Competing Females and Caring Males. Polyandry and Sex-Role

Reversal in African Black Coucals, Centropus grillii

Wolfgang Goymann*�, Andrea Wittenzellner� & John C. Wingfield*

*Department of Biology, University of Washington, Seattle, WA, USA; �MaxPlanck Institute for Ornithology, Andechs, Germany

Abstract

Most species of birds show bi-parental or female-only care. However, aminority of species is polyandrous and expresses male-only care. So far, suchreversals in sex roles have been demonstrated only in precocial bird species, butthere was suggestive evidence that such a mating system may occur in one altricialbird species, the black coucal, Centropus grillii. In a field study in Tanzania weinvestigated whether black coucals are sex-role reversed and polyandrous. Wefound that males were mated to one female, rarely vocalized and provided allparental care from incubation of eggs to feeding of young. In contrast, femaleblack coucals were about 69% heavier and 39% larger than males andpolyandrous. They spent a large proportion of time calling from conspicuousperches, defended breeding territories, did not help in provisioning young and hada higher potential reproductive rate than males. We conclude that the blackcoucal currently represents the only altricial bird species with sole male parentalcare and a classical polyandrous mating system. High nest predation pressure andsmall territory sizes due to high food abundance may have been important factorsin the evolution of sex-role reversal and polyandry in this species.

Correspondence: Wolfgang Goymann, Max Planck Institute for Ornithology,Von-Der-Tann-Str. 7,D-82346Andechs, Germany. E-mail: goymann@orn.mpg.de

Introduction

Most species of birds show biparental care and are socially monogamous, butthere are some species in which one parent deserts the clutch and parental care isprovided by the remaining parent. Usually males desert and females provide care,but in about 1% of the species, these sex roles are reversed (Lack 1968). Classicalpolyandry is a mating system in which a single female mates either sequentially orsimultaneously with two or more males during a single breeding season, and malestypically form bonds with a single female per breeding cycle. Each male has hisown nest, incubates the eggs and provides care for his young, typically with no or

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little help from the female (Oring 1982, 1986; Ligon 1999). With regard to theevolution and maintenance of classical polyandry, these species should have smallclutch sizes and have young that are born at an advanced stage of development(precociality) and which gather their own food (Emlen & Oring 1977; Oring 1982,1986; Erckmann 1983; Clutton-Brock 1991), thus limiting the costs of paternalcare. Indeed, classical polyandry occurs in tinamous (Tinamiformes), shorebirds(Charadriiformes) and buttonquail (Gruiformes) (Ligon 1999), all of which havesmall clutch sizes and precocial young. However, incidental observations (Vernon1971, 1975) suggested that classical polyandry also occurs in a group of birds withlarger clutches and altricial young, the coucals (Centropodinae). Coucals are adistinctive group of cuckoos that are widely distributed in the Old World tropics,mainly Africa and South-east Asia and one species in Australia (Payne 1997).Coucals are non-parasitic, semi-terrestrial birds, ranging in size between 90 and600 g, and feed mainly on large insects and small vertebrates. They vary in thedegree of reversed sexual size dimorphism and sex-role reversal (Andersson 1995).Most coucals are socially monogamous and both parents share parental duties(Andersson 1995). Observations of the black coucal (Centropus grillii), however,suggested that this species may have a classically polyandrous mating system(Vernon 1971). They have a relatively variable clutch size (1–7 eggs; W. Goymann,unpubl. data) and their altricial young need to be fed for several weeks. A closerlook at this and other coucal species might therefore shed new light on theevolution of reversed sex-roles, reversed sexual size dimorphism, and polyandry.Vernon’s (1971) observations have gained some attention (Oring 1982; Andersson1995; Slotow 1996; Ligon 1997, 1999), but a quantitative study with individuallymarked black coucals was still lacking. Thus, the aim of this study was to describethe mating system of black coucals and find quantitative evidence for sex-rolereversal and classical polyandry in this species. In a companion paper (Goymann& Wingfield 2004) we describe the profile of sex-steroids in females and males ofthis species.

Study Area and Methods

We studied a population of black coucals in flooded grassland of the Usanguwetlands, located at 8�41¢S 34�5¢E in Mbeya region, Tanzania, during thebreeding season (January–May) in 2001 and 2002. For further details on the studyarea, capture techniques and ethical considerations see Goymann & Wingfield(2004).

