Anim . Behav., 1975, 23, 869-882

EFFECTS OF STIMULI EMANATING FROM THE NEST ON THE REPRODUCTIVE CYCLE IN THE RING DOVE. II : BUILDING DURING THE PRE-LAYING PERIOD BY

SHEILA J . WHITE

Institute of Animal Behavior, Rutgers University, Newark, New Jersey

Abstract. The nest is a major focal point of the reproductive cycle in the ring dove (Streptopelia risoria) . This study shows that the state of the nest is an important determinant of the type of nest-building exhibited. For example, birds faced with an empty nest bowl every day removed more material from dispensers and built more actively than did those allowed to construct nests normally . Conversely, those given completed nests were not very active, but were more efficient in using the little they removed from the dispensers and showed a reversal of sex roles in building . The relations between nestbuilding and egg-laying, and between male and the female are discussed . The reproductive cycle in birds is known to be influenced by a variety of environmental factors, some of which can be remarkably subtle in their action. One such factor is the presence of a suitable nesting site and of nesting material . Marshall & Disney (1957) demonstrated experimentally that the presence of green grass (used for nesting material) was the principal stimulus for the beginning of breeding in the African red-billed weaver (Quelea quelea) . Lehrman, Brody & Wortis (1961) showed that when female ring doves (Streptopelia risoria) were paired with mates, ovulation was more probable if a nest bowl and nesting material were also provided . Hinde & Warren (1959) demonstrated that stimuli coming from the nest cup accelerated egg-laying in female domestic canaries ; birds deprived of material and nest cups delayed their laying. Whether it is merely the presence of a nest site and nesting material or the actual participation in building that affects laying is not always clear . However, Hinde (1958) suggested that performance of nesting movements had some reinforcing value . Also, Slater (1969) showed that in Bengalese finches (domestic form of Lonchura striata) where the male usually carries nesting material to the female, if the pair was separated and only the male was provided with nesting material, then egg laying in the female was delayed . In other words, some direct involvement by the female was necessary, either in handling or sitting on the material. This involvement occurs in a particular time relationship to egg-laying. White & Hinde (1968) noted that of many measures considered, nestbuilding bore the most constant relation to egg laying during the breeding season in the female

canary. This may give us some clue to understanding the onset of nest-building . The present study is concerned with this relationship in the ring dove, and is further concerned with finding which measures could be used to assess a pair's readiness to build. Pairs of ring doves were either allowed to construct a nest or were given one whose condition was controlled either by being full from the outset or being emptied every day. In the first paper of this series (White 1975a) a variety of behavioural patterns was found to be affected by the state of the nest . In this paper, those activities involving the handling of nesting material are presented in more detail, and the quantitative measures of the products . of these activities (amounts of material removed from dispensers and found in the nest bowls) are also presented . The aim of this study was to analyse how the normal course of nest-building was influenced by experimental manipulations of the nest condition. Methods The subjects, housing, maintenance and basic experimental procedures are all presented in White (1975a). A summary of the experimental groups and any techniques peculiar to this paper will be presented here . (For details, see Miller 1965) . Three groups were established : (1) Empty group (E) : twenty-one pairs of birds, eleven of which were observed ; these pairs were building in a nest bowl that was emptied daily . (2) Continuous group (C) : twenty-one pairs of birds, eleven of which were observed ; these were allowed to build a nest in the normal way without interference from the experimenter . 869



8 70

ANIMAL BEHAVIOUR,

(3) Full group (F) : twenty pairs of birds, ten of which were observed ; these were building in a nest bowl that was full at the start of each day. On the right-hand side of every cage there was a nest bowl (a preparation dish, Fisher catalogue no . 8-807 ; 115 mm outside diameter, 50 mm high) and a nest dispenser, which was designed so that a quantitative measure might be made of the amounts of material removed and handled daily . Each dispenser was a copper box (25 x 5 x 5 cm) sprayed with dove-grey, flat enamel, house paint to blend with the decor of the cage. Two pointed prongs were soldered to the box and bent inward, allowing 6 . 25 cm of space on either side of each prong, to discourage birds from using the dispensers as nesting sites. Mature adults do not fit into these spaces readily . The nesting material was pine needles ('twigs') measuring between 15 cm and 22 . 5 cm in length, supplied by the Palmetto Pigeon Plant, Columbia S.C. These were marked with a 6-mm colourband at each end by dipping them into mixtures of ordinary house paint or rubber latex . By presenting differently coloured nesting material on each day, the time course of nesting activity could be retraced for any pair by matching the colour with the day on which it was presented . Thirteen colours were used in all, to allow sufficient variety to cover the expected duration of the pre- and post-laying periods : (1) red (latex) (2) white (3) pink (4) light blue (5) dark blue (latex) (6) lavender (7) aqua (8) grey (9) yellow (10) green (11) light orange (12) dark orange (latex) (13) purple (latex) . A different colour of nesting material was given each day ; the colours were chosen in random order . Nesting Material Data The measures of nest-building, using the amount of nesting material removed, were derived from two basic counts : (1) the number of twigs removed from the dispensers . (It had been established that a bird removed only one twig from the dispensers at a time .) (2) the number of twigs found inside the nest bowl . For the C and F groups, this count was made at the end of the experiment . For the former group, the day on which any particular coloured twig was placed into the bowl could be ascertained by its colour. Any coloured twig found on the tray other than the colour du jour would have had to have been inside the nest bowl on the previous day(s), and was therefore included in

