Badge size in the house sparrow Passer domesticus
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1 Behav Ecol Sociobiol (1988) 22: Behavioral Ecology and Sociobiology 9 Springer-Verlag 1988 Badge size in the house sparrow Passer domesticus Effects of intra- and intersexual selection Anders Pape Moiler Department of Zoology, Uppsala University, Box 561, S Uppsala, Sweden Received October 1, 1987 / Accepted January 18, 1988 Summary. I studied female mate choice in house sparrows Passer domesticus in relation to the size of the black throat patch of males (badge size), which is a signal of dominance status, and to territory quality. Males with large badges obtained a mate earlier in spring than males with small badges. Males which remained unmated during the entire breeding season had smaller badges than mated males, even when controlling for the effect of other morphological traits and age. Largebadged males had territories with more breeding sites than small-badged males. Territories defended by males with large badges primarily had hole nest sites, which were safe from predators, and nestlings rarely fell from hole nests. Females were implanted with estradiol to induce copulation solicitation displays. Females responded more strongly to a male taxidermic mount and song than to song alone, and they responded more strongly and frequently to male mounts with large badges. Female house sparrows chose mates on the basis of male badges and perhaps on the basis of the quality of the nesting territories offered. Introduction The adaptive significance of intraspecific variation in plumage characters has received much attention in recent years, and a large number of hypotheses have been advanced to explain the variation (Lack 1954; Selander 1965; Rohwer 1975; Shields 1977; Rohwer etal. 1980; Procter-Gray and Holmes 1981; Flood 1984; Fugle et al. 1984; J/irvi and Bakken 1984; Studd and Robertson 1985; Watt 1985; Lyon and Montgomerie 1986). Plumage variation within age and sex classes can have a functional importance during the reproductive and/or non-reproductive seasons. If males with marked expression of a character benefit in dominance relationships by having relatively free access to resources (e.g. in a status signalling system, Rohwer 1975), females may use this character during mate choice, if offspring to some extent inherit the expression of the character. Alternatively, males having a particular dominance status during the non-breeding season may maintain this status during the breeding season. Dominant males may establish territories earlier in spring than other males because of differential access to food; early territory establishment will give males first choice of high quality territories and hence improve their probability of acquiring a mate of superior quality. House sparrow, Passer domesticus, males have black throat patches of variable size. These serve as badges and are signals of dominance rank during winter, even when controlling for the effects of body size and age (Moller 1987 a); between-year variation in badge size of individuals is negligible. Badges are used to signal status during flock feeding, and cheating is socially controlled by frequent testing of the true dominance status of flock members (Moller 1987a, 1987b). Badge size is positively correlated with testes size during the breeding season (Moller 1988). Sperm competition relatively frequently occurs in the house sparrow, and dominant males participate in communal sexual chases of females more often than other males (Moller 1987c). They also follow their female mates more often than other males, and dominant male sparrows therefore are more efficient in terms of defending their certainty of paternity (Moller 1987c). Individual chickens with large testes produce ejaculates with more sperm than do individuals with small testes (e.g. Burrows and Titus 1939; Parker et al. 1940), and, in case of sperm competi-
2 374 tion, the probability of fertilization is proportional to the relative number of sperm provided simultaneously by each male (Martin et al. 1974; Martin and Dzuik 1977), although these patterns have not been demonstrated in any passerine species. For these reasons dominant male house sparrows with large badges may be more certain of their paternity than other males. Males with large badges also provide more paternal care than other males (A.P. Moller unpublished data). Males react differentially to simulated territorial intrusions by male dummies in relation to their badge sizes; male mounts with large badges are approached more cautiously than small-badge mounts (Moller 1987a). Thus, dominance may also be related to badge size during the breeding season (Lyon and Montgomerie 1986). This study was designed to answer the question of whether female house sparrows use male badge size and territory quality when choosing a mate. Methods Field procedures I studied house sparrows at Hollensted (57~ 10~ Denmark, in by catching and colour-ringing more than 95 % of the individuals present. I censused territorial house sparrows during March-May 1984 and 1985 in a larger study area around Hollensted by slowly passing all buildings in the morning from half an hour after sunrise and during the next 2 h. Males sing from their small breeding territories using either a bachelor song (before