RESEARCH ARTICLE

Altered energy flow pathways in a lake ecosystem followingmanipulation of fish community structure

Jari Syvaranta • Pia Hogmander • Tapio Keskinen •

Juha Karjalainen • Roger I. Jones

Received: 8 April 2010 / Accepted: 16 August 2010 / Published online: 28 August 2010

� Springer Basel AG 2010

Abstract We used carbon and nitrogen stable isotope

analyses to assess the relative contributions from pelagic

and littoral energy sources to higher trophic levels in a lake

ecosystem before and after a major food web perturbation.

The food web structure of the lake was altered when the

population sizes of the most abundant fish species (small

perch, roach and bream) were reduced during an attempt to

improve water quality by biomanipulation. Fish removal

was followed by dense year classes of young fish, which

subsequently increased the utilisation of pelagic resources.

This was reflected as a decrease in relative energy contri-

bution from littoral sources and also led to more distinct

pelagic and littoral food chains after fish removal. Com-

munity metrics calculated from stable isotope data

indicated increased trophic diversity and occupied niche

area, and reduced trophic redundancy in the food web.

However, only minor changes were observed in fish trophic

positions, although roach and pike occupied slightly lower

trophic positions after fish removal. Despite the Jyvasjarvi

ecosystem becoming more dependent on pelagic energy

after fish removals, the littoral energy contribution was still

substantial, particularly to certain fish species. Hence, our

results support recent arguments for the importance of

benthic production in lake ecosystems. More generally, our

results illustrate how large-scale perturbations of food web

structure can alter energy flow patterns through an entire

ecosystem.

Keywords Fish removal � Food web � Littoral �Pelagic � Stable isotopes � Trophic cascades

Introduction

Studies of lake ecosystems have traditionally emphasised

the importance of pelagic primary production over benthic

production. However, some studies have argued greater

importance of littoral (benthic) production in supporting

higher trophic levels in lakes (Hecky and Hesslein 1995;

Vander Zanden and Rasmussen 1999; Vander Zanden and

Vadeboncoeur 2002). The contribution of benthic produc-

tion to a whole lake ecosystem depends on many lake-

specific factors such as lake area and morphometry, but also

on lake trophic state, with benthic production becoming less

important with increasing eutrophy and decreasing water

clarity (Vadeboncoeur et al. 2001; Vadeboncoeur et al.

2003).

The relative contributions from benthic and pelagic

primary production to higher trophic levels are also likely

to depend on the species composition and size structure of

the fish community, which can generate both interspecific

and intraspecific competition for available food resources.

In many North European lakes, perch (Perca fluviatilis L.)

and roach (Rutilus rutilus L.) are common species that

compete for food resources (Persson 1986; Persson et al.

1999). Roach is generally considered a superior competitor

for pelagic zooplankton (Persson 1987), whereas perch has

the competitive advantage in the more structured littoral

zone (Persson 1991; Winfield 1986). Moreover, these

species undergo marked ontogenetic shifts in diet from

J. Syvaranta (&) � P. Hogmander � T. Keskinen �J. Karjalainen � R. I. Jones

Department of Biological and Environmental Science,

University of Jyvaskyla, PO Box 35, 40014 Jyvaskyla, Finland

e-mail: jari.syvaranta@jyu.fi

J. Syvaranta

Department of Biology and Ecology of Fishes, Leibniz-Institute

of Freshwater Ecology and Inland Fisheries,

Muggelseedamm 310, 12561 Berlin, Germany

Aquat Sci (2011) 73:79–89

DOI 10.1007/s00027-010-0161-8 Aquatic Sciences

early dependence on zooplankton to progressively greater

diet diversification with increasing size. Perch is a rather

strict carnivore that switches to feeding on littoral macro-

invertebrates and at still larger sizes can switch to

piscivory, while roach is considered more of a generalist

feeder, utilising both plant and animal food (Persson 1983).

Typically the fish community of these lakes may also

contain more specialist benthivores such as bream (Abr-

amis brama L.), specialist planktivores such as smelt

(Osmerus eperlanus L.), as well as littoral piscivores such

as pike (Esox lucius L.) and more open water piscivores

such as zander (Sander lucioperca L.). However, strick

classification to a certain feeding behaviour is not always

desirable and, for example, bream can sometimesalso be

well adapted to planktivory (Van den Berg et al. 1994).

