RESEARCH PAPER

Spatiotemporal changes in diatom ecological profiles:implications for biomonitoring

Irene Alvarez-Blanco • Cristina Cejudo-Figueiras •

Eloy Becares • Saul Blanco

Received: 1 July 2010 / Accepted: 5 September 2010 / Published online: 29 September 2010

� The Japanese Society of Limnology 2010

Abstract Diatom indices developed in certain geographic

regions are frequently used elsewhere, despite the strong

evidence that such metrics are less useful when applied in

regions other than that where species–environment rela-

tionships were originally assessed, showing that species

have particular autoecological requirements in different

geographic areas. In this study, we define the ecological

profiles for selected environmental variables in three

common epilithic diatom species in the Duero Basin (NW

Spain), comparing our results with data gathered from

different geographic regions. We assess differences in

autoecological parameters obtained from the northern and

southern subbasins, and from different years, in order to

observe whether significant small-scale, spatiotemporal

changes exist. Our results show that there are variations

in species’ autoecological parameters between different

regions. Furthermore, there are significant changes com-

paring northern and southern Duero subbasins for certain

species and physiochemical variables. Additionally, dif-

ferent autoecologies have been observed for certain di-

atoms and environmental factors comparing two different

years. It can be concluded that freshwater diatom auto-

ecologies can vary between different geographic areas. This

implies that, in order to improve water-quality bioassess-

ments, autoecology-based diatom metrics should be

developed by quantifying species distributions along

environmental gradients, using datasets representative of

the areas or river types where the metrics will be applied.

Keywords Autoecology � Response curves �Bioindicators � Ecological indices

Introduction

Diatoms have been widely used for water quality assess-

ment in rivers and lakes around the world, considering their

sensitivity to water physical and chemical parameters,

especially pH, conductivity, nutrient concentration, organic

matter, and dissolved oxygen (e.g., Eloranta and Soininen

2002; Blanco et al. 2004; Levkov et al. 2007). Diatom

metrics allow numeric values to be assigned as measures of

the response of species to abiotic factors to obtain a

quantitative water quality bioassessment (Pan et al. 1996;

Rott et al. 1997; Potapova et al. 2004). Two major

advantages of turning diatoms into good indicator organ-

isms are their wide geographical distribution and the well-

known autoecology of most species. However, the question

of whether diatom-based metrics developed for a specific

area could be applied to other regions has been poorly

explored. Several studies carried out in the Iberian Penin-

sula have demonstrated that the specific pollution index

(SPI), developed for Central European watercourses, is an

effective tool for water quality assessment in Mediterra-

nean streams (Almeida 2001; Goma et al. 2004; Blanco

et al. 2008).

Nevertheless, different studies emphasize the impor-

tance of the ecological indicator values that each taxon

exhibits in its natural habitat (Rimet et al. 2004; Charles

et al. 2006). Particularly, there is evidence that an index

related to a particular geographic region is less effective

when applied elsewhere (Pipp 2002). This is due not only

to the diverse floristic spectra found in areas where the

index is applied, but also to environmental differences

I. Alvarez-Blanco � C. Cejudo-Figueiras � E. Becares �S. Blanco (&)

Department of Biodiversity and Environmental Management,

University of Leon, 24071 Leon, Spain

e-mail: sblal@unileon.es

123

Limnology (2011) 12:157–168

DOI 10.1007/s10201-010-0333-1

between zones that modify species response to water

physical and chemical variables. Therefore, if ecological

profiles depend on environmental characteristics, this puts

at risk any plausible extrapolation of indices. This study

focuses on checking this hypothesis and warning about the

possible problematics of indices extrapolation. We define

the ecological profile of three common epilithic diatom

species in the Duero Basin (NW Spain) for selected envi-

ronmental variables, comparing our results with data

gathered from different geographic regions. Furthermore,

we compare the autoecological values obtained from dif-

ferent regions within this basin, and from different years, to

assess the presence of significant changes at small spatio-

temporal scales.

Materials and methods

Study area

The Duero Basin (97,290 km2) is the largest hydrograph-

ical basin on the Iberian Peninsula (Fig. 1). This study was

carried out in the Spanish part of the basin (78,952 km2).

From a geological point of view, this basin consists of a

plateau mostly formed by Tertiary and Quaternary (alluvial

and colluvial) materials, with an average altitude [700 m

a.s.l. (Garcıa and Gonzalez 1986). Most of the basin is

situated under Mediterranean bioclimate, here character-

ized by a strong continental character, with dry summers

and cold winters. Mean annual precipitation is 625 mm,

concentrated in autumn and winter, whereas there is a

pronounced summer rainfall deficit.

Methodology

Samples were collected during summers 2004, 2005, and

2007 along the rivers of the Duero Basin at 397 sites

selected from the Water Quality Surveillance Network of

the Duero Basin Authority (CHD). Water chemical vari-

ables were provided by the CHD automatic water sampling

stations at each site. Epilithic diatom samples were

collected and processed following Spanish standards

[Asociacion Espanola de Normalizacion y Certificacion

(AENOR) 2004]. Permanent microscopic slides were

obtained and diatom taxa were identified and counted fol-

lowing Spanish standards (AENOR 2005). Achnanthidium

pyrenaicum (Hustedt) Kobayasi, Navicula tripunctata

(O.F. Muller) Bory, and Eolimna minima (Grunow) Lange-

Bertalot were the selected species for this study due to their

relatively high abundance and occurrence frequencies in

analyzed samples. Furthermore, these species are near-

cosmopolite and relatively easy to identify, thus allowing

comparative analyses, and demonstrate different auto-

ecological patterns, as they develop preferentially in

oligotraphentic, mesotraphentic, and eutraphentic waters,

respectively. Table 1 shows the ecological classification of

these taxa according to different authors.

