Fig 1.
Cranium and nasal passage of the two ankylosaur species used for this study.
The nodosaurid, Panoplosaurus mirus, ROM 1215 (A) and the ankylosaurid, Euoplocephalus tutus, AMNH 5405 (B). Non-modeled nasal passages are shown in greyscale.
Fig 2.
Summary of models analyzed in this study.
Panoplosaurus (A,B,E,F) and Euoplocephalus (C,D,G,H) nasal passages were modeled as preserved, or bony-bounded (A,C), with soft-tissue correction (B,D), simplified (E,G) or with all convolutions removed (F,H). See Methods section for specifics for each model.
Fig 3.
Airflow and heat transfer within the left nasal passage of a pigeon (Columba livia).
(A) Airway was segmented out from the head and (B) converted into a volumetric mesh for CFD analysis following methods in the text. (C) Heat transfer simulation was performed under an inspiratory flow condition and data from that simulation was used to inform (D) the expiratory flow conditions. Artificial laryngotracheal extension was omitted in C & D as no data from that region was used.
Table 1.
Comparison of values for heat transfer in domestic pigeons (Columba livia) between experimental data [38] and simulation (this study).
Fig 4.
Heat flow within the BB nasal passage of Panoplosaurus mirus (ROM 1215) during inspiration under both high (left) and low (right) flow scenarios.
Numbers of dotted lines indicate cross-section numbers. Cross sections were taken at equivalent locations on both models.
Fig 5.
Heat flow within the soft-tissue corrected nasal passage of Panoplosaurus mirus (ROM 1215) during inspiration under both high (left) and low (right) flow scenarios.
Numbers of dotted lines indicate cross-section numbers. Cross sections were taken at equivalent locations on both models.
Fig 6.
Airflow through the basic airway of Panoplosaurus mirus (ROM 1215).
(A) Left lateral view of nasal passage with air streams showing general air field pattern. Airway is color-coded for temperature (hotter colors = hotter temperatures. Inset: Sagittal cross section of the nasal vestibule and CNP showing central stream of cool air passing through the nasal vestibule. (B) Temperature at the nostril during expiration for the basic airway and the ST airway.
Fig 7.
Airflow comparison between the straightened airway and the ST airway in Panoplosaurus mirus (ROM 1215).
(A) Dorsal view of the skull of P. mirus with left ST airway in situ. (B) Dorsal view of the straightened airway with flow lines in place. Airflow lines are color-coded for temperature (hotter colors = hotter temperatures). Inset: Magnified region of nasal vestibule showing evenly spaced, straight flow lines. (C) Dorsal view of the ST airway under the low flow scenario. Vorticity is observable throughout the nasal vestibule. Note: ST airway in C is not to scale with straightened airway B.
Fig 8.
Heat flow within the BB nasal passage of Euoplocephalus tutus (AMNH 5405) during inspiration under both high (left) and low (right) flow scenarios.
Numbers of dotted lines indicate cross-section numbers. Cross sections were taken at equivalent locations on both models.
Fig 9.
Heat flow within the soft-tissue corrected nasal passage of Euoplocephalus tutus (AMNH 5405) during inspiration under both high (left) and low (right) flow scenarios.
Numbers of dotted lines indicate cross-section numbers. Cross sections were taken at equivalent locations on both models.
Fig 10.
Airflow through the basic airway of Euoplocephalus tutus (AMNH 5405).
(A) Left lateral view of basic airway showing airflow. Streamlines are color-coded for heat (hotter colors = hotter temperatures). Inset: Sagittal cross section of airway showing persistent stream of cool air traversing the nasal vestibule and interacting with the CNP. (B) Temperature at the nostril during expiration for the basic airway and the ST airway.
Fig 11.
Airflow comparison between the straightened airway and the ST airway in Euoplocephalus tutus (AMNH 5405).
