On the Different Nature of Top-Down and Bottom-Up Effects in Pelagic Food Webs

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

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

result of short food supply or by enhanced mortality Introduction through predation. These contrasting views were One of the most fundamental questions in the early most apparent between those plankton ecologists days of zooplankton studies, centred on the relative involved in the International Biological Program importance of competition and predation. The two focussing on productivity, and those taking a more factors used to be looked on as mutually exclusive, so evolutionary approach, mostly ‘Hutchinson’s stu- the question was often asked in a conclusive way as to dents’ who had been inspired by Ivlev’s (1955, 1961) whether zooplankton abundance would be controlled book on the ‘Experimental ecology of the feeding of fishes’ by the limitation of growth and reproduction as a and Hrbaćˇek’s (1962) paper on ‘zooplankton in relation to the fish stock’. Correspondence: Z. Maciej Gliwicz, Department of Hydrobiol- However, the opposing views soon started to be ogy, University of Warsaw, Warsaw, 02-097 Warsaw, Poland. reconciled. An important impetus came from E-mail: [email protected] Hrbaćˇek’s (1962) fishpond observations, which were

2296 2002 Blackwell Science Ltd Top-down versus bottom-up effects 2297 expanded to lake zooplankton by Brooks & Dodson According to McQueen et al. (1989) and their ‘bot- (1965) and formalised as the ‘size-efficiency hypothesis’. tom-up: top-down theory’, the ‘trophic level biomass Although the spirit of the confrontation was still much control is determined by the combined impacts of predation alive at the Dartmouth College workshop on the and energy availability’. According to Lampert (1988), ‘Evolution and ecology of zooplankton communities’ in the population density of Daphnia species would be 1979 (Kerfoot, 1980), the gap between the food and determined by the combined impacts ‘of food limitation predation explanations was being closed. Eventually, and predation’. This view has been imprinted in our the two approaches were combined successfully, as minds, and similar reasoning has been commonplace reflected by publications such as the ‘Effects of food in recent publications on zooplankton communities availability and fish predation’ (Vanni, 1987) and the and populations (e.g. Sommer, 1989; Lampert & ‘Relative importance of food limitation and predation’ Sommer, 1997). (Lampert, 1988). The same reasoning was introduced into the study Two decades after the pioneering papers by Hrbaćˇek of individual life histories and behaviour, and could (1962) and Brooks & Dodson (1965), the importance of often be found in depictions of life in pelagial zones as both food limitation and predation had been widely ‘life between the never-ending…hazards of starvation and accepted by zooplankton ecologists working at both risks to predation’ (e.g. Gliwicz, 2001). The parity of the community (Fig. 1a) and population level (Fig. 1b). top-down and bottom-up impacts on behavioural and Thus, the abundance and specific structure of life-history traits, especially body size at first repro- zooplankton communities has been perceived as being duction, has become a key assumption in studies on controlled from both the top down and the bottom up: the costs of antipredator defences in zooplankton and by predation, because of species-specific vulnerability fish (Fig. 1c): the life history and behaviour of an to predators such as planktivorous fish, and by food individual is assumed to be controlled by predation, levels, because of species-specific efficiency in food because of body-size-specific vulnerability to size- utilisation (Fig. 1a). The density and age structure of selective predators such as planktivorous fish, and by the population would be controlled by predation food levels, because of body-size dependent abilities because of different age-specific mortality, and by to compete for food (food-threshold concentration). food levels because of different body-size-dependent Besides being the two most evident factors of natural abilities to utilise food (Fig. 1b). selection, the top-down and the bottom-up impacts The notion of combined predation and food limita- also seem equally important for the selection of an tion effects had implications for the way commu- appropriate phenotype among a range of phenotypes nity and population structure would be viewed. available within a plastic genotype.

(a) (b) (c)

PREDATION PREDATION PREDATION

Body-size dependent Body-size dependent Mortality vulnerability predation risk

ZOOPLANKTON ABUNDANCE INDIVIDUAL LIFE HISTORY POPULATION DENSITY AND COMMUNITY STRUCTURE AND BEHAVIUOR

Energy-transfer efficiency and body-size-related Body-size dependent Reproduction superiorityin resource food-threshold concentration competition FOOD LIMITATION FOOD LIMITATION FOOD LIMITATION

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).

