Adaptive strategies of sponges to deoxygenated oceans.
Porifera
climate change
dead zones
eutrophication
evolution
hypoxic events
marine benthic hypoxia
oxygen depletion
phenotypic plasticity
sessile organisms
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
03 2022
03 2022
Historique:
revised:
08
11
2021
received:
01
09
2021
accepted:
13
11
2021
pubmed:
3
12
2021
medline:
25
2
2022
entrez:
2
12
2021
Statut:
ppublish
Résumé
Ocean deoxygenation is one of the major consequences of climate change. In coastal waters, this process can be exacerbated by eutrophication, which is contributing to an alarming increase in the so-called 'dead zones' globally. Despite its severity, the effect of reduced dissolved oxygen has only been studied for a very limited number of organisms, compared to other climate change impacts such as ocean acidification and warming. Here, we experimentally assessed the response of sponges to moderate and severe simulated hypoxic events. We ran three laboratory experiments on four species from two different temperate oceans (NE Atlantic and SW Pacific). Sponges were exposed to a total of five hypoxic treatments, with increasing severity (3.3, 1.6, 0.5, 0.4 and 0.13 mg O
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1972-1989Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Altieri, A. H., & Diaz, R. J. (2019). Dead zones: Oxygen depletion in coastal ecosystems. In C. Sheppard (Ed.), World seas: An environmental evaluation (pp. 453-473). Academic Press. https://doi.org/10.1016/b978-0-12-805052-1.00021-8
Altieri, A. H., & Gedan, K. B. (2015). Climate change and dead zones. Global Change Biology, 21(4), 1395-1406. https://doi.org/10.1111/gcb.12754
Altieri, A. H., Harrison, S. B., Seemann, J., Collin, R., Diaz, R. J., & Knowlton, N. (2017). Tropical dead zones and mass mortalities on coral reefs. Proceedings of the National Academy of Sciences of the United States of America, 114(14), 3660-3665. https://doi.org/10.1073/pnas.1621517114
Anderson, M. J. (2001). A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26(1), 32-46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Anderson, M. J. (2014). Permutational multivariate analysis of variance (PERMANOVA). In Wiley Statsref: Statistics reference online (pp. 1-15). https://doi.org/10.1002/9781118445112.stat07841
Anderson, M. J., Gorley, R. N., & Clarke, K. R. (2008). PERMANOVA+ for PRIMER: Guide to software and statistical methods. PRIMER-E.
Ayling, A. L. (1983). Factors affecting the spatial distributions of thinly encrusting sponges from temperate waters. Oecologia, 60(3), 412-418. https://doi.org/10.1007/bf00376861
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01
Bell, J. J. (2008). The functional roles of marine sponges. Estuarine, Coastal and Shelf Science, 79(3), 341-353. https://doi.org/10.1016/j.ecss.2008.05.002
Bell, J. J., & Barnes, D. K. (2000). The distribution and prevalence of sponges in relation to environmental gradients within a temperate sea lough: Vertical cliff surfaces. Diversity and Distributions, 6(6), 283-303. https://doi.org/10.1046/j.1472-4642.2000.00091.x
