Hydrobiologia 308 : 77-82,1995 .© 1995 Kluwer Academic Publishers. Printed in Belgium.

Contrasting responses of oligochaete communities to the abatement ofeutrophication in Lake Geneva

Claude Lang & Olivier ReymondConservation de la faune, Marquisat 1, CH-1025 St-Sulpice, Switzerland

Received 16 November 1993 ; in revised form 14 June 1994 ; accepted 6 July 1994

Key words : biomonitoring, eutrophication, indicator species, lake, recovery, zoobenthos

Abstract

Tubificid and lumbriculid worms were used to monitor, at depths of 150 m, the recovery of Lake Geneva (Switzer-land) from eutrophication . As predicted from the decrease of phosphorus concentrations, relative abundance ofoligotrophic species was higher from 1988 to 1993 than in 1983, i .e. before the abatement of eutrophication .However, this trend towards oligotrophication can be reversed, as indicated by a decrease of oligotrophic species,recorded in 1993 . But this change corresponded to the effects of an increase of water temperature on the abundanceof the mesotrophic species Potamothrix vejdovskyi rather than to a deterioration of the profundal . In addition to thisshort-term setback, oligochaete communities located at a depth of 150 m responded more slowly and less clearly tothe decrease of phosphorus concentrations than those located at a depth of 40 m . However, the zoobenthos indicatedmore clearly the recovery of Lake Geneva than the phytoplankton .

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Introduction

Lake Geneva (Switzerland) is recovering fromeutrophication, at least in terms of phosphorus concen-trations (Blanc et al., 1993). Indeed, after an increasefrom 12 mg m-3 in 1957 to 90 mg m -3 in 1979, totalphosphorus concentrations (averaged over the wholelake) have regularly decreased down to 50 mg m-3 in1992. In contrast, primary production by phytoplank-ton and chlorophyll concentrations fail to demonstratea clear downward trend in response to this recovery(Pelletier, 1993) .

Tubificid and lumbriculid communities, sampled ata depth of 40 m, clearly indicated a reversal of eutroph-ication (Lang & Reymond, 1992) . Mean relative abun-dance of species typical of oligotrophic lakes increasedin oligochaete communities from 17% in 1982 to 41 %in 1991 . Likewise in Lake Neuchatel (Switzerland),the abundance of oligotrophic species, at a depth of40 m, increased from 16% in 1984 to 33% in 1992,in response to decreased phosphorus concentrations(Lang & Reymond, 1993) . According to these values,both lakes were meso-eutrophic at the beginning of the

1980s, but mesotrophic at the beginning of the 1990s(Lang, 1990).

In the present study, we analysed changes inoligochaete communities to see if the recoveryobserved between 1983 and 1993, at a depth of 40 m,had extended its effects down to the mean depth(150 m) of Lake Geneva . This objective follows Lang's(1991) prediction that deep areas of lakes are the lastto recover from eutrophication .

Stations and methods

In 1993 (1-14 June), tubificid and lumbriculid wormswere sampled in the western part of Lake Geneva .Sampling sites were located on eight transects, paral-lel to a line running from the mouth of the Aubonneriver, on the northern shore, to the Redon river, onthe southern shore. Each 4 km long transect began3 km from the northern shore and ended 5 km from thesouthern shore. The eight parallel transects delimitedan area 4 km long and 0 .6 km wide (46 ° 24'-46 ° 26'N, 6 ° 23'-6 ° 24' E). Its mean depth. 150 m (range :140-170 m), corresponded to the mean depth of Lake

78

Geneva (Area 3, Fig . 1, Lang, 1991). On each transect,15 sites (300 m apart) were sampled with a doublebarrel-corer, each 16 cm 2 and 15 cm apart . Hence, 240cores were collected from 120 sites .

The sediment collected in each core was sieved(mesh size aperture 0.2 mm) and the retained materialwas preserved in 5% formalin. Tubificid and lumbri-culid worms, dyed with Bengal Rosa, were picked andidentified after clearing in a mixture of lactic acid andglycerol (1 :1) . Juveniles worms (diameter less than0.3 mm) were excluded from calculations to decreasethe effect of seasonal variability on species abundance(Lang, 1991). In addition, twelve cores without wormsor with juveniles only were not included in the 1993data .

