Editorial: Biological models for the study of ocean acidification: From molecules to ecosystems
Camilla Della Torre
Maria Cristina Gambi
Rosa Freitas
Marco Munari- 1Department of Biosciences, University of Milan, Milan, Italy
- 2National Institute of Oceanography and Applied Geophysics, OGS, Trieste, Italy
- 3Departamento de Biologia & Centre for Environmental and Marine Studies (CESAM), Universidade de Aveiro, Aveiro, Portugal
- 4Department of Integrative Marine Ecology, Stazione Zoologica Anton Dohrn, Fano Marine Centre, Fano, Italy
Editorial on the Research Topic
Biological models for the study of ocean acidification: From molecules to ecosystems
The increase of CO2 emissions in the atmosphere is considered one of the main drivers of global climate change. Higher atmospheric CO2 concentrations generate the ocean acidification phenomenon (OA), occurring at the global ocean scale (Vargas et al., 2022), which is posing a risk to ocean biodiversity and ecosystem functioning (Nagelkerken and Connell, 2015). For this reason, there has been an increase in research on OA and important conceptual and methodological efforts in the last decade, in order to better understand how organisms would cope with OA and to foster conservation and restoration of marine ecosystems in a high-pCO2/low pH scenario. Studies carried out under laboratory conditions have described detrimental effects due to OA across many taxa, highlighting strong species/population-specific sensitivity (Kroeker et al., 2010; Asnicar et al., 2021). Although most of the research has been focused on short/middle-term laboratory/mesocosm experiments usually on single species or a single stage of their life cycle, they have proved useful to understand the physiological effects of OA and the plasticity of individual species/populations. On the other hand, lab simulation experiments do not allow comprehensive predictions of the effects on ecological processes. In this respect, studies carried out in naturally acidified systems (e.g., hydrothermal vent systems and ice melting fronts) help to fill this gap, highlighting the ability of some organisms to survive and thrive under high-pCO2/low pH conditions (Foo et al., 2018; Palombo et al., 2023).
There is now mounting evidence that the response of organisms to OA is a complex puzzle of mechanisms and processes at different scales of biological organization, from genetic (Pespeni et al., 2013) and molecular modifications (Wäge et al., 2018) to ecophysiological performances (Calosi et al., 2013) and the biological traits of the organisms (Gambi et al., 2016), up to ecological interactions such as facilitation, competition (Kroeker et al., 2013; Nagelkerken et al., 2017), and predatory/prey interactions (Ghedini and Connell, 2017), which are still largely unknown and mostly considered singularly.
In this view, the aim of the current topic was to collect papers that could help to identify model species to study the effects of OA on different biological hierarchical levels, from genes to populations, using different approaches in order to better predict how this phenomenon may influence population structure and species interactions, shaping marine communities in the future ocean of the Anthropocene.
The main outcomes of papers submitted to this Research Topic are:
1 The tolerance to high pCO2/low pH is energy-consuming and might occur at the expense of other physiological functions
This consideration has been achieved in two papers of the Research Topic. The first was carried out using the polychaete Platynereis spp. as a model species and investigating a population inhabiting the CO2 vents system of Castello Aragonese on the island of Ischia (Italy), which is considered to be adapted to OA (Signorini et al.). Through the application of the metabolomic approach, it was possible to observe a downregulation of purine and pyrimidine metabolism and a reduction in the content of fatty acids in polychaetes subjected to OA compared to controls. This suggests that an expenditure of energetic reserves is necessary to maintain the basic metabolism under stressful conditions. The second study focused on the calcifying mollusk Ameghinomya antiqua, which was exposed in the laboratory to OA and thermal stress (Martel et al.). Clams were able to persist during the 90 days of exposure, but in this case the survival under stressful conditions implied an investment of energy at the expense of growth and shell formation, potentially also affecting the ecosystem services related to the harvest of this species.
2 Epigenetic modifications as a molecular mechanism potentially underpinning tolerance to OA
The paper on Platynereis spp. from the CO2 vents system on the island of Ischia (Signorini et al.) provided the first evidence of the potential involvement of histone posttranslational modifications (in particular acetylation) in promoting tolerance to OA. This information contributes to increasing the current understanding of the role of epigenetic variations as molecular mechanisms underlying acclimatization/adaptation to environmental stressors in marine species.
3 OA impacts negatively on coral reef carbonate accretion rates
Another study employed a natural wide-scale gradient of OA represented by the coral reefs associated with the US Pacific Islands (Barkley et al.). A decennial (2010-19) variation of the aragonite saturation state (Ωar) was correlated with several metrics such as the benthic cover, genera, and morphology of coral communities, as well as the net carbonate accretion. In this natural OA gradient, the authors did not find a correlation between Ωar variation and the composition of reef communities. Conversely, the decrease in net carbonate accretion was strongly correlated with Ωar. The study pointed out that the measurements of calcification and accretion rates are effective tools for monitoring the adverse impacts of OA on reef ecosystems, and they are more sensitive than other metrics related to benthic community composition.
