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JOURNAL OF PLANKTON RESEARCH j VOLUME 28 j NUMBER 7 j PAGES 707–718 j 2006 Structural and functional properties of low- and high-diversity planktonic food webs URSULA GAEDKE* AND NORBERT KAMJUNKE UNIVERSITY OF POTSDAM, INSTITUTE OF BIOCHEMISTRY AND BIOLOGY, MAULBEERALLEE 2, D-14469 POTSDAM, GERMANY *CORRESPONDING AUTHOR: [email protected] Received November 7, 2005; accepted in principle February 22, 2006; accepted for publication April 6, 2006; published online April 12, 2006 Communicating editor: K.J. Flynn To test the consequences of decreased diversity and exclusion of keystone species, we compared the planktonic food webs in two acidic (pH3), species-poor mining lakes with those in two speciesrich, neutral lakes. The ratio of heterotrophic to autotrophic biomass (H/A) was similar in acidic and neutral lakes with comparable productivity. However, food webs in both acidic lakes were largely restricted to two trophic levels in contrast to the four levels found in neutral lakes. This restriction in food chain length was attributed to the absence of efficient secondary consumers, rather than to productivity or lake size which resulted in unusually low predator–prey weight ratios, with small top predators hardly exceeding their prey in size. In contrast to the neutral lakes, plankton biomass size spectra of acidic lakes were discontinuous due to a lack of major functional groups. The unique size-dependence of feeding modes in pelagic food webs, with bacteria in the smallest size classes followed by autotrophs, herbivores and carnivores, was maintained for bacteria but the other feeding modes strongly overlapped in size. Thus, their characteristic succession along the size gradient was roughly preserved under extreme conditions but the flow of energy along the size gradient was truncated in the acidic lakes. For most but not all attributes studied, differences were larger between acidic and neutral lakes than between neutral lakes of different trophic state. INTRODUCTION Natural and anthropogenic stressors often decrease the taxonomic, functional and trophic diversity of communities with far reaching but still poorly understood consequences for food web structure and function (Duffy, 2002; Hooper et al., 2005). Under extreme conditions species number is typically low, and important functional groups or typical keystone species including top predators may be lacking, leading to simply structured food webs. This was found for sulphurous (Gasol et al., 1991), saline (Wurtsbaugh, 1992), Antarctic (Laybourn-Parry, 1997) and acidic lakes (Kamjunke et al., 2004). This study compares various attributes of the structure and function of multi-trophic level planktonic food webs in two extreme (acidic) lakes with those of two more typical (neutral) lakes to test the effects of low diversity and species exclusion on food web properties. The planktonic food webs of the acidic lakes (Lakes 111 and 117, Eastern Germany) consist mainly of bacteria, two mixotrophic flagellate species, a few protozoan and rotifer species and one (rare) crustacean species (Chydorus sp.) which is found in the less acidic of the two lakes (Wollmann et al., 2000; Kamjunke et al., 2004). Other crustaceans (and fish) acting as keystone elements in planktonic food webs are excluded by the adverse environmental conditions. In contrast, the plankton composition of the neutral lakes (oligo-mesotrophic Lake Constance and highly eutrophic Lake Müggelsee) covers the full range of freshwater plankton from bacteria, small and large phytoplankton and protozoans (mainly heterotrophic nanoflagellates and ciliates) to metazooplankton (rotifers, cladocerans and copepods) (Arndt et al., 1993; Gaedke et al., 2002, 2004). This allowed us to compare species-rich and species-poor plankton food webs with doi:10.1093/plankt/fbl003, available online at www.plankt.oxfordjournals.org Ó The Author 2006. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected] JOURNAL OF PLANKTON RESEARCH j VOLUME and without larger metazoan grazers and to relate their potential differences to the well-studied impact of trophic state on food web properties. Given that microorganisms were less affected by the extreme environment than metazoans, we predict that food web traits dominated by microorganisms such as bacterial and primary production are less altered than metazoan dominated traits, such as consumer composition, top-down control by higher trophic levels, predator–prey weight ratios and food chain length. Without major disturbances, pelagic food webs are characterized by a continuum of organisms along the size gradient (Sheldon et al., 1972; Gaedke, 1992), a restriction of autotrophs to small size classes and predators that exceed their prey in size (Hairston and Hairston, 1993). These properties lead to the