Measuring Baltic herring.

Taking seriously the explanations on shrinking fish in a warming world

Measuring Baltic herring.

Measuring Baltic herring. Photo by Aleksey Kusnetsov, Wikimedia Commons.

As climate change continues to warm and deoxygenate ocean water, the size of fish, aquatic molluscs and crustaceans is showing a concerning reduction pattern. This pattern manifests a life history in which the animals exposed to rising temperatures grow fast when they are young but mature at smaller sizes than before and their final body sizes are also smaller than they used to be.

Two dominant theoretical proposals explain the impact of increasing temperatures on the growth and overall performance of fishes and other aquatic animals: H.-O. Pörtner’s Oxygen- and Capacity-Limited Thermal Tolerance (OCLTT) and the Gill-Oxygen Limitation Theory (GOLT), originally developed by Daniel Pauly.

In simple terms, both of these theories state that as temperatures increase, water-breathing animals need to invest more energy – and thus the little oxygen they get from their environment – in maintaining their body functions, which leaves a smaller fraction of the energy budget for growth.

Given that the temperature increase and fish shrinking trends are not slowing down, the debate around the mechanistic models that explain their causes has become nothing but heated.

The intense discussions are justified not only for mere scientific reasons but also because the shrinking of body sizes has consequences for entire populations, and thus the productivity of commercial fish stocks.

Joining the debate

In a recent paper published in the journal Fishes, the Sea Around Us principal investigator, Dr. Daniel Pauly, and Dr. Johannes Müller, associate professor at Leiden University, join the debate by counterarguing -point by point- some of the criticism expressed by physiologists to the OCLTT and the GOLT, with an emphasis on the latter.

“One line of arguments against the GOLT is based on comparisons between gill growth and oxygen consumption at different body sizes. The GOLT assumes that the increase in oxygen consumption is proportional to the increase in gill surface area – for the simple reason that fish utilize the full capacity of their gills to survive, grow and reproduce – and all existing studies show this,” Dr. Müller said. “However, some criticisms of the GOLT assume that the match between oxygen uptake and gill area invalidates the theory. Their authors seem to believe that matching slopes would allow for continuous growth even at later life stages and, thus, that factors other than oxygen supply must limit the ultimate size of fish.”

According to Dr. Müller, these arguments neglect the fact that measured oxygen uptake in young and growing fishes also includes the costs of growth itself.

“We went back to the datasets on which the criticisms of the GOLT were based and showed that -in studies considering food intake- the fasting periods before measuring fish’s metabolic rates were too short to fully exclude the oxygen that is needed to fuel growth,” he said.

FITTING IN BIASES

Müller and Pauly also found that some of the critiques were grounded on data that had been presented in a distorted way to fit their senior authors’ bias against the Gill-Oxygen Limitation Theory.

One of the tenets of the GOLT is that the gills of growing fish, as two-dimensional surfaces, can’t keep up with the growth pace of a three-dimensional body. Thus, when a fish reaches a point where its gills cannot supply oxygen to a larger body, the animal stops growing.

In one of the papers analyzed, gill surface area measurements were performed in 19 specimens of California horn shark, which ranged in weight from 0.039 kg to 4.44 kg. The data points obtained from these measurements showed that a linear regression would provide a statistically precise estimate of the value that determines a fish’s oxygen supply on a per-weight basis. However, the researchers decided to use a segmented regression in which three pairs of gill area and body weights of the smallest fish were fitted with a line distinct from that for the 16 other, larger specimens.

“This way of interpreting the data provided a false argument against the idea that geometric constraints of gill surface area limit a fish’s metabolism,” Dr. Pauly said. “But they are based on the position of 3 of 19 data points, and on the implicit assumption – not addressed at all – that young sharks have gills that grow more slowly than those of adults. This does not occur in the real world, and it suggests that the authors interpreted their data in a peculiar way so that they could be used against the GOLT.”

The contribution by Müller and Pauly welcomes the increased interest in the GOLT but also calls for better evaluations of its central tenets.

“In times of rapid climate change, it is crucial to adequately test theories whose explanatory scope is wide enough to address unprecedented challenges on a general level,” Dr. Pauly said.

The paper “Fishes in warming waters, the gill-oxygen limitation theory and the debate around mechanistic growth models” appeared in MDPI’s Fishes https://doi.org/10.3390/fishes9110430