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Competing predators and prey: juvenile bottlenecks in whole-lake experiments.

INTRODUCTION

Predators of size-structured populations typically undergo a number of size-specific shifts in niches and trophic positions over their ontogeny (Werner and Gilliam 1984, Ebenmann and Persson 1988, Stein et al. 1988, Olson 1996). These shifts are consequences of increasing metabolic demands and an increase in mean size of consumed prey as predator body size increases, and may cause a predator to occupy the same trophic position as its prospective prey during some part of its ontogeny (Wilbur 1972, Werner and Gilliam 1984, Neill 1988, Persson 1988, Olson et al. 1995). Compared to their prey, which undergo less dramatic ontogenetic shifts in diet, predators are constrained over their ontogeny by more behavioral and morphological tradeoff costs in feeding efficiency on different prey types (Werner 1977, 1986, Werner and Gilliam 1984, Persson 1988, Eklov and Persson 1995). It has therefore been suggested that predators should be inferior to their prospective prey during competitive interactions (Werner 1977, Werner and Gilliam 1984, Persson 1988).

Larvae and juveniles in size-structured populations commonly experience high mortality in early life-history stages, and mortality is often inversely related to size or ontogeny (Paine 1976, Wilbur 1980, Werner and Gilliam 1984, Miller et al. 1988, Neill 1988). The major causes of mortality in young stages have been suggested to be predation (Calef 1973, Morin 1983, Werner and Gilliam 1984, Wilbur 1988, Fuiman 1994) and starvation (May 1974, Neill 1988, Frank and Leggett 1994, Welker et al. 1994). Food shortage can also make starving animals more susceptible to predation (Rice et al. 1987) or increase the time juveniles are exposed to gape-limited predators (Calef 1973, Wilbur et al. 1983, Tonn et al. 1986, 1992, Post and Evans 1989b). In temperate climates, where growth and energy storage are restricted to the growing season, winter mortality in juveniles can be high as small individuals are more vulnerable to starvation than larger conspecifics due to less amount of energy stored and higher metabolic costs per unit body mass (Shul'man 1960, Oliver et al. 1979, Post and Evans 1989a). Competing prey can thus have a negative effect on the growth during early life stages of their predator and therefore severely restrict the recruitment of the latter to predatory stages, a situation referred to as a "competitive juvenile bottleneck" (Werner and Hall 1979, Gilliam 1982, Neill 1988, Persson and Greenberg 1990a, Olson et al. 1995).

Perch (Perca fluviatilis) and roach (Rutilus rutilus) are commonly distributed over Eurasia and are the numerically dominant fish species in many lakes (Sumari 1971, Svardson 1976, Johansson and Persson 1986). Their interactions are characterized by a mixture of competitive and predatory processes (Persson 1988, Persson et al. 1991). Perch are ontogenetic omnivores and potentially undergo three ontogenetic niche shifts (Persson 1988). Larval perch are pelagic and feed predominantly on zooplankton (Guma'a 1978, Treasurer 1988, Wang and Eckmann 1994). They develop into juveniles at a size of [approximately]20 mm and shift to become more littoral in their habitat use and continue to feed mainly on zooplankton (Craig 1978, Guma'a 1978, Coles 1981, Persson 1987c, Treasurer 1988). Thereafter, perch shift to feed on macroinvertebrates to finally become piscivorous (Persson 1988). Piscivorous perch are gape-limited predators and consume roach and juvenile perch predominantly up to sizes of 60 mm (Willemsen 1977, Persson 1988, Treasurer 1989, Eklov and Diehl 1994, Christensen 1996). Roach undergo less dramatic shifts during their ontogeny with respect to prey size and feed on zooplankton at small stages and gradually shift to feed on a mixture of zooplankton, macroinvertebrates, algae, and plant material as adults (Hofer and Weiser 1987, Persson 1983, 1988). As a piscivore, perch are burdened with trade-off costs in feeding efficiency on different prey types, and juvenile perch are an inferior zooplankton feeder compared to roach (Persson 1987a, b). Correspondingly, roach have been shown to be able to depress zooplankton resources to much lower levels than perch (Persson 1987b). If zooplankton resources are low, juvenile perch shift early and at a small size to feed on macroinvertebrates, and exhibit a retarded growth (Persson 1986, Persson 1987c, Persson and Greenberg 1990a). Roach have thus the potential to impose a bottleneck in the recruitment of perch to piscivorous stages by decreasing zooplankton availability (Persson and Greenberg 1990a).

