Influence of salinity on the biology of the Neotropical cladoceran Moina eugeniae Olivier, 1954 (Branchiopoda: Moinidae)

Abstract

Moina eugeniae Olivier, 1954 is a common cladoceran species in the zooplankton of saline lakes in central Argentina. Information on this species comes mainly from field studies, and there are few data on its tolerance to environmental factors that help explain its geographic distribution. The objective of this study was to examine the influence of salinity on its biology through bioassays. Treatments were carried out with 7, 17, and 27 g/L of salt. Offspring less than 24 h old were placed in 25 mL containers. Every 48 hours until death, the medium was renewed, the offspring were fed with Chlorella vulgaris and the moults were measured. The optimum salinity was 17 g/L, which resulted in the highest survival and number of moults (29 ± 2.9 days and 10 ± 0.9 moults), the greatest number of clutches and total offspring per female (8 ± 1.07 clutches and 135 ± 13.14 offspring), and the largest size (1.97 ± 0.13 mm). While the best performance was found with 17 g/L salinity, indicating the halophilic character of this species, the lowest values at 7 and 27 g/L indicate some stress. Thus, changes in the salinity of lakes due to climate change could negatively affect the current geographic distribution of M. eugeniae.

Keywords:
Argentina; bioassays; halophilic cladocerans; salinity tolerance; zooplankton.

INTRODUCTION

The semi-arid center of Argentina is characterized by alternating dry and rainy periods (Viglizzo, 2010; Russian et al., 2015), which leads to numerous temporary shallow lakes (Echaniz and Vignatti, 2017; Echaniz et al., 2013; Vignatti et al., 2012a; 2012b), mainly hyposaline and mesosaline lakes (Hammer, 1986). In the zooplankton of these lakes there are several crustaceans endemic to the Neotropical region (Paggi, 1998; Battistoni, 1998; Menu-Marque et al., 2000; Adamowicz et al., 2004; Boxshall and Defaye, 2008, Forró et al., 2008; José de Paggi et al., 2023), including Moina eugeniaeOlivier, 1954. This species was originally described from specimens from the province of Buenos Aires and following its first recording, it was not found again until its discovery in the province of La Pampa in the early 1990s (Echaniz and Vignatti, 1996).

Moina eugeniae is a halotolerant species and, in the absence of predators, can reach population densities greater than 1000 individuals/L (Echaniz et al., 2013). Although it has been found throughout the year, it tends to reach higher densities during the months when the water temperature exceeds 22 °C (Vignatti et al., 2007; 2017; Echaniz et al., 2013). It is the largest moinid in central Argentina. Due to its size, it has a relatively high filtration rate, and when it reaches high densities, its grazing results in relatively low concentrations of phytoplankton chlorophyll-a and, therefore, relatively high water transparency (Vignatti et al., 2017).

Experimental or field studies have examined the influence of salinity on aspects of the biology of some moinids, including the distribution of cryptic lineages of Moina brachiata (Jurine, 1820) in Hungary (Nédli et al., 2014); the survival and reproduction of Moina hutchinsoni (Brem, 1937) (Martinez-Jeronimo and Espinosa-Chavez, 2005), Moina macrocopa (Straus 1820) (Jimenez et al., 2003; Yuslan et al., 2021; Lopatina et al., 2021; Huang et al., 2022), Moina mongolica Daday, 1901 (He et al., 2001), Moina micrura Kurz, 1875 (Santangelo et al., 2008), Moina salina Daday, 1888 (Rokneddine, 2004), and Moina affinis (Zhao et al., 2006) or the life strategies and resistance to hunger of M. macrocopa, M. micrura and M. wierzejskii (Richard, 1895) (Nandini and Sarma, 2019).

In the case of M. eugeniae, some of the information on population aspects derives from field studies (Vignatti et al., 2007; 2017; Echaniz et al., 2013; 2015; Echaniz and Vignatti, 2017). However, to determine the influence of different concentrations of dissolved solids or of the main ions present in the water of the region’s lakes on the biology of this species, acute bioassays were carried out to determine the tolerance of their offspring to salinity (Vignatti et al., 2012c) and to different concentrations of Cl^- and SO^2- ₄ (Cabrera et al., 2014). These bioassays revealed that the optimal medium for the cultivation of M. eugeniae and for the development of bioassays is that prepared by redissolving salts collected in the natural environment instead of using analytical-grade reagents (Vignatti et al., 2014).

Salinity is a critical factor in organism distribution (He et al., 2001) and it is one of the environmental parameters that most strongly affect cladocerans (Hobæk et al., 2002; Ghazy et al., 2009). The absence of eggs or embryos in M. eugeniae females found in a temporary lake at a salinity of 55 g/L (Echaniz and Vignatti, 2017) suggested that its reproduction is affected by high solute concentrations. Since the influence of salinity on other biological aspects of M. eugeniae is unknown, the objective of this study was to test the hypothesis that the increase in stress due to increased salinity negatively affects its longevity, age, and size at which females produce their first clutch of offspring, the number of moults, the number of offspring produced throughout life, and the maximum size reached at the time of death.

MATERIALS AND METHODS

In order to obtain the organisms for the bioassays, sediment was collected from the dry bottom of a saline lake in the province of La Pampa in 2006, where populations of M. eugeniae usually develop during hydrophases. The sediment was placed in a 300-L tank in the open air, with water with physicochemical characteristics similar to those of the lake at the time when M. eugeniae was recorded. Females of different clonal lineages, but similar body length, were taken from the tank and acclimated in the laboratory in 20-L aquaria for 180 days. Offspring (no more than 24 h old and of relatively similar size) produced by acclimated females were used in the bioassays.