Black coucals were marked with custom-made wing bands (approx. 2 cmlength · 1.5 cm width, <0.4 g) in individual colour combinations. In the 2 yr 23females and 23 males were fitted with a Holohil BD-2G radiotransmitter (<2 g;Holohil Systems Ltd, Carp, Ontario, Canada) using a Rappole harness (Rappole& Tipton 1991) made out of soft polyethylene (PE) microtubing (0.9 mmdiameter). As recapture of coucals was unlikely we made sure that the transmitterswould fall off eventually: the soft PE microtubing offered only limited resistance tobiting (e.g. five coucals bit through the tubing of their transmitters within 2 wk)

808 W. Goymann, A. Wittenzellner & J. C. Wingfield

and, in addition, the harness was closed with a two component adhesive (UHUSofortfest), creating a hyphenation point, so that the transmitter would eventuallyfall off. In fact, the transmitters of two birds that were tagged early during the 2001season broke at the hyphenation point and fell off after 54 and 79 d.

During 2001, eight females and 11 males were equipped with transmitters andtags and there was no incident of depredation. In 2002, 15 females and 12 malesreceived a transmitter and tags, and eight of these females and three of these maleswere depredated by raptors (n ¼ 2) or mammals (n ¼ 9). In contrast to 2001,during 2002 many marsh harriers (Circus aeruginosus) and marsh mongooses(Atilax paludinosus) were present in the area and we observed several attacks byharriers on perching black coucals (tagged and untagged). Thus, the predationrisk may have been generally higher in 2002 than in 2001, but after loosing thefirst five birds to predators we decided to no longer use wing tags because theymay have increased the visibility of black coucals for predators.

We took the followingmeasurements: bodymass (to the nearest 1 g), bill, wingand tail length (to 1 mm), tarsus- and claw-length (to 0.1 mm) and length anddiameter of the cloacal protuberance (to 1 mm), from which we calculated thevolume of the cloacal protuberance (assuming a cylindrical shape: vol. ¼ pr2h).Typically, sexual size dimorphism is estimated using differences in mass (e.g.Butchart 2000). However, as females may increase their mass during the breedingseason we decided to include also structural size measures to estimate sizedifferences between females andmales. To be able to compare linearmeasures (suchas bill, wing, tail, tarsus and claw lengths) with body mass (a measure thatcorrelates with body volume und thus represents a cubic measure) we cubed thelinear measures (Calder 1984, p. 10). The biometric data include measurements of10 birds sampled during a pilot study conducted between January and February2000. In the field, birds were sexed using their body mass, which does not overlapbetween females and males. Upon capture a small blood sample was taken forsubsequent hormonal and genetic analyses (see also Goymann & Wingfield 2004).The gender of each individual was unambiguously confirmed during behaviouralobservations (copulations) and/or in the lab, using genetic sexmarkers (Fridolfsson& Ellegren 1999; W. Goymann & B. Kempenaers, unpubl. data). In 2002, two non-nesting males were killed (with a shotgun) for preliminary brain studies. Bothmalesdied instantaneously. Black coucals are not a threatened species and the killingswere covered by the research permit. We removed the testes of these males andmeasured them with vernier callipers to calculate the volume using the formula vol.(mm3) ¼ 4/3pa2b (a ¼ half the diameter of the testis, b ¼ length of the testis). Todetermine testis mass the tissue was weighed on a Sartorius balance.

Birds were individually identified by reading their wing bands and/ortracking them by telemetry. In addition, three unbanded birds were individuallyidentified using distinctive plumage characteristics. We conducted 288 focalanimal samples with an average duration of 63 ± 2 min (119 and 154 focalsampling hours for females and males, respectively) with binoculars and spottingscopes between 06:00 and 14:00 hours (99%) and occasionally also between 15:00and 19:00 hours (1%). For males, 87% of focal observations were conducted

809Mating System of African Black Coucals

while they were attending nests. As there were very few obstacles the visibility ofthe study area was good. We thus were usually able to observe the movements of afemale throughout her entire home range (allowing to observe interactions withmore than one mate). All observations were conducted from a distance of20–100 m sitting either on the roof of a car or standing on an artificial bank.

We tracked each radio-collared bird at least every 2–3 d and noted itsposition with Global Positioning System (GPS). Additionally, we recorded thepositions of birds perching at or close to landmarks with known GPS positions(e.g. certain bushes, perches or trees). Distances between pairs were calculatedusing GPS data and distance estimates obtained during focal observations. Homerange sizes were calculated connecting the outermost GPS positions obtainedfrom an individual bird to a polygon and calculating the surface area of thepolygon with Mapmaker 3 (Argyll, Scotland, UK). For the calculation weincluded maximally one position per individual and day to ensure that data areindependent. On average, each individual contributed 16.7 ± 1.7 (range: 6–60)independent GPS data points for the calculation of its home range size. To makesure that individuals with small sample sizes did not distort the calculation werepeated the analysis including only data from individuals that contributed morethan average (>16) independent GPS data points.

