within species upper temperature limits and individual size
Size (and by implication, age and sexual maturity) is not often taken into account in investigations of upper lethal limits (Chown, Gaston & Robinson 2002). In the infaunal bivalve mollusc L. elliptica, however, the loss of ability to rebury in sediment with rising temperature is linked to size and oxygen availability (Peck et al. 2007). Ecologically the loss of large animals before small individuals has consequences for macroecological predictions of responses to climate change, as the impact on the effective reproductive population will be greater than average population limits and recruitment will thus be affected by smaller temperature elevations and to a greater than expected degree (Perrin 1993). One area where the effects of the removal of larger individuals has resulted in a cascade of effects on life-history characters is in the impact of fisheries on exploited populations. Fisheries generally target larger individuals, which favours reproduction at earlier ages and slower growth (Coltman 2008). However, unexpected outcomes have also been identified, with behavioural responses to fishing gear that potentially change recruitment patterns (Uusi-Heikkiläet al. 2008) and the demonstration that, in some species, larvae of older individuals have better survival potential than those of younger ones (Bobko & Berkeley 2004; Birkeland & Dayton 2005). Humans act as a strong evolutionary force that is almost ubiquitous across the globe (Palumbi 2001), and climate change is one aspect of this.
Similar effects from the early removal of larger individuals by a warming environment would be expected to those seen from fishing but, without large effort to characterize them across the ecosystem, they will be unpredictable. However, such data would be of direct relevance and great importance to the analysis, and prediction of responses to climate change.
It should, however, be noted here that all of the analyses on relations between temperature change and size to date have been rapid or very rapid compared to the rate of ecologically important and climate change processes. Of specific importance here is that ‘with slower rates of change’ acclimation and adaptation processes become the main elements of species responses, and these are absent from the currently available data. Following 60 days of acclimation to 3 °C acute temperature trials still showed small individuals surviving to higher temperatures than large ones (Peck, Morley & Clark, unpubl) in 6 of the species of Antarctic marine invertebrate studied here.
Despite the above concerns, it is at least likely that where warming is significant over monthly to annual time-scales then large individuals will be more affected than small ones. There will also be cases where acute warming occurs naturally with a regime shift, change in water mass movement or during or following migration. At these times size effects would be expected to be important.
activity and upper temperature limits
The current paradigm is that in short-term trials upper temperatures for survival in marine species are limited by tissue oxygen supply and aerobic scope (Pörtner 2002a; Peck et al. 2004; Pörtner et al. 2007). Our data support this as more active species have higher aerobic scopes than sessile ones. Across species comparisons show that, in mammals, large species have larger aerobic scopes than small ones (Weibel et al. 2004). Thus large species should do better in our comparisons than small ones. However, in our comparison (Fig. 2) the most active species were small (the amphipods C. femoratus and W. obesa) and three of the four least active species were relatively large (the ascidian C. verrucosa, the anemone U. antarcticum and the bivalve mollusc L. elliptica). A concern may be that this could be a difference caused by cross-phylum comparisons compared to the within phylum analyses of mammals. However, our analysis of residuals showed no significant effect at the phylum level, and a bias of this type is therefore unlikely. Phylogenetic effects on data of this type are strongest at higher taxonomic levels (Chown et al. 2002, 2004), and a lack of effect at the phylum level strongly indicates that the major trends identified here would not be altered by a wider-scale phylogenetically based analysis.
It should be noted here that previous within species analyses have also shown smaller individuals survive to higher temperatures than larger ones in marine species (Peck et al. 2004, 2007). However, as small phyla are often more active than larger ones in marine ectotherms, our data may help to explain why small species have been historically suggested to be less vulnerable to extinction events (Cardillo 2003).
