Aquatic insects as vectors of aquatic zoosporic fungi parasitic on fishes

Abstract

The authors investigated aquatic insects (32 species) as vectors of aquatic zoosporic fungi parasitic on fishes in six bodies of water of various trophic state. A total of 127 zoosporic fungus species were noted, with predominance by the Oomycetes (99) and Chytridiomycetes species (24). Out of these 127 species, 28 are known as parasites or necrotrophs of fishes.

Full text

ACTA ICHTHYOLOGICA ET PISCATORIA
Abbrev.: Acta Ichthyol. Piscat. 31 (2): 87-104, Ann. 2001
Bazyli CZECZUGA, Anna GODLEWSKA
Fungi on fishes
AQUATIC INSECTS AS VECTORS OF AQUATIC ZOOSPORIC FUNGI
PARASITIC ON FISHES
OWADY WODNE JAKO WEKTORY ZOOSPOROWYCH GRZYBÓW
PASOŻYTNICZYCH RYB
Department of General Biology, Medical University, Białystok, Poland
The authors investigated aquatic insects (32 species) as
vectors of aquatic zoosporic fungi parasitic on fishes in six
bodies of water of various trophic state. A total of 127 zoo-
sporic fungus species were noted, with predominance by the
Oomycetes (99) and Chytridiomycetes species (24). Out of
these 127 species, 28 are known as parasites or necrotrophs of
fishes.
INTRODUCTION
Mass mortalities of fishes, salmonids in particular, caused by the extensive growth of
certain zoosporic fungus species have been known since the second half of the 19th century
(Stirling 1880). Recent studies have revealed that these species grow also on other aquatic
organisms, both alive and dead (Czeczuga et al. 1998), being the source of infection for
fishes. Fish parasitic fungi occur on plankton crustaceans (Czeczuga et al. 2000), pelagic
inhabitants, as well as on such benthic organisms as crustaceans (Czeczuga et al. 1999b)
and shellfish (Czeczuga 2000) and even on avian excrements (Czeczuga and Mazalska
2000). A number of aquatic insect species or their developmental forms can be found in the
littoral zone of lakes where fishes lay the eggs and where fry remain for a certain period of
time. Therefore we have decided to investigate which aquatic insect species can be the
source of mycotic infection causing fish death.

88
Bazyli Czeczuga, Anna Godlewska
I.
MATERIAL AND METHODS
Specimens of 32 aquatic insects species (Table 2) were collected from Białystok dis-
trict, they were then killed by decapitation and experimental observations began the next
day.
The water for experiments was collected from six different water bodies:
Spring Cypisek, limnokrenic type; width 0.41 m, depth 0.17 m, discharge 0.6 dm3*s-1,
is in the southern part of the Knyszynska Forest.
II. Spring Jaroszówka, limnokrenic type, width 0.65 m, depth 0.12 m, discharge
2.4 dm3*s-1, is in the northern part of Białystok, without trees.
III. River Supraśl, length 106.6 km, is the right-bank tributary of the middle part of the
Narew River, flowing through the Knyszynska Forest.
IV. Lake Komosa, 12.1 ha, max. depth 2.25 m, is surrounded by the densely-growing co-
niferous trees of the Knyszynska Forest.
V. Pond Akcent, 0.45 ha, max. depth 1.50 m, is a habitat of wild ducks and breeding
swans.
VI. Pond Fosa, 2.5 ha, max. depth 1.75 m, situated in the Palace Park—is a habitat of wild
ducks and breeding swans, as well as crucian carp and tench bred for anglers.
Nineteen parameters of these samples were determined (Table 1) according to the
methods of Greenberg et al. (1992).
Table 1
Chemical properties (in mg*dm-3) of water in particular water bodies (n = 5)
Specification
Temperature (°C)
pH
O2
BOD5
COD (Oxidability)
C02
Alkalinity in CaCO3 (mval-dm-3)
N-NH3
N-NO2
N-NO3
P-PO4
Sulphates
Chlorides
Total hardness in Ca
Total hardness in Mg
Fe
Dry residue
Dissolved solids
Suspended solids
Spring
Cypisek
7.8
7.78
8.20
3.20
4.30
15.40
5.20
0.280
0.014
0.080
0.530
25.54
28.00
105.80
21.07
0.007
473.0
461.0
12.0
Spring
Jaroszówka
5.7
7.86
9.40
5.60
5.58
12.20
2.30
0.290
0.020
0.010
0.680
19.33
15.00
110.16
15.19
0.050
465.0
354.0
111.0
River
Supraśl
5.4
7.88
9.20
5.80
7.84
11.95
5.10
0.250
0.005
0.070
0.530
20.16
36.05
72.25
15.91
0.050
242.0
222.0
20.0
Pond
Akcent
7.0
7.77
2.20
1.80
12.54
24.20
7.40
3.530
0.012
0.090
12.720
89.27
49.15
97.52
12.93
0.525
640.0
606.0
34.0
Pond
Fosa
7.2
7.61
3.65
0.50
22.97
18.80
4.50
1.500
0.007
0.900
1.670
39.08
52.15
56.16
11.50
0.450
444.0
433.0
11.0
Lake
Komosa
6.5
7.86
9.42
5.40
8.02
8.82
5.10
0.140
0.005
0.012
0.450
29.62
10.14
73.44
14.19
0.050
280.0
261.0
19.0

