USING DENTAL MICROWEAR ANALYSIS TO PREDICT FEEDING TYPES IN MESOZOIC MARINE REPTILES

A THESES PRESENTED TO THE DEPARTMENT OF BIOLOGY IN CANDIDACY FOR THE DEGREE OF MASTER OF SCIENCE

By JEREMY MARK POYNTER

NORTHWEST MISSOURI STATE UNIVERSITY MARYVILLE, MISSOURI AUGUST 2011

Running Head: DENTAL MICROWEAR IN MESOZOIC MARINE REPTILES

Using Dental Microwear Analysis to Predict Feeding Types in Mesozoic Marine Reptiles Jeremy Mark Poynter Northwest Missouri State University

THESIS APPROVED

Thesis Advisor Date

Dean of Graduate School Date iii

TABLE OF CONTENTS Page

LIST OF FIGURES ...... iv

LIST OF TABLES ...... v

ABSTRACT ...... vi

CHAPTER I – INTRODUCTION ...... 1

CHAPTER II – MATERIALS and METHODS ...... 17

CHAPTER III – RESULTS ...... 37

CHAPTER IV – DISCUSSION...... 46

LITERATURE CITED ...... 54

ACKNOWLEDGEMENTS ...... 61

iv

LIST OF FIGURES Page

FIGURE 1. Tooth of Mosasaurus sp. from Caldwell (2007) ...... 4

FIGURE 2. Figure of tooth of Mosasaurus sp. (USNM 437998) showing measurements of crown height and basal width used to calculate height:base ratio ...... 21

FIGURE 3. Tooth of Mosasaurus sp. (USNM 437998) showing position of the apex (shown is sharply pointed apex) ...... 24

FIGURE 4. Tooth of Mosasaurus sp. (USNM 437998) showing typical pre-mortom apical wear ...... 25

FIGURE 5. Teeth of (A) Mosasaurus sp. (USNM 437998) and (B) Mosasaurus sp. (USNM 481126) showing shape of a cutting edge under low (A) and high (B) magnification ...... 26

FIGURE 6. Injection of polyvinyl siloxane molding material into custom ring 27

FIGURE 7. Diekeen stone poured into tooth mold ...... 29

FIGURE 8. Tooth cast made of Diekeen cast material. Specimen shown is of Tylosaurus sp. (VP 7262) ...... 30

FIGURE 9. Keyence VHX-600 Digital Reflective Microscope ...... 31

FIGURE 10. Lingual surface of Tylosaurus sp. (VP 7262) showing a typical pit microwear feature ...... 33

FIGURE 11. Lingual surface of Globidens sp. (VP 13830) showing a typical scratch microwear feature ...... 34

FIGURE 12. Lingual surface of Platecarpus sp. (VP 13910) showing a typical gouge microwear feature ...... 35

v

LIST OF TABLES Page

TABLE 1. Inventory of specimens sorted by museum accession numbers ...... 18

TABLE 2. Tooth morphology characteristics as related to three feeding types predicted for Mesozoic marine reptiles ...... 22

TABLE 3. Taxonomic summary of specimens ...... 38

TABLE 4. Summary of means and standard errors for crown:base ratios and microwear counts ...... 40

TABLE 5. Summary statistics of total objects, pits, scratches, gouges, and crown height to basal diameter ratio described by feeding type ..... 41

TABLE 6. Kruskal-Wallis one-way analysis of variance results comparing microwear features among feeding types ...... 42

TABLE 7. Mann-Whitney U test results of paired feeding type differences in microwear features ...... 43

vi

ABSTRACT

Extinct predatory marine reptiles constitute a paraphyletic group that includes ichthyosaurs, plesiosaurs, placodonts, and mososaurs. These animals evolved numerous feeding strategies to exploit a diverse prey base that included heavily armored ammonites and belemnoids, and softer-bodied bony fishes, sharks, squid, and other marine reptiles.

Judy Massare's seminal work correlating tooth form and prey preference of Mesozoic marine reptiles suggests morphologic analysis of teeth has significant utility in inferring predator-prey dynamics. Three extreme feeding types within predatory marine Mesozoic reptiles include crush-type, cut-type, and pierce-type feeders.

This project was aimed at establishing (for the first time) if differences in dental microwear patterns are correlated to extreme feeding types in the predatory marine

Mesozoic reptiles. I observed that total numbers of microwear objects, pitting, and gouging all correlated well with diet as predicted by tooth shape. Taxa with crush-type dentition (e.g., Globidens) had significantly more overall wear, pitting, and gouging than cut- and pierce-type feeders. Similarly, cut-type feeders had more wear than pierce-type feeders. These results are consistent with wear that would be expected from consuming prey with hard armoring (crush-type feeders), flesh and bone (cut-type feeders), and soft bodies (pierce-type feeders). Scratch microwear patterns were poor at predicting diet and feeding type.

Dental Microwear 1

INTRODUCTION

Extinct predatory marine reptiles constitute a paraphyletic group that includes

ichthyosaurs, plesiosaurs, placodonts, and mososaurs. These fast swimming predators

dominated many ecological niches in Mesozoic oceans 65 – 250 million years ago (Ma).

They evolved numerous feeding strategies to exploit a diverse prey base that included

heavily armored ammonites and belemnoids, and softer-bodied bony fishes, sharks,

squid, and marine reptiles. Judy Massare’s (1987) seminal work correlating tooth form

and prey preference in Mesozoic marine reptiles suggests morphologic analysis of teeth

has significant utility in inferring predator-prey dynamics in this group. Three extreme

feeding types observed among predatory marine Mesozoic reptiles include crush-type,

cut-type, and pierce-type (Massare 1987).

Dental microwear analysis (DMA) is the study of microscopic scratches and pits

on tooth surfaces as a result of tooth-tooth or tooth-food interactions (e.g., Walker et al.

1978; Scott et al. 2006). Different types of microwear patterns among taxa suggest

variable feeding strategies and diet and is independent of predictions of diet based on

tooth form (Ungar 1996). DMA has been used to study dentition interactions in taxa as

divergent as conodonts, dinosaurs, ungulates, and primates (Fraser et al. 2009). Analysis of microwear features provides a way of testing hypotheses about tooth-tooth and tooth-

food interaction (Williams et al. 2009). To date, there have been no analyses on the dental

microwear of Mesozoic marine reptiles.

My research is aimed at determining if differences in dental microwear patterns

are correlated to feeding types predicted for various predatory marine Mesozoic reptiles.

The working hypothesis of this research project is that Massare’s (1987) tooth form and Dental Microwear 2

function paradigm, originally used to predict foraged prey, will also correlate well with characteristics of dental microwear. Pierce-feeders foraging on soft prey should have little wear; cut-feeders should have medium wear; and crush-feeders should have substantial wear.

Mesozoic marine reptiles represent a paraphyletic group of predatory carnivores of ancient seas. These aquatic predators occupied an ecological niches similar to and as diverse as Cenozoic marine mammals and birds. Fossil evidence suggests that several terrestrial reptile groups began to adapt to aquatic life in the Late Permian (Stearn and

Carroll 1989). Low body temperatures, high tolerance of anoxia, and low metabolic rates provided ancestors of aquatic Mesozoic reptiles good physiological capacities for secondary aquatic adaptation (Carroll 1988). Aquatic reptilian radiations in the Mesozoic did not originate from a single ancestor but rather from several terrestrial clades; however, despite their genealogical diversity, there is surprising anatomical homogeneity and potential behavioral-functional similarities for interesting comparative work across aquatic reptiles (Carroll 1997). Most fauna from this paraphyletic assemblage are extinct marine Mesozoic reptiles.

According to Root (1967: 346), a guild is defined as “a group of species that exploit the same class of environmental resources in a similar way.” Mesozoic marine reptiles foraged on fauna from the water column or benthos (e.g., the mosasaur Globidens and placodonts), preying on animals such as bony fish, sharks, cephlapods, gastropods, and belemnoids (Massare 1987). These creatures did not chew prey but likely swallowed prey whole (Massare 1987). Some reptilian clades from the larger predatory guild Dental Microwear 3

exploiting marine prey in the Mesozoic oceans include Crocodylia, Ichthyosauria,

Mosasauria, Nothosauria, Phytosauria, Placodontia, and Plesiosauria (Mazin 2001).

The study of Mesozoic marine reptiles has made important contributions and advances to our understanding of vertebrate paleontology. This discipline was in its infancy when the discovery of a fossilized crocodile in 1758 on the coast of southern

England (Taylor 1997) and mosasaur skeletons harvested near Maaschrict, the

Netherlands harbingered Georges Cuvier’s transformative thesis of extinction (Schulp et

al. 2005). Contemporary explication of these fossilized Mesozoic marine reptiles

provided science with a unique window into both evolutionary and ecological

transformation.

