Changes in benthic macroinvertebrate abundance and lake isotope (C

Changes in benthic macroinvertebrate abundance and lake isotope (C, N) signals following biomanipulation: an 18-year study in shallow Lake Vaeng, Denmark T. Boll, L. S. Johansson, T. L. Lauridsen, F. Landkildehus, T. A. Davidson, M. Søndergaard, F. Ø. Andersen & E. Jeppesen Hydrobiologia The International Journal of Aquatic Sciences ISSN 0018-8158 Volume 686 Number 1 Hydrobiologia (2012) 686:135-145 DOI 10.1007/s10750-012-1005-4

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Author's personal copy Hydrobiologia (2012) 686:135–145 DOI 10.1007/s10750-012-1005-4

PRIMARY RESEARCH PAPER

Changes in benthic macroinvertebrate abundance and lake isotope (C, N) signals following biomanipulation: an 18-year study in shallow Lake Vaeng, Denmark T. Boll • L. S. Johansson • T. L. Lauridsen • F. Landkildehus • T. A. Davidson • M. Søndergaard • F. Ø. Andersen • E. Jeppesen

Received: 24 June 2011 / Revised: 13 December 2011 / Accepted: 15 January 2012 / Published online: 3 February 2012 Ó Springer Science+Business Media B.V. 2012

Abstract Change in the abundance of benthic macroinvertebrates and the stable isotope composition (C, N) of benthic invertebrates and zooplankton in Lake Vaeng, Denmark, was investigated over an 18-year period following biomanipulation (removal of cyprinids). During the first nine years after biomanipulation, the lake was clear and submerged macrophytes were abundant; after this period, a shift occurred to low plant abundance and high turbidity. Two years after the biomanipulation, total density of

Handling editor: Sonja Stendera T. Boll (&) L. S. Johansson T. L. Lauridsen F. Landkildehus T. A. Davidson M. Søndergaard E. Jeppesen (&) Department of Bioscience, Aarhus University, Vejlsøvej 25, 8600 Silkeborg, Denmark e-mail: [email protected] E. Jeppesen e-mail: [email protected] T. Boll F. Ø. Andersen Institute of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark E. Jeppesen Greenland Climate Research Centre (GCRC), Greenland Institute of Natural Resources, Kivioq 2, P.O. Box 570, 3900 Nuuk, Greenland E. Jeppesen Sino-Danish Education and Research Centre (SDC), Beijing, China

benthic macroinvertebrates reached a maximum of 17042 (±2335 SE) individuals m-2 and the density was overall higher when the lake was in a clear state. Redundancy analysis (RDA) suggested macrophyte abundance and total nitrogen (TN) concentration were the dominant structuring forces on the benthic macroinvertebrate assemblage. Stable isotope analysis revealed that d13C of macroinvertebrates and zooplankton was markedly higher in years with high submerged macrophyte abundance than in years without macrophytes, most likely reflecting elevated d13C of phytoplankton and periphyton mediated by a macrophyte-induced lowering of lake water CO2 concentrations. We conclude that the strong relationship between macrophyte coverage and d13C of macroinvertebrates and cladocerans may be useful in paleoecological studies of past changes in the dynamics of shallow lakes, as change in macrophyte abundance may be tracked by the d13C of invertebrate remains in the sediment. Keywords Stable isotope analysis Chironomidae Zooplankton Cladocera Macrophytes

Introduction Biomanipulation (i.e. removal of benthivorous and zooplanktivorous fish) has been used for decades as a tool to shift eutrophicated lakes from a turbid phytoplankton-dominated state to a clear water macrophyte-

