291Journal of Paleolimnology 30: 291–296, 2003.© 2003 Kluwer Academic Publishers. Printed in the Netherlands.

The long-term succession of high-altitude cladoceran assemblages: a 9000-year record from Sägistalsee (Swiss Alps)

Wolfgang HofmannMax Planck Institute for Limnology, P.O. Box 165, 24302 Plön, Germany (E-mail: wolfg.hofmann@web.de)

Received 28 February 2001; accepted 24 March 2003

Key words: Cladocera, Alpine lakes, Chydorids

Abstract

Cladoceran remains were analysed in a 1344 cm long sediment core from Sägistalsee (Swiss Alps, 1935 m asl)which covered the last 9000 years. Planktonic Cladocera were almost exclusively represented by Daphnia spe-cies, which occurred throughout the core. The chydorid fauna consisted of four species: Alona quadrangularis,Alona affinis, Acroperus harpae and Chydorus sphaericus of which the former was by far the most frequent spe-cies. The chydorid succession was characterised by disappearance and re-appearance of Acroperus harpae andChydorus sphaericus at about 8400 and 3340 cal. BP, respectively. As a result, there was a long period of about5000 years in which only two chydorid species were present with strong predominance (88.9%) of Alona quad-rangularis. There was also a long-term trend of an increase of Alona affinis at the expense of Alona quadrangularisthroughout the core.

Introduction

The species of the cladoceran family Chydoridae aremostly benthic and inhabit various littoral habitats inlakes and ponds. Many species are markedly eury-oecious and occur within a wide range of ecologicalconditions. It is therefore difficult to use individualspecies as biological indicators. They may, however,indicate specific ecological conditions if the total assem-blage is taken into account. In general, the diversity of alake’s chydorid fauna is closely related to the complex-ity of the littoral habitat (Whiteside and Harmsworth,1967). With respect to temperature, distinct oligothermalspecies do not exist (Meijering, 1983). Nevertheless,chydorid faunas show typical changes along latitudi-nal and altitudinal gradients as well as at climatic boun-

daries because the species differ in their cold-tolerance(Harmsworth, 1968; Hofmann, 2000). This trait allowsthe use of the chydorids for the quantitative reconstruc-tion of past temperatures. Using a data set from 68 al-pine lakes from 300–2350 m asl, Lotter et al. (1997)found statistically significant relationships to meansummer temperature for 84.2% of the taxa of benthicCladocera. In four alpine lakes at different altitudes, thechydorid faunas distinctly responded to the major cli-matic shifts at the beginning and the end of the YoungerDryas (Ammann et al., 2000; Hofmann, 2000). Korhola(1999) analysed the distribution pattern of Cladocerain 36 subarctic Fennoscandian lakes and found thatepilimnetic water temperature was among the fivemost significant physical parameters, which togetheraccounted for 67.7% of the variance of the cladocerandata. The aim of this study is to follow the long-termsuccession of chydorid assemblages at a high-altitudesite and to see how the community was affected by thespecific ecological conditions, which might have beeninfluenced by human impact.

This is the fourth in a series of eight papers published in this spe-cial issue dedicated to the palaeolimnology of Sägistalsee. Drs. AndréF. Lotter and H. John B. Birks were the guest editors of this issue.

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Materials and methods

Cladoceran remains were analysed in 112 samples fromthe sediment surface to 1344 cm sediment depth ofSägistalsee (for site details, see Lotter and Birks 2003).The samples consisted of sediment-size fractions >100 µm, which have been prepared for chironomidanalysis. The sediment size fraction < 100 µm was notavailable. The analysis is based on the counts of thecladoceran head shields and shells. These remains areknown to be under-represented in the fraction > 100 µmonly in the case of small taxa, such as Bosmina long-irostris (O. F. Müller) and Alonella nana (Baird), whichwere not present in the material from Sägistalsee. Sam-ple sizes ranged from 5–59 ml sediment (average =35.2 ml). Daphnia ephippia were counted in the totalsamples under a stereo-microscope at 20× magnifica-tion. Chydorids and Bosminas were counted in sub-samples equivalent to 0.83–52 ml (average = 10.4 ml)at 100× magnification. Calculation of fragmented com-ponents follows Frey (1986, Table 32.1). For identifi-cation of the remains the keys by Frey (1958, 1959) andFlößner (1972) were used. Calculation of the speciesdiversity index follows Lloyd and Ghelardi (1964). Forclustering (Euclidian distance, unweighted pair-groupaverages) the software STATISTICA was used.

