Arch. Hydrobiol. Spec. Issues Advanc. Limnol. 53, p. 255-274, December 1998Lake Constance, Characterization of an ecosystem in transition

Crustacean zooplankton in Lake Constance from 1920to 1995: Response to eutrophication andre-ol igotrophication

Dietmar Straile and Waiter Geller

with 9 figures

Abstract: During the first three quarters of this century, the trophic state ofLake Constance changed fromoligotrophic to meso-/eutrophic conditions. The response of crustaceans to the eutrophication process isstudied by comparing biomasses of crustacean zooplankton from recent years, i.e. from 1979-1995, withdata from the early 1920s (AUERBACH et a1. 1924, 1926) and the 1950s (MUCKLE & MUCKLE­ROTTENGATTER 1976). This comparison revealed a several-fold increase in crustacean biomass. Therelative biomass increase was more pronounced from the early 1920s to the 1950s than from the 1950s tothe 1980s. Most important changes of the species inventory included the invasion of Cyclops vicinus andDaphnia galeata and the extinction of Heterocope borealis and Diaphanosoma brachyurum during the1950s and early 1960s. All species which did not become extinct increased their biomass duringeutrophication. This increase in biomass differed between species and throughout the season which re­sulted in changes in relative biomass between species. Daphnids were able to enlarge their seasonalwindow of relative dominance from 3 months during the 1920s (June to August) to 7 months during the1980s (May to November). On an annual average, this resulted in a shift from a copepod dominated lake(biomass ratio cladocerans/copepods = 0.4 during 1920/24) to a cladoceran dominated lake (biomass ratiocladocerans/copepods = 1.5 during 1979/95). The biomass of cyclopoid copepods increased stronglyduring the first half of the year owing to the invasion of Cyclops vicinus, which caused a strong relativedecline ofEudiaptomus. In contrast to the pronounced response to eutrophication, crustaceans have not yetshown an unambiguous response to the beginning re-01igotrophication of Lake Constance.

Introduction

The eutrophication of a lake ecosystem may be regarded as a large-scale ecological experi­

ment, the study of which will offer important insights into the mechanisms structuring eco­logical communities. Recent research has emphasized the importance of phenomena, such asindirect effects (STRAUSS 1991, WOOTTON 1994), species invasions and extinctions (LODGE

1993), and dynamics of resting stages (HAIRSTON et al. 1995, ADRIAN & DENEKE 1996),which act on large temporal and spatial scales and, hence, are difficult to study within labora-

Addresses of the authors: D. Straile, Limno10gical Institute, University of Konstanz, D-78457Konstanz, Germany. e-mail: Dietmar.Straile@uni-konstanz.de. - W. Geller, UFZ-Centre for Environ­mental Research, Institute for Inland Water Research, Magdeburg, D-39I04 Magdeburg, Germany.

0071-1128/98/0053-255 $ 5.00© 1998 E. Schweizerbart'sche Verlagsbuchhandlung, 0-70176 Stuttgart

256 D. Straile and W. Geller

tory and mesocosm experiments. In this respect, the analysis of the "large-scale experimenteutrophication" will complement studies on smaller temporal and spatial scales.

Crustacean zooplankton has been shown to respond to an increase in nutrient loading bothby an increase in overall abundance and biomass and by pronounced changes in the commu­nity structure including the new occurrence and loss of species (RAVERA 1980, EINSLE 1983,1988, DE BERNARDI et al. 1988, GEORGE et al. 1990, NAUWERCK 1991, POLLI & SIMONA1992, FITZSIMONS & ANDREW 1993). Based on long-term records and comparisons of lakes ofdifferent trophy, several workers suggested that rising lake trophy will favour cyclopoidcopepods over ca1anoid copepods (GLIWICZ 1969, PATALAS 1972, ROGNERUD & KJELLBERG1984, LANGELAND & REINERTSEN 1982) and cladocerans over calanoid copepods (PATALAS1972, ROGNERUD & KJELLBERG 1984).

According to pigment concentrations in the sediment, the "experiment eutrophication"started in Lake Constance at the beginning of this century (LENHARD 1994). Since 1952,eutrophication is documented by measurements of total phosphorus concentrations, which in­creased approximately 10-fold until 1979. Due to massive efforts in sewage removal, total phos­phorus concentrations declined down to 33% of the maximum values in recent years (see inletFig. 1 and GliDE et al. 1998). The response of phytoplankton to eutrophication was evidentalready in 1935 (GRIM 1955) and increases in biomass and shifts in species compositioncontinued into the 1970s (WALZ et al. 1987, KUMMERLIN 1998). The response ofphytoplanktonto re-oligotrophication is equally well documented and consist of a decline in biomass duringsummer (GAEDKE & SCHWEIZER 1993, GAEDKE 1998a), pronounced shifts in speciescomposition (SOMMER et al. 1993, KUMMERLIN 1998), and a modest decrease in primaryproductivity only during the most recent years (HAESE et al. 1998).