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 2298 Z. Maciej Gliwicz The concept depicted in Fig. 1 now appears to be Following the pioneering work by Werner & widely accepted, whether at the community, popula- Gilliam (1984) on size-structured fish populations, tion or individual level. Inherent in it is the tacit the two disparate quantities have often been com- assumption that the nature of the two impacts is the pared successfully when they were converted to the same with only the direction, down or up, differing common currency of fitness. Dynamic modelling of (see Reynolds, 1994; Drenner & Hambright, 1999; state-dependent decision-making under the risk of Carpenter et al. 2001; Benndorf, 2002; McQueen et al. predation has been successfully developed to tackle 2001). For two reasons, however, this assumption is the problem of the relative importance of top-down incorrect. The first reason is that top-down and and bottom-up impacts for animal behaviour, espe- bottom-up forces affect differently the behaviour of cially in fish and zooplankton (Mangel & Clark, 1988). an individual animal (e.g. a Daphnia or a fish), which However, the common currency of fitness has not trade off increased safety against decreased feeding solved the problem that the nature of top-down and rates. The second reason is less apparent and has been bottom-up effects is different. While feeding rate, largely overlooked in the top-down versus bottom-up individual growth rate and reproductive potential debate. It relates to the fact that rates (e.g. growth may all be assessed in energy units, predation risk can rates) are controlled from the bottom-up whereas state only be asserted as a probability in regard to the sole variables (e.g. density) at both the population and undivided life of an individual that can either be alive community level are controlled from the top-down. or dead. The importance of this fundamental difference has For an individual, satiation can take any value emerged from recent field studies on fish behaviour in between 0 and 100%. Long periods with an empty an experimental biomanipulated lake, and on the role gut (zero satiation) can be compensated for in future of prey abundance in prey selectivity in planktivorous when food levels increase again. However, at the fish. It is further supported by comparisons of zoo- individual’s level, survival can never be lower than plankton communities in the presence and absence of 100%. Therefore, the hazards of starvation and the fish. These points are discussed in detail in the risk of predation cannot be compared with a following sections. 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- An individual’s and a population’s perspective ity has never been ignored at the level of the We know intuitively that risking life is different from individual. risking hunger. The risk of becoming subject to The situation is different at the population and predation may become lethal within seconds, while community level, because mortality and reproduction the risk of starvation may persist for days or weeks readily combine with each other. The common with future compensation always being possible. currency is the individual. The effect of food limita- Compensation might be readily achieved as soon as tion is reflected in the birth rate, b, and the effect of food levels have increased, as an effect of animals predation in the death rate, d, the two merging into refraining from intense feeding in food-proficient but the intrinsic rate of population-density increase predation-risky areas. The possibility of compensation (r ¼ b ) d). For this reason, the ‘sandwich’ or might account for the difficulty in devising a common ‘squeeze-in’ idea of full symmetry between top- currency for life-history or behavioural decisions when down and bottom-up impacts (Fig. 1) has been considering both the risk of predation and the hazards approved so readily for the population and com- of starvation. The major difference between the two is munity level. in the likelihood of a mistake becoming fatal. It is high However, the illusion of full symmetry at the in the case of predation, but many mistakes in regard population level is revealed as soon as it is recognised to food limitation could be allowed within an individ- that the state variables are controlled from the top ual’s life span (McNamara & Houston, 1986; Lima, down while the rates of change are controlled from the 1998). This difference may be the reason why beha- bottom up. This fundamental difference has accident- vioural responses to increased predation risk tend to ally emerged from our recent data collected within an be stronger than those to decreased food levels. unsuccessful biomanipulation project (Gliwicz et al.,

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 Top-down versus bottom-up effects 2299 1998; Gliwicz, Rutkowska & Wojciechowska, 2000; most intensely in our lakes (Gliwicz & Jachner, 1992, Gliwicz & Dawidowicz, 2001). The argument leading 1993). to this conclusion is developed more fully in the Roach was found to be a more convenient subject following sections. 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 Modifying the feeding behaviour of fish with pelagic fish. They spent the daytime among the littoral an alarm substance vegetation in large aggregations and disintegrated in The principal objective of the project was to determine the evening as individual fish surged offshore to feed whether manipulation of fish abundance (reducing on Daphnia (Fig. 2), causing Daphnia abundance to the density of planktivorous fish) might be substituted increase with increasing distance from shoreline by a manipulation of fish behaviour (reducing feeding (Szynkarczyk, 2000). Secondly, the required large rates of planktivorous fish), by frightening fish with quantities of alarm substance were more easily an alarm substance (skin preparation after Von Frish, obtained from roach. Skin preparation were needed 1941). This idea originated from observations that the for treating a lake area of 8–20 ha. This corresponds to fear of predation can lead to reduced feeding rates up to 100 kg of live fish from commercial catches for a because planktivorous fish hide in the littoral zone or single treatment (Gliwicz et al., 1998). Thirdly, roach aggregate and remain in deepwater refuges (for performed better in captivity, thus allowing for many review see Lima, 1998), where zooplankton is scarce successful laboratory experiments before work in the and difficult to detect (Gliwicz & Jachner, 1992). We lake commenced. Laboratory tests on roach and bleak predicted that the impact of frightened fish on (Alburnus alburnus L.) brought clear evidence that fish zooplankton would be reduced significantly, thus responded to the predator odour and alarm substance allowing for an increase in zooplankton density and by aggregating, hiding in vegetation, and reducing mean body size. We expected that following applica- feeding rate (Fig. 3; see also Ho¨lker et al. 2002). tion of the alarm substance smelt (Osmerus eperlanus The field experiment was run in three intercon- L.) and roach (Rutilus rutilus L.) would tend to remain nected lakes in north-eastern Poland. The lakes were aggregated in their daytime refuges of the hypolim- very similar to each other (area 80–87 ha, maximum nion (smelt) or among the littoral vegetation (roach) depth 23–27 m, Secchi disc transparency 2.0–3.1). One during dusk, when both species normally feed was used as the experimental (treatment) lake and the

