Hydrobiologia 174: 57-65, 1989 0 1989 Kluwer Academic Publishers. Printed in Belgium 57

Eutrophication of Lake Neuchitel indicated by the oligochaete communities

Claude Lang Conservation de la faune, ch. du Marquisat 1, CH 1025 St-Sulpice, Switzerland

Received 9 June 1987; in revised form 29 October 1987; accepted 20 January 1988

Key words: aquatic Oligochaeta, benthos, eutrophication, indicator species, lake, lumbriculid, tubiticid

Abstract

Lake Neuchatel (Switzerland), oligotrophic until 1950, was meso-eutrophic in 1980. The relative abun- dance in worm communities of Peloscolex velutinus and Stylodrilus heringianus was used to monitor the trophic state of the lake. In 1980, the median relative abundance of these oligotrophic species was 9% in the whole of Lake Neuchatel compared with 70% in oligotrophic lakes, 35% in mesotrophic lakes, and 0% in eutrophic lakes. The scarcity of oligotrophic species in the deepest area (153 m) characterized better the meso-eutrophic state of Lake Neuch&tel than oxygen concentrations which never descended below 6 mgal- *. Location of the area within the lake from where worms were sampled was of critical importance to assess the trophic state: some areas reflected the past rather than the present state of the lake.

Introduction

In the present study, changes in worm commu- nities were used to monitor the changing trophic state of Lake Neuchgtel (Switzerland). The lake was oligotrophic until 1950; its trophic state changed during the fifties (Sollberger, 1974). Phosphorus concentrations increased from 1962 to 1980, after which, they decreased (Fig. 1 A). In 1982, phosphorus concentrations indicated that Lake Neuchatel was meso-eutrophic (Pokomi, 1984).

Around 1900, Peloscolex velutinus and Stylo- drilus heringianus were the most abundant worm species in the oligotrophic lakes of Switzerland, including Lake Neuchatel (Monard, 1919; Piguet & Bretscher, 1913). The relative abundance in worm communities of these oligotrophic species decreases with increasing sedimentation (Lang & Hutter, 1981). The organic sedimentation is

related to the productivity in the water column; i.e. to the trophic state of the lake (Binford & Brenner, 1986). Consequently, an increasingly en- riched trophic state can be indicated by a decrease in the relative abundance of oligotrophic species (Lang, 1985).

Material and methods

Twenty areas were studied in Lake Neuchatel (Fig. 1 B). Furthermore, three areas (Fig. 1 C) in Lake Geneva (Switzerland), one area in Lake Michigan (USA), and the whole of Lake Superior (USA and Canada) were used as references (Tab. 1). The areas selected in Lake Geneva were far from the external inputs or they were protected from these inputs by the pattern of currents (Lang, 1986). Lake Geneva was classified as meso- eutrophic (Pelletier, 1983), Lake Michigan as

Table

1.

Desc

riptio

n of

the

ben

thic

surv

eys

used

in

Lake

Ne

uchl

tel

(N),

in La

ke

Gene

va

(G),

in La

ke

Mich

igan

(M)

and

in La

ke

Supe

rior(S

)

Lake

Ye

ar

Area

s Nu

mbe

r of

sta

tions

pe

r de

pth

Num

ber

of

Sam

pling

un

it

20 m

40

m

. ,

60 m

90

m

120m

13

0 m

15

0m

Stat

ions

Co

res

Core

s pe

r st

atio

n

N”

1979

14

, 16

-19

102’

5*,

4 3

2 24

24

0 10

16

03’

N 19

80

1-14

, 16

15

15

13

10

53

21

2 4

643’

N 19

84

1, 1

2-16

, 18

, 19

7

6 6

5 24

96

4

16

N 19

86

18-2

0 1

1 1

3 73

19

, 18

, 36

16

G4

’ 19

84

41-4

5 4

4 4

4 16

64

4

16

G5’

1986

21

,22

12)

1 2

52

18,3

4 16

M

6’

1980

-81

23

1 1

18

37’

460

S8’

1973

24

1

4 19

18

20

10

65

13

7 13

7 19

’ 57

6

1) L

ocat

ion

of th

e ar

eas

on F

ig.

1 B.

2)

Sam

ples

take

n by

a d

iver.

3) W

orm

s pr

esen

t in

10 o

r in

4 co

res

were

poo

led,

then

a s

ubsa

mpl

e wa

s ide

ntifie

d.

4) L

ang

(198

6).

5) A

rea

21 (

150

m d

eep)

, in

ters

ectio

n of

axe

s Ro

lle-T

hono

n,

St-P

rex-

Yvoir

e;

Area

22

, 2

km w

est

of M

eiller

ie (F

ig.

