of combined predation and food limita-

tion effects had implications for the way commu-

nity and population structure would be viewed.

According to McQueen et al. (1989) and their ‘bot-

tom-up: top-down theory’, the ‘trophic level biomass

control is determined by the combined impacts of predation

and energy availability’. According to Lampert (1988),

the population density of Daphnia species would be

determined by the combined impacts ‘of food limitation

and predation’. This view has been imprinted in our

minds, and similar reasoning has been commonplace

in recent publications on zooplankton communities

and populations (e.g. Sommer, 1989; Lampert &

Sommer, 1997).

The same reasoning was introduced into the study

of individual life histories and behaviour, and could

often be found in depictions of life in pelagial zones as

‘life between the never-ending…hazards of starvation and

risks to predation’ (e.g. Gliwicz, 2001). The parity of

top-down and bottom-up impacts on behavioural and

life-history traits, especially body size at first repro-

duction, has become a key assumption in studies on

the costs of antipredator defences in zooplankton and

fish (Fig. 1c): the life history and behaviour of an

individual is assumed to be controlled by predation,

because of body-size-specific vulnerability to size-

selective predators such as planktivorous fish, and by

food levels, because of body-size dependent abilities

to compete for food (food-threshold concentration).

Besides being the two most evident factors of natural

selection, the top-down and the bottom-up impacts

also seem equally important for the selection of an

appropriate phenotype among a range of phenotypes

available within a plastic genotype.

Body-size dependentvulnerability

Energy-transfer efficiencyand body-size-related superiorityin resource

competition

PREDATION

ZOOPLANKTON ABUNDANCEAND COMMUNITY STRUCTURE

FOOD LIMITATION

Body-size dependentpredation risk

Body-size dependentfood-threshold concentration

INDIVIDUAL LIFE HISTORYAND BEHAVIUOR

PREDATION

FOOD LIMITATION

Mortality

Reproduction

PREDATION

POPULATION DENSITY

FOOD LIMITATION

(a) (b) (c)

Fig. 1 Diagrammatic representation of the parity of bottom-up (food limitation) and top-down impacts (predation) on zooplank-

ton abundance and community structure (a), population density and age structure (b), and individual behaviour and life histories (c).

Top-down versus bottom-up effects 2297

� 2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312

The concept depicted in Fig. 1 now appears to be

widely accepted, whether at the community, popula-

tion or individual level. Inherent in it is the tacit

assumption that the nature of the two impacts is the

same with only the direction, down or up, differing

(see Reynolds, 1994; Drenner & Hambright, 1999;

Carpenter et al. 2001; Benndorf, 2002; McQueen et al.

2001). For two reasons, however, this assumption is

incorrect. The first reason is that top-down and

bottom-up forces affect differently the behaviour of

an individual animal (e.g. a Daphnia or a fish), which

trade off increased safety against decreased feeding

rates. The second reason is less apparent and has been

largely overlooked in the top-down versus bottom-up

debate. It relates to the fact that rates (e.g. growth

rates) are controlled from the bottom-up whereas state

variables (e.g. density) at both the population and

community level are controlled from the top-down.

The importance of this fundamental difference has

emerged from recent field studies on fish behaviour in

an experimental biomanipulated lake, and on the role

of prey abundance in prey selectivity in planktivorous

fish. It is further supported by comparisons of zoo-

plankton communities in the presence and absence of

fish. These points are discussed in detail in the

following sections.

An individual’s and a population’s perspective

We know intuitively that risking life is different from

risking hunger. The risk of becoming subject to

predation may become lethal within seconds, while

the risk of starvation may persist for days or weeks

with future compensation always being possible.

Compensation might be readily achieved as soon as

food levels have increased, as an effect of animals

refraining from intense feeding in food-proficient but

predation-risky areas. The possibility of compensation

might account for the difficulty in devising a common

currency for life-history or behavioural decisions when

considering both the risk of predation and the hazards

of starvation. The major difference between the two is

in the likelihood of a mistake becoming fatal. It is high

in the case of predation, but many mistakes in regard

to food limitation could be allowed within an individ-

ual’s life span (McNamara & Houston, 1986; Lima,

1998). This difference may be the reason why beha-

vioural responses to increased predation risk tend to

be stronger than those to decreased food levels.

Following the pioneering work by Werner &

Gilliam (1984) on size-structured fish populations,

the two disparate quantities have often been com-

pared successfully when they were converted to the

common currency of fitness. Dynamic modelling of

state-dependent decision-making under the risk of

predation has been successfully developed to tackle

the problem of the relative importance of top-down

and bottom-up impacts for animal behaviour, espe-

cially in fish and zooplankton (Mangel & Clark, 1988).

However, the common currency of fitness has not

solved the problem that the nature of top-down and

bottom-up effects is different. While feeding rate,

individual growth rate and reproductive potential

may all be assessed in energy units, predation risk can

only be asserted as a probability in regard to the sole

undivided life of an individual that can either be alive

or dead.

