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

Crustacean zooplankton in Lake Constance from 1920 to 1995: Response to eutrophication and re-oligotrophication

Dietmar Straile and Waiter Geller with 9 figures

Abstract: During the first three quarters ofthis century, the trophic state ofLake Constance changed from oligotrophic to meso-/eutrophic conditions. The response ofcrustaceans to the eutrophication process is studied by comparing biomasses ofcrustacean zooplankton from recent years, i.e. from 1979-1995, with data from the early 1920s (AUERBACH et a1. 1924, 1926) and the 1950s (MUCKLE & MUCKLE­ ROTTENGATTER 1976). This comparison revealed a several-fold increase in crustacean biomass. The relative biomass increase was more pronounced from the early 1920s to the 1950s than from the 1950s to the 1980s. Most important changes ofthe species inventory included the invasion of Cyclops vicinus and Daphnia galeata and the extinction of Heterocope borealis and Diaphanosoma brachyurum during the 1950s and early 1960s. All species which did not become extinct increased their biomass during eutrophication. This increase in biomass differed between species and throughout the season which re­ sulted in changes in relative biomass between species. Daphnids were able to enlarge their seasonal window ofrelative dominance from 3 months during the 1920s (June to August) to 7 months during the 1980s (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 ratio cladocerans/copepods = 1.5 during 1979/95). The biomass of cyclopoid copepods increased strongly during the first half of the year owing to the invasion of Cyclops vicinus, which caused a strong relative decline ofEudiaptomus. In contrast to the pronounced response to eutrophication, crustaceans have not yet shown an unambiguous response to the beginning re-01igotrophication ofLake 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 eco­ logical communities. Recent research has emphasized the importance of phenomena, such as indirect 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-78457 Konstanz, Germany. e-mail: [email protected]. - W. Geller, UFZ-Centre for Environ­ mental 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 experiment eutrophication" will complement studies on smaller temporal and spatial scales. Crustacean zooplankton has been shown to respond to an increase in nutrient loading both by an increase in overall abundance and biomass and by pronounced changes in the commu­ nity 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 & SIMONA 1992, FITZSIMONS & ANDREW 1993). Based on long-term records and comparisons oflakes of different trophy, several workers suggested that rising lake trophy will favour cyclopoid copepods over ca1anoid copepods (GLIWICZ 1969, PATALAS 1972, ROGNERUD & KJELLBERG 1984, LANGELAND & REINERTSEN 1982) and cladocerans over calanoid copepods (PATALAS 1972, 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 in­ creased approximately 10-fold until 1979. Due to massive efforts in sewage removal, total phos­ phorus concentrations declined down to 33% of the maximum values in recent years (see inlet Fig. 1 and GliDE et al. 1998). The response of phytoplankton to eutrophication was evident already in 1935 (GRIM 1955) and increases in biomass and shifts in species composition continued into the 1970s (WALZ et al. 1987, KUMMERLIN 1998). Theresponse ofphytoplankton to re-oligotrophication is equally well documented and consist of a decline in biomass during summer (GAEDKE & SCHWEIZER 1993, GAEDKE 1998a), pronounced shifts in species composition (SOMMER et al. 1993, KUMMERLIN 1998), and a modest decrease in primary productivity 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 last century (LEYDIG 1860, WEISMANN 1876). Following the pioneering work of RENSEN (1884) in the ocean, ROFER started in 1892 to study quantitatively horizontal and vertical distributions of various zooplankton species in Lake Constance (ROFER 1896). His work was followed by AUERBACH et al. (1924, 1926) during 1919-1924 and ELSTER during 1932-1935 (ELSTER 1936, 1954, ELSTER & SCHWOERBEL 1970). Recognizing the signs ofeutrophication, a moni­ toring program was initiated by the Institut fUr Seenforschung at Langenargen in 1952 which has continued until now (KIEFER & MUCKLE 1959, MUCKLE & MUCKLE-ROTTENGATTER 1976, EINSLE 1977, 1983, 1987, 1988). These studies were accompanied by investigations of the Limnological Institute at Konstanz since the 1970s (LAMPERT & SCHOBER 1978, GELLER 1985, 1989). A combination of these studies yields a long-term time series of outstanding quantity and quality which covers the period of a dramatic increase ofnutrient loadings during the first three quarters ofthis century, but also includes the years of a beginning re-oligotrophi­ cation. To analyse the zooplankton response to increased nutrient loadings, the present study compares long-term averages of zooplankton biomass from three periods, i.e., 1920-1924 (AUERBACH et al. 1924, 1926), 1952-1962 (KIEFER & MUCKLE 1959, MUCKLE & MUCKLE­ ROTTENGATTER 1976), and 1979-1995, on a seasonal basis (Fig. 1). Subsequently, the response 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, no data for 1983) with a Clarke-Bumpus sampler (mesh-size 140 1Jll1) by vertical hauls from 140 m Crustacean zooplankton 257

