Limnologica 44 (2014) 49–57

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Limnologica
journal homepage: www.elsevier.com/locate/limno

The effect of trophic state and depth on periphytic nematode

communities in lakes
Ardeshir Kazemi-Dinan a , Fabian Schroeder a , Lars Peters a , Nabil Majdi b,c ,
Walter Traunspurger a,∗
a
University Bielefeld, Animal Ecology, Morgenbreede 45, 33615 Bielefeld, Germany
b
Université de Toulouse, INP, UPS, EcoLab, 118 route de Narbonne, 31062 Toulouse, France
c
CNRS, EcoLab, 31062 Toulouse, France

a r t i c l e i n f o a b s t r a c t

Article history: The aim of this study was to investigate whether nematode community patterns are shaped by nutri-
Received 19 March 2013 ent and light availability. Accordingly, nematode communities inhabiting periphyton were investigated
Accepted 27 May 2013 at gradual water depths (50, 150 and 250 cm) in three Swedish lakes showing graded trophic states. It
Available online 10 September 2013
was hypothesized that: (1) nematode density correlates positively with increasing nutrient availabil-
ity and negatively with increasing depth; (2) increasing nutrient availability favors species and feeding
Keywords:
type richness; (3) increasing depth favors deposit-feeders; and (4) differences in the algal composition
Biofilm
of the periphyton affect the diet of algal-feeders. Our results showed that the biomass of periphytic
Community ecology
Trophic structure
algae increased with nutrient availability and decreased with increasing depth. Nematode density also
Meiofauna increased with increasing trophic state. Species richness decreased with increasing depth in the investi-
Algae gated oligotrophic lake, while the opposite pattern was determined in the other two lakes. Lake trophic
Grazing state significantly affected the trophic structure of the nematode community, with more algal-feeders
occurring in the eutrophic lake whereas chewers were found only in the meso- and eutrophic lakes.
Water depth was also shown to influence nematode feeding type structure, as in all lakes the abundance
of deposit-feeders was greater at increasing depth. While diatoms dominated the periphytic algal com-
munity at all lakes and depths, analyses of the gut pigment content of nematodes showed that their diet
shifted toward green algae in the oligotrophic lake and in shallow zones of the mesotrophic lake.
© 2013 Elsevier GmbH. All rights reserved.

Hard substrates in the euphotic littoral zones of lakes are often
coated by periphyton, which consists of autotrophic and het-
erotrophic organisms embedded in a slimy organic matrix. The
conventional view of energy transfers in lakes is based mostly on
pelagic food web functioning (e.g., Hairston 1993; Mittelbach et al.
1995; Brett and Goldman 1997; Vander Zanden and Vadeboncoeur
2002). However, it has long been acknowledged that benthic com-
munities are also involved in the total production of lakes (e.g.,
Lindeman 1942; Bergtold and Traunspurger 2005a). In recent years,
periphytic communities have drawn particular attention, as several
studies have demonstrated the pivotal contribution of benthic algae
to lake total primary production, food webs, and nutrient cycling
(e.g., Strayer and Likens 1986; Wetzel 1996; Vadeboncoeur et al.
2001, 2002; Hillebrand et al. 2002; Ask et al. 2009). Periphyton
productivity, however, remains constrained by light and nutrient
availability (Hillebrand and Kahlert 2001; Rodusky et al. 2001) and
its transfer through food webs involves species assemblages that
∗ Corresponding author. Tel.: +49 5211062702.
E-mail address: traunspurger@uni-bielefeld.de (W. Traunspurger).
are more complex than those inhabiting the water column (Warren
1989; Havens et al. 1996).
Minute metazoan meiofauna densely colonize lake periphyton
(Peters and Traunspurger 2005; Schroeder et al. 2012a). In stream
periphyton, meiofauna specifically prey on microalgae (Borchardt
and Bott 1995; Majdi et al. 2012b), thereby constituting rele-
vant trophic intermediaries between micro- and macro-organisms
(Schmid-Araya et al. 2002). Nematodes usually dominate meioben-
thic communities in freshwater (Traunspurger 1996a,b; Bergtold
and Traunspurger 2004; Michiels and Traunspurger 2004;
Traunspurger et al. 2012) and, given their diverse feeding types,
are able to exploit multiple food resources, including periphytic
microorganisms such as bacteria, protozoans, and micro-algae
(Montagna 1995). Yet, the combined ecological consequences of
nutrient and light availability on periphytic nematodes have thus
far been overlooked.
The decrease in light availability with increasing water depth
causes a switch in periphyton composition, from photoautotrophic
(e.g., diatoms) to heterotrophic (e.g., bacteria) micro-organisms
(Vadeboncoeur et al. 2008). Light penetration depends on the
trophic state of the lake, with increasing nutrient concentrations

