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Received: 10 July 2018 Revised: 2 October 2018 Accepted: 10 October 2018 DOI: 10.1002/ece3.4679
ORIGINAL RESEARCH
Responses of macroalgae to CO2 enrichment cannot be inferred solely from their inorganic carbon uptake strategy Luna M. van der Loos1,2 Christina M. McGraw4 Peter D. Nichols1,5
| Matthias Schmid1 | Damon Britton1
| Pablo P. Leal1,3
| Andrew T. Revill5
| | Patti Virtue1,5,6
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| Catriona L. Hurd1
1 Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, Tasmania, Australia 2
Marine Ecology, University of Groningen, Groningen, The Netherlands 3
Instituto de Fomento Pesquero (IFOP), Puerto Montt, Chile
4
Department of Chemistry, NIWA/ University of Otago Research Centre for Oceanography, University of Otago, Dunedin, New Zealand 5
CSIRO Oceans and Atmosphere, Hobart, Tasmania, Australia
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Antarctic Climate and Ecosystems, Cooperative Research Centre, Hobart, Tasmania, Australia Correspondence Luna M. van der Loos, Institute for Marine and Antarctic Studies, University of Tasmania, Hobart, TAS, Australia. Email:
[email protected] Funding information Holland Scholarship; Groningen University Fund; Deutsche Forschungsgemeinschaft
Abstract Increased plant biomass is observed in terrestrial systems due to rising levels of at‐ mospheric CO2, but responses of marine macroalgae to CO2 enrichment are unclear. The 200% increase in CO2 by 2100 is predicted to enhance the productivity of fleshy macroalgae that acquire inorganic carbon solely as CO2 (non‐carbon dioxide‐concen‐ trating mechanism [CCM] species—i.e., species without a carbon dioxide‐concentrat‐ ing mechanism), whereas those that additionally uptake bicarbonate (CCM species) are predicted to respond neutrally or positively depending on their affinity for bicar‐ bonate. Previous studies, however, show that fleshy macroalgae exhibit a broad vari‐ ety of responses to CO2 enrichment and the underlying mechanisms are largely unknown. This physiological study compared the responses of a CCM species (Lomentaria australis) with a non‐CCM species (Craspedocarpus ramentaceus) to CO2 enrichment with regards to growth, net photosynthesis, and biochemistry. Contrary to expectations, there was no enrichment effect for the non‐CCM species, whereas the CCM species had a twofold greater growth rate, likely driven by a downregulation of the energetically costly CCM(s). This saved energy was invested into new growth rather than storage lipids and fatty acids. In addition, we conducted a comprehensive literature synthesis to examine the extent to which the growth and photosynthetic responses of fleshy macroalgae to elevated CO2 are related to their carbon acquisi‐ tion strategies. Findings highlight that the responses of macroalgae to CO2 enrich‐ ment cannot be inferred solely from their carbon uptake strategy, and targeted physiological experiments on a wider range of species are needed to better predict responses of macroalgae to future oceanic change. KEYWORDS
carbon uptake strategy, carbon dioxide‐concentrating mechanism, CCM, CO2 enrichment, macroalgae, non‐CCM, ocean acidification, physiology
a
Holland Scholarship; Groningen University
Fund; M.S. was funded by the Deutsche Forschungsgemeinschaft (DFG, grant ID: SCHM 3335/1‐1)
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. Ecology and Evolution. 2018;1–16.
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1 | I NTRO D U C TI O N
able to use additional CO2 either exhibit a low affinity for DIC (car‐
Since the beginning of the industrial era, atmospheric CO2 concen‐
(i.e., decreased CCM activity); (b) CCM species that are considered
bon‐limited CCM species) or have CCMs that can be downregulated trations have increased by 40% (IPCC, 2013). In terrestrial systems,
unresponsive to future CO2 concentrations have either a high af‐
there is evidence of a “CO2 enrichment” effect that is resulting in
finity for CO2 or CCMs that cannot be downregulated under ele‐
a higher plant biomass (Zhu et al., 2016) as the availability of CO2
vated CO2 conditions (Cornwall et al., 2017). In contrast, growth and
for carbon fixation in photosynthetic organisms via the enzyme
photosynthesis of non‐CCM species are thought to be limited under
Rubisco increases. In coastal marine systems, macroalgae fulfill
current CO2 concentrations and they are predicted to benefit from
the same functional role as terrestrial plants; they are foundation
the future 200% increase in dissolved CO2 (Cornwall et al., 2015;
species that provide food, habitat, and shelter to higher trophic
Hepburn et al., 2011; Kübler & Dudgeon, 2015).
