Osmoregulation and salinity tolerance in two species of bivalve mollusc: Limnoperna fortunei and Mytilopsis leucophaeta

doi:10.1016/0022-0981(89)90158-5

Journal of Experimental Marine Biology and Ecology

Volume 133, Issues 1–2, 14 December 1989, Pages 67-79

https://doi.org/10.1016/0022-0981(89)90158-5 Get rights and content

Abstract

This paper reports on salinity tolerance and osmotic regulation in two bivalve molluscs: Mytilopsis leucophaeta Conrad, an oligohaline species (subclass Heterodonta) and Limnoperna fortunei Dunker, a freshwater species (subclass Pteriomorphia). The range of osmolality tolerated by Mytilopsis is 5–400 mOsm. Limnoperna survives in deionized water and in osmolalities of ≤400 mOsm. Both species are osmotic and ionic conformers in media with concentrations of > 70 mOsm; at lower ambient osmolalities, both are hyperosmotic regulators. The major hemolymph ions are Na⁺ and Cl⁻; acclimation to dilute media results in hypercalemia in both species. The amino acid content of Mytilopsis soft tissues is 182 μmol · g⁻¹ dry wt in animals acclimated to 10 mOsm. The tissue levels of amino acids increase to 405 μmol · g⁻¹ in Mytilopsis acclimated to 400 mOsm. The free amino acid content of Limnoperna mantle tissue is 9.6 μmol · g⁻¹ dry wt in animals acclimated to 10 mOsm and increases to 35 μmol · g⁻¹ in animals acclimated to 200 mOsm. The differences in osmoregulatory behavior between the two species appear to be quantitative rather than qualitative, despite the phyletic distance between them.

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Cited by (44)

