Biologia 65/6: 1019—1027, 2010 Section Zoology DOI: 10.2478/s11756-010-0123-6

Species co-occurrences based on a presence/absence null model for Copepoda and cladocerans in Patagonia and Tierra del Fuego lakes and ponds

Patricio De los Ríos1, Andrés Mancilla2 & Marcela Vega1

1Laboratorio de Limnología y Recursos Hídricos, Escuela de Ciencias Ambientales, Facultad de Recursos Naturales, Uni- versidad Católica de Temuco, Casilla 15-D, Temuco, Chile; e-mail: [email protected] 2Instituto de la Patagonia, Universidad de Magallanes, Avenida Bulnes 01855,Casilla113-D,PuntaArenas,Chile

Abstract: The zooplankton assemblages in southern Chilean Patagonia are characterized by calanoid dominance and low species number that is observable under oligotrophic status and wide conductivity values, whereas at mesotrophic status the daphnids are dominant with high species number, and finally at hyper-saline environments halophilic species such as Artemia persimilis and/or the calanoid Boeckella poopensis predominate. In the present study data of different lakes and ponds between 45–53◦ S were analyzed, with the aim to determine potential structures at different sites. For this purpose a null model based in guild structure was applied, considering each guild a different kind of water body (lake, small lake, permanent pond, ephemeral pond, and saline lake). The results revealed in two simulations that guild are structured. These results are similar with other descriptions on the basis of null models that revealed a random pattern of species associations for similar ecosystems due to many species repeated in all or practically all studied sites or similarities of ecological features. Ecological and biogeographical topics were discussed. Key words: Calanoid; Daphnia; Artemia; lakes; ponds; null model

Introduction Rodríguez-Fernández et al. 2006; Segurado & Figueredo 2007). These null models are more robust in comparison The zooplankton assemblages in lakes and ponds in cen- with deterministic models (Gotelli 2000, 2001). tral and southern Patagonia (44–53◦ S) have different The aim of the present study is to apply a null patterns (Soto 1990) due the heterogeneity of water model analysis based on presence-absence of species bodies. For example, in large lakes, small lakes and shal- matrix to determine the absence regulator factors for low ponds of Torres del Paine zooplankton species asso- explanation of species associations in zooplankton in ciations are regulated by conductivity and the trophic central and southern Patagonian lakes and ponds. The status (Soto & De los Ríos 2006; De los Ríos et al. aim of this procedure is the use of non-randomness test 2008a; De los Ríos & Soto 2009). This pattern is sim- to understand community ecology in inland water zoo- ilar descriptions for lakes and ponds in Argentinean plankton. Patagonia (Modenutti et al. 1998) and with descrip- tions of New Zealand lakes and ponds (Jeppensen et al. 1997, 2000). The patterns observed for zooplank- Material and methods ton assemblages in southern Chilean lakes are differ- Study area ent to Europe and North America that have high num- The studied region is located between 45–53◦ S(Aysenand ber of species which are directly associated with surface Magallanes region, Chile), and it is characterized by the (Dodson 1992), and with marked dominance of daphnid presence of large diversity of landscapes, glaciers, valleys, cladocerans (Gillooly & Dodson 2000). snowcaps, lakes and ponds (Niemeyer & Cereceda 1984). From this point of view zooplankton assemblages Within the water bodies there are numerous large and deep are not random, regulatory or deterministic factors ex- lakes, small lakes, shallow permanent and ephemeral ponds, ists to explain the community structure. The absence and saline lakes (De los Ríos 2008). The climate is charac- terized by precipitations in the north from 51◦ S, whereas in of regulatory factors and the random distribution in ◦ the south of 51 S (Niemeyer & Cereceda 1984), the climate species co-occurrence are the basis of null models, one is subpolar with less than 700 mm of precipitation a year, of these models used the presence and absence of species and between October and December there is exposition to to determine the absence of deterministic factors as strong winds of approximately 100 km h−1 (Campos et al. regulators of species co-occurrence or guild structure 1994a, b; De los Ríos & Soto 2009). The studied region has (Frutos 1998; Gotelli 2000, 2001; Abelha et al. 2006; difficult access due its marked isolation, that is an advan-