The first descriptions of zooplankton in Lake Constance date back to the middle of the lastcentury (LEYDIG 1860, WEISMANN 1876). Following the pioneering work of RENSEN (1884)in the ocean, ROFER started in 1892 to study quantitatively horizontal and vertical distributionsof various zooplankton species in Lake Constance (ROFER 1896). His work was followed byAUERBACH et al. (1924, 1926) during 1919-1924 and ELSTER during 1932-1935 (ELSTER1936, 1954, ELSTER & SCHWOERBEL 1970). Recognizing the signs of eutrophication, a moni­toring program was initiated by the Institut fUr Seenforschung at Langenargen in 1952 whichhas continued until now (KIEFER & MUCKLE 1959, MUCKLE & MUCKLE-ROTTENGATTER1976, EINSLE 1977, 1983, 1987, 1988). These studies were accompanied by investigations ofthe Limnological Institute at Konstanz since the 1970s (LAMPERT & SCHOBER 1978, GELLER1985, 1989). A combination of these studies yields a long-term time series of outstandingquantity and quality which covers the period of a dramatic increase of nutrient loadings duringthe first three quarters of this century, but also includes the years of a beginning re-oligotrophi­cation. To analyse the zooplankton response to increased nutrient loadings, the present studycompares long-term averages of zooplankton biomass from three periods, i.e., 1920-1924(AUERBACH et al. 1924, 1926), 1952-1962 (KIEFER & MUCKLE 1959, MUCKLE & MUCKLE­ROTTENGATTER 1976), and 1979-1995, on a seasonal basis (Fig. 1). Subsequently, theresponse to decreasing nutrient loadings will be analysed within the years 1979-1995.

Methods

From 1979 to 1995, zoop1ankton was collected weekly (biweekly during the winter months, nodata for 1983) with a Clarke-Bumpus sampler (mesh-size 140 1Jll1) by vertical hauls from 140 m

Crustacean zooplankton 257

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60 ~3

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JFMAMJJASOND

1920-1924

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1952-1962

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1979-1995

Fig. 1. Average monthly crustacean biomass during the three periods of investigation (1920-1924,1952-1962, and 1979-1995). Inlet shows the development of total phosphorus concentrations duringwinter mixis (TPMIX) indicating the trophic state of the lake (no consecutive measurements prior to 1951).Data on TPMIX were provided by the International Commission for the Protection of Lake Constance(IGKB 1997).

depth at the sampling station of the Limnological Institute at the central part of the UberlingerSee, a fjord-like branch of Upper Lake Constance. During routine measurements, seven taxawere identified: Daphnia hyalina, Daphnia galeata, Bosmina sp., Eudiaptomus gracilis,cyclopoid copepods, Leptodora kindtii, and Bythotrephes longimanus. The individual taxa wereseparated into up to 5 size classes. Biomass was calculated from length-dry weight relationshipsestablished for Lake Constance (GELLER & MULLER 1985, WOLFL 1991). Data from previousyears were taken from MUCKLE & MUCKLE-ROTTENGATTER (1976) who give monthly meanabundances for 1920-24 (their Table 1, originally published in AUERBACH et al. 1924, 1926) andfor 1952-62 (their Tables 3-15). During 1952/62, up to 6 stations within the Uberlinger See weresampled (MUCKLE & MUCKLE-ROTTENGATTER 1976) with a Nansen closing net with meshsizes of 130 and 200 !lID. AUERBACH et al. (1924,26) used a Nansen closing net with mesh sizesof 50 !lID and sampled at the Uberlinger See, but also in the main basin ofUpper Lake Constance(Obersee). The taxonomic resolution used in 1920124 and 1979/95 is identical. The biomass ofthree cyclopoid copepods species (Cyclops abyssorum, Mesocyclops leuckartii, and Cyclopsvicinus) distinguished during 1952/62 (MUCKLE & MUCKLE-ROTTENGATTER 1976) wasaggregated for the present study. The biomasses ofDiaphanosoma brachyurum and Heterocopeborealis, which disappeared in later years, were calculated by assuming carbon weights of 2.5/-4SC ind- I for Diaphanosoma and 2.7, 5,13, 19/-4SC ind- I for Heterocope in April, May, June, andJuly-December, respectively (ELSTER 1936). The biomasses of othertaxa in 1920124 and 1952/62 were calculated from abundances and species-specific average carbon weights obtained in1979/95 assuming that average carbon weights have not changed between the study periods.

