Effects of Nutrients, Fish, Charophytes and Algal Sediment Recruitment on the Phytoplankton Ecology of a Shallow Lake

© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim 1434-2944/07/612-626

MARÍA-JOSÉ VILLENA and SUSANA ROMO*

Área de Ecología. Facultad de Biología. Campus de Burjasot. 46100-Burjasot. Valencia. Spain; e-mails: [email protected], [email protected].

Effects of Nutrients, Fish, Charophytes and Algal SedimentRecruitment on the Phytoplankton Ecology of a Shallow Lake

key words: turbid phase, fertilization, cyanobacteria, algae recruitment, macrophytes, planktivorous fish

Abstract

The influence of nutrient levels, fish density and charophytes on the phytoplankton ecology of a shal-low Mediterranean lake was studied by means of an in situ mesocosm experiment. Different levels ofnutrients and fish were added over the course of an eight-week experiment, during which charophyteswere removed towards the end. After submerged plants were removed, phytoplankton biomass increasedsignificantly in all the mesocosms, with a reduction of algal diversity and species richness and domi-nance of cyanobacteria. Cyanobacteria recruited from the sediment played an important role in sustain-ing planktonic populations of the dominant species. Oscillatorial species (Pseudanabaena galeata,Planktolyngbya limnetica) dominated at higher nutrient levels (0.5–1 mg L–1 P and 5–10 mg L–1 N) andchroococcal cyanobacteria (Merismopedia tenuissima) at lower nutrient levels. Density of planktivorousfish had little effect on the algal recruitment from the sediment and phytoplankton biomass and diver-sity.

1. Introduction

Nutrient level is a key factor regulating competition between macrophytes and phyto-plankton and the underwater light climate (KAIRESALO, 1984; CATTANEO et al., 1998; VAN

DONK et al., 1993; STEVENSON et al., 1996; MOSS et al., 1996; JEPPESEN et al., 1998a, KUFEL

and KUFEL, 2002). The bistability hypothesis for shallow temperate lakes postulates that atintermediate nutrient concentrations alternative dominance of submerged macrophyte orphytoplankton is possible, otherwise extreme ranges of nutrients will stabilize one of thesestates (SCHEFFER et al., 1993). The ecology of phytoplankton can be affected by the pres-ence of submerged plants in a number of ways apart from plant nutrient competition (CARIG-NAN, 1982; RATTRAY et al., 1991), as well as competition from their associated epiphytes(BRÖNMARK and VERMAAT, 1998; JONES et al., 1998). Moreover, plants can act as a sub-stratum and refuge for plant-associated invertebrates, zooplankton and small fishes, whichcan increase predation on phytoplankton (TIMMS and MOSS, 1984; BRÖNMARK and WEISNER,1992; LAURIDSEN et al., 1996; JEPPESEN et al., 1998b). Charophyte beds in particular canenhance water transparency by reducing sediment resuspension and bioturbation by fish,especially when compared with other macrophytes (VAN DEN BERG et al., 1998; MEIJER,2000; VAN DONK and VAN DE BUND, 2002). Water stagnancy within charophyte beds induceshigh rates of phytoplankton sedimentation (VAN DEN BERG et al., 1998; CASANOVA et al.,2002), selecting algal size and composition (BALLS et al., 1989; JAMES and BARKO, 1994;

Internat. Rev. Hydrobiol. 92 2007 6 626–639

DOI: 10.1002/iroh.200610906

* Corresponding author

SØNDERGAARD and MOSS, 1998). A relationship has been observed between presence ofcharophytes and lower chlorophyll a concentrations and higher transparency in some shal-low lakes (BLINDOW et al., 2002; TAKAMURA et al., 2003). Additionally, allelopathy of charo-phytes can influence phytoplankton ecology and the whole food web (WIUM-ANDERSEN

et al., 1982; JASSER, 1995; GROSS, 2003; MULDERIJ et al., 2003).MUYLAERT et al. (2003) found that macrophyte presence and water transparency were

