152 AUSTRALIAN FIELD ORNITHOLOGY 2006, 23, 152–158 Observations of Predation, Nest-predation and Other Disturbance Events at Dryandra, South-western Australia II: as Prey of Other

GRAHAM R. FULTON School of Natural Sciences, Centre for Ecosystem Management, Edith Cowan University, 100 Joondalup Drive, Joondalup, Western Australia 6027 (Email: [email protected])

Summary I describe nine predation, nest-predation and disturbance events: four by ants, four by the South-western Carpet Python Morelia spilota imbricata and one by the Bilby Macrotis lagotis. Predation by ants was more important on or near the ground, and Greenslade’s Meat Ant Iridomyrmex greensladei was responsible for three of the four events. The Carpet Python took Rainbow Bee-eater Merops ornatus nestlings from a burrow, and free-flying Australian Ringnecks Barnardius zonarius from the tree-canopy and from the ground. The Bilby dug out a Bee-eater’s burrow, which it either depredated or from which it caused the nestlings to fledge prematurely. All observations were made at Dryandra Woodland, a 27 000-ha remnant of woodland, with an almost full community of animals that have declined or disappeared from the surrounding wheatbelt, 160 km south-east of Perth, Western Australia. The context of each event is discussed in relation to the broader background of a 3-year community-wide study of Dryandra’s birds, which involved continuous monitoring throughout each breeding season.

Introduction The identity of nest-predators is still poorly documented in Australia, although a few important nest-predators such as ravens Corvus spp., Pied Currawong Strepera graculina, Grey Shrike-thrush Colluricincla harmonica and Common Brushtail Possum Trichosurus vulpecula have been identified (Major et al. 1996, 1999; Fulton & Ford 2001; Berry 2002; Piper et al. 2002; Zanette 2002; Fulton in press). This paper presents accounts of predation, nest-predation and other disturbance events by a suite of less well-known and non-avian predators; although as individual species these are not considered important predators, they were collectively important at Dryandra Woodland, south-western Australia. The context surrounding each predation event is given and the diversity of predators identified at Dryandra Woodland is expanded (for details see Fulton 2006). Predators identified in this paper include the South-western Carpet Python Morelia spilota imbricata, which is listed as Schedule 4 specially protected fauna (Edwards 2005), and vulnerable (Cogger et al. 1993); Greenslade’s Meat Ant Iridomyrmex greensladei and Black- headed Sugar Ant Camponotus nigriceps; and the Bilby Macrotis lagotis, which is listed as Vulnerable C2a and Schedule 1, rare or likely to become extinct (IUCN 2004; Edwards 2005).

Methods Scientific and common names for mammals were taken from Strahan (2002); for ants from McArthur & Adams (1996), Shattuck (1999) and Andersen (2002); pythons from Cogger (1996); and birds from Christidis & Boles (1994). The date format used here is dd/mm/yy. The study site (Dryandra Woodland south-east of Perth, Western Australia) is described elsewhere (Fulton 2006). I spent most daylight hours in the field each day throughout the breeding season (August to January inclusive) for three years, 2002–03, 2003–04 and 2004–05. Pythons in VOL. 23 (3) Observations of Predation II: SEPTEMBER 2006Birds as Prey of Other Animals 153 a house garden were observed from the cottage, which acted as a hide. Other observations of pythons were made opportunistically while observing birds (see Fulton 2006 for details of observations). Bilby diggings were compared with known Bilby diggings at Dryandra and with descriptions by Johnson (1989). Rainbow Bee-eater Merops ornatus nests were monitored by placing small sticks in the tunnel’s entrance; if these were moved the adult Bee-eater was presumed to have been to the nest. This approach was combined with listening for young in the nest when the nests had nestlings. Measurements of Bee-eater nest-burrows and observations of the chambers’ contents were made after the young had fledged or the breeding attempt failed. Ant specimens were collected at the site in a dry container and placed in 70% alcohol at the end of the day. Identifications were confirmed by Archie McArthur for the Black-headed Sugar Ant and by Brian Heterick for Greenslade’s Meat Ant.