Bell, J. J., McGrath, E., Kandler, N. M., Marlow, J., Beepat, S. S., Bachtiar, R., Shaffer, M. R., Mortimer, C., Micaroni, V., Mobilia, V., Rovellini, A., Harris, B., Farnham, E., Strano, F., & Carballo, J. L. (2020). Interocean patterns in shallow water sponge assemblage structure and function. Biological Reviews, 95(6), 1720-1758. https://doi.org/10.1111/brv.12637
Bijma, J., Pörtner, H. O., Yesson, C., & Rogers, A. D. (2013). Climate change and the oceans - What does the future hold? Marine Pollution Bulletin, 74(2), 495-505. https://doi.org/10.1016/j.marpolbul.2013.07.022
Breitburg, D. L. (1990). Near-shore hypoxia in the Chesapeake Bay: Patterns and relationships among physical factors. Estuarine, Coastal and Shelf Science, 30(6), 593-609. https://doi.org/10.1016/0272-7714(90)90095-9
Brocks, J. J., Jarrett, A. J., Sirantoine, E., Hallmann, C., Hoshino, Y., & Liyanage, T. (2017). The rise of algae in Cryogenian oceans and the emergence of animals. Nature, 548(7669), 578-581. https://doi.org/10.1038/nature23457
Brooks, M. E., Kristensen, K., Van Benthem, K. J., Magnusson, A., Berg, C. W., Nielsen, A., Skaug, H. J., Machler, M., & Bolker, B. M. (2017). glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. The R Journal, 9(2), 378-400. https://doi.org/10.32614/rj-2017-066
Bumett, L. E., & Stickle, W. B. (2001). Physiological responses to hypoxia. In: N. N. Rabalais & R. E. Turner (Eds). Coastal and estuarine studies, Volume 58. Coastal hypoxia: Consequences for living resources and ecosystems (pp. 101-114). AGU Publications. https://doi.org/10.1029/ce058p0101
Chu, J. W., Curkan, C., & Tunnicliffe, V. (2018). Drivers of temporal beta diversity of a benthic community in a seasonally hypoxic fjord. Royal Society Open Science, 5(4), 172284. https://doi.org/10.1098/rsos.172284
Clarke, K. R., & Gorley, R. N. (2015). Getting started with PRIMER v7. PRIMER-E.
Cole, D. B., Mills, D. B., Erwin, D. H., Sperling, E. A., Porter, S. M., Reinhard, C. T., & Planavsky, N. J. (2020). On the co-evolution of surface oxygen levels and animals. Geobiology, 18(3), 260-281. https://doi.org/10.1111/gbi.12382
Cook, S. D. C. (2010). New Zealand coastal marine invertebrates. Canterbury University Press.
Cornwall, C. E., Hepburn, C. D., Pilditch, C. A., & Hurd, C. L. (2013). Concentration boundary layers around complex assemblages of macroalgae: Implications for the effects of ocean acidification on understory coralline algae. Limnology and Oceanography, 58(1), 121-130. https://doi.org/10.4319/lo.2013.58.1.0121
De Zwaan, A., Cortesi, P., Van den Thillart, G., Roos, J., & Storey, K. B. (1991). Differential sensitivities to hypoxia by two anoxia-tolerant marine molluscs: A biochemical analysis. Marine Biology, 111(3), 343-351. https://doi.org/10.1007/bf01319405
Desai, D. V., & Prakash, S. (2009). Physiological responses to hypoxia and anoxia in Balanus amphitrite (Cirripedia: Thoracica). Marine Ecology Progress Series, 390, 157-166. https://doi.org/10.3354/meps08155
Diaz, R. J., & Breitburg, D. L. (2009). The hypoxic environment. In J. G. Richards, A. P. Farrell, & C. J. Brauner (Eds), Fish physiology (Vol. 27, pp. 1-23). Academic Press. https://doi.org/10.1016/b978-0-12-809633-8.03213-1
Diaz, R. J., & Rosenberg, R. (1995). Marine benthic hypoxia: A review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanography and Marine Biology, 33, 245-303.
