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Effect of parental feeding activity on squab-induced crop sac growth in ring doves (Streptopelia risoria)
HORMONES
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8, 297-309 (1977)
Effect of Parental Crop Sac Growth
Feeding Activity on Squab-Induced in Ring Doves (Streptopelia risoria)l
JOHN D. BUNTIN?
MEI-FANG CHENG, AND ERNST W. HANSEN
Institute
of Animal Behavior, Rutgers-the State University, Newark, New Jersey 07102
Effects of parental regurgitation feeding activity on crop sac development were studied in mate-separated male and female ring doves given 2 hr of daily exposure to food-deprived or recently fed squabs, for 4 consecutive days during the early posthatching period of the breeding cycle. In both sexes, food-deprived squabs stimulated more squab-directed activity, more parental regurgitation feeding activity, and greater crop sac development than recently fed young. Crop sac weights of males in both groups tended to be positively correlated with one or more parental activities. Correlations obtained in males exposed to food-deprived young further suggested that tactile stimuli associated with regurgitation behavior may promote crop sac development. In contrast to males, crop sac weights of females in both groups were not highly correlated with any type of contact-related parental activity or group of activities. These results, together with previous findings, suggest that nontactile stimuli from young played some role in mediating female crop sac weight differences in the two exposure conditions.
The crop sacs of male and female ring doves undergo a three- to four-fold increase in weight during the 2-week period of egg incubation (Hansen, 1966; Friedman and Lehrman, 1968). Although a number of hormones may participate in promoting full crop sac development (Bates et al., 1962; Meier et al., 1971; Raud and Ode& 1971), actual mucosal growth is stimulated by prolactin (Lyons, 1937; Riddle et al., 1933). About the time of hatching, epithelial cells begin to slough off from the crop sac wall (Beams and Meyer, 1931; Patel, 1936) to form crop “milk”. This substance is regurgitated to the young by both parents and provides their principal source of nourishment during the early posthatching period. The 4- to 5-day period of maximal crop “milk” production and parental regurgitation feeding activity which begins at hatching coincides with a period of accelerated crop sac growth in both parents. During this period, ’ This work was supported by USPHS-NIMH Predoctoral Fellowship MH 46279 to J. B. and NIMH Grant MH 02271 to M.-F. C. This study is based on a doctoral dissertation submitted by J. B. to the graduate school of Rutgers University. The technical assistance of Mr. Chuck Rosen is gratefully acknowledged. This is Contribution No. 238 from the Institute of Animal Behavior. 2 Present address: Department of Biology, Princeton University, Princeton, New Jersey 08540. 297 Copyright All rights
@ 1977 by Academic Press, Inc. of reproduction in any form reserved.
ISSN OOlg-506X
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the crop sac undergoes a 50% increase in empty weight over that achieved by the end of the incubation period (Hansen, 1966). During the remainder of the 21-day posthatching period, the crop sac gradually declines in weight and development as the growing young are fed less crop “milk” by their parents (Patel, 1936). Prior to hatching, stimuli received while sitting on eggs (Lehrman and Brody, 1964) and, under certain circumstances, visual cues provided by an incubating mate (Friedman and Lehrman, 1968) are effective in promoting crop sac development. After hatching, however, egg-related stimuli lose their effectiveness in sustaining crop sac growth, and further development depends upon the presence of young in the nest (Hansen, 1966; Buntin, 1977). The magnitude of crop sac growth has been shown to be influenced by the age of the squab (Hansen, 1971) and the type and amount of tactile stimulation received from the squab (Buntin, 1977). Moreover, these types of stimuli exert differential effects of crop sac growth in males and females. However, parent doves normally encounter these types of squab-related stimuli within the context of specific parent-young interactions, and no studies have examined the possibility that these various types of encounters differ in their crop sac growthpromoting effectiveness. Since parental regurgitation feeding behavior is a unique and prominent feature of the early posthatching period, it could be hypothesized that stimuli received during these interactions with young have a facilitative effect on crop sac development in both sexes. The experimental paradigm used to test this hypothesis was based on preliminary results indicating that the frequency of parental feeding activity is geared to the food requirements of the squab. Accordingly, the importance of parental feeding interactions in promoting crop sac growth was investigated by comparing crop sac weights of doves exposed to food-deprived and recently fed squabs during the early posthatching period. METHODS Subjects. The subjects were 37 adult male and 37 adult female ring doves which were hatched and raised in the breeding colony maintained at the Institute of Animal Behavior. Prior to use in the experiment, all birds had received one or two previous breeding experiences that consisted of successfully rearing at least one squab to 21 days of age. All birds were housed in visual isolation cages individually for 3-7 weeks prior to the start of the experiment. Procedure. Birds were initially paired with unfamiliar breeding partners and were placed in 82 x 46 x 36-cm breeding cages constructed of wood with wire-mesh front doors. Food, water, and mineral-grit mixture were continuously available. A transparent glass nest bowl measuring 11.4 cm in diameter was placed in the front center of each breeding cage together
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with straw for nesting material. Lights were clock-controlled on a 14L: 10D cycle (lights on at 0700, off at 2100 hr). Temperature was maintained between 21 and 23.8”C. All pairs were allowed to court, build nests, and lay eggs without experimental interference. On the fourth day after the female laid her second and final egg, both eggs were briefly removed and candled. All fertile eggs were then shaken by hand to detach the embryo from the yolk sac so that hatching would not occur. Pairs with an infertile two-egg clutch were discarded from the experiment. On the fourteenth day after each pair’s second egg was laid (i.e., the day that the second egg would normally hatch), the male and female were separated by a transparent Plexiglas partition inserted into the center of the breeding cage. Each breeding partner was then given its own nest which was placed as close as possible to the original nest site, to the center partition, and to the nest of its mate. Birds were assigned as pairs to one of three exposure groups such that, for each pair, the male and female breeding partners received the same exposure regimen. Each bird in Group SD (N = 12 pairs) was exposed to one 2- to 3-day-old food-deprived squab for 2 hr daily on each of 4 consecutive days (fourteenth to seventeenth day after the second egg was laid). These squabs had been removed from their own parents in the breeding colony and were housed individually in heated nest bowls for 22 to 24 hr before they were placed in the nests of Group SD birds. At the end of the 2-hr exposure period, squabs were returned to their parents and were replaced with two eggs which remained continuously available to SD birds until the next squab exposure period on the following day. Birds in Group SF (N = 13 pairs) were treated identically to the SD birds, except that the 2- to 3-day-old squabs provided were collected from the breeding colony immediately prior to the scheduled time of squab presentation. Squabs chosen for use in Group SF were those with distended crops, indicating that they had been fed recently by their own parents. Group E birds (N = 12 pairs) received no squab exposure during this 4-day period, but were given continuous access to two eggs in their nests during this period. Eggs were briefly removed and replaced at intervals corresponding to the time of squab presentation and removal in Groups SD and SF. Squab exposure was restricted to 2 hr daily in Groups SD and SF to insure that the stimulus characteristics of food-deprived and recently fed squabs remained relatively constant. For all SD and SF birds, daily squab exposure periods began between 0900 and 1000 hr and ended between 1100 and 1200 hr. Under normal conditions, these intervals represent the last part of the female’s morning sitting period and the first part of the male’s daily period on the nest (Craig, 1909). The nest bowls used to house squabs given to SD birds during their 22-24 hr period of food deprivation were heated with woven glass-
