Impaired growth and survival of tropical macroalgae (Sargassum spp.) at elevated temperatures
Tóm tắt
Increasing ocean temperatures associated with ongoing climate change have resulted in regional reductions in the cover of live coral and increasing concerns that coral reefs will be overgrown by macroalgae. The likelihood of macroalgal overgrowth will, however, depend on the thermal sensitivities of the macroalgae themselves. We exposed recently settled propagules of the common canopy-forming macroalga Sargassum swartzii and adult thalli of three species of Sargassum (S. swatzii, S. cristaefolium, S. polycystum) to three experimental temperatures: ambient, + 2 °C, and + 3.5 °C, reflective of summer minimum, mean, and maximum temperatures for the region. Growth and survival of Sargassum swartzii propagules were assessed over 48 days, and the growth, physical toughness, elemental composition, and susceptibility to herbivory of adult thalli were assessed after short-term exposure (2-weeks) to experimental temperatures. Growth and survival of S. swartzii propagules were reduced by 43% and 84%, respectively, when cultured at the elevated (+ 3.5 °C) temperature compared to ambient temperature. Similarly, elevated temperature resulted in a 17–49% decline in the growth of adult Sargassum thalli relative to controls. Susceptability of S. swartzii and S. cristaefolium to herbivory (i.e. mass removed by herbivores) was 50% less for thalli cultured at elevated (+ 3.5 °C) compared to ambient temperature, but this pattern was not related to changes in the physical or chemical properties of the thalli as a result of elevated temperature. The negative effects of elevated temperatures on the growth and survival of both Sargassum propagules and adult thalli will likely restrict the capacity of Sargassum, and potentially other macroalgae, to establish in new areas, and may also threaten the persistence of existing macroalgal meadows under future ocean temperatures. The thermal sensitivities of tropical Sargassum, together with those of corals, suggest ongoing ocean warming may lead to novel reef ecosystems that are low in both coral cover and macroalgal cover.
Tài liệu tham khảo
Alestra T, Schiel DR (2015) Impacts of local and global stressors in intertidal habitats: Influence of altered nutrient, sediment and temperature levels on the early life history of three habitat-forming macroalgae. J Exp Mar Bio Ecol 468:29–36
Anderson BC (2006) Response of tropical marine macroalgae to thermal stress. MS Thesis. Florida Atlantic University, Boca Raton, FL
Andrews S, Bennett S, Wernberg T (2014) Reproductive seasonality and early life temperature sensitivity reflect vulnerability of a seaweed undergoing range reduction. Mar Ecol Prog Ser 495:119–129
Australian Institute of Marine Science (AIMS) (2018) Daily Average Ocean Water Temperatures Against Long Term Average Water Temperature. http://data.aims.gov.au/aimsrtds/yearlytrends.xhtml
Baird AH, Marshall PA (2002) Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar Ecol Prog Ser 237:133–141
Bartón K (2018) MuMIN: Multi-Model Inference
Bates AE, Pecl GT, Frusher S, Hobday AJ, Wernberg T, Smale DA, Sunday JM, Hill NA, Dulvy NK, Colwell RK, Holbrook NJ, Fulton EA, Slawinski D, Feng M, Edgar GJ, Radford BT, Thompson PA, Watson RA (2014) Defining and observing stages of climate-mediated range shifts in marine systems. Glob Environ Chang 26:27–38
Bates D, Machler M, Bolker B, Walker S (2015) Fitting linear mixed effects models using lme4. J Stat Softw 67:1–48
Bauman AG, Hoey AS, Dunshea G, Feary DA, Low J, Todd PA (2017) Macroalgal browsing on a heavily degraded, urbanized equatorial reef system. Sci Rep 7:1–8
Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Curr Biol 16:2434–2439
Bento R, Hoey AS, Bauman AG, Feary DA, Burt JA (2016) The implications of recurrent disturbances within the world’s hottest coral reef. Mar Pollut Bull 105:466–472