Chronic bioassays were performed with three concentrations of dissolved solids: 7, 17, and 27 g/L. The experimental medium was prepared with demineralised water and dissolved salts obtained from a saline lake during a period in which it dried up (Vignatti et al., 2012 c ). Before use, the salts were sterilised by heat (± 260 °C) for 24 h. The ionic composition of the salts used in the bioassays (Tab. 1) was determined according to standardized routines described in Echaniz and Vignatti (2019).

Table 1.
Composition (%) of the natural salts used in the bioassays

CO3 2-	1.86
HCO3 -	0.60
Cl-	29.46
SO4 -	32.65
F-	0.04
As	0.02
Na+	34.13
K+	0.93
Ca2+	0.23
Mg2+	0.08

Offspring were placed in 25 mL plastic containers (one per flask). The numbers of replicates were 14 at 7 g/L, 10 at 17 g/L, and 20 at 27 g/L. Every 48 h until death, the medium was renewed, and the offspring were fed with Chlorella vulgaris from axenic cultures grown in 2-L bottles using Detmer’s medium. Algae in the log phase of growth were centrifuged and resuspended in the experimental medium. The density of this stock concentrate was determined using a haemocytometer. A concentration of 1.5×10⁶ cells/mL was used, which is close to that used to feed cladoceran species of relatively similar size in bioassays (Benider et al., 2002; Nandini and Sarma, 2003; Alva-Martinez et al., 2004; Martinez-Jeronimo and Espinosa-Chavez, 2005). Every 48 h, the produced offspring were removed and counted, and the moults were measured, from the anterior edge of the head to the rear edge of the carapace (Yuslan et al., 2021), using a Leitz® micrometric eyepiece. The photoperiod was 8/16 h (darkness/light), and two 18-watt fluorescent tubes provided lighting. The temperature was maintained at 22 ± 1°C.

The following biological parameters were measured: longevity (average number of days of survival of the females), survival (proportion (%) of individuals surviving to age X), number of moults throughout the life of the specimens, age of the females at the time of the production of the first clutch of offspring (expressed in days), number of clutches and the number of offspring produced by each female, sizes of the females at the time of producing the first clutch of offspring and the maximum size, determined after death, individual mean growth rates throughout the entire life of the specimens (determined as the increase in daily body length, expressed in mm per day). The net reproduction rate (R ₀) and the intrinsic rates of population increase (r) (Yuslan et al., 2021) were calculated for each salinity. To compare the survival in the treatments, log-rank tests were performed (Hammer et al., 2001).

The Q-Q plot and Levene test were conducted to measure the data normality and variance homoscedasticity, respectively (Sokal and Rohlf, 1995; Zar, 1996). Because the tests showed a lack of normality and homoscedasticity, to determine differences between treatments, the non-parametric Kruskal-Wallis analysis (H) (Sokal and Rohlf, 1995; Zar, 1996) and the Mann-Whitney comparison test were used (Hammer et al., 2001).

RESULTS

The mean longevity registered in the three treatments was different (H = 12.4; p = 0.0029), varied between a minimum of 18.14 ± 3.5 days with a salinity of 7 g/L and a maximum of 29 ± 2.9 days in the treatments with 17 g/L. At 27 g/L, an intermediate longevity was recorded (23.30 ± 8.62 days), but with more variability among the different specimens (Fig. 1).

Figure 1.
Comparison of the mean longevity of Moina eugeniae in bioassays carried out under three different salinities.

The log rank test showed that survival differed between treatments (X ² = 8.27; p = 0.01599). Survival of the specimens varied; at 17 g/L, 100% survived until day 25, after which mortality increased markedly, and no specimen survived beyond day 35. At 7 and 27 g/L, most specimens survived until day 13, but beyond that the survival varied. At 7 g/L, mortality increased strongly, and no specimen lived beyond day 27. A salt concentration of 27 g/L resulted in the maximum longevity, as 15% of the specimens reached 40 days (Fig. 2).

Figure 2.
Survival of Moina eugeniae in bioassays performed under three different salinities.

The number of total moults differed (H = 12.72; p < 0.0015). The specimens in the treatments carried out with a salinity of 17 g/L produced 10 ± 0.9 moults, while the number was 7.07 ± 1.21 at 7 g/L and 8.85 ± 2.60 moults at 27 g/L (Fig. 3). Differences were also found in the number of moults before producing the first clutch of offspring (H = 10.74; p < 0.0031). At a salt content of 17 g/L, the females began to reproduce as soon as two moults were produced, while at 7 and 27 g/L they had to produce one additional moult. The number of moults that were produced after the first clutch also varied (H = 14.44; p < 0.0003), with the highest number in the intermediate salinity (Fig. 3).

Figure 3.
Number of moults before and after the first reproduction of Moina eugeniae specimens in the bioassays under three different salinities.

The age at which females produced the first clutch differed (H = 24.93; p < 0.000). It was similar in the treatments with 7 and 17 g/L of salt content, around seven days, but in the treatments with the highest salinity, the first clutch occurred at 9.2 ± 2.24 days (Fig. 4).

Figure 4.
Average (± SD) age (days) of the parthenogenetic females to the first clutch of offspring under three different salinities.

