1 the Oral Processing Behaviors of Mandrills (Mandrillus Sphinx)

The Oral Processing Behaviors of Mandrills (Mandrillus sphinx) in a Captive Setting

Thesis

Presented in Partial Fulfillment of the Requirements for the Degree Master of Arts in the

Graduate School of The Ohio State University

Joseph Geherty

Graduate Program in Anthropology

The Ohio State University

2019

Thesis Committee

W. Scott McGraw, Advisor

Dawn Kitchen

Jeffrey McKee

Copyrighted by

Joseph Geherty

2019

Abstract

Oral processing behaviors are known to co-vary with aspects of feeding ecology, food material properties, and cranio-dental anatomy. Previous field studies on terrestrial mangabeys (Cercocebus) have revealed important age/sex differences in the frequency of incision, isometric biting and chewing frequency related to diet. Here, I provide information on the Cercocebus sister taxon in order to better understand variation within this clade of African papionins. I examined oral processing behavior of captive mandrills

(Mandrillus sphinx) at the Columbus Zoo and tested the hypothesis that extreme sexual dimorphism in this species would result in significant age and sex differences in food processing behaviors. I used focal animal sampling on an adult male and female, and two sub-adult males to quantify ingestive and oral processing behaviors associated with different foods made available to the monkeys. Kruskal-Wallis tests were performed on a sample of over 1,100 ingestive events across subjects. Significance tests revealed a variety of age/sex differences in rates of incision or mastication when individuals consumed the same food items. There was lack of a uniformity in mandrill oral processing behavior. There were certain foods the adult male used more incision or mastication but other foods in which the other individuals used more oral processing.

Mandrill oral processing differs from sooty mangabey oral processing in which adult males had the highest number of incisions and mastications for hard object consumption

iii than adult females or subadults. It is concluded that the extreme degree of sexual dimorphism of mandrills places a biomechanical constraint on oral processing behavior leading to an absence of differences of across ages and sexes. This conclusion needs to be tested further with additional data on free-ranging mandrills.

Acknowledgments

I am extremely grateful to The Ohio State University for providing me with the opportunity to conduct this research project. I would like to express my appreciation to

Dr. W. Scott McGraw for introducing me to this project and helping me with my research and preparation of my thesis. I would also like to express my gratitude to Dr. Jeffrey

McKee and Dr. Dawn Kitchen for serving as my Ohio State University committee members and the support I received from them. Lastly, I would like to thank the

Columbus Zoo for allowing me the opportunity to study their mandrill group and for assisting me on my project.

Vita

2015………………………………………B.S. Anthropology, Biology, Psychology,

University of New Mexico

2016………………………………………Field Research Assistant, Universidad

Nacional Autónoma de México

2017 to present…………………………...Pursuing M.A. Anthropology, The Ohio State

University

Fields of Study

Major Field: Anthropology

Table of Contents

Abstract ...... iii Acknowledgments...... v Vita ...... vi List of Tables ...... viii List of Figures ...... ix Chapter 1. Introduction ...... 1 Cercocebus-Mandrillus relationship ...... 3 Cercocebus oral processing behaviors ...... 8 Mandrill diet...... 10 Captive mandrills as a comparison ...... 13 Research Questions ...... 13 Chapter 2. Methods ...... 15 Subjects ...... 15 Study site ...... 16 Behavioral sampling methods ...... 19 Data analysis ...... 22 Chapter 3. Results ...... 24 Diet ...... 24 Comparison across food types ...... 24 Comparison across age/sex class ...... 33 Chapter 4. Discussion ...... 39 General characteristics of mandrill processing activities...... 40 Oral processing across age/sex classes ...... 41 The role of sexual dimorphism ...... 42 Future directions ...... 45 Bibliography ...... 47

vii

List of Tables

Table 1. Diet Composition ...... 25 Table 2. P-values from Kruskal-Wallis tests that compare mean number of incisions for all eighteen foods: all individuals ...... 27 Table 3. P-values from Kruskal-Wallis tests that compare mean number of mastications for all foods: all individuals ...... 30 Table 4. P-values from Kruskal-Wallis comparisons of individuals for mature leaf incision ...... 35 Table 5. P-values from Kruskal-Wallis comparisons of individuals for lettuce incision. 35 Table 6. P-values from Kruskal-Wallis comparisons of individuals for stem incision. ... 35 Table 7. P-values from Kruskal-Wallis comparisons of individuals for grass incision.... 35 Table 8. P-values from Kruskal-Wallis comparisons of individuals for insect incision. . 35 Table 9. P-values from Kruskal-Wallis comparisons of individuals for ice cube incision...... 35 Table 10. P-values from Kruskal-Wallis comparisons of individuals for mature leaf mastication...... 37 Table 11. P-values from Kruskal-Wallis comparisons of individuals for lettuce mastication...... 37 Table 12. P-values from Kruskal-Wallis comparisons of individuals for stem mastication...... 37 Table 13. P-values from Kruskal-Wallis comparisons of individuals for grass mastication...... 37 Table 14. P-values from Kruskal-Wallis comparisons of individuals for insect mastication...... 37 Table 15. P-values from Kruskal-Wallis comparisons of individuals for ice cube mastication...... 37

viii

List of Figures

Figure 1. Cladograms depicting two possible organizations of Papionin ...... 4 Figure 2. Adult male and female size comparison ...... 16 Figure 3. View of mandrill exhibit from southern exposure ...... 18 Figure 4. View of mandrill exhibit from eastern exposure ...... 19 Figure 5. Incision by adult female ...... 21 Figure 6. Mastication by sub-adult male #1...... 22 Figure 7. Mean number of incisions per action for eighteen food types: all individuals. 29 Figure 8. Mean number of mastications per action for eighteen food types: all individuals...... 32 Figure 9. The average number of incisions per action used during the consumption of six foods by the four study subjects...... 36 Figure 10. The average number of mastications per action used during the consumption of six foods by the four study subjects...... 38

Chapter 1. Introduction

An animal’s acquisition of food represents a complex combination of its behavior, morphology, and physiology (Milton, 1984). The relationship of these factors varies from species to species and this variation, therefore, provides insight into the constraints animals face as they acquire food (Lambert, 1998; Penry, 1993). Animals acquire suites of adaptations designed to overcome the challenges associated with a particular type of food. For instance, orangutans possess highly mobile and prehensile lips that allow for more precise positioning of food for rapid processing by the anterior teeth (Ungar, 1994).

Another suite of adaptations that are related to hard object feeding is an increase in enamel thickness, tooth size, and body mass (Durmont, 1995). Bearded saki monkeys demonstrate another set of adaptations to overcome dietary challenges. Bearded saki monkeys possess robust, laterally displaced canines that aid in the opening of fruits with high resistance to puncturing (Kinzey and Norconk, 1990). Through the study of the relationship between food and its ingestion, it is possible to understand the ways animals have adapted to most efficiently obtain the food and nutrition they require.

Studying the relationship between anatomy, diet, ingestion in extant primates has provided insight into primate evolutionary history. There is a plethora of studies highlighting the role diet and ingestion has played in shaping the anatomy and behavior of primate species. For example, Lambert (1998) highlighted the importance of gut

1 anatomy and gut retention time on the various primate diets. Primates that consume higher quantities of hard to digest foods, such as leaves, are expected to need more time to breakdown foods and absorb the nutrients inside them. Thus, these primates will possess longer gastrointestinal tracts and longer retention times of food in order to maximum nutrient uptake (Lambert, 1998). Diet can also impact the ingestive behavior of a species. For example, Ungar (1994) highlighted that folivores employed their incisors more frequently than frugivores and that larger food items required more incision as well.

