Ontogenetic Variation in the Bony Labyrinth of Monodelphis domestica (Mammalia: Marsupialia) Following Ossification of the Inner Ear Cavities
Version of Record online: 20 AUG 2010
Copyright © 2010 Wiley-Liss, Inc.
The Anatomical Record
Volume 293, Issue 11, pages 1896–1912, November 2010
How to Cite
Ekdale, E. G. (2010), Ontogenetic Variation in the Bony Labyrinth of Monodelphis domestica (Mammalia: Marsupialia) Following Ossification of the Inner Ear Cavities. Anat Rec, 293: 1896–1912. doi: 10.1002/ar.21234
- Issue online: 29 OCT 2010
- Version of Record online: 20 AUG 2010
- Manuscript Accepted: 3 JUN 2010
- Manuscript Revised: 7 MAY 2010
- Manuscript Received: 11 FEB 2010
- National Science Foundation. Grant Number: EAR-03457
- bony labyrinth;
- inner ear;
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
Ontogeny, or the development of an individual from conception to death, is a major source of variation in vertebrate morphology. All anatomical systems are affected by ontogeny, and knowledge of the ontogenetic history of these systems is important to understand when formulating biological interpretations of evolutionary history and physiology. The present study is focused on how variation affects the bony labyrinth across a growth series of an extant mammal after ossification of the inner ear chambers. Digital endocasts of the bony labyrinth were constructed using CT data across an ontogenetic sequence of Monodelphis domestica, an important experimental animal. Various aspects of the labyrinth were measured, including angles between the semicircular canals, number of turns of the cochlea, volumes of inner ear constituents, as well as linear dimensions of semicircular canals. There is a strong correlation between skull length and age, but from 27 days after birth onward, there is no correlation with age among most of the inner ear measurements. Exceptions are the height of the arc of the lateral semicircular canal, the angular deviation of the lateral canal from planarity, the length of the slender portion of the posterior semicircular canal, and the length of the canaliculus cochleae. Adult dimensions of several of the inner ear structures, such as the arcs of the semicircular canals, are achieved before the inner ear is functional, and the non-ontogenetic variation in the bony labyrinth serves as an important source for behavioral, physiological, and possibly phylogenetic information. Anat Rec, 2010. © 2010 Wiley-Liss, Inc.
Variation is a phenomenon that affects all morphological systems. Phenotypic variation is the result of many factors, including phylogenetic history, gender, geography, and ontogeny. Ontogeny, or the development of an individual from conception to death, is a major source of variation that has garnered much attention in scientific literature. Ontogenetic variation is a special complication for systematists, particularly paleontologists, when only one specimen or a small sample of specimens of a taxon is known, which can lead to vexing systematic problems (Brinkman, 1988; Tykoski, 2005; Wiens et al., 2005). For example, two specimens that differ slightly in morphology might represent two separate taxa, or they might represent different ontogenetic stages of a single species, or the variation might indicate any of a series of other possibilities (see Bever, 2006). Because of this, the effect of ontogenetic transformations on anatomy has significant implications for physiological and evolutionary studies.
All morphological systems are affected by ontogenetic variation at some level. The fully formed bony labyrinth of the inner ear, as preserved within the internal cavities of the petrosal bone of mammals, ossifies and matures early in development, and the labyrinth changes little in size, if at all, in humans (Jeffery and Spoor, 2004). Given the precocial development of the inner ear in chickens, Knowlton (1967) hypothesized that “closure in a rigid capsule would inhibit morphological changes in the membranous labyrinth” (p. 184), and the results from subsequent studies in the ear regions of mammals support the hypothesis (Hoyte, 1961; Jeffrey and Spoor, 2004). This is not to say that the mammalian bony labyrinth does not exhibit variation throughout ontogeny. The auditory and vestibular systems undergo profound and pronounced ontogenetic transformations, even postnatally (Curthoys, 1982; Curthoys et al., 1982; Clark and Smith, 1993), but the labyrinth quickly achieves mature morphologies that appear to remain stable through the remainder of the life of an individual once the walls of the inner ear chambers have ossified (Hoyte, 1961; Knowlton, 1967; Curthoys et al., 1982; Jeffrey and Spoor, 2004; Sánchez-Villagra and Schmelzle, 2007; however, see Curthoys, 1982; Curthoys et al., 1982). In contrast, the majority of other systems, such as the long bones of the vertebrate limb, experience a more prolonged ontogeny relative to the inner ear. Given the rapid maturation of the mammalian ear region, as well as the prevalence of petrosal bones in the fossil record (the petrosal is among the densest elements in the body), the otic region of mammals is of special importance to vertebrate paleontologists and evolutionary biologists alike (e.g., Archibald, 1979; Quiroga, 1979; Miao, 1988; Spoor et al., 1994, 1996, 2002; Meng and Fox, 1995; Meng and Wyss, 1995; Hublin et al., 1996; Rougier et al., 1996, 1998, 2009; Wible et al., 2001; Ekdale et al., 2004; Ruf et al., 2009).
If the fully ossified bony labyrinth does not change throughout postnatal ontogeny, then the maturity of a specimen would not need to be known to make biological interpretations of behavior or phylogeny using the ossified inner ear. In fact, the morphology of the bony labyrinth has been used by researchers to investigate bipedalism in fossil hominids (Spoor et al., 1994, 1996; however, see Fitzpatrick et al., 2006), evolutionary relationships among early humans (Hublin et al., 1996), aquatic adaptations in cetaceans (Spoor et al., 2002; Kandel and Hullar, 2010), and behaviors in extinct reptiles (Witmer et al., 2003), including dinosaurs and birds (Rogers, 1998, 1999; Alonso et al., 2004), where the relative maturity of individuals was not ascertained.
