Journal of Plankton Research Vol.22 no.12 pp.2263–2287, 2000
Metazooplankton dynamics and secondary production of Daphnia
magna (Crustacea) in an aerated waste stabilization pond
Henry-Michel Cauchie, Lucien Hoffmann1 and Jean-Pierre Thomé
Université de Liège, Laboratoire d’Ecologie Animale et d’Ecotoxicologie, 22 Quai
Van Beneden, B-4020 Liège and 1Université de Liège, Laboratoire d’Algologie, de
Mycologie et de Systématique Expérimentale, Sart Tilman B22, B-4000 Liège,
Belgium
Abstract. The seasonal dynamics of metazooplankton biomass was monitored in an aerated waste
stabilization pond during three consecutive years (1994–1996). The pond showed a low diversity of
planktonic metazoans because of elevated pH, relatively high concentration of free dissolved
ammonia and low oxygen concentration. The planktonic community was composed of the anomopod
branchiopod Daphnia magna, and the cyclopoid copepods Cyclops vicinus and Cyclops strenuus. Both
predation by cyclopoids and competition with D.magna excluded rotifers from the pond, except
during a short period in spring 1996. Daphnia magna was the dominant organism from a biomass point
of view. In parallel with biomass, demographic parameters, secondary production and the spatial
distribution of D.magna were studied. A significant seasonal and interannual variation in the density,
biomass and production of D.magna was observed. The maximum density of daphnids varied from
264 103 to 686 103 individuals m–2 and the maximum biomass from 4 to 30 g dry weight (DW)
m–2. The annual net production was high compared with the production of Daphnia in natural
environments, ranging from 288 to 593 g DW m–2 year–1. The annual net production of exuviae
accounted for ~25% of the total annual net production. Harvesting of daphnids for commercial applications that took place during the productive period did not have any discernible effect on the population dynamics of D.magna. Sexual reproduction was not observed during the three studied years.
Negative mortality rates, occurring during early spring, however, indicated that recruitment from
ephippia was effective in the pond of Differdange and that sexual reproduction took place before
1994. Swarming was regularly observed in relation to high densities.
Introduction
Waste stabilization ponds are man-made basins used for the extensive treatment
of domestic and agro-industrial waste waters. In such ponds, the organic waste is
degraded by heterotrophic bacteria, leading to a significant reduction of biological
oxygen demand (BOD) and suspended solids (Middlebrooks et al., 1982). Phytoplankton often reach high biomasses in these nutrient-rich waters (Oswald, 1988).
The ponds also often support high biomasses of metazooplankton preying on
bacteria and algae (Sevrin-Reyssac, 1993, 1998; Cauchie et al., 1995, 1999; Canovas
et al., 1996). Brachinoid rotifers and daphnids are the most commonly found
organisms in the waste stabilization ponds. There is a growing commercial interest in these organisms, which are harvested in some waste stabilization ponds to
be used as food for fish in aquaculture (Edwards and Pullin, 1990; Sevrin-Reyssac
et al., 1994).
In spite of this commercial interest and the general interest that limnologists
can have for such extreme environments, little is known about the seasonal
dynamics of metazooplankton in these water bodies, and their biomass and
secondary production have rarely been estimated (Mitchell and Williams, 1982;
Cauchie et al., 1995). The aims of the present study were: (i) to document the
© Oxford University Press 2000
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H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
diversity and seasonal dynamics of metazooplankton in temperate, aerated, waste
stabilization ponds; (ii) to estimate the secondary production of valuable species
such as microcrustaceans in order to evaluate the feasibility of their commercial
exploitation; (iii) to determine the effects of harvesting on the metazooplankton
dynamics. With these aims in view, we characterized the seasonal dynamics of
metazooplankton biomass in a waste stabilization pond with artificial aeration,
located in the Grand-Duchy of Luxembourg. Metazooplankton biomass and the
major physicochemical characteristics of the pond water were monitored fortnightly over three consecutive years. Demographic parameters, daily secondary
production and spatial distribution were analysed in addition to biomass for
Daphnia magna Straus (Crustacea: Branchiopoda), the dominant zooplankter in
the pond. This species was regularly harvested from the pond to be sold as food
for fish. The effects of harvesting on the seasonal dynamics of D.magna were thus
analysed.
Method
Study site
The studied pond is a fishless waste stabilization pond located at Differdange,
Grand-Duchy of Luxembourg (49°32N, 5°55E). It collects the waste waters of
several towns (15 000 inhabitant-equivalents) after conventional primary treatment (coarse screening and decantation). It is a roughly rectangular basin with a
length of ~400 m and a width of ~150 m. The mean and maximum depths are 2.3
and 4.2 m, respectively. Two mechanical aerators provide an oxygen supply of 150
kg O2 h–1 each for 24 h a day. The pond has a complete mixed hydraulic regime
with virtually no short-circuiting or stratification (Cauchie et al., 2000). A small
belt of reed [Phragmites australis (Cav.) Trin. ex Steud.] is present in the shallowest parts of the pond.
Sampling and field measurements
From January 1994 to December 1996, three sites evenly spaced along the
longitudinal axis of the pond were sampled fortnightly 1 h before noon for
zooplankton analysis at four different depths, from the surface to the bottom,
using a 3 l Van Dorn bottle. The dissolved oxygen concentration, temperature
and pH were measured at these stations using an oximeter (WTW oxi 196)
equipped with an oxygen probe and a thermistor, and a pH meter (WTW pH
537), respectively. Measurements were made at a depth of 20 cm, which has
proved to be representative of the mean values throughout the water column
(Cauchie et al., 1999). Water transparency was measured at the three sites using
a Secchi disk.