1 C)

. 6)

Nale

pa

et a

l. (1

985)

, St

atio

n C-

5, 5

0 km

fa

r fro

m t

he e

aste

rn c

oast

. 7)

Sam

ples

take

n wi

th

a Po

nar

grab

on

6 di

ffere

nt

date

s. 8

) Coo

k (1

975)

, th

e wh

ole

lake

. 9)

Sam

ples

secu

red

by P

onar

or

Ship

ek

grab

s.

59

oligo-mesotrophic, and Lake Superior as oligo- trophic (Vollenweider et al., 1974).

Two cores of 16 cm2 - 15 cm apart - were taken simultaneously by a corer. The collected sediment was sieved (mesh size aperture 0.2 mm), preserved in 10% formalin, and then dyed with Bengal Rosa (1 g * l- ‘). All tub&id and lumbri- culid worms present, or a random subsample of them, were picked and mounted in the Water Mounting Medium of Gurr for identification. In 1979, a subsample was obtained from the com- bined worms from 10 cores; in 1980, from 4 cores. Subsamples were taken from each core in 1984 and 1986 (Tab. 1). From 10 to 50 worms were identified per subsample.

Worm species 1 to 4 of Table 2 were classified as typical of the oligotrophic lakes (Lang, 1985). The number of individuals belonging to these four species, expressed as a percentage of the total number of tub&id and lumbriculid worms identi- fied in each sample or subsample, was called the relative abundance of oligotrophic worm species. The relative abundance of oligotrophic worm species in Lake Michigan was calculated from the number of Stylodrilus heringianus reported to the total number of tubificids plus Stylodrilus heringianus. In Lake Superior, the relative abun- dance of Stylodrilus heringianus to the total num- ber of oligochaetes was determined; samples without Stylodrilus heringianus were excluded. Tukey’s box plots are used to display graphically the relative abundance of oligotrophic worm species (Reckhow, 1980).

Results and discussion

Worm species (Tab. 2) In 19 18, Peloscolex velutinus was present in more samples than Stylodrilus heringianus ; the con- trary was true in 1979-1986. In 1979, Peloscolex velutinus was more frequent on ‘La Motte’, an underwater hill located in the middle of the lake (Areas, 17, 18, 19), than on the shore. These differences suggest that Peloscolex velutinus is more sensitive to the increasing eutrophication than Stylodrilus heringianus. Bythonomus lema-

ni, which was present in Lake Geneva in 1918 (Monard, 1919), was absent from Lake Neuchatel. Bichaeta sanguinea, present in Lake Geneva (Lang, 1986), was not found therein dur- ing this study. However, this small size worm species can be easily overlooked. Furthermore, some immature Bichaeta were probably misiden- tified in both lakes as Stylodrilus heringianus.

Potamothrix vejdovskyi, abundant up to 150 m deep in Lake Geneva (Lang, 1986), was classified therein as a mesotrophic species. This species was found for the first time in Lake Neuchatel on ‘La Motte’ in 1986. Its relative abundance was high, indicating that this new species was well acclimat- ized in this area. Potamothrix moldaviensis, also a new species for Lake Neuchatel, was relatively abundant in Areas 14 and 16 up to 25 m deep; this species was scarce deeper.

Potamothrix hammoniensis and Tubifex tubi- fex were the most abundant worm species in Lake Neuchatel and Lake Geneva. Tubifex tubifex seemed to be more abundant than Potamothrix hammoniensis in Lake Neuchatel. Limnodrilus species were never abundant in Lake Neuchatel, at least from 40 m to 150 m deep.

Oligotrophic species in Lake NeuchBtel Relative abundance of oligotrophic worm species was higher than 50% only in some areas of Lake Neuchatel (Fig. 1 D). Most of these areas (20 m to 120 m deep) were located on or around ‘La Motte’. This area, far from the polluted rivers (B. Pokorni, pers. corn.), is swept by strong currents. Furthermore, the bottom slope around ‘La Motte’ is steep. Consequently, the organic sedimentation was decreased in this area, providing a refugium for the oligotrophic species (Lang, 1986). Relative abundances higher than 25% were recorded in Areas 12-15 where conditions of sedimentation were similar. On the contrary, oligotrophic species were absent from the Areas 1 and 7 to 10 directly exposed to the organic inputs of the most polluted rivers (B. Pokorni, pers. corn.).

In 1982 and 1983, oxygen concentrations were always higher than 6 mg * l- ’ in the deepest area (153 m) of Lake Neuchatel (Pokorni, 1984). However, oligotrophic worm species were scarce

Table

2.