Historically, access to the mammalian inner ear cavities, which are enveloped completely in bone, was granted through serial sectioning or dissolution of bone (Gray, 1907, 1908; West, 1985; Novacek, 1986; Luo and Marsh, 1996). More recently, the advent of high-resolution X-ray computed tomography (CT) has allowed observation of the internal cranial structures and description of the cranial osteology of vertebrate taxa in a non-destructive manner (Rowe et al., 1995, 1997; Spoor and Zonneveld, 1995; Maisano et al., 2002; Tykoski et al., 2002; Bever et al., 2005; Hullar and Williams, 2006). Because CT is a common method used to image the inner ear of mammals (e.g., Spoor and Zonneveld, 1995; Isono et al., 1997; Parlier-Cuau et al., 1998; Van Spaendonck et al., 2000; Della Santina et al., 2005; Jäger et al., 2005; Probst and Kneissl, 2006; Kirk and Gosselin-Ildari, 2009; Ruf et al., 2009), the technology was used here to investigate morphological changes following the completion of ossification of the bony labyrinth. Monodelphis domestica (Marsupilaia, Didelphidae), which is a species of mammal that is important for experimental biomedical research (Fadem et al., 1982; Macrini, 2004), was used as a model organism for this investigation, and the results of the current study demonstrate that most dimensions of the bony labyrinth are not strongly correlated with the ontogenetic age of an individual, once the walls of the bony labyrinth have ossified.
MATERIALS AND METHODS
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
Monodelphis domestica as a Model Organism
M. domestica was used as a model to explore postnatal changes within the inner ear of mammals, primarily because the species commonly is used in clinical studies (e.g., Eugenín and Nicholls, 1997; Hubbard et al., 1997; Kusewitt et al., 1999; Wang et al., 2003, 2009; Samollow et al., 2004; Halpern et al., 2005; Holmes et al., 2008), and knowledge of the inner ear of any species benefits future studies of the auditory and vestibular systems of mammals. Furthermore, M. domestica was the first marsupial, and only one of a handful of mammals, to have its genome sequenced (Mikkelsen et al., 2007). The results of previous studies that focused on the ear region of M. domestica (e.g., Reimer, 1996) have been used to illustrate that the timing of onset of hearing, changes in frequency sensitivities, and changes in thresholds and brainstem auditory evoked potential waveforms within M. domestica are comparable to those which have been reported for placental mammals. In particular, the timings of the onset of hearing and attainment of adult hearing abilities of didelphid marsupials fall in the range of placental mammals (Reimer, 1996: Fig. 9).
The timing of the onset of hearing and achievement of adult hearing capabilities in M. domestica follow a similar pattern to that determined for placental mammals of similar size (specifically Mus musculus; Reimer, 1996), allowing M. domestica to be used as a generalized model for physiological investigations of the inner ear of therian mammals (Reimer, 1996). The morphology of the membranous labyrinth of D. virginiana (Larsell et al., 1935) develops in a similar fashion to that of Mus musculus (Morsli et al., 1998), further suggesting that the ontogenetic pattern of the inner ear of didelphids (to which both Monodelphis and Didelphis belong) also may afford insights into the developmental morphology of placentals.
Furthermore, the structure of the inner ear of M. domestica can form an important base for evolutionary studies of the mammalian ear region. Didelphids occupy basal positions on the phylogeny of marsupials (Springer et al., 1998; Bininda-Emonds et al., 2007), and opossums are thought to retain many ancestral therian morphologies (see Gaudin and Biewener, 1992; Nilsson et al., 2003; Beck et al., 2008) and auditory functions (Frost and Masterton, 1994; Faulstich et al., 1996). Comparisons of the bony labyrinths among mammals suggest that the otic morphology of early marsupials, including didelphids, is unspecialized and largely plesiomorphic (Meng and Fox, 1995; Ekdale, 2009).
Specimens and CT Scanning
Eleven whole skulls or heads of M. domestica representing different ages (absolute numbers of postnatal days) were scanned at The University of Texas High-Resolution X-ray CT facility (UTCT). All specimens were born and raised in captivity under controlled conditions at the Southwest Foundation for Biomedical Research in San Antonio, TX, where exact numbers of postnatal days were recorded. Once CT scanned, the specimens were accessioned into the Vertebrate Paleontology Laboratory of the Texas Natural Science Center (Austin, TX) recent mammal collection (TMM M). The specimens used for this study range in age from 27 to 465 days after birth. Day 27 was chosen as the earliest age, because the walls of the bony labyrinth themselves likely are to be fully ossified by that time (see Clark and Smith, 1993).
The specimens used are TMM M 7595 (Day 27, macerated skull), 8261 (Day 27, ethanol preservation), 8265 (Day 27, frozen head), 7536 (Day 48, macerated skull), 8266 (Day 56, frozen specimen), 7539 (Day 57, macerated skull), 7542 (Day 75, macerated skull), 8267 (Day 76, frozen head), 7545 (Day 90, macerated skull), 8268 (Day 90, frozen head), and 8273 (Day 465, frozen head). One additional individual (TMM M 7599, macerated skull), a fully mature retired breeder from the colony, was used in this study, although the exact age of the individual is unknown. That specimen (TMM M 7599) was not used to ascertain age-related changes, but rather it was used for morphological comparisons with the rest of the specimens in the sample. Additional information about the specimens used in this study was reported by Macrini et al. (2007), and scan data for many of the specimens are publicly available at the website entitled ‘Digital Morphology: a National Science Foundation Library at the University of Texas at Austin’ (www.digimorph.org). Table 1 includes scanning parameters used for each specimen as well as a list of specific URLs for which scan data of the specimens are available.
The inner ear cavities were digitally segmented into constituent parts (cochlea; vestibule; anterior, lateral, and posterior semicircular canals; anterior, lateral, and posterior ampullae; common crus) by isolating voxels on individual CT slices that define the anatomical structure of interest. These segmented data can be rendered as a three-dimensional digital endocast (in-filling) of the segmented volume, which provides a detailed model of inner ear structures. Segmentation, visualization, and measurement of digital endocasts was performed in the computer programs VG Studio Max 1.2© (Volume Graphics, 2004) and Amira 3.1© (Mercury Computer Systems, 2003). Anatomical terminology follows Evans (1993) and Spoor and Zonneveld (1995).
Numerous angular and linear measurements, as well as indices describing various aspects of the digital endocasts, were made in Amira software, and volumetric measurements were made in both VG Studio Max and Amira. Measurement methods and indices calculated largely follow those used by Spoor and Zonneveld (1995, 1998), and Jeffery and Spoor (2004), many of which were used previously to formulate interpretations of mammalian systematics and the physiology of the inner ear. A detailed explanation of each measurement is provided in the following section.
Definitions and Exploration of Measurements
Most of the angles considered in this study are thought to be important to inner ear physiology, such as planar relationships between semicircular canals (Calabrese and Hullar, 2006), as well as the evolutionary relationships of mammals, such as coiling of the cochlea (Graybeal et al., 1989; Rougier et al., 1998; Ekdale et al., 2004).
