Tag: morphometrics

In February this year I started my PhD thesis. As with all PhD’s there are various milestones where you must hand in some sort of report to make sure you aren’t just sitting around all day and drinking beer (tempting though it is). This week I finally completed my 3 month report (only 2 months late) and now I can finally worry about doing some research. This post came about after a brief twitter conversation with fellow PhD student Jon Tennant (aka @Protohedgehog, check out his awesome blog here) from Imperial College London, who suggested doing what he did and blogging his 3 month report so everyone can see what I’m getting up to (for better or for worse). So here you go! It’s a little bit drier than my usual blogging style and has a bit more jargon, but have at it anyway! If there’s anything you want to know more about drop me an email (see about section at top of the blog page for the email address).

Proposed thesis title

Investigations into hearing in toothed mysticetes (Cetacea: Mammalia) via studies of the periotic (petrosal) and mandible.

Introduction

This thesis will investigate the auditory structures of the inner ear and mandible shape in toothed mysticetes. Whilst at first, these two subjects may at first appear to be disparate fields, consider that in modern cetaceans, auditory cues are the primary method by which they locate their prey, their olfactory abilities being the poorest of any mammal group (Pihlström 2008) and vision being limited due to low light levels in water at depth. Furthermore, in odontocetes (and most archaeocetes except for pakicetids) sound is/was received via the jawbone. Thus, the structure of the jaw must adequately serve the demands of two processes, namely sound reception and prey capture/feeding.

Whilst these aspects have been investigated to varying extent in archaeocetes, odontocetes and extant mysticetes (e.g. Nummela et al. 2004, 2007, Werth 2006, Yamato et al. 2012, Pyenson et al. 2013), there has been insufficient time devoted to them in toothed mysticetes. Toothed mysticetes are however, of particular interest in these aspects for several reasons. The transition from teeth to baleen is one of the key innovations in cetacean evolution, requiring major morphological changes in the skull and perhaps even led to the shift towards enormous body size (Werth 2000, Fitzgerald 2006, Slater et al. 2010). Some species of toothed mysticetes are reported to have possessed “proto-baleen” (Deméré & Berta 2008, Deméré et al. 2008, Berta 2012), but this is based on the inference of homologous structures in the palate and remains to be corroborated by the presence of fossilised baleen in association with one of these toothed mysticete taxa. Yet it is crucial to remember at this point that these toothed mysticetes were not just transitional species, an intermediate point on the path to baleen; rather they were successfully making a living and had carved their own ecological niche. This is the catalyst for this thesis. I plan to investigate how these animals were making a living, what sounds they could hear and how it affected how they fed. Modern mysticetes have low frequency hearing, very different to the high frequency, echolocating odontocetes. What is unknown is what frequencies the toothed mysticetes were capable of hearing. Did they share the low frequency hearing found in modern mysticetes or did the shift to lower frequencies and the attendant morphological changes of the inner ear coincide with the evolution of baleen? The hearing capabilities of the toothed mysticetes will also add further inferential morphological data to their hypothesised feeding ecologies. I plan to test these hypotheses in quantitative manner for the first time (in toothed mysticetes) using morphometric and finite element analyses (FEA). This will be set out in more detail in the research methodology section

Below I briefly review the evolution of early cetaceans and the mysticetes. I then summarise the current knowledge on the evolution of cetacean hearing and mandible shape before outlining my intended research methodology and estimated timeline for the project.

Cetacean Origins: The Archaeocetes

Cetaceans (whales and dolphins) are a poster child of evolution, their origins from land mammals and transition to the ocean giants of today being one of the most extraordinary tales of adaptation. Yet this has not always been the case, their extremely derived morphology causing earlier workers much frustration in their efforts to classify the “most peculiar and aberrant of mammals” (Simpson 1945), with the key revelations of their ancestry not coming to light until the past few decades (Uhen 2010). Now, the numerous fossils documenting almost every stage of this group’s evolution make it one of the most valuable case studies in macroevolution.

