Biologia 68/6: 1136—1141, 2013
Section Zoology
DOI: 10.2478/s11756-013-0262-7
Ecology of Pectinatella magnifica and associated algae
and cyanobacteria
Irena Šetlíková1, Olga Skácelová2, Jan Šinko3, Josef Rajchard1 & Zuzana Balounová1
1
Faculty of Agriculture, University of South Bohemia in České Budějovice, Studentská 13, CZ-37005 České Budějovice,
Czech Republic; e-mail: setlik@zf.jcu.cz
2
Faculty of Science, University of South Bohemia in České Budějovice, Na Zlaté stoce 10, CZ-37001 České Budějovice;
e-mail: oskacelova@prf.jcu.cz
3
Faculty of Fishery and Protection of Waters, University of South Bohemia in České Budějovice, Zátiší 728/II, CZ-38925
Vodňany, Czech Republic; e-mail: jan.sinko@seznam.cz
Abstract: The freshwater bryozoan species Pectinatella magnifica was found in 6 sandpits and in 19 mostly extensively
managed ponds in the Protected Landscape Area and Biosphere Reserve Třeboňsko (Czech Republic) from its first record (in
2003) to 2012. Mean fresh biomass and abundance of P. magnifica colonies were 0.6 ± 1.5 kg m−2 and 0.7 ± 1.1 colony m−2
(± SD), respectively, in the shoreline zone during the growing season 2006–2011. The maximum biomass was mostly
recorded during the first half of August in all basins. Colonization of further localities was recorded rather than increasing
of P. magnifica biomass or abundance in 2012. There were no correlations between water temperature or water transparency
and biomass/abundance of P. magnifica during the growing season. P. magnifica colonies preferred to grow on the branches
or roots (especially of Salix sp.) to aquatic macrophytes and stones. Most of the water bodies, where this bryozoan species
occurred, had lower concentration of total phosphorus in the water when compared with the typical fishponds in the Czech
Republic. Inner space of colonies of P. magnifica provided suitable higher trophic level substrate when compared with the
water of the sandpits/fishponds especially for green coccal algae. A massive algal colonization was indentified in decomposing
colonies at the end of the growing season.
Key words: bryozoa; Pectinatella magnifica; phytoplankton; perifyton; cyanobacteria; algae
Introduction
Pectinatella magnifica (Leidy, 1851), a species originated from South America, has become a common
species in freshwater bodies of the Protected Landscape Area (PLA) and Biosphere Reserve (BR) Třeboňsko during the last decade. This species started to
spread further towards south – to Austria (Bauer et al.
2010). Pectinatella magnifica was first recorded in the
PLA and BR Třeboňsko in the sandpit Cep in 2003
(Šetlíková et al. 2005). However, this bryozoan species
was noticed in the Czech Republic in the Elbe and Vltava rivers already at the first quarter of the 19th century (Opravilová 2005). In 1951 there was the first literature data about the occurrence of P. magnifica in
the catchment area of the Black Sea (Knoz 1960). Data
about the occurrence and spreading of P. magnifica
in the Czech Republic are rather scarce, random and
concentrated till to the 1975 (Opravilová 2005, 2006).
Recently Balounová et al. (2011) revised occurrence of
this bryozoan species in the South Bohemia (sandpits:
Cep and Vlkov and fishponds: Hejtman, Nový Kanclíř
and Podřezaný, all in the PLA and BR Třeboňsko and
Hněvkovice dam). There is an internet site running for
net mapping of P. magnifica from 2012 (Šinko 2013).
c 2013 Institute of Zoology, Slovak Academy of Sciences
Ten native species of bryozoans described from the
Czech Republic (Hrabě 1954; Sládeček 1980) represent
about 70% of the European species (Wood & Okamura
2004) and about 20% of the total number of freshwater bryozoan species described world-wide (Ruppert &
Barnes 1993; Opravilová 2005). Pectinatella magnifica
colonies differ from colonies of our native bryozoan
species especially in size. Their fresh weight can reach
about 70 kg (Balounová et al. 2011) (or up 1 m in diameter: Rodriguez & Veron 2002), while one of the biggest
native bryozoan species – Plumatella fungosa (Pallas,
1768); grows only up to approximately 0.5 kg of fresh
weight. This is caused by the gelatinous, non-cellular
character of the P. magnifica colonies, where particular individuals (zoids) occupy only a thin layer on their
surface. Morphology of statoblasts (resistant bodies for
asexually reproduction) and gelatinous-adhesive character of P. magnifica colonies could favour their spreading over other native bryozoan species. Furthermore,
unlike most species of native bryozoa, statoblasts of
P. magnifica are armed with attachment hooks around
the margin (Ruppert & Barnes 1993). There is only
one native species – Cristatella mucedo (Cuvier, 1798),
whose statoblasts are also spiny and its colony are somehow gelatinous too. However, size of C. mucedo colonies
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Ecology of Pectinatella magnifica
is rather small (up to 15 cm long and about 0.6 cm
broad) (Wiebach 1958).