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insulated heating cords which were coiled and taped to the base of the bowls. Heating cords were connected to a variable output transformer set to maintain the squab’s dorsal skin temperature within the 36-38X’ range recorded during parental brooding (unpublished observations). To provide an estimate of the amount of parental feeding activity exhibited by each bird in Groups SD and SF, the weight of each squab was recorded at the beginning and end of each 2-hr exposure period. Group comparisons of squab weight gain were based on the cumulative amount of weight gained by all squabs given to each individual during the four exposure periods. Crop sac weight. Between 22 and 24 hr after the fourth and final exposure period, each bird was removed from the breeding cage and was killed for crop sac examination. Crop sacs were weighed after being thoroughly cleaned of adhering fat, emptied of all seeds and crop “milk”, rinsed in saline, and blotted dry. Two additional groups of birds, taken from Buntin (1975, 1977), were included in crop sac weight analyses in order to obtain additional information on the relative crop sac growth-promoting effects of the 2-hr daily squab exposure regimen used in the SD and SF conditions. Prior to Day 14 of incubation, birds in both groups were treated the same as those in Groups SD and SF. Group El4 birds (N = 10 pairs) were killed on the fourteenth day of incubation to determine the degree of crop sac development achieved by the end of the normal incubation period. Group S/me subjects (N = 8 males and 8 females) were separated by a Plexiglas partition from their mates on Day 14. While their mates sat on eggs in the adjacent half of the cage, S/me birds were given unrestricted exposure to a 2- to 3-day-old squab continuously for 96-98 hr. Each squab was replaced by a fresh 2- to 3-day-old squab after 24 hr in the nest of a Group S/me subject. All S/me birds were killed at the same time as SD and SF birds for crop sac weight determinations. Behavioral observations. To estimate the relative frequency of nest occupation in males and females of each group, nine hourly spot checks were made of each subject on the second, third, and fourth days of the exposure period. Spot checks were scheduled between 0900 and 1700 hr, which, under normal conditions, brackets the male’s normal sitting period (Craig, 1909). Analysis was based on the percentage of total spot checks in which each subject occupied the nest on these 3 days. In Groups SD and SF, each bird was also observed during the first 15 min of each daily squab exposure period. Behavior was recorded on data sheets divided into 60 compartments, each of which corresponded to one 15set interval. As the observation period progressed, any display of squab-directed activity was noted in the appropriate 15set interval block. Four categories of squab-directed activity were recorded for analysis: (1)
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pecking and preening the squab (PK-PR); (2) squab-oriented bill opening or bill-to-bill contact (BO-BC); (3) parental regurgitation movements oriented towards the squab but performed without physical contact with the squab (RM); (4) regurgitation feeding, in which regurgitation movements were performed while in bill-to-bill contact with the squab (RF). Crop “milk” exchange presumably takes place during RF episodes. For scoring purposes, each 15set interval in which squab-directed activity occurred was assigned to one and only one of these four categories. The criterion used for assignment of intervals was based on a hierarchical arrangement of squab-directed activity measures corresponding to the order in which they were just presented. This order is characteristic of the typical sequence of parental activities during normal regurgitation feeding interactions. To illustrate, intervals in which pecking or preening the squab occurred were scored in this category only if no other parental activities were recorded during that interval. On the other hand, intervals in which regurgitation feeding was recorded were scored in this category, regardless of whether any or all of the remaining types of squab-directed activities also occurred during the same interval. For statistical comparisons of group differences, the number of 15set intervals assigned to each of the four parental activity categories was converted to and expressed as a percentage of total squab-directed activity. The use of percentage scores allowed for group comparisons of the distribution of parental activities, independent of any differences in the total amount of squab-directed activity displayed. Group comparisons in all cases were based on the sum of the scores obtained during the four observation periods. Statistics. Analyses of variance and Duncan’s new multiple-range tests (Duncan, 1955)were used for all crop sac weight comparisons. Because of significant heterogeneity of variance, the nonparametric Kruskal-Wallis one-way analysis of variance and the Mann-Whitney U-test (Siegel, 1956) were employed for analysis of group differences in squab weight gain and spot-check sitting data. Nonparametric analyses were also conducted on all squab-directed activity measures. A two-tailed significance level of P < 0.05 was used unless otherwise indicated. RESULTS Crop Sac Weight
Crop sac weights differed significantly across the three exposure groups for males (F (2, 34) = 26.04, P < 0.001) and for females (F (2, 34) = 26.59, P < 0.001). For both sexes (see Table l), the crop sacs of birds exposed to food-deprived squabs (Group SD) were significantly heavier than those of SF birds exposed to recently-fed young Cp< 0.05 for both sexes). Males and females in both squab exposure conditions had significantly heavier
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TABLE 1 Mean Crop Sac Weight of Males and Females in Each Exposure Condition Crop sac weight (g) Group
Number of pairs
SD SF E Slmeb E14b
12 13 12 8 10
Male 3.91 f 3.32 ? 1.93 + 4.47 f 2.54 k
0.15” 0.16 0.27 0.23 0.16
Female 4.24 k 0.23 3.39 k 0.23 1.70 lr: 0.28 5.46 i 0.45 2.96 k 0.20
a Mean f SEM. b Group S/me data taken from Buntin (1977 and 1975)for males and females, respectively. Group El4 data for both sexes taken from Buntin (1977). See text for description of groups.
crop sacs than their egg-exposed counterparts in Group E (p < 0.001 for all comparisons). There were no significant sex differences in crop sac weight in any group. To determine if crop sacs of SD and SF birds actually increased in weight during the 4-day exposure period and to compare crop sac weights of SD and SF birds with those of birds receiving continuous squab exposure, a separate analysis was conducted involving Groups SD, SF, E14, and S/me (see Methods). This analysis yielded a significant overall difference for both sexes (males: F (3, 39) = 20.67, P < 0.001; females: F (3,39) = 13.83, P < 0.001). Crop sacs of males in Groups SD and SF were significantly heavier than those of males sacrificed at the end of the incubation period (El4 vs SD and SF: P < 0.001 and < 0.01, respectively; see Table 1). SD females also displayed a significant increase in crop sac weight during the exposure period (SD vs E14: P < O.OOS),but SF females did not. Crop sacs of birds receiving continuous squab exposure (S/me) were significantly heavier than those of birds in both 2-hr daily squab exposure conditions (S/me vs SD: P < 0.05 (males), < 0.005 (females); S/me vs SF: P < 0.001 for both sexes). Squab Weight Gain Squabs fed by SD birds gained nearly three times as much total weight as those fed by SF birds (mean weight in grams + SE = 18.3 2 1.4 and 15.6 f 1.3 for SD males and females, respectively; 6.4 k 0.8 and 5.3 k 0.7 for SF males and females respectively). Indeed, there was no overlap in the distribution of total squab weight gain recorded for these two groups (Mann-Whitney U = 0, P < 0.002 for both sexes). No significant sex differences were evident in either group.
