Female cooing promotes ovarian development in ring doves

Physiology & Behavior, Vol. 37, pp. 371-374. Copyright © Pergamon Press Ltd., 1986. Printed in the U.S.A.

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Female Cooing Promotes Ovarian Development in Ring Doves MEI-FANG CHENG

Institute o f A n i m a l Behavior, Rutgers University, 101 Warren Street, Newark, N J 07102 Received 12 September 1985 CHANG, M.-F. Female cooing promotes ovarian development in ring doves. PHYSIOL BEHAV 37(2)371-374, 1986.--In female ring doves (Streptopelia risoria), hearing their own coos promoted greater follicular growth than hearing males coo, as demonstrated by the playback of various coos to experimentally muted females, under normal conditions. This difference in follicular growth suggests that the females' own cooing, not the males' cooing, stimulates the ovarian response. Ring doves

Cooing

Ovarianresponse

HORMONAL control of the female reproductive system is strikingly similar across different species, including women [15]. Similarly, social influences on ovarian activity have been reported in many species. For example, among college women dormitory roommates and close friends show synchronized menstrual cycles [14]. In mice and rats, the presence of males advances the onset of puberty in females [16,17], and in female praire voles, uterine growth is triggered by male secretion [2]. In most birds, male song induces egg-laying [1, 7, 9, 10]. Most if not all studies of these phenomena have been designed to address which aspects of the social factors (association by human females, odors of male rodents, and specific song characteristics of male birds) stimulate female reproductive functions. Clearly absent in these studies is a consideration of the dynamic nature of social interactions. Most social encounters are reciprocal interactions; the behavior of the recipient may be as important as that of the partner in giving rise to endocrine changes in the recipient. During courtship ring doves exhibit behavioral patterns leading to egg-laying. These patterns have provided a useful model for studying the hormonal and neural bases of reproductive behavior. In the present study we report that in the ring dove it is the female's own courtship nest-cooing, in response to the male's courtship behavior, that directly stimulates her follicular development. When in breeding condition, the male ring dove typically initiates courting by calling two syllable notes (bow-cooing and nest-cooing) interspersed with chasing activity. The female joins in nest-cooing with the male at the nest site for a period of time; the male then leaves and the female performs solo cooing while the male collects nest materials for nestconstruction. A few days later, the female lays a clutch of two eggs. Females stop cooing abruptly after laying the 2nd egg. In the course of studying the function of estrogen binding sites in the midbrain, the n. intercollicularis (ICo) region

[13], we noted that the female's nest-coo response was drastically reduced as a result of lesions in this brain region [5]. Lesioned females were otherwise responsive to male courtship; they approached males and even copulated with them. Unexpectedly there was no sign of follicular growth; since males courted ICo-lesioned females as much as shamlesioned females, the absence of male courtship could not have been the cause of the failure of ovarian development. To determine whether the failure of follicular response in ICo-lesioned doves was due to an impairment of neural tissues mediating ovarian development, we reproduced the muting effect of the above CNS lesion by severing the motor nerves (the tracheosyringealis branch of the hypoglossal nerve) innervating the syrinx, while leaving the brain intact. Females with these peripheral nerve cuts behaved in much the same manner as the ICo-lesioned females when they were paired with courting males; they actively interacted with the males but did not engage in nest-cooing. Again despite the males' vigorous courting, there was little sign of follicular response [4]. These results led to the hypothesis that it is the females' own nest-coo displays which promote their ovarian development [3]. There are two ways by which the female's own nestcooing might affect her follicular development: (1) hearing her own nest-cooing (acoustic feedback), and (2) performing nest-cooing (proprioceptive feedback). If acoustic feedback were involved in the induction of ovarian development, then devocalized females should show follicular growth when they hear recordings of their own nest-cooing, but not when hearing those of their mates. This paper reports the effects of hearing recordings of different kinds of coos on the ovarian responses of muted female ring doves. METHOD A total of 53 females and 60 males were used as experimental birds. Three females were discarded after failing the

371

CHENG

372

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1

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b

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FIG. 1. Sonograms of the nest-coo of the ring dove: (a) female nest-coo and (b) male nest-coo.