Results

Frequencies of Daphnia ephippia ranged from 0–7.2specimens per ml with an average of 1.2 specimens/ml,apart from two exceptional high values of 14.0 speci-mens/ml at 1 cm and 11.2 specimens/ml at 389 cm sedi-ment depth (Fig. 1). Despite the low range of variationthere were distinct zones of low and high concentra-tions of Daphnia ephippia. The lowest frequencies (av-erage: 0.3 ephippia/ml) were found in the 714–1120 cmsection. Relatively high frequencies occurred in thesections 14–141 cm (average: 0.7 ephippia/ml), 563–708cm (0.9 ephippia/ml), and 1142–1344 cm (1.0 ephippia/ml). The highest mean concentrations were found in thesections 401–551 cm (1.8 ephippia/ml) and 156–379cm (3.1 ephippia/ml).

The Bosminidae were represented by three single oc-currences only, i.e., one Bosmina longirostris (O.F.Müller) at 1 cm and two Bosmina longispina Leydigat 218 and 472 cm sediment depth, respectively.

Throughout the core, concentrations of chydorid re-mains varied from 0.2–38.2 specimens/ml (average = 8.0specimens/ml). In the lowest section (1011–1344 cm)

and in the upper 218 cm section mean frequencies were2.1 and 2.2 specimens/ml, respectively, and were dis-tinctly lower than in the middle part of the core (230–999 cm) where, on average, 11.6 specimens were found.In this section there was, however, enormous short-term variation characterised by a total range of 0.9–38.2specimens/ml, three exceptional peaks at 379 cm (34.2specimens/ml), 472 cm (34.1 specimens/ml), and 638 cm(38.2 specimens/ml) and also by a short section (484–571 cm) with lower frequencies (range = 0.9–7.9, av-erage = 4.6 specimens/ml).

In the chydorid material five species were present:Acroperus harpae (Baird), Alona quadrangularis (O.F. Müller), Alona affinis (Leydig), Alonella excisa (Fis-cher), and Chydorus sphaericus (O.F. Müller). From A.excisa only two fragments were found at 184 cm and484 cm, respectively. For 36 samples it was not possi-ble to count at least 50 specimens as a basis for calcu-lating of percentages. This was particularly true for theupper 230 section (17 of 22 samples < 50 specimensper sample) and the section below 1011 cm sedimentdepth (13 of 21 samples < 50 specimens per sample).In these cases only presence and predominance of thespecies are indicated in the diagram.

Along the core, the four chydorid species constitutetwo different assemblages characterised by the co-oc-currence of all the four taxa and by the presence of onlytwo species, i.e., Alona quadrangularis and Alona affinis,respectively. The major pattern in chydorid stratigraphyconsists of an alternation between these two assem-blages and divided the profile into four faunal zones(CHYD1 to CHYD4). The exact positions of the boun-daries were not clear in most cases because quantita-tive data were missing and due to considerable short-termvariation in the percentage abundances. Insufficient mat-erial prevented a classification of the chydorid faunafrom the uppermost 72 cm section of the core.

Four chydorid species occurred in faunal zone CHYD1from 1344–1175 cm sediment depth (approximately9000–8500 cal. BP). With the exception of the lower-most sample, Alona quadrangularis predominated (meanpercentage = 51.1%) and Acroperus harpae (mean per-centage = 25.5%) was more frequent than Chydorussphaericus (13.4%) and Alona affinis (10.0%). Noquantitative samples exist from the section between thezones CHYD1 and CHYD2. So, the disappearance ofAcroperus harpae at 1142 cm in the non-quantitativesamples may indicate this boundary. Zone CHYD2(1142–492 cm; 8400–3400 cal. BP) is characterisedby the almost exclusive occurrence of Alona quad-rangularis and Alona affinis which made up 89.3% of

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the specimens counted. A. quadrangularis clearly pre-dominated with a mean percentage of 88.9%. Withinthis zone, percentages of Alona affinis continuouslyincreased from an average of 3.9% in the 1067–801 cmsection to 15.5% in the 791–492 cm section.

