Trans. Br. mycol. Soc. 73 (1) 109-116 (1979)

l 109 ]

Printed in Great Britain

PERIODICITY OF AQUATIC HYPHOMYCETES IN THESUBARCTIC

By A. MOLLER-HAECKEL

Department of Animal Ecology, University of Umed, Sweden

AND L. MARVANOvA

Czechoslovak Collection of Microorganisms,J. E. Purkyne University, Brno, Czechoslovakia

The annual periodicity of conidial production in some hyphomycete species in a subarcticstream has been measured by 'drift' (conidia suspended in stream water) and 'colonization'(conidia trapped on Plexiglass slides during 24 h periods). Two maxima were found, a mainone in autumn and a smaller one in spring. Increasing quantities of conidia appeared insummer before leaf fall. A comparison is made of the annual pattern of sporulation in thesubarctic and in southern England, and the influence of water temperature, precipitation andlight, including photoperiod are discussed.

Seasonal variations in the occurrence of conidia offreshwater hyphomycetes have been observed bymany mycologists, but few quantitative studieshave been made. Willoughby & Archer (1973)counted the number and abundance of hypho-mycete species that colonized twigs, in an Englishstream in the Lake District during the year andfound that hyphomycete conidia were moreabundant during the wet period (September toNovember) than during the dry period (May toJune). Iqbal & Webster (1973, 1977) counted thenumber of species and conidia in streams nearExeter, England, during the year and founddistinct and different annual periodicities indifferent species. Most showed high sporulationduring autumn, winter and spring with almost noconidial production during the summer months.Two exceptions were found; Tricladium gracilewhich had limited conidial production fromDecember to April, and Lunulospora curuula withrestricted sporulation from August to November.

We have studied the presence of conidia inwater and on exposed Plexiglass slides in a smallstream in the subarctic over 2 years under differentenvironmental conditions.

METHODS

The investigation area is shown in Fig. 1. TheNjakajokk streamflowsfrom lakes and runs throughseveral fenny regions. Water temperature at themain sampling site 3 (Fig. 1) did not exceed 15 °Cand from the end of October until the beginningof May it was at 0'1 ° (recorded by Lambrecht

thermograph) (Fig. 2). Conductivity varied at thesame place between 130 and 176 p,s and the pHfrom 7'3 to 7'8 during the investigation period.From June 1975 to October 1976 untreated watersamples, collected from the Njakajokk, site 3 at10 a.m. were examined for hyphomycete conidia,which were identified and counted under aninverted microscope. These samples representconidial 'drift' or detached conidia, which weredrifting downstream. Conidia were also sampledby trapping on Plexiglass slides (total surfacearea 10 em") exposed for 24 h at the same site andat the other sites (Fig. 1). These samples aredescribed as conidial 'colonization'. The methodshave been described previously (Miiller-Haeckel,1967, 1970; Millier-Haeckel & Marvanovll, 1977).All results are represented as means of 10 dayperiods with three to nine samples in each decade.Occurrence of the dominant species has beencalculated as the mean percentage of 35 decades(number of decades in which samples could betaken). From December until the middle of Aprilonly a few samples could be taken, as in theextreme cold the sampling hole froze over aftera few hours.

RESULTS

Production of conidia during the year

Fourteen species of hyphomycetes were identifiedin the water from the Njakajokk (' drift ') and onthe exposed Plexiglass slides (' colonization ') atsite 3 namely; Flagellospora curvula Ingold,Alataspora acuminata Ingold, Lemonniera aquatica

0007-1536/79/2828-5110 $01.00 © 1979 The British Mycological Society

110 Periodicity of aquatic hyphomycetes in the subarctic

Njakajokk System

23 31 8 20 10 1Site July July Aug. Aug. Sept. Oct.

