Aquatic Fungi Growing on Feathers of Wild and Domestic Bird Species in Limnologically Different Water Bodies

Abstract

The mycoflora developing on the feathers of wild and domestic bird species in the water of 6 limno-logically different water bodies was investigated under laboratory conditions. 97 zoosporic fungus species were found to grow on the feathers investigated, including 21 Chytridiomycetes, 1 Hyphochytriomycetes, 74 Oomycetes and 1 Zygomycetes fungus. The most common fungus species included Chytriomycetes annulatus, Rhizophydium keratinophilum, Blastocladiopsis parva, Catenaria anguillulae, Catenophlyctis variabilis, Aphanomyces helicoides, Aphanomyces irregularis, Leptolegniella piligena, Pythium afertile, Pythium aquatile, Pythium echinulatum, Pythium intermedium and Pythium tenue. The most fungi were noted growing in water from Cypisek spring (64), the fewest in the ponds Akcent (45) and Fosa (47 spe-cies). Out of these 97 species, 17 are known as parasites or necrotrophs of fish. 13 fungus species were recorded for the first time in Poland.

Full text

Polish Journal of Environmental Studies Vol. 13, No. 1 (2004), 21-31
Aquatic Fungi Growing on Feathers of Wild
and Domestic Bird Species in Limnologically
Different Water Bodies
B. Czeczuga*
,
A. Godlewska,
B.
Kiziewicz
Department of General Biology,
Medical University, Kilińskiego 1, 15-089 Białystok, Poland
Received: 10 April 2003
Accepted: 2 June 2003
Abstract
The mycoflora developing on the feathers of wild and domestic bird species in the water of 6 limno-
logically different water bodies was investigated under laboratory conditions. 97 zoosporic fungus species
were found to grow on the feathers investigated, including 21 Chytridiomycetes, 1 Hyphochytriomycetes,
74 Oomycetes and 1 Zygomycetes fungus. The most common fungus species included
Chytriomycetes
annulatus, Rhizophydium keratinophilum, Blastocladiopsis parva, Catenaria anguillulae, Catenophlyctis
variabilis, Aphanomyces helicoides, Aphanomyces irregularis, Leptolegniella piligena, Pythium afertile,
Pythium aquatile, Pythium echinulatum, Pythium intermedium
and
Pythium tenue
. The most fungi were
noted growing in water from Cypisek spring (64), the fewest in the ponds Akcent (45) and Fosa (47 spe-
cies). Out of these 97 species, 17 are known as parasites or necrotrophs of fish. 13 fungus species were
recorded for the first time in Poland.
Keywords:
aquatic zoosporic and keratinophilic fungi, feathers of wild and domestic birds, water bod-
ies, hydrochemical parameters
Introduction
Our preliminary studies on the aquatic keratino-
philic fungi have revealed that species composition of
this physiological group depends on the type of kera-
tin-containing substrate as well as on water bodies,
particularly on water chemism [1,2]. Since the mute
swan was the only species whose feathers, being a
keratin-containing substrate, had been examined [1],
we decided to conduct more detailed investigations
including feathers of 48 bird species, both aquatic and
land, using water samples collected from 6 different
water bodies. Moreover, fungus species of the genus
Pythium
, never before included in such studies, were
examined.
Material and
M
ethods
The feathers of 48 wild and domestic bird species
were subjected to investigation (Table 2). The feathers
(flight-feather and down) were obtained in summer from
birds occurrence in natural conditions and in the Zoologi-
cal Garden in Białystok. The water for experiments was
collected from six different water bodies:
1.
Cypisek Spring is located in the south part of Knyszyn
Forest, limnokrenic type, width 0.41 m, depth 0.17 m,
discharge 0.6 l/sek.
2.
Jaroszówka Spring is located in the northern part of
Białystok, limnokrenic type, width 0.65 m, depth 0.12
m, discharge 2.4 l/sek.
3.
Supraśl River, length 106.6 km, this is the right-bank
tributary of the middle part of the Narew River, flow-
ing through the Knyszyn Forest.
*Corresponding author; e-mail: czecz@amb.edu.pl

Czeczuga B., et al.
22
Table 1. Chemical composition (in mg l
-1
) of water from different sites (mean from 3 samples).
Parameter
Water bodies
Cypisek
Spring
Jaroszówka
Spring
Supraśl
River
Akcent
Pond
Fosa
Pond
Komosa
Lake
Temperature (
o
C)
6.0
3.8
4.5
2.3
1.4
2.8
pH
7.69
7.91
7.84
7.33
7.22
7.88
O
2
10.4
11.8
13.2
1.0
5.8
12.2
BOD
5
3.8
3.8
12.0
1.0
4.6
5.0
COD (Oxidability)
2.50
5.40
10.94
26.50
14.44
8.45
CO
2
13.2
15.4
8.8
41.8
17.6
8.8
Alkalinity in CaCO
3
(mval l
-1
)
5.2
5.9
4.4
8.2
6.1
4.3
N-NH
3
0.040
0.805
0.195
4.180
0.700
0.245
N-NO
2
0.027
0.194
0.013
0.032
0.006
0.008
N-NO
3
3.000
5.010
0.750
0.190
0.050
0.360
P-PO
4
0.800
3.565
0.750
7.080
1.245
0.735
Sulphates
50.60
54.71
19.75
91.74
47.31
32.91
Chlorides
24.0
23.0
16.0
46.0
44.0
14.0
Total hardness in Ca
117.36
123.84
79.20
150.48
101.52
79.20
Total hardness in Mg
16.77
15.48
14.19
31.82
29.67
9.89
Fe (total)
0.60
0.75
0.85
1.05
0.50
0.85
Dry residue
456
443
262
669
529
230
Dissolved solids
420
426
247
636
517
218
Suspended solids
36
17
15
33
12
12
4.
