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97 AUSTRALIAN Field Ornithology 2011, 28, 97–113 The Breeding Biology of the Dusky obscura in the Northern Territory, and the Importance of in the Diet of Nestling

RICHARD A. NOSKE1 and ASHLEY J. CARLSON2 1Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, Northern Territory 0909 (Email: [email protected]) 2P.O. Box 4074, Forster, New South Wales 2428 (Email: [email protected])

Summary The breeding biology of the Dusky Honeyeater Myzomela obscura is poorly known, despite the species’ wide distribution and use of a broad range of habitats. In the Northern Territory, breeding was recorded in all months, but just over 50% of estimated laying dates were in April and May, corresponding with the transition from the wet to the dry season. In Darwin, nests were placed 1.0 to 9.0 m above the ground in a variety of trees or tall shrubs, including exotics. The size of clutches or broods never exceeded two (n = 9). At two closely observed nests, the incubation period was 12.4 and 12.75 days, similar to another myzomeline honeyeater. Nest-attentiveness was ~65% over 2 days at one nest, similar to the few temperate-zone Australian honeyeaters for which such data are available. The nestling period at the only successful nest that we observed was 14.3 ± 0.7 days, consistent with slightly smaller species in other honeyeater genera. Unlike most honeyeater species, nestling Dusky Honeyeaters hatched with much down. Diurnal brooding represented 20–28% of the presumed female’s time during the first 4 days after hatching, but had ceased by Day 6, earlier than in temperate-zone honeyeater species. The mean rate of food provisioning was very low (8.9 feeds/h) compared with that of most other honeyeater species studied to date. Evidence suggests that Dusky Honeyeaters may feed their young largely on nectar.

Introduction The Dusky Honeyeater Myzomela obscura ranges from North Maluku in eastern through southern to coastal and subcoastal Northern Territory (NT; the nominate subspecies, M.o. obscura) and Queensland (M.o. harterti) (Higgins et al. 2001) in . It occurs in a variety of habitats, at recorded densities of 0.06–0.64 /ha (Higgins et al. 2001). Near Darwin, NT, it was most common in eucalypt forest with a dense understorey and semi-evergreen monsoon vine forest (0.4–0.6 bird/ha: Woinarski et al. 1988). In , NT, it was most abundant in monsoon rainforests, particularly in sandstone-spring monsoon rainforests (Brooker et al. 1990; Woinarski 1993). The species appears to be sedentary within large home-ranges. In heterogeneous native vegetation on a 470-ha plot 40 km south-west of Darwin, it was one of five species of honeyeaters that were present throughout a 39-month study (Franklin & Noske 1998). Recapture rates (13%) of banded (n = 149) were slightly lower than for the much commoner, slightly smaller, indistincta, and just over 50% of recaptured Dusky Honeyeaters were retrapped within 200 m of the banding site, with the maximum recorded movement being 1.2 km, and the maximum time elapsed to recapture 29 months (Franklin & Noske 1998). Despite this wide distribution and the broad habitat requirements, the breeding biology of this species is poorly known, with only six nest records in the Nest AUSTRALIAN 98 NOSKE & CARLSON Field Ornithology

Record Scheme (NRS) of Birds Australia up to 1998 (Higgins et al. 2001). Based on the gonadal condition of eight specimens collected in Darwin and Arnhem Land, NT, Deignan (1964) suggested that the ‘breeding season is of long duration in the [Northern] Territory’. Indeed, Noske & Franklin (1999) recorded breeding in almost all months of the year in the monsoon tropics of the NT. This is in contrast with the situation for the congeneric Red-headed Honeyeater Myzomela erythrocephala and several other species of honeyeater (Meliphagidae) in the region, which breed during the dry season (May–October), when nectar is most abundant (Noske & Franklin 1999; Franklin & Noske 2000). In this paper we describe the breeding season and clutch-size of the nominate subspecies of Dusky Honeyeater breeding in the NT from opportunistic observations and published sources, as well the incubation and nestling periods, and parental care at two nests in suburban Darwin.