258 D. Straile and W. Geller

This will overestimate biomass during the more oligotrophic periods if the average body size ofindividuals and consequently their biomass has increased during eutrophication. However, theuncertainty involved in the calculation of biomasses is probably small compared to theuncertainties regarding the differences in sampling gear between the study periods.

To overcome the problem just mentioned, we will focus not on absolute numbers, but ana­lyse the relative response patterns of species. These comparisons are less sensitive to potentialdifferences in the overall sampling efficiency between the study periods. As a comparativetool, we calculate factors of biomass increase (FBI) between the study periods both on anannual average and for different months. The FBI is calculated as the ratio between thebiomass in the later period and the respective biomass during the former one.

Results

Eutrophication

The first study of zooplankton population dynamics in Lake Constance spanning several yearswas carried out by AUERBACH during 1920 to 1924 and yielded a zooplankton communitytypical, both in abundance and species composition, of oligotrophic lakes (AUERBACH et a1.1924, 1926). Since 1920/24, the biomass of crustacean zooplankton has increased drastically(Fig. 1) and changes in the species inventory have occurred. Most notable newcomers wereCyclops vicinus and Daphnia galeata, which were found for the first time in plankton nets in1954 and in 1956, respectively (EINSLE 1983). The last records of Diaphanosoma brachyurumand Heterocope borealis were made in 1958 and 1963, respectively. The genus Bosmina(Eubosmina) was represented by Bosmina longispina (= B. coregoni (MULLER 1985» in Up­per Lake Constance during its oligotrophic period (HOFMANN 1998). Already during the early1940s, a new Bosmina taxon, B. longicomis kessleri, successfully invaded the lake (HOFMANN1998). Another species, Bosmina longirostris, was found in the pelagic realm sporadicallysince the 1950s. Its biomass reached the same magnitude as Bosmina longispina from 1980­1982 onwards (MULLER 1985).

The relative biomass increase of crustaceans was larger during the first period ofeutrophication, i.e. from 1920/24 to 1952/62, than during the second period, i.e. from 1952/62to 1979/95, and not evenly distributed across the different species and taxa (Fig. 2). Thebiomass of carnivorous cladocerans (Leptodora kindtii and Bythotrephes longimanus) anddaphnids increased considerably more than the biomass of copepods and small cladocerans.Excluding Daphnia galeata, differences in FBI between taxa were larger from the 1920s to the1950s than from the 1950s to the 1980s, i.e., biomass increase was more evenly distributedacross the taxa from the 1950s to the 1980s than from the 1920s to the 1950s.

FBI of herbivorous cladocerans is determined to a large extent by daphnids which increasedconsiderably more than Bosmina sp. and Diaphanosoma. The high FBI of Daphnia galeatafrom 1952/62 to 1979/95 was due to the small average biomass of Daphnia galeata during1952/62. Therefore, FBI of total daphnid biomass was not much enhanced compared to theFBI of Daphnia hyalina. Likewise, there is a notably large FBI of carnivorous cladocerans,i.e., Leptodora kindtii and Bythotrephes longimanus, during both time periods.

The differences in FBI between individual taxa resulted in pronounced shifts in crustaceanbiomass composition (Fig. 3). Relative biomasses of daphnids, cyclopoid copepods, and car­nivorous c1adocerans increased on an annual average during eutrophication, whereas the reia-

Crustacean zooplankton 259

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Fig. 2. Factor of biomass increase(FBI) from 1920/24 to 1952/62(upper panel), from 1952/62 to1979/95 (intermediate panel), andfor the overall study period (1920/24-1979/95, lower panel). Thefollowing taxa are analysed sepa­rately: Daphnia hyalina (Dh),Daphnia galeata (Dg), Bosminasp. (Bos), Diaphanosoma brach­yurum (Db), Eudiaptomus graci­lis (Eu), Heterocope borealis(Hb), cyclopoid copepods (Cyc),Leptodora kindtii (Lk), Bytho­trephes longimanus (BI), daphnids(Da = Dh + Dg), carnivorouscladocerans (cCl = Lk + Bl),herbivorous cladocerans (hCl =Da + Bos + Db), copepods (Cop =Eu + Cyc), and total crustaceans(Cr.

tive biomass of Eudiaptomus, Heterocope, Bosmina, and Diaphanosoma decreased. This re­sulted in an increase of the biomass ratio between cladocerans and copepods from 0.4 in1920124 to 0.9 in 1952/62 and to 1.5 in 1979/95, i.e., copepods were dominant in 1920124,cladocerans in 1979/95, and both taxa had roughly similar biomasses on an annual average in1952/62.

