Musk brood parasitism 127

Musk Duck brood parasitism on Black Swans

K. Kraaijeveld1 & R. A. Mulder2

'Department of Zoology, University of Melbourne, Parkville, Vic 3010, . Current address: Department of Biology, Darwin Building, University College London, Gower Street, London WC1E 6BT, UK. 'Department of ZooLogy, University of Melbourne, Parkville, Vic 3010, Australia.

This paper describes incidences of brood parasitism of nests of Black Swans Cygnus atratus by Musk Lobata. Black Swans have a long incubation period, and as they are unlikely to exhibit rejection behaviour, they are potentially suitable as hosts for para­ sitism. Model were used to test whether the success of brood parasitism in this system is constrained by host responses (egg recogni­ tion or nest abandonment), or egg shell strength. The results showed that Black Swans readily accept foreign eggs, even when they are very different from their own. However, there was a substantial loss of weak- shelled model eggs, thought to be accidentally crushed by the swans. The relation of this to the unusually thick shell of Musk Duck eggs is dis­ cussed.

KeyWords: interspecific brood parasitism, egg recognition, egg rejection, model experi­ ments, shell thickness

Interspecific brood parasitism, or 1992). The hosts of parasitic wildfowl females purposely laying eggs in the mostly involve other wildfowl, but also nests of other , is relatively gulls (Laridae), Coots Fulica sp. and widespread among wildfowl (). ibises (Threskiornithidae). The success The behaviour has been recorded in at of interspecific brood parasitism may least 36 out of Π 6 species (25%), and is be constrained by the timing of the par­ particularly common among the asitism, and by host responses, such as (stiff-tailed ducks; Sayler nest site defence, displacement of par-

©Wildfowl & Wetlands Trust W ild fo w l (2002) 53: 127-135 128 Musk Duck brood parasitism asitic eggs, egg rejection and nest a poorly-studied species, and it is not abandonment (Sayter 1992). clear at present how important inter­ Furthermore, parasitic eggs may be specific brood parasitism is as a damaged when quickly deposited in the reproductive strategy. Attiwil et at. nest or when the host attempts to (1981) is the only other study to report puncture it (Mallory 2000). In response interspecific brood parasitism in the to these constraints, some avian brood Musk Duck. Although further studies parasites have evolved are needed, it is possible that interspe­ such as egg mimicry and strong egg cific brood parasitism by Musk Ducks shells (Davies 2000). Studies on wild­ may be relatively common, at least fowl have so far found little evidence for under certain circumstances. Musk egg discrimination among host species Ducks are unusual among wildfowl in (Sorenson 1997, Dugger et at. 1999a, that females directly feed their off­ Dugger et at. 1999b). A study of Hooded spring for a considerable amount of Mergansers Lophodytes cucullatus time after leaving the nest (Frith 1967). reported that Common Goldeneye The incubation period of Black Swans Bucephaia clangula eggs were more takes on average about 41 days likely to be at the periphery of the host (Braithwaite 1977), considerably longer clutch (Mallory & Weatherhead 1993). than that of Musk Ducks (about 24 Furthermore, parasitic species do not days, Marchant & Higgins 1990). Black seem to have evolved 'stronger' egg Swans thus offer a relatively large win­ shells than non-parasitic species dow of opportunity during which the (Mallory & Weatherhead 1990). The parasitic egg can hatch before the host lack of adaptations in relation to brood finishes incubation, compared to host parasitism in both hosts and parasites species with shorter incubation. The among wildfowl is often taken as evi­ main incubation periods of Black dence that the costs of parasitism to Swans and Musk Ducks overlap at our hosts and the benefits to the parasites study site (see Methods). Furthermore, are relatively small in species with pre­ incubation of an additional small egg cocial young, compared to those with should not pose a large extra cost to altricial young (Rohwer & Freeman the host and it would thus seem unlike­ 1989, Lyon & Eadie 1991). ly that Black Swans have evolved egg In this paper, a rather unexpected recognition abilities. Lastly, predation host-parasite combination among rates of Black Swan nests are low com­ Australian wildfowl is reported: Musk pared to those of smaller hosts. To Ducks Biziura lobata laying eggs in the assess whether Black Swans make nests of Black Swans Cygnus atratus. suitable hosts for brood parasitism by Although Musk Ducks are known to be Musk Ducks, a field experiment using brood parasites (Attiwil et al. 1981), they model eggs of different mimetic quali­ have not previously been recorded par­ ties and shell strength was undertaken. asitising Black Swans. Musk Ducks are Musk Duck brood parasitism 129