c 2010 Institute of Zoology, Slovak Academy of Sciences 1020 P. De los Ríos et al. tage because these ecosystems are practically pristine, but column sums of the matrix are preserved. Thus, each ran- the disadvantage is that it is difficult to carry out system- dom community contains the same number of species as the atic field works due to geographical and climatic features original community (fixed column) and each species occurs (Campos et al. 1994a, b; De los Ríos 2008; De los Ríos & with the same frequency as in the original community (fixed Soto 2009). row). (2) Fixed-Equiprobable. In this algorithm only the row sums are fixed and the columns are treated as equiprobable. Data collection This null model considers all the sites (columns) as equally Literature revision. Meta-analysis was applied and the in- available for all species, which occur in the same proportions formation was obtained from literature, according to de- as in the original communities. (3) Fixed-Proportional. This scriptions of Luiselli et al. (2007) and Luiselli (2008a, b) model keeps the species occurrence totals the same as in the nevertheless, in the present study data of species pres- original community and the probability that a species oc- ence/absence for Chilean Patagonian lakes and ponds were curs at a site (column) is proportional to the column total considered; many of these sites are located in a zone difficult for that sample. for access and with a weather characterized by strong wind The variance ratio is the ratio of the variance of the storms (Soto et al. 1994). The information for species asso- column sum to the sum of the row variances. Unlike C- ciations in central and southern Patagonian lakes and ponds score index, the variance ratio does not measure patterns was obtained from literature (Villalobos 1999; De los Ríos of co-occurrence within the matrix, but it is determined ex- & Contreras, 2005; De los Ríos 2005; Soto & De los Ríos clusively by row and column sums of the matrix (Gotelli 2006; De los Ríos & Soto 2007; De los Ríos et al. 2008a, b; 2000). Therefore, this model is not valid for the fixed-fixed Rogers et al. 2008). null model. For this reason, the variance ratio was not tested Field works. Information obtained during field works in Oc- with this null model. The variance ratio measures the vari- tober 2001, October 2006, April 2007, January 2008, and ability in the number of species by sample. If species richness May 2009 was included. The zooplankton was collected us- is regulated by biological interactions, communities should ing horizontal hauls in shallow ponds, whereas in small converge on a relatively constant number of species per sam- lakes, and large and deep lakes, the zooplankton was col- ple (Gotelli 2000). In a competitively structured community, lected by vertical hauls from a boat, for both procedures, by the observed variance ratio should be significantly smaller µ using an Apstein net of 20 cm diameter and 100 mmesh than that expected by chance (Tiho & Johens 2007). A null size, according to the descriptions of Soto & De los Ríos model analysis was carried out using the Ecosim version 7.0 (2006) and De los Ríos & Soto (2009). Zooplankton spec- software (Tondoh 2006; Tiho & Johens 2007; De los Ríos imens were fixed with absolute ethanol, and identified us- 2008; De los Ríos et al. 2008b; Gotelli & Entsminger 2009). ing specialized literature (Araya & Zú˜niga 1985; Reid 1985; Bayly 1992a, b; Paggi 1999; De los Ríos & Zú˜niga 2000; Brték & Mura 2000; Rogers et al. 2008). This literature Results and discussion was also used to explain or confirm the taxonomic status of species found in the literature revision. The information obtained from literature and field observations was applied The results denoted low species richness in large for each site and the species / genera ratio was determined lakes and saline lakes, whereas in small lakes, shal- (Gotelli 2000, 2001). low permanent and temporal ponds a high number of species was reported (Table 1). For large and deep Data analysis lakes and small lakes, the most representative species The data obtained from literature and field works were or- were Boeckella gracilipes (Daday, 1902), B. michaelseni dered using an absence/presence matrix. A Checkerboard (Mrázek, 1901), Daphnia pulex (Scourfield, 1877), and score (“C-score”) is based on the number of checkerboard Ceriodaphnia dubia (Richard, 1894), that agree with units that can be found for each species pair. The number of ◦ checkerboard units (CU) for any species can be calculated similar results for Patagonian lakes (38–51 S; Soto & as: Zú˜niga 1991; Menu-Marque et al. 2000; De los Ríos 2008; Table 2). Whereas for shallow temporal and per- CU =(Ri − S)(Rj − S)(1)manent ponds the most representative species were B. gracilipes, B. michaelseni, B. poppei (Mrázek, 1901), where Ri and Rj are the row totals for species and i and Parabroteas sarsi (Mrázek, 1901) and Daphnia da- species j, respectively, and S is the number of sites occu- dayana (Paggi, 1999) (Table 2) that are similar to de- pied by both species. The C-score measures the degree to scriptions for sub-Antarctic counterparts (Hannson et which species pairs segregates across a set of samples, but it does not require complete segregation. The larger C-score al. 1996; Menu-Marque et al. 2000; Dartnall 2005; Pugh the less the average pairwise species-co-occurrence. For an et al. 2002). In few shallow temporal ponds the presence assemblage that is competitively structured C-score should of species of the genus was detected (Ta- be significantly higher than that expected by chance (Gotelli ble 2), although these species can be found only at low 2000; Tiho & Johens, 2007). salinity and oligotrophy (De los Ríos et al. 2008a). Fi- The C-score is a quantitative index of occurrence and nally, also the presence of the brine shrimp Artemia per- a measure of the extent to which species co-occur less fre- similis (Piccinelli et Prosdocimi, 1968), was reported in quently than expected by chance alone (Gotelli 2000, 2001). two saline lakes, in Amarga lagoon, where it was exclu- Gotelli & Entsminger (2009), Tiho & Johens (2007) and sive component, and De los Cisnes lagoon where it coex- Tondoh (2006) suggested that the following robust statisti- cal models should be used in a co-occurrence analysis. First, isted with B. poopensis and unidentified harpacticoids, the matrix layout needs to include the species names in rows whereas in the third saline lake only B. poopensis was and the sites in the columns. Second, the following models reported (Table 2). This is a different situation in com- should be used: (1) Fixed-Fixed. In this model, the row and parison to saline lakes of Altiplano where B. poopoen- Copepods and cladocerans in Patagonia 1021

Table 1. Geographical location, surface, maximum depth, number of species and species – genera ratio for studied sites.

