Female mate preferences and male attributes in mallard ducks Anas platyrhynchos

Anita. Behav., 1989, 38, 1-7

Female mate preferences and male attributes in mallard ducks

Arias platyrhynchos KERSTIN HOLMBERG*, LENNART EDSMAN* & THORSTEN KLINTt

*Department of Zoology, Division of Ethology, University of Stockholm, S-106 91 Stockholm, Sweden tDepartment of CNS Research, Pharmacia Leo Pharmaceuticals AB, Box 839, S-201 80 Malta6, Sweden

Abstract. Courtship behaviour of mallard ducks breeding in a large pond was studied for 3 successive years. Five male attributes (body weight, sternum length, age, plumage status and social display activity) were measured. In addition, variation in male body condition was induced ez~perimentally by providing males with either an unlimited or a restricted food supply for 5 weeks before observing courtship behaviour. A covariance analysis suggests that variation in all measured characters except body weight significantly affected female mate choice, accounting for 57 % of the variance in the number of females to court each male. Females exclusively courted males in the group fed ad tibitum and among them preferred individuals with a high social display activity, a high plumage status, a small body size and of intermediate age.

Several criteria can be used to predict whether specific male characteristics influence female mate choice (Searcy 1982). First, males must vary with respect to these characteristics. Second, the characteristics (or some correlated trait) must be assessable by females prior to mating. And finally, the characteristics must influence female fitness. These criteria have been used as a basis for understanding mate preferences in red-winged blackbirds, Agelaius phoeniceus (Searcy 1979), and in a number of other species (see e.g. Andersson 1982; Bateson 1983). The mallard has a mating system in which the initial mate choice takes place in a communal display group. But, in contrast to many polygamous species where display groups also occur, mallards finally establish monogamous seasonal pairbonds. After moulting and migration in the autumn, mallards gather in flocks for courtship activities. Most pairs are established at the end of October (Bezzel 1959; Lebret 1961) and the pairbond persists until the next breeding season, 6 months later. Klint (1978, 1980) pointed out that pair formation in the mallard, can, in principle, be determined by either the male or the female, and suggested that male plumage coloration is one important characteristic that females use in choosing their mates. In experiments with wild and domestic mallards, Bossema & Kruijt (1982) and Kruijt et al. (1982) found that 'female-directed male activity' was most 0003-3472/89/070001 +07 $03.00/0

important in attracting females. In a review of mate choice in mallards, Williams (1983) proposed that females pay attention to the cues that signify the males' interest in them, and further emphasized that there is insufficient evidence to conclude that females pay attention to male social display activity. Several factors probably interact to influence female mate choice in the mallard. Thus, to investigate these, we simultaneously studied the influence of five male attributes: (1) body weight; (2) body size; (3) age; (4) plumage status; and (5) male social display activity. In addition, variation in male body condition was induced experimentally by providing males with either an unlimited or a restricted food supply for 5 weeks before observing courtship behaviour. The aims were to determine whether males varied with respect to the attributes and whether the attributes and male body condition influence female mate choice. The experiments were performed in a natural situation where the birds could all interact at the same time and where no artificial feeding was necessary.

M A T E R I A L S AND M E T H O D S The study was carried out at Stockholm University Zoological Research Station Tovetorp (90 km south of Stockholm) in 1982, 1983 and 1984. The experiments were performed during a 10-day

9 1989 The Association for the Study of Animal Behaviour 1

Animal Behaviour, 38, 1 period at the beginning of October, which is the natural time of the year for mallards to gather for courtship behaviour and to form pairs.

