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

Abstract

Ocean acidification (OA) refers to a global decline in the average pH of seawater driven by the absorption of atmospheric carbon dioxide (CO 2 ). 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 CO 2 and HCO 3 ⁻ 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.

Full text

The role of macroalgal habitats as ocean
acidification refugia within coastal seascapes
Carla Edworthy
1,2
, Paul-Pierre Steyn
2,3
and Nicola C. James
1,2
1
South African Institute for Aquatic Biodiversity, Makhanda, South Africa;
2
Institute for Coastal and Marine Research,
Nelson Mandela University, Gqeberha, South Africa and
3
Department of Botany, Nelson Mandela University, Gqeberha,
South Africa
Abstract
Ocean acidification (OA) refers to a global decline in the average pH of seawater driven by the
absorption of atmospheric carbon dioxide (CO
2
). 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 CO
2
and HCO
3

during photosynthesis, raising surround-
ing 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.
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, 2019). OA is a conse-
quence of increasing anthropogenic emissions of carbon dioxide (CO
2
) into the earth’s atmos-
phere (Caldeira and Wickett, 2003; Sabine et al., 2004; Doney et al., 2009). This global process
results from increased absorption of atmospheric CO
2
by the oceans, which ultimately shifts the
carbonate chemistry equilibrium of seawater resulting in a decline in average seawater pH
(Doney et al., 2009; Dickson, 2010). 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 CO
2
and bicarbonate (HCO
3

) and a decrease in carbonate ions (CO
32
) (Feely et al.,
2004; Dickson, 2010).
Cambridge Prisms: Coastal
Futures
www.cambridge.org/cft
Review
Cite this article: Edworthy C, Steyn P-P and
James NC (2023). The role of macroalgal
habitats as ocean acidification refugia within
coastal seascapes. Cambridge Prisms: Coastal
Futures,1, e22, 1–10
https://doi.org/10.1017/cft.2023.9
Received: 31 August 2022
Revised: 10 March 2023
Accepted: 11 March 2023
Keywords:
global change; carbonate chemistry;
photosynthesis; biochemistry
Corresponding author:
Carla Edworthy;
Email: c.edworthy@saiab.nrf.ac.za
© The Author(s), 2023. Published by Cambridge
University Press. 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.

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., 2014; Doney
et al., 2020; Isah et al., 2022; Savoie et al., 2022). These changes in
ocean chemistry have implications for marine organisms and eco-
systems by reducing carbonate ion availability for calcification
(Hofmann et al., 2010) and disrupting key biological processes
through changes in pH (e.g., organism physiology and behaviour;
Pörtner, 2008; Heuer and Grosell, 2014; Clements and Hunt, 2015;
Nagelkerken and Munday, 2016).
While lowered seawater pH caused by OA can have substantial
impacts on coastal vegetation (Koch et al., 2013; Narvarte et al.,
2020), 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.,
2015). 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., 2008; Duarte et al., 2010; Alongi,
2012; Fourqurean et al., 2012; Chmura, 2013; Krause-Jensen and
Duarte, 2016). However, the role that coastal vegetated habitats play
in influencing localised carbonate chemistry and pH of surround-
ing 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 tem-
poral scales (Middelboe and Hansen, 2007; Wahl et al., 2018;
McNicholl et al., 2019) through autotrophic, calcification and
respiration processes (Middelboe and Hansen, 2007; Krause-Jensen
and Duarte, 2016). These localised zones of elevated pH associated
with macroalgal beds could potentially serve as OA refugia
(Noisette and Hurd, 2018). For example, Wahl et al. (2018) 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 photo-
synthetic activity). This allowed mussels (Mytilus edulis) to main-
tain calcification even under acidified conditions and suggests that
seagrass and macroalgae may mitigate the impact of OA on organ-
isms 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 CO
2
, together
with water and light, to produce glucose and oxygen (Hanelt et al.,
2003). In aquatic and marine environments, DIC exists in differ-
ent forms: CO
2
,HCO
3

and CO
32
(Cornwall et al., 2015;Stepien
et al., 2016). In seawater, DIC predominantly occurs in the form of
HCO
3

