Changes in the fish community and water quality during
seven years of stocking piscivorous fish in a shallow lakeC . S K O V , * M . R . P E R R O W , † S . B E R G * and H . S K O V G A A R D ‡
*Danish Institute for Fisheries Research, Department of Inland Fisheries, Silkeborg, Denmark †ECON Ecological Consultancy, University of East Anglia, Norwich, U.K.
‡County of A˚rhus, Environmental Division, A˚rhus, Denmark
SU M M A R Y
1. Piscivores (annual stocking of 1000 individuals ha)1of 0+ pike and a single stocking of 30 kg ha)1of large 20–30 cm perch) were stocked in seven consecutive years in a shallow eutrophic lake in Denmark. The stocking programme aimed at changing food-web structure by reducing zooplanktivorous and benthivorous fish, with resultant effects on lower trophic levels and ultimately water quality.
2. The fish community and water quality parameters (Secchi depth, concentrations of total phosphorus, chlorophyllaand suspended solids) were monitored between 1996 and 2000 and relationships were evaluated between predatory fish and potential prey and between zooplanktivorous or benthivorous fish and water quality parameters. In addition, potential consumption of piscivorous fishes was calculated.
3. The density of fish feeding on larger zooplankton or benthos (roach >15 cm, crucian carp >15 cm) declined distinctly during the study period. This effect was attributed to
predation by large (>50 cm) pike. Based on scale readings, we cautiously suggest that the stocking of 0+ pike boosted the adult pike population to produce an unexpected impact in later years. Conversely, no direct impact of stocked 0+ pike was detected on 0+ roach. 4. A major decline in the recruitment strength of 0+ roach was observed in 2000. A combination of (i) the indirect effect of large pike preying on adult roach, with negative effect on roach reproduction and (ii) the direct predation effect of 0+ pike and⁄or 1+ and 2+ perch recruited in the lake, provides the most likely explanation of this phenomenon. 5. A marked increase in Secchi depth in 2000 and declining trends in suspended solids, chlorophyll-aand total phosphorus concentrations were observed. These changes may also be attributable to changes in the fish community, although the relationships were not straightforward.
6. This 7-year study indicates that piscivorous fish may be a significant structuring force in shallow eutrophic lakes, suggesting that stocking piscivores can increase predation pressure on cyprinids. However, the general lack of impact of 0+ pike points to the need of refining current stocking practices in several countries across Europe.
Keywords: benthivorous fish,Esox lucius,Perca fluviatilis, planktivorous fish, predation, water quality
The presence of a dense population of piscivorous fish can have a profound impact on lake ecosystems (e.g. Benndorf, 1990; Turner & Mittelbach, 1990; Carpenter & Kitchell, 1993). This impact can be direct or indirect (He & Kitchell, 1990). Direct predation on fish,
Correspondence: Christian Skov, Danish Institute for Fisheries Research, Vejlsøvej 39, 8600 Silkeborg, Denmark.
especially on smaller individuals, changes the size-class structure of the fish community in favour of large individuals and reduces population densities (Bro¨nmark et al., 1995). Indirect impacts may occur because predators can force the prey fish to change habitat (Turner & Mittelbach, 1990; Jacobsen & Perrow, 1998) and, potentially, to forage suboptimally. Direct predation on zooplanktivorous fish and, in theory, changes in habitat use induced by increased predation risk can initiate a trophic cascade, increas-ing the impact of grazincreas-ing zooplankton on planktonic algae. In shallow lakes, a resulting increase in light penetration may allow submerged plants to invade and stabilise the lake in a clear-water state (Scheffer et al., 1993). Predators may also impact upon benthi-vorous fish leading to a decrease in suspended material in the water column, thereby increasing Secchi depth (Breukelaar et al., 1994). Moreover, a decrease in foraging activities by benthivores may reduce nutrient release from sediments (Tatrai & Istvanovics, 1986). Given these impacts, stocking eutrophic lakes with piscivorous fish like pike (Esox lucius L), pikeperch [Sander lucioperca (L)] or perch (Perca fluviatilisL) has drawn much attention in recent years (Benndorf, 1990; Prejset al., 1994; Berg, Jeppesen & Søndergaard, 1997) and is commonly referred to as biomanipulation.
It has been argued that for biomanipulation to be successful, piscivores occupying different niches should be present in a lake to optimise predation pressure on prey fish (Benndorf, 1990; Perrow et al., 1997). Stocking with a range of different predators therefore seems to be the optimal strategy.
