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Ceachile.clCrustaceana 86 (13-14) 1634-1643 ZOOPLANKTON IN LAGUNA LEJÍA, A HIGH-ALTITUDE ANDEAN SHALLOW LAKE OF THE PUNA IN NORTHERN CHILE ANDRÉS MUÑOZ-PEDREROS1,3), PATRICIO DE LOS RÍOS1) and PATRICIA MÖLLER2) 1) Escuela de Ciencias Ambientales, Facultad de Recursos Naturales, Núcleo de Estudios Ambientales NEA, Universidad Católica de Temuco, Casilla 15-D, Temuco, Chile 2) Programa de Humedales, Centro de Estudios Agrarios y Ambientales CEA, Casilla 164, The Puna is a high altitude ecosystem of the Central Andes located in the desert plateaus above 3500 m a.s.l. that covers parts of north-eastern Chile, north-western Argentina, south-eastern Peruand mid-western Bolivia. It is characterised by the presence of endorheic basins. Laguna Lejía isan oligohaline shallow lake with alkaline pH, located in the Atacama Puna above 4000 m a.s.l. It issurrounded by volcanoes and enclosed in a secluded basin that is of great scientific interest, due toits ecological insularity. It has been designated by the government as a priority site for biodiversityconservation. The object of this study was to analyse the specific composition and the structure ofthe zooplankton community in this shallow, high altitude lake. In March 2012, zooplankton sampleswere taken for qualitative and quantitative analysis from 13 sampling stations in the lake and twoadjacent pools. The bodies of water were characterised in the field using portable equipment, with thefollowing parameters being measured: pH, water temperature, conductivity, and dissolved oxygen.
The results indicate that the type of zooplankton community matches relatively well that observed inother low salinity, high Andean wetlands, although no calanoid copepods were found. The speciesfound have been reported for high Andean zones and shallow lakes in countries bordering Chile.
The absence of species with wide geographical distribution specific for low salinity, high Andeanenvironments, is presumably due to the presence of geographical and environmental barriers thatprevent colonization by those species.
Key words. — High altitude wetland, Macrothrix palearis, Alona sp., Diacyclops andinus La Puna es un ecosistema de gran altitud de los Andes Centrales que se encuentra en las mesetas del desierto por encima de los 3500 msnm, que cubre partes del noreste de Chile, el noroestede Argentina, el sudeste de Perú y medio oeste de Bolivia. Se caracteriza por la presencia decuencas endorreicas. Laguna Lejía es un lago somero, oligohalino, con pH alcalino, que se encuentra 3) Corresponding author; e-mail: [email protected]; [email protected] Koninklijke Brill NV, Leiden, 2013 ZOOPLANKTON IN LAGUNA LEJÍA, CHILE en la puna de Atacama por encima de 4000. Está rodeada de volcanes, en una cuenca cerradade alto interés científico por su insularidad ecológica que ha sido designado por las autoridadesgubernamentales sitio prioritario para la conservación de la biodiversidad. El objetivo de este estudioes analizar la composición específica y estructura del zooplancton de este lago somero. Se muestreóen marzo de 2012 (verano septentrional) en 13 estaciones abarcando el lago y dos cuerpos de aguaadyacentes, extrayéndose muestras de zooplancton para el análisis cuali y cuantitativo. En terrenose caracterizaron los cuerpos de agua y se midieron los parámetros pH, temperatura del agua,conductividad y oxígeno disuelto, con equipo portátil. Los resultados indican que el tipo de ensamblezooplanctónico se ajustaría relativamente a lo observado para otros humedales altoandinos de bajasalinidad, no obstante no se encontraron copépodos calanoideos. Las especies encontradas han sidoreportadas para zonas altoandinas y lagos someros altoandinos de países limítrofes a Chile. Laausencia de especies de amplia distribución geográfica que son propias de ambientes altoandinos debaja salinidad se debería presumiblemente a que la presencia de barreras geográficas y ambientalesevitarían su colonización por otras especies.
