Ocean warming and increasing incidence of marine heatwaves (MHW) challenge the survival of marine organisms. While the impacts of climate scenario-based ocean warming are well investigated, the response of organisms to extreme events such as MHW is less understood. In this study, the thermal tolerance of the amphipod Hyale niger, an ecologically important amphipod in southeast Australia, and its algal host Sargassum linearifolium, were determined. For H. niger, a broad temperature range (2–33 °C) was tested in 6-day exposures in three seasons (summer, autumn and winter) and extended to 11 days in summer. Despite the 7 °C difference in mean habitat temperature across seasons, H. niger had a similar broad thermal optimum (Topt) range with ≥ 90% survival across a 17–20 degree temperature range. The upper lethal temperature with 50% mortality in the 6-day tests was also similar across seasons (LT50 29–30 °C). In 11-day tests in summer, the LT50 was reduced to 26 °C. Cold tolerance of H. niger indicated potential for poleward migration. Sargassum linearifolium had a similar broad thermal tolerance with a 50% reduction in the photosynthetic capacity at 33 °C. Temperature significantly affected survival of H. niger depending on the size and sex. The decrease in the Topt range over time pointed to the deleterious influence of prolonged heatwaves. The broad thermal tolerance of H. niger and S. linearifolium suggests that this important amphipod–host system may be resilient to habitat warming.
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Angilletta MJ Jr, Angilletta MJ (2009) Thermal adaptation: a theoretical and empirical synthesis. Oxford University Press, Oxford
Angilletta MJ Jr, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509
Babcock RC, Bustamante RH, Fulton EA, Fulton DJ, Haywood MD, Hobday AJ, Kenyon R, Matear RJ, Plagányi EE, Richardson AJ, Vanderklift MA (2019) Severe continental-scale impacts of climate change are happening now: extreme climate events impact marine habitat forming communities along 45% of Australia’s coast. Front Mar Sci 6:411
Bible JM, Evans TG, Sanford E (2020) Differences in induced thermotolerance among populations of Olympia oysters. Mol Integr Physiol (CBPA) 239:110563
Bij de Vaate A (2001) Oxygen consumption, temperature and salinity tolerance of the invasive amphipod Dikerogammarus villosus: indicators of further dispersal via ballast water transport. Arch Hydrobiol 152:633–646
Booth DJ, Figueira WF, Gregson MA, Brown L, Beretta G (2007) Occurrence of tropical fishes in temperate southeastern Australia: role of the East Australian Current. Estuar Coast Shelf Sci 72:102–114
Bui HT, Luu TQ, Fotedar R (2018) Effects of temperature and pH on the growth of Sargassum linearifolium and S. Podacanthum in potassium-fortified inland saline water. Am J of Appl Sci 15:186–197
Cardoso PG, Loganimoce EM, Neuparth T, Rocha MJ, Rocha E, Arenas F (2018) Interactive effects of increased temperature, pCO2 and the synthetic progestin levonorgestrel on the fitness and breeding of the amphipod Gammarus locusta. Environ Pollut 236:937–947
Coleman MA, Wernberg T (2017) Forgotten underwater forests: the key role of fucoids on Australian temperate reefs. Ecol evol 7:8406–8418
Collin R, Rendina F, Goodwin V, McCabe S (2018) Do tropical specialist sea urchins have higher thermal tolerances and optimal temperatures than their more widely distributed relatives? Mar Ecol Prog Ser 589:153–166
Collins MR, Knutti J, Arblaster JL, Dufresne T, Fichefet P, Friedlinstein X, Gao WJ, Gutowski T, Johns G, Krinner M, Shongwe C, Tebaldi AJ, Weaver MW (2013) Long-term climate change: projections, commitments and irreversibility. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Cox DR (1992) Regression models and life-tables. Breakthroughs in statistics. Springer, New York, pp 527–541
Dallas HF, Ketley ZA (2011) Upper thermal limits of aquatic macroinvertebrates: comparing critical thermal maxima with 96-LT50 values. J Therm Biol 36:322–327
Dauby P, Nyssen F, De Broyer C (2003) Amphipods as food sources for higher trophic levels in the Southern Ocean: a synthesis. Antarctic Biology in a Global Context. Backhuys Publishers, Leiden, pp 129–134
Daufresne M, Lengfellner K, Sommer U (2009) Global warming benefits the small in aquatic ecosystems. Proc Natl Acad Sci 106:12788–12793
Duffy JE, Hay ME (1991) Food and shelter as determinants of food choice by an herbivorous marine amphipod. Ecology 72:1286–1298
Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237–263
Figueira WF, Booth DJ (2010) Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Glob Change Biol 16:506–516
Fisher LD, Lin DY (1999) Time-dependent covariates in the Cox proportional-hazards regression model. Annu Rev Public Health 20:145–157