Methods We collated breeding records for the NT from two sources: (1) opportunistic records in Darwin (12°28′S, 130°52′E) since 1988 (by RAN), including those reported by Noske & Franklin (1999); and (2) the published literature, importantly including two records of breeding within 50 km of Darwin (Crawford 1972), three from Nhulunbuy (12°15′S, 136°45′E: Boekel 1976; Officer 1976), one from Kakadu National Park (12°33′S, 132°18′E: Brooker & Parker 1985) and one from Pine Creek (13°49′S, 131°50′E: Rix 1970). The NT lies within the Australian monsoonal tropics, which experiences little seasonal fluctuation in temperature and light availability. However, rainfall is highly seasonal, with >90% falling between November and April (the wet season). Mean annual rainfall at Darwin is ~1700 mm [1941–2009; http://www.bom.gov.au/nt (accessed 10 July 2010)], whereas at Nhulunbuy, farther to the east, mean annual rainfall is slightly lower and less seasonal, and the wet season begins and ends ~1 month later than in the west (Langkamp et al. 1979). Consistent with the literature, we define the breeding season as the months in which eggs are laid. As exact dates for laying were rarely determined, however, we have estimated the month of laying by extrapolation from dates on which eggs, nestlings or fledglings (which comprised most of our observations) were recorded. For example, Crawford’s (1972) breeding records comprise a bird sitting on a nest on 1 June 1968, and a dependent juvenile on 6 December 1970; we have estimated that laying for these birds occurred in May and November, respectively. Where only eggs were recorded, we have assumed that they were laid in the same month, unless the date fell within the first week, in which case half of the clutch was attributed to the previous month. Unless otherwise stated, records of building were excluded from the analyses because of the well-known tendency of many Australian birds to abandon nests before laying in them. In accordance with Marchant (1980), the duration of the incubation period at each nest was calculated from the midpoint between the maximum interval (i.e. from the last observation before the clutch was completed to the first observation of all eggs hatched) and minimum interval (i.e. from the first observation of the full clutch to the last observation of unhatched eggs), plus or minus half the range in hours between the difference of these intervals; the nestling period—i.e. from hatching to fledging—was calculated in a similar way. The contents of some nests were observed by using a mirror mounted on a pole. Detailed observations were made at two nests in Darwin, one in the suburb of Wagaman (12°23′08˝S, 130°53′08˝E) and the other in Jingili (12°23′21˝S, 130°52′18˝E). Both nests were in typical suburban yards consisting of a lawn with isolated exotic shrubs and palms (Wagaman) or garden beds of young native shrubs (Jingili). The Wagaman nest was discovered on 9 April 2008 during its construction, and was watched over 2 days during the incubation period (total 7.5 h) and 1 day during the nestling period (4.2 h) from a distance of 7 m, with the aid of 10 × 42 binoculars. The Jingili nest was built in a pot-plant on a concrete slab under the eaves of a house, beside a carport. It was found on 18 July 2009 during its construction, but observed only sporadically until the eggs hatched, after which nest activity was recorded for up to 6.6 h on each of 9 days during the nestling period (total 29.7 h), using a video camera set up near an open louvred window with a flyscreen inside VOL. 28 (3) SEPTEMBER 2011 Breeding Biology of Dusky Honeyeater, NT 99 a room of the adjacent house. Although the camera was only 1 m from the nest, the birds appeared not to be affected by it, or indeed by the frequent motion of, or sounds made by, human occupants of the room. Consistent with the literature (e.g. Conway & Martin 2000), we refer to bouts of incubating or brooding on the nest and absence from the nest as on- and off-bouts, respectively. Nest-attentiveness (the percentage of time spent by the sitting bird on the nest) was calculated from all video-recorded samples combined. Because video-recording sessions usually started when the incubating or brooding bird was already sitting or absent (incomplete bouts), only complete periods of absence from the nest were considered in calculating the total video-recording sample time, and hence feeding rates and brooding effort. The first or last incubation or brooding bout was discounted from the analysis so that the number of on- and off-bouts was equal. All means are given ± Standard Deviation. The species is sexually monomorphic in plumage and bare parts and, consequently, the sex of the birds attending the nest could not be determined. No more than two adults were observed at each nest, but no attempt was made to trap and colour-band adults. Given the frequency of co-operative breeding in honeyeaters (Higgins et al. 2008), the possibility of helpers cannot be ruled out completely, although we have no evidence for it in this species. Chicks were handled only on Days 11 and 14 to minimise stress to the adults. Meteorological data were sourced from the Bureau of Meteorology [http://www.bom.gov. au/nt/ (accessed 10 July 2010)] for Darwin Airport located 4.5 km south and 4.8 km south- east, respectively, of the two suburban nesting sites. During observations of the Wagaman nest (April 2008), the average temperature was 27.2°C and relative humidity 60% at 0900 h. For the Jingili nest (August 2009), mean temperatures at 0900 and 1500 h were 25.4°C and 30.3°C, respectively, and relative humidity varied between 25% and 76%.

Results

Breeding season, nest-sites and building Laying occurred in all months of the year, but more than half of all records (51.3%; n = 40) were from April (27.5%) and May (23.8%) (Figure 1). Nests were usually built in trees or tall shrubs. Of 13 nests in Darwin, four were in African Mahoganies Khaya senegalensis, a popular street tree, typically growing to 15–20 m tall, and another four were in other exotic trees: mango Mangifera sp., African Tulip Tree Spathodea campanulata, Royal Palm Roystonea sp. and Madagascar Palm Dypsis madagascariensis (1 nest per tree species). The remaining five Darwin nests were in shrubs, comprising Cordyline sp. (2), pot-plants (2), and an exotic fig Ficus sp. (1). In natural habitats within or just outside Darwin, single nests were found in a Damson Terminalia microcarpa and a Common Hakea arborescens and, in Gove, a nest was found in a paperbark sp. tree (Boekel 1976). The average height of nests above ground was 3.9 ± 2.24 m (n = 14, range 1.0–9.0 m), in plants ranging from 1.8 to 13 m in height (n = 4). The Wagaman nest was 1.85 m above the ground in a 2.5-m-tall Cordyline shrub located 3 m from the front door of the single-storey home of AJC. Within the shrub, the nest was positioned in the lower canopy where old leaves were dropping to expose a bare upright stem. The nest was discovered on 9 April 2008, when it consisted of a flat matrix of coarse grass heads and fine twiglets 6–7 cm long, lightly bound with cobweb between two leaf-stems 5 cm apart. Over the next 3 days the nest was shaped into a suspended cup and lined with fine dead grass stems. The external diameter (of the irregular ‘circle’ of the cup) was 59–69 mm and the external depth was 42 mm; the internal diameter was 43–45 mm and the internal depth 33 mm (measurements were taken after the nest was depredated). The nest was porous, its contents being visible from the outside. The Jingili nest AUSTRALIAN 100 NOSKE & CARLSON Field Ornithology

Dusky Honeyeater hatchling and unhatched (but fertile) egg at Wagaman, Darwin Plate 26 Photo: Ashley J. Carlson

Dusky Honeyeater chicks at 4 days old at Jingili Plate 27 Photo: Richard A. Noske VOL. 28 (3) SEPTEMBER 2011 Breeding Biology of Dusky Honeyeater, NT 101

Dusky Honeyeater chicks at 9 days old at Jingili Plate 28 Photo: Richard A. Noske

Dusky Honeyeater chicks at 13 days old at Jingili Plate 29 Photo: Richard A. Noske AUSTRALIAN 102 NOSKE & CARLSON Field Ornithology

Figure 1. Estimated laying dates of Dusky Honeyeaters in the NT (n = 40). For clutches in which the estimated laying date fell within the first week of a month, half of the clutch was attributed to that month and half to the previous month; see Methods for explanation and sources. was 1.03 m from the ground in a potted large-leaved exotic fig 1.8 m tall; its external diameter was 60–65 mm and the external depth was 60 mm; the internal diameter and depth were both ~45 mm (measurements taken after the nest was vacated). This nest and another that had fallen from a palm tree were composed mainly of fine dead twiglets and spiderweb, with a lining of fine dead grass stems and occasional rootlets.

