Ecological diatom guilds are useful but not sensitive enough as indicators of extremely changing water regimes

PRIMARY RESEARCH PAPER

Ecological diatom guilds are useful but not sensitive enoughas indicators of extremely changing water regimes

Viktoria B-Beres • Peter Torok •

Zsuzsanna Kokai • Enik}o T. Krasznai •

Bela Tothmeresz • Istvan Bacsi

Received: 12 January 2014 / Revised: 25 May 2014 / Accepted: 26 May 2014

� Springer International Publishing Switzerland 2014

Abstract Classification of taxa into ecological

guilds is based on the relation of respective taxa to

nutrient enrichment and their resistance to physical

disturbance. We hypothesized that ecological guild’s

proportion and their taxa composition were strongly

effected both by extremely changing water regime and

nutrient contents. Diatom composition, guild dynam-

ics and the diatom-based ecological status assessment

index were studied in the Sebes-Koros River (South-

East Hungary) in a year with extremely changing

water regimes. There were highly pronounced changes

in species composition during the whole vegetation

period including the formation of running and stand-

ing water segments in autumn. While the proportions

of ecological guilds showed no significant correlations

with the studied environmental parameters, they were

more balanced in high water discharge period than in

the low water discharge period. Taxa compositions of

segments were mainly determined by the preferences

and strategies of a respective species and/or genera,

regardless to their guild affiliation. These results point

out that ecological guild characterisation should be

refined using ecological knowledge at the subgenus

level. We suggest to establish several subdivisions

within the guilds to consider the differences in life

strategies (CSR model) and life forms, and to imple-

ment the accumulated knowledge of nutrient prefer-

ences/indication of a respective taxa.

Keywords Diatom species composition � Diversity �Ecological guilds �Medium-sized river �Water quality

Introduction

Nowadays, diatoms are routinely used in environmen-

tal status assessment, because of their importance in

food webs, biochemical linkages and due to their

sensitivity for physical, chemical and biological

disturbances (Stenger-Kovacs et al., 2007; Bolla

et al., 2010; Chetelat et al., 2010; Kireta et al.,

2012). Diatom-based environmental status assessment

requires high taxonomical knowledge. Due to the

expansion of molecular methods and electron

Handling editor: Judit Padisak

V. B-Beres (&) � Z. Kokai � E. T. Krasznai

Environmental Protection and Nature Conservation

Authority, Trans-Tisza Region, Hatvan u. 16,

Debrecen 4025, Hungary

e-mail: [email protected]

P. Torok

MTA-DE Biodiversity and Ecosystem Services Research

Group, Egyetem ter 1, Debrecen 4032, Hungary

B. Tothmeresz

Department of Ecology, University of Debrecen, Egyetem

ter 1, Debrecen 4032, Hungary

I. Bacsi

Department of Hydrobiology, University of Debrecen,

Egyetem ter 1, Debrecen 4032, Hungary

123

Hydrobiologia

DOI 10.1007/s10750-014-1929-y

microscopy in diatom research, several species com-

plexes were divided into several new species (Potap-

ova & Hamilton, 2007; Novais et al., 2009). This

resulted that exact identification to species by light

microscopy techniques (1,000–1,600 fold magnifica-

tion, which is widely used in practice) are not feasable

for each taxa (e.g. Gomphonema parvulum complex,

Achnanthidium minutissimum complex and Encyon-

opsis microcephala complex—Morales et al., 2001;

Rimet & Bouchez, 2012a). Rimet & Bouchez (2012b)

argue that there is only a little loss of ecological

information when the accuracy decreased from spe-

cies to higher taxonomical group. Thus, classifying

taxa into respective ecological functional groups (i.e.

guilds) became more popular in biomonitoring appli-

cations and also in ecological studies (Padisak et al.,

2009, Rimet & Bouchez, 2012a, b). Passy (2007)

ranked the diatom taxa into three guilds (low-profile,

high-profile and motile guilds), which was modified

by Rimet & Bouchez (2012b) as planktic guild.

Changes in flow conditions were found to induce

responses in both composition and physical structure

of benthic diatom communities (Lamb & Lowe, 1987;

Poff et al., 1990; Molloy, 1992; Biggs et al., 1998;

Passy, 2002). Classification of taxa into ecological

guilds is based on the relation of taxa to nutrient

enrichment and on taxa’s resistance to physical

disturbance (e.g. in form of different flow conditions;

Passy, 2007). Studying the relationship between

diatom guilds and environmental factors began in the

last few years (e.g. Berthon et al., 2011; Rimet &

Bouchez, 2012a; Stenger-Kovacs et al., 2013).

Because of the easy use of guilds, it might provide a

great opportunity to apply them in the environmental

status assessment. However, it is still not entirely

clear, how reliable are the guild level ecological

analyses of benthic diatoms in the identification of

relatively rapid changes in the environmental condi-

tions and flow conditions among them as physical

disturbance.

