Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster <italic style="font-style: italic">Crassostrea gigas</italic>

Lingshuai Zhang; Xiudan Wang; Weiqian ZHANG; Xiaoting Yin; Qing Liu; Limei Qiu

doi:10.1007/s00343-021-0462-x

Your Location：

Home >

Browse articles >

Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas

Article | Updated：2023-05-20

- Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas
- Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas
- 海洋湖沼学报（英文） 2022年40卷第2期页码：620-633
- Affiliations：
  
  1.CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Institute of Oceanology, Center for Ocean MegaScience, Chinese Academy of Sciences, Qingdao 266071, China
  2.Qingdao University of Science and Technology, Qingdao 266071, China
  3.University of Chinese Academy of Sciences, Beijing 100049, China
  4.Laboratory for Marine Biology and Biotechnology, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
- Author bio：
  
  Limei QIU, E-mail: qiulimei@qdio.ac.cn
- Funds：
  
  National Natural Science Foundation of China(32072999);National Natural Science Foundation of China(31800414);the Shandong Province Natural Science Foundation(ZR2019BC040);© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2022
- DOI：10.1007/s00343-021-0462-x
  中图分类号：
- 收稿：2020-12-01，
  
  录用：2021-2-27，
  
  网络首发：2021-04-14，
  
  纸质出版：2022-03
- Accepted：
Scan QR Code
Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas[J]. 海洋湖沼学报（英文）, 2022,40(2):620-633.

Lingshuai Zhang, Xiudan Wang, Weiqian ZHANG, et al. Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas[J]. Journal of Oceanology and Limnology, 2022, 40(2): 620-633.
Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas[J]. 海洋湖沼学报（英文）, 2022,40(2):620-633. DOI： 10.1007/s00343-021-0462-x.

Lingshuai Zhang, Xiudan Wang, Weiqian ZHANG, et al. Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas[J]. Journal of Oceanology and Limnology, 2022, 40(2): 620-633. DOI： 10.1007/s00343-021-0462-x.

摘要

Abstract

The hepatopancreas is an important tissue involved in various biological metabolism for mollusks

but its responses to ocean acidification (OA) have not been well evaluated. In this study

the oysters were cultured in simulated conditions by continuously bubbling with ambient air (pH=8.10) or air-CO

(pH=7.50) for up to two months

and the variations on the antioxidant capacity

digestive ability

and microbiota composition in hepatopancreas of

Crassostrea gigas

were analyzed. The results show that although superoxide dismutase and glutathione responded quickly to OA stress

the antioxidant capacity of the hepatopancreas was inhibited

as revealed by the decrease of the total antioxidant capacity

which led to an upward trend of the malondialdehyde

demonstrating that the oxidative damages were accumulated under the OA process. The determination of the digestive ability manifested as the decrease of pepsin activity and the recovery of lipase and amylase activity after long-term acidification

which may be helpful to improve the adaptability of oysters. In addition

analysis on 16S rDNA amplicon revealed that the total species abundance and diversity of the hepatopancreas microbiota experienced a dynamic change

but finally it decreased greatly after long-term acidification. The structure of the hepatopancreas microbiota was changed drastically with the change of the dominant species from aerobic to the anaerobic and facultative anaerobic bacteria

and the abnormal proliferation of some species

such as genus of

Mycoplasma

and order Clostridiales

which may aggravate the adverse effects of OA on the physiological functions of the hepatopancreas. As a result

our findings enrich our understanding of the accumulated oxidative damage and adaptive digestive ability in oyster hepatopancreas caused by OA. For the first time

the changes of the hepatopancreas microbiota under long-term acidification conditions are described

proving a good reference for the study of the response and adaptation mechanisms of bivalve mollusks in a wide range of oceans OA.

关键词

Keywords

references

Amaral V, Cabral H N, Bishop M J. 2012. Moderate acidification affects growth but not survival of 6-month-old oysters. Aquatic Ecology , 46 (1): 119–127..

Aujoulat F, Bouvet P, Jumas-Bilak E, Jean-Pierre H, Marchandin H. 2014. Veillonella seminalis sp. nov., a novel anaerobic Gram-stain-negative coccus from human clinical samples, and emended description of the genus Veillonella . International Journal of Systematic and Evolutionary Microbiology , 64 (Pt 10): 3526–3531..

