This study aimed to examine temperature effects on organisms living in one of the regions where climate is altering fastest and on the seabed where most polar species live. To do this, we investigated in situ warming effects on an Antarctic marine encrusting benthic assemblage over a nine month period. Just 1°C of warming (the approximate shallow sea temperature rise projected over the next 50 years []) substantially changed the recruiting hard substratum assemblage, with likely consequences for the developing epibenthic assemblage and further through bentho-pelagic coupling. Growth rates and bare space colonization increased, and species diversity and evenness in the recruiting assemblage were reduced. If ocean warming projections are realized, these results point to extensive future changes in shallow water Antarctic benthic assemblages with implications for the whole ecosystem.

IPCC (2014). Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Core Writing Team, R.K. Pachauri and L.A. Meyer, eds. (IPCC).

Antarctic species are perceived to have reduced acclimation abilities [] probably resulting from long-term adaptation to stable cold environments. The observed tolerance and in most cases increased growth rates of species under warming treatments in the current study suggests that sessile benthic invertebrates are well adapted to deal with predicted warming over the next 50 years. Furthermore, our in situ manipulations subjected the organisms to rapid warming (especially in the +2°C treatment) that excluded physiological or genetic adaptation; these species should be capable of adapting to gradual warming over 50 years. Rapid growth rate is advantageous in benthic biofouling communities where space is limiting [] and when many measures of success are related to growth rate (e.g., age to reproduction, reproductive output, and competitive ability). The associated consequences for colonization and assemblage recovery after disturbance would be great, possibly counteracting the increased disturbance expected with climate change associated reduction in sea ice and increased glacial retreat []. Increased growth would also impact carbon accumulation in benthic systems, recently demonstrated as a negative feedback mechanism to carbon driven climate change [].

Projected warming of 1°C–2°C could be particularly significant to Antarctic marine biota, which typically experience annual temperature ranges of <4°C []. Antarctic benthic taxa are perceived as vulnerable to environmental shifts [], being considered sentinels for monitoring the effects of climate change []. Over the last 50 years, the Bellingshausen Sea west of the Antarctic Peninsula has been one of the fastest warming globally [], and both polar oceans are forecast to remain among the areas most impacted by climate change. Many biological reactions proceed much more slowly at polar temperatures than would be predicted from the effect of temperature on these functions in temperate and tropical species or from standard Arrhenius relationships []. A steeper gradient in the relationship between temperature and growth, early development, and meal processing rates at cold temperatures would align with the greater than expected response to warming observed here in polar species.

Rapid climate change in the ocean west of the Antarctic Peninsula during the second half of the 20th century.

The increases in growth rate observed on the panels were far beyond expectations. Based on long established Arrhenius relationships and literature reports [], biological reactions, enzyme activity, development, and growth rates should increase 7%–12% per 1°C warming (×2–×3 increase per 10°C rise). In the +1°C treatments, growth rate in some species doubled with a 1°C temperature rise (giving maximum Qs around 1,000). These very large effects of temperature on biological processes at polar temperatures critically change our thinking of how polar benthic communities might respond to ocean warming in the next 50–100 years and make them likely to respond very differently from lower latitude faunas or from current predictions. Although we have a good understanding of the impact of temperature on biochemical processes, our ability to expand, integrate, and apply this knowledge to the organism level is still limited []. The differing magnitude and pattern of responses among organisms highlights the complexity of this challenge [].

Zooid size and growth rate of the bryozoan Cryptosula pallasiana Moll in relation to temperature, in culture and in its natural environment.

Why is the South Orkney Island shelf (the world’s first high seas marine protected area) a carbon immobilization hotspot?.

Assemblage Response

3 Peck L.S.

Morley S.A.

Richard J.

Clark M.S. Acclimation and thermal tolerance in Antarctic marine ectotherms. 17 Barnes D.K.A.

Fenton M.

Cordingley A. Climate-linked iceberg activity massively reduces spatial competition in Antarctic shallow waters. 22 Loreau M.

Naeem S.

Inchausti P.

Bengtsson J.

Grime J.P.

Hector A.

Hooper D.U.

Huston M.A.

Raffaelli D.

Schmid B.

et al. Biodiversity and ecosystem functioning: current knowledge and future challenges. 23 Hooper D.U.

Chapin F.S.

Ewel J.J.

Hector A.