The implications of large-scale food web perturbations

for energy flow patterns and trophic structures in entire

lake ecosystems have not been thoroughly investigated,

probably because of the amount of work needed to cate-

gorise ecosystem properties and processes by conventional

methods. Stable isotope analysis (SIA) potentially provides

more economical and integrative measures of ecosystem

properties, and has proved particularly useful for assessing

the relative importance of littoral and pelagic production in

lake ecosystems. Changes in the ratios of heavy to light

isotopes (13C/12C and 15N/14N, expressed relative to a

standard as d13C% or d15N%) can occur at each trophic

step because of fractionation of isotopes between animals

and their diet during assimilation or excretion (Peterson

and Fry 1987). Carbon fractionates less between trophic

steps and has proven particularly useful for distinguishing

the contributions of different food sources, whereas nitro-

gen fractionates to a greater extent and has been widely

used to define trophic positions of organisms (DeNiro and

Epstein 1978; Minagawa and Wada 1984; Peterson and Fry

1987). Boundary layer effects on inorganic carbon avail-

ability produce differences between phytoplankton and

periphyton photosynthesis in carbon isotope fractionation

(Hecky and Hesslein 1995). Hence pelagic and littoral

energy sources in lakes typically have distinct isotope

signatures (France 1995; Vander Zanden and Rasmussen

1999; Post 2002; Vander Zanden and Vadeboncoeur 2002),

so that the isotope ratios in consumers can be used to assess

the relative contributions from these different energy

sources to higher trophic levels.

Lakes are good model systems to test effects of food

web perturbations, since lake ecosystems have rather

clearly defined boundaries and their food web structure is

relatively easy to alter. Indeed, attempts at lake restoration

by biomanipulation are excellent examples of major eco-

system food web perturbations (Carpenter and Kitchell

1993) and as such they can offer valuable general insights

into ecosystem responses to food web perturbations (Pace

et al. 1999). We used carbon and nitrogen stable isotope

analyses to evaluate changes in lake ecosystem structure

during mass fish removal under a biomanipulation pro-

gramme in Lake Jyvasjarvi, central Finland, and especially

the effect of this food web perturbation on the relative

contributions of production from different sources to higher

levels in the food chain. The removal of fish during bi-

omanipulation can be expected to alter the population

structure of many fish species toward greater abundance

of younger individuals, thereby promoting predation on

zooplankton and reliance on pelagic energy sources. Fur-

thermore, substantial removal of generalist feeders, such as

roach, can also be expected to reduce the linkage between

pelagic and littoral energy flow, leading to more distinct

energy pathways and trophic structures. We tested these

expectations using stable isotope mixing models (SIAR),

and by using community-wide metrics calculated from

stable isotope data to characterise possible changes in the

food web structure of the lake.

Materials and methods

Jyvasjarvi (62�140N, 25�460E) is an urban lake in central

Finland, surrounded by the city of Jyvaskyla with some

80,000 inhabitants. The lake has an area of 337 ha, a

maximum depth of 27 m and a mean depth of 7.2 m, and is

thermally stratified in summer. Jyvasjarvi had become

heavily polluted by the late 1960s, but the condition of the

lake since has been progressively improving (Merilainen

et al. 2003; Salonen et al. 2005). Paleolimnological studies

from chironomid remains indicated mesotrophic conditions

in the lake even before the high anthropogenic pollution

(Merilainen et al. 2003). Nevertheless, the lake is still

somewhat eutrophic and the concentration of total phos-

phorus is typically around 35–40 lg l-1 and of total

nitrogen 850 lg l-1 (Salonen et al. 2005). Hence, an

attempt at further restoration, by biomanipulation involving

mass removals of cyprinid and small percid fish species,

was started by the local authorities in the spring of 2004.

Large traps (30–40 m in length and 10–15 m in width,

mesh size 8 mm) were set around the lake close to shore-

lines at depths less than 5 m. After the first removals of

over 50,000 kg of fish, the catches dropped sharply indi-

cating that there had been an efficient reduction in the fish

stock. A further 50,000 kg of fish were removed during

2005 and 2006, resulting in a total removal of 101,100 kg

(*300 kg ha-1) of fish from Jyvasjarvi during the

biomanipulation.

Zooplankton samples for SIA were collected in 2004

and 2006 bimonthly from May to September–October by

hauling zooplankton nets (mesh size 48 and 100 lm) ver-

tically through the entire water column. Zooplankton

80 J. Syvaranta et al.

samples were then taken to the laboratory and left over-

night in clean water to allow gut evacuation. The next day

these samples were identified and sorted into cladocerans,

and cyclopoid and calanoid copepods. All predatory

zooplankters [such as Leptodora kindtii (Focke) and Cha-

oborus flavicans (Meigen)] were removed from these

samples and, if sufficient, analysed separately. Samples

were then filtered onto glass-fibre filters and dried at 60�C.

Dried zooplankton samples were stored in a dessicator in

petri dishes for later stable isotope analysis. Other zoo-

plankton samples were collected in 2001–2006 from five

sampling sites using a 7.1 l Limnos water sampler. Sam-

ples were taken from 0 to 5 m depth and each was a

composite of 10 hauls, so that a sample from each location

was 71 l. Sampled water was then sieved through a 50-lm

net and preserved using ethanol in 250-ml containers. Five

subsamples (5–10 ml) were taken with a pipette (mouth

4 mm) from each composite sample for later species

identification and enumeration in a sedimentation cuvette

using an inverted microscope. The effect of the subsam-

pling on the precision is described in Karjalainen et al.

(1996). Zooplankton densities were converted into carbon

biomass (lg C) using the average carbon values for the size

classes of each taxon (Rahkola et al. 1998).

