Reconstructing Cetacean Brain Evolution Using Computed Tomography

Home , Archaeoceti, Basilosauridae, Eurhinodelphis, Xenorophus, Zygorhiza

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5-2003

Lori Marino Emory University

Mark D. Uhen Cranbook Institute of Science

Nicholas D. Pyenson University of California - Berkeley

Bruno Frohlich The Smithsonian Institution

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Recommended Citation Marino, L., Uhen, M. D., Pyenson, N. D., & Frohlich, B. (2003). Reconstructing cetacean brain evolution using computed tomography. The Anatomical Record Part B: The New Anatomist, 272(1), 107-117.

This material is brought to you for free and open access by WellBeing International. It has been accepted for inclusion by an authorized administrator of the WBI Studies Repository. For more information, please contact [email protected]. THE ANATOMICAL RECORD (PART B: NEW ANAT.) 272B:107–117, 2003

FEATURE ARTICLE

Reconstructing Cetacean Brain Evolution Using Computed Tomography

LORI MARINO,* MARK D. UHEN, NICHOLAS D. PYENSON, AND BRUNO FROHLICH

Until recently, there have been relatively few studies of brain mass and morphology in fossil cetaceans (dolphins, whales, and porpoises) because of difﬁculty accessing the matrix that ﬁlls the endocranial cavity of fossil cetacean skulls. As a result, our knowledge about cetacean brain evolution has been quite limited. By applying the noninvasive technique of computed tomography (CT) to visualize, measure, and reconstruct the endocranial morphology of fossil cetacean skulls, we can gain vastly more information at an unprecedented rate about cetacean brain evolution. Here, we discuss our method and demonstrate it with several examples from our fossil cetacean database. This approach will provide new insights into the little-known evolutionary history of cetacean brain evolution. Anat Rec (Part B: New Anat) 272B:107–117, 2003. © 2003 Wiley-Liss, Inc.

KEY WORDS: computed tomography; CT; Cetacea; imaging; fossil; endocranial; brain; evolution; encephalization

INTRODUCTION Mysticeti (comprising 11 living species popotamids are their extant sister of baleen whales) are first found in the group (Nikaido et al., 1996; Shimamura The origin and evolutionary history of fossil record in the latest Eocene et al., 1997; Gatesy, 1998; Milinkovitch Cetacea (dolphins, whales, and por- (Mitchell, 1989) and Odontoceti (com- et al., 1998). Recent fossil morphologic poises) represents one of the most dra- evidence confirms an artiodactyl–ceta- matic and provocative transformations prising 66 living species of toothed cean link from both early Eocene pro- in the fossil record. Cetacea consists of whales, dolphins, and porpoises) are tocetid (Gingerich et al., 2001) and pa- one extinct and two modern suborders. first found in the fossil record in the kicetid (Thewissen et al., 2001) whales The Eocene suborder, Archaeoceti, early Oligocene (Barnes et al., 1985). (Geisler and Uhen, 2003). See Figure 1 contained approximately 30 (described) Cetacean terrestrial ancestry is closely for a phylogenetic tree depicting the genera (updated from Thewissen, 1998) tied to that of ungulates (hooved mam- ranges and phylogenetic relationships and survived from the early Eocene, mals) and particularly Artiodactyla, the of extinct and extant cetacean families. around 53 million years ago (Ma) until “even-toed” ungulates. For many years, the late Eocene, around 38 Ma (Barnes molecular evidence has indicated that et al., 1985; Bajpai and Gingerich, 1998; cetaceans are embedded in the Uhen, 1998). Of the modern suborders, paraphyletic Artiodactyla and that hip- Some of the most significant evolutionary Dr. Marino is a senior lecturer in the Neu- Integrative Biology and Museum of Pale- changes that occurred roscience and Behavioral Biology Pro- ontology at the University of California, gram at Emory University in Atlanta, GA, Berkeley, is interested in evolutionary de- among cetaceans are in and a Research Associate at both the Liv- velopment, paleoecology, and major evo- ing Links Center for the Advanced Study lutionary adaptations. Dr. Frohlich is an brain size and structure. of Human and Ape Evolution at Yerkes anthropologist in the Department of An- Regional Primate Research Center and thropology at the National Museum of the National Museum of Natural History at Natural History, The Smithsonian Institu- the Smithsonian Institution in Washington, tion. His research includes the studying of D.C. Her research program is focused on mortuary practices in the Middle East and Skeletal fossils document the major comparative brain and behavioral evolu- in Alaska, and the application of computed transformations in cranial and post- tion studies of cetaceans (dolphins, tomography to the study of archaeological whales, and porpoises) and primates. Dr. artifacts, human remains, and paleobio- cranial morphology that occurred Uhen is the Head of Science and Curator logical specimens. throughout cetacean evolution (Gaskin, of Paleontology and Zoology at Cranbrook *Correspondence to: Dr. Lori Marino, De- Institute of Science. Dr. Uhen’s research partment of Psychology, Emory Univer- 1982; Barnes, 1985; Oelschlager, 1990; focuses on the origin and evolution of sity, Atlanta, GA 30322. Fax: 404-727-0378; Buchholtz, 1998; Luo, 1998). In addi- cetaceans (whales and dolphins), major E-mail: [email protected] tion, some of the most significant evo- evolutionary transitions in general, functional morphology, use of stratigraphic lutionary changes that occurred among data in phylogenetic analysis, and theoret- DOI 10.1002/ar.b.10018 cetaceans are in brain size and struc- ical aspects of diversification. Mr. Pyen- Published online in Wiley InterScience son, a graduate student in the Dept. of (www.interscience.wiley.com). ture. Numerous lines of evidence indicate that the terrestrial ancestors of