During the first period of eutrophication (1920124-1952/62), FBI of total crustaceanzooplankton showed a pronounced peak from May to July, whereas during the second period(1952/62-1979/95) they were more evenly distributed across the months with minor peaksduring early spring and late summer (Fig. 4a). The major biomass increase during the first

260 D. Slraile and W. Geller

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period in May. June. and July could be attributed to herbinll'Ous dadocerans (Fig.4b).cydopoid copcpods (Fig. 4d) as "ell as £lIdiaplOmus (Fig. 4c) with FBI's of approximately47. 30. and 20. respectively. during these three months. During late summer and autumn(August-November). FBI's of herbivorous c1adocerans. Elldiapwmlfs. and cyclopoid cope­pods were lower and more similar (11, 10. and 8. respectively).

The bimodal increase pattem of total crustacean biolllass during the second period (Fig. 4a)can be explained by the increase of dadocerans and cyclopoid copepods. Herbivorousc1adoceran~ and cyclopoid copepods contributcrl to the first peak during early spring (Fig. 4b.4d). 1lle second peak during autumn can be attributed to the high FBI of herbivorous andcarnivorous cladoceroms. Elldiaptomlls biomass approximately doubled from 1952162 to1979195. but its increase sho"ed no se3SQnal pattern (Fig. ok). Thus. from the 19505 to the1980s. differences in FBI between herbivorous c1adocerans and copepods were larger duringhigh summer and autumn than during spring. Carnivorous c1adocerans multiplied theirbiomass during the second half of the year by factors up to 30 and 10 during the first andsecond time period. respectively (Fig. 4e).

As a result of differing increase patterns of taxa and changes in species inventory. the se:l­sona] course of Ihe contributions of different species 10 lotal crustacean biomass changed dur­ing the eutrophication process (Fig. 5). The contribution of £lIdiopI01mls gracilis to the totalcrustacean biomass from January to April diminished from values up to 70% in the early 19205to values of 50% during the 19505 and finally to about 20% during 1979 to 1995. The relativedecline of EudiaplOmlls gracilis was accompanied by a relative increase of cyclopoidcopepods from about 20%- in 1920-1924 to 60-70% in 1979-1995.

Daphnids raised their share ofbiomass from approximately 40% during July-August in the19205 to 40-50% from May-September in the 19505 and to 40-60% from May-November inrecent years. That is. daphnids enhanced their contribution during summer approximately

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262 D. Straile and W. Geller

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Crustacean zooplankton 263

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from 40 to 60%, but more importantly, they enlarged their window of seasonal dominancefrom three months during 1920/24 to 5 months during 1952/62 up to 7 months during 1979/95.The time of maximum contribution of Daphnia hyalina shifted from July during 1920124 toOctober during 1979/95.

264 D. Straile and W. Geller

Changes in relative biomass between Eudiaptomus and cyclopoid copepods duringeutrophication were pronounced within the first half of the year and less obvious from July toDecember (Fig. 6a). Comparing herbivorous cladocerans and Eudiaptomus, the time of pro­nounced change in relative biomass was confined to late summer and autumn (Fig. 6b). A thirdpattern of changes in biomass distribution emerged within herbivorous cladocerans (Fig. 6c).Relative biomasses of daphnids increased at the expense of smaller cladocerans especially inwinter, early spring, and in late summer/autumn (Fig. 6c). Thus, changes in relative biomasswere more pronounced within copepods (Fig. 6a) and herbivorous cladocerans (Fig. 6c) thanbetween herbivorous cladocerans and Eudiaptomus (Fig. 6b).

Re-oligotrophication

In order to identify the long-term effect of eutrophication throughout this century, crustaceanbiomass and species composition during the years 1979-1995 have been considered as rela­tively homogenous, and average conditions prevailing during this time were contrasted againstthe previous observations during the 1920s and 1950s. Given the large differences in trophicstate between these three periods, e.g., mean and median of TPMIX from 1952/62 and 1979/95differ by approximately a factor of five, this approach appears justified. However, the periodfrom 1979 to 1994 covers a decrease in TPM1X by almost a factor of four and thus may enable ananalysis of potential effects of re-oligotrophication.