Mutualism between invertebrates and photosynthetic symbionts (algae and cyanobacteria) are generally known in cnidarians (especially corals) (e.g., Fransolet et al. 2012), sponges (e.g., Weissenfles 1989; Venn
et al. 2008; Erwin et al. 2012), mussels (Gray et al.
1999) and also in ascidians (Erwin et al. 2012). However, coexistence of algae and bryozoa are poorly understood. It seems that gelatinous colony matrix can favour
some groups of cyanobacteria and algae. Cyanobacteria
(90%) dominated on surfaces enclosed by the colonies
and also within the colony matrix of P. magnifica,
whereas mixed communities of diatoms (78%), bluegreen algae (12%) and green algae (11%) developed on
uncolonized surfaces (Joo et al. 1992).
The aims of this study were to (1) quantify spreading of Pectinatella magnifica in the PLA and BR Třeboňsko, (2) specify factors which cause spreading including its substrate preferences and (3) describe assemblages of algae and cyanobacteria algae living on
the surface or inside the colonies of P. magnifica.
Material and methods
The occurrence of P. magnifica was (1) systematically
checked in about 25 water bodies (sandpits and fishponds)
and (2) occasionally recorded by the managers of the fishponds in the Protected Landscape Area (PLA) and Biosphere Reserve (BR) Třeboňsko (latitude: 48◦ 48 –49◦ 11 ;
longitude: 14◦ 38 –15◦ 00 ; area: 700 km2 with 15% water surface) in the South Bohemia from 2003 to 2012. Sandpits are
lakes originated after mining of sandy gravel supplied with
the groundwater and/or from the Lužnice River, while fishponds are mostly drainable basins with various intensity of
fish culture. Fish stocking density in extensively managed
fishponds is up to approximately 100 kg ha−1 . Common
carp (Cyprinus carpio L., 1758) dominates (80%; individual weigh: 3–10 kg) to the other fish species: grass carp
(Ctenopharyngodon idella Valenciennes in Cuvier and Valenciennes, 1844), tench (Tinca tinca (L., 1758)), pikeperch
(Sander lucioperca (L., 1758)), European catfish (Silurus
glanis L., 1758) and pike (Esox lucius L., 1758) (Fish Farming Třeboň, plc). Extensively managed fishponds are mostly
used for anglers and recreation. Sandpits are deeper (mean
depth mostly a few meters) and younger (about 40 years)
than fishponds (mean depth mostly up to 1 m and from
middle-ages, respectively) (Table 1). Furthermore sandy
gravel bedrock and low fish culture in the sandpits are the
reason for their lower trophic level (Kroupa & Drbal 1990)
when compared to the other standing water bodies. This results also in their higher water transparency (mostly > 1 m).
Biomass and abundance of P. magnifica colonies were
assessed in the rectangular area shore (5 m × 10 m along the
shore) in five sandpits and in four fishponds with extensive
fish culture (Table 1). Six random samples were randomly
collected from every water body at the beginning, in the
middle and at the end of each growing season, i.e., from
May (June) to early September in 2006–2011.
Water temperature and transparency (Secchi disc
depth) were measured together with the concentration of
oxygen and pH using WTW 340i or Gryf Magic XBM. Concentrations of NO3 -N, NO2 -N, NH4 -N, total nitrogen (TN),
PO4 -P and total phosphorus (TP) were determined using
1137
Table 1. Characteristics of the (fish)ponds and sandpits where
the biomass and abundance of colonies of P. magnifica were estimated. (Water bodies are ordered according to their area).