0075-9511/$ – see front matter © 2013 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.limno.2013.05.011
50 A. Kazemi-Dinan et al. / Limnologica 44 (2014) 49–57
Table 1
Morphometric and physico-chemical characteristics of the study lakes. TN: total nitrogen, TP: total phosphorus, O2 : dissolved oxygen, T: temperature.
Lake and location State Area (km2 )
◦  ◦ 
Largen (59 59 N, 18 52 E) Oligotrophic 1.5
Erken (59◦ 51 N, 18◦ 36 E) Mesotrophic 24.0
Limmaren (59◦ 72 N, 18◦ 73 E) Eutrophic 5.4
reducing water transparency (Mazumder and Havens 1998). How-
ever, the potential negative effects on periphytic algae of a
reduction in light are overcome by high nutrient availability. Thus,
the periphyton in eutrophic lakes sustains a higher productivity
than in less nutrient-enriched lakes (Vadeboncoeur et al. 2008).
Furthermore, the periphytic algal community is also affected by
lake trophic state: Liboriussen and Jeppesen (2005) reported a shift
under an increasing nutrient availability gradient, from a predom-
inance of diatoms and cyanobacteria toward one of green algae.
Periphytic algal composition also changes with depth in response
to differences in light availability (Jonsson 1987).
These variations in the periphytic community structure may
affect the diet of invertebrate consumers. Hence, the autotrophic
vs. heterotrophic content of the periphyton has the ability to drive
the distribution of algal- vs. bacterial-feeders. In addition, the diet
of algal-feeders might correspond to the availability of the differ-
ent algal groups within the periphyton. This latter possibility can be
verified by using high-performance liquid chromatography (HPLC)
to quantify algal biomarker pigments contained in the guts of graz-
ers. Indeed, this technique yields in situ information on the diet of
grazers and was previously applied to unravel the algal diet of small
invertebrates such as planktonic and benthic copepods, chirono-
mids (Buffan-Dubau et al. 1996; Irigoien et al. 2000; Goldfinch and
Carman 2000) and, more recently, nematodes (Majdi et al. 2012c).
In their study of the Garonne River (SW France), the latter authors
showed that the algal diet of periphytic nematodes is restricted to
diatoms, which also dominate the periphytic algal assemblage.
Against this background, our study investigated the vertical
changes occurring in the meiobenthic community structure of the
periphyton sampled in three Swedish lakes with graded differ-
ences in their trophic states. The nematode community in particular
was detailed (species composition and feeding types), and nema-
tode gut pigment contents were compared to the algal biomarker
pigment composition of the periphyton. We specifically hypothe-
sized that: (1) meiofauna (and nematode) density increases with
increasing lake trophic state and decreases with increasing depth;
(2) nematode species and feeding type richness should increase
with increasing lake trophic state; (3) a switch from a dominance
of algal- toward bacterial-feeders should be detected with increas-
ing depth; and (4) the diet of periphytic nematodes should match
the availability of the algal groups present in the periphyton.
Materials and methods
Study site and sampling
In April 2010, three Swedish lakes differing in their trophic
state, size, and mean depth were sampled (Table 1). The peri-
phytic meiobenthos in these lakes is dense and diverse (Peters
and Traunspurger 2005). In each lake, a site was sampled at three
depths (50, 150, and 250 cm) along a depth transect from the littoral
zone. All samples below 50 cm were taken by a scuba-diver. How-
ever, in the eutrophic lake, high water turbidity prevented sampling
at 250 cm. At each depth, five replicate periphyton samples were
retrieved from hard substrates (stones) using a brush-sampler
(Peters et al. 2005); these samples were used to measure periphytic
dry mass (DM) and ash-free dry mass (AFDM), chlorophyll a (Chl
a), and algal pigments content, as well as meiofaunal density and
Mean depth (m) Max. depth (m) TN (␮g/l) TP (␮g/l) O2 (mg/l) T (◦ C)
8.3 21.0 500 8 8.6 5.8
9.0 21.0 670 28 11.8 5.6
4.6 7.8 1100 44 11.2 6.5
nematode density, diversity, and feeding types. In addition, at each
depth two or three stones were carefully slid, underwater, into 20-
␮m sieve bags, packed in buckets containing lake water, and then
transported to the laboratory. During sampling, the light quantity
(␮mol/s/m2 ) was measured underwater at different depths (50,
100, 200, and 300 cm) using a LI-250A photometer (LI-COR, Lincoln,
NE, USA). Light measurements were carried out at about 1 p.m. dur-
ing slightly overcast but sunny weather. Water temperature and
dissolved oxygen were measured at 15 cm depth using a Hanna
HI 9828 probe (Hanna Inc., RI, USA). Total phosphorus and nitro-
gen concentrations were measured following the Swedish Standard
Institute guidelines at the Erken Laboratory (Uppsala Universitet,
Sweden).
Periphyton biomass and algal composition
Periphyton samples retrieved with the brush-sampler were
adjusted to a defined volume (100 ml). For each sample, one aliquot
(5–10 ml) was filtered onto a pre-combusted (550 ◦ C, 7 h) glass-
fiber filter (Whatman GF/C, ∅ 25 mm, Whatman, Maidstone, UK)
and then dried (105 ◦ C, 24 h) and weighed to calculate dry mass
(DM). To measure the AFDM content of the periphyton the sample
was combusted by 550 ◦ C for 7 h.
Another aliquot (5–10 ml) was centrifuged (3000 × g, 5 min),
and Chl a was extracted from the pellet with 90% EtOH during 24 h
at 4 ◦ C in the dark following the method of Nusch (1980). The Chl
a concentration was measured spectrophotometrically at 644 nm
and 750 nm and determined on the basis of the uncorrected pheo-
phytin values (Stich and Brinker 2005).
Another aliquot (5–10 ml) was centrifuged (3000 × g, 5 min)
and the pellet was freeze-dried and thoroughly homogenized. A
250-mg subsample was retrieved from the pellet and algal pig-
ments were extracted from each subsample three times (−20 ◦ C,
15 min) with a total of 25 ml (10, 10, and 5 ml) of 98% cold-buffered
methanol (with 2% 1 M ammonium acetate) by sonication, after
Buffan-Dubau and Carman (2000). One ml of the pigment solu-
tion was then filtered through a 0.2-␮m PTFE syringe filter and
the filtrate was analyzed using HPLC (LC1200 series, Agilent Tech-
nologies, Santa Clara, CA, USA). The mobile phase was prepared
and programmed following Barlow et al. (1997). Algal pigments
were identified by comparing their retention time and absorp-
tion spectra with those of pure standards (DHI LAB products,
Hørsholm, Denmark; see Majdi et al. 2011 for further details). The
HPLC-analysis of algal biomarker pigments was coupled with a
chemotaxonomic analysis using CHEMTAX software (version 1.95;
Mackey et al. 1996) to estimate the biomass of algal groups in the
periphyton in terms of their contribution to total Chl a biomass. The
biomarker pigment ratios of periphytic microalgal groups reported
in Majdi et al. (2011) were used to supply the initial matrix needed
to run the chemotaxonomic analysis.
Meiofauna and nematode communities
The remaining periphyton suspension was poured through a 20-
␮m sieve. The organisms retained on the sieve were preserved with
4% formaldehyde and stained with Rose Bengal. Invertebrates were
counted und classified into major taxonomic groups (Nematoda,
Rotifera, Crustacea, Tardigrada, Hydrachnidia, and Oligochaeta)
 A. Kazemi-Dinan et al. / Limnologica 44 (2014) 49–57 51