23, 4

the count for the day on which the colour was presented . This measure could account neither for those twigs that might have been built into the nest and removed on the same day, nor for those twigs that might have been built into the nest, removed, and then re-woven . There are two problems to be noted here : (a) In all groups, the trays were cleaned daily and the amount of material removed from the dispensers was counted after the behavioural observations were made . Thus, there could be no nest count on the day of introduction although there were behavioural observations on that day. (b) Since the tray counts were the results of activity over a 24-hr period, it may well be that the count on any one day was more indicative of the activity on the preceding day than for the day on which the count was made . However, since the birds are more active in the morning than in the afternoon (MartinezVargas & Erickson 1973), we shall conclude for the moment that each count is representative of the day on which it was made . These questions are important only when trying to correlate behavioural observations with nesting counts . The nest material data will be presented simply as medians . The counts have been averaged with reference to the first egg . It is to be noted that there were no differences in these measures between those pairs that were observed and those that were not . Behavioural Data Observations were made daily for 30 min of one pair at a time . Those activities that involved the handling of nesting material were recorded in detail and are reported here as frequencies per 30 min. Turning in the nest bowl, treading, and so forth which could also be considered part of the nesting behaviour, were more difficult to measure quantitatively and are not included . All other activities that did not involve the handling of nesting material were recorded as present or absent in each 15-s interval and are reported in White 1975a. The presentation of the behavioural data is as described there. Results The first two sections present the nesting material data from the sixty-two pairs of birds . These sections are followed by the behavioural data from thirty-two of the above pairs which illustrate the effects of the condition of the nest on the handling of nesting material and on the



WHITE : ROLE OF THE NEST : II . PRE-LAYING BUILDING

Fig. 1 . Median number of twigs removed from dispensers over the pre-laying period by the continuous (--- ), empty (-) and full (. . .) groups. Day 0 is the day on which the first egg was laid ; all days are with reference to day 0. roles of the male and female . The data for nesting material removed from the dispensers and the amount found inside the nest bowl were compared for those pairs observed and those not ; there were no differences. The final section will assess the measures used . Nest-building Activity as Measured by the Amount of Nesting Material Removed from the Dispensers Absolute amounts removed daily . Figure 1 depicts the median number of twigs removed from the dispensers each day by each group . There is no overlap between the F-group and the E- and C-groups on any day ; the highest point reached by the F-group (on day - 1 with reference to the laying of the first egg) is no higher than the low level initial activity of the other two groups . This conclusion is also true when data are aligned for averaging with reference to the day of introduction. In other words, the presence of a full nest has a depressing effect on the amount of material a pair will remove from the dispensers, and this depression is evident from the outset .

871

It is of interest to compare the counts of days - 1 and 0 in each group . At this time, the Egroup, whose nests had been emptied every day, was still building at a high rate . On the other hand, the F-group, which had full nests all along, showed a drop in activity on the last day . A feature of the C-group was that their data showed characteristics of each of the above extremes : Fig. 1 shows that there is a drop in activity similar to that of the F-group (which is due to eleven pairs in the C-group that had achieved a full nest), while the higher level of activity was due to ten pairs who had no nests and who, like the E-group, continued to build at a high rate. Therefore, the drop in activity which is thought to be typical at the time of egg laying (Hinde 1958), occurs only if a nest is present . (See also White 1975b). Relative amounts removed daily. It has been shown above that pairs with full nest bowls will remove less material than pairs with empty nest bowls . However, the effect of the stimuli provided by the nest must be considered together with the bird's internal state, which varies through the cycle . If the level of building is a product of the effects of internal state and external stimulation and the internal factor is the same for all groups, then normalizing the scores should remove the differences between the groups . Taking the total amount that any pair removed over the pre-laying period, is there a difference in the proportion of that amount removed from day to day? The points plotted in Fig . 2 are medians of daily scores that were derived for each pair using the following formula : (amount removed daily/total removed over the pre-laying period) x 100. When viewed in this manner, the groups overlap to a large extent . The similarity of the normalized curves would indicate that there is a variation in internal state through the cycle that causes the relative level of building to change, and this is the same in all groups. The nest condition interacts with this, leading to differences between the groups in the overall level of building in a multiplicative way (see Fig . 1) . However, there is a difference shown on day 0, when the E-group continues to pull large amounts of material (x2 = 12 . 68 ; df = 2 ; P = 0 . 01) . Thus, the course of pre-laying building is not a simple product of external and internal factors, but becomes a more complex interaction between the two, such that the absence of the nest is seen to be increasingly important as egg-laying approaches . In the last



8 72

ANIMAL BEHAVIOUR 23, 4

`~

-

-5

-4 DAYS

Fig . 2 . Median percentage of the total number of twigs removed from the dispensers over the pre-laying period accounted for by the number of twigs removed daily by the continuous (--- ), empty (--) and full (. . .) groups .

