Elsevier

Marine Environmental Research

Volume 139, August 2018, Pages 144-150
Marine Environmental Research

Combined effects of ocean acidification and temperature on planula larvae of the moon jellyfish Aurelia coerulea

https://doi.org/10.1016/j.marenvres.2018.05.015Get rights and content

Highlights

  • We addressed the impact of ocean acidification and seawater temperature increases on scyphozoan planulae.

  • A. coerulea planulae can cope well with decreased pH conditions through rapid settlement.

  • Elevated seawater temperature appears to be a crucial stress factor for A. coerulea planulae.

Abstract

Rapidly rising levels of atmospheric CO2 have caused two environmental stressors, ocean acidification and seawater temperature increases, which represent major abiotic threats to marine organisms. Here, we investigated for the first time the combined effects of ocean acidification and seawater temperature increases on the behavior, survival, and settlement of the planula larvae of Aurelia coerulea, which is considered a nuisance species around the world. Three pH levels (8.1, 7.7 and 7.3) and two temperature levels (24 °C and 27 °C) were used in the present study. There were no interactive effects of temperature and pH on the behavior, survival, and settlement of planula larvae of A. coerulea. We found that the swimming speed and mortality of the planula larvae of A. coerulea were significantly affected by temperature, and low pH significantly affected settlement. Planula larvae of A. coerulea from the elevated temperature treatment moved faster and showed higher mortality than those at the control temperature. The settlement rate of A. coerulea planulae was significantly higher at the pH level of 7.3 than at other pH levels. These results suggest that seawater temperature increase, rather than reduced pH, was the main stress factor affecting the survival of A. coerulea planulae. Overall, the planula larvae of the common jellyfish A. coerulea appeared to be resistant to ocean acidification, but may be negatively affected by future seawater temperature increases.

Introduction

Rapidly rising atmospheric carbon dioxide (CO2) concentrations are causing ocean warming and decreasing seawater pH, which represent two important abiotic threats to marine ecosystems (Hoegh-Guldberg et al., 2007; Fabricius et al., 2011; McCulloch et al., 2012). The global ocean temperature has increased by 0.5 °C since the 1970s and an additional increase of 2.6–3.1 °C has been projected to occur by 2100 (IPCC, 2013; Rogelj et al., 2016). The average surface ocean pH has declined by approximately 0.1 units since the industrial revolution and is predicted to decrease by another 0.4 units by 2100 under a “business-as-usual” CO2 emission scenario (IPCC, 2013; Gattuso et al., 2015).

The effects of ocean acidification and ocean warming on marine organisms, such as corals, sea urchins and mussels, have been studied extensively to predict the future population trends of these organisms (e.g., Crain et al., 2008; Byrne and Przeslawski, 2013; Kroeker et al., 2013; Wangensteen et al., 2013; Duarte et al., 2014; Garcia et al., 2015; Hu et al., 2015; Li et al., 2015; Wang et al., 2015b, Wang et al., 2015a; Przeslawski et al., 2015; Wu et al., 2016). These studies indicate that the biological responses of marine organisms to the combined stressors of ocean acidification and seawater temperature increases vary across taxonomic groups, life-history stages and trophic levels (Crain et al., 2008; Byrne and Przeslawski, 2013; Harvey et al., 2013; Kroeker et al., 2013; Przeslawski et al., 2015). For example, Nguyen et al. (2012) showed that warming, not acidification, was the dominant stressor affecting development of the sea star Meridiastra calcar. However, results from Wangensteen et al. (2013) showed that high temperature and low pH had a positive effect on the reproduction of the sea urchin Arbacia lixula (Wangensteen et al., 2013). Chua et al. (2013) found that temperature and pH had negligible or no effects on the larval development of scleractinian corals Acropora millepora and A. tenuis (Chua et al., 2013).

The moon jellyfish Aurelia coerulea is a common scyphozoan jellyfish, found in the major warm temperate regions (e.g., East Asian Marginal Seas, the Mediterranean Sea and the Atlantic Coast of the USA) (Dawson et al., 2005; Ki et al., 2008; Dong et al., 2015; Scorrano et al., 2016). Blooms of A. coerulea medusae have been reported in the East Asian Margin Seas, including the coastal waters of China, Japan, and Korea, and these blooms can negatively impact coastal power plant operations, local fisheries and aquaculture; therefore, it has been suggested that A. coerulea is categorised as a nuisance species (Dong et al., 2010; Uye, 2011; Purcell et al., 2013). On the other hand, mounting evidence indicates that this jellyfish species is preyed upon by other organisms and might also play an important role in the marine pelagic food web (Cardona et al., 2012; Jarman et al., 2013; Hamilton, 2016).

