Download On the different nature of top-down and bottom

Freshwater Biology (2002) 47, 2296–2312
On the different nature of top-down and bottom-up
effects in pelagic food webs
Z. MACIEJ GLIWICZ
Department of Hydrobiology, University of Warsaw, Warsaw, Poland
SU M M A R Y
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
Correspondence: Z. Maciej Gliwicz, Department of Hydrobiology, University of Warsaw, Warsaw, 02-097 Warsaw, Poland.
E-mail: [email protected]
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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 students’ who had been inspired by Ivlev’s (1955, 1961)
book on the ‘Experimental ecology of the feeding of fishes’
and Hrbáček’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
Hrbáček’s (1962) fishpond observations, which were
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Top-down versus bottom-up effects
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According to McQueen et al. (1989) and their ‘bottom-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 reproduction, 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 sizeselective 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.
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 Hrbáček
(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 limitation effects had implications for the way community and population structure would be viewed.
(a)
(b)
(c)
PREDATION
PREDATION
PREDATION
Body-size dependent
vulnerability
Mortality
Body-size dependent
predation risk
ZOOPLANKTON ABUNDANCE
AND COMMUNITY STRUCTURE
POPULATION DENSITY
Energy-transfer efficiency
and body-size-related
superiorityin resource
competition
Reproduction
Body-size dependent
food-threshold concentration
FOOD LIMITATION
FOOD LIMITATION
FOOD LIMITATION
INDIVIDUAL LIFE HISTORY
AND BEHAVIUOR
Fig. 1 Diagrammatic representation of the parity of bottom-up (food limitation) and top-down impacts (predation) on zooplankton abundance and community structure (a), population density and age structure (b), and individual behaviour and life histories (c).
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Z. Maciej Gliwicz
The concept depicted in Fig. 1 now appears to be
widely accepted, whether at the community, population 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 zooplankton 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 individual’s life span (McNamara & Houston, 1986; Lima,
1998). This difference may be the reason why behavioural 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 compared 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, especially 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 disparity 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 limitation 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 topdown and bottom-up impacts (Fig. 1) has been
approved so readily for the population and community 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 accidentally emerged from our recent data collected within an
unsuccessful biomanipulation project (Gliwicz et al.,
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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 application of the alarm substance smelt (Osmerus eperlanus
L.) and roach (Rutilus rutilus L.) would tend to remain
aggregated in their daytime refuges of the hypolimnion (smelt) or among the littoral vegetation (roach)
during dusk, when both species normally feed
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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 Hölker et al. 2002).
The field experiment was run in three interconnected 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
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 aggregations 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).
Depth (m)
10
0
20 30
Sunset
10
0
30
21
10
0
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Distance (m)
200
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Z. Maciej Gliwicz
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 reference 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 sizestructured interactions in fish (see Persson et al. 1991; 1996).
two remaining ones as reference lakes. In the summers 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 manipulating fish distribution in the lake, we also
expected to see the effects of the weakened impact
of fish predation on zooplankton and water transparency 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 dissected, 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 experimental 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 eventually 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 substance. The likely reason for this response is a change
in fish-depth distribution, i.e. the frightened fish were
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312
Top-down versus bottom-up effects
NW
Treatment
Reference
SE
0
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30 Jul
10
0
0
10
10
31 Jul
0
0
1 Aug
10
10
0
Depth (m)
Depth (m)
10
0
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10
2 Aug
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0
10
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3 Aug
0
100
200 0
Distance (m)
100
200
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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 difference 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 thoroughly 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 populations 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).
Fig. 4 Example of fright response of wild roach in an experimental 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 reference, 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).
Species-specific population-density thresholds?
pushed down to the deeper strata (Fig. 5) and cut
short from the half-metre-deep outflow. This happened, 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 Wiśniowska, 1999),
although different body sizes should have translated
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 differed 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 ‘speciesspecific population-density threshold’ level, irrespective
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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 pelagicseine 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 Wiśniowska, 1999).
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Vanderploeg
& Scavia
Ivlev
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Mean
1
–0.59
0
Bosmina
–1
1
–0.65
0
–1
D. cucullat a
1
–0.67
0
–1
D. hyalina
1
–0.67
0
–1
Leptodora
1
–0.83
0
Chaoborus
–1
0
4
8
12
0
4
8
12
Roach body length (cm)
Ind.104 m–2 (0–10 m)
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
Wiśniowska, 1999).
100
10
1
0.1
0.01
MAY
JUL
JUN
AUG
SEP 1996
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).
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312
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Z. Maciej Gliwicz
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 example, 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 exclusively 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 predators? 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
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).
whose individuals are most conspicuous and most
rewarding. They are also, however, generalist predators 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 planktivorous 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
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Top-down versus bottom-up effects
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 showing 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
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312
2305
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 exception 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 (midChesapeake 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 section). The gut contents of roach from our experimental 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 (Chaoborus 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 cladoceran-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 Bosmina 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 variability appears to result from more frequent switching,
rather than from the daily (whole-evening) shift
2306
Z. Maciej Gliwicz
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), Hrbáček (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 throughout 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 population and the rate of population increase are controlled 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. Regardless 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 threshold 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 different prey categories is often a source of frustration for
researchers analysing gut contents; they prefer finding 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
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312
100
50
0
0
30
60
90
Elapsed time (days)
120
100
100
50
50
0
0
0
30
60
90
Chorophyll (µg L–1)
Population density (ind.L–1)
Population density (%K)
Top-down versus bottom-up effects
120
Elapsed time (days from 1 April 1972)
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 equilibrium 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 & Hrbáček,
1980).
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 Hrbácek’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,
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312
2307
Daphnia density would decrease, chlorophyll concentration increase, and ‘ecological space’ become available 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 hypothesis, 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; Hülsmann & 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 competition 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).
Z. Maciej Gliwicz
2308
Such situations observed in fishless habitats suggest 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 individual level a common currency can be conveniently
defined at the population level, the disparity of the
two entities are equally great at both levels.
BOTTOM-UP:
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 assimilation, 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 topdown 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 predators.
TOP-DOWN:
P
A
CONTROL OF STATE VARIABLES
Assimilation (A)
Individual growth rate
Rate of reproduction
Biomass
Individual body size
Population density
Fig. 11 Diagrammatic representation of
the different nature of bottom-up (food
limitation) and top-down impacts (predation) on zooplankton, with its abundance (biomass) controlled from the top
down by planktivorous fish (right), and
process rates (energy ⁄ carbon flow) controlled from the bottom up by phytoplankton food availability (left).
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312
Top-down versus bottom-up effects
CONTROL OF RATES
CONTROL OF STATE VARIABLES
Assimilation (A)
Individual growth rate
Rate of reproduction
Biomass
Individual body size
Population density
2309
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).
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
2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312
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 planktivorous 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 Smyslov Pond. The effect may also be the reason why topdown 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 Plön, 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).
2310
Z. Maciej Gliwicz
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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