VOL. 23 (2) JUNE 2006 37 AUSTRALIAN FIELD ORNITHOLOGY 2007, 24, 37–43 Food Remains in Nests of Rainbow Bee-eaters Merops ornatus in Old-growth Woodland of South-

GRAHAM R. FULTON1 and A.B. ROSE2 1School of Natural Sciences, Centre for Ecosystem Management, Edith Cowan University, 100 Joondalup Drive, Joondalup, Western Australia 6027 (Email: [email protected]) 2Associate, Australian Museum, 6 College Street, Sydney, New South Wales 2010 (Present address: 61 Boundary Street, Forster, New South Wales 2428)

Summary Rainbow Bee-eaters Merops ornatus nest in burrows where they accumulate remains, in their nest-chambers, throughout the breeding season. We report on the food remains in seven nest-chambers, from Dryandra in south-western Australia. Dryandra encompasses 27 000 ha of old-growth woodland that has been identified with a greater richness and abundance of native than the surrounding agricultural region in which it is located. Honeybees Apis mellifera were the most frequent prey taken by Rainbow Bee-eaters, accounting for 94% (by number) of the total food remains found in their nests. The proportions of prey taken were found to vary significantly between some nests, although there was no consistent pattern between and within sites. The dominance of Honeybees in the food remains indicates both that the bees are present in this large reserve and that they are the preferred prey of Rainbow Bee-eaters, at this site, during the Bee-eater’s breeding season.

Introduction The variety of prey taken by Rainbow Bee-eaters Merops ornatus is broad (Barker & Vestjens 1989; Lill & Fell 1997; Rose 1997; Higgins 1999), although several studies have found that Bee-eaters take a disproportionate number of hymenopterans (bees, wasps and ants) and in particular Honeybees Apis mellifera (Serventy & Whittell 1976; Calver et al. 1987; Saffer & Calver 1997; Bellis & Profke 2003a). Conveniently, Rainbow Bee-eaters do not remove faecal material or regurgitated pellets from their nests (Calver et al. 1987; Boland 2004). This habit allows the diet of a full breeding season to be sampled by collecting the food remains after the young have fledged. Old-growth Wandoo woodland at Dryandra has been identified as supporting richer and more abundant arthropod assemblages (in the canopy, bark and litter) than Jarrah E. marginata and Marri Corymbia calophylla forests (Majer 1985; Majer & Recher 1988; Majer et al. 2003). The arthropod abundance at Dryandra is strongly seasonal, with greatest numbers detected during the moister periods, which correspond with winter and spring rainfall and the onset of the Rainbow Bee-eater breeding season (Majer 1985; Majer et al. 2003). Because hymenopterans in general and Honeybees in particular have been identified as the dominant prey taken by Rainbow Bee-eaters, we examined food remains in nests, from this pristine old-growth woodland, to determine whether Bee-eaters would take as many Honeybees when a rich diversity and abundance of native arthropods were available. AUSTRALIAN 38FULTON & ROSE FIELD ORNITHOLOGY

Materials and methods GRF undertook the field work and ABR identified the arthropods. Seven Rainbow Bee-eater nest-burrows (from three sites) were excavated in February 2003 after they had been active from November 2002 to January 2003. They were situated at Dryandra (32°48′S, 117°0′E), in south-western Australia. Dryandra is 27 000 ha of old-growth woodland located about 160 km south-east of Perth, on the western side of the wheatbelt of Western Australia. The woodland is characterised by Powderbark Wandoo Eucalyptus accedens, Jarrah and Brown Mallet E. astringens on the mid and upper slopes, with Wandoo on the lower slopes and valleys; Powderbark and Wandoo woodland make up ~50% of the total area (Coates 1993; DCLM 1995). Dryandra experiences a Mediterranean climate with dry summers and wet winters; the wettest 6-month period is May to October, accounting for 80% of the annual precipitation (DCLM 1995). Bee-eater nests were monitored throughout the breeding season and excavated after the young had fledged (for more detailed descriptions of monitoring see Fulton 2006a,b). The arthropod remains from each excavated burrow were placed in individually numbered containers and frozen within 2 days. At a later date they were thawed, washed in water, then dried and placed in 70% alcohol. As the arthropods were initially mixed with sand when collected, they were separated from sand and other detritus by floating them off after agitation in a bucket of water, and the solution was then passed through 1- and 2-mm sieves. The smaller fragments of arthropods caught in the smaller sieve size provided no additional data, because these were all fragments from the larger arthropod remains caught in the larger sieve size. The arthropods were identified with the aid of a dissecting microscope and were identified to the ordinal level, unless stated, using ABR’s reference collection and a manual (CSIRO 1970); numbers were determined by head count. The locations of the nests and the distances between nests and the commercial bee-hives are straight-line measurements calculated from the differential-GPS co-ordinates with sub-metre accuracy.