Figure 1. Phylogenetic relationships among families of Cetacea. Families of the paraphyletic suborder Archaeoceti are shown in green, whereas those of Mysticeti are shown in blue, and those of the Odontoceti are shown in red. Ranges of families are shown in solid colored lines, and phylogenetic links are shown in dashed lines. Some families (such as the Basilosauridae) are paraphyletic in that they are thought to be ancestral to other groups of cetaceans (in this case, the Neoceti [Odontocetiϩ Mysticeti]). This figure is based on Figure 1 of Barnes et al. (1985). cetaceans were not particularly highly eral cetacean groups with EQs in the problem has been that the data and encephalized and possessed typically range of 4.0 to 5.0, possess enceph- analysis techniques for determining organized mammalian brains alization levels significantly higher the pattern of that dramatic change (Edinger, 1955; Gingerich, 1998). The than all other mammals except mod- from the terrestrial ancestral form to encephalization quotient (EQ) quanti- ern humans with EQs of 7.0 (Marino, the present form have not been avail- fies the actual brain size of an animal 1998) and evince evidence of a sub- able. compared to the expected brain size stantial degree of morphologic diver- of an animal of that body weight gence and cortical reorganization re- CETACEAN NEUROANATOMY within a given reference group. EQs sulting in a different elaborative mode FROM ENDOCASTS higher than 1 are greater than ex- from other mammals (Glezer et al., pected, and those less than 1 are lower 1988). Therefore, cetacean brains There have been relatively few esti- than expected. Presently, when com- have changed significantly through- mates of brain mass and/or brain– pared to other modern mammals, sev- out their evolution. A longstanding body mass ratios in fossil cetaceans FEATURE ARTICLE THE ANATOMICAL RECORD (PART B: NEW ANAT.) 109 because of difficulty accessing the lated over the decades from examina- ceans transformed from a terrestrial matrix that fills the endocranial cav- tions of either natural or artificial en- (Thewissen et al., 2001), to a semia- ity of fossil cetacean skulls, which is docasts. In the past few years, quatic (Gingerich et al., 2001), to a often very hard and difficult to re- computed tomography (CT) imaging fully aquatic creature (Uhen, 1998). move. Also, even when the matrix is has become a breakthrough investiga- Previous studies indicate that Eocene removed, it is difficult and time con- tive tool in the study of fossil endocra- cetaceans (archaeocetes) are not par- suming to make accurate artificial nia because it allows for nondestruc- ticularly encephalized when com- endocasts from which volume mea- tive visualization and measurement of pared with modern odontocetes (Gin- surements can be made. Several endocranial features and digital re- gerich, 1998; Marino et al., 2000). early estimates of brain mass from construction of specimens. CT in- Marino et al. (2000) was the first study endocranial casts have been pub- volves the application of a collimated of cetacean encephalization to use CT lished (Dart, 1923; Marples, 1949; series of x-rays through the target ob- methodology to visualize, measure, Breathnach, 1955). More recently, ject to produce a series of sectional and reconstruct endocranial features Gingerich (1998) used natural endo- images, called tomographs, which re- of archaeocete fossils. The value of CT casts to reinterpret brain and body flect the radiographic densities of tis- was demonstrated in this study by the mass for several archaeocetes and sues in the plane of scanning. When fact that we obtained more data on calculated EQs relative to modern radiographic densities in the sediment archaeocete brain size by using CT terrestrial mammals ranging from that fills the endocranial cavity are than has been collected from natural 0.25 to 0.51, demonstrating that sufficiently different from that of the and artificial endocasts during the early semiaquatic and later fully surrounding bone, the image presents past several decades. aquatic archaeocetes possessed lev- a way to visually isolate, measure, and In Marino et al. (2000), we sug- els of encephalization dramatically reconstruct the endocranial cavity. gested that the principal features of lower than most modern cetaceans. increased encephalization in modern In addition to serving as a proxy for cetaceans emerged as a result of selec- brain size, natural endocasts have also In addition to serving as tive pressures that occurred well after served as the basis for morphologic de- the initial transition from a terrestrial scriptions of brain contours in archaeo- a proxy for brain size, to aquatic existence. This assertion cetes and early modern cetaceans natural endocasts have was based on our analysis of enceph- (Edinger, 1955). Evolutionary changes also served as the basis alization patterns showing that there in brain organization are not as easily was little change in encephalization assessed as changes in brain size. Often, for morphologic over the entire transition in lifestyle as in the case of cetaceans, the enlarged descriptions of brain from terrestrial to aquatic. This obser- cerebrum masks the structures under- vation suggests that hypotheses about neath. However, many morphologic contours in strong drivers of cetacean brain evo- and surface features can be evaluated archaeocetes and early lution should focus on factors other and conservatively interpreted from the than the terrestrial-to-aquatic transi- contour of fossil endocasts and the en- modern cetaceans. tion. docranial cavity wall. Various morpho- There is a prodigious body of litera- logic features of fossil cetacean endo- ture devoted to hypotheses about both casts have been noted in the literature, We have used CT to elucidate and the intelligence of cetaceans and the including cerebral asymmetry (Stefa- measure the endocranial structure of variables that have shaped the evolu- niak, 1993), lobular morphology fossil cetacean skulls for the past 5 tion of such large brains (Ridgway et (Kellogg, 1936; Edinger, 1955; Czyze- years. CT has allowed us to gain un- al., 1966; Jerison, 1978, 1986; Eisen- wska, 1988; Stefaniak, 1993), the rela- precedented views and insights into berg, 1986; Herman, 1986; Worthy and tive size of major structures (Kellogg, the previously largely inaccessible Hickie, 1986; Glezer et al., 1988; Ridg- 1936; Edinger, 1955; Czyzewska, 1988; world of fossil cetacean endocranial way and Wood, 1988; Marino, 1996; Stefaniak, 1993), and imprints of cra- morphology. The result has been a Connor et al., 1998). Theories have nial nerves (Kellogg, 1936; Edinger, substantial increase in the slope of highlighted such varied and not alto- 1955; Czyzewska, 1988). These kinds of our knowledge about cetacean brain gether independent factors as social observations, when interpreted cau- evolution. Here, we describe our ap- ecology (Connor et al., 1998), commu- tiously, can serve as the basis for infer- proach and some of the CT-based nication (Jerison, 1986), climate change ence about functional changes in the methods we are using in the course of (Davies, 1963; Whitmore, 1994), echo- brains of fossil cetaceans. our investigations of fossil cetacean location (Jerison, 1978; Wood and endocrania to reconstruct cetacean Evans, 1980; Worthy and Hickie, 1986; CETACEAN NEUROANATOMY brain evolution. Oelschlager, 1990), and even diving and FROM COMPUTED oxygenation demands as a constraint on brain size (Robin, 1973). The first TOMOGRAPHY OUR PROJECT step in determining which (if any) of Our understanding of cetacean brain Over the course of approximately 13 these hypotheses are potential explana- evolution has been hindered by the million years of evolution, from tions for the origin and evolution of slow trickle of data that has accumu- around 52 Ma to around 39 Ma, ceta- large brains in cetaceans, is to identify 110 THE ANATOMICAL RECORD (PART B: NEW ANAT.) FEATURE ARTICLE

