Evidence for active female choice in a polygynous warbler

,1nim . eehaip ., 1992,44, 3 0 1 -311

Evidence for active female choice in a polygynous warbler STAFFAN BENSCH & DENNIS HASSELQUIST Department of Ecology, Animal Ecology, University of Lund, S-223 62 Lund, Sweden (Received 12 April 1991 ; initial acceptance 4 June 1991 ; final acceptance 29 January 1992 ; MS . number: 3757)

Abstract . Thirteen female great reed warblers, Acrocephalus arundinaceus, were captured soon after pair formation and transported 140 km to another breeding site where they were released with radiotransmitters 1-3 days later . Each female was tracked until she paired with a male . All females settled in the area within a few days after first having visited the territories of on average six males . Male great reed warblers sing two different song types : long and short songs . Males use long song when attracting females to their territories and short song when defending fertile females . All of the released females selected males that sang long song, although they visited territories of males singing short song . Following mating, females soon started building a nest, and egg laying commenced after on average 5 days . Four females selected already-mated males despite the conspicuous presence of nesting females and despite having visited alternative unmated males . Among visited males offering the same mating status as the selected male, the released females seemed to prefer early arriving males . These results indicate that polygyny in the great reed warbler arises from active female choice and suggest that a female's search tactic is to visit several males before returning to mate with a male who offers a better than average breeding option . This implies that females are capable of remembering and evaluating the quality of previously visited males or their territories, or both .

Theories about sexual selection (Andersson 1982a ; Hamilton & Zuk 1982) and the evolution of mating systems (Verner 1964 ; Orians 1969 ; Davies 1989 ; Searcy & Yasukawa 1989) rely on the assumption that females actively choose a male . For most animal groups, however, little is known about the behaviour of females choosing among males . Polygynous mating systems that superficially look similar could be the result of fundamentally different choice processes . For instance, polygyny may occur if females prefer males with certain characteristics (Andersson 1982b ; von Schantz et al . 1989) but also if they mate randomly in which case some males may end up with several females simply by chance (Wotton et al . 1986 ; Lightbody & Weatherhead 1988) . In contrast, if females avoid mating with already-mated males, monogamy will be the rule despite the males' interest in becoming polygynous (Davies 1989) . Some mated males may, however, become polygynous by hiding their mating status (Alatalo et al . 1981) . Although it is commonly accepted that female passerines visit more than one male before settling on a territory, as shown for lekking species (Kruijt & de Vos 1988 ; Petrie et al . 1991), this conclusion is 0003 3472/92/070301 + 11 503 .00/0

derived from casual observations (Payne & Payne 1977; Nolan 1978 ; Searcy 1982 ; Part & Gustafsson 1989) . One important exception is the study by Dale et al . (1990) who showed that female pied flycatchers, Ficedula hypoleuca, visit up to nine males before choosing a partner . In the present study, we investigated the movements and behaviour of 13 great reed warbler, Acrocephalus arundinaceus, females which lacked previous experience of both the study area and its territorial males as they were captured at a distant breeding site and released into the study area . Before releasing the females, we attached radiotransmitters to them . The logic of the experiment was to mimic a situation in which naive females arrive on their spring migration to a breeding locality and there choose partners . Thus, this experiment made it possible to study a female's movements and behaviour from her arrival at the study site until she settled in a male's territory . In particular we were interested in answering the following questions: (1) How long do females take to choose a mate? (2) How many males are inspected before females settle on a territory? (3) Do females avoid mating with already-mated males? (4) Could female Q 1992 The

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Animal Behaviour, 44,

behaviour in the great reed warbler be attributed to any of the mate-sampling tactics suggested (Janetos 1980 ; Wittenberger 1983 ; Real 1990)?