more closely related to the fish community than to nutrient levels in several shallow Bel-gian lakes. The effects that fish exert on phytoplankton have been widely studied in tem-perate lakes (see review, DRENNER and HAMBRIGHT, 2002); however, these effects are lesswell known for shallow tropical, subtropical and Mediterranean lakes (FERNANDO, 1994;BLANCO et al., 2003; LAZZARO et al., 2003; GYLLSTRÖM et al., 2005; BEKLIOGLU et al., 2007).The dominance of small-bodied zooplankton species (GILLOOLY and DODSON, 2000; JEPPE-SEN et al., 2005; GYLLSTRÖM et al., 2005) and higher fish densities within submerged macro-phyte beds (MEERHOFF et al., 2006) can reduce effective top-down control over phytoplank-ton in these ecosystems, making interactions between phytoplankton, aquatic plants andpredators more complex. The relevance of top-down and bottom-up mechanisms on the ecol-ogy of shallow lakes is also dependent on lake features and climate (BENNDORF et al., 2002;HARGEBY et al., 2004; MOSS et al., 2004; NORLIN et al., 2005; BEKLIOGLU et al., 2007).

The absence of submerged plants in shallow waters can boost the recruitment of algaefrom the sediment, especially that of cyanobacteria (HANSSON et al., 1994; HANSSON,1996a, b; SCHWEIZER, 1997; WILLÉN and MATTSSON, 1997; STÅHL-DELBANCO et al., 2003;VERSPAGEN et al., 2005). The recruitment of cyanobacterial resting stages from the sedimentsurface can play an important role as inocula and help develop epilimnic populations; how-ever, there are few reports on how this recruitment is regulated by nutrients and zooplank-ton grazing (HANSSON, 1996a, b; STÅHL-DELBANCO et al., 2003). In general, studies on algalrecruitment have focussed on some frequent bloom-forming cyanobacteria, some of whichproduce cyanotoxins, such as Microcystis (WILLÉN and MATTSSON, 1997; STÅHL-DELBANCO

et al., 2003; VERSPAGEN et al., 2005). Cyanobacteria are more frequently dominant in shal-low tropical, subtropical and Mediterranean lakes (HUSZAR et al., 1998; SCASSO et al., 2001;VILLENA and ROMO, 2003). The abundance of cyanobacteria in shallow temperate lakes hasbeen related to factors like eutrophication, reduced zooplankton grazing and oligophotic con-ditions (REYNOLDS, 1997; SCHEFFER, 1998); meanwhile, the key factors in warmer shallowlakes are being revised (OSBORNE, 2005; BEKLIOGLU et al., 2007).

This paper reports on an experimental mesocosm study conducted to determine the effectsof nutrients, planktivorous fish density and absence of charophytes on the biomass, compo-sition and diversity of phytoplankton in a shallow Mediterranean lake. The study also inves-tigated how algal recruitment from the sediment is affected by nutrient levels and fish den-sities, as well as how resting stages on the sediment surface can influence phytoplanktonpopulations and composition in the water phase.

2. Material and Methods

2.1. Study Site

The mesocosm experiment was carried out in a shallow, 0.5 ha freshwater lake (Lake Xeresa) locat-ed in the wetland of Xeresa, 65 km south of Valencia on the Spanish Mediterranean coast (39°06′ N,0°12′ W). The lake is mainly fed by groundwater and rainfall. Minimum water levels occur during sum-mer due to evaporation and water withdrawal for agriculture. Maximum depths are reached duringautumn-winter as a result of short, but intense rainfalls. During the experiment in summer of 1998, waterdepth gradually fell in the lake and mesocosms from 80 to 58 cm. The lake was completely covered bysubmerged macrophytes, mainly Chara hispida, but also Ch. vulgaris var. vulgaris and Ch. aspera andthe shores were surrounded by a belt of Phragmites australis.

Phytoplankton Ecology of a Shallow Lake 627

© 2007 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.revhydro.com

2.2. Enclosure Experiments

The mesocosm experiment was carried out over nine weeks (8 June to 6 August), including a weekof pre-treatment to establish the initial conditions. Different amounts of nutrients and fish were addedfor eight weeks and charophytes were removed in the last three weeks of this period. Additionally andsimultaneously to sample collection from the mesocosms, samples were also analysed from the openlake (one sampling point nearby the enclosures) throughout the study. The open lake was untreated andsubmerged macrophytes remained present in the lake during the study.

