versão On-line ISSN 0718-560X
Lat. Am. J. Aquat. Res. vol.40 no.2 Valparaíso jun. 2012
Lat. Am. J. Aquat. Res., 40(2): 473-479, 2012
Regulatory factors in crustacean zooplankton assemblages in mountain lakes of northern Chilean Patagonia (38-41°S): a comparison with Bulgarian counterparts (42°N)
Factores reguladores en ensambles de crustáceos zooplanctónicos en lagos de montaña del norte de la Patagonia chilena (38-41°S): una comparación con sus contrapartes de Bulgaria (42°N)
Patricio De los Ríos-Escalante1,2, Enrique Hauenstein1, Patricio Acevedo3,4 Mario Romero-Miéres1 & Ivan Pandourski5
1Laboratorio de Ecología Aplicada y Biodiversidad, Escuela de Ciencias Ambientales Facultad de Recursos Naturales, Universidad Católica de Temuco, P.O. Box 15-D, Temuco, Chile
2Nucleo de Estudios Ambientales, Universidad Católica de Temuco, P.O. Box 15-D, Temuco, Chile
3Departamento de Ciencias Físicas, Facultad de Ingeniería Ciencias y Administración Universidad de la Frontera, P.O. Box 54-D, Temuco, Chile
4Center for Optics and Photonics, Universidad de Concepción, P.O. Box 160-C, Concepción, Chile
5Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences 2 Gagarin Street, 113, Sofia, Bulgaria
ABSTRACT. Chilean Patagonia has protected mountainous areas with evergreen native forests; in which the lakes and rivers, of volcanic or glacial origin, are oligotrophic. In Bulgaria, there are mountainous zones with native forests and associated lakes of volcanic origin. The aim of the present study is to carry out a preliminary comparison of zooplanktonic crustaceans in lake ecosystems associated with native forests of Chilean Patagonia and of Bulgarian mountains. The study revealed that the lakes studied in Chilean Patagonia are associated mainly with Nothofagus forests; they are oligotrophic, with a low number of zooplanktonic crustacean species. Similar results were observed for Bulgarian mountain lakes associated with Fagus forests. A null model analysis of species co-occurrence was applied to the two groups of lakes, and the result revealed the absence of regulatory factors in species associations. These studies agree with similar descriptions of lakes in Andean Patagonia and New Zealand. They highlight the important role of native Nothofagus forests in Argentina and Chile, and of Fagus forests with associated soil properties in Bulgaria, in the oligotrophy of the lakes studied.
Keywords: Nothofagus, Fagus, native forests, lakes, oligotrophy, zooplankton, Bulgaria, Chile.
RESUMEN. La Patagonia de Chile tiene una serie de áreas protegidas con bosques nativos perennes asociados a lagos y ríos oligotróficos y de origen glacial. Por otro lado en Bulgaria hay una serie de zonas montañosas con lagos asociados de origen volcánico o glacial. El objetivo del presente trabajo es realizar una primera descripción de especies de crustáceos zooplanctónicos en ecosistemas lacustres asociados a bosques nativos en la Patagonia de Chile y en las montañas de Bulgaria. Los estudios indican que los lagos de la Patagonia de Chile están asociados principalmente con bosques de Nothofagus, mientras que similares resultados fueron observados en lagos de Bulgaria con bosques de Fagus. La regresión lineal entre concentración de clorofila y número de especies para lagos chilenos, fue significativa mientras que en lagos de Bulgaria el análisis de regresión no indicó diferencias significativas. Se aplicó un análisis de co-ocurrencia de especies para ambos grupos de lagos y los resultados indicaron la ausencia de factores reguladores en las asociaciones de especies. Estos estudios concuerdan con descripciones similares para lagos de la Patagonia andina y Nueva Zelanda, y remarcan el rol de los bosques nativos de Nothofagus en Argentina y Chile, así como la presencia de bosques de Fagus y las propiedades del suelo en Bulgaria, como regulador importante de la oligotrofía asociada a los lagos analizados.
