Proposal of a typology of Spanish mountain lakes and ponds ... · Tipos de impactos que afectan habitualmente a los ecosistemas lacustres en el área de estudio y característicasasociadasa

Limnetica, 29 (2): x-xx (2011)Limnetica, 34 (2): 507-526 (2015)c© Asociación Ibérica de Limnología, Madrid. Spain. ISSN: 0213-8409

Proposal of a typology of Spanish mountain lakes and ponds usingthe composition of functional groups of macrophytes

Gemma Núñez1, Camino Fernández-Aláez1,∗, Margarita Fernández-Aláez1 andCristina Trigal2

1 Department of Biodiversity and Environmental Management. University of León, Campus de Vegazana 24071León, Spain.2 Swedish Species Information Centre. Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden.

∗ Corresponding author: [email protected]

Received: 30/10/14 Accepted: 01/03/15

ABSTRACT

Proposal of a typology of Spanish mountain lakes and ponds using the composition of functional groups of macrophytes

Before establishing the ecological status of lakes, the Water Framework Directive requires their classification in types.Typically, the development of a typology has been based on abiotic variables. However, for the typology to have validity,the classification of lakes should be corroborated with the biological communities in the bodies of water. In this study, todevelop a biologically relevant typology, the natural variability of the macrophyte communities in mountain lakes and pondswas evaluated. The use of functional groups of macrophytes as an alternative to the taxonomic approach was also evaluated.Thirty-one reference mountain lakes and ponds, located in the northwest quadrant of the Iberian Peninsula, were includedin the study. The functional groups of macrophytes were based on the inorganic source of carbon used in photosynthesis.The typology developed from the functional groups was more conclusive than the classification derived from the taxonomicdata. The primary determinants of the variability in the composition of the functional groups of macrophytes among thedifferent types of lakes were the changes in the pH and in the orthophosphate concentration related to the decomposition ofmacrophytes. The submerged macrophytes dominated in the lakes with low concentrations of orthophosphate and the highestlevels of alkalinity. In the lakes with lower pH values, the floating-leaved macrophytes were the dominant plants when thephosphorus concentration was higher, whereas at intermediate concentrations of phosphorus, the bryophytes and isoetids weremore abundant; these two lake types were differentiated because of the dominance of the bryophytes in those lakes with higheracidity.

Key words: Typology, mountain lakes, ponds, macrophyte, functional group.

RESUMEN

Propuesta de una tipología de lagos y lagunas españoles de montaña utilizando la composición de grupos funcionales demacrófitos

Previamente al establecimiento del estado ecológico de los lagos, la DMA requiere su clasificación en tipos. Habitualmente,el desarrollo de una tipología se ha basado en variables abióticas. Sin embargo, su validez debería venir contrastada conlas comunidades presentes en las masas de agua. En este estudio se evalúa la variabilidad natural de las comunidades demacrófitos en lagos y lagunas de montaña, con el fin de desarrollar una tipología que sea biológicamente relevante. Seevalúa además la validez del uso de grupos funcionales como una alternativa a la aproximación taxonómica. En el estudio seincluyeron treinta y un lagos y lagunas de montaña de referencia, localizados en el cuadrante noroccidental de la PenínsulaIbérica. Los grupos funcionales de macrófitos se establecieron en base a la fuente de carbono inorgánica utilizada en lafotosíntesis. La tipología desarrollada a partir de grupos funcionales fue más concluyente que la derivada de los datostaxonómicos. La variabilidad en la composición de grupos funcionales entre los distintos tipos de lagos estuvo determinadafundamentalmente por los cambios de pH y de ortofosfato. Este último, relacionado con el proceso de descomposición dela biomasa macrofítica. En los lagos con bajas concentraciones de ortofosfato y los niveles más elevados de alcalinidad losmacrófitos sumergidos fueron dominantes. Los macrófitos de hojas flotantes dominaron en los lagos con el pH más bajo y conlas concentraciones de ortofosfato más elevadas, mientras que para valores intermedios de este nutriente, briófitos e isoétidos

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508 Núñez et al.

fueron más abundantes. La diferencia entre los lagos definidos por estos dos grupos funcionales se debió a la mayor acidezde aquellos en los que dominaron los briófitos.

Palabras clave: Tipología, lagos de montaña, lagunas, macrófito, grupo funcional.

INTRODUCTION

The Water Framework Directive (WFD; Euro-pean Union, 2000) proposed an innovative modelof water management by changing the conceptof water quality to include a measure of the eco-logical status of the water body. The ecologicalstatus should be determined through the evalua-tion of a number of quality indicator elements,including the composition and the abundance ofmacrophyte communities. To assess the ecolog-ical status of a water body, reference conditionsmust first be established for the different typesof aquatic systems, which have different floraand fauna in the natural state (Free et al., 2006).Therefore, to establish the ecological status, theWFD requires a classification of the aquatic habi-tats into types or ecotypes. A type or ecotypeis a group of aquatic habitats that, in referenceconditions, has a specific composition or abun-dance of flora and fauna that is related to a par-ticular combination of environmental factors forthat group (van de Bund & Solimini, 2006). Thepurpose of the typology is to more easily detectthe ecological changes caused by anthropogenicpressures, and therefore, a typology should en-sure that the natural differences among aquaticecosystems are clearly distinguished from thosecaused by human activity (CIS-WFD, 2003). TheWFD allows member states to define the lake ty-pology using either System A or B (EuropeanUnion, 2000). Most states have opted to use theSystem B, which, in addition to several obliga-tory factors, allows more choice in the variablesused and in the location of boundaries. In Spain,the water planning instruction classified the su-perficial water bodies into four categories (rivers,lakes, transitional waters and coastal waters), andtypes were assigned to each of the categories.For lakes, thirty types were established accord-