Around 800 000 0+ pike (2–4 cm) are stocked in Danish lakes annually in an attempt to increase predation pressure on newly hatched zooplanktivor-ous fish such as roach [Rutilus rutilus (L)] which typically represent the greatest threat to zooplankton (Townsend & Perrow, 1989; Prejset al., 1994; Mehner & Thiel, 1999). There are, however, few examples of a decrease in the smallest zooplanktivorous fish follow-ing pike stockfollow-ing (e.g. Prejs et al., 1994; Berg et al., 1997), and even less for a cascading impact upon lower trophic levels (e.g. Søndergaard, Jeppesen & Berg, 1997). The aim of this study was to evaluate whether and how 7 years of stocking piscivorous fish, initially pike and subsequently pike and perch, changed the fish community and water quality in a shallow eutrophic lake.
Methods Study site
Lake Udbyover in Jutland, Denmark (1010¢N, 5640¢E) is small (20.6 ha), shallow (maximum depth 2.60 m, mean depth 1.05 m) and eutrophic. The lake has a natural origin, but changed character in the middle of the last century as the eastern part of the lake was used for peat cutting. In the mid-1960s, a nearby town used the lake as a recipient for sewage effluent, with resultant severe eutrophication. In the early 1970s, sewage was redirected to a treatment plant and today the water supply to the lake consists of precipitation and percolation from the 1.4 km2 catchment area consisting of agricultural fields with scattered houses. The lake has a small outlet, which is usually dry most of the year, and the estimated water retention time is more than 1 year. The lake is subject to limited recreational use: duck hunting in autumn and, until 1998, some rod fishing. By the end of 1998, a local initiative restricted rod fishing and it has since been minimal.
The natural fish community in the lake comprised roach, large individuals of crucian carp [Carassius carassius(L)], pike and eel [Anguilla anguilla(L)] (Skov, 1997). No eels have been observed in the lake since 1998. In 2000, two specimens of bleak [Alburnus alburnus (L)] of unknown origin were caught in gillnets. The marginal vegetation, covering around 10% of the lake (Skov, 1997), was dominated by common reed [Phragmites australis (Cav.) Trin. ex Steud.] and bogbean (Menyanthes trifoliata L), with sweet flag (Acorus calamusL), reedmace (Typha latifolia L and Typha angustifolia L), amphibious bistort (Polygonum amphibiumL),yellow flag iris (Iris pseuda-corus L), and sedges (Carex spp.) as subdominant species.
Each spring since 1994, the lake has been stocked with 0+ pike. The pike were hatched and raised in a nearby hatchery. At an age of about 1 month and a size of 20–40 mm, they were transported to the lake and released in the littoral zone. The stocking density of 1000 ind. ha)1 was constant during all years. From 1996 to 1999, pike were stocked in the first week of June, but in 2000, stocking was 1 month earlier in order to determine the survival of stocked 0+ pike in relation
to stocking time (Skov, 2002). However, the size of the stocked fish was not different from previous years. Perch (13–36.5 cm total length, mean¼22.8 cm, SE¼0.61), caught over a 2-week period in a nearby lake, were introduced in a single event to the lake on 12th May 1998 (30 kg ha)1). The total weight of the perch was estimated in the fish-transporter, and, before stocking, a random sample of the fish was measured and weighed. At least some of these fish spawned as 0+ perch were recruited successfully within a month after stocking.
The species composition and abundance of the fish stock was determined each August during 1996–2000 by a combination of gillnet sampling, hoop-net sampling and quantitative standardised electrofishing (PASE). For crucian carp, roach older than 1 years and perch, the abundance was determined as catch per unit effort (CPUE) using multiple mesh gillnets (14 mesh sizes ranging from 6.25 to 75 mm, 42 m long, 1.5 m high). Following a Danish test fishing pro-gramme, the lake was divided into five equally sized zones in each of which four nets were set (two near the margin and two in open water). The 20 gill nets were set in the same locations every year. Catch per unit effort in any 1 year was based on the mean CPUE of the four nets in each of the five zones. Fish were caught over four nights in 1996 and 1997 and over three nights in 1998–2000, because fewer fish were found in the nets. The fish were measured to the nearest lowest 5 mm, and five fish from each of these length groups were weighed to the nearest g (fish >100 mm) or nearest 0.1 g (fish <100 mm).
Gillnet sampling is inappropriate for 0+ roach, 0+ pike and larger pike on account of the small size of 0+ roach and the behaviour of pike. The bulk of the smallest pike is restricted to the littoral zone (Chapman & Mackay, 1984; Bry, 1996), and large pike tend to tear the nets and escape. Consequently, standardised quantitative point sampling by electro-fishing (PASE) (Copp & Pen˜a´z, 1988; Perrow, Jowitt & Gonza´lez, 1996) was undertaken in the littoral zone of the lake. In 1996, a total of 100 fixed points were sampled during the season; in the following years, the intensity was reduced slightly to 94 fixed points. Sampling was conducted at regular intervals between June and August to give 9–10 samples each year. Data
from four samplings (late July till late August) were used for the density estimates, while data from all samples were used in calculations of 0+ pike con-sumption.
