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Halotolerant Copepoda in South American inland saline waters

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DOI: 10.1163/15685403-00003780

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 Crustaceana 91 (5) 527-535

HALOTOLERANT COPEPODA IN SOUTH AMERICAN INLAND SALINE

WATERS

BY

PATRICIO DE LOS RÍOS1,2,4 ) and IAN A. E. BAYLY3 )

1 ) Universidad Católica de Temuco, Facultad de Recursos Naturales, Departamento de Ciencias
Biológicas y Químicas, Laboratorio de Ecología Aplicada y Biodiversidad, Casilla 15-D, Temuco,
Chile
2 ) Núcleo de Estudios Ambientales, UCTemuco, Casilla 15-D, Temuco, Chile
3 ) 501 Killiecrankie Road, Flinders Island, TAS 7255, Australia

ABSTRACT

The zooplankton in South American saline waters is mainly dominated by copepods at salinities
lower than 90 g/l, whereas at salinities above 90 g/l Artemia sp. is totally dominant. The aim of
the present study is to analyse the salinity range of halophilic copepods on the basis of a literature
review for South American saline inland waters. The calanoid Boeckella poopoensis Marsh, 1906,
is widespread on the South American Altiplano and southern Argentinian plains, and in southern
Patagonian shallow ponds. In the upper part of the salinity range, 20-90 g/l, B. poopoensis is the
only copepod in the zooplankton of southern Patagonian and Altiplano shallow lakes. In the salinity
range 5-20 g/l B. poopoensis may co-exist with B. palustris (Harding, 1955), two cyclopoids and an
harpacticoid, and at salinities lower than 5 g/l it may co-exist with an even wider range of copepod
species. Ecological and biogeographical aspects are also discussed.

RESUMEN

El zooplancton en las aguas salinas sudamericanas está dominado principalmente por copépodos
a salinidades inferiores a 90 g/l, mientras que en salinidades superiores a 90 g/l Artemia sp. es
totalmente dominante. El objetivo del presente estudio es analizar el rango de ocurrencia de salinidad
de los copépodos halófilicos sobre la base de una revisión de la literatura para las aguas interiores
salinas sudamericanas. El calanoideo Boeckella poopoensis Marsh, 1906, está muy extendida en el
altiplano de Sudamérica y las llanuras argentinas del sur, y en los estanques someros de la Patagonia
austral. En la parte superior del rango de salinidad 20-90 g/l B. poopoensis es el único copépodo
en el zooplancton de los lagos poco profundos del sur de la Patagonia y el Altiplano. En el rango
de salinidad, 5-20 g/l de B. poopoensis pueden coexistir con B. palustris (Harding, 1955), con dos
especies diferentes de ciclopoideos y una de harpacticoideo, y en salinidades inferiores a 5 g/l pueden
coexistir con un amplio rango de especies. Se discuten aspectos ecológicos y biogeográficos.

4 ) Corresponding author; e-mail: prios@uct.cl

© Koninklijke Brill NV, Leiden, 2018 DOI 10.1163/15685403-00003780

528 PATRICIO DE LOS RÍOS & IAN A. E. BAYLY

INTRODUCTION

Saline lakes in South America are located on the Altiplano associated with
volcanic zones in northwestern Argentina, northern Chile, western Bolivia and
southern Peru, the central southern Argentinean plains, southern Argentina and
Patagonia (Hammer, 1986; Williams, 1998). Copepod species dominate in the
zooplankton in South American saline inland waters in salinities up to 90 g/l, and
Artemia spp. at salinities over 90 g/l. Boeckella poopoensis Marsh, 1906 is the
only calanoid copepod species in the zooplankton of South American hypersaline
waters. Looking at regions outside the Americas, some copepod species tolerate
salinities of up to 300 g/l (Vesnina, 2003; Pinder et al., 2005; Anufriieva & Shadrin,
2014; Anufriieva, 2015). Whereas in North America Leptodiaptomus siciloides
(Lilljeborg in Guerne & Richard, 1889) is the only calanoid copepod species in
zooplankton of hypersaline waters (up to 107 g/l) (Moore, 1952).
Salinity is a dominant regulator of zooplankton assemblages. Five to six
Boeckella species, some of which may co-exist, may occur at salinities lower than
5 g/l but at salinities above 20 g/l only one Boeckella species is found. Although
Artemia sp. and B. poopoensis may occur in salinities between 20 and 90 g/l,
these species do not coexist (De los Ríos-Escalante, 2010; De los Ríos-Escalante
& Gajardo, 2010a, b). The aim of the present study is to analyse the salinity
tolerances of copepods in South American saline inland waters based on a literature
review.

