The Recording and Analysis of a Vocal Repertoire for the Red Ruffed Lemur, Varecia rubra

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The Recording and Analysis of a Vocal Repertoire for the Red Ruffed Lemur, Varecia rubra BY DAPHNE HUDSON A Thesis Submitted to the Division of Social Sciences New College of Florida in partial fulfillment for the requirements for the degree Bachelor of Arts in Anthropology Under the sponsorship of Anthony Andrews Sarasota, Florida April, 2013

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ii Dedication I dedicate this work to the people, foundations, and societies who devote themselves to the conservation of all non human primates, in particular, to the Lemur Conservation Foundation. The environmental, financial, and legislative difficulties that face conservation programs seem incredible, and I am in awe of the commitment the staff and researchers have to these amazing ani mals.

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iii Acknowledgements I am deeply grateful for the advice and encouragement of my academic adviser and thesis sponsor, Dr. Anthony Andrew s. Y our patience and guidance has helped me along this final year of my undergraduate education more than I can say. Thank you to Dr. Sandra Gilchrist for your input in this thesis and your emphasis on ethics in your classes. You have opened my eyes to many things I once took for granted. I am immeasurably grateful to Dr. Uzi Baram and Dr. Natalie Vasey ; more than professors, they are mentors, and there are no words to express my gra titude. Thank you to Professor Duff Cooper for your generosity, time, expertise, and jokes that helped make this thesis possible. I am in great debt to the Lemur Conservation Foun dation, its director Pattie Walsh, and especially intern Cait Flannigan for their tolerance, helpfulness, and enthusiasm for the work of an undergradua te student. I am very grateful for the generous contributions of the New College Student Research and Tr avel Grant and the student run CAA that made this project possible. Thank you to Dr. Erik Patel who selflessly loaned out his recording equipment to LCF for our use and walked me through its use. My family is my rock, my inspiration, and my drive. I hop e I have made you proud. Finally, I would be remiss if I did not mention my friends. You have been the silver lining to these gray clouds, and sometimes my only motivation to get out of bed Thank you.

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iv TABLE OF CONTENTS P age DEDICATION ii ACKNOWLEDGEMENTS iii TABLE OF CONTENTS iv LIST OF FIGURES v i LIST OF TABLES vii i LIST OF SPECTOGRAMS ix ABSTRACT x CHAPTER I: BEHAVIORAL VOCAL REPERTOIRES AND RED RUFFED LEMURS 1 CHAPTER II: LEMUR VOCALIZATIONS 14 CHAPTER III: METHODS 30 CHAPTER IV: RESULTS 46 CHAPTER V: DISCUSSION 82 CHAPTER VI: CONCLUSION 97 APPENDIX I: RAW DATA IN DATA EXCEL SHEET WITH KEY 102 APPENDIX II : SPECTRO G RAMS OF CLASSIFIABLE CALLS 103 APPENDIX III: SP E CTROGRAMS OF THREE GROWLS 108 APPENDIX IV: SAS TABLES FOR PRE DURING, A ND POST CALL ACTIVITIES 110 APPENDIX V : SAS TABLES FOR THE PRE CALL

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v ACTIVITY FREQUENCIES 111 APPENDIX VI: SAS TABLES FOR THE DURING CALL ACTIVITY FRE QUENCIES 11 5 APPENDIX VII : SAS TABLES FOR THE POST CALL ACTIVITY FREQUENCIES 1 19 APPENDIX VIII : SAS RESULTS OF THE CHI SQUARED ANALYSIS OF PRE AND POST CALL ACTIVITY FREQUENCY 123 APPENDIX IX : SAS TABLES FOR THE FREQUENCIES OF THE ACTIVITIES OF NEAREST NEIGHBORS 131 APPENDIX X : SAS TABLES FOR THE FREQUENCIES OF THE DISTANCES OF CALL INTIATORS FROM NEAREST NEIGHBORS 134 APPENDIX XI : SAS TABLES FOR THE FREQUENCIES OF VOCALIZATIONS BY TIME OF DAY 140 APPENDIX XII : SAS TABLES FOR THE FREQUENCIES OF THE ACTIVITIES OF THE THIRD INDIVIDUAL 142 APPENDIX XIII : SAS TABLES FOR THE FREQUENCIES OF THE ACTIVITIES OF GROUP BEHAVIOR 144 BIBLIOGRAPHY 148

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vi List of Figures Figure 1. Map of Madagascar relative to Africa ................................ ......................... 6 Figure 2. Light Orange Red Ruffed Lemur ................................ ................................ 9 Figure 3. Map of Madagascar ................................ ................................ .................. 12 Figure 4. Map of the Lemur Conservation Foundation. Image from LCF. ................. 32 Figure 5. Hurricane Dome. Ph oto from LCF website. ................................ ............... 33 Figure 6. Pre Call Activities for the Chatter ................................ .............................. 51 Figure 7. Pre Call Activities for the Growl ................................ ............................... 52 Figure 8. Pre Call Activities for the Growl Snort ................................ ...................... 53 Figure 9. Pre Call Activities for the Grunt ................................ ................................ 54 Figure 10. Pre Call Activities for the Mew ................................ ............................... 55 Figure 11. Pre Call Activities for the Pulsed Squawk ................................ ............... 56 Figure 12. Pre Call Activities for the Roar Shriek Chorus ................................ ........ 57 Figure 13. Pre Call Activities for the Sniff ................................ ............................... 58 Figure 14. Pre Call Activities for the Squeal ................................ ............................. 59 Figure 15. Post Call Activities for the Chatter ................................ ......................... 62 Figure 16. Post Call Activities for the Growl ................................ ........................... 63 Figure 17. Post Call Activities for the Growl S nort ................................ ................. 64 Figure 18. Post Call Activities for the Grunt ................................ ............................ 65 Figure 19. Post Call Activities for the Mew ................................ ............................. 66 Figure 20. Post Call Activities for the Pulsed Squawk ................................ ............. 67 Figure 21. Post Call Activities for the Roar Shriek Chorus ................................ ...... 68

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vii Figure 22. Post Call Activities for the Sniff ................................ ............................. 69 Figure 23. Post Call Activities for the Squeal ................................ .......................... 70 Figure 24. Vocalization Frequencies by Time ................................ ........................... 75 Figure 25. Vocalizations Recorded in the Early Morning (6:00 AM to 8:59 AM) .... 76 Figure 26. Vocalizations Recorded in the Late Morning (9:00 A M to 11:59 AM) .... 77 Figure 27. Vocalizations Recorded in the Afternoon (12:00 PM to 4:00 PM) ........... 78 Figure 28. Vocalizations Recorded in the Evening (5:00 PM to 8:00PM) ................. 79

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viii List of Tables Table 1. Times of Recording Sessions ................................ ................................ ...... 38 Table 2. Classifiable Call Types ................................ ................................ ............... 47 Table 3. Behavioral Vocal Repertoire for the Red Ruffed Lemur ............................. 89

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ix List of Spectrograms Spectrogram 1. Bray ................................ ................................ .............................. 103 Spectrogram 2. Chatter ................................ ................................ .......................... 103 Spectrogram 3. Growl ................................ ................................ ........................... 104 Spectrogram 4. Growl Snort ................................ ................................ .................. 104 Spectrogram 5. Grunt ................................ ................................ ............................ 105 Spectrogram 6. Mew ................................ ................................ ............................. 105 Spectrogram 7. Pulsed Squawk ................................ ................................ .............. 106 Spectrogram 8. Roar Shriek Chorus ................................ ................................ ...... 106 Spectrogram 9. Sniff ................................ ................................ .............................. 107 Spectrogram 10. Squeal ................................ ................................ ......................... 107 Spec trogram 11. Growl 1 ................................ ................................ ....................... 108 Spectrogram 12. Growl 2 ................................ ................................ ....................... 108 Spectrogram 13. Growl 3 ................................ ................................ ....................... 109

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x THE RECORDING AND ANALYSIS OF A BEHAVIORAL VOCAL REPERTOIRE FOR THE RED RUFFED LEMURS, VARECIA RUBRA Daphne Hudson New College of Florida, 2013 ABSTRACT The unusual vocalizations of our non human primate relatives have long fascinated anthropologists and primatologists. To understand what these animals communicate, researchers have recorded an d played back the calls of many species of primate. In the summer of 2012, I embarked on a five week study of five male captive red ruffed lemurs ( Varecia rubra ) in order to create a behavioral vocal repertoire for this species. During this short study, I recorded 977 vocalizations and grouped over 800 of these into ten definitive categories: the bray, chatter, growl, growl snort, grunt, mew, pulsed squawk, roar shriek chorus, sniff, and squeal. A comparison of the contexts of these calls to the contexts of the closely related black and white ruffed lemur ( Varecia variegata ) revealed marked similarities and differences. Though I was able to confidently assign a function or context to most of these calls, I believe the results of this work would benefit from a year long study of these lemurs. _____________________ Anthony Andrews D ivision of Social Sciences

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1 Chapter I: Behavioral Vocal Repertoires and Red Ruffed Lemurs Introduction Our Earth is a noisy place: Animals as large as whales and as small as frogs fill the jungles, forests, savannahs, and seas with their caws chirps, cries, and songs. Human observers have long listened to and wondered about these strange noises. It has been only recently, though, with the invention of audio and visual recorders, that we have had a means to record and study these vocalizations. Ornithologists, marine biologists, and primatologists have begun to study the calls and songs of birds, marine mamma ls, and primates respectively in an attempt to understand what they are communicating and why. Whil e the study of such things may seem superfluous on the surface, each offers something useful to our understanding of our world. Of particular importance is the study of primate vocalizations. As our closest living relatives nonhuman primates represent t o many scholars what early man might have looked and acted like. It is for this reason (among many others) that it is immensely important to protect these animals from extinction. From the point of view of conservation biologists, studying primate vocali zations can directly improve the accuracy of their population estimations which will help policy writers better protect th ese animals (Terry et al. 2005; see Chapter II for more detail). From the point of

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2 view of anthropologist s studying primate vocalizations could help reveal how humans evolved their varied and complex language. While there are those who do not believe we can or should look to our primate relatives to explain the evolution of our language (see Chapter II for m ore detail), the majority of scholars still believe the answer s to our questions lie in our humble past. The first step to understanding with their many distinct calls. This is accomplished through the creation of a behavioral vocal repertoire. Behavioral Vocal Repertoires I define a behavioral vocal repertoire as a list of all of the vocalizations one species of animal can make and a description of the possible meanings or purposes of each call. In this paper, I will discuss the methods I used to create such a repertoire for a population of red ruffed lemurs ( Varecia rubra ). While this will be the first behavioral vocal repertoire created for the red ruffed lemurs, it will not be the first for th e genus Varecia (see Periera et al. 1988 and Morland 1991 ) As early as the 1980 s, primatologists have been studying the vocalizations of the black and white ruffed lemur, Varecia variegata Until very recently, the red ruffed lemurs were taxonomically listed as Varecia variegata rubra which classified them as a subspecies (see Vasey and Tattersall 2002) It is perhaps for this reason that so few scholars have focused on the vocalizations of the red ruffed lemur s; they may have assumed that studying the calls of one closely related species would explain the calls of the others.

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3 Though the primary goal for my field research was simply to create a behavioral repertoire for this species, I feel it is necessary to compare the final vocal repertoire of the red ruffed lemur to that of the black and white ruffed lemur to determine what similarities and what differences these two species share. Any similarities among these repertoires would sugges t t hat the lemurs of the genus Varecia are capable of communicating similar ideas to one another despite their genetic differences Summary of Chapters In the following sections of this first chapter, I introduce the lemurs of Madagascar and the subject of this work, the red ruffed lemurs. In the second chapter, I discuss why it is useful to study primate, specifically prosimian, behavior and vocalizatio ns. I then summarize the findings of previous studies on primate vocalizations and what their findings contributed to the field. I conclude the second chapter by narrowing my focus to review all of the studies and experiments on the vocalizations of the red ruffed lemurs and what they contributed to the general knowledge of the vocalizations for this species. In the third chapter, I describe the goals, history, and facilities of the Lemur Conservation Foundation (LCF) where I conducted my research. Next I introduce the five red ruffed lemurs that I observed, and discuss their personal histories. I then describe the methods I used to record and analyze data and the definition, purpose, and results of an Inter Observer Reliability Test

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4 In Chapter IV, I present the results of my observations. In Chapter V I discuss the results of my study and present a behavioral vocal repertoire for the red ruffed lemurs. I then compare my results to the published behavioral repertoire s for the black and white lemur t o examine the similarities and differences between them. In the conclusion to this work, I review the accomplishments of this thesis, and discuss the limitations to and the future of this project. An Introduction to the Malagasy Lemurs Before the geolog ical history of the island of Madagascar was known, it was assumed that When it was discovered that Madagascar split from the supercontinent Gondwanaland 160 million years ago and assumed its present day position around 90 million years ago (well before the Age of Mammals ; Figure 1 ), the old idea was scrapped (Mittermeier et al. 2006 : 23 25 ). Today, the most likely scenario for the appearance of mammals on the island is the floating landmass hypothesis. This suggests a piece of land broke off from mainland Africa and crossed the Mozambique Channel carrying on it the ancestors of the moder n Malagasy lemurs The most recent chromosomal and molecular evidence suggests that all extant lemurs are descendants of one founding population. These data imply that, until humans, there was only one migration of primates to the island (2006 : 25 ).

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5 Today, there are over 70 species of lemurs alive on Madagascar (11% of the human primates) Sinc e humans arrived on the island around 2,000 years ago, around 16 species of lemurs went extinct (2006 : 26 ). Of the Lemuriformes 13 species IUCN (International Union for Conservation of Nature) Red List (IUCN 2012).