Pond Akcent, 0.45 ha, max. depth of 1.50 m, is
situated within the Zoological Garden in Białystok, in
which swans are bred and wild ducks visit.
5.
Pond Fosa, 2.5 ha, max. depth of 1.75 m, is situated
in the Palace Park in Białystok, in which crucian carp
and tench are bred.
6.
Lake Komosa, 12.1 ha, max. depth 2.25 m, is
surrounded by extensive coniferous woods of
Knyszyńska Forest.
Nineteen water parameters of the above sampling sites
were determined (Table 1) according to the methods of
Greenberg et al. [3].
For the determination of the presence of aquatic
fungal species on the feathers, the following procedure
was employed: feathers were cut into small pieces and
certain amount of pieces (100-200) of each species of
bird were transfered to two samples for each water in an
1.0 litre vessel (altogether twelve vessels for each spe-
cies) and placed in the laboratory (in glass thermostat)
at ambient temperature. A part of the pieces of feather
from each vessel was observed under a microscope and
the mycelium (zoosporic, oogonia and antheridia, and for
Saprolegnia parasitica
secondary cysts) [4]
of aquatic
fungi growing on the feather was recorded. The methods
are described in detail by Fuller
and Jaworski
[5]
. The
feathers of the various bird species were observed under a
microscope for one and a half weeks. The length of time
of the experiments was six weeks. For determination of
the fungi the following keys were used: Johnson [6],
Sparrow [7], Seymour [8], Batko [9], Karling [10], Dick
[11] and Pystina [12].
Results
Hydrochemical data of water used for the experiment
are presented in Table 1. The highest values of ammonium
nitrogen, and phosphates were found in the pond Akcent.
Spring waters appeared to be richest in nitrates and ni-
trites, as well as in calcium.
The growth of 97 zoosporic aquatic fungus species of
7 orders was observed on the feathers of 48 bird species
in the water of 6 limnologically different water bodies
(Table 3, Fig. 1). The most common species included
Chytriomycetes annulatus
and
Rhizophydium keratinophi-
lum
(Chytridiales),
Blastocladiopsis parva
,
Catenaria
anguillulae
and
Catenophlyctis variabilis
(Blastocladia-
les),
Aphanomyces helicoides
,
Aphanomyces irregularis
and
Leptolegniella piligena
(Saprolegniales) and
Leptolegniella piligena (Saprolegniales) and Leptolegniella piligena
Pythium

Aquatic Funghi Growing on...
23
Table 2. Occurrence of aquatic fungi on feathers of the investigated bird species.
Species of bird
Fungi (see Table 3)
Number
of fungus
species
1.
Accipiter gentilis
(L.) - goshawk
6,12,16,17,19,21,40,41,51
9
2.
Acrocephalus arundinaceus
(L.) -
grea reed-warbler
1,12,17,19,22,27,31,34,40,41,44,49,56
13
3.
Anas crecca
L. - teal
2,3,12,18,21,23,31,34,40,42,48,62,65,68,69,92
16
4.
Anas moschata
L. - muscovy duck
1,5,11,12,15,18,21,23,26,30,39,40,43,45,48,49,56,61,65,71,78,81,92,97
24
5.
Anas platyrhynchos
L. - mallard
1,10,12,14,15,18,20,32,40,44,48,49,50,51,56,65,66,71,72,81,92
21
6.
Anas strepera
L. - gadwall
3,8,10,12,15,16,20,21,23,25,26,29,30,39,40,49,50,51,62,65,69,71,81,82,93
25
7.
Anser anser
(L.) - greylag goose
Anser anser (L.) - greylag gooseAnser anser
1,12,14,21,30,32,35,39,40,48,49,57,69,72,80,92,93
17
8.
Anser domestica
L. - goose
5,9,10,12,14,18,20,21,26,30,39,40,48,50,56,57,61,65,71,72,80,81,92
23
9.
Ardea cinerea
L. - grey heron
3,11,12,14,18,21,29,30,32,34,39,40,46,48,62,64,68,80,90,92
20
10.
Aythya ferina
(L.) - pochard
1,2,12,14,17,18,21,29,40,41,42,60,61,62,65,69,73,76,88,92,94,95
22
11.
Aythya fuligula
(L.) - tufted duck
1,3,14,19,21,28,32,34,40,42,48,50,51,58,62,65,73,90
18
12.
Branta bernicla
(L.) - brent goose
3,5,9,12,15,20,21,25,29,30,32,39,40,49,50,51,57,65,72,86,90,92
22
13.
Bubo bubo
(L.) - eagle owl
1,5,11,12,15,20,21,39,40,49,50,56,61,65,68,72,81,92
18
14.
Buteo buteo
(L.) - common buzzard
1,3,12,17,18,21,23,31,40,41,48,49,53,56
14
15.