Diaz, R. J., & Rosenberg, R. (2008). Spreading dead zones and consequences for marine ecosystems. Science, 321(5891), 926-929. https://doi.org/10.1126/science.1156401
Diaz, R. J., & Rosenberg, R. (2011). Introduction to environmental and economic consequences of hypoxia. International Journal of Water Resources Development, 27(1), 71-82. https://doi.org/10.1080/07900627.2010.531379
Dodds, L. A., Roberts, J. M., Taylor, A. C., & Marubini, F. (2007). Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxygen change. Journal of Experimental Marine Biology and Ecology, 349(2), 205-214. https://doi.org/10.1016/j.jembe.2007.05.013
Doney, S. C. (2010). The growing human footprint on coastal and open-ocean biogeochemistry. Science, 328(5985), 1512-1516. https://doi.org/10.1126/science.1185198
Ellington, W. R. (1982). Metabolic responses of the sea anemone Bunodosoma cavernata (Bosc) to declining oxygen tensions and anoxia. Physiological Zoology, 55(3), 240-249. https://doi.org/10.1086/physzool.55.3.30157888
Frieder, C. A., Nam, S. H., Martz, T. R., & Levin, L. A. (2012). High temporal and spatial variability of dissolved oxygen and pH in a nearshore California kelp forest. Biogeosciences, 9(10), 3917-3930. https://doi.org/10.5194/bg-9-3917-2012
Gobler, C. J., & Baumann, H. (2016). Hypoxia and acidification in ocean ecosystems: Coupled dynamics and effects on marine life. Biology Letters, 12(5), 20150976. https://doi.org/10.1098/rsbl.2015.0976
Goldstein, J., Riisgård, H. U., & Larsen, P. S. (2019). Exhalant jet speed of single-osculum explants of the demosponge Halichondria panicea and basic properties of the sponge-pump. Journal of Experimental Marine Biology and Ecology, 511, 82-90. https://doi.org/10.1016/j.jembe.2018.11.009
Gruber, R. K., Lowe, R. J., & Falter, J. L. (2017). Metabolism of a tide-dominated reef platform subject to extreme diel temperature and oxygen variations. Limnology and Oceanography, 62(4), 1701-1717. https://doi.org/10.1002/lno.10527
Haas, A. F., Smith, J. E., Thompson, M., & Deheyn, D. D. (2014). Effects of reduced dissolved oxygen concentrations on physiology and fluorescence of hermatypic corals and benthic algae. PeerJ, 2, e235. https://doi.org/10.7717/peerj.235
Hagerman, L. (1998). Physiological flexibility; a necessity for life in anoxic and sulphidic habitats. Hydrobiologia, 375, 241-254. https://doi.org/10.1007/978-94-017-2864-5_20
Hentschel, U., Fieseler, L., Wehrl, M., Gernert, C., Steinert, M., Hacker, J., & Horn, M. (2003). Microbial diversity of marine sponges. In W. E. G. Müller (Ed.), Progress in molecular and subcellular biology. Sponges (Porifera) (pp. 59-88). Springer. https://doi.org/10.1007/978-3-642-55519-0_3
Hentschel, U., Usher, K. M., & Taylor, M. W. (2006). Marine sponges as microbial fermenters. FEMS Microbiology Ecology, 55(2), 167-177. https://doi.org/10.1111/j.1574-6941.2005.00046.x
Hervé, M. (2021). RVAideMemoire: Testing and plotting procedures for biostatistics. R package version 0.9-79. https://cran.r-project.org/web/packages/RVAideMemoire/index.html
Hochachka, P. W., & Lutz, P. L. (2001). Mechanism, origin, and evolution of anoxia tolerance in animals. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 130(4), 435-459. https://doi.org/10.1016/s1096-4959(01)00408-0
Hoffmann, F., Larsen, O., Thiel, V., Rapp, H. T., Pape, T., Michaelis, W., & Reitner, J. (2005). An anaerobic world in sponges. Geomicrobiology Journal, 22(1-2), 1-10. https://doi.org/10.1080/01490450590922505
Hughes, D. J., Alderdice, R., Cooney, C., Kühl, M., Pernice, M., Voolstra, C. R., & Suggett, D. J. (2020). Coral reef survival under accelerating ocean deoxygenation. Nature Climate Change, 10(4), 296-307. https://doi.org/10.1038/s41558-020-0737-9
IPCC. (2021). Summary for policymakers. In V. Masson-Delmotte, P. Zhai, A. Pirani, S. L. Connors, C. Péan, S. Berger, N. Caud, Y. Chen, L. Goldfarb, M. I. Gomis, M. Huang, K. Leitzell, E. Lonnoy, J. B. R. Matthews, T. K. Maycock, T. Waterfield, O. Yelekçi, R. Yu, & B. Zhou (Eds.), Climate change 2021: The physical science basis. Contribution of working group I to the sixth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press. In press.
