Respiration of invasive bivalve Anadara kagoshimensis (Tokunaga, 1906) at the 14-days starvation and different oxygen content in sea water

doi:10.21203/rs.3.rs-2084480/v1

Download PDF

Research Article

Respiration of invasive bivalve Anadara kagoshimensis (Tokunaga, 1906) at the 14-days starvation and different oxygen content in sea water

https://doi.org/10.21203/rs.3.rs-2084480/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

In the present work the influence of oxygen content in sea water and 14-days starvation on respiration rate of the bivalve species, Anadara kagoshimensis (Tokunaga, 1906), has been studied. The blood clams with shell height 25-30 mm have been used for experiments. Respiration rate varied in the wide range, from maximal value 89.9 mgO₂·l^-1 (at 100% saturation) to 5.0 µgО₂·h^-1·gww^-1 (at 76% saturation) at the salinity 17-18 psu and temperature 18°C. The oxygen consumption of the blood clam was substantially lower compared to other benthic bivalves. Our results suggest the ability of A.kagoshimensis to rapidly transition from aerobic to anaerobic metabolism under conditions that are not critical for them.

Two-weeks starvation led to an increase in respiration rates of the blood clam A. kagoshimensis, which indicates an intensification of oxidative processes of organism by 35 ˗ 55%. The article discusses metabolic processes that require increased oxygen consumption.

alien

blood clam

Anadara kagoshimensis

starvation

respiration

Anadara kagoshimensis, a bivalve alien species, which has been relatively recently observed in the Black Sea region, is widely distributed in the Indian and the Pacific Ocean. The species has been registered in 1969 in Europe (the Adriatic Sea), and in 1980 in the Black Sea (Crocetta, 2012; Revkov, 2016; Strafella et al., 2017). In the earliest works, the species was referred as Scapharca inaequivalvis (Bruguière, 1789), then the taxonomy has been changed to Anadara inaequivalvis, and, finally, the genetic analysis conducted in 2014 allowed to determine the correct species name of the bivalve observed in the Black Sea,

Anadara kagoshimensis (Krapal et al., 2014). The high morphological and genetic similarity between A. kagoshimensis (Tokunaga, 1906) from the Japanese Sea and A. inaequivalvis (Bruguière, 1789), inhabiting the Black Sea, has finally confirmed the taxonomy of the alien bivalve.

Mass settlements of the blood clam larvae are found on water technical facilities, collectors on mussel farms; adult blood clams occur even in river estuaries. A. kagoshimensis possesses salinity and temperature tolerance, and survives under hypoxia and anoxia. Hemocytes of three morphotypes circulating in hemolymph contain hemoglobin and, therefore, are characterized with high oxygen-carrying capacity in contrast to other benthic bivalves (De Zwaan et al., 2002, Xu et al., 2015; Kladchenko et al., 2020). The unique functional, physiological and biochemical features found in soft tissues of blood clam reveal its great potential for research.

Starvation is commonly defined as an absence or deficiency of nutrients in the organism’s diet, which are necessary to restore metabolic costs. Short-term periodic starvation is normal for benthic bivalves. Some authors suggested that mollusks may control processes of food consumption and limit the diet, staying “semi-starved” even during periods of maximal phytoplankton supply. During prolonged food absence the specific adaptive processes are activated, which are aimed to decrease metabolic rate and to enhance alternative pathways for energy production (Bayne, 1973; Liu et al., 2010; Riisgård & Larsen, 2015). All catabolic processes, in this case, are frequently associated with anaerobic metabolism (Bayne et al., 1978; Sadok et al., 1999). The respiration rate (RR) is one of the main parameters characterizing the energy metabolism in aquatic organisms. Changes in RR allow to evaluate the intensity and direction of anabolic and catabolic processes in bivalve mollusks.

The ability to survive during starvation periods is considered an important feature for invasive species of bivalve mollusks and is likely associated with bivalves’ invasiveness. Despite that, relatively little attention has been paid to investigation of the tolerance to food deficiency in alien mollusks, such as A. kagoshimensis, in natural ecosystems and/or under or laboratory conditions. Moreover, fundamental studies are needed to investigate the physiological mechanisms underlying unique tolerance of the mollusks and to evaluate its adaptive potential to natural fluctuations of food availability.