Most experimental studies on competitive and predatory interactions in size-structured populations have been carried out on a small spatial scale (enclosures or ponds) and on a short time scale (at most one growing season) (e.g., Werner et al. 1983a, b, Mittelbach 1984, 1988, Persson 1987a, b, c, Neill 1988, Persson and Greenberg 1990a, b, Olson et al. 1995) or as unreplicated whole-lake experiments (Persson 1986, Carpenter and Kitchell 1993, Persson et al. 1993, Mittelbach et al. 1995, but see Tonn et al. 1992). Small-scale studies are useful in identifying mechanisms that potentially are of major importance for interactions in natural communities. However an evaluation of their realized importance in natural systems calls for experimental tests at natural scales by which one includes potential indirect effects, access to all types of habitats, and natural food resource dynamics (Carpenter and Kitchell 1988, Tonn et al. 1992, Carpenter 1996).

As part of a replicated whole-lake experiment where roach were introduced in two out of four lakes inhabited by perch, we studied the growth and survival of young perch during their first 1.5 yr of life, i.e., to a size ([approximately]70 mm) when they are less likely to be cannibalized by adult perch (cf. Treasurer et al. 1992, L. Persson, unpublished data). based on previous studies (Persson 1986, 1987b, c, 1988, Persson and Greenberg 1990a), we first tested whether roach had a competitive effect on the growth and condition of young-of-the-year (YOY) perch by depressing the zooplankton resource to a level where YOY perch were forced to feed on less profitable benthic invertebrates. Second, we tested whether this predicted effect of roach on YOY perch growth included the larval phase (not previously studied) or was restricted only to the juvenile phase. Finally, we tested whether the predicted effect of roach on YOY perch growth resulted in a size-dependent mortality and if there was any time delay between growth response and mortality related to seasonal variation.

METHODS

Experimental lakes

The experiment was carried out during 1994 and 1995 in four small, adjacent, unproductive lakes - Lakes Abborrtjarn 1, 2, 3, and 4 - situated in central Sweden (64[degrees]29[minutes] N, 19[degrees]26[minutes] E). Detailed information on the lakes is given in Persson et al. (1996). All lakes have natural populations of perch, and two of the lakes (Lakes 1 and 2) are also inhabited by pike (Esox lucius). Intensive trapping of pike started in 1992 and only a few adult pike were left in the lakes in 1994 although [TABULAR DATA FOR TABLE 1 OMITTED] a strong cohort of 0+ pike was recruited in 1994 (L. Persson, unpublished data). The lakes were blocked by pike presence and then randomly assigned to control or roach treatment. Roach were stocked in Lakes 2 and 4 (roach-treatment lakes) on two occasions in 1993 (Table 1). The size structure and numbers of the introduced roach corresponded to natural densities found in similar lakes in the region where perch and roach coexist (Sumari 1971; M. Appelberg, unpublished data). Due to the presence of pike in Lakes 1 and 2, the densities of adult perch in the spring of 1993 and 1994 differed between lakes, but not between treatments (Table 1) (see also Persson et al. 1996). The adult perch populations in Lakes 2, 3, and 4 decreased from May 1994 to May 1995, but this decrease was more pronounced in Lakes Abborrtjarn 2 and 4 than in Lake 3 (Table 1). During the summer of 1994 all four lakes had similar temperature regimes and there was no difference in temperature between the roach-treatment lakes and the control lakes (repeated-measures ANOVA, lake [F.sub.1,2] = 0.458, P = 0.57) [ILLUSTRATION FOR FIGURE 1 OMITTED].

Fish

Larval perch were sampled once a week from hatching to an age of 4 wk with a bongo trawl (a cylinder-shaped trawl that narrows to the posterior end where a collecting device for captured fish is located) attached to a small boat. The trawl had a diameter of 60 cm and a length of 4 m and was held by a steel construction at the prow 0.6 m out on one side of the boat. The trawl could be adjusted to sample water strata from the surface to a depth of 2.0 m. Two flow meters, one inside and one outside the trawl, recorded sampling speed and ensured that the sampling speed did not create a water barrier in front of the trawl opening. For the first 2 wk we used a trawl with a mesh size of 0.5 mm (sampling speed at surface and at 0.5 m depth was 1 m/s and at 2.0 m depth was 0.8 m/s), and for the subsequent 3 wk we used a trawl with a mesh size of 1 mm (sampling speed at surface and at 0.5 m depth was 1.2 m/s and at 2.0 m depth was 0.9 m/s). We sampled three habitats: the littoral (trawl depth = surface), a middle zone that was [approximately]5 m outside the shore line (trawl depth = 0.5 m) and the pelagic (trawl depth = 0.5 m and 2.0 m). In Lakes 3 and 4, two hauls per habitat and depth were made at 1200 and 2400, respectively, and one haul per habitat was made at 0600 and 1800. In Lakes 1 and 2, one haul per habitat was made at 1400. The captured larvae were preserved in Lugol's solution. The volume in the pelagic habitat, from which the total number of larvae in this habitat was calculated, was defined as from the surface to 3 m down, as perch larvae during their pelagic phase rarely are caught below a depth of 3 m (Post and McQueen 1988, Wang and Eckman 1994).

