Hydrobiologia 391: 241–247, 1999.
© 1999 Kluwer Academic Publishers. Printed in the Netherlands.
Seasonal succession of Cladocerans in a riceﬁeld in Italy
, Mario Cotta-Ramusino
& Fiorenza G. Margaritora
Department of Biology, University of Milan, Via Celoria 26, 20133 Milano, Italy
Department of Animal and Human Biology, University of Rome «La Sapienza», Viale dell’Universit`a 32, 00185
Received 3 August 1998; in revised form 22 December 1998; accepted 11 January 1999
Key words: heleoplankton, biological riceﬁeld, ecological succession, Wlassicsia pannonica, Italy
A biological riceﬁeld in northern Italy, without periodic dry spells in its growing cycle and therefore more familiar
to naturally humid zones, was studied for its heleoplankton community. The biocoenosis reached a greater level of
complexity than reported in literature. In particular, the seasonal succession of Cladocerans, the dominant group
throughout the study period, was analyzed. Wlassicsia pannonica (Daday, 1904; Anomopoda Macrothricidae), is
new to Italy; its morphology is compared to that of other populations of the same species and its biological cycle
is compared with that of other dominant Cladocerans.
Numerous studies conducted in the last thirty years on
European riceﬁelds have helped expand and deepen
our knowledge of their biocoenoses. Research related
to the composition and seasonal succession of heleo-
plankton, indicates how the biological physiognomy
of these waters is characterized by a series of com-
mon elements that substantially coincide everywhere,
as well as the existence of a strong correlationbetween
the trophic state of a riceﬁeld and the dominance of
certain euplanktonic species in differentperiods of the
growing cycle (Rossi et al., 1974; Pont, 1978, 1983;
Ferrari et al., 1984, 1991; Leoni & Cotta-Ramusino,
1996; Leoni et al., 1997).
Agronomic techniques greatly inﬂuence the evol-
ution of trophic levels: the frequency and length of
dry spells and the type of chemical treatments in par-
ticular, as well as the quantity of fertilizer initially
supplied to the system. A growing cycle commonly
passes from an oligotrophic situation, typical of the
initial phase of "open waters", to a ﬁnal, eutrophic
phase. In parallel, a progressive increase in biological
diversity and abundance of species can be observed,
becoming, in some cases, a community in dynamic
equilibrium (Pont, 1978, 1983; Ferrari et al., 1984,
1991). Phytophagous prevail in spring, such as Cyc-
lopoid Copepods and some Cladocerans, while during
summer, detritivores associated to macrophytes be-
come more numerous (Pont, 1978). In biological rice-
ﬁelds, where pesticides are not used, dry periods don’t
change the evolving succession, but only inﬂuence its
speed; in traditionally cultivated riceﬁelds this process
is slow and high levels of biocoenotic complexity are
difﬁcult to reach (Leoni & Cotta-Ramusino, 1995).
This paper reports on research carried out in 1995
on the heleoplankton community of a biological rice-
ﬁeld in northern Italy, substantially different from
traditionally cultivated ricelﬁelds, as it remains sub-
merged and is not subject to periodic dry spells.
The stability of this environment, more similar to
the natural humid zones than to an artiﬁcial system,
notably inﬂuences the development of the biocoen-
osis that reaches a great level of complexity here
(Leoni, in prep.). In particular, the seasonal succes-
sion of Cladocerans, the dominant group throughout
the entire period of study, is analyzed. A record
of Wlassicsia pannonica (Daday, 1904; Anomopoda
Macrothricidae), a species new to Italy, is discussed.
The research was carried out in a riceﬁeld (called
Zelata) of about 500 m
, located in Bereguardo in the
province of Pavia. The riceﬁeld was submerged at the
end of April with water coming from a lateral canal of
the Ticino River as well as from some neighbouring
springs, and remained ﬂooded without any interme-
diate phase of dryness until the beginning of August.
The riceﬁeld was emptied on August 14. There was
almost always about 10 cm of water coveringthe ﬁeld.
During the ﬁrst phase of growing cycle the water had
acidic pH values (5.5), low conductivity (90–100 µS)
and high percentages of dissolved oxygen saturation
(about 80%). As the season progressed, so did the
pH (up to 7.1) and conductivity (150–160 µS), while
oxygen content decreased (25%).
Materials and methods
Weekly sampling of heleoplankton was done using
a corer of plexiglass 6.5 cm in diameter and 60 cm
high. With this method, described in detail by Leoni
& Cotta-Ramusino (1994), all organisms present in
both the column of water and sediment can be col-
lected and sampled with equal efﬁciency even when
vegetationis abundantlater in the season. In our study,
taxocoenosis succession was analyzed by means of
PCA (Principal Components Analysis) using the pro-
gramme package CANOCO (Ter Braak, 1988). The
analysis was performed on a total of 16 species, us-
ing a log (x+1) transformation in order to stabilize
the variance (Sneath & Sokal, 1973) and to avoid
over-weighting of abundant species due to dominance
Sixteen species of Cladocerans were found: six Daph-
niidae, three Macrothricidae and Chydoridae, and two
Moinidae and Bosminidae (Table 1); among these, the
presence of Daphnia galeata and Eubosmina core-
goni, typically euplanktonic lake-dwelling species,
should be noted.
