Expanding the scope: integrating costs of digestive metabolism and growth into estimates of maximum oxygen uptake in fishes Free

The recent paper by Rees et al. (2024) provided a comprehensive overview of various methods for estimating the maximum rate of oxygen uptake in fishes (Ṁ_O2,max), as measured during physical activity. Ṁ_O2,max is a critical physiological trait in animals that, when combined with the basal rate of oxygen uptake, allows estimation of the aerobic scope for in situ organismal performance. When measured in fish, Ṁ_O2,max is often equated to maximum metabolic rate (MMR) and thus marks the apparent upper limit on aerobic metabolism, thought to be important for survival and performance during various life history events and tolerance to environmental stressors. When attempting to measure ‘true’ Ṁ_O2,max, an appreciation for how methodological and experimental procedures can influence results is critical, as well highlighted by Rees et al. (2024) in their Commentary on estimating maximum oxygen uptake of fishes during either swimming (peak Ṁ_O2,swim) or following exhaustive chase (peak Ṁ_O2,recovery). As discussed by Rees et al. (2024), Ṁ_O2,swim and Ṁ_O2,recovery measure different physiological processes, yet are both used to estimate Ṁ_O2,max in fishes. In addition to Ṁ_O2,swim and Ṁ_O2,recovery, mounting evidence suggests that consideration for the costs of digestion and growth, both alone and in combination with activity, may be required for understanding and estimating ‘true’ Ṁ_O2,max across species, and, therefore, in understanding ‘true’ MMR.

Although often overlooked, research in some fish species suggests that MMR may only be measured during the digestion and processing of a meal, or when exercise and digestion occur simultaneously. During and following digestion in some fish species, apparent specific dynamic action (SDA) – the cost of digestion, assimilation of nutrients and post-absorptive processes (e.g. protein synthesis and deposition) following feeding (Goodrich et al., 2024) – involves considerably greater oxygen uptake than during or following exhaustive physical activity (Fu et al., 2022; Steell et al., 2019). Existing work in some fish species has already leveraged this phenomenon by combining meal provision with activity when attempting to elicit Ṁ_O2,max in laboratory settings (e.g. Couturier et al., 2013). Although peak oxygen uptake during SDA (peak Ṁ_O2,SDA) does not always match Ṁ_O2,swim or Ṁ_O2,recovery across species, the cost and prioritisation of SDA appear to depend on a species' lifestyle and constitutive capacity for swimming performance. Indeed, species with more sedentary lifestyles appear more likely to achieve Ṁ_O2,max during SDA as compared with during locomotor activity (Fu et al., 2009, 2022). Fish species may therefore exist along a continuum of metabolic types, spanning those prioritising digestive processes and that achieve Ṁ_O2,max through SDA, to those that prioritise locomotor activity and attain Ṁ_O2,max during or following physical exercise (i.e. visceral-type to locomotor-type continuum; Fu et al., 2022). Moreover, when SDA is combined with swimming activity by feeding and exercising animals simultaneously, values of Ṁ_O2,max exceeding peak Ṁ_O2,swim and Ṁ_O2,recovery have been observed in many species (Jourdan-Pineau et al., 2010). Even in the absence of physical activity, elevated temperatures and seasonal conditions may also drive peak Ṁ_O2,SDA to approach or exceed peak Ṁ_O2,swim or Ṁ_O2,recovery (Sandblom et al., 2014), possibly even in species that may otherwise prioritise locomotion. Notably, however, peak oxygen uptake during digestion has not been widely recorded across fish species, limiting our understanding of how the cost of SDA may vary with meal size and environmental conditions, as well as how the cost of SDA then compares with Ṁ_O2,recovery and Ṁ_O2,swim. Therefore, available evidence suggests that Ṁ_O2,max may be achieved following feeding in some species and this phenomenon may be more widespread among fishes than is currently appreciated.

By further incorporating the costs of SDA into our understanding of Ṁ_O2,max and MMR, we would also be better positioned to apply knowledge of MMR and aerobic scope in an ecological context. The digestive system represents the interface between an organism's internal and external environments through foraging and digestion, directly mediating the capacity for and aerobic cost of energy acquisition and growth. It is also among the most dynamic and expensive organ systems, receiving a disproportionate share of resting cardiac output (∼25–40%; Thorarensen et al., 1993) and circulating oxygen (11–25% of total whole-animal oxygen uptake; Brijs et al., 2018). Analogous to the critical periods of high-performance swimming fuelled by peak Ṁ_O2,swim and Ṁ_O2,recovery, values of peak Ṁ_O2,SDA may reflect the capacity for resource acquisition and allocation to growth during critical life history events, or be linked to key aspects of behaviour due to constraints on available aerobic scope (McLean et al., 2018). Given the potential for seasonal plasticity in the digestive tract to drive >2-fold changes in the mass of digestive machinery in at least some fish species (Fernandes et al., 2024), values of in situ SDA during periods of digestive up-regulation are likely to far exceed those measured in the lab. Thus, true Ṁ_O2,max or MMR in some species may be seasonally dynamic, responding to plastic changes in the form and function of digestive tissues, independent of locomotor ability. In such species, times of the year when energy acquisition has a disproportionate impact on survival and organismal fitness (e.g. during reproductive tissue development, peak seasonal growth windows, or energy accumulation prior to overwinter quiescence) may represent seasonal windows of elevated peak Ṁ_O2,SDA that directly shape reproductive potential and survival probability. Conversely, during periods of energy conservation and reduced feeding, the digestive tract can experience substantial down-regulation (Middleton et al., 2024). Corresponding reductions in peak Ṁ_O2,SDA during these periods could shift the true ceiling for whole-animal Ṁ_O2,max to occur in response to locomotor activity, while also providing information about the capacity for flexibility in the costs of digestion and growth. As such, whether true Ṁ_O2,max or MMR can be measured through SDA or in response to physical activity may not only depend on a species' lifestyle, but also on its dynamic responses to ecological and environmental factors that are yet to be thoroughly studied.

Rees et al. (2024) present an excellent and timely perspective on the benefits of understanding the physiological relevance of estimates of Ṁ_O2,max, as determined using two widespread approaches involving physical activity, introducing peak Ṁ_O2,swim and Ṁ_O2,recovery as useful updates to terminology in the field. Here, we suggest that further incorporating Ṁ_O2,SDA into estimates of Ṁ_O2,max offers an additional and fruitful suite of opportunities for understanding fish ecophysiology. We also encourage additional research on a wider diversity of fish species to further our understanding of the processes underlying why some species appear to engage in peak Ṁ_O2 during digestion and post-absorptive processes as opposed to during or following physical activity. This information will then reveal whether the most appropriate measure of Ṁ_O2,max varies within species in response to feeding history or environmental context.