After the first week of July, YOY (young-of-the-year) perch shifted habitat to the littoral zone (P. Bystrom, unpublished data) and were sampled by electrofishing along the shoreline during the rest of the 1994 season. In addition to electrofishing, traps and fyke nets were used in August and September samplings. To obtain a relative measure of YOY perch abundance, YOY perch were sampled in the last week of July (hereafter "August sampling") and in the last week of August and beginning of September (hereafter "September sampling") with fyke nets (mesh size 6 mm). In addition to fyke nets, we also used cylindrical plastic traps (mesh size 5 mm) in September. One fyke net was set at each of 10 littoral stations and two plastic traps were set at 10 littoral stations (depth of 0.5-1 m) and 5 deep stations (in or below the thermocline). In each of the four lakes the traps were set at 1300 and raised at 0900-1100 the following day. In the spring of 1995 (29 May-16 June) a large trapping effort (traps and electrofishing) was done in each lake to mark and recapture the 1-yr-old perch born in 1994 for population estimates. Perch were marked with blue dye injected with a Pan Jet Injector for small fish (Hart and Pitcher 1969). Traps and fyke-net catches of 1-yr-old perch were carried out with the same methods as in 1994 in the first week of July 1995 (hereafter "July 1995").

Perch do not grow in length below a temperature of 10 [degrees] C (Karas 1990). Analyses of size-selective winter mortality were performed on size distributions of the captures from 23 September 1994 and the May 1995 sampling, a time period when the water temperature in our experimental lakes never exceeds 10 [degrees] C with the increment-quantile method (Post and Evans 1989a). The method examines changes in the quantiles of a size distribution between sample occasions and allows for the detection of any size-selective mortality.

Perch larvae were measured in the laboratory to the nearest 0.1 mm (total length) under a stereo-microscope (based on 9-30 individuals for each lake and time). The sampled juvenile perch were measured in the field to the nearest 1 mm (total length). The juvenile perch were released back into the lakes after being measured, except for a subsample that was frozen in water and stored at -20 [degrees] C for later stomach and condition analyses. In the laboratory, fish were measured to the nearest 1 mm (total length) and weighed (wet mass) to the nearest 0.01 g. Condition was defined as (wet mass)/[(length).sup.3] (Fulton 1904). Material for stomach analyses of larvae was taken from the pelagic trawling and for juveniles from electrofishing samples or littoral fyke-net and trap samples. Stomach contents were identified to order, family, genus, or species and, if possible, 10 randomly chosen prey of each category were measured. The length of consumed prey was transformed to dry mass by using length-weight relationships (Dumont et al. 1975, Botrell et al. [1976] for zooplankton, and Persson and Greenberg [1990a] for macroinvertebrates). The consumed zooplankton were classified into two categories: benthic cladocerans (family Chydoridae), which are poor swimmers and found mainly on bottom sediment or in submerged vegetation (Whiteside et al. 1978, Townsend et al. 1986), and free-swimming zooplankton (Copepoda, Holopedium, Daphnidae, Bosmidae, Macrothricidae, Polyphemus and Sididae) (Rybak et al. 1964, Winfield Fairchild 1981, Townsend et al. 1986).

Perch [greater than or equal to]2 yr old were sampled on four occasions in 1994 (June, July, August, and September) with one fyke net and four plastic traps (mesh sizes 10 and 20 mm) per station as for the YOY perch trappings. Captured perch [greater than or equal to]2 yr old were measured to the nearest millimeter (total length), weighed to the nearest 0.1 g, and stomach-flushed for dietary analyses. The fish were thereafter released back into the lakes and the stomach contents were deep frozen for later laboratory analyses as for the YOY perch.

Zooplankton resource

Three pelagic and three littoral stations were sampled in each lake at five sampling dates (June-September) during the YOY-perch growing season. Zooplankton was sampled with a 100-[[micro]meter]-mesh net drawn at an approximate speed of 0.5 m/s. Pelagic zooplankton was sampled from the thermocline to the surface. Littoral zooplankton was sampled with a net drawn 6 m horizontally along the shoreline. Zooplankton samples were preserved in Lugol's solution. In the laboratory the animals were classified to species, genus, family, or suborder, counted, and the body lengths of 15 individuals (all, if fewer) of each category from each sample were measured. Lengths were transformed to biomass using regressions relating length to dry mass (Dumont et al. 1975, Botrell et al. 1976).

