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Seasonal succession of Cladocerans in a ricefield in Italy

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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.
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Hydrobiologia 391: 241–247, 1999.
© 1999 Kluwer Academic Publishers. Printed in the Netherlands.
241
Seasonal succession of Cladocerans in a ricefield in Italy
Barbara Leoni
1
, Mario Cotta-Ramusino
1
& Fiorenza G. Margaritora
2
1
Department of Biology, University of Milan, Via Celoria 26, 20133 Milano, Italy
2
Department of Animal and Human Biology, University of Rome «La Sapienza», Viale dell’Universit`a 32, 00185
Roma, Italy
Received 3 August 1998; in revised form 22 December 1998; accepted 11 January 1999
Key words: heleoplankton, biological ricefield, ecological succession, Wlassicsia pannonica, Italy
Abstract
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.
Introduction
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.
Study area
The research was carried out in a ricefield (called
242
Zelata) of about 500 m
2
, 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
effects.
Results
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
´
evin
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,
1992).
Morphology
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.
243
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.
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 ve setulae this characteristic differentiates
Wlassicsia from the genus Macrothrix which has only
2 or 3 -, endopodite with 10 pinnate setulae, ve
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
(Figure 2(5)).
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
two eggs.
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
245
Figure 3. Density of most important species (or genus) of Cladocera.
246
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
1
.ThecycleofW. pannonica lasted about
ve 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 rst 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
247
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.
Discussion
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
successive phases.
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
ricefield.
248
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... Our observations in the rice fields in Songkhla province support this view where one species in Bosminidae were detected and there was no record of Daphnia. Commonly, a rice growing cycle passes from an oligotrophic situation, typical of the initial phase of open water, to a final, eutrophic phase (Leoni et al. 1999). In parallel, there is a progressive increase in biological diversity and abundance of species. ...
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Non-indigenous species may pose a threat to native ecosystems worldwide. In aquatic environments, invasives may have a negative impact on human food security and livelihoods. Several water fleas (Crustacea: Branchiopoda: Cladocera) are notorious invasive alien species influencing large freshwater lake systems and even inland seas. In the current review, we discuss the state of knowledge regarding non-indigenous species in the Cladocera and their invasiveness potential in different continents. We argue that the potential impacts and occurrence of cladoceran exotics may be higher than generally assumed. We critically review 79 cases from literature sources, involving 61 cladoceran taxa where records outside of their natural distribution ranges were previously interpreted as invasions. We assessed the probability of natural range expansions versus human-mediated introductions and we discuss several major corridors of invasion. We estimate human-mediated transportations for at least 43 taxa (out of 61; ca 70%), while other cases can be seen as natural expansions of their distribution ranges (not necessarily/not likely human-mediated) and/or taxonomical confusion. We confirm non-indigenous presence in recipient regions for at least 41 cladoceran taxa, of which several are true invasives (i.e., with negative impacts on native ecosystems). The majority are zooplankters with effects on pelagic freshwater ecosystems, yet we also report on introductions by littoral taxa. We argue that cryptic introductions of cladocerans are taking place on a global scale, yet they remain under the radar. We highlight several striking case studies, such as the Ponto–Caspian onychopods that have invaded the Baltic Sea and the Laurentian Great Lakes, and several clones of the anomopod genera Daphnia and Bosmina that have successfully colonised new environments, causing equilibria shifts in native aquatic worlds. At the same time, we dispel some myths about taxa that were misconstrued as invasive in certain localities. Based on our review, the first of its kind for freshwater zooplankton, future environmental monitoring tools including molecular techniques and detailed surveys with rigorous and critical taxonomical assessments may help to provide a clearer picture on the extent of invasiveness of cladocerans.
