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Cone beam tomography slices of ten periotic specimens at coronal (A) and transversal (B) cuts. C) Inia geoffrensis MCN-M32, D) Phocoena spinipinnis , E) Sotalia guianensis UFSC 1293, F) cf. Notocetus vanbenedeni MLP 76-IX-25, G) Platanistoidea indet. MPEF-PV 517, H) Delphinidae indet. MLP 76-IX-2-7, I) Delphinapterus leucas MLP1484, J) Physeteridae indet., K) Pontoporia blainvillei UFSC 1093, L) Sotalia fl uviatilis USNM 504316. Anatomical abbreviations: cd) cochlear duct, i.a.m.) internal acoustic meatus, pc) pars cochlearis, bp) body of periotic.
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... and estuarine taxa (e.g., Sotalia guianensis and Pontoporia, Fig. 2) exhibited a dorsal-ventrally globose and thick pars cochlearis. These external, morphological distinctions paralleled cone-beam tomography results (see S1), which showed that the larger cochlear duct sizes directly corresponded to larger external pars cochlearis sizes (see Fig. ...
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... volumetric tomography performed for nine specimens of different groups (see Table 2 and SI.1) provided access to the cochlear and general inner ear bony morphology in a non-destructive manner. The cochlear shape varied from a globose pars cochlearis and expanded cochlear duct to a more compressed cochlea with a similarly flattened pars cochlearis (Fig. 3). We noted that a bulbous profile of the pars cochlearis generally corresponded to a more dorsoventrally expanded cochlear duct, as observed in Sotalia guianensis. Equally, we noted that a slender pars cochlearis profile corresponded to a dorsoventrally compressed cochlear duct in Inia. The relationship between both features was more ...
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... fi ve qualitative groupings that are summarized in this section. These periotic groupings are described among three main anatomical portions (sensu Mead and Fordyce, 2009): the periotic processes (anterior and posterior); the pars cochlearis; and the inner morphology of the cochlea, which were clearly recognized, along with the cochlear duct, from cone- beam tomography imaging. The cochlear duct itself is located inside the pars cochlearis and it is positioned with its base at the ventral surface of the periotic and the apex at the dorsal surface of the periotic, connecting to the acoustic meatus (see Fig. 1 for periotic orientations). When possible, we discussed the inner cochlear duct morphology and orientation in connection to the external pars cochlearis morphology (sensu Mead and Fordyce, 2009:111 – 133, and references therein). In general, we were able to determine that external pars cochlearis morphology consistently discriminated riverine from marine taxa. For example, the riverine odontocetes studied herein (e.g., Inia , Platanista , and an iniid from the Ituzaingó Formation of Argentina [MACN 9231]) presented a consistently rounded, slender and high pars cochlearis morphology (Fig. 2). By comparison, marine and estuarine taxa (e.g., Sotalia guianensis and Pontoporia , Fig. 2) exhibited a dorsal-ventrally globose and thick pars cochlearis. These external, morphological distinctions paralleled cone-beam tomography results (see S1), which showed that the larger cochlear duct sizes directly corresponded to larger external pars cochlearis sizes (see Fig. 3). The fi rst morphological category is characterized by the periotics of Platanista . These periotics were larger, in absolute size, than every other odontocete periotic in this dataset. Notably, the pars cochlearis in Platanista was oval in shape, with a rounded medial surface and rectilineal anterior and posterior surfaces, which can be observed clearly in ventral and dorsal views (Fig. 2). The internal acoustic meatus was circular in shape, as seen medially, which is a condition only observed in other platanistoid periotics (e.g., the extinct Notocetus ). The anterior process in Platanista was elongate and robust, while the posterior process was reduced and narrow. The anterior process showed a noticeable anteromedial deviation. The lateral surface (in ventral view) was expanded, as in Inia geoffrensis and the Ituzaingó Formation iniid (MACN 9231; Fig. 2). The second morphological category is characterized by Inia , which presents an extreme reduction and anteroposteriorly orientation of the anterior and posterior processes. The pars cochlearis was rounded (in ventral view) and more slender (in medial view), with a marked, mediolaterally oriented sulcus. The internal acoustic meatus was circular as in Platanista , but it was not visible in the medial view. Compared with fossil Iniidae from our dataset, Inia only differed by an absence of the pars cochlearis sulcus and the oval shape of the internal acoustic meatus. MACN 9231 showed a widely exposed facial canal. The third morphological category, in contrast to Platanista and Inia , was an overall more slender morphology, characterized by Phocoena . The anterior process here was narrow and both processes were largely separated from the pars cochlearis, whose lateral surface was almost absent, in contrast to Platanista and iniids. The fourth category, characterized by Brachydelphis mazeasi , a fossil inioid, had a relatively small periotic, with a diminished anterior process comparable to Pontoporia and Pliopontos . Brachydelphis differed from these latter taxa by having a broad and rounded posterior process and a pars cochlearis triangular in shape with a clear, medially pointed apex. The anterior process was pointed in its anterior extremity and bent medially, with it being closer to the pars cochlearis. The lateral surface of the anterior process was also somewhat expanded, in contrast to phocoenid and pontoporiid morphology. The fi fth and last morphological category is represented by Delphinodon dividum , which is broadly similar to extant delphinids in periotic morphology. Here the anterior process is elongate and rectan- gular and de fl ected in an anteromedial direction. The pars cochlearis of D. dividum was oval in shape, similar to Platanista (see above, Fig. 2). The internal acoustic meatus was oval in shape, with the endocranial opening of the facial canal exposed dorsally. Its lateral surface was straight and slightly expanded, with the tympanic hiatus anterior-posteriorly elongated when compared to Brachydelphis , for example. The volumetric tomography performed for nine specimens of different groups (see Table 2 and SI.1) provided access to the cochlear and general inner ear bony morphology in a non-destructive manner. The cochlear shape varied from a globose pars cochlearis and expanded cochlear duct to a more compressed cochlea with a similarly fl attened pars cochlearis (Fig. 3). We noted that a bulbous pro fi le of the pars cochlearis generally corresponded to a more dorsoventrally expanded cochlear duct, as observed in Sotalia guianensis . Equally, we noted that a slender pars cochlearis pro fi le corresponded to a dorsoventrally compressed cochlear duct in Inia . The relationship between both features was more diffuse in Phocoena . These patterns are largely quanti fi ed in the results from our analyses, which showed that the