Hydrobiologia 394: 13–28, 1999.

© 1999 Kluwer Academic Publishers. Printed in the Netherlands.

13

Factors related to autotrophic potamoplankton, heterotrophic protists and

micrometazoan abundance, at two sites in a lowland temperate river
during low water flow

Nicole Lair∗ , Véronique Jacquet & Patricia Reyes-Marchant

Université Blaise Pascal de Clermont-Ferrand II, UPRES A CNRS 6042, Equipe Hydrosystèmes & Bassins
Versants, 63177 Aubière, cedex, France
E-mail: lair@cicsun.univ-bpclermont.fr (∗ author for correspondence)

Received 23 June 1998; in revised form 26 November 1998; accepted 16 December 1998

Key words: potamoplankton, algae, ciliates, heterotrophic flagellates, rotifers

Abstract
The potamoplankton of the Middle Loire was studied every two weeks from June to October 1997, a period of low
water flow. The downstream increase in dissolved oxygen, suspended matter, BOD5 and chlorophyll a, and the
decrease in nutrients were associated with algae growth, principally of chlorophytes and bacillariophytes. Algae
reached maxima of 54 × 106 cells l−1 and 78 × 106 cells l−1 up- and downstream respectively. A large ciliate
community of oligotrichs and peritrichs also developed, with densities up to 24 × 103 cells l−1 upstream and
49 × 103 cells l−1 downstream. These maxima were succeeded by large numbers of heterotrophic flagellates
that reached 690 × 103 cells l−1 upstream following a peak of rotifers, and 2430 × 103 cells l−1 downstream
following the ciliate maximum. Nevertheless, these flagellates constituted only a small proportion of the total
protozoan biomass, which was dominated by ciliates. The autotrophic plankton remains the dominant component
for most of the time, confirming that lowland rivers support significant phytoplankton production. The influence
of anthropic disturbances on rotifer development was debated with regard to the results obtained in previous years.
The maximum rotifers density, due to brachionids and trichocercids reached 3500 ind l−1 upstream and 2750 ind
l−1 downstream, a decrease similar to that observed the previous year. In 1997, addition of suspended matter
was probably responsible for the increase in food levels, which enhanced the development of the predators, thus
illustrating that potamoplankton is largely dependent on trophic relationships and local influences, which highlights
the need for a careful evaluation of all assessment criteria.

Introduction & Gallegos, 1991; Basu & Pick, 1996; Gosselain et

Knowledge of the flow of organic matter circulating
in the food webs is important for our understand-
ing of how river systems function. In lowland rivers,
residence time is long enough for the growth and re-
production of plankton that can be important in the
transfer of organic matter within the food web (Reyn-
olds & Descy, 1996). In such environment, there have
been a large number of algal studies (Lack, 1971;
Peelen, 1975; Lair & Sargos, 1981; Descy, 1987;
Reynolds, 1988; Moss & Balls, 1989; Reynolds et al.,
1994; Basu & Pick, 1997a), but few on rotifers and
crustaceans (Lair, 1980; Pourriot et al., 1982; Dolan
al., 1996). Nevertheless, rotifers can reach large dens-
ities (De Ruyter Van Steveninck et al., 1992; Lair &
Reyes-Marchant, 1997) and represent a key group in
the planktonic food webs of eutrophic running waters,
mainly due to their ability to filter nanoplankton. The
microbial food web, another route to higher trophic
levels, may also be particularly important to the car-
bon and nutrient dynamics of large rivers, due to
their abundance in allochthonous and autochthonous
organic matter. Despite this, the overwhelming major-
ity of studies has been conducted in standing waters,
and protozooplankton in rivers remains poorly doc-
14
umented (Baldock et al., 1983; Carlough & Meyer,
1989, 1990; Gracia et al., 1989; Dolan & Gallegos,
1991; De Ruyter Van Steveninck et al., 1990; Basu &
Pick, 1997b).
The Middle Loire was chosen as a model to de-
termine the proportionate role of protozooplankton
in community dynamic, in relation to that of plank-
tonic algae and rotifers. In this zone, which is used
for cooling reactors, an impact assessment monitor-
ing programme has been carried out since 1976 (Lair
& Sargos, 1993; Lair et al., 1996a). This has shown
that rotifer (Lair & Reyes-Marchant, 1997) and ciliate
(Lair et al., 1998) populations develop in association
with algal growth. In 1997, heterotrophic flagellates
were studied in addition to the two other groups, in
order to determine the importance of the microbial
loop (sensu Azam et al., 1983), in relation to the clas-
sical pathway based on photosynthetic assimilation by
autotrophs.
Sites, materials and methods
Dampierre-en-Burly (D) and Saint-Laurent des Eaux
(SL) are situated in meandering stretches of the river
Loire, at 550 and 640 km from the source (river/stream
order 8) (Figure 1). At each site, samples were col-
lected in the natural meandering and enlarged bed of
the river, from floating platforms situated close to the
riverside. Each station was downstream of a cooling
water discharge. Lair & Reyes-Marchant (1997) gave
more detail of these sites.
The flow was recorded continuously by Electricité
de France. Secchi disk transparency, temperature, dis-
solved oxygen, pH and conductivity were measured in
situ. Routine samples were collected during daylight
hours, at fortnightly intervals, from the 24th of June
to the 7th of October, 1997. Each sample was col-
lected at depths between 0.50 cm and 1.50 m, with
a 10 l vertical Van Dorn bottle. Thirty litres were
mixed together in a large tank and used for chem-
ical and biological analysis. One part was stored in
thermos flasks for the observation of living organisms
on the following day, the other was used for water
analysis and counting of organisms. Triplicates were
immediately preserved, before being stored in the cold
and dark. Algae were acidified with HNO3 (diatoms),
or preserved in Lugols iodine (other algae). Rotifers
were treated with formalin sucrose. Ciliates were fixed
with HgCl2 2.5% final concentration (Sime-Ngando &
Grolière, 1991). Heterotrophic flagellates were pre-
served with glutaraldehyde, 1% final concentration
(Caron, 1983; Bloem & Bär Gilissen, 1988).
The following day, the heterotrophic flagellates
were stained with Trizma-buffered primulin filtered
using 0.8 µm pore black filters, and frozen at −30 ◦ C
(Caron, 1983; Bloem et al., 1986). Flagellates were
measured and analysed after only three weeks, separ-
ated into size classes and considered as a functional
group. For each sample, 500–1000 fields were enu-
merated by epifluorescence microscopy (Olympus BX
40) equipped with an epifluorescence illuminator with
UV and blue light filters and a 100 W mercury lamp.
The biomass was obtained from biovolume (Carlough
& Meyer, 1989) and converted into carbon, assum-
ing 1 µm3 = 220 fg C (Borsheim & Bratback, 1987).
Water samples were analysed by the Municipal Labor-
atory of Clermont-Ferrand, registered by the Ministry
of Health.
The chlorophyll a concentration was measured
spectrophotometrically after 6 h extraction in 90%
ethanol. Ciliates were counted under an inverted mi-
croscope (Leica-Dmil, magnification 200). The ana-
lytical procedures for algae, ciliates and rotifers were
as described by Lair & Reyes-Marchant (1997) and
Lair et al. (1998). After observation of living mater-
ial to facilitate the identification, cyanobacteria, algae
and zooplankton species were determined, measured
and counted, and their biomass was derived from
biovolumes. Ciliates were determined to family and
genus when possible, and classified according to De
Puytorac et al. (1987). They were measured and coun-
ted after only one week, and their biovolume was
converted in carbon, using 1 µm3 = 190 fg C (Put &
Stoecker, 1989).
A Principal Component Analysis (PCA) was car-
ried out using ADE, a software for environmental data
analysis (Chessel & Dolédec, 1992), to examine the
relationships between physical and chemical charac-
teristics and the living communities. Among physical
and chemical variables, we retained accurate measure-
ments of flow, Secchi disk transparency, Suspended
Matter (SM), Conductivity, dissolved Oxygen, Bio-
chemical Oxygen Demand (BOD5 ), Chemical Oxygen
Demand (COD), NO2− 3−
3 and PO4 . We retained the
size classes of the heterotrophic flagellates (HF) and
the principal families of the organisms; “others” in-
cluded the less numerous taxa. Finally we performed
a correlation matrix including all the size classes of
the different taxa. HF were separated into < 5 µm
cells, 5–10 µm cells, 10–25 µm cells and ≥ 25 µm
cells. Algae were divided in < 10 µm cells, 10–20

