Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-19T12:29:05.253Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of macroalgal habitats as ocean acidification refugia within coastal seascapes

Published online by Cambridge University Press:  21 March 2023

Carla Edworthy Open the ORCID record for Carla Edworthy [Opens in a new window] ,
Paul-Pierre Steyn Open the ORCID record for Paul-Pierre Steyn [Opens in a new window]  and
Nicola C. James Open the ORCID record for Nicola C. James [Opens in a new window]
Carla Edworthy*
Affiliation:
South African Institute for Aquatic Biodiversity, Makhanda, South Africa Institute for Coastal and Marine Research, Nelson Mandela University, Gqeberha, South Africa
Paul-Pierre Steyn
Affiliation:
Institute for Coastal and Marine Research, Nelson Mandela University, Gqeberha, South Africa Department of Botany, Nelson Mandela University, Gqeberha, South Africa
Nicola C. James
Affiliation:
South African Institute for Aquatic Biodiversity, Makhanda, South Africa Institute for Coastal and Marine Research, Nelson Mandela University, Gqeberha, South Africa
*
Corresponding author: Carla Edworthy; Email: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Ocean acidification (OA) refers to a global decline in the average pH of seawater driven by the absorption of atmospheric carbon dioxide (CO2). Marine macroalgae, while affected by this pH change, are also able to modify seawater pH through their own interaction with inorganic carbon in the carbonate system. Through this action, macroalgae-dominated habitats are potential refugia from OA for associated marine species. This review summarises the most prominent literature on the role of macroalgae in OA mitigation and the potential of macroalgal habitats to serve as OA refugia. It includes a brief overview of macroalgal distribution in an effort to illustrate where such refugia might be most prevalent. Macroalgae influence seawater carbonate chemistry through the absorption of CO2 and HCO3− during photosynthesis, raising surrounding seawater pH in the process. This transient effect on seawater chemistry could provide some respite from the negative effects of OA for many marine species. This refuge role varies over a range of scales along with macroalgal architecture, which varies in size from low-growing turfs to large canopy-forming stands. The associated pH changes can range over various temporal (daily and seasonal) and spatial (from centimetre to kilometre) scales. Areas of high macroalgal biomass are likely to play an important role as significant OA refugia. Such communities are distributed widely throughout the globe. Large brown macroalgae (Laminariales) dominated communities are common in temperate regions, while members of the Fucales are responsible for substantial macroalgal stands in warmer tropical regions. These marine fields and forests have great potential to serve as localised refuges from OA. While more work needs to be done to clarify the effect of macroalgal communities on seawater pH on a large scale, such refuge areas could become important considerations for the management of marine resources and in protected area selection.

Topics structure

Topic(s)

Climate changeConservation and restorationNature-based solutions

Subtopic(s)

Biodiversity and species conservationOcean acidification

Keywords

global changecarbonate chemistryphotosynthesisbiochemistry
Type
Review
Information
Cambridge Prisms: Coastal Futures , Volume 1 , 2023 , e22
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2023. Published by Cambridge University Press

Impact statement

Ocean acidification (OA) is recognised as a significant aspect of global change that will have widespread impacts on marine ecosystems. There has been a recent increase in published research that acknowledges the potential for marine vegetation, such as macroalgae, to modulate local pH conditions through biotic processes and thereby serve as OA refugia for marine organisms. However, the specific role that macroalgae play in the carbonate chemistry dynamics of shallow coastal marine environments has not yet been reviewed in detail. This review assesses the available literature documenting the distribution patterns and structural complexities of macroalgae and how this informs their role in pH modulation over various temporal and spatial extents. A wholistic understanding on the role of macroalgal marine vegetation as OA refugia can facilitate improved local OA management and protected area management to benefit impacted coastal marine species.

Introduction

In the marine environment, ocean acidification (OA) refugia refers to locations where naturally higher pH levels are observed, through biotic or physical drivers, providing periodic or sustained relief from global OA for marine organisms (Kapsenberg and Cyronak, Reference Kapsenberg and Cyronak2019). OA is a consequence of increasing anthropogenic emissions of carbon dioxide (CO2) into the earth’s atmosphere (Caldeira and Wickett, Reference Caldeira and Wickett2003; Sabine et al., Reference Sabine, Feely, Gruber, Key, Lee, Bullister, Wanninkhof, Wong, Wallace and Tilbrook2004; Doney et al., Reference Doney, Fabry, Feely and Kleypas2009). This global process results from increased absorption of atmospheric CO2 by the oceans, which ultimately shifts the carbonate chemistry equilibrium of seawater resulting in a decline in average seawater pH (Doney et al., Reference Doney, Fabry, Feely and Kleypas2009; Dickson, Reference Dickson, Riebesell, Fabry, Hansson and Gattuso2010). Concurrent changes in carbonate chemistry associated with a decline in pH include changes to the concentrations of inorganic carbon, such as an increase in dissolved CO2 and bicarbonate (HCO3−) and a decrease in carbonate ions (CO32−) (Feely et al., Reference Feely, Sabine, Lee, Berelson, Kleypas, Fabry and Millero2004; Dickson, Reference Dickson, Riebesell, Fabry, Hansson and Gattuso2010).

In addition to OA, other natural and anthropogenic processes (e.g., pollution, mariculture, aquaculture, upwelling and freshwater inputs) can result in intensified acidification, resulting in even more complex carbon system dynamics, especially in coastal areas (termed coastal acidification; e.g., Wallace et al., Reference Wallace, Baumann, Grear, Aller and Gobler2014; Doney et al., Reference Doney, Busch, Cooley and Kroeker2020; Isah et al., Reference Isah, Enochs and San Diego-McGlone2022; Savoie et al., Reference Savoie, Moody, Gilbert, Dillon, Howden, Shiller and Hayes2022). These changes in ocean chemistry have implications for marine organisms and ecosystems by reducing carbonate ion availability for calcification (Hofmann et al., Reference Hofmann, Barry, Edmunds, Gates, Hutchins, Klinger and Sewell2010) and disrupting key biological processes through changes in pH (e.g., organism physiology and behaviour; Pörtner, Reference Pörtner2008; Heuer and Grosell, Reference Heuer and Grosell2014; Clements and Hunt, Reference Clements and Hunt2015; Nagelkerken and Munday, Reference Nagelkerken and Munday2016).

While lowered seawater pH caused by OA can have substantial impacts on coastal vegetation (Koch et al., Reference Koch, Bowes, Ross and Zhang2013; Narvarte et al., Reference Narvarte, Nelson and Roleda2020), these species can in turn also affect seawater pH. For example, seagrass and macroalgae can raise pH on a local scale by taking up carbon through photosynthesis (Krause-Jensen et al., Reference Krause-Jensen, Duarte, Hendriks, Meire, Blicher, Marbà and Sejr2015). The role of coastal vegetated habitats, such as seagrass, mangroves, salt marshes and macroalgae as carbon sinks is widely acknowledged (e.g., Bouillon et al., Reference Bouillon, Borges, Castañeda-Moya, Diele, Dittmar, Duke, Kristensen, Lee, Marchand and Middelburg2008; Duarte et al., Reference Duarte, Marbà, Gacia, Fourqurean, Beggins, Barrón and Apostolaki2010; Alongi, Reference Alongi2012; Fourqurean et al., Reference Fourqurean, Duarte, Kennedy, Marbà, Holmer, Mateo, Apostolaki, Kendrick, Krause-Jensen and McGlathery2012; Chmura, Reference Chmura2013; Krause-Jensen and Duarte, Reference Krause-Jensen and Duarte2016). However, the role that coastal vegetated habitats play in influencing localised carbonate chemistry and pH of surrounding seawater, particularly in the context of OA, has only come to the forefront more recently, consequent to the increased attention given to coastal acidification.

Macroalgal vegetation can play a significant role in influencing the carbonate chemistry of seawater over various spatial and temporal scales (Middelboe and Hansen, Reference Middelboe and Hansen2007; Wahl et al., Reference Wahl, Schneider Covachã, Saderne, Hiebenthal, Müller, Pansch and Sawall2018; McNicholl et al., Reference McNicholl, Koch and Hofmann2019) through autotrophic, calcification and respiration processes (Middelboe and Hansen, Reference Middelboe and Hansen2007; Krause-Jensen and Duarte, Reference Krause-Jensen and Duarte2016). These localised zones of elevated pH associated with macroalgal beds could potentially serve as OA refugia (Noisette and Hurd, Reference Noisette and Hurd2018). For example, Wahl et al. (Reference Wahl, Schneider Covachã, Saderne, Hiebenthal, Müller, Pansch and Sawall2018) found that dense beds of brown algae and seagrass in the Western Baltic increased the overall mean pH of the surrounding water by as much as 0.3 units relative to other similar habitats with no macrophytes and also imposed strong diurnal pH fluctuations (due to photosynthetic activity). This allowed mussels (Mytilus edulis) to maintain calcification even under acidified conditions and suggests that seagrass and macroalgae may mitigate the impact of OA on organisms living in these habitats.

Macroalgal physiology and carbon use strategies

Photosynthesis and respiration

The process of photosynthesis (which occurs only during the day) in macroalgae requires the uptake of dissolved inorganic carbon (DIC), which is ultimately required in the form of CO2, together with water and light, to produce glucose and oxygen (Hanelt et al., Reference Hanelt, Wiencke, Bischof, Larkum, Douglas and Raven2003). In aquatic and marine environments, DIC exists in different forms: CO2, HCO3− and CO32− (Cornwall et al., Reference Cornwall, Revill and Hurd2015; Stepien et al., Reference Stepien, Pfister and Wootton2016). In seawater, DIC predominantly occurs in the form of HCO3− (~90%) and not as dissolved CO2 gas (<1%) due to the rapid dissociation of CO2 in seawater (Park, Reference Park1969). As such, most macroalgae have evolved carbon concentrating mechanisms (CCMs), which facilitate the active uptake of DIC in the form of HCO3− using various energy-driven mechanisms, such as external conversion of HCO3− to CO2 catalysed by the enzyme carbonic anhydrase (common in red, green and brown seaweeds; e.g., Flores-Moya and Fernández, Reference Flores-Moya and Fernández1998; Axelsson et al., Reference Axelsson, Larsson and Ryberg1999; Mercado et al., Reference Mercado, Viñgla, Figueroa and Niell1999) or through the uptake of HCO3− directly in this form via anion exchange proteins or proton pumps (Fernández et al., Reference Fernández, Hurd and Roleda2014). Once taken up into the cells, the enzyme carbonic anhydrase facilitates the interconversion of DIC to make it available for photosynthesis (Raven, Reference Raven1995). In many macroalgal species, CCMs are used in addition to passive CO2 diffusion (Maberly, Reference Maberly1990; Raven, Reference Raven2003; Giordano et al., Reference Giordano, Beardall and Raven2005; Cornwall et al., Reference Cornwall, Revill and Hurd2015; Stepien et al., Reference Stepien, Pfister and Wootton2016) depending on the availability and forms of DIC in surrounding seawater. Very few macroalgal species rely on passive CO2 diffusion alone for DIC uptake (Raven, Reference Raven2003; Giordano et al., Reference Giordano, Beardall and Raven2005; Raven and Hurd, Reference Raven and Hurd2012; Stepien et al., Reference Stepien, Pfister and Wootton2016).

