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Latin american journal of aquatic research

On-line version ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.38 no.3 Valparaíso  2010


Lat. Am. J. Aquat. Res., 38(3): 507-513, 2010
DOI: 10.3856/vol38-issue3-fülltext-15



An update of the distribution of Boeckella gracilis (Daday, 1902) (Crustacea, Copepoda) in the Araucania region (38°S), Chile, and a null model for understanding its species associations in its habitat

Actualización de la distribución de Boeckella gracilis (Daday, 1902) (Crustacea, Copepoda) en la región de la Araucanía (38°S), Chile, y un modelo nulo para comprender sus asociaciones específicas en su habitat


Patricio De los Ríos-Escalante1, Eriko Carreño2, Enrique Hauenstein1 & Marcela Vega1

1 Escuela de Ciencias Ambientales, Facultad de Recursos Naturales, Universidad Católica de Temuco, Chile
Escuela de Acuicultura, Facultad de Recursos Naturales, Universidad Católica de Temuco, Chile

Dirección para Correspondencia

ABSTRACT. The crustacean zooplankton of Chilean inland waters are characterized by abundant calanoid copepods, mainly from the gemís Boeckella. The present study aims to update the distribution of Boeckella gracilis in the inland waters of the Araucania region (38-39°S) and to use null model analysis to understand the B. gracilis species associations. In the literature for Chile, this species is reported to be found in one northern lake and in three lakes of northern Patagonia. These fmdings are complemented by reports of this species for coastal and mountain ponds and mountain lakes of the Araucania region. These results agree with descriptions of this species for South American inland waters. The results of the null model analysis reveal factors regulating the species associations, whether comparing all the inhabitats or the guild structure, although some simulations show the opposite situation due to the presence of repeated species at many sites.

Keywords: Boeckella, zooplankton, null model, Patagonia, Chile.

RESUMEN. Los crustáceos zooplanctónicos en aguas continentales chilenas están caracterizados por la abundancia de copépodos calanoideos, principalmente del género Boeckella. El objetivo del presente trabajo es actualizar la distribución de esta especie en aguas continentales de la región de la Araucania (38-39°S), y el uso de modelos nulos para comprender sus especies asociadas. Las descripciones de la literatura indican que en Chile esta especie está en un lago del norte, y tres lagos en el norte de la Patagonia. Estos resultados están complementados con reportes de esta especie en pozas costeras, pozas y lagos de montaña en la región de la Araucania. Estos resultados concuerdan con las descripciones de esta especie para aguas continentales Sudamericanas. Los resultados del análisis de modelos nulos revelan que las asociaciones de especies tuvieron factores reguladores, ya sea comparando todos los habitantes y como estructura de gremios, aunque en algunas simulaciones se observó una situación opuesta, esto se debió a la presencia de especies repetidas en muchos sitios.

Palabras clave: Boeckella, zooplancton, modelos nulos, Patagonia, Chile.

Calanoid copepods are dominant in the zooplankton assemblages of Chilean inland waters due mainly to the oligotrophy of their habitats (Soto & Zúñiga, 1991; De los Ríos & Soto, 2006) but also to their high conductivity (Soto & De los Ríos, 2006). The calanoid copepods are represented by the genera Boeckella, Parabroteas, and Tumeodiaptomus (Soto & Zúñiga, 1991). Boeckella is the most widespread, with 11 species living throughout continental Chile (Bayly, 1992; Menu-Marque et al, 2000). One of the species reported for Chilean inland waters is B. gracilis (Daday, 1902). Widespread in South American inland waters, this species is found mainly in tropical zones and from the eastern Andes Mountains to the Argentinean Patagonia (43°S; Menu-Marque et al, 2000; Trochine et al, 2008). For Chilean inland waters, B. gracilis was reported at five sites: one in northern Chile (18°S) and the other four in northern Patagonia (38-41°S). Unfortunately, there are no more reports of this species in Chilean inland waters. Nevertheless, unpublished data offer preliminary descriptions of the presence of this species in mountain lakes at 38-39°S. Although no additional reports of this species have been made (Villalobos, 2006), its presence in northern Patagonian inland waters has been proposed. The present study aims to update the distribution of B. gracilis and its associated species and to interpret its species associations using null model analysis.