METHODS The great reed warbler weighs about 30 g, is a longdistance migrant wintering in tropical Africa and breeds in highly productive marshes . In spring, males arrive at the European breeding grounds approximately 10 days before females . The species is facultatively polygynous (Catchpole et al . 1985 ; Urano 1985 ; Dyrcz 1986), and in our study population about 40% of the territorial males pair with two to four females each (Hasselquist & Bensch 1991) . The male sings two distinctively different song types : long song when trying to attract females and short song when mate guarding a nest-building female in his territory (Catchpole 1983 ; Ezaki 1987 ; Hasselquist & Bensch 1991) . A male sings long song from the day of arrival and if he succeeds in attracting a female he immediately switches to short song . When the female starts egg laying almost all males resume the long song . This pattern can be repeated several times in a season depending on how many females the male attracts to his territory . By using the change in a male's singing behaviour, the time for pair formation can be assessed very precisely (Hasselquist & Bensch 1991) . The experiment was carried out during May and June in 1989 and 1990 at Lake Kvismaren (59°10'N, 15°25'E), South Central Sweden, where we have studied a population of great reed warblers since 1983 (Bensch & Hasselquist 1991 a) . Throughout the study, all males and females have been uniquely colour ringed . From the day the first male arrived, we visited the area daily in order to identify all males, plot their song positions on maps and register their type of song . To investigate mate-choice behaviour of females lacking previous experience of the area, we captured females at another breeding locality, Lake Takern, and transported them to Lake Kvismaren (140 km north) . Each female was held in captivity for 1-3 days, and in the evening prior to release, a 2 .0 g radio-transmitter was glued to the contour feathers of her back . As far as we know the behaviour of a female is not affected by a transmitter . By video-taping incubating females (Bensch & Hasselquist 1991b) we have seen that females with

attached transmitters do not pay the transmitter any attention at all . Also, they eventually produce as many fledglings as unmanipulated females . All females were released from a specific site in the central part of the area (Fig . I) at 0400 hours and then tracked continuously throughout the daylight hours . The trackings were only interrupted for short periods when we changed observer, during unfavourable weather, or if the female remained sedentary for many hours . Out of the 13 released females we failed to track two for a substantial part of their premating period and these are excluded if not otherwise stated . The position and singing behaviour of males were registered simultaneously as we tracked the females . We considered a female to have visited a male if she approached to within 100m of his song perch . This range criterion was selected knowing that a male's song is clearly heard by humans from a distance of 100 m and that, in most cases, the female at this distance also trespassed across the boundary of his territory . A female that is mated to a male calls from her nest quite regularly, ranging from a few calls per h up to several calls per min (Bensch & Hasselquist 1991 b) . The call can be described as a high pitched and rapid version of the initial phrases of a male's song and is easily heard by a human ear from a distance of 50 m . Thus, prospecting females might use these calls to assess a male's mating status . When a released female was in a territory of a mated male we registered the calling frequency of his females . Throughout the study, we make no distinction between the male and his territory . Although we write that a female has selected a particular male she could have primarily selected the territory, making the term `breeding situation' (Wittenberger 1976) a more accurate expression .

RESULTS The Breeding Candidates In the two study years, 13 and 14 males, respectively, defended territories in the experimental area (Fig . 1) . In Fig . 2 we have given detailed information of the males' arrival dates as well as the dates of each mating in the two years . Early arriving males attracted more females (native and introduced) than males arriving later (1989, r s = - 0 . 781, N=13, P<0 . 001 ; 1990, r,=-0-666, N=14, P<0 . 01) . Also, male arrival date was significantly correlated with the order in which they attracted

Bensch & Hasseiguist : Active female choice

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Figure 1 . Map of the study area showing the location of male territories in 1989 (Roman numerals) and in 1990 (Arabic numerals) . Five males were present in both years (III = 1, V = 7, VI = 11, X1=10, XIII = 8) . Hatched areas indicate grazed meadows surrounding the great reed warbler breeding habitat ; viz . reed beds (stippled) stand in shallow water (white) .

females (1989, r s =0 . 847, N=13, P<0001 ; 1990, rti =0 . 902, N=14, P<0001) . However, a serious complication to this analysis is that not all males had established territories when the first females arrived . In 1990 only one male had established at the time the first female settled and he was of course her choice . A more accurate way to test whether male arrival date influenced their success in attracting their first female is to compare the arrival day for the mated male with those of the unmated males present at the day of mating . By using the data presented in Fig . 2 and combining the 2 years, in 17 out of 22 comparisons the mated male had an arrival date earlier than the median for the unmated males present on the actual day, and later than the median in only two comparisons . The difference is

significant (d= 3 . 44, P<0-001, sign test) and underlines the importance of male arrival date for male mating success .