Frölicher TL, Fischer EM, Gruber N (2018) Marine heatwaves under global warming. Nature 560:360
Galic N, Forbes VE (2017) Effects of temperature on the performance of a freshwater amphipod. Hydrobiologia 785:35–46
Gaylord B, Barclay KM, Jellison BM, Jurgens LJ, Ninokawa AT, Rivest EB, Leighton LR (2019) Ocean change within shoreline communities: from biomechanics to behaviour and beyond. Conserv Physiol 7:77
Gillooly JF, Brown JH, West GB, Savage VM, Charnov EL (2001) Effects of size and temperature on metabolic rate. Science 293:2248–2251
Halcrow K, Boyd CM (1967) The oxygen consumption and swimming activity of the amphipod Gammarus oceanicus at different temperatures. Comp Biochem Phys 23:233–242
Harianto J, Nguyen HD, Holmes SP, Byrne M (2018) The effect of warming on mortality, metabolic rate, heat-shock protein response and gonad growth in thermally acclimated sea urchins (Heliocidaris erythrogramma). Mar Biol 165:96
Hartmann DL, Tank AM, Rusticucci M, Alexander LV, Brönnimann S, Charabi YA, Dentener FJ, Dlugokencky EJ, Easterling DR, Kaplan A, Soden BJ (2013) Observations: atmosphere and surface. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: The physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
Hobday AJ, Lough JM (2011) Projected climate change in Australian marine and freshwater environments. Mar Freshwater Res 62:1000–1014
Hobday AJ, Alexander LV, Perkins SE, Smale DA, Straub SC, Oliver EC, Benthuysen JA, Burrows MT, Donat MG, Feng M, Holbrook NJ (2016) A hierarchical approach to defining marine heatwaves. Prog Oceanogr 141:227–238
Hopkin RS, Qari S, Bowler K, Hyde D, Cuculescu M (2006) Seasonal thermal tolerance in marine Crustacea. J Exp Mar Biol Ecol 331:74–81
Hughes T, Kerry J, Álvarez-Noriega M et al (2017) Global warming and recurrent mass bleaching of corals. Nature 543:373–377
Kingsolver JG, Woods HA (2016) Beyond thermal performance curves: modeling time-dependent effects of thermal stress on ectotherm growth rates. Am Nat 187:283–294
Ledet J, Byrne M, Poore AG (2018) Temperature effects on a marine herbivore depend strongly on diet across multiple generations. Oecologia 187:483–494
Lenton A, McInnes KL, O’Grady JG (2015) Marine projections of warming and ocean acidification in the Australasian region. Aust Meteorol Ocean 65:1–28
Magozzi S, Calosi P (2015) Integrating metabolic performance, thermal tolerance, and plasticity enables for more accurate predictions on species vulnerability to acute and chronic effects of global warming. Glob Change Biol 21:181–194
Mak KK, Chan KY (2018) Interactive effects of temperature and salinity on early life stages of the sea urchin Heliocidaris crassispina. Mar Biol 165:57
Maranhão P, Marques JC (2003) The influence of temperature and salinity on the duration of embryonic development, fecundity and growth of the amphipod Echinogammarus marinus Leach (Gammaridae). Acta Oecol 24:5–13
Martínez B, Radford B, Thomsen MS, Connell SD, Carreño F, Bradshaw CJ, Fordham DA, Russell BD, Gurgel CF, Wernberg T (2018) Distribution models predict large contractions of habitat-forming seaweeds in response to ocean warming. Divers Distrib 24:1350–1366
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998
Neuparth T, Costa FO, Costa MH (2002) Effects of temperature and salinity on life history of the marine amphipod Gammarus locusta. Implications for ecotoxicological testing. Ecotoxicology 11:61–73
Oliver EC, Benthuysen JA, Bindoff NL, Hobday AJ, Holbook NJ, Mundy CN, Perkins-Kirkpatrick SE (2017) The unprecedented 2015/16 Tasman Sea marine heatwave. Nat Commun 8:16101
Oliver EC, Donat MG, Burrows MT, Moore PJ, Smale DA, Alexander LV, Benthuysen JA, Feng M, Gupta AS, Hobday AJ, Holbrook NJ (2018) Longer and more frequent marine heatwaves over the past century. Nat Commun 9:1324
Panov VE, McQueen DJ (1998) Effects of temperature on individual growth rate and body size of a freshwater amphipod. Can J Zool 76:1107–1116
Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA, Emmett Duffy MA, Navarrete S (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15(8):912–922
Poore AG, Graba-Landry A, Favret M, Sheppard Brennand H, Bryne M, Dworjanyn SA (2013) Direct and indirect effects of ocean acidification and warming on a marine plant–herbivore interaction. Oecologia 173:1113–1124
Qiu Z, Coleman MA, Provost E, Campbell AH, Kelaher BP, Dalton SJ, Thomas T, Steinberg PD, Marzinelli EM (2019) Future climate change is predicted to affect the microbiome and condition of habitat-forming kelp. Proc R Soc B 286:20181887
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Ridgway K, Hill K (2009) The East Australian current. A marine climate change impacts and adaptation report card for Australia, 5.
