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Fungi on the food and in the faeces of Gammarus pulex
N otes and brief articles
160
washed repeatedly with dist illed water, and dried at 105 0 for 12 h. The results showed th at there was no loss in weight of cellulo se powder under these conditions and the culture filtrate had no cellulase activity (Table 1). The degradation of wheat straw (loss in weight, degradation of cellulose in wheat straw, C: N ratio of degraded and undegraded material and cellulase activity) was determined by the methods described by Jain et al. (1979). The fungus grew well in wheat straw solid medium (T able 1). The loss in weight of wheat straw and cellulose in wheat straw was 23'0 and 24 '7 % respectively after 60 days and the C :N ratio of the material decreased from 116'3 to 83'3 in the same period. These results indicated that H. lanuginosa has a requirement for some specific substance which is present in wheat straw in order to degrade cellulose as it degraded the cellulose of wheat straw but not pure cellulose powder. To investigate this further, 30 em" of nutrient solution and 5 g Whatman No 1 filter paper strips (5 mrns ) were placed in 100 ern" flasks with and without glucose and in other flasks with wheat straw extract with and without glucose . The flasks were inoculated with 1 em>spore suspension of the fungus and incubated at 50° under stationary conditions. The loss in weight of filter paper was determined after 10 and 20 days incubation (Table 2). As observed earlier the fungus did not grow with filter paper as the sole source of carbon. When glucose was added with the filter paper, the fungus was able to grow but did not degrade the filter paper. Addition of wheat straw extract with or without glucose resulted in the degradation of filter paper and its loss in weight. This indicated th at some water soluble factor is supplied through wheat straw extract which induces cellulolytic activity in H. lanuginosa.
It is concluded that this strain of H. lanuginosa degrades cellulose and it is possible that H. lanuginosa reported earlier as non-cellulolytic may be cellulolytic in natural habitats. The authors thank the Indian Council of Agricultural Research, New Delhi for financing the work and Dr P. Tauro, Professor of Microbiology, for helpful suggestions. REFERENCES
CHANG, Y. (1967). The fungi of wheat straw compost. II. Biochemical and physiological studies. Transactions of the British Mycological Society 50, 667-677.
CHANG, Y. & HUDSON, H. J. (1967). The fungi of wheat straw compost. I. Ecological studies. Tran sactions of the British Mycological Society 50, 649-666.
COONEY, D. E. & EMERSON, R. (1964). Thermophilic Fungi. San Francisco: W. H. Freeman and Co. FERGUS, C. L. (1964). The thermophilic and thermotolerant molds and actinomycetes of mushroom compost during peak heating. Mycologia 56, 267-284. HEDGER, J. N. & HUDSON, H. J. (1974). Nutritional studies of Thermomy ces lanuginosa from wheat straw compost. Transaction s of the British M ycological Society 62, 129-143.
JAIN, M. K., KApOOR, K. K. & MISHRA, M. M. (1979). Cellulase activity, degradation of celluloseand lignin and humus formation by thermoph ilic fungi. Tran sactions of the Br itish My cological Society 73, 85-89· MANDELS, M., ANDREOTTI, R. & ROCHE, C. (1976). Measurement of saccharifying cellulase. Biotechnology B ioengineering Symposium 6, 21-23. MANDELS, M. & STERNBERG, D. (1976). Recent advances in cellulase technology. Journal of Fermentation Technology 54, 267-286. ROSENBERG, S. L. (1978). Cellulose and lignocellulose
degradation by thermophilic and thermotolerant fungi. My cologia 70,1-13 .
FUNGI ON THE FOOD AND IN THE FAECES OF GAMMARUS PULEX BY FELIX BARLOCHER
Botanical Institute, University of Basel, Schonbeinstr. 6, CH-40S6 Basel, Switzerland Recent studies on interactions between microorganisms and invertebrates during leaf-processing in streams have been conducted with the object of determining how fungal and bacterial colonization of leaves affects the feeding of an imals on the substrate. This work is reviewed by Anderson & Sedell (1979), Barlocher & Kendrick (1980) and Tran s. Br. mycol. S oc. 76 (1), (1981) .
Cummins & Klug (1979). The complementary question of how animal feeding affects fungi and bacteria has so far been neglected. It seems reasonable to assume that negative aspects predominate (Barlocher, 1979), and one would therefore expect that special adaptations exist whereby microorganisms lower the damage done
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Notes and brief articles
..
300 .3
E
E 200 5l
eo
E
....
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100
'2 0
u
~/·/~\
0_0
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Fig, Table
1.
1.
161
N
0
S
~:
F
D
Conidium production from leaves and twigs recovered from the stream. • , twigs; 0, leaves.