Comparisons with Unmanipulated Females The 13 introduced females settled in the study area, on average, slightly later than females belonging to the study population but most females were released well within the period when the native females settled (Fig. 2) . Their final mate choice was made within 9-73 h (Table I) . Release date had no effect on the number of days until pair formation (rs = -0 . 01, N= 11, P> 0 1) . Twelve of the females commenced egg laying on average 5 . 7 days after release . In these respects the introduced females



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Bensch & Hasselquist : Active female choice

Table 1 . Results of the radio-tracking experiment Female behaviour Time from release to pair formation (days) Time from pair formation to start of egg laying (days) Linear distance (km)* Distance moved (km)t Number of males visited All males Males singing long song

SD

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N

12

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*The linear distance from the place of release to the selected breeding site . tThe distance moved i s the sum of all movements longer than 10 m . behaved in a similar way to females that had suffered from nest predation, supporting the view that the experiment mimicked a natural situation . Data from 1987-1990 show that after a nest failure, females that renested with the same male started egg laying after 5 . 5 ±0 . 7 days (X±sD, N= 17), significantly sooner than those changing partner (7 . 1 ±2 . 2 days, N=9 ; t,,=2 . 24, P<0 . 05, Student's t-test) . Thus, the latter group had 1 . 6 days that could have been used for mate choice . Behaviour of Unmated Females The general behaviour of the 11 females was rather similar . We have given a more thorough illustration of the movements of one of the females (89-A) in Fig . 3 . She was released on 22 May and after a short survey of the area she almost stopped moving and remained in a reed bed (A) throughout the day . For a short period she was near male V and then male VI . The following morning at 0530 hours she started moving eastwards . During the next 5 h she passed within 100m of all six males in the eastern part of the study area . Finally, she stayed for quite some time in the territory of male VI . After 15 min the male detected her, but it seemed as if the female avoided contact . When the male eventually approached the female, after flying around for 25 min in his territory, she left and flew to an area with no territorial males (B) where she stayed . We lost contact with her for almost 3 h . When she returned to male VI he immediately switched to short song. After 40 min the male was heard singing

305

a rapid and intensive song while the female uttered harsh calls . Based on two previous observations, we conclude that this song is closely associated with copulation . The female started nest building the same evening and egg laying began 5 days later . In general, all the I I tracked females behaved similarly to the female illustrated in Fig . 3 . Normally, when a female was within 100m of a singing male she intermixed periods of quick movements with periods when she sat still . Meanwhile, the male was singing, apparently unaware of the female visitor and listener . When females were visiting males (54 h tracked from close range) they appeared to behave more secretively than when outside territories (115h tracked) . Outside territories we saw females sitting clearly visible more often than when inside territories (19 versus I observation) . In contrast, females flying between clumps of reeds were seen equally often outside as inside territories (18 versus 19 times) indicating that the difference in female visibility inside and outside territorites was due to female behaviour and not to observer or habitat bias . It appeared as if when the male detected the female he immediately approached her . With one exception, when the two birds were sitting on the same reed stem and showed typical courtship display with wing-flicking for a few minutes, the female left the territory when detected by the male (N= 12) . At one instance, the male 90-111 continued to sing long song throughout the day while the female 90-A was in or in the vicinity of his territory which is in sharp contrast to the normal behaviour . At 0800 hours the male sang short song and, according to acoustical cues, the birds appeared to be copulating but he soon resumed long song. After that, the male switched to short song and approached the female several times but she withdrew and the male resumed long song from his song perch . After 9 h the male switched permanently to short song and the female began nest building . During the period between release and pair formation, the females spent a substantial part of their time outside (more than 100 m from a male's song perch) the males' territories (X= 53%) . The linear distance between the site of release and the selected breeding site (Table I) was not correlated with the distance moved (rs = -0 . 34, N= 11, P > 0 . 1) . Thus, the movements cannot be regarded as dispersal from the site of release . In 20 of 61 cases in which females visited territories already containing breeding females, we heard



