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Dietary Consistency and Sutural Morphology: The Complexity of the Mid-Palatal Suture in Procolobus badius and Colobus po...


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DIETARY CONSISTENCY AND SUTURA L MORPHOLOGY: THE COMPLEXITY OF THE MID-PALATAL SUTURE IN Procolobus badius AND Colobus polykomos By JENNIFER LANE HOTZMAN A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLOR IDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF ARTS UNIVERSITY OF FLORIDA 2004

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Copyright 2004 by Jennifer Lane Hotzman

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iii ACKNOWLEDGMENTS I would like to take this oppor tunity to thank Dr. Scott McGraw for allowing me to use his collection of specimens housed at Ohio State University. I also would like to thank Dr. David Daegling (University of Flor ida) for all of his guidance and advice throughout this project. My fellow colleagues Ron Wright and Joe Hefner also offered assistance throughout a difficult pe riod and helped me to probl em shoot certain aspects of this project. Lastly I would like to thank my parents, Malcolm Hotzman and Linda Petty, as well as Benjamin Ripy for their continue d support and encouragement. This project would not have been possible without the help and support I received from all of these individuals.

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iv TABLE OF CONTENTS page ACKNOWLEDGMENTS.................................................................................................iii LIST OF TABLES.............................................................................................................vi LIST OF FIGURES..........................................................................................................vii ABSTRACT.....................................................................................................................vi ii CHAPTER 1 MECHANICS IN BONE GROWTH...........................................................................1 Wolff’s Law..................................................................................................................1 Concepts of Stress and Strain.......................................................................................4 Primary and Secondary Cartilages................................................................................5 Bone Modeling and Remodeling..................................................................................6 Effect of Dietary Cons istency on Bone Growth.........................................................11 2 GROWTH OF THE PALATE....................................................................................16 Embryological Growth and Development..................................................................16 Postnatal Growth and Development...........................................................................18 3 SUTURES...................................................................................................................22 Functions of Sutures...................................................................................................22 Sutural Biology and Morphology...............................................................................24 Sutures and Loads.......................................................................................................27 4 ECOLOGY AND DIET OF COLOBUS MONKEYS...............................................30 Background Information.............................................................................................30 Study Sample..............................................................................................................31 5 FRACTAL ANALYSIS.............................................................................................33 Box Dimension and Information Dimension Methods...............................................34 Ruler Dimension.........................................................................................................35

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v 6 MATERIALS AND METHODS...............................................................................36 7 RESULTS...................................................................................................................39 8 DISCUSSION.............................................................................................................52 9 CONCLUSION...........................................................................................................58 LIST OF REFERENCES...................................................................................................60 BIOGRAPHICAL SKETCH.............................................................................................67

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vi LIST OF TABLES Table page 1 Definitions of measurements collected....................................................................36 2 Basic statistics for variables associated with Colobus polykomos ...........................40 3 Basic statistics for variables associated with Procolobus badius ............................41 4 Bootstrapped versus parametric means for ruler fractal dimension.........................43 5 Boostrapped versus parametric mean s for information fractal dimension...............43 6 Significant regressions.............................................................................................43 7 Fractal dimensions of Colobus polykomos ...............................................................44 8 Fractal dimensions of Procolobus badius ................................................................45 9 Box dimensions for Procolobus badius ...................................................................56 10 Box dimensions for Colobus polykomos ..................................................................57

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vii LIST OF FIGURES Figure page 1 V principle of bone remodeling............................................................................19 2 Box plot for ruler fractal dimension.........................................................................42 3 Box plot for information fractal dimension..............................................................42 4 Mid-palatal suture of Procolobus badius 2107........................................................46 5 Mid-palatal suture of Procolobus badius 9433........................................................47 6 Regression of ruler versus information dimension..................................................48 7 Mid-palatal suture of Procolobus badius 227..........................................................49 8 Mid-palatal suture of Procolobus badius 942..........................................................50 9 Mid-palatal suture of Colobus polykomos 2103.......................................................51 10 Regression of ruler versus box dimension. ..............................................................57

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viii Abstract of Thesis Presen ted to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Arts DIETARY CONSISTENCY AND SUTURA L MORPHOLOGY: THE COMPLEXITY OF THE MID-PALATAL SUTURE IN Procolobus badius AND Colobus polykomos By Jennifer Lane Hotzman August 2004 Chair: David Daegling Major Department: Anthropology The mechanical environment is one of many influential factors affecting craniofacial growth and development. Although the mechanism is unclear, consensus exists that loads elicit a morphogenetic re sponse from bone in general, including the maxillary bone in the craniofacial region. Mastication is one of the major sources of loading for the facial and cranial regions. Th e morphology of cranial and facial sutures is thought to be affected by the loading environment to which it is exposed. If this is true, then dietary consistency, which requires chan ges in the mechanics of mastication, should also affect the morphology of sutures. The hypothesis under construc tion is that the higher the loads the suture is exposed to, the more complexity the suture should exhibit. In order to test this hypothesis, the mid-palatal suture of two sympatric species of colobus monkeys was examined. One species ( Colobus polykomos ) has a particularly hard seed present in its diet that Procolobus badius does not have. If the a bove hypothesis is true, then Colobus

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ix polykomos would be expected to have a more complex mid-palatal suture due to its requirement of producing larger masticatory forces than Procolobus badius. Fractal analysis was used to measure the complexity of the sutures. Once the fractal dimensions were obtained, a 2-wa y ANOVA was performed, separati ng the species as well as the sexes. There were no significant differences in the complexities of the mid-palatal sutures of the two species. The data collected do not support the hypothesis that masticatory changes associated with diet directly influence sutural complexity.

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1 CHAPTER 1 MECHANICS IN BONE GROWTH Craniofacial growth and development is influenced by many different factors, including the mechanical environment (Herri ng 1993). The maxillary bone, in particular the palate, is more than likely exposed to di fferent types of loads throughout the earliest stages of growth. For example, human infants suckle and as they grow older, are weaned and then engage in mastication. These differe nt activities likely re sult in different types and magnitudes of stress, which elicit a mo rphogenetic response from the bone (Herring 1993, Martin et al. 1998). When mastication be gins, the consistency of the diet has been shown experimentally to affect craniofacial growth and development (Beecher et al. 1983, Kiliaridis et al. 1985, Yamamoto 1996, Ciochon et al. 1997). In addition to affecting overall bone grow th and development, masticatory loads may also influence the morphology of crania l sutures. Several researchers have postulated that sutural morphology can reflect th e load history of the structure in question (Herring 1972, Herring and Teng 2000, Wagemans et al. 1988). Provided this is the case, then the morphology of the suture s located in the palate should reflect its load history. If development is mechanically mediated, su tural morphology could pr ovide insight into possible etiologies for abnormal craniofacial de velopments such as cleft lip and palate, a common birth defect requir ing surgical intervention. Wolff’s Law The idea that bone adapts to its mechanical environment is not new. Julius Wolff has been credited with formulating this idea in the late 1800s, but th e idea has been traced

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2 as far back as Galileo in the 1600s (Martin et al. 1998). Wolff’s law states that the architecture of living bone c ontinuously adapts to changes in the mechanical environment to which bone is subjected. Although Wolf f’s law is generally accepted as true, the biological aspects of the law that he formulat ed have proven to be false (Dibbets 1992). Three main biases exist in his arguments: hi s theory on interstitial bone growth, the role of heredity in bone growth, and hi s concept of function (Dibbets 1992). Wolff was convinced that bone growth underwent the same mechanisms as soft tissue growth, which is to say that bone grow th consisted solely of cell division and the accumulation of intracellular material. He adamantly denied the process of remodeling because he did not believe that bone actually resorbed. Dibbets (1992) points out that the reason Wolff held so firmly to this concept of interstitial bone growth was because, in his view, the trabecular architecture preexisted in the compacta (cortical bone) and was not the result of a dynamic process. The idea that trabecular bone architecture was in herited was based on the fact that Wolff had observed the distinct trabecular patterns in fetuses, which could not have been exposed to loads yet (Dibbets 1992). However, the fetus is exposed to mechanical forces in utero Forces are intermittently imposed on the fetus by skeletal tissue stresses that are caused by muscular contractions from the increasingly strong a nd active developing muscular system (Carter and Beaupre 2001). Wolff’s concept of function is the third bias because the definition he provided differs greatly from how function is usually defined today. If resear chers were asked to define the term function today, they would proba bly define it as cha nging structure, i.e. a dynamic process requiring action (Wainwright 1988). Wolff de fined function as a static

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3 requirement that needed to be met (Dibbets 1992). Unfortunately, the term function is often not explicitly defined by researchers, which causes ambiguity as to exactly which definition of function is being applied. If Wolff defined function completely diffe rently than it is defined by most today, where did the modern day definition develop? The answer is from one of Wolff’s contemporaries, Wilhelm Roux. Roux saw function as a dynamic interaction as opposed to a static constraint and recognized that information for the developing bone was partially provided by loading and unloadi ng (Dibbets 1992). He referred to the physicochemical processes that aid deve lopment as “Entwicklungsmechanik” or “developmental mechanics” (Carter et al. 1998). The forces that affect skeletogenesis can be studied at different scales of analysis, including the molecular, cellular, tissue, and organ leve ls (Carter and Beaupre 2001). In the time period in which Wolff and Roux wo rked, the analyses generally took place on the tissue level due to lack of technology. As technologica l advances are made, more studies are conducted at the molecular and cellu lar levels (Carter et al. 1998). Molecular level studies have begun to st udy the role of integrins, wh ich are cell surf ace receptors involved in cell adhesion to other cells and the extracellular matrix, and the cytoskeleton, while cellular studies have shown that hydros tatic pressure and sh ear loading of cells have a direct influence on gene expression a nd cell biosynthesis (Car ter et al. 1998). The tissue level, however, is still the scale at which most analyses occur, including the one conducted here. One reason for this is because the technology needed to conduct tissue level analyses is generally more accessible th an the technology needed for cellular and molecular studies. Analyses can also be c onducted at the organ leve l, but they provide

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4 little insight into the underlying mechanisms of how bone responds to different mechanical conditions (Carter and Beaupre 2001 ). Only when the organs are broken down into smaller units, e.g., tissues, can we begin to evaluate and understand the physical conditions of connective tissue cells (Carter and Beaupre 2001). Concepts of Stress and Strain Two very important concepts that are us eful when studying mechanical forces at the tissue level are stress a nd strain. When discussing st ress and strain in biological materials, it is important to keep in mind that they are defined as if the tissue under study, in this case bone, was a homogenous material (Carter et al. 1998). In this “continuum model” representation, the fact that bone consists of mol ecules, discrete atoms, and crystals interacting with one another is ignored (Carter a nd Beaupre 2001). This means that the material properties represent average properties over some volume that is large in comparison to the microstructural features of the tissue (Car ter and Beaupre 2001). Stress is a measure of normalized intensity of a force and is the load per unit area, while strain is a measure of normalized load deformation. Strain, in simplest terms, is defined as the fractional change in dimension of a loaded body (Martin et al. 1998). Both stress and strain are tensor quantities, so th ey have a magnitude and direction. The stress state can also be represented with scalar quan tities referred to as invariants. Scalar quantities have a magnitude, but no directi on. The two most common stress invariants are referred to as hydrostatic stress and octahe dral shear stress. Hydrostatic stress can either be positive (hydrostatic tension) or negative (hydrostatic compression or pressure) and is calculated as the average value of the three principal stresses. On the other hand, octahedral stress can only be a positive num ber and will only change the shape and not the volume of the material in question (Car ter and Beaupre 2001). These two stress

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5 invariants affect cartilage growth and ossifi cation differently. Octa hedral shear stress causes an acceleration of cart ilage growth and ossification, while hydrostatic compressive stress slows it down (Car ter and Beaupre 2001). Primary and Secondary Cartilages Primary and secondary cartilages are both important to skull growth. These two cartilages are distinguished based on the timi ng of their formation. Primary cartilage precedes the development of the replacement bones that form the primary skeleton. Secondary cartilage is different because it does not form on dermal bones until after intramembranous ossification has begun (Hall 1984). Unlike most of the bones in the human skeleton, dermal bones are not preforme d in cartilage, but arise directly from connective tissue membranes. When studying th e influence of mechanics on craniofacial growth, the secondary cartilage is important because it does not develop in the absence of mechanical stimulation (Herring 1993). S econdary cartilage only differentiates from progenitor cells in response to mechanical stimulation (Hall 1984). This cartilage is found in association with many cranial bones, sutures, and the upper and lower alveolar processes in mammals. These locations are sites of either articulations or muscle attachments, which provides support for the idea that mechanical stimulation is necessary for the differentiation of seconda ry cartilages (Herring 1993). The mandibular condyle is the only major growth site of secondary cartilage anywhere in the mammalian skeleton (Herri ng 1993); therefore most of the studies on jaws have been on the condyle (Simon 1977, Copray 1985, Throckmorton and Dechow 1994). However, the condyle is not the only secondary cartila ge that is sensitive to mechanical changes in the environment. Hinton (1988) studied the response of the cartilage that is present in the mid-palatal su ture to changes in masticatory function. He

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6 divided rats into separate groups based on di etary consistency and/or incisor amputation, then performed biochemical and histological an alyses. Dietary consis tency and/or incisor amputation did alter the morphology and the me tabolism of the mid-palatal suture to varying degrees. The group of rats that were fed a soft diet a nd had their incisors amputated were affected the most, with th eir sutures becoming largely fibrous. The effect of dietary consistency on bone growth will be discussed in more detail later. Bone Modeling and Remodeling There is consensus that the mechanical environment affects bone growth, but how is another story. Several factors are i nvolved when discussing the mechanical environment, such as the frequency of the loading and the types of loads applied. Bone growth and modeling are not the only processe s that the loading conditions affect. Bone remodeling is also heavily influenced by mechanical conditions. Bone modeling and remodeling both refer to the ac tions of osteoblasts and os teoclasts in reshaping and replacing portions of the skel eton (Martin et al. 1998). Howe ver, these two processes are different from one another in several ways. Martin et al. (1998) provid e a list of differences that exist between the processes of modeling and remodeling. Although both modeling a nd remodeling involve osteoblasts and osteoclasts, in modeling thes e two cell types work independently while in remodeling their actions are coupled, i.e. se quential. Another difference between these two processes is that modeling affects the size and/or shape of the bone, while remodeling typically does not affect either size or shape. Modeling and remodeling are both most active before skeletal maturity is reached; however, the rate of modeling versus remodeling is much more reduced after skelet al maturity is reached. Unlike modeling, remodeling occurs throughout life. Finally when modeling occurs at a particular site the

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7 process is continuous and prolonged while re modeling is episodic and has a definite beginning and ending. Although both modeling and remodeling ar e affected by mechanical conditions, most of the experimental studies have only involved the process of remodeling (Lanyon et al. 1982, O’Connor et al. 1982, Ca rter 1984, Lanyon 1984, Lanyon and Rubin 1984, Meade et al. 1984, Burr et al. 1985, Rubin and La nyon 1985). The reason for this is that mature experimental animals are used to try to eliminate as many unknown variables as possible. So many factors influence bone gr owth that controlling all these variables, some of which are still unknown, is difficult, if not impossible. For this reason, most of the experimental research focuses on the process of remodeling since modeling is practically nonexistent once the sk eleton has reached full maturity. Three important variables that are known to influen ce remodeling include strain magnitude, strain rate, and strain dist ribution (Lanyon 1984). Lanyon et al. (1982) conducted an experiment using mature sheep that involved excising a portion of a sheep’s ulna and then exposing the sheep to peak prin ciple walking strains. They found that the bone adapted to produce strains that were lowe r than before the osteotomy, which is not consistent with the view th at bone reacts to control stra in magnitude. Instead, they concluded that adaptive remodeling of perios teal bone is influen ced by alterations in strain distribution rather th an peak strains alone. R ubin and Lanyon (1985) conducted a similar study using turkeys and came to a comp arable conclusion that bone remodeling is sensitive to both strain distributi on as well as strain magnitude. Strain rate is also an in fluential variable in bone rem odeling. In order to evaluate how strain rate affects remodeling, O’Connor et al. (1982) chronically inserted implants

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8 into the radius and ulna of mature sheep. These implants were subjected to both bending and compressive loads while varying the peak st rains and strain rates. Their conclusion was that in order for remodeling to occur th ere needs to be sufficiently high strains and appropriate strain rates. This leads to the question of whether or not the frequency of the loads, i.e. static and dynamic loads, affect bone remodeling. Lanyon and Rubin (1984) conducted experi ments on avian ulna in order to address the question of whether or not both static and dynamic loads affect bone remodeling. Remodeling activity was assessed under three different conditions, disuse alone, disuse with a superimposed continuous compressive load, and disuse interrupted by a short daily period of intermittent loading. From this experiment, Lanyon and Rubin (1984) concluded that remode ling occurs under both dynamic and static loads when the bone is exposed to strains with in the functional strain range but the remodeling is more effective under dynamic loading conditions. Meade et al. (1984) conducted a similar experiment by exposing the femora of adult dogs to continuously applied loads and noted that there was an outward movement of th e periosteal surface in response to the continuously applied loads, but li ttle or no effect was seen on the endosteal surface of the bone. In addition to the changes in strain dist ribution, strain magnitude, and strain rate, bone also initiates remodeling as a response to fatigue microdamage (Burr et al. 1985). Burr et al. (1985) tested the validity of the th eory that osteonal rem odeling is triggered by microdamage by conducting several different e xperiments on adult dogs. The data that was collected support the idea that fatigue mi crodamage is a significant factor in the initiation of remodeling.

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9 No doubt exists that the mechanical envir onment is influential to bone remodeling. Factors other than mechanical environment, however, can also affect bone remodeling. For example, bioelectrical currents gene rated by blood flow and cell membranes may also affect bone remodeling, so the situat ion is not straightforward (Rubinacci and Tessari 1983). According to Herring (1993), characterizat ion of the real lo ading regime of skeletal elements is needed in order to determine the functional influences of bone growth. Although computer models and strain gage technology have been helpful in trying to determine stress distributions, both have limitations. The major limitation of the computer models is that all local effects mu st be ignored or modeled precisely, which is currently impractical. Strain gages help overc ome this problem, but they are limited to a very restricted area of the structure being studied. Even though there are technological difficulties when trying to determine the loadi ng regime of skeletal elements, successful experiments have been conducted th at yielded useful information. Lanyon (1973, 1974) performed experiment s on the calcaneus of sheep using rosette strain gages and was able to de monstrate that the trabecular orientation corresponded with the principal compressive and tensile strain directions. This experiment was able to confirm what Wolff had postulated earlier about principal stress directions coinciding with tr abecular orientation (Martin et al. 1998). Once this was confirmed, attention turned to the question of what type of load is responsible for apposition and resorption. Herring (1993) argues that re sorption corresponds to the orientation of compressive strain, while pe riosteal bone growth corresponds generally with the orientation of tensile strain. Of course, as men tioned earlier, it is not only the

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10 type of force applied, but also the frequenc y and magnitude that determines whether or not bone is deposited or resorbed. The skull may experience loading from se veral sources including forces from the inertia and weight of the skull itself, joint reaction forces, forces from the muscles, and trauma (Russell and Thomason 1993). If these forces act directly on the structure, then shearing stresses will result. Other types of forces that th e skull may experience include bending and torsion. Preuschoft (1989) stated that the bite forces inside the upper jaw evoke shearing forces, torsional moments, a nd bending moments; unfortunately he does not specify the sources or nature of these di fferent loading conditions Different regions of the facial skeleton seem to experience variable amounts of stress during biting and mastication, so every facial bone may not be specifically designed for countering mechanical loads from mastication (Hyla nder et al. 1991, Hylander and Johnson 1997). The mandible is one area of the face wher e extensive research has been conducted to determine the forces experienced duri ng mastication (Hylande r 1975, Hylander 1979). Hylander (1975) explored the issue of whethe r or not the mandible functions like a lever during mastication and concluded that th e mandible does function like a lever and behaves more or less like a curved beam. Hylander (1979) also e xplored the functional significance of the primate mandibular form and concluded that the symphseal region does appear to be an adaptive response to ma sticatory loads, particularly unilateral molar bite force. Unfortunately the upper and lowe r jaws do not function in the same manner. Due to the structural nature of the maxilla, modeling the lower jaw experimentally has been difficult, if not impossible, to date. Although the conclusion can be made that the maxilla does experience bending and twisting lik e the mandible due to the presence of the