The number of clutches and the total number of offspring produced per female differed (H = 15.48, p < 0.0004 and H = 20.7, p < 0.0000, respectively) (Fig. 5). The maximum for both were recorded with a salinity of 17 g/L (8 ± 1.07 clutches and 135 ± 13.14 offspring). At 7 g/L there were 3.9 (± 1.3) clutches and 46.3 (± 11.3) offspring, and at 27 g/L there were 5.20 ± 2.38 clutches and 42.30 ± 19.04 offspring.

Figure 5.
Mean (± SD) number of clutches produced by parthenogenetic females of Moina eugeniae in each treatment (A), and the average (± SD) number of total offspring produced by females in each treatment (B) under three different salinities.

In the same way, the size that the specimens reached when producing the first clutch differed (H = 12.08; p < 0.0024), from a minimum of 0.92 ± 0.09 mm in the treatments carried out with 17 g/L of salt content to a maximum of 1.19 ± 0.21 mm in those with 27 g/L (Fig. 6). The maximum size of the females also differed (H = 16.63; p < 0.0002), but the situation was inverse to that of the size of the females at the first clutch. The largest specimens were recorded in the treatments with a salinity of 17 g/L, in which they reached an average of 2.10 ± 0.14 mm, and they were smaller in the bioassays with salinities of 7 and 27 g/L, in which they measured 1.63 ± 0.17 and 1.60 ± 0.15, respectively (Fig. 6).

Figure 6.
Mean (± SD) size of parthenogenetic females of Moina eugeniae at the time of producing the first clutch of offspring (A), and the maximum size (± SD) reached in each treatment (B) under three different salinities.

The mean rate of daily increase in the size of females differed (H = 6.45: p < 0.0397). It was higher at a salinity of 17 g/L (0.06 ± 0.06 mm/day) than at 7 g/L (0.05 ± 0.04 mm/day) and 27 g/L (0.03 ± 0.04 mm/day). At a salinity of 17 g/L, the females continued to grow until death, while at 7 and 27 g/L their growth slowed and became asymptotic on day 17, when they had barely exceeded 1.6 mm in both treatments (Fig. 7).

Figure 7.
Mean (± SD) daily increase in the size of Moina eugeniae females under three different salinities.

The net reproduction rate (R ₀) and the intrinsic rate of population increase (r) were 44.18 and 0.26 (7 g/L), 135.03 and 0.22 (17 g/L), and 38.21 and 0.16 (27 g/L), respectively.

DISCUSSION

The relatively euryhaline character of Moina eugeniae had been previously verified through field studies, in which the species was found in a wide range of salinity conditions, up to almost 55 g/L (Vignatti et al., 2017). However, the halotolerance of M. eugeniae is lower than that of other congeneric species, such as Moina mongolica, which can survive up to 53.6-55.5 g/L in the laboratory and has been found in nature at 73 g/L (He et al., 2001), or Moina salina, which has been found in hypersaline waters in Mongolia at a salinity of 61 g/L (Alonso, 2010) and in North Africa at a salinity of 225 g/L (Amarouayache et al., 2012).

Despite the fact that Neretina et al. (2020) classified M. eugeniae as a small-sized moinid (1 mm or less), likely based on Olivier (1954), both field and laboratory studies show that it is a species of relatively large size, and specimens of up to 1.72 mm were recorded in lakes in the semi-arid center of Argentina (June 2007, Chadilauquen and San José Lakes; A. M. Vignatti and S. A. Echaniz, unpublished data). Moreover, in this study, some specimens exceeding 2.35 mm were found at a salinity of 17 g/L, indicating that M. eugeniae is larger than other halotolerant species, such as M. mongolica, whose adults range between 1.0 and 1.55 mm in length (Goulden, 1968; He et al., 2001), or M. hutchinsoni, whose females ranged between 0.996 and 1.182 mm (Martinez-Jeronimo et al., 2004). These latter authors also found that the specimens of M. hutchinsoni grown in the laboratory were larger than those from field populations.

The relative preference of M. eugeniae for high salinities was evident in this study, as the maximum longevities and survival times were recorded with the two highest salinities. Moina eugeniae is a relatively long-lived species that can live around 29 days, similar to M. hutchinsoni reared in similar temperature and feeding conditions (Martinez Jeronimo et al., 2004). In contrast, in bioassays with salinities between 2 and 50 g/L, M. mongolica showed maximum longevities close to 14 days (He et al., 2001), while specimens of M. macrocopa lived an average of 12.7 days with 0 salinity (Yuslan et al., 2021).

The number of total moults of M. eugeniae, which is closely related to the longevity of the specimens, was higher at intermediate salinity levels. A comparison with other salinities showed that the number of moults at 7 g/L was lower, which along with the lower survival and longevity found at this concentration, indicates that lower salinity places greater stress on this species.

At the lowest salinities, M. eugeniae reached reproductive maturity in seven days, while at the highest it took nine days, which differed from M. mongolica, M. macrocopa, and M. hutchinsoni, which reach maturity quicker (4.7, 4.33 and from 4.6 to 6.1 days, respectively) at optimal salinities (He et al., 2001; Yuslan et al, 2021; Martinez Jeronimo et al., 2004). The comparison of the three species revealed a different influence of salinity on the moment of first reproduction. In M. eugeniae, it occurred quicker at lower salinities, similar to M. macrocopa (Yuslan et al., 2021) but different from M. mongolica, which reaches maturity more quickly at high salinities, from 6.8 days at 10 g/L to 4.7 days at 40 g/L salinity (He et al., 2001). At intermediate salinity, M. eugeniae reached reproductive maturity after two moults, but at both the lowest and highest salinities three moults were required before the first reproduction.

