FUNGI ON FRUIT TREE PETALS FLOATING IN WATER
41
BIOLOGICAL LETT. 2007, 44(1): 41–50
Available online at http://www.biollett.amu.edu.pl
Fungi and fungus-like organisms (Straminipila)
on fruit tree petals floating in water
BAZYLI CZECZUGA, BO¯ENNA MAZALSKA, ANNA GODLEWSKA,
EL¯BIETA MUSZYÑSKA and KATARZYNA KUÆ
Department of General Biology, Medical University, Kiliñskiego 1, 15-089 Bia³ystok, Poland,
e-mail: [email protected]
(Received on 15 January 2007; Accepted 6 October 2007)
Abstract: Fungi and fungus-like organisms (Straminipila), growing on petals of 5 fruit tree species (Malus
sylvestris, Prunus avium, P. cerasus, P. domestica and Pyrus communis) floating in water from 3 types
of freshwater habitats (spring, river and pond) were investigated. A total of 88 species, including 47 funguslike and 41 fungal species were identified on the petals. The most common species were: Rhizophydium
cornutum, R. globosum (fungi), Aphanomyces irregularis, A. laevis, Saprolegnia litoralis, Pythium butleri,
P. inflatum, P. tardicrescens, P. ultimum, Angulospora aquatica, Arbusculina fragmentans, Lemonniera
aquatica, and Pithomyces obscuriseptatus (Straminipila). Most species were observed on petals of Prunus
cerasus (85 species) and fewest on petals of P. avium (55). Numbers of species observed on petals ranged
from 39 for the spring Cypisek to 55 for the river Supraœl. In water from all 3 habitats, the number of
species of fungi and fungus-like organisms on petals was negatively correlated with the concentration of
sulphates. Ten species are recorded as new to Polish waters.
Keywords: aquatic fungi, fruit trees, freshwater habitats, fungus-like organisms, hydrochemistry, petals,
Poland, saprotrophs, Straminipila
INTRODUCTION
In spring, when fruit trees are flowering (especially apple trees, pear trees, cherry
trees, wild cherry trees, plum trees), many of their petals are blown by wind to freshwater habitats. This especially takes place near orchards. Continuing our studies of
water fungi and fungus-like organisms on various kinds of substrates (CZECZUGA
2004, CZECZUGA & MUSZYÑSKA 2004b, 2005), this time we paid attention to this
untypical kind of substrate – flower petals in freshwaters. Moreover, we attempted
to determine which environmental factors affected the total number of species of fungi
and fungus-like organisms developing on this kind of substrate.
So far, studies on the occurrence of anamorphic fungi (Deuteromycetes) on
similar substrates, i.e. plant petioles and latex, have been carried out only by S RIDHAR & KAVERIAPPA (1983, 1987).
42
Bazyli Czeczuga et al.
MATERIAL AND METHODS
The study included flower petals of 5 species of fruit trees: wild crab (Malus
sylvestris (L.) Mill.), wild cherry (Prunus avium L.), sour cherry (Prunus cerasus L.),
garden plum (Prunus domestica L.), and wild pear (Pyrus communis Medik.), collected in spring in north-eastern Poland. The water for experiments was collected
from 3 different freshwater habitats:
• spring Cypisek, located in the north of Bia³ystok city: limnokrenic type, width
0.65 m, depth 0.12 m, discharge 2.4 dm3 s-1; surrounded by cultivated fields, without
trees; its bed covered with sand;
• river Supraœl, right-bank tributary of the middle part of the river Narew, flowing
through the Knyszyn Forest (Puszcza Knyszyñska): length 106.6 km; samples
collected above the municipal bathing beach, at the sluicegate of an arm of the
river Supraœl flowing just through Supraœl town; sampling site surrounded by
meadows; bed muddy;
• pond Dojlidy, located near Bia³ystok: area 34.2 ha, max. depth 2.85 m; southern
shores border with coniferous woods and western shores with Bia³ystok city. The
samples were collected from the western part of this pond, which is used by the
inhabitants of the city as a bathing beach.
Nineteen water parameters of the above sampling sites were determined
(Table 1) according to the methods recommended by the American Public Health
Association (APHA 1995).