Most vertebrates have toothed jaws, and Mesozoic marine reptiles are no

exception. Caldwell (2007; Fig. 1) and Budney et al. (2006) described mosasaur tooth

structure as being divided into crown and root. The crown is that portion of a tooth

visible in the oral cavity that is covered with enamel. The root is that portion of tooth

embedded in the alveolus and is covered by cementum (Berkovitz et al., 2002). Crown-

root borders are delineated by the cementum-enamel junction (CEJ).

Most known Mesozoic marine reptiles are polyphyodont, where teeth are replaced

continually throughout life (Russell 1967; Peyer 1968). Situated in the dental groove of

maxillary and dentary bones lay multiple replacement teeth within the dental laminae.

There may be multiple teeth in this space for any one tooth position. Developmentally

advanced replacement teeth enter the functional dentition space at varying patterns and

rates (Caldwell 2007).

Dental Microwear 4

Cemento-enamel junction (CEJ)

Figure 1. Tooth of Mosasaurus sp. from Caldwell (2007).

Dental Microwear 5

A common theme of most predatory aquatic tetrapods is development of simple,

homodont teeth used to seize prey prior to swallowing (Taylor 1987). Dental tissue

formation is best understood ontogenically. Odontoblasts form dentine tissue and

ameloblasts create enamel. Differentiation of odontoblasts from neural crest cells situated

below the basal lamina is controlled by ameloblasts found in the internal epidermis of the

enamel organ. Dentine is formed in a soft tooth bud pattern. Enamel is superficially laid

over dentine construction. Dentine and enamel developmentally arise from the

mineralization of an organic matrix (Rieppel and Kearney 2005).

Tooth form is a function of soft tooth bud pattern. Shape of dentine and enamel

reflects the organization of this soft tooth bud. Small modifications to the arrangement of

epithelial cells on the outer bud surface can translate to significant changes in tooth

morphology (De Vree and Gans 1994). Therefore, only slight changes in dental

developmental tissue arrangement can generate significant morphological diversity in tooth form. Morphological differences, in turn, typically correspond to tooth function.

The form of amniote teeth and dental tissue organization and structure is directly

influenced by composition and physical properties of food (Green 2009). Differences in tooth size among species often reflect differences in the external characteristics of food

(e.g., size, shape, and abrasiveness). Variation in tooth shape indicates differences in the

internal characteristics of food (e.g., strength, toughness, and deformability; De Vree and

Gans 1994).

Most Mesozoic marine reptile teeth have striations on the crown-enamel surface

originating a few millimeters from the tooth base and extending towards the apex. Some

striae are muted at the apex from wear or as part of inherent form (Storrs 1997). Dental Microwear 6

Longitudinal striae function to increase grip and bite pressure (Schulp 2005; Lingham-

Soliar 1999). Additionally, many teeth also have anterior and posterior carinae, which are often serrated for cutting. Carinae were used for capturing prey (Massare 1987) and perhaps for tearing apart large prey.

Caldwell (2007) published important anatomical and histological observations on mosasaur dentition. Careful histological examination can inform researchers about how teeth attach to jaw bone, and this can be used to predict morphological limitations on prey hardness and size available to a predator (Budney et al. 2006). Presence of a cementum- covered root situated in a deep socket and presence of ligamentous attachments between root and alveoleor bone suggests thecodont attachment of mosasaur dentition (Caldwell

2007). Thecodont implantation provides teeth with a robust attachment to surrounding bone for withstanding large masticating forces from consuming hard prey. Most ichthyosaur teeth attached to alveolar bone by aulacodontic or subthecodontic attachment. Both types of implantation situate teeth in longitudinal dental grooves of maxillary and dentary bones (Motani 1997). Aulacodontic and subthecodontic attachments lack supportive alveolar bone collar provided by thecodont attachment.

Mesozoic aquatic predators generally had homogenous, conical teeth (Peyer 1968;

Caldwell 2007) with various crown morphologies specialized for hunting particular prey.

Tooth form is closely related to tooth function and prey preference (Massare 1987).

Pollard (1990) explains that piercing-type teeth are generally cone-shaped; cutting-type teeth possess carinae; and crushing-type teeth have a blunt apex.

Diet is key to understanding the paleoecological condition of ancient organisms

(Fleagle 1999). Detailed examinations of particular dietary items that organisms forage Dental Microwear 7

upon and the feeding processes by which those items are consumed are often derived

from direct observation of closely related extant species. However, Adam and Berta

(2002) described methods for dietary reconstruction of extinct vertebrates with no close

relatives. Methods described for dietary study included: 1) stomach content analysis; 2)

potential prey situated in the same stratigraphic biozone as the species in question; 3)

isotope analysis; 4) dental microwear analysis; and 5) form-function comparisons with

extant species.

Of these methods, preserved stomach contents associated with particular

fossilized skeletons and coprolites provide direct evidence of diet in extinct vertebrates.

For examples, coprolites harvested from Mesozoic chalk beds contained partially digested bones, teeth, and fragments of squid pens (Everhart 2005). The crescent-shaped nicks found in fossilized bivalve shells purportedly made by an Early Mesozoic placodont (Bishop 1975) are examples of indirect evidence of diet. Correlating direct and

indirect evidence of diet has helped construct models of prey preference and feeding

strategies. Each analytical method potentially provides important paleodietary

information, but individually, each method is burdened with limitations. The best

approach to diet reconstruction is likely that which uses multiple lines of evidence.

Relationships between tooth morphology and diet for fossilized species are well

established in mammals (e.g., Owen, 1845; Gregory 1922; Kay and Hylander 1978;

Ungar 2004). Massare (1987) used tooth form, stomach content analysis, and

examination of analogous extant marine mammal diets to predict prey of Mesozoic marine reptiles. Correlating diet to dental form in Mesozoic reptiles is difficult because of several confounding factors: 1) there are scant extant marine reptiles for correlative form- Dental Microwear 8

function study (Massare 1987; Taylor 1987); 2) fossils of prey may not show predation marks (Schwenk 2000); and 3) reptilian predators may alter their prey selection due to

changes in abundance or scarcity (Williams et al. 2009).

Judy Massare’s (1987) seminal work correlating tooth form and prey preference

of Mesozoic marine reptiles suggests morphologic analysis of teeth has great utility for

inferring predator preferences for prey. Her work relates tooth form and function, and

provides great insight into the uses of marine reptile dentition (Motani 2005). The

paradigm of my research project is that Massare’s (1987) tooth form-function work,

originally used to predict foraged prey, will also correlate well with characteristics of

dental microwear.

Based on tooth shape, Massare (1987, 1997) recognized three extremes of dental morphology: pierce-, cut-, and crush-type teeth. Representatives from all three feeding types are found in predatory marine Mesozoic reptiles. Pierce-feeding species likely consumed soft-bodied prey (e.g., squid and octopus). Crush-feeding species had dentition well formed for feeding on hard-bodied, armored fauna (e.g., ammonites, belemnites, and clams). Cut-type feeders had teeth specialized for foraging on bony prey (e.g., large fish and smaller marine reptiles). Given the differences in hardness of prey, I predict that feeding types will also differ in tooth microwear (Poynter and Adam 2011a, 2011b).

Pierce-feeders foraging on soft prey should have little wear; cut-feeders should have medium wear; and crush-feeders should have substantial wear owing to their preference for hard-bodied prey.

Dental microwear analysis is likely to be a good independent test of diet as predicted from tooth morphology. Feeding mechanisms and diet reconstruction of Dental Microwear 9

fossilized mammals from tooth morphologies, stable isotope geochemistry, and dental microwear analysis is well documented in the literature (reviewed by Green 2009).

Microwear features are a product of complex interactions involving food properties, jaw mechanics, and taphonomic effects (Beatty 2005; Goswami et al. 2005).

Material wear is a product of surface interaction – forces of action and effect – between two solid objects. Object interaction includes the surface removal of material from one object as it interacts with a second object. Rabinowicz (1965) explicated four forms of material wear: 1) adhesive wear; 2) abrasive wear; 3) corrosive wear; and 4) surface fatigue wear. Dental microwear is a form of abrasive wear in that the enameled tooth crown interacts with some other material. Microwear forming material might include occluding teeth, ingested food material, or environmental substrate.

Different types (i.e., pits, scratches, and gouges) and densities of microwear features reveal additional information about diet. Walker and Teaford (1989) described how microwear features on molars of adult primates can be used to differentiate diets of hard fruit eaters from leaves, stems, and flowers. Williams et al. (2009) and Fiorillo

(1998) employed dental microwear techniques to understand hadrosaurid and sauropod jaw mechanics. Van Valkenburgh et al. (1990) used microwear density and orientation to distinguish features produced from tooth-tooth contact and feeding mechanics from wear objects produced by food and substrate.

