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Patterns of seasonal succession offreshwater epipelic algaeF.E. Round aa Department of Botany , University of BristolPublished online: 17 Feb 2007.

To cite this article: F.E. Round (1972) Patterns of seasonal succession of freshwater epipelicalgae, British Phycological Journal, 7:2, 213-220, DOI: 10.1080/00071617200650221

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Br. phycol. J. 7:213-220 15 July 1972

PATTERNS OF SEASONAL SUCCESSION OF F R E S H W A T E R EPIPELIC A L G A E

By F. E. ROUND

Department of Botany, University of Bristol

The seasonal succession of algal species in the epipelon of two small pools over a period of three years is described in relation to changes in silica, nitrate-nitrogen and phosphate- phosphorus concentrations in the water above the sediments. Recurring patterns of seasonal growth of the various species are discussed.

Much has been wri t ten over the years concerning the seasonal succession o f bo th mar ine and freshwater p l ank ton ic algae but, wi th the no tab le except ion o f a few intensely s tudied species, the control l ing factors cont inue to be elusive. In a recent paper , R o u n d (1971), some prob lems were discussed with reference to the succession o f species o f f reshwater p lank ton and it was po in ted ou t tha t the ac tual seasonal succession o f the non-p lank ton ic algal popu la t ions had ye t to be documented in any detail . Cer ta in pat terns o f seasonal d i s t r ibu t ion and the concept o f ' shock ' events in br inging abou t the sudden col lapse o f popu l a - t ions was pos tu la ted to expla in the often s imul taneous col lapse o f popu la t ions in geographical ly isola ted lakes. These ' shock ' per iods cor responded to per iods o f r ap id change in the aqua t ic hab i t a t usually associa ted with cri t ical levels being reached in the physical environment . These opera te largely t h rough strat if icat ion and de-s t ra t i f icat ion in bodies o f water deep enough to fo rm a thermocline. D a t a for a s imilar s tudy o f epipelic communi t ies are scarce and two years ' cont inuous observat ions are a min imum requirement . The fol lowing da t a were ob ta ined over three years and f rom ext remely shal low and small ponds where no th ing more than d iurna l thermal s trat i f icat ion is l ikely to occur, thus e l iminat ing no rma l s t rat i f icat ion as a direct factor . However , s tudy o f such a s i tuat ion has cons iderable bear ing on s imilar communi t i es in larger bodies o f water capab le o f the rmal s trat i f icat ion since the epipel ic popu la t ions in large water bodies tend to occur only above the thermocl ine wi th the result tha t the effects o f s t rat i f icat ion on this associa t ion are no t necessari ly so d ramat ic . The seasonal sequence o f species is, however, jus t as p ronounc e d as it is in the p lankton .

M E T H O D S

A small amount of surface sediment was drawn off by means of a pipette and rubber bulb from the ponds approximately once every two weeks. The sediments were allowed to settle and then poured into Petri dishes and the excess water removed. Cover glasses were placed on the surface and left for 24 h. These were then removed and the algae adhering to the undersurface identified and counted along standard transects (20 mm), after which the whole coverglass was scanned for rare species. Silicate, nitrate and phosphate content of the water drawn off from directly above the sediment of the ponds was estimated by the methods in Mackereth (1963). Pool 1 was extremely shallow, a few centimetres of water at most covering the sediment. Pool 2 was approximately 50 cm deep. The outflow of Pool 1 ran into Pool 2. The two pools are situated in the Botanical Garden of the University of Birmingham and are

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214 F.E. ROUND

so close as to be under virtually identical conditions of shade, etc. Water percolated into Pool 1 from a surrounding rockery and then overflowed down a short channel into Pool 2. Pool 1 was approximately 1 m and Pool 2 was several metres wide.

RESULTS

Figs 1 and 2 show the seasonal distribution of the major diatoms and other algae on the sediments of the two pools plotted on a similar basis together with data for silicate, phosphate and nitrate contents of the water. The vertical lines are drawn quite arbitrarily mid-way through the year and at the end of the year. These points are, however, important in that they correspond very approximately to the point of longest and shortest day length, i.e. of greatest and least solar radiation and of high and low water temperature.