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dominated state (Hansson et al., 1998; Søndergaard et al., 2008). Roach (Rutilus rutilus L.) and bream (Abramis brama L.) are the main targets of biomanipulation in Northern European temperate lakes as they not only feed on zooplankton but also disturb the sediment in their search for sediment-dwelling invertebrates (Lammens, 1999; Søndergaard et al., 2008). Following removal of benthivorous and zooplanktivorous fish, large-bodied zooplankton increase in density and their grazing pressure on algae is enhanced (Hansson et al., 1998; Søndergaard et al., 2008), leading to higher water clarity. The benthic system is, however, also affected as fish-mediated resuspension of algal cells (Roozen et al., 2007) and sediment (Breukelaar et al., 1994) decreases, and together with the effects of enhanced grazing on phytoplankton by zooplankton, light penetration is enhanced (Meijer et al., 1990). The improved light climate stimulates benthic algae production (Liboriussen & Jeppesen, 2003; Vadeboncoeur et al., 2003), and potentially benthic macroinvertebrate production as well. More importantly, the reduction in the fish stock releases benthic invertebrates from predation often leading to a higher biomass (Ball & Hayne, 1952; Hanson & Butler, 1994; Leppa¨ et al., 2003). If submerged macrophytes become abundant, the number of plant-associated macroinvertebrates may increase as well (Hargeby et al., 1994). However, a dramatic reduction in the biomass of large bream and roach may also release the remaining fish stock from competition and result in more benthivory (Persson & Hansson, 1999; Persson & Bro¨nmark, 2002), which potentially could counteract the positive effects on benthic macroinvertebrate abundance mentioned above. In many case studies, biomanipulated lakes have shifted back to the turbid state 5–10 years after fish removal (e.g. Meijer et al., 1999; Søndergaard et al., 2007, 2008), which have been attributed to a recovery of the stock of zooplanktivorous fish, poor conditions for establishment of macrophytes or continuously high external or internal loading (Jeppesen et al., 1997; Hansson et al., 1998; Søndergaard et al., 2008), but so far the response of macroinvertebrates has not been included in such fairly long-term studies. Biomanipulation aimed to reduce the abundance of roach and bream was conducted in Lake Vaeng during the years 1986–1988 (Søndergaard et al., 1990). Postbiomanipulation, submerged macrophytes established, became abundant and were dominated by

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Elodea canadensis Michx. In 1997, the plants disappeared abruptly following a gradual increase in the abundance of benthivorous and zooplanktivorous fish and the lake returned to the turbid state. Since 1998, submerged macrophytes have been almost disappeared from the lake and the stocks of roach, and to a lesser extent bream and perch (Perca fluviatilis L.), have increased. Information on changes in trophic dynamics and habitat selection has increasingly been obtained from analyses of stable isotopes (Peterson & Fry, 1987; Grey, 2006). The stable isotope d15N changes in predictable ways up through the food chain (change: *3.4% per trophic level) and is therefore a useful indicator of alterations in trophic interactions (Deniro & Epstein, 1981; Minagawa & Wada, 1984; Vander Zanden & Rasmussen, 2001; Post, 2002), while d13C of primary producers depends mainly on carbon source, carbon availability and potential boundary layers and is only slightly affected by trophic position (change: 0–1% per trophic level) (Deniro & Epstein, 1978; France, 1996; Vander Zanden & Rasmussen, 2001; Post, 2002). In shallow lakes, an increase in the abundance of a particular primary producer, for example macrophytes or periphyton, may potentially influence the d13C signal of other primary producers, such as phytoplankton (Ventura et al., 2008), as they compete for CO2 (Sand-Jensen & Borum, 1991). Phytoplankton d13C and periphyton d13C could, however, also be affected by reduced release of CO2 from the sediment due to a macrophyte-induced decrease in resuspension (more quiescent water and less benthivorous fish when macrophytes are abundant). CO2 limitation or a proportional reduction in 13 C-depleted respired CO2 may result in higher d13C of the primary producers (Peterson & Fry, 1987). Recent studies have demonstrated that archive material is useful for analysis of past changes in stable isotopes in freshwater habitats (Sarakinos et al., 2002; Feuchtmayr & Grey, 2003; Maguire & Grey, 2006; Syva¨ranta et al., 2008; Grey et al., 2009; Ventura & Jeppesen, 2009, 2010) and may help to fill in gaps in a data series on trophic dynamics. We hypothesised that (1) the density and taxa richness of benthic macroinvertebrates would be higher in the years with high coverage of submerged vegetation and with low abundance of benthivorous fish, especially that of bream. To investigate how the community of benthic macroinvertebrates responded