Surface water was collected in polypropylene flasks at the station near the
outlet of the pond for determining the concentrations of chlorophyll a, particulate organic matter, ammonium nitrogen and soluble reactive phosphorus (SRP),
and for phytoplankton composition analysis. The phytoplankton samples were
immediately fixed with Lugol’s iodine.
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Seasonal dynamics of D.magna in waste stabilization pond
Laboratory procedures
The concentrations of ammonium (NH4+) and SRP were measured, after filtration with 0.2 µm membranes, using a Dionex DX 500 ionic chromatograph system
equipped with an isocratic pump, a conductivity detector and ion-exchange
columns (Dionex IonPac AG 12A and IonPac CG 12A). The concentration of
unionized ammonia (NH3) was determined on the basis of the NH4+ concentration, pH and water temperature according to Rodier et al. (Rodier et al., 1984).
Chlorophyll a concentration was measured spectrophotometrically after extraction with 90% acetone according to Lorenzen (Lorenzen, 1967). The total food
resource for D.magna was estimated from the concentration of particulate
organic matter that is edible by this species (EPOM), i.e. organic solids with a size
between 0.5 and 40 µm (Geller and Müller, 1981). In the laboratory, surface water
samples were filtered with a nylon gauze (mesh size 40 mm) and the filtrate was
collected on a pre-combusted glass fibre filter (pore size 0.5 µm). Glass fibre filters
were oven-dried at 105ºC for 24 h and weighed to estimate the concentration of
edible suspended solids (ESS). The inorganic fraction of ESS was estimated after
incineration in a muffle furnace at 550ºC for 24 h and was subtracted from the
total ESS concentration to give the EPOM concentration.
In the laboratory, the zooplankton samples were filtered through a nylon net
with a mesh size of 60 µm. Live zooplankton were observed using a Leitz inverted
microscope and, if present, rotifers were enumerated and measured to the nearest
10 µm after anaesthesia with carbonated water. Samples were then preserved
with sugar–formalin (Prepas, 1978) for later crustacean identification, enumeration and measurement. Crustaceans were enumerated and measured to the
nearest 50 µm using a Nikon dissecting microscope equipped with a micrometer.
The eggs present in the brood pouch were also enumerated.
The biomass of rotifers was estimated from their biovolumes according to
Ruttner-Kolisko (Ruttner-Kolisko, 1977). Biovolumes were transformed into dry
biomass assuming a conversion factor of 0.1 pg µm–3 (Doohan, 1973). The
biomass of crustaceans was estimated according to McCauley (McCauley, 1984)
as:
j
B = N EG $ W EG + !N i $ W i
(1)
i=1
where NEG and W EG are the density and the mean weight of eggs in the population, respectively. W EG was taken equal to 9.3 mg dry weight (DW) for D.magna
(Trubetskova and Lampert, 1995) and to 0.2 mg DW for Cyclops (Santer, 1993).
Ni and W i are the density and the mean weight of animals in size class i, respectively. W i was estimated from length–weight regressions (LWR). Daphnids used
to establish the LWR were collected in the pond on five occasions (May 1995,
June 1995, July 1995, December 1995 and February 1996). Copepods were
collected in September and October 1995. Animals were killed with 4%
formaldehyde, immediately rinsed with distilled water and measured to the
nearest 10 mm using a dissecting microscope equipped with a micrometer. Body
length of the daphnids was measured from the top of the head to the base of the
2265
H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
tail spine. The body length of copepod nauplii was measured from the top of the
cephalothorax to the end of the abdomen and that of copepodites from the top
of the cephalothorax to the urosome. Daphnia magna females of six different
sizes (0.5, 1.0, 1.5, 2.0, 2.5 and 3.0 mm), nauplii of two different sizes (0.25 and
0.50 mm) and copepodites of five different sizes (0.75, 1.00, 1.25, 1.50 and 1.75
mm) were isolated, freeze–dried and weighed with a Mettler microbalance (sensitivity 10 µg). When present, eggs were removed from females. The number of
animals used per sample was determined, according to their expected weight, in
order to obtain samples with a dry weight of at least 5 mg (1 mg for nauplii).
According to Bird and Prairie (Bird and Prairie, 1985), the relationship between
length (L) and dry weight (W) is described by the equation:
ln W = ln a + (b ln L)
(2)
where ln a and b are dimensionless coefficients determined by a linear regression
analysis.
For the dominant zooplankter D.magna, birth rate (b), death rate (d) and daily
net production were determined. b was estimated as (Paloheimo, 1974):
b=
ln _ E + 1i
D EG
(3)
where E is the average number of eggs per individual in the population and DEG
is the egg development time, taken from Bottrell et al. (Bottrell et al., 1976). The
instantaneous rate of population increase (r) was calculated as:
r = ln N t + Dt - ln N t
Dt
(4)
where Nt and Nt + ∆t are the densities at two consecutive sampling dates t and t +
∆t. The death rate (d) can be estimated as:
d=b–r
(5)
Daily net somatic production rate of D.magna was estimated using the instantaneous growth method (Rigler and Downing, 1984; Kimmerer, 1987) as:
j
P = !g i $ B i
(6)
i=1
where P is the total daily production rate of all size classes together, gi is the mean
daily growth rate for class i and Bi is the biomass of size class i. For each size class,
the daily growth rate is calculated as:
gi=
_ ln W max i - ln W min i i
Di
(7)
where Wmin i and Wmax i are the minimum and maximum mass, respectively, of
the individuals in size class i, and Di is the time spent by the individuals to grow
from Wmin to Wmax of size class i. Di was graphically deduced from growth curves
2266
Seasonal dynamics of D.magna in waste stabilization pond
determined in situ at five key periods of the year, i.e. spring algal bloom, clear
phase, midsummer, autumn and winter. About 20 neonates were put in Plexiglas hook-bent tubes closed with plankton gauze (mesh size 60 µm) (Wattiez,
1979) and incubated at a depth of 50 cm. The animals were measured every 1–2
days.