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6 Figure 1 Map of Madagascar relative to Africa

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7 The greatest Native Malagasy clear large areas of the forest to make room for their rice paddies, cash crops, and cow pastures. Fuel wood consumption and illegal logging have also taken their toll on the environment. An estimated 90% of the original forest of Madagas car has been lost to these practices ( Mittermeier et al. 2006: 59). The second greatest threat to the lemurs is hunting (2006 : 67 ). Primatologists believe the large, slow moving lemurs of Madagascar were hunted to extinction shortly after humans arrived on the island. To this day, natives illegally hunt certain species of lemurs for their taste or prestige. The black and white ruffed lemur, for example, is considered delicious, and the hair on its neck is used to make a tea that relieve s stubborn cough s (2006: 67). In addition to government laws, strong taboos (locally known as fady ) prohibit the consumption of certain lemurs for various fady diminishes, and people have begun to hunt any and all types of lemurs (2006: 69). An Introduction to Varecia rubra The infra order Lemuriformes is divided into five families: Daubentoniidae, Cheirogaleidae, Indridae, Lepilemuridae, and Lemuridae (2006) The first three of these familie s are nocturnal. T he Lemuridae is made up of the genera Eulemur Hapalemur Lemur Prolemur and Varecia (2006 ) The red ruffed lemurs, as stated above, belong to the genus Varecia and are believed to have been one of the earliest branches of Lemuridae ( Vasey 2003: 1333 )

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8 length of 100 to 120 cm (39 to 46 inches) and a weight averaging 3.3 to 3.6 kg (seven to e ight pounds) ( 2006: 321). The only lemurs larger than the ruffed le murs are certain species of indri (genus Indri ) and sifaka (genus Propithecus ) (personal interview with N. Vasey, March 28 2013) The torsos and limbs of the red ruffed lemurs can be any color from a deep red to a light orange. The u nderside of their torso and limbs their tail, and their face is black. Most have a white patch on the nape of their neck and red tufts around their face ( Figure 2). Variations of color and patterns are common occurrences for this species.

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9 Figure 2 Light Orange Red Ruffed L emur

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10 They are found today in the Masoala Peninsula in the North East corner of Madagascar ( Figure 3). Though they are separated by the Antainambalana R iver from the black and white ruffed lemur, hybrids have been observed in both captive and wild fruit makes up anywhere between 75% and 90% of their diet while flowers and leaves make up the remainder of their intake (Mittermeier et al. 2006 : 322 ). The red ruffed lemurs are described as a fission fusion 1 community. Groups are multi female and multi male with around five or six individuals in each (2006: 322). These groups have and defend home ranges around 20 to 30 hectares (2006: 322). Within these home ranges are core groups where one or two individuals spend most of their time. Ma les spend little time outside their core group, while females will socialize and forage for food. In the colder months during gestation, females will restrict their ranges to preserve energy for their costly gestatio ns (Vasey 1997: 83). The red ruffed lemurs have the shortest gestation period of any lemur on the island which lasts 99 to 106 days (1997: 7). They give birth in the dry and warm month of November to a maximum of five young. Unlike many other species o f lemurs, the red ruffed lemurs do not carry their young around with them; instead, they stash their young usually in abandoned, hollow trees (1997: 8). All lemurs in the group care for young infants, regardless of sex (1997: 8). The infants live for th e first 1 A fission fusion community is one where group members travel or act independently for part of the time (fission), then re group later (fusion).

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11 few months off their mother milk which is high in dry matter, protein, and fat. This di et al lows them to grow and become independent of their mothers more quickly (1997: 8).

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12 Figure 3 Map of Madagascar

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13 L emurs can live up to 20 and sometimes 30 years in captivity (persona l interview with N. Vasey, May 1 2013). Life expectancies for wild lemurs are likely lower as they do not have the specialized care and protection from disease, malnourishment, and predation t hat captive lemurs receive. The greatest non human threats to lemurs are snakes, large birds, and mongoose. Animal predation on the large r lemurs is difficult, however, and humans still pose the biggest threat to these animals through deforestation and hun ting practices. The IUCN lists the red ruffed lemur s as an endangered species and the black and white ruffed lemur (that occupies a much larg er part of the island) as critically endangered (2012)

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14 Chapter II: Past Research on Lemur Vocalizations The Importance of Studying Animal Behaviors and Vocalizations Though it is one of s and is relatively close to the African mainland, Madagascar was colonized by humans only a few thousand years ago (Mittermeier et al. 2 006 : 15 ). It is not hard to imagine th os to the unique fauna of Madagascar, and it might have happened on the first day of their arrival. Vocal, but shy and cautious, the Malagasy lemurs likely gave the newcomers a raucous welcome to the island. As with all primates, lemurs have piq ued the interest of many people: some biologists, some anthropologists, and some without a scholarly title. E ach studies primates for different reasons. Primates play an important role in their environmental ecology: they actively pollinate or disperse seeds simply by eating forest flora (Cowlishaw and Dunbar 2000: 2). Conservation biologists, be they botanists or primatologists, know that deforestation, trapping, and poaching does not affect only primates. When they study (and protect) primates, they help ensure the success of other species, both plant and animal, that coexist and sometimes depend on primates living in the same jungle or savannah (2000: 2). Even economists and government officials should have an interest in studying and saving the primates living in their

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15 country; whole industries h ave sprung up around the idea of showcasing primate species in their natural environment to curious travelers ( 2000: 2 ). Primates are recognized by many to be the only living relatives to humankind. As such, evolutionary biologists, anthropologists, and some primatologists study primates to better understand variou s aspects of their ancestors and themselves (e.g. morphology and behavior) Studying how hominids change anatomically over time is the subject of many morphological studies, the most well kno wn being the evolution of biped alism in hominines. The study of behavior in apes, monkeys, and lemurs helps explain what is and is not natural behavior, uniquely human, or a derived and shared trait. Pan troglodytes ) brought to light the aggressive and carnivor ous nature of our close relative, and demonstrated that hierarchical politics and war like tendencies are not unique to humans ( Miller 1995 ). On the opposite end of the spectrum, observations of bonobos ( Pan paniscus ), an ape just as genetically similar to humans as chimpanzees, revealed a lifestyle with few reported instances of violence whose members use sex indiscriminately to relieve social tension (Waal 1998). Past Studies of Lemur Vocalizations and Their Significance Lemurs are particularly useful to scholars interested in the evolution of man. The similarities among modern lemurs, their more primitive extant relatives 2 and the 35 million year old primate fossils discovered in Africa suggests that study ing lemurs 2 These relatives include the lorises (Lorisidae), the galagos (Galagidae), and the tarsiers (Tarsiidae).

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16 could provide invaluable insight into early primate and human evolution (Gamba and Giacoma 2006 : 749 ). If lemurs truly are representative of the earliest primates then studying them will not only help us reveal what our earliest a ncestor looke d and behaved like but may also provide clues on what and how they communicated. Most primatologists believe the human language is an advanced and evolved derivative of primate vocal communications, but how primitive is too primitive? After all, lemurs a re biologi cally engineered with tools ( such as scent glands and large o lfactory receptors in the brain) to communicate via scent the boundaries of their territories or their reproductive readiness. such a creature that is so genetically and anatomically different from humans rely more heavily on olfaction than hearing to communicate? Though this is a fair and worthy observation to make, most people who have heard these vocal lemurs will agree that despit e their use of vocal communication systems (Petter and Charles Dominique 1979). Contrary to the majority opinion, linguist Robbins Burling argues that human language di communication, but from their cognitive abilities (1993). In his article, Burling frequently cites Robert Seyfarth, Dorothy Cheney, and Peter Though he l auds them for discovering that these creatures have distinct calls for specific predators that elicit

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17 different but dependent responses in their fellow monkeys 3 he disagrees with their conclusion that the alarm calls of the vervet monkeys are synonymous t o the words He finds it more logical to compare these human words (Seyfart h et al. 1980; Burling 1993). In his article, Burli ng proposes that humans have two mechanisms to communicate their ideas or in tentions: the verbal pathway and the nonverbal pathway After listing the similarities the human gesture call system shares with the primat call system he concludes that human nonverbal communicative mechanisms are descended from a common ancestor that humans share with nonhuman primates. The similarities between primate verbal communication and human languages, however, are outweighed by their differences. That the vocalizations made by apes, monkeys, and lemurs are not reflexive, are the popular assumption that primate communication is the source of human language (Burling 1993). Burling concluded h is paper by asking whether it i s even evolutionarily possible for two communication systems that are so different to be related. Is it plausible that a primate communication system could have evolved into language while still leaving behind a fine and well functioning but 3 For example, a vervet monkey who has spotted a jaguar will make a specific call. Upon hearing this call, its neighbors will jump into the trees or cl imb higher up into the trees. When a vervet spots a bird of prey and vocalizes, the neighboring monkeys will look up and descend in their trees. This ability is

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18 language emerged as a pro duct of our evolving mind we should expect to find an animal like ourselves, an animal with a mind that had become dependent on language, that in the process of developing language had itself been radically changed (Burling 1993 : 36 ). While B er rightly critiques Seyfarth, Cheney, Marler, and other primatologists studying communication for their failure to include nonverbal ges tures in their studies ( 1993), his final remarks questioning whether evolution can bring about two things that are alik e in some ways yet different in othe rs is a failure to fully grasp the concept and process of evolution. From this statement it is equally apparent that Burling assumed for his argument that the primates that lived millions of years ago vocalized the sam e way as modern nonhuman primates do today. the verbal or nonverbal capabilities of their primate ancestors is the idea that human language did not evolve directly from nonhuman p rimate vocalizations (Arbib et al. 2008). 008 : 1053 ). When ancient : 1054 ). While I believe it is highly unlikely that human language did not evolve from some form of primate communication, it may be possible that human language arose out of a combination of gesture and speech. This idea is fairly recent, and little work

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19 has be en published that includes gestures in the studies of primate communication systems. To date, there are no publications studying gestures as a part of specific calls in several s tudies. The focus was and still is on what can be learned from the verbal component of lemur communications. Such studies were well underway by the first half of the twentieth century. According to anthropologist R.J. Andrews, the majority of these stu dies classified calls into limiting categories that assumed all vocalizations were motivated by sex, fear, or aggression In his study, he listed several situations that he believed would elicit similar vocal responses in primate groups regardless of gene ra. These were: 1. Perceiving a desired object; 2. Encountering a peer in a non hostile environment; 3. Seeking attention, approaching a desired object, or another animal in an attempt to copulate; 4. The loss of contact with another group member or an at tempt to reach a desired object; 5. Being chased; and 6. Thr eatening another animal ( 1962 : 296 ). (such as the roar shriek chorus and growl goal in this article was to critique primatologists who narrow mindedly grouped all calls into categories a n something entirely different. to attempt to treat scent marking or grooming be acceptable to assume the same about vocalizations ? ( 1962 : 313)

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20 ve) was a milestone in the study of nonhuman primate vocalizations because it was the first F ootnote Three ). Their article sparked a movement withi n the field to research whether referential signaling could be found in different species and genera. 1989 study on ring tailed lemurs ( Lemur catta ). From her 13 month observation of free ranging lemurs in Madagasc ar, she concluded that ring tailed lemurs also used referential signaling to distinguish between certain perceived threats. The click, or click series, is a contagious call. When neighboring lemurs heard the call, they responded by moving into the trees or bushes and s canning the ground This vocalization was used indiscriminately for any terrestrial predator or snake. If the terrestrial predator was a fossa ( Cryptoprocta ferox ) dog, or human, the clicking would evolve into a high intensity yap. If a Madagascar harrier hawk ( Polyboroides radiates ) or buzzard ( Buteo brachypterus ) perched too close to the troop, the lemurs would rapidly approach the bird and chirp or moan until it flew away, at which point the lemurs would shriek They were also o bserved shrieking whenever a bird flew too close to them. These vocalizations are quite distinct from those elicited by the Black kite ( Milvus migrans ): When flocks of these birds landed on trees near the ring tailed lemurs, the lemurs would move to the c enter of their trees and remain quiet until the birds flew away (Sauther 1989).

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21 There were several instances of the ring tailed lemurs using alarm calls in a non conformational event. Sauther attributed these to misinterpretations of situations or to an immature lemur that was still learning when to make the appropriate call. Sauther also observed the ring tailed lemurs responding to the alarm calls of nearby sifakas by clicking and mo ving into the trees (1989). While vervet monkeys are believed to be able to communicate the different to describe the proximity of a predator to their group. Due t o lacking detail on many aspects of prosimian antipredator behavior, it was unclear whether the vocal antipredator behaviors of all lemurs were closer to the referential sign aling observed in some primates und squirrels (Macedonia 1990). To test this, Joseph Macedonia observed groups of semi captive ring tailed and black and white ruffed lemurs while antipredator calls were recorded and then played back to those groups. Macedonia found that ring tailed le murs responded to the play back recordings much as they would when a predator was actually around. Deviations from expected patterns were attributed to observer error and immature lemurs. Interestingly, tailed lemurs would first look to easily spot the threat (1990). Though the alarm calls listed for the semi captive ring tailed lemurs in this study were not the sam

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22 conclusion that the alarm calls of the ring tailed lemurs are referential signals (Sauther 1989; Macedonia 1990). The alarm calls of the black and white ruffed lemurs, however, appeared to be a response urgency system for some calls, but a simple reflection of aggression or defensive disposition in others (1990). black and white ruffed lemurs were concluded to be reflective of the re sponse urgency system, the scan the skies for predatory birds. This led Macedonia to conclude that these calls were not representative of either of the systems he was stud ying, but of an aggressive or defensive disposition towards a disturbance (1990). The vocalizations of the genus Varecia are unique from other lemurs in a number of ways and are the focus of this study. It was not until the late 1980s that the first de tailed behavioral vocal repertoire for any species of the genus Varecia was published. This repertoire was conducted on several semi free ranging black and white ruffed lemurs at Duke University. It was part of a larger behavioral ethogram (defined in la ter chapters), and did not discuss the methods used to collect and analyze the data for the behavioral vocal repertoire. The study of the vocal behaviors of these prosimians grouped calls into 13 call type categories : the roa et al. 1988). The roar shriek chorus was described as a spontaneous call that often lacked any obvious stimuli. All group members participated in the chorus ; males shrieked