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to these changes, we analysed sediment samples collected yearly during the period 1988–2006 and (2) the d13C of primary consumers and detritivores (such as Cladocera, Oligochaeta and Chironomus sp.) and their invertebrate predators (for example Tanypodinae and Ceratopogonidae) would be higher in macrophyte years as a consequence of higher d13C in their food source (i.e. phytoplankton and periphyton), mediated by CO2 limitation caused by the macrophytes and the d13C signal would be related to macrophytes abundance and therefore potentially be useful as a proxy for macrophytes in the past. We, therefore, conducted stable isotope analyses of stored samples of macroinvertebrates and zooplankton from the period 1988–2006 to reveal whether the isotope signal of the invertebrates changed over the period.

Materials and methods Study site Lake Vaeng is a shallow (mean depth 1.2 m, maximum depth 1.9 m) lake located in the central part of Jutland, Denmark (N 56°02.150; E 009°39.300). The lake area is 15.7 ha, and the catchment area of 9 km2 consists of agricultural and forest areas, and a gravel pit. Small ditches enter the lake in the northern part, but the lake receives about 90% of its water via groundwater. The lake has one outlet, and the hydraulic retention time is 15–25 days. Until 1981, sewage from a nearby village entered the lake near the outlet and provided enough nutrients to keep the lake in a turbid phytoplankton-dominated state (Sensu Scheffer et al., 1993). Even when this external loading was diverted, the lake remained turbid (Søndergaard et al., 1990). In an attempt to restore the lake, approximately four tons of benthivorous and zooplanktivorous fish (mainly bream and roach) were removed during the years 1986–1988 by use of gill, fyke and pound nets as well as electrofishing. Following biomanipulation, the lake remained in the clear water state until 1997 when it returned to the turbid state with increasing concentrations of chlorophyll a in the subsequent years (Fig. 1) as well as an increasing biomass of benthivorous and zooplanktivorous fish (Søndergaard et al., 2007). Since 1996, roach has dominated numerically with their abundance increasing during the investigation period. Catch per unit

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effort (CPUE) of both bream and perch was relatively stable during the first half of the study period; as from the late 1990s, it increased, albeit with large year-to-year variations (Fig. 2). Following biomanipulation submerged macrophytes appeared in the lake, initially Potamogeton crispus L. was the most abundant species, but during 1991–1993 E. canadensis became more dominant (Lauridsen et al., 1994), and in 1994–1995 this species was completely dominating. Other species found in the lake included Potamogeton pectinatus L. and P. berchtoldii Fieber. Sampling Sediment samples were collected annually from the lake with thirty samples collected in 1988 and thereafter ten samples per year in 1989–2006 (except for 1995, 2002 and 2005). Sampling points were randomly selected each year assuming an approximately even distribution in the lake. The lake sediment was generally soft, consisting of organic-rich mud (Lauridsen et al., 1993); however, no characterisation of the sediment type or macrophyte cover for the sites of the macroinvertebrate samples is available. Samples were collected in February or March using Kajak cores (diameter: 5.2 cm) and sieved through a 212-lm sieve before the retained material was preserved in 96% ethanol. After sorting and counting, the macroinvertebrates were stored in 70% ethanol. For zooplankton analyses, six litres of water was collected with a tube sampler from the water surface to the lake bottom, and the water was filtered trough a 20-lm filter and preserved in acid Lugol’s solution. Fish surveys were conducted yearly (August/ September) from 1988 to 2006 using multi-mesh-size survey nets (sequence of mesh sizes: 10, 60, 30, 43, 22, 50, 33, 12.5, 25, 38, 75, 16.5, 8, and 6.25 mm). In this study, focus is on the dominant fish species (perch \15 cm, roach and bream). Besides these three species, the lake also has species such as rudd (Scardinius erythropthalmus Bonaparte), pike (Esox lucius L.), European eel (Anguilla anguilla L.) and less common: tench (Tinca tinca L.), ruffe (Gymnocephalus cernuus L.), crucian carp (Carassius carassius L.), common minnow (Phoxinus phoxinus L.) and gudgeon (Gobio gobio L.) (Søndergaard et al., 1990). A description of the macrophyte coverage was conducted using 14 transects that together covered the whole lake (Lauridsen et al., 1994). Each transect

