Cooperative breeding, mate guarding, and nest sharing in two parrot ...

J Ornithol (2009) 150:791–797 DOI 10.1007/s10336-009-0400-8

ORIGINAL ARTICLE

Cooperative breeding, mate guarding, and nest sharing in two parrot species of New Caledonia Jo¨rn Theuerkauf Æ Sophie Rouys Æ Jean Marc Me´riot Æ Roman Gula Æ Ralph Kuehn

Received: 15 July 2008 / Revised: 16 February 2009 / Accepted: 10 March 2009 / Published online: 3 April 2009 Ó Dt. Ornithologen-Gesellschaft e.V. 2009

Abstract We provide evidence for cooperative breeding in two endemic parrot species of New Caledonia, the New Caledonian Parakeet (Cyanoramphus saisseti) and the Horned Parakeet (Eunymphicus cornutus). We intensively monitored 11 breeding attempts in two nests of New Caledonian Parakeets over 5 years, and noticed that two males of different size fed the female and the chicks in

each nest. During one breeding attempt, the larger male guarded the female and the smaller male tried to copulate with her inside the nest. Genetic analyses showed that males shared paternity. During 17 breeding attempts in 11 Horned Parakeet nests, we observed two pairs sharing a nest on one occasion but we never saw feeding helpers. Keywords Communal breeding Cooperative polyandry Cyanoramphus Eunymphicus

Communicated by T. Friedl. J. Theuerkauf R. Gula Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679 Warsaw, Poland e-mail: [email protected] S. Rouys Conservation Research New Caledonia, B.P. 2549, Noumeá Cedex 98846, New Caledonia e-mail: [email protected] S. Rouys LIVE, Universite´ de la Nouvelle-Cale´donie, B.P. 4477, Noumeá Cedex 98847, New Caledonia J. M. Me´riot Parc Provincial de la Rivie`re Bleue, Direction de l’Environnement, Province Sud, B.P. 3718, Noumeá Cedex 98845, New Caledonia e-mail: [email protected] R. Kuehn Unit of Molecular Zoology, Department of Animal Science, Life Science Centre, TU Mu¨nchen, Am Hochanger 13, 85354 Freising, Germany e-mail: [email protected] J. Theuerkauf (&) 45 rue M. Herzog, Noumeá 98800, New Caledonia e-mail: [email protected]

Introduction Cooperative breeding is unevenly distributed across bird taxa, and species of cooperative clades are usually poor migrants (Cockburn 2003). This probably contributed to most islands being colonised by non-cooperative taxa, which occasionally evolved cooperative behaviour (Cockburn 2003). In New Caledonia, the only species known to be a cooperative breeder is the flightless Kagu (Rhynochetos jubatus), which belongs to a cooperative clade (Cockburn 2006; Theuerkauf et al. 2009). Within the parrot family, reports of cooperative breeding are scarce (Aramburu´ 1996; Eberhard 1998; Brightsmith 1999; Heinsohn and Legge 2003; Ekstrom et al. 2007; Taylor and Parkin 2008). Today, only 5% of parrots are known to be cooperative breeders (Cockburn 2006), but this low percentage might be a result of parrots being rarely studied in the wild in comparison to other groups. In New Caledonia, the Uvea Parakeet (Eunymphicus uvaeensis) is the only of four parrot species which breeding biology is known (Robinet and Salas 1999). This endemic species is not a cooperative breeder. The endemic subspecies of the Rainbow Lorikeet (Trichoglossus haematodus deplanchii) has not been studied but subspecies from Vanuatu and Australia are not

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cooperative breeders (Ulrich et al. 1972; Waterhouse 1997). Although Horned Parakeets (Eunymphicus cornutus) and New Caledonian Parakeets (Cyanoramphus saisseti) have been considered endangered since 2000 and near threatened since 2002, respectively (IUCN 2008), their breeding biology has not been studied previously. In this paper, we provide evidence for cooperative breeding in the New Caledonian Parakeet and indications for cooperative breeding in the Horned Parakeet.

