Hydrobiologia 446/447: 29–34, 2001.L. Sanoamuang, H. Segers, R.J. Shiel & R.D. Gulati (eds), Rotifera IX.© 2001 Kluwer Academic Publishers. Printed in the Netherlands.

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The relationship between Trichocerca pusilla (Jennings), Aulacoseira spp.and water temperature in Loch Leven, Scotland, U.K.

Linda May, A.E. Bailey-Watts & A. KirikaCentre for Ecology and Hydrology, Edinburgh Research Station, Bush Estate, Penicuik,Midlothian EH26 0QB, Scotland, U.K.E-mail: lmay@ceh.ac.uk

Key words: Trichocerca pusilla, rotifer, Aulacoseira, diatom, grazing, silica, water temperature, Loch Leven

Abstract

Loch Leven is a shallow, eutrophic lake in the Scottish lowlands that is famous for its brown trout (Salmo truttaL.) fishery. Studies of planktonic rotifer populations began here in January 1977. Since then, samples have beencollected and analysed at more or less weekly intervals. Additional information on the composition and abundanceof phytoplankton and crustacean zooplankton species, and on a variety of physical and chemical determinants, hasbeen recorded on each sampling occasion.

Long-term datasets, such as that described above, are invaluable for identifying interactions between compon-ents of the plankton that only appear for short periods each year, as these interactions would probably be overlookedin data spanning a shorter period of time. This study uses the long-term data from Loch Leven to examine the foodand temperature requirements of the summer rotifer species Trichocerca pusilla (Lauterborn). The results suggestthat T. pusilla prefers water temperatures above 12 ◦C and that it feeds, primarily, on the filamentous diatomAulacoseira spp. During the summer months, its abundance was closely related to the availability of this diatom.When filaments of Aulacoseira spp. were abundant, rotifer densities reached 1000–3000 ind. l−1 and when theywere scarce (e.g. 1980, 1997 and 1998) T. pusilla densities also remained low (i.e. less than 100 ind. l−1). Thereason for the success or failure of Aulacoseira during the summer months each year is unclear but, in general, itsabundance was related to the availability of dissolved silica in the water.

Introduction

Rotifers are an important and numerically abundantcomponent of the plankton of most freshwater lakes,but relatively little is known about the ecology of in-dividual species in the natural environment. This isparticularly true of seasonal species that appear in theplankton for very short periods each year. This com-bined with the relatively long sampling intervals usedin many studies (e.g. 1 month or more) means thatvery little data on such species are collected in studieslasting only a year or two.

The plankton of Loch Leven has been routinelymonitored at weekly or fortnightly intervals since1968, and rotifer studies began here in January 1977.This has provided a long series of data for zooplank-ton, algae and water chemistry that can be examinedfor trends, especially among seasonal species. This pa-

per summarises long-term data and other observationsfrom Loch Leven that contribute to our understandingof the ecology of Trichocerca pusilla (Lauternborn).As the long-term data are incomplete between January1983 and December 1994 (due to a lack of funding forthe analysis of samples collected), this study reportsdata for 1977–1982 and 1994–1998, only.

Site description

Loch Leven (56◦ 12′ N, 3◦ 22′ W) is a shallow lakein lowland Scotland that lies in a morainic basin overOld Red Sandstone. It has a surface area of 13.3km2, and mean and maximum depths of 3.9 m and25.5 m, respectively. The loch is eutrophic due toa relatively high phosphorus load (≈9 tonnes yr−1)from the catchment. This arises from nutrient laden

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inflows draining a mainly agricultural landscape, andphosphorus-rich discharges from local sewage worksand an industrial source. This, combined with the shal-lowness of the site and an average retention time ofabout 5.2 months (Smith, 1974) makes the loch veryprone to algal blooms. As phytoplankton crops hereare generally phosphorus (P) limited, efforts have beenmade to reduce the P load from the catchment first bytargeting point sources and, more latterly, by target-ing diffuse sources (LLCMP, 1999). The overall effectof these measures has been to reduce the P-load fromabout 20 tonnes per year (1985) to about 8.5 tonnes peryear (1995). In addition, annual stocking with rainbowtrout to improve the sport fishery began in 1993.

Methods

Plankton and water chemistry samples have been col-lected from Loch Leven at more or less weekly inter-vals since January 1977, with little change in samplingprocedures. If weather conditions were good, sampleswere usually collected by boat at the Reed Bower site(Fig. 1) with a weighted polythene tube (Lund, 1949).This provided an integrated water sample over the en-tire water column, from the surface to 0.25 m abovethe sediment. This was usually to a depth of 3–3.5 m.However, during adverse weather conditions (strongwinds, ice cover, etc.), samples were collected fromthe shore by dipping a 10 l bucket into deep waterclose to outflow (Site SL, Fig. 1). Long-term recordshave shown that, because Loch Leven is well-mixed,the abundances of small planktonic organisms (suchas algae and rotifers) and the water chemistry at thesetwo sites are usually very similar at any given time(May, 1980). Surface water temperature was recordedon each sampling occasion.