Species composition of conidia recovered from leaves and twigs
Leaves Twigs Alatospora acuminata Ingold Anguillospora /ongissima (de Wild.)
75'0 3 '1
4'0 5'3
2'5 2'3 1·6 H eliscus lugdunensis Sacco& Therry 1·6 L emonniera "aquatica de Wild, Tetracladium marchalianum de Wild. 11'2 T etracladium setigerum (Grove) 1'1
27'1 62'0 0'7 0'7
Ingold Claoariopsis aquatica de Wild.
Plagellospora curuula Ingold
Ingold Tricladium angulatum Ingold
1·6 100'0
0'2
%
100'0
%
by foraging animals. This could be achieved, for example, by producing stru ctures which survive the passage through the digestive tract. To study this possibility, faecal pellets of Gammarus pulex L., freshly collected from a stream, were examined for the presence of viable conidia and conidiumforming structures of aquatic hyphomycetes. These results were compared with the conidium production on potential food of G. pulex, namely leaves and twigs lying in the stream. All materials were collected in the Talmuhlequelle, a spring-fed stream, within an area of approximately 5 m 2 (for chemical characteristics of the water, see Barlocher, OertIi & Guggenheim, 1979). Conidia in the water were counted and identified by the membrane filter method of Iqbal & Webster (1973). Each month, five samples of 0'5 I were taken. To determine conidium production on potential Trans. Br, mycol. Soc. 76 (1), (1981) .
food of G. pulex, each month, 50 to 100 mg of randomly collected twig (diam < 1 em) and leaf material were placed separately in each of ten 250 ern" flasks filled with 200 em" distilled water. The water was aerated for 2 days at 12 °C. Released conidia were counted and identified by the method described by Iqbal & Webster (1973). The leaf and twig material was dried for 3 days at 0 100 and weighed to calculate the number of conidia produced in 2 days, mg-1 dry weight of the substrate. Specimens of G. pulex were captured and returned in stream water to the laboratory. On each sampling occasion, ten animals were examined and the entire digestive tract dissected out and squashed in water. Under the microscope, the relative proportions of vascular plant remains, fine organic particles of unidentifiable origin, mineral particles, mosses and algae, and animal remains were estimated visually. Live G, pulex were rinsed several times in tap water and placed in dishes (20 x 15 x 4 em) filled with water (40 animals per dish). Newly produced faecal pellets were collected and 40 to 50 pellets were pooled to form one sample. The dry weight of this sample was estimated by comparing it to the dry weight of an equal number of pellets collected at the same time. To determine number and types of conidia present in fresh faeces, the pellets were gently teased apart with needles, suspended in 200 ems sterilized distilled water and vigorously shaken. The suspension was filtered and conidia counted by the method of Iqbal & Webster (1973). To determine viability of these spores, filters with attached spores were placed on water agar plates
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MY C
76
Notes and brief articles
162
T able
J
A
8
2 4 2 10 260
1 20 210
6
2
2 286
1 4 239
A latospora acuminata Anguillospora longissima Clavariopsis aquatica
Flagellospora curuula
15 400
Heliscus lugdunensis Lemonniera aquatica Tetracladium marchalianum T etracladium setigerum Tricladium angula tum Totals 423
IV
N umber and types of conidia I - I stream water
2.
1 0~.
40 r-
S
N
D
J
151 24 12 17 49 32 150
113 4 17 5 56
4 2 4 31
31
2
435
226
43
0
20 6 14 330 12 2 8 392
""-.-.-.-."""............._
........... _."""
.
F
M
A
M
J 2
1
3 2 12
17
28 1 1
4
5
17
17
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4
7
.-
r-; ./.".,,/. ""-./. <;> .
•
/'
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... 50
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I
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I
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I
I
I
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M A M J
Fig. 2 . Seasonal variation in the gut content of Gammarus pulex. Percentages of I : vascular plant remains ; II : mineral particles ; III : fine organic particles ; IV : algae and mosses; V: animal remains .
for 24 h .and stained. Using the same procedure conidia filtered from stream water gave 95 % germination for Alatospora acuminata and 100 % for Heliscus lugdunensis and all other species. To determine if faeces contained structures Trans. Br, mycol. Soc. 76 (1), (1981).
capable of producing conidia, pellets were suspended in 200 em" distilled water, and aerated for 2 days at 12°, then filtered and stained. With additional samples, the viability of these conidia was tested as described above.
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0007-1536/81 /2828-7090 $00.35 © 1981 The British Mycological Society
0 0 0
-..:I
... I
VI IN 0\
"<,
...