analysis, the nest must be complete in order to house the egg, and the birds will modify their behaviour accordingly . (See also White 1975b) . Nest-Building Activity as M by the Amount of Nesting Material Found Inside the Nest Bowl Absolute amount of material found in the nest bowl. Figure 3 presents the median numbers of twigs found in the nest bowl daily . Two things are to be noted : (1) the F-and C-groups are similar to one another and (2) although the Egroup tended to be more active than the others as measured behaviourally (following section) and by amounts removed from the dispensers (previous section), they appeared to place less material into their nest bowls . There are two possible reasons for these findings : (a) since the glass nest bowls that were provided tended to be slippery, the initial stages of nest construction were very inefficient because new material was constantly disturbed by the animals' movements in and out of the bowls . If a basic weave had. been established by the time the female began to sit for long periods, there was more likelihood of new material staying in place. The C-group, which was allowed to build normally, was able to achieve such a base, whereas the E-group could never do so . The Fgroup, which handled less material in general (cf. Fig. 1), placed more of what they handled into their nest bowls . (b) There was a higher incidence of building outside the nest bowl

(e .g. in the corners of the cage) in the E-group, which would tend to reduce the score for this group further. To be noted again is the decrease between days - 1 and 0 in both the F- and C-groups, when the E-groups showed an increase . Efficient me of nesting material. The previous measure suggested that the F-group was more efficient in its use of material . A more direct assessment of this is shown in Fig . 4, which represents the median amount of material found inside the nest bowl expressed as a percentage of the amount removed from the dispensers on any one day. To obtain the points on this graph, a percentage figure for each pair was derived using the following formula : (amount found in the nest bowl on any one day/total removed from the dispenser on that day) x 100. The medians of these daily percentages are plotted in Fig. 4. Of the twigs removed from the dispensers, the F-group placed a larger proportion into their nest bowls than did the Cgroup ; the latter, in turn, were more efficient in their use of nesting material than the E-group . The curves show that efficiency increases from the beginning of the cycle in all groups . The F-group is the first to reach a roughly steady level of about 50 per cent at day - 3, followed 1 to 2 days later by the C-group, which reaches a slightly lower asymptote on day -- 1 . The E-group curve, although it shows a continuous increase, suggests that its maximum efficiency is not reached until day 0. It is suggested that the time at which each group reached



87 3

WHITE : ROLE OF THE NEST : II : PRE-LAYING BUILDING

-5

-4

-3

-1

0

DAYS

Fig . 3. Media, number of twigs found inside the nest bowl over the prelaying period for the continuous (--- ), empty (-) and full ( . . .) groups . 60

50

40

MDN 0/0 30

20

10

-8

-1

-6

-5

-4

-3

-2

-i

DAYS

Fig. 4. Median number of twigs found inside the nest bowl expressed as a percentage of the number removed on any one day for the continuous (--- ), empty () and full ( . . .) groups .

0



874

ANIMAL BEHAVIOUR, 23, 4

its asymptotic efficiency corresponds with that at which they achieved a nest base of sufficient size to retain new material . (In the E-group, nine pairs had managed to build a nest in one day .) The question of whether all material removed was `intended' for the nest cannot be determined directly from this study . However, there are two kinds of indirect evidence that it was not (a) none of the groups placed a significant proportion of material removed into their nest bowls early in the cycle (Fig . 4) . Therefore, removal of material may not always be purposive . (b) many of the behavioural sequences involved in handling nesting material (see following section) were not necessarily oriented to the nest ; the more complete sequences occurring from day - 4 onwards (see Figs 6 and 8) . Therefore, one possible effect of the presence of a full nest could be to depress the general level of manipulation of material so that when material is handled by the F-group, it actually is intended for the nest bowl . The fact that a base was present would then act secondarily to insure that the material stayed in place . Thus far it has shown that all birds show nesting activity within the 4 days prior to egglaying as measured by either (a) the amount of material removed from dispensers, (b) the amount placed into nest bowls, or (c) the proportion placed of the amount removed ; the most sensitive measure depending on the state of the nest . The next section presents the behavioural data which, unlike the nesting material counts, can differentiate between the actions of the male and the female . Nest-Building Activity as Measured by the Changes in Frequency of Various Behavioural Activities To simplify presentation of the data, the activities involved with the handling of nesting material have been lumped into four categories according to whether they took place in or out of the nest bowl, and whether they did or did not lead to building . The reason for combining the data is that some activities occurred too infrequently to be presented separately . Activity outside the nest bowl (categories one and two). Potential sources of nesting material outside the nest bowl were : the dispensers, the floor of the cage, and the nest bowl itself . The source of material has not been differentiated in this analysis . Category one. This includes all activities involving manipulation of material outside the

