PerspectiveEcology

Physiology and Climate Change

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Science  31 Oct 2008:
Vol. 322, Issue 5902, pp. 690-692
DOI: 10.1126/science.1163156

Ongoing ecosystem changes in response to climate change include poleward or altitudinal shifts in geographical distribution (1-3), population collapses or local extinctions (4), failure of large-scale animal migrations (5), changes in the seasonal timing of biological events (6), and changes in food availability and food web structure. These changes are largely driven by environmental temperature (1,7). Examples from aquatic animal communities show that study of physiological mechanisms can help to elucidate these ecosystem changes and to project future ecological trends.

All organisms live within a limited range of body temperatures, due to optimized structural and kinetic coordination of molecular, cellular, and systemic processes. Functional constraints result at temperature extremes. Increasing complexity causes narrower thermal windows for whole-organism functions than for cells and molecules, and for animals and plants than for unicellular organisms (8). Direct effects of climatic warming can be understood through fatal decrements in an organism's performance in growth, reproduction, foraging, immune competence, behaviors and competitiveness. Performance in animals is supported by aerobic scope, the increase in oxygen consumption rate from resting to maximal (9). Performance falls below its optimum during cooling and warming. At both upper and lower pejus temperatures, performance decrements result as the limiting capacity for oxygen supply causes hypoxemia (4, 8) (see the figure, left). Beyond low and high critical temperatures, only a passive, anaerobic existence is possible. Fish rarely exploit this anaerobic range, but invertebrates inhabiting the highly variable intertidal environment use metabolic depression, anaerobic energy production, and stress protection mechanisms to provide short- to medium-term tolerance of extreme temperatures.

Thermal windows likely evolved to be as narrow as possible to minimize maintenance costs, resulting in functional differences, between species and subspecies in various climate zones (10-12) and even between populations of a species (13); for example, the optimal and critical temperatures differ by 2° to 3°C between two sockeye salmon populations from the Fraser River in British Columbia, Canada (5).

Long-term fisheries data revealing climate impacts on fish stocks have often been related to food web effects. However, they can also involve direct warming impacts on individual species, linked to thermal windows. For example, in the German Wadden Sea, growth and abundance of a nonmigratory eelpout decreased when summer maximum temperatures surpassed the upper pejus temperature, with larger individuals affected first (4). In the Japan Sea, different thermal windows between sardines and anchovies for individual growth, gamete production and quality, and spawning activity caused a regime shift to anchovies in the late 1990s (14, 15). In the Fraser and Columbia River systems, warming has often delayed spawning migrations of nonfeeding Pacific salmon, potentially causing loss of fitness (16). Cardiac collapse above the critical temperature likely brought on swimming failure and mortality among Fraser River sockeye in 2004 (5).

The ongoing northward shifts of North Sea Atlantic cod stocks likely involve both direct effects on cod and indirect food web effects. Clear correlation of these shifts with winter warming indicates greatest sensitivity of the fishes during their winter reproductive period (1). One reason may be that the oxygen demand of a 20% gonadal mass (17) disadvantages mature females by narrowing their thermal window (see the figure, middle). Also, the enhanced reproductive capacity of large body size reduces optimal temperatures for growth and increases heat sensitivity (13). Furthermore, thermal windows for growing larval fish, which might be as narrow as those of reproducing adults, may also reflect limited oxygen supply, when the developing ventilation and circulatory systems take over from simple diffusion across the body surface.

Temperature effects on aquatic animals.

The thermal windows of aerobic performance (left) display optima and limitations by pejus (pejus means “turning worse”), critical, and denaturation temperatures, when tolerance becomes increasingly passive and time-limited. Seasonal acclimatization involves a limited shift or reshaping of the window by mechanisms that adjust functional capacity, endurance, or protection (4). Positions and widths of windows on the temperature scale shift with life stage (middle). Acclimatized windows are narrow in stenothermal species, or wide in eurytherms, reflecting adaptation to climate zones. Windows still differ for species whose biogeographies overlap in the same ecosystem (right, examples arbitrary). Warming cues start seasonal processes earlier (shifting phenology), causing potential mismatch with processes timed according to constant cues (light). Synergistic stressors like ocean acidification (by CO2) and hypoxia narrow thermal windows according to species-specific sensitivities (broken lines), modulating biogeographies, coexistence ranges, and other interactions further.

An indirect effect of warming is implied in the shifted community composition in the Southern North Sea from larger to smaller zooplankton prey (18), reducing the food available to juvenile cod. This shift likely reflects different thermal windows for these cope-pod species as well as for cod and their prey, given that oxygen-limited thermal tolerance was recently confirmed for small zooplankter (19). Such differences between windows may, in general, underpin changes in species interactions and cause shifts in spatial or temporal overlap (see the figure, right).

Further ecosystem-level responses to climate change include shifts in the seasonal timing of recurring processes (20). Earlier seasonal development of zooplankton or its grazing later in the year may no longer match the timing of phytoplankton blooms (6). Climate could elicit such shifts when warming cues enter or leave thermal windows earlier in the year (see the figure, right). As other cues like seasonal light conditions remain constant, this may cause previously matched species interactions to go out of phase; food availability may change.

Extending the principle of specialization on differing thermal windows to interacting species can help explain changing biogeographies, community composition, and food web structures. These changes mostly set in at the borders of current distributions, where species operate at the limits of their thermal windows; acclimatization mechanisms fail to maintain performance and shift thermal limits further. Such trends can be compensated for by evolutionary selection for adequate genotypes. However, such adaptation may be too slow for long-lived species. Climate change will thus differentially favor species with wide thermal windows, short generation times, and a range of genotypes among its populations.

Carbon dioxide, hypoxia, salinity change, and eutrophication contribute to ecosystem responses to climate change (21). Key to setting sensitivity to ocean acidification are the mechanisms and efficiency of systemic acid-base regulation (22). Such specific effects of each stressor will reduce whole-organism performance, especially at extreme temperatures, thereby narrowing thermal windows and reducing biogeographical ranges. Studies of ecosystem consequences of stressors like ocean acidification through carbon dioxide should thus consider effects on thermally limited oxygen supply. The principles elaborated here may also be applicable to organisms other than animals and to both aquatic and terrestrial ecosystems (23).

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