Statistics Chi-square contingency tables were used to detect whether prey proportions were different between nests, and within and between sites. The procedure used to calculate the Chi-square test statistics followed Lowry (2006), and Microsoft Excel® was used to obtain the P value of this test statistic. A modified Bonferroni adjustment was used to control type 1 errors and detect significant differences at a study-wide P <0.05 (see Jaccard & Wan 1996, p. 30).

Results Overall, 2064 arthropods were identified from seven Rainbow Bee-eater nests: of these 94% were Honeybees, 4% were native Hymenoptera (including 1% ants), 1% Coleoptera (beetles) and 1% Homoptera (cicadas) (Table 1). All of the ants were sugar ants Camponotus nigriceps, except three small black flying ants of a second morpho-species. Of the hymenopterans two spider wasps (Pompilidae) and one potter wasp (Eumenidae) were detected. All the cicadas were the same small Cicadetta sp., and three of the beetles were scarab beetles (Scarabaeidae). All Bee-eater nests fledged young except nest 8. The nests were situated in the central area of Dryandra with a maximum separation of 3485 m (Table 2). Both commercial and feral bee-hives were observed at Dryandra. Three feral hives and one swarm were opportunistically detected at the same sites as Bee-eaters, whereas the only commercial hives found were 5218 m from the nearest Bee-eater nest that was monitored. There were significant differences in the proportions of prey identified at some Bee-eater nests (Table 3). However, these differences were not consistent within site A where five of the seven nests were located, or between the three sites A, B and C. However, at four of the five nests within site A (nests 2, 3, 4 and 7) the proportions of prey did not vary significantly. Only nest 5 exhibited significant differences at this site. VOL. 24 (1) MARCH 2007Diet of Rainbow Bee-eater 39

Table 1 The total numbers of arthropods present for each Rainbow Bee-eater nest, with percentages (rounded to whole integers) in parentheses. Percentages for native Hymenoptera include ants, and percentages for Coleptera and Homoptera are combined.

Nest no. Honeybees Native Ants Coleoptera Homoptera Totals Hymenoptera (beetles) (cicadas) 2 526 (97) 7 (2) 2 5 (1) 2 542 3 350 (97) 1 (1) 1 5 (2) 2 359 4 377 (94) 11 (4) 3 1 (2) 8 400 5 321 (89) 33 (10) 2 1 (1) 5 362 6 65 (80) 8 (15) 4 2 (5) 2 81 7 188 (95) 7 (4) 0 2 (1) 1 198 8 113 (93) 4 (7) 5 0 (0) 0 122 Totals 1940 71 17 16 20 2064 % 94 3 1 1 1 100

Table 2 Locations of Rainbow Bee-eater nest-sites at Dryandra, south-western Australia.

