First nest descriptions, nesting biology and food ...

First nest descriptions, nesting biology and food habits for Bernier’s Vanga, Oriolia bernieri, in Madagascar Russell Thorstrom1 & Lily-Arison René de Roland2 The Peregrine Fund, 566 West Flying Hawk Lane, Boise, ID 83709, U.S.A. Ankoay Trust for Conservation, B.P. 4113, Antananarivo (101), Madagascar

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Thorstrom, R. & René de Roland, L-A.R. 2001. First nest descriptions, nesting biology and food habits for Bernier’s Vanga, Oriolia bernieri, in Madagascar. Ostrich 72(3&4): 00–00. Four nests of the rare and endemic Bernier’s Vanga, Oriolia bernieri, were discovered; one in 1997, one in 1998, and two in 1999 on the Masoala Peninsula, northeastern Madagascar. At the 1998 nest, the female made 189 visits with 186 deliveries of nesting material during 34.6 h of observation. The female spent 9.2% (194.2 min) of the observation time building the nest while an immature male delivered nest material six times and spent 3.2 min at the nest placing the material. Nesting material included: 67.2% (125) decomposed root material, 24.7% (46) palm fibres, 6.5% (12) dry leaves, 1.1% (2) moss, and 0.5% (1) white plant down. In 41.0 h of observation during the incubation period the female incubated for 53% (21.7 h) of the time, the adult male for 32.3% (13.2 h), the immature male for 4.3% (1.8 h), and the nest was unattended for 10.4% (4.3 h). This breeding attempt failed on day 13 of incubation when a Madagascar Harrier-Hawk, Polyboroides radiatus, ate the egg(s). At one of the 1999 nests, the incubation and nestling periods were 17 days each. Three young fledged during the middle of November. Of the 82 identified prey items recorded during the nestling period, 91% were invertebrates and 9% vertebrates. Spiders, crickets, cockroaches, and geckos represented the most numerous prey taken, totaling 77% of the identified prey.

INTRODUCTION Bernier ’s Vanga, Oriolia bernieri, belongs to the family Vangidae, which contains 15 species in 11 genera (Langrand 1990), and nearly all are endemic to Madagascar. The vangids are closely related to the helmet shrikes (Prionopidae) of southern Africa (Benson 1984, 1985). They are best known for their adaptive ecological radiation, resembling that of the Hawaiian drepanids and Galapagos finches (Amadon 1950; Grant 1986). Despite the vangids’ broad distribution and interest to biologists, their basic natural history and ecology remain virtually unknown (Putnam 1996), and even the number of known species changed recently when a new Vanga was described from the southwestern region of Madagascar (Goodman et al. 1997). Bernier’s Vanga is one of the larger members of the Vangidae, and nothing is known of its breeding biology (Langrand 1990). It is listed as ‘vulnerable’ by Collar et al. (1994). Bernier’s Vanga inhabits only the lowland eastern evergreen humid forests of Madagascar, ranging from Zahamena in the south to Marojejy in the north and is rather rare throughout its range (Langrand 1990). On the Masoala Peninsula it was found to be uncommon, patchily distributed and only in undisturbed forest sites (Thorstrom & Watson 1997). In this paper, we report on the first nest description for the Bernier’s Vanga, nest construction and incubation roles of the sexes and diet. STUDY AREA AND METHODS Three nests were located on the eastern interior side of Masoala Peninsula about 20 km northwest of the village of Sahamalaza and one nest was discovered on the west side of the 0030-6525 Ostrich (September 2001) 72(3&4): 0–0