Table!
Insect species investigated and fungi found on this insects

Table 2 (cont.)
* Numbers in parenthesis designate the total number of parasites or necrotrophs

Aquatic insects as vector of fungi parasitic on fishes
91
To determine the presence of aquatic fungi on the insects, the following procedure
was employed: 10-15 small fragments of each species insect were transferred to each two
samples for each water basin in a 1-dm3 vessel (altogether twelve vessels for each species)
and placed in a glass tank (50 x 75 x 75 cm) at ambient temperature in the laboratory.
Some pieces of insects from each vessel were observed under a microscope and the myce-
lium (zoosporic and oogonia and for Saprolegnia parasitica secondary cysts) of aquatic
fungi growing on the insects was recorded. The methods are described in detail by Fuller
and Jaworski (1986). The pieces of various insect species were observed under a micro-
scope once a week, and each experiment lasted three weeks.
To identify the fungi, keys by Johnson (1956), Sparrow (1960), Waterhouse (1967,
1968), Seymour (1970), Batko (1975), Karling (1977), Dick (1990), and Pystina (1998)
were used.
RESULTS
Hydrochemical parameters of water used for the experiment are presented in Table 2.
The highest values of ammonium nitrogen and phosphates were found in pond Akcent and
Fosa. Springs water appeared to the richest in nitrites, as well as in calcium.
We found 127 zoosporic aquatic fungus species on the fragments of 32 aquatic in-
sects species (Table 3). The least colonised were the fragments of Anex imperator larvae
(Odonata) and adult individuals of Hydroporus palustris (Coleoptera) (13 in each case),
while the most colonised were the fragments of adult specimens of Nepa cinerea (Hemi-
ptera) (37 species). Fourteen species have appeared new to Polish waters.
Table 3
Aquatic fungi found on the insects
Taxa fungi
Chytridiomycetes
Olpidiales
1. Blastulidium phaedophthorum Perez
2. Myiophagus ucrainica (Wize) Sparrow
Chytridiales
3. Asterophlyctis irregularis Karling
4. Asterophlyctis sarcoptoides Petersen
5. Chytriomyces attreus Karling
6. Chytriomyces hyalinus Karling
7. Diplophlyctis intestina (Schenk) Schroeter
8. Karlingia chitinophila Karling
9. Phlyctochytrium aureliae Ajello
Insect (see Table 2)
12
13
4,14,20,30
9
1,4,7,8,14,24,27,28,30,32
6,9,10,11,21,28,29
11,14,31
1,2,4,7,10,11,15,18,22,23,27
1,3,8,9,14,19,24,26,32
No of
species
1
1
4
1
10
7
3
11
9