levels (e.g., shellfish and fish), as well as a range of ecosystem ser‐
Carbon uptake strategies in macroalgae can be determined by
vices including nutrient cycling. In addition, they have a potential
analyzing their carbon stable isotope composition (δ13C) (Maberly,
role in the blue carbon economy and climate mitigation (Bennett et
Raven, & Johnston, 1992): CO2 is more depleted in 13C than HCO3−
al., 2015; Chung, Beardall, Mehta, Sahoo, & Stojkovic, 2011; Tuya, Wernberg, & Thomsen, 2008). By the end of the century, CO2 concentrations in seawater will increase by 200% under the RCP
and thus has a lower δ13C value. Macroalgae that possess a CCM typically have δ13C values ranging between −30‰ and −10‰,
whereas a lack of a CCM is indicated by δ13C 0.5% of the
ChemStation software was used for quantification of FAME peaks.
TFA profile were used. Graphs were customized using the pack‐
The individual fatty acids were identified using a GC–mass spec‐
ages ggplot2 (Wickham, 2011), plyr (Wickham, 2011), and reshape2
trometer (MS) using a Finnigan ThermoQuest GCQ GC‐MS System
(Wickham, 2007).
fitted with an on‐column injector and using ThermoQuest Xcalibur software. To determine how macroalgae modify the carbonate chemistry of their local environment, seawater samples (13 ml) were collected
2.5 | Literature synthesis To further determine whether or not patterns in the responses of
from each replicate culture tank immediately after a change in sea‐
fleshy macroalgae to CO2 enrichment depend on their carbon up‐
water and again four hours later. These samples were collected both
take strategy, we conducted a comprehensive literature survey. We
at day 1 and day 7. Simultaneously, pHT was measured in the cul‐
searched the databases Web of Science and Google Scholar using
ture tanks with a Thermo Scientific Orion VERSA STAR 90 meter
the keywords “CO2 enrichment”, “CO2 fertilization”, “ocean acidifi‐
and pH electrode Orion 8107BNUMD Ross Ultra pH/ATC Triode,
cation”, “macroalgae”, and “seaweed” in various combinations. Fifty‐
calibrated with a Tris buffer. Seawater samples were immediately
six studies published between 1989 and 2018 were analyzed, giving
poisoned with HgCl2 and stored under constant darkness. DIC con‐
a total of 61 species. Studies were only examined if they met specific
centrations of the water samples were measured using a DIC an‐
criteria. (a) The study had to report a growth response to CO2 en‐
alyzer (Apollo SciTech DIC Analyzer Model AS‐C3) with an inbuilt
richment (in addition, photosynthetic response and δ13C response
CO2 analyzer (LI‐COR LI‐7000 CO2/H2O Analyzer). The CO2 ana‐
were noted if those were reported); (b) the study needed to be a
lyzer was calibrated with a certified reference material provided by
manipulative experiment comparing one or several macroalgal spe‐
Andrew Dickson, Scripps Institute for Oceanography, San Diego,
cies in different pCO2 treatments (thus, we excluded field studies
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that were conducted in natural pCO2 gradients); (c) the study had
van der
LOOS et al.
to ~8.5 w/w at the end of the experiment for each of the four treat‐
to report whether the species used in the experiment were able to
ment–species combinations, due to an increase in carbon content
utilize HCO3− or not (i.e., if the species possessed a CCM); (d) only
of the tissue (Supporting information Table S4). The magnitude of
studies on marine fleshy macroalgae were considered; (e) the mac‐
change in C:N ratio and C content did not differ between species and
roalgae used in the experiment had to be identified to species level
CO2 treatment (Table 1). The nitrogen content of the tissue remained
(i.e., no “turf”‐forming mats or community responses were included);
relatively constant for both L. australis and C. ramentaceus, with less
(f) studies testing the effect of CO2 enrichment on microscopic early
than 0.39% w/w difference from the start to end of the experiment
developmental stages and spore germination were excluded; and (g)
(Supporting information Table S4).