Figure 1. Map of the river Loire (France), showing locations of the sampling sites.
µm cells, > 20 µm cells, colonies were considered
apart. Ciliates were classed as < 20 µm cells, 20–50
µm cells, > 50 µm cells. Rotifers were categorised
as < 100 µm individuals, 100–200 µm individuals,
> 200 µm individuals, asplanchnids were considered
separately.
Results
Environmental conditions
The study took place during a stable, low water period.
The maximum water discharge, 158 m3 s−1 (D) - 174
m3 s−1 (SL) was registered in July and the minimum,
59 m3 s−1 (D) - 62 m3 s−1 (SL), occurred at the
end of September 1997 (Figure 2). The approximate
travel time between the two sites ranged between 2
and a slightly more than 5 days. Mean Secchi disk
transparencies were 58 cm and 51 cm at the upper
and lower sites, respectively. Water temperature var-
ied from 17.5 ◦ C (June) to 30.5 ◦ C (August) and the
mean values of pH, oxygen, BOD5 , COD and chloro-
phyll a were higher at Saint-Laurent des Eaux than at
Dampierre-en-Burly. In contrast, NO2− 3 , PO4
3− and
SiO2 were lower downstream (Table 1). This illus-
trates the downstream increase in algae in this part of
the Loire, typical of natural and cultural eutrophication
in the course of the river.
15
Phototrophic plankton
Eighty phototrophic species were collected at Dampierre-
en-Burly and 86 at Saint-Laurent des Eaux. The
species of cyanobacteria and algae were identical to
those enumerated in 1995 (Lair & Reyes-Marchant,
1997), and the former were poorly represented.
The more abundant chlorophytes were Actinastrum
hantzschii, Ankistrodesmus mirabilis, Chlorella sp.,
Monoraphidium contortum, M. irregular, M. pusil-
lum, M. saxatile, Sphaerocystis schroeteri, Scene-
desmus spp. (S. dispar, S. quadricauda. . . ) and
different coenobes of Pediastrum. Among the ba-
cillariophytes numerous Cyclotella (C. atomus, C.
glomerata, C. meneghiniana. . . ) plus Fragilaria con-
struens, Aulacoseira granulata var. angustissima were
collected.
As the water moved downstream, the classical in-
crease in algae was observed, they reached maxima
of 54 × 106 cells l−1 and 78 × 106 cells l−1 from
Dampierre-en-Burly to Saint-Laurent des Eaux. The
maximum algal development was observed on the 5th
of August at both sites. The respective means were
32 × 106 cells l−1 and 39 × 106 cells l−1 (Figure 3).
Green algae increased earlier downstream (maximum
59 × 106 cells l−1 , early August), than upstream (max-
imum 38 × 106 cells l−1 , mid-August), as did diatoms
also, with maxima of 14 × 106 cells l−1 in early Oc-
16

Figure 2. Variations in water discharge in the Middle Loire, year 1997.