The few works on the study of this species of invasive mollusks indicate the need to continue the study of its physiology and biology. Previous studies have shown a closed positive correlation between the intensity of respiration in blood clams and temperature and body weight of mollusks (Zhavoronkova & Zolotnitsky, 2017; Zhavoronkova et al., 2018). Anadara kagoshimensis is a bottom-burrowing species that faces changing environmental conditions, including changes in oxygen content.

The aim of the present work is to characterize the level of energy metabolism of the bivalve species, A. kagoshimensis, at normal and changed oxygen content in sea water, and the two-weeks starvation period, as well as to determine the intensity and the direction of metabolic adaptive responses to food shortages.

2.1. Respiration rate of blood clams under different oxygen regimes

Specimens of A. kagoshimensis (shell height 25–30 mm) were collected from the coastal area of the Black Sea and delivered to the laboratory. Clams were cleaned of fouling and placed in aerated tanks equipped with flowing filtered seawater system (filter diameter 1.27 µm). The respiration rate (RR) was evaluated after 24 hours of the adaptation period. The parameter was recorded for 3 h using the of closed chamber method (volume of chamber was 450–500 ml) and expressed as µgО₂·h^-1·g^-1 wet weight. Oxygen concentration was determined using standard ion-selective Clark’s electrodes and flowing oxygen meter Anion-7041. RR of clams was estimated using the following equation: RR = [(DOCo - DOt)/T/WW, where DOCo and DOCt are dissolved oxygen content of the chamber with animals at the beginning and the end of the experiment, respectively; T is the period of the experiment (hours); WW is the whole weight of individual (g). The initial oxygen concentrations of 8.55 mgO₂·l^-1 (saturation) and following declines were obtained via N₂ -bubbling of the seawater. After each measurement, the oxygen concentration in the chamber was gradually increased to saturation level in 2 h by air bubbling. All experiments were carried at 18°C.

2.2. The 14-days starvation modeling

After the period of acclimation to laboratory conditions, the blood clams A. kagoshimensis were randomly divided into two groups containing 7 individuals. The first (control) group was daily fed with 150–200 ml of concentrated microalgae mixture containing Isochrysis galbana and Tetraselmis suecica (algae concentration 6.5·10⁶ cells·ml^− 1). The control group was fed microalgae at concentrations sufficient to support normal vital activity of the clams, but there was no weight growth that could affect the rate of oxygen consumption. The second (experimental) group did not receive food and was referred to as conventionally “starved”. The intensity of RR of A. kagoshimensis was determined at 1, 3, 9, and 14 days of experimental period and expressed as µgО₂·h^− 1·gww^− 1. Total weight of blood clams and survival rate were measured at same time.

Statistical and graphical data processing was done using STATISTICA 8.0 software (StatSoft, 2007). All results are expressed as Mean ± SD.

3.1. Respiration rate of A. kagoshimensis

Oxygen content (100% saturation) in seawater was approximately 8.55 mgO₂·l^− 1 at the salinity level 17–18 psu and temperature 18°C. Respiration rate varied in the wide range, from maximal value 89.9 mgO₂·l^− 1 to 5.0 µgО₂·h^− 1·gww^− 1 at different oxygen concentration. The low RR of A. kagoshimensis (5.0-7.7 µgО₂·h^− 1·gww^− 1) obtained in our experiments at 6.7-7.0 mgO₂·l^− 1 was unexpected. The drop in respiratory rate was more than 94% with a decrease in oxygen content of less than 25%. The RR level was strongly correlated with dissolved oxygen concentration, RR = DOC^11.964·10^− 7, R² = 0.95 (P < 0.05) (Fig. 1). The survival rates of A. kagoshimensis exposed in experimental conditions were 100%.

3.2. Comparison of oxygen consumption between fed and starved clams

The intensity of RR in the control fed group of blood clams varied in the range 49.2–54.15 µgО₂·h^− 1·gww^− 1, so the average fluctuation of the parameter did not exceed 20% (Fig. 2). The significant differences of RR were noted after the third day of starvation, the oxygen consumption of starved clams increased to 62.1 ± 5.8 µgО₂·h^− 1·gww^− 1, while respiration of fed clams remained stable. Then we observed an increased oxygen consumption on 35–55% in the starved group on the 9th and 14th days of the experiment (78.9 ± 1.2 µgО₂·h^− 1·gww^− 1) compared with the control group. The oxygen content in the experiments was about 8 mgO₂·l^− 1. All molluscs were active and had open valves. No mortality of mollusks was noted.