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11 hard palate, there is no experimental evidence pr esent that does state what type of stresses the maxilla experiences during mastication (D aegling and Hylander 1997). Nevertheless, the forces generated by mastication are still of particular interest when examining the palate. Effect of Dietary Consistency on Bone Growth Several studies have been conducted over the years that suppo rt the idea that dietary consistency affects craniofacial bone growth and development. Many of these studies were initiated in an attempt to de termine why Western societies had such high rates of malocclusion compared to non-indus trial societies (Beech er et al. 1983, Ciochon et al. 1997). The theory that forceful ch ewing was necessary for proper growth became one avenue of exploration. Beecher et al. (1983) examined this hypothesis by raising two groups of squirrel monkeys; one group was gi ven a naturally tough diet while the other was given a diet of artificially softened foods. Significant differences were noted between the two groups and they concluded that there is a minimum threshold of stress needed for proper craniofacial development to occur. The animals given the soft diet in th e study of Beecher et al. (1983) exhibited maxillary arch narrowing and increased palatal height. These two characteristics occurring simultaneously suggests that ma xillary arch collapse (maxillary arch narrowing), the most common occlusal proble m in American youths probably occurs because of differences in the growth of the mi d-palatal suture and the fact that teeth from the maxillary alveolar process are not correct ly aligned with the mandibular teeth. Other cranial sutures were also affected by diet ary consistency. Distinct differences in calcification were seen in the lambdoid and sagittal suture s through the use of radiographs. The soft diet animals had a mu ch broader radiolucent area at the sutures

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12 than the hard diet animals, which means that the sutures in the soft diet area are more patently opened and less calcified. Squirrel monkeys are not th e only experimental animal s that have supported the idea that craniofacial growth and developmen t is affected by the consistency of diet. Experiments have also been conducted usi ng rats (Beecher and Corruccini 1981, Bouvier and Hylander 1984, Kiliaridis et al. 1985, Yama moto 1996) and minipigs (Ciochon et al. 1997). Differences were found in the mandibles of Yucatan minipigs that were raised on diets of varying consistencies (Ciochon et al. 1997). In a ddition to examining the bones, Ciochon et al. (1997) also examined the weight of the muscles involved in mastication. They found that the weights for the superficia l masseter, deep masseter, and temporalis muscles were all significantly higher in the hard diet group. The frontal profiles of the cranium also differed between the two groups ; the hard diet group displayed a steep profile while the soft diet group displayed an overall more horizontally oriented profile. Morphological differences in the shape of the mandible between the two groups were also noted. Unfortunately, the maxilla was not the main focus of this study so very little information concerning this structure was pr esented. However, Ci ochon et al. (1997) did note that the palate was relatively longer in the soft diet gr oup. They also took measurements of the maxillary arch breadth and unlike the results reported by Beecher et al. (1983) in the squirrel m onkeys, there was no difference found between the groups of the Yucatan minipigs. Rats have served as another common expe rimental animal for pursuing the effects of dietary consistency on craniofacial grow th and development. Beecher and Corruccini (1981) conducted a study using rats that consisted of two groups, a soft diet group and a

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13 hard diet group. They reported that the rats fed a soft diet had a significantly narrower maxillary arch breadth compared to the hard diet group. The animals in the soft diet group weighed approximately 13% less than the animals in the hard diet group at the end of the experiment; however, the weight di fference was not found to be significant. Bouvier and Hylander (1984) disagree with Beecher and Corrucci ni (1981) about the weight differences not being significant. Bouvier and Hylander (1984) conducted a similar experiment and found that the maxilla ry arch length was si gnificantly different between the animals raised on different diet s, but once corrections were made for the weight differences, the maxillary arch differences became nonsignificant. Kiliaridis et al. (1985) used cephalometric longitudinal analysis for growing rats using a normal diet group and a group fed a so ft diet. Differences were noted in the growth patterns of both the neurocranium and the viscerocranium between the two groups. The viscerocranium of the soft diet group showed a more orthocranial position, which refers to the skull being of medium height relative to length, with the most noticeable changes occurring in the nasal area. Changes were also noted in the incisors of the upper jaw as well as the mandible. Th e incisors of the upper jaw showed a greater proclination in relation to occl usal and palatal planes in th e soft diet group, while the gonial angle of the mandible show ed a decreased appositional rate. As can be seen by comparing the stud ies of Beecher and Corruccini (1981) and Bouvier and Hylander (1984), no consensus exis ts on the effect dietary consistency has on the growth of the palate. Yamamoto ( 1996) examined how food consistency effects the growth of the palatal region of the maxillary complex through the use of bone histomorphometry to try to aid in the resoluti on of this issue. Specifically, the goal was

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14 to investigate how the consistency of the diet affected the pattern of bone apposition at the growth site of the palatal region. As with the previous st udies, the rats were divided into two groups; one was fed a hard (solid) diet while the ot her was fed a soft (liquid) diet. There were significant diffe rences found between the two groups. Yamamoto’s (1996) results agreed with thos e of Kiliaridis et al. (1985) in that the vertical growth of the palate differed be tween the two groups a nd there was a more anteriorly directed growth rotation of the pala te in the soft diet gr oup. Other studies that examine the underlying mechanism for this diffe rence have noted a marked decrease in the bone appositional rate in th e areas of muscle insertion in the anterior part of the viscerocranium (Engstrom et al. 1986); however, the area under consideration in Yamamoto’s (1996) study is not an area of muscle insertion. This implies that the changes in the palatal region of the maxilla can not be caused directly by activities such as muscle action; however, muscle action can have large effects due to mechanical activities such as bending and twisting. Yamamoto (1996) proposes that although the mechanical forces generated by mastication probably have an indirect affect on the growth, another factor to consider is that th e growth of other structures su ch as the neurocranium also affects the growth of the viscerocranium under different occlusal loading conditions. As mentioned previously w ith the study of Ciochon et al. (1997), the growth of the mandible has also been explored in re lation to dietary consistency. One line of reasoning is if an animal has a diet that cons ists of hard items then their mandible would be more massive in terms of bone than a simila r sized animal with a softer diet. Just like the differences reported in the maxillary arch breadth between the different studies cited above, differences exist on this issue c oncerning the mandible. A study conducted by

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15 Daegling and McGraw (2001) does not support the line of reasoning expressed above. They examined the mandibles from two different species of colobus monkeys that are similar in size and sympatric, but one of the species ( Colobus polykomos ) has a diet containing food items of harder cons istency. One would expect that Colobus polykomos would have a more robust mandible than the other species ( Procolobus badius ), but this is not the case. In fact, mandibular morphology does not reflect the diffe rences in diet. The studies mentioned so far have been c oncerned with mastication, but this is not the only process that mammals use for oral food intake. Infant mammals engage in a unique form of feeding referred to as suck ling. Although the mechanism of suckling has been explored (German et al. 1992) as well as the transition from suckling to drinking at weaning (Thexton et al. 1998), there have been no studies conducted on the types of loads this mechanism produces and whether or not these loads also affect craniofacial growth and development.

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16 CHAPTER 2 GROWTH OF THE PALATE Embryological Growth and Development Facial development begins around the third week of gestation with the development of five facial swellings, or primordia, in th e frontonasal and visceral arch regions. These five primordia consist of the frontonasal prom inence, which forms the forehead and nose, two maxillary prominences, which form the lateral stomodeum, or primitive mouth, and two mandibular prominences, which form the caudal stomodeum (Bender 2000, Scheuer and Black 2000). Within each of these promin ences, neural crest cells differentiate into fibrous connective tissue, all the dental tissues except enamel, skeletal and connective tissue of the face, cartilage, and bone. By the end of the fourth week, the lower aspect of the frontonasal prominences develop bilatera l oval thickenings of the surface ectoderm known as nasal placodes, which will produce th e medial and lateral nasal prominences (Kirschner and LaRossa 2000, Moore and Persau d 2003). The intermaxillary segment of the maxilla forms when the medial nasal promin ences merge. This segment gives rise to the philtrum of the upper lip, the premaxillary pa rt of the maxilla, and the primary palate (Moore and Persaud 2003). The maxillary prom inences enlarge during the fifth week and connect with the lateral nasal prominences to establish continuity between the nose and the cheek while the maxillary prominences fu se with the medial nasal prominences to complete the lip. Palatogenesis begins at the end of the fi fth week and continues until the twelfth week. The median palatine process develops from the intermaxillary segment during the

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17 sixth week (Moore and Persaud 2003). This process forms the primary palate, which gives rise to the premaxillary part of the max illa. In the adult hard palate, the premaxilla represents only a small portion of the hard pala te anterior to the incisive foramen forming the part of the maxillary alveolus that bears the incisors. During the sixth week, the secondary pala te develops from the paired lateral palatine processes also known as the palatal shelves. The lateral palatine processes are two mesenchymal projections that extend from the internal aspects of the maxillary prominences (Moore and Persaud 2003). Ini tially both palatal shelves are oriented vertically on either side of the developing tongue. As th e tongue descends, the palatal shelves gradually move to a horizontal posi tion where they will meet and fuse at the midline. An intrinsic shelf elevating force is believed to be responsible for the movement of the palatal shelves. This force is genera ted by the hydration of hyaluronic acid in the mesenchymal cells within the palatal proce sses (Moore and Persaud 2003). Hyaluronic acid acts as a water barrier and provides “t issue turgor” that moves the palatal shelves (Brinkley and Morris-Wiman 1984). The movement of the palatal shelves begins in the seventh week, but fusion is not completed unti l the twelfth week. Fusion of the palatal shelves results in the formation of the uvula, so ft palate, and hard pa late posterior to the incisive foramen (Kirschner and LaRossa 2000). For nonhuman primates such as baboons and macaques, palatogenesis occurs approximately at the same stage as hu mans (Hendrickx and Peterson 1997). The underlying mechanisms for palatal closure are also thought to be the same between these primate species and humans (Bollert and Hendrickx 1971, King and Schneiderman 1993). Since the timing and the underlying mechan isms of palatal closure are similar in

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18 baboons, macaques, and humans, then catarrhine primates may be appropriate animals to use in order to explore orofaci al teratogenesis in humans (B ollert and Hendrickx 1971). Postnatal Growth and Development Growth refers to a structure, in this case bone, changing in magnitude (Enlow and Hans 1996). Contrary to prior belief, there are no centralized and self-contained growth centers; instead all porti ons of the bone play a role in th e growth of the structure (Enlow and Hans 1996). As opposed to growth centers the functional matrix is the determinant of the skeletal growth processe s. The functional matrix is all the tissues and spaces that work together to fulfill a particular f unction (Moss 1969). This concept provides an explanation of what happens during craniofacial growth, but not how the cellular and molecular mechanisms underlying growth work. Remodeling and displacement are two ba sic kinds of growth movements involved in facial growth. Remodeling serves five ma in functions that are outlined by Enlow and Hans (1996): 1) progressivel y changes the size of the w hole bone, 2) sequentially relocates the component regions of the whol e bone to allow for overall enlargement, 3) shapes the bone for its functions, 4) fine-tunes the outline of separate bones to each other and their surrounding soft tissues, and 5) carries out structural adaptatio ns to the intrinsic and extrinsic changes in conditi ons. This remodeling is not synonymous with the type of remodeling discussed earlier. Unlike Martin et al. (1998), Enlow and Hans (1996) do not make a distinction between the processes of modeling and remodeling. Instead, Enlow and Hans (1996) make a distinction be tween remodeling (as defined above) and displacement. Displacement is the process of the physical movement of the whole bone and occurs when remodeling is simulta neously resorbing and depositing bone.

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19 Palatal remodeling occurs through a proce ss known as the “V” principle. This concept is based on the fact that many cranial and facial bones, including the palate, have a V-shaped configuration (Enlow and Ha ns 1996). Bone deposition takes place on the inner side of the V while resorption takes pl ace on the outer side of the V (Figure 1, adapted from Enlow and Hans (1996)). In the case of the maxillae, the external side of the anterior part of the maxillary arch is resorbed while bone is deposited on the inside of the arch. This process increases the width of the arch causing the palate to become wider (Enlow and Hans 1996). Growth along the mid-palatal suture also adds to the progressive widening of the palate and ma xillary (alveolar) arch (Friede 1998). Widening of the palate continues into adulthood (Scheuer and Black 2000). Figure 1. “V” principle of facial growth. As the V moves from position A to position B, the structure increases in overall di mensions. The + marks indicate bone deposition on the inner side of the V, while the – marks indicate bone resorption on the outside surface. Lengthening of the hard palate occurs part ly in the transverse suture and partly by the apposition of bone to the posterior marg in (Melsen 1975). The growth in the transverse suture continues until puberty, but the appositional ac tivity continues until

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20 approximately 18 years of age. Disagreemen t exists concerning the appositional activity on the posterior margin of the palate. Acco rding to Sejrsen et al (1996), little growth occurs at the posterior border of the hard palate. They reached this conclusion by studying archaeological samples that show a constant distance between the greater palatine foramen and the posterior margin of the palatine bone at va rious dental stages. Sejrsen et al. (1996) attribute lengthening of the hard palate almost solely to growth in the transverse suture. Although the amount of apposition that occurs on the posterior margin is controversial, consensus exists on the f act that little to no apposition occurs on the anterior margin. The transverse palatine sutu re remains in the posterior part of the bony palate from birth to adult hood regardless of the minute amount of activity on the anterior margin, which suggests that highly differentia ted growth must occu r postnatally in the transverse palatine suture (Silau et al. 1994). The palatal growth rates of seve ral nonhuman primates, specifically Macaca nemestrina and Papio cynocephalus were investigated to see if there were any differences between the two ge nera (Swindler and Sirianni 1973). Although the absolute size of these primates is different, the growth of the palate occurred at similar rates with both gradually decelerating with age. The deceleration of the growth rate is also characteristic of humans. Another significan t finding from this study is that no sexual dimorphism exists in the rate of growth of the palate within either species (Swindler and Sirianni 1973). As previously noted, both the mid-palata l and transverse palatine sutures play a role in the growth of the palate. In the em bryonic stage, the incisive suture separates the premaxilla and the maxilla, but this suture fu ses before birth; a lthough a slight visible

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21 suture line may appear on the lingual surface of the palate and persist into adulthood (Mann et al. 1987). The mid-palatal and transv erse palatine sutures fuse erratically, but they remain open well into adulthood. Th e morphology of these two sutures changes throughout the different stages of palatal growth. The transver se suture begins broad and slightly sinuous at birth and la ter develops into a typical s quamous suture (Melsen 1975). The mid-palatal suture progresses through three stages; in the first stage the suture is short, broad, and Y-shaped, with the vomerine bone in the groove of the Y between the two maxilla halves; in the second stage the su ture is more sinuous; and in the third stage the suture is heavily interd igitated (Melsen 1975). The change in sutural morphology may be attributed to change s in the mechanical environm ent. Sutural biology, function, and morphology will be explored further as we ll as how sutures are affected by loads.

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22 CHAPTER 3 SUTURES Functions of Sutures Sutures are any articulation between derm al bones of the skull (Herring 2000). These articulations are usually fibrous but some times contain cartilage or fibrocartilage. Evolutionarily, the earliest su tures developed in the armore d jawless fish and consisted simply of the skin that remained between the dermal plates. The properties that are typically associated with sutures, mobili ty, growth, and the potential for synostosis (closure), were already present in these ar mored jawless fish (Herring 2000). Mammals show no evolutionary progression of sutures; in fact, they have lost some of the sutural diversity. All taxonomic groups that have su tures show a complete range of sutural morphology, from loose connective tissue to el aborate interdigitations joined by a welldefined ligament (Herring 2000). Three main biological functions are associ ated with sutures: to unite bones while still allowing slight movement, to act as gr owth areas, and to absorb mechanical stress (Persson 1995, Cohen Jr. 2000). Two types of movements typically take place at the sutures. At birth is when the first ty pe of movement occurs, which entails the displacement of the calvaria bones as the human head is compressed through the birth canal (Persson 1995). This causes a molding of the head that resolves during the first week of life through cranial re-expansion and widening of the sutural areas (Cohen Jr. 2000). The other type of movement at the sutu res is caused by the displacement of bones relative to one another as the skull grows (Persson 1995).

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23 As previously mentioned, the amount of growth that occurs at the sutures is debated, but there is no doubt that sutures do play a role in craniofaci al growth. Sarnat (2003) conducted experiments on macaque monk eys that involved surgically producing clefts of the palate on one side only. The severity in the cl efts varied from a narrow slit to almost the entire half of the palate exci sed. No significant diffe rences were noted in the growth and development of the hard palate or maxillary arch between the operated and unoperated sides or between the experiment al (operated) and c ontrol (not operated) macaques. Sarnat (2003) postulated two po ssible conclusions; either the transverse palatine and mid-palatal sutures do not make a primary contribution to growth or other areas of growth compensated for the altered condition. From this particular experiment there is no way to decide which conclusi on is correct, but othe r researchers have postulated that the palatal sutures only sec ondarily contribute to growth (Melsen 1975). Not only does the same suture grow differentia lly at various times, but the rate and the amount of growth varies for different sutu res at different times (Persson 1970, Sarnat 2003). The problem with intervention studies is that they create a situation that will never be found in nature, so the results cannot be applied to animals in nature. Persson (1970) conducted a study on the postn atal growth of faci al sutures in the rat that revealed different gr owth patterns in individual sutures as well as in the bony margins of the same suture. Four different growth patterns were observed. The first pattern was appositional growth against both sutural margins, which was observed in the premaxillary part of the mid-palatal suture. Another type of pattern observed was appositional growth against only one sutural ma rgin while the other remained inactive. This pattern was found in the main part of the naso-premaxillary suture. The palato-

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24 maxillary suture showed appositional growth against one sutural margin, while the other margin showed resorption. This contradicts Sa rnat (2003) who states that sutural growth is only through apposition w ith no resorption involved. The final growth pattern observed by Persson (1970) is perichondral gr owth in the maxillar y part of the midpalatal suture. This suture is an example of cartilage being present in the articulation as opposed to just collagenous fibers (Herring 2000). Mechanical environment also affects sutural growth and development. Mao (2002) concluded that sutural growth is accelerated when exposed to tension and compression. Another potential stimulus for su tural growth is the oscillatory component of cyclic force. Kopher and Mao (2003) de monstrated that small doses of oscillatory mechanical stimuli can affect sutural growth by either a ccelerating osteogenesis of the suture or initiating net sutu ral bone resorption. This info rmation can potentially affect therapeutic goals in craniofacial disorders. The third biological function of sutures is that they act either as a shock absorber for mechanical stress or to transmit for ce across the sutures (Herring 1972, Persson 1995). The majority of mechanical stress in the suture areas is associated with mastication (Persson 1995). Sutural morphol ogy has been postulated to reflect the loading environment under which the suture is subjected (Herring 1972, Wagemans et al. 1988, Herring and Teng 2000). Whether or not this is true will be explored in the following sections. Sutural Biology and Morphology Pritchard et al. (1956) outlined the developm ent of cranial and facial sutures based on six different species: humans sheep, pigs, cats, rabbits an d rats. At all stages of development, sutures exhibit five intervening la yers as well as two uniting layers between

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25 the adjoining bones. The five in tervening layers consist of a pa ir of cambial layers, a pair of periosteal fibrous capsular layers, and a middle looser layer of cellular mesenchymal tissue. The cambial layers are the sites of active osteogenesis producing woven bone, but the capsular layers must also expand in orde r to keep pace with the growing bone. The two uniting layers occur when the fibrous cap sules are joined by m eans of two fibrous laminae, an external and an internal. The extremities of the fibrous capsules retain their separate identities due to the interven ing layer of loose mesenchymal tissue. The facial and cranial sutures have the same structure, but they arise somewhat differently. Before the sutures are formed in the face, the cambial a nd capsular layers are already present with the mi ddle and uniting layers being derived from the mesenchyme between the approaching bone territories. Th e bones in the cranial vault approach each other within an already diffe rentiated fibrous membrane referred to as the ectomeninx. The capsular layers do not form in the cranium until the cambial layers have almost met and the middle and uniting layers are derive d from the delamination of the ectomeninx between the bones (Pritc hard et al. 1956). The histological structure of sutures, however, is not ag reed upon. Pirelli et al. (1999) conducted a study using biopsy sample s of the mid-palatal suture obtained from patients ranging in age from 10 years old to 30 years old. They reporte d that the capsular and cambial layers reported by Pritchard et al. (1956) were not detected in any of their samples nor were the cells typically associ ated with these layers, osteoblasts and osteoclasts. The absence of osteoblasts and osteoclasts suggest that the bone was in a resting period at the time of the sample. Unlike the woven bone detected by Pritchard et al. (1956), Pirelli et al. (1999) stated that all the sutures were formed by lamellar and