Macroinvertebrate samples for SIA were collected in

2004 and 2006 on several occasions from 4 to 5 littoral

sites. Samples were collected by sweep netting (mesh size

500 lm) at depths less than 1 m, and deeper samples

(mussels from down to 6 meters) were obtained with an

Ekman grab. All macroinvertebrate samples were then

taken to the laboratory and individuals were transferred

into clean water to allow them to void their guts. The

following day macroinvertebrates were sorted either into

small glass vials (2 ml) if a sample was a mixture of sev-

eral individuals of the same taxon, or on glass fibre filters if

samples were analysed individually. Only the foot tissue of

mussels was dissected for SIA. After drying at 60�C, the

samples were ground and weighed (0.6 mg) into small tin

cups.

Fish samples for SIA were collected from summer 2003

to autumn 2006 during open water periods from the large

traps used for biomanipulation and with multipanel gill

nets set around the lake. Gill nets were also used to monitor

the fish community structure and habitat use in Jyvasjarvi

in 2001–2006. The gill nets were 30 m 9 1.5 m with 9

mesh sizes (10, 12, 15, 20, 25, 30, 35, 45 and 55 mm from

knot to knot). The nets were used to sample pelagic, pro-

fundal and littoral habitats by setting nets at the surface in

pelagic areas where the water depth exceeded 3 m, at the

bottom in profundal areas where the water depth exceeded

6 m, and at the bottom in littoral areas where the water

depth was less than 3 m. Each habitat had 7–10 gill nets

and catch-per-unit-effort (CPUE) results were calculated

from these catches for each area in 2001–2006. The large

biomanipulation traps (30–40 m in length and 10–15 m in

width, mesh size 8 mm) were set close to shorelines at

depths less than 5 m. Fish sampled for SIA were divided

into those caught before the biomanipulation (fish caught in

2003 and spring 2004) and those caught after (a few

individual predatory fish from late autumn 2005, but

mostly 2006). Sampled fish included mainly perch, roach,

bream, smelt, zander, pike and burbot (Lota lota L.). Perch

were divided according to their size into planktivorous/

benthivorous (\15 cm) or primarily piscivorous ([15 cm)

(Persson et al. 1991; Horppila et al. 2000). Length and

weight were recorded for all fish and a small piece of dorsal

muscle tissue was dissected. Muscle samples were dried at

60�C, ground to a fine powder using a mortar and pestle,

and a small subsample (0.6 mg) was weighed into a tin cup

for SIA.

Stable isotope analyses were done at the Institute for

Environmental Research, University of Jyvaskyla, using a

FlashEA 1112 elemental analyzer coupled to a Thermo

Finnigan DELTAplus Advantage mass spectrometer

(Thermo Electron Corporation, Waltham, MA, USA).

Pulverised pike muscle tissue was used as a laboratory

working standard and replicate standards were run repeat-

edly in every analysis to ensure accurate analysis and to

allow any required correction for linearity and drift. Stable

isotope ratios are expressed as parts per thousand (%) delta

values (d13C or d15N) referring to the international stan-

dards for carbon (PeeDee Belemnite) and nitrogen

(atmospheric nitrogen) (Peterson and Fry 1987). Internal

precision for standards was always better than 0.2% for

both C and N in each run. Lipids are 13C-depleted,

resulting in low d13C values in tissues rich in lipids (Parker

1964) and, as Post et al. (2007) recently showed, the error

in isotope mixing models resulting from overlooked lipid

variability can be considerable. Seasonally collected zoo-

plankton samples may reflect considerable variation in

their lipid content, particularly in colder climates when

they store energy as lipids to survive the winter, which may

translate into biased d13C values in lipid rich zooplankton

(Smyntek et al. 2007; Syvaranta and Rautio 2010). The

zooplankton samples collected from Jyvasjarvi showed

increased lipid content and higher C:N ratios (up to 6.4) in

late autumn with a corresponding decrease in d13C values.

Therefore, we used an empirical lipid normalisation model

(Syvaranta and Rautio 2010) modified from Smyntek et al.

(2007) to normalise the d13C values in our zooplankton

samples based on a non-linear relationship between zoo-

plankton tissue C:N ratios and the difference in d13C values

of bulk and lipid free tissues. In contrast, all our fish

samples had C:N ratios \3.5 (i.e. low lipid content) and

according to Post et al. (2007) normalising these would

have minimal effect on the d13C values.