Three categories were identified: species whosenumerical abundance in worm communities indi-cate oligotrophic, mesotrophic, or eutrophic condi-tions (Lang, 1991). They are designated oligotroph-ic, mesotrophic and eutrophic species in Table 1 . Therelative abundance of oligotrophic species was calcu-lated as a percentage of the total number of tubificidand lumbriculid worms in each core .

The 1993 results were compared with those col-lected in 1988 and 1990 in the same area (Lang, 1991) .In addition the 1983 survey, covering the whole lake,was used as a reference for conditions before the abate-ment of eutrophication (Lang, 1985) . However, sam-ples without oligotrophic species were much more fre-quent in the 1983 survey than in the following ones,because it included areas more affected by eutrophi-cation than the area sampled in 1993 (Lang, 1985) .Therefore, only samples in which oligotrophic specieswere present in 1983 were used in the comparison withthe other surveys. Most of these 1983 samples werelocated in the area sampled in 1993 . Thus, the treat-ment of the 1983 data was different from that used in aprevious comparison (Lang, 1991) . In addition, resultsfrom surveys made at a depth of 40 m in Lake Genevaand in Lake Neuchatel (Lang & Reymond, 1992,1993)before and after the abatement of eutrophication wereincluded in the comparison, to illustrate the effects ofdepth on the speed of recovery .

Surveys were compared in two ways : either weused all cores or only cores with oligotrophic species .The first set described the whole oligochaete commu-nity, the second set the community of oligotrophicspecies only .

Multiple comparison tests based on the least sig-nificant difference (p = 0.05) were used to comparethe mean relative abundance of oligotrophic species

between surveys (Norusis, 1990) . Log, square root andarcsine transformations were used until the assump-tions of the analysis were met .

Results

The occurrence and relative abundance of themesotrophic species Potamothrix vejdovskyi increasedin Lake Geneva between 1990 and 1993 (Tables 1, 2) .In contrast, the occurrence and abundance of theoligotrophic and eutrophic species were unchanged .If the comparison was based only on samples witholigotrophic species, the mean relative abundanceof oligotrophic species slightly decreased in 1993,because of the increased abundance of Potamothrixvejdovskyi .

If all samples were included in the comparison, themean relative abundances of oligotrophic species werestatistically the same at a depth of 150 m from 1988to 1993, i .e. after the abatement of eutrophication,as they were at a depth of 40 m in 1982 and 1984,i .e . before the abatement of eutrophication (Table 3) .In contrast, mean relative abundance of oligotrophicspecies increased in 1991 and 1992 at a depth of 40 m,after the abatement of eutrophication .

If the comparison was based only on samples witholigotrophic species, the difference between pre- andpost-abatement was evident for all surveys in thatthe relative abundance of oligotrophic species, low in1982-84, increased in 1988-93 . Figure 1 describeshow the median relative abundance of oligotrophicspecies changed with the trophic state of lakes . LakeSuperior (North America) was used as a reference foroligotrophic conditions (Lang, 1990) . Median relativeabundance of oligotrophic species increased after theabatement of eutrophication in Lake Geneva between1983 and 1988 .

The high number of zero values (i .e. of coreswithout oligotrophic species) concealed the fact thatthe mean relative abundance of oligotrophic speciesincreased between 1983 and 1988 at a depth of 150 m(Table 3). This explained why, in a previous com-parison (Lang, 1991), the trophic status was deemedunchanged in the profundal (150 m) .

Table 1 . Changes recorded between 1990 and 1993 in lumbriculid and tubificid communities of LakeGeneva at a depth of 150 m. For species 8 to 11, values based only on mature individuals, unless otherwisestated.

* The 1991 survey is used as a reference for the species present at a depth of 40 m .

Table 2 . Changes recorded in oligochaete communities of Lake Geneva between 1990 and 1993 . Sets 1 and 2based on all cores (n=189, n=228), sets 3 and 4 based only on cores in which oligotrophic species are present(n=85, n=94) . P : probability associated with the t-test . Standard error in parentheses.

