Results of the Dromornithid Paleoneurology Study

Ken Ashwell

Endocranial volume and encephalization

The endocranial volumes (ECV) of the four dromornithid specimens where this could be measured from the CT scans were 126.1 ml for Dromornis stirtoni (NTM-P3249) and 74.8, 93.7 and 81.1 ml (i.e. mean of 83.2 ml) for three specimens of Dromornis planei (NTM-P9973-6, NTM-P9484-106 and NTM-P9464, respectively; see also Table 1).  Figure 3A shows plots of ECV for the two species of dromornithid studied here (Dromornis stirtoni and Dromornis planei) graphed against body weight and compared to minimum side convex polygons enclosing modern birds as a whole (van Dongen, 1998; and Iwaniuk and Nelson, 2003), extant ratites (Ashwell and Scofield, 2008) and moa (Ashwell and Scofield, 2008).  The Iwaniuk and Nelson (2003) dataset for 83 extant anseriformes was also used to predict the expected ECV for an anseriform of the size of the two dromornithid species studied here.  The expected ECV for an anseriform with the estimated body weight of Dromornis stirtoni (490 kg) was found to be 115.1 ml (95% prediction interval of 88.0 to 150.4 ml) and that for Dromornis planei (estimated body weight of 300 kg) was found to be 90.1 ml (95% prediction interval of 68.9 to 117.8 ml).  The actual values of ECV for the dromornithids are therefore very close to what would be predicted for an anseriform of that body size.  The encephalization quotient for each dromornithid specimen i (EQi) was calculated from EQi = Ei/0.1371Wi0.568 using allometric constants for the correlation of brain volume (Ei) versus body mass (Wi) derived from measurements of 1,482 species of birds (r = 0.939; Iwaniuk and Nelson, 2003).  The EQ of Dromornis stirtoni was found to be 0.539 and that for the 3 specimens of Dromornis planei was 0.423, 0.529, 0.459 (mean of 0.470).

Figure 3B shows ECV plotted against body weight for birds as a group, the moa, dromornithids and the largest elephant-bird of Madagascar (Aepyornis maximus).  ECV of Ae. maximus was estimated as 68.2 ml by extrapolating from the measured length of the brain (70 mm; Edinger, 1942).  This has been compared with large-bodied mammals (large ungulates, proboscideans, cetaceans, seals; van Dongen, 1998).  Although there is considerable overlap in ECV for mammals and birds at bodyweights below 100 kg, none of the large bodied birds (i.e. body weight above 100 kg) have an ECV that falls within the range for large-bodied mammals.

Absolute and proportional volumes of endocranial regions

Figure 4 shows CT scan images of the two species of dromornithid in sagittal (A, B) and frontal (C to E) planes and a reconstruction of the endocranial volume (F).  The ECV (Fig. 5A) and absolute and proportional sizes of subregions of the endocranial cavity as measured from CT scans of the 4 specimens of dromornithid are summarised in Table 1 and compared with values for extinct and living ratites, also from CT scans (Ashwell and Scofield, 2008).  The volume of the olfactory bulb was measured from the CT scans and found to be 0.47 ml in a specimen of Dromornis planei (NTM-P9973-6) and 0.54 ml in a specimen of Dromornis stirtoni (NTM-P3249).  These are respectively 0.63% and 0.43% of ECV for those specimens.  These proportional sizes of the olfactory bulbs are lower than values obtained in the same way for living and extinct ratites (Table 1), but there were insufficient dromornithid specimens to test this difference for statistical significance.  The combined volume of the forebrain and midbrain was 95.2 ml for Dromornis stirtoni (75.5% of ECV) and 55.4, 62.6 and 70.5 ml for 3 specimens of Dromornis planei (74.1 to 77.1% of ECV).  The proportional size of the fore- and midbrain in dromornithids was significantly larger than that previously found for ratites, as tested by the Mann-Whitney U test (df = 9, p < 0.05, non-directional).  Pituitary fossa volume was 2.85 ml (2.26% of ECV) in Dromornis stirtoni and 1.17, 1.35 and 1.40 ml (1.44 to 1.80% of ECV) in 3 specimens of Dromornis planei.  This proportional size of the pituitary fossa was not significantly different from ratites (df = 9, p > 0.05).  The volume of the hindbrain in the single specimen of Dromornis stirtoni was 27.5 ml (21.8% of ECV) and 17.4 to 21.8 ml (21.4 to 23.5% of ECV) in Dromornis planei.  This proportional size of the hindbrain was also not significantly different from that in ratites (df = 9, p > 0.05).

