Nesting behavior in early birds

A) The fossil eggs as found on site. B) The eggshell as seen under light microscopy (there are three layers of eggshell because the fossil is collapsed onto itself).
A) The fossil eggs as found on site. B) The eggshell as seen under light microscopy (there are three layers of eggshell because the fossil eggs is broken and collapsed onto itself).

A large number of fossils were found during the 1980s in the late Cretaceous rocks of Neuquén, Argentina. Among these fossils, there were a large amount of eggshell fragments and some intact whole eggs which contained embryonic bone fragments and, in one case, an articulated embryo. These bones and eggs almost certainly belong to Enantiornithes, an extinct group of basal birds; more specifically, they likely belong to the species Neuquenornis volans.

Our research with these birds presented the first evidence for a nesting colony of Mesozoic birds on Gondwana. The Enantiornithes birds nested in an arid and shallow basin, among sand dunes and close to an ephemeral water-course. The eggs were laid either singly or (occasionally) in pairs, onto a sandy substrate. Although there is no evidence for nest structures, the eggs were all half-buried upright in the sand, with their pointed end downwards, a position that would have exposed the pole containing the air cell and precluded egg turning.


Artistic reconstruction of Neuquenornis volans; illustration by B.M. Tomotani.
Artistic reconstruction of Neuquenornis volans on its “nest”; illustration by B.M. Tomotani.

Water vapor conductance

The structure of the eggshell largely determines the incubation and hatching success of reptiles and birds. One of the main physiological properties of an egg is the permeability of its eggshell, meaning the conductance to respiratory gases and water vapor. Gas diffusion through the eggshell pores can be quantified as water vapor conductance (GH2O). The GH2O value is important for assessing moisture content in nesting environments and may also provide additional information on parental nesting strategies.

This measure can be obtained experimentally for modern bird and reptile eggs, but for fossils, where no experiment is possible, it  can  only be calculated by equations. Fortunately, it is a rather simple equation, stemming from work with modern birds. Two oological (i.e., pertaining to the egg) parameters are necessary for this calculation: egg density and egg volume (see the Table below). Egg density was inferred from extant bird eggs. Egg volume must be calculated from the eggs measurements, which basically means, the radius. The shape of the fossil eggs is approximately that of an ellipsoid (more specifically, a prolate spheroid) and ellipsoids have two radii: the Equatorial radius and the polar radius (see Table).

Summary of all parameters, units, equations and results for the fossil eggs.
Summary of all parameters, units, equations and results for the fossil eggs.

We calculated an average GH2O of 4.14 mgH2O/day.Torr for our fossil eggs. Looking at the Table below, it can be seen that this value lies well within the lower end of the known distribution for modern bird eggs (and it is just a little over the only other value known for an enantiornithine bird, the Gobipteryx minuta). Such a low GH2O value indicates relatively little water vapor loss from the eggs and implies an ability to use a dry nesting area with low relative humidity. An arid and dry environment for the site is corroborated by sedimentological data.

GH2O values (in mgH20/day.Torr) for our fossil eggs, alongside those for other taxa from previous studies with fossil and modern eggs.
GH2O values (in mgH20/day.Torr) for our fossil eggs, alongside those for other taxa from previous studies with fossil and modern eggs.

Nesting behavior

As explained above, the eggs were laid singly or in pairs in a single shallow depression on the sand (called a “scrape”), with their pointed side facing downwards. This egg position is not seen in living birds, but it resembles those of some  troodontid theropod dinosaurs that placed their eggs vertically and appear to have hatched by breaking out through the upper pole. Use of the simple “scrapes” as nest structure, however, is known in several modern bird lineages, such as: paleognaths, galloanserans, CharadriiformesFalconiformes, Caprimulgiformes, Otidae and Pteroclidae. Furthermore, the absence of any complex nesting structures and the fact that the fossil eggs were all half-buried suggests that the upper portion of these eggs were exposed on the surface after laying and would thus require an attending brooding parent.

Corresponding with observations on living birds, the relatively low values of GH2O of our fossil eggs may have allowed these early birds to exploit drier patches of habitat. We conclude that these birds present an interesting mixture of primitive and advanced traits. On the one hand, it appears likely that embryos were ventilated by a single, large air chamber (on the larger end of the egg, which is usually found broken off, as by hatching) and used a strategy considered distinctively avian for exiting the egg, while on the other eggs were laid vertically and could not have been turned by the parent. Egg turning is a common behavior in modern birds and is thought to place the embryo in an opportune position and allow effective functioning of the connections between the embryo and the yolk sac: the experimentally unturned eggs of domestic fowl, for instance, have a much higher mortality rate (85%) and take seven hours longer to hatch. We speculate that the vertical nesting strategy evidenced by our fossil eggs was abandoned by later lineages because it was not competitive with the greater incubation success and reduced incubation time of turned eggs. Among modern birds, even the most basal lineages (including some palaeognaths) contain at least some species that turn their eggs.


Bibliography

The preceding text is a summary of the following papers, where this research was published:

  • FERNÁNDEZ, M.S; GARCÍA, R.A.; FIORELLI, L.E.; SCOLARO, A.; SALVADOR, R.B.; COTARO, C.N.; KAISER, G.W.; DYKE, G.J. A Large Accumulation of Avian Eggs from the Late Cretaceous of Patagonia (Argentina) Reveals a Novel Nesting Strategy in Mesozoic Birds. Plos One 8: e61030.  [PDF]
  • SALVADOR, R.B. & FIORELLI, L.E. 2011. Water vapor conductance in fossil early bird eggs and non-avian theropods: implications for the evolution of modern birds exposed nest structure. In: Atas do XXII Congresso Brasileiro de Paleontologia. Natal. Pp. 742-745.  [PDF]