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Impact of ocean warming and ocean acidification on asexual reproduction and statolith formation of the symbiotic jellyfish Cotylorhiza tuberculata

['Angélica Enrique-Navarro', 'Department Of Ecology', 'Coastal Management', 'Instituto De Ciencias Marinas De Andalucia', 'Csic', 'Puerto Real', 'Cadiz', 'I. Emma Huertas', 'Manuel Jesús León Cobo', 'Laura Prieto']

Date: 2021-08

Ocean acidification and warming are challenging marine organisms and ecosystems around the world. The synergetic effects of these two climate change stressors on jellyfish remain still understudied. Here, we examine the independent and combined effects of these two environmental variables on polyp population dynamics of the Mediterranean jellyfish Cotylorhiza tuberculata. An experiment was conducted to examine asexual reproduction by budding and strobilation considering current and ca. 2100 winter (Trial 1, 36 days) and summer (Trial 2, 36 days) conditions under the RCP8.5 (IPCC 2013). In Trial 1, a temperature of 18°C and two pH levels (current: 7.9 and, reduced: 7.7) were tested. Trial 2 considered two temperature levels 24°C and 30°C, under current and reduced acidification conditions (8.0 and 7.7, respectively). Ephyrae size and statolith formation of released ephyrae from polyps exposed to summer temperatures under both acidification treatment was also analyzed. Zooxanthellae density inside the polyps throughout the experiment was measured. C. tuberculata polyps could cope with the conditions mimicked in all experimental treatments and no significant effect of pH, temperature, or the combination of both variables on the abundance of polyps was observed. At 18°C, strobilation was reduced under high P CO2 conditions. Under summer treatments (24°C and 30°C), percentage strobilation was very low and several released ephyrae suffered malformations and reduced size, as a consequence of reduced pH and elevated temperatures, separately. The number of statoliths was not affected by pH or temperature, however, bigger statoliths were formed at elevated temperatures (30°C). Finally, zooxanthellae density was not affected by experimental conditions, even if, the duration of the experiment significantly affected symbiont concentration. Our results show that even though polyps of C. tuberculata would thrive the future worst scenario predicted for the Mediterranean Sea, their capacity to undergo a proper strobilation and to produce healthy ephyrae will be more vulnerable to climate induced environmental conditions, thereby affecting medusae recruitment and, therefore, population dynamics of the species.

Funding: This work was funded by the Spanish Ministerio de Ciencia, Innovación y Universidades ( https://www.ciencia.gob.es ) under grant number CTM2016-75487-R for the project MED2CA. AEN was financially sustained by a Ph.D. fellowship from the MED2CA project ( https://med2ca.csic.es ). This work is a contribution to the CSIC interdisciplinary thematic platform, WATER:iOS and the Project Agreement "Sistema de Observación y Predicción de Medusas en el Mar Balear” among Govern des Illes Balears, SOCIB and CSIC.

Copyright: © 2021 Enrique-Navarro et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Introduction

The world’s oceans are becoming warmer and more acidic as a consequence of the rapid rise of atmospheric carbon dioxide (CO 2 ) concentrations. The ocean mitigates the greenhouse effect by storing excess heat from global warming and by absorbing and storing anthropogenic CO 2 [1, 2]. However, this contribution is leading to an increase in seawater temperatures and a gradual decrease of pH, known as ocean acidification (OA) [3]. Since preindustrial times the global ocean temperature has increased by 0.5°C and global average pH has declined by 0.1 units [4–6]. By 2100, under a “high CO 2 emissions” scenario (RCP8.5, [4]), sea surface temperature is predicted to rise between 2.6 and 4.8°C, and seawater pH to be reduced by 0.32.

The effects of OA and ocean warming on marine ecosystems are being extensively studied to assess their consequences on organisms physiology and future populations trends [7]. Major research has been however, focused on calcifying species [8] due to the direct effects of OA on carbonate chemistry, as the concentration of calcium carbonate decreases as does pH [9]. Alternatively, non-calcifying organisms remain understudied [10, 11] even though it has been suggested that at a community level and within the same trophic level, species more tolerant to high CO 2 might displace others more vulnerable to elevated P CO2 [12–14]. This tendency, would lead to the proliferation of opportunistic species, such as jellyfish, with a higher resilience to warming and acidification [15]. Therefore, assays combining exposure to changing temperature and P CO2 in non-calcifying organisms are needed to disentangle biological responses and adaptation to future climate change conditions [16].

