Download crustacean trophic state index

POLISH JOURNAL OF ECOLOGY
(Pol. J. Ecol.)
61
3
561–573
2013
Regular research paper
Jolanta EJSMONT-KARABIN1, Andrzej KARABIN†
1
Institute of Biology, University of Białystok, Świerkowa 20B, 15-950 Białystok, Poland,
e-mail: [email protected] (corresponding author)
THE SUITABILITY OF ZOOPLANKTON
AS LAKE ECOSYSTEM INDICATORS:
CRUSTACEAN TROPHIC STATE INDEX
ABSTRACT: Industrial processes and the
use of fertilizers are the main causes for the rapid
eutrophication of lakes. Different indices, both
chemical and biological, may be used to assess
a level and a rate of the eutrophication process.
Zooplankton indices can be among them, as zooplankton community structure is determined primarily by the physical and chemical environment
and modified by biological interactions, i.e. predation and interspecific competition for food resources. Among biological indices of trophic state
of lake, those based on densities and structure of
crustacean communities seem to respond weaker.
There are, however, patterns of crustacean communities connected with trophic state of lakes.
Thus, an increase in trophic state causes: (1) an
increase in the total numbers of crustaceans; (2)
an increase in the total biomass of Cyclopoida; (3)
an increase in the contribution of the biomass of
Cyclopidae to the total crustacean biomass; (4) an
increase in the ratio of the biomass of Cyclopoida
to the biomass of Cladocera; (5) a decrease in the
average body weight of Crustacea; (6) an increase
in the ratio of Cladocera to Calanoida numbers;
(7) an increase in the ratio of Cyclopoida to Calanoida numbers; (8) an increase in the dominance
of species indicative of high trophy (Mesocyclops
leuckartii, Thermocyclops oithonoides, Diaphanosoma brachyurum, Chydorus sphaericus, Bosmina
(Eubosmina) coregoni thersites) in the numbers
of all indicative species. Crustacean zooplankton
was sampled at the deepest place in a lake at 1 m
intervals from the surface to the bottom of epilimnion layer, and then samples were pooled together for the layer. Samples were taken once a year,
during the summer stagnation. The material was
collected from a total of 41 dimictic and 33 polymictic lakes within Masurian Lake District, Iława
Lake District and Lubawa Upland.
Among above-mentioned indices, six were the
best correlated with trophic state of lakes. Below
are formulas which enable to assess trophic state of
lakes regardless of their mixis type (TSICR) from parameters of abundance and structure of crustacean
communities: (1) TSICR1 = 25.5 N0.142 (R2 = 0.32),
where TSI = trophic state index; N = numbers (ind.
l–1); (2) TSICR2 = 57.6 B0.081 (R2 = 0.37), where B =
biomass (mg w.wt. l–1); (3) TSICR3 = 40.9 CB0.097 (R2
= 0.35), where CB = percentage of biomass of Cyclopoida in the total biomass of Crustacea (%); (4)
TSICR4 = 58.3 (CY/CL)0.071 (R2 = 0.30), where CY/
CL = ratio of the Cyclopoida biomass to the biomass
of Cladocera (%); (5) TSICR5 = 5.08 Ln (CY/CA) +
46.6 (R2 = 0.37), where CY/CA = ratio of Cyclopoida numbers to the numbers of Calanoida; (the
relationship covering exclusively dimictic lakes);
(6) TSICR6 = 43.8 e0.004 (IHT) (R2 = 0.30), where IHT
= percentage of species indicative of high trophy in
the indicative group’s numbers. It was assumed that
the lakes with a TSICR under 45 are mesotrophic,
those with a TSICR value of 45–55 are meso-eutrophic, those with a TSICR value of 55–65 – eutrophic
and those with a TSICR above 65 – hypertrophic. Although crustacean indices of trophic state of lakes
562
Jolanta Ejsmont-Karabin, Andrzej Karabin†
seem to be less useful than other biological indices,
they may be recommended in assessing the quality
of lake waters.
KEY WORDS: trophic state indices, eutrophication, Crustacea, lakes
1. INTRODUCTION
Although eutrophication is a natural process of water ecosystem succession, its acceleration due to increased input of nutrients
may lead to heavy blooms of Cyanoprokaryota and pollution. The conceptual framework
of lake trophic state leads to a development
of parameters that should help to classify water bodies according to their trophic status.
Since zooplankton community composition
and abundance are affected by eutrophication, these communities have potential value
as indicators of changing trophic conditions
(B ays and Cr isman 1983, Gu l at i 1983,
Hs i eh et al. 2011).
Crustacean zooplankton seems to respond to a trophic state rise, however a high
indicative value was found rather for group
structure parameters, i.e. based on the relative numbers and biomass of crustaceans than
abundance of particular species (Kar abi n
1985a). Generally, crustaceans seem to be
worse indicators of lake trophy than rotifers
(B ays and Cr isman 1983, Karabin 1985a,
Č eirans 2007). One of the most important
reasons of low suitability of Crustacea as trophy indicators, according to Č eirans (2007),
is their susceptibility to negative influence of
summer algae blooms, and toxic influence
of cyanoprokaryotes. Hsieh et al. (2011)
suggest that higher trophic levels may show a
more delayed response or no response to eutrophication than lower ones.