Enclosure experiment

An enclosure experiment on intra-cohort density dependence in growth of YOY perch was carried out in Lake Abborrtjarn 3 in 1996. The purpose was to analyze whether the lower growth of YOY perch in the roach-treatment lakes could be explained by the higher YOY perch densities in these lakes compared to the lakes lacking roach. The enclosures were made of a wood frame (2 x 2 m) with attached polystyrene floating devices. Inside the wood frame there was a circular iron ring with a diameter of 1.6 m. The ring held a plastic (polyethylene) transparent bag with a diameter of 1.6 m and a depth of 9 m. Shortly after the breakup of the ice, the enclosures were placed in the pelagic area and filled with unfiltered lake water. Experiments with larval perch and roach were performed in the enclosures between 5 June and 14 July, hence larval fish had been present in the enclosures prior to the experiment presented here. On 17 July, YOY perch from Lake Abborrtjarn 3 were sampled by electrofishing. To check for possible effects on survival from the handing for sampling, the perch were held in a storage bucket at least 2h before introduction into the enclosures. The perch (26.2 [+ or -] 1.9 mm [mean [+ or -] 1 SD], n = 12) were introduced to the enclosures in numbers of 2, 4, and 8 individuals per enclosure, which corresponds to densities of 1, 2, and 4 individuals/[m.sup.2]. All treatments were replicated four times. The experiment was ended on 28 August and the fish were sampled with a large dipnet. The first haul always caught [greater than or equal to]75% of the recovered fish and the hauling was ended when two subsequent hauls had resulted in zero captures. Sampled fish were treated in the same way as in the whole-lake experiment. One epilimnetic and one hypolimnetic zooplankton sample were taken from each enclosure on 14 June, 10 August, and 28 August with the same procedure as in the whole-lake experiment. In this paper we only present the final zooplankton densities from the epilimnion.

Statistical analyses

All analyses were performed for each lake or enclosure on the mean values of measured variables. In the whole-lake experiment, t tests and repeated-measures ANOVAs with roach presence as the treatment factor were used, and prior to statistical analyses data were ln(x + 1)-transformed to stabilize variance. Data expressed as proportions were arcsine square-root transformed. In the enclosure experiment, one-way ANOVAs were used and data were transformed as for the whole-lake experiment.

RESULTS

Growth and condition

No difference in growth of young-of-the-year (YOY) perch was present between control lakes and roach-treatment lakes during the larval period and the first part of the juvenile period [ILLUSTRATION FOR FIGURE 2 OMITTED]. In August, YOY perch in the roach-treatment lakes showed a decrease in growth that resulted in a smaller size at the end of the first growing season (t = 13.5, P = 0.0055) [ILLUSTRATION FOR FIGURE 2 OMITTED]. In the middle of September, the YOY perch were roughly twice as heavy in the control lakes as in the roach-treatment lakes (see Table 2). The condition of YOY perch decreased in all lakes during the latter part of the growing season, but the decrease was more substantial in the roach-treatment lakes (repeated-measures ANOVA: lake [F.sub.1,2] = 120.9, P = 0.008; time [F.sub.3,6] = 8.48, P = 0.014) [ILLUSTRATION FOR FIGURE 3 OMITTED].

Zooplankton densities and perch diets

Separate analyses (repeated-measure ANOVAs) of pelagic zooplankton biomasses during the larval and the juvenile periods of the YOY perch, respectively, showed that there was no difference between roach-treatment and control lakes during the larval period (lake [F.sub.1,2] = 0.023, P = 0.89; lake x time [F.sub.1,2] = 1.47, P = 0.35) [ILLUSTRATION FOR FIGURE 4A OMITTED]. During the juvenile period, the pelagic zooplankton resource decreased to a lower level in the roach-treatment lakes than in the control lakes (lake [F.sub.1,2] = 19.1, P = 0.05; lake x time [F.sub.2,4] = 0.15, P = 0.87) [ILLUSTRATION FOR FIGURE 4A OMITTED]. There was also a decrease in the total zooplankton biomass during the juvenile period in the littoral habitat, but no difference between treatments was present (lake [F.sub.1,2] = 1.16, P = 0.39; lake x time [F.sub.2,4] = 0.56, P = 0.61) [ILLUSTRATION FOR FIGURE 4B OMITTED].