main variables in the environmental morphometric analysis were pars cochlearis proportions, as detailed below (see 3.3, Figs. 4 – 6). Measurements from the internal portion of the cochlea, including the cochlear duct (i.e., the maximum diameter of the cochlear duct in the base and the maximum distance between the apical and basal portion of the cochlear duct; see Wartzok and Ketten, 1999), were strongly correlated with measurements taken at the external portion, the pars cochlearis. Specif- ically, the inner measurements corresponded to 59 – 74% of the external bony measurements, including different species from different clades and geologic ages (see Fig. 2). The pars cochlearis diameter or width was not recovered as an accu- rate representative of the maximum diameter of the cochlea. Nevertheless, the differences between thickness and the width of the cochlear duct, as observed in the external pars cochlearis morphometrics, hinted at a positive correlation, where Inia , the only riverine species examined with tomography, showed one of the smallest cochlear duct heights in the dataset (Fig. 7). On the other hand, the fully marine species were distributed at the opposite extreme of the scatterplot in Fig. 7, showing the largest cochlear duct heights. Estuarine or coastal species were located between these extremes, yet they appeared to group closer to marine taxa. The main features of the periotic morphology that varied across taxa and environment were the relative proportions among the pars cochlearis, and the anterior and posterior processes. Previous authors have noted that the relative orientation of the latter features, along with their associated foramina, were valuable for discriminating among odontocete taxa at the generic level (Kasuya, 1973; Barnes, 1985; de Muizon, 1988a). Here, we have determined that some of these characteristics also clustered into discrete groups based on known environmental preferences. For example, the pars cochlearis shape was strongly correlated with environment: cochlea from extant “ river dolphins ” was taller, more rounded, and slender than those from oceanic delphinoids (Fig. 4). Signi fi cant results were not recovered for genus-level taxonomic groups in our CVA results. Nevertheless, groupings at family- suprafamilial levels (Fig. 5) recovered some of the groups as signi fi cant, although the fi rst canonical axis only explained 64% of the variation, and both of the axes explained together less than 80% of the total variation. Notably, Delphinidae were signi fi cantly different from all groups (except Platanistidae), with Kentriodontidae, Pontoporiidae, Iniidae, and Phocoenidae following Delphinidae in de- scending order of signi fi cant differences in the pairwise comparisons. Regardless, the most important measurements in both canonical axes were the diameter of the malleus fossa (measurement 7) and the length of the anterior process (measurements 5 and 6), although the latter was less important than the former. In the test for correspondence of these morphometric features with their environmental origin, the CVA results showed signi fi cant differences between each pairwise comparison (see SI.3, Table SI.3.1) with each environmental group (i.e., morphometry versus fully marine, coastal/estuarine, and riverine; see S1). The fi rst canonical axis explained 87.5% of overall variance, where the most important measurements were: length of periotic (measurement 1); width and height of the pars cochlearis (measurements 2, 8, and 11); length of acoustic internal meatus (measurement 4); and width of the periotic (measurement 10). Thus, the majority of these measurements were related to the pars cochlearis shape. Variance for the second canonical axis was represented by the internal acoustic meatus (measurement 3) and the width of the pars cochlearis (measurement 8), but only 12.5% of the variance in the data was explained by this axis. Moreover, there was little differentiation among the groupings on this axis. For the size-independent dataset, CVA results were similar to the raw data, with the fi rst canonical axis explaining 87.1% of the data and dominated by the following measurements (Fig. SI.3.2): periotic length (measurement 1); malleus fossa size (measurement 7); pars cochlearis height (measurement 11); and anterior process length (measurement 5). Additionally, the most relevant measurement in this size-corrected analysis was the maximum thickness of the pars cochlearis (measurement 15), which ...
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... fi rst canonical axis alone. For the second canonical axis, only 12.9% of the variance was explained, with little difference among the possible groupings. For this latter axis, the important measurements were width of the fossa for the stapedial muscle (measurement 13), the maximum and minimum thicknesses of the pars cochlearis (measurements 15, 16), the epitympanic hiatus width (measurement 17), and the internal acoustic meatus depth (measurement 18), which combined accounted for approximately 56% of the variance along the second canonical axis. We also compared inner ear morphology, from tomography data, against environmental classi fi cations because previous authors have suggested that inner ear measurements are functionally relevant to hearing (Wever et al., 1971; Ketten, 1992; Wartzok and Ketten, 1999; Miller et al., 2006). The morphometric analyses of these measurements (Table 1) recovered the pars cochlearis external width, height, and thickness as signi fi cant variables. As expected, these linear dimensions essentially correlated with inner cochlear shape and length. More importantly, these analyses group speci fi c taxa into cochlear types proposed previously (Wever et al., 1971; Ketten and Wartzok, 1990; Ketten, 1992). In this sense, the paired comparisons (measurement versus measurement) revealed that the most signi fi cant differences between the environmental groups (p b 0.01) were thickness versus height and width of pars cochlearis (Fig. 6). These results are in agreement with the aforementioned functional scheme, where the more elongate and thinner pars cochlearis morphology re fl ected the cochlear duct morphologic types I and II (see Section 4.3 for further discussion). Our results also demonstrated that the shape of internal acoustic meatus was signi fi cantly correlated with environmental type: namely, its width (measurement 3) explained the variance of the coastal and estuarine group and its length (measurement 4) correlated with the riverine group. The signi fi cance of the internal acoustic meatus, however, was secondary to the aforementioned, primary measurements. We generated a priori environmental categorizations for fossil specimens by searching the source literature for associated sedimentologic and paleoecologic data (as detailed in Section 2, S1 and S2). Although these data inform only about the environment of fi nal deposition (thanatocoenosis), we view these data as reasonable approximations of the original source habitat (biocenosis) for these extinct taxa based on the general fi delity of extant death assemblages to their source com- munities (e.g., live-dead studies detailed by Pyenson, 2010; 2011). Using the periotic CVA