0 1926

Fig. 2 Example of an evening change in 0 30 near-shore roach distribution in an 20 experimental lake treated with alarm Sunset substance (3 August 1997) starting with typical daytime distribution at 19 : 26 h, 10

and ending an hour after sunset, at Depth (m) 21 : 30 h, when all daytime ﬁsh aggrega- 0 30 tions disintegrated and dispersed, and the 21 majority of individual roach moved into the pelagial zone to forage offshore closer to the lake surface. Some roach escaped 10 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, 0 100 200 2001). Distance (m)

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 2300 Z. Maciej Gliwicz

Alarm substance added 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 35–45 mm 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 45–55 mm 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 60–80 mm 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, Fig. 3 Example of fright response to alarm substance addition in identified and sized); roach of three size categories shown as reduction in feeding rate in per cent of initial food intake before alarm substance addition 4 a higher zooplankton abundance in the experi- (arrow) to treatment aquaria (filled circles) compared with ref- mental lake than in the two reference lakes (weekly erence aquaria (empty circles) (mean from five replicate triplicate plankton samples were taken from each experiments with different roach individuals; details in lake’s centre throughout the seasons). Jachner & Janecki, 1999). Different response times of roach of different body size to overcome fear and maximise feeding again None of these four predicted responses were after exposure to an alarm substance is another example of size- observed and the hypothesised enhancement of water structured interactions in fish (see Persson et al. 1991; 1996). transparency by modifying fish behaviour had eventually to be discarded, as had been foreseen by fellow disbelievers from fish-ecology circles. two remaining ones as reference lakes. In the sum- First, no increase was noted in the number of fish mers of 1996 and 1997, one of the two ends of the leaving the experimental lake, nor was a decrease in experimental lake received alarm substance (roach fish entering the lake from the reference lakes skin preparation concentrate) to a final concentration observed. Instead, the opposite response was equal to that used in earlier laboratory experiments observed following application of the alarm sub- ) such as those shown in Fig. 3 (6 10 5 cm2 of roach stance. The likely reason for this response is a change ) skin area per 1 litre, or 2 10 7 mg hypoxanthine-3(N)- 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 2301

NWReference Treatment SE into higher vulnerability to predation by roach 0 0 (Fig. 7). 10 30 Jul 10 Thirdly, the difference between the treatment and

0 0 reference areas in the abundance and mean body sizes

10 of a dominant zooplankton prey, Daphnia cucullata, 10 31 Jul was never very great nor long-lasting. Such a differ- 0 0 ence could only be detected a day or two following 1 Aug 10 10 the treatment (details in Gliwicz & Dawidowicz,

Depth (m)

Depth (m) 0 0 2001).

10 2 Aug 10 Fourthly, neither the density nor the reproduction in zooplankton prey differed distinctly between the 0 0 lakes. Two Daphnia species were examined tho- 10 3 Aug 10 roughly for these effects (Fig. 8). The only significant difference that was detected was a slightly higher 0 100 200 0 100 200 Distance (m) D. hyalina density in the experimental lake compared with the two reference lakes, after several treatments Fig. 4 Example of fright response of wild roach in an experimental lake (right panels), observed at dusk (20 : 30 h) as a with alarm substance in July and August 1996. decreased fish density following addition of alarm substance in Otherwise, the densities of all three D. hyalina popu- the south-eastern end of the lake on 1 August 1997. Densities in lations were constant and similar in all lakes. The the north-western end of the lake, which was used as a refer- similarity was even more striking in a smaller prey, ence, are shown on the left (details in Gliwicz & Dawidowicz, 2001). The difference in roach distribution between the two areas D. cucullata, which is an order of magnitude more became apparent 1 day after the treatment. Echograms were abundant than D. hyalina in all lakes (details in generated by HADAS from data recorded by an EY-M 70 kHz Gliwicz et al., 2000). 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?

