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Prenatal auditory discrimination in the bobwhite quail
BEHAVIORAL A N D N E U R A L BIOLOGY
31, 242-246 (1981)
BRIEF REPORT Prenatal Auditory Discrimination in the Bobwhite Quail MARIETA BARROW HEATON AND ERIN GALLEHER I
Department of Neuroscience, University of Florida College of Medicine, Gainesville, Florida 32610 Bobwhite quail embryos (Colinus virginianus) were tested to two conspecific calls on Day 22 of incubation (total incubation period = 23-24 days). In previous postnatal tests, one of these calls, a maternal exodus-like call, was highly attractive, and the other, an incidental quail call, was not an effective attractant. The embryos significantly increased their rate of bill-clapping when presented with the exodus-like call, and showed no change in ongoing activity when confronted with the incidental call. Thus, the differential responsiveness parallels that seen postnatally. Such prenatal discriminative ability had previously been shown only in Anseriformes, The advantage of the bobwhite quail for studies of species-specific perceptual development is discussed.
The ability to respond differentially to various inter- and intraspecific vocalizations provides a significant basis for parent-young interactions in many avian forms. Such discriminative behavior has been shown in the domestic chick, Peking, mallard, and wood ducks, ring-billed gulls, and bobwhite quail (Gottlieb, 1971; Evans, 1973; Heat on, Miller, & Goodwin, 1978). In both Peking and wood ducks, this species specificity can also be demonstrated during prenatal periods (Gottlieb, 1971; Heaton, 1972). When confronted with a call that is a postnatal attractant (e.g., the maternal exodus call, uttered as the hen leads the young from the nest), embryos of these species respond by significantly increasing their rate of bill-clapping, vocalization, and/or leg movements. When exposed to calls that are not postnatally attractive (e.g., other species calls, or incidental calls of their own species), responsiveness is either directionally inconsistent, or in some cases, declines (Heaton, 1972). The following study was designed to investigate the possibility of prenatal discriminative respond1 This research was supported by National Institute of Mental Health Grant MH-27677. Requests for reprints should be sent to Dr. M. B. Heaton, Department of Neuroscience, J. H. Miller Health Center, Box J-244, University of Florida, College of Medicine, Gainesville, Fla. 32610. 242 0163- i047/81/020242-05502.00/0 Copyright© 1981by AcademicPress, Inc. All rights of reproductionin any form reserved.
PRENATAL DISCRIMINATION IN QUAIL
243
ing in a species not belonging to the Anseriformes, the bobwhite quail
(Colinus virginianus), of the Galliformes (Phasianidae family). In an earlier study (Heaton et al., 1978), we found hatchlings of this species to be highly responsive in both single-call and simultaneous choice tests, exhibiting a strong preference for their maternal exodus call and calls closely resembling it. They were also able to make fine inter- and intraspecific discriminations. Should this discriminative ability be expressed prenatally, the bobwhite quail would represent an additional species in which the basis of this perception and the dynamics of its emergence might be explored. Such comparative study would be of considerable interest, with the potential to provide insights into the generality of various aspects of the phenomenon, and possible clues as to underlying mechanisms. The subjects of the study were 35 bobwhite quail embryos (Colinus virginianus), aged 22 days of incubation (total incubation period = 23-24 days). The eggs were obtained from the University of Florida Poultry Science Department. They were incubated in forced-draft, automatic turning incubators, with temperature maintained at 37.5°C, and relative humidity at 65-75%. The incubator was located in a quiet room in which no hatchlings were housed. Thus, sibling vocalizations (prenatal) and self-vocalizations were the only sources of auditory stimulation available to the embryos. On Day 22 of incubation, the eggs were taken individually to a Plexiglas observation chamber, in which temperature and humidity were maintained as during incubation. The shell overlying the airspace was removed and the inner-shell membrane moistened with warm saline. The chorioallantoic membrane could then be visualized and it was cut as much as was necessary to gently pull the embryo's head out of the egg (the body remained confined within the shell). This preparation was then placed on a sterile gauze pad. Bill-clapping was monitored either by an observer who maintained a manual count, or by a modified Brush Model 220 analog recorder (the two methods proved equally reliable). The tests were done blind, with the experimenter having no knowledge as to the nature of the stimulus call being used, or any aspect of the previously observed postnatal responsiveness to the cells. Intraobserver reliability coefficients were calculated, with counts for each half of a group compared. These coefficients averaged .82 across all test conditions, and were as high as .96 for the prestimulus baseline periods. A 10-cm speaker inside the testing incubator, connected to a tape recorder, provided the stimulus calls. The speaker was positioned 18 cm from the embryo, and the test calls were played at an acoustic level of 80-82 db, as measured prior to each test, with a Triplett Model 370 sound-level meter. Following a 15-min acclimation period, the test commenced. Each test consisted of three periods: a 5-min prestimulus period, a 1-min stimulus