In the year of 2012, the summer and autumn could

be considered as extremely dry in Hungary based on

the data of the Hungarian Meteorological Service and

the General Directorate of Water Management.

Because of the dry weather, the water discharge of

some lowland rivers—like the Sebes-Koros river—

decreased drastically (max. 90.25 m3 s-1 in May;

min. 1.22 m3 s-1 in September). Due to very low

water discharge, segments characterized by different

water flow conditions were formed in Autumn. These

segments were continuously connected with each

other, and the main differences between them occurred

in the flow conditions: an extremely slowed down

water flow was typical in the so-called standing water

segment, which were formed between the riverbank

and the main stream of the riverbed because of its

morphology.

In this work, the diatom species and guild dynamics

and its effects on the changes of diatom-based

ecological status assessment index (in the followings

abbreviated as IPSITI) were studied from April to

November (during the whole vegetation period). We

hypothesized the followings:

(i) Relative abundance of low-profile guild will be

high in the Spring and early Summer (period

with high water discharge), while the decreasing

water discharge from July will decrease the

proportion of this guild.

(ii) The proportion of high-profile guild will be low

in Spring and early Summer (period with high

water discharge), while the decreasing water

discharge from July will favour this guild.

(iii) The proportion of motile guild will be the lowest

in months with the highest water discharge.

(iv) We assumed that running and standing water

segments can be characterized by different guild

ratios: low-profile guild will be present in higher

relative abundance in running water segments,

while high-profile guild and motile guild will be

present in higher relative abundance in the

standing water segments.

Materials and methods

Sampling setup and environmental parameters

Samples were collected at Korosszakal, on the river-

bed of Sebes-Koros (South- Eastern Hungary; N:

47�00041.9500 E: 21�36025.6800; medium-sized river).

For monthly analyses, benthic diatom samples were

collected from April to November, 2012. Conductiv-

ity, pH, dissolved oxygen and water temperature were

measured in situ in the field with a portable-multipa-

rameter digital metre (Multi 350i-WTW, Germany).

Water samples were kept at 4 �C in cooler bag during

transportation to the laboratory for total nitrogen (TN)

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and total phosphorus (TP) measurements. TN was

calculated by summarising the amount of different

nitrogen forms. Free ammonium concentration and

ammonium concentration disengaged from organic

nitrogen compounds were measured by a manual

spectrophotometric method based on the MSZ ISO

7150-1:1992 (1992) Hungarian Standard. This stan-

dard is totally equivalent in technical content and fully

corresponds in presentation to the International Stan-

dard ISO 7150-1:1984. Measurement of nitrate con-

centration was based on colorimetry by titration of

salicylic acid (MSZ 1484-13:2009, 2009). Colorime-

try was also used to measure nitrite concentration

applying sulphonic acid and aminonaphthalene

reagents (MSZ 1484-13:2009, 2009). Total phospho-

rous was determined by the acid molybdate method

(MSZ EN ISO 6878:2004, 2004). The same physical

and chemical parameters were measured by the same

methods for analyses of the formed segments from

September to November (see below). Water discharge

data were kindly provided by the National Water

Authority, while rainfall data were provided by the

Hungarian Meteorological Service.

The amount of rainfall in 2012 (427 mm) was

25% lower than the hundred-year average (569 mm),

which can be considered as extremely dry according

to the Hungarian Meteorological Service. This

amount is also lower, than in 2011 (441 mm), 2010

(845 mm) and 2009 (485 mm). What was more

important is the distribution of annual rainfall which

was unequial: the quantity of rainfall in the second

part of vegetation period was less than 36% of the

2012’ year amount. This dry weather caused a very

low water discharge from September to November,

resulting that two segments were formed in connec-

tion with each other, but with different water flow

conditions (called ‘running water’ and ‘standing

water’ segment in the followings), because of the

riverbed morphology. This phenomenon was not

observed in the previous years in the Sebes-Koros

at Korosszakal by the colleagues of the Environmen-

tal Protection and the Nature Conservation Authority.

There were no differences in the measured physical

and chemical parameters, only in the water flow

conditions between the formed segments.

Benthic diatom samples were also collected from

these formed segments from September to November.

Sampling was done in these segments in triplicate.

There were no differences in the substrate and depth of

sampling between the standing and running water

segments.

