Hydrobiologia 369/370: 127–131, 1998. 127M. Alvarez-Cobelas, C. S. Reynolds, P. Sanchez-Castillo & J. Kristiansen (eds), Phytoplankton and Trophic Gradients.c 1998Kluwer Academic Publishers. Printed in Belgium.

Responses of the phytoplankton to a deliberate attempt to raise the trophicstatus of an acidic, oligotrophic mountain lake

C. S. Reynolds, G. H. M. Jaworski, J. V. Roscoe, D. P. Hewitt & D. G. GeorgeNERC Institute of Freshwater Ecology, Windermere Laboratory, GB-LA 22 0LP Ambleside, U.K.

Key words:phytoplankton, trophic status, phosphorus, eutrophication, species composition

Abstract

The paper reports the impact of a sharp artificial enrichment of the available phosphorus in a small, acidic andoligotrophic corrie lake and its effects upon the phytoplankton supported. Annual average chlorophyll increasedtenfold within two years, from� 1:2 to 12.6�g chla l�1, but the species represented by large populations are thesame as previously. Chrysophyte species, however, make up a smaller fraction of the total crop.

Introduction

Seathwaite Tarn is a small upland, acidic and olig-otrophic water body in the English Lake District. It isa classic corrie lake, although its level has been raisedbehind a concrete dam, in order to provide compensa-tion water for the River Duddon. Its level is accordinglysubject to artificially enhanced fluctuations. Other lim-nological properties of the lake are given in Table 1.

The catchment (4.80 km2) is based on Ordovicianintrusives (tuffs and andesites) and receives an annu-al rainfall of 2.0–2.2 m. It is classically barren: theroughFestuca-Nardusgrassland alternates with loosescrees and local pockets ofSphagnumbog. There isprecious little neutralising capacity in the scant soil sothe inflowing water to the Tarn is acidic (pH 5.1–5.4),base-poor (bicarbonate alkalinity, zero) and deficientin biologically available phosphorus (< 1 �g P l�1).Accordingly, the lake is normally limpid and free ofsignificant turbidity due to algae.

The site was selected for a large-scale field experi-ment to test the concept of reversal of acidification byuse of phosphate fertilser, rather than the more usuallime treatment. The rationale for this was proposed byDavison (1987) and authenticated in an experimentalpilot restoration of a water-filled former sand quarry(Davison et al., 1989). Essentially, the biological pro-duction promoted consumes acidity (carbon dioxide,nitrate) and generates base. From March 1992, a solu-

tion of a specially formulated phosphate fertiliser wasdosed at fortnightly intervals to the Tarn in order togive a notional average concentration of 20�g P l�1.In 1993, the dosing rate was increased to a maximumof28�g P l�1. In both years, almost all the phosphate wasassimilated biologically with the consequent stimulusto pelagic production. The pH was lifted substantially(> 6) as hypothesised.

Apart from a short period at the end of 1992,the measured concentration of dissolved phosphorusremained< 0:6�g P l�1 throughout 1993, confirmingthat the addition had been insufficient to saturate thepotential phosphorus consumption of the phytoplank-ton. After July, 1993, however, free nitrate remainedat levels below analytical detection. These results havealready been reported in summary form (Davison et al.,1995). This paper is concerned only with the repons-es of the phytoplankton with special reference to thechanges in the species-structure of the assemblage. Inparticular, it seeks to review the relevance of some sup-positions about the influence of nutrients on the assem-bly of planktonic communities and upon the tenancyof the concept of a trophic spectrum.

