Ontogeny of cardiovascular control in amphibians

American Zoologist, Feb 1997 by Regina Fritsche

SYNOPSIS. Cardiovascular variables in developing amphibians are affected by both allometry and organogenesis. Blood pressure, cardiac output, and stroke volume increase during development, whereas peripheral resistance decreases. Invariably, resting heart rate changes as development proceeds from embryo through larva to adult. The pattern of change, however, varies between species and does not even correlate with family. The mechanisms underlying these varying patterns of developmental changes in heart rate of anuran amphibians larvae awaits complete description. Cardiovascular variables in adult vertebrates are influenced by nerves and hormones as well as intrinsic factors. However, information on the development of cardiovascular control systems is scarce, but receptor sensitivity apparently develops before functional innervation becomes apparent. The amphibian heart responds to acetylcholine and adrenaline several stages before functional innervation becomes evident, and in some species the cholinergic and adrenergic sensitivity of the cardiac pacemaker changes with development. As in mammals, acute hypoxia results in different cardiovascular responses depending on the developmental stage of the animal. The different responses reflect the relative maturity of neurohormonal mechanisms operating within the cardiovascular system.

Ontogeny of Cardiovascular Control in Amphibians1

INTRODUCTION

Cardiovascular control is well documented in adult animals and neuronal, humoral, and intrinsic regulation have been described for representatives from the different vertebrate groups (for review see Nilsson, 1983). However, all animals start out as a single cell which after fertilisation divides to form a multicellular embryo. During the process of ontogeny, organs develop and various physiological processes become functional. Some of the most complex developmental transitions occur in the cardiovascular and respiratory systems as an animal makes the transition from embryonic/ fetal/larval life to that of a free-living animal. Adults do not always show the most complex physiological processes. Developing animals are often challenged in much the same way as the adult and must likewise be able to survive conditions of reduced oxygen availability and temperature changes. However, information on the development of the cardiovascular control systems and on the effects of environmental perturbations is scarce. If "critical windows" exist during the developmental period when a specific organ or structure is particularly sensitive to environmental changes, defining these "critical windows" will be of great importance. This review summarises what we know about the development of cardiovascular control systems in amphibians.

AMPHIBIANS AND EMBRYOLOGICAL STUDIES

Amphibians have been used extensively as model animals for studying anatomical changes during vertebrate development, but the majority of physiological experiments have been performed on a few mammalian (most often the fetal lamb) or avian species (usually the chick embryo) (e.g., Girard, 1973; Petery and Mierop, 1974; Dawes et al., 1980; Wispee et al., 1983; Dawes, 1985; Persson et al., 1989; Campbell et al., 1992). However, because of difficulties in instrumenting embryos in utero, most physiological measurements in developing mammals have been made on the later fetal stages rather than in the early embryo. Intravascular recordings in bird embryos necessitate opening of the shell, a process that may have significant consequences on the measured cardiovascular variables.

Against this background, amphibians have become important model animals in studying early cardiovascular development (Burggren and Pinder, 1991; Pelster et al., 1993; Burggren and Just, 1992; Burggren and Warburton, 1994; Burggren, 1995; Burggren and Fritsche, 1995; Fritsche and Burggren, 1996). Amphibians possess important advantages for embryological studies. Some species are easily induced to breed in the laboratory; the larvae have a relatively short life cycle and are easily reared; and relatively large, often transparent eggs are produced in great quantities. Videomicroscopic techniques can be used for heart rate and stroke volume determination without any surgical intervention on transparent animals. Apart from being excellent model animals for understanding how the early vertebrate cardiovascular system develops, the diversity among amphibians together with the complexity involved in the transition from water to air-breathing (Burggren and Infantino, 1994) are ample reasons to study amphibian cardiovascular development.

CARDIOVASCULAR DEVELOPMENT IN AMPHIBIANS

During the last decade or so, several studies have been performed on physiological development of the cardiovascular system in anuran amphibians. A major reason for this upsurge is the recent advances in microtechniques which allow measurements of blood pressure and blood flow in animals weighing as little as a few milligrams (see Burggren and Fritsche, 1995, for a recent review).