Article 5 en Plus

Biogeosciences, 14, 5359–5376, 2017
https://doi.org/10.5194/bg-14-5359-2017
© Author(s) 2017. This work is distributed under
the Creative Commons Attribution 4.0 License.
Species interactions can shift the response of a maerl bed

community to ocean acidification and warming
Erwann Legrand1,2 , Pascal Riera1,2 , Mathieu Lutier1,2 , Jérôme Coudret1,2 , Jacques Grall3 , and Sophie Martin1,2
1 SorbonneUniversity, UPMC, Station Biologique, Place Georges Teissier, 29688 Roscoff CEDEX, France
2 CNRS, Station Biologique, Place Georges Teissier, 29688 Roscoff CEDEX, France
3 UBO, IUEM, Place Nicolas Copernic, 29280 Plouzané, France
Correspondence to: Erwann Legrand ([email protected])
Received: 20 June 2017 – Discussion started: 29 June 2017

Revised: 20 October 2017 – Accepted: 25 October 2017 – Published: 30 November 2017
Abstract. Predicted ocean acidification and warming are growth. However, our results suggest that predicted changes
likely to have major implications for marine organisms, espe- will negatively affect the metabolism of grazers and poten-
cially marine calcifiers. However, little information is avail- tially their ability to control epiphyte abundance. We show
able on the response of marine benthic communities as a here that the effects of pCO2 and temperature on maerl bed
whole to predicted changes. Here, we experimentally exam- communities were weakened when these factors were com-
ined the combined effects of temperature and partial pres- bined. This underlines the importance of examining multi-
sure of carbon dioxide (pCO2 ) increases on the response factorial approaches and community-level processes, which
of maerl bed assemblages, composed of living and dead integrate species interactions, to better understand the impact
thalli of the free-living coralline alga Lithothamnion coral- of global change on marine ecosystems.
lioides, epiphytic fleshy algae, and grazer species. Two 3-
month experiments were performed in the winter and sum-
mer seasons in mesocosms with four different combinations
of pCO2 (ambient and high pCO2 ) and temperature (ambi- 1 Introduction
ent and +3 ◦ C). The response of maerl assemblages was as-
sessed using metabolic measurements at the species and as- A growing body of literature predicts that ocean acidification
semblage scales. This study suggests that seasonal variabil- and warming will be the main anthropogenic drivers affect-
ity represents an important driver influencing the magnitude ing marine species by the end of the century (Kroeker et al.,
and the direction of species and community response to cli- 2013). Due to the increase in atmospheric CO2 , seawater sur-
mate change. Gross primary production and respiration of face temperatures have been predicted to increase by 0.71–
assemblages was enhanced by high pCO2 conditions in the 2.73 ◦ C and pH to decline by 0.07–0.33 units in the surface
summer. This positive effect was attributed to the increase in ocean by the end of the 21st century (Bopp et al., 2013).
epiphyte biomass, which benefited from higher CO2 concen- Species interactions are a key element in ecosystem func-
trations for growth and primary production. Conversely, high tioning and are likely to attenuate or amplify the direct ef-
pCO2 drastically decreased the calcification rates in assem- fects of climate change on individual species (O’Connor et
blages. This response can be attributed to the decline in calci- al., 2011; Hansson et al., 2012; Kroeker et al., 2012). Most
fication rates of living L. corallioides due to acidification and research on benthic ecosystems has focused on the impact
increased dissolution of dead L. corallioides. Future changes of ocean acidification and warming on the response of sin-
in pCO2 and temperature are likely to promote the develop- gle species (Yang et al., 2016) and, despite a growing inter-
ment of non-calcifying algae to the detriment of the engineer est, studies examining the effects of climate change at the
species L. corallioides. The development of fleshy algae may community scale are scarce (Hale et al., 2011; Alsterberg
be modulated by the ability of grazers to regulate epiphyte et al., 2013). Understanding the mechanisms and interac-
tions that occur among marine communities that face the pre-
Published by Copernicus Publications on behalf of the European Geosciences Union.

5360 E. Legrand et al.: Species interactions can shift the response
dicted changes is necessary for a better overview of marine cific interactions (Harley et al., 2012; Auster et al., 2013).
ecosystem response. Climate change is likely to strongly al- In the present study, we therefore performed metabolic mea-
ter interactions between macroalgae (e.g. calcifying and non- surements at the species and at the community scale. At the
calcifying macroalgae; Olabarria et al., 2013; Short et al., species scale, studying species physiology is useful for un-
2014, 2015), interactions between grazers and macroalgae derstanding how organisms cope with changing climatic con-
(Poore et al., 2016; Sampaio et al., 2017), and prey–predator ditions and for analysing the community metabolic response.
dynamics (Asnaghi et al., 2013; Jellison et al., 2016), induc- Community-scale measurements provide information on the
ing drastic consequences on the structure and functioning of potential shifts in species interactions induced by climate
marine ecosystems (Widdicombe and Spicer, 2008; Hale et change. In particular, we tested the hypothesis that climate
al., 2011). change will increase epiphytic fleshy algal growth, exac-
Maerl beds feature high structural and functional diver- erbating the deleterious consequences of predicted changes
sity arising primarily from the numerous species interactions on L. corallioides metabolism. We also investigated whether
that occur in this environment – in particular, interactions the predicted changes can modify interactions between graz-
between fleshy and calcareous macroalgae and grazers and ers and macroalgae and their ability to regulate epiphytic
macroalgae (Hily et al., 1992; Guillou et al., 2002; Grall et biomass.
al., 2006). The accumulation of living and dead thalli of free-
living coralline algae (Corallinaceae, Rhodophyta) creates a
complex three-dimensional structure that provides habitat for 2 Materials and methods
many faunal and floral species (Foster et al., 2007; Amado-
2.1 Species collection and assemblages
Filho et al., 2010; Peña et al., 2014), some of which have
high commercial value (Grall and Hall-Spencer, 2003). In Organisms were collected from a maerl bed in the Bay of
some locations, dead maerl can reach high proportions com- Brest, France (48◦ 180 N, 4◦ 230 W), using a naturalist’s dredge
pared with living maerl (Hily et al., 1992), thereby contribut- (width: 1 m; height: 0.2 m; net: 1.5 m long) deployed from
ing substantially to the local carbonate dynamics (Martin et the research vessel Albert Lucas. In the Bay of Brest, maerl
al., 2007). beds are located at depths of between 0.7 and 6.8 m, accord-
The main species inhabiting maerl beds may respond dif- ing to the tide (Dutertre et al., 2015). We deliberately se-
ferently to ocean acidification and warming. Coralline algae lected thalli of the maerl species L. corallioides Crouan and
are known to be among the most vulnerable species facing Crouan, 1867 that were devoid of any apparent epiphytes;
ocean acidification (McCoy and Kamenos, 2015; Martin and nonetheless, they were not cleaned so as to retain any epi-
Hall-Spencer, 2016) due to their highly soluble Mg-calcite phyte spores that may have been present on their surface.
skeleton (Morse et al., 2006). The deleterious consequences Medium-sized individuals of the three main species of graz-
of ocean acidification have also been demonstrated for other ers living in maerl beds were also sampled: two gastropod
calcareous marine taxa, such as mollusks (Gazeau et al., species (sea snails), Gibbula magus Linnaeus, 1758 and Ju-
2013; Parker et al., 2013) and echinoderms (Dupont et al., jubinus exasperatus Pennant, 1777, and an urchin species,
2010), with reductions in survival, growth, development, and Psammechinus miliaris Müller, 1771 (Grall et al., 2006).
abundance (Kroeker et al., 2013). Conversely, some species Samples were collected on 24 January 2015 (winter condi-
can benefit from the increase in CO2 concentration and tem- tions) and 15 September 2015 (summer conditions). In each
perature. Positive responses, such as increases in primary season, 1 kg of living thalli of L. corallioides, 500 g of dead
production and growth, have been found mostly among non- thalli of L. corallioides, 40 individuals of G. magus (shell
calcifying organisms, such as fleshy algae and seagrasses length range 17–29 mm), 40 individuals of P. miliaris (test
(Koch et al., 2013; Pajusalu et al., 2013). diameter range 11–23 mm), and 80 individuals of J. exasper-
Here, we experimentally investigated the impact of ocean atus (shell height range 5–11 mm) were randomly selected
acidification and warming on the metabolism and the in- and transported in seawater tanks to the Roscoff Marine Sta-
teractions of the main maerl-forming species in Brittany tion. To mitigate the stress experienced by the species during
Lithothamnion coralloides and the epiphytic fleshy macroal- sampling and transport, they were kept in open-flow aquaria
gae and main grazer (gastropods and sea urchins) associated at ambient pH and in situ temperature conditions at the time
with it. Because the response of species and communities of collection for at least 1 week before starting the experi-
to climate change is likely to vary depending on seasonal ments. No mortality was recorded during this period.
changes in environmental factors, such as light intensity, pho-
toperiod, and temperature (Godbold and Solan, 2013; Mar- 2.2 Experimental design
tin et al., 2013; Baggini et al., 2014), it was tested in both
winter and summer conditions. The response of marine com- Two 3-month-long experiments were conducted for both
munities to climate change is likely to be influenced by the winter (March to June 2015) and summer (September to De-
direct effects of environmental stressors on individual organ- cember 2015) conditions. For each season, 20 artificial as-
isms and by the indirect effects induced by shifts in interspe- semblages were created and randomly assigned to twenty
Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