scores, 94 out of 110 total fossil odontocetes were correctly assigned habitat classi fi cations consistent with their geological context. Nevertheless, the post hoc predictions of the CVA results can also work as tests for the likely original habitats of extinct odontocetes. The analyses conducted herein permit the categorization of fossil taxa to speci fi c environmental types. For example, Delphinodon dividum , a kentriodontid from the Miocene of the western Atlantic Ocean, was similar to Delphinapterus in having CVA classify it as a riverine taxon, dictated mostly by its slender pars cochlearis pro fi le. Another fossil taxon, Odobenocetops , an enigmatic walrus-convergent odontocete known from the Pliocene of Peru (de Muizon, 1993) was also an out- lier, with results spread across the total distribution of the coastal/ epicontinental/estuarine specimens. Such a difference could easily be interpreted as a consequence of its relatively large size, but the size-independent matrix showed that it nonetheless was located at the extremes of the scatterplot distribution. Other specimens misclassi fi ed (i.e., a priori classi fi cation differing from statistical predictions) were: Lophocetus pappus and Lophocetus calvertensis from the Calvert Fm.; Brachydelphis mazeasi from Pisco Fm. (given: coastal; predicted: fully marine); Phocoena phocoena (given: marine; predicted: riverine); and Kentriodon sp. from the Calvert Fm. (given: fully marine; predicted: coastal/estuarine). Finally, Platanista showed con fl icting results between its given (riverine) category and its predicted (fully marine) one. The jackknife results from the predicted categories added 10 more misclassi fi ed taxa: Inia geoffrensis ; Neophocaena phocaenoides ; three specimens referred to Pontoporiidae indet. (two as fully marine and one as riverine); and two additional L. pappus specimens. The volumetric tomography data (nine specimens of different groups) were slightly different from the overall patterns observed by Ketten (1992) and Wartzok and Ketten (1999). These authors stated that higher frequency hearing (type I) would be associated to more compressed cochleae, which have fewer turns and a greater expansion of the outer osseous spiral lamina along the length of the basilar membrane (Fig. 3, Table 2). This functional implication is possible in light of basilar membrane morphometrics (e.g., the width to thickness ratio) and the outer spiral lamina extension as acceptable proxies of stiffness of this membrane (von Bekesy, 1960; Wever et al., 1971; Ketten, 1984) at a given scale (for a review see Miller et al., 2006) permitting a relative de fi nition of echolocation types. These features allow the morphologic discrimination of the two main types of echolocation observed in living species. In riverine and coastal species, there is a low frequency cut off in the echolocation beam, which produces a narrow-banded click structure, while fully marine species present both, high and low peak frequency, producing a bimodal sound structure (e.g., T. truncatus and S. attenuata ; Table 2, Miller et al., 2006). This is slightly different from the scheme proposed by Wartzok and Ketten (1999) of cochlear types, where type I cochlea and echolocation high peak frequency (100 kHz) would be associated with a more broad, turned and contracted cochlea, that have the base to apex axis oriented rather ventromedially than dorsoventrally. Type II cochleae would have the base to apex axis oriented dorsoventrally, with a more expanded cochleae associated with broader echolocation ranges including a lower peak frequency (~ 40 to 70 kHz). When the acoustic parameters used for echolocation in living odontocetes are compared with morphology, taxonomy and environment (Table 2), it is notable that the acoustic proprieties sort mainly by emitted frequencies in two ways: fi rst, with a low-peak frequency, giving a bimodal structure to the echolocation beam observed in marine species (not measured here) as T. truncatus and S. attenuata and other delphinidans (see also Morisaka and Connor, 2007; Wartzok and Ketten, 1999); and, second, with riverine species emitting only a high peak frequency (Miller et al., 2006). To explain these two different patterns, Morisaka and Connor (2007) suggested that the narrow-band echolocation clicks (emission) pattern and its low frequency cut off was linked to the loss of whistle (emission) in Pontoporia , Cephalorhynchus and the Phocoenidae family. Nevertheless, here we only could con fi rm that there is a relationship between environment and the shape of the cochlear duct and pars cochlearis (i.e., part of the hearing system). In this sense, it is also plausible to suggest that the morphological differences (type I and type II, hearing) are functionally related to the low frequency cut off, where the frequency range is reduced to one (instead of two) narrow-band higher frequency beam (emission) in accordance with the possible loss of the cochlear portion responsible for hearing at “ lower ” frequencies. In any case, the emitted frequencies may be not very different than the actual acoustic sensitivity (hearing). For example, in Inia the auditory sensitivity is at a lower frequency than the one emitted, but only by a small amount (~10 kHz; see Table 2). The correspondence between odontocete cochlear morphology (both inner and external) and echolocation type was proposed in the literature 40 years ago, with some reinterpretation in subsequent, but singular studies (Wever et al., 1971; Ketten, 1992; Wartzok and Ketten, 1999; Miller et al., 2006). Our study is the fi rst to integrate a morphometric dataset (including extant and extinct taxa) within a robust statistical context. We found that the inner cochlear and the external pars cochlearis morphology were tightly correlated and we propose that these features can be used as ecomorphologic indicators of environmental preference, for both extant and extinct taxa. We nonetheless caution that the accuracy of these correlations depend on appro- priate and independent contexts (i.e., sedimentological data). The robust results showing the discrimination of riverine versus marine and coastal-estuarine classi fi cations for fossil and extant odontocetes strongly suggest the potential for periotic features to serve as valuable indicators of environmental preference, primarily based on the correspondence of these structures to the frequency range of hearing and the particular acoustic properties of water in these environments. Our study fi ts squarely in previous sets of observations that notes the external and osteological convergences among the so-called “ river dolphins ” (Simpson, 1945; Rice, 1998; Hamilton et al., 2001; Nikaido et al., 2001; Geisler et al., 2011). In parallel, there has also been indica- tion that functional aspects of “ river dolphin ” echolocation has con- verged on similar solutions for producing and receiving sound in an environment unlike the putative oceanic conditions of their ancestors. The freshwater systems inhabited by extant “ river dolphins ” differ in acoustic and optic properties from marine ones, including: water temperature, which alone can affect the propagation of echolocation signals (Wartzok and Ketten, ...
