VOL. 14 (3) SEPTEMBER 1991 75

by IAN ROWLEY, CSIRO Division of Wildlife & Ecology, L.M.B. 4, P.O. Midland, W.A. 6056

Summary At least six members of the genus Malurus carry brightly coloured petals in a form of display - M. cyaneus, M. splendens, M. lambeni, M. melanocephalus, M. elegans and M. leucopterus; petal­ carrying is reported here for the first time for the last two species. All species of Malurus are strongly sexually dimorphic and all that carried petals (except for one female) were males in full nuptial . Some of the petals carried matched the plumage of the male, whereas others contrasted strongly; there appeared to be no relationship between choice of petal and rarity. It is suggested that petal-carrying enhances the attractiveness of the male to females. Introduction Communication between birds is usually by sight or sound, the third sense, smell, rarely being important. Visual signals, with or without an auditory component, tend to be stereotyped and characteristic of particular contexts (agonistic, sexual, parental). These specialised signals or displays usually involve postures which, whilst emphasising the size, colour, or intent of the , make use only of the physical attributes of the . Most foraging birds only use their own physical equipment (beak, claws etc.) in the gathering or processing of food. However, a few species have developed the ability to use extraneous items to facilitate their foraging, to extract hidden grubs, to 'fish' for termites, to open shellfish, or to break the shells of tough eggs; such activities, 'tool-using', have been summarised by Boswall (1985). In a similar way, certain species of bird have amplified their displays by incorporating extraneous items, in particular, brightly coloured petals. The most spectacular and best described cases are the performances of various bowerbirds in the Australasian endemic family Ptilonorhynchidae, in particular, that of the male Satin Bowerbird Ptilonorhynchus violaceus, which decorates its bower with a variety of items, including coloured petals (Marshall 1954; Borgia et al. 1987). It is less well known that members of another Australasian endemic family, the Maluridae, sometimes display with coloured petals or berries held in their bills. Hindwood (1948) drew attention to this behaviour, quoting his own observations, those of Chisholm (1934) and an account by Chaffer (in litt.) that would appear to be the earliest description (5 June 1922). Hindwood's note stimulated Loaring (1948) and Jack (1949) to report their observations and he published another of his own in 1951. Since then, Rowley (1965, 1991), Strong & Cuffe (1985), Hughes & Hughes (1988) and Strong (1990) have added further examples. In this paper I record, for the first time, petal-carrying by the Red-winged Fairy­ wren Malurus elegans and the White-winged Fairy-wren M. leucopterus, bringing to six the number of species in the genus Malurus that have been recorded carrying petals or berries in a display. I also elaborate on 86 instances of petal-carrying by the Splendid Fairy-wren M. splendens recorded during a long-term study of that species (Rowley & Russell 1990a). Results Previous descriptions of petal-carrying by fairy-wrens have reported opportunistic observations of unmarked or unidentified . This paper describes petal-carrying AUSTRALIAN 76 ROWLEY BIRD WATCHER

by three species of Malurus, many members of which were individually identifiable colour-banded birds, whose social status, nesting responsibilities and territorial affiliations were known. Individual instances are reported in full forM. elegans (N =8) and M. leucopterus (N=8); the 86 instances by M. splendens are discussed in relation to the promiscuous mating strategy that appears to be exercised by this species (Rowley & Russell 1990b).

Red-winged Fairy-wren During a ten-year study of this species at Smith's Brook (Rowley et al. 1988), petal­ carrying was seen eight times: 1. 24 November 1980, 1800 h; nest 80/09 had hatched that day and the two females and three males in the group were in a state of excitement, noisy and carrying food. One fully plumaged male carried a yellow petal for about 10 metres during this performance, and, although unidentified, he was thought to have belonged to the group tending the nest. 2. 30 December 1981, 1100 h; F582 was lining her nest (81129) escorted by M999, her fully plumaged mate, who was carrying a yellow petal. 3. 26 October 1984, 1730 h; F649 became very excited and noisy whilst we were trying to find her nest (which contained two eggs); two males belonging to her group flew to a nearby branch, one fully plumaged (M618) was carrying a yellow petal with which he postured at the female; F649 began Wing-fluttering (a usual malurid pre-copulatory display) and flew to the branch on which the two males were perched; M618, the older bird which had been seen to mate with F649 three days earlier, took no notice of her now appearing to be engrossed in his petal display; M7764, a one-year-old male, mounted the soliciting F649 who was his mother. 4. 5 November 1984, 1400 h; several unidentified fully plumaged males were attending F6477 closely, one of them was carrying a white petal. 5. 28 September 1986, 1210 h; an unhanded fully plumaged male was seen carrying a yellow petal in the company of a banded (but unidentified) female. All the local males were colour-banded so that this male must have been philandering - seeking a mating outside his social group (Rowley & Russell 1990b). 6. 31 October 1986, 0830 h; an unidentified fully plumaged male displayed with a yellow petal to an unidentified female in thick cover. 7. 6 November 1988, 1200 h; fully plumaged M62209 carried a large yellow Hibbertia cuneiformis petal which he presented to an unhanded female that could have been his new partner; both birds disappeared into thick cover and when they reappeared a minute later, the male was no longer carrying the petal. 8. 8 November 1988, 1103 h; an unhanded fully plumaged male, that was carrying a yellow Hibbertia cuneiformis petal, approached an unidentified female that appeared to take no notice. The male hopped to a parallel branch and, facing the female, again offered the petal to her; again she showed no response.