During sampling, each PASE point was approached discretely, and the anode rapidly immersed in the water. It was activated for 15 s during which time all stunned fish were collected using a dip net. A detailed description of the PASE procedure, evaluation of the method and gear used is given in Skov & Berg (1999). Assuming 0.12 mV to be the threshold voltage gradi-ent, at which fish can be effectively stunned (Copp & Pen˜a´z, 1988), the effective electric field of the gear used (anode of 31 cm diameter), was measured to be 0.69 m2 with a voltmeter. Mean water depth for all sampling points were measured on each sampling occasion, and the number of fish m)3 was calculated under the assumption that the whole water column was sampled. All fish sampled were identified to species and, except for 0+ roach, their total length measured to the nearest mm. For 0+ roach, the number at each PASE point was counted and their length determined from a random sample taken from all points.
In order to obtain an estimate of 0+ roach density in open water, the standard hoop net (2 m long, 0.4 m diameter) employed by the Danish survey programme for 0+ fish monitoring (Mooij, 1992) was used. Samp-ling was undertaken from a small boat fitted with an outboard motor controlled by one person. The second person held the net in front of the boat. The first half of the net has a cylindrical shape (mesh size 2 mm) whereas the second half has a conical shape (mesh size 1 mm). A jar at the end of the net collects the captured fish. In 1996, samples were taken within 3 days of PASE along a total of nine transects. Between 1997 and 2000, sampling took place in the afternoon of the same days of PASE and consisted of eight trawls along randomly selected fixed transects marked with large canes. In all years, the speed of the boat was 2 m s)1, and the centre of the hoop net was fixed at 0.5 m below surface. By calibrating a flow meter within the net and the distance travelled, the total volume of water sampled was determined. Around 140 m3water was sampled on each occasion.
Fish density estimation
The density of each size class of pike was calculated by dividing the number of fish sampled by the area of
the electric field. Total pike density on each PASE occasion was determined as mean catch (ind. m)2) multiplied with the littoral surface area and divided by the total lake area. The littoral lake area, including the vegetation⁄open water interface, was estimated at 13% of the total lake area from aerial photographs. In order to estimate 0+ roach density, a combination of littoral zone and open water estimates was used. The absolute number of 0+ roach in the littoral zone per sampling day was estimated by multiplying the mean density of 0+ roach (ind. m)3) with the littoral water volume (area·mean depth at sampling spots·0.66 to account for decreasing water depths towards the bank). The absolute density of 0+ roach in the open water was estimated by multiplying open water volume by mean density (ind. m)3) of 0+ roach from hoop-net samples. Open water volume was calcula-ted as total water volume minus littoral water volume. The total water volume was calculated to be about 250 000 m3in 1996 (Skov, 1997). It remained constant until 1999 but increased to 270 000 m3 in subsequent years. An overall estimate of 0+ roach density (ind. m)3) in the lake was finally achieved by adding the absolute number of fish in the open water and the littoral zone and dividing by total water volume. In July and August, 0+ perch were too large and hence too mobile to be effectively sampled by the hoop net; therefore, gill net data were used to estimate 0+ perch density.
Estimates of potential consumption by 0+ pike, the stocked perch and pike >50 cm were calculated to aid interpretation of the observed patterns in fish density. The potential consumption of 0+ pike in any 1 year was based on the increase in 0+ pike biomass between the date of stocking and the earliest date of 0+ roach density estimation (21st July). The initial and final total biomass of 0+ pike was determined by multiplying the average weight (g) of an average sized individual from the first sampling after stocking and from the last sampling before 21st July by the absolute 0+ pike density estimated. Weight (g) was estimated by a length– weight relationship based on 389 0+ pike caught in eight different lakes during the summers of 1999 and 2000 (Skov, unpubl. data). The absolute 0+ pike
density was calculated in the same manner as for 0+ roach above, but was founded on the mean density from all PASE samplings (May–August). Only the density estimate from the littoral was used as no 0+ pike were caught in the open water. In order to simplify the consumption calculations, the absolute 0+ pike density was assumed to be constant over the considered period.