TABLE 1 MEAN INCREMENT IN FOLLICLE SIZE (DIAMETER IN ram) OF DEVOCALIZED AND SHAM FEMALES HEARING PLAYBACKS OF THEIR OWN VS. OTHER TYPES OF COOS

Initial follicle* size (range)

Mean folliclet size increment

Number of birds with size increment >2 mm

Stimulus condition

N

Devoc + Male

10

4-5

2.1 a - 2.3

6

10

4-5

6.8a +- 0.9

10

10

4-5

4.7b - 1.8

7

10

4-5

1.7a _-_0.1

4

10

4-5

6.5b _+ 1.1

9

COOS

Devoc + female's own coos

Devoc + other female's coos Devoc + no playback Sham + no playback

Testing for homogeneity of variance, F(4,45)=5.7, p<0.01, is followed by t-test. Different superscripts denote significance at a=0.05. *Follicle size was measured with Vernier callipers 3-5 days before the playback experiment (the initial follicle size) and again on the day after the last playback (the 2ridfollicle size); both measurements were done in the morning. tMean increment in follicle size=the 2rid follicle size.--the initial follicle size.

post-devocalization test with males. Ten of the 60 males were used to prime the females during recordings of females' nest-cooing. These same males also provided the recordings of male nest-cooing. The general procedures were: (1) Recordings of females' nest-cooing were obtained while exposing the females to active male courtship; (2) Females were subjected to devocalization (N=40) or sham-devocalization (N=10) and tested for the effectiveness of the devocalization procedure; (3) Three to five days before playback and five to seven days after devocalization, females were laparotomized to determine size (diameter) of the largest follicle; (4) Playback and behavioral observations were initiated one day after male and female pairs were placed in sound isolation chambers (Industrial Acoustics, Inc.). In this experiment, playbacks were carried out in the presence of the male to mimic normal breeding conditions, varying only the types of coos played. Playbacks without males present were later carded out in a separate study (see discussion).

Surgery Devocalization. Females were devocalized by inserting a 11/2 inch length of polyethlene tubing (3/16" OD, 1/8" ID) into the interclavicular sac immediately surrounding the syrinx. When this tubing is open, the interclavicular sac is no longer inflated during respiration. Movements of the sac provide the energy (air) source required for vocalization. Hence the above procedure renders the bird unable to emit sound. This devocalization procedure is reversible by simply plugging the open end of the tubing. Laparotomy. Females were restrained on a pegboard with their left sides facing up. A small incision was made to expose the left ovary (only the left ovary is functional in this species); the diameter (in mm) of the dominant (largest) follicle was measured with Vernier callipers. Cuthbert [6] has documented clearly that only two follicles out of two dozen develop in each cycle. Moreover, the dominant follicle re-

FEMALE COOING AND OVARIAN DEVELOPMENT mains dominant until ovulation. By measuring the dominant follicle before and after playback, we could be assured that the same follicle was measured. Females were then assigned to the playback of different types of coos: male coos, the female's own coos, or another female's coos; two other groups served as controls, devocalized and shamdevocalized females without playback. Recordings. Nest-coos were recorded with a Nagra IVstage recorder at 19.05 cm/sec on Scotch low-noise magnetic tape, using a Senheiser microphone, Tapes o f females' nestcoos were prepared by editing out those sections containing male calls. Tapes of male calls were obtained in a similar fashion. Playbacks. The tapes were played back to the females in sound isolation chambers, equipped with loud speakers. Before each playback experiment, a male-female pair was introduced to a sound isolation chamber for one day of habituation, during which the male and female were separated by an opaque partition. On the following day the partition was removed, allowing the birds to interact with each other, and playback sessions began. Each session lasted for 2 hr, between 800 and 1300 hr. Sessions were conducted daily for 5 consecutive days. The male and female were allowed to interact during and after sessions. RESULTS AND DISCUSSION