Schulte PM, Healy TM, Fangue NA (2011) Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure. Integr Comp Biol 51:691–702
Schuurmans RM, Pascal van Alphen J, Matthijs HC, Hellingwerf KJ (2015) Comparison of the photosynthetic yield of cyanobacteria and green algae: different methods give different answers. PloS One, p 10.
Sinclair BJ, Marshall KE, Sewell MA, Levesque DL, Willett CS, Slotsbo S, Dong Y, Harley CD, Marshall DJ, Helmuth BS, Huey RB (2016) Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? Ecol Lett 19:1372–1385
Smale DA, Wernberg T (2013) Extreme climatic event drives range contraction of a habitat-forming species. Proc R Soc B 280:20122829
Sokolova IM, Frederich M, Bagwe R, Lannig G, Sukhotin AA (2012) Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar Environ Res 79:1–15
Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers’. J Exp Biol 213:912–920
Sørensen JG, Kristensen TN, Loeschcke V (2003) The evolutionary and ecological role of heat shock proteins. Ecol Lett 6:1025–1037
Sornom P, Felten V, Médoc V, Sroda S, Rousselle P, Beisel JN (2010) Effect of gender on physiological and behavioural responses of Gammarus roeseli (Crustacea Amphipoda) to salinity and temperature. Environ pollut 158:1288–1295
Therneau TM (2015) A package for survival analysis in S. 2015. Version 2.38.
Tomanek L (2010) Variation in the heat shock response and its implication for predicting the effect of global climate change on species' biogeographical distribution ranges and metabolic costs. J Exp Biol 213:971–979
Tsoi KH, Chiu KM, Chu KH (2005) Effects of temperature and salinity on survival and growth of the amphipod Hyale crassicornis (Gammaridea, Hyalidae). J Nat Hist 39:325–336
Vergés A, Steinberg PD, Hay ME, Poore AG, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA, Figueira W (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:20140846
Vilchis LI, Tegner MJ, Moore JD, Friedman CS, Riser KL, Robbins TT, Dayton PK (2005) Ocean warming effects on growth, reproduction, and survivorship of southern California abalone. Ecol Appl 15:469–480
Wernberg T, Russell BD, Moore PJ, Ling SD, Smale DA, Campbell A, Coleman MA, Steinberg PD, Kendrick GA, Connell SD (2011a) Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. J Exp Mar Biol Ecol 400:7–16
Wernberg T, Russell BD, Thomsen MS, Gurgel CFD, Bradshaw CJ, Poloczanska ES, Connell SD (2011b) Seaweed communities in retreat from ocean warming. Curr Biol 21:1828–1832
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 Change 3:78
Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271
Wu L, Cai W, Zhang L, Nakamura H, Timmermann A, Joyce T, Mcphaden MJ, Alexander M, Qiu B, Visbeck M, Chang P (2012) Enhanced warming over the global subtropical western boundary currents. Nat Clim Change 2:161
Xue S, Fang J, Zhang J, Jiang Z, Mao Y, Zhao F (2013) Effects of temperature and salinity on the development of the amphipod crustacean Eogammarus sinensis. Chin J Oceanol Limn 31:1010–1017
We thank Katie Erickson and Sam Sylvester for assistance with experiments. We thank the staff from the Sydney Institute of Marine Science (SIMS) for assistance. The reviewers are thanked for insightful comments that improved the manuscript. This is SIMS contribution number 255
Supported by grants from the ARC (DP150102771) (MB, AP), NSW Environmental Trust 2016RD0159 (MB).
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Campbell, H., Ledet, J., Poore, A. et al. Resilience of the amphipod Hyale niger and its algal host Sargassum linearifolium to heatwave conditions. Mar Biol 167, 72 (2020). https://doi.org/10.1007/s00227-020-03681-2