In zone CHYD3 (484–172 cm; 3340–950 years BP)Acroperus harpae and Chydorus sphaericus re-ap-peared. So, the composition of the assemblage resem-bles CHYD1. Despite considerable short-term variation,Alona quadrangularis was predominant with a meanpercentage of 64.3%. As distinguished from CHYD1,Alona affinis (mean percentage = 21.3%) was morefrequent than Acroperus harpae (11.0%) and Chydorussphaericus (3.5%). The faunal zone CHYD4 (160–82 cm;875–430 yrs BP) was separated by the predominanceof Alona affinis (mean percentage = 56.1%) over Alonaquadrangularis (31.8%). Furthermore, frequencies ofAcroperus harpae and Chydorus sphaericus were very

low with the exception of the singularly high percent-age (51.4%) of the latter species at 160 cm.

In the eight samples from the upper 72 cm sectionof the core only 56 specimens were counted at all. Thedata may indicate that Alona quadrangularis was mostfrequent again and that Acroperus harpae was missing.

The separation of two different chydorid assem-blages that consisted of two and four species, respec-tively, is produced by simultaneous appearances ofAcroperus harpae and Chydorus sphaericus as it isobvious in the diagram (Fig. 1). As for the quantitativesamples, there were 34 samples with at least one ofthese two species. In 22 samples the species were co-occurring, in 9 samples A. harpae occurred alone, andin 3 samples C. sphaericus occurred alone. Accordingto Fager’s index (Mühlenberg, 1976), these data showa significantly positive association between the twotaxa (p < 0.05).

Fig. 1. Sägistalsee, Daphnia: concentrations of phippia; Chydoridae: concentrations of remains, species diversity index (+: index not calcu-lated), percentages of the species (+. present; ++: most frequent), and faunal zones (CHYD1...CHYD4) (dates refer to the depth-age model byLotter and Birks, 2003).

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In some sections of the core, the percentage distri-bution of the chydorid species remained more or lessconstant over long periods. This is particularly true forthe 492–1067 cm section. In contrast, distinct short-term variation was observed in a few sections of thecore. The percentage abundance of A. quadrangularisdecreased from 88.3% at 401 cm to 15.1% at 389 cmand increased again to 82.9% at 379 cm. Similarly,dominance of A. affinis changed in three adjacent sam-ples from 23.8 to 4.3% and 39.1% (305–281 cm).

Chydorid species diversity was high in the sectionswhere four species were present: CHYD1 (mean speciesdiversity index = 1.71), CHYD3 (1.23), and CHYD4(1.14) and low in the zone CHYD2 (0.45) with only twospecies and a strong predominance of Alona quadrang-ularis. Within this zone species diversity increasedtowards the top from an average of 0.25 in the 801–1067 cm section to 0.59 in the 492–791 cm section dueto the increase in the proportion of Alona affinis at theexpense of A. quadrangularis.

Discussion

During the Holocene of Sägistalsee, the planktonicCladocera were represented only by Daphnia whileBosmina species were not able to establish populationsfor considerable periods of time. The data presented by

Lotter et al. (1997) also show that Bosmina species playa minor role in the plankton of alpine sites above1800 m asl. The predominance of large planktonicCladocera, such as Daphnia, suggests reduced verte-brate predation and the absence of fish (Lampert andSommer, 1997).

