Combined Effects of Ocean Acidification and Hypoxia on The

Wang et al. Helgol Mar Res (2020) 74:3 https://doi.org/10.1186/s10152-020-0535-9 Helgoland Marine Research ORIGINAL ARTICLE Open Access Combined efects of ocean acidifcation and hypoxia on the early development of the thick shell mussel Mytilus coruscus Xinghuo Wang1,2,3†, Yueyong Shang1,2,3†, Hui Kong1,2,3, Menghong Hu1,2,3, Jinlong Yang2,3, Yuewen Deng1* and Youji Wang1,2,3* Abstract Ocean acidifcation has become serious, and seawater hypoxia has become evident in acidifed waters. The combi- nation of such stressors may have interactive efects on the ftness of marine organisms. In order to investigate the interactive efects of seawater acidifcation and hypoxia on the early development of marine bivalves, the eggs and sperm of the thick shell mussel Mytilus coruscus were exposed to combined treatments of pH (8.1, 7.7, 7.3) and dissolved oxygen (2, 6 mg/L) for 96 h culture observation to investigate the interactive efects of seawater acidifcation and hypoxia on the early development of marine bivalves. Results showed that acidifcation and hypoxia had signifcant negative efects on various parameters of the early development of the thick shell mussel. However, hypoxia had no efect on fertilization rate. Signifcant interactions between acidifcation and hypoxia were observed during the experiment. Short-term exposure negatively infuenced the early development of the thick shell mussel but did not afect its survival. The efects of long-term exposure to these two environmental stresses need further study. Keywords: Ocean acidifcation, Hypoxia, Mytilus coruscus, Early development Background developmental stage of abalones Haliotis diversicolor and Ocean Acidifcation (OA), i.e., a decrease in seawater pH signifcantly reduces the survival rate of larvae [16]. In (increased acidity) associated with a change in carbonate addition, low pH delays the development of mussel Myti- equilibrium system, is a consequence of the large amount lus galloprovincialis larvae [17]. of anthropogenic CO 2 absorbed by the ocean [1–3]. Te Seawater acidifcation does not occur alone in the current surface seawater pH is approximately 8.1–8.2 and natural environment. Other stressors, such as hypoxia, is predicted to decrease to 7.7–7.8 by 2100 and 7.3–7.4 also afect the marine environment [18–22]. Hypoxia by 2300 [4, 5]. OA can afect the fertilization [6], embry- are areas with hypoxic conditions that the dissolved oxy- onic development, metabolism [7], behavior [8–10], and gen (DO) concentration in the water is < 2.0 mg/L [23]. immunity [11] of various marine organisms; threatens OA is likely to occur in areas where the seawater is def- the survival and reproduction of marine animals; and cient in oxygen [24, 25]. Te decrease in seawater DO damages global marine biodiversity and ecosystem sta- can enhance seawater acidifcation, and the seawater pH bility [12–15]. Acidifcation negatively afects the early decreases with the value of DO [19]. Low DO in water negatively infuences marine organisms and even threat- *Correspondence: [email protected]; [email protected] ens the survival of marine life [26–28]. Clark and Gob- †Xinghuo Wang and Yueyong Shang contributed equally to this work ler [29] found that low DO inhibits the development and 1 Fisheries College, Guangdong Ocean University, Zhanjiang 524088, China signifcantly reduces the survival rate of bay scallop Argo- Full list of author information is available at the end of the article pecten irradians larvae (2.33 mg/L). © The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://crea- tivecommons.org/licenses/by/4.0/. Wang et al. Helgol Mar Res (2020) 74:3 Page 2 of 9 Marine mussels have become a popular model animal Zhejiang Province, China. After cleaning, the mussels in marine environmental monitoring research owing were acclimated in the aquarium for a week. Tempera- to their relatively long lifespan, sessile benthic life style, ture, salinity, and DO were controlled at 20.0 ± 0.3 °C, flter feeding, bioaccumulation capability in body, and 25.0 ± 0.5, and 6.0 ± 0.3 mg O2/L, respectively. Water global distribution [30]. Embryonic and early larval was completely changed once a day, and dead mus- developments are important stages of mollusk life cycle. sels were removed during acclimation. Isochrysis gal- 4 Benthic animals experience stress, such as nutrition bana (2.5 × 10 cells/mL) was fed to mussels daily. After defciency, pollution and infltration, and growth inhibi- 1-week acclimation, 60 parental mussels (45 females, 15 tion during larval stage [31]. Early embryos and