peninsula near Andranobe Field Station (AFS). The peninsula is mainly roadless and composed of a mosaic of slash-and-burn clearings, secondary growth and primary forests. The mature lowland rainforest of the Masoala Peninsula has a canopy height near 30 m with emergent trees, high floristic diversity, and steep mountainous topography (Guillaumet 1984). Elevations on the Masoala Peninsula range from 0–1200 m. Average annual rainfall recorded at AFS approximately 30 km west of the three eastern interior nest sites and near the one western nest site, was 6.049 mm from 1991–1996 (Thorstrom et al. 1997). Monsoon rains and cyclones occur between December and March, whereas rain falls steadily between April and August. September to November are the driest months, receiving on average 481 mm (8%) of the annual rainfall recorded from 1991–1996 (Thorstrom et al. 1997). Nest tree diameter was measured with a diameter-at-breast height (dbh) tape and nest height with a plumb-line. Observations were made using ×10 binoculars at 10–15 m from the nest tree. Nest observations at nest 2 averaged 5.4 h per day and totalled 75.6 h during nest construction and incubation. A mist-net (2.6 × 6 m, 36 mm mesh) was placed near the nest building activity of on pair in 1999. The captured vanga was measured with vernier callipers (nearest 1.0 mm), weighed (nearest 1.0 g, Pesola 100-g scale) and ringed. Measurements taken were: bill length (mm) from the end of feathering on the top mid-line to the tip (Palmer 1962); wing-length (mm) from the front of the folded wrist to the tip of the longest primary with wings unflattened (Biggs et al. 1978); tarsus-length (mm) from the posterior centre of the tibiotarsal-tarsometatarsal joint to the dorsal base of the centre toe (Biggs et al. 1978); tail-length (mm) from the point between middle pair of feathers at their insertion to tip of longest one. RESULTS Nests Four nests were located; one in November 1997, one in November 1998, one in September 1999 and one in December 1999. Three nests were found in the southern interior of Masoala Peninsula at Ihazomay (15° 43’S; 50° 13’E) and one nest was on the western side of Masoala Peninsula at AFS (15° 41’S; 49° 57’E). Two nests were placed in the frond whorls of Pandanus spp. and two in Dracaena reflesca and averaged 12.8 ± 1.6 m (range 10.8–14.4 m) above the ground. The nest trees averaged 23.1 ± 6.8 (S.D.) cm (range 15.5–32 cm) dbh. Nest no. 1. This nest was discovered during the nest construction period by L-A.R. on 27 November 1997 along a small riparian area within the main forest block. The pair building the nest was a black-blue male and a rufous female. During 5 min, from 06h52 to 06h57, the female was twice observed delivering decomposed material. On 28 November 1997, from 0736 to 0815 h, the female delivered one beak full of decomposed material. The nest was situated 10.8 m above the ground in a 32-cm dbh Pandanus sp. and was placed inside the spiralling palm fronds and surround by spikes of the frond. It was composed of detritus 1

and palm fibres. Neither nest contents nor size could be closely observed or measured. One year later a neighbouring tree was climbed in November 1998 and from that vantage point it could be seen that no nest was present at the old site. Nest no. 2. This nest was discovered by R.T. on 11 November 1998, in a multi-branched Pandanus sp. and was placed 14.4 m above ground in a 23 cm dbh palm. This nest was approximately 2.5 km northeast from the 1997 nest site. The pair building the nest was a rufous-plumaged female with a yellow iris, and a rufous-plumaged immature male with three black body feathers on the upper breast. The female was the principal nest builder. In 34.6 h of observations at the nest during nest building, from 11–18 November, the female was observed carrying nesting material to the nest 186 times, twice visiting the nest without material and once removing nesting material. The female spent 194.2 min (3.2 h) and averaged 61.7 ± 2.4 (S.E.) sec (n = 189, range = 0.2–3.25 min) constructing the nest. Nesting material delivered to the nest consisted of decomposed root material 67.2% (125), palm fibres 24.7% (46), dry leaves 6.5% (12), moss 1.1% (2), and white fuzz 0.5% (1). The immature male visited the nest six times for a sum of 3.2 min and averaged 28 ± 4.9 (S.E.) sec (range 10–40 sec) per visit. This male delivered palm fibres four times and decomposed root material twice. The time spent per visit at the nest by the female nearly doubled from the start of nest building to egg-laying/incubation (Table 1). On 12 November, the immature male attempted to feed the female a small cricket (Orthoptera). The female refused the prey item and eventually the male consumed it. During the nest-building period the immature male was observed accompanying the female to and from the nest area and remained in the vicinity, from 5–25 m from the nest. The first observed copulation was on 15 November by the adult-plumaged male (all black-blue plumage) and lasted 5 sec. On 18 November two copulations by the immature male lasted 8 and 9 sec. By 23 November incubation had begun and the female and adult-plumaged male shared in the duties. In 41.0 h of observation during the incubation period, the female incubated for 53% (21.7 h, n = 19, range 3.7–119.6 min), the adultplumaged male for 32.3% (13.2 h, n = 7, range 3.9–210.2 min), the immature-plumaged male incubated once for 4.3% (1.8 h), and the nest was unattended for 10.4% (4.3 h, n = 16, range 0.6–80.0 min). On 4 December, a Madagascar Harrier-Hawk, Polyboroides radiatus, reached the nest and ate the egg(s). Either this bird, or another individual of the same species had tried twice earlier to reach the nest but had been driven off by the female. Both adults, female and adult-plumaged male, continued to visit the nest site frequently for one day after the eggs had been eaten. Nest no. 3. This nest was discovered by R.T. on 30 September 1999, in a hasina palm Dracaena reflesca and was placed on the west side of the frond whorl, 14 m above ground in a hasina with a 15.5 cm dbh. This nest was at an altitude of 60 m a.s.l., 25 m from a creek and 1 km southeast of AFS on the west side of the TABLE 1. Mean time per visit during the nest building period by the female Bernier’s Vanga at nest 2 in 1998. The nest was discovered on 11 November 1998.