Thirty-six mesocosms were made from polyethylene film (125 µm wall thickness) supported at thetop and bottom by circular plastic hoops, measuring 1 m in diameter. The bottom hoops were buried inthe sediment of the lake, leaving the polyethylene cylinders open to the atmosphere and to the lake bot-tom and its plant community. The top hoops of the mesocosms were supported by a wooden frame andplastic tubing. Experimental design was according to an international mesocosm protocol to study foodwebs on shallow lakes (see STEPHEN et al., 2004).

Three fish-density treatments (0, 4 and 20 g fresh mass m–2) and four nutrient-loading treatments (N-P in mg L–1: 0–0, 1–0.1, 5–0.5 and 10–1) were applied and each treatment was replicated three times.Treatments were randomized in a block design. Nutrient loadings were designated N0 (unfertilized) toN3 and fish densities F0 to F2. Nutrient solutions were added as mixtures of sodium nitrate and potas-sium dihydrogen phosphate at weekly intervals. Adjustments were made in the amounts added toaccount for drops in water level. Before fish and nutrient additions, fishes enclosed in the mesocosmswere removed by means of electrofishing. The mosquitofish, Gambusia holbrooki, was the species usedin the experiment, which is an ovoviviparous visual predator on zooplankton, widely distributed in thelake, as well as in other shallow Spanish lakes (BLANCO et al., 2003). Only male fish were stocked toavoid changes in density due to the presence of gravid females. During the experiment, the enclosureswere visually checked twice a week and dead fish were replaced, though need for replacement was infre-quent after the first week.

Chemical and phytoplankton samples were taken weekly from the mesocosms and the open lake dur-ing the experimental period. Samples were taken with a tube sampler integrating the water column andabove submerged macrophytes when plants were present. The chemical variables measured were totalphosphorus, orthophosphate, nitrate, ammonium and total suspended solids, following the StandardMethods (APHA, 1992). Chlorophyll a was extracted from filters (GF/F) into 90% ethanol in a 75 °Cwater bath for 5 minutes and measured spectrophotometrically (APHA, 1992). Phytoplankton sampleswere preserved with Lugol’s solution for later identification and counting, and biovolume calculatedaccording to ROTT (1981) and WETZEL and LIKENS (1991). Species richness was calculated as numberof taxa per sample. The Shannon-Wiener diversity index based on the species abundance was deter-mined according to SHANNON and WEAVER (1963). The Greatest Axial or Linear Dimension (GALD,REYNOLDS, 1984) was measured for at least 25 individuals or colonies, and algae sorted into GALDlarger or smaller than 50 µm. Three samples of macrophytes were randomly taken in each enclosureand the open lake, and after removing periphyton submerged plants were dried and weighed. Resultson zooplankton and top-down interactions during the experiment are reported in ROMO et al. (2004).

2.3. Algal Recruitment

Algal traps were set in the unfertilized (N0) and the highest nutrient level (N3) mesocosms in com-bination with the highest and lowest fish densities (F0 and F2), during the macrophyte-free period, toevaluate algal recruitment from the sediment. The traps consisted of a plastic funnel, face down, attachedto a glass bottle. The openings were covered with a mesh size of 400 µm to prevent large particles andpredators entering the traps. Later analysis of the samples under the microscope showed that this mea-sure had effectively prevented macrozooplankton from entering the traps. Before lowering the traps,they were filled with filtered lake water to minimize the risk of trapping organisms from the water col-umn on lowering. Traps were placed on the sediment surface in the enclosures and left for approxi-mately 3 days (66 h). Thereafter they were removed and the content of the traps was preserved withLugol’s solution for later determination of algal composition and abundance. Further details on the algalrecruitment method are given elsewhere (HANSSON, 1996a; STÅHL-DELBANCO et al., 2003).