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Spot-Check Sitting Although sitting frequency was high in all groups (mean percentage of total spot checks in nest + SE = 96.0 + 1.6, 98.0 + 0.7, and 84.6 + 3.8 for males in Groups SD, SF, and E, respectively; 85.5 + 3.7, 90.3 + 1.7, and 85.5 + 4.2, for females in Groups SD, SF, and E, respectively), a Kruskal-Wallis test revealed a significant difference in spot-check sitting performance of males in the three groups (H (2) = 15.16, P < 0.001). Males in both squab exposure groups showed more frequent nest occupation than males in Group E (E vs SD: U = 24, P < 0.02; E vs SF: U = 12, P < 0.002). There were no significant group differences in female nest occupation frequency during daytime spot checks. Squab-Directed Activity As shown in Table 2, regurgitation feeding (RF) and bill opening-bill contact (BO-BC) with the squab were displayed by significantly more birds in Group SD than in Group SF during observation periods (RF, P < 0.005 for both sexes; BO-BC, P < 0.01 and < 0.05 for males and females, respectively, Fisher’s exact probability test). Using the scores of responding birds for comparison, SD birds of both sexes displayed more total squab-directed activity (SDA) than SF subjects Cp < 0.002 for both sexes). The BO-BC and RF categories represented a greater proportion of total SDA in Group SD than in Group SF (p < 0.002). Conversely, intervals represented exclusively by squab pecking and preening (PK-PR) accounted for a larger percentage of total SDA in SF birds than in SD subjects Cp < 0.002). Regurgitation movements (RI@ were displayed by significantly more females in both exposure conditionsthan by males (SD, P < 0.05; SF, P < 0.025). As a result, this category represented a greater proportion of total SDA in females than in males Cp< 0.05). Males and females in Group SD did not differ significantly in any other squab-directed activity category. In Group SF, however, females displayed significantly more total SDA than males (P < 0.05). Squab Weight Gain, Crop Sac Weight, and Squab-Directed Activity Correlations Spearman rank-order correlations were conducted to determine the relationship between crop sac weight, squab weight gain, and the various squab-directed activity measures. The data already obtained on these measures, as presented before, would allow us to predict that any association obtained between crop sac weight, squab weight gain, and feedingrelated squab-directed activity measures would be positive rather than negative. Accordingly, a one-tailed significance level of P < 0.05 was used for these correlation analyses. Correlations involving each of the
t2.J 5?
Male Male Female Female
Sex
12 13 12 13
N 122.5 (12)” 11.5 (12) 131.0 (12) 26.0 (13)
SDAn*b 7.5 (11) 89.0 (12) 3.5 (12) 77.0 (13)
PK-PR (%)
D Number of 15-set intervals. * See text for abbreviations. c Number of responding birds in each category shown in parentheses.
SD SF SD SF
Group 19.5 (12) 0 (5) 16.0 (12) 3.5 (7)
BO-BC (%I
RM (%I 0 (5) 0 (3) 5.0 (11) 10.0 (10)
TABLE 2 Median Total Squab-Directed Activity @DA) of Responding SD and SF Birds and Median Percentage of SDA Represented by Various Categories
69.0 (12) 0 (3) 67.0 (12) 0 (3)
RF cw
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squab-directed activity categories were based on the number of intervals assigned to each measure rather than to the percentage of total squabdirected activity represented. On measures in which the number of responding birds was small, point-biserial correlation analyses (Bruning and Kintz, 1968) were conducted, based on a classification of subjects into responding and nonresponding categories. The results of all correlation analyses are presented in Table 3. With the exception of SF males, squab weight gain (SWG) tended to be positively correlated with RF, the combined regurgitation behavior category (RB) consisting of RM and RF, and the combined feeding-related activity category (FRA) consisting of BO-BC, RM, and RF. Total SDA was positively correlated with SWG in Group SD but not in Group SF. This is to be expected in view of the high proportion of total parental activity represented by feeding-related behavior in SD birds. Crop sac weight (CSW) was significantly correlated with some squabdirected activities in males, but not in females. Males in Group SD displayed a significant (one-tailed) correlation between CSW and RB, whereas, in Group SF males, squab-directed PK-PR activity was significantly correlated with CSW. CSW was not significantly correlated with SWG in males or females of either group. DISCUSSION
Male and female ring doves exposed to food-deprived squabs for 2 hr daily displayed more total squab-directed activity, more parental regurgitation feeding behavior, and more extensive crop sac growth than birds given recently fed squabs. These findings indicate that (1) the food demands of the squab determine to a great extent the type and amount of parental attention provided by male and female parents, and (2) stimulation associated with parental feeding interactions promotes crop sac development in both sexes. During the incubation period, nontactile cues from incubating females have been shown to be sufficient, under certain conditions, to promote normal crop sac growth in their male partners (Patel, 1936; Friedman and Lehrman, 1968). This raises the possibility that crop sac weights of birds in the present study not only reflected the effects of stimuli received from squabs or eggs placed in their own nests, but also the effects of stimuli from their mates sitting on eggs or squabs in the adjacent half of the cage. However, Buntin (1975, 1977) has demonstrated that, even under the most favorable exposure conditions, “adjacent-nest” exposure to squabs or mate-squab interactions is not sufficient to stimulate crop sac growth in males or females sitting on unhatched eggs beyond the normal incubation period. While this does not exclude the possibility that mate stimulation is more effective in promoting crop sac growth in birds given squabs rather than eggs in their own nests, it appears doubtful from these findings
SWG SWG SWG SWG
Male Male Female Female
SD SF SD SF
SDA 0.49 0.62” 0.25 0.18 0.69d 0.25 0.5@ 0.22
SWG 0.36 0.02 0.11 0.32 -0.50 0.16 -0.50 -0.07
0.17 0.5Y 0.28 0.02
PK-PR
0.10 0.40” 0.42 0.410
0.09 0.21” 0.19 0.03”
BO-BC
0.20” 0.2Y 0.26 0.32
0.21” 0.21a 0.26 0.14
RM
0.66C 0.21Q 0.5r 0.58”*”
0.38 0.28” 0.36 0.17”
RF
(1 Point-biserial correlation coefficient based on classification of subjects into responding and nonresponding categories. * P < 0.05 (one-tailed). c P < 0.025 (one-tailed). d P < 0.01 (one-tailed). e P < 0.005 (one-tailed).