nest bowl that did not lead to building or placing . These are : (1) pecking at the material on the ground, in the dispensers or in the nest bowl while the bird was outside the bowl ; (2) peckinglifting-dropping ; (3) pecking-lifting-carryingdropping ; (4) pecking-lifting-carrying to the nest bowl-dropping . Most of the activity in this category can be accounted for by activity l . Category two . This includes all activities involving manipulation of material outside the nest bowl that did lead to building or placing. (See below for description of building and placing.) These behavioural sequences are : (1) peckingbuilding ; (2) pecking-lifting-building ; (3) pecking-lifting-carrying-building ; (4) pecking-lifting -carrying-placing ; (5) pecking-lifting-carrying to the nest bowl-building ; (6) pecking-liftingcarrying to the nest bowl-placing . Most of the activity in this category can be accounted for by behaviour sequence 6 . (Building involves a downward sweep of the head with material in the bill, followed by tucking of the material into the apterial region . When the head is under the body, side-to-side head movements are occasionally seen, and sometimes the feathers surrounding the apterial region can be seen to open . This activity can take place inside or outside the nest bowl. The motions involved in building and placing are the same ; the difference is that in the latter case, the mate is in the way . Placing is most often exhibited by the male, and does not involve a direct transfer of material to the female's bill . Generally, the male gets onto the rim of the nest bowl or onto the female's back and goes through a building motion on top of her. She may or may not take the piece of material so placed .) Figures 5 and 6 and Tables I and II show that for those groups having to build nests (E- and C-), the males and females differ less from one another early in the cycle than later. For category one activities, a difference emerges at about day - 5 with males increasing their activity, while the females' curve, after reaching their peak, turn over and decline until day 0, when these trends are reversed . The important difference between categories one and two is that the former measures manipulation of nesting material that is not directed towards any apparent end, while the latter comprises fairly complex activity sequences that culminate in building or placing . As shown in a previous study (White 1975a), the appearance of a difference between male and female at about



875

WHITE : ROLE OF THE NEST . II : PRE-LAYING BUILDING

GAVE -t. E . .

Fig. 5 . Category one. Mean frequency of occurrence of activities involving tenial outside the nest bowl which did not lead to the handling of nestin building for the males () and females (--- ) of the continuous (C), empty (E) and full (F) groups . A '0' indicates a male mean score ; a '0' indicates a female mean score . See Table I for significance values .

a .. . ,..

CAT . 2 C

E

70

so a. . MEA N

'u•

ioo r s a

v

a

•

0

9

O

•

O .;

--

0 a--

0

.; . •; - ; GAVE

-a

A

-i -1

a

-s - .

.,

- a -a -, .

." SSS

Fig. 6. Category two. Mean frequency of occurrence of activities involving the handling of nesting material outside the nest bowl which led to building or placing for the males () and females (--- ) of the continuous (C), empty (E) and full (F) groups . A 'S' indicates a male mean score ; a '0' indicates a female mean score. See Table H for significance values .



876

ANIMAL BEHAVIOUR, 23, 4

Table I . The t-values Resulting from Two-tailed t-Tests Between the Coefficients of the Curves for Category One Activities (Fig. 5) df

Ao

A1

A2 t=0 . 3

A3 t=4 . 1**

A4

E-male x E-female

6

t=10 .4***

t=6 .5***

t=1 .6

E-male x C-male

6

2.1

1 .3

1 .4

1 .1

0.4

E-male x F-male

7

.1*** g

4-5**

0 .02

1.3

0 .4

E-female X C-female

8

2 .4*

0.4

1 .0

0 .7

0 .2

E-female x F-female

7

0.5

0.7

0.3

3 .0*

3 .0*

C-male x C-female

7

15 . 1***

10 . 9***

1 .4

4 . 0**

2.0

C-male x F-male

7

10-2***

8-0***

1 .8

0 .4

1.1

C-female X F-female

7

1 .3

0 .4

1 .1

2 . 4*

3-2*

F-male x F-female

6

1 .2

0.9

0.6

0 . 06

0.8

Significance levels are indicated as follows : * = < 0.05, * * _ < 0 . 01, * * * = < 0 . 001 ; where no asterisk appears, the t-value is not significant . The degrees of freedom are indicated, and were derived using the following formula which corrects for non-constant residual variances (Brownlee 1960) : df' : = df(S12 + S2 2)2 / (S1 4 + S2 4). Table II. The t-Values Resulting from Two-Tailed t-Tests Between the Coefficients of the Curves for Category Two Activities (Fig. 6) df

A0

A1

t = 12 .2***

t = 7 .8***

E-male x E-female

7

E-male x C-male

7

3 .6**

E-male x F-male

6

15 .4***

E-female x C-female

7

E-female x F-female

A2

t = 2 .0

A3

t = 4 . 7**

A4

t = 1 .6

1 .5

0.9

1 .4

0.5

8 .7***

2 .0

3 . 5*

0 .4

2-8*

0.8

0 .9

1.1

0.6

4

4-8**

1 .7

0 .7

2 .5

3 . 0*

C-male x C-female

7

15 .5***

10 .4***

0.9

3 . 9**

0.9

C-male x F-male

7

15 .3***

9 .8***

1 .5

2 . 7*

0 .2

C-female x F-female

5

2.1

1 .0

0.4

1 .6

3 . 2*

F-male x F-female

6

1 .4

1 .2

0.7

0.1

1 .1

Significance levels are indicated as follows : * _ < 0 . 05, ** = < 0 .01, *** = < 0 .001 ; where no asterisk appears, the t-value is not significant. The degrees of freedom (df) were derived as indicated in the legend to Table I .