Altered energy flow pathways in a lake ecosystem 81

We used the SIAR (Stable Isotope Analysis in R)

package (Parnell et al. 2010) in R 2.9.2 (R Development

Core Team 2009) to calculate relative contributions from

pelagic and littoral production in fish species before and

after the fish removals. The SIAR isotope mixing model

uses Bayesian inference to estimate source contribution and

allows the input of uncertainties, such as variation around

the isotope values of source end member values and fraction

factors, into the final model (Jackson et al. 2008). The

contribution (possible range from 0 to 1) of littoral carbon

was also used to estimate trophic positions (TP) of fish with

a simple two-source model following Karlsson and Bystrom

(2005): TP = k ? ([d15Nc – d15Np – (d13Cl – d13Cp) 9

BS 9 LC]/DN), where k is the trophic position of the

organism used to calculate end member values (primary

consumers = 2), BS is the slope of the linear relationship

between littoral and pelagic source end members, LC is the

littoral contribution (0–1), DN is the fractionation factor for

d15N and c, p and l correspond to the consumer, pelagic and

littoral end members. We used fractionation factors of

0.5 ± 0.2% for d13C and 3.0 ± 0.5% for d15N, which fall

within the range for most often reported and used factors

(Peterson and Fry 1987; Vander Zanden and Rasmussen

1999; Post 2002). Both values (with uncertainties) were

used in SIAR model and values for nitrogen in the model to

estimate trophic positions.

End points for pelagic d13C values were calculated as a

mean value extracted from the zooplankton (cladocera and

copepods) summer mean and the mean for unionid mussels

collected in 2004 (‘‘before’’ end point) and 2006 (‘‘after’’

end point). Similarly, littoral d13C end points were calcu-

lated from mean values of snails and the most abundant

littoral macroinvertebrates, such as water slater (Asellus

aquaticus L.) and species of mayfly, caddis fly and chir-

onomids. The d15N end points were calculated similarly to

represent secondary consumer d15N values in the pelagic

and littoral, excluding all potentially predatory species. The

d15N values in the pelagic consumers are substantially

higher than in littoral consumers in Jyvasjarvi (Syvaranta

et al. 2006), which highlights the need of a two source

mixing model to be used when assessing trophic positions

accurately.

We also calculated community-wide metrics from stable

isotope data to assess possible changes in food web

structure (Layman et al. 2007). These metrics were calcu-

lated from a mean value d13C–d15N biplot of all analysed

species of the food web (similar to Fig. 4 but only mean

values for each species). The metrics and their application

in SIA studies have been reviewed in detail by Layman

et al. (2007) and the metrics we included were total area

(TA), a convex hull area covering the whole food web as

indicated by species’ mean values in d13C–d15N isotope

space; mean distance to centroid (CD), which is the mean

distance of each species mean value to the d13C–d15N

centroid (mean of all species) indicating the average degree

of trophic diversity within a food web; mean nearest

neighbour distance (NND), the mean of the distances

between all species and their closest neighbouring species

in d13C–d15N space whose values indicate trophic redun-

dancy (smaller NND values ? increased redundancy); and

standard deviation of nearest neighbour distances

(SDNND), the standard deviation of NND which is a

measure of evenness of the distribution of species’ mean

values (i.e. trophic niches).

Statistical analyses included t tests, analysis of variance

(ANOVA) with Levene’s test for homoscedasticity and

Tukey’s multiple comparisons tests when appropriate, and

Kruskall-Wallis test with Mann–Whitney U tests when

assumptions for parametric tests were not met to analyse

differences in littoral contribution and trophic positions

between species and sampling times (before and after fish

removal). Burbot was not included in the ‘before’ analyses

due to low sample size (n = 2). All statistical analyses

were performed using R 2.9.2 (R Development Core Team

2009) and SPSS for Windows v. 14.0.1 software package

(SPSS Inc., Chicago, IL, USA).

Results

Fish catches

After fish removals started in 2004, gill net catches in the

pelagic habitat declined for perch and roach from an

average CPUE of 769 g net-1 (54 ind. net-1) and

747 g net-1 (15 ind. net-1) in 2001–2003 to 232 g net-1

(18 ind. net-1) and 293 g net-1 (13 ind. net-1) in 2005

(Fig. 1). However, in 2006 catches from the pelagic habitat

increased considerably to 2,827 g net-1 (197 ind. net-1)

for perch, while the increase was 962 g net-1 for roach and

the mean size of these roach had increased notably,

equating to an average catch of 17 ind. net-1. Very few

fish were caught from the profundal habitat and the sam-

pled fish are unlikely to efficiently exploit these depths

with very low oxygen concentrations in Jyvasjarvi. The

only exception, shown by Ravinet et al. (2010), is the ruffe

which is partly supported by methane-dervied carbon after

specialising in feeding on profundal chironomids. The ruffe

were therefore excluded from this data set due to their use

of a unique trophic pathway in Jyvasjarvi. The impact of

fish removals on perch and roach catches from the littoral

habitat were minor until 2006, when catches especially for

perch rapidly increased. The removals had an impact on the

size structure of the fish community, making particularly

smaller perch (\15 cm) more abundant in 2006 than before

the removals in 2001–2003 (Fig. 2). The percentage

82 J. Syvaranta et al.

distribution of species in the biomanipualtion trap catches

were estimated from random subsamples but only calcu-

lated for small perch, roach and bream, since other species

were either too rare or released back into the lake as pre-

dators. Perch made up 31%, roach 25% and bream 43% of

the total catches (by weight) in 2004–2006.