The constant population density of both Daphnia species in the three lakes, and the fixed density pushed down to the deeper strata (Fig. 5) and cut difference between the two species, gave us a hint to short from the half-metre-deep outflow. This hap- the nature of the disparity between top-down and pened, for example, after the treatment on 9 August bottom-up impacts. Population densities remained 1996, in the north-western end of the experimental constant, although the intensity of reproduction dif- lake. The number of roach leaving the lake declined fered greatly among the lakes and months with ) from pretreatment values of 600–700 fish day 1 (up to different food levels (Gliwicz et al., 2000). It was also ) 280–350 fish h 1 in the middle of the night) to uniform along the long axis of the experimental lake ) ) 10–20 fish day 1 (up to 10 fish h 1 in the middle of and highly akin to those observed in 14 neighbouring the night), while the numbers of roach entering the lakes showing a wide range in food levels (assessed as lake were unaffected (Gliwicz et al., 1998). chlorophyll a concentrations in the size fraction Secondly, although after each treatment nearly 300 <50 lm; details in Gliwicz, 2001). These observations roach intestines were inspected from trawl samples are not unique. Other coexisting Daphnia species also taken in both areas of the lake, no difference in have been found with ‘fixed’ or ‘species-specific’ feeding intensity was observed in any body-size density levels in many lakes (e.g. Kasprzak, Lathrop category (Gliwicz et al., 1998). Variability in the & Carpenter, 1999). However, the phenomenon has roach diet was unusually high (Fig. 6), and the not attracted much attention in the literature and mean prey selectivity index was very similar for all plausible answers to the questions have not been five major prey species, an unusual observation. For proposed until recently. One possible answer is that example, the index was nearly the same for the two the population density of a given cladoceran species is Daphnia species (details in Wisńiowska, 1999), fixed from the top-down by fish predation at a ‘species- although different body sizes should have translated specific population-density threshold’ level, irrespective

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 2302 Z. Maciej Gliwicz

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 Wisńiowska, 1999).

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 Top-down versus bottom-up effects 2303

Vanderploeg Ivlev & Scavia Mean 1

0 –0.59

–1 Bosmina 1 0 –0.65

–1 D. cucullata 1

0 –0.67

–1 D. hyalina 1

0 –0.67

–1 Leptodora 1

0 –0.83

–1 Chaoborus 0 4 8 12 0 4 8 12 Roach body length (cm)

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 Wis´niowska, 1999).

100 10 m) 10

– 10 (0

2 1 – m 4 0.1

Ind.10 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 2304 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 Fig. 9 Diagrammatic representation of the difference in reactive greater for the larger Daphnia species (Fig. 9). This distance (i.e. the distance at which foraging fish would see prey) for two prey categories, which results in relative reactive field difference should be reflected in different densities of volumes for, and thus relative prey density assessment by, a the two prey species in the lake, as was actually foraging planktivore such as roach. As a 2 : 1 difference in the found in a range of lakes and various seasons radius of the two spheres gives a 10 : 1 difference in volume, (Fig. 8). foraging fish would assess densities of two prey categories as equal when relative prey densities differ 10-fold, as they do in Moreover, at the 10 : 1 ratio of the species-specific case of the two Daphnia species shown in Fig. 8 (details in densities of the two Daphnia species, the selectivity Gliwicz, 2001). 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 whose individuals are most conspicuous and most deviates from 1 : 1, corresponding to a real density rewarding. They are also, however, generalist preda- ratio of 10 : 1 (Fig. 9). This ratio was found in our tors that tend to feed upon the most abundant prey, gut-content data set for roach (Fig. 7), suggesting shifting to the prey category that is most rewarding as that prey vulnerability is not only generated exclu- a result of both the properties of an individual prey sively by the properties of an individual, but also by item and the density of the prey population. the properties of a population. Prey choice was thus The two predatory behaviours are not mutually not only related to the profitability of a single prey exclusive. On the contrary, they must be combined item, but also to the rewards resulting from the and co-ordinated with each other in every decision density of the prey population (planktivorous fish concerning prey choice, regardless of whether the section). 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 Planktivorous fish: selective or general predators? O’Brien, Slade & Viniard (1976), in which a plankti- Are planktivorous fish selective or generalist preda- vorous fish is assumed to select prey actively, tors? Our data of roach gut-contents would seem to pursuing whichever prey appears largest. In addition, show that, although the fish are selective, they should two feeding modes must be compromised in a also be considered generalist predators. They are decision to switch from one prey population to selective in that they would consume the prey species another, such as choosing to feed on a prey category