ing to the variables of humidity index, altitude,lake origin, input regime, hydroperiod, and lakearea, depth, conductivity and alkalinity (ORDENARM/2656/2008).The assessment of the ecological status of

lakes using macrophytes has gained importancebecause aquatic plants were recognized as one ofthe biological indicators for use in the biomoni-toring programmes listed in theWFD (Free et al.,2006; Nõges et al., 2009). Therefore, the es-tablishment of a typology based on the naturalvariability of macrophytes in aquatic ecosystemsis required (Free et al., 2006). Together with thebiological elements, the value of supporting en-vironmental variables (hydro-morphological andphysico-chemical parameters) must be includedwhen assessing the ecological status of a body ofwater. Thus, the typology should identify envi-ronmentally distinct types of water bodies withtheir biological communities in almost pristinereference conditions (Lyche Solheim, 2005).With this approach, the results derived fromindividual indicative parameters can be used toestimate the biological assemblage related toa particular type of water body (Anonymous,2004). Different methods have been used todescribe and to quantify the relationships amongthe environmental variables and the biologicalindicators, such as univariate, multivariate orprobabilistic statistics (Moe & Ptacnik, 2007).For example, linear methods were used exten-sively to analyse the relationships between totalphosphorus or total nitrogen and chlorophyll aas an ecological response and indicator of phyto-plankton biomass (Vollenweider, 1976). Amongthe most adopted methods worldwide, the use ofmultivariate options clusters the groups based onthe biological data and then group membershipis predicted through environmental variables. Ofthe various applications of multivariate analyses,


Typology of mountain lakes and ponds using macrophytes 509

famous examples exist, including RIVPACS(Wright et al., 1997) and the BEAST (Reynold-son et al., 1995) methodologies, which both usebenthic macroinvertebrate communities in ref-erence rivers and lakes to define the referencecommunity groups, respectively. Finally, proba-bilistic methods, such as Bayesian models, areincreasingly used, and these models are basedon and predict probability distributions, whichincorporate uncertainties in a more explicit waythan the other methods (Moe & Ptacnik, 2007).A classification of aquatic systems based on

the macrophyte community can be developedwith two different approaches, i.e., taxonomicidentifications or functional groups. Several fac-tors affect the species of macrophyte in naturalconditions that can be used to define the typesof lake, and the examples include chemical vari-ables such as alkalinity, pH or conductivity (Artset al., 1990; Toivonen & Huttunen, 1995; Ves-tergaard & Sand-Jensen, 2000; Alahuhta et al.,2013). The physical properties, such as the lit-toral slope or the transparency of the water (Duar-te & Kalff, 1986; Scheffer, 1998; Alahuhta et al.,2013), and the interaction of macrophytes withthe other biotic elements of lakes such as fish,zooplankton, macroinvertebrates, phytoplanktonand periphyton are also important (Sand-Jensen& Borum, 1991; Scheffer, 1998; Mulderij etal., 2005; Gross et al., 2007; Mulderij et al.,2007). The use of macrophyte functional groupshas emerged as an alternative to the traditionaltaxonomic approach, and a classification based

on this criterion assumes that the properties of acommunity are better understood and managedwhen the species are grouped into classes withsimilar characteristics or similar behaviours (Sol-brig, 1993). Therefore, researchers focus on asmall set of functional traits that are commonlyshared by many plant species instead of a detailedstudy of each species in the community (Liao& Wang, 2010). Additionally, the functionallydefined groups of plants tend to occupy discretesections of environmental gradients. Thus, withthe identification of the members of the group,we can predict the existence of predefined rangesin such gradients. Despite the advantages of thefunctional group approach, the biocoenotic ty-pologies of lakes based on macrophytes have notused functional groups (Schaumburg et al., 2004;Kolada, 2009). The criteria selected to establishmacrophyte functional groups are multiple, andinclude the morphological features of plantssuch as submerged leaf biomass or total lengthof roots (Ali, 2003), the growth form (McLaren,2006) and the response of the seed bank (Araki& Washitani, 2000). However, the importanceof the source of the inorganic carbon used inphotosynthesis to establish functional groupshas been used less frequently (Margalef, 1983).The primary objective of this study was to de-

velop a classification system of mountain lakesand ponds that was ecologically relevant, withthe ability to explain the variation in macrophytecommunities, as a previous step in the determina-tion of the ecological status of this type of lakes.

Table 1. Types of human impact that typically affect mountain lacustrine systems in the study area, and the characteristics relatedto the two levels of impact: severe and low intensity. Tipos de impactos que afectan habitualmente a los ecosistemas lacustres en elárea de estudio y características asociadas a los dos niveles de impacto: severa y baja intensidad.

Type of impact Intensity Characteristics

Livestock pressureLow No evidence (tracks, excrements) or very few around the pond or lake

Severe Abundant evidences (tracks, excrements) around the pond or lake

TourismLow No significant erosion in the littoral area nor presence of solid waste

Severe Erosion of the littoral area or presence of solid waste

Water regulationLow No alterations or without severe alterations of hydrological regime of pond/lake

Severe Pond/lake with severe alterations of their hydrological regime

Fish introductionsLow Small fish introductionsSevere Massive introductions of fishes with macrophyte bed alteration


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We also assessed whether the existing Spanish ty-pology is appropriate to stratify the variation inmacrophyte assemblages in mountain lakes andponds. Moreover, the use of functional groups asa valid alternative to the taxonomic approach indefining macrophyte communities was evaluated.

