Pelagic trophic transfer efficiency in an oligotrophic, dimictic deep lake (Lake Stechlin, Germany) and its relation to fisheries yield

ELSEVIER

Limnologica 34,264-273 (2004) http://www.elsevier.de/limno

LIMNOLOGICA

Pelagic trophic transfer efficiency in an oligotrophic, dimictic deep lake (Lake Stechlin, Germany) and its relation to fisheries yield Michael Schulz 1,*, Rainer Koschel 2, Claudia Reese 2, Thomas Mehner 1 Leibniz-lnstitute of Freshwater Ecology and Inland Fisheries, Berlin, Germany 2 Department of Limnology of Stratified Lakes, Leibniz-lnstitute of Freshwater Ecology and Inland Fisheries, Stechlin / OT Neuglobsow, Germany Received: June 2, 2004 • Accepted:August 11, 2004

Abstract We investigated trophic transfer efficiency in the pelagic food chain of deep, oligotrophic Lake Stechlin (Germany) by analyses of the primary, secondary, and fish production. Primary production between April and November 2000 was estimated at 78 g C m -z, pelagic secondary production at 14 g C m -2, and production of the main planktivorous fish species [European cisco, Coregonus albula (L.)] at 0.77 g C m -2. Thus, trophic transfer efficiency between primary and pelagic secondary production was around 18%, whereas between pelagic and fish production around 6%. The high efficiency at the first step of the chain is discussed to be due to the high food quality in oligotrophic lakes due to the dominance of Bacillariophyceae and Chlorophyceae rich in essential fatty acids. In turn, the relatively low trophic transfer efficiency between the secondary and the fish production is mainly explained by the avoidance of calanoid copepods as food source by the ciscoes. Concerning the trophic transfer efficiency, results from this study support the general assumption of a 10% transfer between neighbouring trophic levels within ecosystems.

Key words: Oligotrophic lake - trophic transfer - production - Coregonus - fisheries management

Introduction Fish are the main protein supply for more than 1 billion humans (FAO 2002). Decreasing populations of fish have increased the demand to understand trophic relationships and population dynamics within aquatic ecosystems in the last century. Those research activities arose particularly in marine ecosystems because entire fish populations became extinct from overfishing by commercial fisheries, for example the north American cod (Gadus morhua) population (e.g. HUTCHINGS 2000; HUTCH~NGS& MYERS 1994; FRANK

& BRICKMAN 2001), flatfishes (e.g. Pseudopleuronectes americanus, RICE & COOPER 2003) and salmon (e.g. Oncorhynchus tshawytscha, NOAKESet al. 2000). Overfishing is similarly important in freshwater fisheries, especially in the developing countries of Africa, Asia, Eastern Europe and South America (GOPAL & WETZEL 1995; OGUTUOHWAYOet al. 1997). Scholars suggest most freshwater fish stocks are at risk of overfishing (FAO 1997). Fisheries are expected to become an even larger food resource when the global population reaches 10 billion in the new century (e.g. TANAKA2002).

*Corresponding author: Michael Schulz, Leibniz-lnstitute of Freshwater Ecology and Inland Fisheries, Department of Biology and Ecology of Fish, RO.B. 850 119, D-12561 Berlin, Germany; Phone: ++4933082699-57; Fax: ++4933082699-17; e-mail: [email protected] 0075-9511/04/34/03-264 $ 30.00/0

Limnologica (2004) 34,264-273

Pelagic trophic transfer efficiency in Lake Stechlin (Germany) Several models for sustainable management of fish populations have been developed, such as theoretical estimates of the maximum sustainable yield for single or multi species fisheries (e.g. GORDON 1954; PITCrmR & HART 1982; KtNC 1995; HOAGLAND& JrN 1997). Other models test stock and recruitment relationships (e.g. JENMNGS 2000). One problem in most studies is their need for considerable technical and financial effort, as well as a lot of manpower, to collect basic data on fish populations. A more practicable tool is a yield estimation, assuming a defined trophic transfer efficiency (TTE) of organic carbon between neighbouring trophic levels within aquatic ecosystems. Especially for marine systems it was shown that the TTE between trophic levels is usually around 10% (PAULY& CHRISTENSEN1995). Thus, the marine fish production can be easily estimated when primary production and the number of the trophic levels are known. In contrast, detailed studies of the TTE in freshwater lake ecosystems are rare and difficult to apply because of the complicated links within the pelagic food web in lakes (e.g. CARPENTERet al. 1985; CARPENTER et al. 1987; PERSSONet al. 1988; JEPPESENet al. 1997; GAEDKE 1998). To test the relationship between TTE and yield of freshwater fisheries, a system in which the pelagic food web is relatively simple is useful. Oligotrophic Lake Stechlin (Germany, Brandenburg) is ideal due to its low number of aquatic taxa involved in the pelagic trophic relationships (CASPER 1985; KOSCI-mL& ADAMS 2003). In a yearly mean, the total crustacean biomass is represented by just two copepod species, namely Eudiaptomus gracilis and Eurytemora lacustris (KASPRZAK & SCIqWABE 1987; WE~LER et al. 2003). In addition, the pelagic area of the lake is dominated by more than 95% of the total fish catch by two species of ciscoes, Coregonus albula and C. fontanae (SCHULZ& FREYHOF2003; SCHULZet al. 2003) making Lake Stechlin a very good model system, particularly for estimates of TTE, fish biomass, and fish production. Goals of this study were i) to estimate the pelagic trophic transfer efficiency in Lake Stechlin by detailed analyses of the primary, zooplankton secondary, and fish production and ii) to evaluate the sustainability of the commercial fisheries on the lake by comparing the annual cisco yield to the estimate of total cisco production.