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... CT scanning with the cone beam method allowed us to scan an entire set of periotics oriented in the same plane ( fi xed to a wood plate with wax), thereby avoiding the effects of re fl ection (i.e., mirroring), and damage to the specimens. Lastly, this method produced a relative density spectrum for the specimens. The resultant DICOM images were analyzed and rendered in OsiriX (Rosset et al., 2004); we used the open polygon tool to collect all of the measurements. The measurements are described in Table 1 (see also Fig. 1). To test for environmental correlations, we pre-classi fi ed the data matrix with groupings based on the observed habitat environment, as follows: riverine; fully marine; and coastal-estuarine (including the categories of coastal, shallow and epicontinental sea with freshwater input; see S1 and S2). In the case of the fossil specimens, the environmental categories were de fi ned compiling locality, horizon, geologic unit, sedimentologic and paleoecologic data available for each specimen in the literature (e.g., Achurra, 2004; Achurra et al., 2009; Cione et al., 2005a, b; Visaggi and Godfrey, 2010; Ward and Andrews, 2008; Whitmore and Kaltenbach, 2008; see also S1 and S2). For the extant specimens, the distribution data of the species were compiled from literature (Reeves et al., 2002; Shirihai and Jarrett, 2009; see S1). Although data on the environmental context for fossil taxa may re fl ect a variety of taphonomic biases (Uhen and Pyenson, 2007), we assumed that the depositional environment for these specimens was effectively similar to their original habitat. To compare environmental signals of the dataset with phylogenetic history, we also grouped our data taxonomically by family and genus levels following Steeman et al. (2009) and Geisler et al. (2011; see Table S1). Although supra-familial relationships among extant cetaceans, especially among odontocetes, have not yet reached a consensus, we decided to use Steeman et al. (2009) and Geisler et al. (2011) as a proxy for phylogeny. We allotted our taxa among the following stem and crown groups (stem-Inioidea, Iniidae, Pontoporiidae, Delphinidae, Kentriodontidae, Phocoenidae, Platanistidae, stem-Platanistoidea, Odobenocetops + Delphinapterus ) and superfamily level (Platanistoidea, Inioidea, Delphinoidea). The measurements were analyzed in two different ways: fi rst as raw data; and then divided by the total width of the median portion of the periotic (Fig. 1, Table 1; measurement 10), to control for size disparity. We then conducted multivariate analysis of variance and canonical variate analysis (MANOVA and CVA, respectively) using PAST 2.11 (Hammer et al., 2001). We used the CVA biplot option in PAST to inter- pret the canonical axes as they scale CVA loadings by the pooled within- group covariance matrix (see SI.3 and SI.4). The main measurements in the multivariate analysis biplots were then analyzed in a paired comparison analysis, with a Kruskal – Wallis ranked test for signi fi cance, which assessed the differences among the selected measurements. We also compared pairs of variables that had the largest values in the CVA loadings (Fig. SI.3.2) and accounted for the most variance in canonical axes. This step allowed us to compare morphological differences between groups in a simpler way than allowed by the multivariate analyses. Our observations of periotics revealed fi ve qualitative groupings that are summarized in this section. These periotic groupings are described among three main anatomical portions (sensu Mead and Fordyce, 2009): the periotic processes (anterior and posterior); the pars cochlearis; and the inner morphology of the cochlea, which were clearly recognized, along with the cochlear duct, from cone- beam tomography imaging. The cochlear duct itself is located inside the pars cochlearis and it is positioned with its base at the ventral surface of the periotic and the apex at the dorsal surface of the periotic, connecting to the acoustic meatus (see Fig. 1 for periotic orientations). When possible, we discussed the inner cochlear duct morphology and orientation in connection to the external pars cochlearis morphology (sensu Mead and Fordyce, 2009:111 – 133, and references therein). In general, we were able to determine that external pars cochlearis morphology consistently discriminated riverine from marine taxa. For example, the riverine odontocetes studied herein (e.g., Inia , Platanista , and an iniid from the Ituzaingó Formation of Argentina [MACN 9231]) presented a consistently rounded, slender and high pars cochlearis morphology (Fig. 2). By comparison, marine and estuarine taxa (e.g., Sotalia guianensis and Pontoporia , Fig. 2) exhibited a dorsal-ventrally globose and thick pars cochlearis. These external, morphological distinctions paralleled cone-beam tomography results (see S1), which showed that the larger cochlear duct sizes directly corresponded to larger external pars cochlearis sizes (see Fig. 3). The fi rst morphological category is characterized by the periotics of Platanista . These periotics were larger, in absolute size, than every other odontocete periotic in this dataset. Notably, the pars cochlearis in Platanista was oval in shape, with a rounded medial surface and rectilineal anterior and posterior surfaces, which can be observed clearly in ventral and dorsal views (Fig. 2). The internal acoustic meatus was circular in shape, as seen medially, which is a condition only observed in other platanistoid periotics (e.g., the extinct Notocetus ). The anterior process in Platanista was elongate and robust, while the posterior process was reduced and narrow. The anterior process showed a noticeable anteromedial deviation. The lateral surface (in ventral view) was expanded, as in Inia geoffrensis and the Ituzaingó Formation iniid (MACN 9231; Fig. 2). The second morphological category is characterized by Inia , which presents an extreme reduction and anteroposteriorly orientation of the anterior and posterior processes. The pars cochlearis was rounded (in ventral view) and more slender (in medial view), with a marked, mediolaterally oriented sulcus. The internal acoustic meatus was circular as in Platanista , but it was not visible in the medial view. Compared with fossil Iniidae from our dataset, Inia only differed by an absence of the pars cochlearis sulcus and the oval shape of the internal acoustic meatus. MACN 9231 showed a widely exposed facial canal. The third morphological category, in contrast to Platanista and Inia , was an overall more slender morphology, characterized by Phocoena . The anterior process here was narrow and both processes were largely separated from the pars cochlearis, whose lateral surface was almost absent, in contrast to Platanista and iniids. The fourth category, characterized by Brachydelphis mazeasi , a fossil inioid, had a relatively small periotic, with a diminished anterior process comparable to Pontoporia and Pliopontos . Brachydelphis differed from these latter taxa by having a broad and rounded posterior process and a pars cochlearis triangular in shape with a clear, medially pointed apex. The anterior process was pointed in its anterior extremity and bent medially, with it being closer to the pars cochlearis. The lateral surface of the anterior process was also somewhat expanded, in contrast to phocoenid and pontoporiid morphology. The fi fth and last morphological category is represented by Delphinodon dividum , which is broadly similar to extant delphinids in periotic morphology. Here the anterior process is elongate and rectan- gular