Effects of Piscivore-Mediated Habitat Use on Growth, Diet and Zooplankton Consumption of Roach: an Individual-Based Modelling Approach

Freshwater Biology (2002) 47, 2345–2358

Effects of piscivore-mediated habitat use on growth, diet and zooplankton consumption of roach: an individual-based modelling approach

FRANZ HO¨ LKER,* SUSANNE S. HAERTEL,*, † SILKE STEINER* and THOMAS MEHNER* *Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Berlin, Germany †University of Konstanz, Limnological Institute, Konstanz, Germany

SUMMARY 1. We used an individual based modelling approach for roach to (i) simulate observed diel habitat shifts between the pelagic and littoral zone of a mesotrophic lake; (ii) analyse the relevance of these habitat shifts for the diet, activity costs and growth of roach; and (iii) quantify the effects of a hypothetical piscivore-mediated (presence of pikeperch) confinement of roach to the littoral zone on roach diet, activity costs and growth. 2. The model suggests that in the presence of pikeperch, roach shifts from zooplankton as the primary diet to increased consumption of less nutritious food items such as macrophytes, filamentous algae and detritus. 3. The growth of roach between May and October was predicted to be significantly higher in the absence of pikeperch, although the net activity costs were about 60% higher compared with the scenario where pikeperch were present. 4. These modelling results provide quantitative information for interpreting diel horizontal migrations of roach as a result from a trade-off between food availability and predation risk in different habitats of a lake. 5. Altering the habitat selection mode of planktivorous roach by piscivore stocking has the potential to reduce zooplankton consumption by fish substantially, and could therefore be used as a biomanipulation technique complementing the reduction of zooplanktivorous fish.

Keywords: biomanipulation, food uptake, habitat shift, IBM, Rutilus rutilus, trait–mediated indirect interactions

stay in the open water or among littoral vegetation Introduction may therefore be viewed as a trade-off between food The pelagic and littoral zones are two contrasting uptake and predator avoidance (Werner et al., 1983). habitats for planktivorous fish in lentic freshwaters. Such predator-induced modifications of prey traits While vertical gradients of light, temperature and (behaviour, phenotype, or life history) may indirectly other factors are the main structuring forces in the effect prey resources and consequently prey compet- pelagic zone, the littoral zone is characterised by a itors. They are termed trait-mediated indirect interac- high structural complexity. Structures such as macro- tions (Abrams, 1995). phyte beds can provide fish a refuge from predation Roach [Rutilus rutilus (L.)] is a successful generalist (Persson, 1993), but may also reduce feeding rates fish in European freshwater habitats (Schiemer & (Winfield, 1986; Diehl, 1988). The decision whether to Wieser, 1992). Roach of age-classes 1 and older often show diel horizontal migrations. They may shift from Correspondence: Franz Ho¨lker, Leibniz-Institute of Freshwater littoral to pelagic habitats and between different food Ecology and Inland Fisheries, Mu¨ggelseedamm 310, D-12587 items when a specific food component is abundant or Berlin, Germany. E-mail: [email protected] predation risk is high (Gliwicz & Jachner, 1992;