628 M.-J. VILLENA and S. ROMO


2.4. Statistical Methods

A one-way analysis of variance (ANOVA) was used to test homogeneity between mesocosms in thepre-treatment week. The effect of treatments (nutrients and fish) were analysed by an ANOVA test andwhere significant differences were found a Tukey’s test was used to illuminate specific differencesbetween treatments. A Student’s paired t-test was used to compare weekly data from the open lake anduntreated mesocosms and to carry out comparative analyses between the plant and plant-free periods.Time-weighted averages were calculated from time data series corresponding to the presence andabsence of macrophytes. Data were log-transformed when necessary for statistical normality or other-wise analysed by Kruskal-Wallis’s or Wilcoxon’s test. Daily recruitment from the sediment surface ofa specific phytoplankton species in a certain week (t) was correlated with its population numbers in thewater column in the following week (t + 1), using a Pearson’s correlation test.

3. Results

3.1. Lake and Untreated Mesocosms

There were no significant differences for phytoplankton and submerged plant biomassesbetween the mesocosms in the pre-treatment week (P > 0.05). Low nutrient levels were ini-tially observed together with diversified phytoplankton composition, mainly composed byfilamentous cyanobacteria (including N2-fixing species) and flagellate algae (Table 1).

No significant differences were found between the open lake and the untreated mesocosmsduring the presence of submerged macrophytes, although total phosphorus and chlorophyll awere slightly higher in the untreated mesocosms (Table 2, Fig. 1). Phytoplankton composi-



Table 1. Initial limnological lake conditions (pre-treatment week).

Total phosphorus (mg L–1) 0.017Orthophosphate (mg L–1) 0.001Nitrate (mg L–1) 0.001Ammonium (mg L–1) 0.027DIN (mg L–1) 0.028Total Suspended Solids (mg L–1) 8.1Chlorophyll a (µg L–1) 3.4Macrophyte (g dry mass per sample) 8.6GALD biovolume < 50 µm 0.3GALD biovolume > 50 µm 0.5Algal diversity (bits individuals–1) 3.5Species richness (taxa per sample) 29Phytoplankton biovolume (mm3 L–1) 0.8

Algal groups biovolume (%)Cyanobacteria 37Chlorophyceae 29Dinophyceae 20Cryptophyceae 7

Dominant species biovolume (%)Cylindrospermum cf. muscicola 27Peridinium umbonatum 20Mougeotia sp. 19Pseudanabaena galeata 5Cryptomonas erosa 5

tion was also similar, the only difference being that there was a greater presence of smallcyanobacteria and chlorophytes in the untreated mesocosms (Table 2, Fig. 1). Filamentouscyanobacteria predominated (mainly Cylindrospermun cf. muscicola and Pseudanabaenagaleata with 52–30% and 8–7% of the total biovolume, respectively), together with somecryptophytes (Cryptomonas erosa 6–13%), dinophytes (Peridinium umbonatum 5–14%) anda pool of chlorophytes (16–19%) (Fig. 1).

Macrophyte removal in the untreated mesocosms caused a significant increase in ammo-nium concentrations and chlorophyll a, with an increase in Merismopedia tenuissima (40%of total biovolume) and chlorophytes (30% of total biovolume), and a significant decreasein diversity and species richness as compared to the open lake (Table 2). Other algae speciesalso increased during the plant-free period at N0 (Chroococcus spp., Scenedesmus ecornisand Rhodomonas minuta), while some larger ones, such as Mougeotia sp., Peridinium um-



Table 2. Limnological data for the open lake and untreated mesocosms (N0) when arecompared in presence and absence of submerged plants in the mesocosms. P = Probabilities:* P < 0.05, ** P < 0.01, *** P < 0.001, n.s. = not significant. Arrows indicate a positive (↑)

or negative (↓) response to the treatments.

Presence of plants Absence of plants

Lake N0 P Lake (1) N0 P

Total phosphorus (mg L–1) 0.015 0.024 ** ↑ 0.012 0.025 * ↑Orthophosphate (mg L–1) 0.004 0.002 n.s 0.002 0.003 n.s.Nitrate (mg L–1) 0.0008 0.0008 n.s 0.0006 0.010 n.s.Ammonium (mg L–1) 0.05 0.09 n.s 0.02 0.6 ** ↑DIN (mg L–1) 0.05 0.09 n.s 0.02 0.6 ** ↑Total Suspended Solids (mg L–1) 12 10.8 n.s 2 6.8 n.s.Chlorophyll a (µg L–1) 2.7 5.6 * ↑ 3 8.5 * ↑Phytoplankton biovolume (mm3 L–1) 0.66 0.81 n.s 0.35 1.93 n.s.