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 Top-down versus bottom-up effects 2305 that has just been found to be more rewarding, as in field studies examined selectivity in response to prey the model of Murdoch (1969) and Murdoch, Avery & body-size and overall prey abundance. Some of the Smyth (1975). recent studies focused ‘on effects of body size and More rewarding prey may be the prey category zooplankton abundance’ in regard to the functional (species or single ontogenetic stage) that is relatively response (e.g. Johnston & Mathias, 1994). An excep- more abundant or offers a higher net energy gain, tion is Luo, Brandt & Klebasko (1996), who were able given the energy or time invested in a successful to predict the size frequencies of zooplankton prey in individual encounter and ⁄or found by the fish to be anchovy stomachs from the ambient zooplankton most efficient to capture. Each of the three reasons body-size frequencies found in the habitat (mid- should be an equally valid justification for switching Chesapeake Bay). from prey item A to prey item B as soon as B becomes The mutual importance of prey body size and prey more rewarding. Most experimental evidence show- population density as two determinants of food ing a switch to more rewarding prey comes from selectivity in a typical planktivore has recently laboratory studies examining predator switching gained attention, following the realisation that a lake between different patches of prey or between different with an indigenous fish fauna has species-specific feeding habitats, rather than between prey categories population-density thresholds for each cladoceran in a homogeneous mixture of different prey, the real prey category. The threshold density is inversely situation encountered by a planktivorous fish in the related to the individual susceptibility of each field. Field observations focus on the switch between cladoceran species to predation, which is most habitats of different food profitability (e.g. Werner, strongly related to body size at first reproduction Mittelbach & Hall, 1981), or different risk to predation (species-specific population-density thresholds sec- (e.g. Hall et al., 1979; Gliwicz & Jachner, 1992), rather tion). The gut contents of roach from our experi- than on the switch from one food category to another mental lake showed high variability in individual in response to a change in their relative abundance roach diets (Fig. 6) and in the selectivity index for (Murdoch & Bence, 1987). different prey categories (Fig. 7) probably because of Although it is well known that planktivorous fish frequent switching among prey categories. will switch from one zooplankton species to another Part of this variability may be an effect of on a seasonal (Eggers, 1982) or daily basis (Hall et al., switching on a daily basis, especially when the 1979), the importance of prey relative abundance has switch is to or from phantom midge larvae (Chaobo- mostly been ignored in the quest for understanding rus spp.), which were frequently the sole prey found the phenomenon of prey switching and of food in the roach guts (Fig. 6). Such a switch may require selectivity in planktivorous fishes in general. The a shift between two different habitats, the cladocer- focus was on prey relative body size, and the an-rich epilimnion and the deeper strata where question of prey abundance was confined to the Chaoborus can be encountered on the evening forays importance of overall prey density, and an increase offshore, before light intensity becomes too low to in density that would enhance selectivity for more allow foraging roach to detect their prey (Fig. 2). conspicuous prey. The phenomenon that selectivity The behaviour of dailyswitching may also be behind is increased via an increase in the overall density of the high variability of the selectivity index within a prey has been known since the pioneering work of narrow size category of fish, a majority with values Ivlev (1961), and was experimentally explored by close to either )1 or +1 (Fig. 7). This suggests that an Werner & Hall (1974). These authors allowed prey individual roach may prey upon small-bodied Bos- categories, different D. magna instars, to differ in mina or D. cucullata on one evening, but on larger body size and overall abundance, while keeping the D. hyalina on the evening after. This possibility is relative abundance of the prey categories constant. also reflected by the dominance of different prey Relative prey density was often touched on in categories in similar-sized roach guts from the same theoretical approaches (Gerritsen & Strickler, 1977; trawl sample (Fig. 6). Eggers, 1982; Wetterer & Bishop, 1985; Giske, Huse However, a significant part of the high diet variab- & Fiksen, 1998), but was ignored in experimental and ility appears to result from more frequent switching, field studies on planktivorous fish. Experimental and rather than from the daily (whole-evening) shift

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 2306 Z. Maciej Gliwicz between different prey categories. In 60% of all 264 that general predators feed most heavily upon the roach inspected, the diet diversity expressed as a prey most abundant species until their abundance is Shannon-Wiener index (based on species contribution reduced, and that ‘the predator switches the great to the total food volume) was above 0.4, which proportion of its attack to another prey which has corresponds with the diet of fish number 4 in Fig. 6. become the most abundant’ (Murdoch, 1969). Or – as The diverse food composition of an individual roach we should say more precisely being aware of the would suggest that most individuals switch from one effect of body size – relatively the most abundant prey category to another many times within a single (Gliwicz, 2001). For example, it may be speculated feeding session offshore. In its evening thrust towards that that the prey-switching behaviour was the reason the middle of the lake, where zooplankton prey is why the selectivity for Bosmina was found to be more abundant, a foraging roach may slow down to slightly higher than for other prey in our experimental pick up a number of prey of one category, and then lake (Fig. 7). Unlike the other prey species, the move forward again as soon as a local swarm has been Bosmina population may have been just in the phase wiped out. It can do so again with another prey of density increase beyond its species-specific thresh- category once that other prey has been assessed as old level at the time of our fieldwork on the lake. This more rewarding. may also be the reason why the food selectivity for a Since the pioneering work of Ivlev (1961), Hrba´- specific prey was neither found to be similar among cˇek (1962), and Brooks & Dodson (1965), the effect individual fish, nor significantly different for different of predation by planktivorous fish has been prey species, even those representing extremes in assumed to be selective. Our analyses show that body size. this assumption is correct, but only in the sense that High variability of the selectivity index for differ- each different body-sized species has a different ent prey categories is often a source of frustration for population-density threshold that results from a researchers analysing gut contents; they prefer find- different relative reactive field volume. Thus, once ing high values for conspicuous and low values for the relative proportions of coexisting species have less conspicuous prey species (e.g. Bohl, 1982). Clear been fixed by body-size dependent mortality, the differences in selectivity values, which are probably effect of predation is not selective anymore. On the less common than published accounts imply, could contrary, the force of fish predation appears to be a be interpreted as a sign that a change in the strong stabilising factor accounting for constant dominant diet is being witnessed, the majority of relative densities of different prey species through- fish switching from one prey to another ‘which has out the seasons and from one habitat to another become the most abundant’ (Murdoch, 1969), just as (Fig. 8). There are opposing forces that stem from could be the case of Bosmina in our experimental the race between individuals of each population to lake. grow and mature soonest. This is the reason for each population to show a reproductive rate as high Zooplankton in the presence and absence of fish as possible within the constraints set by temperature and food levels, whereas birth rates in the popula- By switching from one zooplankton prey to another, tion and the rate of population increase are con- planktivorous fish would hold the density of each trolled by either time or resources (the ‘time and species below the carrying capacity (K). Each density resource limitation’ of Schoener, 1973). increase would be followed by a shift in fish diet from It thus appears that the availability of resources the most rewarding prey in the past to the most controls the rate of each population increase. Regard- rewarding prey in the present situation (Fig. 10, top). less of the rate of increase, the density of each The most conspicuous prey (the large-bodied and population would eventually be fixed by a mortality thus competitively superior species) would be held at rate resulting from fish predation and fish switching the lowest density, corresponding to its low ‘relative from one prey item to another depending on their density’ resulting from the high vulnerability of relative densities (species-specific population-density individuals at maturation (large body size at first thresholds section). This conclusion is in agreement reproduction). Low abundance would allow for with a notion expressed a long time ago (Elton, 1927): higher food levels, and thus for the coexistence of