Results and discussion

Ants attacking birds 1. 12/1/04 Black-headed Sugar Ants killed nestlings or inadvertently caused a Rainbow Bee-eater brood to fledge prematurely. This Bee-eater’s burrow was 118 cm long and 32 cm below the surface at the base of the nest-chamber. Burrows at Dryandra are dug into flat sandy soil in low-lying areas (unpublished data). Sugar ants Camponotus spp., not regarded as aggressive, are general scavengers that collect nectar and plant secretions, and tend Hemiptera for honeydew (Briese & Macauley 1981). In this case, they may have simply built their nest on top of the Bee-eater burrow. Upon excavation (5/2/04), the Bee- eater nest-chamber was found to have collapsed and was full of Black-headed Sugar Ants. A small amount of avian skeletal and feather remains was also detected. It is not known whether the adult Bee-eaters stopped coming to the nest because the nestlings were dead or because there were too many ants with which to contend. The Sugar Ants were first detected building their nest on 9/1/04, when detritus began to appear at the opening of the Bee-eaters’ nest-tunnel along with a few live worker ants. The Bee-eaters’ nest was active until 11/1/04, with adult birds still coming to their nest although detritus levels were increasing at the nest opening. Adult Bee-eaters stopped coming to the nest on 12/1/04. No fledglings were detected near this nest and the young were not due to fledge for another 12 days (based on averages of nests that fledged young). This is likely to be an unusual event: Black-headed Sugar Ants or any other sugar ants have not, to my knowledge, previously been reported taking vertebrates as food. Adult sugar ants are not able to ingest solid food particles of any size, although in this case the ants may have dismembered the small chicks to feed to their larvae (Brian Heterick and Archie McArthur pers. comm.). Adult sugar ants feed on carbohydrate, and their larvae are fed on protein (Briese & Macauley 1981; A. McArthur pers. comm.). The larvae exist for only a short period in the annual cycle, which varies with each species (A. McArthur pers. comm.). Similarly, Bee-eater nestlings are present underground for only a short period each year. Future research could therefore investigate whether the presence of sugar ant larvae coincides with the brooding of Bee-eaters, and report occurrences of sugar ants nesting in Bee-eater burrows. At Dryandra 59 Bee-eater nests were monitored, and only this one failed on account of the actions of any ant species. 2. 18/12/04 Greenslade’s Meat Ants attempted predation of one of two Common Bronzewing Phaps chalcoptera nestlings that fledged as I approached the nest. One fledgling flew out of sight and the other flapped to the ground near the nest. As I attempted to pick it up to replace it in its nest, hundreds of Greenslade’s Meat Ants swarmed onto my hand and the fledgling. The fledgling AUSTRALIAN 154FULTON FIELD ORNITHOLOGY

was eventually returned to the nest safely, after the ants had been brushed off. The ants had gathered around the fledgling’s eyes, legs and on its soft fleshy cere, taking hold with their mandibles and contorting their bodies, apparently attempting to tear its flesh. Had the fledgling been left on the ground with the ants, they may have killed it. It remains to be established whether fledglings in similar situations can fend for themselves and survive, or whether the ants can kill them. 3. 15/12/02 A Common Quail Coturnix coturnix egg in an artificial ground nest was broken by a primary (i.e. initial) predator, with the yolk and most of the egg-white remaining. Greenslade’s Meat Ants ate the contents of the egg after the shell had been broken; that is, they were opportunistic secondary consumers. Although meat ants are well recorded as scavengers and detritivores in Australia (Read & Wilson 2004), there appears to be a dearth of information on their use of birds’ eggs. This observation indicates that they are interested in eggs. Broken and partially consumed eggs have been reported in many studies of nesting birds (e.g. Hobbs 1990; Picman 1992; Zannette 1997), indicating that ants would experience such events at natural nests. 4. 21/10/02 Greenslade’s Meat Ants killed two Yellow-plumed Honeyeater Lichenostomus ornatus nestlings 2–3 days from fledging. The Honeyeater nest was 3 m from the ground and hung in a cluster of leaves at terminal branches, as is typical for Yellow-plumed Honeyeaters (unpublished data). It was detected on 15/10/02 and monitored on 17, 19 and 21/10/02; the nestlings appeared in good health before being found mostly eaten away, with Meat Ants swarming over them, on 21/10/02. There had been three nestlings when last monitored, but only two carcasses were present on the last day; the missing nestling may have fallen out of the nest attempting to escape the ants, or may have been taken by another predator. Predation by Meat Ants is more likely than death by disease, because the nestlings appeared in good condition at each observation. My presence apparently did not cause the nest to be abandoned, because I had visited it three times previously and the adults had kept feeding the nestlings and gave no discernible reaction to me. In addition, I monitored 66 Yellow-plumed Honeyeater nests and none was abandoned at the nestling or egg stage, or failed from disease (unpublished data). Since two adults had been feeding the nestlings, it is improbable that both adults had died and orphaned the nestlings. One might desert if it lost its partner, although the nestlings were close to fledging and this may have prompted a single adult to continue feeding the young. Greenslade’s Meat Ants forage on the ground and in the tree-canopy at Dryandra (pers. obs). Meat and tyrant ants Iridomyrmex spp. are more likely to be detected in the canopy when the canopy is close to the ground, as in Australian woodlands (Andersen & Yen 1992). Despite the presence of this aggressive ant in the canopy of trees at Dryandra, it is not thought to be an important predator at arboreal nests. I monitored 477 arboreal bird nests at Dryandra and encountered ant predation at an arboreal nest only on this occasion.