Species optima, tolerances, and ranges were calculated

with respect to main limnological variables: pH, con-

ductivity, biological oxygen demand (BOD5), [NH4?–N],

[NO3-–N], [PO4

3-–P], using weighted averages method

(Birks et al. 1990; Denys 2004), where a taxon’s optimum

for a certain environmental variable is the mean of the

variable values at sites where the taxon is present,

weighted by the taxon’s abundance in analyzed samples.

Correspondingly, the environmental tolerance of the taxon

is the weighted standard deviation. The range comprises

the maximum and minimum values for the selected

environmental variable. These values were calculated for

the entire data set, specifically for the samples collected

in 2004 and 2005, and independently for sites located at

the northern and southern subbasins. Resulting data were

statistically compared using weighted comparison of

means (Bland and Kerry 1998). For each studied species,

ecological profiles were represented graphically adjusting

relative abundances to normal distribution curves by

Fig. 1 Geographic location of

the study site

158 Limnology (2011) 12:157–168

123

means of Levenberg–Marquardt nonlinear regression algo-

rithm (More 1977). Statistical analyses were performed using

Statistica 7.0 (StatSoft 2004).

Results

The ecological categories assigned by different authors to

each studied species are shown in Table 1. Especially rele-

vant differences have been observed for A. pyrenaicum,

whereas the sortings for N. tripunctata and E. minima are

more homogeneous. Saprobity levels assigned to N. tri-

punctata are different from one another, whereas the trophic

status categories for this species and for E. minima are sig-

nificantly homogeneous. The rank of values exhibited by the

analyzed variables on each study is presented in Table 2.

Tables 3, 4, and 5 show the autoecological parameters

(optimum and range) calculated for analyzed species at

different regions of the world. Most optima values collected

fall near the median of the rank, thus indicating the presence

of this species under suboptimal conditions within the rank of

conditions explored in each study. The pH optima for the

three diatom species vary around neutrality. Achnanthidium

pyrenaicum has a pH optimum between 6.28 and 8.40,

however N. tripunctata has a pH optimum skewed toward the

alkaline side of the pH spectrum (7.31–8.40). Eolimna

minima has lower pH optimum, although its values cover a

wider range in studied data sets. High differences in con-

ductivity optima have been observed: the optimum for

E. minima varies from 20.62 lS cm-1 in Pyrenean lakes to

2,746.77 lS cm-1 in northern African lakes. This species

has been observed within a wide range of conductivities in

Africa (from 40.00 to 13,500.00 lS cm-1). With respect to

total phosphorus (TP) optima, the highest variability was

recorded for E. minima, whose optimum for this parameter

varies from 6.4 lg L-1 in Russian lakes to 426.29 lg L-1 in

Ireland. Total nitrogen (TN) optima show distinct value

ranges for each species, particularly N. tripunctata, which

has an optimum of 820 lg L-1 in the Pacific Northwest

(USA), whereas it is [2,500 lg L-1 in the Swiss Alps. In

general, ammonium optima show a lower variability within

studied taxa. The scarcity of data for BOD5 and nitrate and

phosphate concentrations prevent further comparative

analyses.

Interannual (2004–2005) variation in the ecological

profiles of studied species for selected environmental

parameters has been analyzed, showing some significant

statistical changes (Fig. 2). In the case of A. pyrenaicum,

only its pH optimum has a significant interannual variation

(Fig. 2a; Table 6), occurring at slightly more acidic waters

in 2005. Eolimna minima has a significant temporal vari-

ation with respect to conductivity optima. In 2004, this

Table 1 Ecological classification of studied species according to different authors

Lowe (1974) Van Dam et al.

(1994)

Hofmann (1993) Lujan (personal

communication)

Taylor et al. (2007) Lange-Bertalot

(2001)

Achnanthidium pyrenaicum

pH – Alkaliphilous Alkalibiontic Circumneutral – –

Conductivity – – Moderate Low Moderate high –

Trophic

status

– Mesotraphentic – – Oligo-

mesotraphentic

–

Saprobity – – b-Mesosaprobous a-b-

Mesosaprobous

– –

Navicula tripunctata

pH Alkaliphilous Alkaliphilous Alkaliphilous–

Alkalibiontic

Indifferent – –

Conductivity Eurihalobious – Moderate high – Moderate high Moderate high

Trophic

status

Eutraphentic Eutraphentic Eutraphentic – Eutraphentic Eutraphentic

Saprobity Oligosaprobous b-Mesosaprobous a-b-Mesosaprobous b-Mesosaprobous – a-b-

Mesosaprobous

Eolimna minima

pH Alkaliphilous Alkaliphilous – – – –

Conductivity Indifferent – – – – –

Trophic

status

Eutraphentic Eutraphentic – – – –

Saprobity Oligosaprobous a-

Mesopolisaprobous

– – a-

Mesopolisaprobous

–

Limnology (2011) 12:157–168 159

123

Table 2 Range of values shown by the analyzed variables in different studies

pH Conductivity

(lS cm-1)

