Friday, May 19, 2023

Regarding A Fossil Collection: Post #2
Cetacean Middle Ear Fossils, Part 1

This is the second in a series of posts about a recently acquired collection of fossils.  Many of these fossils were collected at Plum Point, Maryland, along the Calvert Cliffs on the western shore of the Chesapeake Bay.  They possibly came from the Plum Point Member of the Calvert Formation which would make them roughly 17 to 14 million years old, an age range straddling the line between the lower and middle Miocene Epoch.  The first post described the collection in very general terms, bemoaning the original collector’s abysmal job of organizing and labeling the fossils, and explored the location where most of them were collected:  Plum Point.  I admit that I paid an inordinate amount of space in that post to the derivation of the name “Plum Point.”

Cetaceans are one of my intellectual “basins of attraction,” something to which I am inevitably drawn.  I find the story of their evolutionary trek from land back to the sea and the challenges that posed irresistible.  So, it’s been quite easy to devote time, energy, and blog space to this “new” collection because most of its readily identifiable specimens are two kinds of cetacean fossils – tympanic bullae and periotic bones, both of which are part of these mammals’ middle ears (more on these below).  Identifying these fossils as bones from cetacean middle ears is quite easy, understanding their function is not.

As an initial step in organizing the Plum Point collection, I transferred to a separate case (pictured below) all of these cetacean fossils that were clearly identified by the original collector as coming from Plum Point.

My objective with this present post is to put these fossils into several broader contexts:  (1) cetacean fossils from the Calvert Cliffs, (2) evolution of cetaceans in general, and (3) cetacean hearing with a focus on the middle ear.  I conclude with a brief display of several tympanic bullae from this collection.  A separate post will explore the Plum Point periotic bones and report on my effort to use these bones to identify cetacean genus and species.  They are considered by some to be diagnostically useful in this regard.

It may be helpful to make three points at the outset:

  • the term cetacean includes whales, dolphins, and porpoises, although these animals are frequently referred to collectively as whales;
  • fossils of porpoises are not found at the Calvert Cliffs; and
  • cetaceans are divided into members of the Odontoceti, the toothed cetaceans which includes dolphins and porpoises, and members of the Mysticeti which have baleen.

Cetaceans in the Maryland Miocene

It’s certainly not surprising that this Plum Point collection is awash with cetacean fossils.  The Chesapeake Group formations (ranging from the upper Oligocene, more than 23 million years ago, to the upper Pliocene, fewer than 3 million years ago) that are exposed along the Atlantic Coastal Plain are considered to “contain one of the world’s richest and most diverse assemblages of fossil cetaceans.”  (Michael D. Gottfried, et al., Miocene Cetaceans of the Chesapeake Group, Proceedings of the San Diego Society of Natural History, Number 29, 1994, p. 232.)  Of the Miocene formations in the Chesapeake Group, the Calvert Formation, which produces fossils found at Plum Point, is reportedly the one with the “highest vertebrate diversity” of all.  (Gottfried, p. 233.)  Of the 24 established cetacean genera listed by Gottfried, et al. as found in the Miocene formations of the Chesapeake Group, fully 19 occur in the Calvert Formation.   Relevant to the Plum Point collection, at least 11 of the cetacean genera from the Calvert Formation are genera of dolphin.  The small size of many of the cetacean fossils in this collection suggest they are from dolphin genera. 

Evolution of Cetaceans

Where do these Miocene cetaceans fit into the broad sweep of cetacean evolution?  The evolutionary transitional changes needed to live in the water occurred before the Miocene Epoch (23 to 5 million years ago).  Fossils considered to be cetacean first appear very early in the Eocene Epoch which ran from 56 to 34 million years ago.  The evolutionary arc of these mammals from land to water is well documented in the fossil record:  in the early Eocene, from a common ancestor arose the taxon that would lead to the modern hippopotamus and a separate taxon from which the stem cetaceans, and ultimately the crown cetaceans, would evolve.  In a beautiful figure (no other adjective for it) showing the phylogenic relationships among the cetacean taxa that evolved from that common ancestor, Michael R. McGowen, et al., delineate the appearance over time of the distinguishing attributes for cetaceans.  (Figure 1, Molecular Evolutionary Tracks Macroevolutionary Transitions in Cetacea, Trends in Ecology & Evolution, Volume 29, Number 6, 2014.)  Given copyright concerns, I thought it inappropriate to reproduce that figure here.