The DIC acquisition strategies employed vary among macroalgal species and taxonomic groups (Maberly, Reference Maberly1990; Raven, Reference Raven1997). Green algae, like Ulva, for example, can efficiently use both CO2 and HCO3− as inorganic carbon sources (Beer and Eshel, Reference Beer and Eshel1983; Rautenberger et al., Reference Rautenberger, Fernández, Strittmatter, Heesch, Cornwall, Hurd and Roleda2015). Brown algae species rely almost exclusively on the uptake of DIC in the form of HCO3− (Surif and Raven, Reference Surif and Raven1989; Zou and Gao, Reference Zou and Gao2010; Fernández et al., Reference Fernández, Hurd and Roleda2014). The red algae are also primarily HCO3− users, with some exceptions, like Lomentaria articulata and Delesseria sanguinea, which lack this ability and rely on CO2 as a DIC source (Johnston et al., Reference Johnston, Maberly and Raven1992; Kubler and Raven, Reference Kubler and Raven1994). The ability and efficiency with which different DIC sources are used by macroalgal species appears to be related to habitat rather than specific to particular taxonomic groups (Maberly, Reference Maberly1990; Kubler and Raven, Reference Kubler and Raven1994; Murru and Sandgren, Reference Murru and Sandgren2004).

During periods when photosynthesis is not occurring or limited (e.g., at night or under reduced light availability), there is a net release of CO2 gas into surrounding seawater through respiration (Duarte et al., Reference Duarte, Middelburg and Caraco2005; Middelboe and Hansen, Reference Middelboe and Hansen2007; Semesi et al., Reference Semesi, Kangwe and Björk2009). This process also influences the carbonate chemistry and forces the equilibrium to a state that decreases pH (Middelboe and Hansen, Reference Middelboe and Hansen2007; Saderne et al., Reference Saderne, Fietzek and Herman2013; Wahl et al., Reference Wahl, Schneider Covachã, Saderne, Hiebenthal, Müller, Pansch and Sawall2018). The influence of photosynthesis and respiration on seawater carbonate chemistry is most significant over larger spatial scales when macroalgal growth and density is high. Since the carbonate chemistry equilibrium of seawater is dynamic, the periodic uptake of DIC for photosynthesis by macroalgae acts to increase pH, and CO2 released by respiration, conversely, decreases pH often resulting in diurnal pH cycles. Despite these complex and ongoing changes to this equilibrium, which result in highly variable conditions in these habitats, there is evidence to suggest that macroalgae raise the overall average pH in surrounding seawater, which can have temporary or long-term benefits for the organisms that live in these habitats (Krause-Jensen and Duarte, Reference Krause-Jensen and Duarte2016; Koweek et al., Reference Koweek, Zimmerman, Hewett, Gaylord, Giddings, Nickols, Ruesink, Stachowicz, Takeshita and Caldeira2018; Wahl et al., Reference Wahl, Schneider Covachã, Saderne, Hiebenthal, Müller, Pansch and Sawall2018).

Calcification

In addition to photosynthetic needs, some macroalgal species rely on DIC in the form of CO32−, HCO3− or CO2 to build and maintain calcium carbonate structures through the precipitation of CaCO3 (Roleda et al., Reference Roleda, Boyd and Hurd2012a; Hofmann and Bischof, Reference Hofmann and Bischof2014). This process may also modulate the carbonate chemistry equilibrium of surrounding seawater through both the absorption of DIC and the release of CO2 (Kalokora et al., Reference Kalokora, Buriyo, Asplund, Gullström, Mtolera and Björk2020). As such, the role that calcifying species have on carbon dynamics of surrounding seawater is complex, as processes of photosynthesis, calcification and respiration simultaneously influence the carbon system, and ultimately pH, in counteracting ways (Kalokora et al., Reference Kalokora, Buriyo, Asplund, Gullström, Mtolera and Björk2020).

The best-known calcifying group of algae are the order of red algae, the coralline algae, that form crustose or articulated structures by depositing CaCO3 extracellularly (Hofmann and Bischof, Reference Hofmann and Bischof2014; McCoy and Kamenos, Reference McCoy and Kamenos2015). These algae can form large aggregations spanning several square kilometres or also occur as smaller crusts or as epiphytes on other living organisms (McCoy and Kamenos, Reference McCoy and Kamenos2015). Although calcification in this group is considered to be sensitive to OA, as CO32− is less available in seawater under acidic conditions (Feely et al., Reference Feely, Sabine, Lee, Berelson, Kleypas, Fabry and Millero2004; Fabry et al., Reference Fabry, Seibel, Feely and Orr2008; Raven, Reference Raven2011; Stepien et al., Reference Stepien, Pfister and Wootton2016), the fact that many calcifying macroalgae utilise HCO3− or CO2 as substrate for calcification, and not carbonate may limit this sensitivity (Roleda et al., Reference Roleda, Boyd and Hurd2012a). Furthermore, carbonate concentrations can be increased by these algae through alteration of pH of water in close association with the thallus (e.g., intercellular spaces) during photosynthetic use of CO2 and/or HCO3− (Digby, Reference Digby1977; Borowitzka and Larkum, Reference Borowitzka and Larkum1987), reducing reliance on elevated ambient carbonate ion concentrations. In fact, dissolution of calcified structures because of OA might be a greater problem than reduced calcification rates (Doney et al., Reference Doney, Fabry, Feely and Kleypas2009; Hofmann and Todgham, Reference Hofmann, Barry, Edmunds, Gates, Hutchins, Klinger and Sewell2010).

Through these interactions with the carbonate system of seawater, macroalgae influence the carbon equilibrium of surrounding seawater over various scales. However, for macroalgal vegetation to play a meaningful role as OA refugia for other marine organisms, the density of these primary producers needs to be high enough. Macroalgal vegetation is not evenly distributed with respect to species and biomass and certain regions would be of greater significance in their effect on local seawater carbon fluxes and pH. The greatest potential for OA mitigation is likely to be in coastal areas with large, dense and complex macroalgal communities or seaweed farms (Chung et al., Reference Chung, Oak, Lee, Shin, Kim and Park2013; Zacharia et al., Reference Zacharia, Kaladharan and Rohith2015; Fernández et al., Reference Fernández, Leal and Henríquez2019; Xiao et al., Reference Xiao, Agustí, Yu, Huang, Chen, Hu, Li, Li, Wei, Lu, Xu, Chen, Liu, Zeng, Wu and Duarte2021).

Macroalgal distribution patterns

Globally, macroalgal distribution is determined by seawater surface temperature, while local scale distribution is established in response to substrate properties and depth. Lüning (Reference Lüning1991) described macroalgal floras of the world in detail and the regions identified based on macroalgal vegetation closely resemble the seven temperature zones adopted by Briggs (Reference Briggs1995) (Figure 1).

Figure 1. Distribution of coastal temperature zones based on Briggs, Reference Briggs1995 (reproduced from Bartsch et al., Reference Bartsch, Wiencke, Laepple and Wiencke2012). Blue, polar regions; green, cool temperate; yellow, warm temperate; red, tropical.

Marine forests

Canopy-forming macroalgae occur along various coastlines and include large brown species, such as large Laminarian kelps and smaller Fucalean genera, which dominate marine benthic communities known as marine forests. Large robust canopy-forming brown algae are recognised habitat engineers known for their ability to alter physical conditions in the surrounding benthos (Steneck et al., Reference Steneck, Graham, Bourque, Corbett, Erlandson, Estes and Tegner2002; Schiel and Foster, Reference Schiel and Foster2015; Teagle et al., Reference Teagle, Hawkins, Moore and Smale2017; Wernberg et al., Reference Wernberg, Krumhansl, Filbee-Dexter, Pedersen and Sheppard2019). These subtidal brown algae are the most important macroalgal primary producers based on area cover and net primary production (Duarte et al., Reference Duarte, Bruhn and Krause-Jensen2022). Kelp forest communities include a variety of canopy-forming species that differ widely in stature. Steneck et al. (Reference Steneck, Graham, Bourque, Corbett, Erlandson, Estes and Tegner2002) recognised at least three different groups of large forms that represent the kelp-component in kelp forests. The floating canopy kelps (e.g., Macrocystis) that grow up to 45 m in length, smaller canopy kelps like Ecklonia and Nereocystis (<10 m); and kelps that are held upright by rigid stipes (Laminaria and Ecklonia radiata) (<5 m). These ecosystem engineers create forest-like marine vegetation types that have complex three-dimensional structures. Like terrestrial forests, kelp communities have associated understory algal communities (Leliaert et al., Reference Leliaert, Anderson, Bolton and Coppejans2000; Bennett and Wernberg, Reference Bennett and Wernberg2014; Leclerc et al., Reference Leclerc, Riera, Lévêque and Davoult2016; Smale et al., Reference Smale, Pessarrodona, King, Burrows, Yunnie, Vance and Moore2020).

The smaller canopy-forming algae are from the Fucales, of which Sargassum and Cystoseira species are the most widespread (Nizamuddin, Reference Nizamuddin1970). Sargassum is more common in the warm-temperate, subtropical and tropical coasts (Yip et al., Reference Yip, Quek and Huang2020), while Cystoseira is most diverse in the Mediterranean (Nizamuddin, Reference Nizamuddin1970). This pattern of canopy-forming algal distribution is reflected in the mapped brown algal marine forests, which show strong representation in cool- to cold-temperate regions, but also in some warmer tropical coasts such as the Caribbean and Indo-China (Figure 2) (Assis et al., Reference Assis, Fragkopoulou, Frade, Neiva, Oliveira, Abecasis, Faugeron and Serrão2020).

Figure 2. Modelled distribution of brown forest forming macroalgal species (after Assis et al., Reference Assis, Fragkopoulou, Frade, Neiva, Oliveira, Abecasis, Faugeron and Serrão2020).