During the last two decades, the occurrence of jellyfish blooms has been linked to human-driven ecosystem changes [17] and environmental variations [12, 18]. Many factors have been attributed to influence the abundance of jellyfish, such as overfishing [19], eutrophication [18, 20], temperature increase [21–23] and OA [5, 15, 24].

Scyphozoan jellyfish have a complex bipartite life cycle with alternation of a pelagic sexual stage (medusa) and benthic asexual stage (polyp). Higher temperatures generally leads to increased rates of asexual reproduction of polyps [25]. Yet, the consequences of OA on jellyfish populations remain still diffuse. Despite some early field studies suggested a direct correlation between decreasing seawater pH and abundance of gelatinous zooplankton [26, 27], no direct evidence exists to relate increasing jellyfish blooms and OA [28]. The first laboratory study on the influence of OA on jellyfish polyps showed that survival and asexual reproduction of Aurelia labiata polyps were unaffected by experimental conditions [15]. To our knowledge, there are only a few studies focused on the simultaneous effects of warming and acidification on jellyfish polyps using a realistic end-of-the-century climate scenario, and all of them have dealt with cubozoan species [24, 29, 30]. Polyps of the Irukandji jellyfish Alantina nr mordens were able to cope with warming but, their budding capacity decreased by lowering seawater pH, thereby limiting their possibilities to thrive [24]. On the other hand, polyps of Carukia barnesi showed tolerance to extreme conditions [30]. Despite asexual reproduction appears to be independent of the environmental forcing imposed by both stressors, higher respiration and metabolic rates have been reported in response to warming and OA [29]. Similar results regarding asexual reproduction of scyphozoan polyps were obtained when combining reduced pH with low oxygen concentrations [31, 32]. Recent laboratory studies have tested the effects of OA on other jellyfish life stages, from planula larvae [33, 34] to ephyrae [31, 32, 35] and even on adult medusae [36–38]. The differential responses reported seem to be related to the magnitude of the stressors, life stage, and species-specific tolerance limits.

Massive occurrences of jellyfish populations have been considered a threat to Mediterranean planktonic communities [39]. As the Mediterranean Sea is already experiencing the impact of climate change [40], it has become a priority to elucidate how the future expected warming and acidification conditions will influence jellyfish dynamics due to the important repercussions for biodiversity and ecosystem functioning.

In this work, we examine the combined effects of warming and acidification on the polyp population dynamics of the jellyfish Cotylorhiza tuberculata, one the most common bloom forming Mediterranean scyphozoans. This species reaches very high abundances during summer in shallow semi-enclosed marine areas, such as Vlyho Bay in Greece [41] and, the Mar Menor coastal lagoon in Spain [42], where annual blooms cause economic losses mainly associated with tourism [43]. C. tuberculata polyps reproduce asexually by generating free-swimming buds [44], when lateral outgrowth from the parental polyp is released, swims around before attaching and becomes a new polyp. The transition from benthic to pelagic stage also occurs by asexual reproduction, when polyps undergo monodisc-type strobilation, with every single polyp generating one single ephyra [41]. Also, C. tuberculata harbors endosymbiotic dinoflagellates of the family Symbiodiniaceae [45]. Despite zooxanthellae seem to play a modest role in the polyp stage [46], their presence is indispensable for strobilation [41]. Temperature is known to control survival and asexual reproduction of C. tuberculata polyps [46]. However, rising temperatures will be accompanied by decreasing pH in the future and therefore, it is critical to investigate the interactive effect of these two stressors to better predict the jellyfish population trends in the future.

Our experiments tested predicted future values of temperature and pH expected to occur in the Mediterranean Sea by the end of the current century under the RCP8.5 [4] scenario. Moreover, we investigated the influence of both stressors on the formation of statoliths, a crystal immersed in the sense organ statocyst, known to play a key role in medusa equilibrium [47, 48].

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