Avian Reproduction over an Altitudinal Gradient: Incubation Period, Hatchling Mass, and Embryonic Oxygen Consumption

-Embryonic oxygen consumption, incubation period, and hatchling mass do not vary significantly among populations of Red-winged Blackbirds (Agelaius phoeniceus) breeding over a 2,900-m altitudinal gradient, despite a 28% decrease in oxygen tension from the lowest to the highest altitude. Calculations suggest that embryos develop normally at 2,900 m at air-cell 02 tensions of 7.1 kPa. The regulation of loss of water vapor or CO2 by a reduction of eggshell conductance appears to have been more important for populations breeding in montane environments than maximizing 02 availability to the embryo. The superior tolerance to hypoxia demonstrated by embryos of wild birds, compared to that of embryos of domestic chickens, may relate to the modification of the diffusive resistance of 02 inside the shell. Received 28 September 1981, accepted 24 April 1982. THE ability of a species to invade a new habitat and to establish permanent residency there depends importantly upon successful reproduction. Avian species have exploited a remarkable diversity of habitats. This success is particularly striking in view of the potential vulnerability of avian embryos to environmental stresses. Because avian embryos develop externally from the body of the adult, they are less protected by the homeostatic systems of the adult than are embryos of viviparous vertebrates. Although the physiology of avian embryos has received considerable attention during the last decade, embryonic tolerances of and adaptations to harsh environments have received little study. Avian embryos exchange gases with the environment by diffusion (Wangensteen et al. 1970/71). The diffusive flux of 02 into the egg, and CO2 and water vapor outwards, is described by a modification of the Fick equation (Wangensteen et al. 1970/71, Paganelli et al. 1975): M = (DIRT) (ApIL) -AP (1) Present address: Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721 USA. where M = gas flux (cm3 STPD * s-1), D = diffusion coefficient (cm2 * s-1), Ap = effective pore area (cm2), L = length of diffusion path or shell thickness (cm), RT = gas constant and absolute temperature (cm3 STPD cm-3 kPa-'), and AP = partial pressure difference of gas across shell (kPa). The terms (DIRT)(ApIL) are often combined into the term "G" (cm-3 s-l kPa-1), representing the conductance of the eggshell to each gas (Ar et al. 1974). The progressive decrease in barometric pressure, PB, in montane habitats is an environmental gradient that poses distinct problems for diffusive respiratory systems. Equation 1 suggests two factors that should become progressively more important to avian development as PB falls with increasing altitude. First, 02 flux (MC2) is influenced by the Po2 difference across the eggshell (AP02). Because ambient Po2 falls as PB decreases, the driving force for 02 diffusion will decrease unless internal P02 is lowered commensurately. Therefore, an embryo may not obtain sufficient 02 above certain altitudes to sustain normal metabolism and growth. Second, theoretical predictions and empirical results show that D is inversely proportional to PB (Reid and Sherwood 1966, Paganelli et al. 1975). Therefore, gases exchanged between the embryo and the environment will diffuse more rapidly as PB decreases with al710 The Auk 99: 710-718. October 1982 This content downloaded from 157.55. 39.187 on Wed, 30 Mar 2016 05:48:07 UTC All use subject to http://about.jstor. org/terms October 1982] Avian Reproduction and Altitude 711 titude, if all other factors in Eq. 1 are constant. The enhanced diffusion of 02 into the egg may compensate in part for the detrimental effects of hypoxia on metabolism (Visschedijk et al. 1980), but augmented rates of diffusion of CO2 and water vapor from the egg during incubation may prove harmful to normal embryonic growth (Rahn et al. 1977, Carey 1980). Therefore, successful breeding by montane populations of birds has undoubtedly required that the resistant properties of the eggshell to gaseous diffusion be designed to meet the demands for maximizing 02 supply and minimizing excessive losses of CO2 and water vapor at high elevations. Tolerance to hypoxia has been studied thus far only in embryos of domestic fowl (Gallus domesticus). They are unable to maintain normal levels of metabolism or growth when subjected acutely or for the duration of incubation to moderate hypoxia (Visschedijk et al. 1980). Growth and metabolism of embryos obtained from a colony of chickens raised for more than 15 yr at 3,800 m were significantly reduced below control levels (Wangensteen et al. 1974). These results raise interesting questions concerning the abilities of embryos of wild birds breeding at high altitudes to obtain sufficient 02 for normal metabolism and growth. The purpose of this study was to evaluate 02 Uptake directly by measuring embryonic metabolic rate and indirectly by studying incubation period, hatchling mass, and embryonic mortality in Red-winged Blackbirds (Agelaius phoeniceus) breeding over a 2,900-m altitudinal gradient.