According to our results, the average RR (at 80–100% saturation O₂) at 18°С was 67.81 ± 11.13 µgО₂·h^− 1·gww^− 1. Previously published data, the average daily RR level for S. inaequivalvis at 20°С was 75 ± 25 µgО₂·h^− 1·gww^− 1 and the maximal value of the respiratory dynamics was observed at daytime (Van den Thillart et al., 1992; ). The oxygen consumption of the blood clam was substantially lower compared to other benthic bivalves (De Zwaan et al., 1991; Stolbov & Vialova, 2001; Shin et al., 2006). Scapharca broughtonii (whole weight 5.8 ± 0.4 g) consumed 40 µgО₂·h^− 1·gww^− 1 at the same conditions, which was 5 times lower compared to the Mediterranean mussels, Mytilus galloprovincialis (220 µgО₂.h^− 1gww^− 1) (Stolbov & Vialova, 2001). Kang et al. (2007) reported that maximal RR level for S. broughtonii (189 ± 0.003 µgО₂·h^− 1·gww^− 1) was observed for clams with shell length 11.8 ± 2.1 mm at 20°C. The larger individuals (> 30 mm) showed two times lower RR (90 ± 0.012 µgО₂·h^− 1·gww^− 1). Similarly, Buhadi et al. (2013) reported that RR of Anadara spp. decreased as the weight of the mollusk increased.

Blood clams are typical inhabitants of bottom biocenoses, where oxygen deficiency often occurs because of insufficiently intensive mixing of water and the accumulation of organic compounds in sediments and the bottom layer (Qian et al., 2002). The different resistance of A. kagoshimensis to hypoxia and other adverse factors is primarily associated with the physiological and ecological peculiarities of these animals. Thus, the results of studying the intensity of oxygen consumption showed that the studied mollusks with the same mass of soft tissues under normoxia and at 17–20°C differed significantly: the blood clams had 7 times lower oxygen consumption than mussels (Stolbov & Vialova, 2001; Santini et al., 2002). Thus, even under the conditions of external normoxia, anaerobic processes actively take place in the blood clam tissues and oxygen consumption is low. It was found that mussels exposed to oxygen concentrations decreasing from 9 to 2 mgO₂·l^− 1 resulted in a slow reduction in the respiration rate, while the filtration rate remained high and constant (Tang & Riisgård, 2018). Thus, a decrease of oxygen concentration by 78% only resulted in a 25% decrease in respiration rate of M.edulis. The lowest RR of A. kagoshimensis (5.0-7.7 µgО₂·h^− 1·gww^− 1) obtained in our experiments at 76% oxygen saturation was unexpected. The drop of respiration rates was more than 94%. Such low values are usually observed in bivalves undergoing prolonged hypoxia and anoxia (De Zwaan et al, 1991; Miyamoto & Iwanaga, 2012) and when they tightly close shells, that prevented water flow through the gills (Riisgård & Larsen, 2015). The closed valves of S. inaequivalvis can to depress its energy metabolism to less than 30–40% of the standard metabolic rate measured when the valves were open (Van den Thillart et al., 1992). Our results suggest the features of the organization of tissue metabolism of blood clams and their ability to rapidly transition from aerobic to anaerobic metabolism under conditions that are not critical for them.

In this case low rate of aerobic metabolism in А. kagoshimensis is functionally determinant and possesses an adaptive role for survival of this benthic species. The blood clam lives at depths of up to 30 m, mainly on mud, mud-shell or mud-sand bottom; at certain periods of during the life cycle it may burrow periodically into substrata (Crocetta, 2012; Strafella et al., 2017).