4 The evolution of the DIC carbon isotope signature under OA and its implication for laboratory culturing of marine organisms
This represents a methodological paper where the stable isotope approach is used to better understand the physiological processes contributing to the response of organisms to ocean acidification (Zhang et al.). To simulate OA in laboratory cultures, the direct bubbling of seawater with CO2 is a preferred method because it adjusts pCO2 and pH without altering the total alkalinity. Frequently, the dissolved inorganic carbon (DIC) in the initial seawater culture has a distinct 13C/12C ratio, which is far from the equilibrium expected with the isotopic composition of the bubbled CO2, and this aspect is sometimes ignored. To overcome this problem, the authors have proposed a numerical model that can well predict the DIC carbon isotope ratio and its evolutions during bubbling, which can be traced during the experiment. Their simulations show that, if not properly accounted, CO2 bubbling can lead to large errors in estimated carbon isotope fractionation between seawater and biomass or biominerals, consequently affecting interpretations and hampering comparisons among different experiments.
Author contributions
All authors listed have made a substantial, direct, and intellectual contribution to the work and approved it for publication.
Conflict of interest
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References
Asnicar D., Novoa-Abelleira A., Minichino R., Badocco D., Pastore P., Finos L., et al. (2021). When site matters: Metabolic and behavioural responses of adult sea urchins from different environments during long-term exposure to seawater acidification. Mar. Environ. Res. 169, 105372. doi: 10.1016/j.marenvres.2021.105372
Calosi P., Rastrick S. P. S., Lombardi C., de Guzman H. J., Davidson L., Jahnke M., et al. (2013). Adaptation and acclimatization to ocean acidification in marine ectotherms: an in situ transplant experiment with polychaetes at a shallow CO2 vent system. Phil. Trans. R. Soc B. 368, 20120444. doi: 10.1098/rstb.2012.0444
Foo S. A., Byrne M., Ricevuto E., Gambi M. C. (2018). The carbon dioxide vents of ischia, Italy, a natural system to assess impacts of ocean acidification on marine ecosystems: An overview of research and comparisons with other vent systems. Oceanogr. Mar. Biol. 56, 237–310. doi: 10.1098/rstb.2012.0444
Gambi M. C., Musco L., Giangrande A., Badalamenti F., Micheli F., Kroeker K. J. (2016). Distribution and functional traits of polychaetes in a CO2 vent system: winners and losers among closely related species. Mar. Ecol. Prog. Ser. 550, 121–134. doi: 10.3354/meps11727
Ghedini G., Connell S. D. (2017). Moving ocean acidification research beyond a simple science: Investigating ecological change and their stabilizers. Food Webs. 13, 53–59. doi: 10.1016/j.fooweb.2017.03.003
Kroeker K. J., Kordas R. L., Crim R. N., Singh G. G. (2010). Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419–1434. doi: 10.1111/j.1461-0248.2010.01518.x
Kroeker K., Micheli F., Gambi M. (2013). Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat. Clim. Change 3, 156–159. doi: 10.1038/nclimate1680
Nagelkerken I., Connell S. D. (2015). Global alteration of ocean ecosystem functioning due to increasing human CO2 emissions. Proc. Natl. Acad. Sci. Unit. States Am. 112, 13272–13277. doi: 10.1073/pnas.1510856112
Nagelkerken I., Goldenberg S. U., Ferreira C. M., Russell B. D., Connell S. D. (2017). Species interactions drive fish biodiversity loss in a high-CO2 world. Curr. Biol. 27, 2177–2184. doi: 10.1073/pnas.1220673110
Palombo C., Chiarore A., Ciscato M., Asnicar D., Mirasole A., Fabbrizzi E., et al. (2023). Thanks mum. maternal effects in response to ocean acidification of sea urchin larvae at different ecologically relevant temperatures. Mar. Pollut. Bull. 188, 114700. doi: 10.1016/j.marpolbul.2023.114700
Pespeni M. H., Sanford E., Gaylord B., Hill T. M., Hosfelt J. D., Jaris H. K., et al. (2013). Evolutionary change during experimental ocean acidification. Proc. Natl. Acad. Sci. Unit. States Am. 11, 6937–6942. doi: 10.1073/pnas.1220673110
Vargas C. A., Cuevas A. L., Broitman B. R., San Martin V. A., Lagos N. A., Gaitán-Espitia J. D., et al. (2022). Upper environmental pCO2 drives sensitivity to ocean acidification in marine invertebrates. Nat. Clim. Change 12, 200–207. doi: 10.1038/s41558-021-01269-2
Keywords: ocean acidification, biological models, stress ecology, marine invertebrates, plasticity
Citation: Della Torre C, Gambi MC, Freitas R and Munari M (2023) Editorial: Biological models for the study of ocean acidification: From molecules to ecosystems. Front. Mar. Sci. 10:1166708. doi: 10.3389/fmars.2023.1166708
Received: 15 February 2023; Accepted: 21 February 2023;
Published: 02 March 2023.
Edited and Reviewed by:
Christopher Edward Cornwall, Victoria University of Wellington, New ZealandCopyright © 2023 Della Torre, Gambi, Freitas and Munari. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Camilla Della Torre, camilla.dellatorre@unimi.it