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Fig. 1 A Interpolated daily values of pH and total alkalinity illustrated together with macrophyte coverage. pH and total alkalinity are represented by the y-axes on the left and macrophyte coverage by the axis on the right. B Interpolated daily values of chlorophyll a and temperature (left y-axis) shown together with macrophyte coverage (right y-axis)


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included 6–12 equidistantly spaced stations depending on the length of the transect. The macrophyte coverage at each station was estimated one (1989) to ten times annually and assigned to one of five categories (0, 1–5, 5–25, 25–50, 50–75, 75–100%) (Lauridsen et al., 1994; Jeppesen et al., 1998). During the whole period, chlorophyll a, water temperature and water chemistry were monitored regularly. Chlorophyll a was extracted in ethanol and measured according to Jespersen & Christoffersen (1987), and the chemical variables were measured by standard methods (Jeppesen et al., 1990; Søndergaard et al., 1990). Summer mean concentration of total phosphorous (TP) and total nitrogen (TN) in the lake water ranged from 0.05 to 0.17 mg P/l and 0.5 to 1.2 mg N/l, respectively, with both being lower in years with abundant macrophyte coverage (Jeppesen et al., 1998; Søndergaard et al., 2007). Stable lsotope analyses Macroinvertebrates, stored in ethanol, were rinsed with ultra pure water (Elga maxima) and oven-dried at

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60°C for approximately 24 h. After drying, macroinvertebrates were ground into fine powder, homogenised, weighed (*1 mg) and packed into tin capsules. The number of replicates varied from one to five depending on the amount of available material. Isotope studies on zooplankton included samples from the beginning of April (April 1 ± one month) in the period 1988–2006 except 1994 and 2003 that included samples from 6 June (1994), and from 1 April and 6 June (2003). Zooplankton was rinsed in ultra pure water (Elga maxima) to remove the acid Lugol’s solution, freeze-dried for two hours and otherwise treated as described above. Neither benthic invertebrates nor zooplankton was analysed at species level but was pooled at a higher taxonomic levels (Cladocera, Cyclopoid Copepoda, Ceratopogonidae, Chironomini [excl. Chironomus sp.], Chironomus sp., Oligochaeta, Tanypodinae) to ensure sufficient amounts of material. Stable N and C isotopic analyses were performed on a PDZ Europa ANCA-GSL elemental analyzer interfaced to a PDZ Europa 20–20 isotope ratio mass spectrometer (Sercon Ltd., Cheshire, UK) at UC Davis Stable Isotope Facility, University of Davis, California,

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Fig. 2 A Mean densities (±SE) of benthic macroinvertebrates collected in Lake Vaeng from 1988 to 2006 except for the years 1995, 2002 and 2005. Catch (individuals per net per night [CPUE]) of perch smaller than 15 cm, bream, and roach (from the previous year) is shown on the right y-axis. B Mean densities (±SE) of chironomids collected in Lake Vaeng from 1988 to 2006. Estimates of macrophyte coverage during the periods prior to sampling of benthic macroinvertebrates are shown on the right y-axis