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26 bundle bone. Bundle bone is the term used to describe bone in the suture that closely resembles the alveolar bone lining the periodonta l ligament with a high turnover rate (Pirelli et al. 1999). Although the functional significance of the la mellar bone in the sutures is unclear, Pirelli et al. (1999) stated that the lamellar bone may possibly progressively replace the bundle bone when the suture is no longer active in growth and remodeling. If this is the case, the lamellar bone may represent the structural basis of the physiological process of synostosis (Pirelli et al. 1999). The discrepancies in the sutural structures between Pritchard et al. (1956) and Pirelli et al. (1999) may be attributed to the differences in the ages of the samples examined. The functional significance of the presence of cartilage in some of the postnatal sutures is heavily debated. The cartilage is only present for a limited time and usually only appears in the midline sutures, i.e. the sa gittal and mid-palatal sutures. The function of this cartilage seems to be linked to changes in the mechanical environment (Wagemans et al. 1988). Sutures are nor mally under tension, but during growth the sutures may be exposed to particularly strong pressure and shearing st resses (Pritchard et al. 1956). The secondary cartilage that is pr esent in these sutures is mainly found in rapidly growing areas (Perssons 1995). Pritchard et al. ( 1956) recommends that the effect of masticatory forces should be cons idered in relation to the development of sutures. The morphology of sutures is not only different between sutures, but the morphology of a single suture can vary througho ut its life. Melsen (1975) identified three morphological stages in the developm ent of the mid-palata l suture: Y-shaped, slightly sinuous at birth, a nd interdigitated at puberty. Del Santo Jr. et al. (1998)

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27 conducted a study of the morphological aspects of the mid-palatal suture in the human fetus that partially confirmed the changes in morphology described by Melsen (1975). The first group of fetuses (16-23 weeks) in this study showed a mid-palatal suture that was rectilinear in nature with a wide zone of intense cellula r proliferation. The second (24-31 weeks) and third groups (32-39 weeks) displayed a si nuous form with a narrower cellular proliferation zone. The complex morphology of sutures is thought to reflect their functional environment (Rafferty and Herring 1999). Oudhof (1982) found that although sutural tissue has hereditary character istics that determine the spec ific differentiation, certain environmental influences are necessary fo r the manifestation and development of qualities associated with sutures. For ex ample, in the transplantation experiments conducted by Oudhof (1982), when a portion of a suture was relocated to an area of little or unspecified growth, the suture gradually lost its specific structure. On the other hand, when a suture was transplanted to an area of active growth, the su ture adapts to its surroundings. This was witnessed when a por tion of the sagittal suture of a rat was transplanted into a coronal suture. The sagittal suture adapte d by developing a more intensive formation of fibers and more a nd longer lingulae (Oudhof 1982). The influence of the mechanical environment on sutu res will be the next topic covered. Sutures and Loads Suture morphology is extremely complex a nd several researcher s have postulated that the mechanical environment is one fact or that influences their morphology (Linge 1970, Herring 1972, Oudhof 1982, Wagemans et al. 1988, Herring and Teng 2000, Mao 2002). Herring (1972) examined sutural morphology in suoids to explore the use of cranial sutures as indicators for the amount and direction of stress in the skull. She

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28 assessed sutural morphology in two ways: firs t she examined disarticulated sutural surfaces for six specimens, second she exam ined dried articulated suoid skulls and subjectively categorized them as straight, slig htly interdigitated, interdigitated, and very interdigitated. Another way to classify sutu res is as either beve led or butt-ended. One tentative conclusion that Herring (1972) drew from this research was that the beveling of sutures may allow adjustive move ments or stress reduc tions during forceful operations, like rooting in pigs. Another conclusion was that interdigitations are instrumental in the transmission of force fr om one bone to another and to resist shear loads. Generally speaking, the interdigitations of the sutures will be either perpendicular or parallel to the main force applied and th ese interdigitations serve to increase the surface area for collagen fibe rs to attach (Herring 1972, Jaslow 1990, Rafferty and Herring 1999). Jaslow (1990) examined th e mechanical properties of sutures and concluded that increased interdigitations do improve the bending strength when sutures are loaded slowly when comp ared to cranial bone alone. Jaslow (1990) was also able to provide support for the hypothesis that sutures act as shock absorbers in the skull. This is based on the discovery th at cranial bone with a suture present was able to absorb more energy, regardless of the sutural morphology, than the pure cranial bone. The sutural morphology also influences the amount of energy absorbed. Energy absorption increased as the complexity of sutural interdigitation increased. Interdigitation also seems to be correlated with the degree of compressive strain. The more compressive strain a sutu re is exposed to, th e higher the degree of interdigitation (Rafferty and Herring 1999). Adjacent sutures also seem to experience large magnitude strains of opposite polarity during normal masticati on, at least in pigs

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29 (Rafferty and Herring 1999). This result is intu itive because when one side of a structure is experiencing tension, the other side is experiencing compression. The cranium is a difficult bone to model because of its unusual morphology. The palate in general provides special difficulties because the structure is curved which makes techniques such as strain gages difficult to us e. Since the loading environment influences craniofacial growth and development, de termining the loading environment of bones such as the maxilla is important.

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30 CHAPTER 4 ECOLOGY AND DIET OF COLOBUS MONKEYS Background Information Historically, researchers ha ve classified colobus monke ys as specialists, based on the amount of leaves in their diets. The origin of this belief seems to stem from an early paper by Booth (1956) that refe rs to colobus monkeys as ‘p urely leaf-eating.’ Casual observations and the study of the contents of the stomach formed the basis of this assumption. Anatomical features such as the large complex stomach and high-crowned molars and premolars also support the notion th at colobus monkeys ar e largely leaf-eaters (Campbell and Loy 2000). Recent evidence, howev er, suggests that this initial view of colobines is not accurate, at least not for all species and/or groups (Maisels et al. 1994). Leaves do make up a large portion of most, if not all, colobus monkey diets, but seeds, fruits, and flowers also contribute significantl y to their diets. The original belief that colobines were specialists was based on studies conducted on groups of colobines in east Africa (Dasilva 1994). Research at sites such as Tiwai Is land in western Africa has shown that seasonal variability exists in th eir diets, including seeds, fruits, and both young and mature leaves (Dasilva 1994, Davies et al. 1999). Feeding techniques do not vary much between different species of colobines. The type of food eaten affects the technique used, but regardless of the food type, there is very little manual manipulation involved (Clutt on-Brock 1975). Colobus monkeys have reduced thumbs, which may explain the little amount of manipulation. This appendage does not provide them with the grip of other primates who have larg er thumbs that allow

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31 more precise gripping. Clu tton-Brock (1975) did observe some manipulation, though, such as stripping the pinnules off of the leaf stem by gripping the st em in their teeth and dragging the stem through their clenched fists. He states that he never saw them use their hands to strip or break open fruit; if the c overing was removed from a fruit they opted to use their teeth instead (Clutton-Brock 1975). One difference between red colobus ( Procolobus badius ) and king colobus ( Colobus polykomos ) is their preference for location of feeding. The former usually acquires a large portion of their food from so me of the largest tr ees in the upper canopy of their habitat, while the la tter choose to forage lower in the canopy (Oates 1994). In areas where both of these colobine groups co-occur, the red colobus monkeys choose a more diverse diet than the king colobus. A nother difference is the amount of seeds that are consumed. All colobus species ingest s eeds, but only in the bl ack and white forms do seeds sometimes dominate the diet (Oates 1994). Some researcher s argue that African colobines eat a large portion of seeds whenever the quality of the tree foliage is poor via poor soils (Maisels et al. 1994). Evidence suppo rts this statement for some areas such as Zaire (Maisels et al. 1994), but this explanation does not explain the difference in seed exploitation between sympatric spec ies of colobus monkeys. Study Sample The colobus monkeys used in this study are Procolobus badius (n=39) and Colobus polykomos (n=13) from the Tai Forest of Cote d’Ivoire. They ar e sympatric throughout most of their range and are similar in body si ze and diets except the king colobus exploits a particularly hard seed fr om the African oil bean ( Pentaclethra macrophylla Mimosaceae) at a much larger frequency than the red colobus monkeys.

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32 This African oil bean tree is usually 21 m in height with a girth of about 60 cm. The pods are 40-50 cm long and usually 5-10 cm wide. Inside the pods are 6-10 flat glossy brown seeds that are up to 7 cm long. Colobus polykomos focuses on seeds from this plant and others like it whereas Procolobus badius focuses on leaf eating (Davies et al 1999). The reason for this difference probabl y stems from their individual preference in foraging, i.e. upper versus lower canopy. When the king colobus preys on these hard seeds, they expend a great amount of effort gnawing them until they break through the encasing (Davies et al. 1999). As mentioned earlier, Daegling and McGraw (2001) predicted that the species exploiting the hard seeds should have a more robust mandibular corpus than the species that does not exploit this food item. This prediction is based on the reasoning that the king colobus would have to apply larger loads, therefor e stressing the mandible more, to gnaw through the tough encasements. The results of the st udy, however, showed th at the variation in mandibular morphology in these two sympatri c colobines does not correspond to the predictions based on the dietary differences (Dae gling and McGraw 2001). The underlying reasoning behind the current pr oject is that the palates of these two species of colobus monkeys are exposed to different loading environments. The extensive gnawing of Colobus polykomos on the hard seeds may cause a significantly larger amount of force on the palate. If this is the case, the complexity of the palatal sutures of these two species may reflect this difference in loading environment. In order to test this hypothesis, fractal analysis was completed on the mid-palatal sutures of Colobus polykomos and Procolobus badius

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33 CHAPTER 5 FRACTAL ANALYSIS One of the most difficult tasks facing morphologists is that of quantifying and measuring size and shape. Traditionally, pa rameters such as length and volume were used to try to quantitatively describe and compare morphological characteristics. In Euclidean geometry linear measures are c onsidered one dimension, smooth surfaces are two dimensions, and volumes and weights are three dimensions. Objects that occur in nature, however, seldom have edges that are straight or surfaces that are smooth (Long 1985). Some objects in nature possess certain qual ities that can be described by a nonEuclidean fractional dimension, which lies between the values of one and two (Mandelbrot 1977). These objects are known as fractals. Fractals are geometric objects that are self-similar in nature. Self-similarity means that the fractal object is composed of smaller units that possess the same shape as the whole object. Fr actals have complex edges or surfaces that increase linearly as the resolution of the units used to measure them increase (Hartwig 1991). Fractal analysis is a technique used to interpret the geometric complexities of fractals. Several researchers believe some crania l sutures are fracta l objects (Long 1985, Hartwig 1991, Long and Long 1992, Gibert and Palmqvist 1995, Montiero and Lessa 2000, Yu et al. 2003). Long (1985) explored th e idea of whether or not complex sutures exhibit fractal properties such as self-similarity and a di mension between one and two. To address this question, Long (1985) examin ed the sutures on the shells of extinct ammonites and cranial sutures of white-ta iled deer. The sutures in both of these

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34 organisms are incredibly complex and did exhibi t fractal properties. Other cranial sutures that have been examined using fractal analysis are the sagittal suture in humans (Hartwig 1991, Yu et al. 2003), the sagi ttal and lambdoidal sutures in humans (Long and Long 1992, Gibert and Palmqvist 1995), and cranial sutures in the genus Caiman (Montiero and Lessa 2000). In each of these studies, th e structures under examination exhibited the characteristics of fractals. In this study, fractal analys is was conducted with the use of a software program known as Benoit 1.3 (St. Petersburg, FL). This program allows the user to choose from several different methods on how the fractal analysis is conduc ted. The different methods provided in this program are tailored to accommodate different types of data sets. Based on this data set, three methods s eemed equally applicable Each of these is discussed in further detail. Box Dimension and Information Dimension Methods The box dimension method of fractal analys is is one of the most widely used methods due to the relatively simple math ematics involved (Falconer 1990). In Benoit 1.3, the box dimension is de fined as the exponent Db in the relationship: bDd d N 1 ) ( where N ( d ) is the number of boxes of linear size d necessary to cover a data set of points distributed in a two-dimensional plane. A nu mber of boxes are used to cover the data set points that are evenly distributed on a plane. This may indicate th at point density may influence the results, i.e. the number of data points collected will affect the outcome of the fractal dimension. This method is often re ferred to as the grid dimension because the boxes used are usually part of a grid system.

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35 To accomplish this method, a series of different box sizes d are laid over the object and the program works by tallying the number of boxes filled during each box size overlay. One of the problems with this met hod is that the boxes are weighted the same whether the entire box is full or just a ti ny portion. The information dimension method addresses this problem by assigning wei ghts to the boxes so boxes containing more points are counted more than the boxes with fewer points (Benoit 1.3). Unfortunately this makes the mathematics involved much more complicated. Ruler Dimension Mandelbrot (1977) examined the coastline of Britain and determined that this object was fractal. How was the fractal dimension of this jagged, self-similar line calculated? The method he used is now referre d to as the ruler, or yardstick, method. The ruler method Dr is defined as: rDd d N) ( where N ( d ) represents the number of steps taken to wa lk a divider (or ruler) that is length d According to Benoit 1.3, the formal equivalence between this method and the box dimension can be shown mathematically. Alge braically, this claim is logical, since the box dimension is simply the reciproc al of the ruler dimension.

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36 CHAPTER 6 MATERIALS AND METHODS The skulls of 39 Procolobus badius and 13 Colobus polykomos were examined from a collection housed at Ohio State Univer sity. Eight measurements were also taken from each skull: palate height, internal palate breadth, external palate breadth, palate length, palate depth, upper facial height, facial width, and skull length. With the exception of palate depth and pa late height, the measurements are defined in Bass (1995). Table 1 provides a brief definition of the six measurements taken from Bass (1995). Palate depth was measured usi ng an instrument colloquially referred to as a carpenter’s tool or a contouring tool The contour was traced from th e edge of the alveolar ridge of the second molar to the level of the mid-palatal suture. The height of the contoured tracings was then measured resulting in th e depth of the palate. Palate height was measured with sliding calipers by placing one edge of the caliper on the mid-palatal suture and one edge on the alveolar ridge at the level of the second molar. Table 1. Definitions of measurements collected. Measurement Definition (Craniometric Points*) Facial width zygion to zygion External palate breadth ectomolare to ectomolare Internal palate breadth endomolare to endomolare Palate length prosthion to alveolon Skull length alveol are to opisthocranion Upper facial height nasion to alveolare *Craniometric points defined in Bass (1995) In addition to the measurements take n, the palate of each specimen was photographed using a Minolta 35mm camera with a macro lens attached. Each specimen was oriented with the palate parallel to the lens of the camera. The film was developed

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37 and the negatives were made into 35 mm slides. These slides were then scanned into the computer and saved as bitmap images. Each image was imported into SigmaScan where the mid-palatal suture of each specimen was digitized. The x-y coordinates were imported into SigmaPlot and subsequently graphed using a single spline curve. The spline curve option was chosen over the si ngle straight line option because this represented a more accurate depic tion of the sutures. The reason this has to be done is to override the automated scaling function of Si gmaPlot. The scale of the graphs were changed so equal units were represented on the x and y axes. The image was then inverted from black on white to white on black. This was done because Benoit 1.3 software recognizes white points as data poi nts and the black point s as the background. The images were converted to bitmap files and imported into Benoit 1.3 for the fractal analysis. After explor ing the different methods avai lable through the software, the two methods chosen were the informati on dimension and ruler dimension. The information dimension was chosen over the box dimension because the boxes are weighted and therefore provide a more accurate fractal dimension than the box dimension. There was not, however, an obvi ous advantage of either the information dimension or ruler dimension over the other, so both were used to calculate the fractal dimensions of the colobine mid-palatal sutures. Other researchers have chosen one of the methods over the other but the reasoning be hind their choice is of ten not made clear, although the researchers who chose the ruler di mension often state that they use this method because Mandelbrot (1977) used this method when examining the coastline of Britain.

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38 Once the fractal dimensions were obtaine d, several statistical procedures were conducted. A 2-way ANOVA wa s run separating the sexes and species which resulted in four groups. Regressions were also conducte d between the fractal dimensions and each size/shape variable to try to determine if there was a predictable relationship between any of these variables. The regressions were conducted with only the species separated not the sexes. Both of these procedures were evaluated for significance based on a Pvalue<0.05. The fractal dime nsion data for the four groups was also bootstrapped to obtain a more reliable mean since the sample sizes were small. Bootstrapping makes no assumptions about the distributional properties of the data.

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39 CHAPTER 7 RESULTS Including both fractal dimensions, ten vari ables were examined. Basic statistics were computed for each variable independently (Tables 2 and 3). The parametric medians for each group are graphically represen ted for both fractal dimensions in Figures 2 and 3. Since the samples sizes for these gr oups are small, the data was bootstrapped for 1000 iterations to try to obtain more relia ble means and standard errors, since no assumption is made regarding the distribution of the data. As shown in Tables 4 and 5, there was little difference between the pa rametric mean and the bootstrapped mean. The ruler and information fractal dimens ions for each species were regressed against each of the measured size/shape variab les. Out of the 32 regressions performed, only three resulted in significant P-values, i. e. P-values less than .05. However, the coefficient of determination (r-squared) was very weak for these three regressions, ranging from 12.1% to 37.2% (Table 6). Tables 7 and 8 report the ruler and inform ation fractal dimensions calculated for both species. One interesting (and seemingly impossible) aspect of two of these fractal dimensions is that they are below 1.0. Note in Table 3, Procolobus badius specimen number 2107 (Figure 4) has a rule r fractal dimension of 0.99209 and P. badius specimen number 9433 (Figure 5) has a ruler fractal dimension of 0.98466. However, their information fractal dimensions are both above

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40Table 2. Basic statistics fo r variables associated with Colobus polykomos Variable N Mean MedianStDev SE Mean Minimum Maximum Q1 Q3 Ruler Fractal Dimension 13 1.1880 1.1903 0.0599 0.0166 1.0795 1.2836 1.1416 1.2341 Information Fractal Dimension 13 1.0994 1.1018 0.0404 0.0112 1.0268 1.1659 1.0781 1.1247 Palate Height 13 12.550 12.500 1.268 0.352 10.400 14.800 11.495 13.680 Internal Palate Breadth 13 18.472 19.400 2.513 0.697 12.100 20.700 17.120 20.045 External Palate Breadth 13 36.278 36.800 1.906 0.529 32.200 38.800 35.310 37.450 Palate Length 13 44.138 44.600 2.992 0.830 36.600 48.200 42.800 45.990 Palate Depth 13 6.808 7.000 1.032 0.286 5.000 8.000 6.000 8.000 Upper Facial Height 13 40.124 40.200 3.350 0.929 34.200 46.410 38.700 42.000 Facial Width 13 75.91 74.00 5.53 1.53 67.90 83.60 71.75 81.25 Skull Length 13 108.96 108.00 4.01 1.11 103.00 115.70 106.05 112.65

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41Table 3. Basic statistics fo r variables associated with Procolobus badius Variable N Mean Median StDev SE Mean Minimum Maximum Q1 Q3 Ruler Fractal Dimension 39 1.1355 1.1093 0.0983 0.0157 0.9847 1.3455 1.0615 1.2121 Information Fractal Dimension 39 1.1085 1.1058 0.0276 0.0044 1.0643 1.1676 1.0883 1.1310 Palate Height 39 10.086 9.970 1.181 0.189 6.830 12.130 9.470 10.870 Internal Palate Breadth 39 16.347 16.460 1.554 0.249 12.180 18.740 15.380 17.370 External Palate Breadth 39 32.081 32.030 1.441 0.231 29.280 35.040 30.910 33.000 Palate Length 38 39.170 39.085 2.035 0.330 35.340 43.570 37.615 41.030 Palate Depth 39 6.122 6.000 1.305 0.209 3.000 8.500 5.000 7.000 Upper Facial Height 39 40.784 41.150 2.743 0.439 34.010 44.990 38.900 42.910 Facial Width 37 77.686 78.510 5.002 0.822 68.110 86.750 73.725 81.975 Skull Length 36 101.46 101.90 3.56 0.59 93.54 109.27 99.69 103.71

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42 Figure 2. Box plot of median valu es for the ruler fractal dimensions. Figure 3. Box plot of median values for the information fractal dimensions.