00
--N 00 N 00 r
~ I:l ;t ~
tl:l
:'
~<> C
r~
-..:I
f>
\0
....;a
0 0
~
0 0
w VI
\D)
...
Table 3. Conidia mg :? faecal material through the year
0\ ~
:;... ...':--' ~
\0 00
Heliscus Zugdunensis
\0
..,::r... 00
f>
b:l
~.
1;;'
::r ~
'< n
§-
OS. n
e:.
4' s :;: l:>...
Tricladium angulatum Tetracladium marchaZianum
;;;'
..'" .
Q ~
tl:l
Clauariopsis aquatica Alatospora acuminata
~.
;;;.
J
A
S
0
,--.A---,
,--.A---,
,.----A---.
r-..A..--.
-
-
+
0
1
4
7
8 18
43
0
1
g
Flagellospora curoula
2 0 4
1 1
2 2
1 1
5
1 1
3 5
0 1
0 2
0 2
7
9
9
11
+ -
2 2
2
3
D
1 2
r-..A..--.
2
5
7
3
6
10
2
5 10
9 10 13
3 8
J
F
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A
M
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,....-A---.,
,....-A---.,
,....-A---.,
,....-A---.,
r-"----.
,--.A---,
+ -
+ -
+ 1 1
10 12
4
2
12 13
4
12 15
4 14
15 22
+ -
+ -
+ 2 2
0 1
0
1
1
1
1
5 5
3 3
3
10 12
1 2
3 5
5 5
7
15 18
1
3 3
0 2
0
1
3 3
4 4
3 5 21
5
35
6
3 3
1
4
7
7 10 15
4
3
3
6 6
3
1 1
2 2
+
Increase
5 5
25 31
8 49
3
4
8
~
s ~ ~
t:l...
e:::t-
12 15
3 3
4 5
6 7
1 1
+ -
6
5 5
1 1
1 1
5 5
8 8
6
5 5
28
;:!.
~ ~
.... ~.
"-t
~ eo., 0
0 2
Anguillospora longissima
Increase
5 20
4
Lemonniera aquatica
'<
12 14
0 1
en
fio
18
+ -
+ 1 1
N ,--.A---,
0 1
15
1 2
1 2 10
4
12
18
20
1
1 1
0 2 30
24
2
5
4
4
- : Without aeration; + : with aeration. Upper number: germinated conidia; lower number: total number of conidia. Increase: total number of viable conidia produced during aeration.
"'"
...
~
Notes and brief articles In spring 1978, rain deposited many branches and twigs in the stream. This material gradually disappeared because of removal by forest workers, water transport, etc. Leaf-fall started in Sept. and by Oct., about 50 % of the leaves of riparian trees had been shed, rising to 95 % by Nov. In Dec., leaves in the water were strongly skeletonized, and had almost completely disappeared by Feb. Ash (Fraxinus excelsior L.), sycamore (Acer pseudoplatanus L.), oak (Quercus robur L.) and hazel (Corylus avellana L.) leaves were most abundant. The number of conidia produced mg :" substrate in 2 days are shown in Fig. 1, and the % frequency distribution of the species in Table 1. It is obvious that leaf material can be considerably more productive than the more recalcitrant twigs, and that different species dominate on the two types of substrate. Alatospora acuminata and T etracladium marchalianum are more numerous on leaves, and H. lugdunensis and Flagellospora curvula more numerous on twigs. These substrate preferences are also reflected, at least as a broad trend, in the conidia found in the stream water (Table 2). From July to Sept., and again after Feb., when virtually no leaves could be found in the stream, H. lugdunensis was by far the most common fungus, while A. acuminata and T. marchalianum occurred more frequently between Oct. and Dec. when the supply of leaves was highest. The seasonal variation of kinds and amounts of potential food presumably influences food selection by G. pulex. However, there is no simple correlation between supply and actual amount consumed. Leaves in the stream were most abundant in Oct. and Nov., but the proportion of recognizable vascular plant remains in the guts of G. pulex was highest in Nov. and Dec. (Fig. 2). This delay may be due to the animals' preference for microbially conditioned substrates. Table 3 summarizes the observations on faeces. It clearly shows that in every sample a certain number of conidia had survived passage through the digestive tract. However, germination percentages were generally greatly reduced when compared to those of conidia collected from the stream water. Not only conidia, but also conidium producing structures, can apparently survive when eaten by G. pulex (Table 3). Conidial production mg" faeces was considerably lower (maximum of 30) than the corresponding value for leaves (over 300), which form the basis of roughly 30 % of the animals' food (see Fig. 2). Most conidia produced on faeces belong to Trans. Br. mycol. Soc. 76 (1), (1981).