Enamel scratches in other research has been used to identify tooth-tooth attrition interactions (Teaford 1988; Schubert and Ungar 2005), stripping of leaves from branches by primates (Ang et al. 2006), and tooth-tongue movements in walruses (Gordon 1984).

Scratch-to-pit densities are considered diagnostic of dietary type in primates. Teeth of Dental Microwear 10

primate folivores have more scratches than those of frugivores that eat hard material

(Teaford and Ungar 2000).

Although most microwear studies have been conducted on extant mammalian

systems, Fiorillo (1998), Goswami et al. (2005), and Williams et al. (2009) have

substantially utilized dental microwear analysis to document paleodietary and

paleoecological characteristics of dinosaurs in the Mesozoic. Scratches were the

dominant microwear feature in all three studies. Goswami et al. (2005) and Williams et

al. (2009) used scratch length and orientation as independent evidence for assessing

physical properties of consumed food items in these herbivores. All Mesozoic reptiles in

these studies were terrestrial and not aquatic; nevertheless, these studies demonstrate three important points relevant for microwear research on Mesozoic marine reptiles: 1) microwear study has utility for suggesting broad feeding type of fossilized specimens; 2) microwear study can be used for dietary distinctions among fossilized fauna lacking extant descendents; 3) microwear study can be used for analysis of non-mammalian systems – i.e., Mesozoic marine reptiles.

DMA involves qualitative and quantitative assessment of individual features found on the surface of teeth (Scott et al. 2006). These features include pits, scratches,

and gouges (Solounias and Semprebon 2002). DMA employs various tools and

techniques that include the use of stereoscopic light microscopy and scanning electron

microscopy (SEM) (Fraser et al. 2009). Many tooth microwear studies have examined

enamel surfaces at high magnification. Pioneering scanning electron microscope studies

by Alan Walker and colleagues (1978) were expanded by scientists such as Mark Teaford

and Peter Ungar to understand various aspects of primate, rodent, and ungulate dietary Dental Microwear 11

adaptations (Solounias and Semprebon 2002). However, several factors inherent to SEM

analysis necessitated other methods of dental microwear assessment. For example, SEM

analysis is costly (for training and effective operation) and unrepeatable (Fraser et al.

2009). SEM also creates two-dimensional micropictographs from three-dimensional

objects, making good feature recognition highly dependent on instrument settings and

specimen orientation (Scott et al. 2006).

Solounias and Semprebon’s (2002) and Semprebon et al. (2004) seminal work

introduced a new low-magnification method using a stereoscopic light microscope for

DMA. They compared the efficacy of traditional high-magnification SEM against low-

magnification stereoscopic light microscopy DMA to predict ungulate diets and found

results to be equivalent. They found that low-magnification methods had similar

predictive power of feeding type as the traditional SEM methods. Additionally, they

determined that object area and depth measurements were not necessary for determining

feeding types. Observational methods and objectives are different for each type of

microscopy: stereoscopic light microscopy examines a larger area of tooth at lower

magnification (usually < 50 times magnification) while SEM observes a smaller tooth

area at higher magnification (usually > 100 times magnification). Regardless of method,

the purpose of DMA is the same: to observe the effects of attrition (tooth-tooth contact)

and abrasion (tooth-food or tooth-substrate interaction) on dentition and to describe how

patterns of wear might characterize the feeding of examined specimens (Beatty 2005).

Both SEM and light microscopy DMA present challenges for accurate measurement of observed microwear features on Mesozoic marine reptile teeth, because these teeth are generally conical and lack complex occlusion geometry (e.g., facets) Dental Microwear 12

traditionally examined in DMA of mammals. Measurements made along the surface

curvature of these ancient teeth also require complex algorithms for accurate

measurement of microwear features.

Another challenge for DMA is distinguishing between pre-mortem and post-

mortem taphonomic features. Taphonomy is the science of fossil preservation concerned with dynamics of information loss and information gain available from individual fossils

(Martin 1999). One taphonomic effect on fossil dentition is breakage. From direct observation of Mesozoic marine reptile teeth, there is obvious and apparent post-mortem breakage of teeth. If breakage were pre-mortem, fragments would scatter never to be assembled again. Post-mortem breakage must be accounted for in microwear analysis.

Macroscopic breakage is easy to detect and avoid in analysis, but what about post- mortem microwear features? One potential source of post-mortem wear is from physical

movement of the object in the taphonomic pathway (Martin 1999). Argast et al. (1987)

tested dinosaur teeth to see if movement of teeth in rock matrix affected teeth surface and

found that the process created little to no macroscopic wear. Potential microwear effects

from taphonomic processes (e.g., sedimentation in matrix and movement) are generally

unknown.

A second potential source of taphonomic wear could result from weathering

effects before deposition or after exposure. King et al. (1999) and Goswami et al. (2005)

found that physical and chemical weathering obliterates microwear features rather than

creating microwear artifacts. While weathering might shift overall counts of microwear

densities, the ratio of densities among feeding types should not be affected, assuming

weathering affects teeth from all three feeding types equally. Dental Microwear 13

Diet variability within taxonomic and morphological contrived groups affects

microwear analysis. Several factors affect foraging behavior even within a particular

species. Seasonal changes of available food items, dietary resources available within an

occupied microhabitat, and fall-back food items in times of resource scarcity all

potentially contribute to dentition microwear variability (Scott et al. 2005, Galbany et al.

2009). Additionally, microwear patterns can change because of shifts among prey

species, for example in response to climate changes (Rivals and Solounias 2007).

Mesozoic marine reptiles are represented by approximately 20 lineages that independently and secondarily adapted to marine life (Carroll 1997). Given this great diversity, comprehensive taxonomic sampling is costly and inherently limited to those species exposed and discovered. Research suggests variability in microwear patterns is more related to differences in diet and ecological conditions than to taxonomy (Galbany et al. 2009). Microwear analysis, therefore, would be a good independent test of

Massare’s (1987) predicted prey preference defined by feeding type. This taxon- independent analysis is supported by the work of Villier and Korn (2004) who examined changes in ammonite morphology across extinction events. Their results suggested that when basing comparative work on form differences, “morphological disparity is relatively independent of taxonomy” and thereby allows for “the comparison of samples in which a variable proportion of taxa are preserved or sampled” (Villier and Korn 2004:

264).

Kaiser and Rössner (2007) employ a taxon-independent method of microwear analysis to examine and compare diversity of ruminant feeding types in adjacent Miocene communities. Microwear dentition analysis was used to detect and quantify different Dental Microwear 14

ruminant feeding types within the two bio-communities; this information was not discernable by other metric analysis (e.g., tooth crown height). Therefore, Kaiser and

Rössner (2007) assert that microwear analysis contributes unique information about the

ecological milieu of extinct and extant biomes and that “using the dietary interface as a

taxon-independent pathway may allow a more precise comparison of two biomes more

independent from species historical circumstances.” (Kaiser and Rössner 2007: 425).

Most analyses of tooth wear are based on mammalian taxa. These animals have

one or two generations of teeth (monophyodont) and precise occlusion. Most fish

(Purnell et al. 2006) and Mesozoic marine reptiles (Caldwell 2007) are polyphyodont,

where developmentally advanced replacement teeth enter the functional dentition space at

varying patterns and rates. This creates potential experimental anomalies when

examining limited numbers of teeth from small sample groups. For instance, a tooth

examined with few microwear features might reflect a diet of soft-bodied prey, or it

might reflect that the tooth was newly formed and functional.

Purnell et al. (2006) emphasize that mammalian microwear features are the result

of tooth-tooth and tooth-food-tooth interactions during mastication. They also raise

concern that the feeding processes of many fish (suction or ram feeding) have little use of

teeth, and seemingly less microwear. However, fish do not chew; therefore, the

mechanism of microwear feature production in aquatic animals is different than that of

terrestrial organisms. Adam and Berta (2002) found that microwear analysis was not

useful in paleodietary reconstruction of pinnipeds. One reason they believed microwear

was analytically impotent was because pinnipeds do not masticate their homogenous food

(Adam and Berta 2002). Research work of Taylor (1987) and Massare (1987) suggest Dental Microwear 15

most Mesozoic marine reptiles did not masticate either. However, the benefit of using

Mesozoic aquatic vertebrates is that variation in dietary hardness had extremes: soft-

bodied prey (e.g., squid and octopus); bony prey (e.g., large fish and smaller marine

reptiles); and hard-bodied, armored fauna (e.g., ammonites, belemnites, and clams).

Despite some additional limitations, DMA studies of some aquatic fauna have met

with success. Wear analysis was used to determine patterns of tongue movement of

walrus during feeding (Gordon 1984); walruses forage benthic shelled prey and in

captivity these animals have been observed using a suction feeding mechanism to extract

bivalve feet and/or siphons and to cast out the valves (Gordon 1984). Domning and

Beatty (2007) demonstrated that correlating functional and morphological change is difficult, but showed how microwear helped unravel the Gordian knot of detecting form- function changes of dugong tusks, and how these changes related to diet. Purnell et al.