Material and Methods Study site Lake Stechlin (Brandenburg, Germany, 53°10'N, 13°02'E) is situated approximately 100 km north Berlin (Fig. 1). The medium sized (4.23 km 2 surface area) lake has a maximum depth of 69.5 (average 23.3 m), its the second deepest lake in northern Germany (KOSCHEL & ADAMS 2003). According to the phospho-

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ms load (0.04-0.07 g TP m -2 year-l) and a primary production of 121 g C m -2 year-1, it has preserved its oligotrophic status to present (KOSCHELet al. 2002). The phytoplankton community is dominated by centric diatoms, cyanobacteria of picoplanktic size, and green algae (PADISAK et al. 1998; PADlSAK et al. 2003). Calanoid copepods (Eudiaptomus gracilis and Eurytemora lacustris) dominate the pelagic zooplankton community, followed by cyclopoid copepods (Acanthocyclops robus-

tus, Cyclops kolensis, C. vicinus, Mesocyclops leuckarti, Paracyclops sp., Thermocyclops oithonoides) and cladocerans (Bosmina coregoni, B. longirostris, Bythotrephes longimanus, Ceriodaphnia spp., Daphnia cucullata, D. hyalina, Diaphanosoma brachyurum and Leptodora kindtii) (KASPRZAK & SCHWABE 1987; SCHULZ et al. 2003). In the lake, 13 fish species have been found in a composition which is typical for this lake type (ANWANDet al. 2003). But the pelagic fish community is only dominated by two coregonid species, the European cisco (Coregonus albula) and the Fontane cisco C. fontanae (SCHULZ& FREYHOF2003). There is one single commercial fishery at the lake, mainly fishing for European cisco, perch (Percafluviatilis), and pike (Esox lucius).

Calculations Phytoplankton primary production was analysed once per month in April and November 2000 and biweekly from May to October 2000. Primary production was averaged when two measurements for one month were available. All samples were taken and exposed at the deepest location of the lake (Fig. 1) in 0, 2.5, 5, 7.5, 10, 12.5, 15, 17.5, 20 and 25 m depth. Primary production was estimated by the 14C method (STEEMAN-NIELSEN1952; KOHLER et al. 1999). Duplicate dark and light glass bottles (volume 300 ml) were supplemented with approximately 370 kBq [14C]NaHCO3 and incubated in situ for 4 hours (usually from 1000 to 1400 hours). After incubation the water samples were fixed with 1 ml formaldehyde. From each dark and light duplicate 25 ml subsamples were filtered (vacuum did not exceeded 50 kPa) through 6 ,um (type Schleicher & Scht~ll NC 60) poresize membrane filters to stop total primary production. The amount of 14C radioactivity of each filter was measured by liquid scintillation counting (liquid scintillation counter: Canberra-Packard, type 1900 TR, cocktail Ultima Gold, absorber Carbo-Sorb). The value of the dark bottle was subtracted from the value of the light bottle. To correct for isotope discrimination a factor of 1.06 was used. Further details of standardization, deterruination of activity of the 14C working solution, and corrections of 14C measurements are described in KOHLERet al. (1999). Limnologica (2004) 34,264-273

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T

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500 rn Fig. 1. Bathymetric map of Lake Stechlin (CASPER1985) and its location in Germany (black square). The circle indicates the sampling location for primary production, zooplankton and fishing at the deepest point of the lake.

The 4 hour primary production measurements were extrapolated to daily rates by applying a procedure based on radiation data from the German Weather Service (Station Lake Stechlin) Cassirrdd = CassimJex p *

QG / Qexp

(Equation 1)

where Cas~im/dis the daily primary production, QG is the daily global radiation and Qexpthe 4 h global radiation. Limnologica (2004) 34,264-273

Zooplankton samples of herbivorous species were collected twice a month from April to November 2000. To analyse the vertical distribution and to estimate the population centres of the zooplankton species (HOFMANN 1972), samples were collected with a closing net (mesh size 90 pm, length 1.2 m, opening area 0.027 m 2) in 5 m intervals from the surface to the bottom at the deepest point of the lake (Fig. 1). Simultaneously, tem-