TABLE 1. The number of species (and families) for each geologic epoch of the cenozoic era included in this study*

Epoch Start (Ma) End (Ma) Archaeoceti Mysticeti Odontoceti Epoch Totals Recent 0.8 0.0 0 (0) 0 (0) 20 (9) 20 (9) Pleistocene 1.8 0.8 0 (0) 0 (0) 0 (0) 0 (0) Pliocene 5.3 1.8 0 (0) 0 (0) 3 (3) 03 (3) Miocene 24 5.3 0 (0) 2 (1) 18 (9) 20 (10) Oligocene 34 24 0 (0) 5 (5) 7 (7) 12 (12) Eocene 56 34 6 (3) 1 (1) 1 (1) 7 (3) Suborder Totals 6 (3) 8 (5) 44 (20)

*The Paleocene is not included, since whales did not evolve until the late early Eocene. The boundaries for each epoch are shown in millions of years (Ma), while totals (numbers of species/families) are provided for each epoch. The number of species is listed first, followed by the number of families in parentheses. the periods in cetacean evolutionary particularly when combined with data future studies will allow us to address history associated with increases in on other anatomical and environmen- the generality of existing theories brain size. Different hypotheses require tal factors. Additionally, the present about the relationship between vari- different patterns of brain evolution at study will yield data on the rate and ous habitat types and encephalization different times, under different condi- pattern of cetacean brain evolution in other mammals. tions, and in different segments of the that will inform current theories cetacean phylogenetic tree. Thus, map- about the uniqueness of the rate and ping the evolution of brain size on a pattern of brain evolution in other CETACEAN FOSSIL BRAIN time-constrained phylogenetic history phylogenetic groups, including homi- ANALYSIS will lend support to some hypotheses nids. Finally, as discussed below un- Specimen Selection and eliminate others. der our long-term goals, the data from The present study is a comprehen- the present study will eventually be Most of the samples for this study are sive extension of our initial CT-based considered along with paleoenviron- part of the fossil vertebrate collections studies of archaeocete brain size and mental data to understand which fac- of the United States National Museum encephalization. We use CT scanning tors are correlated with increases in (USNM) at The Smithsonian Institu- and postimage processing to calculate encephalization in cetaceans. These tion. The collection includes over endocranial volume and generate three-dimensional reconstructions of endocranial contour for a larger set of fossil cetacean specimens over a wider range of time, including a subset of modern cetaceans. Specifically, the objectives of this study are to (1) measure and document endocranial volume and morphology, along with postcranial indicators of body mass, in individual fossil and modern cetacean specimens; (2) use these data to estimate encephalization level in fossil and modern taxa; and (3) reconstruct the sequence of change in brain size and morphology in cetacean based on our current understanding of the phylogenetic history of this group. As noted above, some hypotheses about the evolution of cetacean brains make specific testable predictions about when in the evolution of an aquatic lifestyle certain anatomical features of the brain would have de- Figure 2. Photograph (dorsal view) of USNM167622, Eurhinodelphis morrisi, in plaster of Paris veloped. The data to be obtained in cradle with hardened matrix inside skull visible along the midline openings between the the present study will form the basis premaxilla. The anterior end of the rostrum is broken and missing. [Color figure can be for tests of some of these hypotheses, viewed in the online issue, which is available at www.interscience.wiley.com.] FEATURE ARTICLE THE ANATOMICAL RECORD (PART B: NEW ANAT.) 111