Table 1. Physical and chemical characteristics of the Middle Loire in 1997

Year 1997 t ◦C pH O2 O2 Secchi SM cond.

(mg/l) (%) (cm) (mg/l) (µS/cm)

Dampierre-en-Burly
mean 24.2 9.2 9.0 111 58 28 295
min 18.9 8.6 6.3 54 50 16 239
max 30.5 9.5 11.9 140 65 36 329

St-Laurent des Eaux

mean 22.0 9.8 9.3 103 51 36 272
min 17.5 8.8 7.1 82 42 21 238
max 25.6 9.5 11.0 116 62 52 311

Cl BOD5 COD NO3 2− N PO4 3− P SiO2 Chl a

(mg/l) (mg/l) (mg/l) (mg/l) (mg/l) (mg/l) (µg/l)

Dampierre-en-Burly
mean 25.7 4.4 32 2.9 0.24 6.2 75.4
min 24.0 3.0 30 1.4 0.09 2.9 30.7
max 28.0 5.0 34 5.2 0.42 10.5 119.8

St-Laurent des Eau

mean 26.6 6.5 34 2.1 0.28 5.7 89.8
min 24.0 4.0 30 1.0 0.06 2.9 50.8
max 29.0 15.0 43 10.0 1.21 9.6 147.6

tober (D) and 15 × 106 cells l−1 at the end of August
(SL) (Figure 4). The diatoms (24% and 19% from up
to downstream) were less abundant than green algae
(65% and 72% respectively). Blue greens were few
(9% at D and 8% at SL), and other algae rare.
The maximum biomass of the phototrophic plank-
ton was 13 × 103 µg. l−1 upstream and 19 × 103
µg.l−1 downstream (Figure 3). The diatom biomass
(mean 53% and 49%, respectively) was higher than
that of the green algae (mean 41% and 45%, respect-
ively) while blue greens were only 5% at both sites,
and other algae ≤ 1%. The diatom biomass was most
important in early July upstream and early October
downstream (Figure 4). Green algae dominated on the
19th of August at the upper site and two weeks earlier
at the lower.

Figure 3. Seasonal patterns of potamoplankton density (algae, 106 cell l−1 ; ciliates & HF 103 cell. l−1 ; rotifers ind l−1 ), and biomass (algae
& rotifers were in µg dry weight l−1 , ciliates & HF in µg C l−1 ) at two sites in the Middle Loire, in 1997.
Heterotrophic protozooplankton
The heterotrophic flagellates (HF) ranged between ≤
5 µm and ≥ 25 µm, the larger sizes being absent
downstream. At both sites, their maxima (690 × 103
cells.l−1 and 2430 × 103 cells l−1 ) were observed on
16th September (D) and 20th August (SL), following
the decrease in density of the other groups (Figure 3).
With means of 257 × 103 cells l−1 (D) and 956 ×
103 cells l−1 (SL) the downstream increase in number
of HF was considerable. In this functional group, most
were nanoplanktonic: cells < 5 µm represented 60.5%
(D) and 65% (SL) of the community by number. Cells
of 5-10 µm accounted for 34% (D) and 32% (SL),
while larger HF were less numerous: cells 10–25 µm
represented 4% (D) and 3% (SL), and cells ≥ 25 µm
were rare (1.5% upstream) or absent (SL).
At Dampierre-en-Burly, the smaller heterotrophic
nanoflagellates (HNF) decreased at the start of the
study, then were rare until September, and peaked
only after the decrease in density of other organisms.
17
The HNF of 5–10 µm followed the same pattern, but
remained few. Larger cells (10–25 µm) peaked suc-
cessively in July and August and on the same dates
as other flagellates (Figure 5). At Saint-Laurent des
Eaux, a different pattern occurred; from the end of
June to mid-August the 10–25 µm cells were dom-
inant, whereas cells of ≤ 5–10 µm represented 95%
of the HF from mid-summer onwards.
The maximum biomass of 25.5 µg C l−1 occurred
in early summer upstream (mean 9.06 µg C l−1 ), and
it was in the same range downstream (mean 8.75 µg
C l−1 ) peaking at 13.70 µg C l−1 in early October.
Some flagellates ≥ 25 µm peaked upstream at the end
of June and in early August. Cells of 10–25 µm pro-
duced the higher biomass upstream (mean 1.70 µg C
l−1 ), while the highest biomass downstream was due
to 5–10 µm cells (mean 4.06 µg C l−1 ) (Figure 5).
Five classes, 19 families and 22 genera of ciliates
were found in the river. The taxonomic composition
was similar to that observed in 1996 (Lair et al.,
1998). Among the Class of Spirotrichea, Euplotes
18

Figure 4. Seasonal pattern of algal density, and distribution patterns of their biomass at two sites in the Middle Loire, in 1997.