and de fl ected in an anteromedial direction. The pars cochlearis of D. dividum was oval in shape, similar to Platanista (see above, Fig. 2). The internal acoustic meatus was oval in shape, with the endocranial opening of the facial canal exposed dorsally. Its lateral surface was straight and slightly expanded, with the tympanic hiatus anterior-posteriorly elongated when compared to Brachydelphis , for example. The volumetric tomography performed for nine specimens of different groups (see Table 2 and SI.1) provided access to the cochlear and general inner ear bony morphology in a non-destructive manner. The cochlear shape varied from a globose pars cochlearis and expanded cochlear duct to a more compressed cochlea with a similarly fl attened pars cochlearis (Fig. 3). We noted that a bulbous pro fi le of the pars cochlearis generally corresponded to a more dorsoventrally expanded cochlear duct, as observed in Sotalia guianensis . Equally, we noted that a slender pars cochlearis pro fi le corresponded to a dorsoventrally compressed cochlear duct in Inia . The relationship between both features was more diffuse in Phocoena . These patterns are largely quanti fi ed in the results from our analyses, which showed that the main variables in the environmental morphometric analysis were pars cochlearis proportions, as detailed below (see 3.3, Figs. 4 – 6). Measurements from the internal portion of the cochlea, including the cochlear duct (i.e., the maximum diameter of the cochlear duct in the base and the maximum distance between the apical and basal portion of the cochlear duct; see Wartzok and Ketten, 1999), were strongly correlated with measurements taken at the external portion, the pars cochlearis. Specif- ically, the inner measurements corresponded to 59 – 74% of the external bony measurements, including different species from different clades and geologic ages (see Fig. 2). The pars cochlearis diameter or width was not recovered as an accu- rate representative of the maximum diameter of the cochlea. Nevertheless, the differences between thickness and the width of the cochlear duct, as observed in the external pars cochlearis morphometrics, hinted at a positive correlation, where Inia , the only riverine species examined with tomography, showed one of the smallest cochlear duct heights in the dataset (Fig. 7). On ...
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... This fact is supported by archaeocetes having a cochlear morphology and functional patterns resembling terrestrial relatives more than fully aquatic whales (Mourlam and Orliac 2017). The relationship between cochlear morphology and echolocation type was firstly proposed by Wever et al. (1971), and a further study revealed a link between the shape of the cochlear aqueduct, the pars cochlearis, and the environment (Gutstein et al. 2014b). For instance, river dolphins (i.e., Iniidae, Platanistidae, and Lipotidae) have a taller, more rounded, and slender pars cochlearis than oceanic delphinids, but no significant convergence on cochlea morphology was observed among these three families (Park et al. 2019). ...
... While Inia spp. possess a dorsoventrally compressed cochlear aqueduct, Sotalia guianensis, a marine dolphin, has a more bulbous pars cochlearis with an expanded cochlear duct (Gutstein et al. 2014b). However, there are no data regarding S. fluviatilis ear morphology for comparison with its sympatric Amazonian species. ...
The Amazonian basin is inhabited by four river dolphins species, three belonging to the Inia genus (I. geoffrensis, I. boliviensis and I. araguaiaensis) and Sotalia fluviatilis. Although sympatric, these species greatly differ in morphological characteristics mostly related to specific ecologies and use of space in the Amazon environment. Therefore, in this study, we aimed to review current knowledge of the morphological differences among Inia spp. and Sotalia fluviatilis, especially regarding the skeleton, myology, communication, and diet. Studies have shown that Inia spp. differ in skull size and measurement parameters among species and within the same species (subspecies), thus suggesting that these variations might have been environmentally driven. Regarding muscle arrangement, Inia spp. seem to have developed conspicuous features that have provided the genus with unique flipper movements compared to other dolphins, and Sotalia fluviatilis has a modified framework compared to marine dolphins. Finally, both species also differ in echolocation capabilities, which could be explained by morphological traits related to their hearing organs, which also relate to their ecological habits. We present the most important information gaps and aspects that should be further considered in the next morphological studies regarding these species. The presented data highlight species adaptations to their environment and how these changes might have led to niche differentiation among these sympatric species in the Amazon biome.
... echolocation and the environment) to TPC shape (e.g. Gutstein et al. 2014, Ary 2017, Esteves-Ponte et al. 2022. These studies rely on traditional geometric morphometric analyses, which limit a comprehensive assessment of shape variation of the TPC. ...
... 3D geometric morphometric and data measurement 3D geometric morphometrics allows for the quantification of size and shape through points called 'landmarks' and 'semilandmarks', which are defined by 3D Cartesian coordinates (Bookstein 1991, Zelditch et al. 2012, Gunz and Mitterocker 2013. This analysis was not only based on landmarks established in previous studies (Gutstein et al. 2014, Ary 2017) but also on the curved structures and the entire surface that compose the periotic bone. We measured 138 landmarks and semilandmarks on 95 periotic 3D models using VIEWBOX 4.0 software (www. ...
... To analyse the influence of ecological variables on periotic bone morphology, we define eight relevant variables to the ecology and hearing of odontocetes: diving ecology, prey size, habitat, feeding strategy, diet, environment, biosonar, and surface temperature (e.g. Gutstein et al. 2014, Galatius et al. 2019, Berta and Lanzetti 2020, Coombs et al. 2022, Viccari et al. 2022). ...
Hearing is essential for odontocete ecology, supporting navigation, hunting prey, communication, and mother-calf bonding. This study examines morphological variation in the periotic bone, focusing on its taxonomic value, its phylogenetic signal, and the influence of ecological factors on its evolution. Using photogrammetry and 3D geometric morphometrics, we analysed 95 periotic bones from 32 species across five families (Delphinidae, Pontoporiidae, Phocoenidae, Ziphiidae, and Physeteridae). The specimens were mainly sourced from three osteological collections in Argentina, covering a wide range of odontocete taxa. We assessed the association and differentiation between families based on periotic shape, estimated the phylogenetic signal, and evaluated the influence of ecological variables on shape variation. Our results revealed clear differences between odontocete families, with a shared periotic morphotype for ziphiids and physeterids and another distinct periotic morphotype grouping of Delphinidae, Pontoporiidae, and Phocoenidae. Phylogenetic analyses showed a strong phylogenetic signal in periotic morphology, while ecological factors such as diet, habitat, diving ecology, and biosonar types were identified as key influences on its evolution. Overall, periotic shape reflects both phylogenetic history and ecological adaptations, offering significant taxonomic value by enabling clear species differentiation.