4 100

80

60 ~ 3 3 40 , a. NE f- U 20 ~ o en 2 en 2000 ro E :.c0

JFMAMJJASOND JFMAMJJASOND JFMAMJJASOND 1920-1924 1952-1962 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 during winter 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 Uberlinger See, a fjord-like branch of Upper Lake Constance. During routine measurements, seven taxa were identified: Daphnia hyalina, Daphnia galeata, Bosmina sp., Eudiaptomus gracilis, cyclopoidcopepods, Leptodora kindtii, and Bythotrephes longimanus. The individual taxa were separated into up to 5 size classes. Biomass was calculated from length-dry weight relationships established for Lake Constance (GELLER & MULLER 1985, WOLFL 1991). Data from previous years were taken from MUCKLE & MUCKLE-ROTTENGATTER (1976) who give monthly mean abundances for 1920-24 (theirTable 1, originally published in AUERBACH et al. 1924, 1926) and for 1952-62 (their Tables 3-15). During 1952/62, up to 6 stations within the Uberlinger See were sampled (MUCKLE & MUCKLE-ROTTENGATTER 1976) with a Nansen closing net with mesh sizes of 130 and 200 !lID. AUERBACH et al. (1924,26) used a Nansen closing net with mesh sizes of50 !lID and sampled at the Uberlinger See, but also in the main basin ofUpperLake Constance (Obersee). The taxonomic resolution used in 1920124 and 1979/95 is identical. The biomass of three cyclopoid copepods species (Cyclops abyssorum, Mesocyclops leuckartii, and Cyclops vicinus) distinguished during 1952/62 (MUCKLE & MUCKLE-ROTTENGATTER 1976) was aggregated for the present study. The biomasses ofDiaphanosoma brachyurum andHeterocope borealis, 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 inApril, May, June, and July-December, respectively (ELSTER 1936). The biomasses ofothertaxa in 1920124 and 1952/ 62 were calculated from abundances and species-specific average carbon weights obtained in 1979/95 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 ifthe average body size of individuals and consequently their biomass has increased during eutrophication. However, the uncertainty involved in the calculation of biomasses is probably small compared to the uncertainties regarding the differences in sampling gear between the study periods. To overcome the problem just mentioned, we will focus not on absolute numbers, but ana­ lyse the relative response patterns of species. These comparisons are less sensitive to potential differences in the overall sampling efficiency between the study periods. As a comparative tool, we calculate factors of biomass increase (FBI) between the study periods both on an annual average and for different months. The FBI is calculated as the ratio between the biomass in the later period and the respective biomass during the former one.

Results

Eutrophication The first study ofzooplankton population dynamics in Lake Constance spanning several years was carried out by AUERBACH during 1920 to 1924 and yielded a zooplankton community typical, 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 were Cyclops vicinus and Daphnia galeata, which were found for the first time in plankton nets in 1954 and in 1956, respectively (EINSLE 1983). The last records ofDiaphanosoma brachyurum and Heterocope borealis were made in 1958 and 1963, respectively. The genus Bosmina (Eubosmina) was represented by Bosmina longispina (= B. coregoni (MULLER 1985» in Up­ per Lake Constance during its oligotrophic period (HOFMANN 1998). Already during the early 1940s, a new Bosmina taxon, B. longicomis kessleri, successfully invaded the lake (HOFMANN 1998). Another species, Bosmina longirostris, was found in the pelagic realm sporadically since the 1950s. Its biomass reached the same magnitude as Bosmina longispina from 1980­ 1982 onwards (MULLER 1985). The relative biomass increase of crustaceans was larger during the first period of eutrophication, i.e. from 1920/24 to 1952/62, than during the second period, i.e. from 1952/62 to 1979/95, and not evenly distributed across the different species and taxa (Fig. 2). The biomass of carnivorous cladocerans (Leptodora kindtii and Bythotrephes longimanus) and daphnids 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 the 1950s than from the 1950s to the 1980s, i.e., biomass increase was more evenly distributed across 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 increased considerably more than Bosmina sp. and Diaphanosoma. The high FBI of Daphnia galeata from 1952/62 to 1979/95 was due to the small average biomass of Daphnia galeata during 1952/62. Therefore, FBI of total daphnid biomass was not much enhanced compared to the FBI 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 crustacean biomass composition (Fig. 3). Relative biomasses of daphnids, cyclopoid copepods, and car­ nivorous c1adocerans increased on an annual average during eutrophication, whereas the reia- Crustacean zooplankton 259