Figure 5. Seasonal pattern of heterotrophic flagellates density, and distribution patterns of their biomass at two sites in the Middle Loire, in
1997.

sp., Aspidisca sp., Codonella sp. and among the Or-
der of Oligotrichida Strobilidium sp., Strombidium sp.
and Halteria grandinella were dominant with the Oli-
gohymenophorea, the Peritrichia Vorticella sp. and
Hastatella radians sub-dominant. The Prostomatea
(Askenasia volvox, Didinium sp., Monodinium sp.,
Holophrya sp., Urotricha sp., Amphileptus sp., and
Litonotus sp.), the Heterotrichea (Stentor sp.) and the
Phyllopharyngea (Chilodonella sp., Phascolodon vor-
ticella, Podophrya sp., Acineta sp. and Tokophrya sp.)
and the Nassophorea (Nassula sp.) formed smaller
proportions of the populations. These different taxa
are able to live in standing waters as well as in running
waters (Foissner & Berger, 1996) and most of them
(83%) were between 20 and 50 µm.
At Dampierre-en-Burly the maximum develop-
ment of the ciliates (24.50 × 103 cells l−1 ) was
observed at the start of our study, then after a pro-
gressive decrease they reached a second peak in early
September (Figure 3). A downstream increase in dens-
ity was observed, with means of 12 × 103 cells l−1
(102 µg C l−1 ) and 23 × 103 cells l−1 (128 µg C l−1 )
respectively. Oligotrichs and peritrichs were dominant
and alternated from the end of June to the end of Au-
gust, before growing in parallel. In early September,
with a density of 9160 cells l−1 , the oligotrichs rep-
resented 55.5% of the ciliate community (Figure 6).
At Saint-Laurent des Eaux, the ciliate maximum (49
× 103 cells l−1 ) preceded those of the algae and ro-
tifers (Figure 3). The oligotrichs peaked at 14 410
cells l−1 at Dampierre-en-Burly, and 26 560 cells l−1
at Saint-Laurent des Eaux (with respective means of
41% and 45.5% of total ciliate density from up to
downstream). Their density was higher than that of
peritrichs. Attached ciliates reached maximum dens-
ities of 7110 cells l−1 (D) and 10 650 cells l−1 (SL),
with respective means of 31% and 25.5% of total cili-
ate density. Other ciliates developed populations from
the end of July to early August (Figure 6). With dens-
ities of 26.5% (maximum 5720 cells l−1 ) and 28.5%
(maximum 16 600 cells l−1 ) of total ciliates, they were
represented by several species in low numbers. The
large stentorids represented only 1.5% (D) and 0.5%
(SL) of the total ciliate density.
Ciliate biomass reached maxima of 242 µg C l−1
and 245 µg C l−1 in early August at both sites. There
was a downstream increase in biomass, with respect-
ive means of 102.50 µg Cl−1 and 128.50 µg C l−1
(Figure 3). The peritrich biomass accounted for 37%
and 32% from up to downstream, with maxima of 103
and 153 µg C l−1 respectively, measured in early July
19
at both sites. This was higher than that of oligotrichs
whose maxima reached 24 µg C l−1 (D) at the end
of June and 39 µg C l−1 (SL) at the end of July.
Oligotrichs accounting for 8% and 14% of the cili-
ate biomass respectively. Despite their low abundance,
‘other ciliates’ dominated the community upstream in
early August and downstream at the end of August
(Figure 6). They accounted for 26% (D) and 35% (SL)
of the ciliate biomass. With 29% and 19% of the ciliate
biomass respectively, stentorids peaked upstream in
early July (215 µg C l−1 ), and downstream two weeks
later (120 µg C l−1 ).
Rotifers
The production of numerous small algae supported the
growth of rotifers and among the 13 families repres-
ented, most species were Brachionidae, followed by
Trichocercidae, Lecanidae and Synchaetidae. In 1997,
48 and 45 species were sampled upstream and down-
stream, respectively. They were broadly the same as
described in 1995 (Lair & Reyes-Marchant, 1997), ex-
cept Keratella quadrata, which was absent from the
1997 samples. Upstream the dominant species were
Cephalodella gibba, Trichocerca pusilla, T. brachiura,
T. similis and Brachionus angularis. Downstream, T.
pusilla, C. gibba and Anuraeopsis fissa were the most
numerous.
At the beginning of this study a decrease in rotifer
density was observed at both sites (Figure 3). Later at
Dampierre-en-Burly these small metazoans grew from
the thirtieth of July, simultaneously with the algal de-
velopment. The maximum density of this community
(3500 ind.l−1 ) was recorded on the 19th of August,
after which they declined. At Saint-Laurent des Eaux,
the rotifers increase was shorter, but here also their
maximum abundance (2750 ind l−1 ) followed that of
the algae, and was recorded on the same date as up-
stream. In contrast to the other groups a downstream
decrease in density was observed, with mean densities
of 1415 ind l−1 (D) and 790 ind l−1 (SL) the rotifer
density dropped by 44% downstream.
Except for the asplanchnids, which were more
numerous (maxima 128 ind l−1 and 177 ind l−1 re-
spectively) there, the rotifer increase was shorter at
the lower site. From up to downstream the density
of brachionids corresponded to 35% and 32% of the
total, which was higher than that of trichocercids (26%
at both sites). With maxima of 1610 ind l−1 (D) and
980 ind l−1 (SL), the development of the brachionid
populations was less downstream (Figure 7). The tri-
20
Figure 6. Seasonal pattern of ciliates density, and distribution patterns of their biomass at two sites in the Middle Loire, in 1997.
chocercids peaked earlier downstream than upstream
(960 ind l−1 and 850 ind l−1 ) and their decrease in
density was less pronounced downstream than that of
brachionids. Other rotifers reached maxima of 1030
ind l−1 (D) and 750 ind l−1 (SL) and represented 36%
and 35 % of the total rotifer density, respectively.
The brachionids were the dominant component
(45% upstream and 42% downstream) of the roti-
fer biomass (Figure 7) which reached its maximum
(722 µg.l−1 ) simultaneously at both sites (Figure 3),
but the mean biomass remained lower downstream
(757 µg.l−1 ) than upstream (1198 µg.l−1 ). The tri-
chocercids (24% and 26% upstream and downstream
respectively) were the next largest contributor to the
biomass while other rotifers represented 28 % and
25%. Asplanchnids were a larger proportion of the
biomass at the lower site (3% and 7% respectively).
Multivariate analyses
In the PCA analysis made with the densities of the
different organisms, and the physical and chemical
variables measured at Dampierre-en-Burly, the axes
F1 × F2 explained 53.21% of the total inertia (Fig-
ure 8). Axis 1 brings together “cyanobacteria, t ◦ C,
brachionids, other rotifers, chlorophytes, asplanchnids
& trichocercids”. They are opposed to “chl a, flagel-
lates of size ranging from < 5 µm to ≤ 25 µm &
oligotrichs”. On axis 2, the physical and chemical
characteristics “BOD5 , O2 , pH, Secchi, COD” ad-
ded to “other ciliates & ≥ 25 µm flagellates” (these
taxa were rare), are opposed to “SM, conductivity
& PO4 ”. The significant correlations between the
different components were reported in Table 2.
In the PCA analysis made with data from Saint-
Laurent des Eaux, the axes F1 × F2 explained 64.41%
of the total inertia. Axis 1 brought together “Secchi
disk transparency, other ciliates, 10–25 µm flagel-
lates, BOD5 , brachionids, asplanchnids, other rotifers,
trichocercids, chlorophytes and cyanobacteria”. They
are opposed to SM. On axis 2, the physical and chem-
ical characteristics “pH, O−2” added to “Oligotrichs”,
are opposed to “conductivity, bacillariophytes, PO4 ,
COD and chl a” (Figure 8). The significant correla-
tions between the different components were reported
in Table 2.
The significant correlations extracted of the size
structure analysis were reported in Table 3.
 21

