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Acclimation Capacity Underlies Susceptibility to Climate Change

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Science  04 Jul 2003:
Vol. 301, Issue 5629, pp. 65
DOI: 10.1126/science.1083073

Recent reports have presented meta-analyses of global biological impacts of climate change (1, 2). However, there is debate as to the level of confidence ascribed to the certainty that global climate change has caused the observed biological changes (3). Two important considerations in the assessment of how climate change will impact organisms are (i) how close organisms are to their thermal limits in nature and (ii) an understanding of how organisms respond to increasing habitat temperatures, especially the degree to which organisms are able to adjust, or acclimatize, their thermal sensitivity.

Here, I report the effects of thermal acclimation on thermal limits of cardiac function in four congeneric species of marine invertebrates (Porcelain crabs, genus Petrolisthes) from different thermal habitats. Crabs in this genus are distributed throughout the eastern Pacific, from Alaska to Chile, and at all sites in this latitudinal range sympatric species have discrete patterns of vertical intertidal zonation (4). During low tide, these crabs remain under stones, where temperatures during hot, low tide periods have been shown to change over 20°C in 6 hours (4,5). Two of the species (P. gracilis and P. hirtipes) are endemic to the Northern Gulf of California, and the other two (P. cinctipes and P. eriomerus) are distributed in the cold-temperate zone of the northeastern Pacific (4). P. gracilis and P. cinctipes are upper intertidal zone species, P. hirtipes is a middle intertidal zone species, and P. eriomerus is found in and below the low intertidal zone (4). P. gracilis and P. hirtipes are in one phylogenetic clade that diverged ∼6 million years ago (Ma), and P. cinctipes and P. eriomerus are in a different clade with a divergence time of ∼13 Ma (4).

The upper and lower thermal limits of heart function (defined as CTmax and CTmin, respectively) (fig. S1) (5) were determined in specimens acclimated to 10°C temperature ranges (Fig. 1, A and B) (5). CTmax (Fig. 1A) and CTmin (Fig. 1B) values at either acclimation temperature were generally consistent with thermal microhabitat. CTmax values are at or near maximal habitat temperatures (Fig. 1, A and C) (4) in all species except for P. eriomerus. The striking result of this experiment is shown in Fig. 1C. The change in CTmax over the 10°C acclimation temperature range (ΔCTmax) decreased linearly among species in an inverse relation with maximal microhabitat temperature. In other words, the species that have evolved the greatest tolerance to high temperatures have done so at the expense of acclimation capacity of CTmax, and it is these species that will be the most susceptible to the smallest increases in microhabitat temperatures. The opposite effect was apparent for CTmin, where there was a positive correlation between ΔCTmin and maximal habitat temperature. These trends remained apparent after phylogenetic transformation of the data by independent contrasts analysis (5).

Fig. 1.

(A) Upper thermallimits (CT-max, fig. S1A) and (B) lower thermal limits (CTmin, fig. S1B) of cardiac function at two acclimation temperatures separated by 10°C. Low acclimation temperatures (T) were set to normalwintertime sea surface temperatures at the respective collection locations (4); T = 8°C for the two temperate species, P. cinctipes and P. eriomerus; T = 15°C for the two species from the Northern Gulf of California, P. gracilis and P. hirtipes. Acclimations were ≥4 weeks in each case. Each data point is the mean ± 1 SE; n = 5 to 6 individuals. Asterisks indicate significant differences between T and T+10 values for each species (t test, P < 0.05). (C) The change in CTmax and CTmin over the 10°C acclimation range for each species, plotted as a function of maximal habitat temperatures (4). Each data point is the difference in means of CTmax or CTmin for one species. Linear regression (dashed lines) was significant (P = 0.0044) for CTmax but not for CTmin (P = 0.11).

The prediction generated from these results is that the Petrolisthes species that would be impacted the most with increased warming would be those from the Northern Gulf of California. The capacity for acclimation of CTmax in P. gracilis is less than the estimated average amount of global warming that has already occurred (2), and thus this species may have already been impacted by climate change. There is evidence that P. cinctipes has been affected by climate-related increases in thermal microhabitat. An analysis of long-term changes in species composition of the intertidal invertebrate community in Monterey, California, reported that the abundance of P. cinctipes has dramatically declined during a period of 60 years associated with increasing thermal stress levels (6). If a relatively long-term set of data existed for P. gracilis and P. hirtipes in the Gulf of California, similar changes in abundance would have likely been observed. Thus, by understanding the biological bases that underlie the responses of organisms to increasing habitat temperature, we can increase our certainty of the direct impacts that climate change has on life in nature.

Supporting Online Material

www.sciencemag.org/cgi/content/full/301/5629/65/DC1

Materials and Methods

Fig. S1

References

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