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Date

Time on nest (sec ± SE)

11/12 11/13 11/15 11/16 11/17 11/18

42.9 ± 4.4 44.7 ± 4.2 55.4 ± 4.7 71.0 ± 4.3 74.7 ± 5.5 92.1 ± 7.1

Masoala Peninsula. During 19.9 h of observation only the female was seen to bring nest material and to build the nest. Nest building occurred from 30 September to 5 October 1999 and the material used was similar to nest 2. We observed one attempted copulation on 2 October when the male gave a loud ‘jeet’ call and mounted the female but the female flew, knocking the male off and avoiding copulation. Egg-laying occurred between 8 and 11 October and incubation started on 12 or 13 October. R.T. observed this nest for 23.7 h during incubation, during which time the female incubated for 54% (12.8 h), male for 45% (10.6 h) and the nest was unattended for 1% (0.3 h) of the time. This nest contained three eggs similar in appearance to the Helmet Vanga, Euryceros prevostii, eggs; pink-white mottled with carmine red, especially at the larger end (Langrand 1990) but smaller. The incubation period lasted approximately 17 days. Three young hatched between 28 and 29 October. Nest no. 4. This nest was discovered by L-A.R. in the same area as nest 1 and nest 2 on 4 December 1999. This nest was placed in the centre of the frond whorl 12 m above ground in a hasina palm with dbh of 21.8 cm, growing at an altitude of 50 m and 20 m away from a creek. The adults were feeding young at the time of discovery. Nestlings At nest 3 there was a noticeable difference in size and plumage growth between the nestlings, suggesting asynchronous hatching with a one day difference between oldest and youngest. On 1 November (3–4 days of age), nestlings had closed eyes and erupted feather follicles all over the body. The nestlings were covered with grey-brown plumage. By 7 November (9–10 days of age) nestlings started preening and wing exercising. On 9 November (11–12 days of age), the nesltings had brown plumage similar to an adult female. Nestlings wing exercised more frequently, and began stretching and standing in the nest cup. The nestlings had black mouth linings, pale yellow gapes and brown eyes. On 10 November (12–13 days of age) Nestlings wing flapped vigorously with primaries about 25 mm long. On 12 November (14–15 days of age) nestlings were nearly fully feathered, and perched on the nest rim flapping vigorously. Nestlings vocalized a weak ‘jeet-jeet-jeet’ as an adult approached the nest with food. On 13 November (15–16 days of age) two nestlings walked outside the nest cup and returned quickly and wingflapped strenuously. On 14 November (16–17 days of age) all three young fledged from the nest and were not observed returning to the nest or in the nest vicinity after fledgling. Male behaviour At nest 3 the male made a loud wing-whirling flight above the nest and tree canopy five times during nest building, three times during incubation and twice during the nestling period. During the nestling period, both adults sometimes gave a tail-wagging behaviour in the nest vicinity at the arrival of the partner with food. This behaviour was first observed on 1 November and continued until last seen on 13 November. During 20.3 h of nest observation the male was observed displaying this behaviour 13 and the female six times. Measurements The female was trapped at nest 3 on 3 October 1999. Measurements are: bill length 25.5 mm, wing chord flattened 124 mm, tail length 83 mm, tarsus length 22.8 mm, and mass 59 g. Food and foraging behaviour Among the 109 prey items observed delivered to the nestlings at nest 3, 68.8% (75) were invertebrates, 6.4% (7) vertebrates and 24.8% (27) were unidentified. We believe that most of the 27 0030-6525 Ostrich (September 2001) 72(3&4): 0–0

