Dyllan Furness, College of Marine Science
Nearly a century ago, zoologist Ralph Clausen wrote, "That the metabolism of a cold-blooded animal increases as the temperature of its environment increases is a maxim so firmly rooted in the minds of most biologists that it may seem wanton to explore the question again."
Brad Seibel
Brad Seibel, professor of biological oceanography at the USF College of Marine Science, questions this maxim in a recent study. He examined hundreds of measurements from dozens of species of flatfish, looking at their metabolic rates across various body sizes and temperatures.
His findings, , challenge the long-held theory about how animals respond to changes in temperature. Seibel suggests that, as ocean temperatures rise, an 鈥渁rms race鈥 may ensue that sees animals leverage environmental conditions to gain an advantage on their predators and prey.
Here he discusses the foundation of his 鈥渢hermodynamic opportunities hypothesis鈥 and its broader implications for species facing higher temperatures.
Q. Your paper challenges the theory that metabolic rates in animals increase with higher temperatures. Can you briefly explain the conventional metabolic theory that your paper addresses?
A. Metabolic theory generally holds that animals are at the mercy of the "tyranny of the Boltzmann's constant.鈥 That is, whole-animal metabolism responds to an unavoidable constraint that environmental temperature places on the metabolic rate of organisms, primarily via chemical kinetic principles first described by Ludwig Boltzmann in the late 1800s. That constraint dictates that as environmental temperature rises, biochemical reaction rates 鈥 and thus the metabolic rates of ectotherms [cold-blooded animals] 鈥 increase exponentially. The rate of increase is constrained within a narrow range such that a 10掳C increase in temperature results in a two to three-fold increase in metabolic rate.
While it is generally acknowledged that animals can physiologically acclimate and adapt for life at different temperatures, most studies find that whole-animal metabolic rate, both within and across species, increases with temperature as predicted by kinetics. This generality is the basis of a lot of ecological models and predictions about organismal responses to climate change.
A. Your findings instead indicate that metabolic rates across species of flatfish largely do not change from the poles to the equator. Why is this significant?
Q. Some researchers, myself included, maintain that whole-animal metabolic rate is not dictated by chemical kinetics. Metabolic rate is a measure of energetic cost to animals. A high rate is a disadvantage unless it reflects some fitness benefit, such as the cost of activity for predator avoidance or wider foraging ranges. At any given temperature, metabolic rate varies between, for example, active and inactive species by as much as 100 times.
Why then can't animals adjust metabolism lower at higher temperatures? I hypothesized that high temperature represents a thermodynamic opportunity, not a mandate, for increased performance. Muscle contraction can happen faster, nerves can carry signals faster, and metabolism can proceed faster at higher temperatures. If being faster provides a fitness advantage, metabolism will increase with temperature. However, for any group of species for which activity is not a priority, higher rates may represent all cost and no benefit.
I did find that acute 鈥 short-term 鈥 laboratory exposure to higher temperatures elevated metabolism for every species. But I found that all flatfish species had the same metabolic rate from the poles to the equator. They had compensated over longer time scales for increased costs of wasteful processes, such as macromolecular degradation and ion leak, at high temperatures. The costs associated with their ecological lifestyles were similar across latitude and that was reflected in their metabolic rates.
Q. Why do flatfish offer a useful model for studying the broader relationship between metabolic rates and temperature?
A. Flatfish offered several advantages for this study. Most importantly, all flatfish have very similar ecological lifestyles. In every species for which behavior has been described, a majority of their time is spent camouflaged, lying motionless on the seafloor. To facilitate this, they've evolved such that both eyes are found on the same side of the head. This specialization for benthic inactivity allows us to compare between species with less concern that metabolic differences are based on different ecologies. Secondly, because flatfish are economically important, highly diverse, easily maintained in the laboratory, and occupy nearly all environments, I was able to find an abundance of data in the literature. I found hundreds of metabolic rate measurements in about 40 species across a wide range of body sizes and temperatures.
Q. You stated that warm water provides a thermodynamic opportunity for the increase of an animal鈥檚 metabolic rate required for predator-prey interactions. What role does camouflage of flatfish play in this process and how might it influence he metabolic invariance of flatfish?
A. Metabolic capacity is tied, in many cases, to activity including foraging, prey-capture, and predator-avoidance. Camouflage provides an opportunity to capture prey and avoid predators with minimal activity. This is not unlike my earlier work in the deep sea where darkness precludes visual predator-prey interactions and most deep-living fishes have comparably low metabolic rates as a result. Any unnecessary movement, in flatfish or in among deep sea animals, increases the risk of alerting predators and prey to their presence and provides no advantage in finding prey.
Q. What are the broader implications of these findings? How does it expand our understanding of organisms鈥 responses to rising temperatures?Top of Form
A. The thermodynamic opportunities hypothesis explains why, in most cases, metabolism does increase with temperature. The advantages of faster muscle contraction, nervous function, and metabolic processing improve predator-avoidance and prey capture. If just one species takes advantage of that opportunity, they have an advantage over the others that do not take advantage. So, I hypothesize a sort of arms race driven by this thermodynamic opportunity. But the findings in flatfish also demonstrate that species do not have to elevate metabolism at high temperature if it does not provide a specific benefit. Ecology and evolution are in the driver's seat; thermodynamics is an important, but secondary consideration.