Research Article |
Corresponding author: Mathias Wirkner ( mathias.wirkner@senckenberg.de ) Academic editor: Ingmar Werneburg
© 2022 Mathias Wirkner, Katharina Heyder, Irina Ruf.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Wirkner M, Heyder K, Ruf I (2022) Comparative morphology and postnatal ontogeny of the bony labyrinth in Pantherinae (Felidae, Carnivora) with special emphasis on the lion. Vertebrate Zoology 72: 883-905. https://doi.org/10.3897/vz.72.e82874
|
The bony labyrinth (inner ear) of mammals reveals systematic as well as morphofunctional information. However, detailed knowledge of bony labyrinth morphology and ontogeny in Pantherinae, that comprise some of the most iconic mammals, is still pending. Hence, we present the first comparative description of the bony labyrinth in all extant species of Panthera and Neofelis some of which are represented by several postnatal stages; particular focus is set on Panthera leo. Our study is based on µCT scans and virtual 3D reconstructions and accompanied by selected morphometric measurements. Even though quite similar in morphology, both genera as well as their species can be distinguished by several features, e.g., shape and relative size of the semicircular canals and presence or absence of an osseous secondary crus commune. In case of the latter, P. pardus shows some intraspecific variation. We also traced the reduction of the fossa subarcuata during ontogeny in P. leo which conforms with previous studies. Negative allometry of the bony labyrinth in relation to skull basal length can be observed during ontogeny as demonstrated by P. leo as well as between different sized species. Although not correlated with the length of the cochlear canal, the number of cochlear turns is higher in captive non-adult P. leo and P. tigris, but lower in adult captive P. pardus. If these intraspecific differences are related to captivity or represent an ontogenetic pattern, needs to be evaluated in future studies based on larger samples.
fossa subarcuata, inner ear, µCT, Neofelis, Panthera, petrosal bone
The felid subfamily Pantherinae comprises the genera Panthera and Neofelis, which are found in a variety of habitats and characterized by different kinds of ecology, e.g., hunting and locomotion style as well as habitat (
Though Pantherinae are omnipresent iconic animals in our culture, history and everyday life, significant gaps of knowledge concerning their intracranial structures still exist. This also holds true for the inner ear, which comprises the auditory sensory organ and the vestibular system. The membranous inner ear is housed in the bony labyrinth of the petrosal bone, that reflects size and shape of the soft tissue and therefore can be used for investigation of macerated skulls and fossil specimens (
Previous studies on the inner ear and/or bony labyrinth that also include members of Pantherinae are restricted to selected species that are mostly used for comparison as part of a larger sample. Panthera leo (
However, for the deeper understanding of the morphology and morphofunction of intracranial structures associated with sensory organs, it is important to investigate their ontogeny (
Hence, we present the first detailed morphological description of the bony labyrinth of all extant Pantherinae species. In addition, for the first time, the postnatal ontogeny of the bony labyrinth of P. leo and to some extent of P. tigris and P. pardus is described. Selected morphometric data are used for interspecific comparison and evaluation of ontogenetic transformations.
Based on µCT scans of macerated skulls, the bony labyrinth of seven lions (Panthera leo), three tigers (P. tigris), three leopards (P. pardus), one jaguar (P. onca), one snow leopard (P. uncia), one Sunda clouded leopard (Neofelis diardi) and one mainland clouded leopard (N. nebulosa) were studied. All species are represented by adult stages; the studied P. leo, P. tigris and P. pardus sample comprises also younger ontogenetic stages (Table
Pantherinae specimens considered in the present study. Subspecies are assigned according to recent taxonomy (
Genus | Species | Subspecies | Specimen | Source | Origin | Age | IDAS (modified) |
Panthera | leo | ? | SMF 95010 | Zoo Frankfurt | captive | neonate | 1.1 |
Panthera | leo | ? | SMF 15765 | Zoo Frankfurt | captive | juvenile | 1.2 |