E. Legrand et al.: Species interactions can shift the response 5361
Table 1. Summary of the four experimental treatments. Two pCO2 (ambient and high pCO2 ) and temperature (ambient and high tem-
perature) conditions were tested. High pCO2 (H-pCO2 ) corresponded to a pH decrease of −0.33 units compared to ambient conditions
(A-pCO2 ). High temperature (T + 3 ◦ C) corresponded to a temperature increase of 3 ◦ C compared to ambient conditions (T ).
pCO2 Temperature
1 (control) Ambient (A-pCO2 ) Ambient (T ) A-pCO2 ; T
2 High (H-pCO2 ) Ambient (T ) H-pCO2 ; T
3 Ambient (A-pCO2 ) High (T + 3 ◦ C) A-pCO2 ; T + 3 ◦ C
4 High (H-pCO2 ) High (T + 3 ◦ C) H-pCO2 ; T + 3 ◦ C
15 L aquaria. Each assemblage was composed of 45 g of liv- (Dickson et al., 2007). The pH values of the offline feed-
ing L. corallioides thalli, 20 g dead L. corallioides thalli, two back system were adjusted from measurements of pHT car-
G. magus individuals, two P. miliaris individuals, and four ried out every 2 days in each aquarium. Total alkalinity (AT )
J. exasperatus individuals, according to the proportions ob- was also monitored during the experiment in each aquar-
served on maerl beds. ium at different times of the day (Table 2). For AT analy-
Algae and grazers were acclimated to laboratory condi- ses, seawater samples (60 mL) were filtered through 0.7 µm
tions for 7 days. Then, the pH was gradually decreased by Whatman GF/F filters and immediately poisoned with a mer-
0.05 units per day over 7 days and temperature increased by curic chloride solution to prevent further biological activity
0.5 ◦ C per day. The pH was controlled by modifying pCO2 (Dickson et al., 2007). AT was determined using open-cell
through CO2 bubbling. At each season, two pCO2 conditions titration on an automatic titrator (TitroLine alpha, Schott SI
were tested, each with two temperature conditions to exam- Analytics, Mainz, Germany) according to the method devel-
ine the interaction between pCO2 and temperature. These oped by Dickson et al. (2007). AT was calculated using a
four conditions are presented in Table 1. Gran function applied to pH values ranging from 3.5 to 3.0
Ambient pCO2 conditions (A-pCO2 ) were determined ac- (Dickson et al., 2007) and corrected using standard refer-
cording to in situ winter (7.98) and summer (8.06) mean pHT ence material provided by the Andrew G. Dickson labora-
(pH on the total scale) monitored above maerl beds in the tory (CRM Batch 111, accuracy of ±6 µmol kg−1 ). Salin-
Bay of Brest (data from Martin, unpublished). High pCO2 ity was measured every 2 weeks with a conductivity probe
(H-pCO2 ) corresponded to the “business-as-usual” scenario (CDC401, Hach Lange, IntelliCAL, accuracy of 0.1) and re-
predicted for the end of the century, with a pH decrease of mained constant during experiments (35.2 ± 0.2). From AT
−0.33 units (RCP8.5; Bopp et al., 2013). Ambient tempera- and pHT measurements, dissolved inorganic carbon (DIC),
ture (T ) corresponded to in situ winter (10.0 ◦ C) and summer saturation state of seawater with respect to aragonite (Ar ),
(17.1 ◦ C) conditions in the Bay of Brest recorded by SOM- and saturation state of seawater with respect to calcite (Ca )
LIT (from 2003 to 2014), and high temperature (T + 3 ◦ C) were calculated with the CO2SYS software (Table 2). Mean
was determined according to the business-as-usual scenario temperature and parameters of the carbonate chemistry are
predicted for 2100 (Bopp et al., 2013). given in Table 2.
The pH and the temperature were controlled in four 100 L Irradiance was set to the mean in situ daily irradiance
tanks, continuously supplied with filtered (5 µm) natural sea- at 5 m depth in the Bay of Brest according to Martin et
water, with a high water flow rate of 150 L h−1 per tank. They al. (2006a): 30–40 µmol photons m−2 s−1 in winter and 90–
were maintained by an offline feedback system (IKS Aquas- 100 µmol photons m−2 s−1 in summer. The light was pro-
tar, Karlsbad, Germany) that activated or stopped heaters vided by two or four 80 W fluorescent tubes (JBL Solar Ultra
and solenoid valves, controlling temperature and CO2 (Air Marin Day, JBL Aquaria, Nelson, New Zealand) above the
Liquide, France) bubbling in the tanks, respectively. Each aquaria under a 10/14 or 14/10 h light/dark photoperiod for
100 L tank provided seawater to five 15 L aquaria for each winter or summer conditions, respectively.
of the four conditions using pumps. The water flow rate
was 15 L h−1 in each aquarium. Temperature was maintained 2.3 Metabolic measurements
constant in aquaria with water baths. Seawater pH (pHT , ex-
pressed on the total hydrogen ion concentration scale; Dick- After 3 months in experimental conditions, metabolic mea-
son et al., 2007) and temperature were monitored every 2 surements were performed at the species and assemblage
days in the 20 aquaria, at different times of the day (Table 2). level using incubations in acrylic respirometry chambers
Seawater pHT and temperature measurements were carried (Engineering and Design Plastics Ltd, Cambridge, UK).
out using a pH probe associated with a temperature sensor For species-scale measurements, each species was incubated
(PHC101, Hach Lange, IntelliCAL). The pH probe was cal- separately. Community-scale measurements were performed
ibrated using Tris / HCl and 2-aminopyridine / HCl buffers on assemblages, incubating all individuals from all species
present in each aquarium. The chamber volume was adapted
www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

Table 2. Physicochemical parameters (mean ± SE) of seawater in each experimental condition (A-pCO2 is ambient pCO2 ; H-pCO2 is high
pCO2 ; T is ambient temperature; T + 3 ◦ C is high temperature) in the winter and the summer. pHT and temperature were monitored every
2 days in each aquarium (n = 35). Total alkalinity values (AT ) are means (±SE) of 28 samples measured in each aquarium. The CO2 partial
pressure (pCO2 ), dissolved inorganic carbon (DIC), and saturation states of seawater with respect to aragonite (Ar ) and calcite (Ca ) were
calculated from pHT , temperature, salinity, and AT using CO2SYS.
Experimental pCO2 r pHT Temperature AT DIC Ar Ca

condition (µatm) (◦ C) (µmol kg−1 ) (µmol kg−1 )
A-pCO2 ; T 490 (±5) 7.97 (±0.04) 10.1 (±0.3) 2348 (±6) 2189 (±6) 1.84 (±0.02) 2.89 (±0.02)
H-pCO2 ; T 1183 (±10) 7.63 (±0.03) 10.1 (±0.3) 2342 (±7) 2306 (±7) 0.89 (±0.01) 1.40 (±0.01)
Winter
A-pCO2 ; T + 3 ◦ C 513 (±5) 7.97 (±0.03) 13.7 (±0.1) 2341 (±5) 2166 (±5) 2.01 (±0.01) 3.14 (±0.02)
H-pCO2 ; T + 3 ◦ C 1087 (±18) 7.64 (±0.03) 13.6 (±0.2) 2329 (±2) 2266 (±4) 1.09 (±0.01) 1.70 (±0.02)
A-pCO2 ; T 426 (±4) 8.03 (±0.04) 17.1 (±0.2) 2359 (±3) 2127 (±3) 2.60 (±0.02) 4.03 (±0.03)
H-pCO2 ; T 948 (±9) 7.72 (±0.03) 17.1 (±0.2) 2382 (±4) 2279 (±4) 1.45 (±0.01) 2.24 (±0.02)
Summer
A-pCO2 ; T + 3 ◦ C 432 (±4) 8.01 (±0.04) 20.0 (±0.5) 2364 (±3) 2109 (±3) 2.88 (±0.02) 4.43 (±0.03)
H-pCO2 ; T + 3 ◦ C 879 (±7) 7.74 (±0.02) 20.2 (±0.3) 2369 (±2) 2238 (±2) 1.71 (±0.01) 2.64 (±0.02)
to species size. It was 80 mL for J. exasperatus and epiphytes, ter. Net primary production (NPP, µmol O2 g DW−1 h−1 ) or
185 mL for P. miliaris, G. magus and living and dead L. respiration (R, µmol O2 g DW−1 h−1 ) rates were calculated
corallioides, and 600 mL for the assemblages. After assem- following Eq. (1):
blage incubations, epiphytic algae that spontaneously grew
on L. corallioides during the experiments were carefully re- 1O2 × V
NPP or R = , (1)
moved and incubated separately. Metabolic measurements 1t × DW
(net photosynthetic and respiration rates) for the main epi-
where 1O2 is the difference between the initial and final
phytic algae Rhodymenia ardissonei and Solieria chordalis
oxygen concentrations (µmol O2 L−1 ), V the volume of the
were only examined in the summer, when their biomass was
chamber (L), 1t the incubation time (h), and DW the dry
sufficient for measurements. Species were placed on a plas-
weight of the species incubated (g). The dry weight was ob-
tic grid above a stir bar in the chambers to ensure the seawa-
tained after 48 h at 60 ◦ C. For gastropods, the body was sep-
ter was well mixed. For G. magus and P. miliaris, net calci-
arated from the shell to consider the dry weight of the body
fication, respiration, and excretion (ammonia release) rates
only.
were measured. For J. exasperatus, only respiration rates
For algae and the assemblages, gross primary production
were measured due to its limited size and metabolic rates.
(GPP) was calculated following Eq. (2):
For grazers, physiological rates were measured under ambi-
ent irradiance. For each grazer species, individuals present in GPP = NPP − R. (2)
each aquarium were incubated together. For living and dead
L. corallioides and assemblages, net photosynthetic and light Control incubations containing only seawater were carried
calcification rates were measured under ambient irradiance, out to correct for oxygen fluxes due to any additional biolog-
and respiration and dark calcification rates were measured in ical activity in seawater. Oxygen fluxes calculated in control
the dark. For light incubations, chambers were placed inside chambers were subtracted from oxygen fluxes of chambers
aquaria to control temperature. For dark incubations, cham- containing species.
bers were placed in a plastic crate filled with aquaria seawater Seawater samples were taken in the aquaria at the be-
in an open circuit to keep the temperature constant. Incuba- ginning of the incubation and in the chambers at the end
tion duration was adjusted to keep oxygen saturation above of the incubations (except for fleshy algae and J. exasper-
80 %. Incubations lasted approximately from 1 h for G. ma- atus) to measure ammonium (NH+ 4 ) concentration and to-
gus to 2.5 h for dead maerl. For assemblages, the metabolism tal alkalinity (AT ). To do so, 45 mL seawater samples for
was measured from the incubations of all species together. NH+ 4 analyses were fixed with reagent solutions and stored
Oxygen concentrations were measured at the beginning in the dark. NH+ 4 concentrations were determined accord-
and at the end of each incubation, using an optical fibre sys- ing to the Solorzano method (Solorzano, 1969). Absorbance
tem (FIBOX 3, PreSens, Regensburg, Germany). Reactive was measured by spectrophotometry at a wavelength of
spots were calibrated with 0 and 100 % buffer solutions. The 630 nm (spectrophotometer UV-1201V, Shimadzu Corp, Ky-
0 % buffer solution was prepared by dissolving 1 g of sodium oto, Japan). For grazers, ammonia excretion rates (E, µmol
sulfite (Na2 SO3 ) in 100 mL of seawater. The 100 % buffer so- NH+ 4 g DW
−1 h−1 ) were calculated following Eq. (3):
lution was prepared by bubbling air into 100 mL of seawater
using an air pump for 20 min to obtain air-saturated seawa- 1NH4 + × V
E= , (3)
1t × DW