Fossils of the earliest primitive cetaceans are likely more than 50 million years old.  The transition of the early pioneers into the water to the status as fully marine animals took place in what is a paleontological and geological instant, perhaps as few as 10 million years.  The figure in McGowen, et al., shows that the morphological and behavioral changes incumbent upon an initial semiaquatic existence came quickly, beginning with the acquisition of heavy limb bones, loss of some hair, and initiation of underwater nursing.  The steady acquisition of marine and loss of terrestrial attributes meant that, by some 40 million years ago, early cetaceans had become obligate aquatic, that is, they could no longer survive on land.  Paleontologist Nick Pyenson divides the overall evolutionary span of cetaceans into two unequal parts.  As already described, the first (some 10 million years or so) saw key transitional changes necessary for life in the water.  Among these transitional modifications were "shell-shaped ear bones being repurposed for underwater hearing."  The second, longer phase (40 million years) was a time for innovations that allowed cetaceans to diversify markedly:  the development of baleen (Mysticeti) and of echolocation (Odontoceti).  Both of these innovations appeared during the Oligocene Epoch (34 to 23 million years ago) which preceded the Miocene.  (The quoted text is from Pyenson, Spying on Whales:  The Past, Present, and Future of Earth's Most Awesome Creatures, 2018, p. 36; a fuller discussion of these two periods can be found in Nicholas D. Pyenson, The Ecological Rise of Whales Chronicled by the Fossil Record, Current Biology, Volume 27, June 5, 2017.)  

Cetacean Hearing with a Focus on the Middle Ear

Moving into the water posed myriad challenges, one of the most critical was how to hear in this medium so different from air.  Mammalian ears designed for hearing on land are clearly malformed for hearing under water.  For one thing, the acoustical impedance of water and that of the organism's soft tissues are similar, meaning that when such ears are under water, sound will enter the inner ear from multiple avenues, not just through the outer ear and ear canal, and middle ear.  Locating the source and direction of sounds becomes very tricky.  In order to function effectively in water, cetacean ears changed and that transformation happened relatively quickly.  McGowen's Figure 1 shows that almost “immediately” the stem cetaceans developed dense ear bones which were important for hearing under water.  By perhaps as early as some 50 million years ago, stem taxa had evolved a fat pad attached to the lower jaw to aid in hearing (more on that below).  By no later than 40 million years ago outer ears were gone.

To make some sense of these Plum Point cetacean fossils (both kinds coming from the middle ear), I went in search of basic research material on the morphology of the cetacean middle ear.  In a post over a decade ago, I lamented the lack of literature accessible to the layperson on cetacean hearing.  As I prepared the present post, I was dismayed to discover that there were in fact some quite useful sources available back then.  Nevertheless, despite locating these and other sources, my grasp of the basics of cetacean hearing remains tenuous.  I welcome any corrections of errors of fact or interpretation in the following discussion.  In a subsection at the end of this discussion, I discuss some of the principal sources I used.

As the cetacean ear evolved to deal with the new medium through which sound had to travel, I’ve already noted that the bones of the ear became heavier.  The outer ear, of no utility, faded into obscurity.  The air-filled middle and fluid-filled inner ears were encompassed in what is known as the tympano-periotic complex consisting of two bones:  the tympanic bulla and periotic bone.  Pictured below is a periotic bone (top) and a tympanic bulla (bottom) from my Plum Point collection.

To help me orient the overall relationship between the periotic bone and bulla which house the complex, I prepared this drawing of the complex exterior based on a photograph of a modern neonate bottlenose dolphin.