One of the factors most seriously influencing densities and taxonomic composition
of crustacean zooplankton may be fish predation. However, as it was shown in observations on two oligotrophic lakes in southcentral Ontario (R amcharan et al. 1995), in
lakes with long-time persistence of planktivores compensatory responses of prey populations tend to diminish the impacts of fish
populations.
According to literature an increase in a
lake trophy may cause:
•
an increase in the total numbers of
crustaceans (Pat a l as 1972, Kar a bi n 1985a, Pi nto - C o el ho et al.
2005a)
• an increase in the total biomass of
Cyclopoida (Kar abi n 1985a)
• an increase in the contribution of the
biomass of Cyclopidae to the total
crustacean biomass (Hi l lbr i cht I l kowska et al. 1979, Pa c e 1986,
Pi nto- C o el ho et al. 2005b);
• a decrease of cladoceran dominance
and consequently – an increase of
the ratio of the cyclopoid biomass to
the biomass of Cladocera (Kar abi n
1985a);
• a decrease in the average body volume of Crustacea (B ay s and C r is man 1983, Karabi n 1985a);
• an increase in the ratio of Cladocera
to Calanoida numbers (Hsi eh et al.
2011, Pi nto-C o el ho et al. 2005b);
• an increase in the ratio of Cyclopoida
to Calanoida numbers (Je pp e s e n
et al. 2000, Hs i eh et al. 2011, Pi n to- C o el ho et al. 2005b);
• changes in the species structure of
crustacean community, i.e. a decrease
of the dominance of species typical
for low trophy (Heterocope appendiculata (Sars), Bosmina berolinensis
(Imhof), Bythotrephes longimanus
(Leydig), Daphnia galeata (Leydig),
D. cristata (Sars), D. cucullata (Sars))
and an increase of that typical for
high trophy (Mesocyclops leuckarti
(Claus), Thermocyclops oithonoides (Sars), Diaphanosoma brachyurum (Lievin), Chydorus sphaericus
(O.F.M.), Bosmina (E.) coregoni thersites (Poppe), Bosmina longirostris
(O.F.M.)) (Pe j l er 1965, Ha k k ar i
1972, Kar abi n 1985a, Hof man n
1996).
The aim of the paper was to test the citied
above relationships using data on numbers
and biomass of Crustacea in lakes of different
trophy. The best-working formulas describing the relationships could be used to elaborate models that would help researchers to assess trophic state of so-called harmonic lakes
in central and northern Europe basing on
zooplankton data. They would be also useful
Crustacean trophic state index for lakes
in preparing similar indices for lakes in other
parts of the world.
2. STUDY AREA AND METHODS
Lakes under study were located within
three geomorphological units – Masurian
Lake District, Iława Lake District and Lubawa
Upland (Karabin 1985a). The range of trophic state of the lakes was relatively wide, i.e.
from mesotrophy to hypertrophy. The material was collected from a total of 41 dimictic
and 33 polymictic lakes (Table 1). Some of the
lakes were visited twice or three times.
The study was carried out in the years
1976–1996. In 1976–1978, the study covered lakes in all the studied districts except
the lakes of the Suwałki district. The lakes in
the Suwałki district were visited in the years
1983–1985. In the years 1985–1996, only the
water bodies of the Great Masurian Lake System were visited.
Crustacean zooplankton was sampled using 5 L Bernatowicz’s sampler at the deepest
place in a lake at 1 m intervals from the surface to the bottom of epilimnion layer, and
then samples were pooled together for the
layer. Samples were taken once a year, during
the summer stagnation. The period was chosen by Karabin (1985a) as the best for comparative analysis of the zooplankton because
of stability of summer communities being
under the influence of mostly trophic factors.
Individual body-weight was determined
on the basis of the relationship between body
length and body weight for each crustacean
species (B ott rel l et al. 1976, B a lush k i na
and Vinb erg 1979).
Comparison of parameters describing
trophic state of lakes, like Secchi disc transparency, chlorophyll a and total phosphorus
concentrations (methods are described by
Kufel (1999) and Karabin (1985a)) after transformation to trophic state indices
(C arls on 1977), has revealed significant divergences between the parameters’ values for
the same lakes. As differences between TSI
calculated for Secchi-s disc and chlorophyll
a values were lower than these both indices
to total phosphorus concentrations, mean of
the former two was used as variable describing trophic status of the studied lakes (Ej s mont-Karabin 2012).
563
Statistical analysis was performed using
Statistica software, version 5.5 (StatSoft, Inc,
Tulsa).