Pe

rcen

tage

s of

sam

ples

whe

re s

pecie

s of

lum

bricu

lid

(l-3)

an

d tu

bilici

d (4

-16)

wor

ms

were

pre

sent

in

Lake

Neu

chat

el

and

Lake

Gen

eva.

Ol

igotro

phic

spec

ies

1-4.

Pe

rcen

tage

: +

= 5,

1 =

6-1

5, 2

= 1

6-25

, 3

= 26

-35,

4 =

36-

45,

5 =

46-5

5,

6 =

56-6

5, 7

= 6

6-75

, 8

= 76

-85,

9

= 86

-95,

10

= 9

6-10

0

Code

Sp

ecies

(au

tors

) La

ke

Neuc

hkel

Ge

neva

40 m

13

0m

150m

40

m

150m

Ye

ar

1918

’) 19

79’)

1979

19

80

1984

19

86

1986

19

86

1984

19

86

1986

1 2 3 4 5 6 7 83’

9 10

11

12

13

14

15

16

Stylo

drilu

s he

ringia

nus

Clap

ared

e By

thon

omus

lem

ani

Grub

e Bi

chae

ta

sang

uinea

(B

retsc

her)

Pelo

scol

ex

velu

tinus

(G

rube

) Po

tam

othr

ix ve

jdov

skyi

(Hra

be)

Spiro

sper

ma

fero

x (E

isen)

Ps

amm

oryc

tides

ba

rbat

us

(Gru

be)

Pota

mot

hrix

mol

davie

nsis

(Vej

dovs

ky,

Mra

zek)

Ily

odril

us

tem

plet

oni

(Sou

ther

n)

Limno

drilu

s pr

ofim

dicola

(V

errill

) Lim

nodr

ilus

clapa

rede

anus

Ra

tzel

Lir

nnod

rilus

hotfr

neist

eri

Clap

ared

e Po

tam

othr

ix be

doti

(P&e

t) Po

tam

othr

ix he

usch

eri

(Bre

tsche

r) Po

tam

othr

ix ha

mm

onie

nsis

(Mich

aelse

n)

Tubi

fex

tubi

fex

(Mtill

er)

Num

ber

of s

ampl

es

3 9

+ 8 6

1 4

1 2

+ + 1

1 2

6 4

2 4

71

12

6 4

3 6

6 +

4 7

5 2

4 3

+ 2

1 3

1 6

4 1

2 3

10

9 8

+ 2

1 +

3 1

1 +

6 + 1

+ +

1 1

1 +

1 +

2 2

1 1

+ +

2 +

1 1

3 3

4 1

+ 1

+ 3

2 6

5 3

1 4

1 12

53

96

19

18

38

6+

4 1 18

3+4

1) M

onar

d (1

919)

. 2)

Are

as

17,

18,

19; o

ther

s su

rvey

s,

see

Tab.

1. 3

) Valu

es

for

spec

ies

8-16

are

bas

ed o

nly

on m

atur

e ind

ividu

als.

I 75

78

82

I YE

AR

D

8Q

.4

2 01

7 l 1

7,19

?I

60

- -1

8 s

019

5!

-19

40-

l 18,

12

2 -2

2 a

-13

>” 20

-

5 A AZ o

-

.24

018

023

-15

014

04

.14

.13

-14

-15

013

93

l 12,

11

l 2

I I

I I

I I

I

20

40

60

90

120

130

150

DEPT

H (M

)

.18

.18 :i;

-21

:,I6

.20

F I I I I r I I I I I I I

cl

. 53

fr I I .

B n

I I I I I I I t

I

I I I

I I

I

I

I I

I I

I I

I I I

Max

.- x . b

%

75

50

25

n M

in

21

21

28

15

.

g 12

80T

80

84

80T

80

84

YEAR

80

XI

m

60

5 z m

Fig.

I A

. M

ean

annu

al co

ncen

tratio

ns

of t

otal

ph

osph

orus

(T

P)

in La

ke

Neuc

hlte

l fro

m

1975

to

1986

, m

axim

um

valu

es r

ecor

ded

in 19

62 a

nd

1973

(Po

korn

i, 19

83,

1984

, pe

rs.

corn

.) Da

ta

for

1981

are

miss

ing.

Si

nce

1982

, Ar

ea

20 h

as b

een

sam

pled

inst

ead

of A

rea

3 (F

ig.

1 B)

.

Fig.

1.

B.

Loca

tion

of t

he a

reas

(l-2

0)

in La

ke

Neuc

hlte

l. La

Mot

te

is an

und

erwa

ter

hill

whos

e to

p is

10 m

dee

p. A

rrows

, m

ain

river

s:

A, A

reus

e;

B, A

rnon

; C.