At the beginning of June most of the larvae in Lakes Abborrtjarn 3 and 4 had not yet begun to feed exogenously and the yolk sac was still present in most larval stomachs. The larval perch started to feed mainly on rotifers and shifted to macrozooplankton with time [ILLUSTRATION FOR FIGURE 5A OMITTED]. Differences between lakes were observed in the timing of the shift in the diet from rotifers to macrozooplankton as well as taxonomic differences in the zooplankton diet, but no roach-treatment-specific patterns were present [ILLUSTRATION FOR FIGURE 5A OMITTED].

The proportion of zooplankton in the diet of juvenile perch was higher in the control lakes than in the roach-treatment lakes in August and September (lake [F.sub.1,2] = 17.3, P = 0.053; lake x time [F.sub.3,6] = 5.58, P = 0.036) [ILLUSTRATION FOR FIGURE 5B OMITTED]. This coincided in time with the period of growth retardation in the roach-treatment lakes [ILLUSTRATION FOR FIGURE 2 OMITTED]. The proportion of benthic cladocerans in the diet of YOY perch was higher in the roach-treatment lakes compared to the control lakes (lake [F.sub.1,2] = 75.5, P = 0.01; lake x time [F.sub.3,6] = 0.62, P = 0.63) [ILLUSTRATION FOR FIGURE 5C OMITTED], whereas no difference was found for the proportion of chironomids in the diet of YOY perch (lake [F.sub.1,2] = 2.27, P = 0.27, lake x time [F.sub.3,6] = 2.42, P = 0.16) [ILLUSTRATION FOR FIGURE 5D OMITTED].

Mortality patterns of larval and juvenile perch

No significant mortality of YOY perch was present during the larval period in either the roach-treatment lakes or in the control lakes (repeated-measures ANOVA: lake [F.sub.1,2] = 2.18, P = 0.28; lake x time [F.sub.4,8] = 1.91, P = 0.20; time [F.sub.4,8] = 1.91, P = 0.20) [ILLUSTRATION FOR FIGURE 6 OMITTED]. During the rest of the growing season, trap catches in August and September indicated the presence of a higher mortality of YOY in the control lakes compared to the roach-treatment lakes [ILLUSTRATION FOR FIGURES 7A-C OMITTED]. The catch per unit effort (CPUE) in September, however, did not differ between treatments (t = 1.342, P = 0.312), which was mainly due to the large variation between the two control lakes (trap catches in August and September probably underestimated YOY abundance in Lake Abborrtjarn 1; compare with population estimates in May 1995 and CPUE in July 1995, [ILLUSTRATION FOR FIGURES 7B-E OMITTED]). The mortality patterns of YOY perch also corresponded with the observed patterns of cannibalism, which showed that the occurrence of YOY perch in the stomachs of perch [greater than or equal to]2 yr old was low at the end of the larval period when large perch were feeding mainly on macroinvertebrates and zooplankton (L. Persson, unpublished data), and increased during the rest of the summer [ILLUSTRATION FOR FIGURE 8 OMITTED]. Most of the perch [greater than or equal to]2 yr old in Lakes 2 and 4 died during the period July to August 1994 (L. Persson, unpublished data). Although a substantial mortality of perch [greater than or equal to]2 yr old also occurred in Lake 3 in 1994, perch [greater than or equal to]2 yr old were still more abundant in Lake 3 than in Lakes Abborrtjarn 2 and 4 in May 1995 (Table 1). As a result, mortality of YOY perch due to cannibalism was probably higher in the lakes lacking roach than in the roach-treatment lakes as the larger perch continued to feed on YOY perch through out the season [ILLUSTRATION FOR FIGURE 8 OMITTED].

In the middle of September 1994, more than 1000 dead YOY perch were observed along the shore of Lake 4. These individuals were smaller (mean 35.5 mm, n = 34 fish) and had a lower condition index (mean 0.68, n = 34) than those alive in the lake at the same time (length, t = 4.36, df = 72, P [less than] 0.0001; condition, t = 5.09, df = 72, P [less than] 0.0001). In Lake Abborrtjarn 2 only a few dead individuals were observed and in Lakes Abborrtjarn 1 and 3 no dead individuals were observed during the same period. During the winter, YOY perch suffered from a very high mortality in Lake 2 and only a total of 22 individuals were caught in this lake during the intensive catching period in the spring of 1995 [ILLUSTRATION FOR FIGURES 7C AND D OMITTED]. The relative differences between CPUEs in August and September 1994 and the population estimates in May 1995 also pointed to a higher winter mortality among YOY perch in Lake Abborrtjarn 4 compared to Lakes 1 and 3 [ILLUSTRATION FOR FIGURES 7B-D OMITTED]. Size-selective winter mortality on smaller individuals was present in all lakes, which was indicated by the increase in size in the lower quantiles but not in the higher quantiles of the size distributions from autumn 1994 to spring 1995 [ILLUSTRATION FOR FIGURE 9 OMITTED]. There was also a tendency for a more pronounced size-selective winter mortality on smaller individuals in Lake 4 compared to the control lakes although the slope from the increment-quantile regression for Lake 4 did not differ from the slopes from the increment-quantile regressions for Lakes 1 and 3 (t = 0.39-1.52, df = 8-10, P = 0.1-0.6) [ILLUSTRATION FOR FIGURE 9 OMITTED].