(~90%) and not as dissolved CO
2
gas (<1%) due to the
rapid dissociation of CO
2
in seawater (Park, 1969). As such, most
macroalgae have evolved carbon concentrating mechanisms
(CCMs), which facilitate the active uptake of DIC in the form of
HCO
3

using various energy-driven mechanisms, such as exter-
nal conversion of HCO
3

to CO
2
catalysed by the enzyme car-
bonic anhydrase (common in red, green and brown seaweeds; e.g.,
Flores-Moya and Fernández, 1998;Axelssonetal.,1999;Mercado
et al., 1999)orthroughtheuptakeofHCO
3

directly in this form
via anion exchange proteins or proton pumps (Fernández et al.,
2014). Once taken up into the cells, the enzyme carbonic anhy-
drase facilitates the interconversion of DIC to make it available for
photosynthesis (Raven, 1995). In many macroalgal species, CCMs
are used in addition to passive CO
2
diffusion (Maberly, 1990;
Raven, 2003; Giordano et al., 2005;Cornwalletal.,2015;Stepien
et al., 2016) depending on the availability and forms of DIC in
surrounding seawater. Very few macroalgal species rely on passive
CO
2
diffusion alone for DIC uptake (Raven, 2003;Giordanoetal.,
2005; Raven and Hurd, 2012; Stepien et al., 2016).
The DIC acquisition strategies employed vary among macro-
algal species and taxonomic groups (Maberly, 1990; Raven, 1997).
Green algae, like Ulva, for example, can efficiently use both CO
2
and HCO
3

as inorganic carbon sources (Beer and Eshel, 1983;
Rautenberger et al., 2015). Brown algae species rely almost exclu-
sively on the uptake of DIC in the form of HCO
3

(Surif and Raven,
1989; Zou and Gao, 2010; Fernández et al., 2014). The red algae are
also primarily HCO
3

users, with some exceptions, like Lomentaria
articulata and Delesseria sanguinea, which lack this ability and rely
on CO
2
as a DIC source (Johnston et al., 1992; Kubler and Raven,
1994). 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,
1990; Kubler and Raven, 1994; Murru and Sandgren, 2004).
During periods when photosynthesis is not occurring or limited
(e.g., at night or under reduced light availability), there is a net release
of CO
2
gas into surrounding seawater through respiration (Duarte
et al., 2005;MiddelboeandHansen,2007; Semesi et al., 2009). This
process also influences the carbonate chemistry and forces the
equilibrium to a state that decreases pH (Middelboe and Hansen,
2007; Saderne et al., 2013; Wahl et al., 2018). 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 CO
2
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,
2016; Koweek et al., 2018; Wahl et al., 2018).
Calcification
In addition to photosynthetic needs, some macroalgal species rely
on DIC in the form of CO
32
,HCO
3

or CO
2
to build and
maintain calcium carbonate structures through the precipitation
of CaCO
3
(Roleda et al., 2012a; Hofmann and Bischof, 2014).
This process may also modulate the carbonate chemistry equi-
librium of surrounding seawater through both the absorption of
DIC and the release of CO
2
(Kalokora et al., 2020). As such, the
role that calcifying species have on carbon dynamics of surround-
ing seawater is complex, as processes of photosynthesis, calcifi-
cation and respiration simultaneously influence the carbon
system, and ultimately pH, in counteracting ways (Kalokora
et al., 2020).
The best-known calcifying group of algae are the order of red
algae, the coralline algae, that form crustose or articulated
2 Carla Edworthy et al.

structures by depositing CaCO
3
extracellularly (Hofmann and
Bischof, 2014; McCoy and Kamenos, 2015). 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, 2015). Although calcification in this group is con-
sidered to be sensitive to OA, as CO
32
is less available in seawater
under acidic conditions (Feely et al., 2004; Fabry et al., 2008; Raven,
2011; Stepien et al., 2016), the fact that many calcifying macroalgae
utilise HCO
3

or CO
2
as substrate for calcification, and not car-
bonate may limit this sensitivity (Roleda et al., 2012a). Further-
more, 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 CO
2
and/or HCO
3