The daily net production rate of eggs (PEG) was estimated as (Winberg et al.,
1971):
P EG =
_ N EG $ DW EG i
D EG
(8)
where NEG is the egg density, ∆WEG is the weight of the animals at hatching and
DEG is the egg development time. DEG was taken from Bottrell et al. (Bottrell et
al., 1976).
The daily net production rate of exuviae (PEX) was estimated as:
j Ni$ W
$ N EX (i)
EX (i)
P EX =
(9)
Di
!
i=1
where Ni and Di are as in equations (1) and (7), respectively. W EX (i) is the mean
weight of the exuviae produced by the individuals in size class i, NEX(i) is the
number of exuviae produced by the individuals when growing from the lower to
the upper size limit of the size class. W EX (i) was estimated from an LWR established for exuviae (LWEXR) and NEX(i) was determined during the in situ growth
experiments by direct count of the number of exuviae in the tubes. Exuviae used
to established the LWEXR were collected in a laboratory culture of D.magna
(24°C) using Dictyosphaerium ehrenbergianum Nägeli (106 cells ml–1) as food.
Exuviae were grouped according to their length and weighed with a Mettler
microbalance (sensitivity 10 µg). Finally, the relationship between the weight of
the exuviae and body length was determined as for LWR.
The total daily production rate for D.magna was obtained by summing P, PEG
and PEX. Interval production between sampling dates was determined by multiplying the arithmetic mean of daily productions measured at the beginning and
at the end of the interval by the number of days in the interval (Kimmerer, 1987).
Annual production was determined by summing all interval production in each
studied year.
The biomass of D.magna harvested for commercial purposes was estimated on
the basis of the fresh weights of the crops, considering a calculated DW to fresh
weight ratio of 0.07.
The magnitude of the spatial aggregation of D.magna in the waste stabilization
pond of Differdange was measured using the patchiness index (PI) defined by
Lloyd (Lloyd, 1967). PI measures how many times individuals are crowded
compared with a random distribution (Hurlbert, 1990) and was calculated on the
basis of the 12 routine samples (three sites and four depths) as:
J
N
1 K v 2 + n - 1O
PI = d n
(10)
nK n
O
L
P
where µ and 2 are the mean population density and its variance.
2267
H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
The diel spatial migration of D.magna was studied on one occasion (18 July
1995). The pond was sampled twice during that day (01.00–13.00) at 18 sites,
including the three sites sampled routinely. At each sampling site, zooplankton
were collected every metre from the surface to the bottom with a 3 l Van Dorn
bottle. A total of 60 samples were thus collected at each time of the day. Samples
were treated in a similar way to the routine samples (see above).
Principal component analysis (PCA) was used to ordinate sampling dates
according to the zooplankton and physicochemical variables, and to ascertain
relationships between these variables. Data ordinations were performed using
the CANOCO software (ter Braak and Smilauer, 1998). All variables were standardized prior to analysis.
Results
Variations of the physicochemical characteristics of the pond from January 1994
to December 1996 are shown in Figure 1. Water temperature varied from 3.5°C
during winter to 25.3°C during summer. In winter and spring, the dissolved
oxygen concentration varied between 5 and 10 mg O2 l–1. In summer and autumn,
it was often <5 mg O2 l–1 and decreased to <1 mg O2 l–1 in July 1994 and August
1995. No vertical gradient of temperature or oxygen concentration was observed
in the pond as a consequence of the effective water mixing induced by the
mechanical aerators (Cauchie et al., 2000). The artificial aeration also prevented
large diel variations of the oxygen concentration. Unionized ammonia (NH3) was
low during winter, increased during spring and peaked to values around or >1
mg N l–1 in summer. SRP fluctuated between 1.0 and 2.5 mg P l–1 most of the time.
SRP peaked up to 4 mg P l–1 in July 1996. pH ranged from 7.5 to 9.0. From January
1994 to August 1995, high values of chlorophyll a and EPOM [>100 mg l–1 and
>10 mg ash-free dry weight (AFDW) l–1, respectively] alternated with relatively
low values (<0.5 mg l–1 and <2 mg AFDW l–1, respectively). From September 1995
to December 1996, the chlorophyll a concentration was >50 mg l–1 most of the
time and exceeded 200 mg l–1 on two occasions (April–May 1996 and
August–September 1996). From September 1995 to April 1996, EPOM was
constantly >10 mg AFDW l–1. During the remainder of 1996, EPOM peaked in
June (maximum value 21 mg AFDW l–1) and in October (maximum value 18 mg
AFDW l–1). Secchi transparency varied in an inverse way to EPOM. Minimum
values (<0.5 m) were observed from October 1995 to June 1996. Maximum transparency (>2.3 m) was observed in January and April–May 1994. The dominant
algae in the pond were unicellular or colonial, non-motile chlorophytes most of
the time. Phytoflagellates were rarely abundant. Cyanophytes were absent from
the pond and diatoms were only observed in spring.
From January 1994 to December 1996, rotifers were observed sporadically in
the pond of Differdange (Figure 2). In 1994 and 1995, Brachionus rubens briefly
appeared in summer, when its maximum biomass reached ~0.4 g DW m–2. In late
spring 1996, a succession of six rotifer species took place. Rhinoglena frontalis,
observed at the beginning of May, was replaced by Brachionus angularis in June.