The chydorid species found in the Holocene sequenceof Sägistalsee are known from high-altitude sites in theSwiss Alps (Flößner, 1972; Lotter et al., 1997) andwere, for instance, reported from altitudes > 2,000 m aslin the Rila and Pirin Mountains (Bulgaria) (Naidenow,1975). They also occur, together with additional spe-cies, in subarctic Fennoscandian lakes (Korhola, 1999).Harmsworth (1968) classified these taxa with respectto their cold tolerance as ‘arctic’ (Chydorus sphaericus,Acroperus harpae), ‘subarctic’ (Alona affinis), and ‘northtemperate’ (Alona quadrangularis, Alonella excisa), res-pectively. The Sägistalsee fauna was a poor assemblageof cold-tolerant species in which less cold-tolerant spe-cies at present restricted to the region below 1,700 masl, such as species of the genera Leydigia (Kurz) andPleuroxus (Baird), Eurycercus lamellatus (O.F. Müller),Monospilus dispar (Sars), Disparalona rostrata (Koch),Graptoleberis testudinaria (Fischer), were absent(Lotter et al., 1997).

The cluster diagram in Fig. 2 compares six samplesfrom the Sägistalsee sequence as representatives of thefaunal zones CHYD1 to CHYD4 with chydorid assem-

Fig. 2. Dendrogram for the chydorid assemblages based on species percentages from the Sägistalsee core (SAEG82, SAEG273, SAEG347,SAEG581, SAEG801, SAEG1308; numbers refer to sediment depth (cm)) and from surficial-sediment samples from high-altitude lakes in theSwiss Alps (Lotter et al., 1997) (LIO: Lac Lioson, 1848 m; MEL: Melchsee, 1891 m asl; TAN: Tannensee, 1976 m asl; ENG: Engstlensee,1850 m asl; IFF: Iffigsee, 2065 m asl; WAN: Wannisbordsee, 2103 m asl; LAEM: Lämmerensee, 2296 m asl; SEB: Seebergsee, 1831 m asl;SWL: Seewli See, 2028 m asl; SCE: Schwellisee, 1933 m asl; FLU: Flueseeli, 2045 m asl; BAC: Bachsee, 2265 m asl; SAEG: Saegistalsee,1935 m asl; HAG: Hagelseewli, 2339 m asl).

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blages from surficial sediments of 13 high-altitude sites(> 1800 m asl) in the Swiss Alps (Lotter et al., 1997).Five clusters were separated according to the pre-dominating species: Lac Lioson (LIO, 1848 m asl) andLämmerensee (LAEM, 2296 m asl) were isolated dueto the predominance of Alonella excisa plus Alonaaffinis and Alona rectangula, respectively. Melchsee(MEL, 1891 m asl), Tannensee (TAN, 1976 m asl),Engstlensee (ENG, 1850 m asl), and Iffigsee (IFF,2065 m asl) constitute a group of lakes in which Acro-perus harpae dominated alone or together with Alonaaffinis or Chydorus sphaericus. Seven sites were asso-ciated due to the predominance of Chydorus sphaericus:Seebergsee (SEB, 1831 m asl), Seewli See (SWL, 2028m asl), Schwellisee (SCE, 1933 m asl), Flueseeli (FLU,2045 m asl), Bachsee (BAC, 2265 m asl) Hagelseewli(HAG, 2339 m asl), and Sägistalsee (SAEG).

The chydorid assemblages from the Sägistalsee core(SAEG82, SAEG1308, SAEG347, SAEG273, SAEG801,SAEG581) were grouped together with Wannisbordsee(WAN, 2103 m asl) owing to strong predominance orhigh percentage (SAEG82) of Alona quadrangularis.These core samples from Sägistalsee and the assem-blage from the surficial sediment sample (SAEG) werenot located in the same cluster. This discrepancy resultsfrom the fact that quantitative data from the top 70 cmsection of the core were not available because the lownumber of specimens counted did not allow calculationof percentages. The cladoceran assemblage taken fromthe surficial sediment (SAEG) is not likely to representthe most recent stage of the chydorid succession be-cause in this case the quantitative basis was insuffi-cient, too. So, the last phase of about 430 years of thechydorid history of Sägistalsee remains unclear.