Palabras clave: Nothofagus, Fagus, bosques nativos, lagos, oligotrofía, zooplancton, Bulgaria, Chile.
The mountain lakes of Chilean North Patagonia (38-42°S) are oligotrophic, of glacial origin, with low numbers of zooplanktonic crustacean species. They are associated with native Nothofagus Blume forest, particularly N. antarctica (G. Forst.) Oerst., N. pumilio (Poepp. et Endl.) Krasser, and N. dombeyi (Mirb.) Oerst. At altitudes greater than 1000 m.a.s.l., these species coexist with Araucaria araucana (Molina) K. Koch, between 38-39°S (Hauenstein et al., 2011; De los Ríos-Escalante et al., 2011). South of 39°S, Nothofagus species predominate, and south of 41°S, these Nothofagus forests coexist with Fitzroya cupressoides forest (Steinhart et al., 1999, 2002). Access to the lakes is difficult since they are in mountainous areas, accessible only by long mountain paths (De los Ríos et al., 2007; De los Ríos & Roa, 2010) . Bulgarian mountain lakes are also oligotrophic, and are associated with native Fagus L. forest. Their origin is volcanic below 2200 m.a.s.l., and glacial at higher altitudes, with a relatively high number of crustacean zooplankton species and low human intervention (Kalchev et al., 2004; Hristozova et al., 2004). The aim of the present study is to compare data obtained from the literature of chlorophyll-a concentration and crustacean zooplankton populations in North Patagonian mountain lakes and Bulgarian mountain lakes, considering the geographical and ecological differences between the two regions.
Data about the trophic status and zooplanktonic crustacean and littoral species from Chilean mountain lakes were obtained from the literature (n = 8; Steinhart et al., 2002; De los Ríos-Escalante et al., 2011) and from field-work in Alerce Andino National Park. The data from Bulgaria (n = 9) were taken from the literature (Kalchev et al., 2004; Hristozova et al., 2004).
Firstly a regression analysis between chlorophyll-a concentration and number the species of was applied using the xlstat 5.0 software (www.adinsoft.com) in order to determine the potential relationship between the two variables. Next, a species absence/presence matrix was constructed, with the species in rows and sites in columns. When this matrix was complete, the Bray-Curtis Index with single link for similarity was obtained to determine potential similarities between sites, on the basis of species associations (Gotelli & Graves, 1986); this analysis used the Biodiversity Pro.
Version 2.0 software (McAleece et al., 1997). The next step was to calculate a Checkerboard score ("C-score"), a quantitative index of occurrence that measures the extent to which species co-occur less frequently than expected by chance (Gotelli, 2000). A community is structured by competition when the C-score is significantly larger than expected by chance (Gotelli, 2000). Finally, co-occurrence patterns were compared with null expectations by simulation.
Gotelli & Entsminger (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 original community (fixed column), and each species occurs with the same frequency as in the original community (fixed row). (2) Fixed-Equiprobable: in this algorithm only the row sums are fixed, while the columns are treated as equiprobable. This null model considers all the samples (column) as equally available for all species. (3) Fixed-Proportional: in this algorithm the species occurrence totals are maintained as in the original community, and the probability that a species will occur at a site (column) is proportional to the column total for that sample. The null model analyses were performed using the software Ecosim version 7.0 (Gotelli & Entsminger, 2007).
The results revealed a significant correlation between chlorophyll-a concentration and species number for Chilean lakes (Fig. 1); however this significant relationship did not exist for their Bulgarian counterparts (Fig. 1). The cluster analysis for Chilean lakes revealed the existence of two sites with approximately 80% similarity, Icalma and Galletué lakes, whereas the similarities between the remaining sites was approximately 40-60% (Fig. 2). Of the Bulgarian lakes, Alekovo with Gorno Marichino, and Salkata, Babreka and Okoto, formed two different groups with approximately 75% similarity, whereas for the remaining sites the similarities varied between 50-75% (Fig. 2). In the Chilean lakes there are very few species, and many of these are repeated in practically all of the sites studied (Table 1). The Bulgarian lakes contain many species in comparison with their Chilean counterparts, nevertheless there are also many repeated species (Table 1). This would be the reason why the results of null models revealed the absence of regulatory factors in all simulations for Chilean and Bulgarian lakes (Table 2).