Ciconia ciconia
(L.) - white stork
1,5,9,12,14,15,16,17,18,21,30,34,40,42,44,50,59,62,65,66,72,90
22
16.
Ciconia nigra
(L.) - black stork
1,9,11,12,14,15,17,18,20,21,38,39,40,48,50,51,52,61,62,65,72,79,81
23
17.
Columba domestica
L. - pigeon
10,12,15,16,18,20,21,22,23,29,33,40,41,49,50,56,61,65,66,72,73,78,81,90,
92,97
26
18.
Columba palumbus
L. wood pigeon
1,11,12,15,18,21,29,30,34,40,51,53,56,61,62,65,66,72,80,81,90,92,94
23
19.
Corvus corax
L. - raven
1,17,21,23,30,39,40,42,48,53,56,61,62,65,72,92,93,97
18
20.
Corvus corone
L. - carrion-crow
1,3,8,16,17,18,21,27,41,47,49
11
21.
Corvus frugilegus
L. - rook
5,12,15,17,21,23,25,30,34,39,40,42,48,49,56,61,65,72,73,92
20
22.
Corvus monedula
L. - jackdaw
10,12,18,21,22,29,40,42,48,51,57,65,72,81,86,92,93
17
23.
Cygnus olor
(Gmel.) - mute swan
Cygnus olor (Gmel.) - mute swanCygnus olor
1,5,8,10,12,21,22,26,32,34,38,39,40,42,48,65,66,71,72,77,90,92
22
24.
Fulica atra
L. - coot
3,14,16,17,20,21,25,28,29,32,34,38,39,40,45,49,51,61,62,65,66,72,73,81,84,93
26
25.
Gallus bankiva
L. - bantam
9,12,15,16,17,18,21,25,28,39,40,43,48,50,51,57,62,65,72,81,92,93
22
26.
Gallus domesticus
L. - hen
11,12,14,15,18,21,23,34,39,40,42,44,50,53,62,65,70,72,81,92,97
21
27.
Garrulus glandarius
(L.) - jay
2,3,12,15,19,20,21,24,28,42,58,61,62,65,68,78,88,92
18
28.
Grus grus
(L.) - crane
1,3,4,9,14,20,21,41,48,50,62,65,85,91,92,95,96
17
29.
Haliaeetus albicilla
(L.) -
white-tailed eagle
1,6,12,17,18,22,23,40,41,45,48,53
12
30.
Hirundo rustica
L. - swallow
2,11,17,18,21,32,40,41,42,58,62,69,89,92
14
31.
Larus canus
L. - common gull
1,9,11,12,14,16,17,18,20,21,23,25,28,29,30,36,40,44,48,62,72,78,81,87
24
32.
Larus ridibundus
L. -
black-headed gull
1,9,12,14,21,28,40,50,51,56,61,62,65,73,77,78,81,92
18
33.
Lyrurus tetrix
(L.) - black grouse
1,3,5,9,12,20,21,28,31,34,41,42,48,50,56,62,92
17
34.
Meleagris gallopavo
L. - turkey
5,9,10,12,14,17,18,21,28,29,40,50,56,61,65,68,69,71,73,80,84,92,97
23
35.
Mergus merganser
L. - goosander
Mergus merganser L. - goosanderMergus merganser
1,10,11,12,14,15,16,17,18,20,21,28,32,34,39,40,48,50,56,59,62,81
22
36.
Mergus serrator
L. -
Mergus serrator L. - Mergus serrator
red-breasted merganser
3,14,18,21,28,31,32,37,41,42,45,50,54,65,67,73,83,92
18
Table 2 continues on next page...

Czeczuga B., et al.
24
afertile, Pythium aquatile, Pythium echinulatum, Pythium
intermedium
and
Pythium tenue
(Peronosporales). The
largest numbers of fungi were found to grow on the feath-
ers of
Streptopelia decaocto
(28), the smallest on
Accipiter
gentilis
feathers (9). In water, most fungi were found in Cy-
pisek
S
pring (64), the fewest in the ponds Akcent (45) and
Fosa (47). Such species as
Rhizophydium keratinophilum,
Rhizophydium macrosporum, Rhizophydium nodulosum,
Blastocladiopsis parva, Catenaria verrucosa, Cateno-
phlyctis variabilis, Lagenidium humanum, Aphanomyces
helicoides, Aphanomyces irregularis, Aphanomyces laevis,
Leptolegnia caudata, Saprolegnia asterophora, Pythium
acanthicum, Pythium afertile, Pythium aquatile, Pythium
intermedium, Pythium tenue
and
Zoophagus insidians
were
observed on bird feathers in all six water bodies (Table 4).
Out of these 97 species, 17 are known as parasites or necro-
trophs of fish (Table 3). 13 fungus species were recorded
for the first time in Poland.
Discussion
Most frequently, after a few days the first fungus spe-
cies appeared to grow on feathers of the birds examined,
including
Chytriomyces annulatus
and
Rhizophydium
keratinophilum
(Chytridiales),
Blastocladiopsis parva
,
Catenaria anguillulae
and
Catenophlyctis variabilis
(Blastocladiales),
Aphanomyces helicoides
.