For the determination of the presence of aquatic species of fungi and funguslike organisms on the flower petals of fruit trees, the following procedure was employed. A sample of petals (about 2 mg) of each tree species was transferred to each
of two 1-dm3 samples of water representing each site (altogether 6 vessels per tree
species) and placed in the laboratory at ambient temperature. Petals from each vessel
were gradually removed from the vessels and observed under a light microscope, and
mycelia of fungi and fungus-like organisms on the petals of fruit trees were recorded. The methods are described in detail by S EYMOUR & FULLER (1987). The petals
of various species were observed under a microscope for 3–4 days. The experiments
lasted 4 weeks. The water chemistry data and the fungal flora were carried aut in
three parallel repetitions (data of Table 1 and total number of species of Table 2 are
mean values).
Identification of fungi and fungus-like organisms was based on their morphology and biometric data of antheridia and oogonia, or conidiophores and conidia of
anamorphic fungi.
Identification of the fungi was based on the following keys: JOHNSON (1956),
SEYMOUR (1970), BATKO (1975), KARLING (1977), DICK (1990), PYSTINA (1998);
and for anamorphic fungi, DUDKA (1974), INGOLD (1975), CARMICHAEL et al. (1980),
MATSUSHIMA (1993), and works of the authors who were the first to describe the
respective species. The systematics of straminipilous organisms was used according
to DICK (2001).
In order to determine the relation between the number of species of fungal biota
in a given habitat and the various factors in the aquatic environment, statistical calculations were made. For this purpose the multiple correlation coefficient was used
43
FUNGI ON FRUIT TREE PETALS FLOATING IN WATER
Table 1. Physicochemical parameters (in mg l-1, if not stated otherwise) of water from sampling sites
Parameter
Sampling site
spring Cypisek
pond Dojlidy
river Supraœl
14.00
19.00
17.00
pH
7.19
8.10
7.92
O2
4.20
13.60
14.80
BOD5
4.20
12.40
5.20
Oxydability
16.89
15.74
6.52
CO2
Temperature (°C)
11.00
6.60
4.40
Alkalinity in CaCO3 (mval l-1)
2.90
3.10
4.30
N-NH3
0.87
0.08
0.05
N-NO2
0.09
0.01
0.01
N-NO3
0.12
0.02
0.19
1.50
0.06
0.30
Sulphates
20.98
46.89
43.61
Chlorides
24.00
13.10
13.00
Total hardness in Ca
53.28
62.64
74.88
Total hardness in Mg
3.87
11.18
6.45
P-PO4
Fe
2.05
0.60
0.50
Dry residue
270.00
265.00
223.00
Dissolved solids
130.00
213.00
176.00
Suspended solids
140.00
52.00
47.00
(MCGARICAL et al. 2000). The regression programme calculated the multiple correlation coefficient written in the form of a multiple regression aquation.
The student-t test was employed to evaluate the significance of the correlation coefficients, and the aquare of the multiple correlation coefficient (the coefficient of determination) was calculated, its significance being evaluated by the F test.
RESULTS
The physicochemical analysis of water used for the experiments revealed that
the spring Cypisek was the richest in nutrients; only the N-NO3 content was the lowest there (Table 1). The highest N-NO3 concentration was found in the river Supraœl.
On white petals in water from the 3 freshwater habitats, 47 species of funguslike organisms (Straminipila) and 41 fungal species were identified (Table 2, Fig. 1).
Some of the species were not found in Polish waters before: Allomyces moniliformis,
44
Bazyli Czeczuga et al.
a
b
c
d
e
f
Fig. 1. Some fungi and fungus-like organisms (Straminipila) growing on petals: a – Achlya americana,
oogonium; b – A. polyandra, oogonia; c – Aphanomyces irregularis, oogonium; d – Rhizophlyctis rosea,
sporangium; e – Saprolegnia ferax, sporangium; f – S. litoralis, oogonia. Bar scale – 25 mm.
Gonapodya prolifera, Pythium buismaniae, P. coloratum, P. nagae, P. perniciosum,
P. violae, Rhizophydium macroporosum, and 2 species of the genus Septochytrium:
S. macrosporum and S. variable.
The river Supraœl is the second site of Cylindrochytrium johnstonii in Poland.
Karlingia lacustris was found on petals of wild crab in water from the river. In our
study, Karlingia polonica was found to grow on petals of garden plum in water
collected from the pond Dojlidy. As for anamorphic fungi, Beltraniella peruamazonica, Excipularia aequatorialis and Tricladiella pluvialis are new in Poland. The most
common fungus-like organisms and fungal species included Rhizophydium cornu-
45
FUNGI ON FRUIT TREE PETALS FLOATING IN WATER
Table 2. Taxa of aquatic fungi and fungus-like organisms found on petals in water samples (s = spring
Cypisek, p = pond Dojlidy, r = river Supraœl)
Taxa
Malus
sylvestris
Prunus
avium
Prunus
cerasus
Prunus
Pyrus
domestica communis
Straminipila
Perenosporomycetes (Oomycetes)
Lagenidiales
Lagenidium rabenhorstii Zopf.