White-winged Fairy-wren Eight cases of petal-carrying have been observed in this species currently being studied at Pippidinny, W.A. (31 "35'S, 115 °41 'E; Rowley, unpublished). 1. 23 October 1987, 0800 h; E.M. Russell watched an unhanded fully plumaged male carrying a pink Erodium sp. petal. 2. 9 December 1987, 1l30 h; whilst I was searching for a fledgling, fully plumaged M863 circled the area carrying a large yellow petal. · VOL. 14 (3) SEPTEMBER 1991 Petal-carrying by Fairy-wrens 77

3. 2 July 1988, 1435 h; I watched an unhanded fully plumaged male and two unhanded females; the male performed Sea Horse Flight (see below under splendens) and when he landed was seen to be carrying a purple petal. 4. 7 July 1989, 1200 h; whilst I was trying to locate a new group of M. leuconotus, a banded fully plumaged male (M863) landed 3m from me, carrying a narrow strip of purple petal (he was philandering as he was known to belong to a group 200m to the west where he had a nest with a clutch nearing completion; there was another, unhanded, fully plumaged male in the territory under observation). 5 & 6. 18 November 1989; 0800 h; whilst I was watching a nest being lined, a fully plumaged male (Mll6) from the next-door territory (where he was tending four three-week-old young) and an unhanded fully plumaged male from the opposite direction, in tum flew to the nest area, each of them carrying blue petals (that matched their plumage). Male 116 did not stay long and returned to his family; however, the unhanded male stayed for 10 minutes carrying his petal all the time and once perching beside the blue plastic tape with which I had flagged the area to be searched for a nest. 7. 2 June 1990, 1210 h; fully plumaged male M116 was encountered outside his territory, pursuing five or six brown birds. He was carrying a small piece of white petal (est. 10x5 mm: the only candidate flowering species was Hemiandra pungens). 8. 18 September 1990, 1435 h; by using 'playback' of recorded calls, I was trying to persuade birds to show themselves and to be identified. Male M116 from the neighbouring territory flew in carrying a small piece of pale blue or white petal and proceeded to chase a brown bird for ten minutes before returning to his territory. At this time of year the variety of candidate petals is too numerous to permit identification.

Splendid Fairy-wren In the course of a continuing long-term study on Gooseberry Hill, W.A. (Rowley & Russell 1990a) petal-carrying has been observed 86 times, 49 of which involved colour-banded birds that were individually identifiable and whose age, status and territory were known. In fifteen of these events, the actor was not identified, so that we do not know whether he was resident or intruder. On twenty-two occasions the actor was seen to be unhanded and known to be intruding into a territory where the group members were all colour-banded. A further 26 actors were recognised as philandering, colour-banded individuals. This leaves 23 colour-banded individuals that carried petals within their own territory boundaries; one of these was a female which, when disturbed from her nest, performed Rodent-run display (Rowley 1962) to a Hibbenia bush where she picked a yellow petal and then continued to Rodent-run carrying the petal. Of the others, 17 were the senior males in their group and five were helper males. The months when petal-carrying by M. splendens was observed and the months when the first eggs of 680 clutches were laid over 15 years show a clear correlation (Figure 1). Furthermore, at least 56% of the 78 cases took place during the Fertilisation Period (sensu Birkhead 1983) of the female - namely less than 10 days before the third (and final) egg was laid; this figure was probably higher, but the dates for eight events were imprecise. Males engaged in petal-carrying usually erected their body feathers and, in particular; fanned their light blue face feathers (Figure 2) to give a characteristic display -the Face-Fan. When travelling with a petal in their bill, many birds appeared to fly with an impeded flight because the body feathers were still largely erected. Sometimes, it appeared that the individual was progressing horizontally with the body AUSTRALIAN 78 ROWLEY BIRD WATCHER held nearly vertical; the performance was dubbed the Sea-Horse Flight and forward progress was often in a series of i=z aoj a. 0 70 undulations. :::!! Petal-carrying males were in a state of ~ 60 t o. soi great excitement and making themselves ~ 40 I very conspicuous. Several times they were >a: 30 l seen carrying petals whilst pursuing females and, on 12 occasions, the petals -~ 20,,01 II I appeared to be presented to the female. ~ 0 +---,.]_.....-""""-. ..._...... L.JI!III-__..._. ...,....-j The females responded with a Wing­ A S 0 N Fluttering display (pre-copulatory) at only MONTHS three of these events and at none was 200 b. copulation observed (but see M. elegans ...r above). 5 160 :::!! Observations of petal carrying by M. ~ 120. splendens were made by several different 0. ~ 80 people, not all of whom remembered to (/) w record the colour of the petal involved (17 z cases). Of the 69 cases where the colour of the petal is known, 34 were rated pink, A 0 N 25 purple, seven blue, two yellow and one MONTHS white. The Western Australian heathland Figure l(a) Monthly incidence of petal­ contains such a variety of species and carrying (N =86) by Malurus colour that any attempt to apportion splendens. choice by the birds is unrealistic; there (b) Clutch initiation by month in M. was no noticeable change in colour splendens on Gooseberry Hill, preference with months and 85 % of the 1973-1989 (n=680). petals carried were in the pink-purple range although more than 50% of available petals were yellow (esp. Hibbertia spp.). Identified sources of pink-purple petals carried by M. splendens were: Patersonia occidentalis, Hovea pungens, Echium plantagineum, Ihysanotus spp., Oxalis purpurea, Drosera spp., Diplopeltis huegelii, Melaleuca scabra, Tetratheca hirsuta.