T. marchalianum, followed by Tricladium angulatum and Lemonniera aquatica. This may be due to feeding preferences of G. pulex for certain fungi,
to differential survival of the fungi, or to a combination of both factors. Fungi found in faeces do not show the same species distribution as those found on the substrates dominant at the sampling time. For example, between July and Sept. and after Feb., twigs, colonized primarily by H. lugdunensis were far more common than leaves, but H. lugdunensis conidia were not nearly as dominant in the faeces of G. pulex. Again, this may be due to the animals' refusal to eat H. lugdunensis, or to better survival of the other fungi in the digestive tract of G. pulex. Definitive answers will only be possible from strictly controlled laboratory experiments. But whatever the reason, it is likely that such differences will influence the composition of the fungal flora on leaves and other substrates. There is even the possibility that certain fungi may be spread to otherwise difficult to reach streams or stream areas (e.g. upstream) by being carried in the guts of G. pulex and other leaf-eating animals. Conidium production from faecal pellets peaked in Ian., when leaves were few, strongly skeletonized and yielded few conidia. A possible explanation for this apparent paradox is that the fungi may be better protected when growing attached to the relatively tough veins and petioles which will not disintegrate as readily as the softer leaf matrix when chewed. A similar relationship has been demonstrated by Lopez & Levinton (1978) in another system. Digestion efficiency of the snail Hydrobia ventrosa Montagu appears to be constrained by its ability to detach microbial cells from sediment particles. This raises some intriguing questions about fungal evolution as a response to animal behaviour. A fungus could evolve to grow on the leaf matrix which presumably contains more easily digested nutrients, but increases the risk of being eaten, or it could instead grow on the poorer substrate of veins and petioles, and be less exposed to predators. It is likely that different species will have adopted different strategies which will demand different sets of physiological adaptations. This study has shown that some fungi can survive passage through the digestive tract of one leaf-eating invertebrate. It remains to be seen how these results compare with those of other habitats and with different organisms, and how, if at all, this phenomenon influences the species composition of leaf-colonizing fungi in streams. This study was supported by Grant no. 3.208-
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Notes and brief articles 0.77. from the Swiss National Research Foundation. REFERENCES
ANDERSON, N. H. & SWELL, J. R. (1979). Detritus processing by macroinvertebrates in stream ecosystems. Annual Review of Entomology 24, 351-377. BilloCHER,F. (1979).On trophic interactions between microorganisms and animals. The American Naturalist 113, 147-148. BARLOCHER, F. & KENDRICK, B. (1980). The role of aquatic hyphomycetes in the trophic structure of streams. In The Fungal Community, its organisation and role in the ecosystem (ed. D. T. Wicklow & G. C. Carroll). New York: Marcel Dekker, Inc. (In the
BillOCHER, F., OERTLl,J. J. & GUGGENHEIM,R.(1979). Accelerated loss of antifungal inhibitors from Pinus leucodermis needles. Transactions of the British Mycological Society 72, 277-281. CUMMINS, K. W. & KLUG, M. J. (1979). Feeding ecology of stream invertebrates. Annual Review of Ecologyand Systematics 10, 147-172. IQBAL, S. H. & WEBSTER, J. (1973). Aquatic hyphomycete spora of the River Exe and its tributaries. Transactions of the British Mycological Society 61, 331-346. LOPEZ, G. R. & LEVINTON, J. S. (1978).The availability of microorganisms attached to sediment particles as food for Hydrobia ventrosa Montagu (Gastropoda: Prosobranchia). Oecologia 32, 263-275.
Press.)
THE BALLISTOSPORE OF BULLERA ALBA BY C. T. INGOLD 11
Buckner's Close, Benson, Oxford OX9 6LR AND T. W. K. YOUNG
Department of Applied Biology, Chelsea College, Hortensia Road, London SW10 oQX In Vol. 2 of' The Whole Fungus' (Kendrick, 1979), Luttrell, during a discussion on yeasts, suggested that the Sporobolomycetaceae is a heterogeneous taxon and in particular that Sporobolomyces and Bullera differ fundamentally. His remarks were supported by detailed illustrations of the two genera. His contention was that, whereas the aerial spore of Sporobolomyces is borne asymmetrically on its sterigma (i.e. heterotropic, see Pegler & Young, 1979), that of Bullera is placed symmetrically (orthotropic) with a cross-wall visible where spore and sterigma meet. If this were true, presumably different mechanisms of spore discharge would be involved and there would be no distinctive feature linking Bullera with the Basidiomycetes. In an attempt to confirm Luttrell's suggestion, a culture of Bullera alba (Hanna) Derx (IMI 86680) was obtained from the Commonwealth Mycological Institute. Subcultures were examined by one of us (C.T.!.) microscopically and in addition the other (T.W.K.Y.) prepared SEM pictures (Figs 1-6). Both of us observed that the violently-discharged aerial spore was of the ballistospore type found in Hymenomycetes.