day - 5 is initiated by the female who modifies her behaviour in a way that stimulates the male to deliver nesting material to her (i .e . to perform category two activities). The females do not engage in category two activities to any great extent ; the highest point on the female curve is on day 0, which may be viewed as a response to the male's increase in nest-related activities on that day . (On day 0,

the normal incubation pattern is established in some pairs : the male sitting inside the nest bowl during the day ; the females sitting in the late afternoon and through the night . As observations were made in the mornings, this would account for the increase in in-the-nestbowl activities for the males and out-of-thenest-bowl activities for the females (cf . Figs 5, 6, 7 and 8) ; see also White (1975a) for a fuller



WHITE : ROLE OF THE NEST . II . PRE-LAYING BUILDING

discussion of interrelations between the male and female on this day .) The F-group, which did not have to build a nest, showed very low activity and no significant difference between the sexes. The effects of the nest could be seen in all groups. The group that was always building in an emptied bowl had higher mean levels of activity than did the other two groups, in some cases significantly (Tables I and II), in other cases not. The F-group was both quantitatively and qualitatively different from the other two groups : the males showed a quartitative, difference in that the mean level of their activity (A 0) was considerably lower than that of the other males. They showed a qualitative difference in category two activities in that they did not vary in their performance through the cycle. The females showed a qualitative difference from the other females, in that although their mean levels of activity were similar, they engaged in these activities at different times in the cycle . Activities imide the nest bowl (categories three and four). There are potentially three sources of material for a bird who is inside the nest bowl : (1) material scattered in the immediate vicinity of the bowl that is within reaching distance, (2) material that is already inside the bowl that can be re-woven, and (3) material brought from a distance by the mate, distinguished in the following listings by having `taking' as the first step in the sequence . Only those `takes' that occurred within 15 s of a placing were recorded as such . (Often the female seemed to ignore the activity of the male and was more occupied with material in and around the bowl than with the specific twig brought by the male . The average percentage of `taking' was slightly under 25 per cent for the 4 days prior to egg 1, which was when building activity was at its peak .) Category three . This includes all activities involving manipulation of material while sitting inside the nest bowl that does not lead to building . These sequences are : (1) pecking from outside-dropping ; (2) pecking from outsidelifting-dropping ; (3) pulling from inside-dropping ; (4) pulling from inside-lifting-dropping ; (5) taking from the mate-dropping ; (6) taking from the mate-lifting-dropping . Behaviour sequences 1 through 4 account equally for most of the activity in this category . Category four . This includes all activities involving manipulation of material while sitting inside the nest bowl that does lead to building .

877

(In addition to the head-under-body motion of building noted previously, there is also a headsideways motion of building which involves tucking of material under the shoulder or wing region . This has been noted only in the nest bowl and not outside it . Further, as building movements may be impeded by the nest itself, the building sweep is not always completed, and trembling movements may be seen. Head-underbody building, sideways building, and trembling building have all been included under `building' in category four.) The sequences included under this category are : (1) pecking from outsidelifting-building ; (2) pulling from inside-building ; (3) pulling from inside-lifting-building ; (4) taking from the mate-building ; (5) taking from the mate-lifting-building. Most of the activity in this category can be accounted for by items 2 and 3 . (For the males, particularly in the E-group, this activity was sometimes performed on top of the female while she was sitting in the nest bowl .) In those groups having to build nests (Eand C-), Figs 7 and 8 and Tables III and IV show that both males and females participated in category three and four activities, although the females did so to an increasingly greater extent after day - 5. The male's activity decreases as that of the female's increases until day 0, when this tendency is reversed . For the F-group, three things can be noted : (1) the level of activity is extremely depressed, (2) the male curve is consistently higher than the female curve except on day 0, and (3) the shapes of the curves for the male and the female are not different from one another . The effect of the continual emptying of the nest bowl could be seen (a) in the females, where the E-females showed higher peaks of activity than the C-females, and (b) in the males, where the E-males did not show as large a decrease between days - 3 and - 1 as the Cmales. (This was significant only for category three activities.) The effect of having a full nest from the outset was that the level of activity shown by the F-group was extremely low, and the males were more active than the females. Several things should be clear from examination of Figs 5 through 8 : (a) The males were more varied in their activity early in the cycle than were the females. (While the males engaged in all categories of behaviour, the females only engaged in category one activities .) (b) At about day - 5, in those groups having to build nests





878

ANIMAL BEHAVIOUR, 23, 4 200 •

CAT . 3

100

C

E

F

r0 s0

30

a 10 .IAN

role . 10

A

3

a

3

0 0- 0, -1

-,

_A

-

3

-2

-1

-4

-3

_3

-1

DAYS rr1 .FGG

Fig. 7. Category three . Mean frequency of occurrence of activities involving the handling of nesting material inside the nest bowl which did not lead to building for the males (-) and females (--- ) of the continuous (C), empty (E) and full (F) groups . A '0' indicates a male mean score ; a '0' indicates a female mean score . See Table III for significance values .

100

C AT . 4

100

C

E

F

70 .

0

s0 .

30 20 MOAN

role . 10 7

I

e

S

• 3 A

1 -,

•

_3

-4 -3

-2 -1

0

-1 -7

-0

-3

-4

-3 -2 -i

DAYS , ., Fcc

Fig . 8. Category four . Mean frequency of occurrence of activities involving the handling of nesting material inside the nest bowl which led to building for the males () and females (--- ) of the continuous (C), empty (E) and full (F) groups . A ' •' indicates a male mean score ; a 'O' indicates a female mean score. See Table IV for significance values .