(Digby, 1977; Borowitzka and Larkum, 1987),
reducing reliance on elevated ambient carbonate ion concentra-
tions. In fact, dissolution of calcified structures because of OA
might be a greater problem than reduced calcification rates
(Doney et al., 2009; Hofmann and Todgham, 2010).
Through these interactions with the carbonate system of sea-
water, macroalgae influence the carbon equilibrium of surrounding
seawater over various scales. However, for macroalgal vegetation to
play a meaningful role asOA refugia for other marineorganisms,the
density of these primary producers needs to be high enough. Macro-
algal 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 likelyto be in coastal areas with large, dense and
complex macroalgal communities or seaweed farms (Chung et al.,
2013; Zacharia et al., 2015; Fernández et al., 2019; Xiao et al., 2021).
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 (1991) described
macroalgal floras of the world in detail and the regions identified
based on macroalgal vegetation closely resemble the seven tem-
perature zones adopted by Briggs (1995)(Figure 1).
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 commu-
nities 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., 2002; Schiel and Foster, 2015; Teagle et al., 2017; Wernberg
et al., 2019). These subtidal brown algae are the most important
macroalgal primary producers based on area cover and net primary
production (Duarte et al., 2022). Kelp forest communities include a
variety of canopy-forming species that differ widely in stature.
Steneck et al. (2002) 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., 2000;
Bennett and Wernberg, 2014; Leclerc et al., 2016; Smale et al., 2020).
The smaller canopy-forming algae are from the Fucales, of
which Sargassum and Cystoseira species are the most widespread
(Nizamuddin, 1970). Sargassum is more common in the warm-
temperate, subtropical and tropical coasts (Yip et al., 2020), while
Cystoseira is most diverse in the Mediterranean (Nizamuddin,
1970). 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
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.
Cambridge Prisms: Coastal Futures 3

warmer tropical coasts such as the Caribbean and Indo-China
(Figure 2) (Assis et al., 2020).
Lower canopy-forming algae like Gelidium corneum are also
considered foundational, or habitat forming species (Quintano
et al., 2017; Borja et al., 2018; Muguerza et al., 2022), particularly
on some European coasts, with Gelidium canariense representing
an important canopy-forming species on Macronesian islands
(Alfonso et al., 2017; Hernández, 2021). 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, 1987; Quintano et al., 2018; Alfonso et al., 2021;
Hernández, 2021). 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., 2017,2018; Casado-Amezúa et al., 2019) and
Gelidium canariense (Alfonso et al., 2021; Hernández, 2021) 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., 2009). Light limitation during winter
months limits the poleward distribution of kelps that form such
extensive forests in temperate regions (Steneck et al., 2002). However,
a few Laminarian species do occur in these cold polar regions (Filbee-
Dexter et al., 2019), with macroalgal communities in cold polar waters
generally comprised of a canopy of large brown algae, with an under-
story community of foliose and coralline macroalgae (Brouwer et al.,
1995;WienckeandAmsler,2012). 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., 2019),
subtidal macroalgae communities can reach biomass values compar-
able to temperate kelp communities (Wiencke and Amsler, 2012).
Temperate algal vegetation
In cold- and warm-temperate regions, the large brown algae also
dominate the subtidal zone (Flores-Moya, 2012;Huovinenand
Gómez, 2012). 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., 2002). These are common in cooler
regions (warm and cold temperate) but relatively rare along warmer
coastlines (Bolton, 2010).Densebedsofsmallermacroalgal groups are
also common in temperate areas (Lüning, 1991; Shepherd and Edgar,
2013). 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., 2022).
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 abun-
dance of which is dependent on the interplay between herbivory,
nutrients and light availability (Hurd et al., 2014). Foliose algae are
usually rare in coral reef systems, unless there is reduction in
herbivory or an increase in nutrients (Lobban and Harrison,
1994). These algae are often fucoids like Cystoseira, Turbinaria
and Sargassum (Mejia et al., 2012). Foliose algae, along with some
coralline algae, usually form communities on the shallow shore-
ward 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, 1994). 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, 2011). Extensive macro-
algal communities are not common in tropical regions, however,
Wilson et al. (2010)andEvansetal.(2014) 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
Figure 2. Modelled distribution of brown forest forming macroalgal species (after Assis et al., 2020).
4 Carla Edworthy et al.