An invasive mussel is in trouble: How do glyphosate, 2,4-D and its mixture affect Limnoperna fortuneiʹs survival?
2021, Aquatic Toxicology
Citation Excerpt :
The species has been reported to reach high densities in natural environments (150,000 ind. m–2) as well as in invaded areas (Darrigran and Pastorino 2004). Golden mussels are able to colonize soft-water habitats, heated waters, and organically-enriched waters (Morton 1977; Deaton et al. 1989; Darrigran and Pastorino 1995). Due to their high filtering capacity, they act as ecosystem engineers (Sylvester et al. 2005) that can alter the abundance and composition of plankton (Cataldo and Boltovskoy 2000), modify trophic interactions and food availability of benthic and pelagic species, increase the depth of the photic zone, thus favoring macrophytic growth (Boltovskoy et al. 2009), and affect oxygen availability and rates of sedimentation and nutrient recycling (Karatayev et al. 2007).
Contamination and biological invasions are important factors that alter the functioning of freshwater systems. We carried out two experiments involving daily measurements of dissolved oxygen (DO) and Limnoperna fortunei mortality: 1) the impact of DO on mussel survival mediated by glyphosate, 2,4-D and their mixture was analysed in a 22-day indoor experiment (IE) under controlled conditions using microcosms with L. fortunei, with and without air supply; and 2) the effect of each herbicide and their mixture on mussel accumulated mortality was compared in a 18-day outdoor experiment (OE) using mesocosms without air supply, with and without L. fortunei. Results showed that glyphosate, alone or mixed affected L. fortunei survival both directly and indirectly. In IE we observed direct toxicity of glyphosate in treatments with air supply, with accumulated mortality of 20.0% for glyphosate and 10.0% for the mixture. In OE, L. fortunei deepened the changes in the patterns of DO fluctuations driven by the herbicides, which led to hypoxia in the system. The accumulated mortality was 46.7, 8.6 and 48.2% for glyphosate, 2,4-D and the mixture, respectively. This study contributes to the understanding of the mechanisms that control the invasion of L. fortunei in freshwater systems influenced by agrochemicals.
Heritability of acute low salinity survival in the Eastern oyster (Crassostrea virginica)
2020, Aquaculture
Citation Excerpt :
This uptake of water creates a problem maintaining cell volumes efficient to sustain normal cell function and maintenance of cellular constituents (Shumway, 1996). Oysters may be able to handle the stress from the large amount of energy required for maintaining FAA pools, ion gradients, and for the uptake of water when osmoconforming to such low salinities for a short period of time (Shumway, 1996; Deaton et al., 1989), but this stress may become overwhelming and eventually detrimental if conditions persist. This threshold of osmotic stress and elevated temperatures may coincide with our observed peak in mortality during 8–14 days of both experimental exposures, where those individuals unable to handle the stress perish.
On the US east coast, Eastern oyster (Crassostrea virginica) aquaculture has grown substantially over the last century. As aquaculture expands into previously unexploited areas, there is a need for oyster lines bred for specific environmental conditions. In the Maryland portion of the Chesapeake Bay, and in other coastal areas, salinity tends to be below optimal for typical aquaculture productivity, and these areas frequently experience periods of acute low salinity following heavy rain events. While these areas may hinder oyster growth, they provide a refuge from common oyster diseases. Selective breeding focusing on survival in acute low salinity conditions could expand areas suitable for aquaculture, but the genetic framework underlying this trait is currently unknown. In this study, we estimated the heritability of survival at acute low salinity (< 3) by conducting two month-long low salinity exposure experiments with fifty half-sibling families. Hemolymph osmolality was analyzed during the first eight days of the second exposure experiment to track osmoconformation behavior and investigate potential physiological differences underlying variation in salinity survival among families. There were significant differences in mortality among families for both low salinity exposure experiments, with the majority of mortality occurring between 8 and 14 days of exposure for both experiments. Higher overall mortality was observed during the second experiment (53% in experiment 2 versus 23% in experiment 1), which was conducted during the summer when animals were reproductively active. Narrow-sense heritability estimates for survival were moderate to high using both a Bayesian (MCMCglmm, h² = 0.34 for experiment 1 and 0.59 for experiment 2) and a likelihood-based (ASReml-R, h² = 0.4 for both experiments) approach, and estimates from ASReml-R appeared to be lower compared to MCMCglmm for experiment 2 (ASReml-R h² = 0.4, MCMCglmm h² = 0.59). Finally, there were no differences in osmolality among families on either sampling day, but all families remained slightly hyperosmotic after salinity was held static at our desired level (2.5). This study provides the first quantitative genetic analysis of acute low salinity survival in C. virginica and results suggest that this trait is heritable and could be selectable in a breeding program.