(2007) showed that differences in microwear pattern and density of fossil stickleback correlated with different feeding types (e.g., benthic feeding vs. limnetic feeding).

Because sticklebacks provide high spatial and temporal resolution, feeding type differences were used to examine changes in paleoecology and food resources.

Methods for DMA developed by Solounis and Semprebon (2002) provide a good means for distinguishing between broadly defined feeding types (Grine et al. 2002).

There is a common theme in the discussion of many microwear study papers (Gosawami et al. 2005; Purnell et al. 2007; Teaford 2007; Townsend and Croft 2008) that across different microwear analysis methods and experimental designs, microwear analysis provides a good test for gross dietary observations of fossilized assemblages and their feeding type assessment. Dental Microwear 16

This is the first attempt to examine dental microwear of Mesozoic marine reptiles.

Work from this study correlates tooth wear patterns to predicted diet. Pierce-feeders foraging on soft prey should have little wear; cut-feeders should have medium wear; and crush-feeders should have substantial wear.

Dental Microwear 17

MATERIALS AND METHODS

Sampled taxa included representatives of three feeding types (i.e., crush-, cut-,

and pierce-type) as classified by Massare (1987). Taxa were selected to maximize

representation of these feeding types from specimens available at the visited museums.

There is a paucity of Mesozoic marine reptile specimens with teeth attached to the skull.

Most of the specimens examined were made from isolated teeth.

Replicas of selected Mesozoic marine reptile specimen were collected from: Fort

Hays Sternberg Museum of Natural History, Fort Hays, Kansas (FHSM); Kansas

University Natural History Museum, Lawrence, Kansas (KU); United States National

Museum of Natural History, Washington, D.C. (USNM); University of Oklahoma Sam

Noble Museum of National History Norman, Oklahoma (OMNH); Southern Methodist

University Shuler Museum, Dallas, Texas (SMU); and the Royal Ontario Museum

Toronto, Ontario, Canada (ROM).

Museum collection catalogs were examined to identify potential Mesozoic marine

reptile specimens with teeth (Table 1). On-site physical examination of each potential

specimen was necessary to assess the condition of each tooth and to eliminate specimens

with obvious taphonomic breakage and wear that would disrupt the molding process and

obscure microscopic examination.

Teeth suitable for molding were measured using Westward digital calipers to the

nearest 0.01 mm. Crown height and basal diameter of each tooth were measured and

recorded (Fig. 2 and Table 2). Specimens were photographed using a Canon PowerShot

with lens and flash adaptors specific for dental photography, or with a Nikon D90 with a

Speedlight SB-600 flash. Additional notes on crown morphology were made Dental Microwear 18

Table 1. Inventory of specimens sorted by museum accession numbers. MUSEUM ID ORDER FAMILY GENUS Feeding Type KU uncatalogued Sauria Mosasauridae Tylosaurus CUT KU 1178 Sauria Mosasauridae indet PIERCE KU 118936 Plesiosauria indet indet PIERCE KU 1300 Plesiosauria Polycotylidae Trinacromerum PIERCE KU 40001 Plesiosauria Polycotylidae Dolichorhynchops PIERCE KU 85502 Sauria Mosasauridae Platecarpus CUT KU 85585 Sauria Mosasauridae Platecarpus PIERCE KU 950 Sauria Mosasauridae Prognathodon CUT OHNH 1059 Sauria Mosasauridae indet PIERCE OMNH 01046 Sauria Mosasauridae Platecarpus PIERCE OMNH 01046 Sauria Mosasauridae Platecarpus PIERCE OMNH 1011 Crocodylia indet indet PIERCE OMNH 1061 Sauria Mosasauridae Platecarpus PIERCE OMNH 1061 Sauria Mosasauridae Platecarpus PIERCE OMNH 21455 Crocodylia indet indet PIERCE OMNH 23133 Crocodylia indet indet PIERCE OMNH 24486 Crocodylia indet indet PIERCE OMNH 35410 Sauria Mosasauridae indet PIERCE OMNH 35410 Sauria Mosasauridae indet CUT OMNH 35410 Sauria Mosasauridae indet CUT OMNH 64251 Crocodylia indet indet PIERCE ROM uncatalogued Ichthyopterygia Ichthyosauridae Ichthyosarus PIERCE ROM 00310 Placodontia Placohelyidae Placodus CRUSH ROM 00363 Nothosauria Nothosauridae Nothosaurus PIERCE ROM 00364 Nothosauria Nothosauridae Nothosaurus PIERCE ROM 00365 Nothosauria Nothosauridae Nothosaurus PIERCE ROM 00956 Ichthyopterygia Ichtyosauridae Ichthyosaurus PIERCE ROM 01860 Ichthyopterygia Ichthyosauridae Ichthyosarus PIERCE ROM 01872 Plesiosauria Pliosauridae Polyptycodon PIERCE ROM 05596 Plesiosauria Pliosauridae indet CUT ROM 11692 Phytosauria Phytosauridae Phytosaur PIERCE ROM 11692 Phytosauria Phytosauridae Phytosaur CUT ROM 11692 Phytosauria Phytosauridae Phytosaur PIERCE ROM 11692 Phytosauria Phytosauridae Phytosaur PIERCE ROM 11692 Phytosauria Phytosauridae Phytosaur CUT ROM 28549 Plesiosauria Pliosauridae Polyptycodon PIERCE ROM 28964 Ichthyopterygia Ichthyosauridae Ichthyosarus PIERCE ROM 28964 Ichthyopterygia Ichthyosauridae Ichthyosarus PIERCE (continued on next page) Dental Microwear 19

Table 1. (continued) MUSEUM ID ORDER FAMILY GENUS Feeding Type ROM 28964 Ichthyopterygia Ichtyosauridae Ichthyosaurus PIERCE ROM 3180 Ichthyopterygia Ichthyosauridae Stenoptergius PIERCE ROM 45694 Sauria Mosasauridae indet CUT ROM 47690 Plesiosauria Elasmosauridea indet PIERCE ROM 47690 Plesiosauria Elasmosauridea indet PIERCE ROM 47698 Ichthyopterygia Ichthyosauridae Leptonectes PIERCE ROM 52043 Crocodylia Dyrosauridae indet PIERCE ROM 52043 Crocodylia Dyrosauridae indet PIERCE ROM 52550 Sauria Mosasauridae Mosasaurus CUT ROM 52573 Sauria Mosasauridae Platecarpus CUT ROM 52574 Sauria Mosasauridae Platecarpus CUT ROM 52575 Sauria Mosasauridae Platecarpus CUT ROM 52597 Ichthyopterygia Ichthyosauridae Ichthyosarus PIERCE ROM 52598 Ichthyopterygia Ichthyosauridae Ichthyosarus PIERCE ROM 52694 Phytosauria Phytosauridae Phytosaur CUT ROM 52695 Phytosauria Phytosauridae Phytosaur PIERCE ROM 54516 Sauria Mosasauridae Globidens CRUSH ROM 54524 Sauria Mosasauridae Globidens CRUSH ROM 54526 Plesiosauria indet Plesiosaurus PIERCE ROM 54527 Plesiosauria indet indet PIERCE ROM 54527 Plesiosauria indet Plesiosaurus PIERCE ROM 54529 Sauria Mosasauridae Globidens CRUSH ROM 54551 Sauria Mosasauridae Mosasaurus CUT ROM54552 Sauria Mosasauridae Mosasaurus CUT SMU uncatalogued Sauria Mosasauridae Liodon CUT SMU 61113 Sauria Mosasauridae Tylosaurus CUT SMU 62410 Sauria indet Elasmobranch PIERCE SMU 69120 Plesiosauria Elasmosauridae Libonectes PIERCE SMU 72206 Sauria Mosasauridae indet PIERCE SMU 75374 Sauria Mosasauridae Tylosaurus CUT SMU 75586 Sauria Mosasauridae indet CUT SMU 76398 Sauria Mosasauridae Globidens CRUSH SMU 76399 Sauria Mosasauridae Globidens CRUSH SMU 76400 Sauria Mosasauridae Globidens CRUSH SMU 76401 Sauria Mosasauridae Globidens CRUSH SMU 75586 Sauria Mosasauridae indet PIERCE SMU 60314 Plesiosauria Elasmosauridae Polyptycodon PIERCE USNM uncatalogued Ichthysauria indet indet PIERCE (continued on next page) Dental Microwear 20