Assuming an exponential relationship, the daily increase in biomass (%BW d)1) of 0+ pike was calculated for each year using the difference between initial and final biomass and days of growth (t) between these two samples:
%BW¼ eðlnðfinal biomassÞlnðinitial biomassÞÞt
In order to assess the maximum consumption of 0+ roach by 0+ pike in each year, the daily ration was assumed to be three times the daily increase in body weight (%BW d)1), as shown for pike of 20 g at maximum growth (Diana, 1996). Daily ration was converted into a number of 0+ roach eaten per day, adjusted according to the daily increase in roach weight. A daily average weight per individual was calculated from length–weight relationships obtained by gillnet fishing and measured 0+ roach lengths and assuming a linear growth of 0+ roach between June and August. The daily number of 0+ roach potentially eaten was then determined by dividing the daily ration of 0+ pike by the weight of roach per individual on that day. To obtain maximum consumption values, it was assumed that roach constituted the entire diet. An estimate of the maximum number of roach consumed over the consumption period was then obtained by summing up the daily totals. The possible consumption by the 600 kg of stocked perch from the time of stocking until the gill net survey in August 1998 (95 days) was calculated assuming a daily ration of 1–4% of body weight (Popova & Sytina, 1977). The possible consumption of 5–10 cm (mean weight 4.7 g) roach by perch was estimated by assuming that the diet of perch was entirely roach. The potential consumption of fish by pike >50 cm from March 1998 until the gillnet survey (170 days) was calculated using the PASE density estimate from 1998, mean individual biomass from a length–weight relationship from the gillnet survey in 1998 and a daily ration of 2%
BW d)1 (Diana, 1996).
Mortality of stocked pike
Mortality of the 0+ pike from the time of stocking until August was estimated as the number of stocked fish minus the absolute number of 0+ pike in the lake derived from the mean density from all PASE sam-plings in August. The estimate illustrates minimum mortality because it assumes that all 0+ pike caught in the lake originate from the stockings.
Fecundity potential of roach
The potential population fecundity (total number of eggs) of roach in the five study years was estimated. In the absence of an estimate at the time of spawning, the density of roach caught in the gill nets the previous year was used as a proxy of the density of the spawning population. In accordance with the findings of Papageorgiou (1979) and others, it was assumed that female roach aged 2+ and older contributed to population fecundity. Based on the length–weight relationship for the year of interest, the individual weight of each mature fish caught was determined and the number of eggs estimated from weight–egg num-ber regressions for roach from a shallow lake in Greece (Papageorgiou, 1979) with a similar age structure and weight as the population in Lake Udbyover. Annual potential fecundity was calculated by summing the eggs produced by all fish caught, correcting for an increasing number of females with increasing age, i.e. the male to female ratio was assumed to be 1 : 1 until the age of 6+ and 1 : 1.65 for older fish (Mann, 1973). Scale readings from 1996 (Skov, 1997) indicated that fish above 15 cm total length were 6+ or older.
Between 1996 and 2000, Secchi depth and concentra-tions of total phosphorus, chlorophylla and suspen-ded solids in surface water (<0.5 m depth) were determined once a month from 1st May to 1st October according to Danish standard procedures.
The fish species were divided into dominant size categories within three functional groups: larger zooplanktivores and benthivores (roach >15 cm, cru-cian carp >15 cm), small planktivores (0+ perch, 0+
roach and roach between 5 and 10 cm), and piscivores (pike >50 cm, pike 30–50 cm, 0+ pike, perch >20 cm, perch 10–20 cm). Only few crucian carp <15 cm was caught during the study period and therefore not considered as an important functional group.
Between-year differences in density or CPUE of the size groups amongst the different functional groups were determined using the Kruskal–Wallis test. Box & Whiskers plots were used to visually determine where any differences lay, as recommended by
S T A T G R A P H I C S
S T A T G R A P H I C S plus software (Manugistics, 1998).
In cases where differences where difficult to recog-nise visually, the Mann–Whitney W-test of S T A T -S T A T -G R A P H I C S
G R A P H I C S was used. The same procedure was
adopted for Secchi depth and concentrations of total phosphorus, chlorophyll a and suspended solids. To elucidate potential cause and effect relationships between the functional groups most likely to interact, separate Pearson’s correlation analyses were used on log (n + 1) transformed annual means. The proce-dure included matching (i) predators to their most likely prey, (ii) predators to other predators, (iii) benthivores to water quality criteria, (iv) zooplank-tivores to water quality criteria and (v) water quality criteria to other water quality criteria (see Table 2 for details).