Beauchamp C, Fridovich I. 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry , 44 (1): 276–287..

Beniash E, Ivanina A, Lieb N S, Kurochkin I, Sokolova I M. 2010. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica . Marine Ecology Progress Series , 419 : 95–108..

Bernal M G, Fernández N T, Lastra P E S, Marrero R M, Mazón-Suástegui J M. 2017. Streptomyces effect on the bacterial microbiota associated to Crassostrea sikamea oyster. Journal of Applied Microbiology , 122 (3): 601–614..

Bosshard P P, Zbinden R, Altwegg M. 2002. Turicibacter sanguinis gen. nov., sp. nov., a novel anaerobic, Grampositive bacterium. International Journal of Systematic and Evolutionary Microbiology , 52 (Pt 4): 1263–1266..

Butt R L, Volkoff H. 2019. Gut microbiota and energy homeostasis in fish. Frontiers in Endocrinology , 10 : 9..

Caldeira K, Wickett M E. 2003. Oceanography: anthropogenic carbon and ocean pH. Nature , 425 (6956): 365..

Campa-Córdova A I, González-Ocampo H, Luna-González A, Mazón-Suástegui J M, Ascencio F. 2009. Growth, survival, and superoxide dismutase activity in juvenile Crassostrea corteziensis (Hertlein, 1951) treated with probiotics. Hidrobiológica , 19 (2): 151–158..

Canesi L, Borghi C, Ciacci C, Fabbri R, Vergani L, Gallo G. 2007a. Bisphenol-A alters gene expression and functional parameters in molluscan hepatopancreas. Molecular and Cellular Endocrinology , 276 (1–2): 36–44..

Canesi L, Borghi C, Fabbri R, Ciacci C, Lorusso L C, Gallo G, Vergani L. 2007b. Effects of 17β-estradiol on mussel digestive gland. General and Comparative Endocrinology , 153 (1–3): 40–46..

Caporaso J G, Kuczynski J, Stombaugh J, Bittinger K, Bushman F D, Costello E K, Fierer N, Peña A G, Goodrich J K, Gordon J I, Huttley G A, Kelley S T, Knights D, Koenig J E, Ley R E, Lozupone C A, McDonald D, Muegge B D, Pirrung M, Reeder J, Sevinsky J R, Turnbaugh P J, Walters W A, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods , 7 (5): 335–336..

Carter H A, Ceballos-Osuna L, Miller N A, Stillman J H. 2013. Impact of ocean acidification on metabolism and energetics during early life stages of the intertidal porcelain crab Petrolisthes cinctipes . Journal of Experimental Biology , 216 (Pt 8): 1412–1422..

Clements J C, Hunt H L. 2017. Effects of CO 2 -driven sediment acidification on infaunal marine bivalves: a synthesis. Marine Pollution Bulletin , 117 (1–2): 6–16..

Coleman F C, Williams S L. 2002. Overexploiting marine ecosystem engineers: potential consequences for biodiversity. Trends in Ecology & Evolution , 17 (1): 40–44..

Debnath D, Pal A K, Sahu N P, Yengkokpam S, Baruah K, Choudhury D, Venkateshwarlu G. 2007. Digestive enzymes and metabolic profile of Labeo rohita fingerlings fed diets with different crude protein levels. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology , 146 (1): 107–114..

Doney S C, Fabry V J, Feely R A, Kleypas J A. 2009. Ocean acidification: the other CO 2 problem. Annual Review of Marine Science , 1 : 169–192..

Doney S C, Ruckelshaus M, Duffy J E, Barry J P, Chan F English C A, Galindo H M, Grebmeier J M, Hollowed A B, Knowlton N, Polovina J, Rabalais N N, Sydeman W J, Talley L D. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science , 4 : 11–37..

Duncan S H, Hold G L, Harmsen H J M, Stewart C S, Flint H J. 2002. Growth requirements and fermentation products of Fusobacterium prausnitzii , and a proposal to reclassify it as Faecalibacterium prausnitzii gen. nov., comb. nov. International Journal of Systematic and Evolutionary Microbiology , 52 (Pt 6): 2141–2146..