where 1NH+ 4 is the difference between the initial and final respected, two-way ANOVA were performed, using temper-
ammonium concentrations (µmol NH+ 4 g DW
−1 h−1 ). ature and pCO2 as fixed orthogonal factors. When assump-
For AT analyses, 60 mL seawater samples were filtered tions were not respected, two-way nonparametric Scheirer–
through 0.7 µm Whatman GF/F filters and were immediately Ray–Hare tests were run. Statistical analyses were conducted
poisoned with a mercuric chloride solution. Total alkalinity separately for winter and summer experiments in order to
was determined according to the method described above. keep a balanced design. When two-way AVOVAs showed
Net calcification rates at light and in the dark (Gl and Gd , re- significant results, post hoc tests (Tukey honest significant
spectively; in µmol CaCO3 g DW−1 h−1 ) were calculated ac- difference, HSD) were performed to compare the four treat-
cording to the alkalinity anomaly technique (Smith and Key, ments.
1975) and corrected for NH+ 4 fluxes (Gazeau et al., 2015). The effects of pCO2 and temperature on the physiologi-
This correction was applied to calcareous species and assem- cal rates of the epiphytic algae R. ardissonei and S. chordalis
blage incubations following Eq. (4): were only tested in the summer. Statistical analyses were car-
ried out using the statistical package R, version 3.2.2.
(−1AT + 1NH4 + ) × V
Gl or Gd = , (4)
2 × 1t × DW
where Gl is the net calcification in the light, Gd is the net 3 Results
calcification in the dark, and 1AT is the difference between
3.1 Metabolic responses of grazers to acidification and
the initial and final AT (µeq L−1 ).
warming
After the 3-month experiments, epiphytic algae that spon-
taneously grew on L. corallioides during experiments were In the urchin P. miliaris and the gastropod G. magus, the
picked off and dried at 60 ◦ C for 48 h to determine their dry metabolism was significantly higher in the summer than in
weight. the winter, except for P. miliaris R, for which no difference
2.4 Chlorophyll a analysis was detected (Table 3). In the gastropod J. exasperatus, R did
not vary with the season. High temperature (+3 ◦ C) reduced
At the end of the experiments, thalli of living and dead L. P. miliaris R in the summer, while pCO2 had no significant
corallioides were collected in each aquarium and immedi- effect on P. miliaris R (Fig. 1a; Table 4). P. miliaris Gl was
ately frozen at −20 ◦ C pending analyses. In dead maerl, significantly affected by the interaction between temperature
chlorophyll a content was measured in order to check for the and pCO2 in the summer (Figs. 1b, S1b), which negated the
presence of associated microflora and potential subsequent positive effect of increased temperature or pCO2 alone. P.
metabolism. Then samples were freeze-dried and crushed miliaris E was higher under control conditions in the sum-
into a powder using a mortar, in the dark. An aliquot of mer and significantly lower under increased temperature (Ta-
0.15 g of powder was precisely weighed and suspended in ble 4; Fig. 1c). G. magus R was lower under high pCO2 in
10 mL of 90 % acetone and stored in the dark at 4 ◦ C for 12 h. the winter only (Table 4; Fig. 1d). Neither temperature nor
Samples were then centrifuged at 4000 rpm. The supernatant pCO2 increases significantly affected G. magus Gl and E
was collected and absorbance was measured at 630 (A630 ), (Table 4; Fig. 1e–f). In J. exasperatus, R increased under el-
647 (A647 ), 664 (A664 ), and 691 (A691 ) nm. Chlorophyll a evated temperature but in winter conditions only (Table 4;
(Chl a) concentrations (µg g DW−1 ) were calculated from Fig. 1g). J. exasperatus R was negatively influenced by the
Ritchie (2008) following Eq. (5): pCO2 increase in the winter but positively in the summer.
Chl a = 3.2 Metabolic responses of living L. corallioides to

(−0.3319 A630 − 1.7485A647 + 11.9442A664 − 1.4306A691 ) × V
, (5) acidification and warming
mp
where V is the volume of acetone (mL) and mp the mass of The metabolism of living L. corallioides was higher in the
powder (g). summer than in the winter, except for NPP (Table 3). Liv-
ing maerl NPP did not differ among temperature and pCO2
2.5 Data analysis conditions regardless of the season, while GPP was lower
under high temperature in the winter (Table 5; Fig. 2a, b).
Comparisons in species and assemblage physiological rates R was significantly reduced by the high temperature condi-
between the winter and summer seasons was performed us- tion in the winter, whereas an increase in R was observed in
ing t tests, after checking the normality and homogeneity of the summer (Table 5; Fig. 2c). No effect of season was ob-
variances. The influence of temperature and pCO2 was tested served on chlorophyll a content (Tables 3, 6). Chlorophyll a
on metabolic rates of grazers (P. miliaris, G. magus, and J. content was reduced by the high temperature condition in
exasperatus), living and dead maerl, epiphytic biomass and the winter only (Table 5). The Gl of living maerl was not
assemblages. Normality of the data and variance homogene- significantly influenced by increased temperature and pCO2 ,
ity were checked for all variables. When assumptions were regardless of the season (Table 5; Fig. 2d). Conversely, in-

Figure 1. Respiration, net calcification, and excretion rates (mean ± SE, n = 5) of the grazers P. miliaris (a–c) and G. magus (d–f) and
respiration of J. exasperatus (g) in the different pCO2 (A-pCO2 is ambient pCO2 ; H-pCO2 is high-pCO2 ) and temperature (T is ambient
temperature; T + 3 ◦ C is high temperature) conditions. The species were maintained in assemblages for 3 months in winter (dark gray) and
summer conditions (light gray). Different letters show significant differences (Tukey HSD test) between the four treatments in the winter
(letters a and b) and summer (letters x and y). ns is not significant. Tukey tests were performed when a significant effect of temperature or
pCO2 was detected using two-way ANOVAs.
creased temperature enhanced Gd in the winter, but no effect NPP and GPP in either season. However, a decrease in R
was detected in the summer (Fig. 2e). A significant decline in was observed under high pCO2 in the summer. Chlorophyll
Gd occurred under high pCO2 regardless of the season. Net a content did not differ between seasons (Tables 3, 6) but was
dissolution, because Gd was negative, was recorded in the significantly affected by the temperature and pCO2 interac-
winter under high pCO2 conditions. This negative effect of tion (Table 5; Figs. S1a, 1f). Dead maerl Gl significantly in-
increased pCO2 was alleviated under elevated temperature. creased under high temperature (Fig. 2i). Conversely, a neg-
ative impact of high pCO2 was on Gl in the winter and
3.3 Metabolic responses of dead L. corallioides to summer. In the dark, net dissolution was observed on dead
acidification and warming maerl regardless of the temperature and pCO2 conditions
(Fig. 2j). No temperature effect was observed on dark dis-
In dead L. corallioides, NPP, GPP, R, and Gl were signifi- solution. However, dark dissolution rates were significantly
cantly higher in the summer, while no effect of season was higher under high pCO2 treatments, regardless of the season.
observed on Gd (Table 3). The high temperature condition
(+3 ◦ C) did not affect dead maerl NPP, GPP, or R (Table 5;
Fig. 2f–h). The pCO2 increase did not affect dead maerl

Figure 2. Net and gross primary production, respiration, and light and dark calcification rates (mean ± SE, n = 5) of living (a–e) and dead
thalli (f–j) of L. corallioides in the different pCO2 (A-pCO2 is ambient pCO2 ; H-pCO2 is high-pCO2 ) and temperature (T is ambient
temperature; T + 3 ◦ C is high temperature) treatments after 3 months in winter (dark gray) and summer conditions (light gray). Letters
indicate significant differences between the four treatments in winter (a, b, c) and summer (x, y, z) conditions (Tukey HSD test). ns is not
significant. Tukey tests were performed when a significant effect of temperature or pCO2 was detected using two-way ANOVAs.

Figure 3. Summer net and gross primary production and respiration rates (mean ± SE, n = 5) of the two main epiphytic fleshy algae Rhody-
menia ardissonei (a–c) and Solieria chordalis (d–f), in the different pCO2 (A-pCO2 is ambient pCO2 ; H-pCO2 is high-pCO2 ) and temper-
ature (T is ambient temperature; T +3 ◦ C is high temperature) treatments. Letters indicate significant differences between the four treatments
in summer (x, y) conditions (Tukey HSD test). Tukey tests were performed when a significant effect of temperature or pCO2 was detected.
3.4 Growth and metabolic responses of epiphytic algae was enhanced by the high temperature and pCO2 conditions
to acidification and warming and their combination resulted in a greater R (Fig. 3f).
The mean biomass of epiphytic fleshy algae at the end
Mean GPP and R for the two epiphytic algae R. ardissonei of the experiment was significantly higher in the summer
and S. chordalis measured in the summer are presented in than in the winter (+81 %, t test, p = 0.045; Fig. 4). Epi-
Fig. 3. R. ardissonei NPP and GPP were not affected by high phyte biomass was not affected by increased temperature
temperature or pCO2 conditions, and R was reduced under or pCO2 in the winter (two-way ANOVA, p = 0.95 and
high pCO2 (Table 7; Fig. 3a–c). In S. chordalis, NPP and 0.67 respectively). In the summer, increased temperature re-
GPP were significantly affected by the interaction between duced epiphyte biomass under ambient pCO2 and stimulated
temperature and pCO2 (Table 7; Figs. 3d, e; S1c, S1d). R

Table 4. Results the analysis of variance testing the effects of
Table 3. Results of mean comparison tests between seasons for the net and gross primary production, respiration, chlorophyll a content, light and dark calcification, and excretion of
temperature (T ) and pCO2 on respiration, net calcification, and
excretion rates in the urchin Psammechinus miliaris and the two
0.001
< 0.001
p
gastropods Gibbula magus and Jujubinus exasperatus for winter
and summer experiments (n = 5). Statistical analyses were per-
Excretion
formed using two-way crossed ANOVAs and Scheirer–Ray–Hare
E
tests when test assumptions were not respected (in italic). Signifi-
3.5
14.1
t
cant p values are shown in bold (α = 0.05). Degrees of freedom = 1.
38
29
df
Respiration Net calcification Excretion
R G E
< 0.001
0.804
0.003
p
Dark calcification
F p F p F p
Psammechinus miliaris
Winter
Gd
T 1.8 0.184 0.3 0.588 0.0 0.890

6.6
0.3
3.3
t
pCO2 0.0 0.865 1.0 0.343 1.2 0.286

pCO2 x T 0.2 0.672 0.2 0.640 1.6 0.222
38
28
26
df
Summer
T 20.8 < 0.001& 4.8 0.045 7.6 0.014&
0.155
< 0.001
< 0.001
< 0.001
< 0.001
p
Light calcification
pCO2 3.9 0.066 0.1 0.823 2.7 0.119

pCO2 × T 1.4 0.252 6.6 0.022 3.1 0.098
Winter
Gl
T 1.1 0.303 0.0 0.895 0.4 0.550

1.5
5.3
8.3
4.2
9.0
t
Gibbula magus
pCO2 4.8 0.043& 0.1 0.787 0.6 0.435
pCO2 × T 0.0 0.876 3.9 0.065 1.3 0.281
24
19
25
38
38
df
Summer
T 0.0 0.932 0.8 0.381 2.4 0.145
0.662
0.352
p
pCO2 0.2 0.679 0.6 0.449 1.8 0.199

