CSIRO PUBLISHING
Emu, 2003, 103, 255–258
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Quail eggs, modelling clay eggs, imprints and small mammals in an Australian woodland Graham R. FultonA,B and Hugh A. FordA AZoology,
School of Environmental Sciences and Natural Resources Management, University of New England, Armidale, NSW 2351, Australia. BPresent address: Centre for Ecosystem Management, Edith Cowan University, Joondalup, WA 6027, Australia. Email:
[email protected]
Abstract. Artificial nests and eggs have become popular and useful tools for studying nest predation on birds. In particular, they may assist in the identification of nest predators. However, quail eggs commonly used in many nestpredation studies may exclude the detection of predation by small-mouthed mammals, which may not be able to break the eggshells as readily as eggs of small passerines. In this study captive Brown Antechinus (Antechinus stuartii) were given Japanese Quail eggs. They failed to break the shell, although they consumed the egg’s contents if the shell had been broken for them. Field trials were conducted in a large woodland fragment on the New England Tableland, New South Wales, using clay and quail eggs to identify predators. Pied Currawongs (Strepera graculina), and possibly other birds, were found to be the most significant nest predators. Mammals were judged to play a comparatively small role. However, we detected large imprints in one modelling clay egg, which corresponded with Koala (Phascolarctos cinereus) incisors. In addition, we report that clay eggs soften at high temperatures, which may affect the size of a predator’s imprint, and therefore cause its misidentification. Introduction In 1947, Keith Hindwood described, to our knowledge, the earliest artificial nest procedure. A nest, made with ‘fowl feathers,’ was baited with four eggs and positioned alongside a rabbit trap to capture a vagrant Australian Raven (Corvus coronoides), on Lord Howe Island. The raven had been taking a ‘heavy toll’ on the eggs of nesting sea birds (Hindwood 1947). Subsequently, the Australian Raven’s head was collected and identified. Even this early attempt demonstrated the future experimental and management potential of the artificial nest. More recently, artificial nest experiments have become popular for testing various ecological hypotheses relating to nest predation (Paton 1994; Major and Kendal 1996). Nest predation is generally considered the main cause of nest failure for open-nesting passerines (Lack 1954; Skutch 1966; Ricklefs 1969; Martin 1992). The event itself is difficult to record, occurring in only a few seconds (Skutch 1966), and most casual observations are made in daylight hours, missing predation by nocturnal mammals (Major 1991). Various artificial egg types have been used, the most common being imprint-receptive modelling clay eggs and real eggs that provide a reward. Real eggs have varied from the more commercially available quail and chicken eggs to those of smaller and perhaps more appropriate species, such as Budgerigar and Zebra Finch eggs (Major and Kendal © Royal Australasian Ornithologists Union 2003
1996; Rangen et al. 1999). Quail eggs may present a stronger visual cue to nest predators than smaller passerine eggs. On the other hand, they may underestimate the importance of small mammal predators (such as Chipmunks, Tamias striatus, and Deermice, Peromyscus maniculatus, in North America) that are unable to break the quail eggshell (Haskell 1995; Rangen et al. 1999; Bayne and Hobson 1999; but see Craig 1998). Quail eggs may not be the most appropriate egg choice in nest-predation experiments, but are commonly used, and this use is likely to continue due to their ease of acquisition. However, not all small mammals may demonstrate the same ability to break open quail eggs. There have been no tests of the ability of small Australian marsupials’ to break quail eggs. We tested the ability of captive Brown Antechinus (Antechinus stuartii) to break the shell of quail eggs in order to determine whether they could be nest predators of eggs of this size. We also examined tooth and beak marks on artificial eggs used in a field trial conducted in 1999 on the New England Tablelands of New South Wales, to identify potential predators of real eggs. The field trial was designed both to identify predators and to quantify their relative roles, in a large woodland fragment. However, the experiment primarily focused on the effect of the removal of a suspected predator, the Pied Currawong (Strepera graculina) and on the rate of nest predation (see Fulton and Ford 2001). Birds were found to be the most important predators in this study. 10.1071/MU02007