MATERIALS ANDMETHODS

Criteria for selecting reference pondsand lakes

The Water Framework Directive includes severalpossibilities for determining the reference condi-tions, and of these possibilities, a spatial networkof reference sites was chosen. The most effectiveway to select such sites is to use ecologicalor environmental pressure criteria (CIS-WFD,2003). Because understanding of the ecologicalfunctions of the studied mountain lakes was in-sufficient, we chose the environmental pressurecriteria to select the sites. The WFD recognizesa reference locality as one that is minimallyaffected by human activity, and sites with lowintensity pressures may be accepted as referencesites. Therefore, according to the information ob-

tained from the “Catálogo de Zonas Húmedas deCastilla y León” (Decreto 194/1994; Decreto125/2001) and our observations in the field, a listof potential impacts on the ponds and lakes wasdeveloped. The potentially four most influentialeffects of human activity, direct or indirect, onthe macrophyte community were as follow:livestock pressure, tourism, water regulation andfish introductions. Because of the difficulty inestablishing quantitative levels of the effects ofhuman activities, we chose to identify the effectsqualitatively. We established only two levels ofeffect (severe and low intensity; Table 1) becausewith a qualitative assessment, the probabilityof errors would most likely increase with morelevels of the effects of human activity. Thus,all the lakes that were accepted as referencelocalities were those that did not experience anysevere impact or did not accumulate more thantwo low intensity impacts from human activity.

Study area

In this study, we selected 31 mountain lakes andponds of quaternary glacial origin that were lo-cated in the northwest quadrant of the IberianPeninsula (Fig. 1). Twenty-nine of the lakes and

Figure 1. Locations of the 31 study lakes and ponds in northwest Spain. Localización en el noroeste de España de los 31 lagos ylagunas estudiados.



ponds are located on the Castilla and León re-gion, which is a large area (94 223 km2) that con-sists of a wide central plain from 600 to 800 mthat is surrounded by mountains with elevationsup to 2600 m.a.s.l. The other two lakes (AS1and AS2) are located in the Cantabrian Moun-tains in the Asturias region. All these ponds andlakes are in protected areas and are reference sitesor are minimally affected by human activity. Ofthese bodies of water, 26 are permanent systemsand 5 are temporary systems at elevations thatranged from 1070 to 2140 m.a.s.l., with maxi-mum depths between 0.3 and 25 m and lake areasbetween 0.15 and 12 ha. Tables S1 and S2 containthe morphometric and chemical characteristicsand the geographic variables of the lakes, respec-tively (available at www.limnetica.net/internet).

Sampling of vegetation

The macrophyte vegetation was sampled in Juneand July in 2007 and 2008. In the ponds, themacrophyte vegetation was studied along pro-files, which are defined as a line from one shore tothe opposite shore at a right angle to the longestlength. When the lake could not be crossed be-cause of the depth, transects were used. The num-ber of profiles varied according to the area of thelake and the development of the shore (Jensén,1977); however, in situ corrections accounted forthe heterogeneity of the macrophyte communi-ties and the accessibility to the lake. Square sam-pling units were placed along the profiles at vary-ing intervals of 0 to 5 m, depending on the ho-

mogeneity of the vegetation (the number of unitsvaried according to the width of the lake), and thepercentage cover of each species was quantifiedfor each unit.In the deep lakes, when the direct observation

of macrophytes was not possible, the quantifi-cation of submerged vegetation was performedwith a hook that was thrown from the boat.The sampling points were randomly located inzones of different depth, and four samples werecollected in each of the zones. The number ofsample points depended on the area of the lake(lakes< 1 ha: 5 points; lakes 1-5 ha: 10 points;lakes 5-10 ha: 15 points; and lakes> 10 ha: 20points). The coverage values assigned to the speciesin the deep zones were 25%, 50%, 75% and100%, depending on whether the species was col-lected in 1, 2, 3 or 4 of the samples, respectively.The mean cover for each species was calcu-

lated as the sum of the coverage for that speciesfrom the different sample units divided by thetotal number of the sample units used for thatlake. The sampling of the macrophytes was com-pleted with a walk around each pond to registerthe species that were absent in the profiles. Thenomenclature followed the Flora Ibérica (Cas-troviejo et al., 1986-2010), the Flora Europaea(Tutin et al., 1980) and Cirujano et al. (2008).

Functional types of macrophytes

In addition to the taxonomic approach, the com-position of the functional groups of macrophyteswas also determined. Because of the importan-

Table 2. Environmental variables included in the study, grouped into four categories.Variables ambientales incluidas en el estudio,agrupadas en cuatro categorías.

Local variables:Water chemistry variables

Local variables:Physical variables

Catchmentvariables

Geographicallocation variables

pHConductivity

Alkalinity

NitrateTotal Nitrogen

OrthophosphateTotal Phosphorus

Chlorophyll aN:P

Lake Surface AreaMaximum DepthLittoral Slope

Persistence% Silt% Sand% PebbelsSecchi Depth

Catchment AreaCatchment to Lake Area ratio% Bare rock% Shrubland% Forest% Grassland

ElevationLatitudeLongitude


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ce of the inorganic carbon source used in photo-synthesis (den Hartog & Van der Velde, 1988),we established the functional groups accordingto this criterion. The resulting groups were asfollow: the helophytes, that use the atmosphe-ric CO2 as the inorganic carbon source; thefloating-leaved hydrophytes, that use both the at-mospheric CO2 and the bicarbonate of the water;the submerged hydrophytes, which included thecharophytes and the angiosperms, for which thebicarbonate of the water is the inorganic carbonsource; the bryophytes, that assimilate the CO2from the water; and the isoetids, that primarilyuse the sediment CO2 and to a lesser extent theCO2 from the water.