Pelagic trophic transfer efficiency in Lake Stechlin (Germany) perature was measured with an OXI 196 meter (WTW, Weilheim, Germany) at 5 m intervals. Diurnal differences in zooplankton distribution were determined by sampling at midday and the following midnight on each sampling day. All samples for quantitative analyses were preserved in a formalin-sucrose solution (HANEY & HALL 1973). Using an inverted microscope, zooplankton was identified to species level. Subsamples were counted and measured until 30-100 specimens of each dominant species were analysed. Thus, the total abundance of a single zooplankton species was estimated by summarizing the abundances at all depth intervals while biomass (mg C m -2) was calculated using carbon-length correlations (WlNBERG 1971; BOTTRELL et al. 1976; KASPRZAK 1984). No obvious differences in vertical zooplankton distribution between night and day were observed. Therefore, abundance was calculated as average between day and night samples. The calculation of zooplankton production followed STOCKWELL ~% JOHANNSSON(1997), using a regression model based on production/biomass ratios. As suggested, the equation p = 10(-0.26log(M)1.36)1.09 M N

(Equation 2)

was used when the population centre of the respective zooplankton species was in a temperature regime below 10 °C, and the equation p = 10(-0.23 log(M)-0.73) 1 . 1 2

MN

(Equation 3)

was used when the population centre of the population was in water depths with temperatures higher than 10 °C, respectively. P is the daily production ~ug dry weight m -2 day-l), M is the mean individual dry weight ~ g ) for the respective species, and N is the abundance (individuals m -z) of the given species on that day for both equations. Dry weight was converted into carbon content as given by B OTTRELLet al. (1976). Zooplankton species were grouped in small cladocerans (B. longirostris, B. coregoni and Ceriodaphnia sp.), planktonic cyclopoid copepods (A. robustus, C. kolensis, C. vicinus, M. leuckarti, Paracyclops sp. and T. oithonoides) and calanoid copepods (E. gracilis, E. lacustris and H. ap-

pendiculata). Due to the good ability to escape and related problems to quantify the predatory zooplankton species Bythotrephes longimanus and Leptodora kindtii (e.g. KARABIN 1971), we were not able to estimate the abundance and production of those species. The estimates of cisco abundance and biomass using hydroacoustic recordings are described in detail by MEHNER & SCHULZ (2002). Separation of both cisco species using the hydroacoustic data is not possible, and the species were combined for the estimates of fish production. In short, hydroacoustic recordings were done at 12 transects across the lake during nightly surveys once

267

per month between April and November 2000. Due to technical problems with the equipment no data were available in July, and abundances for this month were linearly interpolated between June and August. A SIMRAD EY-500 split-beam echo-sounder with 120 kHz operating frequency (10 ° x 4 ° beam shape, pulse length 0.1 ms, 2-10 pings s-1) was used. Before each survey, the echo-sounder was calibrated with a standard copper sphere. All surveys were conducted during complete darkness at least 1 h after sunset since it was known from previous investigations that cisco strongly dispersed over the water column during the night enabling a high single target resolution (60-75% single targets). Results from the echo-sounding transects were stored on a computer and evaluated by the SIMRAD EP 500 analysis software (version 5.2; abundance estimates) and a test version of Echoview (version 2.20.53, SonarData, Australia; frequency distribution of single targets). Volume backscattering strength (Sv) and target strength (TS) from single fish echoes were separately calculated by simultaneously applying a 20 and a 40 log R time varied gain (TVG) function, a feature which is included in the EP 500 software. To account for the near field effect during vertical beaming, all echoes from a water depth <4 m were excluded. For the analyses, -55 dB was used as the lower threshold for target strength and volume backscattering, excluding echoes from fishes <2.5 cm total length (Lr). The TS of the targets was converted into fish lengths by the general equation for a 120 kHz echo-sounder by LOVE (1971) TS = 19.1 log (Lr) - 63.85

(Equation 4)

where TS in dB and L r are cm. The applicability of this formula for ciscoes has been shown previously (MEnNER et al. 2003). Ciscoes were grouped into age groups 0+, 1+, and 2+ and older according to the length (MEnNER & SCHULZ2002). Production of ciscoes was calculated by the discrete increment summation method (NEWMAN & MARTIN 1983). It was assumed ciscoes grew from the first day in April until the last day in November, and growth of ciscoes was linear at the period. Daily growth rates in length for the three age groups were calculated from an age-length key for cisco in the lake (ANWANDet al. 2003, for the age group 2+ and older the fish lengths from the age groups 2+ to 5+ were averaged); daily mass increments were calculated by the length-mass regression for C. albula from Lake Stechlin (ANWAND et al. 2003). Daily mass increase per age group was multiplied by the average abundance of those age groups, calculated by linear interpolation of available abundance estimates from the hydroacoustics to the respective day. The total daily cisco production was summarized from the three age groups, and the annual production was then the total Limnologica (2004) 34,264-273

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sum of daily fish production between 1 April and 30 November 2000. Fresh weight of fish was converted into carbon content by dividing by 10 following W~Nt3ERG (1971). There is only one single commercial fishery at Lake Stechlin. The fishing season for ciscoes extended from April to November 2000. All ciscoes caught by commercial fisheries were measured and weighed. Recreational fishers do not fish for ciscoes and thus the commercial fish yield was identical to the total cisco catch removed from Lake Stechlin.

ratio between daily primary and zooplankton secondary production and between daily zooplankton secondary and fish production separately for each of the eight months sampled in 2000. Annual total efficiency was calculated based on the annual production rates of each trophic level. To limit the calculation of the TTE between zooplankton and cisco production, diet inspection of fish was necessary. Three fleets of gill nets (ten different mesh sizes each: 6, 8, 10, 12, 15, 20, 22, 30, 40 and 50 mm knot to knot) were used to catch ciscoes monthly between April and November 2000. Fishing took place simultaneously with the echo-sounding surveys near the deepest point of the lake (Fig. 1). One fleet was exposed at the lake bottom, another in the hypolimnion at a depth of about 20 m and the third at the surface.

