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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