Zooplankton and macroinvertebrates

There was only a small indication of zooplankton biomass

response to these fish removals, against a background of

wide interannual fluctuations in biomasses during the per-

iod 2000–2006 with particularly high zooplankton biomass

in 2001 (Fig. 3). After the first fish removals in 2004,

cladoceran biomass increased by 49%, but decreased again

in 2005. The copepod biomass similarly increased (54%) at

first before quickly returning to pre-biomanipulation levels.

There was a slight but statistically insignificant increase in

proportion of larger bodied individuals in both cladoceran

and copepod populations (Fig. 3). These rather minor

changes in zooplankton community had no appreciable

affect on either chlorophyll a concentrations or water

clarity (mean secchi disk depth 2001–2003 was 1.6 m and

2004–2006 1.5 m).

Zooplankton (Ntot = 127) and littoral macroinverte-

brates (Ntot = 141) had distinct d13C and d15N values

consistent with their assumed energy sources (Fig. 4).

Fig. 1 Gill net catches of perch and roach from different habitats in

Jyvasjarvi during summers 2001–2006. Bars represent mean (±SE)

catch per unit effort (CPUE, n) catches of fish from pelagic, profundal

and littoral areas (each with ten replicate nets). Dashed line indicates

the beginning of fish removals

Fig. 2 Size distribution of perch and roach individuals in gill net

catches from Jyvasjarvi before the fish removals (means ± SE of

2001–2003 catches) and after the last removals in 2006. Values on

x-axis denote the upper size limit for each size class, and median and

percentile size values are given for each panel separately

Altered energy flow pathways in a lake ecosystem 83

The zooplankton samples were then used together with

macroinvertebrate samples to calculate end member values

for mixing models to estimate littoral contribution and

trophic positions. The end member values calculated from

these samples did not differ significantly from each other

between years [all P [ 0.05) and were (±SD): (before)

pelagic C = -34.8 ± 1.3% N = 13.7 ± 2.7%, littoral

C = -27.9 ± 1.3% N = 9.3 ± 1.0% (after) pelagic

C = -34.8 ± 0.8% N = 14.1 ± 1.7%, littoral C =

-27.6 ± 3.5% N = 10.2 ± 1.4%]. Although the samples

used to calculate the before end member values were col-

lected during the first fish removals, it is highly unlikely

that there had already been any significant impacts on

stable isotope values due to fish removals, since no impacts

were identified even after 3 years of removals. Also, this

would have been too short of a time period for any major

changes to occur in zooplankton or macroinvertebrate

community structure.

Littoral energy contribution to fish

Taking all fish (Ntot = 543) analysed for stable isotopes

together by species, the fraction of littoral carbon in higher

trophic levels was 0.65 (65%) before and 0.40 (40%) after

fish removals, as estimated using the SIAR model. Both

planktivorous/benthivorous (small perch, roach, bream and

smelt) and piscivorous (larger perch, pike, zander and

burbot) fish showed greater reliance on pelagic production

after fish removals (Table 1). The mean decrease in littoral

contribution was 33% (23% units) for non-piscivores and

44% (27% units) for piscivores, calculated as the mean

from species’ mean values. There were also clear species-

specific differences within these changes (Table 1 and

Fig. 5). For example, there was no change in the littoral

contribution for bream, but 47% change for smaller perch

and 74% change for smelt. Before fish removals, small

perch and smelt did not differ from each other in littoral

contribution, but both differed from roach and bream

(Kruskall-Wallis v2 = 127.14, df = 3, P \ 0.001), which

also differed from each other (Mann–Whitney U = 1019,

P = 0.003). After fish removals, all these planktivorous/

benthivorous fish differed significantly from each other in

littoral contribution (Kruskall-Wallis v2 = 166.07, df = 3,

P \ 0.001). Piscivorous fish did not differ from each other

Fig. 3 Cladocera and copepod zooplankton biomass and population

size structure in Jyvasjarvi during 2001–2006. Data shown are from

samples collected in August from 0 to 5 m depth. Dashed lineindicates the beginning of fish removals

Fig. 4 Isotope biplots illustrating the food web relationships in

Jyvasjarvi before (upper panel) and after (lower panel) the fish

removals. Mean values (±SE) are given for different zooplankton,

macroinvertebrates and piscivorous fish samples. Individual values

are shown for smelt (black filled circles), small perch (grey filledcircles), roach (open diamonds) and bream (open squares). Eu,

Eudiaptomus sp.; Cyc, cyclopoida; Cla cladocera; Pred, predatory

zooplankton (mainly Leptodora kindtii, Chaoborus sp.); Tr, Trichop-

tera, Lp, Leptophlebiidae (Ephemeroptera); Ch, Caenis horaria(Ephemeroptera); Aa, Asellus aquaticus (Isopoda); C, Chironomidae;

P, pike; Z, zander; LP, large perch; B, burbot

84 J. Syvaranta et al.

in terms of littoral reliance before the fish removals

(F3,31 = 1.54, P = 0.227), but pike differed from the rest

of piscivores after removals (F3,49 = 11.54, P \ 0.001),

being significantly more dependent on littoral production.