under a stereomicroscope (40×). From each replicate, 40 nema-

todes were transferred to glycerol solution (Seinhorst 1959),
mounted on slides, and identified to the species level under a Leitz
Dialux microscope (1250×). The Shannon–Wiener index of diver-
sity (H : Ln basis) and Pielou’s index of evenness (J ) were computed
for nematode communities associated with each sample. Nema-
todes were also classified after Traunspurger (1997) according
to the following feeding types: deposit-feeders (mainly bacterial-
feeders), epistrate-feeders (mainly algal-feeders), suction-feeders
(omnivores), and chewers (omnivores, predators).

Nematode gut pigment analysis

The sampled stones covered with periphyton retrieved from

each depth were thoroughly brushed, and the scraped periphyton
was poured through a 20-␮m sieve, transferred to a 15-ml cen-
trifuge tube, and immediately preserved in liquid N2 . This instant
freezing minimizes nematode gut content egestion (Moens et al.
1999). The frozen periphyton was allowed to thaw, after which
350–400 nematodes were sorted under a stereomicroscope (100×)
and carefully transferred to a microcentrifuge tube filled with
MilliQ water. The sorting step was conducted under minimum light
exposure to limit pigment photo-degradation. After centrifugation
(500 × g, 5 min), excess water was removed by freeze-drying. The
pigments contained in the “nematode pellet” were then extracted
in 200 ␮l of 98% cold-buffered methanol (with 2% 1 M ammonium
acetate). Extraction was encouraged by gentle sonication for 90 s in
an ultrasonication bath (Elmasonic S-10 series, IMLAB, Lille, France)
and by an overnight incubation at −20 ◦ C in the dark. The pigment
extract was then filtered onto a 0.2-␮m PTFE syringe filter with a
very low dead volume of <10 ␮l (ReZist series ∅ 13 mm, Whatman
Inc., Florham Park, NJ, USA) and analyzed using the HPLC analytical
protocol described above for periphytic pigments.
Statistical analyses
Differences in periphyton biomass and Chl a, meiofauna and
nematode density, and nematode diversity and feeding types were
analyzed by one-way ANOVA (depths and lakes separately) fol-
lowed by a posteriori pairwise comparisons with Tukey’s HSD test
(˛ = 0.05). Densities were log-transformed to fulfill homoscedas-
ticity assumptions. Meiofaunal and nematode density correlations
with periphyton biomass and Chl a were explored using Spearman’s
rank correlation coefficient. These tests were conducted using SPSS
software (version 15.0, SPSS Inc., Somers, NY, USA).
An analysis of similarity (ANOSIM) using non-metric mul-
tidimensional scaling (nMDS) was performed to explore the
similarities in nematode community structure between lakes and
depths, using the PRIMER software (version 6.1.13, PRIMER-E Ltd.,
Plymouth, UK). The two-way ANOSIM (lakes and depths) was based
on a Bray–Curtis similarity calculated from non-transformed nema-
tode species densities. A one-way ANOSIM was also performed to
Fig. 1. Depth profiles of the relative surface light availability in the analyzed lakes.
test for similarities within lakes. The resulting R has an absolute
interpretation of its value that is potentially more meaningful than
its statistical significance: large values of R, close to 1, indicate a
clear separation of the communities, whereas small values, close to
0, imply little or no separation (Clarke and Warwick 2001). R > 0.5
was considered as indicative of a distinctive difference. Samples
were then represented on a nMDS biplot according to their nema-
tode community similarities with other samples.
Results
Light availability and periphyton structure
In all three lakes, light availability decreased with increasing
depth (Fig. 1). This decrease was especially steep in the eutrophic
lake, where only 25% of the surface light availability was recorded at
50 cm depth. In this lake, below a depth of 200 cm, light availability
was under the detection limits of the probe.
Between lakes, periphyton biomass (measured as its AFDM
content) differed significantly at water depths of 50 cm (ANOVA:
F2,12 = 13.9, P < 0.001) and 150 cm (ANOVA: F2,11 = 14.3, P < 0.001).
Periphytic biomass was especially high in the eutrophic lake, aver-
aging (±SD) 202.5 ± 87 mg/10 cm2 at 50-cm depth (Table 2). Within
the mesotrophic lake, periphytic AFDM decreased significantly
with increasing depth (ANOVA: F2,12 = 17.3, P < 0.05), mostly due to
the strong AFDM decrease observed between 150 cm and 250 cm
depth.
Total periphytic dry mass (DM, including inorganic material)
was lowest at 150 cm depth in the oligotrophic lake and highest
at 150 cm depth in the eutrophic lake (Table 2). In all lakes, the
AFDM to DM ratio decreased with increasing depth. Moreover, this
ratio was especially high in the eutrophic lake (up to 47.5% at 50 cm