(a) (b)

--~··...... __. _..,4-----

Figure 2(a) Male Malurus splendens carrying a petal. (b) Male Malurus splendens fanning his face feathers. Drawn by Belinda Brooker from photographs VOL. 14 (3) SEPTEMBER 1991 Petal-carrying by Fairy-wrens 79

Table 1 The colour of petals carried by various members of the.genus MalurusB- Species Colour N Reference M. cyaneus Superb Fairy-wren Yellow 4 Hindwood I948 7 Rowley I965 M. splendens Splendid Fairy-wren Pink I Loaring I948 Pink Purple 20 Blue 7 Rowley this paper Yellow "]2 White I M. Iamberti Variegated Fairy-wren Yellow Strong & Cuffe I985 Yellow R. Major in !itt. M. elegans Red-winged Fairy-wren Yellow Rowley this paper White iJ M. melanocephalus Red-backed Fairy-wren Orange I Jack I949 Red 2 Chisholm I934, Rowley I99I

Red Hughes & Hughes 1988 Yellow i~ (and ·in !itt.) M. leucopterus White-winged Fairy-wren Purple Blue Yellow !J Rowl

•for plumage colours see plates in Slater et al. I986, pages 247 & 249. bin 3 out of 4 cases, the bird carried a red berry.

Discussion The significance of petal-carrying by fairy-wrens is difficult to interpret. If it were part of an important stereotyped display, one would expect it to have been observed much more often in a long-term study such as ours (Rowley & Russell 1990a) because it is very conspicuous. All the well-studied species of Malurus are sedentary, territorial and long-lived with social bondings that tend to persist for many years. The reason why petal-carrying is rarely seen may be that matings between established group members require few courtship preliminaries and copulation is brief and rarely seen. Recent electrophoretic analysis of blood from 91 nestlings and 63 adult M. splendens has shown that very few of those progeny could have been fathered by the male(s) that lived in the group which was raising the nestlings (Brooker et al. 1990). Such cuckoldry was obviously the result of Extra-Pair Copulation; as analytical techniques improve, such events are being recognised increasingly often in many species. The surprisingly high frequency with which Extra-Pair Fertilisations have been recorded, the extreme sexual dimorphism found throughout the genus and the fact that petal-carrying is generally performed by fully plumaged males, suggest that competition for Extra-Pair Copulations may occur between males and that, in that context, petal-carrying may enhance either the attractiveness of philandering males or the intensity of their performance, either of which may influence mate choice by the female. AUSTRALIAN 80 ROWLEY BIRD WATCHER