Johnson, M. D., Rodriguez, L. M., & Altieri, A. H. (2018). Shallow-water hypoxia and mass mortality on a Caribbean coral reef. Bulletin of Marine Science, 94(1), 143-144. https://doi.org/10.5343/bms.2017.1163
Johnson, P. D., & McMahon, R. F. (1998). Effects of temperature and chronic hypoxia on survivorship of the zebra mussel (Dreissena polymorpha) and Asian clam (Corbicula fluminea). Canadian Journal of Fisheries and Aquatic Sciences, 55(7), 1564-1572. https://doi.org/10.1139/f98-030
Kamke, J., Taylor, M. W., & Schmitt, S. (2010). Activity profiles for marine sponge-associated bacteria obtained by 16S rRNA vs 16S rRNA gene comparisons. The ISME Journal, 4(4), 498-508. https://doi.org/10.1038/ismej.2009.143
Kealoha, A. K., Doyle, S. M., Shamberger, K. E., Sylvan, J. B., Hetland, R. D., & Di Marco, S. F. (2020). Localized hypoxia may have caused coral reef mortality at the Flower Garden Banks. Coral Reefs, 39(1), 119-132. https://doi.org/10.1007/s00338-019-01883-9
Keeling, R. F., Körtzinger, A., & Gruber, N. (2010). Ocean deoxygenation in a warming world. Annual Review of Marine Science, 2, 199-229. https://doi.org/10.1146/annurev.marine.010908.163855
Kroeker, K. J., Bell, L. E., Donham, E. M., Hoshijima, U., Lummis, S., Toy, J. A., & Willis-Norton, E. (2020). Ecological change in dynamic environments: Accounting for temporal environmental variability in studies of ocean change biology. Global Change Biology, 26(1), 54-67. https://doi.org/10.1111/gcb.14868
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. (2017). lmerTest package: Tests in linear mixed effects models. Journal of Statistical Software, 82(13), 1-26. https://doi.org/10.18637/jss.v082.i13
Lavy, A., Keren, R., Yahel, G., & Ilan, M. (2016). Intermittent hypoxia and prolonged suboxia measured in situ in a marine sponge. Frontiers in Marine Science, 3, 263. https://doi.org/10.3389/fmars.2016.00263
Lenth, R. (2021). emmeans: Estimated marginal means, aka least-squares means. R package version 1.6.0. https://CRAN.R-project.org/package=emmeans
Levin, L. A. (2003). Oxygen minimum zone benthos: Adaptation and community response to hypoxia. Oceanography and Marine Biology, 41, 1-45. https://doi.org/10.1201/9780203180570-3
Levin, L. A., & Breitburg, D. L. (2015). Linking coasts and seas to address ocean deoxygenation. Nature Climate Change, 5(5), 401-403. https://doi.org/10.1038/nclimate2595
Levin, L. A., Ekau, W., Gooday, A. J., Jorissen, F., Middelburg, J. J., Naqvi, S. W. A., Neira, C., Rabalais, N. N., & Zhang, J. (2009). Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences, 6(10), 2063-2098. https://doi.org/10.5194/bg-6-2063-2009
Levin, L. A., Huggett, C. L., & Wishner, K. F. (1991). Control of deep-sea benthic community structure by oxygen and organic-matter gradients in the eastern Pacific Ocean. Journal of Marine Research, 49(4), 763-800. https://doi.org/10.1357/002224091784995756
Leys, S. P., & Kahn, A. S. (2018). Oxygen and the energetic requirements of the first multicellular animals. Integrative and Comparative Biology, 58(4), 666-676. https://doi.org/10.1093/icb/icy051
Limburg, K. E., Breitburg, D., & Levin, L. A. (2017). Ocean deoxygenation-A climate-related problem. Frontiers in Ecology and the Environment, 15(9), 479. https://doi.org/10.1002/fee.1728
Love, G. D., Grosjean, E., Stalvies, C., Fike, D. A., Grotzinger, J. P., Bradley, A. S., Kelly, A. E., Bhatia, M., Meredith, W., Snape, C. E., Bowring, S. A., Condon, D. J., & Summons, R. E. (2009). Fossil steroids record the appearance of Demospongiae during the Cryogenian period. Nature, 457(7230), 718-721. https://doi.org/10.1038/nature07673