Results Fish density
Apart from perch >20 cm, there were significant changes in the density of all functional groups over the study period (Fig. 1 and Table 1). The largest of the piscivores, pike >50 cm, increased in abundance after 1997 with a significant increase between 1997 and 1998 (Mann–Whitney W-test, W¼16, P¼0.03), whereas intermediate-sized pike (30–50 cm) declined markedly after 1996. In contrast, the densities of 0+ pike varied little between years, with the exception of 1999 when 0+ pike density was 2.5–5-fold higher. Large perch tended to decline following their intro-duction (Fig. 1), although the effect was not significant (Table 1). Perch between 10 and 20 cm, on the other hand, increased during the period with a marked difference between 1998 and 2000 (Fig. 1), as they recruited from the spawnings of the introduced adults. The recruitment of perch peaked in 1999 (Fig. 1). Crucian carp >15 cm declined throughout the
study period with a clear difference between 1996 and 2000 (Fig. 1). Both roach >15 cm and roach in the 5– 10 cm size class declined strongly between 1997 and 1998 (Fig. 1). Thereafter, larger roach continued to decline, whilst the abundance of smaller roach showed an increasing trend. The abundance of 0+ roach tended to increase slightly from 1996 to 1999 prior to collapse in 2000. Correlations revealed three potential relationships between groups consistent with predation (Table 2). Pike >50 cm was signifi-cantly negatively correlated with both roach >15 cm and crucian carp >15 cm, and perch >20 cm was significantly negatively correlated with roach of 5–10 cm. Within the groups of predators, an unex-pected positive correlation between pike >50 cm and perch >20 cm was found.
0+ roach distribution
The distribution of 0+ roach between the littoral zone and open water varied among years with the percentage of fish in open water ranging from 45%
in 2000 to 98%in 1999 (Table 3).
The mean biomass of 0+ pike in the lake increased three to 10-fold over the considered consumption period in all years, although there were large differ-ences among years (Table 4). For example, the early stocking in 2000 prolonged the consumption period and hence the highest increase in biomass was found in this year. The impact of the early stocking in 2000 is
Fig. 1 Changes during the study period in densities of the principal fish species within different functional groups: P¼piscivores, B¼larger zooplankti-vores and benthizooplankti-vores, Z¼small zoo-planktivores. The full line represents median values and the mean is shown as a single point (+). Also shown are 10, 25, 75 and 90%percentiles.
further illustrated by the fact that 84%of the total 0+ roach consumption by numbers took place during May. The high density of 0+ pike in 1999 led to the highest overall biomass increase (38.2 kg). The maxi-mum number of 0+ roach possibly consumed by the
0+ pike varied 76-fold (between 0.1 106in 1996 and 7.6 106in 1999). In 1998, 1999 and 2000, this number was above the number of 0+ roach estimated to remain in the lake after the consumption period, while in 1996 and 1997 it was below (Table 4).
The density of pike >50 cm in 1998 was estimated to be 2000 individuals with a mean weight of 1700 g, and it was calculated that these could have consumed 11.6 tof prey fish (1700 g ind.)1·0.02%d)1·2000 ind.·
170 days) (Table 5). The perch could have consumed 0.6–2.4 t of prey fish, corresponding to 130 000– 510 000 roach in the size class of 5–10 cm with a mean weight of 4.7 g (Table 5).
Mortality of stocked pike
Estimated mortality of the 0+ pike varied between 62%in 1999 and 89%in 1996, based on the assump-tion that the bulk of the fish originated from the 20 000 individuals stocked each year (Table 4).
Fecundity potential of roach
The fecundity potential of roach declined during the study period, with a distinct drop between 1998 and
Table 1 The Kruskal–Wallis statistic (KW), associated signifi-cance level (P) and total number of replicates (n) for differences in fish density and water quality criteria from 1996 to 2000 in Lake Udbyover. Only the years where perch were present in the lake are included in the tests for perch
Factor KW P n Pike >50 cm 10.7 * 20 Pike 30–50 cm 11.7 * 20 0+ Pike 12.8 * 20 Perch 10–20 cm 5.6 ** 15 Perch >20 cm 11.3 ns 15 Crucian carp >15 cm 12.3 * 25 Roach >15 cm 18.3 ** 25 0+ Perch 8.7 * 15 Roach 5–10 cm 20.5 ** 25 0+ Roach 11.3 * 20 Secchi depth 17.1 ** 28 Chlorophylla 12.3 * 28 Suspended solids 10.6 * 28 Total phosphorus 10.2 * 28 *P< 0.05, **P< 0.01.