Brachionus calyciflorus, B.rubens, Filinia longiseta and Polyarthra remata were
2268
Seasonal dynamics of D.magna in waste stabilization pond
Fig. 1. Seasonal variations in the major physicochemical characteristics of the aerated waste
stabilization pond of Differdange from January 1994 to December 1996. NH3, unionized ammonia
concentration; SRP, soluble reactive phosphorus; EPOM, edible particulate organic matter. In the
graph dealing with chlorophyll a, dominant algae are designated by numbers: 1 = pennate and centric
diatoms, Planktosphaeria sp., Trachelomonas sp.; 2 = Planktosphaeria sp., Tetraedron sp.; 3 = Chlamydomonas sp.; 4 = pennate diatoms, Planktosphaeria sp.; 5 = Tetraedron sp.; 6 = Chlorella sp., Monoraphidium sp., Planktosphaeria sp.; 7 = Cryptomonas sp., Planktosphaeria sp., Scenedesmus sp.; 8 =
Monoraphidium sp.; 9 = Monoraphidium sp., Planktosphaeria sp.; 10 = Trachelomonas sp.,
Scenedesmus sp.; 11 = Closterium sp., Planktosphaeria sp., Monoraphidium sp.
mainly observed in July and August. The total biomass of the rotifer community
reached a maximum of 24.6 g DW m–2 in June, of which B.angularis accounted
for 90%.
Two species of cyclopoid copepods (Cyclops vicinus and Cyclops strenuus)
were observed in the pond from January 1994 to November 1995, from April to
2269
H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
Fig. 2. Seasonal variations in the biomass of rotifers, cyclopoid copepods and D.magna. Abbreviations in the upper panel indicate the dominant rotifer species: Br, Brachionus rubens; Rf, Rhinoglena
frontalis; Ba, Brachionus angularis; Bc, Brachionus calyciflorus; Fl, Filinia longiseta; Pr, Polyarthra
remata. Black and white areas in the middle panel represent the naupliar biomass and copepodite
biomass, respectively. Abbreviations in the copepod biomass panel indicate the dominant cyclopoid
species: Cv, Cyclops vicinus; Cs, Cyclops strenuus.
2270
Seasonal dynamics of D.magna in waste stabilization pond
June 1995 and from August to October 1996 (Figure 2). The relationship between
body length (L) and body weight (W) of Cyclops spp. was successfully described
by a power function (n = 14; r2 = 0.942):
ln W = 1.368 + (2.488 ln L)
The total biomass of copepods did not exceed 0.6 g DW m–2. Adults of C.vicinus
were observed in winter, early spring and autumn 1994, in autumn 1995 and in
late summer 1996. Adults of C.strenuus were observed in spring 1994, spring 1995
and spring 1996. Maximum adult biomass was ~0.4 g DW m–2 in 1994, 0.1 g DW
m–2 in 1995 and 0.2 g DW m–2 in 1996.
Daphnia magna was present in the pond from February 1994 to November 1995
and from late June to December 1996 (Figure 2). The relationship between body
length and body weight of D.magna females was successfully described by a
power function (n = 76; r2 = 0.957):
ln W = 2.276 + (2.512 ln L)
Daphnia magna biomass rarely exceeded a maximum value of 4 g DW m–2 in
1994, but reached up to 10 g DW m–2 in 1995 and 30 g DW m–2 in 1996. Its density
was on the whole higher in 1995 and 1996 than in 1994 (Figure 3). Maximum
density was 264 103 individuals (ind.) m–2 in 1994, 686 103 ind. m–2 in 1995
and 492 103 ind. m–2 in 1996. The birth rate showed a lower interannual variation than population density; it was <0.2 day–1 most of the time. Except from
July to October 1995, when it was constantly >0.15 day–1, the death rate alternated between low values (<0.05 day–1) and relatively high values (~0.2 day–1).
Negative death rates were observed in March, June and November 1994, in
March, July and November 1995, and in June 1996.
The composition of the D.magna population is shown in Figure 4. The proportion of juveniles reached on the whole 50–80% of the population density. Ephippial females were only observed in June–July 1994 and in July 1995. Males were
never observed from January 1994 to December 1996. The median size of individuals was low, varying on the whole between 1 and 2 mm. The maximum size
varied globally from 2 to 4 mm.
Five growth curves were established in situ (Figure 5). The mean water temperature was 7.8, 10.8, 15.6, 20.2 and 23.6°C for experiments A, B, C, D and E, respectively. Survivorship was quite low (17–25 days), mostly because animals suffered
from manipulations during measurements. The growth rate of D.magna varied
significantly among the experiments. In the experiment conducted at a mean
temperature of 7.8°C, animals died before they reached reproduction. At mean
temperatures of 10.8, 15.6, 20.2 and 23.6°C, oldest survivors reached to their fifth,
thirteenth, nineteenth and seventeenth instar, respectively. Growth curves were
almost linear at a mean temperature of 7.8, 10.8 and 15.6°C. At 20.2 and 23.6°C,
growth curves had a sigmoid shape. At 20.2°C, maximum growth rates (i.e. the
steeper length increment per unit time) were observed between the second and
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H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
Fig. 3. Seasonal variations in the population density, birth rate and death rate of D.magna in the
aerated waste stabilization pond of Differdange from January 1994 to December 1996.
the eighth instar. At 23.6°C, they were observed between the sixth and the
eleventh instar.
Seasonal variations in production rates of D.magna were closely related to variations in its density and biomass (Figure 6). Considering somatic and egg production together, daily net production rate of D.magna was >1 g DW m–2 day–1 during
summer 1994, late spring and summer 1995 and summer 1996. Over the 3 years,
a maximum daily net production of 9.6 g DW m–2 day–1 was observed in July 1996.