Table 2
The mean (± SD) periphytic chlorophyll a (Chl a), ash-free dry mass (AFDM), dry mass (DM), AFDM/DM ratio, and Chl a/phaeopigments (Chl a/Phaeo) ratio in all lakes and at
all depths.

Lake Depth (cm) Chl a (␮g/10 cm2 ) AFDM (mg/10 cm2 ) DM (mg/10 cm2 ) AFDM/DM (%) Chl a/Phaeo (%)

50 337.5 ± 61 28.7 ± 20 180.9 ± 46 15.8 ± 10.2 33.9

Oligotrophic 150 177.2 ± 110 24.8 ± 15 161.8 ± 64 14.2 ± 4.9 27.3
250 211.2 ± 96 20.4 ± 13 177.7 ± 71 12.2 ± 6.1 17.4

50 627.8 ± 63 70.1 ± 30 265.0 ± 143 34.5 ± 22.9 23.7

Mesotrophic 150 569.4 ± 149 77.7 ± 58 407.6 ± 81 18.9 ± 12.6 12.9
250 492.1 ± 157 13.7 ± 17 309.9 ± 134 5.0 ± 5.7 11.7

50 1031.3 ± 112 202.5 ± 87 415.3 ± 127 47.5 ± 7.5 12.3

Eutrophic
150 905.0 ± 195 172.0 ± 38 476.4 ± 134 34.7 ± 5.6 3.9
52 A. Kazemi-Dinan et al. / Limnologica 44 (2014) 49–57

Fig. 3. Relative density of periphyton-dwelling meiofauna in all lakes and at all

Fig. 2. Biomass of periphytic algal groups relative to total chlorophyll a biomass in
depths. Hydrachnidia, Tardigrada, and Oligochaeta were summed as “others.” Num-
all lakes and at all depths.
bers near the bars indicate the mean meiofaunal density (individuals/10 cm2 ± SD).

Nematode density and diversity

depth) and tended to decrease with decreasing nutrient availability
(Table 2).
Periphytic Chl a levels were highest in the periphyton of the
eutrophic lake (Table 2) and differed between the lakes at all
depths (ANOVA; 50 cm: F2,12 = 90.4, P < 0.001; 150 cm: F2,11 = 26.2,
P < 0.001; 250 cm: F1,8 = 11.6, P < 0.01). Within the mesotrophic and
eutrophic lakes, periphytic Chl a tended to decrease with increas-
ing depth, although the differences were not significant (Table 2).
Within the oligotrophic lake, Chl a decreased significantly between
50 cm and 150 cm water depth (ANOVA: F2,12 = 4.3, P < 0.05). The
Chl a/phaeopigments ratio, which represents the ratio of viable
vs. decaying phototrophic biomass, decreased with increasing lake
trophic state (ANOVA: F2,21 = 8.2, P < 0.001).
The results of the chemotaxonomic analysis based on algal
biomarker pigment ratios (CHEMTAX) showed that diatoms were
the predominant (>71%) contributor to periphytic algal biomass
in all three lakes and at all depths (Fig. 2). In all samples, the
contribution of green algae was in the range of 5–27%, whereas
that of cyanobacteria to the periphytic algal biomass was minor
(0–7%). Algal composition did not differ significantly with increas-
ing depth. However, the periphyton consisted of relatively more
cyanobacteria (ANOVA: F2,21 = 337.1, P < 0.001) and fewer diatoms
(ANOVA: F2,21 = 5.7, P = 0.01) in the oligotrophic lake than in the
other lakes.
Nematodes dominated the periphytic meiofauna community
(up to 82%), except in the eutrophic lake at 50 cm depth, where
rotifers were the dominant group (Fig. 3). Nematode density ranged
from 132 to 3164 individuals/10 cm2 (Table 3) and was positively
correlated with the Chl a content of the periphyton (Spearman,
R = 0.38, P < 0.01).
Thirty-five nematode species were identified in total (Table 4),
with two species, Chromadorita leuckarti and Punctodora ratzebur-
gensis, found in all lakes and at all depths. More than 70% of the
nematode communities in all lakes and at all depths was made up
by 3–4 species. For instance, C. leuckarti dominated the nematode
community in the eutrophic lake and at 50 cm depth in the olig-
otrophic lake. P. ratzeburgensis strongly dominated at 50 cm depth
in the mesotrophic lake and was the second most abundant species
at 50 cm depth in the oligotrophic lake. The nematode community
in the oligotrophic lake was dominated by Rhabdolaimus aquaticus
at depths of 150 cm and 250 cm.
Species richness decreased with increasing depth in the olig-
otrophic lake, while the opposite pattern was determined in the
other two lakes (Table 3). The Shannon–Wiener diversity index (H )
and Pielou’s evenness (J ) differed between lakes at depths of 50 cm
(ANOVA; H : F2,12 = 90.8, P < 0.001; J : F2,12 = 40.9, P < 0.001) and
150 cm (ANOVA; H : F2,11 = 3.4, P < 0.01; J : F2,11 = 3.7, P < 0.001). At
250 cm, diversity and evenness were higher in the mesotrophic lake

Table 3
Mean (±SD) periphytic nematode density, species richness (S), Shannon–Wiener index of diversity (H ), and Pielou’s evenness (J ) in all lakes and at all depths.