Table 2 Pearson’s correlation coefficients and associated significance levels of potential relationships between different groups of fish and water quality criteria based on log (n + 1) transformed annual means. All correlations were calculated separately. Piscivorous fish (P), larger zooplanktivorous and benthivorous fish (B), small zooplanktivorous fish (Z), and water quality criteria (W)
Group Factor P W Pike >50 cm Pike (30–50 cm) 0+ pike Perch (10–20 cm) Perch >20 cm Suspended solids Chlorophyll a Secchi depth Total phosphorus P Pike >50 cm – – – ns 0.97** – – – – P Pike (30–50 cm) ns – ns ns ns – – – – P 0+ Pike – – – ns ns – – – – B Crucian carp >15 cm )0.98** – – – – ns – – – B Roach >15 cm )0.93* – – – – ns – – – Z Roach (5–10 cm) – ns – – )0.88* – – – – Z 0+ Perch – – ns ns ns – ns – – Z 0+ Roach – – ns ns ns – ns – – W Suspended solids – – – – – – ns – W Chlorophylla – – – – – – – ns ns *P< 0.05, **P< 0.01. Habitat 1996 1997 1998 1999 2000 Open water 0.32 106 0.87 106 1.10 106 1.30 106 0.05 106 Littoral zone 0.15 106 0.03 106 0.06 106 0.02 106 0.06 106
Table 3 Estimated numbers of 0+ roach in August in the open water and littoral zone of Lake Udbyover
1999 (Fig. 2), related to a decline in older fish in particular.
The concentration of suspended solids was signifi-cantly reduced in 2000 compared with 1996 (Mann–Whitney W-test, W¼29.5, P¼0.03) (Fig. 3 and Table 1). Chlorophyll-a concentration showed a similar declining trend, with a significant difference between 1996 and 2000 (Mann–Whitney W-test,
Table 5 Consumption data for the stocked perch and pike >50 cm in 1998
Predator Predator biomass (t) Daily ration (%) Days of consumption Possibly
consumed prey biomass (t)
Perch 0.6 1–4 95 0.6–2.4
Pike 3.4 2 170 11.6
Table 4 Data on the potential consumption of 0+ pike on 0+ roach over the consumption period (shortly after stocking to the 21st July). Mean roach population is the 0+ roach estimates from Fig. 1 multiplied by total water volume in the lake, and illustrates the remaining 0+ roach in the lake after the consumption period. Roach consumption by 20 000 0+ pike is the maximum numbers of 0+ roach possibly consumed if all stocked 0+ pike (1000 ha)1) had been present throughout the consumption period
Parameter 1996 1997 1998 1999 2000
Average number of 0+ pike in the lake 2295 2984 2751 7581 3957
Consumption period (d) 47 43 43 41 79
Initial 0+ pike biomass (kg) 3.3 3.4 4.3 11.8 2.6
Final 0+ pike biomass (kg) 12.0 14.3 11.3 50.0 25.4
Average growth (%BW d)1) 2.7 3.4 2.2 3.5 2.9
Daily ration (%BW d)1) 8.2 10.1 6.7 10.6 8.6
Prey biomass possibly consumed (kg) 26.1 32.7 21.0 114.6 68.4
Max number of 0+ roach consumed (106) 0.1 0.3 2.0 7.6 7.4
Mean number of 0+ roach in August (106) 0.5 0.9 1.2 1.3 0.1
Max number 0+ roach consumed by 20 000 0+ pike (106) 0.8 2.2 14.6 20.1 37.6
Fig. 2 The yearly fecundity potential of different age classes of roach in five successive study years.
Fig. 3 Changes in water quality criteria during the study period. Numbers in parentheses are upper values for the respective years exceeding the abscissa. The full line represents median values and the mean is shown as a single point (+). Also shown are 10, 25, 75 and 90% percentiles.
W¼38,P¼0.01). Total phosphorus (TP) concentra-tion also showed a declining trend from mean values >200lg L)1 between 1996 and 1999, to 150lg L)1in 2000. In summer 2000, with reduced concentrations of suspended solids and chlorophylla, Secchi depth was highest, with a mean of 0.72 m (Fig. 3). Despite similar trends of TP, chlorophyll a and suspended solids, these parameters were not significantly corre-lated with each other (Table 2).
There were clear changes in the fish community and water quality over the 7 years of piscivore stocking in Lake Udbyover. Three questions were posed to evaluate the role of stocked piscivorous fish in the observed changes: (i) was the collapse of 0+ roach in 2000 related to piscivores, and if so, was this collapse because of pike and perch stocking? (ii) can predation explain the overall reduction in zooplanktivores and benthivores from 1998 and onwards, and if so, was this effect because of stocking? (iii) did the reduction in zooplanktivores and benthivores influence water quality?