For an individual, satiation can take any value

between 0 and 100%. Long periods with an empty

gut (zero satiation) can be compensated for in future

when food levels increase again. However, at the

individual’s level, survival can never be lower than

100%. Therefore, the hazards of starvation and the

risk of predation cannot be compared with a

common currency, for instance as a per cent increase

in feeding rate and risk of predation. This obvious

incompatibility might be the reason why the dispar-

ity has never been ignored at the level of the

individual.

The situation is different at the population and

community level, because mortality and reproduction

readily combine with each other. The common

currency is the individual. The effect of food limita-

tion is reflected in the birth rate, b, and the effect of

predation in the death rate, d, the two merging into

the intrinsic rate of population-density increase

(r ¼ b ) d). For this reason, the ‘sandwich’ or

‘squeeze-in’ idea of full symmetry between top-

down and bottom-up impacts (Fig. 1) has been

approved so readily for the population and com-

munity level.

However, the illusion of full symmetry at the

population level is revealed as soon as it is recognised

that the state variables are controlled from the top

down while the rates of change are controlled from the

bottom up. This fundamental difference has accident-

ally emerged from our recent data collected within an

unsuccessful biomanipulation project (Gliwicz et al.,

2298 Z. Maciej Gliwicz


1998; Gliwicz, Rutkowska & Wojciechowska, 2000;

Gliwicz & Dawidowicz, 2001). The argument leading

to this conclusion is developed more fully in the

following sections.

Modifying the feeding behaviour of fish with

an alarm substance

The principal objective of the project was to determine

whether manipulation of fish abundance (reducing

the density of planktivorous fish) might be substituted

by a manipulation of fish behaviour (reducing feeding

rates of planktivorous fish), by frightening fish with

an alarm substance (skin preparation after Von Frish,

1941). This idea originated from observations that the

fear of predation can lead to reduced feeding rates

because planktivorous fish hide in the littoral zone or

aggregate and remain in deepwater refuges (for

review see Lima, 1998), where zooplankton is scarce

and difficult to detect (Gliwicz & Jachner, 1992). We

predicted that the impact of frightened fish on

zooplankton would be reduced significantly, thus

allowing for an increase in zooplankton density and

mean body size. We expected that following applica-

tion of the alarm substance smelt (Osmerus eperlanus

L.) and roach (Rutilus rutilus L.) would tend to remain

aggregated in their daytime refuges of the hypolim-

nion (smelt) or among the littoral vegetation (roach)

during dusk, when both species normally feed

most intensely in our lakes (Gliwicz & Jachner, 1992,

1993).

Roach was found to be a more convenient subject

for in situ manipulations than smelt for three reasons.

First, roach had displayed very regular diel habitat

shifts, especially in lakes free of smelt and other

pelagic fish. They spent the daytime among the littoral

vegetation in large aggregations and disintegrated in

the evening as individual fish surged offshore to feed

on Daphnia (Fig. 2), causing Daphnia abundance to

increase with increasing distance from shoreline

(Szynkarczyk, 2000). Secondly, the required large

quantities of alarm substance were more easily

obtained from roach. Skin preparation were needed

for treating a lake area of 8–20 ha. This corresponds to

up to 100 kg of live fish from commercial catches for a

single treatment (Gliwicz et al., 1998). Thirdly, roach

performed better in captivity, thus allowing for many

successful laboratory experiments before work in the

lake commenced. Laboratory tests on roach and bleak

(Alburnus alburnus L.) brought clear evidence that fish

responded to the predator odour and alarm substance

by aggregating, hiding in vegetation, and reducing

feeding rate (Fig. 3; see also Holker et al. 2002).

The field experiment was run in three intercon-

nected lakes in north-eastern Poland. The lakes were

very similar to each other (area 80–87 ha, maximum

depth 23–27 m, Secchi disc transparency 2.0–3.1). One

was used as the experimental (treatment) lake and the

Dep

th(m

)

0 100 200Distance (m)

10

020Sunset

30

10

02130

10

0 1926

Fig. 2 Example of an evening change in

near-shore roach distribution in an

experimental lake treated with alarm

substance (3 August 1997) starting with

typical daytime distribution at 19 : 26 h,

and ending an hour after sunset, at

21 : 30 h, when all daytime fish aggrega-

tions disintegrated and dispersed, and the

majority of individual roach moved into

the pelagial zone to forage offshore closer

to the lake surface. Some roach escaped

the echosounder when staying in the

upper 0–2 m. Each HADAS-generated

echogram of 500 pings covers 200 m

(3 min; after Gliwicz & Dawidowicz,

2001).



two remaining ones as reference lakes. In the sum-

mers of 1996 and 1997, one of the two ends of the

experimental lake received alarm substance (roach

skin preparation concentrate) to a final concentration

equal to that used in earlier laboratory experiments

such as those shown in Fig. 3 (6 10)5 cm2 of roach

skin area per 1 litre, or 2 10)7 mg hypoxanthine-3(N)-

oxide per 1 litre). The alarm substance was mixed

throughout the epilimnion, down to 4 m depth, by

pumping it into the wake of the propeller of a cruising

boat on a high-speed slalom. Hydroacoustic surveys

following the treatments showed the hypothesised

response on many occasions. Although the daytime

aggregations were breaking apart in the evening

when most fish moved into the pelagial zone

(Fig. 2), the overall fish density in the evening was

significantly lower offshore (Fig. 4) and the mean

depth of roach rushing offshore was greater in the

treatment than in the reference area (Fig. 5).