Lake Depth (cm) Density (individuals/10 cm2 ) S H J

Oligotrophic 50 281.0 ± 58 16 1.90 0.85

Oligotrophic 150 318.5 ± 212 14 1.56 0.75
Oligotrophic 250 132.3 ± 74 12 1.49 0.81
Mesotrophic 50 338.9 ± 271 7 0.64 0.51
Mesotrophic 150 377.9 ± 265 17 1.98 0.85
Mesotrophic 250 442.2 ± 272 18 2.03 0.87
Eutrophic 50 233.8 ± 114 16 1.83 0.80
Eutrophic 150 3163.5 ± 926 19 1.70 0.77
 A. Kazemi-Dinan et al. / Limnologica 44 (2014) 49–57 53

Table 4
Mean relative abundance (%) of periphytic nematode species found in all lakes and at all depths (cm). The feeding types (FT) are classified after Traunspurger (1997): deposit-
feeders (D), epistrate-feeders (E), suction-feeders (S), and chewers (C). Nematodes classified as members of the Rhabditidae family belonged to one species, which was not
identified further. One epistrate-feeder species (species 1) was not identified further.

Nematode taxa FT Oligotrophic Mesotrophic Eutrophic

50 150 250 50 150 250 50 150

Aphanolaimus aquaticus von Daday, 1894 D 0.5 0.5 – – – – – –

Cylindrolaimus communis de Man, 1880 D – – – – – 2.5 0.5 1.3
Eumonhystera barbata Andrássy, 1981 D – – – 0.5 15.0 1.0 – 0.6
Eumonhystera pseudobulbosa (von Daday, 1896) D 0.5 0.5 – 0.5 3.5 6.6 1.0 3.1
Eumonhystera simplex (de Man, 1880) D 6.0 2.0 5.6 – – 4.5 – 3.8
Eumonhystera vulgaris (de Man, 1880) D 2.0 3.5 2.5 – 28.5 13.6 2.5 6.9
Metateratocephalus crassidens (de Man, 1880) D 1.0 – – – – – – –
Monhystera paludicola de Man, 1881 D – – – – 1.0 – – –
Monhystrella paramacrura (Meyl, 1954) D 0.5 – 1.5 – 10.0 16.2 – 0.6
Plectus aquatilis Andrássy, 1985 D – – – – – – 1.5 –
Plectus rhizophilus de Man, 1880 D 2.0 3.0 – – – – 5.1 –
Plectus tenius Bastian, 1865 D – – – 1.5 – – 5.1 0.6
Rhabditidae D – – – – – 0.5 – –
Rhabdolaimus aquaticus de Man, 1880 D 10.0 40.5 36.9 – 1.5 – – –
Rhabdolaimus terrestris de Man, 1880 D 6.0 14.0 30.3 – – – – –
Teratocephalus terrestris (Bütschli, 1873) D 2.5 4.5 2.0 – – – – –
Achromadora micoletzkyi (Stefanski, 1915) E – – – – – – 1.5 0.6
Achromadora terricola (de Man, 1880) E – – – – – – – 1.3
Chromadorina viridis (von Linstow, 1876) E – – – 9.0 16.0 24.2 8.1 23.3
Chromadorita leuckarti (de Man, 1876) E 29.0 2.0 2.4 0.5 3.5 6.1 35.5 32.1
Prismatolaimus intermedius (Bütschli, 1873) E – – – – – – 0.5 –
Prodesmodora arctica (Mulvey, 1969) E 13.0 – 1.0 – – – – 1.3
Punctodora ratzeburgensis (von Linstow, 1876) E 9.5 4.0 2.5 80.4 10.0 11.6 24.9 3.8
Species 1 E – 1.0 11.6 – – – – –
Aphelenchoides sp. S 0.5 1.0 – – 0.5 0.5 – 8.8
Crocodorylaimus flavomaculatus (von Linstow, 1876) S 13.5 20.0 3.0 7.5 0.5 1.0 1.5 –
Dorylaimus stagnalis Dujardin, 1845 S – – – – 0.5 1.0 1.0 0.6
Eudorylaimus agilis (de Man, 1880) S 3.5 3.5 0.6 – 2.0 4.5 – 0.6
Mesodorylaimus subtiliformis (Andrássy, 1959) S – – – – 2.0 – – –
Ironus tenuicaudatus De Man, 1876 C – – – – 4.5 0.5 – –
Tobrilus gracilis (Bastian, 1865) C – – – – – – – 1.3
Neotobrilus longus (Leidy, 1851) C – – – – 0.5 3.0 2.0 4.4
Brevitobrilus stefanskii (Micoletzky, 1925) C – – – – – 2.0 3.6 5.0
Tripyla glomerans Bastian, 1865 C – – – – 0.5 – 5.6 –
Trischistoma monohystera (De Man, 1880) C – – – – – 0.5 – –