... Anatomical terminology for the skull follows Mead and Fordyce (2009) unless indicated otherwise. Measurements follow Perrin (1975), Kasuya (1973) and Gutstein et al. (2014) for the skull, tympanic bulla and periotics respectively. To estimate the total body length of the specimens, we applied the equations from Pyenson and Spondberg (2011) based on the bizygomatic width for stem odontocetes: log(TL) ¼ 0.92 Â (log(BIZYG) -1.72) þ 2.68 where TL is total body length and BIZYG is bizygomatic width. ...
Odontocetes compose the most ecologically and taxonomically diverse clade of marine mammals. All modern odontocetes are homodont, but the early history of this group (Oligocene–Early Miocene) was dominated by a variety of bizarre forms with archaic features. Among these archaic odontocetes was Prosqualodon australis, a medium-sized, brevirostrine species from the Early Miocene of Patagonia (Argentina). It was originally described based on a partial skull; however, extensive fieldwork in Early Miocene outcrops in Patagonia has yielded several new specimens, including skulls with well-preserved basicranium, ear bones and postcranium. Based on this broad new sample we
provide an updated anatomical description and phylogenetic analysis of P. australis and discuss other referred specimens to the species. We also perform a taxonomic revision of the other two species of the genus, P. davidis (Australia) and ‘P.’ hamiltoni (New Zealand). Our studies confirmed the phylogenetic position of P. australis as an early-diverging (i.e. stem) odontocete and add diagnostic characters from the basicranium and periotic to the already known features that define P. australis: presence of a triangular-shaped parafalciform fossa, and a narrow and deep
furrow that originates from the periotic fossa and is anteromedially blind, periotic with a promontorial groove associated with an anteroventral tubercle and well-developed dorsal crest. Most anatomical differences between P. australis and the holotype of P. davidis are interpreted as ontogenetic variation, suggesting that P. davidis is a junior synonym of P. australis, making it the first circumpolar odontocete species from the Southern Hemisphere. Conversely, the anatomical and phylogenetic differences between P. australis and ‘P.’ hamiltoni suggest that these taxa are not
congeneric. The results of our work provide, for the first time, a thorough anatomical and systematic revision of the genus Prosqualodon, focusing on P. australis, based on one of the most outstanding fossil odontocete samples.
... This suggests that the different evolutionary constraints of each habitat have shaped the genetic diversity underlying the toothed whale sonar. Our comparative analysis across 37 odontocete species has revealed patterns of accelerated evolution within coastal and riverine lineages, supporting the hypothesis that these habitats generate specific selective pressures to sonar propagation and foraging, which are not found in the ocean [4,6,[42][43][44]. We also found accelerated evolution in deep-diving oceanic toothed whales, such as sperm whales, which are known to have sonar and behavioral adaptations to hunt in great depths [45]. ...
... Our results agree with previous findings that dolphins evolved specialized sonars and cochlear morphologies in each habitat [43,44,55]. Three types of environments, in particular, were associated with the strongest selective pressures: rivers, shallow coastal waters, and deep oceanic waters. ...
Background
Echolocation was a key development in toothed whale evolution, enabling their adaptation and diversification across various environments. Previous bioacoustic and morphological studies suggest that environmental pressures have influenced the evolution of echolocation in toothed whales. This hypothesis demands further investigation, especially regarding the molecular mechanisms involved in the adaptive radiation of toothed whales across multiple habitats. Here we show that the coding sequences of four hearing genes involved in echolocation (CDH23, prestin, TMC1, and CLDN14) have different signatures of molecular evolution among riverine, coastal, and oceanic dolphins, suggesting that the evolutionary constraints of these habitats shaped the underlying genetic diversity of the toothed whale sonar.
Results
Our comparative analysis across 37 odontocete species revealed patterns of accelerated evolution within coastal and riverine lineages, supporting the hypothesis that shallow habitats pose specific selective pressures to sonar propagation, which are not found in the deep ocean. All toothed whales with genes evolving under positive selection are shallow coastal species, including three species that have recently diverged from freshwater lineages (Cephalorhynchus commersonii, Sotalia guianensis, and Orcaella heinsohni - CDH23), and three species that operate specialized Narrow Band High Frequency (NBHF) Sonars (Phocoena sinus - prestin, Neophocaena phocaenoides - TMC1 and Cephalorhynchus commersonii - CDH23). For river dolphins and deep-diving toothed whales, we found signatures of positive selection and molecular convergence affecting specific sites on CDH23, TMC1, and prestin. Positively selected sites (PSS) were different in number, identity, and substitution rates (dN/dS) across riverine, coastal, and oceanic toothed whales.
Conclusion
Here we shed light on potential molecular mechanisms underlying the diversification of toothed whale echolocation. Our results suggest that toothed whale hearing genes changed under different selective pressures in coastal, riverine, and oceanic environments.
... The inner ear-in particular, the cochlea-is the region of the mammalian auditory pathway where sounds are converted into nerve signals. Cochlear anatomy reflects phylogeny, hearing abilities and habitat, and as such provides clues to the ecology of extinct or rare species (Ketten & Wartzok, 1990;Ketten, 2000;Ekdale, 2013;Gutstein et al., 2014;Ekdale & Racicot, 2015;Ekdale, 2016;Park et al., 2016Park et al., , 2017aRacicot et al., 2016;Mourlam & Orliac, 2017;Costeur et al., 2018;Ritsche et al., 2018;Racicot et al., 2018;Galatius et al., 2019;Viglino et al., 2021). Thus, for example, the cochleae of extant odontocetes seem to have evolved convergently, likely constrained by the acoustic environment of the deep ocean (Park et al., 2019). ...