Leaf ingestion uses a broader range of incisal action compared to fruits because leaves are tougher to shear apart (Ungar, 1994). However, the increase in incision for large foods could result from constraints in gape size to effectively processing these foods.

These two examples indicate that different foods require varying methods of ingestion.

Kinzey (1992) highlighted the connection between diet and ingestion in

Pitheciinae. The pitheciins consume high frequencies of hard objects, a dietary characteristic which separates this group of monkeys from other platyrrhines in terms of diet (Kinzey, 1992). The pitheciins possess several shared derived features other New

World monkeys lack, and which allow them to efficiently process hard seeds. The upper and lower incisors are inclined anteriorly enabling these primates to remove the hard pericarp of seeds (Kinzey, 1992). The canines are enlarged and laterally splayed to facilitate puncturing of large food items which the incisors are not able to (Kinzey, 1992).

Incisor and canine morphology in pitheciins demonstrates the importance of learning the role diet plays in shaping traits associated with ingestion. By continuing to explore the

2 relationship between diet and ingestion in closely related species, it is possible to gain further insight into how morphology and behavior are connected.

Cercocebus-Mandrillus relationship

The Papionin tribe of primates is an ecologically diverse group consisting of several Old World monkey genera. These genera occupy various ecological niches with several species of baboons inhabiting open savanna, while certain species of mangabeys, mandrills, and drills reside in forested habitats (Abernethy et al., 2002; Barton et al.,

1992). Due, in part, to the ecological diversity of this group, the phylogenetic relationship of these genera has been highly debated. This tribe was historically divided based on morphological similarities grouping Mandrillus and Papio as a monophyletic clade while the terrestrial mangabeys (Cercocebus) and the arboreal mangabeys (Lophocebus) were placed in another monophyletic clade (Hill, 1974; Thorington and Groves, 1970) (Figure

1). These divisions were based, in part, on similarities in cranial morphology and body size. For example, the mangabeys were grouped together because both Lophocebus and

Cercocebus possess deep supraorbital fossae (Harris, 2000). The Papio-Mandrillus clade was defined by the presence of shared morphological traits related to elongated faces and rostrums (Harris, 2000). Additionally, these clades were supported by a major disparity in body size: Lophocebus and Cercocebus are similarly sized with males averaging 9kg and

12kg resp. (Singleton, 2002). While baboons, mandrills, and drills are significantly larger: Papio males range from 16kg to 31kg and Mandrillus males average 34kg

(Singleton, 2002).

With the inclusion of genetic information from molecular studies, more light has been shed on the true relationships between these genera. Various genetic studies have revealed that mangabeys are a polyphyletic group with Lophocebus being the sister taxon of Papio, while Cercocebus and Mandrillus form a separate clade (Distotell, 1994;

Distotell et al., 1992). The polyphyly of mangabeys suggests that the shared facial characteristics of a deep supraorbital fossae is a homoplasy and is the result of convergent evolution. The same can be said for mandrills and baboons sharing characteristics for an elongated face.

Figure 1. Cladograms depicting two possible organizations of Papionin. The traditional grouping places Cercocebus and Lophocebus in the same clade (above). A reconstructed clade groups Cercocebus and Mandrillus together (below). Adapted from Singleton (2002). 4

The notion that these facial traits are convergent is supported further by work on the morphological characteristics in Papionin. Groves (1978) was the first to suggest features of the cranium that distinguish the two mangabey groups. He identified a number of features in the nasal bones, zygomatic arches, and ascending ramus of the mandibles separating the terrestrial and arboreal mangabeys. In Lophocebus, nasal bones are concave with the distal ends being upturned giving these species a snub-nosed shape to the rostrum. The zygomatic arches in Lophocebus have a root placed high above the toothrow which swings downward to the molar level before continuing horizontally. The ascending ramus of the mandible in Lophocebus is more horizontal and flares less than

Cercocebus. When combining these morphological characteristics with the molecular evidence, it appears the tradition Papionin phylogeny was incorrect and that Cercocebus and Lophocebus are not sister taxa.

Further research into the dentition and postcranium of mandrills and terrestrial mangabeys provides more evidence for a diphyletic origin of mandrills and baboons despite the shared cranial similarities (Fleagle and McGraw, 1999). Features in the forelimbs of Cercocebus and Mandrillus (relatively deep scapula, broad deltoid plane of the humerus, narrow olecranon fossa, etc.) point to a Cercocebus-Mandrillus clade.

These features are unique to the Cercocebus-Mandrillus clade and represent ecological adaptations towards significant terrestrial foraging behavior for these genera (Fleagle and

McGraw, 1999, 2002).

Both Cercocebus and Mandrillus forage for resources such as insects, seeds, and nuts in leaf litter and decomposing wood using their powerful forelimbs (Fleagle and

McGraw, 1999, 2002). Terrestrial foraging requires a strategy in which aggressive manual foraging is necessary to sift through leaves, dirt, rotten logs, etc. A heavy reliance on manual foraging increases the robusticity of the forelimbs and results in several forelimb adaptations unique to Cercocebus and Mandrillus. The humerus in these species provides a greater attachment point for a larger brachialis muscle to increase the power of elbow flexion (Fleagle and McGraw, 2002). In addition to a larger brachialis muscle, there are more pronounced crests in the ulna and radius for more prominent wrist and flexor musculature (Fleagle and McGraw, 2002). The scapula of monkeys within these genera also indicates a similarity in habitat usage with a heavy reliance on vertical tree climbing while ascending from the forest floor. The short and deep scapula in these primates is similar to what is observed in other primate groups who are known to vertically climb tree trunks (Fleagle and McGraw, 2002). All of these postcranial features indicate a shared evolutionary history with adaptations towards a heavy reliance on terrestrial foraging.

In addition to their shared cranial and postcranial morphologies, Cercocebus and

Mandrillus are united by adaptations in dentition resulting from their heavy reliance on hard object feeding. Terrestrial foraging has placed a selective pressure on these genera towards evolving stronger mandibles and dentition to cope with the greater forces to process food from a terrestrial diet (Daegling and McGraw, 2007). One result of this selective pressure is the enlargement of the upper and lower premolars of these genera

(Fleagle and McGraw, 1999, 2002). These larger premolars are used to crack open hard nuts and seeds found on the forest floor that other primates are not capable of opening

(Fleagle and McGraw, 1999, 2002). The similar response by terrestrial mangabeys and mandrills to increase premolar size in order to overcome the challenges of consuming hard foods might also indicate that these two species would employ similar oral processing behaviors as well.

The connection between large premolars and hard object feeding in extant primates is important for understanding the diets of extinct primate species, including fossil hominins. The genus Paranthropus exhibits major trend in hominin evolution with a significant increase in premolar size. The large premolars for members of this genus have been associated with the consumption and processing of both hard and tough objects based on what is known from extant hard object feeders (Guatelli-Steinberg, 2016).

Further research supported hard object feeding in Paranthropus species. For instance,

Paranthropus robustus has complex microwear textures similar to those of sooty mangabeys (Guatelli-Steinberg, 2016). Microwear texture analysis allows for inferences about diet due to the types of scratches food leaves on the tooth surfaces. Hard foods will leave complex patterns with heavy pitting on teeth while tough foods have high anisotropy or unidirectional scratching (Guatelli-Steinberg, 2016). Given the presumed similarities Paranthropus and sooty mangabeys share in dentition and diet, if it can be shown that oral processing behaviors are conservative across similar diets in primate species, then it would be possible to infer the oral processing behavior for extinct hominin species.