Table 1. (continued) MUSEUM ID ORDER FAMILY GENUS Feeding Type USNM 1 Sauria Mosasauridae Mosasaurus PIERCE USNM 10540 Sauria Mosasauridae Mosasaurus CUT USNM 11647 Sauria Mosasauridae Clidastes PIERCE USNM 11655 Sauria Mosasauridae Platecarpus PIERCE USNM 12287 Sauria Mosasauridae Tylosaurus CUT USNM 16153 Plesiosauria Polycotylidae Polyptycodon PIERCE USNM 16154 Plesiosauria Polycotylidae Polyptycodon PIERCE USNM 17909 Sauria Mosasauridae Tylosaurus CUT USNM 18255 Sauria Mosasauridae Mosasaurus CUT USNM 25444 Plesiosauria Pliosauridae Pliosaurus PIERCE USNM 336480 Sauria Mosasauridae Mosasaurus PIERCE USNM 3765 Sauria Mosasauridae Clidastes PIERCE USNM 3778 Sauria Mosasauridae Clidastes PIERCE USNM 418456 Sauria Mosasauridae indet PIERCE USNM 419635 Plesiosauria Pliosauridae Pliosaurus PIERCE USNM 421698 (cast) Placodontia Placohelyidae Macroplacus CRUSH USNM 421699 (cast) Placodontia Placohelyidae Cynamdus CRUSH USNM 421700 (cast) Placodontia Placohelyidae Placochelys CRUSH USNM 437572 Plesiosauria Polycotylidae Cimoliasaurus PIERCE USNM 437610 Sauria Mosasauridae Mosasaurus CUT USNM 437997 Sauria Mosasauridae Mosasaurus PIERCE USNM 437998 Sauria Mosasauridae Clidastes CUT USNM 4910 Sauria Mosasauridae Mosasaurus CUT USNM 4992 Sauria Mosasauridae Tylosaurus PIERCE USNM 535507 Plesiosauria indet indet PIERCE USNM 6086 Sauria Mosasauridae Tylosaurus CUT USNM 6527 (cast) Sauria Mosasauridae Globidens CRUSH USNM 76 Sauria Mosasauridae Lestosaurus PIERCE USNM 8086 Sauria Mosasauridae Mosasaurus PIERCE VP uncatalogued Sauria Mosasauridae Ectenosaurus PIERCE VP 13830 Sauria Mosasauridae Globidens CRUSH VP 13910 Sauria Mosasauridae Platecarpus CUT VP 15631 Sauria Mosasauridae Tylosaurus CUT VP 17017 Sauria Mosasauridae Platecarpus PIERCE VP 17314 Sauria Mosasauridae Platecarpus CUT VP 17576 Sauria Mosasauridae Clidastes PIERCE VP 7262 Sauria Mosasauridae Tylosaurus CUT Dental Microwear 21

Figure 2. Figure of tooth of Mosasaurus sp. (USNM 437998) showing measurements of crown height and basal width used to calculate height:base ratio.

Dental Microwear 22

Table 2. Tooth morphology characteristics as related to three feeding types predicted for Mesozoic marine reptiles.

Morphological Character CRUSH CUT PIERCE

Apex Shape very blunt Pointed pointed

Apex Wear coronal abrasions breakage common some breakage

Cutting Edges none usually two occasional

Crown-Basal Ratio < 1.0 1.3 – 2.5 1.3 – 4.3

Dental Microwear 23

from specimens, including apex shape, apical wear, and presence or absence of distinct cutting edges (Fig. 3-5 and Table 2).

Teeth were examined and cleaned with a soft brush or cloth to remove dust and debris. 3M Impression II polyvinyl siloxane impression material was injected into custom split ring polyvinyl chloride (PVC) coupling connectors of varying diameters (17, 20, 26, and 34 mm) corresponding to tooth basal diameter (Fig. 6) PVC rings provided a form for the molding material and allowed preservation of three-dimensional tooth structure. Each ring had unique index marks created with a Foredom series TX drill for aligning cured molding material into the ring for storage.

For teeth still associated with skulls or embedded in rock medium, PVC forms could not be used and impression peel molds were made from these teeth using polyvinyl siloxane impression material. Polyvinyl siloxane is a two-part syringeable paste that automixes as it is extruded through an application tip. This combined product was applied directly to the fossilized tooth. The advantage of polyvinyl siloxane product over traditional silicone molding materials is reduced mixing, working, and curing times

(Leiggi and May 1994). Polyvinyl siloxane product cures in approximately ten minutes, in contrast to many hours, without losing resolving detail.

When molding material had dried, specimens were extracted. The split PVC rings were opened and an incision was made into the polyvinyl siloxane mold approximately

0.25 mm from the labial tooth surface. Impression molds were stored at room temperature according to manufacturer specifications. Each study specimen was encased in the labeled PVC ring used in the molding process. Peel molds were stored in plastic bags. Dental Microwear 24

Figure 3. Tooth of Mosasaurus sp. (USNM 437998) showing position of the apex (shown is sharply pointed apex). Dental Microwear 25

Figure 4. Tooth of Mosasaurus sp. (USNM 437998) showing typical pre-mortem apical wear.

Dental Microwear 26

A B Figure 5. Teeth of (A) Mosasaurus sp. (USNM 437998) and (B) Mosasaurus sp. (USNM 481126) showing shape of a cutting edge under low (A) and high (B) magnification.

Dental Microwear 27

Figure 6. Injection of polyvinyl siloxane molding material into custom ring.

Dental Microwear 28

Leiggi and May (1994) found dental gypsum plaster to be a good casting compound for use in paleontological studies. Diekeen stone (Modern Materials

Manufacturing Company: Saint Louis, Missouri) was used to create study casts from polyvinyl siloxane tooth molds. Compatibility of polyvinyl siloxane and Diekeen stone has been tested by the American National Standards Institute (ANSI) and the American

Dental Association (ADA), who found that Diekeen cast material accurately reproduced

20 µm scratches from polyvinyl siloxane molding material (Schelb et al., 1987).

Therefore, I prepared casting material in the same manner: gypsum stone powder was added to water at a ratio of 100 mg of Diekeen powder to 21 ml of water. Diekeen powder was added to the water and hand-spatulated in a vacuum canister for 10 seconds.

This mixture was then vacuum-spatulated using a Vac U Vestor Power Mixer (General

Electric: Louisville, Kentucky) pressurized to 36,200 Torr and stirred at 1725 rpm.

Specimens were placed at an angle on a vibrating plate and the Diekeen mixture was loaded from the vacuum canister using a chemical spatula.

Polyvinyl siloxane molds loaded with the Diekeen casting stone (Fig. 7) were placed at ambient room temperature and allowed to cure overnight. Replica teeth were removed from the polyvinyl siloxane mold, and casts were stored for microscopic examination (Fig. 8). Molds were placed back into the PVC ring for archiving.

Casts were examined using a Keyence VHX-600 progressive scan digital reflective microscope (Fig. 9). A 1628 x 1236 charged-coupled device sensor on this scope provides a 2.11 million-pixel resolution image (Keyence 2007). Casts were illuminated using a unidirectional light with a 12 V, 100 W halogen lamp. Lingual surfaces of teeth (Smith and Dodson 2003) were examined and photographed with Dental Microwear 29

Figure 7. Diekeen stone poured into tooth mold. Dental Microwear 30

Figure 8. Tooth cast made of Diekeen cast material. Specimen shown is of Tylosaurus sp. (VP 7262).

Dental Microwear 31

Figure 9. Keyence VHX-600 Digital Reflective Microscope.

Dental Microwear 32

the microscope at 50X. Alpha chromatic and sharpening adjustments of virtual micropictographs produced greater definition of microwear object boundaries for more accurate visualization and identification. Analytical software embedded into the Keyence microscope also allowed for generation of a working graphics layer to overlay the micropictograph. Keyence graphic tools were used to create a virtual 24 square-grid comprised of 1 mm x 1 mm cells overlayed on tooth images.

Microwear features were classified as in Solounias and Semprebon (2002). Using parameters established by Grine (1987), microwear objects with a length-to-width ratio less than or equal to 4:1 were classified as pits. Pits are circular in nature and regular in appearance with sharp, discrete boundaries, and appear relatively bright (Fig. 10). Wear features with regular edges and a length to width ratio greater than 4:1 were categorized as scratches (Walker and Teaford 1989; Solounias and Semprebon 2002) (Fig. 11).

Gouges are discrete microwear features with jagged, irregular edges; gouges are typically larger and deeper than pits (Fig. 12).

Scratches, pits, and gouges were identified, counted, and digitally recorded from real-time images of positive casts. Observations were made from ten randomly selected 1 mm squares represented by the 24-cell grid superimposed over the lingual surface of the tooth. Random grid cell selections were made using a random number generator in

Microsoft Excel. Cells containing obvious taphonomic artifacts such as post-mortem breakage were avoided and another grid was selected. Microwear features encroaching upon right or bottom gridlines were not included in wear counts. The total number of pits

Dental Microwear 33

Figure 10. Lingual surface of Tylosaurus sp. (VP 7262) showing a typical pit microwear feature. Dental Microwear 34

Figure 11. Lingual surface of Globidens sp. (VP 13830) showing a typical scratch microwear feature.

