Aerobic power and flight capacity in birds: a phylogenetic test of the heart-size hypothesis

Abstract

Flight capacity is one of the most important innovations in animal evolution; it only evolved in insects, birds, mammals and the extinct pterodactyls. Given that powered flight represents a demanding aerobic activity, an efficient cardiovascular system is essential for the continuous delivery of oxygen to the pectoral muscles during flight. It is well known that the limiting step in the circulation is stroke volume (the volume of blood pumped from the ventricle to the body during each beat), which is determined by the size of the ventricle. Thus, the fresh mass of the heart represents a simple and repeatable anatomical measure of the aerobic power of an animal. Although several authors have compared heart masses across bird species, a phylogenetic comparative analysis is still lacking. By compiling heart sizes for 915 species and applying several statistical procedures controlling for body size and/or testing for adaptive trends in the dataset (e.g. model selection approaches, phylogenetic generalized linear models), we found that (residuals of) heart size is consistently associated with four categories of flight capacity. In general, our results indicate that species exhibiting continuous hovering flight (i.e. hummingbirds) have substantially larger hearts than other groups, species that use flapping flight and gliding show intermediate values, and that species categorized as poor flyers show the smallest values. Our study reveals that on a broad scale, routine flight modes seem to have shaped the energetic requirements of birds sufficiently to be anatomically detected at the comparative level.

Maladaptive phenotypic plasticity in cardiac muscle growth is suppressed in high‐altitude deer mice

“…Increases in left ventricle size are generally assumed to be beneficial for O 2 transport by augmenting stroke volume and cardiac output (Nespolo et al. ), and would likely be adaptive at high altitudes. However, this might not always be the case if left ventricle growth comes at the cost of a reduction in the size of the ventricle lumen, which could act to impair the filling of the heart and impede output.…”

“…; Nespolo et al. ), and should be adaptive so long as increases in left ventricle size do not come at the cost of reduced lumen volume. This is not true for the right ventricle of the heart, which pumps blood through the pulmonary circulation, and for which hypertrophy in response to hypoxia is symptomatic of a suite of maladaptive physiological responses.…”

Comparative analysis of avian hearts provides little evidence for variation among species with acquired endothermy

“…We do not know of data that suggests that the variation in these features among birds may be greater than it is in mammals. Also, even though heart weight varies substantially between birds (Nespolo et al, 2018) and, for example, Golden-collared manakins have some 20% greater cardiac mass and left ventricular wall thickness than similar-sized zebra finches (Barske et al, 2019) mammals also have a substantially varied, heart weight (Bishop, 1997;Seymour & Blaylock, 2000). For example, the heart weight of captive pronghorn antelopes is twice that of similarly sized goats (McKean & Walker, 1974).…”

Approaches for testing hypotheses for the hypometric scaling of aerobic metabolic rate in animals

“…There is no evidence for an evolved compensatory response to a putative O 2 limitation in larger birds. Systemic O 2 transport capacity scales similarly relative to O 2 uptake rates as in other vertebrates (87), respiratory surface area scales hypometrically as in mammals (128), larger birds have a slightly thicker pulmonary diffusion barrier (128), heart size scales slightly hypometrically (144), and larger birds have larger cell sizes (114), all arguing against the hypothesis that constraints on O 2 delivery drive the lower MR/g in larger birds.…”