Lower canopy-forming algae like Gelidium corneum are also considered foundational, or habitat forming species (Quintano et al., Reference Quintano, Díez, Muguerza, Figueroa and Gorostiaga2017; Borja et al., Reference Borja, Chust, Fontan, Garmendia and Uyarra2018; Muguerza et al., Reference Muguerza, Díez, Quintano and Gorostiaga2022), particularly on some European coasts, with Gelidium canariense representing an important canopy-forming species on Macronesian islands (Alfonso et al., Reference Alfonso, Sangil and Sansón2017; Hernández, Reference Hernández2021). While these algae are not as tall as the kelps, the canopies formed are similar in height (20–30 cm) to some of the fucalean-dominated communities (Robertson, Reference Robertson1987; Quintano et al., Reference Quintano, Díez, Muguerza, Figueroa and Gorostiaga2018; Alfonso et al., Reference Alfonso, Hernández, Sangil, Martín, Expósito, Díaz and Sansón2021; Hernández, Reference Hernández2021). Smaller brown and red foliose species are usually important components of the under-story vegetation and occur both under canopies of larger brown algae as well as in the gaps between stands of taller algae. However, temperate G. corneum (Quintano et al., Reference Quintano, Díez, Muguerza, Figueroa and Gorostiaga2017, Reference Quintano, Díez, Muguerza, Figueroa and Gorostiaga2018; Casado-Amezúa et al., Reference Casado-Amezúa, Araújo, Bárbara, Bermejo, Borja, Díez, Fernández, Gorostiaga, Guinda and Hernández2019) and Gelidium canariense (Alfonso et al., Reference Alfonso, Hernández, Sangil, Martín, Expósito, Díaz and Sansón2021; Hernández, Reference Hernández2021) are both recognised as short canopy-forming species in their own right.

Polar macroalgae

The polar macroalgae flora is confined predominantly to the subtidal zone due to seasonal ice scour, which abrades rock surfaces on the intertidal reefs (Zacher et al., Reference Zacher, Rautenberger, Hanelt, Wulff and Wiencke2009). Light limitation during winter months limits the poleward distribution of kelps that form such extensive forests in temperate regions (Steneck et al., Reference Steneck, Graham, Bourque, Corbett, Erlandson, Estes and Tegner2002). However, a few Laminarian species do occur in these cold polar regions (Filbee-Dexter et al., Reference Filbee-Dexter, Wernberg, Fredriksen, Norderhaug and Pedersen2019), with macroalgal communities in cold polar waters generally comprised of a canopy of large brown algae, with an understory community of foliose and coralline macroalgae (Brouwer et al., Reference Brouwer, Geilen, Gremmen and Lent1995; Wiencke and Amsler, Reference Wiencke, Amsler, Wiencke and Bischof2012). Although the Arctic has limited potential for substantial macroalgae communities, since only 35% of the benthos in this region has hard substrate that can support large attached macroalgae like kelp forests (Filbee-Dexter et al., Reference Filbee-Dexter, Wernberg, Fredriksen, Norderhaug and Pedersen2019), subtidal macroalgae communities can reach biomass values comparable to temperate kelp communities (Wiencke and Amsler, Reference Wiencke, Amsler, Wiencke and Bischof2012).

Temperate algal vegetation

In cold- and warm-temperate regions, the large brown algae also dominate the subtidal zone (Flores-Moya, Reference Flores-Moya, Wiencke and Bischof2012; Huovinen and Gómez, Reference Huovinen, Gómez, Wiencke and Bischof2012). The most prominent group in this regard are the kelps (Laminariales), which attain the largest size of these brown canopy-forming algae (Steneck et al., Reference Steneck, Graham, Bourque, Corbett, Erlandson, Estes and Tegner2002). These are common in cooler regions (warm and cold temperate) but relatively rare along warmer coastlines (Bolton, Reference Bolton2010). Dense beds of smaller macroalgal groups are also common in temperate areas (Lüning, Reference Lüning1991; Shepherd and Edgar, Reference Shepherd and Edgar2013). Estimates based on habitat availability models show that, while these smaller algae potentially cover a substantial area, they make a limited contribution to primary production (Duarte et al., Reference Duarte, Bruhn and Krause-Jensen2022).

Tropical algal vegetation

Subtidal algal vegetation in tropical regions usually forms a mosaic with coral reefs. These metazoan colonies share space with both turf and foliose macroalgae communities, the relative abundance of which is dependent on the interplay between herbivory, nutrients and light availability (Hurd et al., Reference Hurd, Harrison, Bischof and Lobban2014). Foliose algae are usually rare in coral reef systems, unless there is reduction in herbivory or an increase in nutrients (Lobban and Harrison, Reference Lobban and Harrison1994). These algae are often fucoids like Cystoseira, Turbinaria and Sargassum (Mejia et al., Reference Mejia, Puncher, Engelen, Wiencke and Bischof2012). Foliose algae, along with some coralline algae, usually form communities on the shallow shoreward reef flats of coral atolls, while the seaward slopes are usually occupied by corals, coralline algae and calcified macroalgae such as Halimeda (Littler and Littler, Reference Littler, Littler, Lobban and Harrison1994). One of the reasons for this is the availability of hard substrate on a relatively flat surface to which they can attach (Fong and Paul, Reference Fong, Paul, Dubinsky and Stambler2011). Extensive macroalgal communities are not common in tropical regions, however, Wilson et al. (Reference Wilson, Depczynski, Fisher, Holmes, O’Leary and Tinkler2010) and Evans et al. (Reference Evans, Wilson, Field and Moore2014) report substantial algal meadows off the coast of Australia.

Based on macroalgal distribution models, there appears to be great potential for OA mitigation in algal beds, both in temperate and tropical regions. However, the greatest opportunities for larger scale OA refuge would lie within the high biomass areas offered by temperate marine forests. High biomass can also be created through coastal seaweed aquaculture initiatives, which may alleviate OA stresses in shallow coastal areas.

Trends in ocean acidification refuge provision by macroalgae

Temporal trends

Refuge from OA provided by macroalgae can be temporally consistent or cyclical, depending on several factors such as seasonal productivity (Middelboe and Hansen, Reference Middelboe and Hansen2007), photosynthetic state (diurnal cycles), water retention time and mixing (Middelboe and Hansen, Reference Middelboe and Hansen2007; Buapet et al., Reference Buapet, Gullström and Björk2013; Koch et al., Reference Koch, Bowes, Ross and Zhang2013) and nutrient availability (Gao and McKinley, Reference Gao and McKinley1994; Celis-Pla et al., Reference Celis-Pla, Hall-Spencer, Horta, Milazzo, Korbee, Cornwall and Figueroa2015).

Macroalgae are subject to seasonal differences in productivity and photosynthetic rates, like many other plant species, related to temperature preferences, irradiance and nutrient availability (Takahashi et al., Reference Takahashi, Sutherland, Sweeney, Poisson, Metzl, Tilbrook, Bates, Wanninkhof, Feely and Sabine2002; Saderne et al., Reference Saderne, Fietzek and Herman2013; Attard et al., Reference Attard, Rodil, Berg, Norkko, Norkko and Glud2019; Kapsenberg and Cyronak, Reference Kapsenberg and Cyronak2019). This means that their provision as OA refuges may vary with seasonal differences in productivity (Li et al., Reference Li, Moon, Kang, Kim, Kim, Lee, Kwak, Kim, Kim and Park2022). Studies have found that in most regions macroalgal productivity is typically higher in summer and spring months. For example, Middelboe and Hansen (Reference Middelboe and Hansen2007) identified seasonal pH variability associated with macroalgal productivity (Fucus vesiculosus, F. serratus, Ceramium rubrum and Ulva spp.) on the northeast coast of Zealand (Denmark), evidenced by higher average pH in summer and lower pH in winter, which they attributed mostly to seasonal differences in irradiance. These findings are similar to other studies that also found higher average pH and higher variability in carbonate parameters (pCO2 and DIC) in productive summer months, for example, Krause-Jensen et al. (Reference Krause-Jensen, Duarte, Hendriks, Meire, Blicher, Marbà and Sejr2015) in a subarctic fjord in Greenland and Delille et al. (Reference Delille, Borges and Delille2009) in a Southern Ocean Archipelago. As such, macroalgal-dominated habitats may provide seasonal relief for marine organisms from OA during periods of higher productivity.

Many studies have identified diurnal cycles in seawater pH adjacent to macroalgal vegetation, with the common pattern being higher pH during the day (driven by photosynthesis) and lower pH at night (driven by respiration; e.g., Middelboe and Hansen, Reference Middelboe and Hansen2007; Semesi et al., Reference Semesi, Kangwe and Björk2009; Frieder et al., Reference Frieder, Nam, Martz and Levin2012; Cornwall et al., Reference Cornwall, Hepburn, McGraw, Currie, Pilditch, Hunter, Boyd and Hurd2013; Krause-Jensen et al., Reference Krause-Jensen, Duarte, Hendriks, Meire, Blicher, Marbà and Sejr2015; Wahl et al., Reference Wahl, Schneider Covachã, Saderne, Hiebenthal, Müller, Pansch and Sawall2018). These patterns occur in response to daylight availability for photosynthesis. In some cases, diurnal variability in pH can be as high as 1.2–1.5 units depending on the density of macroalgal growth and resultant levels of productivity (Krause-Jensen et al., Reference Krause-Jensen, Duarte, Hendriks, Meire, Blicher, Marbà and Sejr2015; Wahl et al., Reference Wahl, Saderne and Sawall2015). The extent of diurnal variability can also be influenced by physical factors, such as tidal processes or seawater exchange. Shallow areas with less mixing and higher water retention times usually experience high diurnal pH variability (Middelboe and Hansen, Reference Middelboe and Hansen2007; Hurd, Reference Hurd2015). Diurnal fluctuations in pH can benefit associated organisms by providing cyclical or periodic relief from OA. Wahl et al. (Reference Wahl, Schneider Covachã, Saderne, Hiebenthal, Müller, Pansch and Sawall2018) found that the brown algae F. vesiculosus in the Kiel Fjord increased overall mean pH of seawater by 0.01–0.2 units, with diurnal variability of 1.2 units. Mussels (Mytilus edulis) benefited from this autotrophic pH modulation as they were able to maintain calcification rates even at low pH levels (7.7–8.1 depending on algal density) by shifting their calcification process to daytime periods to fall in with the periods of higher pH provided by the vegetation (Wahl et al., Reference Wahl, Schneider Covachã, Saderne, Hiebenthal, Müller, Pansch and Sawall2018). Other studies have found similar benefits for growth, development and physiology in other bivalve species (summarised in Table 1) (Frieder et al., Reference Frieder, Gonzalez, Bockmon, Navarro and Levin2014; Young and Gobler, Reference Young and Gobler2018; Jiang et al., Reference Jiang, Jiang, Rastrick, Wang, Fang, Du, Gao, Mao, Strand and Fang2022; Young et al., Reference Young, Sylvers, Tomasetti, Lundstrom, Schenone, Doall and Gobler2022). However, there is also evidence to suggest that not all species are capable of adapting their calcification process to benefit from diurnal pH variability (Cornwall et al., Reference Cornwall, Hepburn, McGraw, Currie, Pilditch, Hunter, Boyd and Hurd2013) and, as such, may still be negatively affected by corrosive conditions at night.