BOD5

(mg

O2 L-1)

[NH4?–N]

(mg L-1)

[NO3-–N]

(mg L-1)

[PO43-–P]

(mg L-1)

TP (lg L-1) TN (lg L-1)

Duero Basin (Spain)1 6.33–8.62 20.00–1142.67 0.00–9.00 0.00–28.30 0.00–27.48 0.00–8.17 – –

Hungary and Sweden2 4.80–8.90 156.00–104,950.00 – 0.00–8.90 – 0.00–2.20 0.00–929.00 –

Pyrenees3 5.50–7.46 4.40–38.50 – 0.22–3.08 0.40–18.12 – 2.17–23.50 –

Centroeurope4 6.80–8.50 58.00–498.00 – 0.00–0.88 – – 2.00–266.00 –

Ireland5 5.10–8.50 33.00–462.00 – – – – 0.00–142.30 –

Eastern USA6 3.40–8.80 – 0.10–29.00 0.00–4.90 0.00–100.00 – 3.00–796.00 –

New Jersey (USA)7 6.50–9.00 51.00–983.00 – – 10.00–7,992.00 – 6.00–731.00 170.00–8,547.00

Ohio (USA)8 2.40–7.90 215.00–6,470.00 – – 0.00–1.50 0.02–0.70 – –

Mid-Atlantic Highlands

(USA)9

4.21–8.68 17.70–1,860.00 – – – – 3.00–472.00 140.00–6,090.00

Finland10 5.00–7.70 6.40–46.70 – – – – – –

Fennoscandia11 5.00–8.30 13.60–53.50 – – – – – –

Ireland12 7.09–8.60 93.00–626.00 – 0.01–1.11 0.03–3.26 – 11.00–800.00 330.00–2,230.00

Wales13 6.35–8.61 27.50–442.00 – – 0.02–0.7 – 5.28–1,085.00 –

England14 6.83–8.59 206.00–1,327.00 – – 0.70–5.58 – 25.50–646.00 –

Kola Peninsula (Russia)15 5.00–7.44 8.00–88.00 – – – – 2.00–17.00 94.00–470.00

Europe16 4.33–7.25 7.37–154.00 – – 0.00–0.09 – 5.00–31.00 10.00–982.00

Africa17 5.50–10.90 40.00–47,680.00 – – – – 16.00–50.00 –

North Africa18 5.50–9.10 345–400,000.00 – – – – 20.00–20.00 –

BOD5 biological oxygen demand, TP total phosphorus, TN total nitrogen

References: 1This study; 2Kovacs et al. (2006); 3Catalan et al. (1993); 4Wunsam and Schmidt (1995); 5Chen et al. (2007); 6Charles et al. (2006); 7Ponader

et al. (2007); 8Verb and Vis (2005); 9Pan et al. (1996); 10Weckstrom et al. (1997); 11Korsman and Birks (1996); 12Bennion et al. (1996); 13Bennion (1995);14Bennion (1993); 15Solovieva (2000); 16Stevenson et al. (1991); 17Gasse (1986); 18Gasse et al. (1987)

Table 3 Autoecological parameters [optimum (range)] of Achnanthidium pyrenaicum

No. pH Conductivity

(lS cm-1)

BOD5

(mg O2 L-1)

[NH4?–N]

(mg L-1)

[NO3-–N]

(mg L-1)

[PO43-–P]

(mg L-1)

TP (lg L-1) TN (lg L-1)

Duero Basin

(Spain)1150 7.70

(6.36–8.30)

203.28

(20.00–885.00)

0.14

(0.00–6.00)

0.02

(0.00–3.10)

1.82

(0.00–24.70)

0.02

(0.00–2.23)

– –

Hungary and

Sweden26 7.70 – – – – – – –

Pacific NW

(USA)3214 7.30 101.00 – 0.02 – – 10.00 20.00

NW USA4 355 7.30 87.00 – 0.03 – 0.01 0.02 –

Pyrenees5 98 6.91

(6.84–6.94)

17.13

(14.70–18.60)

– 0.65

(0.54–0.85)

– – 11.07

(5.58–23.23)

–

France6 28 6.28

(5.20–7.41)

66.86

(16.50–143.75)

– – – – 23.41

(5.10–52.45)

–

Swiss Alps7 77 8.28

(7.65–8.90)

235.18

(100.00–564.75)

– – – – 24.35

(5.80–85.75)

910.44

(200.00–6880.00)

Centroeurope8 86 8.15

(7.50–8.30)

254.64

(177.00–432.00)

– 0.04

(0.02–0.55)

0.24

(0.05–0.99)

– 12.24

(8.00–144.00)

–

Alps9 118 6.79

(6.56–6.94)

17.12

(14.70–18.60)

– 0.59

(0.47–0.85)

– – 7.55

(0.50–23.23)

245.00

(245.00–245.00)

No. no. of samples where the species is present

BOD5 biological oxygen demand, TP total phosphorus, TN total nitrogen

References: 1This study; 2Kovacs et al. (2006); 3L. Bahls (personal communication); 4Bahls (2006); 5Catalan et al. (1993); 6Rioual (2000); 7Lotter et al. (1998);8Wunsam and Schmidt (1995); 9N. Cameron (personal communication)

160 Limnology (2011) 12:157–168

123

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Limnology (2011) 12:157–168 161

123

species appears more frequently in sites with lower con-

ductivities than in 2005 (Fig. 2b; Table 6). Navicula

tripunctata seems to have larger fluctuations in its auto-

ecological preferences over time. Significant statistical

differences in its abundance from 2004 to 2005 were

observed for BOD5, ammonium, nitrate, and phosphate

concentrations (Fig. 2c–f; Table 6).