mating) or a mated male song (after mating) (Hansen 1974). The bachelor song is markedly louder and is delivered at a higher rate than the mated male song (Hansen 1974). These two song types can easily be separated by ear, and I was thus able to determine the mating status of ati males (77 in 1984 and 78 in 1985). Male badge size was scored from a distance of less than 10 m on a five-grade scale with the following subdivisions: 1 : badge size below 200 mm z, 2: mm 2, 3: mm 2, 4: mm 2, and 5: above 500 mm 2 (see Moller 1987a, Fig. 1). Males were compared with a drawing of the five-grade scale in the field. Badges of a total of 16 males were scored at a distance, and badge sizes were measured after capture during Badge scores at a distance and from data on badge size (see below) were the same in 15 of 16 cases. The incorrectly classified case concerned a male with a badge of 299 mm 2, i.e. very close to the division between two classes. Territory boundaries were determined from interactions with neighbouring males and from song posts. Male territory quality was scored in 1984 using the following criteria; (1) number of nest sites (nest holes, or crevices between the roof and beams in which nests could be placed) within the territory, and (2) nest sites were scored as either holes, if placed below a roof or within a wall, or open sites if a nest could only be placed in fuu view. I recorded mating status of colour-ringed males by the criteria listed above. Age of males was determined from birds ringed as nestlings, from plumage characters, or from skull ossification in autumn (Svensson 1984). Badge size of males was estimated from maximum length and breadth of badges when holding the bill perpendicular to the body. The area of the badge was estimated from the regression equation. Badge size (mm2)= Length (ram) x Breadth (ram) (see Moiler 1987a). Experimental procedures Female house sparrows were caught at Janum (50~ 09~ and Pandrup (57~ 09~ Denmark, on February, They were kept in a room 3 m x 3 m x 5 m, 45 m 3, sufficient for the housing of 33 individuals (Innis et al. 1985), assuming a minimum individual distance of ca. 25 cm (Cink 1977). The light-dark cycle was changed to 16:8 which is similar to that of the breeding season. Bushes were provided as perches, water was given in a large dish, and food was provided ad libitum in another dish (a mixture of cracked corn, millet, wheat, barley, oats, and sunflower seeds). I measured wing length, bill length, bill depth, tarsus length, and body weight on 16 March All females received a 17-fl-estradiol (Sigma) hormone implant subcutaneously on this date by cutting a small hole in the skin below the right wing. The implant consisted of 16 mm Silastic tubing 1.96 mm outside diameter and 1.47 mm inside diameter. Each tube held 12 mm of hormone and was sealed by Silastic adhesive (Dow Coming). The skin was sewn with two stitches in order to prevent the implant from being expelled. See Searcy and Marler (1981) and Baker et al. (1981) for a fuller description of the method. Experiments were performed on 30 March 1986, between 0630 and 1030 hours. Females were assigned randomly to one of four groups, three groups of 9 individuals to be presented with a male mount each with a different badge size and song, and one group of 6 individuals to be presented with song only. The order of testing in experiments was random. The same 10 females, assigned to a group to be presented to a male mount and song, were in three consecutive experiments presented to all three mounts in random succession. Each female was put into a cage (30 cm x 40 cm x 60 cm) holding two perches and covered with a cloth. After a 2-rain pause I removed the cloth on one side of the cage thus exposing the female to the male mount (in three of the groups; no mount was displayed to the fourth group) at a distance of 30 cm with the badge directed towards the cage. The cloth was removed by pulling a string from behind a light screen, and the female was only able to see the mount and the screen. After a 30-s pause I played a courtship song used during sexual displays (see Hansen 1974) at a sound level similar to that of natural songs for 2 rain. The song had been recorded by P. Hansen in Mid-Jutland in April Female solicitation displays were scored using five measures: (i) latency (in s) until first display, (ii) number of displays measured as bouts separated by 5 s, (iii) time spent displaying during the 2-rain period (in s), (iv) display frequency calculated as number of display bouts divided by time displaying, and (v) display intensity scored as (a) lowering of head, (b) lowering of body, (c) drooping of wings, (d) quivering of wings, (e) raising of tail, and (f) copulation call rate, each on a scale from 0 (no response) to 2 (very intense response as in some copulations during the breeding season). The display intensity score thus ranged from 0 to 18. The female was finally weighed. I used three taxidermic mounts for experiments, all of which had the same posture with fluffed body feathers, slightly drooped wings, and slightly raised tail and head. The male mounts, which were all of birds taken in spring, had similar measurements; 81 mm wing length, I mm bill length, mm bill depth, mm tarsus length, and mm tail length. Badge size was 170, 408, and 646 mm z, respectively.