Cetaceans are first found in the fossil record in the Early Eocene of Pakistan; these animals were semiaquatic “walking whales” belonging to the Pakicetidae and Ambulocetidae (Gingerich et al. 1983, Thewissen et al. 1996, Madar 2007). They still retained the ability to move around on land although their skeleton was denser than their wholly terrestrial relatives (Madar 2007). By the Middle Eocene, the Remingtonocetidae and Protocetidae had appeared (Kumar & Sahni 1986, Hulbert Jr 1998, Gingerich et al. 2001, 2009, Bajpai et al. 2011) and evolved into nearshore marine (Gingerich et al. 1995, Clementz et al. 2006) animals that possessed a crocodile-like morphology, with long bodies, short limbs and a narrow, elongated rostrum (Thewissen & Bajpai 2009). The protocetids rapidly diversified and spread across the globe, reaching as far as North and South America (Hulbert et al. 1998, Uhen et al. 2011). The transition to an obligately aquatic lifestyle was completed with the appearance of the basilosaurids in the late Middle Eocene. Their remains are known from every continent except for Antarctica (Uhen 2009). Features that indicate a fully marine lifestyle include: acoustic isolation of the auditory structures within the skull via enlarged sinuses; shortened neck; forelimb dorsoventrally flattened to form a flipper; greatly reduced hind limbs that were incapable of supporting the animal’s weight on land and the presence of a tail fluke (Gingerich et al. 1990, Uhen 1998, 2004, 2009). The basilosaurids (and especially the Dorudontinae) are thought to have given rise to Neoceti (the group comprised of Mysticeti and Odontoceti) (Uhen 2004).

The Mysticetes

Modern mysticetes, also known as the baleen whales due to the keratinous plates attached to the gum of the upper jaw that are used to sieve small marine organisms from seawater, are some of the most awe-inspiring creatures ever to grace this planet. They include the largest animal to have ever evolved, the blue whale (Balaenoptera musculus), which can reach lengths of 30 m and weigh more than 170 tons (Bannister 2009). There are four extant mysticete families: Balaenidae (right, bowhead whales); Balaenopteridae (rorquals); Eschrichtiidae (gray whale) and the enigmatic pygmy right whale (Caperea marginata) which has traditionally been placed in its own family, the Neobalaenidae, but a recent analysis by Fordyce & Marx (2012) found it to belong to the Cetotheriidae, making it the sole living taxon of this family.

Whilst all living mysticetes possess baleen, not all fossil mysticetes share this feature, with early taxa possessing teeth instead. The transition from these toothed mysticetes into the baleen bearing behemoths of today is one area in cetacean evolution that is still subject to vigorous debate and research (Deméré et al. 2008, Esperante et al. 2008, Fitzgerald 2012, Armfield et al. 2013). There are three families of toothed mysticete, the Llanocetidae, Mammalodontidae and the Aetiocetidae, in addition to the still undescribed “archaeomysticete” taxa from the Oligocene of South Carolina (Barnes & Sanders 1996a, b). The Llanocetidae is represented by Llanocetus denticrenatus, from Seymour Island, Antarctica. The holotype consists of a partial mandible and an endocranial cast (Mitchell 1989), although an almost compete skull and partial skeleton, believed to be from the same individual is currently under study by Ewan Fordyce (Berta & Deméré 2009, Fitzgerald 2010). Llanocetus represents the oldest known mysticete and has been interpreted as a filter feeder that is intermediate in form between basilosaurids and crown mysticetes (Fordyce 2003), with the large diastemata between its teeth allowing the teeth to act as a food sieve (Fordyce 2003), or even potentially being filled by baleen (Berta 2012). The mammalodontids consist of the taxa Mammalodon colliveri and Janjucetus hunderi from the Late Oligocene of Australia (Pritchard 1939, Fitzgerald 2006, 2010). These species were small-bodied with short rostra and large orbits. They have been most recently interpreted as a suction-feeder and a macrophagous predator respectively (Fitzgerald 2006, 2010). The aetiocetids were the most numerous toothed mysticete family with a total of five genera. They too were small bodied (estimated length of 2-3 m) but differed from the mammalodontids in that they had a relatively elongate, broad rostrum and mandible that bowed outwards, similar to modern mysticetes (Berta & Deméré 2009). One species of aetiocetid (Aetiocetus weltoni) reportedly possesses palatal foramina and sulci that may homologous with similar structures found in modern mysticetes. These structures house the blood vessels that supply the epithelia from which baleen develops, meaning that it too may have possessed baleen, if even in only an incipient form (Deméré & Berta 2008). The earliest edentulous (toothless) mysticetes are the eomysticetids, known from North America, New Zealand and Mexico (Sanders & Barnes 2002, Berta & Deméré 2009). However the majority of these specimens are yet to be described, therefore the full diversity of this group remains unknown.