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 Top-down versus bottom-up effects 2307 Daphnia density would decrease, chlorophyll concentration increase, and ‘ecological space’ become avail-

K able to other cladocerans and rotifers that are inferior 100 competitors for resources. This situation appears to be typical of ponds and lakes, where the impact of ﬁsh 50 allows for the coexistence of many species with similar ecological niches, including congeneric species such as D. hyalina and D. cucullata (species-speciﬁc 0

Population density (% ) population-density thresholds section). Concurring 0 30 60 90 120 with Hutchinson’s (1961) ‘paradox of the plankton’ Elapsed time (days) (e.g. Ghilarov, 1984), diverse plankton assemblages have often been accounted for by non-equilibrium

) effects based on the intermediate disturbance hypo- 1 – thesis, or justiﬁed by different abilities to partition 100 100 ) 1 – resources (reviewed by Rothhaupt, 1990). A diverse g L

µ community of planktonic herbivores would also be 50 50 seen following any long-lasting phase of clear-water resulting from a temporary relaxation in fish activity and periodic single-Daphnia-species monopolising 0 0 Chorophyll ( 03060 90 120 resources. This situation has been observed in many Population density (ind.L Elapsed time (days from 1 April 1972) lakes and is well known as ‘Daphnia summer decline’ which usually follows a ‘spring clear-water phase’ Fig. 10 Top panel: Diagrammatic representation of a typical (Sommer, 1989; Hu¨ lsmann & Voigt, 2002). change in population density of a planktonic herbivore, such as The only natural habitats in which the clear-water Daphnia or Bosmina in the absence and presence of planktivorous fish. Bottom panel: example of a real density change of a phase lasts as long as in Smyslov Pond, are those Daphnia population in the absence of fish impact in Smyslov where fish are absent, and a competitively superior Pond in 1972. High numbers of Daphnia pulicaria accompanied large-bodied phyllopode such as D. pulicaria or D. galeata by smaller numbers of (solid line) lasted in equilib- Artemia franciscana monopolise resources, holding rium for 90 days with low levels of small edible algae (dotted line) and high levels of mineral resources, until extermination of them at an equilibrium level below the threshold D. pulicaria by fish (day 100) allowed other zooplankton taxa to food concentration needed for other species to grow form a typical multispecies zooplankton community and algae and reproduce (Gliwicz, in press). In such fishless l )1 to form a bloom of 70 g chlorophyll L , typical of Smyslov habitats, where water remains clear in spite of high Pond (after Fott et al., 1974; and Fott, Desortova & Hrbaćˇek, 1980). nutrient loads, phytoplankton would be suppressed from the top down by the competitively superior herbivore species, whose high population density in other species, including small-bodied cladocerans, turn is restrained from the bottom up by food rotifers and ciliates. This coexistence may last at least availability. The absence of predation allows an until the fish impact has been removed. For example, individual to allocate all its efforts to the competi- in Smyslov Pond, one of Hrbaćek’s famous fishponds tion for resources, as interspecific competition gives in Bohemia, large-bodied D. pulicaria was found to way to intraspecific competition. In the fertile monopolise resources for 90 days in the absence of habitat of the Great Salt Lake, Utah, the diverse fish predation (Fig. 10, bottom). phytoplankton is held at an extremely low biomass ) The Smyslov Pond example shows that, in the (1 lg chlorophyll L 1) by an efficient herbivore, absence of fish, Daphnia density can be controlled Artemia. When Artemia is removed experimentally from the bottom up and held at the equilibrium level or has retreated naturally to diapause, mineral of the carrying capacity of the habitat. Algal food resources are immediately monopolised by the most resources would be effectively controlled from the top effective green algae, Dunaliella viridis, leading to a ) down, well below their high potential, until fish feed concentration of 30 lg chlorophyll L 1 (Gliwicz, in again on Daphnia. With fish predation restored, press).

