Behavioral Ecology Advance Access originally published online on April 13, 2005
Behavioral Ecology 2005 16(4):741-746; doi:10.1093/beheco/ari047
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Effects of water-level fluctuations on the littoral benthic fish community in lakes: a mesocosm experiment
Limnological Institute, University of Konstanz, Mainaustrasse 212, 78457 Konstanz, Germany
Address correspondence to P. Fischer. E-mail: philipp.fischer{at}uni-konstanz.de.
Received 28 October 2003; revised 9 March 2005; accepted 15 March 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Changes in the water level of lakes, either natural or man-made, are important environmental perturbations for eulittoral benthic fish communities. In outdoor mesocosm experiments, we tested the effects of decreasing shelter availability due to autumn lake-level decrease on the behavior and the growth of two littoral benthic dwellers, the juvenile burbot and the stone loach. The two species showed significantly different changes in behavior when shelter availability decreased. Burbot built up a distinct hierarchy when shelter became sparse, with larger fish being significantly more successful in competing for suitable shelter than smaller conspecifics. The hierarchy, however, ceased when shelter availability decreased below a certain level. The largest fish then increasingly abandoned shelter use, while smaller fish persisted with their sheltering behavior. Stone loach, in contrast, showed no hierarchical order or size-related shelter use. Only burbot showed a significant relationship between the ability to occupy the preferred shelter and the somatic growth. These two species provide an example of different strategies to deal with environmental perturbations like lake-level decrease, with the stenoecious, dominant strategy of the burbot and the euryoecious, evasive strategy of stone loach. The results demonstrate the importance of conducting behavioral studies under as natural conditions as possible.
Key words: Barbatula barbatula, competition, dominant, growth, Lota lota, social behavior.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Water-level fluctuations, either natural or man-made, severely affect habitat availability in the littoral zone of lakes (Gasith and Gafny, 1990
). Especially in large lakes with an extensive, shallow slope littoral area, water-level fluctuations may become the major factor controlling the temporal and spatial distribution of the eulittoral community. A variety of studies (Gotceitas and Godin, 1992; Imre et al., 2002; Reinhardt, 1999; Sloman et al., 2001) on the population structure within eulittoral fish communities showed that seasonal fluctuations in the water level not only determine the presence or absence of any species in a temporally inundated area but can provoke complicated changes in the community structure of the eulittoral community.
Significant insights into the effects of lake-level draughts on the community structure in fish populations have been made by Sloman et al. (2001, 2002). They found that unstable environmental conditions like droughts significantly altered dominance structure in a trout community that was stable under experimentally constant conditions (Sloman et al., 2002). These and other authors therefore stress the need to conduct behavioral studies on social interactions in fish under situations that are as representative of natural conditions as possible including perturbations (Imre et al., 2002; Reinhardt, 1999; Sloman and Armstrong, 2002; Sloman et al., 2001).
Compared to epibenthic dwellers like trout, strictly benthic fish species are even more affected by changes in water level because they rely on specific substratum characteristics. In previous work, we showed that juvenile burbot, a widely distributed benthic dweller in the northern hemisphere, show severe stress symptoms and significantly elevated metabolism when displaced from their preferred shelter due to intraspecific competition from larger conspecifics (Fischer, 2000a,b). However, as criticized by Imre et al. (2002), Reinhardt (1999), and Sloman et al. (2001), this test system was entirely stable with respect to shelter availability. Therefore, this result may not be relevant when the abiotic environment becomes dynamic and shelter availability decreases, as in an autumnal lake-level drought condition.
In the present study, we therefore tested the effect of drought-induced decreasing shelter availability on the behavior, dominance structure, and growth rates of two common benthic dwellers in Northern European large lakes: the juvenile burbot Lota lota L. and the stone loach Barbatula barbatula (L.).
We wanted to study the responses of these two species to decreasing shelter availability to elucidate their behavioral strategies to cope with such changes in the environment. Furthermore we wanted to explore if increasing competition for daytime shelter also affected somatic growth of the fish and therefore long-term fitness.