csw csw csw csw
Measure
Male Male Female Female
Sex
SD SF SD SF
Group
Measure
TABLE 3 Spearman Rank Order and Point-Biserial Correlations Between Crop Sac Weight, Squab Weight Gain, and Various Squab-Directed Activities in Groups SD and SF
0.72” 0.39” 0.58” 0.51b
0.53* 0.41” 0.28 0.14
RB
0.7w 0.39a 0.6oc 0.62”
0.52* 0.41” 0.28 0.26
FRA
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that “adjacent-nest” stimuli contributed significantly to crop sac growth under these conditions. When consideration is given to the fact that only 8 hr of exposure to squabs was received, crop sac development in Group SD appears remarkably extensive. Although crop sacs of SD birds did not attain the degree of development seen in mate-separated birds given 96 hr of squab exposure (Group S/me), they were comparable in weight to those of males and females given continuous exposure to a mutually shared squab (see Group S, Buntin, 1977). This suggests that, in both sexes, the amount of squab exposure required to induce normal crop sac development depends upon the nature of the squab stimulation available. Although exposure to recently fed squabs promoted less crop sac growth than exposure to food deprived young, SF birds did have heavier crop sacs than egg-exposed controls in the E condition. For SF males, moreover, crop sac development was more extensive than that achieved by males at the end of the normal incubation period (Group E14). SF females, on the other hand, showed no significant increase in crop sac weight over the 4-day exposure period, even though they showed more total squab-directed activity than males during observation. This sex difference in relative crop sac growth in the SF condition suggests that males may be more responsive to stimuli provided by recently fed squabs than are females, at least under certain conditions. In a previous study, Buntin (1977) demonstrated that visual and auditory cues from young are not sufficient by themselves to stimulate crop sac growth in male ring doves. Furthermore, these stimuli were only effective in maintaining male crop sac weight at the level reached by the end of the incubation period when maximal amounts of in-nest exposure to such cues was provided. It is probable, therefore, that the crop sac development seen in SD and SF males was primarily stimulated by tactile interactions with young, and the finding that male crop sac weight in both groups was positively correlated with a number of contact-related parental activities is consistent with this view. In Group SD males, the best behavioral predictors of crop sac weight were those measures associated with parental feeding activity and, in particular, those associated with regurgitation behavior. This implies that the act of regurgitation may be an important source of stimulation for prolactin secretion in males. The fact that crop sac weight and regurgitation behavior were not significantly correlated in SF males does not necessarily contradict this hypothesis, since other correlation data (see SWG vs RF, RB, and FRA; Table 3) indicate that the amount of feeding-related activity in SF males during observations did not accurately reflect the total amount of parental feeding which took place during the 8 hr of squab exposure. The lack of representative data on feeding-related activity in SF males also creates difficulties in interpreting the significant positive correlation obtained between squab-directed peck-
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ing and preening activity and crop sac weight in these birds. While pecking-preening behavior may provide an additional source of crop sac growth-promoting cues for males under certain conditions, it is also possible that it merely reflects increased prolactin secretion induced by other squab-related stimuli. Since previous studies have shown that noncontact (i.e., visual and auditory) stimuli from young are sufficient to promote normal crop sac growth in females under continuous 96-hr squab exposure conditions (Buntin, 1977), the lack of a significant association between female crop sac weight and the various contact-related parental activities seen in the present study may be attributable to the crop sac growth-promoting effects of nontactile cues. In this regard, it is noteworthy that more females in both groups displayed regurgitation movements during observations than males. Since regurgitation movements were most frequently seen while birds were viewing squabs prior to feeding episodes, rather than following abortive feeding attempts, this result may be a general reflection of the female’s elevated responsiveness to visual and auditory stimuli from young. Although exposure to food-deprived young had the same facilitative effect on crop sac development in males as it did in females, the data suggest that the types of sensory cues mediating this crop sac response may differ for each sex. In males, it is apparent that contact-related stimuli associated with parental feeding interactions were most effective in promoting female crop sac growth. While tactile stimuli from young may have also played a role in promoting female crop sac development, the present results provide no direct or indirect evidence for such involvement. As discussed before, however, it does appear likely that female crop sac growth was influenced to some extent by nontactile cues from squabs. Differences in the behavior of food-deprived and recently fed squabs suggest a possible mechanism whereby nontactile stimuli could differentially affect female crop sac growth. During observations, food-deprived young were considerably more active than recently fed squabs and also showed more begging activities such as neck extension and “bill-searching” behavior (Miller and Miller, 1958). By affecting the quality of nontactile stimulation which females received, these differences in squab behavior could have influenced the pattern of crop sac development seen in the two exposure conditions. REFERENCES Bates, R. W., Miller, R. A., and Garrison, M. D. (1962). Evidence in the hypophysectomized pigeon of a synergism among prolactin, growth hormone, thyroxine, and prednisone upon body, digestive tract, kidney, and fat stores. Endocrinology 71, 34% 360. Beams, H. W., and Meyer, R. K. (1931). The formation of “pigeon milk”. Physiol. ZooI. 4, 486-500.
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Bruning, J., and Kintz, B. (1968). Computational Handbook ofStatistics, Scott, Foresman, Glenview, Illinois. Buntin, J. D. (1975). Stimulus Factors Involved in Squab-Znduced Crop Sac Growth and Parental Responsiveness in the Ring Dove (Streptopelia risoria), unpublished doctoral dissertation, Rutgers University. Buntin, J. D. (1977). Stimulus requirements for squab-induced crop sac growth and nest occupation in ring doves (Streptopelia risoria). J. Comp. Physiol. Psychol. 91, 1728. Craig, W. (1909). The expression of emotion in the pigeons. I. The blond ring dove (Turtur risorius).
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19, 29-82.
Duncan, D. B. (1955). Multiple range and multiple F tests. Biometrics 11, l-42. Friedman, M. C., and Lehrman, D. S. (1968). Physiological conditions for the stimulation of prolactin secretion by external stimuli in the male ring dove. Anim. Behav. 16,233-237. Hansen, E. W. (1966). Squab-induced crop growth in ring dove foster parents. J. Comp. Physiol. Psychol. 62, 120-122. Hansen, E. W. (1971). Responsiveness of ring dove foster parents to squabs. J. Comp. Physiol.
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Lehrman, D. S., and Brody, P. (1964). Effect of prolactin on established incubation behavior in the ring dove. J. Comp. Physiol. Psychol. 57, 161-165. Lyons, W. R. (1937). Preparation and assay of mammotropic hormone. Proc. Sot. Exp. Biol. Med. 35, 645-648.
Meier, A. H., John, T. M., and Joseph, M. (1971). Corticosterone and the circadian pigeon crop sac response to prolactin. Camp. Biochem. Physiol. 40, 459-466. Miller, W. J., and Miller, L. S. (1958). Synopsis of behaviour traits of the ring dove. Anim. Behav. 6, 3-8.