The tympano-periotic complex is largely isolated acoustically from the skull (completely for odontocetes, less so for mysticetes).  In odontocetes, sound waves travel from the cetacean’s thin lower jaw through a fat pad to the tympanic bulla.  For mysticetes, the process through which sound is received is still "unknown," though at least for some genera fat is likely to play a role.  (Maya Yamato and Nicholas D. Pyenson, Early Development and Orientation of the Acoustical Funnel Provides Insights into the Evolution of Sound Reception Pathways in Cetaceans, PLOS One, Volume 10, Number 3, March 11, 2015.)

The bulla is a distinctively shaped bone, much like an elongated cup or scoop, with a greatly thickened medial lip called the involucrum and a much thinner outer lip named the tympanic plate.  Though all mammals have a bulla of sorts, it’s the involucrum that sets the cetacean bulla apart.  As Pyenson observes, the involucrum is a critical feature used by paleontologists to distinguish the earliest cetaceans from other ancient animals:  it's an attribute that "makes them whales and not something else."  (Spying on Whales, p. 29.)   The involucrum and tympanic plates are labelled in the picture below.

The isolation of the bulla from the other bones of the skull and the thick-thin configuration of the bulla lip are instrumental in allowing the bulla to vibrate in response to incoming sound waves (and to forestall conduction of sound to the inner ear through any other bones).  The tympanic plate has a bony connection to an array of ossicles (small bones), beginning with the malleus which in turn connects to the smaller incus and then to the still smaller stapes.  These small bones transmit the sound vibrations to the fluid-filled inner ear canal and to the cochlea.  That process strengthens the sound.  The prominent knob in roughly the top center of the periotic bone (see photograph above) contains the circular passages of the cochlea in which sound waves are converted to electrochemical impulses which are then transmitted to the brain via the vestibulo-cochlear nerve.  The periotic bone has various openings (some of which are visible in the photograph above); through one, the cochlear nerve connects to the brain.  Here is a schematic outline of the key elements in the cetacean middle ear as it directs sound waves to the inner ear.

Some of the Principal Sources for the Preceding Discussion of Cetacean Hearing

Among the available valuable resources on cetacean hearing in general is the first of two extensive posts written by paleontologist Robert Boessenecker for his blog The Coastal Paleontologist:  Perspectives on Marine Vertebrate Paleontology.  This post, titled Bobby’s Guide to Whale & Dolphin Earbones 1:  Introduction, is dated December 3, 2022, and explores the morphology of mammalian ears, contrasting those of land mammals and those of the cetaceans.  (I intend to use the second, Bobby’s Guide to Whale & Dolphin Earbones 2:  Identifying Toothed Whale Periotics, which appeared January 15, 2023, in a later post.)

One of the clearest expositions of the process of cetacean hearing can be found in an article by Sirpa Nummela et al., who used CT scans to delineate how the features of the middle ear of a killer whale (an odontocete) function and how they relate to each other.  (The Anatomy of the Killer Whale Middle Ear (Orcinus orca), Hearing Research, Volume 133, Issues 1-2, July 1999, residing behind a paywall.)

Later, Sirpa Nummela and a different group of colleagues produced a very informative article on the evolution of different ear structures and their role in cetacean hearing.  (Sound Transmission in Archaic and Modern Whales:  Adaptations for Underwater Hearing, Hearing Research, Volume 290, 2007.) 

A wealth of information and relevant images (one of which formed the basis for the drawing above of the complex) can be found in J.G. Mead and R.E. Fordyce’s The Therian Skull:  A Lexicon with Emphasis on the Odontocetes (Smithsonian Contributions to Zoology, Number  627, 2009).

Helpful, and the underlying source of the schematic drawing above of the middle ear, is A Model of the Odontocete Middle Ear by Simo Hemilä, et al. (Hearing Research, Volume 133, 1999, resides behind a paywall).

Selection of Tympanic Bullae from the Plum Point Collection

Here are four additional specimens from the collection.  They are unquestionably quite well worn and their small size certainly suggests dolphin origin.

From my earliest fossil collecting, I found tympanic bullae singularly attractive, capped as they are by the wave-like flow of the involucrum. It's the feature most likely to survive over millions of years, retaining the visible poetry of its sculpted form.

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