TableI. Number ofmallardmalesin the experimental groups for 1982, 1983 and 1984 according to age, group and year

Subjects

Thirty male and 15 female mallards were used in the experiment each year. The males were incubator hatched at the research station, individually marked and reared in groups of normal clutch size, that is, l0 ducklings of mixed sexes in each. Males varied from 6 months to 3'5 years old at the time of the experiments. Individually marked females were reared at the Oster Malma G a m e Management School near Tovetorp. All females in the 1982 and 1983 experiments were 18 months old and all had breeding experience. In 1984 the females varied from 6 months to 3-5 years, and all females more than 18 months old had breeding experience. All 15 females were unknown to the males in each experimental year. Both males and females had their flight feathers cut on one side before the start of the experiment. Procedure

To test the hypothesis that female mate preferences are influenced by male attributes, we measured male body weight (to the nearest 10 g) and body size (sternum length measured to the nearest 0.1 em); we also scored plumage status and observed male courtship display and female sexual behaviour (such as inciting, sexual crouching and copulating). In October, mallard males have completed their moulting and have come into their nuptial plumage. However, some males are more successful than others in reaching a perfect nuptial plumage, that is no premoult feathers are left. To score how successful the experimental males have been in completing their nuptial plumage, the term 'plumage status' was used. Male plumage status was scored for five characters: (1) green head; (2) white neck-ring; (3) brown chest; (4) grey flanks; and (5) tail-curl. Each character was scored on a three-point scale. For characters 1-4, the following scores were used: males with more than five premoult feathers left (1 point); three to five feathers left (2 points); one or two premoult feathers left or moulted completely (3 points). Tail-curl was ranked as follows: a tail with one feather that had just begun to curl or no feather at all (1 point); one round tail feather (2 points); and two round tail feathers (3 points).

Male age (months) Group 1982 UL L 1983 UL L 1984 UL

6 18 30 42 54 Total 5 5

4 4

6 6

5 5

4 3

2 3

10 10

--

15 15 4 -4 --

15 15

2

30

8

Males had either an unlimited food supply (UL; oats and wheat) or a limited food supply (L; 35 g oats and wheat per duck per day) for 5 weeks before the experiment.

Plumage status was expressed as the total score for the five characters. In 1982 experimental males were divided randomly into two groups. For 5 weeks before the start of the experiment one group of males (UL) was given an unlimited food supply (oats and wheat) and the other (L) a limited food supply (35 g of oats and wheat per duck per day), which is about the same amount of food as wild birds get per day. The following year (1983) the males were treated in the same way before the start o f the experiment, but they were kept in the inverse situation; males belonging to the U L group in 1982 became males in the L group in 1983, except for the youngest males which had to be new for each experimental year. In 1984, all 30 males were given an unlimited food supply before the experiment. During this 5-week period the two groups of males were kept in separate outdoor pens with no opportunity to graze. It was not possible to record how much the U L birds were eating during this period. The birds were fed once a day and were checked several times daily. All males were weighed every third day to ensure that no drastic weight loss occurred among the L birds and that the U L birds increased in weight. Sometimes males had to be fed separately because of competition from other males. On two occasions in 1983, a male from the L group was fed in a separate cage for 10 days during the 5-week period, to ensure that h e got his food ration. The

Holmberg et al.: Mate preferences in mallard ducks Table IL Male characteristics O(_+SD) according to feeding regime

Feeding regime UL

L

t or t'

Display activity 12.4_+14-7 3.9_+7.8 --3.54* Plumage status 10.9+3.2 11.6_+3.1 0.94 Body size ( c m ) 10.9_+0.3 11-0+0,4 0.74 Body weight (g) 1261.3-+158-8 1050.0_+215.1 -4.77*

P <0.001 >0.05 >0.05 < 0.001

Male display activity (summarizedfrequencyof grunt-whistle,head-up tail-up and down-up), plumage status (an accumulated score of five characters), body size (sternum length) and body weight according to feeding regime (UL: unlimited food supply; L: limited food supply prior to the experiment) pooled for 1982, 1983 and 1984. Student t, N=90. * t' was used when variances were unequal. number of males and the age of males in each experimental group and year are presented in Table I. Male Condition