Patel, M. D. (1936). The physiology of the formation of “pigeon milk”. Physiol. Zool. 9, 129-152. Raud, H. R., and Odell, W. D. (1971). Studies of the measurement of bovine and porcine prolactin by radioimmunoassay and by systemic pigeon crop-sac bioassay. Endocrinology 88, 991-1002. Riddle, O., Bates, R. W., and Dykshorn, S. W. (1933). The preparation, identification, and assay of prolactin-a hormone of the anterior pituitary. Amer. J. Physiol. 105,191-216. Siegel, S. (1956). Nonparametric Statisticsfor the Behavioral Sciences, McGraw-Hill, New York.
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Effect of Parental Crop Sac Growth
Feeding Activity on Squab-Induced in Ring Doves (Streptopelia risoria)l
JOHN D. BUNTIN?
MEI-FANG CHENG, AND ERNST W. HANSEN
Institute
of Animal Behavior, Rutgers-the State University, Newark, New Jersey 07102
Effects of parental regurgitation feeding activity on crop sac development were studied in mate-separated male and female ring doves given 2 hr of daily exposure to food-deprived or recently fed squabs, for 4 consecutive days during the early posthatching period of the breeding cycle. In both sexes, food-deprived squabs stimulated more squab-directed activity, more parental regurgitation feeding activity, and greater crop sac development than recently fed young. Crop sac weights of males in both groups tended to be positively correlated with one or more parental activities. Correlations obtained in males exposed to food-deprived young further suggested that tactile stimuli associated with regurgitation behavior may promote crop sac development. In contrast to males, crop sac weights of females in both groups were not highly correlated with any type of contact-related parental activity or group of activities. These results, together with previous findings, suggest that nontactile stimuli from young played some role in mediating female crop sac weight differences in the two exposure conditions.
The crop sacs of male and female ring doves undergo a three- to four-fold increase in weight during the 2-week period of egg incubation (Hansen, 1966; Friedman and Lehrman, 1968). Although a number of hormones may participate in promoting full crop sac development (Bates et al., 1962; Meier et al., 1971; Raud and Ode& 1971), actual mucosal growth is stimulated by prolactin (Lyons, 1937; Riddle et al., 1933). About the time of hatching, epithelial cells begin to slough off from the crop sac wall (Beams and Meyer, 1931; Patel, 1936) to form crop “milk”. This substance is regurgitated to the young by both parents and provides their principal source of nourishment during the early posthatching period. The 4- to 5-day period of maximal crop “milk” production and parental regurgitation feeding activity which begins at hatching coincides with a period of accelerated crop sac growth in both parents. During this period, ’ This work was supported by USPHS-NIMH Predoctoral Fellowship MH 46279 to J. B. and NIMH Grant MH 02271 to M.-F. C. This study is based on a doctoral dissertation submitted by J. B. to the graduate school of Rutgers University. The technical assistance of Mr. Chuck Rosen is gratefully acknowledged. This is Contribution No. 238 from the Institute of Animal Behavior. 2 Present address: Department of Biology, Princeton University, Princeton, New Jersey 08540. 297 Copyright All rights
@ 1977 by Academic Press, Inc. of reproduction in any form reserved.
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the crop sac undergoes a 50% increase in empty weight over that achieved by the end of the incubation period (Hansen, 1966). During the remainder of the 21-day posthatching period, the crop sac gradually declines in weight and development as the growing young are fed less crop “milk” by their parents (Patel, 1936). Prior to hatching, stimuli received while sitting on eggs (Lehrman and Brody, 1964) and, under certain circumstances, visual cues provided by an incubating mate (Friedman and Lehrman, 1968) are effective in promoting crop sac development. After hatching, however, egg-related stimuli lose their effectiveness in sustaining crop sac growth, and further development depends upon the presence of young in the nest (Hansen, 1966; Buntin, 1977). The magnitude of crop sac growth has been shown to be influenced by the age of the squab (Hansen, 1971) and the type and amount of tactile stimulation received from the squab (Buntin, 1977). Moreover, these types of stimuli exert differential effects of crop sac growth in males and females. However, parent doves normally encounter these types of squab-related stimuli within the context of specific parent-young interactions, and no studies have examined the possibility that these various types of encounters differ in their crop sac growthpromoting effectiveness. Since parental regurgitation feeding behavior is a unique and prominent feature of the early posthatching period, it could be hypothesized that stimuli received during these interactions with young have a facilitative effect on crop sac development in both sexes. The experimental paradigm used to test this hypothesis was based on preliminary results indicating that the frequency of parental feeding activity is geared to the food requirements of the squab. Accordingly, the importance of parental feeding interactions in promoting crop sac growth was investigated by comparing crop sac weights of doves exposed to food-deprived and recently fed squabs during the early posthatching period. METHODS Subjects. The subjects were 37 adult male and 37 adult female ring doves which were hatched and raised in the breeding colony maintained at the Institute of Animal Behavior. Prior to use in the experiment, all birds had received one or two previous breeding experiences that consisted of successfully rearing at least one squab to 21 days of age. All birds were housed in visual isolation cages individually for 3-7 weeks prior to the start of the experiment. Procedure. Birds were initially paired with unfamiliar breeding partners and were placed in 82 x 46 x 36-cm breeding cages constructed of wood with wire-mesh front doors. Food, water, and mineral-grit mixture were continuously available. A transparent glass nest bowl measuring 11.4 cm in diameter was placed in the front center of each breeding cage together
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with straw for nesting material. Lights were clock-controlled on a 14L: 10D cycle (lights on at 0700, off at 2100 hr). Temperature was maintained between 21 and 23.8”C. All pairs were allowed to court, build nests, and lay eggs without experimental interference. On the fourth day after the female laid her second and final egg, both eggs were briefly removed and candled. All fertile eggs were then shaken by hand to detach the embryo from the yolk sac so that hatching would not occur. Pairs with an infertile two-egg clutch were discarded from the experiment. On the fourteenth day after each pair’s second egg was laid (i.e., the day that the second egg would normally hatch), the male and female were separated by a transparent Plexiglas partition inserted into the center of the breeding cage. Each breeding partner was then given its own nest which was placed as close as possible to the original nest site, to the center partition, and to the nest of its mate. Birds were assigned as pairs to one of three exposure groups such that, for each pair, the male and female breeding partners received the same exposure regimen. Each bird in Group SD (N = 12 pairs) was exposed to one 2- to 3-day-old food-deprived squab for 2 hr daily on each of 4 consecutive days (fourteenth to seventeenth day after the second egg was laid). These squabs had been removed from their own parents in the breeding colony and were housed individually in heated nest bowls for 22 to 24 hr before they were placed in the nests of Group SD birds. At the end of the 2-hr exposure period, squabs were returned to their parents and were replaced with two eggs which remained continuously available to SD birds until the next squab exposure period on the following day. Birds in Group SF (N = 13 pairs) were treated identically to the SD birds, except that the 2- to 3-day-old squabs provided were collected from the breeding colony immediately prior to the scheduled time of squab presentation. Squabs chosen for use in Group SF were those with distended crops, indicating that they had been fed recently by their own parents. Group E birds (N = 12 pairs) received no squab exposure during this 4-day period, but were given continuous access to two eggs in their nests during this period. Eggs were briefly removed and replaced at intervals corresponding to the time of squab presentation and removal in Groups SD and SF. Squab exposure was restricted to 2 hr daily in Groups SD and SF to insure that the stimulus characteristics of food-deprived and recently fed squabs remained relatively constant. For all SD and SF birds, daily squab exposure periods began between 0900 and 1000 hr and ended between 1100 and 1200 hr. Under normal conditions, these intervals represent the last part of the female’s morning sitting period and the first part of the male’s daily period on the nest (Craig, 1909). The nest bowls used to house squabs given to SD birds during their 22-24 hr period of food deprivation were heated with woven glass-