Table 1. Examples of studies assessing the ocean acidification (OA) refuge provision by macroalgal species for various coastal organisms

Spatial trends

Macroalgae can serve as OA refugia over a range of spatial scales as they can form habitats ranging in size from large stands and canopies to low-level algal crusts (Hepburn et al., Reference Hepburn, Pritchard, Cornwall, McLeod, Beardall, Raven and Hurd2011). Macroalgae also occur at a vast range of locations, such as in shallow coastal areas, rock pools, estuaries or deeper subtidal locations (Layton et al., Reference Layton, Coleman, Marzinelli, Steinberg, Swearer, Vergés, Wernberg and Johnson2020; Falkenberg et al., Reference Falkenberg, Scanes, Ducker and Ross2021). The distribution and structure of macroalgal growth will offer refuge from OA at different spatial extents. On a small scale, pH fluctuation related to biological activity can occur at spatial scales as small as centimetres, for example, in the diffusive boundary layer at the thalli surface (Noisette and Hurd, Reference Noisette and Hurd2018; Guy-Haim et al., Reference Guy-Haim, Silverman, Wahl, Aguirre, Noisette and Rilov2020). Conversely, in large- and dense-algal aggregations, biological activity can have an influence at an extent of metres to kilometres (Krause-Jensen et al., Reference Krause-Jensen, Duarte, Hendriks, Meire, Blicher, Marbà and Sejr2015).

On a micro-scale (centimetres) macroalgal metabolism can create favourable micro-zones of higher pH within their diffusive boundary layer (Noisette and Hurd, Reference Noisette and Hurd2018; Guy-Haim et al., Reference Guy-Haim, Silverman, Wahl, Aguirre, Noisette and Rilov2020), where pH can be up to 1–3 units higher than surrounding seawater (Wahl et al., Reference Wahl, Saderne and Sawall2015). Marine organisms that live on the surface of macroalgae can benefit from this chemical refuge, especially during the daytime when photosynthetic activity is highest (Noisette and Hurd, Reference Noisette and Hurd2018) (Table 1). For example, Saderne and Wahl (Reference Saderne and Wahl2013) found that both calcifying (Electra pilosa) and non-calcifying (Alcyonidium hirsutum) Bryozoan species were tolerant of high pCO2 levels (1,193 ± 166 μatm) associated with upwelling events in the Western Baltic Sea, and they attributed this tolerance to the potential periodic relief from OA provided by the brown macroalgal species Fucus serratus on which these species live. Similarly, Doo et al. (Reference Doo, Leplastrier, Graba-Landry, Harianto, Coleman and Byrne2020) found that an epiphytic foraminifera, Marginopora vertebralis, showed higher tolerance to end-of-the-century temperature (±3 °C) and pCO2 (~1,000 μatm) when kept experimentally under these treatments with its red macroalgal host, Laurencia intricata. Similar beneficial symbiotic relationships that facilitate micro-refugia from OA exist between calcifying and non-calcifying algae. For example, Guy-Haim et al. (Reference Guy-Haim, Silverman, Wahl, Aguirre, Noisette and Rilov2020) and Short et al. (Reference Short, Kendrick, Falter and McCulloch2014) found that the coralline algae Ellisolandia elongata and Hydrolithoideae spp. are less susceptible to the effects of OA, evidenced by higher calcification rates at low pH (7.8 and 7.7, respectively), when associated with non-calcifying epiphytic algae. There are also examples of species, such as urchin larvae (Pseudechinus huttoni) that are well adapted to pH variability and therefore show no positive or negative response to the variable pH in their settlement habitats (Houlihan et al., Reference Houlihan, Espinel-Velasco, Cornwall, Pilditch and Lamare2020).

The effect of photosynthesis on surrounding seawater carbonate chemistry can extend further than the immediate vicinity of the algal growth. Macroalgal assemblages that form complex communities can provide refuge from OA over much larger spatial scales from metres (e.g., in rock pools or within canopies) to kilometres (e.g., extensive algal beds in temperate areas) due to higher and more concentrated levels of metabolic activity (Björk et al., Reference Björk, Axelsson and Beer2004; Middelboe and Hansen, Reference Middelboe and Hansen2007; Duarte et al., Reference Duarte, Hendriks, Moore, Olsen, Steckbauer, Ramajo, Carstensen, Trotter and McCulloch2013; Krause-Jensen et al., Reference Krause-Jensen, Duarte, Hendriks, Meire, Blicher, Marbà and Sejr2015). The refuge potential is especially significant in macroalgal assemblages with dense growth and complex canopy structure with the additional benefit of reduced seawater flow, which increases water residence time (Hendriks et al., Reference Hendriks, Olsen, Ramajo, Basso, Steckbauer, Moore, Howard and Duarte2014; Hurd, Reference Hurd2015).

Macroalgae have been reported to increase the average pH (to levels >8.5 pH units) in rock pools (Björk et al., Reference Björk, Axelsson and Beer2004), lagoons (Menéndez et al., Reference Menéndez, Martı́nez and Comı́n2001) and bays (Buapet et al., Reference Buapet, Gullström and Björk2013). For example, Krause-Jensen et al. (Reference Krause-Jensen, Duarte, Hendriks, Meire, Blicher, Marbà and Sejr2015) found pH variability of 0.1–0.3 units occurs within the scale of 1 m2 in response to location within the canopy of a large kelp forest in the Kobbefjord in southwest Greenland. At a slightly larger scale, Buapet et al. (Reference Buapet, Gullström and Björk2013) compared the pH conditions in different vegetation types (mixed macroalgae and seagrass beds) to non-vegetated areas in six shallow coastal bays in temperate Sweden. Their results showed that vegetation can influence the conditions at the scale of an entire bay as evidenced by higher pH and lower DIC concentrations relative to the adjacent seawater outside the bay, even in areas of the bay where vegetation did not occur (Buapet et al., Reference Buapet, Gullström and Björk2013).

Impacts of ocean acidification on macroalgae

It is important to consider the potential negative impacts that OA may have on macroalgae in order to determine their provision as OA refugia under future acidified conditions. Most studies that have assessed the response of macroalgae to changes in seawater carbonate chemistry associated with OA have shown that macroalgal species from all algal groups (red, brown and green) are generally physiologically tolerant to predicted OA and even show enhanced growth under these conditions (see reviews by Porzio et al., Reference Porzio, Buia and Hall-Spencer2011 and Koch et al., Reference Koch, Bowes, Ross and Zhang2013). This tolerance is attributed to the ability of most macroalgal species to efficiently assimilate DIC in various forms for photosynthesis thus allowing them to benefit from increased availability of DIC under acidified conditions (Fernández et al., Reference Fernández, Roleda and Hurd2015; Cornwall and Hurd, Reference Cornwall and Hurd2019). Of course, there are exceptions with some species sensitive to OA, with sensitivity likely linked to mechanisms of carbon uptake and calcification (Cornwall et al., Reference Cornwall, Hepburn, Pritchard, Currie, McGraw, Hunter and Hurd2012; Hofmann and Bischof, Reference Hofmann and Bischof2014) as well as the scale of exposure (e.g., extreme low pH conditions associated with coastal acidification induced by mariculture activities as shown by Narvarte et al., Reference Narvarte, Nelson and Roleda2020). Of all the algal groups, sensitivity to OA is most often reported for calcifying species (see the section “Calcification”), with this group facing the threat of being outcompeted by the more tolerant non-calcifying algae (Hofmann and Bischof, Reference Hofmann and Bischof2014).

Considering that some macroalgal species have heteromorphic life cycles (e.g., many kelp species), it is also important to consider the impact of OA on the different stages, where the early life stages (unicellular and microscopic stages) are usually deemed more sensitive to environmental change (Roleda et al., Reference Roleda, Wiencke, Hanelt and Bischof2007). Although the early life stages of some macroalgal species have been shown to be more sensitive to other environmental factors (e.g., UV radiation; Roleda et al., Reference Roleda, Wiencke, Hanelt and Bischof2007), there is evidence to suggest that early life stages are not affected by OA conditions (Roleda et al., Reference Roleda, Morris, McGraw and Hurd2012b, Reference Roleda, Cornwall, Feng, McGraw, Smith and Hurd2015; Leal et al., Reference Leal, Hurd and Fernández2017). This provides positive evidence for the persistence of macroalgal habitats in future.

Conclusion and relevance

Macroalgae form important components of shallow coastal marine ecosystems and have been identified as potentially beneficial habitats for coastal species facing ongoing OA by provision of higher average pH conditions (Kapsenberg and Cyronak, Reference Kapsenberg and Cyronak2019). Being a dynamic process, autotrophic pH modulation exposes organisms to higher variability in pH in space and time, and therefore alternating periods of stress and recovery (Wahl et al., Reference Wahl, Schneider Covachã, Saderne, Hiebenthal, Müller, Pansch and Sawall2018). As such, the species that occur in vegetated environments, like macroalgal ecosystems, although benefitting from periodic relief from the physiological stress incurred by OA, still require the physiological capacity to withstand high pH variability (Falkenberg et al., Reference Falkenberg, Scanes, Ducker and Ross2021). Despite short-term fluctuations in pH conditions, autotrophic biological activity likely provides associated organisms with long-term relief from ongoing OA (Hurd, Reference Hurd2015; Koweek et al., Reference Koweek, Zimmerman, Hewett, Gaylord, Giddings, Nickols, Ruesink, Stachowicz, Takeshita and Caldeira2018; Pacella et al., Reference Pacella, Brown, Waldbusser, Labiosa and Hales2018). Considering the apparent tolerance of most photosynthetic macroalgae to future OA conditions, and particularly those taxa that are known to form large stands and aggregations, it is likely these habitats will continue to provide an important refuge for the many marine species associated with them.

The research highlighted in this review provides important evidence for the potential OA refuge function of brown, red and green macroalgae by mitigating the negative effects of OA on growth and calcification of mainly bivalves but also bryozoans, foraminifera and coralline algae (Table 1). However, research conducted over large spatial scales, across biogeographic regions, and for many macroalgae-associated species (such as other calcifying organisms and fish) is lacking and needs to be addressed in future research. The role of macroalgal habitats as refugia should be considered for local OA management and protected area management for conservation efforts (Morelli et al., Reference Morelli, Daly, Dobrowski, Dulen, Ebersole, Jackson, Lundquist, Millar, Maher and Monahan2016; Kapsenberg and Cyronak, Reference Kapsenberg and Cyronak2019), especially in productive coastal marine environments where these habitats already provide important nursery areas for many marine species (James and Whitfield, Reference James and Whitfield2022).

Open peer review

To view the open peer review materials for this article, please visit http://doi.org/10.1017/cft.2023.9.

Author contribution

C.E. conceptualised the review, reviewed the literature, wrote sections of the manuscript and edited the final version. P.-P.S. reviewed the literature, wrote sections of the manuscript and edited the final version. N.C.J. conceptualised the review, structured the manuscript and edited the final version.

Financial support

This review forms part of a broader research project on South African nursery seascapes funded by the National Research Foundation (NRF) coastal and marine research grants (Grant Number 136489).

Competing interest

All authors declare that they have no competing interest to disclose.