A characteristic of these seasonal cycles is their general reproducibility from year to year. Obviously there is some variation but this is only to be expected since the 'correct' set of conditions for each species is dependent on the vagaries of the climate in each year. However, without this reproducibility the problem would be even more baffling than it is. For convenience of discussion the species with clear-cut distributions are dealt with first. These can be separated into groups growing at approximately the same time in each year.

Stauroneis anceps Ehrenb., Nitzschia dissipata (Kiitz.) Grun. and Oscillatoria sp. grew in the early part of the year (January/February-May/June) as tem- perature and light intensity were increasing and then declined while these factors were still increasing; one must not, however, presuppose that these are neces- sarily the limiting factors. Navicula pupupla var. capitata Hust. had a slightly more extended growth period but was confined to the first six months of the year in Pool 2 while in Pool 1 it continued growth until slightly later (August) in Years 1 and 3. For some reason its whole growth period was shifted to a later period (May-November) in Year 2.

Nitzschia acicularis W. Sm. is a mid-summer (i.e. high light/high temperature) species in both ponds. In Year 1 and Year 3 it was prominent in June/October but, interestingly, in Year 2 it commenced growth early (January/February) in both pools and ceased growth early (June/July). Cymatopleura elliptica (Brrb.) W. Sm. is another mid-season species and was again maintained in the popula- tion until November in Year 2 (cf. Navicula pupula var. capitata). In Pool 1 this species occurred only in Year 3, somewhat earlier in the year. This is such an obvious species that it could not have been overlooked in previous years. Another June-October species is Navicula pupula Kiitz. in Pool 2, though in Year 2 it occurred much later (September-December). Interestingly, this species followed its variety capitata in the seasonal sequence in both pools but in Pool 1 it grew much later (see below).

Caloneis amphisbaena (Bory) CI., Navicula cuspidata Kiitz., N. radiosa Kiitz., N. pupula (in Pool 1), and N. oblonga Kiitz. (in Pool 2), fall into the category of species growing in cold water under low light conditions. However, in Pool 1, N. oblonga was more widespread throughout the year, though it was still pos- sible to discern a pattern of seasonal distribution with a fairly extended period of occurrence in the first six months of each year followed by a second small burst of growth in August/September.

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S e a s o n a l success ion o f epipel ic a l g a e 215

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FIG. 1. T h e s e a s o n a l c h a n g e s in n i t r a t e - n i t r o g e n , p h o s p h a t e - p h o s p h o r u s , s i l icon a n d epipel ic a l g a e in P o o l 1 o v e r a t h r e e - y e a r pe r iod . N i t r o g e n as m g N O 3 - N ] I , p h o s p h o r u s as m g PO4-P]I , s i l icon as m g Si/1 A l g a l c o u n t s p lo t t ed as log~0 cell n u m b e r s . -+- ind ica tes p r e sence b u t n o c o u n t . A b b r e v i a t i o n s o f a l ga e as fo l lows ( fo r F igs 1 a n d 2) : St a n : Stauroneis anceps, N a c r = Navicula cryptocepha, N a cu = Navicula cuspidata, N a p u = Naviculapupula, N a p u c a = Naviculapupula v. capitata, N a h u ca = Navicula hungarica v. capitata, N a o b : Navicula oblonga. N a r a : Navicula radiosa, N i a c = Nitzchia acicularis, N i di = Nitzschia dissipata, N i p a = Nitzschia palea, C a a m = Caloneis amphisbaena, Cy el = Cymatopleura elliptica, C y so = Cymatopleura solea, CI = Clos- terium spp . , Os : Oscillatoria spp. , Sy = Synura spp. , C h = Chlamydomonas spp . , C r = C r y p t o m o n a d s , E u : E u g l e n o i d s .