characteristic succession of feeding modes (osmotrophy, autotrophy, bacterivory, herbivory and carnivory) from small to large organisms, which distinguishes pelagic food webs from terrestrial ones. They imply that body size provides a simple integrative measure of organism niche. Thus, major changes in trophic structure, keystone species, food chain length and diversity were reflected in the shape and size range covered by the biomass size distribution (Tittel et al., 1998; Gaedke et al., 2004). We use biomass size spectra to provide insight into the functional diversity of the plankton communities, the flux of matter and energy along the size gradient and explanations for biomass accumulations in certain size ranges (Platt and Denman, 1978; Borgman, 1982; Gaedke, 1993). They are also used to determine to what extent a remarkable feature of pelagic food webs (i.e. the continuous succession of feeding modes along a size gradient) is preserved under extreme conditions. For the larger sized organisms, we predict major deviations between biomass size spectra of acidic and neutral lakes in respect to biomass distribution and the succession of feeding modes. To analyse potential deviations in basic food web properties between species-rich and species-poor food webs in common and extreme environments and to test the above-mentioned predictions in particular, we quantified and compared among lakes: (i) (ii) (iii) the bacterial and autotrophic biomass, production and turn-over rates forming the energetic basis of the food webs; the functional composition of each of the plankton communities to provide insight into the quantitative importance of major functional groups and the ratio of heterotrophic and autotrophic biomass (H/A); the trophic structure, using the distribution of biomass across the different trophic levels (i.e. trophic 28 (iv) j NUMBER 7 j PAGES 707–718 j 2006 biomass pyramids), and food chain length, to elucidate major energy flux patterns and taxonomically resolved biomass size spectra, the size spectra of the different modes of nutrition and predator–prey weight ratios. METHODS Study sites For the comparison, we selected two acidic and two neutral lakes. Lakes 111 and 117 are acidic, brown coalmining lakes situated in Eastern Germany (Lusatia; 518290 N, 138380 E). Iron sulphide oxidation in the soils decreased the pH in the mining lakes (pH 2–4), which are buffered by ferric iron hydroxide (Geller et al., 1998). Another characteristic of some lakes (e.g. Lake 111) is the red–brown colouration of the water caused by extremely high concentrations of dissolved ferric iron (150 mg Fe L–1). The two acidic lakes are relatively small (Table I). The planktonic food web of the moreacidic lake (111, pH 2.6) consisted mainly of single-celled and filamentous bacteria, the two mixotrophic flagellates Chlamydomonas acidophila and Ochromonas sp. and Heliozoa as top predators. Very few rotifers (Elosa worallii and Cephalodella hoodi), ciliate and rhizopod species in low densities, and no heterotrophic flagellates, crustaceans or fish, were observed (Wollmann et al., 2000; Kamjunke et al., 2004). In the slightly less-acidic lake (117, pH 3.0), additionally a small pigmented species of Gymnodinium, the large rotifer Brachionus and the small cladoceran Chydorus occurred on occasion in considerable densities (Wollmann et al., 2000). Corixids were excluded from our analysis as they feed predominantly outside the pelagic realm. One of the neutral lakes in our study (Lake Constance) is large, deep, monomictic and meso-oligotrophic and has a food web representative of large open water bodies. The other neutral lake (Müggelsee) is smaller, shallow and eutrophic (Table I). The neutral lakes, therefore, represent two typical lake types with Table I: Morphometric data and pH in the two acidic and the two neutral lakes Lake Area (km2) Mean depth (m) pH 111 0.11 4.6 2.6 117 0.96 7 3.0 Constance Müggelsee 708 476 7.3 101 4.9 7.7–8.5 8 U. GAEDKE AND N. KAMJUNKE j PROPERTIES OF LOW- AND HIGH-DIVERSITY PLANKTONIC FOOD WEBS pronounced differences in productivity and thus in food web structure (Carpenter and Kitchell, 1993). Our considerations focus on the epilimnion of the study lakes. Sampling and data handling In acidic Lakes 111 and 117, the epilimnion was represented by samples from depths of 0–4 and 0–5 m, respectively. For Lake Constance, average values for the upper 20 m were considered, approximately reflecting the euphotic zone and epilimnion of the lake. Data from shallow polymictic Lake Müggelsee were averaged across depth (mean depth 4.5 m). Seasonal means for the period April–October were used for all four lakes. The data describing bacterial biomass, bacterial production and primary production in Lakes 111 and 117 are from Kamjunke et al. (2005). The biomass of phytoplankton and Heliozoa from Lake 111 