Cercocebus oral processing behaviors

Understanding how morphological traits function under natural conditions is an important aspect of research (Gross-Camp and Kaplan, 2011; McGraw et. al., 2016). For primates to most efficiently process their food, it is necessary for individuals employ strategies that provide an optimal order of operations (Chen, 2009). Understanding the strategies primates use to ingest and masticate their food can lead to better knowledge of the role cranial structures play in the consumption of food. For example, Vinyard et al.

(2003) highlighted the shared morphologies among tree gouging primates. Tree gouging is the use of the anterior teeth to bite into trees in order to elicit exudate flow. Those primates that specialize in tree gouging possess lower condyle heights and wider gapes

(Vinyard et al., 2003). The lower condyle heights and wider gapes facilitate tree gouging by effectively aligning the anterior teeth during gouging and reducing the jaw muscle stretching (Vineyard et al., 2003). These cranial and dental adaptations for tree gouging demonstrate how primate species have changed in response to foraging challenges. Thus, establishing connections between morphology and function provides insight into how foraging behavior is impacted.

A window into the selective pressures that help shape anatomical form can be made by comparing the oral processing behaviors of closely-related species who possess similar diets. Due to a shared common ancestry, any divergence in these species’ processing behaviors or craniofacial structures can plausibly be attributed to differences that occur in their diets. Data from McGraw et al. (2016) have shown that the differences in oral processing behaviors between two colobine species from the Taï Forest of Ivory

Coast can be explained by the presence of Pentaclethra macrophylla seeds and pods in the diets of Colobus polykomos. The hardness of the pods containing these seeds results in challenges that C. polykomos responds to with the use of an aggressive processing strategy that involves frequent incisions. The hardness of these pods is also reflected in higher chewing rates in C. polykomos compared to sympatric P. badius. This is because the seeds and pods require longer handling times to process. These differences in oral processing behaviors indicate a constraint on the ability for P. badius to process the same hard foods as C. polykomos.

While the use of dentition has been well-studied within Colobinae, oral processing behaviors have not received the same attention in the Cercocebus-Mandrillus clade. Sooty mangabeys (Cercocebus atys) have had their oral processing detailed the most (McGraw et al., 2011). In this study, McGraw et al. (2011) highlighted differences between age and sex classes in the amount of oral processing following ingestion. The consumption of Sacoglottis gabonensis seeds elicited the most variation in oral processing. Adult males incised and masticated more frequently than adult females. All adults also incised and masticated more than nonadults during processing of this food.

The husk of S. gabonensis seeds are the most mechanically challenging and hardest food in the sooty mangabey diet (Daegling et al., 2010) but it is also one of the most frequently consumed foods (McGraw et al., 2011). According to McGraw et al. (2011) the challenge observed in the processing of these seeds for sooty mangabeys could be explained by a biomechanical difference between sexes due to sexual dimorphism that could reduce masticatory efficiency in males.

In summary, these two studies of Tai Forest monkeys reveal that oral processing behaviors can vary from species to species depending on diet. Colobus polykomos requires more incisal work than Piliocolobus badius due to the presence of more challenging foods in the diet of the former. In addition to dietary differences in oral processing, there is the potential for variation to occur between age and sex classes in the same species. Adult male sooty mangabeys required the most amount of processing for hard object feeding. In general, adults required more processing than nonadults. An increase in the oral processing for a specific sex and age group could signal a constraint for that group. If the constraint arises from sexual dimorphism, then this constraint would be even more pronounced in an extremely sexually dimorphic species such as Mandrillus sphinx.

Mandrill diet

The examination of mandrills (Mandrillus sphinx) provide an excellent opportunity to explore the role sexual dimorphism of craniofacial features plays in the age and sex differences witnessed in its sister taxon sooty mangabey. These two species share a close evolutionary relationship and a variety of morphological similarities, when adjusted for size (Harris, 2000). Mandrills are the most sexually dimorphic primate with males and females possessing the largest disparity in body and canine size (Plavcan and van Schaik, 1992; Plavcan and van Schaik, 1997). Given this disparity, it is reasonable to predict that if differences in oral processing behaviors are indeed related to biomechanical differences between sexes, then this species would be the best representation of this effect.

Little is known about the diet and foraging behaviors of wild mandrills.

Determining what mandrills consume has been difficult due to several factors, one of which is the difficulty of habituating groups. This difficulty is due to this species’ tendency to form the largest stable groups of any primate, with groups averaging greater than six hundred individuals (Abernethy et al., 2002). In a large group, individual monkeys are not able to become accustomed to human presence and frequently flee upon contact, making observation difficult. Another limiting factor is this species’ ranging behavior and habitat. Groups traverse large home ranges and only remain in the same location for upwards to twenty minutes (Hoshino, 1975). Groups travel an average of four kilometers per day (Lahm, 1986). The long travel distances combined with the dense primary forest this species inhabits, makes it nearly impossible to follow groups once contact is made (Lahm, 1986). Direct observations of mandrill feeding are therefore few.

Lahm (1986) reported only 16.91 hours of stationary visual contact over the course of a year-long study.

In order to overcome the difficulties of direct visual observation, other methods of analysis have been employed to infer the mandrill diet. In a study of semi-wild mandrills,

Norris (1988) reported that 75% of the mandrill diet was obtained from terrestrial sources. Unidentified, small objects from the leaf litter (most likely seeds or insects) comprised 45% of the overall diet with ground plants (seeds, roots, fruits, leaves, stem pith, and apical ends of branches) representing 21%, and grasses and animal matter contributed to 10% each of total diet. The remaining 14% of the diet consisted of plant parts from arboreal sources.

Norris’s results differ slightly from previous studies on mandrills. Hoshino (1985) reported dietary data on wild mandrills based on fourteen encounters, fecal samples, and stomach contents from hunted individuals. Hoshino highlighted the importance of fruit, with 84% of the dry weight of feces comprised of fruit. The vast majority of fruit consumed (101 out of the 113 plant species) included the consumption of seeds. Similar to what has been found in sooty mangabeys, seeds are particularly important in the diet of mandrills. Sooty mangabeys consume large quantities of hard seeds and insects with 80% of their diet accounted for by the fruits of three tree species, insects, and fungi (McGraw et al., 2011). Leaves and invertebrates are a significant part of the mandrill diet combining with fruits to account for approximately 95% of total diet (Lahm, 1986).

Lahm (1986) also highlighted the importance of fruits and seeds in the diet of free- ranging mandrill with approximately 72% of their diet comprised of these foods.

One fruit species, Sacoglottis gabonensis, is important to highlight due to its high frequency in the diet of both mandrills and sooty mangabeys. The fruit of Sacoglottis gabonensis is highly seasonal, but during a three month span from August to October, this fruit was present in nearly 100% of mandrill feces (Hoshino, 1985). A heavy reliance on Sacoglottis gabonensis is found in sooty mangabeys with over 50% of their diet comprised of this resource (McGraw et al., 2011). Due to the hardness of these seeds, sooty mangabeys have evolved molarized premolars in order to use an isometric postcanine bite to crush open the seed casings (McGraw et al., 2011).

Captive mandrills as a comparison

Given the difficulty in observing wild mandrill feeding, the study of captive mandrills can provide useful insight into the oral processing behavior within the

Cercocebus-Mandrillus clade. Free-ranging primates have a significantly more diverse diet compared to those in captivity and can have a completely different composition. In captive situations, keepers are more focused on providing primates with appropriate nutrients and minerals than replicating a precise free-ranging diet (Dierenfeld, 1997).

Often, captive primates will receive diets that lack the challenging foods that can dominate wild diets (Cuozzo et al., 2010). It is most likely that captive mandrills will also lack the challenging foods that are present in the diets of their wild counterparts since zoos will not have any foods approaching the hardness of a Sacoglottis gabonensis seed.