Intermediate salinity (17 g/L) seemed to be optimal for the reproduction of M. eugeniae females, resulting in the larger number of clutches and total offspring per female reflected by higher net reproduction rate (R ₀). Although the increase in salinity affects the reproduction of M. eugeniae, shown by the lower net reproductive rate, the lower salinity also seems to be detrimental. This partly contrasts with what was found in other moinids as M. mongolica and M. macrocopa, or in the daphnids Daphniopsis australis (Sergeev and Williams, 1985), Daphnia magna Straus, 1820, and Daphnia menucoensis Paggi, 1996, whose reproduction is only limited by increased salinity (He et al., 2001; Martinez-Jeronimo and Martinez-Jeronimo, 2007; Ismail et al., 2011; Yuslan et al., 2021; Vignatti et al., 2022). The fecundity of M. eugeniae, between three to eight clutches and 42-135 total offspring per female according to the treatments, differs strongly from that of M. mongolica and M. macrocopa. At salinities similar to those used in this study, M. mongolica females produced a maximum of four clutches and 38-42 eggs throughout their lives (He et al., 2001), while M. macrocopa produced a maximum of 29.58 offspring (Yuslan et al., 2021). It should be noted that these parameters depend on the longevity of the species, so the greater number of clutches and offspring of M. eugeniae may be due to the fact that its longevity is more than double that of M. mongolica and M. macrocopa. These reproductive parameters of M. eugeniae are similar to those of M. hutchinsoni, a species that, in bioassays in which it was fed and kept at a temperature similar to that used in our study, produced a maximum number of clutches relatively similar to those of M. eugeniae and a mean progeny of 136.7 offspring (Martinez Jeronimo et al., 2004). However, it should be noted that in the bioassays with M. hutchinsoni, the salinity was 5 g/L (Martinez Jeronimo et al., 2004), in comparison to the 17 g/L used with M. eugeniae, which would indicate the greater halotolerance of the latter species.

At an intermediate salinity level, M. eugeniae females produced the first clutch of offspring when they were smaller than in the other salinity treatments. As the size was related to the number of moults prior to maturity (only two at 17 g/L and three at 7 and 27 g/L), this could indicate that both the lowest and highest salinity produce a certain delay in maturity. Similarly, the 17 g/L specimens reached a larger maximum size. However, it must be considered that due to their greater average longevity, they moulted more times (12 moults for some specimens). It is noteworthy that while the longevity and maximum size of the females in the 27 g/L treatments were lower, one female lived 43 days and moulted 15 times, although its maximum size was not as large as that of the females in the treatments with a salinity of 17 g/L. This is due to the fact that until day 13-15, the daily growth rate was relatively similar in the three treatments, but it later stabilised in the treatments at 7 and 27 g/L, whereas at 17 g/L it increased until the death of the specimens. The smaller sizes found at the lowest and highest salinities could be due to the greater amount of energy required for osmoregulation at these salinities, energy that is taken away from growth.

The calculated values of the natural rate of population increase (r) were relatively high at 7 and 17 g/L, and considerably lower at higher salinity, which would indicate slower population growth with higher salt concentrations. This coincides with what was recorded for D. australis, a typical species of ephemeral saline lakes in southeastern Australia, in which the highest increase rate was recorded at the intermediate salinity used in the experiments (22 g/L) (Ismail et al., 2011) and in D. magna, whose reproductive rate decreases markedly with increasing salinity (Martinez-Jeronimo and Martinez-Jeronimo, 2007). However, they are lower than those determined for Cerodaphnia dubia Richard, 1894 and Ceriodaphnia silvestrii Daday, 1902, which, also in experimental situations, showed rates close to double (Fonseca and Rocha, 2004) those of M. eugeniae at the lowest salinities.

The highest clutches and offspring number and maximum size of M. eugeniae at 17 g/L observed in this study, indicates that changes in the salinity of aquatic ecosystems of Central Argentina due to the effects of climate change could have negative effects on the reproduction of this species (Pinceel et al., 2018; Jeppesen et al., 2020). Most climate models indicate an increase in precipitation, temperatures, and frequency of extreme events in this region (Maenza et al., 2017; Tengroth and Geraldi, 2022). These changes could lead to decreases in salinity due to increases in the level of some lakes, which probably does not represent a severe risk for M. eugeniae. However, the increase in salinity due to evaporation during dry periods could alter several biological parameters (Huang et al., 2022), such as osmoregulation (Aladin and Potts, 1996), feeding activity (Achuthankutty et al., 2000), hormonal secretion (Boeuf and Payan, 2001), the cellular content of carbohydrates, fatty acids, and amino acids (Garreta-Lara et al., 2018; Rasdi et al., 2019) or the viability of its resting eggs (Lopatina et al., 2021). The probable changes in climatic factors could affect the current geographic distribution of M. eugeniae, causing it to disappear from some lakes in which it currently lives, leading to local extinctions (Wiens, 2016; Reid et al., 2019) caused either by increased salinity or, conversely, allowing it to colonize some lakes whose salinity increases until reaching the optimal threshold for M. eugeniae.

ACKNOWLEDGMENTS

Two anonymous reviewers and editors are thanked for their suggestions that allowed us to improve the manuscript.