The degree of coiling completed by the cochlea is calculated to investigate if the number of cochlear turns increases as the bony labyrinth matures after the completion of ossification. The coiling of the cochlea is often used to separate therian mammals from non-therian mammals, including monotremes and non-mammalian synapsids (Pritchard, 1881; Graybeal et al., 1989), and cochlear coiling, in conjunction with the length of the cochlear canal, is related to auditory function (West, 1985). Although the length and number of turns completed by the cochlea are common measurements, the hearing abilities of mammals are also thought to be related to basilar membrane width (Wever et al., 1971; Fleischer, 1976; Ketten and Wartzok, 1990), which can be estimated by the gap between the primary and secondary bony laminae. Other factors include the “stiffness” of the membrane (Echteler et al., 1994), the volume of the cochlea (Kirk and Gosselin-Ildari, 2009), and the shape of the cochlear spiral (Gosselin-Ildari, 2006; Manoussaki et al., 2006, 2008). Further correlations with hearing capabilities exist in the middle (Nummela, 1995; Overstreet and Ruggero, 2002; Ruggero and Temchin, 2002; Nummela et al., 2007; Ravicz et al., 2008) and outer ears (Ruggero and Temchin, 2002), and it is clear that the auditory and vestibular responses are complex functions.
To measure the number of turns of the coil, the cochlea is viewed from above, perpendicular to the axis of rotation. A line is drawn from the proximal termination of the primary and secondary bony laminae at the base of the cochlea (following Geisler and Luo, 1996) to the center of the axis of rotation. Each time that the cochlea crosses this line is counted as one half turn (180°). An additional value is added to this—an angle measured from the line drawn through the axis of rotation to the apex of the cochlear canal—to determine the total number of degrees completed by the cochlea.
The deviations of semicircular canals away from the orthogonal planes of the skull are calculated and reported in several physiological studies (e.g., Calabrese and Hullar, 2006; Hullar and Williams, 2006). The orientation of canals might signify that a vertebrate is more sensitive to certain movements of the head, such as pitch or roll (Hullar and Williams, 2006). Orthogonal planes in the published studies are defined by landmarks across a complete skull, so the orthogonality of the planes of canals cannot be determined for isolated petrosals (which often is the case with fossils). Nonetheless, the angles between the planes of the canals are measured here. If the angles between the canals change across post-ossification ontogeny, then the orientation of the canals with respect to the orthogonal planes of the skull also changes.
Orientations of the canals are measured as the angle between the planes of two canals, when both planes are perpendicular to the field of view (Fig. 1a–c). Three-dimensional planes are rendered in Amira along with the segmented volumes, and the planes appear as straight lines when viewed perpendicularly. The plane of a canal is fit to points at the center of the lumen at the midpoint of the arc, as well as the aperture of the canal into the ampulla at one end and vestibule at the other, using the “fit to points” option within the ObliqueSlice module in the Amira software. The “fit to points” option defines the plane based on three predetermined points placed at the center of the lumen, which was determined graphically.
The plane of the lateral semicircular canal is used to measure the angle between the canal and the cochlea. It is often assumed that mammals hold their heads so that the lateral semicircular canal is parallel to Earth horizontal (de Beer, 1947), but such is not always the case (see Hullar, 2006, for a review). Furthermore, the plane of the cochlea rotates anteriorly and superiorly with respect to the lateral semicircular canal in some primates (Delattre, 1952; Sercer, 1958; Daniel et al., 1982). The angle is measured in the same manner as the orientations of the three canals, where the plane of the cochlea intersects three points equally spaced through the basal turn of the cochlear canal (Fig. 1d).
Measurement of the deviation from planarity of a canal was made following modified protocols outlined by Calabrese and Hullar (2006) and Hullar and Williams (2006). The dimension is calculated by determining the maximum linear deviation achieved by the center of the lumen of the canal when the plane of the canal is oriented parallel to the horizon (Fig. 1e). Partial angles of deviation are determined trigonometrically using the linear deviations and the arc radius of curvature of the semicircular canal (described below with other linear measurements). The total deviation from planarity, reported here, is the sum of the two partial deviations.
The measurements made on digital endocasts are reported in millimeters, and they include total length of the labyrinth, radius of the arcs of the semicircular canals, diameters of the canal lumen, and lengths of the semicircular and cochlear canals, the canaliculus cochleae (for the perilymphatic duct), and the aquaeductus vestibuli (for the endolymphatic duct).
The total length of the bony labyrinth is a linear measure of size of the entire series of inner ear cavities (following Jeffery and Spoor, 2004). The length is measured as the greatest distance from the posterior-most point at the center of the lumen of the posterior semicircular canal to the center of the lumen of the outer bend of the basal turn of the cochlea.
Linear measurements of the size of the cochlear spiral, which may relate to auditory sensitivity, follow the method proposed by Gosselin-Ildari (2006). The width of the cochlea is measured as the greatest distance from the ventral edge of the fenestra cochleae to the outer wall of the outer curve of the basal turn of the cochlea (Fig. 2). The height of the cochlea is measured from the top of the spiral to the level of the dorsal edge of the fenestra cochleae, perpendicular to the width and parallel to the plane of the basal turn of the cochlea.
The radius of curvature of the arc of the semicircular canals (“R” of Jones and Spells, 1963) is correlated to both sensitivity of the canal, as well as agility of the animal. For animals of similar body size, larger canals are more sensitive to rotational movements of the head (Curthoys, 1982; Spoor et al., 2002; Hullar and Williams, 2006; Yang and Hullar, 2007; Lasker et al., 2008) and are indicative of a more maneuverable and agile animal (Gray, 1907; Turkewitsch, 1934; Spoor et al., 2002, 2007; Sipla, 2007; Cox and Jeffrey, 2010). The arc radius of a canal is half the average of the height and width of the arc. The height of the anterior semicircular canal is measured as the greatest distance from the wall of the vestibule to the center of the lumen of the canal, perpendicular to the plane of the lateral canal. The height of the posterior semicircular canal is measured parallel to the plane of the lateral canal from the center of the lumen of the common crus to the center of the lumen of the posterior limb of the canal. The height of the lateral canal is measured as the greatest distance from the wall of the vestibule to the center of the lumen of the canal. The widths for all of the canals are perpendicular to the respective heights, and measured from the center of the lumen of opposing limbs.