Osmoionic homeostasis in bivalve mollusks from different osmotic niches: Physiological patterns and evolutionary perspectives
2020, Comparative Biochemistry and Physiology -Part A : Molecular and Integrative Physiology
Citation Excerpt :
The required standard mixtures were obtained using the amino acids taurine, alanine, and glycine. As noted by myriad authors, these three organic osmolytes are usually involved in maintaining the osmotic equilibrium of bivalves (distributed from fresh to sea water), since large amounts of these compounds are found in the FAA pool in different tissues (Babarro et al., 2011; Burg and Ferraris, 2008; Deaton et al., 1989; Fyhn, 1976; Gilles, 1978; Henry et al., 1980; Hosoi et al., 2008; Jordan and Deaton, 1999; Livingstone et al., 1979; Otto and Pierce, 1981; Pierce and Amende, 1981). Taurine, alanine, and glycine ratios in bivalves, respectively, were established from our literature review (see section 2.3.2) as follows: freshwater (60%, 20%, and 20%), estuarine (20%, 60%, and 20%), and marine (70%, 20%, and 10%).
Physiological knowledge gained from questions focused on the challenges faced and strategies recruited by organisms in their habitats assumes fundamental importance about understanding the ability to survive when subjected to unfavorable situations. In the aquatic environment, salinity is particularly recognized as one of the main abiotic factors that affects the physiology of organisms. Although the physiological patterns and challenges imposed by each occupied environment are distinct, they tend to converge to osmotic oscillations. From a comparative perspective, we aimed to characterize the osmoregulatory patterns of the bivalve mollusks Corbicula largillierti (purple Asian cockle), Erodona mactroides (lagoon cockle), and Amarilladesma mactroides (white clam) - inhabitants of different osmotic niches - when submitted to hypo- and/or hyperosmotic salinity variations. We determined the hemolymph osmotic and ionic concentrations, tissue hydration, and the intracellular isosmotic regulation (IIR) from the use of osmolytes (organic and inorganic) after exposure to species-specific salinity intervals. Additionally, we incorporated phylogenetic perspectives to infer and even broaden the understanding about the patterns that comprise the osmoionic physiology of Bivalvia representatives. According to the variables analyzed in the hemolymph, the three species presented a pattern of osmoconformation. Furthermore, both ionic regulation and conformation patterns were observed in freshwater, estuarine, and marine species. The patterns verified experimentally show greater use of inorganic osmolytes compared to the participation of organic molecules, which varied according to the osmotic niche occupied in the IIR for the mantle, adductor muscle, and gills. This finding widens the classic vision about the preferential use of certain osmolytes by animals from distinct niches. Our phylogenetic perspective also indicates that environmental salinity drives physiological trait variations, including hemolymph osmolality and the ion composition of the extracellular fluid (sodium, chloride, magnesium, and calcium). We also highlight the important role played by the shared ancestry, which influences the interspecific variability of the hemolymph K⁺ in selected representatives of Bivalvia.
Prediction of future risk of invasion by Limnoperna fortunei (Dunker, 1857) (Mollusca, Bivalvia, Mytilidae) in Brazil with cellular automata
2018, Ecological Indicators
Citation Excerpt :
In 2015, for example, there was a rupture of a mine tailings dam that released billions of liters of tailings mud from mining activities on the Doce River (southeastern Brazil), which traveled hundreds of kilometers to the sea (e.g., Escobar, 2015; El Bizri et al., 2016; Garcia et al., 2016; Neves et al., 2016; Fernandes et al., 2016). Although golden mussels are relatively tolerant to contaminants, the presence of mud and heavy metals through the river may adversely affect the development of filter-feeding organisms because the increased water turbidity is a detrimental factor for the survival of adults and larvae (Morton, 1975; Deaton et al., 1989; Ricciardi, 1998; Pareschi et al., 2008; Mackie and Claudi, 2010). The model did not take into account the presence of water transposition systems that should be in full operation in 2018 in the northeast Brazil.
In South America, the presence of the non-native mollusc Limnoperna fortunei (Dunker, 1857) (Mollusca, Bivalvia, Mytilidae) in rivers and reservoirs may result in several impacts on the environment and economic activities. In a continental scale, the factors that most influence the dispersion of the species are anthropogenic vectors such as the movement of boats and people. Due to this, distribution models based solely on climatic variables often fail to predict the areas most subject to invasion, both spatially and temporally. An alternative to overcome this problem is the evaluation assuming the phenomenon as a complex system. In this paper, we have used a cellular automata model to predict the spread of the golden mussel in the Brazilian territory, on a temporal and spatial scale. We assume three parameters of interest: a) altitude b) characteristics of the river, and c) human population density. Transition rules were defined based on various considerations discussed in the article. The algorithm estimated satisfactorily the risk of invasion by L. fortunei to date (year of 2016), and the simulations for the years 2030 and 2050 predicted a high risk of invasion in north and northeastern Brazil. The increased risk of invasion predicted by the model for the next decades indicates that prevention and control measures should be applied immediately and this is of the utmost importance for the country to be able to comply with the #9 Aichi target.