Environmental variables

To determine the effects on the composition ofthe macrophyte, a total of 26 environmental vari-ables were measured (Table 2).The physicochemical variables were collected

simultaneously with the macrophyte sampling.The conductivity, pH, temperature, oxygenconcentration and percentage oxygen saturationwere determined by direct measurement in the

water of the pond or the lake with a multipa-rameter meter. The Secchi disk depth was alsomeasured in the field. In each aquatic system, weestablished transects from the shore to the centre,and the water samples were collected randomlyin areas without vegetation with a core that was6 cm in diameter and one metre in length. Thesesamples were integrated into a final sample ofwater for later laboratory determinations of thealkalinity, total nitrogen (TN), total phosphorus(TP), nitrate, orthophosphate and chlorophyll a.The samples that were used for the determinationof total nutrients were fixed in the field withmercury, whereas those that were used for theanalyses of the dissolved nutrients were filteredthrough a Whatman glass fibre filter (GF/C) andthen were fixed with mercuric chloride in thelaboratory. All samples were refrigerated at 4 ◦Cuntil analysis. All analyses were conducted ac-cording to the standard methods (APHA, 1989).The maximum depth was determined with

several measurements along a series of transects.An approximate estimation of the littoral slopewas performed using a scale of 1 to 4 (1 = veryslight; 2 = slight; 3 = moderate; and 4 = steep).Additionally, the granulometric composition of

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Figure 2. Cluster analysis (a) and NMDS ordination (b) of the 31 study lakes and ponds using the data of the five functionalgroups (isoetids, bryophytes, emergent, submerged and floating-leaved macrophytes). Type 1 = submerged hydrophytes; Type 2 =bryophytes; Type 3 = isoetids; Type 4 = floating-leaved hydrophytes. Resultados de los análisis de agrupación (a) y de ordenaciónNMDS (b) basados en la cobertura de los cinco grupos funcionales (isoétidos, briófitos, helófitos, macrófitos sumergidos y de hojasflotantes) registrados en los 31 lagos y lagunas incluidos en el estudio. Tipo 1 = hidrófitos sumergidos; Tipo 2 = briófitos; Tipo 3 =isoétidos; Tipo 4 = hidrófitos de hojas flotantes.



the substrate for the percentages of silt, sand andpebbles was estimated in the field. Using theapplication SIGPAC (www.sigpac.jcyl.es/visor/),we measured the area of the lake and the basinand estimated the land use in the basin (percent-ages of rocky land, shrubland, forest and grass-land), and the geographical coordinates of eachlake (latitude and longitude) were determined.The persistence, temporary or permanent, was

also used to separate the ponds and lakes, de-pending on whether the body of water dried upcompletely during the summer.

Data analyses

For the statistical analyses, the percentage of cov-erage of each taxon and of the different functionalgroups was transformed to a scale of 1 to 5 (1 ≤1 %; 2 = 1-2 %; 3 = 2-5 %; 4 = 5-30 %; and 5 ≥30 %).The following steps were used to develop the

typology:

• To determine if there were distinct groupsof lakes using the macrophyte community inthe reference lakes.

• To determine whether such biological grou-pings were significantly distinct for the ma-crophytes and the environmental variables.

• To attempt to assign environmental bound-aries that were useful in the definitions of thedistinct biological types.

To develop the typology, cluster analyses withthe abundance data of the different functionalgroups or species in each reference lake or pondwere performed. To assess the significance of thedifferent types suggested by the dendrogram di-visions, the differences in macrophyte compo-sition among these types were evaluated usingthe ANalysis Of SIMilarities (ANOSIM). In thisanalysis, the statistic R is an absolute measureof the distance among the groups. The highestR-value within a given similarity threshold de-termined the types of reference lakes and ponds.To corroborate the groupings suggested by theseanalyses, we conducted a Non-Metric Multidi-

mensional Scaling (NMDS) ordination. The Bray-Curtis index was the similarity measure used inall the analyses.The second step was to determine whether the

types of ponds and lakes previously suggestedwere different for the macrophyte communityand the environmental variables. For this pur-pose, we conducted a SIMilarity of PERcentages(SIMPER) analysis with a cut-off level of 90 %to detect the species or functional groups thatcontributed the most to the differentiation of thetypes. Moreover, a one-way ANOVA was perfor-med to determine whether significant differenceswere found for the environmental variablesamong the types. The homogeneity of the vari-ance and the normal distribution were previouslytested using the Levene’s test and the Kol-mogorov-Smirnov test, respectively. Any vari-ables that did not have homogeneity of thevariance and a normal distribution were trans-formed, and we used the arcsine (x/100)−0.5

transformation for the variables expressed inpercentages and the log (x) or log (x + 0.01)transformation for the rest of the data.To visualize the differences among the types

of water bodies, box-plot graphics of thoseenvironmental variables for which significantdifferences were detected in the ANOVA wereconstructed. We used the Scheffé test to identifythe pairs of groups of samples among which sig-nificant differences (p < 0.05) existed. Becauseenvironmental factors may have complementaryeffects with one another, we evaluated the typesfor combinations of variables with a multiplediscriminant analysis (CVA: Canonical VariateAnalysis) (Ter Braak & Šmilauer, 2002). Thosevariables for which the types presented signif-icant differences were sequentially introduced(forward selection) into the CVA. Before thisanalysis and to remove possible redundancies,we conducted a correlation analysis and elimi-nated the variables with a correlation value grea-ter than 0.5.The statistical packages used for these anal-

yses were PAST v.2.14 for the clustering analy-ses and ANOSIM; PRIMER v.5 for the SIMPERand NMDS ordinations; STATISTICA v.8 for theANOVAs, box-plot graphs, correlation analyses


514 Núñez et al.

and the verification of normality and homogene-ity of variances of the variables; and Canoco forWindows 4.5 for the CVA.

