Benthic algae support zooplankton growth during winter in aclear-water lake

Jan Karlsson and Christin Sawstrom

J. Karlsson (jan.karlsson@emg.umu.se) and C. Sawstrom, Climate Impacts Research Centre (CIRC), Dept of Ecology and EnvironmentalScience, Umea Univ., Box 62, SE�981 07 Abisko, Sweden.

We used stable carbon (d13C) and nitrogen (d15N) isotopes to assess the importance of benthic algae for the zooplanktonindividual growth in winter in a shallow, clear subarctic lake. The d13C values of calanoid (Eudiaptomus graciloides) andcyclopoid (Cyclops scutifer) zooplankton in autumn suggest a food resource of pelagic origin during the ice-free period.The zooplankton d13C values were high in spring compared to autumn. E. graciloides did not grow over winter and thechange in d13C was attributed to a decrease in lipid content during the winter. In contrast, the increase in d13C values ofC. scutifer over the winter was explained by their growth on organic carbon generated by benthic algae. The d15N of theC. scutifer food resource during winter was low compared to d15N of the benthic community, suggesting that organicmatter generated by benthic algae was mainly channelled to zooplankton via 15N-depleted heterotrophic bacteria. Theresults demonstrate that benthic algae can sustain zooplankton metabolic demands and growth during long winters,which, in turn, may promote zooplankton growth on pelagic resources during the summer. Such multi-chain omnivorychallenges the view of zooplankton as mainly dependent on internal primary production and stresses the importance ofbenthic resources for the productivity of plankton food webs in shallow lakes.

Classical food web theory regards pelagic food webs in lakesas simple food chains based on phytoplankton production.This view has been challenged recently in a variety of lakesby the recognition of multi-chain omnivory, wherebypelagic consumers are subsidized by resources generated inadjacent habitats and ecosystems (Vander Zanden andVadeboncoeur 2002, Jansson et al. 2007). These cross-system linkages may affect the cycling of nutrientsand energy (Polis et al. 1997) and ultimately the structureand function of lake food webs by stabilizing food webs andaffecting the strength of trophic cascades (Polis et al. 2000,Vadeboncoeur et al. 2005).

It has been suggested that multi-chain omnivory couldexplain relatively high production in pelagic food webs ofunproductive lakes. Terrestrial organic matter has beenshown to constitute an important source of carbon andenergy for pelagic organisms, including heterotrophicbacteria, metazoan zooplankton and fish (Grey et al.2001, Karlsson et al. 2003, Carpenter et al. 2005). Aspecial feature of many nutrient-poor lakes is the highproduction of benthic algae which, in clear shallow lakescan consitute up to 90% or more of lake primaryproduction (Bjork-Ramberg and Anell 1985, Vadebon-coeur et al. 2003, Ask et al. 2009). Fish rely to a large extenton benthic primary production in these lakes through theirexploitation of benthic prey organisms (Vander Zanden andVadeboncoeur 2002, Karlsson and Bystrom 2005). How-ever, the importance of benthic algae for plankton food

webs is largely unknown. Heterotrophic bacterioplanktoncan grow on organic matter (OM) generated by benthicalgae (Hopkinson et al. 1998, Kamjunke et al. 2006),thereby providing a carbon subsidy for protozoan andmetazoan zooplankton that consume bacterial-generatedcarbon. Further, crustacean zooplankton can consumebenthic OM by grazing directly in the sediment or onfilaments in the water (Hansson and Tranvik 2003, Rautioand Vincent 2007). It has been suggested that benthicresource use can explain high zooplankton biomass in highlatitude shallow ponds (Rautio and Vincent 2006), butstable isotopic data has failed to confirm this duringsummer in subarctic and arctic lakes (Karlsson et al.2003, Rautio and Vincent 2007).