Edgar R C. 2013. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nature Methods , 10 (10): 996–998..

Edgar R C. 2018. Updating the 97% identity threshold for 16S ribosomal RNA OTUs. Bioinformatics , 34 (14): 2371–2375..

Engel S, Jensen P R, Fenical W. 2002. Chemical ecology of marine microbial defense. Journal of Chemical Ecology , 28 (10): 1971–1985..

Ferguson H W, Collins R O, Moore M, Coles M, MacPhee D D. 2004. Pseudomonas anguilliseptica infection in farmed cod, Gadus morhua L. Journal of Fish Diseases , 27 (4): 249–253..

Fernandez-Piquer J, Bowman J P, Ross T, Tamplin M L. 2012. Molecular analysis of the bacterial communities in the live Pacific oyster ( Crassostrea gigas ) and the influence of postharvest temperature on its structure. Journal of Applied Microbiology , 112 (6): 1134–1143..

Fitzer S C, Phoenix V R, Cusack M, Kamenos N A. 2014. Ocean acidification impacts mussel control on biomineralisation. Scientific Reports , 4 : 6218..

Fonseca F, Cerqueira R, Fuentes J. 2019. Impact of ocean acidification on the intestinal microbiota of the marine sea bream ( Sparus aurata L. ). Frontiers in Physiology , 10 : 1446..

García-Bayona L, Comstock L E. 2018. Bacterial antagonism in host-associated microbial communities. Science , 361 (6408): eaat2456..

Gerritsen J, Fuentes S, Grievink W, van Niftrik L, Tindall B J, Timmerman H M, Rijkers G T, Smid H. 2014. Characterization of Romboutsia ilealis gen. nov., sp. nov., isolated from the gastro-intestinal tract of a rat, and proposal for the reclassification of five closely related members of the genus Clostridium into the genera Romboutsia gen. nov., Intestinibacter gen. nov., Terrisporobacter gen. nov. and Asaccharospora gen. nov. International Journal of Systematic and Evolutionary Microbiology , 64 (Pt 5): 1600–1616..

Gobler C J, Talmage S C. 2013. Short- and long-term consequences of larval stage exposure to constantly and ephemerally elevated carbon dioxide for marine bivalve populations. Biogeosciences , 10 (4): 2241–2253..

Green T J, Barnes A C. 2010. Bacterial diversity of the digestive gland of Sydney rock oysters, Saccostrea glomerata infected with the paramyxean parasite, Marteilia sydneyi . Journal of Applied Microbiology , 109 (2): 613–622..

Gu H X, Shang Y Y, Clements J, Dupont S, Wang T, Wei S S, Wang X H, Chen J F, Huang W, Hua M H, Wang Y J. 2019. Hypoxia aggravates the effects of ocean acidification on the physiological energetics of the blue mussel Mytilus edulis . Marine Pollution Bulletin , 149 : 110538..

Gutowska M A, Melzner F, Langenbuch M, Bock C, Claireaux G, Pörtner H O. 2010. Acid-base regulatory ability of the cephalopod ( Sepia officinalis ) in response to environmental hypercapnia. Journal of Comparative Physiology B , 180 (3): 323–335..

Haas B J, Gevers D, Earl A M, Feldgarden M, Ward D V, Giannoukos G, Ciulla D, Tabbaa D, Highlander S K, Sodergren E, Methé B, DeSantis T Z, The Human Microbiome Consortium, Petrosino J F, Knight R, Birren B W. 2011. Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research , 21 (3): 494–504..

Hoegh-Guldberg O, Mumby P J, Hooten A J, Steneck R S, Greenfield P, Gomez E, Harvell C D, Sale P F, Edwards A J, Caldeira K, Knowlton N, Eakin C M, Iglesias-Prieto R, Muthiga N, Bradbury R H, Dubi A, Hatziolos M E. 2007. Coral reefs under rapid climate change and ocean acidification. Science , 318 (5857): 1737–1742..