Panthera | leo | ? | SMF 38325 | ? | ? | juvenile | 1.3 |
Panthera | leo | melanochaita | SMF 4643 | Faradje, Democratic Republic Congo, Africa | wild | adult | 3 |
Panthera | leo | ? | SMF 22101 | Northeast Africa | wild | adult | 3 |
Panthera | leo | ? | SMF 22104 | Northeast Africa | wild | adult | 3 |
Panthera | leo | leo? | SMF 1366 | Batavia (today Jakarta, Indonesia) | wild? | adult | 3 |
Panthera | pardus | pardus | SMF 15745 | Daroli, Arsi Province, Ethiopia, Africa | wild | juvenile | 1.2 |
Panthera | pardus | pardus | SMF 16259 | Africa | wild | adult | 3 |
Panthera | pardus | ? | SMF 94342 | Zoo Frankfurt | captive | adult | 3 |
Panthera | pardus | orientalis? | SMF 95992 | Zoo Frankfurt | captive | adult | 3 |
Panthera | onca | ? | SMF 3067 | Paramaribo, Republic of Suriname, South America | wild | adult | 3 |
Panthera | tigris | tigris | SMF 15722 | Zoo Frankfurt | captive | neonate | 1.1 |
Panthera | tigris | sondaica | SMF 15737 | Java, Indonesia | wild? | adult | 3 |
Panthera | tigris | sondaica | SMF 7020 | Bunga-Bonda, Sumatra, Indonesia | wild | adult | 3 |
Panthera | tigris | sondaica | SMF 92259 | Zoo Frankfurt | captive | adult | 3 |
Panthera | uncia | ? | SMF 5419 | Ferghana / Farg‘ona, Farghona Wiloyati, Uzbekistan | wild | adult | 3 |
Neofelis | diardi | diardi? | SMF 15470 | Zoo Frankfurt, from Sumatra, Indonesia | wild (captive) | adult | 3 |
Neofelis | nebulosa | — | SMF 40850 | Zoo Frankfurt | captive | adult | 3 |
Former studies showed, that due to functional constraints no significant intraspecific and intraindividual variation of the bony labyrinth should be present in fast-moving species, as which we categorize Pantherinae (i.e.,
We used the individual dental age stages (IDAS) of
The skull of the neonate P. tigris (SMF 15722) is most similar in size, cranial development and tooth development to the neonate P. leo (SMF 95010) and therefore assigned to IDAS 1.1. The infant P. pardus (SMF 15745) is in a similar tooth eruption sequence stage as SMF 15765 and therefore assigned to IDAS 1.2.
Body mass is taken from literature (
For outgroup comparison, bony labyrinths of further Carnivora from literature (i.e., Acinonyx jubatus, Canis lupus familiaris, Caracal caracal, Eumetopias jubatus, Felis catus, Felis chaus, Priolainurus viverrinus, Puma concolor) were taken into account (
Tomographic data were obtained with the µCT scanner GE phoenix x|ray v|tome|x s that is housed at the Institut für Geowissenschaften und Meteorologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Germany. The P. tigris SMF 15737 specimen was scanned with an Yxlon FF 85 CT located at Yxlon International GmbH, Hamburg, Germany. See Table S1 for details on scan parameters. In order to increase the resolution, the voxel size of some scans was virtually halved (voxel size res 2) during reconstruction of the raw data by applying the res2 tool of the software datos|x reconstruction (GE Sensing & Inspection Technologies GmbH) (
Morphological observations are supported by selected morphometric measurements on the bony labyrinth. Each measurement was conducted three times and a mean value was calculated (Table
Measurements and indices of the bony labyrinth in the studied Pantherinae sample. Asterisk (*) indicates that the ASC-R of Neofelis nebulosa could not be measured exactly due to partial exposure of the canal (see description). Abbreviations: ASC, anterior semicircular canal; BL, skull basal length; cco, canaliculus cochleae; co, cochlea; IEH, inner ear height; L, length; l, left; LSC, lateral semicircular canal; PSC, posterior semicircular canal; R, radius of curvature; r, right; sbl, secondary bony lamina; SC semicircular canals (mean); A, approximation, because the foramen magnum was damaged in this specimen.
Genus | Species | Specimen | IDAS (modified) | BL (mm) | IEH (mm) | IEH/BL | ASC-R (mm) | LSC-R (mm) | PSC-R (mm) | SC-R (mm) | co-L (mm) | cco-L (mm) | co aspect ratio | co turns | Length of sbl regarding first co turn |
Panthera | leo | SMF 95010 | 1.1 | 64.87 | 13.937 | 0.215 | 3.133 | 2.786 | 2.790 | 2.903 | 48.565 | 2.875 | 0.668 | 3.25 | <1/2 |
Panthera | leo | SMF 15765 | 1.2 | 138.57 | 13.677 | 0.099 | 2.997 | 2.635 | 2.968 | 2.867 | 50.735 | 6.740 | 0.608 | 3.25 | ~1/2 |
Panthera | leo | SMF 38325 | 1.3 | 251.72 | 13.691 | 0.054 | 3.249 | 2.739 | 2.877 | 2.955 | 49.687 | 8.828 | 0.647 | 3.25 | ~1/3 |