 The Evolution of Cetacean Hearing

As cetaceans evolved from wholly terrestrial animals into obligately marine mammals during the course of the Eocene, their organ systems underwent major restructuring and modification. Perhaps no other organ system underwent as profound and wholesale a series of changes as that of the ear region which had to evolve the ability to detect sound in a much denser medium.

The ancestors of cetaceans possessed the generalised form of the majority of land mammals. Sound is transmitted via an air-filled external auditory meatus to the tympanic membrane, where the differential pressures cause it to vibrate and pass the sound onto the three middle ear bones, the malleus, incus and stapes. These bones serve to amplify the sound pressure by decreasing the area through which the sound is passed (Nummela et al. 2007). The stapes, in turn, transmits the sound to the fluid-filled cochlea via a piston-like action (Nummela et al. 2004). The vibrations of the cochlear fluid (perilymph) are transmitted to the hair cells of the cochlea and converted into a neural impulse and sent to the brain. This pathway is not effective underwater however as the external auditory meatus becomes filled with water, reducing the pressure differential at the tympanic membrane and therefore greatly diminishing its ability to transmit sounds to the middle ear bones. Furthermore, when underwater, the similar density of animal tissue to water means that sounds will simply travel through the tissues and bones, a phenomenon known as bone conduction (Nummela et al. 2007) and will lessen the animal’s ability to distinguish which direction the sound originally came from.

The earliest whales, the pakicetids, displayed very few adaptations for underwater hearing. They possessed a thickened tympanic bone that lacked a rostromedial connection to the periotic, allowing the tympanic to vibrate independently of the periotic (Nummela et al. 2004). This enhanced their ability to use bone conduction, which would have been the method by which sound was transmitted when underwater, although directional hearing underwater would still have been poor (Nummela et al. 2004, 2007). In the ambulocetids, we see the first use of the mandible and the development of the tympanic plate for use in a sound conduction pathway in cetaceans. These animals possessed a large mandibular foramen, which would have housed a mandibular fat pad. It has been hypothesised that Ambulocetus may have used bone conduction on land, by placing its lower jaw to the ground and hearing the vibrations, in a similar manner to some extant crocodiles (Thewissen et al. 1996). The remingtonocetids and protocetids also possessed large mandibular foramen, but the lateral wall of the mandible is thinner than that seen in ambulocetids, meaning that the sensitivity of their underwater hearing had increased. The land mammal hearing mechanism is still present, indicating that these animals could also still hear in air, albeit poorly. The contact between the tympanic and periotic is also further reduced and the morphology of the middle ear ossicles are beginning to approach that of modern cetaceans (e.g. the malleus now lacks a manubrium for the attachment of the tympanic membrane (Nummela et al. 2007). In protocetids, the periotic has become more detached from the skull via the development of air sinuses, allowing for improved directional underwater hearing (Nummela et al. 2007). In basilosaurids, the ear is functionally the same as modern cetaceans, with the lateral wall of the mandible almost as thin as that in odontocetes, the middle ear bones are similar to those of modern delphinids and the petrotympanic complex is acoustically isolated via air sinuses, implying that underwater hearing was now the primary function of the air. Despite this the basilosaurids still retained an external auditory meatus, although it was most likely hardly ever used (Nummela et al. 2007). This transition from an exclusively terrestrial hearing system to a sensitive underwater hearing system took place in less than 10 million years (Nummela et al. 2004).

The focus of research on the hearing of modern whales has been toothed echolocating whales (odontocetes). The hearing of mysticetes, especially the sound reception pathway, on the other hand, remains virtually unknown.  A recent study by Yamato et al. (2012) proposed a potential sound reception pathway via fat body that contacts the petrotympanic complex laterally in the minke whale (Balaenoptera acutorostrata). The sound reception in modern mysticetes is patently different to that in odontocetes as the periotic is attached to the skull via the squamosal and exoccipital bones, whereas it is acoustically isolated in odontocetes. The external auditory meatus is vestigial, and remains debatable whether it is still functional (Yamato et al. 2012).

