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Ocean Acidification Causes Mortality in the Medusa Stage of the Cubozoan

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Ocean Acidification Causes Mortality in the Medusa Stage of the Cubozoan www.nature.com/scientificreports OPEN Ocean acidifcation causes mortality in the medusa stage of the cubozoan Carybdea xaymacana Received: 3 January 2019 Pierre J. C. Chuard 1, Maggie D. Johnson2 & Frédéric Guichard3 Accepted: 25 March 2019 Ocean pH is decreasing due to anthropogenic activities, and the consequences of this acidifcation on Published: xx xx xxxx marine fauna and ecosystems are the subject of an increasing number of studies. Yet, the impact of ocean acidifcation (OA) on several abundant and ecologically important taxa, such as medusozoans, is poorly documented. To date there have been no studies on the efect of post-2050 OA projections on the medusa stage of jellyfsh. As medusae represent the reproductive stage of cnidarians, negative impacts on adult jellyfsh could severely impact the long-term survival of this group. Using a laboratory experiment, we investigated the efect of 2300 OA projections (i.e. pH of 7.5) on the mortality rate of the medusa-stage of the cubozoan species Carybdea xaymacana, compared to ambient seawater pH conditions (i.e. pH of 8.1). After a 12-h exposure to OA, C. xaymacana medusae sufered higher mortality rates compared to ambient conditions. This study represents the frst evidence of the potential lethal efects of post-2050 OA projections on jellyfsh. The higher metabolic rates of cubozoans compared to other cnidarians might make box jellyfsh more vulnerable to OA. A decrease in the density of cnidarians could lead to harmful ecological events, such as algal blooms. By 2300, surface ocean pH levels are predicted to decrease by 0.67 units compared to pre-industrial levels1. Tese altered pH conditions (known as ocean acidifcation; OA) are a result of increasing anthropogenic carbon dioxide emissions2. It is well established that OA has detrimental efects on biological processes in several marine organ- isms, particularly calcifcation of invertebrates3. Other potential harmful efects of OA include acidosis4, a process that can lead to reduced metabolic rates5. Jellyfsh populations seem to have grown recently (but see Condon et al.6) and have the potential to dominate surface water biomass7 (i.e. jelly blooms). Te increasing biomass of jellyfshes, sometimes followed by waves of high mortality, is suspected to infuence the ocean biological pump8. Indeed, these high-mortality events allow for more carbon to be sequestered into the ocean foor, and thus increase the capacity of oceans to act as CO2 sinks. Te ocean biological pump is a key mechanism transferring nutrients from surface to deep-ocean ecosystems9, thus connecting ocean food webs over large scales. However, we know little about the biology of many regionally dominant jellyfsh species10. Moreover, though specifc-mechanisms causing jellyfsh blooms are uncertain7,11, climate-driven environmental changes likely play an important role. Understanding the efects of climate-driven stressors on jellyfsh is essential to determining their role within changing ocean ecosystems10,12 (e.g. changes in contribution to climate change mitigation through increase or decrease in population size). Research on the effects of changes in pH on jellyfish species remains limited (Table 1). Within possible long-term OA projection scenarios (i.e. using alkaline pH treatments), these few studies found positive and neg- ative non-lethal efects of pH on jellyfshes, depending on life stages and species, and have led to the general perception that jellyfsh are relatively resilient to OA13. Tus far, only a pH below 4.5 (far more acidic than OA projections) led to mortality in polyps of the moon jellyfsh Aurelia aurita14. Only one study investigated the reproductive life stage of jellyfsh (i.e. medusa)13 in response to short-term (2050) OA projections, and no study has investigated the efects of longer-term OA scenarios on medusae despite their importance for the mainte- nance of genetic diversity within populations. More empirical evidence is necessary to determine the overall resilience of jellyfshes to OA using more species and understudied life-stages. Carybdea xaymacana Conant, 1897 is an abundant cubozoan found in most coastal waters in the tropics and subtropics15. C. xaymacana is a small box jellyfsh (i.e. bell height <3 cm) with four arms each connecting a 1Department of Biological Sciences, Bishop’s University, Sherbrooke, QC, J1M 1Z7, Canada. 