REFERENCES

• Achuthankutty, C; Shrivastava, Y; Mahambre, G; Goswami, S and Madhupratap, M. 2000. Parthenogenetic reproduction of Diaphanosoma celebensis (Crustacea: Cladocera): influence of salinity on feeding, survival, growth and neonate production. Marine Biology, 137(1): 19-22. https://www.doi.org/10.1007/s002270000322
  » https://www.doi.org/10.1007/s002270000322
• Adamowicz S; Hebert P and Marinone MC 2004. Species diversity and endemism in the Daphnia of Argentina: a genetic investigation. Zoological Journal of the Linnean Society, (140): 171-205. https://doi.org/10.1111/j.1096-3642.2003.00089.x
  » https://doi.org/10.1111/j.1096-3642.2003.00089.x
• Aladin N and Potts W 1996. The osmoregulatory capacity of the Ostracoda. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology, 166(3): 215-222. https://www.doi.org/10.1007/BF00263985
  » https://www.doi.org/10.1007/BF00263985
• Alonso M 2010. Branchiopoda and Copepoda (Crustacea) in Mongolian saline lakes. Mongolian Journal of Biological Sciences, 8(1): 9-16. http://dx.doi.org/10.22353/mjbs.2010.08.02
  » http://dx.doi.org/10.22353/mjbs.2010.08.02
• Alva-Martínez A; Sarma SSS and Nandini S 2004. Population growth of Daphnia pulex (Cladocera) on a mixed diet (Microcystis aeruginosa with Chlorella or Scenedesmus). Crustaceana, 77(8): 973-988. https://doi.org/10.1163/1568540042781720
  » https://doi.org/10.1163/1568540042781720
• Amarouayache M; Derbal F and Kara M 2012. Note on the carcinological fauna associated with Artemia salina (Branchiopoda, Anostraca) from Sebkha Ez-Zemoul (Northeast Algeria). Crustaceana, 85(2): 129-137. https://www.doi.org/10.1163/156854012X623728
  » https://www.doi.org/10.1163/156854012X623728
• Battistoni P 1998. Copepoda. p. 519-530. In: Coscarón S and Morrone J (Eds.), Biodiversidad de Artrópodos Argentinos. Ediciones Sur, La Plata.
• Benider A; Tifnouti A and Pourriot R 2002. Growth of Moina macrocopa (Straus 1820) (Crustacea, Cladocera): influence of trophic conditions, population density and temperatura. Hydrobiologia, 468: 1-11. https://www.doi.org/10.1023/A:1015214530485
  » https://www.doi.org/10.1023/A:1015214530485
• Boeuf G and Payan P 2001. Does salinity have an influence on fish growth? Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 130: 411-423. https://www.doi.org/10.1016/ S1532-0456(01)00268-X
  » https://www.doi.org/10.1016/ S1532-0456(01)00268-X
• Boxshall G and Defaye D 2008. Global diversity of copepods (Crustacea: Copepoda) in freshwater. Hydrobiologia, 595: 195-207. https://www.doi.org/10.1007/s10750-007-9014-4
  » https://www.doi.org/10.1007/s10750-007-9014-4
• Cabrera G; Vignatti A and Echaniz S 2014. Acute effects of NaCl and Na₂SO₄ on Daphnia menucoensis Paggi, 1996 and Moina eugeniae Olivier, 1954 (Crustacea, Cladocera). Research in Zoology, 4(1): 8-12. https://www.doi.org/10.5923/j.zoology.20140401.02
  » https://www.doi.org/10.5923/j.zoology.20140401.02
• Echaniz S and Vignatti A 1996. Cladóceros limnéticos de la provincia de La Pampa (Argentina). Revista de la Facultad de Agronomía UNLPam, 9(1): 65-80.
• Echaniz S and Vignatti A 2017. The zooplankton of the shallow lakes of the semi-arid region of southern South America. Annales de Limnologie - International Journal of Limnology, 53: 345-360. https://www.doi.org/10.1051/limn/2017018
  » https://www.doi.org/10.1051/limn/2017018
• Echaniz S and Vignatti A 2019. Limnology of shallow lakes of the semi-arid Central Pampa of Argentina. Acta Limnologica Brasiliensia, 31: e11. https://doi.org/10.1590/S2179-975X4817
  » https://doi.org/10.1590/S2179-975X4817
• Echaniz S ; Cabrera G ; Aliaga P and Vignatti A . 2013. Variations in zooplankton and limnological parameters in a saline lake of La Pampa, Central Argentina, during an annual cycle. International Journal of Ecosystem, 3(4): 72-81. https://www.doi.org/10.5923/j.ije.20130304.03
  » https://www.doi.org/10.5923/j.ije.20130304.03
• Echaniz S ; Cabrera G and Vignatti A 2015. The ecology of the saline lakes in the semiarid Pampa central (Argentina): limnological characterization and zooplankton of Utracán. Advances in Life Sciences, 5(3): 64-72. https://www.doi.org/10.5923/j.als.20150503.03
  » https://www.doi.org/10.5923/j.als.20150503.03
• Fonseca A and Rocha O 2004. The life-cycle of Ceriodaphnia silvestrii Daday, 1902, a Neotropical endemic species (Crustacea, Cladocera, Daphnidae). Acta Limnologica Brasiliensia , 16(4): 319-328. https://www.actalb.org/article/627b1138782aad05cd1891d7/pdf/alb-16-4-319.pdf
  » https://www.actalb.org/article/627b1138782aad05cd1891d7/pdf/alb-16-4-319.pdf