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216 F . E . R O U N D

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Seasonal succession of epipelic algae 217

Three species, Navicula cryptocephala Kiitz., Navicula hungariea var. capitata (Ehrenb.) C1. and Nitzschia palea (Kiitz.) W. Sin., have more extended growing periods. However, two of these, N. cryptocephala and N. palea, are notoriously difficult to identify since many closely related forms can be grouped together and in counting live material less confidence can be placed on the results for these two species. Indeed, there is evidence of two or three growth periods on the graphs of the two species, suggesting the existence of morphologically similar forms varying in their ecological requirements. If this is so one must discount the possibility that some species can grow through the 'shock' periods to which most of these microscopic algae are susceptible. Navicula hungariea vat. capitata is, however, one of the easily recognisable species and is unlikely to be confused with another diatom. In Pool 2 its presence extended roughly from January to October, while in Pool 1 it was present throughout the year but in extremely low numbers in October-November (December) in two of the three years. In Year 2 no reduction in cell numbers occurred in the autumn period which is notably a time of low algal growth in this habitat (a very similar pattern was shown by Nitzsehia palea in Pool 1).

The few remaining algae are difficult to fit into any pattern, possibly because the plots are of groups of species, e.g. cryptomonads and euglenoids. How- ever, the latter, at least, seem to show little growth in June]July/August; this is rather surprising since they are usually associated with high organic matter content which usually coincides with periods of high temperature and hence high rate of decay. In Pool 1 these flagellates occurred only in the first year, a feature which may be related to the chemical conditions which obviously underwent a change after this.

The chemical data show some considerable differences from year to year, due, I believe, to cultivation and fertilisation of the adjacent soils through which the water percolated into these pools. Pool 1 was fed entirely by water dripping out of the soil and in Year 1 had high silicate and phosphate concentrations but very low nitrate. Nitrate then increased somewhat in Years 2 and 3. Pool 2 receives water draining from Pool 1 and from the surrounding soil but, being larger, is more buffered; even so, there was again a tendency for high silicate and phosphate values in Year 1, though nitrate was fairly constant through the three years.

DISCUSSION

A study of the data raises many problems though only a few possible explana- tions can be suggested.

The sequence (Fig. 3 (a)) envisaged by Round (1971) with four growth periods (A - D) during the year was shown to occur fairly frequently in the plankton though the four growth periods tended to fuse as eutrophication in- creased. A hypothesis was suggested based on the assumption that species may persist in the plankton for some period after active growth has ceased and thus seasonal patterns might extend more (as in Fig. 3 (b)). Such a situation probably applies to some species of the epipelic flora and it is possible to select species from these two pools to fit such a graph (Fig. 3 (c)) in which A is represented by a species such as Stauroneis anceps, B by Nitzschia aeicularis, C by Navieula pupula in Pool 2 and D by Navicula cuspidata. As with the plankton the growth

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218 F. E. R O U N D

(b)

(e)

O F M A M O O A S O N D

FIG. 3. (a) Hypothetical growth curves for freshwater populations, assuming fairly rapid death of population following termination of growth (see text for further detail). (b) Hypothetical growth curves with live ceUs remaining in the habitat for some time after division has ceased; arrows indicate times when the populations arc subjected to 'shock' of some kind. (c) Some patterns of epipclic diatom growths from the two pools investigated. (a) and (b) based on Round (|971).

of most species tends to fit into one or other of these periods and only a few algae extend over two or more periods [though, as explained above, this may be due merely to an inability to distinguish closely related forms, whereas the precision of the three cycles of the readily identified Stauroneis anceps compares well with the much better documented cycles of the planktonic species Asterio- nellaformosa Hass. and Melosira italiea subsp, subarctica O. Miill (Lund, 1950, 1954) ]. However, the concept of 'shock' periods in mid-summer and mid- winter is only applicable to some species; others, e.g. Nitzschia aeicularis and Navicula euspidata, extend through these periods, a situation which had also been envisaged for the plankton by Round (1971). The idea of four periods in which growth is most likely to occur is perhaps still valid but some of the epipelic community can obviously grow at other times and the models in Fig. 3 (a) and 3 (b) are .therefore too simple. On the other hand, there is some evi- dence that the epipelic populations build up fairly fast and disappear equally fast and do not behave as in Fig. 3 (b). That no species extends over the whole year is not surprising since, as Hutchinson (1967) points out with relation to the plankton, the changes in climate and water chemistry during an annual cycle in a lake are probably greater than those in the soil chemistry over several millennia and these latter changes have obviously induced great changes in the flora of lakes. Indeed, it is perhaps surprising that the periods of growth of

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Seasonal succession of epipelic algae 219

epipelic algae are measured in months rather than weeks. The seasonal succes- sion of algae in this habitat is not comparable to the type of succession in which one species displaces another since at almost any time of the year several species are co-existing. The sediment may however provide innumerable micro-habitats and the sampling technique aggregates the algae from these.