than in the oligotrophic lake (ANOVA; H : F1,8 = 31.2, P < 0.001; J :
F1,8 = 6.6, P < 0.001). Within the mesotrophic lake, nematode diver-
sity and evenness significantly increased with increasing depth
(ANOVA; H : F2,12 = 143.7, P < 0.001; J : F2,12 = 106.6, P < 0.001).
The global nMDS plot of nematode communities showed a
clustering between lakes and similar depths (Fig. 4). Thus, at
50 cm depth, the nematode communities of all lakes were clus-
tered together. However, with increasing depth, the nematode
community of the oligotrophic lake clearly diverged from that of
the other lakes. Within the meso- and eutrophic lakes, the nema-
tode assemblages at 50 cm depth sharply differed from those of
the deeper-dwelling periphyton. The ANOSIM results strength-
ened these trends by highlighting distinct nematode community
differences between lakes (ANOSIM: R = 1, P < 0.001) and depths
(ANOSIM: R = 0.75, P < 0.001).
Nematode feeding types

Globally, epistrate-feeders and chewers correlated positively

with the Chl a content of the periphyton (Table 5), with the opposite
correlation determined for deposit-feeders.
Specifically, epistrate-feeders dominated at 50 cm depth in all
lakes (Fig. 5), representing 52, 90, and 71% of the nematodes in
the oligo-, meso- and eutrophic lake, respectively. At all depths,
epistrate-feeders were more abundant in the meso- and eutrophic

Table 5
Spearman correlation coefficients (n = 39) determined for the proportion of feeding
types vs. periphytic chlorophyll a (Chl a) ash-free dry mass (AFDM).

Feeding types Chl a AFDM

Deposit-feeders −0.64** −0.37 ns

Epistrate-feeders 0.66*** 0.26 ns
Suction-feeders −0.37 ns −0.02 ns
Chewers 0.72** 0.12 ns