Trophic transfer efficiency (TTE) Transfer efficiency between trophic levels in the pelagic area of Lake Stechlin was estimated by calculating the

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Fig. 2. Average daily production rates (mg C m-2 day ~) of (a) primary production, (b) secondary production of the herbivorous zooplankton community, and (c) production of ciscoes in Lake Stechlin for the eight months between April and November 2000.

Pelagic trophic transfer efficiency in Lake Stechlin (Germany) Biomass proportions of food organisms in the guts were determined volumetrically. A total of 264 ciscoes in the range from 6.5 to 22.2 cm total length were used for diet analyses,

269

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The total annual primary production from April to November 2000 was 78 g C m-2. Highest daily production was observed in June (564 mg C m-2 d-1) whereas the lowest daily production was measured in November (119 mg C m-2 d-1) (Fig. 2a). The zooplankton secondary production for the production period between April and November was approximately a fifth compared to the primary production, with an annual rate of 14 g C m-2 (Fig. 2b). For cladocerans, populations were most productive in spring (mostly B. longirostris), summer (mostly Daphnia spp. and Bosmina coregoni), and late summer (mostly Diaphanosoma brachyurum and Ceriodaphnia sp.). Compared to all other species or groups, calanoid copepods were most productive during the investigated period with exceptions in August and October. The production of nauplii and cyclopoid copepods fluctuated only slightly from April to November but was less than that of the calanoids, Total cisco production was estimated at 0.77 g C m-2, total production for all age groups and between April and October (Fig. 2c). After a period with relatively low daily production values in April, May, and June (0.8, 1.8 and 2.7 mg C m-2 d-~), production increased up to 4.3 mg C m-2 d-1 in August, and ranged around 4 mg C m-2 d-~ from September to November. Ciscoes in age of 0+ and 1+ were much more productive than fish in age of 2+ and older due to the substantially higher abundances of the juvenile fish (Fig. 2c). Annual total cisco production corresponds to 75.9 kg fresh weight ha-l a-1 or 33,000 kg fresh weight for the entire lake in a year. Considering just the age groups of 2+ or older relevant for the fisheries, production was 3.6 kg fresh weight ha-~ a-~ or 1560 kg fresh weight for the entire lake. The annual yield of the commercial fisheries was 1050 kg of ciscoes in the year 2000. Compared to the annual production estimates, the fisheries took around 60% of the production in age classes 2+ or older.

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Trophic transfer efficiency (TTE) of Lake Stechlin The TTE between primary and zooplankton secondary production was 18.1%, based on the total annual primary and zooplankton secondary production. Monthly TTE rates were observed to have been lowest in April (7.1%),

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2000 Fig. 3. Average daily trophic transfer efficiency (TTE) between primary and secondaryproduction (dark circles) as well as between secondary and cisco production (white circles) in Lake Stechlin for the eight months between April and November 2000.

III Herbivorouszooplankton @Carnivorous zooplankton 13Benthic food ]

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highest in September (38.1%) and November (33.1%). A TTE of around 15% was estimated from May to August and October 2000 (Fig. 3). Gut analyses of the ciscoes demonstrated the fish did not feed exclusively on herbivorous zooplankton species (Fig. 4), but ingested benthic diet as well. Therefore, the TTE was corrected by calculating only the transfer from zooplankton to fish production. Based on the total annual production values, the TTE between zooplankton secondary and cisco production was 5.5%. Monthly estimates showed, that the TTE was between 2.6% and 3.8% from April to June. Higher values (5.5%-11.6%) were observed from July to November (Fig. 3). Based on annual production sums, the TTE between primary and cisco production was exactly 1%. Limnologica (2004) 34,264-273

