Limnetica, 29 (2): x-xx (2011)Limnetica, 36 (2): 397-404 (2017). DOI: 10.23818/limn.36.11c© Asociación Ibérica de Limnología, Madrid. Spain. ISSN: 0213-8409

On the possible use of Mongolian branchiopods and copepodsto establish reference conditions for ecological quality assessmentof lacustrine water bodies in Spain

Miguel Alonso

Departament de Biologia Evolutiva, Ecologia i Medi Ambient. Universitat de Barcelona.Avda. Diagonal 643. 08028 Barcelona, Spain.

∗ Corresponding author: malonso@ub.edu2

Received: 12/11/14 Accepted: 10/03/17

ABSTRACT

On the possible use of Mongolian branchiopods and copepods to establish reference conditions for ecological qualityassessment of lacustrine water bodies in Spain

A comparison of assemblages of Branchiopoda and Copepoda living in lakes and wetlands in two very distant territories inthe Palaearctic Region, the Iberian Peninsula and Mongolia, is presented. Both territories have significant similarities in thehydromorphological and physicochemical characteristics of their water bodies and in the structure and composition of theirfauna of branchiopods and copepods. Some species occur in both areas, others are taxonomically closely related, and othersbehave as geographic vicariants. Most of these microcrustaceans are used as indicators of ecological quality of standing waterbodies in industrialized European countries, where reference sites are frequently difficult to find. Taking into account theundisturbed conditions of Mongolian water bodies, the alternative of using their branchiopods and copepods, after setting theproper, statistically-based equivalence between Mongolian and Iberian species, as references to assess ecological status inSpain is discussed.

Key words: Branchiopoda, Copepoda, Spain, Mongolia, lake ecological status assessment, reference conditions.

RESUMEN

Sobre el posible uso de Branquiópodos y Copépodos de Mongolia en el establecimiento de condiciones de referencia parael análisis de la calidad ecológica de las masas de agua lacustre en España

Se presenta una comparación de grupos de Branchiopoda y Copepoda de lagos y humedales en dos territorios muy distantesde la región paleártica: la península ibérica y Mongolia. Los dos territorios tienen similitudes significativas en las carac-terísticas hidromorfológicas y fisicoquímicas de sus masas de agua, y también en la estructura y composición de su faunade branquiópodos y copépodos. Algunas especies coinciden, otras son muy próximas taxonómicamente y otras se comportancomo vicarias geográficas. Muchos de estos microcrustáceos se utilizan como indicadores de calidad ecológica en las masasde agua léntica de los países europeos industrializados, donde las condiciones de referencia son frecuentemente difíciles deencontrar. Teniendo en cuenta la situación inalterada de las masas de agua de Mongolia, se discute la alternativa de utilizarsus copépodos y branquiópodos, tras el necesario análisis de las equivalencias entre ellos y los de la península ibérica, comoreferencia para determinar el estado ecológico de los lagos en España.

Palabras clave: Branchiopoda, Copepoda, España, Mongolia, evaluación del estado ecológico en lagos, condiciones dereferencia.

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398 Miguel Alonso

INTRODUCTION

Maintaining the “good ecological status” ofwater bodies is the main objective of the Wa-ter Framework Directive (WFD) (200/60/CE)in all European countries. This Directive wastransposed into Spanish law at the end of 2003.Subsequently, the Instrucción de PlanificaciónHidrológica (hereafter IPH) (Ministerio de Me-dio Ambiente y Medio Rural y Marino, 2008)was implemented, with its objective being to es-tablish the technical criteria to systematicallyand homogeneously develop River Basin Man-agement Plans in Spain. Concerning lakes, theIPH defines the systems and protocols for theecological status assessment, including the defi-nition and exploitation of the biological controlnetworks, and establishes indicators, indexes andreference conditions. The latter are those pre-sented in water bodies of the same category andtype as those intended for assessment under pris-tine conditions or barely altered by anthropicactivities.Several quality elements are taken into ac-