That petal-carrying is occasionally performed by resident males within their own territories, as well as by philanderers, at first appears to contradict the sexual competition hypothesis. However, multi-male groups are common in Malurus and there may be sufficient competition within such families to make petal-carrying worthwhile. Moreover, many of the cases involving resident males (M. splendens x23; M. elegans x4; M. leucopterus x1) took place in situations where there was general excitement prevailing, related to other than sexual activity (e.g. nestlings hatching; young being banded; nest searching), and the performance of petal-carrying may well have included an element of displacement activity - as was certainly the case when the female M. splendens carried a petal during her Rodent-run display (see above). Satin Bowerbirds have been shown to choose certain colours in preference to others when selecting petals with which to decorate their bowers. This choice has been discussed at length by Borgia et al. (1987) in relation to the rival theories of aesthetic preference (Darwin 1871; Diamond 1982) and matching (Marshall 1954; Morrison­ Scott 1937) and in relation to their own results, namely that the petals were selected for their rarity value. However, these ideas relate to inanimate objects incorporated into a static arrangement and are not necessarily relevant to a petal that is being carried by a bird as part of a dynamic display. Each of the six Malurus known to carry petals appears to show certain colour preferences as are shown in Table 1. Some of these colours appear to match the male plumage (M. splendens, M. melanocephalus and M. leucopterus), whereas others, such as the bright yellow, contrast strongly (M. cyaneus, M. Lamberti and M. elegans) so that no definite conclusion about the basis of petal choice in Malurus is possible. There are still several other species for which we have no records, one of which has been extensively studied without petal-carrying being recorded (M. coronatus; Rowley 1988) and so I end with a request for people to keep their eyes open and to report any cases that they may see.

Acknowledgements I thank Craig Bradley, Michael and Lesley Brooker, Graeme Chapman, Joe Leone, Bob and Laura Payne and Eleanor Russell, all of whom contributed observations. Belinda Brooker drew Figure 2 from photographs. Michael Brooker and Eleanor Russell commented helpfully on the manuscript.

References Borgia, G., Kaatz, I.M. & Condit, R. (1987), 'Flower choice and bower decoration in the Satin Bower­ bird Ptilonorhynchus violaceus: a test of hypotheses for the evolution of male display', Anim. Behav. 35, 1129-1139. Boswall, J.R.H. (1985), 'Tools, use of, in Campbell, B. & Lack, E. (Eds), Dictionary of Birds, p. 599, Poyser, Calton. Brooker, M.G., Rowley, 1., Adams, M. & Baverstock, P.R. (1990), 'Promiscuity- an inbreeding avoidance mechanism in a socially monogamous species?', Behav. Ecol. Sociobiol. 26, 191-199. Darwin, C. (1871), The Descent ofMan and Sexual Selection in Relation to Sex, John Murray, London. Diamond, J. (1982), 'Evolution of bower-birds' bowers: animal origins of the aesthetic sense', Nature, Lond. 297, 99-102. Hindwood, K.A. (1948), 'The use of flower petals in courtship display', Emu 41, 389-391. -- (1951), 'Flo~er petals and bird display', Emu 50, 208-209. Hughes, P. & Hughes, B. (1988), 'Notes on berry and petal display by the Red-backed Wren at Widgee, south-east Queensland', Sunbird 18, 52-53. Jack, N. (1949), 'Wren with flower', Emu 49, 143. Loaring, W.H. (1948), 'Splendid Wren with flower petal', Emu 48, 163-164. Marshall, A.J. (1954), Bower-birds and their Displays and Breeding Cycles, Oxford University Press, Oxford. VOL. 14 (3) SEPTEMBER 1991 Petal-carrying by Fairy-wrens 81

Morrison-Scott, T. (1937), 'Experiments with colour vision in the Satin Bower-bird (Ptilonorhynchus violaceus) with other observations', Proc. Zoo/. Soc. Lond. 1937, 41-49. O'Donald, P. (1983), 'Sexual selection by female choice', in P. Bateson (Ed.), Mate Choice, pp. 53-66. Cambridge University Press, Cambridge. Rowley, I. (1962), ' "Rodent-run" distraction display by a , the Superb Blue Wren Malurus cyaneus (L)', Behaviour 19, 170-176. -- (1965), 'The life history of the Superb Blue Wren Malurus cyaneus', Emu 64, 251-297. --(1988), The Purple-crowned Fairy-wren- an RAOU Conservation Statement, RAOU Report 34, RAOU, Melbourne. - - (1991) , 'Petal-carrying by Red-backed Fairy-wren', Sunbird 21, in press. - - & Russell, E. (1990a, 'Splendid Fairy-wrens: demonstrating the importance of longevity', in Stacey, P.B. & Koenig, W.D. (Eds), Cooperative breeding in Birds, pp. 1-30, Cambridge University Press, Cambridge. -- & -- (1990b), ' "Philandering" - a mixed mating strategy in the Splendid Fairy-wren Malurus splendens', Behav. Ecol. Sociobiol. 27, 431-437. -- , -- , Brown, R. & Brown, M. (1988), 'The ecology and breeding biology of the Red- winged Fairy-wren Malurus elegans', Emu 88, 161-176. Slater, P., Slater, P., & Slater, R. (1986), The Slater Field Guide to Australian Birds, Rigby, Sydney. Strong, M. (1990), 'Furgling by Red-backed Fairy-wrens', Sunbird 20, 37-38. -- & Cuffe, E. (1985), 'Petal display by the Variegated Wren', Sunbird 15, 71. Received 15 October 1990 •