2002 Blackwell Science Ltd 2345 2346 F. Ho€lker et al. Brabrand & Faafeng, 1993; Persson & Eklo¨v, 1995). The importance of diel habitat shifts for an indi- Roach is a generalist feeder, suggesting that vegetated vidual fish and thus the entire population is extremely littoral zones may be a rather attractive habitat in difficult to study in the field. Food consumption and terms of food supply (e.g. Ho¨lker & Breckling, 2001). growth are key factors to consider. The food con- However, foraging of roach for zooplankton is more sumption rate of a fish is determined by food efficient in the pelagic zone (Winfield, 1986; Persson, availability, body size, physiological condition, and a 1987). Therefore, the pelagic zone may be a profitable number of abiotic parameters such as water tempera- feeding habitat for roach, especially when the abun- ture, light conditions and season (Jobling, 1994). The dances of both macrozoobenthos and zooplankton are individual-based modelling approach allows the spe- low in the littoral zone. cification of a population in terms of its individuals. In predator-exclusion experiments, roach showed a To analyse gains and costs of activities associated with preference for open-water habitats (Jacobsen et al., different habitat choices, it is necessary to specify 1997). Day-active predators such as perch (Perca behavioural variability and activity patterns of indi- fluviatilis L.) or pike (Esox lucius L.) are important vidual fish (Ho¨lker & Breckling, 2002). To date, piscivorous predators in European lakes and can however, most individual-based models have simply cause major habitat shifts in roach (Eklo¨v& followed the fates of individuals in a population VanKooten, 2001). In field enclosure experiments, without taking behavioural decisions into account roach moved into or stayed close to the vegetation (Huse, Strand & Giske, 1999). in the presence of piscivorous perch (Eklo¨v& In this study, we used an individual-based model VanKooten, 2001). Conversely, in the presence of (1) to investigate whether roach benefit energetically pike, which stayed mainly within or near macrophyte from diel habitat shifts in the absence of night active beds, roach used almost exclusively the open-water piscivores such as pikeperch, even though the migra- habitat. In the presence of both predators, roach used tion may be associated with higher metabolic costs; vegetated areas and thus became more susceptible to (2) to quantify the effects of the assumed piscivore- pike predation, and they foraged during twilight and mediated habitat use on roach diet and growth after a occasionally during the night in the pelagic zone hypothetical stocking with pikeperch; and (3) to (Eklo¨v & VanKooten, 2001; Haertel, Baade & compare the seasonal consumption of several pelagic Eckmann, 2002). zooplankton groups by roach in the absence and Another important predator in European lakes is presence of pikeperch. pikeperch [Sander lucioperca (L.)]. This species is a pelagic piscivore that unlike perch and pike is most active during twilight and at night (Craig, 1987). Methods Roach <20 cm have been found to be confined to the Study site littoral zone when pikeperch were abundant in a number of Dutch, Norwegian and German lakes Großer Va¨tersee is situated in the Baltic lake region of (Lammens et al., 1992; Brabrand & Faafeng, 1993; north-eastern Germany (5300¢N, 1300¢E). It has a Laude et al., 2000). Thus, when all these predatory maximum depth of 11.5 m, a mean depth of 5.2 m, fishes are present, the feeding impact of roach should and a surface area of 12 ha. The lake has been be primarily directed towards littoral prey species characterised as mesotrophic, with a mean epilimnetic ) during the entire day. As a consequence, the pelagic total phosphorus concentration of 24 lgL1 during zooplankton community would be protected by a 1995–97. Secchi depth was never below 2.0 m behaviourally induced ‘refuge’ effect. This effect (Kasprzak et al., 2000). The lake is thermally stratified would largely decouple the pelagic food web at the from late April to late October, with an anoxic zone up fish-zooplankton link. In spite of this potential, pisci- to 7 m water depth (Kasprzak et al., 2000). Extensive vore-mediated trait modification of zooplanktivorous parts of the littoral zone in Großer Va¨tersee are fish (e.g. altered habitat selection mode, reduced covered by dense stands of Vaucheria dichotoma (L.) activity) to release predation pressure on zooplankton 18% of the total lake area in 1995 and Chara spp. (17% indirectly has received little attention in the context of of the total lake area in 1995; Kasprzak et al., 2000). In biomanipulation (Jacobsen et al., 1997). 1994 and during 1997–99, roach and perch were the

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 Effects of habitat use on diet and growth of roach 2347 dominant fish species in terms of both abundance and zone throughout the day because of the abundance biomass, although age-0 roach recruitment between of piscivores (hereafter referred to as ‘pikeperch’ 1997 and 1999 was low (Radke, 1998; Haertel et al., scenario). 2002). With about 8.7 cm total length at the beginning The simulation programme is written in SIMULA of their third year in 1998, roach grew slowly in and represents a range of structural and functional Großer Va¨tersee (Haertel & Eckmann, 2002), as is aspects of an individual fish and its environment as a characteristic of mesotrophic lakes in the region set of classes. Each of these classes operates on an (Radke, 1998). Age-1 and older roach in addition to, independent updating schedule. The environmental temporarily, age-0 perch are the main vertebrate classes specify factors such as light conditions, tem- predators of cladocerans in the pelagic zone. Pike perature, sight range and abundance of food items. (Esox lucius L.) and perch ‡ 20 cm are the most The FISH class of the model mainly consists of important top predators. Great crested grebes [Podi- bioenergetic parameters, rules for energy allocation ceps cristatus (L.)] were present in small numbers and re-allocation, and rules for scheduling beha- (Haertel et al., 2002). vioural and physiological activities. The latter are Roach of age-classes 1 and older stayed in the used to determine the activity of individuals in littoral zone during daytime and were found in the response to both their internal condition and the pelagic zone at night and twilight (Haertel et al., 2002). environmental context. Additionally, the rules define Food availability for roach was low in the littoral the response of individual roach in relation to their zone, because both macrozoobenthos and zooplank- conspecifics (Ho¨lker & Breckling, 2002). The simula- ton were scarce (Radke, 1998; F. Ho¨lker & S.S. Haertel, tion programme reads several input data sets (see unpublished data), but dense submerged macrophyte details below), including a grid map of the lake, data beds (Kasprzak et al., 2000) provide refuge against on the physical habitat structure, light conditions, predation. The pelagic zone of Großer Va¨tersee would temperature and food availability, and data describ- be expected to be a more profitable feeding habitat for ing the initial status (sex, bioenergetics, behaviour) of roach, but because large piscivorous perch (Perca each individual fish used in the simulation. State fluviatilis L.) occur in this habitat, the daytime preda- variables are, for example, the internal physiological tion risk is probably high (Craig, 1987). conditions (hunger status, status of internal energy Since 1997, ‘cascading trophic interactions’ and the compartments, body size). relative importance of ‘top-down’ versus ‘bottom-up’ control under mesotrophic conditions are studied in Modelling the environment Großer Va¨tersee. Piscivore biomass was increased greatly in 2001 and 2002 by stocking pikeperch [Sander The model environment consists of a habitat represen- lucioperca (L.); age 2+, n ¼ 930], and food-web inter- tation on a grid map and data sets on microclimate, actions before and after this biomanipulation are daytime length and food availability. The grid map is quantified (Kasprzak et al., 2000). based on a bathymetric map of Großer Va¨tersee (Kasprzak et al., 2000). Each grid element has a surface area of 400 m2 and represents the entire water column Modelling approach from the surface to the lake bottom. Following Haertel We used a physiological, spatio-temporal and indi- et al. (2002), the areas with a water depth <3.0 m were vidual-based model that was originally developed for defined as the littoral zone. Water temperature was a roach population of a eutrophic lake in northern recorded in 1 m water depth. Mean daily values based Germany (Ho¨lker, 2000; Ho¨lker & Breckling, 2002). on hourly measurements were used as input para- We first parameterised the model for the conditions of meters. The CBM daylength model of Forsythe et al. Großer Va¨tersee. Next, we compared the simulated (1995) was used to compute daytime length as a diet composition, food consumption and growth of function of latitude and date throughout the season. roach for a model scenario that mimicked the Civil twilight was defined as the period between observed diel migrations in the unmanipulated sunrise or sunset and the time when the centre of the lake (hereafter referred to as ‘pikeperch-free’ scenario) sun is 6 below the horizon. Dissolved oxygen and to a model scenario restricting roach to the littoral turbidity were not considered in the simulations.