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METHODS |
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All fish used in the experiments were caught by beach seining in the littoral zone of Lake Constance and were stocked in two glass tanks (50 x 40 x 50 cm) for 3 weeks prior to further handling. During this time the fish were kept under a light regime similar to the natural light rhythm and were fed daily with chironomid larvae. After this time, fish were tagged with passive integrated transponders (TROVAN, 18 x 2 mm, glass encapsulated) injected into the body cavity as recommended by Prentice et al. (1990)
. The passive integrated transponder tag enables individual fish to be identified by a unique 10-digit alphanumeric code read in situ with a portable transponder decoding system. The tagged fish were held for 2 weeks posttagging for observation. No tagging-induced mortality occurred.
All experiments were done in two outdoor mesocosms with 2 x 2 m base dimension and 40 cm water depth during summer 2001. The length range of the juvenile burbot was 11.9–18.8 cm (total length [TL]) and that of the stone loach 8.0–11.0 cm, which matched the length ranges of juvenile burbot and stone loaches in situ in the littoral zone of Lake Constance (Hofmann and Fischer, 2001).
Shelter preference without conspecific interactions
Shelter was provided by dark PVC tubes with different diameters. PVC tubes have been shown to be superior to stones as experimental shelter because burbot and stone loach accept these objects as shelter as readily as stones (Fischer P, personal observation) and the tubes provide defined interstice space.
To determine the effects of intraspecific competition on the shelter selection of each individual fish in a group of conspecifics, we first tested the shelter tube preference of each fish when alone. We offered each fish six PVC tubes with diameters of 24, 21, 18, 16, 14, and 11 mm (200, 180, 160, 145, 132, and 112 mm length) in a single experiment lasting for 5 days each. Shelter tube diameter preference of each fish was checked once a day between 1500 and 1730 h (except for two occasions when the check was done at 1830 h) with a hand-held tag reader. The tag reader had a reading distance of about 15 cm and therefore allowed data collection without physically touching the tubes or fish. This procedure was chosen because Fischer (2000a) showed that burbot and stone loach are nocturnal and choose their daytime shelter during the preceding dawn. To prevent shelter tube selection due to habituation or due to odor tracks (a fish may smell the shelter that it has used the night before), all tubes were replaced once a day with clean tubes that were randomly distributed within the experimental area. This shelter replacement procedure was done during dusk because both species are most active during this phase of the day and then leave their shelter (Fischer, 2000b), which then can be carefully replaced without disturbing the fish. These single-specimen experiments were performed with 36 juvenile burbot and 36 stone loaches for 5 days each (a total of seventy 5-day experiments).
Shelter preference with conspecific interactions
To determine the effects of intraspecific competition during decreasing shelter availability, we performed experiments with groups of nine fish (either burbot or stone loach) randomly selected from the fish tested in the single-specimen experiment in the same mesocosm as the solitary experiments. This procedure allowed us to calculate changes in shelter selection due to conspecific company individually for each fish. The same shelter tubes used in the single-specimen experiments were offered to the group, but with three tubes per diameter. Therefore, a total of 18 tubes (3 x 24 mm, 3 x 21 mm, 3 x 18 mm, 3 x 16 mm, 3 x 14 mm, and 3 x 11 mm) were available for each group (nine fish) at the beginning of each experiment. Similar to the single-specimen experiment, the shelter use of each fish in the group was tested for 5 days.