The raw water samples were mixed well and sub-sampled for the analyses of water chemistry (250 ml),algal abundance (250 ml) and rotifer numbers (1 lor 500 ml). Dissolved silica analyses were carriedout in accordance with the methods given by Gol-terman et al. (1978). Algal samples were preservedin Lugol’s iodine, concentrated by sedimentation ina 250 ml glass measuring cylinder and counted un-der the microscope in a calibrated glass nannoplank-ton chamber (Lund, 1959, 1962; Youngman, 1971).Counts of Aulacoseira spp. filaments were convertedto an estimate of biomass using a conversion factor of7000 µm3 for per filament. This average value wasbased on the measured linear dimensions of these al-

gae in Loch Leven, approximating each filament to asimple cylindrical shape. Rotifer samples were nar-cotised by adding sufficient procaine hydrochloride(NH2.C6H4.COO.CH2.CH2.N(C2H5)2.HCl) to give afinal concentration of 0.2 g l−1 (May, 1985). Thesamples were then preserved in 4% formalin, concen-trated using a sedimentation technique, sub-sampledand counted under ×100 magnification in the count-ing chamber of a Wild� inverted microscope. Severalsub-samples, each 3 ml in volume, were examined un-til at least 200 rotifers had been recorded from eachsample. Species identifications were carried out onlive specimens in accordance with Koste (1978).

Data on the hatching of T. pusilla from lake sedi-ments collected in winter when incubated at 5 ◦C, 15◦C and 20 ◦C are also presented. The methods for,and further details of, this experiment are describedin detail by May (1987).

Results

Surface water temperature in Loch Leven ranged from0.15 ◦C (on 29 December 1981) to 21.4 ◦C (on 11 July1977) over the period of study (Fig. 2, upper panel).Although temperatures regularly fell below 1 ◦C forshort periods each winter, summer maxima above 20◦C were less common. These only occurred in 1977,1982, 1995 and 1997. The coolest summer was 1978when the highest water temperature recorded was only16.7 ◦C. In general, however, seasonal increases anddecreases in water temperature followed a smooth andregular pattern each year, with the warmest period(>10 ◦C) occurring from the beginning of May to theend of October.

T. pusilla was recorded in Loch Leven during thesummer months only (Fig. 2, lower panel), and itsability to achieve high population densities seemed tobe related to water temperature (Fig. 3). Abundancerarely exceeded 100 ind. l−1 when water temperat-ures were below 12 ◦C, except occasionally in autumnwhen the summer population was declining graduallyas water temperatures began to fall, e.g. October 1981and October 1994. However, at higher water tem-peratures, the species could become very abundant.Figure 3 indicates the range of values recorded in LochLeven over the study period. The data suggest an upperboundary on abundance that is related to water temper-ature and below which lower values probably reflectother constraints on population growth – such as foodlimitation.

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Figure 1. Map of Loch Leven showing the Reed Bower (RB) and Sluices (SL) sampling sites. Inset shows the location of the loch in GreatBritain.

Figure 2. Surface water temperature (upper panel) and abundanceof Trichocerca pusilla (lower panel) in Loch Leven, 1977–1982 and1994–1998.

Although neither resting eggs nor males were everobserved in either the water or sediment samples ex-amined, the apparent absence of T. pusilla from theplankton for most of the year suggested that thisspecies probably ‘overwintered’ in the sediments asresting eggs. Indirect evidence of the existence of suchresting eggs in the sediments during the winter was

Figure 3. Abundance of Trichocerca pusilla in relation to wa-ter temperature in Loch Leven, 1977–1982 and 1994–1998. Greycircles indicate samples collected during low temperatures in au-tumn (see text for details).

also provided by a sediment incubation experimentcarried out in February 1984 and described in fullby May (1987). In this experiment, T. pusilla indi-viduals emerged from these ‘winter’ sediments whenthey were incubated at ‘summer’ temperatures (Fig.

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Figure 4. Cumulative emergence of Trichocerca pusilla from lochsediments incubated at different temperatures in the laboratory.

4). Hatching success was markedly greater at 15 ◦Cthan at 10 ◦C, and no hatching was recorded at 5 ◦C.