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A. stuartii was not detected by the study, but it is considered likely to be present in the study site. Materials and Methods Antechinus experiment We chose A stuartii because captive animals were available for the experiment and they were the most likely small native mammal predator at the field site. Thirteen captive animals were given whole and broken Japanese Quail (Coturnix coturnix) eggs to determine whether they could break the shell. The eggs were placed in eight cages containing either one or two A. stuartii of both sexes and different ages. Young animals (~7 months) were independent of their parents and were as large as the adults. All individuals were bred in captivity. The eggs were provided at their usual feeding time, though the amount of other food was reduced marginally to encourage them to eat the egg. Before presentation, the eggs were covered with water at ~100°C, for one minute, to reduce the risk of Salmonella infection. The contents of the eggs were partly cooked though still fairly fluid. On the first day, a single whole egg was placed into each cage. On the second day, the eggs were cut in half (equatorially), to provide access to the contents; and half an egg (with contents) was placed in each cage. On the third day, whole eggs were again presented. However, one egg was substantially damaged from the initial contact with boiling water, the shell was cracked and broken in one area, but the membrane was still intact and had the pieces of shell attached. This damage appeared much the same as if a hard-boiled egg had been hit with a spoon. Field experiment Study site This study was conducted at Imbota Nature Reserve (INR), formerly Eastwood State Forest (30°35′S, 151°43′E), on the New England Tablelands of New South Wales. INR is a 240-ha woodland remnant, surrounded by cleared grazing lands and degraded grazed woodland on privately owned land (Ford et al. 1985, 1986). Artificial nests and eggs Artificial nests were constructed from halved tennis balls clad outside with bark and fruticose lichen, and lined inside with leaves. The nests in this study were modelled to represent the size and shape of nests of small insectivorous passerines, such as robins and flycatchers, and positioned similarly to natural nests of these birds. One real and one artificial egg were used in each nest. Real eggs were domestic Japanese Quail (Coturnix coturnix) eggs. Artificial eggs were made with Rainbow Modelling Clay. Latex gloves were worn when moulding the eggs to minimise scent transference, but not for any other handling. Black and brown oil paints were mixed in equal parts to match precisely the Japanese Quail egg’s cryptic colouration. The eggs’ variously spotted pattern was duplicated by flicking the mixed paint from a stiff bristled artist paintbrush. All eggs were scented with chicken (Gallus gallus) manure diluted with water (~20:1), which was brushed over the eggs to mask their own scent and to provide a uniform avian scent. In all cases, the odour of the chicken faeces was dominant. Both quail and artificial eggs were quite similar in size, shape and colour. Field-experiment design and data-collection procedures Overall, 416 artificial nests were monitored for predation in control and experimental grids within the reserve, before and after removal of Pied Currawongs (104 nests per grid). The first round took place from 11 to 17 November 1999 and the second round took place from 4 to 10 December 1999. Plastic flagging nest-markers were placed at 50-m
G. R. Fulton and H. A. Ford
intervals east to west and 100-m intervals north to south. The grids were separated by a ‘buffer zone’ at least 450 m wide at the narrowest point. Nests were placed in the field 7 days before the first round and 14 days before the second round, to mimic a natural situation where nests are built before egg-laying. The eggs were added to the nests the day before checking commenced. Thirteen Pied Currawongs were culled from the experimental grid and eggs were added to the nests one day later. Damaged eggs were retrieved daily over seven days. For a more detailed report on the field experiment, see Fulton and Ford (2001). Imprint-identification procedure Skulls and jaws with teeth of potential mammalian predators (from the University of New England’s Zoology Museum) were closely matched with the imprints on clay eggs. The imprinted eggs described herein are held as reference specimens in the Zoology Museum at the University of New England.