Table3 (cont.)
Taxa fungi
10. Podochytrium chitinophilum Willoughby
11. Podochytrium clavatum Pfitzer
12. Polychytrium aggregatum Ajello
13. Rhizidiwn chitinophilum Sparrow
14. Rhizidiwn nowakowskii Karling
15. Rhizidium ramosum Sparrow
16. Rhizophydium globosum (Braun) Rabenhorst
17. Rhizophydium macrosporum Karling
1 8. Rhopalophlyctis sarcoptoides Karling
19. Siphonaria variabilis Petersen
Blastocladiales
20. Blastocladiella britannica Horenstein et Cantinc
21. Blastocladiopsis parva (Whiffen) Sparrow
22. Catenophlyctis variabilis (Karling) Karling
23. Coelomomyces lativittatus Couch et Dodge
24. Coelomomyces pentagulatus Couch
Hyphochytriomycetes
Hyphochytriales
25. Rhizidiomyces bivellatus Nabel
26. Rhizophlyctis petersenii Sparrow
Oomycetes
Lagenidiales
27. Lagenidium giganteum Couch
28. Lagenidium podbielkowski Batko
29. Lagenidium rabenhorstii Batko
30. Myzocytium megastomum de Wildeman
31 . Myzocytium microsporum (Karling) Sparrow
32. Myzocytium zoophthorum Sparrow
Saprolegniales
33.* Achlya ambisexualis Raper
34*Achlya americana Humphrey
35.* Achlya apiculata de Bary
36.* Achlya bisexualis Coker et Couch
37. Achlya cambrica (Trow) Johnson
38.* Achlya caroliniana Coker
39. Achlya colorata Pringsheim
40. Achlya crenulata Ziegler
4 1 . Achlya debaryana Humphrey
42.* Achlya diffusa Harvey et Johnson
43* Achlya dubia Coker
Insect (see Table 2)
14,16
4,14
10,21
2,3,4,5,6,9,11,12,13,14,15,16,
17,18,19,20,21,22,26,27,32
12
2,5,23
7,29
9,16,30
8,10
6,9,11,20,27
3,6,8,9,19,27,29,30
5
5,18
3,19
14,18,31
3,4,6,7,14,16,18,19
5
4,11,25
12,18,29
12
18
18,31
4,5,12,32
10,15,18,20
1,3,6,7,9,10,11,13,14,16,18,19,20,
21,22,23,24,25,26,27,28,29,30,31
8,20,23,24,28
30
19
1,2,5,7,9, 15
3,6,15,18,19
3,7,13,14,18,19,26,31
6,9,
1 0, 1 8,20,22,23,24,28,29,30
1,5,6,9,11,16,20,21,25,30,32
1,3,6,8,9,1 1,18,19,20,22,23,24,
25,27,28,29,30,32
No of
species
2
2
2
21
1
3
2
3
2
5
8
1
2
2
3
8
1
3
3
1
1
2
4
4
24
5
1
1
6
5
8
11
11
18

Table 3 (cont.)
Taxa fungi
44.* Achlya ßagellata Coker
45. Achlya hypogyna Coker et Pemberton
46. Achlya inflata Coker
41.* Achlya klebsiana Pieters
48. Achlya megasperma Humphrey
49. Achlya oblongata de Bary
50. Achlya oligacantha de Bary
51 * Achlya orion Coker et Couch
52.* Achlya polyandra Hildebrand
53.* Achlya prolifera Nees
54.* Achlya proliferoides Coker
55.* Achlya racemosa Hildebrand
56. Achlya rodriguesiana F.T. Wolf
57. Achlya treleaseana (Humphrey) Kauffman
58. Aplanes androgymts (Archer) Humphrey
59. Aphanomyces amphigynus Cutter
60. Aphanomyces astai Schikora
61 . Aphanomyces daphniae Prowse
62. Aphanomyces helicoides Minden
63 . Aphanomyces irregularis Scott
64.* Aphanomyces laevis de Bary
65.* Aphanomyces stellatus de Bary
66. Cladolegnia spiralis (Cornu) Johannes
67. Cladolegnia imispora (Coker et Couch)
Johannes
68. Dictyuchus magnusii Lindtstedt
69.* Dictyuchus monosporus Leitgeb.
70.* Dictyuchus sterile Coker
71.*Isoachlya monilifera (de Bary) Kauffman
72.*Leptolegnia caudata de Bary
73. Saprolegnia anisospora de Bary
74. Saprolegnia asterophora de Bary
75. Saprolegnia delica Coker
76.* Saprolegnia diclina Humphrey
77. Saprolegnia eccentrica (Coker) Seymour
Insect (see Table 2)
3,7,10,16,19,20,24
25
9
1,3,8,9,14,19,21,22,26,27,28,29,32
6,13,24,25,32
4,13,32
10,11,24,26,27,32
1,3,4,6,8,11,16,17,18,19,23,24,30
1 ,4,6,9, 1 0, 1 1 , 1
7,20,23,24,25,26,27
,28,29,30,32
1,3,4,5,6,7,13,19,24,25,27,32
1,2,3,4,8,9,11,12,14,15,19,20,21,
23,24,25,27,28,30,32
7,12,26
4.16
7,8,21,22,23,28
1,7,8,9,10,12,14,15,24,29,32
7,20,23
29
12,13
3,6,18,19,26,32
1,2,4,5,6,9,10,11,14,15,16,17,18,
20,22,23,24,25,27,28,30,31
1,3,4,5,6,9,10,11,15,16,17,18,19,
20,21,24,26,27,28,29,30,31,32
2,3,5,6,7,9,19,30
28
1,3,5,7,9,10,13,15,17,19,20,23,24,
25,27,28,32
3,19
20
3,6,7,8,9,14,16,18,19,21,22,23,26,
27,29,30,31
1,2,3,4,8,9,16,19,23,24,25,27
4,7,10,11,14,15,20,26,32
1,6,8,9,11,14,27,29,32
2,5,10,14,28,29
1,5,9,10,11,14,16,23,24,25,26,27,
30,32
6,13,25
6,7
No of
species
7
1
1
13
5
3
6
13
17
12
20
3
2
6
11
3
1
2
6
22
23
8
1
17
2
1
17
12
9
9
6
14
3
2