Aphanomy-
ces irregularis
and
Leptolegniella piligena
(Saproleg-
niales) and
Pythium afertile, Pythium aquatile, Pythium
echinulatum, Pythium intermedium
and
Pythium tenue
(Peronosporales). About a week or two later the feath-
ers of a certain number of birds showed
Rhizophydium
macrosporum
and
Rhizophydium nodulosum
(Chytridi-
ales),
Catenaria verrucosa
(Blastocladiales),
Lagenidium
humanum
(Lagenidiales). At that time the feathers were
also colonized by
Achlya debaryana
,
Achlya dubia,
Achlya klebsiana, Achlya orion, Leptolegnia caudata,
Leptolegniella keratinophila, Saprolegnia asterophora
and
Saprolegnia parasitica
(Saprolegniales),
Pythium
acanthicum, Pythium rostratum, Pythium teratosporum
and
Zoophagus insidians
(Peronosporales). The remain-
ing aquatic fungus species appeared on feathers in the
final phase of the experiments.
Specificity and dissimilarity of the keratin-containing
substrate affect the colonization of a given substrate by
certain fungus species. For instance,
Aphanomyces kera-
tinophilus
was found to grow only on feathers of 8 bird
species, while on animal hair it was observed on a three
times larger number of species. This refers also to other
zoosporic fungus species [2].
In the present study more fungus species developed
on feathers in water samples collected from running water
basins (springs and the river Supraśl) than from stagnant
waters (ponds and lake Komosa). Moreover, the number
of fungus species growing on bird feathers is also affected
by the load of biogenes and organic matter, which is well
seen in the pond Akcent, where the fewest zoosporic
fungus species were observed. Such a phenomenon was
also observed while studying other physiological aquatic
fungus groups, including chitinophilic fungi [13-16] and
those growing on the eggs of freshwater fish species [17-
19]
,
on the amphibian spawn [20], on avian excrements
[21] or on the remains of plants [22]. This would explain
differences in the composition of keratinophilic fungus
species in limnologically diverse water bodies, except the
pond Akcent. A few species appeared the characteristic of
each water body, others colonized feathers only in some
of them.
Out of these 97 zoosporic fungus species which were
found to grow on the feathers, 17 are known as parasites
or necrotrophs of fresh-water fish. The most common
were species
Achlya
and
Saprolegnia
genus [17-19]. The
present study has revealed that bird feathers are the vec-
tors of many fungus species, being fish parasites.
37.
Motacilla alba
L. - white wagtail
1,10,12,14,17,20,21,23,28,29,30,32,38,39,49,40,42,49,50,56,62,65,70,72,7
9,81,92
27
38.
Pavo cristatus
L. - peacock
1,5,10,12,17,18,21,23,32,39,40,49,56,61,62,64,65,92,93
19
39.
Phalacrocorax carbo
(L.) - cormorant
1,11,12,14,15,16,20,21,28,29,38,39,40,49,50,51,61,62,65,81,82,89,90,92
24
40.
Phasianus colchicus
L. - pheasant
1,10,12,17,18,21,28,35,39,40,48,56,62,65,72,92,97
17
41.
Pica pica
(L.) - magpie
1,3,5,10,12,14,15,18,20,21,22,38,39,40,44,48,50,51,62,65,72,81,87,92,93,97
26
42.
Picus canus
Gm. -
grey-headed woodpecker
12,20,21,22,24,28,31,32,34,40,42,49,50,58,62,63,67,68,74,77,90
21
43.
Picus viridis
(L.) - green woodpecker
11,12,16,17,21,26,32,33,39,40,44,50,57,61,62,65,80,81,89,90,92,93,94,97
24
44.
Podiceps cristatus
(L.) -
great crested grebe
11,12,14,21,27,30,32,39,40,50,51,61,62,65,78,82,90,91,93,97
20
45.
Scolopax rusticola
L. - woodocock
1,12,15,17,18,19,27,40,41,47,50,56
12
46.
Sterna hirundo
L. - common tern
1,3,8,9,12,13,14,17,18,21,23,26,27,34,35,40,48,66,70,72,80,81,92
23
47.
Streptopelia decaocto
(Friv.) -
collared turtle- dove
5,11,12,17,20,21,23,28,29,32,39,40,42,44,49,50,56,65,66,71,72,73,75,77,
80,81,90,93
28
48.
Vanellus vanellus
(L.) - lapwing
1,5,7,9,12,14,15,20,21,28,31,32,34,40,42,55,58,62,69,77,83,92
22

Aquatic Funghi Growing on...
25
Table 3. Aquatic fungi found on feathers of particular birds.
Species of Fungi
Bird (see Table 2)
Number of
bird
species
Chytridiomycetes
Chytridiales
1.
Chytriomyces annulatus
Dogma
2,4,5,7,13,14,15,16,18,19,20,23,29,31,32,35,37,38,39,40,41,45,46,48
24
2.
Chytriomyces lucidus
Karling
3,10,27,30
4
3.
Chytriomyces poculatus
Willoughby et Townley
6,9,12,14,20,24,41,46
8
4.
Chytriomyces spinosus
Fay
28
1
5.
Chytriomyces stellatus
Karling
4,8,12,13,15,21,23,34,38,41,47,48
12
6.
Mitochytridium regale
Hassan
1,29
2
7.
Rhizophlyctis lovetti
Karling
48
1
8.
Rhizophydium apiculatum
Karling
6,20,23,46
4
9.
Rhizophydium condylosum
Karling
8,12,15,16,25,31,32,34,46,48
10
10.