Having succeeded in frightening roach and mani-

pulating fish distribution in the lake, we also

expected to see the effects of the weakened impact

of fish predation on zooplankton and water trans-

parency in the experimental lake. In particular, we

anticipated:

1 a mass exodus of fish from the experimental to

the adjacent reference lake (to check this, all fish

moving out of and into the experimental lake were

counted in the connecting stream several days before

and after the treatment during both day and night);

2 roach intestines to be significantly less filled with

zooplankton in the treatment than in the reference

area (roach were trawl-sampled several days before

and after the treatment, intestines immediately dis-

sected, fixed and later analysed);

3 a higher density of the most vulnerable (i.e.

larger) cladoceran species between the treatment and

reference areas (plankton was sampled at eight

stations along the experimental lake’s long axis,

identified and sized);

4 a higher zooplankton abundance in the experi-

mental lake than in the two reference lakes (weekly

triplicate plankton samples were taken from each

lake’s centre throughout the seasons).

None of these four predicted responses were

observed and the hypothesised enhancement of water

transparency by modifying fish behaviour had even-

tually to be discarded, as had been foreseen by fellow

disbelievers from fish-ecology circles.

First, no increase was noted in the number of fish

leaving the experimental lake, nor was a decrease in

fish entering the lake from the reference lakes

observed. Instead, the opposite response was

observed following application of the alarm sub-

stance. The likely reason for this response is a change

in fish-depth distribution, i.e. the frightened fish were

Alarm substance added

35–45 mm

45–55 mm

60–80 mm

Fig. 3 Example of fright response to alarm substance addition in

roach of three size categories shown as reduction in feeding rate

in per cent of initial food intake before alarm substance addition

(arrow) to treatment aquaria (filled circles) compared with ref-

erence aquaria (empty circles) (mean from five replicate

experiments with different roach individuals; details in

Jachner & Janecki, 1999). Different response times of roach of

different body size to overcome fear and maximise feeding again

after exposure to an alarm substance is another example of size-

structured interactions in fish (see Persson et al. 1991; 1996).



pushed down to the deeper strata (Fig. 5) and cut

short from the half-metre-deep outflow. This hap-

pened, for example, after the treatment on 9 August

1996, in the north-western end of the experimental

lake. The number of roach leaving the lake declined

from pretreatment values of 600–700 fish day)1 (up to

280–350 fish h)1 in the middle of the night) to

10–20 fish day)1 (up to 10 fish h)1 in the middle of

the night), while the numbers of roach entering the

lake were unaffected (Gliwicz et al., 1998).

Secondly, although after each treatment nearly 300

roach intestines were inspected from trawl samples

taken in both areas of the lake, no difference in

feeding intensity was observed in any body-size

category (Gliwicz et al., 1998). Variability in the

roach diet was unusually high (Fig. 6), and the

mean prey selectivity index was very similar for all

five major prey species, an unusual observation. For

example, the index was nearly the same for the two

Daphnia species (details in Wisniowska, 1999),

although different body sizes should have translated

into higher vulnerability to predation by roach

(Fig. 7).

Thirdly, the difference between the treatment and

reference areas in the abundance and mean body sizes

of a dominant zooplankton prey, Daphnia cucullata,

was never very great nor long-lasting. Such a differ-

ence could only be detected a day or two following

the treatment (details in Gliwicz & Dawidowicz,

2001).

Fourthly, neither the density nor the reproduction

in zooplankton prey differed distinctly between the

lakes. Two Daphnia species were examined tho-

roughly for these effects (Fig. 8). The only significant

difference that was detected was a slightly higher

D. hyalina density in the experimental lake compared

with the two reference lakes, after several treatments

with alarm substance in July and August 1996.

Otherwise, the densities of all three D. hyalina popu-

lations were constant and similar in all lakes. The

similarity was even more striking in a smaller prey,

D. cucullata, which is an order of magnitude more

abundant than D. hyalina in all lakes (details in

Gliwicz et al., 2000).

Species-specific population-density thresholds?