MATERIAL AND METHODS

Salinity tolerance data expressed as g/l were obtained from a variety of literature
(Hurlbert et al., 1984, 1986; Bayly, 1993; Williams et al., 1995; De los Ríos &
Crespo, 2004; De los Ríos & Contreras, 2005; Echaniz et al., 2005; Locascio
de Mitrovich et al., 2005; De los Ríos & Gajardo, 2010a; De los Ríos-Escalante
& Gajardo, 2010b; D’Ambrosio et al., 2013). Data from southern Argentinean
plains were not used in our statistical analyses because these are expressed as total
dissolved solids (Echaniz et al., 2006, 2008, 2013a, b; Echaniz & Vignatti, 2001,
2011; Vignatti et al., 2007, 2012a, b, c).
Salinity data were tested for normality and homoscedasticity, and due to
the absence of both conditions, a non-parametric Kruskall-Wallis test, and a
Tukey non-parametric multiple comparison test (Zar, 1999) were employed. The
statistical analysis also used the software R (R Development Core Team, 2009),
package PMCMR (Pohlert, 2014).
 SOUTH AMERICAN HALOPHILIC INLAND WATER COPEPODA 529

RESULTS AND DISCUSSION

The results (tables I and II) showed significant differences in salinity tolerances
for the species under consideration (Chi-squared = 63.582; p-value < 0.001).
The species with the lowest salinity tolerance was Boeckella calcaris (Harding,
1955), and the species with the highest salinity tolerance was B. poopoensis with
means of 0.56 and 23.31 g/l, respectively. B. poopoensis had the widest salinity
tolerance of 0.50 to 86.0 g/l (table I). The results of the multiple comparison
test showed that B. poopoensis was significantly different from other species
of the genus (table II). But B. poopoensis was not significantly different from
the other extremely halotolerant copepod species such as Cletocamptus deitersi
(Richard, 1897), Metacyclops mendocinus (Wierzejski, 1892) and Microcyclops
anceps (Richard, 1897), (table II). More details on geographical location and
salinity occurrence are specified in the Appendix.
The results revealed that South American halophilic copepods have a markedly
different salinity tolerance compared with halophilic copepods in other regions,
such as the Crimea and Australia, where they may occur at salinities of 150-200 g/l
(Bayly, 1993; Shadrin & Anufriieva, 2013a, b; Anufriieva et al., 2014; Anufriieva,
2015). The South American centropagid calanoids are endemic, and some species
are restricted to specific geographic areas such as the Altiplano for B. calcaris
(Harding, 1955), B. palustris (Harding, 1955), B. occidentalis Marsh, 1906 and B.
titicacae Harding, 1955. Other species are widespread in South America such as
B. gracilipes Daday, 1902 and B. poopoensis. There are no Northern Hemisphere
copepod species in South American saline inland waters (Menu-Marque et al.,
2000; Echaniz & Vignatti, 2001, 2011; De los Ríos-Escalante, 2010; Fuentes &
Gajardo, 2017; Vignatti et al., 2017).
In South America, Boeckella has colonized a wide variety of habitats from
small freshwater pools to large saline lakes (Bayly, 1993, 1995; Menu-Marque
et al., 2000; Adamowicz et al., 2007; Bayly & Boxshall, 2009). The existence of
the Altiplano and the Andes mountains has provided a variety of high altitude
habitats that contrast with the plains found in southern Argentina and parts of
Patagonia (Appendix; Menu-Marque et al., 2000). Apart from the evolution of
the physiological “machinery” that permits Artemia and B. poopoensis to tolerate
a wide range of salinities, predator-prey interactions may come into play at the
lower end of their salinity range where they coexist with other species (Hurlbert
et al., 1986; Hammer & Hurlbert, 1992; De los Ríos-Escalante, 2010; Fuentes &
Gajardo, 2017).
 530

TABLE I
Salinity values in water of occurrence (g/l) for halophilic copepods reported for South American inland waters