During focal animal observations we scored an interaction of two or morecoucals as territorial aggression, when one coucal entered the territory of anothercoucal and was chased by the territory owner, or when two or more coucals met atthe border of their territories and called and/or chased each other. We scored aninteraction of coucals as aggressive mate competition when one coucal wasapproaching a coucal of the opposite sex and was then chased away by a coucalthat had the same gender as the approaching coucal. Feeding rates of nestlingswere obtained during focal animal observations. Because of the high visibility andthe limited movement pattern of nesting males it was always possible to observethe male and the area around the nest simultaneously. Thus, feeding attempts ofother birds (i.e. the female) would have been noticed.

We located nests either by following incubating males equipped with aradiotransmitter or by observing feeding males with nestlings. To avoiddisrupting the vegetation close to the nest we never approached the nest directlybut instead passed the nest at a distance of 0.5–1 m. To study incubation patternswe flushed birds from their nests 39 times during different times of day (06:00–15:00 hours). Not a single nest was deserted due to this disruption.

Statistical Analyses

Statistical analyses were performed with Systat 10.2 (Systat Software Inc,Richmond, CA, USA) or by hand (robust rank-order tests and Kolmogorov–Smirnov goodness-of-fit test) following the procedures of Siegel & Castellan(1988). Prior to the analyses we tested for normality (Kolmogorov–SmirnovLillifors test) and equality of variances (Levine test). If possible, data weretransformed to meet criteria for parametric statistical tests. This was carried out

810 W. Goymann, A. Wittenzellner & J. C. Wingfield

for home range sizes (log10[home range size + 1]). If transformation was notfeasible we used non-parametric statistical tests following Siegel & Castellan(1988). The significance level was set at a ¼ 0.05 and all p-values are reported fortwo-tailed tests. Transformed data are graphically represented as back-trans-formed mean values and standard errors. Due to the back-transformation thegraphical representation of the standard errors is not symmetrical.

Results

Proof of Polyandry

During the two breeding seasons we were able to determine the exact numberof mates for 13 individual females: two (15.4%) of these females had one mate,seven (53.8%) had two mates, and four (30.8%) had three mates. Thus, mostfemale black coucals of our study population were simultaneously polyandrous.The habitat and the secretive habits of unmated black coucals prevented us fromestimating the sex-ratio of the adult population. However, vacant territories wererapidly occupied by newcomers, suggesting that there was a pool of non-breedingbirds that readily accept breeding opportunities.

Sexual Size Dimorphism

To estimate the size dimorphism between females and males we conducted aprincipal component analysis of body mass (loading 0.939), tarsus (0.875), bill(0.881), wing (0.941) and tail lengths (0.861) and compared the scores for the firstprincipal component (eigenvalue 4.071), which explained 81% of the variance inthe data, suggesting that the first principal component was a good estimate forsize. Females were significantly larger than males (t-test for pooled variances: t ¼18.974, df ¼ 68, p < 0.0001; Table 1). In body mass, there was no overlap

Table 1: �x ± SEM (and range) of body measurements for adult female and male blackcoucals. A principal component analysis for size differences (including mass, bill, wing, tailand tarsus lengths) revealed that females are significantly larger than males (see text for

further details)

Females N Males NCuberatio

Mass (g) 165.5 ± 2.5 (126–194) 33 97.4 ± 1.2 (78–117) 49Bill length (mm) 25.9 ± 0.2 (22.8–28.5) 28 23.1 ± 0.2 (20.5–27.0) 45 1.41Wing length (mm) 173.1 ± 1.0 (163–187) 28 152.8 ± 0.7 (142–166) 45 1.45Tail length (mm) 188.8 ± 1.9 (155–206) 28 168.1 ± 1.4 (147–185) 42 1.42Tarsus length (mm) 42.7 ± 0.3 (39.5–44.8) 28 38.9 ± 0.2 (34.8–41.9) 45 1.32Claw length (mm) 26.2 ± 0.5 (21.4–33.3) 27 23.7 ± 0.4 (18.9–31.6) 39 1.35Cloacal protuberancevolume (mm3)

296 ± 23 (77–565) 26 796.3 ± 50.0 (201–1693) 39

811Mating System of African Black Coucals

between females and males, and on average, females were 69.8% heavier thanmales (Table 1). Using the mean of the cube of the ratios of linear measures forstructural size estimates (bill, wing, tail, tarsus and claw lengths) females were onaverage 39% times larger than males (Table 1). Only the volume of the cloacalprotuberance was significantly larger in males than in females (t-test for separatevariances: t ¼ )9.227, df ¼ 51.6, p < 0.0001; Table 1). Both males that werekilled had only one testis each. As previously reported (Chapin 1939) the lefttestes were absent. Testis volumes were 571 mm3 (90 g body mass) and 759 mm3

(102 g body mass), thus average volume was 6.9 mm3/g body mass. Testis masseswere 0.64 and 0.63 g, respectively, which is about 0.7% of the body mass.