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43 Table 4. Bootstrapped versus parametr ic means for ruler fractal dimension Species Sex N Bootstrap Mean for 1000 samples Bootstrap Standard Error Parametric Mean Parametric Standard Error Colobus polykomos Male 4 1.1365 0.0200 1.1500 0.0244 Colobus polykomos Female 9 1.1953 0.0172 1.2049 0.0195 Procolobus badius Male 23 1.1295 0.0178 1.1380 0.0194 Procolobus badius Female 16 1.1230 0.0230 1.1362 0.0274 Table 5. Boostrapped versus parametric means for information fractal dimension Species Sex N Bootstrap Mean for 1000 Samples Bootstrap Standard Error Parametric Mean Parametric Standard Error Colobus polykomos Male 4 1.0748 0.0145 1.0817 0.0163 Colobus polykomos Female 9 1.1000 0.0118 1.1072 0.0143 Procolobus badius Male 23 1.1078 0.0056 1.1107 0.0062 Procolobus badius Female 16 1.1030 0.0061 1.1070 0.0071 Table 6. Significant regressions Species Variables Regressed N Slope Yintercept r r-squared (%) Procolobus badius Ruler vs Palate Height 39 0.0289 0.844 .35 12.1 Procolobus badius Ruler vs Palate Depth 39 0.0289 0.959 .38 14.7 Colobus Polykomos Information vs Facial Width 13 0.3100 0.624 .61 37.2 According to Benoit 1.3 software, the rule r and information fractal dimensions are equivalent. If this is true, then a simple regression of these two dimensions should show a linear relationship. As Figure 6 shows, this is not the case. In fact, there is no discernible pattern whatsoever in this gra ph and the r-squared value is 0.0402. Another indication that these methods for determining fr actal dimensions are not equivalent is that

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44 Table 7. Fractal dimensions of Colobus polykomos Specimen Designation Sex Ruler Fractal Dimension Information Fractal Dimension 2100 Male 1.07953 1.03320 2216 Male 1.19034 1.09408 2311 Male 1.15727 1.10373 9418 Male 1.17273 1.09593 2102 Female 1.28359 1.08546 2103 Female 1.24256 1.02679 2119 Female 1.22849 1.10182 2123 Female 1.23009 1.13283 2124 Female 1.11034 1.11666 2238 Female 1.14829 1.15345 2245 Female 1.13496 1.16592 2314 Female 1.22786 1.07076 9426 Female 1.23806 1.11099 the specimens exhibiting the highest and lowe st fractal dimension values differ between these two methods. The highest ru ler fractal dimension is 1.34546 ( Procolobus badius 227, Figure 7) while the highest inform ation fractal dimension is 1.16761 ( Procolobus badius 942, Figure 8). The lowest ruler fractal dimension is 0.98466 ( Procolobus badius 9433, Figure 5) while the lowest inform ation fractal dimension is 1.02679 ( Colobus polykomos 2103, Figure 9). Regardless of which fractal dimensi on is used, a pure model II 2-way ANOVA showed that no significant diffe rences exist in the fractal dimensions between species or sexes. There is also no interaction effect between species and sex. A pure model II was chosen because there were no fixed treatment effects but rather only random effects (Sokal and Rohlf 1981).

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45 Table 8. Fractal dimensions of Procolobus badius Specimen Designation Sex Ruler Fractal Dimension Information Fractal Dimension 2027 Male 1.04962 1.08833 2028 Male 1.29563 1.10579 2118 Male 1.06146 1.14878 2125 Male 1.12647 1.11583 2126 Male 1.30574 1.11583 2013 Male 1.15642 1.11931 2022 Male 1.07645 1.08920 2104 Male 1.13798 1.09966 2105 Male 1.07308 1.09533 2110 Male 1.24166 1.11158 2113 Male 1.23780 1.15081 222 Male 1.13614 1.14766 2231 Male 1.00705 1.10777 224 Male 1.11669 1.11242 2243 Male 1.22389 1.06426 2255 Male 1.07371 1.08930 232 Male 1.10572 1.08667 233 Male 1.06071 1.08017 235 Male 1.07599 1.09189 239 Male 1.14051 1.12176 9413 Male 1.05565 1.11252 942 Male 1.02873 1.16761 945 Male 1.31662 1.06753 2005 Female 1.05978 1.09521 2032 Female 1.09483 1.10217 223 Female 1.30888 1.13372 227 Female 1.34546 1.07348 2014 Female 1.11507 1.16151 2107 Female 0.99209 1.13472 2112 Female 1.09099 1.09856 2215 Female 1.10713 1.11771 2219 Female 1.14706 1.14561 2220 Female 1.10925 1.11490 2240 Female 1.29973 1.07179 2313 Female 1.20520 1.07042 236 Female 1.21207 1.08017 9422 Female 1.07231 1.13104 9433 Female 0.98466 1.08724 972 Female 1.03491 1.09268

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46 Figure 4. Mid-palatal suture of Procolobus badius specimen 2107 with a ruler fractal dimension of 0.99209 and information fractal dimension of 1.13472. The suture is oriented with the anteri or portion at the top of the page.

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47 Figure 5. Mid-palatal suture of Procolobus badius 9433 with a ruler fractal dimension 0.98466 and information fractal dimension of 1.08724. The suture is oriented with the anterior portion at the top of the page.

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48 Figure 6. Regression of rule r fractal dimension vs info rmation fractal dimension.

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49 Figure 7. Mid-palatal suture of Procolobus badius specimen 227 with a ruler fractal dimension of 1.34546 and information fractal dimension of 1.07348. The suture is oriented with the anteri or portion at the top of the page.

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50 Figure 8. Mid-palatal suture of Procolobus badius specimen 942 with a ruler fractal dimension of 1.02873 and information fractal dimension of 1.16761. The suture is oriented with the anteri or portion at the top of the page.

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51 Figure 9. Mid-palatal sutu re of Colobus polykomos specimen 2103 with a ruler fractal dimension of 1.24256 and information fractal dimension of 1.02679. The suture is oriented with the anteri or portion at the top of the page.

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52 CHAPTER 8 DISCUSSION The results of the 2-way ANOVA indicate that the hypothesis proposed for this study, i.e. these two species would differ in mid-palatal suture complexity, is not supported. The colobine monkeys used in this study only have one major difference in their diets. Colobus polykomos must gnaw through a tough pod in order to gain access to a particular type of seed they eat. On e possible explanation for why no significant differences were found is that the seeds do not make up a large enough portion of their diets to have an effect on the sutural complex ity. In other words, seed-eating is dominant in both of these colobine monke ys, but the actual proportion of Pentaclethra macrophylla seeds to the Colobus polykomos diets has never been identifie d (Davies et al. 1999). The difference in masticatory loads between th ese two species may not be large enough to elicit a morphological response fr om the mid-palatal suture. The distribution of stress throughout the palate during mastication may also be a contributing factor to the non-significant results reporte d here. Although numerous studies exist that explore the loading envir onment during mastication in certain parts of the face and cranium, few studies mention a ny stress the palate may receive during this activity. Due to the morphological structur e of the palate, mech anical modeling is difficult. Although the palate probably experi ences different types of stress such as shearing forces, torsional moments, and bending moments (Pre uschoft 1989), it is possible that the stress level is not significant enough to el icit a response from the bone. In order to figure out what the strains are, the maxilla needs to be explored

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53 experimentally. As mentioned earlier, the issue becomes how to model the maxilla. One possible reason the maxilla may experience small loads is the presence of the hard palate. Unlike the mandible, the maxilla has the hard palate which may serve to eliminate or greatly reduce twisting and bendi ng (Daegling and Hylander 1997). Measurements of different size/sh ape variables were also taken from each specimen in order to determine whether or not a relationship exists between these particular measurements and the fractal dimensions of the mid-palatal sutures. Only three regressions showed signifi cance, but the correlation values were very weak (Table 6). When these measurements were regressed against the ruler fractal dimension, palate height and palate depth in Procolobus badius showed significance. Interestingly there were no significant regressions in Colobus polykomos for the ruler fractal dimension. However, the opposite is true for the inform ation fractal dimension. No significant results were found for Procolobus badius but the regression of information fractal dimension versus facial width in Colobus polykomos showed significance. The fact that the so-called equivalent fractal dimensions yield different sign ificances is further evidence that these are not equivalent measur es. More than likely the significant Pvalues for these three regressions reflect a type I error instead of real significance, although there is no way to truly know if a type I error was committed. The results of the regressions suggest that ther e is no predictable pattern be tween either of the fractal dimensions and any of the size/shape variables. One problem limiting interpretation was small sample sizes. When dealing with biological samples, obtaining sufficiently larg e sample sizes can be a problem. An attempt to deal with this problem was made by bootstrapping the data. However, as

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54 previously mentioned, the bootstrapped means were very similar to the parametric means calculated from the raw data, which suggests th at the variation captured in this study is probably a fairly accurate representati on of the populations in question. Another issue arising in this study may stem from the methodology used. Fractal analysis has become a popular method for quan tifying the complexity of intricate cranial sutures. Long (1985) published one of the earliest works on fractals in biology when he examined the sutures present on the shells of ammonites and the cranial sutures of antlered deer. This study was also the firs t to describe how fr actal elaboration is important in the evolutionary process. Long and Long (1992) however, criticize the use of fractal analysis on human cranial sutures beca use they feel that these particular sutures are not self-similar and therefore are not fr actals even though they yield a dimension between 1 and 2. They state that some wa veform curves may yield a dimension up to 1.2, but this is not sufficient to classify them as fractals. Using this reasoning, Long and Long would probably say the sutures presented in this paper are not fractals. If this is true, then this could be an explanation for w hy the two fractal analysis methods used here do not show equivalence. The problem with the above supposition is th at these sutures do fit the definition of a fractal, i.e. they are self-similar and have a dimension between 1 and 2. The main critique of Long and Long (1992) is that th e waveforms that possess a dimension above 1 are not self-similar. Studies conducted on hum an cranial sutures using the box dimension have shown that human cranial sutures are self-similar through the use of logarithmic plots. These graphs show the relationship of the logarithms of the number of squares with length r occupied by the suture against the l ogarithm of 1/ r Benoit 1.3 provided the

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55 logarithmic graphs for each suture analyzed in both of the methods and all of them clearly showed a linear relations hip. This suggests that thes e sutures are self-similar and therefore, by definition, are fractal. Unfortunately this still leaves the proble m of trying to provide an explanation for why the ruler and information fractal dimensions are not de monstrating equivalence like they should. One possibility is that du e to the complicated mathematics that are introduced into the information dimension in order to weight the boxes, the equivalence that exists between the box and ruler dimension is lost. To test this theory, fractal analysis was conducted again on the same sutu res using the box dimension (Tables 9 and 10). A simple regression was conducted and as Figure 9 demonstrates there is still no linear relationship (r-squared 0.0804). This does not support the idea that the more in depth mathematical calculations affected the equivalence. The reason for this may be that the number of points collected could aff ect the outcome of the fractal dimension. This implies that these different methods of fractal analysis are not measuring complexity in the same fashion. Uncert ainty exists as to which method is more appropriate for analyzing human cranial and facial sutures, but one insight gained is that these methods are not equivalent. This means more testing (e.g.) needs to be completed in order to try to determine which method is more accurate. Besides the type of dataset utilized, another factor that may affect which method is better is how the data is collected. In other words, it may be that both methods are appr opriate for analyzing human sutures, but depending on the method used to extract the suture from the specimen and manipulate it so it can be imported into this software, one me thod may prevail over

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56 the other. Regardless of which method was used, no significant results were discovered from this data. Table 9. Box dimensions for Procolobus badius Specimen Designation Sex Box Dimension 2027 Male 1.15339 2028 Male 1.11262 2118 Male 1.18019 2125 Male 1.14647 2126 Male 1.12777 2013 Male 1.12626 2022 Male 1.14486 2104 Male 1.11175 2105 Male 1.12366 2110 Male 1.09819 2113 Male 1.14137 222 Male 1.16990 2231 Male 1.12637 224 Male 1.12912 2243 Male 1.11433 2255 Male 1.12925 232 Male 1.12130 233 Male 1.11166 235 Male 1.12101 239 Male 1.15034 9413 Male 1.12463 942 Male 1.17601 945 Male 1.10132 2005 Female 1.11475 2032 Female 1.14087 223 Female 1.12508 227 Female 1.11091 2014 Female 1.17835 2107 Female 1.12846 2112 Female 1.11445 2215 Female 1.13767 2219 Female 1.14574 2220 Female 1.13643 2240 Female 1.11797 2313 Female 1.12303 236 Female 1.13915 9422 Female 1.12672 9433 Female 1.12309 972 Female 1.11693

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57 Table 10. Box dimensions for Colobus polykomos Specimen Designation Sex Box Dimension 2100 Male 1.12953 2216 Male 1.11993 2311 Male 1.10920 9418 Male 1.10893 2102 Female 1.10568 2103 Female 1.10836 2119 Female 1.13348 2123 Female 1.17746 2124 Female 1.12773 2238 Female 1.15679 2245 Female 1.17051 2314 Female 1.10595 9426 Female 1.13959 Figure 10. Regression of ruler fractal dimension vs box fractal dimension.

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58 CHAPTER 9 CONCLUSION One of the proposed functions of cranial su tures is that they play a role in the transmission and absorption of mechanical load s (Herring 1972). If th is is true, it stands to reason that the morphology of the suture s may reflect the load ing environment to which it is subjected (Rafferty and Herring 1999). Using this r easoning, the hypothesis was made that the more complexity a suture exhibits, the higher amounts of stress it experiences. One problem is how one quantit atively measures sutural complexity. One method that has been applied to this problem over the past two decades is fractal analysis. The fractal analysis conduc ted on the mid-palatal sutures of these two species of colobus monkeys did not show a significan t difference. Sex also did not have a significant effect on the complexity of the mi d-palatal sutures. Although this study does not support the hypothesis that mechanical loadin g is at least partiall y responsible for the morphological complexity of sutures, it by no means discredits this idea. The most probable reason behind the lack of support is that the differences in the diet are not great enough to cause significantly mo re stress in the palate of Colobus polykomos Another aspect that should be examined in the future is the overall structure of the maxilla of these two species. There may possibly be a larger concentration of bone between the point of impact (the teeth) and the mid-palatal sutu re. If so, this bone may absorb the stress before it reaches the suture. Unfortunately, at this point in time, this is pure speculation. The suggestion has also been made that most cranial suture s are not intricate enough to be fractals (Long and Long 1992), but as the term is currently defined human

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59 cranial sutures are fractal objects. This lead s to the question of which fractal analysis technique is most appropriate for examining human cranial su tures. One conclusion that must be drawn from this study is that th e box (information) dimension and the ruler dimension methods are not equivalent. So, which one provides a more accurate depiction of the dimension of these structures? Unfo rtunately, more intensive investigation is required in order to provide an answer for this question. The complexity of these particular sutures did not differ significantly between these species, but this does not mean that the lo ading environment has no effect on sutural growth and morphology. Enough evidence exists to merit further exploration of this topic. Mechanical environments do elicit morphological responses from bone throughout all stages of life whether in modeling or rem odeling. An important point to consider is that sutural complexity may not only be infl uenced by mechanical factors. The sutures serve other functions besides absorption a nd transmission of loads. These other functions, such as growth, may al so affect the complexity of the sutures. Although this is possible, mechanical loading seems to be the most likely factor contributing to the complex morphology of the suture. Many fact ors play a role in palate growth and development; however, exploring the role of mechanical forces is essential to a comprehensive understanding of this process.

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60 LIST OF REFERENCES Bass WM. 1995. Human osteology: a laboratory and field manual, 4th ed. Missouri: Missouri Archaeological Society, Inc. Beecher RM, Corruccini RS. 1981. Effects of dietary consistency on craniofacial and occlusal development in the rat. Angle Orthod 51:61-69. Beecher RM, Corruccini RS, Freeman M. 1983. Craniofacial correlates of dietary consistency in a nonhuman primate. J Craniofac Genet Dev Biol 3:193-202. Bender PL. 2000. Genetics of cleft lip a nd palate. J Pediatric Nursing 15:242-249. Bollert JA, Hendrickx AG. 1971. Morphoge nesis of the palate in the baboon ( Papio cynocephalus ). Teratology 4:343-354. Booth AH. 1956. The distribution of primat es in the Gold Coast. J W Afr Sci Ass 2:122-133. Bouvier M, Hylander WL. 1984. The effect of dietary consistency on gross and histologic morphology in the craniof acial region of young rats. Am J Anat 170:117-126. Brinkley LL, Morris-Wiman J. 1984. The role of extracellular matrices in palatal shelf closure. Curr Top Dev Biol 19:17-36. Burr DB, Martin RB, Schaffler MB, Radin EL. 1985. Bone remodeling in response to in vivo fatigue microdamage. J Biomech 18:189-200. Campbell BG, Loy JD. 2000. Humankind emerging, 8th ed. Boston: Allyn and Bacon. Carter DR. 1984. Mechanical loading histor ies and cortical bone remodeling. Calcif Tissue Int 36:S19-S24. Carter DR, Beaupre GS. 2001. Skeletal func tion and form: mechanobi ology of skeletal development, aging, and regeneration. New York: Cambridge University Press. Carter D, van der Meulen M, Beaupre G. 1998. Mechanobiologic regulation of osteogenesis and arthrogenesi s. In:J Buckwalter, M Ehrlich, L Sandell, S Trippel, editors. Skeletal growth and developm ent: clinical issues and basic science advances. Illinois: American Academ y of Orthopaedic Surgeons. p 99-130.

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61 Ciochon RL, Nisbett RA, Corruccini RS. 1997. Dietary consistency and craniofacial development related to masticatory func tion in minipigs. J Craniofac Genet Dev Biol 17:96-102. Clutton-Brock TH. 1975. Feed ing behaviour of red colobus and black and white colobus in East Africa. Folia Primatol 23:165-207. Cohen, Jr MM. 2000. Sutural Biology. In: Cohen MM, MacLean RE, editors. Craniosynostosis: diagnosis, evaluation and management, 2nd ed New York: Oxford University Press. p 11-23. Copray JCVM, Jansen HWB, Duterloo HS. 1985. An in vitro system for studying the effect of variable compressive forces on the mandibular condylar cartilage of the rat. Archs Oral Biol 30:305-311. Daegling DJ, Hylander WL. 1997. Occlusal fo rces and mandibular bone strain: is the Primate jaw overdesigned? J Hum Evol 33:705-717. Daegling DJ, McGraw WS. 2001. Feeding, diet, and jaw form in West African Colobus and Procolobus Int J Primatol 22:1033-1055. Dasilva GL. 1994. Diet of Colobus polykomos on Tiwai Island: selection of food in relation to its seasonal abundance and nutritional quality. Int J Primatol 15: 655-680. Davies AG, Oates JF, Dasilva GL. 1999. Pa tterns of frugivory in three West African colobine monkeys. Int J Primatol 20:327-357. Del Santo, Jr. M, Minarelli AM, Liberti EA. 1998. Morphological aspects of the midpalatal suture in the human foetus: a light and scanning electron microscopy study. Eur J Orthod 20:93-99. Dibbets JMH. 1992. One century of Wolff’s law. In: DS Carlson, SA Goldstein, editors. Bone biodynamics in orthodontic and ort hopedic treatment. Michigan: Center for Human Growth and Development. p 1-13. Engstrom C, Kiliardis S, Thilander B. 1986. The relationship between masticatory function and craniofacial morphology. II. A histological study in the growing rat fed a soft diet. Eur J Orthodont 8:271-279. Enlow DH, Hans MG. 1996. Essentials of facial growth. New York: W.B. Saunders Company. Falconer K. 1990. Fractal geometry: mathem atical foundations and applications. New York: John Wiley and Sons.

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62 Friede H. 1998. Growth sites and growth m echanisms at risk in cl eft lip and palate. Acta Odontol Scand 56:346-351. German RZ, Crompton AW, Levitch LC, Thexton AJ. 1992. The mechanism of suckling in two species of infant mammal: miniat ure pigs and long-tailed macaques. J Exp Zool 261:322-330. Gibert J, Palmqvist P. 1995. Fractal analysis of the Orce skull sutures. J Hum Evol 28: 561-575. Hall BK. 1984. Developmental processes underlyi ng the evolution of cartilage and bone. Symposium, Zoological Society of London 52:155-176. Hartwig WC. 1991. Fractal analysis of sagittal suture morphology. J Morphol 210:289-298. Hendrickx AG, Peterson PE. 1997. Perspectives on the use of the baboon in embryology and teratology research. Human Reproduction Update 3:575-592. Herring SW. 1972. Suturesa tool in functiona l cranial analysis. Acta Anat 83:222-247. Herring SW. 1993. Epigenetic and functional in fluences on skull growth. In: J Hanken and BK Hall The skull: volume 1. Chica go: University of Chicago Press. p 153206. Herring SW. 2000. Sutures and craniosynostosis: a comparative, functional, and evolutionary perspective. In : MM Cohen, RE MacLean editors. Craniosynostosis: diagnosis, evaluation, and management, 2nd ed. New York: Oxford University Press. p 3-10. Herring SW, Teng S. 2000. Strain in the brai ncase and its suture s during function. Am J Phys Anthropol 112:575-593. Hinton RJ. 1988. Response of the intermaxillary suture cartilage to alterations in masticatory function. Anat Rec 220:376-387. Hylander WL. 1975. The human mandible: leve r or link? Amer J Phys Anthopol 43: 227-242. Hylander WL. 1979. The functional significan ce of primate mandibular form. J Morph 160:223-239. Hylander WL, Johnson KR. 1997. In vivo bone strain patterns in the zygomatic arch of macaques and the significance of these patt erns for functional interpretations of craniofacial form. Amer J Phys Anthropol 102: 203-232.