Fish trophic positions and food web structure

According to the trophic positions calculated from d15N

and d13C values, roach and bream occupied the lowest

trophic positions before and after the fish removals (Fig. 6),

but did not significantly differ from those of small perch or

smelt before the removals. However, the trophic positions

differed after the manipulation within the planktivirous/

benthivorous fish group (v2 = 75.16, df = 3, P \ 0.001),

roach and bream occupying significantly lower trophic

positions compared to smelt while roach also differing

from small perch. Large perch occupied the lowest trophic

position within the piscivorous fish group and differed

significantly from pike (F2,29 = 8.67, P = 0.004) before

the manipulation. No differences in trophic positions were

detected among the piscivorous fish group after the fish

removals. Only roach and pike showed significant intra-

specific changes in mean trophic positions after fish

Table 1 Fractional littoral contribution (0–1) to sampled fish species before and after fish removals in Jyvasjarvi

Before After

Species n Mean (95% CI) n Mean (95% CI) Change

Perch \ 15 cm 84 0.49 (0.46–0.52) 94 0.26 (0.24–0.29)*** 26

Roach 81 0.78 (0.74–0.81) 82 0.60 (0.57–0.64)*** 18

Bream 38 0.93 (0.87–1.00) 23 0.85 (0.75–0.95) 8

Smelt 25 0.54 (0.49–0.59) 29 0.14 (0.10–0.17)*** 40

Total/mean 228 0.69 228 0.46 23

Perch [ 15 cm 16 0.62 (0.53–0.71) 14 0.36 (0.28–0.45)** 26

Pike 9 0.70 (0.58–0.83) 13 0.44 (0.33–0.55)* 26

Zander 5 0.59 (0.37–0.79) 20 0.29 (0.24–0.36)* 30

Burbota 2 0.58 (0.20–0.99) 8 0.29 (0.11–0.45) 29

Total/mean 32 0.62 55 0.35 27

Mean (±95% Bayesian credibility intervals, CI) for littoral contributions are modelled using SIAR as described in the methods. Overall mean

values for littoral contribution are given for prey and predatory fish separately and calculated as means of species’ means. Asterisks indicate the

significance of the change in littoral contribution (***P\0.001, **P\0.01, *P\0.05) and a change (in % units) in littoral contribution for each

species and overall means is givena Low sample size before biomanipulation

Fig. 5 Comparisons of fractional littoral energy contribution (0–1) to

analysed fish species using SIAR modelling. Paired boxplots indicate

littoral contribution before (left box/lighter grey) and after (right box/

dark grey) fish removals. Boxes indicate 50, 75 and 95% Bayesian

credibility intervals for means

Fig. 6 Estimated mean (±95% confidence intervals) trophic posi-

tions of studied fish species before (open symbols) and after (closedsymbols) the fish removals. Trophic positions were calculated using

trophic fractionation factors of 0.5 ± 0.2% for d13C and 3.0 ± 0.5%for d15N

Altered energy flow pathways in a lake ecosystem 85

removals; the mean trophic position for roach decreased

from 3.1 to 2.9 (t161 = 5.33, P \ 0.001) and that for pike

from 3.9 to 3.6 (t20 = 2.41, P = 0.026) during biomanip-

ulation (Fig. 6).

The community-wide isotope metrics also revealed

changes in the food web structure after the fish removals.

Almost all metrics calculated for the whole food web

showed increased values after manipulation; mean distance

to centroid (CD) increased by 41% (from 17 to 24), total

area (TA) by 11% (54–60), and mean nearest neighbour

distance (NND) by 50% (1.6–2.4). However, the standard

deviation of nearest neighbour distances (SDNND)

decreased by 17% (1.8–1.5). The greatest changes in NND

were observed for roach (from 2.2 to 4.5), smelt (0.4–1.9)

and pike (0.4–1.1). After fish removals, NND for bream

was actually calculated against snails since these had

become the nearest neighbour to bream in the isotope

biplot, and the change was only from 2.2 to 2.9. However,

if NND for bream was calculated against the nearest fish

neighbour (roach), the change for bream was from 2.2 to

8.6. When TA and CD were calculated just for the fish part

of the food web, the increases were 72 and 120%,

respectively.

Discussion

The fish removals in 2004–2006 had an impact on the fish

community structure in the lake, particularly on the perch

population. Gill net catches of perch decreased consider-

ably in the pelagic habitat in 2005, while there was no

impact in the littoral zone (Fig. 1). The impact was less

clear on the roach population, although the catches of roach

were also lower in the pelagic habitat in 2004 and 2005 but

little different in the littoral habitat. The catches of perch

dramatically increased in 2006, both in the pelagic and

littoral habitats. This increase was due to a dense juvenile

perch year class in 2005 seen as a peak in the 90–110 mm

size class of perch in 2006 (Fig. 2), which has been typical

in many restoration attempts after some years of fish

removals (e.g. Hansson et al. 1998; Karjalainen et al.