Kind of Number Site water body Geographical location Surface Depth of species S/G Reference

1 Los Palos Small lake 45◦19 S–72◦42 W 5 59 4 1.0 Villalobos (1999) 2 Foitzick Small lake 45◦38 S–72◦05 W 1 2 3 1.0 De los Ríos, field works 2001 3 Pólux Small lake 45◦40 S–71◦52 W 9 No data 4 1.0 De los Ríos, field works 2001 4Riesco Lake 45◦46 S–72◦20 W 147 130 4 1.0 Villalobos (1999) 5 Elizalde Lake 45◦47 S–72◦11 W 30 130 4 1.0 De los Ríos & Soto (2007) 6 Escondida Small lake 45◦49 S–7240 W 7 43 5 1.0 Villalobos (1999) 7 Balmaceda I Permanent pond 45◦53 S–71◦40 W 0.1 1 5 1.3 De los Ríos, field works 2001 8 Balmaceda II Ephemeral pond 45◦53 S–71◦40 W 0.1 1 8 1.6 De los Ríos, field works 2001 9 Balmaceda II Ephemeral pond 45◦53 S–71◦40 W 0.1 1 8 1.6 De los Ríos, field works 2001 10 General Carrera Lake 46◦18 S–71◦ 56 W 1892 410 4 1.0 De los Ríos, field works 2001 11 Amarga Permanent pond 50◦29 S–72◦45 W 6 3 1 1.0 Campos et al. (1996) 12 Pool at Paine River Ephemeral pond 50◦29 S–72◦46 W 0.1 2 2 1.0 De los Ríos, field works 2008 13 Isidoro Permanent pond 50◦57 S–72◦53 W 0.1 2 6 1.2 De los Ríos (2005) 14 Juncos Permanent pond 51◦01 S–72◦52 W 0.1 3 6 1.2 Soto & De los Ríos (2006) 15 Jovito Permanent pond 51◦01 S–72◦54 W 0.1 3 6 1.2 Soto & De los Ríos (2006) 16 Paso Permanent pond 51◦01 S–72◦55 W 0.1 3 7 1.4 Soto & De los Ríos (2006) 17 Redonda Permanent pond 51◦01 S–72◦52 W 0.1 3 8 1.3 Soto & De los Ríos (2006) 18 Larga Permanent pond 51◦01 S–72◦52 W 0.1 5 6 1.0 Soto & De los Ríos (2006) 19 Cisnes Permanent pond 51◦01 S–72◦52 W 0.1 1 7 1.4 Soto & De los Ríos (2006) 20 Don Alvaro Permanent pond 51◦01 S–72◦52 W 0.1 2 7 1.4 De los Ríos (2005) 21 Guanaco Permanent pond 51◦01 S–72◦50 W 0.1 2 7 1.4 De los Ríos (2005) 22 Melliza Este Small lake 51◦03 S–72◦57 W 0.1 16 9 1.8 Soto & De los Ríos (2006) 23 Melliza Oeste Small lake 51◦03 S–72◦57 W 0.1 25 9 1.8 Soto & De los Ríos (2006) 24 Sarmiento Lake 51◦03 S–72◦37 W 86 114 4 1.3 Soto & De los Ríos (2006) 25 Nordenskjold Lake 51◦07 S–72◦56 W 25 104 4 1.3 Soto & De los Ríos (2006) 26 Pehoe Lake 51◦07 S–72◦56 W 15 200 4 1.3 Soto & De los Ríos (2006) 27 Monserrat Permanent pond 51◦07 S–72◦47 W 0.1 2 7 1.8 De los Ríos (2005) 28 Vega del Toro Ephemeral pond 51◦07 S–71◦40 W 0.1 1 8 1.3 De los Ríos (2005) 29 Del Toro Lake 51◦12 S–72◦38 W 196 154 5 1.3 Soto & De los Ríos (2006) 30 Sofia Small lake 51◦30 S–72◦40 W94041.0Ca˜nete (1999) 31 Puerto Natales 1 Permanent pond 51◦42 S–72◦25 W 0.1 1 2 1.0 De los Ríos, field works 2008 32 Puerto Natales 2 Permanent pond 51◦42 S–72◦25 W 0.1 1 4 1.0 De los Ríos, field works 2008 33 Puerto Natales 3 Permanent pond 51◦42 S–72◦25 W 0.1 1 3 1.0 De los Ríos, field works 2008 34 Buenas Tardes Permanent pond 51◦42 S–72◦27 W 0.1 1 2 1.0 De los Ríos, field works 2008 35 Los Palos 2 Permanent pond 52◦43 S–71◦02 W 0.1 1 3 1.0 De los Ríos, field works 2008 36 Pool at Los Palos 2 Ephemeral pond 52◦43 S–71◦02 W 0.1 1 3 1.0 