Likewise, intrabasin variations in the ecological profiles

were assessed. Achnanthidium pyrenaicum is more widely

distributed in the northern subbasin and, additionally, there

develops in waters with lower conductivities and BOD5

levels than in the southern subbasin. Only these parameters

demonstrated statistically significant differences between

both regions (Fig. 3b, c; Table 6). Significant spatial fluc-

tuations in the ecological profile of E. minima for nitrate

concentration and conductivity were observed (Fig. 3b, f;

Table 6). This species develops at lower levels of both

variables in the southern region. Finally, ecological pref-

erences at spatial scale of N. tripunctata have a significant

variation for most of the studied environmental parameters,

with the exception of BOD5 (Fig. 3c). This taxon does not

have clear preferences for particular pH levels or ammo-

nium and phosphate concentrations in the southern part of

the basin, though higher abundances of N. tripunctata at

lower levels of conductivity and nitrate concentrations

were observed in this region.

Discussion

Our results demonstrate both spatial and temporal vari-

abilities in the autoecological spectra of common and

widely distributed diatom species. Most of these variations

can be considered ecologically relevant, as they imply

changes in the autoecological classification of the species,

according to the criteria presented by several authors (e.g.,

Lowe 1974; Hofmann 1993; Van Dam et al. 1994). For

instance, the BOD5 optimum for N. tripunctata increased

up to 260% between 2004 and 2005, so that the species

shifted from indicating oligosaprobic to near b-mesosapr-

obic conditions.

Spatial variation has been assessed on a large scale

comparing remote geographic regions, and on a small

scale, evidencing significant differences within a single

hydrographic basin. Analogue results have been found in

other studies; e.g., patterns of diatom distribution against

several environmental variables were analyzed by Winter

and Duthie (2000) in streams from southern Ontario,

Canada. These authors observed how species optima and

tolerances vary geographically and between different hab-

itats. Charles et al. (2006) studied large-scale regional

variations in diatom–water chemistry relationships in rivers

of the eastern United States, addressing considerable geo-

graphic variations in the ecological characteristics of many

taxa.

In general, diatom ecological patterns are complex and

difficult to quantify and interpret, and consequently, pre-

cise ecological data should be calculated for each geo-

graphic region. The factors leading to such interregional

variability in diatom ecological profiles are several.

According to Charles et al. (2006), this could be due to the

presence of environmental variables differently restricting

the distribution of taxa in different regions, or to a certain

genetic variability related to the coexistence of different

Table 5 Ecology parameters [optimum (range)] of Navicula tripunctata

No. pH Conductivity

(lS cm-1)

BOD5

(mg O2 L-1)

[NH4?–N]

(mg L-1)

[NO3-–N]

(mg L-1)

[PO43-–P]

(mg L-1)

TP (lg L-1) TN (lg L-1)

Duero Basin

(Spain)1141 7.66

(6.33–8.62)

379.25

(27.00–1,076.00)

0.85

(0.00–8.13)

0.18

(0.00–3.74)

8.24

(0.00–27.48)

0.22

(0.00–1.80)

– –

Ireland2 72 7.90 – – – – – 34.60 –

SW Montana

(USA)3289 8.40

(7.70–8.72)

662.00

(239.00–6,100.00)

1.40

(0.50–3.60)

0.01

(0.01–0.30)

– 0.01

(0.00–2.50)

0.02 (0.01–3.70) –

Pacific NW

(USA)4650 7.40 230.00 – 0.21 – – 210.00 820.00

East USA5 35 7.50 – 1.60 – – – – –

New Jersey

(USA)6– – – – – – – 45.84 1,266.25

Ohio (USA)7 22 7.31 – – – – – – –

Swiss Alps8 77 8.16

(8.04–8.40)

391.68

(256.20–544.67)

– – – – 63.19

(22.00–211.00)

2,534.29

(560.00–6160.00)

England9 33 7.95

(7.81–8.13)

668.79

(608.00–723.5.00)

– – – – 348.90

(247.24–468.16)

–

No. no. of samples where the species is present

BOD5 biological oxygen demand, TP total phosphorus, TN total nitrogen

References: 1This study; 2Chen et al. (2007); 3Bahls et al. (1984); 4L. Bahls (personal communication); 5Charles et al. (2006); 6Ponader et al. (2007); 7Verb and Vis

(2005); 8Lotter et al. (1998); 9Bennion (1993)

162 Limnology (2011) 12:157–168

123

3210

[PO43--P] (mg·L-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

7.0 7.5 8.0

pH

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

A. pyrenaicum E. minima N. tripunctata

8006004002000

Conductivity (µ S·cm-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

1086420

[NH4+-N] (mg·L-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

1086420

BOD5 (mg O2·L-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

20151050[NO3

--N] (mg·L-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

ba

dc

fe

Fig. 2 Response curves of studied diatom species against selected environmental variables. Data (omitted) fitted to normal regression curves.