effect of varying rate of warming
The value of short-term experiments in predicting the consequences of climate change on populations and species has been questioned (Barnes & Peck 2008). Short-term data are of value in understanding mechanistic cellular and physiological responses. They may also be of value in quantifying dispersal limits where migrating or drifting individuals cross-thermal thresholds or move to new temperature regimes, phenomena that are common in dispersing organisms, and important for Antarctic marine species colonising island chains away from the main continent. These data are, therefore of great value in identifying limits to dispersal capability. In experiments investigating upper temperature limits, rate of warming is very important. By comparing our data for survival in our acute trials with published data for medium-term warming where temperature is raised around 1–2 °C and animals then allowed to acclimate to the new temperature for several days to a week, and also with data for temperatures that Antarctic marine species have been acclimated to for periods of 1 month or more a relationship between rate of warming and upper temperature limit can be obtained (Fig. 4). The Antarctic species studied survive to temperatures between 8·3 °C and 17·6 °C when temperatures are raised acutely (1 °C day−1 rise), only survive to 4·0–12·3 °C when elevations are weekly and only to 1–6 °C for long-term acclimated treatment. The mean value for acclimated survival of over 1 month is 3·3 °C, where significant numbers of species would be predicted to suffer long-term survival problems. This is 2–3 °C above current summer maximum temperatures in large parts of the southern Ocean. Fitting a regression to the data in Fig 4 after logging both axes (Ln upper temperatures = 2·57 – 0·398 Ln days, r2 = 67·6, F = 59·3, P < 0·001), and extrapolating suggests that average species survival of elevated temperatures for in excess of 1 year would be 1·3 °C. As for the analysis of upper limits and activity, a residuals analysis at the phylum level shows no significant effect (Fig. 5, anova: F6,35 = 0·5, P = 0·81). In some years current summer temperatures already exceed 1·3 °C at Rothera, where this work was done. However, this temperature limit needs very careful interpretation as the 1-year time-scale is well-beyond the current data range. Models do not predict average annual temperatures in Antarctica to rise above 1 °C for many decades and seasonal factors may allow species to survive significantly higher summer temperatures for short periods. Studies that account for seasonal variation in temperature are needed to give a clearer view of the impact of elevated temperature, rather than those based around simple designs with temperature elevation to constant values.
Figure 4. Mean upper temperature tolerance limits vary exponentially with rate of temperature rise. Data shown are upper temperature limits for species (14 species shown for 1 °C day−1 rise (this study); 7 species for 1–2 °C week−1 rise and 16 for long-term acclimation studies, where species survive for in excess of 1 month. Data from this study and: Somero & DeVries (1967); Peck (1989); Gonzales-Cabrera et al. (1995); Pörtner et al. (1999); Peck et al. (2002); Bailey et al. (2005); Lannig et al. (2005); Lowe & Davison (2005); Seebacher et al. (2005); Brodte et al. (2006); Jin & DeVries (2006); Podrabsky & Somero (2006); Peck et al. (2008). Data showing Ophionotus victoriae can acclimate to +1 °C but not +2 °C, M.S. Clark pers. obs.; data showing Laternula elliptica cannot acclimate to +4 °C but can survive > 1 month at +3 °C, S. Morley, pers. obs. Data showing Cheirimedon femoratus can survive > 1 month at +4 °C, Marseniopsis mollis, Sterechinus neumayeri, Paraceradocus gibber, Yoldia eightsi, and Heterocucumis steineni can survive > 1 month at +3 °C M.S. Clark, S. A. Morley & L.S. Peck pers. obs.
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Figure 5. Plot of residuals of data shown in Fig. 4 after Ln transformation of both variables. Residuals are shown as means ± SE and are calculated at the phylum level. There is no significant effect of phylum (anova: F6,35 = 0·5, P = 0·81).
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The long-term limits in Fig. 4 are significantly lower than the medium-term survival values. Where there is data they are also significantly below the temperatures where tissues begin to accumulate anaerobic end-products of metabolism such as succinate (Mark, Bock & Pörtner 2002; Peck et al. 2002; Pörtner et al. 2006). Thus in the bivalve L. elliptica, medium-term temperature limits are around 9 °C and anaerobic end-products accumulate at around 6 °C (Peck et al. 2004; Pörtner et al. 2006). However, its long-term acclimated limit is around 3 °C. The temperatures where anaerobic products begin to accumulate are termed the critical temperatures and have been proposed as the physiological limits for survival (Mark et al. 2002; Pörtner 2002b; Pörtner & Knust 2007). It is possible to explain these data using the oxygen limitation hypothesis where pejus thresholds have been defined as the temperatures where aerobic scope or capacity falls from optimal levels and performance is ‘getting worse’ (Pörtner 2002a, 2006). Although pejus conditions are defined in such a way that the concept of worsening performance must be true when conditions move away from the absolute optimum, this theory could explain the reduction of temperature limits with ex-posure duration seen here. This possibility is also supported by the correlation found between oxygen delivery and environmental temperatures beyond which growth performance and abundance decrease in eelpout (Pörtner & Knust 2007).
