- Email: [email protected]
The Genyornis egg: A commentary on Grellet-Tinner et al., 2016
Quaternary Science Reviews xxx (2017) 1e5
Contents lists available at ScienceDirect
Quaternary Science Reviews journal homepage: www.elsevier.com/locate/quascirev
The Genyornis egg: A commentary on Grellet-Tinner et al., 2016
1. Summary When humans colonized Australia three giant flightless birds were on the landscape, of which the largest, Genyornis newtoni, the sole remaining taxon of the mihirungs, became extinct. Although nearly complete skeletons of Genyornis have been found, they never have been linked directly to an egg. Williams (1981) recognized and described distinct morphological characteristics demonstrating that eggshell fragments from two different taxa were preserved in arid-zone sand dunes. One type had characteristics identical to those of emu (Dromaius novaehollandiae), whereas the other was dissimilar to any extant bird. Based on its estimated volume exceeding that of modern emu egg, he attributed the newly discovered eggshell to Genyornis. Attribution of these eggshell to a Genyornis parent was recently challenged by Grellet-Tinner et al. (2016), who suggested that an extinct megapode of the genus Progura was a more likely candidate parent. They refer to the eggshell Williams (1981) assigned to Genyornis as “putative Genyornis oological material” (PGOM), which for convenience we follow here. The goal of this commentary is to support our claim that Genyornis is by far the most likely candidate parent bird for PGOM, and to show why it is highly unlikely that any megapode could be parent to PGOM. 2. The Grellet-Tinner et. al., 2016 argument Grellet-Tinner et al. (2016) argue that PGOM is unlikely to be derived from Genyornis primarily based on egg size, relying on the only nearly complete PGOM eggshell, the Spooner Egg, found partly intact in aeolian sand near Port Augusta (Fig. 1). Based on the dimensions of the reconstructed Spooner Egg, Grellet-Tinner et al. (2016) argue that PGOM is too small for a bird with the body mass estimated for Genyornis (168e275 kg) even at the low end of the estimates; they predict an egg mass of 1600e2200 g. None of the additional PGOM observations reported by GrelletTinner et al. (2016) are inconsistent with a Genyornis parent. Having concluded that the PGOM egg is too small, Grellet-Tinner et al. (2016) suggest that an extinct 5 kg megapode (Progura) is the more likely parent bird. Extant megapode eggs are unusually large for the parent's body mass, and they argue that extrapolating a plot of bird mass vs. egg length for extant megapodes predicts an egg with a length similar to the Spooner Egg for Progura. 3. Correctly estimating the mass of PGOM A weakness in the Grellet-Tinner et al. (2016) argument is their dependence on the Spooner Egg, which measures 126 97 mm, to
represent typical PGOM dimensions. Eggs of extant birds are known to vary substantially in size and mass, even within a single clutch. For example, Dromaius eggs range between 400 and 700 g, but may reach 900 g (Dzialowski and Sotherland, 2004). Hence, a single sample cannot accurately represent the range of possible dimensions for PGOM. Williams (1981) provides a more thorough estimate of PGOM dimensions. Although Williams never found a whole PGOM, he collected and studied many large fragments. He argued “since the transverse section of an egg is circular, its curvature is a direct measure of egg width at that point. With a suitably large sample of shell fragments there is a good chance that the equatorial region will be represented, so by selection of the smallest values of transverse curvature the actual width of the egg can be estimated” (Williams, 1981: p. 134). The accuracy of this method for reconstructing egg dimensions from eggshell fragments has been documented for modern and fossil Struthionidae (ostrich) eggshell (Sauer, 1968), and for Aepyornis, the elephant bird of Madagascar (Sauer, 1978). Williams tested this assertion, by breaking five modern emu eggs into fragments with areas similar to those of the PGOM that he measured, and used the curvature in those fragments to estimate a breadth of 92.5 ± 2.5 mm, consistent with the breadth of the two whole eggs he used in his experiments (94 mm), and the average of another 32 whole eggs he measured (90.5 ± 3.9 mm). Following the same technique, he measured the curvature of 219 large PGOM fragments, from which their calculated breadth ranged between 125 and 134 mm (Williams, 1981), a considerably larger breadth than for the Spooner Egg (97 mm). Determining egg length from random fragments is more difficult. Williams (1981) estimated an average PGOM length of 155 mm (range: 125e185 mm). He used the low end of the breadth range (125 mm) to calculate a length/breadth ratio of 1.24, a ratio similar to that of the Spooner Egg (1.30). Without explanation Grellet-Tinner et al. (2016) dismiss the entirety of Williams (1981) measurements and base their argument on the single sample represented by the Spooner Egg. We see no reason to reject Williams (1981) PGOM estimate of 155 125 mm based on curvature measurements from 219 large eggshell fragments. Because his measurements are derived from many different eggs, they more likely reflect the average dimensions of PGOM than the Spooner Egg (126 97 mm). Dickison (2007) discusses deriving egg mass from egg dimensions, suggesting that the formula of Worth (1940) is suitable for eggs that are not highly elongate. We use this formula to predict the mass for a PGOM egg (155 125 mm) to be 1220 g Hoyt (1979) uses a slightly different formula that results in an estimated egg mass of 1235 g; we use 1230 g as representative of average
http://dx.doi.org/10.1016/j.quascirev.2016.12.004 0277-3791/© 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
2
G.H. Miller et al. / Quaternary Science Reviews xxx (2017) 1e5
of 0.801 (Dyke and Kaiser, 2010); greater uncertainties are likely for an extinct, flightless bird with no living relatives, and an estimated weight far outside the range of extant birds. Extrapolated onesigma uncertainties on estimates for Genyornis egg mass range between 1230 and 2100 g for a 168 kg parent, and between 1590 and 2890 g for a 275 kg parent. The mass of PGOM derived from Williams' measurements (~1230 g) is within the ±1s uncertainty of the predictions from equations relating extant bird mass to egg mass; therefore, we conclude that the mass of PGOM is consistent with the egg mass predicted for a Genyornis parent, within accepted uncertainties. 5. PGOM is inconsistent with Progura as parent bird Grellet-Tinner et al. (2016) argue that the extinct megapode Progura is a more plausible parent bird for PGOM than Genyornis. Below we bring to bear data showing that it is highly unlikely that any megapode could be parent to PGOM. 5.1. Megapodes have the wrong diet Fig. 1. Map of Australia showing the primary PGOM collection regions in gray, the known fossil occurrences of Progura (yellow circles; from Boles, 2008), the Lake Eyre Basin, and contemporary mean annual precipitation isohyets for 400 and 300 mm. The 400 mm isohyet inscribes the arid zone. WA: Northwest Cape, Western Australia; KT-LE: Kati-Thanda Lake-Eyre, SA; PA: Port Augusta, SA; FR: Lake Frome, SA; DR: Darling-Murray River region, NSW. Modified from Miller et al. (2016b). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