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 2348 F. Ho€lker et al. The food organisms are represented in the model as sampling sites at a water depth of 0.5 m. Benthic habitat-specific density variables. They consist of six insect larvae were sampled at three sites at water different categories: Daphnia spp., other cladocerans, depths of 0.5 and 3 m in May, August and October Chaoborus flavicans (Meigen) larvae (3rd and 4th 1998 (F. Ho¨lker & S.S. Haertel, unpublished data). instars), benthic insect larvae, plants and detritus. Plants and detritus were sampled in the littoral zone Roach of the modelled age-class do not feed on in May, July and September 1998. The caloric content copepods or molluscs in Großer Va¨tersee (Haertel & was determined by bomb calorimetry (Haertel & Eckmann, 2002). Mean abundances, energy contents, Eckmann, 2002). The abundance and, where appro- wet weights and water contents of the different food priate, mean individual biomass of each food category categories during 1998 are summarised in Table 1. throughout the summer were calculated by linear Vertical migration of cladocerans was not considered interpolation between sampling dates. in the simulations. However, first results indicate that migration of larger cladocerans in Großer Va¨tersee Modelling the FISH was not mediated by the habitat use of roach in 1998 because both species occurred in the upper water An essential element of the class FISH is the so-called layer of the pelagic zone from dusk till dawn ‘life loop’ (Fig. 1). As long as the FISH life-status (S. Steiner, unpublished data). variable is ‘true’, the programme will execute this loop Pelagic zooplankton was collected with a cone- and call appropriate activity procedures. A HOLD shaped plankton net (length 1.2 m, opening 0.027 m2, procedure interrupts the execution of the FISH life loop mesh size 90 lm). Chaoborus larvae were collected at and leaves a notation in the internal execution time- least 2 h after sunset using a closing net (length 1.5 m, table to continue execution one time-increment diameter 0.4 m, mesh size 150 lm). For both groups, forward. To specify the behavioural variability and triplicate vertical hauls from 0 to 10 m were taken activity pattern of individual roach, we integrated biweekly in 1998 (Kasprzak et al., 2000). Densities of specific information on roach from field studies in zooplankton and Chaoborus larvae refer to the epilim- Großer Va¨tersee (Haertel et al., 2002; Haertel & netic volume from 0 to 6–9 m. Littoral zooplankton Eckmann, 2002), laboratory experiments (Ho¨lker, was sampled monthly with an Schindler trap at four 2000), and the literature (e.g. Hammer, Temming &

Table 1 Mean abundance, wet weight (mean with range in parentheses) during May to October, and energy and water content of different food categories in the littoral and pelagic zone of mesotrophic Großer Va¨tersee. Pelagic abundances refer to the epilimnetic volume from 0 to 6–9 m depth between May and October 1998

Abundance ) ) (N L 1,Nm 2 Energy content Water ) ) Food category Habitat for insect larvae) Wet weight (mg N 1) (kJ g dw 1) content (%)

Daphnia spp. Pelagial 23 (1–70)* 0.0044 (0.0013–0.0084)* 20.1– 80** Daphnia spp. Littoral 2 (0–3)† – 20.1– 80** Other cladocera Pelagial 20 (1–73)* 0.0014 (0.0004–0.0031)* 20.1– 80** Other cladocera Littoral 8.1 (3–11)† – 20.1– 80** Chaoborus ﬂavicans Pelagial 0.119 (0.034–0.328)‡ 0.230 (0.087–0.319)‡ 20.7†† 80** (third and fourth instar) Insect larvae (without odonata) Littoral 115 (42–207)† 1.001† 21.1– 81– Plants Littoral – 9.4§ 83§ Detritus Littoral – 6.5§ 71§

*S. Steiner (unpublished data). †Ho¨lker & Haertel (unpublished data). ‡I. Ja¨ger (unpublished data). §Haertel & Eckmann (2002). –Hepher (1988). **Winberg et al. (1971). ††Cummins & Wuycheck (1971).