79

Discussion

ther primary production by phytoplankton nor chloro-phyll concentrations demonstrated a clear-cut recov-

Contrasting responses

ery (Blanc et al., 1993 ; Pelletier, 1993) . In contrast,changes in tubificid and lumbriculid communities indi-

Total phosphorus concentrations in Lake Geneva cated a reversal of eutrophication in the sublittoral(Switzerland) decreased from 1979 to 1992, but nei-

SetMeanabundance Year

SpeciesOligotrophic P Mesotrophic P Eutrophic P

1 Absolute 90 1 .03 (0 .13) 1 .06 (0 .16) 3.06 (0.21)(No. per core) 0 .607 0.007 0.105

93 0.94 (0 .12) 1 .73 (0.19) 2.63 (0 .16)2 Relative 90 24.5 (2 .5) 16 .0 (2 .0) 59.5 (2 .6)

(%) 0 .071 0.001 0.25693 18 .7(l .9) 25 .9 (2.2) 55 .4 (2 .5)

3 Absolute 90 2 .29 (0 .22) 0 .72 (0.18) 2.14 (0 .23)(No. per core) 0 .982 0.023 0.880

93 2 .29 (0 .22) 1 .42 (0.25) 2.19 (0 .24)4 Relative 90 54 .4 (3 .3) 9 .0 (2 .1) 36.6 (3 .0)

(%) 0 .051 0.005 0.87693 45 .5 (3 .0) 18 .6 (2 .6) 35 .9 (2 .9)

Code SpeciesOccurrence (%) Chit

POccurrence (%)

1990 1993 1991 (40 m)*

I Bythonomus lemani Grube 2 .6 4 .4 24 .52 Bichaeta sanguinea Bretscher 12 .2 3 .5 1 .03 Stylodrilus heringianus Clapar&de 33 .3 36 .0 43 .84 Peloscolex velutinus (Grube) 7 .9 4 .4 65 .1

Oligotrophic species 1-4 45 .0 41 .2 0.4417 78 .15 Potamothrix vejdovskyi (Hrabe) 33 .3 45 .6 62 .56 Spirosperma ferox (Eisen) 0 0 22.47 Psammoryctides barbatus (Grube) 0 0 28.1

Mesotrophic species 5-7 33 .3 45 .6 0.0108 78.18 Limnodrilus hoffmeisteri (Clapar8de) 0 .5 2 .2 4.2

Limnodrilus sp (immatures included) 14 .8 8 .3 24.09 Potamothrix hammoniensis (Michaelsen) 1 .6 10.1 13.5

10 Potamothrix heuscheri (Bretscher) 12 .7 22.8 9.411 Tubifex tubifex (Miiller) 5 .3 9.2 7.8

Species 9-11 (immatures included) 84.1 79.8 62.0Eutrophic species 8-11 86.8 83 .3 0.3289 67.2No. of 16 cm2 cores 189 228 192

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Table 3. Mean relative abundance (%) of oligotrophic worm species before (1982-1984) and after(1988-1993) the abatement of eutrophication in Lake Neuchdtel and in Lake Geneva . Left column : allcores included . Right column : only cores with oligotrophic species included . Groups marked with acommon digit are not statistically significant at the 5% level .

(40 m) and in the profundal (150 m) . In both areas,mean relative abundance of species typical of olig-otrophic lakes increased in oligochaete communities(Table 3), as predicted from the decrease of phospho-rus concentrations (Lang, 1990) .

However, oligochaete communities of the profun-dal responded more slowly and less clearly to thedecrease of phosphorus concentrations than those ofthe sublittoral . Occurrence of samples without olig-otrophic species was much higher in the profundalthan in the sublittoral (Table 3) . This indicated thatoligotrophic species were unable to recolonize manypatches of the sediment . The most sensitive of the olig-otrophic species, Peloscolex velutinus (Lang & Rey-mond . 1992), was scarce in the profundal, but frequentin the sublittoral after the abatement of eutrophication(Table 1). The delayed recovery of the profundal maybe explained in three ways . Firstly, altered profun-dal sediment recovers more slowly. Secondly, recol-onization takes more time because distances to trav-el to recolonize patches without oligotrophic speciesare greater than in the sublittoral . Thirdly, reproduc-tive output may be slower in profundal sediments thanin sublittoral sediments . Since oxygen concentrationswere always higher than 7 mg 1-t at a depth of 200 m(Blanc et al., 1993), the delayed recovery of the pro-fundal cannot be attributed to oxygen .