3. RESULTS
3.1. The total numbers of Crustacea
The relationship between the numbers
of Crustacea and TSISD-CHL is positive, exponential and significant in both dimictic and
polymictic lakes (Fig. 1). The lowest density
(8 ind. l–1) was recorded in the mesotrophic and dimictic Lake Przystań, whereas
the highest density (729 ind. l–1) was found
in the highly eutrophic and dimictic Lake
Tyrkło. The mean abundance of Crustacea
in dimictic lakes was 239 ind. l–1 (SD = 142;
n = 88), and in polymictic lakes it was markedly higher, i.e. 322 ind. l–1 (SD = 137; n = 41).
The lowest and highest densities in polymictic lakes were 17 ind. l–1 in the mesotrophic
Lake Mamry Małe and 657 ind. l–1 in the hypertrophic Lake Tuchel, respectively. The relationships between TSISDCHL and crustacean
numbers were relatively close for both mictic
types of lakes (Fig. 1, Table 2). Correlation
coefficients (after logarithmic transformation
of number values) were not different statistically (polymictic: n=41; r = 0.45; dimictic: n
= 88, r = 0.52; P = 0.32). Thus, TSICR1 may be
established from the same formula for both
dimictic and polymictic lakes (Table 3).
3.2. The total biomass (wet
weight ) of Cyclopoida
The total biomass of Cyclopoida was increasing with lake trophic state expressed as
TSISD-CHL. The relationship was exponential
and similar in dimictic and polymictic lakes
(Fig. 2). The lowest cyclopoid biomass was
found in two mesotrophic lakes situated in
the northern part of the Great Masurian
Lakes system, i.e. Lake Przystań (0.007 mg l–1)
and Lake Mamry Małe (0.001 mg l–1). The
highest biomass (2.34 mg 1–l) was observed
in the years 1991 and 1994 in the dimictic Lake Niegocin receiving waste waters
(after mechanical treatment) from a town
Giżycko and in the polymictic Lake Sasek
Mały (5.04 mg l–1). The relationships between
TSISDCHL and cyclopoid biomass were nearly
564
Jolanta Ejsmont-Karabin, Andrzej Karabin†
Table 1. Morphometric characteristics of the study lakes of northeastern Poland (Brodzińska et al. 1999)
and the values (or the range ) of Secchi’s disc visibility (SD), concentrations of chlorophyll a (Chl a) and
total phosphorus (TP). Data for epilimnion, midsummer period.
Lake
(local name)
Dimictic lakes
Bełdany
Białe (Krutyńskie)
Białoławki
Czos
Dargin
Dobskie
Ełckie
Gim
Gromskie
Guzianka Wielka
Jaczno
Jagodne
Juno
Kamenduł
Kierzlińskie
Kisajno
Kojle
Kopane
Kuc
Lampackie
Lampasz
Lidzbarskie
Mamry
Maróz
Mikołajskie
Mokre
Nidzkie
Niegocin
Ołów
Piłakno
Probarskie
Ryńskie
Rzeckie
Sarż
Szurpiły
Święcajty
Tajty
Tałtowisko
Tałty
Tyrkło
Zyzdrój Wielki
Polimictic lakes
Barlewickie
Bądze
Brajnickie
Burgale
Hartowieckie
Surface area
(ha)
Mean depth
(m)
Maximum
depth
(m)
SD
(m)
Chl a
(μg l–1)
TP
(µg l–1)
940.6
341.0
211.1
279.1
3030.0
1776.0
382.4
10.0
7.3
9.8
11.1
10.6
7.8
15.0
46.0
31.0
36.1
42.6
37.6
22.5
55.8
0.8–1.0
1.8
2.2–2.8
1.6
2.5–4.2
2.6–3.8
1.6
19.4–21.8
50.0
20.8–24.6
10.8
1.1–14.8
3.6–11.0
46.7
50–71
50
30–40
68
30–88
46–60
202
175.9
7.6
25.8
5.8
5.5
43
240.0
59.6
41.0
942.7
380.7
25.5
92.8
1896.0
16.1
14.5
98.8
198.6
88.2
121.8
2504.0
332.5
497.9
841.0
1818.0
2600.0
61.4
259.0
201.4
670.8
59.0
76.7
80.9
869.4
265.1
326.9
1160.4
236.1
210.0
5.8
6.5
11.7
8.7
11.9
6.8
11.7
8.4
10.9
7.3
8.0
11.1
4.8
10.1
11.9
11.9
11.2
12.7
6.2
10.0
12.9
13.0
9.2
10.0
6.8
5.9
10.0
8.7
7.5
14.0
15.6
9.7
4.8
15.8
25.5
29.6
37.4
33.0
24.5
44.5
25.0
27.5
17.4
28.0
38.5
21.7
25.5
43.8
41.0
25.9
51.0
23.7
39.7
40.1
56.6
31.0
50.8
29.0
15.0
46.2
28.0
34.0
39.5
44.7
29.2
14.5
2.8
2.0
4.0
0.5–1.2
1.2
2.7
6.9
2.5–3.8
5.3
3.0
5.4
1.3–3.0
2.2
1.0
4.3–5.5
2.1
0.9–1.8
1.9
1.3–2.0
0.8–2.8
3.8
6.4
51.