RESULTS

A total of 41 macrophyte taxa were identified,with 23 emergent macrophytes or helophytes,6 floating-leaved hydrophytes, 5 submergedhydrophytes, 5 bryophytes and 2 isoetids (TableS3, available at www.limnetica.net/internet).The helophytes, bryophytes and floating-

leaved hydrophytes were the most frequent func-tional groups and were present in 97 %, 87 %and 77 % of the ponds and lakes, respectively.The isoetids and the submerged hydrophyteswere present in 29 % and 26 % of them, respec-tively. Within the helophytes, the most frequentspecies was Juncus squarrosus L., which waspresent in 65 % of the aquatic systems. Othercommon helophytes were Ranunculus flammulaL. and Glyceria fluitans (L.) R. Br., which wererecorded in 48 % and 45 %, respectively, of theponds and lakes, and Carex rostrata Stokes andViola palustris L., which were found in the 32 %

of them. The Sphagnum sp., Warnstorfia exan-nulata (Schimp.) Loeske and Fontinalis antypi-reticaHedw. were the most common bryophytes,which were present in 74 %, 55 % and 32 %of the ponds and lakes, respectively. For thefloating-leaved hydrophytes, Ranunculus pelta-tus Schrank, Callitriche brutia Petagna and Pota-mogeton natans L. were recorded in 55 %, 42 %and 23 % of the ponds and lakes, respectively.The most common isoetid was Isoetes velatumA. Braum in Bory & Durieu subsp. asturicense(Lainz), which was in 22 % of the aquatic sys-tems, whereas among the submerged hydro-phytes, the charophyte Nitella flexilis (L.) C.Agardh was the most common and was recordedin 13 % of the reference sites.The dendrogram obtained from the taxonomic

composition showed multiple groups that werepoorly differentiated and were formed by a smallnumber of lakes without a defined meaning.By contrast, the dendrogram obtained from thefunctional groups indicated better-defined groupsof ponds and lakes than those obtained fromthe taxonomic composition (Fig. 2a). Thus, thefunctional group data were selected to elaboratethe typology. The similarity analysis (R = 0.871;

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Figure 3. Cluster analysis (a) and NMDS ordination (b) of the 26 study lakes and ponds selected for the typology. The datafor the four functional groups (isoetids, bryophytes, submerged and floating-leaved macrophytes) were used. Type 1 = submergedhydrophytes; Type 2 = bryophytes; Type 3 = isoetids; Type 4 = floating-leaved hydrophytes.Resultados de los análisis de agrupación(a) y de ordenación NMDS (b) basados en la cobertura de cuatro grupos funcionales de macrófitos (isoétidos, briófitos, macrófitossumergidos y de hojas flotantes) registrados en los 26 lagos y lagunas seleccionados para llevar a cabo la tipología. Tipo 1 = hi-drófitos sumergidos; Tipo 2 = briófitos; Tipo 3 = isoétidos; Tipo 4 = hidrófitos de hojas flotantes.



p < 0.001) identified four types of ponds andlakes, which were corroborated with the NMDSordination (Fig. 2b) (Stress= 0.13). The SIM-PER results showed the limited contribution ofthe helophytes in establishing the types of pondsand lakes because they were found in all thebodies of water. Therefore, the helophytes wereomitted in the development of the typology.

In the dendrogram that used only the 4 func-tional groups (floating-leaved hydrophytes, sub-merged hydrophytes, bryophytes and isoetids),we selected the groups with the highest values ofR (R = 0.939) that were statistically significant(p < 0.001) as the final types. The final numberof ponds and lakes selected to establish the ty-pology was 26, which were divided into the types

Table 3. The results of the SIMPER analysis showing the contribution of the functional groups to the dissimilarity among the typesof lakes and ponds. Se indica la contribución de los grupos funcionales a la disimilitud entre tipos de lagos y lagunas.

Functional group TYPE 1 TYPE 2 Mean dissimilarity: 96.89 %

Mean abundance Contribution %

Submerged hydrophytes 4.67 0 45.37

Bryophytes 0 4.29 41.66

Floating-leaved hydrophytes 1.67 0.29 12.96

TYPE 1 TYPE 3 Mean dissimilarity: 83.23 %


Submerged hydrophytes 4.67 0.14 32.78

Isoetids 0 3.71 27.09










Isoetids 0 3.71 44.33


Bryophytes 4.29 3.29 18.13




Bryophytes 4.29 3.44 21.75

Submerged hydrophytes 0 0.78 12.50



Isoetids 3.71 0 54.75

Bryophytes 3.29 3.44 18.31




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Figure 4. Mean relative abundance of the functional groupsin the different types of lakes and ponds. Valores medios de laabundancia relativa de los grupos funcionales en los tipos delagos y lagunas.