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USA. Stable isotope ratios were calculated as dX(%) = (RSample/RStandard - 1) * 1000 where X is either 13C with the corresponding ratio, R, 13C/12C or 15 N with corresponding R, 15N/14N. Pee Dee Belemnite and atmospheric nitrogen (AIR) were used as standards for carbon and nitrogen analysis, respectively. Corrections for effects of preservatives on the signals of d13C and d15N were conducted according to Ventura and Jeppesen (2009). Statistical analysis Detrended correspondence analysis (DCA) (Hill & Gauch, 1980) was carried out to determine the gradient length of the first axis of variation in the invertebrate assemblage. As the length of the gradient was 2.0, linear methods were more appropriate (ter Braak & Prentice, 1988). Indirect gradient analysis using principal components analysis (PCA) was conducted to examine the main axes of variation in the benthic macroinvertebrate assemblages. Redundancy analysis (RDA) with forward selection and Bonferroni correction (Legendre & Legendre, 1998) was employed to assess the relative

importance of environmental variables in explaining the variation in the macroinvertebrate assemblage. Environmental variables tested in the RDA were submerged macrophyte coverage, chlorophyll a, suspended matter, TP, TN, pH and CPUE (CPUE in multimesh sized gill nets set overnight) of bream, roach and perch. Partial RDA (pRDA) (Borcard et al., 1992) was then performed to determine the percentage variance in the macroinvertebrate assemblage data uniquely attributable to each environmental parameter contained in the minimum adequate model from the RDA with forward selection. As there were two significant structuring variables, pRDA entailed placing each on in turn as the active environmental variable with the other as a covariable, which allows the determination of the proportions of variance in the macroinvertebrate assemblages uniquely attributable to each parameter and the proportion of the explained variance that is shared. All variables were log(x)-transformed, with the exception of macrophyte coverage and CPUE, which were log (x ? 1)-transformed, and pH that is already at a log scale. Since benthic macroinvertebrates were collected in February and March and fish in August and

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Total density of benthic macroinvertebrates varied markedly among years, with the highest densities (17042 ± 2335) (mean ± SE) occurring in 1990, shortly after the biomanipulation, and the lowest in 2004 (375 ± 240) when the lake was in a turbid state (Fig. 2). The DCA of the macroinvertebrate assemblage revealed a relatively short gradient length of the first axis (2.0). The first two axes of PCA (Fig. 3) explained 51.2% of the variance in the invertebrate data and demonstrated there were large between year differences in the macroinvertebrate community composition. There was a sharp divide in macroinvertebrate assemblage between years with and without macrophytes. The years with few macroinvertebrate taxa grouped together (left side in Fig. 3) and had low or no macrophyte coverage. Asellus aquaticus (L.), leeches, molluscs including gastropods and Pisidium sp., and insects including Odonata, Ephemeroptera, Trichoptera, Orthocladiinae and Tanytarsini were mainly or only found in years with abundant macrophyte coverage (Fig. 2). The RDA, with forward selection confirm the finding of the PCA revealing macrophyte coverage

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When macrophyte coverage was high, pH reached values up to 10 (Fig. 1A). Chlorophyll a concentrations fluctuated between 2 and 190 lg/l with the exception of 16 March 1992 and 7 February 1995 where peak values of 770 lg/l and 501 lg/l, respectively, were recorded (Fig. 1B).

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September, CPUE of fish from the year prior to the sampling of macroinvertebrates was used as explanatory variable. The other explanatory variables were included as time-interpolated averages covering the expected growth period for the macroinvertebrates (i.e. the period lasting from August 1 in the year prior to the sampling until the sampling date). Numbers of macroinvertebrates per sample were log(x ? 1)-transformed prior to analysis, and this stronger transformation was preferred as the distribution of some taxa contained very large variation in the numbers per m2. Analyses were conducted in CANOCO version 4.5 (ter Braak & Smilauer, 2002). Macroinvertebrates stable isotope signal was also compared with the time-interpolated averages for macrophyte coverage that were described earlier. Due to the relatively short lifespan of zooplankton, the stable isotope signal was related to the time-interpolated averages of macrophyte coverage covering the last 30 days before the date (or dates) where zooplankton were sampled. Results from stable isotope analysis were grouped according to macrophyte (macrophyte coverage[5%) and non-macrophyte years and plotted in a d13C–d15N bi-plot. Macrophyte years included 1989–1994, 1996– 1997 (macroinvertebrates) and 1989–1992, 1994–1996 (zooplankton). Non-macrophyte years were 1988, 1998–2006 (macroinvertebrates) and 1987–1988, 1993, 1997–2006 (zooplankton). Student’s t test was used for testing for differences in d13C and differences in d15N between the two periods, except in cases where variance was unequal. In these cases, an unequal variance t test was used instead of Student’s t test. Macroinvertebrate groups found in only one of the two periods were not included in the stable isotope study. Plots and statistics were conducted in PAST version 2.07 (Hammer et al., 2001) and SAS software version 9.1.3 (SAS Software, 1987).