0.5–1.3
0.9
3.6
6.0
1.5–4.0
2.2
0.6–1.2
0.7–2.4
0.7–1.3
2.8
5.4
8.9
2.9
31.4–258.6
32.8
5.5
2.6
4.0–11.6
2.9
4.8
2.9
10.0–11.1
24.0
61.0
2.8–9.7
9.2
8.7–116.6
15.0
5.3–22.7
7.8–40.5
3.4
1.5
1.1
20.2–61.6
20.9
3.5
3.0
1.1–18.1
5.7
7.4–34.3
20.8–54.6
18.1–38.9
11
66
60
44
92–190
175
88
38
42–78
30
40
40
73–165
95
222
35–50
44
51–320
210
45–110
120–515
30
20
38
50–122
87
31
44
58–97
55
54–385
36–191
60–72
100
63.7
149.9
186.3
79.0
68.6
4.2
2.9
2.7
4.6
2.7
8.5
6.7
5.2
7.4
5.2
0.6
0.5
0.6
1.4
0.9
74.7
35.4
89.3
15.8
19.6
940
141
157
740
176
Crustacean trophic state index for lakes
Lake
(local name)
Surface area
(ha)
Mean depth
(m)
Iławskie
Iłgieł
Jegliniszki
Kirsajty
Kok
Kołowin
Kotek
Liwieniec
Łabap
Mój
Pobondzie
Postawelek
Przechodnie
Rańskie
Sambród
Sasek Mały
Sędańskie
Siercze
Skanda
Spychowskie
Stryjewskie
Szymon
Tuchel
Tuchlin
Udziejek
Warpuńskie
Wistuć
Wiżajny
154.5
17.1
16.0
207.0
37.2
78.2
19.1
81.2
ca. 364
116.5
53.1
3.4
25.4
291.3
128.4
319.1
168.5
55.4
51.1
48.8
67.5
154.0
42.7
219.3
6.1
49.0
18.3
293.1
1.1
4.1
1.2
3.2
3.3
4.0
1.6
1.2
2.4
3.6
2.6
3.3
3.8
1.9
1.6
2.6
1.0
5.8
2.3
2.6
1.1
2.7
2.8
3.8
2.6
1.3
2.6
Maximum
depth
(m)
2.8
9.7
2.4
5.8
11.8
7.2
3.2
4.1
4.1
13.4
10.0
5.4
6.3
7.8
4.3
3.7
6.1
2.0
12.0
7.7
6.2
2.9
5.1
4.9
7.2
6.9
2.4
5.3
the same for polymictic and dimictic lakes
(Fig. 2, Table 2), thus correlation coefficients
(after logarithmic transformation of biomass values) were not different statistically
(polymictic: n=41; r = 0.49; dimictic: n = 88,
r = 0.58; P = 0.52). As a consequence, TSICR2
may be established from the same formula for
both dimictic and polymictic lakes (Table 3).
3.3. The contribution of the biomass
(wet weight) of Cyclopoida to the
total crustacean biomass
The relationship between the percent
share of Cyclopoida in the total biomass of
Crustacea and TSISD-CHL is positive, exponential and significant in dimictic lakes. In polymictic lakes the relationship is markedly less
significant (Fig. 3). The lowest contribution
of cyclopoids to the total crustacean biomass
(<1%) was found in mesotrophic lakes: Lake
565
SD
(m)
Chl a
(μg l–1)
TP
(µg l–1)
0.3
2.3
2.0
2.5
1.1
2.4
0.5
0.4
3.2
0.9
1.7
1.6
1.5
1.4
0.5
1.1
1.3
1.6
4.6
2.1
0.7
0.4–0.8
0.6
0.8–1.2
1.9
0.5
0.7
1.0
44.7
10.7
9.9
4.9
18.3
3.6
63.8
42.1
2.5
20.6
18.3
14.1
24.0
17.7
60.1
39.3
21.5
11.8
10.4
19.0
46.2
24.5–156.1
182,3
8.1–14.3
38.7
14.6
36.3
31.0
420
232
40
53
147
53
103
321
103
80
60
32
48
92
161
142
90
84
44
125
160
86–191
357
22–67
48
134
96
88
Dargin and Lake Mamry Małe, whereas the
highest one (82 and 89%, respectively) in the
highly eutrophic and dimictic Lake Ryńskie
and the meso-eutrophic, polymictic Lake
Jegliniszki. Despite of the differences between correlation coefficients, the relationships between TSISDCHL and crustacean numbers were similar for both mictic types of the
studied lakes (Fig. 3, Table 2) as correlation
coefficients were not different statistically
(polymictic: n=40; r = 0.41; dimictic: n = 88,
r = 0.61; P = 0.15). Thus, TSICR3 may be established from the same formula for dimictic
and polymictic lakes (Table 3).