Pythons preying on birds 5. 19/12/02, 1910 h A 95-cm South-western Carpet Python apparently took at least three Rainbow Bee-eater nestlings. The Python was found coiled alongside the burrow opening in the sun; three distinct lumps were counted in its body. It re-entered the burrow after 5 minutes, its whole body disappearing from view. The burrow was excavated the next morning, and there were no signs in VOL. 23 (3) Observations of Predation II: SEPTEMBER 2006Birds as Prey of Other Animals 155

or around the burrow that indicated any disturbance, nor were there any sightings of adult Bee-eaters in the area. Invertebrate remains inside the nest- chamber were consistent with the nestlings having been there. In Victoria, Eastern Brown Snakes Pseudonaja textilis were detected in and near Bee-eater burrows and may have been responsible for the predation of nestlings and one breeding adult; no signs of predators were left at these nests (Lill 1993). Adult Bee-eaters do not roost with their large nestlings overnight (Filewood et al. 1978), although one bird must stay overnight to incubate eggs and brood newly hatched young. The apparent ease with which this Python was able to rob the Bee-eater’s nest indicates why adult Bee-eaters generally do not roost inside their burrows, which have no escape tunnel. However, Alan Lill (pers. comm.) has seen two adult Bee-eaters emerge at dawn from nests that contained older nestlings, indicating that sometimes they do roost in the burrows. 6. 19/11/02 A South-western Carpet Python, ~90 cm long, caught an adult Australian Ringneck Barnardius zonarius in the canopy of a Wandoo Eucalyptus wandoo tree. Carpet and Diamond Pythons Morelia spilota have been described as ambush predators (Slip & Shine 1988). In this event the Carpet Python positioned itself as if it were a branch in the tree-canopy, and then snatched a Ringneck that came within reach. The bird was killed within 1 minute by constriction, and hence asphyxiation. Constriction was also used to minimise the girth of the Ringneck, by compressing it at the shoulders, to aid swallowing. The Python caught the bird at 1020 h, and had swallowed its head by 1040 h, then its neck, part of its upper breast and the shoulder of one wing by 1055 h. However, at 1117 h, 57 minutes after capture, the Ringneck was dropped: it may have proven too much to swallow. The Python then relocated its jaw by knocking it against a knot in the branch, and resumed its ambush posture. The Ringneck carcass was recovered and measured (36.5 cm long from tip of beak to tip of tail). Many birds responded to the attack by group-mobbing the Python, including Dusky Woodswallows Artamus cyanopterus, Ringnecks, Yellow- plumed Honeyeaters, Willie Wagtails Rhipidura leucophrys and White-browed Babblers Pomatostomus superciliosus. One Willie Wagtail made contact at least twice with the Python. Loop et al. (1995) described two successful ambush attacks on Bee-eaters, in the tree-canopy, by an Amethystine Python Morelia amethystina. 7. 29/12/04 and 25/1/05 A female South-western Carpet Python caught two adult Australian Ringnecks at water-containers in the garden. The 2.3-m Python was monitored at 12 water-containers, which ranged from shallow 5-cm bird- baths to plastic containers up to 40 cm deep, over 11 observation periods, for a total of 690 minutes (mean 63 minutes; standard error 10.8 minutes) from 27/12/04 to 25/1/05. It positioned itself either alongside a container with its head resting on the edge, or coiled within, with its snout just out of the water. It was observed to make a total of nine strikes: six on Ringnecks, two on Little Wattlebirds Anthochaera chrysoptera and one at a young 40-cm-tall Western Grey Kangaroo Macropus fuliginosus. Carpet and Diamond Pythons reportedly take mammalian prey as big as wallabies and possums (Slip & Shine 1988; Pearson 2002), and birds ranging in size from Common Bronzewings to Purple- crowned Lorikeets Glossopsitta porphyrocephala. Birds make up 17% of their diet (Pearson et al. 2002). This Carpet Python appeared old and in poor condition, and may not have been able to catch smaller, more agile birds (or a 40-cm-tall kangaroo) that came to the water-containers. It was thought to be a territorial female that had been resident for many years in the woodland village. The Ringnecks appeared to be the least agile birds and the easiest prey (pers. AUSTRALIAN 156FULTON FIELD ORNITHOLOGY