3 375 Statistical procedures I used non-parametric and parametric statistics in accordance with Sokal and Rohlf (1981) and Siegel (1956). All tests are two-tailed. Values given are mean SD unless otherwise stated. Results Badge size and mating success The earliest male house sparrows started to sing within their territories during March. Such early males had larger badges than later ones. Badge score was negatively correlated with territory establishment both for males that later got mated and for males that remained unmated during the entire breeding season (mated males: 1984: rs = , ts7=7.83, P<0.001, 1985: rs=-0.83, tsv= 11.23, P<0.001; unmated males: 1984: rs =- 0.76, t16=4.68, P<0.001, 1985: rs=-0.63, t17= 3.34, P < 0.01). Mean badge score decreased during spring for both mated and unmated males (Fig. 1). Badge size of mated and unmated males differed also when controlled for the effect of male age. Yearling mated males had larger badges than yearling unmated males (yearling mated: 387 _+ 176 mm 2 (N= 26), yearling unmated: mm 2 (N=37), Mann-Whitney U-test, z=2.47, P=0.014). Older mated males also had larger badges than older unmated males (older mated: mm 2 (N=14), older unmated: nq_ltl 2 (N=6), Mann-Whitney U-test, U= 1, P<0.001). These results were not altered by entering other morphological traits (body weight, tarsus length, wing length, bill length, bill height) as independent variables in partial regression analyses (A.P. Moller unpublished data). Badge size and territory quality House sparrow territories must include nest sites but not necessarily other resources (Summers- Smith 1963). Males with badge scores of 1-3 more often had only a single nest site within their territory (82%, N= 39) than males with badge scores 4-5 (42%, N=38, G~Z= 13.58, P<0.001). Predation on house sparrow nests was rare and not recorded during this study. Nestlings sometimes fall from nests and die on the ground; this happened in 6 of the 19 open nests but in none of the 58 hole nests (binomial test, P=0.0003). On three of these occasions I found the nestling still alive on the ground, so these casualties are not due to parent birds throwing out already dead nestlings. Falls from the nest may go unnoticed because large nestlings can move away and because W I W O MARCH I [ I I I I 1985 i i i i i i APRIL MAY Fig. 1. Badge score of mated OCilledsymbols) and unmated (open symbols) male house sparrows during spring 1984 and Mean + SE (vertical bars) predators quickly remove nestlings on the ground. My observations thus underestimate the frequency of nest falls. Males with badge scores 1-3 had hole nest sites less often (54%, N= 39) than males with larger badges (97%, N= 38, G~ = 22.95, P < 0.001). Copulation solicitation displays Female house sparrows were treated with estradiol in order to record copulation solicitation displays as a response to male taxidermic mounts with different badge sizes. Hormone implantations did not seem seriously to trouble the females, and body weights increased from 28.6-t-1.7 g (N=33) to 30.0_+ 1.8 g 2 weeks after implantation (t64 = 4.50, P<0.001). Females in the four experimental groups did not differ significantly in any of the body measurements recorded. Copulation solicitation displays were affected by the presence of the dummy; females took longer before giving a display and their display intensity was lower in response to song alone as compared to simultaneous presentation of song and male mount (Table 1). Copulation solicitation displays did differ significantly between mounts with different badge sizes (Table 2). Two response measures (number of displays, display intensity) changed significantly with badge size in the predicted direction; females