Panthera | leo | SMF 4643 | 3 | 264.63 | 13.545 | 0.051 | 3.285 | 3.000 | 3.163 | 3.149 | 47.843 | 8.590 | 0.621 | 3.25 | <1/2 |
Panthera | leo | SMF 22101 | 3 | 233.45 | 12.303 | 0.053 | 3.017 | 2.898 | 3.009 | 2.974 | 46.596 | 7.393 | 0.525 | 3 | <1/2 |
Panthera | leo | SMF 22104 | 3 | 240.68 | 13.286 | 0.055 | 3.227 | 3.090 | 2.977 | 3.098 | 46.563 | 8.000 | 0.579 | 2.75 | ~1/3 |
Panthera | leo | SMF 1366 | 3 | 280.77 | 14.113 | 0.050 | 3.387 | 2.935 | 3.281 | 3.201 | 51.733 | 7.330 | 0.574 | 3 | — |
Panthera | pardus | SMF 15745 | 1.2 | 110A | 10.814 | — | 2.807 | 2.615 | 2.797 | 2.740 | 42.430 | — | — | 3.5 | ~1/2 |
Panthera | pardus | SMF 16259 r | 3 | 181.52 | 12.465 | 0.069 | 3.015 | 2.558 | 2.740 | 2.771 | 47.076 | — | — | 3.25 | <1/2 |
Panthera | pardus | SMF 16259 l | 3 | 181.52 | 12.528 | 0.069 | 3.063 | 2.680 | 2.705 | 2.816 | 47.362 | — | — | 3.25 | — |
Panthera | pardus | SMF 94342 | 3 | 197.43 | 11.347 | 0.057 | 2.807 | 2.615 | 2.797 | 2.740 | 44.723 | — | — | 3 | — |
Panthera | pardus | SMF 95992 | 3 | 186.45 | 12.290 | 0.066 | 3.179 | 2.775 | 3.126 | 3.027 | 46.409 | — | — | 3 | — |
Panthera | onca | SMF 3067 | 3 | 194.42 | 13.856 | 0.071 | 3.197 | 2.742 | 2.785 | 2.908 | 50.523 | — | — | 3.5 | <1/2 |
Panthera | tigris | SMF 15722 | 1.1 | 63.72 | 13.596 | 0.213 | 3.200 | 2.831 | 3.021 | 3.017 | 52.196 | 3.001 | — | 3.25 | >1/2 |
Panthera | tigris | SMF 15737 | 3 | 235.18 | 13.128 | 0.056 | 3.039 | 2.815 | 2.731 | 2.862 | 50.940 | 7.900 | — | 3 | <1/2 |
Panthera | tigris | SMF 7020 | 3 | 239.45 | 14.540 | 0.061 | 3.235 | 2.908 | 3.086 | 3.076 | 52.322 | 6.280 | — | 3 | — |
Panthera | uncia | SMF 5419 | 3 | 154.15 | 10.782 | 0.070 | 2.826 | 2.561 | 2.521 | 2.636 | 38.074 | — | — | 3 | — |
Neofelis | diardi | SMF 15470 | 3 | 116.93 | 10.570 | 0.090 | 2.675* | 2.285 | 2.429 | 2.463 | 42.307 | — | — | 3 | <1/2 |
Neofelis | nebulosa | SMF 40850 | 3 | 130.30 | 10.000 | 0.077 | 2.523 | 2.142 | 2.272 | 2.312 | 40.208 | — | — | 3.25 | <3/4 |
Unless otherwise stated, the following measurements were conducted digitally in Avizo® 9.0.1/Avizo® 9.0.1 Lite. For calculating the radius of curvature of each semicircular canal, measurements are taken based on the protocol by
Linear measurements (blue) exemplified on the right bony labyrinth of an adult Panthera leo (SMF 4643) in posterolateral (A), dorsal (B), anterolateral (C) and dorsolateral (D) view. Abbreviations: acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; cco, canaliculus cochleae; cco-L, canaliculus cochleae length; co, cochlea; co-H, cochlear height; co-L, cochlear length; co-W, cochlear width; cp, clipping plane; fv, fenestra vestibuli; IEH, inner ear height; LSC, lateral semicircular canal; PSC, posterior semicircular canal; scc, secondary crus commune; SC-H, semicircular canal height; SC-W, semicircular canal width.
The length of the canaliculus cochleae of P. leo was measured using the SplineProbe tool (Fig.
In order to measure the width of the cochlea, the greatest distance from the vestibular/ventral edge of the aperture of the cochlear fossula to the radial wall of the opposite side of the basal cochlear turn parallel to the plane of the latter was measured (
The height of the cochlea was measured perpendicular to the width of the cochlea as the greatest distance from the apex of the spiral to the plane at the level of the tympanal/dorsal edge of the aperture of the cochlear fossula. This plane was parallel to another plane which went through the basal turn of the cochlear canal (
The cochlea length was measured by using the surface pathway tool. It is measured along the outer curvature of the spiral, starting from the anterior border of the fenestra vestibuli up to the apex of the cochlea (
For the inner ear height (IEH) the linear distance between the dorsal apex of the crus commune and the ventral apex of the cochlea was measured as described by
For the regression analyses we only used adult specimens. In addition, we excluded the right bony labyrinth of SMF 16259, for using only one bony labyrinth from each specimen. Linear regressions were initially done in Microsoft excel® 2010 and PAST 4.03 (
In the following, the bony labyrinth of Panthera leo is described in detail first. This description serves as a base for comparison with all other pantherine species.