The Puna is an ecosystem of the Central Andes located on the desert plateaus above 3500 m a.s.l. (Marquet et al., 1998), and it covers parts of north-easternChile, north-western Argentina, south-eastern Peru, and mid-western Bolivia. It isa region of high peaks and recent volcanic activity. In Chile, it extends from 17°30to 28° south, and westward from the eastern border of the country, with a width of20-70 km (Garcia, 1967; Troll, 1968; Luebert & Gajardo, 2000).
Laguna Lejía is a shallow lake set in the Atacama Puna, in an endorheic basin. This watershed, located in the highland climate zone, has seasonal runoff,and a pluvio-nival regime with a moderate slope (Klohn, 1972; Ferrando, 1992-1993; Grosjean, 1994). Like other secluded basins of the Andean plateau, it ischaracterised by the presence of more depressed areas towards its western edge,where surface and subterranean waters collect. The precipitation that falls on theAndean plateau is collected by drainage systems, which are characterized by theabsence of perennial watercourses that can reach the more depressed areas. Therun-off watercourses which flow across impermeable rocks then infiltrate intofractured rocks or clastic sedimentary material to form phreatic aquifers. The watercommonly is welling up in the form of springs (Risacher et al., 1998).
High mountain wetlands are of great scientific interest due to their ecological insularity, their pristine condition, and are also difficult to access (Locascio deMitrovich et al., 2005). In shallow lakes located on the Andean plateau of northernChile and Peru, endemic species of zooplankton have been recorded (Bayly, 1992;Villalobos, 1994, 2006). The crustacean zooplankton assemblages in water bodiesof the Atacama Puna are characterized by low species richness and an inverserelation between species number and salinity (De los Ríos-Escalante, 2010).
The object of this study is to analyse the specific composition and the structure of the zooplankton of Laguna Lejía as a priority site for biodiversity conservationin northern Chile.
ANDRÉS MUÑOZ-PEDREROS, PATRICIO DE LOS RÍOS & PATRICIA MÖLLER MATERIAL AND METHODS The study area is located 103 km south-east of the town of San Pedro de Atacama, in the Antofagasta Region (fig. 1), northern Chile (23°30S 67°42W).
The area ranges above 4350 m a.s.l. and is located in a desert depression. It liesin a hydrographical basin covering 193 km2, in which the bodies of water cover1.9 km2 (Grosjean, 1994; Risacher et al., 1998). The lake is shallow (1 m) andits hydrological parameters are controlled by subterranean springs. There is littleprecipitation (<200 m year−1), excessive evaporation (>2000 mm year−1), a run-off coefficient (ratio between the amount of precipitation that falls on the drainagebasin and that which enters the lake) of 0.089, and limited internal drainage(estimated at 40 l min−1) (Grosjean et al., 1994, 1995; Risacher et al., 1998).
The lake is the remnant of a large glacial lake, and lies 15 km south of the Láscar volcano, formed in a tectonic depression related with the Miscanti-Callejónde Varela fault.
The geo-morphological units form an amphitheatre, of which Laguna Lejía is the centre. It is surrounded by the Láscar volcano to the northwest (the most activein the central volcanic zone of the Andes), the Aguas Calientes volcano to thenorth, the Chiliques volcano to the south, and the Lena and Lejía mountains to thesouth west, which form part of the Puntas Negras range (Gardeweg et al., 1998).
The average height of the surrounding volcanoes is 5700 m a.s.l., but their elevationfrom base to summit is only 800-900 m. To the north-east of the lake is the Altosde Toro Blanco range, which forms the watershed between the Lejía and Salarde Aguas Calientes basins. It forms a low range between the two wetlands, withaverage height 4300 m a.s.l.
Fig. 1. Study area and sampling stations in the Laguna Lejía, northern Chile. S, south; N, north; E, east; W, west.