Chlorophyll a
pCO2 × T 0.1 0.717 0.4 0.546 0.1 0.749

0.4
0.9
Winter
t
Jujubinus exasperatus
T 8.6 0.010%
pCO2 5.6 0.031&
38
37
df
pCO2 × T 0.8 0.391

the different species and the assemblages. Statistical analyses were performed using t tests.
Summer
< 0.001
< 0.001
0.464
< 0.001
< 0.001
< 0.001
p
T 0.1 0.750
pCO2 8.9 0.009%
Respiration
pCO2 × T 0.8 0.832

−11.6
−20.6
0.7
−12.7
−9.8
−13.1
R
t
24
27
38
38
22
37
df
epiphyte biomass under elevated pCO2 (two-way ANOVA,

p = 0.013; Fig. S1e).
< 0.001
< 0.001
< 0.001
p
Gross production
GPP
3.5 Metabolic responses of assemblages to acidification

5.7
8.4
6.1
t
and warming
38
24
31
df
Assemblage metabolism was significantly higher in the sum-

0.164
< 0.001
< 0.001
p
mer than in the winter regardless of the metabolic parameter

Net production
tested (Table 3). No temperature effect was observed on NPP,

GPP, and R in either season (Table 8; Fig. 5a–c). The high
NPP
1.4
7.5
−4.5
t
pCO2 condition enhanced NPP in both seasons. High pCO2

increased GPP in the summer only. Similarly, R significantly
38
26
31
increased under high pCO2 in summer conditions. Gl in-

df
creased under high temperature in the summer only (Fig. 5d).

Living L. corallioides
Conversely, high pCO2 reduced Gl regardless of the season.

Dead L. corallioides
In the dark, net dissolution was observed in the winter, but

J. exasperatus
net precipitation occurred in summer conditions at high tem-

Assemblage
P. miliaris
perature (Fig. 5e). In the winter, high pCO2 increased net

G. magus
dissolutions rates, while in the summer Gd increased under

elevated temperature.

Table 5. Results the analysis of variance for the effects of temperature (T ) and pCO2 on net and gross primary production, respiration,
chlorophyll a content, and light and dark calcification rates of living and dead Lithothamnion corallioides (n = 5). Statistical analyses were
performed using two-way crossed ANOVAs and Scheirer–Ray–Hare tests when test assumptions were not respected (in italic). Significant p
values are shown in bold (α = 0.05). Degrees of freedom = 1.
Net production Gross production Respiration Chlorophyll a Light calcification Dark calcification
NPP GPP R Gl Gd
F p F p F p F p F p F p
LIVING L. corallioides
Winter
T 4.4 0.052 8.0 0.012& 13.1 0.002& 5.9 0.027& 3.6 0.077 10.0 0.006%
pCO2 0.6 0.438 0.6 0.444 0.1 0.733 1.6 0.227 3.2 0.091 153.3 < 0.001&
pCO2 × T 3.2 0.092 1.0 0.329 3.8 0.070 0.0 0.888 0.8 0.393 3.6 0.075
Summer
T 2.0 0.182 1.9 0.174 20.9 < 0.001% 1.5 0.226 3.3 0.070 0.0 0.981
pCO2 0.8 0.399 0.4 0.545 0.2 0.701 0.7 0.406 3.6 0.059 50.0 < 0.001&
pCO2 × T 1.5 0.240 0.7 0.406 0.4 0.515 0.6 0.450 0.2 0.650 0.0 0.956
Winter
DEAD L. corallioides
T 0.0 0.909 0.0 0.970 0.0 0.991 0.0 0.991 20.2 < 0.001% 0.1 0.717
pCO2 0.1 0.713 0.1 0.764 0.1 0.731 0.1 0.813 61.1 < 0.001& 99.6 < 0.001&
pCO2 × T 0.3 0.592 0.0 0.933 0.9 0.350 6.3 0.024 0.0 0.881 0.0 0.846
Summer
T 3.7 0.073 3.7 0.074 2.0 0.173 0.7 0.414 0.2 0.650 0.2 0.639
pCO2 1.1 0.314 1.8 0.197 4.8 0.043& 9.9 0.006 9.6 0.002 & 17.8 < 0.001&
pCO2 × T 0.9 0.360 0.8 0.390 0.2 0.669 30.3 < 0.001 1.9 0.174 0.6 0.441
Table 6. Chlorophyll a content (mean ± SE) of living and dead L. corallioides in the different pCO2 pCO2 (A-pCO2 is ambient pCO2 ;
H-pCO2 is high-pCO2 ) and temperature (T is ambient temperature; T + 3 ◦ C is high temperature) treatments, after being maintained for 3
months in winter and summer conditions, n = 5.
Chlorophyll a
µg chlorophyll g DW−1
A-pCO2 /T H-pCO2 /T A-pCO2 /T + 3 ◦ C H-pCO2 /T + 3 ◦ C
Living L. corallioides
Winter 59.84 (±1.97) 61.66 (±3.83) 52.93 (±3.44) 56.85 (±2.52)
Summer 55.03 (±2.95) 57.63 (±3.99) 60.35 (±0.70) 62.19 (±3.75)
Dead L. corallioides
Winter 47.09 (±2.72) 39.39 (±5.65) 39.15 (±2.20) 46.36 (±2.19)
Summer 52.21 (±1.92) 36.30 (±1.83) 43.63 (±0.90) 47.96 (±2.54)
4 Discussion portant driver influencing the magnitude and the direction of

species and community response to climate change.
The response of marine communities to increased tempera- Assemblage exhibited a strong seasonal pattern for all
ture and pCO2 conditions is likely to be a complex function metabolic parameters, which is consistent with the higher
of direct effects of climate variables on species physiology metabolism in the summer for most of the species incubated
and shifts in species interactions (Lord et al., 2017). Results at the specific scale. This higher metabolism in the summer
show that predicted changes may alter interactions among has already been shown in urchins (Brockington and Peck,
calcifying and fleshy macroalgae via overgrowth of epiphytic 2001), gastropods (Davies, 1966; Innes and Houlihan, 1985;
algae and an increase in competition for light and nutri- Martin et al., 2006b), and living maerl (Potin et al., 1990;
ents with underlying maerl. Interactions between grazers and Martin et al., 2006a) and is strongly related to changes in
macroalgae were also affected because the grazer physiology numerous environmental and biological variables, such as
was adversely affected by acidification and warming with light intensity and photoperiod, temperature, and nutrient or
potential consequences on epiphyte biomass regulation. Our food availability (Godbold and Solan, 2013; Thomsen et al.,
results underscore the importance of examining community- 2013).
level processes to integrate species interactions in the study Assemblage GPP and R were not affected by the high tem-
of the impact of global change on marine ecosystems. This perature and pCO2 conditions in the winter. Conversely, in
study also shows that seasonal variability represent an im- the summer, GPP and R increased under high pCO2 con-

Table 7. Summary of the effects of pCO2 and temperature (T ) and their combined effect on gross production and respiration of the two
epiphytic algae R. ardissonei and S. chordalis in the summer (n = 5). Statistical analyses were performed using a two-way crossed Scheirer–
Ray–Hare test. Significant p values are presented in bold (α = 0.05). Degrees of freedom = 1.
Net production Gross production Respiration

NPP GPP R
F p value F p value F p value
Rhodymenia T 0.8 0.369 0.2 0.683 1.3 0.253
ardissonei
pCO2 0.0 0.960 0.8 0.381 8.6 0.003&
pCO2 × T 1.0 0.311 1.0 0.312 0.7 0.418
T 0.1 0.762 1.1 0.317 5.5 0.019%

chordalis
Solieria
pCO2 3.0 0.082 5.5 0.032 3.9 0.049%

pCO2 × T 5.8 0.016 7.6 0.014 0.0 0.880
Table 8. Results the analysis of variance testing the effects of temperature (T ) and pCO2 on net and gross primary production, respiration,
and light and dark calcification rates, measured on assemblages (n = 5). Significant p values are presented in bold (α = 0.05). Degrees of
freedom = 1.
Net production Gross production Respiration Light calcification Dark calcification

NPP GPP R Gl Gd
F p F p F p F p F p
Winter
T 0.2 0.704 0.7 0.428 1.7 0.207 0.2 0.707 0.7 0.429
pCO2 8.6 0.011% 0.1 0.717 1.6 0.228 27.3 < 0.001& 65.4 < 0.001&
Assemblages
pCO2 × T 0.9 0.350 1.1 0.727 1.1 0.309 0.8 0.373 0.2 0.656
Summer
T 2.1 0.166 1.6 0.225 0.5 0.513 40.2 < 0.001% 6.8 0.020%
pCO2 8.2 0.011% 14.2 0.002% 11.1 0.004% 16.6 < 0.001& 3.0 0.102
pCO2 × T 1.9 0.192 1.3 0.275 0.3 0.595 0.8 0.384 3.6 0.077
ditions. The response of assemblage GPP and R appeared et al. (2016). R. ardissonei GPP was not affected by increased
closely related to changes in epiphyte biomass and produc- temperature and pCO2 , but its R was significantly lower un-
tivity. For instance, the biomass of maerl epiphytic algae der high pCO2 . Within the same genus, Cook et al. (1986)
was significantly higher in summer than in winter, which showed that Rhodymenia palmata can potentially use HCO− 3
is consistent with other findings in the Bay of Brest (Guil- as source of inorganic carbon for photosynthesis. The same
lou et al., 2002) and other Atlantic maerl beds (Peña and process may occur in R. ardissonei, suggesting that this alga
Barbara, 2010). The high biomass of epiphytic algae in the is not carbon-limited at current oceanic pCO2 levels. In con-
summer led to high contribution to oxygen fluxes. Under trast to R. ardissonei, increased pCO2 stimulated S. chordalis
high pCO2 conditions, the higher availability of CO2 as sub- GPP under ambient conditions of temperature. In their study,
strate for photosynthesis may stimulate epiphyte productiv- Short et al. (2014) indicate that the overgrowth of filamen-
ity and growth (Koch et al., 2013). The two main epiphytic tous algae occurs synergistically with high pCO2 levels and
algae that grew during the experiments, R. ardissonei and S. decreased photosynthesis in coralline algae. Here, the stimu-
chordalis, are naturally found in maerl beds in Brittany (Peña lation of epiphyte productivity and growth under high pCO2
et al., 2014). The response of the alga S. chordalis to in- is likely to increase the competition with underlying maerl,
creased temperature and pCO2 differed from that of R. ardis- especially through reduction in incident light.
sonei. This difference suggests that the response is species- Although assemblages were mainly composed of living
specific, even among fleshy algae, as demonstrated by Kram and dead maerl, the response of GPP and R of L. coral-