Clutch-size and incubation The eggs of the Wagaman and Jingili clutches were lustrous white with many small to medium-sized red-brown blotches, irregular markings and dots of pale khaki, and tiny dots of dark chestnut or chocolate scattered over most of the surface, and with a dense band of blotches and dots of the same colour, but larger and overlapping one another, at the larger end (Plate 25, front cover). All five clutches that could be seen were of two eggs [n = 4: Darwin (this study); n = 1: Gove (Boekel 1976)]. Four additional nests in Darwin contained one (n = 2) or two (n = 2) nestlings. In seven additional breeding records, adults were observed feeding two fledglings, and another 12 records involved at least one fledgling or dependent juvenile. The time between the start of construction of the Wagaman nest and laying of the first egg (16 April) was 7 days. Incubation did not begin until the morning of 17 April, the day after the first egg was laid, when a second egg was laid between 0100 and 0730 h. Only one chick hatched from this clutch (Plate 26), doing so between 1000 and 1700 h on 29 April. The unhatched egg contained a one-third- VOL. 28 (3) SEPTEMBER 2011 Breeding Biology of Dusky Honeyeater, NT 103 developed embryo when retrieved from the nest and examined on 1 May. The incubation period, calculated from the start of incubation to the hatching of the only chick, was 12 days 9 h ± 6.5 h. The Jingili nest was checked at irregular intervals; it was empty on 18 July 2009, contained one egg at 1700 h on 22 July, and two eggs at 0730 h on 27 July. Two chicks hatched between 1800 h on 4 August and 1700 h on the following day. Assuming that the second egg was laid between 0600 and 1700 h on the day following the sighting of the first egg, the incubation period was 12 days 18 h ± 17 h. Detailed observations of incubation were undertaken on the mornings of 19 and 20 April at the Wagaman nest, 2 and 3 days, respectively, after incubation began. Nest-attentiveness was 64% on the first morning (257 min. of observation) and 65% on the second morning (101 min. observation), excluding incomplete on- and off-bouts. The mean duration of complete bouts of incubation was 38.0 ± 18.38 minutes (n = 7, range 20–67 min.), and the mean duration of absences was 18.8 ± 9.54 minutes (n = 8, range 4–37 min.). Although not confirmed by banding, incubation appeared to be performed by only one individual, based on consistency of approach and departure actions to and from the nest by the incubating bird. On four occasions a second bird, presumed to be the mate, visited the nest-shrub but did not feed or physically contact the incubating bird. Soft peeping calls, which lasted <1 minute, were heard on three of the visits. On two occasions the incubating bird captured small prey from leaves adjacent to the nest. Although it never preened while on the nest, it regularly preened in the adjacent palm for several minutes either immediately before or after incubating, when it also often gave single-note peet contact calls at intervals of 3–20 seconds. The incubating bird rolled the eggs while sitting, at average intervals of 7.4 ± 5.42 minutes (n = 31, range 1–26 min.); on return to the nest, it did not touch the eggs before starting to incubate. Occasionally this bird perched below and adjusted the outer structure of the nest.

Description of nestlings and parental care The sole chick that hatched at Wagaman (Plate 26) was depredated on 2 May 2008, only 3 days after hatching. The two chicks at the Jingili nest fledged between 0700 and 1700 h on 19 August, giving a nestling period of 14 days 7 h ± 17 h. The hatchlings at both nests were naked except for fine but dense sooty-brown down on the crown, and along the spinal (from the mantle to the upper rump), femoral and humeral feather-tracts. Their translucent skin was predominantly pink with various hues of yellow, red-brown and purple. The enlarged gape-flanges were yellow, and the mouth was yellow with an orange tinge on the upper palate. Within 3 days, the crown, spinal tract and wings had become blackish in colour, and pins of the primaries, secondaries and rectrices had emerged. By Day 4, feathers in pin had appeared on the spinal and humeral tracts, but the eyes were still closed (Plate 27). By Day 9, the eyes were fully open and the wings were mostly covered by pin-feathers, the feathers emerging from all sheaths (up to one-quarter of the length of the pin), except those of the outermost primaries and secondaries and outer primary coverts, mantle and scapulars (Plate 28). The feathers of the forehead and forecrown, rump and tail were still in pin, the last being ~3 mm long. On Day 11, the two chicks weighed 7.7 and 9.8 g, and their tails measured 4.8 mm and 5.4 mm, respectively. By Day 13, they were fully covered with feathers except on the forehead and chin, and the feathers of the forecrown were still AUSTRALIAN 104 NOSKE & CARLSON Field Ornithology ensheathed (Plate 29). The bill was dusky brown, contrasting with the bright-yellow gape-flanges and pale pinkish-yellow skin of the forehead, and the naked skin around the eyes was pale greenish-yellow. At fledging, the birds were identical in appearance, and the bases of the rectrices were still partly ensheathed. There was no hint of red on the feathers on the head, as is sometimes seen in adult Honeyeaters in the NT. The single chick in the Wagaman nest could be heard calling 2 days after hatching, even when the adults were absent. Similarly, the two chicks at the Jingili nest could be heard from the first day of video-recording (Day 3 after hatching). The Wagaman nest was observed for 253 minutes during the nestling period on 1 May 2008, when the single chick was 2 days old. Only one adult brooded, it being distinguished by a small white patch, possibly cobweb, above one eye. The duration of brooding bouts averaged 3.9 ± 2.43 minutes (n = 13, range 1–8 min.), and total duration of brooding comprised only 20% of the observation time. The duration of absences from the nest averaged 13.7 ± 8.67 minutes (n = 12, range 3–35 min.). At the Jingili nest, brooding was observed on 8 (6.0 h observation) and 9 (2.2 h observation) August 2009, when the chicks were 3 and 4 days old, respectively. The duration of brooding bouts on Day 3 averaged 4.24 ± 2.13 minutes (n = 19, range 0.6–8.37 min.), and on Day 4 averaged 4.34 ± 0.88 minutes (n = 6, range 3.37–5.73 min.). Brooding represented 28% of observation time (165 min.) on the morning of Day 3, and 21% on the afternoon of Day 3 and morning of Day 4 (192 and 126 min. observation time, respectively). The duration of absences from the nest over these 2 days averaged 14.05 ± 9.01 minutes (n = 22, range 6–38.6 min.). The frequency of brooding dropped from 3.99 bouts/h on Day 3 to 2.86 bouts/h on Day 4. Brooding during the day stopped by the morning of Day 6 (11 August), although it is possible that night brooding continued for longer. Because one of the attending adults at the Wagaman nest had a white patch above the eye, it was confirmed that the nestling was fed by two different adults. At the Jingili nest, video footage showed feedings by two adults in quick succession on several occasions. No additional adults (i.e. helpers) were evident at the nest. At the Wagaman nest the 2-day-old chick was fed at a rate of 6.4 feeds/h (3.9 h of observation). Of 27 feeding events, 52% involved transfer of a single arthropod, 26% involved regurgitation of a substance, and the remaining 22% were a combination of both. The length of arthropods was estimated to be 2–4mm (based on width of bird’s bill at the tip), with an average length of 3.1 ± 0.76 mm (n = 20). Regurgitation involved 3–5 rapid jabs into the chick’s mouth, with a mean of 3.7 ± 0.75 jabs (n = 13). The mean interval between feeding visits was 9.3 ± 5.96 minutes (n = 26, range 2–28 min.). The chick produced a faecal sac on three occasions (giving a deaecation rate of 0.77 faecal sac/h), within 1 minute of a feed. The faecal sac was consumed by the attending parent before leaving (twice) or while settling on the nest (once). At the Jingili nest, the rate of provisioning increased between Day 3 after hatching (the first day of video-recording) and Day 11, then decreased over the following 2 days (Days 12 and 13), with the young fledging on Day 14 (Figure 2). Feeding rates varied from a minimum of 6.6 feeds/h on the afternoon of Day 3 to a maximum of 12.7 feeds/h on the afternoon of Day 11, with an average rate of 9.1 ± 2.03 feeds/h (n = 13) over the 9 days of sampling (daily sampling time 63–245 min., totalling 29.1 h). There was no significant difference between feeding rates in the morning and in the afternoon of the same day (paired t-test, t = 0.43, d.f. = 5, P = 0.41). On each feeding visit, the adult fed each nestling alternately 2–5 times in rapid succession, possibly regurgitating liquid as it did so. Items fed VOL. 28 (3) SEPTEMBER 2011 Breeding Biology of Dusky Honeyeater, NT 105