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 con-
sistent or cyclical, depending on several factors such as seasonal
productivity (Middelboe and Hansen, 2007), photosynthetic state
(diurnal cycles), water retention time and mixing (Middelboe and
Hansen, 2007; Buapet et al., 2013; Koch et al., 2013) and nutrient
availability (Gao and McKinley, 1994; Celis-Pla et al., 2015).
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., 2002; Saderne et al., 2013; Attard et al., 2019;
Kapsenberg and Cyronak, 2019). This means that their provision
as OA refuges may vary with seasonal differences in productivity
(Lietal.,2022). Studies have found that in most regions macro-
algal productivity is typically higher in summer and spring
months. For example, Middelboe and Hansen (2007) 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
(pCO
2
and DIC) in productive summer months, for example,
Krause-Jensen et al. (2015) in a subarctic fjord in Greenland and
Delille et al. (2009)inaSouthernOceanArchipelago.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, 2007; Semesi et al., 2009; Frieder et al., 2012;Cornwall
et al., 2013; Krause-Jensen et al., 2015;Wahletal.,2018). These
patterns occur in response to daylight availability for photosyn-
thesis. 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., 2015;Wahl
et al., 2015). The extent of diurnal variability can also be influ-
enced by physical factors, such as tidal processes or seawater
exchange. Shallow areas with less mixing and higher water reten-
tion times usually experience high diurnal pH variability
(Middelboe and Hansen, 2007; Hurd, 2015). Diurnal fluctuations
in pH can benefit associated organisms by providing cyclical or
periodic relief from OA. Wahl et al. (2018) 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.,
2018). Other studies have found similar benefits for growth,
development and physiology in other bivalve species (sum-
marised in Table 1) (Frieder et al., 2014; Young and Gobler,
2018;Jiangetal.,2022;Youngetal.,2022). However, there is
also evidence to suggest that not all species are capable of adapt-
ing their calcification process to benefit from diurnal pH vari-
ability (Cornwall et al., 2013) and, as such, may still be negatively
affected by corrosive conditions at night.
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., 2011). Macro-
algae also occur at a vast range of locations, such as in shallow
coastal areas, rock pools, estuaries or deeper subtidal locations
(Layton et al., 2020; Falkenberg et al., 2021). The distribution and
structure of macroalgal growth will offer refuge from OA at differ-
ent 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, 2018; Guy-Haim et al., 2020). Conversely, in
large- and dense-algal aggregations, biological activity can have an
influence at an extent of metres to kilometres (Krause-Jensen et al.,
2015).
On a micro-scale (centimetres) macroalgal metabolism can
create favourable micro-zones of higher pH within their diffusive
boundary layer (Noisette and Hurd, 2018; Guy-Haim et al., 2020),
where pH can be up to 1–3 units higher than surrounding sea-
water (Wahl et al., 2015). 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, 2018)(Table 1). For example,
Saderne and Wahl (2013) found that both calcifying (Electra
pilosa) and non-calcifying (Alcyonidium hirsutum)Bryozoan
species were tolerant of high pCO
2
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. (2020)foundthatan
epiphytic foraminifera, Marginopora vertebralis, showed higher
tolerance to end-of-the-century temperature (3 °C) and pCO
2
(~1,000 μatm) when kept experimentally under these treatments
with its red macroalgal host, Laurencia intricata. Similar benefi-
cial symbiotic relationships that facilitate micro-refugia from OA
exist between calcifying and non-calcifying algae. For example,
Guy-Haim et al. (2020)andShortetal.(2014) found that the
coralline algae Ellisolandia elongata and Hydrolithoideae spp. are
less susceptible to the effects of OA, evidenced by higher calcifi-
cation 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)thatarewell
adapted to pH variability and therefore show no positive or
negative response to the variable pH in their settlement habitats
(Houlihan et al., 2020).
The effect of photosynthesis on surrounding seawater carbon-
ate 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
Cambridge Prisms: Coastal Futures 5