Water body
Area
(ha)
Mean depth
(maximum) (m)
Staňkovský pond
Hejtman pond
Podřezaný pond
Nový Kanclíř pond
241
82
60
31
6.0
1.0
1.0
1.0
(8.5)
(6.5)
(5.0)
(2.5)
Cep sandpit
Vlkov sandpit
Veselí I sandpit
Horusice sandpit
Veselí sandpit
163
46
24
23
10
7.0
2.8
3.5
6.5
3.5
(11.8)
(5.0)
(5.0)
(2.5)
(5.0)
standard methods (Horáková et al. 1989). Water chemistry
was monitored in the sandpits: Cep and Veselí I and in the
fishponds: Hejtman and Nový Kanclíř at monthly intervals
(from July to September) in 2012.
The communities of algae and cyanobacteria associated with P. magnifica were studied in 2012. Phytoplankton was sampled from open water. Samples were fixed with
iodine Lugol solution. Abundance was estimated by counting the cells in a Bürker chamber after a full sedimentation. Also net-plankton samples (mesh size of 20 µm) were
collected for capturing large species (cyanobacteria of water blooms, colonial green algae and dinophytes). Phytobenthos was taken from both (1) substrates colonized by
P. magnifica and (2) its inner surface attached to substrates.
Occurrence of cyanobacteria and algae was also studied in
coloured spots in gelatinous matrix (bodymatter).
Kruskal-Wallis test was used for comparison of the
biomass (abundance) among all the studied water bodies.
The difference was considered significant when P < 0.05.
The regression analyses of P. magnifica biomass (abundance) and water temperature or transparency was calculated in the Statistica for Windows (9.0) programme.
Results and discussion
Occurrence of P. magnifica in the PLA and BR Třeboňsko
Pectinatella magnifica was found in 6 sandpits and in
10 mostly extensively managed ponds in the PLA and
BR Třeboňsko from 2003 to 2011 (Fig. 1). Most of the
localities of P. magnifica were situated in the east part
of PLA and BR Třeboňsko. In 2012 there were other
9 fishponds in PLA and BR Třeboňsko, where P. magnifica has been found out for the first time (Fig. 1 indicated with 8). The presence of P. magnifica has not
been proved in the sandpits: Horusice I, Cep II, Tušť,
Františkov and Halámky and in the fishponds: Malý
Horusický, Starý Kanclíř, Špačkov, Jamský, Purkrabský and Starý u Cepu (ordered from north to south).
Biomass and abundance of P. magnifica colonies
Pectinatella magnifica appeared mostly already in June
in all years (2006–2011). Mean fresh biomass of P. magnifica colony was 0.6 ± 1.5 kg m−2 (± SD) in the shoreline zone (5 m from the shore) during the growing seaUnauthenticated
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1138
I. Šetlíková et al.
Fig. 1. Sandpits and fishponds (black) in the Protected Landscape Area (PLA) and Biosphere Reserve (BR) Třeboň, where Pectinatella magnifica appeared. Water bodies are numbered according to the year of P. magnifica first appearance and ordered from the
north to the south within the year. The Czech Republic with PLA and BR Třeboňsko is in the right corner.
Notes: 1: Cep sandpit (in 2003); 2a: Cep I sandpit, 2b: Podřezaný fishpond (syn. Nový Lipnický fishpond) (both in 2005); 3a: Svět
fishpond, 3b: Staňkovský fishpond, 3c: Hejtman fishpond and 3d: Vydýmač (by Hejtman) fishpond (all in 2006); 4a: Vlkov sandpit
and 4b: Nový Kanclíř fishpond (both in 2007); 5: Veselí I sandpit (in 2009); 6a: Veselí sandpit, 6b: Horusice sandpit and 6c: Vydýmač
(by Smržov) fishpond (all in 2010); 7a: Stupský and Mlýnský fishponds and 7b: Ruda fishpond (both in 2011); 8a: Prelátský fishpond,
8b: Opatovický fishpond, 8c: Podsedek fishpond, 8d: U Vostudy fishpond (by Lutová), 8e: Staré jezero fishpond (only in the channel);
8f: Mařka fishpond, 8g: Vizír fishpond 8h: Zájezdek fishpond and 8i: Starolipnický fishpond (all in 2012).