the study had to be published in a peer‐reviewed journal. Many stud‐ ies also tested additional experimental conditions (e.g., irradiance or nutrient concentrations), in combination with elevated pCO2. Those
3.4 | Biochemical responses
studies were included in our literature synthesis, but care was taken
L. australis (the CCM species) had a higher total fatty acid content
to only take into account the single‐term effects of elevated pCO2.
than C. ramentaceus (the non‐CCM species), but this was not affected by experimental treatment (Table 1; Supporting information Figure
3 | R E S U LT S 3.1 | Growth For L. australis (the CCM species), linear extension under the future
S5). Both species had similar total lipid content (Table 1; Supporting information Figure S6). Polar lipids dominated the lipid class compo‐ sition of both L. australis and C. ramentaceus (Supporting informa‐ tion Figure S7). There were no differences in lipid class percentage between species and CO2 treatment (Supporting information Figure
CO2 treatment (pH = 7.70) was twofold greater (a Hedge’s g ef‐
S7). A correspondence analysis (CA) showed that fatty acid composi‐
fect size of 1.5) than the current conditions treatment (pH = 8.04)
tion differed significantly between species, but that the composition
(Table 1, Figure 1), whereas for C. ramentaceus (the non‐CCM spe‐
in each species did not change with CO2 treatment (Figure 4). The
cies), there was no significant effect of CO2 enrichment on growth
first CA axis explained 98.2% of the variation, and the second axis
(Table 1, Figure 1). Growth rates of L. australis under the future
explained 0.8% of the variation. The difference in fatty acid compo‐
treatment were ca. eightfold and sevenfold greater (a Hedge’s g ef‐
sition was mainly driven by 16:1n‐7, 18:1n‐9, 18:0, 20:4n‐6, 20:3n‐6,
fect size of 2.8) than C. ramentaceus under both current and future
and 20:5n‐3, where the former four fatty acids were more associ‐
treatments, respectively (p 0.05 for all comparisons, linear mixed model Wald chi‐square test).
3.3 | Stable isotopes and C:N ratios
3.6 | Literature synthesis Approximately 40% of the CCM species that were tested (21 out of 55 species) showed no growth response to CO2 enrichment, five species
L. australis (the CCM species) under the future treatment had a ca.
had decreased growth rates and 16 species increased growth with
twofold greater decrease (a Hedge’s effect size of 1.2) in δ13C, com‐
elevated CO2 (Table 2). For 13 CCM species, mixed responses were
pared to the individuals of the same species in current conditions
reported (i.e., several species were tested in multiple studies, and the
(Figure 3, p 0.05, Tukey’s honestly significant
jority of the CCM species tested (11 and 10 species, respectively); in
difference tests). C:N ratios increased from ~6.5 w/w at the start
four species, photosynthesis decreased; nine species showed mixed
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TA B L E 1 Multivariate analysis of variance (MANOVA) table displaying p‐values and F‐values for all measured responses (linear extension, wet weight relative growth rate, net photosynthesis, chlorophyll a content, phycobiliprotein content, change in δ13C, change in C:N ratio, change in carbon tissue content, change in nitrogen tissue content, total lipid content, total fatty acid content, change in [H+], change in [HCO3−], change in [CO2], change in [CO32−], and change in total DIC) Factor Interaction
Species
Response
F‐value
p‐value
Linear extension
6.474
0.021
Wet weight RGR
3.125
0.095
Chlorophyll a content (mg per g wet weight)
0.509
0.485
Phycobiliprotein content (mg per g wet weight)
1.375
Net photosynthesis (µmol O2 hr−1 g−1)
F‐value
CO2 treatment F‐value
p‐value
–
–
–
15.743
0.001
2.133
0.162
20.563