in the scans prompted us to exclude specimens from the study. In addition, if there was poor contrast between the sediment and bone, or if the sediment scattered the x-rays during scanning and created artifacts, specimens were rejected. The result is a collection of 166 fossil specimens and 50 modern odontocete specimens from which data have been or is being collected. Nine of the fossils are archaeocetes, 15 are mysticetes, 115 are odontocetes, and another 27 have not been identified to Figure 3. Photographs of USNM 11121 Basilosaurus cetoides filled with hardened matrix. A: suborder as yet, but most are likely to Lateral view. B: Dorsal view. [Color figure can be viewed in the online issue, which is be odontocetes. Due to the difficulty available at www.interscience.wiley.com.] of including the large mysticetes, we decided to focus our study on odonto- 9,500 fossil cetacean specimens of in encephalization are related to cetes. Table 1 shows the number of various sorts ranging from single changes in echolocation and/or hear- species and families represented in bones or teeth up to and including ing ability, specimens with associated each time period and suborder. virtually complete skeletons. Addi- periotic bones were favored over Figure 2 depicts a typical odonto- tional specimens from the Charleston those without associated periotics. cete fossil specimen from the Mio- Museum (ChM), the University of Another criterion was the nature of cene, USNM 167622, Eurhinodelphis Michigan Museum of Paleontology the sediment that filled the endocra- morrisi, from Zone 14 of the Calvert (UMMP), and the Natural History Mu- nial cavity. Siliciclastic sediment (sed- Formation, Maryland (approximately seum of Los Angeles County (LACM) iment composed of silica-rich miner- 14 Ma). This specimen shows a con- were studied. als such as quartz and clay minerals) siderable degree of telescoping, the Specimens were selected for this is much more radiotransparent than evolutionary transformation of the study according to several criteria. carbonate sediment (mainly calcite skull by which rostral elements elon- First, we chose specimens that and other carbonate minerals such as gate, caudal elements move dorsoros- spanned from cetacean origins in the barite and celestite). Thus, specimens trally, and the external nares migrate Eocene up to and including the re- preserved in siliciclastic sediment to the dorsal apex of the skull. Figure cent. Endocranial volume values for were favored over those preserved in 3 depicts photographs (lateral and recent (modern/extant taxa) speci- carbonate sediment. dorsal views) of a much older archao- mens included in this study are taken Lastly, specimens were accepted or ecete fossil from the Eocene, USNM from the literature (Marino, 1998) rejected for inclusion in the study 11121, Basilosaurus cetoides, from the and also from recent specimens in the once they were scanned. Any signifi- Ocala Formation, Florida (approxi- vertebrate zoology collection at the cant deformation that revealed itself mately 37 Ma). The condition of the USNM. The second criterion was taxo- nomic. It would be ideal to include specimens representing all families of fossil and modern cetaceans, but un- fortunately some specimens, species, and even entire families could not be included in the study because the specimens were too large to fit into the CT scanner. Most mysticetes were too large to scan, although we have included some small early mysticetes. In addition, larger physeterids (sperm whales) were too large to scan, although some smaller representatives of the Physeteridae were included. The third criterion for inclusion was quality, which was assessed mainly on completeness of the skull and the lack of any obvious deforma- Figure 4. An archaoecete specimen from the Eocene USNM 16638, Zygorhiza kochii,ina tion. In addition, because one of our ventrad position, anterior end pointing away from the scanner, before scanning. [Color goals is to determine whether changes figure can be viewed in the online issue, which is available at www.interscience.wiley.com.] 112 THE ANATOMICAL RECORD (PART B: NEW ANAT.) FEATURE ARTICLE

Figure 5. Posterior-to-anterior series of 1.22-mm-thick coronal CT images at 24.4-mm intervals (except for the last, which is 22 mm) through the cranium of USNM 167622, Eurhinodelphis morrisi. The endocranial cavity of section 82 is outlined to illustrate how measurements are taken. specimen in Figure 3 is typical of a ner and at Methodist Hospital in Arca- ages at 24.4-mm intervals (except for specimen dating from the Eocene. De- dia, California, on a Picker PQ 5000 the last, which is 22 mm) through the spite being filled with hardened ma- single-slice spiral scanner. We obtained cranium of USNM 167622 Eurhinodel- trix we were able to use CT to measure contiguous 1- to 2-mm coronal scans of phis morrisi defining the total endocra- endocranial volume in this specimen. the entire cranium of each specimen nial volume. These images show the ex- using different scanning parameters, cellent contrast between fossil skull CT Scanning Protocol depending on the estimated density of bone and endocranial matrix. the fossil and endocranial matrix, level CT scanning of fossil specimens was conducted using a Siemens Somatom of permineralization of the bone, and Measuring Endocranial Volume SP scanner located in Bruno Frohli- whether the skull was embedded in sur- from CT ch’s laboratory in the Department of rounding hardened matrix. We scanned Anthropology at the National Mu- the entire specimen past the endocra- We used Scion Image, a PC-based ver- seum of Natural History (USNM), nial cavity as well. Specimens were po- sion of NIH Image, and Image J, a Smithsonian Institution. The scanner sitioned on the scan table either ven- Java-based version of NIH Image, to uses a Sun Sparc microcomputer run- trally or dorsally, depending on which digitally trace around the endocranial ning Sun OS. Image acquisition, anal- orientation was more stable and so that cavity on each slice, integrate those ysis, and file conversions are controlled the posterior end was usually scanned areas, and arrive at a volume for the by Siemens SOMARIS software. first. Figure 4 shows an archaoecete entire endocranial cavity. An outlined OSIRIS software (University Hospital specimen from the Eocene, USNM coronal section is shown in section 82 of Geneva) was used to convert Sie- 16638, Zygorhiza kochii, from the Yazoo of Figure 5. The calculated endocra- mens image files into DICOM images. Clay Formation (approximately 37 Ma), nial volume is an estimate for the size Additional scans were conducted at the Choctaw County, Alabama, lying ven- of the brain. For both fossil and mod- Medical University of Charleston in trad on the table just before scanning. ern specimens, the posterior portion Charleston, South Carolina, on a Mar- Figure 5 shows a posterior-to-anterior of the endocranial region was defined coni MX8000 multiple-slice spiral scan- series of 1.22-mm-thick coronal CT im- as the most posterior coronal slice FEATURE ARTICLE THE ANATOMICAL RECORD (PART B: NEW ANAT.) 113

