Cultivating marine macroalgae in CO2-enriched seawater: A bio-economic approach
Introduction
Present day atmospheric CO2 levels approximate 400 ppm and in the era of global changes, within this century, they are expected to reach 900–1200 ppm, while temperatures are predicted to increase by 2–4 °C (Gao et al., 2019; Stocker et al., 2013). As shallow coastal areas will equilibrate with atmospheric CO2 (Reum et al., 2016), leading to important changes in seawater chemistry (Connell et al., 2013; Qu et al., 2017). As a result, the average seawater pH is expected to drop by approximately 0.46 units from current levels (Kang and Kim, 2016; Cornwall et al., 2012) while CO2 and HCO3−, the main inorganic carbon (Ci) substrates for aquatic photosynthesis will increase (Kang and Kim, 2016). Higher CO2 may increase net primary production either directly, especially under globally increasing temperatures (Connell et al., 2013), or indirectly, by reducing the survival of calcified marine organisms that feed on algae (Cornwall et al., 2012). Global warming and ocean acidification are likely to impact the physiological traits of marine algae (Zhang et al., 2020).
For most marine macroalgae (seaweeds), CO2 and HCO3− are the main sources of inorganic carbon (Ci) for photosynthesis and growth. While CO2 enters the cell by diffusion, HCO3 requires the presence of CO2 concentrating mechanisms (CCMs) to become available for fixation into stable compounds, namely sugars (Ji et al., 2016). High seawater CO2 concentrations could directly affect CCMs in many species because it increases the dependence of carbon by diffusion (Kang and Kim, 2016). In addition, down-regulation of CCMs appears through lower HCO3− usage and higher reliance on CO2 utilization (Gao et al., 2012). Unlike species with weak or non-existent CCMs, which usually benefit more from ocean acidification (Gao et al., 2019), seaweed species with CCMs can shift from HCO3− to aqueous CO2 when CO2 levels are high (Cornwall et al., 2012). The low CO2 level in seawater, combined with the higher saturation constant of Rubisco and the slow rate of CO2 diffusion, make CO2 a common limiting factor for algal growth (Gao et al., 2019). Whether a marine alga will respond to external elevated CO2 levels depends on its method and degree of HCO3− utilization, and on the environmental conditions under which Ci enrichment is imposed. As photosynthesis generally translates into growth and biomass production, these expected global changes in Ci and temperature will significantly affect the economics of the seaweed industry.
In the eastern Mediterranean Sea, and especially in the Levantine basin, marine organisms experience higher temperatures and salinity and more oligotrophic conditions as compared to their counterparts in other sea basins. The eastern Mediterranean has warmed up by 1.5–3 °C in the past three decades (Guy-Haim et al., 2016). These local and global climate changes, which are anthropogenic in origin, are affecting marine ecosystems by changing water chemistry and temperature. Israel and Hophy (2002) investigated the short-term response of several seaweeds, when exposed to elevated dissolved CO2 levels. In general, growth rate, maximal photosynthesis rate and Rubisco responses were not significantly affected by doubling dissolved CO2 levels in most of the species studied.
In contrast to terrestrial plants, seaweeds grow in seawater and are highly productive offering an attractive option for a variety of bio-products among them gels for the food industry (Mata et al., 2016). Seaweeds are represented by more than a 6 billion USD industry in which most of the biomass production is from aquaculture, while only a smaller fraction is harvested from naturally growing macroalgae (Lähteenmäki-Uutela et al., 2021). Currently, seaweeds are cultivated mainly in coastal waters (Valderrama et al., 2013), with global production of about 30 million tons fresh weight (FW) in 2015 (Buschmann et al., 2017). Recently, seaweeds became particularly attractive due to their nutritional benefits (Chen et al., 2018), high levels of antioxidants, omega-3 oil (Ryckebosch et al., 2014), carbohydrates (Laurens et al., 2015) and proteins (Rasala and Mayfield, 2015). Seaweeds provide for ecosystem services as provisioning services including human food, fertilizers, cosmetics and pharmaceuticals (Milledge et al., 2016; Holdt and Kraan, 2011; Venugopal, 2016; Suganya et al., 2016; Pereira et al., 2013; Lawton et al., 2013) and regulating services such as carbon sequestration and important source of organic matter and oxygen (Doshi, 2017).