Jemaà M, Morin N, Cavelier P, Cau J, Strub J M, Delsert C. 2014. Adult somatic progenitor cells and hematopoiesis in oysters. Journal of Experimental Biology , 217 (Pt 17): 3067–3077..

Khan B, Clinton S M, Hamp T J, Oliver J D, Ringwood A H. 2018. Potential impacts of hypoxia and a warming ocean on oyster microbiomes. Marine Environmental Research , 139 : 27–34..

Kong H, Wu F L, Jiang X Y, Wang T, Hu M H, Chen J F, Huang W, Bao Y B, Wang Y J. 2019. Nano-TiO 2 impairs digestive enzyme activities of marine mussels under ocean acidification. Chemosphere , 237 : 124561..

Kurihara H. 2008. Effects of CO 2 -driven ocean acidification on the early developmental stages of invertebrates. Marine Ecology Progress Series , 373 : 275–284..

Li J, Cao J L, Wang X, Liu N, Wang W M, Luo Y. 2017. Acinetobacter pittii , an emerging new multi-drug resistant fish pathogen isolated from diseased blunt snout bream ( Megalobrama amblycephala Yih) in China. Applied Microbiology and Biotechnology , 101 (16): 6459–6471..

Li Y F, Chen Y W, Xu J K, Ding W Y, Shao A Q, Zhu Y T, Wang C, Liang X, Yang J L. 2019. Temperature elevation and Vibrio cyclitrophicus infection reduce the diversity of haemolymph microbiome of the mussel Mytilus coruscus . Scientific Reports , 9 (1): 16391..

Liu Y W, Sutton J N, Ries J B, Eagle R A. 2020a. Regulation of calcification site pH is a polyphyletic but not always governing response to ocean acidification. Science Advances , 6 (5): eaax1314..

Liu Z Q, Zhou Z, Zhang Y K, Wang L L, Song X R, Wang W L, Zheng Y, Zong Y N, Lv Z, Song L S. 2020b. Ocean acidification inhibits initial shell formation of oyster larvae by suppressing the biosynthesis of serotonin and dopamine. Science of the Total Environment , 735 : 139469..

Lushchak V I. 2011. Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology , 101 (1): 13–30..

Mackay A. 2008. Climate change 2007: impacts, adaptation and vulnerability. Contribution of working group II to the fourth assessment report of the intergovernmental panel on climate change. Journal of Environment Quality , 37 (6): 2407..

Matozzo V, Chinellato A, Munari M, Bressan M, Marin M G. 2013. Can the combination of decreased pH and increased temperature values induce oxidative stress in the clam Chamelea gallina and the mussel Mytilus galloprovincialis ? Marine Pollution Bulletin , 72 (1): 34–40..

Melzner F, Stange P, Trübenbach K, Thomsen J, Casties I, Panknin U, Gorb S N, Gutowska M A. 2011. Food supply and seawater p CO 2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis . PLoS One , 6 (9): e24223..

Miller N J, Rice-Evans C, Davies M J, Gopinathan V, Milner A. 1993. A novel method for measuring antioxidant capacity and its application to monitoring the antioxidant status in premature neonates. Chemical Science , 84 (4): 407–412..

Mountfort D O, Rainey F A, Burghardt J, Kaspar H F, Stackebrandt E. 1998. Psychromonas antarcticus gen. nov., sp. nov., a new aerotolerant anaerobic, halophilic psychrophile isolated from pond sediment of the McMurdo Ice Shelf, Antarctica. Archives of Microbiology , 169 (3): 231–238..

Muñoz K, Flores-Herrera P, Gonçalves A T, Rojas C, Yáñez C, Mercado L, Brokordt K, Schmitt P. 2019. The immune response of the scallop Argopecten purpuratus is associated with changes in the host microbiota structure and diversity. Fish & Shellfish Immunology , 91 : 241–250..

Paillard C, Le Roux F, Borrego J J. 2004. Bacterial disease in marine bivalves, a review of recent studies: Trends and evolution. Aquatic Living Resources , 17 (4): 477–498..

Pansch C, Schaub I, Havenhand J, Wahl M. 2014. Habitat traits and food availability determine the response of marine invertebrates to ocean acidification. Global Change Biology , 20 (3): 765–777..