Trans. Br. mycol. Soc. 76 (1), (1981).
Indeed, spore liberation in Bullera involving drop development at the hilar appendix just before discharge was reported long ago (Ingold, 1939). It seems to be exactly comparable with what occurs in Sporobolomyces (Buller, 1933; Miiller, 1954)· Luttrell figured a cross-wall where spore and sterigma meet, but it would be difficult to demonstrate this by light microscopy as the junction is only 0'4 pm wide. REFERENCES
BULLER, A. H. R. (1933). Researches on Fungi. 5, London: Longmans, Green & Co. INGOLD, C. T. (1939). Spore Dischargein Land Plants. Oxford: Clarendon Press. KENDRICK, B. ed. (1979). The Whole Fungus. 2, Ottawa: National Museum of Natural Sciences, National Museum of Canada, and the Kananaskis Foundation. MULLER, D. (1954). Die Abschleuderung der Sporen von Sporobolomyces (Spiegelhefe) gefilmt. Friesia 5, 65-'74· PEGLER, D. N. & YOUNG, T. W. K. (1979). The Gasteroid Russulales, Transactions of the British Mycological Society 72, 353-388.
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160
washed repeatedly with dist illed water, and dried at 105 0 for 12 h. The results showed th at there was no loss in weight of cellulo se powder under these conditions and the culture filtrate had no cellulase activity (Table 1). The degradation of wheat straw (loss in weight, degradation of cellulose in wheat straw, C: N ratio of degraded and undegraded material and cellulase activity) was determined by the methods described by Jain et al. (1979). The fungus grew well in wheat straw solid medium (T able 1). The loss in weight of wheat straw and cellulose in wheat straw was 23'0 and 24 '7 % respectively after 60 days and the C :N ratio of the material decreased from 116'3 to 83'3 in the same period. These results indicated that H. lanuginosa has a requirement for some specific substance which is present in wheat straw in order to degrade cellulose as it degraded the cellulose of wheat straw but not pure cellulose powder. To investigate this further, 30 em" of nutrient solution and 5 g Whatman No 1 filter paper strips (5 mrns ) were placed in 100 ern" flasks with and without glucose and in other flasks with wheat straw extract with and without glucose . The flasks were inoculated with 1 em>spore suspension of the fungus and incubated at 50° under stationary conditions. The loss in weight of filter paper was determined after 10 and 20 days incubation (Table 2). As observed earlier the fungus did not grow with filter paper as the sole source of carbon. When glucose was added with the filter paper, the fungus was able to grow but did not degrade the filter paper. Addition of wheat straw extract with or without glucose resulted in the degradation of filter paper and its loss in weight. This indicated th at some water soluble factor is supplied through wheat straw extract which induces cellulolytic activity in H. lanuginosa.
It is concluded that this strain of H. lanuginosa degrades cellulose and it is possible that H. lanuginosa reported earlier as non-cellulolytic may be cellulolytic in natural habitats. The authors thank the Indian Council of Agricultural Research, New Delhi for financing the work and Dr P. Tauro, Professor of Microbiology, for helpful suggestions. REFERENCES
CHANG, Y. (1967). The fungi of wheat straw compost. II. Biochemical and physiological studies. Transactions of the British Mycological Society 50, 667-677.
CHANG, Y. & HUDSON, H. J. (1967). The fungi of wheat straw compost. I. Ecological studies. Tran sactions of the British Mycological Society 50, 649-666.
COONEY, D. E. & EMERSON, R. (1964). Thermophilic Fungi. San Francisco: W. H. Freeman and Co. FERGUS, C. L. (1964). The thermophilic and thermotolerant molds and actinomycetes of mushroom compost during peak heating. Mycologia 56, 267-284. HEDGER, J. N. & HUDSON, H. J. (1974). Nutritional studies of Thermomy ces lanuginosa from wheat straw compost. Transaction s of the British M ycological Society 62, 129-143.
JAIN, M. K., KApOOR, K. K. & MISHRA, M. M. (1979). Cellulase activity, degradation of celluloseand lignin and humus formation by thermoph ilic fungi. Tran sactions of the Br itish My cological Society 73, 85-89· MANDELS, M., ANDREOTTI, R. & ROCHE, C. (1976). Measurement of saccharifying cellulase. Biotechnology B ioengineering Symposium 6, 21-23. MANDELS, M. & STERNBERG, D. (1976). Recent advances in cellulase technology. Journal of Fermentation Technology 54, 267-286. ROSENBERG, S. L. (1978). Cellulose and lignocellulose
degradation by thermophilic and thermotolerant fungi. My cologia 70,1-13 .