In waterfowl, total body weight has been widely used as an index of body condition (Folk et al. 1966; Hay 1974); however, a variety of other indices has recently been employed (Harris 1970; Ankney 1979; Bailey 1979; Raveling 1979; Wishart 1979; Krapu 1981; Young & Boag 1982; Whyte & Bolen 1984; Pehrsson 1987). To see whether any male characteristics are correlated with fat storage, here referred to as condition, the following experiment was performed. Ten captive males were placed on a restricted diet (35 g of oats and wheat per duck per day) for 5 weeks so that their fat reserves depleted steadily. Each week during this period, two males were randomly selected and killed. In total, 10 males were weighed, plucked and separately minced twice. Two samples from each male were analysed for fat content which was expressed as a percentage of total carcass weight (Schmid-Bonzynski-Ratzlaff 1974). A regression of the proportion of body fat on body weight (g), body size (sternum length, cm), wing length (cm) and body weight/sternum length index, was performed to evaluate the predictive power of the four variables. The slopes were significant for body weight (b=0"046, r 2=0.74, P<0-01), wing length (b=7.22, r2= 0.57, P<0.05) and body weight/ sternum length index (b = 63-47, r 2= 0-75, P < 0.01) but not body size. Thus, the best measures of male condition in terms of fat storage are body weight

and body weight/sternum length index. No additional predictive power was gained when adjusting body weight for structural size (see also Whyte & Bolan 1984). Heavy males accordingly have a large proportion of stored fat and were here considered to be in good condition. Observations and Behavioural Terminology

At the beginning of October each year, all individuals were released into a 2.5-ha test pond. Observations continued for 10 days (8 h/day) from a tower close to the pond. Female sexual behaviour patterns such as inciting (a thrusting head movement backward over the shoulder), sexual crouching and copulating were recorded and taken as indicating preference for a certain male (see Johnsgard 1965). The frequency of male social displays such as grunt-whistle, head-up-tail-up and downup (Lorenz 1941) were recorded and expressed as a combined score of total social display activity. Male body weight and plumage status were measured three times during the experiment.

RESULTS Variations in Male Characteristics

After 5 weeks of different food availability, males from the UL group were heavier than those from the L group (Table II). Male body weight in the UL group (X= 1261 g) averaged 100 g higher, and for the L group (X= 1050 g) 100 g lower, than that of wild mallards (X= 1167 g) in October (Folk et al. 1966). Plumage status and body size did not differ

Animal Behaviour, 38, 1 Table Ill. Male characteristics (.~__+so) according to age Male age (months) 6 Display activity 1.4_ 3.3 Plumage status 9.4+2.9 Body size ( c m ) 10.8_+0-3 Body weight (g) 1056.7+158.2

18

>30

18.4__+18.7 10.3 ___10.0 12-1__+3.0 12.0+3.0 10.8• 11.2_+0.3 1220.4• 1284.9_+200.8

F* 14.2 7.9 10.9 13.3

Male display activity (summarized frequency of grunt-whistle, head-uptail-up and down-up), plumage status (an accumulated score of five characters), body size (sternum length) and body weight according to age pooled for 1982, 1983 and 1984. (ANOVA, N=90; df=2,87 in all cases). *All significant at P~<0.001. between the UL and L groups (Table II). However, plumage status and body weight differed between the youngest (6 months of age) and older males (Table III). Furthermore, older males (>_30 months of age) were larger (judged by sternum length) than younger males (Table III). F o r individual males in successive years there is no increase in sternum length between the second and third year (personal observation). Thus the small difference in body size (4 mm) between age classes is probably an experimental artefact of no biological relevance. All comparisons refer to the day of release in the test pond, except for male display activity which was measured during the experiment. Males from the UL group had significantly higher display activity than males from the L group Table II), Of the three male age classes, males 18 months of age had the highest display activity (Table III). In all analyses, the data were pooled for the three experimental years ( N = 90). Correlates of Female Preference