Despite the absence of hard foods, the diets of captive mandrills (i.e. fruits, leaves, stems, and insects) are likely comparable to those of wild populations in terms of their similar properties. This means that it is possible to use a captive mandrills to understand the potential role of sexual dimorphism in oral processing behaviors and how this might vary in closely related species.

Research Questions

Building off previous research on other primates, this thesis explores oral processing behaviors of mandrills in a captive setting. The purpose of this research is to better understand the connection between sexual dimorphism and oral processing behaviors. In order to achieve this goal, I address three overarching questions: 1) what are the main characteristics of captive mandrill oral processing behaviors and how do these

13 characteristics vary with different foods? 2) How conservative are oral processing behaviors across taxa and do these characteristics remain consistent between Cercocebus atys and Mandrillus sphinx? 3) What role does sexual dimorphism play in constraining oral processing behaviors?

Chapter 2. Methods

Subjects

Data collection occurred between May, 2018 and July, 2018 at the Columbus Zoo in Powell, Ohio. The captive mandrill group at this zoo consists of four individuals: one adult male, one adult female, and two sub-adult males. The oldest member is the adult male at twenty-two years of age, while the adult female is twenty years old. Both sub- adult males are considerably younger, with the eldest being six years old and the other five years old. The two sub-adults are not sexually mature, meaning they have not reached maximum adult canine or body size (Wickings and Dixson, 1992). The group composition allows for age/sex class comparisons which could reveal if sexual dimorphism impacts oral processing.

Figure 2. Adult male and female size comparison. As can be seen the adult male (foreground) and female (background) differ significantly in size.

Study site

During summer months, this group inhabits an outdoor exhibit while during winter they are kept in an indoor set of cages. The outdoor exhibit possesses features designed to mimic a natural environment and includes thick patches of grass, real and fake trees, fallen trunks, and large piles of mulch and dirt (Figures 3 and 4). The inclusion of these features encourages foraging behaviors known to occur in this species’ wild counterparts. The most important features are the mulch piles and patches of grass in which zoo keepers hide food. By hiding food, the subjects are required to forage and sift through various mediums which involves considerable manual foraging. This type of foraging behavior is frequently observed in the terrestrial foraging patterns of wild populations of mandrills (Hosino, 1985; Rogers et al., 1996).

The monkeys are fed individual meals twice a day in separate indoor cages. These individual meals ensure that each monkey receives a sufficient amount of food with little competition from others. These two meals comprise the bulk of the captive mandrill diet but zookeepers stock the exhibit with enrichment foods and items. Enrichment foods and items are used to encourage foraging activity for this monkeys throughout the day that is similar to what is observed in wild mandrills. Typically, the enrichment is hidden in a variety of objects, such as boxes, dog toys, or butcher paper, requiring the monkeys to search through these objects. The zookeepers also disperse smaller foods (diced vegetables and snack clusters) throughout the mulch piles and grassy areas as more enrichment for the monkeys. The enrichment foods only constitute a small portion of the mandrill diet but are the foods in which oral processing behavior was analyzed. It is not expected any differences to arise in oral processing between the indoor meals and outdoor enrichment. The meals and enrichment typically consist of the same foods: fruits, vegetables, leaves, and monkey chow. Therefore, there shouldn’t be inconsistencies with observing the oral processing only while the monkeys are in the outdoor exhibit.

Figure 3. View of mandrill exhibit from southern exposure. In the foreground are examples of the mulch piles the subjects forage through. Here, the subjects are also able to reach through the fencing to reach food from trees surrounding the exhibit.

Figure 4. View of mandrill exhibit from eastern exposure. The grassy areas and fake log in this location provide areas for keepers to disperse enrichment foods to encourage foraging activity for the subjects. The paper in this picture is an example of one method of enrichment.

Behavioral sampling methods

On most days, observations began at 9:00 am and continued until 7:00 pm. On certain days, the zoo keepers would disperse a cluster of food in the afternoon typically around 2:00 pm. The administration of the clusters of food, from here on referred to as snack clusters, limited data collection because of the ways in which the subjects orally processed these snack clusters. As explained later, it was necessary to exclude data after

19 the dispersal of snack clusters due to errors that could have arisen in my method of analyzing oral processing behaviors.

Following McGraw et al. (2016), oral processing behavior was recorded using two minute focal animal sampling periods. Data were not used for focal periods in which visual contact was lost before the end of the scan. During a focal period, every time an animal introduced a food item into the oral cavity, it was recorded as an action. For each action, the number of times the focal subject used incisal bites with their anterior teeth was counted. An example of an incisal bite is shown in Figure 5. Once processing with the anterior teeth was completed, the number of masticatory chews using the postcanine teeth was counted for every action. This behavior is demonstrated in Figure 6. This method of data collection allows for the observer to calculate the average number of incisions and mastications per action for each type of food consumed.

As mentioned, the consumption of snack clusters was problematic for data collection. Snack clusters varied in composition but usually contained small foods such as bird seed, sunflower seeds, small nuts, cereal, and monkey chow (manufactured food similar to dog biscuits). The zookeepers distributed snack clusters by throwing handfuls through the wired fence into the grassy and mulch areas of the exhibit. The dispersal of the snack clusters greatly increased the foraging activity for all subjects; however, it was problematic for data collection due to the monkeys’ tendency to cache snack clusters in their cheek pouches. In these instances, the monkeys did not perform any processing during the introduction of the food into the oral cavity and it was assumed they processed foods at later times. The storage of food in cheek pouches obviously prevents the

20 calculation of all possible incisions and mastications for each ingestive action. As noted by McGraw et al. (2011), it is not possible to assign mastications to an ingestive action if there is food that had previously been cached in the cheek pouches. Foods from earlier ingestive actions could be masticated later after further ingestion has occurred leading to confusion as to which food is currently being chewed. Thus, data collection was halted after the dispersal of snack clusters due to the monkeys storing these foods in their cheek pouches for several hours after initially foraging for them.

Figure 5. Incision by adult female. This is an example of an incision for one ingestive action. The subject introduces the food item into its oral cavity (an action) and then may use its anterior teeth to process or remove from a larger substrate.

Figure 6. Mastication by sub-adult male #1. This is an example of the sub-adult male masticating during an action. He is using his postcanine teeth to crush the branch.

Data analysis

Data were analyzed using Kruskal-Wallis tests with a Dunn post-hoc tests. These tests were performed using R software to determine significance across several variables.

These nonparametric tests allow for comparisons between multiple groups of independent variables. Thus, I was able to calculate averages for incision and mastication associated with each food type for the entire group as well as each individual for a particular food type.

The Kruskal-Wallis test and Dunn post-hoc tests were also used in comparisons between different food types. For example, I was able to determine if there were any significant oral processing differences between the adult male, adult female, and sub- adult males during consumption of lettuce. For all analyses, it was determined that a minimum of fifteen observations for each food type was needed to run the tests (M.

Hubbe, pars comm). All eighteen foods had at least fifteen observations when combining all four subjects’ consumption of that particular food. For the comparisons between age and sex classes, four foods met the minimum requirement of fifteen observations for each individual. There were an additional two foods with sufficient data for at least three subjects.

Chapter 3. Results

Diet

Over the course of the study period, the diet for this group consisted of nineteen different foods (Table 1). Even though snack clusters were excluded from data analysis, they accounted for the largest portion of ingestive actions, consisting of nearly 50% of the sample. When excluding feeding on snack clusters, there was a total of 1,111 ingestive actions for the remaining eighteen foods. Six of the eighteen foods were consumed in sufficient quantities (at least 15 observations) by at least three of the four individuals to allow comparisons across age/sex classes. These six food types (grass, lettuce, stems, mature leaves, insects, and ice cubes) represented the six most frequently consumed foods after snack clusters, and constituted approximately 43% of the total actions for the group.

