Universal metabolic constraints shape the evolutionary ecology of diving in animals

Abstract

Diving as a lifestyle has evolved on multiple occasions when air-breathing terrestrial animals invaded the aquatic realm, and diving performance shapes the ecology and behaviour of all air-breathing aquatic taxa, from small insects to great whales. Using the largest dataset yet assembled, we show that maximum dive duration increases predictably with body mass in both ectotherms and endotherms. Compared to endotherms, ectotherms can remain submerged for longer, but the mass scaling relationship for dive duration is much steeper in endotherms than in ectotherms. These differences in diving allometry can be fully explained by inherent differences between the two groups in their metabolic rate and how metabolism scales with body mass and temperature. Therefore, we suggest that similar constraints on oxygen storage and usage have shaped the evolutionary ecology of diving in all air-breathing animals, irrespective of their evolutionary history and metabolic mode. The steeper scaling relationship between body mass and dive duration in endotherms not only helps explain why the largest extant vertebrate divers are endothermic rather than ectothermic, but also fits well with the emerging consensus that large extinct tetrapod divers (e.g. plesiosaurs, ichthyosaurs and mosasaurs) were endothermic.

Keywords: allometry; ectothermy; endothermy; evolutionary physiology; palaeophysiology; scaling.

Figure 1.

Phylogenetic tree of all species (n = 226) used in the analyses, displaying maximum dive duration (length of outer bars) and body mass (gradient in branch colours). Outer bars are colour coded to represent reptiles (purple), mammals (green), insects (orange), birds (red) and amphibians (blue). For image credits see the electronic supplementary material. (Online version in colour.)

Figure 2.

Relationship between maximum dive duration and body mass, colour coded for different groups of animals (a), with 95% prediction intervals shown separately for ectotherms (in blue) and endotherms (in red). Partial residual plots show how maximum dive duration (min) changes with body mass (kg) (b), the index of oxygen storage capacity (c), and temperature (d), whereby species are colour coded according to being ectotherms (blue) or endotherms (red). Note the log₁₀ transformation for dive duration, body mass and the oxygen index. Linear regression equations are given in each plot (full details on the parameters can be found in table 1). Partial residual plots illustrate the relationship between the response variable (here maximum dive duration) and a given independent variable while accounting for the effects of other independent variables in the model. Hence variation in dive duration owing to differences in temperature is accounted for in plots (b) and (c), isolating the effects of body mass and the oxygen index respectively, whereas plot (d) isolates the effects of temperature by accounting for differences in body mass. For image credits see the electronic supplementary material. (Online version in colour.)