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Verh. Internat. Verein. Limnol.

2009, vol. 30, Part 8, p. 11931196, Stuttgart, October 2009


by E. Schweizerbartsche Verlagsbuchhandlung 2009

Isotopic variability in lake littoral organisms presents


a challenge for food web studies
Jari Syvranta and Roger I. Jones

Introduction
Most studies of lake ecosystems, including those that use stable isotope analysis (SIA), have traditionally concentrated on
the pelagic system (Beaudoin et al. 2001, Vander Zanden
& Vadeboncoeur 2002). Hence, temporal, spatial, and
interspecies variability in isotopic signatures of pelagic food
web components (especially zooplankton) have been the
focus of recent studies (e.g., Matthews & Mazumder
2003, 2007). Recent SIA studies have also clearly indicated,
however, that benthic production and the littoral areas of
lakes may contribute more than previously thought to the
whole lake ecosystem energy budget (Hecky & Hesslein
1995, Vander Zanden & Vadeboncoeur 2002, Vander
Zanden et al. 2006).
Studies of lake food webs based on SIA often assume
single isotope values to represent baseline values for
pelagic and littoral food webs. These values may then be
used as end members in isotope mixing models, such as
to assess trophic positions or relative contributions from
different energy sources. But such single values ignore
temporal, spatial or especially inter-specific variation in
stable isotope values for these primary consumers, as
shown for pelagic consumers by Matthews & Mazumder (2003). Such variability may have considerable
impacts on the outputs from mixing models and hence on
the inferences drawn about food web structure. Lake littoral habitats have received much less attention in this
respect, despite being important feeding areas for many
fish species and therefore contributing significantly to the
observed stable isotope signatures at higher trophic levels.
Littoral habitats are also inherently more heterogeneous
than pelagic habitats, and primary production from phytoplankton, periphyton, and macrophytes, combined with
allochthonous sources of energy, potentially result in complex and variable isotopic signatures in littoral primary
consumers (Syvranta et al. 2006). We present stable isotope data for littoral invertebrate consumer populations
(benthic invertebrates and zooplankton) from Lake Jyvsjrvi in central Finland and show how variation in isotope
signatures between different littoral invertebrate consumers
can be reflected at higher trophic levels.

Key words: food web, littoral, macroinvertebrates, perch,


stable isotopes, zooplankton

Methods
Jyvsjrvi (6214'N; 2546'E) is an urban lake in central Finland, in the immediate vicinity of the city of Jyvskyl. The
lake has an area of 3.37 km2, a maximum depth of 27 m, and
a mean depth of 7.2 m and is thermally stratified in summer.
Jyvsjrvi was heavily polluted in the 1960s and 1970s by
industrial and municipal waste waters, and today is recovering from severe eutrophication (Merilinen et al. 2003,
Salonen et al. 2005).
Zooplankton samples were collected in summer 2006 by
hauling a zooplankton net (100-m mesh size) horizontally
behind a boat in the littoral area. Samples were then carefully
sieved through 500, 200 and 100 m sieves with clean water
to remove all extra material. Zooplankton samples were then
left in clean water to allow gut evacuation. Samples were
later picked onto glass fibre filters and dried in an oven at
60 C. About 0.6 mg of zooplankton sample was then carefully weighed into tin cups for SIA. Macroinvertebrate samples were collected in summer 2005 and 2006 by kick-netting
(mesh size 500 m) at depths < 1 m. Collected samples were
transferred into clean water in the laboratory to allow the guts
to void. The following day individuals were identified (usually to family level) and sorted onto glass fibre filters. After
drying at 60 C, samples were picked from filters and
weighed into small tin cups (0.50.6 mg). All snails were
removed from their shells and only the soft tissue was dried
and analysed. For smaller species, each sample was a mixture
of several individuals to obtain sufficient sample for analysis.
Larval and juvenile perch (Perca fluviatilis L.) were collected on 6 occasions between June and August 2006 from
offshore pelagic habitats (larval perch) and, as the perch grew
>15 mm in length, from vegetated areas in the littoral habitat.
Larval perch were collected by hauling a large zooplankton
net (500 m) behind a boat, and juvenile perch by sweeping
the vegetated area with a hand net (mesh size 500 m). After
measuring the total length from each fish, heads and stom0368-0770/09/1193 $ 1.00
by E. Schweizerbartsche Verlagsbuchhandlung 2009

1194

Verh. Internat. Verein. Limnol. 30

achs were removed and the fish were dried at 60 C. After drying, the fish samples were ground into a fine powder and stored
in small (2 ml) glass vials for later SIA. Stomach contents were
visually inspected for comparison with SIA data. All stable isotope analyses were done at the Institute for Environmental
Research, University of Jyvskyl, following standard procedures (described in more detail in Syvranta et al. 2006).