Lunden, J. J., McNicholl, C. G., Sears, C. R., Morrison, C. L., & Cordes, E. E. (2014). Acute survivorship of the deep-sea coral Lophelia pertusa from the Gulf of Mexico under acidification, warming, and deoxygenation. Frontiers in Marine Science, 1, 78. https://doi.org/10.3389/fmars.2014.00078
Maldonado, M., Ribes, M., & van Duyl, F. C. (2012). Nutrient fluxes through sponges: Biology, budgets, and ecological implications. Advances in Marine Biology, 62, 113-182. https://doi.org/10.1016/b978-0-12-394283-8.00003-5
Maloof, A. C., Rose, C. V., Beach, R., Samuels, B. M., Calmet, C. C., Erwin, D. H., Poirier, G. R., Yao, N., & Simons, F. J. (2010). Possible animal-body fossils in pre-Marinoan limestones from South Australia. Nature Geoscience, 3(9), 653-659. https://doi.org/10.1038/ngeo934
Mangum, D. C. (1980). Sea anemone neuromuscular responses in anaerobic conditions. Science, 208(4448), 1177-1178. https://doi.org/10.1126/science.6103580
McAllen, R., Davenport, J., Bredendieck, K., & Dunne, D. (2009). Seasonal structuring of a benthic community exposed to regular hypoxic events. Journal of Experimental Marine Biology and Ecology, 368(1), 67-74. https://doi.org/10.1016/j.jembe.2008.10.019
McAllen, R., Taylor, A. C., & Davenport, J. (1999). The effects of temperature and oxygen partial pressure on the rate of oxygen consumption of the high-shore rock pool copepod Tigriopus brevicornis. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 123(2), 195-202. https://doi.org/10.1016/s1095-6433(99)00050-1
Mentel, M., Röttger, M., Leys, S., Tielens, A. G., & Martin, W. F. (2014). Of early animals, anaerobic mitochondria, and a modern sponge. BioEssays, 36(10), 924-932. https://doi.org/10.1002/bies.201400060
Micaroni, V., McAllen, R., Turner, J., Strano, F., Morrow, C., Picton, B., Harman, L., & Bell, J. J. (2021). Vulnerability of Temperate Mesophotic Ecosystems (TMEs) to environmental impacts: Rapid ecosystem changes at Lough Hyne Marine Nature Reserve, Ireland. Science of the Total Environment, 789, 147708. https://doi.org/10.1016/j.scitotenv.2021.147708
Mills, D. B., Francis, W. R., Vargas, S., Larsen, M., Elemans, C. P., Canfield, D. E., & Wörheide, G. (2018). The last common ancestor of animals lacked the HIF pathway and respired in low-oxygen environments. Elife, 7, e31176. https://doi.org/10.7554/eLife.31176.001
Mills, D. B., Ward, L. M., Jones, C., Sweeten, B., Forth, M., Treusch, A. H., & Canfield, D. E. (2014). Oxygen requirements of the earliest animals. Proceedings of the National Academy of Sciences of the United States of America, 111(11), 4168-4172. https://doi.org/10.1073/pnas.1400547111
Milton, S. L., & Prentice, H. M. (2007). Beyond anoxia: The physiology of metabolic downregulation and recovery in the anoxia-tolerant turtle. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 147(2), 277-290. https://doi.org/10.1016/j.cbpa.2006.08.041
Moitinho-Silva, L., Steinert, G., Nielsen, S., Hardoim, C. C., Wu, Y. C., McCormack, G. P., López-Legentil, S., Marchant, R., Webster, N., Thomas, T., & Hentschel, U. (2017). Predicting the HMA-LMA status in marine sponges by machine learning. Frontiers in Microbiology, 8, 752. https://doi.org/10.3389/fmicb.2017.00752
Morganti, T. M., Ribes, M., Moskovich, R., Weisz, J. B., Yahel, G., & Coma, R. (2021). In situ pumping rate of 20 marine demosponges is a function of osculum area. Frontiers in Marine Science, 8, 583188. https://doi.org/10.3389/fmars.2021.583188
Morris, S., & Taylor, A. C. (1983). Diurnal and seasonal variation in physico-chemical conditions within intertidal rock pools. Estuarine, Coastal and Shelf Science, 17, 339-355. https://doi.org/10.1016/0272-7714(83)90026-4