Except for Bosmina and Eudiaptomus, biomass of crustacean species showed no trendfrom 1979-1995 (Figs. 7, 8). Daphnia hyalina reached highest biomasses with up to10 gC/m2 during the second half of the observation period, i.e. from 1987 to 1995 (Fig. 7).In most years, abundance peaks of Daphnia hyalina in late summer and autumn surpassedthe abundance peaks during the spring development. In contrast, maxima in biomass ofDaphnia galeata occurred during late spring. Average biomasses of daphnids were notrelated to winterly total phosphorus values (Fig. 8). However, the temporal window ofDaphnia galeata during the season is shrinking (Fig. 9). Daphnia galeata occurred later inspring and disappeared earlier in autumn during the 1990s than during the 1980s. The timespan between its first and last occurrence in zooplankton samples in the different years waspositively related to TPMIX (r2 = 0.3, p < 0.05). This relationship is statistically significantdespite the small time spans of occurrence at high phosphorus concentrations during 1979,1980, and 1982. During these years, sampling started not before March or April, whichresulted in a small observation window and probably in an underestimation of theoccurrence window of D. galeata (Fig. 9).

Maximum biomass of Bosmina declined from values around 1 gC/m2 during the 1980s toless than 0.1 gC/m2 from 1991 to 1994. However, in 1995, peak biomasses of Bosminaexceeded 0.5 gC/m2 (Fig. 7). The relationship between yearly averages of Bosmina biomassand TPMIX is highly significant (r =0.83, P < 0.0001) despite the higher biomasses in 1995.Average Bosmina biomass has declined to approximately 10% compared to the early 1980s(Fig. 8). Maximum biomass of Eudiaptomus gracilis declined from 1979 to 1982 and from1984 to 1991, but was high from 1992 onwards (Fig. 7). Despite these large oscillations, theannual averages of Eudiaptomus biomass were positively related to TPMIX (r = 0.53,P < 0.05, Fig. 8). Neither Cyclops vicinus nor the carnivorous cladocerans Leptodora andBythotrephes showed a notable trend in population dynamics within the years 1979-1995(Figs. 7, 8).

Crustacean zooplankton 265

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Discussion

Eutrophication

This study compares the averages of three long-term time series of crustacean plankton in LakeConstance. The concentration on long-term averages reduces the impact of factors acting onsmaller time scales, e.g., interannual variability of weather patterns (GAEDKE et al. 1998) andfish predation (ECKMANN & RbsCH 1998), which cause considerable variability in crustaceanbiomass and might blur the effects of eutrophication.

266 D. Straile and W. Geller

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100 80 60 40 20 10080 60 40 20 100 80 60 40 20

TPMIX [1..19 /1 ] TPMIX [1..19 /1 ] TPMIX [1..19 /1 ]

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10080 60 40 20

TPMIX [1..19/1]

Fig. 8. Averageannual biomass ofcrustacean taxa vs.TPMIX' Each dotrepresents one studyyear and r is Pearson'scorrelation coeffi­cient. Note that thescale on the x-axisfollows the temporaldevelopment and isreversed.

Additionally, comparing long-term averages reduces the potential effects of spatial hetero­geneity and patchiness. Numbers and places of sampling stations differ between the threesampling periods compared in this study, e.g., only one station situated at the Uberlinger See issampled with high frequency from 1979 to 1995 compared to several other stations at theUberlinger See and at the central part of Upper Lake Constance during 1920-1924. Severalauthors found large horizontal heterogeneity in crustacean abundances in Lake Constance atindividual sampling dates, but - with the possible exception of higher abundances in the Bayof Bregenz at the eastern end of the lake - no persistent, large-scale spatial patterns wereidentified (BAYERSDORFER 1924, ELSTER & SCHWOERBEL 1970, EINSLE 1990, ApPENZELLERthis volume). Thus, the comparison of long-term averages should not be hampered by spatialheterogeneity of crustaceans in Lake Constance.

The comparison of the three time series is, however, hampered by differences in samplinggear. Absolute and relative increases in biomass of crustaceans between the three study periodscan only be interpreted cautiously. Nevertheless, the approximately 50-fold biomass increaseof crustaceans from the 1920s to the 1980s fits well with data from phytoplankton and rotifers.Phytoplankton biomass increased between one and two orders of magnitude based on micro­scopic countings (KUMMERLIN 1998) and pigment concentrations in sediments (LENHARD1994). Rotifer biomass increase during eutrophication was estimated to amount also to twoorders of magnitude (WALZ et al. 1987).