The Evolution of Cetacean Mandible Shape

The evolution of the cetacean mandible represents the incorporation of this element into the auditory system as the group became progressively more aquatic. The resulting changes in mandibular shape are the product of a trade-off between the animal’s joint need to use the mandible to secure and manipulate prey as well as receiving the sounds of its environment.

The pakicetids, as noted above, did not possess the ability to hear underwater and this is reflected by the fact that they retained the land mammal morphology of the mandible, with a small mandibular foramen (Nummela et al. 2004, 2007). Ambulocetids show the first sign of the development of underwater hearing in cetaceans, possessing a slightly enlarged mandibular foramen, although the lateral wall of the mandible is still relatively thick, meaning that higher frequency sound would be unable to pass through (Nummela et al. 2007). Remingtonocetids and protocetids on the other hand, have evolved a large mandibular foramen, indicating the presence of the mandibular fat pad. The lateral wall of the mandible also became thinner, implying an improved ability to hear underwater. In basilosaurids, both the size of the mandibular foramen and the thickness of the lateral wall approach those seen in odontocetes.

In the toothed mysticetes however, we see further changes to the shape of the mandible. The mandibular symphysis, which in all archaeocetes had been long (Fitzgerald 2012), is shortened. This symphysis also underwent further evolution within the toothed mysticetes. In Janjucetus the symphysis is rigid and sutured, but in the aetiocetids Chonecetus and Aetiocetus the symphysis is elastic and smooth, allowing the mandibles to rotate which is thought to be an adaptation to bulk feeding. The mandibular coronoid process is also relatively larger in the mammalodontids compared to the aetiocetids, although the coronoid process is still relatively larger compared to later diverging mysticetes such as the eomysticetids. The mandibular foramen is large in all toothed mysticetes, suggesting that this method sound reception pathway was still employed by the toothed mysticetes. Aetiocetid mandibles also differ from mammalodontid mandibles in that they are more tubular (Fitzgerald 2010), whereas mammalodontid mandibles more closely approach the shape of archaeocete mandibles.

Research Methodology

This thesis aims to investigate the internal structure of the periotic in toothed mysticetes and attempt to discover any intragroup differences by comparing their morphological features. Furthermore, by comparing these structures to that of living taxa whom I plan to use as proxies, I hope to be able to infer what frequency range toothed mysticete hearing fell into. I then plan to study mandible shape in the group in order to determine how the mandibles of the mammalodontids and aetiocetids differ in morphospace relative to other marine tetrapods and also how they cope with applied loads and relate this to any differences in hearing abilities and hypothesised feeding ecologies.

This conceptual framework provides a foundation for the following core questions of the thesis:

• What were the hearing capabilities of the mammalodontids?
• What were the hearing capabilities of the aetiocetids?
• Do toothed mysticete ears scale to body size?
• Did the shift to lower frequency hearing in mysticetes occur before or after the acquisition of a bulk filter feeding lifestyle?
• Where does toothed mysticete mandible shape fall in morphospace relative to other marine tetrapods?
• Do mammalodontids and aetiocetids differ in their ability to cope with applied loads to their mandibles?
• Do the differences in hearing (if any) between mammalodontids and aetiocetids correlate with differences in mandible shape and ability to cope with applied loads?
• Does this relate to hypothesised feeding abilities of the clades?

These core questions will test the following hypotheses:

• That mammalodontids required the ability to hear higher frequencies than that found in extant mysticetes.
• That aetiocetids possessed the ability to hear lower frequencies than the mammalodontids but could still hear higher frequencies than extant mysticetes.
• That the petrotympanic complex in toothed mysticetes will scale isometrically with body size.
•  That toothed mysticete mandible shape will fall somewhere in-between that of extant mysticetes and odontocetes in morphospace in a morphometric analysis.
• That the mandibles of mammalodontids (in particular Janjucetus) will be better at coping with shaking and twisting loads than the mandibles of aetiocetids.

These hypotheses will be tested using a variety of methods and technologies. Earlier studies looking at internal structure of the periotic did so using the destructive method of thin sectioning (e.g. Kasuya 1973, Fleischer 1976). This thesis however shall employ the non-destructive method of CT scanning. Extant taxa will be scanned first to establish a proxy for various frequency ranges. Then the fossil taxa will also be scanned and compared to the living taxa to infer hearing capabilities. Whilst I will also research the possibility of defining new characteristics to use, the following list of morphological characters of the petrotympanic complex, both qualitative and quantitative, will be used to help determine hearing capacities in the fossil taxa:

• Mass of the tympanic, periotic, malleus, incus and stapes (where available).
• Volume of the tympanic.
• Area of the tympanic plate and oval window.
• Thickness of tympanic plate.
• Density of malleus, incus and stapes (where available).
• Radii ratio.

