Studi Trent. Sci. Nat., Acta Biol., 80 (2003): 23-26
Studi Trent. Sci. Nat., Acta Biol., 80 (2003): 23-26
© Museo Tridentino di Scienze Naturali, Trento 2004
ISSN 0392-0542
Structure of bdelloid rotifer metacommunities in two alpine streams in northern Italy
Diego FONTANETO, Giulio MELONE*, Claudia RICCI
Dipartimento di Biologia, Università degli Studi di Milano, Via Celoria 26, I-20133 Milano
Corresponding author e-mail: [email protected]
SUMMARY - Structure of bdelloid rotifer metacommunities in two alpine streams in northern Italy - Dispersal in
freshwater invertebrates is one of the forces driving community composition of species. We analysed communities of
small aquatic animals in submerged mosses in two different alpine streams in the Sesia Valley, northern Italy, using a
recently developed tool for meta-community analysis, which deals with a matrix of presence of species in the
communities. The animal model we choose were bdelloid rotifers, often numerically dominant in this kind of
environment, and characterized by poor vagility, obligatory parthenogenesis and anhydrobiotic capabilities. The whole
meta-community resulted significantly nested, although the two groups of communities from the two streams resulted
well separated from each other in the ordered matrix. The resulted structure of the communities and meta-communities
we described may be compatible with two different colonization patterns: 1) different abilities of dormant stages of
different species to reach new areas, and 2) active animals that actively displace from one moss to next one inside a
same riverine system.
RIASSUNTO - Struttura di metacomunità di rotiferi bdelloidei in due torrenti alpini nell’Italia settentrionale - I meccanismi di dispersione negli invertebrati d’acqua dolce rappresentano una delle forze principali che possono strutturare la
composizione in specie nelle comunità. Abbiamo analizzato comunità di piccoli animali acquatici in muschi sommersi in
due ruscelli alpini in Valsesia, Italia settentrionale, utilizzando un nuovo metodo per le analisi di metacomunità, prendendo in considerazione una matrice ottenuta dalle presenze delle diverse specie nelle comunità indagate. Gli animali utilizzati sono stati i rotiferi bdelloidei, spesso dominanti in questo ambiente, e caratterizzati da bassa vagilità, partenogenesi
obbligatoria e capacità di anidrobiosi. L’intero sistema della metacomunità analizzata è risultato essere strutturato gerarchicamente, sebbene le comunità dei due ruscelli siano significativamente separate nella matrice ordinata. La struttura
delle comunità e delle metacomunità da noi osservata è compatibile con due meccanismi di colonizzazione: 1) differente
capacità di colonizzazione indiretta di forme dormienti in specie diverse, sulle lunghe distanze, e 2) capacità di spostamento attivo tra un cuscinetto di muschio e un altro all’interno dello stesso corso d’acqua.
Key words: Rotifera Bdelloidea, nestedness, metacommunity structure, meiofauna, Piedmont
Parole chiave: Rotifera Bdelloidea, nestedness, struttura di metacomunità, meiofauna, Piemonte
Bdelloid rotifers are small (80-1500 µm long) aquatic
animals, characterized by obligate parthenogenetic
reproduction and by the ability to withstand unfavourable
periods through anhydrobiosis (Gilbert 1983; Ricci
2001). Anhydrobiosis allows them to live in all aquatic
habitats, mostly freshwater, and even in temporary
waters: therefore bdelloid rotifers can be found in lakes,
rivers, puddles and interstitial soil water. Bdelloid
rotifers represent a major component of the fauna
associated with mosses in lotic environments (Linhart
et al. 2002a, 2002b; Wallace & Ricci 2002).
Since the ‘80s, some authors approached the study
of the species distribution in metacommunities in which
the communities were hierarchically ordered (Taylor
1997; Wright et al. 1998; Davidar et al. 2002). Such
ordered patterns of distribution (nestedness) occur when
species assemblages of species-poor communities
represent a sub-sample of species-rich ones (Patterson
& Atmar 1986). The causes leading to nested patterns
are generally referred to 1) different colonization abilities
and/or 2) selective local extinction of different species
(Lomolino 1996). Bdelloid rotifers represent a suitable
animal model for the investigation of distribution pattern
in metacommunities, for several reasons: (i) their vagility
is rather poor (Donner 1965) but they can easily disperse due to their dormancy capacity (Cáceres & Soluk
2002); (ii) each single animal can start a new population
due to obligatory parthenogenetic reproduction (Ricci
Fontaneto et al.
2001); (iii) bdelloids can occur in large numbers in small
moss patches (Linhart et al. 2002a, 2002b). Preliminary
investigations showed that not nested patterns are
common in unconnected aquatic and terrestrial habitats,
like moss cushions. Here we present the structure of
bdelloid rotifer metacommunities from two unconnected
alpine streams.
Study area and sampling methods
Bdelloids from mosses in stream
scriminate between the streams (Sokal & Rohlf 1995).
U-test was applied to the moss ranks obtained by
ordering the matrix using reciprocal averaging (known
also as correspondence analyses). Counting the number
of “embedded absences” in this matrix and comparing
it to the number of randomly generated matrices, we
followed the method proposed by Leibold & Mikkelson
(2002) to detect coherence of the matrix.