Parker L M, Ross P M, O'Connor W A, Pörtner H O, Scanes E, Wright J M. 2013. Predicting the response of molluscs to the impact of ocean acidification. Biology , 2 (2): 651–692..

Pitcher D G, Nicholas R A J. 2005. Mycoplasma host specificity: fact or fiction? Veterinary Journal , 170 (3): 300–306..

Pruzzo C, Gallo G, Canesi L. 2005. Persistence of vibrios in marine bivalves: the role of interactions with haemolymph components. Environmental Microbiology , 7 (6): 761–772..

Rada B, Leto T L. 2008. Oxidative innate immune defenses by Nox/Duox family NADPH oxidases. Contributions to Microbiology , 15 : 164–187..

Raimundo J, Reis C M G, Ribeiro M M. 2018. Rapid, simple and potentially universal method for DNA extraction from Opuntia spp. fresh cladode tissues suitable for PCR amplification. Molecular Biology Reports , 45 : 1405–1412..

Ray A K, Ghosh K, Ringø E. 2012. Enzyme-producing bacteria isolated from fish gut: a review. Aquaculture Nutrition , 18 (5): 465–492..

Ribes M, Calvo E, Movilla J, Logares R, Coma R, Pelejero C. 2016. Restructuring of the sponge microbiome favors tolerance to ocean acidification. Environmental Microbiology Reports , 8 (4): 536–544..

Ringwood A H, Conners D E, Keppler C J, DiNovo A A. 1999. Biomarker studies with juvenile oysters ( Crassostrea virginica ) deployed in-situ . Biomarkers , 4 (6): 400–414..

Rodolfo-Metalpa R, Houlbrèque F, Tambutté É, Boisson F, Baggini C, Patti F P, Jeffree R, Fine M, Foggo A, Gattuso J P, Hall-Spencer J M. 2011. Coral and mollusc resistance to ocean acidification adversely affected by warming. Nature Climate Change , 1 (6): 308–312..

Roeselers G, Mittge E K, Stephens W Z, Parichy D M, Cavanaugh C M, Guillemin K, Rawls J F. 2011. Evidence for a core gut microbiota in the zebrafish. The ISME Journal , 5 (10): 1595–1608..

Rottem S. 2003. Interaction of mycoplasmas with host cells. Physiological Reviews , 83 (2): 417–432..

Rungruangsak K, Utne F. 1981. Effect of different acidified wet feeds on protease activities in the digestive tract and on growth rate of rainbow trout ( Salmo gairdneri Richardson). Aquaculture , 22 : 67–79..

Sokolova I M, Sukhotin A A, Lannig G. 2011. Stress effects on metabolism and energy budgets in mollusks. In : Abele D, Vázquez-Medina J P, Zenteno-Savín T eds. Oxidative Stress in Aquatic Ecosystems. John Wiley & Sons, Oxford. p. 263–280.

Soldatov A A, Gostyukhina O L, Golovina I V. 2007. Antioxidant enzyme complex of tissues of the bivalve Mytilus galloprovincialis Lam. under normal and oxidative-stress conditions: a review. Applied Biochemistry and Microbiology , 43 (5): 556–562..

Steiner J M. 2005. Clinical utility of a new lipase activity assay. Veterinary Clinical Pathology , 34 (3): 176–177..

Talmage S C, Gobler C J. 2010. Effects of past, present, and future ocean carbon dioxide concentrations on the growth and survival of larval shellfish. Proceedings of the National Academy of Sciences of the United States of America , 107 (40): 17246–17251..

Thomsen J, Casties I, Pansch C, Körtzinger A, Melzner F. 2013. Food availability outweighs ocean acidification effects in juvenile Mytilus edulis : laboratory and field experiments. Global Change Biology , 19 (4): 1017–1027..

Tremaroli V, Bäckhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature , 489 (7415): 242–249..

Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M. 2006. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety , 64 (2): 178–189..

Vezzulli L, Stagnaro L, Grande C, Tassistro G, Canesi L, Pruzzo C. 2018. Comparative 16SrDNA gene-based microbiota profiles of the pacific oyster ( Crassostrea gigas ) and the mediterranean mussel ( Mytilus galloprovincialis ) from a shellfish farm (Ligurian Sea, Italy). Microbial Ecology , 75 (2): 495–504..