Table 3 (cont.)
Taxa fungi
78.*Saprolegnia ferax (Gruith.) Thuret
79. Saprolegnia glomerata (Tiesenhausen) Lund
80. Saprolegnia hypogyna (Pring.) de Bary
81. Saprolegnia latvica Apinis
82. Saprolegnia litoralis Coker
83.* Saprolegnia monoica Pringsheim
84. Saprolegnia papillosa (Humphrey) Apinis
85.* Saprolegnia parasitica Coker
86. Saprolegnia pseudocrnstosa Lund
87.* Saprolegnia subterranea Dissmann
88. Saprolegnia terrestris Cookson et Seymour
89. Saprolegnia torulosa de Bary
90. Saprolegnia uliginosa Johannes
9\.*Traustotheca clavata (de Bary) Humphrey
Leptomitales
92. Apodachlya pyrifera Zopf
Peronosporales
93. Phytophthora fischeriana (Höhnk) Sparrow
94. Pythium acanthicum Drechsler
95. Pythium afertile Kanouse et Humphrey
96. Pythium aquatile Höhnk
97. Pythium aristosporum Vanterpool
98. Pythium arrhenomanes var. philippinense Roldan
99. Pythium butleri Subramaniarn
100. Pythium cactacearum Preti
101. Pythium calenulalum Matthews
102.. Pythium debaryanum Hesse
103. Pythium deliense Meurs
104. Pythium dissotocum Drechsler
105. Pythium elongatum Matthews
106. Pythium epigynum Höhnk
107. Pythium equiseti Sadebeck
108. Pythium globosum Schenk
109. Pythium graminicola Subramaniam
110. Pythium helicandrum Drechsler
Insect (see Table 2)
1,3,4,5,6,7,8,9,10,11,12,13,14,
15,16,17,18,19,20,21,23,24,25,
26,27,28,29,30,31,32
6,8,9,11,14,20,21,23,25,26,28,30
9,26
3,9,14,19,22,25,26,29
6,29
9,10,15,18,20,23,24,26
1,16,18,23,30
1,4,5,6,7,8,10,11,12,15,16,18,
19,20,21,22,23,24,25,26,27,28,
29,32
6,8
9
28
1
,4,5,6,7,8,9,
10, 11,
14,20,22,23,2
7,28,29,32
8,14,26,28,32
1,3,8,9,15,19,23,24,32
20
23
2,10,14,18,25,26,27,28,29
5,11,16,18,19,20,23,28,30
1,5,6,7,8,9,11,12,15,16,17,18,
21,23,24,25,27,29,30
26
11
1,2,3,5,11,16,17,19,20,30
10
6,25
5,8,21,22
23,28
9,13
4,5,7,10,13,15,20,26,31
10
6
12
13
1, 14,
16,20,24,27,28,29,30,31
No of
species
30
12
2
8
2
8
5
24
2
1
1
17
5
9
1
1
9
9
19
1
1
10
1
2
4
2
2
9
1
1
1
1
10