Territory Size and Territorial Behaviour

Suitable habitat was saturated by black coucals. Since there were very fewobstacles individuals had the potential to observe interactions of other birds thatoccurred in the air or on top of the vegetation. Females had significantly largerhome ranges than males (t-test for separate variances: t ¼ 6.319, df ¼ 38.6,p < 0.0001; Fig. 1), a result that remained unchanged if we include only those 10females and 13 males that contributed more than 16 independent GPS data pointsfor the calculation of their respective territory sizes (females: 2.53 ± 0.31 ha;males: 1.14 ± 0.21 ha; t ¼ 3.698, df ¼ 16.4, p < 0.002). Females engaged interritorial behaviour significantly more often than males: we observed 28 agonisticterritorial interactions between individual females, but only one such interactionbetween individual males [G-test of goodness-of-fit accounting for differences in

Fig. 1: Backtransformed �x ± SE territory sizes of female and male black coucals (numbers above barsrepresent sample sizes and comparisons were made with robust rank order tests following Siegel &

Castellan (1988)

812 W. Goymann, A. Wittenzellner & J. C. Wingfield

focal sampling time of females (39.2%) and males (60.8%), G ¼ 44.02,p < 0.0001]. During four of the 28 agonistic territorial interactions betweenfemales one or both of the females were accompanied by a male, but the activerole was always taken by the female with the male following her.

While females competed for territories, males defended females. During focalsamplings we observed 33 times that a male chased another male which tried toapproach the female he was mated with. This happened mainly while therespective female was singing in the part of her territory that she shared with thedefending male and regardless of the breeding stage of the defending male (matingn ¼ 12, incubation n ¼ 4, nestlings n ¼ 7, fledglings n ¼ 1, unknown n ¼ 9).Typically, the males chased each other and then disappeared in dense vegetation,re-emerged from the grass, and chased each other again, until one of them gave upand flew off or finally disappeared in the vegetation. In contrast, we neverobserved females competing for direct access to males (male–female comparisonof direct competition for access to a mate, taking into account that focal samplingperiods for females and males differed: Kolmogorov–Smirnov test of goodness-of-fit, D ¼ 0.392, p < 0.01).

Calls and Calling Rates

We distinguished five different kind of calls, the �whoot� (Fig. 2a, b), the�k’tuc� (Fig. 2a, b), the bubbling call (Fig. 2c), the coo (Fig. 2d) and the �kiok�.

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Fig. 2: (a) Spectrogram of seven �whoot� calls (frequency range: 265–368 Hz) followed by eight �k’tuc�calls (554–1005 Hz) from a female black coucal. (b) Spectrogram of eight �whoot� calls (333–565 Hz)and four �k’tuc� calls (732–1424 Hz) from a male black coucal. (c) Spectrogram of a bubbling call and

(d) a cooing call

813Mating System of African Black Coucals

The �whoot� consists of a single low note that may be repeated several times(Fig. 2a, b) and is often followed by �k’tuc�, a quick double note repeated onceevery 2 s in bursts of calls, containing 1–25 �k’tuc� (Fig. 2a, b). Our term �k’tuc�corresponds to what Vernon (1971) referred to as an �advertisement call�.Competing females engaged in close agonistic interactions typically lowered thefrequency of �whoot� calls. Females uttered both significantly more �whoot�(robust rank-order test: nf ¼ 22, Nm ¼ 34; U ¼ 28.94, U ¼ 16.18, p < 0.0001;Fig. 3) and �k’tuc� (robust rank-order test: p < 0.0001; Fig. 3) than males. Theytypically gave these calls from a conspicuous perch and often called for a coupleof hours, beginning at dawn. Females of neighbouring territories frequentlyalternated their calling. Male callers had a high pitched voice compared withfemales (compare Fig. 2a with 2b).

The bubbling call is a single loud note, first repeated with a low rate and in alow frequency range (690–1100 Hz) and then repeated more rapidly at a higherfrequency range (750–1500 Hz; �cou… cou… cou… cou.cou.cou.cou.cou�; Fig. 2c).This call was given less frequently than �whoot� or �k’tuc�, but again females called

Fig. 3: Median (thin vertical line), interquartile range (box), 5% and 95% percentiles (lines withwhisker caps), and mean (thick vertical line) calling rates of 22 female and 34 male black coucals for

three types of calls, the �k’tuc�, the �whoot� and the bubbling call

814 W. Goymann, A. Wittenzellner & J. C. Wingfield

more frequently than males (robust rank-order test: U ¼ 2.23, p < 0.05; Fig. 3).Typically, coucals uttered the bubbling call (i) immediately before they initiatedflight, (ii) when another bird approached them, or (iii) during flight.