Starvation is considered an extremely nutritive stressor, and bivalves typically decrease metabolic rate to a minimum value (required to vital functions) to cope with it. Thus, the strategy allows the animal to reduce energy consumption and preserve energy under the starvation period. For example, food limitation of > 15 days decreased respiration of the marine clams Mya arenaria by 80% (Haidera et al., 2020). However, we did not find this in present experiments with blood clams A. kagoshimensis. According to our results, the effect of starvation was expressed in an increase in oxidative processes, which required additional oxygen. The early work found that during initial stages of starvation (6 day) A. inaequivalvis used a resource of tissue lactate in a direction of oxidative decarboxylation reactions (Andreenko et al., 2009). Significant increase in activity of lactate dehydrogenase on a background of lactate content reduction and rise in pyruvate level in tissues was determined. The process of A. inaequivalvis adaptation to starvation involves using the amino acids reserves during tissue biosynthesis. It has been shown, that various stress-factors induce synthesis of low molecular weight proteins, the “acute phase proteins” (Andreenko, 2012; Gostyukhina & Andreenko, 2019, 2020). Protein synthesis is also confirmed by the increase of RNA/DNA index observed in the hepatopancreas of A. kagoshimensis during the 15-day starvation period (Shcherban, 2012). Hepatopancreas of the blood clams is a specific organ, which uses the resource of amino acids for biosynthesis and energy supply of tissues at the initial state of other negative factors, as an anoxia and hypoxia (Andreenko et al., 2009; Andreenko, 2012). In unfavorable conditions clams activate antioxidant enzyme cascade and demonstrate a complex of tissue responses, which regulates the intensity of free radical oxidation (Golovina et al., 2016). Some authors note an increase in the number of erythrocytes and hemoglobin content in the initial period of starvation of hydrobionts (Oubella et al., 1993; Borah & Yadav, 1996). During starvation, the bivalve haemocytes maintained a homeostasis in phagocytic efficacy and nitric oxide generation ability with respect to the control. The mollusk maintained a significantly high protein content in its haemolymph and tissues under the nutritional stress with respect to the control. The dietary stress had no significant impact on the activity of digestive tissue till sixteenth day (Mahapatra et al., 2017). A similar increase in oxygen consumption and amino acid oxidation for energy production was observed in Scapharca subcrenata under the negative influence of heat stress (Jiang et al, 2020). It postpones the use of carbohydrate reserves of the body to the later stages of starvation.

The prolonged starvation did not cause significant inhibition of aerobic metabolism in some species (Choromytilus meridionalis, Modiolus barbatus) (Griffiths, 1980; Glavic et al., 2018). During fifteen days of starvation, oxygen consumption and clearance rate of mussel M. barbatus and ark Arca noae also showed an increase (Glavić et al., 2018).

At the beginning of the experimental period the average weight of A. kagoshimensis was 5.19 ± 0.63 g for the control group and 4.86 ± 0.67 g for the experimental group. The total weight of individuals in both groups did not significantly change during the experiment (P > 0.05). At the end of the experiment the decrease in wet weight of soft tissues of starved clams was less than 4%, but water content of tissues increased from 81–85%. Starvation tolerance in the mussel Limnoperna fortune has been observed and the specimens that were not fed showed no weight loss (Cordeiro et al., 2016; Mahapatra et al., 2017). During starvation, the bivalve haemocytes maintained a homeostasis in phagocytic efficacy and nitric oxide generation ability with respect to the control. The mollusc maintained a significantly high protein content in its haemolymph and tissues under the nutritional stress with respect to the control. The dietary stress had no significant impact on the activity of digestive tissue (Mahapatra et al., 2017). This phenomena has also been observed in other invasive bivalves, such as the freshwater zebra mussel Dreissena polymorpha and the marine mussel Mytilus edulis (Chase & McMahon 1995; Harbach & Palm, 2018). The total shell linear parameters of clams A. kagoshimensis did not change during the experiment.

Benthic organisms are subject to prolonged seasonal food limitation in the temperate shallow coastal waters that can cause energetic stress and affect their performance. Sediment-dwelling marine bivalves cope with prolonged food limitation by adjusting different physiological processes that might cause trade-offs between maintenance and other fitness-related functions. We investigated the effects of 14-days food deprivation on energetic metabolism rate of alien species A. kagoshimensis.

Survival at unfavorable trophic conditions depends on the physiological state of the organism, i.e. complex interaction between the level of internal energy supply, stable metabolic rate and the process of gametogenesis. The energy reserves are primarily used to support the metabolism, growth and maturation of gonads (Bayne et al., 1978; Pipe, 1985; Robinson, 1992; Cannuel & Beninger, 2005; Liu et al., 2010). During the starvation of mollusks in the winter, when the process of gametogenesis is enhanced, energy needs are provided by protein catabolism, while specialized cells of the somatic tissue continue to accumulate glycogen. Starvation during summer months enhances catabolism of carbohydrates in bivalves. The responses of organisms to a deficiency or lack of available food can be largely determined by the size of the animal. For example, according to Rodhouse & Gaffney (1984) small oysters, C. gigas, loose much more soft tissue weight (estimated by a percentage) in comparison to larger individuals. The use of energy depends on the opportunistic or conservative strategy. The result of the study shows that the conservative strategy has been applied. It can be attributed to the fact that the blood clam does not lose weight for a long time (Acarli et al., 2015).