4 376 Table 1. Female copulation solicitation displays in relation to either song or to song and male dummies. Differences were determined using Mann-Whitney U-tests (z-values) Display response Females Females z exposed exposed to song to song and dummy Latency(s) * Number of displays Time in display (s) 5.3 _ Display frequency Display intensity 0.8-t _ * N 6 27 * P<O.05 gave more and stronger displays in response to the model with a large badge as compared to the small- and medium-badged models. A total of 8 females did not respond at all during the experiments, but the results remained the same when these females were excluded. Unresponsive females were distributed fairly evenly across all groups (3 in small-badge group, 2 in medium-badge group, 1 in large-badge group, 2 in control group). Discussion Male house sparrows with large badges apparently had a mating advantage since mated males on average had larger badges than unmated ones. This was so even when controlled for the effects of age and correlations with other body measurements. Large-badged males established territories earlier than small-badged males, but mated males had larger badges than unmated males throughout spring when most mating took place (Fig. 1). Territory quality measured as the availability of nest sites was also related to male badge size. Early establishment of territory may be advantageous if early males can choose among a larger number of territories than later establishing ones. However, male house sparrows fight over territories during establishment (Summers-Smith 1963), and male-male competition for access to territories of superior quality may account for the relationship between badge size and territory quality. It is known that males respond more cautiously to simulated intrusions by male taxidermic mounts with large badges than to intrusions by small-badged mounts (Moller 1987a). Female house sparrows treated with estradiol responded more strongly to a male mount and song than to song alone, and females responded differentially to male mounts with different badge sizes. Females gave more copulation solicitation displays with a stronger intensity in response to large-badged as compared to small-badged mounts. This differential response to male badges could be explained as (1) females choosing mates which will give a genetic advantage to the offspring, (2) females getting better resources (e.g. territory), or (3) females choosing males for their parenting or mate guarding ability (cf. Searcy 1982). In order to demonstrate an effect of territory quality, nest sites will have to be manipulated and subsequent mating success recorded. This is not easily done because most house sparrows build on privately owned houses. Females may either choose male quality per se, benefits offered by the male, e.g. territory quality, or male parenting ability (Searcy 1982). Female choice of territory quality has been demonstrated in several cases (e.g. Alatalo et al. 1986; review in Searcy 1982). Mate choice has less frequently been shown to take place in relation to male quality, and then usually for animals with non-monogamous mating systems (Searcy 1982). Mate choice may, however, also be important for males in monogamous species like the house sparrow because Table 2. Female copulation solicitation display responses in relation to male badge size and song. Overall differences between groups were determined using a Friedman two-way ANOVA 0f~)- Pairwise differences between groups were determined using a Wilcoxon matched-pairs signed-ranks test (T-values) Display response Mount badge size (mm 2) Zr z Pairwise comparisons (1) (2) (3) (1)-(2) (2)-(3) (1)-(3) T T T Latency (s) 79 _ 53 Number of displays Time in display (s) Display frequency Display intensity 2.3_ _ "** 0"** * 0* 0"* 0"** "** 2*** 4* _ "** _ * 0"** 3* 0"** * P<0.05, ** P<0.02, *** P<0.01
5 377 of a surplus of males in the breeding population (in this population 24% (N=42); see also Summers-Smith 1963). The correlation between badge size and dominance rank of males was the only consistent relation between dominance rank and several external male traits (Moller 1987 a). However, the correlation is not a very strong one and females may make a better choice by using cues of both territorial quality and male traits. Male house sparrows actually sing in their few-squaremetre-large territory, and females often visit several territories before making a choice (Summers- Smith 1963; A.P. Moller unpublished