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The Ontogeny of Feeding Behavior of Nicaraguan Mantled Howler Monkeys (Alouatta Palliata)

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The Ontogeny of Feeding Behavior of Nicaraguan Mantled Howler Monkeys (Alouatta Palliata) THE ONTOGENY OF FEEDING BEHAVIOR OF NICARAGUAN MANTLED HOWLER MONKEYS (ALOUATTA PALLIATA) BY MELISSA L. RAGUET-SCHOFIELD DISSERTATION Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in Anthropology in the Graduate College of the University of Illinois at Urbana-Champaign, 2010 Urbana, Illinois Doctoral Committee: Professor Steven Leigh, Chair Professor Paul Garber Assistant Professor Rebecca Stumpf Associate Professor Katherine MacKinnon, St. Louis University ABSTRACT THE ONTOGENY OF FEEDING BEHAVIOR OF NICARAGUAN MANTLED HOWLER MONKEYS (ALOUATTA PALLIATA) Melissa L. Raguet-Schofield, Ph.D. Department of Anthropology University of Illinois at Urbana-Champaign, 2010 Steven Leigh, Advisor This thesis is an investigation of the relationship between diet and life history in Primates. The goal of this research is to evaluate the hypothesis that accelerated growth and maturation schedules of folivorous primates enable these species to rapidly attain the ability to masticate and digest mechanically demanding leaf resources. In order to determine how dietary patterns underlie the evolution of primate life history strategies, I conducted a year-long study on the acquisition of foraging proficiency in juvenile mantled howler monkeys (Alouatta palliata) inhabiting La Isla de Ometepe, Nicaragua (11°40' N, 85°50' W). I predicted that juveniles are less efficient foragers than adults, that juvenile and adult diets differ, that juveniles rely on their mothers’ milk during periods of seasonal food stress, and that juvenile mortality increases when tough resources are an important dietary component. To evaluate these predictions, I followed two groups of mantled howler monkeys— collecting behavioral data on juveniles, adult females, and adult males—and I quantified the toughness of the leaves they consumed. Results indicate that juveniles were less efficient foragers than adults: juveniles spent more time foraging relative to the time they spent feeding, and juveniles devoted a greater proportion of their day to foraging than did adults. Juvenile and adult diets were similar, in terms of gross dietary category and plant species consumed; however, juveniles consumed a diet that was lower in overall toughness than was adults’. Milk served as a “fallback” food for juveniles during the dry season when food availability was limited and ii howlers increasingly relied on tough resources. Nonetheless, juvenile mortality rate increased: half of all juveniles died or disappeared during this time. These results support the initial hypothesis that the accelerated growth rate of folivorous primates is related to dietary toughness. Although juveniles adopted an adult-like diet early in their ontogeny, their inefficient foraging, lower toughness profile, extended reliance on maternal milk, and increased mortality rate during periods of dietary stress indicates that they struggled with the transition to dietary independence. Growing quickly throughout the juvenile period may be a life history strategy that howlers evolved to minimize mortality risks prior to reproduction. Moreover, howlers begin consuming solid food early in their ontogeny while still continuing to nurse, particularly during times of dietary stress. This early intake of solid food reduces mothers’ energetic costs to current offspring and enables them to rapidly shift their energy investment to future offspring. iii ACKNOWLEDGEMENTS Along the way, many people have contributed greatly to my graduate training and the completion of my doctoral degree. Dr. Brian Richmond initially encouraged me to pursue graduate school. Dr. Steven Leigh sparked my interest in diet and ontogeny. He has been an extraordinarily supportive thesis advisor—continually going the extra mile to make me a better researcher—and I am honored to have been his student. Dr. Paul Garber took me as a teaching assistant to Nicaragua, where I saw the monkeys for the first time, and he has been my “cloth mother” throughout graduate school. Drs. Rebecca Stumpf and Katherine MacKinnon are both role models for me. They provided me with encouragement, inspiration, and the expertise upon which I relied while learning to become a primatologist. Drs. Barth Wright and Peter Lucas kindly taught me how to use the toughness tester—without their help, the mechanical properties component of this thesis would not have been possible. Carolina Sternberg and Dr. Martín Kowalewski helped me translate documents necessary to acquire research permits. For the logistical aspect of my fieldwork, the Fondación Ometepe— and in particular Alvaro and Renée Molina—helped me arrange room and board at the