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23 while females and immature males roared. T his chorus is described as an inter intra group spacing mechanism (Periera et al. 1988 : 10 ), but to this date primatologists still debate the possibility of other functions. The pulsed squawk call was described as an antipredator call for mammalian predators though there were a significant number of occurrences where no discernible stimuli were noted. predators left or were chased out of the area. The abrupt roars were thought to serve as indicators of the presence of raptors (1988 : 12 14 ). Brays and quacks were only heard as parts of the whining vocalizations and the roar shriek chorus. This article suggests that t hese calls function as a part of the were believed to represent a low level disturbance, to alert the group, and to announce Growl snorts were thoug ht to alert the group to a surprising or alarming situation (usually) involving mammalian predators (1988 : 14 ). Males wer e observed whining as an appeasement gesture during the mating season, but this call was also believed to convey frustration. believed to represent extreme aggravation and was usually heard when an avian predator was nearby. The mew was most often heard between mothers and their infants, though an individual occasionally mewed to coordinate with other group members (1988 : 16)

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24 P rimatologists had already been studying the strange vocalizations of the ruffed lemurs b efore Michael Periera, Michelle Seeligson, and Joseph Macedonia published their ethogram The loud calls were a particularly popular subject as they were as complicated as they were unusual. Scholars frequently came to different con clu sions on the functions of the loud call s some even contradicting themselves (see Macedonia 1985 and Turner and Harrenstien 1985, then Periera et al. 1988). In 1985, Mary Elizabeth Turner and Lisa Harrenstien came to the conclusion (roar uh the ruffed lemurs were likely not alarm calls, as they had little in common with the alarm calls of nearby neighbors 4 Instead, they argued that the mob roars and the uh strate many of the characteristics common to the morning calls of the gibbons that serve to direct and coordinate group movement. They also suggested an internal function for these calls, postulating that they may help promote group cohesion during stress ful times (Turner and Harrenstien 1985). Should the former hypothesis prove to be correct, they argued that they would expect a group From their results they concluded that, contrary to Periera, Seeligson, and Macedonia, the mob roar exhibited no sexually based elements, though there was usually an initiator to each mob roar (1985 : 4) uh determined, rallied the group at night and announced their presence to other troops of 4 Turner and H arrenstien drew on Peter M primates living near one another to have similar alarm calls so that the neighboring species can also recognize and survive areal and terrestrial threats. Turner and Harrenstien did not discuss w he ther this is evidence of genetic similarities or primate learning capabilities

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25 lemurs, while the m ob roar was an intra group spacing indicator among wild ruffed lemurs. In captive lemurs, it served more as an alarm call and to indicate stress in bond pairs (1985 : 7 ). In 1991, Hilary Morland presented an exhaustive study of the black and white ruffed lemur that included a behavioral vocal repertoire. She reported 16 call types: the a 383). Morland observed the roar shriek chorus to another f emale (or vice versa) and after a male received female aggres sion. She also observed it punctuate abrupt roars and p ulsed squawks and in response to the roar shriek choruses of other ruffed lemurs She believed the abrupt roar was emitted noted that this call was also given when lemurs spotted a raptor (1991: 382). Pulsed squawks and wails were observed when lemurs were in proximity to non conspecifics, during abrupt roars, and possibly in response to humans (1991: 382). Male lemurs brayed during displays, but estrous females or femal es with infants were also heard braying. Males quacked as a form of display (1991: 382). Females coughed when approached by males during the mating and birthing seasons. Morland believed this was a sign of aggression. y Lemurs growled while they were travelling or when they were annoyed. They growl snorted during travel

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26 and pulsed squawks. The whine was only heard from males during a squeal approach and often led into brays (1991: 383). Grumbles punctuated quacks during the mating season Females chuckled during disputes with other females. Mothers and infants mewed when they were separated, but adults also mewed while travelling Distressed infants squeake d when they wanted or needed their mother to return. Females squealed when greeting conspecifics (1991: 383). Like Pereira, Seeligson, and Macedonia, Morland did not describe how she recorded these vocalizations, or how she determined the meanings of the calls she observed. Currently, the most commonly used explanations for the roar shriek chorus are: 1. As an intragroup spacing function, 2. As an alarm function, 3. As a way to establish or defend territories, and 4. For intergroup coordination (Geissmann and Mutschler 2006). struggle to fit this call with a purpose. To test the plausibility of these four hypotheses, Thomas Geissmann and Thomas Mutschler surveyed the vocalizations of wild indri ( Indri indri ) and black and white ruffed lemurs noting only the time of day at which each loud call occurred They theorized that if the roar shriek chorus was meant to vocally establish the boundaries of their territory, it would occur most often in the morning and at night, similar to the territorial calls of other species. After four days of surveying, they concluded that si nce the roar shriek chorus was not heard exclusively at dusk or dawn

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27 but occurred at many diff erent times during the day, the purpose of the chorus was likely not to establish the boundaries of their territory (2006). As their study was conducted over a f our day period only, their results should not be interpreted as definit iv e. Studies of the Vocalizations of the Red Ruffed Lemurs In one of these few studies on the red ruffed lemur, Joseph Macedonia (1985) examined the audio components to the roar shriek chorus and the pulsed squawk to test whether there are sexual or subspecific elements to each. Here he defined the roar shriek chorus as an aerial predator alarm call or a rejection response. He defined the pulsed squawk as a terrestrial predator ala rm call and a spacing mechanism. He observed a troop of black and white ruffed lemurs, a troop of red ruffed lemurs, and one hybrid ruffed lemur at Duke University. He recorded the calls for each and analyzed the pulse rates, durations, and frequencies for sex. In his results, Macedonia noted that there were no sex specific components to either of the loud calls he examined. He did note that the pulse rate, duration, and frequency ranges between the red and black and white ruffed lemurs were significantly different. The hybrid lemur displayed vocal behaviors that were an intermediate to those of the red ruffed and the black and white ruffed species (Macedonia 1985).

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28 Though his study revealed the vocalizations of the ruffe d lemurs to be significantly different from one another, these differences did not elev ate the red ruffed lemurs from subspecies to separate species status. Macedonia was cautious in his conclusion, stating that these differences could be cause d by idiosy ncrasies of the captive population and might not represent the vocalizations of wild ruffed lemurs (1985). Later work conducted in the early 1990s and 2000s provided evidence that vocal data collected from captive populations are reasonably similar to tho se collected from their wild counterparts (Gamba and Giacoma 2007). While the introduction to this chapter emphasized the importance of studying lemur vocalizations as a way to better understand the evolution of our own communication systems, there is one other important reason to study primate communications that merits particular attention in this review. Conservation biologists now believe that understanding the meanings of each primate vocalization may help them to non invasively asses s the health of an (Terry et al. 2005). Current population health models, such as Population Viability Analysis (PVA) 5 though useful, are biased 6 The predictions for animal extinctions by their models are often inaccurate because there is no reliable way to quantify 5 demographics to predict the survivability of that population under specific circumst ances (Terry et al. 2005). 6 Bias in PVA can occur when scientists attempt to account for the sampling error that can occur researchers catch and tag animals or use playback experiments to gather data. Problems arise when researchers may unknowingly catch and tag only the slow, sick, and old members of a population. During playback sessions, some researchers have noted that some recorded calls elicit responses from only a select few members of the population, and not all members equally (Terry et al. 2005).

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29 seemingly random individual behavior (Terry et al. 2005). Greater understanding of vocalizations) can correct for the bias in PVA and create more accurate population models (2005).

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30 Chapter III: Methods The Lemur Conservation Foundation The research for this study took place at the Lemur (LCF) reserve in Myakka City, Florida. Founded in 1996 as the Lower Primate Conservation Foundation, this non and conservation of the primates of Madagascar through captive bre eding, scientific research, educ 2009: 1). The reserve focuses on preserving the species that are not found in most zoos or captive breeding programs but are highly en dangered (LCF 2009). The reserve is home to six species of lemurs, but is looking to welcome more as it continue s to expand. Th ose six species are c ommon brown lemurs ( Eulemur fulvus ), m ongoose lemurs ( Eulemur mongoz ) r ed ruffed lemurs ( Varecia rubra ), r ing tailed lemurs ( Lemur catta Eulemur sanfordi ), and colla r e d lemurs ( Eulemur collaris ) (LCF 2009). T he reserve houses its lemurs in two separate enclosures. The main enclosure includes a 8.7 acr e forest surrounded by a 13 foot fence (where the top foot of the fence is set on a low voltage setting ) and the Reed and Barbara Toomey Pavilion. The second enclosure includes the Jim Toomey Woods ( a 10.4 acre forest also surrounded by a 13 foot partially electrified fence) and the Marilyn K. North Lemur Lodge (Figure 4) The reserve recen tly built hurricane d omes in both forests to house and protect the

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31 free ranging lemurs (the lemurs in the enclosures) during inclement weather (Figure 5)

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32 Figure 4 Map of the Lemur Conservation Foundation Image from LCF.

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33 Figure 5 Hurricane Dome Photo from LCF website.

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34 It is the goal of the LCF staff to keep the l emurs in the forests as much as possible. In certain cases, however, the staff finds it useful to crate the lemurs and bring them to the Pavi lion or the Lemur Lodge where they can be more closely observed (LCF 2009). The vegetation zones in the Myakka City lemur reserve can be described as a rub (LCF 2009: 1). The main forest is mostly an oak pine mix and a wetland. The Toomey Woods are predominately pines and palmettos. Flooding is much more prevalent in the main enclosure. Here, storm water can ris knees and often brings into the enclosure freshwater fish, turtles, mosquitoes, and (occasionally) alligators. The LCF staff actively works to make the forests as similar to the M adagascar jungles as possible. When first planning the main reserve, staff members planted many fruit trees and bamboo stalks with the hope that these trees would bear fr uit to enviro nment and diet (LCF 2009). Thus far, only the bamboo stalks have been a success The Lemurs In t his experiment I collected data on the five male red ruffed lemurs housed in the main enclosure. There were three ring tailed lemurs (a mother and her infa nt

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35 and juvenile son s ) and four mongoose lemurs (one female, her mate, and two sons) that cohabited the main forest during the time this study took place. These three species of lemurs came into contact with each other most frequently during feeding times and during the evenings. This close contact meant that I sometimes recorded the vocalizations of the other lemur species during the data collection period. The calls between these different species are easily distinguished from one another, and I was abl e to separate these The reserve received its first red ruffed lemurs (two females and two males) in 2002 from the Mackie Grove and San Diego Zoos (LCF 2009). They were Bopp and Hale (female) and Tsard and Tsikey (male) In 2007, Orana (male) was born to Bopp and Tsard, and in 2008, the triplets Rivotra, Masoandro, and Volana (all male), were born to Tsikey and Hale. Of the original four lemurs, only Tsikey survives. All of the four red ruffed lemur s born at LCF surviv e to this day. At the time of this study, LCF was in the middle of quarantining a female red ruffed lemur that will hopefully increase the ruffed lemur count at the reserve. She was not introduced to the red ruffed troop until after the observation period f or this study was over, so I did not collect any data from this lemur. Data Collection Techniques Data collection occurred from June 4 th to July 1 st but yielded onl y 16 d ays worth of recordings totaling 36.5 hours. The data col lection period was interrupted from June 20 th to June 27 th by Tropical Storm Debby that flooded the roads to the

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36 reserve and the main forest. During that time, all of the free ranging lemurs were l ocked into the hurricane domes to wait out the storm. They were released from the domes on the 29 th after the forest was drained and deemed safe. Three data observation sessions took place w hile the lemurs were locked in the domes, though none were recor ded due to concern for the safety of the recording equipment Before I began to collect data, I reviewed two behavioral ethograms. An ethogram is a catalogue that attem pts to list and describe all the actions and behaviors of one species. It is a neces sary undertaking for primatologists before they can conduct any field work and it primatologist witnessed during his or her research. The first ethogram I studied was of the black and white ruffed lemur and included a behavioral vocal repertoire of that species (Periera et al. 1988). I studied th is vocal repertoire to familiarize myself with the commonly used names for the calls of these lemurs (as they have the same name s as the calls of the red ruffed lemur) and paid particular attention to the phonetic descriptions of these calls so I would more easily recognize them in the field. The second ethogram was a purely behavioral ethogram of the population and was cre ated by the staff. Once I was familiar with these two ethograms, I introduced myself and my equipment to the red ruffed troop. By f amiliarizing the lemurs with both me and my equipment before data collection took place I ensured that they would not rea ct poorly to strange people and objects. The LCF staff requires all researchers to study the signs of stress and aggression in the species they are studying. Had a member of the troop

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37 displayed any signs of stress or aggression during the introduction se ssion or the data collection period, I was to remove myself from their presence and notify the staff. On the whole, the troop was not interested in me or my equipment, and they never displayed signs of aggression towards me or the microphone, though they did physically examine the windscreen several times over the course of the study. For this study, I used a Marantz PMD 660 audio recorder with a microphone, microphone gun, and a windscreen. A microphone gun is a mount (shaped like a long barrel gun) on which users rest their microphones This reduces the amount of movement the microphone records as it is carried around. A windscreen is a vinyl or fake fur slip that covers the microphone and reduces the amount of wind and background noise the microphone picks up. I began tra cking the lemurs at sunrise around 6:00 Locating the lemurs could take anywhere from ten to 45 minutes, but most recording sessions began before 7:00 Morning recording sessions ran from 6:00 to 10:00 or 11 :00 For the first half of the observation period, I recorded the lemurs during the afternoon from 1:00 to 3:00 or 4:00 For the second half, I recorded the lemurs in the early evenings from 6:00 to 8:00 when it began to get dark (Table 1) By recording the lemurs in both the afternoon and evening I hoped to get a wider and more accurate variety of calls and call functions.