Figure 7. Seasonal pattern of rotifers density, and distribution pattern of their biomass at two sites in the Middle Loire, in 1997.

Figure 8. Situation of the measured variables in the planes of axis F1 × F2 of the PCA.

Discussion ables showed the expected seasonal trend, typical of

General pattern
The period June to October 1997 was characterised
by low discharge and the physical and chemical vari-
eutrophic rivers. The increase in dissolved oxygen,
suspended matter, BOD5 and chlorophyll a were as-
sociated with the downstream decrease in nutrients
(non-depleted), in consequence of the longitudinal
22
Table 2. Significant correlation extracted from the PCA, related to communities

Dampierre-en-Burly Saint-Laurent des Eau

SM & other ciliates −0.654∗ SM & brachionids −0.581∗∗

SM & asplanchnids −0.552∗∗
SM & oligotrichs −0.517∗∗

BOD5 & 10–25 µm HNF +0.584∗∗ BOD5 & brachionids +0.880∗

BOD5 & >25 µm NF +0.518∗∗ BOD5 & trichocercids +0.964∗
BOD5 & other rotifers +0.971∗
BOD5 & asplanchnids +0.835∗
BOD5 & other ciliates +0.647∗

chlorophytes & asplanchnids +0.744∗ chlorophytes & asplanchnids +0.910∗

chlorophytes & brachionids +0.909∗ chlorophytes & brachionids +0.915∗
chlorophytes & trichocercids +0.940∗ chlorophytes & trichocercids +0.821∗
chlorophytes & other rotifers +0.887∗ chlorophytes & other rotifers +0.740∗
chlorophytes & other ciliates +0.619∗

asplanchnids & brachionids +0.856∗ asplanchnids & brachionids +0.987∗

asplanchnids & trichocercids +0.794∗ asplanchnids & trichocercids +0.867∗
asplanchnids & other rotifers +0.926∗ asplanchnids & other rotifers +0.849∗
asplanchnids & other ciliates +0.784∗

5–10 µm HNF & brachionids −0.548∗∗ 10–25 µm HF & brachionids +0.713∗

5–10 µm HNF & trichocercids −0.740∗ 10–25 µm HF & trichocercids +0.858∗
5–10 µm HNF & other rotifers −0.651∗ 10–25 µm HF & other rotifers +0.875∗
< 5 µm HNF & brachionids −0.537∗ 10–25 µm HF & asplanchnids +0.644∗
> 25 µm NF & other ciliates +0.715∗ 10–25 µm HF & other ciliates +0.559∗∗

∗ p = 0.001. ∗∗ p = 0.001∗ .

increase in algal density. The same taxa were col-
lected at both sites, illustrating a continuum of river
processes. This contrasted with quantitative patterns,
which differed between the sites. As in previous years,
algae were more abundant downstream (Lair & Sar-
gos, 1993) and a large rotifer community developed,
parallel to algal growth, but, as in 1996, they decreased
at the lower site in 1997. Heterotrophic flagellates that
peaked after the maxima of algae and rotifers were
much more abundant downstream, and ciliate density
also increased from up to downstream. Their growth
preceded the rotifer increase and they peaked again
after the rotifer maximum, which suggests that exclu-
sion or predation may be operating. Oligotrichs and
peritrichs that grew alternately at both sites were the
most numerous taxa. The maximum abundances of
these components were generally observed two weeks
earlier downstream.
In this large, lowland, nutrient-rich river, and at
this period of the year, green algae were domin-
ant at both sites, followed by centric diatoms, while
blue greens were rare. Indeed, chlorophytes dom-
inated numerically in summer, while diatoms were
dominant in the biomass. This pattern is typical of
the lower courses of temperate rivers (Garnier et al.,
1995), where lowered water discharge increases set-
tling losses of the heavier diatoms (Köhler, 1997). In
such rivers, the density of algae often increases to 100
× 106 cells l−1 (Descy, 1987), and values higher than
200 × 106 cells l−1 have also been recorded in the
Middle Loire (Lair et al., 1996). With 78 × 106 cells
l−1 , the maximum abundance of algae measured in
1997 was lower in comparison with preceding years
under similar climatic conditions.
In the absence of large filter feeders, the Middle
Loire remains among the more rotifer-rich rivers dur-
ing low water flows. In 1997, their density reached
thousands of individuals per litre, which was in the
same range as in 1995–1996. The rotifer community
was also very productive, with a mean rotifer biomass
 23
Table 3. Results extracted from the correlation matrix related to predator-prey size classes