The early developmental stages (i.e., planula, polyp and ephyra) of A. coerulea are sensitive to environmental changes and are crucial to the abundance of the adult medusa population (Lucas et al., 2012). Many research efforts have been conducted to address the impacts of seawater temperature (Liu et al., 2009; Schiariti et al., 2014; Pascual et al., 2015; Wang et al., 2015a, Wang et al., 2015b) or pH conditions (Winans and Purcell, 2010; Tills et al., 2016) on the polyp and ephyra stages of the moon jellyfish Aurelia spp.

The pelagic larvae of marine invertebrates are thought to be vulnerable to predators, physical and chemical stress (Pechenik, 1999). Additionally, there has been growing evidence that ocean acidification and elevated seawater temperatures influence the survival and settlement of pelagic larvae of other marine invertebrate species (reviewed in Gibson et al., 2011).

Aurelia spp. planulae, released by mature female medusae, usually settle on suitable substrate within one week (Brewer, 1978; Conley and Uye, 2015). Hence, the pre-settlement survival and settlement of planula larvae is crucial for the establishment of new polyp populations (Webster and Lucas, 2012; Gambill et al., 2016). During this stage, environmental factors (i.e., temperature, salinity, light and dissolved oxygen), substrate properties (physical properties and bacterial biofilms), and biological factors (conspecifics, competitors and predators) may affect the survival, settlement and metamorphosis of Aurelia spp. planulae (Lucas et al., 2012). Several recent studies have reported how water temperature and salinity influence the survival and settlement of Aurelia spp. planulae (Webster and Lucas, 2012; Conley and Uye, 2015). However, previous work has not determined the impact of ocean warming and reduced pH conditions on the planula larvae of scyphozoan jellyfish.

Ocean acidification and ocean warming can act in a combined manner, affecting the physiological progress of marine organisms. Studies have shown that elevated seawater temperature can either exacerbate the negative effects of ocean acidification on marine organisms (Rodolfo-Metalpa et al., 2011; Wu et al., 2016) or mitigate the negative effects (García et al., 2015). The aim of this study was to evaluate for the first time the combined effects of ocean acidification and seawater temperature increases on the behavior, survival, and settlement of planula larvae of the moon jellyfish A. coerulea. A. coerulea is recognized as a highly tolerant species to environmental stressors, including temperature, salinity and oxygen conditions (Lucas et al., 2012). Therefore, we hypothesized that the elevated seawater temperature and reduced pH levels would not influence the behavior, survival, or settlement of planula larvae of the moon jellyfish A. coerulea.

Section snippets

Aurelia coerulea collection and planulae cultivation

The planulae of A. coerulea were obtained following the methods of Conley and Uye (2015). Five mature A. coerulea medusae with visible planula larvae were collected with a hand net at Sishili Bay, northern Yellow Sea, China (37°29.40′ N; 121°2.89′ E) in August. Medusae were maintained in a 30 L plastic container filled with 160-μm-filtered seawater (salinity 31 psμ) and transported to a controlled temperature laboratory (24 °C). On the second day, medusa incubation seawater was filtered through

Seawater chemistry

Mean (±SD) values of carbonate system parameters in various pH treatments are shown in Table 1. The pH values measured in the filtered seawater samples were close to the target pH (within 0.03 units, Table 1). Total alkalinity remained relatively constant across different pH treatments.

Behavior, survival and settlement of A. coerulea planula larvae

The effect of the temperature-pH interaction on the swimming speed of A. coerulea planulae is shown in Fig. 1. The change in the larval size of A. coerulea planulae is shown in Fig. 2. The day-to-day settlement

Discussion

Previous studies suggest that larvae that calcify are sensitive to both warming and acidification, whereas those that do not calcify are more sensitive to warming (Byrne and Przeslawski, 2013; Kroeker et al., 2013). Our results are consistent with the hypothesis that seawater temperature increase, rather than reduced pH, is the main stress factor affecting the survival of noncalcifying A. coerulea planulae. Elevated seawater temperatures have been confirmed to reduce the survival of the pelagic

Acknowledgment

This work was supported by grants from the National Natural Science Foundation of China (No.41576152), the Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDA11020305), and the Science and Technology Service Network Initiative (STS) Project (No. KFJ-STS-ZDTP-023).

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      Our results showing lower settlement success under ambient pH and O2 conditions refute the assumption that settlement of planulae of many cnidarian species is higher on substrates with normal pH and oxygenation (see Müller and Leitz (2002) review; Ritson-Williams, 2009; Alessi et al., 2019). Instead, our results are consistent with outcomes revealing settlement of planulae of some species of jellyfish (Chrysaora sp., A. coerolea) is enhanced under deoxygenation (Condon et al., 2001; Miller and Graham, 2012) and acidification (Dong and Sun, 2018). The settlement of planulae and creeping polyps into the sessile polyp phase during stress may be a mechanism to persist under CD and CA since settled polyps expend less energy than free-living or motile stages (Ishii and Kobayashi, 2008; Schneider and Weisse, 1985).

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