Sample collection and preparation

Five cobbles were used as sampled substrates all

times. Diatoms were removed from the cobbles by

tooth brushing. The sampling area of cobbles was

approximately 10 cm2. Sampling was done in tripli-

cate in all cases. Samples were fixed in Lugol’s

solution on the field. Diatom valves were prepared by

the hot hydrogen-peroxide method. Naphrax synthetic

resin was used for embedding (MSZ EN 13946:2003,

2003). Leica DMRB research microscope and

1,000–1,600-fold magnification were used for identi-

fication of diatom taxa. At least 400 valves were

counted (MSZ EN 14407:2004, 2004); for diatom

identification, Krammer & Lange-Bertalot (1997a, b),

Krammer & Lange-Bertalot (2004a, b), and Potapova

& Hamilton (2007) were used. Identification of

Achnanthidium minutissimum (Kutzing) Czarnecki

and A. eutrophilum (Lange-Bertalot) Lange-Bertalot

belonging to A. minutissimum species complex was

based on Potapova & Hamilton (2007).

Data processing and analyses

Classifying the diatom taxa into guilds was imple-

mented according to Passy (2007) and Berthon et al.

(2011): low-profile, high-profile and motile guild.

According to Rimet & Bouchez (2012b), planktic

guild was also considered. Multimetric diatom index

developed for streams, and small- and medium-sized

rivers (IPSITI) was calculated to characterize the

water quality of the river. The IPSITI index is

calculated by averaging of IPS, SI and TI indices.

The IPS, SI and TI indices were calculated by the

OMNIDIA version 5.2 software package (Lecointe

et al., 1993). For details about IPS, SI and TI, see

Lecointe et al. (1993); for further data about IPSITI,

see Varbıro et al. (2012). To verify main tendencies

between environmental factors and species composi-

tion and to select crucial factors, principal component

analysis (PCA) was calculated (Leps & Smilauer,

2003; Stenger-Kovacs et al., 2013). Those environ-

mental factors were included in the PCA, which

showed higher differences between months than 10%

from the average calculated for the whole study

period. To analyse diatom assemblages in relation of

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123

verified environmental factors, a canonical correspon-

dence analysis (CCA) was calculated (Ter Braak &

Smilauer, 2002). Kruskal–Wallis correlations were

calculated for significance of guilds’ proportion (Zar,

1999). Relations of species composition of diatom

assemblages and water flowing conditions were dis-

played by a detrended correspondence analysis (DCA)

based on relative species abundances.

Results

Changes in environmental variables

Altogether, seven environmental factors (TN, TP,

water discharge, conductivity, time, temperature and

dissolved oxygen- DO, sample N-1) were included to

the Principal Component Analysis. The first three axes

of PCA explained 85% of variance. The PCA revealed

that the factors with the highest correlation were with

the first axis Time (0.6432) and TN (0.5954), with the

second axis Water discharge (-0.5774), and with the

third axis TP (-0.6136) and Conductivity (0.5921).

Water discharge increased from April to June and

showed drastic decrease from June to July (Fig. 1).

The low water discharge period continued from July to

November, and the lowest water discharge value was

measured in September (Fig. 1). There was an oscil-

lation in TP concentration during the study period: it

decreased from April to May, than there was an

increase from May to July, followed by a remarkable

decrease from July to August (Fig. 2a), than TP

concentration increased from August to November

(Fig. 2a). TN showed opposite changes to water

discharge: it decreased from April to June (Fig. 2b),

than it increased closely three times of its minimum

measured in June (1 mg l-1; Fig. 2b) during the low

water discharge period (from July to November;

Fig. 2b). Closely related to decreasing water discharge

in summer and autumn, conductivity doubled from

May to September (Fig. 2c).

Monthly changes of diatom assemblages

and IPSITI

The measured environmental factors detailed above

were selected for the CCA analysis (Fig. 3). The

eigenvalues of the CCA were 0.488 and 0.453, while

the species and environmental correlations were 100 and

98.2% for the first and second axis, respectively. The

Fig. 1 Daily changes of water discharge provided by the National Water Authority. Black diamonds indicate the dates of diatom

sampling

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Monte-Carlo permutation test indicated the significance

of the CCA and validated that the obtained pattern is

significantly differed from random (N = 99, P = 0.01

for the first, and P = 0.04 for all canonical axes). Some

taxa, like Achnanthidium minutissimum (ADMI),

Amphora pediculus (Kutzing) Grunow (APED), were

characteristic for periods with high water discharge

(from April to June). These taxa were sensitive to the

drastic decrease of water discharge from June to July

(Fig. 3). In contrast, some other taxa, which appeared

and became the most frequent in July, were correlated

positively with the changes of TP (Navicula germainii

Wallace—NGER, Navicula viridula (Kutzing) Ehren-

berg var. rostellata (Kutzing) Cleve—NVRO, Nitzschia

palea (Kutzing) W. Smith—NPAL) (Fig. 3). The taxa,

which were positively correlated with TN reached the

maximum of their individual numbers, when water

discharge was the lowest (Achnanthidium eutrophi-

lum—ADEU, Diatoma vulgaris Bory de Saint-Vin-

cent—DVUL, Melosira varians Agardh—MVAR;

Fig. 3). Relative abundances of Cocconeis placentula

Ehrenberg ssp. (CPLA, CPLE, CPLI) correlated posi-

tively with conductivity (Fig. 3), and they reached their

maximum number of individuals in September.