Fig. 4. nMDS plot (stress: 0.14) of periphytic nematode species composition. The ns: not significant.
Bray–Curtis similarity was calculated from the non-transformed species densities. **
P < 0.01.
Numbers above the symbols indicate the sampling depth. ***
P < 0.001.
54 A. Kazemi-Dinan et al. / Limnologica 44 (2014) 49–57
Fig. 5. Relative occurrence of nematode feeding types in the periphyton in all lakes
and at all depths.
lakes than in the oligotrophic lake (ANOVA: 50 cm: F2,12 = 3.4,
P < 0.001; 150 cm: F2,11 = 18.9, P < 0.05; 250 cm: F1,8 = 18.9, P < 0.01).
Within all lakes, the occurrence of epistrate-feeders decreased
with increasing depth (ANOVA; oligotrophic: F2,12 = 11.7, P < 0.01;
mesotrophic: F2,12 = 4.3, P < 0.05; eutrophic: F1,7 = 67.4, P < 0.001),
such that both the oligo- and the mesotrophic lakes nematode
communities at water depths of 150 and 250 cm shifted toward
a dominance of deposit-feeders.
Within all lakes, the occurrence of deposit-feeders increased
with increasing depth (oligotrophic: F2,12 = 3.3, P < 0.01;
mesotrophic: F2,12 = 17.2, P < 0.001; eutrophic F1,7 = 121, P < 0.001).
At 150 cm depth, the occurrence of deposit-feeders decreased with
increasing lake trophic state (ANOVA: F1,8 = 31.8, P < 0.001).
Suction-feeders occurred in all lakes and depths, accounting for
2.5–24.5% of the nematode communities (Fig. 5). Their distribution
showed no significant trend between lakes or with depth.
Chewers occurred only in the meso- and eutrophic lakes. Their
presence was highest in the eutrophic lake, which resulted in sig-
nificant differences between lakes at depths of 50 cm (ANOVA:
F2,12 = 83.6, P < 0.001), 150 cm (ANOVA: F2,11 = 63.6, P < 0.001), and
250 cm between the oligo- and mesotrophic lakes (ANOVA:
F1,8 = 66.7, P < 0.001).
Nematode gut pigment content
Biomarker pigments typical of diatoms (fucoxanthin and diadi-
noxanthin) and of green algae (chlorophyll b and violaxanthin) but
not of cyanobacteria (zeaxanthin, myxoxanthophyll) were found in
nematode pigment extracts. The proportion of green algae ingested
by nematodes was low and corresponded with that of the sur-
rounding periphyton, except in the oligotrophic lake and at 50 cm
depth in the mesotrophic lake, where green algae was the dominant
contributor (67–92%) to the nematode diet (Fig. 6).
Quantitatively, the Chl a/phaeopigments ratio averaged 4.7
(range: 1.2–11.8) in nematode extracts. To examine Chl a
degradation during digestive processes, we determined the Chl
a-equivalents (Chl a-eq) by summing Chl a, pheophorbide a, and
pheophytin a. Chl a-eq was considered as a proxy for total algal
biomass ingested. Nematode Chl a-eq were relatively high in
the mesotrophic lake, averaging 85.7 pg/individual. In comparison,
Fig. 6. Relative green algal biomass in the periphyton vs. that in nematode guts.
The 1:1 ratio is highlighted by the Y = X dotted line. Deviations from this line reflect
a nematode feeding preference for/deterrence of green algae. Numbers above the
symbols indicate the sampling depth.
nematode Chl a-eq averaged 11.6 and 11.1 pg/individual in the
oligo- and eutrophic lakes, respectively.
Discussion
Lake trophic state and depth effects on periphyton
Nutrient concentration can constrain phytoplanktonic devel-
opment in lakes (e.g., Smith 1979) and thus determine light
penetration to benthic communities (Mazumder and Havens 1998;
Liboriussen et al. 2005). Our measures of light penetration among
lakes provide further evidence of this trend. The positive effects
of light on periphyton biomass have been copiously supported in
studies of numerous freshwater ecosystems (e.g., Steinman and
McIntire 1987; Hillebrand and Kahlert 2001). Vadeboncoeur and
Lodge (2000) also showed that the periphyton production rate
decreased with increasing water depth. Hence, we expected a
periphytic biomass notably reduced with increasing water depth
in the eutrophic lake, as a result of a steep reduction in light
penetration ability. On the contrary, at 150 cm depth, a thick peri-
phyton crowded with meiofauna and algae was found, despite a
surface light availability of only 14%. Thus, finally, high nutrient
concentrations favored periphyton biomass even under these low
light availability conditions. However, as highlighted by the low
Chl a/phaeopigment ratio, this periphyton contained important
amounts of decaying phototrophs, possibly stemming from phy-
toplankton sedimentation and/or from severe grazing pressure.
Periphytic algal biomass was found to correlate positively with
lake trophic state, corroborating other studies (e.g., Cuker 1983;
Hillebrand and Kahlert 2001). The structure of periphytic algal
communities is influenced by factors such as light and nutri-
ent availability (e.g., Stevenson 1997; Ledger and Hildrew 1998;
Kahlert et al. 2002). In our study, diatoms consistently dominated
in all lakes and at all depths. However, it is also likely that sub-
tle taxonomic variations occurred that were not detected with our
chemotaxonomic approach.
Nematode density and diversity patterns
Trophic state affects sediment-dwelling nematode communi-
ties in littoral zones of lakes (Traunspurger et al. 2006; Ristau and
Traunspurger 2011). In this study we found a correlation between
 A. Kazemi-Dinan et al. / Limnologica 44 (2014) 49–57
nematode density and periphytic algal content that increased
with increasing lake trophic state. This result highlights that the
availability of their potential prey (microalgae) can favor the pres-
ence of nematodes. Couplings between nematode density and
the algal content and thickness of the periphyton are increas-
ingly supported by studies of lotic and lentic habitats (Peters and
Traunspurger 2005; Gaudes et al. 2006; Majdi et al. 2011; Schroeder
et al. 2012a,b), with our results strengthening the hypothesis of a
strong bottom-up structuring of periphytic nematode communi-
ties. Such bottom-up effects occur also in sediments (e.g., Beier and
Traunspurger 2003a,b; Michiels and Traunspurger 2005a); how-
ever, since periphyton is both a habitat and a food resource, any
variations of either its thickness or its algal content will substan-
tially constrain nematode density. Of course, top-down and/or
abiotic constraints may also play a role in the distribution of nema-
todes in the periphyton (Hillebrand et al. 2002; Beier et al. 2004;
Peters and Traunspurger, 2012; Majdi et al. 2012a), but the com-
bined effects of these factors require further investigation.
In lakes, the sedimentation rate of autochthonous and
allochthonous resources is pivotal to fuel benthic food webs
(Bergtold and Traunspurger, 2005b; Witthoeft-Muehlmann et al.
2005; Solomon et al. 2008). For instance, deeper zones of lakes are
less prone to wave-induced disturbance, which impacts both the
periphytic algal biomass and the pool of sinking material available
to metazoan consumers (Vadeboncoeur et al. 2002; Stevenson and
Stoermer 2008; Babler et al. 2008). Initially, we hypothesized that
nematode density should decrease with increasing depth, follow-
ing the decline of light and of benthic primary production. However,
our results showed no clear depth trend in nematode density dis-
tribution, although nematode density seemed to increase with
increasing depth, perhaps as a result of the higher periphyton sta-
bility against wave disturbance. Similarly, in the littoral of Lake