Dynamic responses of the semicircular canals are also dependent on the radius of the membranous semicircular duct within the bony canal (Jones and Spells, 1963; Peterka and Tomko, 1984; Ramprashad et al., 1984; Muller, 1999; Yang and Hullar, 2007; also see review by Hullar, 2006), or a combination of duct radius and arc radius of curvature (ten Kate et al., 1970; Oman et al., 1987). There is not a 1:1 size correlation between the bony and membranous labyrinths (Igarashi, 1967; Curthoys et al., 1977a, b), so the radius of the membranous duct cannot be determined in the absence of soft tissues (such is the case with fossils). The diameters of the bony canals are common measurements taken, and diameters for M. domestica are reported here, but they should not be used as proxies for the diameters of the membranous ducts.
The lengths of the slender (unampullated) portion of the semicircular canals relate to sensitivity of rotations by the head (Oman et al., 1987; Muller, 1994; Rabbitt et al., 2004) and potentially aquatic behaviors (Boyer and Georgi, 2007). The canal lengths were measured using the SplineProbe tool in the Amira software, wherein anchor points were placed at varying intervals at the center of the lumen of the canal. The length of the cochlear canal was measured in the same manner, with the starting point at the proximal terminations of the primary and secondary laminae.
Planar boundaries were maintained as much as possible between cavities and the separation between the cochlea and vestibule was made at the medial border of the fenestra vestibuli. The entirety of the fenestra itself was included within the vestibule. The canaliculus cochleae and aquaeductus vestibuli were included (not segmented separately) in the volumes of the cochlea and vestibule, respectively, because they are continuous with those compartments of the bony labyrinth. The slender portions of the semicircular canals were segmented separate from their respective ampullae (as well as the common crus between the anterior and posterior canals). The volume of fluid within the slender portion of the membranous semicircular ducts is related to the flow of endolymph within the duct, which in turn is related to the sensitivity of the duct to rotational movements (Ramprashad et al., 1984; Oman et al., 1987; Yamauchi et al., 2001; Rabbit et al., 2004).
Indices and ratios
Several indices and ratios were calculated from the linear measurements described above. Partial volumes of specific segments were calculated by dividing the volume of the segment (e.g., cochlea) by the total volume of the bony labyrinth.
The majority of the remaining indices describe the aspect ratios of the arcs of the semicircular canals (which might signify agility in locomotion; see Hullar, 2006) and the cochlea, which is related to auditory capabilities (Gosselin-Ildari, 2006; Kirk and Gosselin-Ildari, 2009). The aspect ratios are calculated as respective height over width.
The stapedial ratio is a value that often is used to distinguish marsupials from placentals in systematic studies. Segall (1970) defined the ratio as the greatest height versus width of the footplate of the stapes, and he concluded that marsupials tended towards a more circular footplate, and that placentals tended towards a more elliptical footplate (the fenestra vestibuli is often used as a proxy in absence of a stapes). Subsequently, the ratio has been used in phylogenetic systematic analyses (Rougier et al., 1998; Archibald et al., 2001; Wible et al., 2007) and the subcircular shape has been argued to be plesiomorphic for mammals (Segall, 1970; Rougier et al., 1998; Archibald et al., 2001).
To identify which measurements are correlated with post-ossification age, each measurement was regressed upon number of days and coefficients of correlation (r) were calculated for each comparison (Tables 2–6). At an a priori significance level of 5% (P = 0.05) based on the current sample size (N = 11), any coefficient of correlation 0.60 or above is considered significant (using a two-tailed probability model, which is most common in statistical analyses; Hammer and Harper, 2006). However, a significant correlation might not be strong (that is, a relationship may exist, but the influence of age on a particular measurement might be low), so coefficients of determination (r2) were calculated also to determine the strength of any recovered correlation. The coefficient of determination reports the percentage of variation in variable Y that can be explained by X (e.g., length of cochlear canal versus number of days). For example, if r2 = 0.49 (r = 0.70), then X explains just under half of the variation in Y. If over half of the variation in a measurement can be explained by ontogenetic age among the sample studied here, that correlation could be considered to be strong. Thus, only correlations with coefficients of correlation above 0.70 are considered strong in this study.
|Specimen (# Days)||Canal plane angles||Angular deviation||Cochlea|
|TMM M-7597 (27)||88.5||88.0||86.5||4.60||5.30||8.30||33.7||682||1.9|
|TMM M-8261 (27)||77.9||88.0||91.9||6.90||0.00||6.00||37.9||606||1.7|
|TMM M-8265 (27)||84.4||103||95.5||15.2||2.50||6.80||34.3||604||1.7|
|TMM M-7536 (48)||88.9||89.1||80.0||25.1||3.00||8.20||62.5||658||1.8|
|TMM M-8266 (56)||87.1||100||86.6||12.1||7.00||3.80||47.9||665||1.9|
|TMM M-7539 (57)||80.9||90.0||83.9||0.00||0.00||7.80||55.9||671||1.9|
|TMM M-7542 (75)||87.6||95.9||98.7||20.1||3.80||8.70||57.7||658||1.8|
|TMM M-8267 (76)||88.9||90.1||85.9||10.9||6.10||11.8||30.2||621||1.7|
|TMM M-7545 (90)||91.6||100||91.4||14.5||9.20||5.50||52.9||685||1.9|
|TMM M-8268 (90)||96.2||102||91.0||17.3||5.80||3.20||23.0||638||1.8|
|TMM M-8273 (465)||73.7||83.0||87.0||15.3||12.2||3.80||65.6||650||1.8|
|Specimen (# Days)||Anterior semicircular canal||Lateral semicircular canal||Posterior semicircular canal|
|Specimen (# Days)||Cochlea||Coch. Can.||Aq. Vest.||Bony Lab.||Skull|
|Specimen (# Days)||Cochlea||Semicircular canals||Ampullae||Com. Crus||Vestibule||Total|
|Specimen (# Days)||Volume percentages||Aspect ratios||Stapedial|
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
The basic shape of the bony labyrinth of M. domestica remains constant over the ontogenetic series studied (Fig. 3), but the labyrinthine constituents varied in size across the sample. The specific measurements described above were plotted over number of postnatal days to investigate whether specific dimensions are correlated with maturity, and all measurements with their corresponding coefficients of correlation (r), determination (r2), and significance values (P) are provided in Tables 2–6. There is no clear correlation between most of the angular dimensions measured and age (Table 2), although the total deviation from planarity of the lateral semicircular canal (r = 0.72; P = 0.01) expresses a strong correlation with the number of postnatal days after the walls of the labyrinth have ossified. The oldest M. domestica specimens tend to have lateral semicircular canals that deviated above the canal plane to a greater degree than younger individuals.