Nest no. Nest-site Distance from Latitude (S) Longitude (E) nest no. 6 (m)

2 A 1893 32° 47' 2.7959" 116° 56' 56.1768" 3 A 1995 32° 47' 3.5519" 116° 56' 52.0656" 4 A 1899 32° 47' 2.5439" 116° 56' 55.9680" 5 A 1915 32° 47' 5.1359" 116° 56' 54.9708" 6 B n/a 32° 47' 11.9759" 116° 58' 8.0977" 7 A 1895 32° 47' 5.8919" 116° 56' 55.6440" 8 C 3485 32° 45' 29.7720" 116° 57' 10.6956"

Table 3 Results of Chi-square tests between Rainbow Bee-eater nests, with the nest-sites given in parentheses (see Table 2 for location of nests numbered 2–8). The Chi-square test compared three prey proportions (1: Honeybees, 2: Native Hymenoptera including ants, and 3: Coleoptera and Homoptera combined) for each nest. Significant results are set at a study- wide P <0.05, although individual cells show the calculated P values. Nests were significantly different in the proportions of prey type taken: at three out of 10 comparisons (nests 2, 3, 4, 5 and 7) within site A; at four out of six comparisons for the only nest at site B (nest 6); and at two out of six comparisons for the only nest at site C (nest 8). ns= not significant.

Nest: 2 3 4 5 6 7

3 (A) ns 4 (A) ns ns 5 (A) 2.48 x 10–7 2.10 x 10–7 2.21 x 10–3 6 (B) 3.44 x 10–10 7.35 x 10–11 6.80 x 10–5 ns 7 (A) ns ns ns ns 6.13 x 10–4 8 (C) 1.02 x 10–3 2.59 x 10–5 ns ns ns ns AUSTRALIAN 40FULTON & ROSE FIELD ORNITHOLOGY

Discussion Forest productivity is an important predictor of species richness and faunal abundances (Recher et al. 1996). The presence of abundant water, temperate conditions, nutrients and high productivity are positively correlated with abundant and species-rich animal communities (Braithwaite et al. 1983, 1984, 1989; Recher 1985; Majer et al. 1989, 1992, 1994). Studies at Dryandra have identified a richer and more abundant arthropod fauna in the low-lying areas of Wandoo woodland, compared with mid-slope and laterite ridge-top areas (Majer 1985; Majer & Recher 1988; Majer et al. 2003; Recher & Majer 2006). This result is possibly because richer soils and better soil moisture are found in the low-lying areas and drainage lines at Dryandra (McArthur 1991; Coates 1993). The higher soil moisture in Wandoo woodland almost certainly facilitates higher levels of primary productivity by (particularly in response to seasonal precipitation), which are associated with the identified increases in arthropods found there (Majer 1985; Majer & Recher 1988; Recher et al. 1996; Majer et al. 2003; Recher & Majer 2006). Low- lying areas of Wandoo woodland have been identified as preferential habitat for other birds, including the Splendid Fairy-wren Malurus splendens (Brooker & Rowley 1995), Yellow-plumed Honeyeater Lichenostomus ornatus (Wilson & Recher 2001; Davis & Recher 2002), Rufous Treecreeper Climacteris rufa (Luck 2002a,b), and Western Yellow Robin Eopsaltria griseogularis (Cousin 2004). All the Bee-eater burrows were located in the low-lying areas of old-growth Wandoo woodland, where the greatest abundance and richness of native arthropods, within Dryandra, have been identified. Despite the presence of abundant native arthropods, Bee-eaters still took appreciably more Honeybees than other prey. It has been hypothesised that the diet of Bee-eaters may vary opportunistically from site to site (Blakers et al. 1984; Fry 1984; Saffer & Calver 1997). Saffer & Calver (1997) detected differences in the size and type of prey taken between two widely separated sites in Western Australia. Calver et al. (1987) sampled the food remains in nests of Bee-eaters on Rottnest Island, Western Australia, and found only a minimal quantity of Honeybees (1%), possibly because commercial Honeybee colonies were absent at the time. The present study confirmed that Honeybees are a preferred source of food for Bee-eaters. The results on prey proportions between nest-sites were equivocal, with nests within and between sites exhibiting significant and non- significant differences. However, four nests (nests 2, 3, 4, and 7) grouped together at site A, by sharing similar (not significantly different) prey proportions. Boland (2004) found that colonial Rainbow Bee-eaters renested with their colony each year despite undertaking an annual migration. Observations of the species during migration suggest that the birds migrate in socially cohesive groups that may be genetically related (Garnett 1985). At Dryandra, four (of five) nests grouped together by the proportions of prey taken, suggesting that these birds may forage together but others do not. Social cohesion and/or close genetic ties may explain this result. To date, the accumulating data on the Bee-eater’s diet, including this study, suggest a foraging method whereby the Bee-eater’s diet is flexible and in part habitat-dependent. The same evidence suggests that Bee-eaters prefer hymenopterans, especially Honeybees, when these are available. There are 39 registered apiaries at Dryandra (Sean Bryce pers. comm.), although in the 4 years 2003–06 there have been only two apiarists using Dryandra (Steve Gorton pers. comm.). The commercial hives detected in this study were outside the foraging range of 1000–1250 m suggested for Bee-eaters (Bellis & Profke 2003a,b). However, Honeybees have been recorded travelling up to VOL. 24 (1) MARCH 2007Diet of Rainbow Bee-eater 41