244
HEATON AND GALLEHER
period, and a 5-min poststimulus period. Two stimulus calls were used. The first was the most attractive of the calls used in our previous study of postnatal preferential behavior in this species (Heaton et al., 1978). This call was virtually identical to a bobwhite call recorded during an exodus from the nest, having only slight differences in minor frequency peaks. Its phrasing, duration, repetition rate, dominant frequency, and frequency modulations are the same as those of the exodus call. Since the exodus call in this species occurs in different contexts and subserves more than one function (Stokes, 1967), we considered the two calls synonymous, although the present call (which for convenience we will term the maternal exodus-like call) was not recorded during a parent-young interaction. In a simultaneous choice test in our earlier study, this call was significantly preferred over the call recorded during an actual exodus. Thus, it was chosen for the present study. The call has five notes, uttered at a repetition rate of 1.6 notes per second, with dominant frequencies at 2200 Hz (major peak) and 1475 Hz (minor peak). The second call was an incidental bobwhite quail call, which had a low attractive value in our previous study (only a few animals approached it in a single call test, with long latency of approach and very short duration of stay within the designated approach area). This call consisted of 28 notes, uttered at a rate of 10 notes per second, with dominant frequencies at 775 Hz (major peak) and 680 and 850 Hz (minor peaks). Both calls were recorded under natural conditions. As shown in Table 1, the bobwhite quail embryos responded to the maternal exodus-like call by increasing their rate of bill-clapping, from a baseline rate of 20.73 movements per minute, to a rate of 36.16 moveTABLE 1 Bill-Clapping Measures in 22-day Bobwhite Quail Embryos before, during, and after 1-min Exposure to Two Conspecific Calls Bill-clapping (rate/min) Test call
Mean
SD
p~
Bobwhite maternal exodus-like call (N = 19) Prestimulus period (5 min) Stimulus period (1 min) Poststimulus period (5 min)
20.73 36.16 17.42
19.10 37.54 18.02
-< .02 ns
Bobwhite incidental call (N = 16) Prestimulus period (5 min) stimulus period (1 min) Poststimulus period (5 rain)
22.08 26.18 26.43
15.55 22.64 12.63
-ns ns
Statistical comparisons made to prestimulus period. Two-tailed Wilcoxon test.
PRENATAL DISCRIMINATION IN QUAIL
245
ments per minute. This increase was statistically significant (p < .02, Wilcoxon test, two-tailed). Fifteen out of eighteen animals, or 83%, contributed to this increase (one embryo did not change its baseline rate). When exposed to the incidental call, there was no significant change in bill-clapping. Of the 16 animals tested, 5 increased their rate of billclapping and 10 decreased. In one animal, the baseline rate did not change. This study demonstrates that like the Anseriformes which have been tested, bobwhite quail embryos are capable of auditory discrimination during the last day or two prior to hatching. When confronted with a stimulus call that elicits strong postnatal approach or preferential behavior, these embryos respond by significantly increasing their rate of bill-clapping over nonstimulus baseline levels. Conversely, when exposed to a call which is not postnatally attractive, no significant change in bill-clapping activity occurs. Thus, as in the Peking duck and to some extent, the wood duck, this prenatal differential responsiveness closely parallels, and thus is predictive of, postnatal behavior. The degree to which the quail embryos modified their ongoing billclapping activity in response to their maternal exodus-like call was striking. The mean increase in response rate was 74%, with 15 of 18 animals participating in this excitatory reaction. In Peking duck embryos, a mean increase of 63% has been reported during exposure to the maternal call (Gottlieb, 1971) and in the wood duck, an increase of only 29% has been seen (Heaton, 1972). This high degree of responsivity in the bobwhite again parallels the situation seen postnatally. In three approach tests in which the present attractant call was used in our previous study (both single-call and simultaneous choice tests), 81 animals responded, out of 82 tested, or an incidence of nearly 99% (Heaton et al., 1978). Such exceptionally consistent responsiveness is unusual indeed [see, for example, Gottlieb's (1971) lamentations on the behavioral