Comparison across food types

Kruskal-Wallis and Dunn tests were used to determine if there were significant differences in oral processing between the various foods. Figure 7 shows the mean number of incisions per food for the entire group while Table 2 reports the p-values for

Resource Code Percentage of Total Actions Snack Cluster SC 47.95% Grass GRA 10.32% Lettuce LT 9.94% Stem ST 8.62% Mature Leaf ML 8.32% Insect IN 3.58% Ice Cube IC 2.00% Bark BK 1.96% Diced Cucumber CU 1.83% Diced Carrot CT 1.32% Fruit FR 1.11% Grass Roots GRT 0.90% Watermelon Chunks WA 0.81% Petiole PT 0.55% Grass Flower FLG 0.47% Straw SW 0.34% Cardboard Box Peel CP 0.26% Butcher Paper BP 0.13% Bell Pepper BE 0.04% Table 1. Diet Composition

25 the Kruskal-Wallis and Dunn tests. There was no significant difference between diced carrots and insects (p = 0.1979); however, both of these foods required significantly less

(p < 0.05) incisions per action (usually none) compared to all other foods. At the other end of the spectrum, there were several food types that required more incisal work than other foods. Petioles, stems, and bark had significantly higher averages of incisor usage

(p < 0.05) than other foods. The averages for these three foods were between 2.5 and 3.0 incisions per action, while the averages for the majority of foods fell between 1.0 and 2.0 incisions per action.

Figure 8 shows the mean number of mastications for each food and Table 3 reports the p-values for comparisons of mastication means of each food. Overall, there were fewer significant differences for mastication than in incisor usage. There were several resources that stood out, requiring significantly less chewing than the other foods in the diet. Grass flowers and ripe fruit did not differ significantly from each other (p =

0.4925) but did diverge from the rest of the foods in the sample (p < 0.05). The next lowest average mastication per action was for cardboard box peels with a mean of 6.0 which was significantly lower than most of the other foods. In general, no foods required significantly more chewing than any other with most falling between 10.0 and 15.0 mastications per action.

BE BK BP CP CT CU FLG FR GRA BK 0.0942 BP 0.3615 0.0615 CP 0.096 0.4292 0.0786 CT 0.2249 0.0135* 0.2771 0.08 CU 0.163 0.0633 0.164 0.171 0.1891 FLG 0.0288* 0.057 0.0111* 0.134 0.0038* 0.0109* FR 0.0202* 0.0013* 0.0029* 0.0666 0.0000* 0.0000* 0.4925 GRA 0.1488 0.0446* 0.1374 0.1882 0.097 0.3847 0.0109* 0.0000* GRT 0.1424 0.1887 0.1334 0.2482 0.1368 0.3541 0.0238* 0.0003* 0.4116 IC 0.2078 0.0086* 0.2437 0.088 0.4166 0.2111 0.0038* 0.0000* 0.0832 IN 0.1417 0.0906 0.1271 0.2166 0.087 0.3274 0.0147* 0.0000* 0.3900 LT 0.1631 0.0223* 0.1615 0.1528 0.1579 0.4776 0.0078* 0.0000* 0.2737 ML 0.2094 0.0013* 0.2452 0.0745 0.4254 0.1442 0.0026* 0.0000* 0.0091* PT 0.3092 0.0066* 0.4328 0.0374* 0.2364 0.0736 0.0017* 0.0000* 0.0379* ST 0.1208 0.1821 0.0944 0.2855 0.0294* 0.1492 0.0229* 0.0000* 0.0945 SW 0.2221 0.0893 0.2761 0.1341 0.4599 0.3183 0.0130* 0.0008* 0.2591 WA 0.1669 0.1102 0.1743 0.186 0.234 0.4961 0.0151* 0.0001* 0.4131 continued Table 2. P-values from Kruskal-Wallis tests that compare mean number of incisions for all eighteen foods: all individuals. Significant values are denoted by a *.

Table 2 continued.

GRT IC IN LT ML PT ST SW

IC 0.1501

IN 0.4738 0.0782

LT 0.3163 0.1613 0.2338

ML 0.1089 0.4707 0.0195* 0.0484*

PT 0.0557 0.1734 0.0343* 0.0589 0.1634

ST 0.365 0.0160* 0.2316 0.0357* 0.0003* 0.0139*

SW 0.2478 0.4883 0.2347 0.316 0.4991 0.2604 0.1577 WA 0.3722 0.2674 0.3651 0.4885 0.2267 0.0998 0.2243 0.3347

Figure 7. Mean number of incisions per action for eighteen food types: all individuals combined.

BE BK BP CP CT CU FLG FR GRA BK 0.0942 BP 0.3615 0.0615 CP 0.096 0.4292 0.0786 CT 0.2249 0.0135* 0.2771 0.08 CU 0.163 0.0633 0.164 0.171 0.1891 FLG 0.0288* 0.057 0.0111* 0.134 0.0038* 0.0109* FR 0.0202* 0.0013* 0.0029* 0.0666 0.0000* 0.0000* 0.4925 GRA 0.1488 0.0446* 0.1374 0.1882 0.097 0.3847 0.0109* 0.0000* GRT 0.1424 0.1887 0.1334 0.2482 0.1368 0.3541 0.0238* 0.0003* 0.4116 IC 0.2078 0.0086* 0.2437 0.088 0.4166 0.2111 0.0038* 0.0000* 0.0832 IN 0.1417 0.0906 0.1271 0.2166 0.087 0.3274 0.0147* 0.0000* 0.39 LT 0.1631 0.0223* 0.1615 0.1528 0.1579 0.4776 0.0078* 0.0000* 0.2737 ML 0.2094 0.0013* 0.2452 0.0745 0.4254 0.1442 0.0026* 0.0000* 0.0091* PT 0.3092 0.0066* 0.4328 0.0374* 0.2364 0.0736 0.0017* 0.0000* 0.0379* ST 0.1208 0.1821 0.0944 0.2855 0.0294* 0.1492 0.0229* 0.0000* 0.0945 SW 0.2221 0.0893 0.2761 0.1341 0.4599 0.3183 0.0130* 0.0008* 0.2591 WA 0.1669 0.1102 0.1743 0.186 0.234 0.4961 0.0151* 0.0001* 0.4131 continued Table 3. P-values from Kruskal-Wallis tests that compare mean number of mastications for all foods: all individuals combined. Significant values are denoted by a *.

Table 3 continued GRT IC IN LT ML PT ST SW IC 0.1501 IN 0.4738 0.0782 LT 0.3163 0.1614 0.2338 ML 0.1089 0.4707 0.0195* 0.0484* PT 0.0557 0.1734 0.0343* 0.0589 0.1634 ST 0.365 0.0160* 0.2316 0.0357* 0.003* 0.0139* SW 0.2478 0.4883 0.2347 0.316 0.4991 0.2604 0.1577 WA 0.3722 0.2674 0.3651 0.4885 0.2267 0.0998 0.2243 0.3347

Figure 8. Mean number of mastications per action for eighteen food types: all individuals combined.

Comparison across age/sex class

I tested for significant differences in oral processing between subjects for commonly consumed foods in order to identify any age/sex differences. There were four food resources with at least fifteen observations by all four subjects: grass, lettuce, stems, and mature leaves. There were two other foods in which there were enough data for three out of the four subjects. For insects, there was only enough data for comparisons between the adult female, and both sub-adult males. The other case with sufficient data for three individuals was with ice cube consumption where comparisons were made between the adult male and two sub-adult males.