The constant population density of both Daphnia

species in the three lakes, and the fixed density

difference between the two species, gave us a hint to

the nature of the disparity between top-down and

bottom-up impacts. Population densities remained

constant, although the intensity of reproduction dif-

fered greatly among the lakes and months with

different food levels (Gliwicz et al., 2000). It was also

uniform along the long axis of the experimental lake

and highly akin to those observed in 14 neighbouring

lakes showing a wide range in food levels (assessed as

chlorophyll a concentrations in the size fraction

<50 lm; details in Gliwicz, 2001). These observations

are not unique. Other coexisting Daphnia species also

have been found with ‘fixed’ or ‘species-specific’

density levels in many lakes (e.g. Kasprzak, Lathrop

& Carpenter, 1999). However, the phenomenon has

not attracted much attention in the literature and

plausible answers to the questions have not been

proposed until recently. One possible answer is that

the population density of a given cladoceran species is

fixed from the top-down by fish predation at a ‘species-

specific population-density threshold’ level, irrespective

10

10

10

10

10

10

10

10

10

10

0

0

0

0

0

0

0

0

0

0

0 0100 100200 200Distance (m)

Dep

th(m

)

Dep

th(m

)

NW SE

30 Jul

31 Jul

1 Aug

2 Aug

3 Aug

Reference Treatment

Fig. 4 Example of fright response of wild roach in an experi-

mental lake (right panels), observed at dusk (20 : 30 h) as a

decreased fish density following addition of alarm substance in

the south-eastern end of the lake on 1 August 1997. Densities in

the north-western end of the lake, which was used as a refer-

ence, are shown on the left (details in Gliwicz & Dawidowicz,

2001). The difference in roach distribution between the two areas

became apparent 1 day after the treatment. Echograms were

generated by HADAS from data recorded by an EY-M 70 kHz

echosounder, each covering 200 m traversed in 3 min (20 : 30–

20 : 33 h) when near-shore roach daytime aggregations started

to disintegrate (see Fig. 2).



Fig. 5 Example of fright response of wild roach in the evening (20 : 38–21 : 54 h). Mean depth of the roach population along the

long axis of an experimental lake from its north-western to south-eastern end (1300–1800 m on distance scale) 1 day before the

treatment with alarm substance (31 July) and the day after (2 August 1997). The mean depth of the roach population was greater

at the north-western end of the lake before, on 31 July, reflecting the persisting effect of previous treatment on 11 July. Data were

generated by HADAS from 2 to 10 m depth echos recorded with a SIMRAD EY-M 70 kHz echosounder along a standard transect from

the north-western to the south-eastern corner of the lake (squares, )1 SD), and on reverse (circles, +1 SD) when fish were already

much closer to the surface in the fading light of dusk (details in Gliwicz & Dawidowicz, 2001).

Fig. 6 Example of high variability in food content in five individual roach of the same body size (8–10 cm) from the same pelagic-

seine trawl sample from the north-western part of an experimental lake treated with alarm substance. Fish were caught between

22 : 00 and 22 : 30 h on 31 July 1997. Diverse multi-specific diet is shown on the left; uniform, single-species diet on the right.

Food diversity in individuals 1 and 2 was even greater than can be seen, as both guts had cyclopoid copepods, Daphnia hyalina

and Leptodora kindtii in numbers too small to be visible on the scale shown (details in Wisniowska, 1999).



1

0

–1

1

0

–1 D. cucullat

Bosmina

a

1

0

–1 D. hyalina

1

0

–1 Leptodora

Roach body length (cm)

1

0

–1 Chaoborus

0 04 48 812 12

Ivlev Vanderploeg& Scavia Mean

–0.59

–0.65

–0.67

–0.67

–0.83

Fig. 7 Food selectivity index for individual roach as a function of body length, with Ivlev (1961) scatter plots on the left and

Vanderploeg & Scavia (1979) scatter plots and mean values on the right (n ¼ 264 for each prey category). Five major food categories

were distinguished: Bosmina (three species combined), Daphnia cucullata, D. hyalina, Leptodora kindtii and larvae of the phantom midge,

Chaoborus flavicans. All 264 intestines were taken from roach trawl-sampled on 11–14 July and 30 July)4 August 1997 (details in

Wisniowska, 1999).

MAY JUL JUN AUG SEP 1996

100

10

1

0.1

0.01Ind.

104

m–2

(0–1

0 m

)

Fig. 8 Mean population densities of Daphnia cucullata (open circles) and D. hyalina (filled circles) in an experimental lake (solid

line) and two neighbouring reference lakes (dashed and dotted lines) throughout 1996. Note the logarithmic scale to show order

of magnitude differences between the population densities of D. cucullata (body size at first maturation ¼ 0.58 mm) and D. hyalina

(0.80 mm). For all densities starting from mid June (i.e. excluding the period of spring increase), 99% confidence intervals are

shown as dotted area (details in Gliwicz et al., 2000).



of the level of food limitation, the rate of somatic

growth of an individual, the reproductive effort in the

population, and the maximum rate of population

increase at a given food level.

A possible mechanism for this phenomenon has

been suggested elsewhere (Gliwicz, 2001). It relates

to the way in which dominant planktivorous fish

assess the density of alternate prey. The assessment

depends on the reactive distance of the fish, that is

the distance at which a foraging fish can see the prey

item. If the reactive distance differs for two prey

species, the fish may perceive no difference in

densities when the more conspicuous prey is far less

abundant than the less conspicuous prey. For exam-

ple, if the reactive distance for one species is twice as

great as for the other, as is the case for D. hyalina and

D. cucullata (Sliwowska, 2000), the water volume in

which the Daphnia can be seen by an individual fish,

the so-called reactive field volume (i.e. a sphere with

a radius equal to the reactive distance; Wetterer &

Bishop, 1985), would be up to an order of magnitude

greater for the larger Daphnia species (Fig. 9). This

difference should be reflected in different densities of

the two prey species in the lake, as was actually

found in a range of lakes and various seasons

(Fig. 8).