40

30

20

10 iii u.. o Oh Og Bos Ob Eu Hb Cye Lk BI Oa eCI hCI Cop Cr

Fig. 2. Factor of biomass increase (FBI) from 1920/24 to 1952/62 (upper panel), from 1952/62 to 1979/95 (intermediate panel), and for the overall study period (1920/ 24-1979/95, lower panel). The following taxa are analysed sepa­ rately: Daphnia hyalina (Dh), Oh Og Bos Ob Eu Hb Cye Lk BI Oa eCI hCI Cop Cr Daphnia galeata (Dg), Bosmina sp. (Bos), Diaphanosoma brach­ 200 yurum (Db), Eudiaptomus graci­ lis Heterocope borealis (Eu), 150 (Hb), cyclopoid copepods (Cyc), Leptodora kindtii (Lk), Bytho­ trephes longimanus (BI), daphnids 100 (Da = Dh + Dg), carnivorous cladocerans (cCl = Lk + Bl), herbivorous cladocerans (hCl = 50 Da + Bos + Db), copepods (Cop = Eu + Cyc), and total crustaceans o (Cr. Oh Og Bos Ob Eu Hb Cye Lk BI Oa eCI hCI Cop Cr

tive biomass of Eudiaptomus, Heterocope, Bosmina, and Diaphanosoma decreased. This re­ sulted in an increase of the biomass ratio between cladocerans and copepods from 0.4 in 1920124 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 in 1952/62. During the first period of eutrophication (1920124-1952/62), FBI of total crustacean zooplankton 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 peaks during early spring and late summer (Fig. 4a). The major biomass increase during the first 260 D. Slraile and W. Geller

~ Bytholrephes longimanus 0 Leplo6ot. Iondtii [ill cyclopold copepods Heterocope borelllis lS:J• Eudiaptomus gracilis Diaphanosoma brachyurum •mllIl Bosmlnasp. DlIptna ~leata

Daphnia hyalina Fig. J. Avcragc 0 composition of crustacean bio­ mass during the 19201 1952/ 1979/ three investiga­ 1924 1962 1995 tion periods.

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 approximately 47. 30. and 20. respectively. during these three months. During late summer and autumn (August-November). FBI's of herbivorous c1adocerans. Elldiapwmlfs. and cyclopoid cope­ pods were lower and more similar (11, 10. and 8. respectively). The bimodal increase pattem oftotal crustacean biolllass during the second period (Fig. 4a) can be explained by the increase of dadocerans and cyclopoid copepods. Herbivorous c1adoceran~ 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 and carnivorous cladoceroms. Elldiaptomlls biomass approximately doubled from 1952162 to 1979195. but its increase sho"ed no se3SQnal pattern (Fig. ok). Thus. from the 19505 to the 1980s. differences in FBI between herbivorous c1adocerans and copepods were larger during high summer and autumn than during spring. Carnivorous c1adocerans multiplied their biomass during the second half of the year by factors up to 30 and 10 during the first and second time period. respectively (Fig. 4e). As a result ofdiffering increase patterns of taxa and changes in species inventory. the se:l­ sona] course ofIhe contributions of different species 10 lotal crustacean biomass changed dur­ ing the eutrophication process (Fig. 5). The contribution of £lIdiopI01mls gracilis to the total crustacean biomass from January to April diminished from values up to 70% in the early 19205 to values of 50% during the 19505 and finally to about 20% during 1979 to 1995. The relative decline of EudiaplOmlls gracilis was accompanied by a relative increase of cyclopoid copepods from about 20%- in 1920-1924 to 60-70% in 1979-1995. Daphnids raised their share ofbiomass from approximately 40% during July-August in the 19205 to 40-50% from May-September in the 19505 and to 40-60% from May-November in recent years. That is. daphnids enhanced their contribution during summer approximately N 30 8 "'T1 N 80 20 "'T1 ~ A OJ ID B q ~ N 25 - N L() ..... L() I'\ ..... (j) p_ 6 (j) 60 \ ...0, ID I 15 ID ..... 20 0. CJl ..... \ CJl , , ... , \ I , , I\..l , \ I\..l \ (j) I '( 05 15 ,cl 4 40 10 ""'"£:::I b ... --I\..l £:::I""'" , 6 \ I\..l, 0 0 \ N 10 ..... N , , ..... (j) 'Q \ 2 ID 0) <0 ..... -...j ..... 20 \ 5 -...j 5 ID ~ CO iD CO ~ LL 0 0 ~ LL 0 0 ~ J F M A M J J A S 0 ND J F M A M J J A S 0 N 0