The p-values for the comparisons between individuals for each the six foods are shown in Tables 4 – 9. Figure 9 depicts the mean number of incision for each individual.

Several differences were identified in the frequency individuals employed their incisors while processing the same types of food. The adult male used his incisors more frequently than both the adult female (p = 0.0034) and sub-adult male #2 (p = 0.0014) when consuming grass. In addition, he was observed to incise more frequently consuming ice cubes than sub-adult male #2 (p = 0.0002). However, on average, the adult male used fewer incisions for processing stems compared to the adult female (p = 0.0228) and the sub-adult male #2 (p = 0.0215). The adult female also used more incision for processing insects compared to both the sub-adult males (p = 0.0001 and 0.0012, resp.). The sub- adult male #1 had a higher incision mean when consuming lettuce than the adult female

(p = 0.0432). The only differences between the sub-adult males in incision use occurred during consumption of lettuce (p = 0.0151) and ice cubes (p = 0.0374). The only

33 significant difference between individual incisor use in the consumption of mature leaves was between the adult male and sub-adult male #1 (p = 0.0485) with the sub-adult male using more incision.

The p-values for the tests of significance are shown in Table 10 – 15. Figure 10 shows the mean number of mastications for each food for each subject. There was variation identified in average mastication between individuals for the various food types.

The adult male masticated lettuce more frequently than the adult female (p = 0.0111), sub-adult male #1 (p = 0.0316), and sub-adult male #2 (p = 0.0276). There were several differences in the mastication of grass by the individuals. The adult male significantly masticated grass more than sub-adult #1 (p = 0.0255). Sub-adult male #2 masticated significantly more than both sub-adult #1 (p = 0.0023) and the adult female (p = 0.0255) during consumption of grass. The last significant difference was in the comparison between the adult male and the sub-adult male #2 in the consumption of ice cubes. Sub- adult male #2 required more mastication for ice cubes than the adult male (p = 0.0395).

There were no significant differences in the mastication means for insects, stems, and mature leaves.

AF AM SAM #1 AM 0.1303 SAM #1 0.2444 0.0485* SAM #2 0.2588 0.2406 0.0854 Table 4. P-values from Kruskal-Wallis comparisons of individuals for mature leaf incision.

AF AM SAM #1 AM 0.2059 SAM #1 0.0432* 0.2016 SAM #2 0.4494 0.1709 0.0151* Table 5. P-values from Kruskal-Wallis comparisons of individuals for lettuce incision.

AF AM SAM #1 AM 0.0228* SAM #1 0.1226 0.1651 SAM #2 0.4144 0.0215* 0.1299 Table 6. P-values from Kruskal-Wallis comparisons of individuals for stem incision.

AF AM SAM #1 AM 0.0034* SAM #1 0.0853 0.084 SAM #2 0.4478 0.0014* 0.0561 Table 7. P-values from Kruskal-Wallis comparisons of individuals for grass incision.

AF SAM #1 SAM #1 0.0001* SAM #2 0.0012* 0.0588 Table 8. P-values from Kruskal-Wallis comparisons of individuals for insect incision.

AM SAM #1 SAM #1 0.1242 SAM #2 0.0002* 0.0374* Table 9. P-values from Kruskal-Wallis comparisons of individuals for ice cube incision.

Incision AM AF 2.5 SAM1 2 SAM2

1.5

0.5

Insect Grass Lettuce Stem Mature Leaf Ice Cube Meannumber incisions of per action Food type

Figure 9. The average number of incisions per action during consumption of six foods by the four study subjects. Sufficient data from all four subjects were available for four foods while sufficient data were available for only three subjects for the last two foods.

AF AM SAM #1 AM 0.4551 SAM #1 0.2331 0.2361 SAM #2 0.0586 0.0873 0.259 Table 10. P-values from Kruskal-Wallis comparisons of individuals for mature leaf mastication.

AF AM SAM #1 AM 0.0111* SAM #1 0.3286 0.0316* SAM #2 0.129 0.0276* 0.2956 Table 11. P-values from Kruskal-Wallis comparisons of individuals for lettuce mastication.

AF AM SAM #1 AM 0.3409 SAM #1 0.3778 0.4438 SAM #2 0.0832 0.2862 0.1843 Table 12. P-values from Kruskal-Wallis comparisons of individuals for stem mastication.

AF AM SAM #1 AM 0.1219 SAM #1 0.1844 0.0255* SAM #2 0.0255* 0.3045 0.0023* Table 13. P-values from Kruskal-Wallis comparisons of individuals for grass mastication.

AF SAM #1 SAM #1 0.2149 SAM #2 0.0789 0.2405 Table 14. P-values from Kruskal-Wallis comparisons of individuals for insect mastication.

AM SAM #1 SAM #1 0.3573 SAM #2 0.0395* 0.1248 Table 15. P-values from Kruskal-Wallis comparisons of individuals for ice cube mastication.

Mean Mastication Rates AM AF 16 SAM1 15 SAM2 14

7 Meannumber mastications of per action

6 Insect Grass Lettuce Stem Mature Leaf Ice Cube Food type

Figure 10. The average number of mastications per action during consumption of six foods by the four study subjects. Sufficient data from all four subjects were available for four foods while sufficient data were available for only three subjects for the last two foods.

Chapter 4. Discussion

In general, results from this study suggest absence of an oral processing regime common to all age/sex classes in captive mandrills. One age or sex class does not use more incision or mastication for every food type in this sample. There were several instances in which the adult male used more incision and mastication than the adult female or sub-adult males, but there were also foods in which he used less. Although the data set is modest, the preliminary results presented here contrast with what has been reported in sooty mangabeys. Cercocebus atys in Ivory Coast’s Tai Forest exhibits a strict pattern of oral processing where the only age and sex class differences observed occurred during the processing of Sacoglottis gabonensis seeds. Oral processing profiles of all age/sex classes are similar during consumption of all other foods. During consumption of

Sacoglottis gabonensis seeds, adult males used more incision and mastication for this food than adult females or sub-adults. One possibility for the difference in male oral processing could be males experience a reduction in mechanical efficiency of the chewing apparatus (McGraw et al., 2011). In order for males to maintain large canines, morphological adjustments in the cranium must be made in to accommodate a larger gape

(Hylander, 2013). However, the mandrill adult male did not incise or masticate the most for all foods. There were some instances in which the adult male engaged in more incision and chewing than both the adult female and a sub-adult male but there were also

39 cases where he was more efficient with his processing, chewing less frequently. The lack of general commonality between all individuals indicates that oral processing regimes are age and sex specific, at least in captive mandrills.

General characteristics of mandrill processing activities

In general, the Columbus mandrills exhibited oral processing behaviors that diverged from those observed in sooty mangabeys. When considering all food types and all individuals combined, this mandrill group exhibited means of 1.6 incisions and 9.3 mastications. Comparing these averages to those of wild sooty mangabeys populations

(4.4 and 7.06, resp.) it is clear that mandrills have lower averages for incision but higher averages for mastication (McGraw et al., 2011). These data suggest that mandrills are able to initially break down their foods more efficiently than sooty mangabeys with their anterior teeth but are less efficient when using their molars for mastication. The species difference in processing efficiency could arise from either a difference in diet (captive vs. free-ranging) or craniofacial differences between the two species leading to divergence in chewing efficiency. The captive mandrills could exhibit different oral processing behaviors due to the composition of their diet being significantly softer and easier to process compared to wild sooty mangabeys. Captive mandrill diet is comprised of large quantities of domesticated fruits and vegetables which are far easier to process than foods such as Sacoglottis gabonensis seeds, which could result in lower frequencies in incision and mastication. However craniofacial differences could also be responsible for the species difference in oral processing behaviors. Any changes to the masticatory apparatus could lead to potential decreases in the chewing efficiency for that species.