Crustacean zooplankton 267

360000

00

0 85_0

320 0 00

81- 0 86- - 0(j) 280 84 -87>.co 0~ 0

240 -Fig. 9. Time ofc 80 - -95span CO 90

seasonal occurance of a. 79- -94enDaphnia galeata vs. - -Q)

200 82 89 -TPMIX' Each full dot repre- E 91sents onc study year. :;=;

Circles represent the time •span of sampling within 160 88

the respective years, i.e.,• 93the maximum range of •

Daphnia galeata occurren- 120 92ce which could be obser-ved. During two years 100 80 60 40 20(1984 and 1985) occur-rance and observationwindows were similar. TPMI x [j.Jg/l]

The most pronounced relative increase in crustacean biomass occurred from the early1920s to the 1950s. This is supported by the pattern of sediment pigment concentrations,which from the early 1920s to the 1950s increased approximately three times more than fromthe 1950s to the 1980s (LENHARD 1994 and pers. comm.). That is, although the absolute in­crease in nutrient concentrations was largest after World War II (GliDE et al. 1998), biomass ofphytoplankton and crustaceans indicate a strong relative increase in nutrient concentrationsalready before the 1950s.

The overall changes in community structure of crustacean zooplankton confirm with find­ings from other studies. Cladocerans and cyclopoid copepods increased more strongly thancalanoid copepods during eutrophication, which is in accordance with concepts and observa­tions by GLIWICZ (1969), PATALAS (1972), ROGNERUD & KJELLBERG (1984), and Muck &LAMPERT (1984). Similar shifts in community structure were observed during the course ofeutrophication, for example, in Lago Lugano (POLLI & SIMONA 1992), Lake Mondsee(NAUWERCK 1991), Lough Neagh (FITZSIMONS & ANDREW 1993), and Esthwaite Water(GEORGE et al. 1990). The response of calanoid copepods was most pronounced in LagoLugano, where calanoid copepods disappeared completely for almost 30 years from thepelagic zone and reappeared in the course of re-oligotrophication (POLLI & SIMONA 1992).

The mechanisms behind these changes in species composition are, however, not fully un­derstood. For example, it is difficult to separate the direct effect of eutrophication on the spe­cies composition from the impact of newly invading species (EINSLE 1983).

The first important changes in species inventory, the invasion of Cyclops vicinus andDaphnia galeata, took place during the early 1950s, almost 50 years (!) after the first signs ofincreasing pigment concentrations in the sediment due to eutrophication (LENHARD 1994) and

268 D. Straile and W. Geller

after a pronounced increase in overall crustacean biomass! During one decade, from 1954 to1963, all major changes in species inventory of crustaceans occurred. This comparativelysmall time span suggests that these changes are not independent of each other. Besides in­creased food concentrations due to eutrophication, a severe reduction of fish stocks due tooverfishing during the early 1950s (HARTMANN 1987, ECKMANN & ROSCH 1998) might havefacilitated the establishment of the new species. However, the occurrence of new speciesprobably altered the "ecological theatre" and brought new ecological interactions. Further­more, these new interactions are intertwined with changes in ecological interactions of"native" species due to increased nutrient concentrations.

The invasion of Cyclops vicinus seems to have had the most far-reaching consequencesfor the zooplankton community structure in Lake Constance (EINSLE 1983). Studies byEINSLE (1977, 1983) and WOLFL (1991) revealed that cyclopoid copepod biomass isdominated by Cyclops vicinus during the first five months of the year. During this time, therelative importance of cyclopoid copepods and Eudiaptomus reversed during the course ofeutrophication. Tn early June, a diapause migration of Cyclops vicinus copepodites causes anabrupt decline of cyclopoid copepod planktonic biomass with Cyclops abyssorum andMesocyclops leuckartii as the dominating cyclopoid copepod species (EINSLE 1967, WOLFL1991). From July onwards, the biomass ratio between Eudiaptomus and cyclopoid copepodshas hardly changed from the 1920s to recent years. That is, Eudiaptomus and the "native"cyclopoid copepods showed a roughly similar response to eutrophication during the secondhalf of the year.