ble to fossil cetaceans. Cetacean teeth are not good candidates for a tight correlation with body mass for a variety of reasons. First, most mysticetes lack teeth altogether. Second, most odontocetes do not use their teeth for oral processing, and some, again, lack teeth (Uhen, 2002). Third, even archaeocetes, which retain a more typically mammalian differentiated dentition, have dramatically changed their mode of oral processing from that of their terrestrial ancestors (O’Leary and Uhen, 1999). Besides dentition, long bone dimensions are even less likely to be good predictors of body mass because they no longer resist the force of gravity in fully aquatic cetaceans (Madar, 1998). Two other methods of estimating body weight have been previously used on fossil cetaceans. First, Jerison (1963) used a method of correlating skeletal length and body mass. In Marino et al. (2000), we adapted this method for use on cetaceans by using modern cetacean skeletal lengths and known body masses to predict fossil Figure 6. Three-dimensional reconstructions of the endocranial space in specimen ChMPV cetacean body mass from known skel- 4266, Xenorophus sp. A: Left rostrolateral view. B: Ventral view. C: Dorsal view. D: Left lateral etal lengths. This method assumes view. that fossil cetaceans had a body form similar to those of modern cetaceans. This assumption is more likely to be containing a completely enclosed fo- measuring clay model replicas of en- the case for fossil Neoceti and proba- ramen. In fossil specimens, the ante- docranial retes on existing natural en- bly even the fully aquatic basilosaurid rior extent was defined as the coronal docasts. archaeocetes but less likely to be the slice that includes the anterior edge of case for the earlier semiaquatic ar- the basisphenoid or the most anterior Estimating Postcranial chaeocetes. The second method of es- coronal slice containing the frontal timating body weight that has been Parameters bone where there is still endocranial applied to fossil cetaceans is one de- space. The use of one or the other of Body mass in fossil mammals has veloped by Gingerich (1998) that uses these criteria depended on the cranial been reconstructed using a variety of a variety of anatomical measurements morphology (e.g., degree of telescop- methods. These methods rely on a from the head, vertebral column, and ing) of the fossil specimen. In modern scaling relationship between single or limb elements to estimate body mass. specimens, the anterior extent was de- multiple body parts with body mass. This method uses the relationships of fined as the most anterior coronal Tooth size (particularly molar size) these variables in modern marine slice containing the frontal bone has been used in some mammals that mammals to estimate body mass in where there is still endocranial space. perform a great deal of oral process- fossil cetaceans. Although this The total volume of the endocranial ing of food (Gingerich, 1977). The se- method shows a great deal of promise, space is an overestimate of actual lected molar is usually one that dis- it uses a computer program to per- brain size because it includes the vol- plays low within-species variability form the calculation, which has not ume of the cranial rete mirabile. To (Gingerich, 1974) in an attempt to yet been published. estimate brain mass, we are currently maximize its potential correlation In this study, we use both the body estimating the endocranial rete vol- with body size. Other methods have length method and Gingerich’s ume from total endocranial volume in used a variety of measurements from method (at least for those species to each specimen to obtain brain size es- long bones to predict body mass (Gin- which it has been previously applied). timates for use in calculating EQ val- gerich, 1990). Because long bones re- We have also added a third method, ues. Rete measurements and esti- sist the force of gravity on the body because very few fossil cetacean spec- mates will be obtained either from the mass, their architecture should reflect imens (much fewer species) include literature, from direct measurement the ability to resist that force. entire skeletons from which one can when visible in the CT scans, or by Neither of these methods is applica- obtain a skeletal length or the multi- 114 THE ANATOMICAL RECORD (PART B: NEW ANAT.) FEATURE ARTICLE

the OSIRIS program and then tracing the endocranial space on each image with Adobe Photoshop 5.0. The posterior–anterior extent of our outlines were at the opening of the magnum foramen and either the frontal bone (in more recent specimens) or the front region of the endocranium that tapers off rapidly just posterior to olfactory lobe expansion. In some coronal slices where the endocranial area was unbounded or opened by cranial nerves, it was necessary to delimit the endocranial area using consistent endocranial landmarks. The final tracings were then saved in a TIFF format. We loaded the entire set of two-dimensional tracings for each endocranium into Image J, and used Volume Rendering plug-ins to reconstruct the endocranium as a three-dimensional object that could then be viewed at different angles and shading. Figure 6 displays a three-dimensional reconstruction, in four different views, of the endocranial space in a late Oligocene specimen ChM PV4266, Xenorophus sp. from the Chandler Bridge formation, North Carolina (approximately 27 Ma). Fig- Figure 7. Three-dimensional reconstructions of the endocranial space in specimen USNM 167622, Eurhinodelphis morrisi. A: Left laterocaudal view. B: Caudal view. C: Rostral view. D: ure 7 displays a three-dimensional re- Right laterocaudal view. construction of the endocranial space in specimen USNM 167622, Eurhino- delphis morrisi in four different views. ple anatomical measurements needed brain size relative to expected brain Both reconstructions appear to repre- to apply Gingerich’s method. Because size for a species or genus. EQ values sent the shape of the brain without specimens were included in our CT are calculated from a least-squares re- any obvious distortions. As is the case study if they had relatively intact crania, gression of log mean adult brain for most natural and artificial endo- we looked for a measurement of the weight on log mean adult body weight casts, it is not possible to detect and skull that was independent of brain size ϭ for a given group. The equation, EQ reproduce the pattern of convolutions that might be indicative of body size. 0.67 brain weight/0.12 (body weight) that existed on the surface of the We selected the occipital condyle from Jerison (1973) was used to de- brain. Therefore, interpretations must breadth (OCB), because that was the rive EQ values for each genus, or be based almost entirely on overall point where the head attached to the when possible, each species, repre- shape and morphology of gross struc- body, so we were of the opinion that it sented in our sample. EQ0.67 values tures. had the greatest potential to predict for the present sample may be inter- body size of any cranial measurement. preted as loosely expressing how en- We measured the OCB on a wide range RECONSTRUCTING CETACEAN cephalized each genus or species is of modern cetacean specimens with BRAINS known body masses and found that it with reference to a general modern was very strongly correlated with body mammalian sample. For the purposes of comparing the mass (Pearson r ϭ 0.89). This strategy reconstructed fossil specimens with allowed us to use that regression equa- Three-Dimensional a modern cetacean brain, Figure 8, which displays an MRI (Magnetic tion to estimate body mass from fossil Reconstruction Through CT cetacean specimens where only the cra- Resonance Imaging)-based three-di- nium is known. By using Image J software, we assem- mensional reconstruction of a mod- bled our three-dimensional endocra- ern bottlenose dolphin (Tursiops Calculating Encephalization nial reconstructions by compiling truncatus; Field number WAM545) two-dimensional coronal outlines of brain from a previously published Quotients the CT-scanned endocrania. These study (Marino et al., 2001), is repro- As noted previously, encephalization outlines were created by converting duced. Because of the recent age of quotient is a measure of observed the DICOM images to TIFF files using the specimen, some surface convolu- FEATURE ARTICLE THE ANATOMICAL RECORD (PART B: NEW ANAT.) 115