has been published in Kamjunke et al. (2004). For Lake 117, biomass data were taken from Beulker et al. (2003) for phytoplankton, from Packroff (2000) for ciliates and from Wollmann and Deneke (2004) for zooplankton. The Lake Constance and Lake Müggelsee data were obtained from Gaedke et al. (2002) and Gaedke et al. (2004) for the years 1987– 1993 and 1988–1990, respectively. The lengths and body masses of organisms from the acidic lakes are summarized in Table II. The carbon contents of bacteria, C. acidophila, Ochromonas sp. and Heliozoa were calculated as described in Kamjunke et al. (2004). For Gymnodinium sp. and ciliates, the same factors as for C. acidophila and Heliozoa were used, respectively. The carbon content of Brachionus was measured (G. Weithoff, personal communication), and the individual dry weight of Chydorus sphaericus (1450 ng; Wollmann and Deneke, 2004) was multiplied by 0.5. Table II: Mean length and body mass of the dominant organisms in the planktonic food webs of the acidic lakes (averages ± SD) Length (mm) Single-celled bacteria Filamentous bacteria 0.89 ± 0.19 27.3 ± 7.3 Chlamydomonas 8.4 ± 0.6 Ochromonas 6.2 ± 0.6 Body mass (pg C) 0.02 0.58 23 23 Gymnodinium 12 208 Heliozoa 21.7 ± 2.1 790 Ciliates 20 161 Brachionus 220 160.000 Chydorus 332 725.000 For the neutral lakes, organism size was measured regularly and converted to carbon according to Gaedke et al. (2002, 2004; literature cited therein). The conversion factors used were consistent among lakes. To construct biomass pyramids, we assigned bacteria to the first trophic level (Gaedke and Straile, 1997). In the acidic lakes, the mixotrophic flagellate C. acidophila was regarded to be 80% phototrophic and 20% osmotrophic, and the mixotrophic flagellate Ochromonas sp. was assumed to be 43% autotrophic, 35% bacterivorous and 22% herbivorous (ingesting the similar sized C. acidophila, Tittel et al., 2003). These estimates were obtained from quantitative carbon flow diagrams [modified after Kamjunke et al. (2004)], which were derived from field and laboratory measurements at Lake 111 (e.g. Tittel et al., 2003, 2005; Kamjunke et al., 2004, 2005). Because recent results showed that Heliozoa may grow with bacterial filaments (Bell et al., 2006), we modified the carbon flow diagram of Kamjunke et al. (2004) by assuming that 50% of the production of the bacterial filaments were ingested by Heliozoa. For Lake Constance, the distribution of consumers across the different trophic levels was derived from timeresolved, mass-balanced carbon flow diagrams (Hochstädter, 1997). Sheldon-type biomass size spectra were constructed by placing each organism into a log2-scaled size class according to its individual body mass and summing the biomass in each size class. Filamentous algae were allocated to the size class of the individual cells (for details see Gaedke, 1992). The size spectra of the various feeding modes were obtained by estimating the feeding mode of each component species based on our own measurements (Tittel et al., 2003; Kamjunke et al., 2004; literature cited therein), an extended literature review and mass-balanced carbon flow models (Gaedke et al., 2002). Subsequently, the biomass of each feeding mode per size class was summed up. The biomass of mixotrophs and omnivores was split over the respective feeding modes according to the contribution of each feeding mode. Sensitivity analyses revealed that the inevitable uncertainties involved in the estimation of the diet compositions of individual species did not affect the overall pattern inferred from Fig. 5. Predator–prey weight ratios were calculated for each feeding interaction using the size range covered by the predator and prey species, respectively. Each ratio was weighted by the relative quantitative importance of the feeding interaction for total carbon flux within the food web. For Lake 111, carbon fluxes were derived from quantitative carbon flow diagrams [modified after Kamjunke et al. (2004) to obtain 709 JOURNAL OF PLANKTON RESEARCH j VOLUME 28 j NUMBER 7 j PAGES 707–718 j 2006 seasonal averages and with the additional link between bacterial filaments and Heliozoa]. For Lake Constance, the plankton community was subdivided into 22 trophic guilds ranging from bacteria, through autotrophic picoplankton, heterotrophic nanoflagellates and phytoplankton (five guilds), ciliates (five guilds) and rotifers (four guilds), to crustaceans (five guilds). These trophic guilds were linked by 108 feeding interactions (Lang, 1997). For eukaryotes, the relative quantitative importance of each trophic link was roughly estimated from the biomass and sizedependent metabolic activity of the respective predator and prey guilds assuming mostly unselective feeding for omnivorous guilds. The relative importance of bacteria was inferred from the measured ratio of bacterial and