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38 Table 1 Times of Recording Sessions Morning 6:00 AM to 11:00 AM Afternoon 1:00 PM to 4:00 PM Evening 6:00 PM to 8:00 PM

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39 For the first several days, I focused the microphone on one member of the troop, alternating between them after every 30 minute recording interval ended. I watched the lemurs continuously during all intervals. When they vocalized, I reco rded the time, the type of call, the name of the vocalizer 7 the vocalizer s behavior before, during, and after he vocalized, the distance from the voc alizer to his nearest neighbor, the be havior of his nearest neighbor, the behavior of a third individual (when applicable), and the behavior of the group (when applicable). Though I focused the microphone on one animal, I noted the behaviors of the other vocalizing lemurs so no data would be lost. When I discovered that the quality of the recording was not positively or negatively affected by focusing the microphone on any one animal in particular I decided to change from a focal/all inclusive animal sampling technique to just an all inclus ive animal sampling technique, and trained the microphone on the group as a whole. It was my intention from the b eginning of the study to familiarize an LCF intern with my recording techniques and with the behaviors and vocalizations of the red ruffed le murs so he or she could record an for the first week of my data collection period By combining our data, I could perform an inter observer reliability test which would determine whether we were recording the same behaviors fo r all the calls. While the LCF staff and interns were willing to accommodate my research needs, I was only able to record a few sessions with an 7 The information I hoped to obtain from this repertoire was mostly functional. That is to say, I was primarily concerned with what each call meant. For this reason, I was not interested in which lemur made which call. I collected information on caller identity when it was possible and when it did not distract me from recording what my subjects were doing at the time of their vocalizations.

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40 intern later on in the study period. The results of the inter observer reliability tests are discussed at the end of this chapter Data Analysis Procedures After the five week recording session, I transcribed t he recorded data into a Microsoft Word file. This allowed me to easily view and edit all of the data. I then designe d an E xcel spreadsheet to convert my transcribed data from full sentences to abbreviated codes. The final E xcel spreadsheet is included in this thesis as Appendix One. of the spreadsheet were included for vocalizations that were emi tted rapidly one after the other and might be includes to the calls that did not sound like any of the known calls above. These include the queal/Cha Inaudible and Unknown vocal izations. I recorded three calls that I believed were brays, but because they occurred only during other calls, I did not include them in th e

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4 1 ActivityDuringCall refer to the ethogram categories that were used in the field to record behaviors. In this spreadsheet, they are abbreviated into a code that can be read on the tab labeled I will briefly describe the meanings behind each of the categories here. walking, or climbing. weight on the lower half of his body and remained motionless. not in motion. He may be sitting, hanging, or lying down while he is resting. intentionally produced a sound from his throat or nose (using the nose and hands to move through foliage in search of food). involved a lemur lapping up a li quid with its tongue and swallowing. behavior involved a lemur chasing, swatting at, lunging at, or biting another animal in a non playful manner. troop. Mounting is when a lemur approaches another and wraps his arms around the refers to a lemur that has been mounted. by himself. Self play lemur animal or ( LCF Master Ethogram 2011 are chasing, cuffing, wrestling, or biting one another without the intention of

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42 agonizing or harming each other (LCF Master Ethogram 2011 ). defined as a lemur cleaning himself with his tongue. Where refers to two or more lemurs grooming each other, occurs when only one lemur grooms another. lemur that was approached by another. not change. fit any of the above. sight of the researcher, but was not observed at the time it vocalized. The variables they did not provide any useful information. columns apply on ly to calls where a third individual or all members of the gro up participated in, mainly the roar shriek chorus and the pulsed s quawk. Finally, the included the information that could not be coded bu t might still be context ually relevant. Once added to E xcel, this information wa s transferred to SAS ( Statistical Analysis System) to be statistically analyzed. Using SAS, I divided all of the data points into their call type. I then asked SAS to find the frequencies that each pre

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43 during, and post call activity occurred. I divided the time (from 6:00 AM 9:00 AM to 11:59 AM), 4:00 5:00 to 8:00 PM) and had SAS count the number of times each call occurred during those specific times of day. I analyze d the distance from his nearest neighbor for each call, the activity of the nearest neighbor, and the activity of the 3 rd individual and group (if applicable). Audacity is a free audio editing software that allows its users to play back and edit a sound file (Audacity 2000 ). I used Audacity to isolate samples of all of the known and unclassifiable calls and copy and paste them into new sou nd files. Praat is a free software program that is used to analyze and reconstru ct acoustic speech signals ( Lieshout 2003). Though the freeware was intended for use in human acoustic analysis, it can be applied to the analysis of prima te acoustics with no problems, and is frequently used by primatologists (Gamba and Giacoma 2007). Once I had separated the vocalizations from the recor dings, I entered them into Praat and created waveforms and spectrograms for each call type These spect rograms may be viewed in Appendix II. I believed that by comparing the spectrograms of the unclassifiable calls to those of the known calls, I could sort at least some of the unclassifiable calls into known categories. As can be seen in Appendix II I howe ver, there were variations in the spectrograms and the waveforms of some known type of calls. This lack of symmetry in even the known calls would render any comparisons between any one

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44 known call and any unclassifiable calls useless. Until I am better ab le to analyze spectrograms I will focus only on the call types I am sure exist. Inter Observer Reliability Tests The purpose of performing an int er observer reliability test is to ensure that a researcher is recording data in an unbiased manner. The inter observer reliability test for this specific study was meant to ensure that I was both correctly classifying all of I planned on having a second observer join me in the field for one h our a day during the first week of data collection. After every recording session I planned on sitting down with the second observer and comparing our field notes to see how closely they matched. Ideally, our notes would have match ed perfectly. Matching notes indicates either both researchers have the same biases or both researchers are recording the same things. It was important to me that the inter observer reliability test take place during my first week in the field, as it would have allowed me to c atch any mistakes early on. Due to unforeseen complications, LCF could not spare an intern to help me perform this test until the second week of the study. This observer was supplied with all the necessary materials to familiarize herself with the call t ypes and phonetic descriptions of the call type several weeks prior to data collection. She initially recorded her da ta on a Nagra recorder using a S ennheiser microphone, but switched to a field notebook due to equipment concerns.

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45 ealth we were only able to record three hours of data together. We s imilarly identified 41 of the 97 calls recorded during this period (42.27%), but our contextual information matched only 28.87% of the time. I believe these discrepancies are due to dif ferences in experience. At that point in the study, I already had several weeks of experience that helped me hear and identify vocalizations. I also believe our relative positions to one another and to the lemurs led us to collect different data. Becaus e of these differences in experience and our relative locations, I do not believe these results can be accurate indicators of potential bias in this study.

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46 Chapter IV: Results Over the 16 day observation period, I recorded 977 total vocalizations. Unfortunately, not all of these vocalizations could be easily identified as belonging to a pre existing call type (as seen in Periera et al. 1988 or Morland 1991). The ncl assifiabl eC alysis, but can be seen in the E xcel spreadsheet and are listed in Chapter III. The 898 calls that I could identify were classified as chatters, growls, growl snorts, grunts, mews (or moos), pulsed squawks, roar shriek ch oruses, s niffs, or squeals. Of these 898 three are brays, 56 are chatter s, 448 are growls, 66 are growl snorts, 11 are grunts, 132 are mews, 19 are pulsed squawks, 28 are roar shriek choruses, 33 are sniffs, and 102 are squeals (Table 2) In the followi ng sections, I examine the activities (the actions of the lemurs) before and after they (or their nearest neighbors) vocalized, the distance of the vocalizing lemur from his nearest neighbor, the time(s) of day the call was heard and the activities of a t hird individual or a group during or after the call was made. A brief definition of what all of the activities are was given in Chapter III. The reader will note the number of calls I examine in the following sections does not equal the total number of ca lls overall. There were instances in the data collection period where a behavior occurred out of my line of sight or happened too Reco II, these results were removed from the data analysis as they would not explain the purpose of this call.

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47 Table 2 Classifiable Call Types Call Type Number of Occurrences Bray Three Chatter 56 Growl 448 Growl snort 66 Grunt 11 Mew 132 Pulsed Squawk 19 Roar Shriek Chorus 28 Sniff 33 Squeal 102

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48 Call Activities their behavior before, during, and after they vocalized. Using SAS, I grouped the pre during, and post strategy led to a long list of different variables; very few calls exhibited any similarit ies that occurred frequently enough for me to determine the fun ction of that call (Appendix IV ). The only activity that did reliably repeat in the data was the activity during the ocalize; this does not reveal much about the meaning of a call ( Appendix V ). I then decided to examine only the activities that occurred before and after the call was made ( Appendices IV and VI ). Pre Call Activities Of the 56 chatters I recorded, only 46 were useable. There were 11 activity types recorded while a lemur chattered. The most frequently occurring pre call and chattered 16 times out of the total 46 (34.78%). The second most frequent was third most commonly occurring pre call activity, making up 15.22% (seven out of 46)

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49 of the activities. All other pre call activities each made up less than ten percent of the data. Most of them made up less than five percent of the activities ( Figure 6 ). Of the 448 growls I recorded, only 347 were usable. Growls were most commonly given during t ravelling an d were the most frequently occurring pre call activity, making up 88.47% of the data (307 out of 347). The rest of the seven pre call activities each made up less than five p ercent of the data ( Figure 7 ). The total number of growl snorts observed was 66 but only 37 were usable. There were five categories of activities observed when lemurs gave this call, and the most frequently occurring was sitting (56.76%), followed by resting (24.32%), and then t ravelling (13.51%; Figure 8 ). Of the 11 grunts recor ded, ten were usable. There were four types of activities made up 60% of the data ( Figure 9 ). Of the 132 mews, only 23 were usable. Of the six types of activities observed for this call, sitting occurred 60.87% of the time. The second most commonly occurring activity was resting which made up 17.34% of the activities ( Figure 10 ). I recorded 19 pulsed squawks total, but could only analyze seven of them for pre call activit y. The initiators of this group call were mostly recorded resting before 28.57% of the data ( Figure 11 ). Of the 28 roar shriek choruses I observed, only 14 were usable. Th e most frequently occurring pre (42.86%); i.e., a lemur was vocalizing before he initiated the chorus. Travelling

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50 (28.57%) and sitting (14.29%) make up the second and third most frequently occurring pre call ac tivity ( Figure 1 2 ). Of the 33 sniffs I observed, only 29 were useable. There were eight types of activities recorded for this vocalization, and the most frequently occurring was activity w 1.03% of the time ( Figure 13 ). Of the 102 squeals observed, 88 were usable. There were 11 activity categories 05% respectively; Figure 14 ). A chi squared test of the pre call activities for the growl, growl snort, and squeal revealed significant differences at the 0.01 level. These results can be further reviewed in Appendix VII.

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51 Figure 6 Pre Call Activities for the Chatter 2.17% 34.79% 23.91% 4.35% 2.17% 2.17% 2.17% 6.52% 2.17% 15.22% 4.35% Chatter Aggressive Approached Lemur Was Approached Feed Mutual Play Was Mounted Other Sitting Self Play Travel Vocalized

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52 Figure 7 Pre Call Activities for the Growl 0.29% 0.86% 0.29% 0.29% 3.75% 1.73% 4.32% 88.47% Activity before a Growl Aggressive Approached Lemur Feed Mutual Play Other Rest Sitting Travel

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53 Figure 8 Pre Call Activities for the Growl Snort 2.70% 2.70% 24.32% 56.77% 13.51% Activity before a Growl Snort Mutual Grooming Other Rest Sitting Travel

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54 Figure 9 Pre Call Activities for the Grunt 60.00% 10.00% 10.00% 20.00% Activity before a Grunt Approached Lemur Mutual Grooming Travel Vocalize

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55 Figure 10 Pre Call Activities for the Mew 4.35% 4.35% 17.39% 60.86% 8.70% 4.35% Activity before a Mew Feed Other Rest Sitting Travel Vocalize

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56 Figure 11 Pre Call Activities for the Pulsed Squawk 14.29% 28.57% 42.86% 14.29% Activity before a Pulsed Squawk No Change Other Rest Vocalize

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57 Figure 12 Pre Call Activities for the Roar Shriek Chorus 7.14% 7.14% 14.29% 28.57% 42.86% Activity before a Roar Shriek Chorus Approached Lemur Other Sitting Travel Vocalize

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58 Figure 13 Pre Call Activities for the Sniff 3.45% 31.03% 6.90% 3.45% 3.45% 3.45% 6.90% 41.38% Activity before a Sniff Allo Grooming Approached Lemur Was Approached Mutual Play Sitting Self Grooming Travel Vocalize

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59 Figure 14 Pre Call Activities for the Squeal 2.27% 48.86% 17.05% 4.55% 1.14% 7.95% 2.27% 1.14% 9.09% 5.68% Activity before a Squeal Aggressive Approached Lemur Was Approached Mounted Mutual Play Was Mounted Other Rest Travel Vocalize

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60 Post Call Activity There were 39 chatters that could be used in this post call activity analysis. Of the ten activity types, lemurs were most often observed travelling (33.33%) or vocalizing (20.51%) after chattering. They were only occasionally observed sitting after they gave this voca lization (12.82%; Figure 15 ). Of the 448 gr owls, only 310 were usable for this analysis. The majority of the 11 types of post call activities observed for this vocalization were travelling, which made up 61 .29% of this data ( Figure 16 ). There were 29 growl snorts that could be used in this analy sis. The most common post call activities were sitting (37.93%) and resting (27.59%). There were nine types of activities that were obser ved for this call ( Figure 17 ). Only 30 of the 132 mews could be used in this analysis, and there were six types of activities observed. The most commonly occurring was travelling, which made u p 60% of the data ( Figure 18 ). Only nine grunts could be used in this analysis, and travelling was the most frequently occurring activity type recorded (out of four types), and made up 4 4.44% of the data ( Figure 19 ). There were several commonly occurring post call activities for the roar shriek chorus, though only 11 of the 28 choruses could be used in this analysis. The most Sit twice after the chorus was given (18.18%). The remaining two activity categories occurred less than ten pe rcent of the time ( Figure 20 ). Only three pulsed squawks could be used in this analysis, and the

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61 most commonly occurring post Figure 21 ) Lemurs most often travelled (41.67%) after they sniffed (only 24 out of 33 could be used). They were also observed vocalizing after the call (25%). The other six types of categories each made up less than ten pe rcent of the data ( Figure 22 ). Only 70 of the 102 squeals could be used for this analysis. There were 16 activity categories observed for the call, but lemurs were most often observed travelling after the y vocalized (40%; Figure 23 ). A chi squared analysis of the post call activities revealed only the growl had results that were significantly different at the 0.01 level. These results can be further reviewed in Appendix VII.