Total Cyanobacteria 0.43 0.44 n.s 0.13 1.43 n.s.Filamentous Cyanobacteria 0.43 0.40 n.s 0.12 0.07 n.s.Chroococcal Cyanobacteria 0.01 0.04 ** ↑ 0.01 1.36 n.s.

Chlorophyceae 0.11 0.14 n.s 0.11 0.33 n.s.Cryptophyceae 0.04 0.09 n.s 0.07 0.10 n.s.Bacillarophyceae 0.05 0.04 n.s 0.02 0.03 n.s.Dinophyceae 0.03 0.08 * ↑ 0.02 0.03 n.s.Euglenophyceae 0 0.02 * ↑ 0.01 0.01 n.s.

Phytoplankton abundance (ind mL–1) 872 2600 ** ↑ 1360 8710 ** ↑Total Cyanobacteria 590 787 n.s 484 3030 n.s.

Filamentous Cyanobacteria 585 669 n.s 441 176 n.s.Chroococcal Cyanobacteria 5 118 ** ↑ 42 2854 n.s.

Chlorophyceae 184 1634 * ↑ 766 5437 * ↑Cryptophyceae 35 87 n.s 60 167 n.s.Bacillarophyceae 45 40 n.s 40 60 n.s.Dinophyceae 19 48 * ↑ 10 15 n.s.Euglenophyceae 0 5 n.s 0 1 n.s.

GALD biovolume < 50 µm 0.15 0.37 *** ↑ 0.18 1.85 n.s.GALD biovolume > 50 µm 0.51 0.44 n.s 0.17 0.08 n.s.Shannon-Wiener diversity 2.84 2.58 n.s 3.41 2.44 * ↓

(bits individuals–1)Species richness (taxa per sample) 21 18 n.s 25 18 * ↓(1) Lake with plants

bonatum and Euglena sp. significantly decreased. In the lake, phytoplankton chlorophyll aand total biovolume remained similar with scarce changes in species composition (Ps. galea-ta, Geitlerinema sp. and Cy. cf. muscicola, chlorophytes and cryptophytes, 33%, 31% and19% of total biovolume, respectively) (Table 2, Fig. 1).

3.2. Fertilized Mesocosms

Phytoplankton chlorophyll a, total algal biovolume and abundance were all significantlyrelated to nutrient additions, and this effect was more outstanding in the absence of sub-merged macrophytes (Fig. 1, Table 3). Phytoplanktonic chlorophyll a correlated positivelywith total phosphorus, nitrate and total suspended solids with and without plants (TP: r2 =0.753 and r2 = 0.757; Nitrate: r2 = 0.579 and r2 = 0.219; TSS: r2 = 0.469 and r2 = 0.686,respectively; P < 0.001). Chlorophyll a correlated with ammonium in the presence of plants(r2 = 0.356, P < 0.001), while this correlation was negative in their absence (r2 = 0.058,r = –0.241, P < 0.01).

Diversity and species richness also decreased to lower diversities (< 1.7 bits ind–1) andnumber of species (mean 11 species) at N2 and N3 during the plant-free period (Table 3).The biovolume of total cyanobacteria and chlorophyceae increased significantly in line withincreasing nutrient levels in the absence of charophytes, in detriment to other groups (dino-phytes and euglenophytes, Table 3). Filamentous cyanobacteria with a GALD > 50 µm pre-dominated at higher nutrient levels, while small chroococcal cyanobacteria dominated in N1both in the presence and absence of plants (Table 3, Fig. 1). During the vegetated period, inthe N1 mesocosms small chlorophytes predominated (Scenedesmus ecornis, 28% of totalbiovolume), together with cyanobacteria (M. tenuissima, 16% and Cy. cf. muscicola, 10%



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Figure 1. Phytoplankton chlorophyll a (triangle) and biovolume of the main phytoplankton groups(bars) in the open lake and the mesocosms with different nutrient and fish additions, for the periods ofpresence (P) and absence (A) of submerged macrophytes in the mesocosms. The open lake was untreat-ed and maintained its submerged plants during the study. Values are weighted average ± standard error.