De los Ríos, field works 2008 37 Pali Aike 1 Ephemeral pond 52◦13 S–69◦44 W 0.1 1 4 1.3 De los Ríos, field works 2008 38 Pali Aike 2 Ephemeral pond 52◦13 S–69◦44 W 0.1 1 3 1.0 De los Ríos, field works 2008 39 Ana Saline lake 52◦04 S–69◦47 W 0.1 1 1 1.0 De los Ríos, field works 2008 40 Kon Aikén Ephemeral pond 52◦50 S–71◦10 W 0.1 1 7 1.2 De los Ríos (2005) 41 Kon Aikén 1 Ephemeral pond 52◦51 S–70◦55 W 0.1 1 4 1.0 De los Ríos et al. (2008b, c) 42 Kon Aikén 2 Ephemeral pond 52◦51 S–70◦55 W 0.1 1 4 1.0 De los Ríos et al. (2008b, c) 43 Kon Aikén 3 Ephemeral pond 52◦51 S–70◦55 W 0.1 1 4 1.0 De los Ríos et al. (2008b, c) 44 Kon Aikén 4 Ephemeral pond 52◦51 S–70◦55 W 0.1 1 4 1.0 De los Ríos et al. (2008b, c) 45 Kon Aikén 5 Ephemeral pond 52◦51 S–70◦55 W 0.1 1 4 1.0 De los Ríos et al. (2008b, c) 46 Kon Aikén 6 Ephemeral pond 52◦51 S–70◦55 W 0.1 1 4 1.0 De los Ríos et al. (2008b, c) 47 Pool at Cabeza de Mar Ephemeral pond 52◦46 S–71◦02 W 0.1 1 3 1,0 De los Ríos, field works 2008 48 Tres Puentes 1 Permanent pond 53◦06 S–70◦52 W 0.1 1 3 1.0 Field works 2009 49 Tres Puentes 2 Permanent pond 53◦07 S–70◦53 W 0.1 1 5 1.3 Field works 2009 50 Tres Puentes 3 Permanent pond 53◦07 S–70◦53 W 0.1 1 4 1.3 Field works 2009 51 Tres Puentes 5 Permanent pond 53◦07 S–70◦52 W 0.1 1 3 1.0 Field works 2009 52 Tres Puentes 6 Permanent pond 53◦07 S–70◦53 W 0.1 1 3 1.0 Field works 2009 53 Laredo 1 Permanent pond 52◦57 S–70◦49 W 0.1 1 3 1.0 De los Ríos et al. (2008b, c) 54 Laredo 2 Permanent pond 52◦57 S–70◦49 W 0.1 1 3 1.0 De los Ríos et al. (2008b, c) 55 Rio Chico Permanent pond 53◦06 S–70◦53 W 0.1 1 3 1.0 De los Ríos et al. (2008b, c) 56 Tierra del Fuego 1 Ephemeral pond 52◦32 S–69◦19 W 0.1 1 4 1.0 Field works, 2009 57 Tierra del Fuego 2 Ephemeral pond 53◦13 S–68◦46 W 0.1 1 2 1.0 Field works, 2009 58 Tierra del Fuego 3 Ephemeral pond 53◦12 S–68◦46 W 0.1 1 2 1.0 Field works, 2009 59 Tierra del Fuego 4 Ephemeral pond 53◦09 S–68◦45 W 0.1 1 2 1.0 Field works, 2009 60 Tierra del Fuego 5 Ephemeral pond 53◦09 S–68◦45 W 0.1 1 2 1.0 Field works, 2009 61 Tierra del Fuego 6 Ephemeral pond 53◦09 S–68◦45 W 0.1 1 6 1.0 Field works, 2009 62 Tierra del Fuego 8 Ephemeral pond 53◦09 S–68◦45 W 0.1 1 2 1.0 Field works, 2009 63 Tierra del Fuego 9 Ephemeral pond 52◦30 S–69◦23 W 0.1 1 3 1.0 Field works, 2009 64 Tierra del Fuego 10 Ephemeral pond 52◦30 S–69◦23 W 0.1 1 2 1.0 Field works, 2009 65 De los Cisnes Permanent pond 53◦14 S–70◦00 W 6.0 2 3 1.0 De los Ríos, field works 2008 66 Porvenir Permanent pond 53◦17 S–70◦19 W 0.1 1 5 1.0 De los Ríos (2005) 67 Lillo Permanent pond 53◦21 S–70◦19 W 0.1 1 5 1.0 De los Ríos, field works 2008 68 Santa Maria Este Ephemeral pond 53◦22 S–70◦20 W 0.1 1 2 1.0 De los Ríos, field works 2008 69 Santa Maria Oeste Ephemeral pond 53◦22 S–70◦20 W 0.1 1 2 1.0 De los Ríos, field works 2008 70 Poll Permanent pond 53◦23 S–70◦19 W 0.1 1 2 1.0 De los Ríos, field works 2008 1022 P. De los Ríos et al.