TABLE 2. Prey observed delivered to the nestlings at nest 3 by Bernier’s Vanga from October to November 1999 (n = 109 prey items). Prey type (class, order or genus) Invertebrates Spiders (Arachnida) Crickets (Orthoptera) Grasshoppers (Orthoptera) Katydid (Orthoptera) Cockroaches (Blattaria) Hopper (Homoptera) Mantid (Mantodea) Unidentified insects Vertebrates Geckos (Phelsuma spp.) Gecko egg (Phelsuma sp.) Unidentified Total

Number

Percentage

29 21 4 1 7 1 1 9

26.6 19.2 3.7 0.9 6.4 2.8 0.9 8.0

6 1 27

5.5 1.3 24.7

109

100.0

unidentified prey items were insects; the diet is most accurately described as percentage of identified prey rather than total prey. The most numerous identified prey taken were spiders 35%, crickets 26%, cockroaches 9% and day geckos (Phelsuma spp.) 7%, representing 77% of identified prey (Table 2.). Prey size ranged from 0.5-cm cricket to a 10-cm day gecko, Phelsuma sp. Of 109 prey items observed delivered by this pair to the nestlings, 81% were delivered by the female (n = 88) and 19% were fed by the male (n = 21). On 30 October 1999, the male chased a spider on the palm fronds below the nest. On 1 November 1999, the female flew to a hasina 30 m west of the nest, hopped into the interior area of the palm and searched the fronds for prey by poking and probing into the palm base. The female continued this hopping and searching activity until she had covered the area. On 9 November 1999, the female probed and pulled flaking bark off a tree trunk, picked at a moss-covered branch and the base of an epiphytic bird nest fern (Asplenium sp.) while foraging. On 9 November 1999, the male was observed prying and peeling bark away on a moss-covered branch, catching a cockroach and eating it himself. On 10 November 1999, the male foraged by flaking off bark and probing in moss-covered branches. On 12 November 1999, the female foraged by probing in the base of an epiphytic fern, sometimes disappearing for several minutes behind the hanging dead fern fronds. DISCUSSION The Masoala Peninsula contains the largest intact lowelevation forest left in Madagascar, a threatened habitat type in the eastern biogeographic region of Madagascar. Masoala National Park was inaugurated on October 1997, conserving 220 000 hectares of mature intact rainforest and the endemic fauna and flora of this region. Bernier’s Vanga has a limited distribution in eastern rainforests and appears to be relatively rare throughout its range in northeastern Madagascar (Langrand 1990; Thompson & Evans 1992; Evans et al. 1992). This species is reported to occur from sea level to 1000 m (Rand 1936; Langrand 1990). In Masoala National Park it is considered uncommon but we have observed the species at five of eight inventory sites in 1993 and 1994 (Thorstrom & Watson 1997). Bernier’s Vangas can be heard occasionally in Masoala forest, individually, in pairs or small groups moving through the upper canopy of the forest during the breeding season. They commonly occur in mixed-species vanga flocks (Langrand 1990; Thompson & Evans 1992; Thorstrom & Watson 1997). Yamagishi et al. (1992) measured 22 nests of the Rufous Vanga, 0030-6525 Ostrich (September 2001) 72(3&4): 0–0