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 Effects of habitat use on diet and growth of roach 2349 have the value true or false and trigger the corresponding habitat selection and swimming modes (Table 2). ) Swimming velocities of 0.2–1.6 body lengths s 1 ) (mean of 0.4 body lengths s 1) were found in laboratory experiments for adult roach (Hammer et al., 1994) and were defined in the model as the preferred range. A fish outside an area providing favourable conditions switches to increased swimming speed per time step and to a reduced turning angle until it reaches a favourable area. There, the fish switches to a decreased swimming speed and a greater turning angle. This habitat selection mode is modelled in connection with the energetic requirements for the involved activities (Ho¨lker & Breckling, 2002; Appen- dix). The movement of a simulated roach follows a ‘correlated random walk’. This means that the swimming direction and turning angle are calculated stepwise with a defined random deviation. The corresponding procedures in the process class FISH calculate fish movement steps and new position in the lake every 5 min; the movement steps are preserved in corresponding variables. The probability distribution of the new turning angle consists of a normal distribution with a distinct standard deviation Fig. 1 Life loop of an individual roach within the model class depending on light conditions and habitat type FISH. As long as the FISH life-status variable is ‘true’, the pro- (Table 3). The actual swimming speed is calculated gramme will execute a life loop. Inside the loop, the individual’s by multiplying the preferred swimming speed with a internal physiological status (e.g. hunger status) and its envi- swimming factor that also depends on light condi- ronment are assessed and appropriate activity procedures are called. tions and habitat type (Table 3). Any change in velocity is overlaid with a stochastic aspect, normally Schubert, 1994). An individual roach in the model distributed with a standard deviation of 0.5 m per responds to a set of environmental stimuli (light, 5 min. Vertical movement was modelled by assuming temperature, habitat type) by preferably staying in a that fish maintain their swimming depth and over- favourable area. The internal physiological status of a laying a random vertical deviation of the turning roach is controlled by Boolean variables that either angle followed by a return to horizontal movement.

Table 2 Design of the habitat selection mode of roach under two model scenarios. The internal physiological status of an individual roach is controlled by Boolean variables that trigger the selection of the respective habitat preferences and activity modes

Physiological status (Boolean variable) Hungry Not hungry

Pikeperch-free scenario Light condition Night Twilight Day Night Twilight Day Habitat preference Pelagial Pelagial Littoral Pelagial Pelagial Littoral Swimming mode Low-cost High-cost High-cost Low-cost Low-cost Low-cost Pikeperch scenario Light condition Night Twilight Day Night Twilight Day Habitat preference Littoral Littoral Littoral Littoral Littoral Littoral Swimming mode Low-cost High-cost High-cost Low-cost Low-cost Low-cost

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 2350 F. Ho€lker et al.

Table 3 Parameterisation of the correlated random walk of simulated roach. Any change of direction is overlaid with a stochastic aspect. The probability distribution of the new turning angle consists of a normal distribution with a distinct standard deviation SD (). The preferred swimming speed of roach is 0.4 body lengths per second. The actual swimming speed is calculated by multiplying the preferred swimming speed with a swimming factor depending on light conditions and habitat

Littoral Pelagial

Light Swimming Horizontal change, SD () Swimming Horizontal change, SD () conditions factor of normal distribution factor of normal distribution

Pikeperch-free scenario Day 0.5 130 4.0 45 Twilight 4.0 45 1.0 130 Night 4.0 45 1.0 130 Pikeperch scenario Day 0.5 130 4.0 45 Twilight 0.5 130 4.0 45 Night 0.5 130 4.0 45