Methods

Samples for chlorophyll determination and algal enu-meration have been collected at approximately fort-

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Table 1. Limnological data of the study site

Seathwaite Tarn, Cumbria, UK

Latitude: 54�230 N Longitude: 3�90 W

Altitude: 375 m Ice cover: typically 10–20 d annum�1

Area: 0.267 km2 Volume: 3:28� 106 m3

Max depth: 26 m Mean depth: 7.2 m

Residence time: 120–200 d Mixing frequency: dimictic with winter ice

pH: 5.1–5.4� Secchi disc: 8–15 m�

Max Total P: � 2 �g P l�1� Max and Min SRP always< 1 �g P l�1�

Alkalinity 0� Salinity� 0:001%

� natural state; please see text for experimentally-imposed changes

Table 2. Comparison of trophic-state indicators before (1991) and during experimental enrich-ment of Seathwaite Tarn (1993)

1991 1993

1. Sequence of relative species abundance

Chrysolykos/Chlorella/Dinobryon Monochrysis/Chlorella

! Chlorella/Monochrysis ! Chlorella

! Chlorella/Monochrysis

! Cryptomonas

2. Species accounting for:

> 0:5% 35 18

> 5% 7 4

> 25% 2 2

3. Phases of dominance per year.

�1 2

4. Peaks of biomass per year.

2, March-April and Oct-Nov 3–4

5. Annual mean biomass and the peak:mean ratio

1.16�g chl a l�1, 1.61 12.4�g chl a l�1, 2.95

6. Frequency of mixing to

> 0:5 m daily

> 2:5 m� daily

> 10 m� 200 days (Oct–May)

7. Maximum Shannon-Weaver diversity index,H00

(ignoring spp.< 0:5% of the biomass)

1.029 0.832

8. Equitability at maximum diversity

0.257 0.263

nightly intervals throughout the three-year study peri-od, from the open water at the deepest part of the lake,by means of a 5-m column sampling hose (Lund &

Talling, 1957). Chlorophyll was extracted from GF/C-filtration residues by the hot methanol method (Talling,1974). Phytoplankton were counted from appropriate

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volumes of lake water, fixed on collection with Lugol’sIodine, after concentration by sedimentation, either bythe method of Lund et al. (1958) or according to theWRc modification to Lund’s (1959) method (Young-man, 1971). All counts were expressed per unit volumeof the original sample.

Diversity of the assemblage collected in individu-al samplings were tested by the specialised ShannonWeaver function (Shannon, 1948):

H 00 = ��ni=N log2(ni=N)

whereni is the measure of theith species (as specificwet biomass calculated as the product of a cell-volumeapproximation and the number of cells counted; unfor-tunately, no direct measurements are available) andN

is� ni. The greater the number of species present in asample then the greater is the value ofH 00. The theo-retical maximum isH 00

max = log2 s ands is the numberof species in the sample with specific mass accountingfor > 0:5% of the total. The equitability (or evenness)of the species representation is given fromH 00=H 00

max.

Results

Biomass

The plot tracing the routine measurements of chloro-phyll concentrations through the three-year period,1991–1993 (Figure 1), shows, as was broadly pre-dicted, a significant increase in the size of the algalstanding crop, from being always< 2 �g chl a l�1

throughout the first year, to maximum levels of 9�gchl a l�1 in 1992 and to 36�g chl a l�1 in 1993. Thegreater variability through time should also be noted,as should the emergence of a typical seasonality of bio-mass in enriched lakes (low winter minima and shortperiods of low biomass in summer).

Species dominance in 1991

Some 35 taxa were recorded from the routine algalcounts in 1991. The largest number of these werereferrable to the Chrysophyta; several species ofgreen algae, the CryptophytesRhodomonas, Cryp-tomonasand dinoflagellates conforming toPeridiniuminconspicuumLemm. and toGymnodinium luteofa-ba Javornicky made up most of the rest. It is strik-ing that almost all are unicellular in habit or pro-duce only simple coenobia (Actinastrum, Quadrigula,Scenedesmus); Dinobryon sertulariaEhrenberg, a fil-

amentous green alga (Mougeotia), occasional encoun-ters with the diatom,Aulacoseira distansEhrenbergand with a coenobial cyanobacterium (Merismopedia)together represented the structurally more-complexalgae. Several genera of benthic diatom were also notedin the plankton from time to time. Such a list is rea-sonably congruous within the understanding of mildlyacidic, oligotrophic phytoplankton.