The high-altitude lakes under discussion are inhabitedby a few cold-tolerant chydorid species. The chydoridcommunities at the sites above 1800 m asl are, how-ever, not uniform but may differ with respect to spe-cies composition and predominant species. The datafrom Sägistalsee show that such characteristic commu-nities, although characterised by the strong predomi-nance of one species and thus by extremely low speciesdiversity, may be stable for long periods of time. So,the CHYD2 assemblage from Sägistalsee with a meandominance of Alona quadrangularis of 89.3 % existedfor about 5000 years. This species was a dominant el-ement of the chydorid fauna throughout the period oftime represented by the core, i.e., for more than 9000years. These data show that poor high-altitude com-munities are not always subject to strong fluctuations asproposed by the diversity-stability-hypothesis (Lampert

and Sommer, 1997) but may be constant for long peri-ods of time.

During the chydorid succession of Sägistalsee, spe-cies number and species diversity changed due to thedisappearance and re-appearance of two species, i.e.,Acroperus harpae and Chydorus sphaericus. Althoughthis pattern is well documented by the data, it is diffi-cult to provide an ecological explanation for this de-velopment without a detailed knowledge of the biotopestructure. All four species from the Sägistalsee core arecold-tolerant taxa and typical elements of the fauna ofhigh-altitude alpine sites. On the other hand they oc-cur quite frequently in lowland lakes as well (Lotter etal., 1997), which may indicate their wide ecologicaltolerances and their limited potential as indicator spe-cies.

The chydorid fauna shows a clear distributional pat-tern along altitudinal or latitudinal gradients, which iscorrelated with temperature (Harmsworth, 1968; Lotteret al., 1997). Chydorids also distinctly respond to theclimatic changes, which occurred in the Late-Glacialand early Holocene (Hofmann, 2000). Under such con-ditions they have been successfully used to reconstructthe past temperature regime (Ammann et al., 2000;Lotter et al., 2000). In contrast, the Sägistalsee corerepresents a Holocene sequence from a high-altitudesite, i.e., a series without severe spatial or temporalclimatic changes. The disappearance of two speciescombined with a distinct decrease in species diversityat about 8400 years B.P. was most likely caused byecological stress which excluded the species from thelake or drastically reduced their abundance for a periodof about 5000 years (CHYD2). Both species in ques-tion, i.e., Acroperus harpae and Chydorus sphaericus,have been classified as ‘arctic’ with respect to theircold-tolerance (Harmsworth, 1968). This event was ob-viously not an effect of climatic cooling. Likewise, weare not able to explain why the same species re-ap-peared at about 3400 years B.P. (CHYD3). A corre-sponding pattern, i.e., disappearance of species andlowered species diversity in the 492–1142 cm sec-tion (CHYD2), is not discernible in the chironomidstratigraphy (Lotter and Heiri, 2003).

However, the chydorid zones CHYD1 and CHYD3characterised by the occurrence of two additional spe-cies and increased species diversity appear to corre-spond with macrofossil zones SM-1 and SM-6 whichdenote open woodlands during the early Holocene anda period of deforestation during the Bronze Age and theIron Age, respectively (Wick et al., 2003). Possibly,improved light conditions in the littoral zone favoured

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the submerged vegetation and increased the diversityof the littoral habitat. The extremely poor chydorid as-semblage of zone CHYD2 would indicate a rather uni-form structure of the littoral habitat due to shading ofthe littoral zone by the surrounding forest.

Minima of chydorid concentrations were found at thesame horizons in which accumulation rates of the domi-nant chironomid taxa were extremely low, i.e., in the5.00–5.50 cm section and at about 350 cm. This maybe explained by anoxic conditions in the deeper waterlayer caused by meromixis. However, the chydorids aregenerally restricted to the littoral zone and should there-fore not be affected by the existence of an anoxic mon-imolimnion.

The chydorid succession was also characterised bya long-term increase in Alona affinis combined with adecrease in Alona quadrangularis. This developmentcontinued throughout the period covered by the sedimentcore. These large Alona species are both euryecious andoccur in a wide variety of littoral habitats and ecologi-cal conditions (Flössner, 1972). It is therefore difficultto define the ecological conditions, which caused thislong-term replacement. According to its modern dis-tribution in the Alps Alona affinis is indicating lowertemperatures than Alona quadrangularis. This is inaccordance with Harmsworth (1968) who classifiedAlona affinis as ‘subarctic’ and A. quadrangularis as‘north temperate’.