1999). The size distributions of perch and roach before fish

removals were heavily influenced by a long and warm

summer in 2002 that produced exceptionally abundant

juvenile year classes. This was evident as a 15-fold gill net

catch of 100 mm size class roach in 2003 compared to

years 2001 and 2002, and is seen as a considerable peak in

the catch of these small roach size classes before fish

removals (Fig. 2).

The zooplankton community shifted from dominance by

the small-bodied cladocerans Daphnia cucullata (Sars) and

D. cristata (Sars) towards a greater proportion of the lar-

ger-bodied cladoceran D. galeata (Sars), as would be

expected during the first years after major fish removals

under reduced predation pressure (Hansson et al. 1998).

However, appreciable longer-term interannual fluctuations

in zooplankton biomass obscure any impacts of fish rem-

ovals on zooplankton biomass. Cladoceran and copepod

biomasses increased slightly immediately after the first fish

removals in 2004 but were again lower in 2005. This could

partly be due to a strong juvenile fish year class in 2005

feeding efficiently on zooplankton. There also seemed to be

less impact on the proportion of large copepods and

predatory zooplankton, even though these groups clearly

became more abundant in the SIA samples collected with a

zooplankton net. However, if these larger and more quickly

moving zooplankters effectively evade capture by the

Limnos water sampler used for quantitative zooplankton

sampling, their biomasses would have been underesti-

mated. The data available here for zooplankton biomass

and community composition were from samples collected

in August each year and all larger-bodied copepods were

almost absent from these samples. A few preliminary

samples analysed from June and July indicate that Het-

erocope sp. and Eurytemora sp. biomass increased from

less than 2 lg C l-1 in 2003 to 8–10 lg C l-1 in 2006.

Nevertheless, any cascading effects on chlorophyll-a con-

centrations or water clarity in Jyvasjarvi seem to have been

rather limited.

After fish removal, almost all studied fish species

showed significantly increased energy contributions from

pelagic sources (Table 1; Fig. 5); the only exception was

bream, and also burbot, for which statistical testing was

prevented by low sample size before the fish removals.

Bream is a specialised and efficient benthivore and,

although the bream population was also considerably

reduced (to &30% of stock prior to fish removals based on

a virtual population analysis, T. Keskinen, unpublished

data), there seemed to be little effect on bream feeding

pattern. Smelt and small perch showed the strongest

dependence on pelagic food sources, especially after the

fish removals. Because the smelt population in Jyvasjarvi is

rather small, small perch is likely the primary planktivore

in Jyvasjarvi, particularly after fish removals when abun-

dant year classes of young-of-the-year (YOY) perch

increased the planktivory in Jyvasjarvi. Similar responses

to biomanipulation attempts by fish removals have been

reported before. For example, Karjalainen et al. (1999)

reported decreased predation pressure on benthic inverte-

brates but increased predation on zooplankton after fish

removals due to very dense perch year classes. The fish

removals in Jyvasjarvi had significant impacts on the

feeding niche widths of perch and roach, and many larger

perch specialised in feeding on the abundant fish juveniles

in 2006 (Syvaranta and Jones 2008). Since juvenile fish are

efficient zooplanktivores, predation on juveniles by larger

86 J. Syvaranta et al.

fish promotes the flow of energy from pelagic sources to

higher trophic levels in the food web.

We observed only minor changes in trophic positions of

fish after fish removals. Only roach and pike showed sig-

nificantly decreased trophic positions after biomanipulation

and these changes are likely to be linked. Of the piscivores

in Jyvasjarvi, pike showed the highest littoral contribution

and is therefore likely to feed more on roach than the other

piscivores. Any change in roach trophic position would

then affect the trophic position of pike. According to iso-

tope values, other piscivores in Jyvasjarvi seemed to prey

more on smaller perch, which became more abundant after

the mass removal of larger perch and roach, and were

frequently observed in stomachs of larger perch, burbot and

especially zander. The relatively high temporal variability

in pelagic d15N values observed in Jyvasjarvi (see

Syvaranta et al. 2008) may introduce some bias into our

trophic position calculations. Zooplankton d15N values in

Jyvasjarvi have an increasing trend during summer, with a

peak in autumn. However, the mean cladoceran d15N value

was equivalent to that calculated for mussels, and using a

time series of cladoceran d15N values (Matthews and

Mazumder 2003) together with mussel d15N values as

baseline provides a reasonably good integrated end point

(or baseline) for most longer-lived fish. But some smaller

and more rapidly growing individuals (such as YOY fish)

feeding on zooplankton, may temporarily reflect d15N

values inconsistent with averaged baseline values.

The community-wide measures indicated increased total

occupied niche area and trophic diversity after fish remo-

vals. Greater variability in isotope values associated with

lower trophic levels in a food chain can influence these

metrics, when the whole food web is considered (Layman

et al. 2007). However, these changes were equivalent when

only the fish part of the food web was considered. Roach

and bream (when only fish were considered) showed par-

ticularly pronounced increases in NND values (indicating

decreased trophic redundancy), which suggests that these

species show rather distinct feeding ecologies and are

probably less affected by competition from other fish

species. After fish removals, these species were also less

affected by competition from each other as well as by

intraspecific competition, since the abundance of these

species was substantially reduced. Increases in TA and

especially in CD indicate that the two primary energy

pathways in Jyvasjarvi, one originating from pelagic pri-

mary production and the other from littoral production,

were more distinct after biomanipulation. Fish species

primarily using zooplankton prey (such as smelt and small

perch) were more clearly associated at the top of the zoo-

plankton food chain, whereas benthivorous species (roach

and bream) were closer to the macroinvertebrate food chain

in the d13C–d15N biplot (Fig. 4).