In June 1995 most of the 1-yr-old perch in Lake 4 died and the trap catches in July only amounted to a total of 5 individuals [ILLUSTRATION FOR FIGURE 7E OMITTED]. Apparently the 1-yr-old perch never recovered from the energy losses during the winter, and individuals in poor condition were frequently observed at the surface of the lake and were also caught in the trawl during larval samplings in 1995. As a result, a negative effect of roach on the survival of the perch born in 1994 was present (repeated-measure ANOVA on the CPUE estimates: lake [F.sub.1,2] = 1.08, P = 0.41; lake x time [F.sub.2,4] = 6.90, P = 0.05) and in August trappings 1995 no 1-yr-old perch at all were caught in Lake 4 (L. Persson, unpublished data). It is likely that the presence of pike in two of the lakes affected the mortality patterns of perch as YOY perch were commonly observed in the stomachs of 0+ pike. However, as pike were present in both one roach-treatment lake and one control lake the overall effects of the roach introduction on the survival of young perch cannot be explained by pike presence.

Enclosure experiment

The mortality of YOY perch in the enclosures was independent of perch density (ANOVA: [F.sub.2,9] = 0.74, P = 0.98), whereas the growth was affected by perch density ([F.sub.2,8] = 14.3, P = 0.02) (Table 2). The densities of YOY perch (at the end of the larval period) in all four lakes in 1994 were comparable to the low-density treatments in the enclosure experiment (Table 2). The growth of YOY perch in the control lakes in 1994 was also comparable with the growth of perch in the low-density enclosures. In contrast, the growth of YOY perch in the roach-treatment lakes in 1994 was much lower than the growth of YOY perch in the enclosures with similar densities of perch and only comparable to the growth in enclosures with the highest densities of perch (Table 2). The zooplankton biomasses in the enclosures at the end of the experiment were also comparable to the zooplankton biomasses in the control lakes in 1994 and were [greater than]5 times higher than the zooplankton biomasses in the roach-treatment lakes in 1994 (Table 2). Both growth and zooplankton data thus suggest that the lower growth rates of YOY perch in Lakes 2 and 4 in 1994 cannot be explained only by the tendency for a higher density of YOY perch in these lakes.

DISCUSSION

Juvenile growth and temporal variation in competition intensity

Juvenile perch and roach compete for zooplankton (Persson 1987c, 1988, Persson and Greenberg 1990a) and we predicted that the introduction of roach in Lakes 2 and 4 should have a negative effect on the growth and subsequent survival of young-of-the-year (YOY) perch. Correspondingly, the growth of YOY perch was reduced in the roach-treatment lakes, which resulted in a nearly twofold difference in mass of YOY perch between lakes with roach and control lakes at the end of the first growing season. The difference in growth of YOY perch between treatments was, however, not a result of slower growth over the whole growing season in the roach-treatment lakes, but a result of a decrease in growth limited to August in these lakes. During the larval stage, the period when YOY perch are most sensitive to starvation (Miller et al. 1988, Letcher et al. 1996), there was no effect of roach on the growth of larval perch. Furthermore, mortality of perch larvae was low in all lakes, suggesting that mortality due to starvation during the larval stage was unimportant. The larval period also coincided with a period when there were relatively high pelagic zooplankton resource levels in the lakes.

The decrease in growth of YOY perch in the roach-treatment lakes coincided with (1) a shift in the diet from free-swimming zooplankton to chironomids and benthic cladocerans (cf. Persson 1987c, Persson and Greenberg 1990a, Wu and Culver 1992) and (2) a more pronounced decrease in zooplankton resource levels in these lakes compared to the control lakes. Previous studies in more productive lakes on the competitive interaction between YOY perch and roach have only dealt with the latter part of the growing season (Persson 1986, Persson 1987b, c, Persson and Greenberg 1990a). Those studies show that, in the absence of or in low densities of roach, YOY perch grow fast and feed mainly on zooplankton throughout the season, whereas a shift in diet to less profitable prey and retarded growth is observed at higher densities of roach. The results from our whole-lake experiment agree with these results but also suggest that competition between YOY perch and roach is weak or absent during the larval phase.