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63 Hylander WL, Picq PG, Johnson KR. 1991. Masticatory stress hypotheses and the supraorbital region of primates. Amer J Phys Anthropol 86:1-36. Jaslow CR. 1990. Mechanical properties of cranial sutures. J Biomech 23:313-321. Kiliaridis S, Engstrom C, Thilander B. 1985. The relationship between the masticatory function and craniofacial morphology. I. A cephalometric longitudinal analysis in the growing rat fed a soft diet. Eur J Orthod 7:273-283. King AH, Schneiderman ED. 1993. Differential growth among components of the palate in rhesus monkeys. Cleft Palate-Craniofac J 30:302-308. Kirschner RE, LaRossa D. 2000. Cleft lip and palate. Otolaryngologic clinics of North America 33:1191-1215. Kopher RA, Mao JJ. 2003. Suture growth modulated by the oscill atory component of micromechanical strain. J Bone Miner Res 18:521-528. Lanyon LE. 1973. Analysis of surface bone stra in in the calcaneus of sheep during normal locomotion. J Biomech 6:41-49. Lanyon LE. 1974. Experimental support for the tr ajectorial theory of bone structure. J Bone Joint Surg 56B:160-166. Lanyon LE. 1984. Functional strain as a determinant for bone remodeling. Calcif Tissue Int 36:S56-S61. Lanyon LE, Goodship AE, Pye CJ, MacFie JH 1982. Mechanically adaptive bone remodeling. J Biomech 15:141-154. Lanyon LE, Rubin CT. 1984. Static vs dynamic loads as an influence on bone remodeling. J Biomech 17:897-905. Linge L. 1970. A technique for the study of morphology in facial sutures under mechanical influence. Rep Congr Eur Orthod Soc 553-567. Long CA. 1985. Intricate sutures as fr actal curves. J Morphol 185:285-295. Long CA, Long JE. 1992. Fractal dimensions of cranial sutures and waveforms. Acta Anat 145:201-206. Maisels F, Gautier-Hion A, Gautier JP. 1994. Diets of two sympatric colobines in Zaire: more evidence on seed-eati ng in forests on poor soils. Int J Primatol 15:681701.

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64 Mandelbrot BB. 1977. Fractal geometry of nature. New York: W.H. Freeman and Company. Mann RW, Symes SA, Bass WM. 1987. Maxillary suture obliteration: aging the human skeleton based on intact or fragmentary maxilla. J Forensic Sci 32:148-157. Mao JJ. 2002. Mechanobiology of craniof acial sutures. J Dent Res 81:810-816. Martin RB, Burr DB, Sharkey NA. 1998. Skeletal tissue mechanics. New York: Springer-Verlag, Inc. Meade JB, Cowin SC, Klawitter JJ, Van Bu skirk WC, Skinner HB. 1984. Bone remodeling due to continuously applied loads. Calcif Ti ssue Int 36:S25-S30. Melsen B. 1975. Palatal growth studied on human autopsy material. Am J Orthod 68:42-54. Montiero LR, Lessa LG. 2000. Comparative anal ysis of cranial suture complexity in the genus Caiman (Crocodylia, Alligatoridae). Rev Brasil Biol 60:689-694. Moore KL, Persaud TVN. 2003. The developing human: clinically oriented embryology, 7th ed. Philadelphia: Saunders Publishing. p 221-234. Moss M. 1969. A theoretical analysis of th e functional matrix. Acta Biotheoretica 18: 195-202. Oates JF. 1994. The natural history of Afri can colobines. In: AG Davies, JF Oates, editors. Colobine monkeys: their ecology, behaviour and evolution. Cambridge: Cambridge University Press. p 75-128. O’Connor JA, Lanyon LE, MacFie H. 1982. Th e influence of strain rate on adaptive bone remodeling. J Biomech 15:767-781. Oudhof HAJ. 1982. Sutural growth. Acta Anat 112:58-68. Persson M. 1970. Postnatal growth of faci al sutures. Rep Congr Eur Orthod Soc 543552. Persson M. 1995. The role of sutures in nor mal and abnormal craniofacial growth. Acta Odontol Scand 53:152-161. Pirelli P, Botti F, Ragazzoni E, Arcuri C, Cocchia D. 1999. A light microscopic investigation of the human midpalatal suture. It J Anat Embryol 104:11-18. Preuschoft H. 1989. Biomechanical approach to the evolution of the facial skeleton of hominoid primates. Fortschr itte der Zoologie 35:421-431.

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66 Wainwright SA. 1988. Form and function in organisms. Amer Zool 28:671-680. Yamamoto S. 1996. The effects of food cons istency on maxillary gr owth in rats. Eur J Orthod 18:601-615. Yu JC, Wright R, Williamson MA Braselton JP, Abell ML. 2003. A fractal analysis of human cranial sutures. Clef t Pal-Craniofac J 40:409-415.

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67 BIOGRAPHICAL SKETCH Jennifer Hotzman is one of four children and was born in Meridian, Mississippi. She received her Bachelor of Arts degr ee in anthropology from the University of Southern Mississippi in 2000. After gra duation she continued her education at the University of Florida. While completing he r graduate studies, Ms. Hotzman also worked full-time for Regeneration Technologies, a company that manufactures allografts for surgical procedures. After obtaining her Ma ster of Arts degree, she plans on continuing her graduate studies at th e University of Florida.


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Title: Dietary Consistency and Sutural Morphology: The Complexity of the Mid-Palatal Suture in Procolobus badius and Colobus polykomos
Physical Description: Mixed Material
Copyright Date: 2008

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DIETARY CONSISTENCY AND SUTURAL MORPHOLOGY: THE COMPLEXITY
OF THE MID-PALATAL SUTURE IN Procolobus badius AND Colobus polykomos














By

JENNIFER LANE HOTZMAN


A THESIS PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF ARTS

UNIVERSITY OF FLORIDA


2004

































Copyright 2004

by

Jennifer Lane Hotzman















ACKNOWLEDGMENTS

I would like to take this opportunity to thank Dr. Scott McGraw for allowing me to

use his collection of specimens housed at Ohio State University. I also would like to

thank Dr. David Daegling (University of Florida) for all of his guidance and advice

throughout this project. My fellow colleagues Ron Wright and Joe Hefner also offered

assistance throughout a difficult period and helped me to problem shoot certain aspects of

this project. Lastly I would like to thank my parents, Malcolm Hotzman and Linda Petty,

as well as Benjamin Ripy for their continued support and encouragement. This project

would not have been possible without the help and support I received from all of these

individuals.
















TABLE OF CONTENTS



A C K N O W L E D G M E N T S ................................................................................................. iii

LIST OF TABLES ..................................... .. .......... .................................... vi

LIST OF FIGURES ......................................... .................................... vii

ABSTRACT ................................................... ................. viii

CHAPTER

1 M ECHAN ICS IN BONE GROW TH .....................................................................1...

W o lff s L a w .................................................................................................................. 1
C oncepts of Stress and Strain ........................................ ....................... ...............4...
Prim ary and Secondary C artilages........................................................... ............... 5
B one M odeling and R em odeling ............................................................. ...............6...
Effect of Dietary Consistency on Bone Growth.................................... ............... 11

2 GR O W TH OF TH E PALA TE ...................................... ...................... ................ 16

Embryological Growth and Developm ent............................................. ............... 16
Postnatal G row th and D evelopm ent...................................................... ............... 18

3 S U T U R E S ................................................................................................................. .. 2 2

Functions of Sutures ............................ .......... ........................ 22
Sutural Biology and M orphology ....................... ............................................... 24
Sutures and Loads ..... .. ................... ........... .....................................27

4 ECOLOGY AND DIET OF COLOBUS MONKEYS.........................................30

B ackgrou n d Inform action .............................................................................................30
S tu d y S am p le .............................................................................................................. 3 1

5 FR A C TA L A N A L Y SIS .............................................. ......................................... 33

Box Dimension and Information Dimension Methods.........................................34
R u ler D im en sio n ......................................................................................................... 3 5


iv










6 M A TERIAL S AN D M ETH OD S ............................................................ ................ 36

7 R E S U L T S ........................................................................................... .................... 3 9

8 D ISCU SSION ............................................................................... . .. ...............52

9 CON CLU SION ...........................................................................................................58

LIST O F R EFEREN CE S .................................................................................................60

BIO GR APH ICAL SK ETCH ................ .. ........................ ..................... ................ 67














































v















LIST OF TABLES

Table page

1 D efinitions of m easurem ents collected ............................................... ................ 36

2 Basic statistics for variables associated with Colobuspolykomos ........................ 40

3 Basic statistics for variables associated with Procolobus badius .........................41

4 Bootstrapped versus parametric means for ruler fractal dimension......................43

5 Boostrapped versus parametric means for information fractal dimension ............43

6 Significant regressions ............. ................ ................................................ 43

7 Fractal dim tensions of Colobuspolykomos.......................................... ................ 44

8 Fractal dim tensions of Procolobus badius ........................................... ............... 45

9 Box dim tensions for Procolobus badius .............................................. ................ 56

10 Box dim tensions for Colobuspolykomos............................................. ................ 57















LIST OF FIGURES

Figure page

1 "V principle of bone rem odeling ...................................................... ................ 19

2 B ox plot for ruler fractal dim ension ................................................... ................ 42

3 Box plot for information fractal dimension.........................................................42

4 Mid-palatal suture of Procolobus badius 2107. .................................................46

5 Mid-palatal suture of Procolobus badius 9433. .................................................47

6 Regression of ruler versus information dimension. ............................................48

7 Mid-palatal suture of Procolobus badius 227 ................................................... 49

8 Mid-palatal suture of Procolobus badius 942 ....................................................50

9 Mid-palatal suture of Colobus polykomos 2103..................................................51

10 Regression of ruler versus box dimension ..........................................................57















Abstract of Thesis Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Master of Arts

DIETARY CONSISTENCY AND SUTURAL MORPHOLOGY: THE COMPLEXITY
OF THE MID-PALATAL SUTURE IN Procolobus badius AND Colobus polykomos

By

Jennifer Lane Hotzman

August 2004

Chair: David Daegling
Major Department: Anthropology

The mechanical environment is one of many influential factors affecting

craniofacial growth and development. Although the mechanism is unclear, consensus

exists that loads elicit a morphogenetic response from bone in general, including the

maxillary bone in the craniofacial region. Mastication is one of the major sources of

loading for the facial and cranial regions. The morphology of cranial and facial sutures is

thought to be affected by the loading environment to which it is exposed. If this is true,

then dietary consistency, which requires changes in the mechanics of mastication, should

also affect the morphology of sutures.

The hypothesis under construction is that the higher the loads the suture is

exposed to, the more complexity the suture should exhibit. In order to test this

hypothesis, the mid-palatal suture of two sympatric species of colobus monkeys was

examined. One species (Colobuspolykomos) has a particularly hard seed present in its

diet that Procolobus badius does not have. If the above hypothesis is true, then Colobus









polykomos would be expected to have a more complex mid-palatal suture due to its

requirement of producing larger masticatory forces than Procolobus badius. Fractal

analysis was used to measure the complexity of the sutures. Once the fractal dimensions

were obtained, a 2-way ANOVA was performed, separating the species as well as the

sexes. There were no significant differences in the complexities of the mid-palatal

sutures of the two species. The data collected do not support the hypothesis that

masticatory changes associated with diet directly influence sutural complexity.














CHAPTER 1
MECHANICS IN BONE GROWTH

Craniofacial growth and development is influenced by many different factors,

including the mechanical environment (Herring 1993). The maxillary bone, in particular

the palate, is more than likely exposed to different types of loads throughout the earliest

stages of growth. For example, human infants suckle and as they grow older, are weaned

and then engage in mastication. These different activities likely result in different types

and magnitudes of stress, which elicit a morphogenetic response from the bone (Herring

1993, Martin et al. 1998). When mastication begins, the consistency of the diet has been

shown experimentally to affect craniofacial growth and development (Beecher et al.

1983, Kiliaridis et al. 1985, Yamamoto 1996, Ciochon et al. 1997).

In addition to affecting overall bone growth and development, masticatory loads

may also influence the morphology of cranial sutures. Several researchers have

postulated that sutural morphology can reflect the load history of the structure in question

(Herring 1972, Herring and Teng 2000, Wagemans et al. 1988). Provided this is the case,

then the morphology of the sutures located in the palate should reflect its load history. If

development is mechanically mediated, sutural morphology could provide insight into

possible etiologies for abnormal craniofacial developments such as cleft lip and palate, a

common birth defect requiring surgical intervention.

Wolff's Law

The idea that bone adapts to its mechanical environment is not new. Julius Wolff

has been credited with formulating this idea in the late 1800s, but the idea has been traced









as far back as Galileo in the 1600s (Martin et al. 1998). Wolff's law states that the

architecture of living bone continuously adapts to changes in the mechanical environment

to which bone is subjected. Although Wolff's law is generally accepted as true, the

biological aspects of the law that he formulated have proven to be false (Dibbets 1992).

Three main biases exist in his arguments: his theory on interstitial bone growth, the role

of heredity in bone growth, and his concept of function (Dibbets 1992).

Wolff was convinced that bone growth underwent the same mechanisms as soft

tissue growth, which is to say that bone growth consisted solely of cell division and the

accumulation of intracellular material. He adamantly denied the process of remodeling

because he did not believe that bone actually resorbed. Dibbets (1992) points out that the

reason Wolff held so firmly to this concept of interstitial bone growth was because, in his

view, the trabecular architecture preexisted in the compact (cortical bone) and was not

the result of a dynamic process.

The idea that trabecular bone architecture was inherited was based on the fact that

Wolff had observed the distinct trabecular patterns in fetuses, which could not have been

exposed to loads yet (Dibbets 1992). However, the fetus is exposed to mechanical forces

in utero. Forces are intermittently imposed on the fetus by skeletal tissue stresses that are

caused by muscular contractions from the increasingly strong and active developing

muscular system (Carter and Beaupre 2001).

Wolff s concept of function is the third bias because the definition he provided

differs greatly from how function is usually defined today. If researchers were asked to

define the term function today, they would probably define it as changing structure, i.e. a

dynamic process requiring action (Wainwright 1988). Wolff defined function as a static









requirement that needed to be met (Dibbets 1992). Unfortunately, the term function is

often not explicitly defined by researchers, which causes ambiguity as to exactly which

definition of function is being applied.

If Wolff defined function completely differently than it is defined by most today,

where did the modem day definition develop? The answer is from one of Wolff s

contemporaries, Wilhelm Roux. Roux saw function as a dynamic interaction as opposed

to a static constraint and recognized that information for the developing bone was

partially provided by loading and unloading (Dibbets 1992). He referred to the

physicochemical processes that aid development as "Entwicklungsmechanik" or

"developmental mechanics" (Carter et al. 1998).

The forces that affect skeletogenesis can be studied at different scales of analysis,

including the molecular, cellular, tissue, and organ levels (Carter and Beaupre 2001). In

the time period in which Wolff and Roux worked, the analyses generally took place on

the tissue level due to lack of technology. As technological advances are made, more

studies are conducted at the molecular and cellular levels (Carter et al. 1998). Molecular

level studies have begun to study the role of integrins, which are cell surface receptors

involved in cell adhesion to other cells and the extracellular matrix, and the cytoskeleton,

while cellular studies have shown that hydrostatic pressure and shear loading of cells

have a direct influence on gene expression and cell biosynthesis (Carter et al. 1998). The

tissue level, however, is still the scale at which most analyses occur, including the one

conducted here. One reason for this is because the technology needed to conduct tissue

level analyses is generally more accessible than the technology needed for cellular and

molecular studies. Analyses can also be conducted at the organ level, but they provide









little insight into the underlying mechanisms of how bone responds to different

mechanical conditions (Carter and Beaupre 2001). Only when the organs are broken

down into smaller units, e.g., tissues, can we begin to evaluate and understand the

physical conditions of connective tissue cells (Carter and Beaupre 2001).

Concepts of Stress and Strain

Two very important concepts that are useful when studying mechanical forces at

the tissue level are stress and strain. When discussing stress and strain in biological

materials, it is important to keep in mind that they are defined as if the tissue under study,

in this case bone, was a homogenous material (Carter et al. 1998). In this "continuum

model" representation, the fact that bone consists of molecules, discrete atoms, and

crystals interacting with one another is ignored (Carter and Beaupre 2001). This means

that the material properties represent average properties over some volume that is large in

comparison to the microstructural features of the tissue (Carter and Beaupre 2001).

Stress is a measure of normalized intensity of a force and is the load per unit area,

while strain is a measure of normalized load deformation. Strain, in simplest terms, is

defined as the fractional change in dimension of a loaded body (Martin et al. 1998). Both

stress and strain are tensor quantities, so they have a magnitude and direction. The stress

state can also be represented with scalar quantities referred to as invariants. Scalar

quantities have a magnitude, but no direction. The two most common stress invariants

are referred to as hydrostatic stress and octahedral shear stress. Hydrostatic stress can

either be positive (hydrostatic tension) or negative (hydrostatic compression or pressure)

and is calculated as the average value of the three principal stresses. On the other hand,

octahedral stress can only be a positive number and will only change the shape and not

the volume of the material in question (Carter and Beaupre 2001). These two stress









invariants affect cartilage growth and ossification differently. Octahedral shear stress

causes an acceleration of cartilage growth and ossification, while hydrostatic compressive

stress slows it down (Carter and Beaupre 2001).

Primary and Secondary Cartilages

Primary and secondary cartilages are both important to skull growth. These two

cartilages are distinguished based on the timing of their formation. Primary cartilage

precedes the development of the replacement bones that form the primary skeleton.

Secondary cartilage is different because it does not form on dermal bones until after

intramembranous ossification has begun (Hall 1984). Unlike most of the bones in the

human skeleton, dermal bones are not preformed in cartilage, but arise directly from

connective tissue membranes. When studying the influence of mechanics on craniofacial

growth, the secondary cartilage is important because it does not develop in the absence of

mechanical stimulation (Herring 1993). Secondary cartilage only differentiates from

progenitor cells in response to mechanical stimulation (Hall 1984). This cartilage is

found in association with many cranial bones, sutures, and the upper and lower alveolar

processes in mammals. These locations are sites of either articulations or muscle

attachments, which provides support for the idea that mechanical stimulation is necessary

for the differentiation of secondary cartilages (Herring 1993).

The mandibular condyle is the only major growth site of secondary cartilage

anywhere in the mammalian skeleton (Herring 1993); therefore most of the studies on

jaws have been on the condyle (Simon 1977, Copray 1985, Throckmorton and Dechow

1994). However, the condyle is not the only secondary cartilage that is sensitive to

mechanical changes in the environment. Hinton (1988) studied the response of the

cartilage that is present in the mid-palatal suture to changes in masticatory function. He









divided rats into separate groups based on dietary consistency and/or incisor amputation,

then performed biochemical and histological analyses. Dietary consistency and/or incisor

amputation did alter the morphology and the metabolism of the mid-palatal suture to

varying degrees. The group of rats that were fed a soft diet and had their incisors

amputated were affected the most, with their sutures becoming largely fibrous. The

effect of dietary consistency on bone growth will be discussed in more detail later.

Bone Modeling and Remodeling

There is consensus that the mechanical environment affects bone growth, but how

is another story. Several factors are involved when discussing the mechanical

environment, such as the frequency of the loading and the types of loads applied. Bone

growth and modeling are not the only processes that the loading conditions affect. Bone

remodeling is also heavily influenced by mechanical conditions. Bone modeling and

remodeling both refer to the actions of osteoblasts and osteoclasts in reshaping and

replacing portions of the skeleton (Martin et al. 1998). However, these two processes are

different from one another in several ways.

Martin et al. (1998) provide a list of differences that exist between the processes

of modeling and remodeling. Although both modeling and remodeling involve

osteoblasts and osteoclasts, in modeling these two cell types work independently while in

remodeling their actions are coupled, i.e. sequential. Another difference between these

two processes is that modeling affects the size and/or shape of the bone, while

remodeling typically does not affect either size or shape. Modeling and remodeling are

both most active before skeletal maturity is reached; however, the rate of modeling versus

remodeling is much more reduced after skeletal maturity is reached. Unlike modeling,

remodeling occurs throughout life. Finally when modeling occurs at a particular site the









process is continuous and prolonged while remodeling is episodic and has a definite

beginning and ending.

Although both modeling and remodeling are affected by mechanical conditions,

most of the experimental studies have only involved the process of remodeling (Lanyon

et al. 1982, O'Connor et al. 1982, Carter 1984, Lanyon 1984, Lanyon and Rubin 1984,

Meade et al. 1984, Burr et al. 1985, Rubin and Lanyon 1985). The reason for this is that

mature experimental animals are used to try to eliminate as many unknown variables as

possible. So many factors influence bone growth that controlling all these variables,

some of which are still unknown, is difficult, if not impossible. For this reason, most of

the experimental research focuses on the process of remodeling since modeling is

practically nonexistent once the skeleton has reached full maturity.