Results Antechinus experiment The captive A. stuartii showed immediate curiosity in the quail eggs, more so than in their usual food. All the eggs were displaced, most were pushed against the sides of the cages, indicating that the animals may have tried to break the shell by wedging them against the cage walls. Captive A. stuartii did not break the shell of whole quail eggs on either the first or the third day. However, they ate the contents of the eggs that had been halved. In half of the cages, the animals ate the shell completely or partially, whereas the others left the shell intact. An adult female ate the contents of the egg that had been damaged during boiling after making a hole in the damaged part of the shell. Field experiment Thirty-eight artificial eggs exhibited beak imprints of various sizes while only five artificial eggs collected had tooth imprints. In 86% of depredated nests, no sign was left by predators, with either the quail egg, the artificial egg, or both eggs missing. Most of the recovered quail eggs that exhibited damage (19 out of 22; 86%) had a hole, approximately 1 cm2, in the side. Of the others, two quail eggs had been reduced to large fragments and one was found as a half eggshell. This type of sign suggests mammalian predation: birds usually swallow the egg whole or peck a hole in it. The relative impact of mammalian predators was low, with only eight eggs (artificial and quail) showing signs of mammalian predation. A single artificial egg had large incisor-like imprints (with flat distal surfaces) on each side of the egg, indicative of a single bite. However, these imprints do not match any known predator from INR. The Koala (Phascolarctos cinereus) is tentatively suggested because the distal surfaces of the imprints are flat, yet the imprints are incisor-like (Fig. 1). The other four artificial eggs had tooth imprints that matched with those of the Brushtail Possum (Trichosurus vulpecula). However, the clay eggs were well chewed and lacked clear dentition patterns for precise predator determination.
Predation on artificial eggs
Discussion Exclusion of Antechinus spp. from Japanese Quail eggs Several studies using large eggs have reported biases against small-mouthed predators (Haskell 1995; Bayne and Hobson 1999; Davison and Bollinger 2000; Rangen et al. 2000; Maier and Degraaf 2000, 2001). Haskell (1995) suggested that relatively large quail eggs used in artificial-nest experiments might underestimate the importance of small mammals in North America. Likewise, in Australia, Antechinus spp. may be predators of passerine eggs, but remain undetected by experiments that use quail eggs. Our findings that captive A. stuartii were unable to beak the shell of quail eggs, unless assisted by substantial damage to the shell, support this suggestion. The fact that A. stuartii consumed the contents of eggs that had been cut in half indicates that their failure to break open eggs is not because they are uninterested in them. Our field study did not identify any predation by A. stuartii. A. stuartii is probably present at INR (F. Geiser, personal communication). However, in this study, no imprints in clay eggs were similar to published pictures and descriptions of clay eggs depredated by them. In the field, Antechinus spp. may push the eggs from the nest to break or crack the shell, thus providing access to the contents. Moreover, Antechinus spp. may also prey upon smaller passerine eggs. Buchanan (1989) found shell fragments in Antechinus spp. pellets. A. stuartii has been characterised as an opportunistic feeder, taking invertebrate prey in similar proportions as they occur in pitfall traps (Fox and Archer 1984). A. stuartii may therefore take small passerine eggs as food. Matthews et al. (1999) and Major et al. (1994) collected imprints of A. stuartii teeth in plasticine eggs, though they concluded that their relative impact, compared with that of birds, is very low. Major et al. (1994) found Antechinus spp.
Fig. 1. Possible Koala predation: the teeth imprints in this artificial egg are offset from the centre at the same angle on both sides of the egg, which indicates a single bite. However, the base of the imprints have flat surfaces, with the speckled surface relatively undamaged, indicating flat-surfaced incisors, implicating the Koala. These imprints are too large for Brushtail Possums and rats.