Berumen ML, Pratchett MS (2006) Recovery without resilience: Persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25:647–653
Bonaldo RM, Pires MM, Guimarã PR, Hoey AS, Hay ME (2017) Small marine protected areas in Fiji provide refuge for reef fish assemblages, feeding groups, and corals. PLoS one 12
Brown JH, Gilooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789
Bruno JF, Carr LA, O’Connor MI (2015) Exploring the role of temperature in the ocean through metabolic scaling. Ecology 96:3126–3140
Campbell AH, Harder T, Nielsen S, Kjelleberg S, Steinberg PD (2011) Climate change and disease: Bleaching of a chemically defended seaweed. Glob Chang Biol 17:2958–2970
Choat JH, Clements KD (1998) Vertebrate herbivores in marine and terrestrial environments: A nutritional ecology perspective. Annu Rev Ecol Syst 29:375–403
Chong-Seng KM, Nash KL, Bellwood DR, Graham NAJ (2014) Macroalgal herbivory on recovering versus degrading coral reefs. Coral Reefs 33:409–419
Chu SH, Zhang QS, Liu SK, Tang YZ, Zhang SB, Lu ZC, Yu YQ (2012) Tolerance of Sargassum thunbergii germlings to thermal, osmotic and desiccation stress. Aquat Bot 96:1–6
Clark JS, Poore AGB, Doblin MA (2018) Shaping up for stress: Physiological flexibility is key to survivorship in a habitat-forming macroalga. J Plant Physiol 231:346–355
Clements KD, Raubenheimer D, Choat JH (2009) Nutritional ecology of marine herbivorous fishes: Ten years on. Funct Ecol 23:79–92
Cronin G, Hay ME (1996) Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds. Oikos 77:93
de Bettignies T, Wernberg T, Gurgel CFD (2018) Exploring the influence of temperature on aspects of the reproductive phenology of temperate seaweeds. Front Mar Sci 5
Dell AI, Pawar S, Savage VM (2011) Systematic variation in the temperature dependence of physiological and ecological traits. Proc Natl Acad Sci 108:10591–10596
Diaz-pulido G, McCook LJ (2002) The fate of bleached corals: patterns and dynamics of algal recruitment. Mar Ecol Prog Ser 232:115–128
Diaz-Pulido G, McCook LJ (2003) Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84:2026–2033
Duffy JE, Hay ME (1991) Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72:1286–1298
Forrester GE (1995) Strong density-dependent survival and recruitment regulate the abundance of a coral reef fish. Oecologia 103:275–282
Frieler K, Meinshausen M, Golly A, Mengel M, Lebek K, Donner SD, Hoegh-Guldberg O (2013) Limiting global warming to 2°C is unlikely to save most coral reefs. Nat Clim Chang 3:165–170
Froese R, Pauly D (2018) FishBase. http://www.fishbase.org
Graba-Landry A, Sheppard-Brennand H, Dworjanyn SA, Hoey AS, Matley JK, Poore AGB, Byrne M (2018) Ocean warming has greater and more consistent negative effects than ocean acidification on the growth and health of subtropical macroalgae. Mar Ecol Prog Ser 595:55–69
Graham NAJ, Jennings S, MacNeil MA, Mouillot D, Wilson SK (2015) Predicting climate-driven regime shifts versus rebound potential in coral reefs. Nature 518:94–97
Guiry MD, Guiry MD (2020) Algaebase. Worldwide electronic publication, National University of Ireland, Galway. algaebase.org
Hanisak MD (1993) Nitrogen release from decomposing seaweeds: species and temperature effects. J Appl Phycol 5:175–181
Harborne AR (2013) The ecology, behaviour and physiology of fishes on coral reef flats, and the potential impacts of climate change. J Fish Biol 83:417–447
Hawlena D, Schmitz OJ (2010) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci 107:15503–15507
Henkel SK, Hofmann GE (2008) Differing patterns of hsp70 gene expression in invasive and native kelp species: Evidence for acclimation-induced variation. J Appl Phycol 20:915–924
Hoey AS (2010) Size matters: Macroalgal height influences the feeding response of coral reef herbivores. Mar Ecol Prog Ser 411:299–302