The coo (Fig. 2d) is a soft low frequency (frequency range: 200–400 Hz) andintensity sound very similar to the cooing of pigeons. Due to its low basicfrequency and intensity this sound could only be heard in close proximity(<20 m) of the cooing coucal. In total, we heard this sound during 36 differentoccasions, invariably situations of close distance (<10 m) conflict betweenfemales (n ¼ 30) or when a female chased a male (n ¼ 6).

The �kiok� is a slow clucking sound given by females and males. It consists ofrepeats of a deep single �kok� note in females and a higher pitched �kiok� note inmales. This call was used as a warning call or signalled general alertness. We didnot quantify �kiok� frequencies.

Mating and Courtship

Courtship and mating behaviour was already described in detail by Vernon(1971). Black coucals copulated during all stages of the breeding cycle. From 44copulations with known breeding status of the male nine occurred during themating and egg-laying stage, six during incubation, 21 during the nestling stage,and six during the early fledgling stage. Furthermore, juvenile male coucals of anestimated age of 6–8 wk showed a strong interest in calling females and weobserved two matings and three mating attempts of juvenile males (2–3 mo old)with adult territorial females.

Mate Guarding

Mates were significantly closer to each other during the mating stage(8.8 ± 3.1 m) than during the incubation and chick rearing stage(76.0 ± 16.7 m; Wilcoxon signed ranks test, n ¼ 8 coucal pairs, Z ¼ 2.366,p ¼ 0.018) and individual males spent significantly more time close to their mate(<10 m) during the mating stage (53 ± 13% of total focal observation time)than during the incubation and chick rearing stages (2 ± 0.7%; Wilcoxon signedranks test, n ¼ 6 males, Z ¼ )2.201, p ¼ 0.028). Furthermore, we recorded thesequence of departure in all occasions in which both birds of a pair left a commonperching area. For 36 pairs of black coucals the male was significantly more likelyto follow the female than vice versa (m fi f: n ¼ 87; f fi m: n ¼ 11; sign test:n ¼ 36 pairs, p ¼ 0.0002). This pattern was even more pronounced consideringonly the mating and egg-laying substages (m fi f: n ¼ 73; f fi m: n ¼ 6; sign test:n ¼ 26 coucal pairs, p < 0.0002).

Parental Care

Black coucals build dome-shaped nests 15–50 cm above ground within densevegetation. Nests have an entrance on one side and an additional �break-through

815Mating System of African Black Coucals

emergency exit� on the opposite side of the entrance, which older chicks frequentlytried to use when we approached the nests for measurements. As described byVernon (1971) nests consisted of three materials: living grass blades that werewrapped around and bowed over to form the outer frame, dry grass blades for theinner frame which was thickest at the base, and a lining of leaves in the bowl.

We never observed the initial stages of nest building (the frame is built withliving grasses that grow at the nest site). However, for 22 different nests weobserved that males carried leaves and grasses to the nest at various stages of thenesting cycle (seven at the nest building stage, four during incubation, five whenfeeding nestlings, and six at an unknown stage), suggesting that males are at leastresponsible for building the inner frame and leaf lining of the nest. We never saw afemale carrying nesting material (binomial test, n ¼ 22, p < 0.0001).

Thirty-nine times we flushed birds from 20 different nests during theincubation stage. With one exception (a female during egg laying) it was alwaysthe male of a pair that was flushed from the nest, corroborating earlier suggestionsfor the black coucal (Vernon 1971) and coucals in general (Payne 1997) that malesare responsible for incubation (sign test, n ¼ 20, p < 0.0001).

During nest observations (161 h at 32 nests) we counted a total of 588 fooditems brought to the nestlings, 572 (97.3%) of which were brought by males,suggesting that, in general, only males feed the nestlings (Wilcoxon test, n ¼ 32,Z ¼ )4.938, p < 0.0001). Once, one female brought a single food item to the nestof one of her two mates. Another female provided more substantial parental careby assisting her first mate at the end of the breeding season, after her second matehad lost a clutch and had left the area.

Once their chicks had fledged males spent most of their time on the ground,presumably leading the fledglings (coucals can run but not fly when they leave thenest) to food resources and feeding them on the ground. Hence, it was not feasibleto quantify the feeding rate of fledglings. In general, females did not appear toassist their mates. There was one instructive exception, concerning a pair that hadinitiated their third and last clutch about 2–4 d after the chicks of their secondclutch had left the nest. While the male fed the nestlings of the third clutch we sawhis mate feeding fledged chicks, presumably from the second clutch.