The linear regression relating the weight of exuviae (WEX; µg) of D.magna to
its body length (L; mm) was also successfully described by a power function
(n = 12; r2 = 0.952) as:
ln WEX = 2.264 + (0.438 ln L)
The daily net production rate of exuviae varied in a very similar way to the
2272
Seasonal dynamics of D.magna in waste stabilization pond
Fig. 4. Upper panel: percentage of juveniles (white areas), adult females (cross-hatched areas) and
ephippial females (black areas). Lower panel: median and maximum size of individuals in the
D.magna population of the aerated waste stabilization pond of Differdange from January 1994 to
December 1996.
daily net production rate of soma and eggs (Figure 6). Maximum values were 0.9
g DW m–2 day–1 in 1994, 2.3 g DW m–2 day–1 in 1995 and 2.7 g DW m–2 day–1 in
1996. The daily net production rate of exuviae represented from 20 to 40% of the
total daily net production. Productivity (i.e. the ratio of daily net production rate
of eggs and soma to biomass) increased steeply during spring (1994 and 1995) or
early spring (1996), was >0.5 day–1 during summer and decreased to low values
(<0.1 day–1) during autumn and winter.
The annual net production rates and productivity of D.magna are presented in
Table I. Total net production reached from 288 to 593 g DW m–2 year–1. The
annual net production rate of exuviae reached on average 25% of the total annual
production rate. Annual productivity (P/B) reached from 152 to 183 year–1.
Harvesting of D.magna for commercial applications mainly took place in
summer 1994, spring and summer 1995, and summer and autumn 1996 (Figure 7).
The biomass collected per harvesting day reached on average 4 kg DW in 1994,
12 kg DW in 1995 and 10 kg DW in 1996 (Figure 7A). It represented <10% of the
total biomass most of the time (Figure 7B) and <50% of the daily net production
rate (somatic + eggs) (Figure 7C), except in autumn 1994, spring 1995 and autumn
1996 when it reached up to 1.5 times the daily net production rate of soma and
eggs during short periods. The annual harvesting intensity was quite low, reaching from 9.0 to 27.3 g DW m–2 year–1 (Table I). This represents from 1.5 to 4.8%
of the total annual production.
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H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
Fig. 5. In situ growth curves of D.magna in the waste stabilization pond of Differdange. Water temperature during growth experiments: (A) 7.8°C; (B) 10.8°C; (C) 15.6°C; (D) 20.2°C; (E) 23.6°C. Arrows
indicate the body length and age of the females at first reproduction. Numbers besides the curves indicate the number of moults between two successive body length measurements.
The seasonal variations in the magnitude of D.magna aggregation in the pond
are shown in Figure 8. Daphnia magna appeared to be mainly crowded in spring
and summer. Aggregation was very high in August 1995 (patchiness index
considering all samples, PI = 3.8) and in July 1996 (PI = 3.3). The spatial distribution of D.magna on 18 July 1995 is shown in Figure 9. The animals were almost
evenly distributed at 01.00 h (PI = 1.6). At 1 p.m., on the contrary, animals were
highly aggregated in the deeper layers of the pond (PI = 3.3). Physicochemical
variables had a spatial distribution not different from a random distribution
(Table II).
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Seasonal dynamics of D.magna in waste stabilization pond
Fig. 6. Seasonal variations in the daily net production rate of soma and eggs, daily net production
rate of exuviae and productivity of D.magna in the aerated waste stabilization pond of Differdange
from January 1994 to December 1996.
Table I. Mean biomass, annual net production rates and annual productivity (P/B) of D.magna and
the intensity of D.magna harvesting in the waste stabilization pond of Differdange
m–2)
Mean biomass (g DW
Annual net production (soma + eggs) (g DW m–2 year–1)
Annual net production (exuviae) (g DW m–2 year–1)
Total annual net production (g DW m–2 year–1)
Annual P/B (year–1)
Harvesting intensity (g DW m–2 year–1)
Harvesting intensity (% of total annual net production)
1994
1995
1996
1.9
220.3
67.5
287.8
151.5
9.0
3.1
3.1
422.5
145.1
567.6
183.1
27.3
4.8
3.3
442.1
150.8
592.9
179.7
9.1
1.5
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H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
Fig. 7. Magnitude of D.magna harvesting by the company Bioplancton in the waste stabilization pond
of Differdange. Harvested biomass is expressed (A) in kilograms of dry weight (DW), (B) as a per
centage of the total biomass of D.magna and (C) as a percentage of the daily net production rate
(soma + eggs) per day.
PCA of the sampling dates on the basis of all physicochemical and biological
variables is shown in Figure 10. The two first principal component axes accounted
together for 58.9% of the total variance. The analysis segregated the sampling
dates into six major groups. The sampling dates of 1996 were clearly separated
from those of 1994 and 1995. Daphnia magna productivity was highly correlated
with water temperature.
Discussion
Similar to most waste stabilization ponds (Dinges, 1973; Canovas et al., 1996), the
pond of Differdange proved to have a low metazoan diversity. Fish and planktonic insects were absent. For most of the year, the planktonic community was
2276
Seasonal dynamics of D.magna in waste stabilization pond
Fig. 8. Seasonal variations of the aggregation of D.magna as measured by the patchiness index (PI).
Fig. 9. Spatial distribution of D.magna density (ind. l–1) in the waste stabilization pond of Differdange
at 01.00 (left panel) and 13.00 h (right panel) on 18 July 1995. PI, patchiness index.