Study Area and Methods found by wading through the study area. The contents of all nests at both The study was conducted between study sites were monitored weekly. No July and October 2000 at two sites in Musk Ducks were ever recorded at central Victoria, Australia: Lake Reedy Lake. Wendouree in Ballarat (S37°33' Egg recognition experiments were E 14-3°4-9 ’ ) and Reedy Lake, near conducted at Reedy Lake during Geelong (S38°11 E14-4-°26'). The main September 2000. No experiments were incubation period for Black Swans in conducted at Lake Wendouree, Victoria takes place between early July because the swans refused to leave and m id-November and clutch size their nest, making it impossible to add varies between two and seven experimental eggs unnoticed. Seven (Kraaijeveld 2003). Lake Wendouree is a types of model eggs, differing in size, permanent lake of 238ha, with a popu­ colour and shell strength, were added lation of around 170 Black Swans who to Black Swan clutches of varying age. are present at the site throughout the White and brown eggs came from year. The swans breed mainly in beds of domestic chickens, whitish eggs came Tall Spike-rush Eleocharis sphacelate, from domestic ducks, and infertile and nests were found by searching veg­ swan eggs from the same population etation by canoe. The lake also has a were also used. To investigate the permanent population of about 20-60 effect of shell strength, we filled some Musk Ducks, which are known to breed of the brown and white chicken eggs regularly [Thomas & Wheeler 1983). with plaster of paris. Shells of swan Most egg-laying by Musk Ducks at the eggs (filled or unfilled) were used as a site occurs between September and control. The dimensions of the experi­ November (Frith 1967; K. Kraaijeveld, mental study eggs are listed in Table 1. pers. obs.). Reedy Lake is a system of Each nest only received one model egg. shallow lakes containing numerous Nests were checked two days after reed beds. The study site was an area addition of a model egg. It was of about 90ha around the perimeter of assumed that during this time both the reed beds, which only floods during partners would have had an opportunity spring. The vegetation consisted of low to reject the model eggs. All experiments rushes and narrow strips of Reed described in this paper were approved Phragmites australis water of less than by the Experimentation Ethics 50cm depth. During the study period Committee at the University of about 130 swans inhabited the area, Melbourne. while at other times of the year the To assess whether the egg shell of study area was dry and no swans were Musk Ducks is stronger than would be present. Nests were mostly located expected from its size, we followed the among strips of reeds and were easily approach of Mallory (2000), using data from Mallory et al. (1990). Linear 130 Musk Duck brood parasitism

regression was used to examine the Results relationships between egg mass and shell thickness, or egg mass and egg At Lake Wendouree 66 Black Swan shape. All waterfowl were initially nests were located, constituting 95% of included, and the residuals plotted as a all nests on the lake, and three nests histogram. A second regression was (5%) contained a Musk Duck egg. These then performed on all waterfowl, eggs were greenish white in colour and except the Musk Duck, to generate pre­ unmarked, slightly lighter in colour dictive equations for egg shape and than Black Swan eggs, and consider­ shell thickness based on egg mass. ably smaller (Table 1). One was found in The values for the Musk Duck egg were a clutch of five swan eggs, 21 days after then compared to the 95% confidence the clutch had been completed. The intervals of the predicted value. Data on egg was still present in the nest 17 days egg characteristics were loge trans­ later, after the swan eggs had hatched formed and tested for normality. and the cygnets had left the nest. The egg was cold and contained a fully developed Musk Duck embryo. The second Musk Duck egg was found in a clutch of four swan eggs, 20 days after clutch completion. This egg was still

Table 1. Dimensions (mm± SD] of different types of eggs found in nests of Black Swans and of those used in egg recognition experiments (the latter are marked with *). All eggs are plain in colour.