count in the ecological status assessment oflakes: biological (phytoplankton, phytobenthos,macrophytes, benthic invertebrates and fishes),physicochemical and hydromorphological. Asthis paper is concerned with branchiopods andcopepods, it is necessary to refer to the IBCAEL(Índice Biótico de Calidad Ecológica en La-gos) published by the Ministerio de Agricultura,Alimentación y Medio Ambiente of the Span-ish Government in 2013, whose application ismandatory in the exploitation of the official net-works for lake ecological status assessment incompliance with the WFD. The IBCAEL is anadaptation of the QAELS (Qualitat de l’Aigua enEcosistemes Lenítics Soms) index for the wholeSpanish territory designed to assess the ecolog-ical status of shallow water bodies in northeastSpain (Catalonia) (Boix et al., 2005). The IB-CAEL is calculated as the combination of twosubindexes: ABCO (abundance of benthic bran-chiopods, copepods, and ostracods) and the RIC(insect and crustacean richness). The organismsincluded in both the ABCO and RIC are goodindicators because they are very sensitive to

disturbances and changes in their habitats (Stem-berger & Lazorchak, 1994; Hofmann, 1996;Moreno-Amich et al., 1999; Johansson et al.,2005) and spend their entire life cycles, whichare relatively long, in the water. Moreover, be-cause some of these microcrustaceans, mainlycladocerans and ostracods, leave remains in thesediment that have been largely used in palae-olimnological studies (Kattel & Sirocko, 2011;Horne et al., 2012), they are an appropriate toolfor searching for the existing species assem-blages prior to the existence of anthropic pres-sures, that is, reference conditions.Branchiopods and copepods of continental

standing waters are well known in Spain (Alon-so, 1996; 1998); however, the information re-garding these taxa in Mongolia is scattered andincomplete (Sars, 1903; Brtek et al., 1984; Na-ganawa & Zagas, 2002; Flossner et al., 2005;Penkova et al., 2005; Pomazkova & Sheveleva,2006; Alonso & Naganawa, 2008; Sinev et al.,2009; Alonso, 2010; Alonso & Ventura, 2013).In fact, the most comprehensive inventory forthis country is currently being performed bythe author of this paper, with some of the taxamentioned below only partially reported in theabovementioned publications.Reference conditions in Spain are relatively

easy to find in high mountain lakes; however,they are practically absent in lowlands due to theancient occupation of the totality of the territoryby agricultural activities and human settlements.In particular, the lakes in the steppes, whichwere the jewel of the Spanish lacustrine her-itage in the past and are almost entirely uniquein Western Europe, have disappeared or havebeen significantly altered. In Mongolia, steppesare widespread and host a huge number of lakesin pristine conditions. Although the Mongolianand Iberian steppes are bioclimatically differ-ent, their lakes are similar. This and the presenceof even the same or vicarious species and simi-lar species assemblages in both distant territoriescould allow us to use ABCO values obtainedfrom undisturbed Mongolian lakes as referenceconditions for the Spanish lakes.In this paper, Spanish and Mongolian lakes

and lagoons and their branchiopod and copepod

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On the possible use of Mongolian branchiopods and copepods... 399

assemblages are compared. The convenience ofusing the conditions of Mongolian lakes as areference for Spanish lakes is discussed.

MATERIALS ANDMETHODS

Samples were collected during an extensivesurvey performed throughout the Mongolian ter-ritory, considering all of its natural zones (alpinebelts, taiga, forest-steppe, steppe, semidesert and

desert zones) between 2005 and 2013. In total,878 lakes were sampled. Abbreviated descrip-tions of all the lakes and photos can be seen athttp://geodata.es/mongolian_lakes. The surveyswere conducted in September-October, after therainy season and before the freezing of the lakesurface; during this period, the crustacean com-munities reach their peak of maturity, and malesand gamogenetic females appear in the clado-ceran populations. Samples were obtained fromrepresentative habitats in each lake (littoral ar-

Table 1. Correspondence between the IPH and IBCAEL typologies of lakes and lagoons in Spain and the typologies defined forMongolian lakes in this paper. Correspondencia entre las tipologías IPH e IBCAEL de lagos y lagunas en España y la tipologíadefinida para los lagos de Mongolia en este trabajo.