1 2 6 42 55 164 812 28 72 125 451 1915 7733 116 114 70 116 4104 22414 58 98 12 84 1147 7895 6 180 2016 4 12 316 1727 4 5 195 4978 6 11 652 666

Fig. 1. A map of the investigationareawith thesamplingsites along the Njakajokk stream and a table of conidia'colonization' (number of all conidia 10 cm-2 Plexi-glass slide during 24h) at the sampling sites from Julyto October 1975.

de Wild., Heliscus lugdunensls Sacco & Therry,Anguillospora longissima (Sacc. & Syd.) Ingold,Centrospora angulata Petersen, Lemonniera terrestrisTubaki, Tricladium splendens Ingold, Tetra-cladium marchalianum de Wild., Volucrisporagraminea Ingold, McDougall & Dann, Margarita-spora aquatica Ingold, Geniculospora inflata(Ingold) Nilsson ex Marv. & Nilsson, Clavatosporastellatus (Ingold & Cox) Nilsson ex Marv. &Nilsson, Taeniospora gracilis Marv. The firstseven of these occurred fairly regul arly in 'drift'as well as 'colonization' at the appropriate season(Fig. 3). Three species were predominant;Flagellospora curvula (61 %), Lemonniera aqua-tica (19 %) and Alatospora acuminata (16 %). Theother eleven species accounted for 9 % of the sumof the 'colonized' conidia during the year. Fig. 4shows the seasonal quantitative distribution of allhyphomycete conidia in 'colonization' samples atsite 3 and Figs. 5'-7 that of the three main species.In the 'drift' samples the number of conidia variedgreatly from day to day. Fig. 8 shows the seasonalvariations in the conidial ' dri ft ' at site 3. Both in

'drift' and 'colonization ' the main maximum inconidial production occurred from September toOctober and a smaller one in April. The minimaof sporulation were in Mayor July and inDecember. It seems significant that an increasein conidia occurred before leaf fall (mid August inthe Abisko region) .

Differences in the annual patterns of ' colonization '

Lemonniera aquatica showed poorer conidial pro-duction from May to October 1976 than in 1975.Flagellospora curvula and to a lesser extentAlatospora acuminata had a lower conidial'colonization' from September to October 1976but a higher one in July 1976, compared with1975. Lower water temperatures (Fig. 2), greaterprecipitation in May 1975 (Fig . 9) and/or fewerhours of sunshine (Fig. 10) are thought to havefavoured conidial production in Lemonnieraaquatica in 1975. Flagellospora curvula andAlatospora acuminata seemed to be less sensitiveto these variations, but higher conidial productionin July 1976 coincided with high precipitation(Fig. 9).

Seasonal conidial production at different sites

The eight sampling sites in the Njakajokk systemshowed very different quantities of conidia, but atall sites highest quantities were found in Septemberor October. Least conidia were found immedi-ately downstream from the lakes, at sites 1 and 5,despite the large numbers of birch, alder andwillow along the banks of the Njakajokk in theseareas (Fig. 1).

DISCUSSION

Iqbal & Webster (1973, 1977) and Willoughby &Archer (1973) investigated the annual periodicityofhyphomycete sporulation in the north temperatezone (51 and 540 N), whereas we have studiedconditions in the subarctic, 660 N (Miiller-Haeckel& Marvanova, 1977), and 68° N (Miiller-H aeckel,1977). Water temperature in the streams insouthern England did not fall below 2'5 0 but inthe subarctic region water temperature was at 0'4and 0 '1 0 respectively from the end of October tothe beginning of May. Since many hyphomycetespecies prefer lower temperatures for bothmycelium growth and sporulation (Thornton,1963; Nilsson, 1964; Webster, Moran & Davey,1976), it is understandable that sporulation did notdecrease with the fall of temperature in the latesummer and autumn. The maximum productionof conidia occurred from September to October

A. Muller-Haeckel and L. Marvanovd 111

14

G 12~~

>.'"-e

100

'-0c:'"" 8,5"3e

6 ~~ ~"0.E~~

""'"

4~

2

III III II IIM J

.:.

I

::.::.

II IIIJ

II IIA

II IIIS

I 1976

· ·· I I. ~·;.];] .~~ .II IIIo

Fig. 2. Water temperature in the Njakajokk at sampling site 3 during 1975 and 1976 from May toOctober (means of to-day periods).

A SON D F M A M

( 1 ) f7ageIlOSpora(u""la ~~~~1m(2 ) A tatospora acum inate(3) Lemonniera aquat ica(4 ) Heiiscus lugdunensis D oft

(5) Anguillospora !ongissima n(6) Ctavatospora stellato

(7 ) Centrospora angulata -

(I )68 ' N 1-'-".~(I) 5 I o,C '/t§~WW

A S o

+4!I :W/~:"~~ +;: ' IVIN D J F M A M

1 Drift

Fig. 3. Above: The occurrence of seven hyphomycete species during the year (1975-6) at sampling site3 in 'drift' and 'colonization'. Below: A comparison of the annual pattern of occurrence (' drift ') inFlagellospora curvula in the Njakajokk (690 N) and in the river Creedy (510 N), Iqbal & Webster (1973).The darker parts of the bars denote the chief maxima of conidia production.