• Forró L; Korovchinsky N; Kotov A and Petrusek A 2008. Global diversity of cladocerans (Cladocera; Crustacea) in freshwater. Hydrobiologia, 595: 177-184. https://www.doi.org/10.1007/s10750-007-9013-5
  » https://www.doi.org/10.1007/s10750-007-9013-5
• Garreta-Lara E; Campos B; Barata C; Lacorte S and Tauler R 2018. Combined effects of salinity, temperatures and hypoxia on Daphnia metabolism. Science of the Total Environment, 601-612. https://www.doi.org/10.1016/j.scitotenv.2017.05.190
  » https://www.doi.org/10.1016/j.scitotenv.2017.05.190
• Ghazy M; Habashy M; Kossa F and Mohammady E 2009. Effects of salinity on survival, growth and reproduction of the water flea, Daphnia magna Nature and Science, 7(11): 28-42. https://www.sciencepub.net/nature/ns0711/05_1173_Salinity_ns0711.pdf
  » https://www.sciencepub.net/nature/ns0711/05_1173_Salinity_ns0711.pdf
• Goulden C 1968. The systematics and evolution of the Moinidae. Transactions of the American Philosophical Society, 58(6): 1-101. https://doi.org/10.2307/1006102
  » https://doi.org/10.2307/1006102
• Hammer Ø; Harper D and Ryan P 2001. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 4(1): 1-9. https://palaeo-electronica.org/2001_1/past/past.pdf
  » https://palaeo-electronica.org/2001_1/past/past.pdf
• Hammer U 1986. Saline Lake Ecosystems of the World. Monographiae Biologicae 59. Dordrecht, Dr. W. Junk Publishers, xi+616p . https://link.springer.com/book/9789061935353
  » https://link.springer.com/book/9789061935353
• He Z; Qin J; Wang Y; Jiang H and Wen Z 2001. Biology of Moina mongolica (Moinidae, Cladocera) and perspective as live food for marine fish larvae: review. Hydrobiologia, 457: 25-37. https://www.doi.org/10.1023/A:1012277328391
  » https://www.doi.org/10.1023/A:1012277328391
• Hobæk A; Manca M and Andersen T 2002. Factors influencing species richness in lacustrine zooplankton. Acta Oecologica, 23: 155-163. https://www.doi.org/10.1016/S1146-609X(02)01147-5
  » https://www.doi.org/10.1016/S1146-609X(02)01147-5
• Huang J; Li Y; Sun Y; Zhang L; Lyu K and Yang Z 2022. Size-specific sensitivity of cladocerans to freshwater salinization: Evidences from the changes in life history and population dynamics. Environmental Pollution, 296: 118770. https://www.doi.org/10.1016/j.envpol.2021.118770
  » https://www.doi.org/10.1016/j.envpol.2021.118770
• Ismail H; Qin J and Seuront L 2011. Regulation of life history in the brackish cladoceran, Daphniopsis australis (Sergeev and Williams, 1985) by temperature and salinity. Journal of Plankton Research, 33(5): 763-777. https://doi.org/10.1093/plankt/fbq145
  » https://doi.org/10.1093/plankt/fbq145
• Jeppesen E; Beklioğlu M; Özkan K and Akyürek Z 2020. Salinization increase due to climate change will have substantial negative effects on inland waters: a call for multifaceted research at the local and global scale. The Innovation, 1(2): 100030. https://www.doi.org/10.1016/j.xinn.2020.100030
  » https://www.doi.org/10.1016/j.xinn.2020.100030
• Jiménez D; Rosas J; Velasquez A; Millan J and Cabrera T 2003. Crecimiento poblacional y algunos aspectos biológicos del cladocero Moina macrocopa (Straus, 1820) (Branchiopoda, Anomopoda), alimentado con tres dietas en tres salinidades diferentes. Ciencia, 11(1): 22-30. https://produccioncientificaluz.org/index.php/ciencia/article/view/9145/9134
  » https://produccioncientificaluz.org/index.php/ciencia/article/view/9145/9134
• José de Paggi S; Marinone MC; Küppers G; Claps MC and Paggi J 2023. Taxonomic diversity of the freshwater zooplankton in Argentina: A review. Limnologica, 100: 126029. https://www.doi.org/10.1016/j.limno.2022.126029
  » https://www.doi.org/10.1016/j.limno.2022.126029
• Lopatina T; Anishchenko O; Oskina N and Zadereev E 2021. Threshold concentrations of the road salt for adverse effects on females and resting eggs of cladoceran Moina macrocopa Aquatic Ecology, 55: 283-297. https://www.doi.org/10.1007/s10452-021-09830-z
  » https://www.doi.org/10.1007/s10452-021-09830-z
• Maenza R; Agosta E and Bettolli M 2017. Climate change and precipitation variability over the western ‘Pampas’ in Argentina. International Journal of Climatology, 37(51): 445-463. https://doi.org/10.1002/joc.5014
  » https://doi.org/10.1002/joc.5014
• Martínez-Jeronimo F and Espinosa-Chavez F 2005. Notes on the reproduction and survival of Moina hutchinsoni Brehm, 1937 (Moinidae: Anomopoda) grown in media of varying salinity. Aquatic Ecology , 39(1): 113-118. https://www.doi.org/10.1007/s10452-004-3118-y
  » https://www.doi.org/10.1007/s10452-004-3118-y