Aquatic insects as vector of fungi parasitic on fishes
95
Table 3 (cont.)
Taxa fungi
111. Pythium imperfectum Höhnk
112. Pythium inflation Matthews
113. Pythium jirovecii Cejp
114. Pythium myriotylum Drechsler
115. Pythium oedochilum Drechsler
116. Pythium polysporum Sorokin
117.* Pythium proliferum Schenk
118. Pythium rostratum Butler
119. Pythium salpingophorum Drechsler
120. Pythium tardicrescens Vanterpool
121. Pythium tenue Gobi
122.* Pythium ultimum Trow
123. Pythium undulatum Petersen
124. Pythium volutum Vanterpool
125. Rheosporangium aphanidermatus Edson
Zygomycetes
Zoopagales
126. Zoophagus insidians Sommerstorff
127. Zoophthora rhizospora (Thaxter) Batko
Insect (see Table 2)
8,10,11,16,20,28,30
1,5,8,9,10,11,18,28,31
3,19,20,21,23
1,11,12,13,22,27
7,9,26,31
1,2,5,11,13,28,32
11
11,16,23,26
5
27
6,7,18,23,24,30
1,5,7,9,15,29
25
1,11,30
16
5,11,17,24,28
No of
species
7
9
5
6
4
7
1
4
1
1
6
6
1
3
1
1
5
* Known in literature as parasites or necrotrophs of fish.
The most aquatic fungus species were found on aquatic insects in spring water
(Cypisek 89, Jaroszówka 80 species), the fewest in pond water (Akcent 32, Fosa 61 spe-
cies—Table 4). Out of these 127 species, 28 are known as parasites or necrotrophs of
freshwater fishes. The most common fungus species included Rhizidium chitinophilum,
Achlya americana, Achlya dubia, Achlya polyandra, Achlya proliferoides, Aphanomyces
irregularis, Aphanomyces laevis, Cladolegnia unispora, Dictyuchus sterilis, Saprolegnia
ferax, Saprolegnia parasitica, Saprolegnia torulosa, and Pyhium aquatile were found on
the fragments of most insects species examined.
DISCUSSION
The present study has revealed that aquatic insects are a good substratum for the
growth of 127 aquatic zoosporic fungus species, including a number of species of fish
parasites new to Polish waters.

Table 4
Aquatic fungi found on the insects in different water
Water from
Cypisek Spring
Jaroszówka Spring
Supraśl River
Komosa Lake
Akcent Pond
Fosa Pond
Fungi (see Table 3)
3,5,6,7,8,9,
10,
11
, 13, 18,
19,20,21 ,22,24,25,30,31
,33
,34,3 8,39,41 ,42,43,47,
49,50,51,52,53,55,56,57,58,59,60,61,62,63,64,65,67,69,70,71,73,74,75,77,
78,79,80,82,83,85,86,88,89,90,91 ,92,93 ,94,95,96,99,
101
,
102, 103, 104, 105,
106,107,110,111,112,114,115,116,121,122,124,126,127
2,4,5,6,7,8,9,10,11,13,15,20,24,25,26,31,33,34,35,37,38,39,40,41,42,43,
44,47,48,49,50,51,52,53,54,56,57,58,63,64,65,67,68,70,71,72,74,75,76,78,
79,80,81 ,82,83,85,86,87,89,90,91 ,94,95,96,98,99, 103, 104, 105, 106, 107, 109,
1
10,112,113,115,116,122
3,5,6,8,9,10,13,16,17,20,25,26,28,34,35,36,38,39,41,42,43,44,45,46,47,48,
50,51,52,53,54,56,58,59,60,62,63,64,65,66,67,70,71,72,73,75,78,79,81,83,
85,89,90,91,94,95,96,97,100,101,105,110,112,116,118,119,121,122
1,3,7,8,13,14,15,16,19,25,26,28,29,31,32,33,34,35,33,41,43,44,47,48,49,50,5
1,52,53,54,56,58,59,61,62,63,64,67,70,71,72,73,74,75,76,77,78,79,81,82,
83,84,85,89,94,95,96,99,102,105,106,108,110,111,112,114,115,118,120,
121,122,123
5,6,9,13,19,23,25,43,51,52,54,55,58,59,62,63,64,78,79,83,85,89,91,95,96,
99,105,110,111,115,121,125,127
3,5,6,8,9,12,13,15,24,25,27,32,33,34,35,40,41,42,43,47,51,53,54,57,58,62,
63,64,67,70,71,73,74,75,78,79,81,83,84,85,89,91,94,95,96,99,102,105,110,
111,112,113,114,115,116,117,121,127
Only in one water
18,21,22,30,69,88,92,93,124,126
2,4,37,68,87,98,109
17,36,45,46,66,97, 100,
118,
119
1,14,29,108,120,123
23,125
12,27,117
Total
number of
fungi
85
(20)*
78
(24)
68
(22)
72
(20)
33(10)
58(17)
* Numbers in parenthesis designate the total number of parasites or necrotrophs.