13.7 km from their hives (Eckert 1933), although they are more likely to forage only up to 4 km from their hive (Visscher & Seeley 1982; Paton 1996). In this case, the food remains were dominated by Honeybees, suggesting that these were probably taken from the feral populations closer to the Bee-eaters’ nests. Feral Honeybees can have a detrimental effect on native flora and fauna, and their presence at Dryandra is of some concern, as they compete with birds and mammals for hollows (Paton 1993, 1996). However, this competition is unlikely to be a limiting factor at Dryandra, because old-growth Wandoo woodland retains numerous hollows (Luck 2002b). Honeybees also compete with native nectarivores for nectar and pollen, often changing (reducing or increasing) pollination rates of flowers and the numbers of seeds that are set (Paton 1993, 1996; Celebrezze & Paton 2004). They also aid in the spread of introduced weeds and pathogens such as the root-rot fungus Phytophthora cinnamomi (Paton 1996). These disturbances are likely to be especially important to plants and animals at Dryandra, because this reserve harbours endemic native species, and many that are extinct outside Dryandra or rare in the region (DCLM 1995).

Acknowledgements The Centre for Ecosystem Management, Edith Cowan University, the Stuart Leslie Bird Research Awards (Birds Australia), and the Department of Conservation & Wildlife Management funded this research. We acknowledge Courtney Smithers (Deputy Director at the Australian Museum in the 1970s) for allowing access to the Museum’s insect collection, from which ABR’s reference collection is based. Special thanks to Mercedes Smith for transporting the samples from the field to the freezer; and to John Lawson for helping to excavate the burrows. Stephen Debus, Alan Lill and Mike Calver (as AFO reviewers) gave constructive comments on this manuscript. Mike Calver also provided advice on the statistics used. We wish to acknowledge the Nyoongar people, the traditional owners of the land where this study was undertaken.