Dental Microwear 35

Figure 12. Lingual surface of Platecarpus sp. (VP 13910) showing a typical gouge microwear feature.

Dental Microwear 36

and scratches were counted using the multiple selection tool from the Keyence graphics elements utility.

Absolute numbers of pits, gouges and scratches for individuals per feeding type and taxon were recorded in each of the ten selected cells. Counts from the ten squares were then averaged to obtain a mean number of pits and scratches per cast. These means were then averaged for all individuals per taxon to obtain a final average number of pits and scratches per taxon.

All data sets were tested for normality and homogeneity of variance using the

Shapiro-Wilks W normality test. Kruskal-Wallis non-parametric analysis of variance was used to assess differences among feeding types. Difference in: 1) pit densities; 2) scratch densities; 3) gouge densities; and 4) total microwear features were all tested. Mann-

Whitney U tests were employed to test for differences between feeding type pairs.

Statistical analyses were run using SYSTAT 11.0 (SYSTAT Software Inc.: Richmond,

California) with significance set at p ≤ 0.05.

Dental Microwear 37

RESULTS

This microwear study examined 16 crush-type teeth, 32 cut-type teeth, and 68

pierce-type teeth (Table 1) representing 7 orders, 9 families, and 25 genera (Table 3).

Feeding type was determined using four tooth crown characteristics: 1) shape of apex; 2)

apex wear; 3) presence or absence of cutting edges; and 4) ratio of crown height to basal

diameter. Parameters of tooth crown characteristics used to determine feeding type are

found in Table 2. There were more total microwear objects in crush-type teeth than cut-

type and pierce-type teeth. There was an average of 111 (standard error, SE = 9.74) total

microwear objects per crush-type tooth, 58 (SE = 7.86) average total objects per cut-type

tooth, and an average of 20 (SE = 4.61) total microwear objects per pierce-type tooth

(Table 4). Mean values of total microwear objects per tooth were not normally

distributed, as indicated by a Shapiro-Wilk test for cut-type (p = 0.02) and pierce-type (p

= 0.00) teeth (Table 5) thereby requiring non-parametric testing of mean differences.

Therefore, Kruskal-Wallis one-way analysis of variance was used to test for equality

between feeding types. Results of this test suggested that there were significant

differences (χ2 = 43.31, degrees of freedom, DF = 2, p = 0.000) in the number of total

microwear objects among the three feeding types (Table 6).

Follow-up Mann-Whitney U tests were employed to compare total microwear

object densities among feeding types. Three of these tests (i.e., crush- v. cut-type; crush-

v. pierce-type; and cut- v. pierce-type) revealed statistically significant mean differences

between all treatment group pairs (χ2 = 11.73, 33.92, and 16.21, respectively; DF = 1; p =

0.001, p = 0.000, p = 0.000, respectively; Table 7).

Dental Microwear 38

TABLE 3. Taxonomic summary of specimens. Taxa CRUSH CUT PIERCE AGGREGATE

Total Teeth 16 32 68 116

ORDER (2) (3) (6) (7) Crocodylia 0 0 7 7 Ichthyosauria 0 0 11 11 Nothosauria 0 0 3 3 Phytosauria 0 3 4 7 Placodontia 6 0 0 6 Plesiosauria 0 1 18 19 Sauria 10 28 25 63

FAMILY (3) (3) (8) (9) Dyrosauridae 0 0 2 2 Elasmosauridae 0 0 4 4 Ichthyosauridae 0 0 10 10 Mosasauridae 9 28 24 61 Nothosauridae 0 0 3 3 Phytosauridae 0 3 4 7 Placochelyidae 5 0 0 5 Placodontidae 1 0 0 0 Pliosauridae 0 1 4 5 Polycotylidae 0 0 5 5 Indet 1 0 12 14

GENUS (5) (6) (19) 25 Cimoliasaurus 00 1 1 Clidastes 01 4 5 Cynamdus 10 0 1 Dolichorhynchops 00 1 1 Ectenosaurus 00 1 1 Elasmobranch 00 1 1 Globidens 10 0 0 10 Ichthyosaurus 00 8 8 Leptonectes 00 1 1 Lestosaurus 00 1 1 Libonectes 00 1 1 Macroplacus 20 0 2 (continued on next page) Dental Microwear 39

Table 3. (continued) Taxa CRUSH CUT PIERCE AGGREGATE Mosasaurus 07 4 11 Nothosaurus 00 3 3 Phytosaur 03 4 7 Placochelys 10 0 1 Placodus 20 0 2 Platecarpus 06 6 12 Plesiosaurus 00 2 2 Pliosaurus 00 2 2 Polyptycodon 00 5 5 Prognathodon 01 0 1 Stenoptergius 00 1 1 Trinacromerum 00 1 1 Tylosaurus 08 1 9 Indet 0 6 16 22

Dental Microwear 40

Table 4. Summary of means and standard errors for crown:base ratios and microwear counts.

CRUSH CUT PIERCE

Independent AVG SE AVG SE AVG SE Variable Crown-Basal 0.62 0.09 1.78 0.06 2.30 0.08 Ratio Total Microwear 111 9.74 58 7.86 20 4.61 Features Pits 102 9.91 52 7.48 18 4.61 Scratches 4 1.83 4 1.14 2 0.43 Gouges 5 1.27 1 0.35 0 0.10

Dental Microwear 41

Table 5. Summary statistics of total objects, pits, scratches, gouges, and crown height to basal diameter ratio described by feeding type. Abbreviations: CI = confidence interval; SW = Shapiro Wilk; Dev = deviation.

CRUSH CUT PIERCE Total Total Total microwear microwear microwear

objects Pits Scratches Gouges objects Pits Scratches Gouges objects Pits Scratches Gouges N of cases 16 - - - 32 - - - 68 - - - Minimum 50 50 0 0 0 0 0 0 0 0 0 0 Maximum 190 178 27 18 199 199 45 12 281 281 18 6 Range 140 128 27 18 199 199 45 12 281 281 18 6 Sum 1772.5 1626 71 75.5 1914.5 1734 133 47.5 1385 1241 129 15 Mean 110.781 101.63 4.438 4.719 59.828 54.188 4.156 1.484 20.368 18.25 1.897 0.221 95% CI 131.547 122.75 8.329 7.432 77.874 71.733 7.205 2.607 29.572 27.451 2.753 0.425 Upper 95% CI 90.016 80.502 0.546 2.005 41.783 36.642 1.108 0.361 11.163 9.049 1.041 0.016 Lower Std. Error 9.742 9.91 1.826 1.273 8.848 8.603 1.495 0.551 4.611 4.609 0.429 0.102 Standard 38.97 39.642 7.303 5.092 50.051 48.664 8.455 3.115 38.026 38.011 3.537 0.844 Dev Variance 1518.632 1571.5 53.329 25.932 2505.139 2368.22 71.491 9.701 1445.96 1444.8 12.512 0.712 Skewness 0.305 0.36 2.245 1.201 0.841 1.093 3.942 2.483 5.359 5.509 2.733 5.395 Kurtosis -0.387 -0.927 5.647 1.561 0.687 1.376 18.221 5.694 34.081 35.396 8.279 33.815 SW 0.98 0.947 0.673 0.858 0.92 0.898 0.521 0.554 0.447 0.417 0.604 0.288 Statistic SW P- 0.963 0.442 0 0.018 0.021 0.006 0 0 0 0 0 0 Value Dental Microwear 42

Table 6. Kruskal-Wallis one-way analysis of variance results comparing microwear features among feeding types. Total Objects Pits Scratches Gouges

Kruskal-Wallis Not one-way ANOVA Significant Significant Significant test Significant p value (p = 0.000) (p = 0.000) (p = .309) (p = 0.000)

Dental Microwear 43

Table 7. Mann-Whitney U test results of paired feeding type differences in microwear features. Mann-Whitney U Total Objects Pits Gouges

Pierce v. Cut Significant Significant Significant p value (p = 0.000) (p = 0.000) (p = 0.006)

Pierce v. Crush Significant Significant Significant p value (p = 0.000) (p = 0.000) (p = 0.000)

Cut v. Crush Significant Significant Significant p value (p = 0.001) (p = 0.001) (p = 0.007)

Dental Microwear 44

In addition to total microwear objects, there were differences in the number of pits, gouges, and scratches. Pitting density trends between the three feeding types followed the same pattern as total microwear objects. There was an average of 102 (SE =

9.91) pits per crush-type tooth, 52 (SE = 7.48) per cut-type tooth, and an average of 18

(SE = 4.61) per pierce-type tooth (Table 4). Mean pit values of cut-type (p = 0.00) and

pierce-type (p = 0.00) teeth failed a Shapiro-Wilk test (Table 5) of normality; therefore, a

Kruskal-Wallis test was used to evaluate differences in pit density. Results suggested a significant difference (χ2 = 42.87, DF = 2, p = 0.000; Table 6).