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to be responsible for 5% of predation events compared with more than 50% for birds. Our field study suggests that mammals are minor nest predators compared with birds. Most (38) of the imprinted eggs exhibited beak imprints; only five imprinted eggs had tooth imprints. In addition, at 86% of depredated nests, one or both eggs were removed and no sign was left. Large birds typically leave no sign at the nest (Skutch 1966; Westmoreland and Best 1985; Møller 1987, 1989; Brown et al. 1996; Matthews et al. 1999). Furthermore, birds were probably responsible for the holes pecked in the quail eggs (19 of 22); this type of predation has been described by others (Hobbs 1990; Picman 1992; Zanette 1997). If predation by small mammals is so infrequent it may be that the bias caused by using quail eggs will have little overall impact on the results of artificial nest experiments in Australia. However, Luck (2003) found that mammals at a site in south-west Western Australia were the main predators on a hollow-nesting bird, the Rufous Treecreeper (Climacteris rufa). Likewise, Major (1991) identified mammals as the dominant predators of Scarlet Robins (Petroica m. multicolor) on Norfolk Island. Thus, until more is understood about which predators are important in what habitats, and/or at which nest types, experimental biases, such as the use of quail eggs to replicate small passerine eggs, need to be considered. Identifying predators from imprints Major et al. (1994) found beak imprints to be unreliable because experiments on known predators demonstrated that imprints varied according to vigour of attack. Clay eggs also become soft when warm and can be easily imprinted by small-mouthed predators (Bayne and Hobson 1999; Rangen et al. 1999). Bayne and Hobson (1999) claimed that clay eggs are soft and easily marked by small mammalian predators such as Deer Mice (Peromyscus maniculatus), while quail eggs are thick shelled and cannot be broken by the same species. We found the hardness of modelling clay to be dependent on temperature, varying from very soft to extremely hard. However, small mammals at our study site are mostly active at night when temperatures are low and the modelling clay is quite hard. Therefore, imprints of small teeth may be the result of hard clay and/or low vigour of attack by a medium-to-large-sized predator (bird or mammal). We suggest that researchers using modelling clay eggs consider the properties of the clay along with the vigour of attack when identifying predator imprints. If both these factors are compounded precise predator determinations may be impossible, particularly in the case of birds. For example, determinations of small-, medium- and largebeaked avian predators may be erroneous. An experimental test of our ability to read imprints may shed more light on this. However, we suggest that cameras and videos should be used in conjunction with imprint-receptive eggs to confirm some of the predation and then infer over a larger number of
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nests that an imprint belongs to a certain predator. Alternatively, clay that maintains a constant hardness at different temperatures could be used; however, vigour of attack would still make precise predator determination problematic. ‘Egg-predation’ by Koalas The artificial egg with the bite imprints that most closely matched the Koala was unexpected. A large Koala was observed at INR late in the field study, but before the predation event. Koalas may eat non-eucalypt foliage, but there is no previous evidence that they are ever carnivorous (W. J. Foley, personal communication). Perhaps they have been overlooked as potential nest predators, though it is possible that this ‘predation’ was the result of curiosity. A field trial of suitable artificial nests in an area where Koalas are abundant (for example Kangaroo Island) may provide more information about their predatory activity. Acknowledgments We thank Fritz Geiser for the use of the Antechinus and Gary Luck for his useful comments on the draft manuscript. References Bayne, E. M., and Hobson, K. A. (1999). Do clay eggs attract predators to artificial nests? Journal of Field Ornithology 70, 1–7. Brown, K. P., Moller, H., and Innes, J. (1996). Sign left by Brushtail Possums after feeding on birds’ eggs and chicks. New Zealand Journal of Ecology 20, 277–284. Buchanan, R. (1989). Pied Currawongs (Strepera graculina): their diet and role in weed dispersal in suburban Sydney, New South Wales. Proceedings of the Linnean Society of New South Wales 111, 241–255. Craig, D. P. (1998). Chipmunks use leverage to eat oversized eggs: support for the use of quail eggs in artificial nest studies. Auk 115, 486–489. Davison, W. B., and Bollinger, E. (2000). Predation rates on real and artificial nests of grassland birds. Auk 117, 147–153. Ford, H. A., Bridges, L., and Noske, S. (1985). Density of birds in eucalypt woodland near Armidale, north-eastern New South Wales. Corella 9, 97–107. Ford, H. A., Noske, S., and Bridges, L. (1986). Foraging of birds in eucalypt woodland in north-eastern New South Wales. Emu 86, 168–179. Fox, B. J., and Archer, E. (1984). The diet of Sminthopsis murina and Antechinus stuartii (Marsupialia: Dasyuridae) in sympatry. Australian Wildlife Research 11, 235–248. Fulton, G. R., and Ford, H. A. (2001). The Pied Currawong’s (Strepera graculina) role in avian nest predation: an artificial nest and predator removal experiment. Pacific Conservation Biology 7, 154–160. Haskell, D. G. (1995). Forest fragmentation and nest predation: are experiments with Japanese Quail eggs misleading. Auk 112, 767–770. Hindwood, K. A. (1947). Australian Raven as a straggler. New Zealand Bird Notes 2, 122.