The model calculates the speed and the direction of periodically over 24 h in Großer Va¨tersee (Haertel & an individual in relation to all other roach in sight. Eckmann, 2002). The status ‘hungry’ causes a specific The reaction distance to conspecifics at daylight and food-searching mode, which requires more energy twilight is assumed to be 12 m during 5 min of than straight swimming (Wieser, 1991; Ho¨lker, 2000). simulation time. The list of visible shoal members is A roach strives to achieve Cmax, defined by its size updated and a new centre of the shoal is computed. and the surrounding water temperature. To predict Turning angle and swimming direction are calculated the consumption rates of roach for the food categories according to the shoal centre with a random deviation Daphnia spp., other cladocerans and C. flavicans larvae as shown in Table 3. At night, the shoals disperse and in the pelagic zone, and for benthic insect larvae in the demonstrate no longer shoaling behaviour. littoral zone, roach were assumed to capture prey Information on the distribution and diet of roach in according to a Holling type II functional response the lake were taken from Haertel et al. (2002) and (Holling, 1959) in an approximate version given by Haertel & Eckmann (2002), where roach were Persson (1987): sampled simultaneously from both the littoral and C ¼ aN=ð1 þ ahNÞ pelagic zone during the day (from 10 a.m. until noon) r )1 and immediately after nightfall. Sampling was per- where Cr is the capture rate (prey s ), a is the attack formed monthly with gill nets (bottom set and coefficient, h is the handling time (s), and N is the prey ) ) floating, respectively) of 8–15 mm bar mesh size. density (L 1 or m 2 for planktonic and benthic prey, Roach in Großer Va¨tersee stay in the littoral zone respectively). Because high densities of submerged during daytime, and prefer the pelagic zone at night. macrophytes reduce zooplankton consumption rates The offshore and onshore migrations take place in roach, only one third of the pelagic consumption during dusk and dawn, respectively. This pattern of rates of Daphnia spp. and other cladocerans was roach distribution was set as a target for the para- assumed to be realised in the littoral zone (Winfield, meterisation. A simulated roach has the status ‘hun- 1986). Though our simulations did not take the anoxic gry’ as long as its consumption is below the maximum hypolimnion into account, we assumed that roach are consumption rate (Cmax; Appendix). Because orienta- unable to feed on benthic invertebrates under anoxic tion of roach for catching zooplankton is visual (Bohl, conditions. Therefore, macrozoobenthos is assumed to 1982), the status ‘hungry’ was considered possible be available only in the littoral zone. Functional during daytime and twilight only. At night, the status response curves could not be formulated for macro- hungry is turned to ‘false’, which is in agreement with phytes, filamentous algae and detritus, because the feeding patterns derived from fish samples taken densities of these food categories in Großer Va¨tersee

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 Effects of habitat use on diet and growth of roach 2351 are unknown. However, daily rations of plant mater- ﬁsh (Hepher, 1988). These costs were added to the ial and detritus derived from bioenergetics modelling standard metabolic rate of roach (Appendix). of roach were available for the period from May to September 1998 (Haertel & Eckmann, 2002). Based on Parameterisation of the model for Großer Va¨tersee these data, we calculated a mean consumption rate for detritus and a temperature-dependent consumption The model was parameterised to cover the major rate for plant material for the daytime hours (littoral aspects of a roach’s life from the beginning of the residence) of each day. As long as a simulated roach growing season 1998 in May (Julian day 133) to stays in the littoral zone, both food items are therefore October (Julian day 312). To start a simulation run, 100 constantly consumed at the respective rate. The roach of age 3+ were placed into a starting area. This ) handling time is assumed to be 60 s mg 1 wet weight age-class dominated the roach population in 1998 for both food categories. Within the model, roach was (Haertel et al., 2002). Depending on its internal phy- assumed to prefer benthic prey over cladocerans in siological status and time of the day, each simulated the littoral zone (Ho¨lker & Breckling, 2001), and roach seeks a favourable habitat by using the respect- cladocerans over C. ﬂavicans larvae in the pelagic zone ive activity mode (Tables 2 and 3). As long as a roach

(Haertel & Eckmann, 2002). As chaoborids are found has not achieved its maximum daily ration (Cmax), e.g. in the epilimnion of Großer Va¨tersee only from dusk during daylight, it has the status ‘hungry’, switches to till dawn (I. Ja¨ger, unpublished data), the model the activity mode ‘food searching’ (high-cost swim- assumes that Chaoborus is available only during the ming pattern), and seeks the littoral zone. The result- night. ing consumption rate follows the respective functional In order to simulate the flow and storage of energy, response curves. A roach first meets its costs for the roach’s energetics was divided into five compart- maintenance and activity and only allocates resources ments with specific functions (Ho¨lker, 2000): the gut, to growth when food assimilation exceeds the imme- the short-term carbohydrate storage, the medium- diate metabolic demands. term fat storage, the long-term protein storage, and a Following Ho¨lker & Breckling (2001), we iteratively reproduction compartment. The reproductive com- calibrated and connected the simulated movement of partment was modelled separately because of its high roach and its energetic needs with empirical data on dynamics, although it also consists of carbohydrates, growth and food composition in Großer Va¨tersee. The fat and protein. The assimilated energy (consumed following criteria were used: energy minus energy losses in faeces and ammonia • Start values for iterations were the mean total and urea excretions) was used for either respiration or length (8.7 cm) and the mean weight (5.9 g) of 3+ growth. Energy contained in biomass may also be roach in Großer Va¨tersee in 1998 (Haertel & Eckmann, re-allocated, which results in an additional fractional 2002). energy loss by respiration. All of these physiological • Target values were the seasonal increment in total processes are integrated into the model as procedures length, the food composition and the habitat selection of the class FISH. The corresponding bioenergetic pattern observed for 3+ roach in Großer Va¨tersee parameters and equations are listed in the Appendix. during May to October 1998. Following Haertel et al. To take the metabolic costs of activity into account, (2002), the probability of simulated roach to stay in the the model links fish behaviour to the energetic preferred habitat at a given time of the day was set at requirements for that activity. Relationships between >90% (±10%). the swimming speed and metabolism were deter- • The attack coefficients, a, and the handling times, mined for roach swimming against a unidirectional h, derived from the Holling type II functional current of constant velocity in laboratory experiments response curve served as the search parameters for (Ho¨lker, 2000). Net swimming costs for both low-cost the food categories Daphnia spp., other cladocerans, and high-cost swimming pattern were estimated and C. flavicans larvae. The optimised parameters are using an empirically determined relationship between given in the Appendix. The parameters given by oxygen consumption, fish biomass and average swim- Ho¨lker & Breckling (2001) were used for benthic ming speed (bootstrap statistics, n ¼ 60). The oxica- insect larvae because of the fragmentary data set )1 loric value was set as 14.2 J mg O2 for omnivorous for Großer Va¨tersee. A temperature-dependent