PGOM mass. The same equations predict the mass of the Spooner Egg to be only ~600 g. 4. The mass of PGOM is consistent with the predicted mass of a Genyornis egg Whether an average PGOM mass of ~1230 g is consistent with a Genyornis parent hinges on two factors: the accuracy of estimated Genyornis body mass and uncertainties on the correlation between egg mass and body mass. Genyornis body mass estimates are derived from skeletal remains. Body mass estimates derived from specific bones of extant birds have typical uncertainties of a factor of two (Dickison, 2007; Dyke and Kaiser, 2010). Although Genyornis was not a ratite (Murray and Megirian, 1998), a comparison with that group is probably the most realistic. However, Dickison (2007: Abstract) notes that while “mid-shaft femur circumference is the best measure to use in estimating avian body mass .… the small sample size of extant ratites makes mass estimate extrapolation to larger extinct species inaccurate”. Predictions of Genyornis body mass vary widely. Murray and Megirian (1998) give a range of 250e350 kg, whereas Chan (2014) estimates 325e445 kg based on femoral circumference, 168e253 kg based on tibiotarsal circumference, and 139 kg from one skeleton. It is apparent that the paleontological community has yet to reach consensus on body mass estimates for Genyornis. Grellet-Tinner et al. (2016) use a body mass for Genyornis of 168e275 kg, which we follow here, while noting that the uncertainties are probably larger, given that the lineage is extinct and no extant birds from which these predictions are derived approach the size of Genyornis. Estimating egg mass from body mass (Fig. 2) is even more tenuous (Birchard and Deeming, 2009; Dickison, 2007). The mass of a Genyornis egg given by Grellet-Tinner et al. (2016) (1609 g for a 168 kg bird and 2212 g for a 275 kg bird) is based on a regression derived exclusively from extant, precocial flighted birds, with an r2
Megapodes are strictly omnivorous, opportunistic ground foragers with varied diets including plants, insects, small reptiles, and carrion (Jones et al., 1995; Marchant and Higgins, 1993). Malleefowl (Leipoa), the extant Australian megapode so closely related to Progura that Boles (2008) placed them in the same genus, consume a variety of insects and reptiles, especially during the breeding season (Harlen and Priddel, 1996; Reichelt and Jones, 2008; Jones and Goth, 2008). Because d15N is enriched by 3e4‰ with each trophic level (DeNiro and Epstein, 1981), the high proportion of animal components in Progura diet will be reflected in the d15N of organic components in their eggshell. We test whether the bird responsible for PGOM practiced omnivory during the breeding season by comparing the d15N in PGOM eggshell (n ¼ 476) with d15N in eggshell of co-habitating sameage Dromaius (n ¼ 410), which rarely consume more than 5% non-plant food sources (Davies, 1978; Dawson et al., 1984). Eggshell we sampled was calcified between 140 and 50 ka from four regions across the Australian arid zone (Fig. 1). The mean d15N in PGOM (11.2 ± 0.12‰) differs by only 0.5‰ from the mean d15N in Dromaius eggshell (10.7 ± 0.11‰; SE: standard error of the mean). If the parent bird of PGOM had 50% animal-based diet at the time of breeding, d15N in PGOM would be 1.5e2‰ heavier than in Dromaius eggs, and likely even greater, since some of the animals known to be consumed by megapodes are themselves omnivorous, hence even more enriched in 15N. The d15N indicate that the female bird responsible for PGOM eggshell fed at the same trophic level as Dromaius (<5% animal diet), unlike the diet of megapodes. 5.2. Australian sand dunes are too cold to incubate Progura eggs Megapodes rely on external heat sources to incubate their eggs. All extant Australian megapode taxa nest in self-built vegetation mounds, in which microbial decomposition of plant remains provides the heat to incubate the developing embryos; none nest in sand. Egg incubation requires closely regulated temperatures with little fluctuation, and male birds tend their nests carefully to regulate nest temperatures (Jones et al., 1995). In tropical regions non-mound-building some megapodes bury their eggs in hollows excavated in sand, often associated with geothermal water. Observed incubation temperatures for sand-nesting megapodes remained at 33 ± 2 C with incubation times of 60e80 days (Dekker, 1988). Malleefowl (Leipoa) organic nests are maintained at similar temperatures (32e35 C; Booth, 1987). In our >1500 collections containing PGOM, all, other than rare fragments reworked
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
G.H. Miller et al. / Quaternary Science Reviews xxx (2017) 1e5
3
Fig. 2. Regression lines for the relation between female bird mass and egg mass and for all extant species with all extant ratites plotted as single points (from Dickison, 2007). The left-most ratite points are all species of New Zealand Kiwi. The position of a 168 kg female bird and 1230 g egg representing PGOM is shown in yellow. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
in beach and fluvial channels, were found in organic-free sand dunes, including numerous in situ, but incomplete, eggs. We found no evidence that PGOM were incubated in vegetation mounds. Recognizing the lack of evidence that PGOM were laid in organic mounds, Grellet-Tinner et al. (2016: p.162) suggest “Progura likely just scratched a shallow hole in the sand into which they laid their eggs”. The problem with this conjecture is that Australian sand dunes are too cold for reproductive success. Unlike decaying vegetation, sand does not generate heat; the only source of heat is diurnal solar energy. At the relatively shallow depths eggs would be laid, sand temperatures closely track mean weekly air temperature, which would have to be above 30 C to incubate megapode eggs. Mildura, VIC, is representative of the Darling region (Fig. 1) where there are many PGOM collection sites. The 70-year Mildura mean temperature for January, the hottest month, is 24.5 C (http:// www.bom.gov.au/climate/averages/tables/cw_076031.shtml), which would be the likely temperature of dune sand at nest depth; it is far too low for successful incubation and hatching of nestlings. For Port Augusta (Fig. 1), the site of the Spooner Egg, the mean January temperature is 25.7 C, also far too low, and mean temperatures would have been even lower during glacial periods (Miller et al., 1997).