The abundance of T. pusilla varied from year toyear. The study-period maximum (2860 ind. l−1) wasrecorded on 30 July 1979 (Fig. 2). However, most an-nual maxima were between 1000 ind. l−1 and 1500ind. l−1. Only in 1980 and from 1996 to 1998 werethese values especially low (max. <100 ind. l−1). Thelow population maximum recorded in 1980 appearedto be an isolated event, rather than part of a long termtrend, as it was followed by population maxima of1590 ind. l−1 in 1981, and two similar peaks in abund-ance of about 1440 ind. l−1 in 1982. The most likelyexplanation for this was food limitation (see below).However, from 1994 onwards, a more progressive,long-term decline in the annual population maxima ofthis species was recorded, culminating in its apparentdisappearance from the loch in 1998 (Fig. 2).

During the examination of live plankton samples,individuals of T. pusilla were often observed feed-ing on filamentous algae by piercing the cell wallsand sucking out their contents. Adult females werealso seen depositing their eggs on these filaments.These observations suggested that T. pusilla both fedon, and attached its eggs to, filamentous algae inthe loch. As the dominant filamentous algae in theloch when T. pusilla was abundant were Aulacoseiraspp., and T. pusilla eggs had been seen attached tothese filaments during the examination of the pre-served samples, the monitoring data were examinedfor evidence of interactions between these species.

Comparison of the population dynamics of Tri-chocerca and Aulacoseira spp. suggested that theirabundances were closely linked (Fig. 5). T. pusilla

tended to achieve much higher population densities inyears when the biomass of Aulacoseira in July/Augustwas high (e.g. 1977, 1978, 1979, 1994) than in yearswhen there was no significant summer population ofAulacoseira (e.g. 1980, 1997 and 1998). However, thisrelationship did not hold for 1996, when Aulacoseirawas very abundant in July/August but rotifer numbersremained low, or in 1982 when T. pusilla abundancewas higher than might have been expected given therelatively low abundance of Aulacoseira during thisperiod. The reasons for these apparent deviations fromthe more usual patterns of abundance are unclear.

It has been shown that diatom abundance in LochLeven tends to be closely related to the availabil-ity of dissolved silica (Bailey-Watts & Lund, 1973;Bailey-Watts, 1976a,b). This relationship is illustratedfor Aulacoseira abundance in Figure 6, which clearlyshows that it declined rapidly once the supply of dis-solved silica had become limiting and open waterconcentrations were on the decline (Fig. 6). Figure6 also shows that, in general, the annual maxima ofAulacoseira tended to increase over the study period.However, it should be noted in relation to this studythat these were spring maxima that occurred outsidethe rotifer’s preferred temperature range.

Discussion

There is very little information in the literature on theecology of Trichocerca spp., and even less concerningthat of planktonic forms such as T. pusilla. Pourriot(1970), for example, restricts his detailed study toseven species collected from among the periphytonof shallow pools. The results from Loch Leven sug-gest that Trichocerca pusilla is a summer species,preferring water temperatures higher than 11–12 ◦Cbut occasionally found at lower temperatures. Theseobservations agree with those of Carlin (1943) andBerzinš & Pejler (1989).

Jennings (1903) suggested that the main foodof Trichocerca spp. was probably small, suspendedparticles in the water or flocculant material on thesurface of aquatic plants. However, De Beauchamp(1909) recognised that their virgate trophi were prob-ably adapted to seizing and piercing algal cells, andsucking out their contents. The results of Pourriot(1970), who successfully cultured seven species ofTrichocerca (not including T. pusilla) on filamentousalgae, and the observations from Loch Leven alsosupport this hypothesis.

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Figure 5. The relationship between Aulacoseira spp. biomass and Trichocerca pusilla abundance in summer, 1977–1982 and 1994–1998.Periods when the temperature was ≥ 12 ◦C are indicated by the thick bars along the horizontal axes.

Figure 6. The relationship between dissolved silica concentrations and Aulacoseira spp. biomass, 1977–1982 and 1994–1998.

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The literature also suggests that, in general, plank-tonic Trichocerca species attach their eggs to otherrotifers, especially Brachionus angularis (Ruttner-Kolisko, 1974; Koste, 1976). This does not seem to bethe case in Loch Leven where B. angularis was rarelyrecorded. Here, eggs were frequently seen attached tofilaments of Aulacoseira spp., and other filamentousalgae, but not to other rotifers. There is little informa-tion on the sexual periods or resting eggs of T. pusillain the literature (Ruttner-Kolisko, 1974). However,evidence from Loch Leven suggests that, like manyother rotifer species, T. pusilla survives as resting eggsin the sediments during unfavourable conditions.