N 25 5 "'T1 50 15 ~ OJ N "'T1 N C - ~ ~ L() 20 4 ..... 40 12 (j) ID L() ...... CJl 0) ID , I\..l ..... CJl 15 3 05 30 9 I\..l I\..l 05 ""'" , I\..l a 10 2 ""'"£:::I 20 6 , N ..... 0 (j) ID N ...... -...j 0) ID 5 1 ..... 10 3 -...j CO ~ ~ LL CJl CO ~ 0 0 ~ LL 0 0 ~ F M A M J J A S 0 N D J F M A M J J A S 0 N 0 () 2 ~ llJ N 40 10 "'T1 (') ~ CD ~ E llJ L() 8 ..... :::l 0) 30 ID N ..... CJl 0 , 6 Fig. 4. Factors of biomass increase (FBI) between the investiga- 0 ~ "0 20 I\..l tion periods in distinct months for a) total crustaceans, b) herbivo- £:::I""'" 0. 'Cl ill 0 4 rous cladocerans (daphnids, Bosmina, and Diaphanosoma), :::l N \ ..... ~ (j) 10 \ ID c) Eudiaptomus, d) cyclopoid copepods, and e) carnivorous 0 ..... 2 -...j :::l ID cladocerans (Leptodora and Bythotrephes). The left scale and co iD LL 0 0 ~ dots refer to the FBI from 1920/24 to 1952/62, the right scale and F M A M JJ A S 0 N D open circles to the FBI from 1952/62 to 1979/95. I~ 262 D. Straile and W. Geller

1920 - 1924 (Auerbach et al. 1926) 100 ~ Bytholraphes kmgimanus 80 o Laplodora kindlii 60 fi /~J cydopoid copepods

• Heterocope Dorealis 40 rs::::::J Eudiaplomus gracilis

• Diaphanosoma brachyurum 20 mm Bosmina sp. o o Dapi1nia galeala JFMAMJJASOND D Daphnia hyalina

1952 - 1962 {Muckle & Muckle-Rottengatter 1976}

100

80

60

40

20 o JFMAMJJASOND

1979 - 1995 (this study)

100 ·A- ;z= :':' Fig. S. Monthly crustacean £. 80 ',\ ::= c ~~;;;~~<2<:: biomass composition of oligo­ ~ ',\ trophic Lake ConSlance (1920­ 24, AUERBACH et al. 1926). the •0 60 0- /: lake in transition in respect to E 0 lrr " species composition, i.e., the 0 40 It', ~ I-i'- >-Im new species already present and • I' Diol,lJollosoma and Heterocope •E 20 Ki" not yet disappeared (1952-1962. :c0 MUCKl£ & MucKLE-ROTIEN­ f:rilrl, 10: GAITER 1976), and the eu­ 0 trophic lake (1979-1995. this JFMAMJJASOND study). Crustacean zooplankton 263

100 A ~ 0 en 80 "0 '0 Cl. en..Q ::> (j 60 EG ,S+ 0- en :cell :l 40 ::> E w .8 0- :cell 20 :l w 0 J F M A M JJ A S 0 N D

~ e..... 100 B en c: ~ Q) 80 (j 0 "0 en.!!:! ::> (j 60 E..ci ~Q)o '- O-.!: ~+ 40 :l en w:l E -@. 20 :cell :l w 0 J F M A M JJ A S 0 N D

100

Fig. 6. Biomass relation- 80 ships between a) Eudiapto- ~ mus and cyclopoid cope- 0 en pods, b) Eudiaptomus and c: ~ 60 herbivorous cladocerans, ellQ) .- (j and c) Daphnia and herbivo- c: 0 .&="0 O-cu 40 rous cladocerans. Herbivo- ell- o~ rous cladocerans include -e Daphnia sp., Bosmina sp., Q) 20 and Diaphanosoma brach- .!: yurum. (dots: 1920-1924, opencircles: 1952-1962, tri- O angles: 1979-1995). J F M A M JJ A S 0 N D

from 40 to 60%, but more importantly, they enlarged their window of seasonal dominance from 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 to October during 1979/95. 264 D. Straile and W. Geller

Changes in relative biomass between Eudiaptomus and cyclopoid copepods during eutrophication were pronounced within the first half of the year and less obvious from July to December (Fig. 6a). Comparing herbivorous cladocerans and Eudiaptomus, the time of pro­ nounced change in relative biomass was confined to late summer and autumn (Fig. 6b). A third pattern of changes in biomass distribution emerged within herbivorous cladocerans (Fig. 6c). Relative biomasses of daphnids increased at the expense of smaller cladocerans especially in winter, early spring, and in late summer/autumn (Fig. 6c). Thus, changes in relative biomass were more pronounced within copepods (Fig. 6a) and herbivorous cladocerans (Fig. 6c) than between herbivorous cladocerans and Eudiaptomus (Fig. 6b).