The species accounting for the largest proportionof the planktonic biomass were aChlorella (cf. C.ellipsoideaGerneck), which was present throughoutbut peaked at an estimated 1250 cells ml�1 in Mayand came back with about 2200 ml�1 in September,Chrysolykossp. (1100 cells ml�1 in March),Kephyrion(maximum: 85 ml�1 in April), Dinobryon sertularia(380 cells ml�1 in May) andMonochrysis(maximumc. 70 cells ml�1 in June). Larger algae likePeridiniumscarcely exceeded 500 l�1, although a maximum ofCryptomonascf. ovataEhrenberg (300 l�1) was notedin August.

Species dominance in 1992

The species composition of the Tarn phytoplanktonwas not substantially altered in 1992, even after thephosphorus additions were commenced in March. Atthat time, the dominant species comprisedChlorel-la (� 300 cells ml�1), Kephyrionand Monochrysis(each< 100 cells ml�1). The first effect of fertili-sation was that nearly everything increased in mass,with the strongest performance coming fromMono-chrysis (� 700 cells ml�1 by late April). With fur-ther fertilisation,Chlorella became dominant duringJune (reaching 7000 cells ml�1); later peaks wereoverwhelmingly dominated byChlorella (September:43 000 cells ml�1; October: 29 000 cells ml�1) whenCryptomonasspecies reached> 10 ml�1 for the firsttime. Chrysophytes persisted in similar numbers aspreviously, though the proportion of the biomass wasgreatly diminished.

Species dominance in 1993

The accelerated phosphorus addition in 1993 pre-dictably led to the much larger algal production andstanding crop.Monochrysis(reaching 7 500 cells ml�1

during March) again dominated initially but it wasChlorella, building to a remarkable 1.2 million cellsml�1 which contributed most to the mid-May biomassmaximum. This population abruptly declined duringJune, leaving the water relatively very clear. A sec-

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Figure 1. The seasonal variation in the concentration of chlorophylla in Seathwaite Tarn, 1991–1993. The annotations refer to the dominantspecies and their maximum abundance.

ond, though lesser, maximum then began to develop,comprising some 20 000Chlorella cells ml�1, withsubdominant Chrysophytes andCryptomonas.In bothcases, the rapid reduction in nanoplanktonic biomasscoincided with a phase of intense feeding and recruit-ment of Bosmina corregoniBaird. Interestingly, themicroplanktonicCryptomonas(cf. C. rostratiformisSkuja) continued to increase, eventually to dominatethe October chlorophyll maximumwith 300cells ml�1,before it declined to overwintering levels.

Discussion

The expected promotion of production of phytoplank-ton in response to phophorus additions has occurred,with populations broadly scaled to the phosphorusloads. There is no question that the supportive capac-ity of the lake was restricted by phosphorus and thereis no indication that the demand of the potential bio-mass was ever saturated in the experiments. In 1993, atleast, the biomass assembled matched well the phos-phorus made available to support it (see regression ofReynolds, 1992). The scale of the 1993 phosphorus-addition was also sufficient to promote the biologicaluptake of nitrate as intended, with the consequent ele-vation of pH.

The exercise was not billed as an experiment ineutrophication, though it is perfectly permissible tointerpret it in that way. It is also useful to reflect uponthe fact that the Tarn has not become beset with speciesof eutrophic lakes: any anticipation that the enrichedconditions might have led to the dominance by thediatoms, colonial green algae or even the cyanobac-teria common in the more enriched nearby waters ofthe English Lake District will, so far, have been quiteerroneous. Instead, the flora has continued to comprisemore or less the same algal species, albeit in alteredrelative proportions, but in much greater numbers.

That such little compositional change should besurprising at all perhaps says more about the shal-lowness of our understanding of pelagic systems thanour knowledge of the organisms. Intuition anticipatesspecies which are more or less efficient at obtainingnutrients, operate at higher or lower N:P ratios or usedifferentially the various sources of carbon. If theseare dimensions upon which substantial change couldhave occurred, are we sure that two growing seasons,spanning little more than one year, are sufficient tohave allowed other,potentially more successful speciesto have ‘arrived’ and established competing inocu-la, once the habitat was rendered supposedly moreamenable? We also note that enrichment has not madethe tarn unsuitable for any of its former planktonicplant species. Could it be that, since the lake is still

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acidic, it has not changed sufficiently for there to beany measurable change anyway? Both explanationshave some probability but, if so, both emphasise thatthe common association among phytoplankton speciesstructure and lake trophic status, as formalised by suchas Rodhe (1948), Rawson (1956) and Moss (1973), isnot a simple permutation of the nutrient content of thewater.