FUNGI ON THE FOOD AND IN THE FAECES OF GAMMARUS PULEX BY FELIX BARLOCHER
Botanical Institute, University of Basel, Schonbeinstr. 6, CH-40S6 Basel, Switzerland Recent studies on interactions between microorganisms and invertebrates during leaf-processing in streams have been conducted with the object of determining how fungal and bacterial colonization of leaves affects the feeding of an imals on the substrate. This work is reviewed by Anderson & Sedell (1979), Barlocher & Kendrick (1980) and Tran s. Br. mycol. S oc. 76 (1), (1981) .
Cummins & Klug (1979). The complementary question of how animal feeding affects fungi and bacteria has so far been neglected. It seems reasonable to assume that negative aspects predominate (Barlocher, 1979), and one would therefore expect that special adaptations exist whereby microorganisms lower the damage done
Printed in Great Britain
0007-1536/81/2828-7°90 $00.35 © 1981 The British Mycological Society
Notes and brief articles
..
300 .3
E
E 200 5l
eo
E
....
"c. '" :.0
100
'2 0
u
~/·/~\
0_0
A
Fig, Table
1.
1.
161
N
0
S
~:
F
D
Conidium production from leaves and twigs recovered from the stream. • , twigs; 0, leaves.
Species composition of conidia recovered from leaves and twigs
Leaves Twigs Alatospora acuminata Ingold Anguillospora /ongissima (de Wild.)
75'0 3 '1
4'0 5'3
2'5 2'3 1·6 H eliscus lugdunensis Sacco& Therry 1·6 L emonniera "aquatica de Wild, Tetracladium marchalianum de Wild. 11'2 T etracladium setigerum (Grove) 1'1
27'1 62'0 0'7 0'7
Ingold Claoariopsis aquatica de Wild.
Plagellospora curuula Ingold
Ingold Tricladium angulatum Ingold
1·6 100'0
0'2
%
100'0
%
by foraging animals. This could be achieved, for example, by producing stru ctures which survive the passage through the digestive tract. To study this possibility, faecal pellets of Gammarus pulex L., freshly collected from a stream, were examined for the presence of viable conidia and conidiumforming structures of aquatic hyphomycetes. These results were compared with the conidium production on potential food of G. pulex, namely leaves and twigs lying in the stream. All materials were collected in the Talmuhlequelle, a spring-fed stream, within an area of approximately 5 m 2 (for chemical characteristics of the water, see Barlocher, OertIi & Guggenheim, 1979). Conidia in the water were counted and identified by the membrane filter method of Iqbal & Webster (1973). Each month, five samples of 0'5 I were taken. To determine conidium production on potential Trans. Br, mycol. Soc. 76 (1), (1981) .
food of G. pulex, each month, 50 to 100 mg of randomly collected twig (diam < 1 em) and leaf material were placed separately in each of ten 250 ern" flasks filled with 200 em" distilled water. The water was aerated for 2 days at 12 °C. Released conidia were counted and identified by the method described by Iqbal & Webster (1973). The leaf and twig material was dried for 3 days at 0 100 and weighed to calculate the number of conidia produced in 2 days, mg-1 dry weight of the substrate. Specimens of G. pulex were captured and returned in stream water to the laboratory. On each sampling occasion, ten animals were examined and the entire digestive tract dissected out and squashed in water. Under the microscope, the relative proportions of vascular plant remains, fine organic particles of unidentifiable origin, mineral particles, mosses and algae, and animal remains were estimated visually. Live G, pulex were rinsed several times in tap water and placed in dishes (20 x 15 x 4 em) filled with water (40 animals per dish). Newly produced faecal pellets were collected and 40 to 50 pellets were pooled to form one sample. The dry weight of this sample was estimated by comparing it to the dry weight of an equal number of pellets collected at the same time. To determine number and types of conidia present in fresh faeces, the pellets were gently teased apart with needles, suspended in 200 ems sterilized distilled water and vigorously shaken. The suspension was filtered and conidia counted by the method of Iqbal & Webster (1973). To determine viability of these spores, filters with attached spores were placed on water agar plates
Printed in Great Britain
0007-1536/81 /2828-7090 $00 .35 © 1981 The British Mycological Society 6
MY C
76
Notes and brief articles
162
T able
J
A
8
2 4 2 10 260
1 20 210
6
2
2 286
1 4 239
A latospora acuminata Anguillospora longissima Clavariopsis aquatica
Flagellospora curuula
15 400
Heliscus lugdunensis Lemonniera aquatica Tetracladium marchalianum T etracladium setigerum Tricladium angula tum Totals 423
IV
N umber and types of conidia I - I stream water
2.