Acknowledgments

I wish to thank A. Korhola (Helsinki) and an anony-mous referee for their constructive criticisms and sug-gestions. This is CHILL Contribution 38.

References

Ammann B., Birks H.J.B., Brooks S.J., Eicher U., v. Grafenstein U.,Hofmann W., Lemdahl G., Schwander J., Tobolski K. and WickL. 2000. Quantification of biotic responses to rapid climaticchanges around the Younger Dryas – a synthesis. Palaeogeogr.Palaeoclimat. Palaeoecol. 159: 313–347.

Flössner D. 1972. Branchiopoda, Branchiura. Die Tierwelt Deutsch-lands 60: 1–501.

Frey D.G. 1958. The late-glacial cladoceran fauna of a small lake.Arch. Hydrobiol. 54: 209–275.

Frey D.G. 1959. The taxonomic and phylogenetic significance ofthe head pores of the Chydoridae (Cladocera). Int. Revue ges.Hydrobiol. 44: 27–50.

Frey D.G. 1986. Cladocera analysis. In Berglund B.E. (ed.), Hand-book of Holocene Palaeoecology and Palaeohydrology. J. Wileyand Sons, Chichester, pp. 667–692.

Harmsworth R.V. 1968. The developmental history of Blelham Tarn(England) as shown by animal microfossils, with special ref-erence to the Cladocera. Ecol. Monogr. 38: 223–241.

Heiri O. and Lotter A.F. 2003. 9000 years of chironomid assemblagedynamics in an Alpine lake: long-term trends, sensitivity to dis-turbance, and resilience of the fauna. J. Paleolim. 30: 273–289.

Hofmann W. 2000. Response of the chydorid faunas to rapid climaticchanges in four alpine lakes at different altitudes. Palaeogeogr.Palaeoclimat. Palaeoecol. 159: 281–292.

Korhola A. 1999. Distribution patterns of Cladocera in subarcticFennoscandian lakes and their potential in environmental re-construction. Ecography 22: 357–373.

Lampert W. and Sommer U. 1997. Limnoecology. Oxford Univer-sity Press, New York.

Lloyd M. and Ghelardi R.J. 1964. A table for calculating the‘equitability’ component of species diversity. J. Anim. Ecol. 33:217–225.

Lotter A. F., Birks H.J.B., Hofmann W. and A. Marchetto 1997.Modern diatom, cladocera, chironomid, and chrysophyte cystassemblages as quantitative indicators for the reconstructionof past environmental conditions in the Alps. I. Climate. J.Paleolim. 18: 395–420.

Lotter A. F., Birks H.J.B., Eicher U., Hofmann W., Schwander J. andWick L. 2000. Younger Dryas and Alleröd summer temperaturesat Gerzensee (Switzerland) inferred from fossil pollen andcladoceran assemblages. Palaeogeogr. Palaeoclimat. Palaeoecol.159: 349–361.

Lotter A. F. and Birks H.J.B. 2003. Holocene sediments of Sägistalsee,a small lake at the present-day tree-line in the Swiss Alps. J.Paleolim. 30: 253–260.

Meijering M.P.D. 1983. On the occurrence of ‘arctic‘ Cladocera withspecial reference to those along the Strait of Belle Isle (Que-bec, Labrador, Newfoundland). Int. Rev. ges. Hydrobiol. 68:885–893.

Mühlenberg M. 1976. Freilandökologie. Quelle and Meyer, Hei-delberg.

Naidenow W. 1975. Biologische Eigenheiten der glazialen Hydro-fauna aus den Gebirgen Rila und Pirin (Bulgarien). Symp. Biol.Hung. 15: 281–284.

Whiteside M.C. and Harmsworth R.V. 1967. Species diversity inchydorid (Cladocera) communities. Ecology 48: 664–667.

Wick L., van Leeuwen J.F.N., Van der Knaap W.O. and Lotter A.F.2003. Holocene vegetation development in the catchment ofSägistalsee (1935 m asl), a small lake in the Swiss Alps. J.Paleolim. 30: 261–272.