Another measurement that is correlated strongly with age is the height of the arc of the lateral semicircular canal (r = 0.80; P < 0.01), although the width (r = 0.25; P = 0.46), length (r = 0.55; P = 0.08), and arc radius of curvature (r = 0.54; P = 0.09) are not (Table 3). The correlation between the volume of the slender portion of the lateral semicircular canal and age is not considered strong under the parameters of the current study (r = 0.67; P = 0.02), but it is close. The coefficient of correlation likely will change with an increase in sampling of individuals.
A strong correlation is observed between age and the length of the posterior semicircular canal (r = 0.73; P = 0.01). In short, the posterior canal increases in length through the age sequence studied, even though the volume and radius of curvature of the canal do not. The length of the anterior semicircular canal is not correlated with age (r = 0.55; P = 0.08), nor is any other dimension of that canal.
The length of the canaliculus cochleae also shows a positive correlation to age, (r = 0.86, P < 0.01; Table 4), indicating that this bony tube for the perilymphatic duct increases in length as the bony labyrinth matures. The canaliculus cochleae is included in the segmentation of the cochlea, and therefore its volume is included in the cochlear volume. Despite the strong correlation of the length of the canaliculus cochleae, the overall volume of the cochlea is not significantly correlated with age.
No strong correlations were observed between age and partial or total volumes within the bony labyrinth (Table 5). The only statistically significant correlation was calculated for volume of the lateral semicircular canal (r = 0.67, P = 0.02), which is close to, but does not meet, the criterion for being considered a strong correlation in this study. Likewise, none of the ratios or indices expressed a strong correlation with age, although a significant but weak correlation was found between number of postnatal days the percentage of inner ear volume contributed by the cochlea (r = 0.64; P = 0.03). However, this correlation likely is spurious given that the canaliculus, the length of which is strongly correlated with maturity, is included in the cochlear segment.
Additional correlations also were found among the inner ear dimensions themselves. For example, there is a strong correlation between the total length of the inner ear and the radius of the arcs of the three semicircular canals (anterior, r = 0.86, P < 0.01; lateral, r = 0.72, P = 0.01; posterior, r = 0.73, P = 0.01). All of these values increase as the inner ear becomes longer. The total length of the bony labyrinth also is strongly correlated with the length of the skull (r = 0.74; P < 0.01), which in turn is correlated with number of postnatal days (r = 0.71; 0.01; measurements in Table 4). Although there is a strong link between the lengths of the inner ear and skull, the inner ear length does not show a strong correlation with age (r = 0.60; P = 0.05), even though the skull does. That is, the majority of the variation of the length of the inner ear cannot be explained by increasing age, but it can be explained by skull growth.
The lengths of each canal also correlate with the respective radii of curvature (anterior, r = 0.72, P = 0.01; lateral, r = 0.74, P < 0.01; posterior, r = 0.87, P < 0.01), so that canals with large arc radii of curvature have long slender portions of the canal. An additional strong correlation is observed between the aspect ratio of the anterior semicircular canal and the radius of its arc (r = 0.76; P < 0.01), but there is no observed correlation between the radius of the arc of any semicircular canal and its respective volume. Nor is a single canal more voluminous in every specimen. Either the anterior or posterior semicircular canal expressed the highest volume (each canal with the highest value in 5 of the 11 specimens). Unlike the volume, however, the anterior semicircular canal had the longest arc radius in every individual examined (see Table 3).
The aspect ratios of the semicircular arcs are not correlated with age, and neither is the aspect ratio of the cochlea (Table 6). There is not a strong relationship between maturity and volume, and the percentages that the various chambers of the inner ear contribute to the bony labyrinth do not follow a pattern of change across ontogeny.
- Top of page
- MATERIALS AND METHODS
- LITERATURE CITED
The results of this study show that few of the dimensions of the inner ear strongly correlate with ontogenetic age after ossification of the bony labyrinth is completed, but that variation is present within the structures of the inner ear. To investigate the observed variation, the discussion is divided into a review of the development of the inner ear of Monodelphis from birth through ossification of the bony labyrinth, followed by a discussion of the general patterns of variation within the ear region as compared to other vertebrates. Further exploration of the variation is then placed in both functional and phylogenetic contexts.
Development in Monodelphis domestica
The development of the inner ear of the closely related species Didelphis virginiana is well documented (e.g., Larsell et al., 1935; McCrady, 1938), and both D. virginiana and M. domestica share similar chronologies in skeletal maturation (although both species exhibit different rates of growth; Rowe, 1996, 1997). Because of this, information about the maturation of the inner ear of D. virginiana likely is similar in relative timing to that of M. domestica. At birth, the major structures of the membranous labyrinth of D. virginiana are clearly recognizable (Larsell et al., 1935: Fig. 3, Stage 35), but the inner ear is immature in form. The anterior, lateral, and posterior semicircular canals are present as complete tubes, but they are not as large as those of adults. The cochlea completes one half of a turn at birth, and will eventually complete two and a quarter turns in D. virginiana (Larsell et al., 1935), which is greater than the number of turns in M. domestica (just under two; see Table 2).
Ossification of the bony labyrinth has not begun at birth, and the petrosal bone itself is one of the last endochondral bones to begin ossification in M. domestica, around postnatal Day 12 (Clark and Smith, 1993). Ossification of the petrosal of M. domestica begins in three ossification centers around the developing cochlea, and the bone surrounding the cochlea is fully ossified by Day 25. Expansion of ossification of the cochlear cartilage and ossification of the postparietal into the region of the semicircular canals triggers the onset of ossification of the canalicular cartilage (Clark and Smith, 1993), which is underway by Day 20. The bony walls of the semicircular canals are the first to ossify, followed by the spaces between them.