Table 2. Species reported at the studied sites in the present paper. For site numbers see Table 1.

Sites12345678910

Boeckella brasiliensis (Lubbock, 1855) 0 0 0 0 0 0 0 0 0 0 Boeckella brevicaudata (Brady, 1875) 0 0 0 0 0 0 0 0 1 0 Boeckella gracilipes (Daday, 1902) 1 0 0 1 0 1 0 1 0 1 Boeckella meteoris (Kiefer, 1928) 0 0 0 0 0 0 0 0 0 0 Boeckella. michaelseni (Mrázek, 1901) 0 1 1 0 1 0 1 0 0 0 Boeckella poopoensis (Marsh, 1906) 0 0 0 0 0 0 0 0 0 0 Boeckella poppei (Mrázek, 1901) 0 0 0 0 0 0 0 1 1 1 Parabroteas sarsi (Mrázek, 1901) 1 0 0 1 0 0 0 1 1 1 Acantocyclops vernalis (Fisher, 1853) 0 0 0 0 0 0 0 0 0 0 Mesocyclops longisetus (Thiebaud, 1914) 0 0 0 0 0 1 0 0 0 0 Tropocylops prasinus (Fisher, 1960) 1 1 1 1 1 1 1 0 0 0 Microcyclops sp 0000000000 Juvenilecyclopoida 0000000111 Juvenile harpacticoida 0 0 0 0 0 0 0 0 0 0 Artemia persimilis (Piccinelli et Prosdocimi 1968) 0 0 0 0 0 0 0 0 0 0 Branchinecta gaini (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 Branchinecta granulosa (Daday, 1902). 0 0 0 0 0 0 0 0 0 0 Branchinecta vuriloche (Cohen, 1985) 0 0 0 0 0 0 0 1 1 1 Daphnia ambigua (Scourfield, 1967) 0 0 0 0 0 0 0 0 0 1 Daphnia dadayana (Paggi, 1999) 0 0 0 0 0 0 0 1 0 1 Daphnia obtusa (Kurz, 1874) 0 0 0 0 0 0 0 0 0 0 Daphnia pulex (Scourfield, 1877) 0 0 0 0 0 0 0 1 0 0 Ceriodaphnia dubia (Richard, 1894) 0 0 0 0 0 1 0 0 0 0 Scapholeberis exispinifera (Nicolet, 1849) 0 0 0 0 0 0 0 0 0 0 Simosa vetula (O.F. M¨uller, 1776) 0 0 0 0 0 0 0 0 0 0 Neobosmina chilensis (Daday, 1902) 1 1 1 1 1 1 1 0 0 0 Chydurus sphaericus (O.F. M¨uller, 1785) 0 0 0 0 0 0 0 0 0 0

Sites11121314151617181920

Boeckella brasiliensis (Lubbock, 1855) 0 0 0 0 0 0 0 0 0 0 Boeckella brevicaudata (Brady, 1875) 0 0 0 0 0 0 0 0 0 0 Boeckella gracilipes (Daday, 1902) 0 0 0 0 0 1 1 0 0 1 Boeckella meteoris (Kiefer, 1928) 0 0 0 0 0 0 0 0 1 0 Boeckella. michaelseni (Mrázek, 1901) 0 0 1 1 1 0 0 0 0 0 Boeckella poopoensis (Marsh, 1906) 0 0 0 0 0 0 0 0 1 0 Boeckella poppei (Mrázek, 1901) 0 1 1 0 0 1 1 1 0 0 Parabroteas sarsi (Mrázek, 1901) 0 0 0 0 0 0 1 1 1 0 Acantocyclops vernalis (Fisher, 1853) 0 0 0 0 0 0 0 0 0 0 Mesocyclops longisetus (Thiebaud, 1914) 0 0 0 0 0 0 0 0 0 0 Tropocylops prasinus (Fisher, 1960) 0 0 0 0 0 0 0 0 0 0 Microcyclops sp 0000000000 Juvenilecyclopoida 0011111010 Juvenile harpacticoida 0 0 0 0 0 0 0 0 0 0 Artemia persimilis (Piccinelli et Prosdocimi 1968) 1 0 0 0 0 0 0 0 0 0 Branchinecta gaini (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 Branchinecta granulosa (Daday, 1902). 0 0 0 0 0 0 0 0 0 0 Branchinecta vuriloche (Cohen, 1985) 0 0 0 0 0 0 0 0 0 0 Daphnia ambigua (Scourfield, 1967) 0 0 0 0 0 0 0 0 0 0 Daphnia dadayana (Paggi, 1999) 0 0 1 0 0 0 0 0 1 0 Daphnia obtusa (Kurz, 1874) 0 1 0 1 1 1 1 1 0 1 Daphnia pulex (Scourfield, 1877) 0 0 0 1 1 1 1 0 0 1 Ceriodaphnia dubia (Richard, 1894) 0 0 0 0 0 0 0 0 0 0 Scapholeberis exispinifera (Nicolet, 1849) 0 0 0 0 0 0 0 0 0 0 Simosa vetula (O.F. M¨uller, 1776) 0 0 0 0 0 0 0 0 0 0 Neobosmina chilensis (Daday, 1902) 0 0 1 0 1 1 1 1 1 1 Chydurus sphaericus (O.F. M¨uller, 1785) 0 0 1 1 1 1 1 1 0 1 Copepods and cladocerans in Patagonia 1023

Table 2. (continued)

Sites21222324252627282930

Boeckella brasiliensis (Lubbock, 1855) 0 1 0 0 0 0 0 0 0 0 Boeckella brevicaudata (Brady, 1875) 0 0 0 0 0 0 0 0 0 0 Boeckella gracilipes (Daday, 1902) 0 0 1 1 1 0 0 1 0 0 Boeckella meteoris (Kiefer, 1928) 0 0 0 0 0 0 0 0 0 0 Boeckella. michaelseni (Mrázek, 1901) 0 1 1 1 1 1 1 1 1 0 Boeckella poopoensis (Marsh, 1906) 1 0 0 0 0 0 0 0 0 1 Boeckella poppei (Mrázek, 1901) 1 1 0 0 0 0 0 0 1 0 Parabroteas sarsi (Mrázek, 1901) 0 0 0 0 0 0 0 0 1 0 Acantocyclops vernalis (Fisher, 1853) 0 0 1 1 0 0 0 0 0 0 Mesocyclops longisetus (Thiebaud, 1914) 0 0 1 1 1 1 1 1 0 0 Tropocylops prasinus (Fisher, 1960) 0 0 0 0 1 0 0 1 0 0 Microcyclops sp 0000000000 Juvenilecyclopoida 0100000010 Juvenile harpacticoida 0 0 0 0 0 0 0 0 0 0 Artemia persimilis (Piccinelli et Prosdocimi 1968) 0 0 0 0 0 0 0 0 0 0 Branchinecta gaini (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 Branchinecta granulosa (Daday, 1902). 0 0 0 0 0 0 0 0 1 0 Branchinecta vuriloche (Cohen, 1985) 0 0 0 0 0 0 0 0 0 0 Daphnia ambigua (Scourfield, 1967) 0 0 0 0 0 0 0 0 0 0 Daphnia dadayana (Paggi, 1999) 0 1 0 0 0 0 0 0 1 0 Daphnia obtusa (Kurz, 1874) 0 0 0 0 0 0 0 0 0 0 Daphnia pulex (Scourfield, 1877) 0 0 1 1 0 0 0 0 1 0 Ceriodaphnia dubia (Richard, 1894) 0 1 1 1 0 0 0 0 0 0 Scapholeberis exispinifera (Nicolet, 1849) 0 0 0 0 0 0 0 0 0 1 Simosa vetula (O.F. M¨uller, 1776) 0 0 0 0 0 0 0 0 0 0 Neobosmina chilensis (Daday, 1902) 0 0 1 1 1 0 0 0 0 0 Chydurus sphaericus (O.F. M¨uller, 1785) 0 1 1 1 0 0 0 0 1 0