As predicted, mandrill oral processing behavior co-varied with the food consumed. Certain foods, such as diced carrots, diced cucumbers, and insects, required much less incision compared to others such as bark, stems, and petioles. This conclusion is similar to what was learned about sooty mangabey processing behavior in which smaller, softer food resources, such as invertebrates, mushrooms, and fruits, were associated with lower incision means than the harder seeds of S. gabonensis and

Anthonata fragrans (McGraw et al., 2011). For both mandrills and sooty mangabeys, the most challenging food resources required the most incision but only in sooty mangabeys did this translate to lower averages in mastication. In mandrills, the lowest mastication means were associated with foods that do not present a significant processing challenge, such as flowers and ripe fruits. Thus, there are some oral processing behaviors that are conservative across closely related primate taxa. The similarity in insect processing between mandrills and sooty mangabeys indicates that for small food items oral processing does not differ significantly. However for foods most difficult to process, there are different constraints placed on the two species that result in differing oral processing for these foods.

Oral processing across age/sex classes

Captive mandrills varied in which age/sex class incised or masticated the most for each food. For example, the adult male exhibited the highest incision mean during ice cube consumption but a sub-adult male incised the most during consumption of lettuce.

This contrasts with what was observed in sooty mangabeys. Sooty mangabey oral processing was similar across age/sex classes except during consumption of hard objects

41 such as S. gabonensis seeds (McGraw et al., 2011). Adult male sooty mangabeys used more incisions and mastications to process these hard seeds compared to females and sub-adults. Captive mandrills were similar to sooty mangabeys in their pattern for hard object oral processing with the adult male incising the most their hardest food (i.e. ice cubes). However, mandrills also exhibited significant differences in softer but tougher to chew foods such as grasses and lettuce, where sooty mangabeys showed no significant differences in their consumption of these types of foods in their diets. Another area in which mandrills differed from sooty mangabeys is male mandrills are sometimes more efficient during incision and mastication than the other age and sex classes. The differences in oral processing regimes between mandrills and sooty mangabeys suggests the presence of a constraint on chewing efficiency for one of these species.

The role of sexual dimorphism

Sexual dimorphism could help explain the differences in oral processing behavior between mandrills and sooty mangabeys. Mandrills are the most sexually dimorphic primate, with males over twice the size of females and males possessing canines up to four times larger than those of females (Plavcan and van Schaik, 1992; Plavcan and van

Schaik, 1997). Cercocebus atys is also sexually dimorphic, but to a lesser degree: male body mass averages 11.1 kg while females average 6.3 kg (Delson et al., 2000). The difference in the degree of sexual dimorphism between mandrills and sooty mangabeys might translate into the differences in oral processing.

Sexual dimorphism explains many differences in craniofacial morphology across primates. Several of these differences occur in areas of the cranium that are important in

42 handling the stresses generated during incision and mastication. For instance, in a study of gorilla and orangutan skulls, there were several sexual differences in rostrum morphology in the two species (O’Higgins and Dryden, 1993). In both species, males have increased facial prognathism in order to accommodate dimensional differences in the anterior region of the face compared to females (O’Higgins and Dryden, 1993). These differences result in an increased palate width at the canines, lower facial length, and increased alveolar height for males (O’Higgins and Dryden, 1993). Papionin males also possess morphologically different rostrums with males having a longer and vertically deeper muzzle than females (O’Higgins and Collard, 2002). Additionally, these males have broad zygomatic roots, more vertical posterior aspect of the maxilla, and an increased subnasal height (O’Higgins and Collard, 2002). While these differences in the rostrum are adaptations for larger canines in males, modifications in the morphology of the chewing apparatus could correspond to decreases in the ability for males to process food.

The configuration of the anterior portion of the rostrum significantly influences the ability of an animal to deal with the forces generated during oral processing. Different loads and stresses are placed on the bone in the anterior portion of the maxilla during incision compared to mastication (Daegling and McGraw, 2007). During incision, the anterior region of the rostrum experiences coronal bending due to axial twisting, whereas this region experiences lateral transverse bending during mastication (Daegling and

McGraw, 2007). Any of the sexual dimorphic differences in cranial features that effects how the bone in the rostrum responds to the loads placed on it during incision and

43 mastication could explain the differences in age and sex class oral processing behavior observed in this study.

In sooty mangabeys, the majority of instances in which the adult males used more incision, postcanine bites, and mastication than adult females was during ingestion of

Sacoglottis gabonensis seeds (McGraw et al, 2011). These seeds are the hardest and most mechanically demanding food in the diet of this species and, presumably, would place the highest amounts of stress on the chewing apparatus. The significant increase in processing behavior exhibited by the adult males suggest they may experience a biomechanical disadvantage compared to females. This biomechanical disadvantage might be even more exaggerated with the extreme dimorphism exhibited by male mandrills. Due to the massive size of mandrill canines, they are required to have the largest jaw gape among primates (Smith, 1984; Hylander, 2013). In order to maintain functionality of the canines, the jaws of mandrills “responded” by increasing the range of motion in which they can open (Hylander, 2013). For this range of motion to increase to the degree seen in mandrills, changes in the muscle structure in the jaw are required.

During the power stroke of mastication, there is a decrease in bite force for animals with larger gapes due to a larger gape being correlated with more posteriorly placed jaw muscles and longer muscle fibers (Hylander, 2013). The posterior placement of jaw muscles and the longer muscle fibers they possess decreases mastication efficiency due to longer muscle fibers resulting in a decrease in the amount of force the muscle fibers are able to generate (Hylander, 2013). Therefore, animals, such as mandrills who invest in large canines for male displays of dominance, likely experience a trade-off in the

44 efficiency of their masticatory apparatus. A trade-off in masticatory efficiency will be reflected in their oral processing behaviors. Specifically, these males will exhibit higher frequencies in the number of incisions and mastications that are required to breakdown food compared to females and sub-adults who do not experience this constraint.

Future directions

It is necessary to emphasize the preliminary nature of this study and to reiterate the modesty of sample size and short duration of the observations. Further data are needed to provide scrutinize the conclusions made here and to clarify the role sexual dimorphism may play in constraining oral processing behavior. The small sample size may account for the absence of a pattern found in the oral processing behaviors of this species, especially in the comparisons with the adult male. He was the least active forager of all individuals and often was the limiting factor (i.e., smallest sample size) comparisons across age and sex classes for each food type. In addition to a small sample size, age/sex include no more than two individuals. Therefore, any variation or abnormalities in one individual would significantly influence the results from this study.

For example, there could be issues arising from the age of the adults, both of whom are over twenty years old. In addition to the significant amount of arthritis the adult male possesses (which most likely affected his foraging activity as well), dental wear and dental pathologies increase with age (Cuozzo et al., 2010). The impact of dental wear and dental pathologies on oral processing is not yet known, but if there is an effect, then it is reasonable to suggest this sample population might be susceptible to this impact with the advanced age of half the members.

Further studies on wild or semi-wild populations of mandrills are needed to improve our understanding of oral processing in primates. For example, we need to learn how oral processing differ between mandrills in a captive setting and their wild counterparts. Captive diets likely do not contain as challenging foods as wild diets, and this could result in lower means in incision and mastication. Ice cubes are the only captive food type that could serve as a proxy for hard-object eating even though this food is nowhere near the hardest consumed foods in a free-ranging population. Ice cube processing in mandrills required much less incision than the processing of Sacoglottis gabonensis by sooty mangabeys. There are other foods types in the captive population that serve as better comparisons. Insect consumption was comparable between the captive mandrills and free-ranging sooty mangabeys indicating oral processing for this food type is potentially conserved within the clade, independent of the environment. Processing profiles of mature leaves, stems, petioles, and bark should also be similar between populations, but this hypothesis needs testing.