Figure 1. Regression analysis between chlorophyll-a concentration and number of species for lakes of a) northern Patagonia Chilean, and b) Bulgarian.
Figura 1. Análisis de regresión entre concentración de clorofila-a y número de especies para lagos de a) norte de la Patagonia chilena, y b) Bulgaria.
Figure 2. Dendrogram with the results of Bray-Curtis Similarity index for northern Patagonian Chilean mountain lakes (up) and Bulgarian mountain lakes (low).
Figura 2. Dendrograma con los resultados del análisis del índice de similitud de Bray-Curtis para lagos del norte de la Patagonia chilena (arriba) y lagos de Bulgaria (abajo).
The literature on Chilean North Patagonian lakes and ponds revealed the marked role of oligotrophy in species richness and calanoid dominance (De los Ríos-Escalante, 2010; De los Ríos-Escalante et al., 2011). Nevertheless, the null model showed absence of regulatory factors (De los Ríos & Roa, 2010). The literature on Chilean lakes revealed that the main causes of changes in the trophic status are changes in the surrounding basin, when native forest is replaced by agricultural use, towns and industries (Soto, 2002). Under these conditions, changes in the chemical properties of the soil will lead to a decrease in nutrient composition and an increase in zooplankton biomass, with the consequent generation of clear water phase (Hristozova et al., 2004; Kalchev et al., 2004). Similar results to those found in Chilean lakes were described for Argentinean Patagonian lakes which are oligotrophic and contain a low species number (Modenutti et al., 1998); and for New Zealand lakes, where an increase in the number species of may be found directly associated with the increase in chlorophyll-a concentration (Jeppensen et al., 2000).
Another difference between Chilean and Bulgarian mountain lakes is the fact that many Bulgarian lakes containing introduced salmonids (Salvelinus fontinalis and Salmo trutta), with consequent effects on their zooplankton composition (Kalchev et al., 2004). Such effects would not be found in Chilean lakes containing no salmonids (De los Ríos-Escalante, 2010). The literature describes the effects caused by introduced salmonids on zooplankton composition, specifically the presence of small-sized species, and this effect is indeed observed in Argentinean Patagonian lakes (Reissig et al., 2006), which would probably present similarities to Bulgarian mountain lakes (Kalchev et al., 2004). However no studies exist about the effects of salmonids on zooplankton in Chilean lakes (De los Ríos-Escalante, 2010). This last topic (the presence of fishes, specifically salmonids) would be the main difference between the regulatory mechanisms affecting zooplankton communities in the mountain lakes of Bulgaria on one hand, and Chilean Patagonia on the other. According to descriptions of Patagonian lakes in Argentina and Chile, in the presence of fish, zooplankton assemblages are characterized by small-sized species and low number species of (Soto et al., 1994; Modenutti et al., 1998; Reissig et al., 2006). The results obtained would indicate that more ecological studies are necessary, specifically about trophism in pelagic lake environments.
The present study was founded by projects DGIP-UCT 01-2009 and MECESUP Project UCT 0804, also the authors express the gratitude to the staff of National Forestal Corporation (CONAF-Chile).