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Discussion

Production and sustainability As shown in MEHNER& SCHULZ(2002), fish stock estimates using hydroacoustics correlated with gillnet catches is a promising approach in quantitative fisheries biology, especially for deep lakes where the pelagic area is inhabited by one or just a few fish species. The disadvantage of the monthly technical effort and the related age and length analyses of the fish is counterbalanced by obtaining detailed data of the annual fish production in lake ecosystems. Recent intercalibrations of hydroacoustic systems showed a remarkably high correspondence of fish biomass estimates both within and between different devices (MEHNERet al. 2003; WANZENBOCKet al. 2003). Thus, the estimated cisco biomass and its calculated production there might be reliable for Lake Stechlin. However, the slightly slower growth of C. fontanae (ANWANDet al. 1997; SCHULZ& FREYHOF2003) and its inclusion into the population estimates of C. albula is an error factor. But, according to a preliminary estimate the abundance of the Fontane cisco is less than 10% of the total cisco abundance. Consequently, the correct growth data of the Fontane cisco in the production estimates would result only in minor deviation from the present estimates. The estimated production for ciscoes older than two years was very low, 6.5% of total cisco production. A generally slow growth of the ciscoes from Lake Stechlin and years with low commercial yields were reported previously (BAuCH 1956; MgILLER 1966; ANWAND 1973). Intraspecific competition could be a reason for year class fluctuations resulting in slower growth of single year classes as was shown for example in Finnish lakes (e.g. SARVALAet al. 1998a). However, the fisherman at Lake Stechlin took around 60% of the production of fish aged 2+ or older. Even when the available production of harvestable age classes was exploited to 60% here, the amount of ciscoes kept by the fisherman compared to the total production was just around 3.5%. Based on exploitation experiments, TOIVONEN (1991) suggested that sustained annual fish yield might be 20-25% of total fish biomass. Similar yields were discussed by SARVALAet al. (1998b), based on results for northern waters (BORGMANNet al. 1984; HOUDE & RUTHERFORD 1993). More recently, SARVALA et al. (1999) showed for the African Lake Tanganyika that an exploitation rate of about 25% of the annual production for the pelagic planktivorous fish Stolothrissa tanganicae was sustainable. Subsuming, our results suggest, that the commercial cisco fisheries at Lake Stechlin was sustainable. Mentioned above, assumption of a 10% energy transfer between trophic levels was a good estimate of cisco production. Comparing our results with other established models (KALFF2002) which estimate fish producLimnologica (2004) 34,264-273

tion or fish yields in northern temperate lakes, our calculations were mainly corroborated. DOWNINGet al. (1990) estimated the annual fish production based on primary production rates. Applying their regression, about 63.5 kg fresh weight of fish ha -1 a-1 would be produced in Lake Stechlin. Similarly, HANSON & LE~6ETT (1982) suggested a method to estimate fisheries yields based on total phosphorus concentration. Using their equation, 4.8 kg fresh weight ha -1 a-1 could be harvested from Lake Stechlin. The estimates arising from DOWNIN~ et al. (1990), as well as those from HANSON & LE~CETT (1982) correspond well to our results. But, other estimation procedures like that given by RANDALLet al. (1995) supply lower production values or, in case of KN~)SCHE & BARTHELMES(1998), higher fish yield estimates. RANDALLet al. (1995) also used total phosphorus concentration as base parameter to calculate the fish biomass, then estimated fish production from the fish biomass. Compared to our results and those mentioned before, the predicted production of 13.9 kg fresh weight ha-1 a-1 seems to underestimate fish production. More parameters than primary production and phosphorus concentration are included in the model to estimate the sustainable fish yield by KN6SCHE & BARTHELMES(1998). Herein, lake characteristics like maximum depth and the size of the hypolimnetic area are added in the calculations. This set of regressions would predict a yield of around 8.6 kg fresh weight ha -1 a-~ thus substantially exceeding our estimates. Anyhow, all methods, except for RANDALLet al. (1995), should be close to reality in lakes with evenly distributed age-classes of fish.

Trophic transfer efficiency Energy flow through the pelagic area of Lake Stechlin was quite close to the theoretical value arising from the model with a TTE of 10% between neighbouring trophic levels (PAULY& CHRISTENSEN1995). But, a general pattern, energy transfer efficiency between phytoplankton and zooplankton increases with decreasing trophy in deep lake ecosystems (LACROIX et al. 1999). Monthly TTE between primary and zooplankton secondary production reached values above 10% in deep, oligotrophic Lake Stechlin (Fig. 3). In particular, TTE was highest in September, caused by high production in the zooplankton community on the one hand and a relatively low primary production on the other hand. One reason for high transfer efficiencies at the pelagic producer-consumer interface under oligotrophic conditions could be, that food of the herbivorous zooplankton is of high quality. Highly unsaturated fatty acids, which can be an important food quality factor (WACKER& VON ELERT 2001; M~)LLER-NAVARRAet al. 2004), are certainly available in Lake Stechlin because of the dominance of centric diatoms and green algae. These algae contain large