specimen. Generally, the overall morphology of the cerebral hemispheres of the more recent Eurhinodelphis specimen more closely resembles the modern odontocete brain than the older Xenorophus specimen. The EQ values associated with ChMPV 4266, USNM 167622, and the modern bottlenose dolphin, are approximately 3.28, 2.67, and 4.14, re- spectively. All of these values indicate that the three specimens had brains larger than expected for their body size. However, these EQ values do not show a pattern of increasing encephalization similar to the pattern of increased morphologic development observed. This is likely because there was a wide range of encephalization levels throughout most of cetacean evolution (with values ranging from less than 1 to more than 4.5) and these specimens do not reﬂect an ancestor– descendent lineage. The point here is

Apart from modern humans, cetaceans are the most highly encephalized mammals that have likely ever existed.

that these kinds of reconstructions, considered with encephalization estimates, can serve as the basis for much Figure 8. Reproduction of a three-dimensional reconstruction of the endocranial space in more highly detailed and quantitative a modern bottlenose dolphin specimen (WAM545) from MRI. Dorsal view (A) and rostral left morphologic comparisons of the pro- lateral view with ventral side exposed (B), from Marino et al. (2001). portions and organization of whole brains and brain structures across tional patterns are visible on the the modern specimen (Tursiops trun- specimens that, when registered to three-dimensional reconstruction of catus, WAM545). There is a gradation our best estimate of phylogenetic re- the bottlenose dolphin but the depth of cerebral development ascertainable lations, can inform us directly about of the gyri and sulci are not well across all three, with the oldest speci- the pattern of change that occurred in represented. men ChMPV 4266, showing the least various cetacean lineages. Although all of the present speci- amount of bulbousness characteristic mens compared are odontocetes, of modern odontocete brains. ChMPV BRAIN ELABORATION, none of them are related along a sin- 4266 displays the more elongated ap- BEHAVIOR, AND FUNCTION gle ancestor–descendent lineage. pearance of archaeocete and earlier Therefore, the comparisons we make cetacean specimens. Notably, the re- Cetacean brain evolution is an intrigu- here are for exemplification purposes constructions show that the olfactory ing example of how large complex only and are not meant to suggest di- bulbs of the 27 million-year-old brains can emerge from ordinary be- rect evolutionary change. Yet, both ChMPV 4266 are still intact but that ginnings. As noted above, apart from older fossil specimens (Xenorophus they are considerably regressed and modern humans, cetaceans are the sp., ChMPV4266 and Eurhinodelphis essentially vestigial in the more recent most highly encephalized mammals morrisi, USNM167622) show a lesser 14 million-year-old USNM 167622 that have likely ever existed. The en- degree of cerebral elaboration than and completely gone in the modern cephalization level of many modern 116 THE ANATOMICAL RECORD (PART B: NEW ANAT.) FEATURE ARTICLE odontocete species, particularly in the tance, advice, and support: David Bo- Thewissen JGM, editor. The emergence Delphinid and Phocoenid families, ap- haska, Frank C. Whitmore, Jr., James of whales. New York: Plenum Press. p proach modern human levels. This Mead, and Charles Potter, The Smith- 63–111. Geisler JH, Uhen MD. 2003. New fossils level of brain elaboration exceeds that sonian Institution; Caroline Blane and corroborate a close relationship between achieved by even our closest phyloge- John I. Johnson, Michigan State Uni- hippos and whales. J Vertebr Paleontol netic relatives, the great apes (Marino, versity; Larry Barnes, Natural History (in press). 1998). At the same time, we know Museum of Los Angeles County; Gingerich PD. 1974. Size variability of the teeth in living mammals and the diagno- from modern comparative studies and Philip Gingerich, University of Michi- sis of closely related sympatric fossil spe- also from emerging fossil-based data gan; the Medical University of South cies. J Paleontal 48:895–903. that the large brains of cetaceans Carolina, Charleston, South Carolina; Gingerich PD. 1977. Correlation of tooth evolved along a strikingly different and Methodist Hospital, Arcadia, Cal- size and body size in living hominoid trajectory from other mammalian ifornia. The following students are to primates, with a note on relative brain size in Aegyptopithecus and Proconsul. brains and, notably, from primate be thanked for their assistance with Am J Phys Anthropol 47:395–398. brains (Glezer et al., 1988). The differ- either scanning or data analysis: Evan Gingerich PD. 1990. Prediction of body ences between cetacean and primate Garafalo, Shaun Rotenberg, and Behi mass in mammalian species from long brains exist at the level of gross mor- Shamsai. bone lengths and diameters. Contrib Museum Paleontal Univ Mich 28:79–92. phology, lobular arrangement, pro- Gingerich PD. 1998. Paleobiological per- portions of