Figure 4. Biomass of epiphytic fleshy algae (mean ± SE, n = 5) ob-

tained in the different pCO2 (A-pCO2 is ambient pCO2 ; H-pCO2
is high-pCO2 ) and temperature (T is ambient temperature; T +3 ◦ C
is high temperature) treatments after the 3-month experiments in
winter (dark gray) and summer (light gray) experiments. Letters in-
dicate significant differences between the four treatments (x, y in
the summer; Tukey HSD test). Tukey tests were performed when a
significant effect of temperature or pCO2 was detected using two-
way ANOVAs.
lioides to increased temperature and pCO2 differed from that

observed in assemblages. For example, the temperature in-
crease of +3 ◦ C reduced living L. corallioides R in the winter
but increased R in the summer. Under high pCO2 conditions,
although CO2 availability for photosynthesis was higher, no
difference was observed in L. corallioides, probably due to
the ability of this species to employ inorganic carbon acquisi-
tion mechanisms (Kübler and Dudgeon, 2015). Interestingly,
GPP, R, and chlorophyll a content of dead maerl were of
the same magnitude as for living maerl. Although live algae
prevent bio-fouling by shedding their surface layers (Keats
et al., 1997; Villas Bôas and Figueiredo, 2004), post-mortem
colonisation by photosynthetic endolithic assemblages may
occur within dead crusts (Diaz-Pulido et al., 2012). More-
over, dead thalli may represent a substrate for the settlement
of crustose coralline algae (CCA) that cover small parts of
some thalli. CCA colonisation may also contribute to the ob-
served GPP and R values. In dead maerl, only R decreased
Figure 5. Net and gross primary production (a and b, respectively),
under high pCO2 , while no effect was detected for GPP.
respiration (c), and light and dark calcification rates (d and e, re-
These findings also suggest the importance of dead maerl spectively) rates (mean ± SE, n = 5) of assemblages in the different
to assemblage carbonate fluxes during the experiments. For pCO2 (A-pCO2 is ambient pCO2 ; H-pCO2 is high-pCO2 ) and
example, endolithic algae appear to play an important role in temperature (T is ambient temperature; T + 3 ◦ C is high tempera-
the dissolution of a CCA species, Porolithon onkodes (Reyes- ture) treatments. The assemblages were maintained during 3 months
Nivia et al., 2014). Through their photosynthesis, endolithic in winter (dark gray) and summer conditions (light gray). Letters in-
algae may elevate interstitial pH within the P. onkodes skele- dicate significant differences between the four treatments in winter
ton (Reyes-Nivia et al., 2013), increasing carbonate cement (a, b, c) and summer (x, y, z) conditions (Tukey HSD test). ns is not
precipitation (Diaz-Pulido et al., 2014). Within dead L. coral- significant. Tukey tests were performed when a significant effect of
temperature or pCO2 was detected using two-way ANOVAs.

lioides, the presence of endolithic algae combined with the lusks and urchins, several studies have demonstrated a link
presence of small patches of CCA on the surface of thalli between feeding rates and other metabolic processes, such
may explain the calcification rates observed in light and dis- as respiration, calcification, and excretion (Carr and Bruno,
solution in dark. Considering the high Mg content in the 2013; Navarro et al., 2013; Noisette et al., 2016). In mol-
skeleton of L. corallioides, increased pCO2 likely promotes lusks, a wide range of responses to ocean acidification and
the dissolution of dead thalli. Alternatively, the increase in warming have been revealed (Gazeau et al., 2013; Parker
dissolution observed in the present study may be associated et al., 2013). The differences in sensitivity of mollusks to
with a reduction of CCA recruitment over the surface of dead ocean acidification depend on several parameters, such as
thalli under acidified conditions (Jokiel et al., 2008; Ordoñez the form of CaCO3 they precipitate during calcification (Ries
et al., 2014). These results are consistent with the negative et al., 2009) and their ability to regulate the acid–base bal-
response to increased pCO2 observed here in assemblage Gl ance (Gutowska et al., 2010). Our results corroborate these
and Gd values, which appeared strongly related to the re- studies, given that G. magus and J. exasperatus responded
sponse of living maerl calcification rates. The high sensitivity differently to acidification and warming. Increased tempera-
of coralline algae to ocean acidification has already been at- ture and pCO2 had no effect on G. magus with regard to the
tributed to their high Mg-calcite content (Morse et al., 2006; metabolic functions tested. However, despite the apparent re-
Hofmann and Bischof, 2014). In the present study, the pCO2 sistance of G. magus to the applied changes, other physiolog-
increase had adverse consequences on assemblage Gd in both ical parameters that we did not test here may have been af-
winter and summer. In the dark, assemblage R reduced sea- fected, such as feeding rates, somatic growth, enzyme activ-
water pH by releasing CO2 and hindered the precipitation ity, or immune response (Parker et al., 2013). The respiration
of CaCO3 (Cornwall et al., 2013). Under high pCO2 condi- rates of J. exasperatus showed a decline under high pCO2
tions, the combined effect of acidification and assemblage R in the winter. The lower growth of epiphytes and biofilm
in the dark is likely to increase the sensitivity of living and in winter may reduce the energy available to maintain the
dead L. corallioides to dissolution (Andersson et al., 2009). metabolism under stressful conditions (Thomsen et al., 2013;
Moreover, as discussed above, the overgrowth of epiphytic Pansch et al., 2014). This reduced energy availability may
algae under high pCO2 increased assemblage R in the dark. induce changes in energy partitioning and decrease R under
Therefore, the negative effect of ocean acidification on L. high pCO2 . In the summer, the increased R under high pCO2
corallioides Gd would be exacerbated by the presence of epi- can be attributed to higher food supply, which is likely to in-
phytic algae, which promote a decline in pH in the dark. In crease the resistance of J. exasperatus to climate change, as
light, several studies have suggested that moderate growth reported for several marine taxa (Ramajo et al., 2016).
of fleshy macroalgal communities may reduce the impact Given the relatively high resistance of G. magus and J. ex-
of ocean acidification on coralline calcification by reducing asperatus to predicted changes, the metabolic response of P.
the CO2 concentration of seawater through photosynthesis miliaris appears to have stronger implications on assemblage
(Semesi et al., 2009; Short et al., 2014). Conversely, other functioning. For example, P. miliaris is considered as one of
studies showed that the overgrowth of epiphytic fleshy algae the main macro-epiphytic grazers on maerl beds in the Bay of
may shade underlying coralline algae and reduce coralline Brest (Guillou et al., 2002). During the experiments, P. mil-
net calcification rates (Garrabou and Ballesteros, 2000; Mar- iaris likely played an important role in the regulation of epi-
tin and Gattuso, 2009). The present findings support this idea phytic biomass. The response of Gl to temperature and pCO2
because a decline in assemblage Gl was observed under high changes was complex. The interaction between temperature
pCO2 and high epiphyte biomass. Under high pCO2 , the and pCO2 observed in the summer may cause changes in
overgrowth of epiphytic fleshy algae induced by ocean acid- energy partitioning, thereby inducing a trade-off between
ification in the summer may reduce light, oxygen, and nu- metabolic processes at the expense of respiration and excre-
trient availability for underlying maerl, affecting its primary tion (Garilli et al., 2015). However, the effect of temperature
production and calcification (D’Antonio, 1985; Short et al., and pCO2 on the calcification of P. miliaris must be con-
2014). Thus, overgrown maerl would be negatively affected sidered carefully. For instance, urchins defecated carbonate
by the direct effect of ocean acidification on calcification pellets following consumption of maerl thalli. These feces
rates and indirect effects due to shifts in competition dynam- are likely to dissolve during incubation, introducing a bias
ics with fleshy epiphytic algae (Kuffner et al., 2008). How- in the measurement of calcification (Gazeau et al., 2015). In
ever, the response of epiphytic algae is likely to be species- the summer, temperature increase by 3 ◦ C reduced P. miliaris
specific and it appears difficult to generalize the impacts of respiration rates. Moreover, the decrease in excretion under
epiphytic algae on coralline algae. high temperature and pCO2 conditions was modulated by the
In regard to the present results, the regulation of epiphyte interaction between these two factors. Temperature is a major
biomass by grazers appears essential to maintain the proper factor affecting physiological processes in ectotherms such
functioning of maerl bed communities (Guillou et al., 2002). as metabolic rates and growth (Kordas et al., 2011). In P. mil-
The importance of grazers to control epiphytes growth in iaris, summer temperatures are likely to exceed the physio-
aquaria has been shown by Jokiel et al. (2008). In mol- logical thresholds of organisms, inducing a metabolic decline