Moss samples were collected from two alpine
streams, Argnaccia and Res, in the Sesia Valley (Vercelli
Province, Piedmont Region, northern Italy). Both
streams are tributaries of the Sesia River. Argnaccia
(named after its closest locality) runs in the municipality
of Campertogno, while Res (named after Mount Res)
in the municipality of Varallo Sesia. Submerged mosses
were collected in both streams from 850 to 1000 m a.s.l.,
at 15 sampling sites (A1-A15, R1-R15) located at about
50 meters far apart (from A1 and R1 at the highest points
to A15 and R15 at the lowest). Each sample had a surface
of 5 cm2. Samples were kept in small plastic bottles and
were directly brought to the laboratory, where animals
were maintained alive at 6 °C till identification according
to Donner (1965).
Nineteen species were found in 30 samples in the
two streams (Fig. 1). The overall matrix generated by
Statistical analyses
The patterns of species distribution were tested
for nestedness (Patterson & Atmar 1986) using the
program “nested calculator” (Atmar & Patterson
1995). The program uses a thermodynamic model and
measures the extent of order in a matrix. The data set
was arranged in a presence/absence matrix with the
species according to columns, and the communities
according to rows. Ranking of rows and columns is
obtained by ordering from the highest value to the
lowest, and by minimizing unexpected absences and
presences, in order to obtain the highest value of
nestedness with the data set (Atmar & Patterson
1993). The probability of generating a matrix with
lower/higher temperature (= more/less order) than the
observed data set was tested by comparing its temperature to the temperatures of 500 matrices randomly
generated by Monte Carlo simulations. Each matrix
resulting from the simulation had a fixed number of
occupied cells, equal to that resulting from the
observed data set. The temperature of randomly
generated matrices is roughly normal distributed. We
called mean T the mean temperature of randomly
generated matrices, σ its standard deviation, and T°
the temperature of a metacommunity. Using a two
tailed z test, if T < mean T - 1.96 σ, the probability
that the matrix is as ordered as a random matrix is <
0.05, and the metacommunity is considered nested
(Atmar & Patterson 1995).
T-test and Mann-Whitney U-test were used to di-
Fig. 1 - Overall matrix, composed of species and samples,
ordered using reciprocal averaging (Leibold & Mikkelson
2002). A1 to A15 are moss communities from Argnaccia,
and R1 to R15 are those from Res stream.
Fig. 1 - Matrice generale della presenza delle specie nei 30
campioni esaminati, ordinata secondo “reciprocal
averaging” (Leibold & Mikkelson 2002). Da A1 ad A15 sono
designate le comunità nei muschi campionate lungo il
ruscello Argnaccia, da R1 a R15 quelle campionate lungo il
ruscello Res.
Studi Trent. Sci. Nat., Acta Biol., 80 (2003): 23-26
Fig. 2 - Range of temperature of 500 Monte Carlo simulated matrices. Arrow indicates the observed temperature. Matrix
temperature, average system temperature, matrix fill, and probabilities estimates are given.
Fig. 2 - Range delle temperature delle 500 matrici ottenute con simulazioni Monte Carlo. La freccia indica la temperatura
della matrice osservata. Sono indicati temperatura della matrice, media del sistema, fill della matrice e valore di probabilità.
Fig. 3 - Box-plot of the distribution of the number of species
in 30 analyzed communities, 15 in Argnaccia and 15 in Res.
The horizontal bold line represents the median value; the
box represents upper and lower quartiles; the whiskers are
the largest observations within 1.5 interquartile ranges both
top and bottom; each (o) indicates each observation falling
outside the “3 interquartile range” of the whiskers.
Fig. 3 - Box-plot della distribuzione del numero di specie nelle
30 comunità analizzate nei ruscelli Argnaccia e Res. La linea
orizzontale spessa indica il valore mediano; i rettangoli
comprendono il 50% delle osservazioni intorno alla mediana,
ovvero i valori tra il 1° ed il 3° quartile; le tacche sono le
osservazioni estreme nell’intervallo 1,5 interquartile sia
superiormente che inferiormente; i simboli (o) indicano gli
eventuali valori esterni al range di ampiezza 3 interquartili,
delimitato dalle tacche.
“nested calculator” revealed a significant nested
metacommunity, whose temperature was significantly
lower than expected (Fig. 2). Although the matrix was
significantly coherent (N of observed embedded
absences = 124, N ± s.d. in simulated matrices = 258.9
± 13.3, P < 0.001), the metacommunities of the two
streams were almost completely separated on the
opposite sides of the ordered matrix using reciprocal
averaging (U15,15 = 0, P < 0.001). Also mean number
of species per community was significantly lower in
the communities living in the Argnaccia (5.4 ± 0.9)
than in those found in the Res stream (7.6 ± 1.2) (ttest = 5.71, d.f. = 28, P < 0.001) (Fig. 3).
Habrotrocha collaris, Philodina flaviceps, Philodinavus
paradoxus, Rotaria rotatoria), and of some species that
occur in one stream only (Habrotrocha gracilis,
Philodina nemoralis in Argnaccia, and the other 10
species in Res). This pattern may be produced by the
dispersal capabilities of the dormant stages that might
differ among different species; the “best dispersers” may
colonize both streams, while the “poor colonizers” may
reach one stream only. When a stream is colonized, active
animals could actively occupy almost all submerged
mosses, connected by presence of water.
Bdelloid rotifers are commonly assumed to disperse “blowing in the wind” or by animal transport as
dormant dehydrated stages (Jenkins & Underwood
1998; Cáceres & Soluk 2002). This study suggests that
colonization of bdelloid rotifers can be related not only
to passive transport of dormant stages, but that active
bdelloids can move, at least along the continuous
environment of one stream. The analysis of the bdelloid
metacommunities in the two streams, Argnaccia and
Res, reveals the presence of a group of species that are
shared (Adineta barbata, Adineta vaga minor,
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Structure of bdelloid rotifer metacommunities in two