subcortical structures, and spectives on Mesonychia, Archaeoceti, neocortical cytoarchitecture (Glezer LITERATURE CITED and the origin of whales. In: Thewissen JGM, editor. The emergence of whales. et al., 1988, for a review). There is also Bajpai S, Gingerich PD. 1998. A new Eo- New York: Plenum Press. p 423–449. a prodigious body of literature dem- cene archaeocete (Mammalia, Cetacea) Gingerich PD, ul Haq M, Zalmout IS, Khan from India and the time of origin of onstrating the complex nature of ceta- IH, Sadiq M. 2001. Origin of whales whales.ProcNatlAcadSciUSA95:15464– cean intelligence (Herman, 1986; Re- from early artiodactyls: Hands and feet 15468. of Eocene Protocetidae from Pakistan. iss et al., 1997; Marino, 2002) that Barnes LG. 1985. Review: General features Science 293:2239–2242. rivals and converges with the abilities of the paleobiological evolution of Ceta- Glezer I, Jacobs M, Morgane P. 1988. Im- cea. Mar Mammal Sci 1:90–93. of the great apes. For instance, bottle- plications of the “initial brain” concept Barnes LG, Domning DP, Ray CE. 1985. nose dolphins share the same ex- for brain evolution in Cetacea. Behav Status of studies on fossil marine mam- Brain Sci 11:75–116. tremely rare capacity for mirror self- mals. Mar Mammal Sci 1:15–53. Herman LM. 1986. Cognition and lan- recognition with great apes and Breathnach AS. 1955. Observations on en- guage competencies of bottlenosed dol- humans (Reiss and Marino, 2001). docranial casts of recent and fossil ceta- phins. In: Schusterman RJ, Thomas JA, ceans. J Anat 89:533–546. Therefore, by exploring the divergent Wood FG, editors. Dolphin cognition Buchholtz EA. 1998. Implications of verte- evolutionary natures of cetacean and and behavior: A comparative approach. bral morphology for locomotor evolu- New Jersey: Lawrence Erlbaum. p 221– primate brains, we have an exciting tion in early Cetacea. In: Thewissen 252. opportunity to probe questions about JGM, editor. The emergence of whales. New York: Plenum Press. p 325–351. Jerison HJ. 1963. Interpreting the evolu- alternative neuroanatomical avenues tion of the brain. Hum Biol 35:263–291. to complex cognitive abilities. Connor RC, Mann J, Tyack P, Whitehead H. 1998. Social evolution in toothed Jerison HJ. 1973. Evolution of the brain The application of new noninvasive whales. Trends Ecol Evol 13:228–232. and intelligence. New York: Academic imaging technologies, such as com- Czyzewska T. 1988. Natural endocranial Press. 482 p. puted tomography, have already casts of the whales Pinocetus polonicus Jerison HJ. 1978. Brain and intelligence in Czyzewska & Ryziewicz, 1976, from the whales. In: Frost S, editor. Whales and brought the study of primate and whaling. Vol. 2. Canberra, Australia: hominid brain evolution to a new level Pinczow Limestones (Middle Miocene; southern slopes of the Holy Cross Moun- CJ Thompson. p 159–197. (Zollikofer et al., 1998). Here, we have tains, Central Poland). Acta Geol Pol 38: Jerison HJ. 1986. The perceptual world of demonstrated how the same methods 46–49. dolphins. In: Schusterman RJ, Thomas can elucidate cetacean brain evolu- Dart R. 1923. The brain of the Zeuglodon- JA, Wood, FG, editors. Dolphin cognition and behavior: A comparative ap- tion and, thereby, make possible the tidae (Cetacea). Proc Zool Soc Lond 615–654. proach. New Jersey: Lawrence Erlbaum. kinds of interesting comparative ques- Davies JL. 1963. The antitropical factor in p 141–166. tions mentioned above. For the first cetacean speciation. Evolution 17:107– Kellogg R. 1936. A review of the Archaeo- time, we can address specific hypoth- 116. ceti. Washington DC: Carnegie Institu- eses about selective forces and tempo- Edinger T. 1955. Hearing and smell in tion of Washington. 366 p. Luo Z. 1998. Homology and transforma- ral patterns in cetacean brain evolu- cetacean history. Monatsschr Psychiatr Neurol 129:37–58. tion of cetacean ectotympanic struc- tion through CT-based analyses of Eisenberg JF. 1986. Dolphin behavior and tures. In: Thewissen JGM, editor. The brain morphology. This approach will cognition: Evolutionary and ecological emergence of whales. New York: Plenum bring new rigor to the study of brain aspects. In: Schusterman, RJ, Thomas Press. p 269–301. size and morphologic evolution in JA, Wood FG, editors. Dolphin cognition Madar SI. 1998. Structural adaptations of and behavior: A comparative approach. early archaeocete long bones. In: cetaceans and, thereby, new insights New Jersey: Lawrence Erlbaum. p 261– Thewissen, JGM, editor. The emergence into the neuroanatomical basis of 270. of whales. New York: Plenum Press. p cetacean behavior and intelligence. Gaskin DE. 1982. Evolution of cetacea. In: 353–378. Gaskin DE, editor. The ecology of whales Marino L. 1996. What can dolphins tell us ACKNOWLEDGMENTS and dolphins. New York: Heinemann. p about primate evolution? Evol An- 159–199. thropol 5:81–85. Many thanks are extended to the fol- Gatesy J. 1998. Molecular evidence for the Marino L. 1998. A comparison of enceph- lowing individuals for their assis- phylogenetic affinities of cetacea. In: alization levels between adult anthro- FEATURE ARTICLE THE ANATOMICAL RECORD (PART B: NEW ANAT.) 117