Inchausti P.

Lavorel S.

Lawton J.H.

Lodge D.M.

Loreau M.

Naeem S.

et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. 24 Kordas R.L.

Dudgeon S.

Storey S.

Harley C.D.G. Intertidal community responses to field-based experimental warming. 25 Schiel D.R.

Steinbeck J.R.

Foster M.S. Ten years of induced ocean warming causes comprehensive changes in marine benthic communities. 26 Walker C.W.

Lesser M.P. Manipulation of food and photoperiod promotes out-of-season gametogenesis in the green sea urchin, Strongylocentrotus droebachiensis: implications for aquaculture. 27 Klanderud K.

Totland Ø. Simulated climate change altered dominance hierarchies and diversity of an alpine biodiversity hotspot. The temperatures used here are within the thermal window of most Antarctic benthic species [], but different species responses could critically impact the resulting assemblage composition []. Species diversity, both richness and composition, directly influences ecosystem function []; thus, our understanding of the likely impacts of future climate change relies on our ability to predict responses at this practical and/or pragmatic level. Most experimental studies in the marine environment have observed declines in overall species richness among benthic communities subjected to artificial warming [], mirroring observations from terrestrial environments [].

19 Barnes D.K.A.

Souster T. Reduced survival of Antarctic benthos linked to climate-induced iceberg scouring. In the Antarctic shallows, increased iceberg disturbance driven by ocean warming has already been suggested as a likely driver of change in ecosystem structure []. Our results indicate that ocean warming will also directly influence species composition of shallow benthic assemblages, possibly amplifying secondary effects, including iceberg groundings. Both stressors seem to favor the opportunist F. rugula.

28 Brown J.H.

Valone T.J.

Curtin C.G. Reorganization of an arid ecosystem in response to recent climate change. 29 Bowden D.A.

Clarke A.

Peck L.S.

Barnes D.K.A. Antarctic sessile marine benthos: colonisation and growth on artificial substrata over three years. 30 Ferguson B.G.

Boucher D.H.

Pizzi M.

Rivera C. Recruitment and decay of a pulse of Cecropia in Nicaraguan rain forest damaged by hurricane Joan: relation to mutualism with Azteca ants. 31 Malison R.L.

Baxter C.V. Effects of wildfire of varying severity on benthic stream insect assemblages and emergence. 32 Harley C.D.G.

Randall Hughes A.

Hultgren K.M.

Miner B.G.

Sorte C.J.

Thornber C.S.

Rodriguez L.F.

Tomanek L.

Williams S.L. The impacts of climate change in coastal marine systems. Species contributing most to the differences among treatments were pioneer species, i.e., those colonizing bare space. Such species dominate encrusting Antarctic shallow benthic assemblages up to 3 years old (see []). Shifts in r-strategists also dominate changes in hurricane-impacted forest assemblages [] and in streams affected by wildfire disturbance []. Succession is a variable process, but, as demonstrated here, ocean warming is likely to alter the balance of facilitation, competition, and inhibition among species [], changing the resultant community.

33 Stachowicz J.J.

Terwin J.R.

Whitlatch R.B.

Osman R.W. Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions. 34 Stanwell-Smith D.

Peck L.S. Temperature and embryonic development in relation to spawning and field occurrence of larvae of three Antarctic echinoderms. 35 Gibson R.N.

Atkinson R.J.A.

Gordon J.D.M.

Byrne M. Impact of ocean warming and ocean acidification on marine invertebrate life history stages: Vulnerabilities and potential for persistence in a changing ocean. 26 Walker C.W.

Lesser M.P. Manipulation of food and photoperiod promotes out-of-season gametogenesis in the green sea urchin, Strongylocentrotus droebachiensis: implications for aquaculture. 36 Ramirez Llodra E. Fecundity and life-history strategies in marine invertebrates. 37 Edwards M.

Richardson A.J. Impact of climate change on marine pelagic phenology and trophic mismatch. 38 Durant J.M.

Hjermann D.O.

Ottersen G.

Stenseth N.C. Climate and the match or mismatch between predator requirements and resource availability. Ecological succession could be further altered by different effects or by different intensities of effects on physiological processes among species. For example, growth rates of some species are directly increased under warming ([]; this study) and development rates of marine invertebrates are markedly affected by warming [], whereas onset of reproduction may be more closely related to other stimuli: light or food availability, for example []. With these various effects, changes in ambient temperature will most likely have complex effects on the end result of ecological succession [].