of total biovolume) and cryptophytes (C. erosa, 8%) (Fig. 1). During the plant-free periodcomposition shifted toward M. tenuissima (up to 64% total biovolume, Fig. 1). In the N2and N3 mesocosms, the phytoplankton composition changed from mainly Geitlerinema sp.and Ps. galeata (with 26–33% and 10–3% of total biovolume, respectively) and chlorophytes(Sc. dimorphus and Sc. obliquus, 12–14% and 9–6% of total biovolume, respectively),towards a higher percentage of cyanobacteria (Ps. galeata, Chroococcus spp. and Plank-tolyngbya limnetica, 40–25%, 18–28% and 9–14% of total biovolume) (Fig. 1).

Planktivorous fish only enhanced the biovolume of cryptophytes in the presence of plants(P < 0.01), whereas during the plant-free period the biovolume and abundance of Chroococ-cus spp. and Cy. cf. muscicola increased with fish density (Table 3). In the fishless meso-cosms the number of some oscillatorial species (mostly Ps. galeata and Pl. limnetica)increased during the plant-free period (P < 0.05) (Fig. 1). The highest fish density (20 g freshmass m–2) negatively affected algal diversity and species richness (P < 0.01) in the presenceof plants, conversely, without macrophytes there was no noticeable effect on these variables.

3.3. Algae Recruitment from the Sediment

Total daily algal recruitment from the sediment increased with nutrient levels, while fishdensity was not significant (Table 4, Fig. 2). Mainly cyanobacteria were significantly recruit-ed at higher nutrient levels and there was a positive correlation between the daily recruit-



Table 3. Summary of statistics to study the variables in the mesocosms with different lev-els of nutrients (N) and planktivorous fish (F) during the plant-free period. The phyto-plankton groups and species were compared on the basis of their biovolumes. Probabilities:* P < 0.05, ** P < 0.01, *** P < 0.001, n.s. = not significant. Arrows indicate a positive (↑)

or negative (↓) response to the treatments.

After

N F N · F

Planktonic algal chlorophyll a *** ↑ n.s. n.s.Total phytoplankton *** ↑ n.s. n.s.Total Cyanobacteria ** ↑ n.s. n.s.Chroococcal Cyanobacteria *** ↑ * ↑ n.s.

Chroococcus spp. *** ↑ * ↑ n.s.Merismopedia tenuissima *** ↑ n.s. n.s.

Filamentous Cyanobacteria *** ↑ n.s. n.s.Planktolyngbya limnetica *** ↑ n.s. n.s.Cylindrospermum muscicola n.s. * ↑ n.s.Geitlerinema sp. ** ↑ n.s. n.s.Pseudanabaena galeata *** ↑ n.s. n.s.

Total Chlorophyceae ** ↑ n.s. n.s.Total Cryptophyceae n.s. n.s. n.s.Total Bacillarophyceae n.s. n.s. n.s.Total Dinophyceae ** ↓ n.s. n.s.Total Euglenophyceae ** ↓ n.s. n.s.GALD biovolume < 50 µm *** ↑ n.s. n.s.GALD biovolume > 50 µm n.s. n.s. n.s.Shannon-Wiener diversity (bits individuals–1) ** ↓ n.s. n.s.Species richness (taxa per sample) *** ↓ n.s. *

ment of the dominant cyanobacteria species and their population numbers in the water phase(Table 4, Fig. 2).

Algal recruitment in the N0 mesocosms was mainly composed by a pool of small algaewith a predominance of cyanobacteria (Chroococcus spp. 35%, Peridinium umbonatum11%, Rhodomonas minuta 9%, Chlorella minutissima 7%, Scenedesmus ecornis 7%,M. minutum 4% and Ps. galeata 1.5% of total algal recruitment), although the most abun-dant species in the water phase was not significantly recruited from the sediment (M. tenuis-sima, Fig. 1, Table 4). Numbers of individuals recruited from the sediment surface repre-sented 61% of the planktonic standing crops of P. umbonatum and 25%, 18% and 12% of those of R. minuta, Chroococcus spp. and Ps. galeata, respectively. At the N3 treatment,filamentous cyanobacteria (Planktolyngbya limnetica, Ps. galeata and Geitlerinema sp., with 23%, 14% and 4% of total algal recruitment, respectively), Chroococcus spp. and a pool of chlorophytes (38% and 13% of total algal recruitment, respectively) were the main species recruited in the traps (Table 4, Fig. 2). The contribution of individuals to their planktonic populations was important for Pl. limnetica (28%) and Chroococcus spp.(14%).