primary production. These estimates were cross-checked with more reliable flux estimates derived from mass-balanced carbon flow diagrams with a lower taxonomic resolution (Gaedke and Straile, 1994). No predator–prey weight ratios were computed for Lakes 117 and Müggelsee because no suitable data on the quantity of carbon fluxes were available. We included only lakes into our study for which food web properties could be quantified based on fully comparable assumptions, for example in respect to carbon content, size allocation and growth efficiencies. RESULTS Bacteria and phytoplankton The biomass of bacteria and phototrophs increased from low values in Lakes 117 and 111, intermediate ones in Lake Constance, to high values in eutrophic Lake Müggelsee (Fig. 1). The ratio of bacterial to phototrophic biomass was approximately 1:3 in Lake Constance, 1:5 in Lakes 111 and Müggelsee and 1:7 in Lake 117. Taking the sum of bacterial and primary production as the energy input into the food web, we observed a trophic gradient with increasing values from Lake 111 over Lakes 117 and Constance to Lake Müggelsee. The ratio of bacterial to primary production was 1:5 in Lakes 117 and Constance but 2:1 in Lake 111. The production-to-biomass ratio (P/B) of bacteria was high in the acidic lakes and low in Lake Constance, whereas the P/B of phototrophs was highest in Lake 117, intermediate in Lake Constance and low in Lakes 111 and Müggelsee (Fig. 1). Thus, the substantial variability in the relative importance of bacteria and autotrophs was only partially linked to pH or trophic state. Fig. 1. Biomass, production and production to biomass ratios of bacteria and phototrophs in two extremely acidic mining lakes (111 and 117), one neutral, meso-oligotrophic lake (Constance) and one neutral, highly eutrophic lake (Müggelsee; n.a. = not analysed). Functional composition of the entire planktonic communities The contribution of bacteria to total planktonic biomass was lower in acidic (6–9%) than in neutral lakes (12– 15%; Fig. 2). The contribution of phototrophic biomass to total plankton biomass was 40–44% in the acidic lakes and Lake Constance, and 57% in eutrophic Lake Müggelsee resulting in H/A ratios of 1.3–1.5 and 0.75, respectively. Phototrophic biomass in acidic lakes consisted of the phototrophic fractions of C. acidophila and Ochromonas sp. (both lakes) and the pigmented, mainly phototrophic Gymnodinium sp. (Lake 117), whereas filamentous cyanobacteria played a major role in Lake Müggelsee. For consumers, approximately 45% of plankton biomass was contributed by osmotrophic C. acidophila 710 U. GAEDKE AND N. KAMJUNKE j PROPERTIES OF LOW- AND HIGH-DIVERSITY PLANKTONIC FOOD WEBS Fig. 2. Composition of total plankton biomass in two extremely acidic mining lakes (111 and 117), one neutral, meso-oligotrophic lake (Constance) and one neutral, highly eutrophic lake (Müggelsee). and phagotrophic Ochromonas sp. in the acidic lakes. The share of heterotrophic protozoa was lowest in Lake 111 (Heliozoa), intermediate in Lake 117 (mainly ciliates) and Lake Müggelsee and highest in Lake Constance. In contrast to Lake 111, where the biomass of the two rotifers E. worallii and C. hoodi was too low (<0.1 mg C L–1) to be included in Fig. 2, a rotifer (Brachionus sericus) and a crustacean (C. sphaericus) contributed a few percent to the total biomass in Lake 117. Crustacean plankton contributed 26–33% to the planktonic biomass of the neutral lakes, whilst the contribution of rotifers remained low. Thus, consumer composition was pH-dependent, whereas H/A ratios depended on the trophic state. Trophic structure and food chain length The first trophic level in the acidic lakes consisted of bacteria, C. acidophila, Gymnodinium sp. (Lake 117) and, most importantly, phototrophic Ochromonas sp. Bacteria contributed more to the first trophic level in Lake Constance than in the acidic lakes (Fig. 3). The second trophic level was dominated by phagotrophic Ochromonas sp. under acidic conditions and by ciliates and crustaceans in Lake Constance. In contrast to the neutral lake, biomass at the second trophic level was almost as high as that at the first trophic level in acidic lakes on seasonal average. Biomass at the third trophic level was extremely small in Lake 111, relatively small in Lake 117 and large in Lake Constance which was the only lake with a well-established fourth trophic level. Accordingly, the average trophic position of the consumers as an indicator of mean food chain length increased from 2.01 in Lake 111 (pH 2.6) and 2.10 in Lake 117 (pH 3.0) to 2.48 in Lake Constance (pH 8). Biomass size spectra and predator–prey weight ratios The plankton biomass size spectra of the acidic lakes exhibited distinct peaks and several gaps, i.e. size ranges where no biomass was detected (Fig. 4). In Lake 111 bacteria, mixotrophic flagellates