Three important variables that are known to influence remodeling include strain

magnitude, strain rate, and strain distribution (Lanyon 1984). Lanyon et al. (1982)

conducted an experiment using mature sheep that involved excising a portion of a sheep's

ulna and then exposing the sheep to peak principle walking strains. They found that the

bone adapted to produce strains that were lower than before the osteotomy, which is not

consistent with the view that bone reacts to control strain magnitude. Instead, they

concluded that adaptive remodeling of periosteal bone is influenced by alterations in

strain distribution rather than peak strains alone. Rubin and Lanyon (1985) conducted a

similar study using turkeys and came to a comparable conclusion that bone remodeling is

sensitive to both strain distribution as well as strain magnitude.

Strain rate is also an influential variable in bone remodeling. In order to evaluate

how strain rate affects remodeling, O'Connor et al. (1982) chronically inserted implants









into the radius and ulna of mature sheep. These implants were subjected to both bending

and compressive loads while varying the peak strains and strain rates. Their conclusion

was that in order for remodeling to occur there needs to be sufficiently high strains and

appropriate strain rates. This leads to the question of whether or not the frequency of the

loads, i.e. static and dynamic loads, affect bone remodeling.

Lanyon and Rubin (1984) conducted experiments on avian ulna in order to

address the question of whether or not both static and dynamic loads affect bone

remodeling. Remodeling activity was assessed under three different conditions, disuse

alone, disuse with a superimposed continuous compressive load, and disuse interrupted

by a short daily period of intermittent loading. From this experiment, Lanyon and Rubin

(1984) concluded that remodeling occurs under both dynamic and static loads when the

bone is exposed to strains within the functional strain range, but the remodeling is more

effective under dynamic loading conditions. Meade et al. (1984) conducted a similar

experiment by exposing the femora of adult dogs to continuously applied loads and noted

that there was an outward movement of the periosteal surface in response to the

continuously applied loads, but little or no effect was seen on the endosteal surface of the

bone.

In addition to the changes in strain distribution, strain magnitude, and strain rate,

bone also initiates remodeling as a response to fatigue microdamage (Burr et al. 1985).

Burr et al. (1985) tested the validity of the theory that osteonal remodeling is triggered by

microdamage by conducting several different experiments on adult dogs. The data that

was collected support the idea that fatigue microdamage is a significant factor in the

initiation of remodeling.









No doubt exists that the mechanical environment is influential to bone remodeling.

Factors other than mechanical environment, however, can also affect bone remodeling.

For example, bioelectrical currents generated by blood flow and cell membranes may

also affect bone remodeling, so the situation is not straightforward (Rubinacci and

Tessari 1983).

According to Herring (1993), characterization of the real loading regime of

skeletal elements is needed in order to determine the functional influences of bone

growth. Although computer models and strain gage technology have been helpful in

trying to determine stress distributions, both have limitations. The major limitation of the

computer models is that all local effects must be ignored or modeled precisely, which is

currently impractical. Strain gages help overcome this problem, but they are limited to a

very restricted area of the structure being studied. Even though there are technological

difficulties when trying to determine the loading regime of skeletal elements, successful

experiments have been conducted that yielded useful information.

Lanyon (1973, 1974) performed experiments on the calcaneus of sheep using

rosette strain gages and was able to demonstrate that the trabecular orientation

corresponded with the principal compressive and tensile strain directions. This

experiment was able to confirm what Wolff had postulated earlier about principal stress

directions coinciding with trabecular orientation (Martin et al. 1998). Once this was

confirmed, attention turned to the question of what type of load is responsible for

apposition and resorption. Herring (1993) argues that resorption corresponds to the

orientation of compressive strain, while periosteal bone growth corresponds generally

with the orientation of tensile strain. Of course, as mentioned earlier, it is not only the









type of force applied, but also the frequency and magnitude that determines whether or

not bone is deposited or resorbed.

The skull may experience loading from several sources including forces from the

inertia and weight of the skull itself, joint reaction forces, forces from the muscles, and

trauma (Russell and Thomason 1993). If these forces act directly on the structure, then

shearing stresses will result. Other types of forces that the skull may experience include

bending and torsion. Preuschoft (1989) stated that the bite forces inside the upper jaw

evoke shearing forces, torsional moments, and bending moments; unfortunately he does

not specify the sources or nature of these different loading conditions. Different regions

of the facial skeleton seem to experience variable amounts of stress during biting and

mastication, so every facial bone may not be specifically designed for countering

mechanical loads from mastication (Hylander et al. 1991, Hylander and Johnson 1997).

The mandible is one area of the face where extensive research has been conducted

to determine the forces experienced during mastication (Hylander 1975, Hylander 1979).

Hylander (1975) explored the issue of whether or not the mandible functions like a lever

during mastication and concluded that the mandible does function like a lever and

behaves more or less like a curved beam. Hylander (1979) also explored the functional

significance of the primate mandibular form and concluded that the symphseal region

does appear to be an adaptive response to masticatory loads, particularly unilateral molar

bite force. Unfortunately the upper and lower jaws do not function in the same manner.

Due to the structural nature of the maxilla, modeling the lower jaw experimentally has

been difficult, if not impossible, to date. Although the conclusion can be made that the

maxilla does experience bending and twisting like the mandible due to the presence of the









hard palate, there is no experimental evidence present that does state what type of stresses

the maxilla experiences during mastication (Daegling and Hylander 1997). Nevertheless,

the forces generated by mastication are still of particular interest when examining the

palate.

Effect of Dietary Consistency on Bone Growth

Several studies have been conducted over the years that support the idea that

dietary consistency affects craniofacial bone growth and development. Many of these

studies were initiated in an attempt to determine why Western societies had such high

rates of malocclusion compared to non-industrial societies (Beecher et al. 1983, Ciochon

et al. 1997). The theory that forceful chewing was necessary for proper growth became

one avenue of exploration. Beecher et al. (1983) examined this hypothesis by raising two

groups of squirrel monkeys; one group was given a naturally tough diet while the other

was given a diet of artificially softened foods. Significant differences were noted

between the two groups and they concluded that there is a minimum threshold of stress

needed for proper craniofacial development to occur.

The animals given the soft diet in the study of Beecher et al. (1983) exhibited

maxillary arch narrowing and increased palatal height. These two characteristics

occurring simultaneously suggests that maxillary arch collapse maxillaryy arch

narrowing), the most common occlusal problem in American youths, probably occurs

because of differences in the growth of the mid-palatal suture and the fact that teeth from

the maxillary alveolar process are not correctly aligned with the mandibular teeth. Other

cranial sutures were also affected by dietary consistency. Distinct differences in

calcification were seen in the lambdoid and sagittal sutures through the use of

radiographs. The soft diet animals had a much broader radiolucent area at the sutures









than the hard diet animals, which means that the sutures in the soft diet area are more

patently opened and less calcified.

Squirrel monkeys are not the only experimental animals that have supported the

idea that craniofacial growth and development is affected by the consistency of diet.

Experiments have also been conducted using rats (Beecher and Corruccini 1981, Bouvier

and Hylander 1984, Kiliaridis et al. 1985, Yamamoto 1996) and minipigs (Ciochon et al.

1997). Differences were found in the mandibles of Yucatan minipigs that were raised on

diets of varying consistencies (Ciochon et al. 1997). In addition to examining the bones,

Ciochon et al. (1997) also examined the weight of the muscles involved in mastication.

They found that the weights for the superficial masseter, deep masseter, and temporalis

muscles were all significantly higher in the hard diet group. The frontal profiles of the

cranium also differed between the two groups; the hard diet group displayed a steep

profile while the soft diet group displayed an overall more horizontally oriented profile.

Morphological differences in the shape of the mandible between the two groups were

also noted. Unfortunately, the maxilla was not the main focus of this study so very little

information concerning this structure was presented. However, Ciochon et al. (1997) did

note that the palate was relatively longer in the soft diet group. They also took

measurements of the maxillary arch breadth and unlike the results reported by Beecher et

al. (1983) in the squirrel monkeys, there was no difference found between the groups of

the Yucatan minipigs.

Rats have served as another common experimental animal for pursuing the effects

of dietary consistency on craniofacial growth and development. Beecher and Corruccini

(1981) conducted a study using rats that consisted of two groups, a soft diet group and a









hard diet group. They reported that the rats fed a soft diet had a significantly narrower

maxillary arch breadth compared to the hard diet group. The animals in the soft diet

group weighed approximately 13% less than the animals in the hard diet group at the end

of the experiment; however, the weight difference was not found to be significant.

Bouvier and Hylander (1984) disagree with Beecher and Corruccini (1981) about the

weight differences not being significant. Bouvier and Hylander (1984) conducted a

similar experiment and found that the maxillary arch length was significantly different

between the animals raised on different diets, but once corrections were made for the

weight differences, the maxillary arch differences became nonsignificant.

Kiliaridis et al. (1985) used cephalometric longitudinal analysis for growing rats

using a normal diet group and a group fed a soft diet. Differences were noted in the

growth patterns of both the neurocranium and the viscerocranium between the two

groups. The viscerocranium of the soft diet group showed a more orthocranial position,

which refers to the skull being of medium height relative to length, with the most

noticeable changes occurring in the nasal area. Changes were also noted in the incisors

of the upper jaw as well as the mandible. The incisors of the upper jaw showed a greater

proclination in relation to occlusal and palatal planes in the soft diet group, while the

gonial angle of the mandible showed a decreased appositional rate.

As can be seen by comparing the studies of Beecher and Corruccini (1981) and

Bouvier and Hylander (1984), no consensus exists on the effect dietary consistency has

on the growth of the palate. Yamamoto (1996) examined how food consistency effects

the growth of the palatal region of the maxillary complex through the use of bone

histomorphometry to try to aid in the resolution of this issue. Specifically, the goal was









to investigate how the consistency of the diet affected the pattern of bone apposition at

the growth site of the palatal region. As with the previous studies, the rats were divided

into two groups; one was fed a hard (solid) diet while the other was fed a soft (liquid)

diet. There were significant differences found between the two groups.

Yamamoto's (1996) results agreed with those of Kiliaridis et al. (1985) in that the

vertical growth of the palate differed between the two groups and there was a more

anteriorly directed growth rotation of the palate in the soft diet group. Other studies that

examine the underlying mechanism for this difference have noted a marked decrease in

the bone appositional rate in the areas of muscle insertion in the anterior part of the

viscerocranium (Engstrom et al. 1986); however, the area under consideration in

Yamamoto's (1996) study is not an area of muscle insertion. This implies that the

changes in the palatal region of the maxilla cannot be caused directly by activities such as

muscle action; however, muscle action can have large effects due to mechanical activities

such as bending and twisting. Yamamoto (1996) proposes that although the mechanical

forces generated by mastication probably have an indirect affect on the growth, another

factor to consider is that the growth of other structures such as the neurocranium also

affects the growth of the viscerocranium under different occlusal loading conditions.

As mentioned previously with the study of Ciochon et al. (1997), the growth of

the mandible has also been explored in relation to dietary consistency. One line of

reasoning is if an animal has a diet that consists of hard items then their mandible would

be more massive in terms of bone than a similar sized animal with a softer diet. Just like

the differences reported in the maxillary arch breadth between the different studies cited

above, differences exist on this issue concerning the mandible. A study conducted by









Daegling and McGraw (2001) does not support the line of reasoning expressed above.

They examined the mandibles from two different species of colobus monkeys that are

similar in size and sympatric, but one of the species (Colobuspolykomos) has a diet

containing food items of harder consistency. One would expect that Colobuspolykomos

would have a more robust mandible than the other species (Procolobus badius), but this

is not the case. In fact, mandibular morphology does not reflect the differences in diet.

The studies mentioned so far have been concerned with mastication, but this is not

the only process that mammals use for oral food intake. Infant mammals engage in a

unique form of feeding referred to as suckling. Although the mechanism of suckling has

been explored (German et al. 1992) as well as the transition from suckling to drinking at

weaning (Thexton et al. 1998), there have been no studies conducted on the types of

loads this mechanism produces and whether or not these loads also affect craniofacial

growth and development.














CHAPTER 2
GROWTH OF THE PALATE

Embryological Growth and Development

Facial development begins around the third week of gestation with the development

of five facial swellings, or primordia, in the frontonasal and visceral arch regions. These

five primordia consist of the frontonasal prominence, which forms the forehead and nose,

two maxillary prominences, which form the lateral stomodeum, or primitive mouth, and

two mandibular prominences, which form the caudal stomodeum (Bender 2000, Scheuer

and Black 2000). Within each of these prominences, neural crest cells differentiate into

fibrous connective tissue, all the dental tissues except enamel, skeletal and connective

tissue of the face, cartilage, and bone. By the end of the fourth week, the lower aspect of

the frontonasal prominences develop bilateral oval thickenings of the surface ectoderm

known as nasal placodes, which will produce the medial and lateral nasal prominences

(Kirschner and LaRossa 2000, Moore and Persaud 2003). The intermaxillary segment of

the maxilla forms when the medial nasal prominences merge. This segment gives rise to

the philtrum of the upper lip, the premaxillary part of the maxilla, and the primary palate

(Moore and Persaud 2003). The maxillary prominences enlarge during the fifth week and

connect with the lateral nasal prominences to establish continuity between the nose and

the cheek while the maxillary prominences fuse with the medial nasal prominences to

complete the lip.

Palatogenesis begins at the end of the fifth week and continues until the twelfth

week. The median palatine process develops from the intermaxillary segment during the









sixth week (Moore and Persaud 2003). This process forms the primary palate, which

gives rise to the premaxillary part of the maxilla. In the adult hard palate, the premaxilla

represents only a small portion of the hard palate anterior to the incisive foramen forming

the part of the maxillary alveolus that bears the incisors.

During the sixth week, the secondary palate develops from the paired lateral

palatine processes also known as the palatal shelves. The lateral palatine processes are

two mesenchymal projections that extend from the internal aspects of the maxillary

prominences (Moore and Persaud 2003). Initially both palatal shelves are oriented

vertically on either side of the developing tongue. As the tongue descends, the palatal

shelves gradually move to a horizontal position where they will meet and fuse at the

midline. An intrinsic shelf elevating force is believed to be responsible for the movement

of the palatal shelves. This force is generated by the hydration of hyaluronic acid in the

mesenchymal cells within the palatal processes (Moore and Persaud 2003). Hyaluronic

acid acts as a water barrier and provides "tissue turgor" that moves the palatal shelves

(Brinkley and Morris-Wiman 1984). The movement of the palatal shelves begins in the

seventh week, but fusion is not completed until the twelfth week. Fusion of the palatal

shelves results in the formation of the uvula, soft palate, and hard palate posterior to the

incisive foramen (Kirschner and LaRossa 2000).

For nonhuman primates such as baboons and macaques, palatogenesis occurs

approximately at the same stage as humans (Hendrickx and Peterson 1997). The

underlying mechanisms for palatal closure are also thought to be the same between these

primate species and humans (Bollert and Hendrickx 1971, King and Schneiderman

1993). Since the timing and the underlying mechanisms of palatal closure are similar in









baboons, macaques, and humans, then catarrhine primates may be appropriate animals to

use in order to explore orofacial teratogenesis in humans (Bollert and Hendrickx 1971).

Postnatal Growth and Development

Growth refers to a structure, in this case bone, changing in magnitude (Enlow and

Hans 1996). Contrary to prior belief, there are no centralized and self-contained growth

centers; instead all portions of the bone play a role in the growth of the structure (Enlow

and Hans 1996). As opposed to growth centers, the functional matrix is the determinant

of the skeletal growth processes. The functional matrix is all the tissues and spaces that

work together to fulfill a particular function (Moss 1969). This concept provides an

explanation of what happens during craniofacial growth, but not how the cellular and

molecular mechanisms underlying growth work.

Remodeling and displacement are two basic kinds of growth movements involved

in facial growth. Remodeling serves five main functions that are outlined by Enlow and

Hans (1996): 1) progressively changes the size of the whole bone, 2) sequentially

relocates the component regions of the whole bone to allow for overall enlargement, 3)

shapes the bone for its functions, 4) fine-tunes the outline of separate bones to each other

and their surrounding soft tissues, and 5) carries out structural adaptations to the intrinsic

and extrinsic changes in conditions. This remodeling is not synonymous with the type of

remodeling discussed earlier. Unlike Martin et al. (1998), Enlow and Hans (1996) do not

make a distinction between the processes of modeling and remodeling. Instead, Enlow

and Hans (1996) make a distinction between remodeling (as defined above) and

displacement. Displacement is the process of the physical movement of the whole bone

and occurs when remodeling is simultaneously resorbing and depositing bone.









Palatal remodeling occurs through a process known as the "V" principle. This

concept is based on the fact that many cranial and facial bones, including the palate, have

a V-shaped configuration (Enlow and Hans 1996). Bone deposition takes place on the

inner side of the V while resorption takes place on the outer side of the V (Figure 1,

adapted from Enlow and Hans (1996)). In the case of the maxillae, the external side of

the anterior part of the maxillary arch is resorbed while bone is deposited on the inside of

the arch. This process increases the width of the arch causing the palate to become wider

(Enlow and Hans 1996). Growth along the mid-palatal suture also adds to the

progressive widening of the palate and maxillary (alveolar) arch (Friede 1998).

Widening of the palate continues into adulthood (Scheuer and Black 2000).













/ /

A\ /

Figure 1. "V" principle of facial growth. As the V moves from position A to position B,
the structure increases in overall dimensions. The + marks indicate bone
deposition on the inner side of the V, while the marks indicate bone
resorption on the outside surface.

Lengthening of the hard palate occurs partly in the transverse suture and partly by

the apposition of bone to the posterior margin (Melsen 1975). The growth in the

transverse suture continues until puberty, but the appositional activity continues until









approximately 18 years of age. Disagreement exists concerning the appositional activity

on the posterior margin of the palate. According to Sejrsen et al. (1996), little growth

occurs at the posterior border of the hard palate. They reached this conclusion by

studying archaeological samples that show a constant distance between the greater

palatine foramen and the posterior margin of the palatine bone at various dental stages.

Sejrsen et al. (1996) attribute lengthening of the hard palate almost solely to growth in the

transverse suture. Although the amount of apposition that occurs on the posterior margin

is controversial, consensus exists on the fact that little to no apposition occurs on the

anterior margin. The transverse palatine suture remains in the posterior part of the bony

palate from birth to adulthood regardless of the minute amount of activity on the anterior

margin, which suggests that highly differentiated growth must occur postnatally in the

transverse palatine suture (Silau et al. 1994).

The palatal growth rates of several nonhuman primates, specifically Macaca

nemestrina and Papio cynocephalus, were investigated to see if there were any

differences between the two genera (Swindler and Sirianni 1973). Although the absolute

size of these primates is different, the growth of the palate occurred at similar rates with

both gradually decelerating with age. The deceleration of the growth rate is also

characteristic of humans. Another significant finding from this study is that no sexual

dimorphism exists in the rate of growth of the palate within either species (Swindler and

Sirianni 1973).

As previously noted, both the mid-palatal and transverse palatine sutures play a

role in the growth of the palate. In the embryonic stage, the incisive suture separates the

premaxilla and the maxilla, but this suture fuses before birth; although a slight visible









suture line may appear on the lingual surface of the palate and persist into adulthood

(Mann et al. 1987). The mid-palatal and transverse palatine sutures fuse erratically, but

they remain open well into adulthood. The morphology of these two sutures changes

throughout the different stages of palatal growth. The transverse suture begins broad and

slightly sinuous at birth and later develops into a typical squamous suture (Melsen 1975).

The mid-palatal suture progresses through three stages; in the first stage the suture is

short, broad, and Y-shaped, with the vomerine bone in the groove of the Y between the

two maxilla halves; in the second stage the suture is more sinuous; and in the third stage

the suture is heavily interdigitated (Melsen 1975). The change in sutural morphology

may be attributed to changes in the mechanical environment. Sutural biology, function,

and morphology will be explored further as well as how sutures are affected by loads.














CHAPTER 3
SUTURES

Functions of Sutures

Sutures are any articulation between dermal bones of the skull (Herring 2000).

These articulations are usually fibrous but sometimes contain cartilage or fibrocartilage.

Evolutionarily, the earliest sutures developed in the armored jawless fish and consisted

simply of the skin that remained between the dermal plates. The properties that are

typically associated with sutures, mobility, growth, and the potential for synostosis

(closure), were already present in these armored jawless fish (Herring 2000). Mammals

show no evolutionary progression of sutures; in fact, they have lost some of the sutural

diversity. All taxonomic groups that have sutures show a complete range of sutural

morphology, from loose connective tissue to elaborate interdigitations joined by a well-

defined ligament (Herring 2000).

Three main biological functions are associated with sutures: to unite bones while

still allowing slight movement, to act as growth areas, and to absorb mechanical stress

(Persson 1995, Cohen Jr. 2000). Two types of movements typically take place at the

sutures. At birth is when the first type of movement occurs, which entails the

displacement of the calvaria bones as the human head is compressed through the birth

canal (Persson 1995). This causes a molding of the head that resolves during the first

week of life through cranial re-expansion and widening of the sutural areas (Cohen Jr.

