Ocean Acidification

Ocean acidification (OA) is one of the most significant threats to marine organisms and is linked to climate change. It occurs when anthropogenic CO2 is absorbed by the oceans, resulting in a decrease in seawater pH and the dissolution of calcium carbonate. Projections indicate that OA will exacerbate in the future, highlighting the need to understand its impact on marine ecosystems. Much of our knowledge about the effects of OA comes from laboratory experiments, as predicting responses in natural conditions is challenging. Therefore, studies focusing on species living in naturally acidified systems, such as shallow CO2 seeps or vents, are becoming increasingly popular to obtain more realistic predictions.

This doctoral thesis, consisting of 5 chapters, explores the effects of ocean acidification on benthic communities in the subtropical Atlantic Ocean, using the naturally acidified CO2 vent system off the southern coast of La Palma Island in the Canary Islands, Spain, as a natural laboratory. Chapter 1 serves as an introduction to this thesis, explaining what naturally acidified systems are and discussing the research conducted in various locations worldwide where they have been discovered. Specifically, it focuses on studies that have utilized CO2 vents, which originate from volcanic activity. This chapter provides an overview of the importance, advantages, and disadvantages of using these acidified systems as natural laboratories to study OA in situ. It highlights that although there is no perfect analogue for future oceans, these systems help us to better understand the direct and indirect impacts of OA on different marine communities.

Among all the CO2 vents in the world, one of the few naturally acidified shallow systems in the Atlantic Ocean, and the only one with subtropical communities is located off the southern coast of Fuencaliente municipality in La Palma Island, Canary Islands. Chapter 2 of the thesis characterizes the chemical properties of this natural CO2 system in La Palma. It provides information about its volcanic and hydrological origins, as well as the different emission points along the Punta de Fuencaliente. Furthermore, it describes the carbon dynamics of the system, including variations in total inorganic carbon (CT) from 2120.10 to 10784.84 μmol kg-1, alkalinity (AT) from 2415.20 to 10817.12 μmol kg-1, pH from 7.12 to 8.07, aragonite saturation state (Ω) from 0.71 to 4.15, and calcite Ω from 1.09 to 6.49 units. A high CO2 emission flux ranging from 2.8 to 28 kg of CO2 d-1 has also been detected, making this zone an important natural carbon source. Due to its origins, this acidified system presents disadvantages as a natural laboratory for studying OA, such as natural fluctuations caused by tides or additional input of alkaline substances. Nevertheless, it creates a natural gradient of CO2 or pH along the coast with chemical characteristics very similar to those predicted for future scenarios, making it an exceptional location for studying the long-term and multi-level effects of acidification on marine ecosystems.

Chapter 3 explores rocky benthic communities along the natural pH gradient generated by the CO2 vent system in front of Punta de Fuencaliente. The objective of this chapter was to understand the direct and indirect effects of OA on the diversity and species composition of these subtropical marine communities. The study utilized a high-resolution molecular technique called DNA metabarcoding, which sequences fragments of the mitochondrial gene Cytochrome C Oxidase subunit I (COI) to detect the actual species diversity in each area. In this chapter, metabarcoding analysis reveals, for the first time, high levels of taxonomic diversity in a naturally acidified area. These high levels of diversity are attributed to the detection of small and cryptic species that are undetectable by traditional techniques and are tolerant to natural acidification. The results of this chapter unveil that future subtropical communities could maintain high taxonomic diversity values under an acidification scenario, although they will tend toward miniaturization due to the dominance of small algae and invertebrate species. This will have significant consequences for benthic subtropical communities, leading to important changes in ecosystem functions.
It is not the first time that an increase in species diversity related to environmental variations has been detected. In 1978, Connell first proposed the “Intermediate Disturbance Hypothesis” (IDH), which suggests that ecosystems are more diverse when disturbances occur at intermediate scales.

Chapter 4 investigates whether the IDH can be applied to a naturally acidified system at different biological organization levels (from organisms to communities) using molecular data. In La Palma’s acidified system, a fluctuating pH gradient caused by tides can act as a physical disturbance to marine ecosystems. This chapter utilizes sequenced fragments of the mitochondrial COI gene from two species of sea urchins (Arbacia lixula and Paracentrotus lividus) and metabarcoding analyses of benthic communities from the previous chapter. High levels of genetic and taxonomic diversity were detected at both biological organization levels under intermediate pH fluctuation, respectively. Therefore, the results of this chapter support the validity of the IDH in marine ecosystems affected by natural pH fluctuations and at different biological organization levels. Among the species living under natural acidification in the CO2 vents of La Palma, the sea urchin Arbacia lixula stands out. This is because sea urchins, like other calcareous organisms, should be susceptible to acidification due to their calcareous skeletons, however, this species has been found to live apparently unaffected in both Mediterranean and Atlantic CO2 vents.

The final chapter 5 explores the adaptation potential of A. lixula populations along the natural pH gradient of La Palma Island. Using the 2bRADseq molecular technique, a total of 14,883 SNPs (Single Nucleotide Polymorphisms) were detected in 74 individuals, of which 432 loci were correlated with the pH gradient of La Palma and are considered potential SNPs under selection. Analysis of these SNPs demonstrates that despite the short distance between the studied A. lixula populations, significant differences exist in the genomic structure of the populations correlated with the pH gradient. Additionally, these sequences are aligned and compared with available A. lixula transcriptomes, revealing 17 annotated genes involved in biological functions related to growth, development, membrane functions, and calcification. This chapter suggests that A. lixula can adapt to acidification and, therefore, able to withstand future changes anticipated for the oceans.

This thesis is the first to be developed at the Marine Observatory of Climate Change in Punta de Fuencaliente (OMaCC), where the naturally acidified system of La Palma is located. It emphasizes the importance of these natural laboratories in overcoming the experimental limitations of laboratory studies and contributes to understand how subtropical benthic ecosystems may change in the future. Moreover, it has uncovered evidence of local adaptation to ocean acidification in populations living in these natural laboratories. This thesis highlights the importance of these special environments and observatories for future research on the effects of OA.