879

WHITE : ROLE OF THE NEST. II : PRE-LAYING BUILDING

Table III . The t-Values Resulting from Two-tailed t-Tests Between the Coefficients of the Curves for Category Three Activities (Fig. 7) df

A1

A0

1 = 10-5*** t = 13-4***

A2 t=1 . 7

A3 1=3 . 6*

A4 t=0 .8

E-male x E-female

5

E-male x C-male

7

3 .4*

2 . 9*

3 . 4*

5 .9**

2 .0

E-male x F-male

6

1 .6

0.8

0 .7

0.5

1 .4

E-female x C-female

7

1 .6

2 . 4*

0.7

1.1

0.3

E-female x F-female

8

12 . 5*

9 . 7***

2.3

2 . 9*

1 .1

C-male x C-female

6

10 .9***

13 . 9***

1 .0

8 . 3***

3 . 2*

C-male x F-male

4

2 . 8*

0.2

0.4

2.4

2. 1

C-female x F-female

6

13 . 4***

9 .0***

3 .4*

2.3

1 .0

F-male x F-female

6

0 .2

1 .3

0.5

0.0

1 .8

Significance levels are indicated as follows : * = < 0 .05, * * _ < 0 .01, * * * = < 0.001 ; where no asterisk appears, the t-value is not significant . The degrees of freedom (df) were derived as indicated in Table I .

Table IV. The t-Values Resulting from Two-tailed t-Tests Between the Coefficients of the Curves for Category Four Activities (Fig. 8) df

A0

A1

E-male x E-female

8

t= 5-8***

t = 6 . 3***

E-male x C-male

6

1.2

0 .7

0.4

1 .2

0.02

E-male x F-male

7

2 •S *

0.4

0.4

0.6

1 .5

E-female

C-female

7

1 .6

1 .8

0 .2

0 .7

0 .4

E-female x F-female

5

10-7***

7 .4***

2 .2

3 . 0*

1 .3

C-male x C-female

6

9 . 6***

9 . 5***

1 .9

5 .4**

1 .1

C-male x F-male

6

2.0

0.2

1.1

2.2

2.0

C-female x F-female

7

7 . 8***

3 .6**

3 .2*

1 .3

F-male x F-female

6

1.1

0.5

0.2

0.2

X

12-9*** 1 .2

A2 t = 1 .1

A3 t = 2 .8*

A4 t = 0.3

Significance levels are indicated as follows : * = < 0 .05, ** = < 0 .01, *** = < 0 .001 ; where no asterisk appears, the t-value is not significant . The degrees of freedom (df) were derived as indicated in Table I .

(E- and C-), a division of labour between the sexes emerged, where the males engaged primarily in outside-the-nest-bowl activities and the females tended to handle material while inside the nest bowls. This division of labour did not emerge in those pairs who already had nests (F) . (c) The state of the nest affected not only the division of labour, but also the amount of manipulation of material .

Comparison of the Various Measures of Nesting Activity This section is in part a review, and in part a guide for those interested in an at-a-glance assessment of the intensity of building in a pair of birds . It is argued that the state of the nest should dictate the choice of the most suitable measure.

880

ANIMAL BEHAVIOUR, 23, 4

Stimuli coming from the nest have been shown to have a pronounced effect on the amount of material birds removed from dispensers, on the amount placed into nest bowls, and on the efficient use of the material removed . These measures gave different results depending on the condition of the nest, in that (a) birds with no nests (E-group) removed large amounts from the dispensers (Fig . 1), (b) birds with growing nests (C-group) placed more into their nest bowls (Fig . 3), and (c) birds with full nests (F-group) placed more of the material they removed from dispensers into their nest bowls (Fig . 4) . Thus, any assessment of the nesting activity of a pair of birds based on counts of nesting material should also take into account the state of their nest. If a pair of birds are `poor' builders, or are not building inside the bowl provided, attention must be paid to the amount of nesting material found around the cage. If a pair has achieved a nest early in the cycle or if a nest is already available to them, the amount of material added to the nest should be noted. While the measures above can be used as indicators of the active phase of nest-building, the behaviour of the pair can also be used . Descriptions in the literature of the characteristic nesting pattern in Columbids state that the male does the collecting and carrying of nesting material, while the female fashions it into the nest (e .g. Johnston 1963) . This means that during the active phase, the females will be found in the nest bowls in the mornings, at least until day 0 . This is true if a pair has to build a nest . However, as shown in this study, there are three major behavioural effects of having a full nest from the outset : (1) the general level of building is very low, (2) there is no apparent division of labour between the sexes, and (3) the nest bowl is often unoccupied (see also White 1975a) ; if there is an animal inside, it is equally likely to be the male as the female which makes behavioural assessment difficult for this group . Thus, as shown for the nesting material data, attention must be paid to the condition of the nest when attempting to assess a pair's readiness to engage in nest-building activities . There are other measures which can be used, but they are more derivative than the ones presented here . For example, bout length, bout number, and the percentage of total observation time spent manipulating nesting material were all evaluated, and found to be undesirable . First, it is difficult to define a bout, particularly for the females, who `interrupt' their handling