Pelagic trophic transfer efficiency in Lake Stechlin (Germany) amounts of highly unsaturated fatty acids (= HUFA, see COBELAS & LECADO 1989; A~mGRENet al. 1992), whereas HUFA's are scarcely found in cyanobacteria. Indeed, cyanobacteria were relatively rare in Lake Stechlin in 2000 (PADISAKet al. 2003). Thus, due to the dominance of Bacillariophyceae and Chlorophyceae good food quality for the herbivorous zooplankton could be confirmed. In general, primary production values were higher in spring and summer compared to autumn. Thus, at almost similar levels for zooplankton secondary production TTE was lower here. The TTE between zooplankton secondary and fish production was very low in April and May, then increased with hatching of the larvae of C. albula and increased biomass production related to higher water temperatures and food availability. Two reasons might be responsible for a generally lower TTE between zooplankton secondary and cisco production. First, ciscoes were not exclusively planktivorous. Feeding on herbivorous zooplankton species not only increased their biomass, but energy and matter were available from benthic food (Fig. 4). Estimates of TTE of the total diet uptake including those from benthic origin would increase the pelagic TTE between secondary production and fish. In addition, the neglected influence of L. kindtii and B. longimanus in the food chain also reduced the estimates of the pelagic TTE between zooplankton and fish. Second, the zooplankton secondary production between April and November was represented with more than 50% by the production of calanoid copepods. It was shown, that calanoid copepods are negatively selected by ciscoes, which is caused by their good escape ability (DRE~ER et al. 1980; SC~ULZ et al. 2003). A relatively low proportion of copepods was also found in the diet of ciscoes from Lake Stechlin (ScI-~LZ et al. 2003). Therefore, the production of copepods is difficult for ciscoes to use and this may decrease the overall energy transfer between zooplankton and fish. In summary, comparing primary and fish production, the assumption of a 10% TTE between each of the trophic levels involved was almost perfectly reflected in the data, corroborating the earlier summary by PAULY & CHRISTENSEN (1995) that on average most pelagic food webs show a relatively good correspondence to the theoretically predicted energy loss of 90% per trophic level.

Acknowledgements This study was financially supported by a grant form the German Federal Environmental Foundation (DBU). Thanks to Monika Valentin and Christian Helms, Leibniz-Institute of Freshwater Ecology and Inland Fisheries, and Adolf, Rainer and Ulrike BGttcher, "Fischerei Stechlinsee" for logistic and technical support.

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References AHLGREN,G., GUSTAFSSON,I. B. & BOBERG,M. (1992): Fatty acid content and chemical composition of freshwater microalgae. J. Phycol. 28: 37-50. ANWAND,K. (1973): Gew~isserverzeichnis der Seen- und Flugfischerei der DDR. Berlin. ANWAND,K., STAAKS,G. & VALENTIN,M. (1997): Zwei unterschiedliche Formen von Coregonus albula L. (Teleostei; Coregonidae) im nordbrandenburgischen Stechlinsee (Deutschland). Z. Fischk. 4: 3-14. ANWAND,K., VALENTIN,M. & MEnNER, T. (2003): Species composition, growth and feeding ecology of fish community in Lake Stechlin - an overview. Arch. Hydrobiol., Spec. Issues Advanc. Limnol. 58: 237-246. BAUCH, G. (1956): Chemismus und Fischn~ihrprodnktion in den yon der Kleinmar~ine (Coregonus albula (L.)) bewohnten norddeutschen Gew~issem. Abh. Ber. Naturkde. Vorgesch. Magdeburg 10: 15-36. BORGMANN,U., SHEAR,H. & MOORE,J. (1984): Zooplankton and potential fish production in Lake Ontario. Can. J. Fish. Aquat. Sci. 41: 1303-1309. BOTTRELL,H. H., DUNCAN,A., GLIWICZ,Z., GRYGIEREK,E., HERZIG, A., HILLBRICHT-ILLKOWSKA,A., KURASAVA,H., LARSSON,P. & WEGLENSKA,T. (1976): A review of some problems in zooplankton production studies. Norw. J. Zool. 21: 477-483. CARPENTER,S. R., K~TCnELL,J. F. & HODGSON,J. R. (1985): Cascading trophic interactions and lake productivity. BiGscience 35: 634-638. CARPENTER,S. R., KITCHELL,J. F., HODGSON,J. R., COCHRAN, P. A., ELSER,M. M., LODGE,D. M., KRETSCHMER,D. ~%HE, X. (1987): Regulation of primary productivity by food web structure. Ecology 68: 1863-1967. CASPER,S. J. (ed.) (1985): Lake Stechlin - A temperate oligotrophic lake. Dordrecht, Boston, Lancaster. COBELAS,A. M. & LEC~IADO,Z. J. (1989): Lipids in microalgae: A review. Biochemistry - Grasas y Aceites 41): 118-145. DOWNING,J. A., PLANTE,C. & LALONDE,S. (1990): Fish production is correlated with primary productivity, not the morphoedaphic index. Can. J. Fish. Aquat. Sci. 47: 1929-1036. DRENNER,R. W. & MC COMAS,S. R. (1980): The roles of zooplankton escape ability and size selectivity in the selective feeding and impact of planktivorous fish. In: W. C. KERFOOT(ed.), Evolution and ecology of zooplankton communities, pp. 587-593. London. FAO, Food and Agriculture Organisation of the United Nations (1997): Overfishing is a global threat. Nature 386: 107-107. FAO, Food and Agriculture Organisation of the United Nations (2002): The State of World Fisheries and Aquaculture. Rome. FRANK,K. T. & B RICKMAN,D. (2001): Contemporary management issues confronting fisheries science. Journal of Sea Research 45: 173-187. GAEDKE,U. (1998): The response of the pelagic food web to reoligotrophication of a large and deep lake (L. Constance): evidence for scale-dependent hierarchical patterns. Arch. Hydrobiol., Spec. Issues Advanc. Limnol. 53:317-333. Limnologica (2004) 34,264-273

272

M. Schulz et al.

GOPAL,B. & WETZEL,R. G. (1995): Preface. In: B. GOPAL& R.G. WETZEL(eds.), Limnology in developing countries, p. vii. New Delhi. GORDON, H. S. (1954): The economic theory of a CommonProperty-Resource: The Fishery. J. Politic. Econ. 62: 124-142. HANEY,J. F. & HALL,D. J. (1973): Sugar-coated Daphnia: A preservation technique for Cladocera. Limnol. Oceanogr. 18: 331-333.