(A) Dorsal view of the skull of E. tutus with the left ST airway in situ. (B) Dorsal view of the straightened airway with flow lines in place. Airflow lines are color-coded for temperature (hotter colors = hotter temperatures). Inset: Magnified region of nasal vestibule showing evenly spaced, straight flow lines. (C) Dorsal view of the ST airway under the low flow scenario showing the presence of vorticity throughout the nasal vestibule. Note: ST airway in C is not to scale with straightened airway B.
Table 2.
Energetic cost of heating one bolus of air by 20°C at 50% relative humidity for Panoplosaurus mirus and Euoplocephalus tutus.
Table 3.
Energy savings from reducing expired air temperature in all airway models for Panoplosaurus mirus.
Table 4.
Energy savings from reducing expired air temperature in all airway models for Euoplocephalus tutus.
Table 5.
Core body temperatures recorded for a variety of large, terrestrial amniotes.
Fig 12.
Heat and water savings calculated for the most efficient airway models of Panoplosaurus mirus and Euoplocephalus tutus vs. various extant animals.
Note that variations in experimental protocol means that, although these results are comparable, they should not be viewed as fully equivalent. See Methods for details on graph calculation and references for extant data.
Fig 13.
Heat and water savings between all nasal airway models for Panoplosaurus mirus (top) and Euoplocephalus tutus (bottom).
Models are organized from greatest savings to least in both graphs. Abbreviations: ST low, soft-tissue low flow rate; ST high, soft-tissue high flow rate; BB low, bony-bounded low flow rate; BB high, bony-bounded high flow rate; Straight, straightened airway; basic, basic airway.
Fig 14.
Vascular reconstruction of the venous pathway in the left oronasal apparatus of Euoplocephalus (AMNH 5405).
Venous reconstruction followed the methods of Porter [72]. Red highlighted veins indicate main channels of heat transfer from the oronasal apparatus to the brain.
Fig 15.
Airway reconstruction and soft-tissue correction in Panoplosaurus mirus (ROM 1215).
(A) Initial CT-based bony-bounded segmentation of airway within the skull and (B) isolated BB airway. (C) Airway cleaned and separated, with the addition of a soft-tissue naris and nasopharyngeal duct exiting into an artificially created laryngotracheal region. (D) Nasal passage digitally compressed to reduce airway caliber, better simulating the mucosa-lined airways of extant amniotes. Black lines indicate locations of cross sections (E–F). (E) Cross section of original BB airway caliber. (F) Cross section of airway after soft-tissue correction.
Fig 16.
Airway reconstruction and soft-tissue correction in Euoplocephalus tutus (AMNH 5405).
(A) Initial CT-based bony-bounded segmentation of airway within the skull and (B) isolated. (C) Airway cleaned and separated, with the addition of a soft-tissue naris and nasopharyngeal duct exiting into an artificially created laryngotracheal region. (D) Nasal passage digitally compressed to reduce airway caliber, better simulating the mucosa-lined airways of extant amniotes. Black lines indicate locations of cross sections (E–F). (E) Original bony-bounded airway caliber. (F) Airway caliber after soft-tissue correction.
Fig 17.
Alternate airway models for Panoplosaurus mirus.
(A) Dorsal view of the straightened airway (removal of nasal vestibule curvature) and the original, ST-corrected airway. (B) Lateral view of skull of P. mirus (ROM 1215) with basic airway in situ. A direct connection between the bony narial aperture and the CNP in a loss of 55% of the original nasal vestibule.
Fig 18.
Alternate airway models for Euoplocephalus tutus.
(A) Dorsal view of the straightened airway (removal of nasal vestibule curvature) and the original, ST-corrected airway. (B) Lateral view of skull of E. tutus (AMNH 5405) with basic airway in situ. A direct connection between the bony narial aperture and the CNP resulted in a loss of 80% of the original nasal vestibule.
Table 6.
Nasal vestibule size compared with body mass and endocast volume.
Table 7.
Size estimates of ankylosaurs from the Dinosaur Park Formation.
Fig 19.