vicissitudes of the domestic chick, a difficulty which renders them almost useless in studies of this sort). The bobwhite quail, then, would appear to be an energetic and decisive little animal, and one ideally suited to the study of speciesspecific perceptual development. In the bobwhite quail, as in the Anseriformes, prenatal discriminative abilities develop without benefit of previous exposure to the specific stimulus. Extensive study has been done with the Peking duck embryo and neonate, attempting to factor out the critical features responsible for the attractiveness of the maternal call, as well as those naturally occurring auditory stimuli which may be essential precursors to such discriminative behavior (e.g., Heaton, 1971; Gottlieb, 1971, 1978, 1979). These studies have isolated repetition rate as a particularly powerful aspect contributing to species-specific identific~ition in this species. In light of this, it is tempting to speculate that such a cue might be operative in the present
246
HEATON AND GALLEHER
instance, since the repetition rate of the nonattractive call is almost six times that of the attractive one. However, dominant frequency is also a likely candidate, since these, too, differed radically (2200 Hz in the attractive call versus 775 Hz in the nonattractive one). Further study will be required to clarify these possibilities. REFERENCES Evans, R. M. (1973). Differential responsiveness of young ring-billed gulls and herring gulls to adult vocalizations of their own and other species. Canadian Journal of Zoology, 51, 759-770. Gottlieb, G. (1971). Development of species identification in birds. Chicago: Univ. of Chicago Press. Gottlieb, G. (1978). Development of species identification in ducklings. IV. Change in species-specific perception caused by auditory deprivation. Journal of Comparative and Physiological Psychology, 92, 375-387. Gottlieb, G. (1979). Development of species identification in ducklings: V. Perceptual differentiation in the embryo. Journal of Comparative and Physiological Psychology, 93~ 831-854. Heaton, M. B. (1971). Stimulus coding in the species-specific perception of Peking ducklings. Unpublished doctoral dissertation, North Carolina State University. Heaton, M. B. (1972). Prenatal auditory discrimination in the wood duck (Aix sponsa). Animal Behaviour, 20, 421-424. Heaton, M. B., Miller, D. B., & Goodwin, D. G. (1978). Species-specific auditory discrimination in bobwhite quail neonates. Developmental Psychobiology, 11, 13-21. Stokes, A. W. (1967). Behavior of the bobwhite, Colinus virginianus. Auk, 84, i-33.
31, 242-246 (1981)
BRIEF REPORT Prenatal Auditory Discrimination in the Bobwhite Quail MARIETA BARROW HEATON AND ERIN GALLEHER I
Department of Neuroscience, University of Florida College of Medicine, Gainesville, Florida 32610 Bobwhite quail embryos (Colinus virginianus) were tested to two conspecific calls on Day 22 of incubation (total incubation period = 23-24 days). In previous postnatal tests, one of these calls, a maternal exodus-like call, was highly attractive, and the other, an incidental quail call, was not an effective attractant. The embryos significantly increased their rate of bill-clapping when presented with the exodus-like call, and showed no change in ongoing activity when confronted with the incidental call. Thus, the differential responsiveness parallels that seen postnatally. Such prenatal discriminative ability had previously been shown only in Anseriformes, The advantage of the bobwhite quail for studies of species-specific perceptual development is discussed.
The ability to respond differentially to various inter- and intraspecific vocalizations provides a significant basis for parent-young interactions in many avian forms. Such discriminative behavior has been shown in the domestic chick, Peking, mallard, and wood ducks, ring-billed gulls, and bobwhite quail (Gottlieb, 1971; Evans, 1973; Heat on, Miller, & Goodwin, 1978). In both Peking and wood ducks, this species specificity can also be demonstrated during prenatal periods (Gottlieb, 1971; Heaton, 1972). When confronted with a call that is a postnatal attractant (e.g., the maternal exodus call, uttered as the hen leads the young from the nest), embryos of these species respond by significantly increasing their rate of bill-clapping, vocalization, and/or leg movements. When exposed to calls that are not postnatally attractive (e.g., other species calls, or incidental calls of their own species), responsiveness is either directionally inconsistent, or in some cases, declines (Heaton, 1972). The following study was designed to investigate the possibility of prenatal discriminative respond1 This research was supported by National Institute of Mental Health Grant MH-27677. Requests for reprints should be sent to Dr. M. B. Heaton, Department of Neuroscience, J. H. Miller Health Center, Box J-244, University of Florida, College of Medicine, Gainesville, Fla. 32610. 242 0163- i047/81/020242-05502.00/0 Copyright© 1981by AcademicPress, Inc. All rights of reproductionin any form reserved.