According to Mordor Intelligence (www.mordorintelligence.com/industry-reports/global-carrageenan-market-industry), the global carrageenan market could reach US$ 1.45 billion by 2024, with a compound annual growth rate of 8.12% during the forecast period (2019–2024). For the period 2020–2025, the rate for global algae products market is projected to be 5.1%, and for the global algae ingredients market, 8.1%. Marine macroalgae are also important in a more holistic view in an Integrated Multitrophic Aquaculture (IMTA) approach, which combines the cultivation of seaweed with other valuable organisms such as fish and/or shrimp. Using IMTA, the discharged seawater is first purified by algae, which preserves the nutrients (such as nitrogen and phosphorus), enriches the seawater with oxygen, and fixates the CO2 (Posadas et al., 2015). Seaweed that can serve as biological filters is in demand and has high economic value (Smearman et al., 1997). Martinez-Espiñeira et al. (2016) used data from a contingent valuation survey to estimate the non-use benefits of bio-mitigation that reduced the external costs imposed on the marine environment, through the adoption of IMTA for Atlantic salmon aquaculture in Canada and obtained, that the benefits are US$43–65 million per year for the next five years.
Species of Ulva and Gracilaria are common in the intertidal zone. Both seaweeds are cultivated in Israel in a commercial scale to produce food products and valuable chemicals (Israel et al., 2020), generating and overall revenue of US$ 60 million and US$ 2.3 million per year, respectively (Levy and Mozes, 2016). Ulva species are distributed worldwide and are known for causing macroalgal blooms that can have negative environmental and economic impacts (Rautenberger et al., 2015). Nonetheless, Ulva species are generally beneficial to humans. In the field of bioenergy (Qarri and Israel, 2020), several cost-benefit analyses have indicated a net benefit for bioethanol production using biomass of U. rigida, co-cultured with fish in an intensive offshore aquaculture unit (Korzen et al., 2015a, Korzen et al., 2015b). The results were economically debatable, pending the need for more efficient technologies and sustainable biomass supplies. G. conferta is well known for its various uses in the food and medical industries, particularly for food additives and agar production (Pereira et al., 2013). Recently, characterization of biomimetic adhesives from these algae was used for biomedical application (Dimartino et al., 2013). Excessive nutrient scavenging from aquaculture activities is another useful application of these and other seaweed species (Barceló-Villalobos et al., 2017).
Extrapolating the effects of short-term exposure of macroalgae to elevated CO2 to produce long-term ecological or economical valuable predictions is complex, if not impossible (Sage, 1994; Alaswad et al., 2015; Fernand et al., 2017). Hence, long-term trials under CO2 enrichment are important (Kobayasi et al., 2019). Consequently, the first goal of the current study was to determine the effect of CO2 enrichment over a long-time span on the growth responses of two model seaweeds, Ulva rigida and Gracilaria conferta, jointly with the seasonally occurring variable temperatures. We hypothesized these model seaweeds will respond positively by the interaction of CO2 concentration and temperature. Our second objective was to assess the potential profitability of seaweed production using the results of our first goal. To the best of our knowledge this is the first effort made to address profitability in land-based seaweed cultivation setups.
Section snippets
Algal model species
The seaweeds used in the present study were the green alga Ulva rigida and the red alga Gracilaria conferta. U. rigida can be distinguished with ease (Krupnik et al., 2017), while Gracilaria conventional taxonomy has been extensively revised molecularly to Hydropuntia, Crassa and Agarophyton (Gurgel et al., 2018), with G. conferta still to be defined. Both species are stocked at an experimental seaweed setup at Israel Oceanographic and Limnological Research (IOLR), Haifa, Israel (32°49′N,
Results
A quadratic regression (based on Eq. (2)) of the production function was estimated for each macroalgal species at both current and elevated CO2 concentrations. Our dependent variable was the seaweed FW measured weekly during the 11 months experimental period. The independent variable was seawater temperature, while N and P levels were kept at optimal levels for growth. Table 1 presents the results of four regressions models, two for Ulva rigida (one with ambient CO2 and the other with enriched
Discussion
Near-shore marine areas are highly productive ecosystems that provide important economic and social services (Xu and Gao, 2012). Yet these areas are particularly sensitive to the effect of global changes, including ocean acidification and warming. How these ecosystems will respond to increasing atmospheric CO2 is still poorly understood (Reum et al., 2016). During the 1990's, CO2 concentrations were ca. 360 ppm, and they have increased progressively since then to current records of ca. 414 ppm
Credit author statement
Shiri Zemah Shamir: Conceptualization, Methodology, Data curation, Writing- Original draft preparation, Ziv Zemah Shamir: Conceptualization, Methodology, Data curation, Writing- Original draft preparation, Anat Tchetchik: Visualization, Investigation, Abraham Haim: supervision, Dan Tchernov: supervision, Álvaro Israel: supervision, Project administration.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
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