Species Mean Minimum Maximum N <−5.00 g/l 5.00-20.00 g/l >20.00 g/l
Boeckella calcaris (Harding, 1955) 0.56 0.00 1.00 3 X
B. gracilipes Daday, 1902 1.59 0.27 3.70 9 X
B. occidentalis Marsh, 1906 1.00 0.23 3.50 9 X
B. palustris (Harding, 1955) 2.07 0.46 6.52 4 X X
B. poopoensis Marsh, 1906 23.31 0.50 86.00 52 X X X
B. titicacae Harding, 1955 1.44 0.27 3.70 11 X
Cletocamptus deitersi (Richard, 1897) 10.85 0.47 26.16 14 X X X
Metacyclops mendocinus (Wierzejski, 1892) 11.24 3.37 20.79 6 X X
Microcyclops anceps (Richard, 1897) 8.36 1.38 18.45 5 X X
PATRICIO DE LOS RÍOS & IAN A. E. BAYLY
 SOUTH AMERICAN HALOPHILIC INLAND WATER COPEPODA 531

TABLE II
Results of multiple comparison test for species mentioned in the present study

Species compared P -value

B. calcaris–B. gracilipes 0.999 n.s.
B. calcaris–B. occidentalis 0.999 n.s.
B. calcaris–B. palustris 0.999 n.s.
B. calcaris–B. poopoensis 0.038∗∗
B. calcaris–B. titicacae 0.999 n.s.
B. calcaris–C. deitersi 0.483 n.s.
B. calcaris–M. mendocinus 0.383 n.s.
B. calcaris–M. anceps 0.740 n.s.
B. gracilipes–B. occidentalis 0.999 n.s.
B. gracilipes–B. palustris 0.999 n.s.
B. gracilipes–B. poopoensis 0.001∗∗
B. gracilipes–B. titicacae 0.999 n.s.
B. gracilipes–C. deitersi 0.219 n.s.
B. gracilipes–M. mendocinus 0.218 n.s.
B. gracilipes–M. anceps 0.684 n.s.
B. occidentalis–B. palustris 0.999 n.s.
B. occidentalis–B. poopoensis 0.001∗∗
B. occidentalis–B. titicacae 0.999 n.s.
B. occidentalis–C. deitersi 0.100 n.s.
B. occidentalis–M. mendocinus 0.117 n.s.
B. occidentalis–M. anceps 0.511 n.s.
B. palustris–B. poopoensis 0.036∗∗
B. palustris–B. titicacae 0.999 n.s.
B. palustris–C. deitersi 0.586 n.s.
B. palustris–M. mendocinus 0.477 n.s.
B. palustris–M. anceps 0.845 n.s.
B. poopoensis–B. titicacae 0.001∗∗
B.poopoensis–C. deitersi 0.631 n.s.
B. poopoensis–M.mendocinus 0.998 n.s.
B. poopoensis–M. anceps 0.908 n.s.
B. titicacae–C. deitersi 0.125 n.s.
B. titicacae–M. mendocinus 0.150 n.s.
B. titicacae–M. anceps 0.598 n.s.
C. deitersi–M. mendocinus 0.999 n.s.
C. deitersi–M. anceps 0.999 n.s.
M. mendocinus–M. anceps 0.999 n.s.

∗∗ Significant difference, P <0.05.

ACKNOWLEDGEMENTS

The present study was founded by projects Tides Grant Foundation TRF13-
03011 MECESUP UCT 0804 and the Research Direction of the Catholic Univer-
sity of Temuco. We also thank M.I. for her valuable comments to improve the
manuscript.
532 PATRICIO DE LOS RÍOS & IAN A. E. BAYLY