Dampierre-en-Burly Saint-Laurent des Eaux

ciliates <20 µm & HF < 25 µm +0.701∗∗ ciliates <20 µm & HNF 10–25 µm +0.504∗∗∗
ciliates 20–50 µm & HNF 5–10 µm +0.608∗∗∗ ciliates 20–50 µm & HNF <20 µm +0.930∗

rotifers < 100 µ & HNF < 5 µm −0.552∗∗∗ rotifers <100 µm & HNF 10–25 µm +0.833∗
rotifers >200 µm & HNF <5 µm −0.505∗∗∗ rotifers 100–200 µm & HNF 10–25 µm +0.788∗
rotifers >200 µm & HNF 10–25 µm +0.871∗ asplanchnids & HNF 10–25 µm +0.610∗∗∗

rotifers <100 µm & HNF 5–10 µm −0.728∗∗ rotifers <100 µm & ciliates <20 m +0.596∗∗∗
rotifers 100–200 µm & HNF 5–10 µm −0.664∗∗ rotifers 100–200 µm & ciliates <20 m +0.659∗∗
rotifers >200 µm & HNF 5–10 µm −0.702∗∗ rotifers >200 µm & ciliates <20 m +0.727∗∗
asplanchnids & HNF 5–10 µm −0.556∗∗∗ asplanchnids & ciliates <20 m +0.734∗
rotifers >200 µm & ciliates 20–50 µm +0.534∗∗∗
asplanchnids & ciliates 20–50 µm +0.575∗∗∗

rotifers <100 µm & algae <10 µm −0.580∗∗∗ rotifers <100 µm & algae <10 µm +0.787∗
rotifers >200 µm & algae <10 µm −0.592∗∗∗ rotifers 100–200 µm & algae <10 µm +0.723∗∗
rotifers >200 µm & algae <10 µm +0.668∗∗
asplanchnids & algae <10 µm +0.667∗∗

rotifers <100 µm & algae 10–20 µm +0.905∗ rotifers <100 µm & algae 10–20 µm +0.762∗
rotifers 100–200 µm & algae 10–20 µm +0.842∗ rotifers 100–200 µm & algae 10–20 µm +0.792∗
rotifers >200 µm & algae 10–20 µm +0.906∗ rotifers >200 µm & algae 10–20 µm +0.689∗∗
asplanchnids & algae 10–20 µm +0.737∗∗ asplanchnids & algae 10–20 µm +0.894∗

rotifers <100 µm & algae >20 µm +0.804∗ rotifers <100 µm & algae >20 µm +0.590∗∗∗
rotifers 100–200 µm & algae >20 µm +0.769∗ rotifers 100–200 µm & algae >20 µm +0.591∗∗∗
rotifers >200 µm & algae >20 µm +0.782∗ asplanchnids & algae >20 µm +0.696∗∗
asplanchnids & algae >20 µm +0.788∗

p = 0.001∗ . p = 0.01∗∗ . p = 0.05∗∗∗ .