Potential Reproductive Rates

The potential reproductive rate (PRR) is either defined as �the maximumnumber of independent offspring that parents can produce per unit time�(Clutton-Brock & Vincent 1991) or as the inversed �time out� for males andfemales (Clutton-Brock & Parker 1992). Typically, the PRR is higher for malesthan for females and competition for mates is higher amongst males. In classicallypolyandrous bird species the PRR is reversed (Eens & Pinxten 2000) and thus,competition for mates is more intense amongst females than amongst males.Assuming (i) an incubation time of approx. 14 d (Vernon 1971), (ii) a nestlingperiod of 12.7 ± 0.2 d (n ¼ 20 nests), and (iii) a minimum time period of6 ± 1 d (n ¼ 6) between fledging one clutch and initiating a new clutch, the

816 W. Goymann, A. Wittenzellner & J. C. Wingfield

minimum interclutch interval for a male black coucal was approx. 33 d. With abreeding season of about 4 mo (120 d) a male black coucal could maximally raise3–4 clutches per season. Females produced clutches at a mean interval of13.6 ± 2.0 d (n ¼ 10) measured as the interval between the first days of egglaying of consecutive clutches. Thus, a polyandrous female with three mates couldtherefore produce approximately nine clutches per season. The ratio of PRR wastherefore skewed towards females by about 2–3:1.

Discussion

The results of this study corroborate earlier reports on a small number ofuntagged birds (Vernon 1971), confirming with an individually marked popula-tion that black coucals are polyandrous and sex-role reversed. The black coucalsof our study area expressed traits that are typically associated with a classicalpolyandrous mating system (Eens & Pinxten 2000): (i) Females were much largerthan males, (ii) females aggressively defended large territories, and (iii) in contrastto males, called frequently. (iv) Females generally did not participate in parentalcare and (v) had a PRR that was 2–3 times higher than that of males. Althoughother factors may modify the correspondence between PRR and the intensity ofsexual selection (Kvarnemo & Ahnesjo 1996, 2002), these data suggest thatreversed sexual selection operates in black coucals. More specifically, this matingsystem can be described as resource defence polyandry (Emlen & Oring 1977), asfemales defend territories, but not mates. With the exception of the black coucalall well-documented cases of classical polyandry are from precocial bird specieswith small clutches (see overview in Ligon (1999) and the comparative analysis ofTemrin & Tullberg (1995). It thus seems as if a low reproductive effort for themale would have facilitated the evolution of classical polyandry, but, asdemonstrated by black coucals, it is not a necessary precondition for theevolution of male-only care.

In birds, reversed sexual dimorphism is common not only in species withreversed sex-roles, but also, e.g. in raptors in which sex-roles are not reversed.Previously, few data were available on size differences between female and maleblack coucals (Rowan 1983). Based on these data females were thought to beabout 50% heavier than males (Andersson 1995). The present study demonstratedthat the dimorphism is even more pronounced, with females being almost 70%heavier than males. Based on structural size measures (that are independent ofweight gain that may occur especially in females during the breeding season)female black coucals are about 39% larger than males. Thus, the black coucalrepresents an extreme case of reversed sexual dimorphism, which is only surpassedby a few species of classical polyandrous jacanas (Jenni 1996).

In contrast to males, female black coucals frequently called �k’tuc� and�whoot�. The alternate calling patterns of neighbouring females suggested thatthey conveyed information about their identity and their territorial claims. Whentwo females met at the borders of their territories they typically lowered thefrequency of �whoot� calls, suggesting that this call may carry information about

817Mating System of African Black Coucals

the competitive ability (¼ size) of the caller. Playback of �whoot� and �k’tuc� callsin a territory elicited a strong response of the territory owner during the earlybreeding season. Typically, the female started to call and approached the speakerwithin few seconds after onset of the playback (W. Goymann, unpubl. data).Furthermore, female �k’tuc� and �whoot� calls may help to attract mates, as malesoften responded to calling females or playback of female song by flying towardsthem or to the speaker (Vernon 1971, W. Goymann, unpubl. data). While the�k’tuc�, the �whoot� and the �coo� were clearly calls involved in competition andaggression the function of the bubbling call is not entirely clear. Females alsouttered the bubbling call more often than males, but the difference was not asimpressive as in the previous type of calls. Perhaps, the bubbling call helps themembers of a group to coordinate their activities.