Egg Type Length Width Colour

Black Swan (n=33) 106±3 67+2 Pale Green

Musk Duck (n=2) 58±1 47+7 Pale Greenish-white

White Ibis (n=1 ) 68 47 White

*Chicken (n=16) 57±2 43±1 Brown or White

*Duck (n=12) 62±3 47±1 White Musk Duck brood parasitism 131 present in the nest 14 days later. The monitored. As all of the study area at swan eggs hatched a further seven this site is easily accessible, it is likely days later, so the Musk Duck egg could that all nests were located. None of the have been incubated for over 21 days. nests at Reedy Lake contained Musk The eventual fate of this egg was Duck eggs. unknown, but a Musk Duck chick unac­ The results of the egg recognition companied by a parent was observed experiments are summarised in Figure about 600m from the nest on the first 1. None of the experimental nests were day the swan pair were seen with deserted after addition of the model cygnets away from the nest. The third egg. All model eggs that remained in Musk Duck egg was found with a clutch the nests after two days were warm, of two swan eggs. This nest was found indicating that they had been incubat­ after the clutch was completed, but ed. None of the model eggs had been judging from the hatching date it was pushed outside the nest cup or buried seven days old when found. A week into the nest material. The percentage later the egg had disappeared. Thus the of normal chicken eggs remaining in Musk Duck cannot have been in the the nest after two days was low, but nest for longer than 15 days. The increased significantly when eggshells clutches of swan eggs in all the nests filled with plaster were used (Fisher remained intact and none of the nests Exact test, P<0.0001], Plaster-filled were deserted after being parasitised. chicken eggs did not differ significantly At Reedy Lake, 31 nests were found and from control swan eggs in their likeli-

9 8 100 r

» 80

cn 60 □ Normal

m 40 16 ■ Plaster filled

cć 20 à?

White Brown Duck Swan chicken chicken

Egg type

Figure 1. Percentage of experimental eggs remaining in the nests of Black Swans two days after addi­ tion. Sample sizes are indicated above the bars. No plaster-filled duck eggs were used. 132 Musk Duck brood parasitism hood of remaining in the nest. The From this equation, a 128g egg (the slightly higher percentage of unfilled weight of an average Musk Duck egg) is duck eggs remaining in the swan nests predicted to have a shell thickness of compared to unfilled chicken eggs was 0.49mm, with a 95% confidence interval not significant and probably due to their on the prediction of 0.37 - 0.65mm. The stronger shell. There was no significant average shell thickness of a Musk Duck difference between unfilled chicken egg is 0.70mm [Mallory et at. 1990), eggs of different colour in their likeli­ which falls outside this confidence hood of remaining in the nest. interval, indicating that it is significant­ Figure 2 shows the residuals of the ly thicker than expected for its mass. A regression of egg shell thickness on similar analysis on egg shape showed egg mass for all waterfowl. The egg of that the shape index for the Musk Duck the Musk Duck has a large positive egg is not different from the expected residual, second only to that of the value. Egg shape can be predicted from Hooded Merganser. When Musk Duck egg mass by the equation: is removed from the regression, shell thickness can be predicted from the Loge shape = 0.096+ 0.059 (Loge mass); egg mass by the equation: R2=0.44, F1,120=93.90, P<0.001

Loge thickness = -2.847 + 0.440 (Loge mass); From this equation, a 128g egg is R2=0.77,F1120=408.9, P<0.001 predicted to have a shape index of 1.462, with a 95% confidence interval