Th

ielle;

D,

Men

tue;

E,

Bro

ye;

F, Z

ihlka

nal.

Fig.

1.

C. L

ocat

ion

of t

he a

reas

in

Lake

Ge

neva

. R.

: Rh

Bne

Rive

r, th

e m

ain

orga

nic

input

(L

ang,

19

86).

Fig.

1. D

. Re

lativ

e ab

unda

nce

(2)

of o

ligot

roph

ic wo

rm

spec

ies

per

area

acc

ordin

g to

dep

th.

Value

s be

low

10%

wer

e ex

clude

d,

exce

pt f

or A

rea

20. L

ake

Neuc

hate

l: Ar

eas

l-20

(Fig

. 1

B);

Lake

Ge

neva

: Ar

eas

21,

22 (

Fig.

1

C; L

ake

Mich

igan

: Ar

ea

23;

Lake

Su

perio

r, Ar

ea

24 (

Tab.

1)

.

Fig.

1. E.

Bo

x pl

ots

displa

ying

relat

ive

abun

danc

e (%

) of

olig

otro

phic

worm

sp

ecie

s. L

ake

Neuc

hlte

l in

1980

: 80

T (A

reas

l-1

4,

16);

in 19

80 a

nd 1

984:

80-

84

(Are

as

1, 1

2-14

, 16

, 18

-19)

. Al

l sa

mpl

es i

nclud

ed

in th

e th

ree

left

side

box

plot

s,

sam

ples

wi

thou

t oli

gotro

phic

spec

ies

exclu

ded

from

th

e ot

her

plot

s.

Num

ber

of 6

4 cm

2 sa

mpl

es i

ndica

ted

unde

r ea

ch b

ox p

lot.

Perc

enta

ge

of s

ampl

es

wher

e oli

gotro

phic

spec

ies

were

pre

sent

(f)

.

62

therein. Thus, the worm communities reflected better the increasing eutrophication than did the oxygen concentration.

In 1980, the relative abundance of oligotrophic species in the whole of Lake Neuchatel was low in most cases (Fig. 1 E). The relative abundance of oligotrophic species in selected areas was the same in 1980 and 1984 (Mann-Whitney test, p > 0.44). Similar areas, stations and sampling surface were used for this comparison. The stability of the oligochaete communities suggests that the trophic state of Lake Neuchatel did not change between 1980 and 1984. This contradicts the trend indicated by the decreasing phosphorus concentrations (Fig. 1 A). However, benthic communities respond slowly to decreasing eutrophication (Lang, 1985).

Comparison with other lakes In 1984, the relative abundance of oligotrophic worm species, 40-120 m deep, was the same in Lake Neuchatel and in Lake Geneva (Fig. 2). In 1986, on the contrary, the relative abundance of these species at 150 m was lower in Lake Neuchatel (Area 20) than in Lake Geneva (Area 21; Mann-Whitney test, p = 0.001). This suggests that Lake Neuchatel was more eutrophic than Lake Geneva. However, oligotrophic species were present in the deepest area (150 m) of Lake Neuchatel whereas they were absent in 1983 from the deepest area (300 m) of Lake Geneva (Lang, 1985). In that case, Lake Geneva appears more eutrophic than Lake Neuchatel. The depths selected to compare the lakes influence the outcome of the comparison.

In Lake Neuchatel, the relative abundance of oligotrophic species at 130 m near ‘La Motte’ (Area 18,1986) was similar to the values recorded at 150 m in Lake Geneva (Area 21, 1986). In 1986, the relative abundance of oligotrophic species at 40 m was lower in Lake Neuchatel on ‘La Motte’ (Area 19) than in Lake Geneva near Meillerie (Area 22). Two factors could explain this difference. First, the bottom slope was steeper near Meillerie than in the location sampled on ‘La Motte’. Second Potamothrix vejdovskyi has recently invaded this area of ‘La

Motte’ (Tab. 2); this rapidly expanding species could have ‘squeezed’ the oligotrophic species and reduced their relative abundance.

Trophic state and oligotrophic species Two starting points were used to establish a simple relationship between relative abundance of oligotrophic worm species and the trophic state of several lakes (Fig. 3). First, oligotrophic species were absent from the profundal of eutrophic lakes such as Lake Morat (Lang, unpublished data). Second, median relative abundance of these species was 70% in oligotrophic Lake Superior (Fig. 2 B). Assuming that relative abundance of oligotrophic species decreases smoothly with the changing trophic state, a median relative abun- dance of 35x, halfway between the values 0% and 70%, was used to characterize worm com- munities typical of mesotrophic conditions. Inter- mediate trophic states were defined in the same way.