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 2352 F. Ho€lker et al. consumption rate was assumed for macrophytes and were highest near shore during the daytime. How- filamentous algae, and a constant rate for detritus ever, because of the random character of the correla- (Appendix). ted random walk, the simulated roach were never found exclusively in the more favourable area of the lake. Results Distinct diel differences in the diet of roach were found in the simulation (Fig. 3). During the daytime, Habitat use and food consumption when simulated roach were found onshore, 50–80% To ascertain whether our assumptions of a random- of the consumed prey biomass were littoral food type movement of roach led to a realistic habitat items. At night, when roach stayed mainly in the selection mode, the output data for roach under the pelagic zone, their food was dominated by pelagic pikeperch-free scenario are visualised in Fig. 2. In zooplankton (60–90%). The match with observed diet accordance with observations in Großer Va¨tersee, the composition during night (60–90% pelagic zooplank- simulated roach were mainly found in the pelagic ton) was quite good. However, the proportion of zone from dusk to dawn, whereas simulated densities littoral food items during daytime (70–95%) was higher than found empirically. Differences may be partly because of the temporally discrete sampling in the empirical study. As in the model output, the proportion of cladocerans in the diet of roach during daytime was higher, when roach were sampled in 2 h intervals over 24 h (Haertel & Eckmann, 2002). The simulated daytime diet composition shown in Fig. 3b was therefore used as the target value for zooplankton consumption of roach for subsequent modelling. Roach consumed higher amounts of food during the daytime (up to 0.4 g wet weight per individual) than at night ( £0.12 g; Fig. 3c). Overall food consumption was highest from week 21 (26 May) to week 27 (7 July) and decreased towards the end of the season (Fig. 3c). Under the pikeperch scenario, the habitat use of roach (Fig. 4) differed distinctly from that under the pikeperch-free scenario (Fig. 2). Densities of simulated roach were highest in the littoral zone throughout the day (Fig. 4). As a result, the proportion of pelagic zooplankton in the nocturnal diet was reduced to 10–20%, whereas the proportion of less profitable food items such as vascular plant tissue and detritus reached up to 80% (Fig. 5a). The daily consumption rate decreased slightly to a maximum of 0.35 g wet weight per individual during the daytime. At night, ) there was a strong decrease to 0.06 g wet weight fish 1 (Fig. 5b).

Activity and growth differences

2 For the simulated period of 239 days, an individual Fig. 2 Cumulated counts of 100 roach in 400 m horizontal grid elements in Großer Va¨tersee under the pikeperch-free scenario roach had net activity costs of 46 kJ under the (computed as one count for every 5 min). pikeperch-free scenario and of 28 kJ under the pike-

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 Effects of habitat use on diet and growth of roach 2353

Fig. 3 (a) Empirically determined diet composition (% prey volume) during 1998 (based on data in Haertel & Eckmann, 2002) (b) simulated diet composition in percentage prey biomass, and (c) simulated food consumption (prey wet weight - ) ﬁsh 1) of roach during the daytime and at night (including twilight) in mesotrophic Großer Va¨tersee under the pikeperch-free scenario. perch scenario. This means that over the season roach zone of Großer Va¨tersee (S. Steiner, unpublished spent about 40% less energy on swimming when data). The consumption of other cladocerans by roach restricted to the littoral zone throughout the day. The peaked during the summer maximum of this food net activity costs accounted on average for 1.0 times category. Consumption under the pikeperch-free ) ) (range 0.5–2.7 times) the costs of the standard meta- scenario averaged 208 g wet weight ha 1 day 1 on ) ) bolic rate under the pikeperch-free scenario and for Daphnia spp. and 155 g ha 1 day 1 on other cladoc- 0.7 times (0.3–1.8) under the pikeperch scenario. The erans, whereas the pikeperch scenario resulted in a ) ) pikeperch-free model scenario predicted well the predation of 22 g ha 1 day 1 on Daphnia spp. and of ) ) seasonal increment in total length of roach observed 50 g ha 1 day 1 on other cladocerans. Consumption empirically in 1998 (Fig. 6). A signiﬁcantly lower under the pikeperch scenario was thus reduced by seasonal length increment resulted from the pike- factors of 10 and 3, respectively. perch model scenario (Fig. 6; Mann–Whitney U-test, P < 0.05). Discussion