APPENDIX

Locality and salinity data for copepod species as retrieved from the literature.
I. Altiplano.
Boeckella calcaris: Conchostraca (0.69 g/l; 22°18 S 67°14 W; Bayly, 1993); Abra del Gallo
(<0.01 g/l; 24°16 S 66°22 W; Locascio de Mitrovich et al., 2005)
Boeckella gracilipes: Abra del Gallo (<0.01 g/l; 24°16 S 66°22 W; Locascio de Mitrovich et al.,
2005).
Boeckella meteoris: Pelada (4.10 g/l; 22°45 S 67°10 W; Bayly, 1993); Pozuelos (6.20 g/l; 22°45 S
66°00 W; Bayly, 1993).
Boeckella occidentalis: Suches (0.23 and 0.60 g/l; 16°56 S 70°21 W; Bayly, 1993); Colorada II
(0.27 g/l; 15°22 S 70°21 W; Bayly, 1993); Cotacotani (0.60 g/l; 18°14 S 69°13 W; Bayly,
1993); Pampamarca (0.8-1.0 g/l; 14°08 S 71°29 W; Bayly, 1993); Saracocha (1.10 g/l; 15°47 S
70°38 W; Bayly, 1993); Chungará (1.20 g/l; 18°15 S 69°09 W; Bayly, 1993); Huancaroma
(3.50 g/l; 17°40 S 67°30 W; Bayly, 1993).
Boeckella palustris: Loripongo (0.46 and 0.62 g/l; 16°50 S 70°05 W; Bayly, 1993); Conchostraca
(0.69 g/l; 22°18 S 67°14 W; Bayly, 1993); Salar de Surire (1.00 g/l; 18°51 S 69°07 W; De los
Ríos & Contreras, 2005).
Boeckella poopoensis: Loripongo (0.46 and 0.62 g/l; 16°50 S 70°05 W; Bayly, 1993; 2.60 g/l;
Hurlbert et al., 1986); Parinacochas (5.60 g/l; 15°17 S 73°42 W; Bayly, 1993; 3.0 g/l; Hurlbert
et al., 1986); Santa Rosa (7.50 g/l; 27°05 S 69°10 W; Bayly, 1993; 8.00 g/l De los Ríos &
Crespo, 2004); Catalcito (8.10 g/l; 23°31 S 67°15 W; Bayly, 1993); Puripica Chico (8.20 g/l;
22°31 S 67°30 W; Bayly, 1993); Khara (8.70 g/l; 21°54 S 67°52 W; Bayly, 1993); Calientes
II (= Salar de Capur) (10.00 g/l; 23°31 S 67°34 W; Bayly, 1993; 3.40 g/l De los Ríos &
Crespo, 2004); Loriscota (10.40-11.60 g/l; 16°52 S 70°02 W; Bayly, 1993; 2.6 g/l; Hurlbert
et al., 1986); Soledad (11.00 g/l; 17°44 S 67°22 W; Bayly, 1993); Chojllas (11.10 g/l; 22°2 S
67°06 W; Bayly, 1993); Polques (10.00-13.00 g/l; 22°2 S 67°37 W; Bayly, 1993; Hombre Muerto
(21.00 g/l; 25°30 S 66°51 W; Bayly, 1993); Calientes III (24.20 g/l; 25°00 S 68°38 W; Bayly,
1993); Ramaditas (25.70 g/l; 21°38 S 68°05 W; Bayly, 1993) (47.30 g/l; Williams et al., 1995);
Guacha (36.00 g/l; 22°33 S 67°31 W; Bayly, 1993); Collpacocha (38.60 g/l; 15°15 S 70°03 W;
Bayly, 1993; 39.00 g/l; Hurlbert et al., 1986); Calientes I (47.00 g/l; 23°08 S 67°24 W; Bayly,
1993); Verde II (57.10-58.10 g/l; 22°48 S 67°48 W; Bayly, 1993; 49.00 g/l; Hurlbert, et al., 1984);
Chulluncani (64.50 g/l; 21°32 S 67°52 W; Bayly, 1993; 19.00 g/l; Hurlbert et al., 1984); Este
(86.00 g/l; 22°31 S 67°29 W; Bayly, 1993); Uru-Uru (4.40 g/l; 17°55 S 66°27 W; Williams et al.,
1995); Miniques (9.79 g/l; 23°45 S 67°44 W; De los Ríos & Crespo, 2004); Miscanti (8.98 g/l;
23°44 S 67°46 W; De los Ríos & Crespo, 2004); Gemela Oeste (46.50 g/l; 23°30 S 68°14 W;
De los Ríos & Crespo, 2004); Gemela Este (54.10 g/l; 23°30 S 68°14 W; De los Ríos & Crespo,
2004); Loromayu (94.00 g/l; 22°18 S 67°13 W; Hurlbert et al., 1984);
Boeckella titicacae: Cotacotani (0.60 g/l; 18°14 S 69°13 W; Bayly, 1993); Totoral (0.65 g/l; 22°32 S
67°17 W; Bayly, 1963); Conchostraca (0.69 g/l; 22°18 S 67°14 W; Bayly, 1993); Viscacha
(0.90 g/l; 19°53 S 70°14 W; Bayly, 1993); Campo Grande (3.40 g/l; 22°33 S 67°12 W; Bayly,
1993); Huancaroma (3.50 g/l; 17°40 S 67°30 W; Bayly, 1993); Peñitas Blancas (3.70 g/l; 22°65 S
67°15 W; Bayly, 1993); Peñitas Blancas (3.70 g/l; 22°65 S 67°15 W; Bayly, 1993); Salar de
Surire (1.00 g/l; 18°51 S 69°07 W; De los Ríos & Contreras, 2005).
Cletocamptus deitersi: Pasto Ventura (6.52 g/l; Locascio de Mitrovich et al., 2005); Blanca (0.47 g/l;
26°50 S 66°57 W; Locascio de Mitrovich et al., 2005).
Locality and salinity data for copepod species as retrieved from the literature.
II. Central-southern Argentinean plains.
Boeckella gracilis: El Carancho (11.60 g/l; 37°27 S 65°04 W; Echaniz et al., 2005); Mercedinas
(1.38 g/l; 34°00 S 65°24 W; Cabrera et al., 2013).
 SOUTH AMERICAN HALOPHILIC INLAND WATER COPEPODA 533