The overall goal of this thesis was to determine how conservative oral processing behaviors are across primate taxa. Mandrills and sooty mangabeys serve as appropriate candidates for asking this question due to their close relationship and dietary similarities.

Additional oral processing data on free-ranging mandrill populations will allow for further insight into the differences that arise due to morphological constraints or dietary variation.

Bibliography

Abernethy, K. A., White, L. J. T., and Wickings, E. J. 2002. Hordes of mandrills (Mandrillus sphinx): extreme group size and seasonal male presence. Journal of Zoology 258:131-137.

Barton, R. A., Whiten, A., Strum, S. C., Byrne, R. W., and Simpson, A. J., 1992. Habitat use and resource availability in baboons. Animal Behaviour 43:831-844.

Cuozzo, F.P., Sauther, M.L., Gould, L., Sussman, R.W., Villers, L.M., and Lent, C. 2010. Variation in dental wear and tooth loss among known-aged, older ring-tailed lemurs (Lemur catta): a comparison between wild and captive individuals. American Journal of Primatology 72:1026-1037.

Daegling, D. J. and McGraw, W. S. 2007. Functional morphology of the mangabey mandibular corpus: relationship to dental specializations and feeding behavior. American Journal of Physical Anthropology 134:50-62.

Daegling, D. J., McGraw, W. S., Vick, A. E., Rapoff, A. J., Bitty, A., and Paacho, R. 2010. Masticatory effort and dietary hardness in sooty mangabeys (Cercocebus atys) from Tai Forest, Ivory Coast. American Journal of Physical Anthropology Supplement 50:90.

Dierenfeld, E.S. 1997. Captive wild animal nutrition: a historical perspective. Proceedings of the Nutrition Society 56:989-999.

Distotell, T. R. 1994. Generic level relationships of the Papionini (Cercopithecoidea). American Journal of Physical Anthropology 94:47-57.

Distotell, T. R., Honeycutt, R. L., and Ruvolo, M. 1992. Mitochondrial DNA phylogeny of the Old-world monkey tribe Papionini. Molecular Biology Evolution 9:1-13.

Dumont, E. R. 1995. Enamel thickness and dietary adaptation among extant primate and chiropterans. Journal of Mammalogy 76:1127-1136.

Fleagle, J. G. and McGraw, W. S. 1999. Skeletal and dental morphology supports diphyletic origin of baboons and mandrills. PNAS 96:1157-1161.

Fleagle, J. G. and McGraw, W. S. 2002. Skeletal and dental morphology of African papionins: unmasking a cryptic clade. Journal of Human Evolution 42:267-292.

Groves, C. P. 1978. Phylogenetic and population systematics of the mangabeys (Primates: Cercopithecoidae). Primate 9:1-34.

Guatelli-Steinberg, D. 2016. What teeth reveal about human evolution. Cambridge, UK: Cambridge University Press.

Harris, E. E. 2000. Molecular systematics of the Old World monkey tribe Papionini: analysis of the total available genetic sequences. Journal of Human Evolution 38:235- 256.

Hill, W. C. O. 1974. Primates: comparative anatomy and taxonomy. Volume VII: Cynopithecinae. Edinburgh: The University Press.

Hoshino, J. 1985. Feeding ecology of mandrills (Mandrillus sphinx) in Campo Animal Reserve, Cameroon. Primates 26:248-273.

Hylander W. L. 2013. Functional links between canine height and jaw gape in catarrhines with special reference to early hominins. American Journal of Physical Anthropology 150:247-259.

Jouventin, P. 1975. Observations sur la socio-écologie du mandrill. La Terre et la Vie 29:439-532.

Lahm, S. A. 1986. Diet and habitat preference of Mandrillus sphinx in Gabon: implications of foraging strategy. American Journal of Primatology 11:9-26.

Lambert, J. E. 1998 Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evolutionary Anthropology 7:8-20.

Kinzey, W. G. 1992. Dietary and dental adaptations in the Pitheciinae. American Journal of Physical Anthropology 88:499-514.

Kinzey, W. G. and Norconk, M. A. 1990. Hardness of a basis of fruit choice in two sympatric primates. American Journal of Physical Anthropology 81:5-15.

McGraw, W. S., Vick, A., and Daegling, D. J. 2011. Sex and age differences in the diet and ingestive behaviors of sooty mangabeys (Cercocebus atys) in the Tai Forest, Ivory Coast. American Journal of Physical Anthropology 144:140-153.

McGraw, W. S., Vick, A., and Daegling, D. J. 2014. Dietary variation and food hardness in sooty mangabeys (Cercocebus atys): implications for fallback foods and dental adaptation. American Journal of Physical Anthropology 154:413-423.

Milton, K. 1984. The role of food processing factors in primate food choice. In Rodman, P. S., and Cant J. G. H. (eds), Adaptations for Foraging in Nonhuman Primates: Contributions to an Organismal Biology of Prosimians, Monkeys and Apes, pp. 249–279. New York: Columbia Press.

Norris, J. 1988. Diet and feeding behavior of semi-free ranging mandrills in an enclosed Gabonais Forest. Primates 29:449-463.

O’Higgins, P. and Collard, M. 2002. Sexual dimorphism and facial growth in Papionin monkeys. The Zoological Society of London 257:255-272.

O’Higgins, P. and Dryden, I. L. 1993. Sexual dimorphism in hominoids: further studies of craniofacial shape differences in Pan, Gorilla, and Pongo. Journal of Human Evolution 24:183-205.

Penry, D. L. 1993. Digestive constraints of diet selection. In Hughes, R. W., (ed), Diet Selection: An Interdisciplinary Approach to Foraging Behavior, pp. 32–55. Oxford: Blackwell Scientific.

Plavcan, J. M. and van Schaik, C. P. 1992. Intra-sexual competition and canine dimorphism in anthropoid primates. American Journal of Physical Anthropology 87:461– 477.

Plavcan, J. M. and van Schaik, C. P. 1997. Intrasexual competition and body weight dimorphism in anthropoid primates. American Journal of Physical Anthropology 103:37– 68.

Singleton, M. 2002. Patterns of cranial shape variation in the Papionini (Primates: Cercopithecinae). Journal of Human Evolution 42:547-578.

Smith R.J. 1984. Comparative Functional Morphology of Maximum Mandibular Opening (Gape) in Primates in Chivers et al (eds) Food Acquisition and Processing in Primates, Springer, Boston, Massachusetts.

Thorington, R. W. and Groves, C. P. 1970, An annotated classiﬁcation of the cercopithecoidea, in: Napier, J. R., and Napier, P. H., eds., Old World Monkeys: Evolution, Systematics and Behavior, Academic Press, New York.

Ungar, P. S. 1994. Patterns of ingestive behavior and anterior tooth use differences in sympatric anthropoid primates. American Journal of Physical Anthropology 95:197-219.

Vineyard, C. J., Wall, C. E., Williams, S. H., and Hylander, W. L. 2003. Comparative functional analysis of skull morphology of tree-gouging primates. American Journal of Physical Anthropology 120:153-170.

Wickings, E. J. and Dixson, A. F. 1992. Development from birth to sexual maturity in a semi-free-ranging colony of mandrills (Mandrillus sphinx) in Gabon. Reproduction, 95:129-138.