Schetba rufa. The nests were situated at the first fork from the ground and had a mean height of 4.3 ± 1.9 m (range = 1.6–8.1). By contrast, the four nests of Bernier’s Vanga were built in palms (Pandanus sp. and Dracaena reflesca), placed inside the palm leaf whorl, and averaged 12.6 m above ground. The spiked trunks and prickly fronds of Pandanus palms may restrict access by mammalian predators, but offer no protection from aerial predators such as the Madagascar Harrier-Hawk. At AFS, R.T. observed a Ring-tailed Mongoose, Galidia elegans, climb two 5–6 m Dracaena palms within several metres of the vanga nest tree. Selection of Pandanus and Dracaena for nesting may restrict available nesting habitat for Bernier’s Vangas, especially in areas where these palms do not grow, and may be one of the reasons for the low population density and rarity of this species throughout Madagascar. The female was the major nest builder at two of the nests observed during nest construction. Only the immature male in 1998 assisted in nest construction during six visits. The adult males did not contribute at all during the nest construction period. In comparison, during observations of nest building at two Rufous Vanga nests, males shared nearly equally with the females, and subadult birds only visited once (Yamagishi et al. 1992). The time spent per visit increased and nearly doubled from the start of nest building to incubation. As egg-laying approached, the female spent more time at the nest and possibly in pre-laying lethargy, waiting for the egg-laying period. When the female was engaged in nest building the immature male was present in the area at a distance of 5–25 m, but rarely visited the nest. Unlike the Rufous Vanga, the adult male Bernier’s Vanga did contribute to nest building. In Rufous Vangas, eight of 15 breeding groups, called ‘onefemale groups’, were composed of trios or foursomes, made up of predominately subadult-plumaged birds and one adult female (Yamagishi et al. 1992). At nest 2, three Bernier’s Vangas were observed in association with this nest: an adult female, adult male and an immature male. This young male incubated on one occasion. We suspect that this species may on occasion have a breeding social system similar to that of the Rufous Vanga (Yamagishi et al. 1992). Unfortunately, we did not have further opportunity to observe the role of this immature male during the rest of incubation and nestling period. We had one observation of an attempted courtship feeding when the immature male tried to feed the female during the nest construction period. Courtship feedings may be important behaviour for this species during the courtship period, as in many other species of birds in which the female is fed by the male to prepare her body for egglaying and to strengthen the pair bond. Both male and female Rufous Vangas shared incubation of the eggs (Yamagishi et al. 1992). In two nests of Bernier’s Vanga, the male and female shared incubation with the female spending slightly more time (53–54%) than the male (37–45%) on incubation, with the nest unattended for 1–10.4% of the observation time. The Rufous Vanga had an incubation period of 13–17 days and a nestling period of 13–15 days (Yamagishi et al. 1992). At nest 3, we recorded a 17-day incubation and 16–17-day nestling period. The incubation and nestling periods in Bernier’s Vanga are comparable to those of the Rufous Vanga but slightly longer due to its larger size. In 1994 near AFS, R.T. observed a fledgling being fed three spiders in a 3-hour observation period by a female. Nearly 91% of the diet during the breeding season was invertebrates, mainly spiders, crickets, cockroaches, grasshoppers and homopterans. Rand (1936), Benson et al. (1977), Langrand (1990) and Thompson & Evans (1992) described Bernier ’s Vanga as insectivorous, but on the basis of this study they appear to have a broader diet. We observed several day geckos (Phelsuma spp.) 3