Although the results of this study reveal that there is little appreciable change in the bony labyrinth once ossification has spread through the otic capsule, a few dimensions of the lateral and posterior semicircular canals are strongly correlated with ontogenetic age among the sample of M. domestica examined here. For example, the length of the posterior canal increases after birth (which is not the case for any other features of this canal). The correlation between age and posterior canal length does not signify an ontogenetic lengthening of the membranous canal necessarily, because there is not an exact relationship between size of the bony semicircular canal and the membranous duct within it. At one extreme, the cross-sectional area of the membranous posterior semicircular duct is only 7% of the cross-sectional area of the bony canal (Curthoys et al., 1977b). Although there is a correlation between the length of the posterior canal and maturity, the strength of the correlation likely will decrease as more individuals are added to the sample.
Because different aspects of the semicircular canals are correlated with age, the three canals develop in different fashions. In fact, ossification of the canals is not synchronous in humans (Bast et al., 1947; Jeffrey and Spoor, 2004; Richard et al., 2010), and the membranous ducts of Didelphis (Larsell et al., 1935) and other vertebrates (Norris, 1892; Knowlton, 1967; Haddon and Lewis, 1991; Bissonnette and Fekete, 1996; Mansour and Schoenwolf, 2005) are formed at different times, with the lateral canal the last of the three to fully develop in the opossum (Larsell et al., 1935), rat (Curthoys et al., 1982; Curthoys, 1983), and chicken (Knowlton, 1967; Bissonnette and Fekete, 1996). The arc radii of curvature of the lateral semicircular canal and membranous duct increase for a short period of time after birth in the rat (Curthoys et al., 1982; Curthoys, 1983), but adult size of the canal remains stable after adult size is achieved (however, there is a fair amount of size variation among adults). Only the arc radius of curvature was measured for the rat in those studies, and whether or not the length or deviation from planarity of the canal change in the postnatal rat is unknown at this time.
The petrosal of M. domestica is not fully ossified by Day 30 (Clark and Smith, 1993), but the only unossified portions are part of the styloid process and the lateral wall of the subarcuate fossa, which houses a petrosal lobule of the paraflocculus of the cerebellum. The styloid process does not contribute to the morphology of the bony labyrinth within the petrosal bone, but the subarcuate fossa is defined by the semicircular canals. The development of the bony semicircular canals versus the subarcuate fossa is not entirely independent in primates (Jeffery and Spoor, 2006), but the influence that subarcuate fossa ossification has on the dimensions and orientation of the fully ossified semicircular canals is unknown. The portion of the subarcuate fossa that has yet to ossify by Day 30 is between the lateral and anterior semicircular canals (Clark and Smith, 1993), which might account for the dimensional changes within the lateral canal that were observed in this study (which begins at Day 27).
In addition to the rat, the morphology of the bony labyrinth changes postnatally in Macaca mulatta (Daniel et al., 1982), although the change is in orientation rather than size. As has been noted for humans (Delattre, 1952; Sercer, 1958), the cochlea rotates anteriorly and superiorly with respect to the plane of the lateral semicircular canal during postnatal ontogeny in the macaque. Although absolute ages of the specimens used by Daniel et al. (1982) were unknown, a correlation between the rotation and postnatal stages based on dentition was found. However, there is not a significant correlation between the angle formed by the plane of the basal turn of the cochlea and lateral semicircular canal and age in M. domestica. The so-called “verticality” of the cochlea characterized by humans is thought to be related to the ability of an animal to maintain a bipedal stature (although see Fitzpatrick et al., 2006) which is not a typical behavior in M. domestica.
Although there are few morphologic changes among structures inside of the petrosal across the growth series, there is a correlation between age and features on the external surface of the petrosal. For example, the facial nerve canal of elephantoid proboscideans exhibits ontogenetic variation (Ekdale, 2009), and the length of the bony canaliculus cochleae, which connects the inner ear and the cranial cavity, increases over age in M. domestica (r = 0.86; P < 0.01). The petrosal grows via accretion of bone on external surface of the petrosal (Fig. 4), and the canaliculus cochleae elongates in order to connect the inner ear and endocranial cavities. A lappet of bone that partially shields the perilymphatic duct in echidnas (monotremes do not have a canaliculus cochleae divided form the fenestra cochleae; Kuhn, 1971; Zeller, 1989, 1991) continues to develop postnatally, as do other structures along the posteromedial aspect of the petrosal. For a review of the complex development and evolution of the canaliculus cochleae (and development of the associated processus recessus that separates the canaliculus from the fenestra cochleae), see de Beer (1929, 1937) and Rougier and Wible (2006).
Beyond anatomy, the development of auditory and vestibular physiological responses in M. domestica is well documented (Reimer, 1996; Aitkin et al., 1997). The middle ear cavity of M. domestica is filled with fluid until 26 days after birth, and the external auditory meatus opens 28–30 days postnatal (Aitkin et al., 1997), coinciding with the earliest evoked auditory responses (Reimer, 1996). Pouch young of D. virginiana respond to vestibular stimuli before acoustic reflexes are observed (Larsell et al., 1935), and the same may be the case for M. domestica (given similarities in skeletal development between the two species), although such a relationship between the physiological responses has yet to be determined for M. domestica. Evoked auditory responses can be detected in M. domestica at 28 days after birth, which is around the age of the youngest individuals used in the current study, and adult hearing thresholds are achieved by Day 39 (Reimer, 1996), after mature morphology and size of the bony labyrinth is achieved.
General Patterns and Comparisons
Although most of the measurements taken in this study did not show a correlation with the maturity of the individual, ranges of variation were observed in every dimension. Measurements with varying values are not significant phenomena given that variation is a natural occurrence, and the variation observed within M. domestica is comparable to that for other mammals. For example, the degree to which the anterior semicircular canal deviates from planarity is greater than the values for either the lateral or posterior semicircular canals (Fig. 5; Table 2), which is a pattern that also is observed in laboratory mice (Calabrese and Hullar, 2006). That is to say, the anterior canal is less planar than the other two canals, with an average total deviation of 12.9° versus 5.0° and 6.7° (for the lateral and posterior semicircular canals, respectively) in M. domestica. Further, the radius of the arc of the anterior semicircular canal is the greatest of the three arcs in M. domestica and in most other mammals (Blanks et al., 1972, 1975, 1985; Curthoys et al., 1975, 1977a, b; Ramprashad et al., 1984; Muren et al., 1986; Spoor and Zonneveld, 1998; Jeffrey and Spoor, 2004; Calabrese and Hullar, 2006; Spoor et al., 2007; Ekdale, 2009), as well as in birds (Hopkins, 1906).
