Contributions of reproductive experience to observation - maintained crop growth and incubation in male and female ring doves

Previous work has established that experienced male ring doves (Streptopelia risoria) can maintain prolactindependent crop growth and readiness to incubate by observing an incubating partner. We report that this is also true for female ring doves. The role of experience in this phenomenon was examined in separate experiments with males and females. Observation of an incubating mate from 3 days after completion of egg laying is sufficient to maintain crop growth and incubation in both male and female ring doves in their second, but not in their first, reproductive cycle. Male and female doves in their first cycle must incubate for a greater part of the cycle before observation of an incubating mate is an effective stimulus; there are no differences between first and second cycle doves separated by a glass plate from the mate and nest 8 days after laying. Experience obtained within the first cycle apparently ensures that previously neutral stimuli come to elicit prolactin secretion. The effectiveness of these stimuli is reinstated early in a second cycle. Article: Incubation and care of the young are shared by the male and female of a mated pair of ring doves. During incubation the crop sacs of both birds grow from an initial empty weight of about 600 mg to over 3000 mg (Hansen 1966; Friedman & Lehrman 1968). This rapid growth results in the sloughing off of epithelial cells into the lumen to form crop `milk', the characteristic food for young doves and pigeons (Beams & Meyer 1931). Both parents regurgitate crop milk to the young as their principal source of nourishment during the early posthatching period. By 3 weeks after hatching, crop weight has regressed to resting state in ring doves (Goldsmith et al. 1981), and the young are feeding independently. Although there may be synergistic effects of other hormones, prolactin is necessary for crop growth (Bates et al. 1962). Furthermore, except at the extremes, there is a close correlation between circulating prolactin level and crop weight in incubating ring doves (Goldsmith et al. 1981; Cheng & Burke 1983). An increase in crop weight, therefore, can be used as a valid indicator of prolactin secretion and a valid estimator of plasma prolactin level over most of the range in which prolactin varies. Prolactin secretion may, however., escape detection by crop growth at the low levels characteristic of early incubation, and changes within the very high prolactin levels characteristic of late incubation may not be reflected in crop weight changes (Cheng & Burke 1983). Prolactin is secreted during incubation in doves and pigeons as a result of exposure to the stimulus conditions associated with sitting on eggs. Thus, if incubating doves (Lehrman & Brody 1964) or pigeons (Patel 1936) are removed from their nests before crop growth has started, growth will not begin, and if they are removed from the nest after crop growth has begun, the crop will regress back to the resting state and prolactin levels will fall sharply (Silver 1984). However, if males are removed from their nests to an adjacent cage from which they can observe their incubating mates, then their crops will continue to grow as though they were also incubating (Patel 1936; Friedman & Lehrman 1968). Thus, observation of an incubating mate can provide the stimulus conditions required for maintaining prolactin secretion in males of these species during the incubation phase of a breeding cycle. Friedman & Lehrman (1968) examined the conditions under which observation of an incubating mate would maintain crop growth and readiness to incubate in male ring doves separated from their mates by a glass plate. By testing incubation, and measuring crop growth at the end of the incubation phase of the cycle for nine different groups of males, each separated by a glass partition from their incubating mates at different phases of the cycle, they found that the male must have been sitting on a clutch of eggs for at least 3 days before observation was sufficient to maintain crop growth and incubation state. Separation before 3 days would prevent observation-maintained crop growth and readiness to incubate. Males that were separated after 3 days showed crop weights at the end of the incubation phase (9 days later) that were equivalent to those of males that had not been separated from contact with their mates and nests during that time. Thus, observation of their incubating mate provided the males with conditions that promoted a pattern of prolactin secretion similar to that which would have occurred if they had continued to participate in incubation. Since males separated on the third day readily reestablished incubation at the end of their 9 days of separation from their mates, the prolactin secreted as a result of observing the mate not only continued the growth of the crop but also apparently maintained a state of readiness to incubate (Lehrman & Brody 1964). Thus, these males would have been quite capable of feeding and brooding newly hatched young, despite their physical separation from their mate and nest for most of the incubation phase of the cycle. The male's ability to maintain crop growth by observing his incubating mate has been assessed only in reproductively experienced doves. However, the secretion of prolactin and the growth of the crop are influenced by several different kinds of visual and tactile cues (Lehrman & Brody 1964; Hansen 1966, 1971a; Buntin 1977), and the effectiveness of these influences can differ according to the breeding experience of the doves being tested (Hansen 1971b, 1973). It is possible that reproductively naive and experienced males will differ in their responsiveness to stimuli provided by observing an incubating mate. Although males and females share incubation and care of young, they may not respond equally to the various factors that regulate these behaviours. For example, incubation may be more dependent on endocrine state in females than in males (Silver & Buntin 1973), and females are more sensitive than males to certain non-tactile stimulation of crop growth by squabs during the post-hatching period (Buntin et al. 1977). Since females do most of the incubating and incubate throughout the dark phase of the diurnal cycle (Gerlach et al. 1975), the regulation of prolactin secretion by females during the incubation phase of the cycle may differ from that of males. Therefore, the present study examines the ability of reproductively naive and experienced male and female ring doves to maintain crop growth and readiness to incubate when they are prevented from incubating, but are allowed to observe the incubation of their companion.