Although smelt is not abundant in Jyvasjarvi, it was

originally included in this study to represent a true plank-

tivorous feeder. However, in practice, it may not have been

a representative planktivore. Before the fish removals, the

smelt population in Jyvasjarvi was divided by their isotope

values into two groups, both having similar d13C but one

with notably higher d15N values (Fig. 4). After fish remo-

vals, the isotope values of smelt were considerably more

homogenous (Fig. 4). Total lengths of smelt individuals in

our samples were 90–140 mm and, according to Vinni

et al. (2004), cannibalism is common for smelt of this size,

so those individuals with higher d15N values before fish

removal may have been largely cannibalistic. Smelt typi-

cally feeds on large-bodied predatory zooplankters, but

these were very scarce in Jyvasjarvi before fish removals,

whereas individuals of both predatory zooplankters and a

large bodied calanoid copepod, Heterocope sp., became

sufficiently abundant after the removals to be included in

SIA. Hence cannibalism amongst smelt was probably more

frequent when the smelt population was larger and valuable

zooplankton prey was limiting, but became rare as both the

availability of more profitable large bodied zooplankton

prey increased and the abundance of smelt had decreased.

A change to feeding primarily on predatory zooplankton

also decreased the variation in smelt trophic position

(Fig. 6).

The results reported in this paper illustrate how the lake

food web in Jyvasjarvi became more dependent on pelagic

production after the fish removals, which appears to be the

result of altering the fish community structure by efficient

removal of older fish followed by increases in younger fish

size classes, in particular those of perch. As the fish com-

munity structure changed towards younger and more

planktivorous individuals, it is not surprising that the whole

Jyvasjarvi food web became less supported by benthic

primary production. In another Finnish lake zooplankton

similarly became more important and benthic macroin-

vertebrates less important prey for fish due to changed

population structure after biomanipulation (Karjalainen

et al. 1999). In Jyvasjarvi, although littoral energy contri-

bution was still considerable after fish removal, the more

important response proved to be the rapid production of

strong year classes of planktivorous juvenile fish that

increased exploitation of and reliance on pelagic energy

sources. These abundant small juvenile fish are profitable

and effectively exploited prey for larger piscivorous fish,

which thereby also became ultimately more dependent on

pelagic primary production (Fig. 5). Hence our first

expectation of increasing contribution of pelagic primary

production to the Jyvasjarvi food web after fish removals

seems valid.

The second original expectation of more discrete pelagic

and littoral energy pathways was supported by the isotope

Altered energy flow pathways in a lake ecosystem 87

data before and after fish removal, where the variation

associated with values for individual fish was considerably

reduced. Also, species that mostly use either pelagic or

benthic consumers (such as smelt and bream) became

clearly separated by their isotope values, and the commu-

nity-wide metrics indicated decreased trophic redundancy

and more even distribution of trophic niches.

In conclusion, our results support recent arguments that

littoral/benthic production in lakes is more important to the

whole lake energy budget than is often acknowledged (e.g.

Vander Zanden and Vadeboncoeur 2002), even in rela-

tively deep lakes. The pelagic primary production in

Jyvasjarvi contributed more to the whole ecosystem after

the fish removal; this is an expected, but probably tempo-

rary, outcome of the change in age and size structure of the

fish populations following selective removal of larger fish

and the subsequent stimulation to recruitment of small

planktivorous perch and roach, and of larger fish feeding on

these. Thus, our results show that lakes undergoing an

attempted biomanipulation may experience considerable

ecosystem changes even if the primary targets (decreased

phytoplankton biomass and increased water clarity, etc.)

are being largely unaffected. More generally, these results

illustrate how alterations of the consumer population

structure can exert a change in energy flow patterns

through an entire ecosystem, a finding probably applicable

not only in lake ecosystems but also in other more diverse

ecosystems (Pace et al.1999).

Acknowledgments Pekka Majuri, Antti Eloranta, Sami Vesala, Sari

Oksanen, Katie Aoki and Joanne Kitchen gave valuable assistance in

the field and laboratory. Tuula Sinisalo, Virve Kustula and Tony

Pirkola helped with operating the SIA instrument in Jyvaskyla. All

personnel working in the Jyvasjarvi Project and biomanipulation

fishing are thanked for their help. Two anonymous reviewers pro-

vided useful comments on an earlier version of this paper. This work

was funded by the Maj and Tor Nessling Foundation (research pro-

jects 2004074, 2005020, 2006026 to RIJ and 2007051 to JS) and by

grants from the Finnish Cultural Foundation and the Kone Foundation

to JS.

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