2000). The other type of movement at the sutures is caused by the displacement of bones

relative to one another as the skull grows (Persson 1995).









As previously mentioned, the amount of growth that occurs at the sutures is

debated, but there is no doubt that sutures do play a role in craniofacial growth. Sarnat

(2003) conducted experiments on macaque monkeys that involved surgically producing

clefts of the palate on one side only. The severity in the clefts varied from a narrow slit

to almost the entire half of the palate excised. No significant differences were noted in

the growth and development of the hard palate or maxillary arch between the operated

and unoperated sides or between the experimental (operated) and control (not operated)

macaques. Sarnat (2003) postulated two possible conclusions; either the transverse

palatine and mid-palatal sutures do not make a primary contribution to growth or other

areas of growth compensated for the altered condition. From this particular experiment

there is no way to decide which conclusion is correct, but other researchers have

postulated that the palatal sutures only secondarily contribute to growth (Melsen 1975).

Not only does the same suture grow differentially at various times, but the rate and the

amount of growth varies for different sutures at different times (Persson 1970, Sarnat

2003). The problem with intervention studies is that they create a situation that will

never be found in nature, so the results cannot be applied to animals in nature.

Persson (1970) conducted a study on the postnatal growth of facial sutures in the

rat that revealed different growth patterns in individual sutures as well as in the bony

margins of the same suture. Four different growth patterns were observed. The first

pattern was appositional growth against both sutural margins, which was observed in the

premaxillary part of the mid-palatal suture. Another type of pattern observed was

appositional growth against only one sutural margin while the other remained inactive.

This pattern was found in the main part of the naso-premaxillary suture. The palato-









maxillary suture showed appositional growth against one sutural margin, while the other

margin showed resorption. This contradicts Sarnat (2003) who states that sutural growth

is only through apposition with no resorption involved. The final growth pattern

observed by Persson (1970) is perichondral growth in the maxillary part of the mid-

palatal suture. This suture is an example of cartilage being present in the articulation as

opposed to just collagenous fibers (Herring 2000).

Mechanical environment also affects sutural growth and development. Mao

(2002) concluded that sutural growth is accelerated when exposed to tension and

compression. Another potential stimulus for sutural growth is the oscillatory component

of cyclic force. Kopher and Mao (2003) demonstrated that small doses of oscillatory

mechanical stimuli can affect sutural growth by either accelerating osteogenesis of the

suture or initiating net sutural bone resorption. This information can potentially affect

therapeutic goals in craniofacial disorders.

The third biological function of sutures is that they act either as a shock absorber

for mechanical stress or to transmit force across the sutures (Herring 1972, Persson

1995). The majority of mechanical stress in the suture areas is associated with

mastication (Persson 1995). Sutural morphology has been postulated to reflect the

loading environment under which the suture is subjected (Herring 1972, Wagemans et al.

1988, Herring and Teng 2000). Whether or not this is true will be explored in the

following sections.

Sutural Biology and Morphology

Pritchard et al. (1956) outlined the development of cranial and facial sutures based

on six different species: humans, sheep, pigs, cats, rabbits and rats. At all stages of

development, sutures exhibit five intervening layers as well as two uniting layers between









the adjoining bones. The five intervening layers consist of a pair of cambial layers, a pair

of periosteal fibrous capsular layers, and a middle looser layer of cellular mesenchymal

tissue. The cambial layers are the sites of active osteogenesis producing woven bone, but

the capsular layers must also expand in order to keep pace with the growing bone. The

two uniting layers occur when the fibrous capsules are joined by means of two fibrous

laminae, an external and an internal. The extremities of the fibrous capsules retain their

separate identities due to the intervening layer of loose mesenchymal tissue.

The facial and cranial sutures have the same structure, but they arise somewhat

differently. Before the sutures are formed in the face, the cambial and capsular layers are

already present with the middle and uniting layers being derived from the mesenchyme

between the approaching bone territories. The bones in the cranial vault approach each

other within an already differentiated fibrous membrane referred to as the ectomeninx.

The capsular layers do not form in the cranium until the cambial layers have almost met

and the middle and uniting layers are derived from the delamination of the ectomeninx

between the bones (Pritchard et al. 1956).

The histological structure of sutures, however, is not agreed upon. Pirelli et al.

(1999) conducted a study using biopsy samples of the mid-palatal suture obtained from

patients ranging in age from 10 years old to 30 years old. They reported that the capsular

and cambial layers reported by Pritchard et al. (1956) were not detected in any of their

samples nor were the cells typically associated with these layers, osteoblasts and

osteoclasts. The absence of osteoblasts and osteoclasts suggest that the bone was in a

resting period at the time of the sample. Unlike the woven bone detected by Pritchard et

al. (1956), Pirelli et al. (1999) stated that all the sutures were formed by lamellar and









bundle bone. Bundle bone is the term used to describe bone in the suture that closely

resembles the alveolar bone lining the periodontal ligament with a high turnover rate

(Pirelli et al. 1999). Although the functional significance of the lamellar bone in the

sutures is unclear, Pirelli et al. (1999) stated that the lamellar bone may possibly

progressively replace the bundle bone when the suture is no longer active in growth and

remodeling. If this is the case, the lamellar bone may represent the structural basis of the

physiological process of synostosis (Pirelli et al. 1999). The discrepancies in the sutural

structures between Pritchard et al. (1956) and Pirelli et al. (1999) may be attributed to the

differences in the ages of the samples examined.

The functional significance of the presence of cartilage in some of the postnatal

sutures is heavily debated. The cartilage is only present for a limited time and usually

only appears in the midline sutures, i.e. the sagittal and mid-palatal sutures. The function

of this cartilage seems to be linked to changes in the mechanical environment

(Wagemans et al. 1988). Sutures are normally under tension, but during growth the

sutures may be exposed to particularly strong pressure and shearing stresses (Pritchard et

al. 1956). The secondary cartilage that is present in these sutures is mainly found in

rapidly growing areas (Perssons 1995). Pritchard et al. (1956) recommends that the

effect of masticatory forces should be considered in relation to the development of

sutures.

The morphology of sutures is not only different between sutures, but the

morphology of a single suture can vary throughout its life. Melsen (1975) identified

three morphological stages in the development of the mid-palatal suture: Y-shaped,

slightly sinuous at birth, and interdigitated at puberty. Del Santo Jr. et al. (1998)









conducted a study of the morphological aspects of the mid-palatal suture in the human

fetus that partially confirmed the changes in morphology described by Melsen (1975).

The first group of fetuses (16-23 weeks) in this study showed a mid-palatal suture that

was rectilinear in nature with a wide zone of intense cellular proliferation. The second

(24-31 weeks) and third groups (32-39 weeks) displayed a sinuous form with a narrower

cellular proliferation zone.

The complex morphology of sutures is thought to reflect their functional

environment (Rafferty and Herring 1999). Oudhof (1982) found that although sutural

tissue has hereditary characteristics that determine the specific differentiation, certain

environmental influences are necessary for the manifestation and development of

qualities associated with sutures. For example, in the transplantation experiments

conducted by Oudhof (1982), when a portion of a suture was relocated to an area of little

or unspecified growth, the suture gradually lost its specific structure. On the other hand,

when a suture was transplanted to an area of active growth, the suture adapts to its

surroundings. This was witnessed when a portion of the sagittal suture of a rat was

transplanted into a coronal suture. The sagittal suture adapted by developing a more

intensive formation of fibers and more and longer lingulae (Oudhof 1982). The influence

of the mechanical environment on sutures will be the next topic covered.

Sutures and Loads

Suture morphology is extremely complex and several researchers have postulated

that the mechanical environment is one factor that influences their morphology (Linge

1970, Herring 1972, Oudhof 1982, Wagemans et al. 1988, Herring and Teng 2000, Mao

2002). Herring (1972) examined sutural morphology in suoids to explore the use of

cranial sutures as indicators for the amount and direction of stress in the skull. She









assessed sutural morphology in two ways: first she examined disarticulated sutural

surfaces for six specimens, second she examined dried articulated suoid skulls and

subjectively categorized them as straight, slightly interdigitated, interdigitated, and very

interdigitated. Another way to classify sutures is as either beveled or butt-ended.

One tentative conclusion that Herring (1972) drew from this research was that the

beveling of sutures may allow adjustive movements or stress reductions during forceful

operations, like rooting in pigs. Another conclusion was that interdigitations are

instrumental in the transmission of force from one bone to another and to resist shear

loads. Generally speaking, the interdigitations of the sutures will be either perpendicular

or parallel to the main force applied and these interdigitations serve to increase the

surface area for collagen fibers to attach (Herring 1972, Jaslow 1990, Rafferty and

Herring 1999). Jaslow (1990) examined the mechanical properties of sutures and

concluded that increased interdigitations do improve the bending strength when sutures

are loaded slowly when compared to cranial bone alone.

Jaslow (1990) was also able to provide support for the hypothesis that sutures act

as shock absorbers in the skull. This is based on the discovery that cranial bone with a

suture present was able to absorb more energy, regardless of the sutural morphology, than

the pure cranial bone. The sutural morphology also influences the amount of energy

absorbed. Energy absorption increased as the complexity of sutural interdigitation

increased. Interdigitation also seems to be correlated with the degree of compressive

strain. The more compressive strain a suture is exposed to, the higher the degree of

interdigitation (Rafferty and Herring 1999). Adjacent sutures also seem to experience

large magnitude strains of opposite polarity during normal mastication, at least in pigs






29


(Rafferty and Herring 1999). This result is intuitive because when one side of a structure

is experiencing tension, the other side is experiencing compression.

The cranium is a difficult bone to model because of its unusual morphology. The

palate in general provides special difficulties because the structure is curved which makes

techniques such as strain gages difficult to use. Since the loading environment influences

craniofacial growth and development, determining the loading environment of bones

such as the maxilla is important.














CHAPTER 4
ECOLOGY AND DIET OF COLOBUS MONKEYS

Background Information

Historically, researchers have classified colobus monkeys as specialists, based on

the amount of leaves in their diets. The origin of this belief seems to stem from an early

paper by Booth (1956) that refers to colobus monkeys as 'purely leaf-eating.' Casual

observations and the study of the contents of the stomach formed the basis of this

assumption. Anatomical features such as the large complex stomach and high-crowned

molars and premolars also support the notion that colobus monkeys are largely leaf-eaters

(Campbell and Loy 2000). Recent evidence, however, suggests that this initial view of

colobines is not accurate, at least not for all species and/or groups (Maisels et al. 1994).

Leaves do make up a large portion of most, if not all, colobus monkey diets, but seeds,

fruits, and flowers also contribute significantly to their diets. The original belief that

colobines were specialists was based on studies conducted on groups of colobines in east

Africa (Dasilva 1994). Research at sites such as Tiwai Island in western Africa has

shown that seasonal variability exists in their diets, including seeds, fruits, and both

young and mature leaves (Dasilva 1994, Davies et al. 1999).

Feeding techniques do not vary much between different species of colobines. The

type of food eaten affects the technique used, but regardless of the food type, there is very

little manual manipulation involved (Clutton-Brock 1975). Colobus monkeys have

reduced thumbs, which may explain the little amount of manipulation. This appendage

does not provide them with the grip of other primates who have larger thumbs that allow









more precise gripping. Clutton-Brock (1975) did observe some manipulation, though,

such as stripping the pinnules off of the leaf stem by gripping the stem in their teeth and

dragging the stem through their clenched fists. He states that he never saw them use their

hands to strip or break open fruit; if the covering was removed from a fruit they opted to

use their teeth instead (Clutton-Brock 1975).

One difference between red colobus (Procolobus badius) and king colobus

(Colobuspolykomos) is their preference for location of feeding. The former usually

acquires a large portion of their food from some of the largest trees in the upper canopy

of their habitat, while the latter choose to forage lower in the canopy (Oates 1994). In

areas where both of these colobine groups co-occur, the red colobus monkeys choose a

more diverse diet than the king colobus. Another difference is the amount of seeds that

are consumed. All colobus species ingest seeds, but only in the black and white forms do

seeds sometimes dominate the diet (Oates 1994). Some researchers argue that African

colobines eat a large portion of seeds whenever the quality of the tree foliage is poor via

poor soils (Maisels et al. 1994). Evidence supports this statement for some areas such as

Zaire (Maisels et al. 1994), but this explanation does not explain the difference in seed

exploitation between sympatric species of colobus monkeys.

Study Sample

The colobus monkeys used in this study are Procolobus badius (n=39) and Colobus

polykomos (n=13) from the Tai Forest of Cote d'Ivoire. They are sympatric throughout

most of their range and are similar in body size and diets except the king colobus exploits

a particularly hard seed from the African oil bean (Pentaclethra macrophylla,

Mimosaceae) at a much larger frequency than the red colobus monkeys.









This African oil bean tree is usually 21 m in height with a girth of about 60 cm.

The pods are 40-50 cm long and usually 5-10 cm wide. Inside the pods are 6-10 flat

glossy brown seeds that are up to 7 cm long. Colobuspolykomos focuses on seeds from

this plant and others like it whereas Procolobus badius focuses on leaf eating (Davies et

al 1999). The reason for this difference probably stems from their individual preference

in foraging, i.e. upper versus lower canopy.

When the king colobus preys on these hard seeds, they expend a great amount of

effort gnawing them until they break through the encasing (Davies et al. 1999). As

mentioned earlier, Daegling and McGraw (2001) predicted that the species exploiting the

hard seeds should have a more robust mandibular corpus than the species that does not

exploit this food item. This prediction is based on the reasoning that the king colobus

would have to apply larger loads, therefore stressing the mandible more, to gnaw through

the tough encasements. The results of the study, however, showed that the variation in

mandibular morphology in these two sympatric colobines does not correspond to the

predictions based on the dietary differences (Daegling and McGraw 2001).

The underlying reasoning behind the current project is that the palates of these two

species of colobus monkeys are exposed to different loading environments. The

extensive gnawing of Colobuspolykomos on the hard seeds may cause a significantly

larger amount of force on the palate. If this is the case, the complexity of the palatal

sutures of these two species may reflect this difference in loading environment. In order

to test this hypothesis, fractal analysis was completed on the mid-palatal sutures of

Colobus polykomos and Procolobus badius.














CHAPTER 5
FRACTAL ANALYSIS

One of the most difficult tasks facing morphologists is that of quantifying and

measuring size and shape. Traditionally, parameters such as length and volume were

used to try to quantitatively describe and compare morphological characteristics. In

Euclidean geometry linear measures are considered one dimension, smooth surfaces are

two dimensions, and volumes and weights are three dimensions. Objects that occur in

nature, however, seldom have edges that are straight or surfaces that are smooth (Long

1985). Some objects in nature possess certain qualities that can be described by a non-

Euclidean fractional dimension, which lies between the values of one and two

(Mandelbrot 1977). These objects are known as fractals. Fractals are geometric objects

that are self-similar in nature. Self-similarity means that the fractal object is composed of

smaller units that possess the same shape as the whole object. Fractals have complex

edges or surfaces that increase linearly as the resolution of the units used to measure them

increase (Hartwig 1991). Fractal analysis is a technique used to interpret the geometric

complexities of fractals.

Several researchers believe some cranial sutures are fractal objects (Long 1985,

Hartwig 1991, Long and Long 1992, Gibert and Palmqvist 1995, Montiero and Lessa

2000, Yu et al. 2003). Long (1985) explored the idea of whether or not complex sutures

exhibit fractal properties such as self-similarity and a dimension between one and two.

To address this question, Long (1985) examined the sutures on the shells of extinct

ammonites and cranial sutures of white-tailed deer. The sutures in both of these









organisms are incredibly complex and did exhibit fractal properties. Other cranial sutures

that have been examined using fractal analysis are the sagittal suture in humans (Hartwig

1991, Yu et al. 2003), the sagittal and lambdoidal sutures in humans (Long and Long

1992, Gibert and Palmqvist 1995), and cranial sutures in the genus Caiman (Montiero

and Lessa 2000). In each of these studies, the structures under examination exhibited the

characteristics of fractals.

In this study, fractal analysis was conducted with the use of a software program

known as Benoit 1.3 (St. Petersburg, FL). This program allows the user to choose from

several different methods on how the fractal analysis is conducted. The different

methods provided in this program are tailored to accommodate different types of data

sets. Based on this data set, three methods seemed equally applicable. Each of these is

discussed in further detail.

Box Dimension and Information Dimension Methods

The box dimension method of fractal analysis is one of the most widely used

methods due to the relatively simple mathematics involved (Falconer 1990). In Benoit

1.3, the box dimension is defined as the exponent Db in the relationship:

1
N(d) -I
dDb

where N(d) is the number of boxes of linear size d necessary to cover a data set of points

distributed in a two-dimensional plane. A number of boxes are used to cover the data set

points that are evenly distributed on a plane. This may indicate that point density may

influence the results, i.e. the number of data points collected will affect the outcome of

the fractal dimension. This method is often referred to as the grid dimension because the

boxes used are usually part of a grid system.









To accomplish this method, a series of different box sizes d are laid over the

object and the program works by tallying the number of boxes filled during each box size

overlay. One of the problems with this method is that the boxes are weighted the same

whether the entire box is full or just a tiny portion. The information dimension method

addresses this problem by assigning weights to the boxes so boxes containing more

points are counted more than the boxes with fewer points (Benoit 1.3). Unfortunately

this makes the mathematics involved much more complicated.

Ruler Dimension

Mandelbrot (1977) examined the coastline of Britain and determined that this

object was fractal. How was the fractal dimension of this jagged, self-similar line

calculated? The method he used is now referred to as the ruler, or yardstick, method.

The ruler method Dr is defined as:

N(d) & d Dr

where N(d) represents the number of steps taken to walk a divider (or ruler) that is length

d. According to Benoit 1.3, the formal equivalence between this method and the box

dimension can be shown mathematically. Algebraically, this claim is logical, since the

box dimension is simply the reciprocal of the ruler dimension.














CHAPTER 6
MATERIALS AND METHODS

The skulls of 39 Procolobus badius and 13 Colobuspolykomos were examined

from a collection housed at Ohio State University. Eight measurements were also taken

from each skull: palate height, internal palate breadth, external palate breadth, palate

length, palate depth, upper facial height, facial width, and skull length. With the

exception of palate depth and palate height, the measurements are defined in Bass (1995).

Table 1 provides a brief definition of the six measurements taken from Bass (1995).

Palate depth was measured using an instrument colloquially referred to as a carpenter's

tool or a contouring tool. The contour was traced from the edge of the alveolar ridge of

the second molar to the level of the mid-palatal suture. The height of the contoured

tracings was then measured resulting in the depth of the palate. Palate height was

measured with sliding calipers by placing one edge of the caliper on the mid-palatal

suture and one edge on the alveolar ridge at the level of the second molar.

Table 1. Definitions of measurements collected.
Measurement Definition (Craniometric Points*)
Facial width zygion to zygion
External palate breadth ectomolare to ectomolare
Internal palate breadth endomolare to endomolare
Palate length prosthion to alveolon
Skull length alveolare to opisthocranion
Upper facial height nasion to alveolare
*Craniometric points defined in Bass (1995)

In addition to the measurements taken, the palate of each specimen was

photographed using a Minolta 35mm camera with a macro lens attached. Each specimen

was oriented with the palate parallel to the lens of the camera. The film was developed









and the negatives were made into 35 mm slides. These slides were then scanned into the

computer and saved as bitmap images. Each image was imported into SigmaScan where

the mid-palatal suture of each specimen was digitized. The x-y coordinates were

imported into SigmaPlot and subsequently graphed using a single spline curve. The

spline curve option was chosen over the single straight line option because this

represented a more accurate depiction of the sutures. The reason this has to be done is to

override the automated scaling function of SigmaPlot. The scale of the graphs were

changed so equal units were represented on the x and y axes. The image was then

inverted from black on white to white on black. This was done because Benoit 1.3

software recognizes white points as data points and the black points as the background.

The images were converted to bitmap files and imported into Benoit 1.3 for the

fractal analysis. After exploring the different methods available through the software, the

two methods chosen were the information dimension and ruler dimension. The

information dimension was chosen over the box dimension because the boxes are

weighted and therefore provide a more accurate fractal dimension than the box

dimension. There was not, however, an obvious advantage of either the information

dimension or ruler dimension over the other, so both were used to calculate the fractal

dimensions of the colobine mid-palatal sutures. Other researchers have chosen one of the

methods over the other but the reasoning behind their choice is often not made clear,

although the researchers who chose the ruler dimension often state that they use this

method because Mandelbrot (1977) used this method when examining the coastline of

Britain.