The proportion of diatom guilds changed during the

decreasing water discharge, and the concomitant nutri-

ent content changes throughout the study (Fig. 4a).

According to Kruskal–Wallis correlation, significant

changes in proportion of guilds were observed between

the months of spring and autumn (low-profile guild,

May–October and May–November, P = 0.002; motile

guild, May–October, P = 0.004), between the months

of spring and summer (motile guild, May–July,

P = 0.004) and between the months of summer and

Fig. 2 Monthly changes of environmental variables (a total

phosphorous (TP); b total nitrogen (TN); and c conductivity)

during the whole sampling period

Fig. 3 Changes of relation of species composition of diatom

assemblages and the environmental variables displayed by a

CCA based on relative species abundances. The eigenvalues of

the CCA were 0.488 and 0.453, while the species and

environmental correlations were 100 and 98.2% for the first

and second axis, respectively. Notations The most abundant 30

species were shown using four letter OMNIDIA codes. TN total

nitrogen; TP total phosphorous

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autumn (high-profile guild, July–September and July–

November, P = 0.003).

Increasing water discharge in spring and early

summer (from April to June) caused changes in

proportion of low-profile, motile and planktic guild

(Fig. 4a). Increasing proportion of low-profile guild

occurred in May and June due to the increasing

relative abundances of Achnanthidium minutissimum

(ADMI), Amphora pediculus (APED) and Encyonema

silesiacum (ESLE) taxa, which showed positive cor-

relation with water discharge (Fig. 3). In contrast,

proportion of motile guild decreased from April to

May (Fig. 4a), caused by the decreasing relative

abundances of taxa Navicula tripunctata (NTPT),

Navicula veneta (NVEN), Nitzschia dissipata (Kut-

zing) Grunow (NDIS), Nitzschia inconspicua (NINC),

and Nitzschia fonticola (NFON), which otherwise also

showed positive correlation with water discharge

(Fig. 3). Proportion of planktic guild increased from

April to May (Fig. 4a), caused by the increasing

relative abundances of Aulacoseira granulata (Ehren-

berg) Simonsen and Stephanodiscus sp. Increasing

water discharge and decreasing TN concentration in

spring and early summer changed not only the

proportion of guilds but also taxa number of certain

guilds (Fig. 4b). The taxa number of low-profile guild

Fig. 4 Changes of

a relative abundances of

diatom guilds; b taxa

numbers in guilds during the

whole sampling period

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changed the most conspicuous; it increased with 75%

from April to May, and rare species like Reimeria

uniseriata Sala, Guerrero & Ferrario, Rhoicosphenia

abbreviata (Agardh) Lange-Bertalot and Encyonopsis

microcephala (Grunow) Krammer appeared. Increase

of the proportion of planktic guild was due to the

increase of the already present species, not due to the

increase of taxa number (Fig. 4b).

Drastic decrease in water discharge (from a mean of

51.3 m3 s-1 to a minimum of 7.7 m3s-1; Fig. 1) and

the increase in total nitrogen and total phosphorus

(Fig. 2a, b) favoured taxa showing positive correlation

with TN (Fig. 3, see above), some of them (NAMP,

NGER, NVIR, NVRO, NPAL) belonging to motile

guild. Not only the number of taxa increased in motile

guild (Fig. 4b), but also some of the motile guild taxa

became characteristic due to their increasing individ-

ual numbers. The mean proportion and the taxa

number of low-profile guild decreased from May to

July (Fig. 4). However, this decrease of taxa number

continued in August as well (Fig 4b), but the relative

abundances of those low-profile guild taxa, which

significantly correlated with TN and conductivity

(ADEU, Cocconeis placentula —CPLA ssp., Fig. 3),

increased multiple in August (2.6- and 2.5-fold for

ADEU and CPLA spp., respectively), causing increas-

ing proportion of low-profile guild in these months

(Fig. 4a).

Water discharge was very low (Fig. 1), and TN

concentration reached almost its maximum (Fig. 2b)