Table 4. Summary of statistics for the sediment recruitment of the main algal groups andspecies under different nutrient and fish treatments. The last column shows the correlationbetween the daily recruitment of the species from the sediment in a week and their stand-ing stock in the water phase in the following week. Probabilities: * P < 0.05, ** P < 0.01,***P < 0.001, n.s. = not significant. Arrows indicate a positive (↑) or negative (↓) response

to the treatments.

Nutrient Fish Correlation

Total algal recruitment * ↑ n.s.Total Cyanobacteria * ↑ n.s.Chroococcal Cyanobacteria n.s. n.s.

Chroococcus spp. ** ↑ n.s. **Merismopedia tenuissima n.s. n.s. n.s.

Filamentous Cyanobacteria * ↑ n.s.Planktolyngbya limnetica n.s. n.s. ***Geitlerinema sp. n.s. n.s. **Pseudanabaena galeata * ↑ n.s. ***

Total Chlorophyceae n.s. n.s.Chlorella minutissima n.s. n.s. n.s.Monoraphidium contortum n.s. * ↑ n.s.Monoraphidium minutum * ↑ n.s. **Scenedesmus dimorphus ** ↑ n.s. *Scenedesmus ecornis n.s. n.s. *Scenedesmus obliquus *** ↑ n.s. n.s.Scenedesmus quadricauda * ↑ n.s. **

Total Cryptophyceae n.s. n.s.Cryptomonas erosa n.s. n.s. n.s.Rhodomonas minuta n.s. n.s. n.s.

Total Bacillarophyceae n.s. n.s.Total Dinophyceae n.s. n.s.

Peridinium umbonatum n.s. n.s. n.s.Total Euglenophyceae n.s. n.s.

4. Discussion

Nutrient levels exerted greater influence on the ecology of phytoplankton than density ofplanktivorous fish during the study. Phytoplankton biomass increased in line with nutrientlevels, especially in the absence of submerged plants, with a reduction in algal diversity andspecies richness and dominance of cyanobacteria. Algal diversity and species richness washigher in the lesser enriched mesocosms and with presence of charophytes. The correlationvalues between total phosphorus and chlorophyll a observed in our experiment (r2 = 0.75and r2 = 0.76, with presence and absence of plants, respectively) were similar to thosedescribed for some temperate shallow lakes, but greater than those observed for some trop-ical and subtropical lakes (r2 = 0.42, HUSZAR et al., 2006). The results of this study are inagreement with the critical ratio of total phosphorus to algal chlorophyll a of 3 : 1, whichseparates submerged macrophyte-dominated lakes from algal-dominated deep and shallowlakes (DOKULIL and TEUBNER, 2003). BLINDOW et al. (2002) reported a similar value for thepresence of charophytes in shallow lakes.

According to SØNDERGAARD and MOSS (1998), flagellates and motile algae should pre-dominate in standing waters with macrophytes, and in fact, a higher percentage of motilealgae were present in the phytoplankton assemblage of all the mesocosms during the vege-tated phase. As observed in some shallow lakes (BLINDOW et al., 2002; TAKAMURA et al.,2003), water transparency (measured as total suspended solids) decreased in the absence ofcharophytes, and was mainly related to phytoplankton growth at increasing nutrient levels.During this study cyanobacteria predominated in all the mesocosms, especially in theabsence of submerged macrophytes, in contrast to JASSER (1995), who argued that a phyto-



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Euglenophyceae Bacillariophyceae

Cryptophyceae

Dinophyceae

Chlorophyceae

Chroococcal cyanobacteria

Filamentous cyanobacteria

Phytoplankton abundance

Figure 2. Daily recruitment from the sediment surface of the algal groups (bars) and total phyto-plankton abundance (triangles) in the untreated (N0) and the highest nutrient loading (N3) mesocosms,as well as at the fishless (F0) and the highest fish density (F2) mesocosms. Bars are weighted aver-

age ± standard error.