T. pusilla is also predated upon by Cyclopsabyssorum (Sars) in Loch Leven. Rutkowski (1980)found the remains of this rotifer among the gut con-tents of copepodite stages 3 to adult during her studyof plankton samples from Loch Leven in 1978. How-ever, recognisable remains were found in <2% of theguts examined, suggesting that losses due to predationfrom Cyclops are low. In addition,C. abyssorum feedsheavily on Aulacoseira filaments (Rutkowski, 1980).Some of the filaments grazed by Cyclops will prob-ably have Trichocerca eggs attached, thus exertingsome indirect predation on the rotifer population. Asboth Trichocerca and Cyclops feed on Aulacoseira fil-aments, there will also be some effects of competitionfor food between these species.

The reason for the general decline in T. pusillaabundance from 1994 onwards seemed to be, at leastpartly, related to changes in the timing and abund-ance of Aulacoseira populations. The reason for thesechanges in Aulacoseira abundance is unclear, but itmay be related to recent changes in the managementof the loch and its catchment.

Acknowledgements

This work was funded by the Natural EnvironmentResearch Council and Scottish Natural Heritage.

References

Bailey-Watts, A. E. & J. W. G. Lund, 1973. Observations on adiatom bloom in Loch Leven, Scotland. Biol. J. linn. Soc. 5:235–253.

Bailey-Watts, A. E., 1976a. Planktonic diatoms and silica in LochLeven, Scotland: a one month silica budget. Freshwat. Biol. 6:203–213.

Bailey-Watts, A. E., 1976b. Planktonic diatoms and some diatom-silica relations in a shallow eutrophic Scottish loch. Freshwat.Biol. 6: 69–80.

De Beauchamp, P., 1909. Recherches sur les Rotifères: les forma-tions tégumentaires at l’appareil digestif. Arch. Zool. exp. gJn.10: 1–410.

Berzinš, B. & B. Pejler, 1989. Rotifer occurrence in relation totemperature. Hydrobiologia 175: 223–231.

Carlin, B., 1943. Die Planktonrotatorien des Motalaström: zurtaxonomie und Ökologie der Planktonrotatorien. Medd. LundsUniv. limnol. Inst. 5: 1–255.

Golterman, H. L., R. S. Clymo & M. A. M. Olmstad, 1978. Methodsfor the Physical and Chemical Analysis of Freshwaters. 2nd edn.Publ. Blackwell, Oxford.

Jennings, H. S., 1903. Rotatoria of the United States. II. A mono-graph of the Rattulidae. Bull. U.S. Fish Comm.: 273–352.

Koste, W., 1976. Rotatoria: Die Rädertiere Mitteleuropas. Publ.Gebrhder Borntraeger, Berlin: 673 pp.

LLCMP (Loch Leven Catchment Management Project), 1999. TheLoch Leven Catchment Management Plan: 93 pp.

Lund, J. W. G., 1949. Studies on Asterionella I. The origin andnature of the cells producing seasonal maxima. J. Ecol. 37:389–419.

Lund, J. W. G., 1959. A simple counting chamber for nannoplank-ton. Limnol. Oceanogr. 4: 5–75.

Lund, J. W. G., 1962. Concerning a counting chamber for nanno-plankton described previously. Limnol. Oceanogr. 7: 261–262.

May, L., 1980. Ecology of planktonic rotifers at Loch Leven,Kinross-shire. Ph.D Thesis, Paisley College of Technology: 180pp.

May, L., 1983. Rotifer occurrence in relation to water temperaturein Loch Leven, Scotland. Hydrobiologia 104: 311–315.

May, L., 1985. The use of procaine hydrochloride in the preparationof rotifer samples for counting. Verh. int. Ver. Limnol. 22: 2987–2990.

May, L., 1987. Effect of incubation temperature on the hatching ofresting eggs collected from sediments. Hydrobiologia 147: 335–338.

Pourriot, R., 1970. Quelques Trichocerca (Rotifères) et leurs régimealimentaires. Ann. Hydrobiol. 1: 155–171.

Rutkowski, E. W., 1980. Studies on the feeding of Cyclopsabyssorum Sars in Loch Leven, Kinross-shire, Scotland. MSc.Thesis, University of Stirling: 126 pp., 4 Appendices.

Ruttner-Kolisko, A., 1974. Plankton Rotifers: biology and Tax-onomy. Die Binnengewässer, volume 26, supplement. Publ.Gebrüder Ranz, Dietenkeim: 146 pp.

Smith, I. R., 1974. The structure and physical environment of LochLeven, Scotland. Proc. r. Soc. Edinb. (B) 74: 81–100.

Youngman, R. E., 1971. Algal monitoring of water supply reser-voirs and rivers. Water Research Association TM63. The WaterResearch Association, Medmenham.