Methods Between 2002 and 2008, we followed parakeets in rainforests of the Rivie`re Bleue Park (22°3–120 S, 166°33–460 E) and of the Grandes Fouge`res Park (21°37–380 S, 165°45– 460 E) to find their nests. We found three nests (tree hollows) of New Caledonian Parakeets in the Rivie`re Bleue Park, five tree hollow nests of Horned Parakeets in the Grandes Fouge`res Park and six ground nests (hollows between rocks) of Horned Parakeets in the Rivie`re Bleue Park. We installed infrared illuminator cameras (Sony 1/300 CCD image sensors) and Electret mini microphones with integrated SMD amplifiers (Henri Electronic, Germany) in two New Caledonian Parakeet nests and two Horned Parakeet nests. The cameras and microphones then remained continuously in the nests. We recorded nest images either on VHS recorders (Panasonic NV-HV55, from 2002 to 2007) or digital video recorders (Archos 504 and Archos 700, since 2007), which were placed in a waterproof box within 25 m of the nest (method similar to that described by Pierce and Pobprasert 2007). We watched recorded films at 36-times speed on a TV (VHS recorder) or at 24times speed on a computer (digital recorder) to document the behaviour of the parakeets. To assess the contribution of males in food provision, we counted the number of times that a male fed the female or the chicks. We distinguished males and females of New Caledonian Parakeets by their size (about 27 cm for males and 25 cm for females) and behaviour (e.g. copulation attempts and vocalisation). Combined with size differences, each individual had a unique way of climbing down to the nest bottom and could therefore be recognised individually on most occasions. We could confirm these identifications when the birds where moulting and each had different bare patches. We decided not to band the breeding birds as adult parakeets can easily die of stress (Elliott et al. 1996). We could not install cameras on some nests, so we used binoculars to observe parakeets at these nests and checked inside the nest weekly. We documented a total of 11 breeding attempts in 3 nests for New Caledonian Parakeets and 17 breeding attempts in 11 nests for Horned Parakeets. Of these, we video-monitored 10 breeding attempts of New

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Caledonian Parakeets over 8,350 h in two nests, and two breeding attempts of Horned Parakeets over 160 h in two nests. Additionally, we directly observed four other breeding attempts of Horned Parakeets over 420 h. We fitted chicks with harness-mounted backpack radiotransmitters (Sirtrack, New Zealand, and Biotrack, UK) about 1 week before they fledged. Transmitters (including harnesses) weighed 1.2–3.1 g (on eight New Caledonian Parakeet chicks that weighed 69–96 g) and 6.3 g (on four Horned Parakeet chicks that weighed 160–180 g). Harnesses (Sirtrack) were equipped with weak links as described in Karl and Clout (1987). These links are supposed to release the transmitter from the bird once a cotton string is ripped or has rotted. We located fledged parakeets by radio-tracking and directly observed the behaviour of the fledglings and their parents. We radio-tracked and observed New Caledonian Parakeet fledglings over 200 h and Horned Parakeet fledglings over 120 h. While fitting transmitters on nestlings, we collected feathers of 11 New Caledonian Parakeet chicks for genetic analyses. We assume the genetic sample to be random since the mortality of chicks before sampling was low (Table 1) and we sampled one to two chicks per breeding attempt. To determine their sex, we used the molecular genetic method described by Fridolfsson and Ellegren (1999), which is based on the detection of a constant size difference between CHD1W and CHD1Z introns amplified via polymerase chain reaction (PCR). We repeated the sexing of each individual three times and considered only the ten individuals that provided consistent results. We tested the accuracy of this genetic sexing on the feathers of six males and four females of captive New Caledonian Parakeets. The sex of these ten birds kept at the Parc Zoologique et Forestier in Noumeá, New Caledonia, was known before genetic sexing. All captive individuals were correctly sexed in all three repetitions. To infer the number Table 1 Mean (with range) clutch size, number of hatchlings, chicks fledged and number of chicks sampled for genetic analyses of 11 breeding attempts of the New Caledonian Parakeet (Cyanoramphus saisseti) and 17 breeding attempts of the Horned Parakeet (Eunymphicus cornutus) New Caledonian Horned Parakeet Parakeet Clutch size

3.6 (2–5)

3.4 (2–4)a

Number of chicks hatched

2.5 (0–4)

2.8 (0–4)a

Number of chicks fledged

2.1 (0–4)

1.9 (0–4)a

Number of genetic samples

1.6 (0–2)

–

Number of breeding attempts/ nests with genetic samples

7/2

–

a

Excluded the two breeding attempts in the shared nest with five eggs and five chicks fledged, and another breeding attempt that was predated before the clutch was complete

J Ornithol (2009) 150:791–797 Table 2 The most likely number of parents in the two New Caledonian Parakeet nests estimated by the program PARENTAGE was one female and two males PMode The proportion of the modal value in 1,000 simulations

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Family

Nest 1 Nest 2

Parents

Initial number of parents

Estimated number of parents Mean (±SE)

Minimum

Maximum

Mode

PMode

Mother

6

1.45 (±0.02)

1

3

1

0.551

Father

6

2.61 (±0.02)

1

5

2

0.513

Mother

4

1.03 (±0.01)

1

2

1

0.971

Father

4

2.39 (±0.02)