Figure 2. Rates of provisioning by adult Dusky Honeyeaters at a nest with two chicks, in Jingili, Darwin (n = 13 observations). Dashed line signifies missing data. to the chicks were seen only on Days 3 and 4 (24% of all feeds), and comprised 13 arthropods, including a moth and a spider. The mean estimated length of arthropods was 13.9 ± 4.9 mm (n = 11), based on comparison with the bird’s bill-length. After feeding the nestlings, an adult at the Jingili nest often perched on the rim of the nest, where it apparently waited for a nestling to defaecate. If a faecal sac was produced, the adult immediately collected it with its bill and flew away with it (faecal sac removal), but if not, the adult moved to another position, from where it vigorously and repeatedly probed beneath the chicks, apparently collecting faecal material (nest-cleaning), which was swallowed if small, or carried away if larger. The latter faecal material appeared to lack the white colour characteristic of the membrane surrounding faecal sacs. The time spent at the nest, excluding brooding bouts and including feeding and nest-cleaning activities, occupied up to 10.5% of observation time (video-recording), averaging 5.4 ± 2.6% (n = 12). Just over half (55.7%) of the non-brooding visits lasted 5–14 seconds, and although the maximum value was 346 seconds the median value was 13 seconds (Figure 3). The mean time spent at the nest during the first 5 days of observations (Days 3–7) did not differ significantly from that during the last 5 days (Days 9–13) (t = –0.76, d.f. = 6, P = 0.48). The hourly rate of removal of faecal sacs varied from 0 on Day 4 (2.1 h of observation) to 0.73 on the morning of Day 3 (2.8 h of observation) and 2.2 on the afternoon of Day 3 (3.2 h of observation); the mean rate of removal over the 8 days of sampling was 1.55 ± 0.61 faecal sacs/h (n = 13). The rate of removal of AUSTRALIAN 106 NOSKE & CARLSON Field Ornithology

Figure 3. Duration (sec.) of visits to the nest by adult Dusky Honeyeaters during the nestling period at the Jingili nest. faecal sacs during the first 5 days did not differ significantly from that during the last 5 days (t = –0.87, d.f. = 5, P = 0.43), nor did rates vary between morning and afternoon (paired t-test, t = 0.99, d.f. = 5, P = 0.80). Nest-cleaning, on the other hand, took place significantly more often during the morning than the afternoon (means 2.95 and 0.12/h, respectively; t = 3.24, d.f. = 9, P = 0.01) and was more frequent during the last 5 days than during the first 5 days of the nestling period, though the difference was barely significant (means 4.76 and 1.43/h, respectively; t = 2.36, d.f. = 7, P = 0.05; only morning samples considered).

Nest defence and wariness of nesting adults The adults at the Wagaman nest displayed remarkable tolerance to disturbance by the observer (AJC), with the incubating bird remaining on the nest during lawn maintenance to within 2 m of the nest-shrub, and the dog walking beneath the shrub. Although remaining on the nest, the bird was observed to point its bill upward when more alarmed. This included human approach and departure from the house, presence of the dog, and excessive noise in the surrounding environment. Several interspecific interactions were witnessed when other birds landed in plants adjacent to the nest. A Red-headed Honeyeater and a Rufous- albogularis foraging in a palm 2.0 m from the nest elicited no obvious response from the incubating Dusky Honeyeater, and a Brown Honeyeater and a Double-barred Finch Taeniopygia bichenovii in a shrub 4.5 m from the nest were each approached with no signs of aggression. In contrast, a White-gaped Honeyeater unicolor visiting the bush was chased from the area. Only the White-gaped Honeyeater is much larger than the Dusky Honeyeater, and presumably posed more of a threat. VOL. 28 (3) SEPTEMBER 2011 Breeding Biology of Dusky Honeyeater, NT 107