39 Doney S.C.

Ruckelshaus M.

Duffy J.E.

Barry J.P.

Chan F.

English C.A.

Galindo H.M.

Grebmeier J.M.

Hollowed A.B.

Knowlton N.

et al. Climate change impacts on marine ecosystems. 28 Brown J.H.

Valone T.J.

Curtin C.G. Reorganization of an arid ecosystem in response to recent climate change. Species diversity and evenness in this study were reduced because of the increase in pioneer species growth on heated panels. Although metabolic rates generally increase with rising temperature, other factors, including nutritional status, food processing time, and thermal tolerance, may limit increases in biological processes []. We could not observe later stages of succession, but we suggest that rare species may be impacted by the overwhelming response of common pioneers (F. rugula here). Effects of keystone species can amplify across biotic relationships through networks of interactions to alter the structure and dynamics of ecosystems []. In this assemblage, F. rugula appears as the pivotal species.

40 Smale D.A.

Wernberg T.

Peck L.S.

Barnes D.K.A. Turning on the heat: ecological response to simulated warming in the sea. 33 Stachowicz J.J.

Terwin J.R.

Whitlatch R.B.

Osman R.W. Linking climate change and biological invasions: Ocean warming facilitates nonindigenous species invasions. Assemblage growth on the panels increased under warming treatments. A similar increased cover response was observed in short-term (36 days) heated panels deployed in Perth, Australia []. In that study, an ascidian, Didemnum perlucidum, dominated the increase in cover, even though it rapidly grew out of the heated conditions. In laboratory experiments, growth increased in three ascidian species settled on panels and subsequently warmed to between 5°C and 9°C above ambient []. Ascidians were a minor component of the Antarctic recruiting assemblage in our study, where the response of the dominant bryozoan species, F. rugula, outweighed all others.

41 Huey R.B.

Stevenson R.D. Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Compared to the +1°C panels, warming on the +2°C panels produced divergent responses across species, leading to a further different assemblage after 9 months. The assemblage growth response (as area covered) was more variable across the +2°C treatments, with two panels exhibiting similar growth to the +1°C panels and two panels with less growth (similar to or less than that of controls). The increase in variability is somewhat unsurprising given the nonlinearity of thermal performance curves []. The panels with reduced growth had large areas of non-colonized surface (rather than evenly distributed bare patches; Figure 1 ). Panel construction, warming, and surface texture were identical, and there was no evidence of predation. Reduced recruitment is the most likely contributing factor to the low spatial cover on these panels. Reduction of recruitment success in benthic species under future warming would severely impact the marine ecosystem.

39 Doney S.C.

Ruckelshaus M.

Duffy J.E.

Barry J.P.

Chan F.

English C.A.

Galindo H.M.

Grebmeier J.M.

Hollowed A.B.

Knowlton N.

et al. Climate change impacts on marine ecosystems. 42 Barnes D.K.A. Iceberg killing fields limit huge potential for benthic blue carbon in Antarctic shallows. 43 Kroeker K.J.

Kordas R.L.

Crim R.

Hendriks I.E.

Ramajo L.

Singh G.S.

Duarte C.M.

Gattuso J.P. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. 25 Schiel D.R.

Steinbeck J.R.

Foster M.S. Ten years of induced ocean warming causes comprehensive changes in marine benthic communities. 44 Paine R.T. Food-web analysis through field measurement of per capita interaction strength. 45 Sanford E. Regulation of keystone predation by small changes in ocean temperature. Understanding different species responses to warming is critical to modeling likely community change under ocean warming scenarios. Shifts in abundance, phenology, and spatial organization (distribution and dispersion) should be expected []. However, it is difficult to isolate the relative importance of warming on physiological-, population-, and community-level responses. The response will be complicated further by the interaction of warming with other stressors, e.g., ocean acidification, sea-ice loss, and iceberg impact frequency []. The observed increase in spatial cover in this experiment could be explained by the physiological response of one species, F. rugula, which doubled under 1°C of warming. But the resulting alterations in species composition and impact on later stages of succession are harder to predict. Community and ecosystem processes are often dominated by a few strong interactions against a background of many weak interactions []. In this Antarctic environment, F. rugula may provide a benthic indicator of ecological response to environmental change.