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Fig. 3 PCA plot conducted using data on macroinvertebrate assemblages. The size of each dot indicates the relative coverage of submerged macrophytes. Data were log(x ? 1)-transformed before the analysis. Piscicol Piscicolidae, Erpobdel Erpobdella, Planorbi Planorbidae, Ephemero Ephemeroptera, Corixida Corixidae, Lymnaeid Lymnaeidae, Orthocld Orthocladiinae, Asellida Asellidae, Ceratopo Ceratopogonidae, Glossiph Glossiphonidae, Valvatid Valvatidae, Spaerii Spaeriidae, Trichopt Trichoptera, Tanytars Tanytarsini, Bithynii Bithyniidae, Chironom Chironomini, Oligocha Oligochaeta, Gastropo Gastropoda, Chaobori Chaoboridae

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Fig. 4 A d13C of cladocerans, cyclopoid copepods, and Chaoborus sp. from Lake Vaeng plotted together with macrophyte coverage during the 30-day period prior to zooplankton sampling. B d13C of benthic macroinvertebrates from Lake Vaeng plotted together with macrophyte coverage during the expected growth period for the benthic macroinvertebrates

Macrophyte cover

Discussion The data demonstrate that macrophyte abundance played an important structuring role in benthic macroinvertebrate community composition. In agreement with previous work, some taxa, such as Asellus aquaticus, gastropods, leeches and insects, showed a strong affinity with abundant submerged macrophytes (Hargeby et al., 1994; Marklund et al., 2001). TN was also an important explanatory variable, but it is likely a surrogate for lake trophic state since high TN concentrations were mainly found in years where the lake was in a turbid state and the numbers of macroinvertebrate taxa low. The peak in total density of macroinvertebrates and chironomids observed in 1990, shortly after the biomanipulation, concurs with hypothesis 1 and likely reflects a reduced predation pressure from fish (Ta´trai et al., 1997; Leppa¨ et al., 2003; Persson & Svensson, 2006) and the increase in submerged macrophyte coverage (Hargeby et al., 1994). In our study, it is difficult to separate the direct effects of submerged macrophytes from those of zoobenthivorous fish on the abundance of benthic macroinvertebrates. Some plant-associated macroinvertebrates perform daily migration to the sediment (Marklund et al., 2001), and this may explain the higher abundance of Cyclopoid copepoda

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(P = 0.001) and TN (P = 0.014) as the significant explanatory variables of the macroinvertebrate community composition together explaining 39.9% of variance. pRDA showed that the majority of the variance, 29.1%, in the invertebrate data was uniquely attributable to macrophyte coverage with 10.7% uniquely explained by TN and just 0.1% shared. The d13C isotope signal of both benthic macroinvertebrates and of cladocerans and copepods apparently showed a similar pattern as the coverage of macrophytes and were highest in years with high macrophyte coverage (Fig. 4). After dividing the data set into two periods, one with macrophytes and one without, and comparing means, we found that d13C of Cladocera, Copepoda, Chironomus sp., Tanypodinae, Ceratopogonidae and Oligochaeta was 2.0 and 4.4 per mil lower when the macrophytes were absent (Fig. 5); for Cladocera, Copepoda, Ceratopogonidae and Oligochaeta, this difference was significant (Table 1). No significant differences were found for d15N of these taxa in macrophyte and non-macrophyte periods (Table 1), though it tended to be slightly higher (*0.5 %) for benthic macroinvertebrates and slightly lower (*0.5 %) for the pelagic invertebrates (Cladocera, Copepoda and Chaoborus sp.) in the period with plants (Fig. 5).