5.3. Megapode eggs are the wrong shape and Progura is too small Extant megapode eggs are highly elongate (Dekker and Brom, 1990). Length-breadth ratios are 1.61 ± 0.05 for brush turkey, malleefowl and scrubfowl (Dekker and Brom, 1990), whereas Williams (1981) estimated a PGOM length-breadth ratio of 1.24, and the Spooner Egg is 1.30 (Fig. 3). The elongate shape of megapode eggs is important when evaluating Fig. 11 of Grellet-Tinner et al. (2016), which compares extant megapode female mass to the length of their egg, with the goal of showing that an extrapolation predicts an egg length for a 5 kg megapode similar to the length of the Spooner Egg (126 mm).
Obvious flaws in their regression are that it predicts, for example, that an egg length of 62 mm would require a bird to weigh less than zero grams, an impossibility, and that the authors apparently included their predicted length for a 5 kg megapode in their derived regression. More importantly, egg mass does not scale linearly to egg length, and the predicted mass of a 126-mm-long elongate megapode egg is only 399 g, whereas the more spherical 126mm-long Spooner Egg has a predicted mass of 609 g, based on equations in Marchant and Higgins (1993). Most analyses that compare bird and egg sizes utilize log-log plots of bird mass to egg mass (Dickison, 2007; Dyke and Kaiser, 2010). Following this convention, we derive the predicted mass of a 5 kg megapode egg utilizing bird- and egg-mass data for five extant species of Australian megapodes provided by Dekker and Brom (1990) based on over 1500 measured eggs. Their data, which span nearly the same range of bird mass as used by Grellet-Tinner et al. (2016), predicts an egg mass for a 5 kg megapode to be ~340 g (Fig. 4), far less than PGOM's estimated mass of 1230 g, which, extrapolating from Fig. 4 would require a 45 kg megapode parent. 5.4. PGOM eggshell is too thick to be from a megapode Megapode eggs are characteristically thin, typically 31% thinner than expected for their size when calcified (Booth, 1987). The eggshell thins significantly during incubation, so after fossilization, post-hatching eggshell fragments should be even thinner. This is inconsistent with the observations that preserved PGOM eggshell are about the same thickness as Dromaius eggshell. 5.5. PGOM d13Corg/d13Ccarb offset differs from that in megapode eggs The d13C of both calcite (d13Ccarb) and organic (d13Corg) fractions of avian eggshell are set by the mother bird's diet, offset by biological fractionation factors. From d13Ccarb and 13Corg in 347 PGOM eggshell across the geographic range in Fig. 1, we found the mean
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
4
G.H. Miller et al. / Quaternary Science Reviews xxx (2017) 1e5
relate to differential routing of macromolecules to the organic and calcite fractions of the eggshell. All megapode chicks are super-precocial. To support this, megapode eggs have exceptionally high yolk content, rich in 13C-depleted lipids. For isotopic massbalance the residual bodily carbon reservoir mobilized for eggshell production should be enriched in 13C, resulting in 13C enrichment of the bird's blood CO2, the carbon source for eggshell calcite. The large difference in the isotopic offset between PGOM and megapode eggs suggests PGOM is not from a megapode parent, and the much smaller offset in PGOM suggests that PGOM chicks were not super-precocial, unlike all megapodes. 5.6. There is no overlap in known geographic distributions The known Progura fossil materials have no overlap with the known distribution of PGOM eggshell (Fig. 1). In contrast, Genyornis fossil localities overlap with the distribution of PGOM eggshell. Absence of evidence is not evidence of absence, but the lack of Progura overlap with PGOM and the close correspondence between Genyornis skeletal material and PGOM are consistent with PGOM being derived from Genyornis. 6. Summary and conclusions
Fig. 3. Comparison of the shapes of a typical elongate megapode egg (Megapodius; upper panel) and the more spherical Spooner Egg, a nearly complete PGOM (lower panel); not to scale. Upper panel credit Alfred William Strutt, The Game Birds of India, Burmah and Ceylon, Public Domain; lower panel image provide by T. Worthy.
and SE for the offset (d13Ccarb -d13Corg) is 11.5 ± 0.1‰, without significant trends between climate zones. This differs significantly from the mean offset in eggshell of the megapode Alectura, 15.5 ± 0.9‰ (Clarke, 2005). The larger offset in megapodes may
The lack of PGOM directly associated with Genyornis skeletal remains is not surprising, partly because bones have much lower preservation potential than eggshell, but also because it is unlikely that the birds' breeding grounds correspond with where they died. However, this does raise the question whether attribution of a Genyornis parent to PGOM (Williams, 1981) is certain. Grellet-Tinner et al. (2016) question that association based only on the dimensions of the Spooner Egg. We argue that Williams' (1981) careful measurements provide a more reliable estimate of the average dimensions of PGOM, resulting in an estimated mass of ~1230 g. Given the uncertainties in regressions of egg mass to bird mass, a ~1230 g egg is within the range predicted for a parent bird with a mass of 168 kg. Hence, the size of PGOM is fully consistent a Genyornis assignment. Grellet-Tinner et al. (2016) argue that the extinct 5 kg megapode Progura is the likely parent bird for PGOM. Taking all the evidence as a whole, the assignment of PGOM to a megapode (Progura) source remains unlikely, if not impossible. The female bird responsible for the PGOM egg had a diet incompatible with a megapode, PGOM are found in environments incapable of maintaining the required temperatures for successful unaided incubation of the egg, and the offset between eggshell d13Ccarb and 13Corg are inconsistent with a megapode parent. PGOM are relatively spherical whereas megapode eggs are highly elongate, PGOM are too thick to be from a megapode, and PGOM mass (1230 g) is too great to be derived from for a 5 kg megapode, which is predicted to lay a 340 g egg. As there is no other large bird known to have inhabited the Australian arid zone during the Late Quaternary other than Dromaius and Genyornis, a Genyornis parent is far more compatible with the available evidence than a Progura parent, and we argue that PGOM remain classified as Genyornis eggshell until more secure evidence of an alternative parent bird is provided. Acknowledgements
Fig. 4. Log-log plot of bird mass against egg mass for extant Australian megapodes, with the regression line derived exclusively from extant birds extended to provide an estimate of the predicted egg mass for a 5 kg megapode (340 g), far less than the 1230 g predicted mass for PGOM. Data are from Dekker and Brom (1990).
