Partitioning the metabolic scope: the importance of anaerobic metabolism and implications for the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis

Abstract

Ongoing climate change is predicted to affect the distribution and abundance of aquatic ectotherms owing to increasing constraints on organismal physiology, in particular involving the metabolic scope (MS) available for performance and fitness. The oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis prescribes MS as an overarching benchmark for fitness-related performance and assumes that any anaerobic contribution within the MS is insignificant. The MS is typically derived from respirometry by subtracting standard metabolic rate from the maximal metabolic rate; however, the methodology rarely accounts for anaerobic metabolism within the MS. Using gilthead sea bream (Sparus aurata) and Trinidadian guppy (Poecilia reticulata), this study tested for trade-offs (i) between aerobic and anaerobic components of locomotor performance; and (ii) between the corresponding components of the MS. Data collection involved measuring oxygen consumption rate at increasing swimming speeds, using the gait transition from steady to unsteady (burst-assisted) swimming to detect the onset of anaerobic metabolism. Results provided evidence of the locomotor performance trade-off, but only in S. aurata. In contrast, both species revealed significant negative correlations between aerobic and anaerobic components of the MS, indicating a trade-off where both components of the MS cannot be optimized simultaneously. Importantly, the fraction of the MS influenced by anaerobic metabolism was on average 24.3 and 26.1% in S. aurata and P. reticulata, respectively. These data highlight the importance of taking anaerobic metabolism into account when assessing effects of environmental variation on the MS, because the fraction where anaerobic metabolism occurs is a poor indicator of sustainable aerobic performance. Our results suggest that without accounting for anaerobic metabolism within the MS, studies involving the OCLTT hypothesis could overestimate the metabolic scope available for sustainable activities and the ability of individuals and species to cope with climate change.

Keywords: Aerobic metabolic scope; Trinidadian guppy (Poecilia reticulata); anaerobic metabolism; oxygen- and capacity-limited thermal tolerance (OCLTT); sea bream (Sparus aurata); trade-off.

Figure 1:

(A) Conceptual model and (B and C) raw data describing the metabolic rate as a function of swimming speed. (A) Schematic illustration showing the metabolic rate as function of swimming speed, including metabolic scope (MS; (black double-headed arrow) and gait transition speed (U_GT) as the highest sustainable swimming speed, equivalent to U_STmax of Peake (2008). Using U_GT, swimming performance is partitioned into sustainable (ranging from zero speed to U_GT) and unsustainable (swimming speeds higher than U_GT until U_max) components. The metabolic rate at U_GT is used to distinguish between sustainable metabolic scope (MS_sus; blue double-headed arrow) and unsustainable metabolic scope (MS_unsus; red double-headed arrow). (B and C) Raw data showing oxygen consumption rate ($\dot{M}$O₂; in milligrams of oxygen per kilogram per hour) as a function of swimming speed (in centimetres per second) in an individual Trinidadian guppy (Poecilia reticulata; B) and gilthead sea bream (Sparus aurata; C) used in this study. Data are adapted from Svendsen et al. (2013, 2015). Grey symbols represent $\dot{M}$O₂ when no burst-assisted swimming occurred, whereas red symbols represent $\dot{M}$O₂ when burst-assisted swimming occurred.

Figure 2:

Burst swimming in gilthead sea bream (S. aurata; body length 14.5 cm), with bursts indicated using grey shading. Data were collected in a respirometry chamber [32 cm × 9 cm × 11 cm (length × width × height)], with the water speed adjusted to 48 cm s⁻¹. (A) Longitudinal position of fish snout in the chamber. Bursts are associated with forward movement (grey shading) and followed by backwards movement in the chamber. The y-axis denotes the distance (in centimetres) from the most downstream end of the chamber. (B) Lateral movements of the tail tip as recorded dorsally, with increased tail beat frequency and amplitude providing thrust for each burst. (C) Fish swimming speed in the chamber, with peaks approaching 90 cm s⁻¹ during bursts and speeds below the adjusted water speed (48 cm s⁻¹; indicated by a dashed red line) after bursts. Note that the fish is moving backwards in the chamber (A) when the swimming speed is below 48 cm s⁻¹ (C).

Figure 3:

(A and B) Relationships between sustainable (U_sus) and unsustainable (U_unsus) swimming performances (see Fig. 1A for details). (C and D) Relationships between U_sus and the fraction (percentage) of U_max constituted by U_unsus. Significant relationships for gilthead sea bream (S. aurata) were found between U_sus and U_unsus (A), and between U_sus and the fraction (percentage) of U_max constituted by U_unsus (C). (B and D) No significant relationships were found in Trinidadian guppy (P. reticulata).

Figure 4:

(A and B) Relationships between sustainable metabolic scope (MS_sus) and unsustainable metabolic scope (MS_unsus; see Fig. 1A for details). (C and D) Relationships between MS_sus and the fraction (%) of MS constituted by MS_unsus, Significant negative relationships between MS_sus and MS_unsus or the fraction (percentage) of MS constituted by MS_unsus were found in both gilthead sea bream (S. aurata; A and C) and Trinidadian guppy (P. reticulata; B and D).