The Middle Ear of the Author(s): Winston C. Lancaster Source: Journal of Paleontology, Vol. 10, No. 1 (Mar. 29, 1990), pp. 117-127 Published by: Taylor & Francis, Ltd. on behalf of The Society of Vertebrate Paleontology Stable URL: https://www.jstor.org/stable/4523301 Accessed: 08-04-2021 19:22 UTC

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This content downloaded from 131.204.154.192 on Thu, 08 Apr 2021 19:22:22 UTC All use subject to https://about.jstor.org/terms Journal of Vertebrate Paleontology 10(1): 117-127, March 1990 © 1990 by the Society of Vertebrate Paleontology

THE MIDDLE EAR OF THE ARCHAEOCETI

WINSTON C. LANCASTER Idaho Museum of Natural History, Box 8096, Idaho State University, Pocatello, Idaho 83209-0009 (Present address: Department of Cell Biology and Anatomy, C.B. 7090, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599-7090)

ABSTRACT- The auditory ossicles and tympanic bulla of the Archaeoceti show little intergeneric morphological variation, and are similar to the ossicles of extant cetaceans in most respects. The attachment of the tympanic membrane is separated from its origin indicating that the Archaeoceti possessed an elongated, conical tympanic conus unique to cetaceans. The sigmoid process is an ex- pansion of the anterior limb of the ancestral tympanic bone and is entirely ectotympanic in origin. Expansion of the sigmoid process is partially responsible for the elongation of the tympanic conus by spatially separating the manubrium of the malleus out of the plane of attachment of the tympanic membrane. Elongation is further augmented by the reduction of the manubrium of the malleus, and by the evolutionary rotation of the malleus-incus system about its physiologic axis of rotation. Evo- lutionary rotation, reduction of the manubrium, and an expanded sigmoid process all contributed to a system of angular amplification that is still present in extant cetaceans. The specific gravity of the ossicles is greater than that of any extant cetacean for which it is known. This could have resulted from the systemic increase in bone density experienced by archaeocetes in their adaptation to the marine environment. These adaptations appear in the earliest cetacean, inachus, and are well developed by the Late in the . Such adaptations could have laid the foundation for the development of underwater echolocation by enabling the middle ear to transmit high-frequency sound.

INTRODUCTION Miocene mysticete Thinocetus arthritus (Kellogg, 1969). The holotype of the Miocene odontocete Kentriodon The auditory ossicles, the malleus, incus, pernix and includedstapes, a complete set of auditory ossicles, are rarely recovered in the excavation of which fossil was verte- described by Kellogg (1927). The stapes of brates and hence are poorly known in fossil this specimentaxa. The cannot be relocated (R. Purdy, pers. only previously known auditory ossicles from comm., archaeo- 1983). Auditory ossicles of the Miocene squa- cete cetaceans are those of osiris lodont (Pompeckj, Phocageneus venustus were described by Kel- 1922; Kellogg, 1936) and the stapes of logg (1957). ko- The malleus and stapes of an unnamed chii (Kellogg, 1936). The latter specimen (part middle of Miocene USNM rhabdosteid were described 10857) was removed from the isolated periotic by Fordyce to which (1983). Wilson (1972) described the au- it was attached, and cannot be relocated (F.ditory C. ossiclesWhit- of the Miocene Loxolithax stocktoni and more, pers. comm., 1983). compared them to living delphinids and phocoenids. The purpose of this study is to describe the mor- phology of the auditory ossicles in archaeocetes, Abbreviations and compare them to the auditory ossicles of other fossil AUMP-Auburn University Museum of Paleon- and extant cetaceans. Additionally, the evolution and function of the cetacean middle ear will be discussed. tology, Auburn, Alabama; LSUMG -Museum of Geoscience, Louisiana State University, Baton Rouge, The above-mentioned works are the only references Louisiana; LSUMZ -Museum of Zoology, Louisiana to the auditory ossicles of the Archaeoceti known to me, but the ossicles of several other fossil cetaceans State University, Baton Rouge, Louisiana; USNM-- National Museum of Natural History, Smithsonian In- have been described by Kellogg. Kellogg (1924) illus- stitution, Washington, D.C. trated the malleus of the Miocene mysticete Parieto- balaena palmeri, described a tympanic bulla with an MATERIALS attached malleus of P. palmeri, and provided a de- scription of the three auditory ossicles of the Miocene Specimens examined during the course of this study mysticete Metopocetus durinasus (Kellogg, 1968). A include the following: complete set of auditory ossicles, including a tympanic 1) cetoides (Owen, 1839), LSUMG V 1, bulla with the malleus attached, is described for the Late Eocene, one right malleus, one right incus, one

117

This content downloaded from 131.204.154.192 on Thu, 08 Apr 2021 19:22:22 UTC All use subject to https://about.jstor.org/terms 118 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 10, NO. 1, 1990 left incus, and one right stapes; 2) Globicephala me- las (Traill, 1809), LSUMZ 15912, Recent, one right malleus; 3) Kentriodon pernix Kellogg, 1927, USNM 8060, Miocene, one left malleus and one left incus; 4) Tursiops truncatus (Montague, 1821) AUMP 2623, Recent, one right tympanic bulla with malleus intact; and 5) Zygorhiza kochii (Reichenbach, 1847), LSUMG V160A, Late Eocene, one left tympanic bulla and one left incus; AUMP 2368, complete skull with detached left tympanic bulla and left malleus; USNM 11962, m m complete skull.