A special characteristic of lakes at high latitudes is longwinter periods with low input of allochthonous OM and,due to the thick ice cover and the low solar radiation, lowphotosynthetic activity. Still, zooplankton can persist atrelatively high biomass and abundance during winter and,in Antarctic lakes, this has been suggested to result from useof fat reserves or from grazing on phytoplankton that areadapted to low light climate (Laybourn-Parry and Marchant1992, Henshaw and Laybourn-Parry 2002). However, inregions with high snow accumulation, photosynthesisduring long winter periods is not possible. Rather it appearsthat the high production by benthic algae in summer partlyaccumulates and can support a significant winter metabo-lism in shallow clear-water lakes (Karlsson et al. 2008). The

Oikos 118: 539�544, 2009

doi: 10.1111/j.1600-0706.2008.17239.x,

# 2009 The Authors. Journal compilation # 2009 Oikos

Subject Editor: Beatrix Beissner. Accepted 10 November 2008

539

main portion of the benthic algae is likely to be utilizeddirectly in the benthic food web. However, since primaryproduction can be an order of magnitude higher in thebenthic over the pelagic habitat in clear-water shallow lakes(Bjork-Ramberg and Anell 1985, Ask et al. 2009), somefraction of the benthic algae production could stillconstitute an important food source for zooplankton.

We analyzed crustacean zooplankton size and stableisotopic composition in early and late winter in a subarcticlake in order to test the hypothesis that benthic algaesupport zooplankton growth during the winter period. Thelake is clear and shallow, which results in extensive benthicalgae mats across all lake depths. The benthic algae has ahigh carbon isotopic signature (d13C) compared to pelagicfood sources in the lake (Karlsson and Bystrom 2005,Bystrom et al. 2007) and this will make it possible to detectif benthic algae is supporting the growth of zooplanktonduring the long winter in this lake.

Material and methods

Study lake

We studied Lake 6 (according to the nomenclature inKarlsson and Bystrom 2005), a small (lake area: 0.05 km2)and shallow (mean depth: 1.7 m, max depth: 4.4 m) lakesituated (68810?18ƒN, 19849?34ƒE, 445 m. a.s.l.) in thebirch forest in subarctic northern Sweden. The benthichabitat consists of a rocky nearshore region (0�1 m) andsoft-bottom sediments, with associated mats of algae, atdeeper depths (1�4.4 m). Studies of other clear shallowlakes in the region show that benthic algae constitute80�95% of whole lake primary production (Bjork-Rambergand Anell 1985, Ask et al. 2009). The lake had a permanentice cover between the middle of October 2006 and late May2007. The fish community consists of invaded adultnorthern pike (Esox lucius), resulting in a very low predationpressure on crustacean zooplankton (Bystrom et al. 2007,Bystrom and Karlsson unpubl.).

Sampling and analysis

The lake was sampled from ice in autumn (28 November2006) and spring (7 April 2007). Water samples (1 l) werecollected with a Ruttner sampler from 1 and 4 m depth atthe deepest (4.4 m) point in the lake for analyses ofdissolved organic carbon (DOC), nutrients (Tot-P, MRP,Tot-N, NH4

�, NO3�), dissolved inorganic carbon (DIC)

and bacterioplankton production (BP). Water was passedthrough a preignited (4008C, 3 h) GF/F filter fordetermination of dissolved nutrients and DOC (one sampleper depth and date). For DOC the filtrate was acidified andstored cold until analysis on a Shimadzu TOC analyzer.Sub-samples of 50 ml of filtered and unfiltered water werefrozen for later analysis of nutrients at the department ofLimnology, Uppsala Univ. Molybdate reactive phosphate(MRP) was analyzed according to Murphy and Riley(1962). Tot-P was analyzed as above after oxidativehydrolysis with potassium peroxodisulphate. NH4-N was

determined by the indophenol method (Grasshoff et al.1983). NO3-N was determined, after reduction of NO3-Nwith Cd (Grasshoff et al. 1983). Tot-N was obtained afteranalyzing Kjeldahl-N (Jonsson 1966). The bacterioplank-ton production was determined (three samples per depthand date) by the leucine incorporation method (Smith andAzam 1992) according to a slightly modified proceduredescribed by Karlsson et al. (2001). For estimating the DICconcentration 5 ml of lake water was injected (one sampleper depth and date) into a 22 ml exetainer containingnitrogen gas and CO2-free HCL. During each samplingoccasion exetainers containing DIC standard solutions ofthree different concentrations (three replicates per concen-tration) were also prepared as above. The samples wereshaken for 1 min and then left to stand for 12�18 h forequilibration of CO2 between air and water. The CO2 inthe headspace of the exetainers were analysed using a gaschromatograph (equiped with a headspace sampler). TheDIC concentrations in the lake water samples werecalculated from the relationship between the amount ofCO2 in the headspace and the DIC concentration of thestandard solutions.