Mosch, T., Sommer, S., Dengler, M., Noffke, A., Bohlen, L., Pfannkuche, O., Liebetrau, V., & Wallmann, K. (2012). Factors influencing the distribution of epibenthic megafauna across the Peruvian oxygen minimum zone. Deep Sea Research Part I: Oceanographic Research Papers, 68, 123-135. https://doi.org/10.1016/j.dsr.2012.04.014
Müller, M., Mentel, M., van Hellemond, J. J., Henze, K., Woehle, C., Gould, S. B., Yu, R. Y., van der Giezen, M., Tielens, A. G., & Martin, W. F. (2012). Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiology and Molecular Biology Reviews, 76(2), 444-495. https://doi.org/10.1128/MMBR.05024-11
Murty, S. J., Bett, B. J., & Gooday, A. J. (2009). Megafaunal responses to strong oxygen gradients on the Pakistan margin of the Arabian Sea. Deep Sea Research Part II: Topical Studies in Oceanography, 56(6-7), 472-487. https://doi.org/10.1016/j.dsr2.2008.05.029
Nagasoe, S., Tokunaga, T., Yurimoto, T., & Matsuyama, Y. (2020). Survival and behavior patterns associated with hypoxia at different life stages of the pen shell Atrina cf. japonica. Aquatic Toxicology, 227, 105610. https://doi.org/10.1016/j.aquatox.2020.105610
Nezlin, N. P., Kamer, K., Hyde, J., & Stein, E. D. (2009). Dissolved oxygen dynamics in a eutrophic estuary, Upper Newport Bay, California. Estuarine, Coastal and Shelf Science, 82(1), 139-151. https://doi.org/10.1016/j.ecss.2009.01.004
Nilsson, G. E., & Renshaw, G. M. (2004). Hypoxic survival strategies in two fishes: Extreme anoxia tolerance in the North European crucian carp and natural hypoxic preconditioning in a coral-reef shark. Journal of Experimental Biology, 207(18), 3131-3139. https://doi.org/10.1242/jeb.00979
Nixon, S. W. (1995). Coastal marine eutrophication: A definition, social causes, and future concerns. Ophelia, 41(1), 199-219. https://doi.org/10.1080/00785236.1995.10422044
Osinga, R., Tramper, J., & Wijffels, R. H. (1999). Cultivation of marine sponges. Marine Biotechnology, 1(6), 509-532. https://doi.org/10.1007/PL00011807
Piazzi, L., Atzori, F., Cadoni, N., Cinti, M. F., Frau, F., Pansini, A., Pinna, F., Stipcich, P., & Ceccherelli, G. (2021). Animal forest mortality: Following the consequences of a gorgonian coral loss on a mediterranean coralligenous assemblage. Diversity, 13(3), 133. https://doi.org/10.3390/d13030133
Pinheiro, J., Bates, D., DebRoy, S., & Sarkar, D., & R Core Team. (2021). nlme: Linear and nonlinear mixed effects models. R package version 3.1-152. https://CRAN.R-project.org/package=nlme
R Core Team. (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Rao, D. P., & Ganapati, P. N. (1968). Respiration as a function of oxygen concentration in intertidal barnacles. Marine Biology, 1(4), 309-310. https://doi.org/10.1007/BF00360781
Raupach, M. R., & Canadell, J. G. (2010). Carbon and the Anthropocene. Current Opinion in Environmental Sustainability, 2(4), 210-218. https://doi.org/10.1016/j.cosust.2010.04.003
Robinson, C. (2019). Microbial respiration, the engine of ocean deoxygenation. Frontiers in Marine Science, 5, 533. https://doi.org/10.3389/fmars.2018.00533
Sampaio, E., Santos, C., Rosa, I. C., Ferreira, V., Pörtner, H. O., Duarte, C. M., Levin, L. A., & Rosa, R. (2021). Impacts of hypoxic events surpass those of future ocean warming and acidification. Nature Ecology & Evolution, 5(3), 311-321. https://doi.org/10.1038/s41559-020-01370-3
Sarà, M., Sarà, A., Nickel, M., & Brümmer, F. (2001). Three new species of Tethya (Porifera: Demospongiae) from German Aquaria. Stuttgarter Beiträge zur Naturkunde, 631, 1-15.