Overall, the individual bony labyrinths of the Panthera leo specimens across different ontogenetic stages are quite similar (Figs
Virtual endocasts of the right bony labyrinth of Panthera leo represented by different ontogenetic stages. A–D SMF 95010, neonate (IDAS 1.1); E–H SMF 15765, infant (IDAS 1.2); I–L SMF 38325, infant (IDAS 1.3); M–P SMF 4643, adult (IDAS 3). Abbreviations: aa, anterior ampulla; acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; av, aquaeductus vestibuli; bp, bony protuberance; cc, crus commune; cco, canaliculus cochleae; co, cochlea; de, dorsal extension of the aperture of the cochlear fossula; fv, fenestra vestibuli; la, lateral ampulla; LSC, lateral semicircular canal; pa, posterior ampulla; PSC, posterior semicircular canal; sbl, secondary bony lamina; scc, secondary crus commune. Scale bar: 5 mm.
Ontogenetic transformations of selected structures and proportions in the bony labyrinth of Panthera leo and P. tigris. The y-axis refers to specific ratios, the x-axis refers to IDAS stages. Non-adult stages are represented by one specimen each, adult stages by four in P. leo and two in P. tigris; values of adult specimens are averaged (A–C). A Inner ear height against basal length in P. leo and P. tigris. Size of the radius of curvature of the semicircular canals against basal length in P. leo (B) and P. tigris (C). D Elongation of the canaliculus cochleae during ontogeny in P. leo and P. tigris. Abbreviations: ASC, anterior semicircular canal; BL, skull basal length; cco-L, length of the canaliculus cochleae; IEH, inner ear height; LSC, lateral semicircular canal; PSC, posterior semicircular canal; R, radius of curvature.
The curvature of the semicircular canals is round to oval with only slight undulation. The vestibular apparatus and cochlea are roughly evenly proportioned.
The anterior semicircular canal (ASC) is the most rounded of the semicircular canals in Panthera leo (Figs
The ASC has the largest radius of curvature (R) amongst the three semicircular canals in all studied lion specimens (Table
Proportionally, the SCs of the neonate specimen (IDAS 1.1, SMF 95010) appear to be considerably thicker than the semicircular canals of the specimens in IDAS 1.2, 1.3 and 3 (Fig.
µCT images of the bony labyrinth in Panthera species showing selected structures and ontogenetic transformation of the fossa subarcuata. A neonate P. leo (SMF 95010, IDAS 1.1, right side, transversal), B infant P. leo (SMF 15765, IDAS 1.2, right side, transversal); C infant P. leo (SMF 38325, IDAS 1.3, right side, transversal); D adult P. leo (SMF 4643, right side, oblique transversal); E neonate P. tigris (SMF 15722, IDAS 1.1, left side mirrored, transversal); F adult P. tigris (SMF 15737, right side, transversal); G infant P. pardus (SMF 15745, IDAS1.2, left side mirrored, transversal); H adult P. pardus (SMF 94342, IDAS 3, right side, transversal). Abbreviations: aa, anterior ampulla; acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; av, aquaeductus vestibuli; bv, canal for blood vessels; cc, crus commune; cco, canaliculus cochleae; fs, fossa subarcuata; la, lateral ampulla; LSC, lateral semicircular canal; pa, posterior ampulla; pc, petromastoid canal; PSC, posterior semicircular canal; scc, secondary crus commune; ve, vestibule. Not to scale.
The fossa subarcuata, whose entrance is limited by the ASC, is present in the neonate P. leo (IDAS 1.1, Figs
Virtual 3D models of the right bony labyrinth (red), petrosal bone (grey) and fossa subarcuata (yellow) of Panthera leo revealing ontogenetic changes of size proportions. A–D in dorsomedial view, posterolateral margin to the top and E–G in dorsal view, posterolateral to the top. A, E SMF 95010, neonate (IDAS 1.1); B, F SMF 15765, juvenile (IDAS 1.2); C, G SMF 38325, juvenile (IDAS 1.3); D, H SMF 4643, adult (IDAS 3). Abbreviation: ASC, anterior semicircular canal; co, cochlea; fs, fossa subarcuata; pc, petromastoid canal; PSC, posterior semicircular canal; asterisks (*) refer to unspecified connected cavities. Scale bars: 5 mm.