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Ecology of Pectinatella magnifica
1139
Table 2. Mean fresh biomass (abundance) of colonies of P. magnifica (P. m) (± SD) in 2006–2011. (Water bodies are ordered according
to the year of the first record of P. m).
Water body
Cep sandpit
Podřezaný pond
Hejtman pond
Vlkov sandpit
Nový Kanclíř pond
Veselí I sandpit
Staňkovský pond
Veselí sandpit
Horusice sandpit
1st record of P. m.
20033
20051
20061
20072
20071
20092
20092
20102
20102
Biomass of P. m.
(kg m−2 )
0.2
0.6
0.4
2.0
0.3
1.4
0.01
0.5
0.8
±
±
±
±
±
±
±
±
±
Abundance of P. m.
(colony m−2 )
0.4b
1.1ab
0.7b
2.8a
0.5ab
2.3ab
0.02b
0.5ab
1.5ab
0.5
0.6
0.3
1.6
0.3
1.4
0.1
1.1
0.5
±
±
±
±
±
±
±
±
±
0.6ab
0.9ab
0.7b
1.9a
0.3b
1.5ab
0.1b
1.1ab
0.9ab
Explanations: 1 Balounová et al. (2011); 2 Lukešová (2011); 3 Šetlíková et al. (2005); values with different superscript are significantly
different.
son 2006–2011. The maximum of bryozoan biomass was
mostly recorded during the first half of August in all
basins. The biomass (abundance) of P. magnifica significantly differed among the water bodies [H (8, N = 296)
= 52.9, P < 10−4 ]. The highest mean biomass and also
abundance of P. magnifica was recorded in the sandpit Vlkov, while the lowest biomass of P. magnifica in
the fishponds Hejtman, Staňkovský and in the sandpit
Cep (Table 2). Mean biomass of P magnifica colonies
was 1.3 ± 2.3 kg m−2 (± S.D.) in Cep in 2005–2007
(Balounová et al. 2011), which is higher when compared
with mean biomass in this sandpit determined in 2006–
2011 (Table 2). It seems that the quantity of P. magnifica colonies has decreased during the time in the
sandpits, where it has been recorded for the first time.
Unfortunately there are no other quantitative data of
the P. magnifica occurrence in the literature.
There was no relation found between first recorded
appearance of P. magnifica and the year of its maximum biomass. Some basins (e.g., Hejtman and Podřezaný) reached the maximum of the biomass of P. magnifica one year after its first appearance, while the
others (e.g., Kanclíř and Vlkov) after 4 or 5 years.
Mean abundance of P. magnifica colonies was 0.7 ± 1.1
colony m−2 (± SD) in the shoreline (5 m from the
shore). Biomass and abundance of P. magnifica colonies
did not significantly differ among years (from 2006 to
2011) in particular water bodies. However, the number of both fishponds and sandpits, where P. magnifica
was found, increased with time. Thus colonization of
further localities was recorded rather than increasing
of P. magnifica biomass or abundance (see also Table 2).
Physico-chemical conditions of the water bodies with
P. magnifica
Mean water transparency was 1.7 ± 0.65 m and
0.9 ± 0.3 m (± SD) in the sandpits and fishponds,
respectively. These values are really high when compared with a few centimetres water transparency in
intensively managed fishponds dominating in the surrounding area. Concentration of oxygen ranged from 6.1
to 9.0 mg L−1 and from 5.4 to 11.0 mg L−1 (measured
in the morning: 9 to 11 a. m.) in the sandpits and fish-
Table 3. Hydrochemical parameters (mean ± SD; n = 8; mg L−1 )
in the sandpits (Cep and Veselí I) and in the fishponds (Hejtman
and Nový Kanclíř) in 2012.
Sandpits
PO4 -P
TP
NH4 -N
NO2 -N
NO3 -N
TN
0.009
0.005
0.14
0.009
0.06
1.6
±
±
±
±
±
±
0.008
0.011
0.037
0.008
0.026
0.38
Fishponds
0.010
0.064
0.37
0.001
0.18
2.5
±
±
±
±
±
±
0.008
0.067
0.192
0.003
0.094
0.64
ponds, respectively. Water pH-values varied from 6.0 to
9.5 in both types of water bodies.