Mysticetes (baleen whales) include the largest animals on Earth and are renowned for their songs and long-distance communication. Even so, the scope and origins of their hearing abilities remain poorly understood. Recent work on their sister clade, the toothed whales (odontocetes), has revealed notably convergent trends in the evolution of their inner ear. Here, we test whether the same applies to baleen whales via SURFACE, a phylogenetic method that fits Ornstein-Uhlenbeck models with stepwise Akaike Information Criterion to identify instances of convergent evolution. We identify a single convergent regime, including minke (Balaenoptera acutorostrata) and Bryde’s (Balaenoptera edeni) whales, which, however, is not statistically significant. We discuss potential reasons for the overall absence of convergence and suggest improvements for future work.
... Therefore, a more comprehensive study for 'kentriodontids,' especially their phylogenetic relationships, is necessary to refine the systematics of 'kentriodontids.' In addition to the phylogenetic relationships, previous studies on 'kentriodontids' suggested that their ecological niche was thought to be similar to the extant delphinoids [10,11]. They show high diversity through the late Early and early Late Miocene, and their high diversity during those periods is thought to be parallel to the present day Delphinoidea. ...
... Previous studies [12,13] have suggested that the origin and early diversification of the Delphinoidea were recognized in the Middle to Late Miocene. Although Delphinoidea have been considered to have the same ecological niches as environmental preferences [10] and feeding strategies [11] with most of the Kentriodontoidea, the absence of the Delphinoidea in the Middle Miocene might have been the result of niche partitioning based on our phylogenetic and paleobiogeographic analysis. Similar to some research [4], the results suggest that the Kentriodontoidea might have declined in their niche by the diversification of the Delphinoidea in the Late Miocene. ...
So–called ‘kentriodontids’ are extinct dolphin–like odontocetes known from the Early to Late Miocene worldwide. Although recent studies have proposed that they were monophyletic, their taxonomic relationships still remain controversial. Such a controversy exists partly because of the predominance of primitive morphologies in this taxon, but the fact is that quite a few ‘kentriodontids’ are known only from fragmentary skulls and/or isolated periotics. A new ‘kentriodontid’ Platysvercus ugonis gen. et sp. nov. is described based on a nearly complete skull from the upper Lower Miocene Sugota Formation, Akita Prefecture, northern Japan. Based on the phylogenetic analysis of P. ugonis described here, the monophyly of the ‘kentriodontids’ is confirmed, and it is recognized as the superfamily Kentriodontoidea. This new superfamily is subdivided into two families as new ranks: Kentriodontidae and Lophocetidae. Based on the paleobiogeographic analysis of the Kentriodontoidea, their common ancestor emerged in the North Pacific Ocean and spread over the Northern Hemisphere. Initial diversification of the Kentriodontidae in the North Pacific Ocean and the Lophocetidae in the North Atlantic Ocean was recognized as a vicariance event. The diversification and extinction of the Kentriodontoidea could have been synchronously influenced by climate events during the Middle Miocene.
... The functional consequences of this morphology for underwater hearing capabilities remain unknown. The periotic of Notocetus vanbenedeni also presents a moderately inflated squared pars cochlearis, a morphological characteristic present among extant river dolphins (Gutstein et al. 2014). Recent analyses of the inner ear morphology of Notocetus vanbenedeni showed that this species has a derived cochlear morphology amongst platanistoids, adapted for high-frequency hearing. ...
Platanistoidea remains one of the most evolutionarily intriguing lineages of toothed whales (Odontoceti). The clade comprises mostly extinct species from the late Oligocene–early Miocene onward and a single extant riverine genus (Platanista). There is an ongoing debate as to the membership of Platanistoidea and the causes of their near extinction. In Patagonia (Argentina), the most abundant platanistoid recorded in the lower Miocene Gaiman Formation is Notocetus vanbenedeni, first described by Moreno in 1892 based on two individuals. The goal of the present contribution is to conduct an updated anatomical, palaeobiological and phylogenetic analyses of Notocetus vanbenedeni and hence contribute to an understanding of the evolutionary history of the Platanistoidea. Our analyses, including at least 26 individuals (12 undescribed), show that Notocetus vanbenedeni is a valid platanistoid taxon, recovered as part of a new clade. Among its most outstanding features, this taxon has an elevated dorsal tubercular supraorbital crest formed mainly by the frontal, the precursor of the pneumatized crest of the extant Platanista. Notocetus vanbenedeni also shows initial stages of the plesiomorphic bony connection between the earbones and skull as in Platanista, although the functional implications for hearing remain elusive. The nasal sac system, pterygoid sinus system and morphology of the earbones suggest that this species was able to hear high-frequency sounds and echolocate underwater, similar to extant odontocetes. Thus, Notocetus vanbenedeni presents a mosaic of features that suggest an intermediate platanistoid morphotype. Anatomical differences and phylogenetic analyses suggest that Peruvian specimens could not be referred to this species. The feeding apparatus of Notocetus vanbenedeni makes it the only combination suction-feeder recorded in the early Miocene of Patagonia and among the smallest odontocetes. Finally, the abundant records of Notocetus vanbenedeni in an inner shelf environment with freshwater influence suggest a possible early preference for such protected habitats.
... An alternative approach may be necessary for a robust analysis of periotic shape. Gutstein et al. (2014) compared the morphology of the ear bones of marine and freshwater odontocetes. They compared 114 recent and fossil odontocetes using 18 external and three internal linear measurements. ...
... Few studies have attempted to identify odontocetes quantitatively based on periotic shape. Kasuya (1973) examined tympanic-periotic bones in an effort to further develop taxonomic keys, O'Leary (2010) described the petrosal for 35 artiodactylans (12 extinct and 23 extant) with molecular and morphological data, and Gutstein et al. (2014) used linear morphometry of recent and fossil periotics to provide a description (pars conclearis) of the odontocete periotics in relation to environment. Others have identified morphological characteristics of fossil (Bianucci 1996;Lambert et al. 2009;Li and Pasteris 2014) and archaeological (Fujita et al. 2002;Orliac et al. 2020) specimens. ...
Twenty-three species and four subspecies of odontocete belonging to five families (Delphinidae, Physeteridae, Kogiidae, Phocoenidae, and Ziphiidae) are distributed along the Pacific coast of northern Mexico. The morphological variability of these species has been studied extensively and a number of taxonomic studies have focused on cranial characteristics. The goal of this study was to describe the periotics of the odontocetes of the Pacific coast of northern Mexico and develop a taxonomic tool using descriptions of each species. We used a geometric morphometric analysis of 186 periotics housed in local and national osteological collections. Our results show the taxonomic value of periotics and a significant phylogenetic signal associated with this structure. Based on these results we present a descriptive catalog that can be used for identification purposes.