Moreover, at the 10 : 1 ratio of the species-specific

densities of the two Daphnia species, the selectivity

index for the two alternate prey items should not

differ, because fish would shift from one prey to the

other as soon as the perceived density difference

deviates from 1 : 1, corresponding to a real density

ratio of 10 : 1 (Fig. 9). This ratio was found in our

gut-content data set for roach (Fig. 7), suggesting

that prey vulnerability is not only generated exclu-

sively by the properties of an individual, but also by

the properties of a population. Prey choice was thus

not only related to the profitability of a single prey

item, but also to the rewards resulting from the

density of the prey population (planktivorous fish

section).

Planktivorous fish: selective or general predators?

Are planktivorous fish selective or generalist preda-

tors? Our data of roach gut-contents would seem to

show that, although the fish are selective, they should

also be considered generalist predators. They are

selective in that they would consume the prey species

whose individuals are most conspicuous and most

rewarding. They are also, however, generalist preda-

tors that tend to feed upon the most abundant prey,

shifting to the prey category that is most rewarding as

a result of both the properties of an individual prey

item and the density of the prey population.

The two predatory behaviours are not mutually

exclusive. On the contrary, they must be combined

and co-ordinated with each other in every decision

concerning prey choice, regardless of whether the

subject of choice is a prey individual or a prey

population. For example, fish may choose a prey item

based on size, as in the apparent size model of

O’Brien, Slade & Viniard (1976), in which a plankti-

vorous fish is assumed to select prey actively,

pursuing whichever prey appears largest. In addition,

two feeding modes must be compromised in a

decision to switch from one prey population to

another, such as choosing to feed on a prey category

Fig. 9 Diagrammatic representation of the difference in reactive

distance (i.e. the distance at which foraging fish would see prey)

for two prey categories, which results in relative reactive field

volumes for, and thus relative prey density assessment by, a

foraging planktivore such as roach. As a 2 : 1 difference in the

radius of the two spheres gives a 10 : 1 difference in volume,

foraging fish would assess densities of two prey categories as

equal when relative prey densities differ 10-fold, as they do in

case of the two Daphnia species shown in Fig. 8 (details in

Gliwicz, 2001).



that has just been found to be more rewarding, as in

the model of Murdoch (1969) and Murdoch, Avery &

Smyth (1975).

More rewarding prey may be the prey category

(species or single ontogenetic stage) that is relatively

more abundant or offers a higher net energy gain,

given the energy or time invested in a successful

individual encounter and ⁄or found by the fish to be

most efficient to capture. Each of the three reasons

should be an equally valid justification for switching

from prey item A to prey item B as soon as B becomes

more rewarding. Most experimental evidence show-

ing a switch to more rewarding prey comes from

laboratory studies examining predator switching

between different patches of prey or between different

feeding habitats, rather than between prey categories

in a homogeneous mixture of different prey, the real

situation encountered by a planktivorous fish in the

field. Field observations focus on the switch between

habitats of different food profitability (e.g. Werner,

Mittelbach & Hall, 1981), or different risk to predation

(e.g. Hall et al., 1979; Gliwicz & Jachner, 1992), rather

than on the switch from one food category to another

in response to a change in their relative abundance

(Murdoch & Bence, 1987).

Although it is well known that planktivorous fish

will switch from one zooplankton species to another

on a seasonal (Eggers, 1982) or daily basis (Hall et al.,

1979), the importance of prey relative abundance has

mostly been ignored in the quest for understanding

the phenomenon of prey switching and of food

selectivity in planktivorous fishes in general. The

focus was on prey relative body size, and the

question of prey abundance was confined to the

importance of overall prey density, and an increase

in density that would enhance selectivity for more

conspicuous prey. The phenomenon that selectivity

is increased via an increase in the overall density of

prey has been known since the pioneering work of

Ivlev (1961), and was experimentally explored by

Werner & Hall (1974). These authors allowed prey

categories, different D. magna instars, to differ in

body size and overall abundance, while keeping the

relative abundance of the prey categories constant.

Relative prey density was often touched on in

theoretical approaches (Gerritsen & Strickler, 1977;

Eggers, 1982; Wetterer & Bishop, 1985; Giske, Huse

& Fiksen, 1998), but was ignored in experimental and

field studies on planktivorous fish. Experimental and

field studies examined selectivity in response to prey

body-size and overall prey abundance. Some of the

recent studies focused ‘on effects of body size and

zooplankton abundance’ in regard to the functional

response (e.g. Johnston & Mathias, 1994). An excep-

tion is Luo, Brandt & Klebasko (1996), who were able

to predict the size frequencies of zooplankton prey in

anchovy stomachs from the ambient zooplankton

body-size frequencies found in the habitat (mid-

Chesapeake Bay).