Orbital dimensions and optic canal area

There are no surviving dromornithid scleral ossicles, so the only available indirect indicators of ocular size are orbital diameter and area.  Optic nerve cross-sectional area can also be inferred indirectly from optic canal area, provided one assumes that the proportion of the canal occupied by connective tissue and vasculature is similar at all body sizes.  Actual values for orbital diameter, orbital area and optic canal area were compared with predicted values based on linear regression of measurements from 37 species of extant anseriforms (Supplementary Table 1).  Predictions were made for anseriformes of either the body weight of the dromornithids (i.e. 490 kg for Dromornis stirtoni and 300 kg for Dromornis planei; Table 2) or the ECV of the dromornithids (mean ECV for the two species).

Average orbital diameter (mean of left and right sides + SD) was calculated for the fossils and was 57.0 (+ 0.14) mm for 2 specimens of Dromornis stirtoni and 56.1 (+ 1.4) mm for 3 specimens of Dromornis planei. (Tables 2 and 3)  The predicted orbital diameters for anseriformes with the body weight of the two dromornithid species (Table 2) were slightly above the actual measurements for Dromornis stirtoni (predicted value of 67.6 mm, with a 95% prediction range of 57.7 to 79.2 mm, compared to an actual value of 57.0 mm), but the predicted orbital diameter for Dromornis planeiagreed well with the observed measurement (predicted value of 61.4 mm, with a 95% prediction range of 52.4 to 72.0, compared to an actual mean value of 56.1 mm).  The orbital diameters predicted for anseriformes with the ECV of the two dromornithids were in close agreement with the actual values (see Table 3) and within the 95% prediction ranges.

Average orbital area (+ SD) for one side was 3570 (+ 566) mm2 for 2 specimens of Dromornis stirtoni and 3069 (+ 263) mm2 for 3 specimens of Dromornis planei.  The observed orbital areas for the two dromornithids agreed well with the predicted values based on body weight (Table 2), but predicted orbital areas based on ECV were substantially lower than actual values, particularly for Dromornis planei, where the actual mean value of 3069 mm2 was twice the area predicted for an anseriform with an ECV of that size and outside the 95% prediction range of 784 to 2510 mm2.  The combination of large orbital areas with close-to-predicted orbital diameters suggests that the globes of the eyes were more deeply recessed in large orbits of the dromornithids, compared to modern anseriformes.

Optic canal area (+ SD) for the dromornithids was 21.9 (+ 9.7) mm2 for 4 specimens of Dromornis planei, but this could not be measured in any of the D. stirtoni specimens.  Predicted optic canal area for an anseriform with the body weight of Dromornis planei (128 mm2) was more than 5-fold larger than the actual observed value and the observed value fell well below the 95% prediction range (74 to 222 mm2)(Table 2).  A similar discrepancy between predicted and actual optic canal area was observed when the prediction was based on anseriform ECV (see Fig. 5B and Table 3).  This suggests that the optic canal was much smaller in the Dromornis planei than would be expected for either body or brain size.

Skeletal evidence for stereopsis or lack thereof: orbital convergence and Wulst area

Stereopsis is the ability to form a single representation of the visual world from the fusion of images provided by the two eyes.  It is a key component of effective depth perception.  In birds, the ability to perform stereopsis can be measured by the angle of convergence (Iwaniuk et al., 2008), which is the dihedral angle between the plane of the orbital margin of each eye and the midsagittal plane.  The quadratojugal bar is lost from the dromornithid fossils, so the orbital margin plane can only be defined by a line between the anterior and posterior margins of the orbit (see OA and OP in Figure 2 and caption).  It was found that the orbital convergence angle was 27.5o and 28.6o for two specimens of Dromornis stirtoni (NTM-P9810, NTM-P3249) and 21.1o, 20.1o, 24.9o for 3 specimens of Dromornis planei (NTM9973-6, NTM9464-111, NTM-9484-106).  These are comparable to those reported for the domestic duck Anas platyrhynchos (Iwaniuk et al., 2008).  The mean angle between the orbital axis and the midsagittal plane was also measured in both dromornithid species.  It was found to be 62.5o and 66.2o for 2 specimens of Dromornis stirtoni (NTM-P3249, NTM-P9810) and 53.6o, 51.0o and 49.6o for 3 specimens of Dromornis planei (NTM-P9973-6, NTM-P9464-111, NTM-P9484-106).  These angles are suggestive of minimal convergence of the two eyes in both species of dromornithids.