In all ontogenetic stages of P. leo, the ventral limb and the ampulla of the PSC and the posterior limb of the LSC are fused to form an osseous secondary crus commune. Although their spaces are confluent, the LSC and PSC are partly distinguishable since the lower limb of the PSC is on a lower level as the plane of the LSC, in anterior view (Figs
The ampullae of the semicircular canals, although not prominently inflated, are distinct. Right below the anterior and lateral ampulla there is a bony protuberance into the cavity of the bony labyrinth that is likely associated with the entrance of the anterior and lateral ampullar nerves (CN VIII) (Figs
µCT images of the bony labyrinth in Pantherinae showing the bony protuberance that transmits branches of the nervus vestibulocochlearis (CN VIII) and patterns of the fossa subarcuata. A infant Panthera leo (SMF 15765, IDAS 1.2, right side, transversal); B P. onca (SMF 3067, right side, transversal); C P. uncia (SMF 5419, left side mirrored, transversal); D Neofelis diardi (SMF 15470, left side mirrored, transversal), the ASC is not completely enclosed by the petrosal bone; E N. nebulosa (SMF 40850, right side, transversal). Abbreviations: acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; av, aquaeductus vestibuli; bp, bony protuberance; bv, canal for blood vessels; cc, crus commune; co, cochlea; fs, fossa subarcuata; fv, fenestra vestibuli; LSC, lateral semicircular canal; pa, posterior ampulla; pc, petromastoid canal; PSC, posterior semicircular canal; sbl, secondary bony lamina; scc, secondary crus commune; ve, vestibule. Not to scale.
The aquaeductus vestibuli leaves the vestibule anterior to the crus commune and runs medially. The proximal part is tubelike and increases in length with ongoing age, while the distal part fans out.
The fenestra vestibuli has an oval shape. The fenestra cochleae is hidden by the cochlear fossula and thus not visible in the endocasts as observed in other mammals (e.g.,
In the adult specimens the canaliculus cochleae is a slightly curved, long bony canal, which first thins down in distal direction and then fans out (Figs
SMF 22101 (Fig. S1B, C) features a smaller canal extending from the distal part of the canaliculus cochleae, while in SMF 1366 (Fig. S1J, K) and SMF 38325 (Fig.
The cochlea forms a conical spiral. Except for SMF 22101, all cochlear spirals are sharply pointed (Table
The secondary bony lamina is not or only partly visible in some specimens (µCT slides and digital endocasts), maybe due to scan resolution. In most specimens the secondary bony lamina is traceable close to half a turn of the cochlea and in SMF 95010 half a turn of the cochlea. In SMF 220104 and SMF 38325 it is only visible for one third of a turn and not visible in SMF 1366 (Table
Generally, bony labyrinth morphology of the other Panthera species resembles the patterns observed in P. leo (Figs
Virtual endocasts of the right bony labyrinth of selected Panthera species represented by different ontogenetic stages. A–D infant P. pardus (SMF 15745, left side mirrored); E–H adult P. pardus (SMF 16259); I–L adult P. pardus (SMF 16259, left side mirrored); M–P neonate P. tigris (SMF 15722, left side mirrored); Q–T adult P. tigris (SMF 15737). Abbreviations: aa, anterior ampulla; acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; av, aquaeductus vestibuli; bp, bony protuberance; bv, canal for blood vessels; cc, crus commune; cco, canaliculus cochleae; co, cochlea; de, dorsal extension of the aperture of the cochlear fossula; fv, fenestra vestibuli; la, lateral ampulla; LSC, lateral semicircular canal; pa, posterior ampulla; PSC, posterior semicircular canal; sbl, secondary bony lamina; scc, secondary crus commune. Scale bars: 5 mm.
Virtual endocasts of the right bony labyrinth of selected adult Pantherinae. A–D Panthera onca (SMF 3067); E–H P. uncia (SMF 5419, left side mirrored); I–L Neofelis diardi (SMF 15470, left side mirrored); M–P N. nebulosa (SMF 40850). Abbreviations: aa, anterior ampulla; acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; av, aquaeductus vestibuli; bp, bony protuberance; bv, canal for blood vessels; cc, crus commune; cco, canaliculus cochleae; co, cochlea; fv, fenestra vestibuli; la, lateral ampulla; LSC, lateral semicircular canal; pa, posterior ampulla; PSC, posterior semicircular canal; sbl, secondary bony lamina; scc, secondary crus commune. Scale bars: 5 mm.
When corrected for skull basal length, the larger species (P. leo, P. tigris) have slightly smaller IEH, and thus relatively smaller bony labyrinths, than the smaller species (P. pardus, P. onca, P. uncia) (Fig.
Size comparison of selected structures standardized by basal length in adult stages of all studied Pantherinae species. The values of species represented by multiple specimens are averaged. The linear equation, the coefficient of determination (R²) and the p-value are given in the respective graph. A inner ear height, B cochlear length, C anterior semicircular canal radius of curvature, D lateral semicircular canal radius of curvature, E posterior semicircular canal radius of curvature. Abbreviations: ASC, anterior semicircular canal; BL, skull basal length; co-L, cochlear length; IEH, inner ear height; LSC, lateral semicircular canal; PSC, posterior semicircular canal; R, radius of curvature.
