Noninvasive Determination of Embryonic Heart Rate during Hatching in the Brown Noddy (Anous stolidus)

-We used an audiocartridge system, which measures the ballistic movements of the egg attributable to embryonic cardiac contractions, to determine the heart rate (HR) of the Brown Noddy (Anous stolidus) before and during the prolonged hatching process. The average heart rate at 36? C in 8 embryos (mean fresh egg weight = 38 g) was 262 beats/min (bpm) on the last day of prepipping, and 264 bpm on the first day of shell fracture (external pipping). Heart rate increased to 291 bpm after penetration of the air cell by the beak (internal pipping), and increased to 310 bpm on the last day of incubation. With a few exceptions, the heart rate, which did not change systematically during the last stage of prepipping, remained unchanged early in external pipping and then increased markedly with the initiation of pulmonary respiration. Changes in heart rate during hatch may be related to increases in the oxygen consumption of the embryo. The heart rate was highly variable even at constant ambient temperatures. It changed according to a temperature coefficient (Q,o) of 2 at all developmental stages, when the ambient temperature was modified 2? C from the control (36? C). Received 26 February 1990, accepted 29 December 1990. MANY seabirds breeding in the Hawaiian Archipelago pass through a prolonged hatching process (Pettit and Whittow 1983a, b). Hatching begins with shell fracture (external pipping) and is followed by penetration of the air cell by the beak through the chorioallantoic membrane (internal pipping), which initiates pulmonary respiration (Pettit and Whittow 1982a, b). Although the gas exchange during the hatching process of seabirds has been well studied (see references in Rahn et al. 1985), there are scanty data on the circulatory system. Noninvasive systems to measure embryonic heart rate (HR) take advantage of the calcareous hard shell of the egg, which moves periodically because of the cardiac contractions of the embryo (Cain et al. 1967; Suzuki et al. 1989; Tazawa et al. 1989a, b; Hashimoto et al. 1991). Measurements are based on ballistocardiography and various transducers are employed: piezoelectric transducer (Cain et al. 1967), moving-magnet type audiocartridge (Suzuki et al. 1989, Tazawa et al. 1989a), laser speckle meter (Tazawa et al. 1989b), and laser displacement meter (Hashimoto et al. 1991). Although the physical measurements determined with these transducers are different (Hashimoto et al. 1991), in each case the heart rate of the embryo can be counted from the cardiogenic ballistic waves produced (referred to as the ballistocardiogram). We used an audiocartridge measuring system to elucidate the changes in heart rate of the Brown Noddy (Anous stolidus) during development, particularly just before and during the prolonged pip-to-hatch period. We also estimated the effect of ambient temperature change on the embryonic heart rate. Previously, the initiation of embryonic thermogenesis in the Brown Noddy was determined from the 02 consumption before, during, and after hatching (Matsunaga et al. 1989). We used the Brown Noddy because 02 consumption data were available as a reference point. MATERIALS AND METHODS Eggs were collected on Manana Island, a small offshore island of Oahu in the main Hawaiian Islands. They were brought to the laboratories at the University of Hawaii within 3 h of collection and numbered on the eggshell to distinguish individuals. We measured the length (L, in cm) and maximum breadth (B, in cm) with a micrometer to 0.01 cm, and estimated the fresh mass (W, in g) of each egg from the equation (Hoyt 1979), W = 0.534-LB2. Eggs were incubated at 36? C and 55-60% relative humidity in a forced-draft incubator and turned twice daily (morning and eve594 The Auk 108: 594-601. July 1991 This content downloaded from 157.55.39.11 on Sun, 17 Apr 2016 07:56:59 UTC All use subject to http://about.jstor.org/terms July 1991] Heart Rate during Hatching 595 j. ,, tj ~ ~ ~ . . . . . . . : . .! : ! . 1! 1 r . X 1 Fig. 1. Ballistocardiograms recorded with the audiocartridge measuring system during external pipping (top panel) and internal pipping (center and lower panels). Each record is of 8-s duration. ning). Regular turning was continued until external pipping. The measuring system was described elsewhere (Suzuki et al. 1989, Tazawa et al. 1989a) and is briefly summarized here. Eggs were transferred from the incubator to a Hotpack environmental chamber every day. The chamber was kept at 36? C and contained a floating platform suspended from a frame. An audio-