Example of flow in a hypothetical, serial pipe (top) vs. a parallel pipe (bottom).
Resistance is sensitive to the pipe’s caliber, giving the parallel pipe greater resistance on the outset. However, the parallel arrangement of the smaller caliber tubes offsets some of the increased resistance, resulting in only a modest increase in overall resistance, while simultaneously increasing surface area to volume ratios. In the above example, the parallel pipe has half the caliber of the serial pipe, but is split into fourteen partitions, resulting in approximately identical resistance to the single, serial pipe.
Fig 20.
Airway of the lizard Uromastyx aegyptia (OUVC 10688) in (A) oblique left lateral and (B) dorsal view. As with ankylosaurs, the nasal passage (yellow) exhibits convolutions that increase surface area. (C) Horizontal CT slice image reveals that “slabs” of mucosa are responsible for compressing the airway. It is likely that these mucosal slabs are well vascularized, which would aid in heat and water savings during respiration in this taxon.
Fig 21.
Segmentation of the airway in Panoplosaurus mirus (ROM 1215).
(A) Skull in left lateral view. Line represents the location of (B) axial CT section showing preserved olfactory turbinates. (C) Diagram of CT image showing caliber of airway vs. entire nasal cavity. (D) Segmented olfactory turbinate in same plane as CT image.
Fig 22.
Nostril placement in ankylosaur models.
All skulls in right lateral and rostral views. For Panoplosaurus mirus (A, C) we used (A) ROM 1215 as our base model with nostril placement informed by (C) CMN 8530. For Euoplocephalus tutus (B, D) we used (B) AMNH 5405 as our base model with the skull of (D) ROM 1930 informing us on the limits to the extent of the nostril. Asterisks in A and B denote location of fleshy nostril in our models.
Fig 23.
Lateral and ventral views of extant diapsid skulls illustrating the location of the choana.
Crocodylians such as (A) Alligator mississippiensis (OUVC 9412) have a greatly retracted, apomorphic secondary choana. Inset: The bony boundaries to the secondary choana correspond to the soft-tissue boundaries. Birds such as (B) Meleagris gallopavo (OUVC 9647) retain the plesiomorphic placement of the choana. Inset: Magnified palatal region showing the difference between the bony boundaries to the choana (left side of image) and the soft-tissue boundaries (right side of image). Lizards such as (C) Iguana iguana (OUVC 10446) similarly show the plesiomorphic position of the choana. Inset: Relationship between the bony boundaries to the choana (left side of image) and the more restricted soft-tissue boundaries (right side of image).
Fig 24.
Palate identification and placement in Euoplocephalus tutus (AMNH 5405).
(A) Skull in lateral and (B) ventral view. Inset: Major features of the palatal region. We refer to the caudodorsal secondary palate as equivalent to the lamina transversa observed in many mammals (C). Image in C modified from Cave [124].
Fig 25.
Palate identification and choana placement in Panoplosaurus mirus (ROM 1215).
(A) Skull in lateral and (B) ventral view. Inset: Major features of the palatal region.
Fig 26.
Generic airway diagram for diapsids.
Note the much more constricted airway in the soft-tissue nasal passage (A) vs. the emptier, bony-bounded nasal passage typically preserved in fossils (B).
Fig 27.
Mesh example for Panoplosaurus mirus (ROM 1215).
(A) Nasal passage was assigned a series of boundary conditions (color-coded). Black line indicates location of (B) axial cross section illustrating the distribution of volumetric cells within the nasal passage.
Table 8.
Respiratory values for the ankylosaurs Panoplosaurus mirus and Euoplocephalus tutus.
Fig 28.
Final model resolutions used for simulations.
Surrounding graphs show sample adaptive mesh comparisons between different model resolutions for temperature and velocity within parts of the nasal vestibule.
Table 9.
Taxa used for comparative energy savings graph.
Table 10.
Inspiratory values for taxa studied.
Table 11.
Heat energy savings among taxa studied.