References Barker, R.D. & Vestjens, W.J.M. (1989), The Food of Australian Birds, Volume I, Non- Passerines, CSIRO, Melbourne. Bellis, G.A. & Profke, A.M. (2003a), ‘Rainbow Bee-eaters (Merops ornatus) as a monitoring tool for honeybees (Apis mellifera L.; Hymenoptera: Apidae)’, Australian Journal of Entomology 42, 266–270. Bellis, G.A. & Profke, A.M. (2003b), ‘Roosting behaviour of the Rainbow Bee-eater Merops ornatus in suburban Darwin’, Corella 27, 75–80. Blakers, M., Davies, S.J.J. F. & Reilly, P.N. (1984), The Atlas of Australian Birds, Royal Australasian Ornithologists Union and Melbourne University Press, Melbourne. Boland, C.R.J. (2004), ‘Breeding biology of Rainbow Bee-eaters (Merops ornatus): A migratory, colonial, cooperative bird,’ Auk 121, 811–823. Braithwaite, L.W., Austin, M.P., Clayton, M., Turner, J. & Nicholls, A.O. (1989), ‘On predicting the presence of birds in Eucalyptus forest’, Biological Conservation 50, 33–50. Braithwaite, L.W., Dudzinski, M.L. & Turner, J. (1983), ‘Studies on the arboreal marsupial fauna of eucalypt forests being harvested for woodpulp at Eden, N.S.W. II. Relationship between the fauna density, richness and diversity, and measured variables of the habitat’, Australian Wildlife Research 10, 231–247. Braithwaite, L.W., Turner, J. & Kelly, J. (1984), ‘Studies on the arboreal marsupial fauna of eucalypt forests being harvested for woodpulp at Eden, N.S.W. III. Relationship between the fauna densities, eucalypt occurrence and foliage nutrients, and soil parent materials’, Australian Wildlife Research 11, 41–48. Brooker, M.G. & Rowley, I. (1995), ‘The significance of territory size and quality in the mating strategy of the Splendid Fairy-wren,’ Journal of Animal Ecology 64, 614–627. Calver, M.C., Saunders, D.A. & Porter, B.D. (1987), ‘The diet of nestling Rainbow Bee- eaters, Merops ornatus, on Rottnest Island, Western Australia, and observations on a non-destructive method of diet analysis’, Australian Wildlife Research 14, 541–550. AUSTRALIAN 42FULTON & ROSE FIELD ORNITHOLOGY

Celebrezze, T. & Paton, D.C. (2004), ‘Do introduced Honeybees (Apis mellifera, Hymenoptera) provide full pollination service to bird-adapted Australian plants with small flowers? An experimental study of Brachyloma ericoides (Epacridaceae)’, Austral Ecology 29, 129–136. Coates, A. (1993), Vegetation Survey of Dryandra Forest, Dept Conservation & Land Management, Perth. Cousin, J.A. (2004), ‘Habitat selection of the Western Yellow Robin (Eopsaltria griseogularis) in Wandoo woodland, Western Australia’, Emu 104, 229–234. CSIRO (1970), The Insects of Australia, Melbourne University Press, Melbourne. Davis, W.E. Jr & Recher, H.F. (2002), ‘Mixed-species foraging flocks in winter at Dryandra State Forest, Western Australia,’ Corella 26, 70–73. DCLM (1995), Management Plan 1995–2005, Management Plan 30, Dept Conservation & Land Management, Perth. Eckert, J.E. (1933), ‘Flight range of the honeybee,’ Journal of Apicultural Research 47, 257–285. Fry, C.H. 1984), ‘Kingfishers and bee-eaters’, Birding in Southern Africa 46, 99–102. Fulton, G.R. (2006a), ‘Observations of predation, nest-predation and other disturbance events at Dryandra, in south-western Australia I: Birds as predators’, Australian Field Ornithology 23, 144–151. Fulton, G.R. (2006b), ‘Observations of predation, nest-predation and other disturbance events at Dryandra, in south-western Australia II: Birds as prey of other animals’, Australian Field Ornithology 23, 152–158. Garnett, S. (1985), ‘Mortality and group cohesion in migrating Rainbow Bee-eaters’, Emu 85, 267–268. Higgins, P.J. (Ed.) (1999), Handbook of Australian, New Zealand and Antarctic Birds, vol. 4, Oxford University Press, Melbourne. Jaccard, J. & Wan, C.K. (1996), LISREL Approaches to Interaction Effects in Multiple Regression, Sage, Thousand Oaks, USA. Lill, A. & Fell, P.J. (1997), ‘Aspects of the ecological energetics of development in Rainbow Bee-eaters’, Australian Journal of Zoology 45, 281–294. Lowry, R. (2006), Concepts and Applications of Inferential Statistics, http://faculty.vassar.edu/ lowry/webtext.html 05/8/2006 [online]. Luck, G.W. (2002a), ‘The habitat requirements of the Rufous Treecreeper (Climacteris rufa). 1. Preferential habitat use demonstrated at multiple spatial scales’, Biological Conservation 105, 383–394. Luck, G.W. (2002b), ‘Determining habitat quality for the cooperatively breeding Rufous Treecreeper, Climacteris rufa’, Austral Ecology 27, 229–237. Majer, J.D. (1985), ‘Invertebrate studies in disturbed and pristine habitats of Dryandra State Forest’, Research Paper 80, Forests Department of Western Australia, Perth. Majer, J.D. & Recher, H.F. (1988), ‘Invertebrate communities on Western Australian eucalypts: A comparison of branch clipping and chemical knockdown procedures’, Australian Journal of Ecology 13, 269–278. Majer, J.D., Recher, H.F. & Ganeshanandam, S. (1992), ‘Variation in foliar nutrients and its relation to arthropod communities on Eucalyptus in New South Wales and Western Australia,’ Australian Journal of Ecology 17, 383–394. Majer, J.D., Recher, H.F., Graham, R. & Gupta, R. (2003), ‘Trunk invertebrate faunas of Western Australian forests and woodlands: Influence of species and season’, Austral Ecology 28, 629–641. Majer, J.D., Recher, H.F., Perriman, W.S. & Achuthan, N. (1989), ‘Spatial variation of arthropod abundance within the canopies of Australian eucalypt forests,’ Studies in Avian Biology 13, 65–72. Majer, J.D., Recher, H.F. & Postle, A.C. (1994), ‘Comparison of arthropod species richness in New South Wales and Western Australian canopies: A contribution to the species number debate,’ Memoirs of the Queensland Museum 36, 121–131. McArthur, W.M. (1991), Reference Soils of South-western Australia, Western Australian Department of Agriculture, Perth. Paton, D.C. (1993), ‘Honeybees Apis mellifera in the Australian environment. Does Apis mellifera disrupt or benefit native biota?’ Bioscience 43, 95–103. Paton, D.C. (1996), Overview of Feral and Managed Honeybees in Australia: Distribution, Abundance, Extent of Interactions with Native Biota, Evidence of Impacts and Future Research, Australian Nature Conservation Agency, Canberra. VOL. 24 (1) MARCH 2007Diet of Rainbow Bee-eater 43