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 2308 Z. Maciej Gliwicz Such situations observed in fishless habitats sug- This conclusion is supported by our data, at least as gest that population densities of both phyto- and regards the herbivorous zooplankton. Fish predation zooplankton and body size of zooplankton species at would primarily determine the population density in first reproduction may be controlled from the bottom a herbivore such as Daphnia. It would do so regardless up as long as the top-down impact is effective. High of the somatic growth rate of individual animals, and zooplankton densities cannot last, however, after the the population reproduction rate, which are both impact has been removed. As soon as fish are independent of top-down effects. These rates are introduced, herbivore population density and body bottom-up controlled. The different nature of this size becomes fixed by top-down forces again, and bottom-up control is best reflected in the notion of the bottom-up controls become restricted to rates at which functional response, the processes of food assimil- density or body size can be restored to levels that ation, individual growth, and population increase, would be fixed by fish predation. 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 Conclusions that ‘low food level would not necessarily be equal The species-specific population-density thresholds in with food limitation in animals such as Daphnia cladocerans, the similar values for the selectivity because even at low food levels food production index in roach, and the contrast between zooplankton may be high enough to support high feeding rates and in the presence and absence of fish, all show that an fast individual growth’ (an anonymous review, pers. impact from the top-down can control zooplankton comm.). This would be the case as long as the top- biomass, individual body size and population density. down impact of predators was effective. Its removal In contrast, bottom-up forces influence assimilation would allow a single competitively superior species to rate, individual growth rate and reproduction monopolise resources at an equilibrium level held (Fig. 11). The nature of the impacts from top down near the food-threshold level, as in the fish-free and bottom up hence is distinctly different also at the habitats of alpine and saline lakes (zooplankton in population level. Although in contrast to the individ- the presence and absence of fish section). The same ual level a common currency can be conveniently reasoning is probably valid for the other trophic levels defined at the population level, the disparity of the in the food web, both primary producers and pred- two entities are equally great at both levels. ators.

BOTTOM-UP: TOP-DOWN:

Fig. 11 Diagrammatic representation of the different nature of bottom-up (food limitation) and top-down impacts (pre- CONTROL OF STATE VARIABLES dation) on zooplankton, with its abundance (biomass) controlled from the top Assimilation (A) Biomass down by planktivorous ﬁsh (right), and Individual growth rate Individual body size process rates (energy ⁄ carbon ﬂow) controlled from the bottom up by phyto- Rateof reproduction Population density plankton food availability (left).

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 Top-down versus bottom-up effects 2309

CONTROL OF RATES CONTROL OF STATE VARIABLES

Assimilation (A) Biomass Individual growth rate Individual body size Rate of reproduction Population density

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 density cannot be expected if the above scenario is top-down impact of grazing imposed by herbivores correct. rather than by the trophic state of the habitat. This Thus, with the reasoning from Fig. 11 applied to the effect would be most apparent in the absence of fish, trophic level above (Fig. 12). I hypothesise that only as low phytoplankton abundance is comparable in the state (biomass and population density) of plank- fishless habitats regardless of their potential, from tivorous fish affects the strength of top-down control, ultra-oligotrophic mountain lakes to nutrient-rich not the rate at which the fish reproduce, grow, or feed. saline lakes of hydraulically locked lowlands. The The same effect might account for the fragility of low-biomass multispecies phytoplankton of these effective top-down control: the spring clear-water habitats would last as long as the top-down impact phase is usually a short phenomenon and can, if it of an effective herbivore persists. Its removal would lasts longer, be abruptly terminated as seen in Smy- allow single algal species to monopolise resources at slov Pond. The effect may also be the reason why top- an equilibrium level with mineral resources kept low, down effects are gradually weakened from the top to as in the fish-free habitat of the Great Salt Lake the bottom of the food web as suggested by McQueen (Section 6). et al. (1989). Experiments run in the Plankton Towers These mechanisms could also explain why our at the Max-Planck Institute in Plo¨n, Germany, showed efforts at mediating roach feeding behaviour in the that the top-down effects on roach can be very strong, experimental lake were unsuccessful (modifying fish but also that they are only transitory: fish frightened feeding behaviour section). We attempted to reduce with alarm substance were more reluctant to feed in roach feeding rate, not roach density or biomass, that the daylight than the reference fish, but the initial is a rate, not a state variable. Although treatment with difference in food abundance in the evening (Daphnia alarm substance could possibly affect roach density in density) vanished overnight because fish fed in the the long term, a short-term increase of zooplankton dark (Gliwicz et al., 2001).