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62 Figure 15 Post Call Activities for the Chatter 5.13% 5.13% 2.56% 2.56% 7.69% 7.69% 2.56% 12.82% 33.33% 20.51% Activity after a Chatter Aggressive Feeding Mutual Grooming Mutual Play No Change Other Rest Sitting Travel Vocalize

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63 Figure 16 Post Call Activities for the Growl 0.32% 0.65% 4.52% 0.32% 3.55% 8.39% 1.94% 17.74% 0.32% 61.29% 0.97% Activity after a Growl Aggressive Approached Lemur Feeding Mutual Grooming No Change Other Rest Sitting Self Grooming Travel Vocalize

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64 Figure 17 Post Call Activities for the Growl Snort 3.45% 3.45% 3.45% 3.45% 27.59% 37.93% 3.45% 10.34% 6.90% Activity after a Growl Snort Approached Lemur Feeding Mutual Grooming Other Rest Sitting Self Grooming Travel Vocalize

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65 Figure 18 Post Call Activities for the Grunt 22.22% 11.11% 44.44% 22.22% Activity after a Grunt Feed Mounted Travel Vocalize

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66 Figure 19 Post Call Activities for the Mew 3.33% 3.33% 10.00% 20.00% 60.00% 3.33% Activity after a Mew Approached Lemur No Change Rest Sitting Travel Vocalize

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67 Figure 20 Post Call Activities for the Pulsed Squawk 66.67% 33.33% Activity after a Pulsed Squawk Travel Vocalize

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68 Figure 21 Post Call Activit ies for the Roar Shriek Chorus 9.09% 18.18% 9.09% 18.18% 18.18% 27.27% Activity after a Roar Shriek Chorus Allo Grooming Other Rest Sitting Travel Vocalize

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69 Figure 22 Post Call Activities for the Sniff 4.17% 4.17% 4.17% 4.17% 8.33% 8.33% 41.67% 25.00% Activity after a Sniff Aggressive Allo Grooming No Change Other Rest Sitting Travel Vocalize

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70 Figure 23 Post Call Activities for the Squeal 2.86% 4.29% 1.43% 1.43% 1.43% 2.86% 8.57% 5.71% 1.43% 4.29% 2.86% 1.43% 12.86% 40.00% 8.57% Activity after a Squeal Aggressive Allo Grooming Approached Lemur Allo Play Drink Feed Mounted Mutual Grooming Was Mounted No Change Other Rest Sitting Travel Vocalize

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71 Nearest Neighbor Activity Frequencies I recorded the behaviors of ghbor xcel spreadsheet) at the time of or after the vocalization was made. It was important to collect these data as the actions of a neighbor might be important to the purpose of a call. I was able to use 41 of the 56 chatters, 35 of the 448 growls, 11 of the 66 growl snorts, seven of the 11 grunts, 18 of the 132 mews, nine of the 19 pulsed squawks, 24 of the 28 ro ar shriek choruses, 16 of the 33 sniffs, and 70 of the 102 squeals. The most common behavior a nearest neighbor exhibited during a chatter was travelling (26.83%). The second most common was vocalizing (19.51%) and the third was sitting (14.63%). The mo st common behaviors of a nearest neighbor during a growl were travelling (42.86%) and then vocalizing (20%). During a growl snort, nearest neighbors were most likely observed vocalizing (36.36%) or resting (27.27%). All usable activities recorded for the behaviors of nearest neighbors during the grunt occurred in equal amounts. The most common behaviors a nearest neighbor exhibited during the mew were vocalizing (77.78%) then feeding (11.11%). Nearest neighbors vocalized during all of the useable pulsed squawks. Nearest neighbors mostly vocalized during the roar shriek chorus as well (91.67%). During a sniff, a nearest neighbor was most likely observed vocalizing (37.50%) or travelling (18.75%). The most common behavior recorded for nearest neighbors during a squeal was travelling (32.86%; Appendix VII).

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72 Distance from Nearest Neighbor Frequencies Observer error during data collection only allowed me to analyze 17 of the 56 chatters, 177 growls out of 448, 29 out of 66 growl snorts, five out of 11grunts, 42 mews out of 132, six out of 19 pulsed squawks, 11 of the 28 roar shriek choruses, five out of ten sniffs, and 42 out of 102 squeals. or in contact with another lemur (41.18% each). The majority of usable growls occurred when a lemur was ten feet or less from a nearest ne ighbor (38.63%). Growls were one of the two calls that occurred when a nearest neighbor was greater than 30 feet away. The second was the roar shriek chorus. Growl snorts were mostly observed when a lemur was five feet away from his nearest neighbor (23 .86%). Of the five usable grunts, four of them occurred when a lemur was in contact with another lemur (80%). Most mews occurred ten feet from a nearest neighbor (28.57%). Most pulsed squawks occurred when troop members were body length distance from on e another (66.67%). Roar shriek choruses (11 out of 28) occurred mostly when lemurs were ten feet away from one another (45.45%). Half of the ten useable sniffs occurred when lemurs were in contact with their nearest neighbor. Most of the usable squeals occurred when two lemurs were in con tact with one another (80.95%; Appendix VIII). Time of Day Frequencies The majority of all calls occurred in the early morning, from 6:00 to 8 :59 in the morning. Specifically, 672 of the 977 calls occurred in the ea rly morning, 22 occurred

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73 in the late morning ( 9:00 AM to 11:59 AM), 104 occurred in t he afternoon (from 12:00 to 4:00 PM), and 81 occurred in the evening ( 5:00 PM to 8:00 PM ). Chatters occurred most often in the morning (69.64%) and least often in the lat e morning (1.79%). Chatters occurred equally frequently in the afternoon and evening (14.29%). The majority of growls occurred in the early morning (83.04%). No growls were recorded in the late morning. Growls occurred less frequently in the afternoon ( 5.91%) than in the evening (10.94%). Growl snorts occurred almost equally between the early morning and the afternoon (48.48% and 42.42% respectively). Growl snorts occurred least frequently in the late morning (7.58%), and no growl snorts were observed in the evening. Grunts also occurred mostly frequently in the early morning (63.63%). Mews occurred mostly in the early morning (86.36%). They occurred infrequently in the late morning (2.27%) and the afternoon (1.51%). No mews were observed in the ev ening. Pulsed squawks occurred mostly in the afternoon (68.42%). They were occasionally heard in the early morning (21.05%), and infrequently heard in the late morning (10.53%). No pulsed squawks were heard in the evening. Half of the roar shriek chor uses occurred in the early morning. They occurred somewhat frequently in the late morning (28.57%) and afternoon (14.29%) and infrequently in the evening (7.14%). Sniffs were mostly observed in the early morning (72.72%), but were not heard in the late m orning. They occurred somewhat frequently in the afternoon (18.18%) but infrequently in the evenings (9.09%). Squeals were recorded mostly in the

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74 morning (63.73%), and somewhat frequently in the afternoon (18.63%) and the evening (15.69%). They occurred least frequently in the late morning (1.96%) ( Appendix IX and Figures 24 28 ).

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75 Figure 24 Vocalization Frequencies by Time 74.37% 2.82% 13.18% 9.62% Daily Rythm Early Morning Late Morning Afternoon Evening

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76 Figure 25 Vocalizations Recorded in the Early Morning (6 :00 AM to 8:59 AM) 5.81% 55.44% 4.77% 1.04% 16.99% 0.59% 2.09% 3.58% 9.69% Early Morning Chatter Growl Growl-Snort Grunt Mew Pulsed Squawk Roar-Shriek Sniff Squeal

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77 Figure 26 Vocalizations Recorded in the Late Morning (9 :00 AM to 11:59 AM) 4.55% 22.73% 4.55% 13.64% 9.09% 36.36% 9.09% Late Morning Chatter Growl-Snort Grunt Mew Pulsed Squawk Roar-Shriek Squeal

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78 Figure 27 Vocalizations Recorded in the Afternoon (12:00 PM to 4:00 PM) 7.69% 21.15% 26.92% 1.92% 1.92% 12.50% 3.85% 5.77% 18.27% Afternoon Chatter Growl Growl-Snort Grunt Mew Pulsed Squawk Roar-Shriek Sniff Squeal

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79 Figure 28 Vocalizations Recorded in the Evening (5:00 PM to 8:00PM) 10.13% 62.02% 1.27% 2.53% 3.80% 20.25% Evening Chatter Growl Grunt Roar-Shriek Sniff Squeal

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80 Third Individual and Group Activities Frequencies I attempted to collect data on the actions of any third individuals that I believed were somehow involved in the situation occurring before, during, or after a call. For most of the time, no third individuals participated in the calls. This was recorded as xcel spreadsheet. A third individual was only involved in the activities of a chatter only twice out of the 56 total chatters. Only nine times out of 445 was a third individual involved in the activities of a growling lemur and his nearest neighbor. A third individual was behaviorally involved in only three out of the total 64 gr owl snorts. Of the ten usable grunts, a third individual was only behaviorally involved in one of the call activities. A third individual was observed interacting with a mewing vocalizer and his nearest neighbor in 16 of the 22 usable mews. Travelling m the mew, the pulsed squawk, and the roar shriek did a third lemur involve itself. In pulsed squawks, the third lemur was almost always vocalizing. In roar shriek choruses, third individual s were usually vocalizing (80%; Appendix X). There was no instance where a third individual was seen participating in a sniff. Third individuals were recorded participating in the activities of a squeal six times out of 101. Data for the activity of the group was collected for the calls I suspected to be recorded in the E xcel spreadsheet. Only two group calls were recorded in this observation period. These were the loud calls, the pulsed squawk and the roar shriek. Group members were mostly observed vocalizing during these calls (88% for the roar

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81 shriek and 90% for the pulsed squawk), but several members were sometimes observed sitting or travelling during the ro ar shriek chorus (4% for each; Appendix XI).

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82 Chapter V: Discussion In the following s ections, I discuss the results of this study. These are expressed in detail in the subsequent paragraphs but are also summarized in a short table. I conclude the chapter by comparing my results with those of past studies, and attempt ing to explain the differences between them. Bray As mentioned above, the bray was heard only three times, and was not included in the normal analysis. Lemurs brayed only during the roar shriek chorus. Chatter Based on my results, I conclude that the chatter is most likely a kind of greeting call, as it was most often observed while a lemur was approaching or was being approached by another lemur, and occurred only when lemurs were five or however, may be underestimated. During my data collection, I was very conservative about what I considered an a ct of approaching another l emur. T here were situations incorrect assumption. Therefore, a pre call activity that I described simply as travelling, could very well have been a lemur approaching an other lemur before chattering.

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83 Growl The frequency data for both the pre call and post call activities of the growl clearly demonstrated that this call is somehow linked to travelling. The purpose of the growl could be to inform group members that the vo calizer was travelling or perhaps distance from his nearest neighbor demonstrates that lemurs most often growled when they were no more than twenty feet from a nearest n eighbor. If the purpose of the call sense that most growls were given where group members could still hear them. Growl Snort The data for the growl snort did not provide me with an obvious context for this call. Lemurs were primarily sitting or resting before and after the growl snort was and define. Resting (as defined in Chapter III) requires a lemur remain motionless for a period of at least 30 seconds. Observer error could have led me to classify a pre during, or post resting when he was actually in motion. Nearest neighbors were mostly observed to be a maximum of 15 feet away from the vocalizing lemur and were recorded vocalizing or resting around the time of the call.

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84 The best conclusion that I can draw from this analysis is that it is a small scale inter group spacing mechanism. I say it is a smal l scale spacing mechanism because there were only three instances out of 64 when a third individual was involved in the post call activities of the growl snort. An analysis of the types of vocalizations a neighbor was making in response to this call would verify or reject this hypothesis. For example, if the neighbors were responding with growl snorts, then this call might be a spacing mechanism. It is very possible that I could not see or recognize the stimulus eliciting this call. It is also possible that this vocalization has different meanings and functions. A larger sample size of growl snorts would be useful in assessing what this call could mean. Grunt The majority of grunts were heard after a lemur approached another lemur. The proximity of the vocalizer to his nearest neighbor and the behavior of the nearest neighbor (predominately vocalizing or resting) would suggest that this is also a call given when lemurs approach one another. In eight cases out of nine, a lemur travelled after vocalizi ng. In four of those eight cases, a lemur was clearly displaced by another lemur. As only 11 grunts were recorded during the entire data collection period, this suggestion should not be considered entirely reliable. Mew

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85 Similar to the growl snort, the da ta for the mews did not lead to any obvious function for this call. Vocalizers were mostly observed sitting when they mewed. Nearest neighbors (who were mostly recorded within ten feet from the vocalizer) often vocalized around the time of the mew. From my own observations that I was not able to code into quantifiable data, I believe that the lemurs mewed when they wished to travel to a location with the group. Lemurs would travel a ways, sit down, and mew. When group members began to travel in that le directly after the vocalization) the initial vocalizer would eventually repeat the process of travelling, sitting, and mewing until group members were sufficiently close enough. I was not able to code this informatio n into the spreadsheet due to the time gap that would occur between these activities. That is to say, a lemur would slowly travel along a path, stop, sit, and wait a while before vocalizing. In short, the time that tivity and his vocalizing activity was ofte n too large for me to record it as a travelling activity. This call was heard mostly in the early morning because the majority of all travelling occurred during this time. Pulsed Squawk The data for the pulsed squawk confirm that this is a group call. ( There was only one instance where the group did not participate in a pulsed squawk. ) Though all members of the group participated in this call, I was primarily interested in the actions o f the lemur that initiated this call. In the analysis of the pre and post call activities, I often had very few usable samples. This is because it was often times difficult to