Discussion

Breeding season and construction of the nest Although Dusky Honeyeaters have been recorded breeding in all months of the year in the NT, there is a marked peak in laying during the late wet- and early dry-season months of April and May (Figure 1), often referred to as the wet–dry transition. In 1948, Deignan (1964) collected a male specimen with enlarged gonads in Darwin on 19 March, whereas other adults collected on 14–15 April and on 10 October had only slightly enlarged gonads. Noske & Franklin (1999) showed that breeding seasons of in the of the NT were, contrary to the literature, very diverse. Among the honeyeaters, several species bred almost exclusively in the dry season (Red-headed, Brown, White-throated albogularis and Blue-faced Entomyzon cyanotis Honeyeaters), whereas others bred mainly during the wet season (White-gaped and Bar-breasted fasciatus Honeyeaters) (Noske & Franklin 1999). In suburban Darwin, Rufous-banded Honeyeaters bred in all months of the year except June and July, months in which moult was recorded (Noske 1998; RAN unpubl. data). Noske & Franklin (1999) speculated that the breeding season of the Dusky Honeyeater differed from that of the similar-sized Brown Honeyeater (which breeds in the dry season) because the former was less abundant in eucalypt woodlands and , and therefore less dependent on the predominantly dry-season nectar sources in these habitats. The period between the start of nest-construction and laying (7 days) at the Wagaman nest is consistent with the 8 days reported for a smaller congener, the Scarlet Honeyeater Myzomela sanguinolenta (Higgins et al. 2001). For the slightly smaller Brown-backed Honeyeater Ramsayornis modestus of northern Queensland, nest-construction takes 4–8 days, and laying begins 1–9 days after completion of the nest, with a mean interval of 3.8 days between nest completion and laying (Maher 1988). The nest of the Brown-backed Honeyeater is much larger than that of the Dusky Honeyeater, but is composed almost entirely of bark from paperbarks Melaleuca spp. (Higgins et al. 2001). The dimensions of the Wagaman nest are almost identical to those of a nest described by North (cited in Higgins et al. 2001), which had an external diameter and depth of 64 and 44 mm, respectively, and internal diameter and depth of 44 and 38 mm, respectively; compared with these two nests, the Jingili nest was 16–18 mm deeper externally and 7–12 mm deeper internally. Consistent with the early literature (see Higgins et al. 2001), the Wagaman and Jingili nests were frail structures with gaps in the walls through which the contents could be seen, and were lined with fine grass. Our data suggest that clutch-size in the NT is probably normally two, but as the Wagaman nest shows, not all clutches produce two nestlings. Unlike the closely related Scarlet Honeyeater, there is no evidence for clutches of three in this species (Higgins et al. 2001).

Incubation, nestling morphology and brooding The consistency of approach and departure to and from the nest by the incubating or brooding bird at both the Wagaman and Jingili nests, the lack of observed change-overs, and the moderately low level of attentiveness at the Wagaman nest (65%), indicate that one adult, presumably the female, incubates and broods in this species, as is the norm for most Australian honeyeaters studied to date (see Higgins et al. 2001, 2008). Although male Dusky Honeyeaters are AUSTRALIAN 108 NOSKE & CARLSON Field Ornithology larger and heavier than females (Higgins et al. 2001), the difference in size was not sufficient to distinguish the sexes at the Jingili nest, nor were there any discernible differences in plumage coloration or feather wear. The incubation periods of 12.4 and 12.75 days at the two nests are ~1 day longer than the 11–12-day incubation period reported for the Scarlet Honeyeater (Wolstenholme 1930), but shorter than the incubation periods of the Brown (13–13.5 days: Franklin & Noske 2000), Rufous-banded (14.3 days: Noske 1998), Black Sugomel niger (14.8 days: Higgins et al. 2001) and Brown-backed (~15 days: Maher 1986, 1988) Honeyeaters. Our determination of nest-attentiveness for the Dusky Honeyeater (65%) is based on a very small sample size, yet it is consistent with values for the few other honeyeater species for which nest-attentiveness has been recorded. Female Crescent Honeyeaters pyrrhopterus reduced their attentiveness from 79.5 to 66.6% between the early and late stages of the incubation period (Clarke & Clarke 1999). New Holland P. novaehollandiae and White-naped Melithreptus lunatus Honeyeaters spent comparable times (66.9% and 77%, respectively) on the nest during the incubation period (Paton 1979; Marchant 1986). In Darwin, nest-attentiveness of Brown Honeyeaters at three nests varied from 53 to 67% (54 h observation), but the variation was not related to stage of incubation (RAN unpubl. data). The nestling period at the Jingili nest (14.3 ± 0.7 days) is similar to the nestling periods of the Brown and Rufous-banded Honeyeaters (~13 days and 14.2 days, respectively: Noske 1998; Franklin & Noske 2000), yet apparently much longer than that of the closely related Scarlet Honeyeater (~11–12 days: Wolstenholme 1930), and shorter than that of the (15.6 days: Higgins et al. 2001). More detailed studies of myzomeline honeyeaters would be useful to place the incubation and nestling periods of the Dusky Honeyeater in context. The presence of down on hatchling Dusky Honeyeaters is apparently inconsistent with most honeyeaters, which are said to be naked when they hatch, acquiring grey down on the upperparts between 2 and 5 days after hatching (data for 12 species among six genera: Higgins et al. 2001). However, the Black Honeyeater is purported to hatch with down on the head, back, nape and sides (Higgins et al. 2001). Whereas Franklin & Noske (2000) stated that hatchling Brown Honeyeaters were naked at hatching, with obvious down on the second day, photographs of hatchlings (RAN unpubl. data 2006) clearly show that they have dense tufts of pale down on the frontal (forecrown), occipital, dorsal (spinal), humeral, alar and femoral tracts. In contrast, photographs of Rufous-banded Honeyeater hatchlings at several nests in Darwin show that nestlings develop feather quills by Day 3 after hatching, without any trace of antecedent down (RAN & AC unpubl. data), contrary to information in the NRS, which suggests that these nestlings develop down at 8–9 days old (Higgins et al. 2001). Similarly, the Brown-backed Honeyeater does not develop down, with feather quills emerging from the alar (wing) tract on Day 2 and from the spinal and humeral tracts on Day 3 (Maher 1986). The appearance of down 2–5 days after hatching, as reported in most honeyeaters, is unexpected in terms of its assumed thermoregulatory function. Clearly the occurrence and ontogeny of neossoptiles (natal down) among honeyeaters requires further detailed study, as does an assessment of its taxonomic significance. The mean duration of daytime brooding bouts was ~4 minutes and occupied a total of 20–28% of observation time at both closely observed Darwin nests, but this brooding apparently stopped after Day 4 or 5. In the cooler climate of VOL. 28 (3) SEPTEMBER 2011 Breeding Biology of Dusky Honeyeater, NT 109