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insulated heating cords which were coiled and taped to the base of the bowls. Heating cords were connected to a variable output transformer set to maintain the squab’s dorsal skin temperature within the 36-38X’ range recorded during parental brooding (unpublished observations). To provide an estimate of the amount of parental feeding activity exhibited by each bird in Groups SD and SF, the weight of each squab was recorded at the beginning and end of each 2-hr exposure period. Group comparisons of squab weight gain were based on the cumulative amount of weight gained by all squabs given to each individual during the four exposure periods. Crop sac weight. Between 22 and 24 hr after the fourth and final exposure period, each bird was removed from the breeding cage and was killed for crop sac examination. Crop sacs were weighed after being thoroughly cleaned of adhering fat, emptied of all seeds and crop “milk”, rinsed in saline, and blotted dry. Two additional groups of birds, taken from Buntin (1975, 1977), were included in crop sac weight analyses in order to obtain additional information on the relative crop sac growth-promoting effects of the 2-hr daily squab exposure regimen used in the SD and SF conditions. Prior to Day 14 of incubation, birds in both groups were treated the same as those in Groups SD and SF. Group El4 birds (N = 10 pairs) were killed on the fourteenth day of incubation to determine the degree of crop sac development achieved by the end of the normal incubation period. Group S/me subjects (N = 8 males and 8 females) were separated by a Plexiglas partition from their mates on Day 14. While their mates sat on eggs in the adjacent half of the cage, S/me birds were given unrestricted exposure to a 2- to 3-day-old squab continuously for 96-98 hr. Each squab was replaced by a fresh 2- to 3-day-old squab after 24 hr in the nest of a Group S/me subject. All S/me birds were killed at the same time as SD and SF birds for crop sac weight determinations. Behavioral observations. To estimate the relative frequency of nest occupation in males and females of each group, nine hourly spot checks were made of each subject on the second, third, and fourth days of the exposure period. Spot checks were scheduled between 0900 and 1700 hr, which, under normal conditions, brackets the male’s normal sitting period (Craig, 1909). Analysis was based on the percentage of total spot checks in which each subject occupied the nest on these 3 days. In Groups SD and SF, each bird was also observed during the first 15 min of each daily squab exposure period. Behavior was recorded on data sheets divided into 60 compartments, each of which corresponded to one 15set interval. As the observation period progressed, any display of squab-directed activity was noted in the appropriate 15set interval block. Four categories of squab-directed activity were recorded for analysis: (1)
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pecking and preening the squab (PK-PR); (2) squab-oriented bill opening or bill-to-bill contact (BO-BC); (3) parental regurgitation movements oriented towards the squab but performed without physical contact with the squab (RM); (4) regurgitation feeding, in which regurgitation movements were performed while in bill-to-bill contact with the squab (RF). Crop “milk” exchange presumably takes place during RF episodes. For scoring purposes, each 15set interval in which squab-directed activity occurred was assigned to one and only one of these four categories. The criterion used for assignment of intervals was based on a hierarchical arrangement of squab-directed activity measures corresponding to the order in which they were just presented. This order is characteristic of the typical sequence of parental activities during normal regurgitation feeding interactions. To illustrate, intervals in which pecking or preening the squab occurred were scored in this category only if no other parental activities were recorded during that interval. On the other hand, intervals in which regurgitation feeding was recorded were scored in this category, regardless of whether any or all of the remaining types of squab-directed activities also occurred during the same interval. For statistical comparisons of group differences, the number of 15set intervals assigned to each of the four parental activity categories was converted to and expressed as a percentage of total squab-directed activity. The use of percentage scores allowed for group comparisons of the distribution of parental activities, independent of any differences in the total amount of squab-directed activity displayed. Group comparisons in all cases were based on the sum of the scores obtained during the four observation periods. Statistics. Analyses of variance and Duncan’s new multiple-range tests (Duncan, 1955)were used for all crop sac weight comparisons. Because of significant heterogeneity of variance, the nonparametric Kruskal-Wallis one-way analysis of variance and the Mann-Whitney U-test (Siegel, 1956) were employed for analysis of group differences in squab weight gain and spot-check sitting data. Nonparametric analyses were also conducted on all squab-directed activity measures. A two-tailed significance level of P < 0.05 was used unless otherwise indicated. RESULTS Crop Sac Weight
Crop sac weights differed significantly across the three exposure groups for males (F (2, 34) = 26.04, P < 0.001) and for females (F (2, 34) = 26.59, P < 0.001). For both sexes (see Table l), the crop sacs of birds exposed to food-deprived squabs (Group SD) were significantly heavier than those of SF birds exposed to recently-fed young Cp< 0.05 for both sexes). Males and females in both squab exposure conditions had significantly heavier
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TABLE 1 Mean Crop Sac Weight of Males and Females in Each Exposure Condition Crop sac weight (g) Group
Number of pairs
SD SF E Slmeb E14b
12 13 12 8 10
Male 3.91 f 3.32 ? 1.93 + 4.47 f 2.54 k
0.15” 0.16 0.27 0.23 0.16
Female 4.24 k 0.23 3.39 k 0.23 1.70 lr: 0.28 5.46 i 0.45 2.96 k 0.20
a Mean f SEM. b Group S/me data taken from Buntin (1977 and 1975)for males and females, respectively. Group El4 data for both sexes taken from Buntin (1977). See text for description of groups.
crop sacs than their egg-exposed counterparts in Group E (p < 0.001 for all comparisons). There were no significant sex differences in crop sac weight in any group. To determine if crop sacs of SD and SF birds actually increased in weight during the 4-day exposure period and to compare crop sac weights of SD and SF birds with those of birds receiving continuous squab exposure, a separate analysis was conducted involving Groups SD, SF, E14, and S/me (see Methods). This analysis yielded a significant overall difference for both sexes (males: F (3, 39) = 20.67, P < 0.001; females: F (3,39) = 13.83, P < 0.001). Crop sacs of males in Groups SD and SF were significantly heavier than those of males sacrificed at the end of the incubation period (El4 vs SD and SF: P < 0.001 and < 0.01, respectively; see Table 1). SD females also displayed a significant increase in crop sac weight during the exposure period (SD vs E14: P < O.OOS),but SF females did not. Crop sacs of birds receiving continuous squab exposure (S/me) were significantly heavier than those of birds in both 2-hr daily squab exposure conditions (S/me vs SD: P < 0.05 (males), < 0.005 (females); S/me vs SF: P < 0.001 for both sexes). Squab Weight Gain Squabs fed by SD birds gained nearly three times as much total weight as those fed by SF birds (mean weight in grams + SE = 18.3 2 1.4 and 15.6 f 1.3 for SD males and females, respectively; 6.4 k 0.8 and 5.3 k 0.7 for SF males and females respectively). Indeed, there was no overlap in the distribution of total squab weight gain recorded for these two groups (Mann-Whitney U = 0, P < 0.002 for both sexes). No significant sex differences were evident in either group.