obs.). The Python moved between water-containers where birds gathered to position itself for ambush at them. Slip & Shine (1988) reported that the Diamond Python positions itself along mammal runways and adopts an ambush posture to capture mammals, and suggested that its predominantly mammalian diet indicates that it is primarily a nocturnal predator. The Carpet Python described here took diurnal prey; although it positioned itself overnight on some occasions, the abundance of avian prey and/or the apparent age of this python, however, may have motivated it to adopt a more diurnal strategy.

Mammal depredating birds 8. 21/1/04 A Bilby either took Rainbow Bee-eater nestlings, or caused them to be preyed upon or to fledge prematurely by opening the burrow. The Bee- eater nest had been monitored since 30/12/03; it was last seen active on 18/1/04, with adults feeding nestlings and staying inside the burrow for periods of up to 30 seconds. If the Bee-eater young were ready to fledge, the fittest would have come to the entrance to take food from the adults, and the adults would not have stayed so long in the burrow (pers. obs.). The Bee-eater nest had been dug up from several directions; the largest hole was dug into the burrow just in front of the nest-chamber, and invertebrate remains were visible within. The digging is consistent with Bilby, in that the excavations were circular and straight with sand evenly spread around the excavation. Bilbies are opportunistic dietary generalists with a preference for termites and ants, possibly because these live in colonies and offer a concentrated food source (Smyth & Philpott 1968; Gibson 2001). At Dryandra, Bee-eaters take at least 95% European Honeybees Apis mellifera, with hundreds of invertebrate bodies accumulating inside their nest-chambers (Fulton & Rose unpublished data). The Bilby may have responded to the scent of the invertebrates from the nest-chamber and not to the Bee-eater nestlings. Opening of the Bee-eaters’ nest probably led to the demise of the nestlings; a search of the area failed to detect fledgling or adult Bee-eaters.

General discussion In Australia, ants are seldom reported as predators at arboreal bird nests; they are more likely to be important on or near the ground, as on Christmas Island where the exotic Yellow Crazy Ant Anoplolepis gracilipes has lowered the breeding success of several terrestrial birds (Davis et al. 2002). In Australia, meat and tyrant ants Iridomyrmex spp. have been reported as predators at ground nests of Little Terns Sterna albifrons (Rose 2001), eating corpses of Horsfield’s Bronze-Cuckoo Chrysococcyx basalis nestlings that were abandoned by the Superb Fairy-wren Malurus cyaneus hosts (Langmore et al. 2003), and eating a 9-day-old Southern Scrub-robin Drymodes brunneopygia nestling (Brooker 2001); the nests of all these species were either on or near the ground. The only other reports of possible predation by ants at arboreal nests was at a single site on Eyre Peninsula, South Australia: small back ants were all over a large Yellow-plumed Honeyeater nestling in a bluebush Maireana sp. situated only 1 m from the ground, and at the same site small black ants covered two Rufous Treecreeper rufa chicks that had just hatched in a hollow 4 m from the ground (Anon. 1926). At Dryandra, the voracity of Greenslade’s Meat Ant near the ground suggests that it may be an important predator of birds that have fledged prematurely and are on or near the ground. VOL. 23 (3) Observations of Predation II: SEPTEMBER 2006Birds as Prey of Other Animals 157