Rhizophydium gibbosum
(Zopf) Fischer
5,6,8,17,22,23,34,35,37,38,40,41
12
11.
Rhizophydium globosum
(Braun) Rabenhorst
4,9,13,16,18,26,31,35,39,43,44,47
12
12.
Rhizophydium keratinophilum
Karling
1,2,4,5,6,7,8,9,12,13,14,15,16,17,18,21,22,23,25,26,29,31,32,34,35,
37,38,39,40,41,43,44,45,46,47,48
36
13.
Rhizophydium laterale
(Braun) Rabenhorst
46
1
14.
Rhizophydium macrosporum
Karling
5,7,8,9,15,16,24,26,31,32,34,35,37,39,41,44,46,48
18
15.
Rhizophydium nodulosum
Karling
4,5,6,12,13,15,16,17,18,21,25,26,35,39,41,45,48
17
16.
Rhizophydium piligenum
Ookubo et Kobayashi
1,6,15,17,20,24,25,31,35,39,43
11
Blastocladiales
17.
Blastocladiopsis parva
(Whiffen) Sparrow
1,2,14,15,16,19,20,21,24,25,29,31,34,35,37,38,40,43,45,46,47
21
18.
Catenaria anguillulae
Sorokin
4,5,8,9,14,15,16,17,18,20,22,25,26,29,31,34,35,38,40,41,45,46
22
19.
Catenaria sphaerocarpa
Karling
1,2,45
3
20.
Catenaria verrucosa
Karling
5,6,8,12,13,16,17,24,31,35,37,39,41,47,48
15
21.
Catenophlyctis variabilis
(Karling) Karling
1,4,6,7,8,9,12,13,14,15,16,17,18,19,20,21,22,23,24,25,25,31,32,34,
35,37,38,39,40,41,43,44,46,47,48
35
Hypochytriomycetes
Hypochytriales
22.
Hyphochytrium catenoides
Karling
2,17,22,23,29
5
Oomycetes
Leganidiales
23.
Lagenidium humanum
Karling
3,5,11,14,16,18,23,24,25,29,30,37,38
13
Saprolegniales
24.
Achlya abortiva
Coker et Braxton
27,42
2
25.
*
Achlya bisexualis
Coker et Couch
6,12,21,24,25,31
6
26.
*
Achlya caroliniana
Coker
4,6,8,23,43,46
6
27.
Achlya colorata
Pringsheim
2,20,44,45,46
5
Table 3 continues on next page...

Czeczuga B., et al.
26
28.
Achlya debaryana
Humphrey
24,25,31,32,34,35,37,39,40,47,48
11
29.
*
Achlya dubia
Coker
6,9,12,17,18,22,24,31,34,37,39
11
30.
*
Achlya klebsiana
Pieters
4,6,7,8,9,12,15,18,19,21,31,37,44
13
31.
Achlya oligocantha
de Bary
2,14,48
3
32.
*
Achlya orion
Coker et Couch
5,7,9,12,23,24,35,37,38,43,44,47,48
13
33.
Achlya papillosa
Humphrey
17,41,43
3
34.
*
Achlya polyandra
Hildebrand
2,9,15,18,21,23,24,26,35,46,48
11
35.
*
Achlya proliferoides
Coker
7,40,46
3
36.
*
Achlya racemosa
Hildebrand
31
1
37.
Achlya treleaseana
(Humphrey) Kauffman
36
1
38.
Aphanomyces amphigynus
Cutter
16,23,24,37,39,41
6
39.
Aphanomyces helicoides
Minden
4,6,7,8,9,12,13,16,19,21,23,24,25,26,35,37,38,39,40,41,43,44,47
23
40.
Aphanomyces irregularis
Scott
1,2,4,5,6,7,8,9,12,13,14,15,16,17,18,19,21,22,23,24,25,26,29,31,32,
34,35,37,38,39,40,41,43,44,45,46,47,48
38
41.
Aphanomyces keratinophilus
(Ookubo et Kobayashi)
Seym. et John.
1,2,6,14,17,20,29,45
8
42.
*
Aphanomyces laevis
de Bary
15,19,21,22,23,37,47,48
8
43.
Aphanomyces ovidestruens
Gickelhorn
4,25
2
44.
*
Aphanomyces stellatus
de Bary
2,5,15,26,31,43,47
7
45.
Aplanes androgynus
(Archer) Humphrey
4,24,29
3
46.
Cladolegnia unispora
(Coker et Couch) Johannes
9
1
47.
*
Dictyuchus sterile
Coker
20,45
2
48.
*
Leptolegnia caudata
de Bary
4,5,7,8,9,14,16,19,21,22,23,25,29,31,35,41,46
17
49.
Leptolegniella keratinophila
Huneycutt
2,4,5,6,7,12,13,14,17,20,21,24,37,38,39,47
16
50.
Leptolegniella piligena
Ookubo et Kobayasi
1,5,6,8,12,13,15,16,17,25,26,32,34,35,37,39,41,43,44,45,47
21
51.
Saprolegnia asterophora
de Bary
5,6,12,16,18,22,24,25,32,39,41,44
12
52.
Saprolegnia eccentrica
(Coker) Seymour
16
1
53.
*
Saprolegnia ferax
(Gruith.) Thuret
14,18,19,26,29
5
54.
Saprolegnia glomerata
(Tiesenhausen) Lund
36
1
55.