112

103

.<::

"""!Meo

0~

102'":;'20u'-0...'",D

E::lZ

101

Periodicity of aquatic hyphomycetes in the subarctic

J JASOND AM

1975J A S 0

1976.

Fig. 4. Annual periodicityof conidia colonization (sum of alI species) in the Njakajokk samplmg Site3during 1915-6. The horizontal bar denotes ice cover.

in the Njakajokk. This was found also to be thecase in the Kaltisjokk, northern Sweden (Miiller-Haeckel & Marvanova, 1977). This is probablya consequence of leaf fall which greatly increasesthe amount of available substrate. This maximumoccurred later at 51° N (Iqbal & Webster, 1973,1977)·

A comparison of annual conidial production insouthern England and in Abisko may be made forFlagellospora curoula which is dominant at bothplaces. The rapid decrease of conidial productionby this species in the Njakajokk during November-December cannot be explained by deficiency ofsuitable substrate. It is possible that hyphomycetespecies produce the greatest amount of conidia(assuming availability of substrate) if watertemperature is between 6 and 2° (as at 51 and 68° N,at the time of conidial maxima), but that pro-duction declines at lower temperatures, as atNjakajokk in winter. We know nothing, however,about the possible influence of either stronglyreduced light intensities or extremely shortenedphotoperiod on hyphomycete sporulation, con-

ditions which occur together with the low watertemperature in the subarctic winter.

The relatively high conidial production duringthe early spring (in April under ice) may be dueto the availability of submerged leaves and leaflitter which were not entirely consumed during theshort autumn and to more favourable light con-ditions. At spring flush large quantities of leaflitter together with the hyphomycetes are washeddownstream causing a drop in conidia in May. Theincrease in sporulation from the minima at winterand after the spring flush are difficult to explain.It remains to be seen if the photoperiod functionsas an annual' Zeitgeber' to endogenous periodicityin hyphomycete sporulation activity, as it does toother processes in other organisms.

Alatospora acuminata evidently tolerated bestthe low water temperatures and/or the unfavour-able light conditions during the subarctic winter.Even the differences in weather between the twoyears are barely reflected in the seasonal patternof conidial production in Alatospora acuminata.The much higher conidial production in July

103

A. Miiller-Haeckel and L. Marvanovd 113

..c:

"'" I

~ -r-ME Io

I0-c-; 102

":a'20u'-0....",c,E"Z

101

J A1976

s . 0

Fig. 5. Annual periodicity of conidia colonization in Flagellospora curvula in the Njakajokkat samplingsite 3 during 1975-6. The horizontal bar denotes ice cover.

1976 may be due to the high precipitation in thismonth which would agree with the findings andopinion of Willoughby & Archer (1973). Withrespect to the different weather conditions in1975 and 1976, Lemonniera aquatica seemed to bethe most sensitive species to one or more of thefollowing factors; less precipitation, more sunshinehours, higher water temperatures during latespring and summer 1976. Unfortunately it cannotbe determined which of these factors had a nega-tive influence upon sporulation. Interestinglyunicellular algae in the Njakajokk, investigated atthe same time and with the same methods gaveabsolutely inverse results, i.e. high quantities andpronounced annual periodicity patterns in 1976,much lower quantities and less clear patterns in1975 (Miiller-Haeckel & Hakansson, in press).

At all sampling sites Flagellospora curvula wasthe dominant, Alatospora acuminate second (withthe exception of site 3), while Lemonniera aquaticawas least abundant, especially in the fenny areas.At all sampling sites most conidia were found inSeptember or October, but an increase of conidiawas often recorded in July, prior to leaf fall. Thelow quantities of conidia below the lakes (Fig. 1,

sites 1 and 5) were accompanied with nighabundance of benthic algae. The possible antagon-ism which is indicated in this relationship has beendealt with by Marvanova & Marvan (1963).

The study was supported by the SwedishNatural Science Research Council.

114 Periodicity of aquatic hyphomycetes in the subarctic

....-II

.e 10' Iv~ IN

Eo I

0- I'":a I'"0 Io

.....I0...