References

Alfonso, B, Hernández, JC, Sangil, C, Martín, L, Expósito, FJ, Díaz, JP and Sansón, M (2021) Fast climatic changes place an endemic Canary Island macroalga at extinction risk. Regional Environmental Change 21, 1–16.CrossRefGoogle Scholar
Alfonso, B, Sangil, C and Sansón, M (2017) Morphological and phenological reexamination of the threatened endemic species Gelidium canariense (Gelidiales, Rhodophyta) from the Canary Islands. Botanica Marina 60, 543–553.CrossRefGoogle Scholar
Alongi, DM (2012) Carbon sequestration in mangrove forests. Carbon Management 3, 313–322.CrossRefGoogle Scholar
Assis, J, Fragkopoulou, E, Frade, D, Neiva, J, Oliveira, A, Abecasis, D, Faugeron, S and Serrão, EA (2020) A fine-tuned global distribution dataset of marine forests. Scientific Data 7, 1–9.CrossRefGoogle ScholarPubMed
Attard, KM, Rodil, IF, Berg, P, Norkko, J, Norkko, A and Glud, RN (2019) Seasonal metabolism and carbon export potential of a key coastal habitat: The perennial canopy-forming macroalga Fucus vesiculosus. Limnology and Oceanography 64, 149–164.CrossRefGoogle Scholar
Axelsson, L, Larsson, C and Ryberg, H (1999) Affinity, capacity and oxygen sensitivity of two different mechanisms for bicarbonate utilization in Ulva lactuca L. (Chlorophyta). Plant, Cell and Environment 22, 969–978.CrossRefGoogle Scholar
Bartsch, I, Wiencke, C and Laepple, T (2012) Global seaweed biogeography under a changing climate: the prospected effects of temperature. In Wiencke, C (ed.), Seaweed Biology. Berlin: Springer, pp. 383–406.CrossRefGoogle Scholar
Beer, S and Eshel, A (1983) Photosynthesis of Ulva sp. II. Utilization of CO2 and HCO3− when submerged. Journal of Experimental Marine Biology and Ecology 70, 99–106.Google Scholar
Bennett, S and Wernberg, T (2014) Canopy facilitates seaweed recruitment on subtidal temperate reefs. Journal of Ecology 102, 1462–1470.CrossRefGoogle Scholar
Björk, M, Axelsson, L and Beer, S (2004) Why is Ulva intestinalis the only macroalga inhabiting isolated rockpools along the Swedish Atlantic coast? Marine Ecology Progress Series 284, 109–116.CrossRefGoogle Scholar
Bolton, JJ (2010) The biogeography of kelps (Laminariales, Phaeophyceae): A global analysis with new insights from recent advances in molecular phylogenetics. Helgoland Marine Research 64, 263–279.CrossRefGoogle Scholar
Borja, A, Chust, G, Fontan, A, Garmendia, JM and Uyarra, MC (2018) Long-term decline of the canopy-forming algae Gelidium corneum, associated to extreme wave events and reduced sunlight hours, in the southeastern Bay of Biscay. Estuarine, Coastal and Shelf Science 205, 152–160.CrossRefGoogle Scholar
Borowitzka, MA and Larkum, AWD (1987) Calcification in algae: Mechanisms and the role of metabolism. Critical Reviews in Plant Sciences 6, 1–45.CrossRefGoogle Scholar
Bouillon, S, Borges, AV, Castañeda-Moya, E, Diele, K, Dittmar, T, Duke, NC, Kristensen, E, Lee, SY, Marchand, C and Middelburg, JJ (2008) Mangrove production and carbon sinks: A revision of global budget estimates. Global Biogeochemical Cycles 22, GB003052.CrossRefGoogle Scholar
Briggs, JC (1995) Global Biogeography. Amsterdam: Elsevier.Google Scholar
Brouwer, PEM, Geilen, EFM, Gremmen, NJM and Lent, F (1995) Biomass, cover and zonation pattern of sublittoral macroalgae at Signy Island, South Orkney Islands, Antarctica. Botanica Marina 38, 259–270.CrossRefGoogle Scholar
Buapet, P, Gullström, M and Björk, M (2013) Photosynthetic activity of seagrasses and macroalgae in temperate shallow waters can alter seawater pH and total inorganic carbon content at the scale of a coastal embayment. Marine and Freshwater Research 64, 1040–1048.CrossRefGoogle Scholar
Caldeira, K and Wickett, ME (2003) Anthropogenic carbon and ocean pH. Nature 425, 365.CrossRefGoogle ScholarPubMed
Casado-Amezúa, P, Araújo, R, Bárbara, I, Bermejo, R, Borja, Á, Díez, I, Fernández, C, Gorostiaga, JM, Guinda, X and Hernández, I (2019) Distributional shifts of canopy-forming seaweeds from the Atlantic coast of southern Europe. Biodiversity and Conservation 28, 1151–1172.CrossRefGoogle Scholar
Celis-Pla, PSM, Hall-Spencer, JM, Horta, PA, Milazzo, M, Korbee, N, Cornwall, CE and Figueroa, FL (2015) Macroalgal responses to ocean acidification depend on nutrient and light levels. Frontiers in Marine Science 2, 26.Google Scholar
Chmura, GL (2013) What do we need to assess the sustainability of the tidal salt marsh carbon sink? Ocean & Coastal Management 83, 25–31.Google Scholar
Chung, IK, Oak, JH, Lee, JA, Shin, JA, Kim, JG and Park, K-S (2013) Installing kelp forests/seaweed beds for mitigation and adaptation against global warming: Korean Project Overview. ICES Journal of Marine Science 70, 1038–1044.CrossRefGoogle Scholar
Clements, JC and Hunt, HL (2015) Marine animal behaviour in a high CO2 ocean. Marine Ecology Progress Series 536, 259–279.CrossRefGoogle Scholar
Cornwall, CE, Hepburn, CD, Pritchard, D, Currie, KI, McGraw, CM, Hunter, KA and Hurd, CL (2012) Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. Journal of Phycology 48, 137–144.CrossRefGoogle ScholarPubMed
Cornwall, CE, Hepburn, CD, McGraw, CM, Currie, KI, Pilditch, CA, Hunter, KA, Boyd, PW and Hurd, CL (2013) Diurnal fluctuations in seawater pH influence the response of a calcifying macroalga to ocean acidification. Proceedings of the Royal Society B: Biological Sciences 280, 20132201.CrossRefGoogle ScholarPubMed
Cornwall, CE, Boyd, PW, McGraw, CM, Hepburn, CD, Pilditch, CA, Morris, JN, Smith, AM and Hurd, CL (2014) Diffusion boundary layers ameliorate the negative effects of ocean acidification on the temperate coralline macroalga Arthrocardia corymbosa, PLOS One 9, e109468.Google ScholarPubMed
Cornwall, CE, Revill, AT and Hurd, CL (2015) High prevalence of diffusive uptake of CO2 by macroalgae in a temperate subtidal ecosystem. Photosynthesis Research 124, 181–190.CrossRefGoogle Scholar
Cornwall, CE and Hurd, CL (2019) Variability in the benefits of ocean acidification to photosynthetic rates of macroalgae without CO2-concentrating mechanisms. Marine and Freshwater Research 71, 275–280.Google Scholar
Delille, B, Borges, AV and Delille, D (2009) Influence of giant kelp beds (Macrocystis pyrifera) on diel cycles of pCO2 and DIC in the sub-Antarctic coastal area. Estuarine, Coastal and Shelf Science 81, 114–122.CrossRefGoogle Scholar
Dickson, AG (2010) The carbon dioxide system in seawater: Equilibrium chemistry and measurements. In Riebesell, U, Fabry, VJ, Hansson, L and Gattuso, J-P (eds), Guide to Best Practices for Ocean Acidification Research and Data Reporting. Luxembourg: Publications Office of the European Union, pp. 17–40.Google Scholar
Digby, PSB (1977) Growth and calcification in the coralline algae, Clathromorphum circumscriptum and Corallina officinalis, and the significance of pH in relation to precipitation. Journal of the Marine Biological Association of the United Kingdom 57, 1095–1109.CrossRefGoogle Scholar
Doney, SC, Busch, DS, Cooley, SR and Kroeker, KJ (2020) The impacts of ocean acidification on marine ecosystems and reliant human communities. Annual Reviews of Environment and Resources 45, 83–112.CrossRefGoogle Scholar
Doney, SC, Fabry, VJ, Feely, RA and Kleypas, JA (2009) Ocean acidification: The other CO2 problem. Annual Review of Marine Science 1, 169–192.CrossRefGoogle ScholarPubMed
Doo, SS, Leplastrier, A, Graba-Landry, A, Harianto, J, Coleman, RA and Byrne, M (2020) Amelioration of ocean acidification and warming effects through physiological buffering of a macroalgae. Ecology and Evolution 10, 8465–8475.CrossRefGoogle ScholarPubMed
Duarte, CM, Bruhn, A and Krause-Jensen, D (2022) A seaweed aquaculture imperative to meet global sustainability targets. Nature Sustainability 5, 185–193.CrossRefGoogle Scholar
Duarte, CM, Hendriks, IE, Moore, TS, Olsen, YS, Steckbauer, A, Ramajo, L, Carstensen, J, Trotter, JA and McCulloch, M (2013) Is ocean acidification an open-ocean syndrome? Understanding anthropogenic impacts on seawater pH. Estuaries and Coasts 36, 221–236.CrossRefGoogle Scholar
Duarte, CM, Marbà, N, Gacia, E, Fourqurean, JW, Beggins, J, Barrón, C and Apostolaki, ET (2010) Seagrass community metabolism: Assessing the carbon sink capacity of seagrass meadows. Global Biogeochemical Cycles 24, GB4032.CrossRefGoogle Scholar
Duarte, CM, Middelburg, JJ and Caraco, N (2005) Major role of marine vegetation on the oceanic carbon cycle. Biogeosciences 2, 1–8.CrossRefGoogle Scholar
Evans, RD, Wilson, SK, Field, SN and Moore, JAY (2014) Importance of macroalgal fields as coral reef fish nursery habitat in north-west Australia. Marine Biology 161, 599–607.CrossRefGoogle Scholar
Fabry, VJ, Seibel, BA, Feely, RA and Orr, JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Science: Journal du Conseil 65, 414–432.Google Scholar
Falkenberg, LJ, Scanes, E, Ducker, J and Ross, PM (2021) Biotic habitats as refugia under ocean acidification. Conservation Physiology 9, coab077.CrossRefGoogle ScholarPubMed
Feely, RA, Sabine, CL, Lee, K, Berelson, W, Kleypas, J, Fabry, VJ and Millero, FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362–366.CrossRefGoogle ScholarPubMed
Fernández, PA, Hurd, CL and Roleda, MY (2014) Bicarbonate uptake via an anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH. Journal of Phycology 50, 998–1008.CrossRefGoogle ScholarPubMed
Fernández, PA, Roleda, MY and Hurd, CL (2015) Effects of ocean acidification on the photosynthetic performance, carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera. Photosynthesis Research 124, 293–304.CrossRefGoogle ScholarPubMed
Fernández, PA, Leal, PP and Henríquez, LA (2019) Co-culture in marine farms: macroalgae can act as chemical refuge for shell-forming molluscs under an ocean acidification scenario. Phycologia 58, 542–551.CrossRefGoogle Scholar
Filbee-Dexter, K, Wernberg, T, Fredriksen, S, Norderhaug, KM and Pedersen, MF (2019) Arctic kelp forests: Diversity, resilience and future. Global and Planetary Change 172, 1–14.CrossRefGoogle Scholar
Flores-Moya, A (2012) Warm temperate seaweed communities: A case study of deep water kelp forests from the Alboran Sea (SW Mediterranean Sea) and the strait of Gibraltar. In Wiencke, C and Bischof, K (eds), Seaweed Biology. Berlin, Heidelberg: Springer, pp. 315–327.CrossRefGoogle Scholar