in September. Proportions of both low-profile and

high-profile guilds were higher than in August

(Fig. 4a). On one hand, it was due to the increase of

some species’ relative abundances (2.4-fold for Cocc-

oneis species and 1.8-fold for Achnanthidium eutro-

philum in low-profile guild; 7.6-fold for Gomphonema

parvulum and 17.3-fold for Diatoma vulgaris in high-

profile guild) and on the other hand, due to the increase

of taxa number (Fig 4b). Meanwhile, proportion of

motile guild decreased from 0.73 to 0.40 (Fig. 4a) to

September, because of the decrease of relative abun-

dances of some motile guild taxa (Eolimna minima

(Grunow) Lange-Bertalot—EOMI, Nitzschia micro-

cephala Grunow—NMIC, Navicula schroeteri Mei-

ster—NSHR). Proportion of high-profile guild

decreased from September to October (Fig. 4a), due

to the decreasing relative abundances of Gomphonema

parvulum and Fragilaria species. Drastic decrease of

proportion of low-profile guild occurred due to

decreasing relative abundances of Cocconeis species

and the drastic decrease of taxa number (Fig. 4). In

contrast to decreasing proportion of high and low-

profile guilds, proportion of motile guild increased

from September to October due to increasing taxa

number in motile guild (Fig. 4) and increasing relative

abundance of Navicula capitatoradiata Germain. The

proportion of high-profile guild increased again from

October to November (Fig. 4a), mainly because of the

increasing relative abundance of Melosira varians and

Diatoma vulgaris and the increasing taxa number

(28%) (Fig. 4b).

The tendency changes of both the Berger–Parker

diversity and the number of taxa were the same in the

high water period (May and June; Fig. 5a). There were

many rare taxa detected (e. g. Reimeria uniseriata,

Rhoicosphenia abbreviata, Encyonopsis microcepha-

la, Diatoma ehrenbergii Kutzing, Pseudostaurosira

parasitica (W. Smith) Morales, Pseudostaurosira

parasitica var. subconstricta (Grunow) Morales,

Navicula radiosa Kutzing, Nitzschia dissipata, etc.),

which appeared only in these months. Later, there

were no significant correlation between taxa number

and BP diversity (Fig. 5). This is probably due to the

drastic changes in physical–chemical parameters

(from June to July/August; Figs. 1, 2), which led to

the reorganization of assemblages: some Navicula and

Nitzschia species became dominant with extremely

high abundance (e.g. Navicula viridula var. rostellata

31.5%; Nitzschia microcephala 20.5%) in July and/or

in August.

The index IPSITI reached its maximum in May (the

month with high water discharge and low TN

concentration—Fig. 5b.). Some taxa, which corre-

lated positively with water discharge (Achnanthidium

minutissimum and Encyonema silesiacum; Fig. 3),

were most abundant in this period. In July and August,

both the value of IPSITI and water discharge

decreased in correlation with increasing TN concen-

tration. In this period, taxa such as Nitzschia micro-

cephala, Diadesmis confervacea Kutzing, Navicula

viridula var. rostellata and Eolimna minima were

dominant.

Composition of diatom assemblages in running

and standing water segments

The species composition in the standing water

segments in September was clearly separated from

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the other months’ samples (Fig. 6), due to the high

relative abundance of Fragilaria bidens Heiberg

(FBID; up to 40%). Such marked separation among

the other samples was not detected (Fig. 6). We found

that Cocconeis placentula var. placentula Ehrenberg

(CPLA) and C. placentula Ehrenberg var. euglypta

(Ehrenberg) Grunow (CPLE) were characteristic in

running water segments (habitat more disturbed by

high water flow), whereas Fragilaria species sensu

lato and Nitzschia species were characteristic mostly

in standing water segments (slightly disturbed area by

water flow). The taxa number and Berger-Parker

diversity were the highest in September in the running

water segment, while they were the lowest in the

running water segment in October, where the domi-

nance of Navicula capitatoradiata reached 66%.

Similar to the species composition, the guild compo-

sition was also different in September: the proportion of

motile guild was lower (Fig. 7a) than in the other months.

Low-profile guild taxa, like Cocconeis species, and high-

profile guild taxa like Gomphonema parvulum were

characteristic in running water segments (higher water

flow disturbance), while Fragilaria bidens (high-profile

guild) and Achnanthidium eutrophilum (low-profile

guild) were characteristic in standing water segments

(less pronounced disturbance) in September (Fig. 7b).

Samples collected in October and November were

characterized mostly by motile guild taxa (Fig. 7a). A

low-profile guild species, Achnanthidium eutrophilum,

was also abundant in standing water segment in October

(Fig. 7b). Beside motile guild taxa (Navicula capitato-

radiata and Nitzshia dissipata), a high profile guild

species, Melosira varians, was also characteristic in

running water segment in November (Fig. 7b). Both the

guild composition and the taxa number of guilds differed

in September considerably from the others: in

Fig. 5 Values of the

national multimetric index

applied for Hungarian

streams (IPSITI), taxa

number (Taxa_S) and

Berger–Parker diversity

(Berger–Parker) during the

whole sampling period

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September, taxa numbers of every guild were the highest

in the running water segment (Fig. 7c). Value of IPSITI

was significantly higher in September in the running

water segment (dominant species were Navicula capi-

tatoradiata and Cocconeis placentula ssp.) than in the

standing water segment with high dominance of Ach-

nanthidium eutrophilum and Nitzschia microcephala

(Fig. 7c). In October and November, the taxa number of

low-profile guild was the highest in the standing water

segment (because of Cymbella and Encyonema species),

in contrast to the taxa number of high-profile guild, which

was higher in the running water segment (because of

Diadesmis species). There was no correlation between

the changes of guilds’ proportion, or taxa number and the

value of IPSITI (Fig. 7c).