Saprolegniales
Achlya americana Humphrey
A. colorata Pringsh.
A. polyandra Hildebr.
A. treleaseana (Humphrey) Kauffman
Aphanomyces irregularis W.W. Scott
A. laevis de Bary
Isoachlya unispora Coker et Couch
Saprolegnia anisospora de Bary
S. ferax (Gruith.) Thur.
S. glomerata (Tiesenh.) A.Lund
S. litoralis Coker
S. uliginosa Johannes
Leptomitales
Rhipidium americanum Thaxter
Pythiales
Phytophthora undulata
(H.E. Petersen) M. W. Dick
Pythium acanthicum Drechsler
P. anandrum Drechsler
P. akanese Tokun.
P. aquatile Hõhnk
P. aristosporum Vanterp.
P. arrhenomanes Drechsler
P. buismaniaeder Plaats-Nit.
P. butleri Subraman.
P. catenulatum V. D. Matthews
P. coloratum Vaartaja
P. dissotocum Drechsler
P. echinulatum V. D. Matthews
P. fluminum Park
P. graminicola Subraman.
P. helicandrum Drechsler
P. inflatum V. D. Matthews
P. intermedium de Bary
P. irregulare Buisman
P. myriotilum Drechsler
P. nagae S. Ito et Takun.
P. palingenes Drechsler
P. papillatum V. D. Matthews
P. periplocum Drechsler
P. perniciosum Serbinow
P. pleroticum T. Ito
P. pulchrum Minden
P. rostratum E. J. Butler
P. tardicrescens Vanterp.
r
p
s, r
s, p, r
s, p, r
r
r
p, r
s, p, r
p
p
r
s
s, p, r
s, p, r
r
s
s, p, r
p
r
r
r
p, r
r
s
s, r
s, p, r
s, p, r
s
r
s, r
p, r
s, p, r
p
p
r
s
r
s, p, r
s, p, r
r
r
r
r
p
p
p
p
p
p
p
p
p
p
r
s, p, r
s
r
s
r
r
r
p
s, p, r
p
s
s
r
p
r
p
p
p
p
p
r
s, p, r
s
r
s
r
r
p
s, p, r
p
s
r
s, p, r
s
r
r
r
p
s, p, r
s
r
p
p
s
r
s, p, r
r
r
r
s, p, r
r
p
s, p, r
s
r
p, r
s, p, r
p
s
s, r
s, p, r
s, p, r
r
s, r
p
s, p, r
p
r
r
p
p
p
p
r
s, p, r
r
s
r
r
p
s, p, r
p
s
r
p
p
p
r
p
s, p, r
r
p
p
p
p
s, p, r
s
r
s
r
r
p
s, p, r
p
s
s
r
p
p
s
r
s, p, r
46
Bazyli Czeczuga et al.
P. vanterpoolii V. Kouyeas et H. Kouyeas
P. violae Chesters et Hickman
P. uladhum Park
P. ultimum Trow
s
s, p, r
r
p
s
s, p, r
r
p
s
s, p, r
r
s, r
p
r
r
r
r
p
s, p, r
p
s
s, p, r
s
s
Fungi
Chytridiomycetes
Chytridiales
Chytridium xylophilum Cornu
Cladochytrium hyalinum Berdan
C. polystomum Zopf
C. tenue Nowak.
Cylindrochytrium jahnstonii Karling
Karlingia lacustris Hassan
K. polonica Hassan
Nowakowskiella elegans (Nowak.) J. Schröt.
Phlyctochytrium rheinboltae Persiel
Rhizophlyctis rosea (de Bary et Woronin) A. Fisch.
Rhizophydium cornutum A.M. Hanson
R. globosum (A. Braun) Rabenh.
R. laterale (A. Braun) Rabenh.
R. macroporosum Karling
Septochytrium macrosporum Karling
S.variabile Berdan
Siphonaria petersenii Karling
Blastocladiales
Allomyces moniliformis Coker et Braxton
Blastocladiella britanica Horen. et Cant.
B. simplex V. D. Matthews
Monoblepharidales
Gonapodya prolifera (Cornu) A. Fisch.