TypologyIPH

DescriptionTypologyIBCAEL

TypologyMONGOLIA

1 NORTHERNHIGHMOUNTAIN. DEEP. ACIDIC WATERS

1

A

2 NORTHERNHIGHMOUNTAIN. DEEP. ALKALINEWATERS3 NORTHERNHIGHMOUNTAIN. SHALLOW. ACIDICWATERS4 NORTHERNHIGHMOUNTAIN. SHALLOW. ALKALINEWATERS5 NORTHERNHIGHMOUNTAIN. DEEP. ALKALINEWATERS

6 MEDIUMMOUNTAIN. DEEP. ACIDIC WATERS27 MEDIUMMOUNTAIN. DEEP. ALKALINEWATERS

8 MEDIUMMOUNTAIN.SHALLOW.ALKALINEWATERS

9 SOUTHERNHIGH MOUNTAIN 1

10 KARSTIC, CALCAREOUS, PERMANENT, HYPOGENIC211 KARSTIC, CALCAREOUS, PERMANENT, UPWELLING

12 KARSTIC, CALCAREOUS, PERMANENT, TRAVERTINIC

13 KARSTIC, CALCAREOUS, TEMPORARY 7 B

14 KARSTIC, EVAPORITES, HYPOGENIC OR MIXT, LARGE3

A

15 KARSTIC, EVAPORITES, HYPOGENIC OR MIXT, SMALLB

16 INTERIOR IN SEDIMENTATION BASIN (ISB), LOWMINERALIZATION,PERMANENT 4

17 ISB, LOWMINERALIZATION, TEMPORARY 7 B-D

18 ISB, MEDIUMMINERALIZATION, PERMANENT 4 C

19 ISB, MEDIUMMINERALIZATION, TEMPORARY 8 C-D

20 ISB, HIGH OR VERY HIGH MINERALIZATION, PERMANENT 5 C

21 ISB, HIGH OR VERY HIGH MINERALIZATION, TEMPORARY 8 C-D

22 ISB, HYPERSALINE, PERMANENT 6E

23 ISB, HYPERSALINE, TEMPORARY 9

24 ISB, FLUVIAL ORIGIN, FLOOD PLAIN, LOW OR MEDIUMMINERALIZATION

3

A-B

25 ISB, FLUVIAL ORIGIN, FLOODPLAIN, HIGH OR VERY HIGHMINERALIZATION C

26 ISB, FLUVIAL ORIGIN, FLOODPLAIN, ABANDONEDMEANDERB

27 ISB, ASSOCIATED TO ALKALINE PEATS

28 COASTAL LAGOONSWITHOUTMARINE INFLUENCE 5

29 COASTAL AMONG DUNES, PERMANENT 3

30 COASTAL AMONG DUNES, TEMPORARY 7

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400 Miguel Alonso

eas, open water, among vegetation) using twohandheld nets with mesh sizes of 100 µm forcladocerans and copepods and 1 mm for largebranchiopods. Specimens were preserved in 4%formaldehyde. In the laboratory, most taxa wereidentified to species.

RESULTS

Types of lakes in Mongolia

Five types of lakes can be defined in Mongoliaaccording the following descriptors: morphom-etry, hydroperiod, mineralization, and inorganicturbidity. This approach is similar to that adoptedto classify lakes and lagoons in Spain by Alonso(1998). A brief description of the five types isgiven below.

• Type A. Large permanent freshwater lakes.In this type of lake, the maximum depthexceeds that which might be colonized by sub-merged aquatic vegetation, so lake metabolismis controlled by the plankton (trophic sta-tus). The specific electrical conductance isbelow 4 000 µS/cm. The biota is freshwaterstenohaline. Fish are present.

• Type B. Smaller permanent or semipermanentfreshwater lakes. In these lakes, aquatic sub-merged vegetation can colonize almost all ofthe lake bottom and therefore controls lakemetabolism. Water turbidity is not due to inor-ganic suspended particles. Specific electricalconductance is below 4 000 µS/cm. The biotais freshwater stenohaline. Fish are present inlakes deeper than 4 m (ice cover can exceed athickness of 2 m in winter).

• Type C. Large lakes and lagoons, either per-manent or temporary, with highly mineralizedor even saline (not hypersaline) waters. Spe-cific electrical conductance between 4 000 and45 000 µS/cm. The biota is euryhaline. Fishare present.

• Type D. Shallow lakes and lagoons, either per-manent or temporary, with slightly to highly

mineralized waters, turbid due to suspendedinorganic particles. Specific electrical conduc-tance 4 000-42 500 µS/cm. Turbidity does notallow submerged macrophyte growth. Lakemetabolism is heterotrophic. Euryhaline biota.No fish present.