3.4. The ratio of the biomass of Cyclopoida
to the biomass of Cladocera
The ratio of Cyclopoida to Cladocera
biomass is apparently related to the trophic
status of lake waters (Fig. 4), however the
566
Jolanta Ejsmont-Karabin, Andrzej Karabin†
Table 2. Formulas which enable to assess trophic state of dimictic and polymictic lakes (TSICR) from
parameters of abundance and structure of crustacean communities
Parameter
Numbers of Crustacea
(N, ind. l–1)
Biomass of Cyclopoida
(B, mg w.wt. l–1)
Percentage of cyclopoid biomass in
total biomass of Crustacea (CB, %)
Ratio of the cyclopoid biomass to the
biomass of Cladocera (CY/CL)
Ratio of biomass to numbers (B:N,
mg w.wt. ind.–1)
Ratio of Cladocera to Calanoida
numbers (CL/CA)
Ratio of Cyclopoida to Calanoida
numbers (CY/CA)
Percentage of species indicative of
high trophy in the indicative group’s
numbers (IHT, %)
Formulas and regression coefficients
DIMICTIC LAKES
POLYMICTIC LAKES
TSICR1 = 6.76 Ln(N) + 18.4
TSICR1 = 6.89 Ln(N) + 20.7
R2 = 0.27
R2 = 0.21
TSICR2 = 4.05 Ln(B) + 57.4
TSICR2 = 3.48 Ln(B) + 60.2
R2 = 0.35
R2 = 0.24
TSICR3 = 5.53 Ln(CB) + 38.1
TSICR3 = 3.08 Ln(CB) + 49.4
R2 = 0.37
R2 = 0.16
TSICR4 = 4.05 Ln(CY/CL) + 58.2
TSICR4 = 2.34 Ln(CY/CL) + 60.8
R2 = 0.32
R2 = 0.16
TSICR5 = 23.8 – 6.94 Ln(B:N)
TSICR5 = 52.5 – 1.55 Ln(B:N)
R2 = 0.20
R2 = 0.02
=
TSICR6 = 3.84 Ln(CL/CA) + 50.6
TSICR6 0.41 Ln(CL/CA) + 59.2
R2 = 0.24
R2 = 0.01
TSICR7 = 5.08 Ln(CY/CA) + 46.6
TSICR7 = 1.18 Ln(CY/CA) + 56.6
R2 = 0.37
R2 = 0.03
TSICR8 = 33.0 (IHT)0.128
R2 = 0.33
significance of the relationship is markedly
higher for dimictic than polymictic lakes.
The lowest values of the ratio were observed
in the dimictic Lake Dargin (0.002) and the
polymictic Lake Mamry Małe (0.0004). Crustacean zooplankton was dominated in the
former by large species of Cladocera from
the genus Daphnia, whereas Cyclopoida
were represented by a few nauplii. Similar
taxonomic composition was also observed in
Lake Mamry Małe, although besides of large
Daphnia quite numerous were also Bosmina
berolinensis. The highest values were found
for the dimictic Lake Mikołajskie (24.741)
and the polymictic Lake Jegliniszki (8.205).
Crustacean community in both the lakes
was dominated by species of the genus Mesocyclops. The regression analysis for the ratio of the cyclopoid biomass to the biomass
of Cladocera and TSISD-CHL indicated a negative and statistically significant relationship
of an exponential character in both dimictic
and polymictic lakes. The relationships established separately for dimictic and polymictic
lakes were nearly identical (Fig. 4, Table 2).
Their correlation coefficients (after logarithmic transformation of number values) were
not different statistically (polymictic: n = 41;
r = 0.39; dimictic: n = 88, r = 0.56; P = 0.26)
and TSICR4 may be established from the same
formula for both types of lake mixis (Table 3).
TSICR8 = 44.9 IHT0.067
R2 = 0.25
3.5. The biomass to numbers
ratio in Crustacea
The biomass to numbers ratio is rather
weakly related to the trophic status of dimictic lakes and not related in polymictic ones
(Fig. 5). The lowest values of the ratio were
observed in the dimictic Lake Mikołajskie
(0.0017 mg w.wt. ind.–1) and the polymictic
Lake Jegliniszki (0.0004 mg w.wt. ind.–1). Crus-
Fig. 1. The relationship between the trophic state
of dimictic (n = 88, white circles) and polymictic
(n=41, black circles) lakes and the total numbers
of Crustacea (ind. l–1).
Crustacean trophic state index for lakes
tacean communities in both lakes were dominated by nauplii of copepods: Th. oithonoides
in Lake Mikołajskie, and M. leuckartii in Lake
Jegliniszki. The highest values were found for
the dimictic Lake Mamry (0.1079 mg w.wt.
ind.–1) and the polymictic Lake Mamry Małe
(0.1410 mg w.wt. ind.–1). In both these lakes
strong domination of adult Daphnia cucullata
was observed. The regression analysis for the
mean body volume and TSISD-CHL showed a
negative and significant relationship of an exponential character in dimictic lakes, whereas
in polymictic ones the relationship was statistically insignificant (Fig. 5). The regression
calculated for the total data of both types of
lakes was very weak. Thus it was not accepted
for the purposes of this work.