In summary, the invasive mollusk A. kagoshimensis was found to have a low rate of oxygen consumption as a measurement of energy metabolism, which is functionally determinant and plays an adaptive role in the survival of this benthic species in different habitats. The RR level was correlated with dissolved oxygen concentration, R² = 0.92 (P < 0.05). We did not observe significant changes in body weight (including shell) between control and starved groups at the end of the experimental period. During 14 days of the experiment, the respiration rate in the control fed mollusks varied in the range 49.2–54.15 µgО₂/h/gww, so the average fluctuation of the parameter did not exceed 10%. Two-weeks starvation led to an increase in oxygen consumption of the blood clam A. kagoshimensis, which indicates the intensive oxidative processes of organism. There was an increase in aerobic metabolism by 35 ˗ 55% in the starved group compared to the control group by the end of the experiment.

The study reflects the instinctive urge of the bivalve to maintain immune physiology at heavy metabolic cost under nutrient limited condition. In natural ecosystems available resources of food vary during the annual cycle, presuming periodic starvation or food deficiency for benthic mollusks. Tolerance to starvation is considered to be linked with the invasiveness of bivalves, such as Anadara kagoshimensis. And the success of this invasive species may be explained by its behavior and physiological tolerance to a wide range of ecological conditions. The results of the present work have shown that A. kagoshimensis is tolerant to starvation and maintenance of stable metabolism is provided by the enhancement of oxidative processes. Thus, further research is required to assess the effects of more long-term starvation on the metabolism of blood clams.

Funding statement

These studies were supported by the Ministry of Science and Higher Education of the Russian Federation grant № 121041400077-1.

Data availability statements

Author confirms that all relevant data are included in the article. The author declares that data supporting the findings of this study are available within the article.

Competing interests

The authors declare that they have no competing interests.

Ethics Approval statement

We declare that this manuscript is original, has not been published before and is not currently being considered for publication elsewhere.

Acknowledgements

These studies were supported by the Ministry of Science and Higher Education of the Russian Federation grant № 121041400077-1.