Mean pit density differences were tested among feeding type pairs. Statistically

significant differences were detected using Mann-Whitney U tests (i.e., crush- v. cut-

type, χ2 = 11.06; DF = 1, p = 0.001; crush- v. pierce-type, χ2 = 33.92; DF = 1, p = 0.000;

cut v. pierce, χ2 = 16.21; DF = 1, p = 0.000); (Table 7).

Gouge density patterns were also significantly different for feeding types;

however, gouge density trends are different than trends observed in total microwear or

pitting. There was an average of 5 (SE = 1.27) gouges per crush-type tooth, 1 (SE = 0.35)

gouge per cut-type tooth, and 0 (SE = 0.10) gouges per pierce-type tooth (Table 4). Mean

gouge values of cut- (p = 0.000) and pierce-type (p = 0.000) teeth were not normally distributed according to a Shapiro-Wilk W test (Table 5). Kruskal-Wallis results indicated a significant difference among feeding types (χ2 = 29.38, DF= 2, p = 0.000);

(Table 6).

Differences in gouge density were tested among feeding type pairs. All three

Mann-Whitney U tests confirmed significant difference due to feeding type (i.e., crush- v. Dental Microwear 45

cut-type, χ2 = 7.239; DF = 1, p = 0.007; crush- v. pierce-type, χ2 = 30.09; DF = 1, p =

0.000; cut- v. pierce-type, χ2 = 7.795; DF= 1, p = 0.006); (Table 7).

Scratch density proved less capable of differentiating feeding type. There was an average of 4 (SE = 1.83) scratches per crush-type tooth, 4 (SE = 1.14) per cut-type tooth,

and 2 (SE = 0.43) per pierce-type tooth (Table 4). Mean scratch values of cut- (p = 0.00)

and pierce-type (p = 0.00) teeth were not normally distributed (Shapiro-Wilk W test;

Table 5). Kruskal-Wallis one-way analysis of variance, however, did not indicate

significant mean differences (χ2 = 2.35; DF = 2, p = 0.31) between feeding types (Table

6).

In sum, data suggest that there are significant differences between total number of microwear objects, pitting, and gouging densities. No statistical difference between scratch densities in crush-, cut-, and piece-type teeth was detected.

Dental Microwear 46

DISCUSSION

Feeding type had a statistically significant effect on the total microwear object density in Mesozoic marine reptile teeth (χ2 = 43.31, DF = 2, p = 0.000; Table 6). Results

were consistent with predictions derived from Massare’s (1987) tooth form and function

paradigm used to predict prey foraged and consequent correlation with dental microwear.

Predictions derived from Massare’s (1987) work include that pierce feeding specimens

consumed soft-bodied prey (e.g., squid and octopus), thus creating minimal dental

microwear objects. Crush-type teeth were optimal for feeding on hard-bodied, armored

fauna (e.g., ammonites, belemnites, and clams) and were predicted to have heavy wear.

Cut-type feeders had teeth specialized for foraging bony prey (e.g., large fish and smaller

marine reptiles) creating microwear densities between the two extreme feeding types of

pierce- and crush-types.

Crush-type teeth had higher average microwear objects per tooth (111) than cut-

(58) or pierce-type (20) teeth (Table 4). Dental microwear is a form of abrasive and attritional wear in that the enameled, hardened tooth crown surface interacts with some other material. Microwear-forming material might include occluding teeth, ingested food material, or environmental substrate. Abrasional (formed by tooth-food and tooth- substrate interactions) and attritional (formed by tooth-tooth interactions) microwear features are formed by these interactions (Beatty 2005; Green 2009). Increased total microwear densities suggest that these teeth had more interaction with wear-forming material bearing sufficient force for formation of microwear.

Massare (1987) used tooth crown morphology, stomach content analysis, and diet correlation of extant specimens with similar tooth form to predict prey resources Dental Microwear 47

available to and eaten by animals in each feeding type. She used observations on skull

structure and tooth morphology of crush feeders to infer a hard, armored prey diet. No

stomach content observations of crush feeders were available to Massare, but others

found bivalves in the stomach contents of Globidens skeletons (Martin 1994; Martin and

Fox 2004). I found abundant microwear (avg = 114) on Globidens teeth. No extant taxa

comparison was made by Massare (1987) for crush-type feeding. Taylor (1987) explains

that some extant aquatic tetrapods – like freshwater turtles and walruses – feed on hard- bodied invertebrates. Stomach content analyses of walruses show they consume bivalves

(Gordon 1984) as did benthic predators such as Globidens and placadonts included in my

microwear study. Walruses have molariform teeth with flat or bulbous occlussial surfaces

specialized for crushing prey (Taylor 1987). Although not molariform per se, molars

have a low crown height to basal diameter ratio similar to Globidens and placadont teeth.

Bivalves, gastropods, and armored cephalopods provided Mesozoic marine reptiles with hard-bodied prey that would have inflicted significant tooth-food abrasion.

Significant tooth-to-hard-bodied food interaction likely produces more microwear features in dental tissue compared with soft-bodied prey foraged upon by other feeding

types. Having established a significant difference between total microwear object

densities of crush, cut, and pierce teeth – what kind of features (e.g., pits, scratches, and

gouges) might interaction with hard-bodied prey produce on teeth of these three types?

Crushing teeth were the most pitted and most gouged, but the three tooth types

had similar numbers of scratches. Mean pitting and gouge densities between feeding

types had significant mean variances (χ2 = 42.87, DF = 2, p = 0.000 and χ2 = 29.38, DF =

2, p = 0.000, respectively). My results show crush-type teeth averaged 48.39% more Dental Microwear 48

pitting than cut-type teeth and 82.04% more pits than pierce-type feeders (Table 4).

These differences are likely attributable to varying interactions with hard food items (e.g.,

shells and bones). Average crush-type teeth had 76.77% more gouges than cut feeders

and averaged 95.67% more gouges than pierce-type teeth (Table 4).

These observations are paralleled in terrestrial vertebrates. Microwear analysis of

hyraxes and primates has shown a relationship between food properties and scratch

densities (Walker and Teaford 1989). Animals that consumed food items like hard fruit

had more microwear pits than herbivorous foragers (Calandra et al. 2010). Van

Valkenburgh et al. (1990) compared hyena (bone-consuming) with cheetah (non-bone

consuming) microwear and found a high pit-to-scratch ratio in hyenas. Among the

Mesozoic marine reptiles of my study, highest pit:scratch ratios were found in crush- and

cut-type teeth.

Mesozoic marine reptiles formed part of a predatory guild partitioning food resources from the water column and benthos (Massare 1987). Pitting is the predominant microwear feature found on the surface of carnivore teeth (Goswami et al. 2005). My study confirmed this: there were significantly more pits (102) than gouges (5) or scratches (4) (Table 5) found on the surface of crush-type teeth of Mesozoic marine reptiles. The pit-to-scratch ratio of crush feeders is approximately 25:1. This high pitting ratio is also consistent with a carnivorous diet in terrestrial predator guilds eating hard

prey (Teaford 1988; Van Valkenburgh et al. 1990). High pit-to-scratch ratios likely

reflect ingestion of harder food items.

Scratch wear features were not abundant on examined Mesozoic marine reptile teeth (4 scratches per examined area on crush-type teeth; 4 scratches per examined area Dental Microwear 49

on cut-type teeth; 2 scratches per examined area on pierce-type teeth). Additionally, mean

scratch densities were not found to be statistically different between feeding types (χ2 =

2.35, p = 0.31; Table 6). There was less than a 4% difference between the average number of scratches on crush- and cut-type teeth. The difference between scratches of crush- and pierce-type feeders, however, was 57.11% (Table 4).

If all Mesozoic marine reptiles in this study were ancient carnivores and carnivores usually have high pitting densities, then why is there such a paucity of pitting scribed on the enamel surface of pierce-type teeth? In fact, tooth surfaces examined suggest there is significantly less pitting on pierce-type teeth (18) than crush- (102) or cut-type teeth (52) (Table 4). However, just because pierce feeders have a carnivorous diet does not necessarily translate to the presence of microwear pitting, as microwear pit formation occurs from tooth interaction with hard food or substrate material. Pierce-type feeders had a tooth morphology specialized for preying upon soft-bodied fauna. They had a pointed tooth apex with varying degrees of apical breakage and abrasive wear (Massare

1987). Most soft-bodied cephalopods like squid and octopus do not have hard food parts with which teeth can interact; therefore, although pierce feeders were likely carnivorous, it is plausible that their foraging likely did not usually produce microwear. However, there were significant microwear features observed on the surface of some pierce teeth

(e.g., ROM 52695 Phytosaur with 281 total microwear objects – the most objects found on a tooth from any feeding type; ROM 28549 Pleisosaur with 123 total microwear objects; OMNH 01046 Platecarpus with 99 total microwear objects; and OMNH 1011

Crocodylia with 28 total microwear objects). There are several possible reasons for this observed variation in microwear among pierce-type feeders. Some of these teeth (i.e., Dental Microwear 50

OMNH 1011) were difficult to assign to a single feeding category. Their tooth

morphology seemed to rule out cut- and crush-type feeding because there are no cutting

edges. Further difficulty in classifying teeth was caused by an unusual crown-

height:diameter ratio.