Boeckella palustris: Pasto Ventura (6.52 g/l; 26°43 S 67°10 W; Locascio de Mitrovich et al., 2005).
Boeckella poopoensis: Los Manantiales (8.53 g/l; 37°12 S 64°17 W; Echaniz et al., 2005); El Destino
(12.62 g/l; 37°06 S 64°17 W; Echaniz et al., 2005); Laura (18.45 g/l; 37°10 S 64°17 W; Echaniz
et al., 2005); El Carancho (11.60; 20.79 g/l; Echaniz et al., 2005); Chadilauquén (19.38 g/l;
64°19 S 35°24 W; Echaniz et al., unpublished data); Bajo de Guiliani (10.60 g/l; 36°41 S
64°15 W; 36°41 S 64°15 W; Echaniz et al., unpublished data); Llancahuelo (1.10; 10.80; 22.40;
25.30 g/l; 35°34 S 69°09 W; D’Ambrosio et al., 2016).
Cletocamptus deitersi: Los Manantiales (8.43 g/l; 37°12 S 64°17 W; Echaniz et al., 2005); El
Destino (12.62 g/l; 37°06 S 64°17 W; Echaniz et al., 2005); Laura (18.45 g/l; Echaniz et al.,
2005); El Carancho (20.79 g/l; Echaniz et al., 2005); Bajo de Guiliani (10.60 g/l; 36°41 S
64°15 W; Echaniz et al., unpublished data); Pasto Ventura (6.52 g/l; Locascio de Mitrovich et
al., 2005); Blanca (0.47 g/l; 26°50 S 66°57 W; Locascio de Mitrovich et al., 2005); Mercedinas
(1.67 g/l; 34°00 S 65°24 W; Cabrera et al., 2013).
Metacyclops mendocinus: Los Manantiales (8.43 g/l; 37°12 S 64°17 W; Echaniz et al., 2005); El
Destino (12.62 g/l; 37°06 S 64°17 W; Echaniz et al., 2005); El Carancho (11.60; 20.79 g/l;
Echaniz et al., 2005); Bajo de Guiliani (10.60 g/l; 36°41 S 64°15 W; Echaniz et al., unpublished
data); Mercedinas (3.37 g/l; 34°00 S 65°24 W; Cabrera et al., 2013).
Microcyclops anceps: Los Manantiales (8.43 g/l; 37°12 S 64°17 W; Echaniz et al., 2005); Laura
(18.45 g/l; Echaniz et al., 2005); El Carancho (11.60 g/l; 37°27 S 65°04 W; Echaniz et al., 2005);
Mercedinas (1.38; 1.94 g/l; 34°00 S 65°24 W; Cabrera et al., 2013).

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First received 11 December 2017.

Final version accepted 19 January 2018.

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