PRENATAL DISCRIMINATION IN QUAIL
243
ing in a species not belonging to the Anseriformes, the bobwhite quail
(Colinus virginianus), of the Galliformes (Phasianidae family). In an earlier study (Heaton et al., 1978), we found hatchlings of this species to be highly responsive in both single-call and simultaneous choice tests, exhibiting a strong preference for their maternal exodus call and calls closely resembling it. They were also able to make fine inter- and intraspecific discriminations. Should this discriminative ability be expressed prenatally, the bobwhite quail would represent an additional species in which the basis of this perception and the dynamics of its emergence might be explored. Such comparative study would be of considerable interest, with the potential to provide insights into the generality of various aspects of the phenomenon, and possible clues as to underlying mechanisms. The subjects of the study were 35 bobwhite quail embryos (Colinus virginianus), aged 22 days of incubation (total incubation period = 23-24 days). The eggs were obtained from the University of Florida Poultry Science Department. They were incubated in forced-draft, automatic turning incubators, with temperature maintained at 37.5°C, and relative humidity at 65-75%. The incubator was located in a quiet room in which no hatchlings were housed. Thus, sibling vocalizations (prenatal) and self-vocalizations were the only sources of auditory stimulation available to the embryos. On Day 22 of incubation, the eggs were taken individually to a Plexiglas observation chamber, in which temperature and humidity were maintained as during incubation. The shell overlying the airspace was removed and the inner-shell membrane moistened with warm saline. The chorioallantoic membrane could then be visualized and it was cut as much as was necessary to gently pull the embryo's head out of the egg (the body remained confined within the shell). This preparation was then placed on a sterile gauze pad. Bill-clapping was monitored either by an observer who maintained a manual count, or by a modified Brush Model 220 analog recorder (the two methods proved equally reliable). The tests were done blind, with the experimenter having no knowledge as to the nature of the stimulus call being used, or any aspect of the previously observed postnatal responsiveness to the cells. Intraobserver reliability coefficients were calculated, with counts for each half of a group compared. These coefficients averaged .82 across all test conditions, and were as high as .96 for the prestimulus baseline periods. A 10-cm speaker inside the testing incubator, connected to a tape recorder, provided the stimulus calls. The speaker was positioned 18 cm from the embryo, and the test calls were played at an acoustic level of 80-82 db, as measured prior to each test, with a Triplett Model 370 sound-level meter. Following a 15-min acclimation period, the test commenced. Each test consisted of three periods: a 5-min prestimulus period, a 1-min stimulus
244
HEATON AND GALLEHER
period, and a 5-min poststimulus period. Two stimulus calls were used. The first was the most attractive of the calls used in our previous study of postnatal preferential behavior in this species (Heaton et al., 1978). This call was virtually identical to a bobwhite call recorded during an exodus from the nest, having only slight differences in minor frequency peaks. Its phrasing, duration, repetition rate, dominant frequency, and frequency modulations are the same as those of the exodus call. Since the exodus call in this species occurs in different contexts and subserves more than one function (Stokes, 1967), we considered the two calls synonymous, although the present call (which for convenience we will term the maternal exodus-like call) was not recorded during a parent-young interaction. In a simultaneous choice test in our earlier study, this call was significantly preferred over the call recorded during an actual exodus. Thus, it was chosen for the present study. The call has five notes, uttered at a repetition rate of 1.6 notes per second, with dominant frequencies at 2200 Hz (major peak) and 1475 Hz (minor peak). The second call was an incidental bobwhite quail call, which had a low attractive value in our previous study (only a few animals approached it in a single call test, with long latency of approach and very short duration of stay within the designated approach area). This call consisted of 28 notes, uttered at a rate of 10 notes per second, with dominant frequencies at 775 Hz (major peak) and 680 and 850 Hz (minor peaks). Both calls were recorded under natural conditions. As shown in Table 1, the bobwhite quail embryos responded to the maternal exodus-like call by increasing their rate of bill-clapping, from a baseline rate of 20.73 movements per minute, to a rate of 36.16 moveTABLE 1 Bill-Clapping Measures in 22-day Bobwhite Quail Embryos before, during, and after 1-min Exposure to Two Conspecific Calls Bill-clapping (rate/min) Test call
Mean
SD
p~
Bobwhite maternal exodus-like call (N = 19) Prestimulus period (5 min) Stimulus period (1 min) Poststimulus period (5 min)
20.73 36.16 17.42
19.10 37.54 18.02
-< .02 ns
Bobwhite incidental call (N = 16) Prestimulus period (5 min) stimulus period (1 min) Poststimulus period (5 rain)
22.08 26.18 26.43
15.55 22.64 12.63
-ns ns
Statistical comparisons made to prestimulus period. Two-tailed Wilcoxon test.