2Smithsonian Marine Station, Fort Pierce, FL, USA. 3Department of Biology, McGill University, Montreal, QC, H3A 1B1, Canada. Correspondence and requests for materials should be addressed to P.J.C.C. (email: [email protected]) SCIENTIFIC REPORTS | (2019) 9:5622 | https://doi.org/10.1038/s41598-019-42121-0 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Study Class Species Life stages Lowest pH treatment Efects Swimming inhibited (pH ≤ 6.37) and Kikkawa et al.29 Scyphozoa Aurelia sp. Ephyra 6.15 inverted arms Winans and Purcell43 Scyphozoa Aurelia labiata Polyp; ephyra 7.2 Smaller statoliths in ephyrae Klein et al.23 Cubozoa Alatina nr mordens Polyp 7.6 Slower reproduction Cyanea capillata; Lesniowski et al.44 Scyphozoa Polyp 7.9 None Chrysaora hysoscella Alguero-Muniz et al.45 Scyphozoa Aurelia aurita Ephyra 7.28 Slower growth Tills et al.46 Scyphozoa Aurelia aurita Ephyra 7.6 Smaller size and lower pulsation rate Increased larvae settlement and tissue Goldstein et al.14 Scyphozoa Aurelia aurita Planula larva; polyp 7.4 (larva) 2 (polyp) degradation (pH < 6.5) and mortality (pH < 4.5) of polyps Reproductive and protein content resilience, and increased early Klein et al.24 Cubozoa Alatina alata Polyp 7.55 respiration rate under predicted temperature increase. Decreased prey capture rates Hammill et al.13 Cubozoa Carybdea rastoni Medusa 7.77 Increased foraging rates Treible et al.47 Scyphozoa Aurelia aurita Polyp 7.62 None Table 1. Details from all known studies that investigated the efects of pH on jellyfsh species. ‡ −1 −1 Treatment T (°C) Salinity (psu) pH AT (μmol kg ) pCO2 (µatm) DIC (μmol kg ) ΩΑr Control 28 (±0.4) 2279 8.1 2279 511 2003 3.12 Reduced pH 28 (±0.4) 2277–2287 7.48–7.55 2277–2287 2115–2579 2236–2273 0.89–1.05 Table 2. Physical parameters for each treatment. We measured temperature twice daily. We measured salinity, and collected water sampled for total alkalinity (AT) and pH once for the control treatment (i.e. between the two trial blocks), and twice for the reduced pH treatment (i.e. between and afer the two trial blocks). We derived ‡ pCO2, DIC, and ΩAr from measured values of AT, salinity and pH using CO2SYS. NBS scale. tentacle to the box-shaped bell that is characteristic to cubozoans16–18. With tentacles expanding up to 20 cm, it feeds on zooplankton and small pelagic organisms18. C. xaymacana inhabits calm bays, including our study site in the Caribbean Sea (Bahía de Almirante, Panama). To our knowledge, C. xaymacana has not been the focus of experimental manipulations other than basic taxonomic descriptions18, and some studies investigating the venomousness for which cubozoans are infamous19,20. Te Cubozoa class (Cnidaria) encompasses approximately 50 known species21, whereas the Scyphozoa class (Cnidaria) includes more than 200 described species22. Tis diference, along with the fact that scyphozoans are usually the cause of jelly blooms7, might explain the lower representation of cubozoans compared to scyphozoans in the OA literature (i.e. 3 species; Table 1). Te efects of OA on box-jellyfshes has only been investigated in three other species (Alatina nr mordens23, Alatina alata24, and Carybdea rastoni)13 down to a pH of minimum 7.5524, which does not encompass 2300 OA projections (i.e. 7.51). In the present study, we address these knowledge gaps by investigating long-term OA scenario (pH = 7.5 in 23001) efects on the medusa life stage of C. xaymacana. We exposed groups of individuals in the laboratory to either ambient (pH = 8.1) or reduced pH (pH = 7.5) seawater. We predicted that jellyfsh would survive our lower experimental pH treatment given the reported resilience of jellyfsh to OA (Table 1). Given the physiological dif- ferences between scyphozoan and cubozoan medusae (e.g. higher metabolic rates in box jellyfshes compared to true jellyfshes)25, studies investigating the efects of post-2050 OA projections on adult cubozoans are needed to improve predictions regarding the fate of cnidarians in changing oceans. Results Treatment conditions. As expected, optical dissolved oxygen (ODO) and salinity were similar between treatments. We were able to maintain treatment conditions throughout the duration of the experiment (Table 2). Indeed, ODO and salinity were 5.93–6.10 mg l−1, and 35 psu for the control; 5.88–6.12 mg l−1, and 36 psu for the reduced pH treatment respectively. Tese values were comparable to the sampling site (7.42 mg l−1, 36 psu for ODO and salinity respectively). Te average of the two measurements of pHT and AT in the reduced pH treatment were 7.52 and 2282 µmol kg−1 of seawater respectively. Te diferences between the two measurements for both pHT and AT were small (<1% diference between measurements on average). Te single measurement of the con- trol treatment between the two trial blocks had a pHT of 8.10, comparable to the seawater pHT measured at the sampling site a few minutes before (8.07 pHT). Finally, pCO2 of the control treatment was 511 µatm. Mortality rates. We observed mortality at a rate of 35% (±19% s.e.m.) in the reduced pH treatment afer 12 h and no mortality in the control treatment. Tese mortality rates were signifcantly greater in the reduced pH treatment than in the control (regression coefcient: 3.79, [95% confdence interval: 0.89, 6.69], z score: 2.57, P = 0.010). In addition, compared to the control, most living individuals in the reduced pH treatment displayed signs of poor health, such as general lethargy, loss of tentacles, everted bells, and inefective bell movement.
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