MORPHOLOGY

There is little morphological difference between the auditory ossicles of archaeocetes. The descriptions be- low are for the Archaeoceti in general, with specific differences noted. Terminology follows Fraser and Purves (1960b) except where noted. Dimensions of the ossicles are listed in Table 1. The archaeocete malleus (Fig. lA, B) has a distinct head and column separated by an oblique fissure. The head is globose, and bears two articular surfaces ori- ented perpendicularly to each other. The larger surface is oriented vertically; the smaller is horizontal. The dorsal perimeter of the large facet defines the dorsal edge of the head. The column of the malleus extends FIGURE 1. Archaeocete auditory ossicles. A, right malleus ventrally from the head, and has a small tubercle onof Basilosaurus cetoides (LSUMG V1), posteromedial view; B, left malleus of Zygorhiza kochii (AUMP 2368), postero- its ventral extremity, which is the attachment point of medial view; C, left incus of Basilosaurus cetoides (LSUMG the tympanic membrane. A small pit on the anterior V1), dorsolateral view; D, left incus of Zygorhiza kochii side of the column dorsal to its extremity is the site of (LSUMG Vi160A), ventrolateral view; E, right stapes of Bas- insertion for the tensor tympani muscle. The interspe- ilosaurus cetoides (LSUMG Vi ), posterior view. Abbrevia- cific differences are minor. The fissure between the tions: af, articular facet; c, column of malleus; cb, crus breve; head and column is more distinct in Basilosaurus ce- cl, crus longum; f, stapedial foramen; fp, footplate; h, head toides than in Zygorhiza kochii. The manubrium of of malleus; Ip, lenticular process; m, manubrium; pg, pro- the malleus of B. cetoides is broken, but is retained incessus gracilis; st, stapedial tubercle. the specimens of Z. kochii (AUMP 2368) and Dorudon osiris (Pompeckj, 1922). The insertion of the tensor tympani is more strongly developed on the specimen bulla. In this area, the lateral wall of the bulla is arched of B. cetoides than on that of Z. kochii and is not clear over the tympanic cavity to form a horizontal surface. on the illustration of D. osiris (Pompeckj, 1922). This surface is divided by the anteroposteriorly ori- The malleus is firmly attached to the tympanic bulla ented sulcus for the chorda tympani nerve (Kellogg, by the processus gracilis (Figs. 2, 3C) (gonial, anterior 1936), which is defined by two parallel ridges of bone. process, processus folianus, and processus longus of The sulcus is approximately 3 mm wide at its widest authors). The processus gracilis attaches to the antero- point, and is approximately 18 mm in length. The lateral side of the malleus with a pit at its base for the defining ridges gradually diminish anteriorly and con- chorda tympani nerve (Kellogg, 1936). A channel runs verge posteriorly. The medial ridge turns and meets the length of the processus gracilis giving it a girder- with the lateral ridge, which is continuous with the like appearance. dorsal leg of the processus gracilis. The channel in the The processus gracilis of Zygorhiza kochii (AUMP processus gracilis is not continuous with the sulcus for 2368) is attached to the tympanic bulla anterior and the chorda tympani, which is truncated by the turn of medial to the sigmoid process, against which the mal- the medial ridge. The delicate sculpturing of the an- leus is securely buttressed (Fig. 3C). The sigmoid pro- terior pedicle conforms closely to the form of the ar- cess is an arcuate, dorsal continuation of an S-shaped ticular surface of the bullar process of the squamosal, ridge of bone originating on the thin lateral wall of the thus providing a congruent articulation. The bullar tympanic bulla. It is flattened anteroposteriorly, and process is not fused with the tympanic bulla, but ar- has a thick border that surrounds a central area com- ticulates with the anterior pedicle medial to the sulcus posed of thin bone; thus the posterior side appears for the chorda tympani. concave. It is inclined anteriorly with a flattened sur- On its posterior side, the sigmoid process is sepa- face sloping from the anterior pedicle of the tympanic rated from the smaller conical process (conical apoph-

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It is also concave medially, but is less concave than its lateral counterpart. The two parts of the pedicle are separated by a gap in the thin wall at its posterior extremity, referred to by Kasuya (1973) as the elliptical foramen. The incus is conical (Fig. 1 C, D). The base of the cone forms the larger of two facets for articulation with the malleus. A smaller facet is on the ventral side. Both facets are concave and articulate with the malleus. The crus longum is a stout, direct continuation of the body of the incus. It extends posteriorly from the malleus turning dorsally at its extremity and ending with the oval lenticular process at its articulation with the stapes. The articular surface of the lenticular process is at a right angle to the base of the cone. The crus breve extends posteriorly and dorsally from the incus to ar- ticulate with the fossa incudis of the periotic. The dor- somedial face of this flattened process bears a tear-

i pt

sq

( .:...' .'." earn ; :. ~ ~prp bo ce ...I FIGURE 2. Outline of ventral side of skull of Zygorhiza cc e kochii showing position of tympanic bulla (stippled). Abbre- viations: bo, basioccipital; eam, external auditory meatus; prp, paroccipital process; pt, pterygoid; sq, squamosal; tb, tympanic bulla. 7.7 .'i ysis, or median process of Kellogg, 1936) by a narrow cp cleft (Fig. 3A, B). As noted by Kellogg (1936), the conical process is more steeply inclined on its anterior side than its posterior side. The sigmoid process over- p 5 m m / A hangs the conical process. A low ridge beginning below and lateral to the rounded apex of the conical process extends in a posteroventral direction, terminating at FIGURE 3. A, left tympanic bulla with attached malleus the posterior pedicle. Judging from modern cetacean of Zygorhiza kochii (AUMP 2368), dorsal view; B, same specimen, close-up of malleus and sigmoid process, posterior anatomy, this ridge probably formed part of the an- view; C, same specimen, close-up of malleus and sigmoid choring area for the tympanic membrane. The poste- process, anterior view. Abbreviations: ce, tympanic cavity; rior pedicle has two thin, curved legs. The lateral one cp, conical process; ct, sulcus for chorda tympani; i, invo- is concave medially, and is located on the lateral wall lucrum; 1, lateral wall; m, malleus; pg, processus gracilis; pp, of the bulla, while the shorter medial leg is on the posterior pedicle; s, sigmoid process; tl, insertion point of involucrum (the massive medial portion of the bulla). tympanic conus; tt, insertion point of tensor tympani muscle.

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TABLE 1. Dimensions of archaeocete auditory ossicles and tympanic bulla (mm).