Re-oligotrophication In order to identify the long-term effect of eutrophication throughout this century, crustacean biomass and species composition during the years 1979-1995 have been considered as rela­ tively homogenous, and average conditions prevailing during this time were contrasted against the previous observations during the 1920s and 1950s. Given the large differences in trophic state between these three periods, e.g., mean and median of TPMIX from 1952/62 and 1979/95 differ by approximately a factor of five, this approach appears justified. However, the period from 1979 to 1994 covers a decrease in TPM1X by almost a factor offour and thus may enable an analysis of potential effects of re-oligotrophication. Except for Bosmina and Eudiaptomus, biomass of crustacean species showed no trend from 1979-1995 (Figs. 7, 8). Daphnia hyalina reached highest biomasses with up to 10 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 surpassed the abundance peaks during the spring development. In contrast, maxima in biomass of Daphnia galeata occurred during late spring. Average biomasses of daphnids were not related to winterly total phosphorus values (Fig. 8). However, the temporal window of Daphnia galeata during the season is shrinking (Fig. 9). Daphnia galeata occurred later in spring and disappeared earlier in autumn during the 1990s than during the 1980s. The time span between its first and last occurrence in zooplankton samples in the different years was 2 positively related to TPMIX (r = 0.3, p < 0.05). This relationship is statistically significant despite 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, which resulted in a small observation window and probably in an underestimation of the occurrence window of D. galeata (Fig. 9). Maximum biomass of Bosmina declined from values around 1 gC/m2 during the 1980s to less than 0.1 gC/m2 from 1991 to 1994. However, in 1995, peak biomasses of Bosmina exceeded 0.5 gC/m2 (Fig. 7). The relationship between yearly averages of Bosmina biomass and 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 from 1984 to 1991, but was high from 1992 onwards (Fig. 7). Despite these large oscillations, the annual 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 and Bythotrephes showed a notable trend in population dynamics within the years 1979-1995 (Figs. 7, 8). Crustacean zooplankton 265

D. hyalina cyclopoid copepods '" 10.0 5 E ~ 7. 1 (] 75 .9 .£l 5.0 i en 5.0 en en en ro ro 2.5 E 2.5 E o o :0 :0 0.0 l)..,LiL~-,lII\""~~IowjIlMiIl,J4.L.i,- 79 81 83 85 87 89 91 93 95 79 81 83 85 87 89 91 93 95

7.5 D. galeata Leptodora kindtii NE NE~ 2.0J (] (] 1.5 .£l 5.0 .9 en en 1.0 en en ro 2.5 ro E E 0.5 .Q o .D. 0.0 J,J,y"""-,-JI\-Irlll.,JLc'Y""~H'-;-'L,- :0 0.0 -Y"-r&rJ....-,-JI\A.-"-r",..d!r''r-r"'r''I-"Y''r''r 79 81 83 85 87 89 91 93 95 79 81 83 85 87 89 91 93 95

2.0 Bosmina ~ 0.8 Bythothrephes longimanus E E (] 1.5 (] 0.6 .9 Cl en 1.0 ';; 0.4 en en ro ro E 0.5 E 0.2 o .Q :0 o.0 -',"\-""I'"',,;-&;-""'~_-"'!-"Y'"r'"T'-r'-r''''' .D. O. 0 -'yA\~""'--r"I--r'''''''-''r"''''~t-"'r''o-'"r 79 81 83 85 87 89 91 93 95 79 81 83 85 87 89 91 93 95

~ 1.5 Eudiaptomus gracilis NE (] .9 1.0 en en ro 0.5 E .Q .D. 0.0 79 81 83 85 87 89 91 93 95

Fig. 7. Biomass ofcrustacean zooplankton from 1979 to 1995 measured weekly to biweekly in the north­ western arm of Upper Lake Constance COberlinger See).