The South-western Carpet Python is common at Dryandra and takes a variety of birds and mammals, particularly hollow-nesters and ground-feeders (Pearson 2002); one was seen raiding a Rufous Treecreeper’s nest (Gary Luck pers. comm.). Although the existing and robust populations of most bird species at Dryandra appear largely unaffected by this predator (unpublished data), barriers designed to exclude it could be used to keep it from the nest-sites of rare birds or species that are being reintroduced. Bilbies have been characterised as generalist in exploiting seeds and bulbs, as opportunistic in taking invertebrates as the latter increased in abundance (Gibson 2001), and as a predator of small mammals (Jones 1924), although they showed no interest in House Mice Mus domesticus that shared their enclosure (Johnson & Johnson 1983) and ignored artificial nests baited with quail eggs (unpublished data). Jones (1924) described Bilbies as taking mice and invertebrates around farms of early settlers, and taking mice that were fed to them in captivity. Dryandra provides an opportunity to study this species as it is reintroduced, and to identify its diet where a wide diversity of invertebrate and vertebrate prey is readily obtainable.

Acknowledgements I thank the Centre for Ecosystem Management, Edith Cowan University, and the Department of Conservation & Land Management, for supporting and funding my research. I acknowledge my supervisor Harry F. Recher. Thanks to Brian Heterick and Archie McArthur for identifying the ant species; to Alan Lill, David Pearson and Brian Heterick for commenting on a draft of this manuscript; and to Stephen Debus and Andrew Ley for their editorial comments. I wish to acknowledge the Nyoongar people, the traditional owners of the land where my study was undertaken.

References Andersen, A.N. (2002), ‘Common names for Australian ants (Hymenoptera: Formicidae)’, Australian Journal of Entomology 41, 285–293. Andersen, A.N. & Yen, A.Y. (1992), ‘Canopy ant communities in the semiarid mallee region of north-western Victoria’, Australian Journal of Zoology 40, 205–214. Anon. (1926), ‘North-east Eyre Peninsula,’ South Australian Ornithologist 8, 171–219. Berry, L. (2002), ‘Identifying nest-predator species in southern Victorian woodland using remotely triggered cameras at artificial nests’, Corella 26, 24–26. Briese, D.T. & Macauley, B.J. (1981), ‘Food collection within an ant community in semi-arid Australia, with special reference to seed harvesters’, Australian Journal of Ecology 6, 1–19. Brooker, B. (2001), ‘Biology of the Southern Scrub-robin (Drymodes brunneopygia) at Peron Peninsula, Western Australia’, Emu 101, 181–190. Christidis, L. & Boles, W.E. (1994), The and Species of Birds of Australia and its Territories, RAOU Monograph 2, Royal Australasian Ornithologists Union, Melbourne. Cogger, H.G. (1996), Reptiles and Amphibians of Australia, Reed, Sydney. Cogger, H.G., Cameron, E.E., Sadlier, R.A. & Eggler, P. (1993), The Action Plan for Australian Reptiles, Project 124, Australian Nature Conservation Agency, Canberra. Davis, N., O’Dowd, D J., Green, P.T. & Mac Nally, R.N. (2002), The Invasive Yellow Crazy Ant (Anoplolepis gracilipes) on Christmas Island, Indian Ocean: Impacts on Endemic Land Birds, Report to Environment Australia, Canberra. Edwards, J. (2005), Wildlife Conservation (Specially Protected Fauna) Notice 2005, pp. 648–656, Government Gazette, Perth. Filewood, L.W.C., Hough, K., Morris, I.C. & Peters, D.E. (1978), ‘Helpers at the nest of the Rainbow Bee-eater’, Emu 78, 43–44. Fulton, G.R. (2006), ‘Observations of predation, nest-predation and other disturbance events at Dryandra, south-western Australia I: Birds as predators’, Australian Field Ornithology 23, 144–151. Fulton, G.R. (in press), ‘Identification of nest-predators with remote cameras in continuous woodland of south-western Australia’, Corella. Fulton, G.R. & Ford, H.A. (2001), ‘The Pied Currawong’s role in avian nest predation: An artificial nest and predator removal experiment’, Pacific Conservation Biology 7, 154–160. AUSTRALIAN 158FULTON FIELD ORNITHOLOGY