567
(after logarithmic transformation of number
values) for both groups of lakes were different statistically (polymictic: n = 33; r = 0.08;
dimictic: n = 82, r = 0.49; P = 0.04).
3.7. The ratio of the numbers of
Cyclopoida to the numbers of Calanoida
Similarly to the ratio of Cladocera to
Calanoida numbers, also the ratio of Cyclop-
3.6. The ratio of the numbers of Cladocera
to the numbers of Calanoida
The ratio of Cladocera to Calanoida numbers is related to the trophic status of lake
waters in a case of dimictic lakes, whereas
in polymictic ones the relationship does not
seem to exist (Fig. 6). The lowest values of the
ratio were noted in the dimictic Lake Dargin
(0.12) and the polymictic Lake Bądze (0.04).
Crustacea in the former lake were dominated by the calanoid, Eudiaptomus graciloides
(Lill.), which density was 82% of the total
crustacean numbers. Taxonomic composition
of the community in Lake Bądze was different. Although E. graciloides was there abundant as well, the community was dominated
by Mesocyclops leuckartii, and Cladocera were
scarce. The highest values were found for
the dimictic Lake Sztumskie (29.4) and the
polymictic Lake Sambród (64.5). Crustacean
community in the former lake was dominated by Daphnia cucucullata, which constituted
80% of the total crustacean numbers and 91%
of the community biomass. The community
in Lake Sambród was dominated by Bosmina
longirostris (48% of the community numbers
and 76% for biomass). The regression analysis for the ratio of Cladocera to Calanoida
numbers and TSISD-CHL, done for dimictic
lakes, indicated the relationship of an exponential character (Fig. 6). In polymictic lakes
there was not any relationship between the
ratio of Cladocera to Calanoida numbers and
TSISD-CHL. As a result correlation coefficients
Fig. 2. The relationship between the trophic state
of dimictic (n = 88, white circles) and polymictic
(n = 41, black circles) lakes and the total biomass
of Cyclopoida (mg l–1).
Fig. 3. The relationship between the trophic state
of dimictic (n = 88, white circles) and polymictic
(n = 41, black circles) lakes and the contribution
of the biomass of Cyclopidae to the total crustacean biomass.
568
Jolanta Ejsmont-Karabin, Andrzej Karabin†
Table 3. Formulas which enable to assess trophic state of lakes regardless of their mixis type (TSICR) from
parameters of abundance and structure of crustacean communities
Regression
coefficient
Formulas
Numbers of Crustacea (N, ind. l–1)
R2 = 0.32
TSICR1 = 25.5 N0.142
Biomass of Cyclopoida
(B, mg w.wt. l–1)
R2 = 0.37
TSICR2 = 57.6 B0.081
Percentage of cyclopoid biomass in the total biomass of Crustacea (CB, %)
R2 = 0.35
TSICR3 = 40.9 CB0.097
Ratio of the cyclopoid biomass to the biomass of
Cladocera (CY/CL)
R2 = 0.30
TSICR4 = 58.3 (CY/CL)0.071
Ratio of Cyclopoida to Calanoida numbers (CY/
CA) (for dimictic lakes)
R2 = 0,37
TSICR7 = 5.08 Ln(CY/CA) + 46.6
Percentage of species indicative of high trophy in
the indicative group’s numbers (IHT, %)
R2 = 0.30
TSICR8 = 43.8 e0.004 (IHT)
Parameter
oida to Calanoida numbers is in 37% dependent on the trophic status of dimictic lakes,
whereas there is a lack of the relationship
in the polymictic ones (Fig. 7). The lowest
value of the ratio was found in the dimictic
Lake Dargin (0.06), and the highest one in
the polymictic Lake Krajwelek (128.20). In
the former lake the calanoid, Eudiaptomus
graciloides, was very abundant, whereas cyclopoids were represented by a few nauplii.
In Lake Krajwelek three species of Cyclopoida were found in high densities (dominating Thermocyclops oithonoides, M. crassus
and M. leuckartii), whereas E. graciloides was
scarce there. The regression analysis for the
ratio of Cyclopoida to Calanoida numbers
and TSISD-CHL, indicated the relationship of
an exponential character for dimictic lakes
(Fig. 4), whereas in polymictic lakes the ratio was not correlated with the index (Fig. 7).
As correlation coefficients for both groups of
lakes were different statistically (polymictic:
n = 34; r = 0.17; dimictic: n = 81, r = 0.61;
P = 0.01) and only dimictic lakes had significant relationship between ratio of Cyclopoida
to Calanoida numbers and TSISD-CHL the index
TSICRU7 should be established only for dimictic lakes (Table 3).3.8. The percentage of species indicative of high trophy in the indicative
group’s numbers
Fig. 4. The relationship between the trophic state
of dimictic (n = 88, white circles) and polymictic
(n = 41, black circles) lakes and the ratio of the
cyclopoid biomass to the biomass of Cladocera.