Our deduction is that the development of associ-ations of phytoplankton and the organisation of com-munities are influenced by many factors which act atdiffering scales and it takes time and a history of eventsto bring some degree of similarity (cosmopolitanism)among the species structures of chemically-similar butgeographically-isolated lakes. Merely raising the phos-phorus content may not by itself have overcome theconditions in Seathwaite Tarn which, hitherto, mayhave been perceived by such asAsterionella, Eudori-naor Anabaenaas being hostile (which could includeits temperature range or the suitability of the benthicrefuges). We suspect that the promotion of ‘more of thesame’ (Reynolds, 1992) and the relative distance fromother sites where eutrophic species are already well-established may well reflect the time that it takes forspecies to be transmitted from isolated lake to isolatedlake. Many cases have been documented in the Eng-lish Lake District (see Reynolds, 1998) where, duringenvironmental alteration of lakes through enrichment,the first occasion that species, supposedly suited to thenew conditions, have been noted in routine counts mayoccur 5–10 years later; this is very short against thescale of palaeolimnological investigations but never-theless finite and of interest to the prediction of changein water bodies.

References

Davison, W., 1987. Internal elemental cycles affecting the long-term alkalinity status of lakes: implication for lake restoration.Schweiz. Z. Hydrol. 49: 186–200.

Davison, W., D. G. George & N. J. A. Edwards, 1995. Controlledreversal of lake acidification by treatment with phosphate fertil-izer. Nature 377: 504–507.

Davison, W., C. S. Reynolds, E. Tipping & R. F. Needham, 1989.Reclamation of acid waters using sewage sludge. Envir. Poll. 57:251–274.

Lund, J. W. G., 1959. A simple counting chamber for nannoplankton.Limnol. Oceanogr. 4: 57–65.

Lund, J. W. G., C. Kipling & E. D. Le Cren, 1958. The invertedmicroscope method of estimating algal numbers and the statisticalbasis of estimations by counting. Hydrobiologia 11: 143–170.

Lund, J. W. G. & J. F. Talling, 1957. Botanical limnological methodswith special reference to the algae. Bot. Rev. 23: 489–583.

Moss, B., 1973. The influence of environmental factors on the dis-tribution of freshwater algae: an experimental study. IV. Growthof test species in natural lake waters and conclusion. J. Ecol. 61:193–211.

Rawson, D. S., 1956. Algal indicators of trophic lake types. Limnol.Oceanogr. 1: 18–25.

Reynolds, C. S., 1992. Eutrophication and the management of plank-tonic algae: what Vollenweider couldn’t tell us. In D. W. Sutcliffe& J. G. Jones (eds), Eutrophication; research and applicationto water supply. Freshwater Biological Association, Ambleside:4–29.

Reynolds, C. S., 1998. What factors influence the species com-position of phytoplankton in lakes of different trophic status?Hydrobiologia 369/370: 11–26.

Rodhe, W., 1948. Environmental requirements of freshwater plank-ton algae: experimental studies in the ecology of phytoplankton.Symb. bot. Upsaliensis 10: 5–149.

Shannon, C. E., 1948. A mathematical theory of communication.Bell Syst.tech. J. 27: 623–656.

Talling, J. F., 1974. General outline of spectrophotometric methods.In R. A. Vollenweider (ed.), A manual on methods for measuringprimary production in aquatic environments. Blackell ScientificPublications, Oxford: 22–25.

Talling, J. F. & D. Driver, 1963. Some problems in the estimationof chlorophyll-a in phytoplankton. In U.S. Atomic Energy Com-mission (ed.), Proceedings, Conference on primary productivitymeasurements, marine and freshwater, Hawaii, 1961. USEAC,Washington: 142–146.

Youngman, R. E., 1971. Algal monitoring of water supply reservoirsand rivers. Tech. Memo. Wat. Res. Ass. 63: 1–26.

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