Low food concentrations might have prevented the establishment of a large population ofcyclopoid copepods in oligotrophic Lake Constance. Threshold food concentrations of Cyclopsvicinus juveniles are considerably larger than the threshold food concentrations ofEudiaptomusresulting in slow growth, poor survival, and lower competitive ability ofjuvenile cyclopoids atlow food concentrations (SANTER 1994). In contrast, juvenile cyclopoids might be superior tocalanoid juveniles at higher food concentrations (SANTER & VAN DEN BOSCH 1994), whichwould enable them to exploit more efficiently increasing food concentrations due toeutrophication. Predation by older cyclopoid copepodites on calanoid juveniles (EINSLE 1978,KAWABATA 1991, SANTER & VAN DEN BOSCH 1994) might additionally have contributed to thechanges in relative biomass between Eudiaptomus and cyclopoid copepods duringeutrophication in Lake Constance. However, it should be kept in mind that Eudiaptomus did notdecline in the course ofeutrophication, but rather was less successful than cyclopoid copepods toexploit the increasing food concentrations. The biomass ratios between Eudiaptomus andDaphnia changed with the exception of autumn and early winter only marginally. Hence, thestrong relative decline of Eudiaptomus on an annual average is largely attributable to theinvasion of Cyclops vicinus rather than to competitive interactions with daphnids.

Predation by Cyclops vicinus on the nauplii and small copepodites of Heterocope borealisis thought to be responsible for the decline and disappearance of this large predatory calanoidcopepod in Lake Constance (KrEFER 1973, EINSLE 1983). Heterocope became extinct in anumber of large perialpine lakes (KIEFER 1973). However, this disappearance was notassociated with an increase of cyclopoid copepods, especially Cyclops vicinus, in all lakes. InLago Maggiore, Heterocope disappeared without the invasion of Cyclops vicinus and despite adecrease in the abundance of cyclopoid copepods (DE BERNARDI et al. 1988, 1989), whichsuggests that additional factors influenced the decline of Heterocope in European perialpinelakes. Nevertheless, for Lake Constance, it is likely that at least Cyclops vicinus contributed to

Crustacean zooplankton 269

the extinction of Heterocope (KIEFER 1973, EINSLE 1983), which demonstrates the impor­tance of species interactions in shaping the response of crustaceans to eutrophication.

Daphnia galeata may be considered the second important new zooplankton species in LakeConstance. Daphnia galeata differs from the "native" Daphnia hyalina by higher egg ratiosand growth rates under favourable food conditions (GELLER 1989), but poorer growth whenfood is scarce (STICH & LAMPERT 1984). Consequently, the contribution of Daphnia galeatato crustacean biomass during the 1980s was largest during and shortly after the phytoplanktonspring bloom, whereas Daphnia hyalina reached its highest contributions during late summerand autumn. Higher growth rates of Daphnia galeata might also contribute to the earlier popu­lation development of daphnids during the 1950s and 1980s relatively to the 1920s.

The earlier seasonal development of Daphnia during the 1950s and 1980s compared to the1920s does not support the hypothesis that population development of daphnids in spring isdelayed due to predation by Cyclops vicinus (LAMPERT 1978), which should result - otherthings equal- in an opposite pattern. Adults and late copepodites of Cyclops vicinus have beenobserved to prey on nauplii and small copepodites, but rarely on daphnids in Lake Constance(EINSLE 1978). From 1979 to 1995, no close relationship between the beginning of thediapause of Cyclops vicinus and the timing of the daphnid population increase in spring hasbeen observed (unpublished results). In contrast, the timing of the daphnid population growthis largely controlled by the rise of water temperatures due to vernal warming (GAEDKE et al.1998). This further suggests, that the impact of Cyclops vicinus predation on daphnidpopulation development may have been overestimated.