Königssee (Germany) nematode density increased between water
depths of 1–5 m and decreased between water depths of 5–190 m
(Traunspurger 1996a).
Concerning periphytic nematode diversity, the assemblages
were always dominated by a few species, as commonly observed
within freshwater benthos (Michiels and Traunspurger 2005a;
Peters and Traunspurger 2005; Traunspurger et al. 2006; Majdi et al.
2011; Schroeder et al. 2012b). The dominance of C. leuckarti (Chro-
madoridae) and R. aquaticus (Rhabdolaimidae) in the periphyton of
the oligotrophic lake confirmed the results of Traunspurger (1992).
In his study, two other members of these families, Chromadorina
bioculata (Schultze in Carus, 1857) and Rhabdolaimus terrestris,
dominated the periphyton in the oligotrophic Lake Königssee.
Our results point out the singularity of nematode assemblages in
the oligotrophic lake vs. the other lakes. Nevertheless, periphytic
nematode diversity was lower in the oligotrophic lake, in contrast
to the trend exhibited by sediment-dwelling nematode commu-
nities (Ristau and Traunspurger 2011). Globally, our results also
support a lower nematode diversity in periphyton than in sed-
iments (e.g., Peters and Traunspurger 2005; Gaudes et al. 2006;
Majdi et al. 2011; Schroeder et al. 2012b). This difference is likely
the result of higher physical mixing and greater biological con-
straints, which renders periphyton a more restrictive habitat than
sediments (Majdi et al. 2011; see Discussion therein). Hence, intra-
and interspecific competition can be biased toward typically epi-
phytic species. In turn, nematode populations able to colonize the
periphyton could be mostly influenced by space and food con-
straints.
Opposing depth-driven diversity trends were observed between
the oligotrophic lake and the two other lakes: species richness
tended to decrease with increasing depth in the oligotrophic lake
whereas species richness and assemblage differences increased
with increasing depth in the meso- and eutrophic lakes. While
nematode diversity distribution patterns remain complex and
55
difficult to interpret (Traunspurger et al. 2006; Hodda et al. 2009),
we suggest that the combination of periphyton structure and
stability with external constraints (e.g., wave disturbance, light,
sedimentation rate) partly explains nematode species distribution
in lake periphyton. For instance, Chromadoridae always dominated
in shallow periphyton. Besides being algivores, they can firmly
attach themselves to hard substrates with their caudal sticky silks
(Croll and Zullini 1972), and hence are likely to be less easily
dislodged from the periphyton by wave-driven erosion processes
than other nematodes. Deeper periphyton is more stable against
wave disturbance and could thus harbor more consistent and more
mature nematode assemblages, which would be mostly shaped by
food quality and availability.
Nematode feeding types and algal diet
Lake trophic state affected the composition of nematode feed-
ing types in the periphyton. In fact, there was a clear trade-off
between epistrate- and deposit-feeders: unlike epistrate-feeders,
the proportion of deposit-feeders increased with increasing depth
and decreasing trophic state and periphytic algal biomass. Deposit-
feeders mostly feed on bacterial size-ranged items, using their
minute unarmed buccal cavity, whereas epistrate-feeders can con-
sume larger prey, including diatoms (Traunspurger 1997; Moens
et al. 2006). It is well known that resource availability plays a role
in structuring aquatic communities (e.g., Beaver and Crisman 1982;
Silver et al. 2002; Michiels and Traunspurger 2005b). Thus, we
suggest that the availability of microalgae vs. bacteria and fine par-
ticulate organic matter shaping the periphyton may be at the origin
of the observed trade-off of feeding types. In addition, it should be
noted that chewers (i.e., omnivores–predators) were found only
in the meso- and eutrophic lakes, and their occurrence was pos-
itively correlated with periphytic algal biomass. Most chewers
belonged to the Tobrilidae, which can feed on diatoms and on
small invertebrates (Zullini 2006). Thus, it is likely that their abun-
dance in the periphyton followed the availability of their potential
prey, which increased with increasing trophic state. The presence
of such predators in meso- and eutrophic periphyton also provides
an explanation for the higher species diversity observed, through
the prevention of competitive exclusion due to dominant species
(Michiels et al. 2004; Traunspurger et al. 2006). Taken together,
our results strengthen the observations reported in the review of
Traunspurger (2002), who showed that deposit-feeders are neg-
atively affected by increasing trophic state and that omnivorous
nematodes are more abundant in meso- and eutrophic lakes than
in oligotrophic lakes (Schroeder et al. 2012b).
Although changes in periphytic algal group composition were
expected to occur under a trophic gradient (e.g., Chetelat et al.
1999; Liboriussen and Jeppesen 2005), such changes were not
observed in any of the three lakes; instead, diatoms dominated
in all lakes and at all depths. However, unexpectedly, the nema-
tode diet clearly shifted toward green algae in the oligotrophic
lake and at 50 cm depth in the mesotrophic lake. This result has
to be interpreted with caution, since (1) nematode samples were
not replicated and (2) the HPLC-analysis of nematode gut pigments
is novel and has, so far, only been employed once (Majdi et al.
2012c). Thus, for greater relevance, we recommend applying this
procedure either to nematodes sorted to the best taxonomic level
or to communities strongly dominated by a few species. Majdi
et al. (2012c) analyzed the diet of a periphytic nematode commu-
nity in the Garonne River, France, which was strongly dominated
(75–100%) by C. bioculata and Chromadorina viridis. They showed
exclusive diatom consumption, quantitatively ranging from 2.6 to
9.1 pg Chl a-eq per individual. We found comparable values of
nematode Chl a-eq in the oligo- and eutrophic lakes: 11.6 and
11.1 pg/individual, respectively. However, nematode Chl a-eq was
56 A. Kazemi-Dinan et al. / Limnologica 44 (2014) 49–57
one-order of magnitude higher in the mesotrophic lake, averag-
ing 85.7 pg/individual. Also, our average Chl a/phaeopigments ratio
in nematodes was much higher (4.7) than that (0.18) reported by
Majdi et al. (2012c). The reasons for these differences are complex
but likely involve the following: (1) a temperature-dependent gut
passage time and digestive efficiency of algal pigments, as the aver-
age water temperature was 6 ◦ C in our study vs. 13.5 ◦ C in that
of Majdi et al. (2012c); (2) differences in nematode assemblages,
with the extraction of a higher number of large algal-feeding nema-
todes (e.g., Dorylaimidae and chewers) from the periphyton of the
mesotrophic lake; and (3) a reduction in light availability with
increasing depth and trophic state, which could negatively affect
the nutritional quality of benthic green algae and hence orient the
diet of algal-feeders toward diatoms.
Acknowledgements
We are grateful to Erken’s Laboratory team for their help during
sampling. A German Research Foundation grant (DFG-PE 1522/2-1)
funded this study.
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