fieldsite. The staff at the Hacienda Mérida and the people of Ometepe Island became my family during my year-long stay in Nicaragua. I extend my deepest gratitude towards: Daraysi, Conny, Doña Argentina, Lucila, Alejandra, Reina, Dalila, Doña Dina, and Leda. Simeón Lório worked as my assistant in the forest: he initially helped me locate my study troops, cut trails, and taught me the names of the plants that the monkeys ate. Eduardo José Gonzales reminded me that I have many beautiful things, and he forever changed the way that I saw the world. iv Nancy and Richard Raguet and Barbara and Bruce Schofield were endlessly supportive, encouraging, and patient during the whole process of moving out of the country for a year. Dr. Michelle Lynch inspired me, and Dan Bassett’s enthusiasm about the toughness tester boosted my morale. Rob Raguet-Schofield created and wrote the DataBook Software specifically for this project. He also provided technical, linguistic, and emotional support, and he accompanied me to the field site for the whole year—where he succeeded in winning the admiration of the people of Ometepe for his speed and skill on the bicycle. Without him, this project and this thesis would not exist. Finally, most of all, I wish to thank William Miles Raguet-Schofield for teaching me the truth about maternal investment. v TABLE OF CONTENTS CHAPTER 1: INTRODUCTION………………………………………………………….….1 CHAPTER 2: BACKGROUND…………………………………………………...…………21 CHAPTER 3: METHODOLOGY……………………………………………………………61 CHAPTER 4: ACTIVITY PATTERNS OF MANTLED HOWLER MONKEYS ON LA ISLA DE OMETEPE ……………………………………………………………………….86 CHAPTER 5: DIETARY PATTERNS OF MANTLED HOWLER MONKEYS ON LA ISLA DE OMETEPE………………………………………………………………………..131 CHAPTER 6: TOUGHNESS OF PLANT FOODS CONSUMED BY MANTLED HOWLERS LIVING AT LA ISLA DE OMETEPE………………………………………...170 CHAPTER 7: POPULATION DYNAMICS OF MANTLED HOWLER MONKEYS AT LA ISLA DE OMETEPE……………………………………………………………………192 CHAPTER 8: DISCUSSION…………………………………………………………..……206 CHAPTER 9: DIRECTIONS FOR FUTURE RESEARCH AND CONCLUSIONS............242 REFERENCES………………………………………………………………………………252 ! vi CHAPTER 1: INTRODUCTION 1.1 Introduction This thesis investigates the relationship between diet and the pace of development in primates in order to determine how feeding and foraging patterns underlie the evolution of primate life history strategies. The proximate goal of this research is to evaluate the hypothesis that the accelerated growth rate of folivorous primates (Leigh, 1994) enables these species to rapidly and efficiently meet the masticatory and digestive demands of a leaf-based diet. Although many primate species consume leaves, folivorous primates rely on leaves as a major dietary component, and they typically have dental, anatomical, or behavioral traits that facilitate the acquisition and processing of foliage (Fleagle, 1999; Strier, 2003). For this research, I investigate the ontogeny of feeding behavior in mantled howler monkeys (Alouatta palliata), a New World primate that devotes between 45% to 71% of its annual feeding time to leaves (Glander, 1978; Milton, 1980; Estrada, 1984; Estrada and Coates-Estrada, 1986; Stoner, 1996) and that reaches sexual maturation more rapidly than similarly sized, closely related frugivorous species (Froehlich et al., 1981; Glander, 1980; Martins and Strier, 2004; Milton, 1981; Nishimura, 2003; Strier, 1996). In broader terms, this thesis evaluates two existing models of life history evolution and determines whether either of these theoretical perspectives can accurately explain primate developmental and reproductive strategies. According to the “fast versus slow” model, life history traits are tightly integrated features that proceed along a trajectory that is either uniformly fast or uniformly slow (Charnov and Berrigan, 1993; Harvey and Clutton-Brock, 1985; Harvey et al, 1987; Promislow and Harvey, 1990; Read and Harvey, 1989; Ross, 1988; 1992; 1998; Sacher, 1959; Sacher and Staffeldt, 1974). In contrast, the modular viewpoint of life history ! 1! regards developmental traits as separate, dissociable features that may vary independently of one another (Leigh and Blomquist, 2007; Pereira and Leigh, 2002; Leigh and Bernstein, 2006; Raff, 1996; Williams, 1966a). The ultimate goal of this thesis is to determine whether or not mantled howler life history is consistent with either theoretical framework. In this chapter I discuss life history theory and elaborate on the aforementioned models that attempt to account for the evolution of various life history strategies. I then present the goals of the thesis, describe each of the predictions that the following chapters will address, and provide evidence why I expect these predictions to be met. Finally, I summarize the thesis in a chapter-by-chapter outline. 1.2 Life History Life history refers to the sequence of developmental or reproductive
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