• Type E. Hypersaline lakes. Specific electri-cal conductance from 45 000 to more than200 000 µS/m. Stenohaline athalassic salinebiota. No fish present.

Branchiopod and copepod assemblagesin Mongolia

The inventory of the Mongolian microcrus-taceans on which this paper is based includeseighty-seven branchiopod and forty-nine cope-pod species.Branchiopods include 10 Anostraca, 4 Con-

chostraca, 2 Notostraca, 3 Ctenopoda, 1 Haplo-poda and 66 Anomopoda species. With respectto the Iberian fauna (Alonso, 1996; 1998), anos-tracans, conchostracans and notostracans are themost distinct groups, since only two anostracanspecies coincide. Of the three ctenopods, twoare known in the Iberian Peninsula. Althoughhaplopods do not occur on the Iberian Penin-sula, there are 49 anomopod species in commonbetween the two areas.The copepods include 20 Calanoida, 26 Cy-

clopoida and 3 Harpacticoida species. Of thecalanoids, which are prone to geographical spe-ciation, only three species occur in both areas,whereas twenty cyclopoid species are shared be-tween Mongolia and the Iberian Peninsula. Allharpacticoids found in Mongolia also live in theIberian Peninsula.

DISCUSSION

The use of Mongolian lakes as reference con-ditions for the ABCO subindex relies on twoassumptions: (1) Spanish and Mongolian lakesare typologically equivalent, and (2) microcrus-tacean assemblages in lakes of the same typeresemble one another when undisturbed.

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On the possible use of Mongolian branchiopods and copepods... 401Table2.

CharacteristicBranchiopodaandCopepodaassemblagesinthedifferenttypesoflakesinSpainandinMongolia.Geographicallyvicarioustaxainbold.Asociaciones

característicasdeBranchiopodayCopepodaenlosdiferentestiposdelagosenEspañayenMongolia.Ennegritalostaxonesconvicarianzageográfica.

Typeoflake

AB

CD

E

Characteristicalliance

(Alonso1998)

Daphnionlongispinae

Simocephalionvetuli

Arctodiaptomion

Mixodiaptomion

incrassati

Artemion

Arctodiaptomion

Characteristicassociations

(Alonso1998)

Chydoro-Eucyclopidetum

serrulati,

Eurycercetumlamellati,

Simocephalo-Daphnietum

magnae

Mixodiaptometum

incrassati

AssociationofArtemia

parthenogenetica

Acanthocyclopidetum

Simocephaletumvetuli

Arctodiaptometum

wierzjeski

Triopsetum

mauritanici

Arctodiaptometum

salini

Hemidiaptomo-Chirocephaletum

diaphani

Alona

salina

Branchipetumschaefferi

Branchinecto-Daphnietumatkinsoni

Characteristicspecies

inSpain

Alona

affinis

Chirocephalusdiaphanus

Daphniamagna

Branchipussp.pl.

Artemia

parthenogenetica

Alona

guttata

Simocephalusvetulus

Simocephalusexspinosus

Branchinectaferox

Phallocryptusspinosa

Coronatellarectangula

Scapholeberisrammneri

Pleuroxusletourneuxi

ChirocephalusdiaphanusBranchinectellamedia

Chydorussphaericus

Eurycercuslamellatus

Alonasalina

Streptocephalus

torvicornis

Daphniamediterranea

Eucyclopsserrulatus

Chydorussphaericus

Arctodiaptomus

wierzjeskii

Cyzicusgrubei

Moina

salina

Macrocyclopsalbidus

Pleuroxusaduncus

Diacyclopsbicuspidatus

Triopscancriformis

mauritanicus

Arctodiaptomussalinus

Coronatellarectangula

Megacyclopsviridis

Daphniaatkinsoni

Cletocamptusretrogressus

Graptoleberistestudinaria

Daphniasimilis

Hemidiaptomusroubaui

Moina

brachiata

Diaptomuscyaneus

Pleuroxusletourneuxi

Eucyclopsserrulatus

Mixodiaptomus

incrassatus

Characteristicspecies

inMongolia

Alona

affinis

Chirocephalusbobrinskii

Daphniamagna

Branchipodopsisaffinis

Artemiasinica

Alona

guttata

Simocephalusvetulus

Moina

mongolica

Branchinectaorientalis

Branchinectellamedia

Alonawerestschagini

Eurycercuslamellatus

Alonaflossneri

Phallocryptus

tserensodnomi

Moina

salina

Coronatellarectangula

Chydorussphaericus

Arctodiaptomussalinus

Galaziellasp.pl.