Our data can also be explained in a wider ecological/physiological framework. When conditions change rapidly (acute change), resistance mechanisms are important, and oxygen limitation has been demonstrated, and widely accepted, to be the mechanism dictating survival limits. In our study these responses are clear when temperatures are changed daily or weekly. At slower rates of change (monthly to yearly) acclimation and other processes such as rate of utilization of stored reserves become important in dictating survival. In this context the acclimation of many physiological processes is important (e.g. membrane transport, cell homeostatis, neuro-muscular function, locomotory organization, feeding and absorptive processes) and poor acclimation in any could affect physiological and ecological performance resulting in loss of fitness. Here oxygen limitation is one important mechanism, but not the sole mechanism. At climate change relevant rates of warming (annual to decadal or longer) adaptation and ecological mechanisms are major factors dictating survival. Thus changes in food availability, predator/prey interactions and evolution of new characters are of high importance. Physiological limits will still play an important role in dictating ecological balance, but they will be only one of several mechanisms, and oxygen limitation will only be one of several physiological systems under adaptational limitation (Peck 2005; Barnes & Peck 2008). At rates of change predicted by climate models several ecological factors become important that are outside of physiological limitation mechanisms. These include alien invasion, spread of predator ranges, or contraction of predator ranges changing competitor balance and changes in quantity and quality of resource availability such as food, nutrients and available space for settlement and colonization (Walther et al. 2002; Thomas et al. 2004; Barnes & Peck 2008; Chown & Gaston 2008). There is very little information on where physiological limits trade off with adaptational and ecological constraints. Our data, showing acclimation temperatures to be several degrees below critical oxygen limitation temperatures at faster rates of warming suggest that other factors than oxygen limitation have started to become important in monthly time-scale studies. These probably include energy balance or homeostasis mechanisms.
It has been suggested that the ability to acclimate to changing conditions is the most important criterion in dictating which species will survive and which will fail (Stillman 2003). We would argue that many factors are important, including immediate physiological scopes and temperature effects on biotic interactions. Different species and populations will respond in varying ways to change and the crucial factor dictating success will not always be acclimation. Stillman (2003) also argued that tropical species should be more limited in their ability to acclimate than temperate or polar species. Our data indicate Antarctic ectotherms have very poor abilities to acclimate to elevated temperature and are at least as sensitive as tropical marine ectotherms. Peck et al. (2008b) also showed the Antarctic brittle star O. victoriae to be incapable of acclimating to +2 °C, a temperature < 0·5 °C above currently experienced summer maximum temperatures. Furthermore recent data on temperature tolerances for survival and ability to perform activity in congeneric bivalve molluscs from tropical to Antarctic latitudes show both tropical and polar species to be living permanently close to their thermal limits (Morley et al. 2007, unpublished data). Thus tropical species may not be the most limited in their abilities to acclimate.
Outside of considerations of acclimation, tropical species have been shown to be susceptible to change and this is especially true for coral bleaching where short-term tolerances are close to maximum experienced temperatures (Hoegh-Guldberg 1999) and mortality is markedly affected by symbiont type and host–symbiont relations (Sampayo et al. 2008). However, Antarctic marine ectotherms are recognized as among the most stenothermal on Earth (Peck & Conway 2000; Aronson et al. 2007). They are also characterized by slow physiological rates, growth and great age (Peck & Brey 1996; Peck 2002). They often exhibit very slow larval development rates and unusual reproductive strategies (Peck & Robinson 1994, Peck et al. 2006a,b), and are the only species to lack the classic heat-shock response (Clark, Fraser & Peck 2008a,b; Clark et al. 2008c). These factors may also make them less able to cope with or adapt to change than species from other latitudes.
The type of study presented here, evaluating effects of rate of temperature rise and identifying both size and ecotype effects based on activity is a broad scale physiological approach with the potential for comparing large scale patterns of faunas from different regions. This is a macrophysiological approach. It offers one of the few avenues for bridging the gap between ecophysiological experimental and observational environmental envelope approaches to predicting broad scale and ecosystem level effects of climate change. It also provides a route for identifying ecologically relevant species tolerance limits.