Anamorphic fungi
Angulospora aquatica Sv. Nilsson
Arbusculina fragmentans Marvanová et Descals
Arthrobotrys stilbacea J. Meyer
Beltraniella peruamazonica Matsush.
Canalisporium caribense (Hol.-Jech.et Mercado)
Nawawa et Kuthub.
Excipularia aequatorialis Matsush.
Lemonniera aquatica De Wild.
Leuliisinea amazonensis Matsush.
Mirandina corticola G. Arnaud
Pithomyces obscuriseptatus Matsush.
Pyramidospora casuarinae Sv. Nilsson
Scolecosporiella amazonensis Matsush.
Sigmoidea prolifera (R.H. Petersen) Crane
Spirosphaera beverwijkiana Hennebert
Sporidesmium peruamazonicum Matsush.
Taeniolina deightonii Crane et Schokn.
Tetracladium marchalianum De Wild.
Tricellula aquatica J.Webster
Tricladiella pluvialis K. Ando et Tubaki
Trinacrium subtile Riess
Total number of species
s
p
r
r
r
r
s
s
s
r
s, r
s, p, r
s, p, r
r
p, r
s
s
s
r
p
r
r
r
r
r
s, p, r
s, p, r
r
s, p, r
s, p, r
s, p, r
s, p, r
r
s
p, r
s, p, r
s, p, r
r
r
p
s
r
s
s, p, r
s, p, r
p
s
p
r
s
p, r
s
s, p, r
s, p
s
s, p, r
r
s
r
s
s, p, r
s
s, p, r
r
s
r
r
p
p
p
p
s
64
55
s
s, p, r
s, p
s
s, p, r
r
s
r
r
r
p
p, r
p
p
s
85
r
r
r
p
s
r
s, p, r
s, p, r
r
s, p, r
s, p, r
p
s
r
p
s
s
p
r
r
r
s, p, r
s, p, r
s
p
s, p, r
s, p
s, p, r
r
s
s, p, r
s, p, r
r
p, r
s
s, p, r
s
s, p, r
r
s
r
r
r
p
r
p
s
p, r
p
p
s
61
64
FUNGI ON FRUIT TREE PETALS FLOATING IN WATER
47
tum, R. globosum, Aphanomyces irregularis, A. laevis, Saprolegnia litoralis, Pythium
butleri, P. inflatum, P. tardicrescens, P. ultimum, Angulospora aquatica, Arbusculina
fragmentans, Lemonniera aquatica and Pithomyces obscuriseptatus, which were
found on petals of all investigated fruit tree species and in all 3 water habitats. There
were small differences in number of recorded species between the studied habitats.
The smallest number of species colonized the petals in water from the spring Cypisek (39), while the highest in water from the river Supraœl (55). Correlation analysis
showed that the major environmental factor that influenced the occurrence of fungi
and fungus-like organisms in all 3 freshwater habitats was the concentration of
sulphates (negative correlation in water from all habitats: spring Cypisek r = -0.6092,
pond Dojlidy r = -0.8615, and river Supraœl r = -0.7824, P>0.04).
DISCUSSION
This study shows that white petals of fruit trees are readily colonized by fungi
and fungus-like organisms. Independently of differences in the chemical composition of water from the studied habitats, in all of them the factor that influenced the
number of species of fungus-like organisms and fungi growing on studied petals was
the concentration of sulphates. Its mean values ranged from 20.98 (spring Cypisek)
to 46.89 mg l-1 (pond Dojlidy). A value similar to the latter was recorded in the river
Supraœl (43.61 mg l-1). A similar phenomenon was observed when studying fungi
growing in water on spores of cryptogamic plants (CZECZUGA & MUSZYÑSKA 2004a),
on dead parts of free-floating plants (CZECZUGA et al. 2006a), and on drifting nuts
of birch species (CZECZUGA et al. 2006b). Sulphates in surface waters are one of many
eutrophication factors (HÄKANSON 1999). In oligotrophic waters, sulphates are scanty,
while in eutrophic and hypertrophic waters they are abundant (ca. 10 mg l-1).
Up to now our researches concerning the occurrence of water fungi growing
on various plant and animal substrates showed that in more eutrophic waters, fewer
fungi grow on the same substrate. We observed this when investigating plant substrates, like pollen or emergent plants, and animal substrates, like fragments of chitinous planktonic crustaceans (CZECZUGA et al. 2002, CZECZUGA 2004, CZECZUGA &
MUSZYÑSKA 2004b, 2005).