of the Middle Loire of around 300 µg l−1 dry weight,
compared with a mean of 75 µg l−1 chl a. In compar-
ison, from single measurements during summer, in 31
rivers in southern Ontario and western Quebec, Basu
& Pick (1996) recorded a mean zooplankton biomass
of 11 µg l−1 dry weight, for a mean chl a of 6.6 µg
l−1 .
Heterotrophic flagellates are poorly researched in
temperate rivers, and they did not seem to reach the
densities as those measured in lakes, where they range
from 105 to 108 cells l−1 (Berninger et al., 1991;
Laybourn-Parry et al., 1994). In rivers of varying
trophic status, located in eastern Canada, Basu &
Pick (1997b) found that the densities of heterotrophic
flagellates ranged from 1180 to 17 400 × 103 cells
l−1 (mean 4070 × 103 cells l−1 ), (punctual meas-
urements during summer). In the Middle Loire, the
heterotrophic flagellates reached a maximum of 2400
× 103 cells l−1 .
There are also few studies on ciliates in rivers, in
comparison with standing waters. As in eutrophic and
mesotrophic lakes (Laybourn-Parry, 1992), the sum-
mer protozooplankton of the Middle Loire was dom-
inated by oligotrichs (Strombidium and Strobilidium)
and peritrichs (Vorticella), and as in Windermere,
Askenasia was a common member of the summer
assemblage. In a calcareous and oxygenated river, Bal-
dock et al. (1983) found a mean annual density of
0.70 × 103 cells l−1 . For a eutrophic river Carlough
& Meyer (1989) indicated that the maximum ciliate
abundance reached 302 × 103 cells l−1 . With dens-
ities up to 49 × 103 cells l−1 and biomasses ranging
between 18.7% and 28.5% of the total heterotrophs,
ciliates are important components of the potamoplank-
ton of the Middle Loire. Laybourn-Parry (1992) indic-
ated some mean maximum abundance of 9.2–11.0 ×
103 cells l−1 for ciliates in eutrophic temperate lakes,
which are lower than those measured in the Middle
24
Loire. In 1997, they were three times more numerous
than in 1996 (Lair et al., 1998). In 1996, ciliate abund-
ance followed the peak abundance of phytoplankton at
both sites, and a similar situation was observed at the
upper site in 1997 (their peak preceded the maximum
of algae at the perturbed downstream site).
Community relationships
The major factors regulating the abundance of river
plankton are known to be discharge, water residence
time, light conditions, nutrient concentrations and
grazing (Reynolds, 1988; Köhler, 1997; Gosselain et
al., 1998). The impact of predation and competition
from other grazers may also play a role. In addition,
young fish, which actively swim close to the river bank
of the area studied, can exert predation pressure on
the ciliate and rotifer faunas (Lair et al., 1994; Lair et
al., 1996b), and thus accounting for patterns observed
solely on the basis of available food resources in the
plankton may be misleading.
Little research has focused on the interactions
between phototrophic and heterotrophic potamoplank-
ton, including protozooplankton. In eutrophic rivers,
however, the microbial food web could be particu-
larly important, because of the possibility for organic
matter to transit through heterotrophic protists, via the
bacteria. During low water periods, seasonal growth
and higher temperatures permit larger overall pro-
ductivity by the phytoplankton and bacterioplankton,
and the organisms which exploit them. In fact, het-
erotrophic nanoflagellates have been identified as the
main bacterial consumers in a large variety of marine
and freshwater systems. In turn, they are able to play
a key role in the self-purification of enriched waters.
They may be consumed by larger ciliates and micro-
zooplankton (Laybourn-Parry, 1992; Jürgens, 1994;
Jürgens et al., 1996).
Ciliates are known to have a wide spectrum of
foods, extending from picoplankton to nanoplankton.
They can compete with heterotrophic flagellates and,
for example, large marine ciliates are each capable of
ingesting up to 15 × 103 bacterial cells d−1 (Sherr et
al., 1989). Oligotrichs are efficient feeders on nan-
oflagellates; they can also control bacteria, as well
as small algae, and compete with small metazoans.
Peritrichs are essentially bacterivorous and algivorous,
and among the “other ciliates” collected in the Middle
Loire, some taxa are predators (De Puytorac et al.,
1987; Foissner & Berger, 1996; Jürgens et al., 1996).
The field densities of heterotrophic flagellates are
usually significantly correlated with the abundance of
bacteria in freshwaters (Bloem & Bar-Gilissen, 1989)
and the correlation between the different components
of the potamoplankton can be interpreted as trophic
links. At the upper site, the significant positive cor-
relation between heterotrophic flagellates and BOD5
suggested trophic links derived from the development
of bacterial populations. At the downstream site more
suspended matter has probably induced more bacterial
development and this could explain the large increase
in density of HF, while the significant correlations pos-
itively related to BOD5 were indicative of bacteria and
heterotrophic flagellates production. The interchange
between oligotrichs and peritrichs in the course of
summer, a situation similar to that observed the pre-
vious year, suggests an alternation of grazers between
algae-dominant and bacteria-dominant resources.
Most of the rotifers of the Middle Loire are filter
feeders, and asplanchnids are known to be predat-
ors. These organisms are grazers of bacteria and small
algae, as well as predators of flagellates or small
ciliates (Pourriot, 1977; Lair & Oulad Ali, 1990; Gil-
bert & Jack, 1993; Reche et al., 1997). They are
capable of exerting a significant impact when they
peak, removing > 100% of phytoplankton produc-
tion daily (Lair & Reyes-Marchant, 1997), a situation
similar to that observed in the Belgian section of the
River Meuse (Gosselain et al., 1998), and in the river
Moselle (Bergfeld et al., 1998). The significant posit-
ive correlations related to their principal food (Tables 2
and 3) indicate that, as a whole, food was not the
limiting factor in the Middle Loire. However, pe-
culiarities occurred between sites. The size structure
analysis indicated that the different rotifer size classes
may have affected both small HNF and small algae
at the upper site only (Table 3). Concerning hetero-
trophic flagellates the significant negative correlation
between HNF and rotifers, suggested that upstream,
these micrometazoans may have depressed the nano-
heterotrophic flagellates (more numerous downstream
and not affected).
Influence of anthropic disturbances
In the impact assessment monitoring program carried
out on the Middle Loire, the physical and chemical
characteristics and the algae have been studied for over
20 years (Lair & Sargos, 1993; Lair et al., 1996).
The rotifers were studied in 1977–1978 (Lair, 1980)
and also in 1995 (Lair & Reyes-Marchant, 1997) and
 25
Table 4. Inter-annual variations in density of algae, rotifers and ciliates, and comparison among them {∗ data from Lair & Reyes-Marchant
(1997); ∗∗ data from Lair et al. (1998); 1997 this study}

years 1995∗ 1996∗∗ 1997 1996∗∗ 1997 1997 1995∗ 1996∗∗ 1997
sites algae algae algae ciliates ciliates HF rotifers rotifers rotifers

106 cells l−1 106 cells l−1 106 cells l−1 cells l−1 cells l−1 103 cells l−1 ind. l−1 ind. l−1 ind. l−1
Dampierre-en-Burly
mean 32 34 32 4740 12 000 260 1772 1110 1414
max 68 50 63 6200 24 500 700 3700 3610 3505

St-Laurent des Eaux

mean 44 35 40 8010 23 250 880 2223 654 790
max 106 78 77 14 300 48 820 2400 5800 1775 2750

