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1 2-4 5-10 11-17 Benthic Invertebrates in a High CO 2 World: What does the future hold? Wicks LC 1 & Roberts JM 1,2,3 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 Calcification Energy Budgets Early Life Stages Community-level responses Future Direction & Approaches C O 2 CO 2 + H 2 O H 2 CO 3 H + CO 3 2- HCO 3 HCO 3 CO 2 + H 2 O HCO 3 HCO 3- + Ca 2+ CaCO3 + H + HCO 3 - + H + H + + OH - H + (A) (B) External seawater Oral Tissue Coelenteron Aboral tissue Skeleton CO 2 Z Z A - Z 7.8 7.9 8.0 8.1 10 20 30 40 50 HC cover (% ) 6%, P=0.098 7.8 7.9 8.0 8.1 0 10 20 30 40 50 Massive Porites (% ) 26%, P=0.001 7.8 7.9 8.0 8.1 0 10 20 30 40 Ju v HC m -2 19%, P=0.003 7.8 7.9 8.0 8.1 0 2 4 6 8 Juv Porites m -2 19%, P=0.003 7.8 7.9 8.0 8.1 0 2 4 6 8 10 12 Juv HC richness 12%, P=0.01 7.8 7.9 8.0 8.1 0.0 0.5 1.0 1.5 2.0 2.5 3.0 Juv SC r ichness 13%, P=0.025 7.8 7.9 8.0 8.1 0 5 10 15 CCA co ver (%) 15%, P=0.014 7.8 7.9 8.0 8.1 0 5 10 15 Non-calc MA (%) 14%, P=0.009 pH predicted Adult Larvae Juveniles spawning fecundity fertilisation development rate morphology development rate development rate settlement morphology physiology physiology Survival metamorphosis recruitment Sperm Eggs Overview 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 Multi-Stressors Acclimation & Adaptation 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. 2 Local Stressors Regional Pollution Ocean stratification Terrestrial run-off Expansion of O minimum zones Eutrophication Sea level rise Storm events Warming Overfishing s e i c e p s e v i s a v n I Reduced salinity from ice melt While few studies have examined ecosystem effects of OA, studies in naturally high CO 2 areas have proved helpful for determining future changes. Abundance and distribution The community dynamics of an ecosystem can be altered by OA if even just one species is vulnerable to the changing water chemistry. Examples: 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 individuals 24 . Reductions in coral diversity, recruitment and abundance were also observed on the shallow CO 2 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 Changes in competitive and predative ability from altered energy partitioning, will affect community dynamics, albeit dependent on the relative change of each organism. Examples: Alterations in dominance between species in a community, such as with corals and algae seen in natural CO 2 vents 25 . Acidification-induced disruption of predator avoidance strategies, such as in the snail Littorina littorea 26 . This review addresses the effects of Ocean Acidification (OA) on the benthos 1 , in particular the calcifiers thought to be most sensitive to altered carbonate chemistry. 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. Under short-term experimentally enhanced CO 2 conditions, many organisms have shown trade-offs in their physiological responses, such as reductions in calcification rate and reproductive output. In addition, carry-over effects from fertilization, larval and juvenile stages highlight the need for broad-scale studies over multiple life stages. These organism-level responses may propagate through to altered benthic communities under naturally enhanced CO 2 conditions, evident in studies of upwelling regions and at shallow-water volcanic CO 2 vents. 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. 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. What we know: CaCO 3 crystals are nucleated and grown in an isolated or semi-isolated internal compartment, separate from ambient seawater 2 . Calcification is highly controlled and energetically costly, as the organism must modify and regulate the conditions of the calcifying fluid within the calcifying space 3, 4 . An organism’s ability to control pH will be important in determining how it will respond to changes in external seawater pH. Crustaceans, molluscs, corals and echinoderms are known to use bicarbonate from the external seawater as their carbonate source as well as metabolically produced CO 2 , which is actively converted to bicarbonate intracellularly 5,6 . What we need to know more about: The precise cellular and molecular mechanisms controlling biocalcification and internal pH regulation remain poorly understood. Organisms have been shown to calcify in undersaturated environments 7 , but we do not know how. In particular, we need to know more about the complex processes involved in coral calcification 8 (Fig. 1). 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). 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. 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.) 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) Fig. 4. Potential processes vulnerable to OA at different stages of the life cycle. Mitochondria Zooxanthellae Anion exchanger H + /Ca 2+ exchanger Reductions in one or more of their energy budget parameters in response to OA may be due to: - Altered energy budget partitioning: energy is partitioned away from growth towards increased maintanance costs 9 . - Limitations in feeding ability. - A lack of inherent physiological flexibility in the energy budget to compensate for changing conditions. Growth and calcification 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 corals 10 (Fig. 2) and bivalves 11 . Respiration and metabolism Metabolic responses have been variable between species, with many species exhibiting no detectable change in respiration. Metabolic suppression was observed in cold-water corals 12 , urchins 13 and oysters 14 ; this may be an adaptive strategy for survival under transiently stressful conditions, or an indication that an organism cannot compensate for the internal hypercapnia. Reproductive output 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. Energy intake 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. 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. Robust fertilisation Differing fertilisation responses have been found between even closely related species 15 . 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 reported 16,17,18 . Smaller, delayed embryos and larvae In many invertebrate species, the embryonic and planktonic larval phases have proved vulnerable to experimental OA conditions, evident in extended development times 19 , altered morphologies 17 and reduced growth and survival 20 . However, positive responses have also been observed 21 , with no clear genera-related response at the larval stage to OA. Normal settlement, but prolonged juvenile stage Environmental factors have been shown to disrupt settlement 22 , 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 responses 23, likely due to metabolic priorities. 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. Acknowledgements: UK Ocean Acidification Research Programme, NERC, DECC, DEFRA and Heriot-Watt Environment and Climate Change Theme.