The mutual importance of prey body size and prey

population density as two determinants of food

selectivity in a typical planktivore has recently

gained attention, following the realisation that a lake

with an indigenous fish fauna has species-specific

population-density thresholds for each cladoceran

prey category. The threshold density is inversely

related to the individual susceptibility of each

cladoceran species to predation, which is most

strongly related to body size at first reproduction

(species-specific population-density thresholds sec-

tion). The gut contents of roach from our experi-

mental lake showed high variability in individual

roach diets (Fig. 6) and in the selectivity index for

different prey categories (Fig. 7) probably because of

frequent switching among prey categories.

Part of this variability may be an effect of

switching on a daily basis, especially when the

switch is to or from phantom midge larvae (Chaobo-

rus spp.), which were frequently the sole prey found

in the roach guts (Fig. 6). Such a switch may require

a shift between two different habitats, the cladocer-

an-rich epilimnion and the deeper strata where

Chaoborus can be encountered on the evening forays

offshore, before light intensity becomes too low to

allow foraging roach to detect their prey (Fig. 2).

The behaviour of dailyswitching may also be behind

the high variability of the selectivity index within a

narrow size category of fish, a majority with values

close to either )1 or +1 (Fig. 7). This suggests that an

individual roach may prey upon small-bodied Bos-

mina or D. cucullata on one evening, but on larger

D. hyalina on the evening after. This possibility is

also reflected by the dominance of different prey

categories in similar-sized roach guts from the same

trawl sample (Fig. 6).

However, a significant part of the high diet variab-

ility appears to result from more frequent switching,

rather than from the daily (whole-evening) shift



between different prey categories. In 60% of all 264

roach inspected, the diet diversity expressed as a prey

Shannon-Wiener index (based on species contribution

to the total food volume) was above 0.4, which

corresponds with the diet of fish number 4 in Fig. 6.

The diverse food composition of an individual roach

would suggest that most individuals switch from one

prey category to another many times within a single

feeding session offshore. In its evening thrust towards

the middle of the lake, where zooplankton prey is

more abundant, a foraging roach may slow down to

pick up a number of prey of one category, and then

move forward again as soon as a local swarm has been

wiped out. It can do so again with another prey

category once that other prey has been assessed as

more rewarding.

Since the pioneering work of Ivlev (1961), Hrba-

cek (1962), and Brooks & Dodson (1965), the effect

of predation by planktivorous fish has been

assumed to be selective. Our analyses show that

this assumption is correct, but only in the sense that

each different body-sized species has a different

population-density threshold that results from a

different relative reactive field volume. Thus, once

the relative proportions of coexisting species have

been fixed by body-size dependent mortality, the

effect of predation is not selective anymore. On the

contrary, the force of fish predation appears to be a

strong stabilising factor accounting for constant

relative densities of different prey species through-

out the seasons and from one habitat to another

(Fig. 8). There are opposing forces that stem from

the race between individuals of each population to

grow and mature soonest. This is the reason for

each population to show a reproductive rate as high

as possible within the constraints set by temperature

and food levels, whereas birth rates in the popula-

tion and the rate of population increase are con-

trolled by either time or resources (the ‘time and

resource limitation’ of Schoener, 1973).

It thus appears that the availability of resources

controls the rate of each population increase. Regard-

less of the rate of increase, the density of each

population would eventually be fixed by a mortality

rate resulting from fish predation and fish switching

from one prey item to another depending on their

relative densities (species-specific population-density

thresholds section). This conclusion is in agreement

with a notion expressed a long time ago (Elton, 1927):

that general predators feed most heavily upon the

most abundant species until their abundance is

reduced, and that ‘the predator switches the great

proportion of its attack to another prey which has

become the most abundant’ (Murdoch, 1969). Or – as

we should say more precisely being aware of the

effect of body size – relatively the most abundant

(Gliwicz, 2001). For example, it may be speculated

that that the prey-switching behaviour was the reason

why the selectivity for Bosmina was found to be

slightly higher than for other prey in our experimental

lake (Fig. 7). Unlike the other prey species, the

Bosmina population may have been just in the phase

of density increase beyond its species-specific thresh-

old level at the time of our fieldwork on the lake. This

may also be the reason why the food selectivity for a

specific prey was neither found to be similar among

individual fish, nor significantly different for different

prey species, even those representing extremes in

body size.

High variability of the selectivity index for differ-

ent prey categories is often a source of frustration for

researchers analysing gut contents; they prefer find-

ing high values for conspicuous and low values for

less conspicuous prey species (e.g. Bohl, 1982). Clear

differences in selectivity values, which are probably

less common than published accounts imply, could

be interpreted as a sign that a change in the

dominant diet is being witnessed, the majority of

fish switching from one prey to another ‘which has

become the most abundant’ (Murdoch, 1969), just as

could be the case of Bosmina in our experimental

lake.

Zooplankton in the presence and absence of fish

By switching from one zooplankton prey to another,

planktivorous fish would hold the density of each

species below the carrying capacity (K). Each density

increase would be followed by a shift in fish diet from

the most rewarding prey in the past to the most

rewarding prey in the present situation (Fig. 10, top).