Primary funding for our research on the Quaternary history of the Australian arid zone was provided through U.S. National Science Foundation grants BCS-0914821, EAR-0949398, ATM0502632, ATM-0082254, ATM-9709806, ATM-9311303 to GHM and MLF, and Australian Research Council grants F00103660 and
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
G.H. Miller et al. / Quaternary Science Reviews xxx (2017) 1e5
A00102515 to JWM, with additional support from the University of Colorado Boulder, Carnegie Institution of Washington, University of California Merced, the Australian National Unive-rsity, and Curtin University. References Birchard, G.F., Deeming, D.C., 2009. Avian eggshell thickness: scaling and maximum body mass in birds. J. Zool. 279, 95e101. Boles, W., 2008. Systematics of the fossil Australian giant megapodes Progura (Aves: Megapodiidae). Oryctos 7, 195e215. Booth, D.T., 1987. Effect of temperature on development of Mallee Fowl Leipoa ocellata eggs. Physiol. Zool. 60, 437e445. Chan, N.R., 2014. Does size variation in Genyornis newtoni (Aves, Dromornithidae) encompass eggshell safety limits? J. Vertebr. Paleontol. 34, 976e979. Clarke, S.J., 2005. Isoleucine Epimerisation and Stable Isotope Ratio Studies of Cassowary, Megapode and Aepyornis Eggshells: Biogeochemical and Palaeoenvironmental Implications. School of Earth and Environmental Sciences, University of Wollongong. Doctoral thesis. Davies, S.J.J.F., 1978. The food of emus. Aust. J. Ecol. 3, 411e422. Dawson, T.J., Read, D., Russell, E.M., Herd, R.M., 1984. Seasonal variations in the daily activity and patterns, water relations, and diet of emus. Emu 84, 93e102. Dekker, R.W.R.J., 1988. Notes on ground temperatures at nesting sites of the Maleo Macrocephalon maleo (Megapodiidae). Emu 88, 124e127. Dekker, R.W.R.J., Brom, T.G., 1990. Maleo eggs and the amount of yolk in relation to different incubation strategies in megapodes. Aust. J. Zool. 38, 19e24. DeNiro, M.J., Epstein, S., 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45, 341e351. Dickison, M.R., 2007. The Allometry of Giant Flightless Birds. Duke University. PhD Thesis, Biology. Dyke, G.J., Kaiser, G.W., 2010. Cracking a developmental constraint: egg size and bird evolution. Rec. Aust. Mus. 62, 207e216. Dzialowski, E.M., Sotherland, P.R., 2004. Maternal effects of egg size on emu Dromaius novaehollandiae egg composition and hatchling phenotype. J. Exp. Biol. 207, 597e606. Grellet-Tinner, G., Spooner, N.A., Worthy, T.H., 2016. Is the “Genyornis” egg of a mihirung or another extinct bird from the Australian dreamtime? Quat. Sci. Rev. 133, 147e164. Harlen, R., Priddel, D., 1996. Potential food resources available to malleefowl Leipoa ocellata in marginal mallee lands during drought. Aust. J. Ecol. 21, 418e428. Hoyt, D., 1979. Practical methods of estimating volume and fresh weight of bird eggs. Auk 96, 73e77. Jones, D., Goth, D., 2008. Mound-builders. CSIRO publishing, Collingwood, Australia. Jones, D.N., Dekker, R.W.R.J., Roselaar, C.S., 1995. Bird Families of the World: the
5
Megapodes. Oxford University Press, Oxford. Marchant, S., Higgins, P.J.E., 1993. Handbook of Australian, New Zealand and Antarctic Birds. Oxford University Press, Melbourne. Miller, G.H., Magee, J.W., Jull, A.J.T., 1997. Low-latitude glacial cooling in the Southern Hemisphere from amino acid racemization in emu eggshells. Nature 385, 241e244. Miller, G.H., Fogel, M.L., Magee, J.W., Gagan, M.K., 2016b. Disentangling the impacts of climate and human colonization on the flora and fauna of the Australian arid zone over the past 100 ka using stable isotopes in avian eggshell. Quat. Sci. Rev. 151, 27e57. Murray, P.F., Megirian, D., 1998. The skull of dromornithid birds: anatomical evidence for their relationship to Anseriformes. Rec. South Aust. Mus. 31, 51e97. Reichelt, R.C., Jones, D.N., 2008. Long-term observations of the diet of the malleefowl Leipoa ocellata near the Little Desert, Western Victoria. Aust. Field Ornithol. 25, 22. Sauer, E.G.F., 1968. Calculations of struthious egg sizes from measurements of shell fragments and their correlation with phylogenetic aspects. Cimbebasia Ser. A 1, 27e55. Sauer, E.G.F., 1978. Bezugswerte für vergleichende Untersuchungen an aepyornithi€ ße und Form. J. Ornithol. 119, 412e420. den Eierschalen: Gro Williams, D.L.G., 1981. Genyornis eggshell (Dromornithidae; Aves) from the Late Pleistocene of South Australia. Alcheringa 5, 133e140. Worth, C., 1940. Egg volumes and incubation period. Auk 57, 44e60.