larvae of males) were stimulated with fowing fltered seawater shellfsh are sensitive to environmental disturbances. OA for 10 min before spawning and then transferred to a exposure of oysters during early development can poten- 60 L spawning tank. Termal shock method was applied tially inhibit their subsequent growth and development by rapidly increasing the water temperature from 13 to [32]. Stevens and Gobler [33] studied the efects of ocean 23 °C to achieve large-scale spawning [38, 39]. Male mus- acidifcation and hypoxia on bay scallop Argopecten irra- sels that release sperm and female mussels that spawn dians and found that acidifcation signifcantly reduces were transferred to two 30 L spawning tanks for ejacu- their survival rate, and this efect is further aggravated by lation and spawning, respectively. After ejaculation and hypoxia. Gobler et al. [34] analyzed the efects of ocean spawning, 15 mL of seawater containing eggs (density acidifcation and hypoxia on the early development of of about 2 103/mL) and 15 mL of seawater containing × 6 hard clams Mercenaria mercenaria and found that acidi- sperm (density of about 1 × 10 /mL) were sampled and fcation signifcantly inhibits larval growth, and hypoxia transferred to aquariums (30 L) with diferent pH and intensifes this infuence. Considering that acidifca- DO levels for fertilization. tion and hypoxia exist simultaneously in actual marine ecosystems, the efects of complex ecological efects of Experimental design ① acidifcation and hypoxia on marine organisms must be Six experimental treatments ( pH 8.1 × 6 mg O2/L, ② ③ ④ investigated. Exploring this aspect can further clarify pH 8.1 × 2 mg O2/L, pH 7.7 × 6 mg O2/L, pH ⑤ ⑥ the mechanism underlying acidifcation and hypoxia on 7.7 × 2 mg O2/L, pH 7.3 × 6 mg O2/L, and pH marine organisms and help to assess the impact of envi- 7.3 × 2 mg O2/L) and three replicates were set for each ronmental variability on coastal organisms. treatment. Exposure lasted for 4 days, and the develop- Mussels are the key components of marine intertidal ment of fertilized eggs was investigated and recorded at ecosystems and enhance the coastal diversity [35]. Te 2, 4, 8, 24, 48, 72, and 96 h. thick shell mussel Mytilus coruscus is one of the most Te pH in the experimental aquarium was controlled important aquaculture shellfsh and possesses impor- by using a pCO 2/pH system (DAQ-M) equipped with a tant economic value in China [36]. Heavy mortalities of WTW pH 3310 m and a SenTix 41 pH electrode (Loligo mussels have occurred frequently during summer in the Systems Inc., Denmark) [40]. Low pH treatment was Shengsi island probably due to hypoxia and low pH con- achieved by aerating CO2 into the seawater by this pCO2/ ditions [37]. At present, the interactive efect of ocean pH system. Either N2 or air was passed through the O2 acidifcation and hypoxia on the early development of regulator (Loligo Systems Inc., Denmark) into the seawa- M. coruscus is still unclear. We hypothesize that the early ter to achieve the hypoxic conditions [41]. development of mussels is seriously afected by acidifcation and hypoxia, and these efects are aggravated Seawater chemical parameters when both stressors appear simultaneously. Te eggs Seawater parameters were monitored daily. Total alka- and sperm of the thick shell mussel were exposed to six linity (AT) was determined by titration. Temperature, treatments [three pH levels (8.1, 7.7, and 7.3) and two salinity, and DO were measured using a multi-parameter DO levels (2 and 6 mg O2/L)] for 96 h culture observation water quality instrument (5200A, YSI Inc., America). pH to study the combined efects of ocean acidifcation and was detected by a pH meter (pH-201, MSITECH (Asia- hypoxia on the early development of this species. Ferti- Pacifc) Pte. Ltd., Singapore). Other chemical parameters lization rate, cleavage rate, deformity rate, larval shell [dissolved inorganic carbon (DIC), pCO2, calcite satura- length, and shell height were also evaluated. tion state (Ωcal), and aragonite saturation state (Ωara)] were calculated by CO2SYS [42]. Materials and methods Experimental animals Biological parameters Mussels (shell length 8.0 ± 2.0 cm, dry weight After 2 h of fertilization, the egg samples were observed 1.60 ± 0.90 mg) were collected from the Shengsi Island, by a microscope ftted with an ocular micrometer, and Wang et al. Helgol Mar Res (2020) 74:3 Page 3 of 9 fertilization was evaluated by the presence of polar body ANOVA was employed to analyze whether the interac- and embryonic cleavage [38, 39].

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