• Martinez-Jeronimo F; Elias-Gutierrez M and Suarez-Morales E 2004. A redescription of Moina hutchinsoni, a rare cladoceran (Branchiopoda: Anomopoda) found in remnants of a Mexican Saline Lake, with notes on its life history. Journal of Crustacean Biology, 24(2): 232-245. https://doi.org/10.1651/C-2450
  » https://doi.org/10.1651/C-2450
• Martinez-Jeronimo F and Martinez-Jeronimo L 2007. Chronic effect of NaCl salinity on a freshwater strain of Daphnia magna Straus (Crustacea: Cladocera): A demographic study. Ecotoxicology and Environmental Safety, 67: 411-416. https://doi.org/10.1016/j.ecoenv.2006.08.009
  » https://doi.org/10.1016/j.ecoenv.2006.08.009
• Menu-Marque S; Morrone J and Locascio de Mitrovich C 2000. Distributional patterns of the South American species of Boeckella (Copepoda: Centropagidae): a track analysis. Journal of Crustacean Biology, 20(2): 262-272. https://doi.org/10.1163/20021975-99990038
  » https://doi.org/10.1163/20021975-99990038
• Nandini S and Sarma S 2003. Population growth of some genera of cladocerans (Cladocera) in relation to algal food (Chlorella vulgaris) levels. Hydrobiologia, 491(1-3): 211-219. https://www.doi.org/10.1023/A:1024410314313
  » https://www.doi.org/10.1023/A:1024410314313
• Nandini S and Sarma S 2019. Reproductive strategies of Moina (Cladocera) in relation to their habitat. Limnetica, 38(1): 137-145. https://www.doi.org/10.23818/limn.38.15
  » https://www.doi.org/10.23818/limn.38.15
• Nédli J; De Meester L; Major A; Schwenk K; Szivák I and Forró L 2014. Salinity and depth as structuring factors of cryptic divergence in Moina brachiata (Crustacea: Cladocera). Fundamental and Applied Limnology, 184: 69-85. https://www.doi.org/10.1127/1863-9135/2014/0462
  » https://www.doi.org/10.1127/1863-9135/2014/0462
• Neretina A; Kirdyasheva A and Kotov A 2020. Position of Moina wierzejskii Richard, 1895 (Crustacea: Cladocera) within the genus Moina Baird, 1850 in the light of new morphological data. Zootaxa, 4820(3): 506-522. https://www.doi.org/10.11646/zootaxa.4820.3.5
  » https://www.doi.org/10.11646/zootaxa.4820.3.5
• Olivier SR 1954. Una nueva especie del género Moina Notas del Museo de Ciencias Naturales de La Plata, Sección Zoología, 17(148): 81-86.
• Paggi J 1998. Cladocera (Anomopoda y Ctenopoda). p. 507-518. In: Coscarón S and Morrone S (Eds.), Biodiversidad de Artrópodos Argentinos. La Plata, Ediciones Sur.
• Pinceel T; Buschke F; Weckx M; Brendonck L and Vanschoenwinke B 2018. Climate change jeopardizes the persistence of freshwater zooplankton by reducing both habitat suitability and demographic resilience. BMC Ecology, 18: 2. https://www.doi.org/10.1186/s12898-018-0158-z
  » https://www.doi.org/10.1186/s12898-018-0158-z
• Rasdi N; Suhaimi H; Hagiwara A; Ikhwanuddin M; Ghaffar M; Yuslan A and Najuwa S 2019. Effect of different salinities gradient on fatty acid composition, growth, survival and reproductive performance of Moina macrocopa (Straus 1820) (Crustacea, Cladocera). Preprints, 2019060205. https://www.doi.org/10.20944/preprints201906.0205.v1
  » https://www.doi.org/10.20944/preprints201906.0205.v1
• Reid, A; Carlson, A; Creed, I; Eliason, E; Gell, P; Johnson, P; Kidd, K; MacCormack, T; Olden, J; Ormerod, S; Smol, J; Taylor, W; Tockner, K; Vermaire, J; Dudgeon, D and Cooke, J. 2019. Emerging threats and persistent conservation challenges for freshwater biodiversity. Biological Reviews, 94: 849-873. https://www.doi.org/10.1111/brv.12480
  » https://www.doi.org/10.1111/brv.12480
• Rokneddine A 2004. The effects of salinity and temperature on the growth and reproduction of Moina salina Daday, 1888 (Branchiopoda, Moinidae), Crustaceana, 77(7): 805-824. https://www.doi.org/10.1163/156854004774248690
  » https://www.doi.org/10.1163/156854004774248690
• Russian G; Agosta E and Compagnucci R 2015. Variaciones en baja frecuencia de la precipitación estacional en la región pampa amarilla y posibles forzantes. Meteorologica, 40(1): 17-42. https://repositorio.uca.edu.ar/handle/123456789/5446
  » https://repositorio.uca.edu.ar/handle/123456789/5446
• Santangelo J; Bozelli R; Rocha A and Esteves F 2008. Effects of slight salinity increases on Moina micrura (Cladocera) populations: field and laboratory observations. Marine and Freshwater Research, 59(9): 808-816. https://www.doi.org/10.1071/MF08026
  » https://www.doi.org/10.1071/MF08026
• Sokal R and Rohlf F. 1995. Biometría. Principios y métodos estadísticos en la investigación biológica. Barcelona, Ed. Blume.
• Tengroth C and Geraldi A 2022. Assessment of climate change and prospective analysis on shallow lakes, Las Encadenadas del Oeste watershed, Buenos Aires - Argentina. Investigaciones Geográficas, 77: 221-237. https://doi.org/10.14198/INGEO.18640