35 30

» 2 5 0 § 20 1 15 ¿ 10 5

0 -0.3 -0.2 -0.1 0 0.1 0.2 0.3 0.4 0.5 0.6 Residual

Figure 2. Histogram of residual values from the regression of egg shell thickness on egg mass for 122 species of waterfowl [data from Mallory ef aí. 1990). The Musk Duck is indicated with an asterix. Musk Duck brood parasitism 133 on the prediction of Ί.35 - 1.58. The smaller potential hosts, the observed shape index of a Musk Duck egg is incidences of parasitism in this study 1.503 (Mallory et al. 1990), which falls appear not to have occurred within the inside this confidence interval, indicat­ requisite time window. It has also been ing that the shape of a Musk Duck egg demonstrated that the shell of Musk is not significantly different from that Duck eggs are strong enough to avoid predicted. being crushed by an incubating swan, and is substantially thicker than Discussion expected for its mass when compared to other waterfowl. Without further At first sight, the disappearance of study of the basic biology of the Musk experimental eggs from Black Swan Duck, it remains unclear whether thick nests seems consistent with anti-para- shells produced by the species are an sitic behaviour. However, many of our evolutionary to parasitism of model eggs had thin shells (the shells Black Swans, or are a by-product of of chicken eggs are generally about some other function. 0.33- 0.36mm thick, Verna et at. 1998; It is possible that incidences of par­ Nwosu et al. 1987) and probably disap­ asitism of Black Swans at the study site peared because they were accidentally are due to a lack of nests of other crushed by the incubating swans. This hosts. Previously, Musk Ducks have suggestion was supported by the fact been recorded parasitising Pacific that when similar model eggs filled Black Duck Anas superciliosa, Grey Teal with plaster were added, these were Anas gibberifrons, Hardhead Aythya aus­ accepted by the swans. This highlights tralis, Pink-eared Duck the caution required when interpreting membranaceus, Blue-billed Duck and evidence of egg-recognition or anti- Dusky Moorhen Gallinula tenebrosa parasitic behaviour. The study suggests (Attiwil et al. 1981 ). Of these, the Pacific that Black Swans did not display egg Black Duck and the Dusky Moorhen recognition behaviour, even when pre­ breed commonly at Lake Wendouree, sented with model eggs that were very while the Blue-billed Duck breeds in different from their own. In order to small numbers (Thomas & Wheeler have any chance of hatching, the para­ 1983). As many of these were observed sitic egg needs: (i) to be deposited in breeding concurrently with Black the host nest within the first 17 days of Swans, it is unlikely that no other host the start of incubation of the host nests were 'available'. clutch, and (ii) to have a shell that is The Black Swan, Musk Duck, and strong enough to withstand the weight experimental eggs that were added to of a Black Swan. Even though the win­ nests were plain in colour. The lack of dow of opportunity for parasitism of a markings might constrain recognition swan nest is long compared to that of of parasitic eggs by the host. However, 134- Black Duck brood parasitism this seems unlikely, as the eggs used in Dept, of Natural Resources and our experiment also differed from Environment for permission to conduct Black Swan eggs in colour and size. this study at Lake Wendouree and Diederik Chrysococcyx caprius Parks Victoria for permission to work at parasitise several species of Weavers Reedy Lake. This research was sup­ (Davies 2000), and in this host-parasite ported by grants from the Holsworth system both have unmarked eggs and Wildlife Research Fund and the Stuart the host is able to recognise parasitic Leslie Research Fund. Femmie eggs. Kraaijeveld-Smit and two anonymous The success of brood parasitism of referees provided useful comments on Black Swans by Muck Ducks as a the manuscript. reproductive strategy appears to be facilitated by host egg acceptance, and References may also depend on egg strength and the timing of parasitism. However, Attiwil, A.R., Bourne, J.M. & Parker, S.A. unlike the precocial young of most 1981. Possible nest-parasitism in the other waterbirds, Musk Duck young Australian stiff-tailed ducks (Anatidae: appear to be far more dependent on Oxyurini). Emu 81:4-1 -42. parental care once they leave the nest Braithwaite, L.W. 1977. Ecological studies of (Frith 1967), and females are known to the Black Swan. I. The egg, clutch and feed the young for several weeks. As incubation. Australian Wildlife Research 4: the majority of their potential hosts, 59-79. including Black Swans, do not exhibit Davies, N.B. 2000. , cow/ and such behaviour, it would seem that the other cheats. T & A D Poyser, London. survival chances of the parasitic duck­ ling would be low unless females Dugger, B.D., Blums, P. & Fredrickson, L.H. collect the ducklings once the host has 1999a. Host response to brood parasitism in two species of . Wildfowl 50: finished incubation. Such retrieval of 69-76. young from parasitised nests would be unique among brood parasites (Davies Dugger, B.D., Bollmann, L.C. & 2000) and has not been observed. Fredrickson, L.H.· 1999b. Response of female Hooded Mergansers to eggs of an Acknowledgements interspecific brood parasite. Auk 116: 269-273.

We would like to thank the mem­ Frith, H.J. 1967. Waterfowl in Australia. bers of the Ballarat Field Naturalists, in Angus & Robertson, Sydney. particular John and Elaine Gregurke, Kraaijeveld, K. 2003. Breeding ecology and Carol Hall, Brian, Kevin and Joan the evolution of mutual ornamentation in Andrews for their help in field. We the Black Swan. PhD thesis, University of thank the Ballarat City Council and the Melbourne, Australia. Black Duck brood parasitism 135

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