As shown in Table 1, playing back the females' own coos (Fig. la) resulted in significantly more follicle growth than playing back male coos (Fig. lb) (t=8.70, p<0.005). Follicle growth was as great in females exposed to recordings o f their own coos (for two hours) as it was in females allowed to call and hear their own coos although the latter females (shams) never engaged in nest-cooing continuously for a full 2 hours ( S h a m - - n o playback) (t =0.11 ; p>0.45). Since the females were devocalized, these findings suggest that hearing their own coos stimulated the ovarian response. Furthermore, since under natural conditions a female must produce coos to hear her own, the present finding suggests that audiofeedback is involved in the self-stimulation effect of nest-cooing. Recently it has been reported [18] that motor neurons (such as hyperstriatum ventrialis pars caudalis, HVc) and motor nerves (the tracheosyringeal nerve) innervating the vocal organ (syrinx) selectively respond to auditory stimulation in many species of song birds. This raises the possibility that in the present study, playing back the female's nest-cooing induced proprioceptive responses from the vocal motor system as well as auditory reception in the devocalized birds. This possibility is currently being tested. It is also interesting to note that neurons selectively responsive to a bird's own song have been identified in the HVc region of the white-crowned sparrow [12]. Analogous neurons may exist in the female dove brain. The results also demonstrate that follicular growth may be stimulated by exposure to coos from other females,

373 perhaps as effectively as by exposure to the females' own coos (t= 1.68, p>0.05). An independent pilot study, however, suggested that the effectiveness of hearing nest-coos other than the females' own may depend upon testing conditions. In this instance devocalized females were tested under colony conditions rather than in acoustic isolation. The females were paired with stimulus males for 24 hr, after which the males were removed. On subsequent days females in one subgroup (N=4) were exposed daily to playbacks of their own nest-coos; females in another subgroup (N=4) heard playbacks o f coos from other females. Of course all females could hear colony vocalizations, which included frequent nest-coos by both males and females. Tested under these conditions, devocalized females hearing playbacks of their own coos again responded with follicular enlargement, whereas those exposed to the coos of other females failed to show any increment in follicle size (Cheng and Perrussi, unpublished observation). The effectiveness of the playbacks in promoting follicular development was particularly striking in this study, because it occurred in the absence of male partners. That 24 hr of male courtship by itself was insufficient to induce follicular growth is consistent with the finding of Lehrman et al. [11] that a minimum of 4-5 days of continuous stimulation by males is necessary to enable females to complete ovarian development. In summary, the present findings suggest that the ovarian response culminating in egg-laying, typically observed in a female ring dove after pairing with a stimulus male, is mediated by the female's nest-coos which feed back to stimulate her own hypothalamus-pituitary-ovarian system. This conclusion does not diminish the importance o f male courtship; after all, it is the male's nest-coos that induce the female's nest-coos. The conclusion does mean that as long as the female engages in nest-cooing, whether in response to a male's coos or to a pet owner's hand, ovarian development can be stimulated. Endocrine changes in response to social influences are not limited to the female system. The male endocrine system exhibits the same level of sensitivity. For example, in mammals, including man, olfactory and/or visual cues emitted by estrous females stimulate endocrine release in males [8]. The present findings suggest that these endocrine responses may be an indirect effect of the individual's behavioral response to the social milieu. In this light, endocrine change is not a passive response to social simuli but rather a consequence of an individual's active interaction with those stimuli.

ACKNOWLEDGEMENTS This is contribution number 418 of the Institute of Animal Behavior, Rutgers University. This work was supported in part by NSF grant BNS-8121495 and in part by Charles and Johanna Busch Memorial Fund 6-49124. I thank C. Desiderio for the expert assistance in data collection. Last, but not the least, my special thanks to Dr. Anne Mayer for assistance in standard English.

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