At day 6 of the experiment, we started to simulate decreasing shelter availability by sequentially removing the available shelter tubes in the mesocosm in weekly steps, beginning with the largest shelter tubes. We began with the largest tubes because stone size and therefore substratum interstice size is often significantly correlated with lake level, and when the lake level decreases, the largest stone sizes normally fall dry first (Gafny et al., 1992). After removing the first of the three largest (Ø 24 mm) shelter tubes at day 6, (only two 24-mm tubes were left in the system), the fish had 2 days to adapt to the new situation, after which the shelter use of each individual fish was tested again for 5 days. After this time, another of the largest shelter tubes (Ø 24 mm) was removed and only one 24-mm tube remained. After the 2-day acclimation phase, the shelter selection was again measured for 5 days. After this time the next tube was removed (no more 24-mm tubes were left) and so on. Shelter availability and shelter diameter thus successively decreased over time, simulating the in situ lake-level decrease in autumn. For each of the two species, four identical replicate experiments with different fish were conducted. The experiments were planned to run for a maximum of 9 weeks when only one tube per fish would remain in the system (3 x 16 mm, 3 x 14 mm, and 3 x 11 mm). The experimental time per treatment, however, was shortened to only 4 weeks during the course of the experiments because of significant behavioral changes in juvenile burbot with respect to shelter use (see Results).
Calculating effects of intraspecific competition
To quantify the effect of intraspecific competition for shelter for each individual fish in the group, we calculated the degree of deviation in shelter tube use between the fish when solitary (Experiment 1: single-specimen experiment) and when in a group of conspecifics (Experiment 2: group experiment). We first calculated a frequency distribution of shelter tube diameter use for each fish in the single-specimen experiment and then calculated an identical frequency distribution of shelter tube diameter use for each fish in the group experiment. Separate frequency distributions were calculated for each period of constant shelter availability (one frequency distribution for each 5-day measuring phase, during which the number of available shelter tubes were not changed).
The effect of intraspecific competition on the individual fish at decreasing levels of shelter availability was then calculated as the degree of deviation between these two shelter-use frequency distributions. The degree of deviation was calculated with standard likelihood-ratio chi-square statistics (Sachs, 1997). This analysis provides a single positive test statistic, the Hpx value, which is a linear-scaled measurement for the degree of deviation of the two frequency distributions. An Hpx value of 0 therefore indicates two identical shelter-use frequency distributions, while an increasing Hpx value characterizes increasing differences among the two compared frequency distributions. Even though the likelihood-ratio chi-square statistic is somewhat conservative, it has the advantage of providing one linear-scaled test value (Hpx) that (1) quantifies the difference between two frequency distributions and (2) can be used in further statistical treatments (Kullback, 1959; Theil, 1972). Due to a nonnormal distribution of the calculated Hpx values (Kolmogorov-Smirnov, Dk = 0.1877, p < .001), all Hpx values were square-root transformed to achieve normal distribution (Kolmogorov-Smirnov, Dk = 0.080, p > .05) prior to further statistical analysis. In case of correlation analysis, outlier classification was done by using the standard R-Student statistic (SAS/STAT, 1988). Studentized residual absolute values >2 were classified as outliers and removed from the analysis (SAS, 1998).
The somatic growth (weight increase [g-wet] over the experimental time) of all fish was measured to estimate physiological effects of intraspecific competition for the individual fish in the group. To compare the somatic growth of burbot or stone loach among the different treatments (week 1–week 4), growth was corrected for size using data from daily growth rates of 50 burbot and 38 stone loach of different sizes that were measured under identical experimental conditions but without conspecific competition. The observed growth in the group experiments was standardized to the average body weight for each species used in the group experiment.
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RESULTS |
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Shelter preference of solitary fish
In 70.4% of 235 single-specimen trials with burbot, solitary fish used the largest shelter tube offered (Ø 24 mm), (Table 1). The two smaller shelter tubes (Ø 21 and 18 mm) were only used for 17.4% and 11.7% of the trials, and juvenile burbot never used smaller shelter tubes. Furthermore, in solitary burbot larger fish used larger tubes significantly more often than did smaller fish (F1,54 = 14.00, r = .46, p = .0004).
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In contrast, stone loach showed no preferences for a particular shelter tube size when alone, except for the smallest one (Ø 11 mm), which was used in only 0.7% of all observations (Table 1). Furthermore, no significant relationship between the size of a fish and the size of the preferred shelter tube was found.