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86 correctly identify the lemur that initiated this group call and to describe w hat he was doing before, during, and after he vocalized. Twelve of the 19 pulsed squawks occurred on the same day in the afternoon. I believe these specific pulsed squawks could have occurred for two r easons: there were ring tailed lemurs and mongoose l emurs ( Eulemur mongoz ) present during these vocalizations, and the call was given to warn the other species to keep their distance; or it was a call given to expr ess annoyance or frustration at being feed around two hours after the usual time. Six of the 19 pulsed squawks occurred on the following day in the morning. There were no other lemurs present and there were no other animals (that I could see) present in their area at that time. To this day, I cannot explain or guess at the impetus for the other pulsed squawks. Roar Shriek Chorus The data for the roar shriek chorus confirms that this is a group call. The chorus was often recorded after a lemur chattered, growl snorted, sniffed, squealed, or travelled (though they could have been vocalizing whil e travelling). The vocalizations given prior to a chorus often rose in intensity until a lemur was roaring or shrieking. These calls were not evenly spread out through the day, but occurred mostly in the morning, contradicting what the past literature l ed me to expect (discussed below). I was only able to get information on distances from nearest neighbors for 11 out of 28 vocalizations. These 11 data suggest that calls occurred when lemurs were ten feet or less from a nearest neighbor. Though this su ggests that the function of the call is not a

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87 group spacing mechanism, I do not believe this function should be stricken from the list with data taken from a sample size as small as this. This leads me to propose that this call is related to the actions o f the lemurs; the majority of these calls occurred in the morning perhaps because that was when the lemurs were most active. The number of choruses decreased as the temperature rose and the lemurs became less mobile. This suggests the call was given when the troop was in a state of high arousal. This data does not allow me to come to any conclusion about what this call specifically communicated to conspecifics. Sniff I suggest that the sniff (which I distinguish from the actual act of sniffing) is gi immediate environment). They we re often heard after a vocalization by either the sniffing lemur or by his nearest neighbor. They we re also heard before and after that lem ur or his nearest neighbor travelled The exact purpose of this vocalization cannot be gathered from this data. Squeal It is interesting to note that the majority of squeals are given by the lemur that is approaching another lemur. This differs from t he results of the chatter, as chatters were heard by lemurs both approaching and being approached by another lemur. It is also interesting to note that, despite a small sample size, the majority of usable squeals

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88 occurred when a lemur was in contact with his neighbor, but continued to travel away from that neighbor after vocalizing. The differences between the two calls (and the descriptions by other scholars) leads me to believe that while both of these are involved in greeting rituals, there is a hierarchical component to one, if not both, of these calls. More data would have to be taken to ascertain whether this is the case.

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89 Table 3 Behavioral Vocal Repertoi re for the Red Ruffed Lemur Call Type Phonetic Description Context or Purpose of the Call Bray Nasal, repeating, and trilling rah ah Heard rarely and only during a roar shriek chorus. Chatter Rapid, high pitched, and ik A greeting call given when approaching or being approached by a conspecific. Growl Given while tr avelling to notify the relay the specific location of the vocalizer Growl Snort Small scale i nter group spacing mechanism? Grunt A greeting call? Mew (or Moo) A summon or request for group movement. Pulsed Squawk Loud, high pitched, rapid, repeating, and waivering uh uh uh An indicator of annoyance or a warning call given in the presence of other lemurs. Roar Shriek ra ra Loud, high a wah wah Given when lemurs were in a state of arousal. Sniff Sniffing sound Given in response to a vocalization or a travelling neighbor. Squeal High pitched squealing A greeting call given when approaching a conspecific.

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90 Comparisons to Past Studies The following subsections compare the behavioral vocal repertoire I created for the red ruffed lemurs to the past work of other primatologists on the black and white ruffed lemurs Though the y are two distinct species, researchers have compared the vocalizations of these ruffed lemurs, perhaps because the calls are so similar (see Maced onia 1985). I believe that any similarities between my results and the results of other primatologists indicate that we have successfully identified and described the purpose of that call type. Any differences among the re sults suggest that one (or all) of us have reached the wrong conclusion about a call, that our species have differ ent functions for a vocalization, or that our populations have different functions for a vocalization. Bray Both Pereira and colleagues and I found the bray to occur during the roar shriek choruses (1988: 10). Hilary Morland described the context of t he bray as one used by males during display, but notes that estrous females and females with infants emit a modified version of this call (1991: 382). She did not mention hearing this during the roar shriek chorus. Chatter Pereira and colleagues

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91 concluded that the chatter was emitted as a submissive gesture when males felt threatened by females (1991: 383). A study b y Mary Elizabeth Turner and Lisa data I collected on the chatters of the red ruffed lemur do not suggest this greeting call is a submissive gesture or a stressed pai r. I do personally believe, however, that this call may be given by members of a specific social hierarchy. To test this, future studies on the red ruffed lemur should include the names and social statuses of the lemurs they are studying and track these animals as they vocalize. Growl Both Morland and Pereira and colleagues have linked the growl to a context of travelling and mild disturbance (1991: 383 and 1988: 10). While I have also determined that the red ruffed lemurs growled as they travelled, I did not see any Growl Snort Each repertoire describes the function(s) of the growl snort differently: I postulate its purpose is inter emitted during travel and punctuates pulsed squawks (1991: 383); Pereira and colleagues found t hat it occurred in an alarming situation to alert the group (1988: 10). If Morland and Pereira and colleagues came to different conclusions about this call, then this indicates that these calls have multiple functions or have changing and

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92 different functi ons between captive and wild species. As my data does not allow me to confidently ascribe any meaning to this call, I am reluctant to state that the description I have listed is definitive. The meaning for this call, therefore, may vary by species and popu lation. Grunt Pereira and colleagues noted that the grunt was rarely heard. When it was, they believed it indicated mild aggravation in their study population (1988: 10). While I also found the grunt to be a relatively rare call, unlike Pereira and col leagues I believe the red ruffed lemurs grunted mostly as they came into close proximity to one another. It is important to reiterate, however, that out of the total 977 calls I recorded, only 11 of these were grunts. Mew Both Morland and Pereira and c olleagues agreed that the mew was exchanged between mothers and infants (1991: 383 and 1988: 10). Pereira and colleagues Both Morland and I concluded that adults mewed w hile travelling, though Morland specifically noted that only males mewed while travelling (1991: 383). As there were no females in my study, I could not observe the red ruffed lemurs to see if this was another trait they shared. To determine whether red ruffed mother and infants mew, data would have to be collected for the rubra during the appropriate season.

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93 Pulsed Squawk I was able to identify over half of the pulsed squawks as being related either to an expression of annoyance or to aggression towar ds non conspecifics. Pereira and colleagues predator call, a call territory (1985: 7). J. Petters and P. Charles Dominiqu e believed the pulsed squawk served as a terrestrial predator alarm call and a spacing mechanism for territorial groups (1979). Roar Shriek Chorus The latest work on the roar shriek chorus of the black and white ruffed lemur (as discussed in Chapter II) summarized the four major propose d functions for the call as 1) A n intragroup spac ing mechanism, 2) An alarm function, 3) A call to establish and defend territories, and 4) T o coordinate within a group (Geissman a nd Mutschler 2006). This publication included the results of a four day study that concluded that only the third proposed function of the call was unlikely (Geissman and Mutschler 2006). Morland observed the chorus occurring in response to the choruses o f other red ruffed lemurs, in response to males approaching females, or as calls punctuating other

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94 vocalizations, the abrupt roars and pulsed squawks (1991: 382). Pereira and colleagues suggested the call was a form of intra and inter group communicatio n (1988: 10). Macedonia believed the call alerted group members to avian predators and served as a startle and female rejection response (1985: 296). Turner and Harrenstein p opulations of ruffed lemurs and an alarm call and indicator of stress in pairs of captive lemurs (1985: 7). The data from my study suggests this call was given when lemurs were in a high state of arousal, as no other stimulus was noted and the number of times this call occurred correlated with the activity level of the lemurs. As my study was conducted on a small, all male group living in a comparatively cramped forest with few predators, I believe the roar shriek chorus might serve as a group spacing me chanism or an alarm call in wild lemurs. Sniff Pereira and colleagues sniff) as a call given when an animal was intensely aggravated or in the presence of an avian predator. I concluded that this vocalization had more to do with a response to a not one and the same as Morland believed Pereira and colleagues 83).

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95 Squeal Turner and Harrenstein believed the squeal indicated stress between two lemurs (1985: 7). Pereira and colleagues believe is the squeal as an indicator of behavioral frustration, or an appeasement gest ure (1988: 10). Morland found that females squealed during a greeting display (1991: 383). I found that red ruffed lemur males also squealed when they approached one another, but found no evidence that this was an appeasement gesture (though I do believe there is some chance that this call is given by members of a particular social level). Missing Vocalizations et al. 1988 and Morland 1991). Bo th Morland and Pereira and colleagues noted that the abrupt roar was commonly given when an avian predator flew by. I did not record any such vocalizations, even though there was at least one instance where a bird flew over the red ruffed lemurs. Pereira and colleagues 10) while Morland observed it being vocalized in the same context as a pulsed squawk. Both Morland and Pereira and colleagues found that a quack was gi ven in similar context during the mating or birth seasons (1991: 383).

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96 Both Morland and I recorded vocal izations Morland believed these chuckles were comparable to Pereira and colleagues described their function as aggressive calls emitted during female disputes (1991: 383).

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97 Chapter VI: Conclusion In this thesis, I defined importance to anthropology and primatology. I reviewed the published work of other primatologists interested in the vocalizations of lemurs, and have detailed the methods I used to create such a rep ertoire for the red ruffed lemur, a beautiful, but endangered creature. The results of my observation period yielded ten categories of calls these lemurs used to communicate with. I compared my repertoire to those of the black and white ruffed lemurs to determine the similarities and differences in the types and functions of calls. As mentioned before, the results of this study should not be taken as the final word on the contexts of these calls. Biases in seasonality, sample size, population, and obse rver error may have affected the outcomes reported here Monetary limitations only allowed me to observe the lemurs for a few weeks of the summ er. As several researchers have noticed, however, some vocalizations can only be heard during specific seasons (Vasey 2003: 1335). A year long study would likely have allowed me to record those vocalizations that are only heard during specific seasons (e.g. the quack), and would have increased the number of unclassifiable calls I recorded. This additional time would have helped me determine which of those unclassifiable calls merit their own call category. This increase in sample size would, I believe, also lead to the realization of multiple contexts f or many calls (see Morland 1991: 382 383 and Vasey 2003: 1335).

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98 While the lack of females and infant red ruffed lemurs has undoubtedly affected my results, I believe observing an all male troop has some advantages. Many observers have noticed calls that a re linked to sex. The most obvious example is of the sexual components of the roar shriek chorus, discussed in the second chapter. Most researchers believe males shriek while females and adolescent males roar. In my study, however, males both roared an d shrieked in most of the choru ses. Hilary Morland wrote in her dissertation that the chuckle, cough, and squeal were typically given by females in aggressive or greeting contexts (1991: 383). The chatter, grumble, and whine were usually given by males. The chatter and whine quacks during the mating season (1991: 383). In my study, males both squealed and chattered. A follow up or year long study of this troop would all ow us to see what effect (if any) the arrival of the female ruffed lemur has had on the vocalizations. If she is fertile, a year long study would (hopefully) witness the birth of a baby red ruffed lemur and the vocalizations that occur between it and its mother and other troop members. Contrary to Joseph Macedonia and Katherin Stanger argument that the function of primate vocalizations will remain the same despite location (1994: 3), I have found there are significant differences between the functions of the calls of the black and white ruffed lemurs living in captivity and the black an d white ruffed lemurs living in the wild. Because of this discrepancy, I believe that any year long

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99 Performing such a study would provide the added benefit of allowing res earchers to compare short range calls to long range calls where range here means the distance the sound s travelled. In my study, the growl, growl snort, mew, and roar shriek chorus were all calls given when lemurs were in close proximity to one another an d had a suspected role in social coordination. Unlike the other calls, the roar shriek chorus is a particularly loud call and has a lar ger range than the other three. My data has led me to conclude that the growl and mew (and perhaps the growl snort) pla y some role in inter group social organization, while past research suggests the roar shriek chorus may have something to do with in tra group social organization. A study of wild red ruffed lemurs could determine whether this trend holds true for lemurs l iving in Madagascar A study of lemurs with more gregarious social structures could test to see whether lemurs that do not live in fission fusion communities have similar calls with long and short range functions. In 2007 Marco Gamba and Christina Giacom a published their qualitative repertoire of the crowned lemur ( Eulemur coronatus ) In it, they describe how they analyzed the spectrograms of the vocalizations of this lemur to determine there were ten, not 12 categories of calls (2007: 339). They advoca te performing quantitative step for subsequent analyses of individual differences, behavioral, morpho physiological, and ecological correlates, geographical variation and evolutionary is is the next step for people working with the vocalizations of the black and white ruffed lemur and should be the next step (once

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100 more data is collected) for the red ruffed lemur. Such analyses mig ht reveal the reper toires for these lemur s are acoustically distinct from what humans can hear and might explain the multiple contexts o f certain calls. As the goal is to understand what lemurs are communicating, I believe experimental playback procedure s would be a useful way to test our current hypotheses for the ca lls with questionable contexts. Playing back recordings of the lemurs own vocalizations and examining their reactions might help clarify the meanings of some calls. Playing back recordings of closely related species may also test whether and how much spe cies can understand the vocalizations of their close relatives. The benefit of repertoires is that they can be added to and changed as people study and learn more; though this study has several shortcomings, there is good reason to continue this work. T here are many assumptions, both explicit and tacit, about how Recently, however, thes e most basic examples are being questioned as evidence of non human primate culture is surfacing. To date, language still remains uniquely human. As an anthropologist, I am driven to ask: where did language come from? From whom did it evolve? The work I have presented in my thesis will not answer these questions, and some of these questions may never be answered. My work does, however, have the potential to explain the evolution of language. With the accumulation of enough

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101 behaviora l vocal repertoires for all non human primates, anthropologists and primatologists may one day be able to see grand patterns that reveal the history of the evolution of the human language If nothing else, this work may help future conservation biologists better assess the t roubling condition of red ruffed lemurs in Madagascar to protect them from deforestation and poaching.