Discussion

Monthly changes of diatom assemblages

We assumed that monthly guild ratios were primarily

influenced by the extremely changed water discharge

and TN concentration, because there were found

strong positive correlation between guild proportion

and ecological parameters in small rivers (Stenger-

Kovacs et al., 2013) and in lakes (Passy, 2007;

Gottschalk & Kahlert, 2012).

Our assumptions, that the proportion of low-profile

guild will be high and the proportion of high-profile

guild will be low in spring and early summer (period

with high water discharge), were confirmed by the

results. We found a strong positive correlation between

the relative abundances of Achnanthidium minutissi-

mum and Amphora pediculus and water discharge,

which might explain the increase of proportion of low-

profile guild in May and June, when ‘open’ surfaces can

be formed by the increasing water discharge found in

other studies (Koshmanesh et al., 1997). In our study,

both species were found in the highest of their relative

abundance in May and June, at high water discharge

and low TN (especially in June). These results suggest

that Achnanthidium minutissimum indicates low nutri-

ent levels and the same holds for Amphora pediculus as

well. Berthon et al. (2011) observed that the relative

abundance of Achnanthidium minutissimum only

slightly correlated with the trophic status. Others found

this species in high numbers in nutrient-poor areas (De

Fabricius et al., 2003; Kovacs et al., 2006; Gottschalk &

Kahlert, 2012). Taylor et al. (2007) found that

Achnanthidium minutissimum is characteristic in clear,

less-impacted waters. Nevertheless, preference of hab-

itats with low nutrient content cannot be shown as

clearly in the case of every taxa belonging to low-

profile guild. Other low-profile guild taxa (like

Amphora ovalis (Kutzing) Kutzing) indicate higher

TN concentration (Veraart et al., 2008; Stenger-Kovacs

et al., 2013). There are contrasting opinions about the

nutrient preferences of other taxa belonging to low-

profile guild. For instance, Gottschalk & Kahlert (2012)

suggest Amphora pediculus appears in nutrient-rich

environment, while others say that this species prefers

more nutrient-poor environment (Veraart et al., 2008).

Proportion of high-profile guild was relatively

higher than we expected in spring and early summer

despite to the high water discharge. This was caused

by the high relative abundances of Gomphonema

olivaceum from April to June (when TN decreased

from 2.1 to 1.1 mg l-1), in which species is otherwise

known as eutrophic species (Kovacs et al., 2006). We

found that relative abundances of G. olivaceum did not

show a positive correlation with TN, but it showed

Fig. 6 Relation of species composition of diatom assemblages

and water flowing conditions displayed by a DCA based on

relative species abundances. Large two-letter sample codes in

circles are the following: SS September, standing water

segment; SR September, running water segment; OS October,

standing water segment; OR October, running water segment;

NS November, standing water segment; NR November, running

water segment. The most abundant 30 species were shown using

four letter OMNIDIA codes

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positive correlation with water discharge. Clear

explanation of this phenomenon requires more

focused studies. Not surprisingly, proportion of

planktic guild increased with increasing water dis-

charge. This guild was barely detectable later, in low

water period (from July to September).

Fig. 7 Guild compositions

(a); relative abundances of

the dominant species (b) and

taxa numbers of the

respective guilds (c) in the

running water segment and

standing water segment

formed from September to

November. Species are

shown with their four letter

OMNIDIA codes

Hydrobiologia

123

We hypothesized that decreasing water discharge and

increasing nutrient (mainly TN) concentration from July

to September will increase the proportion of high-profile

guild, and decrease that of low-profile guild. We detected

that increasing nutrient concentration from July to

September really caused an increase in the proportion

of high-profile guild, but this change was not accompa-

nied with the decrease in that of low-profile guild.

However, the proportion of low-profile guild was high

under high TN level in September as well. The relative

abundance of several low-profile guild taxa (Achnanthi-

dium minutissimum, Amphora pediculus) showed a

strong negative correlation with TN. A stronger positive

effect of TN was detected only on the relative abundance

of Achnanthidium eutrophilum from low-profile guild.