when maintained at 20 ◦ C. Although this decline has only Data availability. Data are available by direct request to the corre-
been measured for respiration and excretion, the increase in sponding author.
temperature is also likely to affect sea urchin feeding effi-
ciency (Thomas et al., 2000; Carr and Bruno, 2013). There-
fore, the ability of P. miliaris to regulate epiphyte biomass The Supplement related to this article is available online
may be significantly altered under predicted acidification and at https://doi.org/10.5194/bg-14-5359-2017-supplement.
warming conditions.
In addition to the impact of climate change on grazer-
fleshy macroalgae interactions, predicted changes may also
considerably alter the interaction between grazers and Author contributions. EL, SM, PR, JG, and JC designed the exper-
coralline algae. Asnaghi et al. (2013) demonstrated that the iments; EL, SM, and JC collected the data; EL and ML analysed the
grazing activity by urchins may exacerbate pCO2 effects on data; EL, SM, PR, and JG prepared the manuscript with contribu-
coralline algae. Ocean acidification may alter the structural tions from all co-authors.
integrity of coralline algae, increasing its sensitivity to graz-
ing (Johnson and Carpenter, 2012; Ragazzola et al., 2012).
Coralline algae may thus be more susceptible to grazing by Competing interests. The authors declare that they have no conflict
urchins, which also benefit from a higher carbonate uptake of interest.
from their diet to modulate their response to ocean acidifica-
tion (Asnaghi et al., 2013). In L. corallioides, the decrease
in calcification rates may alter its structural integrity and Acknowledgements. The authors thank the CRBM (Center of
Marine Biologic Resources) at the Station Biologique de Roscoff
increase its susceptibility to grazing, especially by urchins,
for its kind permission to use their premises for the duration of the
which are considered to important bioeroders of coralline al- experiments. We are grateful to Olivier Bohner for his laboratory
gae in marine ecosystems (Ballesteros, 2006; O’Leary and assistance and for the help in system maintenance. We also thank
McClanahan, 2010), particularly in maerl beds (Lawrence, Murielle Jam for freeze-drying samples. We acknowledge the crew
2013). of the research vessel Albert Lucas for its help with species collec-
In conclusion, the community response to climate change tion. We also thank the SOMLIT (Service d’Observation en Milieu
does not appear to only be the result of individual species’ LITtoral, INSU-CNRS) program for the temperature data sets
metabolic responses but also strongly depend on shifts in provided. We thank Carolyn Engel-Gautier for language editing of
species interactions. In contrast with other studies, which the manuscript. This work was supported by the Brittany Regional
have shown larger impacts of the combination of increased Council, the French National Research Agency via the “Investment
pCO2 and temperature than that of these factors alone (Rey- for the Future” program IDEALG (no. ANR-10-BTBR-04), and
the French national EC2CO program (“Écosphère Continentale et
naud et al., 2003; Anthony et al., 2008; Martin and Gattuso,
Côtière”, project MAERLCHANGE).
2009; Rodolfo-Metalpa et al., 2010), we showed here that
the effects of pCO2 and temperature on maerl bed communi- Edited by: Clare Woulds
ties were weakened when these factors were combined. Here, Reviewed by: Laurie Hofmann, G. Diaz-Pulido,
we also demonstrated that climate change may affect grazer and William Ross Hunter
physiology, with major consequences on their ability to reg-
ulate epiphyte biomass. Epiphyte overgrowth is thus likely
to adversely affect underlying coralline algae, increasing the
References
shading effect at light and the pH decline in the dark. Cli-
mate change may also affect other components that we did Alsterberg, C., Eklof, J. S., Gamfeldt, L., Havenhand, J.
not assess in the present study, such as algal palatability and N., and Sundback, K.: Consumers mediate the effects
potential changes in grazer trophic behaviour (Campbell et of experimental ocean acidification and warming on pri-
al., 2014; Duarte et al., 2015; Poore et al., 2013, 2016). Al- mary producers, P. Natl. Acad. Sci. USA, 110, 8603–8608,
gal palatability to grazers may also be affected by predicted https://doi.org/10.1073/pnas.1303797110, 2013.
changes through shifts in the composition and the quantity Amado-Filho, G. M., Maneveldt, G. W., Pereira, G. H., Manso, R.
of allelopathic compounds, as suggested by Del Monaco et C. C., Bahia, R. G., Barros-Barreto, M. B., and Guimaraes, S.:
al. (2017). In order to better understand the consequences Seaweed diversity associated with a Brazilian tropical rhodolith
bed, Cienc. Mar., 36, 371–391, 2010.
of climate change on ecosystem functioning, further work
Andersson, A. J., Kuffner, I. B., Mackenzie, F. T., Jokiel, P.
should focus on the response of marine communities and
L., Rodgers, K. S., and Tan, A.: Net Loss of CaCO3 from
consider more specifically shifts in species interactions, in- a subtropical calcifying community due to seawater acidifica-
cluding changes in trophic interactions between algae and tion: mesocosm-scale experimental evidence, Biogeosciences, 6,
grazers. 1811–1823, https://doi.org/10.5194/bg-6-1811-2009, 2009.
Anthony, K. R. N., Kline, D. I., Diaz-Pulido, G., Dove, S., and
Hoegh-Guldberg, O.: Ocean acidification causes bleaching and

productivity loss in coral reef builders, P. Natl. Acad. Sci. USA, and warming on the mortality and dissolution of coralline
105, 17442–17446, https://doi.org/10.1073/pnas.0804478105, algae, J. Phycol., 48, 32–39, https://doi.org/10.1111/j.1529-
2008. 8817.2011.01084.x, 2012.
Asnaghi, V., Chiantore, M., Mangialajo, L., Gazeau, F., Francour, Diaz-Pulido, G., Nash, M. C., Anthony, K. R. N., Bender, D.,
P., Alliouane, S., and Gattuso, J. P.: Cascading effects of ocean Opdyke, B. N., Reyes-Nivia, C., and Troitzsch, U.: Greenhouse
acidification in a rocky subtidal community, Plos One, 8, e61978, conditions induce mineralogical changes and dolomite accumu-
https://doi.org/10.1371/journal.pone.0061978, 2013. lation in coralline algae on tropical reefs, Nat. Commun., 5, 3310,
Auster, P. J., Estes, J. A., and Coleman, F. C.: Species interactions https://doi.org/10.1038/ncomms4310, 2014.
in marine communities: the invisible fabric of nature, Bull. Mar. Dickson, A. G., Sabine, C. L., and Christian, J. R.: Guide to best
Sci., 89, 3–9, https://doi.org/10.5343/bms.2012.1051, 2013. practices for ocean CO2 measurements. In: PICES special pub-
Baggini, C., Salomidi, M., Voutsinas, E., Bray, L., Krasakopoulou, lication, North Pacific Marine Science Organization, Sidney,
E., and Hall-Spencer, J. M.: Seasonality affects macroalgal com- British Columbia, 3, 191 pp., 2007.
munity response to increases in pCO2 , Plos One, 9, e106520, Duarte, C., Lopez, J., Benitez, S., Manriquez, P. H., Navarro,
https://doi.org/10.1371/journal.pone.0106520, 2014. J. M., Bonta, C. C., Torres, R., and Quijón, P.: Ocean acid-
Ballesteros, E.: Mediterranean coralligenous assemblages: A syn- ification induces changes in algal palatability and herbivore
thesis of present knowledge, in: Oceanography and Marine Biol- feeding behavior and performance, Oecologia, 180, 453–462,
ogy – an Annual Review, edited by: Gibson, R. N., Atkinson, R. https://doi.org/10.1007/s00442-015-3459-3, 2015.
J. A., and Gordon, J. D. M., Crc Press-Taylor & Francis Group, Dupont, S., Ortega-Martinez, O., and Thorndyke, M.: Impact of
Boca Raton, 123–195, 2006. near-future ocean acidification on echinoderms, Ecotoxicology,
Bopp, L., Resplandy, L., Orr, J. C., Doney, S. C., Dunne, J. P., 19, 449–462, https://doi.org/10.1007/s10646-010-0463-6, 2010.
Gehlen, M., Halloran, P., Heinze, C., Ilyina, T., Seferian, R., Dutertre, M., Grall, J., Ehrhold, A., and Hamon, D.:
Tjiputra, J., and Vichi, M.: Multiple stressors of ocean ecosys- Environmental factors affecting maerl bed structure
tems in the 21st century: projections with CMIP5 models, in Brittany (France), Eur. J. Phycol., 50, 371–383,
Biogeosciences, 10, 6225–6245, https://doi.org/10.5194/bg-10- https://doi.org/10.1080/09670262.2015.1063698, 2015.
6225-2013, 2013. Foster, M. S., McConnico, L. M., Lundsten, L., Wadsworth, T.,
Brockington, S. and Peck, L. S.: Seasonality of respira- Kimball, T., Brooks, L. B., Medina-Lopez, M., Riosmena-
tion and ammonium excretion in the Antarctic echinoid Rodriguez, R., Hernandez-Carmona, G., Vasquez-Elizondo, R.
Sterechinus neumayeri, Mar. Ecol. Prog. Ser., 219, 159–168, M., Johnson, S., and Steller, D. L.: Diversity and natural history
https://doi.org/10.3354/meps219159, 2001. of a Lithothamnion muelleri-Sargassum horridum community in
Campbell, J. E., Craft, J. D., Muehllehner, N., Langdon, C., and the Gulf of California, Cienc. Mar., 33, 367–384, 2007.
Paul, V. J.: Responses of calcifying algae (Halimeda spp.) to Garilli, V., Rodolfo-Metalpa, R., Scuderi, D., Brusca, L., Parrinello,
ocean acidification: implications for herbivores, Mar. Ecol. Prog. D., Rastrick, S. P. S., Foggo, A., Twitchett, R. J., Hall-Spencer,
Ser., 514, 43–56, https://doi.org/10.3354/meps10981, 2014. J. M., and Milazzo, M.: Physiological advantages of dwarfing
Carr, L. A. and Bruno, J. F.: Warming increases the top-down ef- in surviving extinctions in high-CO2 oceans, Nature Climate
fects and metabolism of a subtidal herbivore, PeerJ, 1, e109, Change, 5, 678–682, 2015.
https://doi.org/10.7717/peerj.109, 2013. Garrabou, J. and Ballesteros, E.: Growth of Mesophyllum alternans
Cook, C. M., Lanaras, T., and Colman, B.: Evidence for bicarbonate and Lithophyllum frondosum (Corallinales, Rhodophyta) in the
transport in species of red and brown macrophytic marine-algae, northwestern Mediterranean, Eur. J. Phycol., 35, 1–10, 2000.
J. Exp. Bot., 37, 977–984, https://doi.org/10.1093/jxb/37.7.977, Gazeau, F., Parker, L. M., Comeau, S., Gattuso, J. P., O’Connor,
1986. W. A., Martin, S., Pörtner, H. O., and Ross, P. M.: Impacts of
Cornwall, C. E., Hepburn, C. D., McGraw, C. M., Currie, K. I., ocean acidification on marine shelled molluscs, Mar. Biol., 160,
Pilditch, C. A., Hunter, K. A., Boyd, P. W., and Hurd, C. L.: Di- 2207–2245, https://doi.org/10.1007/s00227-013-2219-3, 2013.
urnal fluctuations in seawater pH influence the response of a cal- Gazeau, F., Urbini, L., Cox, T. E., Alliouane, S., and Gattuso, J. P.:
cifying macroalga to ocean acidification, Proc. Roy. Soc. B, 280, Comparison of the alkalinity and calcium anomaly techniques
20132201, https://doi.org/10.1098/rspb.2013.2201, 2013. to estimate rates of net calcification, Mar. Ecol. Prog. Ser., 527,
D’Antonio, C.: Epiphytes on the rocky intertidal red alga 1–12, https://doi.org/10.3354/meps11287, 2015.
Rhodomela latrix (Turner) C. Agardh: Negative effects on the Godbold, J. A. and Solan, M.: Long-term effects of warming and
host and food for herbivores, J. Exp. Mar. Biol. Ecol., 86, 197– ocean acidification are modified by seasonal variation in species
218, https://doi.org/10.1016/0022-0981(85)90103-0, 1985. responses and environmental conditions, Philos. T. Roy. Soc. B,
Davies, S. P.: Physiological ecology of Patella, I. The effect of 368, 20130186, https://doi.org/10.1098/rstb.2013.0186, 2013.
body size and temperature on metabolic rate, J. Mar. Biol. Assoc. Grall, J. and Hall-Spencer, J. M.: Problems facing maerl conser-
UK, 46, 647–658, https://doi.org/10.1017/S0025315400033397, vation in Brittany, Aquat. Conserv.-Mar. Freshw. Ecosyst., 13,
1966. S55–S64, https://doi.org/10.1002/aqc.568, 2003.
Del Monaco, C., Hay, M. E., Gartrell, P., Mumby, P. J., and Diaz- Grall, J., Le Loc’h, F., Guyonnet, B., and Riera, P.: Community
Pulido, G.: Effects of ocean acidification on the potency of structure and food web based on stable isotopes (δ 15 N and δ 13 C)
macroalgal allelopathy to a common coral, Sci. Rep., 7, 41053, analysis of a North Eastern Atlantic maerl bed, J. Exp. Mar. Biol.
https://doi.org/10.1038/srep41053, 2017. Ecol., 338, 1–15, https://doi.org/10.1016/j.jembe.2006.06.013,
Diaz-Pulido, G., Anthony, K. R. N., Kline, D. I., Dove, S., and 2006.
Hoegh-Guldberg, O.: Interactions between ocean acidification