Sperm Competition and Mate Guarding

Sperm competition may arise when females mate with more than one maleduring a single reproductive cycle (Parker 1984; Birkhead & Møller 1992).Although sperm competition may occur in most mating systems (for a recentreview on birds see Ligon 1999) it is likely to be intense in classically polyandrousbird species in which females mate with and provide clutches for multiple males(Oring 1986; Birkhead et al. 1987). Males in classical polyandrous mating systemsface three possible risks to their paternity: (i) fertilizations by males outside thepolyandrous group, (ii) fertilizations by males previously mated to the female, and(iii) fertilizations by other males simultaneously paired to the female (Emlen et al.1998). Because of their primary or exclusive responsibility for parental care, malesof classical polyandrous species should be under strong pressure to preventcuckoldry (Oring 1986) and indeed rates of extra-pair paternity reported forclassical polyandrous species are lower (Owens et al. 1995; Delehanty et al. 1998;Emlen et al. 1998; Dale et al. 1999) than those reported for many sociallymonogamous bird species (Birkhead & Møller 1992; Westneat & Webster 1994).A typical behaviour to prevent cuckoldry is mate guarding (Birkhead & Møller1993) and three lines of evidence suggest that male black coucals guard theirmates. (1) Males spent significantly more time close to their mate during themating phase than during the parental phase. (2) On average, males were foundcloser to their mates during the mating phase than during the parental phase.(3) Males were more likely to follow their mate when she left her perch than viceversa, suggesting that mate guarding behaviour was initiated by males rather thanfemales. Behaviours 1 and 2 could also be explained by female movement patternsbetween the different subterritories of her mates, but behaviour 3 suggests that themale tries to actively guard its mate. While this may help to ensure paternity tosome degree, the incubation pattern of black coucals limits the ability of males toeffectively guard their mates: males do all the incubation and they start incubationof the clutch as soon as the first egg is laid (Vernon 1971; W. Goymann, pers.obs.). Thus, females have the potential to sneak off and seek extra-paircopulations after they have initiated a clutch. We are currently setting up

818 W. Goymann, A. Wittenzellner & J. C. Wingfield

paternity analyses to determine to what degree extra-pair fertilizations occur inthis species.

A second way for males to increase paternity is to engage in frequentcopulations. It is difficult to assess copulation frequency in black coucals, as wewere only able to watch conspicuous copulations on perches. It is unknown towhat degree coucals copulate hidden in the vegetation. Our observations showedthat black coucals copulated during all stages of the male breeding cycle (e.g. afemale may mate with one of her mates who is feeding young while she lays aclutch for one of her other mates), suggesting that copulations may increase spermcompetition, as demonstrated for polyandrous spotted sandpipers (Oring et al.1992) or have additional social functions.

Testis size is considered as an indicator of sperm competition (for birds seee.g. Møller 1991). With regard to other bird species with a classical polyandrousmating system in which total testis mass was typically 1–2% of the body mass(Møller 1991) the value for black coucals (0.7%) was relatively low, possiblyreflecting the importance of mate guarding in this species, which is typicallynegatively correlated with testis size (Møller 1991). Compared with other tropicalbird species (Wikelski et al. 2003) testis volume of black coucals is similar togroup living and lekking species, but larger than in socially monogamous birds,suggesting an intermediate level of sperm competition.

Evolution of Polyandry

Because an individual may maximize its lifetime fitness by restricting theamount or duration of parental care there is conflict between the sexes overinvestment in parental care (Lessels 1999). A number of models have beendeveloped to explain existing patterns of offspring desertion and parental care,but the application of these models to field studies remains problematic (reviewedin Szekely et al. 1996). Earlier attempts to find a common ecological factor thatpredisposes certain species of birds to polyandry and male-only care have failed(reviewed in Erckmann 1983). Recently, Reynolds & Szekely (1997) and Owens(2002) used phylogenetic analyses to find ecological correlates of the extent ofpaternal care. Reynolds & Szekely (1997) identified migration distance as animportant correlate of male-only care in shorebirds, suggesting that paternal caredecreases as migration distance increases. However, the direction of causality ofthis result is debateable and in fact Reynolds & Szekely (1997) think that changesin parental behaviour of shorebirds have led to changes in migration distance,rather than vice versa. For black coucals, which are considered short-distancemigrants (Payne 1997) this hypothesis does not offer a valid explanation for theevolution of classical polyandry. Owens (2002) conducted a comparative analysison the family level and identified nesting density as an important factor,suggesting that male-only care evolves when nesting density is low and rematingopportunities, in particular for males, are rare. Within coucals, however, nestingdensity is certainly higher for polyandrous black coucals with male-only carethan, e.g. for monogamous coppery-tailed (C. cupreicaudus) or white-browed

819Mating System of African Black Coucals

coucals (C. superciliosus) that live in the same habitat, but provide biparental care(W. Goymann, pers. obs.). Thus, low nesting density is unlikely to explain theevolution of male-only care in black coucals. We think, that the evolution ofclassical polyandry asks for an explanation on the species level and that no singleecological hypothesis may be able to explain the occurrence of this mating systemin different species (see also Erckmann 1983).