–          This is the ratio of the radius of the cochlea at its base to the radius of the cochlea at its apex. This ratio is strongly correlated with low frequency hearing limits (Manoussaki et al. 2008).

• Position of areas of high cochlear foramina density.

–          The cochlear foramina housed the cochlear nerve fibres that transmitted the converted sound waves to the brain. Areas of high foramina density therefore represent areas of high nerve density. The position of these high density areas will therefore indicate what frequencies the animal was sensitive to as lower frequency sounds tend to travel further along the cochlear canal due to their longer wavelengths, whereas high frequency sounds will attenuate rapidly and be detected near the base of the cochlear canal (Geisler & Luo 1996).

• Diameter of spiral ganglionic canal.

–          This feature is related to the previous one as Geisler & Luo (1996) found that the highest diameter of the spiral ganglionic canal coincided with the position of the area of high foramina density in the fossil mysticete Herpetocetus.

• Width of the laminar gap.

–          The width of the gap between the two spiral lamina of the cochlea roughly approximates the width of the basilar membrane. A wider laminar gap at the same point in two different cochleae can indicate better sensitivity to lower frequencies. Ketten (2000) however cautions against using the laminar gap as synonymous with basilar membrane width, noting that membrane width can be overestimated by up to 110% in modern mysticetes. However, as a comparison between two cochleae the width of the gap of one relative to the other may indicate sensitivity to higher or lower frequencies.

•     Extent of inner and outer lamina.

–          The length of the outer bony lamina of the cochlea can be used a generic indicator of high or low frequency hearing. In odontocetes the outer lamina is present for a greater length of the cochlea, whereas in mysticetes it is reduced or absent (Ketten 2000). This is believed to affect the stiffness of the basilar membrane, the stiff, rigid membrane of odontocetes being better at detecting high frequencies than the more flexible membrane in modern mysticetes.

• Basal ratio.

–          This is the axial height of the cochlea divided by the basal diameter of the cochlea. This is found to be generally negatively proportional to frequency (Ketten & Wartzok 1990). Geisler & Luo (1996) note that values for the basal ratio may vary across different studies, depending on how the diameter is measured.

• Axial pitch.

–          This is the axial height of the cochlea divided by the number of turns of the cochlea. This is found to be generally negatively proportional to frequency.

• Ratio of scala tympani to scala vestibuli.

–          The cochlea is divided into three chambers by membranes. These are the scala tympani, scala vestibule and scala media. This ratio was proposed by Fleischer (1976) as method for estimating frequency ranges where a large scala tympani relative to a small scala vestibuli implies high frequency hearing. Geisler & Luo (1996) found however that this condition occurs in mysticetes also and stated that it remains to be seen how effective this ratio is in distinguishing between low and high frequency hearing. This feature may or may not yet be used in this thesis.

The morphometric analysis section of this thesis will take a landmark based approach. This will involve obtaining scan data on both extant and fossil specimens. These will be gathered by myself from Museum Victoria specimens, specimens from other museum collections (via travelling to them or engaging the services of researches at those institutions) and scans already collected by colleagues. The specimens will include as wide an array of marine tetrapods (e.g. mysticetes, odontocetes, and pinnipeds) as possible to frame the following FEA study in a broader context. Using this dataset, landmarks on each specimen will be selected using an appropriate software package (e.g. Landmark (O’Higgins & Jones 2006)). Exact landmarks used in the morphometric analysis will be determined at a later point as homology of locations and functional significance must be ensured; however, the following list gives an example of some that will likely be employed:

• Anterior of jaw (origin) – midline.
• Posterior apex of mandible – left and right.
• Posterior apex of symphysis – midline.
• Dorsal apex of coronoid process – left and right.
• Dorsal apex of symphysis at widest point – midline.
• Ventral apex of symphysis at widest point – midline.

Once landmarks have been selected the data will be analyses using morphometric analysis software (e.g. Morphologika). Statistical techniques will be employed to eliminate as many confounding factors (e.g. size) as possible, before a multivariate (principle component analysis will be run.