Of particular interest was a population of Wlas-
sicsia pannonica, a species which favors temporary
waters rich in vegetation, which was ﬁrst recorded for
Italy. It lives on sediment or bottom vegetation; it is
rare in permanent water basins (Petkovski, 1970).
The ﬁrst specimens (indicated as Macrothrix
schauinslandi G.O.S. – Negrea, 1966; 1983), found
in Hungary near Lake Balaton, were described by
Table 1. Species of Cladocera occurring in the zo-
oplankton samples collected in the Zelata riceﬁeld
Daphnia galeata [dg] Sars emend. Richard
Eubosmina coregoni [eu] (Baird)
Bosmina longirostris [bo] (O. F. Müller)
Ceriodaphnia reticulata [cr] (Jurine)
Ceriodaphnia laticaudata [cl] P. E. Müller
Scapholeberis rammneri [sr] Dumont & Pensaert
Simocephalus vetulus [sv] (O. F. Müller)
Simocephalus serrulatus [ss] (Koch)
Macrothrix rosea [mr] Li
Macrothrix laticornis [ml] Jurine
Wlassicsia pannonica [wp] (Daday)
Alona rectangula [ar] Sars
Alonella excisa [ae] (Fischer)
Chydorus sphaericus [cs] (O. F. Müller)
Moina afﬁnis [ma] (Birge)
Moina micrura [mi] Kurz
Daday (1904). Other authors reported it from Slov-
akia, Romania, Macedoniaand CentralAsia (Smirnov,
Females measure from 0.62 to 1.06 mm in length; in
particular weekly morphometric analysis on the adult
indicated a decrease in average size towards the end
of the cycle (Figure 1). Body shape varies from oval
in smaller specimens to squarish in bigger specimens.
The shell is marked (more or less) with elongated
polygonal reticulation forming a series of waves (Fig-
ure 2(6)). The ventral margin has simple spines at the
anterior half and irregularly alternating long and short
spines at the rear third. The head, with little differenti-
ation fromthe rest of the body, had a typicaloutgrowth
on the ventral edge, a relatively big eye, an ocellus,
Figure 1. Body length of Wlassicsia pannonica.
Figure 2. Morphological analysis of W. pannonica. (1) limb I, (2) limb II, (3) limb III, (4) limb IV, (5) limb V, (6) body shape, (7) head shape,
(8) postabdomen. See also p. 244.
Figure 2. Continued.
a sharp labrum and a lamellar expansion of moder-
ate size (Figure 2(7)). Antennule not dilating; antenna
well developed with nine setulae (0,0,1,3/1,1,3) and
three spines (0,1,0,1/0,0,1).
The thorax bears ﬁve pairs of limbs. First pair: the
outer distal lobe has one short pinnate and one long
biarticulate setulae; the innerdistal lobe has threesetu-
lae of decreasing length. Internal margin of endites 1
and 2 with additional seta, modiﬁed to a pseudo-fork
(Figure 2(1)). Second pair: not well-differentiatedepi-
podite, endopodite with eight biarticulated scrapers,
six of which are dentate; the last setulae are smaller
and located at the base of the ﬁrst and seventh setulae,
while at the base of the ﬁfth a hairy conical expansion
can be observed (Figure 2(2)). Third pair: exopod-
ite with ﬁve setulae, endopodite with eight setulae in
the external series and seven in the internal with the
last spine-shaped (Figure 2(3)). Fourth pair: exopod-
ite with ﬁve setulae – this characteristic differentiates
Wlassicsia from the genus Macrothrix which has only
2 or 3 -, endopodite with 10 pinnate setulae, ﬁve
posterior and ﬁve anterior (Figure 2(4)). Fifth pair:
exopodite with one large and two small plume seta
(probably of endital origin, according to Dumont &
Silva-Briano, 1998); endopodite reduced to a big lobe
and gnatobase with one long and two shorter setae
The postabdomenis bilobed, the preanal part bears
a series of spinules while the anal has many series of
irregulary placed spine-shaped setulae (Figure 2(8));
claw with basal spine and denticulated terminal part.
The ephippium is well developed, extending from
the posterior ventral corner of the valves to the suture
of the head to overhalf of the shell, and normallybears
Males have a large head, postabdomenbilobed and
the ﬁrst pair of limbs have a hook, size 0.52 mm.
On the whole, the morphological characteristics of
the Italian population of W. pannonica conform to the
species described by Daday, with a greater afﬁnity to
Slovenian species due to the larger dimension of its
eye and the shape of its labrum (Hudec, 1983).
Structural evolution of the taxocoenosis
Cladocerans were among the ﬁrst organisms to occur
in riceﬁelds, and by the second week of ﬂooding they
were already present in appreciable numbers (Figure
3). The colonizing species, Daphnia galeata and two
Figure 3. Density of most important species (or genus) of Cladocera.