et al., 2004; Middelboe and Hansen, 2007;Duarteetal.,2013;
Krause-Jensen et al., 2015). 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., 2014;Hurd,2015).
Macroalgae have been reported to increase the average pH
(to levels >8.5 pH units) in rock pools (Björk et al., 2004), lagoons
(Menéndez et al., 2001)andbays(Buapetetal.,2013). For
example, Krause-Jensen et al. (2015)foundpHvariabilityof
0.1–0.3 units occurs within the scale of 1 m
2
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.
(2013) 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., 2013).
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 macro-
algal 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., 2011 and Koch et al., 2013). 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., 2015; Cornwall and Hurd, 2019). Of course, there
Table 1. Examples of studies assessing the ocean acidification (OA) refuge provision by macroalgal species for various coastal organisms
References Macroalgal species Refuge function Refuge provision
Phaeophyceae
(brown)
Frieder et al., 2014 Simulations based the La Jolla
Kelp Forest (not species
specific)
Bivalve (Mytilus californianus and Mytilus
galloprovincialis) developmental delays associated with
OA mitigated under variable pH conditions simulating
kelp forest conditions.
✓
Wahl et al., 2018 Fucus vesiculosus Bivalve (mussel Mytilus edulis) calcification impacts
associated with OA mitigated in the presence of
macroalgae (F. vesiculosus).
✓
Young et al., 2022 Saccharina latissima Bivalves (Mercenaria mercenaria, Crassostrea virginica
and M. edulis) showed higher growth rates at low pH in
the presence of macroalgae (Saccharina latissima).
✓
Jiang et al., 2022 Saccharina japonica Bivalve (Pacific oyster, Crassostrea gigas) showed higher
scope for growth, clearance rate and decreased
respiration rate and excretion rate at low pH in the
presence of macroalgae (Saccharina japonica).
✓
Cornwall et al., 2014 pH simulations for a kelp
forest (not species specific)
Coralline algae (Arthrocardia corymbosa) showed further
reduced growth rates under variable OA treatments.

Saderne and Wahl, 2013 Fucus serratus Bryozoan species (calcifying Electra pilosa and non-
calcifying Alcyonidium hirsutum) showed higher tolerance
to OA (high pCO
2
) due to the periodic relief from OA
provided by macroalgae (F. serratus).
✓
Rhodophyceae
(red)
Pettit et al., 2015 Padina pavonica Negative effect of OA on Foraminifera community
composition was not mitigated by macroalgae (Padina
pavonica)

Doo et al., 2020 Laurencia intricata Effect of low pH in Foraminifera (Marginopora vertebralis)
growth and calcification mitigated in the presence of
macroalgae (L. intricata)
✓
Guy-Haim et al., 2020 Polysiphonia sp., Ceramium
sp., Rhodymenia sp.,
Ectocarpus sp. and
Chondracanthus sp.
Coralline algae Ellisolandia elongata is less susceptible to
OA when colonised with non-calcifying macroalgal
epiphytes.
✓
Houlihan et al., 2020 CCA encrusted cobbles (not
species specific)
Urchin (Pseudechinus huttoni) settlement and post
settlement growth unaffected by pH variability
associated with the CCA encrusted cobbles.
—
Chlorophyceae
(green)
Young and Gobler, 2018 Ulva sp. Juvenile North Atlantic bivalves (M. mercenaria,C.
virginica, and Argopecten irradians,M. edulis) showed
higher growth rates under OA conditions when in the
presence of Ulva.
✓
6 Carla Edworthy et al.

are exceptions with some species sensitive to OA, with sensitivity
likely linked to mechanisms of carbon uptake and calcification
(Cornwall et al., 2012; Hofmann and Bischof, 2014) 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., 2020). 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, 2014).
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., 2007). Although
the early life stages of some macroalgal species have been shown to
be more sensitive to other environmental factors (e.g., UV radi-
ation; Roleda et al., 2007), there is evidence to suggest that early life
stages are not affected by OA conditions (Roleda et al., 2012b,2015;
Leal et al., 2017). This provides positive evidence for the persistence
of macroalgal habitats in future.
Conclusion and relevance
Macroalgae form important components of shallow coastal mar-
ine 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, 2019).
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.,
2018). 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., 2021). Despite short-term fluctuations in pH
conditions, autotrophic biological activity likely provides associ-
ated organisms with long-term relief from ongoing OA (Hurd,
2015; Koweek et al., 2018; Pacella et al., 2018). 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 cal-
cifying 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., 2016;
Kapsenberg and Cyronak, 2019), especially in productive coastal
marine environments where these habitats already provide
important nursery areas for many marine species (James and
Whitfield, 2022).
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.
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.
Alongi DM (2012) Carbon sequestration in mangrove forests. Carbon Man-
agement 3, 313–322.
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.
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.
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.
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.
Beer S and Eshel A (1983) Photosynthesis of Ulva sp. II. Utilization of CO
2
and
HCO
3