Results
Invertebrates collected from littoral areas of Jyvsjrvi
spanned a range over 10 in their mean 13C values and
over 4 in their mean 15N values (Fig. 1). The 15N values of typical littoral primary consumers (such as Ephemeroptera, Asellus aquaticus, Oligocheta) were similar,
but considerably lower than those for snails or Orthocladiinae larvae (also considered as mainly primary consumers). Surprisingly the isotope values for Orthocladiinae
larvae were closer to the values for littoral zooplankton
than for any other benthic invertebrates. Most predators
and scavengers (like Trichoptera larvae) were also clearly
separated by their 13C and 15N values from all other
benthic invertebrates, except from snails (Fig. 1). Also,
Tanypodinae larvae had isotope values matching those of

Fig. 1. Isotope biplot showing mean ( SE) stable carbon and


nitrogen isotope values for the most abundant littoral invertebrates in Jyvsjrvi. Filled black circle indicates mean for all
analysed littoral zooplankton (cladocera and cyclopoida).
Filled grey symbols indicate species that are presumed predators or scavengers and open symbols indicate primary consumers. Abbreviations: O = Odonata, H = Hirudinea, P = Phryganeidae (Trichopetra), LP = Limnephilidae (Trichoptera),
OHC = Orthocladiinae (Diptera: Chironomidae), C = Chironominae (Chironomidae), T = Tanypodinae (Chironomidae),
LPB = Leptophlebiidae (Ephemeroptera), CH=Caenis horaria (Ephemeroptera), A = Asellus aquaticus (Isopoda), OGH
= Oligochaeta (Annelida).

Fig. 2. Stable carbon and nitrogen isotope values for individual larval and juvenile perch sampled between June and
August 2006 in Jyvsjrvi.

most benthic primary consumers, although they are usually considered carnivorous.
The 124 larval and juvenile perch analysed ranged
in total length from 6 to 60 mm. The smallest individuals
analysed still reflected isotope signatures inherited
from their parents (Vander Zanden et al. 1998,
Murchie & Power 2004). After this the 13C values
increased and 15N values decreased rapidly to indicate
external feeding and a subsequent change in diet. Fish
length and 13C values correlated significantly (Pearson
r = 0.598, p < 0.001), but length and 15N values did not
(r = 0.172, p = 0.056), because of the greater variability
in 15N values of larger individuals (Fig. 2).

Discussion
Littoral invertebrates from Jyvsjrvi exhibited a considerable range in both mean 13C and 15N values. Snails
have been proposed as isotopic baseline indicators for littoral habitat in lakes (Post 2002), but snails in Jyvsjrvi
had elevated (by ~2) 15N values compared to most
other primary consumers, suggesting they would not be

J. Syvranta & R.I. Jones, Isotopic variability

appropriate baseline indicators. Stomach contents


showed that fish were preying primarily on chironomids
(Orthocladiinae and Chironominae), A. aquaticus, and
littoral zooplankton, which all had mean isotope signatures very different from snails. Isotope values of littoral
zooplankton (Fig. 1) differed from those of pelagic zooplankton in Jyvsjrvi (Syvranta et al. 2006), having
higher 13C and lower 15N values, which further complicates the assessment of trophic positions and especially
contributions from pelagicbenthic production.
Because isotope signatures in fish muscle tissue
change with the synthesis of new tissue material (i.e., as
fish grow), isotope signatures in rapidly growing juvenile
fish can change within a week or 2, as seen in our samples, and can therefore be used to track ontogenetic diet
shifts in these small fish. We expected the diets of developing perch to shift from pelagic zooplankton to primarily littoral zoobenthic prey (Persson & Greenberg
1990), which at first seemed to be a valid assumption
(Fig. 2). However, as perch grew larger, they started to
show more variable dietary preferences as some individuals selectively consumed littoral benthic invertebrates
and others littoral zooplankton. This specialisation
resulted in highly variable isotope values (both 13C and
15N) observed in larger juvenile perch (>30 mm; Fig. 2).
Although stomach contents confirmed that these perch
had a diet dominated by primary consumers in both
cases, there was ~3 difference in their 15N values,
which is typically considered almost one trophic level
increase in 15N. The data presented here for juvenile
perch illustrate how isotopic variability in prey items,
even within the same habitat, can result in considerable
inter-individual variation in 13C and 15N values analysed from consumer muscle tissue.
The range observed, especially in the 13C values of
littoral consumers, has serious implications for selecting
a single value as an end member in more complicated
isotope mixing models. The variation in pelagic primary
consumer 13C values is usually less than presented here
for littoral consumers, and seasonal averages for different
zooplankton taxa can provide a reasonably good end
member to represent the pelagic habitat (Matthews &
Mazumder 2003). In contrast, littoral areas clearly present more problems for calculating such end member values. Taking the mean 13C value for all primary consumers may be one possibility but, at least in the case of
Jyvsjrvi, would result in considerable underestimation
of littoral contribution in mixing models. Another possibility is to use stomach contents of fish to emphasise the
importance of certain prey types when calculating end
members. Isotope mixing models are typically highly
vulnerable to uncertainties in their end member values,

1195

and even a few difference in 13C values may result in


significant differences in the interpretation of results. We
conclude that studies relying on single isotope values as
end members in isotope mixing models may be seriously
compromised by overlooked variability in isotope signatures of the organisms used to calculate these end member values. More attention should be paid especially to
assessing values to represent littoral-benthic end members.

Acknowledgements
Pekka Majuri, Sari Oksanen, Marjo Jyrkk and Hanna Saarikoski are thanked for their valuable assistance in field and
laboratory. This study was supported by grants from Maj and
Tor Nessling Foundation (research projects 200 5020,
200 6026 to RIJ and 200 7051 to JS).

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Authors addresses: J. Syvranta, Department of Biological and Environmental Science, University of Jyvskyl, P.O. Box
35, 40 014 University of Jyvskyl, Finland. E-mail: jasyvara@cc.jyu.fi
R.I. Jones, Department of Biological and Environmental Science, University of Jyvskyl, P.O. Box 35, 40 014 University of
Jyvskyl, Finland.

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