Morphological characters were based on Massare (1987); however, these

characters are in gradients and some diagnostic values overlap. For example, the ratio of

pierce-type crown height to basal diameter ranges from 1.3 – 4.3, while cut-type ranges

from 1.3 – 2.5 (Table 2). Most Phytosaur and Platecarpus teeth examined from the

pierce-type feeders had two cutting edges suggesting some analogy with cutting-type

teeth. Therefore, some teeth designated as pierce-type have some characteristics (e.g., robust base and cutting edges) to process bony prey. Predation on bony prey creates microwear not formed from soft-bodied animal consumption.

There are other possible causes for dental microwear variability. Diet variability within phylogenetically and morphologically contrived groups affects potential microwear formation. Several factors affect foraging behavior and prey selection even within a particular species. For example, seasonal changes of food item availability, dietary resources available within an occupied microhabitat, and fall-back food items in times of resource scarcity all potentially contribute to dentition microwear variability

(Scott et al. 2005, Galbany et al. 2009). Nonetheless, the general picture is clear: crushing-type teeth tend to be more damaged than the other types.

Cut-type feeders had less pitting (52) than crush-type feeders (102) but more than pierce-type feeders (18) (Table 4). These differences suggest cut-type feeders had less hard material in their diet than did crushers; however, observed pitting in cut-type feeders Dental Microwear 51

suggests there was significant interaction with hard food items. Paleodietary and tooth form analysis suggests cut-type feeders had prey resources not utilized by pierce-type feeders. Stomach contents of one Tylosaurus contained bones from a bird, bones of a smaller Clidastes mosasaur, and shark teeth (Everhart 2005). Additionally, members of the cutting class preyed on large fish (Williston 1898; Massare 1987), smaller

Platecarpus (Everhart 2008), and plesiosaurs (Everhart 2004). These food items contained substantial amounts of bone for tooth. Functional studies indicate that craniokinetic joints between tooth-bearing bones of cut-type feeders allowed initial puncture of large prey and then back-and-forth ratcheting of prey as they were processed and swallowed (Taylor 1987; Everhart 2005). Tooth-bone abrasion that occurred as prey were processed in the mouth likely formed microwear pits.

Some teeth categorized as cut-type feeders showed little to no microwear objects on the examined tooth surface (i.e., USNM 4910 Mosasaurus, ROM 52574 Platecarpus, and SMU 75586 Mosasauridae had no microwear features). Although cut-type feeders had a tooth morphology specialized for consuming bony prey, food resources available to the individual might not reflect the fauna available to it as suggested by tooth form. For example, it is possible that Mesozoic marine reptiles with cut-type teeth forged in biozones with abundant soft-bodied prey. In these instances, dentition may not significantly interact with the microwear-forming prey materials. Another possible reason for less wear than predicted is weathering effects when a fossil becomes exposed in sedimentary rock. King et al. (1999) and Goswami et al. (2005) found that physical and chemical weathering tends to obliterate microwear features rather than creating new microwear artifacts Dental Microwear 52

Despite some problems, (e.g., different analysis methods and experimental designs) microwear analysis allows inference of gross dietary observations of fossilized predators (Gosawami et al. 2005; Purnell et al. 2007; Teaford 2007; Townsend and Croft

2008).

Experimental results from my study show significant differences in dental microwear densities between crush-, cut- and pierce-type feeders of Mesozoic marine reptiles (Tables 6 and 7). An important source of microwear is interaction with hard food items in the diet. This study provides strong support for using dental microwear as an independent test of diet as predicted from tooth morphology in Mesozoic marine reptiles.

Good methods for paleoecological and paleodietary reconstruction are limited.

Future research examining dental microwear of Mesozoic marine reptiles might consider biostratigraphical relationships of specimens for greater understanding of the paleoecological context of these ancient marine reptiles. This higher resolution examination might indicate shifts in available prey resources through time. Additionally, future work might examine microwear variation within abundantly recovered species to assess within-species range of diet. For example, while most Tylosaurus teeth have a significant number of microwear objects, some Tylosaurus teeth (i.e., VP 15631) lack significant numbers of microwear features. Wear of anterior-posterior striae likely is not reduced by consumption of a soft-bodied prey diet; however, weathering likely mutes attrition microwear and striae alike. Correlating microwear density with striae wear might help clarify the source of reduced microwear objects in teeth with specialized crown morphology for processing hard or bony prey. Finally, these teeth could be re-examined using a confocal microscope to create a three-dimensional map of a tooth surface. Dental Microwear 53

Geographical Information System (GIS) tools could then be used to quantify feature dimensions and then analyzed to see if more information about the diet of these Mesozoic marine reptiles may be gleaned.

Dental Microwear 54

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ACKNOWLEDGEMENTS

I returned to Northwest Missouri State University to work on a Master’s degree in preparation for dental school which I begin the fall 2011. I sought a research project that afforded me the opportunity to think about teeth and work with dental materials and tools. A journey that started for me in the study of ancient teeth has culminated in an appreciation for what these teeth might be able to tell us about the story of aquatic life in the Mesozoic.

I am thankful for many people helping to make this journey possible. First and foremost I give thanks to my thesis advisor, Peter J. Adam. He was instrumental in my achievement of two goals. The first was to gain admittance to dental school. The second was to leave the graduate program a more educated scientist and a more effective communicator. Adam understood that being a good advisor is a delicate balance of knowing when to listen and encourage and when to be the adversary and critic. I am thankful for both his academic expertise and professionalism as well as his friendship.

I am thankful for the many people at the museums where I did research for allowing me to study and make molds of the Mesozoic marine reptile teeth: Larry Martin and David Burnham at the University of Kansas Natural History Museum; Michael

Everhart at the Sternberg Museum of Natural History at the Ft. Hayes State University;

Michael Brett-Surman and Steve Jabo at the Smithsonian United States National Museum of Natural History; Richard Cifelli and Jennifer Larsen at the Sam Noble Museum of

Natural History at the University of Oklahoma; Louis Jacobs, Dale Winkler, and Mike

Polcyn at the Shuler Museum at Southern Methodist University; and to Kevin Seymour and Brian Iwama at the Royal Ontario Museum. Dental Microwear 62

I gratefully acknowledge the funding sources that made my thesis work possible:

Dean Gregory Haddock and the NWMSU Graduate School; Gregg Dieringer and the

Department of Biology; Dean Charles McAdam and the College of Arts and Sciences at

NWMSU. My father, Phil Poynter, provided dental molding and casting material used for this research work and allowed me to use laboratory space for specimen casting.

For this thesis I would like to thank my committee members: Peter Adam, Kurt

Haberyan, and John Pope for their time and interest toward this thesis and for their insightful questions during my oral defense. Additionally, I thank Peter Adam, Erick

Bourassa, and Rafiq Islam for challenging me with rigorous comprehensive exam questions.

I thank Phil Lucido for conversation and support that resulted in my return to graduate school at NWMSU and serving as the biology graduate student advisor. I give thanks to Lisa Crater for support and friendship. My appreciation goes to Michelle Allen for suggesting I consider using the digital reflective microscope for this microwear research. My friend Loren Baxter provided valuable editorial assistance in formatting the thesis. My time at NWMSU was enriched by colleagues and friends in the Adam lab reading group including Clint Coffey, Aaron Welch, and Ginger Fleer. Additionally, I am grateful for the excellent preparation and support I received from the faculty of the biology and chemistry departments at NWMSU.

Lastly, I’d like to thank my family for their love and encouragement. My parents raised me to be curious and supported me in all pursuits. My father was crucial in creating the successful molding techniques of teeth, was my research colleague on trips to museums in Kansas and Washington, D.C., and guided my comparison of the teeth of Dental Microwear 63

Mesozoic marine reptiles and humans. My grandparents, uncles and aunts, and in-laws supported us in numerous ways from research consultation and brainstorming to cooked meals and childcare. My wife Wendy and children Julia and Miles are the loves of my life and the reason for making cross-country moves and career changes. My deep gratitude goes to them for their steadfast love and support. The journey is worth walking with them beside me.