These observations suggest that Achnanthidium minu-

tissimum and Achnanthidium eutrophilum, both belong-

ing to the Achnanthidium minutissimum species complex

and to the low-profile guild containing disturbance-

tolerant R-strategist species, have quite different ecolog-

ical demands. We observed that the relative abundance of

Achnanthidium minutissimum (mean width 1.5–3.3 lm,

linear lanceolate shape) increased with the decreasing

TN values, while relative abundance of this taxa had a

decrease with one order of magnitude, when the TN

levels increased. In contrast, the relative abundance of

Achnanthidium eutrophilum (mean width 2.1–4.4 lm,

rhombic shape) increased with the increasing TN. Acs

et al. (2006) also showed in their study for river Danube

that relative abundance of Achnanthidium minutissimum

was high under those circumstances which was charac-

terized by high disturbance due to high water discharge

and low TN concentration. De Fabricius et al. (2003)

found also higher relative abundance of Achnanthidium

minutissimum in river segments with low nutrient

contents (low nitrate and nitrite) than in segments with

high nutrient contents, studying the river Cuarto. Acs

et al. (2006) draw attention to the presence of several

variant of Achnanthidium minutissimum taxa with

different ecological demands. Results of Gottschalk &

Kahlert (2012) also suggest that there could be different

ecological demands for species with different morpho-

logical characteristics (i.e. cell size). Studying 73

Swedish lakes, they found that the relative abundance

of Achnanthidium minutissimum with a mean width

between 2.2 and 2.8 lm was higher in lakes with low

nutrient contents. The relative abundance of Achnanthi-

dium minutissimum wider than 2.8 lm was almost the

same in both nutrient-rich and nutrient-poor lakes.

High-profile guild taxa attached by stalks (Gom-

phonema species) prefer to uptake nutrients dissolved

in water than nutrients absorbed in substratum (Prin-

gle, 1990; Berthon et al., 2011). High-profile guild

taxa were dominant from September to November (at

high TN concentration and low water discharge). We

found that the relative abundance of G. parvulum

showed a positive correlation with TN. This species

was dominant in September (at high TN level). Similar

to our results, Gomphonema species were found in

nutrient-rich water earlier (Kovacs et al., 2006;

Gottschalk and Kahlert, 2012); however, in our case,

Gomphonema olivaceum showed different character-

istics (see above).

Motile guild taxa are present in high numbers in

nutrient-rich habitats as competitors (Fairchild et al.,

1985; Van der Grinten et al., 2004), having the ability

to leave the inappropriate habitats (Johnson et al.,

1997). The relative abundance of motile guild taxa

was high in April (when water discharge was

relatively low, and TN was relatively high), and then

(after a temporary decrease in May and June) it was

almost the highest, when water discharge decreased

nearly by 85% from June to July. This decrease in

water discharge was accompanied with a 64% increase

in TN simultaneously. The resulting circumstances

(mainly the higher nutrient content) were not advan-

tageous any more for low-profile guild taxa, but for

motile guild taxa. They are able to produce extracel-

lular enzymes (Pringle, 1990), so presumably they

have higher nutrient uptake rates than low-profile

guild. Further decline of water discharge and increas-

ing TN favoured to increase the individual number of

high-profile guild taxa, which can explain the decrease

of taxa number and proportion of motile guild in

September. Relative abundance of motile guild

increased again in October and November, probably

due to competitive skills of the species.

Composition of diatom assemblages in running

and standing water segments

We assumed that the species composition is different

in running and standing water segments in a given

month. Fragilaria bidens was the most characteristic

to standing water segments in September. Although,

such clear separation was not revealed in the case of

the other samples based on taxa composition, Cocc-

oneis placentula var. placentula, C. placentula var.

Hydrobiologia

123

euglypta and Gomphonema species were characteris-

tic mainly to running water segments. Cocconeis

species able to adapt easily to disturbed circumstances

(Passy, 2007; Stenger-Kovacs et al., 2013), which

explains their presence in running water segments.

Since Gomphonema parvulum and Gomphonema

pumilum (Grunow) Reichardt & Lange-Bertalot are

known as nutrient-rich water preferring taxa (Kovacs

et al., 2006; Gottschalk & Kahlert, 2012), it explains

the high relative abundance of these species in

September (month with high TN concentration). TN

concentrations were the highest in October and

November. Certain taxa usually appear in nutrient-

rich water (Passy, 2007; Berthon et al., 2011; Gotts-

chalk & Kahlert, 2012; Stenger-Kovacs et al., 2013),

which explains the dominance of Diadesmis conferv-

acea in October and Melosira varians and Diatoma

vulgaris in November in running water segment.

Melosira varians and Diatoma vulgaris, similarly to

Cocconeis species, are able to adapt to high distur-

bances (R-strategy—Passy, 2007). These disturbances

were caused by high flow in the running water

segments. Moreover, we observed an interesting

phenomenon in the case of A. minutissimum and A.

eutrophilum: the proportion of A. minutissimum and A.

eutrophilum differed in samples collected from stand-

ing and running water segments in autumn: relative

abundance of A. minutissimum was higher in running

water segments. Conversely, the relative abundance of

A. eutrophilum was higher in standing water segments.

Because of the riverbed morphology and low water

discharge, fast water flow appeared in running water

segments. This was favourable for Achnanthidium

minutissimum, which are tolerant to physical distur-

bance (Passy, 2007; Berthon et al., 2011; Passy &

Larson, 2011). In contrast, we supposed that appear-

ance of Achnanthidium eutrophilum was defined

primarily by nutrients and not physical disturbances.