6 =% >37.5 >2.9 >25.0 >69 >93.75 >238 >25.45 <41.0 <44

1996. The examination of the ciliates started in 1996
(Lair et al., 1998) and heterotrophic flagellates were
added in 1997 (that study). A systematic increase in
algal density has been observed at the lower site from
1977 onwards. Rotifer density was also observed to
increase in this part of the river in 1977–1978, and in
1995. The density of ciliates in 1996–1997 and that
of heterotrophic flagellates in 1997 largely increased
from the upper to the lower site (Table 4), and con-
sequently the decrease in rotifer density observed in
1996–1997 has to be debated.
During the last three years, no floods have disrup-
ted the low water period and most of the physical and
chemical variables were in the same range, so these
years were used for comparison. In 1995, no particular
anthropic disturbance occurred at either site and the
summer algal growth was luxuriant, leading to rotifer
densities among the highest ever reported. In 1996,
a one-off, massive chlorination occurred at the end
of July at the nuclear power plant of Dampierre-en-
Burly (to clean the cooling circuits) before becoming
chronic at low concentration (to prevent invasion of
amoebae) (Cabanes et al., 1997). Moreover, important
excavation works occurred in the riverbed downstream
(installation of a diffuser across the width of the river,
and improvements to the fish pass). In 1997, the
river bed was once again silted up in consequence
of the works supporting the old bridge of Beaugency,
situated approximately 10 km upstream (Map 1).
In 1996, the year with massive followed by chronic
chlorination, the abundance of algae increased slightly
downstream and the rotifers decreased drastically.
However, in the course of the surveillance programme,
after the start of chlorination the species richness of
algae and rotifers, and the density of bacillariophytes
and trichocercids, has only decreased once. Simul-
taneously, there was a decrease in the diversity index
of these communities, before they returned to normal
(Ecological studies in Loire, annual report for im-
pact assessment, EDF 1996). In 1997, under chronic
chlorination, algae, ciliates and heterotrophic flagel-
lates increased downstream. This suggests that one-
off chlorination can depress these organisms, while
chronic chlorination does not do so significantly.
There is no doubt that high food density tends to
increase the frequency with which their filters have to
be active, and that the direct and significant relation-
ships between rotifers and chlorophytes & diatoms,
noticed in 1996, can be interpreted in that way (Lair
et al., 1998). Similarly, the significant positive correl-
ation between rotifers and their potential food items,
noticed for 1997, suggested that food limitation was
not the cause of their downstream decrease. However,
this does not exclude potential competition between
the ciliates and rotifers that succeeded each other, as
well as between ciliates and heterotrophic flagellates
(Jakobsen & Hansen, 1997) etc.
The excavation works, responsible for the dis-
placement of organic matter, have probably enhanced
the growth of protozooplankton downstream. In 1997,
more suspended matter was added to that produced the
precedent year, for example 537 mg l−1 of SM was
measured on one occasion at the reference station. The
increase in ciliates was higher in 1997 than in 1996,
and heterotrophic flagellates increased more than 200
times downstream. With the displacement of organic
matter the bacterial production probably enhanced the
downstream growth of these bacterivorous flagellates
26
and, consequently, provided more food for ciliates and
in turn to other items. In contrast, classically, suspen-
ded matter which contributes to clogging of the filter
feeders’ food grooves during filtering, thus decreas-
ing ingestion rate, can disturb their growth processes
(Kirk, 1991; Montel & Lair, 1997). For example, in
1996, a systematic decrease in rotifer density was ob-
served at a station situated 3 km downstream from the
excavation works (Ecological studies in Loire, annual
report for impact assessment, EDF 1996). In 1997,
at Saint-Laurent des Eaux, the significant negative
correlation between SM and ‘brachionids & asplanch-
nids’ suggested that suspended matter displacements
caused a decrease in rotifer density (the negative cor-
relation between SM and ‘trichocercids & other ro-
tifers’ was not significant). Asplanchnids were more
numerous in 1997 and the growth of these predaceous
rotifers contributed to the biomass stability, but the
feed back response has probably caused a decrease in
density of the filter feeders (particularly brachionids).
Conclusion
As in 1995 and 1996, in this zone the same species
have grown at both sites, but different quantitative
patterns have occurred. This confirmed that the river
was not only enriched by the flow, but was largely
influenced by local conditions and trophic relation-
ships (Lair & Reyes-Marchant, 1997). The autotrophic
plankton remains the dominant component for most
of the time, confirming that lowland rivers can sup-
port significant phytoplankton production (Descy &
Gosselain, 1994). The results illustrate also the im-
portance of protozooplankton in the river food web.
Their biomass changed from 20% to 30% of the
total heterotrophic potamoplankton in a distance of
90 km. Rotifers are known to be efficient filter feed-
ers, whereas ciliates are known for recycling organic
matter and managing the excess primary production.
Both contribute to the decline of algae at the end of
summer. In addition, the HNF were actively depressed
upstream by ciliates and rotifers, their contribution to
the potamoplankton biomass being reduced at both
sites.
That study has shown the complexity of the pro-
cesses active in the regulation of potamoplankton,
and the extent to which they are naturally induced
or caused by human impact. As underlined by Reid
(1997), this highlights the need for a careful evalu-
ation of all the parameters that are used as assessment
criteria. In this eutrophic river, where food appeared
to be non-limiting, anthropic disturbances have in-
duced chain reactions. In 1996 the rotifer decrease was
probably caused by suspended matter, and possibly ac-
centuated by the decrease in the algal abundance, due
to the one-off chlorination. The scenario was different
in 1997, the addition of suspended matter was prob-
ably responsible for the increase in food level, which
contributed to the development of the predators. As a
consequence, both direct and indirect effects seem to
have induced the observed decrease in the rotifers.
Acknowledgements
We thank Electricité de France, which supported this
research, for the opportunity to complete data, for a
better evaluation of variables that need to be used as in
assessment monitoring programs.
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