when submerged. Journal of Experimental Marine Biology and
Ecology 70,99–106.
Bennett S and Wernberg T (2014) Canopy facilitates seaweed recruitment on
subtidal temperate reefs. Journal of Ecology 102, 1462–1470.
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.
Bolton JJ (2010) The biogeography of kelps (Laminariales, Phaeophyceae): A
global analysis with new insights from recent advances in molecular phylo-
genetics. Helgoland Marine Research 64, 263–279.
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.
Borowitzka MA and Larkum AWD (1987) Calcification in algae: Mechanisms
and the role of metabolism. Critical Reviews in Plant Sciences 6,1–45.
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.
Briggs JC (1995) Global Biogeography. Amsterdam: Elsevier.
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.
Buapet P,Gullström M and Björk M (2013) Photosynthetic activity of sea-
grasses 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.
Cambridge Prisms: Coastal Futures 7

Caldeira K and Wickett ME (2003) Anthropogenic carbon and ocean pH.
Nature 425, 365.
Casado-Amezúa P,Araújo R,Bárbara I,Bermejo R,Borja Á,Díez I,Fernán-
dez 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.
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.
Chmura GL (2013) What do we need to assess the sustainability of the tidal salt
marsh carbon sink? Ocean & Coastal Management 83,25–31.
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.
Clements JC and Hunt HL (2015) Marine animal behaviour in a high CO
2
ocean. Marine Ecology Progress Series 536, 259–279.
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.
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.
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.
Cornwall CE,Revill AT and Hurd CL (2015) High prevalence of diffusive
uptake of CO
2
by macroalgae in a temperate subtidal ecosystem. Photosyn-
thesis Research 124, 181–190.
Cornwall CE and Hurd CL (2019) Variability in the benefits of ocean acidifi-
cation to photosynthetic rates of macroalgae without CO2-concentrating
mechanisms. Marine and Freshwater Research 71, 275–280.
Delille B,Borges AV and Delille D (2009) Influence of giant kelp beds
(Macrocystis pyrifera) on diel cycles of pCO
2
and DIC in the sub-Antarctic
coastal area. Estuarine, Coastal and Shelf Science 81, 114–122.
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.
Digby PSB (1977) Growth and calcification in the coralline algae, Clathromor-
phum 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.
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.
Doney SC,Fabry VJ,Feely RA and Kleypas JA (2009) Ocean acidification: The
other CO
2
problem. Annual Review of Marine Science 1, 169–192.
Doo SS,Leplastrier A,Graba‐Landry A,Harianto J,Coleman RA andByrne M
(2020) Amelioration of ocean acidification and warming effects through
physiological buffering of a macroalgae. Ecology and Evolution 10,8465–8475.
Duarte CM,Bruhn A and Krause-Jensen D (2022) A seaweed aquaculture
imperative to meet global su stainability targets. Nature Sustainability 5,185–193.
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.
Duarte CM,Marbà N,Gacia E,Fourqurean JW,Beggins J,Barrón C and
Apostolaki ET (2010) Seagrass community metabolism: Assessing the car-
bon sink capacity of seagrass meadows. Global Biogeochemical Cycles 24,
GB4032.
Duarte CM,Middelburg JJ and Caraco N (2005) Major role of marine
vegetation on the oceanic carbon cycle. Biogeosciences 2,1–8.
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.
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.
Falkenberg LJ,Scanes E,Ducker J and Ross PM (2021) Biotic habitats as
refugia under ocean acidification. Conservation Physiology 9, coab077.
Feely RA,Sabine CL,Lee K,Berelson W,Kleypas J,Fabry VJ and Millero FJ
(2004) Impact of anthropogenic CO
2
on the CaCO
3
system in the oceans.
Science 305, 362–366.
Fernández PA,Hurd CL and Roleda MY (2014) Bicarbonate uptake via an
anion exchange protein is the main mechanism of inorganic carbon acqui-
sition by the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae)
under variable pH. Journal of Phycology 50, 998–1008.
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.
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.
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.
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.
Flores-Moya A and Fernández JA (1998) The role of external carbonic anhy-
drase in the photosynthetic use of inorganic carbon in the deep-water alga
Phyllariopsis purpurascens (Laminariales, Phaeophyta). Planta 207, 115–119.
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.
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.
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.
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.
Gao K and McKinley KR (1994) Use of macroalgae for marine biomass
production and CO
2
remediation: A review. Journal of Applied Phycology
6,45–60.
Giordano M,Beardall J and Raven JA (2005) CO
2
concentrating mechanisms
in algae: Mechanisms, environmental modulation, and evolution. Annual
Review of Plant Biology 56,99–131.
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.
Hanelt D,Wiencke C and Bischof K (2003) Photosynthesis in marine macro-
algae. In Larkum AWD, Douglas SE and Raven JA (eds), Photosynthesis in
Algae. Dordrecht: Springer, pp. 413–435.
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.
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 CO
2
ocean. Global Change Biology 17,
2488–2497.
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.
8 Carla Edworthy et al.