1

4

2

0.609

of paternal genotypes in each of the two New Caledonian Parakeet nests, we genotyped the samples using the seven microsatellites Cfor0809, Cfor1415, Cfor1819, Cfor2021, Cfor2627, Cfor2829 and Cfor3031 transferred from the Chatham Parakeet Cyanoramphus forbesi (Chan et al. 2005). We entered information from all loci simultaneously into the programme PARENTAGE version 1.0 (Emery et al. 2001). Each nest was analysed separately by setting the initial probabilities for the number of potential parents as the number of chicks sampled in each nest. We assumed that the probability of having more than one mother per nest was low (gamma distribution with a shape parameter of 1 and a mean of 0.005). For males, we used a gamma distribution with a shape parameter of 1 and a mean of 0.25. To allow for a mutation rate in agreement with levels observed for microsatellite markers (Weber and Wong 1993), we set the mutation rate using a gamma distribution with a shape parameter of 2 and a mean of 0.001. This allowed for 95% of the mutation rates to fall between 0.00014 and 0.0028 mutations per generation. We ran 1,000 iterations for each family (using a burn-in of 5,000 and a thinning interval of 400).

Results We monitored five breeding attempts in three breeding seasons in the first New Caledonian Parakeet nest. There were always three adults present at the nest: one female, which was preparing the nest, laying and incubating eggs and two males (a large and a small) which fed the female and the chicks. In all these breeding attempts, each of the three parakeets had an individual way of climbing down the nest, which did not change during the years, indicating a stable group composition. The size of the small male did not change in the 4 years during which we monitored this nest. The two males contributed about equally in feeding the female and the chicks (52 and 48% of 882 feeding observations by the large and small male, respectively). During four of five breeding attempts in the second New Caledonian Parakeet nest (we do not know if a third bird was present during the first breeding attempt as we did not monitor for long enough), a third individual

Table 3 Both the large and the small male New Caledonian Parakeets spent more time in the nest during a mate-guarding period (46 days) when the small male most often tried to copulate with the female compared to the following breeding attempt (66 days) during which the small male principally provided female and chicks with food Mateguarding period Large male

Post mateguarding period Small male

Large male

Small male

Nights spent inside nest (%)

93

0

0

0

Time spent inside nest (%)

59.4

3.5

1.9

1.5

Copulation attempts

0

14

0

1

Times feeding female or chicks

234

179

79

171

Males fighting inside nest

11

0

fed the female and regularly entered the nest. This individual was, as in the first nest, of intermediate size between the female and the larger male. We monitored the third New Caledonian Parakeet nest for only about 3 weeks by weekly nest checks and do not know the exact group composition. The sex ratio in chicks of the first two New Caledonian Parakeet nests was biased towards males (eight males out of 10 chicks). In both New Caledonian Parakeet nests, the most likely number of parents was one mother and two fathers (Table 2). During radio-tracking, we observed that all three adults contributed to feeding the fledglings. We observed mate guarding for the first time in a New Caledonian Parakeet nest in the 2006–2007 season. The large male slept in the nest with the female during the first of two breeding attempts. The mate-guarding period (spanning from the first to the last night the male spent in the nest) lasted 46 days, during which the large male spent most nights inside the nest (Table 3). He had never spent a night inside the nest during the two previous breeding attempts and also did not in the following two attempts. Mate guarding began on the day when the small male attempted to copulate inside the nest with the female for the first time. During the mate-guarding period, all three individuals entered the nest simultaneously on 11

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occasions. These encounters lasted from 10 s to 38 min and always ended with a fight between the males. The large male always dominated these fights. As eggs (and later chicks) were present at this time, the female was usually also aggressive and attacked both males. During the mate-guarding period, the large male spent more time inside the nest than the small male (Table 3). All attempts by the small male to copulate with the female inside the nest occurred during the first 10 days of the mateguarding period, but the female refused copulation. During these 10 days, the female was probably not fertile as she laid the first egg of the following clutch not until a month later. The large male stopped overnighting in the nest after the last chick of the first clutch had fledged and the female had laid the third of five eggs of the following clutch (the female started laying when the four nestlings of the first clutch were still inside the nest). In the post mate-guarding period, the small male was the main food provider but he only tried once to copulate with the female inside the nest. This was the day after the large male stopped guarding the female and a few days before the female laid the last egg of the second clutch. The large male never tried to copulate with the female inside the nest. Chicks hatched during the mate-guarding period and those of the following breeding attempt had different genetic fathers. However, since we could not distinguish the genotypes of the fathers, we do not know which male sired which breeding attempt. During the 700 h of nest monitoring and radio tracking Horned Parakeets, we did not see any sign of feeding helpers but once two females shared a nest. In the 2002– 2003 breeding season, a pair nested in a tree hollow that had just been vacated by the chicks of another pair (at that time, the first pair was several km away from the nest with a radio-tracked fledgling). In the following season, we found five eggs in this nest after the two pairs had both regularly visited the nest. On one occasion, we observed the two females peacefully sharing the cavity, while the two males were chasing each other at the entrance of the tree hollow. The clutch size in the other 15 Horned Parakeet breeding attempts that we monitored was two to four eggs. As the two pairs used the nest at the same time and the clutch size was larger than in any other clutch, it is unlikely that the five eggs were laid by only one female. There was always only one female in the nest during incubation and chick-rearing so it is not possible to say whether both females took turns in the nest or if just one female took care of the eggs and chicks. Based on differences in behaviour of the two pairs, we think that both couples continued to attend the nest, but we never saw them again at the same time in the nest.

