scholarly journals Universal metabolic constraints shape the evolutionary ecology of diving in animals

2020 ◽  
Vol 287 (1927) ◽  
pp. 20200488 ◽  
Author(s):  
Wilco C. E. P. Verberk ◽  
Piero Calosi ◽  
François Brischoux ◽  
John I. Spicer ◽  
Theodore Garland ◽  
...  

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.

1986 ◽  
Vol 120 (1) ◽  
pp. 351-367 ◽  
Author(s):  
DENNIS M. HUDSON ◽  
DAVID R. JONES

Pekin ducks, ranging in mass from 0.05 to 3.5 kg, were force-dived to determine the maximum tolerance to diving asphyxia. The size of the respiratory and blood oxygen storage compartments and oxygen utilization during the dive were also measured. By the end of a maximum dive, less than 4% of the original O2 store remained in the blood, whereas almost 25% remained in the respiratory system. In contrast, the level of arterial glucose did not change significantly during diving. The relationship of a number of measured variables to body mass was analysed using linear regression analysis on logio-transformed variables to generate power equations of the form Y = aXb (Y, any variable; X, body mass; a, mass coefficient; b, mass exponent). The mass exponent was 1.19 for the total oxygen stores and 0.64 for maximum diving duration. Using measurements of brain and heart mass and literature estimates of the scaling of O2 consumption, it was also possible to predict a mass exponent aerobic metabolism by these organs during a maximum dive. Allometric cancellation of mass exponents for O2 availability and predicted utilization resulted in a residual mass exponent almost identical to the measured value for maximum dive duration. Thus it is possible to predict the relationship of maximum underwater endurance to body mass in Pekin ducks from a knowledge of the oxygen consumption by, and availability to, the central aerobic organs.


2021 ◽  
Author(s):  
Tommy Norin

Metabolic rate (MR) changes with body mass (BM) as MR = aBMb, where a is a normalisation constant (log–log intercept) and b the scaling exponent (log–log slope). This scaling relationship is fundamental to biology and widely applied, yet a century of research has provided little consensus on why and how steeply metabolic rate scales with body mass. I here show that ontogenetic (within-individual) b can be strongly and positively related to growth rates of juvenile fish when food availability is naturally restricted, with fast growing individuals having steep and near-isometric metabolic scaling (b ≈ 1). I suggest that the steep evolutionary (among-species) scaling also found for fishes (b also approaching 1) is a by-product of natural selection for these fast growing individuals early in ontogeny, and that a weaker relationship between metabolic scaling and growth later in life causes variation in b at lower taxonomic levels (within orders or species). I support these ideas by showing that b within fish orders is linked to natural mortality rates of fish larvae.


ZooKeys ◽  
2020 ◽  
Vol 982 ◽  
pp. 149-159
Author(s):  
Andrzej Antoł ◽  
Jan Kozłowski

The persistent enigma of why the whole-body metabolic rate increases hypoallometrically with body mass should be solved on both the ultimate and proximate levels. The proximate mechanism may involve hyperallometric scaling of metabolically inert tissue/organ masses, hypoallometric scaling of metabolically expensive organ masses, a decrease in mass-specific metabolic rates of organs or a combination of these three factors. Although there are literature data on the tissue/organ masses scaling, they do not consider phylogenetic information. Here, we analyse the scaling of tissue/organ masses in a sample of 100 mammalian and 22 bird species with a phylogenetically informed method (PGLS) to address two questions: the role of phylogenetic differences in organ/tissue size scaling and the potential role of organ/tissue mass scaling in interspecific metabolic rate scaling. Strong phylogenetic signal was found for the brain, kidney, spleen and stomach mass in mammals but only for the brain and leg muscle in birds. Metabolically relatively inert adipose tissue scales isometrically in both groups. The masses of energetically expensive visceral organs scale hypoallometrically in mammals, with the exception of lungs, with the lowest exponent for the brain. In contrast, only brain mass scales hypoallometrically in birds, whereas other tissues and organs scale isometrically or almost isometrically. Considering that the whole-body metabolic rate scales more steeply in mammals than in birds, the mass-specific metabolic rate of visceral organs must decrease with body mass much faster in birds than in mammals. In general, studying whole-body metabolic rate is not adequate for explaining its scaling, and measuring metabolic rates of organs, together with their contribution to body mass, is urgently required.