To determine which of the five male variables had the most important effect on mate preference by females, an analysis of covariance (Nie et al. 1975) was carried out (Table IV). Each F-value in Table IV represents the additional contribution to the explained variation after adjusting for all factors and covariates. This means that the effect in Table IV of, for example, age on female mate preference is the effect that remains when the effect of age mediated through display, plumage, size and weight has been removed. There was no difference in the number of females inciting males between the experimental years

(Table IV). However, the number of females inciting males differed between the two groups of males on different feeding regimes (Table IV). In fact, females incited males only from the UL group. Males 18 months of age from the UL group were incited by more females than males from the other age classes (Table IV). These males also had the highest social display activity. Among the four male attributes (social display activity, plumage status, body size and body weight) in which males varied, it appears that females paid attention to three of them. Males with a high display activity were more likely to be incited by females (Table IV). Males with high plumage status were also preferred by females (Table IV). In addition, small males were preferred by females, the effect being just on the border of significance (Table IV). Females paid no attention to male body weight (Table IV). These male attributes accounted for 57.3% of the variance in female mate preferences, Out of the 57.3%, 36"0% is explained by male display activity. The results suggest that the male attributes analysed in this study interact to have a combined effect on female mate preferences, although male social display activity had the most significant effect on female preference. All females in 1982 and 1983 were 18 months of age and preferred to mate with males of the same age. These males, 18 months of age, were the ones with the highest display activity. A question arises from the results. Were females attracted by the display activity among these males or were they selecting mates from their own age class? In the 1984 experiment, both males and females were of different ages. The aim was to see whether

Holmberg et al.: Mate preferences in mallard ducks Table IV. Female mate preferences in relation to male characteristics Source of variation in males Main effects Factors Feeding regime Unlimited Limited Age class 6 months 18 months > 30 months Year -Covariates Display activity b = 0.069 Plumage status b=0.213 Body size b = -- 1.107 Body weight b = --0-001 Interactions Explained Residual Total

Mean no. females inciting per male

1-68 0.00 0.03 2.84 0-83

df

Mean square

F

P

1

15.78

7-11

<0.01

2

6.97

3.14

<0.05

2

2.66

1.20

> 0.05

1 1 1 1 7 16 73 89

46.12 23-59 8.70 0.79 4.35 18.08 2.22 5.08

20.77 10.63 3.92 0.36 1-96 8-13

< 0.001 <0.01 0.05 >0-05 > 0.05 < 0.001

Multiple r 2= 0.573 (coefficient of determination). Variation in female preferences (measured in number of females inciting a particular male in relation to feeding regime prior to the experiment, age class, year, male display activity, plumage status, body size and body weight of males) pooled for 1982, 1983 and 1984. Each effect is the additional contribution to the explained variation after adjusting for all factors and covariates (N=90, analysis of covariance, Nie et al. 1975; b = regression coefficient).

females preferred to mate with males from their own age class or from other age classes. N o females 6 months of age incited any of the males, and no males in the 6-months age class were incited by any females. O f the l 0 females older than 6 months (five 18 months and five 30 months), nine incited males from the 18-months age class (sign-test, P < 0-05). F o u r of the five 18-month-old females incited males from their own age class. All five older females also incited 18-month-old males, instead of males of their own age (Fisher exact test, P < 0.05). This result suggests that females do not select mates of their own age. Males 18 months old were probably more successful due to their higher display activity. DISCUSSION Ashcroft (1976) suggested that one function of the pairbond in eider, Somateria mollissima, is for the male to protect the female from disturbance by other birds prior to and during the egg-laying period. Furthermore, this protection from disturbance allows the female to feed more quickly, which probably gives her extra reserves required for breeding, and in addition ensures that the

resulting offspring are his. Ashcroft also found that the feeding rate o f males close to their mates is significantly lower than that far from their mates. She suggested that this is not a direct result o f interactions with other birds, but is a consequence of the male being continually alert for intruders and spending time keeping close to the female. Thus, females during pair formation should prefer those mate characteristics that reflect high mate-guarding ability prior to and during the egglaying period. Several male characteristics, investigated in the present study, may be important in this respect. Females in this study exclusively incited males fed ad libitum, but they paid no attention to the body weight of individual males; their preferences were limited to the feeding regime. Since body weight is a good predictor of male condition in terms of fat storage, we had expected it to influence female mate choice. There are two plausible explanations to why it did not. O f the measured male characteristics, body weight is the most difficult one to assess, at least visually. It is therefore a less likely cue to be used in mate selection. It is also possible that a male's ability to feed is of greater importance