Black lines: 2004 data. Grey lines: 2005 data

Limnology (2011) 12:157–168 163

123

cryptic species. This last possibility is also considered by

other authors (e.g., Nygaard 1996; Resende et al. 2005). In

our study, it cannot be ignored that several species with

different autoecologies could have been included inside our

taxonomic concept of A. pyrenaicum or E. minima (Fig. 4).

In particular, A. pyrenaicum may be misidentified as other

similar species, such as A. subatomus (Hustedt) Lange-

Bertalot, A. rivulare Potatova & Ponader, Achnanthes

thienemannii Hustedt, or Rossithidium pusillum (Grunow)

Round & Bukhtiyarova. In turn, E. minima is very similar

to Sellaphora seminulum (Grunow) Mann and S. joubaudii

(Germain) Aboal. Correspondingly, it is possible that their

different optima found in the literature are related to

incorrect taxonomic identifications. However, this argu-

ment cannot be supported in our case, as all these species

were actually identified in the inventories and clearly dis-

criminated from the species here studied.

The study of diatom autoecology provides the basis for

the development of diatom-based bioassessment indices,

which are based on the relative abundance of each taxon,

its sensitivity to environmental stressors, and its ecological

amplitude. Hence, several diatom indices have been pro-

posed for different world regions, e.g., the biological di-

atom index (BDI, Lenoir and Coste 1996) in France, the

Trophic Diatom Index (TDI, Kelly and Whitton 1995) in

the UK, or the Eutrophication Pollution Index (EPI-D,

Dell’Uomo 2004) in Italy. These metrics have been

implemented from surveys performed on particular geo-

graphic areas but subsequently applied elsewhere very

often. There is evidence, however, that resulting water

quality assessments are less successful (Blanco et al. 2007).

For instance, it becomes critical that dominant taxa are

considered when computing the metric (Lobo et al. 1996).

Regarding this, SPI index (CEMAGREF 1982), though

initially developed for French streams, gathers virtually all

known freshwater taxa (Rimet et al. 2004), and it has

therefore been used for ecological assessments not only in

Europe (Eloranta and Soininen 2002, Acs et al. 2004,

Blanco et al. 2008), but also in South Africa (de la Rey

et al. 2004) and Argentina (Gomez and Licursi 2001).

Other European indices such as the TDI have been suc-

cessfully employed worldwide (Belton et al. 2005; Dela-

Cruz et al. 2006; Bellinger et al. 2006).

If ecological preferences of individual taxa vary within

spatial scales and along major environmental gradients,

diatom indication methods are less effective when applied

in very different regions, although they can show, in some

cases, acceptable performances. However, in order to

Table 6 Ecology parameters [optimum (range)] of the studied species in the Duero Basin for the different years and regions analyzed

pH Conductivity (lS cm-1) BOD5 (mg O2 L-1) [NH4?–N] (mg L-1) [NO3

-–N] (mg L-1) [PO43-–P] (mg L-1)

A. pyrenaicum

2004 7.71 (6.36–8.11) 204.82 (23.00–620.67) 0.21 (0.00–5.83) 0.01 (0.00–0.23) 1.42 (0.00–17.61) 0.03 (0.00–0.88)

2005 7.56 (6.95–7.96) 184.84 (48.00–750.67) 0.03 (0.00–5.57) 0.01 (0.00–3.10) 1.29 (0.00–10.07) 0.02 (0.00–1.67)

2.88 (<0.01) 0.91 (0.37) 1.90 (0.06) 0.15 (0.88) 0.40 (0.69) 0.57 (0.57)

North 7.72 (6.36–8.30) 203.33 (20.00–750.67) 0.10 (0.00–6.00) 0.01 (0.00–0.48) 1.81 (0.00–24.70) 0.02 (0.00–2.23)

South 7.76 (6.97–8.30) 341.96 (31.00–885.00) 0.73 (0.00–5.83) 0.06 (0.00–3.10) 0.77 (0.00–9.56) 0.08 (0.00–1.67)

0.59 (0.55) 5.09 (<0.01) 4.01 (<0.01) 1.97 (0.05) 1.39 (0.17) 1.97 (0.05)

E. minima

2004 7.47 (6.33–8.13) 276.33 (22.67–844.00) 1.85 (0.00–8.13) 0.27 (0.00–2.39) 6.68 (0.00–27.48) 0.48 (0.00–1.80)

2005 7.53 (6.76–8.62) 348.79 (31.00–808.00) 1.57 (0.00–8.77) 0.62 (0.00–13.87) 6.72 (0.00–14.13) 0.59 (0.00–3.00)

0.77 (0.44) 2.21 (0.03) 0.71 (0.48) 1.31 (0.19) 0.06 (0.95) 0.92 (0.36)

North 7.60 (6.50–8.20) 368.77 (20.00–844.00) 1.70 (0.00–8.13) 0.36 (0.00–13.87) 7.16 (0.00–27.48) 0.36 (0.00–3.00)

South 7.48 (6.33–8.30) 166.43 (24.00–885.00) 1.58 (0.00–9.00) 0.29 (0.00–9.49) 4.23 (0.00–13.86) 0.59 (0.00–2.88)

1.81 (0.07) 7.62 (<0.01) 0.32 (0.75) 0.33 (0.74) 3.52 (<0.01) 0.41 (0.69)