Figure 4. Percentage of young and adult females of W. pannonica.
species of the genus Moina, were found from the ﬁrst
day of sampling until the beginning of July, reaching
maximum density in the middle of May. The decrease
in D. galeata related to the appearance of Acanthocyc-
lops robustus (Copepoda): young of Daphnia are, in
fact, extremely vulnerable to this predatory copepod
(Gliwicz, 1994). During the ﬁrst week of ﬂooding,
Eubosmina coregoni, a typical euplanktonic species,
was also present. This species had no stable element
in the community but probably came into the riceﬁeld
together with irrigation water. W. pannonica appeared
towards the middle of May, with the water still free of
vegetation and the taxocoenosis of Cladocerans dom-
inated by efﬁcient ﬁlter feeders. During the sixth week
of ﬂooding, the maximum development of the pop-
ulation was observed, with density values equal to
Figure 5. Principal Component Analysis (PCA) of the zooplankton in the Zelata riceﬁeld: scores of taxonomic groups in the plane of the ﬁrst
two axes of ordination.
198 ind l
.ThecycleofW. pannonica lasted about
ﬁve weeks; in this period, only parthenogenetic and
ephippial females occurred (Figure 4). The species
decreased at the end of June when Macrothrix lati-
cornis, another macrothricid, with similar biological
and ecological characteristics appeared.
Starting from June, detritivorous species associ-
ated with vegetation succeeded each other: Scaphole-
beris rammneri, Alona rectangula, Macrothrix lati-
cornis, M. rosea, Ceriodaphnia reticulata, C. lati-
caudata, Simocephalus sp., Chydorus sphaericus and
Alonella excisa. Most of these showed a single cycle,
lasting for the entire period of ﬂooding.
The evolution of the community structure over
time was clariﬁed by Principal Components Analysis.
Figure 5 depicts the ordering of the ﬁfteen weeks
of sampling in the space deﬁned by the two axes of
major variation explained (eigenvalues= 0.48; 0.27).
The data, distributed continuously and progressively,
starting from the second quadrant, were grouped in
three distinct clusters with reference to the principle
evolutionary stages shown by the system. The ﬁrst
group included the ﬁrst six weeks of ﬂooding and
corresponded to the initial phases of development of
the system, when the water was free from vegetation.
The second, consisting of three observations, determ-
ined the intermediary phase during which both the
rice and infesting macrophytes developedrapidly. The
third group grouped the data when the system reached
its maximum degree of evolution. The third and last
Figure 6. Principal Component Analysis (PCA) of the zooplankton in the Zelata riceﬁeld: scores of samples (numbers correspond to sampling
weeks) in the plane of the ﬁrst two axes of ordination.
phase, which remained constant for two months, was
interrupted by the ﬁnal dry spell that preceded harvest.
With regard to the ordering of the organisms, Figure
6 shows the species that characterized and domin-
ated the development phases previously indicated. In
the ﬁrst period, when phytoplankton production was
high, typical euplanktonic forms dominated, such as
D. galeata, two species of the genus Moina and W.
pannonica. In the succeeding phase, another Daph-
niid and three Chydoridae occured. In the last phase,
when decompositionprocesses increased, species con-
nected with the detritus chain prevailed: Chydoridae,
Macrothricidae and Ceriodaphnia reticulata.
The succession of the heleoplankton community stud-
ied here was much more regular than in other Italian
riceﬁelds, where dry periods bring about consider-
able physical and chemical imbalance in the system,
forcing the biocoenosis to start over again at the ini-
tial phases of development. After each dry period,
the characteristic species of the ‘open water’ pion-
eer phase tend to reappear and thus the succession
of the community is interrupted. At least one or two
weeks are necessary to restore the conditions need for
the system to proceed towards a more advanced de-
gree of development and structural complexity (Leoni
& Cotta-Ramusino, 1995). Moreover, many species
cannot complete their biologicalcycle, while the dom-
inant ones are often dicyclic (Margaritora et al., 1987;
Ferrari et al., 1991).
Instead, the succession in this riceﬁeld was con-
tinuous and monocyclicfor most species, carrying out
their own biological cycle and reaching good values
of density. Unlike other studies, where Copepods col-
onize the riceﬁelds and dominate for the ﬁrst two or
three weeks of ﬂooding, here the Cladocerastarted the
cycle to appear and remain dominant (as total number
of adults per liter) from April to August.
Multivariate analysis techniques conﬁrmed these
observations, indicating seasonal trends and identify-
ing the biocoenosis characteristics of the individual
The recording of W. pannonica in riceﬁeld wa-
ter indicates once again the importance of human-
mediated transport in the colonizing of new envir-
onments by Cladocerans: this holarctic species was
seemingly introduced in Italy with seeds. It probably
has a wider distribution than it appears. An ongoing
study of the family Macrothricidae in Italy (Mar-
garitora, in prep.), revealed its occurrence in other
riceﬁelds (riceﬁeld «Merse», Central Italy), where it
was mis-identiﬁed as Echinisca rosea (Moroni, 1967),
probably on the basis of its antennule shape. Find-
ing this population supports the supposition that W.
pannonica is a stable element of the heleoplankton in
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