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Discussion Cooperative polyandry is the case in which a female mates with multiple males who care for the clutch cooperatively (Faaborg and Patterson 1981). In parrots, to our knowledge, only Heinsohn et al. (2007) and Ekstrom et al. (2007) found genetic evidence for polyandry in Eclectus Parrots (Eclectus roratus) and Greater Vasa Parrots (Caracopsis vasa), respectively. Although we have genetic evidence that the New Caledonian Parakeet is polyandrous and observational evidence that a helper tried to copulate with the female, we cannot exclude the possibility that the female mated with an extra-group male. However, we think that our observations indicate that the mating system of New Caledonian Parakeets is probably cooperative polyandry. The two males in both nests that we monitored intensively were not of equal size. It is unlikely that the smaller males were young as their size did not vary from year to year. It might be that the male helpers did not grow large enough to become dominant males. Previous studies that investigated nestling sex ratios in parrots did not report significantly male-biased sex ratios (Heinsohn et al. 1997; Eberhard 1998; Krebs et al. 2002; South and Wright 2002; Budden and Beissinger 2004; Taylor and Parkin 2008), although Eclectus Parrots are able to produce long series of offspring belonging to one sex before switching to the other sex (Heinsohn et al. 1997). Griffin et al. (2005) reported that cooperative birds tend to produce more offspring of the helping sex. Although the sample size was small, the male-biased sex ratio might be a result of the New Caledonian Parakeet being polyandrous. However, another cooperative bird species did not have offspring with biased sex ratio despite potential benefits (Cockburn and Double 2008). It will take more genetic research to confirm our postulation that New Caledonian Parakeets are cooperatively polyandrous, to find out to which extent each male achieved paternity, and more field work to find out if there is generally a size dimorphism in male nest attendants. Mate guarding is widespread in socially monogamous birds (Birkhead et al. 1987) and has been observed in parrots (Arnett and Pepper 1997; Baltz and Clark 1997). Males of the Golden Whistler (Pachycephala pectoralis) started mate guarding when other males intruded their territory but they did not mate guard without any threat (van Dongen 2008). Similarly, the large male of the first New Caledonian Parakeet nest began to guard the female once he recognised the small male as a threat and mate guarded until the female fertility period ended. Mate guarding can reduce extra-pair paternity in birds (Brylawski and Whittingham 2004; Johnsen et al. 2008) and it seems that the New Caledonian Parakeet may follow this

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strategy, although we do not yet know if the mate guarding reduced the chances of the small male achieving paternity. In the cooperatively breeding Brown Jay (Cyanocorax morio), extra-pair fathers provided nestlings with less food than did the social mate (Williams and Hale 2008). This was not the case in New Caledonian Parakeets, as the small male continued to provide female and nestlings with food while the large male reduced his provisioning directly after the mate-guarding period. The mate-guarding period was the only time during which the two males met inside the nest. The large male might have reduced his food provisioning because he was uncertain about his paternity, even though he guarded the female, but he did not reduce his effort in any other breeding attempt. Females that share nests have been observed in polygynous species with two females and one male (e.g. Hamao and Ueda 1998; Checkett et al. 2001) or of females of different species (e.g. Saunders 1976; Crowell et al. 1982). However, a situation in which two females and two males share a common nest and in which a female incubates a common clutch laid by two females and fathered by two males has been observed in Blackbirds (Turdus merula) (Wysocki and Walasz 2004), but not in parrots. Hahn (1993) incidentally observed two Horned Parakeet pairs that shared a ground nest in which the two females had laid their clutches at about 1 m distance and incubated separately but simultaneously. Our observation indicates that females might even incubate common clutches. It is possible that the females laid a common clutch because of the restricted space in the nest hollow (which both pairs used the previous year, though not simultaneously). Subsequently, they might not have been able to distinguish between their own and foreign eggs. As we could not individually mark birds, we do not know if only one female incubated the eggs and fed the chicks or if they did it alternately. The reason that females shared the nest although there was no lack of alternative tree hollows might be that they were used to the nest as they had successfully bred in it before. Considering our single observation and that of Hahn (1993), cooperative breeding does not seem to be common in Horned Parakeets (2 cooperative and 15 single breeding attempts including Hahn’s 1993 study) and feeding helping does not appear to occur. Brown (1978) included nest sharing in cooperative breeding and Cockburn (2006) defined cooperative breeding as the case in which more than 10% of nests are attended by more than two birds. Accordingly, we think that Horned Parakeets can be regarded as cooperative breeders. Holyoak (1973) suggested the merger of the two genera Cyanoramphus and Eunymphicus because of their morphological similarity. A recent study has shown that they are also genetically related (Boon et al. 2008). It is