activities with wing-flipping and turning, etc. Secondly, there is a difficulty in differentiating between bouts consisting of qualitatively different kinds of behaviour . And finally, any measure involving time did not give an adequate picture of the Full group, which spent very little time handling nesting material. (For further details, see Miller 1965 .) It has already been indicated (Methods section) that certain problems may arise regarding the relationship between various measures . Whereas the behavioural data represent a sampling of activity for a 30-min period in the morning, the nesting material counts are the result of activity over a 24-hr period . If one examines the figures in the text for those groups having to build nests (E and C), it will be seen that there is a 1-day discrepancy between the behavioural and the nesting material measures . (A sustained rise occurs in sex typical activities between days - 5 and - 4, with peaks either on days - 2 or - 1 . The analogous events for the nesting material data occur between days - 4 and - 2, and the peaks are either on day - I or 0 .) The same lag is also seen in the Fgroup, although all counts are very low and the behaviour is rather variable . It should be clear though, from viewing the data with the 1-day latency in mind, that behavioural measures and measures based on material counts are consistent in that all groups show a sustained rise in activity about 4 days prior to the appearance of the first egg. Discussion The Relationship Between the Male and Female This study provides evidence that the condition of the nest influences the building behaviour of a pair of birds, and this influence is exerted very early in the cycle . Those groups that were presented with empty nest bowls from the outset (E and C), removed more nesting material from dispensers than did those with full bowls from the outset (see Fig. 1) . From all observations, the male was primarily responsible for this removal. However, actual building (placing of twigs into the nest bowl ; see Figs 3 and 4) did not occur until the females became involved (Figs 7 and 8) . Although the female is not overtly involved with the nest early in the cycle, it has been demonstrated that ovarian development is affected by stimuli coming from the male within 48 hr of exposure (Barfield 1971), and this effect is enhanced by the presence of a nest bowl



WHITE : ROLE OF THE NEST . II : PRE-LAYING BUILDING

and nesting material (Lehrman, Brody & Wortis 1961). Thus, as Warren & Hinde (1961) suggested for the canary, part of what stimulates the female may be the male's behaviour toward the nest . (See also Keith 1938 ; Johnston 1963 ; Slater 1967, 1970a, b) . It is also of interest that the behaviour of the male toward nesting material was more varied than that of the female early in the cycle (cf . Figs 5 to 8 for early differences between the male and female in those groups having to build nests). While it seems that the early stimulation comes from the male, a previous paper (White 1975a) has indicated that the female influences the male to build . Indeed, there is now experimental evidence that this is so : Martinez-Vargas & Erickson (1973) showed that males handled more nesting material when paired with hormonally treated females (oestrogen and progesterone), who were in their nest bowls soliciting for nesting material, than when paired with sesame-oil treated females who showed no interest in the nest . (See also Slater 1970b.) This would also be in line with Warren & Hinde's (1961) finding for the canary, that the male is influential up to the time of nest-building . Once the female is stimulated, the level of building of the pair is dictated by her in response to the condition of the nest . The division of labour, which is so characteristic of columbids, can be viewed as the result of adjustive responses of the male and female toward one another and toward the state of the nest . (See White 1975a) . The decline in building activity, usually noted when the egg is laid, can also be related to the state of the nest : the C- and F-groups both showed declines in removal and use of nest material, whereas the E-group did not . Further, functional nest-building can be demonstrated well into the incubation period in all birds, but at high levels in those that have not achieved nests (White 1975b) . The Relations Between Nest-Building and Egglaying Since females lay eggs, and eggs usually are laid in a nest, it is not surprising that the primary responsibility for the initiation of building falls on the female . There is no other way to understand the close relationship between nestbuilding and egg-laying (4 to 5 days in doves ; 5 to 6 days in Bengalese finches, Slater 1970a ; 7 to 8 days in canaries, White & Hinde 1968) . Even inexperienced doves show this time

88 1

relationship. (They do however, differ from experienced doves in the latency to start building and, concomitantly, lay their eggs later and show more variation around the mean laying date ; unpublished pilot study .) What is it about the presence of a nest or nesting material that influences reproductive development? If it were merely the sight of the material in the nest bowl, then one would expect that the F-group in this study should have laid their eggs earlier than the other two groups . In fact, they laid slightly later (average laying date for the E-group : 8 .19 days, for the C-group : 8 . 38 days, for the F-group : 8 . 65 days ; the differences are not significant) . It may be that tactual stimuli coming from the nest influence ovulation, as in the canary (Hinde, Bell & Steel 1963) . Unlike the canary, the ring dove does not have a brood patch and attempts to show changes in tactile sensitivity using an aesthesiometer have not been fruitful (Beer, unpublished) . However, in observing the birds, one cannot fail to note an occasional animal rubbing itself into nesting material, either on the ground or in the bowl, so that tactual stimuli cannot be ruled out entirely . The problem has always been one of trying to separate the effects of tactual stimulation from those of participation in nest-building . Participation in nest-building may be a factor involved in normal ovulation . Hinde & Warren (1959) noted long delays to egg-laying in canaries deprived of nesting material and nest cups, as did Slater (1969) in Bengalese finches and Lehrman, Brody & Wortis (1961) in ring doves . White & Hinde (1968) noted that of many measures considered for the canary, nestbuilding bore the most constant relation to egglaying through the breeding season . As noted above, those pairs that were always building in empty bowls, tended to lay their eggs earlier than those building in normally progressing nests or in full nests . This same tendency is seen in Hinde & Warren's data (1959, Fig . 1, p . 39) where females were continuously with a mate and had ad-lib access to nesting material, but had their nest bowls emptied three times a day . Further, there are numerous reports in the dove literature of birds taking over abandoned nests ; when they do, new material is always added (e.g . Harris, Morse & Longley 1963, Zenaidura macroura; Johnston 1960, Scardafella inca) . In other words, some participation always seems to be involved .

