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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