Shelter use of fish in conspecific company
Juvenile burbot changed their shelter tube use significantly when living in a group of conspecifics (t = 5.32, df = 35, p < .001). During the first week of the group experiment, when 9 fish and 18 shelter tubes were present in the mesocosm, the three largest tubes available (Ø 24 mm) were used in only 43.0% of all observations compared to 70.4% in the single-specimen trials. The next smaller tubes (Ø 21 and 18 mm) were used for 38.8% (17.4% in the single-specimen trials) and 17.5% (11.7% in the single-specimen trials). The 16-mm tube was used in 1.1% of the cases (0% in the single-specimen trials).
During week 1 of the group experiment, a weak but significant negative correlation (r = –.33; F1,34 = 4.198, p < .048; Figure 1a) was established between the TL of a fish in the group and its potential to occupy its preferred shelter tube size (the tube diameter that the fish preferred in the single-specimen trial).
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After removing the first large shelter tube (Ø 24 mm) at day 6 of the group experiment, the strength of the size-dependent shelter selection significantly increased. Smaller fish were now significantly more often displaced from their originally preferred shelter tubes to smaller tubes, while the remaining larger tubes were almost exclusively occupied by the larger conspecifics (r = –.71; F1,2 = 32.51, p < .0001; Figure 1b).
This size-related shelter-selection behavior persisted during week 3 of the experiment after the second large shelter tube (Ø 24 mm) was removed (Figure 1c, F1,29 = 10.59, p = .029), although the strength of this relationship decreased (r = –.51).
After removing the third 24-mm shelter tube at day 19 of the group experiment, no more size-dependent shelter selection was observed, and fish seemed to select shelter tubes at random, independent of their body size and original preferences (Figure 1d, F1,12 = 0.44, p = .51, r = –.20).
Stone loaches showed similar significant differences in shelter tube selection when living in a group of conspecifics compared to solitary fish (Figure 1e–h; average deviation value Hpx = 8.16 ± SD 1.69; df = 35, t = 5.32, p < .001). However, significant size-dependent shelter selection was observed only in week 2 of the experiment (Figure 1f; F1,25 = 5.829, p = .023, r = +.42). Interestingly, this relationship was positive and therefore inverse to that observed in juvenile burbot, with larger group members being more often displaced from their preferred shelter tubes compared to smaller conspecifics.
Growth rates
The success of a fish in selecting its preferred shelter tube size under conspecific competition was significantly correlated with its somatic growth. With an average growth of 0.34 g day–1 (maximal 0.46 g day–1), burbot with the lowest Hpx values (lowest deviation between shelter size selection when alone and in the group) showed a significantly higher growth compared to fish with higher Hpx values (Figure 2a, F1,22 = 19,84, p = .0002, r = .69).
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Stone loach have a significantly lower growth rate compared to juvenile burbot (Figure 2b). In the group experiments, stone loach showed an average growth of 0.024 g day–1) and no significant correlation was found between the success of a fish to use its preferred shelter and its somatic growth (Figure 2b, F1,23 = 1.73, p = .21, r = .26).