The relative size of the Wulst of the telencephalon has also been shown to be an indicator of stereopsis, because the part of the forebrain that produces this distinctive bulge (the hyperpallium apicale) is (at least in part) concerned with stereopsis.  The greater the proportional size of the Wulst in a bird, the greater is the capacity for stereopsis (Iwaniuk and Wylie, 2006).  Values for the area of the Wulst (both sides combined) in absolute terms, and as a proportion of fore- and midbrain area were 1190 mm2 and 11.8% for NTM-P3249 (Dromornis stirtoni), 932 mm2 and 13.3% for NTM-P9973-6 (Dromornis planei), 866 mm2 and 10.5% for NTM-P9484-106 (Dromornis planei), and 827 mm2 and 10.8% for NTM-P9464 (Dromornis planei).  Wulst area in other large birds was found to be 965 mm2 for Aepyornis maximus (based on measurements made in the present study of a photograph in Edinger, 1942).  Wulst area has previously been measured at 1112 mm2 and 18.3% of combined fore- and midbrain surface area for a female specimen of Dinornis (giganteus) robustus (Ashwell and Scofield, 2008).  The size of the Wulst in a range of birds was used to predict the expected Wulst for a bird with the ECV of the two dromornithid species (Fig. 5C and Table 3).  The predicted Wulst area for a bird with the ECV of Dromornis stirtoni was slightly higher than the actual value (1505 mm2 compared to 1191 mm2) and also higher than the actual for Dromornis planei (1120 mm2 compared to a mean observed area of 856 mm2), but observed areas for both species were well within the relevant 95% prediction ranges (912 to 2486 mm2 and 678 to 1850 mm2, respectively, see Fig. 5C and Table 3).

Oculomotor canal

The area of the oculomotor canal in 5 specimens of Dromornis planei was 7.6 mm2, with a SD of + 3.0 mm2.  This canal could not be measured in the Dromornis stirtoni specimens.  The predicted oculomotor canal area for an anseriform of the body weight of Dromornis planei was 17.9 mm2 (95% prediction range of 7.3 to 44.3 mm2), so the observed value is at the lower end of the prediction range based on body weight.  On the other hand, the predicted oculomotor canal area for an anseriform of the ECV of Dromornis planei was found to be 8.7 mm2 (95% prediction range of 3.4 to 22.5 mm2), indicating that oculomotor canal size is within the range of size that could be expected for an anseriform of the brain size of Dromornis planei.

Skeletal evidence of trigeminal specialization

The skeletal feature that may provide clues to trigeminal specialization of the beak or bill in dromornithids is the maxillomandibular or trigeminal canal, which transmits the maxillary and mandibular divisions of the trigeminal nerve (V2, V3) in birds.  This was found to have an area of 22.6 mm2 in one specimen of Dromornis stirtoni and mean (+ SD) of 15.4 (+ 4.6) mm2 in 6 specimens of Dromornis planei.  The predicted maxillomandibular canal area was calculated for both dromornithid species based on their body weight (Table 2) and ECV (Fig. 5D and Table 3).  The predicted maxillomandibular canal area based on body weight was comparable to the observed value for Dromornis stirtoni(predicted value of 28.8 mm2, with a 95% prediction range of 14.1 to 58.9 mm2) and Dromornis planei (predicted value of 24.8 mm2, with a 95% prediction range of 12.1 to 50.7 mm2).  There was an even closer concordance between predicted and observed maxillomandibular canal area based on ECV (Fig. 5D and Table 3).  These findings indicate that the size of the maxillomandibular canal observed in the two species of dromornithid is within the range of size that could be expected for an anseriform of that body and brain size.