Basilosaurus Zygorhiza kochii cetoides LSUMG AUMP LSUMG V1 V160A 2368

Malleus Greatest length 10.1 9.9 Width of head 7.2 6.2 Width of large facet 4.7 4.7 Width of small facet 3.4 3.2

Incus Greatest length 6.4 5.8 Width of body 5.4 5.2 Width including crus breve - 6.4 Thickness of body 4.3 3.9 Stapes Greatest length 5.4 Greatest width of footplate 3.9 Least width of footplate 3.2 Tympanic Bulla Greatest length 74.7 Greatest transverse width at sigmoid process 53.7 Greatest height-tip of sigmoid process to ventromedial edge 61.2 Width across posterior prominences 43.7 Width of dorsal border of sigmoid process 18.6

shaped articular surface. The The most processus interesting interpreted gracilis soft tissue feature of the malleus and the crus breve of the incus form an axis of the middle ear of the Archaeoceti is the tympanic about which the malleus-incus system rotates (Fleisch- membrane (Fig. 4). In modem cetaceans this is mod- er, 1978). ified into an elongated, conical structure called the tym- The stapes of the Archaeoceti has a patent stapedial panic conus by Reysenbach de Haan (1957). Fraser foramen (intercrural foramen) (Fig. 1E). The footplate and Purves (1960b) and Fleischer (1973, 1978) refer is ovoid, but slightly flattened on the ventral side. toThe the lateral, concave portion of this structure that is base of the footplate is concave. The head of the stapes attached to the tympanic bulla as the tympanic mem- bears a facet for articulation with the lenticular process brane, and to the elongated portion attaching to the of the incus. On the posterior side of the head of malleusthe as the tympanic ligament. This implies a dual- stapes is a distinct tubercle for the insertion of the ity of structure that does not exist and I will conform tendon of the stapedius muscle. to the terminology of Reysenbach de Haan (1957). Important features of the soft tissue anatomy can Figures be 4 and 7 illustrate that the manubrium of the interpreted by extrapolation from the preserved hard malleus in Zygorhiza kochii is approximately 15 mm parts. Muscle scars on the malleus and stapes indicate out of the probable plane of attachment of the tym- that the tensor tympani and stapedius muscles were panic conus, indicating the existence of an elongated, present. The tensor tympani originated in a pit lateral ligamentous tympanic conus such as that possessed by to the pars cochlearis of the periotic, and passed pos- modem . In Z. kochii (AUMP 2368) the tym- teriorly through a channel between the pars cochlearis panic conus originated from the ridge on the conical and an enlarged fossa for the head of the malleus. process,It the posterior edge of the sigmoid process, and inserted on the anterior aspect of the column of thethe anterolateral side of the posterior process and ad- malleus. The stapedius muscle originated in a fossa jacent portions of the squamosal (hereafter referred to also lateral to the pars cochlearis, but posterior to the as the plane of attachment of the tympanic conus). The ossicular chain. The orientation of the stapedial tu- lateral surface of the conus was about 12 mm in di- bercle indicates that the stapedius muscle pulled at an ameter. A model of this system, which was made of angle oblique to the long axis of the footplate. It oc- clay and attached to the appropriate surfaces, indicates cupied a channel with the facial nerve (Kellogg, 1936). that the plane of attachment of the conus was almost The articulation of the incus and the malleus in mod- transverse in orientation, and not perpendicular to the em cetaceans is a synovial joint (Fraser and Purves, obliquely oriented external auditory meatus. The ad- 1960a). This joint in archaeocetes is similar to that of vantages rendered by this system and its function have extant cetaceans, and was probably synovial. It was been discussed by Fraser and Purves (1960a, b), not fused in any of the specimens examined. Fleischer (1973), and Purves and Pilleri (1983). The

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malleus and the head of the stapes, respectively. Fleischer (1978) discussed the qualities and shortcom- ings of this system. The archaeocete ear adapted to its new environment x in a variety of ways, and it is useful at this point to briefly discuss some of the physical differences between sound in air and in water as they relate to mammalian middle ears. Most studies of the function of the ceta- h cean middle ear have addressed this topic (Reysenbach s y c de Haan, 1957, 1960; Fraser and Purves, 1960a, b), and a clear treatment is also given by Hawkins and

ti Myrberg (1983). At approximately 1,500 m/s, the speed of sound in water is roughly five times faster than in air. Since the wavelength of sound is the product of speed and frequency, it can be easily seen that for a given frequency, the wavelength of a sound will be five z times longer in water than in air. As is the case with visible light, the resolving power for acoustic imaging is dependent on the wavelength and on the capability of the ear to detect the frequency. Sounds with small wavelengths provide the capacity for a greater reso- II lution than long wavelengths, but do not propagate as ~5mm far as those with longer wavelengths. The potential for FIGURE 4. Reconstruction of tympanic conus onto left this enhanced resolution of objects with high frequency tympanic bulla and malleus of Zygorhiza kochii, viewed from partly explains the use of ultrasonic signals in echo- dorsal side down the axis of rotation of malleus-incus system location. (Y). Coordinate system refers to orientations in Figure 6. Owing to a density over 800 times greater than air, Abbreviations: ant., anterior; c, column of malleus; h, head the acoustic impedance of water (the product of density of malleus; lat., lateral; s, sigmoid process; tl, insertion point and speed of sound) is far greater than air. A sound of tympanic conus. field in any medium can be described both as periodic fluctuations of pressure and as the back and forth mo- tion of the component particles of the medium (Haw- evolution of this system has been discussed by Fleisch- kins and Myrberg, 1983). Since acoustic impedance er (1978). can also be derived as sound pressure divided by par- ticle velocity, it can be seen that all of these physical EVOLUTION factors are interrelated. Changes in one are countered by proportionate changes in others. Due to the increase In a discourse on the evolution of the mammalian in density and speed of sound encountered in water, middle ear, Fleischer (1978) described and dia- grammed the hypothetical middle ear from which those of all therians were ostensibly derived. It is from this periotic point that I will begin a discussion of the development of the middle ear in the Archaeoceti. i:. incus stapes According to Fleischer (1978) the ancestral therian . - malleus middle ear (Fig. 5) has a U-shaped tympanic bone (ectotympanic) suspended by connective tissues from the surrounding bones of the skull. The malleus is rig- idly attached to the anterior limb of the tympanic via 0*-manubrium the gonial (processus gracilis). The body of the malleus o " tympanic extends posteriorly from the gonial and bears an elon- memmbrane gated manubrium extending ventrally into the plane .. gonial of the tympanic bone. The manubrium attaches to the tympanic membrane, which is stretched between the limbs of the tympanic bone. The incus articulates with .00:: ..~. . 0tympanic bone the malleus dorsally, with its crus breve extending dor- -0 - 0*.* ** ' skull sally into the fossa incudis of the periotic and its crus connective longum extending posteriorly to its articulation with tissue the stapes. The stapes inserts into the fenestra ovalis FIGURE 5. Hypothetical ancestral therian middle ear, left of the periotic. The two middle ear muscles, the tensor ear viewed from medial side, anterior to the right. Adapted tympani and the stapedius, attach to the body of the from Fleischer (1978).