Discussion

Eutrophication

This study compares the averages ofthree long-term time series ofcrustacean plankton in Lake Constance. The concentration on long-term averages reduces the impact of factors acting on smaller time scales, e.g., interannual variability of weather patterns (GAEDKE et al. 1998) and fish predation (ECKMANN & RbsCH 1998), which cause considerable variability in crustacean biomass and might blur the effects ofeutrophication. 266 D. Straile and W. Geller

D. hyalina D. galeata Bosmina E 1.5 r =-0.21, ns 0.8 r =0.09, ns 0.20 r =0.83, P < 0.0001 1.2 • CJ 0.6 • • 0.15 • ..Ql 0.9 • • 0.10 (f) 0.4 •• • (f) 0.6 • • , . .. • ell • •• • • E 0.3 ,,- .. •• 0.2 • • • 0.05 ·•• •• o • • • • • :0 0.0 0.0 · . 0.00 .,,: 100 80 60 40 20 100 80 60 40 20 100 80 60 40 20

E. gracilis cyclopoid copepods B. longimanus N" 30 0.5~ 0.6 n~ 0.05 ..§ 0. 1r = P < 0.05 r =0.08, r =0.31, ns U 0.25 ••••• •• • 0.04 0.4 • •• - ..Ql I· • •... 0.03 0.20~ •• • , (f) • . • ... (/) • 0.02 .- CIl • • 0.2 •• • E 0.15] ..-. .. 0.01 •• o :.c 0.10 0.0 0.00 100 80 60 40 20 10080 60 40 20 100 80 60 40 20 Fig. 8. Average annual biomass of TP MIX [1..19 /1 ] TP MIX [1..19 /1 ] TP MIX [1..19 /1 ] crustacean taxa vs. L. kindtii ~ 0.10 r = 0.16, ns TPMIX' Each dot represents one study U 0.08 • • -- • year and r is Pearson's ..Ql 0.06 • •• (f) .. • • correlation coeffi­ (f) 0.04 • • CIl •• •• cient. Note that the E 0.02 scale on the x-axis .Q ..c 0.00 follows the temporal 10080 60 40 20 development and is TP MIX [1..19/1] reversed.

Additionally, comparing long-term averages reduces the potential effects of spatial hetero­ geneity and patchiness. Numbers and places of sampling stations differ between the three sampling periods compared in this study, e.g., only one station situated at the Uberlinger See is sampled with high frequency from 1979 to 1995 compared to several other stations at the Uberlinger See and at the central part of Upper Lake Constance during 1920-1924. Several authors found large horizontal heterogeneity in crustacean abundances in Lake Constance at individual sampling dates, but - with the possible exception ofhigher abundances in the Bay of Bregenz at the eastern end of the lake - no persistent, large-scale spatial patterns were identified (BAYERSDORFER 1924, ELSTER & SCHWOERBEL 1970, EINSLE 1990, ApPENZELLER this volume). Thus, the comparison of long-term averages should not be hampered by spatial heterogeneity of crustaceans in Lake Constance. The comparison of the three time series is, however, hampered by differences in sampling gear. Absolute and relative increases in biomass ofcrustaceans between the three study periods can only be interpreted cautiously. Nevertheless, the approximately 50-fold biomass increase ofcrustaceans 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 micro­ scopic countings (KUMMERLIN 1998) and pigment concentrations in sediments (LENHARD 1994). Rotifer biomass increase during eutrophication was estimated to amount also to two orders of magnitude (WALZ et al. 1987). Crustacean zooplankton 267

360 00 000 0 85_ 0 320 0 0 0

0 86 81- 0 (j) 280 84 -87 >. -- co 0 ~ 0 c 240 Fig. 9. Time span of 80 -95 a.CO - 90 seasonal occurance of en 79- - Daphnia galeata vs. -94 Q) 200 82 89 TPMIX' Each full dot repre- E - 91 :;=; - sents onc study year. - Circles represent the time 88• span of sampling within 160 the respective years, i.e., the maximum range of • 93 Daphnia galeata occurren- 120 92 • ce which could be obser- ved. During two years 100 80 60 40 20 (1984 and 1985) occur- rance and observation windows were similar. TP MI x [j.Jg/l]