Hoey AS, Bellwood DR (2009) Limited functional redundancy in a high diversity system: Single species dominates key ecological process on coral reefs. Ecosystems 12:1316–1328
Hoey AS, Bellwood DR (2010) Cross-shelf variation in browsing intensity on the Great Barrier Reef. Coral Reefs 29:499–508
Hoey AS, Brandl SJ, Bellwood DR (2013) Diet and cross-shelf distribution of rabbitfishes (f. Siganidae) on the northern Great Barrier Reef: Implications for ecosystem function. Coral Reefs 32:973–984
Hoey AS, Howells E, Johansen JL, Hobbs JPA, Messmer V, McCowan DM, Wilson SK, Pratchett MS (2016) Recent advances in understanding the effects of climate change on coral reefs. Diversity 8
Huey RB, Stevenson R (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19:357–366
Hughes TP, Anderson KD, Connolly SR, Heron SF, Kerry JT, Lough JM, Baird AH, Baum JK, Berumen ML, Bridge TC, Claar DC, Eakin MC, Gilmour JP, Graham NAJ, Harrison HB, Hobbs J-PA, Hoey AS, Hoogenboom MO, Lowe RJ, McCulloch MT, Pandolfi JM, Pratchett MS, Schoepf V, Torda G, Wilson SK (2018a) Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359:80–83
Hughes TP, Connolly SR, Eakin CM, Dietzel A, McWilliam MJ, Hoey AS, Pears RJ, Liu G, Skirving WJ, Heron SF, Pratchett MS, Baird AH, Stella JS, Hoogenboom MO, Torda G, Kerry JT (2018b) Global warming transforms coral reef assemblages. Nature 556:492–496
Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC, Butler IR, Byrne M, Cantin NE, Comeau S, Connolly SR, Cumming GS, Dalton SJ, Diaz-Pulido G, Eakin CM, Figueira WF, Gilmour JP, Harrison HB, Heron SF, Hoey AS, Hobbs JPA, Hoogenboom MO, Kennedy EV, Kuo CY, Lough JM, Lowe RJ, Liu G, McCulloch MT, Malcolm HA, McWilliam MJ, Pandolfi JM, Pears RJ, Pratchett MS, Schoepf V, Simpson T, Skirving WJ, Sommer B, Torda G, Wachenfeld DR, Willis BL, Wilson SK (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377
Hughes TP, Kerry JT, Baird AH, Connolly SR, Chase TJ, Dietzel A, Hill T, Hoey AS, Hoogenboom MO, Jacobson M, Kerswell A, Madin JS, Mieog A, Paley AS, Pratchett MS, Torda G, Woods RM (2019) Global warming impairs stock–recruitment dynamics of corals. Nature 568:387–390
Hughes TP, Rodrigues MJ, Bellwood DR, Ceccarelli D, Hoegh-Guldberg O, McCook L, Moltschaniwskyj N, Pratchett MS, Steneck RS, Willis B (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365
Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Annu Rev Ecol Syst 22:477–503
Jokiel PL, Coles SL (1990) Coral Reefs to elevated temperature. Environ Conserv 8:155–162
Kendrick GA, Walker DI (1995) Dispersal of propagules of Sargassum spp. (Sargassaceae: Phaeophyta): Observations of local patterns of dispersal and consequences for recruitment and population structure. J Exp Mar Bio Ecol 192:273–288
King NG, McKeown NJ, Smale DA, Wilcockson DC, Hoelters L, Groves EA, Stamp T, Moore PJ (2019) Evidence for different thermal ecotypes in range centre and trailing edge kelp populations. J Exp Mar Bio Ecol 514–515:10–17
Koch M, Bowes G, Ross C, Zhang XH (2013) Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob Chang Biol 19:103–132
Lee TC, Hsu BD (2009) Disintegration of the cells of siphonous green alga Codium edule (bryopsidales, chlorophyta) under mild heat stress. J Phycol 45:348–356
Lefévre CD, Bellwood DR (2011) Temporal variation in coral reef ecosystem processes: Herbivory of macroalgae by fishes. Mar Ecol Prog Ser 422:239–251
Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef. Ecol Monogr 56:183–200
Ling SD, Scheibling RE, Rassweiler A, Johnson CR, Shears N, Connell SD, Salomon AK, Norderhaug KM, Pérez-Matus A, Hernández JC, Clemente S, Blamey LK, Hereu B, Ballesteros E, Sala E, Garrabou J, Cebrian E, Zabala M, Fujita D, Johnson LE (2015) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos Trans R Soc B Biol Sci 370:1–10
Lough JM (2012) Small change, big difference: Sea surface temperature distributions for tropical coral reef ecosystems, 1950-2011. J Geophys Res Ocean 117