Comparative evidence for the ancestral state of parental care suggests equalsex roles in ancestral coucals (Andersson 1995). As far as it is known, in all non-parasitic cuckoos the males incubate at night (Ligon 1999). In coucals, a male-biased incubation seems to be common during day and night (Payne 1997). Thispeculiar (and unexplained!) ancestral trait of male incubation may have facilitatedthe evolution of reduced female and increased male parental care in coucals.Andersson (1995) suggested that coucals may have further reduced female andincreased male parental care, because females were resource limited in egg laying.If males take a greater share of parental duties this would allow females to buildup reserves for a replacement or second clutch (Andersson 1995). In this context itis interesting that a recent model suggests that by strategically reducing their ownreserves females may force their mate to provide care (Barta et al. 2002). Inaddition, predation pressure on coucal nests appears to be high (W. Goymann,unpubl. data). Thus, selection could have favoured females that were able toproduce multiple replacement clutches in rapid succession. If involvement inincubation reduces female ability to produce eggs, frequent nesting failure mayselect for female emancipation of incubation, as suggested for jacanas (Jenni 1974;Butchart 2000). Unlike other coucals the black coucal has a more specializedinsect diet and breeds during the lush season of these insects (Andersson 1995).With this increase in food resources, females may have been able to lay multipleclutches for different males in quick succession, and males may have been able toraise the broods on their own, leading to a classical polyandrous breeding system(Andersson 1995).

Andersson (1995) and Ligon (1999) emphasized the importance of foodabundance for a female to rapidly produce several clutches, and for a singleparent to provision its young, respectively. While we agree that this is certainly acritical factor, it is questionable whether the males of all monogamous, biparentalcoucal species really need the assistance of their mate. The only other data forcoucals that are currently available suggest that females do not contribute a largeamount of food in Toulou (C. toulou; Frith 1975) and pheasant coucals(C. phaisaninus; Taplin & Berteaux 1992), but possibly do so in white-browedcoucals (C. superciliosus; van Someren 1956). We therefore propose as an additionto Andersson’s (1995) and Ligon’s (1999) suggestions a hypothesis, which hasbeen previously formulated for shorebirds and jacanas (e.g. Jenni 1974;Erckmann 1983). Coucals are �central place foragers� in which higher foodabundance generally reduces the foraging and territory area (Andersson 1978,1981). If a coucal species, such as the black coucal, is mainly insectivorous andbreeds during the lush season of these insects, then a relatively small territory maycontain sufficient food for a male coucal to raise his brood. This situation may

820 W. Goymann, A. Wittenzellner & J. C. Wingfield

enable the female to monopolize and control a territory that is large enough and/or of sufficient quality to support more than one male and his brood. In contrast,other coucal species depend on a broader diet including small vertebrates(Andersson 1995) and thus may need larger territories to provision their young.This situation may prevent a female from monopolizing and controlling aterritory that is large enough to support more than one male. Thus, in contrast towhat Owens (2002) has found on the comparative family level, we believe thatsmall territories and a high nesting density may be a requirement for the evolutionof classical polyandry in black coucals.

Acknowledgements

We are grateful to the Tanzania Commission of Science and Technology (COSTECH),Dr Felister Urasa from the University of Dar es Salaam, and the management of the Kapunga RiceProject for permission and support to conduct the study. We are especially grateful to WolfgangWickler from the Max-Planck-Institute for Behavioural Physiology for his continuous scientific andfinancial support. We thank Veit Eitner, David Moyer, Dieter Schmidl, Sabine Tebbich and especiallyMusa Makomba for assistance in the field, Liz and Neil Baker, Sonja and Andreas Kummerle andPetra and Peter Neubert for logistic support, Malte Andersson, Michaela Hau, Barbara Knauer, LewOring, Wolfgang Wickler and an anonymous referee for helping to improve previous versions of thismanuscript. This study was funded by grants no. Go 985/2-1 and Go 985/2-2 from DeutscheForschungsgemeinschaft (DFG), the Max Planck Society to WG and by grants OPP-9911333 andIBN-9905679 from the National Science Foundation to JCW.

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Received: November 21, 2003

Initial acceptance: January 18, 2004

Final acceptance: July 2, 2004 (M. Taborsky)

823Mating System of African Black Coucals