Short-term oscillations

The decrease of oligotrophic species in 1993 (Table 2)can indicate either a deterioration of the profundal,due to an increase of organic sedimentation, or it

may reflect a short-term change in water temperature .Organic sedimentation was not regularly measured inLake Geneva. But we know that organic sedimentationwas lower in 1991 than in 1986 (Dominik et al., 1993) .In addition, the decreasing concentrations of particu-late organic carbon, measured in the water at a depthof 309 m, suggested a downward trend for organicsedimentation between 1986 and 1992 (Blanc et al.,1993) .

Furthermore, the changes recorded between 1990and 1993 in oligochaete communities were not thesame as those associated with an increase of organ-ic sedimentation (Lang, 1989) . In this case, abundanceof eutrophic and mesotrophic species increased where-as that of oligotrophic species decreases . In 1993, theabundance of eutrophic and oligotrophic species wasunchanged whereas that of the mesotrophic speciesPotamothrix vejdovskyi increased (Table 2) . There-fore, the increase of P. vejdovskyi in 1993 was proba-bly due to the increase of water temperature recordedin the profundal (200 m) from 1986 to 1992 (Blancet al., 1993) rather than to an increase of sedimentation .Indeed, the reproduction of this species is favoured byan increase of temperature (Lang, 1991) . Hence, short-term oscillations in population abundance can obscurethe long-term trend in community change .

In the present study, abundance changes in P. vej-dovskyi control the relative abundance analysis . Onemight conclude that the dynamics of this species maybe of importance to monitoring in that it may be indica-tive of an environment that is shifting its trophic status .The shift goes towards oligotrophy if relative abun-dance of this species increases whereas its abundance

LakeDepth(m) Year

All cores Cores with oligotrophic speciesMean (SE) Groups n Mean (SE) Groups n

Neuchatel 40 84 15 .8 (2 .8) 1 64 36.2 (3 .8) 1,2 2892 33.1 (2 .7) 2 171 55.8 (2.9) 3 101

Geneva 40 82 16.9 (2 .6) 1 61 25.8 (3 .3) 1 4091 41 .3 (2 .5) 3 192 52 .8 (2 .5) 3 150

150 83 7 .4(l .2) - 199 30.6 (3 .1) 1 4888 21 .4 (3 .0) 1 110 50.1 (4 .5) 3 4790 24.5 (2 .5) 1 189 54.4 (3 .3) 3 8593 18 .7(l .9) 1 228 45 .5 (3 .0) 2,3 94

Lee

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decreases (Lang & Nutter, 1981), it goes towardseutrophy if relative abundance decreases, whereasabundance increases . Hence, the contrasted responseobserved here (Table 2) indicates the effect of temper-ature rather than a shift of trophic status .

Changes in oligochaete communities indicate moreclearly the recovery of Lake Geneva from eutrophica-

1988 1990 1993

8 1

SURVEYFig . 1. Notched box-and-whiskers plots describing the relative abundance (%) of oligotrophic worm species in (1) the oligotrophic LakeSuperior (Lang, 1990), Lake Geneva in 1983, 1988, 1990, 1993 . The central box covers the middle 50% of the data values, between the upperand lower quartiles . The notch corresponds to the middle of a 95% confidence interval for the median . Only samples in which oligotrophicspecies are present are included in these plots (n = 137, 48, 47, 85, 94) .

tion than those using phytoplankton (Pelletier, 1993) .This suggests that the zoobenthos long-term trend maybe less obscured by short-term oscillations in speciesabundance than with phytoplankton . Additionally, itis easier to collect samples indicative of the long-termtrend for zoobenthos than for phytoplankton . Indeed,the spatial and temporal variations of phytoplankton

82

are so extreme in Lake Geneva that an adequate sam-pling is difficult to achieve (Blanc, Pelletier & Moille,1993). Therefore, a significant long-term trend is morelikely to emerge from zoobenthos than from phyto-plankton .

Acknowledgments

The comments of one anonymous referee haveimproved this text. Laurent Cavallini and ClaudeKrending helped to collect the 1993 samples .

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