The shape of the semicircular canal curvature varies from round to oval and shows some variation in those species represented by more than one specimen. This is especially the case in P. tigris (Fig.
Slight undulation of the semicircular canals can also be observed in other Panthera species, whereas P. uncia shows the highest degree of undulation in our sample. As in P. leo the ASC shows the largest radius of curvature in all other Panthera species followed by the PSC and the LSC, except for P. tigris SMF 15737 (Table
Figure
Concerning ontogeny, semicircular canal radii are proportionally larger in the neonate P. tigris than in the adult which resembles the negative allometric pattern as observed in P. leo (Fig.
The adult specimens of the studied Panthera species do not have a fossa subarcuata, but the infant specimens show its ontogenetic transformation (Figs
The osseous secondary crus commune is present in all Panthera species (Figs
As in P. leo, the ampullae in the other Panthera species are distinct, but not significantly inflated. They appear to be proportionally larger in the smaller species (i. e., P. pardus, P. onca, P. uncia, Figs
In all Panthera species, the aquaeductus vestibuli runs medially, leaving the vestibule anterior to the crus commune. Size and proportions of the proximal thin part and the distal fanning out part vary between species and individuals. Additionally, the angle of the fanning differs between individuals (Figs
Both, the fenestra vestibuli and the aperture of the cochlear fossula are oval in all Panthera specimens (Figs
The canaliculus cochleae of adult stages of P. pardus and P. tigris is slightly curved with thinning in the middle section (Figs
In comparison to the canaliculus cochleae of adult P. leo specimens the canaliculus cochleae of P. onca is proportionally shorter with a more consistent diameter and is not fanning out distally (Fig.
The cochlea is conical spiral in all non-lion Panthera specimens and the number of cochlear turns ranges from 3 to 3.5 (Figs
After correction for skull basal length, cochlear length is similar between specimens of the same species (Table
Panthera onca, P. pardus (SMF 15745, right bony labyrinth of SMF 16529), and P. tigris (SMF 15737) show a traceable secondary bony lamina, close to half a turn of the cochlea. In another P. tigris specimen (SMF 15722) the secondary bony lamina reaches over half a turn. No secondary bony lamina is visible in all other specimens (Table
The inner ear morphology of Neofelis resembles those observed in Panthera (Fig.
In absolute values, N. nebulosa has the smallest IEH and N. diardi the second smallest. Corrected for skull basal length, N. diardi has a proportionally larger bony labyrinth than N. nebulosa, representing the size proportion in IDAS 1.2 stage of P. leo (Fig.
Furthermore, the index IEH/BL of both Neofelis species is greater than in the adult Panthera specimens, with the highest value (0.090) in N. diardi (Table
In N. diardi the curvature of the ASC is oval, the LSC and PSC are almost round (Fig.
Overall, N. diardi has the largest inner ear in relation to body weight and skull basal length of all studied Pantherinae (Fig.
In the area of the fossa subarcuata in N. nebulosa a concavity similar to that in P. onca is present, albeit not as pronounced as in the latter. In contrast, N. diardi shows a shallow funnel-shaped depression in the area that we interpret as a remnant of the fossa subarcuata, which transitions into a possible petromastoid canal. However, the density of the surrounding bone as well as the adult age do not indicate any further closing of both cavities (Fig.
Like in the studied Panthera specimens, in anterior view, the lower limb of the PSC is on a lower level as the plane of the LSC but both Neofelis species lack an osseous secondary crus commune (Fig.
Just like in Panthera, the fenestra vestibuli and the aperture of the cochlear fossula are oval in both Neofelis species. However, in N. nebulosa, a small canal is branching off from the dorsal edge of the aperture of the cochlear fossula (Fig.
The canaliculus cochleae of N. diardi resembles mostly the pattern in P. onca whereas that of N. nebulosa is fanning out distally, but not as much as in adult P. leo or P. tigris (Fig.
The cochlea is conical spiral in all Neofelis specimens. The number of turns in N. diardi is 3, while in N. nebulosa, the number of turns is 3.25 (Fig.
Albeit, smaller in skull basal length, both Neofelis species have, in absolute values, a longer cochlea as P. uncia, but shorter than the other adult Panthera specimens (Table
The ASC has the largest radius of curvature in our sample, as it is typical for mammals (e.g.,
Overall, the bony labyrinth morphology is very similar between Pantherinae specimens, although species can be distinguished by certain features. The shape of the semicircular canals can be used to distinguish the genera Panthera and Neofelis. This is most prominent in the ASC, as it is round in almost all Panthera specimens and oval (N. diardi) or angular (N. nebulosa) in Nebulosa.