" 10· I.nE::l Iz

IIIIII

J A S 0 N DI A M J J A S 01975 1976

Fig. 6. Annual periodicity of conidia colonization in Lemonniera aquatica in the Njakajokk at samplingsite 3 dur ing 1915-6 . The horizontal bar denotes ice cover.

..c "'1v~

JN

Eu

0-ee:a'a0o..... I0...".nE::lZ

I1

I

II

A S 0 N D 1 A M J J A S 0

1975 1976

Fig. 1. Annual periodicity of conidia colonization in Alatospora acuminata in the Njakajokk at samplingsite 3 du ring 1975-6 . The horizontal bar denotes ice cover.

103

~

'":;:;·20u

""'0..Q)

.DE:::lZ

102

A. Midler-Haeckel and L. Marvanovd

J A S

1975

o N D A M J A

1976

S 0

Fig. 8. Annual periodicity in conidial drift (sum of all species) in the Njakajokk at sampling site 3 during1975-6. The horizontal bar denotes ice cover.

70

50 iEE • ,

..c:

I•;:

0E ,C , ,s

••••••

•?~

30 •.6.·u

Q)

.~6::~. .~

,lit'

• •• ~n~

10 ~::::

mf~.J F M A M J J A S 0 N D I J

• •

••

I •~~ •~)~ • •,::U

~~PJ~ ~F M A M J J A S 0

Fig. 9. Variations in precipitation (sum of months) at Abisko during 1975-6. Points mean the normallevels (mean of the years 1931-60). (Data from the Abisko Scientific Research Station.)

116 Periodicity of aquatic hyphomycetes in the subarctic

300

..c<: 200o.ge::lo

..c

"c~"::lrIl 100

.J F M A M J J A SON DI J F M A M J J A SON D

1975 1976

Fig. 10. Variations in the hours of sunshine (sum ofmonths) at Abisko during 1975-6. Points mean thenormal levels (mean of the years 1931-60). (Data from the Abisko Scientific Research Station.)

REFERENCES

IQBAL, S. H. & WEBSTER, J. (1973). Aquatic Hypho-mycete spora of the river Exe and its tributaries.Transactions of the British Mycological Society 61,331-346.

IQBAL, S. H. & WEBSTER, J. (1977). Aquatic Hypho-mycete spora of some Dartmoor streams. Trans-actionsof the British Mycological Society 69, 233-241.

MARVANovA, L. & MARVAN, P. (1963). Einige Hypho-myceten aus fliessenden Gewassern des Hruby[esenik, Acta Musei Silesiae Ser. A. 12, 101-118.

MULLER-HAECKEL, A. (1967). Tages- und jahres-periodik von Ceratoneis arcus Kiitz. (Diatomeae).Oikos 18, 351-356.

MULLER-HAECKEL, A. (1970). Messung der tages-periodischen Neukolonisation von Algen in Fliess-gewassern, Oikos Supplementum 13, 273-274.

MULLER-HAECKEL, A. (1977). Annual production ofhyphomycete conidia in a subarctic stream. Oikos29, 396-397.

MULLER-HAECKEL, A. & HAKANSSON, H. The diatom

flora of a small stream near Abisko (SwedishLapland) and its annual periodicity, judged by driftand colonization 1975/76. Archiv fur Hydrobiologie(In the Press).

MULLER-HAECKEL, A. & MARVANovA, L. (1977).Konidienproduetion und -kolonisation von Suss-wasser-Hyphomyceten im Kaltisjokk (Lappland).Botaniska Notiser 129, 405-409.

NILSSON, S. (1964). Freshwater hyphomycetes.Symbolae Botanicae Upsalienses 18, 5'-130.

THORNTON, D. A. (1963). The physiology and nutritionof some aquatic hyphomycetes. Journal of GeneralMicrobiology 33, 23-31.

WEBSTER, J., MORAN, S. T. & DAVEY, R. A. (1976).Growth and sporulation of Tricladium chaetocladiumand Lunulospora curvula in relation to temperature.Transactions of the British Mycological Society 67,491-499.

WILLOUGHBY, L. G. & ARCHER, J. F. (1973). Thefungal spora of a freshwater stream and its colon-ization pattern on wood. Freshwater Biology 3,219-239.

(Accepted for publication 10 November 1978)