Mean concentrations of total nitrogen, NO2 -N and
PO4 -P in the water were comparable in the sandpits
(Cep and Veselí I) and in the extensively managed fishponds (Hejtman and Nový Kanclíř) in 2012. Mean concentrations of NO3 -N, NH4 -N and TP were higher in
the fishponds than in the sandpits (Table 3). In general, concentration of total nitrogen and its all inorganic forms in both sandpits and fishponds were similar with the mean concentration of these nutrients in
the fishponds of the Czech Republic (C. R.). Only concentration of total phosphorus in the sandpits was at
least one order lower than its values found out in the
fishponds in the C. R. (0.025–1.4 mg L−1 ) (Hartman et
al. 1998). Unfortunately, there were no consistent data
about the water chemistry in other sandpits/fishponds
in 2006–2011.
There was no correlation found between water
temperature (mean water temperature: 22.4 ± 2.7 ◦C
(± SD); min 16.6 ◦C, max 26.5 ◦C, n = 97) during
the growing season and biomass/abundance of P. magnifica. The same seems to be true for water transparency (n = 42) and biomass/abundance of P. magnifica. Balounová et al. (2011) reported colonies started
to appear after the water temperature increased above
20 ◦C at least for three consecutive days and they
grew even after short-term drop of water temperature. Maximum biomass of P. magnifica appeared when
mean water temperature decreased (from 30 ◦C) to
19 ◦C (Joo et al. 1992). High variability of bryozoan
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1140
biomass/abundance even within the same water body
at one sampling date did not allow finding any correlation with physical or chemical parameters of the water
environment.
Substrate preferences of P. magnifica
Pectinatella magnifica prefers to be attached on the
objects supporting it in the water column than to be
free floating. Abundance of P. magnifica colonies significantly differed among the substrates [H(2, N = 234) =
7.8, P = 0.02]. Its colonies were mostly found out on
the branches or roots of woody plant (mostly willow –
Salix sp. or pine – Pinus sylvestris fallen into the water) submersed in the water (66% of findings). Twenty
one percent of P. magnifica colonies were also recorded
on the aquatic macrophytes (e.g., reed – Phragmites
australis and cattail – Typha sp.). The least number of
colonies was attached to the stones. However, biomass
of the P. magnifica colonies did not differ among these
3 substrates (woody plants, aquatic macrophytes and
stones). There were no free floating colonies of P. magnifica and this bryozoan species was not found in the
basins without any substrate. These results are in agreement with the results of Balounová et al. (2011), who
found out that biomass and number of colonies significantly differed between the transects where willows
grew and without them in the same sandpits and fishponds in 2005 to 2007. Typical substrates of P. magnifica were also woody, i.e., floating wood in Brno Lake
Dam (Knoz 1960) or wooden moles in Hejtman fishpond (Šinko 2013). Joo et al. (1992) reported no substrate preference showed colonies of P. magnifica in an
Alabama oxbow lake, where dead cypress twigs (Taxodium distichum), aquatic plants (Justicia ovata) and
pine sticks were present (Joo et al. 1992). More controlled conditions with equal substrate occurrence are
needed for proper study of substrate preference.
Cyanobacteria and algae associated with P. magnifica
Gelatinous body matter of P. magnifica colonies appeared to be a suitable substrate for other organisms, i.e. cyanobacteria, green algae, diatoms and also
red-coloured bacteria. The highest abundance of algae
(i.e., planktonic green algae and cyanobacteria Pseudanabaena sp.) was identified in dying colonies at the
end of the growing season. A loss of photosynthetic pigments was observed within some species of cyanobacteria, euglenophyte and dinophyte living in a nutrient
rich microhabitat of old bryozoan matrix.
Species composition of algal assemblages differed
between phytoplankton (“outside”) and matrix of
P. magnifica (“inside”). Probably it is a consequence of
a higher nutrient content in bryozoan matrix when compared with the water. Most of the sandpits (e.g., Veselí,
Veselí I and Horusice) were dominated by tiny filamentous planktonic cyanobacteria (Limnothrix sp. and
Planktolyngbya sp.), accompanied with dinoflagellates
and diatoms. Abundance of coccal green algae in phytoplankton of these sandpits did not exceed 30% (usually
much less). However green spots formed by abundant
I. Šetlíková et al.
coccal algae (especially Desmodesmus, Scenedesmus,
Monoraphidium sp., often also Coenococcus sp. and
Eustigmatos sp.) were found in bryozoan matrix. Similarly small diatoms (Stephanodiscus hantzschii and
Nitzschia sp.) exploited suitable conditions in nutrientrich bryozoan matrix, forming chains, groups or rows
there. On the contrary, planktonic species typical for
nutrient poor conditions in the water of sandpits were
found scarcely and never abundant in the bryozoan matrix.