0+ pike stocking
Pike were stocked in the range recommended by Berg et al. (1997) and Prejs et al. (1994). If all stocked pike had survived, they could in theory have consumed the entire roach population estimated to exist in the lake (the August estimate plus those potentially consumed by the existing pike), as was intended by the stocking programme. This is notwithstanding the additional contribution of pike naturally recruited in the lake. However, the lack of a relationship between 0+ pike and 0+ roach density and the fact that the 0+ roach density in late summer in 1996–99 was main-tained at a high level (3–6 ind. m)2) suggests that there was no measurable control of 0+ roach by 0+ pike. Moreover, there was no correlation between potential consumption by the pike and the numbers of roach remaining in August (Pearson,r¼)0.06,n¼5, P¼0.92). In 2000, however, the number of roach remaining at the end of the year was clearly below the values recorded in previous years, and there is thus the possibility that pike had an impact in this year. This effect could be caused by the stocking of pike earlier in the season in 2000, resulting both in the
exposure of 0+ roach at a smaller size to the pike and a prolonged period of pike predation. The question remains why the 0+ pike did not have a significant impact. One possibility is that mortality of the stocked pike was high, estimated at 60–90%even when it was assumed that there was no natural recruitment within the lake. Reasons for poor survival could be (i) inter-and intracohort cannibalism (Grimm & Klinge, 1996; Skov, 2002) exacerbated by the lack of suitable habitat (Skov & Berg, 1999), (ii) predation by bird and fish (Raat, 1988) and (iii) timing of the stocking (Grimm & Klinge, 1996; Skov, 2002). Other possibilities are that the 0+ roach escaped predation by moving into the open water, as suggested by Berget al. (1997), or that the 0+ pike mainly fed on non-fish prey (Skov, 2002).
Correlation analyses suggest a link between perch >20 cm and larger roach (5–10 cm) rather than 0+ roach. This negative relationship is in accordance with the upper prey size of perch 20–30 cm in length, which is about 7–12 cm (Benndorf, 1990). Although we have no quantitative estimate of roach of this size in the lake, a rough estimate of the number present at the beginning of the season can be obtained from the number of 0+ fish present the previous year (900 000 ind.; Table 4), assuming that they are subject to 40%
mortality (Mann, 1973) over the winter. Given the 130 000–510 000 roach in the 5–10 cm size class potentially consumed by the perch added to the lake, the stocked perch could thus have consumed a large fraction (25–95%) of the 5–10 cm roach in the short period following perch stocking. Whilst not conclu-sive evidence, this estimate illustrates the scope of the impact large perch may have on roach populations. Moreover, perch have spawned in Lake Udbyover every year since stocking, which has resulted in an abundant population of perch between 10 and 20 cm within 3 years.
Several studies have shown that perch of this size can have a significant impact on 0+ fish (e.g. Do¨rner, Wagner & Benndorf, 1999; Do¨rner et al., 2001). The lack of a significant relationship between 0+ roach and 10–20 cm perch in the present study could be due to the few data points available, so that these perch might still have a part to play in the collapse of the 0+ roach population in 2000. Moreover, an increase in predation pressure from the 10–20 cm perch may
have affected the behaviour of 0+ roach. In 2000, during peak abundance of the 10–20 cm perch, a shift in habitat use of 0+ roach occurred from open water to the littoral zone. This observation is consistent with an increased predation risk in the open water, the chief habitat of perch (Thorpe, 1977). Although no statistical evidence for a poststocking decline in perch >20 cm was found, a trend was apparent. Possibly, this decline could be related to the fact that perch stocking in 1998 coincided with the peak density of pike >50 cm. However, the positive correlation between the two piscivore groups does not support this idea, but suggests instead that the two species are comple-mentary.
Pike >50 cm, crucian carp and recruitment failure of roach
With no conclusive evidence of a direct predation impact upon 0+ roach, could a simple failure of the adult population to recruit explain the observed collapse in recruitment of 0+ roach in 2000? Plausible explanations for poor recruitment are that the survival rates of eggs or larvae were low or the number of eggs laid was low.
Temperature is often an important factor determin-ing reproductive success and survival (Mills, 1991). However, apart from a warm spring in 2000, which should have improved recruitment (Mills, 1991), no unusual weather conditions were observed. Estimates of the potential number of eggs laid by the roach population indicate that the largest roach make a significant contribution to population fecundity and that the reduction in the density of these large fish over time results in a strong reduction in population fecundity. This reduction contrasts with the density pattern across years of the 0+ age group, which was reduced only in 2000. However, a threshold decline in the number of recruits is typical of fish populations subject to increased adult mortality (e.g. Pitcher & Hart, 1982). Initially, compensation occurs, perhaps through the provision of better growing conditions for the remaining adults or a lack of spawning inter-ference, but subsequently densities decline as the number of eggs laid becomes too low to ensure effective recruitment.
What caused the decline in the spawning stock of roach? The rapid decline in roach >15 cm observed between 1997 and 1998 might have been caused by a
fish-kill resulting from low oxygen concentrations, rather than by predation. However, there is no direct evidence that such a fish kill occurred. The fact that crucian carp, a species exceptionally tolerant to low oxygen concentrations, also declined, whereas the density of large pike increased, further indicates that the fish-kill hypothesis is unlikely.