Flores-Moya, A and Fernández, JA (1998) The role of external carbonic anhydrase in the photosynthetic use of inorganic carbon in the deep-water alga Phyllariopsis purpurascens (Laminariales, Phaeophyta). Planta 207, 115–119.CrossRefGoogle Scholar
Fong, P and Paul, VJ (2011) Coral reef algae. In Dubinsky, Z and Stambler, N (eds), Coral Reefs: An Ecosystem in Transition. Dordrecht: Springer, pp. 241–272.CrossRefGoogle Scholar
Fourqurean, JW, Duarte, CM, Kennedy, H, Marbà, N, Holmer, M, Mateo, MA, Apostolaki, ET, Kendrick, GA, Krause-Jensen, D and McGlathery, KJ (2012) Seagrass ecosystems as a globally significant carbon stock. Nature Geoscience 5, 505–509.CrossRefGoogle Scholar
Frieder, CA, Gonzalez, JP, Bockmon, EE, Navarro, MO and Levin, LA (2014) Can variable pH and low oxygen moderate ocean acidification outcomes for mussel larvae. Global Change Biology 20, 754–764.CrossRefGoogle ScholarPubMed
Frieder, CA, Nam, SH, Martz, TR and Levin, LA (2012) High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences 9, 3917–3930.CrossRefGoogle Scholar
Gao, K and McKinley, KR (1994) Use of macroalgae for marine biomass production and CO2 remediation: A review. Journal of Applied Phycology 6, 45–60.CrossRefGoogle Scholar
Giordano, M, Beardall, J and Raven, JA (2005) CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56, 99–131.CrossRefGoogle ScholarPubMed
Guy-Haim, T, Silverman, J, Wahl, M, Aguirre, J, Noisette, F and Rilov, G (2020) Epiphytes provide micro-scale refuge from ocean acidification. Marine Environmental Research 161, 105093.CrossRefGoogle ScholarPubMed
Hanelt, D, Wiencke, C and Bischof, K (2003) Photosynthesis in marine macroalgae. In Larkum, AWD, Douglas, SE and Raven, JA (eds), Photosynthesis in Algae. Dordrecht: Springer, pp. 413–435.Google Scholar
Hendriks, IE, Olsen, YS, Ramajo, L, Basso, L, Steckbauer, A, Moore, TS, Howard, J and Duarte, CM (2014) Photosynthetic activity buffers ocean acidification in seagrass meadows. Biogeosciences 11, 333–346.CrossRefGoogle Scholar
Hepburn, CD, Pritchard, DW, Cornwall, CE, McLeod, RJ, Beardall, J, Raven, JA and Hurd, CL (2011) Diversity of carbon use strategies in a kelp forest community: Implications for a high CO2 ocean. Global Change Biology 17, 2488–2497.Google Scholar
Hernández, BA (2021) Canopy-Forming Gelidiales from the Canary Islands: Morphology, Reproduction and Historical Evolution of their Populations. Doctoral dissertation, University de la Laguna, San Cristóbal de La Laguna.Google Scholar
Heuer, RM and Grosell, M (2014) Physiological impacts of elevated carbon dioxide and ocean acidification on fish. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 307, 1061–1084.Google ScholarPubMed
Hofmann, GE, Barry, JP, Edmunds, PJ, Gates, RD, Hutchins, DA, Klinger, T and Sewell, MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: An organism-to-ecosystem perspective. Annual Review of Ecology, Evolution, and Systematics 41, 127–147.CrossRefGoogle Scholar
Hofmann, LC and Bischof, K (2014) Ocean acidification effects on calcifying macroalgae. Aquatic Biology 22, 261–279.CrossRefGoogle Scholar
Houlihan, EP, Espinel-Velasco, N, Cornwall, CE, Pilditch, CA and Lamare, MD (2020) Diffusive boundary layers and ocean acidification implications for urchin settlement and growth. Frontiers in Marine Science 7, 577562.CrossRefGoogle Scholar
Huovinen, P and Gómez, I (2012) Cold-temperate seaweed communities of the southern hemisphere. In Wiencke, C and Bischof, K (eds), Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization. Berlin, Heidelberg: Springer, pp. 293–313.CrossRefGoogle Scholar
Hurd, CL (2015) Slow-flow habitats as refugia for coastal calcifiers from ocean acidification. Journal of Phycology 51, 599–605.CrossRefGoogle ScholarPubMed
Hurd, CL, Harrison, PJ, Bischof, K and Lobban, CS (2014) Seaweed Ecology and Physiology. Campbridge: Cambridge University Press.CrossRefGoogle Scholar
Isah, RR, Enochs, IC and San Diego-McGlone, ML (2022) Sea surface carbonate dynamics at reefs of Bolinao, Phillipines: Seasonal variation and fish mariculture-induced forcing. Frontiers in Marine Science 9, 858853.Google Scholar
James, NC and Whitfield, AK (2022) The role of macroalgae as nursery areas for fish species within coastal seascapes. Coastal Futures 1, e3.CrossRefGoogle Scholar
Jiang, Z, Jiang, W, Rastrick, SPS, Wang, X, Fang, J, Du, M, Gao, Y, Mao, Y, Strand, Ø and Fang, J (2022) The potential of kelp Saccharina japonica in shielding Pacific oyster Crassostrea gigas from elevated pCO2 stress. Frontiers in Marine Science 9, 862172.CrossRefGoogle Scholar
Johnston, AM, Maberly, SC and Raven, JA (1992) The acquisition of inorganic carbon by four red macroalgae. Oecologia 92, 317–326.CrossRefGoogle ScholarPubMed
Kalokora, OJ, Buriyo, AS, Asplund, ME, Gullström, M, Mtolera, MSP, Björk, M (2020) An experimental assessment of algal calcification as a potential source of atmospheric CO2. PLoS One 15, e0231971.CrossRefGoogle ScholarPubMed
Kapsenberg, L and Cyronak, T (2019) Ocean acidification refugia in variable environments. Global Change Biology 25, 3201–3214.CrossRefGoogle ScholarPubMed
Koch, M, Bowes, G, Ross, C and Zhang, X (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19, 103–132.CrossRefGoogle ScholarPubMed
Koweek, DA, Zimmerman, RC, Hewett, KM, Gaylord, B, Giddings, SN, Nickols, KJ, Ruesink, JL, Stachowicz, JJ, Takeshita, Y and Caldeira, K (2018) Expected limits on the ocean acidification buffering potential of a temperate seagrass meadow. Ecological Applications 28, 1694–1714.CrossRefGoogle ScholarPubMed
Krause-Jensen, D and Duarte, CM (2016) Substantial role of macroalgae in marine carbon sequestration. Nature Geoscience 9, 737–742.CrossRefGoogle Scholar
Krause-Jensen, D, Duarte, CM, Hendriks, IE, Meire, L, Blicher, ME, Marbà, N and Sejr, MK (2015) Macroalgae contribute to nested mosaics of pH variability in a subarctic fjord. Biogeosciences 12, 4895–4911.CrossRefGoogle Scholar
Kubler, JE and Raven, JA (1994) Consequences of light limitation for carbon acquisition in three rhodophytes. Marine Ecology Progress Series 110, 203–209.CrossRefGoogle Scholar
Layton, C, Coleman, MA, Marzinelli, EM, Steinberg, PD, Swearer, SE, Vergés, A, Wernberg, T and Johnson, CR (2020) Kelp forest restoration in Australia. Frontiers in Marine Science 7, 74.CrossRefGoogle Scholar
Leal, PP, Hurd, CL and Fernández, PA (2017) Ocean acidification and kelp development: Reduced pH has no negative effects on meiospore germination and gametophyte development of Macrocystis pyrifera and Undaria pinnatifida. Journal of Phycology 53, 557–566.CrossRefGoogle ScholarPubMed
Leclerc, J-C, Riera, P, Lévêque, L and Davoult, D (2016) Contrasting temporal variation in habitat complexity and species abundance distributions in four kelp forest strata. Hydrobiologia 777, 33–54.CrossRefGoogle Scholar
Leliaert, F, Anderson, RJ, Bolton, JJ and Coppejans, E (2000) Subtidal understorey algal community structure in kelp beds around the cape peninsula (Western Cape, South Africa). Botanica Marina 43, 359–366.CrossRefGoogle Scholar
Li, H, Moon, H, Kang, EJ, Kim, JM, Kim, M, Lee, K, Kwak, CW, Kim, H, Kim, IN and Park, KY (2022) The diel and seasonal heterogeneity of carbonate chemistry and dissolved oxygen in three types of macroalgal habitats. Frontiers in Marine Science 9, 857153.CrossRefGoogle Scholar
Littler, MM and Littler, DS (1994) Tropical reefs as complex habitats for diverse macroalgae. In Lobban, CS and Harrison, PJ (eds), Seaweed Ecology and Physiology. New York: Campbridge University Press, pp. 72–75.Google Scholar
Lobban, CS and Harrison, PJ (1994) Seaweed Ecology and Physiology. Campbridge: Cambridge University Press.CrossRefGoogle Scholar
Lüning, K (1991) Seaweeds: Their Environment, Biogeography, and Ecophysiology. New York: John Wiley & Sons.Google Scholar
Maberly, SC (1990) Exogenous sources of inorganic carbon for photosynthesis by marine macroalgae. Journal of Phycology 26, 439–449.CrossRefGoogle Scholar
McCoy, SJ and Kamenos, NA (2015) Coralline algae (Rhodophyta) in a changing world: Integrating ecological, physiological, and geochemical responses to global change. Journal of Phycology 51, 6–24.Google Scholar
McNicholl, C, Koch, MS and Hofmann, LC (2019) Photosynthesis and light-dependent proton pumps increase boundary layer pH in tropical macroalgae: A proposed mechanism to sustain calcification under ocean acidification. Journal of Experimental Marine Biology and Ecology 521, 151208.CrossRefGoogle Scholar
Mejia, AY, Puncher, GN and Engelen, AH (2012) Macroalgae in tropical marine coastal systems. In Wiencke, C and Bischof, K (eds), Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilisation. New York: Springer, pp. 329–358.CrossRefGoogle Scholar
Menéndez, M, Martı́nez, M and Comı́n, FA (2001) A comparative study of the effect of pH and inorganic carbon resources on the photosynthesis of three floating macroalgae species of a Mediterranean coastal lagoon. Journal of Experimental Marine Biology and Ecology 256, 123–136.CrossRefGoogle ScholarPubMed
Mercado, JM, Viñgla, B, Figueroa, FL and Niell, FX (1999) Isoenzymic forms of carbonic anhydrase in the red macroalga Porphyra leucostica. Physiologia Plantarum 106, 69–74.Google Scholar
Middelboe, AL and Hansen, PJ (2007) High pH in shallow-water macroalgal habitats. Marine Ecology Progress Series 338, 107–117.CrossRefGoogle Scholar
Morelli, TL, Daly, C, Dobrowski, SZ, Dulen, DM, Ebersole, JL, Jackson, ST, Lundquist, JD, Millar, CI, Maher, SP and Monahan, WB (2016) Managing climate change refugia for climate adaptation. PLoS One 11, e0159909.CrossRefGoogle ScholarPubMed
Muguerza, N, Díez, I, Quintano, E and Gorostiaga, JM (2022) Decades of biomass loss in the shallow rocky subtidal vegetation of the South-Eastern Bay of Biscay. Marine Biodiversity 52, 1–18.CrossRefGoogle Scholar
Murru, M and Sandgren, CD (2004) Habitat matters for inorganic carbon acquisition in 38 species of red macroalgae (Rhodophyta) from puget sound, Washington, USA. Journal of Phycology 40, 837–845.CrossRefGoogle Scholar
Nagelkerken, I and Munday, PL (2016) Animal behaviour shapes the ecological effects of ocean acidification and warming: Moving from individual to community-level responses. Global Change Biology 22, 974–989.CrossRefGoogle ScholarPubMed
Narvarte, BC, Nelson, WA and Roleda, MY (2020) Inorganic carbon utilization of tropical calcifying macroalgae and the impacts of intensive mariculture-derived coastal acidification on the physiological performance of the rhodolith Sporolithon sp. Environmental Pollution 266, 115344.CrossRefGoogle ScholarPubMed