Composition of benthic communities on the substrate differed from assemblages formed on the inner
bryozoan surface attached to the substrate. Cyanobacteria (e.g., Aphanothece stagnina, Cylindrospermum
spp., Tolypothrix tenuis and Merismopedia elegans) and
algae (i.e., benthic green algae: Bulbochaete sp. and
Tetraspora sp.; diatoms: Frustulia spp., Navicula radiosa, Rhopalodia gibba, Tabellaria flocculosa, Achnanthes spp. and Cymbella spp.) which are common in
mesotrophic and slightly eutrophic waters lived on the
substrate enclosed by a colony of P. magnifica and penetrated into its body matrix. Nevertheless they were
usually spatially very restricted. In contrast, benthic
cyanobacteria (Pseudanabaena spp., Leptolyngbya spp.,
Komvophoron sp. and Phormidium spp.) and algae typical for eutrophic waters (e.g., diatom Nitzschia sp.)
extensively colonized the nutrient rich matrix, even
though they did not prevail in the surrounding benthic
communities. Joo et al. (1992) compared the species
composition of algal assemblages between the substrates enclosed by colonies of P. magnifica and without it in an oxbow lake (Alabama). Similarly to our
results cyanobacteria (especially Oscillatoria limnetica, Phormidium mucicola and Lyngbya birgei) dominated (90%) on surfaces enclosed by the P. magnifica
colonies, accompanied by small numbers (8%) of green
algae. In contrast, diatoms (especially Nitzschia palea,
N. parvula and Cymbella tumida) prevailed (78%) over
green algae (12%) and cyanobacteria (8%) on substrates un-colonized by bryozoan (Joo et al. 1992).
The same algal species colonized both the matrix
and the bryozoan surface attached to the substrate were
recorded in the conditions when (1) abundance of phytoplankton was much higher than phytobenthos or (2)
colonial diatoms dominated in phytoplankton as well
as in submersed surfaces. The first situation was observed in the fishpond (Nový Kanclíř) which had one
of the highest trophic level among localities with occurrence of P. magnifica. Planktonic species prevailed
both in the matrix and on the bryozoan surface attached to the substrate there. Phytobenthos is commonly substantially reduced during a massive development of phytoplankton. As a result the surfaces submersed in the water (e.g. wood and stones) can be
covered with sedimented phytoplankton instead of phytobenthos (Skácelová 2007). Benthic diatoms and filamentous cyanobacteria (Pseudanabaena sp.) dominated
in both bryozoan surfaces attached to substrate and
colony matrix in several of other fishponds (e.g., Hejtman). Mostly colonial diatoms (Fragilaria crotonensis,
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Ecology of Pectinatella magnifica
Asterionella formosa and Aulacoseira spp.) were identified in both phytoplankton and submersed surfaces in
Hejtman fishpond.
Pectinatella magnifica as an invasive species
Rapid spreading of P. magnifica in the PLA and BR
Třeboňsko is evident. It is questionable, if relative nonspecific occurrence of P. magnifica in the waters PLA
and BR Treboňsko can justify its classification as an
invasive species. More frequent records of this species
are partially influenced by increased attention of researchers. In general, biomass of P. magnifica was comparable within all of the water basins (except that of
Nový Kanclíř) during 6 years (2006–2011) and thus its
increase inside each of the water basin should not be
expected. However further spreading of P. magnifica
into other water basins especially with the presence of
shrubs in the shoreline is highly probable (Fig. 1: new
localities indicated with 8, where P. magnifica was noticed in 2012).
Acknowledgements
Financial support to this research was provided by the
Czech Science Foundation (GACR) no.: P503/12/0337, Cenakva no. CZ. 1.05/2.1.00/01.0024. and by the project of
the OPVK CZ.1.07/2.3.00/09.0076.
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65713.85
Received January 18, 2013
Accepted June 16, 2013
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