and Heliozoa were clearly separated in size. The entire plankton size spectrum ranged over six orders of magnitude, which was low compared to the Lake Constance and Lake Müggelsee plankton community (11 orders of magnitude). In Lake 117, Gymnodinium sp. and the ciliates overlapped in size, and Brachionus and Chydorus extended the size spectrum to larger body masses compared with Lake 111. Nevertheless, it remained shorter and more irregular than in the neutral lakes, given the two gaps 711 JOURNAL OF PLANKTON RESEARCH j VOLUME 28 j NUMBER 7 j PAGES 707–718 j 2006 Fig. 3. Trophic pyramids of biomass of the plankton community of Lakes 111, 117 and Constance (seasonal average). For Lake Constance, biomass at the fourth trophic level was underestimated because the quantitative carbon flow diagrams did not account explicitly for piscivorous fish which were at an unnaturally low level due to severe fishing pressure on planktivores (biomass at the fifth and higher trophic levels not shown). within the Lake 117 size spectrum and the extremely high biomass in the size range of the flagellates (Fig. 4). In contrast to the acidic lakes, plankton biomass spectra were continuous, i.e. had no size ranges without detectable biomass, and biomass was more evenly distributed across the size spectrum in Lake Müggelsee and in Lake Constance, in particular. Phytoplankton ranged from autotrophic picoplankton to large forms such as the dinoflagellate Ceratium hirundinella. Protozoa also covered a wide range starting with heterotrophic picoflagellates and ending with large ciliates. Furthermore, the size spectrum for crustaceans was extended because of copepod nauplii at the small end and large carnivorous cladocerans at the other. Overall, plankton biomass stretched continuously over 34–35 log2 size classes in the neutral lakes, whereas it was restricted to 16 and 21 partly disjunctive size classes in Lakes 111 and 117, respectively. A cross-lake comparison of the size distribution of feeding modes revealed similarities in the small size range and substantial deviations for medium and large plankters (Fig. 5). In all lakes, bacteria monopolized the smallest size classes. They covered an extended size range in the acidic lakes and in highly eutrophic Lake Müggelsee but were restricted to a narrow size range in the neutral, oligo-mesotrophic lake where bacterial filaments were less important and autotrophic picoplankton was abundant. Autotrophs were extremely restricted in size in the acidic lakes. In 712 U. GAEDKE AND N. KAMJUNKE j PROPERTIES OF LOW- AND HIGH-DIVERSITY PLANKTONIC FOOD WEBS weight ratios were consistently low, and in some cases extremely low. Quantitatively important feeding interactions were restricted to values of 20 (1:1; Ochromonas : Chlamydomonas), 25 (60:1; Heliozoa : flagellates) and 210–211 (1000–2000:1; Ochromonas : single bacteria and Heliozoa : bacterial filaments, respectively), yielding a trimodal distribution. In Lake Constance, small predator– prey weight ratios (<3:1) contributed considerably less (3%) to total carbon fluxes compared to Lake 111 (21%), whereas high ratios (>3000:1) contributed 3-fold more (36%) than in Lake 111 (11%). The frequency distribution of the predator–prey weight ratios for the Lake Constance planktonic food web was much broader and more regularly shaped owing to the higher number of feeding links. DISCUSSION Choice of lakes The lakes compared in this analysis differed in (i) size, (ii) productivity and (iii) mean acidity. (i) Fig. 4. Sheldon-type plankton biomass size distributions of Lakes 111, 117, Müggelsee and Constance. (ii) contrast, they spanned five orders of magnitude in the neural lakes. In the acidic lakes, bacterivores, herbivores and carnivores partially filled the size range typically covered by autotrophs and did not extend beyond it in Lake 111 (Fig. 5). Therefore, the succession of feeding modes along the size gradient, considered to be one of the outstanding features of pelagic food webs, was roughly maintained in the acidic lake food webs but feeding modes strongly overlapped along a shorter size-spectrum. Considering the size distribution of feeding modes helps to explain the extreme accumulation of biomass in the flagellate size range in the acidic lakes (Fig. 4): here, four feeding modes (osmotrophy, autotrophy, bacterivory and herbivory) co-occur which is unusual for pelagic food webs. The frequency distributions of the predator–prey weight ratios differed greatly between acidic Lake 111 and neutral Lake Constance (Fig. 6). In Lake 111, predator–prey 713 All lakes are sufficiently large and productive to potentially sustain four trophic levels. The volumes of the two acidic lakes were 0.5 106 and 7 106 m3, for which a maximum trophic position of 3.5–4 is predicted by a cross-lake comparison (Post et al., 2000). Furthermore, the