Morphological-behavioral adaptations of two benthic invertebrate species to face strong bed hydrodynamic forces in a large South-American river
2014, Ecohydrology and Hydrobiology
Citation Excerpt :
The juvenile organisms of L. fortunei were observed with sand grains attached through the byssal threads, increasing the body weight several times. This species has a gripping system at the end of the byssal named attachment disk (Fig. 3) with which attaches the sand grains (Deaton et al., 1989). Thus, having increased the body weight, this species could disperse by saltation (close to the bottom) along the main channel of large rivers, without be sweep and drift by the prevailing strong currents.
This scientific communication describes and discusses morphological–behavioral adaptations to flow of two benthic invertebrate species to survive in highly turbulent habitats of the large Paraguay River (Argentina – Paraguay). It is based on field and laboratory observations under microscope made during the performance of usual researches. In this sense, we found that Djalmabatista sp. 1 (Chironomidae, Tanypodinae) ballasts its body by ingestion of fine sediment grains which storage into a dorsal bulge, herein called “dorsal bag”. This specie would have the ability to take or release these grains according to the surrounding hydrodynamic conditions. Otherwise, the juvenile stage of Limnoperna fortunei (Bivalvia, Mytilidae) also ballasts its body but attaching sand grains through the byssal threads.
Low salinity stress experienced by larvae does not affect post-metamorphic growth or survival in three calyptraeid gastropods
2011, Journal of Experimental Marine Biology and Ecology
Citation Excerpt :
Similarly, although larvae of C. fecunda were less tolerant of salinity stress than those of C. fornicata, they were also able to recover from a stress at a salinity of 20, although not from a stress at a salinity of 15 (Fig. 8). Survival of organisms in reduced salinity and the immediate effects of low salinity stress on characteristics such as growth rate have been widely studied, especially in estuarine species (e.g., Lance, 1963—copepods; Lyster, 1965—polychaete larvae; Griffith, 1974—killifish; Brand, 1984—phytoplankton; Dunson and Seidel, 1986—reptiles; Deaton et al., 1989—bivalves; Kirst, 1990—algae). Some of the larvae that we tested could not even tolerate a salinity of 15 for 12 h (C. fecunda, Fig. 3B), while those of other species were able to tolerate that same reduction in salinity for 48 h (C. onyx, Fig. 3C), or even a reduction to a salinity of 10 for 48 h (C. fornicata, Fig. 4).
Marine larvae that experience some sub-lethal stresses can show effects from those stresses after metamorphosis, even when they seem to recover from those stresses before metamorphosis. In this study we investigated the short and long-term effects of exposing the larvae of three calyptraeid gastropods (Crepidula fornicata, Crepidula onyx, and Crepipatella fecunda) to temporary reductions in salinity. Larvae of all three species showed slower larval growth rates, longer time to metamorphic competence, and substantial mortality after being stressed in seawater at salinities of 10, 15, and 20 for less than 48 h. Larval tolerance to low salinities varied widely within and among species, but longer stresses at lower salinities were generally more harmful to larvae. However, larvae in nearly all experiments that were able to metamorphose survived and grew normally as juveniles; there were no documented “latent effects.” For all three species, starving larvae in full-strength seawater was not as harmful as exposing larvae to low salinity stress, indicating that detrimental effects on larvae were caused by the salinity stress per se, rather than by an indirect effect of salinity stress on feeding. C. fornicata that were stressed with low salinity as juveniles were more tolerant of the stress than larvae: all stressed juveniles lived and showed reduced growth rates for no more than 3 days. Our data suggest that even though reduced salinity is clearly stressful to the larvae of these 3 gastropod species, metamorphosis seems to generally provide individuals with a fresh start.

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Research articleOsmoregulation and salinity tolerance in two species of bivalve mollusc: Limnoperna fortunei and Mytilopsis leucophaeta

Abstract

The non-marine aquatic Mollusca of Thailand

Arch. Molluskenkd.

Salinity tolerance of some marine bivalves from inshore and estuarine environments in Virginia waters on the western mid-Atlantic coast

Malacologia

Ion regulation in freshwater and brackish water bivalve molluscs

Physiol. Zool.

Uptake of sodium and chloride by freshwater mussels

Can. J. Zool.

The physiological basis of the species abundance-salinity curve: a speculation

Mar. Biol.

A preliminary survey on the fouling organisms in the Ningbo harbor, China

Acta Oceanol. Sin.

The distribution of fouling organisms in Changjiang river estuary

Oceanol. Limnol. Sin.

Research article
Osmoregulation and salinity tolerance in two species of bivalve mollusc: Limnoperna fortunei and Mytilopsis leucophaeta