1 0~.
40 r-
S
N
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for 24 h .and stained. Using the same procedure conidia filtered from stream water gave 95 % germination for Alatospora acuminata and 100 % for Heliscus lugdunensis and all other species. To determine if faeces contained structures Trans. Br, mycol. Soc. 76 (1), (1981).
capable of producing conidia, pellets were suspended in 200 em" distilled water, and aerated for 2 days at 12°, then filtered and stained. With additional samples, the viability of these conidia was tested as described above.
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0007-1536/81 /2828-7090 $00.35 © 1981 The British Mycological Society
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Notes and brief articles In spring 1978, rain deposited many branches and twigs in the stream. This material gradually disappeared because of removal by forest workers, water transport, etc. Leaf-fall started in Sept. and by Oct., about 50 % of the leaves of riparian trees had been shed, rising to 95 % by Nov. In Dec., leaves in the water were strongly skeletonized, and had almost completely disappeared by Feb. Ash (Fraxinus excelsior L.), sycamore (Acer pseudoplatanus L.), oak (Quercus robur L.) and hazel (Corylus avellana L.) leaves were most abundant. The number of conidia produced mg :" substrate in 2 days are shown in Fig. 1, and the % frequency distribution of the species in Table 1. It is obvious that leaf material can be considerably more productive than the more recalcitrant twigs, and that different species dominate on the two types of substrate. Alatospora acuminata and T etracladium marchalianum are more numerous on leaves, and H. lugdunensis and Flagellospora curvula more numerous on twigs. These substrate preferences are also reflected, at least as a broad trend, in the conidia found in the stream water (Table 2). From July to Sept., and again after Feb., when virtually no leaves could be found in the stream, H. lugdunensis was by far the most common fungus, while A. acuminata and T. marchalianum occurred more frequently between Oct. and Dec. when the supply of leaves was highest. The seasonal variation of kinds and amounts of potential food presumably influences food selection by G. pulex. However, there is no simple correlation between supply and actual amount consumed. Leaves in the stream were most abundant in Oct. and Nov., but the proportion of recognizable vascular plant remains in the guts of G. pulex was highest in Nov. and Dec. (Fig. 2). This delay may be due to the animals' preference for microbially conditioned substrates. Table 3 summarizes the observations on faeces. It clearly shows that in every sample a certain number of conidia had survived passage through the digestive tract. However, germination percentages were generally greatly reduced when compared to those of conidia collected from the stream water. Not only conidia, but also conidium producing structures, can apparently survive when eaten by G. pulex (Table 3). Conidial production mg" faeces was considerably lower (maximum of 30) than the corresponding value for leaves (over 300), which form the basis of roughly 30 % of the animals' food (see Fig. 2). Most conidia produced on faeces belong to Trans. Br. mycol. Soc. 76 (1), (1981).
T. marchalianum, followed by Tricladium angulatum and Lemonniera aquatica. This may be due to feeding preferences of G. pulex for certain fungi,
to differential survival of the fungi, or to a combination of both factors. Fungi found in faeces do not show the same species distribution as those found on the substrates dominant at the sampling time. For example, between July and Sept. and after Feb., twigs, colonized primarily by H. lugdunensis were far more common than leaves, but H. lugdunensis conidia were not nearly as dominant in the faeces of G. pulex. Again, this may be due to the animals' refusal to eat H. lugdunensis, or to better survival of the other fungi in the digestive tract of G. pulex. Definitive answers will only be possible from strictly controlled laboratory experiments. But whatever the reason, it is likely that such differences will influence the composition of the fungal flora on leaves and other substrates. There is even the possibility that certain fungi may be spread to otherwise difficult to reach streams or stream areas (e.g. upstream) by being carried in the guts of G. pulex and other leaf-eating animals. Conidium production from faecal pellets peaked in Ian., when leaves were few, strongly skeletonized and yielded few conidia. A possible explanation for this apparent paradox is that the fungi may be better protected when growing attached to the relatively tough veins and petioles which will not disintegrate as readily as the softer leaf matrix when chewed. A similar