Download Calcification Energy Budgets Early Life Stages Community

Benthic Invertebrates in a High CO2 World:
What does the future hold?
We described the responses of benthic invertebrates to OA conditions predicted up to the end
of the century, examining individual organism responses through to ecosystem-level impacts.
Research over the past decade has found great variability in the physiological and functional
response of different species and communities to OA, with further variability evident between
life stages.
CO 32-
(B)
Under short-term experimentally enhanced CO2 conditions, many organisms have shown
trade-offs in their physiological responses, such as reductions in calcification rate and
reproductive output.
HCO 3
In addition, carry-over effects from fertilization, larval and juvenile stages highlight the need for
broad-scale studies over multiple life stages.
External
seawater
HCO 3
Oral
Tissue
Z
Z
These organism-level responses may propagate through to altered benthic communities under
naturally enhanced CO2 conditions, evident in studies of upwelling regions and at
shallow-water volcanic CO2 vents.
CO2
H + OH+
HCO3
We highlight some of the findings of the review, with vast variability in responses to OA
between species, habitats, life-cycle stages and experimental systems. We also suggest key
areas of research needed to enable a better understanding of the future for benthic
invertebrates in warmer, lower-pH seas.
CO2 + H2O
-
HCO3- + Ca
Mitochondria
Z
Zooxanthellae
+
CaCO3 + H
Anion exchanger
-
A lack of inherent physiological flexibility in the energy budget to compensate for changing conditions.
The majority of calcification responses to OA are negative, with changes in calcification rate
ranging from a 99% decline to a 400% increase. This is highly variable between species/genera.
Alterations in morphology have been observed in corals10 (Fig. 2) and bivalves11.
Metabolic responses have been variable between species, with many species exhibiting no
detectable change in respiration. Metabolic suppression was observed in cold-water corals12,
urchins13 and oysters14; this may be an adaptive strategy for survival under transiently stressful
conditions, or an indication that an organism cannot compensate for the internal hypercapnia.
Aboral
tissue
H+/Ca2+ exchanger
10
No significant change in feeding rate in adults of the benthic species examined, although only
seven studies have been conducted, and the controlled conditions of such studies (absence of
predators) confound potential responses.
30
20
10
OA leads to a reduction in the availability of carbonate ions in the ocean, which are important
for calcifying species; they combine these ions with calcium to form their biogenic calcium
carbonate skeletons or shells.
We examined the OA experiments on early life stages of 44 species. Fig. 4 illustrates the
potential processes which could be affected by OA throughout the life cycle of an organism.
What we know:
Differing fertilisation responses have been found between even closely related species15. While
most studies suggest that fertilization of benthic invertebrates is robust to near-future OA,
some organisms appear susceptible, with reductions in sperm motility, speed and fertilization
success reported16,17,18.
Robust fertilisation
In many invertebrate species, the embryonic and planktonic larval phases have proved
vulnerable to experimental OA conditions, evident in extended development times19, altered
morphologies17 and reduced growth and survival20. However, positive responses have also been
observed21, with no clear genera-related response at the larval stage to OA.
Crustaceans, molluscs, corals and echinoderms are known to use bicarbonate from the external
seawater as their carbonate source as well as metabolically produced CO2, which is actively
converted to bicarbonate intracellularly5,6.
30
20
While few studies have examined ecosystem effects of OA, studies in naturally high CO2 areas
have proved helpful for determining future changes.
10
0
7.8
8
7.9
8.0
8.1
Abundance and distribution
19%, P=0.003
4
The community dynamics of an ecosystem can be altered by OA if even just one species is
vulnerable to the changing water chemistry.
2
Examples:
6
0
0
7.8
12
10
8
6
4
2
0
7.9
8.0
8.1
7.8
12%, P=0.01
15
7.9
8.0
10
5
0
7.8
7.9
8.0
3.0
2.5
2.0
1.5
1.0
0.5
0.0
8.1
15%, P=0.014
8.0
Alterations in benthic community composition after a 60-day period at a pH reduced by 0.3
units, despite no significant difference in species diversity and number of individuals24.