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Number of Visited Males The females visited the territories of 3-11 different males before settling on a territory (Table I) and a few males were visited repeatedly (Table II) . Of the visited males, on average 32% (range 0-55%) sang short song as they had a nest-building female in their territory ; none of these was selected (a significant deviation from randomness, P=0 . 004, exact probability test) . So, although the females did visit males singing short song these were not

accepted as mates (see also Hasselquist & Bensch 1991), thus reducing the number of potential breeding partners to those singing long song (Table I) . Only one female visited all available males and the average female visited 63% of those who sang long song. To test whether female choice was related to the male's position in the females' visiting sequence we used the following statistical test . The null hypothesis is that females choose randomly among the males they visit, with respect to the males' position in the visiting sequence . The data are shown in Fig . 4. The sum of the positions of the chosen males should be a random variable whose mean is the sum of the average positions (2 for a sequence of three visits, 2 . 5 for a sequence of four visits, etc .) . Thus, the expected sum for the positions is 38 for all males (Fig . 4a) and 31 when males singing short song are excluded (Fig . 4b) . In both cases, the observed sum is slightly higher

Bensch & Hasselquist : Active female choice

Table 11 . Visiting sequence of males by transmitter-tagged female great reed warblers listed in order of release Visiting sequence* of males (song typet, mating status$)

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Selected mating status§

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Individual males indicated as in Fig . 1 by Roman numerals (1989) and Arabic numerals (1990). */Indicates change of dates . +Long song (L) or short song (S) . $Unmated (0), monogamous (1), bigynous (2), trigynous (3) . §Primary (1), secondary (2) . **Two females, which we failed to track, selected males in parentheses . than the expected sum, 41 and 35, respectively . We assume these sums to be normally distributed, with variances equal to the sums of the theoretical variances of each of the 11 individuals' sequences (the variance of a choice among three males is 0 . 667, among four males 1 . 25, etc .) . The theoretical standard deviations are 6 . 1 for all males and 4 . 6 for males singing long song . In both cases the standard deviation is larger than the differences between the observed and the expected sum (41-38=3 and 35-31=4) . Thus, the null hypothesis cannot be rejected . The Quality of the Choice Early arriving males attracted more females than those arriving late (Fig . 2) and in a larger analysis

307

male arrival day was very important when explaining male mating success, mostly because early males settled in the best territories (Bensch & Hasselquist 199 la) . Thus, it seems logical to analyse whether the introduced females showed preferences for early arriving males . This would have been easy if all males had been unmated at the time of each release so that the prospecting females were faced with primary options only . All females in the experiment visited both mated and unmated males and we cannot rank the primary and secondary options on the same scale although we know that for any given territory the primary female is, on average . more successful than the secondary female (Bensch & Hasselquist 1991c) . However, we can check whether females within their selected mating status group (primary or secondary) favoured early arriving males . Therefore, we first looked at the four tracked females who selected unmated males and compared the arrival day of their chosen males with the arrival days of the rejected and similarly unmated males . For instance, among the five visited males, excluding a male singing short song, female 89-A (Table II) had four alternative unmated males . She selected male VI who was the second one to arrive, i .e . a male arriving earlier than the median of the four. We treated the seven females who selected already mated males in the same way, i .e . the arrival days of their chosen males were compared with the arrival days of visited males that were already mated with one female. Within their mating status group, the experimental females chose males with an earlier arrival day than the median male (d= 2 . 65, P < 0-0 1, sign test ; Table III) .

DISCUSSION The Experiment This is the first study to show that females of a territorial passerine regularly visit more than one male before settling. The time elapsing from release to pair formation (X=1 . 2 days) was similar to that found for the pied flycatcher (Slagsvold et al . 1988) . During the period between release and pair formation females visited territories of on average six males and only one female visited all males in the study area . The introduction of females into the study population at Kvismaren may have had consequences for both the native birds and the experimental females . making the observed behaviour unlike natural



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Animal Behaviour, 44, 2

10

(a)

