Do chemical markers in ear bones track metabolic rates in fish?

Energy is a fundamental predictor of a wide-range of biological and ecological processes. Measures of energy provide understanding at an individual level, providing insights into performance, growth and reproduction; population level, uncovering population dynamics and interactions; and ecosystem level, such as revealing trophic dynamics and food availabilities.

Energy of an individual is typically quantified by measuring metabolic rates. For air-breathing animals, this involves the doubly labelled water method which measures the elimination of an introduced oxygen isotope signature. However, this approach is ill-suited for fish. Alternatives such as electromyogram telemetry, heart rate monitoring and accelerometry are highly accurate and valuable, but can be unfortunately expensive and logistically difficult.

Our lab group has extensive experience in investigating chemical markers in aquatic animals for ecological applications. We wondered if these skills could be used to discover - is there a naturally occurring chemical marker that tracks metabolic rate in fish?

We were particularly interested in the potential of carbon isotopes in ‘ear bones’ (otoliths). Otoliths are paired calcified structures in all teleost fish that continuously grow and form layers, but are inert so trap chemical signatures within the layers throughout the fish’s life. Carbon isotopes have been shown to relate to indirect metabolic parameters, but very little experimental work has been completed relating direct measures of metabolic rate.

To test this theory, we conducted a laboratory experiment. Our study species was snapper (Chrysophrys auratus). Snapper is an iconic and valuable fishery species found throughout the Indo-pacific region.

We reared juvenile snapper at 4 different temperature treatments for up to 2 months. Then we used intermittent-flow respirometry to calculate metabolic rates. Intermittent-flow respirometry involves placing the fish in enclosed chambers for 24 hours and measuring the rates of oxygen consumption. Using this technique, we could calculate Standard Metabolic Rates, the minimum energy usage needed to sustain life; Maximum Metabolic Rate, the upper limit of metabolic capacity; and Absolute Aerobic Scope, illustrating energy niches and fitness/performance windows. We then measured carbon and oxygen stable isotopes in otoliths using isotope-ratio mass spectrometry.

We found that under higher temperatures, standard and maximum metabolic rates significantly increased, while carbon and oxygen isotopes in otoliths significantly decreased. We then investigated the relationships between isotopes and metabolic rates. We discovered negative logarithmic relationships between the carbon isotopes and standard and maximum metabolic rates. Additionally, exponential decay curves were observed between proportions of metabolically sourced carbon in otoliths and both measured and theoretical metabolic rates.

Our results provide experimental evidence for the quantitative use of carbon isotopes in otoliths as a metabolic proxy in fish. Biogeochemical reconstructions using hard-calcified structures like otoliths offer an inexpensive approach to develop long-term metabolic histories. These chemical approaches have particular value for populations where direct monitoring is unfeasible, particularly historical or extinct species and inaccessible deep-sea species.

Metabolic histories provide a wealth of biological information on individual, population and ecosystem levels. Carbon isotopes as metabolic proxies are a powerful tool for fish and fishery biologists and can be used to better manage our fish populations into the future.

Experimental support towards a metabolic proxy in fish using otolith carbon isotopes

Journal of Experimental Biology (2020)

Martino, Doubleday, Chung, Gillanders