N. tripunctata

2004 7.62 (6.33–8.13) 382.94 (27.00–1076.00) 0.62 (0.00–8.13) 0.10 (0.00–2.39) 9.64 (0.00–27.48) 0.18 (0.00–1.80)

2005 7.59 (7.11–8.62) 358.91 (125.67–808.00) 1.61 (0.00–5.57) 0.53 (0.00–3.74) 5.53 (0.00–14.13) 0.38 (0.00–1.61)

0.29 (0.77) 0.55 (0.58) 2.87 (0.01) 2.75 (0.01) 2.64 (0.01) 2.39 (0.02)

North 7.69 (6.60–8.20) 429.35 (37.33–1076.00) 0.64 (0.00–8.13) 0.08 (0.00–2.39) 10.3 (0.00–27.48) 0.18 (0.00–1.80)

South 7.45 (6.33–8.30) 227.57 (27.00–548.00) 0.81 (0.00–5.33) 0.41 (0.00–3.74) 2.35 (0.00–13.86) 0.39 (0.00–1.61)

2.74 (0.01) 4.17 (<0.01) 0.51 (0.61) 2.61 (0.01) 4.06 (<0.01) 2.59 (0.01)

BOD5 biological oxygen demand

Weighted comparison of means of ecological optima (t statistic and p values) are shown in italics. Significant values (p \ 0.05) highlighted in

bold

164 Limnology (2011) 12:157–168

123

8006004002000

Conductivity (µ S·cm-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

1086420

[NH4+-N] (mg·L-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

20151050

[NO3--N] (mg·L-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

3210

[PO43--P] (mg·L-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

1086420

BOD5 (mg O2·L-1)

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

7.0 7.5 8.0pH

0

10

20

30

40

50

60

Ab

un

dan

ce (

%)

A. pyrenaicum E. minima N. tripunctata

ba

dc

fe

Fig. 3 Response curves of studied diatom species against selected environmental variables. Data (omitted) fitted to normal regression curves.

Black lines: northern subbasin data. Grey lines: southern subbasin data

Limnology (2011) 12:157–168 165

123

design optimal water quality assessment tools, it is

recommended to adapt such metrics to the ecoregional and

river typological particularities of each basin (Rimet et al.

2004, 2005). For instance, Kovas et al. (2007) developed a

new index for Hungarian shallow lakes (Trophic Diatom

Index for Lakes, TDIL), and Potapova and Charles (2007)

designed the NAWQ diatom index for monitoring eutro-

phication in North American rivers. Both new, specific

metrics provide more accurate results than usual diatom

indices.

It can be concluded that freshwater diatom ecological

profiles can vary along both spatial and temporal scales.

This implies that in order to improve water quality bioas-

sessments, autoecology-based diatom metrics should be

developed by quantifying species distributions along

regional environmental gradients, using data sets repre-

sentative of the basins or river types where the metrics will

be applied. Further studies on the ecological preferences of

diatom assemblages within different world regions will

allow development of better diatom-based monitoring

methods for freshwater ecosystem health diagnosis.

Acknowledgments This study was funded by the Duero Basin

Authority, Spain (CHD, Confederacion Hidrografica del Duero)

through the contract Servicio para la elaboracion de un atlas dediatomeas bentonicas de la Cuenca del Duero (fase III de III).Authors are indebted to L. Bahls, N. Cameron, and A. Lujan who

kindly provided data shown in Tables 1–4. Two anonymous referees

are thanked for their valuable comments on the manuscript.

References

Acs E, Szabo K, Toth B, Kiss KT (2004) Investigations of benthic

algal communities, especially diatoms of some Hungarian

streams in connection with reference conditions of the water

framework directives. Acta Bot Hung 46:255–278

AENOR (2004) Norma espanola UNE-EN 13946: 2004 Calidad del

agua Guıa para el muestreo en rutina y pretratamiento de

diatomeas bentonicas de rıos. AENOR, Madrid

AENOR (2005) Norma espanola UNE-EN 14407 Calidad del agua.

Guıa para la identificacion recuento e interpretacion de muestras

de diatomeas bentonicas de rıos. AENOR, Madrid

Almeida SFP (2001) Use of diatoms for freshwater quality evaluation

in Portugal. Limnetica 20:205–213

Bahls LL (2006) Northwest diatoms: a photographic catalogue of

species in the Montana Diatom Collection, with ecological

optima, associates, and distribution records for the nine North-

western United States. Helena

Bahls LL, Weber EE, Jarvie JO (1984) Ecology and distribution of

major diatom ecotypes in the southern Fort Union Coal Region

of Montana. US Geol Surv Prof Pap 1289:1–151

Bellinger BJ, Cocquyt C, O’Reilly CM (2006) Benthic diatoms as

indicators of eutrophication in tropical streams. Hydrobiologia

573:75–87

Belton TJ, Ponader KC, Charles DF (2005) Trophic diatom indices

(TDI) and the development of site-specific nutrient criteria.