... The apex of the cochlea detects low frequency sound waves, whereas the base region detects high frequency sound waves, including ultrasonic sound waves 20 kHz and up (Ketten, 1997). Cochlear traits in cetaceans are greatly influenced by habitat (Costeur et al., 2018;Gutstein et al., 2014). Morphological differences can therefore indicate if the specimen inhabits estuaries or more pelagic zones, for example, because of differences in requirements for hearing in environments of different complexities. ...
... The habitat of Orcaella brevirostris is a highly complex ecological niche of euryhaline river environments and the echolocation abilities have been shown to be unusual (broad band low frequency, BBLF) compared to marine dolphins of similar size (Jensen et al., 2013). We initially hypothesized that the labyrinth morphology of Orcaella brevirostris would be similar to that of river dolphins because of the effect of environmental factors on hearing sensitivity (e.g., Costeur et al. 2018;Gutstein et al. 2014). Three species of extant river-inhabiting dolphins are represented in this PCA, Pontoporia blainvillei, Inia geoffrensis, and Lipotes vexillifer, which are distributed variably across the morphospace. ...
Bony labyrinth morphology varies across marine mammals and contains key information regarding hearing sensitivity and ecology. The hearing ranges of globicephaline (Delphinidae: Globicephalinae) or melon‐headed dolphins, known as “Blackfish,” have been extensively studied using acoustic technologies, but clade‐wide morphological analysis of the bony labyrinth is lacking. In this study, we investigate the variation in hearing‐relevant bony labyrinth morphology within globicephalines using μCT scans of isolated petrosals and digitally isolating the bony labyrinth of all species. Principal components analysis (PCA) of nine hearing‐relevant measurements of the cochlea alongside a broader sampling of terrestrial and aquatic artiodactyls shows Orcaella brevirostris and other globicephalines with higher levels of facial asymmetry and potentially more specialized echolocation abilities plotting near Monodon monoceros, Delphinapterus leucas, and Orcinus orca. The remaining globicephalines, which have more symmetrical skulls and other unique and acoustically relevant attributes, plotted towards the middle of the echolocating odontocete portion of the PCA. Our analysis thus reveals that inner ear morphology may correlate with both facial skull morphology and echolocation specializations, as these are intertwined. Furthermore, this study illustrates how morphological analyses, especially those centered on hearing, may provide critical conservation‐relevant information as direct access to audiograms becomes less tenable.
... Previous studies of extinct cetaceans show that the first underwater hearing morphologies were acquired in archaeocetes, for example, Remingtonocetidae and Basilosauridae (Nummela et al. 2004(Nummela et al. , 2007, and it was proposed that the ancestor of the Neoceti (Mysticeti + Odontoceti) had low-frequency (but likely not infrasonic) hearing (Ekdale and Racicot 2015;Ekdale 2016a,b;Mourlam and Orliac 2017;Park et al. 2017a). Odontocetes have a high-frequency hearing range, and their inner ear is characterized by a short cochlear canal, a stiff basilar membrane with extensive bony support, and a reduced vestibular system, among other characteristics (Oelschläger 1986;Ketten and Wartzok 1990;Ketten 2000;Gutstein et al. 2014;Churchill et al. 2016;Park et al. 2016;Costeur et al. 2018). ...
... They are a textbook example of convergent evolution (e.g., Geisler et al. 2011), with their long rostrum, small eyes, and unfused cervical vertebrae, among other anatomic characteristics (Page and Cooper 2017;Fordyce 2018;Rommel and Reynolds 2018). Riverine dolphins also share acoustic characteristics, with a highfrequency narrow-banded click structure; high echolocation peak energy (>100 kHz) sounds; and periotic characteristics like a rounded, slender, and high pars cochlearis (Ketten and Wartzok 1990;Gutstein et al. 2014). Generally, their cochleae have a nearly planar spiral in less than 2 full turns, longer outer bony lamina than most other odontocetes, and compressed cochlear ducts. ...
... Regarding the remaining odontocetes included in our sample, some brief comparisons are made here. In agreement with Park et al. (2019), but in contrast to Gutstein et al. (2014) and Costeur et al. (2018), we found that Platanista, Inia, Lipotes, and Pontoporia do not fall into the same position in the morphospace (Figs. 3, 4). Moreover, like Costeur et al. (2018), we found no morphological similarity between Lipotes and Inia, although our sample is limited in extant representatives and might therefore be masking such characteristics, though a single specimen should be indicative of morphology (Martins et al. 2020). ...
The inner ear of the two higher clades of modern cetaceans (Neoceti) is highly adapted for hearing infrasonic (mysticetes) or ultrasonic (odontocetes) frequencies. Within odontocetes, Platanistoidea comprises a single extant riverine representative, Platanista gangetica, and a diversity of mainly extinct marine species from the late Oligocene onward. Recent studies drawing on features including the disparate tympanoperiotic have not yet provided a consensus phylogenetic hypothesis for platanistoids. Further, cochlear morphology and evolutionary patterns have never been reported. Here, we describe for the first time the inner ear morphology of late Oligocene-early Miocene extinct marine platanistoids and their evolutionary patterns. We initially hypothesized that extinct marine platanistoids lacked a specialized inner ear like P. gangetica and thus, their morphology and inferred hearing abilities were more similar to those of pelagic odontocetes. Our results reveal there is no "typical" platanistoid cochlear type, as the group displays a disparate range of cochlear anatomies, but all are consistent with high-frequency hearing. Stem odontocete Prosqualodon australis and platanistoid Otekaikea huata present a tympanal recess in their cochlea, of yet uncertain function in the hearing mechanism in cetaceans. The more basal morphology of Aondelphis talen indicates it had lower high-frequency hearing than other platanistoids. Finally, Platanista has the most derived cochlear morphology, adding to evidence that it is an outlier within the group and consistent with a >9-Myr-long separation from its sister genus Zarhachis. The evolution of a singular sound production morphology within Platanistidae may have facilitated the survival of Platanista to the present day.