poid primates and odontocetes (toothed skull. In: Thomas J, Kastelein R, editors. Thewissen JGM. 1998. Cetacean origins. whales). Brain Behav Evol 51:230–238. Sensory abilities of cetaceans. New In: Thewissen JGM, editor. The emer- Marino L. 2002. Convergence in complex York: Plenum Press. p 137–162. gence of whales. New York: Plenum cognitive abilities in cetaceans and pri- O’leary MA, Uhen MD. 1999. The time of Press. p 451–464. mates. Brain Behav Evol 59:21–32. origin of whales and the role of behav- Thewissen JGM, Williams EM, Roe LJ, Marino L, Uhen MD, Frohlich B, Aldag JM, ioral changes in the terrestrial-aquatic Hussain ST. 2001. Skeletons of terres- Blane C, Bohaska D, Whitmore FC Jr. transition. Paleobiol 25:534–556. trial cetaceans and the relationship of 2000. Endocranial volume of mid-late Reiss D, Marino L. 2001. Mirror self-recog- whales to artiodactyls. Nature 413:277– Eocene archaoecetes (Order: Cetacea) 281. revealed by computed tomography: Im- nition in the bottlenose dolphin: A case plications for cetacean brain evolution. J of cognitive convergence. Proc Natl Acad Uhen MD. 1998. New protocetid (Mamma- Mammal Evol 7:81–94. Sci USA 98:5937–5942. lia, Cetacea) from the late middle Eo- Marino L, Sudheimer K, Murphy TL, Davis Reiss D, McCowan B, Marino L. 1997. cene Cook Mountain Formation of Lou- KK, Pabst DA, McLellan W, Rilling JK, Communicative and other cognitive isiana. J Vertebr Paleontal 18:664–668. Johnson JI. 2001. Anatomy and three- characteristics of bottlenose dolphins. Uhen MD. 2002. Dental morphology (ceta- dimensional reconstructions of the bot- Trends Cogn Sci 1:140–145. cean), Evolution of,. In: Perrin WF, Wur- tlenose dolphin (Tursiops truncatus) Ridgway SH, Wood FG. 1988. Dolphin sig B, Thewissen JGM, editors. Encyclo- brain from magnetic resonance images. brain evolution. Behav Brain Sci 11:99– pedia of marine mammals. San Diego: Anat Rec 264:397–414. 100. Academic Press. p 316–319. Marples BJ. 1949. Two endocranial casts Ridgway SH, Flanigan N, McCormick J. Whitmore FC Jr. 1994. Neogene climatic of cetaceans from the Oligocene of New 1966. Brain-spinal cord ratios in por- change and the emergence of the mod- Zealand. Am J Sci 247:462–471. poises: Possible correlations with intelli- ern whale fauna of the North Atlantic Milinkovitch MC, Berube M, Palsboll PJ. gence and ecology. Psychon Sci 6:491– ocean. In: Berta A, Demere TA, editors. 1998. Cetaceans are highly derived artio- 492. Contributions in marine mammal pale- dactyls. In: Thewissen JGM, editor. The Robin ED. 1973. The evolutionary advan- ontology honoring Frank C. Whitmore emergence of whales. New York: Plenum Jr. Proceeding of the San Diego Society Press. p 113–131. tages of being stupid. Perspect Biol Med 16:359–380. of Natural History, San Diego, CA. p Mitchell ED. 1989. A new cetacean from 223–227. the late Eocene La Meseta Formation, Shimamura M, Yasue H, Ohshima K, Abe Wood FG, Evans WE. 1980. Adaptiveness Seymour Island, Antarctic Peninsula. H, Kato H, Kishiro T, Goto M, Mu- Can J Fish Aquat Sci 46:2219–2235. nechika I, Okada N. 1997. Molecular ev- and ecology of echolocation in toothed whales. In: Busnel R, Fish J, editors. An- Nikaido M, Rooney AP, Okada N. 1996. idence from retroposons that whales Phylogenetic relationships among cetar- form a clade within even-toed ungulates. imal sonar systems. New York: Plenum tiodactyls based on insertions of short Nature 388:666–671. Press. p 381–426. and long interspersed elements: Hippo- Stefaniak K. 1993. Natural endocranial Worthy GA, Hickie JP. 1986. Relative brain potamuses are the closest extant rela- cast of a delphinid (Cetacea, Delphini- size in marine mammals. Am Nat 128: tives of whales. Proc Natl Acad Sci USA dae) from the Pinczow Limestones (Mid- 445–459. 96:10261–10266. dle Miocene; Holy Cross Mountains, Zollikofer CPE, Ponce de Leon MS, Martin Oelschlager HA. 1990. Evolutionary mor- Central Poland). Acta Geol Pol 43:116– RD. 1998. Computer-assisted paleoan- phology and acoustics in the dolphin 119. thropology. Evol Anthro 6:41–54.