HANSON,J. & LEGGETT,W. (1982): Empirical prediction of fish biomass and yield. Can. J. Fish. Aquat. Sci. 39: 257-263. HOAGLAYO,D. S. & JIN, D. (1997): A model of bycatch involving a passive use stock. Marine Resource Economics 11: 11-28.

HOFMANN,W. (1972): Zur Populations6kologie des Zooplanktons im Plul3see. Verb. Internat. Verein. Limnol. 18: 410-418. HOUDE, E. D. & RUTHERFORD,E. S. (1993): Recent trends in estuarine fisheries: Predictions of fish production and yield. Estuaries 16: 161-176. HUTCHINGS,J. A. (2000): Collapse and recovery of marine fishes. Nature 406: 882-885. HUTCHINGS,J. A. & MYERS,R. A. (1994): What can be learned from the collapse of a renewable recourse - Atlantic Cod (Gadus morhua), of Newfoundland and Labrador. Can. J. Fish. Aquat. Sci. 51: 2126-2146. JENNINGS,S. (2000): Patterns and prediction of population recovery in marine ecosystems. Rev. Mar. Biol. Fish. 111: 209-231. JEPPESEN,E., JENSEN,J. P., S~NDERGAARD,M., PEDERSEN,L. J. & JENSEN,L. (1997): Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342/343:151-164. KAI~ABIN,K. (1971): A comparison of two methods of sampling the plankton predator Leptodora kindtii (FOCKE) (Crustacea, Cladocera). Bulletin de la Acad6mie Polonaise des Sciences, S~rie des Sciences Biologiques 3: 197-200. KASPP,ZAK, P. (1984): Bestimmung des K6rperkohlenstoffs yon Planktoncrustaceen. Limnologica 15:191-194. KASPRZAK,P. & SCI-IWABE,W. (1987): Some observations on the diurnal vertical migration of zooplankton in a stratified oligotrophic clear water lake (Lake Stechlin, GDR). Limnologica 18: 297-311. KALFF, J. (2002): Limnology: Inland water Ecosystems. New York. KINr, M. (1995): Fisheries biology, assessment and management. Oxford. I~6scrtE, R. & BARTrtELMES,D. (1998): A new approach to estimate lake fisheries yield from limnological basic parameters and first results. Limnologica 28: 133-144. KOHLER,J., KOSCrtEL,R. & ROSSBERC,R. (1999): Primgrproduktionsmessungen mit der Radiokohlenstoffmethode. In: W. YON T~MPLING& G. FRIEDRtCH(eds.), Methoden der Biologischen Gew~isseruntersuchungen, pp. 450-458. Jena, KOSCHEL, R. & ADAMS, D. (2003): Preface: An approach to understanding a temperate oligotrophic lowland lake (Lake Stechlin, Germany). Arch. Hydrobiol., Spec. Issues Advanc. Limnol. 58: 1-9.

KOSEHEL,R. H., GONSIORCZYK,T., KRIENITZ,L., PADISAK,J. & Sc~rZ~ER, W. (2002): Primary production of phytoplankLimnologica (2004) 34,264-273