Recher, H.F. (1985), ‘Eucalypt forests, woodlands and birds: An introduction,’ pp. 1–10 in Keast, A., Recher, H.F., Ford, H. & Saunders, D. (Eds), Birds of Eucalypt Forests and Woodlands: Ecology, Conservation, Management, Surrey Beatty, Sydney. Recher, H.F. & Majer, J.D. (2006), ‘Effects of bird predation on canopy arthropods in Wandoo Eucalyptus wandoo woodland’, Austral Ecology 31, 349–360. Recher, H.F., Majer, J.D. & Ganesh, S. (1996), ‘Eucalypts, arthropods and birds: On the relation between foliar nutrients and species richness’, Forest Ecology and Management 85, 177–196. Rose, A.B. (1997), ‘Notes on the diet of swifts, kingfishers and allies in eastern New South Wales’, Australian Bird Watcher 17, 203–210. Saffer, V.M. & Calver, M.C. (1997), ‘The size and type of prey taken by adult Rainbow Bee- eaters in the south-west of Australia’, Emu 97, 329–332. Serventy, D.L. & Whittell, H.M. (1976), Birds of Western Australia, University of Western Australia Press, Perth. Visscher, P.K. & Seeley, T.D. (1982), ‘Foraging strategy of honeybee colonies in a temperate deciduous forest’, Ecology 63, 1790–1801. Wilson, K. & Recher, H.F. (2001), ‘Foraging ecology and habitat selection of the Yellow- plumed Honeyeater, Lichenostomus ornatus, in a Western Australian woodland: Implications for conservation’, Emu 101, 89–94.

Received 7 August 2006 !