ZOOPLANKTON IN LAGUNA LEJÍA, CHILE The climate according to Köppen's classification is high altitude steppe (BSH) (Di Castri & Hajek, 1976) with low temperatures presenting wide daily oscillationand precipitations concentrated in summer (50 to 150 mm year−1), with strongannual variation and series of very dry or very wet years (three times theprecipitation of a dry year) which exceed the capacity of the poorly developeddrainage network and produce torrential water flows which have modelled themorphology. Evaporation from water and soil surfaces is very high (1500-2500 mmyear−1) and the relative humidity is very low (<20%), all of which explain the higharidity of the site (Luebert & Pliscoff, 2006).
The vegetation surrounding Laguna Lejía has been studied by Muñoz-Pedreros et al. (unpubl.) and is characterized by the presence of two communities: one,set in the lake, is a Stipa-Deyeuxia community consisting of some 23 speciesof herbaceous plants and low shrubs, including Stipa frigida Phil., Stipa nar-doides (Phil.) Hackel ex Hitchc., Deyeuxia cabrerae (Parodi) Parodi, Deyeuxiaantoniana (Griseb.) Parodi, Pycnophyllum bryoides (Phil.) Rohrb., Pycnophyllummacropetalum Mattf., Mulinum crassifolium Phil. and Junellia pappigera (Phil.)N. O'Leary & P. Peralta. It is a community characteristic of the highest sectorsof the Andes, generally marking the upper limit of vegetation. The other com-munity, in the eastern area of the lake, is a Puccinellia-Calandrinia communitywith six herbaceous species (e.g., Puccinellia frigida (Phil.) I. M. Johnst., Calan-drinia compacta Barnéoud, Xenophyllum incisum (Phil.) V. A. Funk and Arenariarivularis Phil.). This is a hygrophilous community typical of the borders of waterbodies, representing the azonal vegetation of this lacustrian wetland, and owes itsexistence to springs of subterranean water to the east of the lake which generatesmall, parallel pools adjacent to it.
Samples were collected in March 2012 at the four cardinal points around Laguna Lejía, with special emphasis on sampling in the eastern sector, both in the lake itselfand in two parallel pools adjacent to the lake (fig. 1). Samples of zooplankton weretaken at the 13 stations (5 replicates for the lake, 3 for pool 1 and 5 for pool 2) forqualitative and quantitative analysis, by filtration of 30 litres of superficial waterper station, using a conventional conical net with 50 μm mesh, and following themethods described by Soto & De los Ríos (2006). The material was fixed in situwith alcohol at 75%.
Observation, taxonomic identification and measurement of the specimens were done under optical microscope and stereoscopic microscope, using specialistliterature for identification (e.g., Araya & Zúñiga, 1985; Reid, 1985; Bayly, 1992;González, 2003). Counts were based on Cassie's formula (Edmonson & Winberg, ANDRÉS MUÑOZ-PEDREROS, PATRICIO DE LOS RÍOS & PATRICIA MÖLLER 1971), with 10% error, in 1 and 5 cm3 samples Sedgwick Rafter chambersfor microzooplankton (crustacean nauplia and rotifers) and macrozooplankton(Cladocera, copepodites and adult copepods) respectively, or total counts whenthe abundance was very scarce. The water bodies were characterised in the field,measuring pH, water temperature, conductivity and dissolved oxygen, using WTW3400i multi-parameter equipment, fitted with: WTA temperature sensor (precision0.1°C); Tetra-con 325 conductivity sensor (precision 0.2 μS); CellOx 325 foroxygen (sensitivity 0.1 mg/l); and pH Sentix 20 (0.1 sensitivity pH units).