*
Saprolegnia monoica
Pringsheim
48
1
56.
*
Saprolegnia parasitica
Coker
2,4,5,8,13,14,17,18,21,32,34,35,37,38,40,45,47
17
57.
*
Saprolegnia subterranea
(Dissmann) Seymour
8,12,22,25,43
5
58.
Sommerstorf a spinosa
Arnaudow
11,27,30,42,48
5
Leptomitales
59.
Apodachlya brachynema
(Hildebrand) Pringsheim
15,35
2
Peronosporales
60.
Nematosporangium epiphanosporon
Sideris
10
1
61.
Pythium acanthicum
Drechsler
4,8,13,16,17,18,19,21,24,32,34,38,39,43,44
15
Table 3 continues on next page...

Aquatic Funghi Growing on...
27
62.
Pythium afertile
Kanouse et Humphrey
6,9,15,16,18,19,24,25,26,31,32,35,37,38,39,40,41,43,44,48
20
63.
Pythium akanense
Tokunaga
42
1
64.
Pythium angustatum
Sparrow
9,38
2
65.
Pythium aquatile
Höhnk
4,5,6,8,12,13,15,16,17,18,19,21,22,23,24,25,26,32,34,37,38,39,40,41,
43,44,47
27
66.
Pythium aristosporum
Vanterpool
5,15,17,18,24,37,46,47
8
67.
Pythium arrhenomanes
Drechsler
36
1
68.
*
Pythium artotrogus
de Bary
9,13,34
3
69.
Pythium butleri
Subramaniam
6,7,34,48
4
70.
Pythium catenulatum
Matthews
26,37,46
3
71.
Pythium deliense
Meurs
4,5,6,8,23,34,47
7
72.
Pythium echinulatum
Matthews
5,7,8,12,13,15,16,17,18,19,21,22,23,24,25,26,31,37,40,41,46,47
22
73.
Pythium elongatum
Matthews
17,21,24,32,34,47
6
74.
Pythium erihaceus
Robertson
42
1
75.
Pythium gracile
Schenk
47
1
76.
Pythium hemmianum
Takahashi
10
1
77.
Pythium helicandrum
Drechsler
23,32,47,48
4
78.
Pythium imperfectum
Höhnk
4,17,31,32,44
5
79.
Pythium indicum
Balakrishman
16,37
2
80.
Pythium in atum
Matthews
7,8,9,18,34,43,46,47
8
81.
Pythium intermedium
de Bary
4,5,6,8,16,17,18,22,24,25,26,31,32,35,37,39,41,43,46,47
20
82.
Pythium jirovecii
Cejp
6,39,44
3
83.
Pythium maritimum
Höhnk
36,48
2
84.
Pythium myriotylum
Drechsler
24,34
2
85.
Pythium oedochilum
Drechsler
28
1
86.
Pythium oligandrum
Drechsler
12,22
2
87.
Pythium periilum
Drechsler
31,41
2
88.
Pythium perniciosum
Serbinow
10,27
2
89.
Pythium polysporum
Sorokin
39,43
2
90.
Pythium rostratum
Butler
9,12,15,17,18,23,39,43,44,47
10
91.
Pythium splendens
Braun
28
1
92.
Pythium tenue
Gobi
4,5,7,8,9,12,13,17,18,19,21,22,23,25,26,32,34,37,38,39,40,41,43,44,
46,48
26
93.
Pythium teratosporum
Sideris
6,7,19,22,24,25,38,41,43,44,47
11
94.
Pythium torulosum
Coker et Patterson
18,43
2
95.
Pythium undulatum
Petersen
10,28
2
96.
Rheosporangium aphanidermatum
Edson
28
1
Zygomycetes
Zoopagales
97.
Zoophagus insidians
Sommerstorff
4,17,19,26,34,40,41,43,44
9
*species known in literature as parasites or necrotrophs of fish

Czeczuga B., et al.
28
Fig. 1. Some keratinophilic (A) and non-keratinophilic (B, C, D) fungus species growing on the feathers (x 200).
A –
Aphanomyces irregularis
– hyphae from oogonia (15-25 μm); B –
Saprolegnia ferax
– discharge sporangium; C –
Saprolegnia
glomerata
– hyphae (10-40 μm diameter) from oogonia (46-58 μm); D –
Saprolegnia parasitica
– hyphae (30-120 μm diameter) from
oogonia (62-75 μm)
A
B
C
D
Worth noting is the finding of five Chytridiales rep-
resentatives, new to Polish waters, namely
Chytriomyces
lucidus, Chytriomyces spinosus, Chytriomyces stellatus,
Rhizophydium gibbosum
and
Rhizophlyctis lovetti
, on
the feathers of several bird species in almost all water
samples used in the experiment. In the literature of the
subject
Chytriomyces lucidus
and
Chytriomyces stel-
latus
was described by Karling
[23]
in Maryland and
are known as a saprophyte, but not of such substrates as
bird feathers [10]
.
Chytriomyces spinosus
was found on
the feathers of
Grus grus
in the water of Cypisek
S
pring
only. This fungus was first isolated by Fay [24]. The water
of Cypisek is characterized by a comparatively low con-
tent of ammonium nitrogen. Water of this spring had the
lowest oxidability (COD).
Rhizophydium gibbosum
was
described already at the end of the 19
th
century as a para-
site of algae [25]. It is also known as a parasite of rotifers
and their eggs [9]
.