2018 ◽  
Vol 314 (4) ◽  
pp. R563-R573 ◽  
Author(s):  
Mun Aw ◽  
Tamara M. Armstrong ◽  
C. Michele Nawata ◽  
Sarah N. Bodine ◽  
Jeeeun J. Oh ◽  
...  

In general, the mammalian whole body mass-specific metabolic rate correlates positively with maximal urine concentration (Umax) irrespective of whether or not the species have adapted to arid or mesic habitat. Accordingly, we hypothesized that the thick ascending limb (TAL) of a rodent with markedly higher whole body mass-specific metabolism than rat exhibits a substantially higher TAL metabolic rate as estimated by Na+-K+-ATPase activity and Na+-K+-ATPase α1-gene and protein expression. The kangaroo rat inner stripe of the outer medulla exhibits significantly higher mean Na+-K+-ATPase activity (~70%) compared with two rat strains (Sprague-Dawley and Munich-Wistar), extending prior studies showing rat activity exceeds rabbit. Furthermore, higher expression of Na+-K+-ATPase α1-protein (~4- to 6-fold) and mRNA (~13-fold) and higher TAL mitochondrial volume density (~20%) occur in the kangaroo rat compared with both rat strains. Rat TAL Na+-K+-ATPase α1-protein expression is relatively unaffected by body hydration status or, shown previously, by dietary Na+, arguing against confounding effects from two unavoidably dissimilar diets: grain-based diet without water (kangaroo rat) or grain-based diet with water (rat). We conclude that higher TAL Na+-K+-ATPase activity contributes to relationships between whole body mass-specific metabolic rate and high Umax. More vigorous TAL Na+-K+-ATPase activity in kangaroo rat than rat may contribute to its steeper Na+ and urea axial concentration gradients, adding support to a revised model of the urine concentrating mechanism, which hypothesizes a leading role for vigorous active transport of NaCl, rather than countercurrent multiplication, in generating the outer medullary axial osmotic gradient.


1997 ◽  
Vol 75 (3) ◽  
pp. 339-358 ◽  
Author(s):  
Jason F. Schreer ◽  
Kit M. Kovacs

Maximum diving depths and durations were examined in relation to body mass for birds, marine mammals, and marine turtles. There were strong allometric relationships between these parameters (log10 transformed) among air-breathing vertebrates (r = 0.71, n = 111 for depth; r = 0.84, n = 121 for duration), although there was considerable scatter around the regression lines. Many of the smaller taxonomic groups also had a strong allometric relationship between diving capacity (maximum depth and duration) and body mass. Notable exceptions were mysticete cetaceans and diving/flying birds, which displayed no relationship between maximum diving depth and body mass, and otariid seals, which showed no relationship between maximum diving depth or duration and body mass. Within the diving/flying bird group, only alcids showed a significant relationship (r = 0.81, n = 9 for depth). The diving capacities of penguins had the highest correlations with body mass (r = 0.81, n = 11 for depth; r = 0.93, n = 9 for duration), followed by those of odontocete cetaceans (r = 0.75, n = 21 for depth; r = 0.84, n = 22 for duration) and phocid seals (r = 0.70, n = 15 for depth; r = 0.59, n = 16 for duration). Mysticete cetaceans showed a strong relationship between maximum duration and body mass (r = 0.84, n = 9). Comparisons across the various groups indicated that alcids, penguins, and phocids are all exceptional divers relative to their masses and that mysticete cetaceans dive to shallower depths and for shorter periods than would be predicted from their size. Differences among groups, as well as the lack of relationships within some groups, could often be explained by factors such as the various ecological feeding niches these groups exploit, or by variations in the methods used to record their behavior.


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