6

Animal Behaviour, 38, 1

to the female than stored fat per se. Male feeding ability may indirectly affect female fitness, since males with high feeding rates probably survive better from the time of pair formation in the autumn to the breeding season 6 months later, and since females could benefit from their more active mate guarding (Goodwin 1956; review in McKinney 1969; Barash 1977; Goodburn 1984). Males fed ad libitum and on a restricted diet did not differ in plumage status, but, irrespective of feeding regime, older males had higher plumage status than the youngest males. One possible explanation could be that, in ducks, yearlings have to moult three times in the course of their first 3 months (Weller 1976) and at the same time use energy for growth. Male social display activity such as grunt-whistle, head-up-tail-up and down-up were performed significantlymore often by the males fed ad libitum and among them most actively by the males of t8 months of age. Furthermore, these males were significantly the most successful in attracting females, in terms of number of females inciting them. It is unlikely that these results are due to females selecting mates of their own age. Canvasbacks, Aythya valisineria, prefer to mate with individuals of their own age (Bluhm 1985). In our study, however, females aged both 18 and 30 or more months preferred to incite the 18-month-old males. Several male attributes probably interact to influence female mate choice. The characteristics in this study, except for age, varied between individual males. The measured male attributes (both factors and covariates) accounted for the major part (57%) of the variation in female mate choice. Among the male characteristics, male display activity was, without exception, of greatest importance and accounted for 36% of the 57% in female mate preference. However, to a certain degree both plumage status and body size affected female mate choice. In particular, females preferred small males, as Petrie (1983) found in moorhens, Gall# nula chloropus. Kruijt et al. (1982) found that female-directed male activity such as approaching, following and staying near were more important for pair formation than was male plumage. Our data do not contradict this but rather emphasize that male social display activity has the most influence on female mate preference. The social display activity by the males is certainly one important aspect of a female-directed male activity particularly during the initial pair formation.

Further investigations must elucidate how females can distinguish between males from the restricted and unlimited feeding regimes. One possibility is that well-fed males in the autumm probably have more time and energy for activities other than feeding, such as social displays. In addition, our measure of display activity (frequency) does not take into account any qualitative properties of the display. Female mate preferences could be affected by how, and from what position a display is performed by a male and the order in which males perform different displays. These details of display behaviour might reflect a male's age and prior feeding conditions and could thus be a possible way for females to assess male age and feeding ability. The present study indicates that mallard males vary considerably in the attributes measured; three of these attributes can be assessed by females (social display activity, plumage status and body size), and are correlated to female inciting behaviour and influence their mate preference. We do not yet know whether male attributes themselves influence female fitness. However, prior food intake proximately controls the male's hormone level, which in turn influences male behaviour such as social display activity (Klint et al., in press) and thereby his chances of being selected. Further, wellfed males might be better prepared for mate guarding prior to and during the egg-laying period and might thereby increase their mate's fitness.

ACKNOWLEDGMENTS We express our gratitude to Dr A. Arak, L. Chapman, Dr O. Gr6nwall and Dr A. Peterson for carefully reading drafts of this manuscript and P. Widenstr6m for typing it. We thank N. Andbjer and C. J. Sandberg for assistance at the Tovetorp Zoological Research Station, Oster Malma Game Management School for lending the female mallards and A. Holmlund at the Swedish University of Agriculture in Uppsala for analysing the fat content in the birds. This work was supported by the Swedish Natural Research Council.

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(Received 15 April 1987; revised 26 April 1988; MS. number: 3005)