Guillou, M., Grall, J., and Connan, S.: Can low sea urchin Kram, S. L., Price, N. N., Donham, E. M., Johnson, M. D.,
densities control macro-epiphytic biomass in a north- Kelly, E. L. A., Hamilton, S. L., and Smith, J. E.: Variable
east Atlantic maerl bed ecosystem (Bay of Brest, Brit- responses of temperate calcified and fleshy macroalgae to el-
tany, France)?, J. Mar. Biol. Assoc. UK, 82, 867–876, evated pCO2 and warming, Ices J. Mar. Sci., 73, 693–703,
https://doi.org/10.1017/s0025315402006276, 2002. https://doi.org/10.1093/icesjms/fsv168, 2016.
Gutowska, M. A., Melzner, F., Langenbuch, M., Bock, C., Kroeker, K. J., Micheli, F., and Gambi, M. C.: Ocean acid-
Claireaux, G., and Pörtner, H.-O.: Acid-base regulatory ability ification causes ecosystem shifts via altered competi-
of the cephalopod (Sepia officinalis) in response to environmen- tive interactions, Nature Climate Change, 3, 156–159,
tal hypercapnia, J. Comp. Physiol. B, 180, 323–335, 2010. https://doi.org/10.1038/nclimate1680, 2012.
Hale, R., Calosi, P., McNeill, L., Mieszkowska, N., and Widdi- Kroeker, K. J., Kordas, R. L., Crim, R., Hendriks, I. E., Ramajo, L.,
combe, S.: Predicted levels of future ocean acidification and Singh, G. S., Duarte, C. M., and Gattuso, J. P.: Impacts of ocean
temperature rise could alter community structure and biodi- acidification on marine organisms: quantifying sensitivities and
versity in marine benthic communities, Oikos, 120, 661–674, interaction with warming, Glob. Change Biol., 19, 1884–1896,
https://doi.org/10.1111/j.1600-0706.2010.19469.x, 2011. https://doi.org/10.1111/gcb.12179, 2013.
Hansson, L.-A., Nicolle, A., Graneli, W., Hallgren, P., Kritzberg, Kübler, J. E. and Dudgeon, S. R.: Predicting effects of
E., Persson, A., Bjork, J., Nilsson, P. A., and Bronmark, C.: ocean acidification and warming on algae lacking car-
Food-chain length alters community responses to global change bon concentrating mechanisms, Plos One, 10, e0132806,
in aquatic systems, Nature Climate Change, 3, 228–233, 2012. https://doi.org/10.1371/journal.pone.0132806, 2015.
Harley, C. D. G., Anderson, K. M., Demes, K. W., Jorve, J. P., Ko- Kuffner, I. B., Andersson, A. J., Jokiel, P. L., Rodgers, K. S., and
rdas, R. L., Coyle, T. A., and Graham, M. H.: Effects of climate Mackenzie, F. T.: Decreased abundance of crustose coralline
change on global seaweed communities, J. Phycol., 48, 1064– algae due to ocean acidification, Nat. Geosci., 1, 114–117,
1078, https://doi.org/10.1111/j.1529-8817.2012.01224.x, 2012. https://doi.org/10.1038/ngeo100, 2008.
Hily, C., Potin, P., and Floch, J. Y.: Structure of subtidal algal as- Lawrence, J. M.: Sea Urchins: Biology and Ecology, 3rd Edition,
semblages on soft-bottom sediments: fauna/flora interactions and Sea Urchins: Biology and Ecology, 3rd Edn., Elsevier Academic
role of disturbances in the Bay of Brest, France, Mar. Ecol. Prog. Press Inc, San Diego, California, USA, 531 pp., 2013.
Ser., 85, 115–130, https://doi.org/10.3354/meps085115, 1992. Lord, J. P., Barry, J. P., and Graves, D.: Impact of climate change
Hofmann, L. C. and Bischof, K.: Ocean acidification ef- on direct and indirect species interactions, Mar. Ecol. Prog. Ser.,
fects on calcifying macroalgae, Aquat. Biol., 22, 261–279, 571, 1–11, 2017.
https://doi.org/10.3354/ab00581, 2014. Martin, S. and Gattuso, J. P.: Response of Mediterranean coralline
Innes, A. J. and Houlihan, D. F.: Aquatic and aerial oxygen con- algae to ocean acidification and elevated temperature, Glob.
sumption of cool temperate gastropods: A comparison with some Change Biol., 15, 2089–2100, https://doi.org/10.1111/j.1365-
mediterranean species, Comp. Biochem. Phys. A, 82, 105–109, 2486.2009.01874.x, 2009.
https://doi.org/10.1016/0300-9629(85)90712-1, 1985. Martin, S. and Hall-Spencer, J. M.: Effects of ocean warming and
Jellison, B. M., Ninokawa, A. T., Hill, T. M., Sanford, E., and acidification on rhodolith/maërl beds, in: Rhodolith/maërl beds: a
Gaylord, B.: Ocean acidification alters the response of intertidal global perspective, edited by: Riosmena-Rodríguez, R., Nelson,
snails to a key sea star predator, P. R. Soc. Lond. B Bio., 283, W., and Aguirre, J., Coastal Research Library, Springer Interna-
20160890, https://doi.org/10.1098/rspb.2016.0890, 2016. tional Publishing, Cham, Vol. 15, 55–85, 2016.
Johnson, M. D. and Carpenter, R. C.: Ocean acidifica- Martin, S., Castets, M. D., and Clavier, J.: Primary production, res-
tion and warming decrease calcification in the crustose piration and calcification of the temperate free-living coralline
coralline alga Hydrolithon onkodes and increase suscepti- alga Lithothamnion corallioides, Aquat. Bot., 85, 121–128,
bility to grazing, J. Exp. Mar. Biol. Ecol., 434, 94–101, https://doi.org/10.1016/j.aquabot.2006.02.005, 2006a.
https://doi.org/10.1016/j.jembe.2012.08.005, 2012. Martin, S., Thouzeau, G., Chauvaud, L., Jean, F., Guerin, L., and
Jokiel, P. L., Rodgers, K. S., Kuffner, I. B., Andersson, A. J., Cox, E. Clavier, J.: Respiration, calcification, and excretion of the in-
F., and Mackenzie, F. T.: Ocean acidification and calcifying reef vasive slipper limpet, Crepidula fornicata L.: Implications for
organisms: a mesocosm investigation, Coral Reefs, 27, 473–483, carbon, carbonate, and nitrogen fluxes in affected areas, Limnol.
https://doi.org/10.1007/s00338-008-0380-9, 2008. Oceanogr., 51, 1996–2007, 2006b.
Keats, D. W., Knight, M. A., and Pueschel, C. M.: Antifouling Martin, S., Clavier, J., Chauvaud, L., and Thouzeau, G.: Com-
effects of epithallial shedding in three crustose coralline algae munity metabolism in temperate maerl beds, I. Carbon
(Rhodophyta, Coralinales) on a coral reef, J. Exp. Mar. Biol. and carbonate fluxes, Mar. Ecol. Prog. Ser., 335, 19–29,
Ecol., 213, 281–293, 1997. https://doi.org/10.3354/meps335019, 2007.
Koch, M., Bowes, G., Ross, C., and Zhang, X. H.: Cli- Martin, S., Cohu, S., Vignot, C., Zimmerman, G., and Gattuso, J.
mate change and ocean acidification effects on seagrasses P.: One-year experiment on the physiological response of the
and marine macroalgae, Glob. Change Biol., 19, 103–132, Mediterranean crustose coralline alga, Lithophyllum cabiochae,
https://doi.org/10.1111/j.1365-2486.2012.02791.x, 2013. to elevated pCO2 and temperature, Ecol. Evolut., 3, 676–693,
Kordas, R. L., Harley, C. D. G., and O’Connor, M. I.: https://doi.org/10.1002/ece3.475, 2013.
Community ecology in a warming world: The influ- McCoy, S. J. and Kamenos, N. A.: Coralline algae (Rhodophyta)
ence of temperature on interspecific interactions in main a changing world: integrating ecological, physiological, and
rine systems, J. Exp. Mar. Biol. Ecol., 400, 218–226, geochemical responses to global change, J. Phycol., 51, 6–24,
https://doi.org/10.1016/j.jembe.2011.02.029, 2011. https://doi.org/10.1111/jpy.12262, 2015.

