Endocrine control of hydromineral balance in bird embryos

Endocrine Control of Hydromineral Balance in Bird Embryosl

MICHAEL J. MURPHY2

Department of Natural Sciences College of Agriculture and Technology, State University of New York, Cobleskill, New York 12043

SYNOPSIS. Amniotes undergoing oviparous development are exquisitely accessible to physiological measurement and manipulation. Further, interpretation of data obtained from studying these embryos is less complicated than that obtained for placentals, where maternal regulatory actions may account, at least in part, for fetal homeostasis. Nevertheless, surprisingly little is known about the developmental physiology of hydromineral balance in bird and reptile embryos, especially when compared to information gleaned from mammalian concepti. The data are even more scarce for specific homeostatic mechanisms which involve embryonic or maternally deposited hormones. Published reports fall into three general categories, the majority of which concern direct or indirect evidence for hypophyseal actions: (1) Classic endocrine organ-deletion experiments involving hypophysectomy (partial decapitation) of chicken embryos. The data strongly suggest that one or more pituitary factors normally act to reduce fluid volumes and electrolyte concentrations of the allantois and to maintain the relatively high sodium and chloride gradients between the allantois and the other embryonic or extraembryonic compartments. Adrenocorticotrophic hormone (ACTH), prolactin (PRL), and arginine vasotocin (AVT) have been implicated as potentially important pituitary hormones involved in these actions. (2) Treatment of embryos with a variety of exogenous hormones, including PRL, growth hormone, and 1, 25 dihydroxycholecalciferol (the hormonal form of vitamin D). These hormones have their most profound effect on the allantoic compartment as well as the yolk sac (vitamin D), resulting in altered fluid volumes and/or perturbations of the fluid electrolytes. (3) Ontogeny of synthesis of hormones with suspected osmoregulatory functions and the subsequent appearance of these hormones in embryonic plasma. This latter group includes synthesis and release of embryonic hormones in response to osmotic challenge during development. The data from these three related areas, combined with basic developmental physiology work, suggest that the target organs for the hormones involved in hydromineral regulation in bird embryos are likely to include the embryonic kidneys as well as the membranes of the extraembryonic compartments, especially the allantois.

INTRODUCTION

Amniote embryos developing in shelled eggs face at least two major hydromineral challenges during development: (1) moving massive amounts of water and salts contained in the albumen and the yolk to the temporary storage compartments of the amnion, allantois, yolk sac, and extraembryonic coelom, and (2) "re"-moving these components to the embryonic circulation and, ultimately, to the embryo proper. (Embryos in the softer shelled eggs of some reptiles must also rely on water absorption from the surrounding environment to supplement water needs during development). As reviewed elsewhere (for example, see Murphy et al., 1991; Wenz et al., 1992) fluid accumulates in the amnion probably as a result of chloride being pumped into this compartment with water following passively. Unlike placental amniotes, there exists no urachal opening into the chick amnion for urine flow into this compartment. The allantois, conversely, accumulates fluid primarily as a result of kidney filtration of plasma; the filtrate that enters the allantois via the allantoic stalk, causing its initial expansion. Allantoic fluid becomes increasingly hypoosmotic to embryonic plasma during incubation due the movement of sodium and chloride across the allantois into the blood. While these massive fluxes are occurring across the embryonic epithelia, the embryo must maintain the relative stability of the embryonic plasma. Studies of these movements in the chick embryo have been favored by accessibility considerations, where fenestration of eggs or shellless culture is routinely utilized (for example, see Packard and Clark, 1987; Murphy et al., 1986; Selleck, 1996). In addition, developmental physiology during embryonic periods in cleidoic eggs is unaffected by direct maternal regulatory actions, as occurs in placentals. Indications of endocrine regulation of hydromineral balance have come from basic physiology experiments elucidating water and electrolyte shifts, particularly in the allantoic compartment, in the face of hydric stress (Buhr, 1995; Davis and Ackerman, 1987; Davis et al., 1988) or saltloading (Zemanova and Babicky, 1990) during development. In addition, studies with shell-less culture (for example, see Packard and Clark, 1987) have demonstrated that resorption of allantoic fluid is exquisitely sensitive to a number of conditions which may also include non-endocrine factors (culture conditions, Ca++ availability).

Some of the older reports in the literature are particularly difficult to interpret since only one aspect of water and electrolyte balance was examined during any single observational period. For example, reduction in allantoic fluid volume cannot be explained as a reduction in urinary output or resorption via the allantoic epithelium unless both are actually measured or individually account for the full volume change in this compartment. Current methods are rapidly improving, however, which allow a more complete compartmental analysis during chick development (for example, see Murphy et al., 1991). Further, a number of researchers have developed methods for studying the physiology of even the early mesonephros, including whole-animal and single-nephron glomerular filtration rate and renal clearance of electrolytes (Clark et al., 1993; Friebova-Zemanov et al., 1982; Murphy et aL, 1991; Murphy and Clark, 1990; Wenz et al., 1992: Zemanova et al., 1993). This present work focuses on those studies directly concerned with the endocrine control of water and salt balance during embryonic development of the chick (see Table 1).