The present review of the geographical distribution of B. gracilis includes the literatee describing B. gracilis for Chilean inland waters (Brehm, 1937; Loefler, 1961; Zúñiga & Domínguez, 1978; Andrew et al, 1989) as well as recent findings (De los Ríos et al, 2007; De los Ríos & Roa, 2010) and field studies of the inland waters of the Araucania region, southern Chile (38°S). These studies were done between September 2008 and September 2009 in two settings. The first, Marimenuco, is a mountain plain that has the following macrophyte species: Isoetes savatieri, Anagallis alternifolia, Áster vahlii, Gratiola peruviana, Carex decidua, C. madoviana, Juncus imbricatus, and J. procerus; and the second, Puaucho, is a coastal dune área with macrophyte species found in salt marshes: Selliera radicans, Distichlis spicata, Juncus articus, Scirpus americanus, S. olneyi, and Rumex cuneifolius. The specimens were collected and fixed with absolute ethanol, then identified with specialized literatee (Araya & Zúñiga, 1985; Reid, 1985; Bayly, 1992; González, 2003).

An absence-presence matrix was used for the species association analysis implemented to test the hypothesis that the reported species are not randomly associated. For this, we used the "C score" index (Stone & Roberts, 1990), which determines co-occurrence based on presence/absence (1/2) matrices for given zooplankton species in the sample. Following Gotelli (2000) and Tiho & Johens (2007), the presence/absence matrix was analysed as follows. (a) Fixed-fixed: In this algorithm, the row and the column sums of the original 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). This algorithm is not prone to type-I errors (falsely rejecting the nuil hypothesis) and has good power for detecting non-randomness (Gotelli, 2000, 2001; Tiho & Johens, 2006). (b) Fixed-equiprobable: In this simulation, the row sums are fixed, but the columns are treated as equiprobable. This null model treats all the samples (columns) as equally suitable for all species (Tiho & Johens, 2006; Gotelli, 2000). (c) Fixed-proportional: In this algorithm, the totals for species occurrence are maintained as in the original community, and the probability that a species will occur in a sample (= column) is proportional to the column total for that sample (Gotelli, 2000; Tiho & Johens, 2006; Tondoh, 2007). Ecosim software was used for all these analyses (Gotelli & Entsminger, 2009).

Our review of the geographical distribution showed that, prior to the recent field studies, B. gracilis had been reported in the literatee at the following sites: Chungara Lake (18°15'S, 69°10'W) (Andrew et al, 1989); Riñihue Lake (39°50'S, 72°19'W) (Zúñiga & Domínguez, 1978); Calbuco Lagoon (41°16'S, 72°32'W) (Lóffler, 1961); and Mausa (41°27'S, 72°58'W) (Brehm, 1937). More recent literatee and findings have revealed the presence of this species in Cañi Park at the ponds Del Risco, Negrita, Escondida, De los Patos, Negra, and Vaca Hundida (39°15'S, 79°42'W) as well as Los Pastos and Seca (39°15'S, 79°43'W) (De los Ríos & Roa, 2010). In Huerquehue National Park, B. gracilis was also found in Verde I Lake (39°10'S, 71°43'W), Los Patos Pond (39°10'S, 71°42'W) (De los Ríos et al, 2007), and Tinquilco Lake (39°10'S, 71°43'W) (De los Ríos et al, 2007). In Conguillío National Park, this species was observed in Verde II Lagoon (38°40'S, 71°37'W) (De los Ríos et al, present study; collected in March 2007). Moreover, specimens have been reported from shallow pools in the coastal dunes of Puaucho Beach (38°57'S, 73°19'-73°20'W) (De los Ríos, et al, present study, collected in September 2009) and the ponds of the Marimenuco mountain plain (38°40'S, 71°05'W) (De los Ríos et al, present study, collected in September 2008).