and one gecko egg fed to the nestlings. The foraging behaviour that Thompson & Evans (1992) described for Bernier’s Vanga is comparable to our observation of the nesting pair but Dracaena palms were used as well as Pandanus and large moss-covered tree branches. Further research on distribution, behaviour, social system and ecological needs of the Bernier’s Vangas is needed for a better understanding of this species. The presence of Bernier’s Vangas may be a good indicator of intact primary forests because they appear to be a forest-dependent species occurring only in mature forest (Thorstrom & Watson 1997). We suspect they have a low population density and are patchily distributed, and this contributes to the difficulties of finding and studying them. ACKNOWLEDGEMENTS We thank Rick Watson and Bill Burnham of The Peregrine Fund for making this study possible. Special thanks to Rick Watson and Lloyd Kiff for comments on earlier drafts. We thank the Direction des Eaux et Forôts, Commission Tripartite, Projet Masoala and ANGAP for their collaboration with The Peregrine Fund’s Project in Madagascar. This work was supported by grants from the Disney Corporation. REFERENCES Amadon, D. 1950. The Hawaiian honeycreepers (Aves, Drepaniidae). Bulletin of the American Museum of Natural History 95: 151–262. Benson, C.W. 1984. The birds of Madagascar. In: Jolly, A., Oberle, P. & Albignac, R. (eds) Madagascar: 115–149. Oxford: Pergamon Press. Benson, C.W. 1985. Vanga. In: Campbell, B. & Lack, E. (eds) A dictionary of birds: 619. Vermillion: Buteo Books. Benson, C.W., Colebrook-Robjent, J.F.R. & Williams, A. 1976–77. Contribution à l’ornithologie de Madagascar. L'Oiseau et la Revue Française d'Ornithologie 47: 41–64. Biggs, H.C., Biggs, R. & Kemp, A.C. 1978. Measurements of raptors. In: Kemp, A.C. (ed.) Proceedings of the Symposium on African Predatory

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Birds: 77–82, Pretoria: Northern Transvaal Ornithological Society. Collar, N.J., Cosby, M.J. & Stattersfield, A.J. 1994. Birds to watch 2: The world list of threatened birds. BirdLife Conservation Series No. 4. Cambridge: BirdLife International. Evans, M.I., Duckworth, J.W., Hawkins, A.F.A., Safford, F.J., Sheldon, B.C. & Wilkinson, F.J. 1992. Key bird species of Marojejy Strict Nature Reserve, Madagascar. Bird Conservation International 2: 201–220. Goodman, S.M., Hawkins, A.F.A. & Domergue, C.A. 1997. A new species of vanga (Vangidae, Calicalicus) from southwestern Madagascar. Bulletin of the British Ornithologists’ Club 117: 5–10. Grant, P.R. 1986. Ecology and evolution of Darwin’s Finches. Princeton, New Jersey: Princeton University Press. Guillaumet, J-L. 1984. The vegetation: an extraordinary diversity. In: Jolly, P., Oberlé, P. & Albignac, R. (eds) Key environments: Madagascar: 27–30. New York: Pergamon Press. Langrand, O. 1990. Guide to the birds of Madagascar. New Haven, Connecticut: Yale University Press. Palmer, R. 1962. Handbook of the North American Birds, vol. 1: loons through flamingos. New Haven & London: Yale University Press. Putnam, M.S. 1996. Aspects of the breeding biology of Pollen’s Vanga (Xenopirostris polleni) in southeastern Madagascar. Auk 113: 233–236. Rand, A.L. 1936. The distribution and habits of Madagascar birds. Bulletin of the American Museum of Natural History 72: 143–499. Thompson, P.M., & Evans, M.I. 1992. The threatened birds of Ambatovaky Special Reserve, Madagascar. Bird Conservation International 2: 221–237. Thorstrom, R. & Watson, R.T. 1997. Avian inventory and key species of Masoala Peninsula, Madagascar. Bird Conservation International 7: 99–115. Thorstrom, R.K., Andrianarimisa, A. & René de Roland, L-A. 1997. In: Watson, R.T. (ed.) Weather at Andranobe Field Station, western Masoala Peninsula. Masoala Project. Progress Report IV: 127–130. Boise, Idaho: The Peregrine Fund. Yamagishi, S., Urano, E. & Eguchi, K. 1992. The social structure of Rufous Vanga (Schetba rufa) in Ampijoroa, Madagascar. In: Yamagishi, S. (ed.) Social structure of Madagascar higher vertebrates in relation to their adaptive radiation: 46–52. Osaka, Japan: Osaka City University. Received June 1999. Accepted April 2000 Editor: L. Bennun

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