Stimulation of ovarian development and egg laying by male courtship vocalization in budgerigars (Melopsittacus undulatus)

STIMULATION OF OVARIAN DEVELOPMENT AND EGG LAYING BY MALE COURTSHIP VOCALIZATION IN BUDGERIGARS (MELOPSITTACUS UNDULATUS) BY BARBARA F . BROCKWAY

Department of Zoology and Entomology, The Ohio State University, Columbus, Ohio . Table Brief Smeary of s thee Typical Siloatioa(s)) is

The budgerigar, Melopsittacus undulatus, is an obligatorily colonial Australian parrot that will breed throughout the year under favourable laboratory conditions. Pairs with nest boxes but isolated from the sight and sound of others, typically engage in little or no vocal and visible reproductive displays and possess undeveloped gonads and sex ducts . Sounds produced by males promote full ovarian development and oviposition in : (1) unpaired females kept without nestboxes in constant darkness which simulates lighting within a nestbox (Vaugien, 1951) ; (2) unpaired females provided with suitable nestboxes and a daily photoperiod of 12 hours (Brockway, 1962) ; (3) pairs provided with suitable nestboxes and a daily photoperiod of 10 to 12 hours (Ficken et al., 1960 ; Brockway, 1964a) . In the third situation, females heard vocalizations of their mates as well as vocalizations of other males . Also, there was no significant difference in ovarian development and oviposition between females of pairs able to see and hear other pairs and females of pairs able only to hear other pairs. In pairs able to see, but not to hear others, only those females laid or showed gonadal development whose mates performed much warbling (Brockway, 1964a) . Since budgerigars seem to be the only avian species known so far in which an auditory stimulus promotes ovarian development and ovulation, this preliminary study was undertaken to identify that stimulus. To minimize environmental influences, tests were conducted under conditions similar to those used by Vaugien (1951) : unpaired females were tested without nestboxes and in constant darkness . Males perform six different vocalizations .

Vocalization

sod they

When typically performed

Squack

Following and during a disturbance

Chedelee*

After squacking subsides or upon the introduction of separately caged new individuals into a room with others

Loud Warblet

Sitting with ruffled crown and throat feathers, either with or without a mate . No specific orientation. Highly mimetic in nature

I Following a rebuffed attempt at

Whedelee

courtship . Often alternated with displacement head flicks Tuks#

Oriented bill to bill with mate . Often in conjunction with Nudging, a precopulatory display

Soft Warble

Oriented bill to bill with mate. Generally preceded and followed by various visible and highly sexually motivated precopulatory actions

*May function as a "location note" . tMay function to stimulate male gonadal activity and sexual behaviour patterns . ;May function to stimulate females to solicit for copulation . Four of these (Loud Warble, Whedelee, Tuks and Soft Warble) are typically performed by individuals with sperm-producing testes in courtship contexts and the frequencies of these four increase with increasing frequencies of their performer's visible precopulatory displays . Information about all six vocalizations is summarized briefly in Table I (for details see Brockway, 1964b, 1964c) .

*The majority of this work was done while the author was a staff member of the Biology Department of Western Reserve University . These studies were supported by a National Science Foundation Institutional Grant to Western Reserve University, and are presently supported by Research Grant GB 3191 made by the National Science Foundation to the Research Foundation of The Ohio State University as well as the generous provision of seed and conditioning food by the R . T. French Company of Rochester, New York .

Materials and Methods Animals Female budgerigars of domesticated strains were laparotomized 3 to 4 days before testing . Only 575