PRENATAL DISCRIMINATION IN QUAIL
245
ments per minute. This increase was statistically significant (p < .02, Wilcoxon test, two-tailed). Fifteen out of eighteen animals, or 83%, contributed to this increase (one embryo did not change its baseline rate). When exposed to the incidental call, there was no significant change in bill-clapping. Of the 16 animals tested, 5 increased their rate of billclapping and 10 decreased. In one animal, the baseline rate did not change. This study demonstrates that like the Anseriformes which have been tested, bobwhite quail embryos are capable of auditory discrimination during the last day or two prior to hatching. When confronted with a stimulus call that elicits strong postnatal approach or preferential behavior, these embryos respond by significantly increasing their rate of bill-clapping over nonstimulus baseline levels. Conversely, when exposed to a call which is not postnatally attractive, no significant change in bill-clapping activity occurs. Thus, as in the Peking duck and to some extent, the wood duck, this prenatal differential responsiveness closely parallels, and thus is predictive of, postnatal behavior. The degree to which the quail embryos modified their ongoing billclapping activity in response to their maternal exodus-like call was striking. The mean increase in response rate was 74%, with 15 of 18 animals participating in this excitatory reaction. In Peking duck embryos, a mean increase of 63% has been reported during exposure to the maternal call (Gottlieb, 1971) and in the wood duck, an increase of only 29% has been seen (Heaton, 1972). This high degree of responsivity in the bobwhite again parallels the situation seen postnatally. In three approach tests in which the present attractant call was used in our previous study (both single-call and simultaneous choice tests), 81 animals responded, out of 82 tested, or an incidence of nearly 99% (Heaton et al., 1978). Such exceptionally consistent responsiveness is unusual indeed [see, for example, Gottlieb's (1971) lamentations on the behavioral vicissitudes of the domestic chick, a difficulty which renders them almost useless in studies of this sort). The bobwhite quail, then, would appear to be an energetic and decisive little animal, and one ideally suited to the study of speciesspecific perceptual development. In the bobwhite quail, as in the Anseriformes, prenatal discriminative abilities develop without benefit of previous exposure to the specific stimulus. Extensive study has been done with the Peking duck embryo and neonate, attempting to factor out the critical features responsible for the attractiveness of the maternal call, as well as those naturally occurring auditory stimuli which may be essential precursors to such discriminative behavior (e.g., Heaton, 1971; Gottlieb, 1971, 1978, 1979). These studies have isolated repetition rate as a particularly powerful aspect contributing to species-specific identific~ition in this species. In light of this, it is tempting to speculate that such a cue might be operative in the present
246
HEATON AND GALLEHER
instance, since the repetition rate of the nonattractive call is almost six times that of the attractive one. However, dominant frequency is also a likely candidate, since these, too, differed radically (2200 Hz in the attractive call versus 775 Hz in the nonattractive one). Further study will be required to clarify these possibilities. REFERENCES Evans, R. M. (1973). Differential responsiveness of young ring-billed gulls and herring gulls to adult vocalizations of their own and other species. Canadian Journal of Zoology, 51, 759-770. Gottlieb, G. (1971). Development of species identification in birds. Chicago: Univ. of Chicago Press. Gottlieb, G. (1978). Development of species identification in ducklings. IV. Change in species-specific perception caused by auditory deprivation. Journal of Comparative and Physiological Psychology, 92, 375-387. Gottlieb, G. (1979). Development of species identification in ducklings: V. Perceptual differentiation in the embryo. Journal of Comparative and Physiological Psychology, 93~ 831-854. Heaton, M. B. (1971). Stimulus coding in the species-specific perception of Peking ducklings. Unpublished doctoral dissertation, North Carolina State University. Heaton, M. B. (1972). Prenatal auditory discrimination in the wood duck (Aix sponsa). Animal Behaviour, 20, 421-424. Heaton, M. B., Miller, D. B., & Goodwin, D. G. (1978). Species-specific auditory discrimination in bobwhite quail neonates. Developmental Psychobiology, 11, 13-21. Stokes, A. W. (1967). Behavior of the bobwhite, Colinus virginianus. Auk, 84, i-33.