Acarli, S., Lök, A., Kirtik, A., Acarli, D., Serdar, S., Kucukdermenci, A., Yigitkurt, S., Yildiz, H., & Nur Saltan, A. (2015) Seasonal variation in reproductive activity and biochemical composition of flat oyster (Ostrea edulis) in the Homa Lagoon, Izmir Bay, Turkey. Scientia Marina, 79 (4), 487–495. DOI: http://dx.doi.org/10.3989/scimar.04202.16A
Andreenko, T.I. (2012) Adaptive changes of protein metabolism in tissue of the mollusk-invader Anadara inaequivalvis (Bruguiere, 1789) under conditions of experimental starvation. Bulletin of SevNTU, Series: Mechanics, Energy, Ecology, 132, 159–164.
Andreenko, T.I., Soldatov, A.A., & Golovina, I.V. (2009) Characteristics of tissue metabolism reorganization in bivalve mollusk Anadara inaequivalvis (Bruguiere, 1789) under experimental starvation conditions. Marine Ecological Journal, 8 (3), 15–24.
Barnard, C., Martineau, C., & Frenette, J.-J. (2006). Trophic position of zebra mussel veligers and their use of dissolved organic carbon. Limnology and Oceanography, 51(3), 1473–1484. DOI: 10.4319/lo.2006.51.3.1473
Bayne, B.L. (1973) Aspects of the metabolism of Mytilus edulis during starvation. Netherlands Journal of Sea Research, 7, 399–410.
Bayne, B.L., Holland, D.L., Moore, M.N., Lowe, D.M., & Widdows, J. (1978). Further studies on the effects of stress in the adult on the eggs of Mytilus edulis. Journal of the Marine Biological Association of the United Kingdom, 58, 825–841.
Borah, S., & Yadav, R.N.S. (1996). Biochemical and haematological responses to starvation in an air breathing fresh water teleost Heteropneustes fossilis (Bloch). Indian Journal of Fisheries, 43(3), 307–311.
Buhadi, Y., Kobari, T., Kawai, K., Yamamoto, T., Suzuki, H., Nishimura, S., Tori, T., & Veitayaki, J. (2013) Food Availability for Particle-Feeding Bivalves, Anadara spp., in Fiji 1. Pacific Science, 67(4), 539–551. DOI: 10.2984/67.4.5
Cannuel, R., & Beninger, P.G. (2005) Is oyster broodstock feeding always necessary? A study using oocyte quality predictors and validators in Crassostrea gigas. Aquatic Living Resources, 18, 5–43. DOI: 10.1051/alr:2005003
Chase, R., & McMahon, R.F. (1995). Effects of starvation at different temperatures on dry tissue and dry shell weights in the zebra mussel, Dreissena polymorpha (Pallas). Technical Report EL-95-4. U.S. Army Engineer Waterways Experiment Station, Vicksburg, 15p.
Cordeiro, N.I.S., Andrade, J.T.M., Montresor, L.C., Luz, D.M.R., Martinez, C.B., Darrigran, G., Pineheiro, J., & Vidigal, T.H.D.A. (2016) Effect of starvation and subsequent feeding on glycogen concentration, behavior and mortality in the golden mussel Limnoperna fortune (Dunker, 1857) (Bivalvia: Mytilidae). Journal of Limnology, 75(3), 618–625. DOI: 10.4081/jlimnol.2016.1465.
Crocetta, F. (2012) Marine alien Mollusca in Italy: a critical review and state of the knowledge. Journal of the Marine Biological Association of the UK, 92(06), 1357–1365. DOI: 10.1017/S002531541100186X
De Zwaan, A., Cortesi, P., Van den Thillart, G., Roos, J., & Storey, K.B. (1991) Differential sensitivities to hypoxia by two anoxia-tolerant marine mollusks: a biochemical analysis. Marine Biology, 111, 343–351.
De Zwaan, A., Babarro, J.M.F., & Monari, M. (2002) Anoxic survival potential of bivalves: (arte)facts. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 131(3), 615–624. DOI: 10.1016/s1095-6433(01)00513-x
Glavić, N., Vlašić, M., Hrustić, E., Bolotin, J., & Dupčić, I.R. (2018) The effect of food quantity on physiological responses of the bearded horse mussel Modiolus barbatus and the Noah's ark shell Arca noae. International Journal of Advanced Research, 6(10), 987–995. DOI: 10.21474/IJAR01/7897
Golovina, I.V., Gostyukhina, O.L., & Andreyenko, T.I. (2016) Specific metabolic features in tissues of the ark clam Anadara kagoshimensis Tokunaga, 1906 (Bivalvia: Arcidae), a Black Sea invader. Russian Journal of Biological Invasions, 7, 137–145. DOI: 10.1134/S2075111716020065.