relationship has been demonstrated by Lopez & Levinton (1978) in another system. Digestion efficiency of the snail Hydrobia ventrosa Montagu appears to be constrained by its ability to detach microbial cells from sediment particles. This raises some intriguing questions about fungal evolution as a response to animal behaviour. A fungus could evolve to grow on the leaf matrix which presumably contains more easily digested nutrients, but increases the risk of being eaten, or it could instead grow on the poorer substrate of veins and petioles, and be less exposed to predators. It is likely that different species will have adopted different strategies which will demand different sets of physiological adaptations. This study has shown that some fungi can survive passage through the digestive tract of one leaf-eating invertebrate. It remains to be seen how these results compare with those of other habitats and with different organisms, and how, if at all, this phenomenon influences the species composition of leaf-colonizing fungi in streams. This study was supported by Grant no. 3.208-
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Notes and brief articles 0.77. from the Swiss National Research Foundation. REFERENCES
ANDERSON, N. H. & SWELL, J. R. (1979). Detritus processing by macroinvertebrates in stream ecosystems. Annual Review of Entomology 24, 351-377. BilloCHER,F. (1979).On trophic interactions between microorganisms and animals. The American Naturalist 113, 147-148. BARLOCHER, F. & KENDRICK, B. (1980). The role of aquatic hyphomycetes in the trophic structure of streams. In The Fungal Community, its organisation and role in the ecosystem (ed. D. T. Wicklow & G. C. Carroll). New York: Marcel Dekker, Inc. (In the
BillOCHER, F., OERTLl,J. J. & GUGGENHEIM,R.(1979). Accelerated loss of antifungal inhibitors from Pinus leucodermis needles. Transactions of the British Mycological Society 72, 277-281. CUMMINS, K. W. & KLUG, M. J. (1979). Feeding ecology of stream invertebrates. Annual Review of Ecologyand Systematics 10, 147-172. IQBAL, S. H. & WEBSTER, J. (1973). Aquatic hyphomycete spora of the River Exe and its tributaries. Transactions of the British Mycological Society 61, 331-346. LOPEZ, G. R. & LEVINTON, J. S. (1978).The availability of microorganisms attached to sediment particles as food for Hydrobia ventrosa Montagu (Gastropoda: Prosobranchia). Oecologia 32, 263-275.
Press.)
THE BALLISTOSPORE OF BULLERA ALBA BY C. T. INGOLD 11
Buckner's Close, Benson, Oxford OX9 6LR AND T. W. K. YOUNG
Department of Applied Biology, Chelsea College, Hortensia Road, London SW10 oQX In Vol. 2 of' The Whole Fungus' (Kendrick, 1979), Luttrell, during a discussion on yeasts, suggested that the Sporobolomycetaceae is a heterogeneous taxon and in particular that Sporobolomyces and Bullera differ fundamentally. His remarks were supported by detailed illustrations of the two genera. His contention was that, whereas the aerial spore of Sporobolomyces is borne asymmetrically on its sterigma (i.e. heterotropic, see Pegler & Young, 1979), that of Bullera is placed symmetrically (orthotropic) with a cross-wall visible where spore and sterigma meet. If this were true, presumably different mechanisms of spore discharge would be involved and there would be no distinctive feature linking Bullera with the Basidiomycetes. In an attempt to confirm Luttrell's suggestion, a culture of Bullera alba (Hanna) Derx (IMI 86680) was obtained from the Commonwealth Mycological Institute. Subcultures were examined by one of us (C.T.!.) microscopically and in addition the other (T.W.K.Y.) prepared SEM pictures (Figs 1-6). Both of us observed that the violently-discharged aerial spore was of the ballistospore type found in Hymenomycetes.
Trans. Br. mycol. Soc. 76 (1), (1981).
Indeed, spore liberation in Bullera involving drop development at the hilar appendix just before discharge was reported long ago (Ingold, 1939). It seems to be exactly comparable with what occurs in Sporobolomyces (Buller, 1933; Miiller, 1954)· Luttrell figured a cross-wall where spore and sterigma meet, but it would be difficult to demonstrate this by light microscopy as the junction is only 0'4 pm wide. REFERENCES
BULLER, A. H. R. (1933). Researches on Fungi. 5, London: Longmans, Green & Co. INGOLD, C. T. (1939). Spore Dischargein Land Plants. Oxford: Clarendon Press. KENDRICK, B. ed. (1979). The Whole Fungus. 2, Ottawa: National Museum of Natural Sciences, National Museum of Canada, and the Kananaskis Foundation. MULLER, D. (1954). Die Abschleuderung der Sporen von Sporobolomyces (Spiegelhefe) gefilmt. Friesia 5, 65-'74· PEGLER, D. N. & YOUNG, T. W. K. (1979). The Gasteroid Russulales, Transactions of the British Mycological Society 72, 353-388.
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