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Fig. 5 d13C–d15N bi-plot showing mean (±SE) isotope signal of A cladocerans, cyclopoid copepods and Chaoborus sp. and B benthic macroinvertebrates from Lake Vaeng. Open circles show years without macrophytes, and dark circles show years with macrophytes

plant-associated macroinvertebrates in the years immediately following the biomanipulation. Moreover, macrophytes make foraging more difficult for benthivorous fish (Diehl, 1988), which indirectly is to the benefit of macroinvertebrates. When plants are absent bream feed efficiently on macroinvertebrates and can have a significant effect on the biomass of certain groups of macroinvertebrates such as clams, gastropods (Persson & Svensson, 2006) and chironomids (Ta´trai et al., 1997). The impact of zoobenthivorous fish on the density and the biomass of benthic macroinvertebrate is therefore expectedly stronger when vegetation is sparse and the lake bottom provides little refuge for the macroinvertebrates (Leppa¨ et al., 2003).

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We found no significant change in d15N for zooplankton and benthic macroinvertebrates between years with macrophytes (and low fish abundance) and those without (when fish biomass was high). Likewise Syva¨ranta and Jones (2008) found no changes in d15N in these taxa from before to after biomanipulation in an urban Finnish lake. Interestingly, however, d15N tended to be lower in zooplankton and higher in benthic macroinvertebrates in years with abundant macrophytes coverage than in years without plants. Unfortunately, due to lack of information of changes in isotope signals in sediment and seston, the reasons behind these changes remain unresolved. There was a synchronous shift in d13C for most of the benthic macroinvertebrates and a similar change of cladocerans and copepods as the lake shifted from a clear macrophyte dominated to a turbid state. It seems likely that an overall decrease in lake d13C rather than a change in the food web structure was responsible as the change in d13C followed the same direction for both benthic and pelagic groups. Syva¨ranta & Jones (2008) found a small increase in d13C of macroinvertebrates two years after a biomanipulation was initiated. The higher d13C of macroinvertebrates by then was explained by a low water level and high production of periphyton and macrophytes and thus a higher contribution of these primary producers than of phytoplankton to the consumer food web. We also found higher d13C of benthic macroinvertebrates in years with macrophytes, but, in contrast to the study of Syva¨ranta & Jones (2008), also in pelagic invertebrates. The higher d13C in macrophyte years could be due to an increase in invertebrates feeding on epiphyton, typically higher in d13C than phytoplankton (France, 1995), as suggested by Syva¨ranta & Jones (2008). However, as the shift in d13C was found in a range of invertebrates from both benthic and pelagic habitats and from different trophic levels render it unlikely that the shift is solely due to a change in diet of the invertebrates but more likely the result of a change in d13C in their preferred food sources. A shift in the species composition within the taxonomic groups analysed as bulk samples might potentially also create a shift in d13C, though it seems unlikely given the fact that the isotope changes in most of the invertebrate groups followed the same pattern. A more probable explanation of the major changes in d13C we observed is that the d13C of the primary producers changed due to CO2 limitation. Lake water

Author's personal copy Hydrobiologia (2012) 686:135–145 Table 1 Results from t test comparing d13C and d15N of benthic macroinvertebrates, cladocerans and cyclopoid copepods between the period with macrophytes (mac.) and the period without macrophytes (no mac.)

Group

Years included (no mac./mac.)

Isotope

df

Cladocera

8/6

d15 N

12

d13 C 15

t value

P

0.62

0.544

6.26

-2.52*

0.044

18 6.93

1.43 -2.65*

0.169 0.033

Cyclopoid Copepoda

13/7

d N d13 C

Ceratopogonidae

6/5

d15 N

9

-0.40

0.697

d13 C

9

-2.83

0.020

d15 N

6

-0.95

0.380

d13 C

6

-0.04

0.969

Chironomini Chironomus sp.