Sites31323334353637383940

Boeckella brasiliensis (Lubbock, 1855) 0 0 0 0 0 0 0 0 0 0 Boeckella brevicaudata (Brady, 1875) 0 0 0 0 0 0 0 0 1 0 Boeckella gracilipes (Daday, 1902) 0 0 0 1 0 0 0 0 0 0 Boeckella meteoris (Kiefer, 1928) 0 0 0 0 0 0 0 0 0 0 Boeckella. michaelseni (Mrázek, 1901) 0 0 0 0 0 0 0 0 0 0 Boeckella poopoensis (Marsh, 1906) 0 1 0 0 0 0 0 0 0 0 Boeckella poppei (Mrázek, 1901) 1 0 0 0 1 1 0 0 1 1 Parabroteas sarsi (Mrázek, 1901) 0 0 0 0 0 0 0 0 1 1 Acantocyclops vernalis (Fisher, 1853) 0 0 0 0 0 0 0 0 0 0 Mesocyclops longisetus (Thiebaud, 1914) 0 0 0 0 0 0 0 0 0 0 Tropocylops prasinus (Fisher, 1960) 0 0 0 0 0 0 0 0 0 0 Microcyclops sp 0000000000 Juvenilecyclopoida 0101000010 Juvenile harpacticoida 0 0 0 0 0 0 0 0 0 0 Artemia persimilis (Piccinelli et Prosdocimi 1968) 0 0 0 0 0 0 0 0 0 0 Branchinecta gaini (Daday, 1902) 0 0 0 0 0 0 0 0 1 1 Branchinecta granulosa (Daday, 1902). 0 0 0 0 0 0 0 0 0 0 Branchinecta vuriloche (Cohen, 1985) 0 0 0 0 0 0 0 0 0 0 Daphnia ambigua (Scourfield, 1967) 0 0 0 0 0 0 0 0 0 0 Daphnia dadayana (Paggi, 1999) 0 0 0 0 0 0 1 0 1 1 Daphnia obtusa (Kurz, 1874) 0 0 0 0 0 0 0 0 0 0 Daphnia pulex (Scourfield, 1877) 1 0 1 0 1 1 1 1 0 0 Ceriodaphnia dubia (Richard, 1894) 0 0 0 0 0 0 0 0 0 0 Scapholeberis exispinifera (Nicolet, 1849) 1 1 0 0 0 0 0 0 0 0 Simosa vetula (O.F. M¨uller, 1776) 0 0 0 0 0 0 1 1 0 0 Neobosmina chilensis (Daday, 1902) 0 0 0 1 0 0 0 0 1 0 Chydurus sphaericus (O.F. M¨uller, 1785) 1 0 1 0 1 1 1 1 0 0 1024 P. De los Ríos et al.

Table 2. (continued)

Sites41424344454647484950

Boeckella brasiliensis (Lubbock, 1855) 0 0 0 0 0 0 0 0 0 0 Boeckella brevicaudata (Brady, 1875) 0 0 0 0 0 0 0 0 0 0 Boeckella gracilipes (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 Boeckella meteoris (Kiefer, 1928) 0 0 0 0 0 0 0 0 0 0 Boeckella. michaelseni (Mrázek, 1901) 0 0 0 0 0 0 0 0 0 0 Boeckella poopoensis (Marsh, 1906) 0 0 0 0 0 1 0 0 0 0 Boeckella poppei (Mrázek, 1901) 1 1 1 1 1 0 0 1 1 1 Parabroteas sarsi (Mrázek, 1901) 1 1 1 1 1 0 0 0 0 0 Acantocyclops vernalis (Fisher, 1853) 0 0 0 0 0 0 0 0 0 0 Mesocyclops longisetus (Thiebaud, 1914) 0 0 0 0 0 0 0 0 0 0 Tropocylops prasinus (Fisher, 1960) 0 0 0 0 0 0 0 0 0 0 Microcyclops sp 0000000001 Juvenilecyclopoida 0000000000 Juvenile harpacticoida 0 0 0 0 0 0 0 0 0 0 Artemia persimilis (Piccinelli et Prosdocimi 1968) 0 0 0 0 0 0 0 0 0 0 Branchinecta gaini (Daday, 1902) 1 1 1 1 1 0 0 0 0 0 Branchinecta granulosa (Daday, 1902). 0 0 0 0 0 0 0 0 0 0 Branchinecta vuriloche (Cohen, 1985) 0 0 0 0 0 0 0 0 0 0 Daphnia ambigua (Scourfield, 1967) 0 0 0 0 0 0 0 0 0 0 Daphnia dadayana (Paggi, 1999) 1 1 1 1 1 0 0 1 1 1 Daphnia obtusa (Kurz, 1874) 0 0 0 0 0 0 0 0 0 0 Daphnia pulex (Scourfield, 1877) 0 0 0 0 0 0 1 0 0 0 Ceriodaphnia dubia (Richard, 1894) 0 0 0 0 0 0 1 0 0 0 Scapholeberis exispinifera (Nicolet, 1849) 0 0 0 0 0 0 0 0 0 0 Simosa vetula (O.F. M¨uller, 1776) 0 0 0 0 0 0 0 0 0 0 Neobosmina chilensis (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 Chydurus sphaericus (O.F. M¨uller, 1785) 0 0 0 0 0 0 1 1 1 0