Carotid canal

The carotid canal transmits the internal carotid artery and provides an indirect indication of the cerebral arterial flow to the brain.  The cross-sectional area of this structure could only be measured in one specimen of Dromornis planei (35.4 mm2).  The predicted size of the canal for an anseriform of the body weight of Dromornis planei was 15.2 mm2 (with a 95% prediction range of 6.5 to 36.0 mm2).  The predicted size of the canal for the ECV of Dromornis planei was 11.2 mm2with a 95% prediction range of 4.9 to 25.7 mm2 (Table 3).  The carotid canal is therefore more than three times the size that would be expected for the ECV of Dromornis planei, but just within the predicted range given the body size of the dromornithid.

External otic recess area and semicircular canals

Tympanic area cannot be directly measured in the fossils.  However, it is possible to estimate the maximum potential size of the tympanum from the area encircled by the rim of the external otic recess (in both the fossils and modern anseriformes; Murray and Vickers-Rich, 2004).  This was measured in sagittal CT scans of one specimen of D. stirtoni(NTM-P3249), CT scans of three specimens of D. planei (NTM-P9464, NTM-P9646-105 and NTM-P9973-6) and from calibrated photographs of 33 modern anseriform species.  The measured external otic recess areas were 345 mm2 for the single D. stirtoni specimen and a mean (+ SD) of 265 (+ 14) mm2 for three D. planei specimens.  The expected areas for anseriformes of those body weights were 742 mm2 (with a 95% prediction range of 407 to 1353 mm2) for D. stirtoniand 556 mm2 (with a 95% prediction range of 305 to 1013 mm2) for D. planei.  This indicates that the actual external otic recess areas of the two dromornithid species studied are smaller than would be expected for an anseriform of that body weight.  However, the actual areas for both species were within the expected values for anseriformes of those ECV (Fig. 5E).  The expected external otic recess area for an ECV of D. stirtoni was 473 mm2 (with a 95% prediction range of 259 to 864 mm2) and the expected area for an ECV of D. planei was 311 mm2 (with a 95% prediction range of 170 to 568 mm2).  This suggests that tympanum size was appropriate for the ECV of these two fossil dromornithid species.

The maximal diameters of the loops of the semicircular canals could be measured in one dromornithid specimen (NTM-9973-6, Fig. 4E).  The lateral (horizontal) semicircular canal loop had a maximal diameter of 5.9 mm, the maximal diameter of the anterior semicircular canal loop was 6.6 mm and that for the posterior semicircular canal was measured as 7.6 mm.

Hypoglossal canal/s

The hypoglossal canal/s transmit the hypoglossal nerves (12n in Fig. 4F), which supply the intrinsic muscles of the tongue, as well as most of the extrinsic muscles.  The area/s of the hypoglossal canal/s (dromornithids may have more than one on each side; Worthy et al., 2015) were found to be a mean (+ SD) of 25.3 (+ 8.5) mm2 for 7 specimens of Dromornis planei, but could not be measured in Dromornis stirtoni.  The predicted size of the hypoglossal canal/s for an anseriform with the body weight of Dromornis planei was 4.00 mm2 (with a 95% prediction range of 1.81 to 8.88 mm2).  The predicted size of the hypoglossal canal/s for an anseriform with the ECV of Dromornis planei (Fig. 5F) was even smaller at 3.08 mm2 (with a 95% prediction range of 1.41 to 6.72 mm2).  These findings suggest that the hypoglossal canal/s are more than 6 times larger than one would expect for an anseriform of the body and brain size of Dromornis planei.

Foramen magnum area

The foramen magnum transmits the spinal cord and can be used as a skeletal indicator of neural connection with the postcranial body.  The mean area (+ SD) of the foramen magnum was 304.4 (+ 123.2) mm2 for Dromornis stirtoni and 290.1 (+105.9) mm2 for Dromornis planei.  The predicted foramen magnum area based on body weight was calculated as 479 mm2 (with a 95% prediction range of 357 to 644 mm2) for Dromornis stirtoni and 393 mm2 (with a 95% prediction range of 293 to 528 mm2) for Dromornis planei.  In other words, the actual foramen magnum sizes for both species were significantly smaller than expected for an anseriform of that body size.  On the other hand, predicted foramen magnum size based on ECV agreed closely with the actual foramen magnum size (see Table 3), indicating that the actual foramen magnum size was about the size one would expect for an anseriform of that brain volume.