TMDL 2005 Specialty conference. Water Environment Feder-

ation, Alexandria

Bennion H (1993) A diatom-phosphorus transfer function for

eutrophic ponds in southeast England. PhD, University College

London, London

Bennion H (1995) Quantitative reconstructions of the nutrient

histories of three Anglesey lakes. CCW Contract Science Report

No. 87. Environmental Change Research Centre

Bennion H, Juggins S, Anderson NJ (1996) Predicting epilimnetic

phosphorus concentrations using an improved diatom-based

transfer function and its application to lake eutrophication

management. Environ Sci Technol 30:2004–2007

Birks HJB, Line JM, Juggins S, Stevenson AC, ter Braak CJF (1990)

Diatoms and pH reconstruction Phil Trans Roy Soc London B

327:263–278

Blanco S, Ector L, Becares E (2004) Epiphytic diatoms as water

quality indicators in Spanish shallow lakes. Vie Milieu 54:71–79

Blanco S, Becares E, Cauchie HM, Hoffmann L, Ector L (2007)

Comparison of biotic indices for water quality diagnosis in the

Duero Basin. Arch Hydrobiol Suppl Large Rivers 17:267–286

Blanco S, Ector L, Huck V, Monnier O, Cauchie HM, Hoffmann L,

Becares E (2008) Diatom assemblages and water quality

assessment in the Duero Basin (NW Spain). Belg J Bot

141:39–50

Bland JM, Kerry SM (1998) Weighted comparison of means. Br Med

J 316:129

Catalan J, Ballesteros E, Garcıa E, Palau A, Camarero L (1993)

Chemical composition of disturbed and undisturbed high-moun-

tain lakes in the Pyrenees: a reference for acidified sites. Water

Res 27:133–141

CEMAGREF (1982) Etude des methodes biologiques d’appreciation

quantitative de la qualite des eaux Rapport Q E. Lyon-A.

F. Bassin Rhone-Mediteranee-Corse, Lyon

Charles DF, Acker FW, Hart DD, Reimer CW, Cotter PB (2006)

Large-scale regional variation in diatom–water chemistry

Fig. 4 Studied diatom taxa.

a–f Achnanthidium pyrenaicum;

g–l Eolimna minima,

m Navicula tripunctata;

a, g scanning electron

microscopy, scale bar 1 lm.

b–f, h–m Light microscopy,

scale bar 10 lm

166 Limnology (2011) 12:157–168

123

relationships: rivers of the eastern United States. Hydrobiologia

561:27–57

Chen G, Dalton C, Leira M, Taylor D (2007) Diatom-based total

phosphorus (TP) and pH transfer functions for the Irish

Ecoregion. J Paleolimnol 40:143–163

de la Rey PA, Taylor JC, Laas A, van Rensburg L, Vosloo A (2004)

Determining the possible application value of diatoms as

indicators of general water quality: a comparison with SASS 5.

Water SA 30:325–332

Dela-Cruz J, Pritchard T, Gordon G, Ajani P (2006) The use of

periphytic diatoms as a means of assessing impacts of point

source inorganic nutrient pollution in south-eastern Australia.

Freshw Biol 51:951–972

Dell’Uomo A (2004) L’Indice Diatomico de Eutrofizzacione/

Polluzione (EPI-D) nel monitoraggio delle acque correnti Linee

guida. APAT, Roma

Denys L (2004) Relation of abundance-weighted averages of diatom

indicator values to measured environmental conditions in

standing freshwater. Ecol Indic 4:255–275

Eloranta P, Soininen J (2002) Ecological status of some Finnish rivers

evaluated using benthic diatom communities. J Appl Phycol

14:1–7

Garcıa D, Gonzalez M (1986) Metodos biologicos para el estudio de

la calidad de las aguas aplicacion a la Cuenca del Duero.

Ministerio de agricultura pesca y alimentacion. ICONA, Madrid

Gasse F (1986) East African diatoms, taxonomy, ecological distribu-

tion. Biblioth Diatomol 11:1–202

Gasse F, Fontes JC, Plaziat JC, Carbonel P, Kaczmarska I, De Deckker

P, Soulie-Marsche I, Callot Y, Dupeuple PA (1987) Biological

remains, geochemistry and stable isotopes for the reconstruction

of environmental and hydrological changes in the Holocene lakes

from North Sahara. Palaeo Palaeo Palaeo 60:1–46

Goma J, Ortız R, Cambra J, Ector L (2004) Water quality evaluation

in Catalonian Mediterranean rivers using epilithic diatoms as

bioindicators. Vie Milieu 54:81–90

Gomez N, Licursi M (2001) The Pampean Diatom Index (IDP) for

assessment of rivers and streams in Argentina. Aquat Ecol

35:173–181

Hofmann G (1993) Aufwuchs-Diatomeen in Seen und ihre Eignung

als Indikatoren der Trophie. Biblioth Diatomol 30:1–241

Kelly MG, Whitton BA (1995) The Trophic Diatom Index: a new

index for monitoring eutrophication in rivers. J Appl Phycol

7:433–444

Korsman T, Birks HJB (1996) Diatom-based reconstruction from

northern Sweden: a comparison of reconstruction techniques.

J Paleolimnol 15:65–77

Kovacs C, Kahlert M, Padisak J (2006) Benthic diatom communities

along pH and TP gradients in Hungarian and Swedish streams.