The modiﬁcation of roach activity and phenotype Effects of the habitat selection mode of roach observed in the presence of pikeperch in our simula- on consumption of cladocerans tions are a typical example of trait-mediated indirect The consumption of Daphnia spp. and other cladocer- species interactions as described by Werner & Peacor ans by roach was estimated as the product of mean (in press). The simulated increase in the predation risk individual daily rations and the abundance of 3+ roach in the pelagic zone of Großer Va¨tersee resulted in a taken from Haertel et al. (2002). Under the pikeperch- modiﬁcation of several traits in roach: a changed free scenario, the consumption of daphnids by roach habitat selection mode, a decreased foraging activity, was highest during spring and autumn (Fig. 7), when and a decreased growth, which may eventually result daphnids were also most abundant in the pelagic in a delayed age at maturity. Increased predation risk

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 2354 F. Ho€lker et al. et al., 1992; Brabrand & Faafeng, 1993; Laude et al., 2000). These findings contrast with observations in a biomanipulated hypertrophic reservoir where age-0 roach were occasionally found in the pelagic zone even during daytime (Mehner et al., 1998). However, the structural complexity created by macrophytes in this reservoir is low and daytime pelagic residence of roach was restricted to periods with low water transparency. Thus, a littoral preference of roach after stocking with pikeperch can realistically be expected for mesotrophic Großer Va¨tersee with a well-developed littoral zone. We addressed the question whether diel horizontal migrations of roach are energetically profitable in Großer Va¨tersee by comparing diet composition, individual consumption rates, activity costs and growth over the season for both scenarios. The simulated shift in the diet of roach from primarily zooplankton to plants and detritus (pikeperch scenario) is in agreement with empirical studies where increased resource limitation led to a proportionally increased consumption of less nutritious, non-animal food items (Persson, 1993). Our simulation results suggest that there is a clear bioenergetic advantage for roach to perform diel onshore-offshore migrations in Großer Va¨tersee. Horizontally migrating dace (Phoxi- nus eos · P. neogaeus) in a small Canadian lake also had, despite higher activity costs, a net benefit compared with conspecifics that were experimentally restricted to the littoral zone (Gauthier & Boisclair, 1997). The merit of our modelling exercises is that they provide quantitative information for interpreting diel horizontal migrations as a result of a trade-off Fig. 4 Cumulated counts of 100 roach in 400 m2 horizontal grid between food availability and predation risk in elements in Großer Va¨tersee under the pikeperch scenario different habitats. (computed as one count for every 5 min). The biomanipulation approach has traditionally focused on the reduction of fish predation on can thus affect one or two major components of zooplankton by reducing zooplanktivorous fish abun- individual fitness in fish (Gliwicz & Jachner, 1992). A dance through intensive fishing and ⁄or stocking of limitation of our simulations is, however, that they do piscivores (Benndorf, 1995; Mehner et al., 2002). Our not consider the actual mortality of roach through model predictions for Großer Va¨tersee suggest that predation. influencing the habitat selection of planktivorous fish The rigid littoral-oriented habitat selection mode may also substantially (up to tenfold) reduce assumed for the pikeperch scenario is in good zooplankton consumption by fish. This approach thus agreement with empirical data. Pikeperch is primarily appears to have great potential for biomanipulation pelagic and mostly active during twilight and at night purposes, as has been suggested earlier by Gliwicz & (Craig, 1987). Accordingly, roach <20 cm in total Jachner (1993). However, competition among other length have been repeatedly found to be confined to planktivorous species (e.g. perch or invertebrate the littoral zone when pikeperch is present (Lammens predators such as Chaoborus or Leptodora) and ⁄or year

2002 Blackwell Science Ltd, Freshwater Biology, 47, 2345–2358 Effects of habitat use on diet and growth of roach 2355

Fig. 5 Diet composition in percentage prey biomass (a) and food consumption (b) of 100 simulated roach at daytime and night (including twilight) under the pikeperch scenario.