Aquatic insects as vector of fungi parasitic on fishes 97
Fewest fungus species were found to grow on fragments of aquatic insects species in
the water of pond Akcent and Fosa. The water of these both ponds were found the lowest
oxygen content and indices of BOD5, and is characterised by a comparatively highest con-
tent of oxidability (COD), CO2, ammonium nitrogen, nitrates, phosphates, sulphates, chlo-
rides, and iron.
Interesting is also the occurrence of numerous fungus species known to cause death
of noble crayfish and many fish species. Aphanomyces astaci, first described by Schikora
(1903), causes the so called crayfish plague. In our study this fungus colonised chitin cov-
ers of Haliplus ruficollis individuals in the water of spring Cypisek and the river Supraśl.
Our earlier studies revealed that Aphanomyces astaci can grow on dragon-fly wings (Czec-
zuga and Godlewska 1994, 1998) on certain plankton crustaceans of the Cladocera (Czec-
zuga et al. 2000) and benthic crustaceans (Czeczuga et al. 1999 b). Moreover, Aphanomy-
ces astaci grows on fragments of dead crayfish specimens (Czeczuga et al. 1998). The
crayfish cuticle, when shed, becomes a carrier of Aphanomyces astaci for healthy crayfish.
A relatively large number of fungus species being fish parasites were found to grow
on the aquatic insect species examined. The most aquatic fungus species, known as fish
parasites were found to grow on the insects in the water of spring Jaroszówka (24), the
fewest in the water of pond Akcent (10) (Table 4). Most aquatic fungus species, fish para-
sites, were found to grow on Nepa cinerea specimens (16), fewest on the larvae of Anex
imperator, Chaoborus cristallinus, Pericoma decipiens, and on adult specimens of Hydro-
porus palustris (4 species on each—Table 2).
The fragments of aquatic insects examined were inhabited by a number of fungus
species which frequently cause significant losses in fish farming, including Achlya ameri-
cana, Achlya dubia, Achlya flagellata, Achlya polyandra, Achlya proliferoides, Aphano-
myces laevis, Dictyuchus sterilis, Leptolegnia caudata, Pythium proliferum, Saprolegnia
ferax, Saprolegnia monoica, and Saprolegnia parasitica. The most common fungus species
of this group found on the insects examined were Saprolegnia ferax (30 out of 32), Sapro-
legnia parasitica (24), Achlya americana (24) and Aphanomyces laevis (23) (Table 3).
Several years ago on a fish farm in England more than half of the Salmo trutta L. popula-
tion died of saprolegniosis (Ferguson and Ride 1980). Three species of Saprolegnia known
as fish parasites (Neish and Hughes 1980) were found on the fragments of aquatic insects,

98 Bazyli Czeczuga, Anna Godlewska
Saprolegnia monoica occurs on eggs of salmonids (Florinskaya 1971; Osipian et al. 1988),
coregonids (Czeczuga and Muszyńska 1998), and other fishes (Czeczuga and Muszyńska
1999a,b). However, the major losses in fish farms are due to the other two species: Sapro-
legnia ferax and Saprolegnia parasitica (cf. Chien 1981; Frick and Reinhold 1987; Dudka
et al. 1989). Saprolegnia ferax, together with other fungi, causes death in acipenserid fish
hatcheries, where losses in incubated eggs can reach 70% (Lartseva and Dudka 1990).
Many cases of saprolegniosis caused by Saprolegnia ferax are known (Neish and Hughes
1980; Dudka et al. 1989). Destructive actions of Saprolegnia parasitica were reported from
fish farms in Miyagi Prefecture, Japan, where in 1987 alone about 30-50% of coho salmon,
Oncorchynchus kisutch (Walbaum) died (Hatai and Hoshiai 1992). Apart from Saprolegnia
ferax, Saprolegnia parasitica is the commonest fungus found in saprolegniosis-induced
fish death and growing on the spawn of certain amphibians (Czeczuga et al. 1998).
Achlya americana and Achlya dubia attack both eggs and adult individuals of many
economically valuable fish species on different continents (Scott and Warren 1964; Bhar-
gava et al. 1971). Achlya flagellata infects eggs of many fish species (Florinskaya 1971;
Sati and Khulbe 1981), and Achlya polyandra infects eggs of salmonid fishes (Lartseva
1986). However, the major losses in fish farms of India are due to the other two species
such as Achlya proliferoides and Dictyuchus sterilis (cf. Srivastava 1976). Aphanomyces
laevis attacks both eggs and adult individuals of many economically valuable fish species
(Dudka et al. 1989). Likewise, Leptolegnia caudata occurs on acipenserid eggs (Dudka et
al. 1989). Pythium proliferum is encountered on both eggs and adults of various fish spe-
cies (Florinskaya 1969; Czeczuga 1996). Fungi of the genus Pythium are frequently found
on fishes; however, because of the difficulty of determining species of Pythium, only the
generic name is used (Scott and O'Bier 1962; Stuart and Fuller 1968; Shah et al. 1977).
Our detailed studies demonstrated that several species of Pythium inhabited the eggs of
various species of freshwater fishes (Czeczuga 1996).
The present study indicates that aquatic insects are a substrate for a number of zoo-
sporic fungi habitats are foci for fungi parasitising fish.
One of the new species is Blastulidium phaedopthorum, found in our study on larvae
of Chaoborus cristallinus in lake Komosa. It was described by Perez (1903) as a parasi-
tises of embryos of plankton crustaceans of the genus Daphnia. Later it turned out that this
fungus parasites also on other crustaceans of the Cladocera (Jirovec 1955). The water of