plankton community in the presence of submerged macrophytes should have a lower amountof cyanobacteria and higher presence of chlorophytes and small algae, given the selectiveeffect of allelopathic substances against cyanobacteria. Results indicate that recruitment ofcyanobacterial resting stages from the sediment played an important role in increasing epil-imnic populations of the dominant species and depleting algal diversity at higher nutrientlevels. The contribution of recruitment to planktonic populations was higher than that report-ed for other cyanobacteria (STÅHL-DELBANCO et al., 2003; VERSPAGEN et al., 2005). The totaldaily recruitment of cyanobacteria was about two-fold higher than that reported by STÅHL-DELBANCO et al. (2003) in a mesocosm experiment. Previous studies have found that therecruitment rate of phytoplankton can be slowed down by the presence of grazers (HANSSON,1996b, 2000). In this study, recruitment of algae did not seem to be significantly affectedby grazers mediated by planktivorous fish predation, as also observed by STÅHL-DELBANCO

et al. (2003). In the absence of plants, the zooplankton to phytoplankton ratio decreased byan order of magnitude (mean from 0.15 to 0.02) and fish significantly removed the macro-zooplankton in the mesocosms, both in the presence and absence of plants (R. MIRACLE, per-sonal communication; ROMO et al., 2004).

In contrast to other studies (BEKLIOGLU and MOSS, 1996; JEPPESEN et al., 1999; JEPPESEN

et al., 2000; VANDER ZANDEN and VADEBONCOEUR, 2002; LAU and LANE, 2002; MUYLAERT

et al., 2003), the effect of planktivorous fish densities on phytoplankton ecology was weak-er than that exerted by nutrients. SCHRIVER et al. (1995) observed that the presence of macro-phytes and absence of planktonic cladocerans enhanced the dominance of large cyanobacte-ria (mainly Planktothrix, Limnothrix, Microcystis and Aphanothece) and dinoflagellates,while in the absence of plants and cladocerans, phytoplankton shifted to small diatoms andchlorophytes. Higher fish densities mainly favoured small chroococcal cyanobacteria(Chroococcus spp.) in the plant-free period, while filamentous cyanobacteria were moreabundant in the fishless mesocosms.

To conclude then, nutrients and submerged plants affected phytoplankton biomass, com-position and diversity, more than the density of planktivorous fish. Absence of charophytesin combination with nutrients significantly increased phytoplankton biomass, turbidity andcyanobacteria in all the mesocosms. Recruitment of cyanobacteria from the sediment (bothchroococcal and filamentous species) significantly supported the standing crops of the dom-inant cyanobacteria species in the water phase. Total daily recruitment of cyanobacteria wasfavoured by high nutrient concentrations, but scarcely affected by the planktivorous fish den-sities. The role played by nutrients, fish, submerged macrophytes and algal recruitment fromthe sediment in shallow tropical, subtropical and Mediterranean lakes needs further study(see for review JEPPESEN et al., 2005; BEKLIOGLU et al., 2007). The results of this study sup-port the idea that cyanobacterial growth can be rapidly enhanced by external nutrient load-ings and their populations maintained by individuals recruited from the sediment surfacewhen lakes are devoid of submerged plants. Therefore, it seems essential to take measuresfor the conservation of submerged macrophytes in order to maintain the ecological qualityof shallow Mediterranean lakes and to prevent cyanobacterial blooming and avoid cyano-toxicity problems.

5. Acknowledgements

We thank our SWALE team for sharing sampling and laboratory work during the study. We are alsoespecially grateful to Dr. LARS ANDERS-HANSSON and Dr. ANNIKA STÅHL-DELBANCO for their advice andsupervision on algae recruitment and to SUSANA MARTÍNEZ for her inestimable collaboration in part ofthis study. We also thank to F. BARRACLOUGH for English revision of the manuscript. This work wasfunded by a European Community project (SWALE, Environment Project ENV4-CT97–0420).



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Manuscript received July 20th, 2006; revised May 3rd, 2007; accepted May 23rd, 2007



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Effects of Nutrients, Fish, Charophytes and Algal Sediment Recruitment on the Phytoplankton Ecology of a Shallow Lake