Within Panthera, P. leo and P. tigris can be distinguished by the length of the osseous secondary crus commune, which is relatively short in the latter. Additionally, in contrast to P. leo, the LSC of most P. tigris specimens protrudes the PSC. Panthera uncia is easily identifiable by the shape of the LSC and the relatively large semicircular canals. The latter indicate a good sense of balance, which is crucial for a mountain dwelling species for locomotion in rocky terrain (e.g.,
The presence or absence of the small branching canals of the canaliculus cochleae cannot be used for identifying the distinct species. It is tempting to assume that these delicate canals are only visible in the specimens whose scans have a higher resolution. However, the infant P. leo (SMF 95010) has been scanned with higher resolution than the other P. leo specimens and does not feature these small canals. In addition, the infant P. tigris (SMF 15722) does not feature them either, while one of the adult tigers (SMF 15737) does. Weather this is intraspecific and/or ontogenetic variation and/or caused by the quality of the scan needs to be elucidated in future studies.
As shown in former studies on different taxa, the larger species have a relatively smaller bony labyrinth than the smaller species, even though, the absolute size does not vary much in case of Pantherinae (e.g.,
Furthermore, the phylogenetic or ecological implications for the different relative sizes of the semicircular canals in Pantherinae species, should be recorded in larger sample sizes and complemented by additional morphometric measurements and statistically evaluated as described by
Among the Felidae studied by
Concerning the osseous secondary crus commune, our findings are similar to data from literature. Hyrtl (1945) describes an osseous secondary crus commune in P. leo, P. tigris and P. pardus. Of the four P. pardus specimens in our sample, two have an osseous secondary crus commune on both sides, one on the right side and one on neither side, which implicates some intraspecific variation. There is no consistency in the order Carnivora regarding presence or absence of an osseous secondary crus commune.
Among Felidae, Neofelis spp., Acinonyx jubatus and Caracal caracal lack an osseous secondary crus commune (
In conclusion, the osseous secondary crus commune grundplan pattern of Felidae and their subfamilies needs to be discussed based on larger samples, especially to elucidate possible convergent character states.
We could not detect a secondary bony lamina of the cochlea in all our specimens which may be due to several reasons: intraspecific variation, scanning resolution and/or quality or simply possible lack of the character (e.g., P. uncia). This problem could be solved with an increased sample for each species of Pantherinae. In specimens for which we could trace the secondary bony lamina, its relative length is comparable to Felis catus whose lamina extends ½ a turn (
It is generally assumed that the bony labyrinth of neonate placental mammals already shows the maturity of adult stages in terms of size and shape and thus, it is justified to incorporate juvenile specimens in morphological and morphometric studies (e.g.,
As observed in P. leo and P. tigris the absolute size of the bony labyrinth between neonate and adult stages is very similar and the elongation of the canaliculus cochleae is obviously correlated with the expanding petrosal bone (see Fig.
In addition, the shape of the cochlea of P. leo also shows some postnatal changes in that higher aspect ratios are mostly found in the neonate and juvenile P. leo specimens (IDAS 1.1–1.3). The same trend has been observed in Orycteropus afer, in which the cochlea of young individuals is more conical than that of adults (
The fossa subarcuata that houses the petrosal lobule of the cerebellar parafloculus is a plesiomorphic mammalian character (e.g.,
Our observations on the postnatal increasing closure of the fossa subarcuata in P. leo, P. tigris, P. pardus support previous descriptions of this process in Carnivora although unfortunately no details on the age of the respective pantherine species in
Over several generations, captive specimens can show differences in their morphology, because of different constraints compared to the natural environment and thus, relaxation of evolutionary constraints can also affect the vestibular organ including the bony labyrinth (
Our study revealed that in P. leo and P. tigris the higher numbers of cochlear turns are found in the captive specimens, with the exception of SMF 4643 (P. leo). Interestingly, P. pardus features the opposite pattern, in which the captive specimens have fewer cochlear turns than the ones of wild origin.
Felids studied by
In our sample the number of turns of the cochlea does not seem to correlate with the length of the cochlea in P. leo. P. pardus and P. tigris. However, the aspect ratio of the cochlea elucidates a certain pattern in P. leo: specimens with an aspect ratio of <0.6 have up to 3 cochlear turns, while specimens with >0.6 have more than 3 cochlear turns, albeit SMF 22104 (P. leo), which features 2.75 cochlear turns, has a higher aspect ratio as the P. leo specimens with 3 turns. Thus, captive P. leo specimens all have an aspect ratio >0.6, but it should be emphasized that our sample lacks adult lions from captive origin. In addition the presumably wild adult P. leo (SMF 4643) features 3.25 turns of the cochlea. The intraspecific differences in aspect ratio could be related to the tightness of coiling.
Based on this approach, in future studies the tightness of the cochlear coiling along the ontogenetic sequence from wild and captive Pantherinae should be systematically investigated with a much larger sample. Additional morphometric measurements, e.g., the laminar gap and cochlear volume, should be carried out in the future as well. This could help to elucidate the developmental or evolutionary drivers for different cochlear turn numbers and cochlear shape between wild and captive specimens.