Among straminipilous organisms, only 12 species of Saprolegniales, including 4 Achlya spp. and 5 Saprolegnia spp., were found in investigated materials. A
relatively large group of representatives of Pythiales (32 Pythium spp. and Phytophthora sp.) were found to grow on petals of fruit trees. On plant substrates, Pythium
spp. colonize mainly ‘soft’ plant substrates, especially root systems of wild and cultivated plants (PYSTINA 1998). Flower petals contain a relatively large amount of
parenchyma, which is also a soft substrate.
Among fungi, chiefly Chytridiales (17 species) and anamorphic fungi (20 species) were found to grow on petals.
As for species new to Polish waters, Allomyces moniliformis grows on petals
in water from the pond Dojlidy. It is known as a saprotroph found in damp sand and
silt (COKER & BRAXTON 1926, BATKO 1975). Gonapodya siliquaeformis was first
described by REINSCH (1878), who assigned it to the genus Saprolegnia. Next, THAXTER (1895) moved it to the genus Gonapodya. It is described as a synonym of Go-
48
Bazyli Czeczuga et al.
napodya prolifera (BATKO 1975). In the literature (SPARROW 1960, BATKO 1975) it
is classified as an aquatic saprotroph growing on fruits and twigs. In this study, it
grew on petals in water from the river Supraœl. Pythium buismaniae, like 5 other
species of Pythiales, was observed on petals of 4 species of fruit trees in river water.
It was first described in the Netherlands on roots of the common flax Linum usitatissimum (PLAATS-NITERINK 1981). However, P. coloratum was known up to now as
a soil fungus (VAARTAYA 1965), so river water is a new habitat in which that fungus
can develop. Pythium nagae was initially described as a parasite of germinating rice
(ITO & TOKUNAGA 1933). In our experiment, P. nagae grew on petals in river water.
Pythium perniciosum grew on petals in water from the pond Dojlidy, although it was
earlier described as a plant parasite (S ERBINOW 1912, YACHEVSKII & YACHEVSKII
1931). Pythium uladhum was described from cellulose in freshwater habitats in Ireland (PARK 1977). We found it on petals in water from the spring Cypisek. The last
representative of Pythiales, Pythium violae, grew on this substrate in water from the
pond Dojlidy. It was first isolated from roots of cultivated Viola sp. (CHESTERS &
HICKMAN 1944). Rhizophydium macrosporum, it was first isolated in New Zealand
(KARLING 1938, 1967) from cooked beef. We observed growth of this fungus on petals
in water from both the river Supraœl and the pond Dojlidy. In water from the spring
Cypisek, we found on the studied substrate 2 Septochytrium spp., which are also new
to Polish waters. Both species were previously described as water and soil saprotrophs in America (BERDAN 1939, KARLING 1942). Siphonaria petersenii, whose
growth on petals was observed also in water from the spring Cypisek, was earlier
described in Brasil as a saprotroph on animal substrates containing chitin (KARLING
1945).
Also some species of anamorphic fungi proved to be new to Polish waters.
Beltraniella peruamazonica and Excipularia aequatorialis grew on petals in water
from the spring Cypisek and Tricladiella pluvialis in water from the pond Dojlidy.
The first 2 species were previously described in the basin of the river Amazon (MATSUSHIMA 1993), whereas the third in Japan in rainwater falling from trees (ANDO &
TUBAKI 1984). Four other anamorphic fungi – Leuliisinea amazonensis, Pithomyces
obscuriseptatus, Scolecosporiella amazonensis and Sporidesmium peruamazonicum
– were first isolated also from the basin of the Amazon (MATSUSHIMA 1993). Cylindrochytrium johnstonii, first described from cellulose substrates decaying in water
in America (KARLING 1941), was encountered on petals of Prunus cerasus in water
from the river Supraœl. This is the second reported site of this fungus in Polish waters.
Cylindrochytrium johnstonii was found on nuts of birches in waters of the pond
Dojlidy and the river Supraœl (CZECZUGA et al. 2006b). Both Karlingia spp. were
described in Poland by HASSAN (1983a, b). Karlingia lacustris was then obtained
by baiting with onion skin in a sample of lake water collected from Lake Miko³ajki
in northeastern Poland. The second species, Karlingia polonica, was then also isolated
by using sterile baits of onion skin from a water sample collected from the pond
M³ociny in Warsaw and the pond Buraków near Warsaw. Supraœl and Dojlidy, respectively, would be the third sites of those fungal species (CZECZUGA et al. 2006b).
FUNGI ON FRUIT TREE PETALS FLOATING IN WATER
49
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