Aquatic insects as vector of fungi parasitic on fishes 99
lake Komosa is characterised by a comparatively highest content of oxygen but by the low-
est content of CO2, ammonium and nitrite nitrogen, phosphates, and chlorides. Myiophagus
ukrainica, another fungus new to Polish hydromycology, colonized the fragments of Chi-
ronomus atracinus larvae in spring Jaroszówka. Water of this spring had the lowest alka-
linity, nitrate nitrogen, and sulphates but by the highest content of nitrite nitrogen and cal-
cium. It was first described by Wize (1904) as an insecticidal fungus parasiting on Cleonus
punctiventris, a beet pest. It was later encountered in Great Britain (Fetch 1940), in Ber-
muda (Karling 1948), in Canada and the United States as a parasite of other land plant pest
insects (Fisher 1950).
Rhizidium nowakowskii, also a new fungus, was found to grow on three insect spe-
cies in the water of spring Jaroszówka, pond Fosa and lake Komosa. It was described by
Nowakowski (1876) and then encountered by Karling (1944) in Brazil. The water of pond
Fosa is characterised by a comparatively lowest content of calcium and magnesium but by
the highest content of nitrates nitrogen and chlorides. Water of this pond had the lowest
BODs and the highest oxidability (COD). Rhizophydium macrosporum was observed on
Gerris lucustris individuals in spring Cypisek. It was first described by Karling (1938) on
cooked beef. The water of spring Cypisek had the lowest oxidability and iron but by the
highest content of magnesium.
The two species of the genus Coelomomyces, have also appeared new to Polish wa-
ters. Coelomomyces lativittatus grew on the individuals of a few insect species in the water
of all six reservoirs, while Coelomomyces pentagulatus colonized only fragments of Palin-
genia longicuada larvae in spring Jaroszówka, river Supraśl and lake Komosa. The water
of river Supraśl had the highest BOD5. They were both described as parasites of mosquito
larvae—the former growing on larvae of the genus Anopheles (Couch 1945), the latter
parasitising on the genus Culex (cf. Couch and Dodge 1947).
Myzocytium megastomum was found on the fragments of four aquatic insect species
in pond Fosa and lake Komosa. It was described by de Wildeman (1890) as a parasite of
algae, both green and desmidia, and is known in the literature of the subject as an alga
parasite (Batko 1975). This would be the first report on the occurrence of Myzocytium
megastomum on animal substratum.

100 Bazyli Czeczuga, Anna Godlewska
Achlya cambrica, never before encountered in Polish waters, was found on four in-
sect species in the water of spring Jaroszówka and river the Supraśl. In the literature of the
subject (Johnson 1956, Batko 1975) it is described as an aquatic saprophyte.
A number of fungus species belonging to the Peronosporales have appeared new to
Polish hydromycology. Phytophthora fischeriana was found on larvae of Phryganea gran-
dis in spring Cypisek. Pythium deliense, first isolated from tobacco in Sumatra (Meurs
1934), colonized fragments of adult individuals of Dytiscus marginalis also in spring
Cypisek. Pythium salpingophorum colonized fragments of Palingenia longicauda larvae in
the river Supraśl. It was first described from decaying roots of pea Pisum sativum L. near
Eden in the State of New York (Drechsler 1930). Pythium tradicrescens was found in lake
Komosa on fragments of adult Cantharis fusca. It was first isolated by Vanterpool (1938)
as a parasite of wheat roots Triticum aestive L. in Canada. Rheosporangium aphaniderma-
tus, was found on fragments of Eristalis tenox larvae in pond Akcent. It was first described
by Edson (1915) as a parasite on sugar beets and radishes. The water of pond Akcent is
characterised by a comparatively lowest content of oxygen but by the highest content of
COi, ammonium nitrogen, phosphates, sulphates and iron. Water of this pond had the
highes alkalinity. Moreover, worth noting is the occurrence of such three rare Pythium spe-
cies as Pythium arrhenomanes var. philippinense, Pythium equiseti, and Pythium volutum.
Pythium equiseti was previously found on the pollens of certain plants (Czeczuga and
Muszyńska 2000), the other two species on dragon-flies (Czeczuga et al. 1999a).
CONCLUSIONS
The myco flora developing on dead specimens of 32 aquatic insect species was inves-
tigated under laboratory conditions. A total of 127 zoosporic fungus species were found to
grow on the fragments of aquatic insect species investigated, including 24 chytridiomyce-
tes, 2 hyphochytriomycetes, 99 oomycetes, and 2 zygomycetes fungus.
The most aquatic fungus species were found on aquatic insects in springs water
(Cypisek 89, Jaroszówka 80 species), the fewest in ponds water (Akcent 32, Fosa 61 spe-
cies).
Out of these 127 species, 28 are known as parasites or necrotrophs of fishes. The
most aquatic fungus species, fish parasites were found to grow on the insects in the water
of spring Jaroszówka (24), the fewest in the water of pond Akcent (10). The most common