Overall changes in shelter-selection behavior
Besides size-related changes in shelter selection in the presence of conspecifics, burbot additionally changed their shelter-use behavior proper during the course of the experiment. Solitary fish as well as fish from the group experiment during week 1 were observed outside a shelter tube during daytime in only 8.8% of all cases. This percentage increased to 17.7% in week 2 (–1 shelter tube) to 25.5% in week 3 (–2 shelter tubes) and 26.1% in week 4 (–3 shelter tubes) (Figure 3a). This shelter-abandonment behavior was significantly related to the size of the fish (Figure 3b; F26,110 = 2.89, p < .0001) with none of the "no daytime shelter use" observations belonging to the smallest size class of fish (LT = 11 cm) and 45% belonging to the largest size class (LT = 18 cm). Contrary to the juvenile burbot, stone loach did not show any changes in the number of "no shelter use" observations over the entire experiment.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Our results revealed distinct differences in behavioral and physiological responses in juvenile burbot and stone loach to decreasing shelter availability. In the single-specimen experiment, juvenile burbot of all sizes preferred the largest shelter tubes available, while stone loach showed no such shelter preference. Shelter selection in the presence of conspecifics, however, significantly changed in both species. In juvenile burbot, changes in shelter selection between the single and the group experiment can be explained by the preferences of all fish for the largest shelter tubes independent of the body size. In the solitary experiment, all fish had unrestricted access to any shelter tube in the mesocosm without any conspecific interference, and fish selected the largest shelter tube in 70.4% of all cases. In the group experiment, however, nine fish competed for three of the largest shelter tubes. Applying a theoretical value of 70.4% usage of the largest shelter tube for each specimen in a group of nine fish, 6.3 fish (9 x 0.7) should have used the largest shelter tube. In our experiment, however, only three largest shelter tubes were available at all. This means that only 3 out of 6.3 fish and therefore 47.6% of the fish in the group had the chance to select their primarily preferred shelter. This calculated percentage is very close to the observed shelter use of 43.0% in week 1 of the experiment and indicates a significant conspecific competition for the largest shelter tube in week 1 of the experiment. This competitive process was significantly related to the body size of burbot, with larger fish being more successful to defend their preferences compared to smaller conspecifics.
The ability of a certain fish to monopolize a resource within a group is often assumed to be a result of its social status (Magurran, 1986). Fish with a high social status are assumed to be able to behave in a way that protects their interests. For juvenile burbot, adequate daytime shelter is an important resource, and its availability in sufficient quantity and quality is important not only for the fish's behavior but also for its metabolism (Fischer, 2000a; Ryder and Pesendorfer, 1992). The fact that in our experiments the potential of a juvenile burbot to compete for its preferred shelter was not only significantly positively correlated to its body size but also significantly positively correlated to its somatic growth indicates a hierarchy among the group members. Such size-related hierarchies have been described in other fish species (Abbott and Dill, 1989; Alanärä and Brännäs, 1997; Fausch, 1984; Joblin and Wandsvik, 1982; Sloman et al., 2000).
However, to our knowledge, only one previous study has shown that an initially stable hierarchy may fail to persist when the resource limitation increases above a certain threshold. After removing the third shelter tube in our experiment in week 4, the hierarchical ranking disappeared and shelter use was no longer related to body size. Sloman et al. (2002) reported a very similar phenomenon in a trout competition experiment. When increasing water flow in a flume above a certain threshold, they also found strong indications for a breakdown of the previously persistent hierarchical order in a trout community and suggested a nonlinear and highly complex change in the group structure.
Our experiments also indicate such a resource limitation–induced reorganization of the group structure during week 4 of the experiment. Then, about 25% of the fish completely abandoned daytime sheltering, a behavior that is most unusual for juvenile burbot (McPhail, 1997) because it causes stress in the fish and significantly negatively affects somatic growth (Fischer, 2000a). Even more remarkable was that not the smallest but the previously dominant (largest) fish in the group showed this behavior.
This especially indicates that the largest fish in the group switched from a primarily linear response in competition for shelter (increasing defense behavior of the preferred shelter against smaller conspecifics) to a nonlinear bimodal behavior with the two alternative expressions "defending daytime shelter" or "abandon daytime shelter."
Bimodal responses to linear changes in resource availability are also described for other fish and invertebrate species (Bernardi and Giussani, 1975; Guiguer et al., 2002; Klemetsen et al., 2003). The alternative behavioral responses can be either facultative or obligate. Salmon change from a territorial-demersal lifestyle when sufficient food is available to a nonterritorial-pelagic one when food is scarce. This change has been shown to be nonlinear but bimodal, and fish switch from one behavior to the other at a certain threshold level of food availability (Brännäs et al., 2003; Harwood et al., 2002). In most of these processes, a threshold level for a certain resource is assumed to initiate the bimodal decision process, with fish having either sufficient or not-sufficient access to a resource at a certain point in their ontogeny.