ton and nutrient metabolism during and after thermal pollution in a deep, oligotrophic lowland lake (Lake Stechlin, Germany). Verb. Internat. Verein. Limnol. 28: 569-575. LACROIX, G., LESCHER-MOUTOUE,F. & BERTOLO,A. (1999): Biomass and production of plankton in shallow and deep lakes: are there general patterns? Ann. Limnol. 35: 111-122. LOVE, R. H. (1971): Dorsal aspect of an individual fish. J. Acoust. Soc. Amer. 49: 816-823. MEHNER,T. & ScrruLz, M. (2002): Monthly variability of hydroacoustic fish stock estimates in a deep lake and its correlation to gill net catches. J. Fish Biol. 61: 1109-1121. MEHNER, T., GASSNER, H., SCH~Z, M. & WANZENBOCK,J. (2003): Comparative fish stock estimates in Lake Stechlin by parallel split-beam echosounding with 120 kHz. Arch. Hydrobiol., Spec. Issues Advanc. Limnol. 58: 227-236. MOLLER,H. (1966): Die ftir die Kleine Marline (Coregonus albula (L.)) geeigneten Gew~isser der DDR. Dtsch. FischereiZtg. 13: 362-372. M/2LLER-NAVARRA,D. C., BRETT, M. T., PARK, S., CHANDRA, S., BALLANTYNE,A. R, ZORITA, E. & GOLDMAN, C. R. (2004): Unsaturated fatty acid content in seston and trophodynamic coupling in lakes. Nature 427: 69-72. NEWMAN, R. M. & MARTIN,F. B. (1983): Estimation of fish production rates and associated variances. Can. J. Fish. Aquat. Sci. 40: 1729-1736. NOAKES,D. J., BEAMISH,R. J. & KENT,M. L. (2000): On the decline of Pacific salmon and speculative links to salmon farming in British Columbia. Aquaculture 183: 363-386. OGuTUOHWAYO,R., HECKY,R. E., COHEN,A. S. & KAUFMANN, L. (1997): Human impacts on the African Great Lakes. Environ. Biol. Fish. 50: 117-131. PADISAK,J., KRIENITZ,L., SCHEFFLER,W., KOSCHEL,R., KRISTIANSEN, J. & GRIGORSZKI,T. (1998): Phytoplankton succession in the oligotrophic Lake Stechlin (Germany) in 1994 and 1995. Hydrobiologia 3691370: 179-197. PADISAK, J., SCHEFFLER,W., KASPRZAK, P., KOSCHEL, R. & KRIENITZ,L. (2003): Interannual variability in the phytoplankton composition of Lake Stechlin (1994-2000). Arch. Hydrobiol., Spec. Issues Adcanc. Limnol. 58: 101-133. PAULY,D. & CHRISTENSEN,V. (1995): Primary production required to sustain global fisheries. Nature 374: 255-257. PERSSON, L., ANDERSSON,G., HAMRJN,S. F. & JOHANSSON,L. (1988): Predator regulating and primary production along productivity gradient of temperate lake ecosystems. In: S. R. CARPENTER(ed.), Complex interactions in lake communities, pp. 45-65. New York. PITCHER,T. J. & HART,P. J. B. (1982): Fisheries ecology. London. RANDALL, R. G., KELEHER,C. J. & ANDERSON,J. L. (1995): Fish production in freshwaters: Are rivers more productive than lakes? Can. J. Fish. Aquat. Sci. 52:631-643. RICE, J. & COOPER,J. A. (2003): Management of flatfish fisheries - what factors matter? Journal of Sea Research 5t}: 227-243. SARVALA,J., VENTELA,A. M., HELMINEN,H., HIRVONEN,A., SAARIKARI,g., SALONEN,S. & VUORIO, K. (1998a): Relations between planktivorous fish abundance, zooplankton and phytoplankton in three lakes of differing productivity. Hydrobiologia 363:81-95.

Pelagic trophic transfer efficiency in Lake Stechlin (Germany)

SARVALA,J., HELMINEN,H. & AUVINEN,H. (1998b): Portrait of a flourishing freshwater fishery: Pyh~jgxvi, a lake in SWFinland. Boreal Env. Res. 3: 329-345. SARVALA,J., SALONEN,K., JARVINEN,M., ARO, E., HUTTULA, T., KOTILAINEN,P., KURKI, H., LANGENBERG,V., MANNINI, P., PELTONEN,A., PLISNlgR,P.-D., VUORINEN,I., M~)LSA,H. & LINDQIST,O. V. (1999): Trophic structure of Lake Tanganyika: carbon flows in the pelagic food web. Hydrobiologia 40'7: 155-179. SCHULZ,M. & FREYHOF,J. (2003): Coregonusfontanae, a new spring-spawning cisco from Lake Stechlin, northern Germany (Salmoniformes: Coregonidae). Ichthyol. Explor. Freshwaters 14: 209-216. SCHULZ,M., MEHNER,T., KASPRZAK,P. & ANWAND,K. (2003): Diet and consumption of vendace (Coregonus albula L.) in response to seasonal zooplankton succession in Lake Stechlin. Arch. Hydrobiol., Spec. Issues Advanc. Limnol. 58: 215-226. STEEMAN-NIELSEN,E. (1952): The use of radioactive carbon (t4C) for measuring organic production in the sea. J. Cons. Int. Explor. Mer. 18: 117-140.

273

STOCKWZI,L, J. D. & JOHANNSSON,O. E. (1997): Temperaturedependent allometric models to estimate zooplankton production in temperate freshwater lakes. Can. J. Fish. Aquat. Sci. 54: 2350-2360. TANAKA,S. (2002): Fisheries management in the 2 lth century. Nippon Suisan Gakkaishi 68: 313-319. TOIVONEN,H. (1991): The fish populations and fisheries in small forest lakes in Finland. Finnish Fisheries Research 12: 19-24. WACKER,A. & VON ELERT,E. (2001): Polyunsaturated fatty acids: evidence for non substitutable biochemical resources in Daphnia galeata. Ecology 82: 2507-2520. WANZENB(3CK,J., MEHNER,T., SCHULZ,M., GASSNER,H. & WINFIELD,I. J. (2003): Quality assurance of hydroacoustic surveys: Repeatability of fish abundance and biomass estimates in lakes within and between hydroacoustic systems. ICES Journal of Marine Sciences 60: 486-492. WEILER,W., KASPRZAK,R, SCHULZ,M. & FLOBNER,D. (2003): Habitat requirements of Eurytemora lacustris (Copepoda, Calanoida) and implications for its distribution. Arch. Hydrobiol., Spec. Issues Advanc. Limnol. 58:201-214. WINBERG,G. G. (1971): Methods for the estimation of production of aquatic animals. London, New York.

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