differences in diversity are presumably not attributable to differences in lake size, as phytoplankton has a modest exponent in the species–area relationship (0.13; Smith et al., 2005). This suggests that lake size is not a dominant factor determining the food web properties studied. Productivity is unlikely to be the major reason for the absence of a third and fourth trophic level in the acidic lakes. In the acidic lakes, the seasonal mean of production at the first trophic level (i.e. bacterial and primary production) was 20–40 mg C m–3 d–1, which was in the same order as that measured, for instance, in oligotrophic Lake Stechlin where four trophic levels were well expressed (Casper, 1985). Potentially, accumulating biomass at higher trophic levels might be hampered under extreme conditions by enhanced metabolic costs for maintenance at each trophic level. Potentially, building up biomass at higher trophic levels might be hampered under extreme conditions by enhanced metabolic costs for maintenance at each trophic level for example, to maintain the strong gradient of protons and other ions across the cell membrane. This may j JOURNAL OF PLANKTON RESEARCH Phototrophs Osmotrophs Percent VOLUME 28 j NUMBER 7 j Bacterivores PAGES 707–718 j 2006 Carnivores Herbivores 100 Lake 111 0 100 Lake 117 0 100 Lake Müggelsee 0 100 Lake Constance 0 –8 4 fg –6 –4 –2 0 1 pg 2 4 6 8 10 12 1 ng 14 16 18 20 1 µg 22 24 26 28 log2 (body mass) (pg C) 0.25 mg Fig. 5. Size distributions of the relative importance of feeding modes of the planktonic organisms in two extremely acidic mining lakes (111 and 117), one neutral, meso-oligotrophic lake (Constance) and one neutral, highly eutrophic lake (Müggelsee). (iii) reduce the trophic transfer efficiency from one trophic level to the next. However, no enhanced costs were detected for Chlamydomonas acidophila (Gerloff-Elias et al., 2005), rotifers (Weithoff, 2005) and Heliozoa (Bell et al., in press). Two well-studied neutral lakes of different productivity were selected as production is well known to influence pelagic food web structure (Carpenter and Kitchell, 1993). These well-established differences in food web structure and function were used as benchmark to rate the impact of mean acidity. For most attributes studied, differences in food web structure were much larger between acidic and neutral lakes than between neutral waters, despite their greatly deviating trophic state and morphology. Mean acidity remains as the most important difference between lakes, and its major effect was the strong reduction not only in species numbers but also in functional groups including crustaceans. Environmental conditions decreased predatory diversity, in particular, and removed the higher trophic levels selectively. The lakes also differed in respect to mixotrophs, which dominated plankton biomass in the acidic, but not in the neutral lakes. This is, however, of minor importance for the present analysis since the contribution of mixotrophs was proportionally allocated to the osmotrophs, autotrophs or phagotrophs, respectively (for details see Methods). Bacteria and phytoplankton A trophic gradient (measured as primary production) existed across the four lakes, increasing from Lake 111, through Lakes 117 and Constance, to Lake Müggelsee (Fig. 1). This trend from low to high similarly existed for pH, plankton diversity, food chain length and the size range covered by plankton organisms. Primary production in the acidic lakes, where mixotrophs dominate frequently (Nixdorf et al., 1998), was at the lower end of the range observed in many other lakes (Cole et al., 1988). The ratios of bacterial production to primary production were within the typical range (20%; Cole et al., 1988), with the exception of Lake 111 (200%; for discussion see Kamjunke et al., 2005). The P/B of bacteria were relatively high in the acidic lakes and were moderate in Lake Constance. Together with the low contribution of bacteria to total plankton biomass, these high ratios indicate a strong top-down 714 U. GAEDKE AND N. KAMJUNKE j PROPERTIES OF LOW- AND HIGH-DIVERSITY PLANKTONIC FOOD WEBS phototrophs: small cells with high surface to volume ratios occurred in Lake 117, a wide size range was found in Lake Constance and large cyanobacterial colonies dominated in Lake Müggelsee (Nixdorf et al., 1992) within which self-shading further limited production. Functional composition of the entire plankton communities Fig. 6. Predator–prey weight ratios within the planktonic food webs of Lakes 111 and Constance weighted according to the relative contribution of the individual feeding interactions to overall carbon fluxes within the respective food webs. control of bacteria by efficient bacterivores in the acidic lakes. Biomass of single-celled bacteria was negatively correlated with Ochromonas biomass in Lake 111 (Kamjunke et al., 2004), and Ochromonas sp. may increase specific bacterial production (Posch et al., 1999). In contrast, the P/B ratio of phototrophs was extremely low in Lake 111 (Fig. 1). Growth conditions for phototrophs are less favourable in this lake because of the very low epilimnetic concentrations of dissolved inorganic carbon present only as CO2 because of the low pH (Tittel et al., 2005). Even if phototrophs were intensively grazed, they would not escape from bottom-up control. Their in situ growth rates are restricted by CO2, and phosphorus concentrations and underwater light intensity, all of which remain low independent of ambient algal density (Kamjunke et al., 2004; Spijkerman et al. in revision). This resolves the apparent contradiction with cascade theory (Oksanen et al., 1981) by having low (phototrophs) and high (bacteria) P/B ratios at the same trophic level. The P/B ratio of phototrophs decreased from high values in well-illuminated Lake 117 to moderate values in Lake Constance to low ratios in Lake Müggelsee. Among others, this may be explained by the size of the The contribution of phototrophs to total plankton biomass and, thus, H/A was similar in the less eutrophic lakes (111, 117 and Constance) and lower in eutrophic Lake Müggelsee. This implies a strong influence of lake trophic state, and a decrease in the H/A ratio with trophic conditions is well established (e.g. Duarte et al., 2000). It was attributed to decreasing P/B ratios of autotrophs (O’Neill and DeAngelis, 1981) and decreasing importance of allochthonous subsidies (Del Giorgio and Gasol, 1995) with increasing trophy. In Lake 111, the H/A ratio was high as predicted by the lake’s low trophic state, although autotrophic P/B ratios were low. This may be attributed to the high P/B ratios of bacteria providing an important additional food source for the dominant primary consumer, to subsidies from benthic primary production (Kamjunke et al., 2006) and to the low predation pressure on primary consumers. The latter was thought to increase H/A ratios in other lakes as well (Straile, 1998). As predicted, the composition of the consumer community was less influenced by trophic conditions but more sensitive to mean acidity. In neutral lakes, crustaceans dominated but were almost or entirely absent in the acidic lakes. Because body size is positively related to the organizational level, which, in turn, is negatively related to the ability to survive under extreme abiotic conditions, the maximum size of organisms within these lakes declined continuously with decreasing pH. Thus, large, highly organized organisms, represented by crustaceans (and fish) in this study, are lacking at low pH, and this has far-reaching consequences for numerous food web attributes. Lower diversity and an enhanced risk of extinction of species at higher trophic levels because of environmental stochasticity and external stressors, which weaken the top-down control, were also found for other terrestrial and aquatic systems (Duffy, 2002). Trophic structure and food chain length Pelagic systems are well known for comprising four quantitatively important trophic levels (Post et al., 2000) in contrast to terrestrial systems where biomass is typically concentrated in three trophic levels (Hairston and Hairston, 1993). However, in both acidic lakes, consumer 715 JOURNAL OF PLANKTON RESEARCH j VOLUME biomass was concentrated in the second trophic level, and the third level contributed only 0.3 and 5% to the total plankton biomass of Lakes 111 and 117, respectively (Lake Constance: 17% at the third level and >5% at the fourth level; Fig. 3). This high biomass at the second trophic level relative to the first is explicable by the relatively high P/B ratio of the bacteria in Lake 111 and of the bacteria and phototrophs in Lake 117. In contrast, the second trophic level was monopolized by Ochromonas sp., which had an extremely slow turn-over rate (P/B 0.03; Kamjunke et al., 2004) compared with the first trophic level and with plankton organisms in general. Remarkably, the epilimnetic biomass seasonal average at the first trophic level was similar to the sum of the biomass at the other trophic levels in all three lakes (111, 117 and Constance) despite the pronounced differences in food chain length between lakes. In Lake 111, the biomass of Ochromonas sp. that monopolized the second trophic level accumulated up to relatively high values. The extremely low P/B values indicate low loss rates. This agrees with the lack of efficient metazoan grazers and the observation that Ochromonas seems to be a poor food source in laboratory cultures for its potential predators (rotifers and heliozoans; Weithoff, 2004; Bell et al., 2006). The latter may explain why Ochromonas biomass accumulates also in Lake 117 even though larger consumers (Brachionus and