J Appl Phycol 18:105–117

Kovas CS, Buczko K, Hajnal E, Padisak J (2007) Epiphytic, littoral

diatoms as bioindicators of shallow lake trophic status: trophic

diatom index for lakes (TDIL) developed in Hungary. Hydro-

biologia 589:141–154

Lange-Bertalot H (2001) Navicula sensu stricto, 10 genera separated

from Navicula sensu lato, Frustulia. Diatoms Eur 2:1–526

Lenoir A, Coste M (1996) Development of a practical diatom index of

overall water quality applicable to the French national water

board network. In: Whitton BA, Rott E (eds) Use of algae for

monitoring rivers II. Institut fur Botanik, Universitat Innsbruck,

Austria, pp 29–43

Levkov Z, Blanco S, Krstic S, Nakov T, Ector L (2007) Ecology of

benthic diatoms from Lake Macro Prespa (Macedonia). Arch

Hydrobiol Suppl Algol Stud 124:71–83

Lobo EA, Callegaro VL, Oliveira MA, Salomoni SE, Schuler S, Asai

K (1996) Pollution tolerant diatoms from lotic systems in the

Jacuı Basin, Rıo Grande do Sul, Brazil. Iherin Ser Bot 47:45–72

Lotter AF, Birks HJB, Hofmann W, Marchetto A (1998) Modern

diatom, cladocera, chironomid, and chrysophyte cyst assem-

blages as quantitative indicators for the reconstruction of past

environmental conditions in the Alps, II, nutrients. J Paleolimno-

limnol 19:443–463

Lowe RL (1974) Environmental requirements and pollution tolerance

of freshwater diatoms. US Environmental Protection Agency,

Cincinnati

More JJ (1977) The Levenberg–Marquardt Algorithm: implementa-

tion and theory. In: Watson GA (ed) Lecture notes in mathe-

matics 630. Springer, Berlin, pp 105–116

Nygaard G (1996) Temporal and spatial development of individual

species of plankton algae from European lakes. Hydrobiologia

332:71–91

Pan Y, Stevenson RJ, Hill BH, Herlihy AT, Collins GB (1996) Using

diatoms as indicators of ecological conditions in lotic systems:

a regional assessment. J N Am Benthol Soc 15:481–495

Pipp E (2002) A regional diatom-based trophic state indication

system for running water sites in Upper Austria an its over

regional applicability. Verh Internat Verein Limnol 27:3376–

3380

Ponader KC, Charles DF, Belton TJ (2007) Diatom-based TP and TN

inference models and indices for monitoring nutrient enrichment

of New Jersey streams. Ecol Indic 7:79–93

Potapova M, Charles DF (2007) Diatom metric for monitoring

eutrophication in rivers of the United States. Ecol Indic 7:48–70

Potapova M, Charles DF, Ponader KC, Winter DM (2004) Quanti-

fying species indicator values for trophic diatom indices:

comparison of approaches. Hydrobiologia 517:21–41

Resende P, Azeiteiro U, Pereira MJ (2005) Diatom ecological

preferences in a shallow temperate estuary (Rıa de Aveiro,

Western Portugal). Hydrobiologia 544:77–88

Rimet F, Ector L, Cauchie HM, Hoffmann L (2004) Regional

distribution of diatom assemblages in the headwater streams of

Luxembourg. Hydrobiologia 520:105–117

Rimet F, Cauchie HM, Hoffmann L, Ector L (2005) Response of

diatom indices to simulated water quality improvements in a

river. J Appl Phycol 17:119–128

Rioual P (2000) Diatom assemblages and water chemistry of lakes in

the French Massif Central: a methodology for reconstruction of

past limnological and climate fluctuations during the Eemian

period. Thesis, University College, London

Rott E, Hofmann G, Pall K, Pfister P, Pipp E (1997) Indikationslisten

fur Aufwuchsalgen in osterreichischen Fliebgewassern. Teil 1:

Saprobielle Indikation. Wasserwirtschaftskataster, Bundesminis-

terium f. Land-u. Forstwirtschaft, Wien

Solovieva N (2000) A palaeoecological study of Holocene environ-

mental change in a small upland lake from the Kola peninsula,

Russia. PhD, University of London, London

StatSoft Inc (2004) STATISTICA (data analysis software system),

version 7

Stevenson AC, Juggins S, Birks HJB, Anderson DS, Anderson NJ,

Battarbee RW, Berge F, Davis RB, Flower RJ, Haworth EY,

Jones VJ, Kingston JC, Kreiser AM, Line JM, Munro M,

Renberg I (1991) The surface waters acidification project

palaeolimnology programme: modern diatom/lake-water chem-

istry data-set. ENSIS Ltd., London

Taylor JC, Harding WR, Archibald GM (2007) An illustrated guide to

some common diatom species from South Africa. WRC Report

TT 282/07, Pretoria

Van Dam H, Mertens A, Sinkeldam J (1994) A coded checklist and

ecological indicator values of freshwater diatoms from the

Netherlands. Neth J Aquat Ecol 28:117–133

Verb RG, Vis ML (2005) Periphyton assemblages as bioindicators of

mine-drainage in Unglaciated Western Allegheny Plateau lotic

system. Wat Air Soil Pollut 161:227–262

Limnology (2011) 12:157–168 167

123

Weckstrom J, Korhola A, Blom T (1997) Diatoms as quantitative

indicators of pH and water temperature in subarctic Fennoscan-

dian lakes. Hydrobiologia 347:171–184

Winter JG, Duthie HC (2000) Epilithic diatoms as indicators of

stream total N and total P concentration. J N Am Benthol Soc

19:32–49

Wunsam S, Schmidt R (1995) A diatom-phosphorus transfer

function for Alpine and pre-alpine lakes. Mem Ist Ital Idrobiol

53:85–99

168 Limnology (2011) 12:157–168

123