Sassaman, C., & Mangum, C. P. (1972). Adaptations to environmental oxygen levels in infaunal and epifaunal sea anemones. The Biological Bulletin, 143(3), 657-678. https://doi.org/10.2307/1540189
Schuster, A., Strehlow, B. W., Eckford-Soper, L., McAllen, R., & Canfield, D. E. (2021). Effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake in Lough Hyne, Ireland. Msphere, 6(1), e00991-e1020. https://doi.org/10.1101/2020.09.09.290791
Seibel, B. A. (2011). Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones. Journal of Experimental Biology, 214(2), 326-336. https://doi.org/10.1242/jeb.049171
Semenza, G. L. (2007). Life with oxygen. Science, 318(5847), 62-64. https://doi.org/10.1126/science.1147949
Smith, V. H., Joye, S. B., & Howarth, R. W. (2006). Eutrophication of freshwater and marine ecosystems. Limnology and Oceanography, 51, 351-355. https://doi.org/10.1007/978-90-481-3385-7_1
Stachowitsch, M. (1984). Mass mortality in the Gulf of Trieste: The course of community destruction. Marine Ecology, 5(3), 243-264. https://doi.org/10.1111/j.1439-0485.1984.tb00124.x
Steckbauer, A., Klein, S. G., & Duarte, C. M. (2020). Additive impacts of deoxygenation and acidification threaten marine biota. Global Change Biology, 26(10), 5602-5612. https://doi.org/10.1111/gcb.15252
Stickle, W. B., Kapper, M. A., Liu, L. L., Gnaiger, E., & Wang, S. Y. (1989). Metabolic adaptations of several species of crustaceans and molluscs to hypoxia: Tolerance and microcalorimetric studies. The Biological Bulletin, 177(2), 303-312. https://doi.org/10.2307/1541945
Strano, F., Micaroni, V., Davy, S. K., Maldonado, M., & Bell, J. J. (2021). Reproduction and early life stages of the poecilosclerid sponge Crella incrustans. Invertebrate Biology, e12335, https://doi.org/10.1111/ivb.12335
Therneau, T. (2021). A package for survival analysis in R. R package version 3.2-10. https://CRAN.R-project.org/package=survival
Thomassen, S., & Riisgård, H. U. (1995). Growth and energetics of the sponge Halichondria panicea. Marine Ecology Progress Series, 128, 239-246. https://doi.org/10.3354/meps128239
Thuesen, E. V., Rutherford, L. D. Jr, & Brommer, P. L. (2005). The role of aerobic metabolism and intragel oxygen in hypoxia tolerance of three ctenophores: Pleurobrachia bachei, Bolinopsis infundibulum and Mnemiopsis leidyi. Journal of the Marine Biological Association of the United Kingdom, 85(3), 627. https://doi.org/10.1017/s0025315405011550
Trowbridge, C. D., Davenport, J., Cottrell, D. M., Harman, L., Plowman, C. Q., Little, C., & McAllen, R. (2017). Extreme oxygen dynamics in shallow water of a fully marine Irish sea lough. Regional Studies in Marine Science, 11, 9-16. https://doi.org/10.1016/j.rsma.2017.01.008
Turner, E. C. (2021). Possible poriferan body fossils in early Neoproterozoic microbial reefs. Nature, 596, 87-91. https://doi.org/10.1038/s41586-021-03773-z
Vacelet, J. (1975). Étude en microscopie électronique de l'association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). Journal de Microscopie et de Biologie Cellulaire, 23, 271-288.