Nizamuddin, M (1970) Phytogeography of the Fucales and their seasonal growth. Botanica Marina 13, 131–139.CrossRefGoogle Scholar
Noisette, F and Hurd, C (2018) Abiotic and biotic interactions in the diffusive boundary layer of kelp blades create a potential refuge from ocean acidification. Functional Ecology 32, 1329–1342.CrossRefGoogle Scholar
Pacella, SR, Brown, CA, Waldbusser, GG, Labiosa, RG and Hales, B (2018) Seagrass habitat metabolism increases short-term extremes and long-term offset of CO2 under future ocean acidification. Proceedings of the National Academy of Sciences 115, 3870–3875.CrossRefGoogle ScholarPubMed
Park, PK (1969) Oceanic CO2 system: An evaluation of ten methods of investigation. Limnology and Oceanography 14, 179–186.CrossRefGoogle Scholar
Pettit, LR, Smart, CW, Hart, MB, Milazzo, M and Hall-Spencer, JM (2015) Seaweed fails to prevent ocean acidification impact on foraminifera along a shallow-water CO2 gradient. Ecology and Evolution 5, 1784–1793.CrossRefGoogle ScholarPubMed
Pörtner, HO (2008) Ecosystem effects of ocean acidification in times of ocean warming: A physiologist’s view. Marine Ecology Progress Series 373, 203–217.CrossRefGoogle Scholar
Porzio, L, Buia, MC and Hall-Spencer, JM (2011) Effects of ocean acidification on macroalgal communities. Journal of Experimental Marine Biology and Ecology 400, 278–287.CrossRefGoogle Scholar
Quintano, E, Díez, I, Muguerza, N, Figueroa, FL and Gorostiaga, JM (2017) Bed structure (frond bleaching, density and biomass) of the red alga Gelidium corneum under different irradiance levels. Journal of Sea Research 130, 180–188.CrossRefGoogle Scholar
Quintano, E, Díez, I, Muguerza, N, Figueroa, FL and Gorostiaga, JM (2018) Depth influence on biochemical performance and thallus size of the red alga Gelidium corneum. Marine Ecology 39, e12478.CrossRefGoogle Scholar
Rautenberger, R, Fernández, PA, Strittmatter, M, Heesch, S, Cornwall, CE, Hurd, CL and Roleda, MY (2015) Saturating light and not increased carbon dioxide under ocean acidification drives photosynthesis and growth in Ulva rigida (Chlorophyta). Ecology and Evolution 5, 874–888.CrossRefGoogle Scholar
Raven, JA (1995) Photosynthetic and non-photosynthetic roles of carbonic anhydrase in algae and cyanobacteria. Phycologia 34, 93–101.CrossRefGoogle Scholar
Raven, JA (1997) Inorganic carbon acquisition by marine autotrophs. Advances in Botanical Research 27, 85–209.CrossRefGoogle Scholar
Raven, JA (2003) Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynthesis Research 77, 155–171.CrossRefGoogle Scholar
Raven, JA (2011) Effects on marine algae of changed seawater chemistry with increasing atmospheric CO2. Biology and Environment – Proceedings of the Royal Irish Academy 111B, 1–17.CrossRefGoogle Scholar
Raven, JA and Hurd, CL (2012) Ecophysiology of photosynthesis in macroalgae. Photosynthesis Research 113, 105–125.CrossRefGoogle ScholarPubMed
Robertson, BL (1987) Reproductive ecology and canopy structure of Fucus spiralis L. Botanica Marina 30, 475–482.CrossRefGoogle Scholar
Roleda, MY, Boyd, PW and Hurd, CL (2012a) Before ocean acidification: Calcifier chemistry lessons. Journal of Phycology 48, 840–843.CrossRefGoogle ScholarPubMed
Roleda, MY, Cornwall, CE, Feng, Y, McGraw, CM, Smith, AM and Hurd, CL (2015) Effect of ocean acidification on the growth and development of corraline algal recruits, and an associated benthic algal assemblage. PLoS One 10, e0140394.CrossRefGoogle Scholar
Roleda, MY, Morris, JN, McGraw, CM and Hurd, CL (2012b) Ocean acidification and seaweed reproduction: Increased CO2 ameliorates the negative effect of lowered pH on meiospore germination in the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae). Global Change Biology 18, 854–864.CrossRefGoogle Scholar
Roleda, MY, Wiencke, C, Hanelt, D and Bischof, K (2007) Sensitivity of the early life stages of macroalgae from the northern hemisphere to ultraviolet radiation. Photochemistry and Photobiology 83, 851–862.CrossRefGoogle ScholarPubMed
Sabine, CL, Feely, RA, Gruber, N, Key, RM, Lee, K, Bullister, JL, Wanninkhof, R, Wong, CSL, Wallace, DWR and Tilbrook, B (2004) The oceanic sink for anthropogenic CO2. Science 305, 367–371.CrossRefGoogle ScholarPubMed
Saderne, V, Fietzek, P and Herman, PM (2013) Extreme variations of pCO2 and pH in a macrophyte meadow of the Baltic Sea in summer: Evidence of the effect of photosynthesis and local upwelling. PLoS One 8, e62689.CrossRefGoogle Scholar
Saderne, V and Wahl, M (2013) Differential responses of calcifying and non-calcifying epibionts of a brown macroalga to present-day and future upwelling pCO2. PLoS One 8, e70455.CrossRefGoogle Scholar
Savoie, AM, Moody, A, Gilbert, M, Dillon, KS, Howden, SD, Shiller, AM and Hayes, CT (2022) Impact of local rivers on coastal acidification. Limnology and Oceanography 67, 2779–2795.CrossRefGoogle Scholar
Schiel, DR and Foster, MS (2015) The Biology and Ecology of Giant Kelp Forests. Oakland: University of California Press.Google Scholar
Semesi, S, Kangwe, J and Björk, M (2009) Alterations in seawater pH and CO2 affect calcification and photosynthesis in the tropical coralline alga, Hydrolithon sp. (Rhodophyta). Estuarine, Coastal and Shelf Science 84, 337–341.CrossRefGoogle Scholar
Shepherd, S and Edgar, G (2013) Ecology of Australian Temperate Reefs: The Unique South. Melbourne: CSIRO Publishing.CrossRefGoogle Scholar
Short, J, Kendrick, GA, Falter, J and McCulloch, MT (2014) Interactions between filamentous turf algae and coralline algae are modified under ocean acidification. Journal of Experimental Marine Biology and Ecology 456, 70–77.CrossRefGoogle Scholar
Smale, DA, Pessarrodona, A, King, N, Burrows, MT, Yunnie, A, Vance, T and Moore, P (2020) Environmental factors influencing primary productivity of the forest-forming kelp Laminaria hyperborea in the Northeast Atlantic. Scientific Reports 10, 1–12.CrossRefGoogle ScholarPubMed
Steneck, RS, Graham, MH, Bourque, BJ, Corbett, D, Erlandson, JM, Estes, JA and Tegner, MJ (2002) Kelp forest ecosystems: Biodiversity, stability, resilience and future. Environmental Conservation 29, 436–459.CrossRefGoogle Scholar
Stepien, CC, Pfister, CA and Wootton, JT (2016) Functional traits for carbon access in macrophytes. PLoS One 11, e0159062.CrossRefGoogle ScholarPubMed
Surif, MB and Raven, JA (1989) Exogenous inorganic carbon sources for photosynthesis in seawater by members of the Fucales and the Laminariales (Phaeophyta): Ecological and taxonomic implications. Oecologia 78, 97–105.CrossRefGoogle ScholarPubMed
Takahashi, T, Sutherland, SC, Sweeney, C, Poisson, A, Metzl, N, Tilbrook, B, Bates, N, Wanninkhof, R, Feely, RA and Sabine, C (2002) Global sea–air CO2 flux based on climatological surface ocean pCO2, and seasonal biological and temperature effects. Deep Sea Research Part II: Topical Studies in Oceanography 49, 1601–1622.CrossRefGoogle Scholar
Teagle, H, Hawkins, SJ, Moore, PJ and Smale, DA (2017) The role of kelp species as biogenic habitat formers in coastal marine ecosystems. Journal of Experimental Marine Biology and Ecology 492, 81–98.CrossRefGoogle Scholar
Wahl, M, Saderne, V and Sawall, Y (2015) How good are we at assessing the impact of ocean acidification in coastal systems? Limitations, omissions and strengths of commonly used experimental approaches with special emphasis on the neglected role of fluctuations. Marine and Freshwater Research 67, 25–36.CrossRefGoogle Scholar
Wahl, M, Schneider Covachã, S, Saderne, V, Hiebenthal, C, Müller, JD, Pansch, C and Sawall, Y (2018) Macroalgae may mitigate ocean acidification effects on mussel calcification by increasing pH and its fluctuations. Limnology and Oceanography 63, 3–21.CrossRefGoogle Scholar
Wallace, RB, Baumann, H, Grear, JS, Aller, RC and Gobler, CJ (2014) Coastal ocean acidification: The other eutrophication problem. Estuarine, Coastal and Shelf Science 148, 1–13.CrossRefGoogle Scholar
Wernberg, T, Krumhansl, K, Filbee-Dexter, K and Pedersen, MF (2019) Status and trends for the world’s kelp forests. In Sheppard, C (ed.), World Seas: An Environmental Evaluation. Amsterdam: Elsevier, pp. 57–78.CrossRefGoogle Scholar
Wiencke, C and Amsler, CD (2012) Seaweeds and their communities in polar regions. In Wiencke, C and Bischof, K (eds), Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization. Berlin, Heidelberg: Springer, pp. 265–294.CrossRefGoogle Scholar
Wilson, SK, Depczynski, M, Fisher, R, Holmes, TH, O’Leary, RA and Tinkler, P (2010) Habitat associations of juvenile fish at Ningaloo reef, Western Australia: The importance of coral and algae. PLoS One 5, e15185.CrossRefGoogle ScholarPubMed
Xiao, X, Agustí, S, Yu, Y, Huang, Y, Chen, W, Hu, J, Li, C, Li, K, Wei, F, Lu, Y, Xu, C, Chen, Z, Liu, S, Zeng, J, Wu, J and Duarte, CM (2021). Seaweed farms provide refugia from ocean acidification. Science of the Total Environment 776, 145192.CrossRefGoogle ScholarPubMed
Yip, ZT, Quek, RZB and Huang, D (2020) Historical biogeography of the widespread macroalga Sargassum (Fucales, Phaeophyceae). Journal of Phycology 56, 300–309.Google ScholarPubMed
Young, CS and Gobler, CJ (2018) The ability of macroalgae to mitigate the negative effects of ocean acidification on four species of North Atlantic bivalve. Biogeosciences 15, 6167–6183.CrossRefGoogle Scholar
Young, CS, Sylvers, LH, Tomasetti, SJ, Lundstrom, A, Schenone, C, Doall, MH and Gobler, CJ (2022) Kelp (Saccharina latissima) mitigates coastal ocean acidification and increases the growth of North Atlantic bivalves in lab experiments on an oyster farm. Frontiers in Marine Science 9, 513.CrossRefGoogle Scholar
Zacher, K, Rautenberger, R, Hanelt, D, Wulff, A and Wiencke, C (2009) The abiotic environment of polar marine benthic algae. Botanica Marina 52, 483–490.CrossRefGoogle Scholar
Zacharia, PU, Kaladharan, P and Rohith, G (2015). Seaweed farming as a climate resilient strategy for Indian coastal waters in The International Conference on Integrating Climate, Crop, Ecology – The Emerging Areas of Agriculture, Horticulture, Livestock, Fishery, Forestry, Biodiversity, and Policy Issues, New Delhi.Google Scholar
Zou, D and Gao, K (2010) Acquisition of inorganic carbon by Endarachne binghamiae (Scytosiphonales, Phaeophyceae). European Journal of Phycology 45, 117–126.CrossRefGoogle Scholar
Figure 0