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Fleischer was correct. Most of the features Fleischer (1973) attributed to the process of evolutionary rota- tion show their beginnings in Zygorhiza kochii, and many were already well developed. By means of a series of schematic diagrams, Fleischer (1973) illustrated and described the geometric relationships of the ossicular chain to the tympanic bulla in T. truncatus. h Fitting the system into a rectangular coordinate sys- x tem (Fig. 6) in which the Y coordinate is the axis of rotation, and the Z coordinate is the long axis of the malleus running from its intersection with the Y co- ordinate to the insertion of the tympanic ligament, Fleischer (1973) measured the angle through which the z malleus had rotated out of the plane of attachment of the tympanic conus. This angle is labeled 'alpha' and FIGURE 6. Rectangular coordinate system superimposed is referred to as the evolutionary angle. Angle 'alpha' onto a schematic archaeocete malleus. The 'Y' coordinate is in T. truncatus is 60 degrees (Fleischer, 1973). By con- the axis of rotation of the malleus-incus system; the 'Z'structing co- a model of the tympanic conus onto the tym- ordinate is the long axis of the malleus. For abbreviations, panic bulla of Zygorhiza kochii, and using photographs see Figure 1. taken orthogonal to the Y coordinate, I measured an evolutionary angle of 75 degrees (Fig. 7). This quantity at first seems surprising, because intuitively one would assume that this angle in a more primitive form would sound pressure increases sixty-fold and particle veloc- be smaller than in a highly derived form such as T. ity decreases by the same proportion (Reysenbach de truncatus. However, the use of a geometric model to Haan, 1957). Therefore, the important physical pa- demonstrate the effects of ossicular rotation as a me- rameters of sound to which the archaeocete middle ear chanical amplification system helps to clarify the point. seems to have been adapted in the transition from airSuch a model was presented by Fraser and Purves to water were increases in the speed of sound, imped- (1960a). They described the cetacean middle ear as a ance of the conducting medium, sound pressures and crank amplification system and, by projecting the sys- wavelengths, and a decrease in particle velocity. tem into a single plane, produced a schematic diagram Among the most drastic of the modifications over that can be easily visualized and quantified. the primitive condition is that seen in the tympanic bone. The small U-shaped tympanic bone of the an- cestral ear developed into the massive tympanic bulla characteristic of the Cetacea. This feature is clearly developed in the most primitive known cetacean, Paki- cetus inachus (Gingerich and Russell, 1981). These au- thors believe the tympanic bulla to the entirely ecto- tympanic in origin and therefore derived solely from the ancestral tympanic bone. While the tympanic bulla of P. inachus retains primitive features (to be discussed below), it is highly modified from the ancestral form. It is clearly elongated into a channel-like structure rath- - - - -.- -. -- : of- "deflection malleus er than the simple U-shaped element of the ancestral S - " " - A(output) ear. The long axis of the channel (the tympanic cavity) is oriented in an oblique direction rather than trans- displacement versely (Gingerich and Russell, 1981:fig. 3). S (input) ''Z Other modifications seen in the archaeocete middle 'plane of ear are within the enlarged tympanic bone and involve tympanic the rotation of the ossicular chain. This rotation was conus probably coupled with the change in orientation of the tympanic bone itself. Fleischer (1973) described the rotation of the ossicular chain in Tursiops truncatus and considered the functional value of this system. FIGURE In 7. Schematic representation of angular amplifi- cation system in archaeocete middle ear based on Zygorhiza a later work, Fleischer (1978:24) further discussed this kochii, oriented as in Figure 4. Heavy dashed line indicates topic in a more evolutionary vein and stated, "This position of B and C after displacement of tympanic conus. evolutionary rotation is common to all cetaceans and See text for explanation. Adapted from Fraser and Purves must have occurred early in their evolution." The mor- (1960a). Abbreviations: B, long axis of the malleus; C, line phology of the archaeocete middle ear indicates that of action of tympanic conus; Y, axis of rotation.

This content downloaded from 131.204.154.192 on Thu, 08 Apr 2021 19:22:22 UTC All use subject to https://about.jstor.org/terms LANCASTER--MIDDLE EAR OF THE ARCHAEOCETI 123 leus) will be a rotation about the Y axis through angle omega. Since the ancestral therian ear, like modem mammalian middle ears, is also a rotational system, ScI; I the effect would be similar. However, in the ancestral ear, the angle at which the line of action acts upon the long axis of the malleus (mu) is approximately 90 de- grees, and therefore the amplifying effect of rotation is insignificant. Since C, the Z coordinate, and the plane of attachment of the tympanic conus form a triangle, alpha and mu are directly proportionate. As alpha in- BA IA i creases, mu decreases. By decreasing mu (and thus increasing alpha), the amplifying effects of the angular rotation are enhanced and can be easily visualized (Fig. 7). Due to the angle, there is a greater rotational output (angle omega) than linear input (tympanic conus dis- placement). With a constant C, B, and displacement,

I the angle of output (omega) is increased by decreasing angle mu.