Table 1 Rates of food provisioning to nestlings by some small honeyeaters (Meliphagidae). Weights are taken from Higgins et al. (2001); minimum and maximum rates in italics are mean values for youngest and oldest nestling stages; n = number hours of observation. Species Weight Food provisioning per hour Source (g) Min. Max. Mean n

Rufous-throated Honeyeater 11 40.0 15.0 Immelmann Conopophila rufogularis (1961) Brown-backed Honeyeater 11 9.0 28.0 20.3 76.8 Maher (1996) Ramsayornis modestus Eastern 11 16.6 25.3 19.1 2.6 higgins et al. Acanthorhynchus tenuirostris (2001) Dusky Honeyeater 13 6.6 12.7 9.1 29.1 This study Myzomela obscura (Jingili nest) White-naped Honeyeater 14 12.0 35.0 25.6 17 Marchant Melithreptus lunatus (1986) 16 6–8a 71 Clarke & Phylidonyris pyrrhopterus Clarke (1999) 16.5 17.7 26.0 21.4 84 dunkerley Lichenostomus fuscus (1989) Yellow-faced Honeyeaterb 17 7.9 17.9 15.0 100+ Clarke et al. L. chrysops (2003) 34 6.4 22.8 14.2 17.2 Franklin et al. L. melanops cassidix (1995) aRange represents means for early and late nestling stages bValues extrapolated from graphs or text, combining sexes south-eastern Australia, daytime brooding appears to continue for longer, and may occupy more time each day. A female White-naped Honeyeater brooded for 55% of observation time during the early stages of the nestling period, <1% on Day 9, and not at all thereafter (Marchant 1986). Similarly, the mean proportion of time spent brooding by female Crescent Honeyeaters was ~50% on Day 1, but steadily declined until Day 8, when brooding had almost stopped (Clarke & Clarke 1999). Yellow-faced Honeyeaters Lichenostomus chrysops also brooded for at least 8 days, with the frequency of brooding bouts decreasing significantly with time (Clarke et al. 2003). In contrast, Brown-backed Honeyeaters of tropical north-eastern Queensland appear to have almost relinquished daytime brooding, as Maher (1996) witnessed it only six times during 76.8 h of observation, and five of these bouts lasted <1 minute. Lack of brooding in that species is probably at least partly related to its atypical nest, which is domed, with thick walls of paperbark, and thus well insulated, unlike the cup-shaped nests of all other honeyeaters (except its single congener: Higgins et al. 2008). Although average maximum temperatures in Townsville were 5°C lower than in Darwin (33.4°C and 28.4°C, respectively: Maher 1996), temperatures within domed nests vary considerably less than those in cup-shaped nests (RAN unpubl. data).