Rhizophlyctis lovetti
was found on the
feathers of
Vanellus vanellus
in the springs Cypisek and
Jaroszówka. This fungus was first isolated in India on hu-
man fibrin film as bait by Karling [26].
Also new to Polish waters is
Achlya abortiva
, which
was found on the feathers of
Garrulus glandarius
and
Picus canus
only in the water of pond Akcent. The
water of pond Akcent had the lowest content of oxygen
and BOD
5
but by the largest amounts of CO
2
, ammo-
nium nitrogen, phosphates, sulphates, chlorides, calcium,
magnesium and iron. Water of this pond had the highest
oxidability (COD) and alkalinity. This fungus was first
isolated as a soil saprophyte [27].
The feathers of certain bird species showed a number
of Peronosporales representatives, never before observed
on such a substrate. The most common fungus species en-
countered on feathers included
Pythium afertile, Pythium
aquatile, Pythium echinulatum, Pythium intermedium
and
Pythium tenue
. These species are observed mostly on the
substrates of plant origin, only
Pythium echinulatum
is
known as an animal saprophyte growing on freshwater
fish eggs [28].
Nematosporangium epiphanosporon
and
among the species of the genus
Pythium
colonizing bird
feathers
Pythium angustatum, Pythium deliense, Pythium
hemmianum, Pythium indicum, Pythium teratosporon
and
Rheosporangium aphanidermatum
are new to Polish
waters.
Nematosporangium epiphanosporon
was found
to grow only on feathers of
Aythya ferina
in Cypisek,
was described by Sideris [29] from the diseased roots of
Ananas sativa
grown on the island of Oahu of the Hawai-
ian Archipelago.
Pythium angustatum
was found on the
feathers of
Ardea cinerea
and
Pavo eristatus
in Jaroszów-
ka
S
pring. The water of Jaroszówka was found to have a
high content of nitrate and nitrite nitrogen and highest pH.
This fungus was first isolated as a parasite of green algae

Aquatic Funghi Growing on...
29
of the genus
Spirogyra
[30].
Pythium deliense
, which
colonized feathers of 7 bird species in the spring Cypisek
and lake Komosa, was described from Sumatra as caus-
ing stemburn in
Deli tobacco
[31].
Pythium hemmianum
was first isolated as causing a damping off of seedlings of
Luffa cylindrica
at Kamigano pref., Kyoto by Takahashi
[32]. This fungus was found to grow on the feathers of
Aythya ferina
in water of all water bodies except Cypisek
S
pring.
Pythium indicum
was found to grow on the feathers
of
Ciconia nigra
and
Motacilla alba
only in the water of
lake Komosa. It was described in India by Balakrishnan
[33] from fallen fruits of
Hibiscus esculentu
s. The water
of lake Komosa is characterized by a comparatively low
content of CO
2
, calcium, chlorides and magnesium. Water
of this lake had the lowest alkalinity.
Pythium teratospo-
ron
, found to colonize feathers of 11 bird species in the
water of all water bodies exscept lake Komosa, was
first isolated on Hawaii from diseased roots of
Spinacea
oleracea
[34].
Rheosporangium aphanidermatum
was
found on the feathers of
Grus grus
in the pond Fosa. This
fungus was described in Wisconsin (USA) by Edson [35]
from damped - off seedlings of sugar beet
Beta vulgaris
.
The water of pond Fosa was found to have a low content
of nitrate and nitrite nitrogen and iron. Water of this pond
had the lowest temperature and pH.
Moreover, worth noting is the finding of two inter-
esting fungus species
Mitochytridium
regale
and
Som-
merstorffia spinosa
on the feathers of several bird spe-
cies. The former was encountered on
Accipiter gentilis
and
Motacilla alba
in the water of Jaroszówka
S
pring,
Supraśl
R
iver, and ponds Akcent and Fosa.
Mitochy-
tridium regale
was first described by Hassan [36] as kera-
tinophilic waters fungus in the pond in the Łazienki Park
of Warsaw. This fungus was reported for the second time
in Poland from lake Necko [37].
Sommerstorffia spinosa
was observed on the feathers of
Aythya fuligula, Garrulus
glandarius, Hirundo rustica, Picus canus
and
Vanellus
vanellus
in water of pond Fosa only. This fungus is a
relatively rare predacious fungus catching rotifers. It has
been mainly isolated from soil samples more seldom from
water [38]. We have shown its growth in spring, rivers,
ponds and lakes of varied trophic states [39].
Keratin, a protein belonging to scleroids, is the main
component of bird feathers. The compound, insoluble in
water, is very resistant to the action of different chemical
compounds and proteolytic enzymes. Keratin is made of
cysteine and cystine (3-15%), and alkaline amino acids.
The first two play a role in the formation of protein struc-
ture, showing the ability to form permanent disulphide
bindings between the respective twisting of the peptide
chain or separate chains. If the amount of cysteine and
cystine increases, keratin becomes more resistant to
enzymatic hydrolysis [40, 41]. The secondary structure
of keratin is characterized by a parallel arrangement of
numerous fibres composed of polypeptide chains, each
assuming the form of differently extended L-helix. The
respective helixes are additionally mutually twisted like
a “ship rope”. The structure so arranged is maintained by
means of numerous disulphide bindings formed due to a
substantial content of cysteine and cystine in this protein;
it determines mechanical strength of keratin-built fibres.