The most pronounced relative increase in crustacean biomass occurred from the early 1920s 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 from the 1950s to the 1980s (LENHARD 1994 and pers. comm.). That is, although the absolute in­ crease in nutrient concentrations was largest after World War II (GliDE et al. 1998), biomass of phytoplankton and crustaceans indicate a strong relative increase in nutrient concentrations already before the 1950s. The overall changes in community structure of crustacean zooplankton confirm with find­ ings from other studies. Cladocerans and cyclopoid copepods increased more strongly than calanoid copepods during eutrophication, which is in accordance with concepts and observa­ tions by GLIWICZ (1969), PATALAS (1972), ROGNERUD & KJELLBERG (1984), and Muck & LAMPERT (1984). Similar shifts in community structure were observed during the course of eutrophication, 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 Lago Lugano, where calanoid copepods disappeared completely for almost 30 years from the pelagic zone and reappeared in the course of re-oligotrophication (POLLI & SIMONA 1992). The mechanisms behind these changes in species composition are, however, not fully un­ derstood. For example, it is difficult to separate the direct effect of eutrophication on the spe­ cies composition from the impact of newly invading species (EINSLE 1983). The first important changes in species inventory, the invasion of Cyclops vicinus and Daphnia galeata, took place during the early 1950s, almost 50 years (!) after the first signs of increasing 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 to 1963, all major changes in species inventory of crustaceans occurred. This comparatively small time span suggests that these changes are not independent of each other. Besides in­ creased food concentrations due to eutrophication, a severe reduction of fish stocks due to overfishing during the early 1950s (HARTMANN 1987, ECKMANN & ROSCH 1998) might have facilitated the establishment of the new species. However, the occurrence of new species probably altered the "ecological theatre" and brought new ecological interactions. Further­ more, 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 consequences for the zooplankton community structure in Lake Constance (EINSLE 1983). Studies by EINSLE (1977, 1983) and WOLFL (1991) revealed that cyclopoid copepod biomass is dominated by Cyclops vicinus during the first five months of the year. During this time, the relative importance of cyclopoid copepods and Eudiaptomus reversed during the course of eutrophication. Tn early June, a diapause migration of Cyclops vicinus copepodites causes an abrupt decline of cyclopoid copepod planktonic biomass with Cyclops abyssorum and Mesocyclops leuckartii as the dominating cyclopoid copepod species (EINSLE 1967, WOLFL 1991). From July onwards, the biomass ratio between Eudiaptomus and cyclopoid copepods has 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 second half of the year. Low food concentrations might have prevented the establishment of a large population of cyclopoid copepods in oligotrophic Lake Constance. Threshold food concentrations ofCyclops vicinusjuveniles are considerably largerthan the threshold food concentrations ofEudiaptomus resulting in slow growth, poor survival, and lower competitive ability ofjuvenile cyclopoids at low food concentrations (SANTER 1994). In contrast, juvenile cyclopoids might be superior to calanoid juveniles at higher food concentrations (SANTER & VAN DEN BOSCH 1994), which would enable them to exploit more efficiently increasing food concentrations due to eutrophication. Predation by older cyclopoid copepodites on calanoid juveniles (EINSLE 1978, KAWABATA 1991, SANTER & VAN DEN BOSCH 1994) might additionally have contributed to the changes in relative biomass between Eudiaptomus and cyclopoid copepods during eutrophication in Lake Constance. However, it should be kept in mind that Eudiaptomus did not decline inthe course ofeutrophication, but rather was less successful than cyclopoid copepods to exploit the increasing food concentrations. The biomass ratios between Eudiaptomus and Daphnia changed with the exception of autumn and early winter only marginally. Hence, the strong relative decline of Eudiaptomus on an annual average is largely attributable to the invasion of Cyclops vicinus rather than to competitive interactions with daphnids. Predation by Cyclops vicinus on the nauplii and small copepodites of Heterocope borealis is thought to be responsible for the decline and disappearance of this large predatory calanoid copepod in Lake Constance (KrEFER 1973, EINSLE 1983). Heterocope became extinct in a number of large perialpine lakes (KIEFER 1973). However, this disappearance was not associated with an increase ofcyclopoid copepods, especially Cyclops vicinus, in all lakes. In Lago Maggiore, Heterocope disappeared without the invasion of Cyclops vicinus and despite a decrease in the abundance of cyclopoid copepods (DE BERNARDI et al. 1988, 1989), which suggests that additional factors influenced the decline of Heterocope in European perialpine lakes. 