Gibson, L.A. (2001), ‘Seasonal changes in the diet, food availability and food preference of the Greater Bilby Macrotis lagotis in south-western Queensland’, Wildlife Research 28, 121–134. Hobbs, J.N. (1990), ‘Nest predation by two species of honeyeater’, Australian Birds 24, 3–4. IUCN (2004), IUCN Red List of Threatened Species, , downloaded on 21 December 2005. Johnson, C.N. & Johnson, K.A. (1983), ‘Behaviour of the Bilby, Macrotis lagotis (Reid), (Marsupialia: Thylacomyidae) in captivity’, Australian Wildlife Research 10, 77–87. Johnson, K.A. (1989), ‘Thylacomyidae’, pp. 625–636 in Walton, D.W. & Richardson, B.J. (Eds), Fauna of Australia, vol. 1B, Australian Government Publishing Service, Canberra. Jones, F.W. (1924), The Mammals of South Australia Part II, Government Printer, Adelaide. Langmore, N.E., Hunt. S. & Kilner, R.M. (2003), ‘Escalation of a coevolutionary arms race through host rejection of brood parasitic young,’ Nature 422, 157–160. Lill, A. (1993), ‘Breeding of Rainbow Bee-eaters in southern Victoria’, Corella 17, 100–106. Loop, K.A., Miller, J.D. & Pollard, D. (1995), ‘Observations of the Amethyst Python Morelia amethystina feeding on Rainbow Bee-eaters Merops ornatus’, Memoirs of the Queensland Museum 38, 504. Major, R.E., Gowing, G. & Kendal, C.E. (1996), ‘Nest predation in Australian urban environments and the role of the Pied Currawong, Strepera graculina’, Australian Journal of Ecology 21, 399–409. Major, R.E., Christie, F.J., Gowing, G. & Ivison, T.J. (1999), ‘Elevated rates of predation on artificial nests in linear strips of habitat’, Journal of Field Ornithology 70, 351–364. McArthur, A.J. & Adams, M. (1996), ‘A morphological and molecular revision of the Camponotus nigriceps group (Hymenoptera: Formicidae) from Australia’, Invertebrate Taxonomy 10, 1–46. Pearson, D.J. (2002), The Ecology and Conservation of the South-Western Carpet Python Morelia spilota imbricata, PhD thesis, University of Sydney, Sydney. Pearson, D. Shine, R. & How, R. (2002), ‘Sex-specific niche partitioning and sexual size dimorphism in Australian pythons Morelia spilota imbricata’, Biological Journal of the Linnean Society 77, 113–125. Picman, J. (1992), ‘Egg destruction by Eastern Meadowlarks’, Wilson Bulletin 104, 520–525. Piper, S., Catterall, C.P. & Olsen, M. (2002), ‘Does adjacent land use affect predation of artificial shrub-nests near eucalypt forest edges?’ Wildlife Research 29, 127–133. Read, J.L. & Wilson, D. (2004), ‘Scavengers and detritivores of kangaroo harvest offcuts in arid Australia’, Wildlife Research 31, 51–56. Rose, A.B. (2001), ‘Predation on nesting Little Terns Sterna albifrons at Forster, New South Wales’, Australian Bird Watcher 19, 79–87. Shattuck, S.O. (1999), Australian Ants: Their Biology and Identification, Monographs on Invertebrate Taxonomy, vols 1–4, CSIRO Publishing, Melbourne. Slip, D.J. & Shine, R. (1988), ‘Feeding habits of the Diamond Python, Morelia s. spilota: Ambush predation by a boid snake’, Journal of Herpetology 22, 323–330. Smyth, D.R. & Philpott, C.M. (1968), ‘Field notes on Rabbit Bandicoots, Macrotis lagotis Reid (Marsupialia), from central western Australia’, Transactions of the Royal Society of South Australia 92, 3–17. Strahan, R. (Ed.) (2002), The Mammals of Australia, New Holland, Sydney Zanette, L. (1997), ‘Predation of an Eastern Yellow Robin nest by a small bird, the Brown- headed Honeyeater’, Australian Bird Watcher 17, 158–159. Zanette, L. (2002), ‘What do artificial nests tells us about nest predation?’ Biological Conservation 103, 323–329.

Received 2 March 2006 !