The morphometric analysis component serves to frame the FEA in a broad phylogenetic context. In order to execute the FEA, scan data of toothed mysticete mandibles will used to create meshes for each taxon. Pending any new data on the effectiveness of low versus high order elements to construct meshes, low order elements will be used for the FEA. In order to ensure that results of the FEA are as consistent as possible with reality, boundary conditions will be set to constrain the model in space (i.e. simulations of muscle attachments, force vectors, etc.). FEA will be undertaken using specific software such as Strand7. Mandible models will be subjected to loading in various directions to compare effects of different hypothesised feeding styles on strain patterns. Statistical analysis of strain values will be undertaken using R.

Thesis Structure & Estimated Timeline

The following sections will form chapter/papers in my thesis. This is a preliminary structure only as these sections may yet be separated or combined into papers as my research progresses:

• Review of petrotympanic morphology of toothed mysticetes.

–          This review paper will complement other works such as Ekdale et al. (2011) and Luo & Gingerich (1999) that have detailed the morphology of the petrotympanic complex in modern mysticetes and archaeocetes respectively.

• Study of mammalodontid hearing.
• Study of aetiocetid hearing.
• Comparison of toothed mysticete hearing, both intragroup and against extant cetaceans.
• Toothed mysticete scaling study.

–          This study may yet be removed from the thesis as I have concerns over the availability of middle ear ossicle data from fossil taxa, preventing all of the necessary data from being compiled. This will be decided upon at a future date and other ideas may be pursued instead.

• Morphometric analysis of marine tetrapod mandible shape.
• FEA of toothed mysticete mandibles.

References

Armfield, B.A., Zheng, Z., Bajpai, S., Vinyard, C.J. & Thewissen, J.G.M., 2013. Development and evolution of the unique cetacean dentition. PeerJ 1:e24 http://dx.doi.org/10.7717/peerj.24.

Barnes, L.G. & Sanders, A.E., 1996a. The transition from archaeocetes to mysticetes: Late Oligocene toothed mysticetes from near Charleston, South Carolina. Paleontological Society Special Publication 8, 24.

Barnes, L.G. & Sanders, A.E., 1996b. The transition from Archaeoceti to Mysticeti: Late Oligocene toothed mysticetes from South Carolina, U.S.A. Journal of Vertebrate Paleontology 16, 21A.

Berta, A., 2012. Return to the Sea. The life and evolutionary times of marine mammals. University of California Press, Berkeley, 205 pp.

Berta, A. & Deméré, T.A., 2009. Mysticetes, Evolution. In Perrin, W.F., Würsig, B. & Thewissen, J.G.M., eds, Encyclopedia of Marine Mammals 2^nd edition. Academic Press, Sydney, 749–753.

Bannister, J.L., 2009. Baleen Whales (Mysticetes). In Perrin, W.F., Würsig, B. & Thewissen, J.G.M., eds, Encyclopedia of Marine Mammals 2^nd edition. Academic Press, Sydney, 80–89.

Clementz, M.T., Goswami, A., Gingerich, P.D. & Koch P.L., 2006. Isotopic records from early whales and sea cows: contrasting patterns of ecological transition. Journal of Vertebrate Paleontology 26, 355–70.

Deméré, T.A., Berta, A., 2008. Skull anatomy of the Oligocene toothed mysticete Aetiocetus weltoni (Mammalia; Cetacea): implications for mysticete evolution and functional anatomy. Zoological Journal of the Linnean Society of London 154, 302–352.

Deméré, T.A., McGowen, M.R., Berta, A., Gatesy, J., 2008. Morphological and molecular evidence for a stepwise evolutionary transition from teeth to baleen in mysticete whales. Systematic Biology 57, 15–37.

Ekdale, E.G., Berta, A. & Deméré, T.A., 2011. The Comparative Osteology of the Petrotympanic Complex (Ear Region) of Extant Baleen Whales (Cetacea: Mysticeti). PLoS ONE 6(6): e21311. doi:10.1371/journal.pone.0021311 http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0021311.

Esperante, R., Brand, L.R., Nick, K.E., Poma, O. & Urbina M., 2008. Exceptional occurrence of fossil baleen in shallow marine sediments of the Neogene Pisco Formation, Southern Peru. Palaeogeography, Palaeoclimatology, Palaeoecology 257, 344–60.