I While the variation of the angle mu has an easily demonstrated effect on the output of the system, it can i I be mathematically demonstrated that changes in the pD ID relative sizes of B and C are also important. Using the proportions of the archaeocete middle ear as the pa- rameters of B and C with the angle mu of Tursiops 1 truncatus (30 degrees) results in a much smaller angle omega than if the dimensions of the T. truncatus ear FIGURE 8. Proposed evolutionary development of the ar- are used for all parameters. It is not surprising that the chaeocete middle ear, left side viewed from a posteromedial angle of attachment on the malleus would be adjusted perspective. Note the original orientation of the footplate of the for the optimal factor of amplification based on the stapes and the changes that occur during the process of evolutionary sizes of the ossicles, and other morphometric factors rotation. In each case, the vertical dotted line is such as ossicularthe density and the stiffness of the entire axis of rotation of the malleus-incus system. A, an adaptation system. The important factor about the rotation of the of the hypothetical ancestral therian middle ear of malleus with respect to the tympanicFleischer conus is that the (1978). B, the manubrium of the malleus and the amplification of the system is based not only on the long process of the incus have shortened and the evo- lutionary angle, but on the lengths of the malleus, ligamentous rotation about the physiologic axis of rotation has begun. portion of the tympanic conus, and other components C, the anterior limb of the tympanic bone has become broader of the system. Therefore, a direct comparison of the and the posterior limb has become less distinct as the tympanic bulla has begun to form. Coupled with con- angles is an oversimplification. The dimensions and tinuing rotation, the axis of rotation has been displaced out of relationships of the system are thealso affected by the plane of the tympanic membrane. D, the sigmoid process sigmoid process. is in place as a buttress to the malleus; rotation and displacement In Tursiops truncatus and all other odontocetes ex- are complete. A-C are hypothetical, D is drawn from amined, the sigmoid process is relatively smaller than Zygorhiza kochii. in the Archaeoceti. This larger size in archaeocetes further contributes to the separation between the plane In of attachment and the point of insertionthis of the tym- system (Fig. 7), C is the longitudinal axis of the panic conus, thus increasing alpha and decreasing mu. tympanic conus, and B is the long axis of the mal- leus, Therefore, the smaller evolutionary angle (alpha) of which lies on the Z coordinate. Point Y is the axis of the derived odontocete over the primitiverotation archaeocete of the malleus-incus system. The semicircle proscribes is in part the result of further reduction of the manu- the arc through which the distal end of the malleus brium of the malleus and a relatively smaller sigmoid (the manubrium) moves as it is acted upon by displacements process. of the tympanic conus. The evolution- ary The elongation of the tympanic conus is not entirelyangle, alpha, is formed by projecting the long axis of explained by the rotation of thethe malleus and the re- malleus along the Z coordinate to the plane of attachment duction of the manubrium. The development of the of the tympanic conus. Angle mu lies be- tween sigmoid process is fundamental to the evolution of the the line of action of the tympanic conus (C) and the cetacean middle ear (Fig. 8). The sigmoid process, seenaxis of the malleus (B). Angle omega, which rep- resents only in the Cetacea, is said to act as a lateral buttress the rotational output, is the angle through which B for the malleus (Fraserrotates and Purves, 1960a). This is for a given displacement of the tympanic conus. certainly the case in the Archaeoceti, in which the en- In this model, if the tympanic conus is displaced along tire lateral face of the malleus is appressed against the the axis of C, the resultant action on B (the mal-