Aquatic insects as vector of fungi parasitic on fishes 101
fungus species of this group found on the insects examined were Saprolegnia ferax (30 out
of 32), Saprolegnia parasitica (24), Achlya americana (24), and Aphanomyces laevis (23).
Fourteen fungus species were recorded for the first time from Poland.
ACKNOWLEDGEMENTS
The authors are grateful to dr Stanisław Czachorowski from Warmia and Mazury
University in Olsztyn, for kind help in this work. We are also grateful to the anonymous
referee for penetrating remarks and offering valuable suggestions.
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104 Bazyli Czeczuga, Anna Godlewska
Bazyli CZECZUGA, Anna GODLEWSKA
OWADY WODNE JAKO WEKTORY ZOOSPOROWYCH GRZYBÓW
PASOŻYTNICZYCH RYB
STRESZCZENIE
Autorzy badali w warunkach laboratoryjnych rozwój zoosporowych grzybów wodnych na
fragmentach osobników 32 gatunków form larwalnych lub doskonałych owadów wodnych w wo-
dzie sześciu różnych zbiorników wodnych o różnej troficzności. Do doświadczeń wodę pobierano
ze źródeł Cypisek i Jaroszówka, z rzeki Supraśl, ze stawów Akcent i Fosa oraz z jeziora Komosa
oznaczając w niej niektóre parametry fizykochemiczne. Najbardziej zasobną w biogeny i inne
wskaźniki troficzności była woda obu stawów.
Na fragmentach badanych gatunków owadów wodnych rozwijało się 127 gatunków zoospo-
rowych grzybów wodnych, z których 24 gatunki należały do Chytridiomycetes, 2 do Hypochy-
triomycetes, 99 do Oomycetes oraz 2 gatunki do Zygomycetes. W najmniejszym stopniu koloni-
zowane były fragmenty larw Anex imperator (Odonata) oraz dorosłe osobniki Hydrophorus palu-
stris (Coleoptera) (po 13 gatunków grzybów w obu przypadkach), zaś w największym stopniu
fragmenty dorosłych osobników Nepa cinerea (Hemiptera) (38). Najwięcej gatunków grzybów
wodnych kolonizowało fragmenty badanych owadów wodnych w wodzie obu źródeł, najmniej zaś
- w wodzie obu stawów.
Wśród stwierdzonych gatunków grzybów zoosporowych rozwijających się na badanych ga-
tunkach owadów wodnych znalazł się Aphanomyces astaci powodujący wśród raków szlachetnych
tak zwaną dżumę raczą oraz 28 gatunków rozwijających się na ikrze i dorosłych osobnikach ryb,
powodujących nieraz ogromne straty w rybostanie. Najwięcej gatunków grzybów wodnych paso-
żytów ryb rozwijało się na osobnikach Nepa cinerea (16), najmniej zaś na larwach Anex impera-
tor, Chaoborus cristallinus, Pericoma decipiens oraz na osobnikach dorosłych Hydroporus palu-
stris (po 4 gatunki). Najczęściej spotykanymi gatunkami grzybów z tej grupy na badanych owa-
dach były Saprolegnia ferax (na 30 z 32 badanych), Saprolegnia parasitica (24), Achlya america-
na (24) oraz Aphanomyces laevis (23). Ponadto 14 gatunków grzybów rozwijających się na frag-
mentach owadów wodnych okazały się nowymi dla hydromykologii Polski.
Received: 21 March 2001
Author's address:
Bazyli Czeczuga, DSc Prof
Department of General Biology
Medical University in Białystok
Kilińskiego 1, 15-230 Białystok, Poland