Fig. 7 Simulated consumption of Daphnia spp. and other cladocerans by roach under the pikeperch-free and pikeperch Fig. 6 Seasonal increment in total length (mean ± 1 SD) for 3+ scenarios in mesotrophic Großer Va¨tersee. Consumption was roach observed in mesotrophic Großer Va¨tersee during 1998 calculated as the product of mean individual daily ration (prey (based on data in Haertel & Eckmann, 2002), simulated under wet weight) and fish abundance. the pikeperch-free model scenario, and simulated under the pikeperch model scenario. classes (e.g. 0+), or other indirect mechanism may Acknowledgments weaken or even nullify the predicted effect (cf. Gliwicz, 2002). For example, decreased predation We would like to thank the two referees as well as the by planktivorous fish on Chaoborus can result in editor, J. Benndorf, for their valuable comments, I. Ja¨ger increased invertebrate predation on Daphnia, which for providing unpublished data, and M. Valentin and can potentially overcompensate the decreased preda- C. Helms for technical support. This work was funded tion by fish (Benndorf et al., 2000). The investigation of in part by DFG grants Ec 146 ⁄2-1+2 and Me 1686 ⁄4-1+2. the effects induced by the recent stocking of Großer Va¨tersee with pikeperch will provide insights to what References extent our model predictions on the trophic structure of a mesotrophic lake hold under biomanipulation Abrams A.A. (1995) Implications of dynamically variable conditions. traits for identifying, classifying, and measuring direct

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Appendix Initial conditions and main parameter values for roach. The relationship between prey density (N) and capture rate

(Cr) was obtained from an approximate version of the Holling II equation (a ¼ attack coefﬁcient, h ¼ handling time). Standard )1 metabolic rate and net swimming costs of roach follow a relationship between oxygen consumption (mg O2 h ), ﬁsh weight W (g), ) temperature T (C) and, in the case of net swimming costs, average swimming speed, U (cm s 1). Defaecation and excretion are ) dependent on consumption, C (J day 1) and Temperature, T (C)

Parameter name Symbol Value or equation Unit Reference

General Number of fish N 100 Total length of fish at start L 8.7 cm Haertel & Eckmann (2002) Wet weight of fish at start W 5.9 g Haertel & Eckmann (2002) Environment Size of grid element on lake map 400 m2 Time of the day CBM model Forsythe et al. (1995) Consumption Attack coefficient for insect larvae a 0.0000028 Ho¨lker & Breckling (2001) Handling time for insect larvae h 6.9 s Ho¨lker & Breckling (2001) Attack coefficient for Daphnia spp. a 0.025 This investigation Handling time for Daphnia spp. h 1.2 s Attack coefficient for other cladocerans a 0.07 This investigation Handling time for other cladocerans h 0.6 s Attack rate for Chaoborus flavicans larvae a 0.01 This investigation Handling time for Chaoborus flavicans larvae h 7.0 s )1 )1 Capture rate Cr aN (1 + ahN) prey s Persson (1987) ) Consumption rate for plants (wet weight) 0.125 T – 1.5 mg 5 min 1 Based on Haertel & if T > 10.84 C Eckmann (2002) ) Consumption rate for detritus (wet weight) 0.18 mg 5 min 1 Based on Haertel & Eckmann (2002) 0.84 (0.133 T) )1 Maximum daily ration (wet weight) Cmax 0.016 W e g day Ho¨lker (2000) Respiration 0.76 (0.088 T) )1 Standard metabolic rate 0.034 W e mg O2 h Ho¨lker (2000) 1.22 0.89 )1 Low-cost swimming pattern 0.0012 U W mg O2 h Ho¨lker (2000) 0.64 0.60 )1 High-cost swimming pattern 0.07 U W mg O2 h Ho¨lker (2000) ) Costs of specific dynamic action 0.19C J day 1 Wieser & Medgyesy (1990) 1 Oxicaloric value 14.2 J mg O2 Hepher (1988) Excretion ) ) Defaecation of insect larvae 0.571 C0.861 e( 0.0502 T) J day 1 Ho¨lker (2000) ) ) Defaecation of zooplankton 0.727 C0.842 e( 0.0502 T) J day 1 Ho¨lker (2000) 1.049 ()0.0584 T) )1 NH4-N excretion of insect larvae 0.0783 C e J day Ho¨lker (2000) 1.046 ()0.0584 T) )1 NH4-N excretion of zooplankton 0.0912 C e J day Ho¨lker (2000) ) ) Urea-N excretion of insect larvae 0.0503 C0.825 e( 0.0357 T) J day 1 Ho¨lker (2000) ) ) Urea-N excretion of zooplankton. 0.0695 C0.860 e( 0.0357 T) J day 1 Ho¨lker (2000) Growth Capacity of short-term buffer (wet weight) 0.6–1.7 % Shimeno et al. (1990) Capacity of medium-term buffer (dry weight) 1.4–29.3 % Pfeiffer (2000) Fractional loss in reallocating energy ) From short and medium-term buffer to respiration 5 % (J J 1) Van Winkle et al. (1997) ) From short and medium-term buffer to gonads 10 % (J J 1) Van Winkle et al. (1997) ) From gonads to respiration 7.5 % (J J 1) Van Winkle et al. (1997) ) From long-term buffer to respiration 10 % (J J 1) Van Winkle et al. (1997) ) From long-term buffer to gonads 15 % (J J 1) Van Winkle et al. (1997) Swimming Preferred range of swimming speed U 0.2–1.6 Body Hammer et al. (1994) ) lengths s 1 ) Change of velocity (SD) 0.5 m 5 min 1 Shoal size N £ 50 Haberlehner (1988) ) Sight range 12 m 5 min 1

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