Fig. 5. The relationship between the trophic state
of dimictic (n=88, white circles) and polymictic
(n = 41, black circles) lakes and the biomass to
numbers ratio in the community of Crustacea.
Crustacean trophic state index for lakes
Fig. 6. The relationship between the trophic state of
dimictic (n=82, white circles) and polymictic (n =
33, black circles) lakes and the ratio of the numbers of Cladocera to the numbers of Calanoida.
The percentage contribution of the crustacean species increasing along the gradient of
lake eutrophication (i.e. Mesocyclops leuckarti,
Th. oithonoides, Diaphanosoma brachyurum,
Chydorus sphaericus, Bosmina (E.) coregoni thersites, Bosmina longirostris), to the total numbers
of Crustacea, indicating both high and low trophy (i.e. additionally, Heterocope appendiculata,
Bosmina berolinensis, Bythotrephes longimanus,
Daphnia galeata, D. cristata, D. cucullata) seems
to be relatively sensitive index of the trophic status of lakes (Fig. 8). Unfortunately, it cannot be
used for the lakes devoid of any of the two ecological groups of Crustacea.
The regression analysis for the percentage
of species indicative of high trophy in the indicative group’s numbers and trophy of lakes,
indicated the relationship described by power
functions for both dimictic and polymictic
lakes (Fig. 4). As correlation coefficients for
both groups of lakes were not different statistically (polymictic: n = 37; r = 0.50; dimictic: n = 87, r = 0.58; P = 0.58), TSICR8 may be
established from the same formula for both
groups of lakes (Table 3).
3.9. Final statements
From among above-mentioned crustacean indices, six were the best correlated with
trophic state of lakes estimated on Secchi’s
disc transparency and chlorophyll a concen-
569
Fig. 7. The relationship between the trophic state
of dimictic (n = 81, white circles) and polymictic
(n = 34, black circles) lakes and the ratio of the numbers of Cyclopoida to the numbers of Calanoida.
Fig. 8. The relationship between the trophic state
of dimictic (n = 87, white circles) and polymictic
(n = 37, black circles) lakes and the percentage of
species indicative of high trophy in the indicative
group’s numbers
trations. These were indices based on: (i) total
numbers of Crustacea; (ii) total biomass of
Crustacea; (iii) contribution of the biomass of
Cyclopidae to the total crustacean biomass;
(iv) ratio of the cyclopoid biomass to the biomass of Cladocera; (v) ratio of Cyclopoida
numbers to the numbers of Calanoida; (the
relationship covering exclusively dimictic
lakes); (vi) percentage of species indicating
high trophy in the total numbers of all species
within the indicative group (Table 3).
570
Jolanta Ejsmont-Karabin, Andrzej Karabin†
4. DISCUSSION
According to Jumpp anen (1976), the
effects of rapid eutrophication first concern
the primary consumers, but finally extend to
the entire food chain. He concluded that the
herbivorous zooplankters are a particularly
weak link in the food chain. Thus their declining role as consumers is taken over by the
decomposers. This may explain why detritobacteriophagous rotifers are good indicators
of high trophy (Ejsmont-Karabi n 2012),
whereas crustaceans seem to respond weaker
to changes in trophic status of their habitat. It
may also explain results of Č eirāns’s (2007)
studies. The author, basing on studies done
in the years 1998–2004 in 113 lakes of different trophic type, suggested that there were no
good low trophy indicators among zooplankton taxa. However, in his studies, a number of
taxa increased in abundance with eutrophication.
Some discrepancies between Carlson’s,
rotifer and crustacean indices may be expected for many reasons. The most serious
source of the difference may be an impact of
fish on crustacean zooplankton. Drenner et
al. (1996) have shown that filter-feeding fish
interact synergistically with trophic state of
lakes so that the ecological effects of omnivorous fish increases with increased eutrophication. The suggestion that fish have a significant structuring role in eutrophic lakes was
supported by data from three lakes in which
major changes in the abundance of planktivorous fish occurred following fish kill or fish
manipulation. A reduction in planktivores
in the lakes resulted in an increase in cladoceran mean size (Jepp es en et al. 2000). On
the other hand, Karabin (1985b), studying zooplankton of 64 lakes, showed that
the pressure of planktivorous fish was not a
factor determining changes in selected structure parameters of the crustacean communities. According to the results of his research,
biomass and composition of phytoplankton
played a significant role in the determination
of changes in numbers, biomass and species
structure of Crustacea in the course of lake
eutrophication. However, if the impact of fish
acts synergically with increasing trophic status of a lake, then it would be rather difficult
to recognize it.
Additionally, crustacean zooplankton is
able to avoid visual predators through vertical
migration to aphotic zone (Gl iw i c z 1986,
L amp e r t 1993). This phenomenon should
have a strong impact on species structure of
zooplankton sampled from epilimnion during day hours. This may explain a strong difference between dimictic and polimictic lakes
as regards crustacean indices of trophic status
of the lakes. Such difference was not observed
for rotifers (Ej s mont - Kar abi n 2012).