(Fig. 3a); the NMDS ordination corroborated thedivision of the lakes into the 4 types (S = 0.08)(Fig. 3b). The SIMPER results identified thefunctional groups that determined the differencesamong the types of ponds and lakes. The aquaticsystems of type 1 were the most clearly differen-tiated because of the predominance of submergedhydrophytes. The differentiating characteristicof the type 3 bodies of water was the isoetids,whereas in type 2, the dominant functional groupwas the bryophytes. The bryophytes and thefloating-leaved hydrophyte functional groupscharacterized type 4 ponds and lakes (Table 3).Figure 4 shows the relative abundance of eachfunctional group in the different types of pondsand lakes, as determined by the cluster analysis.The types of ponds and lakes were significant-

ly differentiated by six environmental variables,which were conductivity (F = 21.05, p < 0.001),pH (F = 15.91, p < 0.001), alkalinity (F = 13.79,p < 0.001), orthophosphate (F = 5.12, p < 0.01),N:P ratio (F = 5.06, p < 0.01) and elevation(F = 4.28, p < 0.05). The type 1 lakes had pH,alkalinity and conductivity values that were

significantly higher than the other three typesof lakes. Moreover, in type 1 lakes, the ortho-phosphate concentration was significantly lowerthan that in the type 4 lakes in which thefloating-leaved hydrophytes were the dominantfunctional group. The box-plot graphs (Fig. 5)suggested threshold values for the pH, alkalinityand conductivity, which allowed us to establishtwo groups: high alkaline lakes (> 1 mg/l) withhigh pH (> 7.5) and relatively high conductivity(> 150 µS/cm) and low alkaline lakes (< 1 mg/l)with low pH (< 7.5) and low conductivity(< 150 µS/cm). The high alkaline group wascomposed of the lakes of type 1, whereas theother types were in the second group.The orthophosphate, N:P ratio, pH and ele-

vation were included in discriminant analysis,whereas the alkalinity and the conductivitywere excluded because of the high correlationswith the pH (r = 0.616, p < 0.001; r = 0.498,p < 0.05, respectively). The variable pH wasselected instead of conductivity or alkalinitybased on the previous results of the ANOVAsand box-plot graphs, both of which indicated thatthe pH resulted in better differentiation amongthe types of lakes than the other variables. Inthis analysis, the combination of pH and ortho-phosphate was selected as the determinant forthe ordination of the ponds and lakes (Fig. 6a).The axis 1 (eigenvalue= 0.713) summarized thedistribution of the bodies of water along a pHgradient, and the lakes characterized by sub-merged hydrophytes (type 1) were located at thebasic end of the gradient, whereas at the acidicend, the lakes were dominated by bryophytes(type 2). The ponds and lakes with isoetids(type 3) and those that were characterized byfloating-leaved hydrophytes (type 4) occupiedan intermediate position on the pH gradient(Fig. 6b). The axis 2 (eigenvalue= 0.399) rep-resented an orthophosphate gradient (Fig. 6a),which thereby marked the differentiation of thelakes with floating-leaved hydrophytes; thesehydrophytes had values of this nutrient that wereslightly higher than those in the other lakes. Bycontrast, the lakes of type 1 had orthophosphatelevels lower than the other types of bodies of wa-ter (Fig. 6b). Furthermore, an increase in the or-



1 2 3 4

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4

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9pH

1-2 = p <0.0011-3 = p <0.011-4 = p <0.0012-3 = p <0.05

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e (�

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ity (m

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tude

(m a

.s.l.

)

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Figure 5. Box-plots of environmental variables that were significantly different among the different types of lacustrine ecosystems.ANOVA results are shown. Gráficos box-plot de las variables ambientales que mostraron diferencias significativas entre los tipos delagos y lagunas. Se muestran los resultados del ANOVA.


518 Núñez et al.

thophosphate concentration resulted in an in-crease of chlorophyll a (r = 0.637, p < 0.001)and in a decrease of transparency (r = −0.714,p < 0.001).

DISCUSSION

The natural variability in the macrophyte com-munity among the studied reference ponds andlakes was better understood when the specieswere grouped into functional groups that wherebased on the inorganic carbon sources used inphotosynthesis. The study of this variability iden-tified two local variables, pH and orthophos-phate, as the optimum predictors of the differ-ences among the aquatic systems. The pH wasclearly related to the lithological characteristicsof the basin. These two variables, which were notconsidered in the official lake and pond typolo-gy (ORDENARM/2656/2008),were used to clas-sify the ponds and lakes into four types (acidicand oligotrophic; alkaline and oligotrophic; mod-erately acidic and oligotrophic; and moderatelyacidic with a greater availability of orthophos-phate), which differed in the compositions of themacrophyte community.

Functional groups of macrophytes versustaxonomy

One of the most important factors to affect thedistributions of species and functional groups ofmacrophytes in lakes is the source of inorganiccarbon used in photosynthesis (den Hartog &Van der Velde, 1988; Vestergaard& Sand-Jensen,2000). Because different species show similarbehaviours in relation to the carbon sourceused in photosynthesis, this criterion can be thebasis to establish a series of functional groupsof plants. A functional group includes speciesthat have a similar response to the environmentwith similar effects on ecosystem function (Gitay& Noble, 1997). The species composition of theplant community in individual aquatic systemsis often highly site-specific (Brock et al., 2003;Alexander et al., 2008; Barrett et al., 2010).However, the use of functional groups reduces