Potapova & Hamilton (2007) also reported Achnan-

thidium eutrophilum with higher relative abundance at

nutrient-rich habitats. These observations also confirm

the possible necessity of revising their current classi-

fication into guilds.

We assumed that running and standing water

segments can be characterized with different guild

ratios. These expectations were not confirmed by the

results. Taxa did not appear in the different segments

according to their guild affiliation. Rather, it was

observed that each genus—regardless of their

belonging to guilds—preferred more one or the other

segment. Within low-profile guild Cocconeis species,

which are known as R-strategist (see above), appeared

in running water segment with higher abundance.

Cymbella and Encyonema species—also belonging to

low-profile guild, which can form colonies and tubes

or can be stalked (Berthon et al., 2011)—preferred the

standing water segment. Similar contradictions

occurred in the high-profile guild as well: Fragilaria

species—except F. capucina var. vaucheriae (Kut-

zing) Lange-Bertalot—were found in standing water

segment with high abundance, in contrast Diatoma

vulgaris and Melosira varians were abundant in

running water segment. Each of these taxa are known

as colonial and/or stalked species (Berthon et al.,

2011). Overall, it seems that preferences and life forms

of given species or genera defined the taxa composi-

tion of segments, regardless to their current guild

affiliation.

Conclusions

Our results confirmed that the proportion of low-

profile guild increased with decreasing nutrient avail-

ability (increasing water discharge), and the propor-

tion of high-profile guild was lower in periods with

high water discharge and low nutrient availability.

Changes of relative abundance of motile guild

confirmed current knowledge that motile guild pre-

ferred nutrient-rich habitats and relatively sensitive to

increased water discharge. Our results suggest that

differences in seasonal patterns and compositional

changes are well reflected by the ecological guilds.

The expectation that running and standing water

segments can be characterized with different guild

ratios was not supported by the results. Our findings

for the relatively short time at the presence of

segments (from September to November) suggested

that further refinement of guild concept was necessary

based on life strategies (CSR model), life forms, and

more current knowledge about nutrient preferences of

taxa.

Our findings clearly indicate that there is a great

potential in the use of diatom guilds for environmental

status assessment. However, our results also suggest

that subdivisions within the current guilds are neces-

sary to make them more feasible for environmental

status assessment. Based on the results presented here

Hydrobiologia

123

and in literature data, the creation of subdivisions

within the low-profile guild could be based on the

nutrient preference of certain taxa. In light of this, a

subgroup in low-profile guild should include first

colonizers/pioneer species, which prefer low nutrient

concentration (e.g. Achnanthidium minutissiumum,

Encyonema and Cymbella species), another subgroup

should contain taxa, which are tolerant to disturbance

and tolerate or require higher nutrient contents (e.g.

Cocconeis placentula varietas, A. eutrophilum). Sub-

groups of high-profile guild may be based on the

disturbance tolerance and life forms of taxa. A

subgroup in high-profile guild should contain taxa

which can be characterized with high nutrient require-

ments and high disturbance tolerance (e.g. Diatoma

species, Melosira varians), an other subgroup in high-

profile guild should include taxa with low disturbance

tolerance (e.g. Fragilaria species). Based on our data,

similar subdivisions cannot be proposed for motile and

planktic guilds, but future research may indicate the

necessity of splitting also these guilds to several

subdivisions. It is pertinent to emphasize that the

confirmation of these suggestions definitely requires

further studies. More precise definitions of life forms,

life strategies and ecological needs of certain taxa are

strictly necessary for this kind of work, to which the

data presented in this work may be contributed.

Acknowledgments The authors are thankful for the support of

the Bolyai Janos Research Scholarship of the Hungarian Academy

of Sciences (Bacsi I.), Internal Research Project of the University of

Debrecen (Bacsi I.) and Hungarian Scientific Research Found PD

100192 (Torok P.) during manuscript preparation. The work was

supported by TAMOP 4.2.1./B-09/1/KONV-2010-0007, TAMOP-

4.2.2/B-10/1-2010-0024, TAMOP 4.2.2.C-11/1/KONV-2012-0010

and TAMOP 4.2.4.A/2-11-1-2012-0001 ‘National Excellence

Program—Elaborating and operating an inland student and

researcher personal support system’, projects. The TAMOP

projects are implemented through the New Hungary Development

Plan, co-financed by the European Social Fund and the European

Regional Development Fund. The authors are thankful for

measuring the physical and chemical parameters to the

Environmental Protection and Nature Conservation Authority,

Trans-Tisza Region, for water discharge data and rainfall data to the

National Water Authority and to the Hungarian Meteorological

Service.

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