Care of nestlings The rate of food provisioning reported here for the Dusky Honeyeater is less than half that of the slightly smaller tropical Brown-backed and Rufous- throated Conopophila rufogularis Honeyeaters. It is also substantially lower than AUSTRALIAN 110 NOSKE & CARLSON Field Ornithology that of larger honeyeater species in temperate Australia, except for the Crescent Honeyeater (Table 1). As in the present study, rates of parental provisioning by Brown-backed, Crescent and Yellow-faced Honeyeaters did not vary significantly with the age of their nestlings (Maher 1996; Clarke & Clarke 1999; Clarke et al. 2003), whereas in Fuscous Lichenostomus fuscus and Helmeted L. melanops cassidix Honeyeaters provisioning rates increased significantly with nestling age (Dunkerley 1989; Franklin et al. 1995). In the wet tropics of Queensland, Maher (1996) attributed the striking difference between the rates of food provisioning by Olive-backed Nectarinia jugularis and Brown-backed Honeyeaters (4.2 versus 20.3 feeds/h) to the type of food delivered to nestlings. Brown-backed Honeyeaters (both male and female) carried single large or several small invertebrates in their bills and fed one nestling at a time during brief visits lasting 2–3 seconds, whereas in the the female fed nestlings several times during comparatively long visits of 5–35 seconds (mean 14.4 sec.) by inserting her bill into their mouths and regurgitating nectar from the stomach using rapid pumping head movements; food was rarely carried in the bill. In the present study, the Dusky Honeyeater resembled the Sunbird more than the Brown-backed Honeyeater, spending up to 346 seconds (mean 22 sec.) at the nest during feeding visits, and feeding two nestlings with rapid, multiple jabs into their mouths on each feeding visit. The jabbing form of food delivery and the lack of discernible food items in the adults’ bills from the first few days after the chicks hatched strongly suggest that the Dusky Honeyeater feeds its young predominantly on nectar. Efficient growth of nestlings normally requires a high-protein diet, so most bird species feed their nestlings with vertebrate or arthropod prey, or both (O’Connor 1984), even when the adults feed largely on a non-protein, carbohydrate-rich diet, such as in the nectarivorous (Trochilidae) and sunbirds (Nectariniidae) (Markman et al. 1999). However, Paton (1979, 1982) found that New Holland Honeyeaters delivered both insects and regurgitated nectar to nestlings in the same feed. Similarly, Crescent Honeyeaters delivered liquid and invertebrates to their nestlings equally frequently (Clarke & Clarke 1999). Even White-naped Honeyeaters, which are considered primarily insectivorous as adults (Ford & Paton 1977), appear to feed nectar to their young. At one nest of this species, Marchant (1986) believed that nectar was involved in 43.5% of provisioning visits (n = 216 visits), during which the two young were fed simultaneously, whereas insects were fed singly to each nestling on the remaining visits (56.5%). Moreover, provisioning of both nestlings, rather than one, on each nest-visit occurred less frequently during the last 2–3 days of the nestling period than during the first 14 days, suggesting an increasing number of insects in the diet of nestlings as they approached fledging (Marchant 1986). In contrast with the White-naped Honeyeater, Dusky Honeyeaters appear to feed more nectar and fewer large insects to older nestlings than to younger nestlings. On the first two days of observation (Days 3 and 4) at the Jingili nest, larger arthropods were brought to the nest on at least 24% of feeding visits, but none was seen on feeding visits during the following 7 days. Thus, it appeared that discernible arthropods were fed to nestlings during their first 4 days only, and that nectar, and presumably small arthropods, formed the diet for the rest of the nestling period. Regent Honeyeaters phrygia fed their nestlings mostly with insects (58%), the rest being carbohydrates (nectar and lerp); fledglings, on the other hand, were fed mainly carbohydrates (61.2%) (Oliver 1998). Over half of VOL. 28 (3) SEPTEMBER 2011 Breeding Biology of Dusky Honeyeater, NT 111 the items brought to nestling Bell Miners melanophrys were lerp, and the proportion of lerp delivered increased with nestling age (Poiani 1993, 1997; te Marvelde et al. 2009). That small insects remained an important component of the diet of nestling Dusky Honeyeaters is indicated by the fairly consistent rate of faecal sac removal over the whole nestling period at the Jingili nest. The mean rate of faecal sac removal (1.6 sacs/h) was similar to that of the Brown-backed Honeyeater (1.0–1.9 /h) and Olive-backed Sunbird (0.7–1.5/h) in the Australian wet tropics (Maher 1996). However, nest-cleaning increased significantly in frequency between the first and second halves of the nestling period, and involved the ingestion or removal of faecal material that had presumably not been collected by the adults when defaecated, perhaps as a result of infrequent parental visits or because the material was not enclosed within a membrane. Hummingbirds also feed their young nectar, but their nestlings are able to forcefully eject their own faecal material from the nest (Schuchmann 1999). It is possible that the predominantly liquid diet of the Dusky Honeyeater nestlings resulted in much soiling of the nest with indigestible arthropod remains and other waste products. The reason for the low rate of food provisioning of the Dusky Honeyeater remains a mystery. Maher (1996) argued that the low activity level at nests of the Olive-backed Sunbird might be beneficial in reducing the risk of attracting attention from visually oriented nest-predators, yet he found no difference between the daily survival rate of nestlings of this species and that of co-existing Brown-backed Honeyeaters, which showed five times as much activity (Maher 1996). Indeed, nesting success of the Crescent Honeyeater, which presumably has similar levels of activity at the nest as the Dusky Honeyeater (see Table 1), experienced lower nesting success than that reported for other honeyeater species (Table 1; Clarke & Clarke 2000). Tropical passerines typically show lower rates of visitation to the nest than do temperate-zone passerines (Stutchbury & Morton 2001), but this comes at the expense of slower nestling development and, consequently, a longer nestling period. The nestling period of the Dusky Honeyeater, however, is no longer than in other honeyeater species of similar size, which suggests that the nectar fed to their nestlings is either exceptionally rich in sugars (e.g. hexoses) or it can be more efficiently digested. Such hypotheses await further studies.

Acknowledgements Special thanks go to Bryan Baker for allowing his Jingili house to become a video- recording studio and for his diligence in setting up the recorder on each of 9 sampling days for up to 3 hours. Special thanks also go to Vicki Carlson, who made opportunistic observations of the Wagaman nest throughout the day and night between work commitments. Thanks to Marc Gardner and Niven McCrie for their breeding records.

References Boekel, C. (1976), ‘Ten months on Gove Peninsula’, Australian Bird Watcher 6, 231–245. Brooker, M.G. & Parker, B.S. (1985), ‘The birds of Kakadu National Park’, pp. 327–388 in Braithwaite, R.W. (Ed.), The Kakadu Fauna Survey: An Ecological Survey of Kakadu National Park, vol. 2, Final Report to Australian National Parks & Wildlife Service, CSIRO Division of Wildlife & Rangelands Research, Darwin. Brooker, M.G., Braithwaite, R.W. & Estbergs, J.A. (1990), ‘Foraging ecology of some insectivorous and nectarivorous species of birds in forests and woodlands of the Wet–Dry Tropics of Australia’, Emu 90, 215–230. Clarke, R.H. & Clarke, M.F. (1999), ‘The social organization of a sexually dimorphic honeyeater – the Crescent Honeyeater Phylidonyris pyrrhoptera, at Wilsons Promontory, Victoria’, Australian Journal of Ecology 204, 604–654. AUSTRALIAN 112 NOSKE & CARLSON Field Ornithology