Fitzgerald, E.M.G., 2006. A bizarre new toothed mysticete (Cetacea) from Australia and the early evolution of baleen whales. Proceedings of the Royal Society B: Biological Sciences 273, 2955–2963.

Fitzgerald, E.M.G., 2010. The morphology and systematics of Mammalodon colliveri (Cetacea: Mysticeti), a toothed mysticete from the Oligocene of Australia. Zoological Journal of the Linnean Society of London 158, 367–476.

Fitzgerald, E.M.G., 2012. Archaeocete-like jaws in a baleen whale. Biology Letters 8, 94–96.

Fleischer, G., 1976. Hearing in extinct cetaceans as determined by cochlear structure. Journal of Paleontology 50, 133–152.

Fordyce, R.E., 2003. Early crown-group Cetacea in the southern ocean: the toothed archaic mysticete Llanocetus. Journal of Vertebrate Paleontology 23, 50A.

Fordyce, R.E. & Marx, F.G., 2012. The pygmy right whale Caperea marginata: the last of the cetotheres. Proceedings of the Royal Society B: Biological Sciences 280, 20122645. http://dx.doi.org/10.1098/rspb.2012.2645.

Geisler, J.H. & Luo, Z.X., 1996. The petrosal and inner ear of Herpetocetus sp. (Mammalia: Cetacea) and their implications for the phylogeny of hearing of archaic mysticetes. Journal of Paleontology 70, 1045–1066.

Gingerich, P.D., Wells, N., Russell, D. & Shah, S.M., 1983. Origin of whales in epicontinental remnant seas: new evidence from the early Eocene of Pakistan. Science 220, 403–406.

Gingerich, P.D., ul-Haq, M., von Koenigswald, W., Sanders, W.J., Smith, B.H. & Zalmout, E.S., 1990. Hindlimbs of Eocene Basilosaurus: evidence of feet in whales. Science 249, 154–157.

Gingerich, P.D., Arif, M. & Clyde, W.C., 1995. New archaeocetes (Mammalia, Cetacea) from the middle Eocene Domanda Formation of the Sulaiman Range, Punjab (Pakistan). Contributions of the Museum Paleontology of the University of Michigan 29, 291–330.

Gingerich, P.D., Haq, M.U., Zalmout, I.S., Khan, I.H., Malakani, M.S., 2001. Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 293, 2239–2242.

Gingerich, P.D., ul-Haq, M., von Koenigswald, W., Sanders, W.J., Smith, B.H., Zalmout, E.S., 2009. New protocetid whale from the middle Eocene of Pakistan: birth on land, precocial development, and sexual dimorphism. PLoS One 4, e4366. http://dx.doi.org/10.1371/journal.pone.0004366.

Hulbert Jr., R.C., 1998. Postcranial osteology of the North American middle Eocene protocetid Georgiacetus. In Thewissen, J.G.M., ed, The Emergence of Whales, Evolutionary Patterns in the Origin of Cetacea. Plenum Press, New York, 235–267.

Hulbert, R.C. Jr, Petkewich, R.M., Bishop, G.A., Bukry, D & Aleshire D.P., 1998. A new middle Eocene protocetid whale (Mammalia: Cetacea: Archaeoceti) and associated biota from Georgia. Journal of Paleontology 72, 907–27.

Kasuya, T., 1973. Systematic consideration of recent toothed whales based on morphology of tympano-periotic bone. The Scientific Reports of the Whale Research Institute (Tokyo) 25, 1–103.

Ketten, D.R., 2000. Cetacean ears. In Au, W.W.L., Popper, A.N., Fay, R.R., eds, Hearing by whales and dolphins. Springer-Verlag, New York, 43–108.

Kumar, K., Sahni, A., 1986. Remingtonocetus harudiensis, new combination, a middle Eocene archaeocete (Mammalia, Cetacea) from western Kutch, India. Journal of Vertebrate Paleontology 6, 326–349.

Luo, Z.X. & Gingerich, P.D., 1999. Terrestrial Mesonychia to aquatic Cetacea: transformation of the basicranium and evolution of hearing in whales. University of Michigan Papers on Paleontology 31, 1–98.

Madar, S.I., 2007. The postcranial skeleton of early Eocene pakicetid cetaceans. Journal of Paleontology 81, 176–200.