Trophic state, estimated from worm commu- nities (Fig. 3), can be compared to assessment based on total phosphorus and/or primary pro- duction. Primary production and oligotrophic worm species indicated both that Lake Michigan was oligo-mesotrophic. This agreement was prob- ably due to the fact that worms were sampled from a station reflecting offshore conditions (Tab. 1). Indeed, the trophic state indicated for Lakes Neuchatel and Geneva changed from mesotrophic to eutrophic according to the area from where worms were sampled.

The rapidly changing trophic state of Lake Neuchatel could explain these discrepancies. With phosphorus concentrations around 40 mg * m- 3 in 1982, the probability for Lake Neuchatel to be mesotrophic was 58 %, eutrophic 38x, and hypereutrophic 4% (Pokorni, 1984). Changes in phosphorus concentrations indicated that Lake Neuchatel was more eutrophic before 1982, more mesotrophic after 1982 (Fig. 1 A). Consequently, worm communities sampled in the whole lake in 1980 (N 80 T) or in its deepest area in 1986 (N 150 m) reflected probably the past meso-eutrophic state of Lake Neuchatel whereas communities sampled 130 m deep in 1986 re-

A 10

-1

80

ae

1 64

64

18

19

18

38

34

38

28

i I I : I I I I

I I I fT

I 74

x

B 75

l

50

n 25

I G

N G

N N

N G

40

-120

40

13

0 15

0

I M

ax

_ -1

00

1 . - r 13

n

16

13

5 18

18

13

7

. ?

L

-80

-60

G N

G N

N N

G M

s

40 -

120

40

130

150

150

16-2

70

LAKE

AN

D DE

PTH

(MI

Fig.

2. Bo

x pl

ots

displa

ying

relat

ive

abun

danc

e (%

) of

olig

otro

phic

worm

sp

ecie

s in

Lake

Ge

neva

(G

), in

Lake

Ne

uchl

tel

(N),

in La

ke

Mich

igan

(M),

and

in La

ke

Supe

rior

(S).

A:

all s

ampl

es i

nclud

ed,

B: o

nly

sam

ples

wi

th

oligo

troph

ic sp

ecie

s inc

luded

. Su

rface

of

sam

pling

un

it 16

cm

2 ex

cept

for

La

kes

Mich

igan

and

Supe

rior

see

Tab.

1.

The

95%

co

nfid

ence

int

erva

l ar

ound

th

e m

edian

is

indica

ted

for

Lake

Su

perio

r.

64

80 i

70 .s

2 60-

i 52.5

l M

d o- .G 40 m

=

z

4 -35 :gg:

l N 40-120m

w .N40m ‘G 40-120m

> 20-17.5 F :NN’s540” a ‘N 80 A ‘N 80T E 00 .MO,G 300m

I I I I I E ME M OM 0

TROPHIC STATE

Fig. 3. Relationship between median relative abundance (%) of oligotrophic worm species and trophic state (E eutrophic, M mesotrophic, 0 oligotrophic) of Lakes Superior (S), Michigan (M), Geneva (G), Neuchatel (N), and Morat (MO). Lake Morat is eutrophic (Lang, unpublished data). Samples without oligotrophic species were excluded. The horizontal lines indicated median

values characterizing five different trophic states. See text for further explanations.

fleeted its present mesotrophic state. Data from Lake Geneva can be interpreted in the same way. In conclusion, location within the lake of the area from where worms are sampled is of critical im- portance to assess its actual trophic state, espe- cially if the lake undergoes rapid changes of tro- phic state.

The median relative abundance of oligotrophic worm species presented in Figure 3 was based exclusively on samples where these species were present. Indeed, the inclusion of many samples without oligotrophic species influenced strongly the median values (cf Fig. 2 A and B). Further- more, two different types of data were mixed when the zero values were included: data indi- cating the absence of oligotrophic species with data describing their presence and their abun- dance. The absence of oligotrophic species from a sample does not necessarily imply eutrophic conditions. In Lake Neuchatel for instance (Lang, 1984), the median number of individuals be- longing to oligotrophic worm species was 700 per

m2 against 10000 for the other species. Conse- quently, the probability of catching at least one individual belonging to these oligotrophic species with a 16 cm2 core was less than for the other species.

Acknowledgments

Genevieve L’Eplattenier provided technical assis- tance. Lyn Treloar corrected the English. Veronique Henriod and Loraine Schmidhauser typed the manuscript.

References

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65

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