Combined effects of ocean acidification and temperature on planula larvae of the moon jellyfish Aurelia coerulea
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).
References (62)
- et al.
Effects of hyposalinity on survival and settlement of moon jellyfish (Aurelia aurita) planulae
J. Exp. Mar. Biol. Ecol.
(2015) - et al.
Jellyfish blooms in China: dominant species, causes and consequences
Mar. Pollut. Bull.
(2010) - et al.
Genetic characterization of the scyphozoan jellyfish Aurelia spp. in Chinese coastal waters using mitochondrial markers
Biochem. Systemat. Ecol.
(2015) - et al.
Combined effects of temperature and ocean acidification on the juvenile individuals of the mussel Mytilus chilensis
J. Sea Res.
(2014) - et al.
Ocean warming ameliorates the negative effects of ocean acidification on Paracentrotus lividus larval development and settlement
Mar. Environ. Res.
(2015) Why and how marine-invertebrate larvae metamorphose so fast
- et al.
Effect of pH and temperature on antioxidant responses of the thick shell mussel Mytilus coruscus
Fish Shellfish Immunol.
(2015) - et al.
3 Jellyfish Life Histories: role of polyps in forming and maintaining scyphomedusa populations
Adv. Mar. Biol.
(2012) - et al.
Jellyfish as Products and Problems of Aquaculture. Advances in Aquaculture Hatchery Technology
(2013) - et al.
Reduced pH affects pulsing behaviour and body size in ephyrae of the moon jellyfish, Aurelia aurita
J. Exp. Mar. Biol. Ecol.
(2016)
Physiological energetics of the thick shell mussel Mytilus coruscus exposed to seawater acidification and thermal stress
Sci. Total Environ.
Some like it hot: temperature and pH modulate larval development and settlement of the sea urchin Arbacia lixula
J. Exp. Mar. Biol. Ecol.
The effects of food and temperature on settlement of Aurelia aurita planula larvae and subsequent somatic growth
J. Exp. Mar. Biol. Ecol.
Combined effects of seawater acidification and high temperature on hemocyte parameters in the thick shell mussel Mytilus coruscus
Fish Shellfish Immunol.
Ocean acidification compromises recruitment success of the threatened Caribbean coral Acropora palmata
Proc. Natl. Acad. Sci. U.S.A.
Larval settlement behavior in the jellyfish Aurelia aurita (Linnaeus)(Scyphozoa: Semaeostomeae)
Estuaries
Multistressor impacts of warming and acidification of the ocean on marine invertebrates' life histories
Integr. Comp. Biol.
Oceanography: anthropogenic carbon and ocean pH
Nature
Massive consumption of gelatinous plankton by Mediterranean apex predators
PLoS One
Effects of ocean acidification on invertebrate settlement at volcanic CO2 vents
Mar. Biol.
Temperature affects the early life history stages of corals more than near future ocean acidification
Mar. Ecol. Prog. Ser.
Interactive and cumulative effects of multiple human stressors in marine systems
Ecol. Lett.
Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species
Proc. Natl. Acad. Sci. U.S.A.
High CO2 reduces the settlement of a spawning coral on three common species of crustose coralline algae
Mar. Ecol. Prog. Ser.
Ocean acidification reduces coral recruitment by disrupting intimate larval-algal settlement interactions
Ecol. Lett.
Losers and winners in coral reefs acclimatized to elevated carbon dioxide concentrations
Nat. Clim. Change
Temperature-dependent settlement of planula larvae of two scyphozoan jellyfish from the North Sea
Estuar. Coast Shelf Sci.
Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios
Science
Approaches and tools to manipulate the carbonate chemistry
Impact of ocean warming and ocean acidification on marine invertebrate life history stages: vulnerabilities and potential for persistence in a changing ocean. Oceanography and Marine Biology
Annu. Rev.
The secret lives of jellyfish: long regarded as minor players in ocean ecology, jellyfish are actually important parts of the marine food web
Nature
Cited by (8)
Physiological and transcriptomic responses of Aurelia coerulea polyps to acidified seawater conditions
2024, Marine Environmental ResearchPotential distribution of Crassostrea sikamea (Amemiya, 1928) along coastal China under global climate change
2024, Global Ecology and ConservationCoastal acidification and deoxygenation enhance settlement but do not influence movement behaviour of creeping polyps of the Irukandji jellyfish, Alatina alata (Cubozoa)
2020, Marine Environmental ResearchCitation Excerpt :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).
Research progress on the ecological roles of 'marine ecosystem engineers'
2022, Chinese Journal of Applied Ecology