8.1
13%, P=0.025
Reductions in coral diversity, recruitment and abundance were also observed on the shallow
CO2 vents of Papua New Guinea (PNG, Fig.3), with massive Porites corals dominating over
branching, foliose and tabulate corals at lowered pH (0.3-unit drop)25.
Competition and Predation
7.8
15
7.9
7.9
8.0
8.1
Changes in competitive and predative ability from altered energy partitioning, will affect
community dynamics, albeit dependent on the relative change of each organism.
14%, P=0.009
Examples:
10
Alterations in dominance between species in a community, such as with corals and algae seen
in natural CO2 vents25.
5
0
8.1
7.8
7.9
8.0
Acidification-induced disruption of predator avoidance strategies, such as in the snail Littorina
littorea26.
8.1
pH predicted
physiology
Adult
Future Direction & Approaches
fecundity
spawning
morphology
development rate
Juveniles
Survival
Sperm
Eggs
fertilisation
metamorphosis
Larvae
physiology
Fig. 2. Progressive changes in the mesoscale skeletal development (A–D), including distortion of
basal plate and retardation of septal development, of 8-day-old corallites of Favia fragum with
decreasing seawater saturation state. In A and E, saturation state Ω = 3.71 (control); in B and F, Ω =
2.40; in C and G, Ω = 1.03; in D and H, Ω = 0.22. (A–D) Scale bar = 200 mm. (Reproduced from
Cohen et al. 2009 with permissions.)
In future experiments, it is important to understand carry-over effects of OA between life-cycle
stages, with even seemingly minor effects on the fitness of larvae and juveniles carrying over to
the adults.
References: 1. Wicks & Roberts (2012) Oceanogr Mar Biol 50: 127-188; 2. Tambutte et al. (2007) Coral Reefs 26:517-529; 3. Al-Horani et al. (2003) JEMBE 288:1-15; 4. Hofmann et al. (2010) Ann Rev Ecol Evol S 41:127-147; 5. Wilbur & Saleuddin (1983) In The Mollusca 235-287; 6. Holcomb et al. (2010) JEMBE 386:27-33; 7. Thomsen et al. (2010) Biogeosciences 7:3879-3891; 8. Brownlee (2009) PNAS
106:16541-16542; 9. Portner et al. (2005) Scientia Marina 69, 271–285; 10. Cohen et al. (2009) Geochem Geophys Geosyst 10; Q07005; 11. Welladsen et al. (2011) J Shellfish Res 30:85-88; 12. Form & Riebesell (2011) Glob Change Biol 8:843-853; 13. Miles et al. (2007) Mar Poll Bull 4:89-96; 14. Chapman et al. (2011) Mol Ecol 20:1431-1449; 15. Byrne et al. (2011) Oceanogr Mar Biol 49:1-42; 16. Havenhand et
al. (2008) Curr Biol 18:651-652; 17. Parker et al. (2009) Glob Change Biol 15:2123-2136; 18. Morita et al. (2010) Zygote 18:103-107; 19. Stumpp et al. (2011) Comp Biochem Phys A 160:331-340; 20. Ellis et al. (2009) J Cell Biol 99:1647-1654; 21. Dupont et al. (2010) J Exp Zool Part B 314:382-389; 22. Rodriguez et al. (1993) MEPS 97:193-207; 23. Cohen & Holcomb (2009) Oceanogr 22:118-127; 24. Hale et al.
(2011) Oikos 120:661-674; 25. Fabricius et al. (2011) Nature Climate Change 1:165–169; 26. Bibby et al. (2007) Aquat Biol 2:67-74.
Regional
Ocean stratification
Terrestrial run-off
Eutrophication
Expansion of O2 minimum zones
Sea level rise
Storm events
Overfishing
Warming
I nvasive species
Reduced salinity from ice melt
Acclimation & Adaptation
Environmental factors have been shown to disrupt settlement22, however, 7 of 8 invertebrates
examined were resilient to near-future OA conditions.
Invertebrate juveniles showed variable responses to OA conditions, with predominantly
negative calcification responses23, likely due to metabolic priorities.
Local Stressors
Pollution
Fig. 4. Potential processes vulnerable to OA at different stages of the life cycle.