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therefore possible that the three New Caledonian species of these two genera (New Caledonian Parakeet, Horned Parakeet, Uvea Parakeet) have evolved from a common ancestor. The New Zealand species of the Cyanoramphus genus are not cooperative breeders (Elliott et al. 1996; Greene 1999, 2003). This supports the statement of Cockburn (2003) that cooperative breeding on islands occasionally evolves from non-cooperative taxa. However, it also raises the question why the New Caledonian Parakeet and, to a lesser degree, the Horned Parakeet, have evolved cooperative behaviour. Environmental conditions have been proposed as one factor responsible for cooperative breeding (e.g. Dow 1980; Ford et al. 1988; Du Plessis et al. 1995; Arnold and Owens 1999). Whereas the two other New Caledonian species of parrots, the Uvea Parakeet (which occurs in forest on coral substrate) and the Rainbow Lorikeet (most common in coastal and alluvial habitats) live in richer habitats, the Horned Parakeet and especially the New Caledonian Parakeet live mainly in rainforest on very low productive soils (authors’ unpublished data). Cooperation with feeding the female and the chicks might therefore improve breeding success to the extent that it compensates for possible shared paternity.

Zusammenfassung Kooperatives Bru¨ten, Partnerbewachung und gemeinsame Nestnutzung bei zwei Papageienarten Neukaledoniens Wir liefern Nachweise fu¨r kooperatives Bru¨ten bei zwei endemischen Papageienarten Neukaledoniens, dem Neukaledoniensittich (Cyanoramphus saisseti) und dem Hornsittich (Eunymphicus cornutus). Durch intensives Filmen von 11 Bruten in zwei Nestern des Neukaledoniensittichs u¨ber 5 Jahre stellten wir fest, dass in beiden Nestern jeweils zwei Ma¨nnchen verschiedener Gro¨ße das Weibchen und die Jungen fu¨tterten. In einer Brut bewachte das gro¨ßere Ma¨nnchen das Weibchen wa¨hrend das kleinere Ma¨nnchen versuchte sich im Nest mit ihr zu paaren. Genetische Analysen zeigten, dass jedes Ma¨nnchen Vater eines Teils der Jungen war. Wa¨hrend 17 Bruten in 11 Hornsittichnestern teilten sich in einem Fall zwei Paare das selbe Nest. In allen Hornsittichbruten fu¨tterten ausschließlich die Eltern. Acknowledgments This study was part of the research project ‘‘Impact of introduced mammals and habitat loss on endemic birds of New Caledonia’’ done in cooperation with the Direction de l’Environnement (Province Sud, New Caledonia), which issued all permissions for this study, and financed by the Loro Parque Fundacioń (Spain), Polish Ministry of Science and Higher Education (grant

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796 2P04F 001 29), Conservation des Espe`ces et Populations Animales (France), La Fondation Nature et Dećouvertes (France), Fonds fu¨r bedrohte Papageien—Zoologische Gesellschaft fu¨r Arten- und Populationsschutz (Germany), and a doctoral grant from Province Sud (to Sophie Rouys). We thank A. Lorenzo, the director of the Parc Zoologique et Forestier, for providing us with feather samples of captive parakeets; M. Broersen, C. Chatreau, P. de Pous, D. Dingemans, S. Duijns, A. Legault, B. Michielsen, E. Minnema, L. Nijdam, H. Theuerkauf, J. van Dijk, M. van Opijnen and J. Wardenaar for their help during field work; T. Greene for informing us about the location of a parakeet nest; and A. Cockburn, T.W.P. Friedl and anonymous reviewers for useful comments.

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