Sites51525354555657585960

Boeckella brasiliensis (Lubbock, 1855) 0 0 0 0 0 0 0 0 0 0 Boeckella brevicaudata (Brady, 1875) 0 0 0 0 0 0 0 0 0 0 Boeckella gracilipes (Daday, 1902) 0 0 0 0 0 1 0 0 0 0 Boeckella meteoris (Kiefer, 1928) 0 0 0 0 0 0 0 0 0 0 Boeckella. michaelseni (Mrázek, 1901) 0 0 0 0 0 0 0 0 0 0 Boeckella poopoensis (Marsh, 1906) 0 0 0 0 0 0 1 0 0 0 Boeckella poppei (Mrázek, 1901) 0 1 1 1 1 0 0 1 1 1 Parabroteas sarsi (Mrázek, 1901) 0 1 0 0 0 0 0 0 0 0 Acantocyclops vernalis (Fisher, 1853) 0 0 0 0 0 0 0 0 0 0 Mesocyclops longisetus (Thiebaud, 1914) 0 0 0 0 0 0 0 0 0 0 Tropocylops prasinus (Fisher, 1960) 0 0 0 0 0 0 0 0 0 0 Microcyclops sp 0000000000 Juvenilecyclopoida 0101100111 Juvenile harpacticoida 1 0 0 0 0 0 1 0 0 0 Artemia persimilis (Piccinelli et Prosdocimi 1968) 1 0 0 0 0 0 1 0 0 0 Branchinecta gaini (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 Branchinecta granulosa (Daday, 1902). 0 0 0 0 0 0 0 0 0 0 Branchinecta vuriloche (Cohen, 1985) 0 0 0 0 0 0 0 0 0 0 Daphnia ambigua (Scourfield, 1967) 0 0 0 0 0 0 0 0 0 0 Daphnia dadayana (Paggi, 1999) 0 1 1 0 0 0 0 1 1 1 Daphnia obtusa (Kurz, 1874) 0 0 0 0 0 0 0 0 0 0 Daphnia pulex (Scourfield, 1877) 0 0 0 0 1 1 0 0 1 1 Ceriodaphnia dubia (Richard, 1894) 0 0 0 0 0 0 0 0 0 0 Scapholeberis exispinifera (Nicolet, 1849) 0 0 0 0 0 0 0 0 0 0 Simosa vetula (O.F. M¨uller, 1776) 0 0 0 0 0 0 0 0 0 0 Neobosmina chilensis (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 Chydurus sphaericus (O.F. M¨uller, 1785) 0 1 0 0 0 1 0 0 1 0 Copepods and cladocerans in Patagonia 1025

Table 2. (continued)

Sites61626364656667686970

Boeckella brasiliensis (Lubbock, 1855) 0 0 0 0 0 0 0 0 0 0 B. brevicaudata (Brady, 1875) 0 0 0 0 0 0 0 0 0 0 B. gracilipes (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 B. meteoris (Kiefer, 1928) 0 0 0 0 0 0 0 0 0 0 B. michaelseni (Mrázek, 1901) 0 0 0 0 0 0 0 0 0 0 B. poopoensis (Marsh, 1906) 0 0 0 0 0 0 0 0 0 0 B. poppei (Mrázek, 1901) 1 1 1 1 1 1 1 1 1 1 Parabroteas sarsi (Mrázek, 1901) 0 0 0 0 0 0 0 0 0 0 Acantocyclops vernalis (Fisher, 1853) 0 0 0 0 0 0 0 0 0 0 Mesocyclops longisetus (Thiebaud, 1914) 0 0 0 0 0 0 0 0 0 0 Tropocylops prasinus (Fisher, 1960) 0 0 0 0 0 0 0 0 0 0 Microcyclops sp 0000000000 Unidentified cyclopoida 1 0 1 1 1 1 1 0 0 0 Unidentifiedharpacticoida 0000000000 Artemia persimilis (Piccinelli et Prosdocimi 1968) 0 0 0 0 0 0 0 0 0 0 Branchinecta gaini (Daday, 1902) 0 0 0 0 0 0 0 0 0 1 B. granulosa (Daday, 1902). 0 0 0 0 0 0 0 0 0 0 B. vuriloche (Cohen, 1985) 0 0 0 0 0 0 0 0 0 0 Daphnia ambigua (Scourfield, 1967) 0 0 0 0 0 0 0 1 0 0 D. dadayana (Paggi, 1999) 1 1 0 0 0 0 0 1 0 0 D. obtusa (Kurz, 1874) 0 0 0 0 0 0 0 1 0 0 D. pulex (Scourfield, 1877) 0 1 1 0 0 0 0 0 0 0 Ceriodaphnia dubia (Richard, 1894) 0 0 0 0 0 0 0 0 0 0 Scapholeberis exispinifera (Nicolet, 1849) 0 0 0 0 0 0 0 0 0 0 Simosa vetula (O.F. M¨uller, 1776) 0 0 0 0 0 0 0 1 0 0 Neobosmina chilensis (Daday, 1902) 0 0 0 0 0 0 0 0 0 0 Chydurus sphaericus (O.F. M¨uller, 1785) 0 0 1 0 0 0 0 1 1 1