The most conspicuous prey (the large-bodied and

thus competitively superior species) would be held at

the lowest density, corresponding to its low ‘relative

density’ resulting from the high vulnerability of

individuals at maturation (large body size at first

reproduction). Low abundance would allow for

higher food levels, and thus for the coexistence of



other species, including small-bodied cladocerans,

rotifers and ciliates. This coexistence may last at least

until the fish impact has been removed. For example,

in Smyslov Pond, one of Hrbacek’s famous fishponds

in Bohemia, large-bodied D. pulicaria was found to

monopolise resources for 90 days in the absence of

fish predation (Fig. 10, bottom).

The Smyslov Pond example shows that, in the

absence of fish, Daphnia density can be controlled

from the bottom up and held at the equilibrium level

of the carrying capacity of the habitat. Algal food

resources would be effectively controlled from the top

down, well below their high potential, until fish feed

again on Daphnia. With fish predation restored,

Daphnia density would decrease, chlorophyll concen-

tration increase, and ‘ecological space’ become avail-

able to other cladocerans and rotifers that are inferior

competitors for resources. This situation appears to be

typical of ponds and lakes, where the impact of fish

allows for the coexistence of many species with

similar ecological niches, including congeneric species

such as D. hyalina and D. cucullata (species-specific

population-density thresholds section). Concurring

with Hutchinson’s (1961) ‘paradox of the plankton’

(e.g. Ghilarov, 1984), diverse plankton assemblages

have often been accounted for by non-equilibrium

effects based on the intermediate disturbance hypo-

thesis, or justified by different abilities to partition

resources (reviewed by Rothhaupt, 1990). A diverse

community of planktonic herbivores would also be

seen following any long-lasting phase of clear-water

resulting from a temporary relaxation in fish activity

and periodic single-Daphnia-species monopolising

resources. This situation has been observed in many

lakes and is well known as ‘Daphnia summer decline’

which usually follows a ‘spring clear-water phase’

(Sommer, 1989; Hulsmann & Voigt, 2002).

The only natural habitats in which the clear-water

phase lasts as long as in Smyslov Pond, are those

where fish are absent, and a competitively superior

large-bodied phyllopode such as D. pulicaria or

Artemia franciscana monopolise resources, holding

them at an equilibrium level below the threshold

food concentration needed for other species to grow

and reproduce (Gliwicz, in press). In such fishless

habitats, where water remains clear in spite of high

nutrient loads, phytoplankton would be suppressed

from the top down by the competitively superior

herbivore species, whose high population density in

turn is restrained from the bottom up by food

availability. The absence of predation allows an

individual to allocate all its efforts to the competi-

tion for resources, as interspecific competition gives

way to intraspecific competition. In the fertile

habitat of the Great Salt Lake, Utah, the diverse

phytoplankton is held at an extremely low biomass

(1 lg chlorophyll L)1) by an efficient herbivore,

Artemia. When Artemia is removed experimentally

or has retreated naturally to diapause, mineral

resources are immediately monopolised by the most

effective green algae, Dunaliella viridis, leading to a

concentration of 30 lg chlorophyll L)1 (Gliwicz, in

press).

0 30

30

60

60

90

90

120

120

Elapsed time (days from 1 April 1972)

100

50

0

Pop

ulat

ion

dens

ity (

ind.

L–1)

Cho

roph

yll (

µg L

–1)

100

50

00

Elapsed time (days)

Pop

ula

tion

dens

ity(%

)K

100

50

0

Fig. 10 Top panel: Diagrammatic representation of a typical

change in population density of a planktonic herbivore, such as

Daphnia or Bosmina in the absence and presence of planktivorous

fish. Bottom panel: example of a real density change of a

Daphnia population in the absence of fish impact in Smyslov

Pond in 1972. High numbers of Daphnia pulicaria accompanied

by smaller numbers of D. galeata (solid line) lasted in equilib-

rium for 90 days with low levels of small edible algae (dotted

line) and high levels of mineral resources, until extermination of

D. pulicaria by fish (day 100) allowed other zooplankton taxa to

form a typical multispecies zooplankton community and algae

to form a bloom of 70 lg chlorophyll L)1, typical of Smyslov

Pond (after Fott et al., 1974; and Fott, Desortova & Hrbacek,

1980).



Such situations observed in fishless habitats sug-

gest that population densities of both phyto- and

zooplankton and body size of zooplankton species at

first reproduction may be controlled from the bottom

up as long as the top-down impact is effective. High

zooplankton densities cannot last, however, after the

impact has been removed. As soon as fish are

introduced, herbivore population density and body

size becomes fixed by top-down forces again, and

bottom-up controls become restricted to rates at which

density or body size can be restored to levels that

would be fixed by fish predation.

Conclusions

The species-specific population-density thresholds in

cladocerans, the similar values for the selectivity

index in roach, and the contrast between zooplankton

in the presence and absence of fish, all show that an

impact from the top-down can control zooplankton

biomass, individual body size and population density.