The data were analysed first by a correlation analysis of the abundances of the species reported and the parameters considered in the present study. Next, ahierarchical agglomerative clustering analysis using the Bray-Curtis index wasapplied to determine possible similarities between the groups. For both theseanalyses, Biodiversity Pro version 2.0 software (Mc Aleece et al., 1997) wasused. The next step was to calculate a Checkerboard score (C-score), which isa quantitative index of occurrence that measures the extent to which species co-occur less frequently than expected by chance (Gotelli, 2000). One can considerthat a community is structured by competition when the C-score is significantlylarger than expected by chance (Gotelli, 2000). Thirdly, co-occurrence patternswith null expectations were compared via simulation. Gotelli & Etsminger (2007)and Gotelli (2000) suggest the following robust statistical null models: (1) Fixed-Fixed: in this model the row and column sums of the matrix are preserved. Thus,each random community contains the same number of species as the originalcommunity (fixed column), and each species occurs with the same frequency asin the original community (fixed row). (2) Fixed-Equiprobable: in this algorithmonly the row sums are fixed, and the columns are treated as equiprobable.
This null model considers all the samples (column) as equally available for allspecies. (3) Fixed-Proportional: in this algorithm the species occurrence totals aremaintained as in the original community, and the probability of a species occurringat a site (column) is proportional to the column total for that sample. These nullmodel analyses were performed using the Ecosim version 7.0 software (Gotelli &Etsminger, 2007). Finally a niche sharing null model was applied using Pianka'sand Czekanowski's overlap indices with retained niche breadth and reshuffled zerostates using the Ecosim version 7.0 software (Gotelli & Etsminger, 2007). TheEcosim program also determines whether measured overlap values differed fromwhat would be expected in random sampling of the species data. Ecosim performsMonte Carlo randomisations to create pseudo-communities and then statisticallycompares the patterns of these randomised communities with those in the real datamatrix (Gotelli & Etsminger, 2007). In this analysis all values of the general matrixwere randomised 1000 times and the niche breadth was retained for each species.
In other words, the algorithm retained the amount of specialisation for each species(Gotelli & Etsminger, 2007).
ZOOPLANKTON IN LAGUNA LEJÍA, CHILE RESULTS AND DISCUSSION High variability is found in almost all the parameters measured at the different sampling stations in the lake Laguna Lejía and the small pools to the east (table I;fig. 1). The oxygen concentrations are lower in the small pools than in the lake. Thehighest concentrations of dissolved oxygen are associated with the stations wherethe water temperature is highest (table I).
The results of the correlation analyses (table I) indicate that the abundance of Macrothrix palearis Harding, 1955 is directly related to the pH, conductivity andthe abundances of Alona sp., Diacyclops andinus Locascio de Mitrovich & Menu-Marque, 2001 and Ostracoda; while the abundance of Alona sp. has a significant,directly proportional relation to the conductivity and the abundance of D. andinusand Ostracoda (table II). At the same time the abundance of harpacticoids hasa significant, directly proportional relation to the temperature; and finally, theabundance of ostracodes has a significant, directly proportional relation to the pH,the conductivity and the abundance of M. palearis (table II).
The results of all simulations in null model species associations showed that the species associations were random (table III), while the results of the nichesharing model indicate that there are differences in the niche structure (table III).
The results of the cluster analysis show that the eastern and southern sites are themost similar, followed by the lake East-1, lake East-2 and North sites, respectively(fig. 2).
The pH values recorded are higher than those recorded by Grosjean et al. (1995) in the same lake, and in the adjacent pools. The great variability in the conductivity Physical and chemical parameters of the water, and taxa recorded in Laguna Lejía, northern Chile Physical and chemical water parameters Temperature (°C) Conductivity dil (5 : 50) (mS cm−1) Dissolved oxygen (mg l−1) Crustacean zooplankton (ind. l−1) Macrothrix palearis Harding, 1955 Alona sp.
Locascio de Mitrovich &Menu-Marque, 2001 Ostracoda indet.
ANDRÉS MUÑOZ-PEDREROS, PATRICIO DE LOS RÍOS & PATRICIA MÖLLER Results of the correlation analyses for species associations and niche sharing Macrothrix Alona sp. Diacyclops andinus Harpacticoida Ostracoda M. palearis Alona sp.