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102 Appendix I Raw Data in Excel Data Sheet with Key See attached DVD.

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10 3 Appendix II Spectrograms of Classifiable Vocalizations Spectrogram 1 Bray Spectrogram 2 Chatter

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104 Spectrogram 3 Growl Spectrogram 4 Growl Snort

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105 Spectrogram 5 Grunt Spectrogram 6 Mew

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106 Spectrogram 7 Pulsed Squawk Spectrogram 8 Roar Shriek Chorus

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107 Spectrogram 9 Sniff Spectrogram 10 Squeal

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108 Appendix III Spectrograms of Three Growls Spectrogram 11 Growl 1 Spectrogram 12 Growl 2

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109 Spectrogram 13 Growl 3

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110 Appendix IV SAS Tables for the Pre During, and Post Call Activity Frequencies See attached DVD.

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111 Appen dix V SAS Tables for the Pre Call Activity Frequencies Chatter PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent --------------------------------------------------------------------------------------------A 1 2.17 1 2.17 AL 16 34.78 17 36.96 AW 11 23.91 28 60.87 F 2 4.35 30 65.22 MP 1 2.17 31 67.39 MR 1 2.17 32 69.57 O 1 2.17 33 71.74 S 3 6.52 36 78.26 SP 1 2.17 37 80.43 T 7 15.22 44 95.65 V 2 4.35 46 100.00 Growl PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent --------------------------------------------------------------------------------------------A 1 0.29 1 0.29 AL 3 0.86 4 1.15 F 1 0.29 5 1.44 MP 1 0.29 6 1.73 O 13 3.75 19 5.48 R 6 1.73 25 7.20 S 15 4.32 40 11.53 T 307 8 8.47 347 100.00

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112 Growl Snort PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------------------------------------G 1 2.70 1 2.70 O 1 2.70 2 5.41 R 9 24.32 11 29.73 S 21 56.76 32 86.49 T 5 13.51 37 100.00 Grunt PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent --------------------------------------------------------------------------------------------AL 6 60.00 6 60.00 MG 1 10.00 7 70.00 T 1 10.00 8 80.00 V 2 20.00 10 100.00 Mew PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent ------------------------------------------------------------F 1 4.35 1 4.35 O 1 4.35 2 8.70 R 4 17.39 6 26.09 S 14 60.87 20 86.96 T 2 8.70 22 95.65 V 1 4.35 23 100.00

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113 Pulsed Squawk PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent --------------------------------------------------------------------------------------------NC 1 14.29 1 14.29 O 2 28.57 3 42.86 R 3 42.86 6 85.71 V 1 14.29 7 100.00 Roar Shriek PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------------------------------------AL 1 7.14 1 7.14 O 1 7.14 2 14.29 S 2 14.29 4 28.57 T 4 28.57 8 57.14 V 6 42.86 14 100.00 Sniff PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------------------------------------AG 1 3.45 1 3.45 AL 9 31.03 10 34.48 AW 2 6.90 12 41.38 MP 1 3.45 13 44.83 S 1 3.45 14 48.28 SG 1 3.45 15 51.72 T 2 6.90 17 58.62 V 12 41.38 29 100.00

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114 Squeal PreCall Cumulative Cumulative Activity Frequency Percent Frequency Percent --------------------------------------------------------------------------------------------A 2 2.27 2 2.27 AK 1 1.14 3 3.41 AL 42 47.73 45 51.14 AW 15 17.05 60 68.18 M 4 4.55 64 72.73 MP 1 1.14 65 73.86 MR 7 7.95 72 81. 82 O 2 2.27 74 84.09 R 1 1.14 75 85.23 T 8 9.09 83 94.32 V 5 5.68 88 100.00

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115 Appendix V I SAS Tables for the During Call Activity Frequencies Chatter Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------M 1 2.04 1 2.04 NC 1 2.04 2 4.08 O 1 2.04 3 6.12 R 1 2.04 4 8.16 V 45 91.84 49 100.00 Growl Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------AL 1 0.28 1 0.28 NC 1 0.28 2 0.56 O 1 0.28 3 0.84 R 2 0.56 5 1.40 S 4 1.12 9 2.53 T 7 1.97 16 4.49 V 340 95.51 356 100.00

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116 Growl Snort Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------G 1 2.63 1 2.63 O 1 2.63 2 5.26 R 4 10.53 6 15.79 S 4 10.53 10 26.32 V 28 7 3.68 38 100.00 Grunt Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------O 1 9.09 1 9.09 T 1 9.09 2 18.18 V 9 81.82 11 100.00 Mew Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------O 1 2.78 1 2.78 R 1 2.78 2 5.56 S 11 30.56 13 36.11 V 23 63.89 36 100.00

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117 Pulsed Squawk Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent ------------------------------------------------------------R 1 14.29 1 14.29 V 6 85.71 7 100.00 Roar Shriek Activity During Cumulative Cumulative Call Frequency Percent F requency Percent -------------------------------------------------------------NC 1 5.26 1 5.26 O 2 10.53 3 15.79 S 2 10.53 5 26.32 V 14 73.68 19 100.00 Sniff Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------O 1 3.45 1 3.45 T 1 3.45 2 6.90 V 27 93.10 29 100.00

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118 Squeal Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------A 1 1.12 1 1.12 AL 2 2.25 3 3.37 M 2 2.25 5 5.62 MR 1 1.12 6 6.74 O 3 3.37 9 10.11 R 1 1.12 10 11.24 T 1 1.12 11 12.36 V 78 87.64 89 100.00

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119 Appendix V I I SAS Tables for the Post Call Activity Frequencies Chatter Post Call Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------A 2 5.13 2 5.13 F 2 5.13 4 10.26 MG 1 2.56 5 12.82 MP 1 2.56 6 15.38 NC 3 7.69 9 23.08 O 3 7.69 12 30.77 R 1 2.56 13 33.33 S 5 12.82 18 46.15 T 13 33.33 31 79.49 V 8 20.51 39 100.00 Growl Post Call Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------A 1 0.32 1 0.32 AL 2 0.65 3 0.97 F 14 4.52 17 5.48 MG 1 0.32 18 5.81 NC 11 3.55 29 9.35 O 26 8.39 55 17.74 R 6 1.94 61 19.68 S 55 17.74 116 37.42 SG 1 0.32 117 37.74 T 190 61.29 307 99.03 V 3 0.97 310 100.00

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120 Growl Snort Post Call Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------AL 1 3.45 1 3.45 F 1 3.45 2 6.90 G 1 3.45 3 10.34 O 1 3.45 4 13.79 R 8 27.59 12 41.38 S 11 37.93 23 79.31 SG 1 3.45 24 82.76 T 3 10.34 27 93.10 V 2 6.90 29 100.00 Grunt Post Call Cumulative Cumulative Activity Frequency Percent Frequency Percent ------------------------------------------------------------F 2 22.22 2 22.22 M 1 11.11 3 33.33 T 4 44.44 7 77.78 V 2 22.22 9 100.00 Mew Post Call Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------AL 1 3.3 3 1 3.33 NC 1 3.33 2 6.67 R 3 10.00 5 16.67 S 6 20.00 11 36.67 T 18 60.00 29 96.67 V 1 3.33 30 100.00

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121 Pulsed Squawk Post Call Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------T 2 66.67 2 66.67 V 1 33.33 3 100.00 Roar Shriek Post Call Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------AG 1 9.09 1 9.09 O 2 18.18 3 27.2 7 R 1 9.09 4 36.36 S 2 18.18 6 54.55 T 2 18.18 8 72.73 V 3 27.27 11 100.00 Sniff Post Call Cumulative Cumulative Activity Frequency Percent Frequency Percent -------------------------------------------------------------A 1 4.17 1 4.17 AG 1 4.17 2 8.33 NC 1 4.17 3 12.50 O 1 4.17 4 16.67 R 2 8.33 6 25.00 S 2 8.33 8 33.33 T 10 41.67 18 75.00 V 6 25.00 24 100.00

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122 Squeal Post Call Cumulative Cumulative Activity Frequen cy Percent Frequency Percent -------------------------------------------------------------A 2 2.86 2 2.86 AG 3 4.29 5 7.14 AL 1 1.43 6 8.57 AP 1 1.43 7 10.00 D 1 1.43 8 11.43 F 2 2.86 10 14.29 M 6 8.57 16 22.86 MG 4 5.71 20 28.57 MR 1 1.43 21 30.00 NC 3 4.29 24 34.29 O 2 2.86 26 37.14 R 1 1.43 27 38.57 S 9 12.86 36 51.43 T 28 40.00 64 91.43 V 6 8.57 70 100.00

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123 Appendix VI I I SAS Results of the Chi Squared Analysis of Pre and Post Call Activity Frequencies Chi Square Analysis of PreCallActivity for Chatter Chi Square Test for Specified Proportions ------------------------Chi Square 61.1304 DF 10 Pr > ChiSq <.0001 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 46 Chi Square Analysis of PreCallActivity for Growl Chi Square Test for Specified Proportions ------------------------Chi Square 1836.0778 DF 7 Pr > ChiSq <.0001 Sample Size = 347 Chi Square Analysis of PreCallActivity for Growl Snort Chi Square Test for Specified Proportions ------------------------Chi Square 37.1892 DF 4 Pr > ChiSq <.0001 Sample Size = 37

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124 Chi Square Analysis of PreCallActivity for Grunt Chi Square Test for Specified Proportions ------------------------Chi Square 6.8000 DF 3 Pr > C hiSq 0.0786 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 10 Chi Square Analysis of PreCallActivity for Mew Chi Square Test for Specified Proportions ------------------------Chi Square 34.1294 DF 5 Pr > ChiSq <.0001 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 23 Chi Square Analysis of PreCallActivity for Roar Shriek Chi Square Test for Specified Proportions ------------------------Chi Square 6.7143 DF 4 Pr > ChiSq 0.1518 WARNING: 100% of the cells have expected counts less

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125 than 5. Chi Square may not be a valid test. Sample Size = 14 Chi Square Analysis of PreCallActivity for Pulsed Squawk Chi Square Test for Specified Proportions ------------------------Chi Square 1.5714 DF 3 Pr > ChiSq 0.6659 WARNING: 100% of the cells have expected coun ts less than 5. Chi Square may not be a valid test. Sample Size = 7 Chi Square Analysis of PreCallActivity for Squeal Chi Square Test for Specified Proportions ------------------------Chi Square 181.2500 DF 10 Pr > ChiSq <.0001 Sample Size = 88 Chi Square Analys is of PreCallActivity for Sniff Chi Square Test for Specified Proportions ------------------------Chi Square 36.3793 DF 7

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126 Pr > ChiSq <.0001 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 29

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127 Chi Square Analys is of Post CallActivity for Chatter Chi Square Test for Specified Proportions ------------------------Chi Square 34.5897 DF 9 Pr > ChiSq <.0001 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 39 Chi Square Analysis of PostCallActivity for Growl Chi Square Test for Specified Proportions ------------------------Chi Square 1115.3871 DF 10 Pr > ChiSq <.0001 Sample Size = 310 Chi Square Analysis of PostCallActivity for G rowl Snort Chi Square Test for Specified Proportions ------------------------Chi Square 34.6102 DF 8 Pr > ChiSq <.0001 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 29

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128 Chi Square Analysis of PostCallActivity for Grunt Chi Square Test for Specified Proportions ------------------------Chi Square 2.1111 DF 3 Pr > ChiSq 0.5497 WAR NING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 9 Chi Square Analysis of PostCallActivity for Mew Chi Square Test for Specified Proportions ------------------------Chi Square 44.4024 DF 5 Pr > ChiSq <.0001 WARNING: 33% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 30 Chi Square Analysis of PostCallActivity for Mew Chi Square Test for Specified Propo rtions ------------------------Chi Square 0.3333 DF 1 Pr > ChiSq 0.5637

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129 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 3 Chi Square Analysis of PostCallActivity for Roar Shriek Chi Square Test for Specified Proportions ------------------------Chi Square 1.5456 DF 5 Pr > ChiSq 0.9077 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 11 Chi Square Analysis of PostCallActivity for Sniff Chi Square Test for Specified Proportions ------------------------Chi Square 25.3333 DF 7 Pr > ChiSq 0.0007 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 24

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130 Chi Square Analysi s of PostCallActivity for Squeal Chi Square Test for Specified Proportions ------------------------Chi Square 141.7328 DF 14 Pr > ChiSq <.0001 WARNING: 100% of the cells have expected counts less than 5. Chi Square may not be a valid test. Sample Size = 70

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131 App endix IX SAS Tables for the Frequencies of the Activities of Nearest Neighbors Chatter Behavior Cumulative Cumulative Of NN Frequency Percent Frequency Percent -------------------------------------------------------------A 1 2.44 1 2.44 AL 2 4.88 3 7.32 F 5 12.20 8 19.51 MG 1 2.44 9 21.95 MP 1 2.44 10 24.39 NC 3 7.32 13 31.71 O 1 2.44 14 34.15 R 2 4.88 16 39.02 S 6 14.63 22 53.66 T 11 26.83 33 80.49 V 8 19.51 41 100.00 Growl Behavior Cumulative Cumulative Of NN Frequency Percent Frequency Percent -------------------------------------------------------------F 2 5.71 2 5.71 M 1 2.86 3 8.57 MG 1 2.86 4 11.43 NA 1 2.86 5 14.29 NC 1 2.86 6 17.14 O 3 8.57 9 25.71 P 1 2.86 10 28.57 R 1 2.86 11 31.43 S 2 5.71 13 37.14 T 15 42.86 28 80.00 V 7 20.00 35 100.00