J

N

I I I I I I I I I I I I 12 2 4 6 8 10 12 2 4 6 8 10 Number of visited males

Figure 4 . Finally selected male in chronological order of encounter by the inspecting female in relation to the total number of males she visited . (a) All males and (b) males singing long song . Table III . Arrival dates of selected males in relation to the median arrival date of visited alternative males offering the same mating status Arrival dates of selected male in relation to the median Earlier Median Later

Female settled as Primary

Secondary

Total

4

4 2 I

8 2 1

Only males singing long song are considered . behaviour . However, observations do not support this view . First, the adult sex ratios (females/males) after the introduction of the females were 1-77 and 1 . 13 in 1989 and 1990, respectively, which does not differ to a great extent to that in the study area in previous years (X= 1 . 28, range 0 . 93-1 . 56, Bensch & Hasselquist 1991 a) . Second, for the release experiment we selected only females that were newly mated (1 -2 days after mating), using the size of their nests under construction as a criterion . At least nine of the 13 females had not bred previously since they had not yet fully developed a brood patch . Thus, the females in this experiment were probably more likely to show normal behaviour than females already laying or incubating eggs. Third, in two important respects the released and native females did not differ, i .e . in their diurnal mating pattern and the number of days between pair formation and start of egg laying (unpublished data) . Also, the number of days between release and pair formation was similar to the period between nest predation and re-mating in females who selected a new male .

Were the females actively evaluating the breeding options when visiting the male territories or were they merely using the territories for feeding and then settling randomly? We have strong indications that females, in general, evaluated the breeding options . Females never mated with males that sang short song, indicating that the behaviour of the male was important, and among the visited males, females settled with early arriving males among males offering a breeding situation with the same mating status (Table III) . This relationship can emerge only if females rejected late males when visiting their territories . Also, the behaviour of females indicates that males were evaluated ; they seemed to conceal their presence in male territories, but not when outside male territories .

Mate Sampling Tactics Theories on mate sampling tactics (Janetos 1980 ; Wittenberger 1983 ; Real 1990) identify five main strategies : (1) random mating, (2) fixed-threshold tactic ; (3) sequential-comparison tactic ; (4) one-step decision tactic ; and (5) best-of-N tactic. These can at least partly be distinguished on the basis of the movement pattern shown by the choosing individual . A female adopting a random mating tactic should settle with the first male encountered since this minimizes the costs of mate choice (Pomiankowski 1987) . A fixed-threshold tactic assumes that the female chooses the first male whose desired variable exceeds a fixed value . This leads to females always settling with the last visited male (all dots on the dashed line in Fig . 4) . Females using a sequential-comparison tactic compare two

Bensch & Hasselquist : Active female choice

males at a time and continue searching as long as the ith male is better than the (i-1)th male . These females should settle with the most recently visited or the immediately preceding male . Females adopting the best-of-N tactic visit a number of candidates and select the best one among these . The one-step decision tactic gives different movement patterns depending on whether the individual's acceptance threshold, Wc, ( Real 1990), is assumed to be constant or decreasing as it is searching for a mate . If .1 is constant, females should behave as if they W ;, used a fixed-threshold tactic since a rejected male can never be acceptable . However, if War ;, decreases with time, a formerly rejected male (male i) can be acceptable when later revisited, given that W ., has fallen below the expected fitness of the male (W;) . This might lead to a movement pattern where some females mate with previously visited males, as in the best-of-N tactic, although a high proportion of females should still select the last visited male . Random settlement can be rejected since all females visited more than one male (Fig . 4), assuming that the females were evaluating the breeding options when visiting male territories . Similarly, few females settled in the territory of the last visited male, thus making both a fixedthreshold tactic and a one-step decision tactic with constant acceptance threshold unlikely . Although females showed a slight but not significant tendency to select males visited after the median male, the sequential-comparison tactic can be rejected since 36-55% of the females (Fig . 4a, b) did not choose any of the last two visited males but returned to a male visited two to seven males back . In fact, the females' choices of males were not significantly related to the males' positions in the females' visiting sequences . This can be interpreted as support for the best-of-N tactic although the one-step decision tactic with a decreasing acceptance threshold cannot be ruled out . When first formulated, individuals using the bestof-n tactic were assumed to be able to recall and return to any one of the N males visited whereas females using the one-step decision tactic lacked this possibility (Janetos 1980) . However, one can also allow individuals using the one-step decision tactic to recall previously encountered males (Real 1990) . In fact, individuals having a brief capacity to remember previously inspected males, together with a decreasing acceptance threshold, would be better off than individuals lacking this capacity . The movement pattern of such individuals would be

