PerspectiveEcology

The Heartbreak of Adapting to Global Warming

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Science  05 Jan 2007:
Vol. 315, Issue 5808, pp. 49-50
DOI: 10.1126/science.1137359

Climatic changes have been linked to altered geographical distributions of many organisms, including marine fish (1, 2). Yet, it remains difficult to distinguish direct causal relations between environmental temperature and species distribution patterns (3) from indirect effects through interactions with prey, predators, pathogens, or competitors (4). An ambitious goal of integrative biology is to understand how temperature affects physiological mechanisms at all levels of biological organization. This could allow predictions of how global warming affects animal performance and population dynamics. Animal physiologists commonly rely on laboratory studies to predict temperature tolerance of animals, but whole-animal performance in natural settings is rarely investigated. On page 95 of this issue, Pörtner and Kunst (5) provide compelling evidence that thermal constraints on oxygen transport are causing the population of a marine fish, the viviparous eelpout (Zoarces viviparus), to decline in the Wadden Sea.

Thermal limits.

Beyond the “pejus” temperature (Tp), the cardiorespiratory system of the fish can no longer ensure sufficient aerobic scope to sustain reproduction and growth; eventually, activity (Tc) and survival (Td) are also compromised. These thermal limits are plastic and amenable to the thermal history (acclimatization) of the animals (top three panels). P örtner and Kunst show that summer temperatures above the pejus cause the population of the European eelpout to decline, indicating that global warming may take effect well before the lethal thermal limits (Td) are reached (bottom panel).

Over the past decade, Pörtner and co-workers have studied various aspects of oxygen transport and metabolism in numerous animal species, including the viviparous eelpout (6). They have identified the pejus temperature (pejus means “turning worse”), beyond which the ability of animals to increase aerobic metabolism is reduced. This reduction is evident from the decline in aerobic scope, which is defined as the proportional difference between resting and maximal rates of oxygen consumption. The temperature range between the lower and higher pejus temperatures is much narrower than that between the critical temperatures (Tc), beyond which the animal only survives for short periods (see the figure).

As in other animals, continued cardiac function is essential in fish, but coronary circulation is normally sparse. Thus oxygen to the fish heart is primarily provided by the venous blood returning from the body (7). The oxygen concentration of venous blood declines if cardiac output does not increase in proportion to the rise in metabolism that occurs with elevated temperature (8). These problems are exacerbated by the fact that the concentration of physically dissolved oxygen in the water declines progressively with increased temperature. As a result, the heart is likely to limit the aerobic scope, rendering the fish more vulnerable to predators and less effective as a forager.

The novel discovery of Pörtner and Kunst is their observation of a strong negative correlation between estimated population sizes and summer temperatures over the past ∼50 years. On a shorter time scale, the authors also found that warm summers strongly reduced population size the following year. It remains difficult to establish increased temperature as the mechanistic cause for the population decline, but the correlation to the pejus and critical threshold temperatures derived from laboratory data is persuasive.

The temperatures causing population declines are considerably lower than the critical temperatures. The population appears to decline before temperature threatens survival of the individual. Thus, lowered scope for growth and reproduction, rather than heat-induced death per se, appears to cause the population decline.

A potential limitation of the study by Pörtner and Kunst is the difficulty of assessing the role of acclimatization. The temperatures to which an animal has previously been exposed can improve its ability to survive heat and cold, and can affect the thermal thresholds at both low and high temperature (9). The tight correlation between summer temperatures and population size observed by the authors may, nevertheless, indicate that such thermal adaptation is exhausted for eelpout in their most southern distribution range. Indeed, a lack of an acclimatory response in marine animals has previously been correlated with the inability to handle thermal shifts (2, 10).

Population dynamics are complex and depend on many biological and physical parameters, but as shown by Pörtner and Kunst, a thorough understanding of physiological limitations may provide the necessary insight to determine how global warming affects animal performance (11). The association between thermal tolerance of the oxygen transport system and population declines shows that old-fashioned physiology can be essential for understanding how temperature determines the geographical distributions of animals.

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