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Spot-Check Sitting Although sitting frequency was high in all groups (mean percentage of total spot checks in nest + SE = 96.0 + 1.6, 98.0 + 0.7, and 84.6 + 3.8 for males in Groups SD, SF, and E, respectively; 85.5 + 3.7, 90.3 + 1.7, and 85.5 + 4.2, for females in Groups SD, SF, and E, respectively), a Kruskal-Wallis test revealed a significant difference in spot-check sitting performance of males in the three groups (H (2) = 15.16, P < 0.001). Males in both squab exposure groups showed more frequent nest occupation than males in Group E (E vs SD: U = 24, P < 0.02; E vs SF: U = 12, P < 0.002). There were no significant group differences in female nest occupation frequency during daytime spot checks. Squab-Directed Activity As shown in Table 2, regurgitation feeding (RF) and bill opening-bill contact (BO-BC) with the squab were displayed by significantly more birds in Group SD than in Group SF during observation periods (RF, P < 0.005 for both sexes; BO-BC, P < 0.01 and < 0.05 for males and females, respectively, Fisher’s exact probability test). Using the scores of responding birds for comparison, SD birds of both sexes displayed more total squab-directed activity (SDA) than SF subjects Cp < 0.002 for both sexes). The BO-BC and RF categories represented a greater proportion of total SDA in Group SD than in Group SF (p < 0.002). Conversely, intervals represented exclusively by squab pecking and preening (PK-PR) accounted for a larger percentage of total SDA in SF birds than in SD subjects Cp < 0.002). Regurgitation movements (RI@ were displayed by significantly more females in both exposure conditionsthan by males (SD, P < 0.05; SF, P < 0.025). As a result, this category represented a greater proportion of total SDA in females than in males Cp< 0.05). Males and females in Group SD did not differ significantly in any other squab-directed activity category. In Group SF, however, females displayed significantly more total SDA than males (P < 0.05). Squab Weight Gain, Crop Sac Weight, and Squab-Directed Activity Correlations Spearman rank-order correlations were conducted to determine the relationship between crop sac weight, squab weight gain, and the various squab-directed activity measures. The data already obtained on these measures, as presented before, would allow us to predict that any association obtained between crop sac weight, squab weight gain, and feedingrelated squab-directed activity measures would be positive rather than negative. Accordingly, a one-tailed significance level of P < 0.05 was used for these correlation analyses. Correlations involving each of the
t2.J 5?
Male Male Female Female
Sex
12 13 12 13
N 122.5 (12)” 11.5 (12) 131.0 (12) 26.0 (13)
SDAn*b 7.5 (11) 89.0 (12) 3.5 (12) 77.0 (13)
PK-PR (%)
D Number of 15-set intervals. * See text for abbreviations. c Number of responding birds in each category shown in parentheses.
SD SF SD SF
Group 19.5 (12) 0 (5) 16.0 (12) 3.5 (7)
BO-BC (%I
RM (%I 0 (5) 0 (3) 5.0 (11) 10.0 (10)
TABLE 2 Median Total Squab-Directed Activity @DA) of Responding SD and SF Birds and Median Percentage of SDA Represented by Various Categories
69.0 (12) 0 (3) 67.0 (12) 0 (3)
RF cw
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squab-directed activity categories were based on the number of intervals assigned to each measure rather than to the percentage of total squabdirected activity represented. On measures in which the number of responding birds was small, point-biserial correlation analyses (Bruning and Kintz, 1968) were conducted, based on a classification of subjects into responding and nonresponding categories. The results of all correlation analyses are presented in Table 3. With the exception of SF males, squab weight gain (SWG) tended to be positively correlated with RF, the combined regurgitation behavior category (RB) consisting of RM and RF, and the combined feeding-related activity category (FRA) consisting of BO-BC, RM, and RF. Total SDA was positively correlated with SWG in Group SD but not in Group SF. This is to be expected in view of the high proportion of total parental activity represented by feeding-related behavior in SD birds. Crop sac weight (CSW) was significantly correlated with some squabdirected activities in males, but not in females. Males in Group SD displayed a significant (one-tailed) correlation between CSW and RB, whereas, in Group SF males, squab-directed PK-PR activity was significantly correlated with CSW. CSW was not significantly correlated with SWG in males or females of either group. DISCUSSION
Male and female ring doves exposed to food-deprived squabs for 2 hr daily displayed more total squab-directed activity, more parental regurgitation feeding behavior, and more extensive crop sac growth than birds given recently fed squabs. These findings indicate that (1) the food demands of the squab determine to a great extent the type and amount of parental attention provided by male and female parents, and (2) stimulation associated with parental feeding interactions promotes crop sac development in both sexes. During the incubation period, nontactile cues from incubating females have been shown to be sufficient, under certain conditions, to promote normal crop sac growth in their male partners (Patel, 1936; Friedman and Lehrman, 1968). This raises the possibility that crop sac weights of birds in the present study not only reflected the effects of stimuli received from squabs or eggs placed in their own nests, but also the effects of stimuli from their mates sitting on eggs or squabs in the adjacent half of the cage. However, Buntin (1975, 1977) has demonstrated that, even under the most favorable exposure conditions, “adjacent-nest” exposure to squabs or mate-squab interactions is not sufficient to stimulate crop sac growth in males or females sitting on unhatched eggs beyond the normal incubation period. While this does not exclude the possibility that mate stimulation is more effective in promoting crop sac growth in birds given squabs rather than eggs in their own nests, it appears doubtful from these findings
SWG SWG SWG SWG
Male Male Female Female
SD SF SD SF
SDA 0.49 0.62” 0.25 0.18 0.69d 0.25 0.5@ 0.22
SWG 0.36 0.02 0.11 0.32 -0.50 0.16 -0.50 -0.07
0.17 0.5Y 0.28 0.02
PK-PR
0.10 0.40” 0.42 0.410
0.09 0.21” 0.19 0.03”
BO-BC
0.20” 0.2Y 0.26 0.32
0.21” 0.21a 0.26 0.14
RM
0.66C 0.21Q 0.5r 0.58”*”
0.38 0.28” 0.36 0.17”
RF
(1 Point-biserial correlation coefficient based on classification of subjects into responding and nonresponding categories. * P < 0.05 (one-tailed). c P < 0.025 (one-tailed). d P < 0.01 (one-tailed). e P < 0.005 (one-tailed).