Wang Q, Cao R W, Ning X X, You L P, Mu C K, Wang C L, Wei L, Cong M, Wu H F, Zhao J M. 2016. Effects of ocean acidification on immune responses of the Pacific oyster Crassostrea gigas . Fish & Shellfish Immunology , 49 : 24–33..

Wang X H, Huang W, Wei S S, Shang Y Y, Gu H X, Wu F Z, Lan Z H, Hu M H, Shi H H, Wang Y J. 2020. Microplastics impair digestive performance but show little effects on antioxidant activity in mussels under low pH conditions. Environmental Pollution , 258 : 113691..

Wei L, Wang Q, Wu H F, Ji C L, Zhao J M. 2015. Proteomic and metabolomic responses of Pacific oyster Crassostrea gigas to elevated p CO 2 exposure. Journal of Proteomics , 112 : 83–94..

Xiao Z Z, Storms R, Tsang A. 2006. A quantitative starch-iodine method for measuring alpha-amylase and glucoamylase activities. Analytical Biochemistry , 351 (1): 146–148..

Xu M X, Sun T L, Tang X X, Lu K Y, Jiang Y S, Cao S, Wang Y. 2020. CO 2 and HCl-induced seawater acidification impair the ingestion and digestion of blue mussel Mytilus edulis . Chemosphere , 240 : 124821..

Zhang G F, Fang X D, Guo X M, Li L, Luo R B, Xu F, Yang P C, Zhang L L, Wang X T, Qi H G, Xiong Z Q, Que H Y, Xie Y L, Holland P W H, Paps J, Zhu Y B, Wu F C, Chen Y X, Wang J F, Peng C F, Meng J, Yang L, Liu J, Wen B, Zhang N, Huang Z Y, Zhu Q H, Feng Y, Mount A, Hedgecock D, Xu Z, Liu Y J, Domazet-Loso T, Du Y S, Sun X Q, Zhang S D, Liu B H, Cheng P Z, Jiang X T, Li J, Fan D D, Wang W, Fu W J, Wang T, Wang B, Zhang J B, Peng Z Y, Li Y X, Li N, Wang J P, Chen M S, He Y, Tan F J, Song X R, Zheng Q M, Huang R L, Yang H L, Du X D, Chen L, Yang M, Gaffney P M, Wang S, Luo L H, She Z C, Ming Y, Huang W, Zhang S, Huang B Y, Zhang Y, Qu T, Ni P X, Miao G Y, Wang J Y, Wang Q, Steinberg C E W, Wang H Y, Li N, Qian L M, Zhang G J, Li Y R, Yang H M, Liu X, Wang J, Yin Y, Wang J. 2012. The oyster genome reveals stress adaptation and complexity of shell formation. Nature , 490 (7418): 49–54..

Zhao L Q, Shirai K, Tanaka K, Milano S, Higuchi T, Murakami-Sugihara N, Walliser E O, Yang F, Deng Y W, Schöne B R. 2020. A review of transgenerational effects of ocean acidification on marine bivalves and their implications for sclerochronology. Estuarine, Coastal and Shelf Science , 235 : 106620..

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

Mercury (Hg2+) effect on enzyme activities and hepatopancreas histostructures of juvenile Chinese mitten crab Eriocheir sinensis

Parental exposure to ocean acidification impacts the larval development and transcriptome of the Pacific oyster Crassostrea gigas

Effects of sulfate content and salinity on growth, oxygen consumption, Na⁺/K⁺-ATPase activity, and hepatopancreas histopathology of Pacific white shrimp Litopenaeus vannamei

Effects of dissolved oxygen on intestinal bacterial community and immunity of Atlantic salmon Salmo salar

含缺陷轮盘失效概率分析流程与数值模拟

Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas

Impact of ocean acidification on physiology and microbiota in hepatopancreas of Pacific oyster Crassostrea gigas

DOI：10.1007/s00343-021-0462-x

摘要

Abstract

关键词

Keywords

references