This content downloaded from 131.204.154.192 on Thu, 08 Apr 2021 19:22:22 UTC All use subject to https://about.jstor.org/terms 124 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 10, NO. 1, 1990 medial surface of the sigmoid process. The ear sigmoid modified as a particle velocity detector rather than process also makes a contribution to rotation a sound by pressure phys- detector could aid cetaceans in the ically separating the axis of rotation of the discrimination malleus of direction. This should not, however, from the plane of attachment of the tympanic be taken toconus. extreme without more substantive evi- Fleischer's diagrams illustrate this separation, dence. but it is not discussed. Surely, in terms of the elongation Another of adaptation the of the cetacean middle ear to tympanic conus, this spatial separation is underwaterequal in soundim- is the reduction of the manubrium portance to the rotation of the malleus. of the malleus and the long process of the incus, and The sigmoid process forms one of the primary the thickening at- of the crura of the stapes. Reduction of tachment sites of the tympanic conus (Pompeckj, these long, 1922; thin elements lessens the tendency of the Kellogg, 1936). If the sigmoid process is indeed ossicles a to struc- vibrate relative to each other when subjected ture unique to the Cetacea, the question of to itshigh homol- frequencies and the higher sound pressures ogies must be addressed. In that the cetacean encountered tympanic in water (Fleischer, 1978). In the Basi- bulla is considered to be entirely ectotympanic losauridae in originthese changes had already occurred. This (Novacek, 1977; Moore, 1981), the sigmoid process can be seen as a fundamental change in the ossicles of can only have developed from the ectotympanic. As the Cetacea and, in the formation of an elongated tym- the anterior attachment site of the tympanic conus, it panic membrane, the reduction of the manubrium seems likely that this is simply an expansion of the probably played as important a role as ossicular ro- anterior leg of the ancestral tympanic bone. This ex- tation, or the enlargement of the sigmoid process. pansion developed in such a way as to spatially sep- The lack of substantive differences between the au- arate the processus gracilis out of the plane of the tym- ditory ossicles of the archaeocetes comes as little sur- panic membrane. This displacement of the malleus prise since the three species are contemporary mem- would alone result in the attenuation of the tympanic bers of the same family (Basilosauridae). The conus and a change in the angle between the malleus configurations of the tympanic bulla and the basicra- and the tympanic conus. Coupled to the simultaneous nial air sinuses are also similar in the three species reduction in the manubrium of the malleus and ossicu- (Kellogg, 1936; Lancaster, 1982), but significant dif- lar rotation, the result was a system of interdependent ferences are seen in the more primitive archaeocetes. dimensions and angles that together comprise the sys- The characteristics of the cetacean tympanic bulla tem of angular amplification. While Fraser and Purves that appear to be common to all members of the order (1960a), Fleischer (1973), and Moore (1981) have are: 1) massive, high density bone, 2) loose attachment quantified the mechanical and acoustic function of this to the skull (the degree of this character varies, partic- system, I have avoided most of the specific quantita- ularly in the Archaeoceti), and 3) the presence of a tive elaborations. Direct tests of this nature on fossil sigmoid process. Other characteristics of the cetacean material would rely on many assumptions that would tympanic bulla such as size relative to the skull, ori- cast serious doubts on the results. entation, and homology are either highly variable with- In the development of their hypotheses, Reysenbach in the order or are shared with other groups of mam- de Haan (1957) and Fraser and Purves (1960b) suggest mals. From the description of Gingerich et al. (1983), that the cetacean middle ear has developed into an it can be seen that the tympanic bulla of Pakicetus amplitude amplifier to compensate for the 60-fold de- inachus is cetacean in form for the first and third char- crease in amplitude in underwater sound as compared acters, but less so for the second. While its attachment to aerial sound (sound amplitude is directly propor- is clearly less secure than in most terrestrial , tionate to particle velocity (Reysenbach de Haan, the four points of articulation are more than in any 1957)). In comparing these two parameters of sound, other cetacean. The rapid adaptation of the cetacean it is of interest that sound pressure, measured in dynes/ middle ear to underwater sound is exemplified by the cm2, is a scalar quantity, variable only in magnitude. fact that occipital articulations and medial supporting Particle velocity, measured in cm/s is a vector quantity, structures of the tympanic bulla of P. inachus are elim- acting in a particular direction. As such, a sound re- inated in the confamilial atavus (Kellogg, ceptive organ that is sensitive to particle velocity will 1936). As for the remaining attachments, the anterior be inherently directional (Hawkins and Myrberg, 1983). pedicle of Z. kochii (AUMP 2368) articulates with a The ears of certain species of fish have been demon- bullar process of the squamosal that is lateral to the strated to be specifically sensitive to particle velocity anterior process of the periotic, the two being separated of sound in water rather than sound pressure and, by a narrow fissure. The same condition exists in Bas- therefore, are particularly sensitive to the directionality ilosaurus cetoides (LSUMG Vi), however, the bullar of sound (Hawkins and Myrberg, 1983). Considering process of the squamosal does not appear to be present the speed of sound in water, interaural distance pro- in all individuals. In at least one specimen of Zygorhiza vides little time delay to be used as a directionality kochii (USNM 11962), the anterior process of the peri- cue. Due to the small difference between the acoustic otic serves as the articular surface for the anterior ped- impedance of water and soft tissues, there would beicle of the tympanic bulla. Other specimens in the col- little difference in sound pressure between the two lectionsears of the USNM are not well enough preserved that would provide directional cues. Thus, a middle for the state of this feature to be determined. Therefore,

This content downloaded from 131.204.154.192 on Thu, 08 Apr 2021 19:22:22 UTC All use subject to https://about.jstor.org/terms LANCASTER--MIDDLE EAR OF THE ARCHAEOCETI 125 TABLE 2. Specific gravity of cetacean auditory ossicles.

Malleus Incus Stapes Basilosaurus cetoides (Archaeoceti) LSUMG V1 2.89 2.89 2.86 Zygorhiza kochii (Archaeoceti) AUMP 2368 2.90 LSUMG V160A 2.89 Kentriodon pernix (Odontoceti) USNM 8060 2.85 2.84 Globicephala melas (Odontoceti) LSUMZ 15912 2.72 (from Girard-Sauveur, 1969) 2.68 2.65 2.62 Delphinus delphis (Odontoceti) (from Girard-Sauveur, 1969) 2.67 2.64 2.58 Phocoena phocoena (Odontoceti) (from Girard-Sauveur, 1969) 2.67 2.66 2.63 Balaenoptera physalus (Mysticeti) (from Girard-Sauveur, 1969) 2.48 2.50 2.38