csw csw csw csw
Measure
Male Male Female Female
Sex
SD SF SD SF
Group
Measure
TABLE 3 Spearman Rank Order and Point-Biserial Correlations Between Crop Sac Weight, Squab Weight Gain, and Various Squab-Directed Activities in Groups SD and SF
0.72” 0.39” 0.58” 0.51b
0.53* 0.41” 0.28 0.14
RB
0.7w 0.39a 0.6oc 0.62”
0.52* 0.41” 0.28 0.26
FRA
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that “adjacent-nest” stimuli contributed significantly to crop sac growth under these conditions. When consideration is given to the fact that only 8 hr of exposure to squabs was received, crop sac development in Group SD appears remarkably extensive. Although crop sacs of SD birds did not attain the degree of development seen in mate-separated birds given 96 hr of squab exposure (Group S/me), they were comparable in weight to those of males and females given continuous exposure to a mutually shared squab (see Group S, Buntin, 1977). This suggests that, in both sexes, the amount of squab exposure required to induce normal crop sac development depends upon the nature of the squab stimulation available. Although exposure to recently fed squabs promoted less crop sac growth than exposure to food deprived young, SF birds did have heavier crop sacs than egg-exposed controls in the E condition. For SF males, moreover, crop sac development was more extensive than that achieved by males at the end of the normal incubation period (Group E14). SF females, on the other hand, showed no significant increase in crop sac weight over the 4-day exposure period, even though they showed more total squab-directed activity than males during observation. This sex difference in relative crop sac growth in the SF condition suggests that males may be more responsive to stimuli provided by recently fed squabs than are females, at least under certain conditions. In a previous study, Buntin (1977) demonstrated that visual and auditory cues from young are not sufficient by themselves to stimulate crop sac growth in male ring doves. Furthermore, these stimuli were only effective in maintaining male crop sac weight at the level reached by the end of the incubation period when maximal amounts of in-nest exposure to such cues was provided. It is probable, therefore, that the crop sac development seen in SD and SF males was primarily stimulated by tactile interactions with young, and the finding that male crop sac weight in both groups was positively correlated with a number of contact-related parental activities is consistent with this view. In Group SD males, the best behavioral predictors of crop sac weight were those measures associated with parental feeding activity and, in particular, those associated with regurgitation behavior. This implies that the act of regurgitation may be an important source of stimulation for prolactin secretion in males. The fact that crop sac weight and regurgitation behavior were not significantly correlated in SF males does not necessarily contradict this hypothesis, since other correlation data (see SWG vs RF, RB, and FRA; Table 3) indicate that the amount of feeding-related activity in SF males during observations did not accurately reflect the total amount of parental feeding which took place during the 8 hr of squab exposure. The lack of representative data on feeding-related activity in SF males also creates difficulties in interpreting the significant positive correlation obtained between squab-directed peck-
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ing and preening activity and crop sac weight in these birds. While pecking-preening behavior may provide an additional source of crop sac growth-promoting cues for males under certain conditions, it is also possible that it merely reflects increased prolactin secretion induced by other squab-related stimuli. Since previous studies have shown that noncontact (i.e., visual and auditory) stimuli from young are sufficient to promote normal crop sac growth in females under continuous 96-hr squab exposure conditions (Buntin, 1977), the lack of a significant association between female crop sac weight and the various contact-related parental activities seen in the present study may be attributable to the crop sac growth-promoting effects of nontactile cues. In this regard, it is noteworthy that more females in both groups displayed regurgitation movements during observations than males. Since regurgitation movements were most frequently seen while birds were viewing squabs prior to feeding episodes, rather than following abortive feeding attempts, this result may be a general reflection of the female’s elevated responsiveness to visual and auditory stimuli from young. Although exposure to food-deprived young had the same facilitative effect on crop sac development in males as it did in females, the data suggest that the types of sensory cues mediating this crop sac response may differ for each sex. In males, it is apparent that contact-related stimuli associated with parental feeding interactions were most effective in promoting female crop sac growth. While tactile stimuli from young may have also played a role in promoting female crop sac development, the present results provide no direct or indirect evidence for such involvement. As discussed before, however, it does appear likely that female crop sac growth was influenced to some extent by nontactile cues from squabs. Differences in the behavior of food-deprived and recently fed squabs suggest a possible mechanism whereby nontactile stimuli could differentially affect female crop sac growth. During observations, food-deprived young were considerably more active than recently fed squabs and also showed more begging activities such as neck extension and “bill-searching” behavior (Miller and Miller, 1958). By affecting the quality of nontactile stimulation which females received, these differences in squab behavior could have influenced the pattern of crop sac development seen in the two exposure conditions. REFERENCES Bates, R. W., Miller, R. A., and Garrison, M. D. (1962). Evidence in the hypophysectomized pigeon of a synergism among prolactin, growth hormone, thyroxine, and prednisone upon body, digestive tract, kidney, and fat stores. Endocrinology 71, 34% 360. Beams, H. W., and Meyer, R. K. (1931). The formation of “pigeon milk”. Physiol. ZooI. 4, 486-500.
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Bruning, J., and Kintz, B. (1968). Computational Handbook ofStatistics, Scott, Foresman, Glenview, Illinois. Buntin, J. D. (1975). Stimulus Factors Involved in Squab-Znduced Crop Sac Growth and Parental Responsiveness in the Ring Dove (Streptopelia risoria), unpublished doctoral dissertation, Rutgers University. Buntin, J. D. (1977). Stimulus requirements for squab-induced crop sac growth and nest occupation in ring doves (Streptopelia risoria). J. Comp. Physiol. Psychol. 91, 1728. Craig, W. (1909). The expression of emotion in the pigeons. I. The blond ring dove (Turtur risorius).
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Lehrman, D. S., and Brody, P. (1964). Effect of prolactin on established incubation behavior in the ring dove. J. Comp. Physiol. Psychol. 57, 161-165. Lyons, W. R. (1937). Preparation and assay of mammotropic hormone. Proc. Sot. Exp. Biol. Med. 35, 645-648.
Meier, A. H., John, T. M., and Joseph, M. (1971). Corticosterone and the circadian pigeon crop sac response to prolactin. Camp. Biochem. Physiol. 40, 459-466. Miller, W. J., and Miller, L. S. (1958). Synopsis of behaviour traits of the ring dove. Anim. Behav. 6, 3-8.
Patel, M. D. (1936). The physiology of the formation of “pigeon milk”. Physiol. Zool. 9, 129-152. Raud, H. R., and Odell, W. D. (1971). Studies of the measurement of bovine and porcine prolactin by radioimmunoassay and by systemic pigeon crop-sac bioassay. Endocrinology 88, 991-1002. Riddle, O., Bates, R. W., and Dykshorn, S. W. (1933). The preparation, identification, and assay of prolactin-a hormone of the anterior pituitary. Amer. J. Physiol. 105,191-216. Siegel, S. (1956). Nonparametric Statisticsfor the Behavioral Sciences, McGraw-Hill, New York.