Gifford H. Millera,b,*, Marilyn L. Fogelc, John W. Mageed, Simon J. Clarkee a INSTAAR and Geological Sciences, University of Colorado, Boulder, CO 80309, USA b c d
Curtin University, Perth, Australia
University of California, Riverside, USA
Australian National University, Australia e
Charles Sturt University, Australia *
Corresponding author. E-mail address: [email protected] (G.H. Miller). 6 November 2016 Available online xxx
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
Contents lists available at ScienceDirect
Quaternary Science Reviews journal homepage: www.elsevier.com/locate/quascirev
The Genyornis egg: A commentary on Grellet-Tinner et al., 2016
1. Summary When humans colonized Australia three giant flightless birds were on the landscape, of which the largest, Genyornis newtoni, the sole remaining taxon of the mihirungs, became extinct. Although nearly complete skeletons of Genyornis have been found, they never have been linked directly to an egg. Williams (1981) recognized and described distinct morphological characteristics demonstrating that eggshell fragments from two different taxa were preserved in arid-zone sand dunes. One type had characteristics identical to those of emu (Dromaius novaehollandiae), whereas the other was dissimilar to any extant bird. Based on its estimated volume exceeding that of modern emu egg, he attributed the newly discovered eggshell to Genyornis. Attribution of these eggshell to a Genyornis parent was recently challenged by Grellet-Tinner et al. (2016), who suggested that an extinct megapode of the genus Progura was a more likely candidate parent. They refer to the eggshell Williams (1981) assigned to Genyornis as “putative Genyornis oological material” (PGOM), which for convenience we follow here. The goal of this commentary is to support our claim that Genyornis is by far the most likely candidate parent bird for PGOM, and to show why it is highly unlikely that any megapode could be parent to PGOM. 2. The Grellet-Tinner et. al., 2016 argument Grellet-Tinner et al. (2016) argue that PGOM is unlikely to be derived from Genyornis primarily based on egg size, relying on the only nearly complete PGOM eggshell, the Spooner Egg, found partly intact in aeolian sand near Port Augusta (Fig. 1). Based on the dimensions of the reconstructed Spooner Egg, Grellet-Tinner et al. (2016) argue that PGOM is too small for a bird with the body mass estimated for Genyornis (168e275 kg) even at the low end of the estimates; they predict an egg mass of 1600e2200 g. None of the additional PGOM observations reported by GrelletTinner et al. (2016) are inconsistent with a Genyornis parent. Having concluded that the PGOM egg is too small, Grellet-Tinner et al. (2016) suggest that an extinct 5 kg megapode (Progura) is the more likely parent bird. Extant megapode eggs are unusually large for the parent's body mass, and they argue that extrapolating a plot of bird mass vs. egg length for extant megapodes predicts an egg with a length similar to the Spooner Egg for Progura. 3. Correctly estimating the mass of PGOM A weakness in the Grellet-Tinner et al. (2016) argument is their dependence on the Spooner Egg, which measures 126 97 mm, to
represent typical PGOM dimensions. Eggs of extant birds are known to vary substantially in size and mass, even within a single clutch. For example, Dromaius eggs range between 400 and 700 g, but may reach 900 g (Dzialowski and Sotherland, 2004). Hence, a single sample cannot accurately represent the range of possible dimensions for PGOM. Williams (1981) provides a more thorough estimate of PGOM dimensions. Although Williams never found a whole PGOM, he collected and studied many large fragments. He argued “since the transverse section of an egg is circular, its curvature is a direct measure of egg width at that point. With a suitably large sample of shell fragments there is a good chance that the equatorial region will be represented, so by selection of the smallest values of transverse curvature the actual width of the egg can be estimated” (Williams, 1981: p. 134). The accuracy of this method for reconstructing egg dimensions from eggshell fragments has been documented for modern and fossil Struthionidae (ostrich) eggshell (Sauer, 1968), and for Aepyornis, the elephant bird of Madagascar (Sauer, 1978). Williams tested this assertion, by breaking five modern emu eggs into fragments with areas similar to those of the PGOM that he measured, and used the curvature in those fragments to estimate a breadth of 92.5 ± 2.5 mm, consistent with the breadth of the two whole eggs he used in his experiments (94 mm), and the average of another 32 whole eggs he measured (90.5 ± 3.9 mm). Following the same technique, he measured the curvature of 219 large PGOM fragments, from which their calculated breadth ranged between 125 and 134 mm (Williams, 1981), a considerably larger breadth than for the Spooner Egg (97 mm). Determining egg length from random fragments is more difficult. Williams (1981) estimated an average PGOM length of 155 mm (range: 125e185 mm). He used the low end of the breadth range (125 mm) to calculate a length/breadth ratio of 1.24, a ratio similar to that of the Spooner Egg (1.30). Without explanation Grellet-Tinner et al. (2016) dismiss the entirety of Williams (1981) measurements and base their argument on the single sample represented by the Spooner Egg. We see no reason to reject Williams (1981) PGOM estimate of 155 125 mm based on curvature measurements from 219 large eggshell fragments. Because his measurements are derived from many different eggs, they more likely reflect the average dimensions of PGOM than the Spooner Egg (126 97 mm). Dickison (2007) discusses deriving egg mass from egg dimensions, suggesting that the formula of Worth (1940) is suitable for eggs that are not highly elongate. We use this formula to predict the mass for a PGOM egg (155 125 mm) to be 1220 g Hoyt (1979) uses a slightly different formula that results in an estimated egg mass of 1235 g; we use 1230 g as representative of average
http://dx.doi.org/10.1016/j.quascirev.2016.12.004 0277-3791/© 2016 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
2
G.H. Miller et al. / Quaternary Science Reviews xxx (2017) 1e5
of 0.801 (Dyke and Kaiser, 2010); greater uncertainties are likely for an extinct, flightless bird with no living relatives, and an estimated weight far outside the range of extant birds. Extrapolated onesigma uncertainties on estimates for Genyornis egg mass range between 1230 and 2100 g for a 168 kg parent, and between 1590 and 2890 g for a 275 kg parent. The mass of PGOM derived from Williams' measurements (~1230 g) is within the ±1s uncertainty of the predictions from equations relating extant bird mass to egg mass; therefore, we conclude that the mass of PGOM is consistent with the egg mass predicted for a Genyornis parent, within accepted uncertainties. 5. PGOM is inconsistent with Progura as parent bird Grellet-Tinner et al. (2016) argue that the extinct megapode Progura is a more plausible parent bird for PGOM than Genyornis. Below we bring to bear data showing that it is highly unlikely that any megapode could be parent to PGOM. 5.1. Megapodes have the wrong diet Fig. 1. Map of Australia showing the primary PGOM collection regions in gray, the known fossil occurrences of Progura (yellow circles; from Boles, 2008), the Lake Eyre Basin, and contemporary mean annual precipitation isohyets for 400 and 300 mm. The 400 mm isohyet inscribes the arid zone. WA: Northwest Cape, Western Australia; KT-LE: Kati-Thanda Lake-Eyre, SA; PA: Port Augusta, SA; FR: Lake Frome, SA; DR: Darling-Murray River region, NSW. Modified from Miller et al. (2016b). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