Why do some species occur in only one or two years of the three sampled ? It could be that conditions are only occasionally favourable and if this is so it is likely that some very special factor is controlling the distribution whereas repeated occurrences are linked with cyclical phenomena of light, temperature, chemicals, etc. Alternatively sources of inoculum may be needed, though, since the waters are a few yards apart, it is unlikely that euglenoids, for example, are not repeatedly transferred from Pool 2 to Pool 1. Yet they are present in Pool 2 in each of the three years but only in the first year in Pool 1. No attempt was made to prevent transfer, even in sampling, and all species must have been transported backwards and forwards many times. These species may, however, be constantly present in such small amounts that the sampling technique does not detect them, though this is unlikely. It might be argued that the initial high levels of phosphate (or low levels of nitrate) in Pool 1 are responsible for the presence of the cryptomonads and euglenoids in Year 1 though this is difficult to reconcile with their occurrence throughout the three years in Pool 2.

A related problem is the apparent absence of species such as Stauroneis anceps for seven months of each year. 'Apparent absence' here means from counts and, since counting was done at frequent intervals and no cells were found in transects across the coverglass, it must be assumed that very few, if any, cells were present. Is re-inoculation necessary every January ? This seems unlikely and the possibility of auxospore formation arises. Such spores are rarely recorded in nature for pennate diatoms but it must be admitted that they would be diffi- cult to detect.

Transfer of species from site to site, discussed in Round (1971) for the plank- ton, is even more likely for the epipelic species. However, in spite of such ready transfer, theoretically leading to a uniform flora in all sites, it is obvious that these apparently very similar habitats are highly selective and only such species grow as are adapted to the micro-habitats. No explanation can be offered for this selection. Presumably, all factors such as grazing, parasitism, species inter- action, etc., combine with the physico-chemical factors to produce the com- plexities of distribution.

Doubts are frequently cast on the validity of the species and varieties des- cribed by diatomists since these are usually based merely on morphological variation. However, that these varieties are only the beginning of the problem of actual morphological variation is now being revealed by electron microscopy. In addition, physiological variants have also been discovered. An ecological approach reveals that the morphological varieties have different habitat require- ments [cf. the distribution of varieties of Fragilaria in the post-glacial period, Round (1957, 1961) ] and can therefore be considered as physiological variants also. The case of Navicula pupula and N. pupula var. capitata is interesting in that in both pools the variety precedes the species in each year with very little overlap. The habitat conditions in these seasons are so different that on this basis alone one must assume that the physiological differences between these

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220 F .E . ROUND

diatoms are also great. Thus from ecological and physiological considerat ions as well as f rom light microscopy and electron microscopy it is becoming a bun - dant ly obvious that there are even more ' t axa ' o f d ia toms than hitherto believed.

REFERENCES

HtrrCHINSON, G. E., 1967. A Treatise on Limnology. Iiol. II. Introduction to Lake Biology and the Limnoplankton. New York.

L~NO, J. W. G., 1950. Studies on Asterionella formosa Hass. IL Nutrient depletion and the spring maximum. J. Ecol., 38: 15-35.

Lur,~o, J. W. G., 1954. The seasonal cycle of the plankton diatom, Melosira italica (Ehr.) Kiitz. subsp, subarctica O. Miill. J. Ecol., 42: 151-179.

MACKERETH, F. J., 1963. Some methods of water analysis for limnologists. Scient. Pubis Freshwatr. biol. Ass., 21 : 1-70.

RotmD, F. E., 1957. The late-glacial and post-glacial diatom succession in the Kentmere Valley Deposit. New Phytol., 56: 98-126.

Rot:r,a3, F. E., 1961. The diatoms of a core from Esthwaite Water. New Phytol., 60: 43-59. RooNI~, F. E., 1971. The growth and succession of algal populations in freshwaters. Mitt.

int. Verein. theor, angew. LimnoL, 19: 70-99.

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