The relationships between the crustacean
indices and TSISD-CHL was always less significant in shallow lakes than in dimictic ones.
Two reasons for the differences may be taken
into consideration: abundance and structure
of crustacean communities changing in different way along eutrophication process or
differences in the processes of eutrophication
themselves. Shallow lakes change between
two contrasting ecosystem states: they may
be very clear and overgrown with macrophytes, or very turbid due to high content of
seston (S che f fe r 2001). In the course of the
eutrophication process in these lakes, gradual
enrichment starting from low nutrient levels
causes increasing turbidity until the critical
level at which macrophytes disappear. Thus,
also changes in zooplankton of the lakes may
be rapid if they follow the changes between
the two contrasting states.
As regards community of Crustacea, the
most important difference between the two
mictic types of lakes is that Cladocera in shallow lakes have no good pelagic refuge (Irv i ne et al. 1990) against predators, which
in stratified lakes is created by dark waters
below trophogenic zone. For this reason, perhaps, the indices based on presence of Cladocera (except one, i.e. ratio of the cyclopoid
biomass to the biomass of Cladocera, See
Table 3) cannot be used for shallow lakes and
are rather weak in dimictic ones. This is also
confirmed by Jepp e s e n et al. (2003) who
found in their study in 466 lakes that predator control on large-bodied zooplankton is
generally higher in shallow than deep lakes.
Shallow lakes covered with macrophytes may,
however, offer another type of refuge, i.e.
dense stands of macrophytes. Even if large
Daphnia are eliminated in these lakes by fish,
macrophyte-associated species such as Ceriodaphnia sp. and Simocephalus sp. appear to
Crustacean trophic state index for lakes
replace them (St ansf ield et al. 1997). This
makes shallow lakes even less predictable as
regards changes in taxonomic composition of
their crustacean communities due to changes
in trophic status of the lakes.
In the scenario of crustacean response to
eutrophication a very important role is played
by rapid shift from relatively low abundance of
diatoms and green algae into high blooms of
Cyanoprokaryota. It is well known that high
concentrations of filamentous forms may affect the nutrition of cladocerans (Webster
and Peters 1978, Gliw icz and L amp er t
1990) by clogging the animal’s filtering apparatus, which reduce the rate of food capture,
increases energy expenditure and thus decreases growth and reproduction (Por ter and
McD onoug h 1984). Thus, in lakes with high
production of Cyanoprokaryota, Cladocera
are more affected than copepods or rotifers.
Some regional differences may be expected as regards taxonomic groups and species
considered to indicate low and high trophic
status in lakes. As an example, although calanoids in general seem to decline with increasing trophic status of lakes (Pat a l as 1972,
Pi nto -C o el ho et al. 2005b), this generalisation does not apply to lakes in New Zealand
(Hane y 1987). In New Zealand’s lakes grazing on colonial cyanobacteria by zooplankton
appears to be an important trophic link and
calanoid copepods seem to be best adapted
to utilising large cyanobacteria. Thus, a list of
indicatory species can be severely determined
by regional specificity (Bl anche r 1984). In
contrast to the results of the studies by Kar abin (1985a), Bl ancher (1984) found that
within Florida lakes the more oligotrophic
systems were dominated by copepods.
From among species considered as good
indicators of low trophy, Bythotrephes longimanus is given the same indicative role by
Ha k kar i (1972), Heterocope appendiculata
by Pejler (1965), Daphnia galeata and D.
cristata by B erzins and B er t i lss on (1989)
and Pejler (1965). Daphnia cucullata, the
species indicative of low trophy in Kar abi n’s
studies (1985a), is treated by Pe j l e r (1965)
as indicative for eutrophy. From among species listed by Karabin (1985 a) as indicative
of high trophy (i.e. Mesocyclops leuckarti,
Th. oithonoides, Diaphanosoma brachyurum,
Chydorus sphaericus, Bosmina (E.) coregoni
571
thersites, Bosmina longirostris) only few were
given the same role. Chydorus sphaericus is
often described as typical for eutrophy (Ha k k ar i 1972, B e r z i ns and B e r t i lss on 1989).
There are some general statements considering zooplankton response to eutrophication. According to Gu l at i (1983) zooplankton community grazing is high and variable
in lakes of low trophy and low and relatively
constant in lakes of high trophy. He suggests
that the dominance of small cladocerans in
lakes may be due to quality of food and trophic level, besides fish predation.
Even if crustacean indices of trophic state
of lakes are less useful than other biological
indices, they may be recommended in assessing the quality of lake waters. Zooplankton
indices described by Kar abi n (1985a, b)
were successfully used for evaluation of trophic state of lakes: Gardno (Patu re j 2006),
Pełcz (Pi as e ck i and Wolska 2007), Wigry
(Karabi n and Ej s mont- Karabi n 1992)
and several lakes of the Suwałki Landscape
Park (Karabi n and Ej s mont- Karabi n
1993, Jekatierynczuk-Rudczyk et al. 2012).
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Received after revision March 2013