the noise caused by the spatial variability in thefloristic data found in the taxonomic level iden-tifications (Campbell et al., 2014). Based on ourstudy, the community characteristics were betterunderstood when the species were grouped intofunctional groups because the results were moreclear than those obtained with the taxonomicapproach, which was consistent with the conclu-sion of previous works (Kumar & Narain, 2010).Moreover, the use of functional groups of macro-phytes allowed us to focus on a smaller numberof variables (5 functional groups compared with41 macrophyte taxa) that were related to a uniquefunctional trait instead of studying each speciesin detail, an advantage that clearly facilitated thedevelopment of a typology. The classification ofspecies into functional groups enables to identifythe relationships between the macrophytes andthe water regime without the requirement for adetailed understanding of botany or a familiaritywith scientific names (Campbell et al., 2014).However, the usefulness of the functional groupof helophytes for this type of studies seemsto be limited because of the weak links withthe water conditions. Moreover, variables suchas water level fluctuations and wave exposuredetermine the distribution and composition ofhelophytes (Coops et al., 1991, 2004); however,these variables were not significant or were notincluded in this study. Thus, we did not includethe helophyte functional group in the analyses,which was consistent with other works related tothe establishment of reference conditions and tothe assessment of the ecological status of bodiesof water (Schaumburg et al., 2004; Free et al.,2006; Søndergaard et al., 2010).

The importance of pH

The clear relationship between the distributionof macrophytes and the pH was demonstrated inprevious studies (Arts et al., 1990; Vestergaard &Sand-Jensen, 2000; Chappuis et al., 2014). Themost extreme conditions of pH are a limitation tothe development of certain functional groups; insuch cases, a small number of functional groupsare dominant in those lakes. This relationshipwas demonstrated for the submerged hydrophy-



-3 5-46

Type 1Type 2 Type 3

Type 4

pH

Orthophosphate

-6 6

-34

(a)

(b)

Type 1

Type 4

Type 3

Type 2

Figure 6. Canonical variate analysis scatter-plots based on five environmental variables and four macrophyte functional groups of26 lakes and ponds. (a) Axes I and II of the CVA plot showing the centroids of the lacustrine ecosystem types. Environmental variablesare indicated by arrows. (b) Ordination of the lakes and ponds of different types on the first two discriminant axes. Resultados delAnálisis Canónico Discriminante para los 26 lagos y lagunas seleccionados, basado en cinco variables ambientales y cuatro gruposfuncionales de macrófitos. (a) Ordenación en el plano definido por los ejes I y II de los centroides correspondientes a los tipos deecosistemas lacustres. Las variables ambientales se indican mediante flechas. (b) Ordenación de los lagos y lagunas pertenecientesa los diferentes tipos en el plano definido por los dos primeros ejes discriminantes.

tes, which dominated the most mineralized of thelakes (type 1). Lacoul & Freedman (2006) notedthat the species richness of this type of plant wasgreater in alkaline waters with a pH > 7. How-ever, the ability to use and the affinity for bicar-bonate varies among species in the same growthform. For example, the charophytes in the mostmineralized aquatic systems were in the genus

Chara, whereas Nitella flexilis was in the pondsand lakes with lower pH values in which thesubmerged hydrophytes were not dominant. Thecharophytes of the genus Nitella were in moreacidic waters than those of Chara, which waspreviously noted (Hutchinson, 1975). Unlike thesubmerged hydrophytes, the growth of bryo-phytes is restricted or prevented in alkaline wa-


520 Núñez et al.

ters. The bryophytes cannot use bicarbonate,limiting the carbon source to free carbon diox-ide, which is not available in water with evenmoderately high pH (Madsen & Sand-Jensen,1991). In general, acidic lakes are poor in sub-merged species (Vestergaard & Sand-Jensen,2000), and in this type of lakes the bryophytesare the dominant functional group because ofthe greater tolerance to acidity (Wetzel, 2001).In our study, this pattern was reflected in thecomposition of type 2 lakes and ponds in whichthe bryophytes dominated. Moreover, accordingto our results, the water acidity and the otherfactors that limit the development of a greaternumber of functional groups should be com-bined. Thereby, for the deepest systems at highelevation (> 2000 m.a.s.l.), the existence of arocky littoral area and steep slope limited thedevelopment of aquatic plants and only the bryo-phytes had the conditions suitable for growth.Aquatic macrophytes are often limited by highelevations (Gacia et al., 1994; Alahuhta et al.,2011), whereas there is a positive relation-ship with aquatic bryophytes (Maristo, 1941).Similarly, in the more shallow lakes, the lowheterogeneity of habitats favours the predomi-nance of a small number of species or functionalgroups. Vestergaard & Sand-Jensen (2000) andJones et al. (2003) both noted that with anincrease in depth more habitats were availablefor macrophyte colonization.

The role of orthophosphate

Under the conditions of medium alkalinity, theorthophosphate concentration was the deter-mining factor in establishing the typology. Theextreme oligotrophic conditions and, therefore,the high water transparency favoured the devel-opment of the isoetids, and this functional groupwas identified as essential for the differentiationof type 3 bodies of water. The isoetids aredominant when the alkalinity or the pH values ofponds and lakes are not very high (Vestergaard &Sand-Jensen, 2000; Raun et al., 2010); becausethe isoetids are unable to use the bicarbonatein the water (Madsen et al., 2002), they usethe carbon dioxide in sediments as the primary

carbon source for photosynthesis (Sand-Jensen,1987). Thus, the isoetids are photosyntheticallyindependent of the bicarbonate concentration inwater. At a similar position on the pH gradient,a greater availability of phosphorus resulted inan increase in chlorophyll a and in a decrease intransparency, which caused a shift in the compo-sition of the functional groups. Thus, the isoetidsand the submerged hydrophytes were replacedby the bryophytes and the floating-leaved hy-drophytes. The transparency of the water, whichis inversely related to the trophic status of thelake, is a conditioning factor in the compositionof the aquatic plant community (Vestergaard& Sand-Jensen, 2000). As previously estab-lished, with a decrease in water transparency,the macrophyte community changes from onedominated with submerged species to a com-munity of floating-leaved and emergent plants,which are groups of macrophytes that are notaffected by the decrease in light availability withdepth (Moss, 1988; Rodríguez et al., 2003).Furthermore, bryophytes are characterized bythe ability to grow under conditions of low lightintensity (Riis & Sand-Jensen, 1997).The identification of phosphorus as a deter-