... Living organisms as indicators of pollution have been used for the conservation of biodiversity in rice fields (Ueno, 2013). Although zooplankton is a key component of the aquatic fauna of rice fields (Lim et al., 1984), only in very few countries, such as Italy and Southeast Asian countries, was zooplankton used as a bioindicator of contamination in paddy fields (Chittapun et al., 2009;Ferrari et al., 1991;Ferrari et al., 1984;Leoni et al., 1998). Especially in developing countries, where control policies are limited, it is important to conduct risk assessments in rice fields based on site-specific measured environmental concentrations (MECs) to identify possible risks to aquatic organisms (Stadlinger et al., 2018). ...
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Invasions by human-introduced non-indigenous species (NIS) are one of the main threats to biodiversity and a driving force of global change (Vitousek et al. 1997, Mack et al. 2000, Clavero and García-Berthou 2005). The Iberian Peninsula (IP) is a hotspot of biodiversity (Médail and Quézel 1999) and a knowledge of the invasive species inhabiting it is essential for conservation and environmental management. Naturalized vertebrates and plants in the IP have received considerable attention (see e.g. Vilà et al. 2001, Pleguezuelos 2002, Sobrino et al. 2002, Lloret et al. 2004, Alcaraz et al. 2005), but its invasive invertebrates are very poorly known. Although there are many records of some invertebrate invasive species, particularly crustaceans, there are very few available reviews of selected taxa of invertebrate invaders in the IP (e.g. Espadaler and Collingwood 2001). The aim of this chapter is to review the animal species naturalized in Iberian inland waters, including vertebrates and free-living and parasitic invertebrates. As usual, the taxonomy and biogeography of vertebrate species are much better known than for invertebrates, so our data for invertebrates should be regarded as a preliminary check-list. Similarly, the parasites of non-commercial aquatic species are poorly studied and the data in the IP mostly come from studies of the eel, Anguilla anguilla (Linnaeus), thus certainly underestimating the range of introduced parasites (Blanc 1997, 2001). We feel, however, that it is important to provide such a first check-list because many of the invertebrates involved are nowadays common in the IP and for many of them it is largely unknown even by biologists that they are not indigenous to the IP. Increasing the awareness on the introduced status and current distribution of these species is essential to reduce their spread and impact.
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The study of heleoplankton samples collected in an experimental ricefield in the province of Reggio Emilia (Northern Italy) evidenced a successional pattern of cladoceran species, characterized by the dominance of Moinidae in the early phase the rice cultivation (from May to July). In particular a species new for Italy,Monia weismanni Ishikawa, 1896, typical of Far East ricefields, was found; it was probably introduced into Italy with seeds and constitutes a stable element of the heleoplankton biocoenosis. The population co-occurs withMoina brachiata, Moina affinis, andMoina micrura in the ricefield. In this short noteM. weismanni is described, pointing out the morphological differences with other populations of the same species and with similar species; furthermore, life cycles in Moinidae are analysed in comparison with those of the other dominant cladocerans.
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The seasonal succession of cladocerans was studied in an experimental ricefield (never treated with biocides) located on the Po River Plain (Province of Reggio Emilia) in 1982, the first year of rice cultivation, and in two later years, 1984 and 1986. A total of 26 species were identified; some of them were found in Northern Italy for the first time. The finding of Latonopsis australis Sars is discussed in detail. A trend of increasing specific diversity during the rice cultivation season was not recurrent every year. The most significant trends emerge when the three years are compared. The total number of species was 14 in 1982, 16 in 1984, and 20 in 1986. Diversity, too, increased strongly over the years: this trend was sustained chiefly by the increase in richness of Chydoridae species associated with the growth and decomposition of a large biomass of weeds and microalgae during the summer.
Annual evolution of the zooplancton diversity in twelve italian ricefields The Macrothricidae of the World. Guides to the Identification of the Macroinvertebrates of the Continetal Waters of the World Numerical Taxonomy
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Proposta per una metodica di campionamento qualitativo dell'eleoplancton di risaia
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Struttura ed evoluzione stagionale dell'eleoplancton di risaia: confronto tra due anni consecutivi
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