Clarke, R.H. & Clarke, M.F. (2000), ‘The breeding biology of the Crescent Honeyeater Phylidonyris pyrrhoptera at Wilsons Promontory, Victoria’, Emu 100, 115–124. Clarke, M.F., Schipper, C., Boulton, R. & Ewen, J. (2003), ‘The social organization and breeding behaviour of the Yellow-faced Honeyeater Lichenostomus chrysops – a migratory from the Southern Hemisphere’, Ibis 145, 611–623. Conway, C.J. & Martin, T.E. (2000), ‘Evolution of passerine incubation behaviour: Influence of food, temperature and nest predation’, Evolution 54, 670–685. Crawford, D.N. (1972), ‘Birds of Darwin area, with some records from other parts of Northern Territory’, Emu 72, 131–148. Deignan, H.G. (1964), ‘Birds of the Arnhem Land Expedition’, pp. 345–425 in Specht, R.L. (Ed.), Records of the American–Australian Expedition to Arnhem Land, vol. 4, Melbourne University Press, Melbourne. Dunkerley, G.M. (1989), The Fuscous Honeyeater: Food Resources and the Bird Community, PhD thesis, University of New England, Armidale, NSW. Ford, H.A. & Paton, D.C. (1977), ‘The comparative ecology of ten species of honeyeaters in South Australia’, Australian Journal of Ecology 2, 399–407. Franklin, D.C. & Noske, R.A. (1998), ‘Local movements of honeyeaters in a sub-coastal vegetation mosaic in the Northern Territory’, Corella 22, 97–103. Franklin, D.C. & Noske, R.A. (2000), ‘The nesting biology of the Brown Honeyeater Lichmera indistincta, in the Darwin region of northern Australia, with notes on nest- flooding’, Corella 24, 38–44. Franklin, D.C., Smales, I.J., Miller, M.A. & Menkhorst, P.W. (1995), ‘The reproductive biology of the Helmeted Honeyeater Lichenostomus melanops cassidix’, Wildlife Research 22, 173–191. Higgins, P.J., Christidis, L. & Ford, H.A. (2008), ‘Family Meliphagidae (Honeyeaters)’, pp. 498–691 in del Hoyo, J., Elliott, A. & Christie, D.A. (Eds), Handbook of the Birds of the World, vol. 13, Lynx Edicions, Barcelona. Higgins, P.J., Peter, J.M. & Steele, W.K. (Eds) (2001), Handbook of Australian, and Antarctic Birds, vol. 5, Oxford University Press, Melbourne. Immelmann, K. (1961), ‘A contribution to the biology and ethology of Australian honeyeaters (Meliphagidae)’, Zeitschrift für Ornithologie 102, 164–207 [in German]. Langkamp, P.J., Dalling, M.J., Calder, D.M. & Farrell, T.P. (1979), ‘Studies on the rehabilitation of mined areas on Groote Eylandt, Northern Territory’, Reclamation Review 2, 147–155. Maher, W.J. (1986), ‘Growth & development of the Brown-backed Honeyeater Ramsayornis modestus in north Queensland’, Emu 86, 245–248. Maher, W.J. (1988), ‘Breeding biology of the Brown-backed Honeyeater Ramsayornis modestus (Meliphagidae) in northern Queensland’, Emu 88, 190–194. Maher, W.J. (1996), ‘Nestling food and feeding frequencies of the Brown-backed Honeyeater Ramsayornis modestus and the Yellow-bellied Sunbird Nectarinia jugularis in northern Queensland’, Emu 96, 17–22. Marchant, S. (1980), ‘Incubation and nestling periods of some Australian birds’, Corella 4, 30–32. Marchant, S. (1986), ‘Nesting notes on the White-naped Honeyeater’, Australian Birds 20, 52–55. Markman, S., Pinshow, B. & Wright, J. (1999),‘Orange-tufted Sunbirds do not feed nectar to their chicks’, Auk 116, 257–259. Noske, R.A. (1998), ‘Breeding biology, demography and success of the rufous-banded honeyeater, Conopophila albogularis, in Darwin, a monsoonal tropical city’, Wildlife Research 25, 339–356. Noske, R.A. & Franklin, D.C. (1999), ‘Breeding seasons of land birds in the Australian monsoonal tropics: Diverse responses to a highly seasonal environment’, Australian Biologist 12, 72–90. O’Connor, R.J. (1984), The Growth and Development of Birds, J. Wiley, New York. Officer, H.R. (1976), ‘Ten days observations of the birds of Gove Penisula [sic]’, Australian Bird Watcher 6, 223–228. Oliver, D.L. (1998), ‘The importance of insects and lerp in the diet of juvenile regent honeyeaters, Xanthomyza phrygia: Implications for the conservation of an endangered woodland bird’, Wildlife Research 25, 409–417. Paton, D.C. (1979), The Behaviour and Feeding Ecology of the , Phylidonyris novaehollandiae, in Victoria, PhD thesis, Monash University, Melbourne. VOL. 28 (3) SEPTEMBER 2011 Breeding Biology of Dusky Honeyeater, NT 113

Paton, D.C. (1982), ‘The diet of the New Holland honeyeater Phylidonyris novaehollandiae’, Australian Journal of Ecology 7, 279–298. Poiani, A. (1993), ‘Bell Miners: What kind of farmers are they?’, Emu 93, 188–194. Poiani, A. (1997), ‘Prey delivered to nestlings: Is there division of labour among nest attendants?’, Emu 97, 87–90. Rix, C.E. (1970), ‘Birds of the Northern Territory’, South Australian Ornithologist 25, 147–191. Schuchmann, K.L (1999), ‘Family Trochilidae (Hummingbirds)’, pp. 468–680 in del Hoyo, J., Elliott, A. & Sargatal, J. (Eds), Handbook of the Birds of the World, vol. 5, Lynx Edicions, Barcelona. Stutchbury, B.J.M. & Morton, E.S. (2001), Behavioural Ecology of Tropical Birds, Academic Press, San Diego, California, USA. te Marvelde, L., McDonald, P.G., Kazem, A.J.N. & Wright, J. (2009), ‘Do helpers really help? Provisioning biomass and prey type effects on nestling growth in the cooperative bell miner’, Behaviour 77, 727–735. Woinarski, J.C.Z. (1993), ‘A cut-and-paste community: Birds of monsoon rainforests in Kakadu National Park, Northern Territory’, Emu 93, 100–120. Woinarski, J.C.Z., Tidemann, S.C. & Kerrin, S. (1988), ‘Birds in a tropical mosaic: The distribution of bird species in relation to vegetation patterns’, Australian Wildlife Research 15, 171–196. Wolstenholme, H. (1930), ‘Triple nesting of the Scarlet Honeyeater’, Emu 29, 264–266.

Received 29 October 2010 

Correction: Shrike-thrush and tree-frog In the recent item on a Little Shrike-thrush Colluricincla megarhyncha hunting a tree-frog (Baird 2011, Australian Field Ornithology 28, 51–52), the frog was identified as an Orange-thighed Tree-Frog Litoria xanthomera (not xanthocera as misspelt). Eric Vanderduys (CSIRO Ecosystem Sciences and author of a forthcoming field-guide to Queensland frogs) has re-identified the frog as the similar Graceful Tree-Frog L. gracilenta. Thanks to Eric for these corrections; publication of a frog photograph in a bird journal was therefore justified! Stephen Debus