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132 Growl Snort Behavior Cumulative Cumulativ e Of NN Frequency Percent Frequency Percent -------------------------------------------------------------AG 1 9.09 1 9.09 NA 1 9.09 2 18.18 R 3 27.27 5 45.45 S 1 9.09 6 54.55 T 1 9.09 7 63.64 V 4 36.36 11 100.00 Grunt Behavior Cumulative Cumulative Of NN Frequency Percent Frequency Percent -------------------------------------------------------------AG 1 14.29 1 14.29 F 1 14.29 2 28.57 MG 1 14.29 3 42.86 MR 1 14.29 4 57.14 NC 1 14.29 5 71.43 S 1 14.29 6 85.71 T 1 14.29 7 100.00 Mew Behavior Cumulative Cumulative Of NN Frequency Percent Frequency Percent -------------------------------------------------------------F 2 11.11 2 11.11 S 1 5.56 3 16.67 T 1 5.56 4 22.22 V 14 77.78 1 8 100.00

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133 Pulsed Squawk Behavior Cumulative Cumulative Of NN Frequency Percent Frequency Percent -------------------------------------------------------------V 9 1 00.00 9 100.00 Roar Shriek Behavior Cumulative Cumulative Of NN Frequency Percent Frequency Percent -------------------------------------------------------------O 1 4.17 1 4.17 S 1 4.17 2 8.33 V 22 91.67 24 100.00 Sniff Behavior Cumulative Cumulative Of NN Frequency Percent Frequency Percent -------------------------------------------------------------A 1 6.25 1 6.25 AG 2 12.50 3 18.75 NC 3 18.75 6 37.50 O 1 6.25 7 43.75 T 3 18.75 10 62.50 V 6 37.50 16 100.00

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134 Squeal Behavior Cumulative Cumulative Of NN Frequency Percent Frequency Percent -------------------------------------------------------------A 1 1.43 1 1.43 AG 3 4.29 4 5.71 AL 2 2.86 6 8.57 F 3 4.29 9 12.86 M 5 7.14 14 20.00 MG 4 5.71 18 25.71 MP 1 1.43 19 27.14 MR 5 7.14 24 34.29 NA 1 1.43 25 35.71 NC 7 10.00 32 45.71 R 2 2.86 34 48.57 S 7 10.00 41 58.57 T 23 32.86 64 91.43 V 6 8.57 70 100.00

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135 Appendix X SAS Tables for the Fr equencies of the Distances of Call Initiators from Nearest Neighbors Distance From Nearest Neighbor = 5 Feet Cumulative Cumulative CallType Frequency Percent Frequency Percent --------------------------------------------------------------Chatter 3 4.92 3 4.92 Growl 36 59.02 39 63.93 Growl Snort 9 14.75 48 78.69 Moo 8 13.11 56 91.80 Roar Shriek 2 3.28 58 95.08 Sniff 2 3.28 60 98.36 Squeal 1 1.64 61 100.00 Distance From Nearest Neighbor = 10 Feet Cumulative Cumulative CallType Frequency Percent Frequency Percent --------------------------------------------------------------Growl 68 74.73 68 74.73 Growl Snort 6 6.59 74 81.32 Moo 12 13.19 86 94.51 Roar Shriek 5 5.49 91 100.00

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136 Distance From Nearest Neighbor = 15 Feet Cumulative Cumulative CallType Frequency Percent Frequency Percent --------------------------------------------------------------Growl 15 62.50 15 62.50 Growl Snort 3 12.50 18 75.00 Moo 3 12.50 21 87.50 Roar Shriek 2 8.33 23 95.83 Sniff 1 4.17 24 100.00 Distance From Nearest Neighbor = 20 Feet Cumulative Cumulative CallType Frequency Percent Frequency Percent Growl 32 74.42 32 74.42 Growl Snort 6 13.95 38 88.37 Moo 3 6.98 41 95.35 Pulsed Squawk 2 4.65 43 100.00 Distance From Nearest Neighbor = 25 Feet Cumulative Cumulative CallType Frequency Percent Frequency Percent ------------------------------------------------------------Growl 5 71.43 5 71.43 Growl Snort 1 14.29 6 85.71 Moo 1 14.29 7 100.00 Distance From Nearest Neighbor = 30 Feet Cumulative Cumulative CallType Frequency Percent Frequency Percent --------------------------------------------------------------Growl 7 50.00 7 50.00 Moo 7 50.00 14 100.00

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137 Distance From Nearest Neighbor = Greater Than 30 Feet Cumulative Cumulative CallType Frequency Percent Frequency Percent ------------------------------------------------------------Growl 8 80.00 8 80.00 Roar Shriek 2 20.00 10 100.00 Distance From Nearest Neighbor = Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 7 2 8.00 7 28.00 Growl 1 4.00 8 32.00 Growl Snort 3 12.00 11 44.00 Grunt 1 4.00 12 48.00 Moo 4 16.00 16 64.00 Sniff 2 8.00 18 72.00 Squeal 7 28.00 25 100.00 Distance From Nearest Neighbor = Body Length Cumulative Cumulative CallType Frequency Percent Frequency Percent ------------------------------------------------------------Growl 4 33.33 4 33.33 Moo 4 33.33 8 66.67 Pulsed Squawk 4 33.33 12 100.00

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138 Distance From Nearest Neighbor = In Contact Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 7 13.46 7 13.46 Growl 1 1.92 8 15.38 Growl Snort 1 1.92 9 17.31 Grunt 4 7.69 13 25.00 Sniff 5 9.62 18 34.62 Squeal 34 65.38 52 100.00 Distance From Nearest Neighbor = Not Applicable Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 1 33.33 1 33.33 Roar Shriek 1 33.33 2 66.67 Squeal 1 33.33 3 100.00 Distance From Nearest Neighbor = Not Recorded Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 34 7.56 34 7.56 Growl 200 44.44 234 52.00 Growl Snort 25 5.56 259 57.56 Grunt 6 1.33 265 58.89 Moo 83 18.44 348 77.33 Pulsed Squawk 13 2.89 361 80.22 Roar Shriek 16 3.56 377 83.78 Sniff 21 4.67 398 88.44 Snort 1 0.22 399 88.67 Squeal 51 11.33 450 100.00

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139 Distance From Nearest Neighbor = Out Of Sight Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 4 3.77 4 3.77 Growl 71 66.98 75 70.75 Growl Snort 12 11.32 87 82.08 Moo 7 6.60 94 88.68 Sniff 2 1.89 96 90.57 Snort 2 1.89 98 92.45 Squeal 8 7.55 106 100.00

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140 Appendix X I SAS Tables for the Frequencies of Vocalizations by Time of Day AMPM=1 (Early Morning) Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 39 5.80 39 5.80 Growl 372 55.36 411 61.16 Growl Snort 32 4.76 443 65.92 Grunt 7 1.04 450 66.96 Moo 114 16.96 564 83.93 Pulsed Squawk 4 0.60 568 84.52 Roar Shriek 14 2.08 582 86.61 Sniff 24 3.57 606 90.18 Snort 1 0.15 607 90.33 Squeal 65 9.67 672 100.00 AMPM=2 (Late Morning) Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 1 4.55 1 4.55 Growl Snort 5 22.73 6 27.27 Grunt 1 4.55 7 31.82 Moo 3 13.64 10 45.45 Pulsed Squawk 2 9.09 12 54.55 Roar Shriek 8 36.36 20 90.91 Squeal 2 9.09 22 100.00

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141 AMPM=3 (Afternoon) Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 8 7.69 8 7.69 Growl 22 21.15 30 28.85 Growl Snort 28 26.92 58 55.77 Grunt 2 1.92 60 57.69 Moo 2 1.92 62 59.62 Pulsed Squawk 13 12.50 75 72.12 Roar Shriek 4 3.85 79 75.96 Sniff 6 5.77 85 81.73 Squeal 19 18.27 104 100.00 AMPM=4 (Evening) Cumulative Cumulative CallType Frequency Percent Frequency Percent -------------------------------------------------------------Chatter 8 9.88 8 9.88 Growl 49 60.49 57 70.37 Grunt 1 1.23 58 71.60 Roar Shriek 2 2.47 60 74.07 Sniff 3 3.70 63 77.78 Snort 2 2.47 65 80.25 Squeal 16 19.75 81 100.00

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142 Appendix X I I SAS Tables for the Frequencies of the Activities of the Third Individuals Chatter Behavior Of 3rd Cumulative Cumulative Individual Frequency Percent Frequency Percent ------------------------------------------------------------NA 54 96.43 54 96.43 R 1 1.79 55 98.21 T 1 1.79 56 100.00 Growl Behavior Of 3rd Cumulative Cumulative Individual Frequency Percent Frequency Percent -----------------------------------------------------------A 1 0.22 1 0.22 NA 436 97.98 437 98.20 O 1 0.22 438 98.43 R 1 0.22 439 98.65 S 1 0.22 440 98.88 T 5 1.12 445 100.00 Growl Snort Behavior Of 3rd Cumulative Cumulat ive Individual Frequency Percent Frequency Percent --------------------------------------------------------------NA 61 95.31 61 95.31 T 1 1.56 62 96.88 V 2 3.13 64 100.00

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143 Grunt Behavior Of 3rd Cumulative Cumulative Individual Frequency Percent Frequency Percent ------------------------------------------------------------NA 9 90.00 9 90.00 T 1 10.00 10 100.00 Mew Behavior Of 3rd Cumulative Cumulative Individual Frequency Percent Frequency Percent ------------------------------------------------------------NA 6 27.27 6 27.27 S 1 4.55 7 31.82 T 10 45.45 17 77.27 V 5 22.73 22 100.00 Pulsed Squawk Behavior Of 3rd Cumula tive Cumulative Individual Frequency Percent Frequency Percent ------------------------------------------------------------V 11 100.00 11 100.00

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144 Roar Shriek Behavior Of 3rd Cumulative Cumulative Individual Frequency Perce nt Frequency Percent ------------------------------------------------------------O 3 12.00 3 12.00 S 1 4.00 4 16.00 T 1 4.00 5 20.00 V 20 80.00 25 100.00 Sniff Behavior Of 3rd Cumulative Cumulative Individual Frequency Percent Frequency Percent --------------------------------------------------------------NA 32 100.00 32 100.00 Squeal Behavior Of 3rd Cumulative Cumulative Individual Frequency Percent Frequency Percent ------------------------------------------------------------AL 1 0.99 1 0.99 NA 95 94.06 96 95.05 O 1 0.99 97 96.04 R 1 0.99 98 97.03 T 2 1.98 100 99.01 V 1 0.99 101 100.00

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145 Appendix XI I I SAS Tables for the Frequencies of th e Activities of Group Behavior Chatter Group Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------NA 56 100.00 56 100.00 Growl Group Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent ------------------------------------------------------------NA 443 99.33 443 99.33 T 3 0.67 446 100.00 Growl Snort Group Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------NA 61 95.31 61 95.31 T 1 1.56 62 96.88 V 2 3.13 64 100.00

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146 Grunt Group Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------NA 10 1 00.0 0 10 100.0 Mew Group Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------NA 16 84.21 16 84.21 R 1 5.26 17 89.47 V 2 10.53 19 100.00 Pulsed Squawk Group Activity During Cumulative Cumu lative Call Frequency Percent Frequency Percent -------------------------------------------------------------NA 1 10.00 1 10.00 V 9 90.00 10 100.00

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147 Roar Shriek Group Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------O 1 4.00 1 4.00 S 1 4.00 2 8.00 T 1 4.00 3 12.00 V 22 88.00 25 100.00 Sniff Group Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------NA 32 100.00 32 100.00 Squeal Group Activity During Cumulative Cumulative Call Frequency Percent Frequency Percent -------------------------------------------------------------NA 100 99.01 100 99.01 V 1 0.99 101 100.00

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150 Petter, J.J., and P. Charles Dominique. 1979 Vocal communication in prosimians. In The Study of Prosimian Behavior (G. A. Doyle and R. D. Martin, eds). New York: Academic Press: 247 305. Rigamonti, Marco M. 1993 Home Range and Diet in Red Ruffed Lemurs ( Varecia variegata rubra ) on the Masoala Peninsula, Madagascar. In Lemur Social Systems and their Ecological Basis (P.M. Kappeler and J.U. Ganzhorn, eds.). New York: Plenum Press: 25 39. Sauther Michelle, L. 1989 Antipredator behavior in troops of free ranging Lemur catta at Beza Mahafaly special reserve, Madagascar. International Journal of Primatology 10: 595 606. Seyfarth, Robert M., Dorothy M. Cheney, and Peter Marler. 1980 Monkey Responses to Three Different Alarm Calls: Evidence of Predator Classification and Semantic Communication. Science 210(4471): 801 03. Terrace, H.S. 1 983 Language in Primates: Perspectives and Implications (J. de Luce and H.T. Wilder, eds.) New York: Springer Verlag New York Inc.: 19 40. Turner, Mary E lizabeth and Lisa Harrensti en. 1985 Loud calls of the ruffed lemur, Varecia variegata. Journal of the Elisha Mitchell Scientific Society 101(1): 1 8. van Lieshout, Pascal. 2003 PRAAT Short Tutorial. http://oraldyna micslab.ca/resources/praat tutorial/ Vasey, Natalie 1997 a Community Ecology and Behavior of Varecia variegata rubra and Lemur fulvus albifrons on the Masoala Peninsula, Madagascar. PhD Dissertation, Washington University. 1997b How Many Red Ruffed Lem urs Are Left? International Journal of Primatology 18(2): 207 16. 2003 Varecia Ruffed Lemurs. In The Natural History of Madagascar (S.M. Goodman and J.P. Benstead, eds.) London: The Univ ersity of Chicago Press: 1332 36.

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151 Vasey, Natalie, and Ian Tattersall. 2002 Do Ruffed Lemurs Form a Hybrid Zone? Distribution and Discovery of Varecia with Systematic and Conservation Implications American Museum Novitates 3376: 1 26. Yoder A.D., and Z H. Yang. 2004 Divergence dates for Malagasy lemurs estimate d from multiple gene loci: geological and evolutionary context. Molecular Ecology 13(4): 757 73.