An increase in resource limitation and competition intensity over time has also been documented in another well-studied system, the competitive interaction between the bluegill sunfish (Lepomus macrochirus) and juveniles of its predator largemouth bass (Micropterus salmoides) (Olson et al. 1995, Olson 1996). In that system the increase in resource limitation over time for juvenile bass arises when competition from small bluegills decrease early YOY bass growth to the extent that bass may not reach the size necessary to shift to feed on YOY bluegill during their first summer. Another plausible mechanism for a within-season variation in competition intensity is the low total metabolic demands of the fish due to the lower temperature and small size of the larvae at the beginning of the growing season and the concomitant increase in total metabolic rates of the fish community over time as a result of both a temperature increase and an increase in size of YOY fish (Persson 1987b, Persson and Johansson 1992, Teucher and Luecke 1996). In temporally variable environments, temporal variation in resource limitation and competition intensity has been commonly [TABULAR DATA FOR TABLE 2 OMITTED] documented (Zaret and Rand 1971, Prejs and Prejs 1987, Grant 1986, Werner 1986, Schmitt and Holbrook 1986, Persson and Johansson 1992, Polis et al. 1996). If the yearly recruitment is a major factor causing the resource limitation, the extent by which it will increase over the growing season will depend on how important other factors like predation are in regulating recruiting-cohort survival. With a high predation rate, resource limitation in YOY cohorts may actually decrease over time due to thinning (Wilbur 1988), although predator behavioral-induced habitat restrictions may increase resource limitation in refuge habitats (Werner et al. 1983b, Mittelbach 1988, Tonn et al. 1992, Persson 1993, Persson and Eklov 1995). Still, in our experiment the decrease in zooplankton resource levels in both the pelagic and littoral habitats over time suggests that an increase in resource limitation occurred for juvenile perch compared to larval perch irrespective of predatory impacts.

Size-selective mortality and competitive juvenile bottlenecks

The suppressed growth of YOY perch in the roach-treatment lakes resulted not only in a smaller size, but also in a lower condition of YOY perch in these lakes compared to the control lakes. YOY perch in the roach lakes thus had a lesser amount of energy storage in relation to body mass in autumn compared to the control lakes (cf. Wicker and Johansson 1987). This resulted in a very high mortality during winter in Lake 2 and a more prolonged period of starvation mortality in Lake 4 that started in autumn 1994 and continued until the beginning of the summer 1995. In temporally variable environments it is necessary to gain enough energy reserves to survive harsh time periods (Shul'man 1960, Gregory 1982, Lima 1986, Piper and Wiley 1990). Starvation may be the direct cause of death as well as indirectly causing death due to increased susceptibility to predation and/or diseases (e.g., Rice et al. 1987). Starvation during the winter season has been suggested to be a major cause of mortality in YOY fish as smaller individuals are more susceptible to starvation due to their low ratio of energy storage to metabolic rates (Shul'man 1960, Oliver et al. 1979, Post and Evans 1989a). Our whole-lake experiment demonstrates the existence of this mortality mechanism and also points to the importance of considering the temporal windows for energy gains and costs in temperate waters, where periods for growth and energy gain (summer) alternate with periods of energy loss (winter).

Competition during early life stages in size-structured populations has been suggested to have a major impact on the recruitment of individuals to adult stages (Wilbur 1972, 1988, Neill 1975, 1988, Svardson 1976, Morin 1983, Werner and Gilliam 1984, Tonn et al. 1986, Werner 1986, Mittelbach 1988, Persson 1988, Persson and Greenberg 1990a, Olson et al. 1995). Retarded growth during early life stages has often been set into the context of competitive juvenile bottlenecks (Neill 1975, 1988, Gilliam 1982, Persson 1986, Persson and Greenberg 1990a, Olson et al. 1995). In fish populations, the bottleneck situation has been suggested to arise during the zooplankton feeding stage, which most species pass through during their ontogeny (Svardson 1976, Werner 1977, Werner and Gilliam 1984, Werner 1986, Persson and Greenberg 1990a). Previous studies of the perch-roach interaction have shown that the competitive effect of the efficient-zooplankton-feeder roach, leads to a shift of juvenile perch early and at a small size to macroinvertebrate feeding and this potentially forms the bottleneck for recruitment to piscivorous stages as a result of an increased intraspecific competition (Persson 1986, Persson and Greenberg 1990a). Two mechanisms have been postulated to increase the mortality following the retarded growth of perch during the bottleneck phase - the increased risk of starvation and the increased time that individuals are susceptible to gape-limited predators (Persson and Greenberg 1990a). Our study is the first to demonstrate the presence of one of the mechanisms, i.e., starvation mortality. The circumstance that the second mechanism, gape-limited predation, was unimportant in our study can obviously be related to the mortality of adult perch in the roach-treatment lakes. However, it can also be hypothesized that the relative importance of starvation compared to predation as the main mechanism behind the mortality of juvenile fish in competitive juvenile-bottleneck situations depends on latitude. In boreal systems, the growing season is relatively short. Thus fish not only face a longer winter (up to seven month of ice cover in the system studied) but also a shorter growing season to increase in body size and gain energy reserves to survive the winter. In contrast, juvenile fish at more southern latitudes are exposed to a much shorter period of ice cover, but may during the longer growing season be exposed to a longer period of predation.