These results revealed the existence of B. gracilis in small mountain lakes (e.g., Captren, Tinquilco, and Verde II), where it can coexist with cladocerans such as Ceriodaphnia dubia and Neobosmina chilensis (Table 1). B. gracilis can also inhabit permanent shallow mountain ponds (e.g., Cañi Park), coexisting with species such as Daphnia pulex, C. dubia, Diaphanosoma díñense, Chydorus sphaericus, Mesocyclops longisetus, and Hyalella araucana (Table 1). Ephemeral shallow mountain ponds (e.g., Los Patos and Marimenuco) constitute a third type of habitat in which B. gracilis coexists with Mesocyclops longisetus, Simocephalus serrulatus, Scapholeberis exspinifera, and Hyalella araucana (Table 1) in the first case and with ostracods in the second (Table 1). Finally, the fourth group, ephemeral shallow pools in a sandy dune área (Puaucho Beach), was practically exceptional, with B. gracilis coexisting with C. dubia and Chydoridae (Table 1). The results of the null model analysis for co-occurrence revealed the existence of regulatory factors in two of the three simulations (Table 2). The lack of regulatory factors in the third simulation (fixed-equiprobable) was due to the high incidence of repeated species at many of the studied sites (Table 1).

The present study contributes knowledge about the distribution of this species in continental Chilean territory. Although findings of juvenile copepods that probably belong to B. gracilis indicate that this species may be distributed in other mountain lakes and ponds of northern and central Patagonia, it was not possible to confirm the presence of this species in, for example, the lakes of Puyehue and Alerce Andino National Parks (De los Ríos, unpublished data). Given this and the numerous mountain lakes of northern and central Patagonia (Steinhart et al, 2002), it is likely that B. gracilis inhabits a wide gradient of mountain lakes between 38° and 42°S, similar to descriptions for Argentinean inland waters (Menu-Marque et al, 2000). One exception was the presence of this species in the shallow ephemeral pools of the Puaucho Beach dimes, although early reports from around Calbuco (Lóffler, 1961) and Puerto Montt (Brehm, 1937) indicate that this species may be found in coastal lagoons. The present study helps us understand this species' distribution in Chilean inland waters, but more studies are needed to understand the ecological processes of these habitats.

The null model analysis revealed that the species associations of B. gracilis are not random. Rather, regulatory factors exist that explain these associations. Both random and regulatory factors occur in species associations when using fixed-proportional simulation due to the recurrence of a few species at many of the study sites, coinciding with similar results for central and southern Patagonian inland waters (De los Ríos, 2008; De los Ríos et al, 2008a, 2008b; De los Ríos & Soto, 2009). These results agree with theoretical ecological studies based on observations made in terrestrial ecosystems (Ribas & Schoereder, 2002; Tondoh, 2006; Franca & Araujo, 2007; Sanders et al, 2007; Tiho & Johens, 2007). Nevertheless, in spite of the existence of regulatory factors (e.g., trophic status), it was possible to detect random species associations (De los Ríos & Roa, 2010). In this scenario of a potential role of trophic status, dominance by calanoids and a low number of species are associated with oligotrophic water bodies, corresponding to descriptions of many kinds of Patagonian lakes, such as those in Cañi park at 38°S (De los Ríos & Roa, 2010) and Torres del Paine National Park (De los Ríos & Soto, 2009).

The species assemblages for oligotrophic waters included calanoid copepods and small cladocerans, mainly Eubosmina hagmanni, whereas for mesotrophic waters, the calanoids decreased in abundance and coexisted with other cladocerans, mainly of the genera Daphnia, Ceriodaphnia, and Chydorus (De los Ríos & Soto, 2009). These results resemble the observations of the present study (Table 1). Similar results about oligotrophy and its association with a low number of species and elevated levéis of calanoid copepods have been reported for Argentinean Patagonian lakes (Modenutti et al., 1998) and New Zealand lakes and ponds (Jeppensen et al, 1997, 2000). Given this information, more ecological studies are necessary because the regulatory factors of the ephemeral pools probably include the combined effects of trophic status and conductivity, specifically in ephemeral coastal (e.g., Puaucho) and mountain (e.g,. Marimenuco) pools, whereas in mountain lakes (e.g., Tinquilco), the trophic status would likely fulfill this role.



The present study was financed by the projects DGI-UCT-2005-04-11 and DGI-CDA 2007-01. The authors also recognize the support of the Schools of Aquaculture and Environmental Sciences at the Catholic University of Temuco, Temuco, Chile.



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Received: 27 October 2009; Accepted: 23 August 2010

Corresponding author: Patricio De los Ríos (