Crustacean zooplankton were collected with a verticalhaul through the water column at the deep location using aplankton net with a mesh size of 100 mm. In the laboratory,animals were counted and measured for total length (notincluding caudal setae, McCauley 1984) using an invertedmicroscope. Zooplankton for analysis of carbon (d13C) andnitrogen (d15N) isotopic signatures were stored in 0.2 mmfiltered lake water for gut evacuation between 10�15 h andthen separated (one sample per date, 200 to 400 individualsper species) into the dominant metazooplankton speciesEudiaptomus graciloides (calanoid copepod, filter feeder) andCyclops scutifer (cyclopoid copepod, raptorial feeder). Thezooplankton (� 150 individuals per species, three samplesper date) were also dried (658C) and weighed. The benthiccommunity, containing algae and heterotrophic organisms(e.g. bacteria, ciliates and rotifers), were collected from softsediments at 1.5, 3 and 4.4 m depths, using a sediment coresampler, and gently scraping the surface (0�0.5 cm) algaeinto a container. The d13C and d15N signatures of thebenthic community show small variability within andbetween years (Karlsson and Bystrom 2005, Bystromet al. 2007) and we used values of the benthic communitysampled in August 2005. The zooplankton and benthiccommunity samples were dried (658C) prior to isotopicanalyses. For analysis of d13C and d15N signatures ofdissolved (DOM) and particulate (POM) OM, watersamples (10 l) were collected with a Ruttner sampler fromthe middle of the water column at the deep (4.4 m) and at ashallow (2 m) location. DOM and POM were extractedfrom the lake water (one sample per depth and date) bytangential flow ultrafiltration (0.2 mm), acidified and freeze-dried before isotopic analysis. The analysis of stable isotopicand elemental ratios of carbon and nitrogen were carriedout at the Dept of Geology and Geochemistry, StockholmUniv. The results are expressed using the d notation in permil (�) as d�(Rsample/Rstandard � 1)�1000, whereR�13C/12C or 15N/14N. The analytical precision of theisotopic analysis was better than 0.2�.

540

Calculations

Lipids are depleted in 13C relative to proteins andcarbohydrates (DeNiro and Epstein 1977) and variationin lipid content causes variation in d13C of zooplankton.Lipids are composed mainly of carbon and the C:N ratio ofanimals is strongly correlated to their lipid content (Postet al. 2007). The d13C of zooplankton was normalized(d13Cnormalized) for lipid concentration using the carbon tonitrogen ratio (C:N) following Post et al. (2007):

d13 Cnormalized � d13 C�3:32�0:99�C:N (1)

From the changes in stable isotopic composition ofzooplankton between autumn and spring we estimatedthe isotopic composition of the food source supporting thezooplankton growth during winter. Metabolic turnover ofbody carbon in ectotherms is very slow and growthcompletely dominates the change in consumer isotopiccomposition after a diet shift (Fry and Arnold 1982, Frazeret al. 1997, Herzka and Holt 2000). CO2 uptake by benthicalgae is diffusion limited resulting in low 13C discrimina-tion and higher d13C values than in phytoplankton (Heckyand Hesslein 1995). Thus, a switch from pelagic to benthicOM supporting zooplankton growth in winter will result ina change of zooplankton isotopic composition. The d13Cand d15N of the food source (dfood) supporting thezooplankton growth in winter was estimated as:

dfood � (Wspring�dspring�Wautumn�dautumn)=(Wspring

�Wautumn)�TF (2)

where Wspring and Wautumn are the average weight of thezooplankton in spring and autumn, dspring and dautumn arethe d13Cnormalized or d15N signature of the zooplankton, andTF is the trophic fractionation between consumer and diet.The TF was taken from Post (2002) which report a mean(9 1 SD) TF of �0.10 (9 0.96) for d13C and 3.42(9 0.99) for d15N for aquatic systems. The effect of thevariability in TF on the dfood was tested by performing thecalculation (Eq. 2) with the variability in TF reported byPost (2002).

Results

There were substantial spatial and temporal differences innutrient concentrations in the lake water (Table 1). Theconcentration of Tot-P and Tot-N were high at deeprelative to shallow depths. Both Tot-N and DIN (NH4

�,NO3

�) concentrations were high in spring compared toautumn, for NO3

� at shallow water depth and for NH4� at

deep water depth. The DIN:Tot-N ratio was 0.26 inautumn and 0.58 in spring (average of both water depths).