Chydorus) occur, albeit at low densities. In contrast, in Lake Constance, consumers are themselves subject to high predatory losses (Gaedke et al., 2002), which decrease their biomass down to a level where losses are counterbalanced by sufficiently high P/B ratios but enable substantial biomass accumulations at the proceeding trophic level. To conclude, the near absence of a third trophic level under acidic conditions was attributable to the lack of predators capable of exploiting the production at the second level efficiently, rather than to a lack of sufficient energy to sustain another trophic level and/or to the small size of the water bodies (Post et al., 2000). Biomass size spectra and predator–prey weight ratios Biomass size spectra represent an ataxonomic approach enabling a comparison of the structure and energetics of taxonomically strongly deviating pelagic food webs using the relationship between an organism’s size and its physiological and ecological properties (Sheldon et al., 1972; Platt and Denman, 1978; Borgman, 1982; Gaedke, 1993). The extended size ranges in the size spectra of the acidic lakes where no organisms were detected illustrate that major functional types were absent: autotrophic picoplankton, heterotrophic flagellates, larger 28 j NUMBER 7 j PAGES 707–718 j 2006 phytoplankton and crustaceans were lacking in Lake 111, and ciliates and rotifers were extremely rare. In addition, even those functional groups present in the food web were often only represented by one species. Poorly exploited resources are thought to attract more efficient users, which in turn favours a more efficient exploitation of available resources and decreases ‘ecological monopolies’ (Leigh and Vermeij, 2002) such as the monopolizing position of Ochromonas. The low plankton diversity observed in the acidic lakes may be attributable to biotic interactions such as competition and to abiotic constraints (Kamjunke et al., 2004), and potentially to the rarity and isolation of such habitats and their low age (50 years). However, old natural acidic lakes of volcanic origin exhibit no higher plankton diversity (Pedrozo et al., 2001). The overall regularity in pelagic food webs of having osmotrophs in the smallest size classes followed by autotrophs was maintained in the acidic lakes. However, the second and, where present, third trophic levels in Lake 111 occurred at a point on the planktonic size-spectrum where phytoplankton dominated in the neutral lakes. Similarly, the consumers in Lake 117 remained small. Thus, the flow of matter and energy from small to large organisms was truncated in the acidic lakes. Remarkably, the slight increase in pH from Lakes 111 to 117 (pH 2.6 and 3.0) and the reduction in ion concentrations (150 and 23 mg Fe L–1) was immediately reflected in a considerably greater size range of extant planktonic organisms [Lake 111, 5.7; Lake 117, 8.7 and Lakes Constance and Müggelsee, 10.5 (with fish 16.8) orders of magnitude, respectively] but less in the trophic pyramid. The third trophic level was still weakly represented in Lake 117 since the biomass of larger organisms was very low. The predator–prey weight ratios were similar in Lakes Constance and 111 at the lower end of the size gradient (bacterivores) but were extremely small at larger prey sizes in Lake 111. This change with size in predator–prey weight ratios coincided with that of P/B ratios, which were normal to high for small organisms (bacteria) and extremely low for flagellates. It suggests that the presence of the strong predator–prey interactions, characteristic of numerous pelagic food webs (Cyr and Pace, 1993), declined with size in the acidic lakes and confirms the prediction that food web traits dominated by microorganisms were less affected by the extreme environmental conditions than those ruled by metazoans. ACKNOWLEDGEMENTS We thank Camilla Beulker, Brigitte Nixdorf and the Special Research Programme ‘Cycling of Matter in Lake Constance’ (SFB 248) for providing data, and Rita Adrian 716 U. GAEDKE AND N. KAMJUNKE j PROPERTIES OF LOW- AND HIGH-DIVERSITY PLANKTONIC FOOD WEBS Gaedke, U. and Straile, D. (1997) The trophic position of dead autochthonous organic material and its treatment in trophic analysis. Environ. Model. Assess., 2, 13–22. for data and for information on the feeding modes of planktonic organisms in Lake Müggelsee. Data handling was supported by Katrin Tirok and Stefan Saumweber. Special thanks to Guntram Weithoff and Jörg Tittel who provided valuable background information and stimulating discussions and to Elly Spijkerman, Jörg Tittel and Elanor Bell for improving the manuscript. This paper is based on research project no. 0339746 of the Federal Ministry of Education and Research (BMBF) of Germany. Gasol, J. M., Guerrero, R. and Pedros-Alio, C. 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