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 impor­ tance of species interactions in shaping the response of crustaceans to eutrophication. Daphnia galeata may be considered the second important new zooplankton species in Lake Constance. Daphnia galeata differs from the "native" Daphnia hyalina by higher egg ratios and growth rates under favourable food conditions (GELLER 1989), but poorer growth when food is scarce (STICH & LAMPERT 1984). Consequently, the contribution of Daphnia galeata to crustacean biomass during the 1980s was largest during and shortly after the phytoplankton spring bloom, whereas Daphnia hyalina reached its highest contributions during late summer and autumn. Higher growth rates ofDaphnia galeata might also contribute to the earlier popu­ lation development of daphnids during the 1950s and 1980s relatively to the 1920s. The earlier seasonal development ofDaphnia during the 1950s and 1980s compared to the 1920s does not support the hypothesis that population development of daphnids in spring is delayed due to predation by Cyclops vicinus (LAMPERT 1978), which should result - other things equal- in an opposite pattern. Adults and late copepodites of Cyclops vicinus have been observed 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 the diapause of Cyclops vicinus and the timing of the daphnid population increase in spring has been observed (unpublished results). In contrast, the timing of the daphnid population growth is 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 daphnid population development may have been overestimated. Increased food concentrations allowed Daphnia hyalina to maintain high population densi­ ties until late autumn at the expense of smaller-sized cladocerans. Small cladocerans are fa­ voured by low food concentrations (ORCUTT & PORTER 1985) and often follow larger-sized cladocerans in seasonal succession (DEMOTT 1989), presumably due to higher growth rates and enhanced starvation resistance of juveniles at low food concentrations (ROMANOVSKI 1985, ROMANOVSKI & FENIOVA 1985, TESSIER & GOULDEN 1987). With augmenting food concentrations due to eutrophication, Daphnia juveniles are able to compete successfully with juveniles of smaller cladocerans and prevent a juvenile bottleneck in Daphnia high summer population dynamics (DEMoTT 1989). The increasing success of Daphnia hyalina in summer does, however, not explain the disappearance of Diaphanosoma brachyurum, which is a regu­ lar component of many mesotrophic and eutrophic lakes (DEMoTT & KERFOOT 1982). The seasonal development of Diaphanosoma overlapped greatly with the occurrence of carnivo­ rous cladocerans, the biomass of which increased strongly during eutrophication. Further­ more, the vertical distribution ofDiaphanosoma 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 the overall increase of potential prey might be responsible for the collapse of the Diaphanosoma population, which was less able to exploit the increasing food supply. This suggests that the disappearance of Diaphanosoma was due to apparent competition (HOLT 1977) rather than exploitative competition. To summarize, biomass of crustaceans increased by a factor of about 50 in the course of eutrophication. The loss and new appearance ofmajor crustacean species were confined to the rather small time span from the late 1950s to the early 1960s and presumably had strong impacts on the populations dynamics of "native" crustaceans and their response to eutro­ phication. 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 during summer and autumn. The increase of both cyclopoid copepods and Daphnia can probably be attributed to an augmenting survival of juvenile stages, i.e., the overcoming of juvenile bottlenecks, 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 recent years values obtained during the early sixties. In contrast to the distinct response of the phytoplankton community to re-oligotrophication (GAEDKE & SCHWEIZER 1993, GAEDKE 1998a), only slight - if any - responses of the crustacean zooplankton community are apparent. The decrease ofphytoplankton biomass in summer was largely due to the declines of large and hardly edible phytoplankton species (GAEDKE 1998a). Summer biomass of small, edible, and fastest growing phytoplankton species was remarkably constant during 1979 to 1996 and the decrease of primary productivity was small (HAESE et al. 1998). This may indicate that the nutritional basis of herbivorous zooplankton changed less than it is inferred from total phytoplankton biomass and TPMIX' The lacking response of primary consumers is additionally supported by long-term data of rotifer biomass in Lake Constance which reveal also hardly any trends related to re-oligotrophication (unpublished results). For a detailed comparison of the response respectively non-response of pelagic taxa to re-oligotrophication see GAEDKE (l998b). The decline of the seasonal window of Daphnia galeata fits into the hypothesis that the response 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 the observed decline ofthe seasonal window ofD. galeata. However, other trends observed during the 1980/90s are opposite to expectations derived from the simple hypothesis that zooplankton response to re-oligotrophication would reverse changes during eutrophication. Both Bosmina and especially Eudiaptomus declined in terms of relative biomass during the course of eutrophication. The low threshold food concentration of Eudiaptomus (MUCK & LAMPERT 1984, SANTER 1994) should make this species the least one vulnerable to decreasing food concentrations. This suggests that during 1979-1995, factors other than lake trophy, such as variability in weather patterns and fish predation (GAEDKE et al. 1998, STRAILE & GELLER 1998), determined fluctuations in crustacean biomass and possibly outweighed the effects of decreased nutrient concentrations. A subsequent analysis should consider the combined effects of lake trophy, weather patterns, and variability in fish predation on the population dynamics of crustacean zooplankton in Lake Constance.

Acknowledgements

This study was performed within the Special Collaborative Program (SFB) "Cycling of matter in Lake Constance" supported by the Deutsche Forschungsgemeinschaft (DFG). Data analysis was additionally funded by the European Union Environment and Climate project REFLECT ('Response of European Freshwater Lakes to Environmental and Climatic Change'). We thank G. Richter and G. Schulze who counted most of the samples. Comments by R. Adrian, U. Gaedke, H. Glide, K.-O. Rothhaupt, and two anonymous reviewers improved the style and content of the manuscript. Crustacean zooplankton 271

References

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