Gostyukhina, O.L., & Andreenko, T.I. (2019) Tissue metabolism and the state of the antioxidant complex in the Black Sea mollusks Anadara kagoshimensis (Tokunaga, 1906) and Mytilus galloprovincialis Lamarck, 1819 with different tolerances to oxidative stress. Russian Journal of Marine Biology, 45(3), 211–220. DOI: 10.1134/S1063074019030039
Gostyukhina, O.L., & Andreenko, T.I. (2020) Enzymatic and low-molecular weight parts of antioxidant complex in two species of Black Sea mollusks with different resistance to oxidative stress: Mytilus galloprovincialis Lam. and Anadara kagoshimensis (Tokunaga, 1906). Biology Bulletin Reviews, 10(1), 38–47. DOI: 10.1134/S2079086420010041
Griffiths, R.J. (1980) Filtration, respiration and assimilation in the black mussel Choromytilus meridionalis. Marine Ecology Progress Series, 3, 63–70.
Haidera, F., Timm, S., Bruhnsa, T., Nusrat, M.N. & Sokolova, I.M. (2020). Effects of prolonged food limitation on energy metabolism and burrowing activity of an infaunal marine bivalve, Mya arenaria. Comparative Biochemistry and Physiology - Part A Molecular & Integrative Physiology, 250(4), 110780. DOI: 10.1016/j.cbpa.2020.110780
Harbach, H., & Palm, H.W. (2018) Development of general condition and flesh water content of long-time starved Mytilus edulis-like under experimental conditions. AACL Bioflux, 11(2), 301–308.
Jiang, Y., Jiao, H., Sun, P., Yin, F., & Tang, B. (2020) Metabolic response of Scapharca subcrenata to heat stress using GC/MS-based metabolomics. PeerJ, 8, 8445. DOI 10.7717/peerj.8445
Kang, K.H., Park, H.-J., Kim, Y.H, Seon, S.C., Zhou, B. (2007) Filtration and oxygen consumption rates on various growth stages of Scapharca broughtonii spat. Aquaculture Research. 39(2), 195–199 DOI: 10.1111/j.1365-2109.2007.01879.x
Kladchenko, E.S., Andreyeva, A.Yu., Kukhareva, T.A., & Soldatov, A.A. (2020) Morphologic, cytometric and functional characterisation of Anadara kagoshimensis hemocytes. Fish and Shellfish Immunology, 98, 1030–1032. DOI: 10.1016/j.fsi.2019.11.061
Krapal, A.M., Popa, O.P., Levarda, A., Iorgu, E.I., & Popa, L.O. (2014) Molecular confirmation on the presence of Anadara kagoshimensis (Tokunaga, 1906) (Mollusca: Bivalvia: Arcidae) in the Black sea. “Grigore Antipa” National Museum of Natural History, LVII (1), 9–12. DOI: 10.2478/travmu-2014-0001
Liu, W., Li, Q., Gao, F., & Kong, L. (2010) Effect of starvation on biochemical composition and gametogenesis in the Pacific oyster Crassostrea gigas. Fisheries Science, 76(5), 737–745. DOI: 10.1007/s12562-010-0274-y
Mahapatra, E., Dasgupta, D., Bhattacharya, N., Mitra, S., Banerjee, D., Goswami, S., Ghosh, N., Dey, A., & Chakraborty, S. (2017). Sustaining immunity during starvation in bivalve mollusc: A costly affair. Tissue and Cell. 49(2), 239–248. DOI: 10.1016/j.tice.2017.02.005
Miyamoto, Y., & Iwanaga, C. (2012) Biochemical responses to anoxia and hypoxia in the ark shell Scapharca kagoshimensis. Plankton & Benthos Research, 7(4), 167–174. https://doi.org/10.3800/pbr.7.167
Oubella, R., Maes, P., Paillard C., & Auffret, M. (1993). Experimentally induced variation in hemocyte density for Ruditapes philippinarum and R. decussates (Mollusca, Bivalvia). Diseases of Aquatic Organisms, 15(3), 193–197.
Qian, Y., Chen, H., & Sun, J. (2002). Effects of starvation on the hematological and blood biochemical indices in cultured Lateolabrax japonicas. Journal of Fishery Sciences of China, 9(2), 133–137.
Pipe, R.K. (1985) Seasonal cycles in and effects of starvation on egg development in Mytilus edulis. Marine Ecology, 24, 121–128.
Revkov, N.K. (2016). Colonization’s features of the Black Sea basin by recent invader Anadara kagoshimensis (Bivalvia: Arcidae) Marine Biological Journal, 1(2), 3–17. doi:10.21072/mbj.2016.01.2.01
Riisgård, H.U., & Larsen, P.S. (2015) Physiologically regulated valve closure makes mussels long-term starvation survivors: test of hypothesis. Journal of Molluscan Studies, 81, 303–307. DOI:10.1093/mollus/eyu087
Robinson, A. (1992) Dietary supplements for reproductive conditioning of Crassostrea gigas kumamoto (Thunberg). I. Effects of gonadal development, quality of ova and larvae through metamorphosis. Journal of Shellfish Research, 11(2), 437–441.