Hobbs. J. N. (1990). Nest predation by two species of honeyeater. Australian Birds 24, 3–4. Lack, D. (1954). ‘The Natural Regulation of Animal Numbers.’ (Clarendon Press: Oxford.) Luck, G. W. (2003). Differences in the reproductive success and survival of the Rufous Treecreeper (Climacteris rufa) between a fragmented and unfragmented landscape. Biological Conservation 109, 1–14. Maier, T. J., and DeGraaf, R. M. (2000). Predation on Japanese Quail vs. House Sparrow eggs in artificial nests: small eggs reveal small predators. Condor 102, 325–332. Maier, T. J., and DeGraaf, R. M. (2001). Differences in predation by small predators limit the use of plasticine and Zebra Finch eggs in artificial-nest studies. Condor 103, 180–183. Major, R. E. (1991). Identification of nest predators by photography, dummy eggs, and adhesive tape. Auk 108, 190–195. Major, R. E., and Kendal, C. E. (1996). The contributions of artificial nest experiments to our understanding of avian reproductive success: a review of methods and conclusions. Ibis 138, 298–307. Major, R. E., Pyke, G. H., Christy, M. T., Gowing, G., and Hill, R. S. (1994). Can nest predation explain the timing of the breeding season and the pattern of nest dispersion of New Holland Honeyeaters? Oikos 69, 364–372. Martin, T. E. (1992). Breeding productivity considerations: what are the appropriate habitat features for management? In ‘Ecology and Conservation of Neotropical Migrant Landbirds’. (Eds J. M. Hagan and D. W. Johnston.) pp. 455–473. (Smithsonian Institution Press: Washington, DC.) Matthews, A., Dickman, C. R., and Major, R. E. (1999). The influence of fragment size on nest predation in urban bushland. Ecography 22, 349–356. Møller, A. P. (1987). Egg predation as a selective factor for nest design: an experiment. Oikos 50, 91–94. Møller, A. P. (1989). Nest site selection across field–woodland ecotones: the effect of nest predation. Oikos 56, 240–246. Paton, P. W. C. (1994). The effect of edge on avian nest success. Conservation Biology 8, 17–26. Picman, J. (1992). Egg destruction by Eastern Meadowlarks. Wilson Bulletin 104, 520–525. Rangen, S. A., Clark, R. G., and Hobson, K. A. (1999). Influence of nest-site vegetation and predator community on the success of artificial songbird nests. Canadian Journal of Zoology 77, 1676–1681. Rangen, S. A., Clark, R. G., and Hobson, K. A. (2000). Visual and olfactory attributes of artificial nests. Auk 117, 136–146. Ricklefs, R. E. (1969). An analysis of nesting mortality in birds. Smithsonian Contributions to Zoology 9, 1–48. Skutch, A. F. (1966). A breeding bird census and nesting success in Central America. Ibis 108, 1–16. Westmoreland, D., and Best, L. B. (1985). The effect of disturbance on Mourning Dove nesting success. Auk 102, 774–780. Zanette, L. (1997). Predation of an Eastern Yellow Robin nest by a small bird, the Brown-headed Honeyeater. The Australian Birdwatcher 17, 158–159.
Manuscript received 18 March 2002; accepted 5 May 2003
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