minant of the typology of ponds and lakes wassurprising because these systems are not or areminimally affected by human activity. Typically,increased concentrations of phosphorus in a lakeare related to an increase in the external phos-phorus loading, which is characteristic of lakeslocated in landscapes that are heavily affectedby human activities (Kagalou et al., 2008). Inour study, it would not be expected that the ex-ternal loading of phosphorus could be the originof the higher values recorded in type 4 com-pared with the rest of the types of ponds andlakes. Therefore, the role of macrophytes as anutrient source should also be considered. Aqua-tic macrophytes play an important role in nutri-ent cycling because of the production of largequantities of biomass and the capacity to accu-mulate large concentrations of nutrients (Clarke& Wharton, 2001; Abdo & Da Silva, 2002). Theintensity of nutrient uptake by roots and/orshoots and the site of this nutrient uptake areamong the processes that determine the roles of



the different macrophytes in nutrient dynamics(Pieczynska, 1993). The concentrations of nutri-ents in the sediments are generally several ordersof magnitude higher than those in the water(Barko & Smart, 1980; Morris & Lajtha, 1986),and therefore, sediments are the primary sourceof nutrients for aquatic macrophytes (Prentki,1979; Barko et al., 1991; Barko & James, 1998),with nutrients supplied by the water column asa secondary source (Thiebaut & Muller, 2000).The emergent and floating-leaved hydrophytesprimarily obtain nutrients from the sediments,a process favoured by their typically large andwell-developed root systems (Hutchinson, 1975;Granéli & Solander, 1988). However, for thesubmerged macrophytes, diverse studies showedthat nutrient uptake occurred both from the watervia the leaves and from the substrate via the roots(Bristow, 1975; Carignan, 1982). Moreover, thisfunctional group generally has fine roots andare considered even pseudo-rooted macrophytes(Granéli & Solander, 1988). In these cases, theaquatic plants obtain most of the nutrients fromthe water column (Thiebaut & Muller, 2000;Shilla et al., 2006). The type 4 bodies of waterwere characterized by the dominance of floating-leaved hydrophytes, and the aerial and under-ground biomass of this functional group, like thatof the helophytes, are large compared with sub-merged vegetation (Granéli & Solander, 1988).The coverage of the helophytes and the floating-leaved hydrophytes was higher in type 4 lakesthan in the other types. Because the sediment isthe primary compartment for phosphorus storage(Da Silva et al., 1994; Shilla et al., 2006), thesemacrophytes accumulate large amounts of phos-phorus during the growing season, and whenthese macrophytes die, the decomposition pro-cess begins and releases the nutrients back intothe water column, which increases the concentra-tion (Howard-Williams & Allanson, 1981; God-shalk & Barko, 1985; Wetzel, 1996).

Comparison with the previous Spanish typology(ORDEN/ARM/2656/2008)

The variables proposed for the classification oflakes in the nationwide typology (ORDENARM/

2656/2008) differ from the variables that wereused to determine the typology in our study. Thelithology, which directly affects the pH of water,was the primary determinant of the differences inthe composition of the macrophyte community inthe study lakes. However, neither the pH nor theorthophosphate concentration are included in thenational typology. Furthermore, lakes that werecategorized as the same type based on the compo-sition of macrophytes are identified as differenttypes according to the abiotic criteria. Thus, thevariables and limits selected for the nationwidetypology are not useful to explain the naturaldistribution of the macrophytes in the mountainlakes of this study. For example, the three type1 lakes, which were clearly dominated by sub-merged macrophytes and were identified as al-kaline and oligotrophic lakes, are placed in threedifferent types of lakes following the national ty-pology. Notably, the Water Framework Directiveindicates that the validity of a typology based onabiotic factors should be derived from the com-parison with the biological communities of bod-ies of water (European Union, 2000).

CONCLUSIONS

The use of macrophyte functional groups, basedon the criterion of the carbon source used inphotosynthesis, to develop a typology for moun-tain ponds and lakes produced better results thanthe taxonomic approach. Four types of pondsand lakes were established as follow: acidic andoligotrophic, characterized by bryophyte domi-nance; alkaline and oligotrophic, dominated bysubmerged hydrophytes; moderately acidic andoligotrophic, distinguished by the presence ofisoetids; and moderately acidic with a greateravailability of phosphorus, characterized by float-ing-leaved macrophytes and bryophytes. The la-kes at both ends of the pH gradient were char-acterized by a lower diversity of the macrophytefunctional groups. Because the ponds and lakes inthis study were not or were minimally affectedby human activity, the phosphorus released by thebreakdown of aquatic plants in lakes with a highcoverage of floating-leaved and emergent macro-


522 Núñez et al.

phytes was the determinant of the variability of themacrophyte community in this type of mountainlakes.Our studypresents a set of preliminary resultsfor the classification of mountain lakes basedon macrophyte functional groups in the IberianPeninsula, and therefore, subsequent validationwith other reference mountain lakes is required.

ACKNOWLEDGMENTS

The Spanish Ministry of Education and Science(project CGL2006-03927) funded this research.

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