The variation and correlations reported here may be influenced by several additional factors. For instance, males tend towards larger bodies than females in M. domestica (Macrini, 2004), but the opossum sample examined here is inadequate for determining sexual dimorphism in the inner ear in the species. However, a study focused on the issue of sexual dimorphism (as well as cranial asymmetry) within the shrew Blarina brevicauda found no statistical correlation between semicircular canal size and gender (Welker et al., 2009). Likewise, there is no statistical difference in size between right and left labyrinths.
Another factor affecting the observed range of variation is an artifact of specimen sampling. With the addition of more individuals, the correlation of these measurements might decrease, or else new correlations may be recovered. Future studies focused on the otic region of M. domestica will further elucidate the causes of variation exhibited by the inner ear.
The results of many studies (e.g., Gray, 1907; Hadžiselimović and Savkrović, 1964; Calabrese and Hullar, 2006; Hullar, 2006; Hullar and Williams, 2006; Sipla, 2007; Spoor et al., 2007; Cox and Jeffrey, 2010) support the hypothesis that the size of the semicircular canals is related to locomotor agility and speed (based on field observations, videos, and published reports; Spoor et al., 2007). Because features of the inner ear are not correlated with post-ossification age, the eventual behavior and function associated with labyrinthine anatomy, such as agility and hearing capabilities, emerges after the morphology is established in M. domestica. For example, adult hearing thresholds are achieved by Day 39 (Reimer, 1996), but the bony cochlea has achieved mature size and shape as late as Day 27.
Although it is well established that semicircular canal size is related to the sensitivity of the canal, the attainment of an adult physiological response of a canal may not be synchronous with the attainment of adult morphology in every situation. For example, the radii of the semicircular canals in the pike continue to grow throughout the life of an individual, but the physiological response of the canals does not increase (ten Kate, 1970). Conversely, gains of the vestibulo-ocular reflex increase into adulthood in the cat some 60 days after the adult size of the canals are met. The results of those studies suggest that, although there are osteological correlates for behavioral responses of the vestibular end organ, changes within the soft tissue structures of the inner ear (within the membranous labyrinth) play an important role in the development of otic physiology, which is only to be expected. After all, the functional units of both the cochlea and vestibule are composed of soft nervous tissue.
A portion of the middle ear region of mammals that is preserved on the external surface of the petrosal is a widely used source of phylogenetic information within and among major groups of mammals, including some of the earliest mammals (MacIntyre, 1972; Archibald, 1979; Wible, 1990; Meng and Fox, 1995; Rougier et al., 1998; Wible et al., 2001; Ekdale et al., 2004; Ladevèze, 2004; Ladevèze and Muizon, 2007), as well as members of crown Placentalia, such as Carnivora (Bugge, 1978; Hunt, 1987, 1989), Cetacea (Geisler and Luo, 1996; Luo and Gingerich, 1999), Chiroptera (Wible and Novacek, 1988; Wible and Davis, 2000), and Primates (MacPhee, 1981; Wible and Martin, 1993; Harvati and Weaver, 2006). Natural endocasts (lithified in-fillings) of the inner ear chambers are known for some fossil mammals (Kielan-Jaworowska, 1984; Miao, 1988; Court, 1992; Meng and Wyss, 1995) allowing the morphology of the inner ear to be used in phylogenetic analyses, but preservation of such fossils in the rock record is rare. Nonetheless, the inner ear has been used as a source for phylogenetic characters.
One measurement that is thought to be phylogenetically informative in mammalian systematics is the stapedial ratio (Segall, 1970; Rougier et al., 1998) describing the shape of the stapedial footplate, which forms part of the ventrolateral wall of the bony labyrinth. In monotremes and many basal mammals, the footplate of the stapes (and fenestra vestibuli) is circular, with a height to width ratio around 1.0 (Segall, 1970; Archibald, 1979; Wible, 1990; Rougier and Wible, 2006). A circular stapedial footplate is thought to be plesiomorphic for mammals, whereas a more elongate footplate is developed in more derived taxa. For example, the footplate of placentals tends to be elliptical with a ratio above 1.8 (although some eutherians are an exception; see also Wible et al., 2001 and Ekdale et al., 2004), and marsupials tend to fall in between monotremes and placentals with ratios less than 1.8 (again, there are some exceptions; see Segall, 1970). Indeed, the average stapedial ratio for M. domestica (1.5) falls within the range for marsupials, but there is variation in the ratio (1.3–1.7; Table 6), related in part to differences in the width of the fenestra vestibuli (which has a measurement range spanning 0.20 mm versus the span of 0.06 mm for the height) among individuals.
The stapedial ratio itself is not strongly correlated with age (r = 0.61, P = 0.05), nor does any M. domestica individual possess a ratio in the placental range proposed by Segall (1970), but the variation that is observed suggests that the use of the stapedial ratio as a discrete character in phylogenetic analyses could be problematic. It appears that the ratio varies in many taxa, not just M. domestica. For example, large ratio ranges are reported for two Cretaceous mammal taxa (Ekdale et al., 2004), as well as a sampling of elephantoid petrosals collected from Pleistocene deposits, wherein the range of ratios crosses the 1.8 cut-off (1.4–2.1) with nearly half of the specimens above 1.8, and half below (N = 57), although the average is at 1.8 (Ekdale, 2009, Table 2.1). Given the range of the measurement, the appropriate treatment of the ratio in phylogenetic analyses is as a continuous character.
The coiling of the cochlea is another character that was used previously in phylogenetic analyses (e.g., Wible, 1990; Rougier et al., 1998; Archibald et al., 2001). The cochlea is a more-or-less straight tube in non-mammalian synapsids, and slightly curved (but not coiled) in modern monotremes (Pritchard, 1881; Graybeal et al., 1989). In therian mammals (Theria is the group containing the most recent common ancestor of marsupials and placentals, plus all of the descendants of that ancestor), the cochlear duct begins its earliest embryogenesis as a straight tube, and it bends medially completing one or more full turns until the mature morphology is met during development (Larsell et al., 1935; Bast, 1947; Morsli et al., 1998; Mansour and Schoenwolf, 2005). No therian mammal possesses a cochlea that is curved <360° (Meng and Fox, 1995), except for a few potential exceptions known for extinct forms. One of these exceptions is the Cretaceous eutherian Uchkudukodon nessovi, the cochlea of which is curved at least 270°, but certainly does not complete an entire revolution (McKenna et al., 2000).