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2296–2312 2310 Z. Maciej Gliwicz Acknowledgments Gliwicz Z.M. (2001) Species-specific population-density thresholds in cladocerans? Hydrobiologia, 442, 291–300. I am thankful to two anonymous reviewers for valuable Gliwicz Z.M. (in press) Between hazards of starvation and comments and multiple suggestions on the earlier fear of predation: the ecology of an offshore animal. version of the manuscript, and to Mark Gessner for Inter-Research Science Publisher, Oldendorf ⁄ Luhe. thorough editorial improvements. The study was Gliwicz Z.M. & Dawidowicz P. (2001) Roach habitat supported by a grant from the European Commission to shifts and foraging modified by alarm substance. 1. Z.M. Gliwicz, W. Lampert, V. Korinek and M.J. Boavida Field evidence. Archiv fu¨r Hydrobiologie, 150, 357–376. (Grant no. CIPA-CT93-0118-DG 12 HSMU) and a grant Gliwicz Z.M., Dawidowicz P., Jachner A. & Lampert W. from the Polish Committee for Scientific Research to (2001) Roach habitat shifts and foraging modified by Z.M. Gliwicz (Grant no. PO4F-074–14). alarm substance. 2. Reasons for different responses of fish in field and laboratory. Archiv fu¨r Hydrobiologie, 150, 377–392. References Gliwicz Z.M. & Jachner A. (1992) Diel migrations of juvenile fish: a ghost of predation past or present? Benndorf J. (2002) Top-down control of lower trophic Archiv fu¨r Hydrobiologie, 124, 385–430. levels: the role of time scale, lake depth and trophic Gliwicz Z.M. & Jachner A. (1993) Lake restoration by status. Freshwater Biology (in press). manipulating the behaviour of planktivorous fish with Bohl E. (1982) Food supply and prey selection in counterfeit information on risk to predation. Verhan- Oecologia planktivorous Cyprinidae. , 53, 134–138. dlungen der Internationalen Vereinigung fu¨r Theoretische Brooks J.L. & Dodson S.I. (1965) Predation, body size and und Angewandte Limnologie, 25, 666–670. composition of plankton. Science, 150, 28–35. Gliwicz Z.M., Lampert W., Korinek V. & Boavida M.J.L. Carpenter S.R., Cole J.J., Hodgson J.R., Kitchell J.E., (1998) Controlling the behavior of planktivorous fish Pace M.L., Bade D., Cottingham K.L., Essington T.E., with counterfeit information on risk to predation. Final Houser J.N. & Schindler D.E. (2001) Trophic cascades, Report European Union Project No CIPA-CT. 93–0118, nutrients, and lake productivity: whole-lake experi- 80 pp. ments. Ecological Monographs, 71, 163–186. Gliwicz Z.M., Rutkowska A.E. & Wojciechowska J. (2000) Drenner R.W. & Hambright K.D. (1999) Review: bioma- Daphnia populations in three interconnected lakes with nipulation of fish assemblages as a lake restoration roach as the principal planktivore. Journal of Plankton technique. Archiv fu¨r Hydrobiologie, 146, 129–165. Research, 22, 1539–1557. Eggers D.M. (1982) Planktivore preference by prey size. Hall D.J., Werner E.E., Gilliam J.F., Mittelbach G.G., Ecology, 63, 381–390. Howard D. & Doner C.G. (1979) Diel foraging Elton C.S. (1927) Animal Ecology. Macmillan, New York. behaviour and prey selection in the golden shiner Fott J., Desortova B. & Hrbaćˇek J. (1980) A comparison of (Notemigonus chrysoleucas). Journal of the Fisheries the growth of flagellates under heavy grazing stress Research Board of Canada, 36, 1029–1039. with a continuous culture. Continuous Cultivation Ho¨lker F., Haertel S.S., Steiner S. & Mehner T. (2002) of Mcroorganisms. Proceedings of 7th Symposium, Effects of piscivore-mediated habitat use on growth, July 10–14, 1978, Czechoslovak Akademy of Science, diet and zooplankton consumption of roach: an Prague, 395–401. individual-based modelling approach. Freshwater Fott J., Korinek V., Prazakova M., Vondrus B. & Forejt K. Biology, 47, 2345–2336. (1974) Seasonal development of phytoplankton in fish Hrbaćˇek J. (1962) Species composition and the amount of ponds. Internationale Revue der Gesamten Hydrobiologie, zooplankton in relation to the fish stock. Rozpravy 59, 629–641. Ceskosloveske Akademie Ve´d, Rada Matematicko-Prirodove- Gerritsen J. & Strickler J.R. (1977) Encounter probabilities decka, 72, 1–114. and community structure in zooplankton: a mathema- Hu¨ lsmann S. & Voigt H. (2002) Life history of Daphnia tical model. Journal of the Fisheries Research Board of galeata in a hypertrophic reservoir and consequences of Canada, 34, 73–82. non-consumptive mortality for the initiation of a Ghilarov A. (1984) The paradox of the plankton midsummer decline. Freshwater Biology, 47, 2313–2324. reconsidered; or why do species coexist? Oikos, 43, Hutchinson G.E. (1961) The paradox of the plankton. 46–52. American Naturalist, 95, 137–146. Giske J., Huse G. & Fiksen Ø. (1998) Modelling spatial Ivlev V.S. (1955) Eksperimentalnaya ekologia pitanya dynamics of fish. Reviews of Fish Biology and Fisheries, 8, ryb. Piscepromizdat, Moskva, 251 pp. 57–91.

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