Morse, J. W., Andersson, A. J., and Mackenzie, F. T.: Ini- Poore, A. G. B., Graham, S. E., Byrne, M., and Dworjanyn, S.
tial responses of carbonate-rich shelf sediments to rising at- A.: Effects of ocean warming and lowered pH on algal growth
mospheric pCO2 and “ocean acidification”: Role of high and palatability to a grazing gastropod, Mar. Biol., 163, 1–11,
Mg-calcites, Geochim. Cosmochim. Ac., 70, 5814–5830, https://doi.org/10.1007/s00227-016-2878-y, 2016.
https://doi.org/10.1016/j.gca.2006.08.017, 2006. Potin, P., Floch, J. Y., Augris, C., and Cabioch, J.: Annual growth
Navarro, J. M., Torres, R., Acuña, K., Duarte, C., Man- rate of the calcareous red alga Lithothamnion corallioides
riquez, P. H., Lardies, M., Lagos, N. A., Vargas, C., (Corallinales, Rhodophyta) in the bay of Brest, France, Hy-
and Aguilera, V.: Impact of medium-term exposure to el- drobiologia, 204, 263–267, https://doi.org/10.1007/bf00040243,
evated pCO2 levels on the physiological energetics of 1990.
the mussel Mytilus chilensis, Chemosphere, 90, 1242–1248, Ragazzola, F., Foster, L. C., Form, A., Anderson, P. S. L., Hansteen,
https://doi.org/10.1016/j.chemosphere.2012.09.063, 2013. T. H., and Fietzke, J.: Ocean acidification weakens the structural
Noisette, F., Bordeyne, F., Davoult, D., and Martin, S.: Assess- integrity of coralline algae, Glob. Change Biol., 18, 2804–2812,
ing the physiological responses of the gastropod Crepidula https://doi.org/10.1111/j.1365-2486.2012.02756.x, 2012.
fornicata to predicted ocean acidification and warming, Lim- Ramajo, L., Perez-Leon, E., Hendriks, I. E., Marba, N., Krause-
nol. Oceanogr., 61, 430–444, https://doi.org/10.1002/lno.10225, Jensen, D., Sejr, M. K., Blicher, M. E., Lagos, N. A.,
2016. Olsen, Y. S., and Duarte, C. M.: Food supply confers cal-
O’Connor, M. I., Gilbert, B., and Brown, C. J.: Theoretical cifiers resistance to ocean acidification, Sci. Rep., 6, 19374,
predictions for how temperature affects the dynamics of in- https://doi.org/10.1038/srep19374, 2016.
teracting herbivores and plants, Am. Nat., 178, 626–638, Reyes-Nivia, C., Diaz-Pulido, G., Kline, D., Ove Hoegh, G., and
https://doi.org/10.1086/662171, 2011. Dove, S.: Ocean acidification and warming scenarios increase
O’Leary, J. K. and McClanahan, T. R.: Trophic cascades result microbioerosion of coral skeletons, Glob. Change Biol., 19,
in large-scale coralline algae loss through differential grazer 1919–1929, https://doi.org/10.1111/gcb.12158, 2013.
effects, Ecology, 91, 3584–3597, https://doi.org/10.1890/09- Reyes-Nivia, C., Diaz-Pulido, G., and Dove, S.: Relative roles of
2059.1, 2010. endolithic algae and carbonate chemistry variability in the skele-
Olabarria, C., Arenas, F., Viejo, R. M., Gestoso, I., Vaz-Pinto, F., tal dissolution of crustose coralline algae, Biogeosciences, 11,
Incera, M., Rubal, M., Cacabelos, E., Veiga, P., and Sobrino, 4615–4626, https://doi.org/10.5194/bg-11-4615-2014, 2014.
C.: Response of macroalgal assemblages from rockpools to cli- Reynaud, S., Leclercq, N., Romaine-Lioud, S., Ferrier-Pages, C.,
mate change: effects of persistent increase in temperature and Jaubert, J., and Gattuso, J. P.: Interacting effects of CO2 par-
CO2 , Oikos, 122, 1065–1079, https://doi.org/10.1111/j.1600- tial pressure and temperature on photosynthesis and calcifica-
0706.2012.20825.x, 2013. tion in a scleractinian coral, Glob. Change Biol., 9, 1660–1668,
Ordoñez, A., Doropoulos, C., and Diaz-Pulido, G.: Effects of https://doi.org/10.1046/j.1529-8817.2003.00678.x, 2003.
ocean acidification on population dynamics and community Ries, J. B., Cohen, A. L., and McCorkle, D. C.: Marine calcifiers
structure of crustose coralline algae, Biol. Bull., 226, 255–268, exhibit mixed responses to CO2 -induced ocean acidification, Ge-
https://doi.org/10.1086/BBLv226n3p255, 2014. ology, 37, 1131–1134, https://doi.org/10.1130/g30210a.1, 2009.
Pajusalu, L., Martin, G., and Pollumae, A.: Results of labo- Ritchie, R. J.: Universal chlorophyll equations for estimating
ratory and field experiments of the direct effect of increas- chlorophylls a, b, c, and d and total chlorophylls in natu-
ing CO2 on net primary production of macroalgal species in ral assemblages of photosynthetic organisms using acetone,
brackish-water ecosystems, P. Est. Acad. Sci., 62, 148–154, methanol, or ethanol solvents, Photosynthetica, 46, 115–126,
https://doi.org/10.3176/proc.2013.2.09, 2013. https://doi.org/10.1007/s11099-008-0019-7, 2008.
Pansch, C., Schaub, I., Havenhand, J., and Wahl, M.: Habitat traits Rodolfo-Metalpa, R., Martin, S., Ferrier-Pagès, C., and Gattuso,
and food availability determine the response of marine inverte- J.-P.: Response of the temperate coral Cladocora caespitosa to
brates to ocean acidification, Glob. Change Biol., 20, 265–277, mid- and long-term exposure to pCO2 and temperature levels
https://doi.org/10.1111/gcb.12478, 2014. projected for the year 2100 AD, Biogeosciences, 7, 289–300,
Parker, L. M., Ross, P. M., O’Connor, W. A., Pörtner, H.-O., Scanes, https://doi.org/10.5194/bg-7-289-2010, 2010.
E., and Wright, J. M.: Predicting the response of molluscs to the Sampaio, E., Rodil, I. F., Vaz-Pinto, F., Fernández, A., and
impact of ocean acidification, Biology, 2, 651–692, 2013. Arenas, F.: Interaction strength between different graz-
Peña, V. and Barbara, I.: Seasonal patterns in the maerl com- ers and macroalgae mediated by ocean acidification
munity of shallow European Atlantic beds and their use as a over warming gradients, Mar. Environ. Res., 125, 25–33,
baseline for monitoring studies, Eur. J. Phycol., 45, 327–342, https://doi.org/10.1016/j.marenvres.2017.01.001, 2017.
https://doi.org/10.1080/09670261003586938, 2010. Semesi, I. S., Kangwe, J., and Bjork, M.: Alterations in seawater pH
Peña, V., Bárbara, I., Grall, J., Maggs, C. A., and Hall-Spencer, and CO2 affect calcification and photosynthesis in the tropical
J. M.: The diversity of seaweeds on maerl in the NE Atlantic, coralline alga, Hydrolithon sp (Rhodophyta), Estuar. Coast. Shelf
Mar. Biodivers., 44, 533–551, https://doi.org/10.1007/s12526- S., 84, 337–341, https://doi.org/10.1016/j.ecss.2009.03.038,
014-0214-7, 2014. 2009.
Poore, A. G. B., Graba-Landry, A., Favret, M., Brennand, Short, J., Kendrick, G. A., Falter, J., and McCulloch, M. T.: Inter-
H. S., Byrne, M., and Dworjanyn, S. A.: Direct and indi- actions between filamentous turf algae and coralline algae are
rect effects of ocean acidification and warming on a ma- modified under ocean acidification, J. Exp. Mar. Biol. Ecol., 456,
rine plant-herbivore interaction, Oecologia, 173, 1113–1124, 70–77, https://doi.org/10.1016/j.jembe.2014.03.014, 2014.
https://doi.org/10.1007/s00442-013-2683-y, 2013.

Short, J. A., Pedersen, O., and Kendrick, G. A.: Turf al- Villas Bôas, A. B. and Figueiredo, M. A. d. O.: Are anti-fouling
gal epiphytes metabolically induce local pH increase, effects in coralline algae species specific?, Braz. J. Oceanogr.,
with implications for underlying coralline algae under 52, 11–18, 2004.
ocean acidification, Estuar. Coast. Shelf S., 164, 463–470, Widdicombe, S. and Spicer, J. I.: Predicting the impact of
https://doi.org/10.1016/j.ecss.2015.08.006, 2015. ocean acidification on benthic biodiversity: What can animal
Smith, S. V. and Key, G. S.: Carbon-dioxide and metabolism physiology tell us?, J. Exp. Mar. Biol. Ecol., 366, 187–197,
in marine environments, Limnol. Oceanogr., 20, 493–495, https://doi.org/10.1016/j.jembe.2008.07.024, 2008.
https://doi.org/10.4319/lo.1975.20.3.0493, 1975. Yang, Y., Hansson, L., and Gattuso, J. P.: Data compilation on
Solorzano, L.: Determination of ammonia in natural waters by the the biological response to ocean acidification: an update, Earth
phenolhypochlorite method, Limnol. Oceanogr., 14, 799–801, Syst. Sci. Data, 8, 79–87, https://doi.org/10.5194/essd-8-79-
1969. 2016, 2016.
Thomas, C. W., Crear, B. J., and Hart, P. R.: The effect of temper-
ature on survival, growth, feeding and metabolic activity of the
southern rock lobster, Jasus edwardsii, Aquaculture, 185, 73–84,
https://doi.org/10.1016/S0044-8486(99)00341-5, 2000.
Thomsen, J., Casties, I., Pansch, C., Kortzinger, A., and Melzner,
F.: Food availability outweighs ocean acidification effects in ju-
venile Mytilus edulis: laboratory and field experiments, Glob.
Change Biol., 19, 1017–1027, 2013.

Article 5 en Plus

Uploaded by

Copyright:

Available Formats

Article 5 en Plus

Uploaded by

Document Information

Original Description:

Original Title

Copyright

Available Formats

Share this document

Share or Embed Document

Sharing Options

Did you find this document useful?

Is this content inappropriate?

Copyright:

Available Formats

Article 5 en Plus

Uploaded by

Copyright:

Available Formats

Biogeosciences, 14, 5359–5376, 2017

Species interactions can shift the response of a maerl bed

Correspondence to: Erwann Legrand ([email protected])

Received: 20 June 2017 – Discussion started: 29 June 2017

Published by Copernicus Publications on behalf of the European Geosciences Union.

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

Experimental pCO2 r pHT Temperature AT DIC Ar Ca

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

Chl a = 3.2 Metabolic responses of living L. corallioides to

www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

Table 4. Results the analysis of variance testing the effects of

T 1.8 0.184 0.3 0.588 0.0 0.890

pCO2 0.0 0.865 1.0 0.343 1.2 0.286

pCO2 3.9 0.066 0.1 0.823 2.7 0.119

T 1.1 0.303 0.0 0.895 0.4 0.550

pCO2 0.2 0.679 0.6 0.449 1.8 0.199

pCO2 × T 0.1 0.717 0.4 0.546 0.1 0.749

pCO2 × T 0.8 0.391

pCO2 × T 0.8 0.832

epiphyte biomass under elevated pCO2 (two-way ANOVA,

3.5 Metabolic responses of assemblages to acidification

Assemblage metabolism was significantly higher in the sum-

mer than in the winter regardless of the metabolic parameter

tested (Table 3). No temperature effect was observed on NPP,

pCO2 condition enhanced NPP in both seasons. High pCO2

increased under high pCO2 in summer conditions. Gl in-

creased under high temperature in the summer only (Fig. 5d).

Conversely, high pCO2 reduced Gl regardless of the season.

In the dark, net dissolution was observed in the winter, but

net precipitation occurred in summer conditions at high tem-

perature (Fig. 5e). In the winter, high pCO2 increased net

dissolutions rates, while in the summer Gd increased under

www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

4 Discussion portant driver influencing the magnitude and the direction of

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

Net production Gross production Respiration

T 0.1 0.762 1.1 0.317 5.5 0.019%

pCO2 3.0 0.082 5.5 0.032 3.9 0.049%

Net production Gross production Respiration Light calcification Dark calcification

www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

Figure 4. Biomass of epiphytic fleshy algae (mean ± SE, n = 5) ob-

lioides to increased temperature and pCO2 differed from that

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

www.biogeosciences.net/14/5359/2017/ Biogeosciences, 14, 5359–5376, 2017

Biogeosciences, 14, 5359–5376, 2017 www.biogeosciences.net/14/5359/2017/

You might also like

Experimental pCO2 r pHT Temperature AT DIC Ar Ca