  » https://doi.org/10.14198/INGEO.18640
• Viglizzo E 2010. El agro, el clima y el agua en La Pampa Semiárida: Revisando paradigmas. Anales de la Academia Nacional de Agronomía y Veterinaria, LXIV: 251-267. http://sedici.unlp.edu.ar/bitstream/handle/10915/27600/Documento_completo.pdf?sequence=1&isAllowed=y
  » http://sedici.unlp.edu.ar/bitstream/handle/10915/27600/Documento_completo.pdf?sequence=1&isAllowed=y
• Vignatti A ; Echaniz S and Martín MC 2007. El zooplancton de lagos someros de diferente salinidad y estado trófico en la región semiárida pampeana (La Pampa, Argentina). Gayana, 71(1): 38-48. https://dialnet.unirioja.es/servlet/articulo?codigo=9448272&orden=0&info=link
  » https://dialnet.unirioja.es/servlet/articulo?codigo=9448272&orden=0&info=link
• Vignatti A ; Cabrera G ; and Echaniz S 2012a. Changes in the zooplankton and limnological variables of a temporary hypo-mesosaline wetland of the central region of Argentina during the drying. Pan American Journal of Aquatic Sciences, 7(2): 93-106. http://panamjas.org/pdf_artigos/PANAMJAS_7(2)_93-106.pdf
  » http://panamjas.org/pdf_artigos/PANAMJAS_7(2)_93-106.pdf
• Vignatti A ; Festa R; Cabrera G and Echaniz S 2012b. Comparación luego de una década de parámetros limnológicos, riqueza y abundancia del zooplancton de una laguna salina de la provincia de La Pampa. BioScriba, 5(1): 23-35. https://www.researchgate.net/publication/294873032
  » https://www.researchgate.net/publication/294873032
• Vignatti A ; Paggi J C; Echaniz S and Cabrera G 2012c. Tolerancia a la salinidad de dos cladóceros halófilos autóctonos: Daphnia menucoensis y Moina eugeniae (Arthropoda, Crustacea). Biología Acuática, 27: 219-231. https://revistas.unlp.edu.ar/bacuatica/article/view/6632/6357
  » https://revistas.unlp.edu.ar/bacuatica/article/view/6632/6357
• Vignatti A ; Cabrera G and Echaniz S 2014. Determination of the optimal culture medium and salts for bioassays with neotropical halophilic cladocerans. American Journal of Life Sciences, 2(2): 40-45. https://www.doi.org/10.11648/j.ajls.20140202.11
  » https://www.doi.org/10.11648/j.ajls.20140202.11
• Vignatti A ; Canosa M; Cabrera G and Echaniz S 2017. The ecology of saline lakes in central Argentina: Environmental and zooplankton changes during the drying of a temporary shallow ecosystem. Unversitas Scientiarum, 22(3): 177-200. https://www.doi.org/10.11144/Javeriana.SC22-3.eazp
  » https://www.doi.org/10.11144/Javeriana.SC22-3.eazp
• Vignatti A ; Echaniz S and Cabrera G 2022. Effects of salinity and temperature on the biology of Daphnia menucoensis Paggi, 1996 (Crustacea, Cladocera). Marine and Freshwater Behaviour and Physiology, 55(1-2): 21-33. https://doi.org/10.1080/10236244.2022.2047965
  » https://doi.org/10.1080/10236244.2022.2047965
• Wiens J 2016. Climate-related local extinctions are already widespread among plant and animal species. PLOS Biology, 14(12): e2001104. https://www.doi.org/10.1371/journal.pbio.2001104
  » https://www.doi.org/10.1371/journal.pbio.2001104
• Yuslan A ; Najuwa S ; Hagiwara A ; Ghaffar M ; Suhaimi H and Rasdi N 2021. Production performance of Moina macrocopa (Straus 1820) (Crustacea, Cladocera) cultured in different salinities: the effect on growth, survival, reproduction, and fatty acid composition of the neonates. Diversity, 13: 105. https://doi.org/10.3390/d13030105
  » https://doi.org/10.3390/d13030105
• Zar JH 1996. Biostatistical analysis. Upper Saddle River, Prentice Hall, 662p.
• Zhao W; Yu B; Wang T and Song L 2006. Adaptability of Moina affinis (Crustacea: Cladocera: Moinidae) to seawater salinity. Chinese Journal of Applied Ecology, 17(8): 1521-1525. [In Chinese, with English abstrac] https://www.cje.net.cn/EN/abstract/abstract1108.shtml#1
  » https://www.cje.net.cn/EN/abstract/abstract1108.shtml#1

• Zoobank:
  http://zoobank.org/urn:lsid:zoobank.org:pub:53361C4C-5E42-4BF5-AD50-22622314E6B2

Additional Information and Declarations

• Consent for publication
  All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document.
• Data availability
  All study data are included in the article.
• Funding and grant disclosures
  There were no external funding sources for this study.

Edited by

• Associate Editor:
  Lourdes Elmoor Loureiro

• Editor-in-chief
  Christopher Tudge

Data availability

All study data are included in the article.

Publication Dates

• Publication in this collection
  08 Sept 2025
• Date of issue
  2025

History

• Received
  07 Feb 2024
• Accepted
  12 Aug 2024