The inner ear is a sensory organ, which is exposed to high evolutionary constraints (
We were able to show a negative allometry of the bony labyrinth with the skull basal length between larger and smaller Pantherinae species. In case of the genus Neofelis, the large size difference likely also has a functional component (
The size of our sample was not sufficient for a statistical analysis and proper discussion of intraspecific variation, albeit we presented certain patterns, which should be investigated further in the future. The same holds true for the comparison of bony labyrinth morphology of wild and captive animals.
This research has been supported by the Paul-Ungerer-Stiftung and Seiko Deutschland Branch of SEIKO Watch Europe B.V.
The authors thank Katrin Krohmann, Juliane Eberhardt (both SGN Frankfurt), Rachel A. Racicot (Vanderbilt University, Nashville, Tennessee), Franziska Fritzsche, Antonia Späth, and Franziska Wagner (all formerly SGN Frankfurt) for technical support. Special thanks go to Patrick Bak (Yxlon International GmbH, Hamburg) for providing the µCT scan of one specimen. Special thanks go to Guillaume Billet and two anonymous reviewers who helped to improve the manuscript.
Tables S1, S2
Data type: .xlsx
Explanation note: Table S1. µCT scan parameters of studied Pantherinae. For some specimens the resolution has been virtually increased (res 2). — Table S2. Raw measurements of the studied Pantherinae specimens. Abbrevations: ASC, anterior semicircular canal; BL, skull basal length; cco, canaliculus cochleae; co, cochlea; H, height; IEH, inner ear height; iH, inner height; iW, inner width; L, lenght; l, left; LSC, lateral semicircular canal; oH, outer height; oW, outer width; PSC, posterior semicircular canal r, right; W, width.
Data type: .pdf
Explanation note: S1 Virtual endocasts of the right bony labyrinth of Panthera leo. A–D SMF 22101; E–H SMF 22104; I–L SMF 1366, left side mirrored. All depicted individuals are adult. Abbreviations: aa, anterior ampulla; acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; av, aquaeductus vestibuli; bp, bony protuberance; cc, crus commune; cco, canaliculus cochleae; co, cochlea; fv, fenestra vestibuli; la, lateral ampulla; LSC, lateral semicircular canal; pa, posterior ampulla; PSC, posterior semicircular canal; sbl, secondary bony lamina; scc, secondary crus commune. Scale bar: 5 mm. — S2 Ontogenetic transformations of the radius of curvature in the bony labyrinth of Panthera leo, P. pardus and P. tigris. The values of species are averaged. A P. leo (n=4), B P. tigris (n=3), C P. pardus (n=2), Abbreviations: ASC, anterior semicircular canal; co-L, cochlear length; IEH, inner ear height; LSC, lateral semicircular canal; PSC, posterior semicircular canal; R, radius of curvature. — S3 Virtual endocasts of the right bony labyrinth of selected Panthera species. A–D Panthera pardus SMF 94342; E–H P. pardus SMF 95992, left side mirrored; I–L P. tigris SMF 7020. All depicted individuals are adult. Abbreviations: aa, anterior ampulla; acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; av, aquaeductus vestibuli; bp, bony protuberance; cc, crus commune; cco, canaliculus cochleae; co, cochlea; fv, fenestra vestibuli; la, lateral ampulla; LSC, lateral semicircular canal; pa, posterior ampulla; PSC, posterior semicircular canal. Scale bars: 5 mm. — S4 Dorsal view of right bony labyrinth endocasts of Panthera species illustrating differences in the secondary crus commune. A Panthera pardus (SMF 95992, left side mirrored), B P. onca (SMF 3067), C P. leo (SMF 4643), D P. uncia (SMF 5419, left side mirrored), E P. tigris (SMF 15737). Abbreviations: aa, anterior ampulla; acf, aperture of the cochlear fossula; ASC, anterior semicircular canal; bv, canal for blood vessels; cc, crus commune; cco, canaliculus cochleae; co, cochlea; de, dorsal extension of the aperture of the cochlear fossula; la, lateral ampulla; LSC, lateral semicircular canal; pa, posterior ampulla; PSC, posterior semicircular canal; scc, secondary crus commune. Scale bar: 5 mm. — S5 Size comparison of selected structures standardized by inner ear height in adult stages of all studied Pantherinae species. The linear equation, the coefficient of determination (R2) and the p-value are given in the respective graph. A cochlear length, B anterior semicircular canal radius of curvature, C lateral semicircular canal radius of curvature, D posterior semicircular canal radius of curvature. Abbreviations: ASC, anterior semicircular canal; co-L, cochlear length; IEH, inner ear height; LSC, lateral semicircular canal; PSC, posterior semicircular canal; R, radius of curvature.