5 76

ANIMAL BEHAVIOUR, XIII,

individuals with undeveloped ovaries (follicles of 1 . 5 mm . or less in diameter) were used . All had bred at least once previously, had been housed in large stock cages without nestboxes and had been visually separated from males for 6 months prior to experimentation . Maintenance Females were individually housed in I in . hardware cloth cages, 2 x 2 x 1 ft . enclosed within thick cardboard boxes. Small holes slanting upward were punched in the cardboard walls to provide ventilation with minimal light. Birds were given an initial lighted half-day to acclimate to cage conditions . Thereafter, all were exposed to about 10 minutes of light daily during the check for food, water and eggs. Although females in any experimental situation could hear each other, they generally remained silent and spatial separation prevented their hearing females or taped male vocalizations of other situations . French's Parakeet Seed, French's Conditioning Food, cuttlebone, gravel and water were provided ad libitum. Procedures Male vocalizations were recorded on either Scotch brand 200-24 or a graphite base tape . They were played daily on Norelco or Wollensak tape recorders either in 2 hour sequences for a total of 6 hours or in one continuous 3 hour sequence . Only sounds made by a single male were heard at any one time ; however, samples of each vocalization from several males were used in each sequence. Each experimental group consisted of five females . The experiments were terminated on day 22 and the ovaries were examined by laparotomy . Females laying during an experiment were credited with the typical follicular diameter (9 . 0 mm .) of an ovulated ovum for each egg, up to a total of two eggs . For non-layers, diameters of the two largest follicles were measured . Results were analysed by analysis of variance and Duncan's multiple range tests (Simpson, Roe & Lewontin, 1960 ; Freund, Livermore & Miller, 1960) . * The null hypothesis was rejected at a P level of less than 0 .05 . Situations Two studies were conducted. In the first, five groups were each presented exclusively with one of the following for 6 hours daily : (a) a mixture *Assuming a homogeneity of variance, the former test indicates if a significant difference exists among the groups whilst the latter enables one to pinpoint which group(s) differ(s) significantly from the other(s) .

4

composed of equal durations of Squacks and Chedelees, (b) Loud Warble, (c) Tuks, (d) Whedelees, and (e) Soft Warble . In addition, one group that could hear no male vocalization and another group presented with a sequence composed of equal durations of each of the male vocalizations (a) to (e) for 6 hours daily served as controls . For the second study, Soft Warble was arbitrarily divided at approximately 2,000 cycles per second into a part containing mainly high pitched components and one containing mainly low pitched components . Each part contained similar amounts of melodious and raspy sounds . Each of four groups was daily presented exclusively with one of the following : (a) 6 hours of high pitched components, (b) 6 hours of low pitched components, (c) 3 hours of high pitched components and, (d) 3 hours of low pitched components of the Soft Warble . The vocal patterns used in this second study were obtained from master tapes of Soft Warble used for the first study . Results and Discussion The results including statistical analyses are presented in Tables II and III . All females that laid eggs did so during the last 5 days of either study . No significant difference was found between any of the groups regarding the dates that first eggs of clutches were laid . Of the three vocalizations temporally associated with visible male precopulatory displays, Soft Warble was found to be the most effective stimulus for ovarian activity . Tuks and Whedelees did elicit laying by one female in each group, but, possibly due to the small number of females per group (five), there was no significant differences in ovarian activity between either of these or and other experimental situation except that involving Soft Warble . Ovarian activity of the groups hearing Tuks or Whedelees was significantly less than that of the group hearing Soft Warble. That the group of females hearing all vocalizations did not show ovarian activity significantly different from those hearing no vocalization, or specific vocalization except for Soft Warble, may have been due to the presentation of a subthreshold quantity of the stimulatory vocalization : the group hearing all male vocalizations heard only one-fifth as much of any one vocalization as the other five groups . This arrangement was necessary so that all groups would hear vocalization for the same daily total number of hours . Both parts of the Soft Warble were equally



BROCKWAY : MALE COURTSHIP VOCALIZATION IN BUDGERIGARS Table

II. Effects of Various

577

Male Vocalizations Upon Ovarian Development .

Experimental groups designated by vocalization heard

Measurements Squacks & Chedelees No . females per group

5

Mean follicular' diameter (mm .)

2.1

No. of females laying : (a) during experiment (b) projected to 24 days

Loud Warble

None

5

All

Tuks

Spft Whedelee Warble

5

5

5

5

5

2.2

2.4

2 .7

6.0

6 .9

13 . 7

0

0

0

0

1

3t

0

0

0

0

1

4

1

Duncan's multiple range$

Abbreviated results of analysis of variance of above follicular diameter data

I

Source of variation

Degrees freedom

Mean square

Between groups

6

77 .47

Residual error

28

19 . 16

"F" value

P

4.04

<0 .01

*Sum of diameters of the two largest follicles per indivudal for all birds of one group was divided by the number of birds in that group (5). t An additional female in this group had an ovum ready to ovulate when laparotomized at experiment's end (day 22) . $Abbreviated results of Duncan's multiple range test on mean follicular diameters . A line drawn under any set of means indicates the difference(s) between/among them are not significant . Table In . Effects of Amount versus Components (comps.) of Male Soft Warble (SW) upon Ovarian Development .*

Situation

No . females

Mean folliculart diamter (mm.)