Normal settlement, but prolonged juvenile stage
What we need to know more about:
Multi-Stressors
morphology
recruitment
settlement
Variable responses between species, habitats and over time make this one of the most complex
challenges facing twenty-first century research. Little is known of synergistic effects of OA with
other stressors, or the acclimation & adaptation potential of organisms and communities
development rate
development rate
Smaller, delayed embryos and larvae
An organism’s ability to control pH will be important in determining how it will respond to
changes in external seawater pH.
Community-level responses
40
8.1
19%, P=0.003
Early Life Stages
Calcification is highly controlled and energetically costly, as the organism must modify and
regulate the conditions of the calcifying fluid within the calcifying space3, 4.
8.0
26%, P=0.001
Fig. 3. Progressive changes in reef biota along a pH gradient at Upa-Upasina Reef, Papua New
Guinea. Red and blue points indicate high and low pCO2 transect sections, respectively, and mean
pH was predicted from seawater measurements . HC, hard corals; SC, soft corals; CCA, Crustose
Coralline Algae; MA, Macroalgae (From Fabricius et al. 2011 with permission)
Calcification
CaCO3 crystals are nucleated and grown in an isolated or semi-isolated internal compartment,
separate from ambient seawater2.
7.9
7.8
Fig. 1. Pathways of carbon from the atmosphere to the coral skeleton. (A) The chemical equilibria of
carbon dioxide in seawater. (B) Model of inorganic carbon entering the coral tissue (solid arrows)
and H+ (broken arrows) fluxes associated with zooxanthellae photosynthesis and coral host
calcification. (Adapted from Brownlee 2009 with permission, see review for further details).
The precise cellular and molecular mechanisms controlling biocalcification and internal pH
regulation remain poorly understood. Organisms have been shown to calcify in undersaturated
environments7, but we do not know how. In particular, we need to know more about the
complex processes involved in coral calcification8 (Fig. 1).
20
40
Respiration and metabolism
Reduction in energy invested into reproduction in response to OA was evident in the few
organisms that have been tested; however is a clear priority for future research.
Skeleton
30
7.8
Growth and calcification
Massive Porites (% )
Limitations in feeding ability.
Energy intake
A2+
-
Reproductive output
+
HCO3 + H
Altered energy budget partitioning: energy is partitioned away from growth towards increased maintanance costs9.
Coelenteron
H
+
-
50
Juv Porites m−2
H 2CO 3
CO 2 + H 2O
Reductions in one or more of their energy budget parameters in response to OA may be due to:
40
Juv SC r ichness
H
Ju v HC m−2
This review addresses the effects of Ocean Acidification (OA) on the benthos1, in particular the
calcifiers thought to be most sensitive to altered carbonate chemistry.
+
Juv HC richness
(A)
6%, P=0.098
Non−calc MA (%)
Energy Budgets
50
CCA co ver (%)
Overview
CO 2
&
1,2,3
Roberts JM
HC cover (% )
1
Wicks LC
1
2-4
5-10
11-17
Fig. 5. Locations of experimental OA simulations on benthic invertebrates, using realistic pH values
up to the end of the century. Size of circle represents number of organisms studied.
Acknowledgements: UK Ocean Acidification Research Programme,
NERC, DECC, DEFRA and Heriot-Watt Environment and Climate
Change Theme. Attendance funded by MASTS, Society of
Experimental Biology and Company fo Biologists Travel Fund.
Benthic invertebrates present in polar and deep waters already naturally experience lower pH
and carbonate ion concentrations than the global average and will be among the first affected
by OA. Despite knowledge of the impending changes in ocean pH and temperature, there is a
lack of studies in both these vulnerable regions and on a global scale (Fig. 5). These areas will
be key to understanding the potential for adaptation, as may already have occurred, and will
enable us to examine the speed and extent at which adaptation can occur and how gene flow
and dispersal may affect future adaptation.
1: Centre for Marine Biodiversity and Biotechnology, Heriot-Watt University, Edinburgh, EH14 4AS, UK
2: Center for Marine Science, University of North Carolina Wilmington, 601 S. College Road, Wilmington, NC 28403-5928, USA
3: Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll, PA37 IQA, UK