data). Intraspecific plumage variation between males has an acoustic parallel in bird songs. Males with large repertoires may be preferred during mate choice (Kroodsma 1977), and females display more intensely to large as compared to small repertoires used as bio-assays (Catchpole et al. 1984; Searcy 1984; Baker et al. 1986, 1987). Acoustic signals, like repertoires, may be under the control of the individual, while this is not always the case for visual signals, the only exception being coverable badges (Hansen and Rohwer 1986). Repertoire size will, in contrast to badge size and other visual traits, not be affected by selection pressures outside the breeding season. The evolutionary outcome of selection may thus differ between acoustic and visual signals, except from cases where the plumage trait becomes so costly to its bearer that a postnuptial moult takes place. Plumage variation in birds within sex and age classes can be attributed to either breeding or nonbreeding factors. If intraspecific variation is maintained during the breeding season after a spring moult, it is likely that the variation owes its existence to some breeding season function. If, on the other hand, it is established during an autumn moult, breeding season plumage variability may be a carry-over from the non-breeding season. Badges of male sparrows are partly covered by light feather tips following the autumn moult, but the black feathers gradually reappear due to wear; species like the house sparrow in this way may show different badges as a result of gradual wear and thus avoid the costs of a spring moult (Moller 1987a). Badges do not change markedly from late spring and onwards during the breeding season. The relative costs and benefits of plumage variation could be assessed by measuring selection coefficients on male badges during different selection episodes (Arnold and Wade 1984). I conclude that male badges have an all-year function in the house sparrow by providing information on the dominance status of the owner (Moller 1987 a, b). Badge size is a relatively reliable predictor of male ability to guard females from sexual chases, and, if such chases occur, from other males during chases (Moller 1987c; A.P. Moller unpublished data). Male badge size is also a good predictor of the extent of paternal care to be expected in terms of feeding of nestlings (A.P. Moller unpublished data). The latter result may be caused by either differential efficiency of males at foraging or by care intensity being related to the certainty of paternity. Female house sparrows may use both male badges and territory quality as cues during their mate choice. Directional sexual selection on badge size thus is probably caused by the positive correlation between male badge size and territory quality and female choice of one or both of these traits. Acknowledgements. I am grateful to E. Flensted-Jensen and W.C. Aarestrup for catching house sparrows and other help. P. Hansen and H. Walhovd provided taxidermic mounts. B. Silverin and W.M. Searcy provided information on hormone implantation. A. Lundberg, W.A. Searcy and S. Ulfstrand commented on an earlier draft of this paper. The study was supported by a grant from the Swedish Natural Science Research Council. References Alatalo RV, Lundberg A, Glynn C (1986) Female pied flycatchers choose territory quality and not male characteristics. Nature 323 : Arnold SJ, Wade MJ (1984) On the measurement of natural and sexual selection. Evolution 38: Baker MC, Spitler-Nabors KJ, Bradley DC (1981) Early experience determines song dialect responsiveness of female sparrows. Science 214:81%821 Baker MC, Bjerke TK, Lampe H, Espmark Y (1986) Sexual response of female great tits to variation in size of males' song repertoires. Am Nat 128: Baker MC, Bjerke TK, Lampe HU, Espmark YO (1987) Sexual response of female yellowhammers to differences in regional song dialects and repertoires. Anim Behav 35: Burrows WH, Titus HW (1939) Some observations on the semen production of the male fowl. Poultry Sci 18:8-10 Catchpole CK, Dittami J. 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