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.
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.
Hofmann LC and Bischof K (2014) Ocean acidification effects on calcifying
macroalgae. Aquatic Biology 22, 261–279.
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.
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.
Hurd CL (2015) Slow‐flow habitats as refugia for coastal calcifiers from ocean
acidification. Journal of Phycology 51, 599–605.
Hurd CL,Harrison PJ,Bischof K and Lobban CS (2014) Seaweed Ecology and
Physiology. Campbridge: Cambridge University Press.
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.
James NC and Whitfield AK (2022) The role of macroalgae as nursery areas for
fish species within coastal seascapes. Coastal Futures 1, e3.
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 pCO
2
stress. Frontiers in
Marine Science 9, 862172.
Johnston AM,Maberly SC and Raven JA (1992) The acquisition of inorganic
carbon by four red macroalgae. Oecologia 92, 317–326.
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 CO
2
.PLoS One 15, e0231971.
Kapsenberg L and Cyronak T (2019) Ocean acidification refugia in variable
environments. Global Change Biology 25, 3201–3214.
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.
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.
Krause-Jensen D and Duarte CM (2016) Substantial role of macroalgae in
marine carbon sequestration. Nature Geoscience 9, 737–742.
Krause-Jensen D,Duarte CM,Hendriks IE,Meire L,Blicher ME,Marbà N
and Sejr MK (2015) Macroalgae contribute to nested mosaics of pH vari-
ability in a subarctic fjord. Biogeosciences 12, 4895–4911.
Kubler JE and Raven JA (1994) Consequences of light limitation for carbon
acquisition in three rhodophytes. Marine Ecology Progress Series 110,
203–209.
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.
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 pinna-
tifida. Journal of Phycology 53, 557–566.
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.
Leliaert F,Anderson RJ,Bolton JJ and Coppejans E (2000) Subtidal under-
storey algal community structure in kelp beds around the cape peninsula
(Western Cape, South Africa). Botanica Marina 43, 359–366.
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. Fron-
tiers in Marine Science 9, 857153.
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.
Lobban CS and Harrison PJ (1994) Seaweed Ecology and Physiology.
Campbridge: Cambridge University Press.
Lüning K (1991) Seaweeds: Their Environment, Biogeography, and Ecophysiol-
ogy. New York: John Wiley & Sons.
Maberly SC (1990) Exogenous sources of inorganic carbon for photosynthesis
by marine macroalgae. Journal of Phycology 26, 439–449.
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.
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.
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.
Menéndez M,Martınez M and ComınFA(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.
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.
Middelboe AL and Hansen PJ (2007) High pH in shallow-water macroalgal
habitats. Marine Ecology Progress Series 338, 107–117.
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.
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.
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.
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.
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 rhodo-
lith Sporolithon sp. Environmental Pollution 266, 115344.
Nizamuddin M (1970) Phytogeography of the Fucales and their seasonal
growth. Botanica Marina 13, 131–139.
Noisette F and Hurd C (2018) Abiotic and biotic interactions in the diffusive
boundary layer of kelp blades create a potential refuge from ocean acidifica-
tion. Functional Ecology 32, 1329–1342.
Pacella SR,Brown CA,Waldbusser GG,Labiosa RG and Hales B (2018)
Seagrass habitat metabolism increases short-term extremes and long-term
offset of CO
2
under future ocean acidification. Proceedings of the National
Academy of Sciences 115, 3870–3875.
Park PK (1969) Oceanic CO
2
system: An evaluation of ten methods of inves-
tigation. Limnology and Oceanography 14, 179–186.
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 CO
2
gradient. Ecology and Evolution 5, 1784–1793.
Pörtner HO (2008) Ecosystem effects of ocean acidification in times of ocean
warming: A physiologist’s view. Marine Ecology Progress Series 373, 203–217.
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.
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.
Cambridge Prisms: Coastal Futures 9