PGOM mass. The same equations predict the mass of the Spooner Egg to be only ~600 g. 4. The mass of PGOM is consistent with the predicted mass of a Genyornis egg Whether an average PGOM mass of ~1230 g is consistent with a Genyornis parent hinges on two factors: the accuracy of estimated Genyornis body mass and uncertainties on the correlation between egg mass and body mass. Genyornis body mass estimates are derived from skeletal remains. Body mass estimates derived from specific bones of extant birds have typical uncertainties of a factor of two (Dickison, 2007; Dyke and Kaiser, 2010). Although Genyornis was not a ratite (Murray and Megirian, 1998), a comparison with that group is probably the most realistic. However, Dickison (2007: Abstract) notes that while “mid-shaft femur circumference is the best measure to use in estimating avian body mass .… the small sample size of extant ratites makes mass estimate extrapolation to larger extinct species inaccurate”. Predictions of Genyornis body mass vary widely. Murray and Megirian (1998) give a range of 250e350 kg, whereas Chan (2014) estimates 325e445 kg based on femoral circumference, 168e253 kg based on tibiotarsal circumference, and 139 kg from one skeleton. It is apparent that the paleontological community has yet to reach consensus on body mass estimates for Genyornis. Grellet-Tinner et al. (2016) use a body mass for Genyornis of 168e275 kg, which we follow here, while noting that the uncertainties are probably larger, given that the lineage is extinct and no extant birds from which these predictions are derived approach the size of Genyornis. Estimating egg mass from body mass (Fig. 2) is even more tenuous (Birchard and Deeming, 2009; Dickison, 2007). The mass of a Genyornis egg given by Grellet-Tinner et al. (2016) (1609 g for a 168 kg bird and 2212 g for a 275 kg bird) is based on a regression derived exclusively from extant, precocial flighted birds, with an r2
Megapodes are strictly omnivorous, opportunistic ground foragers with varied diets including plants, insects, small reptiles, and carrion (Jones et al., 1995; Marchant and Higgins, 1993). Malleefowl (Leipoa), the extant Australian megapode so closely related to Progura that Boles (2008) placed them in the same genus, consume a variety of insects and reptiles, especially during the breeding season (Harlen and Priddel, 1996; Reichelt and Jones, 2008; Jones and Goth, 2008). Because d15N is enriched by 3e4‰ with each trophic level (DeNiro and Epstein, 1981), the high proportion of animal components in Progura diet will be reflected in the d15N of organic components in their eggshell. We test whether the bird responsible for PGOM practiced omnivory during the breeding season by comparing the d15N in PGOM eggshell (n ¼ 476) with d15N in eggshell of co-habitating sameage Dromaius (n ¼ 410), which rarely consume more than 5% non-plant food sources (Davies, 1978; Dawson et al., 1984). Eggshell we sampled was calcified between 140 and 50 ka from four regions across the Australian arid zone (Fig. 1). The mean d15N in PGOM (11.2 ± 0.12‰) differs by only 0.5‰ from the mean d15N in Dromaius eggshell (10.7 ± 0.11‰; SE: standard error of the mean). If the parent bird of PGOM had 50% animal-based diet at the time of breeding, d15N in PGOM would be 1.5e2‰ heavier than in Dromaius eggs, and likely even greater, since some of the animals known to be consumed by megapodes are themselves omnivorous, hence even more enriched in 15N. The d15N indicate that the female bird responsible for PGOM eggshell fed at the same trophic level as Dromaius (<5% animal diet), unlike the diet of megapodes. 5.2. Australian sand dunes are too cold to incubate Progura eggs Megapodes rely on external heat sources to incubate their eggs. All extant Australian megapode taxa nest in self-built vegetation mounds, in which microbial decomposition of plant remains provides the heat to incubate the developing embryos; none nest in sand. Egg incubation requires closely regulated temperatures with little fluctuation, and male birds tend their nests carefully to regulate nest temperatures (Jones et al., 1995). In tropical regions non-mound-building some megapodes bury their eggs in hollows excavated in sand, often associated with geothermal water. Observed incubation temperatures for sand-nesting megapodes remained at 33 ± 2 C with incubation times of 60e80 days (Dekker, 1988). Malleefowl (Leipoa) organic nests are maintained at similar temperatures (32e35 C; Booth, 1987). In our >1500 collections containing PGOM, all, other than rare fragments reworked
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
G.H. Miller et al. / Quaternary Science Reviews xxx (2017) 1e5
3
Fig. 2. Regression lines for the relation between female bird mass and egg mass and for all extant species with all extant ratites plotted as single points (from Dickison, 2007). The left-most ratite points are all species of New Zealand Kiwi. The position of a 168 kg female bird and 1230 g egg representing PGOM is shown in yellow. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
in beach and fluvial channels, were found in organic-free sand dunes, including numerous in situ, but incomplete, eggs. We found no evidence that PGOM were incubated in vegetation mounds. Recognizing the lack of evidence that PGOM were laid in organic mounds, Grellet-Tinner et al. (2016: p.162) suggest “Progura likely just scratched a shallow hole in the sand into which they laid their eggs”. The problem with this conjecture is that Australian sand dunes are too cold for reproductive success. Unlike decaying vegetation, sand does not generate heat; the only source of heat is diurnal solar energy. At the relatively shallow depths eggs would be laid, sand temperatures closely track mean weekly air temperature, which would have to be above 30 C to incubate megapode eggs. Mildura, VIC, is representative of the Darling region (Fig. 1) where there are many PGOM collection sites. The 70-year Mildura mean temperature for January, the hottest month, is 24.5 C (http:// www.bom.gov.au/climate/averages/tables/cw_076031.shtml), which would be the likely temperature of dune sand at nest depth; it is far too low for successful incubation and hatching of nestlings. For Port Augusta (Fig. 1), the site of the Spooner Egg, the mean January temperature is 25.7 C, also far too low, and mean temperatures would have been even lower during glacial periods (Miller et al., 1997).