30 9

almost indistinguishable from that of individuals using a best-of-N tactic . Thus, the moving pattern found in our study (Fig . 4) might reflect a female's ability to remember and return to previously visited (best-of-N) or rejected (one-step decision) males . Costs of Mate Sampling Without costs, a female adopting the best-of-N tactic should sample all potential males in the population before making a choice (Janetos 1980 : Real 1990) . The number of sampled males could also be large if females use a one-step decision tactic, where the optimal acceptance threshold (W«; t) is equivalent to the best male in the population, leading to females continuously searching until such a male is found (Real 1990) . However, the marginal benefit of continued sampling decreases with increasing number of sampled males (Janetos 1980) since choice seems to be costly (Alatalo et al . 1988 ; Slagsvold et al . 1988) . The optimal number of visited males will then be lower for both strategies (Real 1990) . Two different types of costs could constrain the number of visited males for female great reed warblers : (1) direct costs and (2) opportunity costs (Real 1990) . In the case of the great reed warbler, we are able to measure one possible direct cost, time expenditure (see Temrin, in press for discussion at length) . One day of mate choice corresponds to a reduction in fledging success of approximately 0 . 02 young because of a general decrease in reproductive success during the course of the season (126 female settlements in May and June 1984-1989 excluding seven settlements in July ; unpublished data) . Since many males can be visited in I day (Table 1) it seems unlikely that time expenditure is an important limiting factor for the number of visited males . Another direct cost of possible importance is energy expenditure, although the short distances between the males in this study make it unlikely to be an important cost . Risk of adult predation is probably too minute to be of any importance (during our study only one adult great reed warbler has disappeared during the breeding season under circumstances suggesting mortality) . One of the opportunity costs mentioned by Real (1990) could be of importance . If females leave an acceptable male (best-of-N) or a male with a W ; slightly below Wcr;, (one-step decision) in order to inspect other alternatives, this male may meanwhile become

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Animal Behaviour, 44, 2

mated by another female . Although the frequency with which this occurs is difficult to quantify, it probably happens quite often . In fact, it might have been experienced by female 89-C (Table II) . During the first 3 h after her release she first visited males VI, V and IX, who all sang long song . When she returned to male V a few hours later he had a new female and sang short song and this was also the case when she returned to male VI . She soon selected male IX who was now the only available breeding option of the three originally inspected males . This cost may be even more important in species with short breeding seasons and in which female settlement is more synchronized than in the great reed warbler (e .g . pied flycatcher, Alatalo et al . 1981) .

Conclusion Our study shows that females visit a sample of males before settling . Their tendency to choose early arriving males (Table III) supports the view that they evaluate the quality of males or their territories or both . This, together with the fact that visiting females can easily perceive the presence of other females in the territory, indicates that polygyny in the great reed warbler arises from an active choice of already-mated males rather than from males deceiving females (cf. Catchpole et al . 1985) . The movement patterns of searching females show that the majority mate with males other than the one last visited . We argue that this reflects a capacity of females to remember the quality of previously visited males and to return to one of them whether the search model used is a best-of-n or a one-step-decision tactic .

ACKNOWLEDGMENTS We are especially indebted to P . Frodin, F . Haas, M . Haraldsson and U . Ottosson who helped us to keep track of the females . G . Goransson kindly made the transmitters and Takern Field Station gave valuable logistic support when we captured the females for the experiment . We thank S . Douwes for drawing the figures . T . Alerstam, H . Kallander, J-A . Nilsson, T . v . Schantz, H . G . Smith, H . Temrin and three anonymous referees made valuable comments on the manuscript . The study was financially supported by Elis Wide's

Foundation, Royal Swedish Academy of Science (Hierta-Retzius) and Swedish Natural Science Research Council (to T . v . Schantz) . This is report no . 72 from Kvismare Bird Observatory .

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