it would appear that a significant is relatively larger amountthan in most odontocetes of individual or mys- variation is possible in the ticetes, morphology acts as a buttress for the of body the of the bullarmalleus articulations. Despite the as wellpotential as for the processus of variabilitygracilis. The footplate forof these characters in the Basilosauridae, the group is the stapes is relatively thicker than in terrestrial mam- clearly derived over Pakicetus inachus in that the ar- mals (based on a comparison with Doran, 1878), in- ticulating areas are smaller and fewer in number. No dicating a strong annular ligament (a further indication trace of fusion exists regardless of which bones form of increased stiffness, Fleischer, 1978). The congruent the articulation. The opposing articular surfaces were articular surfaces between the incus and malleus are probably separated by a cartilaginous pad. The pos- well developed in the form typical of the Cetacea, in- terior pedicle of Z. kochii (AUMP 2368) is attached suring an interlocking fit. All of these features contrib- to the posterior process of the periotic via two thin ute to an increase in stiffness, which indicates that the bony laminae. This feature is more consistent than the middle ear was developing the ability to transmit high- articulations of the anterior pedicle. frequency vibration. A feature of the cetacean middle ear considered to If the ears of the Archaeoceti developed in a fashion be unusual is the fusion of the malleus to the tympanic parallel to those of other obligately aquatic mammals, bulla. Doran (1878) and Fleischer (1978) point out thatwe would then expect to see an increase in specific this fusion, found in many taxa, is not unique to gravityce- of the ossicles corresponding to the increase in taceans. Doran (1878) and Ridewood (1922) discussed stiffness of the system. The specific gravity of each of the homologies of the processus gracilis, and consid- the ossicles studied was measured using the method of ered the two edges of this girder-like structure to be Parnell and Dreher (1963), which was modified slightly independently derived. The structure of the processus by Girard-Sauveur (1969), and the data are presented gracilis acts to increase the stiffness of the system as in Table 2. One would intuitively assume that the pro- discussed by Reysenbach de Haan (1957) and Fleischer cess of fossilization would alter the mineral compo- (1978). Stiffness is closely coupled to the density of the sition of the bones, and thereby their density as well. ossicles (Reysenbach de Haan, 1957; Parnell and Dreh- While the sample is quite small, the specific gravities er, 1963; Girard-Sauveur, 1969; Fleischer, 1978). of the archaeocete ossicles that were tested were found Natural frequency of vibration of the ossicles in- to be consistent after multiple determinations, showing creases with increased stiffness, and decreases with in- little variation either between species, or between dif- creased density (Reysenbach de Haan, 1957; Parnell ferent individuals of the same species. The archaeocete and Dreher, 1963; Girard-Sauveur, 1969; Fleischer, ossicles represent three individuals collected from three 1978). Excessively high density impairs the ability to widely separated localities, each with a different li- transmit high-frequency vibrations, however, a bal- thology and presumably different conditions of pres- ance between density and stiffness can tune the ossicu- ervation. Additionally, the non-auditory portions of lar chain to the optimum natural frequency range. This each specimen exhibit a great deal of variation in their feature of the cetacean middle ear is not a new dis- color, texture, and state of preservation. As a control, covery; it is discussed in detail by the above-named a malleus from Recent Globicephala melas (LSUMZ authors. However, this bears reiteration because the15912, collected from a stranding) was tested, and data compromise between density and stiffness had already from Girard-Sauveur (1969) are included for compar- begun in the Archaeoceti. The sigmoid process, which ative purposes. The specific gravity of the malleus of

This content downloaded from 131.204.154.192 on Thu, 08 Apr 2021 19:22:22 UTC All use subject to https://about.jstor.org/terms 126 JOURNAL OF VERTEBRATE PALEONTOLOGY, VOL. 10, NO. 1, 1990

LSUMZ 15912, determined to be 2.72, is el higher ancestral than therian middle ear proposed by Fleischer the figure of 2.68 reported for the malleus (1978) of this by thespecies following steps: 1) enlargement of the by Girard-Sauveur (1969), but is within tympanic the 0.5-1.5% bone into the expanded auditory bulla char- range ofintraspecific variation reported byacteristic that author.of the Cetacea, 2) reduction of the long rod- Further confirmation that the specific likegravity processes deter- of the ossicles, 3) expansion of the an- minations accurately reflect the state of terior the animalslimb of thein tympanic bone to form the sigmoid life is the relationship between the specific process, gravities 4) rotation of of the ossicular chain about the the stapes and the other ossicles of Basilosaurus physiologic ce-axis of rotation of the malleus-incus sys- toides. The slightly lower figure for the tem, stapes and as5) increasecom- in density of the auditory ossicles pared with the malleus and incus is consistent following with the trendthe of pachyostosis seen in other bones. trend reported by Girard-Sauveur (1969) Allfor of theseevery changes probably occurred simulta- species tested, regardless of its environment. neously, each affecting the others. The rotation, de- An increase in bone density, or pachyostosis, velopment ofhas the sigmoid process (and resultant an- been theorized to be an early phase of secondarygular amplification), ma- and the general stiffening of the rine adaptation, and is seen in several taxa ossicular (Meister, chain may have lagged slightly behind the 1962). This phenomenon is clearly present increase in penguins in ossicular density, in somewhat of a cause and sirenians and in the case of the Archaeoceti is seen and effect relationship. In turn, the enlargement of the as thick-walled limb bones and ribs with little med- sigmoid process and reduction of the manubrium con- ullary cavity. As the Cetacea became more highly tributed to the development of rotation and the elon- adapted to the marine environment, this trend re- gation of the tympanic conus. It can be seen, therefore, versed itself such that average bone density of modern that although the changes that took place can be iden- cetaceans is lower than that of humans (Felts, 1966). tified separately, each of them is related to the others This trend in the secondary adaptation of terrestrial such that their individual contributions to the system to the marine environment, coupled with in a functional sense cannot be separated or individ- adaptations that aid in the utilization of underwater ually defined. sound, appears to be an important factor affecting the The middle ears of extant odontocetes show few evolution of the middle ear of the Archaeoceti. modifications over the system developed by the Ar- Returning to the relationship between density andchaeoceti in the Eocene. These adaptations improved stiffness of the ossicular chain, it does not seem likely the efficiency of sound transmission to the inner ear that the tympano-periotic complex would be excluded of early cetaceans, thereby laying a foundation for the from the pachyostosis seen in the limb bones, ribs, developmentand of echolocation. other bones of the Archaeoceti and other taxa. If the density of these bones increased along with the rest of ACKNOWLEDGMENTS the skeleton, then the middle ear would have to become I would like to thank Daniel Womochel, James Do- stiffer in order to maintain physical properties suited bie, and Judith Schiebout for their help and discussion to high frequency sound reception. This would explain during the development of this study; and Daryl the exceptionally high density of the auditory ossicles Domning, Richard Lambertsen, O. W. Henson, Jr., in archaeocetes and the development of a high degree and Douglas Lay for critical reviews of the manuscript. of stiffness in the ossicular chain. With the high level For help in locating obscure references, I thank Alta of stiffness and angular amplification system already Copeland. The following persons helped by loaning present in the ossicular chain, the Odontoceti had only comparative material: Mark Hafner, Robert Purdy, to decrease the density of the ossicles and modify the Earl Manning, James Dobie, and Gorden Bell. Ray- dimensions and angles to tune the system for higher mond Hintz and Roger Reep helped in the develop- frequencies. The slightly lower specific gravity of the ment of the mechanical amplification model. I received malleus and incus in Kentriodon pernix (a Miocene assistance in the ossicular density determination from delphinoid) could illustrate the beginnings of a trend Vern Winston and Patricia Klahr, was helped with the toward the tuning of the ossicular chain to high fre- illustrations by Jackie Murray, and was helped in the quencies in odontocetes through reduction of ossicular translation of references by Jane Carson and Arthur density. This idea is supported by the specific gravity Dolsen. Thanks go to Michael Baccala for his help with of the ossicles in the modern Odontoceti, which ranges the manuscript. from 2.58 to 2.68 (Girard-Sauveur, 1969). The ossicu- lar specific gravity of more fossil odontocetes will have to be determined in order to test this hypothesis. LITERATURE CITED