5.3. Megapode eggs are the wrong shape and Progura is too small Extant megapode eggs are highly elongate (Dekker and Brom, 1990). Length-breadth ratios are 1.61 ± 0.05 for brush turkey, malleefowl and scrubfowl (Dekker and Brom, 1990), whereas Williams (1981) estimated a PGOM length-breadth ratio of 1.24, and the Spooner Egg is 1.30 (Fig. 3). The elongate shape of megapode eggs is important when evaluating Fig. 11 of Grellet-Tinner et al. (2016), which compares extant megapode female mass to the length of their egg, with the goal of showing that an extrapolation predicts an egg length for a 5 kg megapode similar to the length of the Spooner Egg (126 mm).
Obvious flaws in their regression are that it predicts, for example, that an egg length of 62 mm would require a bird to weigh less than zero grams, an impossibility, and that the authors apparently included their predicted length for a 5 kg megapode in their derived regression. More importantly, egg mass does not scale linearly to egg length, and the predicted mass of a 126-mm-long elongate megapode egg is only 399 g, whereas the more spherical 126mm-long Spooner Egg has a predicted mass of 609 g, based on equations in Marchant and Higgins (1993). Most analyses that compare bird and egg sizes utilize log-log plots of bird mass to egg mass (Dickison, 2007; Dyke and Kaiser, 2010). Following this convention, we derive the predicted mass of a 5 kg megapode egg utilizing bird- and egg-mass data for five extant species of Australian megapodes provided by Dekker and Brom (1990) based on over 1500 measured eggs. Their data, which span nearly the same range of bird mass as used by Grellet-Tinner et al. (2016), predicts an egg mass for a 5 kg megapode to be ~340 g (Fig. 4), far less than PGOM's estimated mass of 1230 g, which, extrapolating from Fig. 4 would require a 45 kg megapode parent. 5.4. PGOM eggshell is too thick to be from a megapode Megapode eggs are characteristically thin, typically 31% thinner than expected for their size when calcified (Booth, 1987). The eggshell thins significantly during incubation, so after fossilization, post-hatching eggshell fragments should be even thinner. This is inconsistent with the observations that preserved PGOM eggshell are about the same thickness as Dromaius eggshell. 5.5. PGOM d13Corg/d13Ccarb offset differs from that in megapode eggs The d13C of both calcite (d13Ccarb) and organic (d13Corg) fractions of avian eggshell are set by the mother bird's diet, offset by biological fractionation factors. From d13Ccarb and 13Corg in 347 PGOM eggshell across the geographic range in Fig. 1, we found the mean
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
4
G.H. Miller et al. / Quaternary Science Reviews xxx (2017) 1e5
relate to differential routing of macromolecules to the organic and calcite fractions of the eggshell. All megapode chicks are super-precocial. To support this, megapode eggs have exceptionally high yolk content, rich in 13C-depleted lipids. For isotopic massbalance the residual bodily carbon reservoir mobilized for eggshell production should be enriched in 13C, resulting in 13C enrichment of the bird's blood CO2, the carbon source for eggshell calcite. The large difference in the isotopic offset between PGOM and megapode eggs suggests PGOM is not from a megapode parent, and the much smaller offset in PGOM suggests that PGOM chicks were not super-precocial, unlike all megapodes. 5.6. There is no overlap in known geographic distributions The known Progura fossil materials have no overlap with the known distribution of PGOM eggshell (Fig. 1). In contrast, Genyornis fossil localities overlap with the distribution of PGOM eggshell. Absence of evidence is not evidence of absence, but the lack of Progura overlap with PGOM and the close correspondence between Genyornis skeletal material and PGOM are consistent with PGOM being derived from Genyornis. 6. Summary and conclusions
Fig. 3. Comparison of the shapes of a typical elongate megapode egg (Megapodius; upper panel) and the more spherical Spooner Egg, a nearly complete PGOM (lower panel); not to scale. Upper panel credit Alfred William Strutt, The Game Birds of India, Burmah and Ceylon, Public Domain; lower panel image provide by T. Worthy.
and SE for the offset (d13Ccarb -d13Corg) is 11.5 ± 0.1‰, without significant trends between climate zones. This differs significantly from the mean offset in eggshell of the megapode Alectura, 15.5 ± 0.9‰ (Clarke, 2005). The larger offset in megapodes may
The lack of PGOM directly associated with Genyornis skeletal remains is not surprising, partly because bones have much lower preservation potential than eggshell, but also because it is unlikely that the birds' breeding grounds correspond with where they died. However, this does raise the question whether attribution of a Genyornis parent to PGOM (Williams, 1981) is certain. Grellet-Tinner et al. (2016) question that association based only on the dimensions of the Spooner Egg. We argue that Williams' (1981) careful measurements provide a more reliable estimate of the average dimensions of PGOM, resulting in an estimated mass of ~1230 g. Given the uncertainties in regressions of egg mass to bird mass, a ~1230 g egg is within the range predicted for a parent bird with a mass of 168 kg. Hence, the size of PGOM is fully consistent a Genyornis assignment. Grellet-Tinner et al. (2016) argue that the extinct 5 kg megapode Progura is the likely parent bird for PGOM. Taking all the evidence as a whole, the assignment of PGOM to a megapode (Progura) source remains unlikely, if not impossible. The female bird responsible for the PGOM egg had a diet incompatible with a megapode, PGOM are found in environments incapable of maintaining the required temperatures for successful unaided incubation of the egg, and the offset between eggshell d13Ccarb and 13Corg are inconsistent with a megapode parent. PGOM are relatively spherical whereas megapode eggs are highly elongate, PGOM are too thick to be from a megapode, and PGOM mass (1230 g) is too great to be derived from for a 5 kg megapode, which is predicted to lay a 340 g egg. As there is no other large bird known to have inhabited the Australian arid zone during the Late Quaternary other than Dromaius and Genyornis, a Genyornis parent is far more compatible with the available evidence than a Progura parent, and we argue that PGOM remain classified as Genyornis eggshell until more secure evidence of an alternative parent bird is provided. Acknowledgements
Fig. 4. Log-log plot of bird mass against egg mass for extant Australian megapodes, with the regression line derived exclusively from extant birds extended to provide an estimate of the predicted egg mass for a 5 kg megapode (340 g), far less than the 1230 g predicted mass for PGOM. Data are from Dekker and Brom (1990).