Figure 1. Distribution of coastal temperature zones based on Briggs, 1995 (reproduced from Bartsch et al., 2012). Blue, polar regions; green, cool temperate; yellow, warm temperate; red, tropical.

Figure 1

Figure 2. Modelled distribution of brown forest forming macroalgal species (after Assis et al., 2020).

Figure 2

Table 1. Examples of studies assessing the ocean acidification (OA) refuge provision by macroalgal species for various coastal organisms

Author comment: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R0/PR1

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr1 [Opens in a new window]
Carla Edworthy South African Institute for Aquatic Biodiversity, South Africa
Revision round: 0
Role: author

Comments

The Editor in Chief: Coastal Futures

31 August 2022

Herewith please find our invited review entitled “The role of macroalgal habitats as ocean acidification refugia within coastal seascapes” by Carla Edworthy, Paul-Pierre Steyn and Nicola James for consideration in Coastal Futures.

Yours sincerely,

Dr Carla Edworthy

Review: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R0/PR2

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr2 [Opens in a new window]
Michael Y. Roleda [Opens in a new window] University of the Philippines Diliman
Date of review:  25 September 2022
Revision round: 0
Role: reviewer
Recommendation/decision: major-revision

Conflict of interest statement

N/A

Comments

Comments to Author: The review lacks details on the carbon physiology of different taxa and scrutiny on seaweeds with alternating heteromorphic life history. Moreover, discussion on the use of carbonate ions for calcification is controversial.

For the perpetuation of the macroalgal habitats that serve as refugia for other organisms, the authors are advised to consider a brief discussion on how different life history stages of seaweeds with alternating heteromorphic life cycle (i.e., microscopic spores and gametophytes, and macroscopic sporophytes) of e.g., kelps respond to OA. The negative effect is relatively minimal to insignificant (e.g., Roleda et al. 2012, Leal et al. 2017, among others). As such, the microstages readily provide continuous source of propagules for the next generation of macroscopic sporophytes. Moreover, even under a worst-case OA scenario with diel fluctuating pH, benthic floral community of primarily coralline macroalgae and associated diatoms and fleshy macroalgae were observed to develop suggesting the relative resilience of photosynthetic organisms to OA (Roleda et al. 2015).

The carbon physiology of the species is also important to discuss among specific taxa (e.g., brown, red, and green; Fernandez et al. 2014, 2015, Narvarte et al. 2020, and Rautenberger et al. 2015, respectively)- despite mostly being bicarbonate users, they are relatively resilient to OA and/or localized coastal acidification.

On the use carbonate ions for calcification. The authors should check other literature or provide context on the biological/physiological functions of carbonate and information on carbonate uptake/transport mechanism(s). Otherwise, please check Roleda, Boyd and Hurd 2012 (and references therein), who suggested otherwise. Moreover, there is a plethora of literature that suggest CO2 and HCO3, and not CO32, are the substrate for calcification.

Recommendation: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R0/PR3

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr3 [Opens in a new window]
Siyuan Ye [Opens in a new window] Qingdao Institute of Marine Geology, China
Date of review:  14 December 2022
Revision round: 0
Role: Handling Editor
Recommendation/decision: major-revision

Comments

No accompanying comment.

Decision: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R0/PR4

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr4 [Opens in a new window]
Tom Spencer Geography, Cambridge University, United Kingdom of Great Britain and Northern Ireland
Revision round: 0
Role: Editor in Chief
Recommendation/decision: major-revision

Comments

No accompanying comment.

Author comment: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R1/PR5

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr5 [Opens in a new window]
Carla Edworthy South African Institute for Aquatic Biodiversity, South Africa
Revision round: 1
Role: author

Comments

No accompanying comment.

Review: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R1/PR6

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr6 [Opens in a new window]
Michael Y. Roleda [Opens in a new window] University of the Philippines Diliman
Date of review:  09 February 2023
Revision round: 1
Role: reviewer
Recommendation/decision: minor-revision

Conflict of interest statement

Reviewer declares none.

Comments

Comments to Author: The revised manuscript of Edworthy and co-workers is in a fine shape. The author should consider elaborating on coastal acidification and address the few minor concerns below:

Re: coastal acidification. Check Isah et al. 2022 https://doi.org/10.3389/fmars.2022.858853 on spatial and temporal variation of sea surface carbonate chemistry and its potential effects on calcifying seaweed (See Narvarte et al. 2022 https://doi.org/10.1016/j.envpol.2020.115344)

When coastal acidification is related to decomposition of high organic input, releasing CO2 and nutrient during decomposition, does nutrient status mitigate negative impacts of OA? See papers below.

Fernández et al. (2017) Seawater pH, and not inorganic nitrogen source, affects pH at the blade surface of Macrocystis pyrifera: implications for responses of the giant kelp to future oceanic conditions. Physiologia Plantarum 159:107-119. https://doi.org/10.1111/ppl.12478

Fernández et al. (2017) Tissue nitrogen status does not alter the physiological responses of Macrocystis pyrifera to ocean acidification. Marine Biology 164: 177. https://doi.org/10.1007/s00227-017-3204-z

Line 48-50: Is CCM not primarily related to the use of HCO3 as inorganic carbon source facilitated by the enzyme carbonic anhydrase? How is CO2 actively transported through the membrane? Is CO2 not primarily passively transported through the membrane depending on the concentration gradient? Inside the cell CO2 is converted to HCO3 by CA to avoid leakage.

See Fernández PA, Hurd CL, Roleda MY (2014) Bicarbonate uptake via an anion exchange protein is the main mechanism of inorganic carbon acquisition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) under variable pH. Journal of Phycology. 50:998-1008. https://doi.org/10.1111/jpy.12247

Line 68-69: Please contextualize. Respiration do occurs during day and night while photosynthesis occurs only during day time.

Line 82-85: Is the use of carbonate ions in relation to extracellular calcification? Better elaborate as there is no known transport mechanism of carbonate ions from the bulk seawater into the cell for calcification.

Double check integrity of reference list. For example, line 599.

Please submit a clean manuscript with highlighted revised text.

Recommendation: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R1/PR7

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr7 [Opens in a new window]
Siyuan Ye [Opens in a new window] Qingdao Institute of Marine Geology, China
Date of review:  17 February 2023
Revision round: 1
Role: Handling Editor
Recommendation/decision: minor-revision

Comments

Comments to Author: I think the author has addressed the reviewer’s questions. My concerns are that the authors need to make a stronger take home message in the conclusion section. As a review article, it is necessary to tell the knowledge gaps in this research field. The review article also may need some graphs to illustration some significant progresses.

Decision: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R1/PR8

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr8 [Opens in a new window]
Tom Spencer Geography, Cambridge University, United Kingdom of Great Britain and Northern Ireland
Revision round: 1
Role: Editor in Chief
Recommendation/decision: minor-revision

Comments

No accompanying comment.

Author comment: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R2/PR9

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr9 [Opens in a new window]
Carla Edworthy South African Institute for Aquatic Biodiversity, South Africa
Revision round: 2
Role: author

Comments

No accompanying comment.

Recommendation: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R2/PR10

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr10 [Opens in a new window]
Siyuan Ye [Opens in a new window] Qingdao Institute of Marine Geology, China
Revision round: 2
Role: Handling Editor
Recommendation/decision: minor-revision

Comments

Comments to Author: I think the author has addressed the reviewer’s questions. My concerns are that the authors need to make a stronger take home message in the conclusion section. As a review article It is necessary to tell the knowledge gaps in this research field. The review article also needs 1-2 graphs to illustration the research progresses.

Decision: The role of macroalgal habitats as ocean acidification refugia within coastal seascapes — R2/PR11

Published online by Cambridge University Press:  21 March 2023
DOI: https://doi.org/10.1017/cft.2023.9.pr11 [Opens in a new window]
Tom Spencer Geography, Cambridge University, United Kingdom of Great Britain and Northern Ireland
Revision round: 2
Role: Editor in Chief
Recommendation/decision: accept

Comments

No accompanying comment.