Supplementary tables

The original data for the above analyses is available in Supplementary Tables 1 to 4. See below

Figure 3

This figure shows plots of log10 endocranial volume (ECV) against log10 body weight for dromornithids (D. stirtoni and D.planei) in comparison to other birds (A).  Minimum-side convex polygons have been used to encompass values for moa and elephantbirds.  Two minimum-side convex polygons derived from the data sets of other authors have been included for modern birds (221 species - van Dongen, 1998; 1482 species – Iwaniuk and Nelson, 2003) along with the respective regression lines.  The van Dongen avian data, although based on fewer species than that of Iwaniuk and Nelson, includes specimens of higher body weight, which provide a better comparison with moa, elephantbirds and dromornithids.  The lower part of the figure (B) shows avian brain weights against those for large mammals.  The shaded region indicates a minimum-side convex polygon derived from the van Dongen (1998) dataset for mammals, with key large mammal species indicate by symbols and common names.  Note that the brain sizes of all large birds fall well below the range for large mammals.

Figure 4

CT scans of the skulls of Dromornis stirtoni (NTM-P3249 - A, B) and Dromornis planei (C to E).  Matrix fills the skull of NTM-P3249, but the boundary between endocranial cavity and skull can still be seen (marked by asterisks) in A) to D).  The parts of the endocranial cavity in A) and B) have been separated by dashed lines.  Figure F shows a serial section reconstruction of the endocranial volume of NTM-P3249 superimposed on the reconstructed skull.  Scale bar in A) also applies to B).  Scale bar in C) also applies to D). 12n – hypoglossal canal; asc – anterior semicircular canal; Cb - cerebellum; co – cochlea; eor – external otic recess; fm – foramen magnum; hsc – horizontal semicircular canal; Md – medulla oblongata; OB – olfactory bulb; pfl – parafloccular cavity; psc – posterior semicircular canal; sa – saccule; v – vallecula; W – Wulst.

Figure 5

Figure A) shows a plot of ECV (ml) against body weight (kg) for anseriformes (based on data from Iwaniuk and Nelson, 2002) with the 95% prediction interval indicated by the dashed lines and actual values for Dromornis stirtoni and D.planei shown by symbols.  Figure B) shows a plot of the square root of optic canal area against the cube root of ECV (volume expressed in mm3) for anseriformes with 95% prediction interval and actual values as for A).  Figure C) shows the square root of Wulst area (both sides) plotted against the cube root of ECV for selected birds.  Figure D) shows plots of the square root of maxillomandibular canal area plotted against the cube root of ECV.  Figure E) shows the square root of external otic recess area against the cube root of ECV for anseriformes.  Figure F) shows a plot of the square root of hypoglossal canal area against the cube root of ECV for anseriformes.

References

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Iwaniuk AN, Nelson JE (2002) Can endocranial volume be used as an estimate of brain size in birds? Canadian Journal of Zoology 80, 16-23.

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Iwaniuk AN, Heesy CP, Hall MI, Wylie DRW (2008) Relative Wulst volume is correlated with orbit orientation and binocular visual field in birds. Journal of Comparative Physiology A 194, 267-282.

Murray PF, Vickers-Rich P (2004) Magnificent Mihirungs: The Colossal Flightless Birds of the Australian Dreamtime. Indiana University Press, Bloomington & Indianapolis.

Van Dongen PAM (1998) Brain size in vertebrates. In The Central Nervous System of Vertebrates (ed. R. Nieuwenhuys, H. J. Ten Donkelaar, C. Nicholson). Berlin: Springer. pp. 2099–2134.

Worthy TH, Handley WD, Archer M, Hand SJ (2015) The extinct flightless mihirungs (Aves, Dromornithidae): cranial anatomy, a new species, and assessment of Oligo-Miocene lineage diversity. Journal of Vertebrate PaleontologyDOI:10.1080/02724634.2015.103134.