Table 3. Results of null model analysis for co-occurrence of species at the studied sites (P < 0.05 denotes random absence).

C-score V-ratio

Fixed-Fixed Fixed-Proportional Fixed-Equiprobable Fixed-Proportional Fixed-Equiprobable

Observed index 51.692 51.692 51.692 1.176 1.176 Mean of simulated indices 49.343 44.947 50.265 1.720 0.997 SES 5.153 3.736 1.1222 –2.162 1.082 Variance of simulated index 0.020 3.257 1.6162 0.063 0.027 P < 0.001 < 0.001 0.129 0.990 0.143 sis does not coexist with Artemia (Hulrbert et al. 1984, al. 2008a; De los Ríos 2008) and northern Patagonian 1986; Williams et al. 1995; De los Ríos & Crespo 2004; mountain lakes and shallow ponds (De los Ríos et al. De los Ríos 2005). The species observed in the present 2008b, c), where three simulations denoted the absence study included some wide spread species such as B. of random in species regulation. The presence of ran- gracilipes, D. pulex and C. dubia, and endemic species dom in species associations (Fixed-Equiprobable simu- such as B. poppei, P. sarsi and D. dadayana,apartic- lation of –score, and both simulations of V-ratio) is due ular situation is the presence of the halophilic calanoid to the presence of few species repeated in all or practi- copepod B. poopoensis (Marsh, 1906) (Table 2). The cally all sites (De los Ríos et al. 2008a, b, c; De los Ríos values of species genera ratio was low (Table 1), this 2008); similar results would success in terrestrial sys- is probably due to low species number and, from eco- tems (Ribas & Schoereder 2002; Sanders et al. 2007). logical view point, the low competition was due to low Other similar causes can be the homogeneity of stud- environmental productivity (Gotelli & Graves 1996; De ied habitats (Franca & Araujo 2007), or interactions los Ríos 2008). between species with similar ecological characteristics The results of null model revealed that there is a (Tondoh 2006; Tiho & Johens 2007). In an opposite sce- structured pattern in species associations for the stud- nario, the presence of interspecific competition and eco- ied sites which is denoted by the results of two of the logical differentiation denotes the absence of random in three C-score simulations (Table 3). These results agree species association (Ulrich 2004; Rodríguez-Fernandez with observations for zooplankton species associations et al. 2006). In another side, the existence of significant based on null model co-occurrence species for south- effects, expressed in random absence, as it was observed ern Patagonian lakes and/or ponds (De los Ríos et in two simulations denoted the existence of habitat seg- 1026 P. De los Ríos et al. regations and resources partition (Costa de Azevedo et De los Ríos P. & Zú˜niga O. 2000. Comparación biométrica del al. 2006). lóbulo frontal en poblaciones americanas de Artemia (Anos- traca: Artemiidae). Rev. Chil. Hist. Nat. 73: 31–38. De los Ríos P., Acevedo P., Rivera R. & Roa G. 2008a. Comu- Acknowledgements nidades de crustáceos litorales de humedales del norte de la Patagonia chilena (38◦ S): rol potencial de la exposición a la radiación ultravioleta, pp. 209–229. In: Volpedo A. & Fernan- The present study was financed by projects DID-UACH dez L. (eds), Efecto de los cambios globales en la diversidad, d2001–11, CONICYT-Chile (Doctoral Fellowship and Grant Programa CYTED 406RT0285. for support Doctoral Thesis), and the Research Direction of De los Ríos P., Rivera N. & Galindo M. 2008b. The use of null the Catholic University of Temuco (Fund for Development models to explain zooplancton species associations in shallow of Limnology, Project DGI-UCT CDA 2007-01). water bodies of the Magallanes region, Chile. Crustaceana 81: 1219–1228. De los Ríos P., Rogers D. C. & Rivera N. 2008c. Branchinecta References gaini (Daday, 1910) (, ) as a bioindi- cator of oligotrophic and low conductivity shallow ponds in 81: Abelha M.C.F, Goulart E., Kashiwaqui E.A.L. & Da Silva M.R. southern Chilean Patagonia. Crustaceana 1025–1034. 2006. Astyanax paranae Eigenmann, 1914 (Characiformes: Dodson S.I. 1992. Predicting species richness of crus- 37: Characidae) in the Alagados Reservior, Parana, Brazil: diet tacean zooplankton species richness. Limnol. 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