Lüning K (1988) Photoperiodic control of sorus formation in the brown alga Laminaria saccarina. Mar Ecol Prog Ser 45:137–144
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161
McCourt RM (1984) Seasonal patterns of abundance, distributions, and pheology in relation to growth strategies of three Sargassum species. J Exp Mar Bio Ecol 74:141–156
O’Neil JM, Capone DG (2008) Nitrogen Cycling in Coral Reef Environments
Oliver ECJ, Donat MG, Burrows MT, Moore PJ, Smale DA, Alexander LV, Benthuysen JA, Feng M, Sen Gupta A, Hobday AJ, Holbrook NJ, Perkins-Kirkpatrick SE, Scannell HA, Straub SC, Wernberg T (2018) Longer and more frequent marine heatwaves over the past century. Nat Commun 9:1–12
Payri CE, Naim O (1982) Variations entre 1971 et 1980 de la biomasse et de la composition des populations de macroalgues sur le récif corallien de Tiahura (île de Moorea, Polynésie française). Cryptogamie 3:229–240
Pessarrodona A, Moore PJ, Sayer MDJ, Smale DA (2018) Carbon assimilation and transfer through kelp forests in the NE Atlantic is diminished under a warmer ocean climate. Glob Chang Biol 24:4386–4398
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2018) nlme: Linear and nonlinear mixed effects models
Pinsky ML, Eikeset AM, McCauley DJ, Payne JL, Sunday JM (2019) Greater vulnerability to warming of marine versus terrestrial ectotherms. Nature 569:108–112
Poore AGB, Graba-Landry A, Favret M, Sheppard Brennand H, Byrne M, Dworjanyn SA (2013) Direct and indirect effects of ocean acidification and warming on a marine plant-herbivore interaction. Oecologia 173:1113–1124
Poore AGB, Graham SE, Byrne M, Dworjanyn SA (2016) Effects of ocean warming and lowered pH on algal growth and palatability to a grazing gastropod. Mar Biol 163
Rasher DB, Hoey AS, Hay ME (2013) Consumer diversity interacts with prey defenses to drive ecosystem function. Ecology 94:1347–1358
Sakanishi Y, Kasai H, Tanaka J (2017) Trade-off relationship between productivity and thallus toughness in Laminariales (Phaeophyceae). Phycol Res 65:103–110
Steinberg P, Paul V (1990) Fish feeding and chemical defenses of tropical brown algae in Western Australia. Mar Ecol Prog Ser 58:253–259
Sudatti DB, Fujii MT, Rodrigues SV, Turra A, Pereira RC (2011) Effects of abiotic factors on growth and chemical defenses in cultivated clones of Laurencia dendroidea J. Agardh (Ceramiales, Rhodophyta). Mar Biol 158:1439–1446
Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nat Clim Chang 2:686–690
Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the heat on tropical animals. Science 320:1296–1297
Thimijan RW, Heins RD (1982) Photometric, Radiometric, and Quantum Light Units of Measure: A Review of Procedures for Interconversion. HortScience 18:818–822
Trono CGJ (1998) Seaweeds. In: Carpenter KE, Neim VH (eds) FAO Species Identification Guide for Fishery Purposes: The Living Marine Resources of the Western Central Pacific, vol 1. Seaweeds, corals, bivalves and gastropods. Food and Agriculture Organization of the United Nations, Rome, pp 66–76
Vergés A, Tomas F, Cebrian E, Ballesteros E, Kizilkaya Z, Dendrinos P, Karamanlidis AA, Spiegel D, Sala E (2014) Tropical rabbitfish and the deforestation of a warming temperate sea. J Ecol 102:1518–1527
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee T, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395
Webster NS, Soo R, Cobb R, Negri AP (2011) Elevated seawater temperature causes a microbial shift on crustose coralline algae with implications for the recruitment of coral larvae. ISME J 5:759–770
Wernberg T, Smale DA, Thomsen MS (2012) A decade of climate change experiments on marine organisms: Procedures, patterns and problems. Glob Chang Biol 18:1491–1498
Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, De Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Chang 3:78–82