Locascio de Mitrovich &Menu-Marque, 2001 ∗ Significant associations and absence of randomisation (P <0.05).
both within the lake and between it and the pools to the east was also recorded byGrosjean et al. (1995) in Laguna Lejía and the neighbouring pools. As Risacher etal. (1998) suggest, marked salinity gradients in the direction of water run-off occurin the shallow lakes in the basins of Northern Chile due to intense evaporation.
These authors measured a potential evaporation of 1500 mm year−1 in LagunaLejía. The conductivity did not exceed the value of 6.4 mS cm−1 indicated byGrosjean et al. (1995) for Laguna Miscanti, which has the least saline waters in theAndean plateau, in any of the sampling stations.
Hann (1986), in his review of the genus Daphniopsis Sars, 1903 (Cladocera, Daphniidae), described Daphniopsis chilensis Hann, 1986 from the crater lake of Results of the null model analyses for species associations and niche sharing Observed index Average index Standard effect of size Variance Species association Czekanowski's index ∗ Significant associations and absence of randomisation (P <0.05).
ZOOPLANKTON IN LAGUNA LEJÍA, CHILE Fig. 2. Similarity dendrogram of the sites considered in the present work.
the Licancabur volcano (22°50S 67°50W), but this species was not recorded inLejía, despite the relative proximity of the two wetlands.
Information on limnic zooplankton in high Andean wetlands indicates that there is a significant inverse relation between the number of species and the salinity (Delos Ríos-Escalante, 2010). In general it is observed that at salinities between 5 and90 g l−1, the halophilic copepod Boeckella poopoensis Marsh, 1906, predominatesand may even be the exclusive zooplankton species; while at salinities greater than90 g l−1, Artemia franciscana Kellogg, 1906, predominates, and may also be theexclusive component of the zooplankton (De los Ríos-Escalante, 2010; De los Ríos& Gajardo, 2010). At salinities below 5 g l−1 there is a relatively high richness ofspecies, in which calanoid copepods proper to low salinities, such as Boeckellagracilipes Daday, 1902, or Boeckella occidentalis Marsh, 1906, can coexist withcladocerans principally of the Daphnidae and Chydoridae families (De los Ríos-Escalante & Gajardo, 2010). Thus the type of zooplankton community observed inthe present study fits relatively well with that observed in other low salinity, highAndean wetlands, even if no calanoid copepods were found.
The species recorded in Laguna Lejía were observed in high Andean zones. M. palearis and D. andinus have been described for Chungará Lake (Araya & Zúñiga,1985; De los Ríos-Escalante, 2010) and high Andean shallow lakes in countries ANDRÉS MUÑOZ-PEDREROS, PATRICIO DE LOS RÍOS & PATRICIA MÖLLER bordering Chile (Locascio de Mitrovich et al., 2005; De los Ríos & Gajardo, 2010).
The absence of species with wide geographical distribution which are proper to lowsalinity, high Andean environments, such as Daphnia pulex Leydig, 1860 and B.
gracilipes Daday, 1901, is presumably due to the presence of many geographicaland environmental barriers.
The authors are grateful for the project Analysis of the biodiversity of the Antofagasta Region (2007-2008), financed by Comisión Nacional del MedioAmbiente/Fondo Nacional de Desarrollo Regional and executed by the Centrode Estudios Agrarios y Ambientales (CEA). They acknowledge the support ofthe General Directorate of Research and Post-graduate Studies of the CatholicUniversity of Temuco, DGIPUCT Project No CD2010-01 and Mecesup ProjectUCT 0804. They thank Patricia Mejías of the Catholic University of Temucofor the water analyses done in situ and Cesar Pizarro of the National ForestryCorporation (CONAF) of the Antofagasta Region, Chile, for his valuable logisticalassistance in the field.
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First received 1 May 2013.
Final version accepted 20 October 2013.
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