Metadiaptomusasiaticus

Chydorussphaericus

Pleuroxustruncatus

Megacyclopsviridis

Cyzicusdavidi

Cletocamptuscf.

retrogressus

Eucyclopsdumonti

Pleuroxusannandalei

Triopscf.granarius

Macrocyclopsalbidus

Hemidiaptomusignatovi

Daphniasimilis

Arctodiaptomusacutilobatus

Moina

brachiata

Arctodiaptomus

rectispinosus

Metadiaptomusasiaticus

Metacyclopsminutus

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402 Miguel Alonso

Table 1 shows the relationship between thelake typologies of the IPH and IBCAEL forSpain and those categories defined for Mongo-lia. The IPH establishes thirty types of lakes inSpain. Lake typology was defined according tothe origins of the lake basins (glacial, karstic,fluvial, coastal), altitude, mineralization andtype of hydroperiod. The IPH also considers asa distinguishing feature the location in interiorsedimentation basins, which is clearly related tosteppe conditions in Spain (Suarez Cardona et.al., 1992).The IBCAEL typology distinguishes nine

types. Except for types 6, 8 and 9, which uni-vocally correspond to the IPH types 22, 19 and23, the rest correspond to groups of IPH typeshaving similar characteristic microcrustaceanassemblages with regard to the ABCO subindex.Excluding IPH types 28, 29 and 30, which are

coastal, the rest of the Spanish lake types havea homologous type in Mongolia. Mountain andlarge karstic lakes in Spain (IPH types 1-12 and14) correspond mostly to IBCAEL typologies1, 2, and type “A” in Mongolia. IPH types 13,15, 16, 17, 24, 26 and 27, which are generallyfreshwater shallow lagoons, can be assimilatedto type “B” in Mongolia or to type “D” if the wa-ter is turbid because of inorganic particles. IPHtypes 18-20 and 25, which are characterized bymedium or high mineralization, can be assimi-lated to type “C” in Mongolia or also “D” if theyhave inorganic turbidity. In addition, the IPHtypes that are hypersaline can be assimilated totype “E” in Mongolia.The comparison of the benthic microcrus-

tacean assemblages between the types of lakesand lagoons in Mongolia and in Spain is shownin Table 2. In Alonso (1998), the Spanish micro-crustacean communities were characterized bystudying the similarity among 470 inventoriesfrom a group of Spanish lakes and lagoons rep-resentative of all existing types and all regionsin the country. The analysis distinguished fivetaxocenoses, which were designated alliancesand associations and helped to finally define thetypology of lakes and lagoons in Spain. Thistypology coincides with that established in Mon-golia because it is based on the same principles.

“Characteristic species” in Table 2 indicates themost frequent taxa in each taxocenosis so that theabsence of one taxon in one of the assemblagesdoes not necessarily imply that it is absolutelyabsent in the country to which the assemblage inquestion applies.For type “A”, most taxa are coincident. For

the other types, the taxa that could be used inMongolia to establish reference conditions aremainly geographically vicarious, coinciding inmost cases at the genus level. Some cases areinteresting, such as Arctodiaptomus salinus,which has been found in Spain in El Tobar (Mir-acle et al., 1993) and Banyoles karstic lakes(Miracle, 1976) but also in most hypersalineendorheic lakes (Alonso, 1990); such ambiva-lence has never been investigated, and there arelikely two different species under this specificname. In Mongolia, A. salinus never appears inhypersaline waters, only in highly mineralizedwaters, being Metadiaptomus asiaticus whichcharacteristically inhabit hypersaline waters..According to the observations presented here,

the use of Mongolian lakes as reference condi-tions for the IBCAEL index in Spain, mainly forsteppe lakes, seems to be realistic. The next stepshould include the necessary statistical analy-sis to assign to each taxon the sensibility valuewhich, as was done in Spain, is based on an anal-ysis of the fidelity of the different taxa to eachdetermined lake typology.

ACKNOWLEDGEMENTS

This study has been supported by the Programfor Biodiversity Conservation of ENDESA(Empresa Nacional de Electricidad S.A.).

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17140_Limnetica 36(2), pàgina 404, 28/09/2017

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