Bird feathers and mammalian hair are built of keratin,
in which cysteine and cystine content reaches 15%. As
it is known, keratin containing large amounts of these
two amino acids easily bind with heavy metals, which
in turn considerably inhibit enzymatic activity of fungi
[42]. This is perhaps one of many factors that influence
Table 4. Aquatic fungi found on the feathers in the water from different water bodies.
Water bodies
Fungi (see Table 3)
Only in one
water
Number of
fungus species
Cypisek Spring
1, 2, 3, 4, 5, 7, 8, 9, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 23, 28, 29, 30, 32,
34, 35, 37, 39, 40, 41, 42, 43, 44, 45, 48, 50, 51, 56, 57, 59, 60, 61, 62, 63,
65, 66, 68, 69, 70, 71, 72, 73, 77, 80, 81, 83, 84, 86, 87, 90, 91, 92, 93, 94, 97
4, 13, 35, 37,
60, 63, 83, 87,
91, 94
64
Jaroszówka Spring
1, 2, 3, 5, 6, 7, 8, 9, 10, 11, 12, 14, 15, 16, 17, 18, 19, 20, 21, 23, 25, 26, 27,
29, 30, 38, 39, 40, 41, 42, 43, 44, 48, 49, 50, 51, 53, 56, 61, 62, 64, 65, 67,
68, 70, 72, 73, 75, 77, 78, 81, 82, 86, 90, 92, 93, 97
27, 64, 75
57
Supraśl River
1, 3, 5, 6, 8, 9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 23, 25, 26, 28, 29,
33, 34, 36, 39, 40, 41, 42, 44, 45, 48, 49, 50, 51, 52, 55, 56, 59, 61, 62, 65,
66, 68, 69, 70, 72, 73, 74, 77, 78, 80, 81, 85, 89, 90, 92, 93, 97
33, 36, 52, 55,
74, 85
60
Akcent Pond
1, 2, 5, 6, 9, 10, 11, 12, 14, 15, 17, 18, 19, 20, 21, 22, 23, 24, 25, 28, 29, 30,
31, 38, 39, 40, 41, 42, 44, 48, 49, 50, 51, 56, 57, 61, 62, 65, 67, 68, 72, 81,
92, 93, 97
24
45
Fosa Pond
1, 3, 5, 8, 9, 10, 11, 12, 14, 15, 17, 20, 21, 22, 23, 28, 29, 30, 31, 32, 34, 39,
40, 41, 42, 44, 47, 48, 50, 51, 54,58, 61, 62, 65, 69, 72, 73, 76, 78, 81, 90, 92,
93, 95, 96, 97
47, 54, 58,
76, 96
47
Komosa Lake
1, 3, 5, 6, 9, 10, 11, 12, 14, 15, 16, 17, 18, 19, 20, 21, 23, 25, 30, 39, 40, 41,
42, 44, 45, 46, 48, 49, 51, 53, 56, 57, 61, 62, 65, 68, 69, 71, 72, 78, 79, 81,
82, 84, 88, 89, 90, 92, 95, 97
46, 79, 88
50

Czeczuga B., et al.
30
the number of fungus species growing on feathers of
bird species examined. In the present study, the smallest
number of fungus species developed on the feathers of the
predacious goshawk (
Accipiter gentilis
predacious goshawk (Accipiter gentilispredacious goshawk (
), the largest num-
ber on the feathers of collared turtle-dove (
Streptopelia
decaocto
). The goshawk is known to be the terminal link
in the longer alimentary chain as the second or even third
degree consumer, compared with the turtle-dove, a first
degree consumer. The longer the alimentary chain is, the
more heavy metals accumulate in its terminal link [43]. It
is no doubt that the number of fungus species growing on
feathers depends on some other factors, such as the struc-
ture of protein forming the keratin-containing substrate,
its melanin content [2] or trophicity of water reservoir.
The more polyor eutrophic the water is, the fewer fungi
grow on different substrates of animal origin [1,2,13-20].
In water, feathers of domestic fowl (a waste product in
farming) or those from moulting wild fowl and mamma-
lian hair are immediately colonized by bacteria [44] and
saprophytic fungi [45]. The latter use feathers or fur as a
substrate which provides carbon, nitrogen, and sulphur,
but first of all as a source of energy [46]. By means of
broad-substrate keratinases [47], they decompose these
substrates to obtain smaller and smaller peptides [48-50]
until complete keratin dissolution occurs. A number of
non-keratinophilic fungi can be observed on smaller frag-
ments of peptide chains formed (Fig. 1) as the result of
decomposition by keratinophilic fungi [51]. In our study,
this group of non-keratinophilic fungi consisted of numer-
ous species belonging to Oomycetes, including a number
of fish parasites and necrotrophs, as well as a predacious
fungus
Sommerstorffia spinosa
, but first of all a consider-
able number of
Pythium
species, which lead a parasitic
life on the conidia of many plant species [12].
Finally, it should be stated that aquatic zoosporic fun-
gus species substantially contribute to the mineralization
of insoluble in water protein substrates, with keratin as
the basic component, and thus play an important role in
the self-purification of water in natural reservoirs and in
various types of treatment plants [52,53].
Acknowledgement
The authors wish to thank the staff of the Zoological
Garden, Białystok for help in obtaining the material.
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