The DOC concentration was lower in spring compared toautumn and higher at deep compared to shallow waterdepths in spring. The DIC concentration showed highvalues at deep compared to shallow water depths and inspring compared to autumn. The bacterioplankton produc-tion (BP) was slightly higher in autumn compared to springand at deep compared to shallow water depths (Table 1).

The d13C and d15N values (mean91 SD) of lake waterDOM were �27.690.6� and 1.090.3�, respectively, inautumn, and �25.790.2� and 0.590.1�, respectively,in spring (Fig. 1). The d13C and d15N of POM were�24.990.2� and 0.490.7�, respectively, in autumn,and �25.491.1� and 0.690.9�, respectively, in spring.The d13C and d15N values of the benthic community weresimilar at 1.5 m (�19.7�, �1.0�), 3 m (�19.1�,�1.4�) and 4.5 m (�21.3�, �1.9�). Both E. graciloidesand C. scutifer had high d13C values in spring (�31.8� and�27.4� respectively) compared to autumn (�35.7� and�30.7� respectively) and low d15N values in spring (2.8�and 1.7� respectively) compared to autumn (4.3� and4.4� respectively) (Fig. 1).

The weight (t-test, p�0.190) and length of E. graciloideswas similar in autumn and spring while the weight (t-test,pB0.001) and the minimum, maximum and mean lengthof C. scutifer increased from autumn to spring (Table 2). Theabundance of E. graciloides decreased over winter while theabundance of C. scutifer was similar in autumn and spring(Table 2). The C:N ratio (by weight) of E. graciloides was10.2 and 4.9 and of C. scutifer 4.9 and 5.4 in autumn andspring, respectively (Table 2). The decrease in C:N ratiosuggest a decrease in lipid content, and thus an increase ind13C, of E. graciloides during winter (Post et al. 2007).Accordingly, lipid-normalized d13C of E. graciloides wassimilar in autumn (�28.9�) and spring (�30.3�). Incontrast, the C:N ratio of C. scutifer increased slightlyand the d13Cnormalized was considerably higher in spring(�25.3�) compared to autumn (�29.2�), showing thatloss of lipids was not responsible for the increase in d13Cover the winter. The d13C and d15N of the food sourcecontributing to the individual biomass production of C.scutifer in winter was estimated to �19.5� and �5.7�,respectively, which were clearly different from the d13C andd15N of the estimated food source in summer (Fig. 1).

Discussion

The data provide evidence of multi-chain omnivory,whereby support of the growth of the cyclopoid zooplank-ton (Cyclops scutifer) in the lake changed from dominanceby pelagic food resources in summer to a dominance by

Table 1. Data from 1 and 4 m depth at the deepest location (4.4 m) of the lake in autumn 2006 and spring 2007. The bacterioplanktonproduction (BP) is shown as mean (including SE) of three replicate samples. n.a.�not analysed.

Season Depth(m)

T(8C)

DOC(mg l�1)

DIC(mg l�1)

Tot-P(mg l�1)

MRP(mg l�1)

Tot-N(mg l�1)

NO3�

(mg l�1)NH4

�

(mg l�1)BP

(mg C l�1 d�1)

Autumn 1 4.0 4.5 3.9 n.a. 0.1 154 24 9 1.6 (0.1)4 5.0 4.6 5.0 n.a. 1.7 205 19 45 2.0 (0.1)

Spring 1 2.0 3.2 7.0 2.6 0.0 180 104 24 1.2 (0.1)4 4.2 4.0 9.7 4.4 0.1 263 19 101 1.6 (0.1)

541

benthic algae in winter. The d13C values of zooplankton inautumn are in line with findings from other lakes in theregion, and suggest that zooplankton food resources duringthe summer period contained a mixture of autotrophicphytoplankton (assumed to be in the range of �43 to�37�) and allochthonous OM (�27.2�) imported fromthe catchment (Karlsson et al. 2003). The change in d13Cvalues of zooplankton over winter (Fig. 1) was towards d13Cvalues for allochthonous OM and the benthic community.For Eudiaptomus gracioides this change could be explainedby the loss of 13C-depleted lipids (DeNiro and Epstein1977, Post et al. 2007) during the winter. For C. scutifer,however, the increase in d13C must be a result of growth ona food resource rich in 13C compared to the summer foodresource. From the over-winter increase in C. scutifer weightand d13C values we calculated a d13C of the zooplanktonfood during the winter period to be �19.5�, which isclose to the d13C of the benthic community in the lake (Fig.1). The high d13C of the benthic community is a result ofhigh production of 13C-enriched organic carbon (OC) bybenthic algae and low accumulation of 13C-depleted pelagicOC in the sediments of this shallow clear-water lake(Karlsson and Bystrom 2005, Karlsson et al. 2008). Thus,the change in d13C of C. scutifer over winter was the resultof their growth being predominately supported by organicmatter generated by benthic algae.