2277
H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
Fig. 10. PCA ordination of the sampling dates. , Winter and early spring 1994 and 1995; , winter
and early spring 1996; •, late spring, late summer and autumn 1994 and 1995; +, late spring 1996; ,
early summer 1994 and 1995, summer 1996; *, autumn 1996.
composed of D.magna and two species of cyclopoid copepods. Rotifers were only
abundant on one occasion. This low diversity resulted from the physiological
intolerance of many aquatic organisms to the peculiar combination of abiotic
conditions found in waste stabilization ponds (mainly high pH and frequent
hypoxia), on one hand, and to the competitive superiority of D.magna under the
conditions observed in the pond on the other hand.
Elevated pH is known to affect zooplankton physiological rates [filtration and
respiration rates (Ivanova, 1969; Ivanova and Klekowski, 1972); sodium balance
(Potts and Fryer, 1979; Nilssen et al., 1984)] and to decrease crustacean diversity
(Hansen et al., 1991; Beklioglu and Moss, 1995). Besides its impact on the ion
transport through cell membranes (Potts and Parry, 1964), the increase of pH
mainly affects organisms through the transformation of harmless NH4+ into the
toxic unionized NH3 (Lampert and Sommer, 1997). The toxicity level of NH3
(LC50) varies widely among aquatic organisms. It lies between 0.1 and 0.7
mg N l–1 for most fish (Flis, 1968; Thurston et al., 1978; Meade, 1985), while it lies
between 1.2 and 3.0 mg N l–1 for D.magna and B.rubens, respectively (Schlüter
and Groeneweg, 1985; United States Environmental Protection Agency, 1985).
2278
Seasonal dynamics of D.magna in waste stabilization pond
Table II. Patchiness index (PI) of the physicochemical variables on 18 July 1995
Variable
1 a.m.
1 p.m.
Water temperature
Dissolved oxygen concentration
NH3 concentration
SRP concentration
pH
Chlorophyll a concentration
EPOM concentration
1.0
1.0
1.1
0.8
0.9
1.1
1.1
1.0
0.9
0.9
1.0
1.1
1.1
1.0
In the pond of Differdange, pH was <8.5 for most of the time despite periodic
significant phytoplankton blooms (Figure 1), probably because the pond water
was well buffered. As a consequence, the NH3 concentration rarely exceeded 1
mg N l–1. On the basis of their sensitivity to NH3, fish were therefore unable to
survive in the pond while crustaceans and rotifers could both potentially develop.
Low oxygen concentrations (<3 mg O2 l–1) also affect the metabolism of many
aquatic organisms (Davis, 1975) including Daphnia (Kring and O’Brien, 1976;
Heisey and Porter, 1977; Kobayashi and Hoshi, 1984; Weider and Lampert, 1985).
Several species like D.magna are, however, able to stabilize their metabolism and
can tolerate anoxia for at least 10 h by the production of haemoglobin (Kobayashi
and Tanaka, 1991; Paul et al., 1997). In cyclopoids, nauplii present a lower resistance to hypoxia than adults (Woodmansee and Grantham, 1961; Chaston, 1969).
This might explain the dynamics of nauplii and copepodite biomass, which
collapsed when the oxygen concentration was <3 mg O2 l–1 (Figure 2) while
D.magna development, reproduction and mortality (Figure 3) were not affected.
Common predators of daphnids and cyclopoid copepods (i.e. planktivorous
fish and insect larvae) were absent from the pond of Differdange. Ducks, which
can exert a non-negligible predation on daphnids in shallow ponds (Dinges,
1973), were also virtually absent, except during their migration periods. However,
their density did not exceed 60 individuals on the pond at a time. Therefore, in
the absence of insect and vertebrate predation, intra-zooplanktonic predation
and competition for resources were probably the major biotic structuring forces
of the planktonic community of Differdange.
Rotifers are highly vulnerable to both predation by cyclopoid copepods
(Williamson, 1983) and competition with Daphnia (Gilbert, 1985, 1988). In Lake
Constance, for instance, Plaßmann et al. estimated that C.vicinus was able to crop
from 30 to 90% of the Synchaeta population during spring (Plaßmann et al., 1997).
On the other hand, there is a significant overlap in the diets of rotifers and
anomopods, and a strong exploitative competition exists between these two
groups of animals (Gilbert, 1985). Generally, anomopods, namely Daphnia
species, are more effective grazers than rotifers and therefore efficiently outcompete them (Lampert and Rothhaupt, 1991). Moreover, small and medium-sized
rotifers are often swept into the branchial chambers of large daphnids and die as
a consequence of mortal damage (MacIsaac and Gilbert, 1989). In the pond of
Differdange, it is possible that daphnids and cyclopoid copepods were able to
2279
H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
suppress rotifers totally. Brachionus rubens was, however, observed during
summer 1994 and 1995 because its epibiotic mode of life allowed it to avoid
mechanical interference with D.magna and predation by cyclopoid copepods
(Iyer and Rao, 1995). In late spring and early summer 1996, rotifers developed
probably because D.magna was not present and cyclopoid biomass was very low.
This mass development of rotifers confirmed their ability to withstand the abiotic
conditions of the pond and that their absence most probably resulted from a
strong inhibition of biotic nature. The exclusion of rotifers in the pond of Differdange was more likely to be due to mechanical interference and copepod predation than to exploitative competition. Edible particulate organic carbon indeed
never decreased below 0.5 mg carbon (C) l–1 (considering a minimum C content
of 40% in seston), i.e. a value higher than the threshold concentration for growth
in most rotifers, which ranges from 0.1 to 0.4 mg C l–1 (Walz, 1997). The possibility of abiotic limitation of rotifer development, due to the presence of
inhibitory chemicals for instance, obviously cannot be excluded, but this issue was
not tested in our study.