In our experiments, daytime shelter was the limiting resource for which competition increased over time. Even though the largest fish in the group had the highest competitive potential for the largest shelter, defending these shelters seemed no longer worthwhile after a certain competition threshold level.
Juvenile burbot in Lake Constance show a very similar behavior during autumn, when the largest fish of a cohort leave littoral habitats and undergo their obligate habitat shift towards the profundal. During this time, the lake level continuously decreases and parts of the eulittoral zone become increasingly exposed. Fyke-net catches in the littoral and in the profundal zone showed that the largest members of the littoral burbot population then abandon shallow water habitats and migrate towards the profundal zone, while the intermediate and small cohort members stay in the littoral during winter (Fischer et al., 2004). A very similar migration behavior is also described for several other burbot lake populations (Kieckhäfer, 1972; Lehtonen, 1998), indicating a water level–triggered profundal migration in this species. That the largest cohort members leave littoral habitats first may be explained by a trade-off between increasing competitive effort for defending littoral shelter and decreasing predation risk in profundal habitats with increasing body size of the fish.
Fischer and Eckmann (1997) showed that in Lake Constance, the profundal migration of juvenile burbot happens at a size of about 14–15 cm TL and is irreversible. This size approximately matches the size of the fish in our mesocosm experiments that decided to abandon shelter. Assuming a bimodal irreversible decision process in juvenile burbot to leave littoral shelter at a certain size and at a certain level of competition for shelter, the observed behavior of the largest fish in our mesocosm experiments may reflect a similar trade-off, although the chance to complete the profundal behavior is lacking within a mesocosm.
In contrast to juvenile burbot, in stone loach size-related shelter-selection behavior was never seen in either the solitary or the group experiment. Furthermore, stone loach behavior did not change during the experiment, and no significant relationship between the ability of a fish to successfully compete for its preferred shelter tube and its somatic growth rate was found. In addition, during week 2 of the experiment, larger stone loaches seemed to be displaced by smaller fish, indicating a highly complex community structure that, however, does not seem to be based on a size-related dominance-subordinate structure as in juvenile burbot.
Fischer (2000b) showed that stone loach can shift to alternative substrata quite quickly when confronted with interspecific competition and are able to specifically select substrata that are less preferred by a competitor. Additionally, food availability is a much stronger trigger for habitat selection than substrate preference (Welton et al., 1983). This indicates that the stone loach is an environmentally eurytopic species for which the displacement to alternative shelter does not have an overall strong effect.
Energetically expensive aggressive behavior, however, as observed in juvenile burbot, only pays when the renunciation of the defended resource is even more expensive. For juvenile burbot, daytime shelter is an important resource during their short (maximum 1 year) littoral phase, and staying without shelter during daytime is not an option (Fischer, 2000a). Profundal migration, however, is at the expense of a higher risk of mortality especially for the smaller conspecifics. Therefore, littoral shelter defense behavior and profundal migration behavior are the two alternative behavioral responses, with a trade off between body size and littoral competition level.
Stone loach, in contrast, respond to increasing shelter competition in the littoral zone by a typically linear-scaled behavior. They gradually move to other habitats as competition increases. Even though these habitats may not provide optimal shelter quality, stone loach stay in littoral habitats during their entire life span (Brunken, 1989) and do not have an alternative habitat like juvenile burbot. A linear-scaled evasive behavior as a response to resource limitation may then be the best strategy to trade off the necessity of finding a shelter against the need to stay in the same habitat and therefore being confronted with a lifelong conspecific competition.
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ACKNOWLEDGEMENTS |
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We wish to thank M. Schmid, P. Mahler, and M. Wolf for helpful technical assistance during the experiments and R. Eckmann, I. Bussmann, M. Morris, and two unknown reviewers for helpful and welcome comments on the manuscript. This work was supported by the German Research Foundation within the Special Collaborative Project SFB 454 "Littoral of Lake Constance."
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