Our data suggest that the OM generated by benthicalgae was to a large extent transferred to C. scutifer viabacteria. Since copepods are unable to ingest bacteriadirectly, the transfer probably occurred via bacterial

consumers such as flagellates, ciliates and rotifers (Stocknerand Porter 1988, Bern 1994). The d15N values of the foodresource supporting the growth of C. scutifer during thewinter period were 5.7� lower compared to the meand15N value of the benthic community (Fig. 1). Thesedifferences were consistent even when considering the rangein typical values of trophic fractionation between consumersand their diet (Fig. 1). On the contrary, the lowtemperature in winter (Table 1) is expected to promotehigh d15N trophic fractionation (Power et al. 2003). Thus,the d15N data clearly show that C. scutifer were feeding on afood source strongly depleted in 15N compared to thebenthic algae during the winter period (Fig. 1). Bacteriahave been shown to discriminate up to around 10� against15N when the availability of nitrogen is high compared tothe bacterial demand (Hoch et al. 1994, Hopkinson et al.1998). We found an accumulation of DIN in the lake waterduring the winter (Table 1), suggesting high mineralizationof organic matter in the lake. Probably the high DINavailability in winter caused relatively high 15N discrimina-tion during nitrogen uptake by bacteria which, in turn,facilitated low d15N of the bacterial-based food web. Highbacterial activity on benthic OM during the winter issupported by the accumulation of DIC in the lake water(Table 1). The DIC accumulation in the lake water betweenautumn and spring averaged 3.9 mg l�1 and was higher atdeep compared to at shallow depths (Table 1). There wasonly a small decrease in lake water DOM concentrationduring the study period, implying that decomposition ofthe lake water DOM pool present in autumn could notexplain the DIC accumulation over the winter. Also, theinput of allochthonous DOM and the autochthonousproduction of new DOM are expected to be very low orabsent in winter. Thus, the DIC accumulation is presum-ably a result of decomposition of benthic OM in the lakeduring the winter period.

The data also suggest that part of the bacterial use ofOM generated by benthic algae occurred in the watercolumn and that this was the main pathway by whichbenthic algae supported the growth of zooplankton duringthe winter. Similar to zooplankton, the d13C of DOM alsochanged during winter (Fig. 1) and this resulted in higherd13C values of DOM in spring (�25.7�) than found inlakes of the region during summer (�27.7� to �29.9�,Karlsson et al. 2003). Although we can not excludediagenetic effects on the d13C of DOM, it is likely thatpart of the change in d13C is an effect of input of benthicOM to the lake water. Pelagic bacteria have been shown tobe able to efficiently exploit OM released from benthicalgae (Hopkinson et al. 1998, Kamjunke et al. 2006).Accordingly, the bacterioplankton production was unex-pectedly high in spring (Karlsson et al. 2001) despite a longpreceding winter without production of new DOM.

-9

-6

-3

0

3

6

-38 -34 -30 -26 -22 -18δ13C (‰)

δ15N

(‰

)

E. graciloides C. scutifer

DOM

Winter foodC. scutifer

Benthic communitySummer foodE. graciloides

Summer foodC. scutifer

Figure 1. Stable carbon (d13C) and nitrogen (d15N) isotopiccomposition of the calanoid (E. graciloides) and cyclopoid (C.scutifer) zooplankton, the calculated zooplankton food resources(9 1SD) during summer and winter (C. scutifer only), thedissolved organic matter (DOM91SD) of the lake water, and thebenthic community (9 1SD). The arrows show the change instable isotopic values from autumn 2006 to spring 2007.

Table 2. Data on C:N ratio, d13C, d15N, mean (min-max) length, individual mean dry weight (including standard error) and abundance ofzooplankton at the deepest location (4.4 m) of the lake in autumn 2006 and spring 2007.