Doran, A. H. G. 1878. Morphology of the mammalian SUMMARY AND CONCLUSIONS ossicula auditus. Transactions, Linnean Society of Lon- don, Second Series-Zoology 1:371-497. The auditory ossicular chain of archaeocete ceta- Felts, W. J. L. 1966. Some functional and structural char- ceans is a highly derived system adapted to the trans- acteristics of cetacean flippers and flukes; pp. 255-276 mission of underwater sound to the inner ear. The in K. S. Norris (ed.), , , and Porpoises. morphology of this system can be derived from a mod- University of California Press, Berkeley.

This content downloaded from 131.204.154.192 on Thu, 08 Apr 2021 19:22:22 UTC All use subject to https://about.jstor.org/terms LANCASTER--MIDDLE EAR OF THE ARCHAEOCETI 127 Fleischer, G. 1973. Structural analysis of the tympanicum Calvert Cliffs, Maryland. Proceedings, United States Na- complex in the bottle-nosed dolphin (Tursiops trunca- tional Museum 107:279-337. tus). Journal of Auditory Research 13:178-190. 1968. Fossil marine mammals from the Miocene 1978. Evolutionary principles of the mammalian Calvert Formation of Maryland and Virginia. Bulletin, middle ear. Advances in Anatomy, Embryology, and United States National Museum 247:103-201. Cell Biology 55:1-70. - 1969. Cetothere skeletons from the Miocene Chop- Fordyce, R. E. 1983. Rhabdosteid dolphins (Mammalia: tank Formation of Maryland and Virginia. Bulletin, Cetacea) from the middle Miocene Lake Frome area, United States National Museum 294:1-41. South Australia. Alcheringa 7:27-40. Lancaster, W. C. 1982. A morphological and paleoecolog- Fraser, F. C., and P. E. Purves. 1960a. Anatomy and func- ical analysis of the Archaeoceti of Montgomery Landing, tion of the cetacean ear. Proceedings, Royal Society of Louisiana. M.S. thesis, Louisiana State University, Bat- London 152b:62-77. on Rouge, Louisiana, 151 pp. - and - 1960b. Hearing in cetaceans. Bulletin, Meister, W. 1962. Histological structure of the long bones British Museum (Natural History) Zoology 7:1-140. of penguins. Anatomical Record 143:377-388. Gingerich, P. D., and D. E. Russell. 1981. Pakicetus ina- Moore, W. J. 1981. The Mammalian Skull. Cambridge chus, a new archaeocete (Mammalia: Cetacea) from the University Press, Cambridge, 369 pp. early-middle Eocene Kuldana Formation of Kohat (Pa- Novacek, M. J. 1977. Aspects of the problem of variation, kistan). Contributions from the Museum of Paleontol- origin and evolution of the eutherian auditory bulla. ogy, The University of Michigan 25:235-246. Review 7:131-149. , N. A. Wells, D. E. Russell, and S. M. Ibrahim Shah. Parnell, J. E., and J. J. Dreher. 1963. Estimates of auditory 1983. Origin of whales in epicontinental remnant seas: frequency response limits as a function of mammalian new evidence from the early Eocene of Pakistan. Science ossicular density. Report No. 17080, Lockheed Califor- 220:403-406. nia Co., P.O. Box 551, Burbank, CA 91520. Girard-Sauveur, D. 1969. Recherches biophysiques Pompeckj, sur les J. F. 1922. Das Ohrskelett von Zeuglodon. osselets des Cetaces. Mammalia 33:285-340. Senckenbergiana (Frankfurt) 4:43-100. Hawkins, A. D., and A. A. Myrberg, Jr. 1983. Hearing Purves, and P. E., and G. E. Pilleri. 1983. Echolocation in Whales sound communication under water; pp. 347-429 in B. and Dolphins. Academic Press, New York, 261 pp. Lewis (ed.), Bioacoustics, a Comparative Approach. Ac- Reysenbach de Haan, F. W. 1957. Hearing in whales. Acta ademic Press, London. Otolaryngologica: Supplementum 134:1-114. Kasuya, T. 1973. Systematic consideration of recent toothed - 1960. Some aspects of mammalian hearing under whales based on the morphology of tympano-periotic water. Proceedings, Royal Society of London 152b:54- bone. Scientific Reports, Whales Research Institute 25: 62. 1-103. Ridewood, W. G. 1922. Observations on the skull in foetal Kellogg, R. 1924. Description of a new species of - specimens of whales of the genera Megaptera and Ba- bone whale from the Calvert Cliffs, Maryland. Proceed- laenoptera. Philosophical Transactions, Royal Society ings, United States National Museum 63:1-14. of London 21 1b:209-272. 1927. Kentriodon pernix, a Miocene porpoise from Wilson, L. E. 1972. A delphinid (Mammalia: Cetacea) from Maryland. Proceedings, United States National Mu- the Miocene of Palos Verdes Hills, California. Univer- seum 69:1-55. sity of California Publications in Geological Sciences 1936. A Review of the Archaeoceti. Carnegie In- 103:1-34. stitute of Washington Publication 482, Washington, D.C., 366 pp. 1957. Two additional Miocene porpoises from the Received 29 August 1988; accepted 14 June 1989.

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