In contrast, bottom-up forces influence assimilation

rate, individual growth rate and reproduction

(Fig. 11). The nature of the impacts from top down

and bottom up hence is distinctly different also at the

population level. Although in contrast to the individ-

ual level a common currency can be conveniently

defined at the population level, the disparity of the

two entities are equally great at both levels.

This conclusion is supported by our data, at least as

regards the herbivorous zooplankton. Fish predation

would primarily determine the population density in

a herbivore such as Daphnia. It would do so regardless

of the somatic growth rate of individual animals, and

the population reproduction rate, which are both

independent of top-down effects. These rates are

bottom-up controlled. The different nature of this

bottom-up control is best reflected in the notion of the

functional response, the processes of food assimil-

ation, individual growth, and population increase,

which are all controlled by food level. The rate at

which food resources are being produced is not the

critical factor, although some people would assume

that ‘low food level would not necessarily be equal

with food limitation in animals such as Daphnia

because even at low food levels food production

may be high enough to support high feeding rates and

fast individual growth’ (an anonymous review, pers.

comm.). This would be the case as long as the top-

down impact of predators was effective. Its removal

would allow a single competitively superior species to

monopolise resources at an equilibrium level held

near the food-threshold level, as in the fish-free

habitats of alpine and saline lakes (zooplankton in

the presence and absence of fish section). The same

reasoning is probably valid for the other trophic levels

in the food web, both primary producers and pred-

ators.

BOTTOM-UP:

Assimilation (A)Individual growth rateRateof reproduction

TOP-DOWN:

CONTROL OF STATE VARIABLES

BiomassIndividual body sizePopulation density

P

A

Fig. 11 Diagrammatic representation of

the different nature of bottom-up (food

limitation) and top-down impacts (pre-

dation) on zooplankton, with its abun-

dance (biomass) controlled from the top

down by planktivorous fish (right), and

process rates (energy ⁄ carbon flow) con-

trolled from the bottom up by phyto-

plankton food availability (left).



The phytoplankton biomass would depend on the

top-down impact of grazing imposed by herbivores

rather than by the trophic state of the habitat. This

effect would be most apparent in the absence of fish,

as low phytoplankton abundance is comparable in

fishless habitats regardless of their potential, from

ultra-oligotrophic mountain lakes to nutrient-rich

saline lakes of hydraulically locked lowlands. The

low-biomass multispecies phytoplankton of these

habitats would last as long as the top-down impact

of an effective herbivore persists. Its removal would

allow single algal species to monopolise resources at

an equilibrium level with mineral resources kept low,

as in the fish-free habitat of the Great Salt Lake

(Section 6).

These mechanisms could also explain why our

efforts at mediating roach feeding behaviour in the

experimental lake were unsuccessful (modifying fish

feeding behaviour section). We attempted to reduce

roach feeding rate, not roach density or biomass, that

is a rate, not a state variable. Although treatment with

alarm substance could possibly affect roach density in

the long term, a short-term increase of zooplankton

density cannot be expected if the above scenario is

correct.

Thus, with the reasoning from Fig. 11 applied to the

trophic level above (Fig. 12). I hypothesise that only

the state (biomass and population density) of plank-

tivorous fish affects the strength of top-down control,

not the rate at which the fish reproduce, grow, or feed.

The same effect might account for the fragility of

effective top-down control: the spring clear-water

phase is usually a short phenomenon and can, if it

lasts longer, be abruptly terminated as seen in Smy-

slov Pond. The effect may also be the reason why top-

down effects are gradually weakened from the top to

the bottom of the food web as suggested by McQueen

et al. (1989). Experiments run in the Plankton Towers

at the Max-Planck Institute in Plon, Germany, showed

that the top-down effects on roach can be very strong,

but also that they are only transitory: fish frightened

with alarm substance were more reluctant to feed in

the daylight than the reference fish, but the initial

difference in food abundance in the evening (Daphnia

density) vanished overnight because fish fed in the

dark (Gliwicz et al., 2001).

CONTROL OF RATES

Assimilation (A)Individual growth rateRate of reproduction

BiomassIndividual body sizePopulation density

CONTROL OF STATE VARIABLES

Fig. 12 Diagrammatic representation of the different nature of bottom-up and top-down impacts on planktivorous fish, with their

abundance (biomass) controlled from the top down by piscivores (right), and process rates (energy ⁄ carbon flow) controlled from the

bottom up by zooplankton prey availability (left).



Acknowledgments

I am thankful to two anonymous reviewers for valuable

comments and multiple suggestions on the earlier

version of the manuscript, and to Mark Gessner for

thorough editorial improvements. The study was

supported by a grant from the European Commission to

Z.M. Gliwicz, W. Lampert, V. Korinek and M.J. Boavida

(Grant no. CIPA-CT93-0118-DG 12 HSMU) and a grant

from the Polish Committee for Scientific Research to

Z.M. Gliwicz (Grant no. PO4F-074–14).

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(Manuscript accepted 8 February 2002)



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