Cyclops vicinus and C.strenuus had distinct phenologies. Cyclops vicinus
presented either one generation per year with a peak of adult biomass in autumn
(1995 and 1996), or two generations per year with a peak of adult biomass in late
winter–early spring and another in autumn (1994). Cyclops strenuus was monocyclic with peaks of adult biomass in May–June. The phenologies of these species
were in good agreement with the majority of those reported in the literature
(Zankai, 1984; Einsle, 1988, 1996; Maier, 1990; Adrian, 1997). Contrary to daphnids, cyclopoid copepods have different food requirements according to their
development stages. Nauplii are very inefficient feeders that require phytoflagellates for their development (Santer and van den Bosch, 1994). Their food threshold for growth is high (0.4 mg C l–1) (Santer and van den Bosch, 1994) compared
with that of D.magna, which is <0.02 mg C l–1 (Gliwicz, 1990). Small copepodites
were also found to be mainly herbivorous (Brandl, 1998). Late copepodites and
adults are omnivorous, but diets of rotifers and flagellates were found to increase
their survivorship (Hansen and Santer, 1995) and their egg production (Santer
and van den Bosch, 1994).
In the pond of Differdange, algae were not present throughout the year in 1994
and 1995, and phytoflagellates were rarely abundant. However, despite these a
priori unfavourable conditions, naupliar biomass often peaked when the chlorophyll a concentration was virtually nil. This suggests that heterotrophic flagellates, which were potentially very abundant in this bacteria-rich medium, could
also be an adequate food resource for Cyclops nauplii. The fluctuations of nauplii
and copepodite biomass did not appear to be highly influenced by D.magna
dynamics, indicating that exploitative competition was weak due to the high
EPOM concentration in the pond. However, the absence of rotifers was certainly
responsible for the globally low adult biomass observed in the pond.
The dynamics of D.magna density, biomass and production appeared to be
largely influenced by water temperature. The population mainly developed above
10°C. In situ growth experiments revealed that the optimum temperature for
growth was around 20°C and the daily production rates were maximum above
2280
Seasonal dynamics of D.magna in waste stabilization pond
this temperature. This strong dependence of D.magna production rates and
biomass on temperature is clearly demonstrated in the PCA presented in Figure
10. Daily productivity was found to be best correlated to water temperature.
Demographic variables of the D.magna population (birth rate, death rate, mean
and median sizes) were weakly correlated with water temperature. The death rate
was negatively correlated with the dissolved oxygen concentration. This indicates
that even if D.magna is potentially able to withstand intermittent oxygen depletion, a part of the population died during hypoxia. The increase in the death rate
during oxygen depletion did not, however, affect the population dynamics of
D.magna significantly because it was concurrent with an increase in the birth rate.
As for the death rate, D.magna birth rate increased subsequently to the increase
in of the mean and maximum sizes of animals in the population. Indeed, large
females bear more eggs than small ones. The birth rate therefore increased significantly when the females were able to reach large size.
Harvesting of daphnids by the company Bioplancton had no discernible effects
on the dynamics of density, biomass or production. In their study on the mass
cultivation of D.magna on ricebran, De Pauw et al. observed a stimulating effect
of harvests on the reproduction of daphnids (De Pauw et al., 1981). When
decreasing the density from 3000 to 500 ind. l–1, they observed an increase in the
proportion of ovigerous females from 5–10% to 50% within the 2 weeks after
harvesting. No such stimulation of reproduction was observed in the pond of
Differdange because for most of the time the intensity of harvesting was far lower
than in the experiment by De Pauw et al. (De Pauw et al., 1981). In March and
April 1995, when the harvest exceeded the daily production on some days, the
birth rate and the death rate remained low, indicating a weak impact of the cropping on the demography of D.magna. The population did not collapse in these
periods because the harvesting was not continuous, but took place only 4–5 days
a week.
Negative death rates were observed several times over the 3 years, indicating
a regular recruitment of individuals from the sediment ephippia bank. Such
recruitment notably took place in spring when the water temperature increased,
allowing the development of a new population after a period of absence of daphnids from the open water, such as in February 1994 and June 1996. The hatching
of ephippia is induced by an increase in water temperature and their exposure to
the light after a period of cold and dark conditions (Stross, 1987). The combination of cold temperature until the end of March and the persistence of a very
low water transparency until June are therefore likely to be the cause of the late
development of the daphnid population in 1996.
Crowding is known to induce the production of males and sexual, resting eggs
(Hobæk and Larsson, 1990). However, this was not the case in the pond of Differdange. Ephippia formation was very infrequent and was not especially correlated
with periods of crowding. Moreover, males were absent during the studied period
and therefore these eggs were not fertilized. Ephippia are, however, present in
the sediment (H.-M.Cauchie, personal observation) and negative death rates
indicate that they hatch at some periods. The absence of sexual reproduction in
the pond in 1994, 1995 and 1996 therefore remains surprising, all the more
2281
H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
because copulation was observed in 1997 and 1999 (H.-M.Cauchie, personal
observation) when the conditions were similar to those observed in July 1995, for
example.