* Indicates that the test was performed with unequal variance t test. In the other cases, Student’s t test were used

143

Oligochaeta Tanypodinae

concentrations of dissolved inorganic carbon (DIC) are affected by lake productivity, and d13C of submerged macrophyte subfossils has proven useful for detecting the past availability of carbon for submerged macrophytes (Herzschuh et al., 2010). In Lake Vaeng, E. canadensis was the dominant submerged macrophyte (Lauridsen et al., 1994), forming dense stands when abundant. The growth of E. canadensis can be limited by inorganic carbon (Vadstrup & Madsen, 1995), and even though this species is capable of using HCO-3, CO2 is the preferred carbon source (Jones, 2005). In dense macrophyte stands, water circulation can be low and the concentration of CO2 may drop to low levels during daytime (Jones et al., 1996). The reduction in CO2 concentrations is most severe in the upper part of the macrophyte stand (Jones et al., 1996) and may potentially cause a decline in the CO2 concentration of the lake as a whole, since CO2 released from the sediment may be captured in the macrophyte stand. Further support comes from the fact that pH was overall high in the period with abundant macrophytes indicating a lower CO2 concentration, and potentially CO2 limitation of primary producers, with less discrimination of 13C in photosynthetic processes and higher d13C of primary producers, including phytoplankton as a result. A similar response is obtained if the phytoplankton uses a higher proportion of atmospheric-derived CO2 (d13C * -7%) relative to CO2 released from in-lake respiration processes (Peterson & Fry, 1987). In years

4/4 5/5 6/7 4/5

d

15

N

8

-0.50

0.633

d13 C

8

-2.10

0.069

d15 N

11

-0.63

0.539

d13 C

11

-3.10

0.010

d15 N

7

-0.40

0.702

4.11

-1.95*

0.121

d

13

C

when submerged macrophytes were absent from Lake Vaeng, more respired CO2 was available to the phytoplankton, presumably leading to lower d13C of phytoplankton and, consequently, of their grazers. Methods for studying past food web interactions from fossil remains are being developed for both cladocerans (Perga, 2010) and chironomids (van Hardenbroek et al., 2010). If macrophytes cause changes in the d13C of primary producers and, thereby, in invertebrates at higher trophic levels, it opens the opportunity of detecting past shifts in lake trophic state by studying the isotope signal of invertebrate (cladocerans and macroinvertebrates) remains found in the lake sediment. In summary, our study evidenced change in the assemblage composition, total density and taxa richness of benthic macroinvertebrates in Lake Vaeng concurrent with a shift from a clear to a turbid state. Submerged macrophytes clearly played a structuring role in these changes by supporting higher density and taxa richness of benthic macroinvertebrates in years with abundant macrophytes than in years without macrophytes. Changes in d13C of benthic macroinvertebrates and zooplankton indicated marked macrophyte-induced alteration of carbon dynamics, implying also that a shift from the clear macrophyte-dominated state to the turbid phytoplanktondominated state may be tracked back in time using analysis of d13C of invertebrate remains in the sediment.

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Author's personal copy 144 Acknowledgement Valuable technical assistance in the field and laboratory was provided by late Jane Stougaard-Pedersen, Lissa Skov Hansen, Birte Laustsen, Karina Jensen and Kirsten Landkildehus Thomsen. We also thank Søren Erik Larsen for statistical advice, Anne Mette Poulsen for editorial assistance, and Tinna Christensen for layout assistance. We also thank the anonymous reviewers for giving useful suggestions to improve this article. The study was supported by the Danish Centre for Lake Restoration (CLEAR—a Villum Kann Rasmussen Centre of excellence project), EU REFRESH and EU WISER, CRES and the Research Council for Nature and Universe (272-080406).

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