Other stem eutherians possess cochleae that complete around 360°, including Prokennalestes trofimovi (Wible et al., 2001) and zalambdalestids (Kielan-Jaworowska, 1984; Ekdale, 2009) from the Cretaceous of Asia. Zalambdalestids, P. trofimovi, and U. nessovi likely are outside of crown Placentalia (Wible et al., 2005, 2007, 2009), which suggests that a cochlea coiled at or just under 360° might separate crown placental mammals from their closest fossil eutherian relatives (given that most crown placentals have cochleae that complete coils well above 360°; Ekdale, 2009). However, broad ranges in cochlear coiling have tremendous implications for this hypothesis, especially because the variation of cochlear coiling in M. domestica spans 81°, nearly a full quarter of a turn (at the moment, it is unclear what the range of cochlear coiling is in most mammals, although variation is observed in other taxa; Ekdale, 2009). It should be noted that the range in the absolute degrees of coiling completed by the cochlea in M. domestica was measured for a sample for which the walls of the bony cochlea had ossified fully, and adult size of the cochlea had been attained already. The 81° difference is individual variation among mature cochleae, and it does not include the ontogenetic transformation of the membranous cochlea from a straight tube in the embryo to a coiled duct in the adult. Because such a broad range of cochlear coiling has been measured within species of mammals (here and Ekdale, 2009), the degree of coiling should be treated as continuous in phylogenetic analyses, rather than broken into discrete states (which in most studies is two; e.g., Rougier et al., 1998; Archibald et al., 2001; Wible et al., 2007).
All data have the potential to be useful in phylogenetic analyses, and given the over abundance of teeth in the mammalian fossil record, paleontologists constantly attempt to identify new phylogenetically informative characters from anatomical regions besides the dentition. The stapedial ratio and degree of cochlear coiling likely contain phylogenetic signal, and the best way to identify the informativeness of the characters is to treat them as continuous measurements. Continuous characters have been discussed thoroughly in the literature (Mickevich and Johnson, 1976; Thorpe, 1984; Pimentel and Riggins, 1987; Chapill, 1989; Stevens, 1991; Thiele, 1993; Polly, 2001; Rohlf, 2001; Wiens, 2001; Caumul and Polly, 2005; Goloboff et al., 2006; Cardini and Elton, 2008; Klingenberg and Gidaszewski, 2010), and there is controversy as to the treatment of quantitative data. Most agree that morphometric data are phylogenetically valuable, and measurement data are used by either dividing the measurements into discrete states (Archie, 1985; Goldman, 1988; Thiele, 1993; Strait et al., 1996; Gift and Stevens, 1997; Swiderski et al., 1998; Wiens, 2001), or else treating the data as true, continuous sequences (Goloboff et al., 2006; González-José et al., 2008). Although a thorough discussion of the treatment of continuous characters is beyond the scope of the current article, the latter treatment is considered here to be the most appropriate, because it preserves the full range of the data, and even the slightest difference in a measurement might ally taxa (González-José et al., 2008). Recently developed phylogenetic software packages, such as TNT (Goloboff et al., 2008), can analyze continuous data treated in this fashion.
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- MATERIALS AND METHODS
- LITERATURE CITED
The results reported above contribute to the first reconstruction of the bony labyrinth of M. domestica, a biomedically important marsupial mammal, which is consistent with the anatomy and variation observed in placental (e.g., Blanks et al., 1972, 1975, 1985; Curthoys et al., 1977a, b; Hullar and Williams, 2006; Spoor et al., 2007; Ekdale, 2009) and other marsupial mammals (Larsell et al., 1935; McCrady, 1938; Sánchez-Villagra and Schmelzle, 2007). That is, the posterior and lateral semicircular canals join to form a secondary common crus in M. domestica, as they do in other marsupials, and the anterior semicircular canal is the largest among the canals. The results also demonstrate that, first, taxonomists and functional anatomists need not worry about the maturity of individuals when dealing with most metrics of the inner ear of didelphid marsupials (although the implication might be indicative of a broader taxonomic pattern as there is little post-ossification change in the bony labyrinth of rabbits; Hoyte, 1961) as long as the walls of the bony labyrinth are ossified. In several cases, the adult form precedes the onset of function of the system. Second, there is noticeable intraspecific variation that is not related to ontogeny. The variation may be the result of one or any combination of several factors, and observed variation could influence greatly the results of physiological and phylogenetic studies.
Although most of the dimensions do not change shape or size once the walls of the labyrinth have ossified, the variation observed within the inner ear of M. domestica is an important biological phenomenon that cannot be ignored. Without further investigation into the variation within a species, use of measurements, such as the stapedial ratio and coiling of the cochlea, in phylogenetic analyses is problematic. To maximize the utility of the measurements, those dimensions should be treated as continuous characters.
The majority of shape and size variation observed within the bony labyrinth of M. domestica indicates intraspecific variation, regardless of ontogenetic age, as opposed to ontogenetic trends in morphologic change, and the adult morphology of the system is attained before the animal achieves mature hearing or locomotor potential. Barring any major pathology (e.g., Fomina-Kosoplova, 1965; Alkhadhi et al., 2004; Aralşmak et al., 2009), the fully ossified bony labyrinth should retain the same morphology throughout the life of the animal. Therefore, the petrosal of a juvenile is as valuable in interpreting behavior, physiology, and possibly phylogeny as is the petrosal from an elderly individual.
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- LITERATURE CITED
This research was done to fulfill partial requirements for the author's Ph.D. degree at The University of Texas at Austin. He is grateful to the members of his Ph.D. committee, Tim Rowe, Chris Bell, James Sprinkle, Matt Colbert, and Zhe-Xi Luo, for their support during this project. He also thanks Ted Macrini for access to the CT data, and Southwest Foundation for Biomedical Research in San Antonio, TX, for provision of specimens. Kerin Claeson, Jen Olori, Jeri Rodgers, as well as Scott Miller (editor), and two anonymous reviewers, provided helpful comments during preparation of this manuscript. The specimens were scanned by Matt Colbert at UTCT.
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- MATERIALS AND METHODS
- LITERATURE CITED
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