De los Ríos, P., E. Hauenstein, P. Acevedo & X. Jaque. 2007. Littoral crustaceans in mountain lakes of Huerquehue National Park (38°S, Araucania region, Chile). Crustaceana, 80: 401-410. [ Links ]
De los Ríos, P. & G. Roa. 2010. Crustacean species assemblages in mountain shallow ponds: Parque Cañi (38°S, Chile). Zoologia, Curitiba, 27: 81-86. [ Links ]
De los Ríos-Escalante, P. 2010. Crustacean zooplankton communities in Chilean inland waters. Crustaceana Monographs, 12: 1-109. [ Links ]
De los Ríos-Escalante, P., E. Hauenstein & M. Romero-Mieres. 2011. Microcrustacean assemblages composition and environmental variables in lakes and ponds of the Andean region-South of Chile (37-39°S). Braz. J. Biol., 71: 353-358. [ Links ]
Gotelli, N.J. & G.R. Graves. 1986. Null models in ecology. Smithsonian Institution Press, Washington, 368 pp. [ Links ]
Gotelli, N.J. 2000. Null models of species co-occurrence patterns. Ecology, 81: 2606-2621. [ Links ]
Gotelli, N.J. & G.L. Entsminger. 2007. Ecosim: Null models software for ecology. Version 7. Acquired Intelligence Inc. and Kesey-Bear. Jericho, VT 0465. Available from http://garyentsminger.com/ecosim/index.htm Reviewed: 15 October 2011. [ Links ]
Hauenstein, E., K. Barriga & P. De los Ríos-Escalante. 2011. Macrophytes assemblages in mountain lakes of Huerquehue National Park (39°S, Araucanía Region, Chile). Lat. Am. J. Aquat. Res., 39: 593-599. [ Links ]
Hristozova, M., I. Botev, R. Kalchev & W. Naidenow. 2004. Composition and temporal changes of zooplankton in high mountains lakes in the Rila mountains (South-West Bulgaria). Acta Zool. Bulgarica, 56: 341-356. [ Links ]
Jeppensen, E., T.L. Lauridsen, S.F. Mitchell, K. Christofferssen & C.W. Burns. 2000. Trophic structure in the pelagial of 25 shallow New Zealand lakes: changes along nutrient and fish gradients. J. Plankton Res., 22: 951-968. [ Links ]
Kalchev, R., I. Botev, M. Hristozova, W. Naidenow, G. Raikova-Petrova, G. Stoyneva, D. Temmnisjova-Topalova & T. Trichkova. 2004. Ecological relations and temporal changes in the pelagial of the high mountain lakes in the Rila mountains (Bulgaria). J. Limnol., 63: 90-100. [ Links ]
McAleece, N., J. Lambshead, G. Patterson & J. Gage. 1997. Biodiversity Pro: free statistical software for ecology. The Natural History Museum and Scottish Association for Marine Science, U.K. [ Links ]
Modenutti, B.E., E.G. Balseiro, C.P. Queimaliños, D.A. Suarez, M.C. Diéguez & R.J. Albariño. 1998. Structure and dynamics of food webs in Andean lakes. Lak. Reserv., Res. Manage., 3: 179-186. [ Links ]
Reissig, M., C. Trochine, C. Queimaliños, E. Balseiro & B. Modenutti. 2006. The role of fish introduction on planktonic food webs in lakes of the Patagonian Plateau. Biol. Cons., 132: 437-447. [ Links ]
Soto, D. 2002. Oligotrophic patters in southern Chilean lakes: the relevante of nutrients and mixing depth. Rev. Chil. Hist. Nat., 75: 377-393. [ Links ]
Soto, D., H. Campos, W. Steffen, O. Parra & L. Zúñiga. 1994. The Torres del Paine lake district (Chilean Patagonia): A case of poentially N-limited lakes and ponds. Arch. Hydrobiol., 99: 181-197. [ Links ]
Steinhart, G.S., G.E. Likens & D. Soto. 1999. Nutrient limitation in Lago Chaiquenes (Parque Nacional Alerce Andino, Chile): evidence from nutrient enrichment experiments and physiological assays. Rev. Chil. Hist. Nat., 72: 559-568. [ Links ]
Steinhart, G.S., G.E. Likens & D. Soto. 2002. Physiological indicators of nutrient deficiency in phytoplankton in southern Chilean lakes. Hydrobiologia, 489: 21-27. [ Links ]
Received: 1 November 2011; Accepted: 16 June 2012
Corresponding author: Patricio R. De los Ríos-Escalante (firstname.lastname@example.org)