Primary funding for our research on the Quaternary history of the Australian arid zone was provided through U.S. National Science Foundation grants BCS-0914821, EAR-0949398, ATM0502632, ATM-0082254, ATM-9709806, ATM-9311303 to GHM and MLF, and Australian Research Council grants F00103660 and
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004
G.H. Miller et al. / Quaternary Science Reviews xxx (2017) 1e5
A00102515 to JWM, with additional support from the University of Colorado Boulder, Carnegie Institution of Washington, University of California Merced, the Australian National Unive-rsity, and Curtin University. References Birchard, G.F., Deeming, D.C., 2009. Avian eggshell thickness: scaling and maximum body mass in birds. J. Zool. 279, 95e101. Boles, W., 2008. Systematics of the fossil Australian giant megapodes Progura (Aves: Megapodiidae). Oryctos 7, 195e215. Booth, D.T., 1987. Effect of temperature on development of Mallee Fowl Leipoa ocellata eggs. Physiol. Zool. 60, 437e445. Chan, N.R., 2014. Does size variation in Genyornis newtoni (Aves, Dromornithidae) encompass eggshell safety limits? J. Vertebr. Paleontol. 34, 976e979. Clarke, S.J., 2005. Isoleucine Epimerisation and Stable Isotope Ratio Studies of Cassowary, Megapode and Aepyornis Eggshells: Biogeochemical and Palaeoenvironmental Implications. School of Earth and Environmental Sciences, University of Wollongong. Doctoral thesis. Davies, S.J.J.F., 1978. The food of emus. Aust. J. Ecol. 3, 411e422. Dawson, T.J., Read, D., Russell, E.M., Herd, R.M., 1984. Seasonal variations in the daily activity and patterns, water relations, and diet of emus. Emu 84, 93e102. Dekker, R.W.R.J., 1988. Notes on ground temperatures at nesting sites of the Maleo Macrocephalon maleo (Megapodiidae). Emu 88, 124e127. Dekker, R.W.R.J., Brom, T.G., 1990. Maleo eggs and the amount of yolk in relation to different incubation strategies in megapodes. Aust. J. Zool. 38, 19e24. DeNiro, M.J., Epstein, S., 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45, 341e351. Dickison, M.R., 2007. The Allometry of Giant Flightless Birds. Duke University. PhD Thesis, Biology. Dyke, G.J., Kaiser, G.W., 2010. Cracking a developmental constraint: egg size and bird evolution. Rec. Aust. Mus. 62, 207e216. Dzialowski, E.M., Sotherland, P.R., 2004. Maternal effects of egg size on emu Dromaius novaehollandiae egg composition and hatchling phenotype. J. Exp. Biol. 207, 597e606. Grellet-Tinner, G., Spooner, N.A., Worthy, T.H., 2016. Is the “Genyornis” egg of a mihirung or another extinct bird from the Australian dreamtime? Quat. Sci. Rev. 133, 147e164. Harlen, R., Priddel, D., 1996. Potential food resources available to malleefowl Leipoa ocellata in marginal mallee lands during drought. Aust. J. Ecol. 21, 418e428. Hoyt, D., 1979. Practical methods of estimating volume and fresh weight of bird eggs. Auk 96, 73e77. Jones, D., Goth, D., 2008. Mound-builders. CSIRO publishing, Collingwood, Australia. Jones, D.N., Dekker, R.W.R.J., Roselaar, C.S., 1995. Bird Families of the World: the
5
Megapodes. Oxford University Press, Oxford. Marchant, S., Higgins, P.J.E., 1993. Handbook of Australian, New Zealand and Antarctic Birds. Oxford University Press, Melbourne. Miller, G.H., Magee, J.W., Jull, A.J.T., 1997. Low-latitude glacial cooling in the Southern Hemisphere from amino acid racemization in emu eggshells. Nature 385, 241e244. Miller, G.H., Fogel, M.L., Magee, J.W., Gagan, M.K., 2016b. Disentangling the impacts of climate and human colonization on the flora and fauna of the Australian arid zone over the past 100 ka using stable isotopes in avian eggshell. Quat. Sci. Rev. 151, 27e57. Murray, P.F., Megirian, D., 1998. The skull of dromornithid birds: anatomical evidence for their relationship to Anseriformes. Rec. South Aust. Mus. 31, 51e97. Reichelt, R.C., Jones, D.N., 2008. Long-term observations of the diet of the malleefowl Leipoa ocellata near the Little Desert, Western Victoria. Aust. Field Ornithol. 25, 22. Sauer, E.G.F., 1968. Calculations of struthious egg sizes from measurements of shell fragments and their correlation with phylogenetic aspects. Cimbebasia Ser. A 1, 27e55. Sauer, E.G.F., 1978. Bezugswerte für vergleichende Untersuchungen an aepyornithi€ ße und Form. J. Ornithol. 119, 412e420. den Eierschalen: Gro Williams, D.L.G., 1981. Genyornis eggshell (Dromornithidae; Aves) from the Late Pleistocene of South Australia. Alcheringa 5, 133e140. Worth, C., 1940. Egg volumes and incubation period. Auk 57, 44e60.
Gifford H. Millera,b,*, Marilyn L. Fogelc, John W. Mageed, Simon J. Clarkee a INSTAAR and Geological Sciences, University of Colorado, Boulder, CO 80309, USA b c d
Curtin University, Perth, Australia
University of California, Riverside, USA
Australian National University, Australia e
Charles Sturt University, Australia *
Corresponding author. E-mail address: [email protected] (G.H. Miller). 6 November 2016 Available online xxx
Please cite this article in press as: Miller, G.H., et al.The Genyornis egg: A commentary on Grellet-Tinner et al., 2016, Quaternary Science Reviews (2017), http://dx.doi.org/10.1016/j.quascirev.2016.12.004