Increased food concentrations allowed Daphnia hyalina to maintain high population densi­ties until late autumn at the expense of smaller-sized cladocerans. Small cladocerans are fa­voured by low food concentrations (ORCUTT & PORTER 1985) and often follow larger-sizedcladocerans in seasonal succession (DEMOTT 1989), presumably due to higher growth ratesand enhanced starvation resistance of juveniles at low food concentrations (ROMANOVSKI1985, ROMANOVSKI & FENIOVA 1985, TESSIER & GOULDEN 1987). With augmenting foodconcentrations due to eutrophication, Daphnia juveniles are able to compete successfully withjuveniles of smaller cladocerans and prevent a juvenile bottleneck in Daphnia high summerpopulation dynamics (DEMoTT 1989). The increasing success of Daphnia hyalina in summerdoes, however, not explain the disappearance of Diaphanosoma brachyurum, which is a regu­lar component of many mesotrophic and eutrophic lakes (DEMoTT & KERFOOT 1982). Theseasonal development of Diaphanosoma overlapped greatly with the occurrence of carnivo­rous cladocerans, the biomass of which increased strongly during eutrophication. Further­more, the vertical distribution of Diaphanosoma and Leptodora was identical (MUCKLE 1972)and Leptodora is known to prey heavily on Diaphanosoma in other lakes (HERZIG 1994, 1995,MANCA & COMOLI 1995). Enhanced predation pressure by carnivorous cladocerans due to theoverall increase of potential prey might be responsible for the collapse of the Diaphanosomapopulation, which was less able to exploit the increasing food supply. This suggests that thedisappearance of Diaphanosoma was due to apparent competition (HOLT 1977) rather thanexploitative competition.

To summarize, biomass of crustaceans increased by a factor of about 50 in the course ofeutrophication. The loss and new appearance of major crustacean species were confined to therather small time span from the late 1950s to the early 1960s and presumably had strongimpacts on the populations dynamics of "native" crustaceans and their response to eutro­phication. The most pronounced changes in biomass composition were the relative increases

270 D. Straile and W. Geller

in cyclopoid copepod biomass during the first half of the year and in daphnid biomass duringsummer and autumn. The increase of both cyclopoid copepods and Daphnia can probably beattributed to an augmenting survival of juvenile stages, i.e., the overcoming of juvenilebottlenecks, of cyclopoid copepods and daphnids during eutrophication.

Re-oligotrophication

TPMIX declined from 1979 to 1995 from more than 80 to 24 /-lg/l and thus approaches in recentyears values obtained during the early sixties. In contrast to the distinct response of thephytoplankton community to re-oligotrophication (GAEDKE & SCHWEIZER 1993, GAEDKE1998a), only slight - if any - responses of the crustacean zooplankton community areapparent. The decrease of phytoplankton biomass in summer was largely due to the declines oflarge and hardly edible phytoplankton species (GAEDKE 1998a). Summer biomass of small,edible, and fastest growing phytoplankton species was remarkably constant during 1979 to1996 and the decrease of primary productivity was small (HAESE et al. 1998). This mayindicate that the nutritional basis of herbivorous zooplankton changed less than it is inferredfrom total phytoplankton biomass and TPMIX' The lacking response of primary consumers isadditionally supported by long-term data of rotifer biomass in Lake Constance which revealalso hardly any trends related to re-oligotrophication (unpublished results). For a detailedcomparison of the response respectively non-response of pelagic taxa to re-oligotrophicationsee GAEDKE (l998b).

The decline of the seasonal window of Daphnia galeata fits into the hypothesis that theresponse of crustaceans to re-oligotrophication mirrors the responses to eutrophication.Daphnids increased from the 1950s to the 1980s most strongly in early spring and autumn, i.e.,at the margins of their seasonal dominance. A reversal of this development would include theobserved decline of the seasonal window of D. galeata. However, other trends observed duringthe 1980/90s are opposite to expectations derived from the simple hypothesis that zooplanktonresponse to re-oligotrophication would reverse changes during eutrophication. Both Bosminaand especially Eudiaptomus declined in terms of relative biomass during the course ofeutrophication. The low threshold food concentration of Eudiaptomus (MUCK & LAMPERT1984, SANTER 1994) should make this species the least one vulnerable to decreasing foodconcentrations. This suggests that during 1979-1995, factors other than lake trophy, such asvariability in weather patterns and fish predation (GAEDKE et al. 1998, STRAILE & GELLER1998), determined fluctuations in crustacean biomass and possibly outweighed the effects ofdecreased nutrient concentrations. A subsequent analysis should consider the combinedeffects of lake trophy, weather patterns, and variability in fish predation on the populationdynamics of crustacean zooplankton in Lake Constance.

Acknowledgements

This study was performed within the Special Collaborative Program (SFB) "Cycling of matter in LakeConstance" supported by the Deutsche Forschungsgemeinschaft (DFG). Data analysis was additionallyfunded by the European Union Environment and Climate project REFLECT ('Response of EuropeanFreshwater Lakes to Environmental and Climatic Change'). We thank G. Richter and G. Schulze whocounted most of the samples. Comments by R. Adrian, U. Gaedke, H. Glide, K.-O. Rothhaupt, and twoanonymous reviewers improved the style and content of the manuscript.

Crustacean zooplankton 271

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