The negative correlation between the largest roach and their principal predator, large pike, suggests instead that predation was responsible for the decline of roach >15 cm across years. Furthermore, the con-sumption estimates for pike >50 cm indicates that 560 kg prey ha)1 could have been consumed from March to August 1998. This is despite the fact that the obtained estimate of pike from the margin alone is likely to be conservative, as large pike are often distributed throughout the lake (Grimm, 1981; Jepsen et al., 2001). Thus, the estimated consumption could have had a profound impact on the total standing stock of fish likely to be present in a lake of its type (100–800 kg ha)1, Grimm & Backx, 1990). The com-parison of these figures illustrates the scope not only for impacting large roach, but also for contributing to the observed decline in the density of crucian carp, with which pike density was also negatively corre-lated. Predation by pike >50 cm thus could have had an important impact on the principal zooplanktivor-ous and benthivorzooplanktivor-ous fish in the lake through indirect and direct mechanisms, respectively.
Scale samples from pike caught in 1996 and 1998 (Skov, unpubl. data) suggest that two strong year classes 1993 and 1994, each contributed around 50%of the large pike present in this period. Whilst this finding opens the possibility that the pike stocking in 1994 had an impact on the planktivorous fish stock in the lake, although in a different way than expected, it also suggests that in 1993 natural recruitment alone was equally capable of having an impact. However, there is no evidence that such densities had ever been achieved in the past, reinforcing the suggestion that stocking boosted the adult population of pike to levels far above those typically recorded in natural lakes (Craig, 1996).
Changes in water quality
There was a trend of reduced concentrations of TP, chlorophyll a, suspended solids and of increased Secchi depth and hence improved water quality during the study period. By 2000, Secchi depth was
at a peak, although this was not reflected in the chlorophyllaconcentration, which was maintained at 76lg L)1. This is in accordance with the lack of a significant relationship (using both summer and winter data from all years) between Secchi depth and the chlorophyll-a concentration in the lake. Instead, suspended solids could have influenced Secchi depth (Pearson r¼)0.54, n¼52, P< 0.0001). Whilst there was no significant relationship between the density of crucian carp and suspended solids in the lake, the importance of benthivorous fish for sediment resuspension has been frequently observed in other studies (e.g. Zambrano, Scheffer & Martinez-Ramos, 2001). In 1996, a population of 6500 indivi-duals above 20 cm was estimated to be present in the lake using mark⁄recapture methodology (Skov, unpubl. data). At an average weight of 450 g (from gillnet samples in the same year), the resultant biomass of 142 kg ha)1 would be more than capable
of exerting a negative impact upon Secchi depth through re-suspension (Breukelaar et al., 1994). This calculation even ignores the potential contribution of large roach, whose biomass derived from CPUE-estimates probably was of the same order of magni-tude. By 2000, the densities of both crucian carp and roach had been reduced three fold, and a resultant beneficial impact upon suspended solids and conse-quently upon Secchi depth in 2000, seems possible.
This study supports the hypothesis by Benndorf (1990) and others that piscivorous fish may be a significant structuring force in shallow eutrophic lakes. Our data suggest that the collapse in the recruitment of roach was ultimately linked to preda-tion, although the predicted direct route through the food chain was not followed: Stocking of 0+ pike may have ultimately boosted the population of large pike in the lake, which instigated a decline in larger roach and crucian carp. The decline in large roach, in turn, appeared to reduce fecundity of the population. Whether this reduction initiated the collapse of the recruitment of 0+ roach in 2000 is, however, an open question. Predation by 1+ and 2+ perch, which had resulted from the successful spawning of large adults introduced into the lake in 1998, or by 0+ pike, may also have been instrumental. A combination of effects is perhaps most likely. However, if there was any
impact of 0+ pike, it appears to have been achieved through stocking earlier in the year, potentially promoting a far higher predation pressure per survi-ving 0+ pike than was typical during the rest of the study. Whatever the case, the present study suggests the need for considerable refinement and evaluation of current 0+ pike stocking practice, for example in relation to optimising stocking time, stocking density and size of the stocked individuals, and indicates the potential of large perch and pike as tools for lake management.
We thank all technicians at DIFRES, especially Morten Carøe & Hans Jørn Christensen for skilful technical assistance, as well as all friends, past and present, who helped out. We also thank Ju¨rgen Benndorf as well as two anonymous referees for improving the manuscript. This study was supported by the research programme ‘The Role of Fish in Ecosystems, 1999– 2001’, funded by the Danish Ministry of Food, Agriculture and Fisheries.
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(Manuscript accepted 19 July 2002)