Vaquer-Sunyer, R., & Duarte, C. M. (2008). Thresholds of hypoxia for marine biodiversity. Proceedings of the National Academy of Sciences of the United States of America, 105(40), 15452-15457. https://doi.org/10.1073/pnas.0803833105
Vaquer-Sunyer, R., & Duarte, C. M. (2010). Sulfide exposure accelerates hypoxia-driven mortality. Limnology and Oceanography, 55(3), 1075-1082. https://doi.org/10.4319/lo.2010.55.3.1075
Vaquer-Sunyer, R., & Duarte, C. M. (2011). Temperature effects on oxygen thresholds for hypoxia in marine benthic organisms. Global Change Biology, 17(5), 1788-1797. https://doi.org/10.1111/j.1365-2486.2010.02343.x
Vergés, A., McCosker, E., Mayer-Pinto, M., Coleman, M. A., Wernberg, T., Ainsworth, T., & Steinberg, P. D. (2019). Tropicalisation of temperate reefs: Implications for ecosystem functions and management actions. Functional Ecology, 33(6), 1000-1013. https://doi.org/10.1111/1365-2435.13310
Vornanen, M., Stecyk, J. A., & Nilsson, G. E. (2009). The anoxia-tolerant crucian carp (Carassius carassius L.). In J. Richards, A. Farrell & C. Brauner (Eds.), Fish physiology: Hypoxia (Vol. 27, pp. 397-441). Academic Press. https://doi.org/10.1016/s1546-5098(08)00009-5
Whelan, N. V., Kocot, K. M., Moroz, T. P., Mukherjee, K., Williams, P., Paulay, G., Moroz, L. L., & Halanych, K. M. (2017). Ctenophore relationships and their placement as the sister group to all other animals. Nature Ecology & Evolution, 1(11), 1737-1746. https://doi.org/10.1038/s41559-017-0331-3
Wishner, K. F., Ashjian, C. J., Gelfman, C., Gowing, M. M., Kann, L., Levin, L. A., Mullineaux, L. S., & Saltzman, J. (1995). Pelagic and benthic ecology of the lower interface of the Eastern Tropical Pacific oxygen minimum zone. Deep Sea Research Part I: Oceanographic Research Papers, 42(1), 93-115. https://doi.org/10.1016/0967-0637(94)00021-j
Woo, S., Denis, V., Won, H., Shin, K., Lee, G., Lee, T. K., & Yum, S. (2013). Expressions of oxidative stress-related genes and antioxidant enzyme activities in Mytilus galloprovincialis (Bivalvia, Mollusca) exposed to hypoxia. Zoological Studies, 52(1), 1-8. https://doi.org/10.1186/1810-522x-52-15
Woodhead, A. J., Hicks, C. C., Norström, A. V., Williams, G. J., & Graham, N. A. (2019). Coral reef ecosystem services in the Anthropocene. Functional Ecology, 33(6), 1023-1034. https://doi.org/10.1111/1365-2435.13331
Wulff, J. L. (2006). Ecological interactions of marine sponges. Canadian Journal of Zoology, 84(2), 146-166. https://doi.org/10.1139/z06-019
Yahel, G., Marie, D., & Genin, A. (2005). InEx-A direct in situ method to measure filtration rates, nutrition, and metabolism of active suspension feeders. Limnology and Oceanography: Methods, 3(2), 46-58. https://doi.org/10.4319/lom.2005.3.46