Swarming and the reduction of the size of females at their first reproduction
are generally considered to be a response of daphnids to fish predation (Lampert,
1993; Young et al., 1994; Mitchell et al., 1995). Both phenomena were observed in
the pond of Differdange. Patchiness increased as population density increased
(Figure 10). Daphnids often stayed in the deeper layer during the day (H.M.Cauchie, personal observation) as they did on 18 July 1995 (Figure 9). The
aggregation of daphnids on that date was not correlated to any heterogeneity in
the physicochemical characteristics of the pond as the PI of all the physicochemical variables was around one (Table II). On the other hand, the size at first reproduction was around 1.5 mm (Figure 5), i.e. significantly lower than most sizes
reported for D.magna in the literature [1.8–3.4 mm (Lampert, 1991; De Meester,
1995; Boersma, 1997; Ebert, 1997)]. Three hypotheses can be proposed to explain
the reduction in the size at first reproduction observed in the pond where fish are
indeed absent. Firstly, fish kairomones, or environmental contaminants such as
pesticides (carbaryl, endosulfan, etc.) that mimic these kairomones (Hanazato
and Dodson, 1992; Barry, 1998), are present in the waste water flowing into the
pond. Secondly, it results from the selection for fast-growing daphnids due to the
constantly renewed high food conditions in the pond. Thirdly, it is a strategy to
avoid predation on eggs by cyclopoid copepods, the largest daphnids being more
vulnerable to this kind of predation than smaller ones (Gliwicz and Umana,
1994).
The total annual net production of D.magna ranged from 288 to 593
g DW m–2 year–1 in the waste stabilization pond of Differdange. These values
include the net production of exuviae that are generally not estimated for freshwater zooplankton. Our results demonstrate, however, that the net production of
exuviae constitutes a large part of the total net production and is therefore worth
estimating, especially in bioenergetic studies dealing with crustaceans. The total
net production by D.magna at Differdange largely exceeded the annual net
production by Daphnia species in temperate and subtropical lakes (Table III),
and the annual secondary production by aquatic insects and crustaceans in
general (Benke, 1993; Cauchie, 1997). The annual net production by Daphnia
indeed varies widely among lakes. Low annual net production values (<10
g DW m–2 year–1) were observed in the subtropical lakes Samsonvale and le Roux
and in the temperate Tjeukemeer. Intermediate values (20–40 g DW m–2 year–1)
were observed in most of the meso-eutrophic lakes, except Farmoor I where the
annual net production was >100 g DW m–2 year–1. Annual production of Daphnia
was high (>130 g DW m–2 year–1) in both studied waste stabilization ponds.
Differences in both top-down (predation pressure) and bottom-up interactions
(food availability) account for the variability in Daphnia production. Lakes with
low Daphnia production were characterized by high predation pressure by fish
(Lake Samsonvale, Tjeukemeer) or by both fish and carnivorous cyclopoids
(Lake le Roux). In lakes with intermediate annual net production values, fish
stocks were generally moderate but daphnids suffered invertebrate predation
2282
Seasonal dynamics of D.magna in waste stabilization pond
Table III. Daphnia production in lentic ecosystems
Species and site
D.barbata
Lake le Roux, South Africa
D.carinata
WSP, Australia
Mean annual Mean
Annual Reference
production
daily P/B P/B
(day)
(year)
(g DW m–2
year–1)
0.1
0.01
28.1
Hart, 1987
139.2
0.15
19.3
Mitchell and Williams,
1982
0.4
–
33.9
Vijverberg and Richter,
1982
35.3
–
23.4
Farmoor, UK
Tjeukemeer, The Netherlands
132.3
5.1
–
–
–
47.0
Queen Mary Reservoir, UK
Lake Constance
D.galeata
Canyon Ferry Reservoir, USA
Lake Esrom, Denmark
Lake Constance
D.gibba
Lake le Roux, South Africa
D.lumholtzi
Lake Samsonvale, Australia
33.8
18.0
–
–
–
11.2
George and Edwards,
1974
Jones et al., 1979
Vijverberg and Richter,
1982
Andrew, 1983
Geller, 1989
20.1
26.5
24.0
–
–
–
–
35.8
26.6
Wright, 1965
Petersen, 1983
Geller, 1989
0.7
0.01
20.0
Hart, 1987
2.8
0.13
33.0
King and Greenwood,
1992
0.36
–
Present study
–
–
Wright, 1965
D.cucullata
Tjeukemeer, The Netherlands
D.hyalina
Eglwys Nynydd, UK
D.magna
WSP, Grand-Duchy of Luxembourg 361.6
D.schodleri
Canyon Ferry Reservoir, USA
40.3
(Lake Esrom, Canyon Ferry Reservoir) or food limitation (Eglwys Nynnyd, Lake
Constance). Death rates imputed to invertebrate predation or starvation are
indeed not significantly lower than those caused by fish predation. However, fish
predation affects annual production more because it lasts almost throughout the
year while predation by Leptodora, Cyclops or Chaoborus is limited to only some
months in the year. On the other hand, fish predation affects mainly large daphnids whose weight increment from one instar to the next is significantly larger
than for small juveniles. In Farmoor I, predators such as adult Cyclops were
almost absent and food conditions were not limiting most of the time. As a result,
the annual production of Daphnia hyalina was higher than in lakes with significant predation pressure, food limitation or both. The situation in the waste
stabilization pond of Gumeracha in Australia was similar to that observed in
Farmoor I. Moreover, the low diversity of the primary consumers in these water
bodies makes inter-specific competition almost non-existent.
2283
H.-M.Cauchie, L.Hoffmann and J.-P.Thomé
Acknowledgements
This study received financial support from Bioplancton s.a. The process for the
production of microcustaceans in aerated sewage lagoons is patented by the
European Patent Office (EP 0 277 482 B1). H.-M.C. acknowledges financial
support from the Belgian Fund for Research in Industry and Agriculture. L.H. is
research associate of the Belgian National Fund for Scientific Research.
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Received on October 24, 1999; accepted on July 27, 2000
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