Intra-cohort competition and size-selective predation as alternative mechanisms

Two alternative mechanisms may have caused the observed differences in size of YOY perch between roach-treatment lakes and control lakes - intra-cohort competition and size-selective predation on smaller individuals. The die-off of adult perch in the roach-treatment lakes decreased cannibalism on YOY perch in these lakes and caused a tendency for higher YOY perch densities in the roach-treatment lakes compared to the control lakes. It can therefore be argued that the growth retardation in the roach-treatment lakes was caused by intra-cohort competition among YOY perch in the roach-treatment lakes and that the higher growth rate in the control lakes was an effect of predator thinning (Vanni 1986, Wilbur 1988, Persson et al. 1996). Correspondingly, high abundances of YOY perch have been shown to depress zooplankton resources to a level that results in retarded growth (Willemsen 1977, Mills and Forney 1981, 1983). Still, the results from our enclosure experiment suggest that the densities of TOY perch in the roach-treatment lakes were too low to have caused the difference in growth between roach-treatment lakes and control lakes.

Size-selective predation on smaller individual YOY perch by adult perch in August in the control lakes may also have caused the apparent growth difference between control and roach-treatment lakes (Post and Prankevicius 1987). However, no captured YOY perch in the roach-treatment lakes was even close to being as large as the mean size of the perch in the control lakes [ILLUSTRATION FOR FIGURE 9 OMITTED]. This together with the higher condition of YOY perch in the control lakes compared to roach-treatment lakes suggest that the observed differences in the size of TOY perch between control lakes and roach-treatment lakes cannot be explained by size-selective predation on smaller individuals in the control lakes.

Thus, even if both intra-cohort competition and size-selective predation on smaller individuals may have increased the observed difference in size between roach-treatment lakes and control lakes, our results strongly suggest that roach had a direct competitive effect on YOY perch.

Identifying mechanisms - the necessity of whole-lake experiments

Whole-lake experiments may be regarded as the ultimate experimental test of the impacts of mechanisms identified at smaller spatial and shorter temporal scales on population and community dynamics (Carpenter and Kitchell 1988). Although access to experimental lakes as well as costs often limit the degree to which the experiment can be replicated (Carpenter 1989), the advantages of whole-lake experiments are that all natural direct and indirect effects influencing the outcome of the experiment are included (although they cannot necessarily be dissected) (Carpenter and Kitchell 1988, Tonn et al. 1992, Carpenter 1996). Besides yielding results that are directly relevant at the natural population and community scales of the fish community, our whole-lake experiment revealed at least one insight that could not have been obtained at a shorter time scale and at a smaller spatial scale. Due to the scale of the experiment we were able to show a temporal separation between the effect of roach on TOY perch growth and the resulting mortality following from this growth impact. Unless the winter season had been included, we would not have been able to identify the mortality agent present. Finally, our study points to the fact that although replication will always be a practical obstacle in whole-lake experiments, replication may be possible, which will allow us to more conclusively relate observed differences between control and treatment to actual effects of treatment.

ACKNOWLEDGMENTS

We thank Jens Karlsson, Kristina Samuelsson, and Erika Westman for help in the field. We also thank Aman's Fish Co-operative for the exclusive right to use the lakes for experimental studies. Valuable comments on previous drafts of this paper were given by Peter Eklov. The study was supported by grants from the Swedish Natural Research Council to Lennart Persson, the Swedish Council for Forestry and Agricultural Science to Lennart Persson and Par Bystrom, and the Royal Swedish Academy of Science to Par Bystrom.

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