Species Season C:N d13C (�) d15N (�) Length (mm) Weight (mg) Abundance (no. m�2)

E. graciloides autumn 10.2 35.7 4.3 1.125 (1.05�1.20) 8.7 (0.2) 9996spring 4.9 31.8 2.8 1.130 (1.05�1.20) 9.1 (0.2) 5704

C. scutifer autumn 4.9 30.7 4.4 0.893 (0.70�1.30) 2.2 (0.1) 11304spring 5.4 27.4 1.7 1.153 (1.00�1.50) 3.7 (0.2) 10838

542

Assuming a bacterial growth efficiency between 0.05 and0.2 (Jansson et al. 2008) gives a bacterial respiration (0.9and 4.3 mg l�1, respectively) during the sampling periodequivalent to between 23 and 110% of the accumulatedDIC in the lake water. Thus, the data suggest that OMfrom benthic algae were released to the water column whereit was assimilated by bacteria, thus being made available foruse by higher trophic levels. Although we sampled thezooplankton in the water column, the zooplankton couldhave performed frequent vertical migrations betweenbenthic and pelagic habitats, or spent parts of their lifecycle in the benthic habitat (Gyllstrom and Hansson 2004).Analysis of surface sediment (0.02 m2, n�125) from thelake before ice-off in spring 2004 revealed copepods inthe benthic habitat (Karlsson and Bystrom unpubl.), butthe biomass was only 0.2 mg m�2 which is negligible(0.2%) compared to the zooplankton biomass found in thelake water during the winter. Thus, these data suggest thatthe benthic OM was mainly exploited by zooplankton viafeeding in the sediment�water interface or in the open watercolumn, rather in the sediments.

Our data may explain the apparently low importance ofbenthic algae for plankton food webs in summer (Karlssonet al. 2003, Rautio and Vincent 2007), despite the fact thatprimary production can be an order of magnitude higher inthe benthic compared to in the pelagic habitat in these lakes(Bjork-Ramberg and Anell 1985, Karlsson et al. 2008). Thedata suggested that benthic algae were mainly transferred toC. scutifer via release of DOM and subsequent assimilationand growth of heterotrophic bacterioplankton. Thus, eventhough benthic algae constitute the largest food resource inthe lake, the supply of benthic DOM to the pelagic habitatis probably low compared to phytoplankton productionand the input of allochthonous OM during the summer(Fig. 1). Consequently, the zooplankton species utilizingbenthic algae via a DOM�bacteria�bacterivore pathway arelikely to depend to a lower extent on this food sourcerelative to other food sources in summer than in winter.

The results suggest that multi-chain omnivory, throughthe exploitation of food chains based on both pelagic andbenthic resources, is important in plankton food webs, aspreviously reported for various fish species (Vander Zandenand Vadeboncoeur 2002, Karlsson and Bystrom 2005).Thus, the classical view of plankton food webs inunproductive lake ecosystems as simple food chainssupported by phytoplankton production is challenged bythe recognition of multi-chain omnivory via resourceexploitation of energy sources generated both in adjacentecosystems (terrestrial) and habitats (benthic). The changein zooplankton resource use from pelagic resources insummer to benthic algae in winter were probably promotedby the lake being clear and shallow, resulting in highproduction by benthic algae (Hansson 1992, Ask et al.2009). Although this has not been shown before, it has beensuggested that benthic algae can serve as a food source forzooplankton in winter in clear-water lakes (Gibson et al.1998). In deeper and more coloured lakes benthic algae areof lower importance for whole lake primary production andconsequently, for plankton metabolism. However, it islikely that profundal OM supports plankton food webs inmore humic-rich shallow lakes, although this will notalways be possible to trace with stable carbon isotopes. It

must be stressed that the majority of benthic OM utilizationby bacteria, and its transfer to higher trophic levels,probably occurs directly in the sediments (i.e. to zoo-benthos). Still, export and use of a small portion of benthicprimary production in winter could have a substantial effecton the plankton food web. The support of zooplanktonmetabolism by benthic algae may facilitate a relatively highbiomass of these species in winter, and especially so inshallow, clear-water lakes with high benthic primaryproduction in summer. Further, winter exploitation ofbenthic algae produced in the previous summer may notonly sustain zooplankton metabolic demands and growthduring long winter periods but also promote zooplanktongrowth on pelagic resources the next summer. As aconsequence, benthic subsidies could be expected to haveadditional effects on the structure and dynamics of pelagicfood webs in summer.

Acknowledgements � We thank Heike Siegmund and MagnusMorth for the stable isotopic analyses. This study was financiallysupported by the Climate Impacts Research Centre (CIRC), UmeaUniv.

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