Manoussaki, D., Chadwick, R.S., Ketten, D.R., Arruda, J., Dimitriadis, E.K. & O’Malley, J.T., 2008. The influence of cochlear shape on low-frequency hearing. Proceedings of the National Academy of Sciences 105, 6162–6166.

Mitchell, E.D., 1989. A new cetacean from the late Eocene La Meseta Formation, Seymour Island, Antarctic Peninsula. Canadian Journal of Fisheries and Aquatic Sciences 46, 2219–2235.

Nummela, S., Thewissen, J.G.M., Bajpai, S., Hussain, S.T. & Kumar, K., 2004. Eocene evolution of whale hearing. Nature 430, 776–778.

Nummela, S., Thewissen, J.G.M., Bajpai, S., Hussain, T., Kumar, K., 2007. Sound transmission in archaic and modern whales: anatomical adaptations for underwater hearing. Anatomical Record 290, 716–733.

O’Higgins, P. & Jones, N., 2006. Tools for statistical shape analysis. Hull York Medical School, http://sites.google.com/site/hymsfme/resources.

Pihlström, H., 2008. Comparative anatomy and physiology of chemical senses in aquatic mammals. In, Thewissen, J.G.M. & Nummela, S., eds, Sensory Evolution on the Threshold: Adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, 95–109.

Pritchard, G.B., 1939. On the discovery of a fossil whale in the older tertiaries of Torquay, Victoria. Victorian Naturalist 55, 151–59.

Pyenson, N.D., Goldbogen, J.A. & Shadwick, R.E., 2013. Mandible allometry in extant and fossil Balaenopteridae (Cetacea: Mammalia): the largest vertebrate skeletal element and its role in rorqual lunge feeding. Biological Journal of the Linnean Society 108, 586–599.

Sanders, A. E. & Barnes, L.G., (2002). Paleontology of the Late Oligocene Ashley and Chandler Bridge Formations of South Carolina, 3: Eomysticetidae, a new family of primitive mysticetes (Mammalia: Cetacea). Smithsonian Contributions to Paleobiology 93, 313–356.

Simpson, G.G., 1945. The principles of classification and a classification of mammals. Bulletin of the American Museum of Natural History 85, 1–350.

Slater, G.J., Price, S.A., Santini, F. & Alfaro, M.E., 2010. Diversity versus disparity and the radiation of modern cetaceans. Proceedings of the Royal Society B: Biological Sciences 277, 3097–3104.

Thewissen, J.G.M. & Bajpai, S., 2009. New skeletal material of Andrewsiphius and Kutchicetus, two Eocene cetaceans from India. Journal of Paleontology 83, 635–63.

Thewissen, J.G.M., Madar, S.I. & Hussain, S.T., 1996. Ambulocetus natans, an Eocene cetacean (Mammalia) from Pakistan. Courier Forschungsinstitut Senckenberg 191, 1–86.

Uhen, M.D., 2004. Form, function, and anatomy of Dorudon atrox (Mammalia, Cetacea): an archaeocete from the middle to late Eocene of Egypt. University of Michigan Papers in Paleontology 34, 1–222.

Uhen, M.D., 2009. Basilosaurids. In Perrin, W.F., Würsig, B. & Thewissen, J.G.M., eds, Encyclopedia of Marine Mammals 2^nd edition. Academic Press, Sydney, 91–94.

Uhen, M.D., 2010. The origin(s) of whales. Annual Review of Earth and Planetary Sciences 38, 189–219.

Uhen, M.D., Pyenson, N.D., Devries, T.J., Urbina, M. & Renne, P.R., 2011. New Middle Eocene Whales From The Pisco Basin Of Peru. Journal of Paleontology, 85, 955–969.

Werth, A.J., 2000. Marine mammals. In, Schwenk, K., ed, Feeding: Form, Function and Evolution in Tetrapod Vertebrates. Academic Press, New York, 475–514.

Werth, A.J., 2006. Mandibular and dental variation and the evolution of suction feeding in Odontoceti. Journal of Mammalogy 87, 579–588.

Yamato, M., Ketten, D.R., Arruda, J., Cramer, S., Moore, K., 2012. The auditory anatomy of the minke whale (Balaenoptera acutorostrata): a potential fatty sound reception pathway in a baleen whale. Anatomical Record 295, 991–998.