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.
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.
Raven JA (1995) Photosynthetic and non-photosynthetic roles of carbonic
anhydrase in algae and cyanobacteria. Phycologia 34,93–101.
Raven JA (1997) Inorganic carbon acquisition by marine autotrophs. Advances
in Botanical Research 27,85–209.
Raven JA (2003) Inorganic carbon concentrating mechanisms in relation to the
biology of algae. Photosynthesis Research 77, 155–171.
Raven JA (2011) Effects on marine algae of changed seawater chemistry with
increasing atmospheric CO
2
.Biology and Environment –Proceedings of the
Royal Irish Academy 111B,1–17.
Raven JA and Hurd CL (2012) Ecophysiology of photosynthesis in macroalgae.
Photosynthesis Research 113, 105–125.
Robertson BL (1987) Reproductive ecology and canopy structure of Fucus
spiralis L. Botanica Marina 30, 475–482.
Roleda MY,Boyd PW and Hurd CL (2012a) Before ocean acidification:
Calcifier chemistry lessons. Journal of Phycology 48, 840–843.
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.
Roleda MY,Morris JN,McGraw CM and Hurd CL (2012b) Ocean acidifi-
cation and seaweed reproduction: Increased CO
2
ameliorates the negative
effect of lowered pH on meiospore germination in the giant kelp Macro-
cystis pyrifera (Laminariales, Phaeophyceae). Global Change Biology 18,
854–864.
Roleda MY,Wiencke C,Hanelt D and Bischof K (2007) Sensitivity of the early
life stages of macroalgae from the northern hemisphere to ultraviolet radi-
ation. Photochemistry and Photobiology 83, 851–862.
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 CO
2
.Science 305, 367–371.
Saderne V,Fietzek P and Herman PM (2013) Extreme variations of pCO
2
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.
Saderne V and Wahl M (2013) Differential responses of calcifying and non-
calcifying epibionts of a brown macroalga to present-day and future upwell-
ing pCO
2
.PLoS One 8, e70455.
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.
Schiel DR and Foster MS (2015) The Biology and Ecology of Giant Kelp Forests.
Oakland: University of California Press.
Semesi S,Kangwe J and Björk M (2009) Alterations in seawater pH and
CO
2
affect calcification and photosynthesis in the tropical coralline alga,
Hydrolithon sp. (Rhodophyta). Estuarine, Coastal and Shelf Science 84,
337–341.
Shepherd S and Edgar G (2013) Ecology of Australian Temperate Reefs: The
Unique South. Melbourne: CSIRO Publishing.
Short J,Kendrick GA,Falter J and McCulloch MT (2014) Interactions between
filamentous turf algae and coralline algae are modified under ocean acidifi-
cation. Journal of Experimental Marine Biology and Ecology 456,70–77.
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.
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.
Stepien CC,Pfister CA and Wootton JT (2016) Functional traits for carbon
access in macrophytes. PLoS One 11, e0159062.
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.
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 CO
2
flux based on climatological surface ocean pCO
2
, and seasonal biological and
temperature effects. Deep Sea Research Part II: Topical Studies in Oceanog-
raphy 49, 1601–1622.
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 Experi-
mental Marine Biology and Ecology 492,81–98.
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.
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.
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.
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.
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.
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.
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.
Yip ZT,Quek RZB and Huang D (2020) Historical biogeography of the
widespread macroalga Sargassum (Fucales, Phaeophyceae). Journal of Phy-
cology 56, 300–309.
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.
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.
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.
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.
Zou D and Gao K (2010) Acquisition of inorganic carbon by Endarachne
binghamiae (Scytosiphonales, Phaeophyceae). European Journal of Phycology
45, 117–126.
10 Carla Edworthy et al.