Rodhouse, P.G., & Gaffney, P.M. (1984) Effect of heterozygosity on metabolism during starvation in the American oyster Crassostrea virginica. Marine Biology, 80, 179–187.
Sadok, S., Uglow, R.F., & Haswell, S.J. (1999) Some aspects of nitrogen metabolism in Mytilus edulis: effects of aerial exposure. Marine Biology, 135(2), 297–305.
Santini, G., Bianchi, T., & Chelazzi, G. (2002) Metabolic responses to food deprivation in two limpets with different foraging regimes, revealed by recording of cardiac activity. Journal of Zoology, 256(1), 11–15. https://doi.org/10.1017/S095283690200002X
Shcherban, S.A. (2012) Tissue peculiarities of the protein anabolism in bivalve mollusk Anadara inaequivalvis in norm, under food deficit and anoxia. Hydrobiological Journal, 48(2), 21–29. DOI: 10.1615/HydrobJ.v48.i2.40
Shin, Y.K., Kim, B.H., Oh, B.S., Jung, C.G., Sohn, S.G., & Lee, J.S. (2006) Physiological responses of the ark shell Scapharca broughtonii (Bivalvia: Arcidae) to decreases in salinity. Fisheries and Aquatic Sciences, 9(4), 153–159. DOI: 10.5657/fas.2006.9.4.153
StatSoft, Inc. 2007. STATISTICA data analysis software system, ver. 8.0.
Stolbov, A.Y., & Vialova, O.Y. (2001) Respiratory metabolism of the Black Sea mussels Mytilus galloprovincialis under conditions of oxygen deficiency (experimental studies). Ecology of the sea, 56, 59–62.
Strafella, P., Ferrari, A., Fabi, G., Salvalaggio, V., Punzo, E., Cuicchi, C., Santelli, A., Cariani, A., Tinti, F., Tassetti, A.N., & Scarcalla, G. (2017) Anadara kagoshimensis (Mollusca: Bivalvia: Arcidae) in the Adriatic Sea: morphological analysis, molecular taxonomy, spatial distribution, and prediction. Mediterranean Marine Science, 18(3), 443–453. https://doi.org/10.12681/mms.1933
Tang, B.J., & Riisgård, H.U. (2016) Physiological regulation of valve-opening degree enables mussels Mytilus edulis to overcome starvation periods by reducing the oxygen uptake. Journal of Marine Science, 6(3), 341–352. http://dx.doi.org/10.4236/ojms.2016.63029
Tang, B.J., & Riisgård, H.U. (2018). Relationship between oxygen concentration, respiration and filtration rate in blue mussel Mytilus edulis. Journal of Oceanology and Limnology, 36, 395–404. Doi:10.1007/s00343-018-6244-4.
Van den Thillart, G., Lieshout, G., Storey, K., Cortesi, P., & de Zwaan, A. (1992) Influence of long-term hypoxia on the energy metabolism of the haemoglobin-containing bivalve Scapharca inaequivalvis: critical O₂ levels for metabolic depression. Journal of Comparative Physiology, B, 162(4), 297–304. DOI: 10.1007/bf00260756
Xu, B., Zhao, J., Jing, Z., Zhang, Y., Shi, Y., & Fan, T. (2015) Role of hemoglobin from blood clam Scapharca kagoshimensis beyond oxygen transport. Fish & Shellfish Immunology, 44(1), 248–256. https://doi.org/10.1016/j.fsi.2015.02.014
Zhavoronkova, A.M., & Zolotnitsky, A.P. (2017). Respiration intensity of bivalve blood cockle – Anadara inaequivalvis (Bruguière, 1789) acclimatized in the Black Sea. Proceedings of the Southern Scientific Research Institute of Fisheries and Oceanography, 54, 104–109.
Zhavoronkova, A.M., Zolotnitsky, A.P., & Sytnik, N.A. (2017). Effects of body weight and water temperature on the intensity of respiration of blood cockle – Anadara kagoshimensis (Tokunaga, 1906) the Azov-Black sea basin. Scientific Notes of V.I. Vernadsky Crimean Federal University. Biology. Chemistry. 3(4), 70–81.

No competing interests reported.

Download PDF

Version 1

posted

You are reading this latest preprint version

Respiration of invasive bivalve Anadara kagoshimensis (Tokunaga, 1906) at the 14-days starvation and different oxygen content in sea water

Status:

Version 1

Abstract

Figures

1. Introduction

2. Materials And Methods

2.1. Respiration rate of blood clams under different oxygen regimes

2.2. The 14-days starvation modeling

3. Results

3.1. Respiration rate of A. kagoshimensis

3.2. Comparison of oxygen consumption between fed and starved clams

4. Discussion

Conclusion

Declarations

Data availability statements

References

Additional Declarations

Status:

Version 1