882

ANIMAL BEHAVIOUR, 23, 4

The presence of a nest is important for the ultimate success of the cycle (production of young). The importance of the nest is shown by its being the focal point of so large a part of the entire cycle . Not all of the cycle is spent in nest-building, although it will be shown (White 1975b) that functional nest building is an ongoing activity. The initiation of building is determined by the physiological condition of the female at a definite time before egg-laying, the time depending on the species . It seems clear that some participation in nest-building is important in facilitating egg-laying . However, it is not possible to distinguish whether the primary source of stimulation is passive (tactual) or active (participatory). The intensity of building activity is dictated by the condition of the nest at all times. An important implication of this study is that the `characteristic' roles of the male and female during the pre-laying period are not independent of external conditions, and must be viewed as the result of interactions between a varying physiological state and the external environment . REFERENCES Barfield, R. J . (1971). Gonadotrophic hormone secretion in the female ring dove in response to visual and auditory stimulation by the male . J. Endocrinol., 49,305-310. Brownlee, K. A . (1960) . Statistical Theory and Methodology in Engineering . New York . John Wiley and Sons, Inc . Harris, S . W., Morse, M . A. & Longley, W . H . (1963) . Nesting and Production of the Mourning dove in Minnesota. Am . Midi. Nat., 69,150-172. Hinde, R. A . (1958) . The nest-building behaviour of domesticated canaries . Proc. zool. Soc. Lond., 131, 1-48. Hinde, R. A ., Bell, R . Q. & Steel, E . (1963) . Changes in sensitivity of the canary brood patch during the natural breeding season . Anim . Behav., 11, 553-560 . Hinde, R. A. & Warren, R . P . (1959) . The effect of nest building on later reproductive behaviour in domesticated canaries . Anim. Behav ., 7, 35-41 .

Johnston, R . F. (1960) . Behaviour of the Inca dove . Condor, 62, 7-24. Johnston, R. F. (1963) . Stimuli for ovulation in the Rock dove (C. livia) . Condor, 65, 68-69. Keith, O . B . (1938) . Observations on the purple sandpiper in North Eastland . Proc . zool. Soc. Lond., (Ser . A), 108, 185-194. Lehrman, D . S ., Brody, P. N . & Wortis, R. P. (1961) . The presence of the male and of nesting material as stimuli for the development of incubation behavior and for gonadotropin secretion in the ring dove. Endocrinology, 68, 507-516 . Marshall, A . J. & Disney, H . J . de S . (1957) . Experimental induction of the breeding season in a Xerophilous bird . Nature, Lond., 180, 647-649 . Martinez-Vargas, C. & Erickson, C. J. (1973) . Some social and hormonal determinants of nestbuilding behaviour in the ring dove . Behaviour 45, 12-37. Miller, S . J . (1965) . Nest-building activity in the ring dove . Unpublished Ph .D . Thesis, Rutgers Unversity, 123 pp . Slater, P. J. B . (1967) . External stimuli and readiness to incubate in the Bengalese finch . Anim. Behav ., 15, 520-526. Slater, P. J . B . (1969) . The stimulus to egg-laying in the Bengalese finch . J. Zool., Lond ., 158, 427-440 . Slater, P . J . B. (1970a). Nest-building in the Bengalese finch. I . External factors affecting it and its relation to other behaviour early in the breeding cycle. Behaviour, 36, 300-319 . Slater, P . J . B . (1970b). Nest-building in the Bengalese finch. II. The influence of hormonal and experimental factors in the male. Behaviour, 37,24-39 . Warren, R. P . & Hinde, R. A . (1961). Roles of the male and the nest cup in controlling the reproduction of female canaries . Anim . Behav., 9, 64-67. White, S . J. (1975a). Effects of stimuli emanating from the nest on the reproductive cycle in the ring dove. I . Pre-laying behaviour. Anim. Behav., 23,854-868 . White, S . J. (1975b). Effects of stimuli emanating from the nest on the reproductive cycle in the ring dove. III : Building in the post-laying period and effects on the success of the cycle. Anim. Behav., 23, 883-888 . White, S. J . & Hinde, R . A . (1968) . Temporal relations of brood patch development, nest-building and egg-laying in domesticated canaries . J. Zool., Lond., 155, 145-155. (Received 14 August 1972 ; revised 25 March 1973 ; second revision 23 September 1974 ; MS. number : A1368)