Once the fractal dimensions were obtained, several statistical procedures were

conducted. A 2-way ANOVA was run separating the sexes and species which resulted in

four groups. Regressions were also conducted between the fractal dimensions and each

size/shape variable to try to determine if there was a predictable relationship between any

of these variables. The regressions were conducted with only the species separated not

the sexes. Both of these procedures were evaluated for significance based on a P-

value<0.05. The fractal dimension data for the four groups was also bootstrapped to

obtain a more reliable mean since the sample sizes were small. Bootstrapping makes no

assumptions about the distributional properties of the data.














CHAPTER 7
RESULTS

Including both fractal dimensions, ten variables were examined. Basic statistics

were computed for each variable independently (Tables 2 and 3). The parametric

medians for each group are graphically represented for both fractal dimensions in Figures

2 and 3. Since the samples sizes for these groups are small, the data was bootstrapped for

1000 iterations to try to obtain more reliable means and standard errors, since no

assumption is made regarding the distribution of the data. As shown in Tables 4 and 5,

there was little difference between the parametric mean and the bootstrapped mean.

The ruler and information fractal dimensions for each species were regressed

against each of the measured size/shape variables. Out of the 32 regressions performed,

only three resulted in significant P-values, i.e. P-values less than .05. However, the

coefficient of determination (r-squared) was very weak for these three regressions,

ranging from 12.1% to 37.2% (Table 6).

Tables 7 and 8 report the ruler and information fractal dimensions calculated for

both species. One interesting (and seemingly impossible) aspect of two of these fractal

dimensions is that they are below 1.0. Note in Table 3, Procolobus badius specimen

number 2107 (Figure 4) has a ruler fractal dimension of 0.99209 and P. badius specimen

number 9433 (Figure 5) has a ruler fractal dimension of 0.98466. However, their

information fractal dimensions are both above












Table 2. Basic statistics for variables associated with Colobus polykomos
Variable N Mean Median StDev SE Mean Minimum Maximum Q1 Q3

Ruler Fractal 13 1.1880 1.1903 0.0599 0.0166 1.0795 1.2836 1.1416 1.2341
Dimension
Information 13 1.0994 1.1018 0.0404 0.0112 1.0268 1.1659 1.0781 1.1247
Fractal
Dimension
Palate Height 13 12.550 12.500 1.268 0.352 10.400 14.800 11.495 13.680
Internal Palate 13 18.472 19.400 2.513 0.697 12.100 20.700 17.120 20.045
Breadth
External Palate 13 36.278 36.800 1.906 0.529 32.200 38.800 35.310 37.450
Breadth
Palate Length 13 44.138 44.600 2.992 0.830 36.600 48.200 42.800 45.990
Palate Depth 13 6.808 7.000 1.032 0.286 5.000 8.000 6.000 8.000
Upper Facial 13 40.124 40.200 3.350 0.929 34.200 46.410 38.700 42.000
Height
Facial Width 13 75.91 74.00 5.53 1.53 67.90 83.60 71.75 81.25
Skull Length 13 108.96 108.00 4.01 1.11 103.00 115.70 106.05 112.65












Table 3. Basic statistics for variables associated with Procolobus badius
Variable N Mean Median StDev SE Mean Minimum Maximum Q1 Q3
Ruler Fractal 39 1.1355 1.1093 0.0983 0.0157 0.9847 1.3455 1.0615 1.2121
Dimension
Information 39 1.1085 1.1058 0.0276 0.0044 1.0643 1.1676 1.0883 1.1310
Fractal
Dimension
Palate Height 39 10.086 9.970 1.181 0.189 6.830 12.130 9.470 10.870
Internal Palate 39 16.347 16.460 1.554 0.249 12.180 18.740 15.380 17.370
Breadth
External Palate 39 32.081 32.030 1.441 0.231 29.280 35.040 30.910 33.000
Breadth
Palate Length 38 39.170 39.085 2.035 0.330 35.340 43.570 37.615 41.030
Palate Depth 39 6.122 6.000 1.305 0.209 3.000 8.500 5.000 7.000
Upper Facial 39 40.784 41.150 2.743 0.439 34.010 44.990 38.900 42.910
Height
Facial Width 37 77.686 78.510 5.002 0.822 68.110 86.750 73.725 81.975
Skull Length 36 101.46 101.90 3.56 0.59 93.54 109.27 99.69 103.71

















P. badius females


P. badius males


C. polykomos females


C. polykomos males


1.0 1.1 1.2 1.3
Ruler Fractal Dimension

Figure 2. Box plot of median values for the ruler fractal dimensions.


P. badius females -



P. badius males -



C polykomos females -


C polykomos males -


1.00 1.05 1.10 1.15 1
Information Fractal Dimension

Figure 3. Box plot of median values for the information fractal dimensions.


~-U 1H


-#


**
--!









Table 4. Bootstrapped versus parametric means for ruler fractal dimension
Species Sex N Bootstrap Bootstrap Parametric Parametric
Mean for Standard Error Mean Standard
1000 samples Error
Colobus Male 4 1.1365 0.0200 1.1500 0.0244
polykomos
Colobus Female 9 1.1953 0.0172 1.2049 0.0195
polykomos
Procolobus Male 23 1.1295 0.0178 1.1380 0.0194
badius
Procolobus Female 16 1.1230 0.0230 1.1362 0.0274
badius

Table 5. Boostrapped versus parametric means for information fractal dimension
Species Sex N Bootstrap Bootstrap Parametric Parametric
Mean for Standard Error Mean Standard
1000 Samples Error
Colobus Male 4 1.0748 0.0145 1.0817 0.0163
polykomos
Colobus Female 9 1.1000 0.0118 1.1072 0.0143
polykomos
Procolobus Male 23 1.1078 0.0056 1.1107 0.0062
badius
Procolobus Female 16 1.1030 0.0061 1.1070 0.0071
badius

Table 6. Significant regressions
Species Variables N Slope Y- r r-squared
Regressed intercept (%)
Procolobus Ruler vs Palate 39 0.0289 0.844 .35 12.1
badius Height
Procolobus Ruler vs Palate 39 0.0289 0.959 .38 14.7
badius Depth ________
Colobus Information vs 13 0.3100 0.624 .61 37.2
Polykomos Facial Width

According to Benoit 1.3 software, the ruler and information fractal dimensions are

equivalent. If this is true, then a simple regression of these two dimensions should show

a linear relationship. As Figure 6 shows, this is not the case. In fact, there is no

discernible pattern whatsoever in this graph and the r-squared value is 0.0402. Another

indication that these methods for determining fractal dimensions are not equivalent is that









Table 7. Fractal dimensions of Colobus polykomos
Specimen Sex Ruler Fractal Information Fractal
Designation Dimension Dimension
2100 Male 1.07953 1.03320
2216 Male 1.19034 1.09408
2311 Male 1.15727 1.10373
9418 Male 1.17273 1.09593
2102 Female 1.28359 1.08546
2103 Female 1.24256 1.02679
2119 Female 1.22849 1.10182
2123 Female 1.23009 1.13283
2124 Female 1.11034 1.11666
2238 Female 1.14829 1.15345
2245 Female 1.13496 1.16592
2314 Female 1.22786 1.07076
9426 Female 1.23806 1.11099


the specimens exhibiting the highest and lowest fractal dimension values differ between

these two methods. The highest ruler fractal dimension is 1.34546 (Procolobus badius

227, Figure 7) while the highest information fractal dimension is 1.16761 (Procolobus

badius 942, Figure 8). The lowest ruler fractal dimension is 0.98466 (Procolobus badius

9433, Figure 5) while the lowest information fractal dimension is 1.02679 (Colobus

polykomos 2103, Figure 9).

Regardless of which fractal dimension is used, a pure model II 2-way ANOVA

showed that no significant differences exist in the fractal dimensions between species or

sexes. There is also no interaction effect between species and sex. A pure model II was

chosen because there were no fixed treatment effects but rather only random effects

(Sokal and Rohlf 1981).









Table 8. Fractal dimensions of Procolobus badius
Specimen Sex Ruler Fractal Information Fractal
Designation Dimension Dimension
2027 Male 1.04962 1.08833
2028 Male 1.29563 1.10579
2118 Male 1.06146 1.14878
2125 Male 1.12647 1.11583
2126 Male 1.30574 1.11583
2013 Male 1.15642 1.11931
2022 Male 1.07645 1.08920
2104 Male 1.13798 1.09966
2105 Male 1.07308 1.09533
2110 Male 1.24166 1.11158
2113 Male 1.23780 1.15081
222 Male 1.13614 1.14766
2231 Male 1.00705 1.10777
224 Male 1.11669 1.11242
2243 Male 1.22389 1.06426
2255 Male 1.07371 1.08930
232 Male 1.10572 1.08667
233 Male 1.06071 1.08017
235 Male 1.07599 1.09189
239 Male 1.14051 1.12176
9413 Male 1.05565 1.11252
942 Male 1.02873 1.16761
945 Male 1.31662 1.06753
2005 Female 1.05978 1.09521
2032 Female 1.09483 1.10217
223 Female 1.30888 1.13372
227 Female 1.34546 1.07348
2014 Female 1.11507 1.16151
2107 Female 0.99209 1.13472
2112 Female 1.09099 1.09856
2215 Female 1.10713 1.11771
2219 Female 1.14706 1.14561
2220 Female 1.10925 1.11490
2240 Female 1.29973 1.07179
2313 Female 1.20520 1.07042
236 Female 1.21207 1.08017
9422 Female 1.07231 1.13104
9433 Female 0.98466 1.08724
972 Female 1.03491 1.09268























































Figure 4. Mid-palatal suture of Procolobus badius specimen 2107 with a ruler fractal
dimension of 0.99209 and information fractal dimension of 1.13472. The
suture is oriented with the anterior portion at the top of the page.

























































Figure 5. Mid-palatal suture ofProcolobus badius 9433 with a ruler fractal dimension
0.98466 and information fractal dimension of 1.08724. The suture is oriented
with the anterior portion at the top of the page.







48





1.4

*

1.3 -* .



1.2






*
*
1.0 -



0.9 -...... .
1.00 1.02 1.04 1.06 1.08 1.10 1.12 1.14 1.16 1.18
Information Fractal Dimension


Figure 6. Regression of ruler fractal dimension vs information fractal dimension.























































Figure 7. Mid-palatal suture ofProcolobus badius specimen 227 with a ruler fractal
dimension of 1.34546 and information fractal dimension of 1.07348. The
suture is oriented with the anterior portion at the top of the page.























































Figure 8. Mid-palatal suture of Procolobus badius specimen 942 with a ruler fractal
dimension of 1.02873 and information fractal dimension of 1.16761. The
suture is oriented with the anterior portion at the top of the page.




















































Figure 9. Mid-palatal suture of Colobus polykomos specimen 2103 with a ruler fractal
dimension of 1.24256 and information fractal dimension of 1.02679. The
suture is oriented with the anterior portion at the top of the page.














CHAPTER 8
DISCUSSION

The results of the 2-way ANOVA indicate that the hypothesis proposed for this

study, i.e. these two species would differ in mid-palatal suture complexity, is not

supported. The colobine monkeys used in this study only have one major difference in

their diets. Colobuspolykomos must gnaw through a tough pod in order to gain access to

a particular type of seed they eat. One possible explanation for why no significant

differences were found is that the seeds do not make up a large enough portion of their

diets to have an effect on the sutural complexity. In other words, seed-eating is dominant

in both of these colobine monkeys, but the actual proportion of Pentaclethra macrophylla

seeds to the Colobuspolykomos diets has never been identified (Davies et al. 1999). The

difference in masticatory loads between these two species may not be large enough to

elicit a morphological response from the mid-palatal suture.

The distribution of stress throughout the palate during mastication may also be a

contributing factor to the non-significant results reported here. Although numerous

studies exist that explore the loading environment during mastication in certain parts of

the face and cranium, few studies mention any stress the palate may receive during this

activity. Due to the morphological structure of the palate, mechanical modeling is

difficult. Although the palate probably experiences different types of stress such as

shearing forces, torsional moments, and bending moments (Preuschoft 1989), it is

possible that the stress level is not significant enough to elicit a response from the bone.

In order to figure out what the strains are, the maxilla needs to be explored









experimentally. As mentioned earlier, the issue becomes how to model the maxilla. One

possible reason the maxilla may experience small loads is the presence of the hard palate.

Unlike the mandible, the maxilla has the hard palate which may serve to eliminate or

greatly reduce twisting and bending (Daegling and Hylander 1997).

Measurements of different size/shape variables were also taken from each

specimen in order to determine whether or not a relationship exists between these

particular measurements and the fractal dimensions of the mid-palatal sutures. Only

three regressions showed significance, but the correlation values were very weak (Table

6). When these measurements were regressed against the ruler fractal dimension, palate

height and palate depth in Procolobus badius showed significance. Interestingly there

were no significant regressions in Colobuspolykomos for the ruler fractal dimension.

However, the opposite is true for the information fractal dimension. No significant

results were found for Procolobus badius, but the regression of information fractal

dimension versus facial width in Colobuspolykomos showed significance. The fact that

the so-called equivalent fractal dimensions yield different significance is further

evidence that these are not equivalent measures. More than likely the significant P-

values for these three regressions reflect a type I error instead of real significance,

although there is no way to truly know if a type I error was committed. The results of the

regressions suggest that there is no predictable pattern between either of the fractal

dimensions and any of the size/shape variables.

One problem limiting interpretation was small sample sizes. When dealing with

biological samples, obtaining sufficiently large sample sizes can be a problem. An

attempt to deal with this problem was made by bootstrapping the data. However, as









previously mentioned, the bootstrapped means were very similar to the parametric means

calculated from the raw data, which suggests that the variation captured in this study is

probably a fairly accurate representation of the populations in question.

Another issue arising in this study may stem from the methodology used. Fractal

analysis has become a popular method for quantifying the complexity of intricate cranial

sutures. Long (1985) published one of the earliest works on fractals in biology when he

examined the sutures present on the shells of ammonites and the cranial sutures of

antlered deer. This study was also the first to describe how fractal elaboration is

important in the evolutionary process. Long and Long (1992), however, criticize the use

of fractal analysis on human cranial sutures because they feel that these particular sutures

are not self-similar and therefore are not fractals even though they yield a dimension

between 1 and 2. They state that some waveform curves may yield a dimension up to

1.2, but this is not sufficient to classify them as fractals. Using this reasoning, Long and

Long would probably say the sutures presented in this paper are not fractals. If this is

true, then this could be an explanation for why the two fractal analysis methods used here

do not show equivalence.

The problem with the above supposition is that these sutures do fit the definition of

a fractal, i.e. they are self-similar and have a dimension between 1 and 2. The main

critique of Long and Long (1992) is that the waveforms that possess a dimension above 1

are not self-similar. Studies conducted on human cranial sutures using the box dimension

have shown that human cranial sutures are self-similar through the use of logarithmic

plots. These graphs show the relationship of the logarithms of the number of squares

with length r occupied by the suture against the logarithm of 1/r. Benoit 1.3 provided the









logarithmic graphs for each suture analyzed in both of the methods and all of them

clearly showed a linear relationship. This suggests that these sutures are self-similar and

therefore, by definition, are fractal.

Unfortunately this still leaves the problem of trying to provide an explanation for

why the ruler and information fractal dimensions are not demonstrating equivalence like

they should. One possibility is that due to the complicated mathematics that are

introduced into the information dimension in order to weight the boxes, the equivalence

that exists between the box and ruler dimension is lost. To test this theory, fractal

analysis was conducted again on the same sutures using the box dimension (Tables 9 and

10). A simple regression was conducted and as Figure 9 demonstrates there is still no

linear relationship (r-squared 0.0804). This does not support the idea that the more in

depth mathematical calculations affected the equivalence. The reason for this may be

that the number of points collected could affect the outcome of the fractal dimension.

This implies that these different methods of fractal analysis are not measuring

complexity in the same fashion. Uncertainty exists as to which method is more

appropriate for analyzing human cranial and facial sutures, but one insight gained is that

these methods are not equivalent. This means more testing (e.g.) needs to be completed

in order to try to determine which method is more accurate. Besides the type of dataset

utilized, another factor that may affect which method is better is how the data is

collected. In other words, it may be that both methods are appropriate for analyzing

human sutures, but depending on the method used to extract the suture from the specimen

and manipulate it so it can be imported into this software, one method may prevail over









the other. Regardless of which method was used, no significant results were discovered

from this data.

Table 9. Box dimensions for Procolobus badius
Specimen Designation Sex Box Dimension
2027 Male 1.15339
2028 Male 1.11262
2118 Male 1.18019
2125 Male 1.14647
2126 Male 1.12777
2013 Male 1.12626
2022 Male 1.14486
2104 Male 1.11175
2105 Male 1.12366
2110 Male 1.09819
2113 Male 1.14137
222 Male 1.16990
2231 Male 1.12637
224 Male 1.12912
2243 Male 1.11433
2255 Male 1.12925
232 Male 1.12130
233 Male 1.11166
235 Male 1.12101
239 Male 1.15034
9413 Male 1.12463
942 Male 1.17601
945 Male 1.10132
2005 Female 1.11475
2032 Female 1.14087
223 Female 1.12508
227 Female 1.11091
2014 Female 1.17835
2107 Female 1.12846
2112 Female 1.11445
2215 Female 1.13767
2219 Female 1.14574
2220 Female 1.13643
2240 Female 1.11797
2313 Female 1.12303
236 Female 1.13915
9422 Female 1.12672
9433 Female 1.12309
972 Female 1.11693










Table 10. Box dimensions for Colobus polykomos
Specimen Designation Sex Box Dimension
2100 Male 1.12953
2216 Male 1.11993
2311 Male 1.10920
9418 Male 1.10893
2102 Female 1.10568
2103 Female 1.10836
2119 Female 1.13348
2123 Female 1.17746
2124 Female 1.12773
2238 Female 1.15679
2245 Female 1.17051
2314 Female 1.10595
9426 Female 1.13959


0.9 -
1.08


Box Fractal Dimension


Figure 10. Regression of ruler fractal dimension vs box fractal dimension.


0



* *


^^"-o~ *
** O
** -** -
*
*














CHAPTER 9
CONCLUSION

One of the proposed functions of cranial sutures is that they play a role in the

transmission and absorption of mechanical loads (Herring 1972). If this is true, it stands

to reason that the morphology of the sutures may reflect the loading environment to

which it is subjected (Rafferty and Herring 1999). Using this reasoning, the hypothesis

was made that the more complexity a suture exhibits, the higher amounts of stress it

experiences. One problem is how one quantitatively measures sutural complexity. One

method that has been applied to this problem over the past two decades is fractal analysis.

The fractal analysis conducted on the mid-palatal sutures of these two species of

colobus monkeys did not show a significant difference. Sex also did not have a

significant effect on the complexity of the mid-palatal sutures. Although this study does

not support the hypothesis that mechanical loading is at least partially responsible for the

morphological complexity of sutures, it by no means discredits this idea. The most

probable reason behind the lack of support is that the differences in the diet are not great

enough to cause significantly more stress in the palate of Colobuspolykomos. Another

aspect that should be examined in the future is the overall structure of the maxilla of these

two species. There may possibly be a larger concentration of bone between the point of

impact (the teeth) and the mid-palatal suture. If so, this bone may absorb the stress

before it reaches the suture. Unfortunately, at this point in time, this is pure speculation.

The suggestion has also been made that most cranial sutures are not intricate

enough to be fractals (Long and Long 1992), but as the term is currently defined human









cranial sutures are fractal objects. This leads to the question of which fractal analysis

technique is most appropriate for examining human cranial sutures. One conclusion that

must be drawn from this study is that the box (information) dimension and the ruler

dimension methods are not equivalent. So, which one provides a more accurate depiction

of the dimension of these structures? Unfortunately, more intensive investigation is

required in order to provide an answer for this question.

The complexity of these particular sutures did not differ significantly between these

species, but this does not mean that the loading environment has no effect on sutural

growth and morphology. Enough evidence exists to merit further exploration of this

topic. Mechanical environments do elicit morphological responses from bone throughout

all stages of life whether in modeling or remodeling. An important point to consider is

that sutural complexity may not only be influenced by mechanical factors. The sutures

serve other functions besides absorption and transmission of loads. These other

functions, such as growth, may also affect the complexity of the sutures. Although this is

possible, mechanical loading seems to be the most likely factor contributing to the

complex morphology of the suture. Many factors play a role in palate growth and

development; however, exploring the role of mechanical forces is essential to a

comprehensive understanding of this process.















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BIOGRAPHICAL SKETCH

Jennifer Hotzman is one of four children and was born in Meridian, Mississippi.

She received her Bachelor of Arts degree in anthropology from the University of

Southern Mississippi in 2000. After graduation she continued her education at the

University of Florida. While completing her graduate studies, Ms. Hotzman also worked

full-time for Regeneration Technologies, a company that manufactures allografts for

surgical procedures. After obtaining her Master of Arts degree, she plans on continuing

her graduate studies at the University of Florida.