I

"F" value

Effect

P

SW high comps. 6 hr. daily

5

7.0

Amount

6 . 21

<0 .025

SW high comps . 3 hr. daily

5

2 .2

Components

1 . 76

>0. 10

SW low comps . 6 hr. daily

5

11 .4

SW low comps . 3 hr . daily

5

4 .2

Interaction of both factors

0 . 25

l

>0 .20

*Analysis of variance . tSum of diameters of the two largest follicles per individual for all birds of one group was divided by the number of birds in that group (5) . stimulating to ovarian activity in the small sample sizes used ; however, daily presentations of either part for 6 hours were more effective than for 3 hours . This suggests that the proportion of the components of Soft Warble may not be as important as the duration . But, possible differences may exist between or among other arrangements of Soft Warble components . All previous studies which indicated that, apart from the sight of others (pairs), male vocalizations as a whole promote ovarian activity and oviposition (Vaugien, 1951 ; Ficken

et al., 1960 ; Brockway, 1962, 1964a) involved comparison of females able to hear the vocalizing of several males in concert with females hearing no males. The present study demonstrates that hearing the vocalization of a single male is sufficient to stimulate ovarian activity and oviposition. It is possible, however, that vocalizing by several males in concert may prove to be more effective . Summary

Five different tape recorded groups of

male

578

ANIMAL BEHAVIOUR, XIII, 4

vocal patterns were played each to a different group of females kept in constant darkness . Soft Warble, a vocalization closely associated with visible male precopulatory behaviour patterns and performed in intimate relation to the female, was found to greatly stimulate ovarian activity and egg laying in budgerigars . Other vocalizations produced results insignificantly different from a control group hearing no vocalization . While either component half of arbitrarily divided Soft Warble seemed just as stimulating to ovarian development as the other half, daily presentation of either for 6 hours hours was more effective than 3 hours. REFERENCES Brockway, B. F . (1962) . The effects of nest-entrance positions and male vocalizations on reproduction in budgerigars . Living Bird. First Ann . Cornell Lab. Ornithology, 93-101 . Brockway, B. F. (1964a). Social influences on reproductive physiology and ethology of budgerigars

iitacus undulatus). Anim.

Behav.,

12,

(Melop1 Brockway, B . F. (1964b). Ethological studies of the budgerigar (Melopsittacus undulatus) : non-reproductive behaviour. Behaviour, 22, 193-222. Brockway, B . F . (1964c) . Ethological studies of the budgerigar : reproductive behaviour . Behaviour, 23, 294-324 . Ficken, R. W., van Tienhoven, A ., Ficken, M . S . & Sibley, F . C. (1960) . Effect of visual and vocal stimuli on breeding in the budgerigar (Melopsitacus undulatus). Anim . Behav., 8, 104-106. Freund, J . E., Livermore, P. E . & Miller, I . (1960) . Manual of Experimental Statistics . Englewood, New Jersey : Prentice Hall. Simpson, G . G., Roe, A . & Lewontin, R . C. (1960) . Quantitative Zoology . Ames : Iowa State University Press . Vaugien, L . (1951). Ponte induite chez la Perruche ondulee maintenue it l'obscurit6 et dans l'ambience des volitres. C.R. Acad. Sci. (Paris), 232, 1706-

1708 .

(Accepted for publication 2nd August, 1965 ; Ms. number: 555) .

PUBLISHER'S NOTE The publishers regret that a number of printer's errors appeared in the paper "A Descriptive Analysis of the Behaviour of the African Cichlid Fish, Pelmatochromis guentheri (Sauvage)", by Dr . Arthur A . Myrberg which was published in the April/July issue, and offer their apologies to Dr . Myrberg and to their readers.